Skip to content
2000
Volume 21, Issue 6
  • ISSN: 1570-1646
  • E-ISSN: 1875-6247

Abstract

The incidence of Hepatocellular carcinoma (HCC) is rising at an alarming rate. It is now the third leading cause of cancer deaths worldwide. Non-alcoholic fatty liver disease (NAFLD) and its more aggressive form of non-alcoholic steatohepatitis (NASH) are emerging as significant risk factors for liver cirrhosis and HCC. Post-translational modifications in proteins especially glycosylation leading to the synthesis of glycoproteins have been implicated in carcinogenesis. Dysregulated glycoproteins and aberrant glycosylation patterns might contribute to the establishment of a protumorogenic environment in NAFLD/NASH patients leading to the establishment of hepatocarcinogenesis. Understanding the molecular mechanisms underlying the changes in glycosylation patterns of certain proteins would help in deciphering the role of glycoproteins in liver cancer and develop novel prognostic and diagnostic markers and therapeutic strategies for the successful treatment of HCC. Herein we discuss some important glycoproteins and altered glycosylation patterns that can be employed as biomarkers for the early detection of HCC in NASH and NAFLD patients.

Loading

Article metrics loading...

/content/journals/cp/10.2174/0115701646341608241025030547
2024-11-06
2025-07-15
Loading full text...

Full text loading...

References

  1. BrayF. LaversanneM. SungH. FerlayJ. SiegelR.L. SoerjomataramI. JemalA. Global cancer statistics 2022: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.CA Cancer J. Clin.202474322926310.3322/caac.2183438572751
    [Google Scholar]
  2. BrarG. GretenT.F. GraubardB.I. McNeelT.S. PetrickJ.L. McGlynnK.A. AltekruseS.F. Hepatocellular carcinoma survival by etiology: A SEER‐medicare database analysis.Hepatol. Commun.20204101541155110.1002/hep4.156433024922
    [Google Scholar]
  3. ReddyK.R. McLerranD. MarshT. ParikhN. RobertsL.R. SchwartzM. NguyenM.H. BefelerA. Page-LesterS. TangR. SrivastavaS. RinaudoJ.A. FengZ. MarreroJ.A. Incidence and risk factors for hepatocellular carcinoma in cirrhosis: The multicenter hepatocellular carcinoma early detection strategy (HEDS) study.Gastroenterology2023165410531063.e610.1053/j.gastro.2023.06.02737429366
    [Google Scholar]
  4. ZhangH. SpencerK. BurleyS.K. ZhengX.F.S. Toward improving androgen receptor-targeted therapies in male-dominant hepatocellular carcinoma.Drug Discov. Today20212661539154610.1016/j.drudis.2021.02.00133561464
    [Google Scholar]
  5. TohM.R. WongE.Y.T. WongS.H. NgA.W.T. LooL.H. ChowP.K.H. NgeowJ. Global epidemiology and genetics of hepatocellular carcinoma.Gastroenterology2023164576678210.1053/j.gastro.2023.01.03336738977
    [Google Scholar]
  6. RiaziK. AzhariH. CharetteJ.H. UnderwoodF.E. KingJ.A. AfsharE.E. SwainM.G. ConglyS.E. KaplanG.G. ShaheenA.A. The prevalence and incidence of NAFLD worldwide: A systematic review and meta-analysis.Lancet Gastroenterol. Hepatol.20227985186110.1016/S2468‑1253(22)00165‑035798021
    [Google Scholar]
  7. HuangD.Q. El-SeragH.B. LoombaR. Global epidemiology of NAFLD-related HCC: Trends, predictions, risk factors and prevention.Nat. Rev. Gastroenterol. Hepatol.202118422323810.1038/s41575‑020‑00381‑633349658
    [Google Scholar]
  8. BansalS. VachherM. AroraT. KumarB. BurmanA. Visceral fat: A key mediator of NAFLD development and progression.Human Nutrition & Metabolism20233320021010.1016/j.hnm.2023.200210
    [Google Scholar]
  9. TanD.J.H. NgC.H. LinS.Y. PanX.H. TayP. LimW.H. TengM. SynN. LimG. YongJ.N. QuekJ. XiaoJ. DanY.Y. SiddiquiM.S. SanyalA.J. MuthiahM.D. LoombaR. HuangD.Q. Clinical characteristics, surveillance, treatment allocation, and outcomes of non-alcoholic fatty liver disease-related hepatocellular carcinoma: A systematic review and meta-analysis.Lancet Oncol.202223452153010.1016/S1470‑2045(22)00078‑X35255263
    [Google Scholar]
  10. YangJ.D. Detect or not to detect very early stage hepatocellular carcinoma? The western perspective.Clin. Mol. Hepatol.201925433534310.3350/cmh.2019.001030924328
    [Google Scholar]
  11. VachherM. BansalS. KumarB. YadavS. AroraT. WaliN.M. BurmanA. Contribution of organokines in the development of NAFLD/NASH associated hepatocellular carcinoma.J. Cell. Biochem.2022123101553158410.1002/jcb.3025235818831
    [Google Scholar]
  12. WangH. YangL. LiuM. LuoJ. Protein post-translational modifications in the regulation of cancer hallmarks.Cancer Gene Ther.202330452954710.1038/s41417‑022‑00464‑335393571
    [Google Scholar]
  13. KarlssonS. NyströmH. The extracellular matrix in colorectal cancer and its metastatic settling – Alterations and biological implications.Crit. Rev. Oncol. Hematol.202217510371210.1016/j.critrevonc.2022.10371235588938
    [Google Scholar]
  14. VajariaB.N. PatelP.S. Glycosylation: A hallmark of cancer?Glycoconj. J.201734214715610.1007/s10719‑016‑9755‑227975160
    [Google Scholar]
  15. ReilyC. StewartT.J. RenfrowM.B. NovakJ. Glycosylation in health and disease.Nat. Rev. Nephrol.201915634636610.1038/s41581‑019‑0129‑430858582
    [Google Scholar]
  16. ChenC. MaB. WangY. CuiQ. YaoL. LiY. ChenB. FengY. TanZ. Structural insight into why S-linked glycosylation cannot adequately mimic the role of natural O-glycosylation.Int. J. Biol. Macromol.2023253Pt 112664910.1016/j.ijbiomac.2023.12664937666405
    [Google Scholar]
  17. Loaeza-ReyesK.J. ZentenoE. Moreno-RodríguezA. Torres-RosasR. Argueta-FigueroaL. Salinas-MarínR. Castillo-RealL.M. Pina-CansecoS. CerveraY.P. An overview of glycosylation and its impact on cardiovascular health and disease.Front. Mol. Biosci.2021875163710.3389/fmolb.2021.75163734869586
    [Google Scholar]
  18. van der LaarseS.A.M. LeneyA.C. HeckA.J.R. Crosstalk between phosphorylation and O‐Glc NA cylation: Friend or foe.FEBS J.2018285173152316710.1111/febs.1449129717537
    [Google Scholar]
  19. SeebergerP.H. Essentials of Glycobiology.4th edCold Spring Harbor Laboratory PressCold Spring Harbor, NY2022
    [Google Scholar]
  20. BlochJ.S. JohnA. MaoR. MukherjeeS. BoilevinJ. IrobalievaR.N. DarbreT. ScottN.E. ReymondJ.L. KossiakoffA.A. Goddard-BorgerE.D. LocherK.P. Structure, sequon recognition and mechanism of tryptophan C-mannosyltransferase.Nat. Chem. Biol.202319557558410.1038/s41589‑022‑01219‑936604564
    [Google Scholar]
  21. MinakataS. ManabeS. InaiY. IkezakiM. NishitsujiK. ItoY. IharaY. Protein C-Mannosylation and C-Mannosyl Tryptophan in chemical biology and medicine.Molecules20212617525810.3390/molecules2617525834500691
    [Google Scholar]
  22. BuchowieckaA.K. Protein cysteine S-glycosylation: Oxidative hydrolysis of protein S-glycosidic bonds in aqueous alkaline environments.Amino Acids2023551617410.1007/s00726‑022‑03208‑736460841
    [Google Scholar]
  23. FujitaK. HatanoK. HashimotoM. TomiyamaE. MiyoshiE. NonomuraN. UemuraH. Fucosylation in urological cancers.Int. J. Mol. Sci.202122241333310.3390/ijms22241333334948129
    [Google Scholar]
  24. MiyoshiE. MoriwakiK. NakagawaT. Biological function of fucosylation in cancer biology.J. Biochem.2007143672572910.1093/jb/mvn01118218651
    [Google Scholar]
  25. ZhangY. WangR. FengY. MaF. The role of sialyltransferases in gynecological malignant tumors.Life Sci.202026311867010.1016/j.lfs.2020.11867033121992
    [Google Scholar]
  26. MunkleyJ. ElliottD.J. Hallmarks of glycosylation in cancer.Oncotarget2016723354783548910.18632/oncotarget.815527007155
    [Google Scholar]
  27. PinhoS.S. ReisC.A. Glycosylation in cancer: Mechanisms and clinical implications.Nat. Rev. Cancer201515954055510.1038/nrc398226289314
    [Google Scholar]
  28. MatsumotoK. YokoteH. AraoT. MaegawaM. TanakaK. FujitaY. ShimizuC. HanafusaT. FujiwaraY. NishioK. N -Glycan fucosylation of epidermal growth factor receptor modulates receptor activity and sensitivity to epidermal growth factor receptor tyrosine kinase inhibitor.Cancer Sci.20089981611161710.1111/j.1349‑7006.2008.00847.x18754874
    [Google Scholar]
  29. HashimotoS. AsaoT. TakahashiJ. YagihashiY. NishimuraT. SaniabadiA.R. PolandD.C.W. van DijkW. KuwanoH. KochibeN. YazawaS. α 1 ‐Acid glycoprotein fucosylation as a marker of carcinoma progression and prognosis.Cancer2004101122825283610.1002/cncr.2071315536618
    [Google Scholar]
  30. VerhelstX. DiasA.M. ColombelJ.F. VermeireS. Van VlierbergheH. CallewaertN. PinhoS.S. Protein glycosylation as a diagnostic and prognostic marker of chronic inflammatory gastrointestinal and liver diseases.Gastroenterology202015819511010.1053/j.gastro.2019.08.06031626754
    [Google Scholar]
  31. WangY. ChenH. Protein glycosylation alterations in hepatocellular carcinoma: Function and clinical implications.Oncogene202342241970197910.1038/s41388‑023‑02702‑w37193819
    [Google Scholar]
  32. RamachandranP. XuG. HuangH.H. RiceR. ZhouB. LindpaintnerK. SerieD. Serum glycoprotein markers in nonalcoholic steatohepatitis and hepatocellular carcinoma.J. Proteome Res.20222141083109410.1021/acs.jproteome.1c0096535286803
    [Google Scholar]
  33. GoldmanR. RessomH.W. VargheseR.S. GoldmanL. BascugG. LoffredoC.A. Abdel-HamidM. GoudaI. EzzatS. KyselovaZ. MechrefY. NovotnyM.V. Detection of hepatocellular carcinoma using glycomic analysis.Clin. Cancer Res.20091551808181310.1158/1078‑0432.CCR‑07‑526119223512
    [Google Scholar]
  34. MechrefY. PengW. GautamS. AhmadiP. LinY. ZhuJ. ZhangJ. LiuS. SingalA.G. ParikhN.D. LubmanD.M. Mass spectrometry based biomarkers for early detection of HCC using a glycoproteomic approach.Adv. Cancer Res.2023157235610.1016/bs.acr.2022.07.00536725111
    [Google Scholar]
  35. BlommeB. Van SteenkisteC. CallewaertN. Van VlierbergheH. Alteration of protein glycosylation in liver diseases.J. Hepatol.200950359260310.1016/j.jhep.2008.12.01019157620
    [Google Scholar]
  36. WestC.A. WangM. HerreraH. LiangH. BlackA. AngelP.M. DrakeR.R. MehtaA.S. N-linked glycan branching and fucosylation are increased directly in hcc tissue as determined through in situ glycan imaging.J. Proteome Res.201817103454346210.1021/acs.jproteome.8b0032330110170
    [Google Scholar]
  37. BurénS. GomesA.L. TeijeiroA. FawalM.A. YilmazM. TummalaK.S. PerezM. Rodriguez-JustoM. Campos-OlivasR. MegíasD. DjouderN. Regulation of OGT by URI in response to glucose confers c-MYC-dependent survival mechanisms.Cancer Cell201630229030710.1016/j.ccell.2016.06.02327505673
    [Google Scholar]
  38. TakayamaH. OhtaM. IwashitaY. UchidaH. ShitomiY. YadaK. InomataM. Altered glycosylation associated with dedifferentiation of hepatocellular carcinoma: A lectin microarray-based study.BMC Cancer202020119210.1186/s12885‑020‑6699‑532143591
    [Google Scholar]
  39. LiuY. LanL. LiY. LuJ. HeL. DengY. FeiM. LuJ.W. ShangguanF. LuJ.P. WangJ. WuL. HuangK. LuB. N-glycosylation stabilizes MerTK and promotes hepatocellular carcinoma tumor growth.Redox Biol.20225410236610.1016/j.redox.2022.10236635728303
    [Google Scholar]
  40. HuM. ZhangR. YangJ. ZhaoC. LiuW. HuangY. LyuH. XiaoS. GuoD. ZhouC. TangJ. The role of N-glycosylation modification in the pathogenesis of liver cancer.Cell Death Dis.202314322210.1038/s41419‑023‑05733‑z36990999
    [Google Scholar]
  41. ChenC. Schmilovitz-WeissH. LiuX. PappoO. HalpernM. SulkesJ. BraunM. CohenM. BarakN. Tur-KaspaR. VanhoorenV. Van VlierbergheH. LibertC. ContrerasR. Ben-AriZ. Serum protein N-glycans profiling for the discovery of potential biomarkers for nonalcoholic steatohepatitis.J. Proteome Res.20098246347010.1021/pr800656e19140676
    [Google Scholar]
  42. KamadaY. AkitaM. TakedaY. YamadaS. FujiiH. SawaiY. DoiY. AsazawaH. NakayamaK. MizutaniK. FujiiH. YakushijinT. MiyazakiM. EzakiH. HiramatsuN. YoshidaY. KisoS. ImaiY. KawadaN. TakeharaT. MiyoshiE. Serum fucosylated haptoglobin as a novel diagnostic biomarker for predicting hepatocyte ballooning and nonalcoholic steatohepatitis.PLoS One201386e6632810.1371/journal.pone.006632823805214
    [Google Scholar]
  43. MehtaA. BlockT.M. Fucosylated glycoproteins as markers of liver disease.Dis. Markers2008254-525926510.1155/2008/26459419126969
    [Google Scholar]
  44. WangY. FukudaT. IsajiT. LuJ. Loss of Al,6-Fucosyltransferase inhibits chemical-induced hepatocellular carcinoma and tumorigenesis by down-regulating several cell signaling pathways.FASEB J.2015293217322710.1096/fj.15‑27071025873065
    [Google Scholar]
  45. KuoH.H. LinR.J. HungJ.T. HsiehC.B. HungT.H. LoF.Y. HoM.Y. YehC.T. HuangY.L. YuJ. YuA.L. High expression FUT1 and B3GALT5 is an independent predictor of postoperative recurrence and survival in hepatocellular carcinoma.Sci. Rep.2017711075010.1038/s41598‑017‑11136‑w28883415
    [Google Scholar]
  46. NortonP.A. MehtaA.S. Expression of genes that control core fucosylation in hepatocellular carcinoma: Systematic review.World J. Gastroenterol.201925232947296010.3748/wjg.v25.i23.294731249452
    [Google Scholar]
  47. NakagawaT. UozumiN. NakanoM. Mizuno-HorikawaY. OkuyamaN. TaguchiT. GuJ. KondoA. TaniguchiN. MiyoshiE. Fucosylation of N-glycans regulates the secretion of hepatic glycoproteins into bile ducts.J. Biol. Chem.200628140297972980610.1074/jbc.M60569720016899455
    [Google Scholar]
  48. YangJ.D. DaiJ. SingalA.G. GopalP. AddissieB.D. NguyenM.H. BefelerA.S. ReddyK.R. SchwartzM. HarnoisD.M. YamadaH. GoresG.J. FengZ. MarreroJ.A. RobertsL.R. Improved performance of serum alpha-fetoprotein for hepatocellular carcinoma diagnosis in HCV cirrhosis with normal alanine transaminase.Cancer Epidemiol. Biomarkers Prev.20172671085109210.1158/1055‑9965.EPI‑16‑074728258053
    [Google Scholar]
  49. MarreroJ.A. KulikL.M. SirlinC.B. ZhuA.X. FinnR.S. AbecassisM.M. RobertsL.R. HeimbachJ.K. Diagnosis, staging, and management of hepatocellular carcinoma: 2018 Practice guidance by the American association for the study of liver diseases.Hepatology201868272375010.1002/hep.2991329624699
    [Google Scholar]
  50. SauzayC. PetitA. BourgeoisA.M. BarbareJ.C. ChauffertB. GalmicheA. HouessinonA. Alpha-foetoprotein (AFP): A multi-purpose marker in hepatocellular carcinoma.Clin. Chim. Acta2016463394410.1016/j.cca.2016.10.00627732875
    [Google Scholar]
  51. WangX. WangQ. Alpha-Fetoprotein and hepatocellular carcinoma immunity.Can. J. Gastroenterol. Hepatol.201820181810.1155/2018/904925229805966
    [Google Scholar]
  52. TzartzevaK. ObiJ. RichN.E. ParikhN.D. MarreroJ.A. YoppA. WaljeeA.K. SingalA.G. Surveillance imaging and alpha fetoprotein for early detection of hepatocellular carcinoma in patients with cirrhosis: A meta-analysis.Gastroenterology2018154617061718.e110.1053/j.gastro.2018.01.06429425931
    [Google Scholar]
  53. LiD. MalloryT. SatomuraS. AFP-L3: A new generation of tumor marker for hepatocellular carcinoma.Clin. Chim. Acta20013131-2151910.1016/S0009‑8981(01)00644‑111694234
    [Google Scholar]
  54. ChoiJ. KimG.A. HanS. LeeW. ChunS. LimY.S. Longitudinal assessment of three serum biomarkers to detect very early-stage hepatocellular carcinoma.Hepatology20196951983199410.1002/hep.3023330153338
    [Google Scholar]
  55. NishizonoI. IidaS. SuzukiN. KawadaH. MurakamiH. AshiharaY. OkadaM. Rapid and sensitive chemiluminescent enzyme immunoassay for measuring tumor markers.Clin. Chem.19913791639164410.1093/clinchem/37.9.16391716538
    [Google Scholar]
  56. HanifH. AliM.J. SusheelaA.T. KhanI.W. Luna-CuadrosM.A. KhanM.M. LauD.T.Y. Update on the applications and limitations of alpha-fetoprotein for hepatocellular carcinoma.World J. Gastroenterol.202228221622910.3748/wjg.v28.i2.21635110946
    [Google Scholar]
  57. IbrahimH.M. ElghannamM.Z. ElkhawagaO.A.Y. El-SokkaryA.M.A. Evaluation of serum alpha fetoprotein-L3 as an accuracy novel biomarker for the early diagnosis of hepatocellular carcinoma in Egyptian patients.Saudi J. Biol. Sci.202128105760576410.1016/j.sjbs.2021.06.02034588888
    [Google Scholar]
  58. AlsalloomA.A.M. An update of biochemical markers of hepatocellular carcinoma.Int. J. Health Sci. (Qassim)201610111713210.12816/003121927004063
    [Google Scholar]
  59. BertinoG. ArdiriA. MalaguarneraM. MalaguarneraG. BertinoN. CalvagnoG.S. Hepatocellualar carcinoma serum markers.Semin. Oncol.201239441043310.1053/j.seminoncol.2012.05.00122846859
    [Google Scholar]
  60. TaketaK. SekiyaC. NamikiM. AkamatsuK. OhtaY. EndoY. KosakaK. Lectin-reactive profiles of alpha-fetoprotein characterizing hepatocellular carcinoma and related conditions.Gastroenterology199099250851810.1016/0016‑5085(90)91034‑41694805
    [Google Scholar]
  61. ZhouJ.M. WangT. ZhangK.H. AFP-L3 for the diagnosis of early hepatocellular carcinoma.Medicine (Baltimore)202110043e2767310.1097/MD.000000000002767334713864
    [Google Scholar]
  62. BabalıA. ÇakalE. PurnakT. Bıyıkoğluİ. ÇakalB. YükselO. KöklüS. Serum α-fetoprotein levels in liver steatosis.Hepatol. Int.20093455155510.1007/s12072‑009‑9156‑819890679
    [Google Scholar]
  63. BestJ. BechmannL.P. SowaJ.P. SydorS. DechêneA. PflanzK. BedreliS. SchottenC. GeierA. BergT. FischerJ. VogelA. BantelH. WeinmannA. SchattenbergJ.M. HuberY. WegeH. von FeldenJ. SchulzeK. BettingerD. ThimmeR. SinnerF. SchütteK. WeissK.H. ToyodaH. YasudaS. KumadaT. BerhaneS. WichertM. HeiderD. GerkenG. JohnsonP. CanbayA. GALAD score detects early hepatocellular carcinoma in an international cohort of patients with nonalcoholic steatohepatitis.Clin. Gastroenterol. Hepatol.2020183728735.e410.1016/j.cgh.2019.11.01231712073
    [Google Scholar]
  64. LimT.S. RheeH. KimG.M. KimS.U. KimB.K. ParkJ.Y. AhnS.H. HanK.H. ChoiJ.Y. KimD.Y. Alpha-Fetoprotein, Des-Gamma-Carboxy Prothrombin, and modified RECIST response as predictors of survival after transarterial radioembolization for hepatocellular carcinoma.J. Vasc. Interv. Radiol.201930811941200.e110.1016/j.jvir.2019.03.01631235408
    [Google Scholar]
  65. NarakiT. KohnoN. SaitoH. FujimotoY. OhhiraM. MoritaT. KohgoY. γ-Carboxyglutamic acid content of hepatocellular carcinoma-associated des-γ-carboxy prothrombin.Biochim. Biophys. Acta Mol. Basis Dis.20021586328729810.1016/S0925‑4439(01)00107‑711997080
    [Google Scholar]
  66. WangS.B. ChengY.N. CuiS.X. ZhongJ.L. WardS.G. SunL.R. ChenM.H. KokudoN. TangW. QuX.J. Des-γ-carboxy prothrombin stimulates human vascular endothelial cell growth and migration.Clin. Exp. Metastasis200926546947710.1007/s10585‑009‑9246‑y19263229
    [Google Scholar]
  67. ZhangY.S. ChuJ.H. CuiS.X. SongZ.Y. QuX.J. Des-γ-carboxy prothrombin (DCP) as a potential autologous growth factor for the development of hepatocellular carcinoma.Cell. Physiol. Biochem.201434390391510.1159/00036630825200250
    [Google Scholar]
  68. YuenM.F. LaiC.L. Serological markers of liver cancer.Best Pract. Res. Clin. Gastroenterol.2005191919910.1016/j.bpg.2004.10.00315757806
    [Google Scholar]
  69. PanY. ChenH. YuJ. Biomarkers in hepatocellular carcinoma: Current status and future perspectives.Biomedicines202081257610.3390/biomedicines812057633297335
    [Google Scholar]
  70. NakamuraS. NousoK. SakaguchiK. ItoY.M. OhashiY. KobayashiY. ToshikuniN. TanakaH. MiyakeY. MatsumotoE. ShiratoriY. Sensitivity and specificity of des-gamma-carboxy prothrombin for diagnosis of patients with hepatocellular carcinomas varies according to tumor size.Am. J. Gastroenterol.200610192038204310.1111/j.1572‑0241.2006.00681.x16848811
    [Google Scholar]
  71. LiH. LiuH. YanL.J. DingZ.N. ZhangX. PanG.Q. HanC.L. TianB.W. TanS.Y. DongZ.R. WangD.X. YanY.C. LiT. Performance of GALAD score and serum biomarkers for detecting NAFLD-related HCC: A systematic review and network meta-analysis.Expert Rev. Gastroenterol. Hepatol.202317111159116710.1080/17474124.2023.227917537929312
    [Google Scholar]
  72. DobryszyckaW. Biological functions of haptoglobin--new pieces to an old puzzle.Eur. J. Clin. Chem. Clin. Biochem.19973596476549352226
    [Google Scholar]
  73. ZhangS. ShangS. LiW. QinX. LiuY. Insights on N-glycosylation of human haptoglobin and its association with cancers.Glycobiology201626768469210.1093/glycob/cww01626873173
    [Google Scholar]
  74. HülsmeierA.J. ToblerM. BurdaP. HennetT. Glycosylation site occupancy in health, congenital disorder of glycosylation and fatty liver disease.Sci. Rep.2016613392710.1038/srep3392727725718
    [Google Scholar]
  75. NakagawaT. MuramotoY. HoriM. MiharaS. MarubayashiT. NakagawaK. A preliminary investigation of the association between haptoglobin polymorphism, serum ferritin concentration and fatty liver disease.Clin. Chim. Acta20083981-2343810.1016/j.cca.2008.08.00418760271
    [Google Scholar]
  76. BaniniB.A. CazanaveS.C. YatesK.P. AsgharpourA. VincentR. MirshahiF. LeP. ContosM.J. TonasciaJ. ChalasaniN.P. KowdleyK.V. McCulloughA.J. BehlingC.A. SchwimmerJ.B. LavineJ.E. SanyalA.J. Haptoglobin 2 allele is associated with histologic response to vitamin E in subjects with nonalcoholic steatohepatitis.J. Clin. Gastroenterol.2019531075075810.1097/MCG.000000000000114230586008
    [Google Scholar]
  77. NaryznyS.N. LeginaO.K. Haptoglobin as a biomarker.Biochem. Suppl. Ser. B: Biomed. Chem.202115318419810.1134/S199075082103006934422226
    [Google Scholar]
  78. NarisadaM. KawamotoS. KuwamotoK. MoriwakiK. NakagawaT. MatsumotoH. AsahiM. KoyamaN. MiyoshiE. Identification of an inducible factor secreted by pancreatic cancer cell lines that stimulates the production of fucosylated haptoglobin in hepatoma cells.Biochem. Biophys. Res. Commun.2008377379279610.1016/j.bbrc.2008.10.06118951869
    [Google Scholar]
  79. ZhuJ. HuangJ. ZhangJ. ChenZ. LinY. GrigoreanG. LiL. LiuS. SingalA.G. ParikhN.D. LubmanD.M. Glycopeptide biomarkers in serum haptoglobin for hepatocellular carcinoma detection in patients with nonalcoholic steatohepatitis.J. Proteome Res.20201983452346610.1021/acs.jproteome.0c0027032412768
    [Google Scholar]
  80. ShangS. LiW. QinX. ZhangS. LiuY. Aided diagnosis of hepatocellular carcinoma using serum fucosylated haptoglobin ratios.J. Cancer20178588789310.7150/jca.1774728382152
    [Google Scholar]
  81. LinY. ZhuJ. ZhangJ. DaiJ. LiuS. ArroyoA. RoseM. SingalA.G. ParikhN.D. LubmanD.M. Glycopeptides with sialyl lewis antigen in serum haptoglobin as candidate biomarkers for nonalcoholic steatohepatitis hepatocellular carcinoma using a higher-energy collision-induced dissociation parallel reaction monitoring-mass spectrometry method.ACS Omega2022726228502286010.1021/acsomega.2c0260035811936
    [Google Scholar]
  82. AngI.L. PoonT.C.W. LaiP.B.S. ChanA.T.C. NgaiS.M. HuiA.Y. JohnsonP.J. SungJ.J.Y. Study of serum haptoglobin and its glycoforms in the diagnosis of hepatocellular carcinoma: A glycoproteomic approach.J. Proteome Res.20065102691270010.1021/pr060109r17022640
    [Google Scholar]
  83. ZhuJ. LinZ. WuJ. YinH. DaiJ. FengZ. MarreroJ. LubmanD.M. Analysis of serum haptoglobin fucosylation in hepatocellular carcinoma and liver cirrhosis of different etiologies.J. Proteome Res.20141362986299710.1021/pr500128t24807840
    [Google Scholar]
  84. Gutierrez ReyesC.D. HuangY. AtashiM. ZhangJ. ZhuJ. LiuS. ParikhN.D. SingalA.G. DaiJ. LubmanD.M. MechrefY. PRM-MS quantitative analysis of isomeric N-Glycopeptides derived from human serum haptoglobin of patients with cirrhosis and hepatocellular carcinoma.Metabolites202111856310.3390/metabo1108056334436504
    [Google Scholar]
  85. AsazawaH. KamadaY. TakedaY. TakamatsuS. ShinzakiS. KimY. NezuR. KuzushitaN. MitaE. KatoM. MiyoshiE. Serum fucosylated haptoglobin in chronic liver diseases as a potential biomarker of hepatocellular carcinoma development.Clin Chem Lab Med.20155319510210.1515/cclm‑2014‑042725060348
    [Google Scholar]
  86. PetaV. ZhuJ. LubmanD.M. HuguetS. Imbert-BismutdF. BolbachG. ClodicG. MatheronL. NgoY. RalucaP. HoussetC. RezaiK. PoynardT. Input of serum haptoglobin fucosylation profile in the diagnosis of hepatocellular carcinoma in patients with non-cirrhotic liver disease.Clin. Res. Hepatol. Gastroenterol.202044568169110.1016/j.clinre.2019.12.01031964615
    [Google Scholar]
  87. ZhangY. ZhuJ. YinH. MarreroJ. ZhangX.X. LubmanD.M. ESI–LC–MS method for haptoglobin fucosylation analysis in hepatocellular carcinoma and liver cirrhosis.J. Proteome Res.201514125388539510.1021/acs.jproteome.5b0079226503433
    [Google Scholar]
  88. ShiraiK. HikitaH. SakamoriR. DoiA. TahataY. SakaneS. KamadaY. MuraiK. NishioA. YamadaR. KodamaT. NozakiY. KakitaN. IshidaH. NakanishiF. MorishitaN. ImanakaK. SakakibaraM. TatsumiT. MiyoshiE. TakeharaT. Fucosylated haptoglobin is a novel predictive marker of hepatocellular carcinoma after hepatitis C virus elimination in patients with advanced liver fibrosis.PLoS One20221712e027941610.1371/journal.pone.027941636542633
    [Google Scholar]
  89. Kohansal-NodehiM. Swiatek-de LangeM. KroenigerK. RolnyV. TabarésG. PiratvisuthT. TanwandeeT. ThongsawatS. SukeepaisarnjaroenW. EstebanJ.I. BesM. KöhlerB. ChanH.L.Y. BusskampH. Discovery of a haptoglobin glycopeptides biomarker panel for early diagnosis of hepatocellular carcinoma.Front. Oncol.202313121389810.3389/fonc.2023.121389837920152
    [Google Scholar]
  90. TripodiA. LombardiR. PrimignaniM. La MuraV. PeyvandiF. FracanzaniA.L. Hypercoagulability in patients with non-alcoholic fatty liver disease (NAFLD): Causes and consequences.Biomedicines202210224910.3390/biomedicines1002024935203457
    [Google Scholar]
  91. WangJ. WangX. LinS. ChenC. WangC. MaQ. JiangB. Identification of kininogen-1 as a serum biomarker for the early detection of advanced colorectal adenoma and colorectal cancer.PLoS One201387e7051910.1371/journal.pone.007051923894665
    [Google Scholar]
  92. Abdul-RahmanP.S. LimB.K. HashimO.H. Expression of high-abundance proteins in sera of patients with endometrial and cervical cancers: Analysis using 2‐DE with silver staining and lectin detection methods.Electrophoresis200728121989199610.1002/elps.20060062917503403
    [Google Scholar]
  93. DoustjalaliS.R. YusofR. YipC.H. LooiL.M. PillayB. HashimO.H. Aberrant expression of acute‐phase reactant proteins in sera and breast lesions of patients with malignant and benign breast tumors.Electrophoresis200425142392240110.1002/elps.20030595015274022
    [Google Scholar]
  94. XuJ. FangJ. ChengZ. FanL. HuW. ZhouF. ShenH. Overexpression of the Kininogen-1 inhibits proliferation and induces apoptosis of glioma cells.J. Exp. Clin. Cancer Res.201837118010.1186/s13046‑018‑0833‑030068373
    [Google Scholar]
  95. LiuW. LiuB. CaiQ. LiJ. ChenX. ZhuZ. Proteomic identification of serum biomarkers for gastric cancer using multi-dimensional liquid chromatography and 2D differential gel electrophoresis.Clin. Chim. Acta201241313-141098110610.1016/j.cca.2012.03.00322446497
    [Google Scholar]
  96. Quesada-CalvoF. MassotC. BertrandV. LonguespéeR. BlétardN. SomjaJ. MazzucchelliG. SmargiassoN. BaiwirD. De Pauw-GilletM.C. DelvenneP. MalaiseM. Coimbra MarquesC. PolusM. De PauwE. MeuwisM.A. LouisE. OLFM4, KNG1 and Sec24C identified by proteomics and immunohistochemistry as potential markers of early colorectal cancer stages.Clin. Proteomics2017141910.1186/s12014‑017‑9143‑328344541
    [Google Scholar]
  97. WangM. LongR.E. ComunaleM.A. JunaidiO. MarreroJ. Di BisceglieA.M. BlockT.M. MehtaA.S. Novel fucosylated biomarkers for the early detection of hepatocellular carcinoma.Cancer Epidemiol. Biomarkers Prev.20091861914192110.1158/1055‑9965.EPI‑08‑098019454616
    [Google Scholar]
  98. WangM. SandaM. ComunaleM.A. HerreraH. SwindellC. KonoY. SingalA.G. MarreroJ. BlockT. GoldmanR. MehtaA. Changes in the glycosylation of kininogen and the development of a kininogen-based algorithm for the early detection of HCC.Cancer Epidemiol. Biomarkers Prev.201726579580310.1158/1055‑9965.EPI‑16‑097428223431
    [Google Scholar]
  99. WangM. ShenJ. HerreraH. SingalA. SwindellC. RenquanL. MehtaA. Biomarker analysis of fucosylated kininogen through depletion of lectin reactive heterophilic antibodies in hepatocellular carcinoma.J. Immunol. Methods2018462596410.1016/j.jim.2018.08.01030144410
    [Google Scholar]
  100. WangM. SingalA.G. ParikhN. KonoY. MarreroJ. MehtaA. A biomarker panel based upon AFP, fucosylated kininogen and PEG-precipitated IgG is highly accurate for the early detection hepatocellular carcinoma in patients with cirrhosis in phase II and phase III biomarker evaluation.Cancers (Basel)20221423597010.3390/cancers1423597036497452
    [Google Scholar]
  101. GreeneC.M. MarciniakS.J. TeckmanJ. FerrarottiI. BrantlyM.L. LomasD.A. StollerJ.K. McElvaneyN.G. α1-Antitrypsin deficiency.Nat. Rev. Dis. Primers2016211605110.1038/nrdp.2016.5127465791
    [Google Scholar]
  102. ComunaleM.A. Rodemich-BeteshL. HafnerJ. WangM. NortonP. Di BisceglieA.M. BlockT. MehtaA. Linkage specific fucosylation of alpha-1-antitrypsin in liver cirrhosis and cancer patients: Implications for a biomarker of hepatocellular carcinoma.PLoS One201058e1241910.1371/journal.pone.001241920811639
    [Google Scholar]
  103. KobayashiT. OgawaK. FurukawaJ. HanamatsuH. HatoM. YoshinagaT. MorikawaK. SudaG. ShoT. NakaiM. HigashinoK. NumataY. ShinoharaY. SakamotoN. Quantifying protein-specific N-glycome profiles by focused protein and immunoprecipitation glycomics.J. Proteome Res.20191883133314110.1021/acs.jproteome.9b0023231266306
    [Google Scholar]
  104. OgawaK. KobayashiT. FurukawaJ. HanamatsuH. NakamuraA. SuzukiK. KawagishiN. OharaM. UmemuraM. NakaiM. ShoT. SudaG. MorikawaK. BabaM. FuruyaK. TerashitaK. KobayashiT. OnoderaM. HorimotoT. ShinadaK. TsunematsuS. TsunematsuI. MeguroT. MitsuhashiT. HatoM. HigashinoK. ShinoharaY. SakamotoN. Tri-antennary tri-sialylated mono-fucosylated glycan of alpha-1 antitrypsin as a non-invasive biomarker for non-alcoholic steatohepatitis: A novel glycobiomarker for non-alcoholic steatohepatitis.Sci. Rep.202010132110.1038/s41598‑019‑56947‑131941930
    [Google Scholar]
  105. AbbasS.H. PickettE. LomasD.A. ThorburnD. GooptuB. HurstJ.R. MarshallA. Non-invasive testing for liver pathology in alpha-1 antitrypsin deficiency.BMJ Open Respir. Res.202071e00082010.1136/bmjresp‑2020‑00082033323365
    [Google Scholar]
  106. YinH. ZhuJ. WangM. YaoZ.P. LubmanD.M. Quantitative Analysis of α-1-Antitrypsin Glycosylation Isoforms in HCC Patients Using LC-HCD-PRM-MS.Anal. Chem.202092128201820810.1021/acs.analchem.0c0042032426967
    [Google Scholar]
  107. BerginD.A. ReevesE.P. MeleadyP. HenryM. McElvaneyO.J. CarrollT.P. CondronC. ChotirmallS.H. ClynesM. O’NeillS.J. McElvaneyN.G. α-1 Antitrypsin regulates human neutrophil chemotaxis induced by soluble immune complexes and IL-8.J. Clin. Invest.2010120124236425010.1172/JCI4119621060150
    [Google Scholar]
  108. O’BrienM.E. FeeL. BrowneN. CarrollT.P. MeleadyP. HenryM. McQuillanK. MurphyM.P. LoganM. McCarthyC. McElvaneyO.J. ReevesE.P. McElvaneyN.G. Activation of complement component 3 is associated with airways disease and pulmonary emphysema in alpha-1 antitrypsin deficiency.Thorax202075432133010.1136/thoraxjnl‑2019‑21407631959730
    [Google Scholar]
  109. JanciauskieneS. WrengerS. ImmenschuhS. OlejnickaB. GreulichT. WelteT. Chorostowska-WynimkoJ. The multifaceted effects of Alpha1-antitrypsin on neutrophil functions.Front. Pharmacol.2018934110.3389/fphar.2018.0034129719508
    [Google Scholar]
  110. ErcetinE. RichtmannS. DelgadoB.M. Gomez-MarianoG. WrengerS. KorenbaumE. LiuB. DeLucaD. KühnelM.P. JonigkD. YuskaevaK. WarthA. MuleyT. WinterH. MeisterM. WelteT. JanciauskieneS. SchneiderM.A. Clinical significance of SERPINA1 gene and its encoded Alpha1-antitrypsin protein in NSCLC.Cancers (Basel)2019119130610.3390/cancers1109130631487965
    [Google Scholar]
  111. KoukoulisG.K. ShenJ. VirtanenI. GouldV.E. Vitronectin in the cirrhotic liver: An immunomarker of mature fibrosis.Hum. Pathol.200132121356136210.1053/hupa.2001.2967511774169
    [Google Scholar]
  112. HayashidaM. HashimotoK. IshikawaT. MiyamotoY. Vitronectin deficiency attenuates hepatic fibrosis in a non-alcoholic steatohepatitis-induced mouse model.Int. J. Exp. Pathol.20191002728210.1111/iep.1230630887659
    [Google Scholar]
  113. LinY. ZhuJ. PanL. ZhangJ. TanZ. OlivaresJ. SingalA.G. ParikhN.D. LubmanD.M. A panel of glycopeptides as candidate biomarkers for early diagnosis of NASH hepatocellular carcinoma using a stepped HCD method and prm evaluation.J. Proteome Res.20212063278328910.1021/acs.jproteome.1c0017533929864
    [Google Scholar]
  114. HwangH. LeeJ.Y. LeeH.K. ParkG.W. JeongH.K. MoonM.H. KimJ.Y. YooJ.S. In-depth analysis of site-specific N-glycosylation in vitronectin from human plasma by tandem mass spectrometry with immunoprecipitation.Anal. Bioanal. Chem.2014406307999801110.1007/s00216‑014‑8226‑525374123
    [Google Scholar]
  115. SchvartzI. SegerD. ShaltielS. Vitronectin.Int. J. Biochem. Cell Biol.199931553954410.1016/S1357‑2725(99)00005‑910399314
    [Google Scholar]
  116. MontaldoC. MatteiS. BaiocchiniA. RotirotiN. NonnoF.D. PucilloL.P. CozzolinoA.M. BattistelliC. AmiconeL. IppolitoG. van NoortV. ConigliaroA. AlonziT. TripodiM. ManconeC. Spike‐in SILAC proteomic approach reveals the vitronectin as an early molecular signature of liver fibrosis in hepatitis C infections with hepatic iron overload.Proteomics20141491107111510.1002/pmic.20130042224616218
    [Google Scholar]
  117. EdwardsS. LalorP.F. TuncerC. AdamsD.H. Vitronectin in human hepatic tumours contributes to the recruitment of lymphocytes in an αvβ3-independent manner.Br. J. Cancer200695111545155410.1038/sj.bjc.660346717088900
    [Google Scholar]
  118. Vitronectin (VTN) Vitronectin (VTN): A novel diagnostic and prognostic marker for Hepatocellular Carcinoma (HCC) on top of chronic hepatitis C virus related diseases.Egypt. J. Hosp. Med.20239216363637010.21608/ejhm.2023.314498
    [Google Scholar]
  119. Del BenM. OveriD. PolimeniL. CarpinoG. LabbadiaG. BarattaF. PastoriD. NoceV. GaudioE. AngelicoF. ManconeC. Overexpression of the vitronectin V10 subunit in patients with nonalcoholic steatohepatitis: Implications for noninvasive diagnosis of NASH.Int. J. Mol. Sci.201819260310.3390/ijms1902060329463024
    [Google Scholar]
  120. RangaswamiH. BulbuleA. KunduG.C. Osteopontin: Role in cell signaling and cancer progression.Trends Cell Biol.2006162798710.1016/j.tcb.2005.12.00516406521
    [Google Scholar]
  121. WuQ. LiL. MiaoC. HasnatM. SunL. JiangZ. ZhangL. Osteopontin promotes hepatocellular carcinoma progression through inducing JAK2/STAT3/NOX1-mediated ROS production.Cell Death Dis.202213434110.1038/s41419‑022‑04806‑935418176
    [Google Scholar]
  122. NomiyamaT. Perez-TilveD. OgawaD. GizardF. ZhaoY. HeywoodE.B. JonesK.L. KawamoriR. CassisL.A. TschöpM.H. BruemmerD. Osteopontin mediates obesity-induced adipose tissue macrophage infiltration and insulin resistance in mice.J. Clin. Invest.2007117102877288810.1172/JCI3198617823662
    [Google Scholar]
  123. KahlesF. FindeisenH.M. BruemmerD. Osteopontin: A novel regulator at the cross roads of inflammation, obesity and diabetes.Mol. Metab.20143438439310.1016/j.molmet.2014.03.00424944898
    [Google Scholar]
  124. KieferF.W. ZeydaM. GollingerK. PfauB. NeuhoferA. WeichhartT. SäemannM.D. GeyereggerR. SchledererM. KennerL. StulnigT.M. Neutralization of osteopontin inhibits obesity-induced inflammation and insulin resistance.Diabetes201059493594610.2337/db09‑040420107108
    [Google Scholar]
  125. IcerM.A. Gezmen-KaradagM. The multiple functions and mechanisms of osteopontin.Clin. Biochem.201859172410.1016/j.clinbiochem.2018.07.00330003880
    [Google Scholar]
  126. GlassO. HenaoR. PatelK. GuyC.D. GrussH.J. SynW.K. MoylanC.A. StreileinR. HallR. Mae DiehlA. AbdelmalekM.F. Serum interleukin‐8, osteopontin, and monocyte chemoattractant protein 1 are associated with hepatic fibrosis in patients with nonalcoholic fatty liver disease.Hepatol. Commun.20182111344135510.1002/hep4.123730411081
    [Google Scholar]
  127. NardoA.D. GrünN.G. ZeydaM. DumanicM. OberhuberG. RivellesE. HelbichT.H. MarkgrafD.F. RodenM. ClaudelT. TraunerM. StulnigT.M. Impact of osteopontin on the development of non‐alcoholic liver disease and related hepatocellular carcinoma.Liver Int.20204071620163310.1111/liv.1446432281248
    [Google Scholar]
  128. ShangS. PlymothA. GeS. FengZ. RosenH.R. SangrajrangS. HainautP. MarreroJ.A. BerettaL. Identification of osteopontin as a novel marker for early hepatocellular carcinoma.Hepatology201255248349010.1002/hep.2470321953299
    [Google Scholar]
  129. SunH.Y. LiY. GuoK. KangX.N. SunC. LiuY.K. Identification of metastasis-related osteopontin expression and glycosylation in hepatocellular carcinoma.Zhonghua Gan Zang Bing Za Zhi2011191290490722525502
    [Google Scholar]
  130. BruhaR. VitekL. SmidV. Osteopontin – A potential biomarker of advanced liver disease.Ann. Hepatol.202019434435210.1016/j.aohep.2020.01.00132005637
    [Google Scholar]
  131. SunT. LiP. SunD. BuQ. LiG. Prognostic value of osteopontin in patients with hepatocellular carcinoma.Medicine (Baltimore)20189743e1295410.1097/MD.000000000001295430412113
    [Google Scholar]
  132. ZhouF. ShangW. YuX. TianJ. Glypican‐3: A promising biomarker for hepatocellular carcinoma diagnosis and treatment.Med. Res. Rev.201838274176710.1002/med.2145528621802
    [Google Scholar]
  133. CapurroM. WanlessI.R. ShermanM. DeboerG. ShiW. MiyoshiE. FilmusJ. Glypican-3: A novel serum and histochemical marker for hepatocellular carcinoma.Gastroenterology20031251899710.1016/S0016‑5085(03)00689‑912851874
    [Google Scholar]
  134. IsmailM. Glypican-3-expressing hepatocellular carcinoma in a non-cirrhotic patient with nonalcoholic steatohepatitis: Case report and literature review.Gastroenterol. Res.20103522322810.4021/gr224w27957002
    [Google Scholar]
  135. NakatsuraT. YoshitakeY. SenjuS. MonjiM. KomoriH. MotomuraY. HosakaS. BeppuT. IshikoT. KamoharaH. AshiharaH. KatagiriT. FurukawaY. FujiyamaS. OgawaM. NakamuraY. NishimuraY. Glypican-3, overexpressed specifically in human hepatocellular carcinoma, is a novel tumor marker.Biochem. Biophys. Res. Commun.20033061162510.1016/S0006‑291X(03)00908‑212788060
    [Google Scholar]
  136. ChenM. LiG. YanJ. LuX. CuiJ. NiZ. ChengW. QianG. ZhangJ. TuH. Reevaluation of glypican-3 as a serological marker for hepatocellular carcinoma.Clin. Chim. Acta201342310511110.1016/j.cca.2013.04.02623643963
    [Google Scholar]
  137. HaruyamaY. KataokaH. Glypican-3 is a prognostic factor and an immunotherapeutic target in hepatocellular carcinoma.World J. Gastroenterol.201622127528310.3748/wjg.v22.i1.27526755876
    [Google Scholar]
  138. GuoM. ZhangH. ZhengJ. LiuY. Glypican-3: A new target for diagnosis and treatment of hepatocellular carcinoma.J. Cancer20201182008202110.7150/jca.3997232127929
    [Google Scholar]
  139. JaniszewskaE. KmieciakA. KacperczykM. WitkowskaA. KratzE.M. The influence of clusterin glycosylation variability on selected pathophysiological processes in the human body.Oxid. Med. Cell. Longev.2022202212510.1155/2022/765787636071866
    [Google Scholar]
  140. MamunM.A.A. ZhengY.C. WangN. WangB. ZhangY. PangJ.R. ShenD.D. LiuH.M. GaoY. Decoding CLU (Clusterin): Conquering cancer treatment resistance and immunological barriers.Int. Immunopharmacol.202413711235510.1016/j.intimp.2024.11235538851158
    [Google Scholar]
  141. WonJ.C. ParkC.Y. OhS.W. LeeE.S. YounB.S. KimM.S. Plasma clusterin (ApoJ) levels are associated with adiposity and systemic inflammation.PLoS One201497e10335110.1371/journal.pone.010335125076422
    [Google Scholar]
  142. WangY. ShenY. HuT. WangY. MaX. YuH. BaoY. Associations between serum clusterin levels and non-alcoholic fatty liver disease.Endocr. Connect.2023127e22054510.1530/EC‑22‑054537043769
    [Google Scholar]
  143. SeoH.Y. KimM.K. JungY.A. JangB.K. YooE.K. ParkK.G. LeeI.K. Clusterin decreases hepatic SREBP-1c expression and lipid accumulation.Endocrinology201315451722173010.1210/en.2012‑200923515283
    [Google Scholar]
  144. KwonM.J. JuT. HeoJ.Y. KimY.W. KimJ.Y. WonK.C. KimJ.R. BaeY.K. ParkI.S. MinB.H. LeeI.K. ParkS.Y. Deficiency of clusterin exacerbates high-fat diet-induced insulin resistance in male mice.Endocrinology201415562089210110.1210/en.2013‑187024684302
    [Google Scholar]
  145. ParkJ.S. ShimY.J. KangB.H. LeeW.K. MinB.H. Hepatocyte-specific clusterin overexpression attenuates diet-induced nonalcoholic steatohepatitis.Biochem. Biophys. Res. Commun.201849521775178110.1016/j.bbrc.2017.12.04529229391
    [Google Scholar]
  146. ParkJ.S. LeeW.K. KimH.S. SeoJ.A. KimD.H. HanH.C. MinB.H. Clusterin overexpression protects against western diet-induced obesity and NAFLD.Sci. Rep.20201011748410.1038/s41598‑020‑73927‑y33060605
    [Google Scholar]
  147. StefanN. SchickF. BirkenfeldA.L. HäringH.U. WhiteM.F. The role of hepatokines in NAFLD.Cell Metab.202335223625210.1016/j.cmet.2023.01.00636754018
    [Google Scholar]
  148. KangY.K. HongS.W. LeeH. KimW.H. Overexpression of clusterin in human hepatocellular carcinoma.Hum. Pathol.200435111340134610.1016/j.humpath.2004.07.02115668890
    [Google Scholar]
  149. LauS.H. ShamJ.S.T. XieD. TzangC-H. TangD. MaN. HuL. WangY. WenJ-M. XiaoG. ZhangW-M. LauG.K.K. YangM. GuanX-Y. Clusterin plays an important role in hepatocellular carcinoma metastasis.Oncogene20062581242125010.1038/sj.onc.120914116247463
    [Google Scholar]
  150. PengM. DengJ. ZhouS. TaoT. SuQ. XueY. YangX. The role of Clusterin in cancer metastasis.Cancer Manag. Res.2019112405241410.2147/CMAR.S19627331114318
    [Google Scholar]
  151. ComunaleM.A. WangM. Rodemich-BeteshL. HafnerJ. LamontagneA. KleinA. MarreroJ. Di BisceglieA.M. GishR. BlockT. MehtaA. Novel changes in glycosylation of serum Apo-J in patients with hepatocellular carcinoma.Cancer Epidemiol. Biomarkers Prev.20112061222122910.1158/1055‑9965.EPI‑10‑104721467232
    [Google Scholar]
  152. GaoG. LuanX. Diagnostic performance of clusterin in hepatocellular carcinoma: A meta-analysis.Int. J. Biol. Markers202237440441110.1177/0393615522110120635645149
    [Google Scholar]
  153. Beheshti NamdarA. KabiriM. Mosanan MozaffariH. AminifarE. Mehrad-MajdH. Circulating clusterin levels and cancer risk: A systematic review and meta-analysis.Cancer Contr.20222910.1177/1073274821103843735465749
    [Google Scholar]
  154. HellmanN.E. GitlinJ.D. Ceruloplasmin metabolism and function.Annu. Rev. Nutr.200222143945810.1146/annurev.nutr.22.012502.11445712055353
    [Google Scholar]
  155. BanhaJ. MarquesL. OliveiraR. MartinsM.F. PaixãoE. PereiraD. MalhóR. PenqueD. CostaL. Ceruloplasmin expression by human peripheral blood lymphocytes: A new link between immunity and iron metabolism.Free Radic. Biol. Med.200844348349210.1016/j.freeradbiomed.2007.10.03217991445
    [Google Scholar]
  156. KimO.Y. ShinM.J. MoonJ. ChungJ.H. Plasma ceruloplasmin as a biomarker for obesity: A proteomic approach.Clin. Biochem.2011445-635135610.1016/j.clinbiochem.2011.01.01421291874
    [Google Scholar]
  157. MarquesL. AuriacA. WillemetzA. BanhaJ. SilvaB. Canonne-HergauxF. CostaL. Immune cells and hepatocytes express glycosylphosphatidylinositol-anchored ceruloplasmin at their cell surface.Blood Cells Mol. Dis.201248211012010.1016/j.bcmd.2011.11.00522178061
    [Google Scholar]
  158. BielliP. CalabreseL. Structure to function relationships in ceruloplasmin: A ‘moonlighting’ protein.Cell. Mol. Life Sci.20025991413142710.1007/s00018‑002‑8519‑212440766
    [Google Scholar]
  159. LiuZ. WangM. ZhangC. ZhouS. JiG. Molecular functions of ceruloplasmin in metabolic disease pathology.Diabetes Metab. Syndr. Obes.20221569571110.2147/DMSO.S34664835264864
    [Google Scholar]
  160. GolizehM. LeeK. IlchenkoS. ÖsmeA. BenaJ. SadygovR.G. KashyapS.R. KasumovT. Increased serotransferrin and ceruloplasmin turnover in diet-controlled patients with type 2 diabetes.Free Radic. Biol. Med.201711346146910.1016/j.freeradbiomed.2017.10.37329079528
    [Google Scholar]
  161. KimC.H. ParkJ.Y. KimJ.Y. ChoiC.S. KimY.I. ChungY.E. LeeM.S. HongS.K. LeeK.U. Elevated serum ceruloplasmin levels in subjects with metabolic syndrome: A population-based study.Metabolism200251783884210.1053/meta.2002.3334812077727
    [Google Scholar]
  162. XiaZ. HuM. ZhengL. ZhengE. DengM. WuJ. ShengX. Assessing whether serum ceruloplasmin promotes non-alcoholic steatohepatitis via regulating iron metabolism.J. Med. Biochem.202342111312110.5937/jomb0‑3759736819130
    [Google Scholar]
  163. XieL. YuanY. XuS. LuS. GuJ. WangY. WangY. ZhangX. ChenS. LiJ. LuJ. SunH. HuR. PiaoH. WangW. WangC. WangJ. LiN. WhiteM.F. HanL. JiaW. MiaoJ. LiuJ. Downregulation of hepatic ceruloplasmin ameliorates NAFLD via SCO1-AMPK-LKB1 complex.Cell Rep.202241311149810.1016/j.celrep.2022.11149836261001
    [Google Scholar]
  164. JiangQ. WangN. LuS. XiongJ. YuanY. LiuJ. ChenS. Targeting hepatic ceruloplasmin mitigates nonalcoholic steatohepatitis by modulating bile acid metabolism.J. Mol. Cell Biol.2024159mjad06010.1093/jmcb/mjad06037771074
    [Google Scholar]
  165. NunesV.S. AndradeA.R. GuedesA.L.V. DinizM.A. OliveiraC.P. Distinct phenotype of non-alcoholic fatty liver disease in patients with low levels of free copper and of ceruloplasmin.Arq. Gastroenterol.20205724925310.1590/s0004‑2803.202000000‑4732935743
    [Google Scholar]
  166. LopezM.J. RoyerA. ShahN. Biochemistry, Ceruloplasmin.StatPearls PublishingTreasure Island, FL2024
    [Google Scholar]
  167. MacknessM. MacknessB. Human paraoxonase-1 (PON1): Gene structure and expression, promiscuous activities and multiple physiological roles.Gene20155671122110.1016/j.gene.2015.04.08825965560
    [Google Scholar]
  168. Grdic RajkovicM. RumoraL. BarisicK. The paraoxonase 1, 2 and 3 in humans.Biochem. Med. (Zagreb)201121212213010.11613/BM.2011.02022135851
    [Google Scholar]
  169. DeakinS. LevievI. GomaraschiM. CalabresiL. FranceschiniG. JamesR.W. Enzymatically active paraoxonase-1 is located at the external membrane of producing cells and released by a high affinity, saturable, desorption mechanism.J. Biol. Chem.200227764301430810.1074/jbc.M10744020011726658
    [Google Scholar]
  170. RodrigoL. HernándezA.F. López-CaballeroJ.J. GilF. PlaA. Immunohistochemical evidence for the expression and induction of paraoxonase in rat liver, kidney, lung and brain tissue. implications for its physiological role.Chem. Biol. Interact.2001137212313710.1016/S0009‑2797(01)00225‑311551529
    [Google Scholar]
  171. KotaniK. WatanabeJ. MiuraK. GugliucciA. Paraoxonase 1 and non-alcoholic fatty liver disease: A meta-analysis.Molecules2021268232310.3390/molecules2608232333923656
    [Google Scholar]
  172. AtamerA. BiliciA. YeniceN. SelekS. IlhanN. AtamerY. The importance of paraoxonase 1 activity, nitric oxide and lipid peroxidation in hepatosteatosis.J. Int. Med. Res.200836477177610.1177/14732300080360041918652773
    [Google Scholar]
  173. DesaiS. BakerS.S. LiuW. MoyaD.A. BrowneR.W. MastrandreaL. BakerR.D. ZhuL. Paraoxonase 1 and oxidative stress in paediatric non‐alcoholic steatohepatitis.Liver Int.201434111011710.1111/liv.1230824028323
    [Google Scholar]
  174. FedelesovaM. KupcovaV. LuhaJ. TureckyL. Paraoxonase activity in sera of patients with non-alcoholic fatty liver disease.Bratisl. Lek Listy20171181271972029322801
    [Google Scholar]
  175. García-HerediaA. KensickiE. MohneyR.P. RullA. TrigueroI. MarsillachJ. TormosC. MacknessB. MacknessM. ShihD.M. Pedro-BotetJ. JovenJ. SáezG. CampsJ. Paraoxonase-1 deficiency is associated with severe liver steatosis in mice fed a high-fat high-cholesterol diet: A metabolomic approach.J. Proteome Res.20131241946195510.1021/pr400050u23448543
    [Google Scholar]
  176. RozenbergO. ShihD.M. AviramM. Human serum paraoxonase 1 decreases macrophage cholesterol biosynthesis: Possible role for its phospholipase-A2-like activity and lysophosphatidylcholine formation.Arterioscler. Thromb. Vasc. Biol.200323346146710.1161/01.ATV.0000060462.35946.B312615663
    [Google Scholar]
  177. CheungK.J. TillemanK. DeforceD. ColleI. Van VlierbergheH. The HCV serum proteome: A search for fibrosis protein markers.J. Viral Hepat.200916641842910.1111/j.1365‑2893.2009.01083.x19226329
    [Google Scholar]
  178. PrzybyłoM. MartuszewskaD. PochećE. Hoja-ŁukowiczD. LityńskaA. Identification of proteins bearing β1–6 branched N-glycans in human melanoma cell lines from different progression stages by tandem mass spectrometry analysis.Biochim. Biophys. Acta, Gen. Subj.2007177091427143510.1016/j.bbagen.2007.05.00617600626
    [Google Scholar]
  179. XuQ. FengM. RenY. LiuX. GaoH. LiZ. SuX. WangQ. WangY. From NAFLD to HCC: Advances in noninvasive diagnosis.Biomed. Pharmacother.202316511502810.1016/j.biopha.2023.11502837331252
    [Google Scholar]
  180. KamadaY. OnoM. HyogoH. FujiiH. SumidaY. MoriK. TanakaS. YamadaM. AkitaM. MizutaniK. FujiiH. YamamotoA. TakamatsuS. YoshidaY. ItohY. KawadaN. ChayamaK. SaibaraT. TakeharaT. MiyoshiE. A novel noninvasive diagnostic method for nonalcoholic steatohepatitis using two glycobiomarkers.Hepatology20156251433144310.1002/hep.2800226199205
    [Google Scholar]
  181. KamadaY. OnoM. HyogoH. FujiiH. SumidaY. YamadaM. MoriK. TanakaS. MaekawaT. EbisutaniY. YamamotoA. TakamatsuS. YonedaM. KawadaN. ChayamaK. SaibaraT. TakeharaT. MiyoshiE. Use of Mac‐2 binding protein as a biomarker for nonalcoholic fatty liver disease diagnosis.Hepatol. Commun.20171878079110.1002/hep4.108029404494
    [Google Scholar]
  182. KamadaY. MorishitaK. KosekiM. NishidaM. AsukaT. NaitoY. YamadaM. TakamatsuS. SakataY. TakeharaT. MiyoshiE. Serum Mac-2 binding protein levels associate with metabolic parameters and predict liver fibrosis progression in subjects with fatty liver disease: A 7-year longitudinal study.Nutrients2020126177010.3390/nu1206177032545650
    [Google Scholar]
  183. AbeM. MiyakeT. KunoA. ImaiY. SawaiY. HinoK. HaraY. HigeS. SakamotoM. YamadaG. KageM. KorenagaM. HiasaY. MizokamiM. NarimatsuH. Association between Wisteria floribunda agglutinin-positive Mac-2 binding protein and the fibrosis stage of non-alcoholic fatty liver disease.J. Gastroenterol.201550777678410.1007/s00535‑014‑1007‑225326152
    [Google Scholar]
  184. ItoK. MurotaniK. NakadeY. InoueT. NakaoH. SumidaY. KamadaY. YonedaM. Serum Wisteria floribunda agglutinin‐positive Mac‐2‐binding protein levels and liver fibrosis: A meta‐analysis.J. Gastroenterol. Hepatol.201732121922193010.1111/jgh.1380228406534
    [Google Scholar]
  185. JangS.Y. TakW.Y. ParkS.Y. KweonY.O. LeeY.R. KimG. HurK. HanM.H. LeeW.K. Diagnostic efficacy of serum Mac-2 binding protein glycosylation isomer and other markers for liver fibrosis in non-alcoholic fatty liver diseases.Ann. Lab. Med.202141330230910.3343/alm.2021.41.3.30233303715
    [Google Scholar]
  186. FernandesC.L. Ligabue-BraunR. VerliH. Structural glycobiology of human α 1 -acid glycoprotein and its implications for pharmacokinetics and inflammation.Glycobiology201525101125113310.1093/glycob/cwv04126088564
    [Google Scholar]
  187. CecilianiF. LecchiC. The immune functions of α 1 acid glycoprotein.Curr. Protein Pept. Sci.201920650552410.2174/138920372066619040510113830950347
    [Google Scholar]
  188. FournierT. Medjoubi-NN. PorquetD. Alpha-1-acid glycoprotein.Biochim. Biophys. Acta Protein Struct. Mol. Enzymol.200014821-215717110.1016/S0167‑4838(00)00153‑911058758
    [Google Scholar]
  189. CecilianiF. PocacquaV. The acute phase protein alpha1-acid glycoprotein: A model for altered glycosylation during diseases.Curr. Protein Pept. Sci.2007819110810.2174/13892030777994149717305563
    [Google Scholar]
  190. K, T.; K, K.; N, K.; S, I. Multifucosylated Alpha-1-Acid Glycoprotein as a Novel Marker for Hepatocellular Carcinoma.J. Proteome Res.201615
    [Google Scholar]
  191. ÅströmE. StålP. ZenlanderR. EdenvikP. AlexanderssonC. HaglundM. RydénI. PåhlssonP. Reverse lectin ELISA for detecting fucosylated forms of α1-acid glycoprotein associated with hepatocellular carcinoma.PLoS One2017123e017389710.1371/journal.pone.017389728296934
    [Google Scholar]
  192. GaniR.A. SuryaminM. HasanI. LesmanaC.R.A. SanityosoA. Performance of alpha fetoprotein in combination with Alpha-1-acid Glycoprotein for diagnosis of hepatocellular carcinoma among liver cirrhosis patients.Acta Med. Indones.201547321622226586387
    [Google Scholar]
  193. ZhangD. HuangJ. LuoD. FengX. LiuY. LiuY. Glycosylation change of alpha-1-acid glycoprotein as a serum biomarker for hepatocellular carcinoma and cirrhosis.Biomarkers Med.201711542343010.2217/bmm‑2016‑028428621608
    [Google Scholar]
  194. HuhnC. SelmanM.H.J. RuhaakL.R. DeelderA.M. WuhrerM. IgG glycosylation analysis.Proteomics20099488291310.1002/pmic.20080071519212958
    [Google Scholar]
  195. ZhaoZ.Y. LiuD. CaoW.J. SunM. SongM.S. WangW. WangY.X. Association between IgG N-glycans and nonalcoholic fatty liver disease in Han Chinese.Biomed. Environ. Sci.201831645445830025558
    [Google Scholar]
  196. YuanW. SandaM. WuJ. KoomenJ. GoldmanR. Quantitative analysis of immunoglobulin subclasses and subclass specific glycosylation by LC–MS–MRM in liver disease.J. Proteomics2015116243310.1016/j.jprot.2014.12.02025582524
    [Google Scholar]
  197. OlubuyideI.O. SalimonuL.S. AdeniranS.O. Soluble immune complexes and immunoglobulin (IgG, IgA and IgM) levels in Nigerians with primary liver cell carcinoma.Afr. J. Med. Med. Sci.199322457627839931
    [Google Scholar]
  198. YiC.H. WengH.L. ZhouF.G. FangM. JiJ. ChengC. WangH. LiebeR. DooleyS. GaoC.F. Elevated core-fucosylated IgG is a new marker for hepatitis B virus-related hepatocellular carcinoma.OncoImmunology2015412e101150310.1080/2162402X.2015.101150326587313
    [Google Scholar]
  199. SunZ. FuB. WangG. ZhangL. XuR. ZhangY. LuH. High-throughput site-specific N -glycoproteomics reveals glyco-signatures for liver disease diagnosis.Natl. Sci. Rev.2023101nwac05910.1093/nsr/nwac05936879659
    [Google Scholar]
  200. LiuX. FuB. ChenJ. SunZ. ZhengD. LiZ. GuB. ZhangY. LuH. High-throughput intact Glycopeptide quantification strategy with targeted-MS (HTiGQs-target) reveals site-specific IgG N-glycopeptides as biomarkers for hepatic disorder diagnosis and staging.Carbohydr. Polym.202432512149910.1016/j.carbpol.2023.12149938008487
    [Google Scholar]
  201. DelangheJ.R. LangloisM.R. Hemopexin: A review of biological aspects and the role in laboratory medicine.Clin. Chim. Acta20013121-2132310.1016/S0009‑8981(01)00586‑111580905
    [Google Scholar]
  202. TolosanoE. AltrudaF. Hemopexin: Structure, function, and regulation.DNA Cell Biol.200221429730610.1089/10445490275375971712042069
    [Google Scholar]
  203. FioritoV. ChiabrandoD. PetrilloS. BertinoF. TolosanoE. The multifaceted role of heme in cancer.Front. Oncol.20209154010.3389/fonc.2019.0154032010627
    [Google Scholar]
  204. MaJ. SandaM. WeiR. ZhangL. GoldmanR. Quantitative analysis of core fucosylation of serum proteins in liver diseases by LC-MS-MRM.J. Proteomics2018189677410.1016/j.jprot.2018.02.00329427759
    [Google Scholar]
  205. BenickyJ. SandaM. PompachP. WuJ. GoldmanR. Quantification of fucosylated hemopexin and complement factor H in plasma of patients with liver disease.Anal. Chem.20148621107161072310.1021/ac502727s25302577
    [Google Scholar]
  206. ZhaoY. SatoY. IsajiT. FukudaT. MatsumotoA. MiyoshiE. GuJ. TaniguchiN. Branched N‐glycans regulate the biological functions of integrins and cadherins.FEBS J.200827591939194810.1111/j.1742‑4658.2008.06346.x18384383
    [Google Scholar]
  207. DebruyneE.N. VanderschaegheD. Van VlierbergheH. VanheckeA. CallewaertN. DelangheJ.R. Diagnostic value of the hemopexin N-glycan profile in hepatocellular carcinoma patients.Clin. Chem.201056582383110.1373/clinchem.2009.13929520348404
    [Google Scholar]
/content/journals/cp/10.2174/0115701646341608241025030547
Loading
/content/journals/cp/10.2174/0115701646341608241025030547
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error
Please enter a valid_number test