Skip to content
2000
Volume 31, Issue 42
  • ISSN: 0929-8673
  • E-ISSN: 1875-533X

Abstract

Background

Gastric cancer is one of the most common malignant tumours of the gastrointestinal tract, which has a significant negative impact on human health.

Aims

CCL chemokines play important roles in a variety of tumor microenvironments; nevertheless, gastric cancer has surprisingly limited associations with CCL chemokines.

Methods

In our study, we comprehensively utilized bioinformatics analysis tools and databases such as cBioPortal, UALCAN, GEPIA, GeneMANIA, STRING, and TRRUST to clarify the clinical significance and biology function of CCL chemokines in gastric cancer.

Results

The mRNA expression levels of CCL1/3/4/5/7/8/14/15/18/20/21/22/26 were up-regulated, while the mRNA expression levels of CCL2/11/13/16/17/19/23/24/25/28 were down-regulated. The chemokine significantly associated with the pathological stage of gastric cancer is CCL2/11/19/21. In gastric cancer, the expression level of CCL chemokines was not associated with disease-free survival, but low expression of CCL14 was significantly associated with longer overall survival. Therein, associated with the regulation of CCL chemokines are only 10 transcription factors (RELA, NFKB1, STAT6, IRF3, REL, SPI1, STAT1, STAT3, JUN and SP1). The major biological process and functional enrichment of CCL chemokines are to induce cell-directed migration.

Conclusion

These results may indicate that CCL chemokines may be immunotherapeutic targets and promising prognostic biomarkers for gastric cancer.

Loading

Article metrics loading...

/content/journals/cmc/10.2174/0109298673315146240731100101
2023-08-09
2024-11-14
Loading full text...

Full text loading...

References

  1. YeohK.G. TanP. Mapping the genomic diaspora of gastric cancer.Nat. Rev. Cancer2022222718410.1038/s41568‑021‑00412‑734702982
    [Google Scholar]
  2. CaoT. ZhangW. WangQ. WangC. MaW. ZhangC. GeM. TianM. YuJ. JiaoA. WangL. LiuM. WangP. GuoZ. ZhouY. ChenS. YinW. YiJ. GuoH. HanH. ZhangB. WuK. FanD. WangX. NieY. LuY. ZhaoX. Cancer SLC6A6-mediated taurine uptake transactivates immune checkpoint genes and induces exhaustion in CD8+ T cells.Cell2024187922882304.e2710.1016/j.cell.2024.03.01138565142
    [Google Scholar]
  3. WangJ. ZhangJ. LiuH. MengL. GaoX. ZhaoY. WangC. GaoX. FanA. CaoT. FanD. ZhaoX. LuY. N6-methyladenosine reader hnRNPA2B1 recognizes and stabilizes NEAT1 to confer chemoresistance in gastric cancer.Cancer Commun.202444446949010.1002/cac2.1253438512764
    [Google Scholar]
  4. ChenY. WangB. ZhaoY. ShaoX. WangM. MaF. YangL. NieM. JinP. YaoK. SongH. LouS. WangH. YangT. TianY. HanP. HuZ. Metabolomic machine learning predictor for diagnosis and prognosis of gastric cancer.Nat. Commun.2024151165710.1038/s41467‑024‑46043‑y38395893
    [Google Scholar]
  5. WongM.C.S. HuangJ. ChanP.S.F. ChoiP. LaoX.Q. ChanS.M. TeohA. LiangP. Global incidence and mortality of gastric cancer, 1980-2018.JAMA Netw. Open202147e211845710.1001/jamanetworkopen.2021.1845734309666
    [Google Scholar]
  6. ZengY. JinR.U. Molecular pathogenesis, targeted therapies, and future perspectives for gastric cancer.Semin. Cancer Biol.202286Pt 356658210.1016/j.semcancer.2021.12.00434933124
    [Google Scholar]
  7. FatehullahA. TerakadoY. SagirajuS. TanT.L. ShengT. TanS.H. MurakamiK. SwathiY. AngN. RajarethinamR. MingT. TanP. LeeB. BarkerN. A tumour-resident Lgr5+ stem-cell-like pool drives the establishment and progression of advanced gastric cancers.Nat. Cell Biol.202123121299131310.1038/s41556‑021‑00793‑934857912
    [Google Scholar]
  8. NeguraI. Pavel-TanasaM. DanciuM. Regulatory T cells in gastric cancer: Key controllers from pathogenesis to therapy.Cancer Treat. Rev.202312010262910.1016/j.ctrv.2023.10262937769435
    [Google Scholar]
  9. KuangZ.Y. SunQ.H. CaoL.C. MaX.Y. WangJ.X. LiuK.X. LiJ. Efficacy and safety of perioperative therapy for locally resectable gastric cancer: A network meta-analysis of randomized clinical trials.World J. Gastrointest. Oncol.20241631046105810.4251/wjgo.v16.i3.104638577462
    [Google Scholar]
  10. SextonR.E. Al HallakM.N. DiabM. AzmiA.S. Gastric cancer: a comprehensive review of current and future treatment strategies.Cancer Metastasis Rev.20203941179120310.1007/s10555‑020‑09925‑332894370
    [Google Scholar]
  11. ChristodoulidisG. KoumarelasK.E. KouliouM.N. Revolutionizing gastric cancer treatment: The potential of immunotherapy.World J. Gastroenterol.202430428628910.3748/wjg.v30.i4.28638313231
    [Google Scholar]
  12. SongY. WangJ. SunJ. ChenX. ShiJ. WuZ. YuD. ZhangF. WangZ. Screening of potential biomarkers for gastric cancer with diagnostic value using label-free global proteome analysis.Genomics Proteomics Bioinformatics202018667969510.1016/j.gpb.2020.06.01233607292
    [Google Scholar]
  13. FerroA. PeleteiroB. MalvezziM. BosettiC. BertuccioP. LeviF. NegriE. La VecchiaC. LunetN. Worldwide trends in gastric cancer mortality (1980–2011), with predictions to 2015, and incidence by subtype.Eur. J. Cancer20145071330134410.1016/j.ejca.2014.01.02924650579
    [Google Scholar]
  14. BrennerH. RothenbacherD. ArndtV. Epidemiology of stomach cancer.Methods Mol. Biol.200947246747710.1007/978‑1‑60327‑492‑0_2319107449
    [Google Scholar]
  15. SenchukovaM.A. Helicobacter pylori and gastric cancer progression.Curr. Microbiol.2022791238310.1007/s00284‑022‑03089‑936329283
    [Google Scholar]
  16. ThriftA.P. El-SeragH.B. Burden of gastric cancer.Clin. Gastroenterol. Hepatol.202018353454210.1016/j.cgh.2019.07.04531362118
    [Google Scholar]
  17. PanL. ShiY. ZhangJ. LuoG. Association between single nucleotide polymorphisms of mirnas and gastric cancer: a scoping review.Genet. Test. Mol. Biomarkers2022261045946710.1089/gtmb.2021.025836251855
    [Google Scholar]
  18. ChengJ. CaiM. ShuaiX. GaoJ. WangG. TaoK. First-line systemic therapy for advanced gastric cancer: a systematic review and network meta-analysis.Ther. Adv. Med. Oncol.201911p. 175883591987772610.1177/175883591987772631632469
    [Google Scholar]
  19. JainU. SaxenaK. ChauhanN. Helicobacter pylori induced reactive oxygen Species: A new and developing platform for detection.Helicobacter2021263e1279610.1111/hel.1279633666321
    [Google Scholar]
  20. WeiL. SunJ. ZhangN. ZhengY. WangX. LvL. LiuJ. XuY. ShenY. YangM. Noncoding RNAs in gastric cancer: implications for drug resistance.Mol. Cancer20201916210.1186/s12943‑020‑01185‑732192494
    [Google Scholar]
  21. ZhaoA.J. QianY.Y. SunH. HouX. PanJ. LiuX. ZhouW. ChenY.Z. JiangX. LiZ.S. LiaoZ. Screening for gastric cancer with magnetically controlled capsule gastroscopy in asymptomatic individuals.Gastrointest. Endosc.2018883466474.e110.1016/j.gie.2018.05.00329753039
    [Google Scholar]
  22. TanH. ZhangS. ZhangJ. ZhuL. ChenY. YangH. ChenY. AnY. LiuB. Long non-coding RNAs in gastric cancer: New emerging biological functions and therapeutic implications.Theranostics202010198880890210.7150/thno.4754832754285
    [Google Scholar]
  23. JinG. ZhangJ. CaoT. ChenB. TianY. ShiY. Exosome-mediated lncRNA SND1-IT1 from gastric cancer cells enhances malignant transformation of gastric mucosa cells via up-regulating SNAIL1.J. Transl. Med.202220128410.1186/s12967‑022‑03306‑w35739527
    [Google Scholar]
  24. YouL. DouY. ZhangY. XiaoH. LvH. WeiG.H. XuD. SDC2 stabilization by USP14 promotes gastric cancer progression through co-option of PDK1.Int. J. Biol. Sci.202319113483349810.7150/ijbs.8433137496999
    [Google Scholar]
  25. LavyR. KapievA. PolukshtN. HalevyA. Keinan-BokerL. Incidence trends and mortality rates of gastric cancer in Israel.Gastric Cancer201316212112510.1007/s10120‑012‑0155‑422527183
    [Google Scholar]
  26. MachlowskaJ. BajJ. SitarzM. MaciejewskiR. SitarzR. Gastric cancer: Epidemiology, risk factors, classification, genomic characteristics and treatment strategies.Int. J. Mol. Sci.20202111401210.3390/ijms2111401232512697
    [Google Scholar]
  27. LiangZ. XuY. ZhangY. ZhangX. SongJ. JinJ. QianH. Anticancer applications of phytochemicals in gastric cancer: Effects and molecular mechanism.Front. Pharmacol.202313107809010.3389/fphar.2022.107809036712679
    [Google Scholar]
  28. ShenX. ZhaoK. XuL. ChengG. ZhuJ. GanL. WuY. ZhuangZ. YTHDF2 inhibits gastric cancer cell growth by regulating FOXC2 signaling pathway.Front. Genet.20211159204210.3389/fgene.2020.59204233505426
    [Google Scholar]
  29. ZhangY. ZhouX. ChengX. HongX. JiangX. JingG. ChenK. LiY. PRKAA1, stabilized by FTO in an m6A-YTHDF2-dependent manner, promotes cell proliferation and glycolysis of gastric cancer by regulating the redox balance.Neoplasma20226961338134810.4149/neo_2022_220714N71436305690
    [Google Scholar]
  30. ChenJ. RöckenC. MalfertheinerP. EbertM.P.A. Recent advances in molecular diagnosis and therapy of gastric cancer.Dig. Dis.200422438038510.1159/00008360215812163
    [Google Scholar]
  31. YaoF.Z. KongD.G. Identification of kinesin family member 3B (KIF3B) as a molecular target for gastric cancer.Kaohsiung J. Med. Sci.202036751552210.1002/kjm2.1220632237034
    [Google Scholar]
  32. TanZ. Recent advances in the surgical treatment of advanced gastric cancer: A review.Med. Sci. Monit.2019253537354110.12659/MSM.91647531080234
    [Google Scholar]
  33. CaiX. DengJ. MingQ. CaiH. ChenZ. Chemokine- like factor 1: A promising therapeutic target in human diseases.Exp. Biol. Med.2020245161518152810.1177/153537022094522532715782
    [Google Scholar]
  34. LaurenceA.D.J. Location, movement and survival: the role of chemokines in haematopoiesis and malignancy.Br. J. Haematol.2006132325526710.1111/j.1365‑2141.2005.05841.x16409290
    [Google Scholar]
  35. RosteneW. BuckinghamJ.C. Chemokines as modulators of neuroendocrine functions.J. Mol. Endocrinol.200738335135310.1677/JME‑07‑000617339397
    [Google Scholar]
  36. NagarshethN. WichaM.S. ZouW. Chemokines in the cancer microenvironment and their relevance in cancer immunotherapy.Nat. Rev. Immunol.201717955957210.1038/nri.2017.4928555670
    [Google Scholar]
  37. MempelT.R. LillJ.K. AltenburgerL.M. How chemokines organize the tumour microenvironment.Nat. Rev. Cancer2024241285010.1038/s41568‑023‑00635‑w38066335
    [Google Scholar]
  38. BuleP. AguiarS.I. Aires-Da-SilvaF. DiasJ.N.R. Chemokine-directed tumor microenvironment modulation in cancer immunotherapy.Int. J. Mol. Sci.20212218980410.3390/ijms2218980434575965
    [Google Scholar]
  39. DiNataleA. CastelliM.S. NashB. MeucciO. FatatisA. Regulation of tumor and metastasis initiation by chemokine receptors.J. Cancer202213113160317610.7150/jca.7233136118530
    [Google Scholar]
  40. AllinenM. BeroukhimR. CaiL. BrennanC. Lahti- DomeniciJ. HuangH. PorterD. HuM. ChinL. RichardsonA. SchnittS. SellersW.R. PolyakK. Molecular characterization of the tumor microenvironment in breast cancer.Cancer Cell200461173210.1016/j.ccr.2004.06.01015261139
    [Google Scholar]
  41. JiaoX. ShuG. LiuH. ZhangQ. MaZ. RenC. GuoH. ShiJ. LiuJ. ZhangC. WangY. GaoY. The diagnostic value of chemokine/chemokine receptor pairs in hepatocellular carcinoma and colorectal liver metastasis.J. Histochem. Cytochem.201967529930810.1369/002215541882427430633620
    [Google Scholar]
  42. ReschkeR. GajewskiT.F. CXCL9 and CXCL10 bring the heat to tumors.Sci. Immunol.2022773eabq650910.1126/sciimmunol.abq650935867802
    [Google Scholar]
  43. StrieterR.M. PolveriniP.J. ArenbergD.A. KunkelS.L. The role of CXC chemokines as regulators of angiogenesis.Shock19954315516010.1097/00024382‑199509000‑000018574748
    [Google Scholar]
  44. JiS. ChenH. YangK. ZhangG. MaoB. HuY. ZhangH. XuJ. Peripheral cytokine levels as predictive biomarkers of benefit from immune checkpoint inhibitors in cancer therapy.Biomed. Pharmacother.202012911045710.1016/j.biopha.2020.11045732887027
    [Google Scholar]
  45. ZhangM. YangW. WangP. DengY. DongY.T. LiuF.F. HuangR. ZhangP. DuanY.Q. LiuX.D. LinD. ChuQ. ZhongB. CCL7 recruits cDC1 to promote antitumor immunity and facilitate checkpoint immunotherapy to non-small cell lung cancer.Nat. Commun.2020111611910.1038/s41467‑020‑19973‑633257678
    [Google Scholar]
  46. WuZ. SunL. XuY. HuangH. WuZ. QiuB. YanJ. YinX. The value of chemokine and chemokine receptors in diagnosis, prognosis, and immunotherapy of hepatocellular carcinoma.Cancer Manag. Res.20241640342010.2147/CMAR.S45095938736589
    [Google Scholar]
  47. VautrotV. BentayebH. CausseS. GarridoC. GobboJ. Tumor-derived exosomes: Hidden players in PD-1/PD-L1 resistance.Cancers20211318453710.3390/cancers1318453734572764
    [Google Scholar]
  48. TangZ. LiC. KangB. GaoG. LiC. ZhangZ. GEPIA: a web server for cancer and normal gene expression profiling and interactive analyses.Nucleic Acids Res.201745W1W98W10210.1093/nar/gkx24728407145
    [Google Scholar]
  49. ChandrashekarD.S. BashelB. BalasubramanyaS.A.H. CreightonC.J. Ponce-RodriguezI. ChakravarthiB.V. S.K. VaramballyS. UALCAN: A portal for facilitating tumor subgroup gene expression and survival analyses.Neoplasia201719864965810.1016/j.neo.2017.05.00228732212
    [Google Scholar]
  50. ChandrashekarD.S. KarthikeyanS.K. KorlaP.K. PatelH. ShovonA.R. AtharM. NettoG.J. QinZ.S. KumarS. ManneU. CreightonC.J. VaramballyS. UALCAN: An update to the integrated cancer data analysis platform.Neoplasia202225182710.1016/j.neo.2022.01.00135078134
    [Google Scholar]
  51. CeramiE. GaoJ. DogrusozU. GrossB.E. SumerS.O. AksoyB.A. JacobsenA. ByrneC.J. HeuerM.L. LarssonE. AntipinY. RevaB. GoldbergA.P. SanderC. SchultzN. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data.Cancer Discov.20122540140410.1158/2159‑8290.CD‑12‑009522588877
    [Google Scholar]
  52. GaoJ. AksoyB.A. DogrusozU. DresdnerG. GrossB. SumerS.O. SunY. JacobsenA. SinhaR. LarssonE. CeramiE. SanderC. SchultzN. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal.Sci. Signal.20136269pl110.1126/scisignal.200408823550210
    [Google Scholar]
  53. Warde-FarleyD. DonaldsonSL. ComesO. ZuberiK. BadrawiR. ChaoP. FranzM. GrouiosC. KaziF. LopesCT. The GeneMANIA prediction server: biological network integration for gene prioritization and predicting gene function.Nucleic Acids Res201038W214W22010.1093/nar/gkq537
    [Google Scholar]
  54. FranzM. RodriguezH. LopesC. ZuberiK. MontojoJ. BaderG.D. MorrisQ. GeneMANIA update 2018.Nucleic Acids Res.201846W1W60W6410.1093/nar/gky31129912392
    [Google Scholar]
  55. MontojoJ. ZuberiK. RodriguezH. KaziF. WrightG. DonaldsonS.L. MorrisQ. BaderG.D. GeneMANIA Cytoscape plugin: fast gene function predictions on the desktop.Bioinformatics201026222927292810.1093/bioinformatics/btq56220926419
    [Google Scholar]
  56. ZuberiK. FranzM. RodriguezH. MontojoJ. LopesCT. BaderGD. MorrisQ. GeneMANIA prediction server 2013 update.Nucleic Acids Res201341W115W12210.1093/nar/gkt533
    [Google Scholar]
  57. SzklarczykD. GableA.L. LyonD. JungeA. WyderS. Huerta-CepasJ. SimonovicM. DonchevaN.T. MorrisJ.H. BorkP. JensenL.J. MeringC. STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets.Nucleic Acids Res.201947D1D607D61310.1093/nar/gky113130476243
    [Google Scholar]
  58. HanH. ChoJ.W. LeeS. YunA. KimH. BaeD. YangS. KimC.Y. LeeM. KimE. LeeS. KangB. JeongD. KimY. JeonH.N. JungH. NamS. ChungM. KimJ.H. LeeI. TRRUST v2: an expanded reference database of human and mouse transcriptional regulatory interactions.Nucleic Acids Res.201846D1D380D38610.1093/nar/gkx101329087512
    [Google Scholar]
  59. HanH. ShimH. ShinD. ShimJ.E. KoY. ShinJ. KimH. ChoA. KimE. LeeT. KimH. KimK. YangS. BaeD. YunA. KimS. KimC.Y. ChoH.J. KangB. ShinS. LeeI. TRRUST: a reference database of human transcriptional regulatory interactions.Sci. Rep.2015511143210.1038/srep1143226066708
    [Google Scholar]
  60. ZhouY. ZhouB. PacheL. ChangM. KhodabakhshiA.H. TanaseichukO. BennerC. ChandaS.K. Metascape provides a biologist-oriented resource for the analysis of systems-level datasets.Nat. Commun.2019101152310.1038/s41467‑019‑09234‑630944313
    [Google Scholar]
  61. ChenD. FuM. ChiL. LinL. ChengJ. XueW. LongC. JiangW. DongX. SuiJ. LinD. LuJ. ZhuoS. LiuS. LiG. ChenG. YanJ. Prognostic and predictive value of a pathomics signature in gastric cancer.Nat. Commun.2022131690310.1038/s41467‑022‑34703‑w36371443
    [Google Scholar]
  62. ChenK. BaoZ. TangP. GongW. YoshimuraT. WangJ.M. Chemokines in homeostasis and diseases.Cell. Mol. Immunol.201815432433410.1038/cmi.2017.13429375126
    [Google Scholar]
  63. MarcuzziE. AngioniR. MolonB. CalìB. Chemokines and chemokine receptors: orchestrating tumor metastasization.Int. J. Mol. Sci.20182019610.3390/ijms2001009630591657
    [Google Scholar]
  64. Baj-KrzyworzekaM. WęglarczykK. BaranJ. SzczepanikA. SzuraM. SiedlarM. Elevated level of some chemokines in plasma of gastric cancer patients.Cent. Eur. J. Immunol.20164435836210.5114/ceji.2016.6513328450798
    [Google Scholar]
  65. ZhangJ. YanY. CuiX. ZhangJ. YangY. LiH. WuH. LiJ. WangL. LiM. LiuX. WangJ. DuanX. CCL2 expression correlates with Snail expression and affects the prognosis of patients with gastric cancer.Pathol. Res. Pract.2017213321722110.1016/j.prp.2016.12.01328215642
    [Google Scholar]
  66. HwangT.L. LeeL.Y. WangC.C. LiangY. HuangS.F. WuC.M. CCL7 and CCL21 overexpression in gastric cancer is associated with lymph node metastasis and poor prognosis.World J. Gastroenterol.201218111249125610.3748/wjg.v18.i11.124922468089
    [Google Scholar]
  67. JinG. LvJ. YangM. WangM. ZhuM. WangT. YanC. YuC. DingY. LiG. RenC. NiJ. ZhangR. GuoY. BianZ. ZhengY. ZhangN. JiangY. ChenJ. WangY. XuD. ZhengH. YangL. ChenY. WaltersR. MillwoodI.Y. DaiJ. MaH. ChenK. ChenZ. HuZ. WeiQ. ShenH. LiL. Genetic risk, incident gastric cancer, and healthy lifestyle: a meta-analysis of genome-wide association studies and prospective cohort study.Lancet Oncol.202021101378138610.1016/S1470‑2045(20)30460‑533002439
    [Google Scholar]
  68. RustgiS.D. ChingC.K. KastrinosF. Inherited predisposition to gastric cancer.Gastrointest. Endosc. Clin. N. Am.202131346748710.1016/j.giec.2021.03.01034053634
    [Google Scholar]
  69. HanJ. FuR. ChenC. ChengX. GuoT. HuangfuL. LiX. DuH. XingX. JiJ. CXCL16 promotes gastric cancer tumorigenesis via ADAM10-dependent CXCL16/CXCR6 axis and activates Akt and MAPK signaling pathways: erratum.Int. J. Biol. Sci.202319103285328710.7150/ijbs.8434237416762
    [Google Scholar]
  70. LowJ.T. ChristieM. ErnstM. DumoutierL. PreaudetA. NiY. GriffinM.D.W. MielkeL.A. StrasserA. PutoczkiT.L. O’ReillyL.A. Loss of NFKB1 results in expression of tumor necrosis factor and activation of signal transducer and activator of transcription 1 to promote gastric tumorigenesis in mice.Gastroenterology2020159414441458.e1510.1053/j.gastro.2020.06.03932569771
    [Google Scholar]
  71. LiD. WuC. CaiY. LiuB. Association of NFKB1 and NFKBIA gene polymorphisms with susceptibility of gastric cancer.Tumour Biol.201739710.1177/101042831771710728670959
    [Google Scholar]
  72. ChenY. LuR. ZhengH. XiaoR. FengJ. WangH. GaoX. GuoL. The NFKB1 polymorphism (rs4648068) is associated with the cell proliferation and motility in gastric cancer.BMC Gastroenterol.20151512110.1186/s12876‑015‑0243‑025888547
    [Google Scholar]
  73. DengJ.Y. SunD. LiuX.Y. PanY. LiangH. STAT-3 correlates with lymph node metastasis and cell survival in gastric cancer.World J. Gastroenterol.201016425380538710.3748/wjg.v16.i42.538021072904
    [Google Scholar]
  74. LuG. ShiW. ZhengH. Inhibition of STAT6/anoctamin-1 activation suppresses proliferation and invasion of gastric cancer cells.Cancer Biother. Radiopharm.20183313710.1089/cbr.2017.228729466035
    [Google Scholar]
  75. JiaoS. GuanJ. ChenM. WangW. LiC. WangY. ChengY. ZhouZ. Targeting IRF3 as a YAP agonist therapy against gastric cancer.J. Exp. Med.2018215269971810.1084/jem.2017111629339449
    [Google Scholar]
  76. MatsuoK. YoshieO. NakayamaT. Multifaceted roles of chemokines and chemokine receptors in tumor immunity.Cancers (Basel)20211323613210.3390/cancers1323613234885241
    [Google Scholar]
  77. OzgaA.J. ChowM.T. LusterA.D. Chemokines and the immune response to cancer.Immunity202154585987410.1016/j.immuni.2021.01.01233838745
    [Google Scholar]
  78. ProttiM.P. MonteL.D. LulloG.D. Tumor antigen-specific CD4+ T cells in cancer immunity: from antigen identification to tumor prognosis and development of therapeutic strategies.Tissue Antigens201483423724610.1111/tan.1232924641502
    [Google Scholar]
  79. QianB.Z. PollardJ.W. Macrophage diversity enhances tumor progression and metastasis.Cell20101411395110.1016/j.cell.2010.03.01420371344
    [Google Scholar]
/content/journals/cmc/10.2174/0109298673315146240731100101
Loading
/content/journals/cmc/10.2174/0109298673315146240731100101
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