Intratumoral regulatory T cells with higher prevalence and more suppressive activity in hepatocellular carcinoma patients

Journal of Gastroenterology and Hepatology (Australia)

Volumn 28, Issue 9, 2013, Pages 1555-1564

  Wu, Han ^a,c   Chen, Pei ^a   Liao, Rui ^a   Li, Yi Wei ^a   Yi, Yong ^a   Wang, Jia Xing ^a   Cai, Xiao Yan ^a   He, Hong Wei ^a   Jin, Jian Jun ^a   Cheng, Yun Feng ^a   Fan, Jia ^a,b   Sun, Jian ^a   Qiu, Shuang Jian ^a,b  

^a FUDAN UNIVERSITY   (China)

^b BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^c NANTONG UNIVERSITY   (China)

Author keywords

Gene microarray; Hepatocellular carcinoma; Immunosuppression; Regulatory T cell; Tumor immuno escape

Indexed keywords

ALPHA4 INTEGRIN; GLYCOSYLPHOSPHATIDYLINOSITOL; PROTEIN P53;

ADULT; ARTICLE; BIOSYNTHESIS; BLOOD; CD4+ CD25+ T LYMPHOCYTE; COMPLEMENT ACTIVATION; CONTROLLED STUDY; DNA MICROARRAY; DOWN REGULATION; FEMALE; FLOW CYTOMETRY; GENOME; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOSUPPRESSIVE TREATMENT; IMMUNOTHERAPY; IN VITRO STUDY; LIVER CELL CARCINOMA; MAJOR CLINICAL STUDY; MALE; PHENOTYPE; PREVALENCE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY T LYMPHOCYTE; SALIVATION;

GENE MICROARRAY; HEPATOCELLULAR CARCINOMA; IMMUNOSUPPRESSION; REGULATORY T CELL; TUMOR IMMUNO-ESCAPE;

ADULT; ANTIGENS, SURFACE; B-LYMPHOCYTE SUBSETS; CARCINOMA, HEPATOCELLULAR; CASE-CONTROL STUDIES; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNE TOLERANCE; IMMUNOPHENOTYPING; LIVER NEOPLASMS; LYMPHOCYTES, TUMOR-INFILTRATING; MALE; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; T-LYMPHOCYTES, REGULATORY; TUMOR ESCAPE;

EID: 84897584004     PISSN: 08159319     EISSN: 14401746     Source Type: Journal    
DOI: 10.1111/jgh.12202     Document Type: Article

References (46)

1. Ostrand-Rosenberg S. Immune surveillance: a balance between protumor and antitumor immunity. Curr. Opin. Genet. Dev. 2008; 18: 11-18.
2. Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 2011; 331: 1565-1570.
3. Croci DO, Zacarias Fluck MF, Rico MJ etal. Dynamic cross-talk between tumor and immune cells in orchestrating the immunosuppressive network at the tumor microenvironment. Cancer Immunol. Immunother. 2007; 56: 1687-1700.
4. Quezada SA, Peggs KS, Simpson TR, Allison JP. Shifting the equilibrium in cancer immunoediting: from tumor tolerance to eradication. Immunol. Rev. 2011; 241: 104-118.
5. Gao Q, Qiu SJ, Fan J etal. Intratumoral balance of regulatory and cytotoxic T cells is associated with prognosis of hepatocellular carcinoma after resection. J. Clin. Oncol. 2007; 25: 2586-2593.
6. Zhu XD, Zhang JB, Zhuang PY etal. High expression of macrophage colony-stimulating factor in peritumoral liver tissue is associated with poor survival after curative resection of hepatocellular carcinoma. J. Clin. Oncol. 2008; 26: 2707-2716.
7. Ju MJ, Qiu SJ, Fan J etal. Peritumoral activated hepatic stellate cells predict poor clinical outcome in hepatocellular carcinoma after curative resection. Am. J. Clin. Pathol. 2009; 131: 498-510.
8. Li YW, Qiu SJ, Fan J etal. Intratumoral neutrophils: a poor prognostic factor for hepatocellular carcinoma following resection. J. Hepatol. 2011; 54: 497-505.
9. Ju MJ, Qiu SJ, Gao Q etal. Combination of peritumoral mast cells and T-regulatory cells predicts prognosis of hepatocellular carcinoma. Cancer Sci. 2009; 100: 1267-1274.
10. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 1995; 155: 1151-1164.
11. Zou W. Regulatory T cells, tumour immunity and immunotherapy. Nat. Rev. Immunol. 2006; 6: 295-307.
12. + T cells secreting interleukin-10 and transforming growth factor-beta1 mediates suppression in the tumor microenvironment. Clin. Cancer Res. 2007; 13: 4345-4354.
13. Curiel TJ, Coukos G, Zou L etal. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med. 2004; 10: 942-949.
14. Mizukami Y, Kono K, Kawaguchi Y etal. Localisation pattern of Foxp3+ regulatory T cells is associated with clinical behaviour in gastric cancer. Br. J. Cancer 2008; 98: 148-153.
15. Gobert M, Treilleux I, Bendriss-Vermare N etal. Regulatory T cells recruited through CCL22/CCR4 are selectively activated in lymphoid infiltrates surrounding primary breast tumors and lead to an adverse clinical outcome. Cancer Res. 2009; 69: 2000-2009.
16. Deng L, Zhang H, Luan Y etal. Accumulation of foxp3+ T regulatory cells in draining lymph nodes correlates with disease progression and immune suppression in colorectal cancer patients. Clin. Cancer Res. 2010; 16: 4105-4112.
17. Salama P, Phillips M, Grieu F etal. Tumor-infiltrating FOXP3+ T regulatory cells show strong prognostic significance in colorectal cancer. J. Clin. Oncol. 2009; 27: 186-192.
18. Gao Q, Wang XY, Qiu SJ etal. Overexpression of PD-L1 significantly associates with tumor aggressiveness and postoperative recurrence in human hepatocellular carcinoma. Clin. Cancer Res. 2009; 15: 971-979.
19. + T reg cells. J. Exp. Med. 2006; 203: 1701-1711.
20. Unitt E, Rushbrook SM, Marshall A etal. Compromised lymphocytes infiltrate hepatocellular carcinoma: the role of T-regulatory cells. Hepatology 2005; 41: 722-730.
21. Ruitenberg JJ, Boyce C, Hingorani R, Putnam A, Ghanekar SA. Rapid assessment of in vitro expanded human regulatory T cell function. J. Immunol. Methods 2011; 372: 95-106.
22. Ashburner M, Ball CA, Blake JA etal. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 2000; 25: 25-29.
23. Bonnet A, Lagarrigue S, Liaubet L, Robert-Granie C, Sancristobal M, Tosser-Klopp G. Pathway results from the chicken data set using GOTM, Pathway Studio and Ingenuity softwares. BMC Proc. 2009; 3 (Suppl. 4): S11.
24. Bach JF. Regulatory T cells under scrutiny. Nat. Rev. Immunol. 2003; 3: 189-198.
25. Shevach EM. Certified professionals: CD4(+)CD25(+) suppressor T cells. J. Exp. Med. 2001; 193: F41-46.
26. Frentsch M, Arbach O, Kirchhoff D etal. Direct access to CD4+ T cells specific for defined antigens according to CD154 expression. Nat. Med. 2005; 11: 1118-1124.
27. Chattopadhyay PK, Yu J, Roederer M. A live-cell assay to detect antigen-specific CD4+ T cells with diverse cytokine profiles. Nat. Med. 2005; 11: 1113-1117.
28. Yang XH, Yamagiwa S, Ichida T etal. Increase of CD4+ CD25+ regulatory T-cells in the liver of patients with hepatocellular carcinoma. J. Hepatol. 2006; 45: 254-262.
29. Shen X, Li N, Li H, Zhang T, Wang F, Li Q. Increased prevalence of regulatory T cells in the tumor microenvironment and its correlation with TNM stage of hepatocellular carcinoma. J. Cancer Res. Clin. Oncol. 2010; 136: 1745-1754.
30. Kemper C, Verbsky JW, Price JD, Atkinson JP. T-cell stimulation and regulation: with complements from CD46. Immunol. Res. 2005; 32: 31-43.
31. Kemper C, Chan AC, Green JM, Brett KA, Murphy KM, Atkinson JP. Activation of human CD4+ cells with CD3 and CD46 induces a T-regulatory cell 1 phenotype. Nature 2003; 421: 388-392.
32. Truscott SM, Abate G, Price JD, Kemper C, Atkinson JP, Hoft DF. CD46 engagement on human CD4+ T cells produces T regulatory type 1-like regulation of antimycobacterial T cell responses. Infect. Immun. 2010; 78: 5295-5306.
33. Toledo F, Wahl GM. MDM2 and MDM4: p53 regulators as targets in anticancer therapy. Int. J. Biochem. Cell Biol. 2007; 39: 1476-1482.
34. Singh N, Yamamoto M, Takami M etal. CD4(+)CD25(+) regulatory T cells resist a novel form of CD28- and Fas-dependent p53-induced T cell apoptosis. J. Immunol. 2010; 184: 94-104.
35. Jenner J, Kerst G, Handgretinger R, Muller I. Increased alpha2, 6-sialylation of surface proteins on tolerogenic, immature dendritic cells and regulatory T cells. Exp. Hematol. 2006; 34: 1212-1218.
36. Long ET, Baker S, Oliveira V, Sawitzki B, Wood KJ. Alpha-1, 2-mannosidase and hence N-glycosylation are required for regulatory T cell migration and allograft tolerance in mice. PLoS ONE 2010; 5: e8894.
37. Staun-Ram E, Miller A. Cathepsins (S and B) and their inhibitor Cystatin C in immune cells: modulation by interferon-beta and role played in cell migration. J. Neuroimmunol. 2011; 232: 200-206.
38. Marmor MD, Julius M. The function of GPI-anchored proteins in T cell development, activation and regulation of homeostasis. J. Biol. Regul. Homeost. Agents 2000; 14: 99-115.
39. Loertscher R, Lavery P. The role of glycosyl phosphatidyl inositol (GPI)-anchored cell surface proteins in T-cell activation. Transpl. Immunol. 2002; 9: 93-96.
40. Liu D, Zhang T, Marshall AJ, Okkenhaug K, Vanhaesebroeck B, Uzonna JE. The p110delta isoform of phosphatidylinositol 3-kinase controls susceptibility to Leishmania major by regulating expansion and tissue homing of regulatory T cells. J. Immunol. 2009; 183: 1921-1933.
41. Ono M, Yaguchi H, Ohkura N etal. Foxp3 controls regulatory T-cell function by interacting with AML1/Runx1. Nature 2007; 446: 685-689.
42. Gandhi R, Kumar D, Burns EJ etal. Activation of the aryl hydrocarbon receptor induces human type 1 regulatory T cell-like and Foxp3(+) regulatory T cells. Nat. Immunol. 2010; 11: 846-853.
43. Hawiger D, Wan YY, Eynon EE, Flavell RA. The transcription cofactor Hopx is required for regulatory T cell function in dendritic cell-mediated peripheral T cell unresponsiveness. Nat. Immunol. 2010; 11: 962-968.
44. Sugimoto N, Oida T, Hirota K etal. Foxp3-dependent and -independent molecules specific for CD25+CD4+ natural regulatory T cells revealed by DNA microarray analysis. Int. Immunol. 2006; 18: 1197-1209.
45. Klein S, Kretz C, Krammer PH, Kuhn A. CD127low/- and FoxP3+expression levels characterize different regulatory T cell populations in human peripheral blood. J. Invest. Dermatol. 2010; 130: 492-499.
46. Kleinewietfeld M, Starke M, Di Mitri D etal. CD49d provides access to "untouched" human Foxp3+ Treg free of contaminating effector cells. Blood 2009; 113: 827-836.