Regulatory T cells are an important prognostic factor in breast cancer: A systematic review and meta-analysis

Neoplasma

Volumn 63, Issue 5, 2016, Pages 789-798

  Wang, Y ^a   Sun, J ^a   Zheng, R ^b   Shao, Q ^a   Gao, W ^a   Song, B ^a   Chen, X ^a   Qu, X ^a  

^a SHANDONG UNIVERSITY   (China)

^b TIANJIN MEDICAL UNIVERSITY   (China)

Author keywords

Breast cancer; Estrogen receptor status; Meta analysis; Prognosis; Regulatory t cells

Indexed keywords

ESTROGEN RECEPTOR; PROGESTERONE RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ERBB2 PROTEIN, HUMAN;

BREAST CANCER; DATA EXTRACTION; HUMAN; IMMUNOHISTOCHEMISTRY; LYMPH NODE METASTASIS; META ANALYSIS; MORTALITY RATE; OUTCOME ASSESSMENT; OVERALL SURVIVAL; PROGNOSIS; PROGRESSION FREE SURVIVAL; RECURRENT DISEASE; REGULATORY T LYMPHOCYTE; REVIEW; SENSITIVITY ANALYSIS; SYSTEMATIC REVIEW; BREAST TUMOR; CYTOLOGY; FEMALE; IMMUNOLOGY; LYMPHOCYTE COUNT; METABOLISM; MORTALITY; PATHOLOGY; TUMOR ASSOCIATED LEUKOCYTE; TUMOR RECURRENCE;

BREAST NEOPLASMS; FEMALE; HUMANS; LYMPHOCYTE COUNT; LYMPHOCYTES, TUMOR-INFILTRATING; NEOPLASM RECURRENCE, LOCAL; PROGNOSIS; PROGRESSION-FREE SURVIVAL; RECEPTOR, ERBB-2; RECEPTORS, ESTROGEN; RECEPTORS, PROGESTERONE; T-LYMPHOCYTES, REGULATORY;

EID: 84992391485     PISSN: 00282685     EISSN: 13384317     Source Type: Journal    
DOI: 10.4149/neo_2016_517     Document Type: Review

References (44)

1. SIEGEL RL,MILLER KD,JEMAL A. Cancer statistics,2015. CA Cancer J Clin 2015; 65: 5-29. http://dx.doi.org/10.3322/ caac.21254
2. MELLMAN I,COUKOS G,DRANOFF G. Cancer immunotherapy comes of age. Nature 2011; 480: 480-489. http://dx.doi.org/10.1038/nature10673
3. STANTON SE,DISIS ML. Designing vaccines to prevent breast cancer recurrence or invasive disease. Immunotherapy 2015; 7: 69-72. http://dx.doi.org/10.2217/imt.15.5
4. CONVIT J,MONTESINOS H,OVIEDO H,ROMERO G,MACCARONE B et al. Autologous tumor lysate/bacillus Calmette-Guerin immunotherapy as an adjuvant to conventional breast cancer therapy. Clin Transl Oncol 2015; 17: 884-887. http://dx.doi.org/10.1007/s12094-015-1320-0
5. SHEVACH EM. CD4+ CD25+ suppressor T cells: more questions than answers. Nat Rev Immunol 2002; 2: 389-400. doi: 10.1038/nri821.
6. LIOTTA LA,KOHN EC. The microenvironment of the tumour-host interface. Nature 2001; 411: 375-379. http://dx.doi.org/10.1038/35077241
7. LI H,FAN X,HOUGHTON J. Tumor microenvironment: the role of the tumor stroma in cancer. J Cell Biochem 2007; 101: 805-815. http://dx.doi.org/10.1002/jcb.21159
8. ZHAO HQ,LI WM,LU ZQ,YAO YM. Roles of Tregs in development of hepatocellular carcinoma: a meta-analysis. World J Gastroenterol 2014; 20: 7971-7978. http://dx.doi. org/10.3748/wjg.v20.i24.7971
9. HUANG Y,LIAO H,ZHANG Y,YUAN R,WANG F et al. Prognostic value of tumor-infiltrating FoxP3+ T cells in gastrointestinal cancers: a meta analysis. PLOS ONE 2014; 9: e94376. http://dx.doi.org/10.1371/journal. pone.0094376
10. DELEEUW RJ,KOST SE,KAKAL JA,NELSON BH. The prognostic value of FoxP3+ tumor-infiltrating lymphocytes in cancer: a critical review of the literature. Clin Cancer Res 2012; 18: 3022-3029. http://dx.doi.org/10.1158/1078-0432. CCR-11-3216
11. LADOIRE S,MARTIN F,GHIRINGHELLI F. Prognostic role of FOXP3+ regulatory T cells infiltrating human carcinomas: the paradox of colorectal cancer. Cancer Immunol Immunother 2011; 60: 909-918. http://dx.doi.org/10.1007/ s00262-011-1046-y
12. SALAMA P,PHILLIPS M,GRIEU F,MORRIS M,ZEPS N et al. Tumor-infiltrating FOXP3+ T regulatory cells show strong prognostic significance in colorectal cancer. J Clin Oncol 2009; 27: 186-192. http://dx.doi.org/10.1200/ JCO.2008.18.7229
13. KIM ST,JEONG H,WOO OH,SEO JH,KIM A et al. Tumor-infiltrating lymphocytes,tumor characteristics,and recurrence in patients wiThearly breast cancer. Am J Clin Oncol 2013; 36: 224-231. http://dx.doi.org/10.1097/ COC.0b013e3182467d90
14. MAEDA N,YOSHIMURA K,YAMAMOTO S,KURAMASU A,INOUE M et al. Expression of B7-H3,a potential factor of tumor immune evasion in combination with the number of regulatory T cells,affects against recurrence-free survival in breast cancer patients. Ann Surg Oncol 2014; 21 (Suppl 4): S546-S554. http://dx.doi.org/10.1245/s10434-014-3564-2
15. SEO AN,LEE HJ,KIM EJ,KIM HJ,JANG MH et al. Tumourinfiltrating CD8+ lymphocytes as an independent predictive factor for pathological complete response to primary systemic therapy in breast cancer. Br J Cancer 2013; 109: 2705-2713. http://dx.doi.org/10.1038/bjc.2013.634
16. BATES GJ,FOX SB,HAN C,LEEK RD,GARCIA JF et al. Quantification of regulatory T cells enables the identification of high-risk breast cancer patients and those at risk of late relapse. J Clin Oncol 2006; 24: 5373-5380. http://dx.doi. org/10.1200/JCO.2006.05.9584
17. GHEBEH H,BARHOUSH E,TULBAH A,ELKUM N,ALTWEIGERI T et al. FOXP3+ Tregs and B7-H1+/PD-1+ T lymphocytes co-infiltrate the tumor tissues of high-risk breast cancer patients: implication for immunotherapy. BMC Cancer 2008; 8: 57. http://dx.doi.org/10.1186/1471-2407-8-57
18. LIU F,LANG R,ZHAO J,ZHANG X,PRINGLE GA et al. CD8+ cytotoxic T cell and FOXP3+ regulatory T cell infiltration in relation to breast cancer survival and molecular subtypes. Breast Cancer Res Treat 2011; 130: 645-655. http://dx.doi.org/10.1007/s10549-011-1647-3
19. YAN M,JENE N,BYRNE D,MILLAR EK,O’TOOLE SA et al. Recruitment of regulatory T cells is correlated with hypoxia-induced CXCR4 expression,and is associated with poor prognosis in basal-like breast cancers. Breast Cancer Res 2011; 13: R47. http://dx.doi.org/10.1186/bcr2869
20. LIU S,FOULKES WD,LEUNG S,GAO D,LAU S et al. Prognostic significance of FOXP3+ tumor-infiltrating lymphocytes in breast cancer depends on estrogen receptor and human epidermal growth factor receptor-2 expression status and concurrent cytotoxic T-cell infiltration. Breast Cancer Res 2014; 16: 432. http://dx.doi.org/10.1186/s13058-014-0432-8
21. HAYES DF,BAST RC,DESCH CE,FRITSCHE HJR,KEMENY NE et al. Tumor marker utility grading system: a framework to evaluate clinical utility of tumor markers. J Natl Cancer Inst 1996; 88: 1456-1466. http://dx.doi. org/10.1093/jnci/88.20.1456
22. MCSHANE LM,ALTMAN DG,SAUERBREI W,TAUBE SE,GION M et al. REporting recommendations for tumour MARKer prognostic studies (REMARK). Br J Cancer 2005; 93: 387-391. http://dx.doi.org/10.1038/sj.bjc.6602678
23. WEST NR,KOST SE,MARTIN SD,MILNE K,DELEEUW RJ et al. Tumour-infiltrating FOXP3(+) lymphocytes are associated with cytotoxic immune responses and good clinical outcome in oestrogen receptor-negative breast cancer. Br J Cancer 2013; 108: 155-162. http://dx.doi.org/10.1038/ bjc.2012.524
24. HIGGINS JP,THOMPSON SG. Quantifying heterogeneity in a meta-analysis. Statist Med 2002; 21: 1539-1558. http://dx.doi.org/10.1002/sim.1186
25. ARUGA T,SUZUKI E,SAJI S,HORIGUCHI S,HORIGUCHI K et al. A low number of tumor-infiltrating FOXP3-positive cells during primary systemic chemotherapy correlates with favorable anti-tumor response in patients with breast cancer. Oncol Rep 2009; 22: 273-278. http://dx.doi.org/10.3892/ or_00000434
26. GOBERT M,TREILLEUX I,BENDRISS-VERMARE N,BACHELOT T,GODDARD-LEON S et al. 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. http://dx.doi.org/10.1158/0008-5472.CAN-08-2360
27. DE KRUIJF EM,VAN NES JGH,SAJET A,TUMMERS QRJG,PUTTER H et al. The predictive value of HLA class I tumor cell expression and presence of intratumoral Tregs for chemotherapy in patients wiThearly breast cancer. Clin Cancer Res 2010; 16: 1272-1280. http://dx.doi. org/10.1158/1078-0432.CCR-09-1844
28. MAHMOUD SM,PAISH EC,POWE DG,MACMILLAN RD,LEE AH et al. An evaluation of the clinical significance of FOXP3+ infiltrating cells in human breast cancer. Breast Cancer Res Treat 2011; 127: 99-108. http://dx.doi.org/10.1007/ s10549-010-0987-8
29. MA C,ZHANG Q,YE J,WANG F,ZHANG Y et al. Tumorinfiltrating gamma delta T lymphocytes predict clinical outcome in human breast cancer. J Immunol 2012; 189: 5029-5036. http://dx.doi.org/10.4049/jimmunol.1201892
30. DEMIR L,YIGIT S,ELLIDOKUZ H,ERTEN C,SOMALI I et al. Predictive and prognostic factors in locally advanced breast cancer: effect of intratumoral FOXP3+ Tregs. Clin Exp Metastasis 2013; 30: 1047-1062. http://dx.doi.org/10.1007/ s10585-013-9602-9
31. TAKENAKA M,SEKI N,TOH U,HATTORI S,KAWAHARA A. FOXP3 expression in tumor cells and tumor-infiltrating lymphocytes is associated with breast cancer prognosis. Molecular and Clinical Oncology 2013; 1: 625-632. http://dx.doi. org/10.3892/mco.2013.107
32. WON KY,KIM HS,SUNG JY,KIM GY,LEE J et al. Tumoral FOXP3 has potential oncogenic function in conjunction with the p53 tumor suppressor protein and infiltrated Tregs in human breast carcinomas. Pathol Res Pract 2013; 209: 767-773. http://dx.doi.org/10.1016/j.prp.2013.08.010
33. SUN S,FEI X,MAO Y,WANG X,GARFIELD DH et al. PD-1(+) immune cell infiltration inversely correlates with survival of operable breast cancer patients. Cancer Immunol Immunother 2014; 63: 395-406. http://dx.doi.org/10.1007/ s00262-014-1519-x
34. NISHIKAWA H,SAKAGUCHI S. Regulatory T cells in tumor immunity. Int J Cancer 2010; 127: 759-767. http://dx.doi. org/10.1002/ijc.25429
35. LEHE C,GHEBEH H,AL-SULAIMAN A,AL QUDAIHI G,AL-HUSSEIN K et al. The Wilms’ tumor antigen is a novel target for human CD4+ regulatory T cells: implications for immunotherapy. Cancer Res 2008; 68: 6350-6359. http://dx.doi.org/10.1158/0008-5472.CAN-08-0050
36. FACCIABENE A,PENG X,HAGEMANN IS,BALINT K,BARCHETTI A et al. Tumour hypoxia promotes tolerance and angiogenesis via CCL28 and T(reg) cells. Nature 2011; 475: 226-230. http://dx.doi.org/10.1038/nature10169
37. TAN W,ZHANG W,STRASNER A,GRIVENNIKOV S,CHENG JQ et al. Tumour-infiltrating regulatory T cells stimulate mammary cancer metastasis through RANKLRANK signalling. Nature 2011; 470: 548-553. http://dx.doi. org/10.1038/nature09707
38. CURIEL TJ,COUKOS G,ZOU L,ALVAREZ X,CHENG P et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 2004; 10: 942-949. http://dx.doi.org/10.1038/ nm1093
39. MAILLOUX AW,YOUNG MR. Regulatory T-cell trafficking: from thymic development to tumor-induced immune suppression. Crit Rev Immunol 2010; 30: 435-447. http://dx.doi. org/10.1615/CritRevImmunol.v30.i5.30
40. WENDEL C,HEMPING-BOVENKERK A,KRASNYANSKA J,MEES ST,KOCHETKOVA M et al. CXCR4/CXCL12 participate in extravasation of metastasizing breast cancer cells within the liver in a rat model. PLOS ONE 2012; 7: e30046. http://dx.doi.org/10.1371/journal.pone.0030046
41. CADOO KA,FORNIER MN,MORRIS PG. Biological subtypes of breast cancer: current concepts and implications for recurrence patterns. Q J Nucl Med Mol Imaging 2013; 57: 312-321.
42. BROOM RJ,TANG PA,SIMMONS C,BORDELEAU L,MULLIGAN AM et al. Changes in estrogen receptor,progesterone receptor and Her-2/neu status with time: discordance rates between primary and metastatic breast cancer. Anticancer Res 2009; 29: 1557-1562.
43. ELSTON CW,ELLIS IO. Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up. Histopathology 1991; 19: 403-410. http://dx.doi.org/10.1111/ j.1365-2559.1991.tb00229.x
44. WOLFF AC,HAMMOND MEH,HICKS DG,DOWSETT M,MCSHANE LM et al. Recommendations for human epidermal growth factor receptor 2 testing in breast cancer: American Society of Clinical Oncology/College of American Pathologists clinical practice guideline update. J Clin Oncol 2013; 31: 3997-4013. http://dx.doi.org/10.1200/JCO.2013.50.9984