Downregulation of IL-17-producing T cells is associated with regulatory T cell expansion and disease progression in chronic lymphocytic leukemia

Tumor Biology

Volumn 34, Issue 2, 2013, Pages 929-940

  Jadidi Niaragh, Farhad ^a   Ghalamfarsa, Ghasem ^a   Memarian, Ali ^b   Asgarian Omran, Hossein ^a   Razavi, Seyed Mohsen ^c   Sarrafnejad, Abdolfattah ^a   Shokri, Fazel ^a  

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Chronic lymphocytic leukemia; Interleukin 17; Regulatory T cell; Tc17; Th17

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 4; MESSENGER RNA; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR T BET;

ADULT; AGED; ARTICLE; CANCER GROWTH; CANCER STAGING; CELL EXPANSION; CELL PROLIFERATION; CHRONIC LYMPHATIC LEUKEMIA; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; DOWN REGULATION; EFFECTOR CELL; FEMALE; FLOW CYTOMETRY; GENE MUTATION; HUMAN; HUMAN CELL; IGHV GENE; MALE; ONCOGENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY T LYMPHOCYTE; TH17 CELL; ANIMAL; CASE CONTROL STUDY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; COMPARATIVE STUDY; DISEASE COURSE; GENETICS; IMMUNOLOGY; METABOLISM; MIDDLE AGED; MONONUCLEAR CELL; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SHEEP; TH1 CELL;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; CASE-CONTROL STUDIES; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; DISEASE PROGRESSION; DOWN-REGULATION; FEMALE; FLOW CYTOMETRY; HUMANS; INTERLEUKIN-17; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; LEUKOCYTES, MONONUCLEAR; MALE; MIDDLE AGED; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SHEEP; T-LYMPHOCYTES, REGULATORY; TH1 CELLS;

MLCS; MLOWN;

EID: 84877142286     PISSN: 10104283     EISSN: 14230380     Source Type: Journal    
DOI: 10.1007/s13277-012-0628-4     Document Type: Article

References (66)

1. Chiorazzi N, Rai KR, Ferrarini M. Chronic lymphocytic leukemia. N Engl J Med. 2005;352:804-15.
2. Hojjat-Farsangi M, Jeddi-Tehrani M, Razavi SM, Sharifian RA, Mellstedt H, Shokri F, et al. Immunoglobulin heavy chain variable region gene usage and mutational status of the leukemic B cells in Iranian patients with chronic lymphocytic leukemia. Cancer Sci. 2009;100:2346-53.
3. Tamura K, Sawada H, Izumi Y, Fukuda T, Utsunomiya A, Ikeda S, et al. Chronic lymphocytic leukemia (CLL) is rare, but the proportion of T-CLL is high in Japan. European Journal of Haematology. 2001;67:152-7.
4. Ravandi F, O'Brien S. Immune defects in patients with chronic lymphocytic leukemia. Cancer Immunol Immunother. 2006;55:197-209.
5. Kröber A, Seiler T, Benner A, Bullinger L, Brückle E, Lichter P, et al. Vh mutation status, cd38 expression level, genomic aberrations, and survival in chronic lymphocytic leukemia. Blood. 2002;100:1410.
6. Kharfan-Dabaja MA, Chavez JC, Khorfan KA, Pinilla-Ibarz J. Clinical and therapeutic implications of the mutational status of IGVH in patients with chronic lymphocytic leukemia. Cancer. 2008;113:897-906.
7. Kay N, O'Brien S, Pettitt A, Stilgenbauer S. The role of prognostic factors in assessing 'high-risk'subgroups of patients with chronic lymphocytic leukemia. Leukemia. 2007;21:1885-91.
8. Orchard JA, Ibbotson RE, Davis Z, Wiestner A, Rosenwald A, Thomas PW, et al. Zap-70 expression and prognosis in chronic lymphocytic leukaemia. Lancet. 2004;363:105-11.
9. Jadidi-Niaragh F, Mirshafiey A. Th17 cell, the new player of neuroinflammatory process in multiple sclerosis. Scand J Immunol. 2011;74:1-13.
10. Zou W, Restifo NP. T(h)17 cells in tumour immunity and immunotherapy. Nat Rev Immunol. 2010;10:248-56.
11. Alexandrakis MG, Pappa CA, Miyakis S, Sfiridaki A, Kafousi M, Alegakis A, et al. Serum interleukin-17 and its relationship to angiogenic factors in multiple myeloma. Eur J Intern Med. 2006;17:412-6.
12. Dhodapkar KM, Barbuto S, Matthews P, Kukreja A, Mazumder A, Vesole D, et al. Dendritic cells mediate the induction of polyfunctional human IL17-producing cells (th17-1 cells) enriched in the bone marrow of patients with myeloma. Blood. 2008;112:2878-85.
13. Wu C, Wang S, Wang F, Chen Q, Peng S, Zhang Y, et al. Increased frequencies of T helper type 17 cells in the peripheral blood of patients with acute myeloid leukaemia. Clin Exp Immunol. 2009;158:199-204.
14. Yang ZZ, Novak AJ, Ziesmer SC, Witzig TE, Ansell SM. Malignant b cells skew the balance of regulatory T cells and th17 cells in b-cell non-Hodgkin's lymphoma. Cancer Res. 2009;69:5522-30.
15. Kondo T, Takata H, Matsuki F, Takiguchi M. Cutting edge: Phenotypic characterization and differentiation of human cd8+ T cells producing IL-17. J Immunol. 2009;182:1794-8.
16. Huber M, Heink S, Grothe H, Guralnik A, Reinhard K, Elflein K, et al. A Th17-like developmental process leads to cd8(+) Tc17 cells with reduced cytotoxic activity. Eur J Immunol. 2009;39:1716-25.
17. Garcia-Hernandez Mde L, Hamada H, Reome JB, Misra SK, Tighe MP, Dutton RW. Adoptive transfer of tumor-specific Tc17 effector T cells controls the growth of b16 melanoma in mice. J Immunol. 2010;184:4215-27.
18. Hinrichs CS, Kaiser A, Paulos CM, Cassard L, Sanchez-Perez L, Heemskerk B, et al. Type 17 cd8+ T cells display enhanced antitumor immunity. Blood. 2009;114:596-9.
19. Kuang DM, Peng C, Zhao Q, Wu Y, Zhu LY, Wang J, et al. Tumor-activated monocytes promote expansion of IL-17-producing cd8+ T cells in hepatocellular carcinoma patients. J Immunol. 2010;185:1544-9.
20. Beyer M, Kochanek M, Darabi K, Popov A, Jensen M, Endl E, et al. Reduced frequencies and suppressive function of cd4+cd25hi regulatory T cells in patients with chronic lymphocytic leukemia after therapy with fludarabine. Blood. 2005;106:2018-25.
21. D'Arena G, Laurenti L, Minervini MM, Deaglio S, Bonello L, De Martino L, et al. Regulatory T-cell number is increased in chronic lymphocytic leukemia patients and correlates with progressive disease. Leuk Res. 2011;35:363-8.
22. Giannopoulos K, Schmitt M, Kowal M, Wlasiuk P, Bojarska-Junak A, Chen J, et al. Characterization of regulatory T cells in patients with b-cell chronic lymphocytic leukemia. Oncol Rep. 2008;20:677-82.
23. Giannopoulos K, Schmitt M, Wlasiuk P, Chen J, Bojarska-Junak A, Kowal M, et al. The high frequency of T regulatory cells in patients with b-cell chronic lymphocytic leukemia is diminished through treatment with thalidomide. Leukemia. 2008;22:222-4.
24. Jadidi-Niaragh F, Jeddi-Tehrani M, Ansaripour B, Razavi SM, Sharifian RA, Shokri F: Reduced frequency of NKT-like cells in patients with progressive chronic lymphocytic leukemia. Med Oncol. 2012;29(5):3561-9.
25. Li MO, Wan YY, Flavell RA. T cell-produced transforming growth factor-beta1 controls T cell tolerance and regulates Th1- and Th17-cell differentiation. Immunity. 2007;26:579-91.
26. Fletcher JM, Lonergan R, Costelloe L, Kinsella K, Moran B, O'Farrelly C, et al. Cd39+Foxp3+ regulatory T cells suppress pathogenic Th17 cells and are impaired in multiple sclerosis. J Immunol. 2009;183:7602-10.
27. Clayton A, Al-Taei S, Webber J, Mason MD, Tabi Z. Cancer exosomes express cd39 and cd73, which suppress T cells through adenosine production. J Immunol. 2011;187:676-83.
28. Ye ZJ, Zhou Q, Zhang JC, Li X, Wu C, Qin SM, et al. Cd39+ regulatory T cells suppress generation and differentiation of Th17 cells in human malignant pleural effusion via a lap-dependent mechanism. Respir Res. 2011;12:77-87.
29. Jaffe ES. The 2008 who classification of lymphomas: implications for clinical practice and translational research. Hematology Am Soc Hematol Educ Program 2009:523-531.
30. Cheson BD, Bennett JM, Grever M, Kay N, Keating MJ, O'Brien S, et al. National cancer institute-sponsored working group guidelines for chronic lymphocytic leukemia: revised guidelines for diagnosis and treatment. Blood. 1996;87:4990-7.
31. Hallek M, Cheson BD, Catovsky D, Caligaris-Cappio F, Dighiero G, Döhner H, et al. Guidelines for the diagnosis and treatment of chronic lymphocytic leukemia: a report from the international workshop on chronic lymphocytic leukemia updating the national cancer institute-working group 1996 guidelines. Blood. 2008;111:5446-56.
32. Rai KR, Sawitsky A, Cronkite EP, Chanana AD, Levy RN, Pasternack BS. Clinical staging of chronic lymphocytic leukemia. Blood. 1975;46:219-34.
33. Gharagozlou S, Kardar GA, Rabbani H, Shokri F. Molecular analysis of the heavy chain variable region genes of human hybridoma clones specific for coagulation factor viii. Thromb Haemost. 2005;94:1131-7.
34. Dickinson AM, George S, Proctor SJ. T cell subpopulations in CLL: methods of T cell enrichment artificially alter proportions of okt4 and okt8 positive cells. Clin Exp Immunol. 1983;54:525-31.
35. Memarian A, Hojjat-Farsangi M, Asgarian-Omran H, Younesi V, Jeddi-Tehrani M, Sharifian RA, et al. Variation in WNT genes expression in different subtypes of chronic lymphocytic leukemia. Leukemia & Lymphoma. 2009;50:2061-70.
36. Weaver CT, Hatton RD. Interplay between the Th17 and Treg cell lineages: a (co-)evolutionary perspective. Nat Rev Immunol. 2009;9:883-9.
37. Jadidi-Niaragh F, Mirshafiey A: The deviated balance between regulatory T cell and th17 in autoimmunity. Immunopharmacol Immunotoxicol. 2012;34(5):727-39.
38. Chaudhry A, Rudra D, Treuting P, Samstein RM, Liang Y, Kas A, et al. Cd4+ regulatory T cells control Th17 responses in a Stat3-dependent manner. Science. 2009;326:986-91.
39. Zhang Y, Ma D, Tian Y, Wang X, Qiao Y, Cui B. The imbalance of th17/Treg in patients with uterine cervical cancer. Clin Chim Acta. 2011;412:894-900.
40. Yang XO, Nurieva R, Martinez GJ, Kang HS, Chung Y, Pappu BP, et al. Molecular antagonism and plasticity of regulatory and inflammatory T cell programs. Immunity. 2008;29:44-56.
41. Martin-Orozco N, Muranski P, Chung Y, Yang XO, Yamazaki T, Lu S, et al. T helper 17 cells promote cytotoxic T cell activation in tumor immunity. Immunity. 2009;31:787-98.
42. Ankathatti Munegowda M, Deng Y, Mulligan SJ, Xiang J. Th17 and Th17-stimulated Cd8 T cells play a distinct role in Th17-induced preventive and therapeutic antitumor immunity. Cancer Immunol Immunother. 2011;60:1473-84.
43. Sfanos KS, Bruno TC, Maris CH, Xu L, Thoburn CJ, DeMarzo AM, et al. Phenotypic analysis of prostate-infiltrating lymphocytes reveals Th17 and Treg skewing. Clin Cancer Res. 2008;14:3254-61.
44. Gnerlich JL, Mitchem JB, Weir JS, Sankpal NV, Kashiwagi H, Belt BA, et al. Induction of Th17 cells in the tumor microenvironment improves survival in a murine model of pancreatic cancer. J Immunol. 2010;185:4063-71.
45. Kryczek I, Banerjee M, Cheng P, Vatan L, Szeliga W, Wei S, et al. Phenotype, distribution, generation, and functional and clinical relevance of Th17 cells in the human tumor environments. Blood. 2009;114:1141-9.
46. Horlock C, Stott B, Dyson PJ, Morishita M, Coombes RC, Savage P, et al. The effects of trastuzumab on the Cd4+Cd25+Foxp3+ and Cd4+IL17a+ T-cell axis in patients with breast cancer. Br J Cancer. 2009;100:1061-7.
47. Prabhala RH, Pelluru D, Fulciniti M, Prabhala HK, Nanjappa P, Song W, et al. Elevated Il-17 produced by Th17 cells promotes myeloma cell growth and inhibits immune function in multiple myeloma. Blood. 2010;115:5385-92.
48. Giannopoulos K, Wlasiuk P, Dmoszynska A, Rolinski J, Schmitt M. Peptide vaccination induces profound changes in the immune system in patients with B-cell chronic lymphocytic leukemia. Folia Histochem Cytobiol. 2011;49:161-7.
49. Idler I, Giannopoulos K, Zenz T, Bhattacharya N, Nothing M, Dohner H, et al. Lenalidomide treatment of chronic lymphocytic leukaemia patients reduces regulatory T cells and induces Th17 T helper cells. Br J Haematol. 2010;148:948-50.
50. Bouley J, Deriano L, Delic J, Merle-Beral H. New molecular markers in resistant B-CLL. Leuk Lymphoma. 2006;47:791-801.
51. Thunberg U, Johnson A, Roos G, Thorn I, Tobin G, Sallstrom J, et al. Cd38 expression is a poor predictor for VH gene mutational status and prognosis in chronic lymphocytic leukemia. Blood. 2001;97:1892-4.
52. Kryczek I, Wei S, Zou L, Altuwaijri S, Szeliga W, Kolls J, et al. Cutting edge: Th17 and regulatory T cell dynamics and the regulation by IL-2 in the tumor microenvironment. J Immunol. 2007;178:6730-3.
53. Tajima M, Wakita D, Satoh T, Kitamura H, Nishimura T. IL-17/IFN-gamma double producing Cd8(+) T (Tc17/IFN-gamma) cells: a novel cytotoxic T-cell subset converted from Tc17 cells by IL-12. International Immunology. 2011;23:751-9.
54. Hamai A, Pignon P, Raimbaud I, Duperrier-Amouriaux K, Senellart H, Hiret S, et al. Human T(h)17 immune cells specific for the tumor antigen mage-a3 convert to IFN-gamma-secreting cells as they differentiate into effector T cells in vivo. Cancer Research. 2012;72:1059-63.
55. Haabeth OAW, Lorvik KB, Hammarström C, Donaldson IM, Haraldsen G, Bogen B. Corthay A: inflammation driven by tumour-specific Th1 cells protects against B-cell cancer. Nature communications. 2011;2:240.
56. Podhorecka M, Dmoszynska A, Rolinski J, Wasik E. T type 1/type 2 subsets balance in B-cell chronic lymphocytic leukemia - the three-color flow cytometry analysis. Leuk Res. 2002;26:657-60.
57. Hill SJ, Peters SH, Ayliffe MJ, Merceica J, Bansal AS. Reduced IL-4 and interferon-gamma (IFN-gamma) expression by Cd4 T cells in patients with chronic lymphocytic leukaemia. Clin Exp Immunol. 1999;117:8-11.
58. Gallego A, Vargas JA, Castejon R, Citores MJ, Romero Y, Millan I, et al. Production of intracellular IL-2, TNF-alpha, and IFN-gamma by T cells in B-CLL. Cytometry B Clin Cytom. 2003;56:23-9.
59. Pourgheysari B, Bruton R, Parry H, Billingham L, Fegan C, Murray J, et al. The number of cytomegalovirus-specific Cd4+ T cells is markedly expanded in patients with B-cell chronic lymphocytic leukemia and determines the total Cd4+ T-cell repertoire. Blood. 2010;116:2968-74.
60. Walton JA, Lydyard PM, Nathwani A, Emery V, Akbar A, Glennie MJ, et al. Patients with B cell chronic lymphocytic leukaemia have an expanded population of Cd4 perforin expressing T cells enriched for human cytomegalovirus specificity and an effector-memory phenotype. Br J Haematol. 2010;148:274-84.
61. Lindqvist CA, Christiansson LH, Thorn I, Mangsbo S, Paul-Wetterberg G, Sundstrom C, et al. Both Cd4+ Foxp3+ and Cd4+ Foxp3- T cells from patients with B-cell malignancy express cytolytic markers and kill autologous leukaemic B cells in vitro. Immunology. 2011;133:296-306.
62. Weiss L, Melchardt T, Egle A, Grabmer C, Greil R, Tinhofer I. Regulatory T cells predict the time to initial treatment in early stage chronic lymphocytic leukemia. Cancer. 2011;117:2163-9.
63. Pulte D, Furman RR, Broekman MJ, Drosopoulos JHF, Ballard HS, Olson KE, et al. Cd39 expression on T lymphocytes correlates with severity of disease in patients with chronic lymphocytic leukemia. Clinical Lymphoma Myeloma & Leukemia. 2011;11:367-72.
64. Lotz M, Ranheim E, Kipps TJ. Transforming growth factor beta as endogenous growth inhibitor of chronic lymphocytic leukemia B cells. The Journal of experimental medicine. 1994;179:999-1004.
65. Carter NARE, Mauri C. IL-10 produced by B cells is crucial for the suppression of Th17/ Th1 responses, induction of Tr1 cells and reduction of collagen-induced arthritis. Arthritis research and therapy. 2012;14:R32.
66. Huber S, Gagliani N, Esplugues E, O'Connor Jr W, Huber FJ, Chaudhry A, et al. Th17 cells express interleukin-10 receptor and are controlled by Foxp3 and Foxp3+ regulatory Cd4+ T cells in an interleukin-10-dependent manner. Immunity. 2011;34:554-65.