Peripheral blood Th9 cells are a possible pharmacodynamic biomarker of nivolumab treatment efficacy in metastatic melanoma patients

OncoImmunology

Volumn 5, Issue 12, 2016, Pages

  Nonomura, Yumi ^a   Otsuka, Atsushi ^a   Nakashima, Chisa ^a   Seidel, Judith A ^a   Kitoh, Akihiko ^a   Dainichi, Teruki ^a   Nakajima, Saeko ^a   Sawada, Yu ^a   Matsushita, Shigeto ^b   Aoki, Megumi ^b   Takenouchi, Tatsuya ^c   Fujimura, Taku ^d   Hatta, Naohito ^e   Koreeda, Satoshi ^f   Fukushima, Satoshi ^g   Honda, Tetsuya ^a   Kabashima, Kenji ^a,h  

^a KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b NATIONAL HOSPITAL ORGANIZATION KAGOSHIMA MEDICAL CENTER   (Japan)

^c NIIGATA CANCER CENTER HOSPITAL   (Japan)

^d TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e TOYAMA PREFECTURAL CENTRAL HOSPITAL   (Japan)

^f TENRI HOSPITAL   (Japan)

^g KUMAMOTO UNIVERSITY   (Japan)

^h AGENCY FOR SCIENCE   (Singapore)

Author keywords

Anti PD 1 antibody; melanoma; nivolumab; Th9

Indexed keywords

GAMMA INTERFERON; GRANZYME B; INTERLEUKIN 10; INTERLEUKIN 4; INTERLEUKIN 9; NIVOLUMAB; PERFORIN; PROGRAMMED DEATH 1 RECEPTOR; TRANSFORMING GROWTH FACTOR BETA;

ADULT; AGED; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CLINICAL ARTICLE; CYTOTOXICITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; HISTOGRAM; HUMAN; MALE; METASTATIC MELANOMA; MOUSE; NONHUMAN; PHARMACODYNAMICS; PROGRESSION FREE SURVIVAL; REGULATORY T LYMPHOCYTE; TH9 CELL; TUMOR GROWTH;

EID: 85007508410     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2016.1248327     Document Type: Article

References (44)

1. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012; 366:2443-54; PMID:22658127; http://dx.doi.org/10.1056/NEJMoa1200690
2. Robert C, Long GV, Brady B, Dutriaux C, Maio M, Mortier L, Hassel JC, Rutkowski P, McNeil C, Kalinka-Warzocha E, et al. Nivolumab in previously untreated melanoma without BRAF mutation. N Engl J Med 2015; 372:320-30; PMID:25399552; http://dx.doi.org/10.1056/NEJMoa1412082
3. Topalian SL, Sznol M, McDermott DF, Kluger HM, Carvajal RD, Sharfman WH, Brahmer JR, Lawrence DP, Atkins MB, Powderly JD, et al. Survival, durable tumor remission, and long-term safety in patients with advanced melanoma receiving nivolumab. J Clin Oncol 2014; 32:1020-30; PMID:24590637; http://dx.doi.org/10.1200/JCO.2013.53.0105
4. Hino R, Kabashima K, Kato Y, Yagi H, Nakamura M, Honjo T, Okazaki T, Tokura Y. Tumor cell expression of programmed cell death-1 ligand 1 is a prognostic factor for malignant melanoma. Cancer 2010; 116:1757-66; PMID:20143437; http://dx.doi.org/10.1002/cncr.24899
5. McLaughlin J, Han G, Schalper KA, Carvajal-Hausdorf D, Pelekanou V, Rehman J, Velcheti V, Herbst R, LoRusso P, Rimm DL. Quantitative assessment of the heterogeneity of PD-L1 expression in non-small-cell lung cancer. JAMA Oncol 2016; 2:46-54; PMID:26562159; http://dx.doi.org/10.1001/jamaoncol.2015.3638
6. Dardalhon V, Awasthi A, Kwon H, Galileos G, Gao W, Sobel RA, Mitsdoerffer M, Strom TB, Elyaman W, Ho IC, et al. IL-4 inhibits TGF-β-induced Foxp3+ T cells and, together with TGF-β, generates IL-9+ IL-10+ Foxp3(-) effector T cells. Nat Immunol 2008; 9:1347-55; PMID:18997793; http://dx.doi.org/10.1038/ni.1677
7. Veldhoen M, Uyttenhove C, van Snick J, Helmby H, Westendorf A, Buer J, Martin B, Wilhelm C, Stockinger B. Transforming growth factor-β ‘reprograms’ the differentiation of T helper 2 cells and promotes an interleukin 9-producing subset. Nat Immunol 2008; 9:1341-6; PMID:18931678; http://dx.doi.org/10.1038/ni.1659
8. Dunn GP, Koebel CM, Schreiber RD. Interferons, immunity and cancer immunoediting. Nat Rev Immunol 2006; 6:836-48; PMID:17063185; http://dx.doi.org/10.1038/nri1961
9. Hoelzinger DB, Dominguez AL, Cohen PA, Gendler SJ. Inhibition of adaptive immunity by IL9 can be disrupted to achieve rapid T-cell sensitization and rejection of progressive tumor challenges. Cancer Res 2014; 74:6845-55; PMID:25297635; http://dx.doi.org/10.1158/0008-5472.CAN-14-0836
10. Matsushita K, Arima N, Ohtsubo H, Fujiwara H, Hidaka S, Fukumori J, Tanaka H. Frequent expression of interleukin-9 mRNA and infrequent involvement of interleukin-9 in proliferation of primary adult T-cell leukemia cells and HTLV-I infected T-cell lines. Leuk Res 1997; 21:211-6; PMID:9111165; http://dx.doi.org/10.1016/S0145-2126(96)00109-9
11. Lu Y, Hong S, Li H, Park J, Hong B, Wang L, Zheng Y, Liu Z, Xu J, He J, et al. Th9 cells promote antitumor immune responses in vivo. J Clin Invest 2012; 122:4160-71; PMID:23064366; http://dx.doi.org/10.1172/JCI65459
12. Purwar R, Schlapbach C, Xiao S, Kang HS, Elyaman W, Jiang X, Jetten AM, Khoury SJ, Fuhlbrigge RC, Kuchroo VK, et al. Robust tumor immunity to melanoma mediated by interleukin-9-producing T cells. Nat Med 2012; 18:1248-53; PMID:22772464; http://dx.doi.org/10.1038/nm.2856
13. Kuang DM, Xiao X, Zhao Q, Chen MM, Li XF, Liu RX, Wei Y, Ouyang FZ, Chen DP, Wu Y, et al. B7-H1-expressing antigen-presenting cells mediate polarization of protumorigenic Th22 subsets. J Clin Invest 2014; 124:4657-67; PMID:25244097; http://dx.doi.org/10.1172/JCI74381
14. Martin-Orozco N, Muranski P, Chung Y, Yang XO, Yamazaki T, Lu S, Hwu P, Restifo NP, Overwijk WW, Dong C. T helper 17 cells promote cytotoxic T cell activation in tumor immunity. Immunity 2009; 31:787-98; PMID:19879162; http://dx.doi.org/10.1016/j.immuni.2009.09.014
15. Jager A, Dardalhon V, Sobel RA, Bettelli E, Kuchroo VK. Th1, Th17, and Th9 effector cells induce experimental autoimmune encephalomyelitis with different pathological phenotypes. J Immunol 2009; 183:7169-77; PMID:19890056; http://dx.doi.org/10.4049/jimmunol.0901906
16. Bedognetti D, Spivey TL, Zhao Y, Uccellini L, Tomei S, Dudley ME, Ascierto ML, De Giorgi V, Liu Q, Delogu LG, et al. CXCR3/CCR5 pathways in metastatic melanoma patients treated with adoptive therapy and interleukin-2. Br J Cancer 2013; 109:2412-23; PMID:24129241; http://dx.doi.org/10.1038/bjc.2013.557
17. Gonzalez-Martin A, Mira E, Manes S. CCR5 in cancer immunotherapy:More than an “attractive” receptor for T cells. Oncoimmunology 2012; 1:106-8; PMID:22720226; http://dx.doi.org/10.4161/onci.1.1.17995
18. Voskoboinik I, Whisstock JC, Trapani JA. Perforin and granzymes:function, dysfunction and human pathology. Nat Rev Immunol 2015; 15:388-400; PMID:25998963; http://dx.doi.org/10.1038/nri3839
19. Turk MJ, Guevara-Patino JA, Rizzuto GA, Engelhorn ME, Sakaguchi S, Houghton AN. Concomitant tumor immunity to a poorly immunogenic melanoma is prevented by regulatory T cells. J Exp Med 2004; 200:771-82; PMID:15381730; http://dx.doi.org/10.1084/jem.20041130
20. Dankort D, Curley DP, Cartlidge RA, Nelson B, Karnezis AN, Damsky WE, Jr, You MJ, DePinho RA, McMahon M, Bosenberg M. Braf(V600E) cooperates with Pten loss to induce metastatic melanoma. Nat Genet 2009; 41:544-52; PMID:19282848; http://dx.doi.org/10.1038/ng.356
21. Tumeh PC, Harview CL, Yearley JH, Shintaku IP, Taylor EJ, Robert L, Chmielowski B, Spasic M, Henry G, Ciobanu V, et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 2014; 515:568-71; PMID:25428505; http://dx.doi.org/10.1038/nature13954
22. Ribas A, Shin DS, Zaretsky J, Frederiksen J, Cornish A, Avramis E, Seja E, Kivork C, Siebert J, Kaplan-Lefko P, et al. PD-1 Blockade Expands Intratumoral Memory T Cells. Cancer Immunol Res 2016; 4:194-203; PMID:26787823; http://dx.doi.org/10.1158/2326-6066.CIR-15-0210
23. Peng W, Liu C, Xu C, Lou Y, Chen J, Yang Y, Yagita H, Overwijk WW, Lizée G, Radvanyi L, et al. PD-1 blockade enhances T-cell migration to tumors by elevating IFN-gamma inducible chemokines. Cancer Res 2012; 72:5209-18; PMID:22915761; http://dx.doi.org/10.1158/0008-5472.CAN-12-1187
24. Snyder A, Makarov V, Merghoub T, Yuan J, Zaretsky JM, Desrichard A, Walsh LA, Postow MA, Wong P, Ho TS, et al. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N Engl J Med 2014; 371:2189-99; PMID:25409260; http://dx.doi.org/10.1056/NEJMoa1406498
25. Church SE, Galon J. Tumor microenvironment and immunotherapy:the whole picture is better than a glimpse. Immunity 2015; 43:631-3; PMID:26488814; http://dx.doi.org/10.1016/j.immuni.2015.10.004
26. Van Allen EM, Miao D, Schilling B, Shukla SA, Blank C, Zimmer L, Sucker A, Hillen U, Geukes Foppen MH, Goldinger SM, et al. Genomic correlates of response to CTLA-4 blockade in metastatic melanoma. Science 2015; 350:207-11; PMID:26359337; http://dx.doi.org/10.1126/science.aad0095
27. Leivonen SK, Kahari VM. Transforming growth factor-β signaling in cancer invasion and metastasis. Int J Cancer 2007; 121:2119-24; PMID:17849476; http://dx.doi.org/10.1002/ijc.23113
28. Albino AP, Davis BM, Nanus DM. Induction of growth factor RNA expression in human malignant melanoma:markers of transformation. Cancer Res 1991; 51:4815-20; PMID:1716514
29. Javelaud D, Alexaki VI, Mauviel A. Transforming growth factor-beta in cutaneous melanoma. Pigment Cell Melanoma Res 2008; 21:123-32; PMID:18426405; http://dx.doi.org/10.1111/j.1755-148X.2008.00450.x
30. Van Belle P, Rodeck U, Nuamah I, Halpern AC, Elder DE. Melanoma-associated expression of transforming growth factor-beta isoforms. Am J Pathol 1996; 148:1887-94; PMID:8669474
31. Ye H, Zhang C, Wang BJ, Tan XH, Zhang WP, Teng Y, Yang X. Synergistic function of Kras mutation and HBx in initiation and progression of hepatocellular carcinoma in mice. Oncogene 2014; 33:5133-8; PMID:24213574; http://dx.doi.org/10.1038/onc.2013.468
32. Merz H, Houssiau FA, Orscheschek K, Renauld JC, Fliedner A, Herin M, Noel H, Kadin M, Mueller-Hermelink HK, Van Snick J, et al. Interleukin-9 expression in human malignant lymphomas:unique association with Hodgkin's disease and large cell anaplastic lymphoma. Blood 1991; 78:1311-7; PMID:1908723
33. Lv X, Feng L, Fang X, Jiang Y, Wang X. Overexpression of IL-9 receptor in diffuse large B-cell lymphoma. Int J Clin Exp Pathol 2013; 6:911-6; PMID:23638223
34. Nagato T, Kobayashi H, Kishibe K, Takahara M, Ogino T, Ishii H, Oikawa K, Aoki N, Sato K, Kimura S, et al. Expression of interleukin-9 in nasal natural killer/T-cell lymphoma cell lines and patients. Clin Cancer Res 2005; 11:8250-7; PMID:16322282; http://dx.doi.org/10.1158/1078-0432.CCR-05-1426
35. Vegran F, Berger H, Boidot R, Mignot G, Bruchard M, Dosset M, Chalmin F, Rébé C, Dérangère V, Ryffel B, et al. The transcription factor IRF1 dictates the IL-21-dependent anticancer functions of TH9 cells. Nat Immunol 2014; 15:758-66; PMID:24973819; http://dx.doi.org/10.1038/ni.2925
36. Ho PC, Liu PS. Metabolic communication in tumors:a new layer of immunoregulation for immune evasion. J Immunother Cancer 2016; 4:4; PMID:26885366; http://dx.doi.org/10.1186/s40425-016-0109-1
37. Patsoukis N, Bardhan K, Chatterjee P, Sari D, Liu B, Bell LN, Karoly ED, Freeman GJ, Petkova V, Seth P, et al. PD-1 alters T-cell metabolic reprogramming by inhibiting glycolysis and promoting lipolysis and fatty acid oxidation. Nat Commun 2015; 6:6692; PMID:25809635; http://dx.doi.org/10.1038/ncomms7692
38. Wang Y, Bi Y, Chen X, Li C, Li Y, Zhang Z, Wang J, Lu Y, Yu Q, Su H, et al. Histone deacetylase SIRT1 negatively regulates the differentiation of interleukin-9-producing CD4(+) T cells. Immunity 2016; 44:1337-49; PMID:27317260; http://dx.doi.org/10.1016/j.immuni.2016.05.009
39. Dummer R, Schadendorf D, Ascierto PA, Larkin J, Lebbe C, Hauschild A. Integrating first-line treatment options into clinical practice:what's new in advanced melanoma? Melanoma Res 2015; 25:461-9; PMID:26426764; http://dx.doi.org/10.1097/CMR.0000000000000200
40. Huang D, Tani M, Wang J, Han Y, He TT, Weaver J, Charo IF, Tuohy VK, Rollins BJ, Ransohoff RM. Pertussis toxin-induced reversible encephalopathy dependent on monocyte chemoattractant protein-1 overexpression in mice. J Neurosci 2002; 22:10633-42; PMID:12486156
41. Elhofy A, Wang J, Tani M, Fife BT, Kennedy KJ, Bennett J, Huang D, Ransohoff RM, Karpus WJ. Transgenic expression of CCL2 in the central nervous system prevents experimental autoimmune encephalomyelitis. J Leukoc Biol 2005; 77:229-37; PMID:15539456; http://dx.doi.org/10.1189/jlb.0804465
42. Kreider JW, Schmoyer ME. Spontaneous maturation and differentiation of B16 melanoma cells in culture. J Natl Cancer Inst 1975; 55:641-7; PMID:1159842
43. Falo LD, Jr, Kovacsovics-Bankowski M, Thompson K, Rock KL. Targeting antigen into the phagocytic pathway in vivo induces protective tumour immunity. Nat Med 1995; 1:649-53; PMID:7585145; http://dx.doi.org/10.1038/nm0795-649
44. Clarke SR, Barnden M, Kurts C, Carbone FR, Miller JF, Heath WR. Characterization of the ovalbumin-specific TCR transgenic line OT-I:MHC elements for positive and negative selection. Immunol Cell Biol 2000; 78:110-7; PMID:10762410; http://dx.doi.org/10.1046/j.1440-1711.2000.00889.x