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Cancer Immunology, Immunotherapy

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01.03.2016 | Original Article

Requirement of interleukin 7 signaling for anti-tumor immune response under lymphopenic conditions in a murine lung carcinoma model

verfasst von: Toshihiro Suzuki, Hidehiro Kishimoto, Ryo Abe

Erschienen in: Cancer Immunology, Immunotherapy | Ausgabe 3/2016

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Abstract

Induction of lymphopenia before adoptive transfer of T cells was followed by lymphopenia-induced proliferation (LIP) and generated a potent anti-tumor immune response in rodents and in a clinical setting. Previously, we reported that CD28 signaling is essential for the differentiation of functional effector cytotoxic T lymphocytes (CTLs) under lymphopenic conditions and sequential LIP of T cells. In this study, to clarify the correlation between LIP and the anti-tumor effect, LIP was inhibited with interleukin 7 (IL7) receptor blockade at various stages, and the anti-tumor effect then assessed. We confirmed that IL7 signaling at the start of LIP is crucial for the anti-tumor immune response. In contrast, continuous IL7 signaling was not required for tumor regression, although LIP of naïve CD8⁺ T cells is usually regulated by IL7. The expansion and migration of CTLs in lymphopenic hosts depend on IL7 signaling during the induction phase. Here, we propose that IL7 signaling and subsequent LIP of T cells have distinct roles in the induction of T cell immunity during lymphopenia.

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Baccala R, Theofilopoulos AN (2005) The new paradigm of T-cell homeostatic proliferation-induced autoimmunity. Trends Immunol 26(1):5–8CrossRefPubMed

Murali-Krishna K, Ahmed R (2000) Cutting edge: naive T cells masquerading as memory cells. J Immunol 165(4):1733–1737CrossRefPubMed

Cho BK, Rao VP, Ge Q, Eisen HN, Chen J (2000) Homeostasis-stimulated proliferation drives naive T cells to differentiate directly into memory T cells. J Exp Med 192(4):549–556CrossRefPubMedPubMedCentral

Datta S, Sarvetnick N (2009) Lymphocyte proliferation in immune-mediated diseases. Trends Immunol 30(9):430–438CrossRefPubMed

Surh CD, Boyman O, Purton JF, Sprent J (2006) Homeostasis of memory T cells. Immunol Rev 211:154–163CrossRefPubMed

Suzuki T, Ogawa S, Tanabe K, Tahara H, Abe R, Kishimoto H (2008) Induction of antitumor immune response by homeostatic proliferation and CD28 signaling. J Immunol 180(7):4596–4605CrossRefPubMed

Hu HM, Poehlein CH, Urba WJ, Fox BA (2002) Development of antitumor immune responses in reconstituted lymphopenic hosts. Cancer Res 62(14):3914–3919PubMed

Prlic M, Blazar BR, Khoruts A, Zell T, Jameson SC (2001) Homeostatic expansion occurs independently of costimulatory signals. J Immunol 167(10):5664–5668CrossRefPubMed

Rosenberg SA, Dudley ME (2004) Cancer regression in patients with metastatic melanoma after the transfer of autologous antitumor lymphocytes. Proc Natl Acad Sci USA 101(Suppl 2):14639–14645CrossRefPubMedPubMedCentral

10.

North RJ (1982) Cyclophosphamide-facilitated adoptive immunotherapy of an established tumor depends on elimination of tumor-induced suppressor T cells. J Exp Med 155(4):1063–1074CrossRefPubMed

11.

Paulos CM, Wrzesinski C, Kaiser A, Hinrichs CS, Chieppa M, Cassard L, Palmer DC, Boni A, Muranski P, Yu Z, Gattinoni L, Antony PA, Rosenberg SA, Restifo NP (2007) Microbial translocation augments the function of adoptively transferred self/tumor-specific CD8⁺ T cells via TLR4 signaling. J Clin Invest 117(8):2197–2204CrossRefPubMedPubMedCentral

12.

Schiavoni G, Mattei F, Di Pucchio T, Santini SM, Bracci L, Belardelli F, Proietti E (2000) Cyclophosphamide induces type I interferon and augments the number of CD44 (hi) T lymphocytes in mice: implications for strategies of chemoimmunotherapy of cancer. Blood 95(6):2024–2030PubMed

13.

Bracci L, Moschella F, Sestili P, La Sorsa V, Valentini M, Canini I, Baccarini S, Maccari S, Ramoni C, Belardelli F, Proietti E (2007) Cyclophosphamide enhances the antitumor efficacy of adoptively transferred immune cells through the induction of cytokine expression, B-cell and T-cell homeostatic proliferation, and specific tumor infiltration. Clin Cancer Res 13(2 PT 1):644–653CrossRefPubMed

14.

Moller P, Sun Y, Dorbic T, Alijagic S, Makki A, Jurgovsky K, Schroff M, Henz BM, Wittig B, Schadendorf D (1998) Vaccination with IL-7 gene-modified autologous melanoma cells can enhance the anti-melanoma lytic activity in peripheral blood of patients with a good clinical performance status: a clinical phase I study. Br J Cancer 77(11):1907–1916CrossRefPubMed

15.

Colombetti S, Levy F, Chapatte L (2009) IL-7 adjuvant treatment enhances long-term tumor-antigen-specific CD8⁺ T-cell responses after immunization with recombinant lentivector. Blood 113(26):6629–6637CrossRefPubMed

16.

Melchionda F, Fry TJ, Milliron MJ, McKirdy MA, Tagaya Y, Mackall CL (2005) Adjuvant IL-7 or IL-15 overcomes immunodominance and improves survival of the CD8⁺ memory cell pool. J Clin Invest 115(5):1177–1187CrossRefPubMedPubMedCentral

17.

Moniuszko M, Fry T, Tsai WP, Morre M, Assouline B, Cortez P, Lewis MG, Cairns S, Mackall C, Franchini G (2004) Recombinant interleukin-7 induces proliferation of naive macaque CD4⁺ and CD8⁺ T cells in vivo. J Virol 78(18):9740–9749CrossRefPubMedPubMedCentral

18.

Pellegrini M, Calzascia T, Toe JG, Preston SP, Lin AE, Elford AR, Shahinian A, Lang PA, Lang KS, Morre M, Assouline B, Lahl K, Sparwasser T, Tedder TF, Paik JH, DePinho RA, Basta S, Ohashi PS, Mak TW (2011) IL-7 engages multiple mechanisms to overcome chronic viral infection and limit organ pathology. Cell 144(4):601–613CrossRefPubMed

19.

Pellegrini M, Calzascia T, Elford AR, Shahinian A, Lin AE, Dissanayake D, Dhanji S, Nguyen LT, Gronski MA, Morre M, Assouline B, Lahl K, Sparwasser T, Ohashi PS, Mak TW (2009) Adjuvant IL-7 antagonizes multiple cellular and molecular inhibitory networks to enhance immunotherapies. Nat Med 15(5):528–536CrossRefPubMed

20.

Andersson A, Yang SC, Huang M, Zhu L, Kar UK, Batra RK, Elashoff D, Strieter RM, Dubinett SM, Sharma S (2009) IL-7 promotes CXCR3 ligand-dependent T cell antitumor reactivity in lung cancer. J Immunol 182(11):6951–6958CrossRefPubMed

21.

Jin JO, Yu Q (2013) Systemic administration of TLR3 agonist induces IL-7 expression and IL-7-dependent CXCR3 ligand production in the lung. J Leukoc Biol 93(3):413–425CrossRefPubMedPubMedCentral

22.

Karasuyama H, Melchers F (1988) Establishment of mouse cell lines which constitutively secrete large quantities of interleukin 2, 3, 4 or 5, using modified cDNA expression vectors. Eur J Immunol 18(1):97–104CrossRefPubMed

23.

Dummer W, Niethammer AG, Baccala R, Lawson BR, Wagner N, Reisfeld RA, Theofilopoulos AN (2002) T cell homeostatic proliferation elicits effective antitumor autoimmunity. J Clin Invest 110(2):185–192CrossRefPubMedPubMedCentral

24.

Qin Z, Blankenstein T (2000) CD4⁺ T cell-mediated tumor rejection involves inhibition of angiogenesis that is dependent on IFN gamma receptor expression by nonhematopoietic cells. Immunity 12(6):677–686CrossRefPubMed

25.

Beyersdorf NB, Ding X, Karp K, Hanke T (2001) Expression of inhibitory “killer cell lectin-like receptor G1” identifies unique subpopulations of effector and memory CD8 T cells. Eur J Immunol 31(12):3443–3452CrossRefPubMed

26.

Kaech SM, Tan JT, Wherry EJ, Konieczny BT, Surh CD, Ahmed R (2003) Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat Immunol 4(12):1191–1198CrossRefPubMed

27.

Sarkar S, Kalia V, Haining WN, Konieczny BT, Subramaniam S, Ahmed R (2008) Functional and genomic profiling of effector CD8 T cell subsets with distinct memory fates. J Exp Med 205(3):625–640CrossRefPubMedPubMedCentral

28.

Surh CD, Sprent J (2005) Regulation of mature T cell homeostasis. Semin Immunol 17(3):183–191CrossRefPubMed

29.

Overwijk WW, Theoret MR, Finkelstein SE, Surman DR, de Jong LA, Vyth-Dreese FA, Dellemijn TA, Antony PA, Spiess PJ, Palmer DC, Heimann DM, Klebanoff CA, Yu Z, Hwang LN, Feigenbaum L, Kruisbeek AM, Rosenberg SA, Restifo NP (2003) Tumor regression and autoimmunity after reversal of a functionally tolerant state of self-reactive CD8⁺ T cells. J Exp Med 198(4):569–580CrossRefPubMedPubMedCentral

30.

Brown IE, Blank C, Kline J, Kacha AK, Gajewski TF (2006) Homeostatic proliferation as an isolated variable reverses CD8⁺ T cell anergy and promotes tumor rejection. J Immunol 177(7):4521–4529CrossRefPubMed

31.

Gattinoni L, Finkelstein SE, Klebanoff CA, Antony PA, Palmer DC, Spiess PJ, Hwang LN, Yu Z, Wrzesinski C, Heimann DM, Surh CD, Rosenberg SA, Restifo NP (2005) Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumor-specific CD8⁺ T cells. J Exp Med 202(7):907–912CrossRefPubMedPubMedCentral

32.

Wrzesinski C, Paulos CM, Gattinoni L, Palmer DC, Kaiser A, Yu Z, Rosenberg SA, Restifo NP (2007) Hematopoietic stem cells promote the expansion and function of adoptively transferred antitumor CD8 T cells. J Clin Invest 117(2):492–501CrossRefPubMedPubMedCentral

33.

Karyampudi L, Lamichhane P, Scheid AD, Kalli KR, Shreeder B, Krempski JW, Behrens MD, Knutson KL (2014) Accumulation of memory precursor CD8 T cells in regressing tumors following combination therapy with vaccine and anti-PD-1 antibody. Cancer Res 74(11):2974–2985CrossRefPubMedPubMedCentral

34.

Wang LX, Li R, Yang G, Lim M, O’Hara A, Chu Y, Fox BA, Restifo NP, Urba WJ, Hu HM (2005) Interleukin-7-dependent expansion and persistence of melanoma-specific T cells in lymphodepleted mice lead to tumor regression and editing. Cancer Res 65(22):10569–10577CrossRefPubMedPubMedCentral

35.

Hand TW, Morre M, Kaech SM (2007) Expression of IL-7 receptor alpha is necessary but not sufficient for the formation of memory CD8 T cells during viral infection. Proc Natl Acad Sci USA 104(28):11730–11735CrossRefPubMedPubMedCentral

36.

Lee LF, Logronio K, Tu GH, Zhai W, Ni I, Mei L, Dilley J, Yu J, Rajpal A, Brown C, Appah C, Chin SM, Han B, Affolter T, Lin JC (2012) Anti-IL-7 receptor-alpha reverses established type 1 diabetes in nonobese diabetic mice by modulating effector T-cell function. Proc Natl Acad Sci USA 109(31):12674–12679CrossRefPubMedPubMedCentral

37.

Penaranda C, Kuswanto W, Hofmann J, Kenefeck R, Narendran P, Walker LS, Bluestone JA, Abbas AK, Dooms H (2012) IL-7 receptor blockade reverses autoimmune diabetes by promoting inhibition of effector/memory T cells. Proc Natl Acad Sci USA 109(31):12668–12673CrossRefPubMedPubMedCentral

38.

Deshpande P, Cavanagh MM, Le Saux S, Singh K, Weyand CM, Goronzy JJ (2013) IL-7- and IL-15-mediated TCR sensitization enables T cell responses to self-antigens. J Immunol 190(4):1416–1423CrossRefPubMedPubMedCentral

39.

Williams IR, Rawson EA, Manning L, Karaoli T, Rich BE, Kupper TS (1997) IL-7 overexpression in transgenic mouse keratinocytes causes a lymphoproliferative skin disease dominated by intermediate TCR cells: evidence for a hierarchy in IL-7 responsiveness among cutaneous T cells. J Immunol 159(6):3044–3056PubMed

40.

Buentke E, Mathiot A, Tolaini M, Di Santo J, Zamoyska R, Seddon B (2006) Do CD8 effector cells need IL-7R expression to become resting memory cells? Blood 108(6):1949–1956CrossRefPubMed

41.

Kinter AL, Godbout EJ, McNally JP, Sereti I, Roby GA, O’Shea MA, Fauci AS (2008) The common gamma-chain cytokines IL-2, IL-7, IL-15, and IL-21 induce the expression of programmed death-1 and its ligands. J Immunol 181(10):6738–6746CrossRefPubMed

42.

Kerkar SP, Restifo NP (2012) Cellular constituents of immune escape within the tumor microenvironment. Cancer Res 72(13):3125–3130CrossRefPubMed

43.

Hamid O, Robert C, Daud A, Hodi FS, Hwu WJ, Kefford R, Wolchok JD, Hersey P, Joseph RW, Weber JS, Dronca R, Gangadhar TC, Patnaik A, Zarour H, Joshua AM, Gergich K, Elassaiss-Schaap J, Algazi A, Mateus C, Boasberg P, Tumeh PC, Chmielowski B, Ebbinghaus SW, Li XN, Kang SP, Ribas A (2013) Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med 369(2):134–144CrossRefPubMedPubMedCentral

44.

Snyder A, Makarov V, Merghoub T, Yuan J, Zaretsky JM, Desrichard A, Walsh LA, Postow MA, Wong P, Ho TS, Hollmann TJ, Bruggeman C, Kannan K, Li Y, Elipenahli C, Liu C, Harbison CT, Wang L, Ribas A, Wolchok JD, Chan TA (2014) Genetic basis for clinical response to CTLA-4 blockade in melanoma. N Engl J Med 371(23):2189–2199CrossRefPubMedPubMedCentral

45.

Pellegrini M, Mak TW (2010) Tumor immune therapy: lessons from infection and implications for cancer—can IL-7 help overcome immune inhibitory networks? Eur J Immunol 40(7):1852–1861CrossRefPubMed

Titel: Requirement of interleukin 7 signaling for anti-tumor immune response under lymphopenic conditions in a murine lung carcinoma model
verfasst von: Toshihiro Suzuki
Hidehiro Kishimoto
Ryo Abe
Publikationsdatum: 01.03.2016
Verlag: Springer Berlin Heidelberg
Erschienen in: Cancer Immunology, Immunotherapy / Ausgabe 3/2016
Print ISSN: 0340-7004
Elektronische ISSN: 1432-0851
DOI: https://doi.org/10.1007/s00262-016-1808-7

Springer Medizin

Requirement of interleukin 7 signaling for anti-tumor immune response under lymphopenic conditions in a murine lung carcinoma model

Abstract

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Abstract

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