PEGylated IL-10 (Pegilodecakin) Induces Systemic Immune Activation, CD8+ T Cell Invigoration and Polyclonal T Cell Expansion in Cancer Patients

Cancer Cell

Volumn 34, Issue 5, 2018, Pages 775-791.e3

  Naing, Aung ^a   Infante, Jeffrey R ^b   Papadopoulos, Kyriakos P ^c   Chan, Ivan H ^d   Shen, Cong ^e   Ratti, Navneet P ^d   Rojo, Bianca ^d   Autio, Karen A ^e   Wong, Deborah J ^f   Patel, Manish R ^g   Ott, Patrick A ^h   Falchook, Gerald S ⁱ   Pant, Shubham ^j   Hung, Annie ^d   Pekarek, Kara L ^d   Wu, Victoria ^d   Adamow, Matthew ^e   McCauley, Scott ^d   Mumm, John B ^d   Wong, Phillip ^e   Van Vlasselaer, Peter ^d   Leveque, Joseph ^d   Tannir, Nizar M ^a   Oft, Martin ^d   more..

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b SARAH CANNON RESEARCH INSTITUTE   (United States)

^c START Center for Cancer Care   (United States)

^d ELI LILLY AND COMPANY   (United States)

^e MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g SARAH CANNON RESEARCH INSTITUTE   (United States)

^h DANA FARBER CANCER INSTITUTE   (United States)

ⁱ HealthOne   (United States)

^j OKLAHOMA CITY UNIVERSITY   (United States)

more..

Author keywords

AM0010; CD8+ T cell; clinical trial; clonal expansion; clonality; IL 10; pegilodecakin; PEGylated Interleukin 10; T cell invigoration; Th1

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GAMMA INTERFERON; GRANZYME B; HEPATITIS A VIRUS CELLULAR RECEPTOR 2; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 17; INTERLEUKIN 18; INTERLEUKIN 23; INTERLEUKIN 4; PEGILODECAKIN; PEMBROLIZUMAB; STAT3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR;

ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CANCER PATIENT; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELLULAR IMMUNITY; CLINICAL ARTICLE; CLONE; COHORT ANALYSIS; CONTROLLED STUDY; DRUG SELF ADMINISTRATION; HUMAN; HUMAN CELL; LYMPHOCYTE PROLIFERATION; MELANOMA; MONOTHERAPY; MULTIPLE CYCLE TREATMENT; NON SMALL CELL LUNG CANCER; POLYCLONAL ACTIVATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RENAL CELL CARCINOMA; SINGLE DRUG DOSE; SUBCUTANEOUS IMMUNOTHERAPY; T LYMPHOCYTE ACTIVATION; TH1 CELL; TH2 CELL; TUMOR REJECTION; TUMOR VOLUME; UPREGULATION;

EID: 85055890244     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccell.2018.10.007     Document Type: Article

References (50)

1. Afanasiev, O.K., Yelistratova, L., Miller, N., Nagase, K., Paulson, K., Iyer, J.G., Ibrani, D., Koelle, D.M., Nghiem, P., Merkel polyomavirus-specific T cells fluctuate with merkel cell carcinoma burden and express therapeutically targetable PD-1 and Tim-3 exhaustion markers. Clin. Cancer Res. 19 (2013), 5351–5360.
2. Anderson, A.C., Joller, N., Kuchroo, V.K., Lag-3, Tim-3, and TIGIT: co-inhibitory receptors with specialized functions in immune regulation. Immunity 44 (2016), 989–1004.
3. Apetoh, L., Smyth, M.J., Drake, C.G., Abastado, J.P., Apte, R.N., Ayyoub, M., Blay, J.Y., Bonneville, M., Butterfield, L.H., Caignard, A., et al. Consensus nomenclature for CD8+ T cell phenotypes in cancer. Oncoimmunology, 4, 2015, e998538.
4. Berg, D.J., Davidson, N., Kuhn, R., Muller, W., Menon, S., Holland, G., Thompson-Snipes, L., Leach, M.W., Rennick, D., Enterocolitis and colon cancer in interleukin-10-deficient mice are associated with aberrant cytokine production and CD4(+) TH1-like responses. J. Clin. Invest. 98 (1996), 1010–1020.
5. Bromberg, J., Darnell, J.E. Jr., The role of STATs in transcriptional control and their impact on cellular function. Oncogene 19 (2000), 2468–2473.
6. low effectors that exhibit augmented activity against advanced solid tumors. Cell Rep. 21 (2017), 3205–3219.
7. Cohen, C.J., Gartner, J.J., Horovitz-Fried, M., Shamalov, K., Trebska-McGowan, K., Bliskovsky, V.V., Parkhurst, M.R., Ankri, C., Prickett, T.D., Crystal, J.S., et al. Isolation of neoantigen-specific T cells from tumor and peripheral lymphocytes. J. Clin. Invest. 125 (2015), 3981–3991.
8. Cui, W., Liu, Y., Weinstein, J.S., Craft, J., Kaech, S.M., An interleukin-21-interleukin-10-STAT3 pathway is critical for functional maturation of memory CD8+ T cells. Immunity 35 (2011), 792–805.
9. Daud, A.I., Loo, K., Pauli, M.L., Sanchez-Rodriguez, R., Sandoval, P.M., Taravati, K., Tsai, K., Nosrati, A., Nardo, L., Alvarado, M.D., et al. Tumor immune profiling predicts response to anti-PD-1 therapy in human melanoma. J. Clin. Invest. 126 (2016), 3447–3452.
10. Emmerich, J., Mumm, J.B., Chan, I.H., LaFace, D., Truong, H., McClanahan, T., Gorman, D.M., Oft, M., IL-10 directly activates and expands tumor-resident CD8(+) T cells without de novo infiltration from secondary lymphoid organs. Cancer Res. 72 (2012), 3570–3581.
11. Foulds, K.E., Rotte, M.J., Seder, R.A., IL-10 is required for optimal CD8 T cell memory following Listeria monocytogenes infection. J. Immunol. 177 (2006), 2565–2574.
12. Freeman, G.J., Casasnovas, J.M., Umetsu, D.T., DeKruyff, R.H., TIM genes: a family of cell surface phosphatidylserine receptors that regulate innate and adaptive immunity. Immunol. Rev. 235 (2010), 172–189.
13. Fujii, S., Shimizu, K., Shimizu, T., Lotze, M.T., Interleukin-10 promotes the maintenance of antitumor CD8(+) T-cell effector function in situ. Blood 98 (2001), 2143–2151.
14. Green, D.R., Droin, N., Pinkoski, M., Activation-induced cell death in T cells. Immunol. Rev. 193 (2003), 70–81.
15. Gros, A., Parkhurst, M.R., Tran, E., Pasetto, A., Robbins, P.F., Ilyas, S., Prickett, T.D., Gartner, J.J., Crystal, J.S., Roberts, I.M., et al. Prospective identification of neoantigen-specific lymphocytes in the peripheral blood of melanoma patients. Nat. Med. 22 (2016), 433–438.
16. Gros, A., Robbins, P.F., Yao, X., Li, Y.F., Turcotte, S., Tran, E., Wunderlich, J.R., Mixon, A., Farid, S., Dudley, M.E., et al. PD-1 identifies the patient-specific CD8(+) tumor-reactive repertoire infiltrating human tumors. J. Clin. Invest. 124 (2014), 2246–2259.
17. Grosso, J.F., Kelleher, C.C., Harris, T.J., Maris, C.H., Hipkiss, E.L., De Marzo, A., Anders, R., Netto, G., Getnet, D., Bruno, T.C., et al. LAG-3 regulates CD8+ T cell accumulation and effector function in murine self- and tumor-tolerance systems. J. Clin. Invest. 117 (2007), 3383–3392.
18. He, X.S., Mahmood, K., Maecker, H.T., Holmes, T.H., Kemble, G.W., Arvin, A.M., Greenberg, H.B., Analysis of the frequencies and of the memory T cell phenotypes of human CD8+ T cells specific for influenza A viruses. J. Infect. Dis. 187 (2003), 1075–1084.
19. Heidema, J., Rossen, J.W., Lukens, M.V., Ketel, M.S., Scheltens, E., Kranendonk, M.E., van Maren, W.W., van Loon, A.M., et al. Dynamics of human respiratory virus-specific CD8+ T cell responses in blood and airways during episodes of common cold. J. Immunol. 181 (2008), 5551–5559.
20. Hu, B., Ren, J., Luo, Y., Keith, B., Young, R.M., Scholler, J., Zhao, Y., June, C.H., Augmentation of antitumor immunity by human and mouse CAR T cells secreting IL-18. Cell Rep. 20 (2017), 3025–3033.
21. Huang, A.C., Postow, M.A., Orlowski, R.J., Mick, R., Bengsch, B., Manne, S., Xu, W., Harmon, S., Giles, J.R., Wenz, B., et al. T-cell invigoration to tumour burden ratio associated with anti-PD-1 response. Nature 545 (2017), 60–65.
22. Im, S.J., Hashimoto, M., Gerner, M.Y., Lee, J., Kissick, H.T., Burger, M.C., Shan, Q., Hale, J.S., Lee, J., Nasti, T.H., et al. Defining CD8+ T cells that provide the proliferative burst after PD-1 therapy. Nature 537 (2016), 417–421.
23. Iwai, Y., Hemmi, H., Mizenina, O., Kuroda, S., Suda, K., Steinman, R.M., An IFN-gamma-IL-18 signaling loop accelerates memory CD8+ T cell proliferation. PLoS One, 3, 2008, e2404.
24. Kallies, A., Good-Jacobson, K.L., Transcription factor T-bet orchestrates lineage development and function in the immune system. Trends Immunol. 38 (2017), 287–297.
25. Keir, M.E., Butte, M.J., Freeman, G.J., Sharpe, A.H., PD-1 and its ligands in tolerance and immunity. Annu. Rev. Immunol. 26 (2008), 677–704.
26. Knuth, A., Wolfel, T., Klehmann, E., Boon, T., Meyer zum Buschenfelde, K.H., Cytolytic T-cell clones against an autologous human melanoma: specificity study and definition of three antigens by immunoselection. Proc. Natl. Acad. Sci. U S A 86 (1989), 2804–2808.
27. Koppelman, B., Neefjes, J.J., de Vries, J.E., de Waal Malefyt, R., Interleukin-10 down-regulates MHC class II alphabeta peptide complexes at the plasma membrane of monocytes by affecting arrival and recycling. Immunity 7 (1997), 861–871.
28. Langowski, J.L., Kastelein, R.A., Oft, M., Swords into plowshares: IL-23 repurposes tumor immune surveillance. Trends Immunol. 28 (2007), 207–212.
29. Langowski, J.L., Zhang, X., Wu, L., Mattson, J.D., Chen, T., Smith, K., Basham, B., McClanahan, T., Kastelein, R.A., Oft, M., IL-23 promotes tumour incidence and growth. Nature 442 (2006), 461–465.
30. Larkin, J., Chiarion-Sileni, V., Gonzalez, R., Grob, J.J., Cowey, C.L., Lao, C.D., Schadendorf, D., Dummer, R., Smylie, M., Rutkowski, P., et al. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N. Engl. J. Med. 373 (2015), 23–34.
31. Li, W., Kashiwamura, S., Ueda, H., Sekiyama, A., Okamura, H., Protection of CD8+ T cells from activation-induced cell death by IL-18. J. Leukoc. Biol. 82 (2007), 142–151.
32. Mackall, C.L., Fry, T.J., Gress, R.E., Harnessing the biology of IL-7 for therapeutic application. Nat. Rev. Immunol. 11 (2011), 330–342.
33. MacNeil, I.A., Suda, T., Moore, K.W., Mosmann, T.R., Zlotnik, A., IL-10, a novel growth cofactor for mature and immature T cells. J. Immunol. 145 (1990), 4167–4173.
34. Moore, K.W., de Waal Malefyt, R., Coffman, R.L., O'Garra, A., Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19 (2001), 683–765.
35. Mumm, J.B., Emmerich, J., Zhang, X., Chan, I., Wu, L., Mauze, S., Blaisdell, S., Basham, B., Dai, J., Grein, J., et al. IL-10 elicits IFNγ-dependent tumor immune surveillance. Cancer Cell 20 (2011), 781–796.
36. Naing, A., Papadopoulos, K.P., Autio, K.A., Ott, P.A., Patel, M.R., Wong, D.J., Falchook, G.S., Pant, S., Whiteside, M., Rasco, D.R., et al. Safety, antitumor activity, and immune activation of pegylated recombinant human interleukin-10 (AM0010) in patients with advanced solid tumors. J. Clin. Oncol. 34 (2016), 3562–3569.
37. Neven, B., Mamessier, E., Bruneau, J., Kaltenbach, S., Kotlarz, D., Suarez, F., Masliah-Planchon, J., Billot, K., Canioni, D., Frange, P., et al. A Mendelian predisposition to B-cell lymphoma caused by IL-10R deficiency. Blood 122 (2013), 3713–3722.
38. Oft, M., IL-10: master switch from tumor-promoting inflammation to antitumor immunity. Cancer Immunol. Res. 2 (2014), 194–199.
39. Park, J.H., Adoro, S., Lucas, P.J., Sarafova, S.D., Alag, A.S., Doan, L.L., Erman, B., Liu, X., Ellmeier, W., Bosselut, R., et al. ‘Coreceptor tuning’: cytokine signals transcriptionally tailor CD8 coreceptor expression to the self-specificity of the TCR. Nat. Immunol. 8 (2007), 1049–1059.
40. Pauken, K.E., Sammons, M.A., Odorizzi, P.M., Manne, S., Godec, J., Khan, O., Drake, A.M., Chen, Z., Sen, D.R., Kurachi, M., et al. Epigenetic stability of exhausted T cells limits durability of reinvigoration by PD-1 blockade. Science 354 (2016), 1160–1165.
41. Pedicord, V.A., Montalvo, W., Leiner, I.M., Allison, J.P., Single dose of anti-CTLA-4 enhances CD8+ T-cell memory formation, function, and maintenance. Proc. Natl. Acad. Sci. U S A 108 (2011), 266–271.
42. Rizvi, N.A., Hellmann, M.D., Snyder, A., Kvistborg, P., Makarov, V., Havel, J.J., Lee, W., Yuan, J., Wong, P., Ho, T.S., et al. Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 348 (2015), 124–128.
43. Robert, L., Harview, C., Emerson, R., Wang, X., Mok, S., Homet, B., Comin-Anduix, B., Koya, R.C., Robins, H., Tumeh, P.C., Ribas, A., Distinct immunological mechanisms of CTLA-4 and PD-1 blockade revealed by analyzing TCR usage in blood lymphocytes. Oncoimmunology, 3, 2014, e29244.
44. Rosenberg, S.A., Dudley, M.E., Adoptive cell therapy for the treatment of patients with metastatic melanoma. Curr. Opin. Immunol. 21 (2009), 233–240.
45. Shi, L.Z., Fu, T., Guan, B., Chen, J., Blando, J.M., Allison, J.P., Xiong, L., Subudhi, S.K., Gao, J., Sharma, P., Interdependent IL-7 and IFN-gamma signalling in T-cell controls tumour eradication by combined alpha-CTLA-4+alpha-PD-1 therapy. Nat. Commun., 7, 2016, 12335.
46. Subudhi, S.K., Aparicio, A., Gao, J., Zurita, A.J., Araujo, J.C., Logothetis, C.J., Tahir, S.A., Korivi, B.R., Slack, R.S., Vence, L., et al. Clonal expansion of CD8 T cells in the systemic circulation precedes development of ipilimumab-induced toxicities. Proc. Natl. Acad. Sci. U S A 113 (2016), 11919–11924.
47. Tran, E., Ahmadzadeh, M., Lu, Y.C., Gros, A., Turcotte, S., Robbins, P.F., Gartner, J.J., Zheng, Z., Li, Y.F., Ray, S., et al. Immunogenicity of somatic mutations in human gastrointestinal cancers. Science 350 (2015), 1387–1390.
48. Tumeh, P.C., Harview, C.L., Yearley, J.H., Shintaku, I.P., Taylor, E.J., Robert, L., Chmielowski, B., Spasic, M., Henry, G., Ciobanu, V., et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 515 (2014), 568–571.
49. van de Veerdonk, F.L., Netea, M.G., Dinarello, C.A., Joosten, L.A., Inflammasome activation and IL-1beta and IL-18 processing during infection. Trends Immunol. 32 (2011), 110–116.
50. Wherry, E.J., Kurachi, M., Molecular and cellular insights into T cell exhaustion. Nat. Rev. Immunol. 15 (2015), 486–499.