Soluble interleukin-15 complexes are generated in vivo by type i interferon dependent and independent pathways

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Anthony, Scott M ^a,b   Howard, Megan E ^a   Hailemichael, Yared ^a   Overwijk, Willem W ^a,b   Schluns, Kimberly S ^a,b  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAM PROTEIN; ADAM17 PROTEIN; ALPHA INTERFERON; BETA INTERFERON; CD40 ANTIGEN; INTERFERON; INTERLEUKIN 15; POLYINOSINIC POLYCYTIDYLIC ACID; UNCLASSIFIED DRUG; ALPHA BETA INTERFERON RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW DERIVED DENDRITIC CELL; CELL SURFACE; COMPLEX FORMATION; CONTROLLED STUDY; GENE EXPRESSION; IN VIVO STUDY; INTERFERON INDUCTION; INTERFERON PRODUCTION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; VESICULAR STOMATITIS; WHOLE BODY RADIATION; ANIMAL; BLOOD; C57BL MOUSE; CELL CULTURE; DENDRITIC CELL; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY;

MUS; VESICULAR STOMATITIS VIRUS;

ANIMALS; ANTIGENS, CD40; CELLS, CULTURED; DENDRITIC CELLS; INTERFERON-ALPHA; INTERLEUKIN-15; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTOR, INTERFERON ALPHA-BETA; VESICULAR STOMATITIS; WHOLE-BODY IRRADIATION;

EID: 84924368722     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0120274     Document Type: Article

References (46)

1. Kennedy MK, Glaccum M, Brown SN, Butz EA, Viney JL, Embers M, et al.(2000) Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J Exp Med 191: 771-780. PMID: 10704459
2. Lodolce JP, Boone DL, Chai S, Swain RE, Dassopoulos T, Trettin S, et al. (1998) IL-15 receptor maintains lymphoid homeostasis by supporting lymphocyte homing and proliferation. Immunity 9: 669-676. PMID: 9846488
3. Bamford RN, DeFilippis AP, Azimi N, Kurys G, Waldmann TA (1998) The 5' untranslated region, signal peptide, and the coding sequence of the carboxyl terminus of IL-15 participate in its multifaceted translational control. J Immunol 160: 4418-4426. PMID: 9574546
4. Bamford RN, Battiata AP, Waldmann TA (1996) IL-15: the role of translational regulation in their expression. J Leukoc Biol 59: 476-480. PMID: 8613692
5. Nishimura H, Yajima T, Naiki Y, Tsunobuchi H, Umemura M, Itano K, et al. (2000) Differential roles of interleukin 15 mRNA isoforms generated by alternative splicing in immune responses in vivo. J Exp Med 191: 157-170. PMID: 10620614
6. Dubois S, Mariner J, Waldmann TA, Tagaya Y (2002) IL-15Ralpha recycles and presents IL-15 In trans to neighboring cells. Immunity 17: 537-547. PMID: 12433361
7. Mortier E, Woo T, Advincula R, Gozalo S, Ma A (2008) IL-15Ralpha chaperones IL-15 to stable dendritic cell membrane complexes that activate NK cells via trans presentation. J Exp Med 205: 1213-1225. doi: 10.1084/jem.20071913 PMID: 18458113
8. Mortier E, Advincula R, Kim L, Chmura S, Barrera J, Reizis B, et al. (2009) Macrophage- and dendritic-cell-derived interleukin-15 receptor alpha supports homeostasis of distinct CD8(+) T cell subsets. Immunity 31: 811-822. doi: 10.1016/j.immuni.2009.09.017 PMID: 19913445
9. Castillo EF, Schluns KS (2012) Regulating the immune system via IL-15 transpresentation. Cytokine 59: 479-490. doi: 10.1016/j.cyto.2012.06.017 PMID: 22795955
10. Bergamaschi C, Bear J, Rosati M, Kelly BR, Alicea C, Sowder R, et al. (2012) Circulating interleukin-15 (IL-15) exists as heterodimeric complex with soluble IL-15 receptor alpha (IL-15Ralpha) in human serum. Blood 120: 1-8. doi: 10.1182/blood-2012-04-425306 PMID: 22767572
11. Stoklasek TA, Schluns KS, Lefrancois L (2006) Combined IL-15/IL-15Ralpha immunotherapy maximizes IL-15 activity in vivo. J Immunol 177: 6072-6080. PMID: 17056533
12. Rubinstein MP, Kovar M, Purton JF, Cho JH, Boyman O, Surh CD, et al. (2006) Converting IL-15 to a superagonist by binding to soluble IL-15R{alpha}. Proc Natl Acad Sci U S A 103: 9166-9171. PMID: 16757567
13. McInnes IB, al-Mughales J, Field M, Leung BP, Huang FP, Dixon R, et al. (1996) The role of interleukin-15 in T-cell migration and activation in rheumatoid arthritis. Nat Med 2: 175-182. PMID: 8574962
14. Villadsen LS, Schuurman J, Beurskens F, Dam TN, Dagnaes-Hansen F, Skov L, et al. (2003) Resolution of psoriasis upon blockade of IL-15 biological activity in a xenograft mouse model. J Clin Invest 112: 1571-1580. PMID: 14617758
15. Sakai T, Kusugami K, Nishimura H, Ando T, Yamaguchi T, Ohsuga M, et al. (1998) Interleukin 15 activity in the rectal mucosa of inflammatory bowel disease. Gastroenterology 114: 1237-1243. PMID: 9609761
16. Nishimura H, Hiromatsu K, Kobayashi N, Grabstein KH, Paxton R, Sugamura K, et al. (1996) IL-15 is a novel growth factor for murine gamma delta T cells induced by Salmonella infection. J Immunol 156: 663-669. PMID: 8543818
17. Mitani A, Nishimura H, Hirose K, Washizu J, Kimura Y, Tanaka S, et al. (1999) Interleukin-15 production at the early stage after oral infection with Listeria monocytogenes in mice. Immunology 97: 92-99. PMID: 10447719
18. Colpitts SL, Stoklasek TA, Plumlee CR, Obar JJ, Guo C, Lefrancois L (2012) Cutting Edge: The role of IFN-alpha receptor and MyD88 signaling in induction of IL-15 expression in vivo. J Immunol 188: 2483-2487. doi: 10.4049/jimmunol.1103609 PMID: 22327071
19. Zhang X, Sun S, Hwang I, Tough DF, Sprent J (1998) Potent and selective stimulation of memory-phenotype CD8+ T cells in vivo by IL-15. Immunity 8: 591-599. PMID: 9620680
20. Mattei F, Schiavoni G, Belardelli F, Tough DF (2001) IL-15 is expressed by dendritic cells in response to type I IFN, double-stranded RNA, or lipopolysaccharide and promotes dendritic cell activation. J Immunol 167: 1179-1187. PMID: 11466332
21. Doherty TM, Seder RA, Sher A (1996) Induction and regulation of IL-15 expression in murine macrophages. J Immunol 156: 735-741. PMID: 8543827
22. Tough DF, Borrow P, Sprent J (1996) Induction of bystander T cell proliferation by viruses and type I interferon in vivo. Science 272: 1947-1950. PMID: 8658169
23. Dubois SP, Waldmann TA, Muller JR (2005) Survival adjustment of mature dendritic cells by IL-15. Proc Natl Acad Sci U S A 102: 8662-8667. PMID: 15932944
24. Sikora AG, Jaffarzad N, Hailemichael Y, Gelbard A, Stonier SW, Schluns KS, et al. (2009) IFN-alpha enhances peptide vaccine-induced CD8+ T cell numbers, effector function, and antitumor activity. J Immunol 182: 7398-7407. doi: 10.4049/jimmunol.0802982 PMID: 19494262
25. Lodolce JP, Burkett PR, Boone DL, Chien M, Ma A (2001) T cell-independent interleukin 15Ralpha signals are required for bystander proliferation. J Exp Med 194: 1187-1194. PMID: 11602647
26. Zhang M, Ju W, Yao Z, Yu P, Wei BR, Simpson RM, et al. (2012) Augmented IL-15Ralpha expression by CD40 activation is critical in synergistic CD8 T cell-mediated antitumor activity of anti-CD40 antibody with IL-15 in TRAMP-C2 tumors in mice. J Immunol 188: 6156-6164. doi: 10.4049/jimmunol.1102604 PMID: 22593619
27. Horiuchi K, Kimura T, Miyamoto T, Takaishi H, Okada Y, Toyama Y, et al. (2007) Cutting edge: TNF-alpha-converting enzyme (TACE/ADAM17) inactivation in mouse myeloid cells prevents lethality from endotoxin shock. J Immunol 179: 2686-2689. PMID: 17709479
28. Weskamp G, Mendelson K, Swendeman S, Le GS, Ma Y, Lyman S, et al. (2010) Pathological neovascularization is reduced by inactivation of ADAM17 in endothelial cells but not in pericytes. Circ Res 106: 932-940. doi: 10.1161/CIRCRESAHA.109.207415 PMID: 20110534
29. Stonier SW, Ma LJ, Castillo EF, Schluns KS (2008) Dendritic cells drive memory CD8 T cell homeostasis via IL-15 trans-presentation. Blood 4546-4554. doi: 10.1182/blood-2008-05-156307 PMID: 18812469
30. Castillo EF, Stonier SW, Frasca L, Schluns KS (2009) Dendritic cells support the in vivo development and maintenance of NK cells via IL-15 trans-presentation. J Immunol 183: 4948-4956. doi: 10.4049/ jimmunol.0900719 PMID: 19786554
31. Colpitts SL, Stonier SW, Stoklasek TA, Root SH, Aguila HL, Schluns KS, Lefrancois L (2013) Transcriptional regulation of IL-15 expression during hematopoiesis. J Immunol 191: 3017-3024. doi: 10.4049/ jimmunol.1301389 PMID: 23966624
32. Mortier E, Bernard J, Plet A, Jacques Y (2004) Natural, proteolytic release of a soluble form of human IL-15 receptor alpha-chain that behaves as a specific, high affinity IL-15 antagonist. J Immunol 173: 1681-1688. PMID: 15265897
33. Khawam K, Giron-Michel J, Gu Y, Perier A, Giuliani M, Caignard A, et al. (2009) Human renal cancer cells express a novel membrane-bound interleukin-15 that induces, in response to the soluble interleu-kin-15 receptor alpha chain, epithelial-to-mesenchymal transition. Cancer Res 69: 1561-1569. doi: 10. 1158/0008-5472.CAN-08-3198 PMID: 19190330
34. McIlwain DR, Lang PA, Maretzky T, Hamada K, Ohishi K, Maney SK, et al. (2012) iRhom2 regulation of TACE controls TNF-mediated protection against Listeria and responses to LPS. Science 335: 229-232. doi: 10.1126/science.1214448 PMID: 22246778
35. Burnette BC, Liang H, Lee Y, Chlewicki L, Khodarev NN, Weichselbaum RR, et al. (2011) The efficacy of radiotherapy relies upon induction of type i interferon-dependent innate and adaptive immunity. Cancer Res 71: 2488-2496. doi: 10.1158/0008-5472.CAN-10-2820 PMID: 21300764
36. Verbist KC, Cole CJ, Field MB, Klonowski KD (2011) A role for IL-15 in the migration of effector CD8 T cells to the lung airways following influenza infection. J Immunol 186: 174-182. doi: 10.4049/jimmunol. 1002613 PMID: 21098221
37. Bauer JW, Baechler EC, Petri M, Batliwalla FM, Crawford D, Ortmann WA, et al. (2006) Elevated serum levels of interferon-regulated chemokines are biomarkers for active human systemic lupus erythematosus. PLoS Med 3: e491. PMID: 17177599
38. Nestle FO, Gilliet M (2005) Defining upstream elements of psoriasis pathogenesis: an emerging role for interferon alpha. J Invest Dermatol 125: xiv-xxv. PMID: 16354174
39. Colonna M, Trinchieri G, Liu YJ (2004) Plasmacytoid dendritic cells in immunity. Nat Immunol 5: 1219-1226. PMID: 15549123
40. Black RA, Rauch CT, Kozlosky CJ, Peschon JJ, Slack JL, Wolfson MF, et al. (1997) A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature 385: 729-733. PMID: 9034190
41. Caescu CI, Jeschke GR, Turk BE (2009) Active-site determinants of substrate recognition by the metalloproteinases TACE and ADAM10. Biochem J 424: 79-88. doi: 10.1042/BJ20090549 PMID: 19715556
42. Tamzalit F, Barbieux I, Plet A, Heim J, Nedellec S, Morisseau S, et al. (2014) IL-15.IL-15Ralpha complex shedding following trans-presentation is essential for the survival of IL-15 responding NK and T cells. Proc Natl Acad Sci U S A 111: 8565-8570. doi: 10.1073/pnas.1405514111 PMID: 24912180
43. Gattinoni L, Finkelstein SE, Klebanoff CA, Antony PA, Palmer DC, Spiess PJ, et al. (2005) Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumorspecific CD8+ T cells. J Exp Med 202: 907-912. PMID: 16203864
44. Sandau MM, Winstead CJ, Jameson SC (2007) IL-15 is required for sustained lymphopenia-driven proliferation and accumulation of CD8 T cells. J Immunol 179: 120-125. PMID: 17579029
45. Schluns KS, Kieper WC, Jameson SC, Lefrancois L (2000) Interleukin-7 mediates the homeostasis of naive and memory CD8 T cells in vivo. Nature Immunology 1: 426-432. PMID: 11062503
46. Klebanoff CA, Finkelstein SE, Surman DR, Lichtman MK, Gattinoni L, Theoret MR, et al. (2004) IL-15 enhances the in vivo antitumor activity of tumor-reactive CD8+ T cells. Proc Natl Acad Sci U S A 101: 1969-1974. PMID: 14762166