Circulating IL-15 exists as heterodimeric complex with soluble IL-15Rα in human and mouse serum

Blood

Volumn 120, Issue 1, 2012, Pages

  Bergamaschi, Cristina ^a   Bear, Jenifer ^b   Rosati, Margherita ^a   Beach, Rachel Kelly ^a,b   Alicea, Candido ^b   Sowder, Raymond ^c   Chertova, Elena ^c   Rosenberg, Steven A ^d   Felber, Barbara K ^b   Pavlakis, George N ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^c SAIC FREDERICK INC   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HETERODIMER; INTERLEUKIN 15; INTERLEUKIN 15 RECEPTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD ANALYSIS; CANCER PATIENT; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; HUMAN CELL; HYPOTHESIS; IMMUNOASSAY; LYMPHOCYTOPENIA; MELANOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PURIFICATION; PROTEIN SECRETION;

EID: 84863562572     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-10-384362     Document Type: Article

References (50)

1. Burton JD, Bamford RN, Peters C, et al. A lymphokine, provisionally designated interleukin T and produced by a human adult T-cell leukemia line, stimulates T-cell proliferation and the induction of lymphokine-activated killer cells. Proc Natl Acad Sci U S A. 1994;91(11):4935-4939. (Pubitemid 24177765)
2. Grabstein KH, Eisenman J, Shanebeck K, et al. Cloning of a T cell growth factor that interacts with the beta chain of the interleukin-2 receptor. Science. 1994;264(5161):965-968. (Pubitemid 24196167)
3. Berard M, Brandt K, Bulfone-Paus S, Tough DF. IL-15 promotes the survival of naive and memory phenotype CD8+ T cells. J Immunol. 2003; 170(10):5018-5026. (Pubitemid 36554732)
4. Carson WE, Giri JG, Lindemann MJ, et al. Interleukin (IL) 15 is a novel cytokine that activates human natural killer cells via components of the IL-2 receptor. J Exp Med. 1994;180(4):1395-1403. (Pubitemid 24289613)
5. Ma A, Koka R, Burkett P. Diverse functions of IL-2, IL-15, and IL-7 in lymphoid homeostasis. Annu Rev Immunol. 2006;24:657-679.
6. Zhang X, Sun S, Hwang I, Tough DF, Sprent J. Potent and selective stimulation of memoryphenotype CD8+ T cells in vivo by IL-15. Immunity. 1998;8(5):591-599. (Pubitemid 28264750)
7. Giri JG, Ahdieh M, Eisenman J, et al. Utilization of the beta and gamma chains of the IL-2 receptor by the novel cytokine IL-15. EMBO J. 1994; 13(12):2822-2830. (Pubitemid 24191692)
8. Kennedy MK, Glaccum M, Brown SN, et al. Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J Exp Med. 2000;191(5):771-780.
9. Lodolce JP, Boone DL, Chai S, et al. IL-15 receptor maintains lymphoid homeostasis by supporting lymphocyte homing and proliferation. Immunity. 1998;9(5):669-676. (Pubitemid 28557595)
10. Schorle H, Holtschke T, Hunig T, Schimpl A, Horak I. Development and function of T cells in mice rendered interleukin-2 deficient by gene targeting. Nature. 1991;352(6336):621-624. (Pubitemid 21912393)
11. Sadlack B, Merz H, Schorle H, Schimpl A, Feller AC, Horak I. Ulcerative colitis-like disease in mice with a disrupted interleukin-2 gene. Cell. 1993;75(2):253-261. (Pubitemid 23320289)
12. Sharfe N, Dadi HK, Shahar M, Roifman CM. Human immune disorder arising from mutation of the alpha chain of the interleukin-2 receptor. Proc Natl Acad Sci U S A. 1997;94(7):3168-3171. (Pubitemid 27157282)
13. Caudy AA, Reddy ST, Chatila T, Atkinson JP, Verbsky JW. CD25 deficiency causes an immune dysregulation, polyendocrinopathy, enteropathy, X-linked-like syndrome, and defective IL-10 expression from CD4 lymphocytes. J Allergy Clin Immunol. 2007;119(2):482-487. (Pubitemid 46204802)
14. Waldmann TA. The biology of interleukin-2 and interleukin-15: implications for cancer therapy and vaccine design. Nat Rev Immunol. 2006;6(8): 595-601. (Pubitemid 44134092)
15. Giri JG, Kumaki S, Ahdieh M, et al. Identification and cloning of a novel IL-15 binding protein that is structurally related to the alpha chain of the IL-2 receptor. EMBO J. 1995;14(15):3654-3663.
16. Dubois S, Mariner J, Waldmann TA, Tagaya Y. IL-15Ralpha recycles and presents IL-15 in trans to neighboring cells. Immunity. 2002;17(5):537-547. (Pubitemid 35351500)
17. Burkett PR, Koka R, Chien M, Chai S, Boone DL, Ma A. Coordinate expression and trans presentation of interleukin (IL)-15Ralpha and IL-15 supports natural killer cell and memory CD8+ T cell homeostasis. J Exp Med. 2004;200(7):825-834. (Pubitemid 39362919)
18. Koka R, Burkett PR, Chien M, et al. Interleukin (IL)-15Ralpha-deficient natural killer cells survive in normal but not IL-15Ralpha-deficient mice. J Exp Med. 2003;197(8):977-984. (Pubitemid 36523195)
19. Sandau MM, Schluns KS, Lefrancois L, Jameson SC. Cutting edge: transpresentation of IL-15 by bone marrow-derived cells necessitates expression of IL-15 and IL-15Ralpha by the same cells. J Immunol. 2004; 173(11):6537-6541. (Pubitemid 39541036)
20. Schluns KS, Klonowski KD, Lefrancois L. Transregulation of memory CD8 T-cell proliferation by IL-15Ralpha+ bone marrow-derived cells. Blood. 2004;103(3):988-994. (Pubitemid 38129561)
21. Bergamaschi C, Jalah R, Kulkarni V, et al. Secretion and biological activity of short signal peptide IL-15 is chaperoned by IL-15 receptor alpha in vivo. J Immunol. 2009;183(5):3064-3072.
22. Bergamaschi C, Rosati M, Jalah R, et al. Intracellular interaction of interleukin-15 with its receptor alpha during production leads to mutual stabilization and increased bioactivity. J Biol Chem. 2008; 283(7):4189-4199.
23. Dubois S, Patel HJ, Zhang M, Waldmann TA, Muller JR. Preassociation of IL-15 with IL-15R alpha-IgG1-Fc enhances its activity on proliferation of NK and CD8+/CD44high T cells and its antitumor action. J Immunol. 2008;180(4):2099- 2106.
24. Rubinstein MP, Kovar M, Purton JF, et al. Converting IL-15 to a superagonist by binding to soluble IL-15Ralpha. Proc Natl Acad Sci U S A. 2006;103(24):9166-9171. (Pubitemid 43902550)
25. Stoklasek TA, Schluns KS, Lefrancois L. Combined IL-15/IL-15Ralpha immunotherapy maximizes IL-15 activity in vivo. J Immunol. 2006; 177(9):6072-6080. (Pubitemid 44628822)
26. Mortier E, Quemener A, Vusio P, et al. Soluble interleukin-15 receptor alpha (IL-15Ralpha)-sushi as a selective and potent agonist of IL-15 action through IL-15Rbeta/gamma: hyperagonist IL-15 x IL-15R alpha fusion proteins. J Biol Chem. 2006; 281(3):1612-1619.
27. Dudley ME, Yang JC, Sherry R, et al. Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. J Clin Oncol. 2008;26(32):5233-5239.
28. Jalah R, Rosati M, Kulkarni V, et al. Efficient systemic expression of bioactive IL-15 in mice upon delivery of optimized DNA expression plasmids. DNA Cell Biol. 2007;26(12):827-840. (Pubitemid 350274411)
29. Dubois S, Magrangeas F, Lehours P, et al. Natural splicing of exon 2 of human interleukin-15 receptor alpha-chain mRNA results in a shortened form with a distinct pattern of expression. J Biol Chem. 1999;274(38):26978-26984.
30. Kurys G, Tagaya Y, Bamford R, Hanover JA, Waldmann TA. The long signal peptide isoform and its alternative processing direct the intracellular trafficking of interleukin-15. J Biol Chem. 2000;275(39):30653-30659.
31. Boyiadzis M, Memon S, Carson J, et al. Upregulation of NK cell activating receptors following allogeneic hematopoietic stem cell transplantation under a lymphodepleting reduced intensity regimen is associated with elevated IL-15 levels. Biol Blood Marrow Transplant. 2008;14(3):290-300. (Pubitemid 351218196)
32. Gattinoni L, Finkelstein SE, Klebanoff CA, et al. Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumor-specific CD8+ T cells. J Exp Med. 2005;202(7):907-912. (Pubitemid 41396891)
33. Duitman EH, Orinska Z, Bulanova E, Paus R, Bulfone-Paus S. How a cytokine is chaperoned through the secretory pathway by complexing with its own receptor: lessons from interleukin-15 (IL-15)/IL-15 receptor alpha. Mol Cell Biol. 2008; 28(15):4851-4861.
34. Mortier E, Woo T, Advincula R, Gozalo S, Ma A. IL-15Ralpha chaperones IL-15 to stable dendritic cell membrane complexes that activate NK cells via trans presentation. J Exp Med. 2008;205(5): 1213-1225. (Pubitemid 351679694)
35. Salem ML, Kadima AN, El-Naggar SA, et al. Defining the ability of cyclophosphamide preconditioning to enhance the antigen-specific CD8+ T-cell response to peptide vaccination: creation of a beneficial host microenvironment involving type I IFNs and myeloid cells. J Immunother. 2007; 30(1):40-53. (Pubitemid 46052202)
36. Neely GG, Robbins SM, Amankwah EK, et al. Lipopolysaccharide-stimulated or granulocytemacrophage colony-stimulating factor-stimulated monocytes rapidly express biologically active IL-15 on their cell surface independent of new protein synthesis. J Immunol. 2001;167(9):5011-5017. (Pubitemid 33009733)
37. Bracci L, Moschella F, Sestili P, et al. 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. 2007;13(2):644-653. (Pubitemid 46225372)
38. Adrain C, Zettl M, Christova Y, Taylor N, Freeman M. Tumor necrosis factor signaling requires iRhom2 to promote trafficking and activation of TACE. Science. 335(6065):225-228.
39. Huntington ND, Legrand N, Alves NL, et al. IL-15 trans-presentation promotes human NK cell development and differentiation in vivo. J Exp Med. 2009;206(1):25-34.
40. Lucas M, Schachterle W, Oberle K, Aichele P, Diefenbach A. Dendritic cells prime natural killer cells by trans-presenting interleukin 15. Immunity. 2007;26(4):503-517. (Pubitemid 46602996)
41. Ma LJ, Acero LF, Zal T, Schluns KS. Transpresentation of IL-15 by intestinal epithelial cells drives development of CD8alphaalpha IELs. J Immunol. 2009;183(2):1044-1054.
42. Sato N, Patel HJ, Waldmann TA, Tagaya Y. The IL-15/IL-15Ralpha on cell surfaces enables sustained IL-15 activity and contributes to the long survival of CD8 memory T cells. Proc Natl Acad Sci U S A. 2007;104(2):588-593. (Pubitemid 46123069)
43. Stonier SW, Ma LJ, Castillo EF, Schluns KS. Dendritic cells drive memory CD8 T-cell homeostasis via IL-15 transpresentation. Blood. 2008;112(12): 4546-4554.
44. Mortier E, Advincula R, Kim L, et al. Macrophage-and dendritic-cell- derived interleukin-15 receptor alpha supports homeostasis of distinct CD8 T cell subsets. Immunity. 2009;31(5):811-822.
45. Huntington ND, Alves NL, Legrand N, et al. IL-15 transpresentation promotes both human T-cell reconstitution and T-cell-dependent antibody responses in vivo. Proc Natl Acad Sci U S A. 108(15):6217-6222.
46. Huntington N, Alves N, Legrand N, et al. Autonomous and extrinsic regulation of thymopoiesis in human immune system (HIS) mice. Eur J Immunol. 2011;41(10):2883-2893.
47. Berger C, Berger M, Hackman RC, et al. Safety and immunologic effects of IL-15 administration in nonhuman primates. Blood. 2009;114(12):2417-2426.
48. Lugli E, Goldman CK, Perera LP, et al. Transient and persistent effects of IL-15 on lymphocyte homeostasis in nonhuman primates. Blood. 2010; 116(17):3238-3248.
49. Waldmann TA, Lugli E, Roederer M, et al. Safety (toxicity), pharmacokinetics, immunogenicity, and impact on elements of the normal immune system of recombinant human IL-15 in rhesus macaques. Blood. 2011;117(18):4787-4795.
50. Picker LJ, Reed-Inderbitzin EF, Hagen SI, et al. IL-15 induces CD4 effector memory T cell production and tissue emigration in nonhuman primates. J Clin Invest. 2006;116(6):1514-1524.