Adipocyte IL-15 regulates local and systemic NK cell development

Journal of Immunology

Volumn 193, Issue 4, 2014, Pages 1747-1758

  Liou, Yae Huei ^a,b   Wang, Szu Wen ^b   Chang, Chin Ling ^b   Huang, Po Lin ^b   Hou, Mau Sheng ^b   Lai, Yein Gei ^b   Lee, Gilbert Aaron ^b   Jiang, Si Tse ^b   Tsai, Ching Yen ^b   Liao, Nan Shih ^a,b  

^a NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^b INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 15;

ADIPOCYTE; ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL FATE; CELL MATURATION; CELLULAR DISTRIBUTION; CELLULAR IMMUNITY; CHIMERA; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; EPIDIDYMIS FAT; GENE CONTROL; HEMATOPOIETIC SYSTEM; HOMEOSTASIS; IL15 GENE; KNOCKOUT MOUSE; LIVER; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE FUNCTION; LYMPHOID PROGENITOR CELL; MALE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PARENCHYMA; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; SPLEEN; STEM CELL NICHE; TISSUE DISTRIBUTION; TISSUE TRANSPLANTATION;

ADIPOCYTES; ADIPOSE TISSUE; ADOPTIVE TRANSFER; ANIMALS; BONE MARROW CELLS; CELL DIFFERENTIATION; DENDRITIC CELLS; HOMEOSTASIS; INTERLEUKIN-15; KILLER CELLS, NATURAL; LIVER; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY A; RECEPTORS, IMMUNOLOGIC; RNA, MESSENGER; SPLEEN;

EID: 84905964126     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400868     Document Type: Article

References (60)

1. Vivier, E., E. Tomasello, M. Baratin, T. Walzer, and S. Ugolini. 2008. Functions of natural killer cells. Nat. Immunol. 9: 503-510.
2. Vivier, E., D. H. Raulet, A. Moretta, M. A. Caligiuri, L. Zitvogel, L. L. Lanier, W. M. Yokoyama, and S. Ugolini. 2011. Innate or adaptive immunity? The example of natural killer cells. Science 331: 44-49.
3. Barber, G. N. 2001. Host defense, viruses and apoptosis. Cell Death Differ. 8: 113-126.
4. Martín-Fontecha, A., L. L. Thomsen, S. Brett, C. Gerard, M. Lipp, A. Lanzavecchia, and F. Sallusto. 2004. Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat. Immunol. 5: 1260-1265.
5. Sun, J. C., J. N. Beilke, and L. L. Lanier. 2009. Adaptive immune features of natural killer cells. Nature 457: 557-561.
6. Rölle, A., J. Pollmann, and A. Cerwenka. 2013. Memory of infections: an emerging role for natural killer cells. PLoS Pathog. 9: e1003548.
7. Carotta, S., S. H. Pang, S. L. Nutt, and G. T. Belz. 2011. Identification of the earliest NK-cell precursor in the mouse BM. Blood 117: 5449-5452.
8. Rosmaraki, E. E., I. Douagi, C. Roth, F. Colucci, A. Cumano, and J. P. Di Santo. 2001. Identification of committed NK cell progenitors in adult murine bone marrow. Eur. J. Immunol. 31: 1900-1909.
9. Fathman, J. W., D. Bhattacharya, M. A. Inlay, J. Seita, H. Karsunky, and I. L. Weissman. 2011. Identification of the earliest natural killer cell-committed progenitor in murine bone marrow. Blood 118: 5439-5447.
10. Yu, J., A. G. Freud, and M. A. Caligiuri. 2013. Location and cellular stages of natural killer cell development. Trends Immunol. 34: 573-582.
11. Hayakawa, Y., and M. J. Smyth. 2006. CD27 dissects mature NK cells into two subsets with distinct responsiveness and migratory capacity. J. Immunol. 176: 1517-1524.
12. Chiossone, L., J. Chaix, N. Fuseri, C. Roth, E. Vivier, and T. Walzer. 2009. Maturation of mouse NK cells is a 4-stage developmental program. Blood 113: 5488-5496.
13. Dorfman, J. R., and D. H. Raulet. 1998. Acquisition of Ly49 receptor expression by developing natural killer cells. J. Exp. Med. 187: 609-618.
14. Kim, S., K. Iizuka, H. S. Kang, A. Dokun, A. R. French, S. Greco, and W. M. Yokoyama. 2002. In vivo developmental stages in murine natural killer cell maturation. Nat. Immunol. 3: 523-528.
15. Campbell, K. S., and J. Hasegawa. 2013. Natural killer cell biology: an update and future directions. J. Allergy Clin. Immunol. 132: 536-544.
16. Yokoyama, W. M., and S. Kim. 2006. Licensing of natural killer cells by selfmajor histocompatibility complex class I. Immunol. Rev. 214: 143-154.
17. Bessoles, S., G. S. Angelov, J. Back, G. Leclercq, E. Vivier, and W. Held. 2013. Education of murine NK cells requires both cis and trans recognition of MHC class I molecules. J. Immunol. 191: 5044-5051.
18. Vosshenrich, C. A., T. Ranson, S. I. Samson, E. Corcuff, F. Colucci, E. E. Rosmaraki, and J. P. Di Santo. 2005. Roles for common cytokine receptor gamma-chain-dependent cytokines in the generation, differentiation, and maturation of NK cell precursors and peripheral NK cells in vivo. J. Immunol. 174: 1213-1221.
19. Luther, C., K. Warner, and F. Takei. 2011. Unique progenitors in mouse lymph node develop into CD127+ NK cells: thymus-dependent and thymusindependent pathways. Blood 117: 4012-4021.
20. Tang, Y., C. Peitzsch, H. N. Charoudeh, M. Cheng, P. Chaves, S. E. Jacobsen, and E. Sitnicka. 2012. Emergence of NK-cell progenitors and functionally competent NK-cell lineage subsets in the early mouse embryo. Blood 120: 63-75.
21. Colucci, F., M. A. Caligiuri, and J. P. Di Santo. 2003. What does it take to make a natural killer? Nat. Rev. Immunol. 3: 413-425.
22. Caspar-Bauguil, S., B. Cousin, A. Galinier, C. Segafredo, M. Nibbelink, M. André, L. Casteilla, and L. Pénicaud. 2005. Adipose tissues as an ancestral immune organ: site-specific change in obesity. FEBS Lett. 579: 3487-3492.
23. Andrews, D. M., and M. J. Smyth. 2010. A potential role for RAG-1 in NK cell development revealed by analysis of NK cells during ontogeny. Immunol. Cell Biol. 88: 107-116.
24. Tessmer, M. S., E. C. Reilly, and L. Brossay. 2011. Salivary gland NK cells are phenotypically and functionally unique. PLoS Pathog. 7: e1001254.
25. Gonzaga, R., P. Matzinger, and A. Perez-Diez. 2011. Resident peritoneal NK cells. J. Immunol. 187: 6235-6242.
26. Wu, X., Y. Chen, H. Wei, R. Sun, and Z. Tian. 2012. Development of murine hepatic NK cells during ontogeny: comparison with spleen NK cells. Clin. Dev. Immunol. 2012: 759765.
27. Carrega, P., I. Bonaccorsi, E. Di Carlo, B. Morandi, P. Paul, V. Rizzello, G. Cipollone, G. Navarra, M. C. Mingari, L. Moretta, and G. Ferlazzo. 2014. CD56(bright)perforin(low) noncytotoxic human NK cells are abundant in both healthy and neoplastic solid tissues and recirculate to secondary lymphoid organs via afferent lymph. J. Immunol. 192: 3805-3815.
28. Male, V., I. Nisoli, T. Kostrzewski, D. S. Allan, J. R. Carlyle, G. M. Lord, A. Wack, and H. J. Brady. 2014. The transcription factor E4bp4/Nfil3 controls commitment to the NK lineage and directly regulates Eomes and Id2 expression. J. Exp. Med. 211: 635-642.
29. Mortier, E., T. Woo, R. Advincula, S. Gozalo, and A. Ma. 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.
30. Bergamaschi, C., J. Bear, M. Rosati, R. K. Beach, C. Alicea, R. Sowder, E. Chertova, S. A. Rosenberg, B. K. Felber, and G. N. Pavlakis. 2012. Circulating IL-15 exists as heterodimeric complex with soluble IL-15Ra in human and mouse serum. Blood 120: e1-e8.
31. Dubois, S., J. Mariner, T. A. Waldmann, and Y. Tagaya. 2002. IL-15Ralpha recycles and presents IL-15 In trans to neighboring cells. Immunity 17: 537-547.
32. Kobayashi, H., S. Dubois, N. Sato, H. Sabzevari, Y. Sakai, T. A. Waldmann, and Y. Tagaya. 2005. Role of trans-cellular IL-15 presentation in the activation of NK cell-mediated killing, which leads to enhanced tumor immunosurveillance. Blood 105: 721-727.
33. Lodolce, J. P., D. L. Boone, S. Chai, R. E. Swain, T. Dassopoulos, S. Trettin, and A. Ma. 1998. IL-15 receptor maintains lymphoid homeostasis by supporting lymphocyte homing and proliferation. Immunity 9: 669-676.
34. Kennedy, M. K., M. Glaccum, S. N. Brown, E. A. Butz, J. L. Viney, M. Embers, N. Matsuki, K. Charrier, L. Sedger, C. R. Willis, 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.
35. Cooper, M. A., J. E. Bush, T. A. Fehniger, J. B. VanDeusen, R. E. Waite, Y. Liu, H. L. Aguila, and M. A. Caligiuri. 2002. In vivo evidence for a dependence on interleukin 15 for survival of natural killer cells. Blood 100: 3633-3638.
36. Ranson, T., C. A. Vosshenrich, E. Corcuff, O. Richard, W. Müller, and J. P. Di Santo. 2003. IL-15 is an essential mediator of peripheral NK-cell homeostasis. Blood 101: 4887-4893.
37. Sandau, M. M., K. S. Schluns, L. Lefrancois, and S. C. Jameson. 2004. Cutting edge: transpresentation of IL-15 by bone marrow-derived cells necessitates expression of IL-15 and IL-15R alpha by the same cells. J. Immunol. 173: 6537-6541.
38. Schluns, K. S., E. C. Nowak, A. Cabrera-Hernandez, L. Puddington, L. Lefrançois, and H. L. Aguila. 2004. Distinct cell types control lymphoid subset development by means of IL-15 and IL-15 receptor alpha expression. Proc. Natl. Acad. Sci. USA 101: 5616-5621.
39. Mortier, E., R. Advincula, L. Kim, S. Chmura, J. Barrera, B. Reizis, B. A. Malynn, and A. Ma. 2009. Macrophage-And dendritic-cell-derived interleukin-15 receptor alpha supports homeostasis of distinct CD8+ T cell subsets. Immunity 31: 811-822.
40. Soderquest, K., N. Powell, C. Luci, N. Van Rooijen, A. Hidalgo, F. Geissmann, T. Walzer, G. M. Lord, and A. Martín-Fontecha. 2011. Monocytes control natural killer cell differentiation to effector phenotypes. Blood 117: 4511-4518.
41. Quinn, L. S., L. Strait-Bodey, B. G. Anderson, J. M. Argilés, and P. J. Havel. 2005. Interleukin-15 stimulates adiponectin secretion by 3T3-L1 adipocytes: evidence for a skeletal muscle-to-fat signaling pathway. Cell Biol. Int. 29: 449-457.
42. Quinn, L. S., and B. G. Anderson. 2011. Interleukin-15, IL-15 Receptor-Alpha, and Obesity: Concordance of Laboratory Animal and Human Genetic Studies. J. Obes. 2011: 456347.
43. Yang, V. W., R. J. Christy, J. S. Cook, T. J. Kelly, and M. D. Lane. 1989. Mechanism of regulation of the 422(aP2) gene by cAMP during preadipocyte differentiation. Proc. Natl. Acad. Sci. USA 86: 3629-3633.
44. Tontonoz, P., E. Hu, R. A. Graves, A. I. Budavari, and B. M. Spiegelman. 1994. mPPAR gamma 2: tissue-specific regulator of an adipocyte enhancer. Genes Dev. 8: 1224-1234.
45. Shan, T., W. Liu, and S. Kuang. 2013. Fatty acid binding protein 4 expression marks a population of adipocyte progenitors in white and brown adipose tissues. FASEB J. 27: 277-287.
46. He, W., Y. Barak, A. Hevener, P. Olson, D. Liao, J. Le, M. Nelson, E. Ong, J. M. Olefsky, and R. M. Evans. 2003. Adipose-specific peroxisome proliferatoractivated receptor gamma knockout causes insulin resistance in fat and liver but not in muscle. Proc. Natl. Acad. Sci. USA 100: 15712-15717.
47. Lee, K. Y., S. J. Russell, S. Ussar, J. Boucher, C. Vernochet, M. A. Mori, G. Smyth, M. Rourk, C. Cederquist, E. D. Rosen, et al. 2013. Lessons on conditional gene targeting in mouse adipose tissue. Diabetes 62: 864-874.
48. Makowski, L., J. B. Boord, K. Maeda, V. R. Babaev, K. T. Uysal, M. A. Morgan, R. A. Parker, J. Suttles, S. Fazio, G. S. Hotamisligil, and M. F. Linton. 2001. Lack of macrophage fatty-Acid-binding protein aP2 protects mice deficient in apolipoprotein E against atherosclerosis. Nat. Med. 7: 699-705.
49. Urs, S., A. Harrington, L. Liaw, and D. Small. 2006. Selective expression of an aP2/Fatty Acid Binding Protein 4-Cre transgene in non-Adipogenic tissues during embryonic development. Transgenic Res. 15: 647-653.
50. Rolph, M. S., T. R. Young, B. O. Shum, C. Z. Gorgun, C. Schmitz-Peiffer, I. A. Ramshaw, G. S. Hotamisligil, and C. R. Mackay. 2006. Regulation of dendritic cell function and T cell priming by the fatty acid-binding protein AP2. J. Immunol. 177: 7794-7801.
51. Elmasri, H., C. Karaaslan, Y. Teper, E. Ghelfi, M. Weng, T. A. Ince, H. Kozakewich, J. Bischoff, and S. Cataltepe. 2009. Fatty acid binding protein 4 is a target of VEGF and a regulator of cell proliferation in endothelial cells. FASEB J. 23: 3865-3873.
52. Chakrabarti, P. 2010. Promoting adipose specificity: the adiponectin promoter. Endocrinology 151: 2408-2410.
53. Cannon, B., and J. Nedergaard. 2004. Brown adipose tissue: function and physiological significance. Physiol. Rev. 84: 277-359.
54. Peng, H., X. Jiang, Y. Chen, D. K. Sojka, H. Wei, X. Gao, R. Sun, W. M. Yokoyama, and Z. Tian. 2013. Liver-resident NK cells confer adaptive immunity in skin-contact inflammation. J. Clin. Invest. 123: 1444-1456.
55. Huntington, N. D., H. Tabarias, K. Fairfax, J. Brady, Y. Hayakawa, M. A. Degli-Esposti, M. J. Smyth, D. M. Tarlinton, and S. L. Nutt. 2007. NK cell maturation and peripheral homeostasis is associated with KLRG1 up-regulation. J. Immunol. 178: 4764-4770.
56. Reichlin, A., and W. M. Yokoyama. 1998. Natural killer cell proliferation induced by anti-NK1.1 and IL-2. Immunol. Cell Biol. 76: 143-152.
57. Lauwerys, B. R., N. Garot, J. C. Renauld, and F. A. Houssiau. 2000. Cytokine production and killer activity of NK/T-NK cells derived with IL-2, IL-15, or the combination of IL-12 and IL-18. J. Immunol. 165: 1847-1853.
58. Atkinson, E. A., J. M. Gerrard, G. E. Hildes, and A. H. Greenberg. 1990. Studies of the mechanism of natural killer (NK) degranulation and cytotoxicity. J. Leukoc. Biol. 47: 39-48.
59. Tran, T. T., and C. R. Kahn. 2010. Transplantation of adipose tissue and stem cells: role in metabolism and disease. Nat. Rev. Endocrinol. 6: 195-213.
60. Michel, T., A. Poli, O. Domingues, M. Mauffray, M. Théré sine, N. H. Brons, F. Hentges, and J. Zimmer. 2012. Mouse lung and spleen natural killer cells have phenotypic and functional differences, in part influenced by macrophages. PLoS ONE 7: e51230.