Interleukin-15-activated natural killer cells kill autologous osteoclasts via LFA-1, DNAM-1 and TRAIL, and inhibit osteoclast-mediated bone erosion in vitro

Immunology

Volumn 145, Issue 3, 2015, Pages 367-379

  Feng, Shan ^a,b   Madsen, Suzi H ^a   Viller, Natasja N ^a   Neutzsky Wulff, Anita V ^a,c   Geisler, Carsten ^b   Karlsson, Lars ^a   Söderström, Kalle ^a,d  

^a NOVO NORDISK A S   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c CEDARS SINAI MEDICAL CENTER   (United States)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

DNAX accessory molecule 1; Leucocyte function associated antigen 1; Natural killer cytotoxicity; Osteoclast; Tumour necrosis factor related apoptosis inducing ligand

Indexed keywords

CD14 ANTIGEN; CD48 ANTIGEN; COLONY STIMULATING FACTOR 1; DNAX ACCESSORY MOLECULE 1; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 15; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 2; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; OSTEOCLAST DIFFERENTIATION FACTOR; PROTEIN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; CD226 ANTIGEN; T LYMPHOCYTE ANTIGEN;

APOPTOSIS; ARTICLE; BONE EROSION; CELL ACTIVATION; CELL CONTACT; CELL DIFFERENTIATION; CELL FUNCTION; CELL SURFACE; CELL SURVIVAL; CELL VIABILITY; ENZYME ACTIVITY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IN VITRO STUDY; LIMIT OF QUANTITATION; NATURAL KILLER CELL; NORMAL HUMAN; OSTEOCLAST; OSTEOCLAST ACTIVITY; OSTEOLYSIS; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TARGET CELL; CELL COMMUNICATION; CELL CULTURE; COCULTURE; CYTOLOGY; CYTOTOXICITY; DRUG EFFECTS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MONOCYTE;

ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; APOPTOSIS; BONE RESORPTION; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL SURVIVAL; CELLS, CULTURED; COCULTURE TECHNIQUES; CYTOTOXICITY, IMMUNOLOGIC; FLOW CYTOMETRY; HUMANS; INTERLEUKIN-15; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; MONOCYTES; OSTEOCLASTS; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 84931563253     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/imm.12449     Document Type: Article

References (48)

1. Takahashi N, Yamana H, Yoshiki S et al. Osteoclast-like cell formation and its regulation by osteotropic hormones in mouse bone marrow cultures. Endocrinology 1988; 122:1373-82.
2. Teitelbaum SL. Bone resorption by osteoclasts. Science 2000; 289:1504-8.
3. Hughes DE, Boyce BF. Apoptosis in bone physiology and disease. Mol Pathol 1997; 50:132-7.
4. Parfitt AM. The actions of parathyroid hormone on bone: relation to bone remodeling and turnover, calcium homeostasis, and metabolic bone diseases. II. PTH and bone cells: bone turnover and plasma calcium regulation. Metabolism 1976; 25:909-55.
5. Singer FR, Melvin KE, Mills BG. Acute effects of calcitonin on osteoclasts in man. Clin Endocrinol (Oxf) 1976; 5(Suppl.):333S-40S.
6. Yamamoto Y, Yoshizawa T, Fukuda T et al. Vitamin D receptor in osteoblasts is a negative regulator of bone mass control. Endocrinology 2013; 154:1008-20.
7. Shevde NK, Bendixen AC, Dienger KM, Pike JW. Estrogens suppress RANK ligand-induced osteoclast differentiation via a stromal cell independent mechanism involving c-Jun repression. Proc Natl Acad Sci U S A 2000; 97:7829-34.
8. Jimi E, Nakamura I, Duong LT et al. Interleukin 1 induces multinucleation and bone-resorbing activity of osteoclasts in the absence of osteoblasts/stromal cells. Exp Cell Res 1999; 247:84-93.
9. Itonaga I, Sabokbar A, Sun SG et al. Transforming growth factor-β induces osteoclast formation in the absence of RANKL. Bone 2004; 34:57-64.
10. Lam J, Takeshita S, Barker JE, Kanagawa O, Ross FP, Teitelbaum SL. TNF-α induces osteoclastogenesis by direct stimulation of macrophages exposed to permissive levels of RANK ligand. J Clin Invest 2000; 106:1481-8.
11. Ferrari-Lacraz S, Zanelli E, Neuberg M et al. Targeting IL-15 receptor-bearing cells with an antagonist mutant IL-15/Fc protein prevents disease development and progression in murine collagen-induced arthritis. J Immunol 2004; 173:5818-26.
12. Ogata Y, Kukita A, Kukita T et al. A novel role of IL-15 in the development of osteoclasts: inability to replace its activity with IL-2. J Immunol 1999; 162:2754-60.
13. Kotake S, Udagawa N, Takahashi N et al. IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J Clin Invest 1999; 103:1345-52.
14. Hashizume M, Hayakawa N, Mihara M. IL-6 trans-signalling directly induces RANKL on fibroblast-like synovial cells and is involved in RANKL induction by TNF-α and IL-17. Rheumatology (Oxford) 2008; 47:1635-40.
15. Watanabe K, Tanaka Y, Morimoto I et al. Interleukin-4 as a potent inhibitor of bone resorption. Biochem Biophys Res Commun 1990; 172:1035-41.
16. Lari R, Fleetwood AJ, Kitchener PD et al. Macrophage lineage phenotypes and osteoclastogenesis - complexity in the control by GM-CSF and TGF-β. Bone 2007; 40:323-36.
17. Takayanagi H, Ogasawara K, Hida S et al. T-cell-mediated regulation of osteoclastogenesis by signalling cross-talk between RANKL and IFN-γ. Nature 2000; 408:600-5.
18. Trinchieri G. Biology of natural killer cells. Adv Immunol 1989; 47:187-376.
19. Caligiuri MA. Human natural killer cells. Blood 2008; 112:461-9.
20. Fogel LA, Yokoyama WM, French AR. Natural killer cells in human autoimmune disorders. Arthritis Res Ther 2013; 15:216.
21. Gonzalez-Alvaro I, Ortiz AM, Alvaro-Gracia JM et al. Interleukin 15 levels in serum may predict a severe disease course in patients with early arthritis. PLoS ONE 2011; 6:e29492.
22. Soderstrom K, Stein E, Colmenero P et al. Natural killer cells trigger osteoclastogenesis and bone destruction in arthritis. Proc Natl Acad Sci U S A 2010; 107:13028-33.
23. Karsdal MA, Henriksen K, Sorensen MG et al. Acidification of the osteoclastic resorption compartment provides insight into the coupling of bone formation to bone resorption. Am J Pathol 2005; 166:467-76.
24. 1 integrins. J Biol Chem 1993; 268:16737-45.
25. Lanier LL. NK cell receptors. Annu Rev Immunol 1998; 16:359-93.
26. Smyth MJ, Hayakawa Y, Takeda K, Yagita H. New aspects of natural-killer-cell surveillance and therapy of cancer. Nat Rev Cancer 2002; 2:850-61.
27. Wythe SE, Nicolaidou V, Horwood NJ. Cells of the immune system orchestrate changes in bone cell function. Calcif Tissue Int 2014; 94:98-111.
28. Takeda H, Kikuchi T, Soboku K et al. Effect of IL-15 and natural killer cells on osteoclasts and osteoblasts in a mouse coculture. Inflammation 2014; 37:657-69.
29. Kurachi T, Morita I, Murota S. Involvement of adhesion molecules LFA-1 and ICAM-1 in osteoclast development. Biochim Biophys Acta 1993; 1178:259-66.
30. Kakehi S, Nakahama K, Morita I. Expression and possible role of PVR/CD155/Necl-5 in osteoclastogenesis. Mol Cell Biochem 2007; 301:209-17.
31. Pende D, Castriconi R, Romagnani P et al. Expression of the DNAM-1 ligands, Nectin-2 (CD112) and poliovirus receptor (CD155), on dendritic cells: relevance for natural killer-dendritic cell interaction. Blood 2006; 107:2030-6.
32. + T cells is mediated through NKG2D, LFA-1 and TRAIL and dampened via CD94/NKG2A. PLoS ONE 2012; 7:e31959.
33. Nielsen N, Pascal V, Fasth AE et al. Balance between activating NKG2D, DNAM-1, NKP44 and NKP46 and inhibitory CD94/NKG2A receptors determine NK degranulation towards RA synovial fibroblasts. Immunology 2014; 142:581-93.
34. Shibuya K, Lanier LL, Phillips JH et al. Physical and functional association of LFA-1 with DNAM-1 adhesion molecule. Immunity 1999; 11:615-23.
35. Shibuya K, Shirakawa J, Kameyama T et al. CD226 (DNAM-1) is involved in lymphocyte function-associated antigen 1 costimulatory signal for naive T cell differentiation and proliferation. J Exp Med 2003; 198:1829-39.
36. Gonzalez-Alvaro I, Dominguez-Jimenez C, Ortiz AM et al. Interleukin-15 and interferon-γ participate in the cross-talk between natural killer and monocytic cells required for tumour necrosis factor production. Arthritis Res Ther 2006; 8:R88.
37. Martin M, Romero X, de la Fuente MA et al. CD84 functions as a homophilic adhesion molecule and enhances IFN-γ secretion: adhesion is mediated by Ig-like domain 1. J Immunol 2001; 167:3668-76.
38. Tangye SG, Cherwinski H, Lanier LL, Phillips JH. 2B4-mediated activation of human natural killer cells. Mol Immunol 2000; 37:493-501.
39. Colonna M, Nakajima H, Cella M. Inhibitory and activating receptors involved in immune surveillance by human NK and myeloid cells. J Leukoc Biol 1999; 66:718-22.
40. Pan G, O'Rourke K, Chinnaiyan AM et al. The receptor for the cytotoxic ligand TRAIL. Science 1997; 276:111-3.
41. Hayakawa Y, Screpanti V, Yagita H et al. NK cell TRAIL eliminates immature dendritic cells in vivo and limits dendritic cell vaccination efficacy. J Immunol 2004; 172:123-9.
42. Morel J, Audo R, Hahne M, Combe B. Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) induces rheumatoid arthritis synovial fibroblast proliferation through mitogen-activated protein kinases and phosphatidylinositol 3-kinase/Akt. J Biol Chem 2005; 280:15709-18.
43. Colucci S, Brunetti G, Cantatore FP et al. The death receptor DR5 is involved in TRAIL-mediated human osteoclast apoptosis. Apoptosis 2007; 12:1623-32.
44. Kovacic N, Lukic IK, Grcevic D, Katavic V, Croucher P, Marusic A. The Fas/Fas ligand system inhibits differentiation of murine osteoblasts but has a limited role in osteoblast and osteoclast apoptosis. J Immunol 2007; 178:3379-89.
45. Song K, Chen Y, Goke R et al. Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) is an inhibitor of autoimmune inflammation and cell cycle progression. J Exp Med 2000; 191:1095-104.
46. Sarhan D, D'Arcy P, Wennerberg E et al. Activated monocytes augment TRAIL-mediated cytotoxicity by human NK cells through release of IFN-γ. Eur J Immunol 2013; 43:249-57.
47. de Matos CT, Berg L, Michaelsson J, Fellander-Tsai L, Karre K, Soderstrom K. Activating and inhibitory receptors on synovial fluid natural killer cells of arthritis patients: role of CD94/NKG2A in control of cytokine secretion. Immunology 2007; 122:291-301.
48. bright, CD158-negative phenotype. Rheumatology (Oxford) 2003; 42:870-8.