Mice deficient in CD38 develop an attenuated form of collagen type II-induced arthritis

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Postigo, Jorge ^a   Iglesias, Marcos ^a   Cerezo Wallis, Daniela ^b   Rosal Vela, Antonio ^b   García Rodríguez, Sonia ^b   Zubiaur, Mercedes ^b   Sancho, Jaime ^b   Merino, Ramón ^a   Merino, Jesús ^a  

^a UNIVERSITY OF CANTABRIA   (Spain)

^b INSTITUTO DE PARASITOLOGÍA Y BIOMEDICINA LÓPEZ NEYRA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CD38 ANTIGEN; COLLAGEN TYPE 2; GAMMA INTERFERON; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; CD38 PROTEIN, MOUSE; CYTOKINE; HETEROPHILE ANTIBODY; IMMUNOGLOBULIN G; MEMBRANE PROTEIN; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ARTHRITIS; ARTICLE; ATTENUATION; AUTOIMMUNITY; DISEASE SEVERITY; FLOW CYTOMETRY; GENETIC VARIABILITY; IMMUNE RESPONSE; INFLAMMATION; LYMPH NODE; MALE; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY T LYMPHOCYTE; SPLEEN; TH1 CELL; TH17 CELL; ANIMAL; BIOSYNTHESIS; BLOOD; C57BL MOUSE; CHICKEN; GENE EXPRESSION; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; PATHOLOGY;

MUS;

ANIMALS; ANTIBODIES, HETEROPHILE; ANTIGENS, CD38; ARTHRITIS, EXPERIMENTAL; CHICKENS; COLLAGEN TYPE II; CYTOKINES; GENE EXPRESSION; IMMUNOGLOBULIN G; INTERFERON-GAMMA; INTERLEUKIN-1BETA; INTERLEUKIN-6; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NATURAL KILLER T-CELLS; RNA, MESSENGER; SPLEEN; TH1 CELLS; TH17 CELLS;

EID: 84858418518     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033534     Document Type: Article

References (45)

1. Deterre P, Berthelier V, Bauvois B, Dalloul A, Schuber F, et al. (2000) CD38 in T- and B-cell functions. Chem Immunol 75: 146-168.
2. Malavasi F, Deaglio S, Funaro A, Ferrero E, Horenstein AL, et al. (2008) Evolution and function of the ADP ribosyl cyclase/CD38 gene family in physiology and pathology. Physiol Rev 88:. 841-886.
3. Howard M, Grimaldi JC, Bazan JF, Lund FE, Santos-Argumedo L, et al. (1993) Formation and hydrolysis of cyclic ADP-ribose catalyzed by lymphocyte antigen CD38. Science 262: 1056-1059.
4. Zocchi E, Franco L, Guida L, Benatti U, Bargellesi A, et al. (1993) A single protein immunologically identified as CD38 displays NAD-glycohydrolase, ADP-ribosyl cyclase and cyclic ADP-ribose hydrolase activities at the outer surface of human erythrocytes. Biochem Biophys Res Commun 196: 1459-1465.
5. Lee HC, Aarhus R, (1995) A derivate of NADP mobilizes calcium stores insensitive to inositol trisphosphate and cyclic ADP-ribose. J Biol Chem 270: 2152-2157.
6. Schuber F, Lund FE, (2004) Structure and enzymology of ADP-ribosyl cyclases: Conserved enzymes that produce multiple calcium mobilizing metabolites. Curr Mol Med 4: 249-261.
7. Deaglio S, Mallone R, Baj G, Arnulfo A, Surico N, et al. (2000) CD38/CD31, a receptor/ligand system ruling adhesion and signaling in human leukocytes. Chem Immunol 75: 99-120.
8. Frasca L, Fedele G, Deaglio S, Capuano C, Palazzo R, et al. (2006) CD38 orchestrates migration, survival, and Th1 immune response of human mature dendritic cells. Blood 107: 2392-2399.
9. Viegas MS, do Carmo A, Silva T, Seco F, Serra V, et al. (2007) CD38 plays a role in effective containment of mycobacteria within granulomata and polarization of Th1 immune responses against Mycobacterium avium. Microb Infect 9: 847-854.
10. Munoz P, Mittelbrunn M, de la Fuente H, Perez-Martinez M, García-Perez A, et al. (2008) Antigen-induced clustering of surface CD38 and recruitment of intracellular CD38 to the immunologic synapse. Blood 111: 3653-3664.
11. Zubiaur M, Fernandez O, Ferrero E, Salmeron J, Malissen B, et al. (2002) CD38 is associated with lipid rafts and upon receptor stimulation leads to Akt/protein kinase B and Erk activation in the absence of the CD3-zeta immune receptor tyrosine-based activation motifs. J Biol Chem 277: 13-22.
12. Munoz P, Navarro MD, Pavon EJ, Salmeron J, Malavasi F, et al. (2003) CD38 signaling in T cells is initiated within a subset of membrane rafts containing Lck and the CD3-zeta subunit of the T cell antigen receptor. J Biol Chem 278: 50791-50802.
13. Zumaquero E, Munoz P, Cobo M, Lucena G, Pavón EJ, et al. (2010) Exosomes from human lymphoblastoid B cells express enzymatically active CD38 that is associated with signaling complexes containing CD81, Hsc-70 and Lyn. Exp Cell Res 316: 2692-2706.
14. Cockayne DA, Muchamuel T, Grimaldi JC, Muller-Steffner H, Randall TD, et al. (1998) Mice deficient for the ecto-nicotinamide adenine dinucleotide glycohydrolase CD38 exhibit altered humoral immune responses. Blood 92: 1324-1333.
15. Partida-Sanchez S, Goodrich S, Kusser K, Oppenheimer N, Randall TD, et al. (2004) Regulation of dendritic cell trafficking by the ADP-rybosil cyclase CD38: impact on the development of humoral immunity. Immunity 20: 279-291.
16. Partida-Sanchez S, Cockayne DA, Monard S, Jacobson EL, Oppenheimer N, et al. (2001) Cyclic ADP-ribose production by CD38 regulates intracellular calcium release, extracellular calcium influx and chemotaxis in neutrophils and is required for bacterial clearance in vivo. Nat Med 7: 1209-1216.
17. Chen J, Chen YG, Reifsnyder PC, Schott WH, Lee CH, et al. (2006) Targeted disruption of CD38 accelerates autoimmune diabetes in NOD/Lt mice by enhancing autoimmunity in an ADP-ribosyltransferase 2-dependent fashion. J Immunol 176: 4590-4599.
18. Chen YG, Chen J, Osborne MA, Chapman HD, Besra GS, et al. (2006) CD38 is required for the peripheral survival of immunotolerogenic CD4+ invariant NK T cells in nonobese diabetic mice. J Immunol 177: 2939-2947.
19. Seman M, Adriouch S, Scheuplein F, Krebs C, Freese D, et al. (2003) NAD-induced T cell death: ADP-ribosylation of cell surface proteins by ART-2 activates the cytolytic P2X7 purinoceptor. Immunity 19: 571-582.
20. Chiba A, Kaieda S, Oki S, Yamamura T, Miyake S, (2005) The involvement of V(alpha)14 natural killer T cells in the pathogenesis of arthritis in murine models. Arthritis Rheum 52: 1941-1948.
21. Yoshiga Y, Goto D, Segawa S, Ohnishi Y, Matsumoto I, et al. (2008) Invariant NKT cells produce IL-17 through IL-23-dependent and-independent pathways with potential modulation of Th17 response in collagen-induced arthritis. Int J Mol Med 22: 369-374.
22. Driver JP, Scheuplein F, Chen YG, Grier AE, Wilson SB, et al. (2010) Invariant natural killer T-cell control of type 1 diabetes: a dendritic cell genetic decision of a silver bullet or Russian roulette. Diabetes 59: 423-432.
23. Choe CU, Lardong K, Gelderblom M, Ludewig P, Leypoldt F, et al. (2011) CD38 exacerbates focal cytokine production, postischemic inflammation and brain injury after focal cerebral ischemia. PLoS One 6: e19046.
24. Lund FE, (2006) Signaling properties of CD38 in the mouse immune system: enzyme-dependent and-independent roles in immunity. Mol Med 12: 328-333.
25. Guedes AG, Jude JA, Paulin J, Kita H, Lund FE, et al. (2008) Role of CD38 in TNF-alpha-induced airway hyperresponsiveness. Am J Physiol Lung Cell Mol Physiol 294: L290-299.
26. Grammer AC, Slota R, Fischer R, Gur H, Girschick H, et al. (2003) Abnormal germinal center reactions in systemic lupus erythematosus demonstrated by blockade of CD154-CD40 interactions. J Clin Invest 112: 1506-1520.
27. Cho YG, Cho ML, Min SY, Kim HY, (2007) Type II collagen autoimmunity in a mouse model of human rheumatoid arthritis. Autoimmun Rev 7: 65-70.
28. Kelchtermans H, De Klerck B, Mitera T, Van Balen M, Bullens D, et al. (2005) Defective CD4+CD25+ regulatory T cell functioning in collagen-induced arthritis: an important factor in pathogenesis, counter-regulated by endogenous IFN-gamma. Arthritis Res Ther 7: R402-415.
29. Frey O, Petrow PK, Gajda M, Siegmund K, Huehn J, et al. (2005) The role of regulatory T cells in antigen-induced arthritis: aggravation of arthritis after depletion and amelioration after transfer of CD4+CD25+ T cells. Arthritis Res Ther 7: R291-301.
30. González J, Tamayo E, Santiuste I, Marquina R, Buelta L, et al. (2007) CD4+CD25+ T cell-dependent inhibition of autoimmunity in transgenic mice overexpressing human Bcl-2 in T lymphocytes. J Immunol 178: 2778-2786.
31. Yanaba K, Hamaguchi Y, Venturi GM, Steeber DA, St Clair EW, et al. (2007) B cell depletion delays collagen-induced arthritis in mice: arthritis induction requires synergy between humoral and cell-mediated immunity. J Immunol 179: 1369-1380.
32. Svensson L, Jirholt J, Holmdahl R, Jansson L, (1998) B cell-deficient mice do not develop type II collagen-induced arthritis (CIA). Clin Exp Immunol 111: 521-526.
33. Fossati-Jimack L, Ioan-Facsinay A, Reininger L, Chicheportiche Y, Watanabe N, et al. (2000) Markedly different pathogenicity of four immunoglobulin G isotype-switch variants of an antierythrocyte autoantibody is based on their capacity to interact in vivo with the low-affinity Fcγ receptor III. J Exp Med 191: 1293-1302.
34. Ravetch JV, Bolland S, (2001) IgG Fc receptors. Annu Rev Immunol 19: 275-290.
35. Neuberger MS, Rajewsky K, (1981) Activation mouse complement by monoclonal mouse antibodies. Eur J Immunol 11: 1012-1016.
36. Lubberts E, Koenders MI, Oppers-Walgreen B, van den Bersselaar L, et al. (2004) Treatment with a neutralizing anti-murine interleukin-17 antibody after the onset of collagen-induced arthritis reduces joint inflammation, cartilage destruction, and bone erosion. Arthritis Rheum 50: 650-659.
37. Sato K, Suematsu A, Okamoto K, Yamaguchi A, Morishita Y, et al. (2006) Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction. J Exp Med 203: 2673-2682.
38. Chu CQ, Song Z, Mayton L, Wu B, Wooley PH, (2003) IFNã deficient C57BL/6 (H-2b) mice develop collagen induced arthritis with predominant usage of T cell receptor Vβ6 and Vβ8 in arthritic joints. Ann Rheum Dis 62: 983-990.
39. Guedez YB, Whittington KB, Clayton JL, Joosten LA, van de Loo FA, et al. (2001) Genetic ablation of interferon-ã up-regulates interleukin-1β expression and enables the elicitation of collagen-induced arthritis in a nonsusceptible mouse strain. Arthritis Rheum 44: 2413-2424.
40. Manoury-Schwartz B, Chiocchia G, Bessis N, Abehsira-Amar O, Batteux F, et al. (1997) High susceptibility to collagen-induced arthritis in mice lacking IFN-ã receptors. J Immunol 158: 5501-5506.
41. Vermeire K, Heremans H, van de Putte M, Huang S, Billiau A, et al. (1997) Accelerated collagen-induced arthritis in IFN-ã receptor-deficient mice. J Immunol 158: 5507-5513.
42. Postigo J, Genre F, Iglesias M, Fernández-Rey M, Buelta L, et al. (2011) Exacerbation of collagen type II-induced arthritis in ApoE deficient mice in association with the expansion of Th1 and Th17 cells. Arthritis Rheum 63: 971-980.
43. Lamacchia C, Palmer G, Seemayer C, Talabot-Ayer D, Gabay C, (2010) Enhanced Th1 and Th17 responses and arthritis severity in mice with a deficiency of myeloid cell-specific interleukin-1 receptor antagonist. Arthritis Rheum 62: 452-462.
44. Griffiths MM, Cremer MA, Harper DS, McCall S, Cannon GW, (1992) Immunogenetics of collagen-induced arthritis in rats: both MHC and non-MHC gene products determine the epitope specificity of immune response to bovine and chick type II collagens. J Immunol 149: 309-316.
45. Harrell MI, Iritani BM, Ruddell A, (2008) Lymph node mapping in the mouse. J Immunol Methods 332: 170-174.