The tetraspanin CD37 orchestrates the α4β1 integrin-Akt signaling axis and supports long-lived plasma cell survival

Science Signaling

Volumn 5, Issue 250, 2012, Pages

  Van Spriel, Annemiek B ^a   De Keijzer, Sandra ^a   Van Der Schaaf, Alie ^a   Gartlan, Kate H ^b   Sofi, Mariam ^b   Light, Amanda ^c   Linssen, Peter C ^d   Boezeman, Jan B ^d   Zuidscherwoude, Malou ^a   Reinieren Beeren, Inge ^a   Cambi, Alessandra ^a   Mackay, Fabienne ^b   Tarlinton, David M ^c   Figdor, Carl G ^a   Wright, Mark D ^b  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b MONASH UNIVERSITY   (Australia)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CD37 ANTIGEN; IMMUNOGLOBULIN G; PROTEIN KINASE B; VASCULAR CELL ADHESION MOLECULE 1; VERY LATE ACTIVATION ANTIGEN 4;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL MEMBRANE; CELL SURVIVAL; CLUSTER ANALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; IMMUNE SYSTEM; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PLASMA CELL; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

ANIMALS; ANTIGENS, CD; ANTIGENS, NEOPLASM; CELL MOVEMENT; CELL SURVIVAL; GERMINAL CENTER; IMMUNOGLOBULIN G; INTEGRIN ALPHA4BETA1; MICE; MICE, KNOCKOUT; PLASMA CELLS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SPLEEN; TETRASPANINS;

EUKARYOTA; MUS;

EID: 84869395208     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2003113     Document Type: Article

References (55)

1. B. A. Hemmings, Akt signaling: Linking membrane events to life and death decisions. Science 275, 628-630 (1997).
2. D. Cantrell, Protein kinase B (Akt) regulation and function in T lymphocytes. Semin. Immunol. 14, 19-26 (2002).
3. M. Calamito, M. M. Juntilla, M. Thomas, D. L. Northrup, J. Rathmell, M. J. Birnbaum, G. Koretzky, D. Allman, Akt1 and Akt2 promote peripheral B-cell maturation and survival. Blood 115, 4043-4050 (2010).
4. J. Jacob, R. Kassir, G. Kelsoe, In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. I. The architecture and dynamics of responding cell populations. J. Exp. Med. 173, 1165-1175 (1991).
5. C. L. Cozine, K. L. Wolniak, T. J. Waldschmidt, The primary germinal center response in mice. Curr. Opin. Immunol. 17, 298-302 (2005).
6. D. Tarlinton, B-cell memory: Are subsets necessary? Nat. Rev. Immunol. 6, 785-790 (2006).
7. C. C. Goodnow, C. G. Vinuesa, K. L. Randall, F. Mackay, R. Brink, Control systems and decision making for antibody production. Nat. Immunol. 11, 681-688 (2010).
8. D. Finke, F. Baribaud, H. Diggelmann, H. Acha-Orbea, Extrafollicular plasmablast B cells play a key role in carrying retroviral infection to peripheral organs. J. Immunol. 166, 6266-6275 (2001).
9. E. J. Kunkel, E. C. Butcher, Plasma-cell homing. Nat. Rev. Immunol. 3, 822-829 (2003).
10. G. Koopman, R. M. Keehnen, E. Lindhout, W. Newman, Y. Shimizu, G. A. van Seventer, C. de Groot, S. T. Pals, Adhesion through the LFA-1 (CD11a/CD18)-ICAM-1 (CD54) and the VLA-4 (CD49d)-VCAM-1 (CD106) pathways prevents apoptosis of germinal center B cells. J. Immunol. 152, 3760-3767 (1994).
11. Y. R. Carrasco, F. D. Batista, B-cell activation by membrane-bound antigens is facilitated by the interaction of VLA-4 with VCAM-1. EMBO J. 25, 889-899 (2006).
12. C. E. Leuker, M. Labow, W. Müller, N. Wagner, Neonatally induced inactivation of the vascular cell adhesion molecule 1 gene impairs B cell localization and T cell-dependent humoral immune response. J. Exp. Med. 193, 755-768 (2001).
13. A. Cambi, B. Joosten, M. Koopman, F. de Lange, I. Beeren, R. Torensma, J. A. Fransen, M. Garcia-Parajó, F. N. van Leeuwen, C. G. Figdor, Organization of the integrin LFA-1 in nanoclusters regulates its activity. Mol. Biol. Cell 17, 4270-4281 (2006).
14. O. Barreiro, H. de la Fuente, M. Mittelbrunn, F. Sánchez-Madrid, Functional insights on the polarized redistribution of leukocyte integrins and their ligands during leukocyte migration and immune interactions. Immunol. Rev. 218, 147-164 (2007).
15. F. G. Giancotti, E. Ruoslahti, Integrin signaling. Science 285, 1028-1032 (1999).
16. F. Berditchevski, E. Odintsova, Characterization of integrin-tetraspanin adhesion complexes: Role of tetraspanins in integrin signaling. J. Cell Biol. 146, 477-492 (1999).
17. S. Levy, T. Shoham, The tetraspanin web modulates immune-signalling complexes. Nat. Rev. Immunol. 5, 136-148 (2005).
18. M. E. Hemler, Tetraspanin functions and associated microdomains. Nat. Rev. Mol. Cell Biol. 6, 801-811 (2005).
19. S. Charrin, F. le Naour, O. Silvie, P. E. Milhiet, C. Boucheix, E. Rubinstein, Lateral organization of membrane proteins: Tetraspanins spin their web. Biochem. J. 420, 133-154 (2009).
20. M. D. Wright, G. W. Moseley, A. B. van Spriel, Tetraspanin microdomains in immune cell signalling and malignant disease. Tissue Antigens 64, 533-542 (2004).
21. M. Zöller, Tetraspanins: Push and pull in suppressing and promoting metastasis. Nat. Rev. Cancer 9, 40-55 (2009).
22. A. B. van Spriel, M. Sofi, K. H. Gartlan, A. van der Schaaf, I. Verschueren, R. Torensma, R. A. Raymakers, B. E. Loveland, M. G. Netea, G. J. Adema, M. D. Wright, C. G. Figdor, The tetraspanin protein CD37 regulates IgA responses and anti-fungal immunity. PLoS Pathog. 5, e1000338 (2009).
23. K. P. Knobeloch, M. D. Wright, A. F. Ochsenbein, O. Liesenfeld, J. Löhler, R. M. Zinkernagel, I. Horak, Z. Orinska, Targeted inactivation of the tetraspanin CD37 impairs T-cell-dependent B-cell response under suboptimal costimulatory conditions. Mol. Cell. Biol. 20, 5363-5369 (2000).
24. A. B. van Spriel, K. L. Puls, M. Sofi, D. Pouniotis, H. Hochrein, Z. Orinska, K. P. Knobeloch, M. Plebanski, M. D. Wright, A regulatory role for CD37 in T cell proliferation. J. Immunol. 172, 2953-2961 (2004).
25. F. Meyer-Wentrup, C. G. Figdor, M. Ansems, P. Brossart, M. D. Wright, G. J. Adema, A. B. van Spriel, Dectin-1 interaction with tetraspanin CD37 inhibits IL-6 production. J. Immunol. 178, 154-162 (2007).
26. K. C. Sheng, A. B. van Spriel, K. H. Gartlan, M. Sofi, V. Apostolopoulos, L. Ashman, M. D. Wright, Tetraspanins CD37 and CD151 differentially regulate Ag presentation and T-cell co-stimulation by DC. Eur. J. Immunol. 39, 50-55 (2009).
27. A. L. Rops, C. G. Figdor, A. van der Schaaf, W. P. Tamboer, M. A. Bakker, J. H. Berden, H. B. Dijkman, E. J. Steenbergen, J. van der Vlag, A. B. van Spriel, The tetraspanin CD37 protects against glomerular IgA deposition and renal pathology. Am. J. Pathol. 176, 2188-2197 (2010).
28. A. Cumano, K. Rajewsky, Clonal recruitment and somatic mutation in the generation of immunological memory to the hapten NP. EMBO J. 5, 2459-2468 (1986).
29. F. Berditchevski, Complexes of tetraspanins with integrins: More than meets the eye. J. Cell Sci. 114, 4143-4151 (2001).
30. D. M. Rose, P. M. Cardarelli, R. R. Cobb, M. H. Ginsberg, Soluble VCAM-1 binding to a4 integrins is cell-type specific and activation dependent and is disrupted during apoptosis in T cells. Blood 95, 602-609 (2000).
31. B. D. Manning, L. C. Cantley, AKT/PKB signaling: Navigating downstream. Cell 129, 1261-1274 (2007).
32. S. R. Datta, H. Dudek, X. Tao, S. Masters, H. Fu, Y. Gotoh, M. E. Greenberg, Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91, 231-241 (1997).
33. T. Kawabe, T. Naka, K. Yoshida, T. Tanaka, H. Fujiwara, S. Suematsu, N. Yoshida, T. Kishimoto, H. Kikutani, The immune responses in CD40-deficient mice: Impaired immunoglobulin class switching and germinal center formation. Immunity 1, 167-178 (1994).
34. A. L. Dent, A. L. Shaffer, X. Yu, D. Allman, L. M. Staudt, Control of inflammation, cytokine expression, and germinal center formation by BCL-6. Science 276, 589-592 (1997).
35. I. Vikstrom, S. Carotta, K. Lüthje, V. Peperzak, P. J. Jost, S. Glaser, M. Busslinger, P. Bouillet, A. Strasser, S. L. Nutt, D. M. Tarlinton, Mcl-1 is essential for germinal center formation and B cell memory. Science 330, 1095-1099 (2010).
36. L. J. McHeyzer-Williams, N. Pelletier, L. Mark, N. Fazilleau, M. G. McHeyzer-Williams, Follicular helper T cells as cognate regulators of B cell immunity. Curr. Opin. Immunol. 21, 266-273 (2009).
37. C. G. Vinuesa, M. A. Linterman, C. C. Goodnow, K. L. Randall, T cells and follicular dendritic cells in germinal center B-cell formation and selection. Immunol. Rev. 237, 72-89 (2010).
38. K. G. Smith, A. Light, G. J. Nossal, D. M. Tarlinton, The extent of affinity maturation differs between the memory and antibody-forming cell compartments in the primary immune response. EMBO J. 16, 2996-3006 (1997).
39. C. Berlin, R. F. Bargatze, J. J. Campbell, U. H. von Andrian, M. C. Szabo, S. R. Hasslen, R. D. Nelson, E. L. Berg, S. L. Erlandsen, E. C. Butcher, a4 integrins mediate lymphocyte attachment and rolling under physiologic flow. Cell 80, 413-422 (1995).
40. D. M. Rose, J. Han, M. H. Ginsberg, a4 integrins and the immune response. Immunol. Rev. 186, 118-124 (2002).
41. S. W. Feigelson, V. Grabovsky, R. Shamri, S. Levy, R. Alon, The CD81 tetraspanin facilitates instantaneous leukocyte VLA-4 adhesion strengthening to vascular cell adhesion molecule 1 (VCAM-1) under shear flow. J. Biol. Chem. 278, 51203-51212 (2003).
42. L. L. Chen, A. Whitty, R. R. Lobb, S. P. Adams, R. B. Pepinsky, Multiple activation states of integrin a4b1 detected through their different affinities for a small molecule ligand. J. Biol. Chem. 274, 13167-13175 (1999).
43. K. K. Lin, L. Rossi, N. C. Boles, B. E. Hall, T. C. George, M. A. Goodell, CD81 is essential for the re-entry of hematopoietic stem cells to quiescence following stress-induced proliferation via deactivation of the Akt pathway. PLoS Biol. 9, e1001148 (2011).
44. K. H. Heider, K. Kiefer, T. Zenz, M. Volden, S. Stilgenbauer, E. Ostermann, A. Baum, H. Lamche, Z. Küpcü, A. Jacobi, S. Müller, U. Hirt, G. R. Adolf, E. Borges, A novel Fc-engineered monoclonal antibody to CD37 with enhanced ADCC and high proapoptotic activity for treatment of B-cell malignancies. Blood 118, 4159-4168 (2011).
45. R. Lapalombella, Y. Y. Yeh, L. Wang, A. Ramanunni, S. Rafiq, S. Jha, J. Staubli, D. M. Lucas, R. Mani, S. E. Herman, A. J. Johnson, A. Lozanski, L. Andritsos, J. Jones, J. M. Flynn, B. Lannutti, P. Thompson, P. Algate, S. Stromatt, D. Jarjoura, X. Mo, D. Wang, C. S. Chen, G. Lozanski, N. A. Heerema, S. Tridandapani, M. A. Freitas, N. Muthusamy, J. C. Byrd, Tetraspanin CD37 directly mediates transduction of survival and apoptotic signals. Cancer Cell 21, 694-708 (2012).
46. C. Lagaudrière-Gesbert, S. Lebel-Binay, C. Hubeau, D. Fradelizi, H. Conjeaud, Signaling through the tetraspanin CD82 triggers its association with the cytoskeleton leading to sustained morphological changes and T cell activation. Eur. J. Immunol. 28, 4332-4344 (1998).
47. M. Sala-Valdés, A. Ursa, S. Charrin, E. Rubinstein, M. E. Hemler, F. Sánchez-Madrid, M. Yánez-Mó, EWI-2 and EWI-F link the tetraspanin web to the actin cytoskeleton through their direct association with ezrin-radixin-moesin proteins. J. Biol. Chem. 281, 19665-19675 (2006).
48. 4 integrins modifies integrin-dependent biological responses. Nature 402, 676-681 (1999).
49. S. J. Hyduk, J. Oh, H. Xiao, M. Chen, M. I. Cybulsky, Paxillin selectively associates with constitutive and chemoattractant-induced high-affinity α4β1 integrins: Implications for integrin signaling. Blood 104, 2818-2824 (2004).
50. 4-cytoplasmic domain. J. Cell Biol. 171, 1073-1084 (2005).
51. C. W. Cairo, R. Mirchev, D. E. Golan, Cytoskeletal regulation couples LFA-1 conformational changes to receptor lateral mobility and clustering. Immunity 25, 297-308 (2006).
52. S. N. Mueller, R. N. Germain, Stromal cell contributions to the homeostasis and functionality of the immune system. Nat. Rev. Immunol. 9, 618-629 (2009).
53. N. D. Huntington, Y. Xu, H. Puthalakath, A. Light, S. N.Willis, A. Strasser, D. M. Tarlinton, CD45 links the B cell receptor with cell survival and is required for the persistence of germinal centers. Nat. Immunol. 7, 190-198 (2006).
54. D. J. Krooshoop, R. Torensma, G. J. van den Bosch, J. M. Nelissen, C. G. Figdor, R. A. Raymakers, J. B. Boezeman, An automated multi well cell track system to study leukocyte migration. J. Immunol. Methods 280, 89-102 (2003).
55. E. A. Kabat, T. T. Wu, H. M. Perry, K. S. Gottesman, C. Foeller, Sequences of Proteins of Immunological Interest (U.S. National Institutes of Health, Bethesda, MD, 1991).