Dynamic control of β1 integrin adhesion by the plexinD1-sema3E axis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 1, 2014, Pages 379-384

  Choi, Young I ^a,b   Duke Cohan, Jonathan S ^a,b   Chen, Wei ^c,d   Liu, Baoyu ^c,d   Rossy, Jérémie ^e,f   Tabarin, Thibault ^e,f   Ju, Lining ^c,d   Gui, Jingang ^a,b   Gaus, Katharina ^e,f   Zhu, Cheng ^c,d   Reinherz, Ellis L ^a,b  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^d GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^e UNIVERSITY OF NEW SOUTH WALES   (Australia)

^f UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Autoimmunity; Central tolerance; Integrin activation; Mechanobiology; Thymocyte development

Indexed keywords

BETA1 INTEGRIN; FIBRONECTIN; INTERCELLULAR ADHESION MOLECULE 1; LAMININ; MUCOSAL ADDRESSIN CELL ADHESION MOLECULE 1; OSTEOPONTIN; PLEXIN; PLEXIN D1; SEMAPHORIN; SEMAPHORIN 3E; THROMBOSPONDIN; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL LOSS; CELL MIGRATION; CELL SELECTION; CONTROLLED STUDY; DOWN REGULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; THYMOCYTE;

AUTOIMMUNITY; CENTRAL TOLERANCE; INTEGRIN ACTIVATION; MECHANOBIOLOGY; THYMOCYTE DEVELOPMENT;

ANIMALS; ANTIGENS, CD29; AUTOANTIBODIES; CELL ADHESION; CELL ADHESION MOLECULES, NEURONAL; CHEMOKINES; CHEMOTAXIS; GENE EXPRESSION REGULATION; GLYCOPROTEINS; INTEGRINS; LIGANDS; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; SIGNAL TRANSDUCTION; STOCHASTIC PROCESSES; THYMOCYTES;

EID: 84891952179     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1314209111     Document Type: Article

References (49)

1. Kolodkin AL, Matthes DJ, Goodman CS (1993) The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell 75(7): 1389-1399.
2. Tessier-Lavigne M, Goodman CS (1996) The molecular biology of axon guidance. Science 274(5290): 1123-1133.
3. Sakurai A, Doçi CL, Gutkind JS (2012) Semaphorin signaling in angiogenesis, lymphangiogenesis and cancer. Cell Res 22(1): 23-32.
4. Takamatsu H, Kumanogoh A (2012) Diverse roles for semaphorin-plexin signaling in the immune system. Trends Immunol 33(3): 127-135.
5. Hota PK, Buck M (2012) Plexin structures are coming: Opportunities for multilevel investigations of semaphorin guidance receptors, their cell signaling mechanisms, and functions. Cell Mol Life Sci 69(22): 3765-3805.
6. Choi YI, et al. (2008) PlexinD1 glycoprotein controls migration of positively selected thymocytes into the medulla. Immunity 29(6): 888-898.
7. Yin X, et al. (2007) CCR7 expression in developing thymocytes is linked to the CD4 versus CD8 lineage decision. J Immunol 179(11): 7358-7364.
8. Suzuki G, et al. (1998) Loss of SDF-1 receptor expression during positive selection in the thymus. Int Immunol 10(8): 1049-1056.
9. Uehara S, Song K, Farber JM, Love PE (2002) Characterization of CCR9 expression and CCL25/thymus-expressed chemokine responsiveness during T cell development: CD3 (high)CD69+ thymocytes and gammadeltaTCR+ thymocytes preferentially respond to CCL25. J Immunol 168(1): 134-142.
10. Davalos-Misslitz AC, Worbs T, Willenzon S, Bernhardt G, Förster R (2007) Impaired responsiveness to T-cell receptor stimulation and defective negative selection of thymocytes in CCR7-deficient mice. Blood 110(13): 4351-4359.
11. Egerton M, Scollay R, Shortman K (1990) Kinetics of mature T-cell development in the thymus. Proc Natl Acad Sci USA 87(7): 2579-2582.
12. Klein L, Hinterberger M, Wirnsberger G, Kyewski B (2009) Antigen presentation in the thymus for positive selection and central tolerance induction. Nat Rev Immunol 9(12): 833-844.
13. Love PE, Bhandoola A (2011) Signal integration and crosstalk during thymocyte migration and emigration. Nat Rev Immunol 11(7): 469-477.
14. Starr TK, Jameson SC, Hogquist KA (2003) Positive and negative selection of T cells. Annu Rev Immunol 21: 139-176.
15. Takahama Y (2006) Journey through the thymus: Stromal guides for T-cell development and selection. Nat Rev Immunol 6(2): 127-135.
16. von Boehmer H, Kisielow P (2006) Negative selection of the T-cell repertoire: Where and when does it occur? Immunol Rev 209: 284-289.
17. Patel DD, Haynes BF (1993) Cell adhesion molecules involved in intrathymic T cell development. Semin Immunol 5(4): 282-292.
18. St-Pierre Y, Hugo P, Legault D, Tremblay P, Potworowski EF (1996) Modulation of integrin-mediated intercellular adhesion during the interaction of thymocytes with stromal cells expressing VLA-4 and LFA-1 ligands. Eur J Immunol 26(9): 2050-2055.
19. Shu F, Holzmann B, Seibold F, Erle D, Kearney JF (2002) Activated alpha4 integrins are preferentially expressed on immature thymocytes and activated T cells. Dev Immunol 9(2): 73-84.
20. Savino W, Dalmau SR, Dealmeida VC (2000) Role of extracellular matrix-mediated interactions in thymocyte migration. Dev Immunol 7(2-4): 279-291.
21. Shortman K, Egerton M, Spangrude GJ, Scollay R (1990) The generation and fate of thymocytes. Semin Immunol 2(1): 3-12.
22. Cambi A, et al. (2006) Organization of the integrin LFA-1 in nanoclusters regulates its activity. Mol Biol Cell 17(10): 4270-4281.
23. Kucik DF (2002) Rearrangement of integrins in avidity regulation by leukocytes. Immunol Res 26(1-3): 199-206.
24. Rossy J, Owen DM, Williamson DJ, Yang Z, Gaus K (2013) Conformational states of the kinase Lck regulate clustering in early T cell signaling. Nat Immunol 14(1): 82-89.
25. Lelek M, et al. (2012) Superresolution imaging of HIV in infected cells with FlAsHPALM. Proc Natl Acad Sci USA 109(22): 8564-8569.
26. Chen W, Lou J, Evans EA, Zhu C (2012) Observing force-regulated conformational changes and ligand dissociation from a single integrin on cells. J Cell Biol 199(3): 497-512.
27. Chen W, Lou J, Zhu C (2010) Forcing switch from short- to intermediate- and longlived states of the alphaA domain generates LFA-1/ICAM-1 catch bonds. J Biol Chem 285(46): 35967-35978.
28. Yago T, et al. (2004) Catch bonds govern adhesion through L-selectin at threshold shear. J Cell Biol 166(6): 913-923.
29. Liston A, Lesage S, Wilson J, Peltonen L, Goodnow CC (2003) Aire regulates negative selection of organ-specific T cells. Nat Immunol 4(4): 350-354.
30. Zuklys S, et al. (2000) Normal thymic architecture and negative selection are associated with Aire expression, the gene defective in the autoimmune-polyendocrinopathycandidiasis- ectodermal dystrophy (APECED). J Immunol 165(4): 1976-1983.
31. Anderson MS, et al. (2002) Projection of an immunological self shadow within the thymus by the aire protein. Science 298(5597): 1395-1401.
32. Kurts C, et al. (1996) Constitutive class I-restricted exogenous presentation of self antigens in vivo. J Exp Med 184(3): 923-930.
33. Robertson JM, Jensen PE, Evavold BD (2000) DO11.10 and OT-II T cells recognize a C-terminal ovalbumin 323-339 epitope. J Immunol 164(9): 4706-4712.
34. Holl EK, et al. (2011) Plexin-D1 is a novel regulator of germinal centers and humoral immune responses. J Immunol 186(10): 5603-5611.
35. Marshall BT, et al. (2003) Direct observation of catch bonds involving cell-adhesion molecules. Nature 423(6936): 190-193.
36. Kong F, García AJ, Mould AP, Humphries MJ, Zhu C (2009) Demonstration of catch bonds between an integrin and its ligand. J Cell Biol 185(7): 1275-1284.
37. Guo B, Guilford WH (2006) Mechanics of actomyosin bonds in different nucleotide states are tuned to muscle contraction. Proc Natl Acad Sci USA 103(26): 9844-9849.
38. Yakovenko O, et al. (2008) FimH forms catch bonds that are enhanced by mechanical force due to allosteric regulation. J Biol Chem 283(17): 11596-11605.
39. Yago T, et al. (2008) Platelet glycoprotein Ibalpha forms catch bonds with human WT vWF but not with type 2B von Willebrand disease vWF. J Clin Invest 118(9): 3195-3207.
40. Akiyoshi B, et al. (2010) Tension directly stabilizes reconstituted kinetochore-microtubule attachments. Nature 468(7323): 576-579.
41. Rakshit S, Zhang Y, Manibog K, Shafraz O, Sivasankar S (2012) Ideal, catch, and slip bonds in cadherin adhesion. Proc Natl Acad Sci USA 109(46): 18815-18820.
42. Lee CY, et al. (2013) Actin depolymerization under force is governed by lysine 113: glutamic acid 195-mediated catch-slip bonds. Proc Natl Acad Sci USA 110(13): 5022-5027.
43. Oinuma I, Katoh H, Negishi M (2006) Semaphorin 4D/Plexin-B1-mediated R-Ras GAP activity inhibits cell migration by regulating beta(1) integrin activity. J Cell Biol 173(4): 601-613.
44. Janssen BJ, et al. (2010) Structural basis of semaphorin-plexin signalling. Nature 467(7319): 1118-1122.
45. Nogi T, et al. (2010) Structural basis for semaphorin signalling through the plexin receptor. Nature 467(7319): 1123-1127.
46. Springer TA, Wang JH (2004) The three-dimensional structure of integrins and their ligands, and conformational regulation of cell adhesion. Adv Protein Chem 68: 29-63.
47. Lefort CT, et al. (2012) Distinct roles for talin-1 and kindlin-3 in LFA-1 extension and affinity regulation. Blood 119(18): 4275-4282.
48. Casazza A, et al. (2010) Sema3E-Plexin D1 signaling drives human cancer cell invasiveness and metastatic spreading in mice. J Clin Invest 120(8): 2684-2698.
49. Liu H, et al. (2010) Structural basis of semaphorin-plexin recognition and viral mimicry from Sema7A and A39R complexes with PlexinC1. Cell 142(5): 749-761.