Regulation of adhesion site dynamics by integrin traffic

Current Opinion in Cell Biology

Volumn 24, Issue 5, 2012, Pages 582-591

  Valdembri, Donatella ^a   Serini, Guido ^a  

^a UNIVERSITY OF TURIN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

INTEGRIN; SCLEROPROTEIN;

CELL ADHESION; CELL MIGRATION; CONFORMATIONAL TRANSITION; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TRANSPORT; REVIEW;

ANIMALS; CELL ADHESION; CELL MOVEMENT; ENDOSOMES; EXTRACELLULAR MATRIX; HUMANS; INTEGRINS; PROTEIN BINDING; PROTEIN TRANSPORT;

EUKARYOTA;

EID: 84867863906     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2012.08.004     Document Type: Review

References (75)

1. Hynes R.O. Evolution: the evolution of metazoan extracellular matrix. J Cell Biol 2012, 196:671-679.
2. Hynes R.O. The extracellular matrix: not just pretty fibrils. Science 2009, 326:1216-1219.
3. Moser M., Legate K.R., Zent R., Fassler R. The tail of integrins, talin, and kindlins. Science 2009, 324:895-899.
4. Critchley D.R. Biochemical and structural properties of the integrin-associated cytoskeletal protein talin. Annu Rev Biophys 2009, 38:235-254.
5. Brown N.H. Extracellular matrix in development: insights from mechanisms conserved between invertebrates and vertebrates. Cold Spring Harb Perspect Biol 2011, 3. 10.1101/cshperspect.a005082.
6. Zhang H., Gally C., Labouesse M. Tissue morphogenesis: how multiple cells cooperate to generate a tissue. Curr Opin Cell Biol 2010, 22:575-582.
7. Margadant C., Charafeddine R.A., Sonnenberg A. Unique and redundant functions of integrins in the epidermis. FASEB J 2010, 24:4133-4152.
8. Hultgårdh-Nilsson A., Durbeej M. Role of the extracellular matrix and its receptors in smooth muscle cell function: implications in vascular development and disease. Curr Opin Lipidol 2007, 18:540-545.
9. Sparrow J.C., Schöck F. The initial steps of myofibril assembly: integrins pave the way. Nat Rev Mol Cell Biol 2009, 10:293-298.
10. Hinz B., Phan S.H., Thannickal V.J., Prunotto M., Desmoulière A., Varga J., De Wever O., Mareel M., Gabbiani G. Recent developments in myofibroblast biology: paradigms for connective tissue remodeling. Am J Pathol 2012, 180:1340-1355.
11. Caswell P.T., Vadrevu S., Norman J.C. Integrins: masters and slaves of endocytic transport. Nat Rev Mol Cell Biol 2009, 10:843-853.
12. Ivaska J., Heino J. Cooperation between integrins and growth factor receptors in signaling and endocytosis. Annu Rev Cell Dev Biol 2011, 27:291-320.
13. Parsons J.T., Horwitz A.R., Schwartz M.A. Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat Rev Mol Cell Biol 2011, 11:633-643.
14. Hanein D., Horwitz A.R. The structure of cell-matrix adhesions: the new frontier. Curr Opin Cell Biol 2012, 24:134-140.
15. Pankov R., Cukierman E., Katz B.-Z., Matsumoto K., Lin D.C., Lin S., Hahn C., Yamada K.M. Integrin dynamics and matrix assembly: tensin-dependent translocation of alpha5beta1 integrins promotes early fibronectin fibrillogenesis. J Cell Biol 2000, 148:1075-1090.
16. Clark K., Pankov R., Travis M.A., Askari J.A., Mould A.P., Craig S.E., Newham P., Yamada K.M., Humphries M.J. A specific alpha5beta1-integrin conformation promotes directional integrin translocation and fibronectin matrix formation. J Cell Sci 2005, 118:291-300.
17. Smilenov L.B., Mikhailov A., Pelham R.J., Marcantonio E.E., Gundersen G.G. Focal adhesion motility revealed in stationary fibroblasts. Science 1999, 286:1172-1174.
18. Ballestrem C., Hinz B., Imhof B.A., Wehrle-Haller B. Marching at the front and dragging behind: differential alphaVbeta3-integrin turnover regulates focal adhesion behavior. J Cell Biol 2001, 155:1319-1332.
19. Brower D.L. Platelets with wings: the maturation of Drosophila integrin biology. Curr Opin Cell Biol 2003, 15:607-613.
20. Yuan L., Fairchild M.J., Perkins A.D., Tanentzapf G. Analysis of integrin turnover in fly myotendinous junctions. J Cell Sci 2010, 123:939-946.
21. Emery G., Knoblich J.A. Endosome dynamics during development. Curr Opin Cell Biol 2006, 18:407-415.
22. Wirtz-Peitz F., Zallen J.A. Junctional trafficking and epithelial morphogenesis. Curr Opin Genet Dev 2009, 19:350-356.
23. de Beco S., Gueudry C., Amblard Fo, Coscoy S. Endocytosis is required for E-cadherin redistribution at mature adherens junctions. Proc Natl Acad Sci USA 2009, 106:7010-7015.
24. Valdembri D., Caswell P.T., Anderson K.I., Schwarz J.P., Konig I., Astanina E., Caccavari F., Norman J.C., Humphries M.J., Bussolino F., et al. Neuropilin-1/GIPC1 signaling regulates alpha5beta1 integrin traffic and function in endothelial cells. PLoS Biol 2009, 7:e25.
25. Ribeiro I., Yuan L., Tanentzapf G., Dowling J.J., Kiger A. Phosphoinositide regulation of integrin trafficking required for muscle attachment and maintenance. PLoS Genet 2011, 7:e1001295.
26. Hogg N., Patzak I., Willenbrock F. The insider's guide to leukocyte integrin signalling and function. Nat Rev Immunol 2011, 11:416-426.
27. Shattil S.J., Kim C., Ginsberg M.H. The final steps of integrin activation: the end game. Nat Rev Mol Cell Biol 2010, 11:288-300.
28. Byron A., Humphries J.D., Askari J.A., Craig S.E., Mould A.P., Humphries M.J. Anti-integrin monoclonal antibodies. J Cell Sci 2009, 122:4009-4011.
29. Askari J.A., Tynan C.J., Webb S.E., Martin-Fernandez M.L., Ballestrem C., Humphries M.J. Focal adhesions are sites of integrin extension. J Cell Biol 2010, 188:891-903.
30. Vicente-Manzanares M., Ma X., Adelstein R.S., Horwitz A.R. Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat Rev Mol Cell Biol 2009, 10:778-790.
31. Friedland J.C., Lee M.H., Boettiger D. Mechanically activated integrin switch controls alpha5beta1 function. Science 2009, 323:642-644.
32. Kong F., García A.J., Mould A.P., Humphries M.J., Zhu C. Demonstration of catch bonds between an integrin and its ligand. J Cell Biol 2009, 185:1275-1284.
33. Adair B.D., Xiong J.P., Maddock C., Goodman S.L., Arnaout M.A., Yeager M. Three-dimensional EM structure of the ectodomain of integrin alphaVbeta3 in a complex with fibronectin. J Cell Biol 2005, 168:1109-1118.
34. Arnaout M.A., Goodman S.L., Xiong J.P. Structure and mechanics of integrin-based cell adhesion. Curr Opin Cell Biol 2007, 19:495-507.
35. Nagae M., Re S., Mihara E., Nogi T., Sugita Y., Takagi J. Crystal structure of alpha5beta1 integrin ectodomain: atomic details of the fibronectin receptor. J Cell Biol 2012, 197:131-140.
36. Leitinger B., McDowall A., Stanley P., Hogg N. The regulation of integrin function by Ca(2+). Biochim Biophys Acta 2000, 1498:91-98.
37. Mould A.P., Askari J.A., Barton S., Kline A.D., McEwan P.A., Craig S.E., Humphries M.J. Integrin activation involves a conformational change in the alpha 1 helix of the beta subunit A-domain. J Biol Chem 2002, 277:19800-19805.
38. Mould A.P., Barton S.J., Askari J.A., Craig S.E., Humphries M.J. Role of ADMIDAS cation-binding site in ligand recognition by integrin alpha5beta1. J Biol Chem 2003, 278:51622-51629.
39. Valdramidou D., Humphries M.J., Mould A.P. Distinct roles of beta1 metal ion-dependent adhesion site (MIDAS), adjacent to MIDAS (ADMIDAS), and ligand-associated metal-binding site (LIMBS) cation-binding sites in ligand recognition by integrin alpha2beta1. J Biol Chem 2008, 283:32704-32714.
40. Puklin-Faucher E., Vogel V. Integrin activation dynamics between the RGD-binding site and the headpiece hinge. J Biol Chem 2009, 284:36557-36568.
41. Shi F., Sottile J. Caveolin-1-dependent beta1 integrin endocytosis is a critical regulator of fibronectin turnover. J Cell Sci 2008, 121:2360-2371.
42. Ng T., Shima D., Squire A., Bastiaens P.I., Gschmeissner S., Humphries M.J., Parker P.J. PKCalpha regulates beta1 integrin-dependent cell motility through association and control of integrin traffic. EMBO J 1999, 18:3909-3923.
43. Dozynkiewicz M.A., Jamieson N.B., Macpherson I., Grindlay J., van den Berghe P.V., von Thun A., Morton J.P., Gourley C., Timpson P., Nixon C., et al. Rab25 and CLIC3 collaborate to promote integrin recycling from late endosomes/lysosomes and drive cancer progression. Dev Cell 2012, 22:131-145.
44. Arjonen A., Alanko J., Veltel S., Ivaska J. Distinct recycling of active and inactive β1 integrins. Traffic 2012, 13:610-625.
45. Lawson M.A., Maxfield F.R. Ca(2+)- and calcineurin-dependent recycling of an integrin to the front of migrating neutrophils. Nature 1995, 377:75-79.
46. Pierini L.M., Lawson M.A., Eddy R.J., Hendey B., Maxfield F.R. Oriented endocytic recycling of alpha5beta1 in motile neutrophils. Blood 2000, 95:2471-2480.
47. Neufeld G., Kessler O. The semaphorins: versatile regulators of tumour progression and tumour angiogenesis. Nat Rev Cancer 2008, 8:632-645.
48. Santambrogio M., Valdembri D., Serini G. Increasing traffic on vascular routes. Mol Aspects Med 2011, 32:112-122.
49. Valdembri D., Sandri C., Santambrogio M., Serini G. Regulation of integrins by conformation and traffic: it takes two to tango. Mol Biosyst 2011, 7:2539-2546.
50. Cai H., Reed R.R. Cloning and characterization of neuropilin-1-interacting protein: a PSD-95/Dlg/ZO-1 domain-containing protein that interacts with the cytoplasmic domain of neuropilin-1. J Neurosci 1999, 19:6519-6527.
51. Reed B.C., Cefalu C., Bellaire B.H., Cardelli J.A., Louis T., Salamon J., Bloecher M.A., Bunn R.C. GLUT1CBP(TIP2/GIPC1) interactions with GLUT1 and myosin VI: evidence supporting an adapter function for GLUT1CBP 10.1091/mbc.E04-11-0978. Mol Biol Cell 2005, 16:4183-4201.
52. Spudich J.A., Sivaramakrishnan S. Myosin VI: an innovative motor that challenged the swinging lever arm hypothesis. Nat Rev Mol Cell Biol 2010, 11:128-137.
53. Tani T.T., Mercurio A.M. PDZ interaction sites in integrin a subunits. TIP-2/GIPC binds to a type I recognition sequence in α6A/α5 and a novel sequence in α6B. J Biol Chem 2001, 276:36535-36542.
54. Zhu G., Chen J., Liu J., Brunzelle J.S., Huang B., Wakeham N., Terzyan S., Li X., Rao Z., Li G., et al. Structure of the APPL1 BAR-PH domain and characterization of its interaction with Rab5. EMBO J 2007, 26:3484-3493.
55. Sandri C., Caccavari F., Valdembri D., Camillo C., Veltel S., Santambrogio M., Lanzetti L., Bussolino F., Ivaska J., Serini G. The R-Ras/RIN2/Rab5 complex controls endothelial cell adhesion and morphogenesis via active integrin endocytosis and Rac signaling. Cell Res 2012, [Epub ahead of print] PubMed PMID: 22825554. 10.1038/cr.2012.110.
56. Huotari J., Helenius A. Endosome maturation. EMBO J 2011, 30:3481-3500.
57. Faundez V., Hartzell H.C. Intracellular chloride channels: determinants of function in the endosomal pathway. Sci STKE 2004, 2004:re8.
58. Webb D.J., Zhang H., Majumdar D., Horwitz A.F. alpha5 integrin signaling regulates the formation of spines and synapses in hippocampal neurons. J Biol Chem 2007, 282:6929-6935.
59. Sandilands E., Frame M.C. Endosomal trafficking of Src tyrosine kinase. Trends Cell Biol 2008, 18:322-329.
60. Sandilands E., Cans C., Fincham V.J., Brunton V.G., Mellor H., Prendergast G.C., Norman J.C., Superti-Furga G., Frame M.C. RhoB and actin polymerization coordinate Src activation with endosome-mediated delivery to the membrane. Dev Cell 2004, 7:855-869.
61. Tu C., Ortega-Cava C.F., Winograd P., Stanton M.J., Reddi A.L., Dodge I., Arya R., Dimri M., Clubb R.J., Naramura M., et al. Endosomal-sorting complexes required for transport (ESCRT) pathway-dependent endosomal traffic regulates the localization of active Src at focal adhesions. Proc Natl Acad Sci USA 2010, 107:16107-16112.
62. Roberts M., Barry S., Woods A., van der Sluijs P., Norman J. PDGF-regulated rab4-dependent recycling of alphavbeta3 integrin from early endosomes is necessary for cell adhesion and spreading. Curr Biol 2001, 11:1392-1402.
63. Wang Y., McNiven M.A. Invasive matrix degradation at focal adhesions occurs via protease recruitment by a FAK-p130Cas complex. J Cell Biol 2012, 196:375-385.
64. Shi F., Sottile J. MT1-MMP regulates the turnover and endocytosis of extracellular matrix fibronectin. J Cell Sci 2011, 124:4039-4050.
65. Ezratty E.J., Bertaux C., Marcantonio E.E., Gundersen G.G. Clathrin mediates integrin endocytosis for focal adhesion disassembly in migrating cells. J Cell Biol 2009, 187:733-747.
66. Chao W.-T., Kunz J. Focal adhesion disassembly requires clathrin-dependent endocytosis of integrins. FEBS Lett 2009, 583:1337-1343.
67. Lobert V.H., Brech A., Pedersen N.M., Wesche J., Oppelt A., Malerød L., Stenmark H. Ubiquitination of α5β1 integrin controls fibroblast migration through lysosomal degradation of fibronectin-integrin complexes. Dev Cell 2010, 19:148-159.
68. Williams R.L., Urbé S. The emerging shape of the ESCRT machinery. Nat Rev Mol Cell Biol 2007, 8:355-368.
69. Cullen P.J. Endosomal sorting and signalling: an emerging role for sorting nexins. Nat Rev Mol Cell Biol 2008, 9:574-582.
70. Böttcher R.T., Stremmel C., Meves A., Meyer H., Widmaier M., Tseng H.Y., Fässler R. Sorting nexin 17 prevents lysosomal degradation of β1 integrins by binding to the β1-integrin tail. Nat Cell Biol 2012, 14:584-592.
71. Steinberg F., Heesom K.J., Bass M.D., Cullen P.J. SNX17 protects integrins from degradation by sorting between lysosomal and recycling pathways. J Cell Biol 2012, 197:219-230.
72. Komander D., Clague M.J., Urbé S. Breaking the chains: structure and function of the deubiquitinases. Nat Rev Mol Cell Biol 2009, 10:550-563.
73. Clague M.J., Coulson J.M., Urbé S. Cellular functions of the DUBs. J Cell Sci 2012, 125:277-286.
74. Scita G., Di Fiore P.P. The endocytic matrix. Nature 2010, 463:464-473.
75. Pines M, Das R, Ellis SJ, Morin A, Czerniecki S, Yuan L, Klose M, Coombs D, Tanentzapf G. Mechanical force regulates integrin turnover in Drosophila in vivo. Nat Cell Biol 2012, [Epub ahead of print]. http://dx.doi%3a%2010.1038/ncb2555.