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Integrins: masters and slaves of endocytic transport

Caswell, Patrick T., Vadrevu, Suryakiran, Norman, Jim C.·2009·Nature Reviews Molecular Cell Biology
DOI 10.1038/nrm2799
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Abstract

Since it has become clear that adhesion receptors are trafficked through the endosomal pathway and that this can influence their function, much effort has been invested in obtaining detailed descriptions of the molecular machinery responsible for internalizing and recycling integrins. New findings indicate that integrin trafficking dictates the nature of Rho GTPase signalling during cytokinesis and cell migration. Furthermore, integrins can exert control over the trafficking of other receptors in a way that drives cancer cell invasion and tumour angiogenesis.

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Integrity signals

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Crossref · 10.1038/nrm2799

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  • Studies in cultured cells suggested a role of Dab2 in endocytic recycling and trafficking of integrins and thus impact cell mobility.

    “Studies in cultured cells suggested a role of Dab2 in endocytic recycling and trafficking of integrins and thus impact cell mobility”

    From Endocytosis and Physiology: Insights from Disabled-2 Deficient Mice (2016) · cites this paper as Caswell et al., 2009

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  1. Hynes, R. O. Integrins: bidirectional, allosteric signaling machines. Cell 110, 673–687 (2002). · DOI
  2. Schwartz, M. A. Integrin signaling revisited. Trends Cell Biol. 11, 466–470 (2001). · DOI
  3. Walker, J. L., Fournier, A. K. & Assoian, R. K. Regulation of growth factor signaling and cell cycle progression by cell adhesion and adhesion-dependent changes in cellular tension. Cytokine Growth Factor Rev. 16, 395–405 (2005). · DOI
  4. Harburger, D. S., Bouaouina, M. & Calderwood, D. A. Kindlin-1 and -2 directly bind the C-terminal region of β integrin cytoplasmic tails and exert integrin-specific activation effects. J. Biol. Chem. 284, 11485–11497 (2009). · DOI · Paper page
  5. Moser, M. et al. Kindlin-3 is required for β2 integrin-mediated leukocyte adhesion to endothelial cells. Nature Med. 15, 300–305 (2009). · DOI
  6. Moser, M., Legate, K. R., Zent, R. & Fassler, R. The tail of integrins, talin, and kindlins. Science 324, 895–899 (2009). · DOI
  7. Wegener, K. L. et al. Structural basis of integrin activation by talin. Cell 128, 171–182 (2007). · DOI
  8. Caswell, P. & Norman, J. Endocytic transport of integrins during cell migration and invasion. Trends Cell Biol. 18, 257–263 (2008). · DOI
  9. Caswell, P. T. & Norman, J. C. Integrin trafficking and the control of cell migration. Traffic 7, 14–21 (2006). · DOI
  10. Jones, M. C., Caswell, P. T. & Norman, J. C. Endocytic recycling pathways: emerging regulators of cell migration. Curr. Opin. Cell Biol. 18, 549–557 (2006). · DOI
  11. Pellinen, T. & Ivaska, J. Integrin traffic. J. Cell Sci. 119, 3723–3731 (2006). · DOI
  12. Bretscher, M. S. Moving membrane up to the front of migrating cells. Cell 85, 465–467 (1996). · DOI
  13. Pellinen, T. et al. Integrin trafficking regulated by Rab21 is necessary for cytokinesis. Dev. Cell 15, 371–385 (2008). Shows that integrins are trafficked under the control of RAB21 to the cytokinetic cleavage furrow, where they engage with the ECM to activate RhoA and drive the abscission reaction. This also indicates that the loss of RAB21 may drive genetic instability in cancer. · DOI
  14. Caswell, P. T. et al. Rab25 associates with α5β1 integrin to promote invasive migration in 3D microenvironments. Dev. Cell 13, 496–510 (2007). · DOI
  15. White, D. P., Caswell, P. T. & Norman, J. C. αvβ3 and α5β1 integrin recycling pathways dictate downstream Rho kinase signaling to regulate persistent cell migration. J. Cell Biol. 177, 515–525 (2007). · DOI
  16. Caswell, P. T. et al. Rab-coupling protein coordinates recycling of α5β1 integrin and EGFR1 to promote cell migration in 3D microenvironments. J. Cell Biol. 183, 143–155 (2008). Shows that RCP has a pivotal role in the recycling of α5β1 integrin and in coordinating its trafficking with that of EGFR1 as cells migrate on 3D matrices. The ability of RCP to function in this way is activated following inhibition of αvβ3 integrin. · DOI
  17. Reynolds, A. R. et al. Stimulation of tumor growth and angiogenesis by low concentrations of RGD-mimetic integrin inhibitors. Nature Med. 15, 392–400 (2009). Reveals that treatment with competitive inhibitors of αvβ3 integrin promotes angiogenesis in a similar manner to genetic knockout of β3 integrin. This is owing to upregulation of Rab4-dependent recycling of VEGFR2, which opposes receptor degradation. · DOI
  18. Shi, F. & Sottile, J. Caveolin-1-dependent β1 integrin endocytosis is a critical regulator of fibronectin turnover. J. Cell Sci. 121, 2360–2371 (2008). · DOI
  19. Galvez, B. G. et al. Caveolae are a novel pathway for membrane-type 1 matrix metalloproteinase traffic in human endothelial cells. Mol. Biol. Cell 15, 678–687 (2004). · DOI
  20. Nishimura, T. & Kaibuchi, K. Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3. Dev. Cell 13, 15–28 (2007). · DOI
  21. Vignoud, L., Usson, Y., Balzac, F., Tarone, G. & Block, M. R. Internalization of the α5β1 integrin does not depend on “NPXY” signals. Biochem. Biophys. Res. Commun. 199, 603–611 (1994). · DOI
  22. Ortiz, D. F. et al. Identification of HAX-1 as a protein that binds bile salt export protein and regulates its abundance in the apical membrane of Madin-Darby canine kidney cells. J. Biol. Chem. 279, 32761–32770 (2004). · DOI
  23. Ramsay, A. G. et al. HS1-associated protein X-1 regulates carcinoma cell migration and invasion via clathrin-mediated endocytosis of integrin αvβ6. Cancer Res. 67, 5275–5284 (2007). Reveals that αvβ6 integrin is likely to be important in the progression and invasion of cancer. HAX1 binds to the cytodomain of β6 integrin and promotes its trafficking in a way that drives invasion. · DOI
  24. Calderwood, D. A. et al. Integrin β cytoplasmic domain interactions with phosphotyrosine-binding domains: a structural prototype for diversity in integrin signaling. Proc. Natl Acad. Sci. USA 100, 2272–2277 (2003). · DOI
  25. Chao, W. T. & Kunz, J. Focal adhesion disassembly requires clathrin-dependent endocytosis of integrins. FEBS Lett. 583, 1337–1343 (2009). · DOI · Paper page
  26. Teckchandani, A. et al. Quantitative proteomics identifies a Dab2/integrin module regulating cell migration. J. Cell Biol. 186, 99–111 (2009). A novel proteomic approach to the identification of endocytic cargos highlights β1 integrins as the main clients of DAB2-regulated, clathrin-dependent internalization. · DOI · Paper page
  27. Ezratty, E. J., Partridge, M. A. & Gundersen, G. G. Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nature Cell Biol. 7, 581–590 (2005). · DOI
  28. Valdembri, D. et al. Neuropilin-1/GIPC1 signaling regulates α5β1 integrin traffic and function in endothelial cells. PLoS Biol. 7, e25 (2009). Use of novel photoactivation and FRET–FLIM microscopy to define an interaction between α5β1 integrin and NRP1 and how this functions in integrin trafficking and fibronectin polymerization during angiogenesis. · DOI
  29. Shimizu, M., Murakami, Y., Suto, F. & Fujisawa, H. Determination of cell adhesion sites of neuropilin-1. J. Cell Biol. 148, 1283–1293 (2000). · DOI
  30. Soker, S., Takashima, S., Miao, H. Q., Neufeld, G. & Klagsbrun, M. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 92, 735–745 (1998). · DOI
  31. Naccache, S. N., Hasson, T. & Horowitz, A. Binding of internalized receptors to the PDZ domain of GIPC/synectin recruits myosin VI to endocytic vesicles. Proc. Natl Acad. Sci. USA 103, 12735–12740 (2006). · DOI
  32. Salikhova, A. et al. Vascular endothelial growth factor and semaphorin induce neuropilin-1 endocytosis via separate pathways. Circ. Res. 103, e71–e79 (2008). · DOI · Paper page
  33. Sigismund, S. et al. Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Dev. Cell 15, 209–219 (2008). · DOI
  34. Ng, T. et al. PKCα regulates β1 integrin-dependent cell motility through association and control of integrin traffic. EMBO J. 18, 3909–3923 (1999). · DOI
  35. Upla, P. et al. Clustering induces a lateral redistribution of α2β1 integrin from membrane rafts to caveolae and subsequent protein kinase C-dependent internalization. Mol. Biol. Cell 15, 625–636 (2004). · DOI
  36. Fabbri, M. et al. Dynamic partitioning into lipid rafts controls the endo–exocytic cycle of the αL/β2 integrin, LFA-1, during leukocyte chemotaxis. Mol. Biol. Cell 16, 5793–5803 (2005). · DOI
  37. Fabbri, M. et al. A tyrosine-based sorting signal in the β2 integrin cytoplasmic domain mediates its recycling to the plasma membrane and is required for ligand-supported migration. EMBO J. 18, 4915–4925 (1999). · DOI
  38. Valdez-Taubas, J. & Pelham, H. R. Slow diffusion of proteins in the yeast plasma membrane allows polarity to be maintained by endocytic cycling. Curr. Biol. 13, 1636–1640 (2003). · DOI
  39. Jekely, G., Sung, H. H., Luque, C. M. & Rorth, P. Regulators of endocytosis maintain localized receptor tyrosine kinase signaling in guided migration. Dev. Cell 9, 197–207 (2005). · DOI
  40. Palamidessi, A. et al. Endocytic trafficking of Rac is required for the spatial restriction of signaling in cell migration. Cell 134, 135–147 (2008). Shows that endocytosis is required to bring Rac into contact with one of its exchange factors, Tiam1, at endosomal membranes. Active Rac is then returned to the nearby plasma membrane by an Arf6-dependent recycling pathway to maintain localized actin polymerization in dorsal ruffles. · DOI
  41. Pierini, L. M., Lawson, M. A., Eddy, R. J., Hendey, B. & Maxfield, F. R. Oriented endocytic recycling of α5β1 in motile neutrophils. Blood 95, 2471–2480 (2000). · DOI
  42. Rappoport, J. Z. & Simon, S. M. Real-time analysis of clathrin-mediated endocytosis during cell migration. J. Cell Sci. 116, 847–855 (2003). · DOI
  43. Laukaitis, C. M., Webb, D. J., Donais, K. & Horwitz, A. F. Differential dynamics of α5 integrin, paxillin, and α-actinin during formation and disassembly of adhesions in migrating cells. J. Cell Biol. 153, 1427–1440 (2001). · DOI
  44. 45. Hopkins, C. R., Gibson, A., Shipman, M., Strickland, D. K. & Trowbridge, I. S. In migrating fibroblasts, recycling receptors are concentrated in narrow tubules in the pericentriolar area, and then routed to the plasma membrane of the leading lamella. J. Cell Biol. 125, 1265–1274 (1994). · DOI
  45. Prigozhina, N. L. & Waterman-Storer, C. M. Protein kinase D-mediated anterograde membrane trafficking is required for fibroblast motility. Curr. Biol. 14, 88–98 (2004). · DOI
  46. Schmoranzer, J., Kreitzer, G. & Simon, S. M. Migrating fibroblasts perform polarized, microtubule-dependent exocytosis towards the leading edge. J. Cell Sci. 116, 4513–4519 (2003). · DOI
  47. Pellinen, T. et al. Small GTPase Rab21 regulates cell adhesion and controls endosomal traffic of β1-integrins. J. Cell Biol. 173, 767–780 (2006). · DOI
  48. Ridley, A. J. et al. Cell migration: integrating signals from front to back. Science 302, 1704–1709 (2003). · DOI
  49. Pankov, R. et al. A Rac switch regulates random versus directionally persistent cell migration. J. Cell Biol. 170, 793–802 (2005). · DOI
  50. Sturge, J., Wienke, D. & Isacke, C. M. Endosomes generate localized Rho–ROCK–MLC2-based contractile signals via Endo180 to promote adhesion disassembly. J. Cell Biol. 175, 337–347 (2006). · DOI
  51. Danen, E. H. et al. Integrins control motile strategy through a Rho–cofilin pathway. J. Cell Biol. 169, 515–526 (2005). · DOI · Paper page
  52. Bement, W. M., Benink, H. A. & von Dassow, G. A microtubule-dependent zone of active RhoA during cleavage plane specification. J. Cell Biol. 170, 91–101 (2005). · DOI
  53. Wilson, G. M. et al. The FIP3–Rab11 protein complex regulates recycling endosome targeting to the cleavage furrow during late cytokinesis. Mol. Biol. Cell 16, 849–860 (2005). · DOI
  54. Cao, J., Albertson, R., Riggs, B., Field, C. M. & Sullivan, W. Nuf, a Rab11 effector, maintains cytokinetic furrow integrity by promoting local actin polymerization. J. Cell Biol. 182, 301–313 (2008). · DOI
  55. Narumiya, S. & Yasuda, S. Rho GTPases in animal cell mitosis. Curr. Opin. Cell Biol. 18, 199–205 (2006). · DOI
  56. del Pozo, M. A. et al. Integrins regulate Rac targeting by internalization of membrane domains. Science 303, 839–842 (2004). · DOI
  57. del Pozo, M. A. et al. Phospho-caveolin-1 mediates integrin-regulated membrane domain internalization. Nature Cell Biol. 7, 901–908 (2005). · DOI
  58. Balasubramanian, N., Scott, D. W., Castle, J. D., Casanova, J. E. & Schwartz, M. A. Arf6 and microtubules in adhesion-dependent trafficking of lipid rafts. Nature Cell Biol. 9, 1381–1391 (2007). Shows that Arf6 contributes to Rac activation by promoting the recycling of internalized lipid rafts to the plasma membrane. · DOI
  59. Nisato, R. E., Tille, J. C., Jonczyk, A., Goodman, S. L. & Pepper, M. S. αvβ3 and αvβ5 integrin antagonists inhibit angiogenesis in vitro. Angiogenesis 6, 105–119 (2003). · DOI
  60. Maubant, S. et al. Blockade of αvβ3 and αvβ5 integrins by RGD mimetics induces anoikis and not integrin-mediated death in human endothelial cells. Blood 108, 3035–3044 (2006). · DOI
  61. Stupp, R. & Ruegg, C. Integrin inhibitors reaching the clinic. J. Clin. Oncol. 25, 1637–1638 (2007). · DOI
  62. Tucker, G. C. Integrins: molecular targets in cancer therapy. Curr. Oncol. Rep. 8, 96–103 (2006). · DOI
  63. Dechantsreiter, M. A. et al. N-methylated cyclic RGD peptides as highly active and selective αVβ3 integrin antagonists. J. Med. Chem. 42, 3033–3040 (1999). · DOI · Paper page
  64. Reynolds, L. E. et al. Enhanced pathological angiogenesis in mice lacking β3 integrin or β3 and β5 integrins. Nature Med. 8, 27–34 (2002). · DOI
  65. Irie, H. Y. et al. Distinct roles of Akt1 and Akt2 in regulating cell migration and epithelial–mesenchymal transition. J. Cell Biol. 171, 1023–1034 (2005). · DOI
  66. Mills, G. B., Jurisica, I., Yarden, Y. & Norman, J. C. Genomic amplicons target vesicle recycling in breast cancer. J. Clin. Invest. 119, 2123–2127 (2009).
  67. Zhang, J. et al. RCP is a human breast cancer-promoting gene with Ras-activating function. J. Clin. Invest. 119, 2171–2183 (2009). A novel genetic screen that identifies RCP as an oncogenic driver in a common form of breast cancer. Increased RCP levels are shown to contribute to increased migration of cancer cells.
  68. Zhong, C. et al. Rho-mediated contractility exposes a cryptic site in fibronectin and induces fibronectin matrix assembly. J. Cell Biol. 141, 539–551 (1998). · DOI
  69. Pankov, R. et al. Integrin dynamics and matrix assembly: tensin-dependent translocation of α5β1 integrins promotes early fibronectin fibrillogenesis. J. Cell Biol. 148, 1075–1090 (2000). · DOI · Paper page
  70. Jones, M. C. et al. VEGFR1 (Flt1) regulates Rab4 recycling to control fibronectin polymerization and endothelial vessel branching. Traffic 10, 754–766 (2009). · DOI
  71. Sakai, T., Larsen, M. & Yamada, K. M. Fibronectin requirement in branching morphogenesis. Nature 423, 876–881 (2003). · DOI
  72. Serrels, A. et al. Real-time study of E-cadherin and membrane dynamics in living animals: implications for disease modeling and drug development. Cancer Res. 69, 2714–2719 (2009). · DOI
  73. De Deyne, P. G. et al. The vitronectin receptor associates with clathrin-coated membrane domains via the cytoplasmic domain of its β5 subunit. J. Cell Sci. 111, 2729–2740 (1998). · DOI
  74. Liu, L. et al. Tetraspanin CD151 promotes cell migration by regulating integrin trafficking. J. Biol. Chem. 282, 31631–31642 (2007). · DOI
  75. Panicker, A. K., Buhusi, M., Erickson, A. & Maness, P. F. Endocytosis of β1 integrins is an early event in migration promoted by the cell adhesion molecule L1. Exp. Cell Res. 312, 299–307 (2006).
  76. Parsons, M. et al. Site-directed perturbation of protein kinase C–integrin interaction blocks carcinoma cell chemotaxis. Mol. Cell. Biol. 22, 5897–5911 (2002). · DOI
  77. Altankov, G. & Grinnell, F. Fibronectin receptor internalization and AP-2 complex reorganization in potassium-depleted fibroblasts. Exp. Cell Res. 216, 299–309 (1995). · DOI
  78. Cera, M. R. et al. JAM-A promotes neutrophil chemotaxis by controlling integrin internalization and recycling. J. Cell Sci. 122, 268–277 (2009). · DOI
  79. Dunphy, J. L. et al. The Arf6 GEF GEP100/BRAG2 regulates cell adhesion by controlling endocytosis of β1 integrins. Curr. Biol. 16, 315–320 (2006). · DOI
  80. Woods, A. J., White, D. P., Caswell, P. T. & Norman, J. C. PKD1/PKCμ promotes αvβ3 integrin recycling and delivery to nascent focal adhesions. EMBO J. 23, 2531–2543 (2004). · DOI
  81. Vukmirica, J., Monzo, P., Le Marchand-Brustel, Y. & Cormont, M. The Rab4A effector protein Rabip4 is involved in migration of NIH 3T3 fibroblasts. J. Biol. Chem. 281, 36360–36368 (2006). · DOI
  82. Ivaska, J. et al. PKCɛ-mediated phosphorylation of vimentin controls integrin recycling and motility. EMBO J. 24, 3834–3845 (2005). · DOI
  83. Ivaska, J., Whelan, R. D., Watson, R. & Parker, P. J. PKCɛ controls the traffic of β1 integrins in motile cells. EMBO J. 21, 3608–3619 (2002). · DOI
  84. Jovic, M., Naslavsky, N., Rapaport, D., Horowitz, M. & Caplan, S. EHD1 regulates β1 integrin endosomal transport: effects on focal adhesions, cell spreading and migration. J. Cell Sci. 120, 802–814 (2007). · DOI
  85. Tayeb, M. A. et al. Inhibition of SNARE-mediated membrane traffic impairs cell migration. Exp. Cell Res. 305, 63–73 (2005). · DOI
  86. Li, J. et al. Phosphorylation of ACAP1 by Akt regulates the stimulation-dependent recycling of integrin β1 to control cell migration. Dev. Cell 9, 663–673 (2005). · DOI

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Metadata

Authors
Caswell, P. T., Vadrevu, S., & Norman, J. C.
Venue
Nature Reviews Molecular Cell Biology
Publisher
Springer Science and Business Media LLC
Published
2009-12
Volume
10
Issue
12
Pages
843-853
ISSN
  • 1471-0072
  • 1471-0080
DOI
10.1038/nrm2799
Cited by
460
References
1
Language
en
Licence
www.springer.com/tdm (tdm)

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