Syndecan-4 independently regulates multiple small GTPases to promote fibroblast migration during wound healing

Small GTPases

Volumn 3, Issue 2, 2012, Pages 73-79

  Brooks, Rebecca ^a   Williamson, Rosalind C ^a   Bass, Mark D ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Arf6; Integrin; Migration; RhoA; RhoG, Rac1; Syndecan 4; Wound healing

Indexed keywords

ACID ANHYDRIDE HYDROLASE; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; GUANOSINE TRIPHOSPHATASE; RAC1 PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; RHOG PROTEIN; SYNDECAN 4; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 5;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL MATURATION; CELL MIGRATION; CONTROLLED STUDY; EMBRYO; ENDOCYTOSIS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME INHIBITION; ENZYME REACTIVATION; ENZYME REGULATION; FIBROBLAST; FIBROBLAST CULTURE; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PROTEIN FUNCTION; PROTEIN TRANSPORT; WOUND HEALING;

EID: 84861476052     PISSN: 21541248     EISSN: 21541256     Source Type: Journal    
DOI: 10.4161/sgtp.19301     Document Type: Article

References (32)

1. Shaw TJ, Martin P. Wound repair at a glance. J Cell Sci 2009; 122:3209-13; PMID:19726630; http://dx. doi.org/10.1242/jcs.031187
2. Tscharntke M, Pofahl R, Chrostek-Grashoff A, Smyth N, Niessen C, Niemann C, et al. Impaired epidermal wound healing in vivo upon inhibition or deletion of Rac1. J Cell Sci 2007; 120:1480-90; PMID:17389689; http://dx.doi.org/10.1242/jcs.03426
3. Hinz B. Formation and function of the myofibroblast during tissue repair. J Invest Dermatol 2007; 127:526-37; PMID:17299435; http://dx.doi.org/10.1038/sj.jid. 5700613
4. Kwon AH, Qiu Z, Hirao Y. Topical application of plasma fibronectin in full-thickness skin wound healing in rats. Exp Biol Med (Maywood) 2007; 232:935-41; PMID:17609510
5. Lin F, Ren XD, Doris G, Clark RA. Three-dimensional migration of human adult dermal fibroblasts from collagen lattices into fibrin/fibronectin gels requires syndecan-4 proteoglycan. J Invest Dermatol 2005; 124:906-13; PMID:15854029; http://dx.doi.org/10. 1111/j.0022-202X.2005.23740.x
6. Bass MD, Roach KA, Morgan MR, Mostafavi-Pour Z, Schoen T, Muramatsu T, et al. Syndecan-4-dependent Rac1 regulation determines directional migration in response to the extracellular matrix. J Cell Biol 2007; 177:527-38; PMID:17485492; http://dx.doi.org/10. 1083/jcb.200610076
7. Woods A, Couchman JR, Johansson S, Höök M. Adhesion and cytoskeletal organisation of fibroblasts in response to fibronectin fragments. EMBO J 1986; 5:665-70; PMID:3709521
8. Echtermeyer F, Streit M, Wilcox-Adelman S, Saoncella S, Denhez F, Detmar M, et al. Delayed wound repair and impaired angiogenesis in mice lacking syndecan-4. J Clin Invest 2001; 107:R9-14; PMID:11160142; http://dx.doi.org/10.1172/JCI10559
9. Bass MD, Morgan MR, Roach KA, Settleman J, Goryachev AB, Humphries MJ. p190RhoGAP is the convergence point of adhesion signals from a 5 β 1 integrin and syndecan-4. J Cell Biol 2008; 181:1013-26; PMID:18541700; http://dx.doi.org/10.1083/jcb. 200711129
10. Dovas A, Yoneda A, Couchman JR. PKCbetadependent activation of RhoA by syndecan-4 during focal adhesion formation. J Cell Sci 2006; 119:2837-46; PMID:16787950; http://dx.doi.org/10.1242/jcs. 03020
11. Bass MD, Williamson RC, Nunan RD, Humphries JD, Byron A, Morgan MR, et al. A syndecan-4 hair trigger initiates wound healing through caveolin-and RhoG-regulated integrin endocytosis. Dev Cell 2011; 21:681-93; PMID:21982645; http://dx.doi.org/10. 1016/j.devcel.2011.08.007
12. Elfenbein A, Rhodes JM, Meller J, Schwartz MA, Matsuda M, Simons M. Suppression of RhoG activity is mediated by a syndecan 4-synectin-RhoGDI1 complex and is reversed by PKCalpha in a Rac1 activation pathway. J Cell Biol 2009; 186:75-83; PMID: 19581409; http://dx.doi.org/10.1083/jcb.200810179
13. Katoh H, Negishi M. RhoG activates Rac1 by direct interaction with the Dock180-binding protein Elmo. Nature 2003; 424:461-4; PMID:12879077; http://dx. doi.org/10.1038/nature01817
14. Prieto-Sánchez RM, Berenjeno IM, Bustelo XR. Involvement of the Rho/Rac family member RhoG in caveolar endocytosis. Oncogene 2006; 25:2961-73; PMID:16568096; http://dx.doi.org/10.1038/sj.onc. 1209333
15. Samson T, Welch C, Monaghan-Benson E, Hahn KM, Burridge K. Endogenous RhoG is rapidly activated after epidermal growth factor stimulation through multiple guanine-nucleotide exchange factors. Mol Biol Cell 2010; 21:1629-42; PMID:20237158; http://dx.doi.org/10.1091/mbc.E09-09-0809
16. Donaldson JG, Jackson CL. ARF family G proteins and their regulators: roles in membrane transport, development and disease. Nat Rev Mol Cell Biol 2011; 12:362-75; PMID:21587297; http://dx.doi.org/10. 1038/nrm3117
17. D'Souza-Schorey C, Chavrier P. ARF proteins: roles in membrane traffic and beyond. Nat Rev Mol Cell Biol 2006; 7:347-58; PMID:16633337; http://dx.doi.org/ 10.1038/nrm1910
18. Caswell PT, Norman JC. Integrin trafficking and the control of cell migration. Traffic 2006; 7:14-21; PMID:16445683; http://dx.doi.org/10.1111/j.1600-0854.2005.00362.x
19. Powelka AM, Sun J, Li J, Gao M, Shaw LM, Sonnenberg A, et al. Stimulation-dependent recycling of integrin β1 regulated by ARF6 and Rab11. Traffic 2004; 5:20-36; PMID:14675422; http://dx.doi.org/ 10.1111/j.1600-0854.2004.00150.x
20. Poupart ME, Fessart D, Cotton M, Laporte SA, Claing A. ARF6 regulates angiotensin II type 1 receptor endocytosis by controlling the recruitment of AP-2 and clathrin. Cell Signal 2007; 19:2370-8; PMID:17719203; http://dx.doi.org/10.1016/j.cellsig.2007.07.015
21. Ikeda S, Ushio-Fukai M, Zuo L, Tojo T, Dikalov S, Patrushev NA, et al. Novel role of ARF6 in vascular endothelial growth factor-induced signaling and angiogenesis. Circ Res 2005; 96:467-75; PMID:15692085; http://dx.doi.org/10.1161/01.RES.0000158286.51045. 16
22. Ohkawara B, Glinka A, Niehrs C. Rspo3 binds syndecan 4 and induces Wnt/PCP signaling via clathrin-mediated endocytosis to promote morphogenesis. Dev Cell 2011; 20:303-14; PMID:21397842; http://dx.doi.org/10.1016/j.devcel.2011.01.006
23. Ezratty EJ, Bertaux C, Marcantonio EE, Gundersen GG. Clathrin mediates integrin endocytosis for focal adhesion disassembly in migrating cells. J Cell Biol 2009; 187:733-47; PMID:19951918; http://dx.doi. org/10.1083/jcb.200904054
24. Ridley AJ. Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol 2006; 16:522-9; PMID:16949823; http://dx. doi.org/10.1016/j.tcb.2006.08.006
25. Tkachenko E, Lutgens E, Stan RV, Simons M. Fibroblast growth factor 2 endocytosis in endothelial cells proceed via syndecan-4-dependent activation of Rac1 and a Cdc42-dependent macropinocytic pathway. J Cell Sci 2004; 117:3189-99; PMID:15226395; http://dx.doi.org/10.1242/jcs.01190
26. Koo BK, Jung YS, Shin J, Han I, Mortier E, Zimmermann P, et al. Structural basis of syndecan-4 phosphorylation as a molecular switch to regulate signaling. J Mol Biol 2006; 355:651-63; PMID: 16310216; http://dx.doi.org/10.1016/j.jmb.2005.09. 087
27. Dovas A, Choi Y, Yoneda A, Multhaupt HA, Kwon SH, Kang D, et al. Serine 34 phosphorylation of rho guanine dissociation inhibitor (RhoGDIalpha) links signaling from conventional protein kinase C to RhoGTPase in cell adhesion. J Biol Chem 2010; 285:23296-308; PMID:20472934; http://dx.doi.org/ 10.1074/jbc.M109.098129
28. Raftopoulou M, Hall A. Cell migration: Rho GTPases lead the way. Dev Biol 2004; 265:23-32; PMID: 14697350; http://dx.doi.org/10.1016/j.ydbio.2003.06. 003
29. Matthews HK, Marchant L, Carmona-Fontaine C, Kuriyama S, Larraín J, Holt MR, et al. Directional migration of neural crest cells in vivo is regulated by Syndecan-4/Rac1 and non-canonical Wnt signaling/ RhoA. Development 2008; 135:1771-80; PMID: 18403410; http://dx.doi.org/10.1242/dev.017350
30. Liu S, Kapoor M, Leask A. Rac1 expression by fibroblasts is required for tissue repair in vivo. Am J Pathol 2009; 174:1847-56; PMID:19349358; http:// dx.doi.org/10.2353/ajpath.2009.080779
31. Grande-García A, Echarri A, de Rooij J, Alderson NB, Waterman-Storer CM, Valdivielso JM, et al. Caveolin-1 regulates cell polarization and directional migration through Src kinase and Rho GTPases. J Cell Biol 2007; 177:683-94; PMID:17517963; http://dx.doi.org/ 10.1083/jcb.200701006
32. del Pozo MA, Alderson NB, Kiosses WB, Chiang HH, Anderson RG, Schwartz MA. Integrins regulate Rac targeting by internalization of membrane domains. Science 2004; 303:839-42; PMID:14764880; http:// dx.doi.org/10.1126/science.1092571