Insights into the biological functions of Dock family guanine nucleotide exchange factors

Genes and Development

Volumn 28, Issue 6, 2014, Pages 533-547

  Laurin, Mélanie ^a,b   Côté, Jean François ^a,b,c  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

Dock180; Elmo; Migration; Mouse models; Myoblast fusion; Neurogenesis

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CELL SURFACE PROTEIN; CHEMOKINE RECEPTOR CXCR4; DBL PROTEIN; DOCK PROTEIN; DOCK1 PROTEIN; DOCK2 PROTEIN; DOCK5 PROTEIN; EPHRIN B3; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE; MEMBRANE PROTEIN; NETRIN; PERTUSSIS TOXIN; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN CDC42; RAC PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; STROMAL CELL DERIVED FACTOR 1; UNCLASSIFIED DRUG;

ADAMS OLIVER SYNDROME; BRAIN DEVELOPMENT; BREAST CANCER; CAENORHABDITIS ELEGANS; CANCER GROWTH; CELL ADHESION; CELL MIGRATION; CELL POLARITY; CYTOSKELETON; DOWN REGULATION; DROSOPHILA; ENDOTHELIUM CELL; EPITHELIAL MESENCHYMAL TRANSITION; FIBROBLAST; GENE MUTATION; GLIOBLASTOMA; HIPPOCAMPUS; HUMAN; METASTASIS; MICROCEPHALY; MYOBLAST; NERVOUS SYSTEM DEVELOPMENT; NEURAL TUBE; NEUTROPHIL; NONHUMAN; OSTEOCLAST; OSTEOLYSIS; POLARIZATION; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REVIEW; SENSORIMOTOR FUNCTION; SIGNAL TRANSDUCTION; SPINAL GANGLION; TUMOR INVASION; VASCULARIZATION;

DOCK180; ELMO; MIGRATION; MOUSE MODELS; MYOBLAST FUSION; NEUROGENESIS;

ANIMALS; DISEASE; ENZYME ACTIVATION; GROWTH AND DEVELOPMENT; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; NEUROGENESIS; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EID: 84896363604     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.236349.113     Document Type: Review

References (97)

1. Abmayr SM, Pavlath GK. 2012. Myoblast fusion: lessons from flies and mice. Development 139: 641-656.
2. Alan JK, Lundquist EA. 2013. Mutationally activated Rho GTPases in cancer. Small GTPases 4: 159-163.
3. Allen KM, Gleeson JG, Bagrodia S, Partington MW, MacMillan JC, Cerione RA, Mulley JC, Walsh CA. 1998. PAK3 mutation in nonsyndromic X-linked mental retardation. Nat Genet 20: 25-30.
4. Bergmann C, Zerres K, Senderek J, Rudnik-Schoneborn S, Eggermann T, Hausler M, Mull M, Ramaekers VT. 2003. Oligophrenin 1 (OPHN1) gene mutation causes syndromic X-linked mental retardation with epilepsy, rostral ventricular enlargement and cerebellar hypoplasia. Brain 126: 1537-1544.
5. Blasius AL, Brandl K, Crozat K, Xia Y, Khovananth K, Krebs P, Smart NG, Zampolli A, Ruggeri ZM, Beutler BA. 2009. Mice with mutations of Dock7 have generalized hypopigmentation and white-spotting but show normal neurological function. Proc Natl Acad Sci 106: 2706-2711.
6. Bryan BA, Li D, Wu X, Liu M. 2005. The Rho family of small GTPases: crucial regulators of skeletal myogenesis. Cell Mol Life Sci 62: 1547-1555.
7. Cancelas JA, Williams DA. 2009. Rho GTPases in hematopoietic stem cell functions. Curr Opin Hematol 16: 249-254.
8. Castets M, Coissieux MM, Delloye-Bourgeois C, Bernard L, Delcros JG, Bernet A, Laudet V, Mehlen P. 2009. Inhibition of endothelial cell apoptosis by netrin-1 during angiogenesis. Dev Cell 16: 614-620.
9. Chen Q, Peto CA, Shelton GD, Mizisin A, Sawchenko PE, Schubert D. 2009. Loss of modifier of cell adhesion reveals a pathway leading to axonal degeneration. J Neurosci 29: 118-130.
10. Cichorek M, Wachulska M, Stasiewicz A, Tyminska A. 2013. Skin melanocytes: biology and development. Postepy Dermatol Alergol 30: 30-41.
11. Cote JF, Vuori K. 2002. Identification of an evolutionarily conserved superfamily of DOCK180-related proteins with guanine nucleotide exchange activity. J Cell Sci 115: 4901-4913.
12. Cote JF, Vuori K. 2006. In vitro guanine nucleotide exchange activity of DHR-2/DOCKER/CZH2 domains. Methods Enzymol 406: 41-57.
13. Cote JF, Vuori K. 2007. GEF what? Dock180 and related proteins help Rac to polarize cells in new ways. Trends Cell Biol 17: 383-393.
14. Duchek P, Somogyi K, Jekely G, Beccari S, Rorth P. 2001. Guidance of cell migration by the Drosophila PDGF/VEGF receptor. Cell 107: 17-26.
15. Dulak AM, Stojanov P, Peng S, Lawrence MS, Fox C, Stewart C, Bandla S, Imamura Y, Schumacher SE, Shefler E, et al. 2013. Exome and whole-genome sequencing of esophageal adenocarcinoma identifies recurrent driver events and mutational complexity. Nat Genet 45: 478-486.
16. Elliott MR, Zheng S, Park D, Woodson RI, Reardon MA, Juncadella IJ, Kinchen JM, Zhang J, Lysiak JJ, Ravichandran KS. 2010. Unexpected requirement for ELMO1 in clearance of apoptotic germ cells in vivo. Nature 467: 333-337.
17. Elsegood CL, Zhuo Y, Wesolowski GA, Hamilton JA, Rodan GA, Duong LT. 2006. M-CSF induces the stable interaction of cFms with αVβ3 integrin in osteoclasts. Int J Biochem Cell Biol 38: 1518-1529.
18. Epting D, Wendik B, Bennewitz K, Dietz CT, Driever W, Kroll J. 2010. The Rac1 regulator ELMO1 controls vascular morphogenesis in zebrafish. Circ Res 107: 45-55.
19. Feng H, Hu B, Liu KW, Li Y, Lu X, Cheng T, Yiin JJ, Lu S, Keezer S, Fenton T, et al. 2011. Activation of Rac1 by Src-dependent phosphorylation of Dock180(Y1811) mediates PDGFRαstimulated glioma tumorigenesis in mice and humans. J Clin Invest 121: 4670-4684.
20. Feng H, Hu B, Jarzynka MJ, Li Y, Keezer S, Johns TG, Tang CK, Hamilton RL, Vuori K, Nishikawa R, et al. 2012. Phosphorylation of dedicator of cytokinesis 1 (Dock180) at tyrosine residue Y722 by Src family kinases mediates EGFRvIIIdriven glioblastoma tumorigenesis. Proc Natl Acad Sci 109: 3018-3023.
21. Feng H, Hu B, Vuori K, Sarkaria JN, Furnari FB, Cavenee WK, Cheng SY. 2013. EGFRvIII stimulates glioma growth and invasion through PKA-dependent serine phosphorylation of Dock180. Oncogene doi: 10.1038/onc.2013.198.
22. Friedl P, Wolf K. 2003. Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 3: 362-374.
23. Fukui Y, Hashimoto O, Sanui T, Oono T, Koga H, AbeM, Inayoshi A, Noda M, Oike M, Shirai T, et al. 2001. Haematopoietic cellspecific CDM family protein DOCK2 is essential for lymphocyte migration. Nature 412: 826-831.
24. Gadea G, Sanz-Moreno V, Self A, Godi A, Marshall CJ. 2008. DOCK10-mediated Cdc42 activation is necessary for amoeboid invasion of melanoma cells. Curr Biol 18: 1456-1465.
25. Hall A, Lalli G. 2010. Rho and Ras GTPases in axon growth, guidance, and branching. Cold Spring Harb Perspect Biol 2: a001818.
26. Hamoud N, Tran V, Croteau L-P, Kania A, Côté J-F. 2014. G-protein coupled receptor BAI3 controls myoblast fusion in vertebrates. Proc Natl Acad Sci doi: 10.1073/pnas. 1313886111.
27. Hanawa-Suetsugu K, Kukimoto-Niino M, Mishima-Tsumagari C, Akasaka R, Ohsawa N, Sekine S, Ito T, Tochio N, Koshiba S, Kigawa T, et al. 2012. Structural basis for mutual relief of the Rac guanine nucleotide exchange factor DOCK2 and its partner ELMO1 from their autoinhibited forms. Proc Natl Acad Sci 109: 3305-3310.
28. Harada Y, Tanaka Y, Terasawa M, Pieczyk M, Habiro K, Katakai T, Hanawa-Suetsugu K, Kukimoto-Niino M, Nishizaki T, Shirouzy M, et al. 2012. DOCK8 is a Cdc42 activator critical for interstitial dendritic cell migration during immune responses. Blood 119: 4451-4461.
29. Hart MJ, Eva A, Evans T, Aaronson SA, Cerione RA. 1991. Catalysis of guanine nucleotide exchange on the CDC42Hs protein by the dbl oncogene product. Nature 354: 311-314.
30. Heasman SJ, Ridley AJ. 2008. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol 9: 690-701.
31. Hochreiter-Hufford AE, Lee CS, Kinchen JM, Sokolowski JD, Arandjelovic S, Call JA, Klibanov AL, Yan Z, Mandell JW, Ravichandran KS. 2013. Phosphatidylserine receptor BAI1 and apoptotic cells as new promoters of myoblast fusion. Nature 497: 263-267.
32. Jarzynka MJ, Hu B, Hui KM, Bar-Joseph I, Gu W, Hirose T, Haney LB, Ravichandran KS, Nishikawa R, Cheng SY. 2007. ELMO1 and Dock180, a bipartite Rac1 guanine nucleotide exchange factor, promote human glioma cell invasion. Cancer Res 67: 7203-7211.
33. Jurdic P, Saltel F, Chabadel A, Destaing O. 2006. Podosome and sealing zone: specificity of the osteoclast model. Eur J Cell Biol 85: 195-202.
34. Kashiwa A, Yoshida H, Lee S, Paladino T, Liu Y, Chen Q, Dargusch R, Schubert D, Kimura H. 2000. Isolation and characterization of novel presenilin binding protein. J Neurochem 75: 109-116.
35. Kawazu M, Ueno T, Kontani K, Ogita Y, Ando M, Fukumura K, Yamato A, Soda M, Takeuchi K, Miki Y, et al. 2013. Transforming mutations of RAC guanosine triphosphatases in human cancers. Proc Natl Acad Sci 110: 3029-3034.
36. 3. Biochem J 354: 73-78.
37. Komander D, Patel M, Laurin M, Fradet N, Pelletier A, Barford D, Cote JF. 2008. An α-helical extension of the ELMO1 pleckstrin homology domain mediates direct interaction to DOCK180 and is critical in Rac signaling. Mol Biol Cell 19: 4837-4851.
38. Krauthammer M, Kong Y, Ha BH, Evans P, Bacchiocchi A, McCusker JP, Cheng E, Davis MJ, Goh G, Choi M, et al. 2012. Exome sequencing identifies recurrent somatic RAC1 mutations in melanoma. Nat Genet 44: 1006-1014.
39. Kunisaki Y, Nishikimi A, Tanaka Y, Takii R, Noda M, Inayoshi A, Watanabe K, Sanematsu F, Sasazuki T, Sasaki T, et al. 2006. DOCK2 is a Rac activator that regulates motility and polarity during neutrophil chemotaxis. J Cell Biol 174: 647-652.
40. Larrivee B, Freitas C, Suchting S, Brunet I, Eichmann A. 2009. Guidance of vascular development: lessons from the nervous system. Circ Res 104: 428-441.
41. Laurin M, Fradet N, Blangy A, Hall A, Vuori K, Cote JF. 2008. The atypical Rac activator Dock180 (Dock1) regulates myoblast fusion in vivo. Proc Natl Acad Sci 105: 15446-15451.
42. Laurin M, Huber J, Pelletier A, Houalla T, Park M, Fukui Y, Haibe-Kains B, Muller WJ, Cote JF. 2013. Rac-specific guanine nucleotide exchange factor DOCK1 is a critical regulator of HER2-mediated breast cancer metastasis. Proc Natl Acad Sci 110: 7434-7439.
43. Lazer G, Katzav S. 2011. Guanine nucleotide exchange factors for RhoGTPases: good therapeutic targets for cancer therapy? Cell Signal 23: 969-979.
44. Li X, Gao X, Liu G, Xiong W, Wu J, Rao Y. 2008. Netrin signal transduction and the guanine nucleotide exchange factor DOCK180 in attractive signaling. Nat Neurosci 11: 28-35.
45. Li H, Yang L, Fu H, Yan J, Wang Y, Guo H, Hao X, Xu X, Jin T, Zhang N. 2013. Association between Gαi2 and ELMO1/ Dock180 connects chemokine signalling with Rac activation and metastasis. Nat Commun 4: 1706.
46. Lin Q, Yang W, Baird D, Feng Q, Cerione RA. 2006. Identification of a DOCK180-related guanine nucleotide exchange factor that is capable of mediating a positive feedback activation of Cdc42. J Biol Chem 281: 35253-35262.
47. Lu X, Le Noble F, Yuan L, Jiang Q, De Lafarge B, Sugiyama D, Breant C, Claes F, De Smet F, Thomas JL, et al. 2004. The netrin receptor UNC5B mediates guidance events controlling morphogenesis of the vascular system. Nature 432: 179-186.
48. Lu M, Kinchen JM, Rossman KL, Grimsley C, Hall M, Sondek J, Hengartner MO, Yajnik V, Ravichandran KS. 2005. A Stericinhibition model for regulation of nucleotide exchange via the Dock180 family of GEFs. Curr Biol 15: 371-377.
49. Lu Z, Elliott MR, Chen Y, Walsh JT, Klibanov AL, Ravichandran KS, Kipnis J. 2011. Phagocytic activity of neuronal progenitors regulates adult neurogenesis. Nat Cell Biol 13: 1076-1083.
50. Luo L, O'Leary DD. 2005. Axon retraction and degeneration in development and disease. Annu Rev Neurosci 28: 127-156.
51. Margaron Y, Fradet N, Cote JF. 2013. ELMO recruits actin crosslinking family 7 (ACF7) at the cell membrane for microtubule capture and stabilization of cellular protrusions. J Biol Chem 288: 1184-1199.
52. Meller N, Irani-Tehrani M, Kiosses WB, Del Pozo MA, Schwartz MA. 2002. Zizimin1, a novel Cdc42 activator, reveals a new GEF domain for Rho proteins. Nat Cell Biol 4: 639-647.
53. Miyamoto Y, Torii T, Yamamori N, Ogata T, Tanoue A, Yamauchi J. 2013. Akt and PP2A reciprocally regulate the guanine nucleotide exchange factor Dock6 to control axon growth of sensory neurons. Sci Signal 6: ra15.
54. Montell DJ, Yoon WH, Starz-Gaiano M. 2012. Group choreography: mechanisms orchestrating the collective movement of border cells. Nat Rev Mol Cell Biol 13: 631-645.
55. Moore CA, Parkin CA, Bidet Y, Ingham PW. 2007. A role for the Myoblast city homologues Dock1and Dock5 and the adaptor proteins Crk and Crk-like in zebrafish myoblast fusion. Development 134: 3145-3153.
56. Nagai Y, Osawa K, Fukushima H, Tamura Y, Aoki K, Ohya K, Yasuda H, Hikiji H, Takahashi M, Seta Y, et al. 2013. p130Cas plays important roles in osteoclastic bone resorption. J Bone Miner Res 28: 2449-2462.
57. Nakamura I, Jimi E, Duong LT, Sasaki T, Takahashi N, Rodan GA, Suda T. 1998. Tyrosine phosphorylation of p130Cas is involved in actin organization in osteoclasts. J Biol Chem 273: 11144-11149.
58. Nakamura I, Rodan GA, Duong LT. 2003. Distinct roles of p130Cas and c-Cbl in adhesion-induced or macrophage colony-stimulating factor-mediated signaling pathways in prefusion osteoclasts. Endocrinology 144: 4739-4741.
59. Namekata K, Harada C, Taya C, Guo X, Kimura H, Parada LF, Harada T. 2010. Dock3 induces axonal outgrowth by stimulating membrane recruitment of the WAVE complex. Proc Natl Acad Sci 107: 7586-7591.
60. Namekata K, Harada C, Guo X, Kimura A, Kittaka D, Watanabe H, Harada T. 2012. Dock3 stimulates axonal outgrowth via GSK-3β-mediated microtubule assembly. J Neurosci 32: 264-274.
61. Nishikimi A, Fukuhara H, Su W, Hongu T, Takasuga S, Mihara H, Cao Q, Sanematsu F, Kanai M, Hasegawa H, et al. 2009. Sequential regulation of DOCK2 dynamics by two phospholipids during neutrophil chemotaxis. Science 324: 384-387.
62. Nishikimi A, Kukimoto-Niino M, Yokoyama S, Fukui Y. 2013. Immune regulatory functions of DOCK family proteins in health and disease. Exp Cell Res 319: 2343-2349.
63. Nugent AA, Kolpak AL, Engle EC. 2012. Human disorders of axon guidance. Curr Opin Neurobiol 22: 837-843.
64. Omi N, Kiyokawa E, Matsuda M, Kinoshita K, Yamada S, Yamada K, Matsushima Y, Wang Y, Kawai J, Suzuki M, et al. 2008. Mutation of Dock5, a member of the guanine exchange factor Dock180 superfamily, in the rupture of lens cataract mouse. Exp Eye Res 86: 828-834.
65. Park D, Tosello-Trampont AC, Elliott MR, Lu M, Haney LB, Ma Z, Klibanov AL, Mandell JW, Ravichandran KS. 2007. BAI1 is an engulfment receptor for apoptotic cells upstream of the ELMO/Dock180/Rac module. Nature 450: 430-434.
66. Patel M, Margaron Y, Fradet N, Yang Q, Wilkes B, Bouvier M, Hofmann K, Cote JF. 2010. An evolutionarily conserved autoinhibitory molecular switch in ELMO proteins regulates Rac signaling. Curr Biol 20: 2021-2027.
67. Patel M, Chiang TC, Tran V, Lee FJ, Cote JF. 2011a. The Arf family GTPase Arl4A complexes with ELMO proteins to promote actin cytoskeleton remodeling and reveals a versatile Ras-binding domain in the ELMO proteins family. J Biol Chem 286: 38969-38979.
68. Patel M, Pelletier A, Cote JF. 2011b. Opening up on ELMO regulation: new insights into the control of Rac signaling by the DOCK180/ELMO complex. Small GTPases 2: 268-275.
69. Pittenger C, Duman RS. 2008. Stress, depression, and neuroplasticity: a convergence of mechanisms. Neuropsychopharmacology 33: 88-109.
70. Ransome MI, Renoir T, Hannan AJ. 2012. Hippocampal neurogenesis, cognitive deficits and affective disorder in Huntington's disease. Neural Plast 2012: 874387.
71. Riccomagno MM, Hurtado A, Wang H, Macopson JG, Griner EM, Betz A, Brose N, Kazanietz MG, Kolodkin AL. 2012. The RacGAP β2-Chimaerin selectively mediates axonal pruning in the hippocampus. Cell 149: 1594-1606.
72. Ron D, Zannini M, Lewis M, Wickner RB, Hunt LT, Graziani G, Tronick SR, Aaronson SA, Eva A. 1991. A region of proto-dbl essential for its transforming activity shows sequence similarity to a yeast cell cycle gene, CDC24, and the human breakpoint cluster gene, bcr. New Biol 3: 372-379.
73. Rossman KL, Der CJ, Sondek J. 2005. GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat Rev Mol Cell Biol 6: 167-180.
74. Round J, Stein E. 2007. Netrin signaling leading to directed growth cone steering. Curr Opin Neurobiol 17: 15-21.
75. Sanematsu F, Hirashima M, Laurin M, Takii R, Nishikimi A, Kitajima K, Ding G, Noda M, Murata Y, Tanaka Y, et al. 2010. DOCK180 is a Rac activator that regulates cardiovascular development by acting downstream of CXCR4. Circ Res 107: 1102-1105.
76. Sanematsu F, Nishikimi A, Watanabe M, Hongu T, Tanaka Y, Kanaho Y, Cote JF, Fukui Y. 2013. Phosphatidic aciddependent recruitment and function of the Rac activator DOCK1 during dorsal ruffle formation. J Biol Chem 288: 8092-8100.
77. Sanz-Moreno V, Gadea G, Ahn J, Paterson H, Marra P, Pinner S, Sahai E, Marshall CJ. 2008. Rac activation and inactivation control plasticity of tumor cell movement. Cell 135: 510-523.
78. Shaheen R, Faqeih E, Sunker A, Morsy H, Al-Sheddi T, Shamseldin HE, Adly N, Hashem M, Alkuraya FS. 2011. Recessive mutations in DOCK6, encoding the guanidine nucleotide exchange factor DOCK6, lead to abnormal actin cytoskeleton organization and Adams-Oliver syndrome. Am J Hum Genet 89: 328-333.
79. Sierro F, Biben C, Martinez-Munoz L, Mellado M, Ransohoff RM, Li M, Woehl B, Leung H, Groom J, Batten M, et al. 2007. Disrupted cardiac development but normal hematopoiesis in mice deficient in the second CXCL12/SDF-1 receptor, CXCR7. Proc Natl Acad Sci 104: 14759-14764.
80. Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, McGuire WL. 1987. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 235: 177-182.
81. Southgate L, Machado RD, Snape KM, Primeau M, Dafou D, Ruddy DM, Branney PA, Fisher M, Lee GJ, Simpson MA, et al. 2011. Gain-of-function mutations of ARHGAP31, a Cdc42/Rac1 GTPase regulator, cause syndromic cutis aplasia and limb anomalies. Am J Hum Genet 88: 574-585.
82. Tachibana K, Hirota S, Iizasa H, Yoshida H, Kawabata K, Kataoka Y, Kitamura Y, Matsushima K, YoshidaN, Nishikawa S, et al. 1998. The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature 393: 591-594.
83. Taverna E, Huttner WB. 2010. Neural progenitor nuclei IN motion. Neuron 67: 906-914.
84. Teitelbaum SL, Ross FP. 2003. Genetic regulation of osteoclast development and function. Nat Rev Genet 4: 638-649.
85. Ursini-Siegel J, Schade B, Cardiff RD, Muller WJ. 2007. Insights from transgenic mouse models of ERBB2-induced breast cancer. Nat Rev Cancer 7: 389-397.
86. Ursini-Siegel J, Hardy WR, Zuo D, Lam SH, Sanguin-Gendreau V, Cardiff RD, Pawson T, Muller WJ. 2008. ShcA signalling is essential for tumour progression in mouse models of human breast cancer. EMBO J 27: 910-920.
87. Van Meir EG, Hadjipanayis CG, Norden AD, Shu HK, Wen PY, Olson JJ. 2010. Exciting new advances in neuro-oncology: the avenue to a cure for malignant glioma. CA Cancer J Clin 60: 166-193.
88. Vasyutina E, Martarelli B, Brakebusch C, Wende H, Birchmeier C. 2009. The small G-proteins Rac1 and Cdc42 are essential for myoblast fusion in the mouse. Proc Natl Acad Sci 106: 8935-8940.
89. Vitriol EA, Zheng JQ. 2012. Growth cone travel in space and time: the cellular ensemble of cytoskeleton, adhesion, and membrane. Neuron 73: 1068-1081.
90. Vives V, Laurin M, Cres G, Larrousse P, Morichaud Z, Noel D, Cote JF, Blangy A. 2011. The Rac1 exchange factor Dock5 is essential for bone resorption by osteoclasts. J Bone Miner Res 26: 1099-1110.
91. Watabe-Uchida M, John KA, Janas JA, Newey SE, Van Aelst L. 2006. The Rac activator DOCK7 regulates neuronal polarity through local phosphorylation of stathmin/Op18. Neuron 51: 727-739.
92. Whitley CB, Gorlin RJ. 1991. Adams-Oliver syndrome revisited. Am J Med Genet 40: 319-326.
93. Xu NJ, Henkemeyer M. 2009. Ephrin-B3 reverse signaling through Grb4 and cytoskeletal regulators mediates axon pruning. Nat Neurosci 12: 268-276.
94. Yamauchi J, Miyamoto Y, Hamasaki H, Sanbe A, Kusakawa S, Nakamura A, Tsumura H, Maeda M, Nemoto N, Kawahara K, et al. 2011. The atypical guanine-nucleotide exchange factor, dock7, negatively regulates schwann cell differentiation and myelination. J Neurosci 31: 12579-12592.
95. Yang WH, Lan HY, Huang CH, Tai SK, Tzeng CH, Kao SY, Wu KJ, Hung MC, Yang MH. 2012a. RAC1 activation mediates Twist1-induced cancer cell migration. Nat Cell Biol 14: 366-374.
96. Yang YT, Wang CL, Van Aelst L. 2012b. DOCK7 interacts with TACC3 to regulate interkinetic nuclear migration and cortical neurogenesis. Nat Neurosci 15: 1201-1210.
97. Zhou Y, Johnson JL, Cerione RA, Erickson JW. 2013. Prenylation and membrane localization of Cdc42 are essential for activation by DOCK7. Biochemistry 52: 4354-4363.