Endothelial cell migration during murine yolk sac vascular remodeling occurs by means of a Rac1 and FAK activation pathway in vivo

Developmental Dynamics

Volumn 239, Issue 10, 2010, Pages 2570-2583

  Enciso, Josephine M ^a   Konecny, Christine M ^b,c   Karpen, Heidi E ^b   Hirschi, Karen K ^b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c CENTER FOR CELL AND GENE THERAPY   (United States)

Author keywords

Endothelial cell; FAK; Focal adhesions; Migration; Paxillin; Rac1; Raldh2 mutant mice; Retinoic acid; RhoA; Vascular remodeling; Vinculin; WAVE2; Yolk sac

Indexed keywords

4 AMINO 6 [2 [[4 (DIETHYLAMINO) 1 METHYLBUTYL]AMINO] 6 METHYL 4 PYRIMIDINYL] 2 METHYLQUINOLINE; ALDEHYDE DEHYDROGENASE; BASIC FIBROBLAST GROWTH FACTOR RECEPTOR; FOCAL ADHESION KINASE; PAXILLIN; RAC1 PROTEIN; RETINALDEHYDE DEHYDROGENASE 2; RETINOIC ACID; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SONIC HEDGEHOG PROTEIN; TYROSINE; UNCLASSIFIED DRUG; VASCULOTROPIN A; VINCULIN; FOCAL ADHESION KINASE 1; PTK2 PROTEIN, MOUSE; RALDH2 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENDOTHELIUM CELL; ENZYME ACTIVATION; FOCAL ADHESION; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIUM; VASCULAR REMODELING; VASCULARIZATION; WESTERN BLOTTING; YOLK SAC; ANIMAL; ANIMAL EMBRYO; CELL CULTURE; CELL MOTION; CYTOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; GENOTYPE; IMMUNOPRECIPITATION; METABOLISM; MOUSE MUTANT; PHOSPHORYLATION; PHYSIOLOGY; POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ALDEHYDE OXIDOREDUCTASES; ANIMALS; BLOTTING, WESTERN; CELL MOVEMENT; CELLS, CULTURED; EMBRYO, MAMMALIAN; ENDOTHELIAL CELLS; FLUORESCENT ANTIBODY TECHNIQUE; FOCAL ADHESION KINASE 1; GENOTYPE; IMMUNOPRECIPITATION; MICE; MICE, KNOCKOUT; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; RAC1 GTP-BINDING PROTEIN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; VINCULIN; YOLK SAC;

EID: 79952563699     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22389     Document Type: Article

References (52)

1. Abedi H, Zachary I. 1997. Vascular endothelial growth factor stimulates tyrosine phosphorylation and recruitment to new focal adhesions of focal adhesion kinase and paxillin in endothelial cells. J Biol Chem 272:15442-15451.
2. Adams RH, Wilkinson GA, Weiss C, Diella F, Gale NW, Deutsch U, Risau W, Klein R. 1999. Roles of ephrinB ligands and EphB receptors in cardiovascular development: demarcation of arterial/ venous domains, vascular morphogenesis, and sprouting angiogenesis. Genes Dev 13:295-306.
3. Barry ST, Flinn HM, Humphries MJ, Critchley DR, Ridley AJ. 1997. Requirement for Rho in integrin signalling. Cell Adhes Commun 4:387-398.
4. Bohnsack BL, Lai L, Dolle P, Hirschi KK. 2004. Signaling hierarchy downstream of retinoic acid that independently regulates vascular remodeling and endothelial cell proliferation. Genes Dev 18: 1345-1358.
5. Byrd N, Becker S, Maye P, Narasimhaiah R, St-Jacques B, Zhang X, McMahon J, McMahon A, Grabel L. 2002. Hedgehog is required for murine yolk sac angiogenesis. Development 129:361-372.
6. Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, Fahrig M, Vandenhoeck A, Harpal K, Eberhardt C, Declercq C, Pawling J, Moons L, Collen D, Risau W, Nagy A. 1996. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380:435-439.
7. Clark EA, King WG, Brugge JS, Symons M, Hynes RO. 1998. Integrin-mediated signals regulated by members of the rho family of GTPases. J Cell Biol 142: 573-586.
8. Coll JL, Ben-Ze'ev A, Ezzell RM, Rodriguez Fernandez JL, Baribault H, Oshima RG, Adamson ED. 1995. Targeted disruption of vinculin genes in F9 and embryonic stem cells changes cell morphology, adhesion, and locomotion. Proc Natl Acad Sci USA 92:9161-9165.
9. Doetschman TA, Gossler A, Kemler R. 1987. Blastocyst-derived embryonic stem cells as a model for embryogenesis. In: Feichtingen W, Kemeter P, editors. Future aspects in human in vitro fertilization. Berlin: Springer-Verlag. p 187-195.
10. Etienne-Manneville S, Hall A. 2002. Rho GTPases in cell biology. Nature 420: 629-635.
11. Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'Shea KS, Powell-Braxton L, Hillan KJ, Moore MW. 1996. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380:439-442.
12. Gallant ND, Michael KE, Garcia AJ. 2005. Cell adhesion strengthening: contributions of adhesive area, integrin binding, and focal adhesion assembly. Mol Biol Cell 16:4329-4340.
13. Gao Y, Dickerson JB, Guo F, Zheng J, Zheng Y. 2004. Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc Natl Acad Sci USA 101:7618-7623.
14. Gerety SS, Anderson DJ. 2002. Cardiovascular ephrinB2 function is essential for embryonic angiogenesis. Development 129:1397-1410.
15. Guleria RS, Pan J, Dipette D, Singh US. 2006. Hyperglycemia inhibits retinoic acid-induced activation of Rac1, prevents differentiation of cortical neurons, and causes oxidative stress in a rat model of diabetic pregnancy. Diabetes 55:3326-3334.
16. Hagel M, George EL, Kim A, Tamimi R, Opitz SL, Turner CE, Imamoto A, Thomas SM. 2002. The adaptor protein paxillin is essential for normal development in the mouse and is a critical transducer of fibronectin signaling. Mol Cell Biol 22:901-915.
17. Hamadi A, Bouali M, Dontenwill M, Stoeckel H, Takeda K, Ronde P. 2005. Regulation of focal adhesion dynamics and disassembly by phosphorylation of FAK at tyrosine 397. J Cell Sci 118: 4415-4425.
18. Ilic D, Furuta Y, Kanazawa S, Takeda N, Sobue K, Nakatsuji N, Nomura S, Fujimoto J, Okada M, Yamamoto T. 1995. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377: 539-544.
19. Ilic D, Kovacic B, McDonagh S, Jin F, Baumbusch C, Gardner DG, Damsky CH. 2003. Focal adhesion kinase is required for blood vessel morphogenesis. Circ Res 92:300-307.
20. Ishibe S, Joly D, Zhu X, Cantley LG. 2003. Phosphorylation-dependent paxillin-ERK association mediates hepatocyte growth factor-stimulated epithelial morphogenesis. Mol Cell 12:1275-1285.
21. Ishibe S, Joly D, Liu ZX, Cantley LG. 2004. Paxillin serves as an ERK-regulated scaffold for coordinating FAK and Rac activation in epithelial morphogenesis. Mol Cell 16:257-267.
22. Krebs LT, Xue Y, Norton CR, Shutter JR, Maguire M, Sundberg JP, Gallahan D, Closson V, Kitajewski J, Callahan R, Smith GH, Stark KL, Gridley T. 2000. Notch signaling is essential for vascular morphogenesis in mice. Genes Dev 14: 1343-1352.
23. Lai L, Bohnsack BL, Niederreither K, Hirschi KK. 2003. Retinoic acid regulates endothelial cell proliferation during vasculogenesis. Development 130: 6465-6474.
24. Lamalice L, Le Boeuf F, Huot J. 2007. Endothelial cell migration during angiogenesis. Circ Res 100:782-794.
25. Li DY, Sorensen LK, Brooke BS, Urness LD, Davis EC, Taylor DG, Boak BB, Wendel DP. 1999. Defective angiogenesis in mice lacking endoglin. Science 284:1534-1537.
26. Lifschitz-Mercer B, Czernobilsky B, Feldberg E, Geiger B. 1997. Expression of the adherens junction protein vinculin in human basal and squamous cell tumors: relationship to invasiveness and metastatic potential. Hum Pathol 28:1230-1236.
27. Limbourg FP, Takeshita K, Radtke F, Bronson RT, Chin MT, Liao JK. 2005. Essential role of endothelial Notch1 in angiogenesis. Circulation 111: 1826-1832.
28. Lucitti JL, Jones EA, Huang C, Chen J, Fraser SE, Dickinson ME. 2007. Vascular remodeling of the mouse yolk sac requires hemodynamic force. Development 134:3317-3326.
29. Mills E, LaMonica K, Hong T, Pagliaruli T, Mulrooney J, Grabel L. 2005. Roles for Rho/ROCK and vinculin in parietal endoderm migration. Cell Commun Adhes 12:9-22.
30. Nath AK, Enciso J, Kuniyasu M, Hao XY, Madri JA, Pinter E. 2004. Nitric oxide modulates murine yolk sac vasculogenesis and rescues glucose induced vasculopathy. Development 131: 2485-2496.
31. Niederreither K, Subbarayan V, Dolle P, Chambon P. 1999. Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat Genet 21:444-448.
32. Nobes CD, Hall A. 1995. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81:53-62.
33. Nobes CD, Hall A. 1999. Rho GTPases control polarity, protrusion, and adhesion during cell movement. J Cell Biol 144:1235-1244.
34. Pan J, Kao YL, Joshi S, Jeetendran S, Dipette D, Singh US. 2005. Activation of Rac1 by phosphatidylinositol 3-kinase in vivo: role in activation of mitogen-activated protein kinase (MAPK) pathways and retinoic acid-induced neuronal differentiation of SH-SY5Y cells. J Neurochem 93:571-583.
35. Ren XD, Kiosses WB, Schwartz MA. 1999. Regulation of the small GTPbinding protein Rho by cell adhesion and the cytoskeleton. EMBO J 18: 578-585.
36. Ren XD, Kiosses WB, Sieg DJ, Otey CA, Schlaepfer DD, Schwartz MA. 2000. Focal adhesion kinase suppresses Rho activity to promote focal adhesion turnover. J Cell Sci 113(pt 20):3673-3678.
37. Ridley AJ, Hall A. 1992. The small GTPbinding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70:389-399.
38. Ridley AJ, Paterson HF, Johnston CL, Diekmann D, Hall A. 1992. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70:401-410.
39. Risau W, Gautschi-Sova P, Bohlen P. 1988. Endothelial cell growth factors in embryonic and adult chick brain are related to human acidic fibroblast growth factor. EMBO J 7:959-962.
40. Rodriguez Fernandez JL, Geiger B, Salomon D, Ben-Ze'ev A. 1992. Overexpression of vinculin suppresses cell motility in BALB/c 3T3 cells. Cell Motil Cytoskeleton 22:127-134.
41. Rodriguez Fernandez JL, Geiger B, Salomon D, Ben-Ze'ev A. 1993. Suppression of vinculin expression by antisense transfection confers changes in cell morphology, motility, and anchorage-dependent growth of 3T3 cells. J Cell Biol 122:1285-1294.
42. Saunders RM, Holt MR, Jennings L, Sutton DH, Barsukov IL, Bobkov A, Liddington RC, Adamson EA, Dunn GA, Critchley DR. 2006. Role of vinculin in regulating focal adhesion turnover. Eur J Cell Biol 85:487-500.
43. Sieg DJ, Hauck CR, Schlaepfer DD. 1999. Required role of focal adhesion kinase (FAK) for integrin-stimulated cell migration. J Cell Sci 112(pt 16):2677-2691.
44. Subauste MC, Pertz O, Adamson ED, Turner CE, Junger S, Hahn KM. 2004. Vinculin modulation of paxillin-FAK interactions regulates ERK to control survival and motility. J Cell Biol 165: 371-381.
45. Suri C, Jones PF, Patan S, Bartunkova S, Maisonpierre PC, Davis S, Sato TN, Yancopoulos GD. 1996. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87:1171-1180.
46. Tan W, Palmby TR, Gavard J, Amornphimoltham P, Zheng Y, Gutkind JS. 2008. An essential role for Rac1 in endothelial cell function and vascular development. FASEB J 22:1829-1838.
47. Webb DJ, Donais K, Whitmore LA, Thomas SM, Turner CE, Parsons JT, Horwitz AF. 2004. FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly. Nat Cell Biol 6:154-161.
48. Xu W, Baribault H, Adamson ED. 1998a. Vinculin knockout results in heart and brain defects during embryonic development. Development 125:327-337.
49. Xu W, Coll JL, Adamson ED. 1998b. Rescue of the mutant phenotype by reexpression of full-length vinculin in null F9 cells; effects on cell locomotion by domain deleted vinculin. J Cell Sci 111(pt 11):1535-1544.
50. Yamazaki D, Suetsugu S, Miki H, Kataoka Y, Nishikawa S, Fujiwara T, Yoshida N, Takenawa T. 2003. WAVE2 is required for directed cell migration and cardiovascular development. Nature 424:452-456.
51. Yang X, Castilla LH, Xu X, Li C, Gotay J, Weinstein M, Liu PP, Deng CX. 1999. Angiogenesis defects and mesenchymal apoptosis in mice lacking SMAD5. Development 126:1571-1580.
52. Zhao ZS, Manser E, Loo TH, Lim L. 2000. Coupling of PAK-interacting exchange factor PIX to GIT1 promotes focal complex disassembly. Mol Cell Biol 20: 6354-6363.