Requisite role for Nck adaptors in cardiovascular development, endothelial-to-mesenchymal transition, and directed cell migration

Molecular and Cellular Biology

Volumn 35, Issue 9, 2015, Pages 1573-1587

  Clouthier, Derek L ^a   Harris, Cameron N ^a   Harris, Richard A ^a   Martin, Claire E ^a   Puri, Mira C ^b   Jones, Nina ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b MOUNT SINAI HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOPOIETIN 1; ANGIOPOIETIN RECEPTOR; CALVASCULIN; CLAUDIN 5; CRE RECOMBINASE; MOLECULAR MARKER; NCK PROTEIN; NCK1 PROTEIN; NCK2 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2; ONCOPROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOPHOSPHORYLATION; CELL ADHESION; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CELL SPREADING; CELL TRANSFORMATION; CONTROLLED STUDY; EMBRYO; ENDOCARDIAL CUSHION; ENDOTHELIAL TO MESENCHYMAL TRANSITION; FEMALE; FOCAL ADHESION; GENE DELETION; HEART DEVELOPMENT; HEART VALVE; LOXP SITE; MALE; MORPHOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; CARDIOVASCULAR MALFORMATION; CARDIOVASCULAR SYSTEM; CELL MOTION; CYTOLOGY; EMBRYOLOGY; ENDOTHELIUM CELL; EPITHELIAL MESENCHYMAL TRANSITION; GENETICS; METABOLISM; TRANSGENIC MOUSE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CARDIOVASCULAR ABNORMALITIES; CARDIOVASCULAR SYSTEM; CELL MOVEMENT; ENDOTHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; GENE DELETION; MICE; MICE, TRANSGENIC; ONCOGENE PROTEINS;

EID: 84929167918     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00072-15     Document Type: Article

References (55)

1. Carmeliet P. 2003. Blood vessels and nerves: common signals, pathways and diseases. Nat Rev Genet 4:710-720. http://dx.doi.org/10.1038/nrg1158.
2. Carmeliet P. 2000. Mechanisms of angiogenesis and arteriogenesis. Nat Med 6:389-395. http://dx.doi.org/10.1038/74651.
3. Armulik A, Abramsson A, Betsholtz C. 2005. Endothelial/pericyte interactions. Circ Res 97:512-523. http://dx.doi.org/10.1161/01.RES.0000182903.16652.d7.
4. Srivastava D, Olson EN. 2000. A genetic blueprint for cardiac development. Nature 407:221-226. http://dx.doi.org/10.1038/35025190.
5. Adams RH, Alitalo K. 2007. Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol 8:464-478. http://dx.doi.org/10.1038/nrm2183.
6. Jones N, Iljin K, Dumont DJ, Alitalo K. 2001. Tie receptors: new modulators of angiogenic and lymphangiogenic responses. Nat Rev Mol Cell Biol 2:257-267. http://dx.doi.org/10.1038/35067005.
7. Lamalice L, Le Boeuf F, Huot J. 2007. Endothelial cell migration during angiogenesis. Circ Res 100:782-794. http://dx.doi.org/10.1161/01.RES.0000259593.07661.1e.
8. Pawson T. 2004. Specificity in signal transduction: from phosphotyrosine-SH2domain interactions to complex cellular systems. Cell 116:191-203. http://dx.doi.org/10.1016/S0092-8674(03)01077-8.
9. Jones N, Blasutig IM, Eremina V, Ruston JM, Bladt F, Li H, Huang H, Larose L, Li SS, Takano T, Quaggin SE, Pawson T. 2006. Nck adaptor proteins link nephrin to the actin cytoskeleton of kidney podocytes. Nature 440:818-823. http://dx.doi.org/10.1038/nature04662.
10. Fawcett JP, Georgiou J, Ruston J, Bladt F, Sherman A, Warner N, Saab BJ, Scott R, Roder JC, Pawson T. 2007. Nck adaptor proteins control the organization of neuronal circuits important for walking. Proc Natl Acad Sci U S A 104:20973-20978. http://dx.doi.org/10.1073/pnas.0710316105.
11. Li W, Fan J, Woodley DT. 2001. Nck/Dock: an adapter between cell surface receptors and the actin cytoskeleton. Oncogene 20:6403-6417. http://dx.doi.org/10.1038/sj.onc.1204782.
12. Buday L, Wunderlich L, Tamas P. 2002. The Nck family of adapter proteins: regulators of actin cytoskeleton. Cell Signal 14:723-731. http://dx.doi.org/10.1016/S0898-6568(02)00027-X.
13. Tu Y, Li F, Goicoechea S, Wu C. 1999. The LIM-only protein PINCH directly interacts with integrin-linked kinase and is recruited to integrinrich sites in spreading cells. Mol Cell Biol 19:2425-2434.
14. Goicoechea SM, Tu Y, Hua Y, Chen K, Shen TL, Guan JL, Wu C. 2002. Nck-2 interacts with focal adhesion kinase and modulates cell motility. Int J Biochem Cell Biol 34:791-805. http://dx.doi.org/10.1016/S1357-2725 (02)00002-X.
15. Eden S, Rohatgi R, Podtelejnikov AV, Mann M, Kirschner MW. 2002. Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck. Nature 418:790-793. http://dx.doi.org/10.1038/nature00859.
16. Higgs HN, Pollard TD. 1999. Regulation of actin polymerization by Arp2/3 complex and WASp/Scar proteins. J Biol Chem 274:32531-32534. http://dx.doi.org/10.1074/jbc.274.46.32531.
17. Rohatgi R, Nollau P, Ho HY, Kirschner MW, Mayer BJ. 2001. Nck and phosphatidylinositol 4,5-bisphosphate synergistically activate actin polymerization through the N-WASP-Arp2/3 pathway. J Biol Chem 276: 26448-26452. http://dx.doi.org/10.1074/jbc. M103856200.
18. Igarashi K, Isohara T, Kato T, Shigeta K, Yamano T, Uno I. 1998. Tyrosine 1213 of Flt-1 is a major binding site of Nck and SHP-2. Biochem Biophys Res Commun 246:95-99. http://dx.doi.org/10.1006/bbrc.1998.8578.
19. Stoletov KV, Ratcliffe KE, Spring SC, Terman BI. 2001. NCK and PAK participate in the signaling pathway by which vascular endothelial growth factor stimulates the assembly of focal adhesions. J Biol Chem 276:22748-22755. http://dx.doi.org/10.1074/jbc. M009720200.
20. Lamalice L, Houle F, Huot J. 2006. Phosphorylation of Tyr1214 within VEGFR-2 triggers the recruitment of Nck and activation of Fyn leading to SAPK2/p38 activation and endothelial cell migration in response to VEGF. J Biol Chem 281:34009-34020. http://dx.doi.org/10.1074/jbc. M603928200.
21. Jones N, Dumont DJ. 1998. The Tek/Tie2 receptor signals through a novel Dok-related docking protein, Dok-R. Oncogene 17:1097-1108. http://dx.doi.org/10.1038/sj.onc.1202115.
22. Master Z, Jones N, Tran J, Jones J, Kerbel RS, Dumont DJ. 2001. Dok-R plays a pivotal role in angiopoietin-1-dependent cell migration through recruitment and activation of Pak. EMBO J 20:5919-5928. http://dx.doi.org/10.1093/emboj/20.21.5919.
23. Braren R, Hu H, Kim YH, Beggs HE, Reichardt LF, Wang R. 2006. Endothelial FAK is essential for vascular network stability, cell survival, and lamellipodial formation. J Cell Biol 172:151-162. http://dx.doi.org/10.1083/jcb.200506184.
24. Friedrich EB, Liu E, Sinha S, Cook S, Milstone DS, MacRae CA, Mariotti M, Kuhlencordt PJ, Force T, Rosenzweig A, St-Arnaud R, Dedhar S, Gerszten RE. 2004. Integrin-linked kinase regulates endothelial cell survival and vascular development. Mol Cell Biol 24:8134-8144. http://dx.doi.org/10.1128/MCB.24.18.8134-8144.2004.
25. 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. http://dx.doi.org/10.1038/nature01770.
26. Bladt F, Aippersbach E, Gelkop S, Strasser GA, Nash P, Tafuri A, Gertler FB, Pawson T. 2003. The murine Nck SH2/SH3 adaptors are important for the development of mesoderm-derived embryonic structures and for regulating the cellular actin network. Mol Cell Biol 23:4586-4597. http://dx.doi.org/10.1128/MCB.23.13.4586-4597.2003.
27. Nomura-Kitabayashi A, Anderson GA, Sleep G, Mena J, Karabegovic A, Karamath S, Letarte M, Puri MC. 2009. Endoglin is dispensable for angiogenesis, but required for endocardial cushion formation in the midgestation mouse embryo. Dev Biol 335:66-77. http://dx.doi.org/10.1016/j.ydbio.2009.08.016.
28. Camenisch TD, Molin DG, Person A, Runyan RB, Gittenberger-de Groot AC, McDonald JA, Klewer SE. 2002. Temporal and distinct TGFbeta ligand requirements during mouse and avian endocardial cushion morphogenesis. Dev Biol 248:170-181. http://dx.doi.org/10.1006/dbio.2002.0731.
29. Cattelino A, Liebner S, Gallini R, Zanetti A, Balconi G, Corsi A, Bianco P, Wolburg H, Moore R, Oreda B, Kemler R, Dejana E. 2003. The conditional inactivation of the beta-catenin gene in endothelial cells causes a defective vascular pattern and increased vascular fragility. J Cell Biol 162:1111-1122. http://dx.doi.org/10.1083/jcb.200212157.
30. Peng X, Ueda H, Zhou H, Stokol T, Shen TL, Alcaraz A, Nagy T, Vassalli JD, Guan JL. 2004. Overexpression of focal adhesion kinase in vascular endothelial cells promotes angiogenesis in transgenic mice. Cardiovasc Res 64: 421-430. http://dx.doi.org/10.1016/j.cardiores.2004.07.012.
31. Hawley SP, Wills MK, Jones N. 2010. Adenovirus-mediated genetic removal of signaling molecules in cultured primary mouse embryonic fibroblasts. J Vis Exp 2010:2160. http://dx.doi.org/10.3791/2160.
32. Latreille M, Laberge MK, Bourret G, Yamani L, Larose L. 2011. Deletion of Nck1 attenuates hepatic ER stress signaling and improves glucose tolerance and insulin signaling in liver of obese mice. Am J Physiol Endocrinol Metab 300:E423-E434. http://dx.doi.org/10.1152/ajpendo.00088.2010.
33. Shen TL, Park AY, Alcaraz A, Peng X, Jang I, Koni P, Flavell RA, Gu H, Guan JL. 2005. Conditional knockout of focal adhesion kinase in endothelial cells reveals its role in angiogenesis and vascular development in late embryogenesis. J Cell Biol 169:941-952. http://dx.doi.org/10.1083/jcb.200411155.
34. de Lange WJ, Halabi CM, Beyer AM, Sigmund CD. 2008. Germ line activation of the Tie2 and SMMHC promoters causes noncell-specific deletion of floxed alleles. Physiol Genomics 35:1-4. http://dx.doi.org/10.1152/physiolgenomics.90284.2008.
35. Majesky MW, Dong XR, Regan JN, Hoglund VJ. 2011. Vascular smooth muscle progenitor cells: building and repairing blood vessels. Circ Res 108:365-377. http://dx.doi.org/10.1161/CIRCRESAHA.110.223800.
36. Armstrong EJ, Bischoff J. 2004. Heart valve development: endothelial cell signaling and differentiation. Circ Res 95:459-470. http://dx.doi.org/10.1161/01.RES.0000141146.95728.da.
37. Potenta S, Zeisberg E, Kalluri R. 2008. The role of endothelial-tomesenchymal transition in cancer progression. Br J Cancer 99:1375-1379. http://dx.doi.org/10.1038/sj.bjc.6604662.
38. Huveneers S, Danen EH. 2009. Adhesion signaling- crosstalk between integrins, Src and Rho. J Cell Sci 122:1059-1069. http://dx.doi.org/10.1242/jcs.039446.
39. Dumont DJ, Gradwohl G, Fong GH, Puri MC, Gertsenstein M, Auerbach A, Breitman ML. 1994. Dominant-negative and targeted null mutations in the endothelial receptor tyrosine kinase, tek, reveal a critical role in vasculogenesis of the embryo. Genes Dev 8:1897-1909. http://dx.doi.org/10.1101/gad.8.16.1897.
40. 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. http://dx.doi.org/10.1016/S0092-8674(00)81813-9.
41. Tachibana K, Jones N, Dumont DJ, Puri MC, Bernstein A. 2005. Selective role of a distinct tyrosine residue on Tie2 in heart development and early hematopoiesis. Mol Cell Biol 25:4693-4702. http://dx.doi.org/10.1128/MCB.25.11.4693-4702.2005.
42. Patan S. 1998. TIE1 and TIE2 receptor tyrosine kinases inversely regulate embryonic angiogenesis by the mechanism of intussusceptive microvascular growth. Microvasc Res 56:1-21. http://dx.doi.org/10.1006/mvre.1998.2081.
43. 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. http://dx.doi.org/10.1242/dev.02883.
44. Li XY, Zhou X, Rowe RG, Hu Y, Schlaepfer DD, Ilic D, Dressler G, Park A, Guan JL, Weiss SJ. 2011. Snail1 controls epithelial-mesenchymal lineage commitment in focal adhesion kinase-null embryonic cells. J Cell Biol 195:729-738. http://dx.doi.org/10.1083/jcb.201105103.
45. Yang Z, Rayala S, Nguyen D, Vadlamudi RK, Chen S, Kumar R. 2005. Pak1 phosphorylation of snail, a master regulator of epithelial-tomesenchyme transition, modulates snail's subcellular localization and functions. Cancer Res 65:3179-3184. http://dx.doi.org/10.1158/0008-5472.CAN-04-3480.
46. Ruusala A, Pawson T, Heldin CH, Aspenstrom P. 2008. Nck adapters are involved in the formation of dorsal ruffles, cell migration, and Rho signaling downstream of the platelet-derived growth factor beta receptor. J Biol Chem 283:30034-30044. http://dx.doi.org/10.1074/jbc. M800913200.
47. Guan S, Fan J, Han A, Chen M, Woodley DT, Li W. 2009. Noncompensating roles between Nckalpha and Nckbeta in PDGF-BB signaling to promote human dermal fibroblast migration. J Invest Dermatol 129:1909-1920. http://dx.doi.org/10.1038/jid.2008.457.
48. Mihira H, Suzuki HI, Akatsu Y, Yoshimatsu Y, Igarashi T, Miyazono K, Watabe T. 2012. TGF-beta-induced mesenchymal transition of MS-1 endothelial cells requires Smad-dependent cooperative activation of Rho signals and MRTF-A. J Biochem 151:145-156. http://dx.doi.org/10.1093/jb/mvr121.
49. Shen W, Li S, Chung SH, Zhu L, Stayt J, Su T, Couraud PO, Romero IA, Weksler B, Gillies MC. 2011. Tyrosine phosphorylation of VEcadherin and claudin-5 is associated with TGF-beta1-induced permeability of centrally derived vascular endothelium. Eur J Cell Biol 90:323-332. http://dx.doi.org/10.1016/j.ejcb.2010.10.013.
50. Mammoto T, Parikh SM, Mammoto A, Gallagher D, Chan B, Mostoslavsky G, Ingber DE, Sukhatme VP. 2007. Angiopoietin-1 requires p190 RhoGAP to protect against vascular leakage in vivo. J Biol Chem 282: 23910-23918. http://dx.doi.org/10.1074/jbc. M702169200.
51. Lampugnani MG, Zanetti A, Breviario F, Balconi G, Orsenigo F, Corada M, Spagnuolo R, Betson M, Braga V, Dejana E. 2002. VE-cadherin regulates endothelial actin activating Rac and increasing membrane association of Tiam. Mol Biol Cell 13:1175-1189. http://dx.doi.org/10.1091/mbc.01-07-0368.
52. Pelletier S, Duhamel F, Coulombe P, Popoff MR, Meloche S. 2003. Rho family GTPases are required for activation of Jak/STAT signaling by G protein-coupled receptors. Mol Cell Biol 23:1316-1333. http://dx.doi.org/10.1128/MCB.23.4.1316-1333.2003.
53. Liu S, Li L, Zhang Y, Zhang Y, Zhao Y, You X, Lin Z, Zhang X, Ye L. 2012. The oncoprotein HBXIP uses two pathways to up-regulate S100A4 in promotion of growth and migration of breast cancer cells. J Biol Chem 287:30228-30239. http://dx.doi.org/10.1074/jbc. M112.343947.
54. Chaki SP, Barhoumi R, Berginski ME, Sreenivasappa H, Trache A, Gomez SM, Rivera GM. 2013. Nck enables directional cell migration through the coordination of polarized membrane protrusion with adhesion dynamics. J Cell Sci 126:1637-1649. http://dx.doi.org/10.1242/jcs.119610.
55. Gerhardt H, Golding M, Fruttiger M, Ruhrberg C, Lundkvist A, Abramsson A, Jeltsch M, Mitchell C, Alitalo K, Shima D, Betsholtz C. 2003. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol 161:1163-1177. http://dx.doi.org/10.1083/jcb.200302047.