Phactr4: A new integrin modulator required for directional migration of enteric neural crest cells

Cell Adhesion and Migration

Volumn 6, Issue 5, 2012, Pages 419-423

  Zhang, Ying ^a   Lee, Niswander ^b  

^a UNIVERSITY OF COLORADO   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Directional migration; Enteric nervous system; Phactr4; PP1; 1 integrin

Indexed keywords

EID: 84868136242     PISSN: 19336918     EISSN: 19336926     Source Type: Journal    
DOI: 10.4161/cam.21266     Document Type: Article

References (47)

1. Heanue TA, Pachnis V. Enteric nervous system development and Hirschsprung's disease: advances in genetic and stem cell studies. Nat Rev Neurosci 2007; 8:466-79; PMID:17514199; http://dx.doi.org/10.1038/nrn2137 (Pubitemid 46789228)
2. Druckenbrod NR, Epstein ML. Behavior of enteric neural crest-derived cells varies with respect to the migratory wavefront. Dev Dyn 2007; 236:84-92; PMID:17039523; http://dx.doi.org/10.1002/dvdy.20974 (Pubitemid 46095081)
3. Young HM, Bergner AJ, Anderson RB, Enomoto H, Milbrandt J, Newgreen DF, et al. Dynamics of neural crest-derived cell migration in the embryonic mouse gut. Dev Biol 2004; 270:455-73; PMID:15183726; http://dx.doi.org/10.1016/j. ydbio.2004.03.015 (Pubitemid 38748565)
4. Young HM, Hearn CJ, Farlie PG, Canty AJ, Thomas PQ, Newgreen DF. GDNF is a chemoattractant for enteric neural cells. Dev Biol 2001; 229:503-16; PMID:11150245; http://dx.doi.org/10.1006/dbio.2000.0100 (Pubitemid 32108709)
5. Leibl MA, Ota T, Woodward MN, Kenny SE, Lloyd DA, Vaillant CR, et al. Expression of endothelin 3 by mesenchymal cells of embryonic mouse caecum. Gut 1999; 44:246-52; PMID:9895385; http://dx.doi.org/10.1136/gut.44.2.246 (Pubitemid 29119369)
6. Druckenbrod NR, Epstein ML. The pattern of neural crest advance in the cecum and colon. Dev Biol 2005; 287:125-33; PMID:16197939; http://dx.doi.org/10. 1016/j.ydbio.2005.08.040 (Pubitemid 41587483)
7. Monier-Gavelle F, Duband JL. Cross talk between adhesion molecules: control of N-cadherin activity by intracellular signals elicited by beta1 and beta3 integrins in migrating neural crest cells. J Cell Biol 1997; 137: 1663-81; PMID:9199179; http://dx.doi.org/10.1083/jcb.137.7.1663 (Pubitemid 27282245)
8. Dufour S, Beauvais-Jouneau A, Delouvée A, Thiery JP. Differential function of N-cadherin and cadherin-7 in the control of embryonic cell motility. J Cell Biol 1999; 146:501-16; PMID:10427101; http://dx.doi.org/10.1083/jcb.146. 2.501 (Pubitemid 29369784)
9. Breau MA, Dahmani A, Broders-Bondon F, Thiery JP, Dufour S. Beta1 integrins are required for the invasion of the caecum and proximal hindgut by enteric neural crest cells. Development 2009; 136:2791-801; PMID: 19633172; http://dx.doi.org/10.1242/dev.031419
10. Humphries JD, Byron A, Humphries MJ. Integrin ligands at a glance. J Cell Sci 2006; 119:3901-3; PMID:16988024; http://dx.doi.org/10.1242/jcs.03098 (Pubitemid 44650863)
11. Hynes RO. Integrins: bidirectional, allosteric signaling machines. Cell 2002; 110:673-87; PMID:12297042; http://dx.doi.org/10.1016/S0092-8674(02)00971-6 (Pubitemid 35283958)
12. Fässler R, Meyer M. Consequences of lack of beta 1 integrin gene expression in mice. Genes Dev 1995; 9: 1896-908; PMID:7544313; http://dx.doi.org/10.1101/gad.9.15.1896
13. Stephens LE, Sutherland AE, Klimanskaya IV, Andrieux A, Meneses J, Pedersen RA, et al. Deletion of beta 1 integrins in mice results in inner cell mass failure and peri-implantation lethality. Genes Dev 1995; 9:1883-95; PMID:7544312; http://dx.doi.org/10.1101/gad.9.15.1883
14. Pietri T, Eder O, Breau MA, Topilko P, Blanche M, Brakebusch C, et al. Conditional beta1-integrin gene deletion in neural crest cells causes severe developmental alterations of the peripheral nervous system. Development 2004; 131:3871-83; PMID:15253938; http://dx.doi.org/10.1242/dev.01264 (Pubitemid 39232148)
15. Breau MA, Pietri T, Eder O, Blanche M, Brakebusch C, Fässler R, et al. Lack of beta1 integrins in enteric neural crest cells leads to a Hirschsprung-like pheno-type. Development 2006; 133:1725-34; PMID: 16571628; http://dx.doi.org/10.1242/dev.02346 (Pubitemid 43810979)
16. Zhang Y, Kim TH, Niswander L. Phactr4 regulates directional migration of enteric neural crest through PP1, integrin signaling, and cofilin activity. Genes Dev 2012; 26:69-81; PMID:22215812; http://dx.doi.org/10.1101/gad.179283. 111
17. Allen PB, Greenfield AT, Svenningsson P, Haspeslagh DC, Greengard P. Phactrs 1-4: A family of protein phosphatase 1 and actin regulatory proteins. Proc Natl Acad Sci U S A 2004; 101:7187-92; PMID:15107502; http://dx.doi.org/10. 1073/pnas.0401673101 (Pubitemid 38596464)
18. Miralles F, Posern G, Zaromytidou AI, Treisman R. Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell 2003; 113:329-42; PMID: 12732141; http://dx.doi.org/10.1016/S0092-8674(03)00278-2 (Pubitemid 36556115)
19. Sagara J, Arata T, Taniguchi S. Scapinin, the protein phosphatase 1 binding protein, enhances cell spreading and motility by interacting with the actin cytoskeleton. PLoS One 2009; 4:e4247; PMID:19158953; http://dx.doi.org/10. 1371/journal.pone.0004247
20. Guettler S, Vartiainen MK, Miralles F, Larijani B, Treisman R. RPEL motifs link the serum response factor cofactor MAL but not myocardin to Rho signaling via actin binding. Mol Cell Biol 2008; 28: 732-42; PMID:18025109; http://dx.doi.org/10.1128/MCB.01623-07
21. Kim TH, Goodman J, Anderson KV, Niswander L. Phactr4 regulates neural tube and optic fissure closure by controlling PP1-, Rb-, and E2F1-regulated cell-cycle progression. Dev Cell 2007; 13:87-102; PMID: 17609112; http://dx.doi.org/10.1016/j.devcel.2007.04.018 (Pubitemid 46991577)
22. Favot L, Gillingwater M, Scott C, Kemp PR. Overexpression of a family of RPEL proteins modifies cell shape. FEBS Lett 2005; 579:100-4; PMID: 15620697; http://dx.doi.org/10.1016/j.febslet.2004.11.054 (Pubitemid 40023380)
23. Cohen PT. Protein phosphatase 1-targeted in many directions. J Cell Sci 2002; 115:241-56; PMID: 11839776 (Pubitemid 34145174)
24. Oliver CJ, Terry-Lorenzo RT, Elliott E, Bloomer WA, Li S, Brautigan DL, et al. Targeting protein phospha-tase 1 (PP1) to the actin cytoskeleton: the neurabin I/ PP1 complex regulates cell morphology. Mol Cell Biol 2002; 22:4690-701; PMID:12052877; http://dx.doi.org/10.1128/MCB.22.13.4690-4701.2002 (Pubitemid 34620405)
25. Fernandez A, Brautigan DL, Mumby M, Lamb NJ. Protein phosphatase type-1, not type-2A, modulates actin microfilament integrity and myosin light chain phosphorylation in living nonmuscle cells. J Cell Biol 1990; 111:103-12; PMID:2164027; http://dx.doi.org/10.1083/jcb.111.1.103 (Pubitemid 20202620)
26. Shi Y. Serine/threonine phosphatases: mechanism through structure. Cell 2009; 139:468-84; PMID: 19879837; http://dx.doi.org/10.1016/j.cell.2009.10.006
27. Virshup DM, Shenolikar S. From promiscuity to precision: protein phosphatases get a makeover. Mol Cell 2009; 33:537-45; PMID:19285938; http://dx.doi.org/10.1016/j.molcel.2009.02.015
28. Lauffenburger DA, Horwitz AF. Cell migration: a physically integrated molecular process. Cell 1996; 84: 359-69; PMID:8608589; http://dx.doi.org/10. 1016/S0092-8674(00)81280-5 (Pubitemid 26058561)
29. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, et al. Cell migration: integrating signals from front to back. Science 2003; 302:1704-9; PMID:14657486; http://dx.doi.org/10.1126/science.1092053 (Pubitemid 37505725)
30. 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
31. Woods AJ, White DP, Caswell PT, Norman JC. PKD1/PKCmu promotes alphavbeta3 integrin recycling and delivery to nascent focal adhesions. EMBO J 2004; 23:2531-43; PMID:15192707; http://dx.doi.org/10.1038/sj.emboj.7600267 (Pubitemid 38988225)
32. Roberts M, Barry S, Woods A, van der Sluijs P, Norman J. PDGF-regulated rab4-dependent recycling of alphavbeta3 integrin from early endosomes is necessary for cell adhesion and spreading. Curr Biol 2001; 11:1392-402; PMID:11566097; http://dx.doi.org/10.1016/S0960-9822(01)00442-0 (Pubitemid 32863188)
33. White DP, Caswell PT, Norman JC. alpha v beta3 and alpha5beta1 integrin recycling pathways dictate downstream Rho kinase signaling to regulate persistent cell migration. J Cell Biol 2007; 177:515-25; PMID: 17485491; http://dx.doi.org/10.1083/jcb.200609004 (Pubitemid 46718279)
34. Danen EH, van Rheenen J, Franken W, Huveneers S, Sonneveld P, Jalink K, et al. Integrins control motile strategy through a Rho-cofilin pathway. J Cell Biol 2005; 169:515-26; PMID:15866889; http://dx.doi.org/10.1083/jcb.200412081 (Pubitemid 40686701)
35. Nishimura T, Kaibuchi K. Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3. Dev Cell 2007; 13:15-28; PMID: 17609107; http://dx.doi.org/10.1016/j.devcel.2007.05.003 (Pubitemid 46972036)
36. Mishima A, Suzuki A, Enaka M, Hirose T, Mizuno K, Ohnishi T, et al. Over-expression of PAR-3 suppresses contact-mediated inhibition of cell migration in MDCK cells. Genes Cells 2002; 7:581-96; PMID: 12059961; http://dx.doi.org/10.1046/j.1365-2443.2002.00540.x (Pubitemid 34679055)
37. Traweger A, Wiggin G, Taylor L, Tate SA, Metalnikov P, Pawson T. Protein phosphatase 1 regulates the phosphorylation state of the polarity scaffold Par-3. Proc Natl Acad Sci U S A 2008; 105:10402-7; PMID: 18641122; http://dx.doi.org/10.1073/pnas.0804102105
38. Bharucha JP, Larson JR, Konopka JB, Tatchell K. Saccharomyces cerevisiae Afr1 protein is a protein phosphatase 1/Glc7-targeting subunit that regulates the septin cytoskeleton during mating. Eukaryot Cell 2008; 7:1246-55; PMID:18552279; http://dx.doi.org/10.1128/EC.00024-08
39. Konopka JB, DeMattei C, Davis C. AFR1 promotes polarized apical morphogenesis in Saccharomyces cerevisiae. Mol Cell Biol 1995; 15:723-30; PMID: 7823940
40. Tong AH, Drees B, Nardelli G, Bader GD, Brannetti B, Castagnoli L, et al. A combined experimental and computational strategy to define protein interaction networks for peptide recognition modules. Science 2002; 295:321-4; PMID:11743162; http://dx.doi.org/10.1126/science.1064987 (Pubitemid 34074361)
41. Tonikian R, Xin X, Toret CP, Gfeller D, Landgraf C, Panni S, et al. Bayesian modeling of the yeast SH3 domain interactome predicts spatiotemporal dynamics of endocytosis proteins. PLoS Biol 2009; 7:e1000218; PMID:19841731; http://dx.doi.org/10.1371/journal.pbio.1000218
42. Bender L, Lo HS, Lee H, Kokojan V, Peterson V, Bender A. Associations among PH and SH3 domain-containing proteins and Rho-type GTPases in Yeast. J Cell Biol 1996; 133:879-94; PMID:8666672; http://dx.doi.org/10.1083/jcb.133.4. 879 (Pubitemid 26160988)
43. Petrie RJ, Doyle AD, Yamada KM. Random versus directionally persistent cell migration. Nat Rev Mol Cell Biol 2009; 10:538-49; PMID:19603038; http://dx.doi.org/10.1038/nrm2729
44. Haugh JM, Codazzi F, Teruel M, Meyer T. Spatial sensing in fibroblasts mediated by 3' phosphoinositides. J Cell Biol 2000; 151:1269-80; PMID:11121441; http://dx.doi.org/10.1083/jcb.151.6.1269
45. Mouilleron S, Guettler S, Langer CA, Treisman R, McDonald NQ. Molecular basis for G-actin binding to RPEL motifs from the serum response factor coacti-vator MAL. EMBO J 2008; 27:3198-208; PMID: 19008859; http://dx.doi.org/ 10.1038/emboj.2008.235
46. Olson EN, Nordheim A. Linking actin dynamics and gene transcription to drive cellular motile functions. Nat Rev Mol Cell Biol 2010; 11:353-65; PMID: 20414257; http://dx.doi.org/10.1038/nrm2890
47. Posern G, Sotiropoulos A, Treisman R. Mutant actins demonstrate a role for unpolymerized actin in control of transcription by serum response factor. Mol Biol Cell 2002; 13:4167-78; PMID:12475943; http://dx.doi.org/10.1091/mbc.02- 05-0068 (Pubitemid 35471176)