Phactr4 regulates directional migration of enteric neural crest through PP1, integrin signaling, and cofilin activity

Genes and Development

Volumn 26, Issue 1, 2012, Pages 69-81

  Zhang, Ying ^a   Kim, Tae Hee ^a,b   Niswander, Lee ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

1 integrin; Cofilin; Directional cell migration; Enteric neural crest cell; Hirschsprung disease; Phactr4; PP1

Indexed keywords

BETA1 INTEGRIN; COFILIN; INTEGRIN; PHOSPHOPROTEIN PHOSPHATASE 1; PROTEIN PHACTR4; REGULATOR PROTEIN; RHO FACTOR; RHO KINASE; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL SPECIFICITY; CYTOSKELETON; ENTERIC NEURAL CREST CELL; ENZYME ACTIVITY; GENE DISRUPTION; GENE MUTATION; HIRSCHSPRUNG DISEASE; LAMELLIPODIUM; MOUSE; NEURAL CREST CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TIME LAPSE IMAGING;

ACTIN DEPOLYMERIZING FACTORS; ANIMALS; CELL MOVEMENT; CELLS, CULTURED; ENTERIC NERVOUS SYSTEM; GASTROINTESTINAL TRACT; INTEGRINS; MICE; NEURAL CREST; NUCLEAR PROTEINS; PROTEIN PHOSPHATASE 1; SIGNAL TRANSDUCTION;

MUS;

EID: 84855303522     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.179283.111     Document Type: Article

References (45)

1. Abbondanzo SJ, Gadi I, Stewart CL. 1993. Derivation of embryonic stem cell lines. Methods Enzymol 225: 803-823.
2. Allen PB, Greenfield AT, Svenningsson P, Haspeslagh DC, Greengard P. 2004. Phactrs 1-4: A family of protein phosphatase 1 and actin regulatory proteins. Proc Natl Acad Sci 101: 7187-7192.
3. Ambach A, Saunus J, Konstandin M, Wesselborg S, Meuer SC, Samstag Y. 2000. The serine phosphatases PP1 and PP2A associate with and activate the actin-binding protein cofilin in human T lymphocytes. Eur J Immunol 30: 3422-3431.
4. Amiel J, Sproat-Emison E, Garcia-Barcelo M, Lantieri F, Burzynski G, Borrego S, Pelet A, Arnold S, Miao X, Griseri P, et al. 2008. Hirschsprung disease, associated syndromes and genetics: A review. J Med Genet 45: 1-14.
5. Anderson RB. 2010. Matrix metalloproteinase-2 is involved in the migration and network formation of enteric neural crestderived cells. Int J Dev Biol 54: 63-69.
6. Anderson RB, Turner KN, Nikonenko AG, Hemperly J, Schachner M, Young HM. 2006. The cell adhesion molecule L1 is required for chain migration of neural crest cells in the developing mouse gut. Gastroenterology 130: 1221-1232.
7. Arber S, Barbayannis FA, Hanser H, Schneider C, Stanyon CA, Bernard O, Caroni P. 1998. Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature 393: 805-809.
8. Asai N, Fukuda T, Wu ZQ, Enomoto A, Pachnis V, Takahashi M, Costantini F. 2006. Targeted mutation of serine 697 in the Ret tyrosine kinase causes migration defect of enteric neural crest cells. Development 133: 4507-4516.
9. Bernstein BW, Bamburg JR. 2010. ADF/cofilin: A functional node in cell biology. Trends Cell Biol 20: 187-195.
10. Bharucha JP, Larson JR, Konopka JB, Tatchell K. 2008. Saccharomyces cerevisiae Afr1 protein is a protein phosphatase 1/ Glc7-targeting subunit that regulates the septin cytoskeleton during mating. Eukaryot Cell 7: 1246-1255.
11. Breau MA, Pietri T, Eder O, Blanche M, Brakebusch C, Fassler R, Thiery JP, Dufour S. 2006. Lack of b1 integrins in enteric neural crest cells leads to a Hirschsprung-like phenotype. Development 133: 1725-1734.
12. Breau MA, Dahmani A, Broders-Bondon F, Thiery JP, Dufour S. 2009. β1 integrins are required for the invasion of the caecum and proximal hindgut by enteric neural crest cells. Development 136: 2791-2801.
13. Danen EH, van Rheenen J, Franken W, Huveneers S, Sonneveld P, Jalink K, Sonnenberg A. 2005. Integrins control motile strategy through a Rho-cofilin pathway. J Cell Biol 169: 515-526.
14. Dawe HR, Minamide LS, Bamburg JR, Cramer LP. 2003. ADF/ cofilin controls cell polarity during fibroblast migration. Curr Biol 13: 252-257.
15. Druckenbrod NR, Epstein ML. 2005. The pattern of neural crest advance in the cecum and colon. Dev Biol 287: 125-133.
16. Enomoto H, Crawford PA, Gorodinsky A, Heuckeroth RO, Johnson EM, Milbrandt J. 2001. RET signaling is essential for migration, axonal growth and axon guidance of developing sympathetic neurons. Development 128: 3963-3974.
17. Etienne-Manneville S, Hall A. 2001. Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta. Cell 106: 489-498.
18. Favot L, Gillingwater M, Scott C, Kemp PR. 2005. Overexpression of a family of RPEL proteins modifies cell shape. FEBS Lett 579: 100-104.
19. Geiger B, Bershadsky A, Pankov R, Yamada KM. 2001. Transmembrane crosstalk between the extracellular matrix-cytoskeleton crosstalk. Nat Rev Mol Cell Biol 2: 793-805.
20. Ghosh M, Song X, Mouneimne G, Sidani M, Lawrence DS, Condeelis JS. 2004. Cofilin promotes actin polymerization and defines the direction of cell motility. Science 304: 743-746.
21. Heanue TA, Pachnis V. 2007. Enteric nervous system development and Hirschsprung's disease: Advances in genetic and stem cell studies. Nat Rev Neurosci 8: 466-479.
22. Hearn CJ, Young HM, Ciampoli D, Lomax AE, Newgreen D. 1999. Catenary cultures of embryonic gastrointestinal tract support organ morphogenesis, motility, neural crest cell migration, and cell differentiation. Dev Dyn 214: 239-247.
23. Kim TH, Goodman J, Anderson KV, Niswander L. 2007. Phactr4 regulates neural tube and optic fissure closure by controlling PP1-, Rb-, and E2F1-regulated cell-cycle progression. Dev Cell 13: 87-102.
24. Lange A, Wickstrom SA, Jakobson M, Zent R, Sainio K, Fassler R. 2009. Integrin-linked kinase is an adaptor with essential functions during mouse development. Nature 461: 1002-1006.
25. Larsen M, Tremblay ML, Yamada KM. 2003. Phosphatases in cell-matrix adhesion and migration. Nat Rev Mol Cell Biol 4: 700-711.
26. Legate KR, Wickstrom SA, Fassler R. 2009. Genetic and cell biological analysis of integrin outside-in signaling. Genes Dev 23: 397-418.
27. Maekawa M, Ishizaki T, Boku S, Watanabe N, Fujita A, Iwamatsu A, Obinata T, Ohashi K, Mizuno K, Narumiya S. 1999. Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science 285: 895-898.
28. McCallion AS, Emison ES, Kashuk CS, Bush RT, Kenton M, Carrasquillo MM, Jones KW, Kennedy GC, Portnoy ME, Green ED, et al. 2003. Genomic variation in multigenic traits: Hirschsprung disease. Cold Spring Harb Symp Quant Biol 68: 373-381.
29. Montanez E, Wickstrom SA, Altstatter J, Chu H, Fassler R. 2009. α-Parvin controls vascular mural cell recruitment to vessel wall by regulating RhoA/ROCK signalling. EMBO J 28: 3132-3144.
30. Mouneimne G, Soon L, DesMarais V, Sidani M, Song X, Yip SC, Ghosh M, Eddy R, Backer JM, Condeelis J. 2004. Phospholipase C and cofilin are required for carcinoma cell directionality in response to EGF stimulation. J Cell Biol 166: 697-708.
31. Newgreen DF, Minichiello J. 1995. Control of epitheliomesenchymal transformation. I. Events in the onset of neural crest cell migration are separable and inducible by protein kinase inhibitors. Dev Biol 170: 91-101.
32. Nishimura T, Kaibuchi K. 2007. Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3. Dev Cell 13: 15-28.
33. Okamura Y, Saga Y. 2008. Notch signaling is required for the maintenance of enteric neural crest progenitors. Development 135: 3555-3565.
34. Oleinik NV, Krupenko NI, Krupenko SA. 2010. ALDH1L1 inhibits cell motility via dephosphorylation of cofilin by PP1 and PP2A. Oncogene 29: 6233-6244.
35. Paavilainen VO, Bertling E, Falck S, Lappalainen P. 2004. Regulation of cytoskeletal dynamics by actin-monomerbinding proteins. Trends Cell Biol 14: 386-394.
36. Petrie RJ, Doyle AD, Yamada KM. 2009. Random versus directionally persistent cell migration. Nat Rev Mol Cell Biol 10: 538-549.
37. Riedl J, Crevenna AH, Kessenbrock K, Yu JH, Neukirchen D, Bista M, Bradke F, Jenne D, Holak TA, Werb Z, et al. 2008. Lifeact: A versatile marker to visualize F-actin. Nat Methods 5: 605-607.
38. Sagara J, Arata T, Taniguchi S. 2009. Scapinin, the protein phosphatase 1 binding protein, enhances cell spreading and motility by interacting with the actin cytoskeleton. PLoS ONE 4: e4247. doi: 10.1371/journal.pone.0004247.
39. Simpson MJ, Zhang DC, Mariani M, Landman KA, Newgreen DF. 2007. Cell proliferation drives neural crest cell invasion of the intestine. Dev Biol 302: 553-568.
40. Wallace AS, Barlow AJ, Navaratne L, Delalande JM, Tauszig- Delamasure S, Corset V, Thapar N, Burns AJ. 2009. Inhibition of cell death results in hyperganglionosis: Implications for enteric nervous system development. Neurogastroenterol Motil 21: 768-e49. doi: 10.1111/j.1365-2982.2009.01309.x.
41. White DP, Caswell PT, Norman JC. 2007. αvβ3 and α5β1 integrin recycling pathways dictate downstream Rho kinase signaling to regulate persistent cell migration. J Cell Biol 177: 515-525.
42. Yang Y, Guo L, Blattner SM, Mundel P, Kretzler M, Wu C. 2005. Formation and phosphorylation of the PINCH-1-integrin linked kinase-a-parvin complex are important for regulation of renal glomerular podocyte adhesion, architecture, and survival. J Am Soc Nephrol 16: 1966-1976.
43. Young HM, Hearn CJ, Farlie PG, Canty AJ, Thomas PQ, Newgreen DF. 2001. GDNF is a chemoattractant for enteric neural cells. Dev Biol 229: 503-516.
44. Young HM, Bergner AJ, Anderson RB, Enomoto H, Milbrandt J, Newgreen DF, Whitington PM. 2004. Dynamics of neural crest-derived cell migration in the embryonic mouse gut. Dev Biol 270: 455-473.
45. Zhang Y, Chen K, Tu Y, Velyvis A, Yang Y, Qin J, Wu C. 2002. Assembly of the PINCH-ILK-CH-ILKBP complex precedes and is essential for localization of each component to cell- matrix adhesion sites. J Cell Sci 115: 4777-4786.