Caldesmon regulates actin dynamics to influence cranial neural crest migration in Xenopus

Molecular Biology of the Cell

Volumn 22, Issue 18, 2011, Pages 3355-3365

  Nie, Shuyi ^a   Kee, Yun ^b,c   Bronner Fraser, Marianne ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b Kangwon National University   (South Korea)

^c Korea Basic Science Institute (KBSI)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ANTISENSE OLIGONUCLEOTIDE; CALCIUM; CALDESMON; CYCLIN DEPENDENT KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE;

ACTIN FILAMENT; ARTICLE; BINDING SITE; CELL MIGRATION; CELL MOTILITY; CELL SHAPE; CELL STRUCTURE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EXPLANT; MOLECULAR DYNAMICS; MUTATION; NEURAL CREST; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; XENOPUS LAEVIS;

ACTIN CYTOSKELETON; ACTINS; AMINO ACID SEQUENCE; ANIMALS; CALMODULIN-BINDING PROTEINS; CARTILAGE; CELL MOVEMENT; CELLS, CULTURED; GENE KNOCKDOWN TECHNIQUES; LARVA; MOLECULAR SEQUENCE DATA; MORPHOLINOS; NEURAL CREST; PHALLOIDINE; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SKULL; XENOPUS LAEVIS;

EID: 80052836811     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-02-0165     Document Type: Article

References (60)

1. Alfandari D, Cousin H, Gaultier A, Hoffstrom BG, DeSimone DW (2003). Integrin alpha5beta1 supports the migration of Xenopus cranial neural crest on fibronectin. Dev Biol 260, 449-464. (Pubitemid 36960091)
2. Borchers A, David R, Wedlich D (2001). Xenopus cadherin-11 restrains cranial neural crest migration and influences neural crest specification. Development 128, 3049-3060. (Pubitemid 32825750)
3. Borchers A, Epperlein HH, Wedlich D (2000). An assay system to study migratory behavior of cranial neural crest cells in Xenopus. Dev Genes Evol 210, 217-222. (Pubitemid 30175584)
4. Carmona-Fontaine C, Matthews HK, Kuriyama S, Moreno M, Dunn GA, Parsons M, Stern CD, Mayor R (2008). Contact inhibition of locomotion in vivo controls neural crest directional migration. Nature 456, 957-961.
5. Chalovich JM, Chen YD, Dudek R, Luo H (1995). Kinetics of binding of caldesmon to actin. J Biol Chem 270, 9911-9916.
6. Chang C, Wilson PA, Mathews LS, Hemmati-Brivanlou A (1997). A Xenopus type I activin receptor mediates mesodermal but not neural specification during embryogenesis. Development 124, 827-837. (Pubitemid 27107431)
7. Childs TJ, Watson MH, Sanghera JS, Campbell DL, Pelech SL, Mak AS (1992). Phosphorylation of smooth muscle caldesmon by mitogen-activated protein (MAP) kinase and expression of MAP kinase in differentiated smooth muscle cells. J Biol Chem 267, 22853-22859.
8. Dabrowska R, Hinssen H, Galazkiewicz B, Nowak E (1996). Modulation of gelsolin-induced actin-filament severing by caldesmon and tropomyosin and the effect of these proteins on the actin activation of myosin Mg(2+)-ATPase activity. Biochem J 315, 753-759.
9. De Calisto J, Araya C, Marchant L, Riaz CF, Mayor R (2005). Essential role of non-canonical Wnt signalling in neural crest migration. Development 132, 2587-2597. (Pubitemid 40883257)
10. DeSimone DW, Davidson L, Marsden M, Alfandari D (2005). The Xenopus embryo as a model system for studies of cell migration. Methods Mol Biol 294, 235-245.
11. Eppinga RD, Li Y, Lin JL, Mak AS, Lin JJ (2006). Requirement of reversible caldesmon phosphorylation at P21-activated kinase-responsive sites for lamellipodia extensions during cell migration. Cell Motil Cytoskeleton 63, 543-562. (Pubitemid 44384280)
12. Eves R, Webb BA, Zhou S, Mak AS (2006). Caldesmon is an integral component of podosomes in smooth muscle cells. J Cell Sci 119, 1691-1702. (Pubitemid 43810996)
13. Foster DB, Huang R, Hatch V, Craig R, Graceffa P, Lehman W, Wang CL (2004). Modes of caldesmon binding to actin: sites of caldesmon contact and modulation of interactions by phosphorylation. J Biol Chem 279, 53387-53394. (Pubitemid 40051844)
14. Foster DB, Shen LH, Kelly J, Thibault P, Van Eyk JE, Mak AS (2000). Phosphorylation of caldesmon by p21-activated kinaseImplications for the Ca(2+) sensitivity of smooth muscle contraction. J Biol Chem 275, 1959-1965. (Pubitemid 30060822)
15. Fukumoto K, Morita T, Mayanagi T, Tanokashira D, Yoshida T, Sakai A, Sobue K (2009). Detrimental effects of glucocorticoids on neuronal migration during brain development. Mol Psychiatry 14, 1119-1131.
16. Goncharova EA, Shirinsky VP, Shevelev AY, Marston SB, Vorotnikov AV (2001). Actomyosin cross-linking by caldesmon in non-muscle cells. FEBS Lett 497, 113-117. (Pubitemid 32476888)
17. Grosheva I, Vittitow JL, Goichberg P, Gabelt BT, Kaufman PL, Borras T, Geiger B, Bershadsky AD (2006). Caldesmon effects on the actin cytoskeleton and cell adhesion in cultured HTM cells. Exp Eye Res 82, 945-958. (Pubitemid 44287907)
18. Gu Z, Kordowska J, Williams GL, Wang CL, Hai CM (2007). Erk1/2 MAPK and caldesmon differentially regulate podosome dynamics in A7r5 vascular smooth muscle cells. Exp Cell Res 313, 849-866.
19. Helbling PM, Tran CT, Brandli AW (1998). Requirement for EphA receptor signaling in the segregation of Xenopus third and fourth arch neural crest cells. Mech Dev 78, 63-79. (Pubitemid 28566212)
20. Helfman DM, Levy ET, Berthier C, Shtutman M, Riveline D, Grosheva I, Lachish-Zalait A, Elbaum M, Bershadsky AD (1999). Caldesmon inhibits nonmuscle cell contractility and interferes with the formation of focal adhesions. Mol Biol Cell 10, 3097-3112. (Pubitemid 29489548)
21. Hemric ME, Tracy PB, Haeberle JR (1994). Caldesmon enhances the binding of myosin to the cytoskeleton during platelet activation. J Biol Chem 269, 4125-4128. (Pubitemid 24237765)
22. Huang R, Li L, Guo H, Wang CL (2003). Caldesmon binding to actin is regulated by calmodulin and phosphorylation via different mechanisms. Biochemistry 42, 2513-2523. (Pubitemid 36330604)
23. Ishikawa R, Yamashiro S, Kohama K, Matsumura F (1998). Regulation of actin binding and actin bundling activities of fascin by caldesmon coupled with tropomyosin. J Biol Chem 273, 26991-26997. (Pubitemid 28471722)
24. Ishikawa R, Yamashiro S, Matsumura F (1989a). Annealing of gelsolin-severed actin fragments by tropomyosin in the presence of Ca2+. Potentiation of the annealing process by caldesmon. J Biol Chem 264, 16764-16770. (Pubitemid 19243574)
25. Ishikawa R, Yamashiro S, Matsumura F (1989b). Differential modulation of actin-severing activity of gelsolin by multiple isoforms of cultured rat cell tropomyosin. Potentiation of protective ability of tropomyosins by 83-kDa nonmuscle caldesmon. J Biol Chem 264, 7490-7497. (Pubitemid 19119165)
26. Kashef J, Kohler A, Kuriyama S, Alfandari D, Mayor R, Wedlich D (2009). Cadherin-11 regulates protrusive activity in Xenopus cranial neural crest cells upstream of Trio and the small GTPases. Genes Dev 23, 1393-1398.
27. Kordowska J, Hetrick T, Adam LP, Wang CL (2006). Phosphorylated l-caldesmon is involved in disassembly of actin stress fibers and postmitotic spreading. Exp Cell Res 312, 95-110. (Pubitemid 41721173)
28. Li Y, Lin JL, Reiter RS, Daniels K, Soll DR, Lin JJ (2004). Caldesmon mutant defective in Ca(2+)-calmodulin binding interferes with assembly of stress fibers and affects cell morphology, growth and motility. J Cell Sci 117, 3593-3604. (Pubitemid 39206399)
29. Lin JJ, Li Y, Eppinga RD, Wang Q, Jin JP (2009). Chapter 1: roles of caldesmon in cell motility and actin cytoskeleton remodeling. Int Rev Cell Mol Biol 274, 1-68.
30. Mak AS, Carpenter M, Smillie LB, Wang JH (1991). Phosphorylation of caldesmon by p34cdc2 kinase. Identification of phosphorylation sites. J Biol Chem 266, 19971-19975. (Pubitemid 21908414)
31. Matthews HK, Broders-Bondon F, Thiery JP, Mayor R (2008a). Wnt11r is required for cranial neural crest migration. Dev Dyn 237, 3404-3409.
32. Matthews HK, Marchant L, Carmona-Fontaine C, Kuriyama S, Larrain J, Holt MR, Parsons M, Mayor R (2008b). Directional migration of neural crest cells in vivo is regulated by Syndecan-4/Rac1 and non-canonical Wnt signaling/RhoA. Development 135, 1771-1780.
33. Mayanagi T, Morita T, Hayashi K, Fukumoto K, Sobue K (2008). Glucocorticoid receptor-mediated expression of caldesmon regulates cell migration via the reorganization of the actin cytoskeleton. J Biol Chem 283, 31183-31196.
34. McFawn PK, Shen L, Vincent SG, Mak A, Van Eyk JE, Fisher JT (2003). Calcium-independent contraction and sensitization of airway smooth muscle by p21-activated protein kinase. Am J Physiol Lung Cell Mol Physiol 284, L863-870.
35. Mellitzer G, Xu Q, Wilkinson DG (1999). Eph receptors and ephrins restrict cell intermingling and communication. Nature 400, 77-81. (Pubitemid 29315114)
36. Nie S, Kee Y, Bronner-Fraser M (2009). Myosin-X is critical for migratory ability of Xenopus cranial neural crest cells. Dev Biol 335, 132-142.
37. Nomura M, Yoshikawa K, Tanaka T, Sobue K, Maruyama K (1987). The role of tropomyosin in the interactions of F-actin with caldesmon and actin-binding protein (or filamin). Eur J Biochem 163, 467-471. (Pubitemid 17036343)
38. Novy RE, Lin JL, Lin JJ (1991). Characterization of cDNA clones encoding a human fibroblast caldesmon isoform and analysis of caldesmon expression in normal and transformed cells. J Biol Chem 266, 16917-16924. (Pubitemid 21907888)
39. Numaguchi Y, Huang S, Polte TR, Eichler GS, Wang N, Ingber DE (2003). Caldesmon-dependent switching between capillary endothelial cell growth and apoptosis through modulation of cell shape and contractility. Angiogenesis 6, 55-64. (Pubitemid 37305340)
40. Paul ER, Ngai PK, Walsh MP, Groschel-Stewart U (1995). Embryonic chicken gizzard: expression of the smooth muscle regulatory proteins caldesmon and myosin light chain kinase. Cell Tissue Res 279, 331-337.
41. Rangarajan J, Luo T, Sargent TD (2006). PCNS: a novel protocadherin required for cranial neural crest migration and somite morphogenesis in Xenopus. Dev Biol 295, 206-218. (Pubitemid 44041335)
42. Robinson V, Smith A, Flenniken AM, Wilkinson DG (1997). Roles of Eph receptors and ephrins in neural crest pathfinding. Cell Tissue Res 290, 265-274. (Pubitemid 27470059)
43. Sadaghiani B, Thiebaud CH (1987). Neural crest development in the Xenopus laevis embryo, studied by interspecific transplantation and scanning electron microscopy. Dev Biol 124, 91-110.
44. Santiago A, Erickson CA (2002). Ephrin-B ligands play a dual role in the control of neural crest cell migration. Development 129, 3621-3632.
45. Smith A, Robinson V, Patel K, Wilkinson DG (1997). The EphA4 and EphB1 receptor tyrosine kinases and ephrin-B2 ligand regulate targeted migration of branchial neural crest cells. Curr Biol 7, 561-570. (Pubitemid 27335651)
46. Sobue K, Sellers JR (1991). Caldesmon, a novel regulatory protein in smooth muscle and nonmuscle actomyosin systems. J Biol Chem 266, 12115-12118. (Pubitemid 21907062)
47. Tanaka J, Watanabe T, Nakamura N, Sobue K (1993). Morphological and biochemical analyses of contractile proteins (actin, myosin, caldesmon and tropomyosin) in normal and transformed cells. J Cell Sci 104, 595-606. (Pubitemid 23098697)
48. Theveneau E, Marchant L, Kuriyama S, Gull M, Moepps B, Parsons M, Mayor R (2010). Collective chemotaxis requires contact-dependent cell polarity. Dev Cell 19, 39-53.
49. Vallin J, Girault JM, Thiery JP, Broders F (1998). Xenopus cadherin-11 is expressed in different populations of migrating neural crest cells. Mech Dev 75, 171-174. (Pubitemid 28423700)
50. Van Eyk JE, Arrell DK, Foster DB, Strauss JD, Heinonen TY, Furmaniak-Kazmierczak E, Cote GP, Mak AS (1998). Different molecular mechanisms for Rho family GTPase-dependent, Ca2+-independent contraction of smooth muscle. J Biol Chem 273, 23433-23439. (Pubitemid 28417533)
51. Warren KS, Shutt DC, McDermott JP, Lin JL, Soll DR, Lin JJ (1996). Overexpression of microfilament-stabilizing human caldesmon fragment, CaD39, affects cell attachment, spreading, and cytokinesis. Cell Motil Cytoskeleton 34, 215-229. (Pubitemid 26242169)
52. Winklbauer R, Selchow A, Nagel M, Angres B (1992). Cell interaction and its role in mesoderm cell migration during Xenopus gastrulation. Dev Dyn 195, 290-302. (Pubitemid 23131716)
53. Yamakita Y, Oosawa F, Yamashiro S, Matsumura F (2003). Caldesmon inhibits Arp2/3-mediated actin nucleation. J Biol Chem 278, 17937-17944. (Pubitemid 36799400)
54. Yamashiro S, Chern H, Yamakita Y, Matsumura F (2001). Mutant caldesmon lacking cdc2 phosphorylation sites delays M-phase entry and inhibits cytokinesis. Mol Biol Cell 12, 239-250. (Pubitemid 32060590)
55. Yamashiro S, Yamakita Y, Hosoya H, Matsumura F (1991). Phosphorylation of non-muscle caldesmon by p34cdc2 kinase during mitosis. Nature 349, 169-172. (Pubitemid 21912039)
56. Yamashiro S, Yamakita Y, Ishikawa R, Matsumura F (1990). Mitosis-specific phosphorylation causes 83K non-muscle caldesmon to dissociate from microfilaments. Nature 344, 675-678.
57. Yamashiro S, Yoshida K, Yamakita Y, Matsumura F (1994). Caldesmon: possible functions in microfilament reorganization during mitosis and cell transformation. Adv Exp Med Biol 358, 113-122. (Pubitemid 24284917)
58. Yoshio T, Morita T, Kimura Y, Tsujii M, Hayashi N, Sobue K (2007). Caldesmon suppresses cancer cell invasion by regulating podosome/invadopodium formation. FEBS Lett 581, 3777-3782. (Pubitemid 47102304)
59. Zheng PP, Severijnen LA, van der Weiden M, Willemsen R, Kros JM (2009a). A crucial role of caldesmon in vascular development in vivo. Cardiovasc Res 81, 362-369.
60. Zheng PP, Severijnen LA, Willemsen R, Kros JM (2009b). Caldesmon is essential for cardiac morphogenesis and function: in vivo study using a zebrafish model. Biochem Biophys Res Commun 378, 37-40.