Non-muscle myosin II regulates neuronal actin dynamics by interacting with guanine nucleotide exchange factors

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Shin, Eun Young ^a   Lee, Chan Soo ^b   Yun, Cheong Yong ^a   Won, So Yoon ^a   Kim, Hyong Kyu ^a   Lee, Yong Hee ^a   Kwak, Sahng June ^c   Kim, Eung Gook ^a  

^a Chungbuk National University College of Medicine   (South Korea)

^b Korea Food and Drug Administration   (South Korea)

^c Dankook University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BETA PIX PROTEIN; BLEBBISTATIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; INTERSECTIN; KALIRIN; MYOSIN II; NERVE GROWTH FACTOR; PROTEIN CDC42; RAC1 PROTEIN; UNCLASSIFIED DRUG; FUSED HETEROCYCLIC RINGS; MYOSIN IIB; P21 ACTIVATED KINASE; PROTEIN BINDING; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; FETUS; FILOPODIUM; GROWTH CONE; HIPPOCAMPUS; NERVE CELL DIFFERENTIATION; NERVE FIBER; NONHUMAN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT; ANIMAL; BIOLOGICAL MODEL; CELL CULTURE; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; FEMALE; METABOLISM; NERVE CELL; NEURITE; PROTEIN TERTIARY STRUCTURE; PSEUDOPODIUM; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ACTINS; ANIMALS; AXONS; CDC42 GTP-BINDING PROTEIN; CELLS, CULTURED; FEMALE; GROWTH CONES; HETEROCYCLIC COMPOUNDS WITH 4 OR MORE RINGS; HIPPOCAMPUS; MODELS, BIOLOGICAL; NERVE GROWTH FACTORS; NEURITES; NEURONS; NONMUSCLE MYOSIN TYPE IIB; P21-ACTIVATED KINASES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PSEUDOPODIA; RAC1 GTP-BINDING PROTEIN; RATS, SPRAGUE-DAWLEY; RHO GUANINE NUCLEOTIDE EXCHANGE FACTORS; SIGNAL TRANSDUCTION;

EID: 84899687377     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0095212     Document Type: Article

References (51)

1. Forscher P, Lin CH, Thompson C (1992) Novel form of growth cone motility involving site-directed actin filament assembly. Nature 357:515-518.
2. Mallavarapu A, Mitchison T (1999) Regulated actin cytoskeleton assembly at filopodium tips controls their extension and retraction. J Cell Biol 146:1097-1106. (Pubitemid 29430450)
3. Forscher P, Smith SJ (1998) Actions of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone. J Cell Biol 107:1505-1516.
4. Okabe S, Hirokawa N (1991) Actin dynamics in growth cones. J Neurosci 11:1918-1929.
5. Welch MD, Mallavarapu A, Rosenblatt J, Mitchison TJ (1997) Actin dynamics in vivo. Curr Opin Cell Biol 9:54-61. (Pubitemid 27065109)
6. Gallo G, Yee HF Jr, Letourneau PC (2002) Actin turnover is required to prevent axon retraction driven by endogenous actomyosin contractility. J Cell Biol 158:1219-1228.
7. Schmidt A, Hall A (2002) Guanine nucleotide exchange factors for Rho GTPases: Turning on the switch. Genes Dev 16:1587-1609. (Pubitemid 34743321)
8. Etienne-Manneville S, Hall A (2000) Rho GTPases in cell biology. Nature 420:629-635. (Pubitemid 36764489)
9. Luo L (2000) Rho GTPases in neuronal morphogenesis. Nat Rev 1:173-180.
10. Rochlin MW, Itoh K, Adelstein RS, Bridgman PC (1995) Localization of myosin IIA and B isoforms in cultured neurons. J Cell Sci 108:3661-3670. (Pubitemid 26003199)
11. Brown ME, Bridgman PC (2003) Retrograde flow rate is increased in growth cones from myosin IIB knockout mice. J Cell Sci 116:1087-1094. (Pubitemid 36395618)
12. Lin CH, Espreafico EM, Mooseker MS, Forscher P (1996) Myosin drives retrograde f-actin flow in neuronal growth cones. Neuron 16:769-782. (Pubitemid 26124054)
13. Medeiros NA, Burnette DT, Forscher P (2006) Myosin II functions in actin-bundle turnover in neuronal growth cones. Nat Cell Biol 8:215-226. (Pubitemid 43336063)
14. Straight AF, Cheung A, Limouze J, Chen I, Westwood NJ, et al. (2003) Dissecting temporal and spatial control of cytokinesis with a myosin II inhibitor. Science 299:1743-1747. (Pubitemid 36337202)
15. Vicente-Manzanares M, Zareno J, Whitmore L, Choi CK, Horwitz AF (2007) Regulation of protrusion, adhesion dynamics, and polarity by myosins iia and iib in migrating cells. J Cell Biol 176:573-580. (Pubitemid 46333973)
16. Lee CS, Choi CK, Shin EY, Schwartz MA, Kim EG (2010) Myosin II directly binds and inhibits dbl family guanine nucleotide exchange factors: A possible link to rho family GTPases. J Cell Biol 190:663-674.
17. Lee CS, Kim KY, Im JB, Choi JW, Kim HK, et al. (2004) βPAK-interacting exchange factor may regulate actin cytoskeleton through interaction with actin. Exp Mol Med 36:582-587.
18. Kim S, Lee SH, Park D (2001) Leucine zipper-mediated homodimerization of the p21-activated kinase-interacting factor, βPIX. Implication for a role in cytoskeletal reorganization. J Biol Chem 276:10581-10584. (Pubitemid 38089224)
19. Banker GA, Cowan WM (1977) Rat hippocampal neurons in dispersed cell culture. Brain Res 126:397-425. (Pubitemid 8090742)
20. Benard V, Bohl BP, Bokoch GM (1999) Characterization of Rac and Cdc42 activation in chemoattractant-stimulated human neutrophils using a novel assay for active GTPases. J Biol Chem 274:13198-13204.
21. Park E, Na M, Choi J, Kim S, Lee JR, et al. (2003) The shank family of postsynaptic density proteins interacts with and promotes synaptic accumulation of beta PIX guanine nucleotide exchange factor for Rac1 and Cdc42. J Biol Chem 278:19220-19229. (Pubitemid 36799313)
22. Shin EY, Shin KS, Lee CS, Woo KN, Quan SH, et al. (2002) Phosphorylation of p85 beta PIX, a Rac/Cdc42-specific guanine nucleotide exchange factor, via the Ras/ERK/PAK2 pathway is required for basic fibroblast growth factor-induced neurite out growth. J Biol Chem 277:44417-44430.
23. Schlenker O, Rittinger K (2009) Structure of dimeric GIT1 and trimeric beta-PIX and implications for GIT-PIX complex assembly. J Mol Biol 386:280-289.
24. Loudon RP, Silver LD, Yee HF Jr, Gallo G (2006) RhoA-kinase and myosin II are required for the maintenance of growth cone polarity and guidance by nerve growth factor. J Neurobiol 66:847-867. (Pubitemid 44025538)
25. Somlyo AP, Somlyo AV (2003) Ca2+ sensitivity of smooth muscle and nonmuscle myosin II: Modulated by g proteins, kinases, and myosin phosphatase. Physiol Rev 1325-1358. (Pubitemid 37222274)
26. Redowicz MJ (2001) Regulation of nonmuscle myosins by heavy chain phosphorylation. J Muscle Res Cell Motil 22:163-173.
27. Even-Faitelson L, Rosenberg M, Ravid S (2005) Pak1 regulates myosin IIB phosphorylation, filament assembly, localization and cell chemotaxis. Cell Signal 17:1137-1148. (Pubitemid 40933533)
28. van Leeuwen FN, van Delft S, Kain HE, van der Kammen RA, Collard JG (1999) Rac regulates phosphorylation of the myosin II heavy chain, actinomyosin disassembly and cell spreading. Nat Cell Biol 1:242-248. (Pubitemid 129500944)
29. Buxton DB, Adelstein RS (2000) Calcium-dependent threonine phosphorylation of nonmuscle myosin in stimulated rbl-2h3 mast cells. J Biol Chem 275:34772-34779.
30. Straussman R, Even L, Ravid S (2001) Myosin II heavy chain isoforms are phosphorylated in an EGF-dependent manner: Involvement of protein kinase C. J Cell Sci 114:3047-3057. (Pubitemid 32821542)
31. Even-Faitelson L, Ravid S (2006) Pak1 and aPKCzeta regulate myosin IIB phosphorylation: A novel signaling pathway regulating filament assembly. Mol Biol Cell 17:2869-2881. (Pubitemid 43993493)
32. Rosenberg M, Ravid S (2006) Protein Kinase Cgamma regulates myosin IIB phosphorylation, cellular localization, and filament assembly. Mol Bio Cell 17:1364-1374. (Pubitemid 43376556)
33. Kimura K, Ito M, Amano M, Chihara K, Fukata Y, et al. (1996) Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase) Science 273:245-248. (Pubitemid 26285892)
34. Aoki K, Nakamura T, Matsuda M (2004) Spatio-temporal regulation of Rac1 and Cdc42 activity during nerve growth factor-induced neurite outgrowth in pc12 cells. J Biol Chem 279:713-719. (Pubitemid 38044876)
35. Birukova AA, Smurova K, Birukov KG, Usatyuk P, Liu F, et al. (2004) Microtubule disassembly induces cytoskeletal remodeling and lung vascular barrier dysfunction: Role of Rho-dependent mechanisms. J Cell Physiol 201:55-70. (Pubitemid 39187045)
36. Birukova AA, Adyshev D, Gorshkov B, Bokoch GM, Birukov KG, et al. (2006) Verin AD: GEF-H1 is involved in agonist-induced human pulmonary endothelial barrier dysfunction. Am J Physiol Lung Cell Mol Physiol 290:L540-548. (Pubitemid 43725099)
37. Nakamura T, Aoki K, Matsuda M (2005) FRET imaging in nerve growth cones reveals a high level of RhoA activity within the peripheral domain. Brain Res Mol Brain Res 139:277-287. (Pubitemid 41317941)
38. Rosner H, Moller W, Wassermann T, Mihatsch J, Blum M (2007) Attenuation of actinomyosinii contractile activity in growth cones accelerates filopodia-guided and microtubule-based neurite elongation. Brain Res 1176:1-10. (Pubitemid 47553114)
39. Even-Ram S, Doyle AD, Conti MA, Matsumoto K, Adelstein RS, et al. (2007) Myosin IIA regulates cell motility and actomyosin-microtubule crosstalk. Nat Cell Biol 9:299-309. (Pubitemid 46344609)
40. Rossman KL, Worthylake DK, Snyder JT, Siderovski DP, Campbell SL, et al. (2002) A crystallographic view of interactions between Dbs and Cdc42: PH domain-assisted guanine nucleotide exchange. Embo J 21:1315-1326. (Pubitemid 34246510)
41. Chhatriwala MK, Betts L, Worthylake DK, Sondek J (2007) The DH and PH domains of Trio coordinately engage Rho GTPases for their efficient activation. J Mol Biol 368:1307-1320. (Pubitemid 46617588)
42. Liu X, Wang H, Eberstadt M, Schnuchel A, Olejniczak ET, et al. (1998) NMR structure and mutagenesis of the N-terminal Dbl homology domain of the nucleotide exchange factor Trio. Cell 95:269-277. (Pubitemid 28473787)
43. Shin EY, Lee CS, Cho TG, Kim YG, Song S, et al. (2006) bPak-interacting exchange factor-mediated Rac1 activation requires smgGDS guanine nucleotide exchange factor in basic fibroblast growth factor-induced nuerite outgrowth. J Biol Chem 281:35954-35964. (Pubitemid 46041327)
44. ten Klooster JP, Jaffer ZM, Chernorff J, Hordijk PL (2006) Targeting and activation of Rac1 are mediated by the exchange factor βPIX. J Cell Biol 172:759-769.
45. Kornack DR, Giger RJ (2005) Probing microtubule +TIPs: Regulation of axon branching. Curr Opin Neurobiol 15:58-66. (Pubitemid 40249962)
46. Moon MS, Gomez TM (2010) Balanced vav2 GEF activity regulates neurite outgrowth and branching in vitro and in vivo. Mol Cell Neurosci 44:118-128.
47. Santiago-Medina M, Gregus KA, Gomez TM (2013) PAK-PIX interactions regulate adhesion dynamics and membrane protrusion to control neurite outgrowth. J Cell Sci 126:1122-1133.
48. Fischer RS, Gardel M, Ma X, Adelstein RS, Waterman CM (2009) Local cortical tension by myosin II guides 3d endothelial cell branching. Curr Biol 19:260-265.
49. Sutton TA, Mang HE, Atkinson SJ (2001) Rho-kinase regulates myosin II activation in MDCK cells during recovery after ATP depletion. Am J Physiol 281:F810-818.
50. Raz L, Zhang QG, Zhou CF, Han D, Gulati P, et al. (2010) Role of Rac1 GTPase in NADPH oxidase activation and cognitive impairment following cerebral ischemia in the rat. PLoS One 5:e12606.
51. Trapp T, Olah L, Holker I, Besselmann M, Tiesler C, et al. (2001) GTPase RhoB: An early predictor of neuronal death after transient focal ischemia in mice. Mol Cell Neurosci 17:883-894. (Pubitemid 32510536)