Myosin-II negatiwely regulates minor process extension and the temporal development of neuronal polarity

Developmental Neurobiology

Volumn 69, Issue 5, 2009, Pages 279-298

  Kollins, K M ^a   Hy, J ^a   Bridgman, P C ^b   Hyang, Y Q ^a   Gallo, G ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Minor process; Myosin II; Myosin light chain kinase; Neuronal development; Polarity; Rhokinase

Indexed keywords

1 (5 IODO 1 NAPHTHALENESULFONYL)HEXAHYDRO 1H 1,4 DIAZEPINE; 4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; BLEBBISTATIN; EXOENZYME C3; MYOSIN II; MYOSIN IIB; MYOSIN LIGHT CHAIN KINASE; RHO KINASE; ENZYME INHIBITOR; FUSED HETEROCYCLIC RINGS; ISOENZYME; METALLOPROTEINASE; MYOSIN; MYOSIN LIGHT CHAIN; MYOSINASE II;

ANIMAL CELL; ARTICLE; BRAIN DEVELOPMENT; CELL ASSAY; CELL MATURATION; CELL MEMBRANE PERMEABILITY; CELL SIZE; CONTROLLED STUDY; EMBRYO; ENZYME INHIBITION; FOREBRAIN; GENE REPRESSION; HIPPOCAMPUS; IMAGING SYSTEM; KNOCKOUT GENE; LIGHT CHAIN; MOUSE; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVE CONDUCTION; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE; CELL GROWTH; CELL POLARITY; CHICK EMBRYO; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; METABOLISM; METHODOLOGY; NERVE CELL; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; PHOSPHORYLATION; PHYSIOLOGY; TIME;

ANIMALS; CELL GROWTH PROCESSES; CELL POLARITY; CELLS, CULTURED; CHICK EMBRYO; ENZYME INHIBITORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HETEROCYCLIC COMPOUNDS WITH 4 OR MORE RINGS; HIPPOCAMPUS; ISOENZYMES; METALLOENDOPEPTIDASES; MYOSIN LIGHT CHAINS; MYOSIN TYPE II; MYOSIN-LIGHT-CHAIN KINASE; MYOSINS; NEUROGENESIS; NEURONAL PLASTICITY; NEURONS; PHOSPHORYLATION; PROSENCEPHALON; RHO-ASSOCIATED KINASES; TIME FACTORS; TRANSFECTION;

EID: 65649115129     PISSN: 00223034     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.20704     Document Type: Article

References (64)

1. Allingham J. S. Smith R. Rayment I. 2005, The structural basis of blebbistatin inhibition and specificity for myosin II, Nat Struct Mol Biol 12: 378-379.
2. Amano M. Fukata Y. Kaibuchi K. 2000. Regulation and functions of Rho-associated kinase. Exp Cell Res 261
3. Arimura N. Kaibuchi K. 2007, Neuronal polarity: From extracellular signals to intracellular mechanisms. Nat Rev Neurosci 8: 194-205.
4. Bao J. Ma X. Liu C. Adelstein R. 2007. Replacement of nonmuscle myosin 1I-B with II-A rescues brain but not cardiac defects in mice. J Biol Chem 282: 22102-22111.
5. Barnes A. P. Lilley B. N. Pan Y. A. Plummer L. J. Powell A. W. Raines A. N. Sanes J. R. et al. 2007, LKB1 and SAD kinases define a pathway required for the polarization of cortical neurons. Cell 129: 549-563.
6. Bellion A. Baudoin J. P. Alvarez C. Bornens M. Metin C. 2005. Nucleokinesis in tangentially migrating neurons comprises two alternating phases: Forward migration of the Golgi/centrosome associated with centrosome splitting and myosin contraction at the rear. J Neurosci 25: 5691-5699.
7. Beningo K. A. Hamao K. Dembo M. Wang Y. L. Hosoya H. 2006. Traction forces of fibroblasts are regulated by the Rho-dependent kinase but not by the myosin light chain kinase. Arch Biochem Biophys 456: 224-231.
8. Birkenfeld J. Betz H. Roth D. 2001. Inhibition of neurite extension by overexpression of individual domains of LIM kinase 1. J Neurochem 78: 924-927.
9. Bito H. Furuyashiki T. Ishihara H. Shibasaki Y. Ohashi K. Mizuno K. Maekawa M. Ishizaki T. Narumiya S. 2000. A critical role for a Rho-associated kinase, p160ROCK, in determining axon outgrowth in mammalian CNS neurons. Neuron 26: 431-441.
10. Bradke F. Dotti C. G. 2000a. Establishment of neuronal polarity: Lessons from cultured hippocampal neurons. Curr Opin Neurobiol 10: 574-581.
11. Bradke F. Dotti C. G. 2000b. Changes in membrane trafficking and actin dynamics during axon formation in cultured hippocampal neurons. Microsc Res Tech 48: 3-11.
12. Bresnick A. R. 1999. Molecular mechanisms of nonmuscle myosin-II regulation. Curr Opin Cell Biol 11: 26-33.
13. Brown M. E. Bridgman P. C. 2004, Myosin function in nervous and sensory systems. J Neurobiol 58: 118-130.
14. Calderon de Anda F. Gartner A. Tsai L. H. Dotti C. G. 2008. Pyramidal neuron polarity axis is defined at the bipolar stage. J Cell Sci 121: 178-185.
15. Chada S. Lamoureux P. Buxbaum R. E. Heidemann S. R. 1997. Cytomechanics of neurite outgrowth from chick brain neurons. J Cell Sci 110 (Pt 10): 1179-1186.
16. Chantler P. D. Wylie S. R. 2003. Elucidation of the separate roles of myosins IIA and IIB during neurite outgrowth, adhesion and retraction. IEE Proc Nanobiotechnol 150: 111-125.
17. Conti M. A. Adelstein R. S. 2008. Nonmuscle myosin moves in new directions. J Cell Sci 121: 11-18.
18. Craig A. M. Banker G. 1994. Neuronal polarity. Annu Rev Neurosci 17: 267-310.
19. Da Silva J. S. Dotti C. G. 2002. Breaking the neuronal sphere: Regulation of the actin cytoskeleton in neuritogenesis. Nat Rev Neurosci 3: 694-704.
20. Da Silva J. S. Medina M. Zuliani C. Di Nardo A. Witke W. Dotti C. G. 2003. RhoA/ROCK regulation of neuritogenesis via profilin IIa-mediated control of actin stability. J Cell Biol 162: 1267-1279.
21. Dehmelt L. Halpain S. 2004. Actin and microtubules in neurite initiation: Are MAPs the missing link? J Neurobiol 58: 18-33.
22. Dehmelt L. Smart F. M. Ozer R. S. Halpain S. 2003. The role of microtubule-associated protein 2c in the reorganization of MTs and lamellipodia during neurite initiation. J Neurosci 29: 9479-9990.
23. Dent E. W. Gertler F. B. 2003. Cytoskelet al. dynamics and transport in growth cone motility and axon guidance. Neuron 40: 209-227.
24. Dent E. W. Kwiatkowski A. V. Mebane L. M. Philippar U. Barzik M. Rubinson D. A. Gupton S. et al. 2007. Filopodia are required for cortical neurite initiation. Nat Cell Biol 9: 1347-1359.
25. Gallagher E. D. Gutowski S. Sternweis P. C. Cobb M. H. 2004, RhoA binds to the amino terminus of MEKK1 and regulates its kinase activity. J Biol Chem 279: 1872-1877.
26. Gallo G. 2004. Myosin II activity is required for severinginduced axon retraction in vitro. Exp Neurol 189: 112-121.
27. Gallo G. Yee H. F. Jr. Letourneau P. C. 2002. Actin turnover is required to prevent axon retraction driven by endogenous actomyosin contractility. J Cell Biol 158: 1219-1228.
28. Golomb E. Ma X. Jana S. S. Preston Y. A. Kawamoto S. Shoham N. G. Goldin E. et al. 2004. Identification and characterization of nonmuscle myosin II-C, a new member of the myosin II family. J Biol Chem 279: 2800-2808.
29. Goslin K. Banker G. 1989. Experimental observations on the development of polarity by hippocampal neurons in culture. J Cell Biol 108: 1507-1516.
30. Govek E. E. Newey S. E. Van Aelst L. 2005. The role of the Rho GTPases in neuronal development. Genes Dev 19: 1-49.
31. Heidemann S. R. Reynolds M. Ngo K. Lamoureux P. 2003. The culture of chick forebrain neurons. Methods Cell Biol 71: 51-65.
32. Jacobson C. Schnapp B. Banker G. A. 2006. A change in the selective translocation of the Kinesin-1 motor domain marks the initial specification of the axon. Neuron 49: 797-804.
33. Ketschek A. R. Jones S. L. Gallo G. 2007. Axon extension in the fast and slow lanes: Substratum-dependent engagement of myosin II functions. Dev Neurobiol 67: 1305-1320.
34. Kim Y. S. Chang S. 2004. Modulation of actomyosin contractility by myosin light chain phosphorylation/dephosphorylation through Rho GTPases signaling specifies axon formation in neurons. Biochem Biophys Res Commun 318: 579-587.
35. Kim Y. S. Fritz J. L. Seneviratne A. K. VanBerkum M. F. 2002. 4Constitulively active myosin light chain kinase alters axon guidance decisions in Drosophila embryos. Dev Biol 249: 367-381.
36. Koh C. G. 2006. Rho GTPases and their regulators in neuronal functions and development. Neurosignals 15: 228-237.
37. Kostic A. Sap J. Sheetz M. 2007. RPTPα is required for rigidity-dependent inhibition of extension and differentiation of hippocampal neurons. J Cell Sci 120: 3895-3904.
38. Kubo T. Endo M. Hata K. Taniguehi J. Kitajo K. Tomura S. Yamaguchi A. et al. 2008. Myosin IIA is required for neurite outgrowth inhibition produced by repulsive guidance molecule. J Neurochem 105: 113-126.
39. Kwiatkowski A. V. Rubinson D. A. Dent E. W. Edward van Veen J. Leslie J. D. Zhang J. Mebane L. M. et al. 2007. Ena/VASP is Required for neuritogenesis in the developing cortex. Neuron 56: 441-455.
40. Lamoureux P. Ruthel G. Buxbaum R. E. Heidemann S. R. 2002. Mechanical tension can specify axonal fate in hippocampal neurons. J Cell Biol 159: 499-508.
41. Letourneau P. C. Shattuck T. A. Ressler A. H. 1987. "Pull" and "push" in neurite elongation: Observations on the effects of different concentrations of cytochalasin B and taxol. Cell Motil Cyto 8: 193-209.
42. LoTurco J. J. Bai J. 2006. The multipolar stage and disruptions in neuronal migration. Trends Neurosci 29: 407-413.
43. Loudon R. P. Silver L. D. Yee H. F. 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.
44. Luo L. 2000. Rho GTPases in neuronal morphogenesis. Nat Rev Neurosci 1: 173-180.
45. Ma X. Bao J. Adelstein R. 2007. Loss of cell adhesion causes hydrocephalus in nonmuscle myosin II-B-ablated and mutated mice. Mol Biol Cell 18: 2305-2312.
46. Marsh L. Letourneau P. C. 1984. Growth of neurites without filopodial or lamellipodial activity in the presence of cytochalasin B. J Cell Biol 99: 2041-2047.
47. Medeiros N. A. Burnette D. T. Forscher P. 2006. Myosin II functions in actin-bundle turnover in neuronal growth cones. Nat Cell Biol 8: 215-226.
48. Metin C. Baudoin J. P. Rakic S. Parnavelas J. G. 2006. Cell and molecular mechanisms involved in the migration of cortical interneurons. Eur J Neurosci 23: 894-900.
49. Ng J. Luo L. 2004. Rho GTPases regulate axon growth through convergent and divergent signaling pathways. Neuron 44: 779-793.
50. Nishimura T. Yamaguchi T. Kato K. Yoshizawa M. Nabeshima Y. Ohno S. Hoshino M. et al. 2005. PAR-6-PAR-3 mediates Cdc42-induced Rac activation through the Rac GEFs STEF/Tiam 1. Nat Cell Biol 7: 270-277.
51. Noctor S. C. Martinez-Cerdeno V. Ivic L. Kriegstein A. R. 2004. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7: 136-144.
52. Rochlin M. W. Wickline K. M. Bridgman P. C. 1996. Microtubule stability decreases axon elongation but not axoplasm production. J Neurosci 16: 3236-3246.
53. Rösner H. Moller W. Wassermann T. Mihatsch J. Blum M. 2007. Attenuation of actinomyosin II contractile activity in growth cones accelerates filopodia-guided and microtubule-based neurite elongation. Brain Res 1176: 1-10.
54. Ryu J. Liu L. Wong T. P. Wu D. C. Burette A. Weinberg R. Wang Y. T. et al. 2006. A critical role for myosin IIb in dendritic spine morphology and synaptic function. Neuron 49: 175-182.
55. Shelly M. Cancedda L. Heilshorn S. Sumbre G. Poo M. M. 2007. LKB1/STRAD promotes axon initiation during neuronal polarization. Cell 129: 565-577.
56. Solecki D. J. Govek E. E. Tomoda T. Flatten M. E. 2006. Neuronal polarity in CNS development. Genes Dev 20: 2639-2647.
57. Straight A. F. Cheung A. Limouze J. Chen I. Westwood N. J. Sellers J. R. Mitchison T. J. 2003. Dissecting temporal and spatial control of cytokinesis with a myosin II inhibitor. Science 299: 1743-1747.
58. Totsukawa G. Wu Y. Sasaki Y. Hartshorne D. J. Yamakita Y. Yamashiro S. Matsumura F. 2004. Distinct roles of MLCK and ROCK in the regulation of membrane protrusions and focal adhesion dynamics during cell migration of fibroblasts. J Cell Biol 164: 427-439.
59. Tullio A. N. Bridgman P. C. Tresser N. J. Chan C. C. Conti M. A. Adelstein R. S. Hara Y. 2001. Structural abnormalities develop in the brain after ablation of the gene encoding nonmuscle myosin II-B heavy chain. J Comp Neurol 433: 62-74.
60. Verkhovsky A. B. Svitkina T. M. Borisy G. G. 1997. Polarity sorting of actin filaments in cytochalasin-treated fibroblasts. J Cell Sci 110: 1693-1704.
61. Wiggin G. R. Fawcett J. P. Pawson T. 2005. Polarity proteins in axon specification and synaptogenesis. Dev Cell 8: 803-816.
62. Wylie S. R. Chantler P. D. 2001. Separate but linked functions of conventional myosins modulate adhesion and neurite outgrowth. Nat Cell Biol 3: 88-92.
63. Wylie S. R. Chantler P. D. 2003. Myosin IIA drives neurite retraction. Mol Biol Cell 14: 4654-4666.
64. Yoshimura T. Arimura N. Kaibuchi K. 2006. Signaling networks in neuronal polarization. J Neurosci 26: 10626-10630.