MLCK regulates Schwann cell cytoskeletal organization, differentiation and myelination

Journal of Cell Science

Volumn 124, Issue 22, 2011, Pages 3784-3796

  Leitman, Ellen M ^a   Tewari, Ambika ^a   Horn, Meryl ^a   Urbanski, Mateusz ^a,b   Damanakis, Evangelos ^a   Einheber, Steven ^a   Salzer, James L ^c   de Lanerolle, Primal ^d   Melendez Vasquez, Carmen V ^a  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Mlck; Myelination; Myosin II; Schwann cell

Indexed keywords

CYCLIC AMP; MYELIN; MYOSIN II; MYOSIN LIGHT CHAIN; MYOSIN LIGHT CHAIN KINASE; PROTEIN C JUN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL MEMBRANE; CELL NUCLEUS; CONTROLLED STUDY; CYTOSKELETON; DOWN REGULATION; GENE SILENCING; GENETIC TRANSCRIPTION; LYSOSOME; MYELINATION; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SCHWANN CELL;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; CYTOSKELETON; MYELIN SHEATH; MYOSIN-LIGHT-CHAIN KINASE; RATS; SCHWANN CELLS;

EID: 84856797075     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.080200     Document Type: Article

References (68)

1. Adelstein, R. S. and Conti, M. A. (1975). Phosphorylation of platelet myosin increases actin activated myosin ATPase activity. Nature 256, 597-598.
2. Andzelm, M. M., Chen, X., Krzewski, K., Orange, J. S. and Strominger, J. L. (2007). Myosin IIA is required for cytolytic granule exocytosis in human NK cells. J. Exp. Med. 204, 2285-2291.
3. Benninger, Y., Thurnherr, T., Pereira, J. A., Krause, S., Wu, X., Chrostek-Grashoff, A., Herzog, D., Nave, K. A., Franklin, R. J., Meijer, D. et al. (2007). Essential and distinct roles for cdc42 and rac1 in the regulation of Schwann cell biology during peripheral nervous system development. J. Cell Biol. 177, 1051-1061.
4. Blue, E. K., Goeckeler, Z. M., Jin, Y., Hou, L., Dixon, S. A., Herring, B. P., Wysolmerski, R. B. and Gallagher, P. J. (2002). 220- and 130-kDa MLCKs have distinct tissue distributions and intracellular localization patterns. Am. J. Physiol. Cell Physiol. 282, C451-C460.
5. Bunge, R. P., Bunge, M. B. and Bates, M. (1989). Movements of the Schwann cell nucleus implicate progression of the inner (axon-related) Schwann cell process during myelination. J. Cell Biol. 109, 273-284.
6. Chang, Y., Aurade, F., Larbret, F., Zhang, Y., Le Couedic, J. P., Momeux, L., Larghero, J., Bertoglio, J., Louache, F., Cramer, E. et al. (2007). Proplatelet formation is regulated by the Rho/ROCK pathway. Blood 109, 4229-4236.
7. Chen, J. W., Murphy, T. L., Willingham, M. C., Pastan, I. and August, J. T. (1985). Identification of two lysosomal membrane glycoproteins. J. Cell Biol. 101, 85-95.
8. Chen, Z., Naveiras, O., Balduini, A., Mammoto, A., Conti, M. A., Adelstein, R. S., Ingber, D., Daley, G. Q. and Shivdasani, R. A. (2007). The May-Hegglin anomaly gene MYH9 is a negative regulator of platelet biogenesis modulated by the Rho-ROCK pathway. Blood 110, 171-179.
9. Chhabra, E. S. and Higgs, H. N. (2007). The many faces of actin: matching assembly factors with cellular structures. Nat. Cell Biol. 9, 1110-1121.
10. Colman, D. R., Kreibich, G., Frey, A. B. and Sabatini, D. D. (1982). Synthesis and incorporation of myelin polypeptides into CNS myelin. J. Cell Biol. 95, 598-608.
11. de Lanerolle, P., Adelstein, R. S., Feramisco, J. R. and Burridge, K. (1981). Characterization of antibodies to smooth muscle myosin kinase and their use in localizing myosin kinase in nonmuscle cells. Proc. Natl. Acad. Sci. USA 78, 4738-4742.
12. de Lanerolle, P., Nishikawa, M., Yost, D. A. and Adelstein, R. S. (1984). Increased phosphorylation of myosin light chain kinase after an increase in cyclic AMP in intact smooth muscle. Science 223, 1415-1417.
13. de Lanerolle, P., Nishikawa, M., Felsen, R. and Adelstein, R. S. (1987). Immunological properties of myosin light-chain kinases. Biochim. Biophys. Acta 914, 74-82.
14. DePina, A. S., Wollert, T. and Langford, G. M. (2007). Membrane associated nonmuscle myosin II functions as a motor for actin-based vesicle transport in clam oocyte extracts. Cell Motil. Cytoskeleton 64, 739-755.
15. DerMardirossian, C. and Bokoch, G. M. (2005). GDIs: central regulatory molecules in Rho GTPase activation. Trends Cell Biol. 15, 356-363.
16. Einheber, S., Hannocks, M. J., Metz, C. N., Rifkin, D. B. and Salzer, J. L. (1995). Transforming growth factor-beta 1 regulates axon/Schwann cell interactions. J. Cell Biol. 129, 443-458.
17. Gallagher, P. J., Herring, B. P. and Stull, J. T. (1997). Myosin light chain kinases. J. Muscle Res. Cell Motil. 18, 1-16.
18. Gould, R. M. and Mattingly, G. (1990). Regional localization of RNA and protein metabolism in Schwann cells in vivo. J. Neurocytol. 19, 285-301.
19. Hofmann, W. A., Stojiljkovic, L., Fuchsova, B., Vargas, G. M., Mavrommatis, E., Philimonenko, V., Kysela, K., Goodrich, J. A., Lessard, J. L., Hope, T. J. et al. (2004). Actin is part of pre-initiation complexes and is necessary for transcription by RNA polymerase II. Nat. Cell Biol. 6, 1094-1101.
20. Ihnatovych, I., Hu, W., Martin, J. L., Fazleabas, A. T., de Lanerolle, P. and Strakova, Z. (2007). Increased phosphorylation of myosin light chain prevents in vitro decidualization. Endocrinology 148, 3176-3184.
21. Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., Kominami, E., Ohsumi, Y. and Yoshimori, T. (2000). LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19, 5720-5728.
22. Kimura, K., Ito, M., Amano, M., Chihara, K., Fukata, Y., Nakafuku, M., Yamamori, B., Feng, J., Nakano, T., Okawa, K. et al. (1996). Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273, 245-248.
23. Kippert, A., Trajkovic, K., Rajendran, L., Ries, J. and Simons, M. (2007). Rho regulates membrane transport in the endocytic pathway to control plasma membrane specialization in oligodendroglial cells. J. Neurosci. 27, 3560-3570.
24. Kippert, A., Fitzner, D., Helenius, J. and Simons, M. (2009). Actomyosin contractility controls cell surface area of oligodendrocytes. BMC Cell Biol. 10, 71.
25. Lamb, N. J., Fernandez, A., Conti, M. A., Adelstein, R., Glass, D. B., Welch, W. J. and Feramisco, J. R. (1988). Regulation of actin microfilament integrity in living nonmuscle cells by the cAMP-dependent protein kinase and the myosin light chain kinase. J. Cell Biol. 106, 1955-1971.
26. Larocque, D., Fragoso, G., Huang, J., Mushynski, W. E., Loignon, M., Richard, S. and Almazan, G. (2009). The QKI-6 and QKI-7 RNA binding proteins block proliferation and promote Schwann cell myelination. PLoS One 4, e5867.
27. Latham, V. M., Yu, E. H., Tullio, A. N., Adelstein, R. S. and Singer, R. H. (2001). A Rhodependent signaling pathway operating through myosin localizes beta-actin mRNA in fibroblasts. Curr. Biol. 11, 1010-1016.
28. Li, Q. and Sarna, S. K. (2009). Nuclear myosin II regulates the assembly of preinitiation complex for ICAM-1 gene transcription. Gastroenterology 137, 1051-1060.
29. Maddala, R., Skiba, N. and Vasantha Rao, P. (2007). Lens fiber cell elongation and differentiation is associated with a robust increase in myosin light chain phosphorylation in the developing mouse. Differentiation 75, 713-725.
30. Marchiando, A. M., Shen, L., Graham, W. V., Weber, C. R., Schwarz, B. T., Austin, J. R., 2nd, Raleigh, D. R., Guan, Y., Watson, A. J., Montrose, M. H. et al. (2010). Caveolin-1-dependent occluding endocytosis is required for TNF-induced tight junction regulation in vivo. J. Cell Biol. 189, 111-126.
31. Melendez-Vasquez, C. V., Einheber, S. and Salzer, J. L. (2004). Rho kinase regulates Schwann cell myelination and formation of associated axonal domains. J. Neurosci. 24, 3953-3963.
32. Michailov, G. V., Sereda, M. W., Brinkmann, B. G., Fischer, T. M., Haug, B., Birchmeier, C., Role, L., Lai, C., Schwab, M. H. and Nave, K. A. (2004). Axonal neuregulin-1 regulates myelin sheath thickness. Science 304, 700-703.
33. Monje, P. V., Rendon, S., Athauda, G., Bates, M., Wood, P. M. and Bunge, M. B. (2009). Nonantagonistic relationship between mitogenic factors and cAMP in adult Schwann cell re-differentiation. Glia 57, 947-961.
34. Monje, P. V., Soto, J., Bacallao, K. and Wood, P. M. (2010). Schwann cell dedifferentiation is independent of mitogenic signaling and uncoupled to proliferation: role of cAMP and JNK in the maintenance of the differentiated state. J. Biol. Chem. 285, 31024-31036.
35. Monk, K. R., Naylor, S. G., Glenn, T. D., Mercurio, S., Perlin, J. R., Dominguez, C., Moens, C. B. and Talbot, W. S. (2009). A G protein-coupled receptor is essential for Schwann cells to initiate myelination. Science 325, 1402-1405.
36. Monuki, E. S., Weinmaster, G., Kuhn, R. and Lemke, G. (1989). SCIP: a glial POU domain gene regulated by cyclic AMP. Neuron 3, 783-793.
37. Morgan, L., Jessen, K. R. and Mirsky, R. (1991). The effects of cAMP on differentiation of cultured Schwann cells: progression from an early phenotype (04+) to a myelin phenotype (P0+, GFAP-, NCAM-, NGF-receptor-) depends on growth inhibition. J. Cell Biol. 112, 457-467.
38. Musch, A., Cohen, D. and Rodriguez-Boulan, E. (1997). Myosin II is involved in the production of constitutive transport vesicles from the TGN. J. Cell Biol. 138, 291-306.
39. Niemann, S., Sereda, M. W., Suter, U., Griffiths, I. R. and Nave, K. A. (2000). Uncoupling of myelin assembly and Schwann cell differentiation by transgenic overexpression of peripheral myelin protein 22. J. Neurosci. 20, 4120-4128.
40. Nodari, A., Zambroni, D., Quattrini, A., Court, F. A., D'Urso, A., Recchia, A., Tybulewicz, V. L., Wrabetz, L. and Feltri, M. L. (2007). Beta1 integrin activates Rac1 in Schwann cells to generate radial lamellae during axonal sorting and myelination. J. Cell Biol. 177, 1063-1075.
41. Notterpek, L., Shooter, E. M. and Snipes, G. J. (1997). Upregulation of the endosomal-lysosomal pathway in the trembler-J neuropathy. J. Neurosci. 17, 4190-4200.
42. Novak, N., Bar, V., Sabanay, H., Frechter, S., Jaegle, M., Snapper, S. B., Meijer, D. and Peles, E. (2011). N-WASP is required for membrane wrapping and myelination by Schwann cells. J. Cell Biol. 192, 243-250.
43. Parkinson, D. B., Bhaskaran, A., Droggiti, A., Dickinson, S., D'Antonio, M., Mirsky, R. and Jessen, K. R. (2004). Krox-20 inhibits Jun-NH2-terminal kinase/ c-Jun to control Schwann cell proliferation and death. J. Cell Biol. 164, 385-394.
44. Parkinson, D. B., Bhaskaran, A., Arthur-Farraj, P., Noon, L. A., Woodhoo, A., Lloyd, A. C., Feltri, M. L., Wrabetz, L., Behrens, A., Mirsky, R. et al. (2008). c-Jun is a negative regulator of myelination. J. Cell Biol. 181, 625-637.
45. Pedraza, L., Owens, G. C., Green, L. A. and Salzer, J. L. (1990). The myelinassociated glycoproteins: membrane disposition, evidence of a novel disulfide linkage between immunoglobulin-like domains, and posttranslational palmitylation. J. Cell Biol. 111, 2651-2661.
46. Pereira, J. A., Benninger, Y., Baumann, R., Goncalves, A. F., Ozcelik, M., Thurnherr, T., Tricaud, N., Meijer, D., Fassler, R., Suter, U. et al. (2009). Integrin-linked kinase is required for radial sorting of axons and Schwann cell remyelination in the peripheral nervous system. J. Cell Biol. 185, 147-161.
47. Philimonenko, V. V., Zhao, J., Iben, S., Dingova, H., Kysela, K., Kahle, M., Zentgraf, H., Hofmann, W. A., de Lanerolle, P., Hozak, P. et al. (2004). Nuclear actin and myosin I are required for RNA polymerase I transcription. Nat. Cell Biol. 6, 1165-1172.
48. Poperechnaya, A., Varlamova, O., Lin, P. J., Stull, J. T. and Bresnick, A. R. (2000). Localization and activity of myosin light chain kinase isoforms during the cell cycle. J. Cell Biol. 151, 697-708.
49. Ray, R. M., Guo, H., Patel, M., Jin, S., Bhattacharya, S. and Johnson, L. R. (2007). Role of myosin regulatory light chain and Rac1 in the migration of polyaminedepleted intestinal epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 292, G983-G995.
50. Rosenberg, S. S., Powell, B. L. and Chan, J. R. (2007). Receiving mixed signals: uncoupling oligodendrocyte differentiation and myelination. Cell Mol. Life Sci. 64, 3059-3068.
51. Sanders, L. C., Matsumura, F., Bokoch, G. M. and de Lanerolle, P. (1999). Inhibition of myosin light chain kinase by p21-activated kinase. Science 283, 2083-2085.
52. Scherer, S. S., Wang, D. Y., Kuhn, R., Lemke, G., Wrabetz, L. and Kamholz, J. (1994). Axons regulate Schwann cell expression of the POU transcription factor SCIP. J. Neurosci. 14, 1930-1942.
53. Sobue, G. and Pleasure, D. (1984). Schwann cell galactocerebroside induced by derivatives of adenosine 3′,5′-monophosphate. Science 224, 72-74.
54. Syed, N., Reddy, K., Yang, D. P., Taveggia, C., Salzer, J. L.,Maurel, P. and Kim, H. A. (2010). Soluble neuregulin-1 has bifunctional, concentration-dependent effects on Schwann cell myelination. J. Neurosci. 30, 6122-6131.
55. Taveggia, C., Zanazzi, G., Petrylak, A., Yano, H., Rosenbluth, J., Einheber, S., Xu, X., Esper, R. M., Loeb, J. A., Shrager, P. et al. (2005). Neuregulin-1 type III determines the ensheathment fate of axons. Neuron 47, 681-694.
56. Togo, T. and Steinhardt, R. A. (2004). Nonmuscle myosin IIA and IIB have distinct functions in the exocytosis-dependent process of cell membrane repair. Mol. Biol. Cell 15, 688-695.
57. Totsukawa, G., Yamakita, Y., Yamashiro, S., Hartshorne, D. J., Sasaki, Y. and Matsumura, F. (2000). Distinct roles of ROCK (Rho-kinase) and MLCK in spatial regulation of MLC phosphorylation for assembly of stress fibers and focal adhesions in 3T3 fibroblasts. J. Cell Biol. 150, 797-806.
58. Totsukawa, G., Wu, Y., Sasaki, Y., Hartshorne, D. J., Yamakita, Y., Yamashiro, S. and 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. Trapp, B. D., Kidd, G. J., Hauer, P., Mulrenin, E., Haney, C. A. and Andrews, S. B. (1995). Polarization of myelinating Schwann cell surface membranes: role of microtubules and the trans-Golgi network. J. Neurosci. 15, 1797-1807.
60. Wadgaonkar, R., Nurmukhambetova, S., Zaiman, A. L. and Garcia, J. G. (2003). Mutation analysis of the non-muscle myosin light chain kinase (MLCK) deletion constructs on CV1 fibroblast contractile activity and proliferation. J. Cell Biochem. 88, 623-634.
61. Wang, H., Tewari, A., Einheber, S., Salzer, J. L. and Melendez-Vasquez, C. V. (2008). Myosin II has distinct functions in PNS and CNS myelin sheath formation. J. Cell Biol. 182, 1171-1184.
62. Wolf, R. M., Wilkes, J. J., Chao, M. V. and Resh, M. D. (2001). Tyrosine phosphorylation of p190 RhoGAP by Fyn regulates oligodendrocyte differentiation. J. Neurobiol. 49, 62-78.
63. Xu, J., Gao, X. P., Ramchandran, R., Zhao, Y. Y., Vogel, S. M. and Malik, A. B. (2008). Nonmuscle myosin light-chain kinase mediates neutrophil transmigration in sepsis-induced lung inflammation by activating beta2 integrins. Nat. Immunol. 9, 880-886.
64. Yin, X., Kidd, G. J., Wrabetz, L., Feltri, M. L., Messing, A. and Trapp, B. D. (2000). Schwann cell myelination requires timely and precise targeting of P(0) protein. J. Cell Biol. 148, 1009-1020.
65. Yuen, T., Wurmbach, E., Pfeffer, R. L., Ebersole, B. J. and Sealfon, S. C. (2002a). Accuracy and calibration of commercial oligonucleotide and custom cDNA microarrays. Nucleic Acids Res. 30, e48.
66. Yuen, T., Zhang, W., Ebersole, B. J. and Sealfon, S. C. (2002b). Monitoring Gprotein-coupled receptor signaling with DNA microarrays and real-time polymerase chain reaction. Methods Enzymol. 345, 556-569.
67. Zalfa, F., Eleuteri, B., Dickson, K. S., Mercaldo, V., De Rubeis, S., di Penta, A., Tabolacci, E., Chiurazzi, P., Neri, G., Grant, S. G. et al. (2007). A new function for the fragile X mental retardation protein in regulation of PSD-95 mRNA stability. Nat. Neurosci. 10, 578-587.
68. Zanazzi, G., Einheber, S., Westreich, R., Hannocks, M. J., Bedell-Hogan, D., Marchionni, M. A. and Salzer, J. L. (2001). Glial growth factor/neuregulin inhibits Schwann cell myelination and induces demyelination. J. Cell Biol. 152, 1289-1299.