RhoA-ROCK-Myosin pathway regulates morphological plasticity of cultured olfactory ensheathing cells

Experimental Cell Research

Volumn 317, Issue 20, 2011, Pages 2823-2834

  Huang, Zhi hui ^a,b   Wang, Ying ^a,b   Yuan, Xiao bing ^c   He, Cheng ^a,b  

^a WENZHOU MEDICAL UNIVERSITY   (China)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

^c INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

Morphological plasticity; Myosin; Olfactory ensheathing cells; Regeneration; RhoA

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; COMPLEMENT COMPONENT C3; F ACTIN; LYSOPHOSPHATIDIC ACID; MYOSIN; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL CELL; ARTICLE; BIOSENSOR; CELL SHAPE; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVATION; MALE; NONHUMAN; OLFACTORY ENSHEATHING CELL; PLASTICITY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SIGNAL TRANSDUCTION;

EID: 82555165928     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2011.09.004     Document Type: Article

References (62)

1. Raisman G., Li Y. Repair of neural pathways by olfactory ensheathing cells. Nat. Rev. Neurosci. 2007, 8:312-319.
2. Franssen E.H., de Bree F.M., Verhaagen J. Olfactory ensheathing glia: their contribution to primary olfactory nervous system regeneration and their regenerative potential following transplantation into the injured spinal cord. Brain Res. Rev. 2007, 56:236-258.
3. Kato T., Honmou O., Uede T., Hashi K., Kocsis J.D. Transplantation of human olfactory ensheathing cells elicits remyelination of demyelinated rat spinal cord. Glia 2000, 30:209-218.
4. Li Y., Field P.M., Raisman G. Regeneration of adult rat corticospinal axons induced by transplanted olfactory ensheathing cells. J. Neurosci. 1998, 18:10514-10524.
5. Su Z., He C. Olfactory ensheathing cells: biology in neural development and regeneration. Prog. Neurobiol. 2010, 92:517-532.
6. Ramon-Cueto A., Munoz-Quiles C. Clinical application of adult olfactory bulb ensheathing glia for nervous system repair. Exp. Neurol. 2011, 229:181-194.
7. Mackay-Sim A., St John J.A. Olfactory ensheathing cells from the nose: clinical application in human spinal cord injuries. Exp. Neurol. 2011, 229:174-180.
8. Ramon-Cueto A., Nieto-Sampedro M. Glial cells from adult rat olfactory bulb: immunocytochemical properties of pure cultures of ensheathing cells. Neuroscience 1992, 47:213-220.
9. Au E., Roskams A.J. Olfactory ensheathing cells of the lamina propria in vivo and in vitro. Glia 2003, 41:224-236.
10. Franceschini I.A., Barnett S.C. Low-affinity NGF-receptor and E-N-CAM expression define two types of olfactory nerve ensheathing cells that share a common lineage. Dev. Biol. 1996, 173:327-343.
11. Pixley S.K. The olfactory nerve contains two populations of glia, identified both in vivo and in vitro. Glia 1992, 5:269-284.
12. Huang Z.H., Wang Y., Cao L., Su Z.D., Zhu Y.L., Chen Y.Z., Yuan X.B., He C. Migratory properties of cultured olfactory ensheathing cells by single-cell migration assay. Cell Res. 2008, 18:479-490.
13. Vincent A.J., West A.K., Chuah M.I. Morphological and functional plasticity of olfactory ensheathing cells. J. Neurocytol. 2005, 34:65-80.
14. Vincent A.J., West A.K., Chuah M.I. Morphological plasticity of olfactory ensheathing cells is regulated by cAMP and endothelin-1. Glia 2003, 41:393-403.
15. van den Pol A.N., Santarelli J.G. Olfactory ensheathing cells: time lapse imaging of cellular interactions, axonal support, rapid morphologic shifts, and mitosis. J. Comp. Neurol. 2003, 458:175-194.
16. Doucette R., Devon R. Elevated intracellular levels of cAMP induce olfactory ensheathing cells to express GAL-C and GFAP but not MBP. Glia 1995, 13:130-140.
17. Alexander C.L., Fitzgerald U.F., Barnett S.C. Identification of growth factors that promote long-term proliferation of olfactory ensheathing cells and modulate their antigenic phenotype. Glia 2002, 37:349-364.
18. Wang Y., Huang Z.H. cAMP mediates the morphological change of cultured olfactory ensheathing cells induced by serum. Sheng Li Xue Bao 2011, 63:31-38.
19. Tisay K.T., Key B. The extracellular matrix modulates olfactory neurite outgrowth on ensheathing cells. J. Neurosci. 1999, 19:9890-9899.
20. Vukovic J., Ruitenberg M.J., Roet K., Franssen E., Arulpragasam A., Sasaki T., Verhaagen J., Harvey A.R., Busfield S.J., Plant G.W. The glycoprotein fibulin-3 regulates morphology and motility of olfactory ensheathing cells in vitro. Glia 2009, 57:424-443.
21. Etienne-Manneville S., Hall A. Rho GTPases in cell biology. Nature 2002, 420:629-635.
22. DeMali K.A., Burridge K. Coupling membrane protrusion and cell adhesion. J. Cell Sci. 2003, 116:2389-2397.
23. Su Z., Cao L., Zhu Y., Liu X., Huang Z., Huang A., He C. Nogo enhances the adhesion of olfactory ensheathing cells and inhibits their migration. J. Cell Sci. 2007, 120:1877-1887.
24. Yan H., Lu D., Rivkees S.A. Lysophosphatidic acid regulates the proliferation and migration of olfactory ensheathing cells in vitro. Glia 2003, 44:26-36.
25. 2+-dependent cofilin activation and RhoA inhibition. J. Cell Sci. 2011, 124:186-197.
26. Barnett S.C., Roskams A.J. Olfactory ensheathing cells. Isolation and culture from the rat olfactory bulb. Methods Mol. Biol. 2002, 198:41-48.
27. Cao L., Su Z., Zhou Q., Lv B., Liu X., Jiao L., Li Z., Zhu Y., Huang Z., Huang A., He C. Glial cell line-derived neurotrophic factor promotes olfactory ensheathing cells migration. Glia 2006, 54:536-544.
28. Zhu Y., Cao L., Su Z., Mu L., Yuan Y., Gao L., Qiu Y., He C. Olfactory ensheathing cells: attractant of neural progenitor migration to olfactory bulb. Glia 2010, 58:716-729.
29. Cao L., Zhu Y.L., Su Z., Lv B., Huang Z., Mu L., He C. Olfactory ensheathing cells promote migration of Schwann cells by secreted nerve growth factor. Glia 2007, 55:897-904.
30. Yoshizaki H., Ohba Y., Kurokawa K., Itoh R.E., Nakamura T., Mochizuki N., Nagashima K., Matsuda M. Activity of Rho-family GTPases during cell division as visualized with FRET-based probes. J. Cell Biol. 2003, 162:223-232.
31. Feige J.N., Sage D., Wahli W., Desvergne B., Gelman L. PixFRET, an ImageJ plug-in for FRET calculation that can accommodate variations in spectral bleed-throughs. Microsc. Res. Tech. 2005, 68:51-58.
32. Fu G., Yang H.Y., Wang C., Zhang F., You Z.D., Wang G.Y., He C., Chen Y.Z., Xu Z.Z. Detection of constitutive heterodimerization of the integrin Mac-1 subunits by fluorescence resonance energy transfer in living cells. Biochem. Biophys. Res. Commun. 2006, 346:986-991.
33. Zhang F., Fu G., Wang C., Cao L., Yang H.Y., Wang G.Y., Chen Y.Z., He C. Detection of homo- or hetero-association of Doks by fluorescence resonance energy transfer in living cells. Mol. Imaging Biol. 2009, 11:188-194.
34. Guan C.B., Xu H.T., Jin M., Yuan X.B., Poo M.M. Long-range Ca(2+) signaling from growth cone to soma mediates reversal of neuronal migration induced by slit-2. Cell 2007, 129:385-395.
35. Bhadriraju K., Yang M., Alom Ruiz S., Pirone D., Tan J., Chen C.S. Activation of ROCK by RhoA is regulated by cell adhesion, shape, and cytoskeletal tension. Exp. Cell Res. 2007, 313:3616-3623.
36. Samaniego R., Sanchez-Martin L., Estecha A., Sanchez-Mateos P. Rho/ROCK and myosin II control the polarized distribution of endocytic clathrin structures at the uropod of moving T lymphocytes. J. Cell Sci. 2007, 120:3534-3543.
37. Ridley A.J., Schwartz M.A., Burridge K., Firtel R.A., Ginsberg M.H., Borisy G., Parsons J.T., Horwitz A.R. Cell migration: integrating signals from front to back. Science 2003, 302:1704-1709.
38. Totsukawa G., Yamakita Y., Yamashiro S., Hartshorne D.J., Sasaki Y., Matsumura F. 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. 2000, 150:797-806.
39. Yoneda A., Multhaupt H.A., Couchman J.R. The Rho kinases I and II regulate different aspects of myosin II activity. J. Cell Biol. 2005, 170:443-453.
40. Minambres R., Guasch R.M., Perez-Arago A., Guerri C. The RhoA/ROCK-I/MLC pathway is involved in the ethanol-induced apoptosis by anoikis in astrocytes. J. Cell Sci. 2006, 119:271-282.
41. Franklin R.J., Gilson J.M., Franceschini I.A., Barnett S.C. Schwann cell-like myelination following transplantation of an olfactory bulb-ensheathing cell line into areas of demyelination in the adult CNS. Glia 1996, 17:217-224.
42. Li Y., Decherchi P., Raisman G. Transplantation of olfactory ensheathing cells into spinal cord lesions restores breathing and climbing. J. Neurosci. 2003, 23:727-731.
43. Kurokawa K., Matsuda M. Localized RhoA activation as a requirement for the induction of membrane ruffling. Mol. Biol. Cell 2005, 16:4294-4303.
44. Pertz O., Hodgson L., Klemke R.L., Hahn K.M. Spatiotemporal dynamics of RhoA activity in migrating cells. Nature 2006, 440:1069-1072.
45. Hirose M., Ishizaki T., Watanabe N., Uehata M., Kranenburg O., Moolenaar W.H., Matsumura F., Maekawa M., Bito H., Narumiya S. Molecular dissection of the Rho-associated protein kinase (p160ROCK)-regulated neurite remodeling in neuroblastoma N1E-115 cells. J. Cell Biol. 1998, 141:1625-1636.
46. Jalink K., van Corven E.J., Hengeveld T., Morii N., Narumiya S., Moolenaar W.H. Inhibition of lysophosphatidate- and thrombin-induced neurite retraction and neuronal cell rounding by ADP ribosylation of the small GTP-binding protein Rho. J. Cell Biol. 1994, 126:801-810.
47. Kranenburg O., Poland M., van Horck F.P., Drechsel D., Hall A., Moolenaar W.H. Activation of RhoA by lysophosphatidic acid and Galpha12/13 subunits in neuronal cells: induction of neurite retraction. Mol. Biol. Cell 1999, 10:1851-1857.
48. Ramakers G.J., Moolenaar W.H. Regulation of astrocyte morphology by RhoA and lysophosphatidic acid. Exp. Cell Res. 1998, 245:252-262.
49. Chen C.J., Ou Y.C., Lin S.Y., Liao S.L., Huang Y.S., Chiang A.N. L-glutamate activates RhoA GTPase leading to suppression of astrocyte stellation. Eur. J. Neurosci. 2006, 23:1977-1987.
50. Burgos M., Calvo S., Molina F., Vaquero C.F., Samarel A., Llopis J., Tranque P. PKCepsilon induces astrocyte stellation by modulating multiple cytoskeletal proteins and interacting with Rho A signalling pathways: implications for neuroinflammation. Eur. J. Neurosci. 2007, 25:1069-1078.
51. Goldman J.E., Abramson B. Cyclic AMP-induced shape changes of astrocytes are accompanied by rapid depolymerization of actin. Brain Res. 1990, 528:189-196.
52. Safavi-Abbasi S., Wolff J.R., Missler M. Rapid morphological changes in astrocytes are accompanied by redistribution but not by quantitative changes of cytoskeletal proteins. Glia 2001, 36:102-115.
53. Lim S.M., Kreipe B.A., Trzeciakowski J., Dangott L., Trache A. Extracellular matrix effect on RhoA signaling modulation in vascular smooth muscle cells. Exp. Cell Res. 2010, 316:2833-2848.
54. Hall A. Rho GTPases and the actin cytoskeleton. Science 1998, 279:509-514.
55. Ridley A.J. Rho GTPases and cell migration. J. Cell Sci. 2001, 114:2713-2722.
56. Munoz-Quiles C., Santos-Benito F.F., Llamusi M.B., Ramon-Cueto A. Chronic spinal injury repair by olfactory bulb ensheathing glia and feasibility for autologous therapy. J. Neuropathol. Exp. Neurol. 2009, 68:1294-1308.
57. Kumar R., Hayat S., Felts P., Bunting S., Wigley C. Functional differences and interactions between phenotypic subpopulations of olfactory ensheathing cells in promoting CNS axonal regeneration. Glia 2005, 50:12-20.
58. Devon R., Doucette R. Olfactory ensheathing cells myelinate dorsal root ganglion neurites. Brain Res. 1992, 589:175-179.
59. Ramon-Cueto A., Perez J., Nieto-Sampedro M. In vitro enfolding of olfactory neurites by p75 NGF receptor positive ensheathing cells from adult rat olfactory bulb. Eur. J. Neurosci. 1993, 5:1172-1180.
60. Kocsis J.D., Lankford K.L., Sasaki M., Radtke C. Unique in vivo properties of olfactory ensheathing cells that may contribute to neural repair and protection following spinal cord injury. Neurosci. Lett. 2009, 456:137-142.
61. Perez-Bouza A., Wigley C.B., Nacimiento W., Noth J., Brook G.A. Spontaneous orientation of transplanted olfactory glia influences axonal regeneration. Neuroreport 1998, 9:2971-2975.
62. Sonigra R.J., Brighton P.C., Jacoby J., Hall S., Wigley C.B. Adult rat olfactory nerve ensheathing cells are effective promoters of adult central nervous system neurite outgrowth in coculture. Glia 1999, 25:256-269.