Shape change controls supporting cell proliferation in lesioned mammalian balance epithelium

Journal of Neuroscience

Volumn 27, Issue 16, 2007, Pages 4313-4325

  Meyers, Jason R ^a,b   Corwin, Jeffrey T ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Cytoskeleton; Hair cell; LPA; Lysophosphatidic acid; Regeneration; Vestibular; Wound healing

Indexed keywords

ACTIN; LYSOPHOSPHATIDIC ACID; RHO FACTOR; RHO KINASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CYCLE S PHASE; CELL DAMAGE; CELL MATURATION; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; CYTOSKELETON; EMBRYO; EPITHELIUM; HAIR CELL; MAMMAL; MICROSCOPY; MOUSE; NEUROEPITHELIUM; NONHUMAN; PRIORITY JOURNAL; STIMULATION; UTRICLE; VESTIBULAR DISORDER; WOUND HEALING;

ACTINS; ANIMALS; CELL PROLIFERATION; CELL SHAPE; MICE; MUSCULOSKELETAL EQUILIBRIUM; ORGAN CULTURE TECHNIQUES; REGENERATION; SACCULE AND UTRICLE; WOUND HEALING;

EID: 34247391143     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5023-06.2007     Document Type: Article

References (67)

1. Balazs L, Okolicany J, Ferrebee M, Tigyi G (2000) Topical application of LPA accelerates wound healing. Ann NY Acad Sci 905:270-273.
2. Bement WM, Forscher P, Mooseker MS (1993) A novel cytoskeletal structure involved in purse string wound closure and cell polarity maintenance. J Cell Biol 121:565-578.
3. Bement WM, Mandato CA, Kirsch MN (1999) Wound-induced assembly and closure of an actomyosin purse string in Xenopus oocytes. Curr Biol 9:579-587.
4. Brock J, Midwinter K, Lewis J, Martin P (1996) Healing of incisional wounds in the embryonic chick wing bud: characterization of the actin purse-string and demonstration of a requirement for Rho activation. J Cell Biol 135:1097-1107.
5. Chen CS, Mrksich M, Huang S, Whitesides GM, Ingber DE (1997) Geometric control of cell life and death. Science 276:1425-1428.
6. Chen P, Segil N (1999) p27(Kip1) links cell proliferation to morphogenesis in the developing organ of Corti. Development 126:1581-1590.
7. Chen P, Zindy F, Abdala C, Liu F, Li X, Roussel MF, Segil N (2003) Progressive hearing loss in mice lacking the cyclin-dependent kinase inhibitor Ink4d. Nat Cell Biol 5:422-426.
8. Cook TA, Nagasaki T, GundersenGG (1998) Rho guanosine triphosphatase mediates the selective stabilization of microtubules induced by lysophosphatidic acid. J Cell Biol 141:175-185.
9. Corwin JT, Jones JE, Katayama A, Kelley MW, Warchol ME (1991) Hair cell regeneration: the identities of progenitor cells, potential triggers and instructive cues. Ciba Found Symp 160:103-120; discussion 120-130.
10. Corwin JT, Warchol ME, Saffer LD, Finley JE, Gu R, Lamber PR (1996) Growth factors as potential drugs for the sensory epithelia of the ear. Ciba Found Symp 196:167-182; discussion 182-167.
11. Cotanche DA (1987) Regeneration of hair cell stereociliary bundles in the chick cochlea following severe acoustic trauma. Hear Res 30:181-195.
12. Cotanche DA, Dopyera CE (1990) Hair cell and supporting cell response to acoustic trauma in the chick cochlea. Hear Res 46:29-40.
13. Danjo Y, Gipson IK (1998) Actin "purse string" filaments are anchored by E-cadherin-mediated adherens junctions at the leading edge of the epithelial wound, providing coordinated cell movement. J Cell Sci 111:3323-3332.
14. Davies D, Magnus C, Corwin JT (2007) Developmental changes in cell-extracellular matrix interactions limit proliferation in the mammalian inner ear. Eur J Neurosci 25:985-998.
15. Davies SP, Reddy H, Caivano M, Cohen P (2000) Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351:95-105.
16. Desai SS, Zeh C, Lysakowski A (2005) Comparative morphology of rodent vestibular periphery. I. Saccular and utricular maculae. J Neurophysiol 93:251-266.
17. Eichholtz T, Jalink K, Fahrenfort I, Moolenaar WH (1993) The bioactive phospholipid lysophosphatidic acid is released from activated platelets. Biochem J 291:677-680.
18. Folkman J, Moscona A (1978) Role of cell shape in growth control. Nature 273:345-349.
19. Fringer J, Grinnell F (2001) Fibroblast quiescence in floating or released collagen matrices: contribution of the ERK signaling pathway and actin cytoskeletal organization. J Biol Chem 276:31047-31052.
20. Furuse M, Hirase T, Itoh M, Nagafuchi A, Yonemura S, Tsukita S (1993) Occludin: a novel integral membrane protein localizing at tight junctions. J Cell Biol 123:1777-1788.
21. Gale JE, Meyers JR, Periasamy A, Corwin JT (2002) Survival of bundleless hair cells and subsequent bundle replacement in the bullfrog's saccule. J Neurobiol 50:81-92.
22. Gu R, Marchionni M, Corwin JT (1996) Glial growth factor enhances supporting cell proliferation in rodent vestibular epithelia cultured in isolation. Soc Neurosci Abstr 21:520.
23. Gu R, Marchionni M, Corwin JT (1997) Age-related decreases in proliferation within isolated mammalian vestibular epithelia cultured in control and glial growth factor 2 medium. Assoc Res Otolaryngol Abstr 20:98.
24. Gu R, Montcouquiol M, Marchionni M, Corwin JT (2007) Proliferative responses to growth factors decline rapidly during postnatal maturation of mammalian hair cell epithelia. Eur J Neurosci 25:1363-1372.
25. Hadjantonakis AK, Gertsenstein M, Ikawa M, Okabe M, Nagy A (1998) Generating green fluorescent mice by germline transmission of green fluorescent ES cells. Mech Dev 76:79-90.
26. Hatten ME (1985) Neuronal regulation of astroglial morphology and proliferation in vitro. J Cell Biol 100:384-396.
27. Heath JP (1996) Epithelial cell migration in the intestine. Cell Biol Int 20:139-146.
28. Hirose M, Ishizaki T, Watanabe N, Uehata M, Kranenburg O, Moolenaar WH, Matsumura F, Maekawa M, Bito H, Narumiya S (1998) Molecular dissection of the Rho-associated protein kinase (p160ROCK)-regulated neurite remodeling in neuroblastoma N1E-115 cells. J Cell Biol 141:1625-1636.
29. Huang S, Chen CS, Ingber DE (1998) Control of cyclin D1, p27(Kip1), and cell cycle progression in human capillary endothelial cells by cell shape and cytoskeletal tension. Mol Biol Cell 9:3179-3193.
30. Hume CR, Kirkegaard M, Oesterle EC (2003) ErbB expression: the mouse inner ear and maturation of the mitogenic response to heregulin. J Assoc Res Otolaryngol 4:422-443.
31. Ihara S, Motobayashi Y (1992) Wound closure in foetal rat skin. Development 114:573-582.
32. Jacinto A, Martinez-Arias A, Martin P (2001) Mechanisms of epithelial fusion and repair. Nat Cell Biol 3:E117-E123.
33. Kelley RO, Dekker RA, Bluemink JG (1973) Ligand-mediated osmium binding: its application in coating biological specimens for scanning electron microscopy. J Ultrastruct Res 45:254-258.
34. Kranenburg O, Poland M, van Horck FP, Drechsel D, Hall A, Moolenaar WH (1999) Activation of RhoA by lysophosphatidic acid and Galpha12/13 subunits in neuronal cells: induction of neurite retraction. Mol Biol Cell 10:1851-1857.
35. Lambert PR (1994) Inner ear hair cell regeneration in a mammal: identification of a triggering factor. Laryngoscope 104:701-718.
36. Lee H, Goetzl EJ, An S (2000) Lysophosphatidic acid and sphingosine 1-phosphate stimulate endothelial cell wound healing. Am J Physiol Cell Physiol 278:C612-C618.
37. Li L, Forge A (1997) Morphological evidence for supporting cell to hair cell conversion in the mammalian utricular macula. Int J Dev Neurosci 15:433-446.
38. Lowenheim H, Furness DN, Kil J, Zinn C, Gultig K, Fero ML, Frost D, Gummer AW, Roberts JM, Rubel EW, Hackney CM, Zenner HP (1999) Gene disruption of p27(Kip1) allows cell proliferation in the postnatal and adult organ of corti. Proc Natl Acad Sci USA 96:4084-4088.
39. Malick LE, Wilson RB (1975) Modified thiocarbohydrazide procedure for scanning electron microscopy: routine use for normal, pathological, or experimental tissues. Stain Technol 50:265-269.
40. Mammoto A, Huang S, Moore K, Oh P, Ingber DE (2004) Role of RhoA, mDia, and ROCK in cell shape-dependent control of the Skp2-p27kip1 pathway and the G1/S transition. J Biol Chem 279:26323-26330.
41. Marsh RR, Xu LR, Moy JP, Saunders JC (1990) Recovery of the basilar papilla following intense sound exposure in the chick. Hear Res 46:229-237.
42. Martin P, Lewis J (1992) Actin cables and epidermal movement in embryonic wound healing. Nature 360:179-183.
43. Meiteles LZ, Raphael Y (1994) Scar formation in the vestibular sensory epithelium after aminoglycoside toxicity. Hear Res 79:26-38.
44. Montcouquiol M, Corwin JT (2001a) Intracellular signals that control cell proliferation in mammalian balance epithelia: key roles for phosphatidylinositol-3 kinase, mammalian target of rapamycin, and S6 kinases in preference to calcium, protein kinase C, and mitogen-activated protein kinase. J Neurosci 21:570-580.
45. Montcouquiol M, Corwin JT (2001b) Brief treatments with forskolin enhance S-phase entry in balance epithelia from the ears of rats. J Neurosci 21:974-982.
46. Moolenaar WH (1999) Bioactive lysophospholipids and their G proteincoupled receptors. Exp Cell Res 253:230-238.
47. Nodder S, Martin P (1997) Wound healing in embryos: a review. Anat Embryol (Berl) 195:215-228.
48. Palazzo AF, Cook TA, Alberts AS, Gundersen GG (2001) mDia mediates Rho-regulated formation and orientation of stable microtubules. Nat Cell Biol 3:723-729.
49. Parizi M, Howard EW, Tomasek JJ (2000) Regulation of LPA-promoted myofibroblast contraction: role of Rho, myosin light chain kinase, and myosin light chain phosphatase. Exp Cell Res 254:210-220.
50. Ramakers GJ, Moolenaar WH (1998) Regulation of astrocyte morphology by RhoA and lysophosphatidic acid. Exp Cell Res 245:252-262.
51. Raphael Y, Altschuler RA (1991) Scar formation after drug-induced cochlear insult. Hear Res 51:173-183.
52. Redd MJ, Cooper L, Wood W, Stramer B, Martin P (2004) Wound healing and inflammation: embryos reveal the way to perfect repair. Philos Trans R Soc Lond B Biol Sci 359:777-784.
53. Rogers JH (1989) Two calcium-binding proteins mark many chick sensory neurons. Neuroscience 31:697-709.
54. Roovers K, Klein EA, Castagnino P, Assoian RK (2003) Nuclear translocation of LIM kinase mediates Rho-Rho kinase regulation of cyclin D1 expression. Dev Cell 5:273-284.
55. Sage C, Huang M, Karimi K, Gutierrez G, Vollrath MA, Zhang DS, Garcia-Anoveros J, Hinds PW, Corwin JT, Corey DP, Chen ZY (2005) Proliferation of functional hair cells in vivo in the absence of the retinoblastoma protein. Science 307:1114-1118.
56. Saitoh M, Ishikawa T, Matsushima S, Naka M, Hidaka H (1987) Selective inhibition of catalytic activity of smooth muscle myosin light chain kinase. J Biol Chem 262:7796-7801.
57. Sturm A, Sudermann T, Schulte KM, Goebell H, Dignass AU (1999) Modulation of intestinal epithelial wound healing in vitro and in vivo by lysophosphatidic acid. Gastroenterology 117:368-377.
58. Warchol ME (1995) Supporting cells in isolated sensory epithelia of avian utricles proliferate in serum-free culture. NeuroReport 6:981-984.
59. Warchol ME (2002) Cell density and N-cadherin interactions regulate cell proliferation in the sensory epithelia of the inner ear. J Neurosci 22:2607-2616.
60. Warchol ME, Lambert PR, Goldstein BJ, Forge A, Corwin JT (1993) Regenerative proliferation in inner ear sensory epithelia from adult guinea pigs and humans. Science 259:1619-1622.
61. Wersäll J, Flock A (1965) Functional anatomy of the vestibular and lateral line organs. Contrib Sens Physiol 14:39-61.
62. White PM, Doetzlhofer A, Lee YS, Groves AK, Segil N (2006) Mammalian cochlear supporting cells can divide and trans-differentiate into hair cells. Nature 441:984-987.
63. Witte MC, Montcouquiol M, Corwin JT (2001) Regeneration in avian hair cell epithelia: identification of intracellular signals required for S-phase entry. Eur J Neurosci 14:829-838.
64. Wood W, Jacinto A, Grose R, Woolner S, Gale J, Wilson C, Martin P (2002) Wound healing recapitulates morphogenesis in Drosophila embryos. Nat Cell Biol 4:907-912.
65. Woolley K, Martin P (2000) Conserved mechanisms of repair: from damaged single cells to wounds in multicellular tissues. BioEssays 22:911-919.
66. Zhang XF, Schaefer AW, Burnette DT, Schoonderwoert VT, Forscher P (2003) Rho-dependent contractile responses in the neuronal growth cone are independent of classical peripheral retrograde actin flow. Neuron 40:931-944.
67. Zheng JL, Helbig C, Gao WQ (1997) Induction of cell proliferation by fibroblast and insulin-like growth factors in pure rat inner ear epithelial cell cultures. J Neurosci 17:216-226.