cAMP-induced auditory supporting cell proliferation is mediated by ERK MAPK signaling pathway

JARO - Journal of the Association for Research in Otolaryngology

Volumn 11, Issue 2, 2010, Pages 173-185

  Bell, Thomas J ^a   Oberholtzer, John Carl ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Auditory hair cells; CAMP; ERK; Supporting cells

Indexed keywords

B RAF KINASE; BROXURIDINE; CYCLIC AMP; FORSKOLIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUDITORY SUPPORTING CELL; AUDITORY SYSTEM; CELL PROLIFERATION; CONTROLLED STUDY; EPITHELIUM; FOWL; HAIR CELL; IMMUNOHISTOCHEMISTRY; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; ANTIMETABOLITES; APIGENIN; BIRDS; BROMODEOXYURIDINE; BUTADIENES; CELL DIVISION; CYCLIC AMP; ENZYME INHIBITORS; EPITHELIAL CELLS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FLAVONOIDS; FORSKOLIN; HAIR CELLS, AUDITORY; MACROLIDES; MAP KINASE SIGNALING SYSTEM; MYOSINS; NITRILES; ORGAN CULTURE TECHNIQUES; ORGAN OF CORTI; PROTO-ONCOGENE PROTEINS B-RAF;

EID: 77954760017     PISSN: 15253961     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10162-009-0205-8     Document Type: Article

References (52)

1. ADLER HJ, POJE CP, SAUNDERS JC (1993) Recovery of auditory function and structure in the chick after two intense pure tone exposures. Hear Res 71:214-224.
2. ALESSI DR, CUENDA A, COHEN P, DUDLEY DT, SALTIEL AR (1995) PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J Biol Chem 270:27489-27494.
3. BAROVSKY K, PEDONE C, BROOKER G (1983) Forskolin-stimulated cyclic AMP accumulation mediates protein synthesis-dependent refractoriness in C6-2B rat glioma cells. J Cyclic Nucleotide Protein Phosphor Res 9:181-189.
4. BERMINGHAM-MCDONOGH O, RUBEL EW (2003) Hair cell regeneration: winging our way towards a sound future. Curr Opin Neurobiol 13:119-126.
5. BERMINGHAM-MCDONOGH O, STONE JS, REH TA, RUBEL EW (2001) FGFR3 expression during development and regeneration of the chick inner ear sensory epithelia. Dev Biol 238:247-259.
6. BHAVE SA, STONE JS, RUBEL EW, COLTRERA MD (1995) Cell cycle progression in gentamicin-damaged avian cochleas. J Neurosci 15:4618-4628.
7. BRIGNULL HR, RAIBLE DW, STONE JS (2009) Feathers and fins: non-mammalian models for hair cell regeneration. Brain Res 1277:12-23.
8. CHEN P, SEGIL N (1999) p27(Kip1) links cell proliferation to morphogenesis in the developing organ of Corti. Development 126:1581-1590.
9. CORWIN JT, COTANCHE DA (1988) Regeneration of sensory hair cells after acoustic trauma. Science 240:1772-1774.
10. CORWIN JT, OBERHOLTZER JC (1997) Fish n' chicks: model recipes for hair-cell regeneration? Neuron 19:951-954.
11. COTANCHE DA (1997) Hair cell regeneration in the avian cochlea. Ann Otol Rhinol Laryngol Suppl 168:9-15.
12. COTANCHE DA, SAUNDERS JC, TILNEY LG (1987) Hair cell damage produced by acoustic trauma in the chick cochlea. Hear Res 25:267-286.
13. CRUZ RM, LAMBERT PR, RUBEL EW (1987) Light microscopic evidence of hair cell regeneration after gentamicin toxicity in chick cochlea. Arch Otolaryngol Head Neck Surg 113:1058-1062.
14. DE ROOIJ J, ZWARTKRUIS FJ, VERHEIJEN MH, COOL RH, NIJMAN SM, WITTINGHOFER A, BOS JL (1998) Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 396:474-477.
15. DE ROOIJ J, REHMANN H, VAN TRIEST M, COOL RH, WITTINGHOFER A, BOS JL (2000) Mechanism of regulation of the Epac family of cAMP-dependent RapGEFs. J Biol Chem 275:20829-20836.
16. DERKINDEREN P, ENSLEN H, GIRAULT JA (1999) The ERK/MAP-kinases cascade in the nervous system. Neuroreport 10:R24-R34.
17. DUGAN LL, KIM JS, ZHANG Y, BART RD, SUN Y, HOLTZMAN DM, GUTMANN DH (1999) Differential effects of cAMP in neurons and astrocytes. Role of B-raf. J Biol Chem 274:25842-25848.
18. DUMAZ N, MARAIS R (2005) Integrating signals between cAMP and the RAS/RAF/MEK/ERK signalling pathways. Based on the anniversary prize of the Gesellschaft fur Biochemie und Molekularbiologie Lecture delivered on 5 July 2003 at the Special FEBS Meeting in Brussels. Febs J 272:3491-3504.
19. EDGE AS, CHEN ZY (2008) Hair cell regeneration. Curr Opin Neurobiol 18:377-382.
20. FAVATA MF, HORIUCHI KY, MANOS EJ, DAULERIO AJ, STRADLEY DA, FEESER WS, VAN DYK DE, PITTS WJ, EARL RA, HOBBS F ET AL (1998) Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J Biol Chem 273:18623-18632.
21. HAGEMANN C, RAPP UR (1999) Isotype-specific functions of Raf kinases. Exp Cell Res 253:34-46.
22. HASSON T, HEINTZELMAN MB, SANTOS-SACCHI J, COREY DP, MOOSEKER MS (1995) Expression in cochlea and retina of myosin VIIa, the gene product defective in Usher syndrome type 1B. Proc Natl Acad Sci USA 92:9815-9819.
23. HENNIG AK, COTANCHE DA (1998) Regeneration of cochlear efferent nerve terminals after gentamycin damage. J Neurosci 18 (9):3282-3296.
24. KAWASAKI H, SPRINGETT GM, MOCHIZUKI N, TOKI S, NAKAYA M, MATSUDA M, HOUSMAN DE, GRAYBIEL AM (1998) A family of cAMP-binding proteins that directly activate Rap1. Science 282:2275-2279.
25. KUNTZ AL, OESTERLE EC (1998) Transforming growth factor-alpha with insulin induces proliferation in rat utricular extrasensory epithelia. Otolaryngol Head Neck Surg 118:816-824.
26. KUO ML, YANG NC (1995) Reversion of v-H-ras-transformed NIH 3T3 cells by apigenin through inhibiting mitogen activated protein kinase and its downstream oncogenes. Biochem Biophys Res Commun 212:767-775.
27. LABARCA C, PAIGEN K (1980) A simple, rapid, and sensitive DNA assay procedure. Anal Biochem 102(2):344-352.
28. LAMBERT PR (1994) Inner ear hair cell regeneration in a mammal: identification of a triggering factor. Laryngoscope 104:701-718.
29. LAURENZA A, SUTKOWSKI EM, SEAMON KB (1989) Forskolin: a specific stimulator of adenylyl cyclase or a diterpene with multiple sites of action? Trends Pharmacol Sci 10:442-447.
30. MCFADDEN EA, SAUNDERS JC (1989) Recovery of auditory function following intense sound exposure in the neonatal chick. Hear Res 41:205-215.
31. MONTCOUQUIOL M, CORWIN JT (2001A) Brief treatments with forskolin enhance s-phase entry in balance epithelia from the ears of rats. J Neurosci 21:974-982.
32. MONTCOUQUIOL M, CORWIN JT (2001B) 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.
33. MORICE C, NOTHIAS F, KONIG S, VERNIER P, BACCARINI M, VINCENT JD, BARNIER JV (1999) Raf-1 and B-Raf proteins have similar regional distributions but differential subcellular localization in adult rat brain. Eur J Neurosci 11:1995-2006.
34. NAVARATNAM DS, SU HS, SCOTT SP, OBERHOLTZER JC (1996) Proliferation in the auditory receptor epithelium mediated by a cyclic AMP-dependent signaling pathway. Nat Med 2:1136-1139.
35. PETER ME, HALL C, RÜHLMANN A, SANCHO J, TERHORST C (1992) The T-cell receptor zeta chain contains a GTP/GDP binding site. EMBO J 11(3):933-941.
36. 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.
37. SEAMON KB, DALY JW (1986) Forskolin: its biological and chemical properties. Adv Cyclic Nucleotide Protein Phosphorylation Res 20:1-150.
38. SHEN S, WIEMELT AP, MCMORRIS FA, BARRES BA (1999) Retinal ganglion cells lose trophic responsiveness after axotomy. Neuron 23:285-295.
39. SOGA S, KOZAWA T, NARUMI H, AKINAGA S, IRIE K, MATSUMOTO K, SHARMA SV, NAKANO H, MIZUKAMI T, HARA M (1998) Radicicol leads to selective depletion of Raf kinase and disrupts K-Ras-activated aberrant signaling pathway. J Biol Chem 273:822-828.
40. STONE JS, COTANCHE DA (2007) Hair cell regeneration in the avian auditory epithelium. Int J Dev Biol 51:633-647.
41. STONE JS, SHANG JL, TOMAREV S (2004) cProx1 immunoreactivity distinguishes progenitor cells and predicts hair cell fate during avian hair cell regeneration. Dev Dyn 230:597-614.
42. STORK PJ (2003) Does Rap1 deserve a bad Rap? Trends Biochem Sci 28:267-275.
43. TILNEY LG, TILNEY MS, SAUNDERS JS, DEROSIER DJ (1986) Actin filaments, stereocilia, and hair cells of the bird cochlea. III. The development and differentiation of hair cells and stereocilia. Dev Biol 116:100-118.
44. TUCCI DL, RUBEL EW (1990) Physiologic status of regenerated hair cells in the avian inner ear following aminoglycoside ototoxicity. Otolaryngol Head Neck Surg 103:443-450.
45. VOSSLER MR, YAO H, YORK RD, PAN MG, RIM CS, STORK PJ (1997) cAMP activates MAP kinase and Elk-1 through a B-Raf- and Rap1-dependent pathway. Cell 89:73-82.
46. WARCHOL ME, CORWIN JT (1996) Regenerative proliferation in organ cultures of the avian cochlea: identification of the initial progenitors and determination of the latency of the proliferative response. J Neurosci 16:5466-5477.
47. WIDMANN C, GIBSON S, JARPE MB, JOHNSON GL (1999) Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev 79:143-180.
48. WIEMELT AP, ENGLEKA MJ, SKORUPA AF, MCMORRIS FA (1997) Immunochemical visualization and quantitation of cyclic AMP in single cells. J Biol Chem 272:31489-31495.
49. 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.
50. YAMASHITA H, OESTERLE EC (1995) Induction of cell proliferation in mammalian inner-ear sensory epithelia by transforming growth factor alpha and epidermal growth factor. Proc Natl Acad Sci USA 92:3152-3155.
51. YORK RD, YAO H, DILLON T, ELLIG CL, ECKERT SP, MCCLESKEY EW, STORK PJ (1998) Rap1 mediates sustained MAP kinase activation induced by nerve growth factor. Nature 392:622-626.
52. 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.