Mature mice lacking Rbl2/p130 gene have supernumerary inner ear hair cells and supporting cells

Journal of Neuroscience

Volumn 31, Issue 24, 2011, Pages 8883-8893

  Rocha Sanchez, Sonia M ^a   Scheetz, Laura R ^a   Contreras, Melissa ^a   Weston, Michael D ^a   Korte, Megan ^b   McGee, JoAnn ^b   Walsh, Edward J ^b  

^a CREIGHTON UNIVERSITY SCHOOL OF DENTISTRY   (United States)

^b BOYS TOWN NATIONAL RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; PROTEIN P107; PROTEIN P130; PROTEIN RB1; RETINOBLASTOMA PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; COCHLEA; CONTROLLED STUDY; CORTI ORGAN; DOWN REGULATION; FEMALE; GENE DELETION; HAIR CELL; INNER EAR; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ACOUSTIC STIMULATION; AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; CELL PROLIFERATION; EAR, INNER; EMBRYO, MAMMALIAN; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HAIR CELLS, AUDITORY, INNER; IMMUNOPRECIPITATION; LABYRINTH SUPPORTING CELLS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOSINS; OTOACOUSTIC EMISSIONS, SPONTANEOUS; RECEPTORS, NERVE GROWTH FACTOR; RETINOBLASTOMA PROTEIN; SOXB1 TRANSCRIPTION FACTORS; TUBULIN;

EID: 79959324887     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5821-10.2011     Document Type: Article

References (48)

1. Burkhart DL, Sage J (2008) Cellular mechanisms of tumor suppression by the retinoblastoma gene. Nat Rev Cancer 8:671-682.
2. Cafaro J, Lee GS, Stone JS (2007) Atoh1 expression defines activated progenitors and differentiating hair cells during avian hair cell regeneration. Dev Dyn 236:156-170.
3. Calvisi DF, Ladu S, Pinna F, Frau M, Tomasi ML, Sini M, Simile MM, Bonelli P, Muroni MR, Seddaiu MA, Lim DS, Feo F, Pascale RM (2009) SKP2 and CKS1 promote degradation of cell cycle regulators and are associated with hepatocellular carcinoma prognosis. Gastroenterology 137:1816-1826.e1-10.
4. Chen P, Segil N (1999) p27(Kip1) links cell proliferation to morphogenesis in the developing organ of Corti. Development 126:1581-1590.
5. 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.
6. Choi HH, Jong HS, Hyun Song S, You Kim T, Kyeong Kim N, Bang YJ (2002) p130 mediates TGF-beta-induced cell-cycle arrest in Rb1 mutant HT-3 cells. Gynecol Oncol 86:184-189.
7. Cobrinik D (2005) Pocket proteins and cell cycle control. Oncogene 24:2796-2809.
8. Cobrinik D, Lee MH, Hannon G, Mulligan G, Bronson RT, Dyson N, Harlow E, Beach D, Weinberg RA, Jacks T (1996) Shared role of the pRB-related p130 and p107 proteins in limb development. Genes Dev 10:1633-1644.
9. Cotanche DA (1997) Hair cell regeneration in the avian cochlea. Ann Otol Rhinol Laryngol Suppl 168:9-15.
10. Duncan LJ, Mangiardi DA, Matsui JI, Anderson JK, McLaughlin-Williamson K, Cotanche DA (2006) Differential expression of unconventional my-osins in apoptotic and regenerating chick hair cells confirms two regeneration mechanisms. J Comp Neurol 499:691-701.
11. Dyson N (1998) The regulation of E2F by pRB-family proteins. Genes Dev 12:2245-2262.
12. Echteler SM, Fay RR, Popper AN (1994) Structure of the mammalian cochlea. In: Comparative hearing: mammals (FayRR, ed), pp 134-171. New York: Springer.
13. Hernandez PP, Olivari FA, Sarrazin AF, Sandoval PC, Allende ML (2007) Regeneration in zebrafish lateral line neuromasts: expression of the neural progenitor cell marker sox2 and proliferation-dependent and-independent mechanisms of hair cell renewal. Dev Neurobiol 67:637-654.
14. Jackson MW, Agarwal MK, Yang J, Bruss P, Uchiumi T, Agarwal ML, Stark GR, Taylor WR (2005) p130/p107/p105Rb-dependent transcriptional repression during DNA-damage-induced cell-cycle exit at G2. J Cell Sci 118:1821-1832.
15. Jones JE, Corwin JT (1993) Replacement of lateral line sensory organs during tail regeneration in salamanders: identification of progenitor cells and analysis of leukocyte activity. J Neurosci 13:1022-1034.
16. Kaiser CL, Kamien AJ, Shah PA, Chapman BJ, Cotanche DA (2009) 5-Ethynyl-2'-deoxyuridine labeling detects proliferating cells in the regenerating avian cochlea. Laryngoscope 119:1770-1775.
17. Kanzaki S, Beyer LA, Swiderski DL, Izumikawa M, Stover T, Kawamoto K, Raphael Y (2006) p27(Kip1) deficiency causes organ of Corti pathology and hearing loss. Hear Res 214:28-36.
18. Kawamoto K, Ishimoto S, Minoda R, Brough DE, Raphael Y (2003) Math1 gene transfer generates new cochlear hair cells in mature guinea pigs in vivo. J Neurosci 23:4395-4400.
19. ip collaborate to maintain the postmitotic state of auditory hair cells, their codeletion leading to DNA damage and p53-mediated apoptosis. J Neurosci 27:1434-1444.
20. Litovchick L, Chestukhin A, DeCaprio JA (2004) Glycogen synthase kinase 3 phosphorylates RBL2/p130 during quiescence. Mol Cell Biol 24:8970-8980.
21. Litovchick L, Sadasivam S, Florens L, Zhu X, Swanson SK, Velmurugan S, Chen R, Washburn MP, Liu XS, DeCaprio JA (2007) Evolutionarily conserved multisubunit RBL2/p130 and E2F4 protein complex represses human cell cycle-dependent genes in quiescence. Mol Cell 26:539-551.
22. Kip1 allows cell proliferation in the postnatal and adult organ of corti. Proc Natl Acad Sci USA 96:4084-4088.
23. Mantela J, Jiang Z, Ylikoski J, Fritzsch B, Zacksenhaus E, Pirvola U (2005) The retinoblastoma gene pathway regulates the postmitotic state of hair cells of the mouse inner ear. Development 132:2377-2388.
24. Mayol X, Garriga J, Grana X (1996) G1 Cyclin/CDK-independent phosphorylation and accumulation of p130 during the transition from G1 to G0 leads to its association with E2F4. Oncogene 13:237-246.
25. Minoda R, Izumikawa M, Kawamoto K, Zhang H, Raphael Y (2007) Manipulating cell cycle regulation in the mature cochlea. Hear Res 232:44-51.
26. Morest DK, Cotanche DA (2004) Regeneration of the inner ear as a model of neural plasticity. J Neurosci Res 78:455-460.
27. Mulligan G, Jacks T (1998) The retinoblastoma gene family: cousins with overlapping interests. Trends Genet 14:223-229.
28. Murata J, Ohtsuka T, Tokunaga A, Nishiike S, Inohara H, Okano H, Kageyama R (2009) Notch-Hes1 pathway contributes to the cochlear prosensory formation potentially through the transcriptional down-regulation of p27Kip1. J Neurosci Res 87:3521-3534.
29. Ono K, Nakagawa T, Kojima K, Matsumoto M, Kawauchi T, Hoshino M, Ito J (2009) Silencing p27 reverses postmitotic state of supporting cells in neonatal mouse cochleae. Mol Cell Neurosci 42:391-398.
30. Kip1: regulation and function of a haploinsufficient tumor suppressor and its misregulation in cancer. Exp Cell Res 264:148-168.
31. Poplawski P, Nauman A (2008) Thyroid hormone-triiodothyronine- has contrary effect on proliferation of human proximal tubules cell line (HK2) and renal cancer cell lines (Caki-2, Caki-1)-role of E2F4, E2F5 and p107, p130. Thyroid Res 1:5.
32. Popov B, Chang LS, Serikov V (2005) Cell-cycle-related transformation of the E2F4-p130 repressor complex. Biochem Biophys Res Commun 336:762-769.
33. Rocha-Sanchez SM, Beisel KW (2007) Pocket proteins and cell cycle regulation in inner ear development. Int J Dev Biol 51:585-595.
34. Rocha-Sanchez SM, Morris KA, Kachar B, Nichols D, Fritzsch B, Beisel KW (2007) Developmental expression of Kcnq4 in vestibular neurons and neurosensory epithelia. Brain Res 1139:117-125.
35. Ruben RJ (1967) Development of the inner ear of the mouse: a radioauto-graphic study of terminal mitoses. Acta Otolaryngol Suppl 220:221-244.
36. Sage C, Huang M, Karimi K, Gutierrez G, Vollrath MA, Zhang DS, García-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. Sage C, Huang M, Vollrath MA, Brown MC, Hinds PW, Corey DP, Vetter DE, Chen ZY (2006) Essential role of retinoblastoma protein in mammalian hair cell development and hearing. Proc Natl Acad Sci U S A 103: 7345-7350.
38. Shou J, Zheng JL, Gao WQ (2003) Robust generationofnew hair cells in the mature mammalian inner earbyadenoviral expressionofHath1. Mol Cell Neurosci 23:169-179.
39. Stone JS, Cotanche DA (2007) Hair cell regeneration in the avian auditory epithelium. Int J Dev Biol 51:633-647.
40. Taylor RR, Forge A (2005) Hair cell regeneration in sensory epithelia from the inner ear of a urodele amphibian. J Comp Neurol 484:105-120.
41. Walsh EJ, McGee J (2001) Hypothyroidism in the Tshr mutant mouse. In: Handbook of mouse auditory research: from behavior to molecular biology (Willot J, ed), pp 537-555. Boca Raton, FL: CRC.
42. Walsh EJ, McGee J, Javel E (1986) Development of auditory-evoked potentials in the cat. I. Onset of response and development of sensitivity. J Acoust Soc Am 79:712-724.
43. Weber T, Corbett MK, Chow LM, Valentine MB, Baker SJ, Zuo J (2008) Rapid cell-cycle reentry and cell death after acute inactivation of the ret-inoblastoma gene product in postnatal cochlear hair cells. Proc Natl Acad Sci U S A 105:781-785.
44. 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.
45. Woods C, Montcouquiol M, Kelley MW (2004) Math1 regulates development of the sensory epithelium in the mammalian cochlea. Nat Neurosci 7:1310-1318.
46. Worley MJ Jr, Landen CN, Slomovitz BM, Malpica A, Palla SL, Ramirez PT (2010) Expression of the retinoblastoma-related gene Rb2/p130 in the pathogenesis of serous carcinoma of the ovary. Appl Immunohistochem Mol Morphol 18:509-511.
47. Yamasoba T, Kondo K (2006) Supporting cell proliferation after hair cell injury in mature guinea pig cochlea in vivo. Cell Tissue Res 325:23-31.
48. Yu Y, Weber T, Yamashita T, Liu Z, Valentine MB, Cox BC, Zuo J (2010) In vivo proliferation of postmitotic cochlear supporting cells by acute ablation of the retinoblastoma protein in neonatal mice. J Neurosci 30:5927-5936.