DNA damage signaling regulates age-dependent proliferative capacity of quiescent inner ear supporting cells

Aging

Volumn 6, Issue 6, 2014, Pages 496-510

  Laos, Maarja ^a   Anttonen, Tommi ^a   Kirjavainen, Anna ^a   Hällström, Taija Af ^a   Laiho, Marikki ^b   Pirvola, Ulla ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cell cycle re entry; DNA damage; DNA repair; Hair cell; Inner ear; Regeneration; Supporting cell

Indexed keywords

ADULT STEM CELL; ANIMAL; CELL PROLIFERATION; CYTOLOGY; DNA DAMAGE; LABYRINTH SUPPORTING CELLS; MOUSE; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ADULT STEM CELLS; ANIMALS; CELL PROLIFERATION; DNA DAMAGE; LABYRINTH SUPPORTING CELLS; MICE; ORGAN CULTURE TECHNIQUES; SIGNAL TRANSDUCTION;

EID: 84903456727     PISSN: 19454589     EISSN: None     Source Type: Journal    
DOI: 10.18632/aging.100668     Document Type: Article

References (49)

1. Wan G, Corfas G, Stone JS. Inner ear supporting cells: Rethinking the silent majority. Semin Cell Dev Biol. 2013; 24:448-459.
2. Gonzalez F, Georgieva D, Vanoli F, Shi ZD, Stadtfeld M, Ludwig T, Jasin M, Huangfu D. Homologous recombination DNA repair genes play a critical role in reprogramming to a pluripotent state. Cell Rep. 2013; 3:651-660.
3. Laurent LC, Ulitsky I, Slavin I, Tran H, Schork A, Morey R, Lynch C, Harness JV, Lee S, Barrero MJ, Ku S, Martynova M, Semechkin R et al. Dynamic changes in the copy number of pluripotency and cell proliferation genes in human ESCs and iPSCs during reprogramming and time in culture. Cell Stem Cell. 2011; 8:106-118.
4. Loponen H, Ylikoski J, Albrecht JH, Pirvola U. Restrictions in cell cycle progression of adult vestibular supporting cells in response to ectopic cyclin D1 expression. PLoS One. 2011; 6:e27360.
5. Kastan MB, Bartek J. Cell-cycle checkpoints and cancer. Nature. 2004; 432:316-323.
6. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem. 1998; 273:5858-5868.
7. Rogakou EP, Boon C, Redon C, Bonner WM. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol. 1999; 146:905-916.
8. Adams BR, Golding SE, Rao RR, Valerie K. Dynamic dependence on ATR and ATM for double-strand break repair in human embryonic stem cells and neural descendants. PLoS One. 2010; 5:e10001.
9. Schneider L, Fumagalli M, d'Adda di Fagagna F. Terminally differentiated astrocytes lack DNA damage response signaling and are radioresistant but retain DNA repair proficiency. Cell Death Differ. 2012; 19:582-591.
10. Ye W, Blain SW. S phase entry causes homocysteine-induced death while ataxia telangiectasia and Rad3 related protein functions anti-apoptotically to protect neurons. Brain. 2010; 133:2295-2312.
11. Sulg M, Kirjavainen A, Pajusola K, Bueler H, Ylikoski J, Laiho M, Pirvola U. Differential sensitivity of the inner ear sensory cell populations to forced cell cycle re-entry and p53 induction. J Neurochem. 2010; 112:1513-1526.
12. Biton S, Gropp M, Itsykson P, Pereg Y, Mittelman L, Johe K, Reubinoff B, Shiloh Y. ATM-mediated response to DNA double strand breaks in human neurons derived from stem cells. DNA Repair (Amst). 2007; 6:128-134.
13. Gorodetsky E, Calkins S, Ahn J, Brooks PJ. ATM, the Mre11/Rad50/Nbs1 complex, and topoisomerase I are concentrated in the nucleus of purkinje neurons in the juvenile human brain. DNA Repair (Amst). 2007; 6:1698-1707.
14. Zhang Z, Yang Z, Jaamaa S, Liu H, Pellakuru LG, Iwata T, af Hallstrom TM, De Marzo AM, Laiho M. Differential epithelium DNA damage response to ATM and DNA-PK pathway inhibition in human prostate tissue culture. Cell Cycle. 2011; 10:3545-3553.
15. Gu R, Montcouquiol M, Marchionni M, Corwin JT. Proliferative responses to growth factors decline rapidly during postnatal maturation of mammalian hair cell epithelia. Eur J Neurosci. 2007; 25:1363-1372.
16. Burns JC, On D, Baker W, Collado MS, Corwin JT. Over half the hair cells in the mouse utricle first appear after birth, with significant numbers originating from early postnatal mitotic production in peripheral and striolar growth zones. J Assoc Res Otolaryngol. 2012; 13:609-627.
17. Oesterle EC, Campbell S, Taylor RR, Forge A, Hume CR. Sox2 and JAGGED1 expression in normal and drug-damaged adult mouse inner ear. J Assoc Res Otolaryngol. 2008; 9:65-89.
18. Laine H, Sulg M, Kirjavainen A, Pirvola U. Cell cycle regulation in the inner ear sensory epithelia: Role of cyclin D1 and cyclindependent kinase inhibitors. Dev Biol. 2010; 337:134-146.
19. Chai R, Kuo B, Wang T, Liaw EJ, Xia A, Jan TA, Liu Z, Taketo MM, Oghalai JS, Nusse R, Zuo J, Cheng AG. Wnt signaling induces proliferation of sensory precursors in the postnatal mouse cochlea. Proc Natl Acad Sci U S A. 2012; 109:8167-8172.
20. Bartkova J, Rezaei N, Liontos M, Karakaidos P, Kletsas D, Issaeva N, Vassiliou LV, Kolettas E, Niforou K, Zoumpourlis VC, Takaoka M, Nakagawa H, Tort F et al. Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature. 2006; 444:633-637.
21. Di Micco R, Fumagalli M, Cicalese A, Piccinin S, Gasparini P, Luise C, Schurra C, Garre' M, Nuciforo PG, Bensimon A, Maestro R, Pelicci PG, D'Adda di Fagagna F. Oncogene-induced senescence is a DNA damage response triggered by DNA hyperreplication. Nature. 2006; 444:638-642.
22. de Feraudy S, Revet I, Bezrookove V, Feeney L, Cleaver JE. A minority of foci or pan-nuclear apoptotic staining of gammaH2AX in the S phase after UV damage contain DNA double-strand breaks. Proc Natl Acad Sci U S A. 2010; 107:6870-6875.
23. Rappold I, Iwabuchi K, Date T, Chen J. Tumor suppressor p53 binding protein 1 (53BP1) is involved in DNA damage-signaling pathways. J Cell Biol. 2001; 153:613-620.
24. Branzei D, Foiani M. Regulation of DNA repair throughout the cell cycle. Nat Rev Mol Cell Biol. 2008; 9:297-308.
25. Jackson SP, Bartek J. The DNA-damage response in human biology and disease. Nature. 2009; 461:1071-1078.
26. Anttonen T, Kirjavainen A, Belevich I, Laos M, Richardson WD, Jokitalo E, Brakebusch C, Pirvola U. Cdc42-dependent structural development of auditory supporting cells is required for wound healing at adulthood. Sci Rep. 2012; 2:978.
27. Yu Y, Weber T, Yamashita T, Liu Z, Valentine MB, Cox BC, Zuo J. In vivo proliferation of postmitotic cochlear supporting cells by acute ablation of the retinoblastoma protein in neonatal mice. J Neurosci. 2010; 30:5927-5936.
28. Yamamoto N, Tanigaki K, Tsuji M, Yabe D, Ito J, Honjo T. Inhibition of notch/RBP-J signaling induces hair cell formation in neonate mouse cochleas. J Mol Med (Berl). 2006; 84:37-45.
29. Lin V, Golub JS, Nguyen TB, Hume CR, Oesterle EC, Stone JS. Inhibition of notch activity promotes nonmitotic regeneration of hair cells in the adult mouse utricles. J Neurosci. 2011; 31:15329-15339.
30. Doetzlhofer A, Basch ML, Ohyama T, Gessler M, Groves AK, Segil N. Hey2 regulation by FGF provides a notch-independent mechanism for maintaining pillar cell fate in the organ of corti. Dev Cell. 2009; 16:58-69.
31. Schimmang T, Pirvola U. Coupling the cell cycle to development and regeneration of the inner ear. Semin Cell Dev Biol. 2013; 24:507-513.
32. Mellado Lagarde MM, Cox BC, Fang J, Taylor R, Forge A, Zuo J. Selective ablation of pillar and deiters' cells severely affects cochlear postnatal development and hearing in mice. J Neurosci. 2013; 33:1564-1576.
33. Chen J, Cohen ML, Lerner AJ, Yang Y, Herrup K. DNA damage and cell cycle events implicate cerebellar dentate nucleus neurons as targets of alzheimer's disease. Mol Neurodegener. 2010; 5:60-1326-5-60.
34. Oesterle EC. Changes in the adult vertebrate auditory sensory epithelium after trauma. Hear Res. 2013; 297:91-98.
35. Kirjavainen A, Sulg M, Heyd F, Alitalo K, Yla-Herttuala S, Moroy T, Petrova TV, Pirvola U. Prox1 interacts with Atoh1 and Gfi1, and regulates cellular differentiation in the inner ear sensory epithelia. Dev Biol. 2008; 322:33-45.
36. Marinoglou K. The role of the DNA damage response kinase ataxia telangiectasia mutated in neuroprotection. Yale J Biol Med. 2012; 85:469-480.
37. Andrusiak MG, Vandenbosch R, Park DS, Slack RS. The retinoblastoma protein is essential for survival of postmitotic neurons. J Neurosci. 2012; 32:14809-14814.
38. Burns JC, Yoo JJ, Atala A, Jackson JD. MYC gene delivery to adult mouse utricles stimulates proliferation of postmitotic supporting cells in vitro. PLoS One. 2012; 7:e48704.
39. Nouspikel T, Hanawalt PC. DNA repair in terminally differentiated cells. DNA Repair (Amst). 2002; 1:59-75.
40. Goodarzi AA, Jeggo PA. The heterochromatic barrier to DNA double strand break repair: How to get the entry visa. Int J Mol Sci. 2012; 13:11844-11860.
41. Mantela J, Jiang Z, Ylikoski J, Fritzsch B, Zacksenhaus E, Pirvola U. The retinoblastoma gene pathway regulates the postmitotic state of hair cells of the mouse inner ear. Development. 2005; 132:2377-2388.
42. Burns JC, Cox BC, Thiede BR, Zuo J, Corwin JT. In vivo proliferative regeneration of balance hair cells in newborn mice. J Neurosci. 2012; 32:6570-6577.
43. Waldhaus J, Cimerman J, Gohlke H, Ehrich M, Muller M, Lowenheim H. Stemness of the organ of corti relates to the epigenetic status of Sox2 enhancers. PLoS One. 2012; 7:e36066.
44. Fernando RN, Eleuteri B, Abdelhady S, Nussenzweig A, Andang M, Ernfors P. Cell cycle restriction by histone H2AX limits proliferation of adult neural stem cells. Proc Natl Acad Sci U S A. 2011; 108:5837-5842.
45. Rieck S, Zhang J, Li Z, Liu C, Naji A, Takane KK, Fiaschi-Taesch NM, Stewart AF, Kushner JA, Kaestner KH. Overexpression of hepatocyte nuclear factor-4alpha initiates cell cycle entry, but is not sufficient to promote beta-cell expansion in human islets. Mol Endocrinol. 2012; 26:1590-1602.
46. Marino S, Vooijs M, van Der Gulden H, Jonkers J, Berns A. Induction of medulloblastomas in p53-null mutant mice by somatic inactivation of rb in the external granular layer cells of the cerebellum. Genes Dev. 2000; 14:994-1004.
47. Young KM, Mitsumori T, Pringle N, Grist M, Kessaris N, Richardson WD. An Fgfr3-iCreER(T2) transgenic mouse line for studies of neural stem cells and astrocytes. Glia. 2010; 58:943-953.
48. Albrecht JH, Hansen LK. Cyclin D1 promotes mitogenindependent cell cycle progression in hepatocytes. Cell Growth Differ. 1999; 10:397-404.
49. Hasson T, Gillespie PG, Garcia JA, MacDonald RB, Zhao Y, Yee AG, Mooseker MS, Corey DP. Unconventional myosins in innerear sensory epithelia. J Cell Biol. 1997; 137:1287-1307.