How to Bury the Dead: Elimination of Apoptotic Hair Cells from the Hearing Organ of the Mouse

JARO - Journal of the Association for Research in Otolaryngology

Volumn 15, Issue 6, 2014, Pages 975-992

  Anttonen, Tommi ^a   Belevich, Ilya ^b   Kirjavainen, Anna ^a   Laos, Maarja ^a   Brakebusch, Cord ^c   Jokitalo, Eija ^b   Pirvola, Ulla ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

actin; apoptosis; extrusion; hair cell; hearing; inner ear; phagocytosis; Repair; SBEM; supporting cell; wound healing

Indexed keywords

ACTIN; F ACTIN; MYOSIN ADENOSINE TRIPHOSPHATASE; PROTEIN CDC42; TAMOXIFEN;

ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; AUDITORY SYSTEM; CELL DEATH; CELL FUNCTION; CELL SURFACE; CONTROLLED STUDY; CORTI ORGAN; EMBRYO; EPITHELIUM CELL; FEMALE; HAIR CELL; HEARING; IN VITRO STUDY; IN VIVO STUDY; INNER EAR; INNER HAIR CELL; MALE; MOLECULAR DYNAMICS; MOUSE; MUSCLE FIBER CONTRACTION; NONHUMAN; OUTER HAIR CELL; PHAGOCYTE; PHAGOCYTOSIS; PHALANX; SCANNING ELECTRON MICROSCOPY; ANIMAL; METABOLISM; PHYSIOLOGY; ULTRASTRUCTURE; WOUND HEALING;

ACTINS; ANIMALS; APOPTOSIS; FEMALE; MALE; MICE; MICROSCOPY, ELECTRON, SCANNING; ORGAN OF CORTI; PHAGOCYTOSIS; WOUND HEALING;

EID: 84911978932     PISSN: 15253961     EISSN: 14387573     Source Type: Journal    
DOI: 10.1007/s10162-014-0480-x     Document Type: Article

References (49)

1. Abrashkin KA, Izumikawa M, Miyazawa T, Wang CH, Crumling MA, Swiderski DL, Beyer LA, Gong TW, Raphael Y (2006) The fate of outer hair cells after acoustic or ototoxic insults. Hear Res 218:20–9
2. Ahmad M, Bohne BA, Harding GW (2003) An in vivo tracer study of noise-induced damage to the reticular lamina. Hear Res 175:82–100
3. Anttonen T, Kirjavainen A, Belevich I, Laos M, Richardson WD, Jokitalo E, Brakebusch C, Pirvola U (2012) Cdc42-dependent structural development of auditory supporting cells is required for wound healing at adulthood. Sci Rep 2:978
4. Bird JE, Daudet N, Warchol ME, Gale JE (2010) Supporting cells eliminate dying sensory hair cells to maintain epithelial integrity in the avian inner ear. J Neurosci 30:12545–56
5. Bohne BA, Harding GW, Lee SC (2007) Death pathways in noise-damaged outer hair cells. Hear Res 223:61–70
6. Burns JC, Corwin JT (2013) A historical to present-day account of efforts to answer the question: “what puts the brakes on mammalian hair cell regeneration?”. Hear Res 297:52–67
7. Burns JC, Corwin JT (2014) Responses to cell loss become restricted as the supporting cells in mammalian vestibular organs grow thick junctional actin bands that develop high stability. J Neurosci 34:1998–2011
8. Burns JC, Collado MS, Oliver ER, Corwin JT (2013) Specializations of intercellular junctions are associated with the presence and absence of hair cell regeneration in ears from six vertebrate classes. J Comp Neurol 521:1430–48
9. Cotanche DA, Dopyera CE (1990) Hair cell and supporting cell response to acoustic trauma in the chick cochlea. Hear Res 46:29–40
10. Crouch JJ, Sakaguchi N, Lytle C, Schulte BA (1997) Immunohistochemical localization of the Na–K–Cl co-transporter (NKCC1) in the gerbil inner ear. J Histochem Cytochem 45:773–8
11. Denk W, Horstmann H (2004) Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure. PLoS Biol 2:e329
12. Flock A, Flock B, Fridberger A, Scarfone E, Ulfendahl M (1999) Supporting cells contribute to control of hearing sensitivity. J Neurosci 19:4498–507
13. Forge A (1985) Outer hair cell loss and supporting cell expansion following chronic gentamicin treatment. Hear Res 19:171–82
14. Forge A, Jagger DJ, Kelly JJ, Taylor RR (2013) Connexin30-mediated intercellular communication plays an essential role in epithelial repair in the cochlea. J Cell Sci 126:1703–12
15. Fredelius L (1988) Time sequence of degeneration pattern of the organ of corti after acoustic overstimulation. A transmission electron microscopy study. Acta Otolaryngol 106:373–85
16. Fuchs PA, Lehar M, Hiel H (2014) Ultrastructure of cisternal synapses on outer hair cells of the mouse cochlea. J Comp Neurol 522:717–29
17. 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
18. Guillot C, Lecuit T (2013) Mechanics of epithelial tissue homeostasis and morphogenesis. Science 340:1185–9
19. Hirose K, Westrum LE, Cunningham DE, Rubel EW (2004) Electron microscopy of degenerative changes in the chick basilar papilla after gentamicin exposure. J Comp Neurol 470:164–80
20. Hochreiter-Hufford A, Ravichandran KS (2013) Clearing the dead: apoptotic cell sensing, recognition, engulfment, and digestion. Cold Spring Harb Perspect Biol 5:a008748
21. Hordichok AJ, Steyger PS (2007) Closure of supporting cell scar formations requires dynamic actin mechanisms. Hear Res 232:1–19
22. Kuipers D, Mehonic A, Kajita M, Peter L, Fujita Y, Duke T, Charras G, Gale JE (2014) Epithelial repair is a two-stage process driven first by dying cells and then by their neighbours. J Cell Sci 127:1229–41
23. Kurihara K, Moore-Hoon ML, Saitoh M, Turner RJ (1999) Characterization of a phosphorylation event resulting in upregulation of the salivary Na(+)–K(+)–2Cl(−) cotransporter. Am J Physiol 277:1184–C1193
24. Leonova EV, Raphael Y (1997) Organization of cell junctions and cytoskeleton in the reticular lamina in normal and ototoxically damaged organ of corti. Hear Res 113:14–28
25. MacVicar BA, Feighan D, Brown A, Ransom B (2002) Intrinsic optical signals in the rat optic nerve: role for K(+) uptake via NKCC1 and swelling of astrocytes. Glia 37:114–23
26. McDowell B, Davies S, Forge A (1989) The effect of gentamicin-induced hair cell loss on the tight junctions of the reticular lamina. Hear Res 40:221–32
27. Meyers JR, Corwin JT (2007) Shape change controls supporting cell proliferation in lesioned mammalian balance epithelium. J Neurosci 27:4313–25
28. Monks J, Rosner D, Geske FJ, Lehman L, Hanson L, Neville MC, Fadok VA (2005) Epithelial cells as phagocytes: apoptotic epithelial cells are engulfed by mammary alveolar epithelial cells and repress inflammatory mediator release. Cell Death Differ 12:107–14
29. Monzack EL, Cunningham LL (2013) Lead roles for supporting actors: critical functions of inner ear supporting cells. Hear Res 303:20–9
30. Oesterle EC (2013) Changes in the adult vertebrate auditory sensory epithelium after trauma. Hear Res 297:91–8
31. Oesterle EC, Campbell S, Taylor RR, Forge A, Hume CR (2008) Sox2 and JAGGED1 expression in normal and drug-damaged adult mouse inner ear. J Assoc Res Otolaryngol 9:65–89
32. Parnaik R, Raff MC, Scholes J (2000) Differences between the clearance of apoptotic cells by professional and non-professional phagocytes. Curr Biol 10:857–60
33. Piazza V, Ciubotaru CD, Gale JE, Mammano F (2007) Purinergic signalling and intercellular Ca2+ wave propagation in the organ of corti. Cell Calcium 41:77–86
34. Raphael Y, Altschuler RA (1991) Reorganization of cytoskeletal and junctional proteins during cochlear hair cell degeneration. Cell Motil Cytoskeleton 18:215–27
35. Raphael Y, Altschuler RA (2003) Structure and innervation of the cochlea. Brain Res Bull 60:397–422
36. Ridley AJ (2006) Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol 16:522–9
37. Rosenblatt J, Raff MC, Cramer LP (2001) An epithelial cell destined for apoptosis signals its neighbors to extrude it by an actin- and myosin-dependent mechanism. Curr Biol 11:1847–57
38. Sakaguchi N, Crouch JJ, Lytle C, Schulte BA (1998) Na–K–Cl cotransporter expression in the developing and senescent gerbil cochlea. Hear Res 118:114–22
39. Saunders JC, Dear SP, Schneider ME (1985) The anatomical consequences of acoustic injury: a review and tutorial. J Acoust Soc Am 78:833–60
40. Silva MT (2010) Secondary necrosis: the natural outcome of the complete apoptotic program. FEBS Lett 584:4491–9
41. Sonnemann KJ, Bement WM (2011) Wound repair: toward understanding and integration of single-cell and multicellular wound responses. Annu Rev Cell Dev Biol 27:237–63
42. Souter M, Nevill G, Forge A (1997) Postnatal maturation of the organ of corti in gerbils: morphology and physiological responses. J Comp Neurol 386:635–51
43. Taylor RR, Nevill G, Forge A (2008) Rapid hair cell loss: a mouse model for cochlear lesions. J Assoc Res Otolaryngol 9:44–64
44. Taylor RR, Jagger DJ, Forge A (2012) Defining the cellular environment in the organ of corti following extensive hair cell loss: a basis for future sensory cell replacement in the cochlea. PLoS One 7:e30577
45. Wang F, Wang F, Zou Z, Liu D, Wang J, Su Y (2011) Active deformation of apoptotic intestinal epithelial cells with adhesion-restricted polarity contributes to apoptotic clearance. Lab Invest 91:462–71
46. Wilke SA, Antonios JK, Bushong EA, Badkoobehi A, Malek E, Hwang M, Terada M, Ellisman MH, Ghosh A (2013) Deconstructing complexity: serial block-face electron microscopic analysis of the hippocampal mossy fiber synapse. J Neurosci 33:507–22
47. Wu X, Li S, Chrostek-Grashoff A, Czuchra A, Meyer H, Yurchenco PD, Brakebusch C (2006) Cdc42 is crucial for the establishment of epithelial polarity during early mammalian development. Dev Dyn 236:2767–78
48. Ylikoski J (1974) Correlative studies on the cochlear pathology and hearing loss in guinea-pigs after intoxication with ototoxic antibiotics. Acta Otolaryngol Suppl 326:1–62
49. Young KM, Mitsumori T, Pringle N, Grist M, Kessaris N, Richardson WD (2010) An Fgfr3-iCreER(T2) transgenic mouse line for studies of neural stem cells and astrocytes. Glia 58:943–53