Macrophage and microglia-like cells in the avian inner ear

Journal of Comparative Neurology

Volumn 398, Issue 2, 1998, Pages 241-256

  Bhave, Sujata A ^a   Oesterle, Elizabeth C ^a   Coltrera, Marc D ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Auditory; Cochlea; Hair cell regeneration; Leukocytes proliferation; Vestibular

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CYCLE; CELL DENSITY; CELL REGENERATION; CHICKEN; COCHLEA; CONTROLLED STUDY; FOWL; HAIR CELL; INNER EAR DISEASE; LEUKOCYTE; MACROPHAGE; MICROGLIA; NEUROEPITHELIUM; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTIMETABOLITES; BROMODEOXYURIDINE; CELL DEATH; CHICKENS; GENTAMICINS; HAIR CELLS; IMMUNOHISTOCHEMISTRY; MACROPHAGES; MICROGLIA; MICROSCOPY, ELECTRON, SCANNING; SACCULE AND UTRICLE;

EID: 0032563734     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19980824)398:2<241::AID-CNE6>3.0.CO;2-0     Document Type: Article

References (96)

1. Andersson, P.B., V.H. Perry, and S. Gordon (1991) The kinetics and morphological characteristics of the macrophage-microglial response to kainic acid-induced neuronal degeneration. Neuroscience 42:201-214.
2. Assoian, R.K., B.E. Fleurdelys, H.C. Stevenson, P.J. Miller, D.K. Madtes, E.W. Raines, R. Ross, and M.B. Sporn (1987) Expression and secretion of type beta transforming growth factor by activated human macrophages. Proc. Natl. Acad. Sci. USA 84:6020-6024.
3. Baird, A., P. Mormede, and P. Bohlen (1985) Immunoreactive fibroblast growth factor in cells of peritoneal exudate suggests its identity with macrophage-derived growth factor. Biochem. Biophys. Res. Commun. 126:358-364.
4. Baird, R.A., M.A. Torres, and N.R. Schuff (1993) Hair cell regeneration in the bullfrog vestibular otolith organs following aminoglycoside toxicity. Hear. Res. 65:164-174.
5. Balak, K.J., J.T. Corwin, and J.E. Jones (1990) Regenerated hair cells can originate from supporting cell progeny: Evidence from phototoxicity and laser ablation experiments in the lateral line system. J. Neurosci. 10:2502-2512.
6. Bellanti, J.A. (1985) Immunology III. Philadelphia: W.B. Saunders Company.
7. Bhave, S.A., J.S. Stone, E.W. Rubel, and M.D. Coltrera (1995) Cell cycle progression in gentamicin-damaged avian cochleas. J. Neurosci. 15: 4618-4628.
8. Bhave, S.A., E.C. Oesterle, and M.D. Coltrera (1996) Macrophages and microglia in regenerating inner ear sensory epithelia. Assoc. Res. Otolaryngol. Abstr. 19:199.
9. Bohne, B. (1971) Scar formation in the inner ear following acoustical injury. Doctoral dissertation, Washington University.
10. Carey, J.P., A.F. Fuchs, and E.W. Rubel (1996) Hair cell regeneration and recovery of the vestibuloocular reflex in the avian vestibular system. J. Neurophys. 76:3301-3312.
11. Chugani, D.C., N.L. Kedersha, and L.H. Rome (1991) Vault immunofluorescence in the brain: New insights regarding the origin of microglia. J. Neurosci. 11:256-268.
12. Corwin, J.T. and D.A. Cotanche (1988) Regeneration of sensory hair cells after acoustic trauma. Science 240:1772-1774.
13. Cotanche, D.A. (1987) Regeneration of hair cell stereociliary bundles in the chick cochlea following severe acoustic trauma. Hear. Res. 30:181-196.
14. Cruz, R.M., P.R. Lambert, and E.W. Rubel (1987) Light microscopic evidence of hair cell regeneration after gentamicin toxicity in chick cochlea. Arch. Otolaryngol. Head Neck Surg. 113:1058-1062.
15. Davis, E.J., T.D. Foster, and W.E. Thomas (1994) Cellular forms and functions of brain microglia. Brain Res. Bull. 34:73-78.
16. Dunning, H.S. (1935) Studies on the relation between microglia, histocytes and monocytes. Am. J. Pathol. 11:895-913.
17. Fredelius, L. and A.-H. Rask (1990) The rule of macrophages in the disposal of degeneration products within the organ of corti after acoustic overstimulation. Acta Otolaryngol. Stockh. 109:76-82.
18. Girod, D.A., L.G. Duckert, and E.W. Rubel (1989) Possible precursors of regenerated hair cells in the avian cochlea following accoustic trauma. Hear. Res. 42:175-194.
19. Giulian, D., J. Chen, J.E. Ingeman, J.K. George, and M. Noponen (1989) The role of mononuclear phagocytes in wound healing after traumatic injury to adult mammalian brain. J. Neurosci. 9:4416-4429.
20. Gloddek, B., A.F. Ryan, and J.P. Harris (1991) Homing of lymphocytes to the inner ear. Acta Otolaryngol. Stockh. 111:1051-1059.
21. Gratzner, H.G. (1982) Monoclonal antibody to 5-bromo-and 5-iododeoxyuridine: A new reagent for detection of DNA replication. Science 218:474-475.
22. Haas, W., P. Pereira, and S. Tonegawa (1993) Gamma/delta cells. Annu. Rev. Immunol. 11:637-685.
23. Hashino, E. and R. Salvi (1993) Changing patterns of DNA replication in the noise-damaged chick cochlea. J. Cell Sci. 105:23-31.
24. Hashino, E. and M. Sokabe (1989) Kanamycin induced low-frequency hearing loss in the budgerigar (Melopsittacus undulatus). J. Acoust. Soc. Am. 85:289-294.
25. Hayes, G.M., M.N. Woodroofe, and M.L. Cuzner (1987) Microglia are the major cell type expressing MHC class II in human white matter. J. Neurol. Sci. 80:25-37.
26. Higashiyama, S., J.A. Abraham, J. Miller, J.C. Fiddes, and M. Klagsbrun (1991) A heparin-binding growth factor secreted by macrophage-like cells that is related to EGF. Science 251:936-939.
27. Hirokawa, N. (1978) The ultrastructure of the basilar papilla of the chick. J. Comp. Neurol. 181:361-374.
28. Hume, D.A., V.H. Perry, and S. Gordon (1983) Immunohistochemical localization of a macrophage-specific antigen in developing mouse retina: Phagocytosis of dying neurons and differentiation of microglial cells to form a regular array in the plexiform layers. J. Cell Biol. 97:253-257.
29. Janas, J.D., D.A. Cotanche, and E.W. Rubel (1995) Avian cochlear hair cell regeneration: Stereological analyses of damage and recovery from a single high dose of gentamicin. Hear. Res. 92:17-29.
30. Johnson, P., A. Maiti, and D.H.W. Ng (1996) CD45: A Family of Leukocyte-Specific Cell Surface Glycoproteins. Cambridge: Blackwell Science.
31. Jones, J.E. and J.T. Corwin (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.
32. Jones, J.E. and J.T. Corwin (1996) Regeneration of sensory cells after laser ablation in the lateral line system: Hair cell lineage and macrophage behavior revealed by time-lapse video microscopy. J. Neurosci. 16:649-662.
33. Jørgensen, J.M. (1991) Regeneration of lateral line and inner ear vestibular cells. In: Regeneration of Vertebrate Sensory Receptor Cells. G.R. Bock and J. Whelan (ed.) Chichester: John Wiley and Sons, pp. 151-170.
34. Jørgensen, J.M. and J.T. Christensen (1989) The inner ear of the common rhea (Rhea americana L.). Brain Behav. Evol. 34:273-280.
35. Jørgensen, J.M. and C. Mathiesen (1988) The avian inner ear. Continuous production of hair cells in vestibular sensory organs, but not in the auditory papilla. Naturwissenschaften 75:319-320.
36. Kil, J., M.E. Warchol, and J.T. Corwin (1997) On-going and aminoglycoside-induced hair cell death in the vestibular sensory epithelia of the chicken. Hearing Res. 114:117-126.
37. Kuntz, A.L. and E.C. Oesterle (1996) TGF alpha induces hair cell production in mature mammalian vestibular sensory epithelia in vivo. Assoc. Res. Otolaryngol. Abstr. 19:790.
38. Lambert, P.R. (1994) Inner ear hair cell regeneration in a mammal: Identification of a triggering factor. Laryngoscope 104:701-718.
39. Lindholm, D., E. Castr'en, R. Kiefer, F. Zafra, and H. Thoenen (1992) Transforming growth factor-beta 1 in the rat brain: Increase after injury and inhibition of astrocyte proliferation. J. Cell Biol. 117:395-400.
40. Ling, E.A. (1981) Ultrastructure and peroxidase cytochemistry of macrophages present in the retina of postnatal rats. Arch. Histol. Jpn. 44:167-176.
41. Ling, E.A. and W.C. Wong (1993) The origin and nature of ramified and amoeboid microglia: A historical review and current concepts. Glia 7:9-18.
42. Linzenbold, A., R.J. Dooling, and B. Ryals (1993) A behavioral audibility curve for a Japanese quail. Assoc. Res. Otolaryngol. Abstr. 16:53.
43. Lombarte, A., H.Y. Yan, A.N. Popper, J.S. Chang, and C. Platt (1993) Damage and regeneration of hair cell ciliary bundles in a fish ear following treatment with gentamicin. Hear. Res. 64:166-174.
44. Madtes, D.K., E.W. Raines, K.S. Sakariassen, R.K. Assoian, M.B. Sporn, G.I. Bell and R. Ross (1988) Induction of transforming growth factor-alpha in activated human alveolar macrophages. Cell 53:285-293.
45. Mallat, M., R. Houlgatte, P. Brachet, and A. Prochiantz (1989) Lipopolysaccharide-stimulated rat brain macrophages release NGF in vitro. Dev. Biol. 133:309-311.
46. Manley, G.A. (1990) Peripheral Hearing Mechanisms in Reptiles and Birds. New York: Springer-Verlag.
47. Marean, G.C., J.M. Burt, M.D. Beecher, and E.W. Rubel (1993) Hair cell regeneration in the European starling (Sturnus vulgaris): Recovery of pure-tone detection thresholds. Hear. Res. 71:125-136.
48. Mason, J.C., J. Kil, M.E. Warchol, and J.T. Corwin (1995) Acoustic trauma results in apoptotic death of cochlear hair cels. J. Neurosci. Abstr. 25:396.
49. Mori, S. and C.P. Leblond (1969) Identification of microglia in light and electron microscopy. J. Comp. Neurol. 135:57-80.
50. Murabe, Y. and Y. Sano (1982) Morphological studies on neuroglia. VI. Postnatal development of microglial cells. Cell Tissue Res. 225:469-485.
51. Nathan, C.F. (1987) Secretory products of macrophages. J. Clin. Invest. 79:319-326.
52. Nomura, Y., M. Hara, and T. Kurata (1988) Experimental herpes simplex virus and cytomegalovirus labyrinthitis. Acta Otolaryngol. 457:57-66.
53. Oesterle, E.C. and E.W. Rubel (1993) Postnatal production of supporting cells in the chick cochlea. Hear. Res. 66:213-124.
54. Oesterle, E.C., D.E. Cunningham, and E.W. Rubel (1992) Ultrastructure of hyaline, border, and vacuole cells in chick inner ear. J. Comp. Neurol. 318:64-82.
55. Oesterle, E.C., T.T. Tsue, T.A. Reh, and E.W. Rubel (1993) Hair-cell regeneration in organ cultures of the postnatal chicken inner ear. Hear. Res. 70:85-108.
56. Oesterle, E.C., T.T. Tsue, and E.W. Rubel (1997) Induction of cell proliferation in avian inner ear sensory epithelia by insulin-like growth factor I and insulin. J. Comp. Neurol. 380:262-274.
57. Ol'ah, I. and B. Glick (1995) Dendritic cells in the bursal follicles and germinal centers of the chicken's caecal tonsil express vimentin but not desmin. Anat. Rec. 243:384-389.
58. Paramithiotis, E., L. Tkalec, and M.J. Ratcliffe (1991) High levels of CD45 are coordinately expressed with CD4 and CD8 on avian thymocytes. J. Immunol. 147:3710-3717.
59. Penfold, P.L., M.C. Madigan, and J.M. Provis (1991) Antibodies to human leucocyte antigens indicate subpopulations of microglia in human retina. Vis. Neurosci. 7:383-388.
60. Perry, V.H., D.A. Hume, and S. Gordon (1985) Immunohistochemical localization of macrophages and microglia in the adult and developing mouse brain. Neuroscience 15:313-326.
61. Perry, V.H., P.B. Andersson, and S. Gordon (1993) Macrophages and inflammation in the central nervous system. Trends Neurosci. 16:268-273.
62. Plata Salam'an, C.R. (1991) Epidermal growth factor and the nervous system. Peptides 12:653-663.
63. Pow, D.V., V.H. Perry, J.F. Morris, and S. Gordon (1989) Microglia in the neurohypophysis associate with and endocytose terminal portions of neurosecretory neurons. Neuroscienee 33:567-578.
64. Presson, J.C. and A.N. Popper (1990) Possible precursors to new hair cells, support cells, and Schwann cells in the ear of a post-embryonic fish. Hear. Res. 46:9-21.
65. Provis, J.M., P.L. Penfold, A.J. Edwards, and D. van-Driel (1995) Human retinal microglia: Expression of immune markers and relationship to the glia limitans. Glia 14:243-256.
66. Raphael, Y. (1992) Evidence for supporting cell mitosis in response to acoustic trauma in the avian inner ear. J. Neurocytol. 21:663-671.
67. Rappolee, D.A., D. Mark, M.J. Banda, and Z. Werb (1988) Wound macrophages express TGF-alpha and other growth factors in vivo: Analysis by mRNA phenotyping. Science 241:708-712.
68. Roberson, D.F., P. Weisleder, P.S. Bohrer, and E.W. Rubel (1992) Ongoing production of sensory cells in the vestibular epithelium of the chick. Hear. Res. 57:166-174.
69. Roessmann, U. and R.L. Friede (1968) Entry of labeled monocytic cells into the central nervous system. Acta Neuropathol. Berl. 10:359-362.
70. Rom, W.N., P. Basset, G.A. Fells, T. Nukiwa, B.C. Trapnell, and R.G. Crysal (1988) Alveolar macrophages release an insulin-like growth factor I-type molecule. J. Clin. Invest. 82:1685-1693.
71. Ryals, B.M. and E.W. Rubel (1988) Hair cell regeneration after acoustic trauma in adult Coturnix quail. Science 240:1774-1776.
72. Saunders, S.S., R.J. Salvi, and K.M. Miller (1995) Recovery of thresholds and temporal integration in adult chickens after high level 525 Hz pure tone exposure. J. Acoust. Soc. Am. 97:1150-1164.
73. Shimojo, M., K. Nakajima, N. Takei, M. Hamanoue, and S. Kohsaka (1991) Production of basic fibroblast growth factor in cultured rat brain microglia. Neurosci. Lett. 123:229-231.
74. Shimokado, K., E.W. Raines, D.K. Madtes, T.B. Barrett, E.P. Benditt, and R. Ross (1985) A significant part of macrophage-derived growth factor consists of at least two forms of PDGF. Cell 43:277-286.
75. Smith, C.A. (1981) Recent advances in structural correlates of auditory receptors. In D. Ottoson, (ed): Progress in Sensory Physiology 2. New York: Springer-Verlag, pp. 1-182.
76. Smith, C.A. (1985) Inner Ear. London: Academic Press.
77. Stone, J.S. and D.A. Cotanche (1994) Identification of the timing of S phase and patterns of cell proliferation during hair cell regeneration in the chick cochlea. J. Comp. Neurol. 341:50-67.
78. Stone, J.S., S.G. Leano, L.P. Baker, and E.W. Rubel (1996) Hair cell differentiation in chick cochlear epithelium after aminoglycoside toxicity: In vivo and in vitro observations. J. Neurosci. 16:6157-6174.
79. Tanaka, K. and C.A. Smith (1978) Structure of the chicken's inner ear: SEM and TEM study. Am. J. Anat. 153:251-272.
80. Thomas, R., L.S. Davis, and P.E. Lipsky (1993) Isolation and characterization of human peripheral blood dendritic cells. J. Immunol. 150:821-834.
81. Tilney, L.G. and J.C. Saunders (1983) Actin filaments, stereocilia, and hair cells of the bird cochlea I. Length, number, width, and distribution of stereocilia of each hair cell are related to the position of the hair cell on the cochlea. J. Cell Biol. 96:807-821.
82. Tsue, T.T., E.C. Oesterle, and E.W. Rubel (1994a) Diffusible factors regulate hair cell regeneration in the avian inner ear. Proc. Natl. Acad. Sci. USA 91:1584-1588.
83. Tsue, T.T, D.L. Watling, P. Weisleder, M.D. Coltrera, and E.W. Rubel (1994b) Identification of hair cell progenitors and intermitotic migration of their nuclei in the normal and regenerating avian inner ear. J. Neurosci. 14:140-152.
84. Ulvestad, E., K. Williams, R. Bjerkvig, K. Tiekotter, J. Antel, and R. Matre (1994) Human microglial cells have phenotypic and functional characteristics in common with both macrophages and dendritic antigen-presenting cells. J. Leukoc. Biol. 56:732-740.
85. van Furth, R., P.H. Nibbering, J.T. van Dissel, and M.M. Diesselhoff den Dulk (1985) The characterization, origin, and kinetics of skin macrophages during inflammation. J. Invest. Dermatol. 85:398-402.
86. Warchol, M.E. (1995) Supporting cells in isolated sensory epithelia of avian utricles proliferate in serum-free culture. Neuroreport 6:981-984.
87. Warchol, M.E. (1997) Macrophage activity in organ cultures of the avian cochlea: Demonstration of a resident population and recruitment to sites of hair cell lesions. J. Neurobiol. 33:724-734.
88. Warchol, M.E. and J.T. Corwin (1993) Supporting cells in avian vestibular organs proliferate in serum-free culture. Hear. Res. 71:28-36.
89. Warchol, M.E. and J.T. Corwin (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.
90. Weisleder, P. and E.W. Rubel (1993) Hair cell regeneration after streptomycin toxicity in the avian vestibular epithelium. J. Comp. Neurol. 331:97-110.
91. Wersäll, J. (1956) Studies on the structure and innervation of the sensory epithelium of the cristae ampullaris in the guinea pig. Acta Otolaryngol. Supplement 126:56-61.
92. Yamamoto, M., K. Fujihashi, K.W. Beagley, J.R. McGhee, and H. Kiyono (1993) Cytokine synthesis by intestinal intraepithelial lymphocytes. Both gamma/delta T cell receptor-positive and alpha/beta T cell receptor-positive T cells in the G1 phase of cell cycle produce IFN-gamma and IL-5. J. Immunol. 150:106-114.
93. Yamane, H., H. Iguchi, K. Konishi, T. Nakagawa, Y. Nakai, K. Takahashi and H.R. Andersen. (1995) Natural killer cell response in the inner ear. Acta Otolaryngol. Stockh. 115:738-741.
94. Yamashita, H. and E.C. Oesterle (1994) Mitogenic effects of EGF and TGF-alpha on cultured vestibular sensory epithelium from the mammalian inner ear. Assoc. Res. Otolaryngol. Abstr. 17:131A.
95. Yamashita, H. and E.C. Oesterle (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.
96. Zheng, J.L., C. Helbig, and W. Gao (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.