Changes in calcium-binding protein expression in the auditory brainstem nuclei of the jaundiced Gunn rat

Hearing Research

Volumn 171, Issue 1-2, 2002, Pages 129-141

  Spencer, Robert F ^a   Shaia, Wayne T ^a   Gleason, Ann T ^a   Sismanis, Aristides ^a   Shapiro, Steven M ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Cochlear nucleus; Electron microscopy; Hyperbilirubinemia; Immunohistochemistry; Inferior colliculus; Jaundice; Kernicterus; Lateral lemniscus nucleus; Light microscopy; Superior olivary complex

Indexed keywords

CALBINDIN; CALCIUM BINDING PROTEIN; PARVALBUMIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUDITORY NERVOUS SYSTEM; BRAIN NUCLEUS; BRAIN STEM; CONTROLLED STUDY; DENDRITE; ELECTRON MICROSCOPY; FEMALE; HETEROZYGOSITY; HOMOZYGOSITY; HYPERBILIRUBINEMIA; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INFERIOR COLLICULUS; JAUNDICE; MALE; MEDIAL GENICULATE BODY; MEDIAL LEMNISCUS; MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RAT STRAIN; SUPERIOR OLIVARY NUCLEUS;

ANIMALS; ANIMALS, NEWBORN; BRAIN STEM; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; COCHLEAR NUCLEUS; DISEASE MODELS, ANIMAL; FEMALE; HEARING LOSS, SENSORINEURAL; HUMANS; IMMUNOHISTOCHEMISTRY; INFANT, NEWBORN; INFERIOR COLLICULUS; JAUNDICE, NEONATAL; MALE; MICROSCOPY, IMMUNOELECTRON; OLIVARY NUCLEUS; PARVALBUMINS; RATS; RATS, GUNN; RATS, MUTANT STRAINS;

EID: 0036768228     PISSN: 03785955     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0378-5955(02)00494-X     Document Type: Article

References (76)

1. Adams J.C., Mugnaini E. Immunocytochemical evidence for inhibitory and disinhibitory circuits in the superior olive. Hear. Res. 49:1990;281-298.
2. Ahlfors C.E., Shapiro S.M. Auditory brainstem response and unbound bilirubin in jaundiced (jj) Gunn rat pups. Biol. Neonate. 80:2001;158-162.
3. Airaksinen M.S., Eilers J., Garaschuk O., Thoenen H., Konnerth A., Meyer M. Ataxia and altered dendritic calcium signaling in mice carrying a targeted null mutation of the calbindin D28k gene. Proc. Natl. Acad. Sci. USA. 94:1997;1488-1493.
4. Aoki E., Semba R., Seto-Ohshima A., Heizmann C.W., Kashiwamata S. Coexistence of parvalbumin and glycine in the rat brainstem. Brain Res. 525:1990;140-143.
5. Belal A. Effect of hyperbilirubinemia on the inner ear in Gunn rats. J. Laryngol. Otol. 89:1975;259-265.
6. Bergman I., Hirsch R.P., Fria T.J., Shapiro S.M., Holzman I., Painter M.J. Cause of hearing loss in the high-risk premature infant. J. Pediatr. 106:1985;5-101.
7. Blackburn S. Hyperbilirubinemia and neonatal jaundice. Neonatal Netw. 14:1995;15-25.
8. Blanc W.A., Johnson L. Studies on kernicterus; relationship with sulfonamide intoxication, report on kernicterus in rats with glucuronyl transferase deficiency and review of pathogenesis. J. Neuropathol. Exp. Neurol. 18:1959;165-189.
9. Caicedo A., d'Aldin C., Puel J.L., Eybalin M. Distribution of calcium-binding protein immunoreactivities in the guinea pig auditory brainstem. Anat. Embryol. (Berl.). 194:1996;465-487.
10. Caicedo A., d'Aldin C., Eybalin M., Puel J.L. Temporary sensory deprivation changes calcium-binding proteins levels in the auditory brainstem. J. Comp. Neurol. 378:1997;1-15.
11. Carhart R. Probable mechanisms underlying kernicteric hearing loss. Acta Otolaryngol. Suppl. 1967;1-41.
12. Celio M.R. Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience. 35:1990;375-475.
13. Chisin R., Perlman M., Sohmer H. Cochlear and brain stem responses in hearing loss following neonatal hyperbilirubinemia. Ann. Otol. 88:1979;352-357.
14. 2+/calmodulin-dependent kinase II activity in vitro. Pediatr. Res. 38:1995;949-954.
15. Conlee J.W., Shapiro S.M. Morphological changes in the cochlear nucleus and nucleus of the trapezoid body in Gunn rat pups. Hear. Res. 57:1991;23-30.
16. 2+/calmodulin kinase II in the cerebellum of jaundiced Gunn rats during development: a quantitative light microscopic analysis. Acta Neuropathol. (Berl.). 99:2000;393-401.
17. Connolly A.M., Volpe J.J. Clinical features of bilirubin encephalopathy. Clin. Perinatol. 17:1990;371-379.
18. de Vries L.S., Lary S., Dubowitz L.M.S. Relationship of serum bilirubin levels to ototoxicity and deafness in high-risk, low birth-weight infants. Pediatrics. 76:1985;351-354.
19. de Vries L.S., Lary S., Whitelaw A.G., Dubowitz L.M. Relationship of serum bilirubin levels and hearing impairment in newborn infants. Early Hum. Dev. 15:1987;269-277.
20. Deltenre P., Mansbach A.L., Bozet C., Clercx A., Hecox K.E. Auditory neuropathy: a report on three cases with early onsets and major neonatal illnesses. Electroencephalogr. Clin. Neurophysiol. 104:1997;17-22.
21. 14C into the CNS. J. Clin. Invest. 45:1966;678-689.
22. Dublin W. Central auditory pathology. Otolaryngol. Head Neck Surg. 95:1986;363-424.
23. el Barbary A. Auditory nerve of the normal and jaundiced rat. I. Spontaneous discharge rate and cochlear nerve histology. Hear. Res. 54:1991;75-90.
24. Enderlin S., Norman A.W., Celio M.R. Ontogeny of the calcium binding protein calbindin D-28k in the rat nervous system. Anat. Embryol. (Berl.). 177:1987;15-28.
25. Friauf E. Transient appearance of calbindin-D28k-positive neurons in the superior olivary complex of developing rats. J. Comp. Neurol. 334:1993;59-74.
26. Friauf E. Distribution of calcium-binding protein calbindin-D28k in the auditory system of adult and developing rats. J. Comp. Neurol. 349:1994;193-211.
27. Frisina R.D., Zettel M.L., Kelley P.E., Walton J.P. Distribution of calbindin D-28k immunoreactivity in the cochlear nucleus of the young adult chinchilla. Hear. Res. 85:1995;53-68.
28. Grothe B., Sanes D.H. Synaptic inhibition influences the temporal coding properties of medial superior olivary neurons: an in vitro study. J. Neurosci. 14:1994;1701-1709.
29. Gunn C.K. Hereditary acholuric jaundice in a new mutant strain of rats. J. Hered. 29:1938;137-139.
30. Helfert R.H., Bonneau J.M., Wenthold R.J., Altschuler R.A. GABA and glycine immunoreactivity in the guinea pig superior olivary complex [published erratum appears in Brain Res. 509 (1990) 180]. Brain Res. 501:1989;269-286.
31. Helfert R.H., Juiz J.M., Bledsoe S.C. Jr., Bonneau J.M., Wenthold R.J., Altschuler R.A. Patterns of glutamate, glycine, and GABA immunolabeling in four synaptic terminal classes in the lateral superior olive of the guinea pig. J. Comp. Neurol. 323:1992;305-325.
32. Irvine, D.R.F., 1992. In: Popper, A.N., Fay, R.R. (Eds.), The Mammalian Auditory Pathway: Neurophysiology. Springer-Verlag, New York, pp. 153-231.
33. Jew J.Y., Sandquist D. CNS changes in hyperbilirubinemia. Arch. Neurol. 36:1979;149-154.
34. Jew J.Y., Williams T.H. Ultrastructural aspects of bilirubin encephalopathy in cochlear nuclei of the Gunn rat. J. Anat. 124:1977;599-614.
35. Johnson L., Sarmiento F., Blanc W.A., Day R. Kernicterus in rats with an inherited deficiency of glucuronyl transferase. Am. J. Dis. Child. 97:1959;591-608.
36. Johnson L., Garcia M.L., Figueroa E., Sarmiento F. Kernicterus in rats lacking glucuronyl transferase. Am. J. Dis. Child. 101:1961;322-349.
37. Johnson L.H., Bhutani V.K., Brown A.K. System-based approach to management of neonatal jaundice and prevention of kernicterus. J. Pediatr. 140:2002;396-403.
38. Kandler K., Friauf E. Pre- and postnatal development of efferent connections of the cochlear nucleus in the rat. J. Comp. Neurol. 328:1993;161-184.
39. Kandler K., Friauf E. Development of electrical membrane properties and discharge characteristics of superior olivary complex neurons in fetal and postnatal rats. Eur. J. Neurosci. 7:1995;1773-1790.
40. Kelley P.E., Frisina R.D., Zettel M.L., Walton J.P. Differential calbindin-like immunoreactivity in the brain stem auditory system of the chinchilla. J. Comp. Neurol. 320:1992;196-212.
41. Kotak V.C., Sanes D.H. Synaptically evoked prolonged depolarizations in the developing auditory system. J. Neurophysiol. 74:1995;1611-1620.
42. Kotak V.C., Sanes D.H. Developmental influence of glycinergic transmission: regulation of NMDA receptor-mediated EPSPs. J. Neurosci. 16:1996;1836-1843.
43. Kumoi K., Saito N., Tanaka C. Immunohistochemical localization of gamma-aminobutyric acid- and aspartate-containing neurons in the guinea pig superior olivary complex. Hear. Res. 68:1993;173-179.
44. Lohmann C., Friauf E. Distribution of the calcium-binding proteins parvalbumin and calretinin in the auditory brainstem of adult and developing rats. J. Comp. Neurol. 367:1996;90-109.
45. Martich-Kriss V., Kollias S.S., Ball W.S. Jr. MR findings in kernicterus. Am. J. Neuroradiol. 16:1995;819-821.
46. Matsubara J.A. Calbindin D-28K immunoreactivity in the cat's superior olivary complex. Brain Res. 508:1990;353-357.
47. McBurney R.N., Neering I.R. Neuronal calcium homeostasis. Trends Neurosci. 10:1987;164-169.
48. Morino-Wannier P., Fujita S.C., Jones E.G. GABAergic neuronal populations in monkey primary auditory cortex defined by co-localized calcium binding proteins and surface antigens. Exp. Brain Res. 88:1992;422-432.
49. Pack A.K., Slepecky N.B. Cytoskeletal and calcium-binding proteins in the mammalian organ of Corti: cell type-specific proteins displaying longitudinal and radial gradients. Hear. Res. 91:1995;119-135.
50. Rose A.L., Wisniewski H. Acute bilirubin encephalopathy induced with sulfadimethoxine in Gunn rats. J. Neuropathol. Exp. Neurol. 38:1979;152-165.
51. Salley L.H., Shaia W.T., Sismanis A., Shapiro S.M., Spencer R.F. Calcium-binding protein expression in the cochlea of the jaundiced Gunn rat. Pediatr. Res. 1999;45.
52. Sanes D.H., Takacs C. Activity-dependent refinement of inhibitory connections. Eur. J. Neurosci. 5:1993;570-574.
53. Schofield B.R., Cant N.B. Organization of the superior olivary complex in the guinea pig: II. Patterns of projection from the periolivary nuclei to the inferior colliculus. J. Comp. Neurol. 317:1992;438-455.
54. Schutta H.S., Johnson L. Clinical signs and morphologic abnormalities in Gunn rats treated with sulfadimethoxine. J. Pediatr. 75:1969;1070-1079.
55. Seto-Ohshima A., Aoki E., Semba R., Emson P.C., Heizmann C.W. Parvalbumin immunoreactivity in the central auditory system of the gerbil: a developmental study. Neurosci. Lett. 119:1990;60-63.
56. Shapiro S.M. Acute brainstem auditory evoked potential abnormalities in jaundiced Gunn rats given sulfonamide. Pediatr. Res. 23:1988;306-310.
57. Shapiro S.M. Binaural effects in brainstem auditory evoked potentials of jaundiced Gunn rats. Hear. Res. 53:1991;41-48.
58. Shapiro S.M. Reversible brainstem auditory evoked potential abnormalities in jaundiced Gunn rats given sulfonamide. Pediatr. Res. 34:1993;629-633.
59. Shapiro S.M. Brainstem auditory evoked potentials in an experimental model of bilirubin neurotoxicity. Clin. Pediatr. (Philadelphia). 33:1994;460-467.
60. Shapiro S.M., Conlee J.W. Brainstem auditory evoked potentials correlate with morphological changes in Gunn rat pups. Hear. Res. 57:1991;16-22.
61. Shapiro S.M., Hecox K.E. Development of brainstem auditory evoked potentials in heterozygous and homozygous jaundiced Gunn rats. Brain Res. 469:1988;147-157.
62. Shapiro S.M., Hecox K.E. Brain stem auditory evoked potentials in jaundiced Gunn rats. Ann. Otol. Rhinol. Laryngol. 98:1989;308-317.
63. Shapiro S.M., Te Selle M.E. Cochlear microphonics in the jaundiced Gunn rat. Am. J. Otolaryngol. 15:1994;129-137.
64. Silverman W.A., Andersen D.H., Blanc W.A., Crozier D.N. A difference in mortality rate and incidence of kernicterus among premature infants allotted to two prophylactic antibacterial regimens. Pediatrics. 18:1956;614-625.
65. Solbach S., Celio M.R. Ontogeny of the calcium binding protein parvalbumin in the rat nervous system. Anat. Embryol. (Berl.). 184:1991;103-124.
66. Spitzer M.W., Semple M.N. Neurons sensitive to interaural phase disparity in gerbil superior olive: diverse monaural and temporal response properties. J. Neurophysiol. 73:1995;1668-1690.
67. Starr A., Picton T.W., Sininger Y., Hood L.J., Berlin C.I. Auditory neuropathy. Brain. 119:1996;741-753.
68. Strebel L., Odell G.B. Bilirubin uridine disphosphoglucuronyltransferase in rat liver microsomes: genetic variation and maturation. Pediatr. Res. 5:1971;548-559.
69. Sturrock R., Y J.J. A quantitative histological study of changes in neurons and glia in the Gunn rat. Neuropathol. Appl. Neurobiol. 4:1978;209-223.
70. Tsuchitani, C., Johnson, D.H., 1991. In: Altschuler, R.A., Bobbin, R.P., Clopton, B.M., Hoffman, D.W. (Eds.), Neurobiology of Hearing: The Central Auditory System. Raven Press, New York, pp. 163-193.
71. Usami S., Shinkawa H., Inoue Y., Kanzaki J., Anniko M. Calbindin-D28K localization in the primate inner ear. ORL J. Otorhinolaryngol. Relat. Spec. 57:1995;94-99.
72. Uziel A., Marot M., Pujol R. The Gunn rat: an experimental model for central deafness. Acta Otolaryngol. 95:1983;651-656.
73. Watchko J.F., Claassen D. Kernicterus in premature infants: current prevalence and relationship to NICHD Phototherapy Study exchange criteria. Pediatrics. 93:1994;996-999.
74. Webster W.R., Batini C., Buisseret-Delmas C., Compoint C., Guegan M., Thomasset M. Colocalization of calbindin and GABA in medial nucleus of the trapezoid body of the rat. Neurosci. Lett. 111:1990;252-257.
75. Wenthold, R.J., 1991. In: Altschuler, R.A., Bobbin, R.P., Clopton, B.M., Hoffman, D.W. (Eds.), Neurobiology of Hearing: The Central Auditory System. Raven Press, New York, pp. 121-139.
76. Yokochi K. Magnetic resonance imaging in children with kernicterus. Acta Paediatr. 84:1995;937-939.