Postnatal glucocorticoid-induced hypomyelination, gliosis, and neurologic deficits are dose-dependent, preparation-specific, and reversible

Experimental Neurology

Volumn 263, Issue , 2015, Pages 200-213

  Zia, Muhammad T K ^a,b   Vinukonda, Govindaiah ^a   Vose, Linnea R ^a   Bhimavarapu, Bala B R ^a   Iacobas, Sanda ^a   Pandey, Nishi K ^a   Beall, Ann Marie ^b   Dohare, Preeti ^a   LaGamma, Edmund F ^a   Iacobas, Dumitru A ^a   Ballabh, Praveen ^a  

^a NEW YORK MEDICAL COLLEGE   (United States)

^b Department of Pharmacy Hudson Valley Hospital   (United States)

Author keywords

Astrocytes; Betamethasone; Dexamethasone; Glucocorticoids; Myelination; Oligodendrocytes

Indexed keywords

BETAMETHASONE; DEXAMETHASONE; MIFEPRISTONE; MITOGEN ACTIVATED PROTEIN KINASE; MYELIN BASIC PROTEIN; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; ASTROCYTOSIS; CELL CYCLE; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; DEMYELINATION; DEVELOPMENTAL DISORDER; FEMALE; GENE MUTATION; GLIOSIS; MALE; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; MYELINATION; NEUROLOGIC DISEASE; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGODENDROGLIA; PERINATAL PERIOD; PROTEIN EXPRESSION; RABBIT; TRANSCRIPTOMICS; ANIMAL; BRAIN; CHEMICALLY INDUCED; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; IMMUNOHISTOCHEMISTRY; METABOLISM; MYELIN SHEATH; NEWBORN; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TUNEL ASSAY; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; BETAMETHASONE; BLOTTING, WESTERN; BRAIN; DEXAMETHASONE; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; GLIOSIS; GLUCOCORTICOIDS; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; MYELIN SHEATH; RABBITS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, GLUCOCORTICOID;

EID: 84910652825     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2014.09.013     Document Type: Article

References (63)

1. Abraham I., Harkany T., Horvath K.M., Veenema A.H., Penke B., Nyakas C., Luiten P.G. Chronic corticosterone administration dose-dependently modulates Abeta(1-42)- and NMDA-induced neurodegeneration in rat magnocellular nucleus basalis. J. Neuroendocrinol. 2000, 12:486-494.
2. Bakker J.M., van Bel F., Heijnen C.J. Neonatal glucocorticoids and the developing brain: short-term treatment with life-long consequences?. Trends Neurosci. 2001, 24:649-653.
3. Ballabh P., Xu H., Hu F., Braun A., Smith K., Rivera A., Lou N., Ungvari Z., Goldman S.A., Csiszar A., Nedergaard M. Angiogenic inhibition reduces germinal matrix hemorrhage. Nat. Med. 2007, 13:477-485.
4. Barres B.A., Lazar M.A., Raff M.C. A novel role for thyroid hormone, glucocorticoids and retinoic acid in timing oligodendrocyte development. Development 1994, 120:1097-1108.
5. Barrington K.J. The adverse neuro-developmental effects of postnatal steroids in the preterm infant: a systematic review of RCTs. BMC Pediatr. 2001, 1:1.
6. Baud O., Foix-L'Helias L., Kaminski M., Audibert F., Jarreau P.H., Papiernik E., Huon C., Lepercq J., Dehan M., Lacaze-Masmonteil T. Antenatal glucocorticoid treatment and cystic periventricular leukomalacia in very premature infants. N. Engl. J. Med. 1999, 341:1190-1196.
7. Baud O., Verney C., Evrard P., Gressens P. Injectable dexamethasone administration enhances cortical GABAergic neuronal differentiation in a novel model of postnatal steroid therapy in mice. Pediatr. Res. 2005, 57:149-156.
8. Bohn M.C., Friedrich V.L. Recovery of myelination in rat optic nerve after developmental retardation by cortisol. J. Neurosci. 1982, 2:1292-1298.
9. Buser J.R., Maire J., Riddle A., Gong X., Nguyen T., Nelson K., Luo N.L., Ren J., Struve J., Sherman L.S., Miller S.P., Chau V., Hendson G., Ballabh P., Grafe M.R., Back S.A. Arrested preoligodendrocyte maturation contributes to myelination failure in premature infants. Ann. Neurol. 2012, 71:93-109.
10. Cambonie G., Mesnage R., Milesi C., Pidoux O., Veyrac C., Picaud J.C. Betamethasone impairs cerebral blood flow velocities in very premature infants with severe chronic lung disease. J. Pediatr. 2008, 152:270-275.
11. Chua C.O., Chahboune H., Braun A., Dummula K., Chua C.E., Yu J., Ungvari Z., Sherbany A.A., Hyder F., Ballabh P. Consequences of intraventricular hemorrhage in a rabbit pup model. Stroke 2009, 40:3369-3377.
12. Claessens S.E., Belanoff J.K., Kanatsou S., Lucassen P.J., Champagne D.L., Ronald de Kloet E. Acute effects of neonatal dexamethasone treatment on proliferation and astrocyte immunoreactivity in hippocampus and corpus callosum: towards a rescue strategy. Brain Res. 2012, 1482:1-12.
13. Clancy B., Luo L., Thomas J.E. Observation of nearly perfect irrotational flow in normal and superfluid strongly interacting Fermi gases. Phys. Rev. Lett. 2007, 99:140401.
14. Coulter D.M., LaPine T., Gooch W.M. Intraventricular hemorrhage in the premature rabbit pup. Limitations of this animal model. J. Neurosurg. 1984, 60:1243-1245.
15. Craig D.B., Kannan S., Dombkowski A.A. Augmented annotation and orthologue analysis for Oryctolagus cuniculus: better bunny. BMC Bioinforma. 2012, 13:84.
16. Crotty K.C., Ahronovich M.D., Baron I.S., Baker R., Erickson K., Litman F.R. Neuropsychological and behavioral effects of postnatal dexamethasone in extremely low birth weight preterm children at early school age. J. Perinatol. 2012, 32:139-146.
17. DeBattista C., Belanoff J. The use of mifepristone in the treatment of neuropsychiatric disorders. Trends Endocrinol. Metab. 2006, 17:117-121.
18. DeCastro M., El-Khoury N., Parton L., Ballabh P., LaGamma E.F. Postnatal betamethasone vs dexamethasone in premature infants with bronchopulmonary dysplasia: a pilot study. J. Perinatol. 2009, 29:297-304.
19. Doyle L.W., Ehrenkranz R.A., Halliday H.L. Early (<8days) postnatal corticosteroids for preventing chronic lung disease in preterm infants. Cochrane Database Syst. Rev. 2014, 5. CD001146.
20. Doyle L.W., Ehrenkranz R.A., Halliday H.L. Late (>7days) postnatal corticosteroids for chronic lung disease in preterm infants. Cochrane Database Syst. Rev. 2014, 5. CD001145.
21. Duksal F., Kilic I., Tufan A.C., Akdogan I. Effects of different corticosteroids on the brain weight and hippocampal neuronal loss in rats. Brain Res. 2009, 1250:75-80.
22. Dummula K., Vinukonda G., Chu P., Xing Y., Hu F., Mailk S., Csiszar A., Chua C., Mouton P., Kayton R.J., Brumberg J.C., Bansal R., Ballabh P. Bone morphogenetic protein inhibition promotes neurological recovery after intraventricular hemorrhage. J. Neurosci. 2011, 31:12068-12082.
23. Durand M., Mendoza M.E., Tantivit P., Kugelman A., McEvoy C. A randomized trial of moderately early low-dose dexamethasone therapy in very low birth weight infants: dynamic pulmonary mechanics, oxygenation, and ventilation. Pediatrics 2002, 109:262-268.
24. Ghoumari A.M., Ibanez C., El-Etr M., Leclerc P., Eychenne B., O'Malley B.W., Baulieu E.E., Schumacher M. Progesterone and its metabolites increase myelin basic protein expression in organotypic slice cultures of rat cerebellum. J. Neurochem. 2003, 86:848-859.
25. Gokhan S., Marin-Husstege M., Yung S.Y., Fontanez D., Casaccia-Bonnefil P., Mehler M.F. Combinatorial profiles of oligodendrocyte-selective classes of transcriptional regulators differentially modulate myelin basic protein gene expression. J. Neurosci. 2005, 25:8311-8321.
26. Grier D.G., Halliday H.L. Corticosteroids in the prevention and management of bronchopulmonary dysplasia. Semin. Neonatol. 2003, 8:83-91.
27. Gross S.J., Anbar R.D., Mettelman B.B. Follow-up at 15years of preterm infants from a controlled trial of moderately early dexamethasone for the prevention of chronic lung disease. Pediatrics 2005, 115:681-687.
28. Halliday H.L., Ehrenkranz R.A., Doyle L.W. Moderately early (7-14days) postnatal corticosteroids for preventing chronic lung disease in preterm infants. Cochrane Database Syst. Rev. 2003, CD001144.
29. Huang W.L., Harper C.G., Evans S.F., Newnham J.P., Dunlop S.A. Repeated prenatal corticosteroid administration delays myelination of the corpus callosum in fetal sheep. Int. J. Dev. Neurosci. 2001, 19:415-425.
30. Iacobas D.A., Iacobas S., Urban-Maldonado M., Scemes E., Spray D.C. Similar transcriptomic alterations in Cx43 knockdown and knockout astrocytes. Cell Commun. Adhes. 2008, 15:195-206.
31. Ishii A., Fyffe-Maricich S.L., Furusho M., Miller R.H., Bansal R. ERK1/ERK2 MAPK signaling is required to increase myelin thickness independent of oligodendrocyte differentiation and initiation of myelination. J. Neurosci. 2012, 32:8855-8864.
32. Jenkins S.I., Pickard M.R., Khong M., Smith H.L., Mann C.L., Emes R.D., Chari D.M. Identifying the cellular targets of drug action in the central nervous system following corticosteroid therapy. ACS Chem. Neurosci. 2014, 5:51-63.
33. Jones R.A. Randomized, controlled trial of dexamethasone in neonatal chronic lung disease: 13- to 17-year follow-up study: I. Neurologic, psychological, and educational outcomes. Pediatrics 2005, 116:370-378. Collaborative Dexamethasone Trial Follow-up, G.
34. Kim J.W., Kim Y.J., Chang Y.P. Administration of dexamethasone to neonatal rats induces hypomyelination and changes in the morphology of oligodendrocyte precursors. Comp. Med. 2013, 63:48-54.
35. Lorch S.A., Baiocchi M., Ahlberg C.E., Small D.S. The differential impact of delivery hospital on the outcomes of premature infants. Pediatrics 2012, 130:270-278.
36. Malaeb S.N., Hovanesian V., Sarasin M.D., Hartmann S.M., Sadowska G.B., Stonestreet B.S. Effects of maternal antenatal glucocorticoid treatment on apoptosis in the ovine fetal cerebral cortex. J. Neurosci. Res. 2009, 87:179-189.
37. Maloney S.E., Noguchi K.K., Wozniak D.F., Fowler S.C., Farber N.B. Long-term effects of multiple glucocorticoid exposures in neonatal mice. Behav. Sci. (Basel) 2011, 1:4-30.
38. McEvoy C., Bowling S., Williamson K., McGaw P., Durand M. Randomized, double-blinded trial of low-dose dexamethasone: II. Functional residual capacity and pulmonary outcome in very low birth weight infants at risk for bronchopulmonary dysplasia. Pediatr. Pulmonol. 2004, 38:55-63.
39. Mouton P.R., Chachich M.E., Quigley C., Spangler E., Ingram D.K. Caloric restriction attenuates amyloid deposition in middle-aged dtg APP/PS1 mice. Neurosci. Lett. 2009, 464:184-187.
40. Murphy B.P., Inder T.E., Huppi P.S., Warfield S., Zientara G.P., Kikinis R., Jolesz F.A., Volpe J.J. Impaired cerebral cortical gray matter growth after treatment with dexamethasone for neonatal chronic lung disease. Pediatrics 2001, 107:217-221.
41. Okret S., Poellinger L., Dong Y., Gustafsson J.A. Down-regulation of glucocorticoid receptor mRNA by glucocorticoid hormones and recognition by the receptor of a specific binding sequence within a receptor cDNA clone. Proc. Natl. Acad. Sci. U. S. A. 1986, 83:5899-5903.
42. Powell K., Kerkering K.W., Barker G., Rozycki H.J. Dexamethasone dosing, mechanical ventilation and the risk of cerebral palsy. J. Matern. Fetal Neonatal Med. 2006, 19:43-48.
43. Pozniak C.D., Langseth A.J., Dijkgraaf G.J., Choe Y., Werb Z., Pleasure S.J. Sox10 directs neural stem cells toward the oligodendrocyte lineage by decreasing suppressor of fused expression. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:21795-21800.
44. Shinwell E.S., Karplus M., Reich D., Weintraub Z., Blazer S., Bader D., Yurman S., Dolfin T., Kogan A., Dollberg S., Arbel E., Goldberg M., Gur I., Naor N., Sirota L., Mogilner S., Zaritsky A., Barak M., Gottfried E. Early postnatal dexamethasone treatment and increased incidence of cerebral palsy. Arch. Dis. Child. Fetal Neonatal Ed. 2000, 83:F177-F181.
45. Stahn C., Buttgereit F. Genomic and nongenomic effects of glucocorticoids. Nat. Clin. Pract. Rheumatol. 2008, 4:525-533.
46. Stolt C.C., Rehberg S., Ader M., Lommes P., Riethmacher D., Schachner M., Bartsch U., Wegner M. Terminal differentiation of myelin-forming oligodendrocytes depends on the transcription factor Sox10. Genes Dev. 2002, 16:165-170.
47. Taylor C., Shah P.S., Dunn M.S. Meta-analysis of postnatal steroid use challenged. Pediatrics 2002, 109:716-717. (author reply 716-717).
48. Trenque T., Lamiable D., Vistelle R., Millart H., Leperre A., Choisy H. Comparative pharmacokinetics of two diastereoisomers dexamethasone and betamethasone in plasma and cerebrospinal fluid in rabbits. Fundam. Clin. Pharmacol. 1994, 8:430-436.
49. Truffert P., Empana J.P., Breart G., Saugstad O.D., Goelz R., Halliday H.L., Anceschi M. Treatment strategies for bronchopulmonary dysplasia with postnatal corticosteroids in Europe: the EURAIL survey. Acta Paediatr. 2003, 92:948-951.
50. Tsuneishi S., Takada S., Motoike T., Ohashi T., Sano K., Nakamura H. Effects of dexamethasone on the expression of myelin basic protein, proteolipid protein, and glial fibrillary acidic protein genes in developing rat brain. Brain Res. Dev. Brain Res. 1991, 61:117-123.
51. Unemura K., Kume T., Kondo M., Maeda Y., Izumi Y., Akaike A. Glucocorticoids decrease astrocyte numbers by reducing glucocorticoid receptor expression in vitro and in vivo. J. Pharmacol. Sci. 2012, 119:30-39.
52. Uno H., Lohmiller L., Thieme C., Kemnitz J.W., Engle M.J., Roecker E.B., Farrell P.M. Brain damage induced by prenatal exposure to dexamethasone in fetal rhesus macaques. I. Hippocampus. Brain Res. Dev. Brain Res. 1990, 53:157-167.
53. Uno H., Eisele S., Sakai A., Shelton S., Baker E., DeJesus O., Holden J. Neurotoxicity of glucocorticoids in the primate brain. Horm. Behav. 1994, 28:336-348.
54. Velasco-Miguel S., Buckbinder L., Jean P., Gelbert L., Talbott R., Laidlaw J., Seizinger B., Kley N. PA26, a novel target of the p53 tumor suppressor and member of the GADD family of DNA damage and growth arrest inducible genes. Oncogene 1999, 18:127-137.
55. Vermont Oxford Network Steroid Study, G. Early postnatal dexamethasone therapy for the prevention of chronic lung disease. Pediatrics 2001, 108:741-748.
56. Vielkind U., Walencewicz A., Levine J.M., Bohn M.C. Type II glucocorticoid receptors are expressed in oligodendrocytes and astrocytes. J. Neurosci. Res. 1990, 27:360-373.
57. Vinukonda G., Dummula K., Malik S., Hu F., Thompson C.I., Csiszar A., Ungvari Z., Ballabh P. Effect of prenatal glucocorticoids on cerebral vasculature of the developing brain. Stroke 2010, 41:1766-1773.
58. Walther F.J., Findlay R.D., Durand M. Adrenal suppression and extubation rate after moderately early low-dose dexamethasone therapy in very preterm infants. Early Hum. Dev. 2003, 74:37-45.
59. Watterberg K.L. Policy statement-postnatal corticosteroids to prevent or treat bronchopulmonary dysplasia. Pediatrics 2010, 126:800-808.
60. Watterberg K. Evidence-based neonatal pharmacotherapy: postnatal corticosteroids. Clin. Perinatol. 2012, 39:47-59.
61. Wilson-Costello D., Friedman H., Minich N., Fanaroff A.A., Hack M. Improved survival rates with increased neurodevelopmental disability for extremely low birth weight infants in the 1990s. Pediatrics 2005, 115:997-1003.
62. Yates H.L., Newell S.J. Postnatal intravenous steroids and long-term neurological outcome: recommendations from meta-analyses. Arch. Dis. Child. Fetal Neonatal Ed. 2012, 97:F299-F303.
63. Yeh T.F., Lin Y.J., Lin H.C., Huang C.C., Hsieh W.S., Lin C.H., Tsai C.H. Outcomes at school age after postnatal dexamethasone therapy for lung disease of prematurity. N. Engl. J. Med. 2004, 350:1304-1313.