Minocycline protects the immature white matter against hyperoxia

Experimental Neurology

Volumn 254, Issue , 2014, Pages 153-165

  Schmitz, Thomas ^a   Krabbe, Grietje ^b   Weikert, Georg ^a   Scheuer, Till ^a   Matheus, Friederike ^a   Wang, Yan ^a   Mueller, Susanne ^a   Kettenmann, Helmut ^b   Matyash, Vitali ^b   Bührer, Christoph ^a   Endesfelder, Stefanie ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

Hyperoxia; Hypomyelination; Immature brain; Microglial activation; Minocycline; Neuroprotection; Preterm infants; White matter damage

Indexed keywords

CYTOKINE; INTERLEUKIN 1BETA; MINOCYCLINE; OXYGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ACTIVATION; CELL MATURATION; CELL PROLIFERATION; CELL SURVIVAL; CYTOKINE RELEASE; DIFFUSION TENSOR IMAGING; HYPEROXIA; LONG TERM EXPOSURE; MICROGLIAL CELL CULTURE; NEURAL STEM CELL; NEUROPROTECTION; NEWBORN; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OLIGODENDROGLIA; OXYGEN CONCENTRATION; OXYGEN TENSION; PREMATURE LABOR; PRIORITY JOURNAL; RAT; WHITE MATTER INJURY;

HYPEROXIA; HYPOMYELINATION; IMMATURE BRAIN; MICROGLIAL ACTIVATION; MINOCYCLINE; NEUROPROTECTION; PRETERM INFANTS; WHITE MATTER DAMAGE;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; ANTI-BACTERIAL AGENTS; DIFFUSION TENSOR IMAGING; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; HYPEROXIA; INFANT, NEWBORN; LEUKOENCEPHALOPATHIES; MALE; MICROGLIA; MINOCYCLINE; NERVE FIBERS, MYELINATED; NEUROPROTECTIVE AGENTS; OLIGODENDROGLIA; PREGNANCY; PRIMARY CELL CULTURE; RATS; RATS, WISTAR;

EID: 84896721258     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2014.01.017     Document Type: Article

References (54)

1. Arvin K., Han B., Du Y., Lin S., Paul S., Holtzman D. Minocycline markedly protects the neonatal brain against hypoxic-ischemic injury. Ann. Neurol. 2002, 52:54-61.
2. Back S., Gan X., Li Y., Rosenberg P., Volpe J. Maturation-dependent vulnerability of oligodendrocytes to oxidative stress-induced death caused by glutathione depletion. J. Neurosci. 1998, 18:6241-6253.
3. Bansal R., Pfeiffer S. Reversible inhibition of oligodendrocyte progenitor differentiation by a monoclonal antibody against surface galactolipids. Proc. Natl. Acad. Sci. U. S. A. 1989, 86:181-185.
4. Bell M.J., Hallenbeck J.M. Effects of intrauterine inflammation on developing rat brain. J. Neurosci. Res. 2002, 15:570-579.
5. Buller K., Carty M., Reinebrant H., Wixey J. Minocycline: a neuroprotective agent for hypoxic-ischemic brain injury in the neonate?. J. Neurosci. Res. 2009, 87:599-608.
6. Burd I., Balakrishnan B., Kannan S. Models of fetal brain injury, intrauterine inflammation, and preterm birth. Am. J. Reprod. Immunol. 2012, 67:287-294.
7. Cai Z., Lin S., Fan L., Pang Y., Rhodes P. Minocycline alleviates hypoxic-ischemic injury to developing oligodendrocytes in the neonatal rat brain. Neuroscience 2006, 137:425-435.
8. Cai Z., Yan Y., Chen R. Minocycline reduces astrocytic reactivation and neuroinflammation in the hippocampus of a vascular cognitive impairment rat model. Neurosci. Bull. 2010, 26:28-36.
9. Cande C., Cohen I., Daugas E., Ravagnan L., Larochette N. Apoptosis-inducing factor (AIF): a novel caspase-independent death effector released from mitochondria. Biochimie 2002, 84:215-222.
10. Castillo A., Sola A., Baquero H., Neira F., Alvis R., Deulofeut R., Critz A. Pulse oxygen saturation levels and arterial oxygen tension values in newborns receiving oxygen therapy in the neonatal intensive care unit: is 85% to 93% an acceptable range?. Pediatrics 2008, 121:882-889.
11. Chahboune H., Ment L., Stewart W., Douglas L., Rothman D., Vaccarino F., Hyder F., Schwartz M. Hypoxic injury during neonatal development in murine brain: correlation between in vivo DTI findings and behavioral assessment. Cereb. Cortex 2009, 12:2891-2901.
12. Chen S.D., Yin J.H., Hwang C.S., Tang C.M., Yang D.I. Anti-apoptotic and anti-oxidative mechanisms of minocycline against sphingomyelinase/ceramide neurotoxicity: implication in Alzheimer's disease and cerebral ischemia. Free Radic. Res. 2012, 46:940-950.
13. Chew L., King W., Kennedy A., Gallo V. Interferon-gamma inhibits cell cycle exit in differentiating oligodendrocyte progenitor cells. Glia 2005, 52:127-143.
14. Collins M., Lorenz J., Jetton J., Paneth N. Hypocapnia and other ventilation-related risk factors for cerebral palsy in low birth weight infants. Pediatr. Res. 2001, 50:712-719.
15. Curtis R., Cohen J., Fok-Seang J., Hanley M., Gregson N., Reynolds R., Wilkin G.P. Development of macroglial cells in rat cerebellum. I. Use of antibodies to follow early in vivo development and migration of oligodendrocytes. J. Neurocytol. 1988, 17:43-54.
16. Deulofeut R., Dudell G., Sola A. Treatment-by-gender effect when aiming to avoid hyperoxia in preterm infants in the NICU. Acta Paediatr. 2007, 96:990-994.
17. Fan L., Pang Y., Lin S., Tien L., Ma T., Rhodos P., Cai Z. Minocycline reduces lipopolysaccharide-induced neurological dysfunction and brain injury in the neonatal rat. J. Neurosci. Res. 2005, 82:71-82.
18. Fan L., Mitchell H., Tien L., Rhodes P., Cai Z. Interleukin-1beta-induced brain injury in the neonatal rat can be ameliorated by alpha-phenyl-n-tert-butyl-nitrone. Exp. Neurol. 2009, 220:143-153.
19. Favrais G., van de Looij Y., Fleiss B., Ramanantsoa N., Bonnin P., Stoltenburg-Didinger G., Lacaud A., Saliba E., Dammann O., Gallego J., Sizonenko S., Hagberg H., Lelièvre V., Gressens P. Systemic inflammation disrupts the developmental program of white matter. Ann. Neurol. 2011, 70:550-565.
20. Felderhoff-Mueser U., Sifringer M., Jarosz B., Korobowicz E., Mahler L., Piening T., Moysich A., Grune T., Thor F., Heumann R., Bührer C., Ikonomidou C. Oxygen causes cell death in the developing brain. Neurobiol. Dis. 2004, 17:273-282.
21. Felderhoff-Mueser U., Sifringer M., Polley O., Dzietko M., Leineweber B., Mahler L., Baier M., Bittigau P., Obladen M., Ikonomidou C., Buehrer C. Caspase-1-processed interleukins in hyperoxia-induced cell death in the developing brain. Ann. Neurol. 2005, 57:50-59.
22. Feldman H., Lee E., Loe I., Yeom K., Grill-Spector K., Luna B. White matter microstructure on diffusion tensor imaging is associated with conventional magnetic resonance imaging findings and cognitive function in adolescents born preterm. Dev. Med. Child Neurol. 2012, 54:809-814.
23. French H., Reid M., Mamontov P., Simmons R., Grinspan J. Oxidative stress disrupts oligodendrocyte maturation. J. Neurosci. Res. 2009, 87:3076-3087.
24. Gallo V., Armstrong R. Developmental and growth factor induced regulation of nestin in oligodendrocyte lineage cells. J. Neurosci. 1995, 15:394-406.
25. Gerstner B., Bührer C., Rheinländer C., Polley O., Schülle r.A., Berns M., Obladen M., Felderhoff-Mueser U. Maturation-dependent oligodendrocyte apoptosis caused by hyperoxia. J. Neurosci. Res. 2006, 84:306-315.
26. Hanisch U., Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat. Neurosci. 2007, 10:1387-1394.
27. Horsfield M., Jones D. Applications of diffusion-weighted and diffusion tensor MRI to white matter diseases - a review. NMR Biomed. 2002, 15.
28. Huang T., Zou Y., Corniola R. Oxidative stress and adult neurogenesis-effects of radiation and superoxide dismutase deficiency. Semin. Cell Dev. Biol. 2012, 23:738-744.
29. Huppi P.S., Dubois J. Diffusion tensor imaging of brain development. Neonatal Med. J. 2006, 11:489-497.
30. Lampl Y., Boaz M., Gilad R., Lorberboym M., Dabby R., Rapoport A., Anca-Hershkowitz M., M.S. Minocycline treatment in acute stroke: an open-label, evaluator-blinded study. Neurology 2007, 69:1404-1410.
31. Leigh M., Nguyen D., Mu Y., Winarni T., Schneider A., Chechi T., Polussa J., Doucet P., Tassone F., Rivera S., Hess l.D., Hagerman R. A randomized double-blind, placebo-controlled trial of minocycline in children and adolescents with fragile x syndrome. J. Dev. Behav. Pediatr. 2013, 34:147-155.
32. Leviton A., Dammann O. Coagulation, inflammation, and the risk of neonatal white matter damage. Pediatr. Res. 2004, 55:541-545.
33. Leviton A., Allred E., Kuban K., Dammann O., O'Shea T., Hirtz D., Schreiber M., Paneth N., ELGAN Study Investigators Early blood gas abnormalities and the preterm brain. Am. J. Epidemiol. 2010, 172:907-916.
34. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
35. McCarthy K., de Vellis J. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J. Cell Biol. 1980, 85:890-902.
36. McClain J., Morris S., Deeny M., Marshall S., Hayes D., Kiser Z., Nixon K. Adolescent binge alcohol exposure induces long-lasting partial activation of microglia. Brain Behav. Immun. 2001, 25:S120-S128.
37. Moseley M. Diffusion tensor imaging and aging - a review. NMR Biomed. 2002, 15:553-560.
38. Nelson K.B., Dambrosia J.M., Grether J.K., Phillips T.M. Neonatal cytokines and coagulation factors in children with cerebral palsy. Ann. Neurol. 1998, 44:665-675.
39. Pajevic S., Pierpaoli C. Color schemes to represent the orientation of anisotropic tissues from diffusion tensor data: application to white matter fiber tract mapping in the human brain. Magn. Reson. Med. 1999, 42:526-540.
40. Pardo C., Buckley A., Thurm A., Lee L., Azhagiri A., Neville D., Swedo S. A pilot open-label trial of minocycline in patients with autism and regressive features. J. Neurodev. Disord. 2013, 8:9.
41. Pistollato F., Chen H., Schwartz P., Basso G., Panchision D. Oxygen tension controls the expansion of human CNS precursors and the generation of astrocytes and oligodendrocytes. Mol. Cell. Neurosci. 2007, 35:424-435.
42. Rose J., Butler E., Lamont L., Barnes P., Atlas S., Stevenson D. Neonatal brain structure on MRI and diffusion tensor imaging, sex, and neurodevelopment in very-low-birthweight preterm children. Dev. Med. Child Neurol. 2009, 51:526-535.
43. Schmitz T., Ritter J., Mueller S., Felderhoff-Mueser U., Chew L., Gallo V. Cellular changes underlying hyperoxia-induced delay of white matter development. J. Neurosci. 2011, 31:4327-4344.
44. Schmitz T., Endesfelder S., Reinert M., Klinker F., Müller S., Bührer C., Liebetanz D. Adolescent hyperactivity and impaired coordination after neonatal hyperoxia. Exp. Neurol. 2012, 235:347-349.
45. Skranes J., Vangberg T., Kulseng S., Indredavik M., Evensen K., Martinussen M., Dale A., Haraldseth O., Brubakk A. Clinical findings and white matter abnormalities seen on diffusion tensor imaging in adolescents with very low birth weight. Brain 2007, 130:654-666.
46. Song W., Su H., Song S., Paudel H., Schipper H. Over-expression of heme oxygenase-1 promotes oxidative mitochondrial damage in rat astroglia. J. Cell. Physiol. 2006, 206:655-663.
47. Susin S., Lorenzo H., Zamzami N., Marzo I., Snow B., Brothers G., Mangion J., Jacotot E., Costantini P., Loeffler M., Larochette N., Goodlett D., Aebersold R., Siderovski D., Penninger J., Kroemer G. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999, 397:441-446.
48. Tang M., Alexander H., Clark R., Kochanek P., Kagan V., Bayir H. Minocycline reduces neuronal death and attenuates microglial response after pediatric asphyxial cardiac arrest. J. Cereb. Blood Flow Metab. 2010, 30:119-129.
49. Volpe J. Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol. 2009, 8:110-120.
50. Vottier G., Pham H., Pansiot J., Biran V., Gressens P., Charriaut-Marlangue C., Baud O. Deleterious effect of hyperoxia at birth on white matter damage in the newborn rat. Dev. Neurosci. 2011, 33:261-269.
51. Yan H., Rivkees S.A. Hypoglycemia influences oligodendrocyte development and myelin formation. Neuroreport 2006, 17:55-59.
52. Yoon B.H., Romero R., Kim C.J., Koo J.N., Choe G., Syn H.C., Chi J.G. High expression of tumor necrosis factor-alpha and interleukin-6 in periventricular leukomalacia. Am. J. Obstet. Gynecol. 1997, 177:406-411.
53. Yuan X., Eisen A., McBain C., Gallo V. A role for glutamate and its receptors in the regulation of oligodendrocyte development in cerebellar tissue slices. Development 1998, 125:2901-2914.
54. Zabad R.K., Metz L.M., Todoruk T.R., Zhang Y., Mitchell J.R., Yeung M., Patry D.G., Bell R.B., Yong V.W. The clinical response to minocycline in multiple sclerosis is accompanied by beneficial immune changes: a pilot study. Mult. Scler. 2007, 13:517-526.