Inhaled NO prevents hyperoxia-induced white matter damage in neonatal rats

Experimental Neurology

Volumn 252, Issue , 2014, Pages 114-123

  Pham, Hoa ^a,b,c   Vottier, Gaelle ^a,b,c   Pansiot, Julien ^a,b,c   Duong Quy, Sy ^d   Bollen, Bieke ^a,b,c,e   Dalous, Jérémie ^a,b,c   Gallego, Jorge ^a,b,c   Mercier, Jean Christophe ^b,f   Dinh Xuan, Anh Tuan ^d   Bonnin, Philippe ^b,g,h   Charriaut Marlangue, Christiane ^a,b,c   Baud, Olivier ^a,b,c,f  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c Fondation PremUP   (France)

^d Institut Cochin   (France)

^e UNIVERSITY OF LEUVEN   (Belgium)

^f ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^g Université René Diderot   (France)

^h HÔPITAL LARIBOISIÈRE   (France)

Author keywords

Developing brain; Hyperoxia; Neuroprotection; Nitric oxide; White matter damage

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIN DEPENDENT KINASE INHIBITOR 1B; NITRIC OXIDE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASSOCIATION; BRAIN TISSUE; CELL DEATH; CELL DENSITY; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE SEVERITY; DRUG EFFICACY; DRUG MECHANISM; ENCEPHALITIS; EXPOSURE; FEMALE; HISTOPATHOLOGY; HYPEROXIA; LOW DRUG DOSE; LUNG DYSPLASIA; MOLECULAR BIOLOGY; NEUROPROTECTION; NEWBORN; NONHUMAN; OLIGODENDROGLIA; PERINATAL PERIOD; PREMATURITY; PRIORITY JOURNAL; RAT; UPREGULATION; WHITE MATTER INJURY;

BPD; BRONCHOPULMONARY DYSPLASIA; CC3; CLEAVED CASPASE 3; DEVELOPING BRAIN; HYPEROXIA; INHALED NO; INO; MEAN LINEAR INTERCEPT; MLI; NEUROPROTECTION; NITRIC OXIDE; RAC; RADIAL ALVEOLAR COUNT; WHITE MATTER DAMAGE; WMD;

ADMINISTRATION, INHALATION; AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; ANOXIA; BLOOD GAS ANALYSIS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL DEATH; CYCLIN-DEPENDENT KINASE INHIBITOR P27; DISEASE MODELS, ANIMAL; FEMALE; LEUKOENCEPHALOPATHIES; LUNG; MALE; NEUROPROTECTIVE AGENTS; NITRIC OXIDE; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84891123404     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2013.11.025     Document Type: Article

References (46)

1. Anjari M., Counsell S.J., Srinivasan L., Allsop J.M., Hajnal J.V., Rutherford M.A., Edwards A.D. The association of lung disease with cerebral white matter abnormalities in preterm infants. Pediatrics 2009, 124:268-276.
2. Back S.A., Riddle A., McClure M.M. Maturation-dependent vulnerability of perinatal white matter in premature birth. Stroke 2007, 38:724-730.
3. Baud O., Daire J.L., Dalmaz Y., Fontaine R.H., Krueger R.C., Sebag G., Evrard P., Gressens P., Verney C. Gestational hypoxia induces white matter damage in neonatal rats: a new model of periventricular leukomalacia. Brain Pathol. 2004, 14:1-10.
4. Bonnin P., Leger P.L., Deroide N., Fau S., Baud O., Pocard M., Charriaut-Marlangue C., Renolleau S. Impact of intracranial blood-flow redistribution on stroke size during ischemia-reperfusion in 7-day-old rats. J Neurosci Methods 2011 May 15, 198(1):103-9.
5. Bonnin P., Leger P.L., Villapol S., Deroide N., Gressens P., Pocard M., Renolleau S., Baud O., Charriaut-Marlangue C. Dual action of NO synthases on blood flow and infarct volume consecutive to neonatal focal cerebral ischemia. Exp. Neurol. 2012, 236:50-57.
6. Bouslama M., Durand E., Chauvière L., Van den Bergh O., Gallego J. Olfactory classical conditioning in newborn mice. Behav. Brain Res. 2005, 161:102-106.
7. Charriaut-Marlangue C., Bonnin P., Gharib A., Leger P.L., Villapol S., Pocard M., Gressens P., Renolleau S., Baud O. Inhaled nitric oxide reduces brain damage by collateral recruitment in a neonatal stroke model. Stroke 2012, 43:3078-3084.
8. Charriaut-Marlangue C., Bonnin P., Pham H., Loron G., Leger P.L., Gressens P., Renolleau S., Baud O. Nitric oxide signaling in the brain: A new target for inhaled nitric oxide?. Ann. Neurol. 2013, 73:442-448.
9. Chiueh C.C. Neuroprotective properties of nitric oxide. Ann. N. Y. Acad. Sci. 1999, 890:301-311.
10. Cole F.S., Alleyne C., Barks J.D., Boyle R.J., Carroll J.L., Dokken D., Edwards W.H., Georgieff M., Gregory K., Johnston M.V., Kramer M., Mitchell C., Neu J., Pursley D.M., Robinson W.M., Rowitch D.H. NIH Consensus Development Conference statement: inhaled nitric-oxide therapy for premature infants. Pediatrics 2011, 127:363-369.
11. Dammann O., Leviton A., Bartels D.B., Dammann C.E. Lung and brain damage in preterm newborns. Are they related? How? Why?. Biol. Neonate 2004, 85:305-313.
12. Dunnill M.S. Quantitative methods in the study of pulmonary pathology. Thorax 1962, 17:320-328.
13. Emery J.L., Mithal A. The number of alveoli in the terminal respiratory unit of man during late intrauterine life and childhood. Arch. Dis. Child. 1960, 35:544-547.
14. Fontaine R.H., Olivier P., Massonneau V., Leroux P., Degos V., Lebon S., El Ghouzzi V., Lelièvre V., Gressens P., Baud O. Vulnerability of white matter towards antenatal hypoxia is linked to a species-dependent regulation of glutamate receptor subunits. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:16779-16784.
15. Gerstner B., DeSilva T.M., Genz K., Armstrong A., Brehmer F., Neve R.L., Felderhoff-Mueser U., Volpe J.J., Rosenberg P.A. Hyperoxia causes maturation-dependent cell death in the developing white matter. J. Neurosci. 2008, 28:1236-1245.
16. Haynes R.L., Baud O., Li J., Kinney H.C., Volpe J.J., Folkerth D.R. Oxidative and nitrative injury in periventricular leukomalacia: a review. Brain Pathol. 2005, 15:225-233.
17. Huang Z., Huang P.L., Panahian N., Dalkara T., Fishman M.C., Moskowitz M.A. Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science 1994, 265:1883-1885.
18. Iadecola C. Bright and dark sides of nitric oxide in ischemic brain injury. Trends Neurosci. 1997, 20:132-139.
19. Ikonomidou C., Kaindl A.M. Neuronal death and oxidative stress in the developing brain. Antioxid. Redox Signal. 2011, 14:1535-1550.
20. Jobe A.H. The new bronchopulmonary dysplasia. Curr. Opin. Pediatr. 2011, 23:167-172.
21. Li Y.S., Shemmer B., Stone E., A.Nardi M., Jonas S., Quartermain D. Neuroprotection by inhaled nitric oxide in a murine stroke model is concentration and duration dependent. Brain Res. 2013, 1507:134-145.
22. Lin Y.J., Markham N.E., Balasubramaniam V., Tang A., Maxey J.R., Kinsella J.P., Abman S.H. Inhaled nitric oxide enhances distal lung growth after exposure to hyperoxia in neonatal rats. Pediatr. Res. 2005, 58:22-29.
23. Mercier J.C., Hummler H., Durrmeyer X., Sanchez-Luna M., Carnielli V., Field D., Greenough A., Van Overmeire B., Jonsson B., Hallman M., Baldassarre J., EUNO Study Group Inhaled nitric oxide for prevention of bronchopulmonary dysplasia in premature babies (EUNO): a randomised controlled trial. Lancet 2010, 376:346-354.
24. Moncada S., Palmer R.M., Higgs E.A. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 1991, 43:109-142.
25. Olivier P., Baud O., Evrard P., Gressens P., Verney C. Prenatal ischemia and white matter damage in rats. J. Neuropathol. Exp. Neurol. 2005, 64:998-1006.
26. Olivier P., Loron G., Fontaine R.H., Pansiot J., Dalous J., Thi H.P., Charriaut-Marlangue C., Thomas J.L., Mercier J.C., Gressens P., Baud O. Nitric oxide plays a key role in myelination in the developing brain. J. Neuropathol. Exp. Neurol. 2010, 69:828-837.
27. Pansiot J., Loron G., Olivier P., Fontaine R., Charriaut-Marlangue C., Mercier J.C., Gressens P., Baud O. Neuroprotective effect of inhaled nitric oxide on excitotoxic-induced brain damage in neonatal rat. PLoS One 2010, 5:e10916.
28. Pawloski J.R., Hess D.T., Stamler J.S. Export by red blood cells of nitric oxide bioactivity. Nature 2001, 409:622-626.
29. Pham H., Vottier G., Pansiot J., Dalous J., Gallego J., Gressens P., Duong-Quy S., Dinh-Xuan A.T., Mercier J.C., Biran V., Charriaut-Marlangue C., Baud O. Inhaled NO protects cerebral white matter in neonatal rats with combined brain and lung injury. Am. J. Respir. Crit. Care Med. 2012, 185:897-899.
30. Rieger-Fackeldey E., Hentschel R. Bronchopulmonary dysplasia and early prophylactic inhaled nitric oxide in preterm infants: current concepts and future research strategies in animal models. J. Perinat. Med. 2008, 36:442-447.
31. Ritter J., Schmitz T., Chew L.J., Bührer C., Möbius W., Zonouzi M., Gallo V. Neonatal hyperoxia exposure disrupts axon-oligodendrocyte integrity in the subcortical white matter. J. Neurosci. 2013, 33:8990-9002.
32. Rosenberg P.A., Li Y., Ali S., Altiok N., Back S.A., Volpe J.J. Intracellular redox state determines whether nitric oxide is toxic or protective to rat oligodendrocytes in culture. J. Neurochem. 1999, 73:476-484.
33. Schmitz T., Ritter J., Mueller S., Felderhoff-Mueser U., Chew L.J., Gallo V. Cellular changes underlying hyperoxia-induced delay of white matter development. J. Neurosci. 2011, 31:4327-4344.
34. Shaffer S.G., O'Neill D., Bradt S.K., Thibeault D.W. Chronic vascular pulmonary dysplasia associated with neonatal hyperoxia exposure in the rat. Pediatr. Res. 1987, 21:14-20.
35. Tang J.R., Markham N.E., Lin Y.J., McMurtry I.F., Maxey A., Kinsella J.P., Abman S.H. Inhaled nitric oxide attenuates pulmonary hypertension and improves lung growth in infant rats after neonatal treatment with a VEGF receptor inhibitor. Am. J. Physiol. Lung Cell. Mol. Physiol. 2004, 287:L344-L351.
36. Terpolilli N.A., Kim S.W., Thal S.C., Kataoka H., Zeisig V., Nitzsche B., Klaesner B., Zhu C., Schwarzmaier S., Meissner L., Mamrak U., Engel D.C., Drzezga A., Patel R.P., Blomgren K., Barthel H., Boltze J., Kuebler W.M., Plesnila N. Inhalation of nitric oxide prevents ischemic brain damage in experimental stroke by selective dilatation of collateral arterioles. Circ. Res. 2012, 110:727-738.
37. Terpolilli N.A., Kim S.W., Thal S.C., Kuebler W.M., Plesnila N. Inhaled nitric oxide reduces secondary brain damage after traumatic brain injury in mice. J. Cereb. Blood Flow Metab. 2013, 33:311-318.
38. Thurlbeck W.M., Dunnill M.S., Hartung W., Heard B.E., Heppleston A.G., Ryder R.C. A comparison of three methods of measuring emphysema. Hum. Pathol. 1970, 1:215-226.
39. Toda N., Okamura T. The pharmacology of nitric oxide in the peripheral nervous system of blood vessels. Pharmacol. Rev. 2003, 55:271-324.
40. Tourneux P., Markham N., Seedorf G., Balasubramaniam V., Abman S.H. Inhaled nitric oxide improves lung structure and pulmonary hypertension in a model of bleomycin-induced bronchopulmonary dysplasia in neonatal rats. Am. J. Physiol. Lung Cell. Mol. Physiol. 2009, 297:L1103-L1111.
41. Vaucher E., Tong X.K., Cholet N., Lantin S., Hamel E. GABA neurons provide a rich input to microvessels but not nitric oxide neurons in the rat cerebral cortex: a means for direct regulation of local cerebral blood flow. J. Comp. Neurol. 2000, 421:161-171.
42. Volpe J.J. Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol. 2009, 8:110-124.
43. 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.
44. Yamamoto S., Golanov E.V., Berger S.B., Reis D.J. Inhibition of nitric oxide synthesis increases focal ischemic infarction in rat. J. Cereb. Blood Flow Metab. 1992, 12:717-726.
45. Yun H.Y., Dawson V.L., Dawson T.M. Neurobiology of nitric oxide. Crit. Rev. Neurobiol. 1996, 10:291-316.
46. Zhu C., Sun Y., Gao J., Wang X., Plesnila N., Blomgren K. Inhaled nitric oxide protects males but not females from neonatal mouse hypoxia-ischemia brain injury. Transl. Stroke Res. 2013, 4:201-207.