Involvement of neuronal nitric oxide synthase in ongoing fetal brain injury following near-term rabbit hypoxia-ischemia

Developmental Neuroscience

Volumn 33, Issue 3-4, 2011, Pages 288-298

  Rao, Suma ^a   Lin, Zhenlang ^d   Drobyshevsky, Alexander ^b   Chen, Lina ^e   Ji, Xinhai ^b   Ji, Haitao ^c   Yang, Yirong ^b   Yu, Lei ^b   Derrick, Matthew ^a,b   Silverman, Richard B ^c   Tan, Sidhartha ^b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NORTHSHORE UNIVERSITY HEALTHSYSTEM   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

^d WENZHOU MEDICAL UNIVERSITY   (China)

^e SICHUAN UNIVERSITY   (China)

Author keywords

Brain slice model; Hypoxia ischemia in utero; Neuronal nitric oxide synthase; Neuronal nitric oxide synthase inhibitor

Indexed keywords

DYE; JC 1; JI 8; N [3 (AMINOMETHYL)BENZYL]ACETAMIDINE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR; PROPIDIUM IODIDE; RHODAMINE 123; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CELL DEATH; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; FLUORESCENCE ANALYSIS; GESTATION PERIOD; HIPPOCAMPUS; HYPOXIA; ISCHEMIA; MALE; MITOCHONDRIAL MEMBRANE; NEUROPROTECTION; NONHUMAN; PARIETAL CORTEX; PRIORITY JOURNAL; PROTEIN FUNCTION; RABBIT; SEX DIFFERENCE; UTERUS DISEASE;

ANIMALS; BRAIN INJURIES; FEMALE; FETUS; HYPOXIA-ISCHEMIA, BRAIN; MALE; MITOCHONDRIA; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE II; PREGNANCY; RABBITS;

EID: 80255132664     PISSN: 03785866     EISSN: 14219859     Source Type: Journal    
DOI: 10.1159/000327241     Document Type: Article

References (29)

1. Volpe JJ: Neurology of the Newborn, ed 4. Philadelphia, WB Saunders, 2001.
2. Vannucci RC: Hypoxic-ischemic encephalopathy. Am J Perinatol 2000; 17: 113-120.
3. MacDonald HM, Mulligan JC, Allen AC, Taylor PM: Neonatal asphyxia. 1. Relationship of obstetric and neonatal complications to neonatal mortality in 38,405 consecutive deliveries. J Pediatr 1980; 96: 898-902. (Pubitemid 10068229)
4. O'Shea TM: Cerebral palsy in very preterm infants: new epidemiological insights. Ment Retard Dev Disabil Res Rev 2002; 8: 135-145. (Pubitemid 36378155)
5. Ancel PY, Livinec F, Larroque B, Marret S, Arnaud C, Pierrat V, Dehan M, N'Guyen S, Escande B, Burguet A, Thiriez G, Picaud JC, André M, Bréart G, Kaminski M: Cerebral palsy among very preterm children in relation to gestational age and neonatal ultrasound abnormalities: the EPIPAGE cohort study. Pediatrics 2006; 117: 828-835. (Pubitemid 46063226)
6. Gluckman PD, Wyatt JS, Azzopardi D, Ballard R, Edwards AD, Ferriero DM, Polin RA, Robertson CM, Thoresen M, Whitelaw A, Gunn AJ: Selective head cooling with mild systemic hypothermia after neonatal encephalopathy: multicentre randomised trial. Lancet 2005; 365: 663-670. (Pubitemid 40260887)
7. Shankaran S, Laptook AR, Ehrenkranz RA, Tyson JE, McDonald SA, Donovan EF, Fanaroff AA, Poole WK, Wright LL, Higgins RD, Finer NN, Carlo WA, Duara S, Oh W, Cotten CM, Stevenson DK, Stoll BJ, Lemons JA, Guillet R, Jobe AH: Whole-body hypothermia for neonates with hypoxic-ischemic encephalopathy. N Engl J Med 2005; 353: 1574-1584. (Pubitemid 41434636)
8. Perlman JM: Intervention strategies for neonatal hypoxic-ischemic cerebral injury. Clin Ther 2006; 28: 1353-1365. (Pubitemid 44740075)
9. Taeusch HW, Ballard RA, Gleason CA, Avery ME: Avery's Diseases of the Newborn. Philadelphia, Elsevier Saunders, 2005, pp 965-992.
10. Hölscher C: Nitric oxide, the enigmatic neuronal messenger: its role in synaptic plasticity. Trends Neurosci 1997; 20: 298-303. (Pubitemid 27348739)
11. Park JH, Straub VA, O'Shea M: Anterograde signaling by nitric oxide: characterization and in vitro reconstitution of an identified nitrergic synapse. J Neurosci 1998; 18: 5463-5476. (Pubitemid 28311961)
12. Bredt DS, Snyder SH: Nitric oxide, a novel neuronal messenger. Neuron 1992; 8: 3-11.
13. Calabrese V, Mancuso C, Calvani M, Rizzarelli E, Butterfield DA, Stella AM: Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity. Nat Rev Neurosci 2007; 8: 766-775. (Pubitemid 47462116)
14. Dawson VL, Dawson TM, Bartley DA, Uhl GR, Snyder SH: Mechanisms of nitric oxidemediated neurotoxicity in primary brain cultures. J Neurosci 1993; 13: 2651-2661. (Pubitemid 23151779)
15. Derrick M, Luo NL, Bregman JC, Jilling T, Ji X, Fisher K, Gladson CL, Beardsley DJ, Murdoch G, Back SA, Tan S: Preterm fetal hypoxia-ischemia causes hypertonia and motor deficits in the neonatal rabbit: a model for human cerebral palsy? J Neurosci 2004; 24: 24-34. (Pubitemid 38181666)
16. Eliasson MJ, Huang Z, Ferrante RJ, Sasamata M, Molliver ME, Snyder SH, Moskowitz MA: Neuronal nitric oxide synthase activation and peroxynitrite formation in ischemic stroke linked to neural damage. J Neurosci 1999; 19: 5910-5918. (Pubitemid 29327926)
17. Vincent SR, Kimura H: Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 1992; 46: 755-784.
18. Tan S, Zhou F, Nielsen VG, Wang Z, Gladson CL, Parks DA: Sustained hypoxia-ischemia results in reactive nitrogen and oxygen species production and injury in the premature fetal rabbit brain. J Neuropathol Exp Neurol 1998; 57: 544-553.
19. Tan S, Zhou F, Nielsen VG, Wang Z, Gladson CL, Parks DA: Increased injury following intermittent fetal hypoxia-reoxygenation is associated with increased free radical production in fetal rabbit brain. J Neuropathol Exp Neurol 1999; 58: 972-981. (Pubitemid 29441925)
20. Ayata C, Ayata G, Hara H, Matthews RT, Beal MF, Ferrante RJ, Endres M, Kim A, Christie RH, Waeber C, Huang PL, Hyman BT, Moskowitz MA: Mechanisms of reduced striatal NMDA excitotoxicity in type I nitric oxide synthase knock-out mice. J Neurosci 1997; 17: 6908-6917. (Pubitemid 27427869)
21. Dalkara T, Yoshida T, Irikura K, Moskowitz MA: Dual role of nitric oxide in focal cerebral ischemia. Neuropharmacology 1994; 33: 1447-1452. (Pubitemid 24353740)
22. Ferriero DM, Holtzman DM, Black SM, Sheldon RA: Neonatal mice lacking neuronal nitric oxide synthase are less vulnerable to hypoxic-ischemic injury. Neurobiol Dis 1996; 3: 64-71. (Pubitemid 26145406)
23. Derrick M, He J, Brady E, Tan S: The in vitro fate of rabbit fetal brain cells after acute in vivo hypoxia. J Neurosci 2001; 21:RC138.
24. Ji H, Stanton BZ, Igarashi J, Li H, Martasek P, Roman LJ, Poulos TL, Silverman RB: Minimal pharmacophoric elements and fragment hopping, an approach directed at molecular diversity and isozyme selectivity: design of selective neuronal nitric oxide synthase inhibitors. J Am Chem Soc 2008; 130: 3900-3914. (Pubitemid 351429856)
25. Ji H, Tan S, Igarashi J, Li H, Derrick M, Martasek P, Roman LJ, Vasquez-Vivar J, Poulos TL, Silverman RB: Selective neuronal nitric oxide synthase inhibitors and the prevention of cerebral palsy. Ann Neurol 2009; 65: 209-217.
26. Derrick M, Drobyshevsky A, Ji X, Chen L, Yang Y, Ji H, Silverman RB, Tan S: Hypoxiaischemia causes persistent movement deficits in a perinatal rabbit model of cerebral palsy: assessed by a new swim test. Int J Dev Neurosci 2009; 27: 549-557.
27. Ji H, Li H, Martasek P, Roman LJ, Poulos TL, Silverman RB: Discovery of highly potent and selective inhibitors of neuronal nitric oxide synthase by fragment hopping. J Med Chem 2009; 52: 779-797.
28. Drobyshevsky A, Derrick M, Prasad PV, Ji X, Englof I, Tan S: Fetal brain magnetic resonance imaging response acutely to hypoxiaischemia predicts postnatal outcome. Ann Neurol 2007; 61: 307-314. (Pubitemid 46676730)
29. Jaroszeski MJ, Radcliff G: Fundamentals of flow cytometry. Mol Biotechnol 1999; 11: 37-53. (Pubitemid 29249364)