Endogenous heme oxygenase prevents impairment of cerebral vascular functions caused by seizures

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 285, Issue 3 54-3, 2003, Pages

  Carratu, Pierluigi ^a   Pourcyrous, Massroor ^a   Fedinec, Alex ^a   Leffler, Charles W ^a   Parfenova, Helena ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Bicuculline; Carbon monoxide; Cerebral circulation; Cranial window; Newborn piglets; Pial arterioles; Seizure; Tin protoporphyrin; Vascular injury; Vascular reactivity

Indexed keywords

BICUCULLINE; BRADYKININ; CARBON MONOXIDE; HEME; HEME OXYGENASE; ISOPRENALINE; NITROPRUSSIDE SODIUM; PROTOPORPHYRIN TIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL REACTIVITY; BRAIN ARACHNOID; BRAIN BLOOD VESSEL; BRAIN MICROCIRCULATION; CEREBROSPINAL FLUID; CONTROLLED STUDY; DOSE TIME EFFECT RELATION; HYPERCAPNIA; HYPEREMIA; NEWBORN; NONHUMAN; PIA ARTERY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEIZURE; SWINE; VASCULAR DISEASE; VASODILATATION;

EID: 0041357192     PISSN: 03636135     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpheart.00091.2003     Document Type: Article

References (39)

1. Anderson KE, Simionatto CS, Drummond GS, and Kappas A. Tissue distribution and disposition of tin-protoporphyrin, a potent competitive inhibitor of heme oxygenase. J Pharmacol Exp Ther 228: 327-333, 1984.
2. Borch K, Pryds O, Holm S, Lou H, and Greisen G. Regional cerebral blood flow during seizures in neonates. J Pediatr 132: 431-435, 1998.
3. Bolwig TG. Blood-brain barrier studies with special reference to epileptic seizures. Acta Psychiatr Scand Suppl 345: 15-20, 1988.
4. Boylan GB, Panerai RB, Rennie JM, Evans DH, Rabe-Hesketh S, and Binnie CD. Cerebral blood flow velocity during neonatal seizures. Arch Dis Child Fetal Neonatal Ed 80: F105-F110, 1999.
5. Busija DW and Leffler CW. Dilator effects of amino acid neurotransmitters on piglet pial arterioles. Am J Physiol Heart Circ Physiol 257: H1200-H1203, 1989.
6. Busija DW and Leffler CW. Role of prostanoids in cerebrovascular responses during seizures in piglets. Am J Physiol Heart Circ Physiol 256: H120-H125, 1989.
7. Cornford EM. Epilepsy and the blood brain barrier: endothelial cell responses to seizures. Adv Neurol 79: 845-862, 1999.
8. DiGeronimo RJ, Gegg CA, and Zuckerman SL. Adenosine depletion alters postictal hypoxic cerebral vasodilation in the newborn pig. Am J Physiol Heart Circ Physiol 274: H1495-H1501, 1998.
9. Dore S, Goto S, Sampei K, Blackshaw S, Hester LD, Ingi T, Sawa A, Traystman RJ, Koehler RC, and Snyder SH. Heme oxygenase-2 acts to prevent neuronal death in brain cultures and following transient cerebral ischemia. Neuroscience 99: 587-592, 2000.
10. Dore S, Takahashi M, Ferris CD, Zakhary R, Hester LD, Guastella D, and Snyder SH. Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury. Proc Natl Acad Sci USA 96: 2445-2450, 1999.
11. Drummond GS and Kappas A. Sn-protoporphyrin inhibition of fetal and neonatal brain heme oxygenase. Transplacental passage of the metalloporphyrin and prenatal suppression of hyperbilirubinemia in the newborn animal. J Clin Invest 77: 971-976, 1986.
12. Dwyer BE, Nishimura RN, and Lu SY. Differential expression of heme oxygenase-1 in cultured cortical neurons and astrocytes determined by the aid of a new heme oxygenase antibody. Response to oxidative stress. Brain Res Mol Brain Res 30: 37-47, 1995.
13. Faraci FM, Breese KR, and Heistad DD. Nitric oxide contributes to dilatation of cerebral arterioles during seizures. Am J Physiol Heart Circ Physiol 265: H2209-H2212, 1993.
14. 2 inhibitors. Brain Res Brain Res Rev 38: 61-78, 2001.
15. Fiumana E, Parfenova H, Jaggar JH, and Leffler CW. Carbon monoxide mediates vasodilator effects of glutamate in isolated pressurized cerebral arterioles of newborn pigs. Am J Physiol Heart Circ Physiol 284: H1073-H1079, 2003.
16. Jefferys GR and Traub RD. Electrophysiological substrates for focal epilepsies. Prog Brain Res 116: 351-358, 1998.
17. Leffler CW, Balabanova L, Fedinec AL, Waters CM, and Parfenova H. Mechanism of glutamate stimulation of CO production in cerebral microvessels. Am J Physiol Heart Circ Physiol 285: H74-H80, 2003. First published March 6, 2003; 10.1152/ajpheart.01081.2002.
18. Leffler CW, Nasjletti A, Yu C, Johnson RA, Fedinec AL, and Walker N. Carbon monoxide and cerebral microvascular tone in newborn pigs. Am J Physiol Heart Circ Physiol 276: H1641-H1646, 1999.
19. Maines MD. Zinc protoporphyrin is a selective inhibitor of heme oxygenase activity in the neonatal rat. Biochim Biophys Acta 673: 339-350, 1981.
20. Maines MD. The heme oxygenase system and its functions in the brain. Cell Mol Biol (Noisy-le-grand) 46: 573-585, 2000.
21. Mark JA and Maines MD. Tin-protoporphyrin-mediated disruption in vivo of heme oxygenase-2 protein integrity and activity in rat brain. Pediatr Res 32: 324-329, 1992.
22. Meldrum BS. Glutamate as a neurotransmitter in the brain: review of physiology and pathology. J Nutr 130: 1007S-1015S, 2000,
23. Montecot C, Borredon J, Seylaz J, and Pinard E. Nitric oxide of neuronal origin is involved in cerebral blood flow increase during seizures induced by kainate. J Cereb Blood Flow Metab 17: 94-99, 1997.
24. Montecot C, Seylaz J, and Pinard E. Carbon monoxide regulates cerebral blood flow in epileptic seizures but not in hypercapnia. Neuroreport 9: 2341-2346, 1998.
25. Palmer AM, Hutson PH, Lowe SL, and Bowen DM. Extracellular concentrations of aspartate and glutamate in rat neostriatum following chemical stimulation of frontal cortex. Exp Brain Res 75: 659-663, 1989.
26. Parfenova H, Fedinec A, and Leffler CW. Ionotropic glutamate receptors in cerebral microvascular endothelium are functionally linked to heme oxygenase. J Cereb Blood Flow Metab 23: 190-197, 2003.
27. Parfenova H, Neff RA III, Alonso JS, Shlopov BV, Jamal CN, Sarkisova SA, and Leffler CW. Cerebral vascular endothelial heme oxygenase: expression, localization, and activation by glutamate. Am J Physiol Cell Physiol 281: C1954-C1963, 2001.
28. Perlman JM and Volpe JJ. Seizures in the preterm infant: effects on cerebral blood flow velocity, intracranial pressure, and arterial blood pressure, J Pediatr 102: 288-293, 1983.
29. Platt JL and Nath KA. Heme oxygenase: protective gene or Trojan horse. Nat Med 4: 1364-1365, 1998.
30. Poucyrous M, Bada H, Parfenova H, Daley M, Korones S, and Leffler CW. Cerebrovasodilatory contribution of endogenous carbon monoxide during seizures in newborn pigs. Pediatr Res 51: 579-585, 2002.
31. Pourcyrous M, Leffler CW, Bada HS, Korones SB, Stidham GL, and Busija DW. Effects of pancuronium bromide on cerebral blood flow changes during seizures in newborn pigs. Pediatr Res 31: 636-639, 1992.
32. Robinson JS, Fedinec AL, and Leffler CW. Role of carbon monoxide in glutamate receptor-induced dilation of newborn pig pial arterioles. Am J Physiol Heart Circ Physiol 282: H2371-H2376, 2002.
33. Rowley HL, Martin KF, and Marsden CA. Decreased GABA release following tonic-clonic seizures is associated with an increase in extracellular glutamate in rat hippocampus in vivo. Neuroscience 68: 415-422, 1995.
34. Scheyer RD. Involvement of glutamate in human epileptic activities. Prog Brain Res 116: 359-369, 1998.
35. Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, and Ames BN. Bilirubin is an antioxidant of possible physiological importance. Science 235: 1043-1046, 1987.
36. Tanaka K, Watase K, Manabe T, Yamada K, Watanabe M, Takahashi K, Iwama H, Nishikawa T, Ichihara N, Hori S, Takimoto M, and Wada K. Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science 276: 1699-1702, 1997.
37. Theard MA, Baughman VL, Wang Q, Pelligrino DA, and Albrecht RF. The role of nitric oxide in modulating brain activity and blood flow during seizure. Neuroreport 6: 921-924, 1995.
38. Volpe JJ. Neonatal seizures. In: Neurology of the Newborn (3rd ed.). Philadelphia, PA: Saunders, 1995, p. 172-173.
39. Willis AP and Leffler CW. Endothelial NO and prostanoid involvement in newborn and juvenile pig pial arteriolar vasomotor responses. Am J Physiol Heart Circ Physiol 281: H2366-H2377, 2001.