Skip to main content

RETRACTED CHAPTER: Dysfunction of nitric oxide synthases as a cause and therapeutic target in delayed cerebral vasospasm after SAH

  • Conference paper
  • First Online:
Cerebral Vasospasm

Part of the book series: Acta Neurochirurgica Supplement ((NEUROCHIRURGICA,volume 104))

Abstract

Nitric oxide (NO), also known as endothelium-derived relaxing factor, is produced by endothelial nitric oxide synthase (eNOS) in the intima and by neuronal nitric oxide synthase (nNOS) in the adventitia of cerebral vessels. It dilates the arteries in response to shear stress, metabolic demands, pterygopalatine ganglion stimulation, and chemoregulation. Subarachnoid haemorrhage (SAH) interrupts this regulation of cerebral blood flow. Hemoglobin, gradually released from erythrocytes in the subarachnoid space destroys nNOS-containing neurons in the conductive arteries. This deprives the arteries of NO, leading to the initiation of delayed vasospasm. But such vessel narrowing increases shear stress, which stimulates eNOS. This mechanism normally would lead to increased production of NO and dilation of arteries. However, a transient eNOS dysfunction evoked by an increase of the endogenous competitive nitric oxide synthase (NOS) inhibitor, asymmetric dimethyl-arginine (ADMA), prevents this vasodilation. eNOS dysfunction has been recently shown to be evoked by increased levels of ADMA in CSF in response to the presence of bilirubin-oxidized fragments (BOXes). A direct cause of the increased ADMA CSF level is most likely decreased ADMA elimination due to the disappearance of ADMA-hydrolyzing enzyme (DDAH II) immunoreactivity in the arteries in spasm. This eNOS dysfunction sustains vasospasm. CSF ADMA levels are closely associated with the degree and time-course of vasospasm; when CSF ADMA levels decrease, vasospasm resolves. Thus, the exogenous delivery of NO, inhibiting the L-arginine-methylating enzyme (IPRMT3) or stimulating DDAH II, may provide new therapeutic modalities to prevent and treat vasospasm. This paper will present results of preclinical studies supporting the NO-based hypothesis of delayed cerebral vasospasm development and its prevention by increased NO availability.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Achan V, Tran C, Arrigoni F, Whitley GS, Leiper JM, Vallance P (2002) All-trans-retinoic acid increases nitric oxide synthesis by endothelial cells. A role for the induction of dimethylarginine dimethylaminohydrolase. Circ Res 90: 764–769

    CAS  PubMed  Google Scholar 

  2. Afshar J, Pluta R, Boock R, Thompson BG, Oldfield EH (1995) Effect of intracarotid nitric oxide on primate cerebral vasospasm after subarachnoid hemorrhage. J Neurosurg 83: 118–122

    CAS  PubMed  Google Scholar 

  3. Allen G (1976) Cerebral arterial spasm: Part 8. The treatment of delayed cerebral arterial spasm in human beings. Surg Neurol 6: 71–80

    CAS  PubMed  Google Scholar 

  4. Asano T (1999) Oxyhemoglobin as the principal cause of cerebral vasospasm: a holistic view of its actions. Crit Rev Neurosurg 9: 303–318

    CAS  PubMed  Google Scholar 

  5. Blaumanis O, Grady P, Nelson E (1979) Hemodynamic and morphologic aspects of cerebral vasospasm. In: Price T, Nelson E (eds) Cerebrovascular diseases. Raven Press, New York, pp 283–294

    Google Scholar 

  6. Boger R, Sydow K, Borlak J, Thum T, Lenzen H, Schubert B, Tsikas D, Bode-Boger SM (2000) LDL cholesterol upregulates synthesis of asymmetrical dimethylarginine in human endothelial cells: involvement of S-adenosyl-methionine-dependent methyltransferases. Circ Res 87: 99–105

    CAS  PubMed  Google Scholar 

  7. Bredt D, Hwang P, Glatt C, Lowenstein C, Reed RR, Snyder SH (1991) Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature 351: 714–718

    CAS  PubMed  Google Scholar 

  8. Brown F, Hanlon K, Crockard H, Mullan S (1977) Effect of sodium nitroprusside on cerebral blood flow in conscious human beings. Surg Neurol 7: 67–70

    CAS  PubMed  Google Scholar 

  9. Brown M (2002) Brain attack: a new approach to stroke. Clin Med 2: 60–65

    Google Scholar 

  10. Bryan N, Rassaf T, Maloney R, Rodriquez CM, Saijo F, Rodriguez JR, Feelisch M (2004) Cellular targets and mechanism of nitros( yl)ation: an insight into their nature and kinetics in vivo. PNAS 101: 4308–4313

    CAS  PubMed  Google Scholar 

  11. Buchanan JE, Philis JW (1993) The role of nitric oxide in the regulation of cerebral blood flow. Brain Res 610: 248–255

    CAS  PubMed  Google Scholar 

  12. Chen H, Ward MH, Tucker KL, Graubard BI, McComb RD, Potischman NA, Weisenburger DD, Heineman EF (2002) Diet and risk of adult glioma in eastern Nebraska, United States. Cancer Causes Control 13: 647–655

    PubMed  Google Scholar 

  13. Clark J, Reilly M, Sharp F (2002) Oxidation of bilirubin produces compounds that cause prolonged vasospasm of rat cerebral vessels: a contributor to subarachnoid hemorrhage-induced vasospasm. J Cereb Blood Flow Metab 22: 472–478

    CAS  PubMed  Google Scholar 

  14. Cosby K, Partovi KS, Crawford JH, Patel RP, Reiter CD, Martyr S, Yang BK, Waclawiw MA, Zalos G, Xu X, Huang KT, Shields H, Kim-Shapiro DB, Schechter AN, Cannon RO 3rd, Gladwin MT (2003) Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. Nature Medicine 9: 1498–1505

    CAS  PubMed  Google Scholar 

  15. Dirnagl U, Lindauer U, Villringer A (1992) Role of nitric oxide coupling of cerebral blood flow to neuronal activation in rats. Neurosci Lett 149: 43–462

    Google Scholar 

  16. Dorsch N (2002) Therapeutic approaches to vasospasm in subarachnoid hemorrhage. Curr Opin Crit Care 2002: 128–133

    Google Scholar 

  17. Doyle M, Hoekstra J (1981) Oxidation of nitrogen oxides by bound dioxygen in hemoproteins. J Inorg Biochem 14: 351–358

    CAS  PubMed  Google Scholar 

  18. Ecker A, Rimenschneider P (1951) Arteriographic demonstration of spasm of the intracranial arteries with special reference to saccular arterial aneurysms. J Neurosurg 8: 660–667

    CAS  PubMed  Google Scholar 

  19. Egemen N, Turker R, Sanlidilik U, Zorlutuna A, Bilgic S, Baskaya M, Unlu A, Caglar S, Spetzler RF, McCormick JM (1993) The effect of intrathecal sodium nitroprusside on severe chronic vasospasm. Neurol Res 15: 310–315

    CAS  PubMed  Google Scholar 

  20. Findlay J, Weir B, Steinke D, Tanabe T, Gordon P, Grace M(1988) Effect of intrathecal thrombolytic therapy on subarachnoid clot and chronic vasospasm in primate model of SAH. J Neurosurg 69: 723–735

    CAS  PubMed  Google Scholar 

  21. Frazee JG, Giannotta SL, Stern ES (1981) Intravenous nitroglycerin for the treatment of chronic cerebral vasoconstriction in the primate. J Neurosurg 55: 865–868

    CAS  PubMed  Google Scholar 

  22. Furchgott R, Zawadzki J (1980) The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288: 373–376

    CAS  PubMed  Google Scholar 

  23. Gabikian P, Clatterbuck R, Eberhart C, Tyler BM, Tierney TS, Tamargo RJ (2002) Prevention of experimental cerebral vasospasm by intracranial delivery of a nitric oxide donor from a controlled-release polymer: toxicity and efficacy studies in rabbits and rats. Stroke 33: 2681–2686

    PubMed  Google Scholar 

  24. Gallo O, Masino E, Morbidelli L, Franchi A, Fini-Storchi I, Vergari WA, Ziche M (1998) Role of nitric oxide in angiogenesis and tumor progression in head and neck cancer. J Natl Cancer Inst 90: 587–596

    CAS  PubMed  Google Scholar 

  25. Gladwin M, Crawford J, Patel R (2004) The biochemistry of nitric oxide, nitrite, and hemoglobin: role in blood flow regulation. Free Rad Biol Med 36: 707–716

    CAS  PubMed  Google Scholar 

  26. Gull W (1859) Cases of aneurism of the cerebral vessels. Guy’s Hosp Rep 5: 281–304

    Google Scholar 

  27. Handa Y, Weir B, Nosko M, Mosewich R, Tsuji T, Grace M(1987) The effect of timing of clot removal on chronic vasospasm ina primate model. J Neurosurg 67: 558–564

    CAS  PubMed  Google Scholar 

  28. Hanel R, Lopes D, Wehman J, Sauvageau E, Levy ET, Guterman LR, Hopkins LN (2005) Endovascular treatment of intracranial aneurysms and vasospasm after aneurysmal subarachnoid hemorrhage. Neurosurg Clin N Am 16: 317–353

    PubMed  Google Scholar 

  29. Hashi K, Mayer J, Shinmaru S, Welch KM, Teraura T (1972) Cerebral hemodynamic and metabolic changes after subarachnoid hemorrhage. J Neurol Sci 17: 1–14

    CAS  PubMed  Google Scholar 

  30. Hernandez-Perera O, Perez-Sala D, Navarro-Antolin J, Sanchez-Pascuala R, Hernandez G, Diaz C, Lamas S (1998) Effects of 3-hyrdoxy-3-methylglutaryl-CoA reductase inhibitors, Atarvostatin and Simvastatin, on the expression of endothelin-1 and endothelial nitric oxide synthase in vascular endothelial cells. JCI 101: 2711–2719

    CAS  PubMed  Google Scholar 

  31. Heros R, Zervas N, Lavyne M, Pickren KS (1976) Reversal of experimental cerebral vasospasm by intravenous nitroprusside therapy. Surg Neurol 6: 227–229

    CAS  PubMed  Google Scholar 

  32. Holden D, Cartwright J, Nussey S, Whitley GS (2003) Estrogen stimulates DDAH activity and the metabolism of ADMA. Circulation 108: 1575–1580

    CAS  PubMed  Google Scholar 

  33. Horky LL, Pluta RM, Boock RJ, Oldfield EH (1998) Role of ferrous iron chelator 2.2′-dipyridyl in preventing delayed vasospasm in a primate model of subarachnoid hemorrhage. J Neurosurg 88: 298–303

    CAS  PubMed  Google Scholar 

  34. Huncharek M, Kupelnick B (2004) A meta-analysis of maternal cured meat consumption during pregnancy and the risk of childhood brain tumors. Neuroepidemiology 23: 78–84

    PubMed  Google Scholar 

  35. Ignarro L (2002) Nitric oxide as a unique signaling molecule in the vascular system: a historical overview. J Physiol Pharmacol 53: 503–514

    CAS  PubMed  Google Scholar 

  36. Ito Y, Isotani E, Mizuno Y, Azuma H, Hirakawa K (2000) Effective improvement of the cerebral vasospasm after subarachnoid hemorrhage with low-dose nitroglycerin. J Cardiovasc Pharmacol 35: 45–50

    CAS  PubMed  Google Scholar 

  37. Iuliano B, Pluta R, Jung C, Oldfield EH (2004) Endothelial dysfunction in a primate model of cerebral vasospasm. J Neurosurg 100: 287–294

    PubMed  Google Scholar 

  38. Jiang J-L, Li N-S, Deng H-W (2002) Probucol preserves endothelial function by reduction of the endogenous nitric oxide synthase inhibitor level. Br J Pharmacol 135: 1175–1182

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Jung C, Iuliano B, Harvey-White J, Espey MG, Oldfield EH, Pluta RM (2004) Association between cerebrospinal fluid levels of asymmetric dimethyl-L-arginine, an endogenous inhibitor of endothelial nitric oxide synthase, and cerebral vasospasm in a primate model of subarachnoid hemorrhage. J Neurosurg 101: 836–842

    CAS  PubMed  Google Scholar 

  40. Jung C, Iuliano B, Harvey-White J et al (2004) CSF levels of ADMA, an endogenous inhibitor of nitric oxide synthase, are associated with cerebral vasospasm after subarachnoid hemorrhage. In: Macdonald R (ed) Cerebral vasospasm: proceedings of the 8th International Conference, Vol. 92–93. Thieme, New York

    Google Scholar 

  41. Kassell N, Helm G, Simmons N, Phillips CD, Cail WS (1992) Treatment of cerebral vasospasm with intra-arterial papaverine. J Neurosurg 77: 848–852

    CAS  PubMed  Google Scholar 

  42. Kassell NF, Torner JC (1984) The International Cooperative Study in timing of aneurysm surgery — an update. Stroke 15: 566–570

    CAS  PubMed  Google Scholar 

  43. Kasuya H, Weir B, Nakane M, Pollock JS, Johns L, Marton LS, Stefansson K (1995) Nitric oxide synthase and guanylate cyclase levels in canine basilar artery after subarachnoid hemorrhage. J Neurosurg 82: 250–255

    CAS  PubMed  Google Scholar 

  44. Kiris T (1999) Reversal of cerebral vasospasm by the nitric oxide donor SNAP in an experimental model of subarachnoid haemorrhage. Acta Neurochir (Wien) 141: 1323–1328

    CAS  PubMed  Google Scholar 

  45. Kistler J, Lees R, Candia G, Zervas NT, Crowell RM, Ojemann RG (1979) Intravenous nitroglycerin in experimental vasospasm. A preliminary report. Stroke 10: 26–29

    CAS  PubMed  Google Scholar 

  46. Kleinbongard P, Dejam A, Lauer T, Rassaf T, Schindler A, Picker O, Scheeren T, Godecke A, Schrader J, Schulz R, Heusch G, Schaub GA, Bryan NS, Feelisch M, Kelm M (2003) Plasma nitrite reflects constitutive nitric oxide synthase activity in mammals. Free Radical Biol Med 35: 790–796

    CAS  Google Scholar 

  47. Klimo P Jr, Kestle JR, MacDonald JD, Schmidt RH (2004) Marked reduction of cerebral vasospasm with lumbar drainage of cerebrospinal fluid after subarachnoid hemorrhage. J Neurosurg 100: 215–224

    PubMed  Google Scholar 

  48. Lau AK, Leichtweis SB, Hume P, Mashima R, Hou JY, Chaufour X, Wilkinson B, Hunt NH, Celermajer DS, Stocker R (2003) Probucol promotes functional reendothelization in balloon-injured rabbit aortas. Circulation 107: 2031–2036

    CAS  PubMed  Google Scholar 

  49. Lauer T, Preik M, Rassaf T, Strauer BE, Deussen A, Feelisch M, Kelm M (2001) Plasma nitrite rather than nitrate reflects regional endothelial nitric oxide synthase activity but lacks intrinsic vasodilator action. Proc Natl Acad Sci USA 98: 12814–12819

    CAS  PubMed  Google Scholar 

  50. Leiper J, Murray-Rust J, McDonald N, Vallance P (2002) S-nitrosylation of dimethylarginine dimethylaminohydrolase regulates enzyme activity: further interactions between nitric oxide synthase and dimethylarginine dimethylaminehydrolase. Proc Natl Acad Sci USA 99: 13527–13532

    CAS  PubMed  Google Scholar 

  51. Little N, Morgan M, Grinnell V et al (1994) Intra-arterial papaverine in the management of cerebral vasopasm following subarachnoid hemorrhage. J Clin Neurosci 1: 42–46

    CAS  PubMed  Google Scholar 

  52. Liu X, Miller M, Joshi H, Sadowska-Krowicka H, Clark DA, Lancaster JR Jr (1998) Diffusion-limited reaction of free nitric oxide with erythrocytes. J Biol Chem 273: 18709–18713

    CAS  PubMed  Google Scholar 

  53. Macdonald R, Weir B (2001) Cerebral vasospasm. Academic Press, San Diego, pp 449–450

    Google Scholar 

  54. Macdonald R, Weir B (1991) A review of hemoglobin and the pathogenesis of cerebral vasospasm. Stroke 22: 971–982

    CAS  PubMed  Google Scholar 

  55. Macdonald RL, Zhang ZD, Curry D, Elas M, Aihara Y, Halpern H, Jahromi BS, Johns L (2002) Intracisternal sodium nitroprusside fails to prevent vasospasm in nonhuman primates. Neurosurgery 51: 761–770

    PubMed  Google Scholar 

  56. McGirt MJ, Lynch J, Parra A, Sheng H, Pearlstein RD, Laskowitz DT, Pelligrino DA, Warner DS (2002) Simvastatin increases endothelial nitric oxide synthase and ameliorates cerebral vasospasm resulting from subarachnoid hemorrhage. Stroke 33: 2950–2956

    CAS  PubMed  Google Scholar 

  57. McKean-Cowdin R, Pogoda JM, Lijinsky W, Holly EA, Mueller BA, Preston-Martin S (2003) Maternal prenatal exposure to nitrosatable drugs and childhood brain tumours. Int J Epidemiol 32: 211–217

    PubMed  Google Scholar 

  58. Moniz E (1935) Scientific raisins from 125 years SMW (Swiss Medical Weekly). Clinical and physiological results of cerebral angiography. Schweiz Med Wochenschr 125: 1503–1507

    Google Scholar 

  59. Nagababu E, Ramasamy S, Abernethy DR, Rifkind JM (2003) Active nitric oxide produced in the red cell under hypoxic conditions by deoxyhemoglobin-mediated nitrite reduction. J Biol Chem 278: 46349–46356

    CAS  PubMed  Google Scholar 

  60. Nakao K, Murata H, Kanamaru K, Waga S (1996) Effects of nitroglycerin on vasospasm and cyclic nucleotides in a primate model of subarachnoid hemorrhage. Stroke 27: 1882–1887

    CAS  PubMed  Google Scholar 

  61. Neuwelt EA, Hill SA, Frenkel EP (1984) Osmotic blood-brain barrier modification and combination chemotherapy: concurrent tumor regression in areas of barrier opening and progression in brain regions distant to barrier opening. Neurosurgery 15: 362–366

    CAS  PubMed  Google Scholar 

  62. Newberne PM (1979) Nitrite promotes lymphoma incidence in rats. Science 204: 1079–1081

    CAS  PubMed  Google Scholar 

  63. Newell D, Eskridge J, Mayberg M, Grady MS, Lewis D, Winn HR (1992) Endovascular treatment of intracranial aneurysms and cerebral vasospasm. Clin Neurosurg 39: 348–360

    CAS  PubMed  Google Scholar 

  64. Ng W, Moochhala S, Yeo T, Ong PL, Ng PY (2001) Nitric oxide and subarachnoid hemorrhage: elevated levels in cerebrospinal fluid and their implications. Neurosurgery 49: 622–627

    CAS  PubMed  Google Scholar 

  65. Nishizawa S, Yamamoto S, Yokoyama T, Uemura K (1997) Dysfunction of nitric oxide synthase induces protein kinase C activation resulting in vasospasm after subarachnoid hemorrahge. Neurol Res 19: 558–562

    CAS  PubMed  Google Scholar 

  66. Ohkita M, Takaoka M, Shiota Y, Nojiri R, Matsumura Y (2002) Nitric oxide inhibits endothelin-1 production through the suppression of nuclear factor kappa B. Clin Sci (London) 103(Suppl 48): 68S–71S

    CAS  PubMed  Google Scholar 

  67. Oka M (2001) Phosphodiesterase 5 inhibition restores impaired ACh relaxation in hypertensive conduit pulmonary arteries. Am J Physiol Lung Cell Mol Physiol 280: L432–L435

    CAS  PubMed  Google Scholar 

  68. Paulson O (1970) Regional cerebral blood flow in appoplexy due to occlusion of the middle cerebral artery. Neurology 20: 63–77

    CAS  PubMed  Google Scholar 

  69. Pipili-Synetos E, Papageorgious A, Sakkoula E, Sotiropoulou G, Fotsis T, Karakiulakis G, Maragoudakis ME (1995) Inhibition of angiogenesis, tumour growth and metastasis by the NO-releasing vasodilators, isosorbide mononitrate and dinitrate. Br J Pharmacol 116: 1829–1834

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Pluta R (2005) Delayed cerebral vasospasm and nitric oxide: review, new hypothesis, and proposed treatment. Pharmacol Therap 105: 23–56

    CAS  Google Scholar 

  71. Pluta R, Afshar J, Boock R, Oldfield EH (1998) Temporal changes in perivascular concentrations of oxyhemoglobin, deoxyhemoglobin and, methemoglobin in subarachnoid hemorrhage. J Neurosurg 88: 557–561

    CAS  PubMed  Google Scholar 

  72. Pluta R, Boock R, Oldfield E (1997) Intracarotid chronic infusion of nitric oxide donors prevents cerebral vasospasm in a primate model of subarachnoid hemorrhage, in American Association of Neurological Surgeons Annual meeting. Denver, CO

    Google Scholar 

  73. Pluta R, Jung C, Shilad S et al (2005) Probucol does not inhibit production of ADMA or prevent vasospasm in randomized, double-blind placebo-controlled trial in a primate model of vasospasm. J Neurosurg (in press)

    Google Scholar 

  74. Pluta R, Oldfield E, Boock R (1997) Reversal and prevention of cerebral vasospasm by intracarotid infusions of nitric oxide donors in a primate model of subarachnoid hemorrhage. J Neurosurg 87: 746–751

    CAS  PubMed  Google Scholar 

  75. Pluta R, Thompson B, Dawson T, Snyder SH, Boock RJ, Oldfield EH (1996) Loss of nitric oxide synthase immunoreactivity in cerebral vasospasm. J Neurosurg 84: 648–654

    CAS  PubMed  Google Scholar 

  76. Pluta RM, Dejam A, Grimes G, Gladwin MT, Oldfield EH (2005) Nitrite infusions prevent cerebral artery vasospasm in a primate model of subarachnoid aneurismal hemorrhage. JAMA 293: 1477–1484

    CAS  PubMed  Google Scholar 

  77. Pradilla G, Thai Q, Legnani F, Hsu W, Kretzer RM, Wang PP, Tamargo RJ (2004) Delayed intracranial delivery of a nitric oxide donor from a controlled-release polymer prevents experimental cerebral vasospasm in rabbits. Neurosurgery 2004: 1393–1399

    Google Scholar 

  78. Pyne-Geithman G, Morgan C, Wagner K, Dulaney EM, Carrozzella J, Kanter DS, Zuccarello M, Clark JF (2005) Bilirubin production and oxidation in CSF of patients with cerebral vasospasm after subarachnoid hemorrhage. J Cereb Blood Flow Metab 25: 1070–1077

    CAS  PubMed  Google Scholar 

  79. Raabe A, Zimmermann M, Setzer M, Vatter H, Berkefeld J, Seifert V (2002) Effect of intraventricular sodium nitroprusside on cerebral hemodynamics and oxygenation in poor-grade aneurysm patients with severe, medically refractory vasospasm. Neurosurgery 50: 1006–1013

    PubMed  Google Scholar 

  80. Ram Z, Spiegelman R, Findler G, Hadani M (1989) Delayed postoperative neurological deterioration from prolonged sodium nitroprusside administration. Case report. J Neurosurg 71(4): 605–607

    CAS  PubMed  Google Scholar 

  81. Reid, Johnson, Ollenshow (1950) In: White R (1983) Vasospasm. I. Experimental findings. Intracranial aneurysms. In: Fox JL (ed) Springer, Berlin Heidelberg New York, Tokyo I: 218–249

    Google Scholar 

  82. Saavedra JE, Southan GJ, et al (1996) Localizing antithrombotic and vasodilatory activity with a novel, ultrafast nitric oxide donor. J Med Chem 39(22): 4361–4365

    CAS  PubMed  Google Scholar 

  83. Sambrook M, Hutchinson E, Aber G (1973) Metabolic studies in subarachnoid haemorrhage and strokes. I. Serial changes in acid-base values in blood and cerebrospinal fluid. Brain 96: 171–190

    CAS  PubMed  Google Scholar 

  84. Saver J (2001) Intra-arterial thrombolysis. Neurology (Suppl 2) 57: S58–S60

    CAS  PubMed  Google Scholar 

  85. Sawayama Y, Shimizu C, Maeda N, Tatsukawa M, Kinukawa N, Koyanagi S, Kashiwaqi S, Hayashi J (2002) Effects of probucol and pravastatin on common carotid atherosclerosis in patients with asymptomatic hypercholesterolemia: Fukuoka Atherosclerosis Trial (FAST). J Am Coll Cardiol 39: 610–616

    CAS  PubMed  Google Scholar 

  86. Schievink W (1997) Intracranial aneurysms. NEJM 336: 28–40

    CAS  PubMed  Google Scholar 

  87. Sehba F, Chereshnev I, Maayani S, Friedrich V Jr, Bederson JB (2004) Nitric oxide synthase in acute alteration of nitric oxide levels after subarachnoid hemorrhage. Neurosurgery 55: 671–678

    PubMed  Google Scholar 

  88. Serbinenko F (1979) Six hundred endovascular neurosurgical procedures in vascular pathology. A ten-year experience. Acta Neurochir Suppl (Wien) 28: 310–311

    CAS  PubMed  Google Scholar 

  89. Smith R (1980) Nitrites: FDA beats a surprising retreat. Science 209: 1100–1101

    CAS  PubMed  Google Scholar 

  90. Sobey C (2001) Cerebrovascular dysfunction after subarachnoid hemorrhage: novel mechanisms and directions for therapy. Clin Exp Pharm Physiol 28: 926–929

    CAS  Google Scholar 

  91. Soderberg L (1999) Increased tumor growth in mice exposed to inhaled isobutyl nitrite. Toxicol Lett 104: 35–41

    CAS  PubMed  Google Scholar 

  92. Stapf C, Mohr J (2004) Aneurysms and subarachnoid hemorrhageepidemiology. In: Le Roux PD, Winn HW, Newell DW (eds) Management of cerebral aneurysms. Elsevier Inc., Philadelphia, PA, pp 183–187

    Google Scholar 

  93. Steinmeier R, Laumer R, Bondar I, Priem R, Fahlbusch R (1993) Cerebral hemodynamics in subarachnoid hemorrhage evaluated by Transcranial Doppler sonography. Part 2. Pulsatility indices: normal reference values and characteristics in subarachnoid hemorrhage. Neurosurgery 33: 10–19

    CAS  PubMed  Google Scholar 

  94. Stoodley M, Macdonald R, Weir B, Marton LS, Johns L, Du Zhang Z, Kowalczuk A (2000) Subarachnoid hemorrhage as a cause of an adaptive response in cerebral vessels. J Neurosurg 93: 463–470

    CAS  PubMed  Google Scholar 

  95. StoodleyM,Weihl CC, Zhang Z, Lin G, Johns LM, Kowalczuk A, Ghadge G, Roos RP, Macdonald RL (2000) Effect of adenovirusmediated nitric oxide synthase gene transfer on vasospasm after experimental subarachnoid hemorrhage. Neurosurgery 46: 1193–1203

    CAS  PubMed  Google Scholar 

  96. Suzuki Y, Osuka K, Noda A, Tanazawa T, Takayasu M, Shibuya M, Yoshida J (1997) Nitric oxide metabolites in the cisternal cerebral spinal fluid in patients with subarachnoid hemorrhage. Neurosurgery 41: 807–812

    CAS  PubMed  Google Scholar 

  97. Thomas J, Nemirovsky A, Zelman V, Giannotta SL (1997) Rapid reversal of endothelin-1-induced vasoconstriction by intrathecal administration of nitric oxide donor. Neurosurgery 40: 1245–1249

    CAS  PubMed  Google Scholar 

  98. Thomas J, Rosenwasser R (1999) Reversal of severe cerebral vasospasm in three patients after aneurysmal subarachnoid hemorrhage: initial observations regarding the use of intraventricular sodium nitroprusside in humans. Neurosurgery 44: 48–57

    CAS  PubMed  Google Scholar 

  99. Thompson BG, Pluta RM, Girton M, Oldfield EH (1996) Nitric oxide mediation of chemoregulation but not autoregulation of cerebral blood flow in primates. J Neurosurg 84: 71–78

    CAS  PubMed  Google Scholar 

  100. Thompson W, Piazza G, Li H, Liu L, Fetter J, Zhu B, Sperl G, Ahnen D, Pamukcu R (2000) Exisulind induction of apoptosis involves guanosine 3′,5′-cyclic monophosphate phosphodiesterase inhibition, protein kinase G activation, and attenuated betacatenin. Cancer Res 60: 3338–3342

    CAS  PubMed  Google Scholar 

  101. Toda N, Tanaka T, Ayajiki K, Okamura T (2000) Cerebral vasodilatation induced by stimulation of the pterygopalatine ganglion and greater petrosal nerve in anesthetized monkeys. Neuroscience 96: 393–398

    CAS  PubMed  Google Scholar 

  102. Tran DC, Yeh KC, Brazeau DA, Fung HL (2003) Inhalant nitrite exposure alters mouse hepatic angiogenic gene expression. Biochem Biophys Res Commun 310: 439–445

    CAS  PubMed  Google Scholar 

  103. Treggiari-Venzi M, Suter P, Romand J-A (2001) Review of medical prevention of vasospasm after aneurysmal subarachnoid hemorrhage: a problem of neurointensive care. Neurosurgery 48: 249–262

    CAS  PubMed  Google Scholar 

  104. Vallance P, Chan N (2001) Endothelial dysfunction and nitric oxide: clinical relevance. Heart 85: 342–350

    CAS  PubMed  PubMed Central  Google Scholar 

  105. Vemulapalli S, Watkins R, Chintala M, Davis H, Ahn HS, Fawzi A, Tulshian D, Chiu P, Chatterjee M, Lin CC, Sybertz EJ (1996) Antiplatelet and antiproliferative effects of SCH 51866, a novel type 1 and type 5 phosphodiesterase inhibitor. J Cardiovasc Pharmacol 28: 862–869

    CAS  PubMed  Google Scholar 

  106. Watkins L (1995) Nitric oxide and cerebral blood flow: an update. Cerebrovasc Brain Metabol Rev 7: 324–337

    CAS  Google Scholar 

  107. Weir B, Grace M, Hansen J, Rothberg C (1978) Time course of vasospasm in man. J Neurosurg 48: 173–181

    CAS  PubMed  Google Scholar 

  108. Weyerbrock A, Walbridge S, Pluta RM, Saavedra JE, Keefer LK, Oldfield EH (2003) Selective opening of the blood-tumor barrier by a nitric oxide donor and long-term survival in rats with C6 gliomas. J Neurosurg 99: 728–737

    CAS  PubMed  Google Scholar 

  109. Wilkins R (1980) Attempted prevention or treatment of intracranial arterial spasm: a survey. Neurosurgery 6: 198–210

    CAS  PubMed  Google Scholar 

  110. Wilkins R (1986) Attempts at prevention or treatment of intracranial arterial spasm: an update. Neurosurgery 18: 808–825

    CAS  PubMed  Google Scholar 

  111. Wink D, Cook J, Pacelli R, DeGraff W, Gamson J, Liebmann J, Krishna MC, Mitchell JB (1996) Effect of various nitric oxidedonor agents on peroxide mediated toxicity. A direct correlation between nitric oxide formation and protection. Arch Biochem Biophys 331: 241–248

    CAS  PubMed  Google Scholar 

  112. Wolf E, Banerjee A, Soble-Smith J, Dohan FC Jr, White RP, Robertson JT (1998) Reversal of cerebral vasospasm using an intrathecally administered nitric oxide donor. JNeurosurg 89: 279–288

    CAS  Google Scholar 

  113. Zhang F, White J, Iadecola C (1994) Nitric oxide donors increase blood flow and reduce brain damage in focal ischemia: evidence that nitric oxide is beneficial in the early stages of cerebral ischemia. J Cereb Blood Flow Metab 14: 217–226

    CAS  PubMed  Google Scholar 

  114. Zweier J, Wang P, Samouilov A, Kuppusamy P (1995) Enzymeindependent formation of nitric oxide in biological tissues. Nature Med 1: 804–809

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ryszard M. Pluta M.D., Ph.D. .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer-Verlag

About this paper

Cite this paper

Pluta, R.M. (2008). RETRACTED CHAPTER: Dysfunction of nitric oxide synthases as a cause and therapeutic target in delayed cerebral vasospasm after SAH. In: Kırış, T., Zhang, J.H. (eds) Cerebral Vasospasm. Acta Neurochirurgica Supplement, vol 104. Springer, Vienna. https://doi.org/10.1007/978-3-211-75718-5_28

Download citation

  • DOI: https://doi.org/10.1007/978-3-211-75718-5_28

  • Published:

  • Publisher Name: Springer, Vienna

  • Print ISBN: 978-3-211-75717-8

  • Online ISBN: 978-3-211-75718-5

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics