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The Role of Polyamine Metabolism in Neuronal Injury Following Cerebral Ischemia

Published online by Cambridge University Press:  02 December 2014

Grace H. Kim ,
Ricardo J. Komotar ,
Margy E. McCullough-Hicks ,
Marc L. Otten ,
Robert M. Starke ,
Christopher P. Kellner ,
Matthew C. Garrett ,
Maxwell B. Merkow ,
Michal Rynkowski  and
Kelly A. Dash
...Show all authors
Grace H. Kim
Affiliation:
Department of Neurological Surgery, Columbia University, New York, New York, USA
Ricardo J. Komotar*
Affiliation:
Department of Neurological Surgery, Columbia University, New York, New York, USA
Margy E. McCullough-Hicks
Affiliation:
Department of Neurological Surgery, Columbia University, New York, New York, USA
Marc L. Otten
Affiliation:
Department of Neurological Surgery, Columbia University, New York, New York, USA
Robert M. Starke
Affiliation:
Department of Neurological Surgery, Columbia University, New York, New York, USA
Christopher P. Kellner
Affiliation:
Department of Neurological Surgery, Columbia University, New York, New York, USA
Matthew C. Garrett
Affiliation:
Department of Neurological Surgery, Columbia University, New York, New York, USA
Maxwell B. Merkow
Affiliation:
Department of Neurological Surgery, Columbia University, New York, New York, USA
Michal Rynkowski
Affiliation:
Department of Neurological Surgery, Columbia University, New York, New York, USA
Kelly A. Dash
Affiliation:
Department of Neurological Surgery, Columbia University, New York, New York, USA
E. Sander Connolly
Affiliation:
Department of Neurological Surgery, Columbia University, New York, New York, USA
*
Department of Neurosurgery, Columbia University, 710 West 168th Street, Room 431, New York, New York, 10032, USA.
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Abstract

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Stroke is a leading cause of morbidity and mortality in the US, with secondary damage following the initial insult contributing significantly to overall poor outcome. Prior investigations have shown that the metabolism of certain polyamines such as spermine, spermidine, and putrescine are elevated in ischemic parenchyma, resulting in an increase in their metabolite concentration. Polyamine metabolites tend to be cytotoxic, leading to neuronal injury in the penumbra following stroke and expansion of the area of infarcted tissue. Although the precise mechanism is unclear, the presence of reactive aldehydes produced through polyamine metabolism, such as 3-aminopropanal and acrolein, have been shown to correlate with the incidence of cerebral vasospasm, disruption of oxidative metabolism and mitochondrial functioning, and disturbance of cellular calcium ion channels. Regulation of the polyamine metabolic pathway, therefore, may have the potential to limit injury following cerebral ischemia. To this end, we review this pathway in detail with an emphasis on clinical applicability.

Type
Review Article
Information
Canadian Journal of Neurological Sciences , Volume 36 , Issue 1 , January 2009 , pp. 14 - 19
Copyright
Copyright © The Canadian Journal of Neurological 2009

References

1.Adibhatla, RM, Hatcher, JF, Dempsey, RJ.Phospholipase A2, hydroxyl radicals, and lipid peroxidation in transient cerebral ischemia. Antioxid Redox Signal. 2003 Oct;5(5):647–54.Google Scholar
2.Ivanova, S, Batliwalla, F, Mocco, J, Kiss, S, Huang, J, Mack, W, et al.Neuroprotection in cerebral ischemia by neutralization of 3-aminopropanal. Proc Natl Acad Sci USA. 2002 Apr 16;99(8):5579–84.Google Scholar
3.Goodenough, S, Davidson, M, Kidd, G, Matsumoto, I, Wilce, P.Cell death and immunohistochemistry of p53, c-Fos and c-Jun after spermine injection into the rat striatum. Exp Brain Res. 2000 Mar;131(1):126–34.Google Scholar
4.Slotkin, TA, Bartolome, J.Role of ornithine decarboxylase and the polyamines in nervous system development: a review. Brain Res Bull. 1986 Sep;17(3):307–20.Google Scholar
5.Iqbal, Z, Koenig, H.Polyamines appear to be second messengers in mediating Ca2+ fluxes and neurotransmitter release in potassium-depolarized synaptosomes. Biochem Biophys Res Commun. 1985 Dec 17;133(2):563–73.Google Scholar
6.Rock, DM, Macdonald, RL.Polyamine regulation of N-methyl-D-aspartate receptor channels. Annu Rev Pharmacol Toxicol. 1995; 35:463–82.Google Scholar
7.Williams, K, Romano, C, Molinoff, PB.Effects of polyamines on the binding of [3H]MK-801 to the N-methyl-D-aspartate receptor: pharmacological evidence for the existence of a polyamine recognition site. Mol Pharmacol. 1989 Oct;36(4):575–81.Google Scholar
8.Seiler, N.Polyamine oxidase, properties and functions. Prog Brain Res. 1995;106:333–44.Google Scholar
9.Ferioli, ME, Berselli, D, Caimi, S.Effect of mitoguazone on polyamine oxidase activity in rat liver. Toxicol Appl Pharmacol. 2004 Dec 1;201(2):105–11.Google Scholar
10.Takano, K, Ogura, M, Yoneda, Y, Nakamura, Y.Oxidative metabolites are involved in polyamine-induced microglial cell death. Neuroscience. 2005;134(4):1123–31.Google Scholar
11.Nagesh Babu, G, Sailor, KA, Sun, D, Dempsey, RJ.Spermidine/spermine N1-acetyl transferase activity in rat brain following transient focal cerebral ischemia and reperfusion. Neurosci Lett. 2001 Mar 2;300(1):17–20.Google Scholar
12.Tomitori, H, Usui, T, Saeki, N, Ueda, S, Kase, H, Nishimura, K, et al.Polyamine oxidase and acrolein as novel biochemical markers for diagnosis of cerebral stroke. Stroke. 2005 Dec;36(12): 2609–13.CrossRefGoogle ScholarPubMed
13.Alarcon, RA.Acrolein. IV. Evidence for the formation of the cytotoxic aldehyde acrolein from enzymatically oxidized spermine or spermidine. Arch Biochem Biophys. 1970 Apr;137(2):365–72.CrossRefGoogle ScholarPubMed
14.Wallace, HM, Fraser, AV.Inhibitors of polyamine metabolism: review article. Amino Acids. 2004 Jul;26(4):353–65.Google Scholar
15.Seiler, N.Catabolism of polyamines. Amino Acids. 2004 Jun;26(3):217–33.Google Scholar
16.Paschen, W.Polyamine metabolism in different pathological states of the brain. Mol Chem Neuropathol. 1992 Jun;16(3):241–71.Google Scholar
17.Cockroft, KM, Meistrell, M, 3rd, Zimmerman, GA, Risucci, D, Bloom, O, Cerami, A, et al.Cerebroprotective effects of aminoguanidine in a rodent model of stroke. Stroke. 1996 Aug;27(8):1393–8.Google Scholar
18.Temiz, C, Dogan, A, Baskaya, MK, Dempsey, RJ.Effect of difluoromethylornithine on reperfusion injury after temporary middle cerebral artery occlusion. J Clin Neurosci. 2005 May;12(4):449–52.Google Scholar
19.Wood, PL, Khan, MA, Kulow, SR, Mahmood, SA, Moskal, JR.Neurotoxicity of reactive aldehydes: the concept of “aldehyde load” as demonstrated by neuroprotection with hydroxylamines. Brain Res. 2006 Jun 20;1095(1):190–9.Google Scholar
20.Paschen, W, Schmidt-Kastner, R, Djuricic, B, Meese, C, Linn, F, Hossmann, KA.Polyamine changes in reversible cerebral ischemia. J Neurochem. 1987 Jul;49(1):35–7.Google Scholar
21.Takano, K, Ogura, M, Nakamura, Y, Yoneda, Y.Neuronal and glial responses to polyamines in the ischemic brain. Curr Neurovasc Res. 2005 Jul;2(3):213–23.Google Scholar
22.Ivanova, S, Botchkina, GI, Al-Abed, Y, Meistrell, M, 3rd, Batliwalla, F, Dubinsky, JM, et al.Cerebral ischemia enhances polyamine oxidation: identification of enzymatically formed 3-amino-propanal as an endogenous mediator of neuronal and glial cell death. J Exp Med. 1998 Jul 20;188(2):327–40.Google Scholar
23.Peasley, MA, Shi, R.Ischemic insult exacerbates acrolein-induced conduction loss and axonal membrane disruption in guinea pig spinal cord white matter. J Neurol Sci. 2003 Dec 15;216(1):23–32.Google Scholar
24.Li, W, Yuan, XM, Ivanova, S, Tracey, KJ, Eaton, JW, Brunk, UT.3-Aminopropanal, formed during cerebral ischaemia, is a potent lysosomotropic neurotoxin. Biochem J. 2003 Apr 15;371(Pt 2):429–36.CrossRefGoogle ScholarPubMed
25.Echlin, F.Experimental vasospasm, acute and chronic, due to blood in the subarachnoid space. J Neurosurg. 1971 Dec;35(6):646–56.Google Scholar
26.Conklin, DJ, Boyce, CL, Trent, MB, Boor, PJ.Amine metabolism: a novel path to coronary artery vasospasm. Toxicol Appl Pharmacol. 2001 Sep 1;175(2):149–59.Google Scholar
27.Liu-Snyder, P, McNally, H, Shi, R, Borgens, RB.Acrolein-mediated mechanisms of neuronal death. J Neurosci Res. 2006 Jul;84(1):209–18.CrossRefGoogle ScholarPubMed
28.Liu-Snyder, P, Borgens, RB, Shi, R.Hydralazine rescues PC12 cells from acrolein-mediated death. J Neurosci Res. 2006 Jul;84(1):219–27.Google Scholar
29.Tanel, A, Averill-Bates, DA.P38 and ERK mitogen-activated protein kinases mediate acrolein-induced apoptosis in Chinese hamster ovary cells. Cell Signal. 2007 May;19(5):968–77.Google Scholar
30.Finkelstein, EI, Nardini, M, van der Vliet, A.Inhibition of neutrophil apoptosis by acrolein: a mechanism of tobacco-related lung disease? Am J Physiol Lung Cell Mol Physiol. 2001 Sep;281(3):L732–9.CrossRefGoogle ScholarPubMed
31.Li, L, Hamilton, RF Jr., Taylor, DE, Holian, A.Acrolein-induced cell death in human alveolar macrophages. Toxicol Appl Pharmacol. 1997 Aug;145(2):331–9.Google Scholar
32.Picklo, MJ, Montine, TJ.Acrolein inhibits respiration in isolated brain mitochondria. Biochim Biophys Acta. 2001 Feb 14;1535(2):145–52.Google Scholar
33.Zollner, H.Inhibition of some mitochondrial functions by acrolein and methylvinylketone. Biochem Pharmacol. 1973 May 15;22(10):1171–8.Google Scholar
34.Harper, ME, Bevilacqua, L, Hagopian, K, Weindruch, R, Ramsey, JJ.Ageing, oxidative stress, and mitochondrial uncoupling. Acta Physiol Scand. 2004 Dec;182(4):321–31.Google Scholar
35.Luo, J, Shi, R.Acrolein induces oxidative stress in brain mitochondria. Neurochem Int. 2005 Feb;46(3):243–52.Google Scholar
36.Hurtado, O, Cardenas, A, Pradillo, JM, Morales, JR, Ortego, F, Sobrino, T, et al.A chronic treatment with CDP-choline improves functional recovery and increases neuronal plasticity after experimental stroke. Neurobiol Dis. 2007 Apr;26(1): 105–11.CrossRefGoogle ScholarPubMed