Spermidine/spermine-N1-acetyltransferase ablation protects against liver and kidney ischemia-reperfusion injury in mice

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 296, Issue 4, 2009, Pages

  Zahedi, Kamyar ^a   Lentsch, Alex B ^a   Okaya, Tomohisa ^a   Barone, Sharon ^a   Sakai, Nozomu ^a   Witte, David P ^b   Arend, Lois J ^a   Alhonen, Leena ^c   Jell, Jason ^d   Jänne, Juhani ^c   Porter, Carl W ^d   Soleimani, Manoocher ^a,e  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^c UNIVERSITY OF EASTERN FINLAND   (Finland)

^d ROSWELL PARK CANCER INSTITUTE   (United States)

^e VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Acute kidney injury; Acute liver failure; Polyamine backconversion; Polyamine catabolism

Indexed keywords

ORNITHINE DECARBOXYLASE; OXIDOREDUCTASE; POLYAMINE; PUTRESCINE; SPERMIDINE; SPERMIDINE SPERMINE N1 ACETYLTRANSFERASE; SPERMINE; SPERMINE OXIDASE; UNCLASSIFIED DRUG; ACYLTRANSFERASE; DIAMINE ACETYLTRANSFERASE; DIAMINE N-ACETYLTRANSFERASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY LIGATION; ARTICLE; CONTROLLED STUDY; FEMALE; HEPATIC ARTERY; HISTOPATHOLOGY; KIDNEY INJURY; KIDNEY ISCHEMIA; LIVER FUNCTION; LIVER INJURY; LIVER ISCHEMIA; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RENAL ARTERY; REPERFUSION INJURY; ANIMAL; ENZYMOLOGY; GENETICS; KIDNEY; KIDNEY DISEASE; LIVER; LIVER DISEASE; METABOLISM; MOUSE MUTANT; PATHOLOGY;

ACETYLTRANSFERASES; ANIMALS; KIDNEY; KIDNEY DISEASES; LIVER; LIVER DISEASES; MICE; MICE, KNOCKOUT; POLYAMINES; REPERFUSION INJURY;

EID: 67149099215     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.90507.2008     Document Type: Article

References (44)

1. 11-diethylnorspermine in primary fetal fibroblasts derived from transgenic mice overexpressing spermidine/spermine N1-acetyltransferase. J Biol Chem 273: 1964-1969, 1998.
2. Alhonen L, Parkkinen JJ, Keinanen T, Sinervirta R, Herzig KH, Janne J. Activation of polyamine catabolism in transgenic rats induces acute pancreatitis. Proc Natl Acad Sci USA 97: 8290-8295, 2000.
3. Alhonen L, Rasanen TL, Sinervirta R, Parkkinen JJ, Korhonen VP, Pietila M, Janne J. Polyamines are required for the initiation of rat liver regeneration. Biochem J 362: 149-153, 2002.
4. Barone S, Okaya T, Rudich S, Petrovic S, Tehrani K, Wang Z, Zahedi K, Casero RA, Lentsch AB, Soleimani M. Distinct and sequential upregulation of genes regulating cell growth and cell cycle progression during hepatic ischemia/reperfusion injury. Am J Physiol Cell Physiol 289: C826-C835, 2005.
5. Baskaya MK, Rao AM, Dogan A, Donaldson D, Gellin G, Dempsey RJ. Regional brain polyamine levels in permanent focal cerebral ischemia. Brain Res 744: 302-308, 1997.
6. Bonventre JV. Mechanisms of ischemic acute renal failure. Kidney Int 43: 1160-1178, 1993.
7. Chen Y, Kramer DL, Diegelman P, Vujcic S, Porter CW. Apoptotic signaling in polyamine analogue-treated SK-MEL-28 human melanoma cells. Cancer Res 61: 6437-6444, 2001.
8. Clarkson AN, Liu H, Pearson L, Kapoor M, Harrison JC, Sammut IA, Jackson DM, Appleton I. Neuroprotective effects of spermine following hypoxic-ischemic-induced brain damage: a mechanistic study. FASEB J 18: 1114-1116, 2004.
9. Coert BA, Anderson RE, Meyer FB. Exogenous spermine reduces ischemic damage in a model of focal cerebral ischemia in the rat. Neurosci Lett 282: 5-8, 2000.
10. Das KC, Misra HP. Hydroxyl radical scavenging and singlet oxygen quenching properties of polyamines. Mol Cell Biochem 262: 127-133, 2004.
11. Dogan A, Rao AM, Hatcher J, Rao VL, Baskaya MK, Dempsey RJ. Effects of MDL 72527, a specific inhibitor of polyamine oxidase, on brain edema, ischemic injury volume, and tissue polyamine levels in rats after temporary middle cerebral artery occlusion. J Neurochem 72: 765-770, 1999.
12. Hasan R, Alam MK, Ali R. Polyamine induced Z-conformation of native calf thymus DNA. FEBS Lett 368: 27-30, 1995.
13. Hasegawa S, Nakano M, Hamana K, Taniguchi Y, Iwasaki T, Kanda T, Suzuki T, Nagai R. Decrease in myocardial polyamine concentration in rats with myocardial infarction. Life Sci 60: 1643-1650, 1997.
14. Hegardt C, Johannsson OT, Oredsson SM. Rapid caspase-dependent cell death in cultured human breast cancer cells induced by the polyamine analogue N(1),N(11)-diethylnorspermine. Eur J Biochem 269: 1033-1039, 2002.
15. Higaki I, Matsui-Yuasa I, Tanaka H, Terakura M, Kinoshita H, Otani S. The effect of hepatic ischemia-reperfusion on polyamine metabolism in some organs of the rat. Transplantation 55: 268-273, 1993.
16. Igarashi K, Kashiwagi K. Polyamines: mysterious modulators of cellular functions. Biochem Biophys Res Commun 271: 559-564, 2000.
17. Ivanova S, Batliwalla F, Mocco J, Kiss S, Huang J, Mack W, Coon A, Eaton JW, Al-Abed Y, Gregersen PK, Shohami E, Connolly ES Jr, Tracey KJ. Neuroprotection in cerebral ischemia by neutralization of 3-aminopropanal. Proc Natl Acad Sci USA 99: 5579-5584, 2002.
18. Ivanova S, Botchkina GI, Al-Abed Y, Meistrell M 3rd, Batliwalla F, Dubinsky JM, Iadecola C, Wang H, Gregersen PK, Eaton JW, Tracey KJ. Cerebral ischemia enhances polyamine oxidation: identification of enzymatically formed 3-aminopropanal as an endogenous mediator of neuronal and glial cell death. J Exp Med 188: 327-340, 1998.
19. Janne J, Alhonen L, Leinonen P. Polyamines: from molecular biology to clinical applications. Ann Med 23: 241-259, 1991.
20. 1-acetyltransferase affects fat metabolism in mice via acetyl-CoA. J Biol Chem 282: 8404-8413, 2007.
21. Kramer D, Mett H, Evans A, Regenass U, Diegelman P, Porter CW. Stable amplification of the S-adenosylmethionine decarboxylase gene in Chinese hamster ovary cells. J Biol Chem 270: 2124-2132, 1995.
22. Kramer DL, Diegelman P, Jell J, Vujcic S, Merali S, Porter CW. Polyamine acetylation modulates polyamine metabolic flux, a prelude to broader metabolic consequences. J Biol Chem 283: 4241-4251, 2008.
23. Kunduzova OR, Escourrou G, De La Farge F, Salvayre R, Seguelas MH, Leducq N, Bono F, Herbert JM, Parini A. Involvement of peripheral benzodiazepine receptor in the oxidative stress, death-signaling pathways, and renal injury induced by ischemia-reperfusion. J Am Soc Nephrol 15: 2152-2160, 2004.
24. Linas SL, Whittenburg D, Parsons PE, Repine JE. Ischemia increases neutrophil retention and worsens acute renal failure: role of oxygen metabolites and ICAM 1. Kidney Int 48: 1584-1591, 1995.
25. Lovaas E. Antioxidative and metal-chelating effects of polyamines. Adv Pharmacol 38: 119-149, 1997.
26. Lovaas E, Carlin G. Spermine: an anti-oxidant and anti-inflammatory agent. Free Radic Biol Med 11: 455-461, 1991.
27. Marton LJ, Pegg AE. Polyamines as targets for therapeutic intervention. Annu Rev Pharmacol Toxicol 35: 55-91, 1995.
28. 1-acetyltransferase (SSAT). J Biol Chem 277: 3647-3657, 2002.
29. Niiranen K, Halmekyto M, Pietila M, Diegelman P, Parkkinen JJ, Eloranta T, Porter CW, Alhonen L, Janne J. Relation of skin polyamines to the hairless phenotype in transgenic mice overexpressing spermidine/spermine N-acetyltransferase. Mol Pharmacol 59: 231-238, 2001.
30. 1-acetyltransferase. J Biol Chem 272: 18746-18751, 1997.
31. Rao AM, Donaldson D, Prasad MR, Dempsey RJ, Baskaya MK. Regional brain polyamine levels in permanent focal cerebral ischemia. Neurosurgery 40: 364-370, 1997.
32. Sava IG, Battaglia V, Rossi CA, Salvi M, Toninello A. Free radical scavenging action of the natural polyamine spermine in rat liver mitochondria. Free Radic Biol Med 41: 1272-1281, 2006.
33. Soda K, Kano Y, Nakamura T, Kasono K, Kawakami M, Konishi F. Spermine, a natural polyamine, suppresses LFA-1 expression on human lymphocyte. J Immunol 175: 237-245, 2005.
34. Suppola S, Heikkinen S, Parkkinen JJ, Uusi-Oukari M, Korhonen VP, Keinanen T, Alhonen L, Janne J. Concurrent overexpression of ornithine decarboxylase and spermidine/spermine N(1)-acetyltransferase further accelerates the catabolism of hepatic polyamines in transgenic mice. Biochem J 358: 343-348, 2001.
35. 1-acetyltransferase. Cancer Res 65: 5390-5398, 2005.
36. Wang Z, Zahedi K, Barone S, Tehrani K, Rabb H, Matlin K, Casero RA, Soleimani M. Overexpression of SSAT in kidney cells recapitulates various phenotypic aspects of kidney ischemia-reperfusion injury. J Am Soc Nephrol 15: 1844-1852, 2004.
37. 1- acetyltransferase overexpression in kidney epithelial cells disrupts polyamine homeostasis, leads to DNA damage, and causes G2 arrest. Am J Physiol Cell Physiol 292: C1204-C1215, 2007.
38. Zahedi K, Wang Z, Barone S, Prada AE, Kelly CN, Casero RA, Yokota N, Porter CW, Rabb H, Soleimani M. Expression of SSAT, a novel biomarker of tubular cell damage, increases in kidney ischemia-reperfusion injury. Am J Physiol Renal Physiol 284: F1046-F1055, 2003.
39. Zhang M, Borovikova LV, Wang H, Metz C, Tracey KJ. Spermine inhibition of monocyte activation and inflammation. Mol Med 5: 595-605, 1999.
40. Zhang M, Caragine T, Wang H, Cohen PS, Botchkina G, Soda K, Bianchi M, Ulrich P, Cerami A, Sherry B, Tracey KJ. Spermine inhibits proinflammatory cytokine synthesis in human mononuclear cells: a counterregulatory mechanism that restrains the immune response. J Exp Med 185: 1759-1768, 1997.
41. Zhang M, Wang H, Tracey KJ. Regulation of macrophage activation and inflammation by spermine: a new chapter in an old story. Crit Care Med 28: N60-N66, 2000.
42. Zhang W, Wang M, Xie HY, Zhou L, Meng XQ, Shi J, Zheng S. Role of reactive oxygen species in mediating hepatic ischemia-reperfusion injury and its therapeutic applications in liver transplantation. Transplant Proc 39: 1332-1337, 2007.
43. Zhao YJ, Xu CQ, Zhang WH, Zhang L, Bian SL, Huang Q, Sun HL, Li QF, Zhang YQ, Tian Y, Wang R, Yang BF, Li WM. Role of polyamines in myocardial ischemia/reperfusion injury and their interactions with nitric oxide. Eur J Pharmacol 562: 236-246, 2007.
44. Zweier JL, Duilio C, Kuppusamy P, Santoro G, Elia PP, Tritto I, Cirillo P, Condorelli M, Chiariello M. A short burst of oxygen radicals at reflow induces sustained release of oxidized glutathione from postischemic hearts. J Biol Chem 268: 18532-18541, 1993.