Neurobiology of Aging
Volume 31, Issue 3 , Pages 425-433 , March 2010

Prevention of cognitive deficits and brain oxidative stress with superoxide dismutase/catalase mimetics in aged mice

  • Aaron Clausen

      Affiliations

    • Neuroscience Program, University of Southern California, Los Angeles, CA 90089, USA
  • ,
  • Susan Doctrow

      Affiliations

    • Proteome Systems Inc., Woburn, MA 01801, USA
  • ,
  • Michel Baudry

      Affiliations

    • Neuroscience Program, University of Southern California, Los Angeles, CA 90089, USA
    • Corresponding Author InformationCorresponding author. HNB 534, University of Southern California, Los Angeles, CA 90089-2520, USA. Tel.: +1 213 740 9188; fax: +1 213 740 5687.

Received 9 February 2008 ,Revised 15 April 2008 ,Accepted 6 May 2008.

References 

  1. Barnes CA, Markowska AL, Ingram DK, Kametani H, Spangler EL, Lemken VJ, et al. Acetyl-1-carnitine. 2: effects on learning and memory performance of aged rats in simple and complex mazes. Neurobiol. Aging. 1990;11:499–506
  2. Boveris A, Chance B. The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem. J. 1973;134:707–716
  3. Bruce AJ, Baudry M. Oxygen free radicals in rat limbic structures after kainate-induced seizures. Free Radic. Biol. Med. 1995;18:993–1002
  4. Butterfield DA, Reed T, Perluigi M, De Marco C, Coccia R, Cini C, et al. Elevated protein-bound levels of the lipid peroxidation product 4-hydroxy-2-nonenal, in brain from persons with mild cognitive impairment. Neurosci. Lett. 2006;397:170–173
  5. Calabrese V, Scapagnini G, Ravagna A, Colombrita C, Spadaro F, Butterfield DA, et al. Increased expression of heat shock proteins in rat brain during aging: relationship with mitochondrial function and glutathione redox state. Mech. Ageing Dev. 2004;125:325–335
  6. Carney JM, Starke-Reed PE, Oliver CN, Landum RW, Cheng MS, Wu JF, et al. Reversal of age-related increase in brain protein oxidation, decrease in enzyme activity, and loss in temporal and spatial memory by chronic administration of the spin trapping compound N-tert-butyl-alpha-phenylnitrone. Proc. Natl. Acad. Sci. U.S.A. 1991;88:3633–3636
  7. Cini M, Moretti A. Studies on lipid peroxidation and protein oxidation in the aging brain. Neurobiol. Aging. 1995;16:53–57
  8. Davis HP, Small SA, Stern Y, Mayeux R, Feldstein SN, Keller FR. Acquisition, recall and forgetting of verbal information in long-term memory by young, middle-aged, and elderly individuals. Cortex. 2003;39:1063–1091
  9. Doctrow SR, Huffman K, Marcus CB, Tocco G, Malfroy E, Adinolfi CA, et al. Salen–manganese complexes as catalytic scavengers of hydrogen peroxide and cytoprotective agents: structure-activity relationship studies. J. Med. Chem. 2002;45:4549–4558
  10. Finkel T, Holbrook NJ. Oxidants, oxidative stress and the biology of ageing. Nature. 2000;408:239–247
  11. Forster MJ, Dubey A, Dawson KM, Stutts WA, Lal H, Sohal RS. Age-related losses of cognitive function and motor skills in mice are associated with oxidative protein damage in the brain. Proc. Natl. Acad. Sci. U.S.A. 1996;93:4765–4769
  12. Fukui K, Onodera K, Shinkai T, Suzuki S, Urano S. Impairment of learning and memory in rats caused by oxidative stress and aging, and changes in antioxidant defense mechanisms. Ann. N. Y. Acad. Sci. 2001;928:168–175
  13. Halliwell B. Reactive oxygen species and the central nervous system. J. Neurochem. 1992;59:1609–1623
  14. Hamilton ML, Van Remmen H, Drake JA, Yang H, Guo ZM, Kewitt K, et al. Does oxidative damage to DNA increase with age?. Proc. Natl. Acad. Sci. U.S.A. 2001;98:10469–10474
  15. Liu R, Liu IY, Bi X, Thompson RF, Doctrow SR, Malfroy B, et al. Reversal of age-related learning deficits and brain oxidative stress in mice with superoxide dismutase/catalase mimetics. Proc. Natl. Acad. Sci. U.S.A. 2003;100:8526–8531
  16. Malfroy-Camine, B., Doctrow, S.R., 2003. Cyclic salen metal complexes: reactive oxygen species scavengers useful as antioxidants for treatment and prevention of disease. U.S. Patent 6,589,948.
  17. Maren S, Aharonov G, Fanselow MS. Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats. Behav. Brain Res. 1997;88:261–274
  18. Melov S, Doctrow SR, Schneider JA, Haberson J, Patel M, Coskun PE, et al. Life extension and rescue of spongiform encephalopathy in superoxide dismutase 2 nulliygous mice treated with superoxide dismutase-catalase mimetics. J. Neurosci. 2001;21:8348–8353
  19. Melov S, Wolf N, Strozyk D, Doctrow SR, Bush AI. Mice transgenic for Alzheimer disease beta-amyloid develop lens cataracts that are rescued by antioxidant treatment. Free Radic. Biol. Med. 2005;38:258–261
  20. Nicolle MM, Gonzalez J, Sugaya K, Baskerville KA, Bryan D, Lund K, et al. Signatures of hippocampal oxidative stress in aged spatial learning-impaired rodents. Neuroscience. 2001;107:415–431
  21. O’Donnell E, Lynch MA. Dietary antioxidant supplementation reverses age-related neuronal changes. Neurobiol. Aging. 1998;19:461–467
  22. O’Donnell E, Vereker E, Lynch MA. Age-related impairment in LTP is accompanied by enhanced activity of stress-activated protein kinases: analysis of underlying mechanisms. Eur. J. Neurosci. 2000;12:345–352
  23. Petersen RC, Doody R, Kurz A, Mohs RC, Morris JC, Rabins PV, et al. Current concepts in mild cognitive impairment. Arch. Neurol. 2001;59:1985–1992
  24. Phillips RG, LeDoux JE. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 1992;106:274–285
  25. Quick KL, Ali SS, Arch R, Xiong C, Wozniak D, Dugan LL. A carboxyfullerene SOD mimetic improves cognition and extends the lifespan of mice. Neurobiol. Aging. 2008;29:117–128
  26. Raghavendra V, Kulkarni SK. Possible antioxidant mechanisms in melatonin reversal of aging and chronic ethanol-induced amnesia in plus-maze and passive avoidance memory tasks. Free Radic. Biol. Med. 2001;30:595–602
  27. Rao G, Xia E, Richardson A. Effect of age on the expression of antioxidant enzymes in male Fischer F344 rats. Mech. Ageing Dev. 1990;53:49–60
  28. Sawada M, Carlson JC. Changes in superoxide radical and lipid peroxide formation in the brain, heart, and liver during the lifetime of the rat. Mech. Ageing Dev. 1987;41:125–137
  29. Sharpe MA, Ollosson R, Stewart VC, Clark JB. Oxidation of nitric oxide by oxomanganese salen complexes: a new mechanism for cellular protection by superoxide dismutase/catalase mimetics. Biochem. J. 2002;366(Pt 1):97–107
  30. Siqueira RI, Fochesatto C, Da Silva Torres IL, Dalmaz C, Netto CA. Aging affects oxidative state in hippocampus, hypothalamus and adrenal glands of Wistar rats. Life Sci. 2005;78:271–278
  31. Sohal RS, Ku HH, Agarwal S, Forster MJ, Lal H. Oxidative damage, mitochondrial oxidant generation and antioxidant defenses during aging and in response to food restriction in the mouse. Mech. Ageing Dev. 1994;74:121–133
  32. Stoll S, Rostock A, Bartsch R, Korn E, Meichelbock A, Muller WE. The potent free radical scavenger alpha-lipoic acid improves cognition in rodents. Ann. N. Y. Acad. Sci. 1994;717:122–128

PII: S0197-4580(08)00151-6

doi: 10.1016/j.neurobiolaging.2008.05.009

Neurobiology of Aging
Volume 31, Issue 3 , Pages 425-433 , March 2010