Nanomedicine: Nanotechnology, Biology and Medicine
Volume 4, Issue 4 , Pages 283-294 , December 2008

SOD Activity of carboxyfullerenes predicts their neuroprotective efficacy: a structure-activity study

  • Sameh Saad Ali, PhD

      Affiliations

    • Department of Medicine, University of California, San Diego, California
    • Corresponding Author InformationCorresponding author. Division of Geriatrics, Department of Medicine, University of California, SCRB/SOM, Mailcode 0746, La Jolla, California, USA 92093-0746.
    • ,
  • Joshua I. Hardt, BS

      Affiliations

    • Department of Neurology, Washington University School of Medicine, St. Louis Missouri
    • ,
  • Laura L. Dugan, MD

      Affiliations

    • Department of Medicine, University of California, San Diego, California
    • Departments of Medicine and Neurosciences, University of California, San Diego, California, USA

Received 13 March 2008 ,Accepted 9 May 2008.

References 

  1. Finkel T. Oxidant signals and oxidative stress. Curr Opin Cell Biol. 2003;15:247–254
  2. Liu H, Colavitti R, Rovira II, Finkel T. Redox-dependent transcriptional regulation. Circ Res. 2005;97:967–974
  3. McCord JM, Edeas MA. SOD, oxidative stress and human pathologies: a brief history and a future vision. Biomed Pharmacother. 2005;59:139–142
  4. Maren S, Baudry M. Properties and mechanisms of long-term synaptic plasticity in the mammalian brain: relationships to learning and memory. Neurobiol Learn Mem. 1995;63:1–18
  5. Asztely F, Gustafsson B. Ionotropic glutamate receptors. Their possible role in the expression of hippocampal synaptic plasticity. Mol Neurobiol. 1996;12:1–11
  6. Nakanishi S. Molecular diversity of glutamate receptors and implications for brain function. Science. 1992;258:597–603
  7. Nakanishi S, Nakajima Y, Masu M, Ueda Y, Nakahara K, Watanabe D, et al. Glutamate receptors: brain function and signal transduction. Brain Res Brain Res Rev. 1998;26:230–235
  8. Brauner-Osborne H, Egebjerg J, Nielsen EO, Madsen U, Krogsgaard-Larsen P. Ligands for glutamate receptors: design and therapeutic prospects. J Med Chem. 2000;43:2609–2645
  9. Dingledine R, Borges K, Bowie D, Traynelis SF. The glutamate receptor ion channels. Pharmacol Rev. 1999;51:7–61
  10. Choi D. Antagonizing excitotoxicity: a therapeutic strategy for stroke?. Mt Sinai J Med. 1998;65:133–138
  11. Beal MF, Howell N, Bodis-Wollner I. Mitochondria and free radicals in neurodegenerative diseases. New York: John Wiley and Sons; 1997;
  12. Reynolds IJ, Hastings TG. Glutamate induces the production of reactive oxygen species in cultured forebrain neurons following NMDA receptor activation. J Neurosci. 1995;15:3318–3327
  13. Dugan LL, Sensi SL, Canzoniero LM, Handran SD, Rothman SM, Lin TS, et al. Mitochondrial production of reactive oxygen species in cortical neurons following exposure to N-methyl-d-aspartate. J Neurosci. 1995;15:6377–6388
  14. Bindokas VP, Jordan J, Lee CC, Miller RJ. Superoxide production in rat hippocampal neurons: selective imaging with hydroethidine. J Neurosci. 1996;16:1324–1336
  15. Sengpiel B, Preis E, Krieglstein J, Prehn JH. NMDA-induced superoxide production and neurotoxicity in cultured rat hippocampal neurons: role of mitochondria. Eur J Neurosci. 1998;10:1903–1910
  16. Dugan LL, Gabrielesen JK, Yu SP, Lin T-S, Choi DW. Buckminsterfullerenol free radical scavengers reduce ex-cytotoxic and apoptotic death of cultured cortical neurons. Neurobiol Dis. 1996;3:129-35, 305-10.
  17. Budd SL, Nicholls DG. Mitochondria, calcium regulation, and acute glutamate excitotoxicity in cultured cerebellar granule cells. J Neurochem. 1996;67:2282–2291
  18. Monyer H, Hartley DM, Choi DW. 21-Aminosteroids attenuate excitotoxic neuronal injury in cortical cell cultures. Neuron. 1990;5:121–126
  19. Dugan LL, Turetsky DM, Du C, Lobner D, Wheeler M, Almli CR, et al. Carboxyfullerenes as neuroprotective agents. Proc Natl Acad Sci U S A. 1997;94:9434–9439
  20. Tauskela JS, Brunette E, O'Reilly N, Mealing G, Comas T, Gendron TF, et al. An alternative Ca2+-dependent mechanism of neuroprotection by the metalloporphyrin class of superoxide dismutase mimetics. FASEB J. 2005;19:1734–1736
  21. Rosen GM, Britigan BE, Halpern HJ, Pou S. Free radicals, biology and detection by spin trapping. New York: Oxford University Press; 1999;
  22. Utsumi H, Yamada K, Ichikawa K, Sakai K, Kinoshita Y, Matsumoto S, et al. Simultaneous molecular imaging of redox reactions monitored by Overhauser-enhanced MRI with 14N- and 15N-labeled nitroxyl radicals. Proc Natl Acad Sci U S A. 2006;103:1463–1468
  23. Sola M, Mestres J, Duran M. Molecular size and pyramidalization: two keys for understanding the reactivity of fullerenes. J Phys Chem. 1995;99:10752–10758
  24. Haddon RC, Palmer RE, Kroto HW, Sermon PA. The fullerenes: powerful carbon-based electron acceptors. Philos Trans Phys Sci Eng. 1993;343:53–62
  25. Diener MD, Alford JM. Isolation and properties of small-bandgap fullerenes. Nature. 1998;393:668–671
  26. Ali SS, Hardt JI, Quick KL, Kim-Han JS, Erlanger BF, Huang TT, et al. A biologically effective fullerene (C60) derivative with superoxide dismutase mimetic properties. Free Radic Biol Med. 2004;37:1191–1202
  27. Ali SS, Xiong C, Lucero J, Behrens MM, Dugan LL, Quick KL. Gender differences in free radical homeostasis during aging: shorter-lived female C57BL6 mice have increased oxidative stress. Aging Cell. 2006;5:565–574
  28. 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
  29. Behrens MM, Ali SS, Dao DN, Lucero J, Shekhtman G, Quick KL, et al. Ketamine-induced loss of phenotype of fast-spiking interneurons is mediated by NADPH-oxidase. Science. 2007;318:1645–1647
  30. Koh JY, Choi DW. Quantitative determination of glutamate mediated cortical neuronal injury in cell culture by lactate dehydrogenase efflux assay. J Neurosci Methods. 1987;20:83–90
  31. Furukawa H, Singh SK, Mancusso R, Gouaux E. Subunit arrangement and function in NMDA receptors. Nature. 2005;438:185–192
  32. Furukawa H, Gouaux E. Mechanisms of activation, inhibition and specificity: crystal structures of the NMDA receptor NR1 ligand-binding core. EMBO J. 2003;22:2873–2885
  33. Wang X, Quinn PJ. The location and function of vitamin E in membranes. Mol Membr Biol. 2000;17:143–156
  34. Quick KL, Hardt JI, Dugan LL. Rapid microplate assay for superoxide scavenging efficiency. J Neurosci Methods. 2000;97:139–144
  35. McCord JM, Fridovich I. Superoxide dismutase. an enzymic function for erythrocuprein (hemocuprein). J Biol Chem. 1969;244:6049–6055
  36. Gotoh N, Niki E. Rates of interactions of superoxide with vitamin E, vitamin C and related compounds as measured by chemiluminescence. Biochim Biophys Acta. 1992;1115:201–207
  37. Chen PE, Wyllie DJ. Pharmacological insights obtained from structure-function studies of ionotropic glutamate receptors. Br J Pharmacol. 2006;147:839–853
  38. Dugan LL, Lovett E, Cuddihy S, Almli CR, Lin T-S, Choi DW. Carboxyfullerenes as neuroprotective antioxidants. In:  Kreiglstein J editors. Pharmacology of Cerebral Ischemia. New York: Academic Press; 1998;p. 257–266
  39. Choi DW. Glutamate neurotoxicity and diseases of the nervous system. Neuron. 1988;1:623–634
  40. Choi DW, Rothman SM. The role of glutamate neurotoxicity in hypoxic-ischemic neuronal death. Annu Rev Neurosci. 1990;13:171–182
  41. Gardoni F, Di Luca M. New targets for pharmacological intervention in the glutamatergic synapse. Eur J Pharmacol. 2006;545:2–10
  42. Foley S, Crowley C, Smaihi M, Bonfils C, Erlanger BF, Seta P, et al. Cellular localization of a water-soluble fullerene derivative. Biochem Biophys Res Commun. 2002;294:116–119
  43. Lotharius J, Dugan LL, O'Malley KL. Distinct mechanisms underlie neurotoxin-mediated cell death in cultured dopaminergic neurons. J Neurosci. 1999;19:1284–1293

 This work was funded by a Paul Beeson Physician Scholar Award, the Selma I. Hartke fund for aging research, and NIH NS47966 (L.L.D.).

PII: S1549-9634(08)00083-X

doi: 10.1016/j.nano.2008.05.003

Nanomedicine: Nanotechnology, Biology and Medicine
Volume 4, Issue 4 , Pages 283-294 , December 2008

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