Liposome-delivered superoxide dismutase prevents nitric oxide-dependent motor neuron death induced by trophic factor withdrawal

Free Radical Biology and Medicine

Volumn 28, Issue 3, 2000, Pages 437-446

  Estévez, Alvaro G ^a,b   Sampson, Jacinda B ^a   Zhuang, Ying Xin ^a   Spear, Nathan ^a   Richardson, Gloria J ^a   Crow, John P ^a   Tarpey, Margaret M ^a   Barbeito, Luis ^b,c   Beckman, Joseph S ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

^c INSTITUTO DE INVESTIGACIONES BIOLÓGICAS CLEMENTE ESTABLE   (Uruguay)

Author keywords

Apoptosis; BDNF; Differentiation; Free radicals; Motor neuron; Nitric oxide; Peroxynitrite

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; COPPER ZINC SUPEROXIDE DISMUTASE; HYDROGEN PEROXIDE; LIPOSOME; N(G) METHYLARGININE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRITE; SUPEROXIDE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELL MATURATION; CELL SURVIVAL; CONTROLLED STUDY; CULTURE MEDIUM; EMBRYO; IMMUNOFLUORESCENCE; MOTONEURON; NERVE CELL CULTURE; NONHUMAN; PH; PRIORITY JOURNAL; RAT; TECHNIQUE;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CASPASES; CELL AGING; CELL DEATH; CELL SURVIVAL; CELLS, CULTURED; CYSTEINE PROTEINASE INHIBITORS; DRUG CARRIERS; EMBRYO; HUMANS; HYDROGEN PEROXIDE; LIPOSOMES; MOTOR NEURONS; NERVE DEGENERATION; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; OMEGA-N-METHYLARGININE; RATS; RECOMBINANT PROTEINS; SPINAL CORD; SUPEROXIDE DISMUTASE; TIME FACTORS;

EID: 0039852971     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0891-5849(99)00261-0     Document Type: Article

References (34)

1. Rosen D.R., Siddique T., Patterson D., Figlewicz D.A., Sapp P., Hentati A., Donaldson D., Goto J., O'Regan J.P., Deng H.-X., Rahmani Z., Krizus A., McKenna-Yasek D., Cayabyab A., Gaston S.M., Berger R., Tanszi R.E., Halperin J.J., Herzfeldt B., Van den Bergh R., Hung W.-Y., Bird T., Deng G., Mulder D.W., Smyth C., Lang N.G., Soriana E., Pericak-Vance M.A., Haines J., Rouleau G.A., Gusella J.S., Horvitz H.R., Brown R.H. Jr. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature. 362:1993;59-62.
2. Deng H.-X., Hentati A., Tainer J., Igbal Z., Cayabyab A., Hung W.-Y., Getzoff E., Hu P., Herzfeldt B., Roos R., Warner C., Deng G., Soriano E., Smyth C., Parge H., Ahmed A., Roses A., Hallewell R., Pericak-Vance M., Siddique T. Amyotrophic lateral sclerosis and structural defects in Cu, Zn superoxide dismutase. Science. 261:1993;1047-1051.
3. Gurney M.E., Pu H., Chiu A.Y., Dal Corto M.C., Polchow C.Y., Alexander D.D., Caliendo J., Hentati A., Kwon Y.W., Deng H.-X., Chen W., Zhai P., Sufit R.L., Siddique T. Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science. 264:1994;1772-1775.
4. Henderson C.E., Camu W., Mettling C., Gouin A., Poulsen K., Karihaloo M., Rullamas J., Evans T., McMahon S.B., Armanini M.P., Berkemeier L., Phillips H.S., Rosenthal A. Neurotrophins promote motor neuron survival and are present in embryonic limb bud. Nature. 363:1993;266-270.
5. Hughes R.A., Sendtner M., Thoenen H. Members of several gene families influence survival of rat motoneurons in vitro and in vivo. J. Neurosci. Res. 36:1993;663-671.
6. Henderson C.E., Phillips H.S., Pollock R.A., Davies A.M., Lemeulle C., Armanini M., Simpson L.C., Moffet B., Vandlen R.A., Koliatsos V.E., Rosenthal A. GDNF a potent survival factor for motoneurons present in peripheral nerve and muscle . Science. 266:1994;1062-1064.
7. Milligan C.E., Prevette D., Yaginuma H., Homma S., Cardwell C., Fritz L.C., Tomaselli K.J., Oppenheim R.W., Schwartz L.M. Peptide inhibitors of the ICE protease family arrest programmed cell death of motoneurons in vivo and in vitro. Neuron. 15:1995;385-393.
8. Pennica D., Arce V., Swanson T.A., Vejsada R., Pollock R.A., Armanini M., Dudley K., Phillips H.S., Rosenthal A., Kato A.C., Henderson C.E. Cardiotrophin-1, a cytokine present in embryonic muscle, supports long-term survival of spinal motoneurons. Neuron. 17:1996;63-74.
9. Estévez A.G., Spear N., Manuel S.M., Radi R., Henderson C.E., Barbeito L., Beckman J.S. Nitric oxide and superoxide contribute to motor neuron apoptosis induced by trophic factor deprivation. J. Neurosci. 18:1998;923-931.
10. Arce V., Pollock R., Philippe J., Pennica D., Henderson C., deLapeyrière O. Synergistic effects of Schwann-. and muscle-derived factors on motoneuron survival involved GDNF and Cardiotrophin (CT-1). J. Neurosci. 18:1998;1440-1448.
11. Estévez A.G., Spear N., Thompson J.A., Cornwell T.L., Radi R., Barbeito L., Beckman J.S. Nitric oxide dependent production of cGMP supports the survival of rat embryonic motor neurons cultured with brain derived neurotrophic factor. J. Neurosci. 18:1998;3708-3714.
12. Szabó C., Day B.J., Salzman A.L. Evaluation of the relative contribution of nitric oxide and peroxynitrite to the suppression of mitochondrial respiration in immunostimulated macrophages using a manganese mesoporphyrin superoxide dismutase mimetic and peroxynitrite scavenger. FEBS Lett. 381:1996;82-86.
13. Rothstein J.D., Bristol L.A., Hosler B., Brown R.H. Jr, Kuncl R.W. Chronic inhibition of superoxide dismutase produces apoptotic death of spinal neurons. Proc. Natl. Acad. Sci. USA. 91:1994;4155-4159.
14. Troy C.M., Shelanski M.L. Down-regulation of copper/zinc superoxide dismutase causes apoptotic death in PC12 neuronal cells. Proc. Natl. Acad. Sci. USA. 91:1994;6384-6387.
15. Troy C.M., Derossi D., Prochiantz A., Greene L.A., Shelanski M.L. Downregulation of Cu/Zn superoxide dismutase leads to cell death via the nitric oxide-peroxynitrite pathway. J. Neurosci. 16:1996;253-261.
16. Greenlund L.J., Deckwerth T.L., Johnson E.M. Superoxide dismutase delays neuronal apoptosis a role for reactive oxygen species in programmed neuronal death . Neuron. 14:1995;303-315.
17. Jordan J., Ghadge G.D., Prehn J.H.M., Toth P.T., Roos R.P., Miller R.J. Expression of human copper/zinc-superoxide dismutase inhibits the death of rat sympathetic neurons caused by withdrawal of nerve growth factor. Mol. Pharmacol. 47:1995;1095-1100.
18. Ghadge G.D., Lee J.P., Bindokas V.P., Jordan J., Ma L., Miller R.J., Roos R.P. Mutant superoxide dismutase-1-linked familial amyotrophic lateral sclerosis molecular mechanisms of neuronal death and protection . J. Neurosci. 17:1997;8756-8766.
19. Keller J.N., Kindy M.S., Holtsberg F.W., St.Clair D.K., Yen H.-C., Germeyer A., Steiner S.M., Bruce-Keller A.J., Hutchins J.B., Mattson M.P. Mitochondrial manganese superoxide dismutase prevents neural apoptosis and reduces ischemic brain injury suppression of peroxynitrite production, lipid peroxidation, and mitochondrial dysfunction . J. Neurosci. 18:1998;687-697.
20. Gonzalez-Zulueta M., Ensz L.M., Mukhina G., Lebovitz R.M., Zwacka R.M., Engelhard J.F., Oberley L.W., Dawson V.L., Dawson T.M. Manganese superoxide dismutase protects nNOS neurons from NMDA and nitric oxide-mediated neurotoxicity. J. Neurosci. 18:1998;2040-2055.
21. Brewer G.J., Torricelli J.R., Evege E.K., Price P.J. Optimized survival of hippocampal neurons in B27-supplemented Neurobasal™, a new serum-free medium combination. J. Neurosci. Res. 35:1993;567-576.
22. Chandler C.E., Parsons L.M., Hosang M., Shooter E.M. A monoclonal antibody modulates the interaction of nerve growth factor with PC12 cells. J. Biol. Chem. 259:1984;6882-6889.
23. Henderson C.E., Bloch-Gallego E., Camu W. Purification and culture of embryonic motorneurons. Cohen J., Wilkin G. Neural cell culture a practical approach . 1995;61-81 IRL Press, Oxford, England.
24. Yan Q., Johnson E.M. Jr. An immunohistochemical study of the nerve growth factor receptor in developing rats. J. Neurosci. 8:1988;3481-3498.
25. Ericson J., Thor S., Edlund T., Jessell T., Yamada T. Early stages of motor neuron differentiation revealed by expression of homeobox gene Islet-1. Science. 256:1992;1555-1560.
26. Tsuchida T., Ensini M., Morton S.B., Baldassare M., Edlund T., Jessell T.M., Pfaff S.L. Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell. 79:1994;957-970.
27. Herdergen T., Brecht S., Mayer B., Leah J., Kummer W., Bravo R., Zimmermann M. Long-lasting expression of JUN and KROX transcription factors and nitric oxide synthase in intrinsic neurons of the rat brain following axotomy. J. Neurosci. 13:1993;4130-4145.
28. Crow J.P., Sampson J.B., Zhuang Y., Thompson J.A., Beckman J.S. Decreased zinc affinity of amyotrophic lateral sclerosis-associated superoxide dismutase mutants leads to enhanced catalysis of tyrosine nitration by peroxynitrite. J. Neurochem. 69:1997;1936-1944.
29. Ischiropoulos H., Zhu L., Chen J., Tsai H.M., Martin J.C., Smith C.D., Beckman J.S. Peroxynitrite-mediated tyrosine nitration catalyzed by superoxide dismutase. Arch. Biochem. Biophys. 298:1992;431-437.
30. Hope M., Bally M., Webb G., Cullis P. Production of large unilamellar vesicles by a rapid extrussion procedure. Characterization of size distribution, trapped volume, and ability to maintain a membrane potential. Biochim. Biophys. Acta. 812:1985;55-65.
31. Briscoe P., Caniggia I., Graves A., Benson B., Huang L., Tanswell A.K., Freeman B.A. Delivery of superoxide dismutase to pulmonary epithelium via pH-sensitive liposomes. Amer. J. Physiol. 268:1995;L374-L380.
32. Kaal, E. C. A.; Veldman, H.; Sodaar, P.; Joosten, E. A. J.; Dop Bar P. R. Oxidant treatment causes a dose-dependent phenotype of apoptosis in cultured motoneurons. J. Neurosci. Res. 54:778-786; 1998.
33. Estévez A.G., Crow J.P., Sampson J.B., Reiter C., Zhuang Y.-X., Richardson G.J., Tarpey M.M., Barbeito L., Beckman J.S. Induction of nitric oxide-dependent apoptosis in motor neurons by zinc-deficient superoxide dismutase. Science. 286:1999;2498-2500.
34. Lyons T.J., Liu H., Goto J.J., Nersissian A., Roe J.A., Graden J.A., Café C., Ellerby L.M., Bredesen D.E., Gralla E.B., Valentine J.S. Mutations in copper-zinc superoxide dismutase that cause amyotrophic lateral sclerosis alter the zinc binding site and the redox behavior of the protein. Proc. Natl. Acad. Sci. USA. 93:1996;12240-12244.