Insulin-like growth factor-I mediates neuroprotection in proteasome inhibition-induced cytotoxicity in SH-SY5Y cells

Molecular and Cellular Neuroscience

Volumn 47, Issue 3, 2011, Pages 181-190

  Cheng, Benxu ^a,c   Maffi, Shivani Kaushal ^a,b   Martinez, Alex Anthony ^c   Acosta, Yolanda P Villarreal ^d   Morales, Liza D ^a   Roberts, James L ^c,e  

^a Medical Research Division   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^c Mays Cancer Center at UT Health San Antonio   (United States)

^d UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

^e TRINITY UNIVERSITY   (United States)

Author keywords

Apoptosis; Epoxomicin; IGF 1; Proteasome inhibition; SH SY5Y cells; Ubiquitin

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; CASPASE 3; CYTOCHROME C; EPOXOMICIN; PROTEIN KINASE B; RECOMBINANT SOMATOMEDIN C; UBIQUITINATED PROTEIN;

APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVATION; ENZYME RELEASE; HUMAN; HUMAN CELL; MITOCHONDRION; NEUROBLASTOMA CELL; NEUROPROTECTION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN PHOSPHORYLATION;

APOPTOSIS; CASPASE 3; CELL LINE, TUMOR; CELL SURVIVAL; CYTOPROTECTION; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; INSULIN-LIKE GROWTH FACTOR I; MITOCHONDRIA; NEURONS; NEUROPROTECTIVE AGENTS; OLIGOPEPTIDES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 79957644799     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2011.04.002     Document Type: Article

References (64)

1. Bianchi P., Seguelas M.-H., Parini A., Cambon C. Activation of pro-apoptotic cascade by dopamine in renal epithelial cells is fully dependent on hydrogen peroxide generation by monoamine oxidases. J. Amer. Soc. Nephrol. 2003, 14. 885-862.
2. Boutillier A.-L., Kienlen-Campard P., Loeffler J.-P. Depolarization regulates cyclin D1 degradation and neuronal apoptosis: a hypothesis about the role of the ubiquitin/proteasome signaling pathway. Eur. J. Neurosci. 1999, 11:441-448.
3. Canu N., Barbato C., Ciotti M.T., Serafino A., Dus L., Calissano P. Proteasome involvement and accumulation of ubiquitinated proteins in cerebellar granule neurons undergoing apoptosis. J. Neurosci. 2000, 20:589-599.
4. Carro E., Trejo J.L., Gomez-Isla T., LeRoith D., Torres-Aleman I. Serum Insulin-like growth factor-I regulates brain amyloid-beta levels. Nat. Med. 2002, 8:1390-1397.
5. Cheng H.L., Feldman E.L. Bidirectional regulation of p38 kinase and c-Jun N-terminal protein kinase by insulin-like growth factor-I. J. Biol. Chem. 1998, 273:14560-14565.
6. Coux O., Tanaka K., Goldberg A.L. Structure and functions of the 20S and 26S proteasomes. Annu. Rev. Biochem. 1996, 65:801-847.
7. Crowe E., Sell C., Thomas J.D., Johannes G.J., Torres C. Activation of proteasome by insulin-like growth factor-I may enhance clearance of oxidized proteins in the brain. Mech. Aging Dev. 2009, 130:793-800.
8. D'Ercole A.J., Ye P., Calikoglu A.S., Gutierrez-Ospina G. The role of the insulin-like growth factors in the central nervous system, (Review 190 refs.). Mol. Neurobiol. 1996, 13:227-255.
9. Datta S.R., Brunet A., Greenberg M.E. Cellular survival: a play in three AKTs. Gene dev. 1999, 13:2905-2927. (Review).
10. Ding Q., Keller J.N. Proteasome inhibition in oxidative stress neurotoxicity: implications for heat shock proteins. J. Neurochem. 2001, 77:1010-1017.
11. Ding Q., Bruce-Keller A.J., Chen Q., Keller J.N. Analysis of gene expression in neural cells subject to chronic proteasome inhibition. Free Radic. Biol. Med. 2004, 3:445-455.
12. Dore S., Kar S., Quirion R. Insulin-like growth factor-I protects and rescues hippocampal neurons against beta-amyloid- and human amylin-induced toxicity. Proc. Natl. Acad. Sci. U S A 1997, 94:4772-4777.
13. Drexler H.C. The role of p27kipl in proteasome inhibitor induced apoptosis. Cell Cycle. 2003, 2:438-441.
14. Encinas M., Iglesias M., Llecha N., Comella J.X. Extracellular-regulated kinases and phosphatidylinositol 3-kinase are involved in brain-derived neurotrophic factor-mediated survival and neuritogenesis of the neuroblastoma cell line SH-SY5Y. J. Neurochem. 1999, 73:1409-1421.
15. Feuillette S., Blard O., Lecourtois M., Frebourg T., Campion D., Dumanchin C. Tau is normally degraded by the proteasome. J. Neurosci. Res. 2005, 80:400-405.
16. Gurusamy N., Goswami S., Malik G., Das D.K. Oxidative injury induces selective rather than global inhibition of proteasomal activity. J. Mol. Cell. Cardiol. 2008, 44:419-428.
17. Gustafsson H., Soderdahl T., Jonsson G., Bratteng J.-O., Forsby A. Insulin-like growth factor type1 prevents hyperglycemia-induced uncoupling protein 3 down-regulation and oxidative stress. J. Neurosci. Res. 2004, 77:285-291.
18. Halvorsen E.M., Dennis J., Keeney P.M., Sturgill T.W., Tuttle J.B., Bennet J.P. Methylpyridinium (MPP+)- and nerve growth factor-induced changes in pro-and anti-apoptotic signaling pathways in SH-SY5Y neuroblastoma cells. Brain Res. 2002, 952:98-110.
19. Heck S., Lezoualc'h F., Engert S., Behl C. Insulin-like growth factor-1 mediated neuroprotection against oxidative stress is associated with activation of nuclear factor kappaB. J. Biol. Chem. 1999, 274:9828-9835.
20. Hsuan S.-L., Klintworth H.M., Xia Z. Basic fibroblast growth factor protects against rotenone-induced dopaminergic cell death through activation of extracellular signal-regulated kinases 1/2 and phosphatidylinositol-3 kinase pathway. J. Neurosci. 2006, 26:4481-4491.
21. Jian Z., Yu P.H. Involvement of extracellular signal-regulated kinases 1/2 and (phosphoinositide 3-kinase)/AKT signal pathways in acquired resistance against neurotoxin of 6-hydroxydopamine in SH-SY5Y cells following cell-cell interaction with astrocytes. Neurosci. 2005, 133. 405-401.
22. Kar S., Chabot J.G., Quirion R. Quantitative autoradiographic localization of [125I] insulin-like growth factor I, [125I] insulin-like growth factor II, and [125I]insulin receptor binding sites in developing and adult rat brain. J. Comp. Neur. 1993, 333:375-397.
23. Keller J.N., Hanni K.B., Markesbery W.R. Impaired proteasome function in Alzheimer's disease. J. Neurochem. 2000, 75:436-439.
24. Keller J.N., Huang F.F., Markesbery W.R. Decreased levels of proteasome activity and proteasome expression in aging spinal cord. Neurosci. 2000, 98:149-156.
25. Keller J.N., Gee J., Ding Q. The proteasome in brain aging. Aging Res. Rev. 2002, 1:279-293.
26. Kenchappa P., Yadav A., Singh G., Nandana S., Banerjee K. Rescue of TNFα-inhibited neuronal cells by IGF-1 involves AKT and c-Jun N-terminal kinases. J. Neurosci. Res. 2004, 76:466-474.
27. Kikuchi S., Shinpo K., Tsuji S., Takeuchi M., Yamagishi S., Makita Z., Niino M., Yabe I., Tashiro K. Effect of proteasome inhibitor on cultured mesencephalic dopaminergic cells. Brain Res. 2003, 964:228-236.
28. Kitada T., Asakawa S., Hattori N., Matsumine H., Yamamura Y., Minoshima S., Yokoki M., Mizuno Y., Shimizu N. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 1998, 392:605-608.
29. Koch A., Lehmann-Horn K., Dächsel J.C., Gasser T., Kahle P.J., lucking C.B. Proteasomal inhibition reduces parkin mRNA in PC12 and SH-SY5Y cells. Parkinsonism Rel. Disord. 2009, 15:220-225.
30. Kordower J.H., Kanaan N.M., Chu Y., Babu R.S., Stansell J., Terpstra B.T., Sortwell C.E., Steece-Collier K., Collier T.J. Failure of proteasome inhibitor administration to provide a model of Parkinson's disease in rats and monkeys. Ann. Neurol. 2006, 60:264-268.
31. Lackey B.R., Gray S.L., Henricks D.M. Actions and interactions of the IGF system in Alzheimer's disease: review and hypotheses. Growth Horm. IGF Res. 2000, 10:1-13.
32. Leroy E., Boyer R., Auburger G., Leube B., Ulm G., Mezey E., Harta G., Brownstein M.J., Jonnalagada S., Chernova T., Dehejia A., Lavedan C., Gasser T., Steinbach P.J., Wilkinson K.D., Polymeropoulos M.H. The ubiquitin pathway in Parkinson's disease. Nature 1998, 395:451-452.
33. Lopes U.G., Erhardt P., Yao R., Cooper G.M. p53-dependent induction of apoptosis by proteasome inhibitors. J. Biol. Chem. 1997, 172:12893-12896.
34. Lopez Salon M., MOrelli L., Castano E.M., Soto E.F., Pasquini J.M. Defective ubiquitination of cerebral protein in Alzheimer's disease. J. Neurosci. Res. 2000, 62:302-310.
35. Lu S., Hoestje S.M., Choo E., Epner D.E. Induction of caspase-dependent and -independent apoptosis in response to methionine restriction. Int. J. Oncol. 2003, 22:415-420.
36. Maffi S.K., Rathinam M.L., Cherian P.P., Pate W., Hamby-Mason R., Schenker S., Henderson G.I. Glutathione content as a potential mediator of the vulnerability of cultured fetal cortical neurons to ethanol-induced apoptosis. J. Neurosci. Res. 2008, 86:1064-1076.
37. Mattson M.P. Apoptosis in neurodegenerative disorders. Nat. Rev. Mol. Cell Biol. 2000, 1:120-129.
38. McNaught K.S., Jenner P. Proteasome function is impaired in substantia nigra in Parkinson's disease. Neurosci. Lett. 2001, 297:191-194.
39. McNaught K.S., Olanow C.W. Proteolytic stress: a unifying concept for the etiopathogenesis of Parkinson's Disease. Ann. Neurol. 2003, 53(Suppl. 3):S73-S86.
40. McNaught K.S., Bjorklund L.M., Belizaire R., Isacson O., Jenner P., Olanow C.W. Proteasome inhibition causes nigral degeneration with inclusion bodies in rats. Neuroreport 2002, 13:1437-1444.
41. McNaught K.S., Mytilineou C., Jonbaptiste R., Yabut J., Shashidharan P., Jennert P., Olanow C.W. Impairment of the ubiquitin-proteasome system causes dopaminergic cell death and inclusion body formation in ventral mesencephalic cultures. J. Neurochem. 2002, 81:301-306.
42. McNaught K.S., Belizaire R., Isacson O., Jenner P., Olanow C.W. Altered proteasomal function in sporadic Parkinson's Disease. Exp. Neurol. 2003, 179:38-46.
43. McNaught K.S., Perl D.P., Brownell A.L., Olanow C.W. Systemic exposure to proteasome inhibitors causes a progressive model of Parkinson's Disease. Ann. Neurol. 2004, 56:149-162.
44. Meng L., Mohan R., Kwok B.H.B., Elofsson M., Sin N., Crews C.M. Epoxomicin, a potent and selective proteasome inhibitor, exhibits in vivo anti inflammatory activity. Proc. Natl. Acad. Sci. U S A 1999, 96:10403-10408.
45. Moore D.J., West A.B., Dawson V.L., Dawson T.M. Molecular pathophysiology of Parkinson's Disease. Annu. Rev. Neurosci. 2005, 28:57-87.
46. Nitta A., Zheng W.-H., Quirion R. Insulin-like growth factor-1 prevents neuronal cell death induced by corticosterone through activation of the PI3K/AKT pathway. J. Neurosci. Res. 2004, 76:98-103.
47. Okada K., Wangpoengtrakul C., Osawa T., Toyokuni S., Tanaka K., Uchida K. 4-hydroxyl-2-nonenal-mediated impairment of intracellular proteolysis during oxidative stress. Identification of proteasomes as target molecules. J. Biol. Chem. 1999, 274:23787-23793.
48. Okubo Y., Blakesley V.A., STannard B., Gutkind S., Le Roith D. Insulin like growth factor-I inhibits the stress-activated protein kinase/c-Jun N-terminal kinase. J. Biol. Chem. 1998, 273:25961-25966.
49. Papa L., Rockwell P. Persistent mitochondrial dysfunction and oxidative stress hinder neuronal cell recovery from reversible proteasome inhibition. Apoptosis 2008, 13:588-599.
50. Papa L., Gomes E., Rockwell P. Reactive oxygen species induced by proteasome inhibition in neuronal cells mediate mitochondrial dysfunction and a caspase-independent cell death. Apoptosis 2007, 12:1389-1405.
51. Pasquini L.A., Besio Moreno M., Ademo A.M., Pasquini J.M., Soto E.F. Lactacystin, a specific inhibitor of the proteasome, induces apoptosis and activate caspase-3 in cultured cerebellar granule cells. J. Neurosci. Res. 2000, 59:601-611.
52. Polymeropoulos M.H., Lavedan C., Leroy E., Ide S.E., Dehejia A., Dutra A., Pike B., Root H., Rubenstein J., Boyer R., Stenroos E.S., Chandrasekharappa S., Athanassiadou A., Papapetropoulos T., Johnson W.G., Lazzarini A.M., Duvoisin R.C., Di Iorio G., Golbe L.I., Nussbaum R.L. Mutation in the alphasynuclein gene identified in families with Parkinson's disease. Science 1997, 276:2045-2047.
53. Princiotta M.F., Schubert U., Chen W., Bennink J.R., Myung J., Crews C.M., Yewdell J.W. Cells adapted to the proteasome inhibitor 4-hydroxy-5-iodo-3-nitrophenylacetyl-Leu-Leu-leucinal-vinyl sulfone require enzymatically active proteasomes for continued survival. Proc. Natl. Acad. Sci. U S A 2001, 98:513-518.
54. Qiu J.H., Asai A., Chi S., Saito N., Hamada H., Kirino T. Proteasome inhibitors induce cytochrome c-caspase-3-like protease-mediated apoptosis in cultured neurons. J. Neurosci. 2000, 20:259-265.
55. Reinheckel T., Sitte N., Ullrich O., Kuckelkorn U., Davies K.J., Grune T. Comparative resistance of the 20S and 26S proteasome to oxidative stress. Biochem. J. 1998, 335:637-642.
56. Saeki M., Maeda S., Wada K., Kamisaki Y. Insulin-like growth factor-1 protects peroxynitrite-induced cell death by preventing cytochrome c-induced caspase-3 activation. J. Cell. Biochem. 2002, 84:708-716.
57. Shavali S., Ren J., Ebadi M. Insulin-like growth factor-1 protects human dopaminergic SH-SY5Y cells from Salsolinol-induced toxicity. Neurosci. Lett. 2003, 340:79-82.
58. Tamatani M., Ogawa S., Niitsu Y., Tohyama M. Involvement of Bcl-2 family and caspase-3-like protease in NO-mediated neuronal apoptosis. J. Neurochem. 1998, 71:1588-1596.
59. Vestling M., Wiehager B., Tanii H., Cowburn R.F. AKT activity in presenilin 1 wild type and mutation transfected human SH-SY5Y neuroblastoma cells after serum deprivation and high glucose stress. J. Neurosci. Res. 2001, 66:448-456.
60. Wei W., Wang X., Kusiak J.W. Signaling events in amyloid β-peptide-induced neuronal death and insulin-like growth factor I protection. J. Biol. Chem. 2002, 277:17649-17656.
61. Xia Z., Dickens M., Raingeaud J., Davis R.J., Greenberg M.E. Opposing effects of ERK and JNK-p38 MAP kinase on apoptosis. Science 1995, 270:1326-1331.
62. Xing C., Peng Y., Chang R., Yin Y., Xie Z. Effects of insulin-like growth factor-1 on okadaic acid-induced apoptosis in SH-SY5Y cells. Cell Bio. Int. 2005, 29:803-808.
63. Yamamoto N., Sawada H., Izumi Y., Kume T., Katsuki H., Shimohama S. Proteasome inhibition induces glutathione synthesis and protects cells from oxidative stress. J. Biol. Chem. 2007, 282:4364-4372.
64. Zackenfels K., Oppenheim R.W., Rohrer H. Evidence for an important role of IGF-1 and IGF-II for the early development of chick sympathetic neurons. Neuron 1995, 14:731-741.