Identification of Bax-interacting proteins in oligodendrocyte progenitors during glutamate excitotoxicity and perinatal hypoxia-ischemia

ASN Neuro

Volumn 5, Issue 5, 2013, Pages 377-390

  Simonishvili, Sopio ^a   Jain, Mohit Raja ^a   Li, Hong ^a   Levison, Steven W ^a   Wood, Teresa L ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Apoptosis; Bcl xL; Bid; Cofilin; Insulin like growth factor 1 (IGF I); Oligodendrocyte

Indexed keywords

COFILIN; GLUTAMIC ACID; PROTEIN BAX; PROTEIN BCL XL; SOMATOMEDIN C;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CULTURE; CELL FRACTIONATION; CONTROLLED STUDY; ENZYME ACTIVATION; EXCITOTOXICITY; FEMALE; FLOW CYTOMETRY; GLIA CELL; HYPOXIC ISCHEMIC ENCEPHALOPATHY; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; MALE; MASS SPECTROMETRY; NEWBORN; NONHUMAN; OLIGODENDROGLIA; PROTEIN ANALYSIS; RAT; STEM CELL; WESTERN BLOTTING; WHITE MATTER; ANIMAL; CEREBELLUM; CHEMISTRY; CULTURE MEDIUM; CYTOLOGY; DISEASE MODEL; DRUG EFFECT; GENE EXPRESSION REGULATION; HUMAN; METABOLISM; MITOCHONDRION; PATHOLOGY; PHYSIOLOGY; PROTEIN TRANSPORT; TIME; TOXICITY AND INTOXICATION; WISTAR RAT;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CELLS, CULTURED; CEREBELLUM; CULTURE MEDIA, CONDITIONED; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; GLUTAMIC ACID; HUMANS; HYPOXIA-ISCHEMIA, BRAIN; INSULIN-LIKE GROWTH FACTOR I; MITOCHONDRIA; NEUROTOXICITY SYNDROMES; OLIGODENDROGLIA; PROTEIN TRANSPORT; RATS; RATS, WISTAR; STEM CELLS; TIME FACTORS;

EID: 84892462488     PISSN: 17590914     EISSN: None     Source Type: Journal    
DOI: 10.1042/AN20130027     Document Type: Article

References (78)

1. 2+ influx through AMPA or kainate receptors alone is sufficient to initiate excitotoxicity in cultured oligodendrocytes. Neurobiol Disease 9:234-243.
2. Almad A, Sahinkaya FR, McTigue DM (2011) Oligodendrocyte fate after spinal cord injury. Neurotherapeutics 8:262-273.
3. Back SA, Luo NL, Borenstein NS, Levine JM, Volpe J, Kinney HC (2001) Late oligodendrocyte progenitors coincide with the developmental window of vulnerability for human perinatal white matter injury. J Neurosci 21:1302-1312.
4. Back SA, Craig A, Kayton RJ, Luo NL, Meshul CK, Allcock N, Fern R (2007) Hypoxia-ischemia preferentially triggers glutamate depletion from oligodendroglia and axons in perinatal cerebral white matter. J Cereb Blood Flow Metab 27:334-347.
5. Back SA, Han BH, Luo NL, Chricton CA, Xanthoudakis S, Tam J, Arvin KL, Holtzman DM (2002) Selective vulnerability of late oligodendrocyte progenitors to hypoxia-ischemia. J Neurosci 22:455-463.
6. Bankston AN, Mandler MD, Feng Y (2013) Oligodendroglia and neurotrophic factors in neurodegeneration. Neurosci Bull 29:216-228.
7. Bernstein BW, Bamburg JR (2010) ADF/cofilin: a functional node in cell biology. Trends Cell Biol 20:187-195.
8. Billen LP, Kokoski CL, Lovell JF, Leber B, Andrews DW (2008) Bcl-XL inhibits membrane permeabilization by competing with Bax. PLoS Biol6:e147.
9. Bossy-Wetzel E, Green DR (1999) Caspases induce cytochrome c release from mitochondria by activating cytosolic factors. J Biol Chem 274:17484-17490.
10. Bradke F, Dotti CG (2000) Differentiated neurons retain the capacity to generate axons from dendrites. Curr Biol 10:1467-1470.
11. Bradl M, Lassmann H (2010) Oligodendrocytes: biology and pathology. Acta Neuropathol 119:37-53.
12. Buser JR, Segovia KN, Dean JM, Nelson K, Beardsley D, Gong X, Luo NL, Ren J, Wan Y, Riddle A, McClure MM, Ji X, Derrick M, Hohimer AR, Back SA, Tan S (2010) Timing of appearance of late oligodendrocyte progenitors coincides with enhanced susceptibility of preterm rabbit cerebral white matter to hypoxia-ischemia. J Cereb Blood Flow Metab 30:1053-1065.
13. Buser JR, Maire J, Riddle A, Gong X, Nguyen T, Nelson K, Luo NL, Ren J, Struve J, Sherman LS, Miller SP, Chau V, Hendson G, Ballabh P, Grafe MR, Back SA (2012) Arrested preoligodendrocyte maturation contributes to myelination failure in premature infants. Ann Neurol 71:93-109.
14. Chipuk JE, Green DR (2008) How do BCL-2 proteins induce mitochondrial outer membrane permeabilization? Trends Cell Biol 18:157-164.
15. Chua BT, Volbracht C, Tan KO, Li R, Yu VC, Li P (2003) Mitochondrial translocation of cofilin is an early step in apoptosis induction. Nat Cell Biol 5:1083-1089.
16. Datta SR, Katsov A, Hu L, Petros A, Fesik SW, Yaffe MB, Greenberg ME (2000) 14-3-3 proteins and survival kinases cooperate to inactivate BAD by BH3 domain phosphorylation. Mol Cell 6:41-51.
17. Dong H, Fazzaro A, Xiang C, Korsmeyer SJ, Jacquin MF, McDonald JW (2003) Enhanced oligodendrocyte survival after spinal cord injury in Bax-deficient mice and mice with delayed Wallerian degeneration. J Neurosci 23:8682-8691.
18. Edlich F, Banerjee S, Suzuki M, Cleland MM, Arnoult D, Wang C, Neutzner A, Tjandra N, Youle RJ (2011) Bcl-x(L) retrotranslocates Bax from the mitochondria into the cytosol. Cell 145:104-116.
19. Falahati S, Breu M, Waickman AT, Phillips AW, Arauz EJ, Snyder S, Porambo M, Goeral K, Comi AM, Wilson MA, Johnston MV, Fatemi A (2013) Ischemia-induced neuroinflammation is associated with disrupted development of oligodendrocyte progenitors in a model of periventricular leukomalacia. Dev Neurosci 35:182-196.
20. Fox MA, Afshari FS, Alexander JK, Colello RJ, Fuss B (2006) Growth conelike sensorimotor structures are characteristic features of postmigratory, premyelinating oligodendrocytes. Glia 53:563-566.
21. Ghibelli L, Diederich M (2010) Multistep and multitask Bax activation. Mitochondrion 10:604-613.
22. Giam M, Huang DC, Bouillet P (2008) BH3-only proteins and their roles in programmed cell death. Oncogene 27 (Suppl 1):S128-S136.
23. Gill MB, Bockhorst K, Narayana P, Perez-Polo JR (2008) Bax shuttling after neonatal hypoxia-ischemia: hyperoxia effects. J Neurosci Res 86:3584-3604.
24. Gross A, Jockel J, Wei MC, Korsmeyer SJ (1998) Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis. EMBO J 17:3878-3885.
25. Hacker G, Weber A (2007) BH3-only proteins trigger cytochrome c release, but how? Arch Biochem Biophys 462:150-155.
26. Itoh T, Itoh A, Pleasure D (2003) Bcl-2-related protein family gene expression during oligodendroglial differentiation. J Neurochem 85:1500-1512.
27. Iwata M, Muneoka KT, Shirayama Y, Yamamoto A, Kawahara R (2005) A study of a dendritic marker, microtubule-associated protein 2 (MAP-2), in rats neonatally treated neurosteroids, pregnenolone and dehydroepiandrosterone (DHEA). Neurosci Lett 386:145-149.
28. Karadottir R, Cavelier P, Bergersen LH, Attwell D (2005) NMDA receptors are expressed in oligodendrocytes and activated in ischaemia. Nature 438:1162-1166.
29. Keller A, Nesvizhskii AI, Kolker E, Aebersold R (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74:5383-5392.
30. Klamt F, Zdanov S, Levine RL, Pariser A, Zhang Y, Zhang B, Yu LR, Veenstra TD, Shacter E (2009) Oxidant-induced apoptosis is mediated by oxidation of the actin-regulatory protein cofilin. Nat Cell Biol 11:1241-1246.
31. Labi V, Erlacher M, Kiessling S, Villunger A (2006) BH3-only proteins in cell death initiation, malignant disease and anticancer therapy. Cell Death Differ 13:1325-1338.
32. Lee Y, Morrison BM, Li Y, Lengacher S, Farah MH, Hoffman PN, Liu Y, Tsingalia A, Jin L, Zhang PW, Pellerin L, Magistretti PJ, Rothstein JD (2012) Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 487:443-448.
33. Lovell JF, Billen LP, Bindner S, Shamas-Din A, Fradin C, Leber B, Andrews DW (2008) Membrane binding by tBid initiates an ordered series of events culminating in membrane permeabilization by Bax. Cell 135:1074-1084.
34. Marsick BM, Flynn KC, Santiago-Medina M, Bamburg JR, Letourneau PC (2010) Activation of ADF/cofilin mediates attractive growth cone turning toward nerve growth factor and netrin-1. Dev Neurobiol 70:565-588.
35. Matute C, Ransom BR (2012) Roles of white matter in central nervous system pathophysiologies. ASN NEURO 4 (2):art:e00079, doi:10.1042/AN20110060.
36. Matute C, Sanchez-Gomez M, Martinez-Millan L, Miledi R (1997) Glutamate receptor-mediated toxicity in optic nerve oligodendrocytes. Proc Natl Acad Sci USA 94:8830-8835.
37. McCarthy K, de Vellis J (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 85:890-902.
38. McDonald J, Althomsons S, Hyrc K, Choi D, Goldberg M (1998a) Oligodendrocytes from forebrain are highly vulnerable to AKPA/kainate receptor-mediated excitotoxicity. Nat Med 4:291-297.
39. McDonald JW, Levine JM, Qu Y (1998b) Multiple classes of the oligodendrocyte lineage are highly vulnerable to excitotoxicity. NeuroReport 9:2757-2762.
40. McTigue DM, Tripathi RB (2008) The life, death, and replacement of oligodendrocytes in the adult CNS. J Neurochem 107:1-19.
41. Micu I, Jiang Q, Coderre E, Ridsdale A, Zhang L, Woulfe J, Yin X, Trapp BD, McRory JE, Rehak R, Zamponi GW, Wang W, Stys PK (2006) NMDA receptors mediate calcium accumulation in myelin during chemical ischaemia. Nature 439:988-992.
42. Mizuno K (2013) Signaling mechanisms and functional roles of cofilin phosphorylation and dephosphorylation. Cell Signal 25:457-469.
43. Ness JK, Wood TL (2002) Insulin-like growth factor I, but not neurotrophin-3, sustains Akt activation and provides long-term protection of immature oligodendrocytes from glutamate-mediated apoptosis. Mol Cell Neurosci 20:476-488.
44. Ness JK, Scaduto RC, Jr, Wood TL (2004) IGF-I prevents glutamate-mediated bax translocation and cytochrome C release in O4+ oligodendrocyte progenitors. Glia 46:183-194.
45. Ness JK, Romanko MJ, Rothstein RP, Wood TL, Levison SW (2001) Perinatal hypoxia-ischemia induces apoptotic and excitotoxic death of periventricular white matter oligodendrocyte progenitors. Dev Neurosci 23:203-208.
46. Nesvizhskii AI, Keller A, Kolker E, Aebersold R (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75:4646-4658.
47. Oka A, Belliveau MJ, Rosenberg PA, Volpe JJ (1993) Vulnerability of oligodendroglia to glutamate: pharmacology, mechanisms, and prevention. J Neurosci 13:1441-1453.
48. Pang Y, Zheng B, Fan LW, Rhodes PG, Cai Z (2007) IGF-1 protects oligodendrocyte progenitors against TNFα-induced damage by activation of PI3K/Akt and interruption of the mitochondrial apoptotic pathway. Glia 55:1099-1107.
49. Park E, Velumian AA, Fehlings MG (2004) The role of excitotoxicity in secondary mechanisms of spinal cord injury: a review with an emphasis on the implications for white matter degeneration. J Neurotrauma 21:754-774.
50. Patneau DK, Wright PW, Winters C, Mayer ML, Gallo V (1994) Glial cells of the oligodendrocyte lineage express both kainate-and AMPA-preferring subtypes of glutamate receptors. Neuron 12:357-371.
51. Petito CK, Olarte JP, Roberts B, Nowak TS, Pulsinelli WA (1998) Selective glial vulnerability following transient global ischemia in rat brain. J Neuropath Exp Neurol 57:231-238.
52. Philips T, Bento-Abreu A, Nonneman A, Haeck W, Staats K, Geelen V, Hersmus N, Kusters B, Van Den Bosch L, Van Damme P, Richardson WD, Robberecht W (2013) Oligodendrocyte dysfunction in the pathogenesis of amyotrophic lateral sclerosis. Brain 136:471-482.
53. Posadas I, Perez-Martinez FC, Guerra J, Sanchez-Verdu P, Cena V (2012) Cofilin activation mediates Bax translocation to mitochondria during excitotoxic neuronal death. J Neurochem 120:515-527.
54. Rice JE, Vannucci RC, Brierley JB (1981) The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann Neurol 9:131-141.
55. Romanko MJ, Zhu C, Bahr BA, Blomgren K, Levison SW (2007) Death effector activation in the subventricular zone subsequent to perinatal hypoxia/ischemia. J Neurochem 103:1121-1131.
56. Roy SS, Madesh M, Davies E, Antonsson B, Danial N, Hajnoczky G (2009) Bad targets the permeability transition pore independent of Bax or Bak to switch between Ca2+-dependent cell survival and death. Mol Cell 33:377-388.
57. Salter MG, Fern R (2005) NMDA receptors are expressed in developing oligodendrocyte processes and mediate injury. Nature 438:1167-1171.
58. Sanchez-Gomez MV, Alberdi E, Ibarretxe G, Torre I, Matute C (2003) Caspase-dependent and caspase-independent oligodendrocyte death mediated by AMPA and kainate receptors. J Neurosci 23:9519-9528.
59. Sanchez-Gomez MV, Alberdi E, Perez-Navarro E, Alberch J, Matute C (2011) Bax and calpain mediate excitotoxic oligodendrocyte death induced by activation of both AMPA and kainate receptors. J Neurosci 31:2996-3006.
60. Segovia KN, McClure M, Moravec M, Luo NL, Wan Y, Gong X, Riddle A, Craig A, Struve J, Sherman LS, Back SA (2008) Arrested oligodendrocyte lineage maturation in chronic perinatal white matter injury. Ann Neurol 63:520-530.
61. Sharpe JC, Arnoult D, Youle RJ (2004) Control of mitochondrial permeability by Bcl-2 family members. Biochim Biophys Acta 1644:107-113.
62. Slee EA, Adrain C, Martin SJ (1999) Serial killers: ordering caspase activation events in apoptosis. Cell Death Differ 6:1067-1074.
63. Slee EA, Keogh SA, Martin SJ (2000) Cleavage of BID during cytotoxic drug and UV radiation-induced apoptosis occurs downstream of the point of Bcl-2 action and is catalysed by caspase-3: a potential feedback loop for amplification of apoptosis-associated mitochondrial cytochrome c release. Cell Death Differ 7:556-565.
64. Soriano ME, Scorrano L (2011) Traveling Bax and forth from mitochondria to control apoptosis. Cell 145:15-17.
65. Tang HL, Le AH, Lung HL (2006) The increase in mitochondrial association with actin precedes Bax translocation in apoptosis. Biochem J 396:1-5.
66. Vogel S, Raulf N, Bregenhorn S, Biniossek ML, Maurer U, Czabotar P, Borner C (2012) Cytosolic Bax: does it require binding proteins to keep its pro-apoptotic activity in check? J Biol Chem 287:9112-9127.
67. Volpe J (2001) Perintal brain injury: from pathogenesis to neuroprotection. Ment Retard Dev Disabil Res Rev 7:56-64.
68. Vottier G, Pham H, Pansiot J, Biran V, Gressens P, Charriaut-Marlangue C, Baud O (2011) Deleterious effect of hyperoxia at birth on white matter damage in the newborn rat. Dev Neurosci 33:261-269.
69. Walensky LD, Gavathiotis E (2011) BAX unleashed: the biochemical transformation of an inactive cytosolic monomer into a toxic mitochondrial pore. Trends Biochem Sci 36:642-652.
70. Willis SN, Adams JM (2005) Life in the balance: how BH3-only proteins induce apoptosis. Curr Opin Cell Biol 17:617-625.
71. Willis SN, Fletcher JI, Kaufmann T, van Delft MF, Chen L, Czabotar PE, Ierino H, Lee EF, Fairlie WD, Bouillet P, Strasser A, Kluck RM, Adams JM, Huang DC (2007) Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science 315:856-859.
72. Wood TL, Loladze V, Altieri S, Gangoli N, Levison SW, Brywe KG, Mallard C, Hagberg H (2007) Delayed IGF-1 administration rescues oligodendrocyte progenitors from glutamate-induced cell death and hypoxic-ischemic brain damage. Dev Neurosci 29:302-310.
73. Wu C, Parrott AM, Liu T, Jain MR, Yang Y, Sadoshima J, Li H (2011) Distinction of thioredoxin transnitrosylation and denitrosylation target proteins by the ICAT quantitative approach. J Proteomics 74:2498-2509.
74. Yin XM (2006) Bid, a BH3-only multi-functional molecule, is at the cross road of life and death. Gene 369:7-19.
75. Yoshioka A, Bacskai B, Pleasure D (1996) Pathophysiology of oligodendroglial excitotoxicity. J Neurosci Res 46:427-437.
76. Yoshioka A, Hardy M, Younkin D, Grinspan J, Stern J, Pleasure D (1995) α-Amino-3-hydroxy-5-methyl-4-isoxazolepropionate (AMPA) receptors mediate excitotoxicity in the oligodendroglial lineage. J Neurochem 64:2442-2448.
77. Yoshioka A, Yamaya Y, Saiki S, Kanemoto M, Hirose G, Beesley J, Pleasure D (2000) Non-N-methyl-D-aspartate glutamate receptors mediate oxygen-glucose deprivation-induced oligodendroglial injury. Brain Res 854:207-215.
78. Young G, Levison S (1997) An improved method for propagating oligodendrocyte progenitors in vitro. J Neurosci Methods 77:163-168.