Branched chain amino acids induce apoptosis in neural cells without mitochondrial membrane depolarization or cytochrome c release: Implications for neurological impairment associated with maple syrup urine disease

Molecular Biology of the Cell

Volumn 11, Issue 5, 2000, Pages 1919-1932

  Jouvet, Philippe ^a   Rustin, Pierre ^b   Taylor, Deanna L ^a   Pocock, Jennifer M ^c   Felderhoff Mueser, Ursula ^a   Mazarakis, Nicholas D ^a,d   Sarraf, Catherine ^a   Joashi, Umesh ^a   Kozma, Mary ^a   Greenwood, Kirsty ^a   David Edwards, A ^a   Mehmet, Huseyin ^a  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b HÔPITAL NECKER ENFANTS MALADES   (France)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d OXFORD BIOMEDICA UK LTD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

2 OXOACID DEHYDROGENASE; 2 OXOISOCAPROIC ACID; BRANCHED CHAIN AMINO ACID; CYTOCHROME C OXIDASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL RESPIRATION; CONTROLLED STUDY; CYTOSOL; DEGENERATIVE DISEASE; ENZYME RELEASE; GLIA CELL; INBORN ERROR OF METABOLISM; MAPLE SYRUP URINE DISEASE; MEMBRANE DEPOLARIZATION; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; MOUSE; NERVE CELL; NEUROLOGICAL COMPLICATION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; RESPIRATORY CHAIN;

EID: 0034108632     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.11.5.1919     Document Type: Article

References (56)

1. Adachi, S., Cross, A.R., Babior, B.M., and Gottlieb, R.A. (1997). Bcl-2 and the outer mitochondrial membrane in the inactivation of cytochrome c during Fas-mediated apoptosis. J. Biol. Chem. 272, 21878-21882.
2. Ansari, B., Coates, P., Greenstein, B., and Hall, P. (1993). In situ end-labeling detects DNA strand breaks in apoptosis and other physiological and pathological states. J. Pathol. 170, 1-8.
3. Barres, B.A., Hart, I.K., Coles, H.S.R., Burne, J.F., Voyvodic, J.T., Richardson, W.D., and Raff, M.C. (1992). Cell death and control of cell survival in the oligodendrocyte lineage. Cell 70, 31-46.
4. Bindokas, V.P., Lee, C.C., Colmers, W.F., and Miller, R.J. (1998). Changes in mitochondrial function resulting from synaptic activity in the rat hippocampal slice. J. Neurosci. 18, 4570-4587.
5. Bissel, M., Bensch, K., and Herman, M. (1974). Effects of maple syrup urine disease metabolites on mouse L-fibroblasts in vitro: a fine structural and biochemical study. J. Neurochem. 22, 957-964.
6. Bossy-Wetzel, E., Newmeyer, D., and Green, D. (1998). Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. EMBO J. 17, 37-49.
7. Bradford, M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
8. Brand, K., Hauschildt, S., and Lüthje, J. (1984). Effect of diets on the activity of enzymes involved in branched chain α-keto acid metabolism. In: Branched Chain Amino and Keto Acids in Health and Disease, vol. 1, ed. S.A. Adibi, W. Fekl, U. Langenbeck, and P. Schauder, Basel: Karger, 100-111.
9. Brismar, J., Aqeel, A., Brismar, G., Coates, R., Gascon, G., and Ozand, P. (1990). Maple syrup urine disease: findings on CT and MR scans of the brain in 10 infants. AJNR Am. J. Neuroradiol. 11, 1219-1228.
10. Chauhan, D., Pandey, P., Ogata, A., Teoh, G., Krett, N., Halgren, R., Rosen, S., Kufe, D., Kharbanda, S., and Anderson, K. (1997). Cytochrome odependent and -independent induction of apoptosis in multiple myeloma cells. J. Biol. Chem. 272, 29995-29997.
11. Collarini, E.J., Kuhn, R., Marshall, C.J., Monuki, E.S., Lemke, G., and Richardson, W.D. (1992). Down-regulation of the POU transcription factor SCIP is an early event in oligodendrocyte differentiation in vitro. Development 116, 193-200.
12. Drenou, B., Blancheteau, V., Burgess, D.H., Fauchet, R., Charron, D.J., and Mooney, N.A. (1999). A caspase-independent pathway of MHC class II antigen-mediated apoptosis of human B lymphocytes. J. Immunol. 163, 4115-4124.
13. Dreyfus, P., and Prensky, A. (1967). Further observations on the biochemical lesion in maple syrup urine disease. Nature 214, 276.
14. Finucane, D.M., Waterhouse, N.J., Amarante-Mendes, G.P., Cotter, T.G., and Green, D.R. (1999). Collapse of the inner mitochondrial transmembrane potential is not required for apoptosis of HL60 cells. Exp. Cell Res. 25, 166-174.
15. Garland, J.M., Sondergaard, K.L., and Jolly, J. (1997). Redox regulation of apoptosis in interleukin-3-dependent hemopoietic cells: absence of alteration in both mitochondrial membrane potential (delta psi (m)) and free radical production during apoptosis induced by IL3 withdrawal. Br. J. Haematol. 99, 756-765.
16. Ha, H.C., Woster, P.M., and Casero, R.A., Jr. (1998). Unsymmetrically substituted polyamine analogue induces caspase-independent programmed cell death in Bcl-2-overexpressing cells. Cancer Res. 58, 2711-2714.
17. Hansen, M., Nielsen, S., and Berg, K. (1989). Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill. J. Immunol. Methods 119, 203-210.
18. Hockenbery, D., Oltvai, Z., Yin, X., Milliman, C., and Korsmeyer, S. (1993). Bcl-2 functions in an antioxidant pathway to prevent apo-ptosis. Cell 75, 241-251.
19. Jackson, R., and Singer, T. (1983). Inhibition of the 2-ketoglutarate and pyruvate dehydrogenase complexes of beef heart by branched chain keto acids. J. Biol. Chem. 258, 1857-1865.
20. Joashi, U.C., Greenwood, K., Taylor, D., Kozma, M., Mazarakis, N.D., Edwards, A.D., and Mehmet, H. (1999). Poly (ADP ribose) polymerase cleavage precedes neuronal death in the hippocampus and cerebellum following injury to the developing rat forebrain. Eur. J. Neurosci. 11, 91-100.
21. Jones, B.E., Lo, C.R., Liu, H., Srinivasan, A., Streetz, K., Valentino, K.L., and Czaja M.J. (2000). Hepatocytes sensitized to tumor necrosis factor-alpha cytotoxicity undergo apoptosis through caspase-dependent and caspase-independent pathways. J. Biol. Chem. 275, 705-712.
22. Khan, S., Kayahara, M., Joashi, U., Mazarakis, N.D., Sarraf, C., Edwards, A.D., Hughes, M.N., and Mehmet, H. (1997). Differential induction of apoptosis in Swiss 3T3 cells by nitric oxide and the nitrosonium cation. J. Cell Sci. 110, 2315-2322.
23. Kluck, R., Bossy-Wetzel, E., Green, D., and Newmeyer, D. (1997). The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275, 1132-1136.
24. Krippner, A., Matsuno-Yagi, A., Gottlieb, R., and Babior, B. (1996). Loss of function of cytochrome c in jurkat cells undergoing Fas-mediated apoptosis. J. Biol. Chem. 271, 21629-21636.
25. Laird, P., Zijderveld, A., Linders, K., Rudnicki, M., Jaenisch, M., and Berns, A. (1991). Simplified mammalian DNA isolation procedure. Nucleic Acids Res. 19, 4293.
26. Land, J., Mobray, J., and Clark, J. (1976). Control of pyruvate and β-hydroxybutyrate utilization in rat brain mitochondria and its relevance to phenylketonuria and maple syrup urine disease. J.Neurochem. 26, 823-830.
27. Langenbeck, U. (1984). Pathobiochemical and pathophysiologic analysis of the MSUD phenotype. In: Branched Chain Amino and Keto Acids in Health and Disease, vol. 1, ed. S.A. Adibi, W. Fekl, U. Langenbeck, and P. Schauder, Basel: Karger, 315-334.
28. Levin, M., Scheinmann, A., Lewis, R., and Beaudet, A. (1993). Cerebral edema in maple syrup urine disease. J. Pediatr. 122, 167-168.
29. Li, F., Srinivasan, A., Wang, Y., Armstrong, R., Tomaselli, K., and Fritz, L. (1997). Cell-specific induction of apoptosis by microinjection of cytochrome c. Bcl-xL has activity independent of cytochrome c release. J. Biol. Chem. 272, 30299-30305.
30. Liao, C., Herman, M., and Bensch, K. (1978). Prolongation of G1 and S phase in C-6 glioma cells treated with maple syrup urine disease metabolites. Morphologic and cell cycle studies. Lab. Invest. 38, 122-133.
31. Mateo, V., Lagneaux, L., Bron, D., Biron, G., Armant, M., Delespesse, G., and Sarfati, M. (1999). CD47 ligation induces caspase-independent cell death in chronic lymphocytic leukemia. Nat. Med. 5, 1277-1284.
32. Miller, T.M., Molder, K.L., Knudson, C.M., Creedon, D.J., Deshmukh, M., Korsmeyer, S.J., and Johnson, E.M., Jr. (1997). Bax deletion further orders the cell death pathway in cerebellar granule cells and suggests a caspase-independent pathway to cell death. J. Cell Biol. 139, 205-217.
33. Monney, L., Otter, I., Olivier, R., Ozer, H.L., Haas, A.L., Omura, S., and Borner, C. (1998). Defects in the ubiquitin pathway induce caspase-independent apoptosis blocked by Bcl-2. J. Biol. Chem. 273, 6121-6131.
34. Patel, M. (1974). Inhibition by the branched chain 2-oxoacids of the 2-oxoglutarate dehydrogenase complex in developing rat and human brain. Biochem. J. 144, 91-97.
35. Paterson, I., Zhang, D., Warrington, R., and Boulton, A. (1998). R-deprenyl and R-2-heptyl-N-methylpropargylamine prevent apoptosis in cerebellar granule neurons induced by cytosine arabino-side but not low extracellular potassium. J. Neurochem. 70, 515-523.
36. 2+ channel coupled to the exocytosis of L-glutamate from cerebellar granule cells is inhibited by the spider toxin Aga-GI. Neuropharmacology 32, 1185-1194.
37. Reers, M., Smith, T., and Chen, L. (1991). J-aggregate formation of a carbocyanine as a quantitative fluorescent indicator of membrane potential. Biochemistry 30, 4480-4486.
38. Rickwood, D., Wilson, M., and Darky-Usmar, V. (1987). Isolation and characteristics of intact mitochondria. In: Mitochondria: A Practical Approach, ed V. Darky-Usmar, D. Rickwood, and M. Wilson, Oxford: IRL Press, 1-16.
39. Riviello, J., Rezvani, I., DiGeorge, A., and Foley, C. (1991). Cerebral edema causing death in children with maple syrup urine disease. J. Pediatr. 119, 42-45.
40. Rustin, P., Chretien, D., Bourgeron, T., Gérard, B., Rštig, A., Saudubray, J.M., and Munnich, A. (1994). Biochemical and molecular investigations in respiratory chain deficiencies. Clin. Chim. Acta 228, 35-51.
41. Salvioli, S., Ardizzoni, A., Franceschi, C., and Cossarizza, A. (1997). JC-1, but not DiOC6 (3) or rhodamine 123, is a reliable fluorescent probe to assess Δψ changes in intact cells: implications for studies on mitochondrial functionality during apoptosis. FEBS Lett. 411, 77-82.
42. Scaduto, R.C., Jr., and Grotyohann, L.W. (1999). Measurement of mitochondrial membrane potential using fluorescent rhodamine derivatives. Biophys. J. 76, 469-477.
43. Sherwood, N., and Timiras, P. (1970). A Stereotaxic Atlas of the Developing Rat Brain, London: University of California Press, 78-141.
44. Silberberg, D. (1969). Maple syrup urine disease metabolites studied in cerebellum cultures. J. Neurochem. 16, 1141-1146.
45. Skaper, S., Molden, D., and Seegmiller, J. (1976). Maple syrup urine disease: branched-chain amino acid concentrations and metabolism in cultured human lymphoblasts. Biochem. Genet. 14, 527.
46. Smiley, S., Reers, M., and Motrola-Hartshorn, C. (1991). Intracellular heterogeneity in mitochondrial membrane potential revealed by a J-aggregate-forming lipophilic cation JC-1. Proc. Natl. Acad. Sci. USA 88, 3671-3675.
47. Snyderman, S. (1988). Treatment outcome of maple syrup urine disease. Acta Paediatr. Jpn. 30, 417-424.
48. Snyderman, S., Goldstein, F., Sansaricq, C., and Norton, P. (1984). The relationship between the branched chain amino acids and their α-keto acids in maple syrup urine disease. Pediatr. Res. 18, 851-853.
49. Steinlin, M., Blaser, S., and Boltshauser, E. (1998). Cerebellar involvement in metabolic disorders: a pattern-recognition approach. Neuroradiology 40, 347-354.
50. Tang, D., Li, L., Zhu, Z., and Joshi, B. (1998). Apoptosis in the absence of cytochrome c accumulation in the cytosol. Biochem. Biophys. Res. Commun. 242, 380-384.
51. Walajtys-Rode, E., and Williamson, J. (1980). Effects of branched chain α-ketoacids on the metabolism of isolated rat liver cells. J. Biol. Chem. 255, 413-418.
52. Wyllie, A., Arends, M., Morris, R., Walker, S., and Evan, G. (1992). The apoptosis endonuclease and its regulation. Semin. Immunol. 4, 389-397.
53. Wyllie, A., and Duvall, E. (1992). Cell injury and death. In: Oxford Textbook of Pathology, ed. P.I. Jo'D McGee and N.A. Wright, Oxford: Oxford University Press, 141-193.
54. Yan, G.M., Ni, B., Weller, M., Wood, K.A., and Paul, S.M. (1994). Depolarisation of glutamate receptor activations blocks apoptotic cell death of cultured cerebellar granule neurons. Brain Res. 656, 43-51.
55. Yang, J., Liu, X., Bhalla, K., Kim, C., Ibrado, A., Cai, J., Peng, T., Jones, D., and Wang, W. (1997). Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275, 1129-1132.
56. Zielke, H.R., Huang, Y., Baab, P.J., Collins, R.M., Zielke, C.L., and Tildon, J.T. (1997). Effect of alpha-ketoisocaproate and leucine on the in vivo oxidation of glutamate and glutamine in the rat brain. Neurochem. Res. 22, 1159-1164.