Yeast as a tool to study Bax/mitochondrial interactions in cell death

FEMS Yeast Research

Volumn 4, Issue 1, 2003, Pages 15-27

  Priault, Muriel ^a   Camougrand, Nadine ^a   Kinnally, Kathleen W ^b   Vallette, François M ^c   Manon, Stéphen ^a  

^a Institut de Biochimie et Genetique Cellulaires   (France)

^b NEW YORK UNIVERSITY   (United States)

^c INSERM   (France)

Author keywords

AIF, apoptosis inducing factor; ANT, adenine nucleotide translocator; Apoptosis; Autophagy; Bax; Cytochrome c; MAC, mitochondrial apoptosis induced channel; Mitochondrion; PTP, permeability transition pore; ROS, reactive oxygen species; Yeast

Indexed keywords

CYTOCHROME C; MITOCHONDRIAL PROTEIN; OXYGEN; PROTEIN; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BID;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; APOPTOSIS; AUTOPHAGY; CARBOXY TERMINAL SEQUENCE; CELL DEATH; CELL PERMEABILIZATION; DEGRADATION; HYPOTHESIS; MITOCHONDRION; MODEL; MOLECULAR MECHANICS; NONHUMAN; OUTER MEMBRANE; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN SECRETION; REGULATORY MECHANISM; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; SHORT SURVEY; SIGNAL TRANSDUCTION; YEAST;

APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; GENE EXPRESSION REGULATION; MITOCHONDRIA; MODELS, GENETIC; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; SACCHAROMYCES CEREVISIAE;

INSERTION SEQUENCES; MYCOBACTERIUM AVIUM COMPLEX (MAC); SACCHAROMYCES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 1042264219     PISSN: 15671356     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1567-1356(03)00143-0     Document Type: Short Survey

References (115)

1. Gross A., McDonnell J.M., Korsmeyer S.J. Bcl-2 family members and the mitochondria in apoptosis. Genes Dev. 13:1999;1899-1911.
2. Adams J.M., Cory S. Life-or-death decisions by the Bcl-2 protein family. Trends Biochem. Sci. 26:2001;61-66.
3. Mignotte B., Vayssière J.L. Mitochondria and apoptosis. Eur. J. Biochem. 252:1998;1-15.
4. Cai J., Yang J., Jones D.P. Mitochondrial control of apoptosis: the role of cytochrome c. Biochim. Biophys. Acta. 1366:1998;139-149.
5. Desagher S., Martinou J.C. Mitochondria as the central control point of apoptosis. Trends Cell Biol. 10:2000;369-377.
6. Muchmore S.W., Sattler M., Liang H., Meadows R.P., Harlan J.E., Yoon H.S., Nettesheim D.G., Chang B.S., Thompson C.B., Wong S.L., Ng S.L., Fesik F.W. X-ray and NMR structure of human Bcl-xL, an inhibitor of programmed cell death. Nature. 381:1996;335-341.
7. Suzuki M., Youle R.J., Tjandra N. Structure of Bax: coregulation of dimer formation and intracellular localization. Cell. 103:2000;645-654.
8. Petros A.M., Medek A., Nettesheim D.G., Kim D.H., Yoon H.S., Swift K., Matayoshi E.D., Oltersdorf T., Fesik F.W. Solution structure of the antiapoptotic protein Bcl-2. Proc. Natl. Acad. Sci. USA. 98:2001;3012-3017.
9. Cheng E.H., Kirsch D.G., Clem R.J., Ravi R., Kastan M.B., Bedi A., Ueno K., Hardwick J.M. Conversion of Bcl-2 to a Bax-like death effector by caspases. Science. 278:1997;1966-1968.
10. Liang Y., Nylander K.D., Yan C., Schor N.F. Role of caspase 3-dependent Bcl-2 cleavage in potentiation of apoptosis by Bcl-2. Mol. Pharmacol. 61:2002;142-149.
11. Boise L.H., Gonzalez-Garcia M., Postema C.E., Ding L., Lindsten T., Turka L.A., Mao X., Nunez G., Thompson C.B. Bcl-x, a Bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell. 74:1993;597-608.
12. Clem R.J., Cheng E.H., Karp C.L., Kirsch D.G., Ueno K., Takahashi A., Kastan M.B., Griffin D.E., Earnshaw W.C., Veliuona M.A., Hardwick J.M. Modulation of cell death by Bcl-XL through caspase interaction. Proc. Natl. Acad. Sci. USA. 95:1998;554-559.
13. Antonsson B., Montessuit S., Lauper S., Eskes R., Martinou J.C. Bax oligomerization is required for channel-forming activity in liposomes and to trigger cytochrome c release from mitochondria. Biochem. J. 345:2000;271-278.
14. Antonsson B., Montessuit S., Sanchez B., Martinou J.C. Bax is present as a high molecular weight oligomer/complex in the mitochondrial membrane of apoptotic cells. J. Biol. Chem. 276:2001;11615-11623.
15. Hanada M., Aimé-Sempe C., Sato T., Reed J.C. Structure-function analysis of Bcl-2 protein. Identification of conserved domains important for homodimerization with Bcl-2 and heterodimerization with Bax. J. Biol. Chem. 270:1995;11962-11969.
16. Frohlich K.U., Madeo F. Apoptosis in yeast: a monocellular organism exhibits altruistic behaviour. FEBS Lett. 473:2000;6-9.
17. Costa V., Moradas-Ferreira P. Oxidative stress and signal transduction in Saccharomyces cerevisiae: insights into ageing, apoptosis and diseases. Mol. Aspects Med. 22:2001;217-246.
18. Madeo F., Engelhardt S., Herker E., Lehmann N., Maldener C., Proksch A., Wissing S., Frohlich K.U. Apoptosis in yeast: a new model system with applications in cell biology and medicine. Curr. Genet. 41:2002;208-216.
19. Ameisen J.C. On the origin, evolution, and nature of programmed cell death: a timeline of four billion years. Cell Death Differ. 9:2002;367-393.
20. Zha H., Fisk H.A., Yaffe M.P., Mahajan M., Herman B., Reed J.C. Structure-function comparisons of the proapoptotic protein Bax in yeast and mammalian cells. Mol. Cell. Biol. 16:1996;6494-6508.
21. Greenhalf W., Stephan C., Chaudhuri B. Role of mitochondria and C-terminal membrane anchor of Bcl-2 in Bax-induced growth arrest and mortality in Saccharomyces cerevisiae. FEBS Lett. 380:1996;169-175.
22. Manon S., Chaudhuri B., Guérin M. Release of cytochrome c and decrease of cytochrome c oxidase in Bax-expressing yeast cells, and prevention of these effects by coexpression of Bcl-xL. FEBS Lett. 415:1997;29-32.
23. Yang J., Liu X., Bhalla K., Kim C.N., Ibrado A.M., Cai J., Peng T.I., Jones D.P., Wang X. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science. 275:1997;1129-1132.
24. Kluck R.M., Bossy-Wetzel E., Green D.R., Newmeyer D.D. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science. 275:1997;1132-1136.
25. Matsuyama S., Nouraini S., Reed J.C. Yeast as a tool for apoptosis research. Curr. Opin. Microbiol. 2:1999;618-623.
26. Wolter K.G., Hsu Y.T., Smith C.L., Nechushtan A., Xi X.G., Youle R.J. Movement of Bax from the cytosol to mitochondria during apoptosis. J. Cell Biol. 139:1997;1281-1292.
27. Tremblais K., Oliver L., Juin P., Le Cabellec M.T., Grégoire M., Meflah K., Vallette F.M. The C-terminus of Bax is not a membrane addressing/anchoring signal. Biochem. Biophys. Res. Commun. 260:1999;582-591.
28. Nguyen M., Millar D.G., Yong V.W., Korsmeyer S.J., Shore G.C. Targeting of Bcl-2 to the mitochondrial outer membrane by a COOH-terminal signal anchor sequence. J. Biol. Chem. 268:1993;25265-25268.
29. Janiak F., Leber B., Andrews D.W. Assembly of Bcl-2 into microsomal and outer mitochondrial membranes. J. Biol. Chem. 269:1994;9842-9849.
30. Martinez-Senac M.D.M., Corbalan-Garcia S., Gomez-Fernandez J.C. Conformation of the C-terminal domain of the pro-apoptotic protein Bax and mutants and its interaction with membranes. Biochemistry. 40:2001;9983-9992.
31. Priault, M., Cartron, P.F., Camougrand, N., Antonsson, B., Vallette, F.M. and Manon, D. (2003) Investigation of the role of C-terminus of Bax and of tc-Bid on Bax-interaction with yeast mitochondria. Cell Death Differ. (in press).
32. Clow A., Greenhalf W., Chaudhuri B. Under respiratory growth conditions, Bcl-x(L) and Bcl-2 are unable to overcome yeast cell death triggered by a mutant Bax protein lacking the membrane anchor. Eur. J. Biochem. 258:1998;19-28.
33. Priault M., Camougrand N., Chaudhuri B., Manon S. Role of the C-terminal domain of Bax and Bcl-XL in their localization and function in yeast cells. FEBS Lett. 443:1999;225-228.
34. Susin S.A., Zamzami N., Castedo M., Hirsch T., Marchetti P., Macho A., Daugas E., Geuskens M., Kroemer G. Bcl-2 inhibits the mitochondrial release of an apoptogenic protease. J. Exp. Med. 184:1996;1331-1341.
35. Du C., Fang M., Li Y., Li L., Wang X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell. 102:2000;33-42.
36. Verhagen A.M., Ekert P.G., Pakusch M., Silke J., Connolly L.M., Reid G.E., Moritz R.L., Simpson R.J., Vaux D.L. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell. 102:2000;43-53.
37. Li L.Y., Luo X., Wang X. Endonuclease G is an apoptotic DNase when released from mitochondria. Nature. 412:2001;95-99.
38. Li P., Nijhawan D., Budihardjo I., Srinivasula S.M., Ahmad M., Alnemri E.S., Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell. 91:1997;479-489.
39. Daugas E., Susin S.A., Zamzami N., Ferri K.F., Irinopolou T., Larochette N., Prevost M.C., Leber B., Andrews D., Penninger J., Kroemer G. Mitochondrio-nuclear translocation of AIF in apoptosis and necrosis. FASEB J. 14:2000;729-739.
40. Bernardi P. Mitochondrial transport of cations: channels, exchangers and permeability transition. Physiol. Rev. 79:1999;1127-1155.
41. Bernardi P., Scorrano L., Colonna R., Petronilli V., Di Lisa F. Mitochondria and cell death. Mechanistic aspects and methodological issues. Eur. J. Biochem. 264:1999;687-701.
42. Petronilli V., Nicolli A., Costantini P., Colonna R., Bernardi P. Regulation of the permeability transition pore, a voltage-dependent mitochondrial channel inhibited by cyclosporin A. Biochim. Biophys. Acta. 1187:1994;255-259.
43. Costantini P., Chernyak B.V., Petronilli V., Bernardi P. Modulation of the mitochondrial permeability transition pore by pyridine nucleotides and dithiol oxidation at two separate sites. J. Biol. Chem. 271:1996;6476-6751.
44. Scorrano L., Petronilli V., Bernardi P. On the voltage dependence of the mitochondrial permeability transition pore: a critical appraisal. J. Biol. Chem. 272:1997;12295-12299.
45. Beutner G., Ruck A., Riede B., Brdiczka D. Complexes between porin, hexokinase, mitochondrial creatine kinase and adenylate translocator display properties of the permeability transition pore. Implication for regulation of permeability transition by the kinases. Biochim. Biophys. Acta. 1368:1998;7-18.
46. Zamzami N., Susin S.A., Marchetti P., Hirsch T., Gomez-Monterrey I., Castedo M., Kroemer G. Mitochondrial control of nuclear apoptosis. J. Exp. Med. 183:1996;1533-1544.
47. Zamzami N., Marchetti P., Castedo M., Hirsch T., Susin S.A., Masse B., Kroemer G. Inhibitors of permeability transition interfere with the disruption of the mitochondrial transmembrane potential during apoptosis. FEBS Lett. 384:1996;53-57.
48. Marzo I., Brenner C., Zamzami N., Jurgensmeier J.M., Susin S.A., Vieira H.L., Prevost M.C., Xie Z., Matsuyama S., Reed J.C., Kroemer G. Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science. 281:1998;2027-2031.
49. Zamzami N., Marzo I., Susin S.A., Brenner C., Larochette N., Marchetti P., Reed J.C., Kofler R., Kroemer G. The thiol crosslinking agent diamide overcomes the apoptosis-inhibitory effect of Bcl-2 by enforcing mitochondrial permeability transition. Oncogene. 16:1998;1055-1063.
50. Vancompernolle K., Van Herreweghe F., Pynaert G., Van de Craen M., De Vos K., Totty N., Sterling A., Fiers W., Vandenabeele P., Grooten J. Atractyloside-induced release of cathepsin B, a protease with caspase-processing activity. FEBS Lett. 438:1998;150-158.
51. Guicciardi M.E., Deussing J., Miyoshi H., Bronk S.F., Svingen P.A., Peters C., Kaufmann S.H., Gores G.J. Cathepsin B contributes to TNF-alpha-mediated hepatocyte apoptosis by promoting mitochondrial release of cytochrome c. J. Clin. Invest. 107:2001;21-22.
52. Schotte P., Declercq W., Van Huffel S., Vandenabeele P., Beyaert R. Non-specific effects of methyl ketone peptide inhibitors of caspases. FEBS Lett. 442:1999;117-121.
53. Wigdal S.S., Kirkland R.A., Franklin J.L., Haak-Frendscho M. Cytochrome c release precedes mitochondrial membrane potential loss in cerebellar granule neuron apoptosis: lack of mitochondrial swelling. J. Neurochem. 82:2002;1029-1038.
54. Vander Heiden M.G., Chandel N.S., Williamson E.K., Schumacker P.T., Thompson C.B. Bcl-xL regulates the membrane potential and volume homeostasis of mitochondria. Cell. 91:1997;627-637.
55. 2+ ions. J. Cell Biol. 143:1998;217-224.
56. Kluck R.M., Esposti M.D., Perkins G., Renken C., Kuwana T., Bossy-Wetzel E., Goldberg M., Allen T., Barber M.J., Green D.R., Newmeyer D.D. The pro-apoptotic proteins, Bid and Bax, cause a limited permeabilization of the mitochondrial outer membrane that is enhanced by cytosol. J. Cell Biol. 147:1999;809-822.
57. Appaix F., Guerrero K., Rampal D., Izikki M., Kaambre T., Sikk P., Brdiczska D., Riva-Lavieille C., Olivares J., Longuet M., Antonsson B., Saks V.A. Bax and heart mitochondria: uncoupling and inhibition of respiration without permeability transition. Biochim. Biophys. Acta. 1556:2002;155-167.
58. Adrain C., Creagh E.M., Martin S.J. Apoptosis-associated release of Smac/DIABLO from mitochondria requires active caspases and is blocked by Bcl-2. EMBO J. 20:2001;6627-6636.
59. Arnoult D., Parone P., Martinou J.C., Antonsson B., Estaquier J., Ameisen J.C. Mitochondrial release of apoptosis-inducing factor occurs downstream of cytochrome c release in response to several proapoptotic stimuli. J. Cell Biol. 159:2002;923-929.
60. Priault M., Chaudhuri B., Clow A., Camougrand N., Manon S. Investigation of Bax-induced release of cytochrome c from yeast mitochondria permeability of mitochondrial membranes, role of VDAC and ATP requirement. Eur. J. Biochem. 260:1999;684-691.
61. Manon S., Priault M., Camougrand N. Mitochondrial AAA-type protease Yme1p is involved in Bax effects on cytochrome c oxidase. Biochem. Biophys. Res. Commun. 289:2001;1314-1319.
62. Jung D.W., Bradshaw P.C., Pfeiffer D.R. Properties of a cyclosporin-insensitive permeability transition pore in yeast mitochondria. J. Biol. Chem. 272:1997;21104-21112.
63. Manon S., Roucou X., Guérin M., Rigoulet M., Guérin B. Characterization of the yeast mitochondria unselective channel: a counterpart to the mammalian permeability transition pore? J. Bioenerg. Biomembr. 30:1998;419-429.
64. Priault M., Camougrand N., Chaudhuri B., Schaeffer J., Manon S. Comparison of the effects of Bax-expression in yeast under fermentative and respiratory conditions: investigation of the role of adenine nucleotides carrier and cytochrome c. FEBS Lett. 456:1999;232-238.
65. L. Mol. Cell. Biol. 20:2000;3125-3136.
66. Kissova I., Polcic P., Kempna P., Zeman I., Sabova L., Kolarov J. The cytotoxic action of Bax on yeast cells does not require mitochondrial ADP/ATP carrier but may be related to its import to the mitochondria. FEBS Lett. 471:2000;113-118.
67. Shimizu S., Narita M., Tsujimoto Y. Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature. 399:2000;483-487.
68. Antonsson B., Conti F., Ciavatta A., Montessuit S., Lewis S., Martinou I., Bernasconi L., Bernard A., Mermod J.J., Mazzei G., Maundrell K., Gambale F., Sadoul R., Martinou J.C. Inhibition of Bax channel-forming activity by Bcl-2. Science. 277:1997;370-372.
69. Schlesinger P.H., Gross A., Yin X.M., Yamamoto K., Saito M., Waksman G., Korsmeyer S.J. Comparison of the ion channel characteristics of proapoptotic BAX and antiapoptotic BCL-2. Proc. Natl. Acad. Sci. USA. 94:1997;11357-11362.
70. Pavlov E.V., Priault M., Pietkiewicz D., Cheng E.H., Antonsson B., Manon S., Korsmeyer S.J., Mannella C.A., Kinnally K.W. A novel, high-conductance channel of mitochondria linked to apoptosis in mammalian cells and Bax expression in yeast. J. Cell Biol. 155:2001;725-731.
71. Roucou X., Prescott M., Devenish R.J., Nagley P. A cytochrome c-GFP fusion is not released from mitochondria into the cytoplasm upon expression of Bax in yeast cells. FEBS Lett. 471:2000;235-239.
72. Lassus P., Opitz-Araya X., Lazebnik Y. Requirement for caspase-2 in stress-induced apoptosis before mitochondrial permeabilization. Science. 297:2002;1352-1354.
73. L does not affect its subcellular localization but abrogates its pro-apoptotic properties. FEBS Lett. 487:2000;161-165.
74. Scorrano L., Ashiya M., Buttle K., Weiler S., Oakes S.A., Mannella C.A., Korsmeyer S.J. A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev. Cell. 2:2002;55-67.
75. L independently regulate apoptotic changes of yeast mitochondria that require VDAC but not adenine nucleotide translocator. Oncogene. 19:2000;4309-4318.
76. Paumard P., Vaillier J., Coulary B., Schaeffer J., Soubannier V., Mueller D.M., Brethes D., Di Rago J.P., Velours J. The ATP synthase is involved in generating mitochondrial cristae morphology. EMBO J. 21:2002;221-230.
77. Nechushtan A., Smith C.L., Hsu Y.T., Youle R.J. Conformation of the Bax C-terminus regulates subcellular location and cell death. EMBO J. 18:1999;2330-2341.
78. Goping I.S., Gross A., Lavoie J.N., Nguyen M., Jemmerson R., Roth K., Korsmeyer S.J., Shore G.C. Regulated targeting of BAX to mitochondria. J. Cell Biol. 143:1998;207-215.
79. Cartron P.F., Priault M., Oliver L., Meflah K., Manon S., Vallette F.M. The N-terminal end of Bax contains a mitochondrial-targeting signal. J. Biol. Chem. 278:2003;11633-11641.
80. Cartron P.F., Moreau C., Oliver L., Mayat E., Meflah K., Vallette F.M. Involvement of the N-terminus of Bax in its intracellular localization and function. FEBS Lett. 512:2002;95-100.
81. L and pro-apoptotic activity. J. Biol. Chem. 272:1997;24101-24104.
82. L proteins. J. Biol. Chem. 272:1997;30866-30972.
83. Li H., Zhu H., Xu C.J., Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell. 94:1998;491-501.
84. Lutter M., Fang M., Luo X., Nishijima M., Xie X., Wang X. Cardiolipin provides specificity for targeting of tBid to mitochondria. Nat. Cell Biol. 2:2002;754-761.
85. Eskes R., Desagher S., Antonsson B., Martinou J.C. Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane. Mol. Cell. Biol. 20:2000;929-935.
86. Roucou X., Rostovtseva T., Montessuit S., Martinou J.C., Antonsson B. Bid induces cytochrome c-impermeable Bax channels in liposomes. Biochem. J. 363:2002;547-552.
87. Wei M.C., Lindsten T., Mootha V.K., Weiler S., Gross A., Ashiya M., Thompson C.B., Korsmeyer S.J. tBid, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev. 14:2000;2060-2071.
88. Kuwana T., Mackey M.R., Perkins G., Ellisman M.H., Latterich M., Schneiter R., Green D.R., Newmeyer D.D. Bid, Bax and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell. 111:2002;331-342.
89. Madeo F., Frohlich E., Ligr M., Grey M., Sigrist S.J., Wolf D.H., Frohlich K.U. Oxygen stress: a regulator of apoptosis in yeast. J. Cell Biol. 145:1999;757-767.
90. Priault M., Bessoule J.J., Grelaud-Coq A., Camougrand N., Manon S. Bax-induced cell death in yeast depends on mitochondrial lipid oxidation. Eur. J. Biochem. 269:2002;5440-5450.
91. Ligr M., Madeo F., Frohlich E., Hilt W., Frohlich K.U., Wolf D.H. Mammalian Bax triggers apoptotic changes in yeast. FEBS Lett. 438:1998;61-65.
92. Marza E., Camougrand N., Manon S. Bax expression protects yeast plasma membrane against ethanol-induced permeabilization. FEBS Lett. 521:2002;47-52.
93. Nuñez G., Benedict M.A., Hu Y., Inohara N. Caspases: the proteases of the apoptotic pathway. Oncogene. 17:1998;3237-3245.
94. Stennicke H.R., Salvesen G.S. Catalytic properties of the caspases. Cell Death Differ. 6:1999;1054-1059.
95. Madeo F., Herker E., Maldener C., Wissing S., Lachelt S., Herlan M., Fehr M., Lauber K., Sigrist S.J., Wesselborg S., Frohlich K.U. A caspase-related protease regulates apoptosis in yeast. Mol. Cell. 9:2002;911-917.
96. Ligr M., Velten I., Frohlich E., Madeo F., Ledig M., Frohlich K.U., Wolf D.H., Hilt W. The proteasomal substrate Stm1 participates in apoptosis-like cell death in yeast. Mol. Biol. Cell. 12:2001;2422-2432.
97. Ludovico P., Rodrigues F., Almeida A., Silva M.T., Barrientos A., Côrte-Real M. Cytochrome c release and mitochondria involvement in programmed cell death induced by acetic acid in Saccharomyces cerevisiae. Mol. Biol. Cell. 13:2002;2598-2606.
98. Abeliovich H., Klionsky D.J. Autophagy in yeast: mechanistic insights and physiological function. Microbiol. Mol. Biol. Rev. 65:2001;463-479.
99. Beck T., Hall M.N. The TOR signalling pathway controls nuclear localization of nutrient-regulated transcription factors. Nature. 402:1999;689-692.
100. George M.D., Baba M., Scott S.V., Mizushima M., Garrisson B.S., Ohsumi Y., Kionsky D.J. Apg5p functions in the sequestration steps in the cytoplasm-to-vacuole targeting and macroautophagy pathways. Mol. Biol. Cell. 11:2000;969-982.
101. Hammond E.M., Brunet C.L., Johnson G.D., Parkhill J., Milner A.E., Brady G., Gregory C.D., Grand R.J. Homology between a human apoptosis-specific protein and the product of APG5, a gene involved in autophagy in yeast. FEBS Lett. 425:1998;391-395.
102. Liang X.H., Jackson S., Seaman M., Brown K., Kempkes B., Hibshoosh H., Levine B. Induction of autophagy and inhibition of tumorigenesis by beclin-1. Nature. 402:1999;672-676.
103. Xue L., Fletcher G.C., Tolkovsky A.M. Autophagy is activated by apoptotic signalling in sympathetic neurons: an alternative mechanism of death execution. Mol. Cell. Neurosci. 14:1999;180-198.
104. Petiot A., Ogier-Denis E., Blommaart F., Meijer A.J., Codogno P. Distinct classes of phosphatidylinositol 3′-kinases are involved in signalling pathways that control macroautophagy in HT-29 cells. J. Biol. Chem. 275:2000;992-998.
105. Abudugupur A., Mitsui K., Yokota S., Tsurugi K. An ARL1 mutation affected autophagic cell death in yeast, causing a defect in central vacuole formation. Cell Death Differ. 9:2002;158-168.
106. Camougrand N., Grelaud-Coq A., Marza E., Priault M., Bessoule J.J., Manon S. The product of the UTH1 gene, required for Bax-induced cell death in yeast, is involved in the response to rapamycin. Mol. Microbiol. 47:2003;495-506.
107. Bandara P.D., Flattery-O'Brien J.A., Grant C.M., Dawes I.W. Involvement of the Saccharomyces cerevisiae UTH1 gene in the oxidative-stress response. Curr. Genet. 34:1998;259-268.
108. Camougrand N., Mouassite M., Velours G., Guérin M. The 'SUN' family: UTH1, an ageing gene, is also involved in the regulation of mitochondria biogenesis in Saccharomyces cerevisiae. Arch. Biochem. Biophys. 375:2000;154-160.
109. Mouassite M., Guérin M., Camougrand N. The SUN family of Saccharomyces cerevisiae: the double knock-out of UTH1 and SIM1 promotes defects in nucleus migration and increased drug sensitivity. FEMS Microbiol. Lett. 182:2000;137-141.
110. Camougrand N., Rigoulet M. Studies of some genes involved both in aging and in response to oxidative stress. Respir. Physiol. 128:2001;393-401.
111. Velours G., Boucheron C., Manon S., Camougrand N. Dual cell wall/mitochondria localization of the 'SUN' family proteins. FEMS Microbiol. Lett. 207:2002;165-172.
112. Longo V.D., Ellerby L.M., Bredesen D.E., Valentine J.S., Gralla E.B. Human Bcl-2 reverses survival defects in yeast lacking superoxide dismutase and delays death of wild-type yeast. J. Cell Biol. 137:1997;1581-1588.
113. Greenhalf W., Lee J., Chaudhuri B. A selection system for human apoptosis inhibitors using yeast. Yeast. 15:1999;1307-1321.
114. Xu Q., Reed J.C. Bax inhibitor-1, a mammalian apoptosis suppressor identified by functional screening in yeast. Mol. Cell. 1:1998;337-346.
115. Laun P., Pichova A., Madeo F., Fuchs J., Ellinger A., Kohlwein S., Dawes I., Frohlich K.U., Breitenbach M. Aged mother cells of Saccharomyces cerevisiae show markers of oxidative stress and apoptosis. Mol. Microbiol. 39:2001;1166-1173.