Calnexin regulates apoptosis induced by inositol starvation in fission yeast

PLoS ONE

Volumn 4, Issue 7, 2009, Pages

  Guérlin, Renée ^a   Beauregard, Pascale B ^a   Leroux, Alexandre ^a   Rokeach, Luis A ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALNEXIN; FUNGAL PROTEIN; INOSITOL; METACASPASE PCA1P PROTEIN; PROTEIN IRE1P; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL DEATH; CELL LEVEL; CONTROLLED STUDY; FUNGUS GROWTH; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SCHIZOSACCHAROMYCES POMBE; SIGNAL TRANSDUCTION; STARVATION; YEAST CELL; AMINO ACID SEQUENCE; CHEMISTRY; CYTOLOGY; GEL CHROMATOGRAPHY; GENETICS; HYDROLYSIS; MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; MUTATION; PHYSIOLOGY; SCHIZOSACCHAROMYCES;

SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

AMINO ACID SEQUENCE; APOPTOSIS; CALNEXIN; CHROMATOGRAPHY, GEL; HYDROLYSIS; INOSITOL; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; MUTATION; SCHIZOSACCHAROMYCES;

EID: 67650904442     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0006244     Document Type: Article

References (130)

1. Bukau B, Deuerling E, Pfund C, Craig EA (2000) Getting newly synthesized proteins into shape. Cell 101: 119-122.
2. Fewell SW, Travers KJ, Weissman JS, Brodsky JL (2001) The action of molecular chaperones in the early secretory pathway. Annu Rev Genet 35: 149-191.
3. Trombetta ES, Parodi AJ (2003) Quality control and protein folding in the secretory pathway. Annu Rev Cell Dev Biol 19: 649-676.
4. Lai E, Teodoro T, Volchuk A (2007) Endoplasmic reticulum stress: signaling the unfolded protein response. Physiology (Bethesda) 22: 193-201.
5. Boyce M, Yuan J (2006) Cellular response to endoplasmic reticulum stress: a matter of life or death. Cell Death Differ 13: 363-373.
6. Breckenridge DG, Germain M, Mathai JP, Nguyen M, Shore GC (2003) Regulation of apoptosis by endoplasmic reticulum pathways. Oncogene 22: 8608-8618.
7. Szegezdi E, Logue SE, Gorman AM, Samali A (2006) Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep 7: 880-885.
8. Ron D, Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8: 519-529.
9. Patil C, Walter P (2001) Intracellular signaling from the endoplasmic reticulum to the nucleus: the unfolded protein response in yeast and mammals. Curr Opin Cell Biol 13: 349-355.
10. Schroder M, Kaufman RJ (2005) ER stress and the unfolded protein response. Mutat Res 569: 29-63.
11. Wu J, Kaufman RJ (2006) From acute ER stress to physiological roles of the Unfolded Protein Response. Cell Death Differ 13: 374-384.
12. Ahner A, Brodsky JL (2004) Checkpoints in ER-associated degradation: excuse me, which way to the proteasome? Trends Cell Biol 14: 474-478.
13. Meusser B, Hirsch C, Jarosch E, Sommer T (2005) ERAD: the long road to destruction. Nat Cell Biol 7: 766-772.
14. Marciniak SJ, Ron D (2006) Endoplasmic reticulum stress signaling in disease. Physiol Rev 86: 1133-1149.
15. Schroder M, Kaufman RJ (2005) The mammalian unfolded protein response. Annu Rev Biochem 74: 739-789.
16. Xu C, Bailly-Maitre B, Reed JC (2005) Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest 115: 2656-2664.
17. Kerr JF (2002) History of the events leading to the formulation of the apoptosis concept. Toxicology 181-182: 471-474.
18. Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26: 239-257.
19. Severin FF, Meer MV, Smirnova EA, Knorre DA, Skulachev VP (2008) Natural causes of programmed death of yeast Saccharomyces cerevisiae. Biochim Biophys Acta 1783: 1350-1353.
20. Hamann A, Brust D, Osiewacz HD (2008) Apoptosis pathways in fungal growth, development and ageing. Trends Microbiol 16: 276-283.
21. Frohlich KU, Fussi H, Ruckenstuhl C (2007) Yeast apoptosis-from genes to pathways. Semin Cancer Biol 17: 112-121.
22. Roux AE, Quissac A, Chartrand P, Ferbeyre G, Rokeach LA (2006) Regulation of chronological aging in Schizosaccharomyces pombe by the protein kinases Pka1 and Sck2. Aging Cell 5: 345-357.
23. Wissing S, Ludovico P, Herker E, Buttner S, Engelhardt SM, et al. (2004) An AIF orthologue regulates apoptosis in yeast. J Cell Biol 166: 969-974.
24. Walter D, Wissing S, Madeo F, Fahrenkrog B (2006) The inhibitor-of-apoptosis protein Bir1p protects against apoptosis in S. cerevisiae and is a substrate for the yeast homologue of Omi/HtrA2. J Cell Sci 119: 1843-1851.
25. Jin C, Reed JC (2002) Yeast and apoptosis. Nat Rev Mol Cell Biol 3: 453-459.
26. Fahrenkrog B, Sauder U, Aebi U (2004) The S. cerevisiae HtrA-like protein Nma111p is a nuclear serine protease that mediates yeast apoptosis. J Cell Sci 117: 115-126.
27. Burhans WC, Weinberger M (2007) Yeast endonuclease G: complex matters of death, and of life. Mol Cell 25: 323-325.
28. Madeo F, Herker E, Maldener C, Wissing S, Lachelt S, et al. (2002) A caspase-related protease regulates apoptosis in yeast. Mol Cell 9: 911-917.
29. De Camilli P, Emr SD, McPherson PS, Novick P (1996) Phosphoinositides as regulators in membrane traffic. Science 271: 1533-1539.
30. Majerus PW, Connolly TM, Deckmyn H, Ross TS, Bross TE, et al. (1986) The metabolism of phosphoinositide-derived messenger molecules. Science 234: 1519-1526.
31. Steiner S, Lester RL (1972) Studies on the diversity of inositol-containing yeast phospholipids: incorporation of 2-deoxyglucose into lipid. J Bacteriol 109: 81-88.
32. Berridge MJ (1987) Inositol trisphosphate and diacylglycerol: two interacting second messengers. Annu Rev Biochem 56: 159-193.
33. Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4: 517-529.
34. Belde PJ, Vossen JH, Borst-Pauwels GW, Theuvenet AP (1993) Inositol 1,4,5-trisphosphate releases Ca2+ from vacuolar membrane vesicles of Saccharomyces cerevisiae. FEBS Lett 323: 113-118.
35. Donahue TF, Henry SA (1981) myo-Inositol-1-phosphate synthase. Characteristics of the enzyme and identification of its structural gene in yeast. J Biol Chem 256: 7077-7085.
36. Eisenberg F, Bolden AH, Loewus FA (1964) Inositol formation by cyclization of glucose chain in rat testis. Biochem Biophys Res Commun 14: 419-424.
37. Klig LS, Antonsson B, Schmid E, Friedli L (1991) Inositol biosynthesis: Candida albicans and Saccharomyces cerevisiae genes share common regulation. Yeast 7: 325-336.
38. Klig LS, Henry SA (1984) Isolation of the yeast INO1 gene: located on an autonomously replicating plasmid, the gene is fully regulated. Proc Natl Acad Sci U S A 81: 3816-3820.
39. Majumder AL, Johnson MD, Henry SA (1997) 1L-myo-inositol-1-phosphate synthase. Biochim Biophys Acta 1348: 245-256.
40. Dean-Johnson M, Henry SA (1989) Biosynthesis of inositol in yeast. Primary structure of myo-inositol-1-phosphate synthase (EC 5.5.1.4) and functional analysis of its structural gene, the INO1 locus. J Biol Chem 264: 1274-1283.
41. Greenberg ML, Lopes JM (1996) Genetic regulation of phospholipid biosynthesis in Saccharomyces cerevisiae. Microbiol Rev 60: 1-20.
42. Chang HJ, Jones EW, Henry SA (2002) Role of the unfolded protein response pathway in regulation of INO1 and in the sec14 bypass mechanism in Saccharomyces cerevisiae. Genetics 162: 29-43.
43. Cox JS, Chapman RE, Walter P (1997) The unfolded protein response coordinates the production of endoplasmic reticulum protein and endoplasmic reticulum membrane. Mol Biol Cell 8: 1805-1814.
44. MacNeill SA (2002) Genome sequencing: and then there were six. Curr Biol 12: R294-296.
45. Yarbrough HF Jr, Clark FM (1957) Utilization of inositol, an essential metabolite for Schizosaccharomyces pombe. J Bacteriol 73: 318-323.
46. Niederberger C, Graub R, Schweingruber AM, Fankhauser H, Rusu M, et al. (1998) Exogenous inositol and genes responsible for inositol transport are required for mating and sporulation in Shizosaccharomyces pombe. Curr Genet 33: 255-261.
47. Poitelea M, Rusu M (1997) [Inositol is necessary to sexual differentiation in Schizosaccharomyces pombe]. Rev Med Chir Soc Med Nat Iasi 101: 87-91.
48. Voicu PM, Poitelea M, Schweingruber E, Rusu M (2002) Inositol is specifically involved in the sexual program of the fission yeast Schizosaccharomyces pombe. Arch Microbiol 177: 251-258.
49. Fernandez S, Homann MJ, Henry SA, Carman GM (1986) Metabolism of the phospholipid precursor inositol and its relationship to growth and viability in the natural auxotroph Schizosaccharomyces pombe. J Bacteriol 166: 779-786.
50. Minskoff SA, Gaynor PM, Greenberg ML (1992) Mutant enrichment of Schizosaccharomyces pombe by inositol-less death. J Bacteriol 174: 4078-4085.
51. Ingavale SS, Bachhawat AK (1999) Restoration of inositol prototrophy in the fission yeast Schizosaccharomyces pombe. Microbiology 145 (Pt 8): 1903-1910.
52. Williams DB (2006) Beyond lectins: the calnexin/calreticulin chaperone system of the endoplasmic reticulum. J Cell Sci 119: 615-623.
53. Arunachalam B, Cresswell P (1995) Molecular requirements for the interaction of class II major histocompatibility complex molecules and invariant chain with calnexin. J Biol Chem 270: 2784-2790.
54. Beaulieu H, Elagoz A, Crine P, Rokeach LA (1999) Interaction of mammalian neprilysin with binding protein and calnexin in Schizosaccharomyces pombe. Biochem J 340 (Pt 3): 813-819.
55. Fernandez F, Jannatipour M, Hellman U, Rokeach LA, Parodi AJ (1996) A new stress protein: synthesis of Schizosaccharomyces pombe UDP-Glc:glycoprotein glucosyltransferase mRNA is induced by stress conditions but the enzyme is not essential for cell viability. Embo J 15: 705-713.
56. Hebert DN, Garman SC, Molinari M (2005) The glycan code of the endoplasmic reticulum: asparagine-linked carbohydrates as protein maturation and quality-control tags. Trends Cell Biol 15: 364-370.
57. Jannatipour M, Rokeach LA (1998) A Schizosaccharomyces pombe gene encoding a novel polypeptide with a predicted alpha-helical rod structure found in the myosin and intermediate-filament families of proteins. Biochim Biophys Acta 1399: 67-72.
58. Marechal A, Tanguay PL, Callejo M, Guerin R, Boileau G, et al. (2004) Cell viability and secretion of active proteins in Schizosaccharomyces pombe do not require the chaperone function of calnexin. Biochem J 380: 441-448.
59. Parodi AJ (2000) Protein glucosylation and its role in protein folding. Annu Rev Biochem 69: 69-93.
60. Saito Y, Ihara Y, Leach MR, Cohen-Doyle MF, Williams DB (1999) Calreticulin functions in vitro as a molecular chaperone for both glycosylated and non-glycosylated proteins. Embo J 18: 6718-6729.
61. Thammavongsa V, Mancino L, Raghavan M (2005) Polypeptide substrate recognition by calnexin requires specific conformations of the calnexin protein. J Biol Chem 280: 33497-33505.
62. Denzel A, Molinari M, Trigueros C, Martin JE, Velmurgan S, et al. (2002) Early postnatal death and motor disorders in mice congenitally deficient in calnexin expression. Mol Cell Biol 22: 7398-7404.
63. Jannatipour M, Rokeach LA (1995) The Schizosaccharomyces pombe homologue of the chaperone calnexin is essential for viability. J Biol Chem 270: 4845-4853.
64. Parlati F, Dignard D, Bergeron JJ, Thomas DY (1995) The calnexin homologue cnx1+ in Schizosaccharomyces pombe, is an essential gene which can be complemented by its soluble ER domain. EMBO J 14: 3064-3072.
65. Elagoz A, Callejo M, Armstrong J, Rokeach LA (1999) Although calnexin is essential in S. pombe, its highly conserved central domain is dispensable for viability. J Cell Sci 112 (Pt 23): 4449-4460.
66. Hajjar F, Beauregard PB, Rokeach LA (2007) The 160 N-terminal residues of calnexin define a novel region supporting viability in Schizosaccharomyces pombe. Yeast 24: 89-103.
67. Torgler CN, de Tiani M, Raven T, Aubry JP, Brown R, et al. (1997) Expression of bak in S. pombe results in a lethality mediated through interaction with the calnexin homologue Cnx1. Cell Death Differ 4: 263-271.
68. Groenendyk J, Zuppini A, Shore G, Opas M, Bleackley RC, et al. (2006) Caspase 12 in calnexin-deficient cells. Biochemistry 45: 13219-13226.
69. Zuppini A, Groenendyk J, Cormack LA, Shore G, Opas M, et al. (2002) Calnexin deficiency and endoplasmic reticulum stress-induced apoptosis. Biochemistry 41: 2850-2858.
70. Delom F, Emadali A, Cocolakis E, Lebrun JJ, Nantel A, et al. (2006) Calnexin-dependent regulation of tunicamycin-induced apoptosis in breast carcinoma MCF-7 cells. Cell Death Differ.
71. Takizawa T, Tatematsu C, Watanabe K, Kato K, Nakanishi Y (2004) Cleavage of calnexin caused by apoptotic stimuli: implication for the regulation of apoptosis. J Biochem (Tokyo) 136: 399-405.
72. Guerin R, Arseneault G, Dumont S, Rokeach LA (2008) Calnexin is involved in apoptosis induced by endoplasmic reticulum stress in the fission yeast. Mol Biol Cell 19: 4404-4420.
73. Lim HW, Kim SJ, Park EH, Lim CJ (2007) Overexpression of a metacaspase gene stimulates cell growth and stress response in Schizosaccharomyces pombe. Can J Microbiol 53: 1016-1023.
74. Uren AG, O'Rourke K, Aravind LA, Pisabarro MT, Seshagiri S, et al. (2000) Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol Cell 6: 961-967.
75. Elorza MV, Rico H, Sentandreu R (1983) Calcofluor white alters the assembly of chitin fibrils in Saccharomyces cerevisiae and Candida albicans cells. J Gen Microbiol 129: 1577-1582.
76. Shahinian S, Dijkgraaf GJ, Sdicu AM, Thomas DY, Jakob CA, et al. (1998) Involvement of protein N-glycosyl chain glucosylation and processing in the biosynthesis of cell wall beta-1,6-glucan of Saccharomyces cerevisiae. Genetics 149: 843-856.
77. Turcotte C, Roux A, Beauregard PB, Guerin R, Senechal P, et al. (2007) The calnexin-independent state does not compensate for all calnexin functions in Schizosaccharomyces pombe. FEMS Yeast Res 7: 196-208.
78. Buttner S, Eisenberg T, Herker E, Carmona-Gutierrez D, Kroemer G, et al. (2006) Why yeast cells can undergo apoptosis: death in times of peace, love, and war. J Cell Biol 175: 521-525.
79. Knorre DA, Smirnova EA, Severin FF (2005) Natural conditions inducing programmed cell death in the yeast Saccharomyces cerevisiae. Biochemistry (Mosc) 70: 264-266.
80. Balzan R, Sapienza K, Galea DR, Vassallo N, Frey H, et al. (2004) Aspirin commits yeast cells to apoptosis depending on carbon source. Microbiology 150: 109-115.
81. King DA, Hannum DM, Qi JS, Hurst JK (2004) HOCl-mediated cell death and metabolic dysfunction in the yeast Saccharomyces cerevisiae. Arch Biochem Biophys 423: 170-181.
82. Silva RD, Sotoca R, Johansson B, Ludovico P, Sansonetty F, et al. (2005) Hyperosmotic stress induces metacaspase- and mitochondria-dependent apoptosis in Saccharomyces cerevisiae. Mol Microbiol 58: 824-834.
83. Madeo F, Frohlich E, Ligr M, Grey M, Sigrist SJ, et al. (1999) Oxygen stress: a regulator of apoptosis in yeast. J Cell Biol 145: 757-767.
84. Pozniakovsky AI, Knorre DA, Markova OV, Hyman AA, Skulachev VP, et al. (2005) Role of mitochondria in the pheromone- and amiodarone-induced programmed death of yeast. J Cell Biol 168: 257-269.
85. Ludovico P, Sousa MJ, Silva MT, Leao C, Corte-Real M (2001) Saccharomyces cerevisiae commits to a programmed cell death process in response to acetic acid. Microbiology 147: 2409-2415.
86. Huh GH, Damsz B, Matsumoto TK, Reddy MP, Rus AM, et al. (2002) Salt causes ion disequilibrium-induced programmed cell death in yeast and plants. Plant J 29: 649-659.
87. Granot D, Levine A, Dor-Hefetz E (2003) Sugar-induced apoptosis in yeast cells. FEMS Yeast Res 4: 7-13.
88. Mitsui K, Nakagawa D, Nakamura M, Okamoto T, Tsurugi K (2005) Valproic acid induces apoptosis dependent of Yca1p at concentrations that mildly affect the proliferation of yeast. FEBS Lett 579: 723-727.
89. Harada H, Grant S (2003) Apoptosis regulators. Rev Clin Exp Hematol 7: 117-138.
90. Chowdhury I, Tharakan B, Bhat GK (2006) Current concepts in apoptosis: the physiological suicide program revisited. Cell Mol Biol Lett 11: 506-525.
91. Carmody RJ, Cotter TG (2001) Signalling apoptosis: a radical approach. Redox Rep 6: 77-90.
92. Delom F, Fessart D, Chevet E (2007) Regulation of calnexin sub-cellular localization modulates endoplasmic reticulum stress-induced apoptosis in MCF-7 cells. Apoptosis.
93. Chang Q, Petrash JM (2008) Disruption of aldo-keto reductase genes leads to elevated markers of oxidative stress and inositol auxotrophy in Saccharomyces cerevisiae. Biochim Biophys Acta 1783: 237-245.
94. Hirsch JP, Henry SA (1986) Expression of the Saccharomyces cerevisiae inositol-1-phosphate synthase (INO1) gene is regulated by factors that affect phospholipid synthesis. Mol Cell Biol 6: 3320-3328.
95. Jesch SA, Zhao X, Wells MT, Henry SA (2005) Genome-wide analysis reveals inositol, not choline, as the major effector of Ino2p-Ino4p and unfolded protein response target gene expression in yeast. J Biol Chem 280: 9106-9118.
96. Nunez LR, Jesch SA, Gaspar ML, Almaguer C, Villa-Garcia M, et al. (2008) Cell wall integrity MAPK pathway is essential for lipid homeostasis. J Biol Chem 283: 34204-34217.
97. Nikawa J, Yamashita S (1992) IRE1 encodes a putative protein kinase containing a membrane-spanning domain and is required for inositol phototrophy in Saccharomyces cerevisiae. Mol Microbiol 6: 1441-1446.
98. Joseph SK, Hajnoczky G (2007) IP3 receptors in cell survival and apoptosis: Ca2+ release and beyond. Apoptosis 12: 951-968.
99. Pinton P, Giorgi C, Siviero R, Zecchini E, Rizzuto R (2008) Calcium and apoptosis: ER-mitochondria Ca2+ transfer in the control of apoptosis. Oncogene 27: 6407-6418.
100. Rong Y, Distelhorst CW (2008) Bcl-2 protein family members: versatile regulators of calcium signaling in cell survival and apoptosis. Annu Rev Physiol 70: 73-91.
101. White C, Li C, Yang J, Petrenko NB, Madesh M, et al. (2005) The endoplasmic reticulum gateway to apoptosis by Bcl-X(L) modulation of the InsP3R. Nat Cell Biol 7: 1021-1028.
102. Criollo A, Vicencio JM, Tasdemir E, Maiuri MC, Lavandero S, et al. (2007) The inositol trisphosphate receptor in the control of autophagy. Autophagy 3: 350-353.
103. Sarkar S, Floto RA, Berger Z, Imarisio S, Cordenier A, et al. (2005) Lithium induces autophagy by inhibiting inositol monophosphatase. J Cell Biol 170: 1101-1111.
104. Sarkar S, Rubinsztein DC (2008) Small molecule enhancers of autophagy for neurodegenerative diseases. Mol Biosyst 4: 895-901.
105. Criollo A, Maiuri MC, Tasdemir E, Vitale I, Fiebig AA, et al. (2007) Regulation of autophagy by the inositol trisphosphate receptor. Cell Death Differ 14: 1029-1039.
106. Scarlatti F, Granata R, Meijer AJ, Codogno P (2009) Does autophagy have a license to kill mammalian cells? Cell Death Differ 16: 12-20.
107. Lam D, Golstein P (2008) A specific pathway inducing autophagic cell death is marked by an IP3R mutation. Autophagy 4: 349-350.
108. Sarkar S, Rubinsztein DC (2006) Inositol and IP3 levels regulate autophagy: biology and therapeutic speculations. Autophagy 2: 132-134.
109. Iwanyshyn WM, Han GS, Carman GM (2004) Regulation of phospholipid synthesis in Saccharomyces cerevisiae by zinc. J Biol Chem 279: 21976-21983.
110. Galluzzi L, Joza N, Tasdemir E, Maiuri MC, Hengartner M, et al. (2008) No death without life: vital functions of apoptotic effectors. Cell Death Differ 15: 1113-1123.
111. Sinha S, Colbert CL, Becker N, Wei Y, Levine B (2008) Molecular basis of the regulation of Beclin 1-dependent autophagy by the gamma-herpesvirus 68 Bcl-2 homolog M11. Autophagy 4: 989-997.
112. Zhang Q, Chieu HK, Low CP, Zhang S, Heng CK, et al. (2003) Schizosaccharomyces pombe cells deficient in triacylglycerols synthesis undergo apoptosis upon entry into the stationary phase. J Biol Chem 278: 47145-47155.
113. Low CP, Liew LP, Pervaiz S, Yang H (2005) Apoptosis and lipoapoptosis in the fission yeast Schizosaccharomyces pombe. FEMS Yeast Res 5: 1199-1206.
114. Low CP, Shui G, Liew LP, Buttner S, Madeo F, et al. (2008) Caspase-dependent and -independent lipotoxic cell-death pathways in fission yeast. J Cell Sci 121: 2671-2684.
115. Shaltiel G, Shamir A, Shapiro J, Ding D, Dalton E, et al. (2004) Valproate decreases inositol biosynthesis. Biol Psychiatry 56: 868-874.
116. Sun Q, Bi L, Su X, Tsurugi K, Mitsui K (2007) Valproate induces apoptosis by inducing accumulation of neutral lipids which was prevented by disruption of the SIR2 gene in Saccharomyces cerevisiae. FEBS Lett 581: 3991-3995.
117. Vaden DL, Ding D, Peterson B, Greenberg ML (2001) Lithium and valproate decrease inositol mass and increase expression of the yeast INO1 and INO2 genes for inositol biosynthesis. J Biol Chem 276: 15466-15471.
118. Hauptmann P, Riel C, Kunz-Schughart LA, Frohlich KU, Madeo F, et al. (2006) Defects in N-glycosylation induce apoptosis in yeast. Mol Microbiol 59: 765-778.
119. Perez-Sala D, Mollinedo F (1995) Inhibition of N-linked glycosylation induces early apoptosis in human promyelocytic HL-60 cells. J Cell Physiol 163: 523-531.
120. Wada I, Rindress D, Cameron PH, Ou WJ, Doherty JJ 2nd, et al. (1991) SSR alpha and associated calnexin are major calcium binding proteins of the endoplasmic reticulum membrane. J Biol Chem 266: 19599-19610.
121. Hammond C, Braakman I, Helenius A (1994) Role of N-linked oligosaccharide recognition, glucose trimming, and calnexin in glycoprotein folding and quality control. Proc Natl Acad Sci U S A 91: 913-917.
122. Hebert DN, Foellmer B, Helenius A (1995) Glucose trimming and reglucosylation determine glycoprotein association with calnexin in the endoplasmic reticulum. Cell 81: 425-433.
123. Kapoor M, Srinivas H, Kandiah E, Gemma E, Ellgaard L, et al. (2003) Interactions of substrate with calreticulin, an endoplasmic reticulum chaperone. J Biol Chem 278: 6194-6200.
124. Brockmeier A, Williams DB (2006) Potent lectin-independent chaperone function of calnexin under conditions prevalent within the lumen of the endoplasmic reticulum. Biochemistry 45: 12906-12916.
125. Jannatipour M, Callejo M, Parodi AJ, Armstrong J, Rokeach LA (1998) Calnexin and BiP interact with acid phosphatase independently of glucose trimming and reglucosylation in Schizosaccharomyces pombe. Biochemistry 37: 17253-17261.
126. Leach MR, Williams DB (2004) Lectin-deficient calnexin is capable of binding class I histocompatibility molecules in vivo and preventing their degradation. J Biol Chem 279: 9072-9079.
127. Ellgaard L, Helenius A (2003) Quality control in the endoplasmic reticulum. Nat Rev Mol Cell Biol 4: 181-191.
128. Chevet E, Wong HN, Gerber D, Cochet C, Fazel A, et al. (1999) Phosphorylation by CK2 and MAPK enhances calnexin association with ribosomes. EMBO J 18: 3655-3666.
129. Delom F, Chevet E (2006) In vitro mapping of calnexin interaction with ribosomes. Biochem Biophys Res Commun 341: 39-44.
130. Moreno S, Klar A, Nurse P (1991) Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol 194: 795-823.