A LAPF/phafin1-like protein regulates TORC1 and lysosomal membrane permeabilization in response to endoplasmic reticulum membrane stress

Molecular Biology of the Cell

Volumn 26, Issue 25, 2015, Pages 4631-4645

  Kim, Adam ^a   Cunningham, Kyle W ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN INHIBITOR; FLUCONAZOLE; PHAFIN1 LIKE PROTEIN; PHOSPHATIDYLINOSITOL 3 PHOSPHATE; PROTEIN; RAPAMYCIN; TERCONAZOLE; TORC1 PROTEIN; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MULTIPROTEIN COMPLEX; PIB2 PROTEIN, S CEREVISIAE; POLYPHOSPHOINOSITIDE; SACCHAROMYCES CEREVISIAE PROTEIN; TARGET OF RAPAMYCIN KINASE;

APOPTOSIS; ARTICLE; CANDIDA ALBICANS; CELL PERMEABILIZATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM MEMBRANE; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVE SITE; ENZYME ACTIVITY; GENETIC ASSOCIATION; LIPOGENESIS; LYSOSOME MEMBRANE; MUTANT; MUTATION; NONHUMAN; PRIORITY JOURNAL; ANIMAL; CELL MEMBRANE PERMEABILITY; CELL VACUOLE; GENETICS; LYSOSOME; MAMMAL; METABOLISM; SACCHAROMYCES CEREVISIAE;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CELL MEMBRANE PERMEABILITY; ENDOPLASMIC RETICULUM STRESS; LYSOSOMES; MAMMALS; MULTIPROTEIN COMPLEXES; PHOSPHATIDYLINOSITOL PHOSPHATES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TOR SERINE-THREONINE KINASES; VACUOLES;

EID: 84951191098     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E15-08-0581     Document Type: Article

References (70)

1. Alby K, Schaefer D, Sherwood RK, Jones SK Jr, Bennett RJ (2010). Identification of a cell death pathway in Candida albicans during the response to pheromone. Eukaryot Cell 9, 1690-1701.
2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 25, 3389-3402.
3. Arnandis T, Ferrer-Vicens I, Garcia-Trevijano ER, Miralles VJ, Garcia C, Torres L, Vina JR, Zaragoza R (2012). Calpains mediate epithelial-cell death during mammary gland involution: mitochondria and lysosomal destabilization. Cell Death Differ 19, 1536-1548.
4. Baars TL, Petri S, Peters C, Mayer A (2007). Role of the V-ATPase in regulation of the vacuolar fission-fusion equilibrium. Mol Biol Cell 18, 3873-3882.
5. Banuelos MG, Moreno DE, Olson DK, Nguyen Q, Ricarte F, Aguilera-Sandoval CR, Gharakhanian E (2010). Genomic analysis of severe hypersensitivity to hygromycin B reveals linkage to vacuolar defects and new vacuolar gene functions in Saccharomyces cerevisiae. Curr Genet 56, 121-137.
6. Binda M, Peli-Gulli MP, Bonfils G, Panchaud N, Urban J, Sturgill TW, Loewith R, De Virgilio C (2009). The Vam6 GEF controls TORC1 by activating the EGO complex. Mol Cell 35, 563-573.
7. Bonilla M, Cunningham KW (2003). Mitogen-Activated protein kinase stimulation of Ca2+ signaling is required for survival of endoplasmic reticulum stress in yeast. Mol Biol Cell 14, 4296-4305.
8. Bonilla M, Nastase KK, Cunningham KW (2002). Essential role of calcineurin in response to endoplasmic reticulum stress. EMBO J 21, 2343-2353.
9. Boya P, Kroemer G (2008). Lysosomal membrane permeabilization in cell death. Oncogene 27, 6434-6451.
10. Bridges D, Fisher K, Zolov SN, Xiong T, Inoki K, Weisman LS, Saltiel AR (2012). Rab5 proteins regulate activation and localization of target of rapamycin complex 1. J Biol Chem 287, 20913-20921.
11. Caraveo G, Auluck PK, Whitesell L, Chung CY, Baru V, Mosharov EV, Yan X, Ben-Johny M, Soste M, Picotti P, et al. (2014). Calcineurin determines toxic versus beneficial responses to alpha-synuclein. Proc Natl Acad Sci USA 111, E3544-E3552.
12. Chen W, Li N, Chen T, Han Y, Li C, Wang Y, He W, Zhang L, Wan T, Cao X (2005). The lysosome-Associated apoptosis-inducing protein containing the pleckstrin homology (PH) and FYVE domains (LAPF), representative of a novel family of PH and FYVE domain-containing proteins, induces caspase-independent apoptosis via the lysosomal-mitochondrial pathway. J Biol Chem 280, 40985-40995.
13. Costanzo M, Baryshnikova A, Bellay J, Kim Y, Spear ED, Sevier CS, Ding H, Koh JL, Toufighi K, Mostafavi S, et al. (2010). The genetic landscape of a cell. Science 327, 425-431.
14. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004). WebLogo: A sequence logo generator. Genome Res 14, 1188-1190.
15. Dudgeon DD, Zhang N, Ositelu OO, Kim H, Cunningham KW (2008). Nonapoptotic death of Saccharomyces cerevisiae cells that is stimulated by Hsp90 and inhibited by calcineurin and Cmk2 in response to endoplasmic reticulum stresses. Eukaryot Cell 7, 2037-2051.
16. Eastwood MD, Cheung SW, Meneghini MD (2013). Programmed nuclear destruction in yeast: self-eating by vacuolar lysis. Autophagy 9, 263-265.
17. Eisen MB, Spellman PT, Brown PO, Botstein D (1998). Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95, 14863-14868.
18. Epple UD, Suriapranata I, Eskelinen EL, Thumm M (2001). Aut5/Cvt17p, a putative lipase essential for disintegration of autophagic bodies inside the vacuole. J Bacteriol 183, 5942-5955.
19. Fox DS, Heitman J (2002). Good fungi gone bad: The corruption of calcineurin. Bioessays 24, 894-903.
20. Gailite I, Egger-Adam D, Wodarz A (2012). The phosphoinositide-Associated protein Rush hour regulates endosomal trafficking in Drosophila. Mol Biol Cell 23, 433-447.
21. Gao M, Kaiser CA (2006). A conserved GTPase-containing complex is required for intracellular sorting of the general amino-Acid permease in yeast. Nat Cell Biol 8, 657-667.
22. Giaever G, Chu AM, Ni L, Connelly C, Riles L, Veronneau S, Dow S, Lucau-Danila A, Anderson K, Andre B, et al. (2002). Functional profiling of the Saccharomyces cerevisiae genome. Nature 418, 387-391.
23. Glass NL, Dementhon K (2006). Non-self recognition and programmed cell death in filamentous fungi. Curr Opin Microbiol 9, 553-558.
24. Gonzalez A, Shimobayashi M, Eisenberg T, Merle DA, Pendl T, Hall MN, Moustafa T (2015). TORC1 promotes phosphorylation of ribosomal protein S6 via the AGC kinase Ypk3 in Saccharomyces cerevisiae. PLoS One 10, e0120250.
25. Hatsugai N, Yamada K, Goto-Yamada S, Hara-Nishimura I (2015). Vacuolar processing enzyme in plant programmed cell death. Front Plant Sci 6, 234.
26. Hoepfner D, Helliwell SB, Sadlish H, Schuierer S, Filipuzzi I, Brachat S, Bhullar B, Plikat U, Abraham Y, Altorfer M, et al. (2014). High-resolution chemical dissection of a model eukaryote reveals targets, pathways and gene functions. Microbiol Res 169, 107-120.
27. Huber A, Bodenmiller B, Uotila A, Stahl M, Wanka S, Gerrits B, Aebersold R, Loewith R (2009). Characterization of the rapamycin-sensitive phosphoproteome reveals that Sch9 is a central coordinator of protein synthesis. Genes Dev 23, 1929-1943.
28. Jin N, Mao K, Jin Y, Tevzadze G, Kauffman EJ, Park S, Bridges D, Loewith R, Saltiel AR, Klionsky DJ, Weisman LS (2014). Roles for PI(3, 5)P2 in nutrient sensing through TORC1. Mol Biol Cell 25, 1171-1185.
29. Kihara A, Noda T, Ishihara N, Ohsumi Y (2001). Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J Cell Biol 152, 519-530.
30. Kim H, Kim A, Cunningham KW (2012). Vacuolar H+-ATPase (V-ATPase) promotes vacuolar membrane permeabilization and nonapoptotic death in stressed yeast. J Biol Chem 287, 19029-19039.
31. Kreuzaler PA, Staniszewska AD, Li W, Omidvar N, Kedjouar B, Turkson J, Poli V, Flavell RA, Clarkson RW, Watson CJ (2011). Stat3 controls lysosomal-mediated cell death in vivo. Nat Cell Biol 13, 303-309.
32. Li N, Zheng Y, Chen W, Wang C, Liu X, He W, Xu H, Cao X (2007). Adaptor protein LAPF recruits phosphorylated p53 to lysosomes and triggers lysosomal destabilization in apoptosis. Cancer Res 67, 11176-11185.
33. Lin WJ, Yang CY, Li LL, Yi YH, Chen KW, Lin YC, Liu CC, Lin CH (2012). Lysosomal targeting of phafin1 mediated by Rab7 induces autophagosome formation. Biochem Biophys Res Commun 417, 35-42.
34. Liu S, Hou Y, Liu W, Lu C, Wang W, Sun S (2015). Components of the calcium-calcineurin signaling pathway in fungal cells and their potential as antifungal targets. Eukaryot Cell 14, 324-334.
35. Loewith R, Hall MN (2011). Target of rapamycin (TOR) in nutrient signaling and growth control. Genetics 189, 1177-1201.
36. Longtine MS, McKenzie A III, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR (1998). Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961.
37. MacGurn JA, Hsu PC, Smolka MB, Emr SD (2011). TORC1 regulates endocytosis via Npr1-mediated phosphoinhibition of a ubiquitin ligase adaptor. Cell 147, 1104-1117.
38. Martin DC, Kim H, Mackin NA, Maldonado-Baez L, Evangelista CC, Beaudry VG, Dudgeon DD, Naiman DQ, Erdman SE, Cunningham KW (2011). New regulators of a high affinity Ca2+ influx system (HACS) revealed through a genome-wide screen in yeast. J Biol Chem 286, 10744-10754.
39. Mehta S, Li H, Hogan PG, Cunningham KW (2009). Domain architecture of the regulators of calcineurin (RCANs) and identification of a divergent RCAN in yeast. Mol Cell Biol 29, 2777-2793.
40. Michaillat L, Baars TL, Mayer A (2012). Cell-free reconstitution of vacuole membrane fragmentation reveals regulation of vacuole size and number by TORC1. Mol Biol Cell 23, 881-895.
41. Mrschtik M, Ryan KM (2015). Lysosomal proteins in cell death and autophagy. FEBS J 282, 1858-1870.
42. Muller EM, Locke EG, Cunningham KW (2001). Differential regulation of two Ca2+ influx systems by pheromone signaling in Saccharomyces cerevisiae. Genetics 159, 1527-1538.
43. Oliveira AP, Ludwig C, Zampieri M, Weisser H, Aebersold R, Sauer U (2015). Dynamic phosphoproteomics reveals TORC1-dependent regulation of yeast nucleotide and amino acid biosynthesis. Sci Signal 8, rs4.
44. Peterson JS, McCall K (2013). Combined inhibition of autophagy and caspases fails to prevent developmental nurse cell death in the Drosophila melanogaster ovary. PLoS One 8, e76046.
45. Pinan-Lucarre B, Paoletti M, Clave C (2007). Cell death by incompatibility in the fungus Podospora. Semin Cancer Biol 17, 101-111.
46. Reinke A, Chen JC, Aronova S, Powers T (2006). Caffeine targets TOR complex I and provides evidence for a regulatory link between the FRB and kinase domains of Tor1p. J Biol Chem 281, 31616-31626.
47. Schultz J, Copley RR, Doerks T, Ponting CP, Bork P (2000). SMART: A Webbased tool for the study of genetically mobile domains. Nucleic Acids Res 28, 231-234.
48. Schu PV, Takegawa K, Fry MJ, Stack JH, Waterfield MD, Emr SD (1993). Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting. Science 260, 88-91.
49. Sengupta S, Peterson TR, Sabatini DM (2010). Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Mol Cell 40, 310-322.
50. Shin ME, Ogburn KD, Varban OA, Gilbert PM, Burd CG (2001). FYVE domain targets Pib1p ubiquitin ligase to endosome and vacuolar membranes. J Biol Chem 276, 41388-41393.
51. Starai VJ, Jun Y, Wickner W (2007). Excess vacuolar SNAREs drive lysis and Rab bypass fusion. Proc Natl Acad Sci USA 104, 13551-13558.
52. Stefan CP, Cunningham KW (2013). Kch1 family proteins mediate essential responses to endoplasmic reticulum stresses in the yeasts Saccharomyces cerevisiae and Candida albicans. J Biol Chem 288, 34861-34870.
53. Stefan CP, Zhang N, Sokabe T, Rivetta A, Slayman CL, Montell C, Cunningham KW (2013). Activation of an essential calcium signaling pathway in Saccharomyces cerevisiae by Kch1 and Kch2, putative low-Affinity potassium transporters. Eukaryot Cell 12, 204-214.
54. Steinbach WJ, Reedy JL, Cramer RA Jr, Perfect JR, Heitman J (2007). Harnessing calcineurin as a novel anti-infective agent against invasive fungal infections. Nat Rev Microbiol 5, 418-430.
55. Stracka D, Jozefczuk S, Rudroff F, Sauer U, Hall MN (2014). Nitrogen source activates TOR (target of rapamycin) complex 1 via glutamine and independently of Gtr/Rag proteins. J Biol Chem 289, 25010-25020.
56. Syntichaki P, Samara C, Tavernarakis N (2005). The vacuolar H+-ATPase mediates intracellular acidification required for neurodegeneration in C. elegans. Curr Biol 15, 1249-1254.
57. Syntichaki P, Xu K, Driscoll M, Tavernarakis N (2002). Specific aspartyl and calpain proteases are required for neurodegeneration in C. elegans. Nature 419, 939-944.
58. Tarassov K, Messier V, Landry CR, Radinovic S, Serna Molina MM, Shames I, Malitskaya Y, Vogel J, Bussey H, Michnick SW (2008). An in vivo map of the yeast protein interactome. Science 320, 1465-1470.
59. Teter SA, Eggerton KP, Scott SV, Kim J, Fischer AM, Klionsky DJ (2001). Degradation of lipid vesicles in the yeast vacuole requires function of Cvt17, a putative lipase. J Biol Chem 276, 2083-2087.
60. Thompson JD, Higgins DG, Gibson TJ (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673-4680.
61. Toth ML, Simon P, Kovacs AL, Vellai T (2007). Influence of autophagy genes on ion-channel-dependent neuronal degeneration in Caenorhabditis elegans. J Cell Sci 120, 1134-1141.
62. van Doorn WG (2011). Classes of programmed cell death in plants, compared to those in animals. J Exp Bot 62, 4749-4761.
63. Vida TA, Emr SD (1995). A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J Cell Biol 128, 779-792.
64. Wang T, Lao U, Edgar BA (2009). TOR-mediated autophagy regulates cell death in Drosophila neurodegenerative disease. J Cell Biol 186, 703-711.
65. Wanke V, Cameroni E, Uotila A, Piccolis M, Urban J, Loewith R, De Virgilio C (2008). Caffeine extends yeast lifespan by targeting TORC1. Mol Microbiol 69, 277-285.
66. Wu X, Tu BP (2011). Selective regulation of autophagy by the Iml1-Npr2-Npr3 complex in the absence of nitrogen starvation. Mol Biol Cell 22, 4124-4133.
67. Yacobi-Sharon K, Namdar Y, Arama E (2013). Alternative germ cell death pathway in Drosophila involves HtrA2/Omi, lysosomes, and a caspase-9 counterpart. Dev Cell 25, 29-42.
68. Yamashima T, Oikawa S (2009). The role of lysosomal rupture in neuronal death. Prog Neurobiol 89, 343-358.
69. Yuan HX, Russell RC, Guan KL (2013). Regulation of PIK3C3/VPS34 complexes by MTOR in nutrient stress-induced autophagy. Autophagy 9, 1983-1995.
70. Zhang NN, Dudgeon DD, Paliwal S, Levchenko A, Grote E, Cunningham KW (2006). Multiple signaling pathways regulate yeast cell death during the response to mating pheromones. Mol Biol Cell 17, 3409-3422.