Proline biosynthesis is required for endoplasmic reticulum stress tolerance in Saccharomyces cerevisiae

Journal of Biological Chemistry

Volumn 289, Issue 40, 2014, Pages 27794-27806

  Liang, Xinwen ^a   Dickman, Martin B ^b   Becker, Donald F ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BIOCHEMISTRY; BIOSYNTHESIS; CELL MEMBRANES; CYTOLOGY; PROTEINS;

ANAEROBIC GROWTH; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; GENETIC COMPLEMENTATION; MISFOLDED PROTEINS; PROTEIN AGGREGATION; REACTIVE OXYGEN SPECIES; UNFOLDED PROTEIN RESPONSE;

YEAST;

GLUTATHIONE; MITOGEN ACTIVATED PROTEIN KINASE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; PROLINE; REACTIVE OXYGEN METABOLITE; THIOL REAGENT; TUNICAMYCIN; DELTA-1-PYRROLINE-5-CARBOXYLATE REDUCTASE; GLUTAMATE 5-KINASE; PHOSPHOTRANSFERASE; PYRROLINE 5 CARBOXYLATE REDUCTASE;

AMINO ACID SYNTHESIS; ANAEROBIC GROWTH; ANTIBIOTIC SENSITIVITY; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; GENETIC COMPLEMENTATION; NONHUMAN; NULL ALLELE; OSMOLALITY; PRO1 GENE; PRO2 GENE; PRO3 GENE; PROTEIN AGGREGATION; SACCHAROMYCES CEREVISIAE; UNFOLDED PROTEIN RESPONSE; BIOSYNTHESIS; GENETICS; METABOLISM;

ENDOPLASMIC RETICULUM STRESS; NADP; PHOSPHOTRANSFERASES (CARBOXYL GROUP ACCEPTOR); PROLINE; PYRROLINE CARBOXYLATE REDUCTASES; SACCHAROMYCES CEREVISIAE; UNFOLDED PROTEIN RESPONSE;

EID: 84907494685     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.562827     Document Type: Article

References (79)

1. Pérez-Arellano, I, Carmona-Álvarez, F., Gallego, J., and Cervera, J. (2010) Molecular mechanisms modulating glutamate kinase activity. Identification of the proline feedback inhibitor binding site. J. Mol. Biol. 404,890-901
2. Liang, X., Zhang, L., Natarajan, S. K., and Becker, D. F. (2013) Proline mechanisms of stress survival. Antioxid. Redox Signal. 19, 998-1011
3. Krishnan, N., Dickman, M. B., and Becker, D. F. (2008) Proline modulates the intracellular redox environment and protects mammalian cells against oxidative stress. Free Radic. Biol. Med. 44, 671-681
4. Natarajan, S. K., Zhu, W., Liang, X., Zhang, L., Demers, A. J., Zimmerman, M. C., Simpson, M. A., and Becker, D. F. (2012) Proline dehydrogenase is essential for proline protection against hydrogen peroxide-induced cell death. Free Radie. Biol. Med. 53,1181-1191
5. Liu, W., Le, A., Hancock, C., Lane, A. N., Dang, C. V., Fan, T. W., and Phang, J. M. (2012) Reprogramming of proline and glutamine metabolism contributes to the proliferative and metabolic responses regulated by oncogenic transcription factor c-MYC. Proc. Natl. Acad. Sci. U.S.A. 109, 8983-8988
6. Zarse, K., Schmeisser, S., Groth, M., Priebe, S., Beuster, G., Kuhlow, D., Guthke, R., Platzer, M., Kahn, C. R., and Ristow, M. (2012) Impaired insulin/IGF1 signaling extends life span by promoting mitochondrial L-proline catabolism to induce a transient ROS signal. Cell Metab. 15, 451-465
7. Szabados, L., and Savouré, A. (2010) Proline: a multifunctional amino acid. Trends Plant Sci. 15, 89-97
8. Székely, G., Abrahám, E., Cséplo, A., Rigó, G., Zsigmond, L., Csiszár, J., Ayaydin, F., Strizhov, N., Jásik, J., Schmelzer, E., Koncz, C., and Szabados,L. (2008) Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. Plant J. 53, 11-28
9. Yildirim, Y., Tolun, A., and Tuysuz, B. (2011) The phenotype caused by PYCR1 mutations corresponds to geroderma osteodysplasticum rather than autosomal recessive cutis laxa type 2. Am. J. Med. Genet. A 155,134-140
10. Reversade, B., Escande-Beillard, N., Dimopoulou, A., Fischer, B., Chng, S. C., Li, Y., Shboul, M., Tham, P. Y., Kayserili, H., Al-Gazali, L., Shahwan,M., Brancati, F., Lee, H., O'Connor, B. D., Schmidt-von Kegler, M., Merriman, B., Nelson, S. F., Masri, A., Alkazaleh, F., Guerra, D., Ferrari, P., Nanda, A., Rajah, A., Markie, D., Gray, M., Nelson, J., Grix, A., Sommer, A., Savarirayan, R., Janecke, A. R., Steichen, E., Sillence, D., Hausser, I, Budde, B., Nürnberg, G., Nürnberg, P., Seemann, P., Kunkel, D., Zambruno, G., Dallapiccola, B., Schuelke, M., Robertson, S., Hamamy, H., Wollnik, B.,Van Maldergem, L., Mundlos, S., and Kornak, U. (2009) Mutations in PYCR1 cause cutis laxa with progeroid features. Nat. Genet. 41, 1016-1021
11. Baumgartner, M. R., Hu, C. A., Almashanu, S., Steel, G., Obie, C., Aral, B., Rabier, D., Kamoun, P., Saudubray, J. M., and Valle, D. (2000) Hyperammonemia with reduced ornithine, citrulline, arginine and proline: a new inborn error caused by a mutation in the gene encoding delta(1)-pyrroline-5-carboxylate synthase. Hum. Mol. Genet. 9, 2853-2858
12. Bicknell, L. S., Pitt, J., Aftimos, S., Ramadas, R., Maw, M. A., and Robertson, S. P. (2008) A missense mutation in ALDH18A1, encoding Δ1-pyrroline5-carboxylate synthase (P5CS), causes an autosomal recessive neurocutaneous syndrome. Eur. J. Hum. Genet. 16,1176-1186
13. Ernst, T., Hergenhahn, M., Kenzelmann, M., Cohen, C. D., Bonrouhi, M., Weninger, A., Klären, R., Gröne, E. F., Wiesel, M., Güdemann, C., Küster, J., Schott, W., Staehler, G., Kretzler, M., Hollstein, M., and Gröne, H. J. (2002) Decrease and gain of gene expression are equally discriminatory markers for prostate carcinoma: a gene expression analysis on total and microdissected prostate tissue. Am. J. Pathol. 160, 2169-2180
14. Jariwala, U., Prescott, J., Jia, L., Barski, A., Pregizer, S., Cogan, J. P., Arasheben, A., Tilley, W. D., Scher, H. I., Gerald, W. L, Buchanan, G., Coetzee, G. A., and Frenkel, B. (2007) Identification of novel androgen receptor target genes in prostate cancer. Mol. Cancer 6, 39
15. Olcabe, H., Satoh, S., Kato, T., Kitahara, O., Yanagawa, R., Yamaoka, Y., Tsunoda, T., Furukawa, Y., and Nakamura, Y. (2001) Genome-wide analysis of gene expression in human hepatocellular carcinomas using cDNA microarray: identification of genes involved in viral carcinogenesis and tumor progression. Cancer Res. 61, 2129-2137
16. Nilsson, R., Jain, M., Madhusudhan, N., Sheppard, N. G., Strittmatter, L., Kampf, C., Huang, J., Asplund, A., and Mootha, V. K. (2014) Metabolic enzyme expression highlights a key role for MTHFD2 and the mitochondrial folate pathway in cancer. Nat. Commun. 5, 3128
17. Takagi, H. (2008) Proline as a stress protectant in yeast: physiological functions, metabolic regulations, and biotechnological applications. Appl. Microbiol. Biotechnol. 81, 211-223
18. Ando, A., Nakamura, T., Murata, Y., Takagi, H., and Shima, J. (2007) Identification and classification of genes required for tolerance to freezethaw stress revealed by genome-wide screening of Saccharomyces cerevisiae deletion strains. FEMS Yeast Res. 7, 244-253
19. Lin, J.H., Walter, P., and Yen, T. S. (2008) Endoplasmic reticulum stress in disease pathogenesis. Annu. Rev. Pathol. 3, 399-425
20. Tabas, L, and Ron, D. (2011) Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat. Cell Biol. 13,184-190
21. Patil, C., and 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
22. Bonilla, M., and Cunningham, K. W. (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
23. Bonilla, M., Nastase, K. K., and Cunningham, K. W. (2002) Essential role of calcineurin in response to endoplasmic reticulum stress. EMBO J. 21, 2343-2353
24. Torres-Quiroz, F., García-Marqués, S., Coria, R., Randez-Gil, F., and Prieto, J. A. (2010) The activity of yeast Hog1 MAPK is required during endoplasmic reticulum stress induced by tunicamycin exposure. J. Biol.Chem. 285, 20088-20096
25. Bicknell, A. A., Tourtellotte, J., and Niwa, M. (2010) Late phase of the endoplasmic reticulum stress response pathway is regulated by Hogl MAP kinase.J. Biol. Chem. 285,17545-17555
26. Rand, J. D., and Grant, C. M. (2006) The thioredoxin system protects ribosomes against stress-induced aggregation. Mol. Biol. Cell 17,387-401
27. Samuel, D., Kumar, T. K., Ganesh, G., Jayaraman, G., Yang, P. W., Chang, M. M., Trivedi, V. D., Wang, S. L., Hwang, K. C., Chang, D. K., and Yu, C. (2000) Proline inhibits aggregation during protein refolding. Protein Sci. 9, 344-352
28. Kumar, T. K., Samuel, D., Jayaraman, G., Srimathi, T., and Yu, C. (1998) The role of proline in the prevention of aggregation during protein folding in vitro. Biochem. Mol. Biol. Int. 46, 509-517
29. Ignatova, Z., and Gierasch, L. M. (2006) Inhibition of protein aggregationin vitro and in vivo by a natural osmoprotectant. Proc. Natl. Acad. Sci. U.S.A. 103,13357-13361
30. Longtine, M. S., McKenzie, A., 3rd, Demarini, D. J., Shah, N. G., Wach, A., Brachat, A., Philippsen, P., and Pringle, J. R. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961
31. Grant, C. M., Perrone, G., and Dawes, I. W. (1998) Glutathione and catalase provide overlapping defenses for protection against hydrogen peroxide in the yeast Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 253, 893-898
32. Vandeputte, C., Guizon, I, Genestie-Denis, I, Vannier, B., and Lorenzon, G. (1994) A microtiter plate assay for total glutathione and glutathione disulfide contents in cultured/isolated cells: performance study of a new miniaturized protocol. Cell Biol. Toxicol. 10, 415-421
33. Chen, C., Wanduragala, S., Becker, D. F., and Dickman, M. B. (2006) Tomato QM-like protein protects Saccharomyces cerevisiae cells against oxidative stress by regulating intracellular proline levels. Appl. Environ. Microbiol. 72, 4001-4006
34. Carlberg, I, and Mannervik, B. (1985) Glutathione reductase. Methods Enzymol. 113, 484-490
35. Tan, S. X., Teo, M., Lam, Y. T., Dawes, I. W., and Perrone, G. G. (2009) Cu,Zn superoxide dismutase and NADP(H) homeostasis are required for tolerance of endoplasmic reticulum stress in Saccharomyces cerevisiae. Mol. Biol. Cell 20, 1493-1508
36. Zerez, C. R., Lee, S. J., and Tanaka, K. R. (1987) Spectrophotometric determination of oxidized and reduced pyridine nucleotides in erythrocytes using a single extraction procedure. Anal. Biochem. 164, 367-373
37. Cox, J. S., and Walter, P. (1996) A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 87,391-404
38. Cox, J.S., Shamu, C. E., and Walter, P. (1993) Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 73,1197-1206
39. Tomenchok, D. M., and Brandriss, M. C. (1987) Gene-enzyme relationships in the proline biosynthetic pathway of Saccharomyces cerevisiae. J. Bacteriol. 169, 5364-5372
40. Brandriss, M. C., and Magasanik, B. (1981) Subcellular compartmentation in control of converging pathways for proline and arginine metabolism in Saccharomyces cerevisiae. J. Bacteriol. 145,1359-1364
41. Brandriss, M. C. (1979) Isolation and preliminary characterization of Saccharomyces cerevisiae proline auxotrophs. J. Bacteriol. 138, 816-822
42. Balasubramanian, M. N., Butterworth, E. A., and Kalberg, M. S. (2013) Asparagine synthetase: regulation by cell stress and involvement in tumor biology. Am. J. Physiol. Endocrinol. Metab. 304, E789 -E799
43. Jämsä, E., Simonen, M., and Makarow, M. (1994) Selective retention of secretory proteins in the yeast endoplasmic reticulum by treatment of cells with a reducing agent. Yeast 10, 355-370
44. Pollard, M. G., Travers, K. J., and Weissman, J.S. (1998) Ero1p: a novel and ubiquitous protein with an essential role in oxidative protein folding in the endoplasmic reticulum. Mol. Cell 1,171-182
45. Barnes, G., Hansen, W. J., Holcomb, C. L., and Rine, J. (1984) Asparaginelinked glycosylation in Saccharomyces cerevisiae: genetic analysis of an early step. Mol. Cell. Biol. 4, 2381-2388
46. Hinnebusch, A. G. (2005) Translational regulation of GCN4 and the general amino acid control of yeast. Annu. Rev. Microbiol. 59, 407-450
47. Han, J., Back, S. H., Hur, J., Lin, Y. H., Gildersleeve, R., Shan, J., Yuan, C. L., Krokowski, D., Wang, S., Hatzoglou, M., Kalberg, M. S., Sartor, M. A., and Kaufman, R. J. (2013) ER stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nat. Cell Biol. 15,481-490
48. Chen, C., and Dickman, M. B. (2004) Dominant active Rae and dominant negative Rac revert the dominant active Ras phenotype in Colletotrichum trifolii by distinct signalling pathways. Mol. Microbiol. 51,1493-1507
49. Chakravarthi, S., Jessop, C. E., and Bulleid, N. J. (2006) The role of glutathione in disulphide bond formation and endoplasmic-reticulum-generated oxidative stress. EMBO Rep. 7, 271-275
50. Zhao, H., Kalivendi, S., Zhang, H., Joseph, J., Nithipatikom, K., VásquezVivar, J., and Kalyanaraman, B. (2003) Superoxide reacts with hydroethidine but forms a fluorescent product that is distinctly different fromethidium: potential implications in intracellular fluorescence detection of superoxide. Free Radic. Biol. Med. 34,1359 -1368
51. Chen, J., Zhang, Y., Wang, C, Lü, W., Jin, J. B., and Hua, X. (2011) Proline induces calcium-mediated oxidative burst and salicylic acid signaling.Amino Acids 40,1473-1484
52. Stathopoulos, A. M., and Cyert, M. S. (1997) Calcineurin acts through the CRZ1/TCN1-encoded transcription factor to regulate gene expression inyeast. Genes Dev. 11, 3432-3444
53. Marco-Marin, C., Gil-Ortiz, F., Pérez-Arellano, I., Cervera, J., Fita, I., and Rubio, V. (2007) A novel two-domain architecture within the amino acid kinase enzyme family revealed by the crystal structure of Escherichia coli glutamate 5-knase.J. Mol. Biol. 367,1431-1446
54. Sekine, T., Kawaguchi, A., Hamano, Y., and Takagi, H. (2007) Desensitization of feedback inhibition of the Saccharomyces cerevisiae yγ-glutamyl kinase enhances proline accumulation and freezing tolerance. Appl. Environ. Microbiol. 73, 4011-4019
55. Harding, H. P., Zhang, Y., Zeng, H., Novoa, I., Lu, P. D., Calfon, M., Sadri, N., Yun, C., Popko, B., Paules, R., Stojdl, D. F., Bell, J. C., Hettmann, T., Leiden, J. M., and Ron, D. (2003) An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 11, 619-633
56. Patil, C. K., Li, H., and Walter, P. (2004) Gcn4p and novel upstream activating sequences regulate targets of the unfolded protein response. PLoS Biol. 2, E246
57. Jousse, C., Oyadomari, S., Novoa, I, Lu, P., Zhang, Y., Harding, H. P., and Ron, D. (2003) Inhibition of a constitutive translation initiation factor 2α phosphatase, CReP, promotes survival of stressed cells. J. Cell Biol. 163,767-775
58. Delaney, J. R., Ahmed, U., Chou, A., Sim, S., Carr, D., Murakami, C. J., Schleit, J., Sutphin, G. L., An, E. H., Castanza, A., Fletcher, M., Higgins, S., Jelic, M., Klum, S., Muller, B., Peng, Z. J., Rai, D., Ros, V., Singh, M., Wende, H. V., Kennedy, B. K., and Kaeberlein, M. (2013) Stress profiling of longevity mutants identifies Afg3 as a mitochondrial determinant of cytoplasmic mRNA translation and aging. Aging Cell 12,156-166
59. Steffen, K. K., McCormick, M. A., Pham, K. M., MacKay, V. L., Delaney, J. R., Murakami, C. J., Kaeberlein, M., and Kennedy, B. K. (2012) Ribosome deficiency protects against ER stress in Saccharomyces cerevisiae. Genetics 191,107-118
60. Bhandary, B., Marahatta, A., Kim, H. R., and Chae, H. J. (2012) An involvement of oxidative stress in endoplasmic reticulum stress and its associated diseases. Int. J. Mol. Sci. 14, 434-456
61. Santos, C. X., Tanaka, L. Y., Wosniak, J., and Laurindo, F. R. (2009) Mechanisms and implications of reactive oxygen species generation during the unfolded protein response: roles of endoplasmic reticulum oxidoreductases, mitochondrial electron transport, and NADPH oxidase. Antioxid. Redox Signal. 11, 2409-2427
62. Jessop, C. E., and Bulleid, N. J. (2004) Glutathione directly reduces an oxidoreductase in the endoplasmic reticulum of mammalian cells.J. Biol.Chem. 279,55341-55347
63. Cuozzo, J. W., and Kaiser, C. A. (1999) Competition between glutathione and protein thiols for disulphide-bond formation. Nat. Cell Biol. 1, 130-135
64. Molteni, S. N., Fassio, A., Ciriolo, M. R., Filomeni, G., Pasqualetto, E., Fagioli, C., and Sitia, R. (2004) Glutathione limits Ero1-dependent oxidation in the endoplasmic reticulum. J Biol. Chem. 279, 32667-32673
65. Cullinan, S. B., Zhang, D., Hannink, M., Arvisais, E., Kaufman, R. J., and Diehl, J. A. (2003) Nrf2 is a direct PERK substrate and effector of PERK -dependent cell survival. Mol. Cell. Biol. 23, 7198-7209
66. Rouschop, K. M., Dubois, L. J., Keulers, T. G., van den Beucken, T., Lambin, P., Bussink, J., van der Kogel, A. J., Koritzinsky, M., and Wouters, B. G. (2013) PERK/eIF2α signaling protects therapy resistant hypoxic cells through induction of glutathione synthesis and protection against ROS. Proc. Natl. Acad. Sci. U.S.A. 110, 4622-4627
67. Haynes, C. M., Titus, E. A., and Cooper, A. A. (2004) Degradation of misfolded proteins prevents ER-derived oxidative stress and cell death. Mol. Cell 15, 767-776
68. Ying, W. (2008) NAD+/NADH and NADP+/NADPH in cellular functions and cell death: regulation and biological consequences. Antioxid.Redox Signal. 10,179-206
69. Wu, A. L., and Moye-Rowley, W. S. (1994) GSH1, which encodes y-glut tcysteine synthetase, is a target gene for yAP-1 transcriptional regulation. Mol. Cell. Biol. 14, 5832-5839
70. Stephen, D. W., Rivers, S. L., and Jamieson, D. J. (1995) The role of the YAP1 and YAP2 genes in the regulation of the adaptive oxidative stress responses of Saccharomyces cerevisiae. Mol. Microbiol. 16, 415-423
71. Grant, C. M., Collinson, L. P., Roe, J. H., and Dawes, I. W. (1996) Yeast glutathione reductase is required for protection against oxidative stress and is a target gene for yAP-1 transcriptional regulation. Mol. Microbiol. 21,171-179
72. Drakulic, T., Temple, M. D., Guido, R., Jarolim, S., Breitenbach, M., Attfield, P. V., and Dawes, I. W. (2005) Involvement of oxidative stress response genes in redox homeostasis, the level of reactive oxygen species, and ageing in Saccharomyces cerevisiae. FEMS Yeast Res. 5,1215-1228
73. Trotter, E. W., and Grant, C. M. (2002) Thioredoxins are required for protection against a reductive stress in the yeast Saccharomyces cerevisiae. Mol. Microbiol. 46, 869-878
74. Scherz-Shouval, R., and Elazar, Z. (2007) ROS, mitochondria and the regulation of autophagy. Trends Cell Biol. 17, 422-427
75. Scherz-Shouval, R., Shvets, E., Fass, E., Shorer, H., Gil, L., and Elazar, Z. (2007) Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J. 26,1749-1760
76. Chen, Y., Azad, M. B., and Gibson, S. B. (2009) Superoxide is the major reactive oxygen species regulating autophagy. Cell Death Differ. 16, 1040-1052
77. Cao, S. S., and Kaufman, R. J. (2014) Endoplasmic reticulum stress and oxidative stress in cell fate decision and human disease. Antioxid. Redox Signal. 21, 396-413
78. Chen, C., and Dickman, M. B. (2005) Proline suppresses apoptosis in the fungal pathogen Colletotrichum trifolii. Proc. Natl. Acad. Sci. U.S.A. 102,3459-3464
79. Hagedorn, C. H., and Phang, J. M. (1986) Catalytic transfer of hydride ions from NADPH to oxygen by the interconversions of proline and Δ1-pyrroline-5-carboxylate. Arch. Biochem. Biophys. 248,166-174