The impact of oxygen on the transcriptome of recombinant S. cerevisiae and P. pastoris - a comparative analysis

BMC Genomics

Volumn 12, Issue , 2011, Pages

  Baumann, Kristin ^a   Dato, Laura ^b   Graf, Alexandra B ^c,d   Frascotti, Gianni ^b   Dragosits, Martin ^c,f   Porro, Danilo ^b   Mattanovich, Diethard ^c,e   Ferrer, Pau ^a   Branduardi, Paola ^b  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b UNIVERSITY OF MILANO BICOCCA   (Italy)

^c UNIVERSITY OF AGRICULTURAL SCIENCES   (Austria)

^d Fachhochschule Campus Wien   (Austria)

^e AUSTRIAN CENTRE OF INDUSTRIAL BIOTECHNOLOGY   (Austria)

^f Davis   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; ERGOSTEROL; IMMUNOGLOBULIN F(AB) FRAGMENT; OXYGEN; RECOMBINANT PROTEIN;

ADAPTATION; ARTICLE; CARBON METABOLISM; CHEMOSTAT; COMPARATIVE STUDY; CONTROLLED STUDY; FERMENTATION; FUNGAL METABOLISM; FUNGUS CULTURE; FUNGUS GROWTH; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; HYPOXIA; NONHUMAN; OXYGEN CONSUMPTION; PICHIA PASTORIS; PRODUCTIVITY; PROTEIN SYNTHESIS; SACCHAROMYCES CEREVISIAE; STEADY STATE; STEROL SYNTHESIS; STRESS; TRANSCRIPTOMICS; UNFOLDED PROTEIN RESPONSE; BIOREACTOR; CLUSTER ANALYSIS; DRUG EFFECT; GENETIC ENGINEERING; GENETICS; GENOMICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; PICHIA; PRINCIPAL COMPONENT ANALYSIS; SPECIES DIFFERENCE;

EUKARYOTA; PICHIA PASTORIS; SACCHAROMYCES CEREVISIAE;

BIOREACTORS; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; GENETIC ENGINEERING; GENOMICS; HUMANS; OXYGEN; PICHIA; PRINCIPAL COMPONENT ANALYSIS; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SPECIES SPECIFICITY; TRANSCRIPTION, GENETIC;

EID: 79955687321     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-12-218     Document Type: Article

References (66)

1. Idiris A, Tohda H, Kumagai H, Takegawa K. Engineering of protein secretion in yeast: strategies and impact on protein production. Appl Microbiol Biotechnol 2010, 86(2):403-417. 10.1007/s00253-010-2447-0, 20140428.
2. Graumann K, Premstaller A. Manufacturing of recombinant therapeutic proteins in microbial systems. Biotechnol J 2006, 1(2):164-186. 10.1002/biot.200500051, 16892246.
3. Graf A, Dragosits M, Gasser B, Mattanovich D. Yeast systems biotechnology for the production of heterologous proteins. FEMS Yeast Res 2009, 9(3):335-348. 10.1111/j.1567-1364.2009.00507.x, 19341379.
4. Gasser B, Saloheimo M, Rinas U, Dragosits M, Rodríguez-Carmona E, Baumann K, Giuliani M, Parrilli E, Branduardi P, Lang C, et al. Protein folding and conformational stress in microbial cells producing recombinant proteins: a host comparative overview. Microb Cell Fact 2008, 7:11. 10.1186/1475-2859-7-11, 2322954, 18394160.
5. Gasch A, Spellman P, Kao C, Carmel-Harel O, Eisen M, Storz G, Botstein D, Brown P. Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 2000, 11(12):4241-4257. 15070, 11102521.
6. Causton H, Ren B, Koh S, Harbison C, Kanin E, Jennings E, Lee T, True H, Lander E, Young R. Remodeling of yeast genome expression in response to environmental changes. Mol Biol Cell 2001, 12(2):323-337. 30946, 11179418.
7. Wentz A, Shusta E. A novel high-throughput screen reveals yeast genes that increase secretion of heterologous proteins. Appl Environ Microbiol 2007, 73(4):1189-1198. 10.1128/AEM.02427-06, 1828678, 17189442.
8. Sevastsyanovich Y, Alfasi S, Cole J. Sense and nonsense from a systems biology approach to microbial recombinant protein production. Biotechnol Appl Biochem 2010, 55(1):9-28. 10.1042/BA20090174, 20044926.
9. Gasser B, Sauer M, Maurer M, Stadlmayr G, Mattanovich D. Transcriptomics-based identification of novel factors enhancing heterologous protein secretion in yeasts. Appl Environ Microbiol 2007, 73(20):6499-6507. 10.1128/AEM.01196-07, 2075068, 17766460.
10. De Schutter K, Lin Y, Tiels P, Van Hecke A, Glinka S, Weber-Lehmann J, Rouzé P, Van de Peer Y, Callewaert N. Genome sequence of the recombinant protein production host Pichia pastoris. Nat Biotechnol 2009, 27(6):561-566. 10.1038/nbt.1544, 19465926.
11. Mattanovich D, Graf A, Stadlmann J, Dragosits M, Redl A, Maurer M, Kleinheinz M, Sauer M, Altmann F, Gasser B. Genome, secretome and glucose transport highlight unique features of the protein production host Pichia pastoris. Microb Cell Fact 2009, 8:29. 10.1186/1475-2859-8-29, 2702363, 19490607.
12. Graf A, Gasser B, Dragosits M, Sauer M, Leparc G, Tüchler T, Kreil D, Mattanovich D. Novel insights into the unfolded protein response using Pichia pastoris specific DNA microarrays. BMC Genomics 2008, 9:390. 10.1186/1471-2164-9-390, 2533675, 18713468.
13. Dragosits M, Stadlmann J, Albiol J, Baumann K, Maurer M, Gasser B, Sauer M, Altmann F, Ferrer P, Mattanovich D. The effect of temperature on the proteome of recombinant Pichia pastoris. J Proteome Res 2009, 8(3):1380-1392. 10.1021/pr8007623, 19216534.
14. Dragosits M, Stadlmann J, Graf A, Gasser B, Maurer M, Sauer M, Kreil D, Altmann F, Mattanovich D. The response to unfolded protein is involved in osmotolerance of Pichia pastoris. BMC Genomics 2010, 11(1):207. 10.1186/1471-2164-11-207, 2867824, 20346137.
15. Baumann K, Carnicer M, Dragosits M, Graf A, Stadlmann J, Jouhten P, Maaheimo H, Gasser B, Albiol J, Mattanovich D, et al. A multi-level study of recombinant Pichia pastoris in different oxygen conditions. BMC Syst Biol 2010, 4(1):141. 10.1186/1752-0509-4-141, 2987880, 20969759.
16. Gach J, Maurer M, Hahn R, Gasser B, Mattanovich D, Katinger H, Kunert R. High level expression of a promising anti-idiotypic antibody fragment vaccine against HIV-1 in Pichia pastoris. J Biotechnol 2007, 128(4):735-746. 10.1016/j.jbiotec.2006.12.020, 17270302.
17. Gach J, Quendler H, Strobach S, Katinger H, Kunert R. Structural analysis and in vivo administration of an anti-idiotypic antibody against mAb 2F5. Mol Immunol 2008, 45(4):1027-1034. 10.1016/j.molimm.2007.07.030, 17804071.
18. Sørensen H. Towards universal systems for recombinant gene expression. Microb Cell Fact 2010, 9:27. 10.1186/1475-2859-9-27, 2876075, 20433754.
19. Baumann K, Maurer M, Dragosits M, Cos O, Ferrer P, Mattanovich D. Hypoxic fed-batch cultivation of Pichia pastoris increases specific and volumetric productivity of recombinant proteins. Biotechnol Bioeng 2008, 100(1):177-183. 10.1002/bit.21763, 18078287.
20. Raychaudhuri S, Stuart J, Altman R. Principal components analysis to summarize microarray experiments: application to sporulation time series. Pac Symp Biocomput 2000, 455-466.
21. Daran-Lapujade P, Jansen M, Daran J, van Gulik W, de Winde J, Pronk J. Role of transcriptional regulation in controlling fluxes in central carbon metabolism of Saccharomyces cerevisiae. A chemostat culture study. J Biol Chem 2004, 279(10):9125-9138. 10.1074/jbc.M309578200, 14630934.
22. de Groot M, Daran-Lapujade P, van Breukelen B, Knijnenburg T, de Hulster E, Reinders M, Pronk J, Heck A, Slijper M. Quantitative proteomics and transcriptomics of anaerobic and aerobic yeast cultures reveals post-transcriptional regulation of key cellular processes. Microbiology 2007, 153(Pt 11):3864-3878.
23. Wiebe M, Rintala E, Tamminen A, Simolin H, Salusjärvi L, Toivari M, Kokkonen J, Kiuru J, Ketola R, Jouhten P, et al. Central carbon metabolism of Saccharomyces cerevisiae in anaerobic, oxygen-limited and fully aerobic steady-state conditions and following a shift to anaerobic conditions. FEMS Yeast Res 2008, 8(1):140-154. 10.1111/j.1567-1364.2007.00234.x, 17425669.
24. Bagnat M, Keränen S, Shevchenko A, Simons K. Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast. Proc Natl Acad Sci USA 2000, 97(7):3254-3259. 10.1073/pnas.060034697, 16225, 10716729.
25. Proszynski T, Klemm R, Gravert M, Hsu P, Gloor Y, Wagner J, Kozak K, Grabner H, Walzer K, Bagnat M, et al. A genome-wide visual screen reveals a role for sphingolipids and ergosterol in cell surface delivery in yeast. Proc Natl Acad Sci USA 2005, 102(50):17981-17986. 10.1073/pnas.0509107102, 1312417, 16330752.
26. Jin H, McCaffery J, Grote E. Ergosterol promotes pheromone signaling and plasma membrane fusion in mating yeast. J Cell Biol 2008, 180(4):813-826. 10.1083/jcb.200705076, 2265586, 18299351.
27. Carnicer M, Baumann K, Töplitz I, Sánchez-Ferrando F, Mattanovich D, Ferrer P, Albiol J. Macromolecular and elemental composition analysis and extracellular metabolite balances of Pichia pastoris growing at different oxygen levels. Microb Cell Fact 2009, 8:65. 10.1186/1475-2859-8-65, 2799386, 20003217.
28. Shobayashi M, Mitsueda S, Ago M, Fujii T, Iwashita K, Iefuji H. Effects of culture conditions on ergosterol biosynthesis by Saccharomyces cerevisiae. Biosci Biotechnol Biochem 2005, 69(12):2381-2388. 10.1271/bbb.69.2381, 16377897.
29. Jahnke L, Klein HP. Oxygen requirements for formation and activity of the squalene epoxidase in Saccharomyces cerevisiae. J Bacteriol 1983, 155(2):488-492. 217714, 6348021.
30. Rosenfeld E, Beauvoit B. Role of the non-respiratory pathways in the utilization of molecular oxygen by Saccharomyces cerevisiae. Yeast 2003, 20(13):1115-1144. 10.1002/yea.1026, 14558145.
31. Rintala E, Toivari M, Pitkänen J, Wiebe M, Ruohonen L, Penttilä M. Low oxygen levels as a trigger for enhancement of respiratory metabolism in Saccharomyces cerevisiae. BMC Genomics 2009, 10:461. 10.1186/1471-2164-10-461, 2767370, 19804647.
32. Andreasen A, Stier T. Anaerobic nutrition of Saccharomyces cerevisiae. I. Ergosterol requirement for growth in a defined medium. J Cell Physiol 1953, 41(1):23-36. 10.1002/jcp.1030410103, 13034889.
33. Andreasen A, Stier T. Anaerobic nutrition of Saccharomyces cerevisiae. II. Unsaturated fatty acid requirement for growth in a defined medium. J Cell Physiol 1954, 43(3):271-281. 10.1002/jcp.1030430303, 13192151.
34. Bunn HF, Poyton RO. Oxygen sensing and molecular adaptation to hypoxia. Physiol Rev 1996, 76(3):839-885.
35. Guan XL, Souza CM, Pichler H, Dewhurst G, Schaad O, Kajiwara K, Wakabayashi H, Ivanova T, Castillon GA, Piccolis M, et al. Functional interactions between sphingolipids and sterols in biological membranes regulating cell physiology. Mol Biol Cell 2009, 20(7):2083-2095. 10.1091/mbc.E08-11-1126, 2663937, 19225153.
36. Eisenkolb M, Zenzmaier C, Leitner E, Schneiter R. A specific structural requirement for ergosterol in long-chain fatty acid synthesis mutants important for maintaining raft domains in yeast. Mol Biol Cell 2002, 13(12):4414-4428. 10.1091/mbc.E02-02-0116, 138643, 12475962.
37. Munn AL, Heese-Peck A, Stevenson BJ, Pichler H, Riezman H. Specific sterols required for the internalization step of endocytosis in yeast. Mol Biol Cell 1999, 10(11):3943-3957. 25690, 10564282.
38. Bruinenberg P, van Dijken J, Scheffers W. An enzymic analysis of NADPH production and consumption in Candida utilis. J Gen Microbiol 1983, 129(4):965-971.
39. González-Siso M, Freire-Picos M, Ramil E, González-Domínguez M, Rodríguez Torres A, Cerdán M. Respirofermentative metabolism in Kluyveromyces lactis: Insights and perspectives. Enzyme Microb Technol 2000, 26(9-10):699-705. 10.1016/S0141-0229(00)00161-7, 10862875.
40. Blank L, Sauer U. TCA cycle activity in Saccharomyces cerevisiae is a function of the environmentally determined specific growth and glucose uptake rates. Microbiology 2004, 150(Pt 4):1085-1093.
41. Gancedo C, Serrano R. Energy-yielding metabolism. The Yeasts 1989, 205-259. New York: Academic Press, Harrison JS, Rose AH, 2.
42. Petrash J, Murthy B, Young M, Morris K, Rikimaru L, Griest T, Harter T. Functional genomic studies of aldo-keto reductases. Chem Biol Interact 2001, 130-132(1-3):673-683. 10.1016/S0009-2797(00)00258-1, 11306085.
43. Ingram J, Wood W. Enzymatic basis for D-Arabitol production by Saccharomyces Rouxii. J Bacteriol 1965, 89:1186-1194. 277626, 14292984.
44. Marsh L, Rose M. The pathway of cell and nuclear fusion during mating in S. cerevisiae. The Molecular and Cellular Biology of the Yeast Saccharomyces 1997, 827-888. Cold Spring Harbor, NY, Pringle JR, Broach JR, Jones EW.
45. Tolstorukov I, Cregg JM. Classical genetics. Methods Mol Biol 2007, 389:189-202. 10.1007/978-1-59745-456-8_14, 17951644.
46. Epstein C, Waddle J, Hale W, Davé V, Thornton J, Macatee T, Garner H, Butow R. Genome-wide responses to mitochondrial dysfunction. Mol Biol Cell 2001, 12(2):297-308. 30944, 11179416.
47. Tuttle D, Dunn WJ. Divergent modes of autophagy in the methylotrophic yeast Pichia pastoris. J Cell Sci 1995, 108(Pt 1):25-35.
48. Piper M, Daran-Lapujade P, Bro C, Regenberg B, Knudsen S, Nielsen J, Pronk J. Reproducibility of oligonucleotide microarray transcriptome analyses. An interlaboratory comparison using chemostat cultures of Saccharomyces cerevisiae. J Biol Chem 2002, 277(40):37001-37008. 10.1074/jbc.M204490200, 12121991.
49. Kwast K, Lai L, Menda N, James D, Aref S, Burke P. Genomic analyses of anaerobically induced genes in Saccharomyces cerevisiae: functional roles of Rox1 and other factors in mediating the anoxic response. J Bacteriol 2002, 184(1):250-265. 10.1128/JB.184.1.250-265.2002, 134782, 11741867.
50. Martíez-Force E, Benítez T. Changes in yeast amino acid pool with respiratory versus fermentative metabolism. Biotechnol Bioeng 1992, 40(6):643-649. 10.1002/bit.260400602, 18601163.
51. Krantz M, Nordlander B, Valadi H, Johansson M, Gustafsson L, Hohmann S. Anaerobicity prepares Saccharomyces cerevisiae cells for faster adaptation to osmotic shock. Eukaryot Cell 2004, 3(6):1381-1390. 10.1128/EC.3.6.1381-1390.2004, 539022, 15590813.
52. François J, Parrou J. Reserve carbohydrates metabolism in the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev 2001, 25(1):125-145.
53. Kane S, Roth R. Carbohydrate metabolism during ascospore development in yeast. J Bacteriol 1974, 118(1):8-14. 246633, 4595206.
54. Argüelles J. Physiological roles of trehalose in bacteria and yeasts: a comparative analysis. Arch Microbiol 2000, 174(4):217-224. 10.1007/s002030000192, 11081789.
55. Singer M, Lindquist S. Multiple effects of trehalose on protein folding in vitro and in vivo. Mol Cell 1998, 1(5):639-648. 10.1016/S1097-2765(00)80064-7, 9660948.
56. Chen Q, Ma E, Behar K, Xu T, Haddad G. Role of trehalose phosphate synthase in anoxia tolerance and development in Drosophila melanogaster. J Biol Chem 2002, 277(5):3274-3279. 10.1074/jbc.M109479200, 11719513.
57. Cleves A, Cooper D, Barondes S, Kelly R. A new pathway for protein export in Saccharomyces cerevisiae. J Cell Biol 1996, 133(5):1017-1026. 10.1083/jcb.133.5.1017, 2120850, 8655575.
58. Esposito RE, Klapholz S. Meiosis and ascospore development. The Molecular Biology of the Yeast Saccharomyces Life Cycle and Inheritance 1981, 211-287. Cold Spring Harbor, NY, Strathern JN, Jones EW, Broach JR.
59. Neiman A. Ascospore formation in the yeast Saccharomyces cerevisiae. Microbiol Mol Biol Rev 2005, 69(4):565-584. 10.1128/MMBR.69.4.565-584.2005, 1306807, 16339736.
60. Coleman ST, Fang TK, Rovinsky SA, Turano FJ, Moye-Rowley WS. Expression of a glutamate decarboxylase homologue is required for normal oxidative stress tolerance in Saccharomyces cerevisiae. J Biol Chem 2001, 276(1):244-250.
61. Jang HH, Lee KO, Chi YH, Jung BG, Park SK, Park JH, Lee JR, Lee SS, Moon JC, Yun JW, et al. Two enzymes in one; two yeast peroxiredoxins display oxidative stress-dependent switching from a peroxidase to a molecular chaperone function. Cell 2004, 117(5):625-635. 10.1016/j.cell.2004.05.002, 15163410.
62. Trotter EW, Rand JD, Vickerstaff J, Grant CM. The yeast Tsa1 peroxiredoxin is a ribosome-associated antioxidant. Biochem J 2008, 412(1):73-80. 10.1042/BJ20071634, 18271751.
63. Schröder M, Kaufman R. ER stress and the unfolded protein response. Mutat Res 2005, 569(1-2):29-63.
64. Cox J, Chapman R, Walter P. The unfolded protein response coordinates the production of endoplasmic reticulum protein and endoplasmic reticulum membrane. Mol Biol Cell 1997, 8(9):1805-1814. 305738, 9307975.
65. Frand A, Kaiser C. The ERO1 gene of yeast is required for oxidation of protein dithiols in the endoplasmic reticulum. Mol Cell 1998, 1(2):161-170. 10.1016/S1097-2765(00)80017-9, 9659913.
66. Caspi R, Altman T, Dale JM, Dreher K, Fulcher CA, Gilham F, Kaipa P, Karthikeyan AS, Kothari A, Krummenacker M, et al. The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res 2010, 38(Database issue):D473-479. 2808959, 19850718.