Quantitative iTRAQ LC-MS/MS proteomics reveals the cellular response to heterologous protein overexpression and the regulation of HAC1 in Pichia pastoris

Journal of Proteomics

Volumn 91, Issue , 2013, Pages 58-72

  Lin, Xiao Qiong ^a   Liang, Shu Li ^a   Han, Shuang Yan ^a   Zheng, Sui Ping ^a   Ye, Yan Rui ^a   Lin, Ying ^a  

^a SOUTH CHINA UNIVERSITY OF TECHNOLOGY   (China)

Author keywords

HAC1; ITRAQ; Pichia pastoris; Unfolded protein response (UPR); Xylanase

Indexed keywords

UNCLASSIFIED DRUG; XYLAN ENDO 1,3 BETA XYLOSIDASE; XYLANASE A;

AMINO ACID METABOLISM; ARTICLE; BACILLUS; BACILLUS HALODURANS; BACTERIUM CULTURE; CARBON METABOLISM; CELL VACUOLE; CONTROLLED STUDY; DATA ANALYSIS; ENDOPLASMIC RETICULUM; GENE DOSAGE; GENE OVEREXPRESSION; GLYCOLYSIS; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; PENTOSE PHOSPHATE CYCLE; PICHIA PASTORIS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; PROTEIN TARGETING; PROTEIN TRANSPORT; PROTEOMICS; RIBOSOME; TANDEM MASS SPECTROMETRY; TRANSLATION INITIATION; UNFOLDED PROTEIN RESPONSE; UPREGULATION;

HAC1; ITRAQ; PICHIA PASTORIS; UNFOLDED PROTEIN RESPONSE (UPR); XYLANASE;

BACILLUS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CITRIC ACID CYCLE; ENDO-1,4-BETA XYLANASES; ENDOPLASMIC RETICULUM; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; GLYCOLYSIS; MOLECULAR CHAPERONES; PENTOSE PHOSPHATE PATHWAY; PICHIA; PROTEIN FOLDING; PROTEOME; PROTEOMICS; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TANDEM MASS SPECTROMETRY; TRANSCRIPTION FACTORS; UNFOLDED PROTEIN RESPONSE;

EID: 84881273430     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2013.06.031     Document Type: Article

References (73)

1. Gellissen G. Heterologous protein production in methylotrophic yeasts. Appl Microbiol Biotechnol 2000, 54:741-750.
2. Daly R., Hearn M.T. Expression of heterologous proteins in Pichia pastoris: a useful experimental tool in protein engineering and production. J Mol Recognit 2004, 18:119-138.
3. Demain A.L., Adrio J.L. Strain improvement for production of pharmaceuticals and other microbial metabolites by fermentation. Prog Drug Res 2008, 18:251-289.
4. De Schutter K., Lin Y.-C., Tiels P., Van Hecke A., Glinka S., Weber-Lehmann J., et al. Genome sequence of the recombinant protein production host Pichia pastoris. Nat Biotechnol 2009, 27:561-566.
5. Mattanovich D., Callewaert N., Rouzé P., Lin Y.-C., Graf A., Redl A., et al. Open access to sequence: browsing the Pichia pastoris genome. Microb Cell Fact 2009, 8:53.
6. Demain A.L., Vaishnav P. Production of recombinant proteins by microbes and higher organisms. Biotechnol Adv 2009, 27:297-306.
7. Damasceno L.M., Huang C.-J., Batt C.A. Protein secretion in Pichia pastoris and advances in protein production. Appl Microbiol Biotechnol 2012, 93:1-9.
8. Zhu T., Guo M., Tang Z., Zhang M., Zhuang Y., Chu J., et al. Efficient generation of multi-copy strains for optimizing secretory expression of porcine insulin precursor in yeast Pichia pastoris. J Appl Microbiol 2009, 107:954-963.
9. Marx H., Mecklenbräuker A., Gasser B., Sauer M., Mattanovich D. Directed gene copy number amplification in Pichia pastoris by vector integration into the ribosomal DNA locus. FEMS Yeast Res 2009, 9:1260-1270.
10. Zhu T., Guo M., Zhuang Y., Chu J., Zhang S. Understanding the effect of foreign gene dosage on the physiology of Pichia pastoris by transcriptional analysis of key genes. Appl Microbiol Biotechnol 2011, 89:1127-1135.
11. Hohenblum H., Borth N., Mattanovich D. Assessing viability and cell-associated product of recombinant protein producing Pichia pastoris with flow cytometry. J Biotechnol 2003, 102:281-290.
12. Vassileva A., Arora Chugh D., Swaminathan S., Khanna N. Effect of copy number on the expression levels of Hepatitis B surface antigen in the methylotrophic yeat Pichia pastoris. Protein Expr Purif 2001, 21:71-80.
13. Cudna R.E., Dickson A.J. Endoplasmic reticulum signaling as a determinant of recombinant protein expression. Biotechnol Bioeng 2003, 81:56-65.
14. Kauffman K.J., Pridgen E.M., Doyle F.J., Dhurjati P.S., Robinson A.S. Decreased protein expression and intermittent recoveries in BiP levels result from cellular stress during heterologous protein expression in Saccharomyces cerevisiae. Biotechnol Prog 2002, 18:942-950.
15. Damasceno L.M., Anderson K.A., Ritter G., Cregg J.M., Old L.J., Batt C.A. Cooverexpression of chaperones for enhanced secretion of a single-chain antibody fragment in Pichia pastoris. Appl Microbiol Biotechnol 2007, 74:381-389.
16. Inan M., Aryasomayajula D., Sinha J., Meagher M.M. Enhancement of protein secretion in Pichia pastoris by overexpression of protein disulfide isomerase. Biotechnol Bioeng 2006, 93:771-778.
17. Zhang W., Hl Zhao, Xue C., Xh Xiong, Xq Yao, Xy Li, et al. Enhanced secretion of heterologous proteins in Pichia pastoris following overexpression of Saccharomyces cerevisiae chaperone proteins. Biotechnol Prog 2008, 22:1090-1095.
18. Guerfal M., Ryckaert S., Jacobs P.P., Ameloot P., Van Craenenbroeck K., Derycke R., et al. The HAC1 gene from Pichia pastoris: characterization and effect of its overexpression on the production of secreted, surface displayed and membrane proteins. Microb Cell Fact 2010, 9:49.
19. Vanz A.L., Lünsdorf H., Adnan A., Nimtz M., Gurramkonda C., Khanna N., et al. Physiological response of Pichia pastoris GS115 to methanol-induced high level production of the Hepatitis B surface antigen: catabolic adaptation, stress responses, and autophagic processes. Microb Cell Fact 2012, 11:103.
20. Graf A., Gasser B., Dragosits M., Sauer M., Leparc G.G., Tüchler T., et al. Novel insights into the unfolded protein response using Pichia pastoris specific DNA microarrays. BMC Genomics 2008, 9:390.
21. Gasser B., Maurer M., Rautio J., Sauer M., Bhattacharyya A., Saloheimo M., et al. Monitoring of transcriptional regulation in Pichia pastoris under protein production conditions. BMC Genomics 2007, 8:179.
22. Whyteside G., Nor R.M., Alcocer M.J., Archer D.B. Activation of the unfolded protein response in Pichia pastoris requires splicing of a HAC1 mRNA intron and retention of the C-terminal tail of Hac1p. FEBS Lett 2011, 585:1037-1041.
23. Travers K.J., Patil C.K., Wodicka L., Lockhart D.J., Weissman J.S., Walter P. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 2000, 101:249-258.
24. Dragosits M., Stadlmann J., Graf A., Gasser B., Maurer M., Sauer M., et al. The response to unfolded protein is involved in osmotolerance of Pichia pastoris. BMC Genomics 2010, 11:207.
25. Moritz B., Meyer H.E. Approaches for the quantification of protein concentration ratios. Proteomics 2003, 3:2208-2220.
26. Pütz S.M., Boehm A.M., Stiewe T., Sickmann A. iTRAQ analysis of a cell culture model for malignant transformation, including comparison with 2D-PAGE and SILAC. J Proteome Res 2012, 11:2140-2153.
27. Maillet I., Lagniel G., Perrot M., Boucherie H., Labarre J. Rapid identification of yeast proteins on two-dimensional gels. J Biol Chem 1996, 271:10263-10270.
28. Dragosits M., Stadlmann J., Albiol J., Baumann K., Maurer M., Gasser B., et al. The effect of temperature on the proteome of recombinant Pichia pastoris. J Proteome Res 2009, 8:1380-1392.
29. Rossignol T., Kobi D., Jacquet-Gutfreund L., Blondin B. The proteome of a wine yeast strain during fermentation, correlation with the transcriptome. J Appl Microbiol 2009, 107:47-55.
30. Brejning J., Arneborg N., Jespersen L. Identification of genes and proteins induced during the lag and early exponential phase of lager brewing yeasts. J Appl Microbiol 2004, 98:261-271.
31. Pfeffer M., Maurer M., Stadlmann J., Grass J., Delic M., Altmann F., et al. Intracellular interactome of secreted antibody Fab fragment in Pichia pastoris reveals its routes of secretion and degradation. Appl Microbiol Biotechnol 2012, 1-10.
32. Cellulaire B. Two-dimensional gel electrophoresis in proteomics: old, old fashioned, but it still climbs up the mountains. Proteomics 2002, 2:3-10.
33. Mann M., Hendrickson R.C., Pandey A. Analysis of proteins and proteomes by mass spectrometry. Annu Rev Biochem 2001, 70:437-473.
34. de Godoy L.M., Olsen J.V., Cox J., Nielsen M.L., Hubner N.C., Fröhlich F., et al. Comprehensive mass-spectrometry-based proteome quantification of haploid versus diploid yeast. Nature 2008, 455:1251-1254.
35. Rossouw D., van den Dool A.H., Jacobson D., Bauer F.F. Comparative transcriptomic and proteomic profiling of industrial wine yeast strains. Appl Environ Microbiol 2010, 76:3911-3923.
36. Lin X.-q., Han S.-y., Zhang N., Hu H., Zheng S.-p., Ye Y.-r., et al. Bleach boosting effect of xylanase A from Bacillus halodurans C-125 in ECF bleaching of wheat straw pulp. Enzyme Microb Technol 2012, 52:91-98.
37. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J Biol Chem 1951, 193:265-275.
38. Qiao J., Wang J., Chen L., Tian X., Huang S., Ren X., et al. Quantitative iTRAQ LC-MS/MS proteomics reveals metabolic responses to biofuel ethanol in cyanobacterial Synechocystis sp. PCC 6803. J Proteome Res 2012, 11:5286-5300.
39. Gan C.S., Chong P.K., Pham T.K., Wright P.C. Technical, experimental, and biological variations in isobaric tags for relative and absolute quantitation (iTRAQ). J Proteome Res 2007, 6:821-827.
40. Unwin R.D., Griffiths J.R., Whetton A.D. Simultaneous analysis of relative protein expression levels across multiple samples using iTRAQ isobaric tags with 2D nano LC-MS/MS. Nat Protoc 2010, 5:1574-1582.
41. Tian X., Chen L., Wang J., Qiao J., Zhang W. Quantitative proteomics reveals dynamic responses of Synechocystis sp. PCC 6803 to next-generation biofuel butanol. J Proteomics 2012, 78:326-345.
42. Charbonneau M.-È., Girard V., Nikolakakis A., Campos M., Berthiaume F., Dumas F., et al. O-linked glycosylation ensures the normal conformation of the autotransporter adhesin involved in diffuse adherence. J Bacteriol 2007, 189:8880-8889.
43. Wu J., Mao X., Cai T., Luo J., Wei L. KOBAS server: a web-based platform for automated annotation and pathway identification. Nucleic Acids Res 2006, 34:W720-W724.
44. Köhrer K., Domdey H. Preparation of high molecular weight RNA. Methods Enzymol 1991, 194:398-405.
45. -δδCT method. Methods 2001, 25:402-408.
46. Cox J.S., Shamu C.E., Walter P. Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 1993, 73:1197-1206.
47. Kawahara T., Yanagi H., Yura T., Mori K. Endoplasmic reticulum stress-induced mRNA splicing permits synthesis of transcription factor Hac1p/Ern4p that activates the unfolded protein response. Mol Biol Cell 1997, 8:1845-1862.
48. Gasser B., Maurer M., Gach J., Kunert R., Mattanovich D. Engineering of Pichia pastoris for improved production of antibody fragments. Biotechnol Bioeng 2006, 94:353-361.
49. Valkonen M., Penttilä M., Saloheimo M. Effects of inactivation and constitutive expression of the unfolded-protein response pathway on protein production in the yeast Saccharomyces cerevisiae. Appl Environ Microbiol 2003, 69:2065-2072.
50. Champion M.M., Campbell C.S., Siegele D.A., Russell D.H., Hu J.C. Proteome analysis of Escherichia coli K-12 by two-dimensional native-state chromatography and MALDI-MS. Mol Microbiol 2003, 47:383-396.
51. Zhang W., Gritsenko M.A., Moore R.J., Culley D.E., Nie L., Petritis K., et al. A proteomic view of Desulfovibrio vulgaris metabolism as determined by liquid chromatography coupled with tandem mass spectrometry. Proteomics 2006, 6:4286-4299.
52. Feldman D.E., Frydman J. Protein folding in vivo: the importance of molecular chaperones. Curr Opin Struct Biol 2000, 10:26-33.
53. Hattendorf D.A., Andreeva A., Gangar A., Brennwald P.J., Weis W.I. Structure of the yeast polarity protein Sro7 reveals a SNARE regulatory mechanism. Nature 2007, 446:567-571.
54. Govindan B., Bowser R., Novick P. The role of Myo2, a yeast class V myosin, in vesicular transport. J Cell Biol 1995, 128:1055-1068.
55. Sata M., Donaldson J.G., Moss J., Vaughan M. Brefeldin A-inhibited guanine nucleotide-exchange activity of Sec7 domain from yeast Sec7 with yeast and mammalian ADP ribosylation factors. Proc Nati Acad Sci 1998, 95:4204-4208.
56. Tibbetts A.S., Sun Y., Lyon N.A., Ghrist A.C., Trotter P.J. Yeast mitochondrial oxodicarboxylate transporters are important for growth on oleic acid. Arch Biochem Biophys 2002, 406:96-104.
57. Bieganowski P., Seidle H.F., Wojcik M., Brenner C. Synthetic lethal and biochemical analyses of NAD and NADH kinases in Saccharomyces cerevisiae establish separation of cellular functions. J Biol Chem 2006, 281:22439-22445.
58. Lange A., Mills R.E., Lange C.J., Stewart M., Devine S.E., Corbett A.H. Classical nuclear localization signals: definition, function, and interaction with importin α. J Biol Chem 2007, 282:5101-5105.
59. 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, 73:6499-6507.
60. Payne T., Hanfrey C., Bishop A.L., Michael A.J., Avery S.V., Archer D.B. Transcript-specific translational regulation in the unfolded protein response of Saccharomyces cerevisiae. FEBS Lett 2008, 582:503-509.
61. Steffen K.K., McCormick M.A., Pham K.M., MacKay V.L., Delaney J.R., Murakami C.J., et al. Ribosome deficiency protects against ER stress in Saccharomyces cerevisiae. Genetics 2012, 191:107-118.
62. Schröder M., Chang J.S., Kaufman R.J. The unfolded protein response represses nitrogen-starvation induced developmental differentiation in yeast. Genes Dev 2000, 14:2962-2975.
63. Schröder M., Kaufman R.J. The mammalian unfolded protein response. Annu Rev Biochem 2005, 74:739-789.
64. Ron D., Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007, 8:519-529.
65. Kim H.M., Yu Y., Cheng Y. Structure characterization of the 26S proteasome. Biochim Biophys Acta 1809, 2011:67-79.
66. Picard D. Heat-shock protein 90, a chaperone for folding and regulation. Cell Mol Life Sci 2002, 59:1640-1648.
67. Goswami A.V., Chittoor B., D'Silva P. Understanding the functional interplay between mammalian mitochondrial Hsp70 chaperone machine components. J Biol Chem 2010, 285:19472-19482.
68. Hartner F.S., Glieder A. Regulation of methanol utilisation pathway genes in yeasts. Microb Cell Fact 2006, 5:39.
69. Cos O., Serrano A., Montesinos J.L., Ferrer P., Cregg J.M., Valero F. Combined effect of the methanol utilization (Mut) phenotype and gene dosage on recombinant protein production in Pichia pastoris fed-batch cultures. J Biotechnol 2005, 116:321-335.
70. Hohenblum H., Gasser B., Maurer M., Borth N., Mattanovich D. Effects of gene dosage, promoters, and substrates on unfolded protein stress of recombinant Pichia pastoris. Biotechnol Bioeng 2004, 85:367-375.
71. Yano T., Takigami E., Yurimoto H., Sakai Y. Yap1-regulated glutathione redox system curtails accumulation of formaldehyde and reactive oxygen species in methanol metabolism of Pichia pastoris. Eukaryot Cell 2009, 8:540-549.
72. Yurimoto H., Kato N., Sakai Y. Assimilation, dissimilation, and detoxification of formaldehyde, a central metabolic intermediate of methylotrophic metabolism. Chem Rec 2005, 5:367-375.
73. Costenoble R., Picotti P., Reiter L., Stallmach R., Heinemann M., Sauer U., et al. Comprehensive quantitative analysis of central carbon and amino-acid metabolism in Saccharomyces cerevisiae under multiple conditions by targeted proteomics. Mol Syst Biol 2011, 7.