Absence of Yps7p, a putative glycosylphosphatidylinositol-linked aspartyl protease in Pichia pastoris, results in aberrant cell wall composition and increased osmotic stress resistance

FEMS Yeast Research

Volumn 12, Issue 8, 2012, Pages 969-979

  Guan, Bo ^a   Lei, Jianyong ^a   Su, Shuai ^a   Chen, Fengxiang ^a   Duan, Zuoying ^a   Chen, Yun ^a,b   Gong, Xiaohai ^a,b   Li, Huazhong ^a   Jin, Jian ^a,b  

^a JIANGNAN UNIVERSITY   (China)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

Cell wall integrity; Chitin; Glycosylphosphatidylinositol linked aspartyl protease; Osmotic stress; Pichia pastoris; Yps7

Indexed keywords

ASPARTIC PROTEINASE; BETA 1,3 GLUCAN; CALCOFLUOR WHITE; CHITIN; CONGO RED; DODECYL SULFATE SODIUM; FUNGAL PROTEIN; GLYCEROL; GLYCOSYLPHOSPHATIDYLINOSITOL; MKC7 PROTEIN; REAGENT; UNCLASSIFIED DRUG; YPS1 PROTEIN; YPS2 PROTEIN; YPS3 PROTEIN; YPS7 PROTEIN; YPS7P PROTEIN;

ANIMAL CELL; ARTICLE; CELL WALL; CONTROLLED STUDY; CROSS LINKING; FUNGAL CELL; FUNGAL GENE; FUNGAL STRAIN; FUNGUS CULTURE; GENE DISRUPTION; GENE EXPRESSION; MUTANT; NONHUMAN; OSMOTIC STRESS; PICHIA PASTORIS; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; TRANSMISSION ELECTRON MICROSCOPY;

ASPARTIC ACID PROTEASES; BETA-GLUCANS; CELL WALL; CHITIN; COMPUTATIONAL BIOLOGY; FUNGAL PROTEINS; GLYCOSYLPHOSPHATIDYLINOSITOLS; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; MUTATION; OSMOSIS; PHENOTYPE; PICHIA; PLASMIDS; STRESS, PHYSIOLOGICAL;

CANDIDA ALBICANS; PICHIA PASTORIS; SACCHAROMYCES CEREVISIAE;

EID: 84868661661     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1111/1567-1364.12002     Document Type: Article

References (41)

1. Alonso-Monge R, Navarro-Garcia F, Molero G, Diez-Orejas R, Gustin M, Pla J, Sanchez M & Nombela C (1999) Role of the mitogen-activated protein kinase Hog1p in morphogenesis and virulence of Candida albicans. J Bacteriol 181: 3058-3068.
2. Azaryan AV, Wong M, Friedman TC, Cawley NX, Estivariz FE, Chen HC & Loh YP (1993) Purification and characterization of a paired basic residue-specific yeast aspartic protease encoded by the YAP3 gene. Similarity to the mammalian pro-opiomelanocortin-converting enzyme. J Biol Chem 268: 11968-11975.
3. Bulawa CE (1992) CSD2, CSD3, and CSD4, genes required for chitin synthesis in Saccharomyces cerevisiae: the CSD2 gene product is related to chitin synthases and to developmentally regulated proteins in Rhizobium species and Xenopus laevis. Mol Cell Biol 12: 1764-1776.
4. Bulawa CE, Slater M, Cabib E, Au-Young J, Sburlati A, Adair WL Jr & Robbins PW (1986) The S. cerevisiae structural gene for chitin synthase is not required for chitin synthesis in vivo. Cell 46: 213-225.
5. Carotti C, Ferrario L, Roncero C, Valdivieso MH, Duran A & Popolo L (2002) Maintenance of cell integrity in the gas1 mutant of Saccharomyces cerevisiae requires the Chs3p-targeting and activation pathway and involves an unusual Chs3p localization. Yeast 19: 1113-1124.
6. Cho EY, Cheon SA, Kim H, Choo J, Lee DJ, Ryu HM, Rhee SK, Chung BH, Kim JY & Kang HA (2010) Multiple-yapsin-deficient mutant strains for high-level production of intact recombinant proteins in Saccharomyces cerevisiae. J Biotechnol 149: 1-7.
7. De Schutter K, Lin YC, Tiels P, Van Hecke A, Glinka S, Weber-Lehmann J, Rouze P, Van de Peer Y & Callewaert N (2009) Genome sequence of the recombinant protein production host Pichia pastoris. Nat Biotechnol 27: 561-566.
8. Egel-Mitani M, Flygenring HP & Hansen MT (1990) A novel aspartyl protease allowing KEX2-independent MF alpha propheromone processing in yeast. Yeast 6: 127-137.
9. 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.
10. Gagnon-Arsenault I, Tremblay J & Bourbonnais Y (2006) Fungal yapsins and cell wall: a unique family of aspartic peptidases for a distinctive cellular function. FEMS Yeast Res 6: 966-978.
11. Ganatra MB, Vainauskas S, Hong JM et al. (2011) A set of aspartyl protease-defcient strains for improved expression of heterologous proteins in Kluyveromyces lactis. FEMS Yeast Res 11: 168-178.
12. Garcia-Rodriguez LJ, Duran A & Roncero C (2000) Calcofluor antifungal action depends on chitin and a functional high-osmolarity glycerol response (HOG) pathway: evidence for a physiological role of the Saccharomyces cerevisiae HOG pathway under noninducing conditions. J Bacteriol 182: 2428-2437.
13. Imai K, Noda Y, Adachi H & Yoda K (2005) A novel endoplasmic reticulum membrane protein Rcr1 regulates chitin deposition in the cell wall of Saccharomyces cerevisiae. J Biol Chem 280: 8275-8284.
14. Kaeberlein M & Guarente L (2002) Saccharomyces cerevisiae MPT5 and SSD1 function in parallel pathways to promote cell wall integrity. Genetics 160: 83-95.
15. Kaur R, Ma B & Cormack BP (2007) A family of glycosylphosphatidylinositol-linked aspartyl proteases is required for virulence of Candida glabrata. P Natl Acad Sci U S A 104: 7628-7633.
16. Kerry-Williams SM, Gilbert SC, Evans LR & Ballance DJ (1998) Disruption of the Saccharomyces cerevisiae YAP3 gene reduces the proteolytic degradation of secreted recombinant human albumin. Yeast 14: 161-169.
17. Klis FM, Mol P, Hellingwerf K & Brul S (2002) Dynamics of cell wall structure in Saccharomyces cerevisiae. FEMS Microbiol Rev 26: 239-256.
18. Klis FM, Boorsma A & De Groot PW (2006) Cell wall construction in Saccharomyces cerevisiae. Yeast 23: 185-202.
19. Krysan DJ, Ting EL, Abeijon C, Kroos L & Fuller RS (2005) Yapsins are a family of aspartyl proteases required for cell wall integrity in Saccharomyces cerevisiae. Eukaryot Cell 4: 1364-1374.
20. Latge JP (2007) The cell wall: a carbohydrate armour for the fungal cell. Mol Microbiol 66: 279-290.
21. Lesage G & Bussey H (2006) Cell wall assembly in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 70: 317-343.
22. Lesage G, Shapiro J, Specht CA, Sdicu AM, Menard P, Hussein S, Tong AH, Boone C & Bussey H (2005) An interactional network of genes involved in chitin synthesis in Saccharomyces cerevisiae. BMC Genet 6: 8.
23. Levin DE (2005) Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 69: 262-291.
24. Martin H, Dagkessamanskaia A, Satchanska G, Dallies N & Francois J (1999) KNR4, a suppressor of Saccharomyces cerevisiae cwh mutants, is involved in the transcriptional control of chitin synthase genes. Microbiology 145(Pt 1): 249-258.
25. Moreno-Ruiz E, Ortu G, de Groot PW, Cottier F, Loussert C, Prevost MC, de Koster C, Klis FM, Goyard S & d'Enfert C (2009) The GPI-modified proteins Pga59 and Pga62 of Candida albicans are required for cell wall integrity. Microbiology 155(Pt 6): 2004-2020.
26. Osumi M (1998) The ultrastructure of yeast: cell wall structure and formation. Micron 29: 207-233.
27. Pan R, Zhang J, Shen WL, Tao ZQ, Li SP & Yan X (2011) Sequential deletion of Pichia pastoris genes by a self-excisable cassette. FEMS Yeast Res 11: 292-298.
28. Pittet M & Conzelmann A (2007) Biosynthesis and function of GPI proteins in the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 1771: 405-420.
29. Pringle JR (1991) Staining of bud scars and other cell wall chitin with calcofluor. Methods Enzymol 194: 732-735.
30. Ram AF, Kapteyn JC, Montijn RC, Caro LH, Douwes JE, Baginsky W, Mazur P, van den Ende H & Klis FM (1998) Loss of the plasma membrane-bound protein Gas1p in Saccharomyces cerevisiae results in the release of beta1, 3-glucan into the medium and induces a compensation mechanism to ensure cell wall integrity. J Bacteriol 180: 1418-1424.
31. Reissig JL, Storminger JL & Leloir LF (1955) A modified colorimetric method for the estimation of N-acetylamino sugars. J Biol Chem 217: 959-966.
32. Roncero C & Duran A (1985) Effect of Calcofluor white and Congo red on fungal cell wall morphogenesis: in vivo activation of chitin polymerization. J Bacteriol 163: 1180-1185.
33. Sekiya-Kawasaki M, Abe M, Saka A, Watanabe D, Kono K, Minemura-Asakawa M, Ishihara S, Watanabe T & Ohya Y (2002) Dissection of upstream regulatory components of the Rho1p effector, 1, 3-beta-glucan synthase, in Saccharomyces cerevisiae. Genetics 162: 663-676.
34. Shevchuk NA, Bryksin AV, Nusinovich YA, Cabello FC, Sutherland M & Ladisch S (2004) Construction of long DNA molecules using long PCR-based fusion of several fragments simultaneously. Nucleic Acids Res 32: e19.
35. Tamás MJ & Hohmann S (2003) The osmotic stress response of Saccharomyces cerevisiae. Top Curr Genet 1: 121-200.
36. Thomas JR, Dwek RA & Rademacher TW (1990) Structure, biosynthesis, and function of glycosylphosphatidylinositols. Biochemistry 29: 5413-5422.
37. Trilla JA, Duran A & Roncero C (1999) Chs7p, a new protein involved in the control of protein export from the endoplasmic reticulum that is specifically engaged in the regulation of chitin synthesis in Saccharomyces cerevisiae. J Cell Biol 145: 1153-1163.
38. Vadaie N, Dionne H, Akajagbor DS, Nickerson SR, Krysan DJ & Cullen PJ (2008) Cleavage of the signaling mucin Msb2 by the aspartyl protease Yps1 is required for MAPK activation in yeast. J Cell Biol 181: 1073-1081.
39. Werten MW & de Wolf FA (2005) Reduced proteolysis of secreted gelatin and Yps1-mediated alpha-factor leader processing in a Pichia pastoris kex2 disruptant. Appl Environ Microbiol 71: 2310-2317.
40. Wojda I, Alonso-Monge R, Bebelman JP, Mager WH & Siderius M (2003) Response to high osmotic conditions and elevated temperature in Saccharomyces cerevisiae is controlled by intracellular glycerol and involves coordinate activity of MAP kinase pathways. Microbiology 149(Pt 5): 1193-1204.
41. Yao XQ, Zhao HL, Xue C, Zhang W, Xiong XH, Wang ZW, Li XY & Liu ZM (2009) Degradation of HSA-AX15 (R13K) when expressed in Pichia pastoris can be reduced via the disruption of YPS1 gene in this yeast. J Biotechnol 139: 131-136.