Saccharomyces cerevisiae proteinase A excretion and wine making

Song, Lulu; Chen, Yefu; Du, Yongjing; Wang, Xibin; Guo, Xuewu; Dong, Jian; Xiao, Dongguang

doi:10.1007/s11274-017-2361-z

Review
Published: 09 November 2017

Saccharomyces cerevisiae proteinase A excretion and wine making

Lulu Song¹,
Yefu Chen¹,
Yongjing Du¹,
Xibin Wang¹,
Xuewu Guo¹,
Jian Dong¹ &
Dongguang Xiao¹

World Journal of Microbiology and Biotechnology volume 33, Article number: 210 (2017) Cite this article

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Abstract

Proteinase A (PrA), the major protease in Saccharomyces cerevisiae, plays an essential role in zymogen activation, sporulation, and other physiological processes in vivo. The extracellular secretion of PrA often occurs during alcoholic fermentation, especially in the later stages when the yeast cells are under stress conditions, and affects the quality and safety of fermented products. Thus, the mechanism underlying PrA excretion must be explored to improve the quality and safety of fermented products. This paper briefly introduces the structure and physiological function of PrA. Two transport routes of PrA, namely, the Golgi-to-vacuole pathway and the constitutive Golgi-to-plasma membrane pathway, are also discussed. Moreover, the research history and developments on the mechanism of extracellular PrA secretion are described. In addition, it is briefly discussed that calcium homeostasis plays an important role in the secretory pathway of proteins, implying that the regulation of PrA delivery to the plasma membrane requires the involvement of calcium ion. Finally, this review focuses on the effects of PrA excretion on wine making (including Chinese rice wine, grape wine, and beer brewage) and presents strategies to control PrA excretion.

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References

Abeijon C, Orlean P, Robbins PW et al (1989) Topography of glycosylation in yeast: characterization of GDPmannose transport and lumenal guanosine diphosphatase activities in Golgi-like vesicles. Proc Nat Acad Sci USA 86:6935–6939. doi:10.1073/pnas.86.18.6935
CAS Article Google Scholar
Aguilar CF, Cronin NB, Badasso M et al (1997) The three-dimensional structure at 2.4 Å resolution of glycosylated proteinase a from the lysosome-like vacuole of Saccharomyces cerevisiae. J Mol Biol 267:899–915. doi:10.1006/jmbi.1996.0880
CAS Article Google Scholar
Ammerer G, Hunter CP, Rothman JH et al (1986) PEP4 gene of Saccharomyces cerevisiae encodes proteinase A, a vacuolar enzyme required for processing of vacuolar precursors. Mol Cell Biol 6:2490–2499. doi:10.1128/MCB.6.7.2490
CAS Article Google Scholar
Antebi A, Fink GR (1992) The yeast Ca(2+)-ATPase homologue, PMR1, is required for normal Golgi function and localizes in a novel Golgi-like distribution. Mol Biol Cell 3:633. doi:10.1091/mbc.3.6.633
CAS Article Google Scholar
Baranski TJ, Faust PL, Kornfeld S (1990) Generation of a lysosomal enzyme targeting signal in the secretory protein pepsinogen. Cell 63:281–129. doi:10.1016/0092-8674(90)90161-7
CAS Article Google Scholar
Barlowe CK, Miller EA (2013) Secretory protein biogenesis and traffic in the early secretory pathway. Genetics 193:383–410. doi:10.1534/genetics.112.142810
CAS Article Google Scholar
Benli M, Döring F, Robinson DG et al (1996) Two GTPase isoforms, Ypt31p and Ypt32p, are essential for Golgi function in yeast. EMBO J 15:6460–6475
CAS Google Scholar
Bonifacino JS, Glick BS (2004) The mechanisms of vesicle budding and fusion. Cell 116:153–166. doi:10.1016/S0092-8674(03)01079-1
CAS Article Google Scholar
Booth C, Koch GL (1989) Perturbation of cellular calcium induces secretion of luminal ER proteins. Cell 59(4):729–737. doi:10.1016/0092-8674(89)90019-6
CAS Article Google Scholar
Brion C, Miller SG, Moore HP (1992) Regulated and constitutive secretion. Differential effects of protein synthesis arrest on transport of glycosaminoglycan chains to the two secretory pathways. J Biol Chem 267:1477–1483
CAS Google Scholar
Bröcker C, Engelbrecht-Vandré S, Ungermann C (2010) Multisubunit tethering complexes and their role in membrane fusion. Curr Biol Cb 20:943–952. doi:10.1016/j.cub.2010.09.015
Article CAS Google Scholar
Bruno SNF, Vaitsman DS, Kunigami CN et al (2007) Influence of the distillation processes from rio de janeiro in the ethyl carbamate formation in brazilian sugar cane spirits. Food Chem 104:1345–1352. doi:10.1016/j.foodchem.2007.01.048
CAS Article Google Scholar
Burgess TL, Kelly RB (1987) Constitutive and regulated secretion of proteins. Ann Rev Cell Biol 3:243–293. doi:10.1146/annurev.cb.03.110187.001331
CAS Article Google Scholar
Chen S, Xu Y (2010) The influence of yeast strains on the volatile flavour compounds of chinese rice wine. J Inst Brew 116:190–196. doi:10.1002/j.2050-0416.2010.tb00417.x
CAS Article Google Scholar
Chen QH, Liu XJ, Fu ML et al (2010) Effect of PrA encoding gene-PEP4 deletion in industrial S. cerevisiae wz65 on key enzymes in relation to the glycolytic pathway. Eur Food Res Technol 231:943–950. doi:10.1007/s00217-010-1355-y
CAS Article Google Scholar
Chen Y, Song L, Han Y et al (2017) Decreased proteinase a excretion by strengthening its vacuolar sorting and weakening its constitutive secretion in Saccharomyces cerevisiae. J Ind Microbiol Biotechnol 44:149–159. doi:10.1007/s10295-016-1868-x
CAS Article Google Scholar
Cooper AA, Stevens TH (1996) Vps10p cycles between the late-golgi and prevacuolar compartments in its function as the sorting receptor for multiple yeast vacuolar hydrolases. J Cell Biol 133:529–541. doi:10.1083/jcb.133.3.529
CAS Article Google Scholar
Cooper DJ, Stewart GG, Bryce JH (2000) Yeast proteolytic activity during high and low gravity wort fermentations and its effect on head retention. J Inst Brewtitute Brew 106:197–201. doi:10.1002/j.2050-0416.2000.tb00057.x
Article Google Scholar
Curwin AJ, von Blume J, Malhotra V (2012) Cofilin-mediated sorting and export of specific cargo from the Golgi apparatus in yeast. Mol Biol Cell 23:2327–2338. doi:10.1091/mbc.E11-09-0826
CAS Article Google Scholar
Dreyer T, Biedermann K, Ottesen M (1983) Yeast proteinase in beer. Carlsberg Res Commun 48:249. doi:10.1007/BF02907771
CAS Article Google Scholar
Dreyer T, Halkier B, Svendsen I et al (1986) Primary structure of the aspartic proteinase a from Saccharomyces cerevisiae. Carlsberg Res Commun 51:27–41. doi:10.1007/BF02907993
CAS Article Google Scholar
Dürr G, Strayle J, Plemper R et al (1998) The medial-Golgi ion pump Pmr1 supplies the yeast secretory pathway with Ca²⁺ and Mn²⁺ required for glycosylation, sorting, and endoplasmic reticulum-associated protein degradation. Mol Biol Cell 9:1149–1162. doi:10.1091/mbc.9.5.1149
Article Google Scholar
Fokina AV, Chechenova MB, Karginov AV et al (2015) Genetic evidence for the role of the vacuole in supplying secretory organelles with Ca²⁺ in Hansenula polymorpha. PLoS ONE 10:e0145915. doi:10.1371/journal.pone.0145915
Article CAS Google Scholar
Fuller RS, Brake A, Thorner J (1989) Yeast prohormone processing enzyme (KEX2 gene product) is a Ca²⁺-dependent serine protease. Proc Nat Acad Sci USA 86:1434. doi:10.1073/pnas.86.5.1434
CAS Article Google Scholar
Gibson BR, Lawrence SJ, Leclaire JP et al (2007) Yeast responses to stresses associated with industrial brewery handling. FEMS Microbiol Rev 31:535–569. doi:10.1111/j.1574-6976.2007.00076.x
CAS Article Google Scholar
Guo Y, Yang Y, Peng Q et al (2015a) Biogenic amines in wine: a review. Int J Food Sci Technol 50:1523–1532. doi:10.1111/ijfs.12833
CAS Article Google Scholar
Guo X, Guan X, Wang Y et al (2015b) Reduction of biogenic amines production by eliminating the PEP4 gene in Saccharomyces cerevisiae during fermentation of Chinese rice wine. Food Chem 178:208. doi:10.1016/j.foodchem.2015.01.089
CAS Article Google Scholar
Gustchina A, Li M, Phylip LH et al (2002) An unusual orientation for Tyr75 in the active site of the aspartic proteinase from Saccharomyces cerevisiae. Biochem Biophys Res Commun 295:1020–1026
CAS Article Google Scholar
Hansen RJ, Switzer RL, Hinze H et al (1977) Effects of glucose and nitrogen source on the levels of proteinases, peptidases, and proteinase inhibitors in yeast. Biochim Biophys Acta 496:103–114. doi:10.1016/0304-4165(77)90119-2
CAS Article Google Scholar
Hao J, Dong J, Speers R et al (2008) Construction of a single PEP4 allele deletion in saccharomyces carlsbergensis and a preliminary evaluation of its brewing performance. J Inst Brew 114:322–328. doi:10.1002/j.2050-0416.2008.tb00776.x
CAS Article Google Scholar
Hao X, Xiao DG, Zhang CY et al (2010) Influence of nutrients on proteinase a activity in draft beer during fermentation. Int J Food Sci Technol 45:1169–1174. doi:10.1111/j.1365-2621.2010.02252.x
CAS Article Google Scholar
Harris SD, Cotter DA (1987) Vacuolar (lysosomal) trehalase of Saccharomyces cerevisiae. Curr Microbiol 15:247–249. doi:10.1007/BF01589375
CAS Article Google Scholar
Hata T, Hayashi R, Doi E (1967) Purification of yeast proteinases: part III. Isolation and physicochemical properties of yeast proteinase A and C^*. Agr Biol Chern 31:357–367. doi:10.1271/bbb1961.31.150
Google Scholar
Hirsch HH, Schiffer HH, Wolf DH (1992) Biogenesis of the yeast vacuole (lysosome). Proteinase yscB contributes molecularly and kinetically to vacuolar hydrolase-precursor maturation. Eur J Biochem 207:867. doi:10.1111/j.1432-1033.1992.tb17118.x
CAS Article Google Scholar
Hong W, Lev S (2014) Tethering the assembly of SNARE complexes. Trends Cell Biol 24:35–43. doi:10.1016/j.tcb.2013.09.006
CAS Article Google Scholar
Jones EW (1984) The synthesis and function of proteases in saccharomyces: genetic approaches. Ann Rev Gene 18:233–270. doi:10.1146/annurev.ge.18.120184.001313
CAS Article Google Scholar
Jørgensen MU, Emr SD, Winther JR (1999) Ligand recognition and domain structure of Vps10p, a vacuolar protein sorting receptor in Saccharomyces cerevisiae. Eur J Biochem 260:461–469. doi:10.1046/j.1432-1327.1999.00176.x
Article Google Scholar
Kelly RB (1985) Pathways of protein secretion in eukaryotes. Science 230:25–32. doi:10.1126/science.2994224
CAS Article Google Scholar
Kienzle C, Von Blume J (2014) Secretory cargo sorting at the trans-Golgi network. Trends Cell Biol 24:584–593. doi:10.1016/j.tcb.2014.04.007
CAS Article Google Scholar
Klionsky DJ, Banta LM, Emr SD (1988) Intracellular sorting and processing of a yeast vacuolar hydrolase: proteinase a propeptide contains vacuolar targeting information. Mol Cell Biol 8:2105–2116. doi:10.1128/MCB.8.5.2105
CAS Article Google Scholar
Klionsky DJ, Cueva R, Yaver DS (1992) Aminopeptidase I of Saccharomyces cerevisiae is localized to the vacuole independent of the secretory pathway. J Cell Biol 119:287–299. doi:10.1083/jcb.119.2.287
CAS Article Google Scholar
Kondo H, Shibano Y, Amachi T et al (1998) Substrate specificities and kinetic properties of proteinase a from the yeast Saccharomyces cerevisiae and the development of a novel substrate. J Biochem 124:141–147. doi:10.1093/oxfordjournals.jbchem.a022072
CAS Article Google Scholar
Kondo H, Yomo H, Furukubo S et al (1999) Advanced method for measuring proteinase a in beer and application to brewing. J Inst Brew 105:293–300. doi:10.1002/j.2050-0416.1999.tb00523.x
CAS Article Google Scholar
Lachenmeier DW (2007) Consequences of IARC re-evaluation of alcoholic beverage consumption and ethyl carbamate on food control. Dtsch Lebensmitt Rundsch 103:307–311
CAS Google Scholar
Lee KG (2013) Analysis and risk assessment of ethyl carbamate in various fermented foods. Eur Food Res Technol 236:891–898. doi:10.1007/s00217-013-1953-6
CAS Article Google Scholar
Lee S, Yoo M, Shin D (2015) The identification and quantification of biogenic amines in Korean turbid rice wine, Makgeolli by HPLC with mass spectrometry detection. LWT–Food Sci Technol 62:350–356. doi:10.1016/j.lwt.2015.01.016
CAS Article Google Scholar
Lenney JF, Dalbec JM (1967) Purification and properties of two proteinases from Saccharomyces cerevisiae. Arch Biochem Biophys 120:42–48. doi:10.1016/0003-9861(67)90595-4
CAS Article Google Scholar
Liu JL, Guo W (2012) The exocyst complex in exocytosis and cell migration. Protoplasma 249:587–597. doi:10.1007/s00709-011-0330-1
Article Google Scholar
Lodish HF, Kong N (1990) Perturbation of cellular calcium blocks exit of secretory proteins from the rough endoplasmic reticulum. J Biol Chem 265(19):10893–10899
CAS Google Scholar
Lu J, Dong J, Wu D et al (2012) Construction of recombinant industrial brewer’s yeast with lower diacetyl production and proteinase A activity. Eur Food Res Technol 235:951–961. doi:10.1007/s00217-012-1821-9
CAS Article Google Scholar
Lundblad RL, Stein WH (1969) On the reaction of diazoacetyl compounds with pepsin. J Biol Chem 244:154–160
CAS Google Scholar
Maddox IS, Hough JS (1970) Proteolytic enzymes of Saccharomyces carlsbergensis. Biochem J 117:843–852. doi:10.1042/bj1170843
CAS Article Google Scholar
Marcusson EG, Horazdovsky BF, Cereghino JL et al (1994) The sorting receptor for yeast vacuolar carboxypeptidase Y is encoded by the gene. Curr Biol 77:579–586. doi:10.1016/S0960-9822(00)00231-1
CAS Google Scholar
Marks VD, Ho Sui SJ, Erasmus D et al (2008) Dynamics of the yeast transcriptome during wine fermentation reveals a novel fermentation stress response. FEMS Yeast Res 8:35–52
CAS Article Google Scholar
Mechler B, Wolf DH (1981) Analysis of proteinase A function in yeast. Eur J Biochem 121:47–52. doi:10.1111/j.1432-1033.1981.tb06427.x
CAS Article Google Scholar
Meussdoerffer F, Tortora P, Holzer H (1980) Purification and propertiesof proteinase a from yeast. J Biol Chem 255:12087–12093
CAS Google Scholar
Oda K (1992) Calcium depletion blocks proteolytic cleavages of plasma protein precursors which occur at the Golgi and/or trans-Golgi network. Possible involvement of Ca(2+)-dependent Golgi endoproteases. J Biol Chem 267(24):17465–17471
CAS Google Scholar
Ortiz D, Medkova M, Walchsolimena C et al (2002) Ypt32 recruits the Sec4p guanine nucleotide exchange factor, Sec2p, to secretory vesicles; evidence for a Rab cascade in yeast. J Cell Biol 157:1005. doi:10.1083/jcb.200201003
CAS Article Google Scholar
Parr CL, Keates RAB, Bryksa BC et al (2007) The structure and function of Saccharomyces cerevisiae proteinase A. Yeast 24:467–480. doi:10.1002/yea.1485
CAS Article Google Scholar
Peña-Gallego A, Hernández-Orte P, Cacho J et al (2012) High-performance liquid chromatography analysis of amines in must and wine: a review. Food Rev Int 28:71–96. doi:10.1080/87559129.2011.594973
Article CAS Google Scholar
Pretorius IS (2000) Tailoring wine yeast for the new millennium: novel approaches to the ancient art of winemaking. Yeast 16:675–729. doi:10.1002/1097-0061(20000615)16:8<675::AID-YEA585>3.3.CO;2-2
CAS Article Google Scholar
Pryer NK, Wuestehube LJ, Schekman R (1992) Vesicle-mediated protein sorting. Annu Rev Biochem 61:471–516. doi:10.1146/annurev.bi.61.070192.002351
CAS Article Google Scholar
Riffkin HL, Wilson R, Howie D et al (1989) Ethyl carbamate formation in the production of pot still whisky. J Inst Brewtitute Brew 95:115–119. doi:10.1002/j.2050-0416.1989.tb04618.x
CAS Article Google Scholar
Rothman JH, Hunter CP, Valls LA et al (1986) Overproduction-induced mislocalization of a yeast vacuolar protein allows isolation of its structural gene. Proc Nati Acad Sci USA 83:3248–3252. doi:10.1073/pnas.83.10.3248
CAS Article Google Scholar
Rudolph HK, Antebi A, Fink GR et al (1989) The yeast secretory pathway is perturbed by mutations in PMR1, a member of a Ca²⁺ ATPase family. Cell 58:133–145. doi:10.1016/0092-8674(89)90410-8
CAS Article Google Scholar
Saheki T, Holzer H (1975) Proteolytic activities in yeast. Biochim Biophys Acta 384:203–214. doi:10.1016/0005-2744(75)90109-6
CAS Article Google Scholar
Saheki T, Matsuda Y, Holzer H (1974) Purification and characterization of macromolecular inhibitors of proteinase A from yeast. Eur J Biochem 47:325–332. doi:10.1111/j.1432-1033.1974.tb03697.x
CAS Article Google Scholar
Sambrook JF (1990) The involvement of calcium in transport of secretory proteins from the endoplasmic reticulum. Cell 61:197–199. doi:10.1016/0092-8674(90)90798-J
CAS Article Google Scholar
Sanchez Y, Taulien J, Borkovich KA et al (1992) Hspl04 is required for tolerance to many forms of stress. EMBO J 11:2357–2364. doi:10.1111/j.1567-1364.2006.00035.x
CAS Google Scholar
Schehl B, Senn T, Lachenmeier DW et al (2007) Contribution of the fermenting yeast strain to ethyl carbamate generation in stone fruit spirits. Appl Microbiol Biotechnol 74:843–850. doi:10.1007/s00253-006-0736-4
CAS Article Google Scholar
Smit AY, Toit WJD, Toit MD (2008) Biogenic amines in wine: understanding the headache. South Afr J Enol Vitic 29:109–127. doi:10.21548/29-2-1444
CAS Google Scholar
Söllner T, Whiteheart SW, Brunner M et al (1993) SNAP receptors implicated in vesicle targeting and fusion. Nature 362:318–324. doi:10.1038/362318a0
Article Google Scholar
Somlyo AP, Bond M, Somlyo AV (1985) Calcium content of mitochondria and endoplasmic reticulum in liver frozen rapidly in vivo. Nature 314:622–625. doi:10.1038/314622a0
CAS Article Google Scholar
Springer S, Spang A, Schekman R (1999) A primer on vesicle budding. Cell 97:145–148. doi:10.1016/S0092-8674(00)80722-9
CAS Article Google Scholar
Stevens TH, Rothman JH, Payne GS et al (1986) Gene dosage-dependent secretion of yeast vacuolar carboxypeptidase Y. J Cell Biol 102:1551–1557. doi:10.1083/jcb.102.5.1551
CAS Article Google Scholar
Streb H, Bayerdörffer E, Haase W et al (1984) Effect of inositol-1,4,5-trisphosphate on isolated subcellular fractions of rat pancreas. J Membr Biol 81:241. doi:10.1007/BF01868717
CAS Article Google Scholar
Tang J (1971) Specific and irreversible inactivation of pepsin by substrate-like epoxides. J Biol Chem 246:4510–4517
CAS Google Scholar
Teichert U, Mechlere B, Müller H, Wolf DH (1989) Lysosomal (vacuolar) proteinases of yeast are essential catalysts for protein degradation, differentiation, and cell survival. J Biol Chem 264:16037–16045
CAS Google Scholar
Terbush DR, Novick P (1995) Sec6, Sec8, and Secl5 are components of a multisubunit complex which localizes to small bud tips in Saccharomyces cerevisiae. J Cell Biol 130:299–312. doi:10.1083/jcb.130.2.299
CAS Article Google Scholar
Tian YP, Zhang KC (2005) Purification and characterization of a novel proteinase a inhibitor from Ganoderma lucidum by submerged fermentation. Enzyme Microb Technol 36:357–361. doi:10.1016/j.enzmictec.2004.10.003
CAS Article Google Scholar
Traub LM, Kornfeld S (1997) The trans-Golgi network: a late secretory sorting station. Curr Opin Cel Biol 9:527–533. doi:10.1016/S0955-0674(97)80029-4
CAS Article Google Scholar
Valls LA, Hunter CP, Rothman JH et al (1987) Protein sorting in yeast: the localization determinant of yeast vacuolar carboxypeptidase Y resides in the propeptide. Cell 48:887–897. doi:10.1016/0092-8674(87)90085-7
CAS Article Google Scholar
van den Hazel HB, Kielland-brandt MC, Winther JR (1992) Autoactivation of proteinase A initiates activation of yeast vacuolar zymogens. Eur J Biochem 207:277–283. doi:10.1111/j.1432-1033.1992.tb17048.x
Article Google Scholar
van den Hazel HB, Kielland-Brandt MC, Winther JR (1993) The propeptideis required for in vivo formation of stable active yeast proteinase a and can function even when not covalently linked to the mature region. J Biol Chem 263:18002–18007
Google Scholar
van den Hazel HB, Kielland-brandt MC, Winther JR (1995) Random substitution of large parts of the propeptide of yeast proteinase A. J Biol Chem 270:8602. doi:10.1074/jbc.270.15.8602
Article Google Scholar
van den Hazel HB, Kielland-brandt MC, Winther JR (1996) Review: biosynthesis and function of yeast vacuolar proteases. Yeast 12:1–16. doi:10.1002/(SICI)1097-0061(199601)12:1<1:AID-YEA902>3.0.CO;2-N
Article Google Scholar
Von Blume J, Duran JM, Forlanelli E et al (2009) Actin remodeling by ADF/cofilin is required for cargo sorting at the trans-Golgi network. J Cell Biol 187:1055–1069. doi:10.1083/jcb.200908040
Article CAS Google Scholar
Von Blume J, Alleaume AM, Cantero-Recasens G et al (2011) ADF/cofilin regulates secretory cargo sorting at the TGN via the Ca²⁺ ATPase SPCA1. Dev Cell 20:652–662. doi:10.1016/j.devcel.2011.03.014
Article CAS Google Scholar
Wang ZY, He XP, Zhang BR (2007a) Over expression of GSH1 gene and disruption of PEP4 gene in self-cloning industrial brewer’s yeast. Int J Food Microbiol 119:192–199. doi:10.1016/j.ijfoodmicro.2007.07.015
CAS Article Google Scholar
Wang ZY, He GQ, Ruan H et al (2007b) Construction of proteinase A deficient transformant of industrial brewing yeast. Eur Food Res Technol 225:831–835. doi:10.1007/s00217-006-0488-5
CAS Article Google Scholar
Waters EJ, Alexander G, Muhlack R et al (2010) Preventing protein haze in bottled white wine. Aust J Grape Wine Res 11:215–225. doi:10.1111/j.1755-0238.2005.tb00289.x
Article Google Scholar
Weber JV, Sharypov VI (2009) Ethyl carbamate in foods and beverages: a review. Environ Chem Lett 7:233–247. doi:10.1007/s10311-008-0168-8
CAS Article Google Scholar
Westphal V, Marcusson EG, Winther JR et al (1996) Multiple pathways for vacuolar sorting of yeast proteinase A. J Biol Chem 271:11865–11870
CAS Article Google Scholar
Whyte JRC, Munro S (2001) A yeast homolog of the mammalian mannose 6-phosphate receptors contributes to the sorting of vacuolar hydrolases. Curr Biol 11:1074–1078. doi:10.1016/S0960-9822(01)00273-1
CAS Article Google Scholar
Wileman T, Kane LP, Carson GR, Terhorst C (1991) Depletion of cellular calcium accelerates protein degradation in the endoplasmic reticulum. J Biol Chem 266:4500
CAS Google Scholar
Wolff AM, Din N, Petersen JGL (1996) Vacuolar and extracellular maturation of Saccharomyces cerevisiae proteinase A. Yeast 12:823. doi:10.1002/(SICI)1097-0061(199607)12:9<823::AID-YEA975>3.0.CO;2-J
CAS Article Google Scholar
Woolford CA, Daniels LB, Park FJ et al (1996) The PEP4 gene encodes an aspartyl protease implicated in the posttranslational regulation of Saccharomyces cerevisiae vacuolar hydrolases. Mol Cell Biol 6:2500–2510. doi:10.1128/MCB.6.7.2500
Article Google Scholar
Wu D, Chen Y, Li C et al (2016) Construction of self-cloning industrial brewer’s yeast with SOD1 gene insertion into PEP4 prosequence locus by homologous recombination. J Inst Brew 122:322–332. doi:10.1002/jib.314
CAS Article Google Scholar
Yokoi S, Shigyo T, Tamaki T (1996) A fluorometric assay for proteinase a in beer and its application for the investigation of enzymatic effects on foam stability. J Inst Brew 102:33–37. doi:10.1002/j.2050-0416.1996.tb00892.x
CAS Article Google Scholar
Zhang Q, Chen QH, Fu ML et al (2008) Construction of recombinant industrial Saccharomyces cerevisiae strain with bglS gene insertion into PEP4 locus by homologous recombination. J Zhejiang Univ Sci B 9:527–535. doi:10.1631/jzus.B0820019
CAS Article Google Scholar
Zhang HB, Ruan H, Li WF et al (2011) Construction of recombinant industrial S. cerevisiae strain with barley lipid-transfer protein 1 secretion capability and lower PrA activity. Eur Food Res Technol 233:707–716. doi:10.1007/s00217-011-1559-9
CAS Article Google Scholar
Zhao X, Du G, Zou H et al (2013) Progress in preventing the accumulation of ethyl carbamate in alcoholic beverages. Trends Food Sci Technol 32:97–107. doi:10.1016/j.tifs.2013.05.009
Article CAS Google Scholar
Zhao XR, Zou HJ, Fu JW et al (2014) Metabolic engineering of the regulators in nitrogen catabolite repression to reduce the production of ethyl carbamate in a model rice wine system. Appl Environ Microbiol 80:392–398. doi:10.1128/AEM.03055-13
CAS Article Google Scholar
Zhong J, Ye X, Fang Z et al (2012) Determination of biogenic amines in semi-dry and semi-sweet Chinese rice wines from the Shaoxing region. Food Control 28:151–156. doi:10.1016/j.foodcont.2012.05.011
CAS Article Google Scholar
Zubenko GS, Park FJ, Jones EW (1982) Genetic properties of mutations at the PEP4 locus in Saccharomyces cerevisiae. Genetics 102:679–690
CAS Google Scholar

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The current study was financially supported by the program for the National Natural Science Foundation of China (No. 31271916).

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Key Laboratory of Industrial Fermentation Microbiology, Ministry of Education, Tianjin Industrial Microbiology Key Laboratory, College of Biotechnology, Tianjin University of Science and Technology, Tianjin, 300457, People’s Republic of China
Lulu Song, Yefu Chen, Yongjing Du, Xibin Wang, Xuewu Guo, Jian Dong & Dongguang Xiao

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Lulu Song
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Yefu Chen
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Yongjing Du
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Xibin Wang
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Jian Dong
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Song, L., Chen, Y., Du, Y. et al. Saccharomyces cerevisiae proteinase A excretion and wine making. World J Microbiol Biotechnol 33, 210 (2017). https://doi.org/10.1007/s11274-017-2361-z

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Received: 02 August 2017
Accepted: 26 September 2017
Published: 09 November 2017
DOI: https://doi.org/10.1007/s11274-017-2361-z

Keywords

Proteinase A
Golgi-to-vacuole pathway
Constitutive Golgi-to-plasma membrane pathway
Calcium homeostasis
Wine making
Saccharomyces cerevisiae