The Candida albicans Kar2 protein is essential and functions during the translocation of proteins into the endoplasmic reticulum

Current Genetics

Volumn 57, Issue 1, 2011, Pages 25-37

  Morrow, Michael W ^a   Janke, Megan R ^a   Lund, Kyle ^a   Morrison, Emily P ^a   Paulson, Benjamin A ^a  

^a UNIVERSITY OF MONTANA WESTERN   (United States)

Author keywords

Candida albicans; ER translocation; KAR2; Secretory pathway; Translocation assay

Indexed keywords

FUNGAL PROTEIN; GENOMIC DNA; MESSENGER RNA; MUTANT PROTEIN; PROTEIN KAR2; UNCLASSIFIED DRUG;

ARTICLE; CANDIDA ALBICANS; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ESSENTIAL GENE; FUNGAL GENE; FUNGUS GROWTH; GENE DOSAGE; GENE EXPRESSION; GENE FUNCTION; IN VITRO STUDY; KAR2 GENE; MICROSOME; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SECRETORY PATHWAY; SIGNAL TRANSDUCTION; TEMPERATURE SENSITIVITY; WILD TYPE;

CANDIDA ALBICANS; ENDOPLASMIC RETICULUM; FUNGAL PROTEINS; HSP70 HEAT-SHOCK PROTEINS; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE;

CANDIDA ALBICANS; EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 78951474863     PISSN: 01728083     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00294-010-0323-1     Document Type: Article

References (76)

1. NN Alder Y Shen JL Brodsky LM Hendershot AE Johnson 2005 The molecular mechanism underlying BiP-mediated gating of the Sec61 translocon of the endoplasmic reticulum J Cell Biol 168 389 399 1:CAS:528:DC%2BD2MXhtVWktLs%3D 10.1083/jcb.200409174 15684029
2. S Bates DM MacCallum G Bertram CA Munro HB Hughes ET Buurman AJ Brown FC Odds NA Gow 2005 Candida albicans Pmr1p, a secretory pathway P-type Ca2+/Mn2+-ATPase, is required for glycosylation and virulence J Biol Chem 280 23408 23415 1:CAS:528:DC%2BD2MXltVygs7g%3D 10.1074/jbc.M502162200 15843378
3. SM Bernardo Z Khalique J Kot JK Jones SA Lee 2008 Candida albicans VPS1 contributes to protease secretion, filamentation and biofilm formation Fungal Genet Biol 45 861 877 1:CAS:528:DC%2BD1cXmtVSmu7k%3D 10.1016/j.fgb.2008.01.001 18296085
4. JL Brodsky R Schekman 1993 A Sec63p-BiP complex from yeast is required for protein translocation in a reconstituted proteoliposome J Cell Biol 123 1355 1363 1:CAS:528:DyaK3sXms1Ckurw%3D 10.1083/jcb.123.6.1355 8253836
5. JL Brodsky S Hamamoto D Feldheim R Schekman 1993 Reconstitution of protein translocation from solubilized yeast membranes reveals topologically distinct roles for BiP and cytosolic Hsc70 J Cell Biol 120 95 102 1:CAS:528:DyaK3sXjsFKnug%3D%3D 10.1083/jcb.120.1.95 8416998
6. JL Brodsky J Goeckeler R Schekman 1995 BiP and Sec63p are required for both co- and posttranslational protein translocation into the yeast endoplasmic reticulum Proc Natl Acad Sci 92 9643 9646 1:CAS:528:DyaK2MXoslCms7w%3D 10.1073/pnas.92.21.9643 7568189
7. RS Care J Trevethick KM Binley PE Sudbery 1999 The MET3 promoter: a new tool for Candida albicans molecular genetics Mol Microbiol 34 792 798 1:CAS:528:DyaK1MXnslyjsb0%3D 10.1046/j.1365-2958.1999.01641.x 10564518
8. WL Chaffin 2008 Candida albicans cell wall proteins Microbiol Mol Biol Rev 72 495 544 1:CAS:528:DC%2BD1cXhtFylsrbI 10.1128/MMBR.00032-07 18772287
9. WL Chaffin JL López-Ribot M Casanova D Gozalbo JP Martínez 1998 Cell wall and secreted proteins of Candida albicans: identification, function and expression Microbiol Mol Biol Rev 62 130 180 1:CAS:528: DyaK1cXitF2jsb8%3D 9529890
10. M Clément H Fournier L De Repentigny P Belhumeur 1998 Isolation and characterization of the Candida albicans SEC4 gene Yeast 14 675 680 10.1002/(SICI)1097-0061(199805)14:7<675::AID-YEA252>3.0.CO;2-9 9639314
11. DA Davis VM Bruno L Loza SG Filler AP Mitchell 2002 Candida albicans Mds3p, a conserved regulator of pH responses and virulence identified through insertional mutagenesis Genetics 162 1573 1581 1:CAS:528:DC%2BD3sXht1Wqu7g%3D 12524333
12. JM De la Rosa JM González F Gutiérrez T Ruíz L Rodríguez 2004 Characterization of Candida albicans orthologue of the Saccharomyces cerevisiae signal-peptidase-subunit encoding gene SPC3 Yeast 21 883 894 10.1002/yea.1137
13. JM De la Rosa T Ruíz WA Fonzi L Rodríguez 2004 Analysis of heterologous expression of Candida albicans SEC61 gene reveals differences in Sec61p homologues related to species-specific functionality Fungal Genet Biol 41 941 953 10.1016/j.fgb.2004.07.004 15341916
14. B Enloe A Diamond AP Mitchell 2000 A single-transformation gene function test in diploid Candida albicans J Bacteriol 182 5730 5736 1:CAS:528: DC%2BD3cXnt1aisrk%3D 10.1128/JB.182.20.5730-5736.2000 11004171
15. Filler SG, Kullberg BJ (2002) Deep-seated candidal infections. In: Calderone RA (ed) Candida and candidiasis. ASM Press, Washington, DC, pp 341-348
16. WA Fonzi 2009 The protein secretory pathway of Candida albicans Mycoses 52 291 303 1:CAS:528:DC%2BD1MXosFCkur4%3D 10.1111/j.1439-0507.2008.01673.x
17. I Gagnon-Arsenault J Tremblay Y Bourbonnais 2006 Fungal yapsins and cell wall: a unique family of aspartic peptidases for a distinctive cellular function FEMS Yeast Res 6 966 978 1:CAS:528:DC%2BD28XhtFGqtr7L 10.1111/j.1567-1364.2006. 00129.x 17042746
18. MJ Gething 1999 Role and regulation of the ER chaperone BiP Semin Cell Dev Biol 10 465 472 1:CAS:528:DyaK1MXnvFOmsLs%3D 10.1006/scdb.1999.0318 10597629
19. RD Gietz RA Woods 2002 Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method Methods Enzymol 350 87 96 1:CAS:528:DC%2BD38XlsVaqs7g%3D 10.1016/S0076-6879(02)50957-5 12073338
20. AM Gillum EY Tsay DR Kirsch 1984 Isolation of the Candida albicans gene for orotidine-5′-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations Mol Gen Genet 198 179 182 1:CAS:528:DyaL2MXhsl2qurk%3D 10.1007/BF00328721 6394964
21. NG Haigh AE Johnson 2002 A new role for BiP: closing the aqueous translocon pore during protein integration into the ER membrane J Cell Biol 156 261 270 1:CAS:528:DC%2BD38XosFCmuw%3D%3D 10.1083/jcb.200110074 11807091
22. BD Hamman LM Hendershot AE Johnson 1998 BiP maintains the permeability barrier of the ER membrane by sealing the lumenal end of the translocon pore before and early in translocation Cell 92 747 758 1:CAS:528:DyaK1cXit1KlsLo%3D 10.1016/S0092-8674(00)81403-8 9529251
23. B Hube 1996 Candida albicans secreted aspartyl proteinases Curr Top Med Mycol 7 55 69 1:STN:280:DyaK1c7msVyisg%3D%3D 9504059
24. M Kabani SS Kelley MW Morrow DL Montgomery R Sivendran MD Rose LM Gierasch JL Brodsky 2003 Dependence of endoplasmic reticulum-associated degradation on the peptide binding domain and concentration of BiP Mol Biol Cell 14 3437 3448 1:CAS:528:DC%2BD3sXmvFWksL8%3D 10.1091/mbc.E02-12-0847 12925775
25. Kullberg BJ, Filler SG (2002) Candidemia. In: Calderone RA (ed) Candida and candidiasis. ASM Press, Washington, DC, pp 327-340
26. M Latterich R Schekman 1994 The karyogamy gene KAR2 and novel proteins are required for ER-membrane fusion Cell 78 87 98 1:CAS:528:DyaK2cXlt1OjsL4%3D 10.1016/0092-8674(94)90575-4 8033215
27. RJ Lee C Liu C Harty AA McCracken M Latterich K Römisch GN DeMartino PJ Thomas JL Brodsky 2004 Uncoupling retro-translocation and degradation in the ER-associated degradation of a soluble protein EMBO J 23 2206 2215 1:CAS:528:DC%2BD2cXksV2hsbY%3D 10.1038/sj.emboj.7600232 15152188
28. RJ Lee AA McCracken JL Brodsky 2005 Reconstitution of endoplasmic reticulum-associated degradation using yeast membranes and cytosol Methods Mol Biol 301 175 184 1:CAS:528:DC%2BD2MXkt12qsLY%3D 15917632
29. SA Lee J Jones S Hardison J Kot Z Khalique SM Bernardo A Lazzell C Monteagudo J Lopez-Ribot 2009 Candida albicans VPS4 is required for secretion of aspartyl proteases and in vivo virulence Mycopathologia 167 55 63 1:CAS:528:DC%2BD1MXlsFKmtQ%3D%3D 10.1007/s11046-008-9155-7 18814053
30. -ΔΔC method Methods 25 402 408 1:CAS:528: DC%2BD38XhtFelt7s%3D 10.1006/meth.2001.1262 11846609
31. SK Lyman R Schekman 1995 Interaction between BiP and Sec63p is required for the completion of protein translocation into the ER of Saccharomyces cerevisiae J Cell Biol 131 1163 1171 1:CAS:528:DyaK2MXpvVWjs70%3D 10.1083/jcb.131.5.1163 8522580
32. T Makio S Nishikawa T Nakayama H Nagai T Endo 2008 Identification and characterization of a Jem1p ortholog of Candida albicans: dissection of Jem1p functions in karyogamy and protein quality control in Saccharomyces cerevisiae Genes Cells 13 1015 1026 1:CAS:528:DC%2BD1cXht1ygtbzM 10.1111/j.1365-2443.2008. 01223.x 18754794
33. Y Mao VF Kalb B Wong 1999 Overexpression of a dominant-negative allele of SEC4 inhibits growth and protein secretion in Candida albicans J Bacteriol 181 7235 7242 1:CAS:528:DyaK1MXnslOmt7g%3D 10572126
34. KE Matlack K Plath B Misselwitz TA Rapoport 1997 Protein transport by purified yeast Sec somplex and Kar2p without membranes Science 277 938 941 1:CAS:528:DyaK2sXltlCrtbw%3D 10.1126/science.277.5328.938 9252322
35. KES Matlack B Misselwitz K Plath TA Rapoport 1999 BiP acts as a molecular ratchet during posttranslational transport of prepro-α factor across the ER membrane Cell 97 553 564 1:CAS:528:DyaK1MXjs1yqtb8%3D 10.1016/S0092-8674(00) 80767-9 10367885
36. AJ McClellan JB Endres JP Vogel D Palazzi MD Rose JL Brodsky 1998 Specific molecular chaperone interactions and an ATP-dependent conformational change are required during posttranslational protein translocation into the yeast ER Mol Biol Cell 9 3533 3545 1:CAS:528:DyaK1cXnvFOmtbs%3D 9843586
37. AA McCracken JL Brodsky 1996 Assembly of ER-associated protein degradation in vitro: dependence on cytosol, calnexin and ATP J Cell Biol 132 291 298 1:CAS:528:DyaK28XpsVaqtw%3D%3D 10.1083/jcb.132.3.291 8636208
38. MS Meda AJ Lopez A Guyot 2007 Candida inferior vena cava filter infection and septic thrombophlebitis Br J Radiol 80 e48 e49 1:STN:280: DC%2BD2s3os1amtg%3D%3D 10.1259/bjr/13944004 17495055
39. L Monteoliva M Sánchez J Pla C Gil C Nombela 1996 Cloning of Candida albcians SEC14 gene homologue coding for a putative essential function Yeast 12 1097 1105 1:CAS:528:DyaK28Xmt1ais7Y%3D 10.1002/(SICI)1097- 0061(19960915)12:11<1097::AID-YEA990>3.0.CO;2-E 8896277
40. MW Morrow JL Brodsky 2001 Yeast ribosomes bind to highly purified reconstituted Sec61p complex and to mammalian p180 Traffic 2 705 716 1:CAS:528:DC%2BD3MXnvVaqu7g%3D 10.1034/j.1600-0854.2001.21005.x 11576447
41. Morrow MW, Brodsky JL (2005) Protein import into endoplasmic reticulum: methods. In: The encyclopedia of life sciences. Nature Publishing Group, New York 15:346-348
42. JR Naglik SJ Challacombe B Hube 2003 Candida albicans secreted aspartyl proteinases in virulence and pathogenesis Micro Mol Biol Rev 67 400 428 1:CAS:528:DC%2BD3sXnvF2nt7g%3D 10.1128/MMBR.67.3.400-428.2003
43. DT Ng P Walter 1996 ER membrane protein complex required for nuclear fusion J Cell Biol 132 499 509 1:CAS:528:DyaK28XhtF2ksb4%3D 10.1083/jcb.132.4. 499 8647883
44. A Nieto P Sanz R Sentandreu LDC Agudo 1993 Cloning and characterization of the SEC18 gene from Candida albicans Yeast 9 875 887 1:CAS:528:DyaK2cXhvVGh 10.1002/yea.320090808 8212895
45. S Nishikawa SW Fewell Y Kato JL Brodsky T Endo 2001 Molecular chaperones in the yeast endoplasmic reticulum maintain the solubility of proteins for retrotranslocation and degradation J Cell Biol 153 1061 1069 1:CAS:528:DC%2BD3MXktVags78%3D 10.1083/jcb.153.5.1061 11381090
46. S Nishikawa JL Brodsky K Nakatsukasa 2005 Roles of molecular chaperones in endoplasmic reticulum (ER) quality control and ER-associated degradation (ERAD) J Biochem 137 551 555 1:CAS:528:DC%2BD2MXlvF2lsbk%3D 10.1093/jb/mvi068 15944407
47. C Nombela C Gil L Chaffin 2006 Non-conventional protein secretion in yeast Trends Micro 14 15 21 1:CAS:528:DC%2BD28XksVWmuw%3D%3D 10.1016/j.tim.2005.11.009
48. K Normington K Kohno Y Kozutsumi MJ Gething J Sambrook 1989 S. cerevisiae encodes an essential protein homologous in sequence and function to mammalian BiP Cell 57 1223 1236 1:CAS:528:DyaK3cXpt1ymtA%3D%3D 10.1016/0092-8674(89)90059- 7 2661019
49. S Panzner L Dreier E Hartmann S Kostka TA Rapoport 1995 Posttranslational protein transport in yeast reconstituted with a purified complex of Sec proteins and Kar2p Cell 81 561 570 1:CAS:528:DyaK2MXlvVGguro%3D 10.1016/0092-8674(95)90077-2 7758110
50. K Plath W Mothes BM Wilkinson CJ Stirling TA Rapoport 1998 Signal sequence recognition in pottranslational protein transport across the yeast ER membrane Cell 94 795 807 1:CAS:528:DyaK1cXmtlCjsL8%3D 10.1016/S0092-8674(00) 81738-9 9753326
51. RK Plemper S Böhmler J Bordallo T Sommer DH Wolf 1997 Mutant analysis links the translocon and BiP to retrograde protein transport for ER degradation Nature 388 891 895 1:STN:280:DyaK2svit1artg%3D%3D 10.1038/42276 9278052
52. M Regnacq E Hewitt J Allen J Rosamond CJ Stirling 1998 Deletion analysis of yeast Sec65p reveals a central domain that is sufficient for function in vivo Mol Microbiol 29 753 762 1:CAS:528:DyaK1cXlsFCksbs%3D 10.1046/j.1365-2958.1998. 00969.x 9723915
53. H Rico E Herrero F Miragall R Sentandreu 1991 An electron microscopy study of wall expansion during Candida albicans yeast and mycelial growth using concanavalin A-ferritin labeling of mannoproteins Arch Microbiol 156 111 114 1:CAS:528:DyaK3MXlsFCku7c%3D 10.1007/BF00290982 1781727
54. L Romani F Bistoni P Puccetti 2003 Adaptation of Candida albicans to the host environment: the role of morphogenesis in virulence and survival in mammalian hosts Curr Opin Microbiol 6 338 343 10.1016/S1369-5274(03)00081-X 12941401
55. MD Rose LM Misra JP Vogel 1989 KAR2, a karyogamy gene, is the yeast homolog of the mammalian BiP/GRP78 gene Cell 57 1211 1221 1:CAS:528: DyaK3cXpt1ymtw%3D%3D 10.1016/0092-8674(89)90058-5 2661018
56. Rose MD, Winston F, Hieter P (1990) Methods in yeast genetics: a laboratory course manual. Cold Springs Harbor Laboratory Press, Cold Springs Harbor, NY
57. JA Rothblatt RJ Deshaies SL Sanders G Daum R Schekman 1989 Multiple genes are required for proper insertion of secretory proteins into the endoplasmic reticulum of yeast J Cell Biol 109 2641 2652 1:CAS:528:DyaL1MXmt1yrs78%3D 10.1083/jcb.109.6.2641 2687285
58. Ruhnke M (2002) Skin and mucous membrane infections. In: Calderone RA (ed) Candida and candidiasis. ASM Press, Washington, DC, pp 307-325
59. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
60. SL Sanders KM Whitfield JP Vogel MD Rose RW Schekman 1992 Sec61p and BiP directly facilitate polypeptide translocation into the ER Cell 69 353 365 1:CAS:528:DyaK38XisFSlsrc%3D 10.1016/0092-8674(92)90415-9 1568250
61. H Sandovsky-Losica E Segal 2006 Infection of HEp2 epithelial cells with Candida albicans: adherence and postadherence events FEMS Immunol Med Microbiol 46 470 475 1:CAS:528:DC%2BD28XktVCktr8%3D 10.1111/j.1574-695X.2006.00070.x 16553823
62. M Schaller C Borelli HC Korting B Hube 2005 Hydrolytic enzymes as virulence factors of Candida albicans Mycoses 48 365 377 1:CAS:528: DC%2BD2MXhtlSjsrzF 10.1111/j.1439-0507.2005.01165.x 16262871
63. JF Simons S Ferro-Novick MD Rose A Helenius 1995 BiP/Kar2p serves as a molecular chaperone during carboxypeptidase Y folding in yeast J Cell Biol 130 41 49 1:CAS:528:DyaK2MXmsFWhuro%3D 10.1083/jcb.130.1.41 7790376
64. K Sohn J Schwenk C Urban J Lechner M Schweikert S Rupp 2006 Getting in touch with Candida albicans: the cell wall of a fungal pathogen Curr Drug Targets 7 505 512 1:CAS:528:DC%2BD28Xjt1Siur4%3D 10.2174/138945006776359395 16611038
65. PK Sorger HRB Pelham 1987 Purification and characterization of a heat-shock element binding protein from yeast EMBO J 6 3035 3041 1:CAS:528:DyaL1cXjtlOqsw%3D%3D 3319580
66. CJ Stirling J Rothblatt M Hosobuchi R Deshaies R Schekman 1992 Protein translocation mutants defective in the insertion of integral membrane proteins into the endoplasmic reticulum Mol Biol Cell 3 129 142 1:CAS:528: DyaK3sXhvVOgu7c%3D 1550957
67. P Sudbery N Gow J Berman 2004 The distinct morphogenic states of Candida albicans Trends Microbiol 12 317 324 1:CAS:528:DC%2BD2cXlt1ansbc%3D 10.1016/j.tim.2004.05.008 15223059
68. DP Thomas JL Lopez-Ribot SA Lee 2009 A proteomic analysis of secretory proteins of a pre-vacuolar mutant of Candida albicans J Proteomics 73 342 351 1:CAS:528:DC%2BD1MXhsVWqu7rP 10.1016/j.jprot.2009.10.003 19819358
69. G Tronchin JP Bouchara V Annaix R Robert JM Senet 1991 Fungal cell adhesion molecules in Candida albicans Eur J Epidemiol 7 23 33 1:CAS:528:DyaK3MXmtVaktbc%3D 10.1007/BF00221338 2026220
70. KJ Verstrepen FM Klis 2006 Flocculation, adhesion and biofilm formation in yeasts Mol Microbiol 60 5 15 1:CAS:528:DC%2BD28Xjsleht70%3D 10.1111/j.1365-2958.2006.05072.x 16556216
71. JP Vogel LM Misra MD Rose 1990 Loss of BiP/GRP78 function blocks translocation of secretory proteins in yeast J Cell Biol 110 1885 1895 1:CAS:528:DyaK3cXitFeks7k%3D 10.1083/jcb.110.6.1885 2190988
72. A Wach A Brachat R Pöhlmann P Philippsen 1994 New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae Yeast 10 1793 1808 1:CAS:528:DyaK2MXks1Kqt7Y%3D 10.1002/yea.320101310 7747518
73. Y Weber UJ Santore JF Ernst RK Swoboda 2001 Divergence of eukaryotic secretory components: the Candida albicans homolog of the Saccharomyces cerevisiae Sec20 protein is N terminally truncated, and its levels determine antifungal drug resistance and growth J Bacteriol 183 46 54 1:CAS:528: DC%2BD3MXhtFGhug%3D%3D 10.1128/JB.183.1.46-54.2001 11114899
74. RB Wilson D Davis AP Mitchell 1999 Rapid hypothesis testing with Candida albicans through gene disruption with short homology regions J Bacteriol 181 1868 1874 1:CAS:528:DyaK1MXitVCmsrk%3D 10074081
75. TT Wimalasena B Enjalbert T Guillemette A Plumridge S Budge Z Yin AJP Brown DB Archer 2008 Impact of the unfolded protein response upon genome-wide expression patterns, and the role of Hac1 in the polarized growth of Candida albicans Fungal Genet Biol 45 1235 1247 1:CAS:528:DC%2BD1cXhtVKmsb7O 10.1016/j.fgb.2008.06.001 18602013
76. BP Young RA Craven PJ Reid M Willer C Stirling 2001 Sec63p and Kar2p are required for the translocation of SRP-dependent precursors into the yeast endoplasmic reticulum in vivo EMBO J 20 262 271 1:CAS:528:DC%2BD3MXhvVCmu7Y%3D 10.1093/emboj/20.1.262 11226176