Association of calcineurin with the COPI protein Sec28 and the COPII protein Sec13 revealed by quantitative proteomics

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Kozubowski, Lukasz ^a   Thompson, J Will ^a   Cardenas, Maria E ^a   Moseley, M Arthur ^a   Heitman, Joseph ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; COAT PROTEIN COMPLEX II; PHOSPHOPROTEIN PHOSPHATASE; SEC13 PROTEIN; SEC28 PROTEIN; SERINE; THREONINE; UBIQUITIN PROTEIN LIGASE COP1; UNCLASSIFIED DRUG; COAT PROTEIN COMPLEX I; FUNGAL PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN;

ARTICLE; CANDIDA ALBICANS; CONTROLLED STUDY; CRYPTOCOCCUS NEOFORMANS; CYTOPLASM; IMMUNOPRECIPITATION; MASS SPECTROMETRY; MEMBRANE TRANSPORT; NONHUMAN; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; PROTEOMICS; TEMPERATURE STRESS; BIOLOGICAL MODEL; CHEMISTRY; HUMAN; METABOLISM; METHODOLOGY; PHYSIOLOGICAL STRESS; PROTEIN BINDING; PROTEIN TRANSPORT; TEMPERATURE;

FILOBASIDIELLA NEOFORMANS;

CALCINEURIN; COAT PROTEIN COMPLEX I; CRYPTOCOCCUS NEOFORMANS; FUNGAL PROTEINS; GREEN FLUORESCENT PROTEINS; HUMANS; IMMUNOPRECIPITATION; MASS SPECTROMETRY; MODELS, BIOLOGICAL; PROTEIN BINDING; PROTEIN TRANSPORT; PROTEOMICS; RECOMBINANT FUSION PROTEINS; STRESS, PHYSIOLOGICAL; TEMPERATURE;

EID: 80053439003     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0025280     Document Type: Article

References (64)

1. Aramburu J, Heitman J, Crabtree GR, (2004) Calcineurin: a central controller of signalling in eukaryotes. EMBO Rep 5: 343-348.
2. Crabtree GR, Schreiber SL, (2009) SnapShot: Ca2+-calcineurin-NFAT signaling. Cell 138: 210, 210 e211.
3. Cyert MS, (2003) Calcineurin signaling in Saccharomyces cerevisiae: how yeast go crazy in response to stress. Biochem Biophys Res Commun 311: 1143-1150.
4. Crabtree GR, Olson EN, (2002) NFAT signaling: choreographing the social lives of cells. Cell 109 (Suppl): S67-79.
5. Liu JP, Sim AT, Robinson PJ, (1994) Calcineurin inhibition of dynamin I GTPase activity coupled to nerve terminal depolarization. Science 265: 970-973.
6. Wang HG, Pathan N, Ethell IM, Krajewski S, Yamaguchi Y, et al. (1999) Ca2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science 284: 339-343.
7. Long YC, Glund S, Garcia-Roves PM, Zierath JR, (2007) Calcineurin regulates skeletal muscle metabolism via coordinated changes in gene expression. J Biol Chem 282: 1607-1614.
8. Zelter A, Bencina M, Bowman BJ, Yarden O, Read ND, (2004) A comparative genomic analysis of the calcium signaling machinery in Neurospora crassa, Magnaporthe grisea, and Saccharomyces cerevisiae. Fungal Genet Biol 41: 827-841.
9. Stie J, Fox D, (2008) Calcineurin regulation in fungi and beyond. Eukaryot Cell 7: 177-186.
10. Miyakawa T, Mizunuma M, (2007) Physiological roles of calcineurin in Saccharomyces cerevisiae with special emphasis on its roles in G2/M cell-cycle regulation. Biosci Biotechnol Biochem 71: 633-645.
11. Yoshida T, Toda T, Yanagida M, (1994) A calcineurin-like gene ppb1+ in fission yeast: mutant defects in cytokinesis, cell polarity, mating and spindle pole body positioning. J Cell Sci 107 (Pt 7): 1725-1735.
12. Kraus PR, Heitman J, (2003) Coping with stress: calmodulin and calcineurin in model and pathogenic fungi. Biochem Biophys Res Commun 311: 1151-1157.
13. Steinbach WJ, Reedy JL, Cramer RA Jr, Perfect JR, Heitman J, (2007) Harnessing calcineurin as a novel anti-infective agent against invasive fungal infections. Nat Rev Microbiol 5: 418-430.
14. Odom A, Muir S, Lim E, Toffaletti DL, Perfect J, et al. (1997) Calcineurin is required for virulence of Cryptococcus neoformans. EMBO J 16: 2576-2589.
15. Brown SM, Campbell LT, Lodge JK, (2007) Cryptococcus neoformans, a fungus under stress. Curr Opin Microbiol 10: 320-325.
16. Kozubowski L, Lee SC, Heitman J, (2009) Signalling pathways in the pathogenesis of Cryptococcus. Cell Microbiol 11: 370-380.
17. Vermeulen M, Hubner NC, Mann M, (2008) High confidence determination of specific protein-protein interactions using quantitative mass spectrometry. Curr Opin Biotechnol 19: 331-337.
18. Blagoev B, Kratchmarova I, Ong SE, Nielsen M, Foster LJ, et al. (2003) A proteomics strategy to elucidate functional protein-protein interactions applied to EGF signaling. Nat Biotechnol 21: 315-318.
19. Ranish JA, Yi EC, Leslie DM, Purvine SO, Goodlett DR, et al. (2003) The study of macromolecular complexes by quantitative proteomics. Nat Genet 33: 349-355.
20. Andersen JS, Wilkinson CJ, Mayor T, Mortensen P, Nigg EA, et al. (2003) Proteomic characterization of the human centrosome by protein correlation profiling. Nature 426: 570-574.
21. Rinner O, Mueller LN, Hubalek M, Muller M, Gstaiger M, et al. (2007) An integrated mass spectrometric and computational framework for the analysis of protein interaction networks. Nat Biotechnol 25: 345-352.
22. Kozubowski L, Aboobakar EF, Cardenas ME, Heitman J, (2011) Calcineurin co-localizes with P-bodies and stress granules during thermal stress in Cryptococcus neoformans. Eukaryot Cell doi:10.1128/EC.05087-11.
23. Trinkle-Mulcahy L, Boulon S, Lam YW, Urcia R, Boisvert FM, et al. (2008) Identifying specific protein interaction partners using quantitative mass spectrometry and bead proteomes. J Cell Biol 183: 223-239.
24. Idnurm A, Giles SS, Perfect JR, Heitman J, (2007) Peroxisome function regulates growth on glucose in the basidiomycete fungus Cryptococcus neoformans. Eukaryot Cell 6: 60-72.
25. Mackiewicz P, Kowalczuk M, Mackiewicz D, Nowicka A, Dudkiewicz M, et al. (2002) How many protein-coding genes are there in the Saccharomyces cerevisiae genome? Yeast 19: 619-629.
26. Fox DS, Cruz MC, Sia RA, Ke H, Cox GM, et al. (2001) Calcineurin regulatory subunit is essential for virulence and mediates interactions with FKBP12-FK506 in Cryptococcus neoformans. Mol Microbiol 39: 835-849.
27. Gorlach J, Fox DS, Cutler NS, Cox GM, Perfect JR, et al. (2000) Identification and characterization of a highly conserved calcineurin binding protein, CBP1/calcipressin, in Cryptococcus neoformans. EMBO J 19: 3618-3629.
28. Duden R, Kajikawa L, Wuestehube L, Schekman R, (1998) epsilon-COP is a structural component of coatomer that functions to stabilize alpha-COP. EMBO J 17: 985-995.
29. Salama NR, Chuang JS, Schekman RW, (1997) Sec31 encodes an essential component of the COPII coat required for transport vesicle budding from the endoplasmic reticulum. Mol Biol Cell 8: 205-217.
30. Siniossoglou S, Wimmer C, Rieger M, Doye V, Tekotte H, et al. (1996) A novel complex of nucleoporins, which includes Sec13p and a Sec13p homolog, is essential for normal nuclear pores. Cell 84: 265-275.
31. Bannykh SI, Rowe T, Balch WE, (1996) The organization of endoplasmic reticulum export complexes. J Cell Biol 135: 19-35.
32. Rossanese OW, Soderholm J, Bevis BJ, Sears IB, O'Connor J, et al. (1999) Golgi structure correlates with transitional endoplasmic reticulum organization in Pichia pastoris and Saccharomyces cerevisiae. J Cell Biol 145: 69-81.
33. Tokheim AM, Martin BL, (2006) Association of calcineurin with mitochondrial proteins. Proteins 64: 28-33.
34. Singer MA, Lindquist S, (1998) Thermotolerance in Saccharomyces cerevisiae: the Yin and Yang of trehalose. Trends Biotechnol 16: 460-468.
35. Petzold EW, Himmelreich U, Mylonakis E, Rude T, Toffaletti D, et al. (2006) Characterization and regulation of the trehalose synthesis pathway and its importance in the pathogenicity of Cryptococcus neoformans. Infect Immun 74: 5877-5887.
36. Moorhead G, Douglas P, Cotelle V, Harthill J, Morrice N, et al. (1999) Phosphorylation-dependent interactions between enzymes of plant metabolism and 14-3-3 proteins. Plant J 18: 1-12.
37. Glinski M, Weckwerth W, (2005) Differential multisite phosphorylation of the trehalose-6-phosphate synthase gene family in Arabidopsis thaliana: a mass spectrometry-based process for multiparallel peptide library phosphorylation analysis. Mol Cell Proteomics 4: 1614-1625.
38. Blankenship JR, Wormley FL, Boyce MK, Schell WA, Filler SG, et al. (2003) Calcineurin is essential for Candida albicans survival in serum and virulence. Eukaryot Cell 2: 422-430.
39. Fradin C, Kretschmar M, Nichterlein T, Gaillardin C, d'Enfert C, et al. (2003) Stage-specific gene expression of Candida albicans in human blood. Mol Microbiol 47: 1523-1543.
40. Peters J, Sypherd PS, (1979) Morphology-associated expression nicotinamide adenine dinucleotide-dependent glutamate dehydrogenase in Mucorracemosus. J Bacteriol 137: 1134-1139.
41. Khale-Kumar A, Deshpande MV, (1993) Possible involvement of cyclic adenosine 3′,5′-monophosphate in the regulation of NADP-/NAD-glutamate dehydrogenase ratio and in yeast-mycelium transition of Benjaminiella poitrasii. J Bacteriol 175: 6052-6055.
42. Chen YL, Kozubowski L, Cardenas ME, Heitman J, (2010) On the roles of calcineurin in fungal growth and pathogenesis. Curr Fungal Infect Rep 4: 244-255.
43. Kmetzsch L, Staats CC, Simon E, Fonseca FL, de Oliveira DL, et al. The vacuolar Ca(2)(+) exchanger Vcx1 is involved in calcineurin-dependent Ca(2)(+) tolerance and virulence in Cryptococcus neoformans. Eukaryot Cell 9: 1798-1805.
44. Bultynck G, Heath VL, Majeed AP, Galan JM, Haguenauer-Tsapis R, et al. (2006) Slm1 and slm2 are novel substrates of the calcineurin phosphatase required for heat stress-induced endocytosis of the yeast uracil permease. Mol Cell Biol 26: 4729-4745.
45. Daquinag A, Fadri M, Jung SY, Qin J, Kunz J, (2007) The yeast PH domain proteins Slm1 and Slm2 are targets of sphingolipid signaling during the response to heat stress. Mol Cell Biol 27: 633-650.
46. Cowart LA, Gandy JL, Tholanikunnel B, Hannun YA, (2010) Sphingolipids mediate formation of mRNA processing bodies during the heat-stress response of Saccharomyces cerevisiae. Biochem J 431: 31-38.
47. Tabuchi M, Audhya A, Parsons AB, Boone C, Emr SD, (2006) The phosphatidylinositol 4,5-biphosphate and TORC2 binding proteins Slm1 and Slm2 function in sphingolipid regulation. Mol Cell Biol 26: 5861-5875.
48. Luberto C, Toffaletti DL, Wills EA, Tucker SC, Casadevall A, et al. (2001) Roles for inositol-phosphoryl ceramide synthase 1 (IPC1) in pathogenesis of C. neoformans. Genes Dev 15: 201-212.
49. Balagopal V, Parker R, (2009) Polysomes, P bodies and stress granules: states and fates of eukaryotic mRNAs. Curr Opin Cell Biol 21: 403-408.
50. Keeling KM, Salas-Marco J, Osherovich LZ, Bedwell DM, (2006) Tpa1p is part of an mRNP complex that influences translation termination, mRNA deadenylation, and mRNA turnover in Saccharomyces cerevisiae. Mol Cell Biol 26: 5237-5248.
51. Bartz R, Sun LP, Bisel B, Wei JH, Seemann J, (2008) Spatial separation of Golgi and ER during mitosis protects SREBP from unregulated activation. EMBO J 27: 948-955.
52. Tanida I, Hasegawa A, Iida H, Ohya Y, Anraku Y, (1995) Cooperation of calcineurin and vacuolar H(+)-ATPase in intracellular Ca2+ homeostasis of yeast cells. J Biol Chem 270: 10113-10119.
53. Garrett-Engele P, Moilanen B, Cyert MS, (1995) Calcineurin, the Ca2+/calmodulin-dependent protein phosphatase, is essential in yeast mutants with cell integrity defects and in mutants that lack a functional vacuolar H(+)-ATPase. Mol Cell Biol 15: 4103-4114.
54. Hemenway CS, Dolinski K, Cardenas ME, Hiller MA, Jones EW, et al. (1995) vph6 mutants of Saccharomyces cerevisiae require calcineurin for growth and are defective in vacuolar H(+)-ATPase assembly. Genetics 141: 833-844.
55. Conboy MJ, Cyert MS, (2000) Luv1p/Rki1p/Tcs3p/Vps54p, a yeast protein that localizes to the late Golgi and early endosome, is required for normal vacuolar morphology. Mol Biol Cell 11: 2429-2443.
56. Conibear E, Stevens TH, (1998) Multiple sorting pathways between the late Golgi and the vacuole in yeast. Biochim Biophys Acta 1404: 211-230.
57. Sun T, Wu XS, Xu J, McNeil BD, Pang ZP, et al. The role of calcium/calmodulin-activated calcineurin in rapid and slow endocytosis at central synapses. J Neurosci 30: 11838-11847.
58. Song HO, Lee J, Ji YJ, Dwivedi M, Cho JH, et al. Calcineurin regulates coelomocyte endocytosis via DYN-1 and CUP-4 in Caenorhabditis elegans. Mol Cells 30: 255-262.
59. West M, Zurek N, Hoenger A, Voeltz GK, A 3D analysis of yeast ER structure reveals how ER domains are organized by membrane curvature. J Cell Biol 193: 333-346.
60. Alspaugh JA, Perfect JR, Heitman J, (1997) Cryptococcus neoformans mating and virulence are regulated by the G-protein alpha subunit GPA1 and cAMP. Genes Dev 11: 3206-3217.
61. Davidson RC, Cruz MC, Sia RA, Allen B, Alspaugh JA, et al. (2000) Gene disruption by biolistic transformation in serotype D strains of Cryptococcus neoformans. Fungal Genet Biol 29: 38-48.
62. Perfect JR, Ketabchi N, Cox GM, Ingram CW, Beiser CL, (1993) Karyotyping of Cryptococcus neoformans as an epidemiological tool. J Clin Microbiol 31: 3305-3309.
63. Nielsen K, Cox GM, Wang P, Toffaletti DL, Perfect JR, et al. (2003) Sexual cycle of Cryptococcus neoformans var. grubii and virulence of congenic a and alpha isolates. Infect Immun 71: 4831-4841.
64. Kojima K, Bahn YS, Heitman J, (2006) Calcineurin, Mpk1 and Hog1 MAPK pathways independently control fludioxonil antifungal sensitivity in Cryptococcus neoformans. Microbiology 152: 591-604.