Uncoupling of mRNA synthesis and degradation impairs adaptation to host temperature in Cryptococcus neoformans

Molecular Microbiology

Volumn 89, Issue 1, 2013, Pages 65-83

  Bloom, Amanda L M ^a   Solomons, J T Graham ^a   Havel, Virginia E ^a   Panepinto, John C ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CCR4 PROTEIN; FUNGAL ENZYME; MESSENGER RNA; RIBONUCLEASE H; RIBOSOME PROTEIN; RNA POLYMERASE II; RPB4 PROTEIN; UNCLASSIFIED DRUG;

ADAPTATION; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; CRYPTOCOCCUS NEOFORMANS; CYTOPLASM; ENDOPLASMIC RETICULUM STRESS; ENZYME SUBUNIT; FUNGAL VIRULENCE; FUNGUS MUTANT; GENETIC TRANSCRIPTION; HOST; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEADENYLATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN STABILITY; RNA DEGRADATION; RNA SYNTHESIS; TEMPERATURE;

CRYPTOCOCCUS NEOFORMANS; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; RNA STABILITY; RNA, MESSENGER; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TEMPERATURE;

FILOBASIDIELLA NEOFORMANS; FUNGI;

EID: 84879506957     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12258     Document Type: Article

References (56)

1. Albig, A.R., and Decker, C.J. (2001) The target of rapamycin signaling pathway regulates mRNA turnover in the yeast Saccharomyces cerevisiae. Mol Biol Cell 12: 3428-3438.
2. Alspaugh, J.A., Cavallo, L.M., Perfect, J.R., and Heitman, J. (2000) RAS1 regulates filamentation, mating and growth at high temperature of Cryptococcus neoformans. Mol Microbiol 36: 352-365.
3. Armache, K.J., Kettenberger, H., and Cramer, P. (2003) Architecture of initiation-competent 12-subunit RNA polymerase II. Proc Natl Acad Sci USA 100: 6964-6968.
4. Armache, K.J., Mitterweger, S., Meinhart, A., and Cramer, P. (2005) Structures of complete RNA polymerase II and its subcomplex, Rpb4/7. J Biol Chem 280: 7131-7134.
5. Bartlam, M., and Yamamoto, T. (2010) The structural basis for deadenylation by the CCR4-NOT complex. Protein Cell 1: 443-452.
6. Brown, S.M., Campbell, L.T., and Lodge, J.K. (2007) Cryptococcus neoformans, a fungus under stress. Curr Opin Microbiol 10: 320-325.
7. Bushnell, D.A., and Kornberg, R.D. (2003) Complete, 12-subunit RNA polymerase II at 4.1-A resolution: implications for the initiation of transcription. Proc Natl Acad Sci USA 100: 6969-6973.
8. Chabrier-Rosello, Y., Gerik, K.J., Koselny, K., Didone, L., Lodge, J.K., and Krysan, D.J. (2013) Cryptococcus neoformans phosphoinositide-dependent kinase 1 (PDK1) ortholog is required for stress tolerance and survival in murine phagocytes. Eukaryot Cell 12: 12-22.
9. Chauhan, N., Inglis, D., Roman, E., Pla, J., Li, D., Calera, J.A., and Calderone, R. (2003) Candida albicans response regulator gene SSK1 regulates a subset of genes whose functions are associated with cell wall biosynthesis and adaptation to oxidative stress. Eukaryot Cell 2: 1018-1024.
10. Chen, C.Y., and Shyu, A.B. (2011) Mechanisms of deadenylation-dependent decay. Wiley Interdiscip Rev RNA 2: 167-183.
11. Cowart, L.A., Gandy, J.L., Tholanikunnel, B., and Hannun, Y.A. (2010) Sphingolipids mediate formation of mRNA processing bodies during the heat-stress response of Saccharomyces cerevisiae. Biochem J 431: 31-38.
12. Doidge, R., Mittal, S., Aslam, A., and Winkler, G.S. (2012) Deadenylation of cytoplasmic mRNA by the mammalian Ccr4-Not complex. Biochem Soc Trans 40: 896-901.
13. Dori-Bachash, M., Shema, E., and Tirosh, I. (2011) Coupled evolution of transcription and mRNA degradation. PLoS Biol 9: e1001106.
14. Farago, M., Nahari, T., Hammel, C., Cole, C.N., and Choder, M. (2003) Rpb4p, a subunit of RNA polymerase II, mediates mRNA export during stress. Mol Biol Cell 14: 2744-2755.
15. Gerik, K.J., Bhimireddy, S.R., Ryerse, J.S., Specht, C.A., and Lodge, J.K. (2008) PKC1 is essential for protection against both oxidative and nitrosative stresses, cell integrity, and normal manifestation of virulence factors in the pathogenic fungus Cryptococcus neoformans. Eukaryot Cell 7: 1685-1698.
16. Goldstrohm, A.C., Seay, D.J., Hook, B.A., and Wickens, M. (2007) PUF protein-mediated deadenylation is catalyzed by Ccr4p. J Biol Chem 282: 109-114.
17. Goler-Baron, V., Selitrennik, M., Barkai, O., Haimovich, G., Lotan, R., and Choder, M. (2008) Transcription in the nucleus and mRNA decay in the cytoplasm are coupled processes. Genes Dev 22: 2022-2027.
18. Havel, V.E., Wool, N.K., Ayad, D., Downey, K.M., Wilson, C.F., Larsen, P., etal. (2011) Ccr4 promotes resolution of the endoplasmic reticulum stress response during host temperature adaptation in Cryptococcus neoformans. Eukaryot Cell 10: 895-901.
19. Herruer, M.H., Mager, W.H., Raue, H.A., Vreken, P., Wilms, E., and Planta, R.J. (1988) Mild temperature shock affects transcription of yeast ribosomal protein genes as well as the stability of their mRNAs. Nucleic Acids Res 16: 7917-7929.
20. Heung, L.J., Luberto, C., Plowden, A., Hannun, Y.A., and Poeta, M.D. (2004) The sphingolipid pathway regulates Pkc1 through the formation of diacylglycerol in Cryptococcus neoformans. J Biol Chem 279: 21144-21153.
21. Inagaki, M., Schmelzle, T., Yamaguchi, K., Irie, K., Hall, M.N., and Matsumoto, K. (1999) PDK1 homologs activate the Pkc1-mitogen-activated protein kinase pathway in yeast. Mol Cell Biol 19: 8344-8352.
22. Keene, J.D. (2007) RNA regulons: coordination of post-transcriptional events. Nat Rev Genet 8: 533-543.
23. Kozubowski, L., Aboobakar, E.F., Cardenas, M.E., and Heitman, J. (2011) Calcineurin colocalizes with P-bodies and stress granules during thermal stress in Cryptococcus neoformans. Eukaryot Cell 10: 1396-1402.
24. Kraus, P.R., Boily, M.J., Giles, S.S., Stajich, J.E., Allen, A., Cox, G.M., etal. (2004) Identification of Cryptococcus neoformans temperature-regulated genes with a genomic-DNA microarray. Eukaryot Cell 3: 1249-1260.
25. Lee, H., Khanal Lamichhane, A., Garraffo, H.M., Kwon-Chung, K.J., and Chang, Y.C. (2012) Involvement of PDK1, PKC and TOR signalling pathways in basal fluconazole tolerance in Cryptococcus neoformans. Mol Microbiol 84: 130-146.
26. Liu, K., Zhang, X., Lester, R.L., and Dickson, R.C. (2005) The sphingoid long chain base phytosphingosine activates AGC-type protein kinases in Saccharomyces cerevisiae including Ypk1, Ypk2, and Sch9. J Biol Chem 280: 22679-22687.
27. Liu, O.W., Chun, C.D., Chow, E.D., Chen, C., Madhani, H.D., and Noble, S.M. (2008) Systematic genetic analysis of virulence in the human fungal pathogen Cryptococcus neoformans. Cell 135: 174-188.
28. Lotan, R., Bar-On, V.G., Harel-Sharvit, L., Duek, L., Melamed, D., and Choder, M. (2005) The RNA polymerase II subunit Rpb4p mediates decay of a specific class of mRNAs. Genes Dev 19: 3004-3016.
29. Lotan, R., Goler-Baron, V., Duek, L., Haimovich, G., and Choder, M. (2007) The Rpb7p subunit of yeast RNA polymerase II plays roles in the two major cytoplasmic mRNA decay mechanisms. J Cell Biol 178: 1133-1143.
30. Luberto, C., Toffaletti, D.L., Wills, E.A., Tucker, S.C., Casadevall, A., Perfect, J.R., etal. (2001) Roles for inositol-phosphoryl ceramide synthase 1 (IPC1) in pathogenesis of C. neoformans. Genes Dev 15: 201-212.
31. Luo, G., Gruhler, A., Liu, Y., Jensen, O.N., and Dickson, R.C. (2008) The sphingolipid long-chain base-Pkh1/2-Ypk1/2 signaling pathway regulates eisosome assembly and turnover. J Biol Chem 283: 10433-10444.
32. Luo, G., Costanzo, M., Boone, C., and Dickson, R.C. (2011) Nutrients and the Pkh1/2 and Pkc1 protein kinases control mRNA decay and P-body assembly in yeast. J Biol Chem 286: 8759-8770.
33. McCluskey, K., Wiest, A., and Plamann, M. (2010) The Fungal Genetics Stock Center: a repository for 50 years of fungal genetics research. J Biosci 35: 119-126.
34. Maeng, S., Ko, Y.J., Kim, G.B., Jung, K.W., Floyd, A., Heitman, J., and Bahn, Y.S. (2010) Comparative transcriptome analysis reveals novel roles of the Ras and cyclic AMP signaling pathways in environmental stress response and antifungal drug sensitivity in Cryptococcus neoformans. Eukaryot Cell 9: 360-378.
35. Meka, H., Werner, F., Cordell, S.C., Onesti, S., and Brick, P. (2005) Crystal structure and RNA binding of the Rpb4/Rpb7 subunits of human RNA polymerase II. Nucleic Acids Res 33: 6435-6444.
36. Munchel, S.E., Shultzaberger, R.K., Takizawa, N., and Weis, K. (2011) Dynamic profiling of mRNA turnover reveals gene-specific and system-wide regulation of mRNA decay. Mol Biol Cell 22: 2787-2795.
37. Murray, E.L., and Schoenberg, D.R. (2008) Assays for determining poly(A) tail length and the polarity of mRNA decay in mammalian cells. Methods Enzymol 448: 483-504.
38. Odom, A., Muir, S., Lim, E., Toffaletti, D.L., Perfect, J., and Heitman, J. (1997) Calcineurin is required for virulence of Cryptococcus neoformans. EMBO J 16: 2576-2589.
39. Orlicky, S.M., Tran, P.T., Sayre, M.H., and Edwards, A.M. (2001) Dissociable Rpb4-Rpb7 subassembly of RNA polymerase II binds to single-strand nucleic acid and mediates a post-recruitment step in transcription initiation. J Biol Chem 276: 10097-10102.
40. Paldanius, P.M., Ivaska, K.K., Hovi, P., Andersson, S., Vaananen, H.K., Kajantie, E., and Makitie, O. (2012) The effect of oral glucose tolerance test on serum osteocalcin and bone turnover markers in young adults. Calcif Tissue Int 90: 90-95.
41. Panepinto, J., Liu, L., Ramos, J., Zhu, X., Valyi-Nagy, T., Eksi, S., etal. (2005) The DEAD-box RNA helicase Vad1 regulates multiple virulence-associated genes in Cryptococcus neoformans. J Clin Invest 115: 632-641.
42. Panepinto, J.C., Komperda, K.W., Hacham, M., Shin, S., Liu, X., and Williamson, P.R. (2007) Binding of serum mannan binding lectin to a cell integrity-defective Cryptococcus neoformans ccr4Delta mutant. Infect Immun 75: 4769-4779.
43. Park, B.J., Wannemuehler, K.A., Marston, B.J., Govender, N., Pappas, P.G., and Chiller, T.M. (2009) Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS. AIDS 23: 525-530.
44. Parker, R., and Sheth, U. (2007) P bodies and the control of mRNA translation and degradation. Mol Cell 25: 635-646.
45. Perfect, J.R. (2006) Cryptococcus neoformans: the yeast that likes it hot. FEMS Yeast Res 6: 463-468.
46. Rendl, L.M., Bieman, M.A., and Smibert, C.A. (2008) S. cerevisiae Vts1p induces deadenylation-dependent transcript degradation and interacts with the Ccr4p-Pop2p-Not deadenylase complex. RNA 14: 1328-1336.
47. Rittershaus, P.C., Kechichian, T.B., Allegood, J.C., Merrill, A.H., Jr, Hennig, M., Luberto, C., and Del Poeta, M. (2006) Glucosylceramide synthase is an essential regulator of pathogenicity of Cryptococcus neoformans. J Clin Invest 116: 1651-1659.
48. Roelants, F.M., Torrance, P.D., and Thorner, J. (2004) Differential roles of PDK1- and PDK2-phosphorylation sites in the yeast AGC kinases Ypk1, Pkc1 and Sch9. Microbiology 150: 3289-3304.
49. Runner, V.M., Podolny, V., and Buratowski, S. (2008) The Rpb4 subunit of RNA polymerase II contributes to cotranscriptional recruitment of 3′ processing factors. Mol Cell Biol 28: 1883-1891.
50. Serrano, R., Martin, H., Casamayor, A., and Arino, J. (2006) Signaling alkaline pH stress in the yeast Saccharomyces cerevisiae through the Wsc1 cell surface sensor and the Slt2 MAPK pathway. J Biol Chem 281: 39785-39795.
51. Shalem, O., Groisman, B., Choder, M., Dahan, O., and Pilpel, Y. (2011) Transcriptome kinetics is governed by a genome-wide coupling of mRNA production and degradation: a role for RNA Pol II. PLoS Genet 7: e1002273.
52. Sheth, U., and Parker, R. (2003) Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science 300: 805-808.
53. Sun, Y., Miao, Y., Yamane, Y., Zhang, C., Shokat, K.M., Takematsu, H., etal. (2012) Orm protein phosphoregulation mediates transient sphingolipid biosynthesis response to heat stress via the Pkh-Ypk and Cdc55-PP2A pathways. Mol Biol Cell 23: 2388-2398.
54. Toffaletti, D.L., Rude, T.H., Johnston, S.A., Durack, D.T., and Perfect, J.R. (1993) Gene transfer in Cryptococcus neoformans by use of biolistic delivery of DNA. J Bacteriol 175: 1405-1411.
55. Ujvári, A., and Luse, D.S. (2006) RNA emerging from the active site of RNA polymerase II interacts with the Rpb7 subunit. Nat Struct Mol Biol 13: 49-54.
56. Wiederhold, K., and Passmore, L.A. (2010) Cytoplasmic deadenylation: regulation of mRNA fate. Biochem Soc Trans 38: 1531-1536.