Polysome profiling reveals broad translatome remodeling during endoplasmic reticulum (ER) stress in the pathogenic fungus Aspergillus fumigatus

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Krishnan, Karthik ^a   Ren, Zhaowei ^b   Losada, Liliana ^c   Nierman, William C ^c   Lu, Long J ^b   Askew, David S ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^c J CRAIG VENTER INSTITUTE   (United States)

Author keywords

Aspergillus fumigatus; ER stress; Polysome profiling; Translational regulation; Unfolded protein response; UPR; Yvc1

Indexed keywords

DITHIOTHREITOL; ERGOSTEROL; MESSENGER RNA; RNA; TRANSLATOME; TUNICAMYCIN; UNCLASSIFIED DRUG;

ADAPTATION; ARTICLE; ASPERGILLUS FUMIGATUS; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; FUNGAL CELL WALL; FUNGAL GENE; GENE EXPRESSION REGULATION; GENE POOL; HEAT STRESS; HOMEOSTASIS; HYBRIDIZATION; MICROARRAY ANALYSIS; NONHUMAN; POLYSOME; RIBOSOME; SIGNAL TRANSDUCTION; TRANSLATION REGULATION; UNFOLDED PROTEIN RESPONSE; UPREGULATION; YVC1 GENE;

ASPERGILLUS FUMIGATUS; FUNGI;

ADAPTATION, BIOLOGICAL; ASPERGILLUS FUMIGATUS; CELL MEMBRANE; CELL WALL; CLUSTER ANALYSIS; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; HOT TEMPERATURE; POLYRIBOSOMES; PROTEIN BIOSYNTHESIS; REPRODUCIBILITY OF RESULTS; RNA ISOFORMS; RNA, MESSENGER; SECRETORY PATHWAY; TRANSCRIPTION, GENETIC; UNFOLDED PROTEIN RESPONSE;

EID: 84895468658     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-159     Document Type: Article

References (62)

1. Shoham S, Marr KA. Invasive fungal infections in solid organ transplant recipients. Future Microbiol 2012, 7(5):639-655. 10.2217/fmb.12.28, 22568718.
2. Segal BH. Aspergillosis. N Engl J Med 2009, 360(18):1870-1884. 10.1056/NEJMra0808853, 19403905.
3. Kim A, Nicolau DP, Kuti JL. Hospital costs and outcomes among intravenous antifungal therapies for patients with invasive Aspergillosis in the United States. Mycoses 2011, 54(5):e301-312. 10.1111/j.1439-0507.2010.01903.x, 20557463.
4. Wilson LS, Reyes CM, Stolpman M, Speckman J, Allen K, Beney J. The direct cost and incidence of systemic fungal infections. Value Health 2002, 5(1):26-34. 10.1046/j.1524-4733.2002.51108.x, 11873380.
5. Lin SJ, Schranz J, Teutsch SM. Aspergillosis case-fatality rate: systematic review of the literature. Clin Infect Dis 2001, 32(3):358-366. 10.1086/318483, 11170942.
6. Feng X, Krishnan K, Richie DL, Aimanianda V, Hartl L, Grahl N, Powers-Fletcher MV, Zhang M, Fuller KK, Nierman WC, et al. HacA-independent functions of the ER stress sensor IreA synergize with the canonical UPR to influence virulence traits in Aspergillus fumigatus. PLoS Pathog 2011, 7(10):e1002330. 10.1371/journal.ppat.1002330, 3197630, 22028661.
7. Richie DL, Hartl L, Aimanianda V, Winters MS, Fuller KK, Miley MD, White S, McCarthy JW, Latge JP, Feldmesser M, et al. A role for the unfolded protein response (UPR) in virulence and antifungal susceptibility in Aspergillus fumigatus. PLoS Pathog 2009, 5(1):e1000258. 10.1371/journal.ppat.1000258, 2606855, 19132084.
8. Cheon SA, Jung KW, Chen YL, Heitman J, Bahn YS, Kang HA. Unique evolution of the UPR pathway with a novel bZIP transcription factor, Hxl1, for controlling pathogenicity of Cryptococcus neoformans. PLoS Pathog 2011, 7(8):e1002177. 10.1371/journal.ppat.1002177, 3154848, 21852949.
9. Joubert A, Simoneau P, Campion C, Bataille-Simoneau N, Iacomi-Vasilescu B, Poupard P, Francois JM, Georgeault S, Sellier E, Guillemette T. Impact of the unfolded protein response on the pathogenicity of the Neurotrophic fungus Alternaria brassicicola. Mol Microbiol 2011, 79(5):1305-1324. 10.1111/j.1365-2958.2010.07522.x, 21251090.
10. Miyazaki T, Nakayama H, Nagayoshi Y, Kakeya H, Kohno S. Dissection of Ire1 functions reveals stress response mechanisms uniquely evolved in Candida glabrata. PLoS Pathog 2013, 9(1):e1003160. 10.1371/journal.ppat.1003160, 3561209, 23382685.
11. Gardner BM, Pincus D, Gotthardt K, Gallagher CM, Walter P. Endoplasmic reticulum stress sensing in the unfolded protein response. Cold Spring Harbor Perspect Biol 2013, 5(3):a013169.
12. Wimalasena TT, Enjalbert B, Guillemette T, Plumridge A, Budge S, Yin Z, Brown AJ, Archer DB. 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 2008, 45(9):1235-1247. 10.1016/j.fgb.2008.06.001, 18602013.
13. Hartmann T, Sasse C, Schedler A, Hasenberg M, Gunzer M, Krappmann S. Shaping the fungal adaptome-stress responses of Aspergillus fumigatus. Int J Med Microbiol 2011, 301(5):408-416. 10.1016/j.ijmm.2011.04.008, 21565548.
14. Kohno K. Stress-sensing mechanisms in the unfolded protein response: similarities and differences between yeast and mammals. J Biochem 2010, 147(1):27-33. 10.1093/jb/mvp196, 19942680.
15. Kimata Y, Oikawa D, Shimizu Y, Ishiwata-Kimata Y, Kohno K. A role for BiP as an adjustor for the endoplasmic reticulum stress-sensing protein Ire1. J Cell Biol 2004, 167(3):445-456. 10.1083/jcb.200405153, 2172501, 15520230.
16. Gardner BM, Walter P. Unfolded proteins are Ire1-activating ligands that directly induce the unfolded protein response. Science 2011, 333(6051):1891-1894. 10.1126/science.1209126, 3202989, 21852455.
17. Kimata Y, Ishiwata-Kimata Y, Ito T, Hirata A, Suzuki T, Oikawa D, Takeuchi M, Kohno K. Two regulatory steps of ER-stress sensor Ire1 involving its cluster formation and interaction with unfolded proteins. J Cell Biol 2007, 179(1):75-86. 10.1083/jcb.200704166, 2064738, 17923530.
18. Credle JJ, Finer-Moore JS, Papa FR, Stroud RM, Walter P. On the mechanism of sensing unfolded protein in the endoplasmic reticulum. Proc Natl Acad Sci USA 2005, 102(52):18773-18784. 10.1073/pnas.0509487102, 1316886, 16365312.
19. Korennykh AV, Egea PF, Korostelev AA, Finer-Moore J, Zhang C, Shokat KM, Stroud RM, Walter P. The unfolded protein response signals through high-order assembly of Ire1. Nature 2009, 457(7230):687-693. 10.1038/nature07661, 2846394, 19079236.
20. Shamu CE, Walter P. Oligomerization and phosphorylation of the Ire1p kinase during intracellular signaling from the endoplasmic reticulum to the nucleus. EMBO J 1996, 15(12):3028-3039. 450244, 8670804.
21. Gygi SP, Rochon Y, Franza BR, Aebersold R. Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 1999, 19(3):1720-1730. 83965, 10022859.
22. Washburn MP, Koller A, Oshiro G, Ulaszek RR, Plouffe D, Deciu C, Winzeler E, Yates JR. Protein pathway and complex clustering of correlated mRNA and protein expression analyses in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 2003, 100(6):3107-3112. 10.1073/pnas.0634629100, 152254, 12626741.
23. Greenbaum D, Colangelo C, Williams K, Gerstein M. Comparing protein abundance and mRNA expression levels on a genomic scale. Genome Biol 2003, 4(9):117. 10.1186/gb-2003-4-9-117, 193646, 12952525.
24. Gebauer F, Hentze MW. Molecular mechanisms of translational control. Nat Rev Mol Cell Biol 2004, 5(10):827-835. 10.1038/nrm1488, 15459663.
25. Halbeisen RE, Gerber AP. Stress-dependent coordination of transcriptome and translatome in yeast. PLoS Biol 2009, 7(5):e1000105. 2675909, 19419242.
26. Beilharz TH, Preiss T. Translational profiling: the genome-wide measure of the nascent proteome. Brief Funct Genom Proteom 2004, 3(2):103-111.
27. Payne T, Hanfrey C, Bishop AL, Michael AJ, Avery SV, Archer DB. Transcript-specific translational regulation in the unfolded protein response of Saccharomyces cerevisiae. FEBS Lett 2008, 582(4):503-509. 10.1016/j.febslet.2008.01.009, 18206654.
28. Guillemette T, van Peij NN, Goosen T, Lanthaler K, Robson GD, van den Hondel CA, Stam H, Archer DB. Genomic analysis of the secretion stress response in the enzyme-producing cell factory Aspergillus niger. BMC Genomics 2007, 8:158. 10.1186/1471-2164-8-158, 1894978, 17561995.
29. Back SH, Schroder M, Lee K, Zhang K, Kaufman RJ. ER stress signaling by regulated splicing: IRE1/HAC1/XBP1. Methods 2005, 35(4):395-416. 10.1016/j.ymeth.2005.03.001, 15804613.
30. Harding HP, Zhang Y, Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 1999, 397(6716):271-274. 10.1038/16729, 9930704.
31. Korennykh A, Walter P. Structural basis of the unfolded protein response. Ann Rev Cell Dev Biol 2012, 28:251-277.
32. Warner JR, McIntosh KB. How common are extraribosomal functions of ribosomal proteins?. Mol Cell 2009, 34(1):3-11. 10.1016/j.molcel.2009.03.006, 2679180, 19362532.
33. Gastebois A, Clavaud C, Aimanianda V, Latge JP. Aspergillus fumigatus: cell wall polysaccharides, their biosynthesis and organization. Future Microbiol 2009, 4(5):583-595. 10.2217/fmb.09.29, 19492968.
34. Mo C, Bard M. Erg28p is a key protein in the yeast sterol biosynthetic enzyme complex. J Lipid Res 2005, 46(9):1991-1998. 10.1194/jlr.M500153-JLR200, 15995173.
35. Lewis RE, Viale P, Kontoyiannis DP. The potential impact of antifungal drug resistance mechanisms on the host immune response to Candida. Virulence 2012, 3(4):368-376. 10.4161/viru.20746, 3478239, 22722245.
36. Hartland RP, Fontaine T, Debeaupuis JP, Simenel C, Delepierre M, Latge JP. A novel beta-(1-3)-glucanosyltransferase from the cell wall of Aspergillus fumigatus. J Biol Chem 1996, 271(43):26843-26849. 10.1074/jbc.271.43.26843, 8900166.
37. Mouyna I, Morelle W, Vai M, Monod M, Lechenne B, Fontaine T, Beauvais A, Sarfati J, Prevost MC, Henry C, et al. Deletion of GEL2 encoding for a beta(1-3)glucanosyltransferase affects morphogenesis and virulence in Aspergillus fumigatus. Mol Microbiol 2005, 56(6):1675-1688. 10.1111/j.1365-2958.2005.04654.x, 15916615.
38. Li H, Zhou H, Luo Y, Ouyang H, Hu H, Jin C. Glycosylphosphatidylinositol (GPI) anchor is required in Aspergillus fumigatus for morphogenesis and virulence. Mol Microbiol 2007, 64(4):1014-1027. 10.1111/j.1365-2958.2007.05709.x, 17501924.
39. Gastebois A, Fontaine T, Latge JP, Mouyna I. beta(1-3)Glucanosyltransferase Gel4p is essential for Aspergillus fumigatus. Eukaryot Cell 2010, 9(8):1294-1298. 10.1128/EC.00107-10, 2918925, 20543062.
40. Hata K, Horii T, Miyazaki M, Watanabe NA, Okubo M, Sonoda J, Nakamoto K, Tanaka K, Shirotori S, Murai N, et al. Efficacy of oral E1210, a new broad-spectrum antifungal with a novel mechanism of action, in murine models of candidiasis, Aspergillosis, and fusariosis. Antimicrob Agents Chemother 2011, 55(10):4543-4551. 10.1128/AAC.00366-11, 3187015, 21788462.
41. Miyazaki M, Horii T, Hata K, Watanabe NA, Nakamoto K, Tanaka K, Shirotori S, Murai N, Inoue S, Matsukura M, et al. In vitro activity of E1210, a novel antifungal, against clinically important yeasts and molds. Antimicrob Agents Chemother 2011, 55(10):4652-4658. 10.1128/AAC.00291-11, 3186989, 21825291.
42. McLellan CA, Whitesell L, King OD, Lancaster AK, Mazitschek R, Lindquist S. Inhibiting GPI anchor biosynthesis in fungi stresses the endoplasmic reticulum and enhances immunogenicity. ACS Chem Biol 2012, 7(9):1520-1528. 10.1021/cb300235m, 22724584.
43. Bhabhra R, Askew DS. Thermotolerance and virulence of Aspergillus fumigatus: role of the fungal nucleolus. Med Mycol 2005, 43(Suppl 1):S87-S93.
44. Matsumoto R, Akama K, Rakwal R, Iwahashi H. The stress response against denatured proteins in the deletion of cytosolic chaperones SSA1/2 is different from heat-shock response in Saccharomyces cerevisiae. BMC Genomics 2005, 6:141. 10.1186/1471-2164-6-141, 1262714, 16209719.
45. Do JH, Yamaguchi R, Miyano S. Exploring temporal transcription regulation structure of Aspergillus fumigatus in heat shock by state space model. BMC Genomics 2009, 10:306. 10.1186/1471-2164-10-306, 2714559, 19586549.
46. Nierman WC, Pain A, Anderson MJ, Wortman JR, Kim HS, Arroyo J, Berriman M, Abe K, Archer DB, Bermejo C, et al. Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature 2005, 438(7071):1151-1156. 10.1038/nature04332, 16372009.
47. Mulder HJ, Nikolaev I. HacA-dependent transcriptional switch releases hacA mRNA from a translational block upon endoplasmic reticulum stress. Eukaryot Cell 2009, 8(4):665-675. 10.1128/EC.00131-08, 2669205, 19181870.
48. Ruegsegger U, Leber JH, Walter P. Block of HAC1 mRNA translation by long-range base pairing is released by cytoplasmic splicing upon induction of the unfolded protein response. Cell 2001, 107(1):103-114. 10.1016/S0092-8674(01)00505-0, 11595189.
49. Hooks KB, Griffiths-Jones S. Conserved RNA structures in the non-canonical Hac1/Xbp1 intron. RNA Biol 2011, 8(4):552-556. 10.4161/rna.8.4.15396, 3225973, 21593604.
50. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, Harding HP, Clark SG, Ron D. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 2002, 415(6867):92-96. 10.1038/415092a, 11780124.
51. Mulder HJ, Saloheimo M, Penttila M, Madrid SM. The transcription factor HACA mediates the unfolded protein response in Aspergillus niger, and up-regulates its own transcription. Mol Genet Genomics 2004, 271(2):130-140. 10.1007/s00438-003-0965-5, 14730445.
52. Saloheimo M, Valkonen M, Penttila M. Activation mechanisms of the HAC1-mediated unfolded protein response in filamentous fungi. Mol Microbiol 2003, 47(4):1149-1161. 10.1046/j.1365-2958.2003.03363.x, 12581366.
53. Yanagitani K, Imagawa Y, Iwawaki T, Hosoda A, Saito M, Kimata Y, Kohno K. Cotranslational targeting of XBP1 protein to the membrane promotes cytoplasmic splicing of its own mRNA. Mol Cell 2009, 34(2):191-200. 10.1016/j.molcel.2009.02.033, 19394296.
54. Denis V, Cyert MS. Internal Ca(2+) release in yeast is triggered by hypertonic shock and mediated by a TRP channel homologue. J Cell Biol 2002, 156(1):29-34. 10.1083/jcb.200111004, 2173594, 11781332.
55. Krappmann S, Sasse C, Braus GH. Gene targeting in Aspergillus fumigatus by homologous recombination is facilitated in a nonhomologous end- joining-deficient genetic background. Eukaryot Cell 2006, 5(1):212-215. 10.1128/EC.5.1.212-215.2006, 1360265, 16400185.
56. Bhabhra R, Richie DL, Kim HS, Nierman WC, Fortwendel J, Aris JP, Rhodes JC, Askew DS. Impaired ribosome biogenesis disrupts the integration between morphogenesis and nuclear duplication during the germination of Aspergillus fumigatus. Eukaryot Cell 2008, 7(4):575-583. 10.1128/EC.00412-07, 2292631, 18296619.
57. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987, 162(1):156-159.
58. Priebe S, Linde J, Albrecht D, Guthke R, Brakhage AA. FungiFun: a web-based application for functional categorization of fungal genes and proteins. Fungal Genet Biol 2011, 48(4):353-358. 10.1016/j.fgb.2010.11.001, 21073976.
59. Eisen MB, Spellman PT, Brown PO, Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 1998, 95(25):14863-14868. 10.1073/pnas.95.25.14863, 24541, 9843981.
60. Saldanha AJ. Java Treeview-extensible visualization of microarray data. Bioinformatics 2004, 20(17):3246-3248. 10.1093/bioinformatics/bth349, 15180930.
61. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009, 25(9):1105-1111. 10.1093/bioinformatics/btp120, 2672628, 19289445.
62. Trapnell C, Hendrickson DG, Sauvageau M, Goff L, Rinn JL, Pachter L. Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat Biotechnol 2013, 31(1):46-53. 3869392, 23222703.