Transcriptome and Biochemical Analysis Reveals That Suppression of GPI-Anchor Synthesis Leads to Autophagy and Possible Necroptosis in Aspergillus fumigatus

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Yan, Jianghong ^a   Du, Ting ^a   Zhao, Wan ^a   Hartmann, Thomas ^a   Lu, Hua ^a   Lü, Yang ^a   Ouyang, Haomiao ^a   Jiang, Xuejun ^a   Sun, Lei ^b   Jin, Cheng ^a  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b INSTITUTE OF BIOPHYSICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; PHOSPHATIDYLINOSITOL; TRANSCRIPTOME;

ARTICLE; ASPERGILLUS FUMIGATUS; AUTOPHAGY; CALCIUM CELL LEVEL; CELL DEATH; CELL STRUCTURE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; FUNGAL GENE; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE REPRESSION; GENE SYNTHESIS; GENOME ANALYSIS; GPI GENE; NECROPTOSIS; NONHUMAN; SIGNAL TRANSDUCTION;

APOPTOSIS; ASPERGILLUS FUMIGATUS; AUTOPHAGY; CALCIUM; CELL WALL; CYTOSOL; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION PROFILING; GENE ORDER; GLYCOSYLPHOSPHATIDYLINOSITOLS; GPI-LINKED PROTEINS; MEMBRANE PROTEINS; MUTATION; PHOSPHATIDYLINOSITOLS; PROTEIN BIOSYNTHESIS; SIGNAL TRANSDUCTION;

EID: 84875070439     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059013     Document Type: Article

References (64)

1. Lat A, Bhadelia N, Miko B, Furuya EY, Thompson III GR, (2010) Invasive aspergillosis after pandemic (H1N1) 2009. Emerging infectious diseases 16: 971.
2. Bodey GP, Vartivarian S, (1989) Aspergillosis. European Journal of Clinical Microbiology & Infectious Diseases 8: 413-437.
3. Zmeili OS, Soubani AO, (2007) Pulmonary aspergillosis: a clinical update. QJM 100: 317-334.
4. Fontaine T, Simenel C, Dubreucq G, Adam O, Delepierre M, et al. (2000) Molecular organization of the alkali-insoluble fraction of Aspergillus fumigatus cell wall. Journal of Biological Chemistry 275: 27594-27607.
5. Latgé J, Mouyna I, Tekaia F, Beauvais A, Debeaupuis J, et al. (2005) Specific molecular features in the organization and biosynthesis of the cell wall of Aspergillus fumigatus. Medical Mycology 43: 15-22.
6. Upadhyay S, Shaw BD, (2006) A phos oglucose isomerase mutant in Aspergillus nidulans is defective in hyphal polarity and conidiation. Fungal Genetics and Biology 43: 739-751.
7. Mouyna I, Fontaine T, Vai M, Monod M, Fonzi WA, et al. (2000) Glycosylphosphatidylinositol-anchored glucanosyltransferases play an active role in the biosynthesis of the fungal cell wall. Journal of Biological Chemistry 275: 14882-14889.
8. Mouyna I, Morelle W, Vai M, Monod M, Léchenne B, et al. (2005) Deletion of GEL2 encoding for a β (1-3) glucanosyltransferase affects morphogenesis and virulence in Aspergillus fumigatus. Molecular Microbiology 56: 1675-1688.
9. Bruneau JM, Magnin T, Tagat E, Legrand R, Bernard M, et al. (2001) Proteome analysis of Aspergillus fumigatus identifies glycosylphosphatidylinositol- anchored proteins associated to the cell wall biosynthesis. Electrophoresis 22: 2812-2823.
10. Chabane S, Sarfati J, Ibrahim-Granet O, Du C, Schmidt C, et al. (2006) Glycosylphosphatidylinositol-anchored Ecm33p influences conidial cell wall biosynthesis in Aspergillus fumigatus. Applied and Environmental Microbiology 72: 3259-3267.
11. Romano J, Nimrod G, Ben-Tal N, Shadkchan Y, Baruch K, et al. (2006) Disruption of the Aspergillus fumigatus ECM33 homologue results in rapid conidial germination, antifungal resistance and hypervirulence. Microbiology 152: 1919-1928.
12. De Groot PWJ, Ram AF, Klis FM, (2005) Features and functions of covalently linked proteins in fungal cell walls. Fungal Genetics and Biology 42: 657-675.
13. Li H, Zhou H, Luo Y, Ouyang H, Hu H, et al. (2007) Glycosylphosphatidylinositol (GPI) anchor is required in Aspergillus fumigatus for morphogenesis and virulence. Molecular Microbiology 64: 1014-1027.
14. Gastebois A, Fontaine T, Latgé JP, Mouyna I, (2010) β (1-3) glucanosyltransferase Gel4p is essential for Aspergillus fumigatus. Eukaryotic Cell 9: 1294-1298.
15. Eisenhaber B, Maurer-Stroh S, Novatchkova M, Schneider G, Eisenhaber F, (2003) Enzymes and auxiliary factors for GPI lipid anchor biosynthesis and post-translational transfer to proteins. Bioessays 25: 367-385.
16. Ohishi K, Inoue N, Maeda Y, Takeda J, Riezman H, et al. (2000) Gaa1p and gpi8p are components of a glycosylphosphatidylinositol (GPI) transamidase that mediates attachment of GPI to proteins. Molecular Biology of the Cell 11: 1523-1533.
17. Takeda J, Miyata T, Kawagoe K, Iida Y, Endo Y, et al. (1993) Deficiency of the GPI anchor caused by a somatic mutation of the PIG-A gene in paroxysmal nocturnal hemoglobinuria. Cell 73: 703-711.
18. Leidich SD, Kostova Z, Latek RR, Costello LC, Drapp DA, et al. (1995) Temperature-sensitive Yeast GPI Anchoring Mutants gpi2 and gpi3 Are Defective in the Synthesis of N-Acetylglucosaminyl Phosphatidylinositol. Journal of Biological Chemistry 270: 13029-13035.
19. Xia G, Jin C, Zhou J, Yang S, Zhang S, et al. (2001) A novel chitinase having a unique mode of action from Aspergillus fumigatus YJ-407. European Journal of Biochemistry 268: 4079-4085.
20. Weidner G, d'Enfert C, Koch A, Mol PC, Brakhage AA, (1998) Development of a homologous transformation system for the human pathogenic fungus Aspergillus fumigatus based on the pyrG gene encoding orotidine 5′-monophosphate decarboxylase. Current Genetics 33: 378-385.
21. Cove D, (1966) The induction and repression of nitrate reductase in the fungus Aspergillus nidulans. Biochimica et Biophysica Acta 113: 51.
22. Waring RB, May GS, Morris NR, (1989) Characterization of an inducible expression system in Aspergillus nidulans using alcA and tubulincoding genes. Gene 79: 119-130.
23. Langfelder K, Gattung S, Brakhage A, (2002) A novel method used to delete a new Aspergillus fumigatus ABC transporter-encoding gene. Current Genetics 41: 268-274.
24. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ, (1951) Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193: 265-275.
25. Elorza MV, Murgui A, Sentandreu R, (1985) Dimorphism in Candida albicans: contribution of mannoproteins to the architecture of yeast and mycelial cell walls. Journal of General Microbiology 131: 2209-2216.
26. Hearn V, Sietsma J, (1994) Chemical and immunological analysis of the Aspergillus fumigatus cell wall. Microbiology 140: 789-795.
27. Schoffelmeer E, Klis F, Sietsma J, Cornelissen B, (1999) The cell wall of Fusarium oxysporum. Fungal Genetics and Biology 27: 275-282.
28. Dubois M, Gilles KA, Hamilton JK, Rebers P, Smith F, (1956) Colorimetric method for determination of sugars and related substances. Analytical Chemistry 28: 350-356.
29. Lee JI, Yu YM, Rho YM, Park BC, Choi JH, et al. (2005) Differential expression of the chsE gene encoding a chitin synthase of Aspergillus nidulans in response to developmental status and growth conditions. FEMS Microbiology Letters 249: 121-129.
30. Mousavi SAA, Robson GD, (2003) Entry into the stationary phase is associated with a rapid loss of viability and an apoptotic-like phenotype in the opportunistic pathogen Aspergillus fumigatus. Fungal Genetics and Biology 39: 221-229.
31. Marion MB, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72: 248-254.
32. Romero B, Turner G, Olivas I, Laborda F, de Lucas RJ, (2003) The Aspergillus nidulans alcA promoter drives tightly regulated conditional gene expression in Aspergillus fumigatus permitting validation of essential genes in this human pathogen. Fungal Genetics and Biology 40: 103-114.
33. Valiante V, Jain R, Heinekamp T, Brakhage AA, (2009) The MpkA MAP kinase module regulates cell wall integrity signaling and pyomelanin formation in Aspergillus fumigatus. Fungal Genetics and Biology 46: 909-918.
34. Dichtl K, Helmschrott C, Dirr F, Wagener J, (2012) Deciphering cell wall integrity signalling in Aspergillus fumigatus: identification and functional characterization of cell wall stress sensors and relevant Rho GTPases. Molecular Microbiology.
35. Zhang L, Feng D, Fang W, Ouyang H, Luo Y, et al. (2009) Comparative proteomic analysis of an Aspergillus fumigatus mutant deficient in glucosidase I (AfCwh41). Microbiology 155(7): 2157-67.
36. Richie DL, Hartl L, Aimanianda V, Winters MS, Fuller KK, et al. (2009) A role for the unfolded protein response (UPR) in virulence and antifungal susceptibility in Aspergillus fumigatus. Plos Pahtogens 5.
37. He C, Klionsky DJ, (2009) Regulation mechanisms and signaling pathways of autophagy. Annual Review of Genetics 43: 67.
38. Abraham RT, Wiederrecht GJ, (1996) Immunopharmacology of rapamycin 1. Annual Review of Immunology 14: 483-510.
39. Cameron AM, Nucifora Jr FC, Fung ET, Livingston DJ, Aldape RA, et al. (1997) FKBP12 binds the inositol 1, 4, 5-trisphosphate receptor at leucine-proline (1400-1401) and anchors calcineurin to this FK506-like domain. Journal of Biological Chemistry 272: 27582-27588.
40. Cameron AM, Steiner JP, Roskams AJ, Ali SM, Ronnett G, et al. (1995) Calcineurin associated with the inositol 1, 4, 5-trisphosphate receptor-FKBP12 complex modulates Ca2+ flux. Cell 83: 463.
41. Cameron AM, Steiner JP, Sabatini DM, Kaplin AI, Walensky LD, et al. (1995) Immunophilin FK506 binding protein associated with inositol 1, 4, 5-trisphosphate receptor modulates calcium flux. Proceedings of the National Academy of Sciences 92: 1784-1788.
42. Dargan SL, Lea EJA, Dawson AP, (2002) Modulation of type-1 Ins (1, 4, 5) P3 receptor channels by the FK506-binding protein, FKBP12. Biochemical Journal 361: 401.
43. MacMillan D, Currie S, Bradley KN, Muir TC, McCarron JG, (2005) In smooth muscle, FK506-binding protein modulates IP3 receptor-evoked Ca2+ release by mTOR and calcineurin. Journal of Cell Science 118: 5443-5451.
44. Christofferson DE, Yuan J, (2010) Necroptosis as an alternative form of programmed cell death. Current Opinion in Cell Biology 22: 263-268.
45. Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, et al. (2009) Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death and Differentiation 16: 3-11.
46. Carmona-Gutierrez D, Eisenberg T, Büttner S, Meisinger C, Kroemer G, et al. (2010) Apoptosis in yeast: triggers, pathways, subroutines. Cell Death and Differentiation 17: 763-773.
47. Richie DL, Miley MD, Bhabhra R, Robson GD, Rhodes JC, et al. (2007) The Aspergillus fumigatus metacaspases CasA and CasB facilitate growth under conditions of endoplasmic reticulum stress. Molecular Microbiology 63: 591-604.
48. Yang Z, Klionsky DJ, (2009) An overview of the molecular mechanism of autophagy. Autophagy in Infection and Immunity pp. 1-32.
49. Yang Z, Klionsky DJ, (2010) Mammalian autophagy: core molecular machinery and signaling regulation. Current Opinion in Cell Biology 22: 124-131.
50. Vandenabeele P, Galluzzi L, Berghe TV, Kroemer G, (2010) Molecular mechanisms of necroptosis: an ordered cellular explosion. Nature Reviews Molecular Cell Biology 11: 700-714.
51. Hitomi J, Christofferson DE, Ng A, Yao J, Degterev A, et al. (2008) Identification of a molecular signaling network that regulates a cellular necrotic cell death pathway. Cell 135: 1311-1323.
52. Galluzzi L, Vanden BT, Vanlangenakker N, Buettner S, Eisenberg T, et al. (2011) Programmed necrosis from molecules to health and disease. International Review of Cell and Molecular Biology 289: 1.
53. Sun X, Yin J, Starovasnik MA, Fairbrother WJ, Dixit VM, (2002) Identification of a novel homotypic interaction motif required for the phosphorylation of receptor-interacting protein (RIP) by RIP3. Journal of Biological Chemistry 277: 9505-9511.
54. Festjens N, Berghe TV, Cornelis S, Vandenabeele P, (2007) RIP1, a kinase on the crossroads of a cell's decision to live or die. Cell Death and Differentiation 14: 400-410.
55. Jain R, Valiante V, Remme N, Docimo T, Heinekamp T, et al. (2011) The MAP kinase MpkA controls cell wall integrity, oxidative stress response, gliotoxin production and iron adaptation in Aspergillus fumigatus. Molecular Microbiology.
56. Samara C, Syntichaki P, Tavernarakis N, (2007) Autophagy is required for necrotic cell death in Caenorhabditis elegans. Cell Death and Differentiation 15: 105-112.
57. Holler N, Zaru R, Micheau O, Thome M, Attinger A, et al. (2000) Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nature 1: 489-495.
58. Matsumura H, Shimizu Y, Ohsawa Y, Kawahara A, Uchiyama Y, et al. (2000) Necrotic Death Pathway in Fas Receptor Signaling. Cell Biology 151: 1247-1255.
59. Cho YS, Challa S, Moquin D, Genga R, Ray TD, et al. (2009) Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 137: 1112-1123.
60. He S, Wang L, Miao L, Wang T, Du F, et al. (2009) Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-α. Cell 137: 1100-1111.
61. Zhang DW, Shao J, Lin J, Zhang N, Lu BJ, et al. (2009) RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science Signalling 325: 332.
62. Upton JW, Kaiser WJ, Mocarski ES, (2010) Virus inhibition of RIP3-dependent necrosis. Cell Host and Microbe 7: 302-313.
63. Vanlangenakker N, Bertrand M, Bogaert P, Vandenabeele P, Berghe TV, (2011) TNF-induced necroptosis in L929 cells is tightly regulated by multiple TNFR1 complex I and II members. Cell Death and Disease 2: e230.
64. Golstein P, Kroemer G, (2007) A multiplicity of cell death pathways. EMBO Rep 8: 829-833.