Comparative analysis of programmed cell death pathways in filamentous fungi

BMC Genomics

Volumn 6, Issue , 2005, Pages

  Fedorova, Natalie D ^a   Badger, Jonathan H ^a   Robson, Geoff D ^b   Wortman, Jennifer R ^a   Nierman, William C ^a,c  

^a J CRAIG VENTER INSTITUTE   (United States)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL ENZYME; FUNGAL PROTEIN;

APOPTOSIS; ARTICLE; ASPERGILLOSIS; ASPERGILLUS; CELL CYCLE; CELL MATURATION; CONTROLLED STUDY; FUNGAL CELL; FUNGAL GENE; GENETIC CONSERVATION; GENETIC INCOMPATIBILITY; GENETIC LINE; HETEROKARYON; MAMMAL; METAZOON; MYCOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; NUTRIENT AVAILABILITY; PHYLOGENY; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; SACCHAROMYCES CEREVISIAE; SEX DIFFERENTIATION; SIGNAL TRANSDUCTION; SPECIES; SPECIES DIFFERENCE; STRESS; AMINO ACID SEQUENCE; ANIMAL; ASPERGILLUS FUMIGATUS; BIOLOGICAL MODEL; COMPARATIVE STUDY; FUNGAL GENOME; FUNGUS; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; MOUSE; PHAGOCYTOSIS; PHYSIOLOGY; PROTEIN CONFORMATION;

ASPERGILLUS; ASPERGILLUS FUMIGATUS; FUNGI; MAMMALIA; METAZOA; SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; ASPERGILLUS FUMIGATUS; FUNGI; GENES, FUNGAL; GENOME, FUNGAL; HUMANS; MICE; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; MYCOSES; PHAGOCYTOSIS; PHYLOGENY; PROTEIN CONFORMATION; SACCHAROMYCES CEREVISIAE;

EID: 29244443634     PISSN: 14712164     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-6-177     Document Type: Article

References (86)

1. Latge JP: Aspergillus fumigatus and aspergillosis. Clin Microbiol Rev 1999, 12:310-350.
2. Wilson DM, Mubatanhema W, Jurjevic Z: Biology and ecology of mycotoxigenic Aspergillus species as related to economic and health concerns. Adv Exp Med Biol 2002, 504:3-17.
3. Gupta AK, Tomas E: New antifungal agents. Dermatol Clin 2003, 21:565-576.
4. Cheng J, Park TS, Chio LC, Fischl AS, Ye XS: Induction of apoptosis by sphingoid long-chain bases in Aspergillus nidulans. Mol Cell Biol 2003, 23:163-177.
5. Krishnan S, Manavathu EK, Chandrasekar PH: A comparative study of fungicidal activities of voriconazole and amphotericin B against hyphae of Aspergillus fumigatus. J Antimicrob Chemother 2005.
6. Leiter E, Szappanos H, Oberparleiter C, Kaiserer L, Csernoch L, Pusztahelyi T, Emri T, Pocsi I, Salvenmoser W, Marx F: Antifungal protein PAF severely affects the integrity of the plasma membrane of Aspergillus nidulans and induces an apoptosis-like phenotype. Antimicrob Agents Chemother 2005, 49:2445-2453.
7. Mousavi SA, Robson GD: Oxidative and amphotericin B-mediated cell death in the opportunistic pathogen Aspergillus fumigatus is associated with an apoptotic-like phenotype. Microbiology 2004, 150:1937-1945.
8. Pinan-Lucarre B, Paoletti M, Dementhon K, Coulary-Salin B, Clave C: Autophagy is induced during cell death by incompatibility and is essential for differentiation in the filamentous fungus Podospora anserina. Mol Microbiol 2003, 47:321-333.
9. Marek SM, Wu J, Louise Glass N, Gilchrist DG, Bostock RM: Nuclear DNA degradation during heterokaryon incompatibility in Neurospora crassa. Fungal Genet Biol 2003, 40:126-137.
10. Jacobson DJ, Beurkens K, Klomparens KL: Microscopic and Ultrastructural Examination of Vegetative Incompatibility in Partial Diploids Heterozygous at het Loci in Neurospora crassa. Fungal Genet Biol 1998, 23:45-56.
11. Dementhon K, Paoletti M, Pinan-Lucarre B, Loubradou-Bourges N, Sabourin M, Saupe SJ, Clave C: Rapamycin mimics the incompatibility reaction in the fungus Podospora anserina. Eukaryot Cell 2003, 2:238-246.
12. Glass NL, Rasmussen C, Roca MG, Read ND: Hyphal homing, fusion and mycelial interconnectedness. Trends Microbiol 2004, 12:135-141.
13. Glass NL, Jacobson DJ, Shiu PK: The genetics of hyphal fusion and vegetative incompatibility in filamentous ascomycete fungi. Annu Rev Genet 2000, 34:165-186.
14. Saupe SJ, Clave C, Begueret J: Vegetative incompatibility in filamentous fungi: Podospora and Neurospora provide some clues. Curr Opin Microbiol 2000, 3:608-612.
15. Saupe SJ: Molecular genetics of heterokaryon incompatibility in filamentous ascomycetes. Microbiol Mol Biol Rev 2000, 64:489-502.
16. Saenz GS, Stam JG, Jacobson DJ, Natvig DO: Heteroallelism at the het-c locus contributes to sexual dysfunction in outcrossed strains of Neurospora tetrasperma. Fungal Genet Biol 2001, 34:123-129.
17. Biella S, Smith ML, Aist JR, Cortesi P, Milgroom MG: Programmed cell death correlates with virus transmission in a filamentous fungus. Proc Biol Sci 2002, 269:2269-2276.
18. Coustou V, Deleu C, Saupe S, Begueret J: The protein product of the het-s heterokaryon incompatibility gene of the fungus Podospora anserina behaves as a prion analog. Proc Natl Acad Sci U S A 1997, 94:9773-9778.
19. Mir-Rashed N, Jacobson DJ, Dehghany MR, Micali OC, Smith ML: Molecular and functional analyses of incompatibility genes at het-6 in a population of Neurospora crassa. Fungal Genet Biol 2000, 30:197-205.
20. Milgroom MG, Cortesi P: Analysis of population structure of the chestnut blight fungus based on vegetative incompatibility genotypes. Proc Natl Acad Sci USA 1999, 96:10518-10523.
21. Saupe SJ, Clave C, Sabourin M, Begueret J: Characterization of hch, the Podospora anserina homolog of the het-c heterokaryon incompatibility gene of Neurospora crassa. Curr Genet 2000, 38:39-47.
22. Wu J, Saupe SJ, Glass NL: Evidence for balancing selection operating at the het-c heterokaryon incompatibility locus in a group of filamentous fungi. Proc Natl Acad Sci U S A 1998, 95:12398-12403.
23. Sarkar S, Iyer G, Wu J, Glass NL: Nonself recognition is mediated by HET-C heterocomplex formation during vegetative incompatibility. Embo J 2002, 21:4841-4850.
24. Saupe S, Turcq B, Begueret J: A gene responsible for vegetative incompatibility in the fungus Podospora anserina encodes a protein with a GTP-binding motif and G beta homologous domain. Gene 1995, 162:135-139.
25. Anwar MM, Croft JH, Dales RB: Analysis of heterokaryon incompatibility between heterokaryon-compatibility (h-c) groups R and GL provides evidence that at least eight het loci control somatic incompatibility in Aspergillus nidulans. J Gen Microbiol 1993, 139:1599-1603.
26. Saupe S, Descamps C, Turcq B, Begueret J: Inactivation of the Podospora anserina vegetative incompatibility locus het-c, whose product resembles a glycolipid transfer protein, drastically impairs ascospore production. Proc Natl Acad Sci U S A 1994, 91:5927-5931.
27. Rao CS, Lin X, Pike HM, Molotkovsky JG, Brown RE: Glycolipid transfer protein mediated transfer of glycosphingolipids between membranes: a model for action based on kinetic and thermodynamic analyses. Biochemistry 2004, 43:13805-13815.
28. Brodersen P, Petersen M, Pike HM, Olszak B, Skov S, Odum N, Jorgensen LB, Brown RE, Mundy J: Knockout of Arabidopsis accelerated-cell-death11 encoding a sphingosine transfer protein causes activation of programmed cell death and defense. Genes Dev 2002, 16:490-502.
29. Cheng J, Park TS, Fischl AS, Ye XS: Cell cycle progression and cell polarity require sphingolipid biosynthesis in Aspergillus nidulans. Mol Cell Biol 2001, 21:6198-6209.
30. Mattjus P, Turcq B, Pike HM, Molotkovsky JG, Brown RE: Glycolipid intermembrane transfer is accelerated by HET-C2, a filamentous fungus gene product involved in the cell-cell incompatibility response. Biochemistry 2003, 42:535-542.
31. Saupe SJ, Kuldau GA, Smith ML, Glass NL: The product of the het-C heterokaryon incompatibility gene of Neurospora crassa has characteristics of a glycine-rich cell wall protein. Genetics 1996, 143:1589-1600.
32. Davies JR, Osmani AH, De Souza CP, Bachewich C, Osmani SA: Potential link between the NIMA mitotic kinase and nuclear membrane fission during mitotic exit in Aspergillus nidulans. Eukaryot Cell 2004, 3:1433-1444.
33. Smith ML, Micali OC, Hubbard SP, Mir-Rashed N, Jacobson DJ, Glass NL: Vegetative incompatibility in the het-6 region of Neurospora crassa is mediated by two linked genes. Genetics 2000, 155:1095-1104.
34. Deleu C, Clave C, Begueret J: A single amino acid difference is sufficient to elicit vegetative incompatibility in the fungus Podospora anserina. Genetics 1993, 135:45-52.
35. Anantharaman V, Aravind L: New connections in the prokaryotic toxin-antitoxin network: relationship with the eukaryotic nonsense-mediated RNA decay system. Genome Biol 2003, 4:R81.
36. Balguerie A, Dos Reis S, Ritter C, Chaignepain S, Coulary-Salin B, Forge V, Bathany K, Lascu I, Schmitter JM, Riek R, Saupe SJ: Domain organization and structure-function relationship of the HET-s prion protein of Podospora anserina. Embo J 2003, 22:2071-2081.
37. Dalstra HJ, Swart K, Debets AJ, Saupe SJ, Hoekstra RF: Sexual transmission of the [Het-S] prion leads to meiotic drive in Podospora anserina. Proc Natl Acad Sci USA 2003, 100:6616-6621.
38. Balguerie A, Dos Reis S, Coulary-Salin B, Chaignepain S, Sabourin M, Schmitter JM, Saupe SJ: The sequences appended to the amyloid core region of the HET-s prion protein determine higher-order aggregate organization in vivo. J Cell Sci 2004, 117:2599-2610.
39. Leipe DD, Koonin EV, Aravind L: STAND, a class of P-loop NTPases including animal and plant regulators of programmed cell death: multiple, complex domain architectures, unusual phyletic patterns, and evolution by horizontal gene transfer. J Mol Biol 2004, 343:1-28.
40. Graziani S, Silar P, Daboussi MJ: Bistability and hysteresis of the 'Secteur' differentiation are controlled by a two-gene locus in Nectria haematococca. BMC Biol 2004, 2:18.
41. Espagne E, Balhadere P, Penin ML, Barreau C, Turcq B: HET-E and HET-D belong to a new subfamily of WD40 proteins involved in vegetative incompatibility specificity in the fungus Podospora anserina. Genetics 2002, 161:71-81.
42. Girardin SE, Sansonetti PJ, Philpott DJ: Intracellular vs extracellular recognition of pathogens - common concepts in mammals and flies. Trends Microbiol 2002, 10:193-199.
43. Belkhadir Y, Subramaniam R, Dangl JL: Plant disease resistance protein signaling: NBS-LRR proteins and their partners. Curr Opin Plant Biol 2004, 7:391-399.
44. van der Biezen EA, Jones JD: The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals. Curr Biol 1998, 8:R226-227.
45. Mushegian AR, Koonin EV: Unexpected sequence similarity between nucleosidases and phosphoribosyltransferases of different specificity. Protein Sci 1994, 3:1081-1088.
46. Beeston AL, Surette MG: pfs-dependent regulation of autoinducer 2 production in Salmonella enterica serovar Typhimurium. J Bacteriol 2002, 184:3450-3456.
47. Avila MA, Garcia-Trevijano ER, Lu SC, Corrales FJ, Mato JM: Methylthioadenosine. Int J Biochem Cell Biol 2004, 36:2125-2130.
48. Bok JW, Keller NP: LaeA, a regulator of secondary metabolism in Aspergillus spp. Eukaryot Cell 2004, 3:527-535.
49. Bok JW, Balajee SA, Marr KA, Andes D, Nielsen KF, Frisvad JC, Keller NP: LaeA, a Regulator of Morphogenetic Fungal Virulence Factors. Eukaryot Cell 2005, 4:1574-1582.
50. Xiang Q, Glass NL: The control of mating type heterokaryon incompatibility by vib-1, a locus involved in het-c heterokaryon incompatibility in Neurospora crassa. Fungal Genet Biol 2004, 41:1063-1076.
51. Barreau C, Iskandar M, Loubradou G, Levallois V, Begueret J: The mod-A suppressor of nonallelic heterokaryon incompatibility in Podospora anserina encodes a proline-rich polypeptide involved in female organ formation. Genetics 1998, 149:915-926.
52. Loubradou G, Begueret J, Turcq B: MOD-D, a Galpha subunit of the fungus Podospora anserina, is involved in both regulation of development and vegetative incompatibility. Genetics 1999, 152:519-528.
53. Loubradou G, Begueret J, Turcq B: A mutation in an HSP90 gene affects the sexual cycle and suppresses vegetative incompatibility in the fungus Podospora anserina. Genetics 1997, 147:581-588.
54. Marx F, Haas H, Hofer S, Stoffler G, Redl B: Sequence and structure of Penicillium chrysogenum phoG, homologous to an acid phosphatase-encoding gene of Aspergillus nidulans. Gene 1995, 160:137-138.
55. MacRae WD, Buxton FP, Sibley S, Garven S, Gwynne DI, Davies RW, Arst HN, Jr.: A phosphate-repressible acid phosphatase gene from Aspergillus niger: its cloning, sequencing and transcriptional analysis. Gene 1988, 71:339-348.
56. Hepworth SR, Friesen H, Segall J: NDT80 and the meiotic recombination checkpoint regulate expression of middle sporulation-specific genes in Saccharomyces cerevisiae. Mol Cell Biol 1998, 18:5750-5761.
57. Han KH, Seo JA, Yu JH: Regulators of G-protein signalling in Aspergillus nidulans: RgsA downregulates stress response and stimulates asexual sporulation through attenuation of GanB (Galpha) signalling. Mol Microbiol 2004, 53:529-540.
58. Liebmann B, Muller M, Braun A, Brakhage AA: The cyclic AMP-dependent protein kinase a network regulates development and virulence in Aspergillus fumigatus. Infect Immun 2004, 72:5193-5203.
59. Xiang Q, Glass NL: Identification of vib-1, a locus involved in vegetative incompatibility mediated by het-c in Neurospora crassa. Genetics 2002, 162:89-101.
60. Loubradou G, Begueret J, Turcq B: An additional copy of the adenylate cyclase-encoding gene relieves developmental defects produced by a mutation in a vegetative incompatibility-controlling gene in Podospora anserina. Gene 1996, 170:119-123.
61. Szent-Gyorgyi C: A bipartite operator interacts with a heat shock element to mediate early meiotic induction of Saccharomyces cerevisiae HSP82. Mol Cell Biol 1995, 15:6754-6769.
62. Patil C, Walter P: Intracellular signaling from the endoplasmic reticulum to the nucleus: the unfolded protein response in yeast and mammals. Curr Opin Cell Biol 2001, 13:349-355.
63. Dementhon K, Saupe SJ, Clave C: Characterization of IDI-4, a bZIP transcription factor inducing autophagy and cell death in the fungus Podospora anserina. Mol Microbiol 2004, 53:1625-1640.
64. Dementhon K, Saupe SJ: DNA-binding specificity of the IDI-4 basic leucine zipper factor of Podospora anserina defined by systematic evolution of ligands by exponential enrichment (SELEX). Eukaryot Cell 2005, 4:476-483.
65. Bourges N, Groppi A, Barreau C, Clave C, Begueret J: Regulation of gene expression during the vegetative incompatibility reaction in Podospora anserina. Characterization of three induced genes. Genetics 1998, 150:633-641.
66. Reichard U, Cole GT, Hill TW, Ruchel R, Monod M: Molecular characterization and influence on fungal development of ALP2, a novel serine proteinase from Aspergillus fumigatus. Int J Med Microbiol 2000, 290:549-558.
67. Strittmatter AW, Irniger S, Braus GH: Induction of jlbA mRNA synthesis for a putative bZIP protein of Aspergillus nidulans by amino acid starvation. Curr Genet 2001, 39:327-334.
68. Kamada Y, Sekito T, Ohsumi Y: Autophagy in yeast: a TOR-mediated response to nutrient starvation. Curr Top Microbiol Immunol 2004, 279:73-84.
69. Mousavi SA, Robson GD: 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 Genet Biol 2003, 39:221-229.
70. Thrane C, Kaufmann U, Stummann BM, Olsson S: Activation of caspase-like activity and poly (ADP-ribose) polymerase degradation during sporulation in Aspergillus nidulans. Fungal Genet Biol 2004, 41:361-368.
71. Goldman GH, McGuire SL, Harris SD: The DNA damage response in filamentous fungi. Fungal Genet Biol 2002, 35:183-195.
72. Burhans WC, Weinberger M, Marchetti MA, Ramachandran L, D'Urso G, Huberman JA: Apoptosis-like yeast cell death in response to DNA damage and replication defects. Mutat Res 2003, 532:227-243.
73. Eisler H, Frohlich KU, Heidenreich E: Starvation for an essential amino acid induces apoptosis and oxidative stress in yeast. Exp Cell Res 2004, 300:345-353.
74. Ligr M, Velten I, Frohlich E, Madeo F, Ledig M, Frohlich KU, Wolf DH, Hilt W: The proteasomal substrate Stm1 participates in apoptosis-like cell death in yeast. Mol Biol Cell 2001, 12:2422-2432.
75. Madeo F, Herker E, Wissing S, Jungwirth H, Eisenberg T, Frohlich KU: Apoptosis in yeast. Curr Opin Microbiol 2004, 7:655-660.
76. Hong SJ, Dawson TM, Dawson VL: Nuclear and mitochondrial conversations in cell death: PARP-1 and AIF signaling. Trends Pharmacol Sci 2004, 25:259-264.
77. Aravind L, Dixit VM, Koonin EV: Apoptotic molecular machinery: vastly increased complexity in vertebrates revealed by genome comparisons. Science 2001, 291:1279-1284.
78. Koonin EV, Aravind L: Origin and evolution of eukaryotic apoptosis: the bacterial connection. Cell Death Differ 2002, 9:394-404.
79. Koonin EV, Galperin MY: Comparative Genomics and New Evolutionary Biology. In Sequence - Evolution - Function. First edition. Boston, Dordrecht, London: Kluwer Academic Press; 2002: 227-294
80. Aravind L, Dixit VM, Koonin EV: The domains of death: evolution of the apoptosis machinery. Trends Biochem Sci 1999, 24:47-53.
81. Gene Ontology [http://www.geneontology.org]
82. Apoptosis database [http://www.apoptosis-db.org]
83. HMMer package [http://hmmer.wustl.edu]
84. Edgar RC: MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 2004, 5:113.
85. Howe K, Bateman A, Durbin R: QuickTree: building huge Neighbour-Joining trees of protein sequences. Bioinformatics 2002, 18:1546-1547.
86. Retief JD: Phylogenetic analysis using PHYLIP. Methods Mol Biol 2000, 132:243-258.