The diverse roles of autophagy in medically important fungi

Autophagy

Volumn 4, Issue 8, 2008, Pages 982-988

  Palmer, Glen E ^a   Askew, David S ^b   Williamson, Peter R ^c,d  

^a LOUISIANA STATE UNIVERSITY SCHOOL OF DENTISTRY   (United States)

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

^c UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^d JESSE BROWN VA MEDICAL CENTER   (United States)

Author keywords

Autophagy; Fungus; Human; Infection; Pathogenesis; Virulence

Indexed keywords

ASPERGILLUS FUMIGATUS; AUTOPHAGY; CANDIDA ALBICANS; CRYPTOCOCCUS NEOFORMANS; ENTERIC FEEDING; EVOLUTIONARY ADAPTATION; FUNGAL MORPHOLOGY; FUNGAL VIRULENCE; FUNGUS; HOST CELL; HOST RESISTANCE; HUMAN; INTESTINE INFECTION; MACROPHAGE; MYCOSIS; NONHUMAN; OPPORTUNISTIC INFECTION; PATHOGENESIS; REVIEW;

ASPERGILLUS FUMIGATUS; CANDIDA ALBICANS; EUKARYOTA; FILOBASIDIELLA NEOFORMANS; FUNGI;

EID: 58149091301     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.7075     Document Type: Review

References (65)

1. Edmond M, Wallace S, McClish D, Pfaller M, Jones R, Wenzel R. Nosocomial bloodstream infections in United States hospitals: a three-year analysis. Clin Infect Dis 1999; 29:239-44.
2. Wilson L, Reyes C, Stolpman M, Speckman J, Allen K, Beney J. The direct cost and incidence of systemic fungal infections. Value in Health 2002; 5:26-34.
3. Barnes PD, Marr KA. Aspergillosis: spectrum of disease, diagnosis and treatment. Infect Dis Clin North Am 2006; 20:545-61.
4. Bicanic T, Harrison TS. Cryptococcal meningitis. Br Med Bull 2004; 72:99-118.
5. Bicanic T, Meintjes G, Wood R, Hayes M, Rebe K, Bekker L, Harrison T. Fungal burden, early fungicidal activity, and outcome in cryptococcal meningitis in antiretroviral-naive or antiretroviral-experienced patients treated with amphotericin B or fluconazole. Clin Infect Dis 2007; 45:76-80.
6. Bokazhanova A, Rutherford GW. The epidemiology of HIV and AIDS in the world. Coll Antropol 2006; 30 Suppl 2:3-10.
7. Panepinto J, Williamson P. Intersection of fungal fitness and virulence in Cryptococcus neoformans. FEMS Yeast Res 2006; 6:489-98.
8. Fradin C, Kretschmar M, Nichterlein T, Gaillardin C, d'Enfert C, Hube B. Stage-specific gene expression of Candida albicans in human blood. Mol Microbiol 2003; 47:1523-43.
9. Steen BR, Zuyderduyn S, Toffaletti DL, Marra M, Jones SJ, Perfect JR, Kronstad J. Cryptococcus neoformans gene expression during experimental cryptococcal meningitis. Eukaryot Cell 2003; 2:1336-49.
10. Casadevall A, Pirofski L. The damage-response framework of microbial pathogenesis. Nat Rev Microbiol 2003; 1:17-24.
11. Klionsky DJ. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 2007; 8:931-7.
12. Levine B, Yuan J. Autophagy in cell death: an innocent convict? J Clin Invest 2005; 115:2679-88.
13. Wang CW, Klionsky DJ. The molecular mechanism of autophagy. Mol Med 2003; 9:65-76.
14. Klionsky DJ, Cregg JM, Dunn WA Jr, Emr SD, Sakai Y, Sandoval IV, Sibirny A, Subramani S, Thumm M, Veenhuis M, Ohsumi Y. A unified nomenclature for yeast autophagy-related genes. Dev Cell 2003; 5:539-45.
15. Hu G, Hacham M, Waterman SR, Panepinto J, Shin S, Liu X, Gibbons J, Valyi-Nagy T, Obara K, Jaffe HA, Ohsumi Y, Williamson PR. PI3K signaling of autophagy is required for starvation tolerance and virulenceof Cryptococcus neoformans. J Clin Invest 2008; 118:1186-97.
16. Reggiori F, Tucker KA, Stromhaug PE, Klionsky DJ. The Atg1-Atg13 complex regulates Atg9 and Atg23 retrieval transport from the pre-autophagosomal structure. Dev Cell 2004; 6:79-90.
17. Lang T, Schaeffeler E, Bernreuther D, Bredschneider M, Wolf D, Thumm M. Aut2p and Aut7p, two novel microtubule-associated proteins are essential for delivery of autophagic vesicles to the vacuole. EMBO J 1998; 17:3597-607.
18. Palmer G, Kelly M, Sturtevant J. Autophagy in the pathogen Candida albicans. Micobiology 2007; 153:51-8.
19. Lang T, Reiche S, Straub M, Bredschneider M, Thumm M. Autophagy and the cvt pathway both depend on AUT9. J Bacteriol 2000; 182:2125-33.
20. Noda T, Kim J, Huang WP, Baba M, Tokunaga C, Ohsumi Y, Klionsky DJ. Apg9p/Cvt7p is an integral membrane protein required for transport vesicle formation in the Cvt and autophagy pathways. J Cell Biol 2000; 148:465-80.
21. Takeshige K, Baba M, Tsuboi S, Noda T, Ohsumi Y. Autophagy in yeast demonstrated with proteinase-deficient mutants and conditions for its induction. J Cell Biol 1992; 119:301-11.
22. Richie DL, Fuller KK, Fortwendel J, Miley MD, McCarthy JW, Feldmesser M, Rhodes JC, Askew DS. Unexpected link between metal ion deficiency and autophagy in Aspergillus fumigatus. Eukaryot Cell 2007; 6:2437-47.
23. Robson G. Hyphal Cell Biology. In: Oliver R, Schweizer M, eds. Molecular Fungal Biology. Cambridge, UK: Cambridge University Press 1999; 164-84.
24. Matsuura A, Tsukada M, Wada Y, Ohsumi Y. Apg1p, a novel protein kinase required for the autophagic process in Saccharomyces cerevisiae. Gene 1997; 192:245-50.
25. Richie DL, Askew DS. Autophagy: A role in metal ion homeostasis? Autophagy 2008; 4:115-7.
26. Feldmesser M, Kress Y, Novikoff P, Casadevall A. Cryptococcus neoformans is a facultative intracellular pathogen in murine pulmonary infection. Infect Immun 2000; 68:4225-37.
27. Chretien F, Lortholary O, Kansau I, Neuville S, Gray F, Dromer F. Pathogenesis of cerebral Cryptococcus neoformans infection after fungemia. J Infect Dis 2002; 186:522-30.
28. Luberto C, Martinez-Marino B, Taraskiewicz D, Bolanos B, Chitano P, Toffaletti DL, Cox GM, Perfect JR, Hannun YA, Balish E, Del Poeta M. Identification of App1 as a regulator of phagocytosis and virulence of Cryptococcus neoformans. J Clin Invest 2003; 112:1080-94.
29. Fan W, Kraus P, Boily M, Heitman J. Cryptococcus neoformans gene expression during murine macrophage infection. Eukaryot Cell 2005; 4:1420-33.
30. Panepinto J, Liu L, Ramos J, Zhu X, Valyi-Nagy T, Eksi S, Fu J, Jaffe H, Wickes B, Williamson P. The DEAD-box RNA helicase Vad1 regulates multiple virulence-associated genes in Cryptococcus neoformans. J Clin Invest 2005; 115:632-41.
31. Dromer F, Mathoulin S, Dupont B, Laporte A. Epidemiology of cryptococcosis in France: a 9-year survey (1985-1993). French Cryptococcosis Study Group. Clin Infect Dis 1996; 23:82-90.
32. Lorenz M, Bender J, Fink G. Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot Cell 2004; 3:1076-87.
33. Rubin-Bejerano I, Fraser I, Grisafi P, Fink GR. Phagocytosis by neutrophils induces an amino acid deprivation response in Saccharomyces cerevisiae and Candida albicans. Proc Natl Acad Sci USA 2003; 100:11007-12.
34. Reboli AC, Rotstein C, Pappas PG, Chapman SW, Kett DH, Kumar D, Betts R, Wible M, Goldstein BP, Schranz J, Krause DS, Walsh TJ. Anidulafungin versus fluconazole for invasive candidiasis. N Engl J Med 2007; 356:2472-82.
35. Segal BH, Walsh TJ. Current approaches to diagnosis and treatment of invasive aspergillosis. Am J Respir Crit Care Med 2006; 173:707-17.
36. Bonnett CR, Cornish EJ, Harmsen AG, Burritt JB. Early neutrophil recruitment and aggregation in the murine lung inhibit germination of Aspergillus fumigatus Conidia. Infect Immun 2006; 74:6528-39.
37. Stephen C, Lester S, Black W, Fyfe M, Raverty S. Multispecies outbreak of cryptococcosis on southern Vancouver Island, British Columbia. Can Vet J 2002; 43:792-4.
38. Dromer F, Mathoulin-Pelissier S, Fontanet A, Ronin O, Dupont B, Lortholary O. Epidemiology of HIV-associated cryptococcosis in France (1985-2001): comparison of the pre- and post-HAART eras. Aids 2004; 18:555-62.
39. Clemons KV, Calich VL, Burger E, Filler SG, Grazziutti M, Murphy J, Roilides E, Campa A, Dias MR, Edwards JE Jr, Fu Y, Fernandes-Bordignon G, Ibrahim A, Katsifa H, Lamaignere CG, Meloni-Bruneri LH, Rex J, Savary CA, Xidieh C. Pathogenesis I: interactions of host cells and fungi. Med Mycol 2000; 38:99-111.
40. Boza JJ, Moennoz D, Vuichoud J, Jarret AR, Gaudard-de-Weck D, Fritsche R, Donnet A, Schiffrin EJ, Perruisseau G, Ballevre O. Food deprivation and refeeding influence growth, nutrient retention and functional recovery of rats. J Nutr 1999; 129:1340-6.
41. van den Berg A, van Elburg RM, Teerlink T, Lafeber HN, Twisk JW, Fetter WP. A randomized controlled trial of enteral glutamine supplementation in very low birth weight infants: plasma amino acid concentrations. J Pediatr Gastroenterol Nutr 2005; 41:66-71.
42. Allen HL, Deepe GS Jr. B cells and CD4-CD8- T cells are key regulators of the severity of reactivation histoplasmosis. J Immunol 2006; 177:1763-71.
43. Kirisako T, Ichimura Y, Okada H, Kabeya Y, Mizushima N, Yoshimori T, Ohsumi M, Takao T, Noda T, Ohsumi Y. The reversible modification regulates the membrane-binding state of Apg8/Aut7 essential for autophagy and the cytoplasm to vacuole targeting pathway. J Cell Biol 2000; 151:263-76.
44. Andrade BB, de Oliveira CI, Brodskyn CI, Barral A, Barral-Netto M. Role of sand fly saliva in human and experimental leishmaniasis: current insights. Scand J Immunol 2007; 66:122-7.
45. Veneault-Fourrey C, Barooah M, Egan M, Wakley G, Talbot N. Autophagic fungal cell death is necessary for infection by the rice blast fungus. Science 2006; 312:580-3.
46. Liu XH, Lu JP, Zhang L, Dong B, Min H, Lin FC. Involvement of a Magnaporthe grisea serine/threonine kinase gene, MgATG1, in appressorium turgor and pathogenesis. Eukaryot Cell 2007; 6:997-1005.
47. Bunting LA, Neilson JB, Bulmer GS. Cryptococcus neoformans: gastronomic delight of a soil ameba. Sabouraudia 1979; 17:225-32.
48. Steenbergen JN, Shuman HA, Casadevall A. Cryptococcus neoformans interactions with amoebae suggest an explanation for its virulence and intracellular pathogenic strategy in macrophages. Proc Natl Acad Sci USA 2001; 98:15245-50.
49. Liu X, Hu G, Panepinto J, Williamson P. Role of a VPS41 homolog in starvation response and virulence of Cryptococcus neoformans. Mol Microbiol 2006; 61:1132-46.
50. Soll DR. Candida commensalism and virulence: the evolution of phenotypic plasticity. Acta Trop 2002; 81:101-10.
51. Nierman WC, Pain A, Anderson MJ, Wortman JR, Kim HS, Arroyo J, Berriman M, Abe K, Archer DB, Bermejo C, Bennett J, Bowyer P, Chen D, Collins M, Coulsen R, Davies R, Dyer PS, Farman M, Fedorova N, Feldblyum TV, Fischer R, Fosker N, Fraser A, Garcia JL, Garcia MJ, Goble A, Goldman GH, Gomi K, Griffith-Jones S, Gwilliam R, Haas B, Haas H, Harris D, Horiuchi H, Huang J, Humphray S, Jimenez J, Keller N, Khouri H, Kitamoto K, Kobayashi T, Konzack S, Kulkarni R, Kumagai T, Lafon A, Latge JP, Li W, Lord A, Lu C, Majoros WH, May GS, Miller BL, Mohamoud Y, Molina M, Monod M, Mouyna I, Mulligan S, Murphy L, O'Neil S, Paulsen I, Penalva MA, Pertea M, Price C, Pritchard BL, Quail MA, Rabbinowitsch E, Rawlins N, Rajandream MA, Reichard U, Renauld H, Robson GD, Rodriguez de Cordoba S, Rodriguez-Pena JM, Ronning CM, Rutter S, Salzberg SL, Sanchez M, Sanchez-Ferrero JC, Saunders D, Seeger K, Squares R, Squares S, Takeuchi M, Tekaia F, Turner G, Vazquez de Aldana CR, Weidman J, White O, Woodward J, Yu JH, Fraser C, Galagan JE, Asai K, Machida M, Hall N, Barrell B, Denning DW. Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature 2005; 438:1151-6.
52. Kabani M, Beckerich J, Brodsky J. Nucleotide exchange factor for the yeast Hsp70 molecular chaperone Ssa1p. Mol Cell Biol 2002; 22:4677-89.
53. Casadevall A, Perfect J. Cryptococcus neoformans. Wash D.C.: ASM Press 1998.
54. Martinez LR, Casadevall A. Specific antibody can prevent fungal biofilm formation and this effect correlates with protective efficacy. Infect Immun 2005; 73:6350-62.
55. Martinez LR, Casadevall A. Susceptibility of Cryptococcus neoformans Biofilms to Antifungal Agents In Vitro. Antimicrob Agents Chemother 2006; 50:1021-33.
56. Nobile CJ, Andes DR, Nett JE, Smith FJ, Yue F, Phan QT, Edwards JE, Filler SG, Mitchell AP. Critical role of Bcr1-dependent adhesins in C. albicans biofilm formation in vitro and in vivo. PLoS Pathog 2006; 2:63.
57. Hanada T, Noda NN, Satomi Y, Ichimura Y, Fujioka Y, Takao T, Inagaki F, Ohsumi Y. The Atg12-Atg5 conjugate has a novel E3-like activity for protein lipidation in autophagy. J Biol Chem 2007; 282:37298-302.
58. Jounai N, Takeshita F, Kobiyama K, Sawano A, Miyawaki A, Xin KQ, Ishii KJ, Kawai T, Akira S, Suzuki K, Okuda K. The Atg5 Atg12 conjugate associates with innate antiviral immune responses. Proc Natl Acad Sci USA 2007; 104:14050-5.
59. Fan QW, Cheng CK, Nicolaides TP, Hackett CS, Knight ZA, Shokat KM, Weiss WA. A dual phosphoinositide-3-kinase alpha/mTOR inhibitor cooperates with blockade of epidermal growth factor receptor in PTEN-mutant glioma. Cancer Res 2007; 67:7960-5.
60. Stephan JS, Herman PK. The regulation of autophagy in eukaryotic cells: do all roads pass through Atg1? Autophagy 2006; 2:146-8.
61. Cheong H, Yorimitsu T, Reggiori F, Legakis JE, Wang CW, Klionsky DJ. Atg17 regulates the magnitude of the autophagic response. Mol Biol Cell 2005; 16:3438-53.
62. Kabeya Y, Kamada Y, Baba M, Takikawa H, Sasaki M, Ohsumi Y. Atg17 functions in cooperation with Atg1 and Atg13 in yeast autophagy. Mol Biol Cell 2005; 16:2544-53.
63. Weber SM, Levitz SM, Harrison TS. Chloroquine and the fungal phagosome. Curr Opin Microbiol 2000; 3:349-53.
64. Amaravadi RK, Yu D, Lum JJ, Bui T, Christophorou MA, Evan GI, Thomas-Tikhonenko A, Thompson CB. Autophagy inhibition enhances therapy-induced apoptosis in a Mycinduced model of lymphoma. J Clin Invest 2007; 117:326-36.
65. Yang Z, Klionsky DJ. An overview of the molecular mechanism of autophagy. Infect Immun 2008; In press.