A fungal pH-responsive signaling pathway regulating Aspergillus adaptation and invasion into the cornea

Investigative Ophthalmology and Visual Science

Volumn 51, Issue 3, 2010, Pages 1517-1523

  Hua, Xia ^a   Yuan, Xiaoyong ^a   Wilhelmus, Kirk R ^a  

^a CULLEN EYE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; PROTEIN PACC; PROTEIN PALB; UNCLASSIFIED DRUG; CYSTEINE PROTEINASE; PACC PROTEIN, ASPERGILLUS; PALB PROTEIN, ASPERGILLUS NIDULANS; TRANSCRIPTION FACTOR; ZINC FINGER PROTEIN;

ACIDITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPERGILLOSIS; ASPERGILLUS NIDULANS; CONTROLLED STUDY; FUNGAL GENE; FUNGAL SPORE GERMINATION; FUNGAL STRAIN; FUNGAL VIRULENCE; FUNGUS GROWTH; FUNGUS HYPHAE; GENE FUNCTION; GENOTYPE; GROWTH RATE; HUMAN; HUMAN TISSUE; IN VITRO STUDY; KERATOMYCOSIS; MICROBIAL ACTIVITY; NONHUMAN; PACC GENE; PALB GENE; PATHOGENESIS; PH; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STROMA; WILD TYPE; ANIMAL; CORNEA ULCER; FUNGAL EYE INFECTION; GENETICS; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; SWINE; VIRULENCE;

ANIMALS; ASPERGILLOSIS; ASPERGILLUS NIDULANS; CORNEAL ULCER; CYSTEINE ENDOPEPTIDASES; EYE INFECTIONS, FUNGAL; FUNGAL PROTEINS; HUMANS; HYDROGEN-ION CONCENTRATION; SIGNAL TRANSDUCTION; SWINE; TRANSCRIPTION FACTORS; VIRULENCE; ZINC FINGERS;

EID: 77949902686     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.09-4348     Document Type: Article

References (71)

1. Leber T. Keratomycosis aspergillina als Ursache von Hypopyonkeratitis. Albrecht von Graefes Arch Ophthalmol. 1879;25:285-301.
2. Behrens-Baumann W. Mycosis of the Eye and Its Adnexa. Basel: Karger; 1999:48-107.
3. Gopinathan U, Garg P, Fernandes M, Sharma S, Athmanathan S, Rao GN. The epidemiological features and laboratory results of fungal keratitis: a 10-year review at a referral eye care center in South India. Cornea. 2002;21:555-559.
4. Leck AK, Thomas PA, Hagan M, et al. Aetiology of suppurative corneal ulcers in Ghana and south India, and epidemiology of fungal keratitis. Br J Ophthalmol. 2002;86:1211-1215.
5. Bharathi MJ, Ramakrishnan R, Vasu S, Meenakshi R, Palaniappan R. Epidemiological characteristics and laboratory diagnosis of fungal keratitis: a three-year study. Indian J Ophthalmol. 2003;51:315-321.
6. Sun XG, Zhang Y, Li R, et al. Etiological analysis on ocular fungal infection in the period of 1989-2000. Chin Med J (Engl). 2004; 117:598-600.
7. Chowdhary A, Singh K. Spectrum of fungal keratitis in North India. Cornea. 2005;24:8-15.
8. Höfling-Lima AL, Forseto A, Duprat JP, et al. Estudo laboratorial das micoses oculares e fatores associados ̀s ceratites. Arq Bras Oftalmol. 2005;68:21-27.
9. Saha R, Das S. Mycological profile of infectious keratitis from Delhi. Indian J Med Res. 2006;123:159-164.
10. Ibrahim MM, Vanini R, Ibrahim FM, et al. Epidemiologic aspects and clinical outcome of fungal keratitis in southeastern Brazil. Eur J Ophthalmol. 2009;19:355-361.
11. Tuft SJ, Tullo AB. Fungal keratitis in the United Kingdom 2003-2005. Eye. 2009;23:1308-1313.
12. Puttanna ST. Mycotic infections of the cornea. J All India Ophthalmol Soc. 1967;15:11-18.
13. Bharathi MJ, Ramakrishnan R, Vasu S, Meenakshi R, Palaniappan R. Aetiological diagnosis of microbial keratitis in South India: a study of 1618 cases. Indian J Med Microbiol. 2002;20:19-24.
14. Xie L, Zhong W, Shi W, Sun S. Spectrum of fungal keratitis in north China. Ophthalmology. 2006;113:1943-1948.
15. Avunduk AM, Beuerman RW, Warnel ED, Kaufman HE, Greer D. Comparison of efficacy of topical and oral fluconazole treatment in experimental Aspergillus keratitis. Curr Eye Res. 2003;26:113-117.
16. Panda A, Ahuja R, Biswas NR, Satpathy G, Khokhar S. Role of 0.02% polyhexamethylene biguanide and 1% povidone iodine in experimental Aspergillus keratitis. Cornea. 2003;22:138-141.
17. Martínez-Ramos M, Claros BJA, Vale-Oviedo MA, et al. Effect of the vehicle on the topical itraconazole efficacy for treating corneal ulcers caused by Aspergillus fumigatus. Clin Exp Ophthalmol. 2008;36:335-338.
18. Clemons KV, Stevens DA. The contribution of animal models of aspergillosis to understanding pathogenesis, therapy and virulence. Med Mycol. 2005;43(suppl 1):S101-S110.
19. Latgé JP. The pathobiology of Aspergillus fumigatus. Trends Microbiol. 2001;9:382-389.
20. Cooney NM, Klein BS. Fungal adaptation to the mammalian host: it is a new world, after all. Curr Opin Microbiol. 2008;11:511-516.
21. Pirofski LA, Casadevall A. The damage-response framework of microbial pathogenesis and infectious diseases. Adv Exp Med Biol. 2008;635:135-146.
22. Penãlva MA, Arst HN Jr. Regulation of gene expression by ambient pH in filamentous fungi and yeasts. Microbiol Mol Biol Rev. 2002; 66:426-446.
23. Tilburn J, Sarkar S, Widdick DA, et al. The Aspergillus PacC zinc finger transcription factor mediates regulation of both acid-and alkaline-expressed genes by ambient pH. EMBO J. 1995;14:779-790.
24. Diez E, Alvaro J, Espeso EA, et al. Activation of the Aspergillus PacC zinc finger transcription factor requires two proteolytic steps. EMBO J. 2002;21:1350-1359.
25. Penãlva MA, Tilburn J, Bignell E, Arst HN Jr. Ambient pH gene regulation in fungi: making connections. Trends Microbiol. 2008; 16:291-300.
26. Rollins JA. The Sclerotinia sclerotiorum pac1 gene is required for sclerotial development and virulence. Mol Plant Microbe Interact. 2003;16:785-795.
27. Ortoneda M, Guarro J, Madrid MP, et al. Fusarium oxysporum as a multihost model for the genetic dissection of fungal virulence in plants and mammals. Infect Immun. 2004;72:1760-1766.
28. You BJ, Choquer M, Chung KR. The Colletotrichum acutatum gene encoding a putative pH-responsive transcription regulator is a key virulence determinant during fungal pathogenesis on citrus. Mol Plant Microbe Interact. 2007;20:1149-1160.
29. Bignell E, Negrete-Urtasun S, Calcagno AM, Haynes K, Arst HN Jr, Rogers T. The Aspergillus pH-responsive transcription factor PacC regulates virulence. Mol Microbiol. 2005;55:1072-1084.
30. Davis D. Adaptation to environmental pH in Candida albicans and its relation to pathogenesis. Curr Genet. 2003;44:1-7.
31. Mitchell BM, Wu TG, Jackson BE, Wilhelmus KR. Candida albicans strain-dependent virulence and Rim13p-mediated filamentation in experimental keratomycosis. Invest Ophthalmol Vis Sci. 2007;48:774-780.
32. Yuan X, Hua X, Mitchell BM, Wilhelmus KR. Fungal filamentous growth and the RIM101 pathway of Candida albicans during experimental keratomycosis. Invest Ophthalmol Vis Sci. In press.
33. Martinelli SD. Aspergillus nidulans as an experimental organism. Prog Ind Microbiol. 1994;29:33-58.
34. Penãlva MA, Arst HN Jr. Recent advances in the characterization of ambient pH regulation of gene expression in filamentous fungi and yeasts. Annu Rev Microbiol. 2004;58:425-451.
35. Andersen MR, Lehmann L, Nielsen J. Systemic analysis of the response of Aspergillus niger to ambient pH. Genome Biol. 2009; 10:R47.
36. Amich J, Leal F, Calera JA. Repression of the acid ZrfA/ZrfB zincuptake system of Aspergillus fumigatus mediated by PacC under neutral, zinc-limiting conditions. Int Microbiol. 2009;12:39-47.
37. Flueckiger F, Kodjikian L, Halberstadt M, Boehnke M, Garweg JG. An ex-vivo, whole-globe porcine model of corneoepithelial wound healing tested using immunomodulatory drugs. J Ocul Pharmacol Ther. 2005;21:367-375.
38. Vermeltfoort PBJ, van Kooten TG, Bruinsma GM, Hooymans AM, van der Mei HC, Busscher HJ. Bacterial transmission from contact lenses to porcine corneas: an ex vivo study. Invest Ophthalmol Vis Sci. 2005;46:2042-2046.
39. Clutterbuck AJ. Aspergillus nidulans. In: O'Brien SJ, ed. Genetic Maps: Locus Maps of Complex Genomes. 6th ed. Cold Spring Harbor, NY: Cold Spring Harbor Press; 1993:3.71-3.84.
40. Barratt RW, Johnson GB, Ogata WN. Wild-type and mutant stocks of Aspergillus nidulans. Genetics. 1965;52:233-246.
41. McCluskey K. The Fungal Genetics Stock Center: from molds to molecules. In: Laskin AI, Bennett JW, Gadd GM, eds. Advances in Applied Microbiology. San Diego: Academic Press; 2003:246-262.
42. Denison SH, Orejas M, Arst HN Jr. Signaling of ambient pH in Aspergillus involves a cysteine protease. J Biol Chem. 1995;270: 28519-28522.
43. Fernández-Martinez J, Brown CV, Diez E, et al. Overlap of nuclear localisation signal and specific DNA-binding residues within the zinc finger domain of PacC. J Mol Biol. 2003;334:667-684.
44. Mingot JM, Tilburn J, Diez E, et al. Specificity determinants of proteolytic processing of Aspergillus PacC transcription factor are remote from the processing site, and processing occurs in yeast if pH signalling is bypassed. Mol Cell Biol. 1999;19:1390-1400.
45. Wu TG, Keasler VV, Mitchell BM, Wilhelmus KR. Immunosuppression affects the severity of experimental Fusarium solani keratitis. J Infect Dis. 2004;190:192-198.
46. Trinci APJ. A kinetic study of the growth of Aspergillus nidulans and other fungi. J Gen Microbiol. 1969;57:11-24.
47. Marin S, Sanchis V, Teixido A, et al. Water and temperature relations and microconidial germination of Fusarium moniliforme and Fusarium proliferatum from maize. Can J Microbiol. 1996;42:1045-1050.
48. Lahlali R, Serrhini MN, Jijakli MH. Studying and modelling the combined effect of temperature and water activity on the growth rate of P. expansum. Int J Food Microbiol. 2005;103:315-322.
49. Wu TG, Wilhelmus KR, Mitchell BM. Experimental keratomycosis in a mouse model. Invest Ophthalmol Vis Sci. 2003;44:210-216.
50. Thomas PA. Fungal infections of the cornea. Eye. 2003;17:852-862.
51. Brakhage AA. Systemic fungal infections caused by Aspergillus species: epidemiology, infection process and virulence determinants. Curr Drug Targets. 2005;6:875-886.
52. Dong X, Shi W, Zeng Q, Xie L. Roles of adherence and matrix metalloproteinases in growth patterns of fungal pathogens in cornea. Curr Eye Res. 2005;30:613-620.
53. Fons A, García-de-Lomas J, Nogueira JM, Buesa FJ, Gimeno C. Histopathology of experimental Aspergillus fumigatus keratitis. Mycopathologia. 1988;101:129-131.
54. Xie L, Zhai H, Shi W, Zhao J, Sun S, Zang X. Hyphal growth patterns and recurrence of fungal keratitis after lamellar keratoplasty. Ophthalmology. 2008;115:983-987.
55. Gopinathan U, Ramakrishna T, Willcox M, et al. Enzymatic, clinical and histologic evaluation of corneal tissues in experimental fungal keratitis in rabbits. Exp Eye Res. 2001;72:433-442.
56. Ward OP, Qin WM, Dhanjoon J, Ye J, Singh A. Physiology and biotechnology of Aspergillus. Adv Appl Microbiol. 2006;58:1-75.
57. Rementeria A, López-Molina N, Ludwig A, et al. Genes and molecules involved in Aspergillus fumigatus virulence. Rev Iberoam Micol. 2005;22:1-23.
58. Rhodes JC, Brakhage AA. Molecular determinants of virulence in Aspergillus fumigatus. In: Heitman J, Filler SG, Edwards JE, Jr., Mitchell AP, eds. Molecular Principles of Fungal Pathogenesis. Washington, DC: ASM Press; 2006:333-345.
59. Caddick MX, Brownlee AG, Arst HN, Jr. Regulation of gene expression by pH of the growth medium in Aspergillus nidulans. Mol Gen Genet. 1986;203:346-353.
60. Andersen MR, Nielsen J. Current status of systems biology in aspergilli. Fungal Genet Biol. 2009;46(suppl 1):S180-S190.
61. Sarfati J, Diaquin M, Debeaupuis JP, et al. A new experimental murine aspergillosis model to identify strains of Aspergillus fumigatus with reduced virulence. Nippon Ishinkin Gakkai Zasshi. 2002;43:203-213.
62. Penãs MM, Hervás-Aguilar A, Múnera-Huertas T, et al. Further characterization of the signaling proteolysis step in the Aspergillus nidulans pH signal transduction pathway. Eukaryot Cell. 2007;6: 960-970.
63. Paisley D, Robson GD, Denning DW. Correlation between in vitro growth rate and in vivo virulence in Aspergillus fumigatus. Med Mycol. 2005;43:397-401.
64. Yamada M, Mochizuki H, Kawai M, Yoshino M, Mashima Y. Fluorophotometric measurement of pH of human tears in vivo. Curr Eye Res. 1997;16:482-486.
65. Lin MC, Graham AD, Polse KA, McNamara NA, Tieu TG. The effects of one-hour wear of high-Dk soft contact lenses on corneal pH and epithelial permeability. CLAO J. 2000;26:130-133.
66. Norn MS. Tear fluid pH in normals, contact lens wearers, and pathological cases. Acta Ophthalmol (Copenh). 1988;66:485-489.
67. Denison SH. pH regulation of gene expression in fungi. Fungal Genet Biol. 2000;29:61-71.
68. Hervás-Aguilar A, Rodríguez JM, Tilburn J, Arst HN, Jr, Penãlva MA. Evidence for the direct involvement of the proteasome in the proteolytic processing of the Aspergillus nidulans zinc finger transcription factor PacC. J Biol Chem. 2007;282:34735-34747.
69. Wortman JR, Gilsenan JM, Joardar V, et al. The 2008 update of the Aspergillus nidulans genome annotation: a community effort. Fungal Genet Biol. 2009;46(suppl 1):S2-S13.
70. Sexton AC, Howlett BJ. Parallels in fungal pathogenesis on plant and animal hosts. Eukaryot Cell. 2006;5:1941-1949.
71. Vemuganti GK, Garg P, Gopinathan U, et al. Evaluation of agent and host factors in progression of mycotic keratitis: a histologic and microbiologic study of 167 corneal buttons. Ophthalmology. 2002;109:1538-1546.