Divergent Protein Kinase A isoforms co-ordinately regulate conidial germination, carbohydrate metabolism and virulence in Aspergillus fumigatus

Molecular Microbiology

Volumn 79, Issue 4, 2011, Pages 1045-1062

  Fuller, Kevin K ^a,c   Richie, Daryl L ^a,d   Feng, Xizhi ^a   Krishnan, Karthik ^a   Stephens, Timothy J ^a   Wikenheiser Brokamp, Kathryn A ^a,b   Askew, David S ^a   Rhodes, Judith C ^a  

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

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^c DARTMOUTH MEDICAL SCHOOL   (United States)

^d NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE 1; CYCLIC AMP DEPENDENT PROTEIN KINASE 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPERGILLUS FUMIGATUS; CARBOHYDRATE METABOLISM; CARBON METABOLISM; DELETION MUTANT; FEMALE; FUNGAL COLONIZATION; FUNGAL DEVELOPMENT; FUNGAL SPORE GERMINATION; FUNGAL VIABILITY; FUNGAL VIRULENCE; FUNGUS GROWTH; HISTOPATHOLOGY; HOMEOSTASIS; INTRACELLULAR SIGNALING; METABOLIC ACTIVATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SEQUENCE ANALYSIS;

AMINO ACID SEQUENCE; ANIMALS; ASPERGILLUS FUMIGATUS; CARBOHYDRATE METABOLISM; CYCLIC AMP-DEPENDENT PROTEIN KINASES; FEMALE; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENOME, FUNGAL; GLUCOSE; ISOENZYMES; MICE; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; RNA, FUNGAL; SEQUENCE DELETION; SPORES, FUNGAL; VIRULENCE;

ASPERGILLUS FUMIGATUS; MURINAE;

EID: 79551670802     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07509.x     Document Type: Article

References (64)

1. Adachi, K., and Hamer, J.E. (1998) Divergent cAMP signaling pathways regulate growth and pathogenesis in the rice blast fungus Magnaporthe grisea. Plant Cell 10: 1361-1374.
2. Al-Bader, N., Vanier, G., Liu, H., Gravelat, F.N., Urb, M., Hoareau, C.M.-Q., etal. (2010) Role of trehalose biosynthesis in Aspergillus fumigatus development, stress response, and virulence. Infect Immun 78: 3007-3018.
3. Askew, D.S. (2008) Aspergillus fumigatus: virulence genes in a street-smart mold. Curr Opin Microbiol 11: 331-337.
4. Aufauvre-Brown, A., Mellado, E., Gow, N.A.R., and Holden, D.W. (1997) Aspergillus fumigatus chse: a gene related to chs3 of Saccharomyces cerevisiae and important for hyphal growth and conidiophore development but not pathogenicity. Fungal Genet Biol 21: 141-152.
5. Beauvais, A., Maubon, D., Park, S., Morelle, W., Tanguy, M., Huerre, M., etal. (2005) Two alpha(1-3) glucan synthases with different functions in Aspergillus fumigatus. Appl Environ Microbiol 71: 1531-1538.
6. Beffa, T., Staib, F., Lott Fischer, J., Lyon, P., Gumowski, P., Marfenina, O., etal. (1998) Mycological control and surveillance of biological waste and compost. Med Mycol 36 (Suppl. I): 137-145.
7. Bhabhra, R., Miley, M.D., Mylonakis, E., Boettner, D., Fortwendel, J., Panepinto, J.C., etal. (2004) Disruption of the Aspergillus fumigatus gene encoding nucleolar protein CgrA impairs thermotolerant growth and reduces virulence. Infect Immun 72: 4731-4740.
8. Bockmühl, D.P., Krishnamurthy, S., Gerads, M., Sonneborn, A., and Ernst, J.F. (2001) Distinct and redundant roles of the two protein kinase A isoforms Tpk1p and Tpk2p in morphogenesis and growth of Candida albicans. Mol Microbiol 42: 1243-1257.
9. Catlett, N.L., Lee, B.N., Yoder, O.C., and Turgeon, B.G. (2002) Split-marker recombination for efficient targeted deletion of fungal genes. Fungal Genet Newsl 50: 9-11.
10. Chen, D., Janganan, T.K., Chen, G., Marques, E.R., Kress, M.R., Goldman, G.H., etal. (2007) The cAMP pathway is important for controlling the morphological switch to the pathogenic yeast form of Paracoccidioides brasiliensis. Mol Microbiol 65: 761-779.
11. Cove, D. (1966) The induction and repression of nitrate reductase in the fungus Aspergillus nidulans. Biochim Biophys Acta 113: 51-56.
12. D'Souza, C.A., and Heitman, J. (2001) Conserved cAMP signaling cascades regulate fungal development and virulence. FEMS Microbiol Rev 25: 349-364.
13. D'Souza, C.A., Alspaugh, J.A., Yue, C., Harashima, T., Cox, G.M., Perfect, J.R., and Heitman, J. (2001) Cyclic AMP-dependent protein kinase controls virulence of the fungal pathogen Cryptococcus neoformans. Mol Cell Biol 21: 3179-3191.
14. Dürrenberger, F., Wong, K., and Kronstad, J.W. (1998) Identification of a cAMP-dependent protein kinase catalytic subunit required for virulence and morphogenesis in Ustilago maydis. Proc Natl Acad Sci USA 95: 5684-5689.
15. Ejzykowicz, D.E., Cunha, M.M., Rozental, S., Solis, N.V., Gravelat, F.N., Sheppard, D.C., and Filler, S.G. (2009) The Aspergillus fumigatus transcription factor Ace2 governs pigment production, conidiation and virulence. Mol Microbiol 72: 155-169.
16. d'Enfert, C. (1997) Fungal spore germination: insights from the molecular genetics of Aspergillus nidulans and Neurospora crassa. Fungal Genet Biol 21: 163-172.
17. d'Enfert, C., Bonini, B.M., Zapella, P.D.A., Fontaine, T., da Silva, A.M., and Terenzi, H.F. (1999) Neutral trehalases catalyse intracellular trehalose breakdown in the filamentous fungi Aspergillus nidulans and Neurospora crassa. Mol Microbiol 32: 471-483.
18. Fleck, C.B., and Brock, M. (2010) Aspergillus fumigatus catalytic glucokinase and hexokinase: expression analysis and importance for germination, growth, and conidiation. Eukaryot Cell 9: 1120-1135.
19. Fortwendel, J.R., Fuller, K.K., Stephens, T.J., Bacon, W.C., Askew, D.S., and Rhodes, J.C. (2008) Aspergillus fumigatus RasA regulates asexual development and cell wall integrity. Eukaryot Cell 7: 1530-1539.
20. Fuller, K.K., Zhao, W., Askew, D.S., and Rhodes, J.C. (2009) Deletion of the protein kinase A regulatory subunit leads to deregulation of mitochondrial activation and nuclear duplication in Aspergillus fumigatus. Eukaryot Cell 8: 271-277.
21. Gold, S., Duncan, G., Barrett, K., and Kronstad, J. (1994) cAMP regulates morphogenesis in the fungal pathogen Ustilago maydis. Genes Dev 8: 2805-2816.
22. Grosse, C., Heinekamp, T., Kniemeyer, O., Gehrke, A., and Brakhage, A.A. (2008) Protein kinase A regulates growth, sporulation, and pigment formation in Aspergillus fumigatus. Appl Environ Microbiol 74: 4923-4933.
23. Hahn, M. (2009) Distinguishing among evolutionary models for the maintenance of gene duplicates. J Hered 5: 605-617.
24. van Heerden, I., Cronje, C., Swart, S., and Kotze, J. (2002) Microbial, chemical and physical aspects of citrus waste composting. Bioresour Technol 81: 71-76.
25. Hicks, J.K., and Heitman, J. (2007) Divergence of protein kinase A catalytic subunits in Cryptococcus neoformans and Cryptococcus gattii illustrates evolutionary reconfiguration of a signaling cascade. Eukaryot Cell 6: 413-420.
26. Hicks, J.K., D'Souza, C.A., Cox, G.M., and Heitman, J. (2004) Cyclic AMP-dependent protein kinase catalytic subunits have divergent roles in virulence factor production in two varieties of the fungal pathogen Cryptococcus neoformans. Eukaryot Cell 3: 14-26.
27. Jones, D.L., Petty, J., Hoyle, D.C., Hayes, A., Ragni, E., Popolo, L., etal. (2003) Transcriptome profiling of a Saccharomyces cerevisiae mutant with a constitutively activated ras/cAMP pathway. Physiol Genomics 16: 107-118.
28. Jung, W.H., Warn, P., Ragni, E., Popolo, L., Nunn, C.D., Turner, M.P., and Stateva, L. (2005) Deletion of PDE2, the gene encoding the high-affinity cAMP phosphodiesterase, results in changes of the cell wall and membrane in Candida albicans. Yeast 22: 285-294.
29. Latge, J.-P. (1999) Aspergillus fumigatus and aspergillosis. Clin Microbiol Rev 12: 310-350.
30. Latgé, J.-P. (2001) The pathobiology of Aspergillus fumigatus. Trends Microbiol 9: 382-389.
31. Latgé, J.-P. (2007) The cell wall: a carbohydrate armour for the fungal cell. Mol Microbiol 66: 279-290.
32. Liebmann, B., Gattung, S., Jahn, B., and Brakhage, A.A. (2003) cAMP signaling in Aspergillus fumigatus is involved in the regulation of the virulence gene pksP and in defense against killing by macrophages. Mol Genet Genomics 269: 420-435.
33. Liebmann, B., Muller, M., Braun, A., and Brakhage, A.A. (2004) The cyclic AMP-dependent protein kinase a network regulates development and virulence in Aspergillus fumigatus. Infect Immun 72: 5193-5203.
34. Lynch, M., and Conery, J. (2000) The evolutionary fate and consequences of duplicate genes. Science 290: 1151-1155.
35. Ma, Y., Qiao, J., Liu, W., Wan, Z., Wang, X., Calderone, R., and Li, R. (2008) The Sho1 sensor regulates growth, morphology, and oxidant adaptation in Aspergillus fumigatus but is not essential for development of invasive pulmonary aspergillosis. Infect Immun 76: 1695-1701.
36. McDonagh, A., Fedorova, N., Crabtree, J., Yu, Y., Kim, S., Chen, D., etal. (2008) Sub-telomere directed gene expression during initiation of invasive aspergillosis. PLoS Pathog 4: e1000154.
37. Maeda, H., Sano, M., Maruyama, Y., Tanno, T., Akao, T., Totsuka, Y., etal. (2004) Transcriptional analysis of genes for energy catabolism and hydrolytic enzymes in the filamentous fungus Aspergillus oryzae using cDNA microarrays and expressed sequence tags. Appl Environ Microbiol 65: 74-83.
38. Maubon, D., Park, S., Tanguy, M., Huerre, M., Schmitt, C., Prévost, M.C., etal. (2006) ags3, an α(1-3)glucan synthase gene family member of Aspergillus fumigatus, modulates mycelium growth in the lung of experimentally infected mice. Fungal Genet Biol 43: 366-375.
39. Mazon, M., Behrens, M., Morgado, E., and Portillo, F. (1993) Low activity of the yeast cAMP-dependent protein kinase catalytic subunit Tpk3 is due to the poor expression of the TPK3 gene. Eur J Biochem 213: 501-506.
40. Mouyna, I., Morelle, W., Vai, M., Monod, M., Léchenne, B., Fontaine, T., etal. (2005) Deletion of gel2 encoding for a beta(1-3)glucanosyltransferase affects morphogenesis and virulence in Aspergillus fumigatus. Mol Microbiol 56: 1675-1688.
41. Ni, M., Rierson, S., Seo, J.-A., and Yu, J.-H. (2005) The pkaB gene encoding the secondary protein kinase A catalytic subunit has a synthetic lethal interaction with pkaA and plays overlapping and opposite roles in Aspergillus nidulans. Eukaryot Cell 4: 1465-1476.
42. Oliver, B., Panepinto, J., Fortwendel, J., Smith, D., Askew, D., and Rhodes, J. (2002a) Cloning and expression of pkaC and pkaR, the genes encoding the cAMP-dependent protein kinase of Aspergillus fumigatus. Mycopathologia 154: 85-91.
43. Oliver, B.G., Panepinto, J.C., Askew, D.S., and Rhodes, J.C. (2002b) cAMP alteration of growth rate of Aspergillus fumigatus and Aspergillus niger is carbon-source dependent. Microbiology 148: 2627-2633.
44. Paisley, D., Robson, G., and Denning, D. (2005) Correlation between in vitro growth rate and in vivo virulence in Aspergillus fumigatus. Med Mycol 43: 397-401.
45. Pan, X., and Heitman, J. (1999) Cyclic AMP-dependent protein kinase regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Mol Cell Biol 19: 4874-4887.
46. Pandey, A., Roca, M.G., Read, N.D., and Glass, N.L. (2004) Role of a mitogen-activated protein kinase pathway during conidial germination and hyphal fusion in Neurospora crassa. Eukaryot Cell 3: 348-358.
47. Pearce, L., Komander, D., and Alessi, D. (2010) The nuts and bolts of AGC protein kinases. Nat Rev Mol Cell Biol 11: 9-22.
48. Puttikamonkul, S., Willger, S.D., Grahl, N., Perfect, J.R., Movahed, N., Bothner, B., etal. (2010) Trehalose 6-phosphate phosphatase is required for cell wall integrity and fungal virulence but not trehalose biosynthesis in the human fungal pathogen Aspergillus fumigatus. Mol Microbiol 77: 891-911.
49. de Prost, N., and Saumon, G. (2007) Glucose transport in the lung and its role in liquid movement. Respir Physiol Neurobiol 159: 331-337.
50. Reyes, G., Romans, A., Nguyen, C.K., and May, G.S. (2006) Novel mitogen-activated protein kinase MpkC of Aspergillus fumigatus is required for utilization of polyalcohol sugars. Eukaryot Cell 5: 1934-1940.
51. Rhodes, J.C., Oliver, B.G., Askew, D.S., and Amlung, T.W. (2001) Identification of genes of Aspergillus fumigatus up-regulated during growth on endothelial cells. Med Mycol 39: 253-260.
52. Richie, D., Hartl, L., Aimanianda, V., Winters, M., Fuller, K., Miley, M., etal. (2009) A role for the unfolded protein response (upr) in virulence and antifungal susceptibility in Aspergillus fumigatus. PLoS Pathog 5: e1000258.
53. Robertson, L.S., and Fink, G.R. (1998) The three yeast A kinases have specific signaling functions in pseudohyphal growth. Proc Natl Acad Sci USA 95: 13783-13787.
54. Robertson, L.S., Causton, H.C., Young, R.A., and Fink, G.R. (2000) The yeast A kinases differentially regulate iron uptake and respiratory function. Proc Natl Acad Sci USA 97: 5984-5988.
55. Romano, J., Nimrod, G., Ben-Tal, N., Shadkchan, Y., Baruch, K., Sharon, H., and Osherov, N. (2006) Disruption of the Aspergillus fumigatus ECM33 homologue results in rapid conidial germination, antifungal resistance and hypervirulence. Microbiology 152: 1919-1928.
56. Thevelein, J.M., Geladé, R., Holsbeeks, I., Lagatie, O., Popova, Y., Rolland, F., etal. (2005) Nutrient sensing systems for rapid activation of the protein kinase A pathway in yeast. Biochem Soc Trans 33: 253-256.
57. Toda, T., Cameron, S., Sass, P., Zoller, M., and Wigler, M. (1987) Three different genes in S. cerevisiae encode the catalytic subunit of the cAMP-dependent protein kinase. Cell 50: 277-287.
58. Upton, A., Kirby, K.A., Carpenter, P., Boeckh, M., and Marr, K.A. (2007) Invasive aspergillosis following hematopoietic cell transplantation: outcomes and prognostic factors associated with mortality. Clin Infect Dis 44: 531-540.
59. Valiante, V., Heinekamp, T., Jain, R., Härtl, A., and Brakhage, A.A. (2008) The mitogen-activated protein kinase MpkA of Aspergillus fumigatus regulates cell wall signaling and oxidative stress response. Fungal Genet Biol 45: 618-627.
60. Wagener, J., Echtenacher, B., Rohde, M., Kotz, A., Krappmann, S., Heesemann, J., and Ebel, F. (2008) The putative {alpha}-1, 2-mannosyltransferase AfMnt1 of the opportunistic fungal pathogen Aspergillus fumigatus is required for cell wall stability and full virulence. Eukaryot Cell 7: 1661-1673.
61. Willger, S., Puttikamonkul, S., Kim, K., Burritt, J., Grahl, N., Metzler, L., etal. (2008) A sterol-regulatory element binding protein is required for cell polarity, hypoxia adaptation, azole drug resistance, and virulence in Aspergillus fumigatus. PLoS Pathog 4: e1000200.
62. Xie, X., Wilkinson, H.H., Correa, A., Lewis, Z.A., Bell-Pedersen, D., and Ebbole, D.J. (2004) Transcriptional response to glucose starvation and functional analysis of a glucose transporter of Neurospora crassa. Fungal Genet Biol 41: 1104-1119.
63. Xue, T., Nguyen, C.K., Romans, A., and May, G.S. (2004) A mitogen-activated protein kinase that senses nitrogen regulates conidial germination and growth in Aspergillus fumigatus. Eukaryot Cell 3: 557-560.
64. Yang, Z., and Dickman, M.B. (1999) Colletotrichum trifolii mutants disrupted in the catalytic subunit of cAMP-dependent protein kinase are nonpathogenic. Mol Plant Microbe Interact 12: 430-439.