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HOG-MAPK Signaling Regulates the Adaptive Responses of Aspergillus fumigatus to Thermal Stress and Other Related Stress

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Abstract

Aspergillus fumigatus is naturally exposed to a highly variable environment and subjected to various kinds of stresses. High-osmolarity glycerol mitogen-activated protein kinase (HOG-MAPK) pathway plays a crucial role in regulating cellular homeostasis in response to environmental changes. Here, we explored the contribution of HOG-MAPK pathway to the adaptive responses to thermal stress and other related stresses in A. fumigatus. We observed the phenotype features of wild-type strains and their derived mutants at 37 and 48 °C, and the results suggested that tcsB participates in response to high temperature. Furthermore, susceptibility test for antifungal drugs showed that SHO1 branch is probably involved in the susceptibility of A. fumigatus to itraconazole at high temperature. Although sakA expression at mRNA level appeared unchanged in wild-type AF293 subjected to thermal stress, phosphorylated SakAp level increased significantly in the strains exposed to cold stress, 250 mmol/L nystatin or 10 % dimethyl sulfoxide in a manner dependent on the SLN1 branch and independent on the SHO1 branch. Taken together, these results indicate that HOG-MAPK pathway, especially the SLN1 branch, plays an important role in the adaptations of A. fumigatus to thermal stress and other related stresses.

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References

  1. Latgé JP. Aspergillus fumigatus and aspergillosis. Clin Microbiol Rev. 1999;12:310–50.

    PubMed  Google Scholar 

  2. Denning DW. Invasive aspergillosis. Clin Infect Dis. 1998;26:781–803.

    Article  PubMed  CAS  Google Scholar 

  3. Kontoyiannis DP, Bodey GP. Invasive aspergillosis in 2002: an update. Eur J Clin Microbiol Infect Dis. 2002;21:161–72.

    Article  PubMed  CAS  Google Scholar 

  4. Perfect JR. Antifungal resistance: the clinical confront. Oncology. 2004;18:15–22.

    Google Scholar 

  5. Bahn YS. Master and commander in fungal pathogens: the two-component system and the HOG signaling pathway. Eukaryot Cell. 2008;7:2017–36.

    Article  PubMed  CAS  Google Scholar 

  6. Gustin MC, Albertyn J, Alexander M, et al. MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol Mol Biol Rev. 1998;62:1264–300.

    PubMed  CAS  Google Scholar 

  7. Kawasaki L, Sánchez O, Shiozaki K, et al. SakA MAP kinase is involved in stress signal transduction, sexual development and spore viability in Aspergillus nidulans. Mol Microbiol. 2002;45:1153–63.

    Article  PubMed  CAS  Google Scholar 

  8. Marshall CJ. MAP kinase kinase kinase, MAP kinase kinase and MAP kinase. Curr Opin Genet Dev. 1994;4:82–9.

    Article  PubMed  CAS  Google Scholar 

  9. Hirt H. Multiple roles of MAP kinases in plant signal transduction. Trends Plant Sci. 1997;2:11–5.

    Article  Google Scholar 

  10. Herskowitz I. MAP kinase pathways in yeast: for mating and more. Cell. 1995;80:187–97.

    Article  PubMed  CAS  Google Scholar 

  11. Roychoudhury S, Zielinski NA, Ninfa AJ, et al. Inhibitors of two-component signal transduction systems: inhibition of alginate gene activation in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A. 1993;90:965–9.

    Article  PubMed  CAS  Google Scholar 

  12. López-Goñi I, Guzmán-Verri C, Manterola L, et al. Regulation of Brucella virulence by the two-component system BvrR/BvrS. Vet Microbiol. 2002;90:329–39.

    Article  PubMed  Google Scholar 

  13. Hayashi J, Nishikawa K, Hirano R, et al. Identification of a two-component signal transduction system involved in fimbriation of Porphyromonas gingivalis. Microbiol Immunol. 2000;44:279–82.

    PubMed  CAS  Google Scholar 

  14. Moskowitz SM, Ernst RK, Miller SI, et al. A two-component regulatory system of Pseudomonas aeruginosa that modulates resistance to cationic antimicrobial peptides and addition of aminoarabinose to lipid A. J Bacteriol. 2004;186:575–9.

    Article  PubMed  CAS  Google Scholar 

  15. Brewster JL, de Valoir T, Dwyer ND, et al. An osmosensing signal transduction pathway in yeast. Science. 1993;259:1760–3.

    Article  PubMed  CAS  Google Scholar 

  16. Lawrence CL, Botting CH, Antrobus R, et al. Evidence of a new role for the high-osmolarity glycerol mitogen-activated protein kinase pathway in yeast: regulating adaptation to citric acid stress. Mol Cell Biol. 2004;24:3307–23.

    Article  PubMed  CAS  Google Scholar 

  17. Winkler A, Arkind C, Mattison CP, et al. Heat stress activates the yeast high-osmolarity glycerol mitogen-activated protein kinase pathway and protein tyrosine phosphatases are essential under heat stress. Eukaryot Cell. 2002;2:163–73.

    Article  Google Scholar 

  18. Alonso-Monge R, Real E, Wojda I, et al. Hyperosmotic stress response and regulation of cell wall in Saccharomyces cerevisiae share common functional aspects. Mol Microbiol. 2001;41:717–30.

    Article  PubMed  CAS  Google Scholar 

  19. Gacto M, Soto T, Vicente-Soler J, et al. Learning from yeasts: intracellular sensing of stress conditions. Int Microbiol. 2003;6:211–9.

    Article  PubMed  CAS  Google Scholar 

  20. Hayashi M, Maeda T. Activation of the HOG Pathway upon cold stress in Saccharomyces cerevisiae. J Biochem. 2006;139:797–803.

    Article  PubMed  CAS  Google Scholar 

  21. Hospenthal DR, Kwon-Chung KJ, Bennett JE. Concentrations of airborne Aspergillus compared to the incidence of invasive aspergillosis: lack of correlation. Med Mycol. 1998;36:165–8.

    PubMed  CAS  Google Scholar 

  22. Ma Y, Qiao J, Liu W, et al. The Sho1 sensor regulates growth, morphology, and oxidant adaptation in Aspergillus fumigatus but is not essential for development of invasive pulmonary aspergillosis. Infect Immun. 2008;76:1695–701.

    Article  PubMed  CAS  Google Scholar 

  23. 马彦,乔建军,刘伟, 等. 烟曲霉pbs2基因功能初步探讨. 中华微生物学和免疫学杂志. 2008;28:1126–30.

  24. Du C, Sarfati J, Latge JP, et al. The role of the sakA (Hog1) and tcsB (sln1) genes in the oxidant adaptation of Aspergillus fumigatus. Med Mycol. 2006;44:211–8.

    Article  PubMed  CAS  Google Scholar 

  25. Clinical and Laboratory Standards Institute. Reference method for broth dilution antifungal susceptibility testing of filamentous fungi; approved standard-second edition. CLSI document M38-A2. Wayne, PA: Clinical and Laboratory Standards Institute; 2008.

  26. Shiozaki K, Shiozaki M, Russell P. Heat stress activates fission yeast Spc1/StyI MAPK by a MEKK-independent mechanism. Mol Biol Cell. 1998;9:1339–49.

    PubMed  CAS  Google Scholar 

  27. Hartmann T, Sasse C, Schedler A, et al. Shaping the fungal adaptome–stress responses of Aspergillus fumigatus. Med Microbiol. 2011;301:408–16.

    Article  CAS  Google Scholar 

  28. Abad A, Fernández-Molina JV, Bikandi J, et al. What makes Aspergillus fumigatus a successful pathogen? Genes and molecules involved in invasive aspergillosis. Rev Iberoam Micol. 2010;27:155–82.

    Article  PubMed  Google Scholar 

  29. Furukawa K, Katsuno Y, Urao T, et al. Isolation and functional analysis of a gene, tcsB, encoding a transmembrane hybrid-type histidine kinase from Aspergillus nidulans. Appl Environ Microbiol. 2002;68:5304–10.

    Article  PubMed  CAS  Google Scholar 

  30. Alonso-Monge R, Navarro-García F, Román E, et al. The Hog1 mitogen-activated protein kinase is essential in the oxidative stress response and chlamydospore formation in Candida albicans. Eukaryot Cell. 2003;2:351–61.

    Article  PubMed  CAS  Google Scholar 

  31. Segmüller N, Ellendorf U, Tudzynski B, et al. A stress-activated mitogen-activated protein kinase, is involved in vegetative differentiation and pathogenicity in Botrytis cinerea. Eukaryot Cell. 2007;6:211–21.

    Article  PubMed  Google Scholar 

  32. Han KH, Prade RA. Osmotic stress-coupled maintenance of polar growth in Aspergillus nidulans. Mol Microbiol. 2002;43:1065–78.

    Article  PubMed  CAS  Google Scholar 

  33. Lenassi M, Vaupotic T, Gunde-Cimerman N, et al. The MAP kinase HwHog1 from the halophilic black yeast Hortea werneckii: coping with stresses in solar salterns. Saline Syst. 2007;3:3–14.

    Article  PubMed  Google Scholar 

  34. Yang F, Ma D, Wan Z, et al. The role of sho1 in polarized growth of Aspergillus fumigatus. Mycopathologia. 2011;172:347–55.

    Article  PubMed  Google Scholar 

  35. Hohmann S. Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev. 2002;66:300–72.

    Article  PubMed  CAS  Google Scholar 

  36. Orvar BL, Sangwan V, Omann F, et al. Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity. Plant J. 2000;23:785–94.

    Article  PubMed  CAS  Google Scholar 

  37. Sangwan V, Orvar BL, Beyerly J, et al. Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. Plant J. 2002;31:629–38.

    Article  PubMed  CAS  Google Scholar 

  38. Hayashi M, Maeda T. Activation of the HOG pathway upon cold Stress in Saccharomyces cerevisiae. J Biochem. 2006;139:797–803.

    Article  PubMed  CAS  Google Scholar 

  39. Mejía R, Gómez-Eichelmann MC, Fernández MS. Membrane fluidity of Escherichia coli during heat shock. Biochim Biophys Acta. 1995;1239:195–200.

    Article  PubMed  Google Scholar 

  40. Swan TM, Watson K. Membrane fatty acid composition and membrane fluidity as parameters of stress tolerance in yeast. Can J Microbiol. 1997;43:70–7.

    Article  PubMed  CAS  Google Scholar 

  41. Rodríguez-Peña JM, García R, Nombela C, et al. The high-osmolarity glycerol (HOG) and cell wall integrity (CWI) signalling pathways interplay: a yeast dialogue between MAPK routes. Yeast. 2010;27:495–502.

    Article  PubMed  Google Scholar 

  42. Bahn YS, Geunes-Boyer S, Heitman J. Ssk2 mitogen-activated protein kinase kinase kinase governs divergent patterns of the stress-activated Hog1 signaling pathway in Cryptococcus neoformans. Eukaryot Cell. 2007;6:2278–89.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Prof. J. P. Latgé (Institute Pasteur, Paris, France) for his constructive comments on this study and the gifts of A. fumigatus △sakA, △tcsB, and wild-type DAL strains. This project was supported by the National Fund of Natural Sciences in China (No.30930006).

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Authors and Affiliations

  1. Department of Dermatology and Venereology, Peking University First Hospital, No. 8, Xi-Shi-Ku St., Xicheng District, Beijing, 100034, People’s Republic of China

    Yajuan Ji, Fang Yang, Dongmei Ma, Jinqing Zhang, Zhe Wan, Wei Liu & Ruoyu Li

  2. Research Center for Medical Mycology, Peking University, Beijing, People’s Republic of China

    Yajuan Ji, Fang Yang, Dongmei Ma, Jinqing Zhang, Zhe Wan, Wei Liu & Ruoyu Li

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  1. Yajuan Ji
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Correspondence to Ruoyu Li.

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Ji, Y., Yang, F., Ma, D. et al. HOG-MAPK Signaling Regulates the Adaptive Responses of Aspergillus fumigatus to Thermal Stress and Other Related Stress. Mycopathologia 174, 273–282 (2012). https://doi.org/10.1007/s11046-012-9557-4

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