The response of Mucor plumbeus to pentachlorophenol: A toxicoproteomics study

Journal of Proteomics

Volumn 78, Issue , 2013, Pages 159-171

  Carvalho, M B ^a   Martins, I ^a,b   Medeiros, J ^a   Tavares, S ^a   Planchon, S ^c   Renaut, J ^c   Nunez O ^d   Gallart Ayala, H ^d   Galceran, M T ^d   Hursthouse, A ^e   Silva Pereira, C ^a,b  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^b INSTITUTO DE BIOLOGIA EXPERIMENTAL E TECNOLÓGICA   (Portugal)

^c LUXEMBOURG INSTITUTE OF SCIENCE AND TECHNOLOGY   (Luxembourg)

^d UNIVERSITY OF BARCELONA   (Spain)

^e UNIVERSITY OF THE WEST OF SCOTLAND   (United Kingdom)

Author keywords

Detoxification; Mucor plumbeus; Oxidative stress; Pentachlorophenol; Toxicoproteomics; Zygomycota

Indexed keywords

CYTOCHROME C PEROXIDASE; HEAT SHOCK PROTEIN 70; PENTACHLOROPHENOL; VASOPRESSIN; ZINC;

ARTICLE; CELL WALL; CYTOSKELETON; ENERGY; ENZYME DEGRADATION; GEL ELECTROPHORESIS; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MITOCHONDRION; MUCOR; MYCELIUM; NUCLEOTIDE SEQUENCE; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; STRESS; TOXICITY; ZYGOMYCETES;

BIOTRANSFORMATION; ENVIRONMENTAL POLLUTANTS; FUNGAL PROTEINS; MUCOR; PENTACHLOROPHENOL; PROTEOMICS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

FUNGI; MUCOR PLUMBEUS; ZYGOMYCOTA;

EID: 84871778585     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2012.11.006     Document Type: Article

References (83)

1. Crosby D.G. Iupac reports on pesticides: (14) environmental chemistry of pentachlorophenol. Pure Appl Chem 1981, 53:1051-1080.
2. Czaplicka M. Sources and transformations of chlorophenols in the natural environment. Sci Total Environ 2004, 322:21-39.
3. McLellan I., Carvalho M., Silva Pereira C., Hursthouse A., Morrison C., Tatner P., et al. The environmental behaviour of polychlorinated phenols and its relevance to cork forest ecosystems: a review. J Environ Monit 2007, 9:1055-1063.
4. McAllister K.A., Lee H., Trevors J.T. Microbial degradation of pentachlorophenol. Biodegradation 1996, 7:1-40.
5. Proudfoot A.T. Pentachlorophenol poisoning. Toxicol Rev 2003, 22:3-11.
6. Dong Y.L., Zhou P.J., Jiang S.Y., Pan X.W., Zhao X.H. Induction of oxidative stress and apoptosis by pentachlorophenol in primary cultures of Carassius carassius hepatocytes. Comp Biochem Physiol C-Toxicol Pharmacol 2009, 150:179-185.
7. Chen X., Yin D., Hu S., Hou Y. Immunotoxicity of pentachlorophenol on macrophage immunity and IgM secretion of the Crucian carp (Carassius auratus). Bull Environ Contam Toxicol 2004, 73:153-160.
8. Yang S.Z., Han X.D., Wei C., Chen J.X., Yin D.Q. The toxic effects of pentachlorophenol on rat Sertoli cells in vitro. Environ Toxicol Pharmacol 2005, 20:182-187.
9. Chen J., Jiang J., Zhang F., Yu H., Zhang J. Cytotoxic effects of environmentally relevant chlorophenols on L929 cells and their mechanisms. Cell Biol Toxicol 2004, 20:183-196.
10. Fernández Freire P., Labrador V., Pérez Martín J.M., Hazen M.J. Cytotoxic effects in mammalian Vero cells exposed to pentachlorophenol. Toxicology 2005, 210:37-44.
11. Wispriyono B., Matsuoka M., Igisu H. Effects of pentachlorophenol and tetrachlorohydroquinone on mitogen-activated protein kinase pathways in Jurkat T cells. Environ Health Perspect 2002, 110:139-143.
12. Wang Y.J., Lee C.C., Chang W.C., Liou H.B., Ho Y.S. Oxidative stress and liver toxicity in rats and human hepatoma cell line induced by pentachlorophenol and its major metabolite tetrachlorohydroquinone. Toxicol Lett 2001, 122:157-169.
13. Harms H., Schlosser D., Wick L.Y. Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Nat Rev Microbiol 2011, 9:177-192.
14. Kataoka R., Takagi K., Kamei I., Kiyota H., Sato Y. Biodegradation of dieldrin by a soil fungus isolated from a soil with annual endosulfan applications. Environ Sci Technol 2010, 44:6343-6349.
15. León-Santiestebán H., Bernal R., Fernández F.J., Tomasini A. Tyrosinase and peroxidase production by Rhizopus oryzae strain ENHE obtained from pentachlorophenol-contaminated soil. J Chem Technol Biotechnol 2008, 83:1394-1400.
16. Pinedo-Rivilla C., Aleu J., Collado I.G. Pollutants biodegradation by fungi. Curr Org Chem 2009, 13:1194-1214.
17. Webster J., Weber R.W.S. Introduction to fungi 2007, Cambridge University Press, New York. 3rd ed.
18. Santos P.M., Simões T., Sá-Correia I. Insights into yeast adaptive response to the agricultural fungicide mancozeb: a toxicoproteomics approach. Proteomics 2009, 9:657-670.
19. Bombek L.K., Lapornik A., Ukmar M., Matis M., Črešnar B., Katalinić J.P., et al. Aspects of the progesterone response in Hortaea werneckii: steroid detoxification, protein induction and remodelling of the cell wall. Steroids 2008, 73:1465-1474.
20. Kim Y., Nandakumar M.P., Marten M.R. Proteomics of filamentous fungi. Trends Biotechnol 2007, 25:395-400.
21. Medina M.L., Haynes P.A., Breci L., Francisco W.A. Analysis of secreted proteins from Aspergillus flavus. Proteomics 2005, 5:3153-3161.
22. Fang Y., Gao X., Zha J., Ning B., Li X., Gao Z., et al. Identification of differential hepatic proteins in rare minnow (Gobiocypris rarus) exposed to pentachlorophenol (PCP) by proteomic analysis. Toxicol Lett 2010, 199:69-79.
23. Carvalho M.B., Martins I., Leitão M.C., Garcia H., Rodrigues C., San Romão V., et al. Screening pentachlorophenol degradation ability by environmental fungal strains belonging to the phyla Ascomycota and Zygomycota. J Ind Microbiol Biotechnol 2009, 36:1249-1256.
24. Carvalho M.B., Tavares S., Medeiros J., Núñez O., Gallart-Ayala H., Leitão M.C., et al. Degradation pathway of pentachlorophenol by Mucor plumbeus involves phase II conjugation and oxidation-reduction reactions. J Hazard Mater 2011, 198:133-142.
25. Kniemeyer O., Lessing F., Scheibner O., Hertweck C., Brakhage A.A. Optimisation of a 2-D gel electrophoresis protocol for the human-pathogenic fungus Aspergillus fumigatus. Curr Genet 2006, 49:178-189.
26. Ramagli L.S. Quantifying protein in 2-D PAGE solubilization buffers. 2-D Proteome analysis protocols 1999, 99-103. Humana Press Inc., Totowa.
27. Kang Y.Y., Techanukul T., Mantalaris A., Nagy J.M. Comparison of three commercially available DIGE analysis software packages: minimal user intervention in gel-based proteomics. J Proteome Res 2009, 8:1077-1084.
28. Valledor L., Jorrín J. Back to the basics: maximizing the information obtained by quantitative two dimensional gel electrophoresis analyses by an appropriate experimental design and statistical analyses. J Proteomics 2011, 74:1-18.
29. Perkins D.N., Pappin D.J.C., Creasy D.M., Cottrell J.S. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999, 20:3551-3567.
30. Grigoriev I.V., Nordberg H., Shabalov I., Aerts A., Cantor M., Goodstein D., et al. The genome portal of the Department of Energy Joint Genome Institute. Nucleic Acids Res 2012, 40:D26-D32.
31. Condell O., Sheridan A., Power K.A., Bonilla-Santiago R., Sergeant K., Renaut J., et al. Comparative proteomic analysis of Salmonella tolerance to the biocide active agent triclosan. J Proteomics 2012, 75:4505-4519.
32. Sergeant K., Spieβ N., Renaut J., Wilhelm E., Hausman J.F. One dry summer: a leaf proteome study on the response of oak to drought exposure. J Proteomics 2011, 74:1385-1395.
33. Ruepp A., Zollner A., Maier D., Albermann K., Hani J., Mokrejs M., et al. The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res 2004, 32:5539-5545.
34. UniProt C. Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res 2012, 40:D71-D75.
35. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J.H., Zhang Z., Miller W., et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.
36. Bendtsen J.D., Jensen L.J., Blom N., von Heijne G., Brunak S. Feature-based prediction of non-classical and leaderless protein secretion. Protein Eng Des Sel 2004, 17:349-356.
37. Bendtsen J.D., Nielsen H., von Heijne G., Brunak S. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 2004, 340:783-795.
38. Mann M., Jensen O.N. Proteomic analysis of post-translational modifications. Nat Biotechnol 2003, 21:255-261.
39. Vödisch M., Albrecht D., Leβing F., Schmidt A.D., Winkler R., Guthke R., et al. Two-dimensional proteome reference maps for the human pathogenic filamentous fungus Aspergillus fumigatus. Proteomics 2009, 9:1407-1415.
40. Schlüter H., Apweiler R., Holzhütter H.G., Jungblut P.R. Finding one's way in proteomics: a protein species nomenclature. Chem Cent J 2009, 3.
41. Folch J., Yeste-Velasco M., Alvira D., de la Torre A.V., Bordas M., López M., et al. Evaluation of pathways involved in pentachlorophenol-induced apoptosis in rat neurons. Neurotoxicology 2009, 30:451-458.
42. Yadav V., Shitiz K., Pandey R., Yadav J. Chlorophenol stress affects aromatic amino acid biosynthesis - a genome-wide study. Yeast 2011, 28:81-91.
43. Rangel-Porras R.A., Meza-Carmen V., Martinez-Cadena G., Torres-Guzmán J.C., González-Hernández G.A., Arnau J., et al. Molecular analysis of an NAD-dependent alcohol dehydrogenase from the zygomycete Mucor circinelloides. Mol Genet Genomics 2005, 274:354-363.
44. +-dependent alcohol dehydrogenase activities in YR-1 strain of Mucor circinelloides a potential bioremediator of petroleum contaminated soils. Appl Biochem Biotechnol 2005, 121:279-288.
45. Zazueta-Sandoval R., Gutiérrez-Corona J.F. Developmental and environmental influences in the production of a single NAD-dependent fermentative alcohol dehydrogenase by the zygomycete Mucor rouxii. Arch Microbiol 1999, 172:280-286.
46. Kollock R., Mein W., Schneider H., Batke M., Frank H., Seidel A., et al. Efficient oxidation of promutagenic hydroxymethylpyrenes by cDNA-expressed human alcohol dehydrogenase ADH2 and its inhibition by various agents. Biochem Pharmacol 2008, 75:527-537.
47. Kollock R., Rost K., Batke M., Glatt H. Effect of pentachlorophenol and 2,6-dichloro-4-nitrophenol on the activity of cDNA-expressed human alcohol and aldehyde dehydrogenases. Toxicol Lett 2009, 191:360-364.
48. Reddy G.V., Gold M.H. Degradation of pentachlorophenol by Phanerochaete chrysosporium: intermediates and reactions involved. Microbiology 2000, 146:405-413.
49. Lubbehusen T.L., Nielsen J., McIntyre M. Aerobic and anaerobic ethanol production by Mucor circinelloides during submerged growth. Appl Microbiol Biotechnol 2004, 63:543-548.
50. Volkov A.N., Nicholls P., Worrall J.A.R. The complex of cytochrome c and cytochrome c peroxidase: the end of the road?. Biochim Biophys Acta 2011, 1807:1482-1503.
51. Tunc-Ozdemir M., Miller G., Song L.H., Kim J., Sodek A., Koussevitzky S., et al. Thiamin confers enhanced tolerance to oxidative stress in arabidopsis. Plant Physiol 2009, 151:421-432.
52. Chiapello M., Daghino S., Martino E., Perotto S. Cellular response of Fusarium oxysporum to crocidolite asbestos as revealed by a combined proteomic approach. J Proteome Res 2010, 9:3923-3931.
53. Asensi-Fabado M.A., Munné-Bosch S. Vitamins in plants: occurrence, biosynthesis and antioxidant function. Trends Plant Sci 2010, 15:582-592.
54. Zhao G.Z., Hou L.H., Yao Y.P., Wang C.L., Cao X.H. Comparative proteome analysis of Aspergillus oryzae 3.042 and A. oryzae 100-8 strains: Towards the production of different soy sauce flavors. J Proteomics 2012, 75:3914-3924.
55. Morales M., Planelló R., Martínez-Paz P., Herrero O., Cortés E., Martínez-Guitarte J.L., et al. Characterization of Hsp70 gene in Chironomus riparius: expression in response to endocrine disrupting pollutants as a marker of ecotoxicological stress. Comp Biochem Physiol C-Toxicol Pharmacol 2011, 153:150-158.
56. Bierkens J., Maes J., Vander Plaetse F. Dose-dependent induction of heat shock protein 70 synthesis in Raphidocelis subcapitata following exposure to different classes of environmental pollutants. Environ Pollut 1998, 101:91-97.
57. Pincus D., Chevalier M.W., Aragón T., van Anken E., Vidal S.E., El-Samad H., et al. BiP Binding to the ER-stress sensor ire1 tunes the homeostatic behavior of the unfolded protein response. PLoS Biol 2010, 8.
58. Boström S.L., Johansson R.G. Effects of pentachlorophenol on enzymes involved in energy metabolism in liver of eel. Comp Biochem Physiol 1972, 41:359-369.
59. Szabados L., Savouré A. Proline: a multifunctional amino acid. Trends Plant Sci 2010, 15:89-97.
60. Pronk J.T., Steensma H.Y., Van Dijken J.P. Pyruvate metabolism in Saccharomyces cerevisiae. Yeast 1996, 12:1607-1633.
61. Battaglia E., Benoit I., van den Brink J., Wiebenga A., Coutinho P.M., Henrissat B., et al. Carbohydrate-active enzymes from the zygomycete fungus Rhizopus oryzae: a highly specialized approach to carbohydrate degradation depicted at genome level. BMC Genomics 2011, 12.
62. Hohmann S., Meacock P.A. Thiamin metabolism and thiamin diphosphate-dependent enzymes in the yeast Saccharomyces cerevisiae: genetic regulation. Biochim Biophys Acta 1998, 1385:201-219.
63. Tsigos I., Martinou A., Kafetzopoulos D., Bouriotis V. Chitin deacetylases: new, versatile tools in biotechnology. Trends Biotechnol 2000, 18:305-312.
64. Ghormade V., Kulkarni S., Doiphode N., Rajamohanan P.R., Deshpande M.V. Chitin deacetylase: a comprehensive account on its role in nature and its biotechnological applications. Current research, technology and education topics in applied microbiology and microbial biotechnology: Formatex Research Center 2010, 1054-1066. A. Méndez-Vilas (Ed.).
65. Kang T.H., Hwang E.I., Yun B.S., Park K.D., Kwon Y.M., Shin C.S., et al. Inhibition of chitin synthases and antifungal activities by 2'-benzoyloxycinnamaldehyde from Pleuropterus ciliinervis and its derivatives. Biol Pharm Bull 2007, 30:598-602.
66. Emri T., Molnár Z., Pusztahelyi T., Pócsi I. Physiological and morphological changes in autolyzing Aspergillus nidulans cultures. Folia Microbiol 2004, 49:277-284.
67. Göthel S.F., Marahiel M.A. Peptidyl-prolyl cis-trans isomerases, a superfamily of ubiquitous folding catalysts. Cell Mol Life Sci 1999, 55:423-436.
68. Moseley J.B., Goode B.L. The yeast actin cytoskeleton: from cellular function to biochemical mechanism. Microbiol Mol Biol Rev 2006, 70:605-645.
69. Lasserre J.P., Fack F., Revets D., Planchon S., Renaut J., Hoffmann L., et al. Effects of the endocrine disruptors atrazine and PCB 153 on the protein expression of MCF-7 human cells. J Proteome Res 2009, 8:5485-5496.
70. White P., Aberle H., Vincent J.P. Signaling and adhesion activities of mammalian β-catenin and plakoglobin in Drosophila. J Cell Biol 1998, 140:183-195.
71. Jamieson C., Sharma M., Henderson B.R. Wnt signaling from membrane to nucleus: β-catenin caught in a loop. Int J Biochem Cell Biol 2012, 44:847-850.
72. Zhao Y., Park R.D., Muzzarelli R.A.A. Chitin deacetylases: properties and applications. Mar Drugs 2010, 8:24-46.
73. Ibba M., Söll D. Aminoacyl-tRNA synthesis. Annu Rev Biochem 2000, 69:617-650.
74. Brown M.V., Reader J.S., Tzima E. Mammalian aminoacyl-tRNA synthetases: cell signaling functions of the protein translation machinery. Vasc Pharmacol 2010, 52:21-26.
75. Espino J.J., Gutiérrez-Sánchez G., Brito N., Shah P., Orlando R., González C. The Botrytis cinerea early secretome. Proteomics 2010, 10:3020-3034.
76. Cherrad S., Girard V., Dieryckx C., Gonçalves I.R., Dupuy J.-W., Bonneu M., et al. Proteomic analysis of proteins secreted by Botrytis cinerea in response to heavy metal toxicity. Metallomics 2012, 4:835-846.
77. Manavalan A., Adav S.S., Sze S.K. iTRAQ-based quantitative secretome analysis of Phanerochaete chrysosporium. J Proteomics 2011, 75:642-654.
78. Chaffin W.L., López-Ribot J.L., Casanova M., Gozalbo D., Martínez J.P. Cell wall and secreted proteins of Candida albicans: identification, function, and expression. Microbiol Mol Biol Rev 1998, 62:130-180.
79. Nombela C., Gil C., Chaffin W.L. Non-conventional protein secretion in yeast. Trends Microbiol 2006, 14:15-21.
80. Sirover M.A. On the functional diversity of glyceraldehyde-3-phosphate dehydrogenase: biochemical mechanisms and regulatory control. Biochim Biophys Acta 2011, 1810:741-751.
81. Tristan C., Shahani N., Sedlak T.W., Sawa A. The diverse functions of GAPDH: views from different subcellular compartments. Cell Signal 2011, 23:317-323.
82. Lim D.B., Hains P., Walsh B., Bergquist P., Nevalainen H. Proteins associated with the cell envelope of Trichoderma reesei: a proteomic approach. Proteomics 2001, 1:899-909.
83. Jaszek M., Grzywnowicz K., Malarczyk E., Leonowicz A. Enhanced extracellular laccase activity as a part of the response system of white rot fungi: Trametes versicolor and Abortiporus biennis to paraquat-caused oxidative stress conditions. Pest Biochem Physiol 2006, 85:147-154.