A PLAC8-containing protein from an endomycorrhizal fungus confers cadmium resistance to yeast cells by interacting with Mlh3p

Nucleic Acids Research

Volumn 39, Issue 17, 2011, Pages 7548-7563

  Abba S ^a   Vallino, M ^a   Daghino, S ^a   Di Vietro, L ^a   Borriello, R ^a   Perotto, S ^a  

^a UNIVERSITY OF TURIN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CADMIUM; FUNGAL PROTEIN; PROTEIN OMFCR; PROTEIN PLAC8; UNCLASSIFIED DRUG;

ARTICLE; BIOTRANSFORMATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOMYCORRHIZA; FUNGAL GENE; GENE IDENTIFICATION; GENE SEQUENCE; GENETIC CONSERVATION; MISMATCH REPAIR; MLH3P GENE; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOTIDE SEQUENCE; OIDIODENDRON MAIUS; PHYSICAL RESISTANCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS; YEAST CELL;

AMINO ACID SEQUENCE; ASCOMYCOTA; CADMIUM; CELL CYCLE PROTEINS; COMPUTATIONAL BIOLOGY; DNA MISMATCH REPAIR; FUNGAL PROTEINS; GENES, FUNGAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTAGENS; MUTATION; NUCLEAR PROTEINS; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT; TRANSCRIPTION FACTORS; TWO-HYBRID SYSTEM TECHNIQUES;

EUKARYOTA; FUNGI; OIDIODENDRON MAIUS;

EID: 80053187067     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr336     Document Type: Article

References (77)

1. Hartwell, L. (1992) Defects in a cell cycle checkpoint may be responsible for the genomic instability of cancer cells. Cell, 71, 543-546.
2. Boiteux, S., Gellon, L. and Guibourt, N. (2002) Repair of 8-oxoguanine in Saccharomyces cerevisiae: interplay of DNA repair and replication mechanisms. Free Rad. Biol. Med., 32, 1244-1253. (Pubitemid 34607628)
3. Doetsch, P.W., Morey, N.J., Swanson, R.L. and Jinks-Robertson, S. (2001) Yeast Base Excision Repair: Interconnections and Networks. Academic Press Inc., San Diego.
4. Giaginis, C., Gatzidou, E. and Theocharis, S. (2006) DNA repair systems as targets of cadmium toxicity. Toxicol. Appl. Pharmacol., 213, 282-290. (Pubitemid 43833373)
5. Banerjee, S. and Flores-Rozas, H. (2005) Cadmium inhibits mismatch repair by blocking the ATPase activity of the MSH2-MSH6 complex. Nucleic Acids Res., 33, 1410-1419. (Pubitemid 41439932)
6. Clark, A.B. and Kunkel, T.A. (2004) Cadmium inhibits the functions of eukaryotic MutS complexes. J. Biol. Chem., 279, 53903-53906. (Pubitemid 40053119)
7. Jin, Y.H., Clark, A.B., Slebos, R.J.C., Al-Refai, H., Taylor, J.A., Kunkel, T.A., Resnick, M.A. and Gordenin, D.A. (2003) Cadmium is a mutagen that acts by inhibiting mismatch repair. Nat. Genet., 34, 326-329. (Pubitemid 36792867)
8. Wieland, M., Levin, M.K., Hingorani, K.S., Biro, F.N. and Hingorani, M.M. (2009) Mechanism of cadmium-mediated inhibition of Msh2-Msh6 function in DNA mismatch repair. Biochemistry, 48, 9492-9502.
9. Yen, J.L., Su, N.Y. and Kaiser, P. (2005) The yeast ubiquitin ligase SCFMet30 regulates heavy metal response. Mol. Biol. Cell, 16, 1872-1882. (Pubitemid 40471956)
10. McLaughlin, M.J., Parker, D.R. and Clarke, J.M. (1999) Metals and micronutrients-food safety issues. Field Crops Res., 60, 143-163.
11. Greszta, J., Braniewski, S., Chrzanowska, E., Nosek, A., Chlodny, J. and Zwolinski, J. (1987) The influence of dusts from chosen industrial lands on particular links of forest ecosystems of the Niepolomice forest. Ekologia Polska, 35, 291-326. (Pubitemid 19321269)
12. Martino, E., Turnau, K., Girlanda, M., Bonfante, P. and Perotto, S. (2000) Ericoid mycorrhizal fungi from heavy metal polluted soils: their identification and growth in the presence of zinc ions. Mycol. Res., 104, 338-344. (Pubitemid 30437900)
13. Abbà, S., Khouja, H.R., Martino, E., Archer, D.B. and Perotto, S. (2009) SOD1-targeted gene disruption in the ericoid mycorrhizal fungus Oidiodendron maius reduces conidiation and the capacity for mycorrhization. Mol. Plant-Microbe Interactions, 22, 1412-1421.
14. Kuge, S. and Jones, N. (1994) YAP1 dependent activation of TRX2 is essential for the response of Saccharomyces cerevisiae to oxidative stress by hydroperoxides. EMBO J., 13, 655-664. (Pubitemid 24050680)
15. Ruotolo, R., Marchini, G. and Ottonello, S. (2008) Membrane transporters and protein traffic networks differentially affecting metal tolerance: a genomic phenotyping study in yeast. Genome Biol., 9, R67.
16. Cotton, V.E., Hoffmann, E.R. and Borts, R.H. (2010) Distinct regulation of Mlh1p heterodimers in meiosis and mitosis in Saccharomyces cerevisiae. Genetics, 185, 459-467.
17. Gietz, R.D. and Woods, R.A. (2006) Yeast transformation by the LiAc/SS carrier DNA/PEG method. Methods Mol. Biol., 313, 107-120.
18. Kuwayama, H., Obara, S., Morio, T., Katoh, M., Urushihara, H. and Tanaka, Y. (2002) PCR-mediated generation of a gene disruption construct without the use of DNA ligase and plasmid vectors. Nucleic Acids Res., 30, e2.
19. Chen, C., Merrill, B.J., Lau, P.J., Holm, C. and Kolodner, R.D. (1999) Saccharomyces cerevisiae pol30 (proliferating cell nuclear antigen) mutations impair replication fidelity and mismatch repair. Mol. Cell. Biol., 19, 7801-7815. (Pubitemid 29493444)
20. Serero, A., Lopes, J., Nicolas, A. and Boiteux, S. (2008) Yeast genes involved in cadmium tolerance: identification of DNA replication as a target of cadmium toxicity. DNA Repair, 7, 1262-1275.
21. Song, W.Y., Martinoia, E., Lee, J., Kim, D., Kim, D.Y., Vogt, E., Shim, D., Choi, K.S., Hwang, I. and Lee, Y. (2004) A novel family of cys-rich membrane proteins mediates cadmium resistance in Arabidopsis. Plant Physiol., 135, 1027-1039. (Pubitemid 38819046)
22. Song, W.Y., Choi, K.S., Kim, D.Y., Geisler, M., Park, J., Vincenzetti, V., Schellenberg, M., Kim, S.H., Lim, Y.P., Noh, E.W. et al. (2010) Arabidopsis PCR2 is a zinc exporter involved in both zinc extrusion and long-distance zinc transport. Plant Cell Online, 22, 2237-2252.
23. Song, W.Y., Hö rtensteiner, S., Tomioka, R., Lee, Y. and Martinoia, E. (2011) Common functions or only phylogenetically related? The large family of PLAC8 motif-containing/PCR genes. Mol. Cells, 31, 1-7.
24. Nakagawa, Y., Katagiri, T., Shinozaki, K., Qi, Z., Tatsumi, H., Furuichi, T., Kishigami, A., Sokabe, M., Kojima, I., Sato, S. et al. (2007) Arabidopsis plasma membrane protein crucial for Ca2+influx and touch sensing in roots. PNAS, 104, 3639-3644. (Pubitemid 46364211)
25. Guo, M., Rupe, M.A., Dieter, J.A., Zou, J., Spielbauer, D., Duncan, K.E., Howard, R.J., Hou, Z. and Simmons, C.R. (2010) Cell number regulator1 affects plant and organ size in maize: implications for crop yield enhancement and heterosis. Plant Cell, 22, 1057-1073.
26. Galaviz-Hernandez, C., Stagg, C., de Ridder, G., Tanaka, T.S., Ko, M.S.H., Schlessinger, D. and Nagaraja, R. (2003) Plac8 and Plac9, novel placental-enriched genes identified through microarray analysis. Gene, 309, 81-89. (Pubitemid 36577504)
27. Rogulski, K., Li, Y., Rothermund, K., Pu, L., Watkins, S., Yi, F. and Prochownik, E.V. (2005) Onzin, a c-Myc-repressed target, promotes survival and transformation by modulating the Akt-Mdm2-p53 pathway. Oncogene, 24, 7524-7541. (Pubitemid 41638028)
28. Li, Y., Rogulski, K., Zhou, Q., Sims, P.J. and Prochownik, E.V. (2006) The negative c-Myc target onzin affects proliferation and apoptosis via its obligate interaction with phospholipid scramblase I. Mol. Cell. Biol., 26, 3401-3413.
29. Ledford, J.G., Kovarova, M. and Koller, B.H. (2007) Impaired host defense in mice lacking onzin. J. Immunol., 178, 5132-5143. (Pubitemid 46595297)
30. Wu, S.F., Huang, Y., Hou, J.K., Yuan, T.T., Zhou, C.X., Zhang, J. and Chen, G.Q. (2010) The downregulation of onzin expression by PKCe-ERK2 signaling and its potential role in AML cell differentiation. Leukemia, 24, 544-551.
31. Notredame, C., Higgins, D.G. and Heringa, J. (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol., 302, 205-217.
32. Rost, B. and Liu, J.F. (2003) The PredictProtein server. Nucleic Acids Res., 31, 3300-3304. (Pubitemid 37442144)
33. Horton, P., Park, K.J., Obayashi, T., Fujita, N., Harada, H., dams-Collier, C.J. and Nakai, K. (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res., 35, W585-W587.
34. Ceroni, A., Passerini, A., Vullo, A. and Frasconi, P. (2006) DISULFIND: a disulfide bonding state and cysteine connectivity prediction server. Nucleic Acids Res., 34, W177-W181. (Pubitemid 44529759)
35. Blom, N., Gammeltoft, S. and Brunak, S. (1999) Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol., 294, 1351-1362. (Pubitemid 30008805)
36. Fomenko, D.E., Marino, S.M. and Gladyshev, V.N. (2008) Functional diversity of cysteine residues in proteins and unique features of catalytic redox-active cysteines in thiol oxidoreductases. Mol. Cells, 26, 228-235.
37. Solioz, M. and Vulpe, C. (1996) CPx-type ATPases: a class of P-type ATPases that pump heavy metals. Trends Biochem. Sci., 21, 237-241. (Pubitemid 26228269)
38. Griffith, O.W. and Meister, A. (1979) Potent and specific inhibition of glutathione synthesis by buthionine sulfoximine (S-n-butyl homocysteine sulfoximine). J. Biol. Chem., 254, 7558-7560. (Pubitemid 10230219)
39. Gomes, D.S., Riger, C.J., Pinto, M.L.C., Panek, A.D. and Eleutherio, E.C.A. (2005) Evaluation of the role of Ace1 and Yap1 in cadmium absorption using the eukaryotic cell model Saccharomyces cerevisiae. Environ. Toxicol. Pharmacol., 20, 383-389. (Pubitemid 41318050)
40. Flores-Rozas, H. and Kolodner, R.D. (1998) The Saccharomyces cerevisiae MLH3 gene functions in MSH3-dependent suppression of frameshift mutations. Proc. Natl Acad. Sci. USA, 95, 12404-12409. (Pubitemid 28483778)
41. Witte, C., Jensen, R.E., Yaffe, M.P. and Schatz, G. (1988) MAS1, a gene essential for yeast mitochondrial assembly, encodes a subunit of the mitochondrial processing protease. EMBO J., 7, 1439-1447.
42. Vallino, M., Martino, E., Boella, F., Murat, C., Chiapello, M. and Perotto, S. (2009) Cu, Zn superoxide dismutase and zinc stress in the metal-tolerant ericoid mycorrhizal fungus Oidiodendron maius Zn. FEMS Microbiol. Lett., 293, 48-57.
43. Langlands, K., Anand, G., Yin, X. and Prochownik, E.V. (1997) Differential interactions of Id proteins with basic-helix-loop-helix transcription factors. J. Biol. Chem., 272, 19785-19793. (Pubitemid 27340071)
44. Chen, S.h., Smolka, M.B. and Zhou, H. (2007) Mechanism of Dun1 activation by Rad53 phosphorylation in Saccharomyces cerevisiae. J. Biol. Chem., 282, 986-995.
45. Jaroszewski, L., Li, Z., Krishna, S.S., Bakolitsa, C., Wooley, J., Deacon, A.M., Wilson, I.A. and Godzik, A. (2009) Exploration of uncharted regions of the protein universe. PLoS Biol., 7, e1000205.
46. Galperin, M.Y. and Koonin, E.V. (2010) From complete genome sequence to 'complete' understanding? Trends Biotechnol., 28, 398-406.
47. Finn, R.D., Mistry, J., Tate, J., Coggill, P., Heger, A., Pollington, J.E., Gavin, O.L., Gunasekaran, P., Ceric, G., Forslund, K. et al. (2010) The Pfam protein families database. Nucleic Acids Res., 38, D211-D222.
48. Galperin, M.Y. and Koonin, E.V. (2004) 'Conserved hypothetical' proteins: prioritization of targets for experimental study. Nucleic Acids Res., 32, 5452-5463. (Pubitemid 39545662)
49. Fomenko, D.E. and Gladyshev, V.N. (2003) Identity and Functions of CxxC-derived motifs. Biochemistry, 42, 11214-11225. (Pubitemid 37158888)
50. Argüello, J.M. (2003) Identification of ion-selectivity determinants in heavy-metal transport P1B-type ATPases. J. Membrane Biol., 195, 93-108. (Pubitemid 37243987)
51. Wemmie, J.A., Szczypka, M.S., Thiele, D.J. and Moye-Rowley, W.S. (1994) Cadmium tolerance mediated by the yeast AP-1 protein requires the presence of an ATP-binding cassette transporter-encoding gene, YCF1. J. Biol. Chem., 269, 32592-32597.
52. Lee, J., Godon, C., Lagniel, G., Spector, D., Garin, J., Labarre, J. and Toledano, M.B. (1999) Yap1 and Skn7 control two specialized oxidative stress response regulons in yeast. J. Biol. Chem., 274, 16040-16046.
53. Kolodner, R.D. and Marsischky, G.T. (1999) Eukaryotic DNA mismatch repair. Curr. Opin. Genetics Develop., 9, 89-96. (Pubitemid 29080392)
54. Kolas, N.K. and Cohen, P.E. (2004) Novel and diverse functions of the DNA mismatch repair family in mammalian meiosis and recombination. Cytogenet. Genome Res., 107, 216-231. (Pubitemid 39370384)
55. Hoffmann, E.R. and Borts, R.H. (2004) Meiotic recombination intermediates and mismatch repair proteins. Cytogenet. Genome Res., 107, 232-248. (Pubitemid 39370385)
56. Pang, Q., Prolla, T.A. and Liskay, R.M. (1997) Functional domains of the Saccharomyces cerevisiae Mlh1p and Pms1p DNA mismatch repair proteins and their relevance to human hereditary nonpolyposis colorectal cancer-associated mutations. Mol. Cell. Biol., 17, 4465-4473. (Pubitemid 27318123)
57. Lipkin, S.M., Wang, V., Jacoby, R., Banerjee-Basu, S., Baxevanis, A.D., Lynch, H.T., Elliott, R.M. and Collins, F.S. (2000) MLH3: a DNA mismatch repair gene associated with mammalian microsatellite instability. Nat. Genet., 24, 27-35. (Pubitemid 30041416)
58. Kondo, E., Horii, A. and Fukushige, S. (2001) The interacting domains of three MutL heterodimers in man: hMLH1 interacts with 36 homologous amino acid residues within hMLH3, hPMS1 and hPMS2. Nucleic Acids Res., 29, 1695-1702. (Pubitemid 32427850)
59. Harrington, J.M. and Kolodner, R.D. (2007) Saccharomyces cerevisiae Msh2-Msh3 acts in repair of base-base mispairs. Mol. Cell. Biol., 27, 6546-6554. (Pubitemid 47435758)
60. McMurray, C.T. and Tainer, J.A. (2003) Cancer, cadmium and genome integrity. Nat. Genet., 34, 239-241.
61. Lü tzen, A., Liberti, S.E. and Rasmussen, L.J. (2004) Cadmium inhibits human DNA mismatch repair in vivo. Biochem. Biophys. Res. Commun., 321, 21-25. (Pubitemid 39055599)
62. Liu, W., Yang, Y.S., Francis, D., Rogers, H.J., Li, P. and Zhang, Q. (2008) Cadmium stress alters gene expression of DNA mismatch repair related genes in Arabidopsis seedlings. Chemosphere, 73, 1138-1144.
63. Liu, W., Zhou, Q., Li, P., Gao, H., Han, Y.P., Li, X.J., Yang, Y.S. and Li, Y. (2009) DNA mismatch repair related gene expression as potential biomarkers to assess cadmium exposure in Arabidopsis seedlings. J. Hazardous Mater., 167, 1007-1013.
64. Fujs, S., Gazdag, Z., Poljsak, B., Stibilj, V., Milacic, R., Pesti, M., Raspor, P. and Batic, M. (2005) The oxidative stress response of the yeast Candida intermedia to copper, zinc, and selenium exposure. J. Basic Microbiol., 45, 125-135. (Pubitemid 40589307)
65. Samikkannu, T., Chen, C.H., Yih, L.H., Wang, A.S.S., Lin, S.Y., Chen, T.C. and Jan, K.Y. (2003) Reactive oxygen species are involved in arsenic trioxide inhibition of pyruvate dehydrogenase activity. Chem. Res. Toxicol., 16, 409-414. (Pubitemid 36373706)
66. Chiou, T.J. and Tzeng, W.F. (2000) The roles of glutathione and antioxidant enzymes in menadione-induced oxidative stress. Toxicology, 154, 75-84.
67. Davidson, J.F., Whyte, B., Bissinger, P.H. and Schiestl, R.H. (1996) Oxidative stress is involved in heat-induced cell death in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA, 93, 5116-5121. (Pubitemid 26162880)
68. Prakash, S. and Prakash, L. (2000) Nucleotide excision repair in yeast. Mutation Res/Fundamental and Mol. Mech. Mutagenesis, 451, 13-24. (Pubitemid 30488101)
69. Cortes-Ledesma, F. and Aguilera, A. (2006) Double-strand breaks arising by replication through a nick are repaired by cohesin-dependent sister-chromatid exchange. EMBO Rep., 7, 919-926. (Pubitemid 44523972)
70. van Peer, A.F., de Bekker, C., Vinck, A., Wosten, H.A.B. and Lugones, L.G. (2009) Phleomycin increases transformation efficiency and promotes single integrations in Schizophyllum commune. Appl. Environ. Microbiol., 75, 1243-1247.
71. O'Brien, V. and Brown, R. (2006) Signalling cell cycle arrest and cell death through the MMR system. Carcinogenesis, 27, 682-692.
72. Wang, J.Y.J. and Edelmann, W. (2006) Mismatch repair proteins as sensors of alkylation DNA damage. Cancer Cell, 9, 417-418. (Pubitemid 43842122)
73. Polosina, Y.Y. and Cupples, C.G. (2010) Wot the [']L-Does MutL do? Mutat. Res./Rev. Mut. Res., 705, 228-238.
74. Frary, A., Nesbitt, T.C., Frary, A., Grandillo, S., Knaap, E.V.D., Cong, B., Liu, J., Meller, J., Elber, R., Alpert, K.B. et al. (2000) Fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science, 289, 85-88. (Pubitemid 30463294)
75. Cong, B. and Tanksley, S.D. (2006) FW2.2 and cell cycle control in developing tomato fruit: a possible example of gene co-option in the evolution of a novel organ. Plant Mol. Biol., 62, 867-880. (Pubitemid 44730324)
76. Libault, M., Zhang, X.C., Govindarajulu, M., Qiu, J., Ong, Y.T., Brechenmacher, L., Berg, R.H., Hurley-Sommer, A., Taylor, C.G. and Stacey, G. (2010) A member of the highly conserved FWL (tomato FW2.2-like) gene family is essential for soybean nodule organogenesis. Plant J., 62, 852-864.
77. Libault, M. and Stacey, G. (2010) Evolution of FW2.2-like (FWL) and PLAC8 genes in eukaryotes. Plant Signal. Behavior, 5, 1226-1228.