Transcription of the Neurospora crassa 70-kDa class heat shock protein genes is modulated in response to extracellular pH changes

Cell Stress and Chaperones

Volumn 15, Issue 2, 2010, Pages 225-231

  Squina, Fabio M ^a,b   Leal, Juliana ^a   Cipriano, Vivian T F ^a   Martinez Rossi, Nilce M ^a   Rossi, Antonio ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b Associacao Brasileira de Informatica   (Brazil)

Author keywords

Heat shock; Hsp70; Neurospora crassa; Nuc 1; Pacc; Ph regulation; Pi sensing

Indexed keywords

HEAT SHOCK PROTEIN 70; NUC 1 PROTEIN; PACC PROTEIN; PHOSPHATE; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; FUNGUS GROWTH; GENE EXPRESSION; GENE INDUCTION; HEAT SHOCK RESPONSE; MYCELIUM; NEUROSPORA CRASSA; NONHUMAN; PH; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; EXTRACELLULAR SPACE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; PHYLOGENY;

EUKARYOTA; NEUROSPORA CRASSA; PROKARYOTA;

EXTRACELLULAR SPACE; GENE EXPRESSION REGULATION, FUNGAL; HSP70 HEAT-SHOCK PROTEINS; HYDROGEN-ION CONCENTRATION; NEUROSPORA CRASSA; PHYLOGENY; TRANSCRIPTION, GENETIC;

EID: 77950360438     PISSN: 13558145     EISSN: 14661268     Source Type: Journal    
DOI: 10.1007/s12192-009-0131-z     Document Type: Article

References (62)

1. Britton ME, Kapoor M (2002) The oligomeric state, complex formation, and chaperoning activity of hsp70 and hsp80 of Neurospora crassa. Biochem Cell Biol 80:797-809
2. Bukau B, Weissman J, Horwich A (2006) Molecular chaperones and protein quality control. Cell 125:443-451
3. Caddick MX, Brownlee AG, Arst HN (1986) Regulation of geneexpression by pH of the growth-medium in Aspergillus nidulans. Mol Gen Genet 203:346-353
4. Christis C, Lubsen NH, Braaknian I (2008) Protein folding includes oligomerization-examples from the endoplasmic reticulum, and cytosol. FEBS J 275:4700-4727
5. Craig EA, Kramer J, Shilling J, Werner-Washburne M, Holmes S, Kosic-Smitliers J, Nicolet CM (1989) SSC1, an essential member of the yeast HSP70 multigene family, encodes a mitochondrial protein. Mol Cell. Biol 9:3000-3008 (Pubitemid 19163064)
6. Daugaard M, Rohde M, Jaattela M (2007) The heat shock protein 70 family: Highly homologous proteins with overlapping and distinct functions. FEBS Lett 581:3702-3710 (Pubitemid 47081009)
7. Deocaris CC, Kaul SC, Wadhwa R (2006) On the brotherhood of the mitochondrial, chaperones mortalin and heat shock protein 60. Cell Stress Chaperones 11:116-128
8. Ellis RJ (2006) Molecular chaperones: assisting assembly in addition to folding. Trends Biochem Sci 31:395-401 (Pubitemid 44038913)
9. Ellwood MS, Craig EA (1984) Differential regulation of the 70 K heat shock gene and related genes in Saccharomyces cerevisiae. Mol Cell Biol 4:1454-1459
10. Faircloth LM, Churchill PF, Caldwell GA, Caldwell KA (2009) The microtubule-associated protein, NUD-1, exhibits chaperone activity in vitro. Cell Stress Chaperones 14:95-103
11. Fox GC, Shafiq M, Briggs DC, Knowles PP, Collister M et al (2007) Redox-mediated substrate recognition by Sdpl defines a new group of tyrosine phosphatases. Nature 447:487-492
12. Freitag DG, Ouimet PM, Girvitz TL, Kapoor M (1997) Heat shock protein 80 of Neurospora crassa, a cytosolic molecular chaper-one of the eukaryotic stress 90 family, interacts directly with heat shock protein 70. Biochemistry 36:10221-10229
13. Freitas JS, Silva EM, Rossi A (2007) Identification of nutrientdependent changes in extracellular pH and acid phosphatase secretion in Aspergillus nidulans. Genet Mol Res 6:721-729
14. Galagan JE, Calvo SE, Borkovich KA, Selker EU, Read ND et al (2003) The genome sequence of the filamentous fungus Neurospora crassa. Nature 422:859-868
15. Georg RC, Gomes SL (2007) Comparative expression analysis of members of the Hsp70 family in the chytridiomycete Blastocladiella emersonii. Gene 386:24-34
16. Gras DE, Silveira HCS, Martinez-Rossi NM, Rossi A (2007) Identification of genes displaying differential expression in the nuc-2 mutant strain of the mold Neurospora crassa grown under phosphate starvation. FEMS Microbiol Lett 269:196-200
17. Gras DE, Silveira HCS, Peres NTA, Sanches PR, Martinez-Rossi NM, Rossi A (2009) Transcriptional changes in the nuc-2A mutant strain of Neurospora crassa cultivated under conditions of phosphate shortage. Microbiol Res . doi:10.1016/j.micres.2008.1012.1005
18. Hahn JS, Neef DW, Thiele DJ (2006) A stress regulatory network for co-ordinated activation of proteasome expression mediated by yeast heat shock transcription factor. Mol Microbiol 60:240-251
19. Haiti FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852-1858
20. Hashikawa N, Yamamoto N, Sakurai H (2007) Different mechanisms are involved in the transcriptional activation by yeast heat shock transcription factor through two different types of heat shock elements. J Biol Chem 282:10333-10340 (Pubitemid 47093400)
21. Hohmann S (2002) Osmotic stress signaling and osmoadaptation in yeasts. Microbiol MbI Biol Rev 66:300-372
22. Kalmar B, Greensmith L (2009) Induction of heat shock proteins for protection against oxidative stress. Adv Drug Deliv Rev 61 (4):310-318. doi: 10.1016/j.addr.2009.1002.1003
23. Kang S (1993) Functional domains of the transcriptional activator NUC-I in Neurospora crassa. Gene 130:259-264
24. +, a gene controlling phosphorus acquisition in Neurospora crassa. Mol Cell. Biol. 10:5839-5848
25. Kapoor M, Curie CA, Runham C (1995) The Hsp70 gene family of Neurospora crassa-cloning, sequence-analysis, expression, and genetic-mapping of the major stress-inducible member. J Bacteriol 177:212-221
26. Kregel KC (2002) Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J Appl Physiol 92:2177-2186
27. Lamb TM, Mitchell AP (2003) The transcription factor Rim 101p governs ion tolerance and cell differentiation by direct repression of the regulatory genes NRG1 and SMP1 in Saccharomyces cerevisiae. MoI Cell Biol 23:677-686
28. c mutant strain of Neurospora crassa grown under phosphate starvation. Can J Microbiol 53:1011-1015
29. Leal J, Squina FM, Freitas JS, Silva EM, Ono CJ, Martinez-Rossi NM, Rossi A (2009) A splice variant of the Neurospora crassa hex-1 transcript, which encodes the major protein of the Woronin body, is modulated by extracellular phosphate and pH changes. FEBS Lett 583:180-184
30. Li F, Luan W, Zhang C, Zhang J, Wang B, Xie Y, Li S, Xiang J (2009) Cloning of cytoplasmic heat shock protein 90 (FcHSP90) from Fenneropenaeus chinensis and its expression response to heat shock and hypoxia. Cell. Stress Chaperones 14:161-172
31. Mayer MP, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62:670-684 (Pubitemid 40500927)
32. McCluskey K (2003) The Fungal. Genetics Stock. Center: from molds to molecules. Adv Appl Microbiol 52:245-262
33. Metzenberg RL (1979) Implications of some genetic control mechanisms in Neurospora. Microbiol Rev 43:361-383
34. Montero-Barrientos M, Hermosa R, Nicolas C, Cardoza RE, Gutierrez S, Monte E (2008) Overexpression of a Trichoderma HSP70 gene increases fungal resistance to heat and other abiotic stresses. Fungal Genet. Biol 45:1506-1513
35. Nahas E, Terenzi HF, Rossi A (1982) Effect of carbon source and pH on the production and secretion of acid-phosphatase (EC3.1.3.2) and. alkaline-phosphatase (EC3.1.3.1) in Neurospora crassa. J Gen Microbiol 128:2017-2021 (Pubitemid 13231358)
36. Nicchitta CV (2009) Cell biology: how to combat stress. Nature 457:668-669
37. Nozawa SR, Ferreira-Nozawa MS, Martinez-Rossi NM, Rossi A (2003a) The pH-induced glycosylation of secreted phosphatases is mediated in Aspergillus nidulans by the regulatory gene pacCdependent pathway. Fungal Genet Biol. 39:286-295
38. Nozawa SR, May GS, Martinez-Rossi NM, Ferreira-Nozawa MS, Coutinlio-Netto J, Maccheroni W Jr, Rossi A (2003b) Mutation in a calpain-like protease affects the posttranslational mannosylation of phosphatases in Aspergillus nidulans. Fungal Genet Biol 38:220-227
39. Ogawa N, DeRisi J, Brown PO (2000) New components of a system for phosphate accumulation and polyphosphate metabolism in Saccharomyces cerevisiae revealed by genomic expression analysis. Mol Biol Cell 11:4309-4321
40. Peleg Y, Addison R, Aramayo R, Metzenberg RL (1996a) Translocation of Neurospora crassa transcription factor NUC-1 into the nucleus is induced by phosphorus limitation. Fungal Genet Biol 20:185-191
41. Peleg Y, Aramayo R, Kang S, Hall JG, Metzenberg RL (1996b) NUC-2, a component of the phosphate-regulated signal transduction pathway in Neurospora crassa, is an ankyrin repeat protein. Mol Gen Genet 252:709-716
42. Peflas MM, Hervas-Aguilar A, Munera-Huertas T, Reoyo E, Penalva MA, Arst HN Jr, Tilbum J (2007) Further characterization of the signaling proteolysis step in the Aspergillus nidulans pH signal transduction pathway. Eukaryot Cell 6:960-970
43. Perez-Esteban B, Orejas M, Gomez-Pardo E, Penalva MA (1993) Molecular characterization of a fungal, secondary metabolism promoter: transcription of the Aspergillus nidulans isopenicillin N synthetase gene is modulated by upstream negative elements. Mol Microbiol 9:881-895
44. Plesofsky NS, Levery SB, Castle SA, Brambl R (2008) Stress-induced cell death is mediated by ceramide synthesis in Neurospora crassa. Eukaryot. Cell 7:2147-2159
45. Ramon AM, Fonzi WA (2003) Diverged binding specificity of RimlOlp, the Candida albicans ortholog of PacC. Eukaryot Cell 2:718-728
46. Rensing L, Monnerjahn C, Meyer U (1998) Differential stress gene expression during the development of Neurospora crassa and other fungi. FEMS Microbiol Lett 168:159-166
47. Rezaie S, Ban J, Mildner M, Poitschek. C, Brna C, Tschachler E (2000) Characterization of a cDNA clone, encoding a 70 kDa heat shock protein from the dermatophyte pathogen Trichophyton rubrum. Gene 241:27-33
48. Ritossa F (1962) A new puffing pattern induced by temperature shock and DNP in Drosophila. Experientia 18:571-573
49. Ritossa F (1996) Discovery of the heat shock response. Cell Stress Chaperones 1:97-98
50. Rodrigues SA, Rossi A (1985) Effect of phosphate levels on the synthesis of acid phosphatases (EC 3.1.3.2) in Neurospora crassa. Genet Res 45:239-249 (Pubitemid 15027404)
51. Sakurai H, Takemori Y (2007) Interaction between heat shock transcription factors (HSFs) and divergent binding sequences: binding specificities of yeast HSFs and human HSF1. J Biol Chem 282:13334-13341 (Pubitemid 47100495)
52. Selker EU, Garrett PW (1988) DNA-Sequence Duplications Trigger Gene Inactivation in Neurospora crassa. Proc Natl Acad Sci U S A. 85:6870-6874
53. Silva EM, Freitas JS, Gras DE, Squina FM, Leal J, Silveira HCS, Martinez-Rossi NM, Rossi A (2008) Identification of genes differentially expressed in a strain of the mold Aspergillus nidulans carrying a loss-of-function mutation in the palA gene. Can J Microbiol 54:803-811
54. Steel GJ, Fullerton DM, Tyson JR, Stirling CJ (2004) Coordinated activation of Hsp70 chaperones. Science 303:98-101
55. Thompson S, Croft NJ, Sotiriou A, Piggins HD, Crosthwaite SK (2008) Neurospora crassa heat shock factor 1 is an essential gene; a second heat shock factor-like gene, hsf2, is required for asexual spore formation. Eukaryot Cell 7:1573-1581
56. Tilburn J, Sarkar S, Widdick DA, Espeso EA, Orejas M, Mungroo J, Peñalva MA, Arst HN Jr (1995) The Aspergillus PacC zinc finger transcription factor mediates regulation of both acid- and alkaline-expressed genes by ambient pH. EMBO J 14:779-790
57. Tokuriki N, Tawfik. DS (2009) Chaperonin overexpression promotes genetic variation and enzyme evolution. Nature 459:668-673
58. Tremmel D, Duarte M, Videira A, Tropschug M (2007) FKBP22 is part of chaperone/folding catalyst complexes in the endoplasmic reticulum of Neurospora crassa. FEBS Lett 581:2036-2040
59. Turkel S, Turgut T, Kayakent N (2006) Effect of osmotic stress on the derepression of invertase synthesis in nonconventional yeasts. Lett Appl Microbiol 42:78-82
60. Ungermann C, Neupert W, Cyr DM (1994) The role of Hsp70 in conferring unidirectionality on protein translocation into mitochondria. Science 266:1250-1253 (Pubitemid 24371284)
61. Werner-Washburne M, Becker J, Kosic-Smitliers J, Craig EA (1989) Yeast Hsp70 RNA levels vary in response to the physiological status of the cell. J Bacteriol 171:2680-2688
62. Xavier IJ, Kliachatourians GG, Ovsenek N (1999) Constitutive and heat-inducible heat shock element binding activities of heat shock factor in a group of filamentous fungi. Cell. Stress Chaperones 4:211-222