HACA, the transcriptional activator of the unfolded protein response (UPR) in Aspergillus niger, binds to partly palindromic UPR elements of the consensus sequence 5′-CAN(G/A)NTGT/GCCT-3′

Fungal Genetics and Biology

Volumn 43, Issue 8, 2006, Pages 560-572

  Mulder, Harm J ^a   Nikolaev, Igor ^a   Madrid, Susan M ^a  

^a DANISCO A S   (Denmark)

Author keywords

Aspergillus niger; bZIP; DNA binding; ER stress; hacA; UPR; UPRE

Indexed keywords

CIS ACTING ELEMENT; DNA BASE; FUNGAL PROTEIN; NUCLEOTIDE; PALINDROMIC DNA; SPACER DNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HACA; UNCLASSIFIED DRUG;

ARTICLE; ASPERGILLUS NIDULANS; BINDING SITE; CONSENSUS SEQUENCE; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; ENDOPLASMIC RETICULUM; GENE IDENTIFICATION; GENE LOCATION; GENETIC SELECTION; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN FOLDING; STRESS; TRANSCRIPTION INITIATION; TRANSCRIPTION INITIATION SITE; UNFOLDED PROTEIN RESPONSE ELEMENT;

ASPERGILLUS NIGER; BASE SEQUENCE; BINDING SITES; CONSENSUS SEQUENCE; DIMERIZATION; DNA MUTATIONAL ANALYSIS; DNA, FUNGAL; DNA-BINDING PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ENDOPLASMIC RETICULUM; FUNGAL PROTEINS; LEUCINE ZIPPERS; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS (GENETICS); RESPONSE ELEMENTS; TRANS-ACTIVATORS; TRANSCRIPTION INITIATION SITE;

ASPERGILLUS; ASPERGILLUS NIGER;

EID: 33745699785     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2006.02.005     Document Type: Article

References (56)

1. Bertolotti A., Zhang Y., Hendershot L.M., Harding H.P., and Ron D. Dynamic interaction of BiP and ER stress transducers in the unfolded- protein response. Nat. Cell Biol. 2 (2000) 326-332
2. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
3. Calfon M., Zeng H., Urano F., Till J.H., Hubbard S.R., Harding H.P., Clark S.G., and Ron D. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415 (2002) 92-96
4. Chapman R.E., and Walter P. Translational attenuation mediated by an mRNA intron. Curr. Biol. 7 (1997) 850-859
5. Conesa A., Punt P.J., van Luijk N., and van den Hondel C.A. The secretion pathway in filamentous fungi: a biotechnological view. Fungal Genet. Biol. 33 (2001) 155-171
6. Cox J.S., Shamu C.E., and Walter P. Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 73 (1993) 1197-1206
7. Cox J.S., and Walter P. A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 87 (1996) 391-404
8. Derkx P.M., and Madrid S.M. The foldase CYPB is a component of the secretory pathway of Aspergillus niger and contains the endoplasmic reticulum retention signal HEEL. Mol. Genet. Genomics 266 (2001) 537-545
9. Ellgaard L., and Helenius A. ER quality control: towards an understanding at the molecular level. Curr. Opin. Cell Biol. 13 (2001) 431-437
10. Foulds G.J., and Etzkorn F.A. A capillary electrophoresis mobility shift assay for protein-DNA binding affinities free in solution. Nucleic Acids Res. 26 (1998) 4304-4305
11. Gething M.J., and Sambrook J. Protein folding in the cell. Nature 355 (1992) 33-45
12. Gonzalez T.N., Sidrauski C., Dorfler S., and Walter P. Mechanism of non-spliceosomal mRNA splicing in the unfolded protein response pathway. EMBO J. 18 (1999) 3119-3132
13. Goodbourn S. Eukaryotic Gene Transcription (1996), Oxford University Press, Oxford
14. Gouka R.J., Punt P.J., and van den Hondel C.A. Efficient production of secreted proteins by Aspergillus: progress, limitations and prospects. Appl. Microbiol. Biotechnol. 47 (1997) 1-11
15. Helenius A., Marquardt T., and Braakman I. The endoplasmic reticulum as a protein-folding compartment. Trends Cell Biol. 2 (1992) 227-231
16. Jeenes D.J., Pfaller R., and Archer D.B. Isolation and characterisation of a novel stress-inducible PDI-family gene from Aspergillus niger. Gene 193 (1997) 151-156
17. Kaufman R.J. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev. 13 (1999) 1211-1233
18. Kawahara T., Yanagi H., Yura T., and Mori K. Endoplasmic reticulum stress-induced mRNA splicing permits synthesis of transcription factor Hac1p/Ern4p that activates the unfolded protein response. Mol. Biol. Cell 8 (1997) 1845-1862
19. Kawahara T., Yanagi H., Yura T., and Mori K. Unconventional splicing of HAC1/ERN4 mRNA required for the unfolded protein response. Sequence-specific and non-sequential cleavage of the splice sites. J. Biol. Chem. 273 (1998) 1802-1807
20. Kokame K., Kato H., and Miyata T. Identification of ERSE-II, a new cis-acting element responsible for the ATF6-dependent mammalian unfolded protein response. J. Biol. Chem. 276 (2001) 9199-9205
21. Kusters-van Someren M.A., Harmsen J.A., Kester H.C., and Visser J. Structure of the Aspergillus niger pelA gene and its expression in Aspergillus niger and Aspergillus nidulans. Curr. Genet. 20 (1991) 293-299
22. Latchman D. Gene Regulation: A Eukaryotic Perspective (1995), Chapman & Hall, London
23. Martinez I.M., and Chrispeels M.J. Genomic analysis of the unfolded protein response in Arabidopsis shows its connection to important cellular processes. Plant Cell 15 (2003) 561-576
24. Mori K. Tripartite management of unfolded proteins in the endoplasmic reticulum. Cell 101 (2000) 451-454
25. Mori K., Kawahara T., Yoshida H., Yanagi H., and Yura T. Signalling from endoplasmic reticulum to nucleus: transcription factor with a basic-leucine zipper motif is required for the unfolded protein-response pathway. Genes Cells 1 (1996) 803-817
26. Mori K., Ma W., Gething M.J., and Sambrook J. A transmembrane protein with a cdc2+/CDC28-related kinase activity is required for signaling from the ER to the nucleus. Cell 74 (1993) 743-756
27. Mori K., Ogawa N., Kawahara T., Yanagi H., and Yura T. Palindrome with spacer of one nucleotide is characteristic of the cis- acting unfolded protein response element in Saccharomyces cerevisiae. J. Biol. Chem. 273 (1998) 9912-9920
28. Mori K., Sant A., Kohno K., Normington K., Gething M.J., and Sambrook J.F. A 22 bp cis-acting element is necessary and sufficient for the induction of the yeast KAR2 (BiP) gene by unfolded proteins. EMBO J. 11 (1992) 2583-2593
29. Mulder H.J., Saloheimo M., Penttila M., and Madrid S.M. The transcription factor HACA mediates the unfolded protein response in Aspergillus niger, and up-regulates its own transcription. Mol. Genet. Genomics 271 (2004) 130-140
30. Ngiam C., Jeenes D.J., and Archer D.B. Isolation and characterisation of a gene encoding protein disulphide isomerase, pdiA, from Aspergillus niger. Curr. Genet. 31 (1997) 133-138
31. Okamura K., Kimata Y., Higashio H., Tsuru A., and Kohno K. Dissociation of Kar2p/BiP from an ER sensory molecule, Ire1p, triggers the unfolded protein response in yeast. Biochem. Biophys. Res. Commun. 279 (2000) 445-450
32. Partaledis J.A., and Berlin V. The FKB2 gene of Saccharomyces cerevisiae, encoding the immunosuppressant-binding protein FKBP-13, is regulated in response to accumulation of unfolded proteins in the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 90 (1993) 5450-5454
33. Patil C.K., Li H., and Walter P. Gcn4p and novel upstream activating sequences regulate targets of the unfolded protein response. PLoS. Biol. 2 (2004) E246
34. Pierrou S., Enerback S., and Carlsson P. Selection of high-affinity binding sites for sequence-specific, DNA binding proteins from random sequence oligonucleotides. Anal. Biochem. 229 (1995) 99-105
35. Riggs A.D., Suzuki H., and Bourgeoss S. Lac repressor-operator interaction. I. Equilibrium studies. J. Mol. Biol. 48 (1970) 67-83
36. Roy B., and Lee A.S. The mammalian endoplasmic reticulum stress response element consists of an evolutionarily conserved tripartite structure and interacts with a novel stress-inducible complex. Nucleic Acids Res. 27 (1999) 1437-1443
37. Ruegsegger U., Leber J.H., and Walter P. Block of HAC1 mRNA translation by long-range base pairing is released by cytoplasmic splicing upon induction of the unfolded protein response. Cell 107 (2001) 103-114
38. Rutkowski D.T., and Kaufman R.J. A trip to the ER: coping with stress. Trends Cell Biol. 14 (2004) 20-28
39. Saloheimo M., Valkonen M., and Penttila M. Activation mechanisms of the HACI-mediated unfolded protein response in filamentous fungi. Mol. Microbiol. 47 (2003) 1149-1161
40. Sambrook J., Fritsch E.F., and Maniatis T. Molecular Cloning: A Laboratory Manual. second ed. (1989), Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
41. Schuler G.D., Altschul S.F., and Lipman D.J. A workbench for multiple alignment construction and analysis. Proteins 9 (1991) 180-190
42. Sidrauski C., Chapman R., and Walter P. The unfolded protein response: an intracellular signalling pathway with many surprising features. Trends Cell Biol. 8 (1998) 245-249
43. Sidrauski C., and Walter P. The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell 90 (1997) 1031-1039
44. Sims A.H., Gent M.E., Lanthaler K., Dunn-Coleman N.S., Oliver S.G., and Robson G.D. Transcriptome analysis of recombinant protein secretion by Aspergillus nidulans and the unfolded-protein response in vivo. Appl. Environ. Microbiol. 71 (2005) 2737-2747
45. Travers K.J., Patil C.K., Wodicka L., Lockhart D.J., Weissman J.S., and Walter P. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101 (2000) 249-258
46. Valkonen M., Penttila M., and Saloheimo M. Effects of inactivation and constitutive expression of the unfolded- protein response pathway on protein production in the yeast Saccharomyces cerevisiae. Appl. Environ. Microbiol. 69 (2003) 2065-2072
47. van Gemeren I.A., Punt P.J., Drint-Kuyvenhoven A., Broekhuijsen M.P., van't Hoog A., Beijersbergen A., Verrips C.T., and van den Hondel C.A. The ER chaperone encoding bipA gene of black Aspergilli is induced by heat shock and unfolded proteins. Gene 198 (1997) 43-52
48. van Hartingsveldt W., Mattern I.E., van Zeijl C.M., Pouwels P.H., and van den Hondel C.A. Development of a homologous transformation system for Aspergillus niger based on the pyrG gene. Mol. Gen. Genet. 206 (1987) 71-75
49. Vilela C., and McCarthy J.E. Regulation of fungal gene expression via short open reading frames in the mRNA 5′untranslated region. Mol. Microbiol. 49 (2003) 859-867
50. Vishniac W., and Santer M. The thiobacilli. Bacteriol. Rev. 21 (1957) 195-213
51. Wang H., and Ward M. Molecular characterization of a PDI-related gene prpA inAspergillus niger var. awamori. Curr. Genet. 37 (2000) 57-64
52. Wang Y., Shen J., Arenzana N., Tirasophon W., Kaufman R.J., and Prywes R. Activation of ATF6 and an ATF6 DNA binding site by the endoplasmic reticulum stress response. J. Biol. Chem. 275 (2000) 27013-27020
53. Wanke C., Eckert S., Albrecht G., van Hartingsveldt W., Punt P.J., van den Hondel C.A., and Braus G.H. The Aspergillus niger GCN4 homologue, cpcA, is transcriptionally regulated and encodes an unusual leucine zipper. Mol. Microbiol. 23 (1997) 23-33
54. Welihinda A.A., Tirasophon W., and Kaufman R.J. The cellular response to protein misfolding in the endoplasmic reticulum. Gene Expr. 7 (1999) 293-300
55. Yoshida H., Haze K., Yanagi H., Yura T., and Mori K. Identification of the cis-acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose- regulated proteins. Involvement of basic leucine zipper transcription factors. J. Biol. Chem. 273 (1998) 33741-33749
56. Zhang K., and Kaufman R.J. Signaling the unfolded protein response from the endoplasmic reticulum. J. Biol. Chem. 279 (2004) 25935-25938