A novel plant protein disulfide isomerase family homologous to animal P5 - Molecular cloning and characterization as a functional protein for folding of soybean seed-storage proteins

FEBS Journal

Volumn 275, Issue 3, 2008, Pages 399-410

  Wadahama, Hiroyuki ^a   Kamauchi, Shinya ^a,c   Nakamoto, Yumi ^b   Nishizawa, Keito ^b   Ishimoto, Masao ^b   Kawada, Teruo ^a   Urade, Reiko ^a  

^a KYOTO UNIVERSITY   (Japan)

^b NATIONAL AGRICULTURAL RESEARCH CENTER FOR HOKKAIDO REGION   (Japan)

^c OSAKA BIOSCIENCE INSTITUTE   (Japan)

Author keywords

Endoplasmic reticulum; Protein disulfide isomerase; Soybean; Storage protein; Unfolded protein response

Indexed keywords

BETA CONGLYCININ; COMPLEMENTARY DNA; DISULFIDE; GLYCININ; ISOMERASE; MESSENGER RNA; PROTEIN GMPDIM; PROTEINASE K; RIBONUCLEASE A; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

AMINO ACID COMPOSITION; AMINO ACID SEQUENCE; ARTICLE; CELLULAR DISTRIBUTION; DISULFIDE BOND; DNA ISOLATION; GENE SEQUENCE; IMMUNOPRECIPITATION; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SOYBEAN;

ANIMALS; BLOTTING, WESTERN; CLONING, MOLECULAR; COTYLEDON; DNA, COMPLEMENTARY; DNA, PLANT; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GLOBULINS; IMMUNOPRECIPITATION; MOLECULAR SEQUENCE DATA; PLANT LEAVES; PROTEIN BINDING; PROTEIN DISULFIDE-ISOMERASE; PROTEIN FOLDING; RECOMBINANT PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEEDS; SEQUENCE ANALYSIS, DNA; SOYBEAN PROTEINS; SOYBEANS;

ANIMALIA; ARABIDOPSIS THALIANA; ESCHERICHIA COLI; GLYCINE MAX; ORYZA SATIVA;

EID: 38149054229     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2007.06199.x     Document Type: Article

References (41)

1. Helenius A Aeb M (2004) Roles of N-linked glycans in the endoplasmic reticulum. Annu Rev Biochem 73, 1019 1049.
2. Freedman RB, Hirst TR Tuite MF (1994) Protein disulphide isomerase: building bridges in protein folding. Trends Biochem Sci 19, 331 336.
3. Creighton TE, Zapun A Darby NJ (1995) Mechanisms and catalysts of disulfide bond formation in proteins. Trends Biotechnol 13, 18 23.
4. Gilbert HF (1998) Protein disulfide isomerase. Methods Enzymol 290, 26 50.
5. Ellgaard L Ruddock LW (2005) The human protein disulphide isomerase family: substrate interactions and functional properties. EMBO Rep 6, 28 32.
6. Chaudhuri MM, Tonin PN, Lewis WH Srinivasan PR (1992) The gene for a novel protein, a member of the protein disulphide isomerase/form I phosphoinositide-specific phospholipase C family, is amplified in hydroxyurea-resistant cells. Biochem J 281, 645 650.
7. Kikuchi M, Doi E, Tsujimoto I, Horibe T Tsujimoto Y (2002) Functional analysis of human P5, a protein disulfide isomerase homologue. J Biochem 132, 451 455.
8. Kimura T, Nishida A, Ohara N, Yamagishi D, Horibe T Kikuchi M (2004) Functional analysis of the CXXC motif using phage antibodies that cross-react with protein disulphide-isomerase family proteins. Biochem J 382, 169 176.
9. Hoshijima K, Metherall JE Grunwald DJ (2002) A protein disulfide isomerase expressed in the embryonic midline is required for left/right asymmetries. Genes Dev 16, 2518 2529.
10. Kaiser BK, Yim D, Chow IT, Gonzalez S, Dai Z, Mann HH, Strong RK, Groh V Spies T (2007) Disulphide-isomerase-enabled shedding of tumour-associated NKG2D ligands. Nature 447, 482 486.
11. Houston NL, Fan C, Xiang QY, Schulze JM, Jung R Boston RS (2005) Phylogenetic analyses identify 10 classes of the protein disulfide isomerase family in plants, including single-domain protein disulfide isomerase-related proteins. Plant Physiol 137, 762 778.
12. Goldberg RB, Barker SJ Perez-Grau L (1989) Regulation of gene expression during plant embryogenesis. Cell 56, 149 160.
13. Müntz K (1998) Deposition of storage proteins. Plant Mol Biol 38, 77 99.
14. Ereken-Tumer N, Richter JD Nielsen NC (1982) Structural characterization of the glycinin precursors. J Biol Chem 257, 4016 4018.
15. Tumer NE, Thanh VH Nielsen NC (1981) Purification and characterization of mRNA from soybean seeds. Identification of glycinin and beta-conglycinin precursors. J Biol Chem 256, 8756 8760.
16. Dickinson CD, Hussein EH Nielsen NC (1989) Role of posttranslational cleavage in glycinin assembly. Plant Cell 1, 459 469.
17. Jung R, Nam YW, Saalbach I, Müntz K Nielsen NC (1997) Role of the sulfhydryl redox state and disulfide bonds in processing and assembly of 11S seed globulins. Plant Cell 9, 2037 2050.
18. Utsumi S, Gidamis AB, Mikami B Kito M (1993) Crystallization and preliminary X-ray crystallographic analysis of the soybean proglycinin expressed in Escherichia coli. J Mol Biol 233, 177 178.
19. Adachi M, Okuda E, Kaneda Y, Hashimoto A, Shutov AD, Becker C, Müntz K Utsumi S (2003) Crystal structures and structural stabilities of the disulfide bond-deficient soybean proglycinin mutants C12G and C88S. J Agric Food Chem 51, 4633 4639.
20. Wadahama H, Kamauchi S, Ishimoto M, Kawada T Urade R (2007) Protein disulfide isomerase family proteins involved in soybean protein biogenesis. FEBS J 274, 687 703.
21. Munro S Pelham HR (1986) An Hsp70-like protein in the ER: identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein. Cell 46, 291 300.
22. Munro S Pelham HR (1987) A C-terminal signal prevents secretion of luminal ER proteins. Cell 48, 899 907.
23. Lappi AK, Lensink MF, Alanen HI, Salo KE, Lobell M, Juffer AH Ruddock LW (2004) A conserved arginine plays a role in the catalytic cycle of the protein disulphide isomerases. J Mol Biol 335, 283 295.
24. Simpson CG, Clark G, Davidson D, Smith P Brown JW (1996) Mutation of putative branchpoint consensus sequences in plant introns reduces splicing efficiency. Plant J 9, 369 380.
25. Yoshida H, Haze K, Yanagi H, Yura T Mori K (1998) 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, 33741 33749.
26. Martìnez IM Chrispeels MJ (2003) Genomic analysis of the unfolded protein response in Arabidopsis shows its connection to important cellular processes. Plant Cell 15, 561 576.
27. Kamauchi S, Nakatani H, Nakano C Urade R (2005) Gene expression in response to endoplasmic reticulum stress in Arabidopsis thaliana. FEBS J 272, 3461 3476.
28. Buzeli RA, Cascardo JC, Rodrigues LA, Andrade MO, Almeida RS, Loureiro ME, Otoni WC Fontes EP (2000) Tissue-specific regulation of BiP genes: a cis- acting regulatory domain is required for BiP promoter activity in plant meristems. Plant Mol Biol 50, 757 771.
29. Urade R (2007) Cellular response to unfolded proteins in the endoplasmic reticulum of plants. FEBS J 274, 1152 1171.
30. Puig A Gilbert HF (1994) Protein disulfide isomerase exhibits chaperone and anti-chaperone activity in the oxidative refolding of lysozyme. J Biol Chem 269, 7764 7771.
31. Iwata K Koizumi N (2005) An Arabidopsis transcription factor, AtbZIP60, regulates the endoplasmic reticulum stress response in a manner unique to plants. Proc Natl Acad Sci USA 102, 5280 5285.
32. Yoshino M, Nagamatsu A, Tsutsumi K Kanazawa A (2006) The regulatory function of the upstream sequence of the beta-conglycinin alpha subunit gene in seed-specific transcription is associated with the presence of the RY sequence. Genes Genet Syst 81, 135 141.
33. Beachy RN, Jarvis NP Barton KA (1981) Biosynthesis of subunits of the soybean 7S storage protein. J Mol Appl Genet 1, 19 27.
34. Coates JB, Medeiros JS, Thanh VH Nielsen NC (1985) Characterization of the subunits of beta-conglycinin. Arch Biochem Biophys 243, 184 194.
35. Liu YG, Shirano Y, Fukaki H, Yanai Y, Tasaka M, Tabata S Shibata D (1999) Complementation of plant mutants with large genomic DNA fragments by a transformation-competent artificial chromosome vector accelerates positional cloning. Proc Natl Acad Sci USA 96, 6535 6540.
36. Harada K Xia Z (2004) Soybean genomics: efforts to reveal the complex genome. Breed Sci 54, 215 224.
37. Pace CN, Vajdos F, Fee L, Grimsley G Gray T (1995) How to measure and predict the molar absorption coefficient of a protein. Protein Sci 4, 2411 2423.
38. Creighton TE (1977) Kinetics of refolding of reduced ribonuclease. J Mol Biol 113, 329 341.
39. Lyles MM Gilbert HF (1991) Catalysis of the oxidative folding of ribonuclease A by protein disulfide isomerase: dependence of the rate on the composition of the redox buffer. Biochemistry 30, 613 619.
40. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680 685.
41. Samoylov VM, Tucker DM Parrott WA (1998) Soybean [Glycine Max (L.) Merrill] embryogenic cultures: the role of sucrose and total nitrogen content on proliferation. In Vitro Cell Dev Biol Plant 34, 8 13.