Protein disulfide isomerase-2 of arabidopsis mediates protein folding and localizes to both the secretory pathway and nucleus, where it interacts with maternal effect embryo arrest factor

Molecules and Cells

Volumn 32, Issue 5, 2011, Pages 459-475

  Cho, Eun Ju ^a   Yuen, Christen Y L ^a   Kang, Byung Ho ^b   Ondzighi, Christine A ^c   Staehelin, L Andrew ^c   Christopher, David A ^a  

^a UNIVERSITY OF HAWAII AT MANOA   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

Chaperone; Endoplasmic reticulum; Nuclear factor; Plant disulfide isomerase; Protein folding

Indexed keywords

ALKALINE PHOSPHATASE; CHAPERONE; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PROTEIN DISULFIDE ISOMERASE; PROTEIN DISULFIDE ISOMERASE 2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MEE8; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CELL LABELING; CELL NUCLEUS; CELL VACUOLE; CELL WALL; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ESCHERICHIA COLI; GOLGI COMPLEX; IMMUNOELECTRON MICROSCOPY; MESOPHYLL CELL; MICROSOME; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT ROOT; PLANT SEED; PLANT TISSUE; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTOPLAST; SECRETORY PATHWAY; SEED DEVELOPMENT;

AMINO ACID SEQUENCE; ARABIDOPSIS; CELL NUCLEUS; ENDOPLASMIC RETICULUM; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; PLANT PROTEINS; PROTEIN DISULFIDE-ISOMERASES; PROTEIN FOLDING; SECRETORY PATHWAY; SEEDS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EUKARYOTA;

EID: 84855691883     PISSN: 10168478     EISSN: 02191032     Source Type: Journal    
DOI: 10.1007/s10059-011-0150-3     Document Type: Article

References (88)

1. Adikesavan, A., Karani, U., Emmanual, J., and Anil, K. (2008). Overlapping signal sequences control nuclear localization and endoplasmic reticulum retention of GRP58. Biochem. Biophys. Res. Commun. 377, 407-412.
2. Amaya, Y., Nakai, T., Komaru, K., Tsuneki, M., and Miura, S. (2008). Cleavage of the ER-targeting signal sequence of parathyroid hormone-related protein is cell-type-specific and regulated in cis by its nuclear localization signal. J. Biochem. 143, 569-579. (Pubitemid 351451772)
3. Armstrong, D.J., and Roman, A. (1993). The anomalous electrophoretic behavior of the human papillomavirus type 16 E7 protein is due to the high content of acidic amino acid residues. Biochem. Biophys. Res. Commun. 192, 1380-1387. (Pubitemid 23218565)
4. Asally, M., and Yoneda, Y. (2005). Beta-catenin can act as a nuclear import receptor for its partner transcription factor, lymphocyte enhancer factor-1 (lef-1). Exp. Cell. Res. 308, 357-363.
5. Aslund, F., and Beckwith, J. (1999). Bridge over troubled waters: Sensing stress by disulfide bond formation. Cell 96, 751-753. (Pubitemid 29165077)
6. Battey, N.H., James, N.C., Greenland, A.J., and Brownlee, C. (1999). Exocytosis and Endocytosis. Plant Cell 11, 643-659.
7. Bendtsen, J.D., Nielsen, H., von Heijne, G., and Brunak, S. (2004). Improved prediction of signal peptides: SignalP 30. J. Mol. Biol. 340, 783-795. (Pubitemid 38829638)
8. Bertolotti, A., Zhang, Y., Hendershot, L.M., Harding, H.P., and Ron, D. (2000). Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat. Cell. Biol. 2, 326-332.
9. Bleckmann, A., Weidtkamp-Peters, S., Seidel, C.A., and Simon, R. (2010). Stem cell signaling in Arabidopsis requires CRN to localize CLV2 to the plasma membrane. Plant Physiol. 152, 166-176.
10. Cheug, P.Y., and Churchich, J.E. (1999). Recognition of protein substrates by protein-disulfide isomerase A sequence of the b' domain responds to substrate binding. J. Biol. Chem. 274, 32757-61. (Pubitemid 129535307)
11. Christopher, D.A., Borsics, T., Yuen, C.Y., Ullmer, W., Andème-Ondzighi, C., Andres, M.A., Kang, B.H., and Staehelin, L.A. (2007). The cyclic nucleotide gated cation channel AtCNGC10 traffics from the ER via Golgi vesicles to the plasma membrane of Arabidopsis root and leaf cells. BMC Plant Biol. 7, 1471-2229.
12. Chun, L., Kawakami, A., and Christopher, D.A. (2001). Phytochrome A mediates blue light and UV-A dependent chloroplast gene transcription in green leaves. Plant Physiol. 125, 1957-1966. (Pubitemid 32375778)
13. Clive, D.R., and Greene, J.J. (1996). Cooperation of protein disulfide isomerase and redox environment in the regulation of NF-?B and AP1 binding to DNA. Cell Biochem. Funct. 14, 49-55.
14. Clough, S., and Bent, A. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
15. Cokol, M., Nair, R., and Rost, B. (2000). Finding nuclear localisation signals. EMBO Rep. 1, 411-415.
16. Couet, J., De Bernard, S., Loosfelt, H., Saunier, B., Milgrom, E., and Misrahi, M. (1996). Cell surface protein disulfide-isomerase is involved in the shedding of human thyrotropin receptor ectodomain. Biochemistry 35, 14800-14805. (Pubitemid 26423813)
17. Cramer, J.H., Lea, K., Schaber, M.D., and Kramer, R.A. (1987). Signal peptide specificity in post-translational processing of the plant protein phaseolin in Saccharomyces cerevisiae. Mol. Cell. Biol. 7, 121-128. (Pubitemid 17230391)
18. Durfee, T., Becherer, K., Chen, P.L., Yeh, S.H., Yang, Y., Kilburn, A.E., Lee, W.H., and Elledge, S.J. (1993). The retinoblastoma protein associates with the protein phosphatase type 1 catalytic subunit. Genes Dev. 7, 555-569. (Pubitemid 23125257)
19. Favaloro, V., Spasic, M., Schwappach, B., and Dobberstein, B. (2008). Distinct targeting pathways for the membrane insertion of tail-anchored (TA). proteins. J. Cell Sci. 121, 1832-1840. (Pubitemid 351943376)
20. Ferrari, D.M., and Soling, H.D. (1999). The protein disulphide-isomerase family: Unraveling a string of folds. Biochem. J. 339, 1-10. (Pubitemid 29179283)
21. Fields, S., and Song, O. (1989). A novel genetic system to detect protein-protein interactions. Nature 20, 245-246. (Pubitemid 19171591)
22. Finn, R.D., Mistry, J., Schuster-Böckler, B., Griffiths-Jones, S., Hollich, V., Lassmann, T., Moxou, S., Marshall, M., Khanna, A., Durbin, R., et al. (2006). Pfam: Clans, web tools and services. Nucleic Acids Res. 34, D247-D251.
23. Frand, A.R., and Kaiser, C.A. (1998). The ERO1 gene of yeast is required for oxidation of protein dithiols in the endoplasmic reticulum. Mol. Cell 1, 161-170. (Pubitemid 128378657)
24. Furumizu, C., Tsukaya, H., and Komeda, Y. (2010). Characterization of EMU, the Arabidopsis homolog of the yeast THO complex member HPR1. RNA 16, 1809-1817.
25. Gruber, C.W., Cemazar, M., Heras, B., Martin, J.L., and Craik, D.J. (2006). Protein disulfide isomerase: The structure of oxidative folding. Trends Biochem. Sci. 31, 455-464. (Pubitemid 44108657)
26. Gruber, C.W., Cemazar, M., Clark, R.J.T., Renda, R.F., Anderson, M.A., and Craik, D.J. (2007). A novel plant protein-disulfide isomerase involved in the oxidative folding of cystine knot defense proteins. J. Biol. Chem. 282, 20435-20446. (Pubitemid 47099996)
27. Haseloff, J., Siemering, K.R., Prasher, D.C., and Hodge, S. (1997). Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc. Natl. Acad. Sci. USA 94, 2122-2127. (Pubitemid 27136838)
28. Helm, M., Schmid, M., Hierl, G., Terneus, K., Tan, L., Lottspeich, F., Kieliszewski, M.J., and Gietl, C. (2008). KDEL-tailed cysteine endopeptidases involved in programmed cell death, intercalation of new cells, and dismantling of extensin scaffolds. Am. J. Bot. 95, 1049-1062.
29. Higuchi, T., Watanabe, Y., and Waga, I. (2004). Protein disulfide isomerase suppresses the transcriptional activity of NF-kB. Bio chem. Biophys. Res. Commun. 318, 46-52. (Pubitemid 38526243)
30. Holst, B., Tachibana, C., and Winther, J.R. (1997). Active site mutations in yeast protein disulfide isomerase cause dithiothreitol densitivity and a reduced rate of protein folding in the endoplasmic reticulum. J. Cell. Biol. 138, 1229-1238. (Pubitemid 27415050)
31. Honscha, W., Ottallah, M., Kistner, A., Platte, H., and Petzinger, E. (1993). A membrane-bound form of protein disulfide isomerase (PDI). and the hepatic uptake of organic anions. Biochim. Biophys. Acta 1153, 175-183. (Pubitemid 24028286)
32. Houston, N.L., Fan, C., Xiang, J.Q., Schulze, J.M., Jung, R., and Boston, R.S. (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. (Pubitemid 43126704)
33. Jackson, R.C., and Blobel, G. (1977). Post-translational cleavage of presecretory proteins with an extract of rough microsomes from dog pancreas containing signal peptidase activity. Proc. Natl. Acad. Sci. USA 74, 5598-5602.
34. James, P., Halladay, J., and Craig, E.A. (1996). Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144, 1425-1436.
35. Jauvion, V., Elmayan, T., and Vaucheret, H. (2010). The conserved RNA trafficking proteins HPR1 and TEX1 are involved in the production of endogenous and exogenous small interfering RNA in Arabidopsis. Plant Cell 22, 2697-2709.
36. John, D.C., and Bulleid, N.J. (1994). Prolyl 4-hydroxylase: Defective assembly of alpha-subunit mutants indicates that assembled alpha-subunits are intramolecularly disulfide bonded. Biochemistry 33, 14018-14025.
37. Jones, A.M., and Herman, E.M. (1993). A K-D-E-L-containing auxinbinding protein is located at the plasma membrane and within the cell wall. Plant Physiol. 101, 595-606.
38. Kanai, S., Toh, H., Hayano, T., and Kikuchi, M. (1998). Molecular evolution of the domain structures of protein disulfide isomerases. J. Mol. Evol. 47, 200-210. (Pubitemid 28373211)
39. Karniely, S., and Pines, O. (2005). Single translation-dual destination: Mechanisms of dual protein targeting in eukaryotes. EMBO Rep. 6, 420-425. (Pubitemid 40767074)
40. Kerk, D., Bulgrien, J., Smith, D.W., and Gribskov, M. (2003). Arabidopsis proteins containing similarity to the universal stress protein domain of bacteria. Plant Physiol. 131, 1209-1219. (Pubitemid 36400353)
41. Kim, J.M., and Mayfield, S.P. (1997). Protein disulfide isomerase as a regulator of chloroplast translational activation. Science 278, 1954-1957. (Pubitemid 28013238)
42. Kong, Z., Li, M., Yang, W., Xu, W., and Xue, Y. (2006). A novel nuclear-localized CCCH-type zinc finger protein, OsDOS, is involved in delaying leaf senescence in rice. Plant Physiol. 141, 1376-1388. (Pubitemid 44223289)
43. Lahav, J., Gofer-Dadosh, N., Luboshitz, J., Hess, O., and Shaklai, M. (2000). Protein disulfide isomerase mediates integrindependent adhesion. FEBS Lett. 475, 89-92. (Pubitemid 30365056)
44. Lamberg, A., Jauhiainen, M., Metso, J., Ehnholm, C., Shoulders, C., Scott, J., Pihlajaniemi, T., and Kivirikko, K.I. (1996). The role of protein disulphide isomerase in the microsomal triacylglycerol transfer protein does not reside in its isomerase activity. Biochem. J. 315, 533-536. (Pubitemid 26129503)
45. Lange, A., Mills, R.E., Lange, C.J., Stewart, M., Devine, S.E., and Corbett, A.H. (2007). Classical nuclear localization signals: Definition, function, and interaction with importin alpha. J. Biol. Chem. 282, 5101-5105. (Pubitemid 47093710)
46. Lappi, A.K., Lensink, M.F., Alanen, H.I., Salo, K.E., Lobell, M., Juffer, A.H., and Ruddock, L.W. (2004). A conserved arginine plays a role in the catalytic cycle of the protein disulphide isomerases. J. Mol. Biol. 335, 283-295. (Pubitemid 37494979)
47. Lee, S.-O., Cho, K., Cho, S., Kim, I., Oh, C., and Ahn, K. (2010). Protein disulphide isomerase is required for signal peptide peptidase-mediated protein degradation. EMBO J. 29, 363-375.
48. Levitan, A., Trebitsh, T., Kiss, V., Pereg, Y., Dangoor, I., and Danon, A. (2005). Dual targeting of the protein disulfide isomerase RB60 to the chloroplast and the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 102, 6225-6230. (Pubitemid 40594282)
49. Li, C.P., and Larkins, B.A. (1996). Expression of protein disulfide isomerase is elevated in the endosperm of the maize floury 2 mutant. Plant Mol. Biol. 30, 873-882. (Pubitemid 126834382)
50. Lu, D.-P., and Christopher, D.A. (2006). Immunolocalization of a protein disulfide isomerase to Arabidopsis thaliana chloroplasts and its association with starch biogenesis. Int. J. Plant Sci. 167, 1-9. (Pubitemid 43052320)
51. Lu, D.-P., and Christopher, D.A. (2008). Endoplasmic reticulum stress activates the expression of a sub-group of protein disulfide isomerase genes and AtbZIP60 modulates the response in Arabidopsis thaliana. Mol. Genet. Genomics 280, 199-210.
52. Lucero, H.A., and Kaminer, B. (1999). The role of calcium on the activity of ER calcistorin/Protein-disulfide Isomerase and the significance of the C-terminal and itscalcium binding A comparison with mammalian protein-disulfide isomerase. J. Biol. Chem. 274, 3243-3251. (Pubitemid 29075415)
53. Lumb, R.A., and Bulleid, N.J. (2002). Is protein disulfide isomerase a redox-dependent molecular chaperone? EMBO J. 21, 6763-6770. (Pubitemid 36014548)
54. Markus, M., and Benezra, R. (1999). Two isoforms of protein disulfide isomerase alter the dimerization status of E2A proteins by a redox mechanism. J. Biol. Chem. 274, 1040-1049. (Pubitemid 29058078)
55. Maruyama, D., Endo, T., and Nishikawa, S. (2010). BiP-mediated polar nuclei fusion is essential for the regulation of endosperm nuclei proliferation in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 107, 1684-1689.
56. Mayer, M., Kies, U., Kammermeier, R., and Buchner, J. (2000). BiP and PDI cooperate in the oxidative folding of antibodies in vitro. J. Biol. Chem. 275, 29421-29425. (Pubitemid 32043816)
57. Motohashi, K., Kondoh, A., Stumpp, M.T., and Hisabori, T. (2001). Comprehensive survey of proteins targeted by chloroplast thioredoxin. Proc. Natl. Acad. Sci. USA 98, 11224-11229. (Pubitemid 32928710)
58. Nelson, B.K., Cai, X., and Nebenführ, A. (2007). A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51, 1126-1136. (Pubitemid 47373577)
59. Neuteboom, L.W., Matsumoto, K.O., and Christopher, D.A. (2009). An extended AE-rich N-terminal trunk in secreted pineapple cystatin enhances inhibition of fruit bromelain and is post-translationally removed during ripening. Plant Physiol. 151, 515-527.
60. Ohtani, H., Wakui, H., Ishino, T., Komatsuda, A., and Miura, A.B. (1993). An isoform of protein disulfide isomerase is expressed in the developing acrosome of spermatids during rat spermiogenesis and is transported into the nucleus of mature spermatids and epididymal spermatozoa. Histochemistry 100, 423-429. (Pubitemid 24049311)
61. Okita, T.W., and Rogers, J.C. (1996). Compartmentation of proteins in the endomembrane system of plant cells. Annu. Rev. Plant. Physiol. Plant Mol. Biol. 47, 327-350.
62. Onda, Y., Nagamine, A., Sakurai, M., Kumamaru, T., Ogawa, M., and Kawagoe, Y. (2011). Distinct roles of protein disulfide isomerase and p5 sulfhydryl oxidoreductases in multiple pathways for oxidation of structurally diverse storage proteins in rice. Plant Cell 23, 210-223.
63. Ondzighi, C.A., Christopher, D.A., Cho, E.J., Chang, S.C., and Staehelin, L.A. (2008). Arabidopsis protein disulfide isomerase-5 inhibits cysteine proteases during trafficking to vacuoles before programmed cell death of the endothelium in developing seeds. Plant Cell 20, 2205-2220. (Pubitemid 352844520)
64. Ostermeier, M., De Sutter, K., and Georgiou, G. (1996). Eukaryotic protein disulfide isomerase complements E. coli dsbA mutants and increases the yield of heterologous secreted protein with disulfide bonds. J. Biol. Chem. 271, 10616-10622. (Pubitemid 26145795)
65. Pagnussat, G.C., Yu, H.J., Ngo, Q.A., Rajani, S., Mayalagu, S., Johnson, C.S., Capron, A., Xie, L.F., Ye, D., and Sundaresan, V. (2005). Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis. Development 132, 603-614. (Pubitemid 40277699)
66. Plath, K., Mothes, W., Wilkinson, B.M., Stirling, C.J., and Rapoport, T.A. (1998). Signal sequence recognition in posttranslational protein transport across the yeast ER membrane. Cell 94, 795-807. (Pubitemid 28436011)
67. Pomeranz, M.C., Hah, C., Lin, P.-C., Kang, S.G., Finer, J.J., Blackshear, P.J., and Jang, J.C. (2010). The Arabidopsis tandem zinc finger protein AtTZF1 traffics between the nucleus and cytoplasmic foci and binds both DNA and RNA. Plant Physiol. 152, 151-165.
68. Powers, T., and Walter, P. (1996). The nascent polypeptide-associated complex modulates interactions between the signal recognition particle and the ribosome. Curr. Biol. 6, 331-338.
69. Rapoport, T.A., Matlack, K.E., Plath, K., Misselwitz, B., and Staeck, O. (1999). Posttranslational protein translocation across the membrane of the endoplasmic reticulum. Biol. Chem. 380, 1143-1150. (Pubitemid 29516402)
70. Rigobello, M.P., Donella-Deana, A., Cesaro, L., and Bindoli, A. (2001). Distribution of protein disulphide isomerase in rat liver mitochondria. Biochem. J. 356, 567-570. (Pubitemid 32536819)
71. Rosenthal, J.A., Chen, H., Slepnev, V.I., Pellegrini, L., Salcini, A.E., Di Fiore, P.P., and De Camilli, P. (1999). The epsins define a family of proteins that interact with components of the clathrin coat and contain a new protein module. J. Biol. Chem. 274, 33959-33965. (Pubitemid 129511724)
72. Rout, M.P., Aitchison, J.D., Magnasco, M.O., and Chait, B.T. (2003). Virtual gating and nuclear transport: The hole picture. Trends Cell Biol. 13, 622-628. (Pubitemid 37415027)
73. Shimada, H., Mochizuki, M., Ogura, K., Froehlich, J.E., Osteryoung, K.W., Shirano, Y., Shibata, D., Masuda, S., Mori, K., and Takamiya, K. (2007). Arabidopsis cotyledon-specific chloroplast biogenesis factor CYO1 is a protein disulfide isomerase. Plant Cell 19, 3157-3169. (Pubitemid 350276718)
74. Shimoni, Y., Zhu, X.Z., Levanony, H., Segal, G., and Galili, G. (1995). Purification characterization and intracellular localization of glycosylated protein disulfide isomerase from wheat grains. Plant Physiol. 108, 327-335.
75. Sone, M., Kishigami, S., Yoshihisa, T., and Ito, K. (1997). Roles of disulfide bonds in bacterial alkaline phosphatase. J. Biol. Chem. 272, 6174-6178. (Pubitemid 27118085)
76. Stockton, J.D., Merkert, M.C., and Kellaris, K.V. (2003). A complex of chaperones and disulfide isomerases occludes the cytosolic face of the translocation protein Sec61p and affects translocation of the prion protein. Biochemistry 42, 12821-12834. (Pubitemid 37385813)
77. Swanson, R., Locher, M., and Hochstrasser, M. (2001). A conserved ubiquitin ligase of the nuclear envelope/endoplasmic reticulum that functions in both ER-associated and matalpha2 repressor degradation. Genes Dev. 15, 2660-2674. (Pubitemid 32988877)
78. Takemoto, Y., Coughlan, S.J., Okita, T.W., Satoh, H., Ogawa, M., and Kumamaru, T. (2002). The rice mutant esp2 greatly accumulates the glutelin precursor and deletes the protein disulfide isomerase. Plant Physiol. 128, 1212-1222. (Pubitemid 34305775)
79. Tamura, K., Yamada, K., Shimada, T., and Hara-Nishimura, I. (2004). Endoplasmic reticulum-resident proteins are constitutively transported to vacuoles for degradation. Plant J. 39, 393-402. (Pubitemid 39040144)
80. Tu, B., Ho-Schleyer, S.C., Travers, K.J., and Weissman, K.J. (2000). Biochemical basis of oxidative protein folding in the endoplasmic reticulum. Science 290, 1571-1574.
81. Turano, C., Coppari, S., Altieri, F., and Ferraro, A. (2002). Proteins of the PDI family: Unpredicted non-ER locations and functions. J. Cell. Physiol. 193, 154-163.
82. Wang, H., Boavida, L.C., Ron, M., and McCormick, S. (2008). Truncation of a protein disulfide isomerase, PDIL2-1, delays embryo sac maturation and disrupts pollen tube guidance in Arabidopsis thaliana. Plant Cell 20, 3300-3311.
83. Wilson, R., Lees, J.F., and Bulleid, N.J. (1998). Protein disulfide isomerase acts as a molecular chaperone during the assembly of procollagen. J. Biol. Chem. 273, 9637-9643. (Pubitemid 28183052)
84. Wu, F.H., Shen, S.C., Lee, L.Y., Lee, S.H., Chan, M.T., and Lin, C. -S. (2009). Tape-Arabidopsis sandwich -a simpler Arabidopsis protoplast isolation method. Plant Methods 5, 1-10.
85. Xu, P., Radena, D., Doyle, III F.J., and Robinson, A.S. (2005). Analysis of unfolded protein response during single-chain antibody expression in Saccaromyces cerevisiae reveals different roles for BiP and PDI in folding. Metab. Eng. 7, 269-279. (Pubitemid 41225444)
86. Yoo, S.D., Cho, Y.H., and Sheen, J. (2007). Arabidopsis mesophyll protoplasts: A versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565-1572. (Pubitemid 47028844)
87. Yoshimori, T., Semba, T., Takemoto, H., Akagi, S., Yamamoto, A., and Tashiro, Y. (1990). Protein disulfide-isomerase in rat exocrine pancreatic cells is exported from the endoplasmic reticulum despite possessing the retention signal. J. Biol. Chem. 265, 15984-15990.
88. Zaltsman, A., Yi, B.Y., Gafni, Y., and Citovsky, V. (2007). Yeastplant coupled vector system for identification of nuclear proteins. Plant Physiol. 145, 1264-1271. (Pubitemid 350276745)