Phylogenetic characterization and promoter expression analysis of a novel hybrid protein disulfide isomerase/cargo receptor subfamily unique to plants and chromalveolates

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• 作者：Christen Y. L. Yuen ; Katharine Wong…
• 关键词：Endoplasmic reticulum ; Cargo receptor ; Protein disulfide isomerase ; Golgi apparatus
• 刊名：Molecular Genetics and Genomics
• 出版年：2016
• 出版时间：February 2016
• 年：2016
• 卷：291
• 期：1
• 页码：455-469
• 全文大小：2,609 KB
• 参考文献：Andème Ondzighi C, Christopher DA, Cho EJ, Chang SC, Staehelin LA (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 20:2205–2220PubMed PubMedCentral CrossRef
  Anelli T, Alessio M, Mezghrani A, Simmen T, Talamo F, Bachi A, Sitia R (2002) ERp44, a novel endoplasmic reticulum folding assistant of the thioredoxin family. EMBO J 21:835–844PubMed PubMedCentral CrossRef
  Biterova EI, Svärd M, Possner DD, Guy JE (2013) The crystal structure of the lumenal domain of Erv41p, a protein involved in transport between the endoplasmic reticulum and Golgi apparatus. J Mol Biol 425:2208–2218PubMed CrossRef
  Brandizzi F, Barlowe C (2013) Organization of the ER-Golgi interface for membrane traffic control. Nat Rev Mol Cell Biol 14:382–392PubMed PubMedCentral CrossRef
  Burki F, Shalchian-Tabrizi K, Pawlowski J (2008) Phylogenomics reveals a new ‘megagroup’ including most photosynthetic eukaryotes. Biol Lett 4:366–369PubMed PubMedCentral CrossRef
  Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552PubMed CrossRef
  Chivers PT, Laboissiere MCA, Raines RT (1998) Protein disulfide isomerase: Cellular enzymology of the CXXC motif. In: Guzman N (ed) Prolyl hydroxylase, protein disulfide isomerase, and other structurally related proteins. Marcel Dekker, New York, pp 487–505
  Cho EJ, Yuen CY, Kang BH, Ondzighi CA, Staehelin LA, Christopher DA (2011) 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. Mol Cells 32:459–475PubMed PubMedCentral CrossRef
  Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743PubMed CrossRef
  d’Aloisio E, Paolacci AR, Dhanapal AP, Tanzarella OA, Porceddu E, Ciaffi M (2010) The protein disulfide isomerase gene family in bread wheat (T. aestivum L.). BMC Plant Biol 10:101PubMed PubMedCentral CrossRef
  Drozdetskiy A, Cole C, Procter J, Barton GJ (2015) JPred4: a protein secondary structure prediction server. Nucleic Acids Res 43:W389–W394PubMed PubMedCentral CrossRef
  Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797PubMed PubMedCentral CrossRef
  Edman JC, Ellis L, Blacher RW, Roth RA, Rutter WJ (1985) Sequence of protein disulphide isomerase and implications of its relationship to thioredoxin. Nature 317:267–270PubMed CrossRef
  Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer EL, Tate J, Punta M (2014) Pfam: the protein families database. Nucleic Acids Res 42:D222–D230PubMed PubMedCentral CrossRef
  Freedman RB (2009) Eukaryotic protein disulfide-isomerases and their potential in the production of disulfide-bonded protein products: what we need to know but do not! In: Buchner J, Moroder L (eds) Oxidative folding of peptides and proteins. Royal Society of Chemistry, Cambridge, pp 121–157
  Hampl V, Hug L, Leigh JW, Dacks JB, Lang BF, Simpson AG, Roger AJ (2009) Phylogenomic analyses support the monophyly of excavata and resolve relationships among eukaryotic “supergroups”. Proc Natl Acad Sci USA 106:3859–3864PubMed PubMedCentral CrossRef
  Houston NL, Fan C, Xiang JQ, 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 13:762–778CrossRef
  Jackson MR, Nilsson T, Peterson PA (1990) Identification of a consensus motif for retention of transmembrane proteins in the endoplasmic reticulum. EMBO J 9:3153–3162PubMed PubMedCentral
  Kemmink J, Darby NJ, Dijkstra K, Nilges M, Creighton TE (1997) The folding catalyst protein disulfide isomerase is constructed of active and inactive thioredoxin modules. Curr Biol 7:239–245PubMed CrossRef
  Kim K-W, Franceschi VR, Davin LB, Lewis NG (2006) β-Glucuronidase as reporter gene: advantages and limitations. In: Salinas J, Sanchez-Serrano JJ (eds) Arabidopsis protocols. Humana Press, Totowa, pp 263–273CrossRef
  Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580PubMed CrossRef
  Le SQ, Gascuel O (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25:1307–1320PubMed CrossRef
  Lu DP, Christopher DA (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 280:199–210PubMed CrossRef
  Onda Y, Nagamine A, Sakurai M, Kumamaru T, Ogawa M, 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 23:210–223PubMed PubMedCentral CrossRef
  Orci L, Ravazzola M, Mack GJ, Barlowe C, Otte S (2003) Mammalian Erv46 localizes to the endoplasmic reticulum-Golgi intermediate compartment and to cis-Golgi cisternae. Proc Natl Acad Sci USA 100:4586–4591PubMed PubMedCentral CrossRef
  Otte S, Barlowe C (2002) The Erv41p-Erv46p complex: multiple export signals are required in trans for COPII-dependent transport from the ER. EMBO J 21:6095–6104PubMed PubMedCentral CrossRef
  Otte S, Belden WJ, Heidtman M, Liu J, Jensen ON, Barlowe C (2001) Erv41p and Erv46p: new components of COPII vesicles involved in transport between the ER and Golgi complex. J Cell Biol 152:503–518PubMed PubMedCentral CrossRef
  Overvoorde P, Fukaki H, Beeckman T (2010) Auxin control of root development. Cold Spring Harb Perspect Biol 2:1–16CrossRef
  Porter BW, Yuen CY, Christopher DA (2015) Dual protein trafficking to secretory and non-secretory cell compartments: clear or double vision? Plant Sci 234:174–179PubMed CrossRef
  Price DC, Chan CX, Yoon HS, Yang EC, Qiu H, Weber AP, Schwacke R, Gross J, Blouin NA, Lane C, Reyes-Prieto A, Durnford DG, Neilson JA, Lang BF, Burger G, Steiner JM, Löffelhardt W, Meuser JE, Posewitz MC, Ball S, Arias MC, Henrissat B, Coutinho PM, Rensing SA, Symeonidi A, Doddapaneni H, Green BR, Rajah VD, Boore J, Bhattacharya D (2012) Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science 335:843–847PubMed CrossRef
  Ren J, Wen L, Gao X, Jin C, Xue Y, Yao X (2009) DOG 1.0: illustrator of protein domain structures. Cell Res 19:271–273PubMed CrossRef
  Scherens B, Dubois E, Messenguy F (1991) Determination of the sequence of the yeast YCL313 gene localized on chromosome III. Homology with the protein disulfide isomerase (PDI gene product) of other organisms. Yeast 7:185–193PubMed CrossRef
  Selles B, Jacquot JP, Rouhier N (2011) Comparative genomic study of protein disulfide isomerases from photosynthetic organisms. Genomics 97:37–50PubMed CrossRef
  Shibuya A, Margulis N, Christiano R, Walther TC, Barlowe C (2015) The Erv41-Erv46 complex serves as a retrograde receptor to retrieve escaped ER proteins. J Cell Biol 208:197–209PubMed PubMedCentral CrossRef
  Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729PubMed PubMedCentral CrossRef
  Wang CC, Tsou CL (1993) Protein disulfide isomerase is both an enzyme and a chaperone. FASEB J 7:1515–1517PubMed
  Wang H, Boavida LC, Ron M, 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 20:3300–3311PubMed PubMedCentral CrossRef
  Winter AD, McCormack G, Page AP (2007) Protein disulfide isomerase activity is essential for viability and extracellular matrix formation in the nematode Caenorhabditis elegans. Dev Biol 308:449–461PubMed CrossRef
  Wittenberg G, Levitan A, Klein T, Dangoor I, Keren N, Danon A (2014) Knockdown of the Arabidopsis thaliana chloroplast protein disulfide isomerase 6 results in reduced levels of photoinhibition and increased D1 synthesis in high light. Plant J 78:1003–1013PubMed CrossRef
  
• 作者单位：Christen Y. L. Yuen (1)
  Katharine Wong (1)
  David A. Christopher (1)
  
  1. Department of Molecular Biosciences and Bioengineering, University of Hawaii, 1955 East-West Rd., Ag. Science Rm 218, Honolulu, HI, 96822, USA
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Cell Biology
  Biochemistry
  Microbial Genetics and Genomics
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1617-4623

文摘

Protein disulfide isomerases (PDIs) play critical roles in protein folding by catalyzing the formation and rearrangement of disulfide bonds in nascent secretory proteins. There are six distinct PDI subfamilies in terrestrial plants. A unique feature of PDI-C subfamily members is their homology to the yeast retrograde (Golgi-to-endoplasmic reticulum) cargo receptor proteins, Erv41p and Erv46p. Here, we demonstrate that plant Erv41p/Erv46p-like proteins are divided into three subfamilies: ERV-A, ERV-B and PDI-C, which all possess the N-proximal and C-proximal conserved domains of yeast Erv41p and Erv46p. However, in PDI-C isoforms, these domains are separated by a thioredoxin domain. The distribution of PDI-C isoforms among eukaryotes indicates that the PDI-C subfamily likely arose through an ancient exon-shuffling event that occurred before the divergence of plants from stramenopiles and rhizarians. Arabidopsis has three PDI-C genes: PDI7, PDI12, and PDI13. PDI12- and PDI13-promoter: β-glucuronidase (GUS) gene fusions are co-expressed in pollen and stipules, while PDI7 is distinctly expressed in the style, hydathodes, and leaf vasculature. The PDI-C thioredoxin domain active site motif CxxS is evolutionarily conserved among land plants. Whereas PDI12 and PDI13 retain the CxxS motif, PDI7 has a CxxC motif similar to classical PDIs. We hypothesize that PDI12 and PDI13 maintain the ancestral roles of PDI-C in Arabidopsis, while PDI7 has undergone neofunctionalization. The unusual PDI/cargo receptor hybrid arrangement in PDI-C isoforms has no counterpart in animals or yeast, and predicts the need for pairing redox functions with cargo receptor processes during protein trafficking in plants and other PDI-C containing organisms. Keywords Endoplasmic reticulum Cargo receptor Protein disulfide isomerase Golgi apparatus