Importance of post-translational modifications for functionality of a chloroplast-localized carbonic anhydrase (CAH1) in Arabidopsis thaliana

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Burén, Stefan ^a,c   Ortega Villasante, Cristina ^b   Blanco Rivero, Amaya ^b   Martínez Bernardini, Andrea ^a,b   Shutova, Tatiana ^a   Shevela, Dmitriy ^a   Messinger, Johannes ^a   Bako, Laszlo ^a   Villarejo, Arsenio ^b   Samuelsson, Göran ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^c Centro Nacional de Investigaciones Oncológicas   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CARBONATE DEHYDRATASE I; CHAPERONE; CYSTEINE; ARABIDOPSIS PROTEIN; CAH1 PROTEIN, ARABIDOPSIS; CARBONATE DEHYDRATASE; DISULFIDE; POLYSACCHARIDE;

ARABIDOPSIS; ARTICLE; CHLOROPLAST; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME LOCALIZATION; GLYCOSYLATION; IN VIVO STUDY; MASS SPECTROMETRY; NONHUMAN; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN STABILITY; SECRETORY PATHWAY; TRANSIENT EXPRESSION; WILD TYPE; AMINO ACID SEQUENCE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; CYTOLOGY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN CONFORMATION; PROTEIN TRANSPORT;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EMBRYOPHYTA;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BINDING SITES; CARBONIC ANHYDRASES; CHLOROPLASTS; DISULFIDES; ENDOPLASMIC RETICULUM; GLYCOSYLATION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; POLYSACCHARIDES; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT;

EID: 79958744741     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021021     Document Type: Article

References (54)

1. Khalifah RG, (1971) The carbon dioxide hydration activity of carbonic anhydrase. I. Stop-flow kinetic studies on the native human isoenzymes B and C. J Biol Chem 246: 2561-2573.
2. Moroney JV, Bartlett SG, Samuelsson G, (2001) Carbonic anhydrases in plants and algae. Plant Cell Environ 24: 141-153.
3. Samuelsson G, Karlsson J, (2001) Chloroplastic Carbonic Anhydrases. In: Aro E-M, Andersson B, editors. Regulation of Photosynthesis Dordrecht, The Netherlands Kluwer Academic Publishers pp. 313-320.
4. Fabre N, Reiter IM, Becuwe-Linka N, Genty B, Rumeau D, (2007) Characterization and expression analysis of genes encoding alpha and beta carbonic anhydrases in Arabidopsis. Plant Cell Environ 30: 617-629.
5. Sawaya MR, Cannon GC, Heinhorst S, Tanaka S, Williams EB, et al. (2006) The structure of beta-carbonic anhydrase from the carboxysomal shell reveals a distinct subclass with one active site for the price of two. J Biol Chem 281: 7546-7555.
6. Hewett-Emmett D, Tashian RE, (1996) Functional diversity, conservation, and convergence in the evolution of the alpha-, beta-, and gamma-carbonic anhydrase gene families. Mol Phylogenet Evol 5: 50-77.
7. Villarejo A, Buren S, Larsson S, Dejardin A, Monne M, et al. (2005) Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast. Nat Cell Biol 7: 1224-1231.
8. Emanuelsson O, Brunak S, von Heijne G, Nielsen H, (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2: 953-971.
9. Hebert DN, Molinari M, (2007) In and out of the ER: protein folding, quality control, degradation, and related human diseases. Physiol Rev 87: 1377-1408.
10. Asatsuma S, Sawada C, Itoh K, Okito M, Kitajima A, et al. (2005) Involvement of alpha-amylase I-1 in starch degradation in rice chloroplasts. Plant Cell Physiol 46: 858-869.
11. Kitajima A, Asatsuma S, Okada H, Hamada Y, Kaneko K, et al. (2009) The Rice {alpha}-Amylase Glycoprotein Is Targeted from the Golgi Apparatus through the Secretory Pathway to the Plastids. Plant Cell 21: 2844-2858.
12. Chen MH, Liu LF, Chen YR, Wu HK, Yu SM, (1994) Expression of alpha-amylases, carbohydrate metabolism, and autophagy in cultured rice cells is coordinately regulated by sugar nutrient. Plant J 6: 625-636.
13. Chen MH, Huang LF, Li HM, Chen YR, Yu SM, (2004) Signal peptide-dependent targeting of a rice alpha-amylase and cargo proteins to plastids and extracellular compartments of plant cells. Plant Physiol 135: 1367-1377.
14. Nanjo Y, Oka H, Ikarashi N, Kaneko K, Kitajima A, et al. (2006) Rice plastidial N-glycosylated nucleotide pyrophosphatase/phosphodiesterase is transported from the ER-golgi to the chloroplast through the secretory pathway. Plant Cell 18: 2582-2592.
15. Jarvis P, Robinson C, (2004) Mechanisms of protein import and routing in chloroplasts. Curr Biol 14: R1064-1077.
16. Mitra N, Sinha S, Ramya TN, Surolia A, (2006) N-linked oligosaccharides as outfitters for glycoprotein folding, form and function. Trends Biochem Sci 31: 156-163.
17. Parodi AJ, (2000) Role of N-oligosaccharide endoplasmic reticulum processing reactions in glycoprotein folding and degradation. Biochem J 348 Pt 1: 1-13.
18. Maley F, Trimble RB, Tarentino AL, Plummer TH Jr, (1989) Characterization of glycoproteins and their associated oligosaccharides through the use of endoglycosidases. Anal Biochem 180: 195-204.
19. Kornfeld R, Kornfeld S, (1985) Assembly of asparagine-linked oligosaccharides. Annu Rev Biochem 54: 631-664.
20. Bencur P, Steinkellner H, Svoboda B, Mucha J, Strasser R, et al. (2005) Arabidopsis thaliana beta1,2-xylosyltransferase: an unusual glycosyltransferase with the potential to act at multiple stages of the plant N-glycosylation pathway. Biochem J 388: 515-525.
21. Downing WL, Galpin JD, Clemens S, Lauzon SM, Samuels AL, et al. (2006) Synthesis of enzymatically active human alpha-L-iduronidase in Arabidopsis cgl (complex glycan-deficient) seeds. Plant Biotechnol J 4: 169-181.
22. Lerouge P, Cabanes-Macheteau M, Rayon C, Fischette-Laine AC, Gomord V, et al. (1998) N-glycoprotein biosynthesis in plants: recent developments and future trends. Plant Mol Biol 38: 31-48.
23. Faye L, Chrispeels MJ, (1985) Characterization of N-linked oligosaccharides by affinoblotting with concanavalin A-peroxidase and treatment of the blots with glycosidases. Anal Biochem 149: 218-224.
24. von Schaewen A, Sturm A, O'Neill J, Chrispeels MJ, (1993) Isolation of a mutant Arabidopsis plant that lacks N-acetyl glucosaminyl transferase I and is unable to synthesize Golgi-modified complex N-linked glycans. Plant Physiol 102: 1109-1118.
25. Shental-Bechor D, Levy Y, (2008) Effect of glycosylation on protein folding: a close look at thermodynamic stabilization. Proc Natl Acad Sci U S A 105: 8256-8261.
26. Wujek P, Kida E, Walus M, Wisniewski KE, Golabek AA, (2004) N-glycosylation is crucial for folding, trafficking, and stability of human tripeptidyl-peptidase I. J Biol Chem 279: 12827-12839.
27. Williams DB, (2006) Beyond lectins: the calnexin/calreticulin chaperone system of the endoplasmic reticulum. J Cell Sci 119: 615-623.
28. Li J, Zhao-Hui C, Batoux M, Nekrasov V, Roux M, et al. (2009) Specific ER quality control components required for biogenesis of the plant innate immune receptor EFR. Proc Natl Acad Sci U S A 106: 15973-15978.
29. Hong Z, Jin H, Tzfira T, Li J, (2008) Multiple mechanism-mediated retention of a defective brassinosteroid receptor in the endoplasmic reticulum of Arabidopsis. Plant Cell 20: 3418-3429.
30. Sung DY, Vierling E, Guy CL, (2001) Comprehensive expression profile analysis of the Arabidopsis Hsp70 gene family. Plant Physiol 126: 789-800.
31. Crofts AJ, Leborgne-Castel N, Pesca M, Vitale A, Denecke J, (1998) BiP and calreticulin form an abundant complex that is independent of endoplasmic reticulum stress. Plant Cell 10: 813-824.
32. Kjaer S, Ibanez CF, (2003) Intrinsic susceptibility to misfolding of a hot-spot for Hirschsprung disease mutations in the ectodomain of RET. Hum Mol Genet 12: 2133-2144.
33. Forsayeth JR, Gu Y, Hall ZW, (1992) BiP forms stable complexes with unassembled subunits of the acetylcholine receptor in transfected COS cells and in C2 muscle cells. J Cell Biol 117: 841-847.
34. Waheed A, Okuyama T, Heyduk T, Sly WS, (1996) Carbonic anhydrase IV: purification of a secretory form of the recombinant human enzyme and identification of the positions and importance of its disulfide bonds. Arch Biochem Biophys 333: 432-438.
35. Husic HD, (1991) Extracellular carbonic anhydrase of Chlamydomonas reinhardtii: localization, structural properties, and catalytic properties. Canadian Journal of Botany 69: 1079-1087.
36. Hilvo M, Tolvanen M, Clark A, Shen B, Shah GN, et al. (2005) Characterization of CA XV, a new GPI-anchored form of carbonic anhydrase. Biochem J 392: 83-92.
37. Price GD, Caemmerer S, Evans YR, Yu Y-W, Lloyd Y, et al. (1994) Specific reduction of chloroplast carbonic anhydrase activity by antisense RNA in transgenic tobacco plants has a minor effect on photosynthetic CO2 assimilation. Planta 193: 331-340.
38. Badger MR, Price GD, (1994) THE ROLE OF CARBONIC ANHYDRASE IN PHOTOSYNTHESIS. Annu Rev Plant Physiol Plant Mol Biol 45: 369-392.
39. Jin H, Yan Z, Nam KH, Li J, (2007) Allele-specific suppression of a defective brassinosteroid receptor reveals a physiological role of UGGT in ER quality control. Mol Cell 26: 821-830.
40. Hancock KR, Phillips LD, White DW, Ealing PM, (1997) pPE1000: a versatile vector for the expression of epitope-tagged foreign proteins in transgenic plants. Biotechniques 22: 861-862, 865.
41. Curtis MD, Grossniklaus U, (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133: 462-469.
42. Song CJ, Steinebrunner I, Wang XZ, Stout SC, Roux SJ, (2006) Extracellular ATP induces the accumulation of superoxide via NADPH oxidases in Arabidopsis. Plant Physiology 140: 1222-1232.
43. Leung J, Orfanidi S, Chefdor F, Meszaros T, Bolte S, et al. (2006) Antagonistic interaction between MAP kinase and protein phosphatase 2C in stress recovery. Plant Science 171: 596-606.
44. Yoo SD, Cho YH, Sheen J, (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2: 1565-1572.
45. Gasparian M, Pusterla M, Baldan B, Downey PM, Rossetto O, et al. (2000) Identification and characterization of an 18-kilodalton, VAMP-like protein in suspension-cultured carrot cells. Plant Physiol 122: 25-34.
46. Richardson MC, Ingamells S, Simonis CD, Cameron IT, Sreekumar R, et al. (2009) Stimulation of lactate production in human granulosa cells by metformin and potential involvement of adenosine 5′ monophosphate-activated protein kinase. J Clin Endocrinol Metab 94: 670-677.
47. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
48. Arnold K, Bordoli L, Kopp J, Schwede T, (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201.
49. Kiefer F, Arnold K, Kunzli M, Bordoli L, Schwede T, (2009) The SWISS-MODEL Repository and associated resources. Nucleic Acids Res 37: D387-392.
50. Peitsch MC, (1995) Protein modelling by e-mail. Bio/Technology 13: 658-660.
51. Huang S, Xue Y, Sauer-Eriksson E, Chirica L, Lindskog S, et al. (1998) Crystal structure of carbonic anhydrase from Neisseria gonorrhoeae and its complex with the inhibitor acetazolamide. J Mol Biol 283: 301-310.
52. Guex N, Peitsch MC, (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18: 2714-2723.
53. Clausen J, Beckmann K, Junge W, Messinger J, (2005) Evidence that bicarbonate is not the substrate in photosynthetic oxygen evolution. Plant Physiol 139: 1444-1450.
54. Messinger J, Badger M, Wydrzynski T, (1995) Detection of one slowly exchanging substrate water molecule in the S3 state of photosystem II. Proc Natl Acad Sci U S A 92: 3209-3213.