A second protein L-isoaspartyl methyltransferase gene in Arabidopsis produces two transcripts whose products are sequestered in the nucleus

Plant Physiology

Volumn 136, Issue 1, 2004, Pages 2652-2664

  Xu, Qilong ^a   Belcastro, Marisa P ^a,d   Villa, Sarah T ^c   Dinkins, Randy D ^b   Clarke, Steven G ^c   Downie, A Bruce ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CARBOXYLIC ACIDS; ENZYMES; FRACTIONATION; PLANTS (BOTANY); SEED; TISSUE;

CELL FRACTIONATION; GENES ENCODING; IMMUNOBLOT DETECTION; SEED GERMINATION;

GENES;

ABSCISIC ACID; AMINO ACIDS; ENZYMES; FRACTIONATION; GENES; PLANTS; SEEDS; TISSUE;

ARABIDOPSIS;

COMPLEMENTARY DNA; ISOENZYME; PLANT DNA; PLANT RNA; PROTEIN DEXTRO ASPARTATE METHYLTRANSFERASE; RECOMBINANT PROTEIN;

ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CELL NUCLEUS; ENZYMOLOGY; GENE; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; SEEDLING; TRANSGENIC PLANT;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ARABIDOPSIS; BASE SEQUENCE; CELL NUCLEUS; DNA, COMPLEMENTARY; DNA, PLANT; GENE EXPRESSION; GENES, PLANT; ISOENZYMES; MOLECULAR SEQUENCE DATA; PLANTS, GENETICALLY MODIFIED; PROTEIN D-ASPARTATE-L-ISOASPARTATE METHYLTRANSFERASE; RECOMBINANT PROTEINS; RNA, PLANT; SEEDLING; TRANSCRIPTION, GENETIC;

EID: 16544392723     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.104.046094     Document Type: Article

References (64)

1. Aswad DW, Paranandi MV, Schurter BT (2000) Isoaspartate in peptides and proteins: formation, significance, and analysis. J Pharm Biomed Anal 21: 1129-1136
2. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K[r] (1994) Current Protocols in Molecular Biology. John Wiley & Sons, New York
3. Bannai H, Tamada Y, Maruyama O, Nakai K, Miyano S (2002) Extensive feature detection of N-terminal protein sorting signals. Bioinformatics 18: 298-305
4. Bhatt NP, Patel K, Borchardt RT (1990) Chemical pathways of peptide degradation. I. Deamidation of adrenocorticotropic hormone. Pharm Res 7: 593-599
5. Brennan TV, Anderson JW, Jia Z, Waygood EB, Clarke S (1994) Repair of spontaneously deamidated HPr phosphocarrier protein catalyzed by the L-isoaspartate-(D-aspartate) O-methyltransferase. J Biol Chem 269: 24586-24595
6. Clarke S (1999) A protein carboxyl methyltransferase that recognizes age-damaged peptides and proteins and participates in their repair. In X Cheng, RM Blumenthal, eds, S-Adenosylmethionine-Dependent Methyltransferases: Structures and Functions. World Scientific, Singapore, pp 123-148
7. Clarke S (2003) Aging as war between chemical and biochemical processes: protein methylation and the recognition of age-damaged proteins for repair. Ageing Res Rev 2: 263-285
8. David CL, Keener J, Aswad DW (1999) Isoaspartate in ribosomal protein S11 of Escherichia coli. J Bacteriol 181: 2872-2877
9. Dinkins RD, Conn HM, Dirk LMA, Williams MA, Houtz RL (2003) The Arabidopsis thaliana PEPTIDE DEFORMYLASE 1 protein is localized to both mitochondria and chloroplasts. Plant Sci 165: 751-758
10. Esposito L, Vitagliano L, Sica F, Sorrentino G, Zagari A, Mazzarella L (2000) The ultrahigh resolution crystal structure of ribonuclease A containing an isoaspartyl residue: hydration and sterochemical analysis. J Mol Biol 297: 713-732
11. Flinta C, Persson B, Jornvall H, von Heihne G (1986) Sequence determinants of cytosolic N-terminal protein processing. Eur J Biochem 154: 193-196
12. Gallelti P, Ingrosso D, Manna C, Clemente G, Zappia V (1995) Protein damage and methylation-mediated repair in the erythrocyte. Biochem J 306: 313-325
13. Gehrig HH, Winter K, Cushman J, Borland A, Taybi T (2000) An improved RNA isolation method for succulent plant species rich in polyphenols and polysaccharides. Plant Mol Biol Report 18: 369-376
14. Geiger T, Clarke S (1987) Deamidation, isomerization, and racemization at asparaginyl and aspartyl residues in peptides: succinimide-linked reactions that contribute to protein degradation. J Biol Chem 262: 785-794
15. Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27: 297-300
16. Himmelbach A, Yang Y, Grill E (2003) Relay and control of abscisic acid signaling. Curr Opin Plant Biol 6: 470-479
17. Hoshi T, Heinemann S (2001) Regulation of cell function by methionine oxidation and reduction. J Physiol 531: 1-11
18. Hu YJ, Wei Y, Zhou Y, Rajagopalan PT, Pei D (1999) Determination of substrate specificity for peptide deformylase through the screening of a combinatorial peptide library. Biochemistry 38: 643-650
19. Johnson BA, Nigo SQ, Aswad DW (1991) Widespread phylogenetic distribution of a protein methyltransferase that modifies L isoaspartyl residues. Biochem Int 24: 841-848
20. Joyce C (2002) Quantitative RT-PCR. In J O'Connell, ed, RT-PCR Protocols, Vol 193. Humana Press, Totowa, NJ, pp 83-102
21. Kagan RM, Clarke S (1994) Widespread occurrence of three sequence motifs in diverse S-adenosylmethionine-dependent methyltransferases suggests a common structure for these enzymes. Arch Biochem Biophys 310: 417-427
22. Kagan RM, McFadden HJ, McFadden PN, O'Connor C, Clarke S (1997a) Molecular phylogenetics of a protein repair methyltransferase. Comp Biochem Physiol 117B: 379-385
23. Kagan RM, Niewmierzycka A, Clarke S (1997b) Targeted gene disruption of the Caenorhabditis elegans L-isoaspartyl protein repair methyltransferase impairs survival of dauer stage nematodes. Arch Biochem Biophys 348: 320-328
24. Karssen CM, Brinkhorst-van der Swan DLC, Breekland AE, Koornneef M (1983) Induction of dormancy during seed development by endogenous abscisic acid: studies on abscisic acid deficient genotypes of Arabidopsis thaliana (L.) Heynh. Planta 157: 158-165
25. Kazan K (2003) Alternative splicing and proteome diversity in plants: the tip of the iceberg has just emerged. Trends Pharmacol Sci 8: 468-471
26. Kester ST, Geneve RL, Houtz RL (1997) Priming and accelerated aging affect L-isoaspartyl methyltransferase activity in tomato (Lycopersicon esculentum Mill.) seed. J Exp Bot 309: 943-949
27. Kim E, Lowenson JD, MacLaren DC, Clarke S, Young SG (1997) Deficiency of a protein-repair enzyme results in the accumulation of altered proteins, retardation of growth, and fatal seizures in mice. Proc Natl Acad Sci USA 94: 6132-6137
28. Konieczny A, Ausubel FM (1993) A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J 4: 403-410
29. Kuhn JM, Schroeder JI (2003) Impacts of altered RNA metabolism on abscisic acid signaling. Curr Opin Plant Biol 6: 463-469
30. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685
31. Lowenson JD, Clarke S (1992) Recognition of D-aspartyl residues in polypeptides by the erythrocyte L-isoaspartyl/D-aspartyl protein methyltransferase: implications for the repair process. J Biol Chem 267: 5985-5995
32. Maclaren DC, Kagan RM, Clarke S (1992) Alternative splicing of the human isoaspartyl protein carboxyl methyltransferase RNA leads to the generation of a C-terminal-RDEL sequence in isozyme II. Biochem Biophys Res Commun 185: 277-283
33. Mamula MJ, Gee RJ, Elliott JI, Sette A, Southwood S, Jones PJ, Blier PR (1999) Isoaspartyl post-translational modification triggers autoimmune responses to self-proteins. J Biol Chem 274: 22321-22327
34. Martinez-Garcia JF, Monte E, Quail PH (1999) A simple, rapid and quantitative method for preparing Arabidopsis protein extracts for immunoblot analysis. Plant J 20: 251-257
35. Mudgett MB, Clarke S (1993) Characterization of plant L-isoaspartyl mehtyltransferases that may be involved in seed survival: purification, cloning and sequence analysis of the wheat germ enzyme. Biochemistry 32: 11100-11111
36. Mudgett MB, Clarke S (1994) Hormonal and environmental responsiveness of a developmentally regulated protein repair L-isoaspartyl methyltransferase in wheat. J Biol Chem 41: 25606-25612
37. Mudgett MB, Clarke S (1996) A distinctly regulated protein repair L-isoaspartyl methyltransferase from Arabidopsis thalinana. Plant Mol Biol 30: 723-737
38. Mudgett MB, Lowenson JD, Clarke S (1997) Protein repair L-isoaspartyl methyltransferase in plants: phylogenetic distribution and the accumulation of substrate proteins in aged barley seeds. Plant Physiol 115: 1481-1489
39. O'Connor CM (1987) Regulation and subcellular distribution of a protein methyltransferase and its damaged aspartyl substrate sties in developing Xenopus oocytes. J Biol Chem 262: 10398-10403
40. O'Connor CM, Germain BJ (1987) Kinetic and electrophoretic analysis of transmethylation reactions in intact Xenopus oocytes. J Biol Chem 262: 10404-10411
41. Pliyev BK, Gurvits BY (1999) Peptidyl-prolyl cis-trans isomerases: structure and functions. Biochemistry 64: 738-751
42. Potter SM, Johnson BA, Henschen A, Aswad DW (1992) The type II isoform of bovine brain protein L-isoaspartyl methyltransferase has an endoplasmic reticulum retention signal (...RDEL) at its C-terminus. Biochemistry 31: 6337-6347
43. Reissner KJ, Aswad DW (2003) Deamidation and isoaspartate formation in proteins: unwanted alterations or surreptitious signals? Cell Mol Life Sci 60: 1281-1295
44. Romanik EA, Ladino CA, Killoy LC, D'Adrenne SC, O'Conner CM (1992) Genomic organization and tissue expression of the murine gene encoding the protein β-aspartate methyltransferase. Gene 118: 217-222
45. Rost B (1996) PHD: predicting one-dimensional protein structure by profile based neural networks. Methods Enzymol 266: 525-539
46. Sarnowski TJ, Swiezewski S, Pawlikowska K, Kaczanowski S, Jerzmanowski A (2002) AtSWI3B, an Arabidopsis homolog of SWI3, a core subunit of yeast Swi/Snf chromatin remodeling complex, interacts with FCA, a regulator of flowering time. Nucleic Acids Res 30: 3412-3421
47. Schardl CL, Byrd AD, Benzion G, Altschuler MA, Hildebrand DF, Hunt AG (1987) Design and construction of a versatile system for the expression of foreign genes in plants. Gene 61: 1-12
48. Schumacher RJ, Hansen WJ, Freeman BC, Alnemri E, Litwack G, Toft DO (1996) Cooperative action of Hsp70, Hsp90, and DnaJ proteins in protein renaturation. Biochemistry 35: 14889-14898
49. Scott A, Wyatt S, Tsou PL, Roberston D, Strömgren Allen N (1999) Model system for plant cell biology: GFP imaging in living onion epidermal cells. Biotechniques 26: 1125-1132
50. Stamm S (2002) Signals and their transduction pathways regulating alternative splicing: a new dimension of the human genome. Hum Mol Genet 11: 2409-2416
51. Szymanska G, Leszyk JD, O'Connor CM (1998) Carboxyl methylation of deamidated calmodulin increases its stability in Xenopus oocyte cytoplasm: implications for protein repair. J Biol Chem 273: 28516-28523
52. Talcott B, Moore MS (1999) Getting across the nuclear pore complex. Trends Cell Biol 9: 312-318
53. 2+ free calmodulin and calmodulin damaged by in vitro aging are selectively degraded by 26 S proteasomes without ubiquitination. J Biol Chem 275: 20295-20301
54. Thapar N, Clarke S (2000) Expression, purification, and characterization of the protein repair L-isoaspartyl methyltransferase from Arabidopsis thaliana. Protein Expr Purif 20: 237-251
55. Thapar N, Griffith SC, Yeates TO, Clarke S (2002) Protein repair methyltransferase from the hyperthermophilic archaeon Pyrococcus furiosus: unusual methyl-accepting affinity for D-aspartyl and N-succinyl-containing peptides. J Biol Chem 277: 1058-1065
56. Thapar N, Kim A-K, Clarke S (2001) Distinct patterns of expression but similar biochemical properties of protein L-isoaspartyl methyltransferase in higher plants. Plant Physiol 125: 1023-1035
57. Trievel RC, Beach BM, Dirk LMA, Houtz RL, Hurley JH (2002) Structure and catalytic mechanism of a SET domain protein methyltransferase. Cell 111: 91-103
58. Visick JE, Cai H, Clarke S (1998) The L-isoaspartyl protein repair methyltransferase enhances survival of aging Escherichia coli subjected to secondary environmental stresses. J Bacteriol 180: 2623-2629
59. Visick JE, Clarke S (1995) Repair, refold, recycle: how bacteria can deal with spontaneous and environmental damage to proteins. Mol Microbiol 16: 835-845
60. Wan C-Y, Wilkins TA (1994) A modified hot borate method significantly enhances the yield of high quality RNA from cotton (Gossypium hirsutum L.). Anal Biochem 223: 7-12
61. Yamamoto A, Takagi H, Kitamura D, Tatsuoka H, Nakano H, Kawano H, Kuroyanagi H, Yahagi Y, Kobayashi S, Koizumi K, et al (1998) Deficiency in protein L-isoaspartyl methyltransferase results in a fatal progressive epilepsy. J Neurosci 18: 2063-2074
62. Ying Z, Mulligan RM, Janney N, Houtz RL (1999) Rubisco small and large subunit N-methyltransferases: Bi- and mono-functional methyltransferases that methylate the small and large subunits of RUBISCO. J Biol Chem 274: 36750-36756
63. Young AL, Carter WG, Doyle HA, Mamula MJ, Aswad DW (2001) Structural integrity of histone H2B in vivo requires the activity of protein L-isoaspartate O-methyltransferase, a putative repair enzyme. J Biol Chem 276: 37161-37165
64. Zou Y, Crowley DJ, Van Houten B (1998) Involvement of molecular chaperonins in nucleotide excision repair: DnaK leads to increased thermal stability of UvrA, catalytic UvrB loading, enhanced repair, and increased UV resistance. J Biol Chem 273: 12887-12892