A novel C-terminal proteolytic processing of cytosolic pyruvate kinase, its phosphorylation and degradation by the proteasome in developing soybean seeds

Plant Journal

Volumn 34, Issue 1, 2003, Pages 77-93

  Tang, Guo Qing ^a   Hardin, Shane C ^a   Dewey, Ralph ^a   Huber, Steven C ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

C terminal truncation; Degradation; Phosphorylation site; Proteasome; Pyruvate kinase; Soybean (Glycine max (L.) cv. Ransom)

Indexed keywords

CENTRIFUGATION; DEGRADATION; ENZYMES; POLYPEPTIDES; SIZE EXCLUSION CHROMATOGRAPHY;

PHOSPHORYLATION;

SEED;

AMINO ACID SEQUENCE; CYTOSOL; MOLECULAR WEIGHT; PEPTIDE HYDROLASES; PHOSPHORYLATION; PHYLOGENY; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN SUBUNITS; PYRUVATE KINASE; SEEDS; SOYBEANS;

CENTRIFUGATION; DEGRADATION; ENZYMES; SEEDS;

EMBRYOPHYTA; GLYCINE MAX;

EID: 0037699019     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.2003.01711.x     Document Type: Article

References (45)

1. Attaix, D., Combaret, L., Pouch, M.N. and Taillandier, D. (2001) Regulation of proteolysis. Curr. Opin. Clin. Nutr. Metab. Care, 4, 45-54.
2. Bachmann, M., Shiraishi, N., Campbell, W.H., Yoo, B.-C., Harmon, A.C. and Huber, S.C. (1996) Identification of Ser-543 as the major regulatory phosphorylation site in spinach leaf nitrate reductase. Plant Cell, 8, 505-517.
3. Biederer, T., Volkwein, C. and Sommer, T. (1997) Role of Cue1p in ubiquitination and degradation at the ER surface. Science, 278 (5344), 1806-1809.
4. Blakeley, S.D., Plaxton, W.C. and Dennis, D.T. (1990) Cloning and characterization of a cDNA for the cytosolic isozyme of plant pyruvate kinase: the relationship between the plant and non-plant enzyme. Plant Mol. Biol. 15, 665-669.
5. Brazill, D.T., Thorner, J. and Marin, G.S. (1997) Mck1, a member of the glycogen synthase kinase 3 family of protein kinases, is a negative regulator of pyruvate kinase in the yeast Saccharomyces cerevisiae. J. Bacteriol. 179, 4415-4423.
6. Callis. J. and Vierstra, R.D. (2000) Protein degradation in signaling. Curr. Opin. Plant Biol. 3, 381-386.
7. Cough, R.C. and Vierstra, R.D. (1997) Phytochrome degradation. Plant Cell Environ. 20, 713-721.
8. Doelling, J.H., Yan, N., Kurepa, J., Walker, J. and Viestra, R.D. (2001) The ubiquitin-specific protease UBP14 is essential for early embryo development in Arabidopsis thaliana. Plant J. 27, 393-405.
9. Doucet, J.P., Murphy, B.J. and Tuana, B.S. (1990) Modification of a discontinuous and highly porous sodium dodecyl sulfate-polyacrylamide gel system for mini gel electrophoresis. Anal. Biochem. 190, 209-211.
10. Engstrom, L. (1980) Regulation of liver pyruvate kinase by phosphorylation-dephosphorylation. In Molecular Aspects of Cellular Regulation. Recently Discovered Systems of Enzyme Regulation by Reversible Phosphorylation, Vol. 1 (Cohen, P., ed.). New York: Elsevier/North-Holland Biomedical Press, pp. 11-31.
11. Estelle, M. (2001) Proteases and cellular regulation in plants. Curr. Opin. Plant Biol. 4, 254-260.
12. Ferreira, R.M.B., Ramos, P.C.R., Franco, E., Ricardo, C.P.P. and Teixeira, A.R.N. (1995) Changes in ubiquitin and ubiquitin-protein conjugates during seed formation and germination. J. Exp. Bot. 46, 211-219.
13. Fujinami, K., Tanahashi, N., Tanaka, K., Ichihara, A., Cejka, Z., Baumeister, W., Miyawaki, M., Sato, T. and Nakagawa, H. (1994) Purification and characterization of the 26S proteasome from spinach leaves. J. Biol. Chem. 269, 25905-25910.
14. Gray, W.M., Kepinski, S., Rouse, D., Leyser, O. and Estelle, M. (2001) Auxin regulates SCF (TIR1)-dependent degradation of AUX/IAA proteins. Nature, 414, 271-276.
15. Halford, N.G. and Hardie, D.G. (1998) SNF1-related protein kinases: global regulators of carbon metabolism in plants? Plant Mol. Biol. 37, 735-748.
16. Hardin, S., Winter, H. and Huber, S.C. (2002) Sucrose synthase is phosphorylated on a novel secondary site (serine 170) that may promote proteasome-dependent degradation. In Proceedings of Plant Biology 2002, 3-7 August, Deveur, Colorado. Rockville, MD: American Society of Plant Biologists, (http://www.aspb.org/annual-meeting/pb-2002/2002.html) (Abstract #752).
17. 2+ signal? Trends Plant Sci. 5, 154-159.
18. Harper, J.W. (2002) A phosphorylation-driven ubiquitination switch for cell-cycle control. Trends Cell Biol. 12, 104-107.
19. Hershko, A. and Ciechanover, A. (1998) The ubiquitin system. Annu. Rev. Biochem. 67, 425-479.
20. Hu, Z. and Plaxton, W.C. (1996) Purification and characterization of cytosolic pyruvate kinase from leaves of the castor oil plant. Arch. Biochem. Biophys. 333, 298-307.
21. Hu, Z., Zhang, Z.S., Doo, E., Coux, O., Goldberg, A.L. and Liang, T.J. (1999) Hepatitis B vitrus X protein is both a substrate and a potential inhibitor of the proteasome complex. J. Virol. 73, 7231-7240.
22. Huang, Z.J. and Huber, S.C. (2001) Phosphorylation of synthetic peptides by a CDPK and plant SNF1-related protein kinase. Influence of proline and basic amino acid residues at selected positions. Plant Cell Physiol. 42, 1079-1087.
23. Imamura, K. and Tanaka, T. (1982) Pyruvate kinase isozymes from rat. Meth. Enzymol. 90, 150-165.
24. Kiefer, E., Heller, W. and Ernst, D. (2000) A simple and efficient protocol for isolation of functional RNA from plant tissue rich in secondary metabolites. Plant Mol. Biol. Rep. 18, 33-39.
25. Kisselev, A.F., Akopian, T.N., Woo, K.M. and Goldberg, A.L. (1999) The size of peptide generated from protein by mammalian 26 and 20S proteasomes. J. Biol. Chem. 274, 3363-3371.
26. Ljungstrom, O., Berglund, L. and Engstrom, L. (1976) Studies on the kinetic effects of adenosine-3′:5′-monophosphate-dependent phosphorylation of purified pig-liver pyruvate kinase type L. Eur. J. Biochem. 68, 497-506.
27. Lone, Y.-C., Simon, M.-P., Kahn, A. and Marie, J. (1986) Complete nucleotide and deduced amino acid sequence of rat L-type pyruvate kinase. FEBS Lett. 195, 97-100.
28. Miller, W.A., Waterhouse, P.M., Brown, J.W.S. and Browning, K.S. (2001) The RNA world in plants: post-transcriptional control III. Plant Cell, 13, 1710-1717.
29. Noguchi, T., Inoue, H. and Tanaka, T. (1986) The M1- and M2-tryp isozymes of rat pyruvate kinase are produced from the same gene by alternative RNA splicing. J. Biol. Chem. 261, 13807-13812.
30. O'Hagan, R.C., Ohh, M., David, G., Alboran, I., Moreno, D., Alt, F.W., Kaelin, J.W.G. and DePinho, R.A. (2000) Myc-enhanced expression of cull promotes ubquitin-dependent proteolysis and cell cycle progression. Genes Dev. 14, 2185-2191.
31. Peng, Z., Staub, J.M., Serino, G., Kwok, S.F., Kurepa, J., Bruce, B.D., Vierstra, R.D., Wei, N. and Deng, X.W. (2001) The cellular level of PR500, a protein complex related to the 19S regulatory particle of the proteasome, is regulated in response to stresses in plants. Mol. Biol. Cell, 12, 383-392.
32. Platt, S.G. and Bassham, J.A. (1978) Photosynthesis and increased production of protein. Adv. Expl. Med. Biol. 105, 195-247.
33. Plaxton, W.C. (1996) The organization and regulation of plant glycolysis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 185-214.
34. Podesta, F.E. and Plaxton, W.C. (1991) Kinetic and regulatory properties of cytosolic pyruvate kinase from germinating castor oil seeds. Biochem. J. 279, 495-501.
35. Podust, V.N., Brownell, J.E., Gladysheva, T.B., Luo, R.S., Wang, C., Coggins, M.B., Pierce, J.W., Lightcap, E.S. and Chau, V.A. (2000) Nedd8 conjugation pathway is essential for proteolytic targeting of p27Kip1 by ubiquitination. Proc. Natl. Acad. Sci. USA, 97, 4579-4584.
36. Rivoal, J., Smith, C.R., Moraes, T.F., Turpin, D.H. and Plaxton, W.C. (2002) A method for activity staining after native polyacrylamide gel electrophoresis using a coupled enzyme assay and fluorescence detection: application to the analysis of several glycolytic enzymes. Anal. Biochem. 300, 94-99.
37. Ruuska, S.A., Girke, T., Benning, C. and Ohlrogge, J.B. (2002) Contrapuntal networks of gene expression during Arabidopsis seed filling. Plant Cell, 14, 1191-1206.
38. Schwechheimer, C. and Deng, X.W. (2001) COP9 signalosome revisited: a novel mediator of protein degradation. Trends Cell Biol. 11, 420-426.
39. Shrestha, M.K., Peri, I., Smirnoff, P., Birk, Y. and Golan-Goldhirsh, A. (2002) Jojoba seed meal proteins associated with proteolytic and protease inhibitory activities. J. Agric. Food Chem. 50, 5670-5675.
40. Smith, C.R., Knowles, V.L. and Plaxton, W.C. (2000) Purification and characterization of cytosolic pyruvate kinase from Brassica napus (rapeseed) suspension cell cultures. Eur. J. Bichem. 267, 4477-4485.
41. Smith, A.J., Rinne, R.W. and Seif, R.D. (1989) Phosphoenolpyruvate carboxylase and pyruvate kinase involvement in protein and oil biosynthesis during soybean seed development. Crop Sci. 29, 349-353.
42. Turner, W.L. and Plaxton, W.C. (2000) Purification and characterization of cytosolic pyruvate kinase from banana fruit. Biochem. J. 352, 875-882.
43. 4-form phosphoenolpyruvate carboxylase with specific antibodies raised against a synthetic phosphorylated peptide. Plant J. 21, 17-26.
44. de Virgilio, M., Weninger, H. and Ivessa, N.E. (1998) Ubiquitination is required for the retro-translocation of a short-lived luminal endoplasmic reticulum glycoprotein to the cytosol for degradation by the proteasome. J. Biol. Chem. 273, 9734-9743.
45. Wu, H.B. and Turpin, D.H. (1992) Purification and characterization of pyruvate kinase from the green algae Chlamydomonas reinhardtii. J. Phycol. 28, 472-581.