Structure-function characterization of the recombinant aspartic proteinase A1 from Arabidopsis thaliana

Phytochemistry

Volumn 71, Issue 5-6, 2010, Pages 515-523

  Mazorra Manzano, Miguel A ^a   Tanaka, Takuji ^b   Dee, Derek R ^c   Yada, Rickey Y ^c  

^a CENTRO DE INVESTIGACIÓN EN ALIMENTACIÓN Y DESARROLLO   (Mexico)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

^c UNIVERSITY OF GUELPH   (Canada)

Author keywords

Arabidopsis thaliana; Cruciferae; pH stability; Plant aspartic proteinase; Plant specific insert; Proteases; Substrate specificity; Thermal stability

Indexed keywords

ARABIDOPSIS PROTEIN; ASPARTIC PROTEINASE; ASPARTIC PROTEINASE A; ASPARTIC PROTEINASE A1 PROTEIN, ARABIDOPSIS; RECOMBINANT PROTEIN;

ARABIDOPSIS; ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; CIRCULAR DICHROISM; ENZYME SPECIFICITY; ENZYMOLOGY; HYDROLYSIS; PH; PROTEIN CONFORMATION; STRUCTURE ACTIVITY RELATION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; ASPARTIC ACID ENDOPEPTIDASES; ASPARTIC ACID PROTEASES; CIRCULAR DICHROISM; HYDROGEN-ION CONCENTRATION; HYDROLYSIS; MODELS, MOLECULAR; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BRASSICACEAE; MAMMALIA;

EID: 77949618648     PISSN: 00319422     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.phytochem.2009.12.005     Document Type: Article

References (59)

1. Ahn V.E., Leyko P., Alattia J., Chen L., and Privé G.G. Crystal structures of saposins A and C. Protein Sci. 15 (2006) 1849-1857
2. Arnold K., Bordoli L., Kopp J., and Schwede T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22 (2006) 195-201
3. Asakura T., Asakura T., Matsumoto I., Funaki J., Arai S., and Abe K. The plant aspartic proteinase-specific polypeptide insert is not directly related to the activity of oryzasin. Eur. J. Biochem. 267 (2000) 5115-5122
4. Athauda S.B., Matsumoto K., Rajapakshe S., Kuribayashi M., Kojima M., Kubomura-Yoshida N., Iwamatsu A., Shibata C., and Inoue H. Enzymic and structural characterization of nepenthesin, a unique member of a novel subfamily of aspartic proteinases. Biochem. J. 381 (2004) 295-306
5. Bleukx W., and Delcour J.A. A second aspartic proteinase associated with wheat gluten. J. Cereal Sci. 32 (2000) 31-42
6. Bleukx W., Brijs K., Torrekens S., Van-Leuven F., and Delcour J.A. Specificity of a wheat gluten aspartic proteinase. Biochim. Biophys. Acta 1387 (1998) 317-324
7. Brodelius M., Hiraiwa M., Marttila S., Karadaghi S.A., Picaud S., and Brodelius P.E. Immunolocalization of the saposin-like insert of plant aspartic proteinases exhibiting saposin C activity. Expression in young flower tissues and in barley seeds. Physiol. Plant. 125 (2005) 405-418
8. Bryksa B.C., Tanaka T., and Yada R.Y. N-terminal modifications increase the neutral-pH stability of pepsin. Biochemistry 42 (2003) 13331-13338
9. Carter C., Pan S., Zouhar J., Avila E.L., Girke T., and Raikhelet N.T. The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unexpected proteins. Plant Cell 16 (2004) 3285-3303
10. Castanheira P., Samyn B., Sergeant K., Clemente J.C., Dunn B.M., Pires E., Van-Beeumen J., and Faro C. Activation, proteolytic processing, and peptide specificity of recombinant cardosin A. J. Biol. Chem. 280 (2005) 13047-13054
11. Chen X., Pfeil J.E., and Gal S. The three typical aspartic proteinase genes of Arabidopsis thaliana are differentially expressed. Eur. J. Biochem. 269 (2002) 4675-4684
12. Davies D.R. The structure and function of the aspartic proteinases. Ann. Rev. Biophys. Biophys. Chem. 19 (1990) 189-215
13. Duarte P., Figueiredo R., Pereira S., and Pissarra J. Structural characterization of the stigma-style complex of Cynara cardunculus (Asteraceae) and immunolocalization of cardosins A and B during floral development. Can. J. Bot. 84 (2006) 737-749
14. Egas C., Lavoura N., Resende R., Brito R.M.M., Pires E., De Lima M.C.P., and Faro C. The saposin-like domain of the plant aspartic proteinase precursor is a potent inducer of vesicle leakage. J. Biol. Chem. 275 (2000) 38190-38196
15. Faro C., and Gal S. Aspartic proteinase content of the Arabidopsis genome. Curr. Protein Pept. Sci. 6 (2005) 493-500
16. Frazao C., Bento I., Costa J., Soares C.M., Verissimo P., Faro C., Pires E., Cooper J., and Carrondo M.A. Crystal structure of cardosin A, a glycosylated and Arg-Gly-Asp-containing aspartic proteinase from the flowers of Cynara cardunculus L. J. Biol. Chem. 274 (1999) 27694-27701
17. Glathe S., Kervinen J., Nimtz M., Li G.H., Tobin G.J., Copeland T.D., Ashford D.A., Wlodawer A., and Costa J. Transport and activation of the vacuolar aspartic proteinase phytepsin in barley (Hordeum vulgare L.). J. Biol. Chem. 273 (1998) 31230-31236
18. Guevara M.G., Oliva C.R., Huarte M., and Daleo G.R. An aspartic protease with antimicrobial activity is induced after infection and wounding in intercellular fluids of potato tubers. Eur. J. Plant Pathol. 108 (2002) 131-137
19. Guevara M.G., Verissimo P., Pires E., Faro C., and Daleo G.R. Potato aspartic proteases: induction, antimicrobial activity and substrate specificity. J. Plant Pathol. 86 (2004) 233-238
20. Guevara M.G., Almeida C., Mendieta J.R., Faro C.J., Verissimo P., Pires E.V., and Daleo G.R. Molecular cloning of a potato leaf cDNA encoding an aspartic protease (StAsp) and its expression after P. infestans infection. Plant Physiol. Biochem. 43 (2005) 882-889
21. Hayes M.G., Hurley M.J., Larsen L.B., Heegaard C.W., Magboul A.A.A., Oliveira J.C., McSweeney P.L.H., and Kelly A.L. Thermal inactivation kinetics of bovine cathepsin D. J. Dairy Res. 68 (2001) 267-276
22. Humphrey W., Dalke A., and Schulten K. VMD: visual molecular dynamics. J. Mol. Graphics 14 (1996) 33-38
23. Kale L., Skeel R., Bhandarkar M., Brunner R., Gursoy A., Krawetz N., Phillips J., Shinozaki A., Varadarajan K., and Schulten K. NAMD2: greater scalability for parallel molecular dynamics. J. Comput. Phys. 151 (1999) 283-312
24. Kelly S.M., Jess T.J., and Price N.C. How to study proteins by circular dichroism. Biochim. Biophys. Acta 1751 (2005) 119-139
25. Kervinen J., Sarkkinen P., Kalkkinen N., Mikola L., and Saarma M. Hydrolytic specificity of the barley grain aspartic proteinase. Phytochemistry 32 (1993) 799-803
26. Kervinen J., Tobin G.J., Costa J., Waugh D.S., Wlodawer A., and Zdanov A. Crystal structure of plant aspartic proteinase prophytepsin: inactivation and vacuolar targeting. EMBO J. 18 (1999) 3947-3955
27. Knight C.G. Active-site titration of peptidases. Methods Enzymol. 248 (1995) 85-101
28. Lah T., Drobnickosorok M., Turk V., and Pain R.H. Conformation, structure and activation of bovine cathepsin-D - unfolding and refolding studies. Biochem. J. 218 (1984) 601-608
29. Lee A.Y., Gulnik S.V., and Erickson J.W. Conformational switching in an aspartic proteinase. Nat. Struct. Biol. 5 (1998) 866-871
30. Lindman S., Wei-Feng X., Szczepankiewicz O., Bauer M.C., Nilsson H., and Linse S. Salting the charged surface: pH and salt dependence of protein G B1 stability. Biophys. J. 90 (2006) 2911-2921
31. Llorente B.E., Brutti C.B., and Caffini N.O. Purification and characterization of a milk-clotting aspartic proteinase from globe artichoke (Cynara scolymus L.). J. Agric. Food Chem. 52 (2004) 8182-8189
32. Mazorra-Manzano M.A., and Yada R.Y. Expression and characterization of the recombinant aspartic proteinase A1 from Arabidopsis thaliana. Phytochemistry 69 (2008) 2439-2448
33. Mutlu A., and Gal S. Plant aspartic proteinases: enzymes on the way to a function. Physiol. Plant. 105 (1999) 569-576
34. Mutlu A., Pfeil J.E., and Gal S. A probarley lectin processing enzyme purified from Arabidopsis thaliana seeds. Phytochemistry 47 (1998) 1453-1459
35. Mutlu A., Chen X., Reddy S.M., and Gal S. The aspartic proteinase is expressed in Arabidopsis thaliana seeds and localized in the protein bodies. Seed Sci. Res. 9 (1999) 75-84
36. Otegui M.S., Herder R., Schulze J., Jung R., and Staehelin L.A. The proteolytic processing of seed storage proteins in Arabidopsis embryo cells starts in the multivesicular bodies. Plant Cell 18 (2006) 2567-2581
37. Pace C.N., Alston R.W., and Shaw K.L. Charge-charge interactions influence the denatured state ensemble and contribute to protein stability. Protein Sci. 9 (2000) 1395-1398
38. Park H., Yamanaka N., Mikkonen A., Kusakabe I., and Kobayashi H. Purification and characterization of aspartic proteinase from sunflower seeds. Biosci. Biotech. Biochem. 64 (2000) 931-939
39. Payie K.G., Tanaka T., Gal S., and Yada R.Y. Construction, expression and characterization of a chimaeric mammalian-plant aspartic proteinase. Biochem. J. 372 (2003) 671-678
40. Pereira C.S., Soares-da-Costa D., Pereira S., de-Moura-Nogueira F., Albuquerque P.M., Teixeira J., Faro C., and Pissarra J. Cardosins in postembryonic development of cardoon: towards an elucidation of the biological function of plant aspartic proteinases. Protoplasma 323 (2008) 203-213
41. Pina D.G., Oliveira C.S., Sarmento A.C., Barros M., Pires E., Zhadan G.G., Villar E., Gavilanes F., and Shnyrov V.L. Thermostability of cardosin A from Cynara cardunculus L. Thermochim. Acta 402 (2003) 123-134
42. Privalov P.L., Mateo P.L., Khechinashvili N.N., Stepanov V.M., and Revina L.P. Comparative thermodynamic study of pepsinogen and pepsin structure. J. Mol. Biol. 152 (1981) 445-464
43. Ramalho-Santos M., Verissimo P., Cortes L., Samyn B., Beeumen J.V., Pires E., and Faro C. Identification and proteolytic processing of procardosin A. Eur. J. Biochem. 255 (1998) 133-138
44. Richter C., Tanaka T., Koseki T., and Yada R.Y. Contribution of a prosegment lysine residue to the function and structure of porcine pepsinogen A and its active form pepsin A. Eur. J. Biol. 261 (1999) 746-752
45. Rodrigo I., Vera P., and Van-Loon L.C. Degradation of tobacco pathogenesis-related proteins. Evidence for conserved mechanisms of degradation of pathogenesis-related proteins in plants. Plant Physiol. 95 (1991) 616-622
46. Runeberg-Roos P., Kervinen J., Kovaleva V., Raikhel N.V., and Gal S. The aspartic proteinase of barley is a vacuolar enzyme that processes probarley lectin in vitro. Plant Phisiol. 105 (1994) 321-329
47. Senthilkumar S., Ramasamy D., and Subramanian S. Isolation and partial characterization of milk-clotting aspartic proteases from Streblus asper. Food Sci. Technol. Int. 12 (2006) 103-109
48. Sidrach L., García-Canovas F., Tudela J., and Rodríguez-Lopez N.J. Purification of cynarases from artichoke (Cynara scolymus L.): enzymatic properties of cynarase A. Phytochemistry 66 (2005) 41-49
49. Simoes I., and Faro C. Structure and function of plant aspartic proteinases. Eur. J. Biochem. 271 (2004) 2067-2075
50. Simoes I., Faro R., Bur D., and Faro C. Characterization of recombinant CDR1, an Arabidopsis aspartic proteinase involved in disease resistance. J. Biol. Chem. 282 (2007) 31358-31365
51. Stigter D., and Dill K.A. Charge effects on folded and unfolded proteins. Biochemistry 29 (1990) 1262-1271
52. Tamura T., Terauchi K., Kiyosaki T., Asakura T., Funaki J., Matsumoto I., Misaka T., and Abe K. Differential expression of wheat aspartic proteinases, WAP1 and WAP2, in germinating and maturing seeds. J. Plant Physiol. 164 (2007) 470-477
53. Tanaka T., and Yada R.Y. Expression of soluble cloned porcine pepsinogen A in Escherichia coli. Biochem. J. 315 (1996) 443-446
54. Terauchi K., Asakura T., Ueda H., Tamura T., Tamura K., Matsumoto I., Misaka T., Hara-Nishimura I., and Abe K. Plant-specific insertions in the soybean aspartic proteinases, soyAP1 and soyAP2, perform different functions of vacuolar targeting. J. Plant Physiol. 163 (2006) 856-862
55. Tormakangas K., Hadlington J.L., Piml P., Hillmer S., Brandizzi F., Teeri T.H., and Denecke J. A vacuolar sorting domain may also influence the way in which proteins leave the endoplasmic reticulum. Plant Cell 13 (2001) 2021-2032
56. Verissimo P., Esteves C., Faro C., and Pires E. The vegetable rennet of Cynara cardunculus L. contains two proteinases with chymosin and pepsin-like specificities. Biotechnol. Lett. 17 (1995) 621-626
57. Waring A.J., Chen Y., Faull K.F., Stevens R., Sherman M.A., and Fluharty A.L. Porcine cerebroside sulfate activator (saposin B) secondary structure: CD, FTIR, and NMR studies. Mol. Genet. Metab. 63 (1998) 14-25
58. White P.C., Cordeiro M.C., Arnold D., Brodelius P.E., and Kay J. Processing, activity, and inhibition of recombinant cyprosin, an aspartic proteinase from cardoon (Cynara cardunculus). J. Biol. Chem. 274 (1999) 16685-16693
59. Whitmore L., and Wallace B.A. DICHROWEB: an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucl. Acids Res. 32 (2004) W668-W673