Purification and characterization of native and recombinant SaPIN2a, a plant sieve element-localized proteinase inhibitor

Plant Physiology and Biochemistry

Volumn 45, Issue 10-11, 2007, Pages 757-766

  Wang, Zhen Yu ^a   Ding, Ling Wen ^a   Ge, Zhi Juan ^a   Wang, Zhaoyu ^a   Wang, Fanghai ^a   Li, Ning ^b   Xu, Zeng Fu ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

Author keywords

Insect; Phloem; Protease inhibitor; Proteinase; Proteolysis; Sieve element; Solanum americanum

Indexed keywords

CHYMOTRYPSIN; CYSTEINE PROTEINASE; PROTEINASE INHIBITOR; RECOMBINANT PROTEIN; SERINE PROTEINASE; SUBTILISIN; TRYPSIN; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; DRUG ANTAGONISM; GENETICS; ISOLATION AND PURIFICATION; KINETICS; METABOLISM; MOLECULAR GENETICS; PH; PHLOEM; PLANT STEM; POLYACRYLAMIDE GEL ELECTROPHORESIS; SEQUENCE ANALYSIS; SOLANUM; TEMPERATURE;

AMINO ACID SEQUENCE; CHYMOTRYPSIN; CYSTEINE ENDOPEPTIDASES; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HYDROGEN-ION CONCENTRATION; KINETICS; MOLECULAR SEQUENCE DATA; PHLOEM; PLANT PROTEINS; PLANT STEMS; PROTEASE INHIBITORS; RECOMBINANT PROTEINS; SEQUENCE ANALYSIS, PROTEIN; SERINE ENDOPEPTIDASES; SOLANUM; SUBTILISIN; TEMPERATURE; TRYPSIN;

ESCHERICHIA COLI; HEXAPODA; SOLANUM; SOLANUM AMERICANUM; SPODOPTERA LITURA; TRICHOPLUSIA NI;

EID: 35048891468     PISSN: 09819428     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plaphy.2007.07.012     Document Type: Article

References (52)

1. Chen X.Y., and Kim J.Y. Transport of macromolecules through plasmodesmata and the phloem. Physiol. Plant. 126 (2006) 560-571
2. Ruiz-Medrano R., Xoconostle-Cazares B., and Lucas W.J. The phloem as a conduit for inter-organ communication. Curr. Opin. Plant Biol. 4 (2001) 202-209
3. Esau K. Anatomy of Seed Plants. second ed. (1977), John Wiley & Sons, New York
4. Sjolund R.D. The phloem sieve element: a river runs through it. Plant Cell 9 (1997) 1137-1146
5. Beers E.P. Programmed cell death during plant growth and development. Cell Death Differ 4 (1997) 649-661
6. Beers E.P., Woffenden B.J., and Zhao C. Plant proteolytic enzymes: possible roles during programmed cell death. Plant Mol. Biol. 44 (2000) 399-415
7. Yoo B.C., Aoki K., Xiang Y., Campbell L.R., Hull R.J., Xoconostle-Cazares B., Monzer J., Lee J.Y., Ullman D.E., and Lucas W.J. Characterization of Cucurbita maxima phloem serphin-1 (CmPS-1). A developmentally regulated elastase inhibitor. J. Biol. Chem. 275 (2000) 35122-35128
8. Schobert C., Baker L., Szederkenyi J., Gromann P., Komor E., Hayashi H., Chino M., and Lucas W.J. Identification of immunologically related proteins in sieve-tube exudate collected from monocotyledonous and dicotyledonous plants. Planta 206 (1998) 245-252
9. Murray C., and Christeller J.T. Purification of a trypsin inhibitor (PFTI) from pumpkin fruit phloem exudate and isolation of putative trypsin and chymotrypsin inhibitor cDNA clones. Biol. Chem. Hoppe. Seyler 376 (1995) 281-287
10. Habu Y., Fukushima H., Sakata Y., Abe H., and Funada R. A gene encoding a major Kunitz proteinase inhibitor of storage organs of winged bean is also expressed in the phloem of stems. Plant Mol. Biol. 32 (1996) 1209-1213
11. Balachandran S., Xiang Y., Schobert C., Thompson G.A., and Lucas W.J. Phloem sap proteins from Cucurbita maxima and Ricinus communis have the capacity to traffic cell to cell through plasmodesmata. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 14150-14155
12. Christeller J.T., Farley P.C., Ramsay R.J., Sullivan P.A., and Laing W.A. Purification, characterization and cloning of an aspartic proteinase inhibitor from squash phloem exudate. Eur. J. Biochem. 254 (1998) 160-167
13. Kehr J., Haebel S., Blechschmidt-Schneider S., Willmitzer L., Steup M., and Fisahn J. Analysis of phloem protein patterns from different organs of Cucurbita maxima Duch. by matrix-assisted laser desorption/ionization time of flight mass spectroscopy combined with sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Planta 207 (1999) 612-619
14. Dannenhoffer J.M., Suhr R.C., and Thompson G.A. Phloem-specific expression of the pumpkin fruit trypsin inhibitor. Planta 212 (2001) 155-162
15. Xu Z.F., Qi W.Q., Ouyang X.Z., Yeung E., and Chye M.L. A proteinase inhibitor II of Solanum americanum is expressed in phloem. Plant Mol. Biol. 47 (2001) 727-738
16. Roberts I.N., Murray P.F., Caputo C.P., Passeron S., and Barneix A.J. Purification and characterization of a subtilisin-like serine protease induced during the senescence of wheat leaves. Physiol. Plant. 118 (2003) 483
17. Vilaine F., Palauqui J.C., Amselem J., Kusiak C., Lemoine R., and Dinant S. Towards deciphering phloem: a transcriptome analysis of the phloem of Apium graveolens. Plant J. 36 (2003) 67-81
18. Walz C., Giavalisco P., Schad M., Juenger M., Klose J., and Kehr J. Proteomics of curcurbit phloem exudate reveals a network of defence proteins. Phytochemistry 65 (2004) 1795-1804
19. Petersen M.L., Hejgaard J., Thompson G.A., and Schulz A. Cucurbit phloem serpins are graft-transmissible and appear to be resistant to turnover in the sieve element-companion cell complex. J. Exp. Bot. 56 (2005) 3111-3120
20. Giavalisco P., Kapitza K., Kolasa A., Buhtz A., and Kehr J. Towards the proteome of Brassica napus phloem sap. Proteomics 6 (2006) 896-909
21. Liu J., Xia K.F., Zhu J.C., Deng Y.G., Huang X.L., Hu B.L., Xu X., and Xu Z.F. The nightshade proteinase inhibitor IIb gene is constitutively expressed in glandular trichomes. Plant Cell Physiol. 47 (2006) 1274-1284
22. Xu Z.F., Teng W.L., and Chye M.L. Inhibition of endogenous trypsin- and chymotrypsin-like activities in transgenic lettuce expressing heterogeneous proteinase inhibitor SaPIN2a. Planta 218 (2004) 623-629
23. Sin S.F., and Chye M.L. Expression of proteinase inhibitor II proteins during floral development in Solanum americanum. Planta 219 (2004) 1010-1022
24. Sin S.F., Yeung E.C., and Chye M.L. Downregulation of Solanum americanum genes encoding proteinase inhibitor II causes defective seed development. Plant J. 45 (2006) 58-70
25. Chye M.L., Sin S.F., Xu Z.F., and Yeung E.C. Serine proteinase inhibitor proteins: exogenous and endogenous functions. In Vitro Cell. Dev. Biol. Plant 42 (2006) 100-108 (109)
26. Hedrick J.L., and Smith A.J. Size and charge isomer separation and estimation of molecular weights of proteins by disc gel electrophoresis. Arch. Biochem. Biophys. 126 (1968) 155-164
27. Z.F. Xu, Proteinase Inhibitor II from Solanum americanum, Molecular Characterization and Potential Use in Generating Insect-resistant Transgenic Vegetables, Ph.D. dissertation, The University of Hong Kong, Hong Kong, 2001, http://sunzi.lib.hku.hk/hkuto/record/B30252453.
28. Beekwilder J., Schipper B., Bakker P., Bosch D., and Jongsma M. Characterization of potato proteinase inhibitor II reactive site mutants. Eur. J. Biochem. 267 (2000) 1975-1984
29. Plunkett G., Senear D.F., Zuroske G., and Ryan C.A. Proteinase inhibitors I and II from leaves of wounded tomato plants: purification and properties. Arch. Biochem. Biophys. 213 (1982) 463-472
30. Odani S., Yokokawa Y., Takeda H., Abe S., and Odani S. The primary structure and characterization of carbohydrate chains of the extracellular glycoprotein proteinase inhibitor from latex of Carica papaya. Eur. J. Biochem. 241 (1996) 77-82
31. Fernanda Troncoso M., Cerda Zolezzi P., Hellman U., and Wolfenstein-Todel C. A novel trypsin inhibitor from Peltophorum dubium seeds, with lectin-like properties, triggers rat lymphoma cell apoptosis. Arch. Biochem. Biophys. 411 (2003) 93-104
32. Coffeen W.C., and Wolpert T.J. Purification and characterization of serine proteases that exhibit caspase-like activity and are associated with programmed cell death in Avena sativa. Plant Cell 16 (2004) 857-873
33. Svensson J., Palva E.T., and Welin B. Purification of recombinant Arabidopsis thaliana dehydrins by metal ion affinity chromatography. Protein Expr. Purif. 20 (2000) 169-178
34. Barrette-Ng I.H., Ng K.K., Cherney M.M., Pearce G., Ghani U., Ryan C.A., and James M.N. Unbound form of tomato inhibitor-II reveals interdomain flexibility and conformational variability in the reactive site loops. J. Biol. Chem. 278 (2003) 31391-31400
35. Barrette-Ng I.H., Ng K.K., Cherney M.M., Pearce G., Ryan C.A., and James M.N. Structural basis of inhibition revealed by a 1:2 complex of the two-headed tomato inhibitor-II and subtilisin Carlsberg. J. Biol. Chem. 278 (2003) 24062-24071
36. Azzouz H., Cherqui A., Campan E.D., Rahbe Y., Duport G., Jouanin L., Kaiser L., and Giordanengo P. Effects of plant protease inhibitors, oryzacystatin I and soybean Bowman-Birk inhibitor, on the aphid Macrosiphum euphorbiae (Homoptera, Aphididae) and its parasitoid Aphelinus abdominalis (Hymenoptera, Aphelinidae). J. Insect Physiol. 51 (2005) 75-86
37. Kehr J. Phloem sap proteins: their identities and potential roles in the interaction between plants and phloem-feeding insects. J. Exp. Bot. 57 (2006) 767-774
38. Vercammen D., Belenghi B., van de Cotte B., Beunens T., Gavigan J.A., De Rycke R., Brackenier A., Inze D., Harris J.L., and Van Breusegem F. Serpin1 of Arabidopsis thaliana is a suicide inhibitor for Metacaspase 9. J. Mol. Biol. 364 (2006) 625-636
39. Atkinson A.H., Heath R.L., Simpson R.J., Clarke A.E., and Anderson M.A. Proteinase inhibitors in Nicotiana alata stigmas are derived from a precursor protein which is processed into five homologous inhibitors. Plant Cell 5 (1993) 203-213
40. Ausloos G.R.J., Proost P., van Damme J., and Vendrig J.C. Proteinase inhibitor II is developmentally regulated in Nicotiana flowers. Physiol. Plant. 94 (1995) 701-707
41. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
42. Hatakeyama T., Kohzaki H., and Yamasaki N. A microassay for proteases using succinylcasein as a substrate. Anal. Biochem. 204 (1992) 181-184
43. Bubnis W.A., and Ofner III C.M. The determination of ε-amino groups in soluble and poorly soluble proteinaceous materials by a spectrophotometric method using trinitrobenzenesulfonic acid. Anal. Biochem. 207 (1992) 129-133
44. Rickauer M., Fournier J., and Esquerre-Tugaye M. Induction of proteinase inhibitors in tobacco cell suspension culture by elicitors of Phytophthora parasitica var. nicotianae. Plant Physiol. 90 (1989) 1065-1070
45. Yasuda Y., Kageyama T., Akamine A., Shibata M., Kominami E., Uchiyama Y., and Yamamoto K. Characterization of new fluorogenic substrates for the rapid and sensitive assay of cathepsin E and cathepsin D. J. Biochem. (Tokyo) 125 (1999) 1137-1143
46. Mitsudo K., Jayakumar A., Henderson Y., Frederick M.J., Kang Y., Wang M., El-Naggar A.K., and Clayman G.L. Inhibition of serine proteinases plasmin, trypsin, subtilisin A, cathepsin G, and elastase by LEKTI: a kinetic analysis. Biochemistry 42 (2003) 3874-3881
47. Sambrook J., Fritsch E.F., and Maniatis T. Molecular Cloning: A Laboratory Manual. second ed. (1989), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
48. Bryant J., Green T.R., Gurusaddaiah T., and Ryan C.A. Proteinase inhibitor II from potatoes: isolation and characterization of its protomer components. Biochemistry 15 (1976) 3418-3424
49. Altpeter F., Diaz I., McAuslane H., Gaddour K., Carbonero P., and Vasil I.K. Increased insect resistance in transgenic wheat stably expressing trypsin inhibitor CMe. Mol. Breeding 5 (1999) 53-63
50. Burgess E.P., Lovei G.L., Malone L.A., Nielsen I.W., Gatehouse H.S., and Christeller J.T. Prey-mediated effects of the protease inhibitor aprotinin on the predatory carabid beetle Nebria brevicollis. J. Insect Physiol. 48 (2002) 1093-1101
51. Alfonso-Rubi J., Ortego F., Castanera P., Carbonero P., and Diaz I. Transgenic expression of trypsin inhibitor CMe from barley in indica and japonica rice, confers resistance to the rice weevil Sitophilus oryzae. Transgenic Res. 12 (2003) 23-31
52. J. Xie, X.Z. Ouyang, K.F. Xia, Y.F. Huang, W.B. Pan, Y.P. Cai, X. Xu, B. Li, Z.F. Xu, Chloroplast-like organelles were found in enucleate sieve elements of transgenic plants overexpressing a proteinase inhibitor, Biosci. Biotechnol. Biochem., in press.