Proteolysis of the peanut allergen Ara h 1 by an endogenous aspartic protease

Plant Physiology and Biochemistry

Volumn 96, Issue , 2015, Pages 301-310

  Wilson, Karl A ^a   Tan Wilson, Anna ^a  

^a BINGHAMTON UNIVERSITY   (United States)

Author keywords

7S globulin storage protein; Allergen; Ara h 1; Aspartic protease; Germination; Peanut; Proteolysis

Indexed keywords

ARA H 1 PROTEIN, ARACHIS HYPOGAEA; ASPARTIC PROTEINASE; GLYCOPROTEIN; PLANT ANTIGEN; PLANT PROTEIN;

AMINO ACID SEQUENCE; ARACHIS; CHEMISTRY; CONFOCAL MICROSCOPY; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; PH; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN DEGRADATION; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANTIGENS, PLANT; ARACHIS; ASPARTIC ACID PROTEASES; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GLYCOPROTEINS; HYDROGEN-ION CONCENTRATION; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; PLANT PROTEINS; PROTEOLYSIS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84941281887     PISSN: 09819428     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plaphy.2015.08.008     Document Type: Article

References (40)

1. Bleukx W., Brijs K., Torrekens S., Van Leuven F., Delcour J.A. Specificity of a wheat gluten aspartic proteinase. Biochim. Biophys. Acta 1998, 1387:317-324. 10.1016/S0167-4838(98)00146-0.
2. Boyd P.M., Barnaby N., Tan-Wilson A., Wilson K.A. Cleavage specificity of the subtilisin-like protease C1 from soybean. Biochim. Biophys. Acta 2002, 1596:269-282. 10.1016/S0167-4838(02)00228-5.
3. Cabanillas B., Pedrosa M.M., Rodriguez J., Muzquiz M., Maleki S.J., Cuadrado C., Burbano C., Crespo J.F. Influence of enzymatic hydrolysis on the allergenicity of roasted peanut protein extract. Int. Arch. Allergy Immunol. 2012, 157:41-50. 10.1159/000324681.
4. Chassaigne H., Tregoat V., Norgaard J.V., Maleki S.J., van Hengel A.J. Resolution and identification of major peanut allergens using a combination of fluorescence two-dimensional differential gel electrophoresis, Western blotting and Q-TOF mass spectrometry. J. Proteom. 2009, 72:511-526. 10.1016/j.jprot.2009.02.002.
5. Chruszcz M., Maleki S.J., Majorek K.A., Demas M., Bublin M., Solberg R., Hurlburt B.K., Ruan S., Mattison C.P., Breiteneder H., Minor W. Structural and immunologic characterization of Ara h 1, a major peanut allergen. J. Biol. Chem. 2011, 286:39318-39327. 10.1074/jbc.M111.270132.
6. Frazão C., Bento I., Costa J., Soares C.M., Veríssimo P., Faro C., Pires E., Cooper J., 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. 1999, 274:27694-27701. 10.1074/jbc.274.39.27694.
7. Gatehouse J.A., Lycett G.W., Delauney A.J., Croy R.R., Boulter D. Sequence specificity of the post-translational proteolytic cleavage of vicilin, a seed storage protein of pea (Pisum sativum L.). Biochem. J. 1983, 212:427-432.
8. He F., Huang F., Wilson K.A., Tan-Wilson A. Protein storage vacuole acidification as a control of storage protein mobilization in soybeans. J. Exp. Bot. 2007, 58:1059-1070. 10.1093/jxb/erl267.
9. Kim J., Lee J., Seo W.H., Han Y., Ahn K., Lee S.I. Changes in major peanut allergens under different pH conditions. Allergy Asthma Immunol. Res. 2012, 4:157-160. 10.4168/aair.2012.4.3.157.
10. Kolarich D., Altmann F. N-Glycan analysis by matrix-assisted laser desorption/ionization mass spectrometry of electrophoretically separated nonmammalian proteins: application to peanut allergen Ara h 1 and olive pollen allergen Ole e 1. Anal. Biochem. 2000, 285:64-75. 10.1006/abio.2000.4737.
11. Kulkarni A., Rao M. Differential elicitation of an aspartic protease inhibitor: regulation of endogenous protease and initial events in germination in seeds of Vigna radiata. Peptides 2009, 30:2118-2126. 10.1016/j.peptides.2009.08.024.
12. Magni C., Sessa F., Tedeschi G., Negri A., Scarafoni A., Consonni A., Duranti M. Identification in lupin seed of a serine-endopeptidase activity cleaving between twin arginine pairs and causing limited proteolysis of seed storage proteins. Mol. Plant 2012, 5:1011-1019. 10.1093/mp/ssr116.
13. Mahaboob Basha S.M., Cherry J.P. Proteolytic enzyme activity and storage protein degradation in cotyledons of germinating peanut (Arachis hypogaea L.) seeds. J. Agric. Food Chem. 1978, 26:229-234. 10.1021/jf60215a045.
14. Maruyama Y., Maruyama N., Mikami B., Utsumi S. Structure of the core region of the soybean beta-conglycinin alpha' subunit. Acta Crystallogr. D Biol. Crystallogr. 2004, D60:289-297. 10.1107/S0907444903027367.
15. Mazorra-Manzano M.A., Tanaka T., Dee D.R., Yada R.Y. Structure-function characterization of the recombinant aspartic proteinase A1 from Arabidopsis thaliana. Phytochemistry 2010, 71:515-523. 10.1016/j.phytochem.2009.12.005.
16. McIlvaine T.C. A buffer solution for colorimetric comparison. J. Biol. Chem. 1921, 49:183-186.
17. Millot C., Millot J.M., Morjani H., Desplaces A., Manfait M. Characterization of acidic vesicles in multidrug-resistant and sensitive cancer cells by acridine orange staining and confocal microspectrofluorometry. J. Histochem. Cytochem. 1997, 45:1255-1264. 10.1177/002215549704500909.
18. Moreno F.J. Gastrointestinal digestion of food allergens: effect on their allergenicity. Biomed. Pharmacother. 2007, 61:50-60. 10.1016/j.biopha.2006.10.005.
19. Muntz K., Belozersky M.A., Dunaevsky Y.E., Schlereth A., Tiedemann J. Stored proteinases and the initiation of storage protein mobilization in seeds during germination and seedling growth. J. Exp. Bot. 2001, 52:1741-1752. 10.1093/jexbot/52.362.1741.
20. Mutlu A., Chen X., Reddy S.M., Gal S. The aspartic proteinase is expressed in Arabidopsis thaliana seeds and localized in the protein bodies. Seed Sci. Res. 1999, 9:75-84. 10.1016/S0031-9422(97)00834-0.
21. Pan D., Hill A.P., Kashou A., Wilson K.A., Tan-Wilson A. Electrophoretic transfer protein zymography. Anal. Biochem. 2011, 411:277-283. 10.1016/j.ab.2011.01.015.
22. Park H., Yamanaka N., Mikkonen A., Kusakabe I., Kobayashi H. Purification and characterization of aspartic proteinase from sunflower seeds. Biosci. Biotechnol. Biochem. 2000, 64:931-939. 10.1271/bbb.64.931.
23. Pereira C.S., da Costa D.S., Pereira S., de Moura Nogueira F., Albuquerque P.M., Teixeira J., Faro C., Pissarra J. Cardosins in postembryonic development of cardoon: towards an elucidation of the biological function of plant aspartic proteinases. Protoplasma 2008, 232:203-213. 10.1007/s00709-008-0288-9.
24. Piersma S.R., Gaspari M., Hefle S.L., Koppelman S.J. Proteolytic processing of the peanut allergen Ara h 3. Mol. Nutr. Food Res. 2005, 49:744-755. 10.1002/mnfr.200500020.
25. Qi X., Chen R., Wilson K.A., Tan-Wilson A.L. Characterization of a soybean beta-conglycinin-degrading protease cleavage site. Plant Physiol. 1994, 104:127-133. 10.1104/pp.104.1.127.
26. Salvador S.M., Novo C., Domingos A. Evaluation of the presence of aspartic proteases from Centaurea calcitrapa during seed germination. Enzyme Microb. Technol. 2006, 38:893-898. 10.1016/j.enzmictec.2005.06.025.
27. Santos C.N., Alves M.M., Bento I.T., Ferreira R.B. Missing pieces in protein deposition and mobilization inside legume seed storage vacuoles: calcium and magnesium ions. Seed Sci. Res. 2012, 22:249-258. 10.1017/S0960258512000177.
28. Senyuk V., Rotari V., Becker C., Zakharov A., Horstmann C., Müntz K., Vaintraub I. Does an asparaginyl-specific cysteine endopeptidase trigger phaseolin degradation in cotyledons of kidney bean seedlings?. Eur. J. Biochem. 1998, 258:546-558. 10.1016/S0167-4838(00)00277-6.
29. Seo S., Tan-Wilson A., Wilson K.A. Protease C2, a cysteine endopeptidase involved in the continuing mobilization of soybean beta-conglycinin seed proteins. Biochim. Biophys. Acta 2001, 1545:192-206. 10.1016/S0167-4838(00)00277-6.
30. Shutov A.D., Baumlein H., Blattner F.R., Müntz K. Storage and mobilization as antagonistic functional constraints on seed storage globulin evolution. J. Exp. Bot. 2003, 54:1645-1654. 10.1093/jxb/erg165.
31. Shutov A.D., Kakhovskaya I.A., Bastrygina A.S., Bulmaga V.P., Horstmann C., Müntz K. Limited proteolysis of beta-conglycinin and glycinin, the 7S and 11S storage globulins from soybean [Glycine max (L.) Merr.]. Structural and evolutionary implications. Eur. J. Biochem. 1996, 241:221-228. 10.1111/j.1432-1033.1996.0221t.x.
32. Simoes I., Faro C. Structure and function of plant aspartic proteinases. Eur. J. Biochem. 2004, 271:2067-2075. 10.1111/j.1432-1033.2004.04136.x.
33. Szecsi P.B. The aspartic proteases. Scand. J. Clin. Lab. Invest. Suppl. 1992, 210:5-22.
34. Tan-Wilson A., Bandak B., Prabu-Jeyabalan M. The PA domain is crucial for determining optimum substrate length for soybean protease C1: structure and kinetics correlate with molecular function. Plant Physiol. Biochem. 2012, 53:27-32. 10.1016/j.plaphy.2012.01.005.
35. Tan-Wilson A.L., Liu X., Chen R., Qi X., Wilson K.A. An acidic amino acid-specific protease from germinating soybeans. Phytochemistry 1996, 42:313-319. 10.1016/0031-9422(95)00896-9.
36. Tan-Wilson A.L., Wilson K.A. Mobilization of seed protein reserves. Physiol. Plant 2012, 145:140-153. 10.1111/j.1399-3054.2011.01535.x.
37. Timotijevic G.S., Radovic S.R., Maksimovic V.R. Characterization of an aspartic proteinase activity in buckwheat (Fagopyrum esculentum Moench) seeds. J. Agric. Food Chem. 2003, 51:2100-2104. 10.1021/jf026043b.
38. Voigt J., Biehl B., Voigt G., Heinrichs H. Cocoa-specific aroma precursors are generated by proteolytic digestion of the vicilin-like globulin of cocoa seeds. Food Chem. 1994, 50:177-184. 10.1016/0308-8146(94)90117-1.
39. Wichers H.J., De Beijer T., Savelkoul H.F., Van Amerongen A. The major peanut allergen Ara h 1 and its cleaved-off N-terminal peptide; possible implications for peanut allergen detection. J. Agric. Food Chem. 2004, 52:4903-4907. 10.1021/jf049697o.
40. Zakharov A., Carchilan M., Stepurina T., Rotari V., Wilson K., Vaintraub I. A comparative study of the role of the major proteinases of germinated common bean (Phaseolus vulgaris L.) and soybean (Glycine max (L.) Merrill) seeds in the degradation of their storage proteins. J. Exp. Bot. 2004, 55:2241-2249. 10.1093/jxb/erh247.