Nicotiana benthamiana cathepsin B displays distinct enzymatic features which differ from its human relative and aleurain-like protease

Biochimie

Volumn 122, Issue , 2016, Pages 119-125

  Niemer, Melanie ^a   Mehofer, Ulrich ^a   Verdianz, Maria ^a   Porodko, Andreas ^a   Schähs, Philipp ^a   Kracher, Daniel ^a   Lenarcic, Brigita ^b   Novinec, Marko ^b   Mach, Lukas ^a  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^b UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

Antibody; Cathepsin; Cysteine protease; Expression platform; Plant; Proteolysis

Indexed keywords

ALEURAIN LIKE PROTEASE; CATHEPSIN B; CATHEPSIN H; PEPTIDASE; PEPTIDYLDIPEPTIDASE; PROTEINASE; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; ALEURAIN; CYSTEINE PROTEINASE; ENZYME PRECURSOR; PEPTIDE HYDROLASE; PLANT PROTEIN;

ANIMAL CELL; ARTICLE; CATALYSIS; CONTROLLED STUDY; DOWN REGULATION; HETEROLOGOUS EXPRESSION; NICOTIANA BENTHAMIANA; NONHUMAN; PH; PROTEIN EXPRESSION; AMINO ACID SEQUENCE; ANIMAL; BIOCATALYSIS; ENZYME SPECIFICITY; ENZYMOLOGY; GENETICS; HUMAN; KINETICS; METABOLISM; PROTEIN DEGRADATION; SF9 CELL LINE; SPODOPTERA; TOBACCO; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; BIOCATALYSIS; BLOTTING, WESTERN; CATHEPSIN B; CYSTEINE ENDOPEPTIDASES; ENZYME PRECURSORS; HUMANS; HYDROGEN-ION CONCENTRATION; KINETICS; PEPTIDE HYDROLASES; PLANT PROTEINS; PROTEOLYSIS; RECOMBINANT PROTEINS; SF9 CELLS; SPODOPTERA; SUBSTRATE SPECIFICITY; TOBACCO;

EID: 84957840951     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2015.06.017     Document Type: Article

References (48)

1. A. Giritch, S. Marillonnet, C. Engler, G. van Eldik, J. Botterman, V. Klimyuk, and Y. Gleba Rapid high-yield expression of full-size IgG antibodies in plants coinfected with noncompeting viral vectors Proc. Natl. Acad. Sci. U. S. A. 103 2006 14701 14706
2. R. Strasser, A. Castilho, J. Stadlmann, R. Kunert, H. Quendler, P. Gattinger, J. Jez, T. Rademacher, F. Altmann, L. Mach, and H. Steinkellner Improved virus neutralization by plant-produced anti-HIV antibodies with a homogeneous beta1,4-galactosylated N-glycan profile J. Biol. Chem. 284 2009 20479 20485
3. R. Strasser, F. Altmann, and H. Steinkellner Controlled glycosylation of plant-produced recombinant proteins Curr. Opin. Biotechnol. 30 2014 95 100
4. X. Qiu, G. Wong, J. Audet, A. Bello, L. Fernando, J.B. Alimonti, H. Fausther-Bovendo, H. Wei, J. Aviles, E. Hiatt, A. Johnson, J. Morton, K. Swope, O. Bohorov, N. Bohorova, C. Goodman, D. Kim, M.H. Pauly, J. Velasco, J. Pettitt, G.G. Olinger, K. Whaley, B. Xu, J.E. Strong, L. Zeitlin, and G.P. Kobinger Reversion of advanced Ebola virus disease in nonhuman primates with ZMapp Nature 514 2014 47 53
5. M.E. Villani, B. Morgun, P. Brunetti, C. Marusic, R. Lombardi, I. Pisoni, C. Bacci, A. Desiderio, E. Benvenuto, and M. Donini Plant pharming of a full-sized, tumour-targeting antibody using different expression strategies Plant Biotechnol. J. 7 2009 59 72
6. B. De Muynck, C. Navarre, and M. Boutry Production of antibodies in plants: status after twenty years Plant Biotechnol. J. 8 2010 529 563
7. R. Lombardi, M.E. Villani, M. Di Carli, P. Brunetti, E. Benvenuto, and M. Donini Optimisation of the purification process of a tumour-targeting antibody produced in N. benthamiana using vacuum-agroinfiltration Transgenic Res. 19 2010 1083 1097
8. V.K. Hehle, M.J. Paul, P.M. Drake, J.K. Ma, and C.J. van Dolleweerd Antibody degradation in tobacco plants: a predominantly apoplastic process BMC Biotechnol. 11 2011 128
9. C. Goulet, M. Khalf, F. Sainsbury, M.A. D'Aoust, and D. Michaud A protease activity-depleted environment for heterologous proteins migrating towards the leaf cell apoplast Plant Biotechnol. J. 10 2012 83 94
10. M. Niemer, U. Mehofer, J.A. Torres Acosta, M. Verdianz, T. Henkel, A. Loos, R. Strasser, D. Maresch, T. Rademacher, H. Steinkellner, and L. Mach The human anti-HIV antibodies 2F5, 2G12, and PG9 differ in their susceptibility to proteolytic degradation: down-regulation of endogenous serine and cysteine proteinase activities could improve antibody production in plant-based expression platforms Biotechnol. J. 9 2014 493 500
11. M.K. Mandal, R. Fischer, S. Schillberg, and A. Schiermeyer Inhibition of protease activity by antisense RNA improves recombinant protein production in Nicotiana tabacum cv. Bright Yellow 2 (BY-2) suspension cells Biotechnol. J. 9 2014 1065 1073
12. V.K. Hehle, R. Lombardi, C.J. van Dolleweerd, M.J. Paul, P. Di Micco, V. Morea, E. Benvenuto, M. Donini, and J.K. Ma Site-specific proteolytic degradation of IgG monoclonal antibodies expressed in tobacco plants Plant Biotechnol. J. 13 2015 235 245
13. M. Martinez, I. Cambra, P. Gonzalez-Melendi, M.E. Santamaria, and I. Diaz C1A cysteine-proteases and their inhibitors in plants Physiol. Plant 145 2012 85 94
14. K.H. Richau, F. Kaschani, M. Verdoes, T.C. Pansuriya, S. Niessen, K. Stuber, T. Colby, H.S. Overkleeft, M. Bogyo, and R.A. Van der Hoorn Subclassification and biochemical analysis of plant papain-like cysteine proteases displays subfamily-specific characteristics Plant Physiol. 158 2012 1583 1599
15. V. Turk, V. Stoka, O. Vasiljeva, M. Renko, T. Sun, B. Turk, and D. Turk Cysteine cathepsins: from structure, function and regulation to new frontiers Biochim. Biophys. Acta 1824 2012 68 88
16. L. Hao, T. Hsiang, and P.H. Goodwin Role of two cysteine proteinases in the susceptible response of Nicotiana benthamiana to Colletotrichum destructivum and the hypersensitive response to Pseudomonas syringae pv. tomato Plant Sci. 170 2006 1001 1009
17. E.M. Gilroy, I. Hein, R. van der Hoorn, P.C. Boevink, E. Venter, H. McLellan, F. Kaffarnik, K. Hrubikova, J. Shaw, M. Holeva, E.C. Lopez, O. Borras-Hidalgo, L. Pritchard, G.J. Loake, C. Lacomme, and P.R. Birch Involvement of cathepsin B in the plant disease resistance hypersensitive response Plant J. 52 2007 1 13
18. R.A. van der Hoorn, and M. Kaiser Probes for activity-based profiling of plant proteases Physiol. Plant 145 2012 18 27
19. C. Gu, M. Shabab, R. Strasser, P.J. Wolters, T. Shindo, M. Niemer, F. Kaschani, L. Mach, and R.A. van der Hoorn Post-translational regulation and trafficking of the granulin-containing protease RD21 of Arabidopsis thaliana PLoS One 7 2012 e32422
20. E. Kowalewski-Nimmerfall, P. Schahs, D. Maresch, D. Rendic, H. Kramer, and L. Mach Drosophila melanogaster cellular repressor of E1A-stimulated genes is a lysosomal protein essential for fly development Biochim. Biophys. Acta 1843 2014 2900 2912
21. A. Bombarely, H.G. Rosli, J. Vrebalov, P. Moffett, L.A. Mueller, and G.B. Martin A draft genome sequence of Nicotiana benthamiana to enhance molecular plant-microbe biology research Mol. Plant Microbe Interact. 25 2012 1523 1530
22. P. Schähs, P. Weidinger, O.C. Probst, B. Svoboda, J. Stadlmann, H. Beug, T. Waerner, and L. Mach Cellular repressor of E1A-stimulated genes is a bona fide lysosomal protein which undergoes proteolytic maturation during its biosynthesis Exp. Cell. Res. 314 2008 3036 3047
23. M. Novinec, M. Pavsic, and B. Lenarcic A simple and efficient protocol for the production of recombinant cathepsin V and other cysteine cathepsins in soluble form in Escherichia coli Protein Expr. Purif. 82 2012 1 5
24. M. Novinec, M. Korenc, A. Caflisch, R. Ranganathan, B. Lenarcic, and A. Baici A novel allosteric mechanism in the cysteine peptidase cathepsin K discovered by computational methods Nat. Commun. 5 2014 3287
25. D.H. Rich, M.A. Brown, and A.J. Barrett Purification of cathepsin B by a new form of affinity chromatography Biochem. J. 235 1986 731 734
26. A.J. Barrett, H. Kirschke, B. Cathepsin, H. cathepsin, and L. cathepsin Methods Enzymol. 80 1981 535 561
27. L. Mach, J.S. Mort, and J. Glossl Maturation of human procathepsin B. Proenzyme activation and proteolytic processing of the precursor to the mature proteinase, in vitro, are primarily unimolecular processes J. Biol. Chem. 269 1994 13030 13035
28. C.G. Knight Active-site titration of peptidases Methods Enzymol. 248 1995 85 101
29. J.C. Krupa, S. Hasnain, D.K. Nagler, R. Menard, and J.S. Mort S2' substrate specificity and the role of His110 and His111 in the exopeptidase activity of human cathepsin B Biochem. J. 361 2002 613 619
30. S.S. Cotrin, L. Puzer, W.A. de Souza Judice, L. Juliano, A.K. Carmona, and M.A. Juliano Positional-scanning combinatorial libraries of fluorescence resonance energy transfer peptides to define substrate specificity of carboxydipeptidases: assays with human cathepsin B Anal. Biochem. 335 2004 244 252
31. D. Greenbaum, K.F. Medzihradszky, A. Burlingame, and M. Bogyo Epoxide electrophiles as activity-dependent cysteine protease profiling and discovery tools Chem. Biol. 7 2000 569 581
32. G. Lalmanach, R. Mayer, C. Serveau, J. Scharfstein, and F. Gauthier Biotin-labelled peptidyl diazomethane inhibitors derived from the substrate-like sequence of cystatin: targeting of the active site of cruzipain, the major cysteine proteinase of Trypanosoma cruzi Biochem. J. 318 1996 395 399
33. N. Schaschke, I. Assfalg-Machleidt, T. Lassleben, C.P. Sommerhoff, L. Moroder, and W. Machleidt Epoxysuccinyl peptide-derived affinity labels for cathepsin B FEBS Lett. 482 2000 91 96
34. S.W. Rogers, M. Burks, and J.C. Rogers Monoclonal antibodies to barley aleurain and homologs from other plants Plant J. 11 1997 1359 1368
35. I. Cambra, M. Martinez, B. Dader, P. Gonzalez-Melendi, J. Gandullo, M.E. Santamaria, and I. Diaz A cathepsin F-like peptidase involved in barley grain protein mobilization, HvPap-1, is modulated by its own propeptide and by cystatins J. Exp. Bot. 63 2012 4615 4629
36. T. Vernet, D.C. Tessier, C. Richardson, F. Laliberte, H.E. Khouri, A.W. Bell, A.C. Storer, and D.Y. Thomas Secretion of functional papain precursor from insect cells. Requirement for N-glycosylation of the pro-region J. Biol. Chem. 265 1990 16661 16666
37. M. Fonovic, D. Bromme, V. Turk, and B. Turk Human cathepsin F: expression in baculovirus system, characterization and inhibition by protein inhibitors Biol. Chem. 385 2004 505 509
38. M. Cygler, J. Sivaraman, P. Grochulski, R. Coulombe, A.C. Storer, and J.S. Mort Structure of rat procathepsin B: model for inhibition of cysteine protease activity by the proregion Structure 4 1996 405 416
39. C.E. Halls, S.W. Rogers, and J.C. Rogers Purification of a proaleurain maturation protease Plant Sci. 168 2005 1267 1279
40. B.C. Holwerda, and J.C. Rogers Purification and characterization of aleurain: a plant thiol protease functionally homologous to mammalian cathepsin H Plant Physiol. 99 1992 848 855
41. O. Vasiljeva, M. Dolinar, V. Turk, and B. Turk Recombinant human cathepsin H lacking the mini chain is an endopeptidase Biochemistry 42 2003 13522 13528
42. A. Tsuji, Y. Kikuchi, K. Ogawa, H. Saika, K. Yuasa, and M. Nagahama Purification and characterization of cathepsin B-like cysteine protease from cotyledons of daikon radish, Raphanus sativus FEBS J. 275 2008 5429 5443
43. M. Montaser, G. Lalmanach, and L. Mach CA-074, but not its methyl ester CA-074Me, is a selective inhibitor of cathepsin B within living cells Biol. Chem. 383 2002 1305 1308
44. M. Rothe, A. Zichner, E.A. Auerswald, and J. Dodt Structure/function implications for the aminopeptidase specificity of aleurain Eur. J. Biochem. 224 1994 559 565
45. D.K. Nägler, W. Tam, A.C. Storer, J.C. Krupa, J.S. Mort, and R. Menard Interdependency of sequence and positional specificities for cysteine proteases of the papain family Biochemistry 38 1999 4868 4874
46. G. Guncar, M. Podobnik, J. Pungercar, B. Strukelj, V. Turk, and D. Turk Crystal structure of porcine cathepsin H determined at 2.1 A resolution: location of the mini-chain C-terminal carboxyl group defines cathepsin H aminopeptidase function Structure 6 1998 51 61
47. M. Rothe, and J. Dodt Studies on the aminopeptidase activity of rat cathepsin H Eur. J. Biochem. 210 1992 759 764
48. R.W. Mason Interaction of lysosomal cysteine proteinases with alpha 2-macroglobulin: conclusive evidence for the endopeptidase activities of cathepsins B and H Arch. Biochem. Biophys. 273 1989 367 374