Cysteine proteinases and cystatins

Brazilian Archives of Biology and Technology

Volumn 46, Issue 1, 2003, Pages 91-104

  Oliveira, Adeliana S ^a   Xavier Filho, José ^b   Sales, Maurício P ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO NORTE   (Brazil)

^b UNIVERSIDADE ESTADUAL DO NORTE FLUMINENSE DARCY RIBEIRO   (Brazil)

Author keywords

Cystatin; Cysteine proteinases; Phytocystatins

Indexed keywords

ANIMALIA; VERTEBRATA;

EID: 33746987550     PISSN: 15168913     EISSN: 15168913     Source Type: Journal    
DOI: 10.1590/S1516-89132003000100014     Document Type: Review

References (108)

1. Abe, K.; Emori, Y.; Kondo, H.; Susuki, K. and Arai, S. (1987), Molecular cloning of a cysteine proteinase inhibitor of rice (oryzacystatin) - Homology with animal cystatins and transient expression in the ripening process of rice seeds. J. Biol. Chem., 262: (35), 16793-16797.
2. Abe, M.; Kondo, H. and Arai, S. (1987), Purification and characterization of a rice cysteine proteinase inhibitor. Agric. Biol. Chem., 51, 2763-2768.
3. Abe, K.; Emori, Y.; Kondo, H.; Arai, S. and Suzuki, K. (1988), The NH2- terminal 21 amino acid residues are not essential for the papain-inhibitory activity of oryzacystatin, a member of the cystatin superfamily. J. Biol Chem., 263: (16), 7655-7659.
4. Abe, M. and Arai, S. (1991), Some properties of a cysteine proteinase inhibitors from corn endosperm. Agric. Biol. Chem., 55: (9), 2417-2418.
5. Abe, M.; Abe, K.; Kudora, M. and Arai, S. (1992), Corn kernel cysteine proteinase inhibitor as novel cystatin superfamily member of plant origin. Eur. J. Biochem., 209, 933-937.
6. Abe, M.; Abe, K.; Iwabuchi, K.; Domoto, C. and Arai, S. (1994), Corn cystatin I expressed in Escherichia coli: investigation of its inhibitory profile and occurence in corn kernels. J. Biochem., 116: (3), 488-492.
7. Abrahanson, M.; Ritonja, A.; Brown, M. A.; Grubb, A.; Machleidt, W. and Barrett, A. J. (1987), Identification of the probable inhibitory reactive sites of the cysteine proteinase inhibitors, human cystatin C, and chicken cystatin. J. Biol. Chem., 262, 9688-9494.
8. Arai, S.; Watanabe, H.; Kondo, H.; Emori, Y. and Abe, K. (1991), Papain-inhibitory activity of oryzacystatin, a rice seed cysteine proteinase inhibitor, depends on the central Gln-Val-Val-Ala-Gly region conserved among cystatin superfamily members. Biochem., 109, 294-298.
9. Applebaum, S. W. (1985), Biochemistry of digestion. In: Kerkut, G. A and Gilbert, L. I. (eds.). Compehensive insect Physiology, Biochemistry and Pharmacology. Oxford: Pergamon Press. 4, 279-311.
10. Baumgartner, B. and Chrispeels, M. J. (1976), Partial characterization of a protease Inhibitor which inhibits the major endopeptidase present in the cotyledons of mung-beans. Plant Physiol. 58, 1-6.
11. Baumgartner, B. and Chrispeels, M. J. (1977), Purification and characterization of Vicilin peptidohydrolase, the major endopeptidase in the cotyledons of mung-bean seedling. Eur. J. Biochem., 77, 223-233.
12. Barrett, A. J.; Rawlings, N. D.; Davies, E. M.; Macheleidt, M.; Salve-sen, G. and Turk, V. (1986), In: Barrett, A. J. and Sal-vesen, G. E. (eds.). Proteinase Inhibitors. Amsterdan: Science Publishers. 12, 515-569.
13. Barrett, A. J. (1987), The Cystatins; a new class of peptidase inhibitors. Trend Biochem. Sci., 12, 193-196.
14. Birk, Y. and Applebaum, Y. (1960), Effect of soybean trypsin inhibitors on the development and midgut proteolytic activity of Tribolium castaneum larvae. Enzymologia., 22, 318-326.
15. Blanco-Labra, A.; Martinez-Gallardo, N. A.; Sandoval-Carboso, L. and Delano-Frier, J. (1996), Purification and characterization of a digestive cathepsin Dproteinase isolated from Tribolium castaneum larvae (Herbst). Insect Biochem. Molec. Biol., 26: (1), 95-100.
16. Bode, W.; Engh, R.; Musil, D.; Thiele, U.; Huber, R.; Karshikov, A.; Brzin, J.; Kos, J. and Turk, V. (1988), The 2.0 A° X-ray crystal structure of chicken egg white cystatin and its possible mode of interaction with cysteine proteinase. The EMBO Journal., 7: (8), 2593-2599.
17. Bode, W. and Huber, R. (1992), Natural protein proteinase inhibitors and their interaction with proteinases. J. Biochem., 204, 433-451.
18. Bolter, C. J. (1993), Methyl Jasmonate induces papain inhibitor(s) in tomato leaves. Plant Physiol., 103, 1347-135.
19. Bolter, C. J. and Jongsma, M. A. (1995), Colorado potato beetles (Leptinotarsa decemlineata) adapt to proteinase inhibitors induced in potato leaves by methyl jasmonate. J. Insect Physiol., 41, 1071-1078.
20. Botella, M. A.; Xu, Y.; Prabha, T. N., Zhao, Y., Narasimhan, M. L., Wilson, K. A., Nielsen, S.S., Bressan, R. A. and Hasegawa, P.A. (1996), Differential expressio of soybean cysteine proteinase inhibitor genes during development and in response to wounding and methyl jasmonate. Plant Physiol., 112, 1201-1210.
21. Brzin, J.; Popovic, T.; Drobnic-Kosorok, M.; Kotnik, M. and Turk, V. (1988), Inhibitors of cysteine proteinases from potato. Biol. Chem. Hoppe Seyler., 369, 233-238.
22. Campos, F. A. P.; Xavier-Filho, J.; Silva, C. P. and Ary, M. B. (1989), Resolution and partial characterization of proteinases and α-amylases from midguts of larvae of the bruchid beetle Callosobruchus maculatus (F). Comp Biochem. Physiol., 92: (B), 51-57.
23. Ceros, M. and Carbonell, J. (1993), Purification and characterization of thiol-protease induced during senescence of unpollinated ovaries of Pisum sativum. Physiol Plant., 88, 267-274.
24. Chen, M. S.; Johnson, B.; Wen, L.; Muthukrishnan, S.; Kramer, K. J.; Morgan, T. D. and Reeck, G. R. (1992), Rice cystatin: bacterial expression, purification, cysteine proteinase inhibitory activity, and insect growth suppres-sing activity of a truncated form of the protein. Prot. Exp. Purif., 3, 41-49.
25. Colella, R.; Sakaguchi, Y.; Nagase, H. and Bird, J. W. C. (1989), Chiken egg white cystatin. J. Biol Chem., 264, 17164-17117.
26. Cygler, M. and Morb, J. S. (1997), Proregion structure of members of the papain superfamily modeof inhibition of enzymatic activity. Biochem., 79, 645-652.
27. Domoney, C.; Welhan, I. and Sidebotton, C. (1993), Purification and characterization of Pisum seed trypsin Inhibitors. J. Exp. Bot., 44: (261), 701-709.
28. Fernandes, K. V. S.; Sabelli, P. A.; Barratt, P.; Richardson, M.; Xavier-Filho, J. and Shewry, R. (1993), The resistence of cowpea seeds to bruchid beetle is not related to levels of cysteine proteinase inhibitors. Plant. Mol. Biol., 23, 215-219.
29. Gatehouse, A. M. R.; Butler, K. F.; Fenton, K. A. and Gatehouse, J. (1985), Presence and partical characterization of a major proteolytic enzyme in the larval gut of Callosobruchus maculatus. Entomol. Exp. Appl., 39, 279-86.
30. Gillikin, J. W.; Bevilacqua, S. and Graham, J. S. (1992), Partial characterization of digestive tract proteinases from western corn root-worm larvae, Diabrotica virgifera. Arch Insect Biochem. Physiol., 19, 285-298.
31. Groover, A.; DewilL, N.; Heidel, A. and Djones, A. (1997), Programmed cell death of plant tracheary elements differentiating in vitro. Protoplasma., 196, 197-211.
32. Greenberg, J. T. (1996), Programmed cell death: A way of life for plants. Proc. Natl. Acad. Sci., 93, 12094-12097.
33. Gruden, K.; Strukel, J. B.; Ravnikar, M.; Poljsak-Prijately, M.; Mavric, I.; Brzin, J.; Pungercar, J. and Kregar, I. (1997), Potato cysteine proteinase inhibitor gene family: molecular cloning, characterization and immunocytochemica localisation studies. Plant Mol. Biol., 34, 317-323.
34. Hatano, K. I.; Kojima, M.; Tanokura, M. and Takahashi, K. (1996), Solution structure of bromelain inhibitor VI from pineapple stem: Structural similarity with Bowman Birk trypsin/chymotrypsin inhibitor from soybean. J. Biochem., 35, 5379-5384.
35. Hatano, K. I., Tanokura, M. and Takahashi, K. (1998), The amino acid sequences of isoforms of the bromelain inhibitor from pineapple stem. J. Biochem., 124, 457-461.
36. Hines, M. E.; Osuala, C. I. and Nielsen, S. S. (1991), Isolation and partial characterization of a soybean cystatin cysteine proteinase inhibitor of Coleopteran digestive proteolitic activity. J. Agric. Food. Chem., 39, 1515-1520.
37. Hirashiki, I.; Ogata, F.; Yoshida, N.; Makisumi, S. and Ito, A. (1990), Purification and complex formation analysis of a cysteine proteinase inhibitor (Cystatin) from seeds of Wisteria floribunda. J. Biochem., 108, 604-608.
38. Homma, K.; Kurata, S. and Natori, S. (1994), Purification, characterization, and cDNA cloning of procathepsin L from the culture medium of NIH-Sape-4, an embryonic cell line of Sarcophaga peregrina (flesh fly), and its involvement in the differentiation of imaginal discs. J. Biol. Chem., 269, 15258-15264.
39. Houseman, J. G. and Downe, A. E. R. (1982), Characterization an acidic proteinase from the posterior midgut of Rhodnius prolixus stal (Hemiptera:Reduviidae). Insect Biochem., 12: (6), 651-655.
40. Houseman, J. G. and Downe, A. E. R. (1983), Cathepsin D-like activity in the posterior gut hemipteran insect. Comp. Biochem Physiol., 75: (B), 509-512.
41. Irie, K.; Hosoyama, H.; Takeuchi, T.; Iwabuchi, K. and Watanabe, A. (1996), Transgenic rice established to express corn cystatin exhibits strong inhibitors activity against insect gut proteinases. Plant. Mol. Biol., 30, 149-157.
42. Jongsma, M. A.; Bakker, P. L.; Peters, J.; Bosch, D. and Stiekema, W. J. (1995), Adaptation of Spodoptera exigua larvae to plant proteinase inhibitors by induction of gut proteinase activity insensitive to inhibition. Proc. Natl. Acad. Sci., 92, 8041-8045.
43. Jongsma, M. A.; Peters, J.; Stiekema, W. J. and Bosch, D. (1996), Characterization and partial purification of gut proteinases of Spodoptera exigua Hübner (Lepidoptera:Noctuidae). Insect Biochem. Mol. Biol., 26, 623-632.
44. Jouanin, L.; Bonadé-Bottino, M.; Girard, C.; Morrot, G. and Giband, M. (1998), Transgenic plants for insert resistance. Plant Science., 131, 1-11.
45. Karrer, K. M.; Peifer, S. L. and Ditomas, M. E. (1993), Two distinct gene subfamilies within the family of cysteine protease genes. Proc. Natl. Acad. Sci., 90, 3063-3067.
46. Kim, J. Y.; Chung, Y. S.; Paek, K. H.; Park, Y. I.; Kim, J. K.; Yu, S. N.; Oh, B. J. and Shin, J. S. (1999), Isolation and characterization of a cDNA encoding the cysteine proteinase inhibitor, induced upon flower maturation in carnation using supression subtractive hybridization. Mol. Cells., 9: (4), 392-397.
47. Kimura, M.; Ikeda, T.; Fukumoto, D.; Yamasaki, N. and Yonekura, M. (1995), Primary structure of a cysteine proteinase inhibitor from the fruit of avocado (Persea americana Mill). Biosci Biotechnol Biochem., 59: (12), 2328-2329.
48. Kitch, L. W. and Murdock, L. L. (1986), Partial characterization of a major proteinase from larval of Callosobruchus maculatus (F.). Arc. Insect Biochem. Physiol., 3, 561-76.
49. Koehler, S. M. and Ho, T-HD. (1990), A major gibberellic acid-induced barley aleurone cysteine protease which digests hordein. Plant Physiol., 94, 251-258.
50. Koiwa, H.; Shade, R. E.; Zhu-Salzman, K.; Subramanian, L.; Murdock, L. L.; Nielsen, S. S.; Bressan, R. A. and Hasegawa, P. M. (1998), Phage display selection can differentiate insecticidal activity of soybean cystatins. Plant Journal., 14: (3), 371-379.
51. Kondo, H.; Abe, K.; Emori, Y. and Arai, S. (1991), Gene organization of oryzacystatin-II, a new cystatin superfamily member of plant origin, is closely related to that of oryzacystatin-I but different from those of animal cystatins. FEBS. Lett., 278, 87-90.
52. Kondo, H.; Abe, K.; Nishimura, I.; Iwatanabe, H.; Emori, Y. and Arai, S. (1990), Two distinct cystatin species in rice seeds with different specificities against cysteine proteinases. J. Biol. Chem., 265: (26), 15832-15837.
53. Kouzuma, Y.; Kawano, K.; Kimura, M.; Yamasaki, N.; Kadowaki, T. and Yamamoto, K. (1996), Purification, characterization, and sequencing of two cysteine proteinase L. inhibitors, Sea and Scb, from sunflower (Helianthus annus) seeds. J. Biochem., 6, 1106-1113.
54. Kuroda, M.; Ishimoto, M.; Suzuki, K.; Kondo, H.; Abe, K.; Kitamura, K. and Arai, S. (1996), Oryzacystatins exhibit growth-inhibitory and lethal effects on different species of bean insect pests Callosobruchus chinensis (Coleoptera) and Riptortus clavatus (Hemiptera). Biosci Biotechnol. Biochem., 60, 209-212.
55. Lamb, C. and Dixon, R. A. (1997). The oxidative burst in plant dissease resistance. Annu. Ver. Plant Physiol. Plant Mol. Biol., 48, 251-275.
56. Le Boulay, C.; Van Wormhoudt, A. and Sellos, D. (1995), Molecular cloning and sequencing of two cDNAs encoding cathepsin L-related cysteine proteinases in the nervous system and in the stomach of the Norway lobster (Nephrops norvegi-cus). Comp Biochem. Physiol. 111: (B), 353-359.
57. Lemos, F. J. A.; Campos, F. A. P.; Silva, C. P. and Xavier-Filho, J. (1990), Proteinases and amylases of larval midgut of Zabrotes subfasciatus eared on cowpea (Vigna unguiculata) seeds. Entomol. Exp. Appl., 56, 219-227.
58. Lenarcic, B.; Ritonja, A.; Turk, B.; Dolenc, I. D. and Turk, V. (1992), Characterization and structure of pineapple stem inhibitor of cysteine proteinase. Biol._ Chem. Hoppe-Seyler, 373, 454-464.
59. Li, Z.; Sommer, A.; Dingermann, T. and Noe, C. R. (1996), Molecular cloning and sequence analysis of a cDNA encoding a cysteine proteinase inhibitor from Sorghum bicolor seedlings. Mol. Gen. Genet., 251: (4), 499-502.
60. Liang, C.; Brookhart, G.; Feng, G. H.; Reeck, G. R. and Kramer, K. J. (1991), Inhibition of digestive proteinase of stored grain Coleoptera by oryzacystatin, a cysteine proteinase inhibitor from rice seed. FEBS Lett., 278: (2), 139-142.
61. Machleidt, W.; Borchart, U.; Fritz, H.; Brzin, J.; Ritonja, A. and Turk, V. (1983), Protein inhibitors of cysteine proteinase II. Primary structure of stefin, a cytosolic inhibitor of cysteine proteinases for human polymorphonuclear granulocyles. Hoppe-Seyler's Physiol Chem., 364, 1481-1486.
62. Machleidt, W.; Thiele, U.; Laber, B.; Arsfald-Machleidt, I.; EsterL, A.; Wiegand, G.; Kos, J.; Turk, V. and Bode, W. (1989), Mechanism of inhibition of papain by chicken egg white cystatin: Inhibition constants of N-terminally truncated forms and cyanogen bromid fragments of the inhibitor. FEBS., 243: (2), 234-238.
63. Matsumoto, I.; Watanabe, H.; Abe, K.; Arai, S. and Emori, Y. (1995), A putative digestive cysteine proteinase from Drosophila melanogaster in predominantly expressed in the embryonic and larval midgut. Eur. J. Biochem., 227, 582-587.
64. Matsumoto, I.; Emori, Y.; Abe, K. and Arai, S. (1997), Characterization of a gene family encoding cysteine proteinases of Sitophilus zeamais (Maize weevil), and analysis of the protein distribution in various tissues including alimentary tract and germ cells. J. Biochem., 121, 464-476.
65. Michaud, D.; Cantin, L. and Vrain, T. C. (1995), Carboxyl-terminal truncation of oryzacystatin II by oryzacystatin insect digestive proteinases. Arch. Biochem Biphys., 322: (2), 469-474.
66. Michaud, D.; Nguyen-Quoc, B.; Vrain, T. C.; Fong, D. and Yelle, S. (1996). Response of digestive proteinases from the Colorado potato beetle (Leptinotarsa decemlineata) and black vine weevil (Otiorynchus sulcatus) to a recombinant form of human stefin). Arch. Insect Biochem. Physiol., 31, 451-464.
67. Mikkonen, A.; Porali, I.; Ceros, M. and Ho, T. D. (1996), A major cysteine proteinase, EPB, in germinating barley seeds: structure of two intronless genes and regulation of expression. Plant Mol. Biol., 31, 239-254.
68. Misaka, T.; Kuroda, M.; Iwabuchi, K.; Abe, K. and Arai, S. (1996), Soyacystatin, a novel cysteine proteinase inhibitor in soybean, is distinct in protein structure and gene organization from other cystatins of animal and plan origin. Eur. J. Biochem., 240, 609-614.
69. Mitsuhashi, W.; Koshiba, T. and Minamikawa, T. (1986). Separation and characterization of two endopeptidases from cotyledons of germinating Vigna mungo seeds. Plant Physiol., 80, 628-634.
70. Murdock, L. L.; Brookehart, G.; Dunn, P. E.; Foard, D. E.; Kelly, S.; Kitch, L.; Shade, R. E.; Shuckle, R. H. and Wofson, J. L. (1987), Cysteine digestive proteinases in Coleoptera. Comp. Biochem. Physiol., 87: (B), 783-787.
71. Murdock, L. L.; Shade, R. E. and Pomeroy, M. A. (1988), Effects of E-64, a cysteine proteinase inhibitor, on Cowpea weevil growth, developmente and fecundity. Environ. Entomol., 17: (3), 467-469.
72. Nakajima, Y.; Tsuji, Y.; Homma, K-I. and Naton, S. (1997), A novel protease in the pupal yellow body of Sarcophaga peregrina (flesh fly). The Jour. Biol. Chem., 272: (38), 23805-23810.
73. Neurath, H. (1984), Evolution of Proteolytic Enzimes. Science., 224, 350-357.
74. Ojima, A.; Shiota, H.; Higashi, K.; Kamada, H.; Shimma, Yoh-Ichi Wadamasata and Satoh, S. (1997). An extracellular insoluble inhibitor of cysteine proteinases in cell cultures And seeds of carrot. Plant. Mol. Biol., 34, 99-109.
75. Oliva, M. L. V.; Sampaio, M. U. and Sampaio, C. A. M. (1987), Serine- and SH-proteinase inhibitors from Enterolobium contorsiliquum Beans. Purification and preliminary characterization. Brazilian J. Med. Res., 20, 767-770.
76. Oliveira, A. S. (2000), Purificação c caracterizaç ão de um inibidor de proteinase cisteínica de sementes de algaroba (Prosopis juliflora). Meinster thesis, Universidade Federal do Rio Grande do Norte, Natal/RN, Brazil.
77. Orr, G. L.; Strickland, J. A. and Walsh, T.A. (1994), Inhibition of Diabrotica larval growth by a multicystatin from potato tubers. J. Insect Physiol., 40: (10), 893-900.
78. Pereira, R. A. (2000), Isolamento e caracterização parcial de uma proteinase serinica presente no intestino médio de larvas de Mimosestes mimosae (Coleoptera:Bruchidae). Meinster thesis, Universidade Federal do Rio Grande do Norte, Natal/RN, Brazil.
79. Pernas, M.; Sanchez-Monge, R.; Gomez, L. and Salcedo, G. (1998), A chestnut seed cystatin differentially effective against cysteine proteinases from closely related pests. Plant Mol. Biol., 38: (6), 1235-1242.
80. Rawlings, N. D. and Barrett, A. J. (1994), Families of cysteine peptidases. Methods Enzymol., 244, 461-486.
81. Ryan, C. A. (1990). Protease inhibitors in plants: Genes for Improving Defenses gainst Insects and Pathogens. Annu. Rev. Phytopathol., 28, 425-429.
82. Ryan, S. N.; Liang, W. A. and McManus, M. T. (1998), A cysteine proteinase inhibitor purified from apple fruit. Phytochemistry., 49, 957-63.
83. Saitoh, F.; Isrmura, S.; Sanada, K. and Ohnishi, K. (1991), Cystatins of family II are harboring two domains which retain inhibitory activities against the proteinase. Biol. Ciophys. Res. Commun., 175, 1070-1075.
84. Sato, N.; Ishidoh, K.; Uchiyama, Y. and Kominami, E. (1990), Molecular cloning and sequencing of cDNA for rat cystatin β. Nucleic Acids Res., 18: (22), 6698.
85. Salmia, M. A. (1980), Inhibitors of endogenous proteinases in Scot pine seeds: fracionation and activity changes during germination. Physiol Plant., 48, 266-270.
86. Salvesen, G.; Parkes, C.; Abrahamson, M.; Grubb, A. and Barrett, A. J. (1986), Human low-Mr kininogen contain three copies of a cystatin sequence that are divergent in structure and in inhibitory activity for cysteine proteinases. Biochem. J., 234, 429-434.
87. Silva, C. P. and Xavier-Filho, J. (1991), Comparison between the levels of aspartic and cysteine proteinases of the larval midgut of Callosobruchus maculatus (F.) and Zabrotes subfascitus (Boh.) (Coleoptera:Bruchidae). Comp. Biochem. Physiol., 99: (B), 529-533.
88. Schukle, R. H. and Murdock, L. L. (1983), Lipoxygenase, trypsin inhibitor, and lectin from soybeans: effects on larval growth of Manduca Sexta (Lepidoptera:Sphigidae). Environ. Ent., 12, 787-791.
89. Solommon, M.; Belenghi, B.; Delledonne, M.; Menachen, E. and Levine, A. (1999), The involvement of cysteine proteinase and protease inhibitor genes in the regulation of programmed cell death in plants. The Plant Cell., 11, 431-443.
90. Stubbs, M. T.; Laber, B.; Bode, W.; Huber, R.; Jerala, R.; Lenarcic, B. and Turk, V. (1990), The refined 2.4 A X-ray crystal structure of recombinant human stefin B in complex with the cysteine proteinase papain: a novel type of proteinase inhibitor interaction. EMBO J., 9, 1939-1947.
91. Steller, H. (1995), Mechanisms and genes of cellular suicide. Science., 267, 1445-1449.
92. Takahashi, N.; Kurata, S. and Natori, S. (1993), Molecular cloning of cNDA for the 29 kDa proteinase participating in decomposition of the larval fat body during metamorphosis of Sarcophaga peregrina (flesh fly). FEBS Lett., 334, 153-157.
93. Tanaka, T.; Yamauchi, D. and Minamikawa, T. (1991), Nucleotide sequence of cDNA for an endopeptidase (EP-C1) from pods of maturing Phaseolus vulgaris fruits. Plant Mol. Biol., 16, 1083-1084.
94. Tanaka, T.; Minamikawa, T.; Yamauchi, D. and Ogushi, Y. (1993), Expression of an endopeptidase (EP-C1) in Phaseolus vulgaris plant. Plant Physiol., 101, 421-428.
95. Thie, N. M. R. and Houseman, J. G. (1990), Identification of cathepsin B, D and H in the larval midgut of Colorado potato beetle Leptinotarsa decemlineata. Insect Biochem. 20, 313-318.
96. Trysellius, Y. and Hultmark, D. (1997), Cysteine proteinase 1 (CP1), a chatepsin L-like enzyme expressed in the Drosophila melanogaster haemocyte cell line mbn-2. Insect Mol. Biol., 6: (2), 173-181.
97. Turk, V. and Bode, W. (1991), The cystatins: proteinase inhibitors of cysteine proteinases. FEBS Lett., 285, 213-219.
98. Turk, B.; Turk, V. and Turk, D. (1997), Structural and functional aspects of papain-like cysteine proteinases and their protein inhibitors. Biol. Chem. Hopp Seyler., 378, 141-150.
99. Urwin, P. E.; Atkinson, H. J.; Waller, D. A. and McPherson, M. J. (1995), Engineered oryzacystatin-I expressed in transgenic hairy roots confers resistance to Globodera pallida. Plant. J., 8: (1), 121-131.
100. Urwin, P. E.; Lilley, C. J.; McPherson, M. J. and Atkinson, H. J. (1997), Resistance to both cyst and root-knot nematodes confered by transgenic Arabidopsis expressing a modified plant cystatin. Plant. J., 12: (2), 455-61.
101. Waldron, C.; Lynett, M.; Wegrich, P.; Merlo, A. O. and Walsh, T. A. (1993), Characterization of a genomic sequence coding for potato multicystatin, an eight-domain cysteine proteinase inhibitor. Plant Mol. Biol., 23, 801-812.
102. Walsh, T. A. and Strickland, J. A. (1993), Proteolysis of the 85-Kilodalton crystalline cysteine proteinase inhibitor from potato release functional cystatin domains. Plant Physiol., 103: (4), 1227-1234.
103. Wolfson, J. L. and Murdock, L. L. (1987), Suppression of larval Colorado potato beetle growth and development by digestive proteinase inhibitors. Entomol. Exp. Appl., 44, 235.
104. Watanabe, H.; Abe, K.; Emori, Y.; Hosoyama, H. and Arai, S. (1991), Molecular cloning and gibberellin-induced expression of multiple cysteine protease of rice seeds (orizains). J. Biol. Chem., 266, 16897-16902.
105. Wieman, K. F. and Nielsen, S. S. (1988), Isolation and partial characterization of a major gut proteinases from larval Acanthoscelides obtectus Say (Coleoptera, Bruchidae). Comp Biochem Physiol., 89B: (2), 419-426.
106. Xavier-Filho, J. and Coelho, A. N. (1980), Acid proteinases of Callosobruchus maculatus and proteinase inhibitors of Vigna unguiculata. Abstract from the Annual Meeting of the American Soc. Plant Physiol. And Phytochcmical Society of North America. Plant Physiol., 65, 138.
107. Yamamoto, Y.; Takimoto, K.; Izumi, S.; Toriyama-Sakurai, M.; Kageyama, T. and Takahashi, S. Y. (1994), Molecular cloning and sequencing of cDNA that encodes cysteine proteinase in the eggs of the silkmoth, Bombys mori, J. Biochem., 116, 1330-1335.
108. Zhao, Y.; Botella, M. A.; Subramanian, L.; Niu, X.; Nielson, S. S.; Bressan, R. A. and Hasegawa, P. M. (1996), Two wound inducible Soybean cystein proteinase inhibitors have greater insect digestive proteinase inhibitory activities then a constitutive homolog. Plant Physiol., 111, 1299-1306.