SOLANUM PROTEASE INHIBITORS AND THEIR THERAPEUTIC POTENTIALITIES: A REVIEW
DOI:
https://doi.org/10.22159/ijpps.2016v8i12.14836Keywords:
Solanum, Protease inhibitors, Biological potentialities, Diversity, CharacterizationAbstract
Protease inhibitors (PIs) are diverse group of proteins with low molecular weight that are ubiquitous in all life forms. PIs are reducers of the physiological activity of proteases and fascinated the attention of biotechnological researchers. In the evolutionary course, plants have developed diverse adaptive mechanisms of defence against various unfavorable conditions including that of predators and pathogens. Phylogenetic relationships among diverse PI families like serpin, Bowman–Birk, cereal trypsin/α-amylase inhibitor, proteinase inhibitor I, proteinase inhibitor II and cystatin have been evaluated. PIs evolution seems to occur through multiple interacting mechanisms and not commonly seen with other co-evolving molecules. Interaction of PIs produced by host organisms and the invasive/dietary protease of pathogens or parasites or predators, leads to a phylogenetic ‘arms race' of rapid structural modulation in both interacting proteins. Further, the high rate of retention of gene duplication and inhibitory domain multiplication results the PI as potential model system to trace the basic evolutionary process of functional diversification. The mode of action of PI is either via inactivating the hydrolytic enzymes or depolarization of cell membrane of the pathogens thereby inhibiting its growth and invasion. Generally, PIs possess significant number of disulfide bonds due to cysteine residues that provide them resistance to heat, extremes of pH, and proteolysis. However, PIs have been extracted and purified only from few monocots and dicots plants. Currently, PI genes were used for developing insect-resistant transgenic plants for crop improvements. Classification of PIs over the last several years has been based on structural–functional relationships. This review bridges the gap between the folkloric uses of Solanum PIs, their diversity and biological potentialities.
Downloads
References
Birk Y. Plant protease inhibitors, significance in nutrition, plant protection, cancer prevention and genetic engineering, springer-verlag berlin Heidelberg. 1st edn; 2003. p. 1-5.
Laskowski M, Kato I. Protein inhibitors of proteinases. Annu Rev Biochem 1980;49:593-626.
Hung CH, Huang CC, Tsai WS, Wang HL, Chen YL. Purification and characterization of a trypsin inhibitor from Brassica campestris seeds. J Yuanpei Univ Sci Technol 2003;10:13-22.
Fan XM, Wong BCY, Wang WP, Zhou XM, Cho CH. Inhibition of proteasome function is induced apoptosis in gastric cancer. Int J Cancer 2001;93:481-8.
Miller EA, Lee MCS, Atkinson AHO, Anderson MA. Identification of a novel four-domain member of the proteinase inhibitor II family from the stigmas of Nicotiana alata. Plant Mol Biol 2000;42:329-33.
Edmonds JM. Biosystematics of Solanum L. section Solanum (Maurella). The Biology and Taxonomy of the Solanaceae. JG Hawkes, RN Lester, AD Skelding. eds. Academic Press: London; 1979a. p. 529-48.
Patel K, Singh RB, Patel DK. Medicinal significance, pharmacological activities, and analytical aspects of solasodine: a concise report of current scientific literature. J Acute Disease 2013;2:92–8.
Bode W, Hubr R. Natural protein proteinase inhibitors and their interaction with proteinases. Eur J Biochem 1992;204:433-51.
Barrett AJ, Rawlings ND, Woessner JF. Handbook of proteolytic enzymes. New York: Academic Press; 1998. p. 101-24.
Meulenbroek EM, Thomassen EA, Pouvreau L, Abrahams JP, Gruppen H, Pannu NS. The structure of a post-translationally processed heterodimeric double-headed Kunitz-type serine protease inhibitor from potato. Acta Crystallogr Sect D: Biol Crystallogr 2012;68:794-9.
Richardson M. Seed storage proteins: The Enzyme Inhibitors. In: LJ Rogers. ed. Methods in plant biochemistry amino acids, proteins, and nucleic acids New York: Academic Press; 1995;5:259-305.
Green TR, Ryan CA. Wound-induced proteinase inhibitor in plant leaves a possible defense mechanism against insects. Science 1972;175:776-7.
Kuo T, Pearce G, Ryan CA. lsolation and characterization of proteinase inhibitor I from etiolated tobacco leaves. Arch Biochem Biophys 1984;230:504-10.
Graham JS, Pearce J, Merryweather K, Titani LH, Ericsson, Ryan CA. Wound-induced proteinase inhibitors from tomato leaves. I. The cDNA-deduced primary structure of pre-inhibitor I and its post-translational processing. J Biol Chem 1985a;260:6555-60.
Ryan CA, Balls AK. An inhibitor of chymotrypsin from Solanum tuberosm and its behavior toward trypsin. Proc Natl Acad Sci 1962;48:1839-44.
Wingate VP, Broadway RM, Ryan CA. Isolation and characterization of a novel, developmentally regulated proteinase inhibitor I protein and cDNA from the fruit of a wild species of tomato. J Biol Chem 1989;264:17734-8.
Lee JS, Brown WE, Graham JS, Pearce G, Fox EA, Dreher TW, et al. Molecular characterization and phylogenetic studies of a wound-inducible proteinase inhibitor I gene in Lycopersicon species). Proc Natl Acad Sci USA 1986;83:7277-81.
Pearce G, Johnson S, Ryan CA. Purification and characterization from Tobacco (Nicotiana tabacum) leave of six small, wound-inducible, proteinase isoinhibitors of the potato inhibitor II family. Plant Physiol 1993;102:639-44.
Taylor BH, Young, Scheuring CF. Induction of a proteinase inhibitor II-class gene by auxin in tomato roots. Plant Mol Biol 1993;23:1005-14.
Schmidt DD, Kessler A, Kessler D, Schmidt S, Lim M, Gase K, et al. Solanum nigrum: a model ecological expression system and its tools. Mol Ecol 2004;13:981–95.
Ledoigt G, Griffaut B, Debiton E, Vian C, Mustel A, Evray G, et al. Analysis of secreted protease inhibitors after water stress in potato tubers. Int J Biol Macromols 2006;38:268-71.
Ryan CA. Proteolytic enzymes and their inhibitors in plants. Annu Rev Plant Physiol 1973;24:173-96.
De Leo F, Volpicella M, Licciulli F, Liuni S, Gallerani R, Ceci LR. PLANT-PIs: a database for plant protease inhibitors and their genes. Nucl Acids Res 2002;30:347-8.
Rawlings ND, Barrett AJ. Evolutionary families of peptidases. Biochem J 1993;290:205-18.
Heibges A, Salamini F, Gebhardt C. Functional comparison of homologous membranes of three groups of Kunitz-type enzyme inhibitors from potato tubers (Solanum tuberosum L). Mol Genet Genomics 2003;269:535-41.
Hass GM, Hermodson MA. Amino acid sequence of a carboxypeptidase inhibitor from tomato fruit. Biochemistry 1981;20:2256-60.
Havkioja E, Neuvonen L. Induced long-term resistance to birch foliage against defoliators: defense or incidental. Ecology 1985;66:1303-8.
Greenblatt HM, Ryan CA, James MNG. The structure of the complex of Streptomyces griseus proteinase B and polypeptide chymotrypsin inhibitor-I from russet Burbank potato tubers at 2.1 Ã… resolution. J Mol Biol 1989;205:201-28.
Strukelj B, Pungercar J, Mesko P, Barlic-Maganja D. Characterization of aspartic proteinase inhibitors from potato at the gene, cDNA and protein levels. Biol Chem Hoppe-Seyler 1992;373:477-82.
Gruden K, Strukelj B, Ravnikar M, Poljsak-Prijatelj M. Potato cysteine proteinase inhibitor gene family: molecular cloning, characterisation and immunocytochemical localization studies. Plant Mol Biol 1997;34:317-23.
Richardson M. Chymotryptic inhibitor I from potatoes. The amino acid sequence of subunit A. Biochem J 1974;137:101-12.
Keil M, Sanchez-Serrano J, Schell J, Willmitzer L. Primary structure of a proteinase inhibitor II gene from potato (Solanum tuberosum). Nucleic Acids Res 1986;14:5641-50.
Graham RA, Holland-Czytko H, Andersen JL, Ryan CA. Vacuolar localization of wound-induced carboxypeptidase inhibitor in potato leaves. Plant Physiol 1985;78:76-9.
Barrette-Ng IH, Ng KKS, Cherney MM, Pearce G. Structural basis of inhibition revealed by a 1:2 complex of the two-headed tomato inhibitor-II and subtilisin carlsberg. J Biol Chem 2003;278:24062-71.
Koiwa H, Bressan RA, Hasegawa PM. Regulation of protease inhibitors and plant defense. Trends Plant Sci 1997;2:379–84.
Kim JY, Chung YS, Paek KH, Park YI, Kim JK, Yu SN, et al. Isolation and characterization of a cDNA encoding the cysteine proteinase inhibitor, induced upon flower maturation incarnation using suppression subtractive hybridization. Mol Cells 1999;9:392-7.
Habib H, Fazili KM. Plant protease inhibitors: a defense strategy in plants. Biotechnol Mol Biol Rev 2007;2:68-85.
Valueva TA, Revina TA, Gvozdeva EL, Gerasimova NG, Ilhinskaia LI, Ozretskovakaia OL. Effects of elicitors on the accumulation of proteinase inhibitors in injured potato tubers. Appl Biochem Microbiol 2001;37:512-6.
Lison P, Rodrigo I, Conejero V. A novel function for the cathepsin D inhibitor in tomato. Plant Physiol 2006;142:1329-39.
Keilova H, Tomasek V. Isolation and properties of cathepsin D inhibitor from potatoes. Collect Czech Chem Commun 1976;41:489-97.
Mistry R, Snashall PD, Totty N, Briskin S, Guz A, Tetley TD. Purification and characterization of a novel–type serine proteinase inhibitor of neutrophil elastase from sheep lung. Biochim Biophys Acta 1997;1342:51-61.
Miaoying Tian, Brett Benedetti, Sophien Kamoun. A second kazal-like protease inhibitor from Phytophthora infestans inhibits and interacts with the apoplastic pathogenesis-related protease P69B of tomato. Plant Physiol 2005;138:1785–93.
Ali Aberoumand. Screening of phytochemical compounds and toxic proteinaceous protease inhibitor in some lesser-known food based plants and their effects and potential applications in food. Int J Food Sci Nutr Eng 2012;2:16-20.
Sarnthima, Rakrudee, Khammuang, Saranyu. Antibacterial activities of Solanum stramonifolium seed extract. Int J Agric Biol 2012;14:111.
Park Y, Choi BH, Kwak JS, Kang CW, Lim HT, Cheong HS, et al. Kunitz-type serine protease inhibitor from potato (Solanum tuberosum L. cv. Jopung). J Agric Food Chem 2005;53:6491-6.
Sritanyarat W, Pearce G, Siems WF, Ryan CA, Wititsuwannakul R, Wititsuwannakul D. Isolation and characterization of isoinhibitors of the potato protease inhibitor I family from the latex of the rubber trees, Hevea brasiliensis. Phytochemistry 2006;67:1644-50.
Meenu Krishnan VG, Murugan K. Purification, characterization and kinetics of protease inhibitor from fruits of Solanum aculeatissimum Jacq. Food Sci Human Wellness 2015;4:97–107.
Kunal R Shah, Dhaval K Patel, Anju Pappachan, C Ratna Prabha, Desh Deepak Singh. Characterization of a kunitz-type serine protease inhibitor from Solanum tuberosum having lectin activity. Int J Biol Macromol 2016;83:259-69.
Heibges A, Glaczinski H, Ballvora A, Salamini F, Gebhardt C. Structural diversity and organiza tion of three gene families for Kunitztype enzyme inhibitors from potato tubers (Solanum tuberosum L.). Mol Genet Genomics 2003;269:526–34.
Speransky AS, Cimaglia F, Krinitsina AA, Poltronieri P, Fasano P, Bogacheva AM, et al. Kunitztype protease inhibitors group B from Solanum palustre. Biotechnol J 2007;2:1417-24.
Speransky AS, Cimaglia F, Krinitsina AA, Poltronieri P, Fasano P. Shevelev, et al. Molecular cloning of Kunitz-type proteinase inhibitor group B genes from potato, Biochemistry 2005;70:292-9.
Xu ZF, Qi WQ, Ouyang XZ, Yeung E, Chye ML. A proteinase inhibitor II of Solanum americanum is expressed in the phloem. Plant Mol Biol 2001;47:727-38.
Krinitsinaa B, Melnikovac MS, Belenikinc P, Poltronierid A, Santinod AV, Kudryavtsevac, et al. Polymorphism of the KPIA gene sequence in the potato subgenera Potatoe (Sect. Petota, Esolonifera, and Lycopersicum) and Solanum A. A. Mol Biol 2013;47:358–63.
Hartl M, Ashok P, Giri, Harleen Kaur, Ian Baldwin. Serine protease inhibitors specifically defend Solanum nigrum against generalist herbivores but do not influence plant growth and development. Plant Cell 2010;22:4158–75.
Fischer Matthias, Markus Kuckenberg, Robin Kastilan, Jost Muth, Christiane Gebhardt. Novel in vitro inhibitory functions of potato tuber proteinaceous inhibitors. Mol Gen Genom 2015;290:387–98.
Anna Speranskaya, Anastasia Krinitsina A, Kudryavtseva AV, Palmiro Poltronieri, Angelo Santino. The impact of recombination on polymorphism of genes encoding Kunitz-type protease inhibitors in the genus Solanum. Biochimie 2012;94:1687-96.
Zavala JA, Baldwin IT. Fitness benefits of trypsin protease inhibitor expression in Nicotiana attenuata are greater than their costs when plants are attacked. BMC Ecol 2004;4:11.
Moulin MM, Rodrigues R, Ribeiro SFF, Gonçalves LSA, Bento CS, Sudré CP, et al. Trypsin inhibitors from Capsicum baccatum var. pendulum leaves involved in pepper yellow mosaic virus resistance. Genet Mol Res 2014;13:9229-43.
Revina TA, Speranskaya AS, Kladnitskaya GV, Shevelev AB, Valueva TA. Subtilisin protein inhibitor from potato tubers. Biochemistry (Moscow) 2004;69:1092-8.
Pouvreau L, Gruppen H, Piersma SR, van den Broek LAM, van Koningsveld GA, Voragen AGJ. Relative abundance and inhibitory distribution of protease inhibitors in potato juice from cv Elkana. J Agric Food Chem 2001;49:2864–74.
Liu J, Xia KF, Deng YG, Huang XL, Hu BL, Xu X, et al. The nightshade proteinase inhibitor IIb gene is constitutively expressed in glandular trichomes. Plant Cell Physiol 2006;47:1274-84.
Xu ZF, Teng WL, Chye ML. Inhibition of endogenous trypsin and chymotrypsin-like activities in transgenic lettuce expressing heterogeneous proteinase inhibitor SaPIN2a. Planta 2004;218:623-29.
Mosolov VV, Valueva TA. Proteinase inhibitors and their function in plants: a review. Appl Biochem Microbiol 2005;41:227–46.
Silvia S, Ian TB. Systemin in Solanum nigrum. The tomato-homologous polypeptide does not mediate direct defense responses. Plant Physiol 2006;142:1751–8.
Sin SF, Chye ML. Expression of proteinase inhibitor II proteins during floral development in Solanum americanum. Planta 2004;219:1010-22.
Cloutier C, Jean C, Fournier M, Yelle S, Michaud D. Adult colorado potato beetles, Leptinotarsa decemlineata compensate for nutritional stress on Oryza cystatin I-transgenic potato plants by hypertrophic behavior and over-production of insensitive proteases. Arch Insect Biochem Physiol 2000;44:69-81.
Pallavi Sharma, Ambuj Bhushan Jha, Rama Shanker Dubey, Mohammad Pessarakli. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012;26. http://dx.doi.org/ 10.1155/2012/217037
Beekwilder J, Schipper B, Bakker P, Bosch D, Jongsma M. Characterization of potato proteinase inhibitor II reactive site mutants. Eur J Biochem 2000;267:1975-84.
Lison P, Rodrigo I, Conejero V. A novel function for the cathepsin D inhibitor in tomato. Plant Physiol 2006;142:1329–39.
Duan X, Li X, Xue Q, Abo-El-Saad M, Xu D, Wu R. Transgenic rice plants harboring an introduced potato proteinase inhibitor II gene are insect resistant. Nat Biotechnol 1996;14:494-8.
Ari Y, Kusnandar A, Riana Annisa NA. Antifungal activity of kombucha tea against human pathogenic fungi, Asian J Pharm Clin Res 2016;9:253-5.
Julieta RM, Mariana RP, Fernando FM, Gustavo RD, Maria GG. Antimicrobial activity of potato aspartic proteases (StAPs) involves membrane permeabilization. Microbiology 2006;152:2039–47.
Ussuf KK, Laxmi NH, Mitra R. Proteinase inhibitors. Plant-derived genes of insecticidal protein for developing insect-resistant transgenic plants. Curr Sci 2001;7:847-53.
Kim MH, Park SC, Kim JY, Lee SY, Lim HT, Cheong H, et al. Purification and characterization of a heat-stable serine protease inhibitor from the tubers of new potato variety "Golden Valley". Biochem Biophys Res Commun 2006;346:681-6.
Bar-Ziv A, Levy Y, Hak H, Mett A. The tomato yellow leaf curl virus (TYLCV) V2 protein interacts with the host papain-like cysteine protease CYP1. Plant Signaling Behav 2012;7:983-9.
Sanchez-Serrano JJ. Abscisic acid and jasmonic acid activate wound-inducible genes in potato through separate, organ-specific signal transduction pathways. Plant J 1997;11:773-82.
Chaves MM, Flexas J, Pinheiro C. Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 2009;103:551-60.
Broadway RM, Duffey SS. Plant proteinase inhibitors: mechanism of action and effect on the growth and digestive physiology of larval Heliothis zea and Spodoptera exigua. J Insect Physiol 1986b;32:827-33.
Paulraj KL, Kripa RK. Plant protease inhibitors in control of phytophagous insects. Elect J Biotechnol 2002;5:93-109.
Dunsea KM, Kaasc Q, Guarinoa RF, Bartond D, Craikc J, Anderson MA. Molecular basis for the resistance of an insect chymotrypsin to a potato type II proteinase inhibitor. Proc Natl Acad Sci USA 2010;107:15016–21.
Seung Ho Chung, Gary W Felton. Specificity of induced resistance in tomato against specialist lepidopteran and coleopteran species. J Chem Ecol 2004;37:378-86.
Urwin PE, Troth KM, Zubko EI Atkinson HJ. Effective transgenic resistance to Globodera pallida in potato field trials. Mol Breed 2001;8:95–101.
Markus Hartl, Ashok PG, Baldwin IA. The multiple functions of plant serine protease inhibitors. Plant Signaling Behav 2011;6:1009-11.
Remya PP, Sameena U, Bindu PP, Kannan KM. Identification of plant extracts containing protease inhibitors against the gut proteases of Spodoptera mauritia Boisduval (Lepidoptera: Noctuidae). Acta Biol Indica 2013;2:451-5.
Hilder VA, Gatehouse AMR, Sheerman SE, Barker RF, Boulter D. A novel mechanism of insect resistance engineered into tobacco. Nature 1987;300:160–3.
Sane VA, Nath P, Aminuddin, Sane PV. Development of insect-resistant transgenic plants used in plant genes: expression of cowpea trypsin inhibitor in transgenic tobacco plants. Curr Sci 1997;72:741-7.
Novatus F Mushi, Zakaria H Mbwambo, Ester Innocent, Supinya Tewtrakul. Antibacterial, anti-HIV-1 protease and cytotoxic activities of aqueous ethanolic extracts from Combretum adenogonium Steud. Ex A. Rich (Combretaceae). BMC Complementary Altern Med 2012;12:163.
Chen H, Wilkerson CG, Kuchar JA, Phinney BS, Howe GA. Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut. Proc Natl Acad Sci USA 2005;102:19237-42.
Johnson R, Narraez J, Ryan CA. Expression of proteinase inhibitors I and II in transgenic tobacco plants: effects on natural defense against Manduca sexta larvae. Proc Natl Acad Sci USA 1989;86:9871-75.
Heath RG, Mc Donald JT, Christeller M, Lee K, Bateman J, West R, et al. Proteinase inhibitors from Nicotiana alata enhance plant resistance to insect pests. J Insect Physiol 1997;9:833-42.
Charity Julia AA, Merilyn AB, Dennis JW, Malcom Higgins TJV. Transgenic tobacco and peas expressing a proteinase inhibitor from Nicotiana alata have increased insect resistance. Mol Breed 1999;5:357-65.
Plate NA, Valuev TA, Valueva VV. Biospecific haemo sorbents based on proteinase inhibitor. I. Synthesis and properties. Biomaterials 1993;14:51–6.
Jorge AZ, Aparna GP, Klaus Gase, Dequan Hui, Ian TB. Manipulation of Endogenous trypsin proteinase inhibitor production in Nicotiana attenuata demonstrates their function as antiherbivore defenses. Plant Physiol 2004;134:1181–90.
Ali M, Koichi Sugimoto, Abdelaziz Ramadan, Gen-ichiro Arimura. The memory of plant communications for priming anti-herbivore responses. Sci Reports 2013;3:18-25.
Nwaoguikpe RN, Braide W, Ezejiofor TI. The effect of Aloevera plant (aloe barbadensis) extracts on sickle cell blood (HbSS). Afr J Food Sci Technol 2010;1:58-63.
Meenu Krishnan VG, Murugan K. Antioxidant power of purified protease inhibitors from the fruits of Solanum aculeatissimum Jacq. J Pharm 2016;6:231-40.
Vinyas Mayasa, Vijay Kumar R, Banappa SU. Evaluation of phenol content, antioxidant, and proteinase inhibitory activity of plant derived protease inhibitors of eight anti-diabetic plants. Asian J Pharm Clin Res 2016;9:215-9.
Patick AK, Potts KE. Protease inhibitors as antiviral agents. Clin Microbiol Rev 1998;11:614–27.
Tariq Javed, Usman Ali Ashfaq, Sana Riaz, Sidra Rehman, Sheikh Riazuddin.,In vitro antiviral activity of Solanum nigrum against Hepatitis C Virus. Virol J 2011;8:26-34.
Faiza M, Syed Muhammad Saqlan, Tariq M. In vitro and in silico characterization of Solanum lycopersicum wound-inducible proteinase inhibitor-II gene. Turkish J Biol 2013;37:1-10.
Lee JS, Brown WE, Graham JS, Pearce G, Fox EA, Dreher TW, et al. Molecular characterization and phylogenetic studies of a wound-inducible proteinase inhibitor I gene in Lycopersicon species). Proc Natl Acad Sci USA 1986;83:7277-81.
Kumar GN, Lisa OK, Richard K. Zebra chip disease decreases tuber (Solanum tuberosum L.) protein content by attenuating protease inhibitor levels and increasing protease activities. Planta 2015;242:1153–66.
Weeda SM, Kumar GNM, Knowles NR. Protein mobilization from potato tubers during long-term storage and daughter tuber formation. Int J Plant Sci 2011;172:459–70.