Functionally Expression of Metalloproteinase in Taenia solium Metacestode and Its Evaluation for Serodiagnosis of Cysticercosis
Abstract
Background: Parasite proteases have important roles in cleavage of host proteins during the invasion of host tissues and participate in the parasite’s evasion from the host’s immune response. The aim of the present study was to estimate a metalloproteinase properties of Taenia solium metacestode (TsMP) during host-parasite interactions, and evaluate its potential as a serodiagnostic antigen for cysticercosis.
Methods: The cDNA coding for the mature catalytic domain of TsMP was cloned into pGEX-6P-1 expression vector. A recombinant glutathione S-transferase and TsMP fusion protein was induced. After refolding and purification, enzymatic properties of the recombinant metalloproteinase were observed. Immunoblot assay was processed to evaluate its potential as a serodiagnostic antigen for cysticercosis.
Results: The recombinant TsMP protein showed proteolytic activity, which preferred host extracellular matrix proteins such as collagen and fibronectin as degradable substrates. In immunoblot assay, 87.5% of sera from patients with cysticercosis showed strong reactivity. In sera from patients with other parasitic infections and from normal controls, it showed high specificity.
Conclusions: TsMP might be involved in the processing of numerous host proteins and play an important role in the parasite life cycle. A single recombinant TsMP antigen could have a potential value for serodiagnosis of cysticercosis.Silva-Almeida M, Souza-Silva F, Pereira BA, Ribeiro-Guimarães ML, Alves CR. Overview of the organization of protease genes in the genome of Leishmania spp. Parasit Vectors. 2014; 7: 387.
Trap C, Boireau P. Proteases in heminthic parasites. Vet Res. 2000; 31: 461-471.
Williamson AL, Brindley PJ, Knox DP, Hotez PJ, Loukas A. Digestive proteases of blood feeding nematodes. Trends Parasitol. 2003; 19: 417-423.
Lv X, Chen W, Wang X, Li X, Sun J, Deng C, Men J, Tian Y, Zhou C, Lei H, Liang C, Yu X. Molecular characterization and expression of a cysteine protease from Clonorchis sinensis and its application for serodiagnosis of clonorchiasis. Parasitol Res. 2012; 110: 2211-2219.
Rosenthal PJ. Proteases of malaria parasites: new targets for chemotherapy. Emerg Infect Dis. 1998; 4: 49-57.
Cazzulo JJ. Proteinases of Trypoansoma cruzi: patential targets for the chemotherapy of changas desease. Curr Top Med Chem. 2002; 2: 1261-1271.
Klemba M, Goldberg DE. Biological roles of proteases in parasitic protozoa. Annu Rev Biochem. 2002; 71: 275-305.
Janwan P, Intapan PM, Yamasaki H, Laummaunwai P, Sawanyawisuth K, Wongkham C, Tayapiwatana C, Kitkhuandee A, Lulitanond V, Nawa Y, Maleewong W. A recombinant matrix metalloproteinase protein from Gnathostoma spinigerum for serodiagnosis of neurognathostomiasis. Korean J Parasitol. 2013; 51: 751-754.
Williamson AL, Lustigman S, Oksov Y, Deumic V, Plieskatt J, Mendez S, Zhan B, Bottazzi ME, Hotez PJ, Loukas A. Ancylostoma caninum MTP-1, an astacin-like metalloprotease secreted by infective hookworm larvae, is involved in tissue migration. Infect Immun. 2006; 74: 961-967.
Hotez P, Haggerty J, Hawdon J, Milstone L, Gamble HR, Schad G, Richards, F. Mealloproteinases of infective Ancylostoma hookworm larvae and their possible functions in tissue invasion and ecdysis. Infect Immun. 1990; 58: 3883-3892.
Bąska P, Wiśniewski M, Krzyżowska M, Długosz E, Zygner W, Górski P, Wędrychowicz H. Molecular cloning and characterization of in vitro immune response against astacin-like metalloprotease Ace-MTP-2 from Ancylostoma ceylanicum. Exp Parasitol. 2013; 133: 472-482
Haffner A, Guilavogui AZ, Tischendorf FW, Brattig NW. Onchocerca volvulus: Microfilariae secrete elastinolytic and males nonelastinolytic matrix-degrading serine and metalloproteases. Exp Parasitol. 1998; 90: 26-33.
Hong XQ, Bouvier J, Wong MM, Yamagata GYL, Mckerrow JH. Brugia pahangi - Identification and characterization of an aminopeptidase associated with larval molting. Exp Parasitol. 1993; 76: 127-133.
Chirgwin SR, Coleman SU, Porthouse KH, Klei TR. Tissue migration capability of larval and adult Brugia pahangi. J Parasitol. 2006; 92: 46-51.
Polzer M, Overstreet RM, Taraschewski H. Proteinase activity in the plerocercoid of Proteocephalus ambloplitis (Cestoda). Parasitology. 1994; 109: 209-213.
Vázquez-Lopez C, Armas-Serra C, Gimenez-Pardo C, Rodriguez-Caaberio F. Proteolytic activity of the Gymnorhynchus gigas plerocercoid: purification and properties of a collagenase from the crude extract. Parasitol Res. 1999; 85: 64-70.
Culley FJ, Brown A, Conroy DM, Sabroe I, Pritchard DI, Williams TJ. Eotaxin is specifically cleaved by hookworm metalloproteases preventing its action in vitro and in vivo. J Immunol. 2000; 165: 6447-6453.
Blelloch R, Kimble J. Control of organ shape by a secreted metalloproteinase in the nematode Caenorhabditis elegans. Nature. 1999; 399: 586-590.
Moerman DG. Organ morphogenesis: a metalloprotease prepares the way. Curr Biol. 1999; 9: 701-703.
Altincicek B, Fischer M, Fischer M, Lüersen K, Boll M, Wenzel U, Vilcinskas A. Role of matrix metalloproteinase ZMP-2 in pathogen resistance and development in Caenorhabditis elegans. Dev Comp Immunol. 2010; 34: 1160-1169.
Coombs GH, Mottram JC. Parasite proteinases and amino acid metabolism: possibilities for chemotherapeutic exploitation. Parasitology. 1997; 114: S 61-80.
Smith WD, Newlands GFJ, Smith SK, Pettit D, Skuce PJ. Metalloendopeptidases from the intestinal border of Haemonchus contortus as protective antigens for sheep. Parasite Immunol. 2003; 25: 313-323.
Deprez-Poulain R, Flipo M, Piveteau C, Leroux F, Dassonneville S, Florent I, Maes L, Cos P, Deprez B. Structure-activity relationships and blood distribution of antiplasmodial aminopeptidase-1 inhibitors. J Med Chem 2012; 55: 10909-10917.
Wandra T, Ito A, Swastika K, Sako Y, Okamoto M. Taeniases and cysticercosis in Indonesia: past and present situations. Parasitology. 2013; 140: 1608-1616.
Hawk MW, Shahlaie K, Kim KD, Theis JH. Neurocystercosis: a review. Surg Neurol. 2005; 63: 123-132.
Hancock K, Khan A, Williams FB, Yushak ML, Pattabhi S, Noh J, Tsang VC. Characterization of the 8-kilodalton antigens of Taenis solium metacestodes and evaluation of the use in an enzyme-linked immunosorbot assay for serodiagnosis. J Clin Microbiol. 2003; 41: 2577-2586.
White AC Jr. Neurocysticercosis: updates on epidemiology, pathogenesis, diagnosis, and management. Annu Rev Med. 2000; 51: 187-206.
Willingham AL, Engels D. Control of Taenia solium cysticercosis/taeniosis. Adv Parasitol. 2006; 61: 509-566.
Cai GB, Bae YA, Kim SH, Na BK, Kim TS, Jiang MS, Kong Y. A membrane-associated metalloprotease of Taenia solium metacestode structurally related to the FACE-1/Ste24p protease family. Int J Parasitol. 2006; 36: 925-935.
Long X, Gou Y, Luo M, Zhang S, Zhang H, Bai L, Wu S, He Q, Chen K, Huang A, Zhou J, Wang D. Soluble expression, purification, and characterization of active recombinant human tissue plasminogen activator by auto-induction in E. coli. BMC Biotechnol. 2015; 15: 13.
Kroger M, Tschesche H. Cloning, expression and activation of a truncated 92-kDa gelatinase minienzyme. Gene. 1997; 196: 175-180.
Zhao X, Acheampong DO, Wang Y, Tang M, Xie W, Chen Z, Wang M, Zhang J. Efficient In Vitro Refolding and Characterization of Major Histocompatibility Complex Class I-Related Chain Molecules A (MICA) and Natural Killer Group 2 Member D (NKG2D) Expressed in E. coli. Protein Pept Lett. 2015 ; 22: 460-469.
Secades P, Alvarez B, Guijarro JA. Purification and properties of a new psychrophilic metalloprotease (Fpp2) in the fish pathogen Flavobacterium psychrophilum. FEMS Microbiol Lett. 2003 ; 226: 273-279.
Wang WJ, Shih CH, Huang TF. A novel P-І class metalloproteinase with broad substrate-cleaving activity, agkislysin, from Agkistrodon acutus venom. Biochem Biophys Res Commun. 2004; 324: 224-230.
Larsen KS, Auld DS. Characterization of an inhibitory metal binding site in carboxypeptidase A. Biochemistry. 1991; 30: 2613-2618.
Windle HJ, Kelleher D. Identification and characterization of a metalloprotease activity from Helicobacter pylori. Infect Immun. 1997; 65: 3132-3137.
Kong Y, Chung YB, Cho SY, Choi SH, Kang SY. Characterization of three neutral proteases of Spirometra mansoni plerocercoid. Parasitology. 1994; 108: 359-368.
Ihara S, Nishiwaki K. Stage-specific activation of MIG-17/ADAMTS controls cell migration in Caenorhabditis elegans. FEBS J. 2008; 275: 4296-4305.
Roggério A, Sambiase NV, Palomino SA, de Castro MA, da Silva ES, Stolf NG, de Lourdes Higuchi M. Correlation of bacterial coinfection versus matrix metalloproteinase 9 and tissue inhibitor of metalloproteinase 1 expression in aortic aneurysm and atherosclerosis. Ann Vasc Surg. 2013; 27: 964-971.
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Issue | Vol 11 No 1 (2016) | |
Section | Original Article(s) | |
Keywords | ||
Taenia solium Metalloproteinase Host substrate Serodiagnosis Cysticercosis |
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