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Identification of a novel PYP-1 gene in Sarcoptes scabiei and its potential as a serodiagnostic candidate by indirect-ELISA

Published online by Cambridge University Press:  08 November 2017

Jing Xu ,
Xing Huang ,
Manli He ,
Yongjun Ren ,
Nengxing Shen ,
Chunyan Li ,
Ran He ,
Yue Xie ,
Xiaobin Gu  and
Bo Jing
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Jing Xu
Affiliation:
Department of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, China
Xing Huang
Affiliation:
Chengdu Agricultural College, Chengdu 611130, China
Manli He
Affiliation:
Department of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, China
Yongjun Ren
Affiliation:
Sichuan Animal Sciences Academy, Sichuan Chengdu 610066, China Animal Breeding and Genetics key Laboratory of Sichuan Province, Sichuan Chengdu 610066, China
Nengxing Shen
Affiliation:
Department of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, China
Chunyan Li
Affiliation:
Department of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, China
Ran He
Affiliation:
Department of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, China
Yue Xie
Affiliation:
Department of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, China
Xiaobin Gu
Affiliation:
Department of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, China
Bo Jing
Affiliation:
Department of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, China
Xuerong Peng
Affiliation:
College of Science, Sichuan Agricultural University, Ya'an 625014, China
Guangyou Yang*
Affiliation:
Department of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, China
*
Author for Correspondence: Guangyou Yang, E-mail: guanyouyang@hotmail.com; guangyou1963@aliyun.com
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Abstract

Scabies is a parasitic disease caused by the ectoparasite Sarcoptes scabiei, affecting different mammalian species, including rabbits, worldwide. In the present study, we cloned and expressed a novel inorganic pyrophosphatase, Ssc-PYP-1, from S. scabiei var. cuniculi. Immunofluorescence staining showed that native Ssc-PYP-1 was localized in the tegument around the mouthparts and the entire legs, as well as in the cuticle of the mites. Interestingly, obvious staining was also observed on the fecal pellets of mites and in the integument of the mites. Based on its good immunoreactivity, an indirect enzyme-linked immunosorbent assay (ELISA) using recombinant Ssc-PYP-1 (rSsc-PYP-1) as the capture antigen was developed to diagnose sarcoptic mange in naturally infected rabbits; the assay had a sensitivity of 92·0% and specificity of 93·6%. Finally, using the rSsc-PYP-1-ELISA, the Ssc-PYP-1 antibody from 10 experimentally infected rabbits could be detected from 1 week post-infection. This is the first report of S. scabiei inorganic pyrophosphatase and the protein could serve as a potential serodiagnostic candidate for sarcoptic mange in rabbits.

Keywords

Sarcoptes scabieiinorganic pyrophosphatasefluorescence immunohistochemistryserodiagnosisindirect ELISA
Type
Research Article
Information
Parasitology , Volume 145 , Issue 6 , May 2018 , pp. 752 - 761
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Copyright
Copyright © Cambridge University Press 2017 

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References

Alasaad, S, Rossi, L, Heukelbach, J, Pérez, JM, Hamarsheh, O, Otiende, M and Zhu, XQ (2013) The neglected navigating web of the incomprehensibly emerging and re-emerging Sarcoptes mite. Infection, Genetics and Evolution 17, 253–259.CrossRefGoogle ScholarPubMed
Angelone-Alasaad, S, Min, AM, Pasquetti, M, Alagaili, AN, D'Amelio, S, Berrilli, F, Obanda, V, Gebely, MA, Soriguer, RC and Rossi, L (2015) Universal conventional and real-time PCR diagnosis tools for Sarcoptes scabiei. Parasites & Vectors 8, 587.CrossRefGoogle ScholarPubMed
Arlian, LG, Morgan, MS, Rapp, CM and Vyszenski-Moher, DL (1996) The development of protective immunity in canine scabies. Veterinary Parasitology 62, 133–142.CrossRefGoogle ScholarPubMed
Bates, P (1999) Inter-and intra-specific variation within the genus Psoroptes (Acari: Psoroptidae). Veterinary Parasitology 83, 201–217.CrossRefGoogle ScholarPubMed
Beckham, SA, Boyd, SE, Reynolds, S, Willis, C, Johnstone, M, Mika, A, Simerská, P, Wijeyewickrema, LC, Smith, AI and Kemp, DJ (2009) Characterization of a serine protease homologous to house dust mite group 3 allergens from the scabies mite Sarcoptes scabiei. Journal of Biological Chemistry 284, 34413–34422.CrossRefGoogle ScholarPubMed
Bornstein, S, Zakrisson, G and Thebo, P (1994) Clinical picture and antibody response to experimental Sarcoptes scabiei var. Vulpes infection in red foxes (Vulpes vulpes). Acta Veterinaria Scandinavica 36, 509–519.CrossRefGoogle Scholar
Casais, R, Goyena, E, Martínez-Carrasco, C, de Ybáñez, RR, de Vega, FA, Ramis, G, Prieto, J and Berriatua, E (2013) Variable performance of a human derived Sarcoptes scabiei recombinant antigen ELISA in swine mange diagnosis. Veterinary Parasitology 197, 397–403.CrossRefGoogle ScholarPubMed
Casais, R, Dalton, KP, Millán, J, Balseiro, A, Oleaga, Á, Solano, P, Goyache, F, Prieto, JM and Parra, F (2014) Primary and secondary experimental infestation of rabbits (Oryctolagus cuniculus) with Sarcoptes scabiei from a wild rabbit: factors determining resistance to reinfestation. Veterinary Parasitology 203, 173–183.CrossRefGoogle ScholarPubMed
Casais, R, Millán, J, Rosell, JM, Dalton, KP and Prieto, JM (2015) Evaluation of an ELISA using recombinant Ssλ20ΔB3 antigen for the serological diagnosis of Sarcoptes scabiei infestation in domestic and wild rabbits. Veterinary Parasitology 214, 315–321.CrossRefGoogle ScholarPubMed
Chosidow, O (2000) Scabies and pediculosis. The Lancet 355, 819–826.CrossRefGoogle ScholarPubMed
Crowther, J and Walker, J (2009) The ELISA Guidebook, 2nd edn. Humana Press, New Jersey, US.CrossRefGoogle Scholar
Engelman, D, Kiang, K, Chosidow, O, McCarthy, J, Fuller, C, Lammie, P, Hay, R, Steer, A and Members of the International Alliance for the Control of Scabies (IACS) (2013) Toward the global control of human scabies: introducing the international alliance for the control of scabies. PLoS Neglected Tropical Diseases 7, e2167.CrossRefGoogle ScholarPubMed
Espiau, B, Lemercier, G, Ambit, A, Bringaud, F, Merlin, G, Baltz, T and Bakalara, N (2006) A soluble pyrophosphatase, a key enzyme for polyphosphate metabolism in Leishmania. Journal of Biological Chemistry 281, 1516–1523.CrossRefGoogle ScholarPubMed
Fairchild, TA and Patejunas, G (1999) Cloning and expression profile of human inorganic pyrophosphatase. Biochimica et Biophysica Acta (BBA) – Gene Structure and Expression 1447, 133–136.CrossRefGoogle ScholarPubMed
Fukuyama, S, Nishimura, T, Yotsumoto, H, Gushi, A, Tsuji, M, Kanekura, T and Matsuyama, T (2010) Diagnostic usefulness of a nested polymerase chain reaction assay for detecting Sarcoptes scabiei DNA in skin scrapings from clinically suspected scabies. British Journal of Dermatology 163, 892–894.CrossRefGoogle ScholarPubMed
Galizzi, M, Bustamante, JM, Fang, J, Miranda, K, Soares Medeiros, LC, Tarleton, RL and Docampo, R (2013) Evidence for the role of vacuolar soluble pyrophosphatase and inorganic polyphosphate in Trypanosoma cruzi persistence. Molecular Microbiology 90, 699–715.CrossRefGoogle ScholarPubMed
Haas, N and Sterry, W (2001) The use of ELM to monitor the success of antiscabietic treatment. Archives of Dermatology 137, 1656–1657.Google ScholarPubMed
Hay, R, Steer, A, Engelman, D and Walton, S (2012) Scabies in the developing world—its prevalence, complications, and management. Clinical Microbiology and Infection 18, 313–323.CrossRefGoogle ScholarPubMed
Hay, RJ, Johns, NE, Williams, HC, Bolliger, IW, Dellavalle, RP, Margolis, DJ, Marks, R, Naldi, L, Weinstock, MA and Wulf, SK (2014) The global burden of skin disease in 2010: an analysis of the prevalence and impact of skin conditions. Journal of Investigative Dermatology 134, 1527–1534.CrossRefGoogle ScholarPubMed
He, R, Shen, N, Lin, H, Gu, X, Lai, W, Peng, X and Yang, G (2017) Molecular characterization of calmodulin from Sarcoptes scabiei. Parasitology International 66, 1–6.CrossRefGoogle ScholarPubMed
Heikinheimo, P, Tuominen, V, Ahonen, AK, Teplyakov, A, Cooperman, B, Baykov, A, Lahti, R and Goldman, A (2001) Toward a quantum-mechanical description of metal-assisted phosphoryl transfer in pyrophosphatase. Proceedings of the National Academy of Sciences of the United States of America 98, 3121–3126.CrossRefGoogle Scholar
Heinonen, JK (2001) Biological Role of Inorganic Pyrophosphate. Springer, Boston, MA.CrossRefGoogle Scholar
Heukelbach, J, Wilcke, T, Winter, B and Feldmeier, H (2005) Epidemiology and morbidity of scabies and pediculosis capitis in resource-poor communities in Brazil. British Journal of Dermatology 153, 150–156.CrossRefGoogle ScholarPubMed
Islam, MK, Miyoshi, T, Kasuga-Aoki, H, Isobe, T, Arakawa, T, Matsumoto, Y and Tsuji, N (2003) Inorganic pyrophosphatase in the roundworm Ascaris and its role in the development and molting process of the larval stage parasites. European Journal of Biochemistry 270, 2814–2826.CrossRefGoogle ScholarPubMed
Islam, MK, Miyoshi, T, Yamada, M and Tsuji, N (2005) Pyrophosphatase of the roundworm Ascaris suum plays an essential role in the worm's molting and development. Infection and Immunity 73, 1995–2004.CrossRefGoogle ScholarPubMed
Islam, MK, Miyoshi, T, Yamada, M, Alim, MA, Huang, X, Motobu, M and Tsuji, N (2006) Effect of piperazine (diethylenediamine) on the moulting, proteome expression and pyrophosphatase activity of Ascaris suum lung-stage larvae. Acta Tropica 99, 208–217.CrossRefGoogle ScholarPubMed
Jacobson, R (1998) Validation of serological assays for diagnosis of infectious diseases. Revue Scientifique et Technique (International Office of Epizootics) 17, 469–526.Google ScholarPubMed
Jayaraj, R, Hales, B, Viberg, L, Pizzuto, S, Holt, D, Rolland, JM, O'Hehir, RE, Currie, BJ and Walton, SF (2011) A diagnostic test for scabies: IgE specificity for a recombinant allergen of Sarcoptes scabiei. Diagnostic Microbiology and Infectious Disease 71, 403–407.CrossRefGoogle ScholarPubMed
Ko, KM, Lee, W, Yu, JR and Ahnn, J (2007) PYP-1, inorganic pyrophosphatase, is required for larval development and intestinal function in C. elegans. FEBS Letters 581, 5445–5453.CrossRefGoogle ScholarPubMed
Lacarrubba, F, Musumeci, ML, Caltabiano, R, Impallomeni, R, West, DP and Micali, G (2001) High-magnification videodermatoscopy: a new noninvasive diagnostic tool for scabies in children. Pediatric Dermatology 18, 439–441.CrossRefGoogle ScholarPubMed
Lahti, R, Kolakowski, LF, Heinonen, J, Vihinen, M, Pohjanoksa, K and Cooperman, BS (1990) Conservation of functional residues between yeast and E. coli inorganic pyrophosphatases. Biochimica et Biophysica Acta (BBA) – Protein Structure and Molecular Enzymology 1038, 338–345.CrossRefGoogle ScholarPubMed
Lemercier, G, Espiau, B, Ruiz, FA, Vieira, M, Luo, S, Baltz, T, Docampo, R and Bakalara, N (2004) A pyrophosphatase regulating polyphosphate metabolism in acidocalcisomes is essential for Trypanosoma brucei virulence in mice. Journal of Biological Chemistry 279, 3420–3425.CrossRefGoogle ScholarPubMed
Ljunggren, E, Bergström, K, Morrison, D and Mattsson, J (2006) Characterization of an atypical antigen from Sarcoptes scabiei containing an MADF domain. Parasitology 132, 117–126.CrossRefGoogle ScholarPubMed
Lu, Y, Jia, R, Zhang, Z, Wang, M, Xu, Y, Zhu, D, Chen, S, Liu, M, Yin, Z and Chen, X (2014) In vitro expression and development of indirect ELISA for capsid protein of duck circovirus without nuclear localization signal. International Journal of Clinical and Experimental Pathology 7, 4938.Google ScholarPubMed
Mahmood, W, Viberg, LT, Fischer, K, Walton, SF and Holt, DC (2013) An aspartic protease of the scabies mite Sarcoptes scabiei is involved in the digestion of host skin and blood macromolecules. PLoS Neglected Tropical Diseases 7, e2525.CrossRefGoogle ScholarPubMed
McDonald, M, Currie, BJ and Carapetis, JR (2004) Acute rheumatic fever: a chink in the chain that links the heart to the throat? The Lancet Infectious Diseases 4, 240–245.CrossRefGoogle Scholar
Micali, G, Lacarrubba, F and Lo, GG (1999) Scraping versus videodermatoscopy for the diagnosis of scabies: a comparative study. Acta Dermato-Venereologica 79, 396.Google ScholarPubMed
Micali, G, Lacarrubba, F and Tedeschi, A (2004) Videodermatoscopy enhances the ability to monitor efficacy of scabies treatment and allows optimal timing of drug application. Journal of the European Academy of Dermatology and Venereology 18, 153–154.CrossRefGoogle ScholarPubMed
Mimouni, D, Ankol, O, Davidovitch, N, Gdalevich, M, Zangvil, E and Grotto, I (2003) Seasonality trends of scabies in a young adult population: a 20-year follow-up. British Journal of Dermatology 149, 157–159.CrossRefGoogle Scholar
Morgan, MS and Arlian, LG (2006) Enzymatic activity in extracts of allergy-causing astigmatid mites. Journal of Medical Entomology 43, 1200–1207.CrossRefGoogle ScholarPubMed
Ráez-Bravo, A, Granados, JE, Serrano, E, Dellamaria, D, Casais, R, Rossi, L, Puigdemont, A, Cano-Manuel, FJ, Fandos, P and Pérez, JM (2016) Evaluation of three enzyme-linked immunosorbent assays for sarcoptic mange diagnosis and assessment in the Iberian ibex, Capra pyrenaica. Parasites & Vectors 9, 558.CrossRefGoogle ScholarPubMed
Rampton, M, Walton, SF, Holt, DC, Pasay, C, Kelly, A, Currie, BJ, McCarthy, JS and Mounsey, KE (2013) Antibody responses to Sarcoptes scabiei apolipoprotein in a porcine model: relevance to immunodiagnosis of recent infection. PLoS ONE 8, e65354.CrossRefGoogle Scholar
Rider, SD Jr., Morgan, MS and Arlian, LG (2015) Draft genome of the scabies mite. Parasit Vectors 8, 585.CrossRefGoogle ScholarPubMed
Rodríguez-Cadenas, F, Carbajal-González, M, Fregeneda-Grandes, J, Aller-Gancedo, J, Huntley, J and Rojo-Vázquez, F. A. (2010a). Development and evaluation of an antibody ELISA for sarcoptic mange in sheep and a comparison with the skin-scraping method. Preventive Veterinary Medicine 96, 82–92.CrossRefGoogle Scholar
Rodriguez-Cadenas, F, Carbajal-González, M, Fregeneda-Grandes, J, Aller-Gancedo, J. and Rojo-Vázquez, F. A. (2010b). Clinical evaluation and antibody responses in sheep after primary and secondary experimental challenges with the mange mite Sarcoptes scabiei var. ovis. Veterinary Immunology and Immunopathology 133, 109–116.CrossRefGoogle ScholarPubMed
Sanchez, J, Dohoo, IR, Markham, F, Leslie, K and Conboy, G (2002) Evaluation of the repeatability of a crude adult indirect Ostertagia ostertagi ELISA and methods of expressing test results. Veterinary Parasitology 109, 75–90.CrossRefGoogle ScholarPubMed
Sarasa, M, Rambozzi, L, Rossi, L, Meneguz, PG, Serrano, E, Granados, J.-E., González, FJ, Fandos, P, Soriguer, RC and Gonzalez, G (2010) Sarcoptes scabiei: specific immune response to sarcoptic mange in the Iberian ibex Capra pyrenaica depends on previous exposure and sex. Experimental Parasitology 124, 265–271.CrossRefGoogle ScholarPubMed
Steer, AC, Jenney, AW, Kado, J, Batzloff, MR, La Vincente, S, Waqatakirewa, L, Mulholland, EK and Carapetis, JR (2009) High burden of impetigo and scabies in a tropical country. PLoS Neglected Tropical Diseases 3, e467.CrossRefGoogle Scholar
Tamura, K, Peterson, D, Peterson, N, Stecher, G, Nei, M and Kumar, S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.CrossRefGoogle ScholarPubMed
Tarigan, S (2014) Antibody response in naïve and sensitised goats infested by Sarcoptes scabiei. Jurnal Ilmu Ternak dan Veteriner 9, 258–265.Google Scholar
Thompson, JD, Gibson, TJ, Plewniak, F, Jeanmougin, F and Higgins, DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.CrossRefGoogle ScholarPubMed
Van der Heijden, H, Rambags, P, Elbers, A, Van Maanen, C and Hunneman, W (2000) Validation of ELISAs for the detection of antibodies to Sarcoptes scabiei in pigs. Veterinary Parasitology 89, 95–107.CrossRefGoogle ScholarPubMed
Walton, SF and Currie, BJ (2007) Problems in diagnosing scabies, a global disease in human and animal populations. Clinical Microbiology Reviews 20, 268–279.CrossRefGoogle ScholarPubMed
Wilson, P, Slade, R, Currie, BJ, Walton, SF, Holt, DC, Fischer, K, Allen, GE, Wilson, D and Kemp, DJ (2003) Mechanisms for a novel immune evasion strategy in the scabies mite Sarcoptes scabiei: a multigene family of inactivated serine proteases. Journal of Investigative Dermatology 121, 1419–1424.CrossRefGoogle Scholar
Worth, C, Heukelbach, J, Fengler, G, Walter, B, Liesenfeld, O and Feldmeier, H (2012) Impaired quality of life in adults and children with scabies from an impoverished community in Brazil. International Journal of Dermatology 51, 275–282.CrossRefGoogle ScholarPubMed
Xie, Y, Chen, S, Yan, Y, Zhang, Z, Li, D, Yu, H, Wang, C, Nong, X, Zhou, X and Gu, X (2013) Potential of recombinant inorganic pyrophosphatase antigen as a new vaccine candidate against Baylisascaris schroederi in mice. Veterinary Research 44, 90.CrossRefGoogle ScholarPubMed
Yang, YY, Ko, TP, Chen, CC, Huang, G, Zheng, Y, Liu, W, Wang, I, Ho, MR, Hsu, S. T. D., O'Dowd, B, Huff, HC, Huang, CH, Docampo, R, Oldfield, E and Guo, RT (2016) Structures of trypanosome vacuolar soluble pyrophosphatases: antiparasitic drug targets. ACS Chemical Biology 11, 1362–1371.CrossRefGoogle ScholarPubMed
Zhang, R, Zheng, W, Wu, X, Jise, Q, Ren, Y, Nong, X, Gu, X, Wang, S, Peng, X and Lai, S (2013) Characterisation and analysis of thioredoxin peroxidase as a potential antigen for the serodiagnosis of sarcoptic mange in rabbits by dot-ELISA. BMC Infectious Diseases 13, 336.CrossRefGoogle ScholarPubMed
Zheng, Y, He, R, He, M, Gu, X, Wang, T, Lai, W, Peng, X and Yang, G (2016) Characterization of Sarcoptes scabiei cofilin gene and assessment of recombinant cofilin protein as an antigen in indirect-ELISA for diagnosis. BMC Infectious Diseases 16, 21.CrossRefGoogle ScholarPubMed