Skip to main content Accessibility help
×
Home
Hostname: page-component-7ccbd9845f-l8x48 Total loading time: 0.588 Render date: 2023-01-30T22:51:47.409Z Has data issue: true Feature Flags: { "useRatesEcommerce": false } hasContentIssue true

Article contents

A member of the HSP90 family from ovine Babesia in China: molecular characterization, phylogenetic analysis and antigenicity

Published online by Cambridge University Press:  09 July 2015

GUIQUAN GUAN
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Xujiaping 1, Lanzhou, Gansu 730046, People's Republic of China LUNAM Université, Oniris, Ecole nationale vétérinaire, agroalimentaire et de l'alimentation Nantes-Atlantique, UMR Biologie, Epidémiologie et Analyse de Risque en santé animale, CS 40706, F-44307 Nantes, France INRA, UMR1300, F-44307 Nantes, France
JUNLONG LIU
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Xujiaping 1, Lanzhou, Gansu 730046, People's Republic of China
AIHONG LIU
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Xujiaping 1, Lanzhou, Gansu 730046, People's Republic of China
YOUQUAN LI
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Xujiaping 1, Lanzhou, Gansu 730046, People's Republic of China
QINGLI NIU
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Xujiaping 1, Lanzhou, Gansu 730046, People's Republic of China
JINLIANG GAO
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Xujiaping 1, Lanzhou, Gansu 730046, People's Republic of China
JIANXUN LUO
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Xujiaping 1, Lanzhou, Gansu 730046, People's Republic of China
ALAIN CHAUVIN
Affiliation:
LUNAM Université, Oniris, Ecole nationale vétérinaire, agroalimentaire et de l'alimentation Nantes-Atlantique, UMR Biologie, Epidémiologie et Analyse de Risque en santé animale, CS 40706, F-44307 Nantes, France INRA, UMR1300, F-44307 Nantes, France
HONG YIN*
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Xujiaping 1, Lanzhou, Gansu 730046, People's Republic of China Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou 225009, People's Republic of China
EMMANUELLE MOREAU*
Affiliation:
LUNAM Université, Oniris, Ecole nationale vétérinaire, agroalimentaire et de l'alimentation Nantes-Atlantique, UMR Biologie, Epidémiologie et Analyse de Risque en santé animale, CS 40706, F-44307 Nantes, France INRA, UMR1300, F-44307 Nantes, France
*
*Corresponding authors. Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Xujiaping 1, Lanzhou, Gansu 730046, People's Republic of China; LUNAM Université, Oniris – Site de la Chantrerie, UMR 1300 BioEpAR, Route de Gachet, BP 40706, F-44307 Nantes Cedex 03, France. E-mail: yinhong@caas.cn; emmanuelle.moreau@oniris-nantes.fr
*Corresponding authors. Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Xujiaping 1, Lanzhou, Gansu 730046, People's Republic of China; LUNAM Université, Oniris – Site de la Chantrerie, UMR 1300 BioEpAR, Route de Gachet, BP 40706, F-44307 Nantes Cedex 03, France. E-mail: yinhong@caas.cn; emmanuelle.moreau@oniris-nantes.fr

Summary

Heat shock protein 90 (HSP90) is a key component of the molecular chaperone complex essential for activating many signalling proteins involved in the development and progression of pathogenic cellular transformation. A Hsp90 gene (BQHsp90) was cloned and characterized from Babesia sp. BQ1 (Lintan), an ovine Babesia isolate belonging to Babesia motasi-like group, by screening a cDNA expression library and performing rapid amplification of cDNA ends. The full-length cDNA of BQHsp90 is 2399 bp with an open reading frame of 2154 bp encoding a predicted 83 kDa polypeptide with 717 amino acid residues. It shows significant homology and similar structural characteristics to Hsp90 of other apicomplex organisms. Phylogenetic analysis, based on the HSP90 amino acid sequences, showed that the Babesia genus is clearly separated from other apicomplexa genera. Five Chinese ovine Babesia isolates were divided into 2 phylogenetic clusters, namely Babesia sp. Xinjiang (previously designated a new species) cluster and B. motasi-like cluster which could be further divided into 2 subclusters (Babesia sp. BQ1 (Lintan)/Babesia sp. Tianzhu and Babesia sp. BQ1 (Ningxian)/Babesia sp. Hebei). Finally, the antigenicity of rBQHSP90 protein from prokaryotic expression was also evaluated using western blot and enzyme-linked immunosorbent assay (ELISA).

Type
Research Article
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ahmed, J. S., Luo, J., Schnittger, L., Seitzer, U., Jongejan, F. and Yin, H. (2006). Phylogenetic position of small ruminant infecting piroplasms. Annals of the New York Academy of Sciences 1081, 498504.CrossRefGoogle ScholarPubMed
Bai, Q., Liu, G. Y., Liu, D. K., Ren, J. and Li, X. (2002). Isolation and preliminary characterization of a large Babesia sp. from sheep and goats in the eastern part of Gansu Province, China. Parasitology Research 88, S16S21.CrossRefGoogle ScholarPubMed
Brandau, S., Dresel, A. and Clos, J. (1995). High constitutive levels of heat-shock proteins in human-pathogenic parasites of the genus Leishmania . Biochemical Journal 310, 225232.CrossRefGoogle ScholarPubMed
Buchanan, K. L. (2000). Stress and the evolution of condition-dependent signals. Trends in Ecology and Evolution 15, 156160.CrossRefGoogle ScholarPubMed
Cavalier-Smith, T. and Chao, E. E. (2003). Phylogeny of choanozoa, apusozoa and other protozoa and early eukaryote megaevolution. Journal of Molecular Evolution 56, 540563.CrossRefGoogle ScholarPubMed
Chen, D. M. (1982). Investigations on ovine piroplasmosis (in Chinese). Chinese Journal of Veterinary Science and Technology 3, 3132.Google Scholar
Crane, C. A., Han, S. J., Ahn, B., Oehlke, J., Kivett, V., Fedoroff, A., Butowski, N., Chang, S. M., Clarke, J., Berger, M. S., McDermott, M. W., Prados, M. D. and Parsa, A. T. (2013). Individual patient-specific immunity against high-grade glioma after vaccination with autologous tumor derived peptides bound to the 96 KD chaperone protein. Clinical Cancer Research 19, 205214.CrossRefGoogle ScholarPubMed
De Andrade, C. R., Kirchhoff, L. V., Donelson, J. E. and Otsu, K. (1992). Recombinant Leishmania Hsp90 and Hsp70 are recognized by sera from visceral leishmaniasis patients but not Chagas’ disease patients. Journal of Clinical Microbiology 30, 330335.Google Scholar
De Luca, F., Di Vito, M., Fanelli, E., Reyes, A., Greco, N. and De Giorgi, C. (2009). Characterization of the heat shock protein 90 gene in the plant parasitic nematode Meloidogyne artiellia and its expression as related to different developmental stages and temperature. Gene 440, 1622.CrossRefGoogle ScholarPubMed
Echeverria, P. C., Matrajt, M., Harb, O. S., Zappia, M. P., Costas, M. A., Roos, D. S., Dubremetz, J. F. and Angel, S. O. (2005). Toxoplasma gondii Hsp90 is a potential drug target whose expression and subcellular localization are developmentally regulated. Journal of Molecular Biology 350, 723734.CrossRefGoogle ScholarPubMed
Feng, Y. Y., Dearen, T., Cama, V. and Xiao, L. H. (2009). 90-kilodalton heat shock protein, Hsp90, as a target for genotyping Cryptosporidium spp. known to infect humans. Eukaryotic Cell 8, 478482.CrossRefGoogle ScholarPubMed
Fukuda, Y. and Endoh, H. (2008). Phylogenetic analyses of the dinoflagellate Noctiluca scintillans based on beta-tubulin and Hsp90 genes. European Journal of Protistology 44, 2733.CrossRefGoogle ScholarPubMed
Gerhards, J., Ebel, T., Dobbelaere, D. D. A. E., Morzaria, S. P., Musoke, A. J., Williams, R. O. and Lipp, J. (1994). Sequence and expression of a 90-kilodalton heat-shock protein family member of Theileria parva . Molecular and Biochemical Parasitology 68, 235246.CrossRefGoogle ScholarPubMed
Girvitz, T. L., Ouimet, P. M. and Kapoor, M. (2000). Heat shock protein 80 of Neurospora crassa: sequence analysis of the gene and expression during the asexual phase. Canadian Journal of Microbiology 46, 981991.CrossRefGoogle ScholarPubMed
Gou, H. T., Guan, G. Q., Liu, A. H., Ma, M. L., Chen, Z., Liu, Z. J., Ren, Q. Y., Li, Y. Q., Yang, J. F., Yin, H. and Luo, J. X. (2013 a). Coevolutionary analyses of the relationships between piroplasmids and their hard tick hosts. Ecology and Evolution 3, 29852993.CrossRefGoogle ScholarPubMed
Gou, H. T., Guan, G. Q., Ma, M. L., Liu, A. H., Liu, Z. J., Ren, Q. Y., Li, Y. Q., Yang, J. F., Chen, Z., Yin, H. and Luo, J. X. (2013 b). Phylogenetic analysis based on 28S rRNA of Babesia spp. in ruminants in China. Experimental and Applied Acarology 59, 463472.CrossRefGoogle Scholar
Guan, G. Q., Yin, H., Luo, J. X., Lu, W. S., Zhang, Q. C., Ma, M. L., Yuan, G. L., Lu, B. Y., Wang, Y. J. and Muhe, T. E. (2001). Isolation of a large ovine Babesia sp. in Xinjiang, China (in Chinese). Chinese Journal of Veterinary Science of Technology 31, 3536.Google Scholar
Guan, G. Q., Yin, H., Luo, J. X., Lu, W. S., Zhang, Q. C., Gao, Y. L. and Lu, B. Y. (2002). Transmission of Babesia sp. to sheep with field-collected Haemaphysalis qinghaiensis . Parasitology Research 88, S22S24.CrossRefGoogle ScholarPubMed
Guan, G. Q., Chauvin, A., Rogniaux, H., Luo, J. X., Yin, H. and Moreau, E. (2010 a). Merozoite proteins from Babesia sp. BQ1 (Lintan) as potential antigens for serodiagnosis by ELISA. Parasitology 137, 927938.CrossRefGoogle ScholarPubMed
Guan, G. Q., Moreau, E., Brisseau, N., Luo, J. X., Yin, H. and Chauvin, A. (2010 b) Determination of erythrocyte susceptibility of Chinese sheep (Tan mutton breed) and French sheep (Vendéen breed) to Babesia sp. BQ1 (Lintan) by in vitro culture. Veterinary Parasitology 170, 3743.CrossRefGoogle ScholarPubMed
Guan, G. Q., Moreau, E., Liu, J. L., Ma, M. L., Rogniaux, H., Liu, A. H., Niu, Q. L., Li, Y. Q., Ren, Q. Y., Luo, J. X., Chauvin, A. and Yin, H. (2012 a). BQP35 is a novel member of the intrinsically unstructured protein (IUP) family which is a potential antigen for the sero-diagnosis of Babesia sp. BQ1 (Lintan) infection. Veterinary Parasitology 187, 421430.CrossRefGoogle ScholarPubMed
Guan, G. Q., Ma, M. L., Liu, A. H., Ren, Q. Y., Wang, J. M., Yang, J. F., Li, A. Y., Liu, Z. J., Du, P. F., Li, Y. Q., Liu, Q., Zhu, H., Yin, H. and Luo, J. X. (2012 b). A recently identified ovine Babesia in China: serology and sero-epidemiology. Parasitology International 61, 532537.CrossRefGoogle ScholarPubMed
Gubbels, M. J., Yin, H., van der Weide, M., Bai, Q., Nijman, I. J., Liu, G. Y. and Jongejan, F. (2000). Molecular characterisation of the Theileria buffeli/orientalis group. International Journal for Parasitology 30, 943952.CrossRefGoogle ScholarPubMed
Gullo, C. A. and Teoh, G. (2004). Heat shock proteins: to present or not, that is the question. Immunology Letters 94, 110.CrossRefGoogle ScholarPubMed
Hermann, P. and Dobbelaere, D. A. (2006). Theileria-induced constitutive IKK activation is independent of functional Hsp90. FEBS Letters 580, 50235028.CrossRefGoogle ScholarPubMed
Inokuma, H., Yoshizaki, Y., Shimada, Y., Sakata, Y., Okuda, M. and Onishi, T. (2003). Epidemiological survey of Babesia species in Japan performed with specimens from ticks collected from dogs and detection of new Babesia DNA closely related to Babesia odocoilei and Babesia divergens DNA. Journal of Clinical Microbiology 41, 34943498.CrossRefGoogle ScholarPubMed
Khan, M. K., He, L., Zhang, W., Wang, Y., Tao, Q., Song, Q., Sajid, M. S., Yu, Q., Hu, J., Fang, R., Hu, M., Zhou, Y. and Zhao, J. (2014). Identification of two novel HSP90 proteins in Babesia orientalis: molecular characterization, and computational analyses of their structure, function, antigenicity and inhibitor interaction. Parasites and Vectors 7, 293.CrossRefGoogle ScholarPubMed
Kumar, R., Musiyenko, A. and Barik, S. (2003). The heat shock protein 90 of Plasmodium falciparum and antimalarial activity of its inhibitor, geldanamycin. Malaria Journal 2, 30.CrossRefGoogle ScholarPubMed
Kumar, R., Pavithra, S. R. and Tatu, U. (2007). Three-dimensional structure of heat shock protein 90 from Plasmodium falciparum: molecular modelling approach to rational drug design against malaria. Journal of Bioscience 32, 531536.CrossRefGoogle ScholarPubMed
Liu, A. H., Yin, H., Guan, G. Q., Schnittger, L., Liu, Z. J., Ma, M. L., Dang, Z. S., Liu, J. L., Ren, Q. Y., Bai, Q., Ahmed, J. S. and Luo, J. X. (2007). At least two genetically distinct large Babesia species infective to sheep and goats in China. Veterinary Parasitology 147, 246251.CrossRefGoogle Scholar
Martinez, J., Pérez-Serrano, J., Bernadina, W. E. and Rodríguez-Caabeiro, F. (2001). HSP60, HSP70 and HSP90 from Trichinella spiralis as targets of humoral immune response in rats. Parasitology Research 87, 453458.Google ScholarPubMed
McCarthy, M. M., Pick, E., Kluger, Y., Gould-Rothberg, B., Lazova, R., Camp, R. L., Rimm, D. L. and Kluger, H. M. (2008). HSP90 as a marker of progression in melanoma. Annals of Oncology 19, 590594.CrossRefGoogle ScholarPubMed
Niu, Q. L., Luo, J. X., Guan, G. Q., Liu, Z. J., Ma, M. L., Liu, A. H., Gao, J. L., Ren, Q. Y., Li, Y. Q., Qiu, J. X. and Yin, H. (2009). Differentiation of two ovine Babesia based on the ribosomal DNA internal transcribed spacer (ITS) sequences. Experimental Parasitology 121, 6468.CrossRefGoogle ScholarPubMed
Oosthuizen, M. C., Zweygarth, E., Collins, N. E., Troskie, M. and Penzhorn, B. L. (2008). Identification of a novel Babesia sp. from a sable Antelope (Hippotragus niger Harris, 1838). Journal of Clinical Microbiology 46, 22472251.CrossRefGoogle Scholar
Pashov, A., Kenderov, A., Kyurkchiev, S., Kehayov, I., Hristova, S., Lacroix-Desmazes, S., Giltiay, N., Varamballi, S., Kazatchkine, M. D. and Kaveri, S. V. (2002). Autoantibodies to heat shock protein 90 in the human natural antibody repertoire. International Immunology 14, 453461.CrossRefGoogle ScholarPubMed
Pearl, L. H. and Prodromou, C. (2006). Structure and mechanism of the Hsp90 molecular chaperone machinery. Annual Review of Biochemistry 75, 271294.CrossRefGoogle ScholarPubMed
Philippe, H., Lopez, P., Brinkmann, H., Budin, K., Germot, A., Laurent, J., Moreira, D., Müller, M. and Le Guyader, H. (2000). Early-branching or fast-evolving eukaryotes? An answer based on slowly evolving positions. Proceedings of the Royal Society B: Biological Sciences 267, 12131221.CrossRefGoogle ScholarPubMed
Reitsma, D. J. and Combest, A. J. (2012). Challenges in the development of an autologous heat shock protein based anti-tumor vaccine. Human Vaccines and Immunotherapeutics 8, 11521155.CrossRefGoogle ScholarPubMed
Ruef, B. J., Ward, T. J., Oxner, C. R., Conley, P. G., Brown, W. C. and Rice-Ficht, A. C. (2000). Phylogenetic analysis with newly characterized Babesia bovis hsp70 and hsp90 provides strong support for paraphyly within the piroplasms. Molecular and Biochemical Parasitology 109, 6772.CrossRefGoogle ScholarPubMed
Schnittger, L., Rodriguez, A. E., Florin-Christensen, M. and Morrison, D. A. (2012). Babesia: a world emerging. Infection, Genetics and Evolution 12, 17881809.CrossRefGoogle ScholarPubMed
Shen, W. W., Liu, H. C., Yang, Y. Y., Lin, C. Y., Chen, K. P., Yeh, T. S. and Leu, S. J. (2006). Anti-heat shock protein 90 is increased in acute mania. Australian and New Zealand Journal of Psychiatry 40, 712716.CrossRefGoogle ScholarPubMed
Stechmann, A. and Cavalier-Smith, T. (2003). Phylogenetic analysis of eukaryotes using heat-shock protein Hsp90. Journal of Molecular Evolution 57, 408419.CrossRefGoogle ScholarPubMed
Tian, Z. C., Liu, G. Y., Yin, H., Luo, J. X., Guan, G. Q., Xie, J. R., Luo, J., Zheng, J. F., Tian, M. Y., Yuan, X. S., Wang, F. F., Chen, R. G. and Wang, H. J. (2013 a). Cytochrome c oxidase subunit III (COX3) gene, an informative marker for phylogenetic analysis and differentiation of Babesia species in China. Infection, Genetics and Evolution 18, 1317.CrossRefGoogle Scholar
Tian, Z. C., Luo, J., Zheng, J. F., Xie, J. R., Shen, H., Yin, H., Luo, J. X., Tian, M. Y., Yuan, X. S., Wang, F. F. and Liu, G. Y. (2013 b). Phylogenetic analysis of Babesia species in China based on cytochrome b (COB) gene. Infection, Genetics and Evolution 13, 3640.CrossRefGoogle ScholarPubMed
Tosti, G., di Pietro, A., Ferrucci, P. F. and Testori, A. (2009). HSPPC-96 vaccine in metastatic melanoma patients: from the state of the art to a possible future. Expert Review of Vaccines 8, 15131526.CrossRefGoogle ScholarPubMed
Uilenberg, G. (2006). Babesia – a historical overview. Veterinary Parasitology 138, 310.CrossRefGoogle ScholarPubMed
Virdi, A. S., Thakur, A., Dutt, S., Kumar, S. and Singh, P. (2009). A sorghum 85 kDa heat stress-modulated protein shows calmodulin-binding properties and cross-reactivity to anti-Neurospora crassa Hsp80 antibodies. FEBS Letters 583, 767770.CrossRefGoogle Scholar
Vovlas, N., Troccoli, A., Palomares-Rius, J. E., De Luca, F., Cantalapiedra-Navarrete, C., Liébanas, G., Landa, B. B., Subbotin, S. A. and Castillo, P. (2015). A new stem nematode, Ditylenchus oncogenus n. sp. (Nematoda: Tylenchida), parasitizing sowthistle from Adriatic coast dunes in southern Italy. Journal of Helminthology 3, 114.Google Scholar
Yamasaki, M., Inokuma, H., Sugimoto, C., Shaw, S. E., Aktas, M., Yabsley, M. J., Yamato, O. and Maede, Y. (2007). Comparison and phylogenetic analysis of the heat shock protein 70 gene of Babesia parasites from dogs. Veterinary Parasitology 145, 217227.CrossRefGoogle ScholarPubMed
Yin, H., Lu, W. S., Luo, J. X., Zhang, Q. C., Lu, W. X. and Dou, H. F. (1997). Isolation and morphological observation of Babesia motasi and Babesia ovis in China (in Chinese). Chinese Journal of Veterinary Science and Technology 10, 79.Google Scholar
Zhang, M. H., Botër, M., Li, K. Y., Kadota, Y., Panaretou, B., Prodromou, C., Shirasu, K. and Pearl, L. H. (2008). Structural and functional coupling of Hsp90- and Sgt1-centred multi-protein complexes. EMBO Journal 27, 27892798.CrossRefGoogle ScholarPubMed
Zhao, X. R., Li, C. R. and Min, Y. G. (1986). Investigations on ovine Babesiosis (in Chinese). Chinese Journal of Veterinary Science and Technology 1, 2627.Google Scholar
Supplementary material: File

Guan supplementary material

Table S1 and Figures S1-S2

Download Guan supplementary material(File)
File 402 KB
6
Cited by

Save article to Kindle

To save this article to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

A member of the HSP90 family from ovine Babesia in China: molecular characterization, phylogenetic analysis and antigenicity
Available formats
×

Save article to Dropbox

To save this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about saving content to Dropbox.

A member of the HSP90 family from ovine Babesia in China: molecular characterization, phylogenetic analysis and antigenicity
Available formats
×

Save article to Google Drive

To save this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about saving content to Google Drive.

A member of the HSP90 family from ovine Babesia in China: molecular characterization, phylogenetic analysis and antigenicity
Available formats
×
×

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *