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Characterization of heat shock protein 70 gene from Haemonchus contortus and its expression and promoter analysis in Caenorhabditis elegans

Published online by Cambridge University Press:  29 January 2013

HONGLI ZHANG ,
QIANJIN ZHOU ,
YI YANG ,
XUEQIU CHEN ,
BAOLONG YAN  and
AIFANG DU
HONGLI ZHANG
Affiliation:
Institute of Preventive Veterinary Medicine, College of Animal Sciences, Zhejiang University, Hangzhou, Zhejiang 310058, China
QIANJIN ZHOU
Affiliation:
Institute of Preventive Veterinary Medicine, College of Animal Sciences, Zhejiang University, Hangzhou, Zhejiang 310058, China
YI YANG
Affiliation:
Institute of Preventive Veterinary Medicine, College of Animal Sciences, Zhejiang University, Hangzhou, Zhejiang 310058, China
XUEQIU CHEN
Affiliation:
Institute of Preventive Veterinary Medicine, College of Animal Sciences, Zhejiang University, Hangzhou, Zhejiang 310058, China
BAOLONG YAN
Affiliation:
Institute of Preventive Veterinary Medicine, College of Animal Sciences, Zhejiang University, Hangzhou, Zhejiang 310058, China
AIFANG DU*
Affiliation:
Institute of Preventive Veterinary Medicine, College of Animal Sciences, Zhejiang University, Hangzhou, Zhejiang 310058, China
*
*Corresponding author. Tel: +86 571 88982583. Fax: +86 571 88982583. E-mail: [email protected].
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Summary

Haemonchus contortus infections in small ruminants are of major economic importance worldwide. Heat shock proteins (HSPs) are a family of molecular chaperones that play important roles in the process of invasion and survival of nematodes. Although HSP70 has been identified in several parasitic nematodes, little is known of its distribution and function in Haemonchus contortus. The aims of this study were to characterize HSP70 from Haemonchus contortus (designed as Hc-hsp70), express Hc-hsp70 and analyse the promoter activity in Caenorhabditis elegans. Bioinformatic analysis revealed that the open reading frame of the Hc-hsp70 cDNA encodes a 646-amino acid peptide, which is highly conserved in comparison to HSP70 in other nematodes. Phylogenetic analysis indicated that H. contortus is closely related to Caenorhabditis. The 5′-flanking region promoted green fluorescence protein (GFP) expression in the intestine in all larval stages and adult with 2 expression patterns in C. elegans. Expression of Hc-hsp70 mRNA transcripts in C. elegans increased following 2, 4, 6 h of heat shock and peaked at 4 h. However, its expression induced down-regulation of hsp-1 of C. elegans. These results suggest that the H. contortus hsp70 might have a similar function to that of C. elegans hsp-1.

Keywords

Haemonchus contortusHSP70promoter activityCaenorhabditis elegans
Type
Research Article
Information
Parasitology , Volume 140 , Issue 6 , May 2013 , pp. 683 - 694
Copyright
Copyright © Cambridge University Press 2013

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References

REFERENCES

Bairoch, A. (1993). The PROSITE dictionary of sites and patterns in proteins, its current status. Nucleic Acids Research 21, 3097–3103.CrossRefGoogle ScholarPubMed
Bateman, A., Birney, E., Durbin, R., Eddy, S. R., Howe, K. L. and Sonnhammer, E. L. L. (2000). The Pfam Protein families database. Nucleic Acids Research 28, 263–266. doi: 10.1093/nar/gkh121.CrossRefGoogle ScholarPubMed
Birnby, D. A., Link, E. M., Vowels, J. J., Tian, H., Colacurcio, P. L. and Thomas, J. H. (2000). A transmembrane guanylyl cyclase (DAF-11) and Hsp90 (DAF-21) regulate a common set of chemosensory behaviors in Caenorhabditis elegans. Genetics 155, 85–104.CrossRefGoogle ScholarPubMed
Brand, A. M., Varghese, G., Majewski, W. and Hawdon, J. M. (2005). Identification of a DAF-7 ortholog from the hookworm Ancylostoma caninum. International Journal for Parasitology 35, 1489–1498. doi: 10.1016/j.ijpara.2005.07.004.CrossRefGoogle ScholarPubMed
Britton, C., Redmond, D. L., Knox, D. P., McKerrow, J. H. and Barry, J. D. (1999). Identification of promoter elements of parasite nematode genes in transgenic Caenorhabditis elegans. Molecular and Biochemical Parasitology 103, 171–181. doi: 10.1016/S0166-6851(99)00121-8.CrossRefGoogle ScholarPubMed
Bruschi, F. (2002). The immune response to the parasitic nematode Trichinella and the ways to escape it, from experimental studies to implications for human infection. Current Drug Targets- Immune, Endocrine & Metabolic Disorders 2, 269–280. doi: 10.2174/1568008023340523.CrossRefGoogle Scholar
Calderwood, S. K., Mambula, S. S., Gray, P. J. Jr. and Theriault, J. R. (2007). Extracellular heat shock proteins in cell signaling. FEBS Letters 581, 3689–3694. doi: 10.1016/j.febslet.2007.04.044.CrossRefGoogle ScholarPubMed
Carrillo, E., Crusat, M., Nieto, J., Chicharro, C., Thomas, M. C., Martínez, E., Valladares, B., Cañavate, C., Requena, J. M., López, M. C., Alvar, J. and Moreno, J. (2008). Immunogenicity of HSP-70, KMP-11 and PFR-2 leishmanial antigens in the experimental model of canine visceral leishmaniasis. Vaccine 26, 1902–1911. doi: 10.1016/j.vaccine.2008.01.042.CrossRefGoogle ScholarPubMed
Cherkasova, V., Ayyadevara, S., Egilmez, N. and Reis, S. R. (2000). Diverse Caenorhabditis elegans genes that are upregulated in dauer larvae also show elevated transcript levels in long-lived, aged, or starved adults. Journal of Molecular Biology 300, 433–448. doi: 10.1006/jmbi.2000.3880.CrossRefGoogle ScholarPubMed
Clark, S. G. and Chiu, C. (2003). C. elegans ZAG-1, a Zn-finger-homeodomain protein, regulates axonal development and neuronal differentiation. Development 130, 3781–3794. doi: 10.1242/dev.00571.CrossRefGoogle ScholarPubMed
Dadna, H., Pauline, A. C., Keith, W. S., Mrinal, B., Paul, J. A. P., Lawrie, F., Marzena, W. and Susan, E. N. (2003). Haemonchus contortus: molecular characterization of a small heat shock protein. Experimental Parasitology 104, 96–103. doi: 10.1016/S0014-4894(03)00138-3.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, 16–22. doi: 10.1016/j.gene.2009.03020.CrossRefGoogle ScholarPubMed
Devaney, E., O'Neill, K., Harnett, W., Whitesell, L. and Kinnaird, J. H. (2005). Hsp90 is essential in the filarial nematode Brugia pahangi. International Journal for Parasitology 35, 627–636. doi: 10.1016/j.ijpara.2005.01.007.CrossRefGoogle ScholarPubMed
Dworniczak, B. and Mirault, M. E. (1987). Structure and expression of a human gene coding for a 71 kd heat shock ‘cognate’ protein. Nucleic Acids Research 15, 5181–5197. doi: 10.1093/nar/15.13.5181.CrossRefGoogle ScholarPubMed
Dzik, J. M. (2006). Molecules released by helminth parasites involved in host colonization. Acta Biochimica Polonica 53, 33–64.CrossRefGoogle ScholarPubMed
Egan, C. R., Chung, M. A., Allen, F. L., Heschl, M. F., Van Buskirk, C. L. and McGhee, J. D. (1995). A gut-to-pharynx/tail switch in embryonic expression of the Caenorhabditis elegans ges-1 gene centers on two GATA sequences. Developmental Biology 170, 397–419. doi: 10.1006/dbio.1995.1225.CrossRefGoogle ScholarPubMed
Engman, D. M., Dragon, E. A. and Donelson, J. E. (1990). Human humoral immunity to hsp70 during Trypanosoma cruzi infection. Journal of Immunology 144, 3987–3991.CrossRefGoogle ScholarPubMed
Gillan, V., Maitland, K., McCormack, G., Nik Him, A. I. I. N. and Devaney, E. (2009). Functional genomics of hsp-90 in parasitic and free-living nematodes. International Journal for Parasitology 39, 1071–1081. doi: 10.1016/j.ijpara.2009.02.024.CrossRefGoogle ScholarPubMed
Gomez-Escobar, N., Gregory, W. F. and Maizels, R. M. (2000). Identification of tgh-2, a filarial nematode homolog of Caenorhabditis elegans daf-7 and human transforming growth factor β, expressed in microfilarial and adult stages of Brugia malayi. Infection and Immunity 68, 6402–6410. doi: 10.1128/IAI.68.11.6402-6410.2000.CrossRefGoogle ScholarPubMed
Grant, W. N., Skinner, S. J. M., Newton-Howes, J., Grant, K., Shuttleworth, G., Heath, D. D. and Shoemaker, C. B. (2006). Heritable transgenesis of Parastrongyloides trichosuri: a nematode parasite of mammals. International Journal for Parasitology 36, 475–483. doi: 10.1016/j.ijpara.2005.12.002.CrossRefGoogle ScholarPubMed
Guha Thakurta, D., Palomar, L. and Stormo, G. D. (2002). Identification of a novel cis-regulatory element involved in the heat shock response in Caenorhabditis elegans using microarray gene expression and computational methods. Genome Research 12, 701–712. doi: 10.1101/gr.228902.Google ScholarPubMed
Heinrich, J. C., Li, X., Henry, R. A., Haack, N., Stringfellow, L., Heath, A. C. and Scott, M. J. (2002). Germ-line transformation of the Australian sheep blowfly Lucilia cuprina. Insect Molecular Biology 11, 1–10. doi: 10.1046/j.0962-1075.2001.00301.x.CrossRefGoogle ScholarPubMed
Hu, M., Lok, J. B., Ranjit, N., Massey, H. C., Sternberg, P. W. and Gasser, R. B. (2010). Structural and functional characterisation of the fork head transcription factor-encoding gene, Hc-daf-16, from the parasitic nematode Haemonchus contortus (Strongylida). International Journal for Parasitology 40, 405–415. doi: 10.1016/j.ijpara.2009.09.005.CrossRefGoogle ScholarPubMed
Hunt, S. M., Wilkins, M. R., Stokes, H. W., Daggard, G. E. and Frankham, R. (1992). Induced expression of a Drosophila hsp70 promoter-fusion transgene is reduced after repeated heat shocks. Genetical Research 59, 183–188. doi: 10.1017/S0016672300030469.CrossRefGoogle ScholarPubMed
Jones, S. J., Riddle, D. L., Pouzyrev, A. T., Velculescu, V. E., Hillier, L., Eddy, S. R., Stricklin, S. L., Baillie, D. L., Waterston, R. and Marra, M. A. (2001). Changes in gene expression associated with developmental arrest and longevity in Caenorhabditis elegans. Genome Research 11, 1346–1352. doi: 10.1101/gr.184401.CrossRefGoogle ScholarPubMed
Kanamura, H. Y., Hancock, K., Rodrigues, V. and Damian, R. T. (2002). Schistosoma mansoni heat shock protein 70 elicits an early humoral immune response in S. mansoni infected baboons. Memórias do Instituto Oswaldo Cruz 97, 711–716.CrossRefGoogle ScholarPubMed
Kimura, K., Tanaka, N., Nakamura, N., Takano, S. and Ohkuma, S. (2007). Knockdown of mitochondrial heat shock protein 70 promotes progeria-like phenotypes in Caenorhabditis elegans. Journal of Biological Chemistry 282, 5910–5918. doi: 10.1074/jbc.M609025200.CrossRefGoogle ScholarPubMed
Kimura, K. D., Tissenbaum, H. A., Liu, Y. and Ruvkun, G. (1997). daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277, 942–946. doi: 10.1126/science.277.5328.942.CrossRefGoogle ScholarPubMed
Li, Z. and Srivastava, P. (2004). Heat-shock proteins. Current Protocols in Immunology Appendix 1, Appendix 1 T. Cambridge University Press, Cambridge, UK. doi: 10.1002/0471142735.ima01ts58.Google Scholar
Li, Z., Menoret, A. and Srivastava, P. (2002). Roles of heat-shock proteins in antigen presentation and cross-presentation. Current Opinion in Immunology 14, 45–51. doi: 10.1016/S0952-7915(01)00297-7.CrossRefGoogle ScholarPubMed
Lindquist, S. (1986). The heat-shock response. Annual Review of Biochemistry 55, 1151–1191. doi: 10.1146/annurev.bi.55.070186.005443.CrossRefGoogle ScholarPubMed
Livak, K. J. and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408. doi: 10.1006/meth.2001.1262.CrossRefGoogle Scholar
Maresca, B. and Carratú, L. (1992). The biology of heat shock response in parasites. Parasitology Today 8, 260–266. doi: 10.1016/0169-4758(92)90137-Q.CrossRefGoogle ScholarPubMed
Marshall, S. G. and McGhee, J. D. (2001). Coordination of ges-1 expression between the Caenorhabditis pharynx and intestine. Developmental Biology 239, 350–363. doi: 10.1006/dbio.2001.0442.CrossRefGoogle ScholarPubMed
Massey, H. C. Jr., Bhopale, M. K., Li, X. S., Castelletto, M. and Lok, J. B. (2006). The fork head transcription factor FKTF-1b from Strongyloides stercoralis restores DAF-16 developmental function to mutant Caenorhabditis elegans. International Journal for Parasitology 36, 347–352. doi: 10.1016/j.ijpara.2005.11.007.CrossRefGoogle ScholarPubMed
Mello, C. C., Kramer, J. M., Stinchcomb, D. and Ambros, V. (1991). Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO Journal 10, 3959–3970.CrossRefGoogle Scholar
Merritt, C., Rasoloson, D, Ko, D. and Seydoux, G. (2008). 3′ UTRs are the primary regulators of gene expression in the C. elegans germline. Current Biology 18, 1476–1482. doi: 10.1016/j.cub.2008.08.013.CrossRefGoogle ScholarPubMed
Mohamed, R. M., Aosai, F., Chen, M., Mun, H. S., Norose, K., Belal, U. S., Piao, L. X. and Yano, A. (2003). Induction of protective immunity by DNA vaccination with Toxoplasma gondii HSP70, HSP30 and SAG1 genes. Vaccine 21, 2852–2861. doi: 10.1016/S0264-410X(03)00157-9.CrossRefGoogle ScholarPubMed
Morgan, W. D., Williams, G. T., Morimoto, R. I., Greene, J., Kingston, R. E. and Tjian, R. (1987). Two transcriptional activators, CCAAT-box-binding transcription factor and heat shock transcription factor, interact with a human hsp70 gene promoter. Molecular and Cellular Biology 7, 1129–1138. doi: 10.1128/MCB.7.3.1129.Google ScholarPubMed
Morley, J. F. and Morimoto, R. I. (2004). Regulation of longevity in Caenorhabditis elegans by heat shock factor and molecular chaperones. Molecular Biology of the Cell 15, 657–664. doi: 10.1091/mbc.E03-07-0532.CrossRefGoogle ScholarPubMed
Newton-Howes, J., Heath, D. D., Shoemaker, C. B. and Grant, W. N. (2006). Characterization and expression of an Hsp70 gene from Parastrongyloides trichosuri. International Journal for Parasitology 36, 467–474. doi: 10.1016/j.ijpara.2005.12.001.CrossRefGoogle ScholarPubMed
O'Malley, K., Mauron, A., Barchas, J. D. and Kedes, L. (1985). Constitutively expressed rat mRNA encoding a 70-kilodalton heat-shock-like protein. Molecular and Cellular Biology 5, 3476–3483. doi: 10.1128/MCB.5.12.3476.Google ScholarPubMed
Pockley, A. G., Muthana, M. and Calderwood, S. K. (2008). The dual immunoregulatory roles of stress proteins. Trends in Biochemical Sciences 33, 71–79. doi: 10.1016/j.tibs.2007.10.005.CrossRefGoogle ScholarPubMed
Ravi, V., Kubofcik, J., Bandopathyaya, S., Geetha, M., Narayanan, R. B., Nutman, T. B. and Kaliraja, P. (2004). Wuchereria bancrofti: cloning and characterization of heat shock protein 70 from the human lymphatic filarial parasite. Experimental Parasitology 106, 1–10. doi: 10.1016/j.exppara.2004.01.001.CrossRefGoogle ScholarPubMed
Ren, P., Lim, C. S., Johnsen, R., Albert, P. S., Pilgrim, D. and Riddle, D. L. (1996). Control of C. elegans larval development by neuronal expression of a TGF-beta homolog. Science 274, 1389–1391. doi: 10.1126/science.274.5291.1389.Google ScholarPubMed
Requena, J. M., Jimenez-Ruiz, A., Soto, M., Assiego, R., Santaren, J. F., Lopez, M. C., Patarroyo, M. E. and Alonso, C. (1992). Regulation of hsp70 expression in Trypanosoma cruzi by temperature and growth phase. Molecular and Biochemical Parasitology 53, 201–211. doi: 10.1016/0166-6851(92)90022-C.CrossRefGoogle ScholarPubMed
Rothstein, N. M., Higashi, G. J., Yates, J. and Rajan, T. V. (1989). Onchocerca volvulus heat shock protein 70 is a major immunogen in amicrofilaremic individuals from a filariasis-endemic area. Molecular and Biochemical Parasitology 33, 229–235. doi: 10.1016/0166-6851(89)90084-4.CrossRefGoogle Scholar
Rothstein, N. and Rajan, T. V. (1991). Characterization of an hsp70 gene from the human filarial parasite, Brugia malayi (Nematoda). Molecular and Biochemical Parasitology 49, 229–237. doi: 10.1016/0166-6851(91)90066-F.CrossRefGoogle ScholarPubMed
Rothwell, J. T. and Sangster, N. C. (1993). An in vitro assay utilizing parasitic larval Haemonchus contortus to detect resistance to Closantel and other anthelmintics. International Journal for Parasitology 23, 573–578. doi: 10.1016/0020-7519(93)90162-R.CrossRefGoogle Scholar
Scheufler, C., Brinker, A., Bourenkov, G., Pegoraro, S., Moroder, L., Bartunik, H., Hartl, F. U. and Moarefi, I. (2000). Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101, 199–210. doi: 10.1016/S0092-8674(00)80830-2.CrossRefGoogle ScholarPubMed
Selkirk, M. E., Denham, D. A., Partono, F. and Maizels, R. M. (1989). Heat shock cognate 70 is a prominent immunogen in Brugian filariasis. Journal of Immunology 143, 299–308.CrossRefGoogle ScholarPubMed
Shu, L. M., Katholi, C. R., Higazi, T. and Unnasch, T. R. (2003). Analysis of the Brugia malayi HSP70 promoter using a homologous transient transfection system. Molecular and Biochemical Parasitology 128, 67–75. doi: 10.1016/S0166-6851(03)00052-5.CrossRefGoogle ScholarPubMed
Snutch, T. P., Heschl, M. F. P. and Baillie, D. L. (1988). The Caenorhabditis elegans hsp70 gene family: a molecular genetic characterization. Gene 64, 241–255. doi: 10.1016/0378-1119(88)90339-3.CrossRefGoogle Scholar
Song, K. J., Song, K. H., Na, B. K., Kim, J. H., Kwon, D., Park, S., Pak, J. H., Im, K. I. and Shin, H. J. (2007). Molecular cloning and characterization of a cytosolic heat shock protein 70 from Naegleria fowleri. Parasitology Research 100, 1083–1089. doi: 10.1007/s00436-006-0404-8.CrossRefGoogle ScholarPubMed
Sorger, P. K. and Pelham, H. R. B. (1988). Yeast heat shock protein is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation. Cell 54, 855–864. doi: 10.1016/S0092-8674(88)91219-6.CrossRefGoogle ScholarPubMed
Tamai, K. T., Liu, X., Silar, P., Sosinowski, T. and Thiele, D. J. (1994). Heat shock transcription factor activates yeast metallothionein gene expression in response to heat and glucose starvation via distinct signalling pathways. Molecular and Cellular Biology 14, 8155–8165. doi: 10.1128/MCB.14.12.8155.Google ScholarPubMed
Tazir, Y., Steisslinger, V., Soblik, H., Younis, A. E., Beckmann, S., Grevelding, G. G., Steen, H., Brattig, N. W. and Erttmann, K. D. (2009). Molecular and functional characterisation of the heat shock protein 10 of Strongyloides ratti. Molecular and Biochemical Parasitology 168, 149–157. doi: 10.1016/j.molbiopara.2009.07.007.CrossRefGoogle ScholarPubMed
Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680. doi: 10.1093/nar/22.22.4673.CrossRefGoogle ScholarPubMed
Thon, M., Abdallah, Q. A. I., Hortschansky, P., Scharf, D. H., Eisendle, M., Haas, H. and Brakhage, A. A. (2010). The CCAAT-binding complex coordinates the oxidative stress response in eukaryotes. Nucleic Acids Research 38, 1098–1113. doi: 10.1093/nar/gkp1091.CrossRefGoogle ScholarPubMed
Tsan, M-F. and Gao, B. (2004). Cytokine function of heat shock proteins. American Journal of Physiology-Cell Physiology 286, C739–C744. doi: 10.1152/ajpcell.00364.2003.CrossRefGoogle ScholarPubMed
Tsuji, N., Ohta, M. and Fujisaki, K. (1997). Expression of a 70-kDa heat-shock-related protein during transformation from free-living infective larvae to the parasitic stage in Strongyloides venezuelensis. Parasitology Research 83, 99–102. doi: 10.1007/s004360050218.CrossRefGoogle Scholar
Vayssier, M., Le-Guerhier, F., Fabien, J. F., Philippe, H., Vallet, C., Ortega-Pierres, G., Soule, C., Perret, C., Liu, M., Vega-Lopez, M. and Boireau, P. (1999). Cloning and analysis of a Trichinella britovi gene encoding a cytoplasmic heat shock protein of 72 kDa. Parasitology 119, 81–93.CrossRefGoogle Scholar
Wallin, R. P., Lundqvist, A., More, S. H., von Bonin, A., Kiessling, R. and Ljunggren, H. G. (2002). Heat-shock proteins as activators of the innate immune system. Trends in Immunology 23, 130–135. doi: 10.1016/S1471-4906(01)02168-8.CrossRefGoogle ScholarPubMed
Wang, S. H., Zhu, X. P., Yang, Y. P., Yang, J., Gu, Y., Wei, J. F., Hao, R., Boireau, P. and Cui, S. J. (2009). Molecular cloning and characterization of heat shock protein 70 from Trichinella spiralis. Acta Tropica 110, 46–51. doi: 10.1016/j.actatropica.2009.01.003.CrossRefGoogle ScholarPubMed
Watson, K. (1990). Microbial stress proteins. Advance in Microbial Physiology 31, 183–223.CrossRefGoogle ScholarPubMed
Wiederrecht, G., Seto, D. and Parker, C. (1988). Isolation of the gene encoding the S. cerevisiae heat shock transcription factor. Cell 54, 841–853. doi: 10.1016/S0092-8674(88)91197-X.CrossRefGoogle ScholarPubMed
Wieten, L., Broere, F., van der Zee, R., Koerkamp, E. K., Wagenaar, J. and van Eden, W. (2007). Cell stress induced HSP are targets of regulatory T cells: A role for HSP inducing compounds as anti-inflammatory immuno-modulators? FEBS Letters 581, 3716–3722. doi: 10.1016/j.febslet.2007.04.082.CrossRefGoogle ScholarPubMed
Yang, Y. F., Tan-ariya, P., Sharma, Y. D. and Kilejian, A. (1987). The primary structure of a Plasmodium falciparum polypeptide related to heat shock proteins. Molecular and Biochemical Parasitology 26, 61–67. doi: 10.1016/0166-6851(87)90130-7.CrossRefGoogle ScholarPubMed