Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-24T08:12:41.124Z Has data issue: false hasContentIssue false
  • English
  • Français

Genomic organization and expression of the HSP70 locus in New and Old World Leishmania species

Published online by Cambridge University Press:  23 October 2006

C. FOLGUEIRA ,
C. CAÑAVATE ,
C. CHICHARRO  and
J. M. REQUENA
C. FOLGUEIRA
Affiliation:
Centro de Biología Molecular “Severo Ochoa”, Universidad Autónoma de Madrid, 28049 Madrid, Spain
C. CAÑAVATE
Affiliation:
WHO Collaborating Centre for Leishmaniasis, Servicio de Parasitología, Centro Nacional de Microbiología, Instituto de Salud Carlos III, 28220 Madrid, Spain
C. CHICHARRO
Affiliation:
WHO Collaborating Centre for Leishmaniasis, Servicio de Parasitología, Centro Nacional de Microbiología, Instituto de Salud Carlos III, 28220 Madrid, Spain
J. M. REQUENA
Affiliation:
Centro de Biología Molecular “Severo Ochoa”, Universidad Autónoma de Madrid, 28049 Madrid, Spain
Get access Rights & Permissions [Opens in a new window]

Abstract

Heat shock is believed to be a developmental inductor of differentiation in Leishmania. Furthermore, heat shock genes are extensively studied as gene models to decipher mechanisms of gene regulation in kinetoplastids. Here, we describe the organization and expression of the HSP70 loci in representative Leishmania species (L. infantum, L. major, L. tropica, L. mexicana, L. amazonensis and L. braziliensis). With the exception of L. braziliensis, the organization of the HSP70 loci was found to be well conserved among the other Leishmania species. Two types of genes, HSP70-I and HSP70-II, were found to be present in these Leishmania species except for L. braziliensis that lacks HSP70-II gene. Polymorphisms in the HSP70 locus allow the differentiation of the Old and New World species within the subgenus Leishmania. A notable discrepancy between our data and those of the L. major genome database in relation to the gene copy number composing the L. major HSP70 locus was revealed. The temperature-dependent accumulation of the HSP70-I mRNAs is also conserved among the different Leishmania species with the exception of L. braziliensis. In spite of these differences, analysis of the HSP70 synthesis indicated that the HSP70 mRNAs are also preferentially translated during heat shock in L. braziliensis.

Keywords

LeishmaniaHSP70genomic organization3′UTRmRNA stabilityde novo synthesis of proteins
Type
Research Article
Information
Parasitology , Volume 134 , Issue 3 , March 2007 , pp. 369 - 377
Copyright
© 2006 Cambridge University Press

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

Anonymous ( 1990). Control of the leishmaniasis: Report of a WHO Expert Committee. World Health Organization Technical Report Series, No. 793.
Aslett, M., Mooney, P., Adlem, E., Berriman, M., Berry, A., Hertz-Fowler, C., Ivens, A. C., Kerhornou, A., Parkhill, J., Peacock, C. S., Wood, V., Rajandream, M. A., Barrell, B. and Tivey, A. ( 2005). Integration of tools and resources for display and analysis of genomic data for protozoan parasites. International Journal for Parasitology 35, 481–493.CrossRefGoogle Scholar
Bock, J. H. and Langer, P. J. ( 1993). Sequence and genomic organization of the hsp70 genes of Leishmania amazonensis. Molecular and Biochemical Parasitology 62, 187–197.CrossRefGoogle Scholar
Brandau, S., Dresel, A. and Clos, J. ( 1995). High constitutive levels of heat-shock proteins in human-pathogenic parasites of the genus Leishmania. The Biochemical Journal 310, 225–232.CrossRefGoogle Scholar
Britto, C., Ravel, C., Bastien, P., Blaineau, C., Pages, M., Dedet, J. P. and Wincker, P. ( 1998). Conserved linkage groups associated with large-scale chromosomal rearrangements between Old World and New World Leishmania genomes. Gene 222, 107–117.CrossRefGoogle Scholar
Clayton, C. E. ( 2002). Life without transcriptional control? From fly to man and back again. The EMBO Journal 21, 1881–1888.CrossRefGoogle Scholar
Clos, J. and Krobitsch, S. ( 1999). Heat shock as a regular feature of the life cycle of Leishmania parasites. American Zoologist 39, 848–856.CrossRefGoogle Scholar
Croan, D. G., Morrison, D. A. and Ellis, J. T. ( 1997). Evolution of the genus Leishmania revealed by comparison of DNA and RNA polymerase gene sequences. Molecular and Biochemical Parasitology 89, 149–159.CrossRefGoogle Scholar
Desjeux, P. ( 2004). Leishmaniasis: current situation and new perspectives. Comparative Immunology, Microbiology and Infectious Diseases 27, 305–318.CrossRefGoogle Scholar
El-Sayed, N. M., Myler, P. J., Bartholomeu, D. C., Nilsson, D., Aggarwal, G., Tran, A. N., Ghedin, E., Worthey, E. A., Delcher, A. L., Blandin, G., Westenberger, S. J., Caler, E., Cerqueira, G. C., Branche, C., Haas, B., Anupama, A., Arner, E., Aslund, L., Attipoe, P., Bontempi, E., Bringaud, F., Burton, P., Cadag, E., Campbell, D. A., Carrington, M., Crabtree, J., Darban, H., da Silveira, J. F., de Jong, P., Edwards, K., Englund, P. T., Fazelina, G., Feldblyum, T., Ferella, M., Frasch, A. C., Gull, K., Horn, D., Hou, L., Huang, Y., Kindlund, E., Klingbeil, M., Kluge, S., Koo, H., Lacerda, D., Levin, M. J., Lorenzi, H., Louie, T., Machado, C. R., McCulloch, R., McKenna, A., Mizuno, Y., Mottram, J. C., Nelson, S., Ochaya, S., Osoegawa, K., Pai, G., Parsons, M., Pentony, M., Pettersson, U., Pop, M., Ramirez, J. L., Rinta, J., Robertson, L., Salzberg, S. L., Sanchez, D. O., Seyler, A., Sharma, R., Shetty, J., Simpson, A. J., Sisk, E., Tammi, M. T., Tarleton, R., Teixeira, S., Van Aken, S., Vogt, C., Ward, P. N., Wickstead, B., Wortman, J., White, O., Fraser, C. M., Stuart, K. D. and Andersson, B. ( 2005). The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309, 409–415.CrossRefGoogle Scholar
Fernandes, O., Murthy, V. K., Kurath, U., Degrave, W. M. and Campbell, D. A. ( 1994). Mini-exon gene variation in human pathogenic Leishmania species. Molecular and Biochemical Parasitology 66, 261–271.CrossRefGoogle Scholar
Folgueira, C., Quijada, L., Soto, M., Abanades, D. R., Alonso, C. and Requena, J. M. ( 2005). The translational efficiencies of the two Leishmania infantum HSP70 mRNAs, differing in their 3′-untranslated regions, are affected by shifts in the temperature of growth through different mechanisms. The Journal of Biological Chemistry 280, 35172–35183.CrossRefGoogle Scholar
Garlapati, S., Dahan, E. and Shapira, M. ( 1999). Effect of acidic pH on heat shock gene expression in Leishmania. Molecular and Biochemical Parasitology 100, 95–101.CrossRefGoogle Scholar
Hartl, F. U. and Hayer-Hartl, M. ( 2002). Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295, 1852–1858.CrossRefGoogle Scholar
Ivens, A. C., Peacock, C. S., Worthey, E. A., Murphy, L., Aggarwal, G., Berriman, M., Sisk, E., Rajandream, M. A., Adlem, E., Aert, R., Anupama, A., Apostolou, Z., Attipoe, P., Bason, N., Bauser, C., Beck, A., Beverley, S. M., Bianchettin, G., Borzym, K., Bothe, G., Bruschi, C. V., Collins, M., Cadag, E., Ciarloni, L., Clayton, C., Coulson, R. M., Cronin, A., Cruz, A. K., Davies, R. M., De Gaudenzi, J., Dobson, D. E., Duesterhoeft, A., Fazelina, G., Fosker, N., Frasch, A. C., Fraser, A., Fuchs, M., Gabel, C., Goble, A., Goffeau, A., Harris, D., Hertz-Fowler, C., Hilbert, H., Horn, D., Huang, Y., Klages, S., Knights, A., Kube, M., Larke, N., Litvin, L., Lord, A., Louie, T., Marra, M., Masuy, D., Matthews, K., Michaeli, S., Mottram, J. C., Muller-Auer, S., Munden, H., Nelson, S., Norbertczak, H., Oliver, K., O'Neil, S., Pentony, M., Pohl, T. M., Price, C., Purnelle, B., Quail, M. A., Rabbinowitsch, E., Reinhardt, R., Rieger, M., Rinta, J., Robben, J., Robertson, L., Ruiz, J. C., Rutter, S., Saunders, D., Schafer, M., Schein, J., Schwartz, D. C., Seeger, K., Seyler, A., Sharp, S., Shin, H., Sivam, D., Squares, R., Squares, S., Tosato, V., Vogt, C., Volckaert, G., Wambutt, R., Warren, T., Wedler, H., Woodward, J., Zhou, S., Zimmermann, W., Smith, D. F., Blackwell, J. M., Stuart, K. D., Barrell, B. and Myler, P. J. ( 2005). The Genome of the Kinetoplastid Parasite, Leishmania major. Science 309, 436–442.CrossRefGoogle Scholar
Laurentino, E. C., Ruiz, J. C., Fazelinia, G., Myler, P. J., Degrave, W., Alves-Ferreira, M., Ribeiro, J. M. C. and Cruz, A. K. ( 2004). A survey of Leishmania braziliensis genome by shotgun sequencing. Molecular and Biochemical Parasitology 137, 81–86.CrossRefGoogle Scholar
Lee, M. G.-S., Atkinson, B. L., Giannini, S. H. and Van der Ploeg, L. H. T. ( 1988). Structure and expression of the hsp70 gene family of Leishmania major. Nucleic Acids Research 16, 9567–9585.CrossRefGoogle Scholar
MacFarlane, J., Blaxter, M. L., Bishop, R. P. and Kelly, J. M. ( 1990). Identification and characterisation of a Leishmania donovani antigen belonging to the 70-kDa heat-shock protein family. European Journal of Biochemistry 190, 377–384.CrossRefGoogle Scholar
Momen, H. and Cupolillo, E. ( 2000). Speculations on the origin and evolution of the genus Leishmania. Memórias do Instituto Oswaldo Cruz 95, 583–588.CrossRefGoogle Scholar
Murray, H. W., Berman, J. D., Davies, C. R. and Saravia, N. G. ( 2005). Advances in leishmaniasis. Lancet 366, 1561–1577.CrossRefGoogle Scholar
Pearson, R. D. and de Queiroz Sousa, A. ( 1996). Clinical spectrum of Leishmaniasis. Clinical Infectious Diseases 22, 1–13.CrossRefGoogle Scholar
Quijada, L., Soto, M., Alonso, C. and Requena, J. M. ( 1997). Analysis of post-transcriptional regulation operating on transcription products of the tandemly linked Leishmania infantum hsp70 genes. The Journal of Biological Chemistry 272, 4493–4499.CrossRefGoogle Scholar
Quijada, L., Soto, M., Alonso, C. and Requena, J. M. ( 2000). Identification of a putative regulatory element in the 3′-untranslated region that controls expression of HSP70 in Leishmania infantum. Molecular and Biochemical Parasitology 110, 79–91.CrossRefGoogle Scholar
Requena, J. M., Lopez, M. C., Jimenez-Ruiz, A., de la Torre, J. C. and Alonso, C. ( 1988). A head-to-tail tandem organization of hsp70 genes in Trypanosoma cruzi. Nucleic Acids Research 16, 1393–1406.CrossRefGoogle Scholar
Rico, A. I., Angel, S. O., Alonso, C. and Requena, J. M. ( 1999). Immunostimulatory properties of the Leishmania infantum heat shock proteins HSP70 and HSP83. Molecular Immunology 36, 1131–1139.CrossRefGoogle Scholar
Sambrook, J., Fritsch, E. F. and Maniatis, T. ( 1989). Molecular Cloning: A Laboratory Manual. 2nd Edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
Zilberstein, D. and Shapira, M. ( 1994). The role of pH and temperature in the development of Leishmania parasites. Annual Reviews of Microbiology 48, 449–470.CrossRefGoogle Scholar
Zilka, A., Garlapati, S., Dahan, E., Yaolsky, V. and Shapira, M. ( 2001). Developmental Regulation of Heat Shock Protein 83 in Leishmania. 3′ processing and mRNA stability control transcript abundance, and translation is directed by a determinant in the 3′-untranslated region. The Journal of Biological Chemistry 276, 47922–47929.Google Scholar
Zurita, A. I., Rodriguez, J., Piñero, J. E., Pacheco, R., Carmelo, E., del Castllo, A. and Valladares, B. ( 2003). Cloning and characterization of the Leishmania (Viannia) braziliensis Hsp70 gene. Diagnostic use of the C-terminal fragment rLb70(513–663). The Journal of Parasitology 89, 372–378.Google Scholar