Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-29T01:07:26.627Z Has data issue: false hasContentIssue false

Leishmaniasis epidemiology: all down to the DNA

Published online by Cambridge University Press:  06 April 2009

J. M. Blackwell
Affiliation:
University of Cambridge Clinical School, Department of Medicine, Addenbrooke's Hospital, Hills Road, Cambridge CB2 2QQ

Summary

Application of quantitative methods to the study of leishmaniasis epidemiology has allowed Dye (1992) to pinpoint important biological parameters which, if they could be accurately measured in the field, would contribute most to our knowledge of the spread of disease and key targets for control. Three areas in which laboratory-based research could impact most on leishmaniasis epidemiology were highlighted by Dye (1992): (i) the development of accurate diagnostic tools which can distinguish between current and past infection; (ii) to determine the underlying molecular/genetic basis to virulence polymorphisms in the parasite and study these in the context of field epidemiological studies; and (iii) to provide the molecular tools to measure genetic variation in resistance to infection in humans and in reservoir hosts of disease. This paper describes current progress in attaining these goals, highlighting first the work on isolation and field application of genomic and kDNA probes for species-specific diagnosis, and the development of PCR-based assays which can be performed under field conditions. At a more preliminary stage, studies are described in which variability in the major molecular determinants of virulence (lipophosphoglycan, GP63, and members of the HSP7O family of stress proteins) identified through studies of laboratory models of infection, is being measured in primary field isolates of Leishmania peruviana. To complete the picture, current progress in identifying and cloning the genes which control host resistance to leishmanial infection is described, along with field studies of multicase families of human disease in which linkage analysis using marker genes from the chromosomal regions bearing these genes can be used to find evidence for their role in determining disease phenotypes in man. The leishmaniasis epidemiology will be all down to the DNA. projected view from these studies is that the future of leishmaniasis epidemiology will be all down to the DNA.

Type
Leishmaniasis
Copyright
Copyright © Cambridge University Press 1992

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

Abel, L. & Demenais, F. (1988). Detection of major genes for susceptibility to leprosy and its subtypes in a Caribbean island: Desirade island. American Journal of Human Genetics 42, 256–66.Google Scholar
Ajioka, J. W., Skinner, A. C. & Blackwell, J. M. (1992). Production of a chromosome-specific library for Leishmania major. Journal of Cell Science Suppl. 16A, 119.Google Scholar
Badaro, R., Jones, T. C., Lorenco, B. J. C., Sampaio, D., Carvalho, E. M., Rocha, H., Teixeira, R. & Johnson, W. D. (1986 a). A prospective study of visceral leishmaniasis in an endemic area of Brazil. Journal of Infectious Diseases 154, 639–49.CrossRefGoogle Scholar
Badaro, R., Jones, T. C., Carvalho, E. M., Sampaio, D., Reed, S. G., Barral, A., Teixeira, R. & Johnson, W. D. (1986 b). New perspectives on a subclinical form of visceral leishmaniasis. Journal of Infectious Diseases 154, 1003–11.CrossRefGoogle ScholarPubMed
Barker, D. C. (1989). Molecular approaches to DNA diagnosis. Parasitology 99 (Suppl.), S125S146.CrossRefGoogle ScholarPubMed
Barker, D. C. & Butcher, J. (1983). The use of DNA probes in the identification of leishmaniasis: discrimination between isolates of Leishmania mexicana and L. braziliensis complexes. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 285–97.CrossRefGoogle Scholar
Ben-Ismail, R., Smith, D. F., Ready, P. D., Ayadi, A., Gramiccia, M., Ben-Osman, A. & Ben-Rachid, M. S. (1991). Sporadic cutaneous leishmaniasis in North Tunisia: identification of a species-specific recombinant DNA probe. Transactions of the Royal Society of Tropical Medicine and Hygiene (in the Press).Google Scholar
Bishop, D. & Williamson, J. A. (1990). The power of identity-by-state methods for linkage analysis. American Journal of Human Genetics 46, 254–65.Google ScholarPubMed
Blackwelder, W. C. & Elston, R. C. (1985). A comparison of sib-pair linkage tests for disease susceptibility loci. Genetic Epidemiology 2, 8597.CrossRefGoogle ScholarPubMed
Blackwell, J. M. (1989). The macrophage resistance gene Lsh/Ity/Bcg. Research in Immunology 140, 767828.CrossRefGoogle ScholarPubMed
Blackwell, J. M.(1992). Immunology of leishmaniasis. Clinical Aspects of Immunology (in the Press.)Google ScholarPubMed
Blackwell, J. M. & Alexander, J. (1986). Different host genes recognise and control infection with taxonomically distinct Leishmania species. In Leishsnania. Taxononjie et phylogenese. Applications eco-epidemiologiques, (ed. Rioux, J. A. & Peters, W.) pp. 211219. Montpellier, France: IMEEE Publishers.Google Scholar
Blacewell, J. M., Crocker, P. R. & Channon, J. Y. (1985 a). In Mononuclear Phagocytes: Characteristics, Physiology and Function, (ed. van Furth, R.), pp. 677833. Dordrecht, Boston and Lancaster: Martinus Nijhoff Publishers.CrossRefGoogle Scholar
Blackwell, J., Freeman, J. & Bradley, D. (1980). Influence of H-2 complex on acquired resistance to Leishmania donovani infection in mice. Nature, London 283, 72–4.CrossRefGoogle ScholarPubMed
Blackwell, J. M., Hale, C., Roberts, M. B., Ulczak, O. M., Liew, F. Y. & Howard, J. G. (1985 b). An H-11- linked gene has a parallel effect on Leishinania major and L. donovani infections in mice. Immunogenetics 21, 385–95.CrossRefGoogle Scholar
Blackwell, J. M., Toole, S., King, M., Dawda, P., Roach, T. I. A. & Cooper, A. (1988). Analysis of Lsh gene expression in congenic B10.L-Lsh r mice. Current Topics in Microbiology and Immunology 137, 301–9.Google ScholarPubMed
Blackwell, J. M., Roach, T. I. A., Kiderlen, A. & Kaye, P. M. (1989). Role of Lsh in regulating macrophage priming/activation. Research in Immunology 140, 798805.CrossRefGoogle ScholarPubMed
Blackwell, J. M., Roach, T. I. A., Atkinson, S. E., Ajioka, J. W., Barton, C. H. & Shaw, M.-A. (1991). Genetic regulation of macrophage priming activation: the Lsh gene story. Immunology Letters 30, 241–8.CrossRefGoogle ScholarPubMed
Bordier, C. (1987). The promastigote surface protease of Leishmania. Parasitology Today 3, 151–3.CrossRefGoogle ScholarPubMed
Bouvier, C., Bordier, C., Vogel, H., Reichelt, R. & Etges, R. J. (1989). Characterization of the promastigote surface protease of Leishmania as a membrane-bound zinc endopeptidase. Molecular and Biochemical Parasitology 37, 235–46.CrossRefGoogle ScholarPubMed
Bradley, D. J. (1974). Genetic Control of natural resistance to Leishmania donovani Nature, London 250, 353–4.CrossRefGoogle ScholarPubMed
Bradley, D. J. (1977). Regulation of Leishmania populations within the host. II Genetic control of acute susceptibility of mice to Leishmania donovani infection. Clinical and Experimental Immunology 30, 130–40.Google ScholarPubMed
Bradley, D. J. & Kirkley, J. (1972). Variation in susceptibility of mouse strains to Leishmania donovani infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 66, 527–8.Google ScholarPubMed
Bradley, D. J. & Kiekley, J. (1977). Regulation of Leishmania populations within the host. I. The variable course of L. donovani infections in mice. Clinical and Experimental Immunology 30, 119–29.Google Scholar
Bradley, D. J., Taylor, B. A., Blackwell, J. M., Evans, E. P. & Freeman, J. (1979). Regulation of Leishmania populations within the host. III. Mapping the locus controlling susceptibility to visceral leishmaniasis in the mouse. Clinical and Experimental Immunology 37, 714.Google ScholarPubMed
Brenner, D. A., O'hara, M., Angel, P., Chojkier, M. & Karin, M. (1989). Prolonged activation of jun and collagenase genes by tumour necrosis factor-α. Nature, London 337, 661–3.CrossRefGoogle ScholarPubMed
Brown, I. N., Glynn, A. A. & Plant, J. E. (1982). Inbred mouse strain resistance to Mycobacterium lepraesnurium follows the Ity/Lsh pattern. Immunology 47, 149–56.Google ScholarPubMed
Button, L. L. & McMaster, W. R. (1988). Molecular cloning of the major surface antigen of Leishmania. Journal of Experimental Medicine 167, 724–9.CrossRefGoogle ScholarPubMed
Cantor, R. M. & Rotter, J. I. (1987). Marker concordance in pairs of distant relatives: a new method of linkage analysis for common diseases. American Journal of Human Genetics 41, A252.Google Scholar
Carvalho, E. M., Teixeira, R. S. & Johnson, W. D. (1981). Cell mediated immunity in American visceral leishmaniasis: reversible immunosuppression during acute infection. Infection and Immunity 33, 498502.CrossRefGoogle ScholarPubMed
Carvalho, E. M., Johnson, W. D., Barreto, E., Marsden, P. D., Costa, J. L. M., Reed, S. & Rocha, H. (1985). Cell mediated immunity in American cutaneous and mucosal leishmaniasis. Journal of Immunology 135, 4144–8.CrossRefGoogle ScholarPubMed
Castes, M., Agnelli, A., Verde, O. & Rondon, A. J. (1983). Characterization of the cellular response in American cutaneous leishmaniasis. Clinical Immunology and Immunopathology 27, 176–86.CrossRefGoogle ScholarPubMed
Castes, M., Agnelli, A. & Rondon, A. J. (1984). Mechanisms associated with immunoregulation of human American cutaneous leishmaniasis. Clinical and Experimental Immunology 57, 279–86.Google ScholarPubMed
Chan, J., Fujiwara, T., Brennan, P., McNeil, M. & Turco, S. J. (1989). Microbial glycolipids: possible virulence factors that scavenge oxygen radicals. Proceedings of the National Academy of Sciences, USA 86, 2453–7.CrossRefGoogle ScholarPubMed
Chang, C. S., Inserra, T. J., Kink, J. A., Fong, D. & Chang, K.-P. (1986). Expression and size heterogeneity of a 63kDa membrane glycoprotein during growth and transformation of Leishmania mexicana amazonensis. Molecular Biochemistry and Parasitology 18, 197210.CrossRefGoogle Scholar
Chang, K.-P., Chaudhuri, G. & Fong, D. (1990). Molecular determinants of Leishmania virulence. Annual Reviews in Microbiology 44, 499529.CrossRefGoogle ScholarPubMed
Channon, J. Y., Roberts, M. B. & Blackwell, J. M. (1984). A study of the differential respiratory burst elicited by promastigotes and amastigotes of Leishmania donovani in murine resident peritoneal macrophages. Immunology 53, 345–55.Google ScholarPubMed
Chaudhuri, G. & Chang, K.-P. (1988). Acid protease activity of major surface membrane glycoprotein (gp63) from Leishmania mexicana promastigotes. Molecular and Biochemical Parasitology 27, 4352.CrossRefGoogle ScholarPubMed
Chaudhuri, G., Chaudhuri, M., Pan, A. & Chang, K.-P. (1989). Surface acid proteinase (gp63) of Leishmania mexicana. A metalloenzyme capable of protecting liposome-encapsulated proteins from phagolysosomal degradation by macrophages. Journal of Biological Chemistry 264, 7483–9.CrossRefGoogle ScholarPubMed
Colomer-Gould, V., Quinitao, L. G., Keithly, J. & Nogueira, N. (1985). A common major surface antigen on amastigotes and promastigotes of Leishmania species. Journal of Experimental Medicine 162, 902–16.CrossRefGoogle ScholarPubMed
Crocker, P. R., Blackwell, J. M. & Bradley, D. J. (1984). Expression of the natural resistance gene Lsh in resident liver rnacrophages. Infection and Immunity 43, 1033–40.CrossRefGoogle Scholar
Crocker, P. R., Davies, E. V. & Blackwell, J. M. (1987). Variable expression of the murine natural resistance gene Lsh in different macrophage populations infected in vitro with Leishmania donovani. Parasite Immunology 9, 705–19.CrossRefGoogle ScholarPubMed
Da Silva, R. P., Hall, B. F., Joiner, K. A. & Sacks, D. L. (1989). CR1, the C3b receptor, mediates binding of infective Leishmania major metacvclic promastigotes to human macrophages. Journal of Immunology 143, 617–22.CrossRefGoogle ScholarPubMed
Davies, E. V., Singleton, A. M. T. & Blacewell, J. M. (1988). Differences in Lsh gene control over systemic Leishmania major and Leishmania donovani or Leishmania mexicana mexicana infections are caused by differential targeting to infiltrating and resident liver macrophage populations. Infection and Immunity 56, 1128–34.CrossRefGoogle ScholarPubMed
De Bruijn, M. H. L. & Barker, D. C. (1992). Diagnosis of New World Leishmaniasis: relationships between and detection by amplification of kinetoplast DNA of species of the Leishmania braziliensis complex. Molecular and Biochemical Parasitology (in the Press).Google Scholar
De Vries, R. R. P., Mehra, N. K., Vaidya, M. C., Gupta, M. D., Meera Khan, P. & Van Rood, J. J. (1980). HLA linked control of susceptibility to tuberculoid leprosy and association with HLA-DR types. Tissue Antigens 16, 294304.CrossRefGoogle ScholarPubMed
Dye, C. (1992). Leishmaniasis epidemiology: the theory catches up. Parasitology 104 (Suppl.), S7S18.CrossRefGoogle ScholarPubMed
Etges, R., Bouvier, J. & Bordier, C. (1986). The major surface protein of Leishmania promastigotes is a protease. Journal of Biological Chemistry 261, 9098–101.CrossRefGoogle ScholarPubMed
Fine, P. E. M. (1989). The BCG story: lessons from the past and implications for the future. Reviews of Infectious Diseases 11, S353S359.CrossRefGoogle ScholarPubMed
Gonzalez, G A., Yamamoto, K. K., Fischer, W. H., Karr, D., Menzel, P., Biggs, W., Vale, W. E. & Montimy, M. R. (1989). A cluster of phosphorylation sites on the cyclic AMP-regulated nuclear factor CREB predicted by its sequence. Nature, London 337, 749–52.CrossRefGoogle ScholarPubMed
Goto, Y., Nakamara, R. M., Takahashi, H. & Tokunaca, T. (1984). Genetic control of resistance to Mycobacterium intracellulare infection in mice. Infection and Immunity 46, 135–40.CrossRefGoogle ScholarPubMed
Gramiccia, M., Smith, D. F., Angelica, M. C., Ready, P. D. & Gradoni, L. (1992). A kinetoplast DNA probe diagnostic for Leishmania infantum. Parasitology (in the Press).CrossRefGoogle ScholarPubMed
Green, E. D. & Olson, M. V. (1990). Chromosomal region of the cystic fibrosis gene in yeast artificial chromosomes: a model for human genome mapping. Science 250, 94–8.CrossRefGoogle Scholar
Gros, P., Skamene, E. & Forget, A. (1981). Genetic control of natural resistance to Mycobacterium bovis (BCG) in mice. Journal of Immunology 127, 2417–21.CrossRefGoogle ScholarPubMed
Haldar, J. P., Ghose, S., Saha, K. C. & Ghose, A. C. (1983). Cell mediated immune response in Indian kala-azar and post kala-azar dermal leishmaniasis. Infection and Immunity 42, 702–7.CrossRefGoogle ScholarPubMed
Handman, E., Schnur, L. F., Spithill, T. W. & Mitchell, G. F. (1986). Passive transfer of Leishmania lipopolysaccharide confers parasite survival in macrophages. Journal of Immunology 137, 3608–14.CrossRefGoogle ScholarPubMed
Heisch, R. B., Grainger, W. E. & Harvey, E. C. (1959). Isolation of a Leishmania from gerbils in Kenya. Journal of Tropical Medicine and Hygiene 62, 158–63.Google ScholarPubMed
Ho, M., Siongok, T. K., Lyerly, W. H. & Smith, D. H. (1982). Prevalence and disease-spectrum in a new focus of visceral leishmaniasis in Kenya. Transactions of the Roal Society of Tropical Medicine and Hygiene 76, 741–6.CrossRefGoogle Scholar
Ho, M., Koech, D. K., Iha, D. W. & Bryceson, A. D. M. (1983). Immunosuppression in Kenyan visceral leishmaniasis. Clinical and Experimental Immunology 51, 207–14.Google ScholarPubMed
Hoeffler, J. P., Meyer, T. E., Waeber, G. & Habener, J. F. (1990). Multiple adenosine 3′, S′-monophosphate response element DNA-binding proteins generated by gene diversification and alternative exon splicing. Molecular Endocrinology 4, 920–30.CrossRefGoogle ScholarPubMed
Howard, J. C., Hale, C. & Chan-Liew, W. L. (1980 b). Immunological regulation of experimental cutaneous leishmaniasis. I. Immunogenetic aspects of susceptibility to Leishmania tropica in mice. Parasite Immunology 2, 303–1 4.CrossRefGoogle ScholarPubMed
Howard, J. G., Hale, C. & Liew, F. Y. (1980 a). Genetically determined susceptibility to Leishmania tropica infection is expressed by haematopoietic donor cells in mouse radiation chimaeras. Nature, London 288, 161–2.CrossRefGoogle ScholarPubMed
Howard, M. K., Kelly, J. M., Lane, R. P. & Miles, M. A. (1991). A sensitive repetitive DNA probe that is specific to the Leishmania donovani complex and its use as an epidemiological and diagnostic reagent. Molecular and Biochemical Parasitology 44, 6372.CrossRefGoogle Scholar
Hunter, T. (1991). Cooperation between oncogenes. Cell 64, 249–70.CrossRefGoogle ScholarPubMed
Hyer, R. N., Julier, C., Buckley, J. D., Trucco, M., Rotter, J., Spielman, R., Barnett, A., Bain, S., Boitard, C., Deschamps, I., Todd, J. A., Bell, J. I. & Lathrop, G. M. (1991). High-resolution linkage mapping for susceptibility genes in human polygenic disease: Insulin-dependent diabetes mellitus and chromosome 11q. American Journal of Human Genetics 48, 243–5 7.Google ScholarPubMed
Introna, M., Hamilton, T. A., Kaufman, R. E., Adams, D. O. & Bast, R. C. JR. (1986). Treatment of murine peritoneal macrophages with bacterial lipopolysaccharide alters expression of c-fos and c myc oncogenes. Journal of Immunology 137, 2711–15.CrossRefGoogle ScholarPubMed
Introna, M., Bast, R. C. JR., Tannenbaum, C. S., Hamilton, T. A. & Adams, D. O. (1987). The effect of LPS on expression of the early ‘competence’ genes JE and KC in murine peritoneal macrophages. Journal of Immunology 138, 3891–6.CrossRefGoogle ScholarPubMed
Kaye, P. M. & Blackwell, J. M. (1989). Lsh, antigen presentation and the development of CMI. Research in Immunology 140, 810–15.CrossRefGoogle ScholarPubMed
Kaye, P. M., Patel, N. K. & Blackwell, J. M. (1988). Acquisition of cell-mediated immunity to Leishmania. II. Lsh gene regulation of accesory cell function. Immunology 65, 1722.Google Scholar
Kennedy, W. P. K. (1984). Novel identification of differences in the kinetoplast DNA of Leishmania isolates by recombinant DNA techniques and in situ hybrization. Molecular and Biochemical Parasitology 12, 313–25.Google Scholar
Kweider, M., Lemesre, J. P., Darcy, F., Kusniehz, J. P., Capron, A. & Santoro, F. (1987). Infectivity of Leishmania braziliensis promastigotes is dependent on the increasing expression of a 65,000-dalton surface antigen. Journal of Immunology 138, 299305.CrossRefGoogle ScholarPubMed
Lamph, W. W., Dwarki, L. V. J., Ofir, R., Montimy, M. & Verma, I. M. (1990). Negative and positive regulation by transfector cAMP response element binding protein is modulated by phosphorylation. Proceedings of the National Academy of Sciences, USA 87, 4320–4.CrossRefGoogle Scholar
Larin, Z., Monaco, A. P. & Lehrach, H. (1991). Yeast artificial chromosome libraries containing inserts from mouse and human DNA. Proceedings of the National Academy of Sciences, USA 88, 4123–7.CrossRefGoogle ScholarPubMed
Lee, M. G. S., Atkinson, B. L., Giannini, S. H. & Van Der Ploeg, L. H. T. (1988). Structure and expression of the hsp7O gene family of Leishmania major. Nucleic Acids Research 16, 9567–85.CrossRefGoogle Scholar
Lin, J.-X & Vilcek, J. (1987). Tumour necrosis factor and interleukin-1 cause a rapid and transient stimulation of c-fos and c-myc mRNA levels in human fibroblasts. Journal of Biological Chemistry 262, 11908–11.CrossRefGoogle Scholar
Love, J. M., Knight, A. M., McAleer, M. A. & Todd, J. A. (1990). Towards construction of a high resolution map of the mouse genome using PCR-analysed microsatellites. Nucleic Acids Research 18, 4123–30.CrossRefGoogle ScholarPubMed
Lynch, N. R., Yarzabel, L., Verde, O., Avila, J. L., Monzon, H. & Convit, J. (1982). Delayed-type-hypersensitivity and immunoglobulin E in American Cutaneous Leishmaniasis. Infection and Immunity 38, 877–81.CrossRefGoogle ScholarPubMed
McConville, M. J. (1990). Structures of the glycoinositol phospholipids from Leishmania major. Journal of Biological Chemistry 265, 7385–94.CrossRefGoogle Scholar
McConville, M. J. & Bacic, A. (1989). A family of glycoinositol phospholipids from Leishmania major. Isolation, characterization and antigenicity. Journal of Biological Chemistry 264, 757–66.CrossRefGoogle ScholarPubMed
MacFarlane, J., Blaxter, M. L., Bishop, R. P., Miles, M. A. & 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, 377–84.CrossRefGoogle Scholar
McNeely, T. B. & Turco, S. J. (1987). Inhibition of protein kinase C activity by the Leishmania donovani lipophosphoglycan. Biochemical and Biophysical Research Communications 148, 653–7.CrossRefGoogle ScholarPubMed
McNeely, T. B. & Turco, S. J. (1990). Requirement of LPG for intracellular survival of Leishmania donovani within human monocytes. Journal of Immunology 144, 2745–50.CrossRefGoogle Scholar
McNeely, T. B., Rosen, G., Londner, M. V. & Turco, S. J. (1989). Inhibitory effect on protein kinase C activity by lipophosphoglycan fragments and glycosyiphosphatidylinositol antigens of the protozoan parasite Leishmania. The Biochemical Journal 259, 601–4.CrossRefGoogle ScholarPubMed
Malo, D., Schurr, E., Epstein, D. J., Vekemans, M., Skamene, E. & Gros, P. (1991). The host resistance locus Bcg is tightly linked to a group of cytoskeleton associated protein genes that include villin and desmin. Genomics 10, 356–64.CrossRefGoogle ScholarPubMed
Mock, B., Krall, M., Blackwell, J., O'Brien, A., Schurr, E., Gros, P., Skamene, E. & Potter, M. (1990). A genetic map of mouse chromosome 1 near the Lsh Ity-Bcg disease resistance locus. Genomics 7, 5764.CrossRefGoogle ScholarPubMed
Murray, P. J., Handman, E., Glaser, T. A. & Spithill, T. W. (1990). Leishmania major: Expression and gene structure of glycoprotein 63 molecule in virulent and avirulent clones and strains. Experimental Parasitology 71, 294304.CrossRefGoogle ScholarPubMed
Neronov, V. M., Stelkova, M. V., Shurkal, A. V., Luschekina, A. A. & Artemyev, M. M. (1987). Natural focality of zoonotic cutaneous leishmaniasis in the Mongolian People's Republic; results and objectives of integrated research. Folia Parasitologia 34, 19.Google ScholarPubMed
O'brien, A. D., Rosenstreich, D. L. & Taylor, B. A. (1980). Control of natural resistance to Salmonella typhimurium and Leishmania donovani in mice by closely linked but distinct genetic loci. Nature, London 287, 440–2.CrossRefGoogle ScholarPubMed
Pampiglione, S., Manson-Bahr, P. E. C., Giungi, F., Giumti, C., Parenti, A. & Trotti, G. C. (1974). Studies of Mediterranean leishmaniasis. 2. Asymptomatic cases of visceral leishmaniasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 68, 447–53.CrossRefGoogle ScholarPubMed
Pelech, S. L. & Vance, D. E. (1989). Signal transduction via phosphatidylcholine cycles. TIBS 14, 2830.Google Scholar
Petersen, E. A., Neva, F. A., Oster, C. N. & Bogaert-Diaz, H. (1982). Specific inhibition of lymphocyte- proliferation responses by adherent suppressor cells in diffuse cutaneous leishmaniasis. New England Journal of Medicine 306, 387–92.CrossRefGoogle ScholarPubMed
Plant, J. & Glynn, A. A. (1974). Natural resistance to Salmonella infection, delayed hypersensitivity and Ir genes in different strains of mice. Nature, London 248, 345–7.CrossRefGoogle ScholarPubMed
Plant, J. & Glynn, A. A. (1976). Genetics of resistance to infection with Salmonella typhimurium in mice. Journal of Infectious Diseases 133, 72–8.CrossRefGoogle ScholarPubMed
Plant, J. & Glynn, A. A. (1979). Locating a salmonella resistance gene on mouse chromosome 1. Clinical and Experimental Immunology 37, 16.Google ScholarPubMed
Plant, J. E., Blackwell, J. M., O'brien, A. D., Bradley, D. J. & Glynn, A. A. (1982). Are the Ish and Ity disease resistance genes at one locus on mouse chromosome 1? Nature, London 297, 510–11.CrossRefGoogle Scholar
Puentes, S. M., Sacks, D. L., Da Silva, R. P. & Joiner, K. A. (1988). Complement binding of two developmental stages of Leishmania major promastigotes varying in expression of a surface lipophosphoglycan. Journal of Experimental Medicine 167, 887902.CrossRefGoogle ScholarPubMed
Puentes, S. M., Da Silva, R. P., Sacks, D. L., Hammer, C. H. & Joiner, K. A. (1990). Serum resistance of metacylcic stage Leishmania major promastigotes is due to release of C5b-9. Journal of Immunology 145, 4311–16.CrossRefGoogle ScholarPubMed
Ready, P. D., Smith, D. F. & Killick-Kendrick, R. (1988). DNA hybridizations on squash-blotted sandflies to identify both insect vector and infection. Leishmania major. Medical and Veterinary Entomology 2, 109–16.CrossRefGoogle Scholar
Reiner, N. E., Lo, R., Llanos-Cuentas, A., Guerra, H., Button, L. L. & McMaster, W. R. (1989). Genetic heterogeneity in Peruvian Leishmania isolates. American Journal of Tropical Medicine and Hygiene 41, 416–21.CrossRefGoogle ScholarPubMed
Rezai, H. R., Ardehali, S. M., Amirhakami, G. & Kharazmi, A. (1978). Immunological features of kala azar. American Journal of Tropical Medicine and Hygiene 27, 1079–83.CrossRefGoogle ScholarPubMed
Risch, N. (1990 a). Linkage strategies for genetically complex traits. I. Multilocus models. American Journal of Human Genetics 46, 222–8.Google ScholarPubMed
Risch, N. (1990 b). Linkage strategies for genetically complex traits. II. The power of affected relative pairs. American Journal of Human Genetics 46, 229–41.Google ScholarPubMed
Risch, N. (1990 c). Linkage strategies for genetically complex traits. III. The effect of marker polymorphism on analysis of affected relative pairs. American Journal of Human Genetics 46, 242–53.Google ScholarPubMed
Roach, T. I. A., Kiderlen, A. F. & Blackwell, J. M. (1991). Role of inorganic nitrogen oxides and TNF-α in killing of Leishmania donovani amastigotes in interferon-γ/LPS activated macrophages from Lsh s and Lshr congenic mouse strains. Infection and Immunity 59, 3935–44.CrossRefGoogle Scholar
Roberts, M., Alexander, J. & Blackwell, J. M. (1989 a). Influence of Lsh, H-2 and H-11-linked gene on visceralization and metastasis associated with Leishmania mexicana infection in mice. Infection and Immunity 57, 875–81.CrossRefGoogle ScholarPubMed
Roberts, M., Alexander, J. & Blackwell, J. M.(1990). Genetic analysis of Leishmania mexicana infection in mice: single gene (Scl-2) controlled predisposition to cutaneous lesion development. Journal of Immunogenetics 17, 89100.CrossRefGoogle ScholarPubMed
Roberts, M., Kaye, P. M., Milon, G. & Blackwell, J. M. (1989 b). Studies of immune mechanisms in H-11- linked genetic susceptibility to murine visceral leishmaniasis. In Leishmaniasis: The Current Status and New Strategies for Control, (ed. Hart, D. T.) pp. 259266. New York and London: Plenum Press.CrossRefGoogle Scholar
Russell, D. G. (1987). The macrophage-attachment glycoprotein gp63 is the predominant C3-acceptor site on Leishmania mexicana promastigotes. European Journal of Biochemistry 164, 213–21.CrossRefGoogle ScholarPubMed
Russell, D. C. & Wilhelm, H. (1986). The involvement of the major surface glycoprotein (gp63) of Leishmania promastigotes in attachment to macrophages. Journal of Immunology 136, 2613–20.CrossRefGoogle ScholarPubMed
Russell, D. C. & Wright, S. D.. (1988). Complement receptor type 3 (CR3) binds to an Arg-Gly-Asp containing region of the major surface glycoprotein, gp63, of Leishmania promastigotes. Journal of Experimental Medicine 168, 279–92.CrossRefGoogle Scholar
Sacks, D. L., Lal, S. L., Shrivastava, S. N., Blackwell, J. M. & Neva, F. A. (1987). An analysis ofT cell responsiveness in Indian kala-azar. Journal of Immunology 138, 908–13.CrossRefGoogle Scholar
Schurr, E., Skamene, E., Forget, A. & Gros, P. (1989). Linkage analysis of the Bcg gene on mouse chromosome 1: identification of a tightly linked marker. Journal of Immunology 142, 4507–13.CrossRefGoogle ScholarPubMed
Schurr, E., Skamene, E., Morgan, K., Chu, M.-L. & Gros, P. (1990). Mapping of Col3a1 and Col6a3 to proximal murine chromosome 1 identifies conserved linkage of structural protein genes between murine chromosome 1 and human chromosome 2q. Genomics 8, 477–86.CrossRefGoogle ScholarPubMed
Schurr, E., Radzioch, D., Malo, D., Gros, P. & Skamene, E. (1991). Molecular genetics of inherited susceptibility to intracellular parasites. Behring Institut Mitteilungen 88, 112.Google Scholar
Searle, S., Campos, A. J. R., Coulson, R. M. R., Spithill, T. W. & Smith, D. F. (1989). A family of heat shock protein-related genes are expressed in the promastigotes of Leishmania major. Nucleic Acids Research 17, 5081–95.CrossRefGoogle Scholar
Skamene, E., Gros, P., Forget, A., Kongshavn, P. A. L., St Charles, C. & Taylor, B. A. (1982). Genetic regulation of resistance to intracellular pathogens. Nature, London 297, 506–9.CrossRefGoogle ScholarPubMed
Skamene, E., Gros, P., Forget, A., Patel, P. J. & Nesbitt, M. N. (1984). Regulation of resistance to leprosy by chromosome 1 gene in the mouse. Immunogenetics 19, 117–24.CrossRefGoogle ScholarPubMed
Smith, D. F., Searle, S., Ready, P. D., Gramiccia, M. & Ben-Ismail, R. (1989). A kinetoplast DNA probe diagnostic for Leishmania major: sequence homologies between regions of Leishmania minicircies. Molecular and Biochemical Parasitology 37, 213–24.CrossRefGoogle Scholar
Smyth, A. J., De Bruijn, M. H. L., Barker, D. C., Ghosh, A., Hassan, M. Q. & Adhya, S. (1992). Rapid and sensitive detection of Leishmania kinetoplast DNA from spleen and blood samples of Kala-Azar patients. Parasitology (in the Press).CrossRefGoogle ScholarPubMed
Strelkova, M. V., Shurkal, A. V., Kellina, O. I., Eliseev, L. N., Evans, D. A., Peters, W., Chapman, C. J., Le Blancq, S. M. & Van Eys, G. J. J. M.(1990). A new species of Leishmania isolated from the great gerbil Rhosnbomys opimus. Parasitology 101, 327–35.CrossRefGoogle ScholarPubMed
Taylor, A. K., Klisak, I., Mohandas, T., Sparkes, R. S., Li, C., Gaynor, R. & Lusis, A. J. (1990). Assignment of the human gene for CREB1 to chromosome 2q32.3/34. Genomics 7, 416–21.CrossRefGoogle Scholar
Taylor, B. A. & O'brien, A. D. (1982). Position on mouse chromosome 1 of a gene that controls resistance to Salmonella typhimurium. Infection and Immunity 36, 1257–60.CrossRefGoogle ScholarPubMed
Tzinia, A. K. & Soteriadou, K. P. (1991). Substrate-dependent pH optima of gp63 purified from seven strains of Leishmania. Molecular and Biochemical Parasitology 47, 8390.CrossRefGoogle ScholarPubMed
Turco, S. J. (1988). The lipophosphoglycan of Leishmania. Parasitology Today 4, 255–7.CrossRefGoogle ScholarPubMed
Turco, S. J. (1990). The Leishmanial lipophosphoglycan: A multifunctional molecule. Experimental Parasitology 70, 241–5.CrossRefGoogle ScholarPubMed
Van Eden, W., Gonzalez, N. M., De Vries, R. H. P., Convit, J. & Van Rood, J. J. (1985). HLA linked control of predisposition to lepromatous leprosy. Journal of Infectious Diseases 151, 914.CrossRefGoogle ScholarPubMed
Verma, I. M. & Sassone-Corsi, P. (1987). Proto-oncogene fos: complex but versatile regulation. Cell 51, 513–14.CrossRefGoogle ScholarPubMed
Webb, J. R., Button, L. L. & McMaster, W. R. (1991). Heterogeneity of the genes encoding the major surface glycoproteins of Leishmania donovani. Molecular and Biochemical Parasitology 48, 173–84.CrossRefGoogle ScholarPubMed
Weeks, D. E. & Lange, K. (1988). The affected-pedigree-member method of linkage analysis. American Journal of Human Genetics 42, 315–26.Google ScholarPubMed
Wilson, A. F., Elston, R. C., Tran, L. D. & Siervogel, H. M. (1991). Use of the robust sib-pair method to screen for single-locus, multiple-locus, and pleiotropic effects: Application to traits related to hypertension. American Journal of Human Genetics 48, 862–72.Google ScholarPubMed
Wilson, M. E., Hardin, K. K. & Donelson, J. E. (1989). Expression of the major surface glycoprotein of Leishmania donovani chagasi in virulent and attenuated promastigotes. Journal of Immunology 143, 678–84.CrossRefGoogle ScholarPubMed
Wirth, D. F. & McMahon-Pratt, D. M. (1982). Rapid identification of Leishmania species by specific hybridization of kinetoplast DNA in cutaneous lesions. Proceedings of the National Academy of Sciences, USA 79, 69997003.CrossRefGoogle ScholarPubMed
Zwilling, B. S., Vespa, L. & Massie, M. S. (1987). Regulation of 1-A expression by murine peritoneal macrophages: differences linked to the Bcg gene. Journal of Immunology 138, 1372–6.CrossRefGoogle Scholar