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Variation and polymorphism in helminth parasites

Published online by Cambridge University Press:  29 May 2003

R. M. MAIZELS  and
A. KURNIAWAN-ATMADJA
R. M. MAIZELS
Affiliation:
Institute of Cell, Animal and Population Biology, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK
A. KURNIAWAN-ATMADJA
Affiliation:
Department of Parasitology, Faculty of Medicine, University of Indonesia, Salemba Raya 6, Jakarta 10430, Indonesia
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Abstract

There are strong biological, evolutionary and immunological arguments for predicting extensive polymorphism among helminth parasites, but relatively little data and few instances from which the selective forces acting on parasite diversity can be discerned. The paucity of information on intraspecific variation stands in contrast to the fine detail with which helminth species have been delineated by morphological techniques, accentuating a trend towards considering laboratory strains as representative of a relatively invariant organism. However, in the fast-moving evolutionary race between host and parasite one would predict a monomorphic species would be driven to extinction. We review the arena of intraspecific variation for the major helminth parasites, ranging from biological properties such as host or vector preference, to biochemical and immunological characteristics, as well as molecular markers such as DNA sequence variants. These data are summarized, before focusing in more detail on polymorphisms within protein-coding genes of potential relevance to the host-parasite relationship, such as vaccine candidates. In particular, we discuss the available data on a number of major antigens from the filarial nematode Brugia malayi. Information is currently too sparse to answer the question of whether there is antigenic variation in filariasis, but the indications are that proteins from the blood-borne microfilarial stage show significant intraspecific variability. Future work will define whether polymorphisms in these antigens may be driven by exposure to the host immune response or reflect some other facet of parasite biology.

Keywords

Antigenic variationgenetic polymorphismnematodesfilariasis
Type
Research Article
Information
Parasitology , Volume 125 , Issue 7 , May 2002 , pp. S25 - S37
Copyright
© 2002 Cambridge University Press

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References

ANDERSON, T. J. C., BLOUIN, M. S. & BEECH, R. N. (1998). Population biology of parasitic nematodes: applications of genetic markers. Advances in Parasitology 41, 219–283.CrossRefGoogle Scholar
ANDERSON, T. J. C. & JAENIKE, J. (1997). Host specificity, evolutionary relationships and macrogeographic differentiation among Ascaris populations from humans and pigs. Parasitology 115, 325–342.CrossRefGoogle Scholar
ANDERSON, T. J. C., ROMERO-ABAL, M. E. & JAENIKE, J. (1993). Genetic structure and epidemiology of Ascaris populations: patterns of host affiliation in Guatemala. Parasitology 107, 319–334.CrossRefGoogle Scholar
ANDERSON, T. J. C., ROMERO-ABAL, M. E. & JAENIKE, J. (1995). Mitochondrial DNA and Ascaris microepidemiology: the composition of parasite populations from individual hosts, families and villages. Parasitology 110, 221–229.CrossRefGoogle Scholar
ARNOLD, K., VENEGAS, A., HOUSEWEART, C. & FUHRMAN, J. A. (1996). Discrete transcripts encode multiple chitinase isoforms in Brugian microfilariae. Molecular and Biochemical Parasitology 80, 149–158.CrossRefGoogle Scholar
BAIN, O., CHANDRASEKHARAN, S. A., PARTONO, F., MAK, J. W., ZHENG, H. J., SEO, B. S. & WU, S. H. (1989). Discrimination de souches géographiques de Brugia malayi périodique par l'ornementation cuticulaire des males. Annales de Parasitologie Humaine et Comparée 63, 209–223.Google Scholar
BEECH, R. N., PRICHARD, R. K. & SCOTT, M. E. (1994). Genetic variability of the beta-tubulin genes in benzimidazole-susceptible and -resistant strains of Haemonchus contortus. Genetics 138, 103–110.Google Scholar
BELLABY, T., ROBINSON, K. & WAKELIN, D. (1996). Induction of differential T-helper-cell responses in mice infected with variants of the parasitic nematode Trichuris muris. Infection and Immunity 64, 791–795.Google Scholar
BELLABY, T., ROBINSON, K., WAKELIN, D. & BEHNKE, J. M. (1995). Isolates of Trichuris muris vary in their ability to elicit protective immune responses in mice. Parasitology 111, 353–357.CrossRefGoogle Scholar
BIANCO, A. E., ROBERTSON, B. D., KUO, Y.-M., TOWNSON, S. & HAM, P. (1990). Developmentally regulated expression and secretion of a polymorphic antigen by Onchocerca infective-stage larvae. Molecular and Biochemical Parasitology 39, 203–212.CrossRefGoogle Scholar
BIANCO, A. E., WU, Y. & JENKINS, R. E. (1995). Onchocerca spp: a “family” of secreted acidic proteins expressed by infective larvae in blackflies. Experimental Parasitology 81, 344–354.CrossRefGoogle Scholar
BLACKHALL, W. J., LIU, H. Y., XU, M., PRICHARD, R. K. & BEECH, R. N. (1998). Selection at a P-glycoprotein gene in ivermectin- and moxidectin-selected strains of Haemonchus contortus. Molecular and Biochemical Parasitology 95, 193–201.CrossRefGoogle Scholar
BLAXTER, M. L., ASLETT, M., GUILIANO, D., DAUB, J. & THE FILARIAL GENOME PROJECT (1999). Parasitic helminth genomics. In Parasitology 118, S39–S51.CrossRef
BOLAS-FERNANDEZ, F. & WAKELIN, D. (1990). Infectivity, antigenicity and host responses to isolates of the genus Trichinella. Parasitology 100, 491–497.CrossRefGoogle Scholar
BOTTO, C., ARANGO, M. & YARZÁBAL, L. (1984). Onchocerciasis in Venezuela: prevalence of microfilaraemia in Amerindians and morphological characteristics of the microfilariae from the Upper Orinoco focus. Tropenmedizin und Parasitologie 35, 167–173.Google Scholar
BUCKLEY, J. J. C. (1960). On Brugia gen. nov. for Wuchereria spp. of the malayi group i.e. Wuchereria malayi (Brug, 1927) Wuchereria pahangi Buckley and Edeson 1956 and Wuchereria patei Buckley, Nelson, Heisch 1958. Annals of Tropical Medicine and Parasitology 54, 75–77.Google Scholar
COOKSON, E., BLAXTER, M. L. & SELKIRK, M. E. (1992). Identification of the major soluble cuticular protein of lymphatic filarial nematode parasites (gp29) as a secretory homolog of glutathione peroxidase. Proceedings of the National Academy of Sciences, USA 89, 5837–5841.CrossRefGoogle Scholar
COOKSON, E., TANG, L. & SELKIRK, M. E. (1993). Conservation of primary sequence of gp29, the major soluble cuticular glycoprotein, in three species of lymphatic filariae. Molecular and Biochemical Parasitology 58, 155–160.CrossRefGoogle Scholar
CURTIS, J. & MINCHELLA, D. J. (2000). Schistosome population genetic structure: when clumping worms is not just splitting hairs. Parasitology Today 16, 68–71.CrossRefGoogle Scholar
DUKE, B. O. L. (1980). Observations on Onchocerca volvulus in experimentally infected chimpanzees. Tropenmedizin und Parasitologie 31, 41–54.Google Scholar
EDESON, J. F. B. & WHARTON, R. H. (1958). The experimental transmission of Wuchereria malayi from man to various animals on Malaya. Transactions of the Royal Society of Tropical Medicine and Hygiene 52, 25–45.CrossRefGoogle Scholar
ELARD, L., COMES, A. M. & HUMBERT, J. F. (1996). Sequences of β-tubulin cDNA from benzimidazole-susceptible and -resistant strains of Teladorsagia circumcincta, a nematode parasite of small ruminants. Molecular and Biochemical Parasitology 79, 249–253.CrossRefGoogle Scholar
ERTTMANN, K. D., UNNASCH, T. R., GREENE, B. M., ALBIEZ, E. J., BOATENG, J., DENKE, A. M., FERRARONI, J. J., KARAM, M., SCHULZ-KEY, H. & WILLIAMS, P. N. (1987). A DNA sequence specific for forest form Onchocerca volvulus. Nature 327, 415–417.CrossRefGoogle Scholar
FLOCKHART, H. A., CIBULSKIS, R. E., KARAM, M. & ALBIEZ, E. J. (1986). Onchocerca volvulus: enzyme polymorphism in relation to the differentiation of forest and savannah strains of this parasite. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 285–292.CrossRefGoogle Scholar
FRASER, E. M. & KENNEDY, M. W. (1991). Heterogeneity in the expression of surface-exposed epitopes among larvae of Ascaris lumbricoides. Parasite Immunology 13, 219–225.CrossRefGoogle Scholar
FUHRMAN, J. A. (1995). Filarial chitinases. Parasitology Today 11, 259–261.CrossRefGoogle Scholar
FUHRMAN, J. A., LANE, W. S., SMITH, R. F., PIESSENS, W. F. & PERLER, F. B. (1992). Transmission-blocking antibodies recognize microfilarial chitinase in brugian lymphatic filariasis. Proceedings of the National Academy of Sciences, USA 89, 1548–1552.CrossRefGoogle Scholar
FUHRMAN, J. A., LEE, J. & DALAMAGAS, D. (1995). Structure and function of a family of chitinase isozymes from Brugian microfilariae. Experimental Parasitology 80, 672–680.CrossRefGoogle Scholar
GILLEARD, J. S., DUNCAN, J. L. & TAIT, A. (1995). An immunodominant antigen on the Dictyocaulus viviparus L3 sheath surface coat and a related molecule in other strongylid nematodes. Parasitology 111, 193–200.CrossRefGoogle Scholar
GOYAL, P. K. & WAKELIN, D. (1993). Vaccination against Trichinella spiralis in mice using antigens from different isolates. Parasitology 107, 311–317.CrossRefGoogle Scholar
GREGORY, W. F., ATMADJA, A. K., ALLEN, J. E. & MAIZELS, R. M. (2000). The abundant larval transcript 1/2 genes of Brugia malayi encode stage-specific candidate vaccine antigens for filariasis. Infection and Immunity 68, 4174–4179.CrossRefGoogle Scholar
HACKETT, F., SIMPSON, A. J. G., OMER-ALI, P. & SMITHERS, S. R. (1987). Surface antigens of and cross-protection between two geographical isolates of Schistosoma mansoni. Parasitology 94, 301–312.CrossRefGoogle Scholar
HARNETT, W., CHAMBERS, A. E., RENZ, A. & PARKHOUSE, R. M. E. (1989). An oligonucleotide probe specific for Onchocerca volvulus. Molecular and Biochemical Parasitology 35, 119–125.CrossRefGoogle Scholar
HAWDON, J. M., JONES, B. F., HOFFMAN, D. R. & HOTEZ, P. J. (1996). Cloning and characterization of Ancylostoma-secreted protein. A novel protein associated with the transition to parasitism by infective hookworm larvae. Journal of Biological Chemistry 271, 6672–6678.Google Scholar
HAWKING, F. (1975). Circadian and other rhythms of parasites. Advances in Parasitology 13, 123–182.CrossRefGoogle Scholar
HIRZMANN, J., SCHNAUFER, A., HINTZ, M., CONRATHS, F., STIRM, S., ZAHNER, H. & HOBOM, G. (1995). Brugia spp. and Litomosoides carinii: identification of a covalently cross-linked microfilarial sheath matrix protein (shp2). Molecular and Biochemical Parasitology 70, 95–106.Google Scholar
HOEKSTRA, R., OTSEN, M., TIBBEN, J., LENSTRA, J. A. & ROOS, M. H. (2000). Transposon associated markers for the parasitic nematode Haemonchus contortus. Molecular and Biochemical Parasitology 105, 127–135.CrossRefGoogle Scholar
JOHNSTON, D. A., BLAXTER, M. L., DEGRAVE, W. M., FOSTER, J., IVENS, A. C. & MELVILL, S. E. (1999). Genomics and the biology of parasites. BioEssays 21, 131–147.3.0.CO;2-I>CrossRefGoogle Scholar
JOSEPH, G. T., HUIMA, T. & LUSTIGMAN, S. (1998). Characterization of an Onchocerca volvulus L3-specific larval antigen, Ov-ALT-1. Molecular and Biochemical Parasitology 96, 177–183.CrossRefGoogle Scholar
KEDDIE, E. M., HIGAZI, T., BOAKYE, D., MERRIWEATHER, A., WOOTEN, M. C. & UNNASCH, T. R. (1999). Onchocerca volvulus: limited heterogeneity in the nuclear and mitochondrial genomes. Experimental Parasitology 93, 198–206.CrossRefGoogle Scholar
KWA, M. S. G., VEENSTRA, J. G. & ROOS, M. H. (1994). Benzimidazole resistance in Haemonchus contortus is correlated with a conserved mutation at amino acid 200 in β-tubulin isotype 1. Molecular and Biochemical Parasitology 63, 299–303.CrossRefGoogle Scholar
LAURIE, C. C. & STAM, L. F. (1994). The effect of an intronic polymorphism on alcohol dehydrogenase expression in Drosophila melanogaster. Genetics 138, 379–385.Google Scholar
LESLIE, J. F., CAIN, G. D., MEFFE, G. K. & VRIJENHOEK, R. C. (1982). Enzyme polymorphism in Ascaris suum (Nematoda). Journal of Parasitology 68, 576–587.CrossRefGoogle Scholar
LOVERDE, P. T., DEWALD, J., MINCHELLA, D. J., BOSSHARDT, S. C. & DAMIAN, R. T. (1985). Evidence for host-induced selection in Schistosoma mansoni. Journal of Parasitology 71, 297–301.CrossRefGoogle Scholar
MACKENZIE, A. & QUINN, J. (1999). A serotonin transporter gene intron 2 polymorphic region, correlated with affective disorders, has allele-dependent differential enhancer-like properties in the mouse embryo. Proceedings of the National Academy of Sciences, USA 96, 15251–15255.CrossRefGoogle Scholar
MAIZELS, R. M. & LAWRENCE, R. A. (1991). Immunological tolerance: the key feature in human filariasis? Parasitology Today 7, 271–276.Google Scholar
MAIZELS, R. M., BLAXTER, M. L. & SCOTT, A. L. (2001). Immunogenomics of filariasis: genes implicated in immune evasion and protective immunity. Parasite Immunology 23, 327–344.CrossRefGoogle Scholar
MAIZELS, R. M., GOMEZ-ESCOBAR, N., GREGORY, W. F., MURRAY, J. & ZANG, X. (2001). Immune evasion genes from filarial nematodes. International Journal for Parasitology 31, 889–898.CrossRefGoogle Scholar
MAIZELS, R. M., GREGORY, W. F., KWAN-LIM, G.-E. & SELKIRK, M. E. (1989). Filarial surface antigens: the major 29,000 mol.wt. glycoprotein and a novel 17,000–200,000 mol.wt. complex from adult Brugia malayi parasites. Molecular and Biochemical Parasitology 32, 213–227.Google Scholar
MAIZELS, R. M., PARTONO, F., OEMIJATI, S., DENHAM, D. A. & OGILVIE, B. M. (1983). Cross-reactive surface antigens on three stages of Brugia malayi, B. pahangi and B. timori. Parasitology 87, 249–263.Google Scholar
MCGREEVY, P. B., RATIWAYANTO, S., TUTI, S., MCGREEVY, M. M. & DENNIS, D. T. (1980). Brugia malayi: relationship between anti-sheath antibodies and amicrofilaremia in natives living in an endemic area of South Kalimantan, Borneo. American Journal of Tropical Medicine and Hygiene 29, 553–562.CrossRefGoogle Scholar
MCMAHON, J. E., SOWA, S. I., MAUDE, G. H. & KIRKWOOD, B. R. (1988). Onchocerciasis in Sierra Leone 2: a comparison of forest and savanna villages. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 595–600.CrossRefGoogle Scholar
MCMANUS, D. P. & BOWLES, J. (1996). Molecular genetic approaches to parasite identification: their value in diagnostic parasitology and systematics. International Journal for Parasitology 26, 687–704.CrossRefGoogle Scholar
MEREDITH, S. E. O., UNNASCH, T. R., KARAM, M., PIESSENS, W. F. & WIRTH, D. F. (1989). Cloning and characterization of an Onchocerca volvulus specific DNA sequence. Molecular and Biochemical Parasitology 36, 1–10.CrossRefGoogle Scholar
MOLONEY, N. A., GARCIA, E. G. & WEBBE, G. (1985). The strain specificity of vaccination with ultra violet attenuated cercariae of the Chinese strain of Schistosoma japonicum. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 245–247.CrossRefGoogle Scholar
MOLONEY, N. A., HINCHCLIFFE, P. & WEBBE, G. (1989). Cross protection between a laboratory passaged Chinese strain of Schistosoma japonicum and field isolates of S. japonicum from China. Transactions of the Royal Society of Tropical Medicine and Hygiene 83, 83–85.CrossRefGoogle Scholar
MURRAY, J., GREGORY, W. F., GOMEZ-ESCOBAR, N., ATMADJA, A. K. & MAIZELS, R. M. (2001). Expression and immune recognition of Brugia malayi VAL-1, a homologue of vespid venom allergens and Ancylostoma secreted proteins. Molecular and Biochemical Parasitology 118, 89–96.CrossRefGoogle Scholar
NADLER, S. A. (1986). Biochemical polymorphism in Parascaris equorum, Toxocara canis and Toxocara cati. Molecular and Biochemical Parasitology 18, 45–54.CrossRefGoogle Scholar
NADLER, S. A. (1990). Molecular approaches to studying helminth population genetics and phylogeny. International Journal for Parasitology 20, 11–29.CrossRefGoogle Scholar
NADLER, S. A. (1995). Microevolution and the genetic structure of parasite populations. Journal of Parasitology 81, 395–403.CrossRefGoogle Scholar
PALMIERI, J. R., PURNOMO, DENNIS, D. T. & MARWOTO, H. A. (1980). Filarid parasites of South Kalimantan (Borneo) Indonesia. Wuchereria kalimantani sp. n. (Nematoda: Filarioidea) from the silvered leaf monkey, Presbytis cristatus Eschscholtz 1921. Journal of Parasitology 66, 645–651Google Scholar
PARTONO, F. (1987). The spectrum of disease in lymphatic filariasis. In Filariasis (ed. EVERARD, D. & CLARK, S.), pp. 15–31. Chichester, Chichester.
PARTONO, F. & PURNOMO (1987). Periodicity studies of Brugia malayi in Indonesia: recent findings and a modified classification of the parasite. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 657–662.CrossRef
PRICHARD, R. (2001). Genetic variability following selection of Haemonchus contortus with anthelmintics. Trends in Parasitology 17, 445–453.CrossRefGoogle Scholar
QIANG, S., BIN, Z., SHU-HUA, X., ZHENG, F., HOTEZ, P. & HAWDON, J. M. (2000). Variation between ASP-1 molecules from Ancylostoma caninum in China and the United States. Journal of Parasitology 86, 181–185.CrossRefGoogle Scholar
RAVINDRAN, B., SATAPATHY, A. K. & SAHOO, P. K. (1994). Bancroftian filariasis – differential reactivity of anti-sheath antibodies in microfilariae carriers. Parasite Immunology 16, 321–323.CrossRefGoogle Scholar
READ, A. F. & VINEY, M. E. (1996). Helminth immunogenetics: why bother? Parasitology Today 12, 337–343.Google Scholar
ROMEO DE LEON, J. & DUKE, B. O. (1966). Experimental studies on the transmission of Guatemalan and West African strains of Onchocerca volvulus by Simulium ochraceum, S. metallicum and S. callidum. Transactions of the Royal Society of Tropical Medicine and Hygiene 60, 735–752.CrossRefGoogle Scholar
SANGSTER, N. (1996). Pharmacology of anthelmintic resistance. Parasitology 113, S201–S216.CrossRefGoogle Scholar
SASA, M. (1976). Human Filariasis. A Global Survey of Epidemiology and Control. Baltimore, University Park Press.
SELKIRK, M. E., YAZDANBAKHSH, M., FREEDMAN, D., BLAXTER, M. L., COOKSON, E., JENKINS, R. E. & WILLIAMS, S. A. (1991). A proline-rich structural protein of the surface sheath of larval Brugia filarial nematode parasites. Journal of Biological Chemistry 266, 11002–11008.Google Scholar
SEN, H. G. (1972). Necator americanus: behaviour in hamsters. Experimental Parasitology 32, 26–32.CrossRefGoogle Scholar
SHIMOGIRI, T., KONO, M., MANNEN, H., MIZUTANI, M. & TSUJI, S. (1998). Chicken ornithine transcarbamylase gene, structure, regulation, and chromosomal assignment: repetitive sequence motif in intron 3 regulates this enzyme activity. Journal of Biochemistry (Tokyo) 124, 962–971.CrossRefGoogle Scholar
SOLOMON, M. S. & HALEY, A. J. (1966). Biology of the rat nematode Nippostrongylus brasiliensis (Travassos, 1914). V. Characteristics of N. brasiliensis after serial passage in the laboratory mouse. Journal of Parasitology 52, 237–241.Google Scholar
STAM, L. F. & LAURIE, C. C. (1996). Molecular dissection of a major gene effect on a quantitative trait: the level of alcohol dehydrogenase expression in Drosophila melanogaster. Genetics 144, 1559–1564.Google Scholar
SU, Z. & DOBSON, C. (1997). Genetic and immunological adaptation of Heligmosomoides polygyrus in mice. International Journal for Parasitology 27, 653–663.CrossRefGoogle Scholar
TANG, L., SMITH, V. P., GOUNARIS, K. & SELKIRK, M. E. (1996). Brugia pahangi: the cuticular glutathione peroxidase (gp29) protects heterologous membranes from lipid peroxidation. Experimental Parasitology 82, 329–332.CrossRefGoogle Scholar
THE FILARIAL GENOME PROJECT (1999). Deep within the filarial genome: an update on progress in the Filarial Genome Project. Parasitology Today 15, 219–224.Google Scholar
UNDERWOOD, A. P., SUPALI, T., WU, Y. & BIANCO, A. E. (2000). Two microsatellie loci from Brugia malayi show polymorphisms among isolates from Indonesia and Malaysia. Molecular and Biochemical Parasitology 106, 299–302.CrossRefGoogle Scholar
UNNASCH, T. R. & WILLIAMS, S. A. (2000). The genomes of Onchocerca volvulus. International Journal for Parasitology 30, 543–552.CrossRefGoogle Scholar
WAKELIN, D. & GOYAL, P. K. (1996). Trichinella isolates: parasite variability and host responses. International Journal for Parasitology 26, 471–481.CrossRefGoogle Scholar
WESCOTT, R. B. & TODD, A. C. (1966). Adaptation of Nippostrongylus brasiliensis to the mouse. Journal of Parasitology 52, 233–236.CrossRefGoogle Scholar
WILSON, T., EDESON, J. F. B., WHARTON, R. H., REID, J. A., TURNER, L. H. & LAING, A. B. G. (1959). The occurrence of two forms of Wuchereria malayi in man. Transactions of the Royal Society of Tropical Medicine and Hygiene 53, 480–481.Google Scholar
ZAHNER, H., HOBOM, G. & STIRM, S. (1995). The microfilarial sheath and its proteins. Parasitology Today 11, 116–120.CrossRefGoogle Scholar
ZENG, W. & DONELSON, J. E. (1992). The actin genes of Onchocerca volvulus. Molecular and Biochemical Parasitology 55, 207–216.CrossRefGoogle Scholar