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Immunogenic Glycoconjugates Implicated in Parasitic Nematode Diseases

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Immunogenic Glycoconjugates Implicated in Parasitic Nematode Diseases View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Biochimica et Biophysica Acta 1455 (1999) 353^362 www.elsevier.com/locate/bba Review Immunogenic glycoconjugates implicated in parasitic nematode diseases Anne Dell a;*, Stuart M. Haslam a, Howard R. Morris a, Kay-Hooi Khoo b a Department of Biochemistry, Imperial College of Science Technology and Medicine, London SW7 2AZ, UK b Institute of Biological Chemistry, Academia Sinica, Taipei, Taiwan Received 13 October 1998; received in revised form 11 February 1999; accepted 1 April 1999 Abstract Parasitic nematodes infect billions of people world-wide, often causing chronic infections associated with high morbidity. The greatest interface between the parasite and its host is the cuticle surface, the outer layer of which in many species is covered by a carbohydrate-rich glycocalyx or cuticle surface coat. In addition many nematodes excrete or secrete antigenic glycoconjugates (ES antigens) which can either help to form the glycocalyx or dissipate more extensively into the nematode's environment. The glycocalyx and ES antigens represent the main immunogenic challenge to the host and could therefore be crucial in determining if successful parasitism is established. This review focuses on a few selected model systems where detailed structural data on glycoconjugates have been obtained over the last few years and where this structural information is starting to provide insight into possible molecular functions. ß 1999 Elsevier Science B.V. All rights reserved. Keywords: Nematode; Glycoconjugate; Antigen; Structure Contents 1. Introduction .......................................................... 354 2. The biology of nematodes ................................................ 355 3. Glycosylated nematode antigens ............................................ 355 3.1. Overview . ...................................................... 355 3.2. O-Methylated glycans of Toxocara ...................................... 356 3.3. Tyvelose as an immunodominant epitope .................................. 357 3.4. Phosphorylcholine substituted glycans . .................................. 358 3.5. Novel fucosylated N-glycan core structures ................................ 359 4. Concluding remarks . ................................................. 359 Acknowledgements . ...................................................... 360 References ............................................................... 360 * Corresponding author. Fax: +44-171-2250458; E-mail: [email protected] 0925-4439 / 99 / $ ^ see front matter ß 1999 Elsevier Science B.V. All rights reserved. PII: S0925-4439(99)00064-2 BBADIS 61869 15-9-99 354 A. Dell et al. / Biochimica et Biophysica Acta 1455 (1999) 353^362 1. Introduction Table 1 Outline classi¢cation of the nematodes, emphasis on nematode `Parasitic helminth' is a loosely de¢ned term that is orders and families containing important human parasites commonly used to describe metazoan parasites from Phylum: Nematoda (roundworms) mainly two phyla, the Nematoda (roundworms) (see Subclass: Aphasmidia Order: Trichocephalida Table 1), and the Platyhelminths (£atworms) which Trichinella spiralis, Trichuris trichuria (whipworm) include the class Cestoda (tapeworms) and the class Subclass: Phasmidia Trematoda (£ukes). Helminth infections are highly Order: Rhabditida prevalent globally, particularly among the popula- Strongyloides stercoralis, Caenorhabditis elegans (laboratory tion of the developing world. It is estimated that model) over 3 billion cases of single or mixed infections Order: Strongylida Family: Trichostrongylidae are caused by the three most prevalent intestinal Haemonchus contortus (parasite of domestic ruminants) nematodes: large roundworm (Ascaris lumbricoides), Family: Ancylostomatidae (hookworm) whipworm (Trichuris trichuria), and hookworm (An- Necator americanus, Ancylostoma duodenale, and other Ancylos- cylostoma duodenale and Necator americanus) [5]. In toma spp. addition, about 150 million people are a¥icted by Order: Ascaridida Family: Ascaridae lymphatic ¢lariasis and onchocerciasis due to infec- Ascaris lumbricoides, Toxocara spp. (only larvae in humans) tion with one of the ¢larial nematodes (Wuchereria Order: Oxyurida bancrofti, Brugia malayi, Onchocerca volvulus) Enterobius vermicularis (pinworm) [40,41]. Order: Spirurida In humans, the most striking feature of parasitic Family: Filariidae helminths is protracted survival within the host, with Wuchereria bancrofti, Brugia malayi (causing lymphatic ¢laria- sis), Onchocerca volvulus (causing river blindness and onchoder- disease severity typically related to cumulative worm matitis), Acanthocheilonema viteae (laboratory model) burden. Disease may result from local host immuno- Family: Dracunculidae logical responses to sites at which the parasites have Dracunculus mediinensis (causing dracunculiasis or guinea worm accumulated, as well as tissue damage generated by disease) the invasion, migration, and development of larvae in the host. Tissue reactions include immediate hy- persensitivity, allergic reactions, and delayed-type cell mediated reactions with granuloma and giant sion, host mimicry, evasive diversionary strategies, or cell formation. Although infection seldom leads to perhaps involvement in host lectin binding, targeting, severe acute illness or death, moderate and chronic and signalling. Any role in disease manifestation is infection does engender morbidity and signi¢cantly arguably incidental, due to improper or excessive impairs the quality of life, economic productivity, host responses to the o¡ensive antigens. and even the physical and cognitive development in This minireview is not intended to be a compre- children with high worm load. hensive coverage of all glycoconjugates identi¢ed or To date, there is no de¢nitive identi¢cation of a implicated in parasitic helminth diseases or immu- particular helminth glycoconjugate in mediating a nobiology. Rather, we focus on a few selected model speci¢c host immune response which would lead to systems where detailed structural data on glycocon- manifestation of clinical pathology or disease. Yet it jugates have been obtained over the last few years. It is well recognised that the parasite antigens, either is our ¢rm belief that only when structural data are excreted-secreted (ES antigens) or on the surface, in hand can we begin to understand the glycobiology are key modulators or targets of host immune sys- of host-parasite interactions. The trematode schisto- tems [3,28], and that the immunodominant epitopes some remains the single most well studied system and are often glycans of very unique structures [31^34]. It is separately addressed elsewhere in this volume [6]. is felt that the respective glycoconjugates must medi- We focus here on the parasitic nematodes. Several ate speci¢c parasite defense or survival mechanisms, recent general reviews on helminth immunology can possibly in the form of immune-modulation/suppres- be found elsewhere [1,10,11,14,37,38,45] and inter- BBADIS 61869 15-9-99 A. Dell et al. / Biochimica et Biophysica Acta 1455 (1999) 353^362 355 ested readers are referred to these articles for a more at least some of the excretory/secretory (ES) prod- in-depth discussion on the immunological responses ucts. elicited by parasitic antigens. 3. Glycosylated nematode antigens 2. The biology of nematodes 3.1. Overview The important parasitic nematodes of humans are commonly grouped into two subsets, the intestinal The nematode surface and ES antigens represent nematodes and the ¢larial species. Most nematodes the major immunogenic challenge to the host and share highly conserved developmental stages. The di- may be the key to successful parasite defense strat- oecious adults sexually produce eggs that hatch to egies. It is well recognised that the immunodominant release L1 larvae which, with intervening cuticular epitopes on both sources of antigens are often peri- moults and size increases, develop through three odate- and/or peptide-N-glycosidase sensitive. The more larval phases (L2, L3, and L4) before attaining prevalence of saccharide determinants on the parasite full sexual maturity. Transmission to a new host de- surface and the ES antigens was further shown by pends upon the ingestion of mature infectious eggs numerous lectin binding studies (reviewed in [34]). or larvae, or the penetration of the skin or mucous Yet, to date, only a few of the implicated glycans membrane by the larvae. The soil-transmitted intes- have actually been structurally de¢ned. Two oppos- tinal nematodes have evolved a direct life cycle; their ing characteristics are applicable to these glycosy- eggs or larvae normally leave the host via the faeces lated epitopes, namely antigenic speci¢city and and become infective during a period of development cross-reactivity. The former implies that a particular in the soil. Infections with the insect vector-transmit- nematode species or its larval stage may harbour ted ¢larial species are initiated when the blood suck- unique saccharide sequences which are speci¢c ing vectors bite; the L3 larvae emerge from the insect enough to be clinically diagnostic, as exempli¢ed by mouth parts and actively penetrate the feeding the tyvelose containing glycans of T. spiralis (see wound in the skin before migrating to the ¢nal site Section 3.3). The latter relates to the phenomenon of infection. Not uncommonly larval stages in mam- that the same immunogenic
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