- Email: [email protected]
Echinostomes as experimental models for interactions between adult parasites and vertebrate hosts
Update
TRENDS in Parasitology
Vol.21 No.6 June 2005
Research Focus
Echinostomes as experimental models for interactions between adult parasites and vertebrate hosts Rafael Toledo1 and Bernard Fried2 1
Departamento de Parasitologı´a, Facultad de Farmacia, Universidad de Valencia, Avenida Vicente Andre´s Estelle´s, 46100 Burjassot, Valencia, Spain 2 Department of Biology, Lafayette College, Easton, PA 18042, USA
Echinostomes are intestinal trematodes that, for years, have served as experimental models in different areas of parasitology. However, the usefulness of these trematodes in experimental parasitology has been underappreciated. In this article, we examine the characteristics that make echinostomes useful models for analysis of the interactions between adult parasites and vertebrate hosts, particularly in relation to the host-related factors that determine the establishment of the parasites.
de
f
o st
(a)
Activ e in fect ion of the firs t in te
es ti o
by
eh t iv in i
Definitive host
ia ed rm
n
Seeking a perfect model The understanding of host-related factors that determine the course of intestinal helminth infections is essential for helminthologists. However, the investigation of this topic
is difficult because it requires the use of experimental models that enable comparative studies of the development of a single parasite species in different hosts. In this context, echinostomes, particularly Echinostoma caproni, can be suitable models. As shown in previous studies, the course and characteristics of E. caproni infections are dependent largely on host-related factors [1,2]. This enables the study of one species of helminth within different experimental hosts in which the course of infection differs markedly. Echinostomes are important intestinal parasitic flatworms that invade domestic animals, wildlife and humans [3]. In their larval stages, echinostomes parasitize several invertebrate and cold-blooded vertebrate hosts (Figure 1).
(c)
(b)
st ho te
Ing
Water
(d) (h) (e) Second intermediate host (g)
A c ti
ve in fe
c ti o n o f t
(f) First intermediate host
Water
t hos diate he second inter me
Figure 1. Generalized life cycle of Echinostoma spp. (a) Adult worms inhabit the small intestine of several vertebrate hosts, including humans. (b) Eggs are voided with the host faeces. (c) Miracidia hatch in fresh water and actively infect snails. (d) Sporocysts, (e) mother rediae and (f) daughter rediae are the intramolluscan stages. (g) Cercariae are released and swim to locate the second intermediate host (snails, amphibians, bivalves and fishes), in which they encyst to become metacercariae. (h) Metacercariae are ingested by the definitive host and excyst to become adults. Images adapted, with permission, from Ref. [23]. Corresponding author: Toledo, R. ([email protected]). Available online 26 April 2005 www.sciencedirect.com
252
Update
TRENDS in Parasitology
These ubiquitous parasites are easy to maintain in the laboratory as larval and adult worm stages. For this reason, echinostomes (particularly members of the genus Echinostoma) have served as experimental animal models at all levels of organization and have contributed to studies in different areas of parasitology. However, the usefulness of these trematodes in experimental parasitology has often been underappreciated. Further use of echinostomes as experimental models might be helpful for identifying the host-related factors responsible for either worm rejection or worm maintenance in intestinal helminth infections. The need for new experimental models The factors that determine the course of intestinal helminth infection have been studied extensively using intestinal nematode parasites. Several nematode and rodent species (mainly mice) have been used as experimental models [4,5]. However, the results obtained have not been definitive and it has been observed that the course of infection depends on several factors related to both the host and the parasite species [6]. It is generally accepted that worm rejection is related to T helper (Th)2 responses mediated by the production of interleukin (IL)-4. By contrast, chronicity seems to be associated with Th1 responses mediated by IL-12, tumor necrosis factor (TNF)-a and interferon (IFN)-g [5–9]. However, the mechanisms involved in these responses and the host- and parasite-dependent factors are difficult to study [6,9]. One factor preventing further conclusions is the absence of adequate experimental models. To date, the models used present several problems: (i) some of the nematode species used develop only in one species of experimental host, thereby preventing comparative studies; (ii) other nematode species present tissue phases or inhabit the caecum, making it difficult to interpret the experimental results. Hence, there is a need to develop new experimental models [9]. In this context, echinostomes, particularly E. caproni, could be extremely useful. Echinostomes and interactions between adult parasites and vertebrate hosts E. caproni has a wide range of definitive hosts, although its compatibility differs considerably among rodent species on the basis of worm survival in each host species. In highly compatible hosts, E caproni infections become chronic, whereas the worms are rapidly expelled from hosts with low compatibility. Development of Echinostoma caproni in mice This combination is characterized by a high rate of initial worm establishment and growth that is similar to other highly compatible echinostome–rodent models [10,11]. It has been shown that E. caproni can survive for at least 29 weeks postinfection (wpi) in mice [12]. In infected mice, the intestine was atrophied with fused or eroded villi, crypt hyperplasia and reduced alkaline phosphatase activity [13–15]. E. caproni evokes important humoral responses in mice. Antibodies such as immunoglobulin (Ig)M, IgG and IgA have been detected in serum and the small intestine [16,17]. It has been shown recently that www.sciencedirect.com
Vol.21 No.6 June 2005
the immune response is consistent with a Th1 cytokine pattern because antigen-specific IgG2a and elevated levels of IFN-g were observed [18]. This pattern seems to be essential for the development of E. caproni chronic infections in mice. Development of Echinostoma caproni in hamsters There is a high degree of compatibility in the E. caproni and hamster model [19]. It has been shown that hamsters retain the infection for up to 20 wpi, at least [1,2]. The intestinal tissue of hamsters is clearly affected by E. caproni infection, which manifests as erosion of villi, ballooning and bleeding of the intestinal wall [20]. Important humoral responses have been detected in hamsters experimentally infected with E. caproni [2]. Development of Echinostoma caproni in rats Rats show a low degree of compatibility with E. caproni. The rate of primary worm establishment in rats was lower than that observed in mice and hamsters, and all of the adult worms were expelled 7–10 wpi. Moreover, increased levels of peripheral blood eosinophilia were detected [21]. Only low levels of systemic antibody responses against E. caproni developed in rats [2,22]. Although relatively few studies have been performed until now, the results obtained suggest that comparative studies of the development of E. caproni in hosts with high and low compatibility could be useful for analysing the course of intestinal helminth infections. Important hostdependent differences have been detected in E. caproni egg output and in several morphometrical features in rats and hamsters, making it evident that the host species affects the progressive development of E. caproni [1]. Moreover, several immunological parameters are also dependent on the host species. Hamsters were positive for E. caproni seroantigens from 14 to 21 days postinfection until the end of the experiment [2], seemingly because adult worms secrete antigens that can cross the intestinal mucosa and reach the circulatory system in relation to a strong local inflammatory response. In contrast to hamsters, low levels of serum antigen were detected in rats [2]. The pathological effects of E. caproni in the intestines of rats remain to be studied but the differences in serum antigen levels compared with those in hamsters could reflect weaker local inflammatory responses. The differences in the local inflammatory responses are also indicated by the course of E. caproni infection in each host species. For intestinal nematodes, local inflammation mediated by IFN-g and other pro-inflammatory cytokines inhibits protective immunity, resulting in chronic infections [5–7]. It is likely that differences in local inflammatory responses mediate the establishment of chronic infections in hamsters and the earlier worm rejection in rats. Moreover, the antibody production against E. caproni infection in each host species seems to be related to the kinetics of seroantigens. The intestinal absorption of E. caproni antigens might induce systemic antibody responses by B-cell stimulation, resulting in the generation of humoral responses in hamsters [2]. All of these factors make evident the development of different
Update
TRENDS in Parasitology
Vol.21 No.6 June 2005
253
Table 1. Laboratories in which echinostome life cycles are currently maintained Laboratory Fayez Bakry Department of Environmental Research and Medical Malacology, Theodor Bilharz Research Institute, Egypt (http://www.tbri.sci.eg/about.htm) Christine Coustau Unite de Parasitologie Fonctionnelle et Evolutive, Universite de Perpignan, France (http://www.univ-perp.fr/see/rch/parasito/GB/perso/coustau.html) Armand Kuris Deptartment of Biology, University of California, USA (http://www.lifesci.ucsb.edu/eemb/faculty/kuris/) Bernard Fried Deptartment of Biology, Lafayette College, USA (http://ww2.lafayette.edu/wbiology/BFres.html) Reinalda Marisa Lanfredi Laborato´rio de Biologia de Helmintos Otto Wucherer, Universidade Federal do Rio de Janeiro, Brasil (http://www.ufrj.br/) Eric S. Loker Department of Biology, University of New Mexico, USA (http://biology.unm.edu/biology/esloker/) Arnaldo Maldonado, Jr Laborato´rio.de Medicina Tropical, Instituto Oswaldo Cruz, Brasil (http://www.ioc.fiocruz.br/) Attef Saad Department of Zoology, Cairo University, Egypt (http://www.cu.edu.eg/) Guillermo Salgado-Maldonado Instituto de Biologı´a, Universidad Nacional Autonoma de Mexico, Mexico (http://www.ibiologia.unam.mx/directorio/s/salgado_guillermo.htm) Gregory J. Sandland Department of Biological Sciences, Purdue University, USA (http://www.purdue.edu/) Allen W. Shostak Department of Biological Sciences, University of Alberta, Canada (http://www.ualberta.ca/washostak/) Woon-Mok Sohn Department of Parasitology, Gyeongsang National University, Korea (http://www.gsnu.ac.kr/) Rafael Toledo, Carla Mun˜oz-Antoli and J. Guillermo Esteban Departamento de Parasitologia, Universidad de Valencia, Spain (http://www.uv.es/wtoledo/)
responses to the same parasite species in relation to host compatibility. The course of E. caproni infection is dependent on hostand parasite-related factors. The E. caproni and rodent model offers the possibility of determining the parasiterelated factors that influence the course of infection. This could enable the establishment of host-dependent variables and their consequences to the parasite, determining the rejection of the worms in intestinal helminth infections or, by contrast, the establishment of chronic infections. Comparative studies that include histopathological, immunological, genomic and proteomic approaches to the development of E. caproni in different rodent species hold great promise in the search for the factors determining the course of intestinal helminth infections. Maintenance of echinostome life cycles The types of study mentioned require a consistent source of material for continued research of these helminths. The ideal situation would be to maintain the complete life cycle in the laboratory. The material required for completion of the life cycle can be obtained from the wild but an alternative is to request materials from laboratory workers www.sciencedirect.com
Species Echinostoma caproni
E. caproni
E. caproni
E. caproni
Echinostoma paraensei
E. paraensei
E. paraensei
Echinoparyphium recurvatum
E. recurvatum
Echinostoma revolutum
E. caproni
Echinostoma cinetorchis; Echinostoma hortense E. caproni; Echinostoma friedi; Echinostoma trivolvis; Euparyphium albuferensis; Hypoderaeum conoideum
who maintain species of interest. We have compiled a list of laboratories worldwide in which the life cycles of various echinostome species are being maintained. For this purpose, we have extensively reviewed the relevant articles published during the past 20 years, searching for laboratories that have maintained echinostome life cycles. Forty-five workers from laboratories were contacted and responses were obtained from most of them. Table 1 is a list of researchers and laboratories worldwide that are maintaining echinostome life cycles, and the species being maintained.
Future perspectives Echinostomes have served as models for experimental parasitology for many years. However, they can be exploited further, particularly with regard to the study of relationships between vertebrate hosts and adult parasites, and the host-related factors involved in the establishment of intestinal helminths. Further studies of these topics will be of great interest to those in the field of biological sciences. The use of echinostomes as experimental models could facilitate further studies to
Update
254
TRENDS in Parasitology
determine the generation of the responses that cause intestinal helminth resistance. Acknowledgements Our work was supported by project GV04B-107 de la Conselleria de Cultura, Educacio´ i Esport de la Generalitat Valenciana (Spain). We thank all of the researchers who helped us to compile the registry.
References 1 Toledo, R. et al. (2004) The comparative development of Echinostoma caproni (Trematoda: Echinostomatidae) adults in experimentally infected hamsters and rats. Parasitol. Res. 93, 439–444 2 Toledo, R. et al. (2004) Kinetics of Echinostoma caproni (Trematoda: Echinostomatidae) antigens in feces and serum of experimentally infected hamsters and rats. J. Parasitol. 90, 752–758 3 Fried, B. et al. (2004) Food-borne intestinal trematodiases in humans. Parasitol. Res. 93, 159–170 4 Gause, W.C. et al. (2003) The immune response to parasitic helminths: insights from murine models. Trends Immunol. 24, 269–277 5 Finkelman, F.D. et al. (1997) Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annu. Rev. Immunol. 15, 505–533 6 Maizels, R.M. and Yazdanbakhsh, M. (2003) Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat. Rev. Immunol. 3, 733–744 7 Maizels, R.M. and Holland, M.J. (1998) Pathways for expelling intestinal helminths. Curr. Biol. 8, R11–R14 8 Garside, P. et al. (2000) Immunopathology of intestinal helminth infections. Parasite Immunol. 22, 605–612 9 Lawrence, C.E. (2003) Is there a common mechanism of gastrointestinal nematode expulsion? Parasite Immunol. 25, 271–281 10 Odaibo, A.B. et al. (1988) Establishment, survival and fecundity in Echinostoma caproni (Trematoda) infections in NMRI mice. Proc. Helminthol. Soc. Wash. 55, 265–269 11 Odaibo, A.B. et al. (1989) Further studies on the population regulation in Echinostoma caproni infections in NMRI mice. Proc. Helminthol. Soc. Wash. 56, 192–198 12 Hosier, D.W. and Fried, B. (1991) Infectivity, growth, and distribution of Echinostoma caproni (Trematoda) in the ICR mouse. J. Parasitol. 77, 640–642
Vol.21 No.6 June 2005
13 Weinstein, M.S. and Fried, B. (1991) The expulsion of Echinostoma trivolvis and retention of Echinostoma caproni in the ICR mouse: pathological effects. Int. J. Parasitol. 21, 255–257 14 Fujino, T. and Fried, B. (1993) Echinostoma caproni and E. trivolvis alter the binding of glycoconjugates in the intestinal mucosa of C3H mice as determined by lectin histochemistry. J. Helminthol. 67, 179–188 15 Fujino, T. et al. (1996) Rapid expulsion of the intestinal trematodes Echinostoma trivolvis and E. caproni from C3H mice by trapping with increased goblet cell mucins. Int. J. Parasitol. 26, 319–324 16 Agger, M.K. et al. (1993) The antibody response in serum, intestinal wall and intestinal lumen of NMRI mice infected with Echinostoma caproni. J. Helminthol. 67, 169–178 17 Graczyk, T.K. and Fried, B. (1994) ELISA method for detecting antiEchinostoma caproni (Trematoda) antibodies in experimentally infected ICR mice. J. Parasitol. 80, 544–549 18 Brunet, L.R. et al. (2000) Immune responses during the acute stages of infection with the intestinal trematode Echinostoma caproni. Parasitology 120, 565–571 19 Christensen, N.Ø. et al. (1990) Establishment, survival and fecundity in Echinostoma caproni (Trematoda) in hamsters and jirds. J. Helminthol. Soc. Wash. 57, 104–107 20 Isaacson, A.C. et al. (1989) Infectivity, growth, development and pathology of Echinostoma caproni (Trematoda) in the golden hamster. Int. J. Parasitol. 19, 943–944 21 Hansen, K. et al. (1991) Echinostoma caproni in rats: worm population dynamics and host blood eosinophilia during primary 6, 25, and 50 metacercarial infections. Parasitol. Res. 77, 686–690 22 Toledo, R. et al. (2003) Development of an antibody-based capture enzyme-linked immunosorbent assay for detecting Echinostoma caproni (Trematoda) in experimentally infected rats: kinetics of coproantigen excretion. J. Parasitol. 89, 1227–1231 23 Toledo, R. et al. (2000) The life-cycle of Echinostoma friedi n. sp. (Trematoda: Echinostomatidae) in Spain and a discussion on the relationships within the ‘revolutum’ group based on cercarial chaetotaxy. Syst. Parasitol. 45, 199–217
1471-4922/$ - see front matter Q 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.pt.2005.04.006
Rhomboid-like proteins in Apicomplexa: phylogeny and nomenclature Timothy J. Dowse1 and Dominique Soldati1,2 1
Department of Biological Sciences, Sir Alexander Fleming Building, Imperial College London, UK, SW7 2AZ De´partement de Microbiologie et Medecine Mole´culaire, Falculte´ de Medecine, Universite´ de Gene`ve, CMU, Rue Michel-Servet 1, Geneva 1211, Switzerland 2
Rhomboids form a family of polytopic intramembrane serine proteases. In Toxoplasma gondii, an essential activity called microneme protein protease 1 (MPP1) cleaves secreted adhesive proteins within their transmembrane domains, at a site conserved in similar proteins of other Apicomplexa. Current evidence suggests that MPP1 is ubiquitous in the phylum and is encoded by a rhomboid gene. In this article, we present Corresponding author: Soldati, D. ([email protected]). Available online 27 April 2005 www.sciencedirect.com
the current repertoire of rhomboid-like proteins in Apicomplexa using a nomenclature based on phylogenetic analyses.
What are rhomboids? Rhomboids are a family of intramembrane serine proteases. The founding member of the family is Rhomboid-1 from Drosophila melanogaster, which has a role in signalling during development. The membrane-tethered
TRENDS in Parasitology
Vol.21 No.6 June 2005
Research Focus
Echinostomes as experimental models for interactions between adult parasites and vertebrate hosts Rafael Toledo1 and Bernard Fried2 1
Departamento de Parasitologı´a, Facultad de Farmacia, Universidad de Valencia, Avenida Vicente Andre´s Estelle´s, 46100 Burjassot, Valencia, Spain 2 Department of Biology, Lafayette College, Easton, PA 18042, USA
Echinostomes are intestinal trematodes that, for years, have served as experimental models in different areas of parasitology. However, the usefulness of these trematodes in experimental parasitology has been underappreciated. In this article, we examine the characteristics that make echinostomes useful models for analysis of the interactions between adult parasites and vertebrate hosts, particularly in relation to the host-related factors that determine the establishment of the parasites.
de
f
o st
(a)
Activ e in fect ion of the firs t in te
es ti o
by
eh t iv in i
Definitive host
ia ed rm
n
Seeking a perfect model The understanding of host-related factors that determine the course of intestinal helminth infections is essential for helminthologists. However, the investigation of this topic
is difficult because it requires the use of experimental models that enable comparative studies of the development of a single parasite species in different hosts. In this context, echinostomes, particularly Echinostoma caproni, can be suitable models. As shown in previous studies, the course and characteristics of E. caproni infections are dependent largely on host-related factors [1,2]. This enables the study of one species of helminth within different experimental hosts in which the course of infection differs markedly. Echinostomes are important intestinal parasitic flatworms that invade domestic animals, wildlife and humans [3]. In their larval stages, echinostomes parasitize several invertebrate and cold-blooded vertebrate hosts (Figure 1).
(c)
(b)
st ho te
Ing
Water
(d) (h) (e) Second intermediate host (g)
A c ti
ve in fe
c ti o n o f t
(f) First intermediate host
Water
t hos diate he second inter me
Figure 1. Generalized life cycle of Echinostoma spp. (a) Adult worms inhabit the small intestine of several vertebrate hosts, including humans. (b) Eggs are voided with the host faeces. (c) Miracidia hatch in fresh water and actively infect snails. (d) Sporocysts, (e) mother rediae and (f) daughter rediae are the intramolluscan stages. (g) Cercariae are released and swim to locate the second intermediate host (snails, amphibians, bivalves and fishes), in which they encyst to become metacercariae. (h) Metacercariae are ingested by the definitive host and excyst to become adults. Images adapted, with permission, from Ref. [23]. Corresponding author: Toledo, R. ([email protected]). Available online 26 April 2005 www.sciencedirect.com
252
Update
TRENDS in Parasitology
These ubiquitous parasites are easy to maintain in the laboratory as larval and adult worm stages. For this reason, echinostomes (particularly members of the genus Echinostoma) have served as experimental animal models at all levels of organization and have contributed to studies in different areas of parasitology. However, the usefulness of these trematodes in experimental parasitology has often been underappreciated. Further use of echinostomes as experimental models might be helpful for identifying the host-related factors responsible for either worm rejection or worm maintenance in intestinal helminth infections. The need for new experimental models The factors that determine the course of intestinal helminth infection have been studied extensively using intestinal nematode parasites. Several nematode and rodent species (mainly mice) have been used as experimental models [4,5]. However, the results obtained have not been definitive and it has been observed that the course of infection depends on several factors related to both the host and the parasite species [6]. It is generally accepted that worm rejection is related to T helper (Th)2 responses mediated by the production of interleukin (IL)-4. By contrast, chronicity seems to be associated with Th1 responses mediated by IL-12, tumor necrosis factor (TNF)-a and interferon (IFN)-g [5–9]. However, the mechanisms involved in these responses and the host- and parasite-dependent factors are difficult to study [6,9]. One factor preventing further conclusions is the absence of adequate experimental models. To date, the models used present several problems: (i) some of the nematode species used develop only in one species of experimental host, thereby preventing comparative studies; (ii) other nematode species present tissue phases or inhabit the caecum, making it difficult to interpret the experimental results. Hence, there is a need to develop new experimental models [9]. In this context, echinostomes, particularly E. caproni, could be extremely useful. Echinostomes and interactions between adult parasites and vertebrate hosts E. caproni has a wide range of definitive hosts, although its compatibility differs considerably among rodent species on the basis of worm survival in each host species. In highly compatible hosts, E caproni infections become chronic, whereas the worms are rapidly expelled from hosts with low compatibility. Development of Echinostoma caproni in mice This combination is characterized by a high rate of initial worm establishment and growth that is similar to other highly compatible echinostome–rodent models [10,11]. It has been shown that E. caproni can survive for at least 29 weeks postinfection (wpi) in mice [12]. In infected mice, the intestine was atrophied with fused or eroded villi, crypt hyperplasia and reduced alkaline phosphatase activity [13–15]. E. caproni evokes important humoral responses in mice. Antibodies such as immunoglobulin (Ig)M, IgG and IgA have been detected in serum and the small intestine [16,17]. It has been shown recently that www.sciencedirect.com
Vol.21 No.6 June 2005
the immune response is consistent with a Th1 cytokine pattern because antigen-specific IgG2a and elevated levels of IFN-g were observed [18]. This pattern seems to be essential for the development of E. caproni chronic infections in mice. Development of Echinostoma caproni in hamsters There is a high degree of compatibility in the E. caproni and hamster model [19]. It has been shown that hamsters retain the infection for up to 20 wpi, at least [1,2]. The intestinal tissue of hamsters is clearly affected by E. caproni infection, which manifests as erosion of villi, ballooning and bleeding of the intestinal wall [20]. Important humoral responses have been detected in hamsters experimentally infected with E. caproni [2]. Development of Echinostoma caproni in rats Rats show a low degree of compatibility with E. caproni. The rate of primary worm establishment in rats was lower than that observed in mice and hamsters, and all of the adult worms were expelled 7–10 wpi. Moreover, increased levels of peripheral blood eosinophilia were detected [21]. Only low levels of systemic antibody responses against E. caproni developed in rats [2,22]. Although relatively few studies have been performed until now, the results obtained suggest that comparative studies of the development of E. caproni in hosts with high and low compatibility could be useful for analysing the course of intestinal helminth infections. Important hostdependent differences have been detected in E. caproni egg output and in several morphometrical features in rats and hamsters, making it evident that the host species affects the progressive development of E. caproni [1]. Moreover, several immunological parameters are also dependent on the host species. Hamsters were positive for E. caproni seroantigens from 14 to 21 days postinfection until the end of the experiment [2], seemingly because adult worms secrete antigens that can cross the intestinal mucosa and reach the circulatory system in relation to a strong local inflammatory response. In contrast to hamsters, low levels of serum antigen were detected in rats [2]. The pathological effects of E. caproni in the intestines of rats remain to be studied but the differences in serum antigen levels compared with those in hamsters could reflect weaker local inflammatory responses. The differences in the local inflammatory responses are also indicated by the course of E. caproni infection in each host species. For intestinal nematodes, local inflammation mediated by IFN-g and other pro-inflammatory cytokines inhibits protective immunity, resulting in chronic infections [5–7]. It is likely that differences in local inflammatory responses mediate the establishment of chronic infections in hamsters and the earlier worm rejection in rats. Moreover, the antibody production against E. caproni infection in each host species seems to be related to the kinetics of seroantigens. The intestinal absorption of E. caproni antigens might induce systemic antibody responses by B-cell stimulation, resulting in the generation of humoral responses in hamsters [2]. All of these factors make evident the development of different
Update
TRENDS in Parasitology
Vol.21 No.6 June 2005
253
Table 1. Laboratories in which echinostome life cycles are currently maintained Laboratory Fayez Bakry Department of Environmental Research and Medical Malacology, Theodor Bilharz Research Institute, Egypt (http://www.tbri.sci.eg/about.htm) Christine Coustau Unite de Parasitologie Fonctionnelle et Evolutive, Universite de Perpignan, France (http://www.univ-perp.fr/see/rch/parasito/GB/perso/coustau.html) Armand Kuris Deptartment of Biology, University of California, USA (http://www.lifesci.ucsb.edu/eemb/faculty/kuris/) Bernard Fried Deptartment of Biology, Lafayette College, USA (http://ww2.lafayette.edu/wbiology/BFres.html) Reinalda Marisa Lanfredi Laborato´rio de Biologia de Helmintos Otto Wucherer, Universidade Federal do Rio de Janeiro, Brasil (http://www.ufrj.br/) Eric S. Loker Department of Biology, University of New Mexico, USA (http://biology.unm.edu/biology/esloker/) Arnaldo Maldonado, Jr Laborato´rio.de Medicina Tropical, Instituto Oswaldo Cruz, Brasil (http://www.ioc.fiocruz.br/) Attef Saad Department of Zoology, Cairo University, Egypt (http://www.cu.edu.eg/) Guillermo Salgado-Maldonado Instituto de Biologı´a, Universidad Nacional Autonoma de Mexico, Mexico (http://www.ibiologia.unam.mx/directorio/s/salgado_guillermo.htm) Gregory J. Sandland Department of Biological Sciences, Purdue University, USA (http://www.purdue.edu/) Allen W. Shostak Department of Biological Sciences, University of Alberta, Canada (http://www.ualberta.ca/washostak/) Woon-Mok Sohn Department of Parasitology, Gyeongsang National University, Korea (http://www.gsnu.ac.kr/) Rafael Toledo, Carla Mun˜oz-Antoli and J. Guillermo Esteban Departamento de Parasitologia, Universidad de Valencia, Spain (http://www.uv.es/wtoledo/)
responses to the same parasite species in relation to host compatibility. The course of E. caproni infection is dependent on hostand parasite-related factors. The E. caproni and rodent model offers the possibility of determining the parasiterelated factors that influence the course of infection. This could enable the establishment of host-dependent variables and their consequences to the parasite, determining the rejection of the worms in intestinal helminth infections or, by contrast, the establishment of chronic infections. Comparative studies that include histopathological, immunological, genomic and proteomic approaches to the development of E. caproni in different rodent species hold great promise in the search for the factors determining the course of intestinal helminth infections. Maintenance of echinostome life cycles The types of study mentioned require a consistent source of material for continued research of these helminths. The ideal situation would be to maintain the complete life cycle in the laboratory. The material required for completion of the life cycle can be obtained from the wild but an alternative is to request materials from laboratory workers www.sciencedirect.com
Species Echinostoma caproni
E. caproni
E. caproni
E. caproni
Echinostoma paraensei
E. paraensei
E. paraensei
Echinoparyphium recurvatum
E. recurvatum
Echinostoma revolutum
E. caproni
Echinostoma cinetorchis; Echinostoma hortense E. caproni; Echinostoma friedi; Echinostoma trivolvis; Euparyphium albuferensis; Hypoderaeum conoideum
who maintain species of interest. We have compiled a list of laboratories worldwide in which the life cycles of various echinostome species are being maintained. For this purpose, we have extensively reviewed the relevant articles published during the past 20 years, searching for laboratories that have maintained echinostome life cycles. Forty-five workers from laboratories were contacted and responses were obtained from most of them. Table 1 is a list of researchers and laboratories worldwide that are maintaining echinostome life cycles, and the species being maintained.
Future perspectives Echinostomes have served as models for experimental parasitology for many years. However, they can be exploited further, particularly with regard to the study of relationships between vertebrate hosts and adult parasites, and the host-related factors involved in the establishment of intestinal helminths. Further studies of these topics will be of great interest to those in the field of biological sciences. The use of echinostomes as experimental models could facilitate further studies to
Update
254
TRENDS in Parasitology
determine the generation of the responses that cause intestinal helminth resistance. Acknowledgements Our work was supported by project GV04B-107 de la Conselleria de Cultura, Educacio´ i Esport de la Generalitat Valenciana (Spain). We thank all of the researchers who helped us to compile the registry.
References 1 Toledo, R. et al. (2004) The comparative development of Echinostoma caproni (Trematoda: Echinostomatidae) adults in experimentally infected hamsters and rats. Parasitol. Res. 93, 439–444 2 Toledo, R. et al. (2004) Kinetics of Echinostoma caproni (Trematoda: Echinostomatidae) antigens in feces and serum of experimentally infected hamsters and rats. J. Parasitol. 90, 752–758 3 Fried, B. et al. (2004) Food-borne intestinal trematodiases in humans. Parasitol. Res. 93, 159–170 4 Gause, W.C. et al. (2003) The immune response to parasitic helminths: insights from murine models. Trends Immunol. 24, 269–277 5 Finkelman, F.D. et al. (1997) Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annu. Rev. Immunol. 15, 505–533 6 Maizels, R.M. and Yazdanbakhsh, M. (2003) Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat. Rev. Immunol. 3, 733–744 7 Maizels, R.M. and Holland, M.J. (1998) Pathways for expelling intestinal helminths. Curr. Biol. 8, R11–R14 8 Garside, P. et al. (2000) Immunopathology of intestinal helminth infections. Parasite Immunol. 22, 605–612 9 Lawrence, C.E. (2003) Is there a common mechanism of gastrointestinal nematode expulsion? Parasite Immunol. 25, 271–281 10 Odaibo, A.B. et al. (1988) Establishment, survival and fecundity in Echinostoma caproni (Trematoda) infections in NMRI mice. Proc. Helminthol. Soc. Wash. 55, 265–269 11 Odaibo, A.B. et al. (1989) Further studies on the population regulation in Echinostoma caproni infections in NMRI mice. Proc. Helminthol. Soc. Wash. 56, 192–198 12 Hosier, D.W. and Fried, B. (1991) Infectivity, growth, and distribution of Echinostoma caproni (Trematoda) in the ICR mouse. J. Parasitol. 77, 640–642
Vol.21 No.6 June 2005
13 Weinstein, M.S. and Fried, B. (1991) The expulsion of Echinostoma trivolvis and retention of Echinostoma caproni in the ICR mouse: pathological effects. Int. J. Parasitol. 21, 255–257 14 Fujino, T. and Fried, B. (1993) Echinostoma caproni and E. trivolvis alter the binding of glycoconjugates in the intestinal mucosa of C3H mice as determined by lectin histochemistry. J. Helminthol. 67, 179–188 15 Fujino, T. et al. (1996) Rapid expulsion of the intestinal trematodes Echinostoma trivolvis and E. caproni from C3H mice by trapping with increased goblet cell mucins. Int. J. Parasitol. 26, 319–324 16 Agger, M.K. et al. (1993) The antibody response in serum, intestinal wall and intestinal lumen of NMRI mice infected with Echinostoma caproni. J. Helminthol. 67, 169–178 17 Graczyk, T.K. and Fried, B. (1994) ELISA method for detecting antiEchinostoma caproni (Trematoda) antibodies in experimentally infected ICR mice. J. Parasitol. 80, 544–549 18 Brunet, L.R. et al. (2000) Immune responses during the acute stages of infection with the intestinal trematode Echinostoma caproni. Parasitology 120, 565–571 19 Christensen, N.Ø. et al. (1990) Establishment, survival and fecundity in Echinostoma caproni (Trematoda) in hamsters and jirds. J. Helminthol. Soc. Wash. 57, 104–107 20 Isaacson, A.C. et al. (1989) Infectivity, growth, development and pathology of Echinostoma caproni (Trematoda) in the golden hamster. Int. J. Parasitol. 19, 943–944 21 Hansen, K. et al. (1991) Echinostoma caproni in rats: worm population dynamics and host blood eosinophilia during primary 6, 25, and 50 metacercarial infections. Parasitol. Res. 77, 686–690 22 Toledo, R. et al. (2003) Development of an antibody-based capture enzyme-linked immunosorbent assay for detecting Echinostoma caproni (Trematoda) in experimentally infected rats: kinetics of coproantigen excretion. J. Parasitol. 89, 1227–1231 23 Toledo, R. et al. (2000) The life-cycle of Echinostoma friedi n. sp. (Trematoda: Echinostomatidae) in Spain and a discussion on the relationships within the ‘revolutum’ group based on cercarial chaetotaxy. Syst. Parasitol. 45, 199–217
1471-4922/$ - see front matter Q 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.pt.2005.04.006
Rhomboid-like proteins in Apicomplexa: phylogeny and nomenclature Timothy J. Dowse1 and Dominique Soldati1,2 1
Department of Biological Sciences, Sir Alexander Fleming Building, Imperial College London, UK, SW7 2AZ De´partement de Microbiologie et Medecine Mole´culaire, Falculte´ de Medecine, Universite´ de Gene`ve, CMU, Rue Michel-Servet 1, Geneva 1211, Switzerland 2
Rhomboids form a family of polytopic intramembrane serine proteases. In Toxoplasma gondii, an essential activity called microneme protein protease 1 (MPP1) cleaves secreted adhesive proteins within their transmembrane domains, at a site conserved in similar proteins of other Apicomplexa. Current evidence suggests that MPP1 is ubiquitous in the phylum and is encoded by a rhomboid gene. In this article, we present Corresponding author: Soldati, D. ([email protected]). Available online 27 April 2005 www.sciencedirect.com
the current repertoire of rhomboid-like proteins in Apicomplexa using a nomenclature based on phylogenetic analyses.
What are rhomboids? Rhomboids are a family of intramembrane serine proteases. The founding member of the family is Rhomboid-1 from Drosophila melanogaster, which has a role in signalling during development. The membrane-tethered