Anais da Academia Brasileira de Ciências ISSN: 0001-3765 [email protected] Academia Brasileira de Ciências Brasil Azambuja, Patrícia; A. Ratcliffe, Norman; S. Garcia, Eloi Towards an understanding of the interactions of Trypanosoma cruzi and Trypanosoma rangeli within the reduviid insect host Rhodnius prolixus Anais da Academia Brasileira de Ciências, vol. 77, núm. 3, set., 2005, pp. 397-404 Academia Brasileira de Ciências Rio de Janeiro, Brasil Available in: http://www.redalyc.org/articulo.oa?id=32777304 How to cite Complete issue Scientific Information System More information about this article Network of Scientific Journals from Latin America, the Caribbean, Spain and Portugal Journal's homepage in redalyc.org Non-profit academic project, developed under the open access initiative Anais da Academia Brasileira de Ciências (2005) 77(3): 397-404 (Annals of the Brazilian Academy of Sciences) ISSN 0001-3765 www.scielo.br/aabc Towards an understanding of the interactions of Trypanosoma cruzi and Trypanosoma rangeli within the reduviid insect host Rhodnius prolixus PATRÍCIA AZAMBUJA1, NORMAN A. RATCLIFFE2 and ELOI S. GARCIA1 1Department of Biochemistry and Molecular Biology, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz Av. Brasil 4365, 21045-900 Rio de Janeiro, RJ, Brasil 2Biomedical and Physiologial Research Group, School of Biological Sciences, University of Wales Swansea, Singleton Park, Swansea, SA28PP, United Kingdom Manuscript received on March 3, 2005; accepted for publication on March 30, 2005; contributed by Eloi S. Garcia* ABSTRACT This review outlines aspects on the developmental stages of Trypanosoma cruzi and Trypanosoma rangeli in the invertebrate host, Rhodnius prolixus. Special attention is given to the interactions of these parasites with gut and hemolymph molecules and the effects of the organization of midgut epithelial cells on the parasite development. The vector insect’s permissiveness to T. cruzi, which develops in the vector gut, largely depends on the host nutritional state, the parasite strain and the molecular interactions with trypanolytic compounds, lectins and resident bacteria in the gut. T. rangeli invades the hemocoel and once in the hemolymph, can be recognized and activates the defense system of its insect vector, i.e., the prophenoloxidase system, phago- cytosis, hemocyte microaggregation, superoxide and nitric oxide activity and the eicosanoid biosynthesis pathway. Taken together, these findings not only provide a better understanding of the interactions para- site - insect vector, but also offer new insights into basic physiological processes involved in the parasites transmission. Key words: Trypanosomes, Rhodnius prolixus, vector, parasites. INTRODUCTION the Trypanosoma cruzi and T. rangeli- triatomine vector interactions results from their complexity and The co-evolution of parasites and insects has pro- modes of parasite transmission (Garcia and Azam- moted the development of a powerful and sophisti- buja 1991, Kollien and Schaub 2000). Like T. cruzi, cated strategy based on both physiological and bio- T. rangeli infects humans and a wide range of other chemical vector and/or parasite mechanisms, which mammals and has a similar geographic distribution act to facilitate parasite development or its disrup- (Guhl and Vallejo 1998). tion in the invertebrate host. The debate concerning Many factors are believed to contribute to the establishment of trypanosomes in the gut of the in- Dedicated to the memory of Prof. Dr. Herman Lent by initiative of Pedro L. Oliveira, Instituto de Bioquímica Médica. vertebrate host. However, differences in the biolog- Universidade Federal do Rio de Janeiro (UFRJ), RJ, Brasil. ical cycles between both parasites exist: T. rangeli, *Member Academia Brasileira de Ciências but not T. cruzi, invades the hemocoel and physico- Correspondence to: Dr. Patrícia Azambuja E-mail: azambuja@ioc.fiocruz.br chemical barriers such as the gut membranes, which An Acad Bras Cienc (2005) 77 (3) 398 PATRÍCIA AZAMBUJA, NORMAN A. RATCLIFFE and ELOI S. GARCIA are important to T. cruzi development, but not to T. see Garcia and Azambuja 1997), and analyzed a va- rangeli in the digestive tract (Gonzalez et al. 1999, riety of factors, such as the clone used and feeding Azambuja and Garcia, personal observation). with azadirachtin, influencing the life cycle of T. This review outlines research on the develop- cruzi in the gut of the vector, R. prolixus (Garcia mental aspects of Trypanosoma cruzi and Trypano- and Azambuja 1991). soma rangeli in the insect vector, which may reveal Results showed that feeding R. prolixus with new perspectives for the control of Chagas disease. the inhibitor of acid SH-proteinase, pepstatin, had no effect on rates of T. cruzi infection (Garcia and Gilliam 1980). Also, trypomastigotes from single- TRYPANOSOMA CRUZI AND VECTOR INTERACTIONS cell-isolates of two clones of T. cruzi produced dif- Before considering more details of the vector – par- ferent rates of growth because of different popula- asite interactions, it is important to understand some tion doubling times of the parasites and only one aspects of the parasite life cycle in the invertebrate clone underwent epimastigote to metacyclic trypo- host. Points of contact between T. cruzi, the eti- mastigote transformation (Garcia and Dvorak 1982). ologic agent of Chagas disease, and its triatomine Results therefore indicate that not only the kinetics vectors begin with ingestion of the infective blood of T. cruzi epimastigote multiplication but also the meal. Blood feeding is essential for the parasite transformation to metacyclic trypomastigotes de- growth in all instars and in the adult insect (Kollien pend on the strains and clones of the infecting para- and Schaub 1998). Interactions between T. cruzi and site (Garcia et al. 1984b). In addition, the passage of its vector insects begin with the arrival of an infected homogeneous strains of T. cruzi through the inverte- blood meal in the insect gut. During feeding, the try- brate host gut was identical with the host was unable pomastigotes forms from the blood of the infected to modify any biological, biochemical or genetic vertebrate host are ingested by the insect (Garcia and characteristics of the parasite (Garcia et al. 1986b). Azambuja 1991, Kollien and Schaub 2000). After a Although many factors are thought to be impor- few days in the stomach (anterior part of the midgut) tant to the establishment of T. cruzi infection in the of the insect most of the bloodstream trypomastig- gut of the vector, only a few molecules have been otes transform into epimastigotes and some sphero- implicated, such as a stomach lytic factor (Azam- mastigotes (Garcia andAzambuja 1991, Kollien and buja et al. 1983, 1989), lectins (Pereira et al. 1981, Schaub 2000). Subsequently, mainly in the intestine Mello et al. 1996) and hemoglobin fragments (Gar- (posterior part of the midgut), the epimastigotes di- cia et al. 1995), all of which have been tested di- vide repeatedly by binary division and can attach to rectly against the parasite. The work of Pereira et the perimicrovillar membranes in the intestinal cells al. (1981) reported lectins in the digestive tube (Gonzalez et al. 1999). At later stages in the rectum, and hemolymph of R. prolixus and suggested that a proportion of the epimastigotes attach to the rectal these molecules could be involved in the develop- cuticle and transform into metacyclic trypomastig- ment of T. cruzi in the triatomine bug. Mello et al. otes that are eliminated with the feces and urine and (1996) demonstrated differences in the development are able to infect the vertebrate host (Garcia and of three strains of T. cruzi in the gut of R. prolixus Azambuja 1991, Kollien and Schaub 2000). and related the infectivity of these to the ability of Since the gut of triatomines is the first environ- the digestive tube extract to agglutinate these para- ment for the establishment of T. cruzi infection, we sitesin vitro. Interestingly, lectins agglutinated the studied the possible influence of digestive enzymes Dm28c clone of T. cruzi which achieved high infec- on parasite development (Garcia 1987), developed tivity levels while, in contrast, the Y strain of the suitable bioassays for specific aspects of triatomine parasite which was not agglutinated, was lysed and physiology and biochemistry in the gut (for review failed to develop in the vector gut (Azambuja et al. An Acad Bras Cienc (2005) 77 (3) UNDERSTANDING TRYPANOSOME – RHODNIUS INTERACTIONS 399 1989, Mello et al. 1996, 1999). cytes and T. cruzi demonstrated that: (i) at 0◦Cor Frainderaich et al. (1993) demonstrated that 30◦C, both SM365 and RPH reduced the popula- metacyclogenesis of T. cruzi is promoted in vitro by tions of Y strain, but not of the DM28c clone, and an αD-globin-derived peptide present in hemoglobin DB11 was unable to lyse either T. cruzi strain; and corresponding to residue 1-40 from the amino ter- (ii) all three strains of S. marcescens were able to minus found in the gut of Triatoma infestans. Syn- lyse erythrocytes (Azambuja et al. 2004). These thetic peptides having the amino terminal globin se- results suggest that S. marcescens trypanolytic ac- quences and containing conserved domains span- tivity from the SM365 and RPH strains is distinct ning amino acid residues 30 to 40 are recognized from the hemolytic activity and that prodigiosin is by a surface receptor in epimastigote cells and stim- an important factor for the trypanolytic action of the ulate T. cruzi adenylyl cyclase (Frainderaich