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Penetration of the salivary glands of Rhodnius domesticus Neiva & Pinto, 1923 (Hemiptera: Reduviidae) by Trypanosoma rangeli Tejera, 1920 (Protozoa: Kinetoplastida)

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Abstract

Penetration of the heteroxenous protozoan Trypanosoma rangeli into the salivary glands of its invertebrate host Rhodnius domesticus has been investigated here using different approaches. Electron microscopy showed that epimastigotes coming from the insect hemocoel cross the basal lamina that surrounds the salivary glands and penetrate through the gland cells cytoplasm. After reaching the gland lumen, epimastigote forms remain adhered to the gland cell microvilli by their flagella, while metacyclic trypomastigotes are found swimming free in the saliva. Analysis by flow cytometry, western blotting and hemolytic activity allowed to demonstrate the presence in T. rangeli of a hemolytic molecule with antigenic cross-reactivity with murine perforin, which could be used by the parasites to reach the salivary gland lumen. This molecule, which we named as rangelysin, has 120 kDa molecular weight, is able to induce hemolysis only in acidic pH, and is produced by both trypomastigote and epimastigote forms.

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References

  • Añez N (1984) Studies on Trypanosoma rangeli Tejera, 1920. VII—its effect on the survival of infected triatomine bugs. Mem Inst Oswaldo Cruz 79:249–255

    PubMed  Google Scholar 

  • Acosta L, Romanha AJ, Cosenza H, Krettli AU (1991) Trypanosomatid isolates from Honduras: differentiation between Trypanosoma cruzi and Trypanosoma rangeli. Am J Trop Med Hyg 44:676–683

    CAS  PubMed  Google Scholar 

  • Andrews NW (1990) The acid-active hemolysin of Trypanosoma cruzi. Exp Parasitol 71:241–244

    Article  CAS  PubMed  Google Scholar 

  • Andrews NW, Portnoy DA (1994) Cytolysins from intracellular pathogens. Trends Microbiol 2:261–263

    Article  CAS  PubMed  Google Scholar 

  • Andrews NW, Abrams CK, Slatin SL, Grifiths G (1990) A T. cruzi-secreted protein immunologically related to the complement component C9: evidence for membrane pore-forming activity at low pH. Cell 61:1277–1287

    Article  CAS  PubMed  Google Scholar 

  • Basseri HR, Tew IF, Ratcliffe NA (2002) Identification and distribution of carbohydrate moieties on the salivary glands of Rhodnius prolixus and their possible involvement in attachment/invasion by Trypanosoma rangeli. Exp Parasitol 100:226–234

    Article  CAS  PubMed  Google Scholar 

  • Bhakdi S, Tranun-Jensen J (1988) Damage to cell membranes by pore-forming bacterial cytolysins. Prog Allergy 40:1–43

    CAS  Google Scholar 

  • Bielecki J, Youngman PC, Portnoy DA (1990) Bacillus subtilis expressing a haemolysin gene from Listeria monocytogenes can grow in mammalian cells. Nature 345:175–176

    Article  CAS  PubMed  Google Scholar 

  • Carruthers VB (1999) Armed and dangerous: Toxoplasma gondii uses an arsenal of secretory proteins to infect host cells. Parasitol Internat 48:1–10

    Article  CAS  Google Scholar 

  • Cuba-Cuba CA (1998) Review of biological and diagnostic aspects of Trypanosoma (Herpetosoma) rangeli. Rev Soc Brasil Med Trop 31:207–220

    CAS  Google Scholar 

  • D’Alessandro A (1976) The biology of Trypanosoma (Herpetosoma) rangeli. In: Lumsden WHR, Evans DA (eds) Biology of kinetoplastida, vol 1. Academic Press, London, pp 328–403

  • D’Alessandro A, Saravia NG (1992) Trypanosoma rangeli. In: Kreier J, Baker JR (eds) Parasitic protozoa, vol. 2. Academic Press, New York, pp 1–45

  • D’Alessandro A, Saravia NG (1999) Trypanosoma rangeli. In: Gilles HM (ed) Protozoal diseases. Arnold, London

    Google Scholar 

  • Desai SA, Rosenberg RL (1997) Pore size of the malaria parasite’s nutrient channel. Proc Natl Acad Aci USA 94:2045–2049

    Article  CAS  Google Scholar 

  • Ellis DS, Evans DA, Stanford S (1980) The penetration of the salivary glands of Rhodnius prolixus by Trypanosoma rangeli. Z Parasitenk 62:63–73

    Article  CAS  PubMed  Google Scholar 

  • Fiori PL, Rappelli P, Addis MF, Sechi A, Cappuccinelli P (1996) Trichomonas vaginalis haemolysis: pH regulates a contact-independent mechanism based on pore-forming proteins. Microb Pathog 20:109–118

    Article  CAS  PubMed  Google Scholar 

  • Forbes MS, Plantholt BA, Sperelakis N (1977) Cytochemical staining procedures selective for sarcotubular systems of muscle: modifications and applications. J Ultrastruct Res 60:306–327

    Article  CAS  PubMed  Google Scholar 

  • Garnham PCC (1980) The significance of inapparent infections in Chagas’ disease and other forms of trypanosomiasis. Mem Inst Oswaldo Cruz 75:181–188

    Google Scholar 

  • Grewal MS (1957) Pathogenicity of Trypanosoma rangeli Tejera, 1920 in the invertebrate host. Exp Parasitol 6:123–130

    Article  CAS  PubMed  Google Scholar 

  • Grisard EC (2002) Salivaria or stercoraria? The Trypanosoma rangeli dilemma. Kinetoplastid Biol Dis 1:5

    Article  PubMed  Google Scholar 

  • Grisard EC, Steindel M, Guarneri AA, Eger-Mangrich L, Campbell DA, Romanha AJ (1999) Characterization of Trypanosoma rangeli strains isolated in Central and South America: an overview. Mem Inst Oswaldo Cruz 94:203–209

    Article  CAS  Google Scholar 

  • Guhl F, Vallejo GA (2003) Trypanosoma (Herpetosoma) rangeli Tejera, 1920—an updated review. Mem Inst Oswaldo Cruz 98:435–442

    Article  PubMed  Google Scholar 

  • Guhl F, Jaramillo C, Carranza JC, Vallejo GA (2002) Molecular characterization and diagnosis of Trypanosoma cruzi and T. rangeli. Arch Med Res 33:362–370

    Article  CAS  PubMed  Google Scholar 

  • Hecker H, Schwarzenbach M, Rudin W (1990) Development and interaction of Trypanosoma rangeli in and with reduviid bug Rhodnius prolixus. Parasitol Res 76:311–318

    Article  CAS  PubMed  Google Scholar 

  • Hoare CA (1972) The trypanosomes of mammals. Blackwell Scientific, Oxford-Edinburgh, pp 288–314

    Google Scholar 

  • Horstmann RD, Leippe M, Tannich E (1992) Host tissue destruction by Entamoeba histolytica: molecules mediating adhesion, cytolysis and proteolysis. Mem Inst Oswaldo Cruz 87:57–60

    Google Scholar 

  • Horta MF (1997) Pore forming proteins in pathogenic protozoan parasites. Trends Microbiol 5:363–366

    Article  CAS  PubMed  Google Scholar 

  • Jiang SB, Ojcius DM, Young JD (1990) Perforin binding to cells and lipid membranes determined by a simple competition assay. J Immunol Meth 126:29–37

    Article  CAS  Google Scholar 

  • Koerich LB, Emmanuelle-Machado P, Santos K, Grisard EC, Steindel M (2002) Differentiation of Trypanosoma rangeli: high production of infective trypomastigote forms in vitro. Parasitol Res 88:21–25

    PubMed  Google Scholar 

  • Laemmli VK (1970) Most commonly used discontinuous buffer system for SDS electrophoresis. Nature 227:680

    CAS  PubMed  Google Scholar 

  • Ley V, Robbins ES, Nussenzweig V, Andrews NW (1990) The exit of Trypanosoma cruzi from the phagosome is inhibited by raising the pH of acidic compartments. J Exp Med 171:401–413

    Article  CAS  PubMed  Google Scholar 

  • Liu C-C, Walsh CM, Young JD-E (1995) Perforin: structure and function. Immunol Today 16:194–201

    Article  PubMed  Google Scholar 

  • Ludwig A (1996) Cytolytic toxins from gram-negative bacteria. Microbiologia 12:281–296

    CAS  PubMed  Google Scholar 

  • Lynch EC, Rosenberg IM, Gitler C (1982) An ion-channel forming protein produced by Entamoeba histolytica. EMBO J 1:801–804

    CAS  PubMed  Google Scholar 

  • Molyneux DH, Wallbanks KR, Ingram GA (1987) Trypanosomatids-vector interfaces—in vitro studies on parasite substrate interactions. In: Chang KP, Snary D (eds) Host-parasite cellular and molecular interactions in protozoal infections, vol H11, Springer, Berlin Heidelberg New York

  • Nickel R, Ott C, Dandeka T, Leippe M (1999) Pore-forming peptides of Entamoeba dispar—similarity and divergence to amoebapores in structure, expression and activity. Eur J Biochem 265:1002–1007

    Article  CAS  PubMed  Google Scholar 

  • Noronha FSM, Ramalho-Pinto FJ, Horta MF (1994) Identification of a putative pore-forming hemolysin active at acid pH in Leishmania amazonensis. Braz J Med Biol Res 27:477–482

    CAS  PubMed  Google Scholar 

  • Noronha FSM, Ramalho-Pinto FJ, Horta MF (1996) Cytolitic activity in the genus Leishmania: involvement of a putative pore-forming protein. Infect Immun 64:3975–3982

    CAS  PubMed  Google Scholar 

  • Oliveira MA, De Souza W (2001) An electron microscopic study of penetration by Trypansoma rangeli into midgut cells of Rhodnius prolixus. J Invert Pathol 77:22–26

    Article  Google Scholar 

  • Osorio Y, Travi BL, Palma GI, Saravia NG (1995) Infectivity of Trypanosoma rangeli in a promonocytic mammalian cell line. J Parasitol 96:449–460

    Google Scholar 

  • Schaub GA, Wunderlich F (1985) Die chagas krankheit. Biol Med Bull 41:187–194

    Google Scholar 

  • Shahabuddin M, Pimenta PFP (1998) Plasmodium parasites selectively invade vesicular ATPase-expressing cells in mosquito midgut. Proc Natl Acad Sci USA 95:3385–3389

    Article  CAS  PubMed  Google Scholar 

  • Steindel M, Carvalho-Pinto C, Toma HK, Mangia RH, Ribeiro-Rodrigues R, Romanha A (1991) Trypanosoma rangeli (Tejera 1920) isolated from a sylvatic rodent (Echmys dasythrix) in Santa Catarina Island, Santa Catarina State: first report of this trypanosome in Southern Brazil. Mem Inst Oswaldo Cruz 86:73–79

    CAS  PubMed  Google Scholar 

  • Suss-Toby E, Zimmerberg J, Ward GE (1996) Toxoplasma invasion: the parasithophorous vacuole is formed from host cell plasma membrane and pinches off via a fission pore. Proc Natl Acad Sci USA 93:8413–8418

    Article  CAS  PubMed  Google Scholar 

  • Tejera E (1920) Un noveau flagellé de Rhodnius prolixus, Trypanosoma (ou Crihtidia) rangeli n. sp. Bull Soc Pathol Exot 13:527–530

    Google Scholar 

  • Tieszen KL, Molyneux DH, Abdel-Hafez K (1986) Host–parasite relationships of Blastocrithidia familiaris in Ligaeus pandurus Scop. (Hemiptera-Lygaeidae). Parasitology 92:1–12

    Google Scholar 

  • Tieszen KL, Molyneux DH, Abdel-Hafez K (1989) Host-parasite relationships and cysts of Leptomonas lygaei (Trypanosomatidae) in Lygaeus pandurus (Hemiptera: Lygaeidae). Parasitology 98:395–400

    Google Scholar 

  • Tobie EJ (1965) Biological factors influencing transmission of Trypanosoma rangeli by Rhodnius prolixus. J Parasitol 51:837–841

    CAS  PubMed  Google Scholar 

  • Tweten RK (1995) In: Roth JA et al. (eds) Virulence mechanisms of bacterial pathogens. ASM Press, pp 207–229

  • Watkins R (1971) Histology of Rhodnius prolixus infected with Trypanosoma rangeli. J Invert Pathol 117:59–66

    Article  Google Scholar 

  • Young JDE, Young TM, LU LP, Unkelles JC, Cohn ZA (1982) Characterization of a membrane pore-forming protein from Entamoeba histolytica. J Exp Med 156:1677–1690

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank Dr. Pedro M. Persechini (Institute of Biophysics, UFRJ, Rio de Janeiro, Brazil) for kindly supplying the anti-perforin antibody and Mr. José Lopes de Faria for the photographic work. This work was supported by CNPq, FAPERJ, PAPES-III/FIOCRUZ and FIOCRUZ. All experiments were performed according to the Brazilian laws.

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Correspondence to Maurilio J. Soares.

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Meirelles, R.M.S., Henriques-Pons, A., Soares, M.J. et al. Penetration of the salivary glands of Rhodnius domesticus Neiva & Pinto, 1923 (Hemiptera: Reduviidae) by Trypanosoma rangeli Tejera, 1920 (Protozoa: Kinetoplastida). Parasitol Res 97, 259–269 (2005). https://doi.org/10.1007/s00436-005-1433-4

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