Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-10T10:51:06.811Z Has data issue: false hasContentIssue false
  • English
  • Français

The role of sex steroids in the complex physiology of the host-parasite relationship: the case of the larval cestode of Taenia crassiceps

Published online by Cambridge University Press:  23 May 2005

J. MORALES-MONTOR  and
C. LARRALDE
J. MORALES-MONTOR
Affiliation:
Departamento de Inmunología, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, AP 70228, México D.F. 04510
C. LARRALDE
Affiliation:
Departamento de Inmunología, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, AP 70228, México D.F. 04510
Get access Rights & Permissions [Opens in a new window]

Abstract

Sex steroids play a significant role in regulating the parasite load in experimental intraperitoneal Taenia crassiceps cysticercosis of male and female Balbc/anN mice. Briefly, oestrogens increase parasite loads and androgens decrease them (1) by acting directly on the parasite, favouring or hindering its reproduction, respectively, and (2) by biasing the hosts' immune response towards a parasite-permissive Th2 or a parasite-restrictive Th1 response. The infected male host also undergoes drastic endocrinological and behavioural changes that may impinge upon the course of infection, and the host's mating behaviour and its exposure to predators. In addition, at different times of infection, significant changes occur in the expression of c-fos in the host's hyppocampus, hypothalamus and preoptic area. Thus, the host's brain seems to sense and/or react to intraperitoneal infection. The physiological domains of the network affected by the infection, which classically included the hypothalamus-pituitary-axis and the immune system, must now incorporate the host's sexual hormones and other areas of the brain. The network's complex circuitry and functions may help understand some basic questions of parasitology (i.e. the hosts' sexual dimorphism in parasite infections, host-parasite specificity, heterogeneity in the course and outcome of infections at different stages of parasite and host development). The plurality of elements and the complexity of the network that regulates the host-parasite relationship also point to additional strategies for the treatment and control of infections.

Keywords

sex steroidscysticercosisTaenia crassicepshost-parasite relationship
Type
Review Article
Information
Parasitology , Volume 131 , Issue 3 , September 2005 , pp. 287 - 294
Copyright
© 2005 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Addis, C. J. Jr. ( 1946). Experiments on the relation between sex hormones and the growth of tapeworms. Journal of Parasitology 32, 229–236.Google Scholar
Aguilar-Delfin, I., Homer, M. J., Wettstein, P. J. and Persing, D. H. ( 2001). Innate resistance to Babesia infection is influenced by genetic background and gender. Infection and Immunity 69, 7955–7958.CrossRefGoogle Scholar
Ahmed, S. A., Talal, N. and Christadoss, P. ( 1987). Genetic regulation of testosterone-induced immune suppression. Cellular Immunology 104, 91–98.CrossRefGoogle Scholar
Arteaga, M., Chavarria, A. and Morales-Montor, J. ( 2002). The immunoneuroendocrine communication network and the regulation of homeostasis: the use of hormones and neurohormones as immunotherapy. Revista de Investigacion Clinica 54, 542–549.Google Scholar
Barriga, O. O. and Al-Khalidin, W. ( 1991). Effect of host sex and litter on the population dynamics of Echinococcus granulosus in dogs. Journal of Parasitology 77, 927–930.CrossRefGoogle Scholar
Bojalil, R., Terrazas, L. I., Govezensky, T., Sciutto, E. and Larralde, C. ( 1993). Thymus-related cellular immune mechanisms in sex associated resistance to experimental murine cysticercosis (Taenia crassiceps). Journal of Parasitology 78, 471–476.CrossRefGoogle Scholar
Beck, J. W. ( 1951). Effect of diet upon singly established Hymenolepis diminuta in rats. Experimental Parasitology 1, 46–59.CrossRefGoogle Scholar
Booth, M., Mwatha, J. K., Joseph, S., Jones, F. M., Kadzo, H., Ireri, E., Kazibwe, F., Kemijumbi, J., Kariuki, C., Kimani, G., Ouma, J. H., Kabatereine, N. B., Vennervald, B. J. and Dunne, D. W. ( 2004). Periportal fibrosis in human Schistosoma mansoni infection is associated with low IL-10, low IFN-γ, high TNF-α, or low RANTES, depending on age and gender. Journal of Immunology 172, 1295–303.CrossRefGoogle Scholar
Dorais, F. J. and Esch, G. W. ( 1969). Growth rates of two Taenia crassiceps strains. Experimental Parasitology 25, 395–398.CrossRefGoogle Scholar
Escobedo, G., Larralde, C., Chavarria, A., Cerbón, M. A. and Morales-Montor, J. ( 2005). Molecular mechanisms involved in the differential effects of sex-steroids on the reproduction and infectivity of Taenia crassiceps. Journal of Parasitology 90, 1–10.Google Scholar
Esch, G. W. ( 2004). Parasites, People and Places. Cambridge University Press, Cambridge, UK.
Fleury, A., Dessein, A., Preux, P. M., Dumas, M., Tapia, G., Larralde, C. and Sciutto, E. ( 2004). Symptomatic human neurocysticercosis-age, sex and exposure factors relating with disease heterogeneity. Journal of Neurology 251, 830–837.Google Scholar
Freeman, R. S. ( 1962). Studies on the biology of Taenia crassiceps (Zeder 1800) Rudolphi, 1810 (Cestoda). Canadian Journal of Zoology 40, 969–990.CrossRefGoogle Scholar
Gomez, Y., Valdez, R. A., Larralde, C. and Romano, M. C. ( 2000). Sex steroids and parasitism: Taenia crassiceps cisticercus metabolizes exogenous androstenedione to testosterone in vitro. Journal of Steroid Biochemistry and Molecular Biology 74, 143–147.CrossRefGoogle Scholar
Gourbal, B. E., Lacroix, A. and Gabrion, C. ( 2002). Behavioural dominance and Taenia crassiceps parasitism in BALB/c male mice. Parasitology Research 88, 912–927.Google Scholar
Gourbal, B. E., Righi, M., Petit, G. and Gabrion, C. ( 2001). Parasite-altered host behavior in the face of a predator: manipulation or not? Parasitology Research 87, 186–192.Google Scholar
Huerta, L., Terrazas, L. I., Sciutto, E. and Larralde, C. ( 1992). Immunological mediation of gonadal effects on experimental murine cysticercosis caused by Taenia crassiceps metacestodes. Journal of Parasitology 78, 471–476.CrossRefGoogle Scholar
Isseroff, H., Sylvester, P. W., Bessette, C. L., Jones, P. L., Fisher, W. G., Rynkowsky, T. and Gregor, K. T. ( 1989). Schistosomiasis: role of endogenous opioids in suppression of gonadal steroid secretion. Comparative Biochemistry and Physiology 94, 41–45.CrossRefGoogle Scholar
Klein, S. L. ( 2000). Hormones and mating system affect sex and species differences in immune function among vertebrates. Behavioural Processes 51, 149–166.CrossRefGoogle Scholar
Larralde, C., Padilla, A., Hernández, M., Govezensky, T., Sciutto, E., Gutierrez, G., Tapia-Conyer, R., Salvatierra, B. and Sepúlveda, J. ( 1992). Seroepidemiology of cysticercosis in Mexico. Salud Publica de México 34, 197–210.Google Scholar
Larralde, C., Morales, J., Terrazas, I., Govezensky, T. and Romano, M. C. ( 1995). Sex hormone changes induced by the parasite lead to feminization of the male host in murine Taenia crassiceps cysticercosis. Journal of Steroid Biochemistry and Molecular Biology 52, 575–581.CrossRefGoogle Scholar
Lin, Y. C., Kikihisha, Y., Kono, H. and Gu, Y. ( 1990). Effects of larval tapeworm of (Teania taeniformis) on reproductive functions in male and female host rats. Experimental Parasitology 70, 344–352.CrossRefGoogle Scholar
Morales-Montor, J., Arrieta, I., Del Castillo, L. I., Rodriguez-Dorantes, M., Cerbon, M. A. and Larralde, C. ( 2004b). Remote sensing of intraperitoneal parasitism by the host's brain: regional changes of c-fos gene expression in the brain of feminized cysticercotic male mice. Parasitology 128, 343–351.Google Scholar
Morales-Montor, J., Baig, S., Hallal-Calleros, C. and Damian, RT. ( 2002 a). Taenia crassiceps: androgen reconstitution of the host leads to protection during cysticercosis. Experimental Parasitology 100, 209–216.Google Scholar
Morales-Montor, J., Baig, S., Kabbani, A. and Damian, R. T. ( 2002 c). Do interleukin-6 and macrophage-migration inhibitory factor play a role during sex-associated susceptibility in murine cysticercosis? Parasitology Research 88, 901–914.Google Scholar
Morales-Montor, J., Baig, S., Mitchell, R., Deway, K., Hallal-Calleros, C. and Damian, R. T. ( 2001). Immunoendocrine interactions during chronic cysticercosis determine male mouse feminization: role of IL-6. Journal of Immunology 167, 4527–4533.CrossRefGoogle Scholar
Morales-Montor, J., Chavarria, A., De Leon, M. A., Del Castillo, L. I., Escobedo, E. G., Sánchez, E. N., Vargas, J. A., Hernandez-Flores, M., Romo-Gonzalez, T. and Larralde, C. ( 2004 a). Host gender in parasitic infections of mammals: an evaluation of the female host supremacy paradigm. Journal of Parasitology 90, 531–546.Google Scholar
Morales-Montor, J., Hallal-Calleros, C., Romano, M. and Damián, R. T. ( 2002 b). Inhibition of P-450 aromatase prevents feminisation & induces protection during cysticercosis. International Journal for Parasitology 32, 1379–1387.Google Scholar
Morales, J., Larralde, C., Arteaga, M., Govezensky, T., Romano, M. C. and Morali, G. ( 1996). Inhibition of sexual behavior in male mice infected with Taenia crassiceps cysticerci. Journal of Parasitology 82, 689–693.CrossRefGoogle Scholar
Morales-Montor, J., Rodriguez-Dorantes, M. and Cerbon, M. A. ( 1999). Modified expression of steroid 5α-reductase as well as aromatase, but not cholesterol side-chain cleavage enzyme, in the reproductive system of male mice during (Taenia crassiceps) cysticercosis. Parasitology Research 85, 393–398.CrossRefGoogle Scholar
Morales-Montor, J., Rodriguez-Dorantes, M., Mendoza-Rodriguez, C. A., Camacho-Arroyo, I. and Cerbon, M. A. ( 1998). Differential expression of the estrogen-regulated proto-oncogenes c-fos, c-jun, bcl-2 and of the tumor-suppressor p53 gene in the male mouse chronically infected with Taenia crassiceps cysticerci. Parasitology Research 84, 616–622.CrossRefGoogle Scholar
Morales, J., Velasco, T., Tovar, V., Fragoso, G., Fleury, A., Beltrán, C., Villalobos, N., Aluja, A., Rodarte, L. F., Sciutto, E. and Larralde, C. ( 2002). Castration and pregnancy of rural pigs significantly increase the prevalence of naturally acquired Taenia solium cysticercosis. Veterinary Parasitology 108, 41–48.CrossRefGoogle Scholar
Mosmann, T. R. and Coffman, R. L. ( 1989). TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Annual Review of Immunology 7, 145–173.CrossRefGoogle Scholar
Nacher, M., Singhasivanon, P., Treeprasertsuk, S., Silamchamroon, U., Phumratanaprapin, W., Fontanet, A. L. and Looareesuwan, S. ( 2003). Gender differences in the prevalences of human infection with intestinal helminths on the Thai-Burmese border. Annals of Tropical Medical Parasitology 97, 433–435.CrossRefGoogle Scholar
Padilla, A., Govezensky, T., Sciutto, E., Jimenez-Garcia, L. F., Gonsebatt, M. E., Ramirez, P. and Larralde, C. ( 2001). Kinetics and characterization of cellular responses in the peritoneal cavity of mice infected with Taenia crassiceps. Journal of Parasitology 87, 591–599.CrossRefGoogle Scholar
Phillips, W. J. and Cannon L. R. G. ( 1978). Ecological observations on the commercial sand crab Portunus pelagicus (L) and its parasite Sacculina granifera Boshma, 1973 (Cirripeda: Rizocephala). Journal of Fish Diseases 1, 137–149.CrossRefGoogle Scholar
Reed, M. J., Topping, L., Coldham, N. G., Purohit, A., Ghilchik, M. W. and James, V. H. T. ( 1993). Control of aromatase activity in breast cancer cells: the role of cytokines and growth factors. Journal of Steroid Biochemistry and Molecular Biology 44, 589–593.CrossRefGoogle Scholar
Roberts, C. W., Walker, A. H. and Alexander, J. ( 2001). Sex-associated hormones and immunity to protozoan parasites. Clinical Microbiological Reviews. 14, 476–488.CrossRefGoogle Scholar
Rodriguez-Sosa, M., David, J. R., Bojalil, R., Satoskar, A. R. and Terrazas LI. ( 2002). Cutting edge: susceptibility to the larval stage of the helminth parasite Taenia crassiceps is mediated by Th2 response induced via STAT6 signaling. Journal of Immunology 168, 3135–3139.CrossRefGoogle Scholar
Sciutto, E., Fragoso, G., Diaz, M. L., Valdez, F., Montoya, R. M., Govezensky, T., Lomeli, C. and Larralde, C. ( 1991). Murine Taenia crassiceps cysticercosis: H-2 complex and sex influence on susceptibility. Parasitology Research 77, 243–246.CrossRefGoogle Scholar
Sciutto, E., Fragoso, G., Trueba, L., Lemus, D., Montoya, R. M., Diaz, M. L., Govezensky, T., Lomeli, C., Tapia, G. and Larralde, C. ( 1990). Cysticercosis vaccine: cross protecting immunity with T. solium antigens against experimental murine T. crassiceps cysticercosis. Parasite Immunology 12, 687–696.Google Scholar
Smith, J. K., Esch, G. E. and Kuhn, R. E. ( 1972). Growth and development of larval Taenia crassiceps (cestoda). I. Aneuploidy in the anomalous ORF strain. International Journal for Parasitology 2, 261–263.CrossRefGoogle Scholar
Terrazas, L. I., Bojalil, R., Govezensky, T. and Larralde, C. ( 1998). Shift from an early protective TH1 immune response to a late permissive TH2-type response in murine cysticercosis (Taenia crassiceps). Journal of Parasitology 84, 74–81.CrossRefGoogle Scholar
Terrazas, L. I., Bojalil, R., Govezensky, T. and Larralde, C. ( 1994). A role for 17β-estradiol in immunoendocrine regulation of cysticercosis (Taenia crassiceps). Journal of Parasitology 80, 563–568.CrossRefGoogle Scholar
Terrazas, L. I., Cruz, M., Rodriguez-Sosa, M., Bojalil, R., Garcia-Tamayo, F. and Larralde, C. ( 1999). Th1-type cytokines improve resistance to murine cysticercosis caused by Taenia crassiceps. Parasitology Research 85, 135–141.CrossRefGoogle Scholar
Toenjes, S. A., Spolski, R. J., Mooney, K. A. and Kuhn, R. E. ( 1999). The systemic immune response of BALB/c mice infected with larval Taenia crassiceps is a mixed Th1/Th2-type response. Parasitology 118, 623–633.CrossRefGoogle Scholar
Vega, R., Pinero, D., Ramanankandrasana, B., Dumas, M., Bouteille, B., Fleury, A., Sciutto, E., Larralde, C. and Fragoso G. ( 2003). Population genetic structure of Taenia solium from Madagascar and Mexico: implications for clinical profile diversity and immunological technology. International Journal for Parasitology 33, 1479–1485.CrossRefGoogle Scholar
Zuk, M. and McKean, K. A. ( 1996). Sex differences in parasite infections: patterns and processes. International Journal for Parasitology 260, 1009–1023.CrossRefGoogle Scholar