Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-12T22:03:32.648Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  03 March 2004

J. MORALES-MONTOR ,
I. ARRIETA ,
L. I. DEL CASTILLO ,
M. RODRÍGUEZ-DORANTES ,
M. A. CERBÓN  and
C. LARRALDE
J. MORALES-MONTOR
Affiliation:
Departamento de Inmunología, Instituto de Investigaciones Biomédicas and
I. ARRIETA
Affiliation:
Departamento de Biología, Facultad de Química, Universidad Nacional Autónoma de Mexico
L. I. DEL CASTILLO
Affiliation:
Departamento de Inmunología, Instituto de Investigaciones Biomédicas and
M. RODRÍGUEZ-DORANTES
Affiliation:
Departamento de Biología, Facultad de Química, Universidad Nacional Autónoma de Mexico
M. A. CERBÓN
Affiliation:
Departamento de Biología, Facultad de Química, Universidad Nacional Autónoma de Mexico
C. LARRALDE
Affiliation:
Departamento de Inmunología, Instituto de Investigaciones Biomédicas and Centro Internacional de Ciencias, Cuernavaca, Morelos, Mexico
Get access Rights & Permissions [Opens in a new window]

Abstract

Experimental intraperitoneal Taenia crassiceps cysticercosis in mice exhibits distinct genetical, immunological and endocrinological features possibly resulting from the complex interactive network of their physiological systems. Very notable is the tendency of parasites to grow faster in hosts of the female sex. It is also remarkable in the feminization process that the infection induces in chronically infected male mice, characterized by their estrogenization, deandrogenization and loss of sexual and aggressive patterns of behaviour. The proto-oncogene c-fos is a sex steroid-regulated transcription factor gene, expressed basally and upon stimulation by many organisms. In the CNS of rodents, c-fos is found expressed in association to sexual stimulation and to various immunological and stressful events. Hence, we suspected that changes in c-fos expression in the brain could be involved in the feminization of the infected male mice. Indeed, it was found that c-fos expression increased at different times during infection in the hypothalamus, hippocampus, less so in the preoptic area and cortex, and not in several other organs. The significant and distinctive regional changes of c-fos in the CNS of infected mice indicate that the brain of the host senses intraperitoneal cysticercosis and may also announce its active participation in the regulation of the host–parasite relationship. Possibly, the host's CNS activity is involved in the network that regulates the estrogenization and deandrogenization observed in the chronically infected male mice, as well as in the behavioural and immunological peculiarities observed in this parasitic infection.

Keywords

c-fosfeminizationTaenia crassicepscysticercosisparasitisminfectioncentral nervous systembrain
Type
Research Article
Information
Parasitology , Volume 128 , Issue 3 , March 2004 , pp. 343 - 351
Copyright
2004 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

BESEDOVSKY, H. O. & DEL REY, A. (2002). Introduction: immune-neuroendocrine network. Frontiers in Hormone Research 29, 1–14.Google Scholar
BIGSBY, R. M. & LI, A. (1994). Differentially regulated immediate early genes in the rat uterus. Endocrinology 134, 1820–1826.CrossRefGoogle Scholar
BOJALIL, R., TERRAZAS, L. I., GOVEZENSKY, T., SCIUTTO, E. & LARRALDE, C. (1993). Thymus-related cellular immune mechanisms in sex associated resistance to experimental murine cysticercosis (Taenia crassiceps). Journal of Parasitology 78, 384–389.CrossRefGoogle Scholar
DORAIS, F. J. & ESCH, G. W. (1969). Growth rates of two Taenia crassiceps strains. Experimental Parasitology 25, 395–398.CrossRefGoogle Scholar
FRALEY, G. S., SHIMADA, I., BAUMGARTNER, J. W., CLIFTON, D. K. & STEINER, R. A. (2003). Differential patterns of Fos induction in the hypothalamus of the rat following central injections of galanin-like peptide and galanin. Endocrinology 144, 1143–1146.CrossRefGoogle Scholar
FREEMAN, R. S. (1962). Studies on the biology of Taenia crassiceps (Zeder 1800) Rudolphi, 1810 (Cestoda). Canadian Journal of Zoology 40, 869–872.CrossRefGoogle Scholar
GÓMEZ, Y., VALDEZ, R. A., LARRALDE, C. & ROMANO, M. C. (2000). Sex steroids and parasitism: Taenia crassiceps cysticercosis metabolizes exogenous androstenedione to testosterone in vitro. Journal of Steroid Biochemistry and Molecular Biology 74, 143–147.CrossRefGoogle Scholar
GOTTSTEIN, B. V., TSANG, V. C. & SCHANTZ, P. M. (1986). Demonstration of species-specific and cross-reactive components of Taenia solium metacestodes antigens. American Journal of Tropical Medicine and Hygiene 35, 308–313.CrossRefGoogle Scholar
GOURBAL, B. E., RIGHI, M., PETIT, G. & GABRION, C. (2001). Parasite-altered host behaviour in the face of a predator: manipulation or not? Parasitology Research 87, 186–192.Google Scholar
HYDER, S. M., SHIPLEY, G. L. & STANCEL, G. M. (1995). Oestrogen action in target cells: selective requirements for activation of different hormone response elements. Molecular and Cellular Endocrinology 112, 35–43.CrossRefGoogle Scholar
HYDER, S. M., STANCEL, G. M., NAWAZ, Z., McDONNELL, D. P. & LOOSE-MITCHELL, D. S. (1992). Identification of an oestrogen response element in the 3′-flanking region of the murine c-fos proto-oncogene. Journal of Biological Chemistry 267, 18047–18054.Google Scholar
KUMAR, A., DUDLEY, C. A. & MOSS, R. L. (1999). Functional dichotomy within the vomeronasal system: distinct zones of neuronal activity in the accessory olfactory bulb correlate with sex-specific behaviour. Journal of Neurosciences 19, RC32–RC38.CrossRefGoogle Scholar
KUMEI, Y., TODA, K., KAWAUCHI, Y., SHIMOKAWA, R., SHIMOKAWA, H. & MAKITA, K. (2000). Nociceptive responses and immunohisto-chemical changes in the rat brain under gravity stress. Journal of Gravitational Physiology 7, 91–102.Google Scholar
LARRALDE, C., MORALES, J., TERRAZAS, L. I., GOVEZENSKY, T. & ROMANO, M. C. (1995). Sex hormone changes induced by the parasite lead to feminisation of the male host in murine Taenia crassiceps cysticercosis. Journal of Steroid Biochemistry and Molecular Biology 52, 575–580.CrossRefGoogle Scholar
LARRALDE, C., SOTELO, J., MONTOYA, R. M., PALENCIA, G., PADILLA, A., GOVEZENSKY, T., DIAZ, M. L. & SCIUTTO, E. (1990). Immunodiagnosis of human cysticercosis in cerebrospinal fluid: Antigens from murine Taenia crassiceps cysticerci effectively substitute those from porcine Taenia solium. Archives of Pathology and Laboratory Medicine 114, 926–928.Google Scholar
LEE, H. H., SHIOW, S. J., CHUNG, H. C., HUANG, C. Y., LIN, C. L., HSU, J. D., SHYU, L. Y. & WANG, C. J. (2000). Development of brain injury in mice by Angiostrongylus cantonensis infection is associated with the induction of transcription factor NF-kappaB, nuclear proto-oncogenes, and protein tyrosine phosphorylation. Experimental Parasitology 95, 202–208.CrossRefGoogle Scholar
MORALES, J., LARRALDE, C., ARTEAGA, M., GOVEZENSKY, T., ROMANO, M. C. & MORALÍ, G. (1996). Inhibition of sexual behaviour in male mice infected with Taenia crassiceps cysticerci. Journal of Parasitology 82, 689–693.CrossRefGoogle Scholar
MORALES-MONTOR, J., BAIG, S., KABBANI, A. & DAMIAN, R. T. (2002). Do interleukin-6 and macrophage migration inhibitory factor have a role during sex-associated susceptibility to cysticercosis? Parasitology Research 88, 901–904.Google Scholar
MORALES-MONTOR, J., MITCHELL, R., DEWAY, K., HALLAL-CALLEROS, C., BAIG, S. & DAMIAN, R. T. (2001). Immunoendocrine interactions determine male mouse feminisation during chronic infection with Taenia crassiceps cysticerci: Role of IL-6. Journal of Immunology 167, 4527–4533.CrossRefGoogle Scholar
MORALES-MONTOR, J., RODRÍGUEZ-DORANTES, M., MÉNDOZA-RODRGUEZ, C. A., CAMACHO-ARROYO, I. & CERBÓN, M. A. (1998). Differential expression of oestrogen-induced proto-oncogenes c-fos, c-jun and bcl-2 and the tumor supressor p53 gene in the male mouse during chronic infection with Taenia crassiceps cysticerci. Parasitology Research 84, 616–622.CrossRefGoogle Scholar
OLTVAI, Z. N. & BARABASI, A. L. (2002). Systems biology. Life's complexity pyramid. Science 25, 763–764.Google Scholar
PACHECO-LÓPEZ, G., ESPINOSA, E., ZAMORANO-ROJAS, H. M., RAMIREZ-AMAYA, V. & BERMUDEZ-RATTONI, F. (2002). Peripheral protein immunization induces rapid activation of the CNS, as measured by c-fos expression. Journal of Neuroimmunology 131, 50–59.CrossRefGoogle Scholar
PALMER, J. M., WONG-RILEY, M. & SHARKEY, K. A. (1998). Functional alterations in jejunal myenteric neurons during inflammation in nematode-infected guinea pigs. American Journal of Physiology 275, G922–G935.CrossRefGoogle Scholar
PAXINOS, G., ASHWELL, K. W. S. & TORK, I. (1994). Atlas of the Developing Rat Nervous System, 3rd Edn. Academic Press, San Diego.
PAXINOS, G. & WATSON, C. (1998). The Rat Brain in Sterotaxic Coordinates, 5th Edn. Academic Press, New York.
RAVASZ, E., SOMERA, A. L., MONGRU, D. A., OLTVAI, Z. N. & BARABASI, A. L. (2002). Hierarchical organization of modularity in metabolic networks. Science 30, 1551–1555.CrossRefGoogle Scholar
SCIUTTO, E., FRAGOSO, G., DÍAZ, M. L., VALDEZ, F., LOMELÍ, C., GOVEZENSKY, T., MONTOYA, R. M. & LARRALDE, C. (1991). Murine Taenia crassiceps cysticercosis: H-2 and sex influence on susceptibility. Parasitology Research 77, 243–246.CrossRefGoogle Scholar
SCHANTZ, P. M., TSANG, V. C. & MADDISON, S. E. (1988). Serodiagnosis of neurocysticercosis. Review in Infectious Diseases 10, 1231–1233.CrossRefGoogle Scholar
SMITH, K. J., DORAIS, G. W. & 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
SVARNIK, O. E., ANOKHIN, K. V. & ALEKSANDROV, Y. I. (2003). Distribution of behaviourally specialized neurons and expression of transcription factor c-fos in the rat cerebral cortex during learning. Neurosciences Behavioural Physiology 33, 139–142.CrossRefGoogle Scholar
TERRAZAS, L. I., BOJALIL, R., GOVEZENSKY, T. & LARRALDE, C. (1994). A role for 17β-estradiol in immunoendocrine regulation of cysticercosis (Taenia crassiceps). Journal of Parasitology 80, 563–568.CrossRefGoogle Scholar
TOLEDO, A., FRAGOSO, G., ROSAS, G., HERNÁNDEZ, M., GEVORKIAN, G., LÓPEZ-CASILLAS, F., HERNÁNDEZ, B., ACERO, G., HUERTA, M., LARRALDE, C. & SCIUTTO, E. (2001). Two epitopes shared by Taenia crassiceps and Taenia solium confer protection against murine T. crassiceps cysticercosis along with a prominent Th1 response. Infection and Immunity 69, 1766–1773.Google Scholar
WERSINGER, S. R. & RISSMAN, E. F. (2000). Oestrogen receptor alpha is essential for female-directed chemo-investigatory behaviour but is not required for the pheromone-induced luteinizing hormone surge in male mice. Journal of Neuroendocrinology 12, 103–110.Google Scholar
XU, S., GUO, S., JIANG, X., YIN, Q., UMEZAWA, T. & HISAMITSU, T. (2003). Effect of indomethacin on the c-fos expression in AVP and TH neurons in rat brain induced by lipopolysaccharide. Brain Research 14, 13–18.CrossRefGoogle Scholar
ZHANG, J., ZHANG, D., McQUADE, J. S., BEHBEHANI, M., TSIEN, J. Z. & XU, M. (2002). c-fos regulates neuronal excitability and survival. Nature, Genetics 30, 416–420.CrossRefGoogle Scholar