Neonatal exposure to estradiol induces resistance to helminth infection and changes in the expression of sex steroid hormone receptors in the brain and spleen in adult mice of both sexes

Brain, Behavior, and Immunity

Volumn 23, Issue 5, 2009, Pages 709-715

  Guzmán, Carolina ^a   Camacho Arroyo, Ignacio ^a   De León Nava, Marco A ^a   Morales Montor, Jorge ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Cysticercosis; Defeminization; Demasculinization; Early development; Estradiol; Estrogen receptor; Infection; Interferon ; Interleukin 4; Progesterone receptor; Sex steroid receptors; Taenia crassiceps

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR; GAMMA INTERFERON; INTERLEUKIN 4; PROGESTERONE RECEPTOR;

ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; CELLULAR IMMUNITY; CONTROLLED STUDY; ESTROGEN ACTIVITY; ESTRUS CYCLE; FEMALE; FEMINIZATION; HELMINTHIASIS; INFECTION RESISTANCE; INFECTION SENSITIVITY; MALE; MOUSE; NEONATAL STRESS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEX DIFFERENCE; SPLEEN CELL; TAENIA CRASSICEPS; TAENIASIS; VIRILIZATION;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BRAIN; BRAIN CHEMISTRY; CYSTICERCOSIS; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTRUS; FEMALE; IMMUNE SYSTEM; IMMUNITY, INNATE; INTERFERON-GAMMA; INTERLEUKIN-4; MALE; MICE; MICE, INBRED BALB C; RECEPTORS, ESTROGEN; RECEPTORS, PROGESTERONE; SEXUAL MATURATION; SPLEEN; TAENIA; TH1 CELLS; TH2 CELLS;

EID: 68649109082     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbi.2009.02.014     Document Type: Article

References (51)

1. Ansar A.S., Penhale W.J., and Talal N. Sex hormones, immune responses, and autoimmune diseases. Mechanisms of sex hormone action. Am. J. Pathol. 121 (1985) 531-551
2. Arrieta I., Diaz-Ibanez L.B., Morales T., Mendoza-Garces L., Morimoto S., Moreno-Mendoza N., and Cerbon M.A. Progesterone receptor gene and protein expression in the anterior preoptic area and hypothalamus of defeminized rats. J. Neurobiol. 56 (2003) 338-346
3. Arteaga M., Chavarria A., and Morales Montor J. Immunoneuroendocrine communication network and homeostasis regulation: the use of hormones and neurohormones as immunotherapy. Rev. Invest. Clin. 54 (2002) 542-549
4. Auger A.P. Steroid receptor control of reproductive behavior. Horm. Behav. 45 (2004) 168-172
5. Ayi K., Giribaldi G., Skorokhod A., Schwarzer E., Prendergast P.T., and Arese P. 16alpha-bromoepiandrosterone, an antimalarial analogue of the hormone dehydroepiandrosterone, enhances phagocytosis of ring stage parasitized erythrocytes: a novel mechanism for antimalarial activity. Antimicrob. Agents Chemother. 46 (2002) 3180-3184
6. Beyer C., Damm N., Brito V., and Kuppers E. Developmental expression of progesterone receptor isoforms in the mouse midbrain. Neuroreport 13 (2002) 877-880
7. Camacho-Arroyo I., Guerra-Araiza C., Dominguez R., Mendoza-Rodriguez C.A., Cruz M.E., and Cerbon M.A. C-fos expression pattern in the hypothalamus and the preoptic area of the rat during proestrus. Life Sci. 62 (1998) 1153-1159
8. Camacho-Arroyo I., Gonzalez-Arenas A., and Gonzalez-Moran G. Ontogenic variations in the content and distribution of progesterone receptor isoforms in the reproductive tract and brain of chicks. Comp. Biochem. Physiol. A - Mol. Integr. Physiol. 146 (2007) 644-652
9. Carrero J.C., Cervantes C., Moreno-Mendoza N., Saavedra E., Morales-Montor J., and Laclette J.P. Dehydroepiandrosterone decreases while cortisol increases in vitro growth and viability of Entamoeba histolytica. Microbes Infect. 8 (2006) 323-331
10. Correale J., Arias M., and Gilmore W. Steroid hormone regulation of cytokine secretion by proteolipid protein-specific CD4+ T cell clones isolated from multiple sclerosis patients and normal control subjects. J. Immunol. 161 (1998) 3365-3374
11. Davies M.J., and Norman R.J. Programming and reproductive functioning. Trends Endocrinol. Metab. 13 (2002) 386-392
12. Dorais F.J., and Esch G.W. Growth rate of two Taenia crassiceps strains. Exp. Parasitol. 25 (1969) 395-398
13. Everitt B.J., and Hokfelt T. Neuroendocrine anatomy of the hypothalamus. Acta Neurochir. Suppl. (Wien) 47 (1990) 1-15
14. Faas M., Bouman A., Moesa H., Heineman M.J., de Leij L., and Schuiling G. The immune response during the luteal phase of the ovarian cycle: a Th2-type response?. Fertil. Steril. 74 (2000) 1008-1013
15. Fox H.S., Bond B.L., and Parslow T.G. Estrogen regulates the IFN-γ promoter. J. Immunol. 146 (1991) 4362-4367
16. Giangrande P.H., and McDonnell D.P. The A and B isoforms of the human progesterone receptor: two functionally different transcription factors encoded by a single gene. Recent Prog. Horm. Res. 54 (1999) 291-313 discussion 313-294
17. Gilmore W., Weiner L.P., and Correale J. Effect of estradiol on cytokine secretion by proteolip protein-specific T cell clones isolated from multiple sclerosis patients and normal control subjects. J. Immunol. 158 (1997) 446-451
18. Giron-Gonzalez J.A., Moral F.J., Elvira J., Garcia-Gil D., Guerrero F., Gavilan I., and Escobar L. Consistent production of a higher Th1:Th2 cytokine ratio by stimulated T cells in men compared with women. Eur. J. Endocrinol. 43 (2000) 31-36
19. Gourbal B.E., Righi M., Petit G., and Gabrion C. Parasite-altered host behavior in the face of a predator: manipulation or not?. Parasitol. Res. 87 (2001) 186-192
20. Grossman C.J. Possible underlaying mechanism of sexual dimorphism in the immune response, fact and hypothesis. J. Steroid Biochem. 34 (1989) 241-251
21. Guerra-Araiza C., Cerbon M.A., Morimoto S., and Camacho-Arroyo I. Progesterone receptor isoforms expression pattern in the rat brain during the estrous cycle. Life Sci. 66 (2000) 1743-1752
22. Jones J.H. Fetal programming: adaptive life-history tactics or making the best of a bad start?. Am. J. Hum. Biol. 17 (2005) 22-33
23. Katsuda S., Yoshida M., Watanabe G., Taya K., and Maekawa A. Irreversible effects of neonatal exposure to p-tert-octylphenol on the reproductive tract in female rats. Toxicol. Appl. Pharmacol. 165 (2000) 217-226
24. Khurana S., Ranmal S., and Ben-Jonathan N. Exposure of newborn male and female rats to environmental estrogens: delayed and sustained hyperprolactinemia and alterations in estrogen receptor expression. Endocrinology 141 (2000) 4512-4517
25. Kouki T., Kishitake M., Okamoto M., Oosuka I., Takebe M., and Yamanouchi K. Effects of neonatal treatment with phytoestrogens, genistein and daidzein, on sex difference in female rat brain function: estrous cycle and lordosis. Horm. Behav. 44 (2003) 140-145
26. Larralde C., Morales J., Terrazas I., Govezensky T., and Romano M.C. Sex hormone changes induced by the parasite lead to feminization of the male host in murine Taenia crassiceps cysticercosis. J. Steroid Biochem. Mol. Biol. 52 (1995) 575-580
27. Loria R.M., and Padgett D.A. Control of the immune response by DHEA and its metabolites. Rinsho Byori 46 (1998) 505-517
28. Lydon J.P., DeMayo F.J., Funk C.R., Mani S.K., Hughes A.R., Montgomery Jr. C.A., Shyamala G., Conneely O.M., and O'Malley B.W. Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev. 9 (1995) 2266-2278
29. Mani S.K., Reyna A.M., Chen J.Z., Mulac-Jericevic B., and Conneely O.M. Differential response of progesterone receptor isoforms in hormone-dependent and -independent facilitation of female sexual receptivity. Mol. Endocrinol. 20 (2006) 1322-1332
30. Manikkam M., Steckler T.L., Welch K.B., Inskeep E.K., and Padmanabhan V. Fetal programming: prenatal testosterone treatment leads to follicular persistence/luteal defects; partial restoration of ovarian function by cyclic progesterone treatment. Endocrinology 147 (2006) 1997-2007
31. Mendoza-Rodriguez C.A., Merchant-Larios H., Segura-Valdez M.L., Moreno-Mendoza N., Cruz M.E., Arteaga-Lopez P., Camacho-Arroyo I., Dominguez R., and Cerbon M. C-fos and estrogen receptor gene expression pattern in the rat uterine epithelium during the estrous cycle. Mol. Reprod. Dev. 64 (2003) 379-388
32. Morales J., Larralde C., Arteaga M., Govezensky T., Romano M.C., and Morali G. Inhibition of sexual behavior in male mice infected with Taenia crassiceps cysticerci. J. Parasitol. 82 (1996) 689-693
33. Morales-Montor J., Rodriguez-Dorantes M., Mendoza-Rodriguez C.A., Camacho-Arroyo I., and Cerbon M.A. Differential expression of the estrogen-regulated proto-oncogenes c-fos, c-jun, and bcl-2 and of the tumor-suppressor p53 gene in the male mouse chronically infected with Taenia crassiceps cysticerci. Parasitol. Res. 84 (1998) 616-622
34. Morales-Montor J., Baig S., Mitchell R., Deway K., Hallal-Calleros C., and Damian R.T. Immunoendocrine interactions during chronic cysticercosis determine male mouse feminization: role of IL-6. J. Immunol. 167 (2001) 4527-4533
35. Morales-Montor J., Hallal-Calleros C., Romano M.C., and Damian R.T. Inhibition of p-450 aromatase prevents feminisation and induces protection during cysticercosis. Int. J. Parasitol. 32 (2002) 1379-1387
36. Morales-Montor J., Chavarria A., De Leon M.A., Del Castillo L.I., Escobedo E.G., Sanchez E.N., Vargas J.A., Hernandez-Flores M., Romo-Gonzalez T., and Larralde C. Host gender in parasitic infections of mammals: an evaluation of the female host supremacy paradigm. J. Parasitol. 90 (2004) 531-546
37. Newbold R.R., and Liehr J.G. Induction of uterine adenocarcinoma in CD-1 mice by catechol estrogens. Cancer Res. 60 (2000) 235-237
38. Newbold R.R., Hanson R.B., Jefferson W.N., Bullock B.C., Haseman J., and McLachlan J.A. Proliferative lesions and reproductive tract tumors in male descendants of mice exposed developmentally to diethylstilbestrol. Carcinogenesis 21 (2000) 1355-1363
39. Olsen N.J., and Kovacs W.J. Gonadal steroids and immunity. Endocr. Rev. 17 (1996) 369-384
40. Olster D.H., and Blaustein J.D. Development of steroid-induced lordosis in female guinea pigs: effects of different estradiol and progesterone treatments, clonidine, and early weaning. Horm. Behav. 23 (1989) 118-129
41. Palanza P., Morellini F., Parmigiani S., and vom Saal F.S. Prenatal exposure to endocrine disrupting chemicals: effects on behavioral development. Neurosci. Biobehav. Rev. 23 (1999) 1011-1027
42. Paredes R.G. Medial preoptic area/anterior hypothalamus and sexual motivation. Scand. J. Psychol. 44 (2003) 203-212
43. Paxinos, E.F. (Ed.), 1997. The mouse brain in stereotaxic coorinates.
44. Pfaff D.W., Freidin M.M., Wu-Peng X.S., Yin J., and Zhu Y.S. Competition for DNA steroid response elements as a possible mechanism for neuroendocrine integration. J. Steroid Biochem. Mol. Biol. 49 (1994) 373-379
45. Safeukui I., Mangou F., Malvy D., Vincendeau P., Mossalayi D., Haumont G., Vatan R., Olliaro P., and Millet P. Plasmodium berghei: dehydroepiandrosterone sulfate reverses chloroquino-resistance in experimental malaria infection; correlation with glucose 6-phosphate dehydrogenase and glutathione synthesis pathway. Biochem. Pharmacol. 68 (2004) 1903-1910
46. Sarma H.N., Manikkam M., Herkimer C., Dell'Orco J., Welch K.B., Foster D.L., and Padmanabhan V. Fetal programming: excess prenatal testosterone reduces postnatal luteinizing hormone, but not follicle-stimulating hormone responsiveness, to estradiol negative feedback in the female. Endocrinology 146 (2005) 4281-4291
47. Schauenstein K., Rinner I., Felsner P., Liebmann P., Hass H., Wolfler S., Stevenson A., Westermann R.J., Cohen R.L., and Chambers D.A. The dialogue between the brain and the immune system involves not only the HPA-axis. Z. Rheumatol. 59 (2000) 49-53
48. Sciutto E., Fragoso G., Diaz M.L., Valdez F., Montoya R.M., Govezensky T., Lomeli C., and Larralde C. Murine Taenia crassiceps cysticercosis: H-2 complex and sex influence on susceptibility. Parasitol. Res. 77 (1991) 243-246
49. Sohoni P., and Sumpter J.P. Several environmental oestrogens are also anti-androgens. J. Endocrinol. 158 (1998) 327-339
50. Steckler T., Wang J., Bartol F.F., Roy S.K., and Padmanabhan V. Fetal programming: prenatal testosterone treatment causes intrauterine growth retardation, reduces ovarian reserve and increases ovarian follicular recruitment. Endocrinology 146 (2005) 3185-3193
51. Yoshida M., Takenaka A., Katsuda S., Kurokawa Y., and Maekawa A. Neonatal exposure to p-tert-octylphenol causes abnormal expression of estrogen receptor alpha and subsequent alteration of cell proliferating activity in the developing Donryu rat uterus. Toxicol. Pathol. 30 (2002) 357-364