Sex differences in parasitic infections: Beyond the dogma of female-biased resistance

Sex Hormones and Immunity to Infection

Volumn , Issue , 2010, Pages 187-204

  Escobedo, Galileo ^b   De León Nava, Marco A ^b   Morales Montor, Jorge ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84877694907     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-3-642-02155-8_7     Document Type: Chapter

References (128)

1. Addis CJ Jr (1946) Experiments on the relation between sex hormones and the growth of tapeworms. J Parasitol 32:229-236.
2. Agrawal AF, Lively CM (2001) Parasites and the evolution of self-fertilization. Int J Organic Evol 55:869-879.
3. Arnott MA, Cassella JP, Aitken PP, Hay J (1990) Social interactions of mice with congenital Toxoplasma infection. Ann Trop Med Parasitol 84:149-156.
4. Barnard CJ, Behnke JM, Gage AR, Brown H, Smithurst PR (1998) The role of parasite-induced immunodepression, rank and social environment in the modulation of behaviour and hormone concentration in male laboratory mice (Mus musculus). Proc R Soc Lond B Biol Sci 22:693-701.
5. Barnea ER (2001) Embryo maternal dialogue: From pregnancy recognition to proliferation control. Early Preg 5:65-66.
6. Barrabes A, Duong TH, Combescot C (1979) Effect of testosterone or progesterone implants on the intensity of experimental infestation with Schistosoma mansoni in the female golden hamster. C R Seances Soc Biol Fil 173:153-6.
7. Barrabes A, Goma-Mouanda J, Reynouard F, Combescot C (1986) 17 beta-estradiol receptors in Schistosoma mansoni. Contribution to the explanation of the protective power of this hormone in Schistosoma mansoni bilharziasis in the mouse. Preliminary study. Ann Parasitol Hum Comp 61:637-41.
8. Benten WP, Becker A, Schmitt-Wrede HP, Wunderlich F (2002) Developmental regulation of intracellular and surface androgen receptors in T cells. Steroids 67:925-931.
9. Berdoy M, Webster JP, MacDonald DW (1995) The manipulation of rat behaviour by Toxoplasma gondii. Mammalia 59:605-613.
10. Besedovsky HO, del Rey A (2002) Introduction: Immune-neuroendocrine network. Front Hormone Res 29:1-14.
11. Boissier J, Chlichlia K, Digon Y, Ruppel A, Mone H (2003) Preliminary study on sex-related inflammatory reactions in mice infected with Schistosoma mansoni. Parasitol Res 91(2): 144-50.
12. Bojalil R, Terrazas LI, Govezensky T, Sciutto E, Larralde C (1993) Thymus-related cellular immune mechanisms in sex associated resistance to experimental murine cysticercosis (Taenia crassiceps). J Parasitol 79:384-389.
13. Briggs MH (1972) Metabolism of steroid hormones by schistosomes. Biochim Biophys Acta 280:481-485.
14. Brouwers JFHM, Van Hellemond JJ, van Golde LMG, Tielens AG (1998) Ether lipids and their possible physiological function in adult Schistosoma mansoni. Mol Biochem Parasitol 96: 49-58.
15. Carrero JC, Cervantes C, Moreno Mendoza N, Saavedra E, Morales Montor J, Laclette JP (2006) Dehydroepiandrosterone decreases while cortisol increases in vitro growth and viability of Entamoeba histolytica. Microbes Infect 8:323-31.
16. Cernetich A, Garver LS, Jedlicka AE, Klein PW, Kumar N, Scott AL, Klein SL (2006) Involvement of gonadal steroids and gamma interferon in sex differences in response to blood-stage malaria infection. Infect Immun 74:3190-3203.
17. Charlab R, Blaineau C, Schechtman D, Barcinski MA (1990) Granulocyte-macrophage colonystimulating factor is a growth-factor for promastigotes of Leishmania mexicana amazonensis. J Protozool 37:352-7.
18. Charles S, Morand S, Chasse JL, Auger DP (2002) Host patch selection induced by parasitism: Basic reproduction ratio r(0) and optimal virulence. Theor Pop Biol 62:97-109.
19. Cleator M, Delves CJ, Howells RE, Rees HH (1987) Identity and tissue localization of free and conjugated ecdysteroids in adults of Dirofilaria immitis and Ascaris suum. Mol Biochem Parasitol 25:93-105.
20. Cruz-Revilla C, Rosas G, Fragoso G, Lopez-Casillas F, Toledo A, Larralde C, Sciutto E (2000) Taenia crassiceps cysticercosis: Protective effect and immune response elicited by DNA immunization. J Parasitol 86:67-74.
21. Culbreth KL, Esch GW, Kuhn RE (1972) Growth and development of larval Taenia crassiceps (Cestoda) III. The relationships between larval biomass and the uptake and incorporation of Cleucine. Exp Parasitol 32:272-281.
22. Daly TM, Long CA (1995) Humoral response to a carboxylterminal region of the merozoite surface protein-1 plays a predominant role in controlling blood-stage infection in rodent malaria. J Immunol 55:236-243.
23. Degu G, Mengistu G, Jones J (2002) Some factors affecting prevalence of and immune responses to Schistosoma mansoni in schoolchildren in Gorgora, northwest Ethiopia. Ethiop Med J 40:345-52.
24. Del Brutto OH, Garcia E, Talamas O, Sotelo J (1988) Sex related severity of inflammation in parenchymal brain cysticercosis. Arch Int Med 148:544-546.
25. Derijk R, Berkenbosch F (1991) The immune-hypothalamo-pituitary-adrenal axis and autoimmunity. Int J Neurosci 59:91-100.
26. Dissanayake S (2000) Upregulation of a raf kinase and a DP-1 family transcription factor in epidermal growth factor (EGF) stimulated filarial parasites. Int J Parasitol 30:1089-97.
27. Do Prado JC, Leal MP, Anselmo-Franci JA, de Andrade HF, Kloetzel JK (1998) Influence of female gonadal hormones on the parasitemia of female Calomys callosus infected with the "Y" strain of Trypanosoma cruzi. Parasitol Res 84:100-105.
28. Do Prado JC, Jr Lam, Leal MP, Bernard E, Kloetzel JK (1999) Influence of male gonadal hormones on the parasitemia and humoral response of male Calomys callosus infected with the Y strain of Trypanosoma cruzi. Parasitol Res 85:826-9.
29. Eloi-Santos S, Olsen NJ, Correa-Oliveira R, Colley DG (1992) Schistosoma mansoni: mortality, pathophysiology, and susceptibility differences in male and female mice. Exp Parasitol 75:168-75.
30. Esch GW, Smith JD (1976) Studies on the in vitro culture of Taenia crassiceps. Int J Parasitol 6:143-149.
31. Escobedo G, Larralde C, Chavarria A, Cerbón MA, Morales-Montor J (2004) Molecular mechanism involved in the differential effects of sex steroids on the reproduction and infectivity of Taenia crassiceps. J Parasitol 90:1235-1244.
32. Escobedo G, Roberts CW, Carrero JC, Morales-Montor J (2005) Parasite regulation by host hormones: An old mechanism of host exploitation? Trends Parasitol 21:588-593.
33. Evershed RP, Mercer JG, Rees HH (1987) Capillary gas chromatography/mass spectrometry of ecdysteroids. J Chromatogr 390:357-369.
34. Flegr J, Lindova J, Kodym P (2008) Sex-dependent toxoplasmosis-associated differences in testosterone concentrations in humans. Parasitology 135:427-431.
35. Fleming MW (1985) Ascaris suum: Role of ecdysteroids in molting. Exp Parasitol 60:207-210.
36. Fleury A, Gomez T, Alvarez I, Meza D, Huerta M, Chavarria A, Carrillo-Mezo RA, Lloyd C, Dessein A, Preux PM, Dumas M, Larralde C, Sciutto E, Fragoso G (2003) High prevalence of calcified silent neurocysticercosis in a rural village of Mexico. Neuroepidemiology 22: 139-145.
37. Foster JM, Pennock JF, Marshall I, Rees HH (1993) Biosynthesis of isoprenoid compounds in Schistosoma mansoni. Mol Biochem Parasitol 61:275-284.
38. Fragoso G, Lamoyi E, Mellor A, Lomeli C, Govezensky T, Sciutto E (1996) Genetic control of susceptibility to Taenia crassiceps cysticercosis. Parasitology 112:119-124.
39. Fragoso G, Lamoyi E, Mellor A, Lomeli C, Hernandez M, Sciutto E (1998) Increased resistance to Taenia crassiceps murine cysticercosis in Qa-2 transgenic mice. Infect Immun 66:760-764.
40. Fragoso G, Meneses G, Sciutto E, Fleury A, Larralde C (2008) Preferential growth of Taenia crassiceps cysticerci in female mice holds across several laboratory mice strains and parasite lines. J Parasitol 94(2):551-3.
41. Freeman RS (1962) Studies on the biology of Taenia crassiceps (Zeder 1800) Rudolphi, 1810 (Cestoda). Can J Zool 40:969-990.
42. Freilich D, Ferris S, Wallace M, Leach L, Kallen A, Frincke J, Ahlem C, Hacker M, Nelson D, Hebert J (2000) 16-alpha-bromoepiandrosterone, a dehydroepiandrosterone (DHEA) analogue, inhibits Plasmodium falciparum and Plasmodium berghei growth. Amer J Trop Med Hyg 63:280-283.
43. Gaillard RC, Spinedi E (1998) Sex- and stress-steroids interactions and the immune system: Evidence for a neuroendocrineimmunological sexual dimorphism. Dom An Endocrinol 15:345-352.
44. Ganley LS, Rajan TV (2001) Endogenous testosterone levels do not affect filarial worm burdens in mice. Exp Parasitol 98:29-34.
45. Ghansah TJ, Ager EC, Freeman-Junior P, Villalta F, Lima MF (2002) Epidermal growth factor binds to a receptor on Trypanosoma cruzi amastigotes inducing signal transduction events and cell proliferation. J Eukaryot Microbiol 49:383-90.
46. Ghosh PK, Gupta S, Leon LR, Ghosh R, Ruiz-Ordaz BH, Ortiz-Ortiz L (1998) Intestinal amoebiasis: Antibody-secreting cells and humoral antibodies. J Diarrhoeal Dis Res 1:1-7.
47. Gomez Y, Valdez RA, Larralde C, Romano MC (2000) Sex steroids and parasitism: Taenia crassiceps cisticercus metabolizes exogenous androstenedione to testosterone in vitro. J Steroid Biochem Mol Biol 74:143-7.
48. Gourbal BE, Righi M, Petit G, Gabrion C (2001) Parasite-altered host behavior in the face of a predator: Manipulation or not? Parasitol Res 87:186-192.
49. Grossman CJ, Sholiton LJ, Nathan P (1979) Rat thymic estrogen receptor. I. Preparation, location, and physiochemical properties. J Steroid Bio chem 11:1233-40.
50. Grossman CJ, Roselle GA, Mendenhall CL (1991) Sex steroid regulation of autoimmunity. J Steroid Biochem Molec Biol 40:649-659.
51. Hanssen SA, Folstad I, Erikstad KE (2003) Reduced immuno competence and cost of reproduction in common eiders. Oecologia 136:457-464.
52. Huerta L, Terrazas LI, Sciutto E, Larralde C (1992) Immunological mediation of gonadal effects on experimental murine cysticercosis caused by Taenia crassiceps metacestodes. J Parasitol 78:471-476.
53. Hughes VL, Randolph SE (2001) Testosterone increases the transmission potential of tick-borne parasites. Parasitol 123:365-71.
54. Johnson LL, Sayles PC (2002) Deficient humoral responses underlie susceptibility to Toxoplasma gondii in CD4-deficient mice. Infect Immunity 70:185-191.
55. Kavaliers M, Colwell DD (1993) Multiple opioid system involvement in the mediation of parasitic-infection induced analgesia. Brain Res 623:316-320.
56. Kavaliers M, Choleris E, Colwell DD (2001) Brief exposure to female odors "emboldens" male mice by reducing pre datorinduced behavioral and hormonal responses. Hormones Behav 40:497-509.
57. Klein SL (2000) The effects of hormones on sex differences in infection: From genes to behavior. Neuro Biobehavior Rev 24:627-638.
58. Klein SL, Marson AL, Scott AL, Ketner G, Glass GE (2002) Neonatal sex steroids affect responses to Seoul virus infection in male but not female Norway rats. Brain Behav Immunol 16:736-746.
59. Kyes S, Horrocks P, Newbold C (2001) Antigenic variation at the infected red cell surface in malaria. Ann Rev Microbiol 55:673-707.
60. Larralde C, Morales J, Terrazas I, Govezensky T, Romano MC (1995) Sex hormone changes induced by the parasite lead to feminization of the male host in murine Taenia crassiceps cysticercosis. J Steroid Biochem Mol Biol 52:575-580.
61. Liesenfeld O, Nguyen TA, Pharke C, Suzuki Y (2001) Importance of gender and sex hormones in regulation of susceptibility of the small intestine to peroral infection with Toxoplasma gondii tissue cysts. J Parasitol 87:1491-3.
62. Lingnau A, Margos G, Maier WA, Seitz HM (1993) The effects of hormones on the gametocytogenesis of Plasmodium falciparum in vitro. Appl Parasitol 34:153-60.
63. Marguerite M, Gallissot MC, Diagne M, Moreau C, Diakkhate MM, Roberts M et al (1999) Cellular immune responses of a Senegalese community recently exposed to Schistosoma mansoni: correlations of infection level with age and inflammatory cytokine production by soluble egg antigen-specific cells. Trop Med Int Health 4:530-43.
64. Martal J, de la Llosa-Permier MP, Chene N, Huynh L, Millet S, Haridon RL, Assal A, Roignant N, Chaouat G (1995) Trophoblastic interferons and embryonal immune tolerance. Contracep Fert Sexual 23:562-572.
65. Martin JT (2000) Sexual dimorphism in immune function: The role of prenatal exposure to androgens and estrogens. Eur J Pharmacol 405:251-261.
66. Maswoswe SM, Peters W, Warhurst DC (1985) Corticosteroid stimulation of the growth of Plasmodium falciparum gametocytes in vitro. Ann Trop Med Parasitol 79:607-16.
67. Matzinger P (2002) The danger model: A renewed sense of self. Science 296:301-305.
68. Medzhitov R, Janeway CA (2002) Decoding the patterns of self and non self by the innate immune system. Sci 296:298-300.
69. Mendis AHW, Rose ME, Rees HH, Goodwin TW (1983) Ecdysteroids in adults of the filarial nematode Dirofilaria immitis. Mol Biochem Parasitol 9:209-226.
70. Mendis AHW, Rees HH, Goodwin TW (1984) The occurrence of ecdysteroids in the cestode Monienza expansa. Mol Biochem Parasitol 10:123-138.
71. Mercer JG, Munn AE, Rees HH (1987) Echinococcus granulosus: occurrence of ecdysteroids in protoscoleces and hydatic cyst fluid. Mol Biochem Parasitol 24:203-214.
72. Mercer JG, Barker GC, Howells RE, Rees HH (1990) Investigation of ecdysteroid excretion by adult Dirofilaria immitis and Brugia pahangi. Mol Biochem Parasitol 39:89-96.
73. Meyer F, Meyer H, Bueding E (1970) Lipid metabolism in the parasitic and free-living flatworms, Schistosoma mansoni and Dugesia dorotocephala. Biochem Biophys Acta 210:257-266.
74. Moore SL, Wilson K (2002) Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297:2015-2018.
75. Morales J, Larralde C, Arteaga M, Govezensky T, Romano MC, Morali DG (1996) Inhibition of sexual behavior in male mice infected with Taenia crassiceps cysticerci. J Parasitol 82:689-693.
76. Morales J, Velasco T, Tovar V, Fragoso G, Fleury A, Beltran C, Villalobos N, Aluja A, Rodarte LF, Sciutto E, Larralde C (2002) Castration and pregnancy of rural porcines significantly increase the prevalence of naturally acquired Taenia solium cysticercosis. Vet Parasitol 30:41-48.
77. Morales-Montor J, Baig S, Mitchell R, Deway K, Hallal-Calleros C, Damian RT (2001a) Immunoendocrine interactions during chronic cysticercosis determine male mouse feminization: Role of IL-6. J Immunol 167:4527-4533.
78. Morales-Montor J, Mohamed F, Ghaleb AM, Baig S, Hallal-Calleros C, Damian RT (2001b) In vitro effects of hypothalamic-pituitary-adrenal axis (HPA) hormones on Schistosoma mansoni. J Parasitol 87:1132-1139.
79. Morales-Montor J, Baig S, Kabbani A, Damian RT (2002a) Do interleukin- 6 and macrophagemigration inhibitory factor play a role during sex-associated susceptibility in murine cysticercosis? Parasitol Res 88:901-904.
80. Morales-Montor J, Baig S, Hallal-Calleros C, Damian RT (2002b) Taenia crassiceps: Androgen reconstitution of the host leads to protection during cysticercosis. Exp Parasitol 100:209-216.
81. Morales-Montor J, Hallal-Calleros C, Romano C, Damian RT (2002c) Inhibition of P-450 aromatase prevents feminisation and induces protection during cysticercosis. Int J Parasitol 32:1379-1387.
82. Morales-Montor J, Arrieta I, del castillo LI, Rodríguez-Dorantes M, Cerbón MA, Larralde C (2004) Remote sensing of intraperitoneal parasitism by the host's brain: Regionalchanges of c-fos gene expression in the brain of feminised cysticercotic male mice. Parasitol 128:1-9.
83. Nakazawa M, Fantappie MR, Freeman GL Jr, Eloi-Santos S, Olsen NJ, Kovacs WJ et al (1997) Schistosoma mansoni: susceptibility differences between male and female mice can be mediated by testosterone during early infection. Exp Parasitol 85:233-40.
84. Oltvai ZN, Barabási AL (2002) Systems biology Life's complexity pyramid. Science 298 (5594):763-4.
85. Owens IP (2002) Ecology and evolution: Sex differences in mortality rate. Science 297:2008- 2009.
86. Panhuis TM, Butlin R, Zuk M, Tregenza T (2001) Sexual selection and speciation. Trends Ecol Evol 1:364-371.
87. Philipp M, Parkhouse RM, Ogilvie BM (1980) Changing proteins on the surface of a parasitic nematode. Nature 287:538-540.
88. Phillips AN, Antunes F, Stergious G, Ranki A, Jensen GF, Bentwich Z et al (1994) A sex comparison of rates of new AIDS-defining disease and death in 2554 AIDS cases AIDS in Europe Study Group. Aids 8:831-835.
89. Potti J, Davila JA, Tella JL, Frias O, Villar S (2002) Gender and viability selection on morphology in fledgling pied flycatchers. Mol Ecol 11:1317-1326.
90. Poulin R, Thurn JR (1996) Sexual inequalities in helminth infections: A cost of being a male? Am Nat 147:287-295.
91. Pung OJ, Luster MI (1986) Toxoplasma gondii: decreased resistance to infection in mice due to estrogen. Exp Parasitol 61:48-56.
92. Rafati S, Salmanian AH, Hashemi K, Schaff C, Belli S, Fasel N (2001) Identification of Leishmania major cysteine proteinases as targets of the immune response in humans. Mol Biochem Parasitol 113:35-43.
93. Remoue F, Van To D, Schacht AM, Picquet M, Garraud O, Vercruysse J, Ly A, Capron A, Riveau G (2001) Gender-dependent specific immune response during chronic human Schistosomiasis haematobia. Clin Exp Immunol 124:62-8.
94. Remoue F, Mani JC, Pugniere M, Schacht AM, Capron A, Riveau G (2002) Functional specific binding of testosterone to Schistosoma haematobium 28-Kilodalton glutathione S-transferase. Infect Immun 70:601-5.
95. Restrepo BI, Aguilar MI, Melby PC, Teale JM (2001) Analysis of the peripheral immune response in patients with neurocysticercosis: Evidence for T cell reactivity to parasite glycoprotein and vesicular fluid antigens. Am J Trop Med Hyg 65:366-370.
96. Roberts CW, Cruickshank SM, Alexander J (1995) Sex-determined resistance to Toxoplasma gondii is associated with temporal differences in cytokine production. Infect Immun 63:2549- 2555.
97. Roberts CW, Walker W, Alexander J (2001) Sex-associated hormones and immunity to protozoan parasites. Clin Micro biol Rev 14:476-488.
98. Romano MC, Valdéz RA, Cartas AL, Gómez Y, Larralde C (2003) Steroid hormone production by parasites: The case of Taenia crassiceps and Taenia solium cysticerci. J Steroid Biochem Mol Biol 85:221-225.
99. Rumjanek FD, Simpson AJG (1980) The incorporation and utilization of radiola belled lipids by adult Schistosoma mansoni. Mol Biochem Parasitol 1:31-44.
100. Sani BP, Vaid A, Comley JC, Montgomery JA (1985) Novel retinoid-binding proteins from filarial parasites. Bio chem J 232:577-83.
101. Sciutto E, Fragoso G, Diaz ML, Valdez F, Montoya RM, Govezensky T, Lomeli C, Larralde C (1991) Murine Taenia crassiceps cysticercosis: H-2 complex and sex influence on susceptibility. Parasitol Res 77:243-246.
102. Sciutto E, Fragoso G, Manoutcharian K, Gevorkian G, Rosas-Salgado G, Hernandez-Gonzalez M, Herrera-Estrella L, Cabrera-Ponce L, López-Casillas F, Gonzalez-Bonilla C, Santiago- Machuca A, Ruiz-Pérez F, Sanchez J, Goldbaum F, Aluja A, Larralde C (2002) New approaches to improve a peptide vaccine against porcine Taenia solium cysticercosis. Arch Med Res 33:371-378.
103. Sher A, Gazzinelli RT, Oswald IP, Clerici M, Kullberg M, Pearce EJ, Berzofsky JA, Mosmann TR, James SL, Morse HC III (1992) Role of T-cell derived cytokines in the down regulation of immune responses in parasitic and retroviral infection. Immunol Rev 127:183-204.
104. Sinisi AA, Pasquali D, Notaro A, Bellastella A (2003) Sexual differentiation. J Endocrinol Invest 26:S23-S28.
105. Sternberg EM (1997) Neural-immune interactions in health and disease. J Clin Invest 100:2641-7.
106. Strohman R (2003) Thermodynamics-old laws in medicine and complex disease. Nat Bio technol 21(5):477-9.
107. Tella JL, Scheuerlein A, Ricklefs RE (2002) Is cell-mediated immunity related to the evolution of life-history strategies in birds? Proc Royal Soc London Biol Sci 22:1059-1066.
108. Terrazas LI, Bojalil R, Govezensky T, Larralde C (1994) A role for 17-beta-estradiol in immunoendocrine regulation of murine cysticercosis (Taenia crassiceps). J Parasitol 80:563-568.
109. Terrazas LI, Bojalil R, Govezensky T, Larralde C (1998) Shift from an early protective Th1-type immune response to a late permissive TH2-type response in murine cysticercosis (Taenia crassiceps). J Parasitol 84:74-81.
110. Terrazas LI, Cruz M, Rodriguez-Sosa M, Bojalil R, Garcia-Tamayo F, Larralde C (1999) Th1-type cytokines improve resistance to murine cysticercosis caused by Taenia crassiceps. Parasitol Res 85:135-141.
111. Toenjes SA, Spolski RJ, Mooney KA, Kuhn RE (1999) The systemic immune response of BALB/c mice infected with larval Taenia crassiceps is a mixed Th1/TH2-type response. Parasitol 118:623-633.
112. Townson S, Tagboto SK (1996) In vitro cultivation and development of Onchocerca volvulus and Onchocerca lienalis micro filariae. Am J Trop Med Hyg 54:32-7.
113. Travis BL, Osorio Y, Melby PC, Chandrasekar B, Arteaga L, Saravia NG (2002) Gender is a major determinant of the clinical evolution and immune response in hamsters infected with Leishmania spp. Infect Immun 70:2288-96.
114. Unnasch TR, Bradley J, Beauchamp J, Tuan R, Kennedy MW (1999) Characterization of a putative nuclear receptor from Onchocerca volvulus. Mol Biochem Parasitol 104:259-69.
115. Vacchina P, Valdéz RA, Gómez Y, Revelli S, Romano MC (2008) Steroidogenic capacity of Trypanosoma cruzi trypomastigotes. J Steroid Biochem Mol Biol 111:282-6.
116. Valdéz RA, Jiménez P, Cartas AL, Gómez Y, Romano MC (2006) Taenia solium cysticerci synthesize androgens and estrogens in vitro. Parasitol Res 98(5):472-6.
117. Vargas-Villavicencio JA, Larralde C, Morales-Montor J (2006) Gonadectomy and progesterone treatment induce protection in murine cysticercosis. Parasite Immunol 28:667-674.
118. Vargas-Villavicencio JA, Larralde C, De León-Nava MA, Escobedo G, Morales-Montor J (2007) Tamoxifen treatment induces protection in murine cysticercosis. J Parasitol 93:1512-1517.
119. Verthelyi D (2001) Sex hormones as immunomodulators in health and disease. Int Immunopharmacol 1:983-93.
120. Vicogne J, Pin JP, Lardans V, Capron M, Noel C, Dissous C (2003) An unusual receptor tyrosine kinase of Schistosoma mansoni contains a Venus Flytrap module. Mol Biochem Parasitol 126:51-62.
121. Walker W, Roberts CW, Ferguson DJ, Jebbari H, Alexander J (1997) Innate immunity to Toxoplasma gondii is influenced by gender and is associated with differences in interleukin- 12 and gamma interferon production. Infect Immun 65(3):1119-21.
122. Watanabe K, Hamano KS, Noda K, Koga M, Tada I (1999) Strongyloides ratti: Additive effect of testosterone implantation and carbon injection on the susceptibility of female mice. Parasitol Res 85:522-526.
123. Webster JP, Brunton CFA, MacDonald DW (1994) Effect of Toxoplasma gondii upon neophobic behaviour in wild brown rats, Rattus norvegicus. Parasitology 109:37-43.
124. Willis C, Poulin R (2000) Preference of female rats for the odours of non-parasitised males: The smell of good genes? Folia Parasitologica (Praha) 47:6-10.
125. Yates RA, Tuan RS, Shepley KJ, Unnasch TR (1995) Characterization of genes encoding members of the nuclear hormone receptor superfamily from Onchocerca volvulus. Mol Biochem Parasitol 70:19-31.
126. Zhang S, Li Z, Cai S, Zeng L (2000) Observation of T lymphocyte subsets in the liver of patients with advanced schistosomiasis and advanced schistosomiasis accompanied with hepatitis B. J Tongji Med Univ 20:137-8.
127. Zuk M (1994) Immunology and the evolution of behavior. In: Real L (ed) Behavioral mechanisms in evolutionary ecology. University of Chicago Press, Chicago, Illinois, pp 354-368.
128. Zuk M, McKean KA (1996) Sex differences in parasite infections: Patterns and processes. Int J Parasitol 26:1009-1023.