Skip to main content

Sex Differences in Parasitic Infections: Beyond the Dogma of Female-Biased Resistance

  • Chapter
  • First Online:
Sex Hormones and Immunity to Infection

Abstract

Sex differences in parasitic infections are a biological phenomenon of considerable significance for individual health and disease as well as for the evolution of a species. The general rule of thumb is that females are more resistant to infectious diseases than males. There are, however, many notable exceptions to this rule that illustrate a female bias in susceptibility to infection. By studying sex differences to cysticercosis infection, it has been demonstrated that females are more likely than males to become infected, to carry larger parasite loads, to be more severely affected, and more reticent to developing protective immunity. Our animal studies illustrate that female-biased susceptibility to parasitic infection is influenced by hormones, reproductive status, age, and genetic background. The mechanisms underlying the sexual dimorphism in murine cysticercosis involve the effects of sex steroids on both the host immune and central nervous systems as well as directly on the parasite. In this chapter, the causes of female-biased susceptibility to parasitic, and possibly other, infections are examined.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 219.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 279.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 279.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Addis CJ Jr (1946) Experiments on the relation between sex hormones and the growth of tapeworms. J Parasitol 32:229–236

    Google Scholar 

  • Agrawal AF, Lively CM (2001) Parasites and the evolution of self-fertilization. Int J Organic Evol 55:869–879

    CAS  Google Scholar 

  • Arnott MA, Cassella JP, Aitken PP, Hay J (1990) Social interactions of mice with congenital Toxoplasma infection. Ann Trop Med Parasitol 84:149–156

    PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Barnea ER (2001) Embryo maternal dialogue: From pregnancy recognition to proliferation control. Early Preg 5:65–66

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Berdoy M, Webster JP, MacDonald DW (1995) The manipulation of rat behaviour by Toxoplasma gondii. Mammalia 59:605–613

    Article  Google Scholar 

  • Besedovsky HO, del Rey A (2002) Introduction: Immune-neuroendocrine network. Front Hormone Res 29:1–14

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Briggs MH (1972) Metabolism of steroid hormones by schistosomes. Biochim Biophys Acta 280:481–485

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Charlab R, Blaineau C, Schechtman D, Barcinski MA (1990) Granulocyte-macrophage colony-stimulating factor is a growth-factor for promastigotes of Leishmania mexicana amazonensis. J Protozool 37:352–7

    PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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 C-leucine. Exp Parasitol 32:272–281

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Derijk R, Berkenbosch F (1991) The immune-hypothalamo-pituitary-adrenal axis and autoimmunity. Int J Neurosci 59:91–100

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Esch GW, Smith JD (1976) Studies on the in vitro culture of Taenia crassiceps. Int J Parasitol 6:143–149

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Evershed RP, Mercer JG, Rees HH (1987) Capillary gas chromatography/mass spectrometry of ecdysteroids. J Chromatogr 390:357–369

    Article  PubMed  CAS  Google Scholar 

  • Flegr J, Lindova J, Kodym P (2008) Sex-dependent toxoplasmosis-associated differences in testosterone concentrations in humans. Parasitology 135:427–431

    Article  PubMed  CAS  Google Scholar 

  • Fleming MW (1985) Ascaris suum: role of ecdysteroids in molting. Exp Parasitol 60:207–210

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Foster JM, Pennock JF, Marshall I, Rees HH (1993) Biosynthesis of isoprenoid compounds in Schistosoma mansoni. Mol Biochem Parasitol 61:275–284

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Freeman RS (1962) Studies on the biology of Taenia crassiceps (Zeder 1800) Rudolphi, 1810 (Cestoda). Can J Zool 40:969–990

    Article  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Ganley LS, Rajan TV (2001) Endogenous testosterone levels do not affect filarial worm burdens in mice. Exp Parasitol 98:29–34

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Grossman CJ, Sholiton LJ, Nathan P (1979) Rat thymic estrogen receptor. I. Preparation, location, and physiochemical properties. J Steroid Biochem 11:1233–40

    Article  PubMed  CAS  Google Scholar 

  • Grossman CJ, Roselle GA, Mendenhall CL (1991) Sex steroid regulation of autoimmunity. J Steroid Biochem Molec Biol 40:649–659

    Article  PubMed  CAS  Google Scholar 

  • Hanssen SA, Folstad I, Erikstad KE (2003) Reduced immunocompetence and cost of reproduction in common eiders. Oecologia 136:457–464

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hughes VL, Randolph SE (2001) Testosterone increases the transmission potential of tick-borne parasites. Parasitol 123:365–71

    CAS  Google Scholar 

  • Johnson LL, Sayles PC (2002) Deficient humoral responses underlie susceptibility to Toxoplasma gondii in CD4-deficient mice. Infect Immunity 70:185–191

    Article  CAS  Google Scholar 

  • Kavaliers M, Colwell DD (1993) Multiple opioid system involvement in the mediation of parasitic-infection induced analgesia. Brain Res 623:316–320

    Article  PubMed  CAS  Google Scholar 

  • Kavaliers M, Choleris E, Colwell DD (2001) Brief exposure to female odors ‘‘emboldens’’ male mice by reducing predatorinduced behavioral and hormonal responses. Hormones Behav 40:497–509

    Article  CAS  Google Scholar 

  • Klein SL (2000) The effects of hormones on sex differences in infection: From genes to behavior. Neuro Biobehavior Rev 24:627–638

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kyes S, Horrocks P, Newbold C (2001) Antigenic variation at the infected red cell surface in malaria. Ann Rev Microbiol 55:673–707

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Martin JT (2000) Sexual dimorphism in immune function: the role of prenatal exposure to androgens and estrogens. Eur J Pharmacol 405:251–261

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Matzinger P (2002) The danger model: A renewed sense of self. Science 296:301–305

    Article  PubMed  CAS  Google Scholar 

  • Medzhitov R, Janeway CA (2002) Decoding the patterns of self and nonself by the innate immune system. Sci 296:298–300

    Article  CAS  Google Scholar 

  • Mendis AHW, Rose ME, Rees HH, Goodwin TW (1983) Ecdysteroids in adults of the filarial nematode Dirofilaria immitis. Mol Biochem Parasitol 9:209–226

    Article  PubMed  CAS  Google Scholar 

  • Mendis AHW, Rees HH, Goodwin TW (1984) The occurrence of ecdysteroids in the cestode Monienza expansa. Mol Biochem Parasitol 10:123–138

    Article  PubMed  CAS  Google Scholar 

  • Mercer JG, Munn AE, Rees HH (1987) Echinococcus granulosus: occurrence of ecdysteroids in protoscoleces and hydatic cyst fluid. Mol Biochem Parasitol 24:203–214

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Moore SL, Wilson K (2002) Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297:2015–2018

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Morales-Montor J, Baig S, Kabbani A, Damian RT (2002a) Do interleukin- 6 and macrophage-migration inhibitory factor play a role during sex-associated susceptibility in murine cysticercosis? Parasitol Res 88:901–904

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Oltvai ZN, Barabási AL (2002) Systems biology Life’s complexity pyramid. Science 298(5594):763–4

    Article  PubMed  CAS  Google Scholar 

  • Owens IP (2002) Ecology and evolution: Sex differences in mortality rate. Science 297:2008–2009

    Article  PubMed  Google Scholar 

  • Panhuis TM, Butlin R, Zuk M, Tregenza T (2001) Sexual selection and speciation. Trends Ecol Evol 1:364–371

    Article  Google Scholar 

  • Philipp M, Parkhouse RM, Ogilvie BM (1980) Changing proteins on the surface of a parasitic nematode. Nature 287:538–540

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Poulin R, Thurn JR (1996) Sexual inequalities in helminth infections: A cost of being a male? Am Nat 147:287–295

    Article  Google Scholar 

  • Pung OJ, Luster MI (1986) Toxoplasma gondii: decreased resistance to infection in mice due to estrogen. Exp Parasitol 61:48–56

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Roberts CW, Walker W, Alexander J (2001) Sex-associated hormones and immunity to protozoan parasites. Clin Microbiol Rev 14:476–488

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Rumjanek FD, Simpson AJG (1980) The incorporation and utilization of radiolabelled lipids by adult Schistosoma mansoni. Mol Biochem Parasitol 1:31–44

    Article  PubMed  CAS  Google Scholar 

  • Sani BP, Vaid A, Comley JC, Montgomery JA (1985) Novel retinoid-binding proteins from filarial parasites. Biochem J 232:577–83

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 downregulation of immune responses in parasitic and retroviral infection. Immunol Rev 127:183–204

    Article  PubMed  CAS  Google Scholar 

  • Sinisi AA, Pasquali D, Notaro A, Bellastella A (2003) Sexual differentiation. J Endocrinol Invest 26:S23–S28

    Google Scholar 

  • Sternberg EM (1997) Neural-immune interactions in health and disease. J Clin Invest 100:2641–7

    Article  PubMed  CAS  Google Scholar 

  • Strohman R (2003) Thermodynamics–old laws in medicine and complex disease. Nat Biotechnol 21(5):477–9

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Townson S, Tagboto SK (1996) In vitro cultivation and development of Onchocerca volvulus and Onchocerca lienalis microfilariae. Am J Trop Med Hyg 54:32–7

    PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Vargas-Villavicencio JA, Larralde C, Morales-Montor J (2006) Gonadectomy and progesterone treatment induce protection in murine cysticercosis. Parasite Immunol 28:667–674

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Verthelyi D (2001) Sex hormones as immunomodulators in health and disease. Int Immunopharmacol 1:983–93

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Webster JP, Brunton CFA, MacDonald DW (1994) Effect of Toxoplasma gondii upon neophobic behaviour in wild brown rats, Rattus norvegicus. Parasitology 109:37–43

    Article  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Zuk M, McKean KA (1996) Sex differences in parasite infections: Patterns and processes. Int J Parasitol 26:1009–1023

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Financial support was provided by Dirección General de Asuntos del Personal Académico, Universidad Nacional Autonoma de México (UNAM), IN213108, by The National Council of Science and Technology of Mexico (CONACyT, 58283) and by a special grant from Fundación Miguel Alemán-SSA, the three of them to J.M.-M. G.E., and MADL were CONACyT Ph.D. fellows.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jorge Morales-Montor .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Escobedo, G., De León-Nava, M.A., Morales-Montor, J. (2010). Sex Differences in Parasitic Infections: Beyond the Dogma of Female-Biased Resistance. In: Klein, S., Roberts, C. (eds) Sex Hormones and Immunity to Infection. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-02155-8_7

Download citation

Publish with us

Policies and ethics