Toxoplasma, testosterone, and behavior manipulation: The role of parasite strain, host variations, and intensity of infection

Frontiers in Biology

Volumn 9, Issue 2, 2014, Pages 151-160

  Abdoli, Amir ^a,b  

^a KASHAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b TARBIAT MODARES UNIVERSITY   (Iran)

Author keywords

behavior manipulation; host variations; intensity of infection; neurologic and psychiatric disorders; parasite strain; testosterone; Toxoplasma gondii

Indexed keywords

EID: 84897581472     PISSN: 16747984     EISSN: 16747992     Source Type: Journal    
DOI: 10.1007/s11515-014-1291-5     Document Type: Review

References (112)

1. Abdoli A (2013). Toxoplasma gondii and neuropsychiatric diseases: strain hypothesis. Neurol Sci, 34(9): 1697-1698.
2. Abdoli A, Dalimi A, Arbabi M, Ghaffarifar F (2014). Neuropsychiatric manifestations of latent toxoplasmosis on mothers and their offspring. J Matern Fetal Neonatal Med, doi: 10. 3109/14767058. 2013. 858685.
3. Abdoli A, Dalimi A, Movahedin M (2012). Impaired reproductive function of male rats infected with Toxoplasma gondii. Andrologia, 44(Suppl 1): 679-687.
4. Achermann J C, Jameson J L (1999). Fertility and infertility: genetic contributions from the hypothalamic-pituitary-gonadal axis. Mol Endocrinol, 13(6): 812-818.
5. Aikey J L, Nyby J G, Anmuth D M, James P J (2002). Testosterone rapidly reduces anxiety in male house mice (Mus musculus). Horm Behav, 42(4): 448-460.
6. Alonso R, Chaudieu I, Diorio J, Krishnamurthy A, Quirion R, Boksa P (1993). Interleukin-2 modulates evoked release of [3H]dopamine in rat cultured mesencephalic cells. J Neurochem, 61(4): 1284-1290.
7. Arantes T P, Lopes W D, Ferreira R M, Pieroni J S, Pinto V M, Sakamoto C A, Costa A J (2009). Toxoplasma gondii: evidence for the transmission by semen in dogs. Exp Parasitol, 123(2): 190-194.
8. Berdoy M, Webster J P, Macdonald D W (1995). Parasite-altered behaviour: is the effect of Toxoplasma gondii on Rattus norvegicus specific? Parasitology, 111(Pt 4): 403-409.
9. Berdoy M, Webster J P, Macdonald D W (2000). Fatal attraction in rats infected with Toxoplasma gondii. Proc Biol Sci, 267(1452): 1591-1594.
10. Booth A, Granger D A, Mazur A, Kivlighan K T (2006). Testosterone and social behavior. Soc Forces, 85(1): 167-191.
11. Choksi N Y, Jahnke G D, St Hilaire C, Shelby M (2003). Role of thyroid hormones in human and laboratory animal reproductive health. Birth Defects Res B Dev Reprod Toxicol, 68(6): 479-491.
12. Cox R M, John-Alder H B (2007). Increased mite parasitism as a cost of testosterone in male striped plateau lizards Sceloporus virgatus. Funct Ecol, 21(2): 327-334.
13. Dalimi A, Abdoli A (2012). Latent toxoplasmosis and human. Iran J Parasitol, 7(1): 1-17.
14. Dalimi A, Abdoli A (2013). Toxoplasma gondii and male reproduction impairment: a new aspect of toxoplasmosis research. Jundishapur J Microbiol, 6(8): e7184.
15. Dardé M L (2008). Toxoplasma gondii, "new" genotypes and virulence. Parasite, 15(3): 366-371.
16. Dass S A, Vasudevan A, Dutta D, Soh L J, Sapolsky R M, Vyas A (2011). Protozoan parasite Toxoplasma gondii manipulates mate choice in rats by enhancing attractiveness of males. PLoS ONE, 6(11): e27229.
17. de Moraes E P, Batista A M, Faria E B, Freire R L, Freitas A C, Silva M A, Braga V A, Mota R A (2010). Experimental infection by Toxoplasma gondii using contaminated semen containing different doses of tachyzoites in sheep. Vet Parasitol, 170(3-4): 318-322.
18. Dominguez J M, Hull E M (2005). Dopamine, the medial preoptic area, and male sexual behavior. Physiol Behav, 86(3): 356-368.
19. Dubey J P, Ferreira L R, Martins J, McLeod R (2012). Oral oocystinduced mouse model of toxoplasmosis: effect of infection with Toxoplasma gondii strains of different genotypes, dose, and mouse strains (transgenic, out-bred, in-bred) on pathogenesis and mortality. Parasitology, 139(1): 1-13.
20. Dubey J P, Frenkel J K (1998). Toxoplasmosis of rats: a review, with considerations of their value as an animal model and their possible role in epidemiology. Vet Parasitol, 77(1): 1-32.
21. Eisenegger C, Haushofer J, Fehr E (2011). The role of testosterone in social interaction. Trends Cogn Sci, 15(6): 263-271.
22. Fabiani S, Pinto B, Bruschi F (2013). Toxoplasmosis and neuropsychiatric diseases: can serological studies establish a clear relationship? Neurol Sci, 34(4): 417-425.
23. Flegr J (2007). Effects of toxoplasma on human behavior. Schizophr Bull, 33(3): 757-760.
24. Flegr J (2010). Influence of latent toxoplasmosis on the phenotype of intermediate hosts. Folia Parasitol (Praha), 57(2): 81-87.
25. Flegr J (2013a). Influence of latent Toxoplasma infection on human personality, physiology and morphology: pros and cons of the Toxoplasma-human model in studying the manipulation hypothesis. J Exp Biol, 216(Pt 1): 127-133.
26. Flegr J (2013b). How and why Toxoplasma makes us crazy. Trends Parasitol, 29(4): 156-163.
27. Flegr J, Hruskový M, Hodná Z, Novotná M, Hanusová J (2005). Body height, body mass index, waist-hip ratio, fluctuating asymmetry and second to fourth digit ratio in subjects with latent toxoplasmosis. Parasitology, 130(Pt 6): 621-628.
28. Flegr J, Lindová J, Kodym P (2008a). Sex-dependent toxoplasmosisassociated differences in testosterone concentration in humans. Parasitology, 135(4): 427-431.
29. Flegr J, Lindová J, Pivoñková V, Havlícek J (2008b). Brief Communication: Latent toxoplasmosis and salivary testosterone concentration-important confounding factors in second to fourth digit ratio studies. Am J Phys Anthropol, 137(4): 479-484.
30. Flegr J, Novotná M, Lindová J, Havlícek J (2008). Neurophysiological effect of the Rh factor. Protective role of the RhD molecule against Toxoplasma-induced impairment of reaction times in women. Neuro Endocrinol Lett, 29(4): 475-481.
31. Gaskell E A, Smith J E, Pinney J W, Westhead D R, McConkey G A (2009). A unique dual activity amino acid hydroxylase in Toxoplasma gondii. PLoS ONE, 4(3): e4801.
32. Gatkowska J, Wieczorek M, Dziadek B, Dzitko K, Dlugonska H (2013). Sex-dependent neurotransmitter level changes in brains of Toxoplasma gondii infected mice. Exp Parasitol, 133(1): 1-7.
33. Grear D A, Perkins S E, Hudson P J (2009). Does elevated testosterone result in increased exposure and transmission of parasites? Ecol Lett, 12(6): 528-537.
34. Groër MW, Yolken RH, Xiao JC, Beckstead JW, Fuchs D, Mohapatra SS, Seyfang A, Postolache TT (2011). Prenatal depression and anxiety in Toxoplasma gondii-positive women. Am J Obstet Gynecol, 204: 433. e1-7.
35. Hay J, Aitken P P, Graham D I (1984). Toxoplasma infection and response to novelty in mice. Z Parasitenkd, 70(5): 575-588.
36. Hay J, Hutchison W M, Aitken P P, Graham D I (1983). The effect of congenital and adult-acquired Toxoplasma infections on activity and responsiveness to novel stimulation in mice. Ann Trop Med Parasitol, 77(5): 483-495.
37. Hermans E J, Putman P, Baas JM, Koppeschaar H P, van Honk J (2006). A single administration of testosterone reduces fear-potentiated startle in humans. Biol Psychiatry, 59(9): 872-874.
38. Hermes G, Ajioka J W, Kelly K A, Mui E, Roberts F, Kasza K, Mayr T, Kirisits M J, Wollmann R, Ferguson D J, Roberts C W, Hwang J H, Trendler T, Kennan R P, Suzuki Y, Reardon C, Hickey WF, Chen L, McLeod R (2008). Neurological and behavioral abnormalities, ventricular dilatation, altered cellular functions, inflammation, and neuronal injury in brains of mice due to common, persistent, parasitic infection. J Neuroinflammation, 5(1): 48.
39. Hill R D, Gouffon J S, Saxton A M, Su C (2012). Differential gene expression in mice infected with distinct Toxoplasma strains. Infect Immun, 80(3): 968-974.
40. Hodková H, Kodym P, Flegr J (2007b). Poorer results of mice with latent toxoplasmosis in learning tests: impaired learning processes or the novelty discrimination mechanism? Parasitology, 134(Pt 10): 1329-1337.
41. Hodková H, Kolbeková P, Skallová A, Lindová J, Flegr J (2007a). Higher perceived dominance in Toxoplasma infected men-a new evidence for role of increased level of testosterone in toxoplasmosisassociated changes in human behavior. Neuro Endocrinol Lett, 28(2): 110-114.
42. Hönekopp J, Bartholdt L, Beier L, Liebert A (2007). Second to fourth digit length ratio (2D: 4D) and adult sex hormone levels: new data and a meta-analytic review. Psychoneuroendocrinology, 32(4): 313-321.
43. Hughes V L, Randolph S E (2001). Testosterone increases the transmission potential of tick-borne parasites. Parasitology, 123(Pt 4): 365-371.
44. Hull E M, Du J, Lorrain D S, Matuszewich L (1995). Extracellular dopamine in the medial preoptic area: implications for sexual motivation and hormonal control of copulation. J Neurosci, 15(11): 7465-7471.
45. Hull E M, Du J, Lorrain D S, Matuszewich L (1997). Testosterone, preoptic dopamine, and copulation in male rats. Brain Res Bull, 44(4): 327-333.
46. Hull E M, Muschamp J W, Sato S (2004). Dopamine and serotonin: influences on male sexual behavior. Physiol Behav, 83(2): 291-307.
47. Hutchison W M, Aitken P P, Wells W P (1980). Chronic Toxoplasma infections and familiarity-novelty discrimination in the mouse. Ann Trop Med Parasitol, 74(2): 145-150.
48. Innes E A (1997). Toxoplasmosis: comparative species susceptibility and host immune response. Comp Immunol Microbiol Infect Dis, 20(2): 131-138.
49. James W H (2008). Evidence that mammalian sex ratios at birth are partially controlled by parental hormone levels around the time of conception. J Endocrinol, 198(1): 3-15.
50. James W H (2010). Potential solutions to problems posed by the offspring sex ratios of people with parasitic and viral infections. Folia Parasitol (Praha), 57(2): 114-120.
51. Kaňková S, Kodym P, Flegr J (2011). Direct evidence of Toxoplasma-induced changes in serum testosterone in mice. Exp Parasitol, 128(3): 181-183.
52. Kaňková S, Kodym P, Frynta D, Vavrinová R, Kubena A, Flegr J (2007b). Influence of latent toxoplasmosis on the secondary sex ratio in mice. Parasitology, 134(Pt 12): 1709-1717.
53. Kaňková Š, Sulc J, Flegr J (2010). Increased pregnancy weight gain in women with latent toxoplasmosis and RhD-positivity protection against this effect. Parasitology, 137(12): 1773-1779.
54. Kanková Š, Sulc J, Nouzová K, Fajfrlík K, Frynta D, Flegr J (2007a). Women infected with parasite Toxoplasma have more sons. Naturwissenschaften, 94(2): 122-127.
55. Kannan G, Moldovan K, Xiao J C, Yolken R H, Jones-Brando L, Pletnikov M V (2010). Toxoplasma gondii strain-dependent effects on mouse behaviour. Folia Parasitol (Praha), 57(2): 151-155.
56. Khaki A, Farzadi L, Ahmadi S, Ghadamkheir E, Khaki AA, shojaee S, Sahizadeh R (2011). Recovery of spermatogenesis by Allium cepa in Toxoplasma gondii infected rats. Afr. J. Pharm. Pharmacol, 5: 903-907.
57. King J A, De Oliveira W L, Patel N (2005). Deficits in testosterone facilitate enhanced fear response. Psychoneuroendocrinology, 30(4): 333-340.
58. Klein S L (2000). The effects of hormones on sex differences in infection: from genes to behavior. Neurosci Biobehav Rev, 24(6): 627-638.
59. Lamberton P H, Donnelly C A, Webster J P (2008). Specificity of the Toxoplasma gondii-altered behaviour to definitive versus nondefinitive host predation risk. Parasitology, 135(10): 1143-1150.
60. Lim A, Kumar V, Hari Dass S A, Vyas A (2013). Toxoplasma gondii infection enhances testicular steroidogenesis in rats. Mol Ecol, 22(1): 102-110.
61. Lindová J, Kubena A A, Sturcová H, Krivohlavá R, Novotná M, Rubesová A, Havlícek J, Kodym P, Flegr J (2010). Pattern of money allocation in experimental games supports the stress hypothesis of gender differences in Toxoplasma gondii-induced behavioural changes. Folia Parasitol (Praha), 57(2): 136-142.
62. Lindová J, Novotná M, Havlícek J, Jozífková E, Skallová A, Kolbeková P, Hodný Z, Kodym P, Flegr J (2006). Gender differences in behavioural changes induced by latent toxoplasmosis. Int J Parasitol, 36(14): 1485-1492.
63. Liu S G, Qin C, Yao Z J, Wang D (2006). Study on the transmission of Toxoplasma gondii by semen in rabbits. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi, 24(3): 166-170.
64. Lopes W D, Rodriguez J D, Souza F A, dos Santos T R, dos Santos R S, Rosanese W M, Lopes W R, Sakamoto C A, da Costa A J (2013). Sexual transmission of Toxoplasma gondii in sheep. Vet Parasitol, 195(1-2): 47-56.
65. Lutchmaya S, Baron-Cohen S, Raggatt P, Knickmeyer R, Manning J T (2004). 2nd to 4th digit ratios, fetal testosterone and estradiol. Early Hum Dev, 77(1-2): 23-28.
66. Mack D G, Johnson J J, Roberts F, Roberts C W, Estes R G, David C, Grumet F C, McLeod R (1999). HLA-class II genes modify outcome of Toxoplasma gondii infection. Int J Parasitol, 29(9): 1351-1358.
67. McConkey G A, Martin H L, Bristow G C, Webster J P (2013). Toxoplasma gondii infection and behaviour-location, location, location? J Exp Biol, 216(Pt 1): 113-119.
68. Miller C M, Boulter N R, Ikin R J, Smith N C (2009). The immunobiology of the innate response to Toxoplasma gondii. Int J Parasitol, 39(1): 23-39.
69. Mitra R, Sapolsky R M, Vyas A (2013). Toxoplasma gondii infection induces dendritic retraction in basolateral amygdala accompanied by reduced corticosterone secretion. Dis Model Mech, 6(2): 516-520.
70. Montoya E R, Terburg D, Bos P A, van Honk J (2012). Testosterone, cortisol, and serotonin as key regulators of social aggression: A review and theoretical perspective. Motiv Emot, 36(1): 65-73.
71. Montoya J G, Liesenfeld O (2004). Toxoplasmosis. Lancet, 363(9425): 1965-1976.
72. Mougeot F, Redpath S M, Piertney S B (2006). Elevated spring testosterone increases parasite intensity in male red grouse. Behav Ecol, 17(1): 117-125.
73. Muehlenbein M P, Bribiescas R G (2005). Testosterone-mediated immune functions and male life histories. Am J Hum Biol, 17(5): 527-558.
74. Nava-Castro K, Hernández-Bello R, Muñiz-Hernández S, Camacho-Arroyo I, Morales-Montor J (2012). Sex steroids, immune system, and parasitic infections: facts and hypotheses. Ann N Y Acad Sci, 1262(1): 16-26.
75. Novotná M, Havlícek J, Smith A P, Kolbeková P, Skallová A, Klose J, Gasová Z, Písacka M, Sechovská M, Flegr J (2008). Toxoplasma and reaction time: role of toxoplasmosis in the origin, preservation and geographical distribution of Rh blood group polymorphism. Parasitology, 135(11): 1253-1261.
76. Oktenli C, Doganci L, Ozgurtas T, Araz R E, Tanyuksel M, Musabak U, Sanisoglu S Y, Yesilova Z, Erbil M K, Inal A (2004). Transient hypogonadotrophic hypogonadism in males with acute toxoplasmosis: suppressive effect of interleukin-1 beta on the secretion of GnRH. Hum Reprod, 19(4): 859-866.
77. Petitto J M, McCarthy D B, Rinker C M, Huang Z, Getty T (1997). Modulation of behavioral and neurochemical measures of forebrain dopamine function in mice by species-specific interleukin-2. J Neuroimmunol, 73(1-2): 183-190.
78. Prandovszky E, Gaskell E, Martin H, Dubey J P, Webster J P, McConkey G A (2011). The neurotropic parasite Toxoplasma gondii increases dopamine metabolism. PLoS ONE, 6(9): e23866.
79. Prast H, Philippu A (2001). Nitric oxide as modulator of neuronal function. Prog Neurobiol, 64(1): 51-68.
80. Robert-Gangneux F, Dardé ML (2012). Epidemiology of and diagnostic strategies for toxoplasmosis. Clin Microbiol Rev, 25(2): 264-296.
81. Roberts C W, Walker W, Alexander J (2001). Sex-associated hormones and immunity to protozoan parasites. Clin Microbiol Rev, 14(3): 476-488.
82. Schwarcz R, Hunter C A (2007). Toxoplasma gondii and schizophrenia: linkage through astrocyte-derived kynurenic acid? Schizophr Bull, 33(3): 652-653.
83. Shirbazou S, Abasian L, Meymand F T (2011). Effects of Toxoplasma gondii infection on plasma testosterone and cortisol level and stress index on patients referred to Sina hospital, Tehran. Jundishapur J Microbiol, 4: 167-173.
84. Skallová A, Kodym P, Frynta D, Flegr J (2006). The role of dopamine in Toxoplasma-induced behavioural alterations in mice: an ethological and ethopharmacological study. Parasitology, 133(Pt 5): 525-535.
85. Soh L J, Vasudevan A, Vyas A (2013). Infection with Toxoplasma gondii does not elicit predator aversion in male mice nor increase their attractiveness in terms of mate choice. Parasitol Res, 112(9): 3373-3378.
86. Stahl W, Dias J A, Turek G (1985). Hypothalamic-adenohypophyseal origin of reproductive failure in mice following chronic infection with Toxoplasma gondii. Proc Soc Exp Biol Med, 178(2): 246-249.
87. Stahl W, Dias J A, Turek G, Kaneda Y (1995). Etiology of ovarian dysfunction in chronic murine toxoplasmosis. Parasitol Res, 81(2): 114-120.
88. Stahl W, Kaneda Y (1998a). Impaired thyroid function in murine toxoplasmosis. Parasitology, 117(Pt 3): 217-222.
89. Stahl W, Kaneda Y (1998b). Aetiology of thyroidal dysfunction in murine toxoplasmosis. Parasitology, 117(Pt 3): 223-227.
90. Stahl W, Kaneda Y, Noguchi T (1994). Reproductive failure in mice chronically infected with Toxoplasma gondii. Parasitol Res, 80(1): 22-28.
91. Stibbs H H (1985). Changes in brain concentrations of catecholamines and indoleamines in Toxoplasma gondii infected mice. Ann Trop Med Parasitol, 79(2): 153-157.
92. Stutz A, Kessler H, Kaschel M E, Meissner M, Dalpke A H (2012). Cell invasion and strain dependent induction of suppressor of cytokine signaling-1 by Toxoplasma gondii. Immunobiology, 217(1): 28-36.
93. Sullivan W J Jr, Jeffers V (2012). Mechanisms of Toxoplasma gondii persistence and latency. FEMS Microbiol Rev, 36(3): 717-733.
94. Suzuki Y, Wong S Y, Grumet F C, Fessel J, Montoya J G, Zolopa A R, Portmore A, Schumacher-Perdreau F, Schrappe M, Köppen S, Ruf B, Brown B W, Remington J S (1996). Evidence for genetic regulation of susceptibility to toxoplasmic encephalitis in AIDS patients. J Infect Dis, 173(1): 265-268.
95. Tenter A M, Heckeroth A R, Weiss L M (2000). Toxoplasma gondii: from animals to humans. Int J Parasitol, 30(12-13): 1217-1258.
96. van Honk J, Peper J S, Schutter D J (2005). Testosterone reduces unconscious fear but not consciously experienced anxiety: implications for the disorders of fear and anxiety. Biol Psychiatry, 58(3): 218-225.
97. Vyas A (2013). Parasite-augmented mate choice and reduction in innate fear in rats infected by Toxoplasma gondii. J Exp Biol, 216(Pt 1): 120-126.
98. Vyas A, Kim S K, Giacomini N, Boothroyd J C, Sapolsky R M (2007). Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors. Proc Natl Acad Sci USA, 104(15): 6442-6447.
99. Wagner M S, Wajner SM, Maia A L (2008). The role of thyroid hormone in testicular development and function. J Endocrinol, 199(3): 351-365.
100. Wanderley F S, Porto WJ, Câmara D R, da Cruz N L, Feitosa B C, Freire R L, de Moraes E P, Mota R A (2013). Experimental vaginal infection of goats with semen contaminated with the "CPG" strain of Toxoplasma gondii. J Parasitol, 99(4): 610-613.
101. Webster J P (1994). The effect of Toxoplasma gondii and other parasites on activity levels in wild and hybrid Rattus norvegicus. Parasitology, 109(Pt 5): 583-589.
102. Webster J P (2007). The effect of Toxoplasma gondii on animal behavior: playing cat and mouse. Schizophr Bull, 33(3): 752-756.
103. Webster J P, Kaushik M, Bristow G C, McConkey G A (2013). Toxoplasma gondii infection, from predation to schizophrenia: can animal behaviour help us understand human behaviour? J Exp Biol, 216(Pt 1): 99-112.
104. West A R, Galloway M P, Grace A A (2002). Regulation of striatal dopamine neurotransmission by nitric oxide: effector pathways and signaling mechanisms. Synapse, 44(4): 227-245.
105. Witting P A (1979). Learning capacity and memory of normal and Toxoplasma-infected laboratory rats and mice. Z Parasitenkd, 61(1): 29-51.
106. Worth A R, Lymbery A J, Thompson R C (2013). Adaptive host manipulation by Toxoplasma gondii: fact or fiction? Trends Parasitol, 29(4): 150-155.
107. Xiao J, Buka S L, Cannon T D, Suzuki Y, Viscidi R P, Torrey E F, Yolken R H (2009). Serological pattern consistent with infection with type I Toxoplasma gondii in mothers and risk of psychosis among adult offspring. Microbes Infect, 11(13): 1011-1018.
108. Xiao J, Jones-Brando L, Talbot C C Jr, Yolken R H (2011). Differential effects of three canonical Toxoplasma strains on gene expression in human neuroepithelial cells. Infect Immun, 79(3): 1363-1373.
109. Xiao J, Kannan G, Jones-Brando L, Brannock C, Krasnova I N, Cadet J L, Pletnikov M, Yolken R H (2012). Sex-specific changes in gene expression and behavior induced by chronic Toxoplasma infection in mice. Neuroscience, 206: 39-48.
110. Xiao J, Li Y, Jones-Brando L, Yolken R H (2013). Abnormalities of neurotransmitter and neuropeptide systems in human neuroepithelioma cells infected by three Toxoplasma strains. J Neural Transm, 120(12): 1631-1639.
111. Zalcman S, Green-Johnson J M, Murray L, Nance D M, Dyck D, Anisman H, Greenberg A H (1994). Cytokine-specific central monoamine alterations induced by interleukin-1, -2 and-6. Brain Res, 643(1-2): 40-49.
112. Zghair KH, AL-Qadhi BN, Mahmood SH (2013). The effect of toxoplasmosis on the level of some sex hormones in males blood donors in Baghdad. J Parasit Dis. doi: 10. 1007/s12639-013-0382-6.