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Toxoplasma, testosterone, and behavior manipulation: the role of parasite strain, host variations, and intensity of infection |
Amir ABDOLI1,2,*( ) |
1. Department of Parasitology, Faculty of Medical Sciences, Kashan University of Medical Sciences, Kashan, Iran
2. Department of Parasitology, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran |
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Abstract Toxoplasma gondii is an intracellular parasite involved in the etiology of various behavioral and hormonal alterations in humans and rodents. Various mechanisms, including induction changes of testosterone production, have been proposed in the etiology of behavioral alterations during T. gondii infection. However, controversy remains about the effects of T. gondii infection on testosterone production; in some studies, increased levels of testosterone were reported, whereas other studies reported decreased levels. This is a significant point, because testosterone has been shown to play important roles in various processes, from reproduction to fear and behavior. This contradiction seems to indicate that different factors—primarily parasite strains and host variations—have diverse effects on the intensity of T. gondii infection, which consequently has diverse effects on testosterone production and behavioral alterations. This paper reviews the role of parasite strains, host variations, and intensity of T. gondii infection on behavioral alterations and testosterone production, as well as the role of testosterone in the etiology of these alterations during toxoplasmosis.
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Toxoplasma gondii
testosterone
behavior manipulation
parasite strain
host variations
intensity of infection
neurologic and psychiatric disorders
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Corresponding Author(s):
Amir ABDOLI
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Issue Date: 13 May 2014
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| 1 |
AbdoliA (2013). Toxoplasma gondii and neuropsychiatric diseases: strain hypothesis. Neurol Sci, 34(9): 1697–1698
doi: 10.1007/s10072-012-1264-x pmid: 23224584
|
| 2 |
AbdoliA, DalimiA, ArbabiM, GhaffarifarF (2014). Neuropsychiatric manifestations of latent toxoplasmosis on mothers and their offspring. J Matern Fetal Neonatal Med,doi: 10.3109/14767058.2013.858685
|
| 3 |
AbdoliA, DalimiA, MovahedinM (2012). Impaired reproductive function of male rats infected with Toxoplasma gondii. Andrologia, 44(Suppl 1): 679–687
doi: 10.1111/j.1439-0272.2011.01249.x pmid: 22098674
|
| 4 |
AchermannJ C, JamesonJ L (1999). Fertility and infertility: genetic contributions from the hypothalamic-pituitary-gonadal axis. Mol Endocrinol, 13(6): 812–818
doi: 10.1210/me.13.6.812 pmid: 10379880
|
| 5 |
AikeyJ L, NybyJ G, AnmuthD M, JamesP J (2002). Testosterone rapidly reduces anxiety in male house mice (Mus musculus). Horm Behav, 42(4): 448–460
doi: 10.1006/hbeh.2002.1838 pmid: 12488111
|
| 6 |
AlonsoR, ChaudieuI, DiorioJ, KrishnamurthyA, QuirionR, BoksaP (1993). Interleukin-2 modulates evoked release of [3H]dopamine in rat cultured mesencephalic cells. J Neurochem, 61(4): 1284–1290
doi: 10.1111/j.1471-4159.1993.tb13620.x pmid: 8376986
|
| 7 |
ArantesT P, LopesW D, FerreiraR M, PieroniJ S, PintoV M, SakamotoC A, CostaA J (2009). Toxoplasma gondii: evidence for the transmission by semen in dogs. Exp Parasitol, 123(2): 190–194
doi: 10.1016/j.exppara.2009.07.003 pmid: 19622353
|
| 8 |
BerdoyM, WebsterJ P, MacdonaldD W (1995). Parasite-altered behaviour: is the effect of Toxoplasma gondii on Rattus norvegicus specific? Parasitology, 111(Pt 4): 403–409
doi: 10.1017/S0031182000065902 pmid: 11023404
|
| 9 |
BerdoyM, WebsterJ P, MacdonaldD W (2000). Fatal attraction in rats infected with Toxoplasma gondii. Proc Biol Sci, 267(1452): 1591–1594
doi: 10.1098/rspb.2000.1182 pmid: 11007336
|
| 10 |
BoothA, GrangerD A, MazurA, KivlighanK T (2006). Testosterone and social behavior. Soc Forces, 85(1): 167–191
doi: 10.1353/sof.2006.0116
|
| 11 |
ChoksiN Y, JahnkeG D, St HilaireC, ShelbyM (2003). Role of thyroid hormones in human and laboratory animal reproductive health. Birth Defects Res B Dev Reprod Toxicol, 68(6): 479–491
doi: 10.1002/bdrb.10045 pmid: 14745982
|
| 12 |
CoxR M, John‐AlderH B (2007). Increased mite parasitism as a cost of testosterone in male striped plateau lizards Sceloporus virgatus. Funct Ecol, 21(2): 327–334
doi: 10.1111/j.1365-2435.2007.01251.x
|
| 13 |
DalimiA, AbdoliA (2012). Latent toxoplasmosis and human. Iran J Parasitol, 7(1): 1–17
pmid: 23133466
|
| 14 |
DalimiA, AbdoliA (2013). Toxoplasma gondii and male reproduction impairment: a new aspect of toxoplasmosis research. Jundishapur J Microbiol, 6(8): e7184
doi: 10.5812/jjm.7184
|
| 15 |
DardéM L (2008). Toxoplasma gondii, “new” genotypes and virulence. Parasite, 15(3): 366–371
doi: 10.1051/parasite/2008153366 pmid: 18814708
|
| 16 |
DassS A, VasudevanA, DuttaD, SohL J, SapolskyR M, VyasA (2011). Protozoan parasite Toxoplasma gondii manipulates mate choice in rats by enhancing attractiveness of males. PLoS ONE, 6(11): e27229
doi: 10.1371/journal.pone.0027229 pmid: 22073295
|
| 17 |
de MoraesE P, BatistaA M, FariaE B, FreireR L, FreitasA C, SilvaM A, BragaV A, MotaR A (2010). Experimental infection by Toxoplasma gondii using contaminated semen containing different doses of tachyzoites in sheep. Vet Parasitol, 170(3–4): 318–322
doi: 10.1016/j.vetpar.2010.02.017 pmid: 20227187
|
| 18 |
DominguezJ M, HullE M (2005). Dopamine, the medial preoptic area, and male sexual behavior. Physiol Behav, 86(3): 356–368
doi: 10.1016/j.physbeh.2005.08.006 pmid: 16135375
|
| 19 |
DubeyJ P, FerreiraL R, MartinsJ, McLeodR (2012). Oral oocyst-induced 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
doi: 10.1017/S0031182011001673 pmid: 22078010
|
| 20 |
DubeyJ P, FrenkelJ 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
doi: 10.1016/S0304-4017(97)00227-6 pmid: 9652380
|
| 21 |
EiseneggerC, HaushoferJ, FehrE (2011). The role of testosterone in social interaction. Trends Cogn Sci, 15(6): 263–271
doi: 10.1016/j.tics.2011.04.008 pmid: 21616702
|
| 22 |
FabianiS, PintoB, BruschiF (2013). Toxoplasmosis and neuropsychiatric diseases: can serological studies establish a clear relationship? Neurol Sci, 34(4): 417–425
doi: 10.1007/s10072-012-1197-4 pmid: 23010876
|
| 23 |
FlegrJ (2007). Effects of toxoplasma on human behavior. Schizophr Bull, 33(3): 757–760
doi: 10.1093/schbul/sbl074 pmid: 17218612
|
| 24 |
FlegrJ (2010). Influence of latent toxoplasmosis on the phenotype of intermediate hosts. Folia Parasitol (Praha), 57(2): 81–87
pmid: 20608469
|
| 25 |
FlegrJ (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
doi: 10.1242/jeb.073635 pmid: 23225875
|
| 26 |
FlegrJ (2013b). How and why Toxoplasma makes us crazy. Trends Parasitol, 29(4): 156–163
doi: 10.1016/j.pt.2013.01.007 pmid: 23433494
|
| 27 |
FlegrJ, HruskovýM, HodnáZ, NovotnáM, HanusováJ (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
doi: 10.1017/S0031182005007316 pmid: 15977898
|
| 28 |
FlegrJ, LindováJ, KodymP (2008a). Sex-dependent toxoplasmosis-associated differences in testosterone concentration in humans. Parasitology, 135(4): 427–431
doi: 10.1017/S0031182007004064 pmid: 18205984
|
| 29 |
FlegrJ, LindováJ, PivoñkováV, HavlícekJ (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
doi: 10.1002/ajpa.20888 pmid: 18615572
|
| 30 |
FlegrJ, NovotnáM, LindováJ, HavlícekJ (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
pmid: 18766148
|
| 31 |
GaskellE A, SmithJ E, PinneyJ W, WestheadD R, McConkeyG A (2009). A unique dual activity amino acid hydroxylase in Toxoplasma gondii. PLoS ONE, 4(3): e4801
doi: 10.1371/journal.pone.0004801 pmid: 19277211
|
| 32 |
GatkowskaJ, WieczorekM, DziadekB, DzitkoK, DlugonskaH (2013). Sex-dependent neurotransmitter level changes in brains of Toxoplasma gondii infected mice. Exp Parasitol, 133(1): 1–7
doi: 10.1016/j.exppara.2012.10.005 pmid: 23098668
|
| 33 |
GrearD A, PerkinsS E, HudsonP J (2009). Does elevated testosterone result in increased exposure and transmission of parasites? Ecol Lett, 12(6): 528–537
doi: 10.1111/j.1461-0248.2009.01306.x pmid: 19392718
|
| 34 |
GroërMW, YolkenRH, XiaoJC, BecksteadJW, FuchsD, MohapatraSS, SeyfangA, PostolacheTT (2011). Prenatal depression and anxiety in Toxoplasma gondii-positive women. Am J Obstet Gynecol, 204:433.e1–7
|
| 35 |
HayJ, AitkenP P, GrahamD I (1984). Toxoplasma infection and response to novelty in mice. Z Parasitenkd, 70(5): 575–588
doi: 10.1007/BF00926588 pmid: 6506841
|
| 36 |
HayJ, HutchisonW M, AitkenP P, GrahamD 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
pmid: 6660954
|
| 37 |
HermansE J, PutmanP, BaasJ M, KoppeschaarH P, van HonkJ (2006). A single administration of testosterone reduces fear-potentiated startle in humans. Biol Psychiatry, 59(9): 872–874
doi: 10.1016/j.biopsych.2005.11.015 pmid: 16458259
|
| 38 |
HermesG, AjiokaJ W, KellyK A, MuiE, RobertsF, KaszaK, MayrT, KirisitsM J, WollmannR, FergusonD J, RobertsC W, HwangJ H, TrendlerT, KennanR P, SuzukiY, ReardonC, HickeyW F, ChenL, McLeodR (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
doi: 10.1186/1742-2094-5-48 pmid: 18947414
|
| 39 |
HillR D, GouffonJ S, SaxtonA M, SuC (2012). Differential gene expression in mice infected with distinct Toxoplasma strains. Infect Immun, 80(3): 968–974
doi: 10.1128/IAI.05421-11 pmid: 22144491
|
| 40 |
HodkováH, KodymP, FlegrJ (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
doi: 10.1017/S0031182007002673 pmid: 17445326
|
| 41 |
HodkováH, KolbekováP, SkallováA, LindováJ, FlegrJ (2007a). Higher perceived dominance in Toxoplasma infected men—a new evidence for role of increased level of testosterone in toxoplasmosis-associated changes in human behavior. Neuro Endocrinol Lett, 28(2): 110–114
pmid: 17435678
|
| 42 |
HönekoppJ, BartholdtL, BeierL, LiebertA (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
doi: 10.1016/j.psyneuen.2007.01.007 pmid: 17400395
|
| 43 |
HughesV L, RandolphS E (2001). Testosterone increases the transmission potential of tick-borne parasites. Parasitology, 123(Pt 4): 365–371
doi: 10.1017/S0031182001008599 pmid: 11676368
|
| 44 |
HullE M, DuJ, LorrainD S, MatuszewichL (1995). Extracellular dopamine in the medial preoptic area: implications for sexual motivation and hormonal control of copulation. J Neurosci, 15(11): 7465–7471
pmid: 7472498
|
| 45 |
HullE M, DuJ, LorrainD S, MatuszewichL (1997). Testosterone, preoptic dopamine, and copulation in male rats. Brain Res Bull, 44(4): 327–333
doi: 10.1016/S0361-9230(97)00211-6 pmid: 9370196
|
| 46 |
HullE M, MuschampJ W, SatoS (2004). Dopamine and serotonin: influences on male sexual behavior. Physiol Behav, 83(2): 291–307
pmid: 15488546
|
| 47 |
HutchisonW M, AitkenP P, WellsW P (1980). Chronic Toxoplasma infections and familiarity-novelty discrimination in the mouse. Ann Trop Med Parasitol, 74(2): 145–150
pmid: 7436599
|
| 48 |
InnesE A (1997). Toxoplasmosis: comparative species susceptibility and host immune response. Comp Immunol Microbiol Infect Dis, 20(2): 131–138
doi: 10.1016/S0147-9571(96)00038-0 pmid: 9208198
|
| 49 |
JamesW 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
doi: 10.1677/JOE-07-0446 pmid: 18577567
|
| 50 |
JamesW 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
pmid: 20608473
|
| 51 |
KaňkováS, KodymP, FlegrJ (2011). Direct evidence of Toxoplasma-induced changes in serum testosterone in mice. Exp Parasitol, 128(3): 181–183
doi: 10.1016/j.exppara.2011.03.014 pmid: 21458453
|
| 52 |
KaňkováS, KodymP, FryntaD, VavrinováR, KubenaA, FlegrJ (2007b). Influence of latent toxoplasmosis on the secondary sex ratio in mice. Parasitology, 134(Pt 12): 1709–1717
doi: 10.1017/S0031182007003253 pmid: 17651529
|
| 53 |
KaňkováŠ, SulcJ, FlegrJ (2010). Increased pregnancy weight gain in women with latent toxoplasmosis and RhD-positivity protection against this effect. Parasitology, 137(12): 1773–1779
doi: 10.1017/S0031182010000661 pmid: 20602855
|
| 54 |
KankováŠ, SulcJ, NouzováK, FajfrlíkK, FryntaD, FlegrJ (2007a). Women infected with parasite Toxoplasma have more sons. Naturwissenschaften, 94(2): 122–127
doi: 10.1007/s00114-006-0166-2 pmid: 17028886
|
| 55 |
KannanG, MoldovanK, XiaoJ C, YolkenR H, Jones-BrandoL, PletnikovM V (2010). Toxoplasma gondii strain-dependent effects on mouse behaviour. Folia Parasitol (Praha), 57(2): 151–155
pmid: 20608478
|
| 56 |
KhakiA, FarzadiL, AhmadiS, GhadamkheirE, KhakiAA, shojaeeS, SahizadehR (2011). Recovery of spermatogenesis by Allium cepa in Toxoplasma gondii infected rats. Afr. J. Pharm. Pharmacol, 5: 903–907
|
| 57 |
KingJ A, De OliveiraW L, PatelN (2005). Deficits in testosterone facilitate enhanced fear response. Psychoneuroendocrinology, 30(4): 333–340
doi: 10.1016/j.psyneuen.2004.09.005 pmid: 15694113
|
| 58 |
KleinS L (2000). The effects of hormones on sex differences in infection: from genes to behavior. Neurosci Biobehav Rev, 24(6): 627–638
doi: 10.1016/S0149-7634(00)00027-0 pmid: 10940438
|
| 59 |
LambertonP H, DonnellyC A, WebsterJ P (2008). Specificity of the Toxoplasma gondii-altered behaviour to definitive versus non-definitive host predation risk. Parasitology, 135(10): 1143–1150
doi: 10.1017/S0031182008004666 pmid: 18620624
|
| 60 |
LimA, KumarV, Hari DassS A, VyasA (2013). Toxoplasma gondii infection enhances testicular steroidogenesis in rats. Mol Ecol, 22(1): 102–110
doi: 10.1111/mec.12042 pmid: 23190313
|
| 61 |
LindováJ, KubenaA A, SturcováH, KrivohlaváR, NovotnáM, RubesováA, HavlícekJ, KodymP, FlegrJ (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
pmid: 20608476
|
| 62 |
LindováJ, NovotnáM, HavlícekJ, JozífkováE, SkallováA, KolbekováP, HodnýZ, KodymP, FlegrJ (2006). Gender differences in behavioural changes induced by latent toxoplasmosis. Int J Parasitol, 36(14): 1485–1492
doi: 10.1016/j.ijpara.2006.07.008 pmid: 16978630
|
| 63 |
LiuS G, QinC, YaoZ J, WangD (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
pmid: 17094613
|
| 64 |
LopesW D, RodriguezJ D, SouzaF A, dos SantosT R, dos SantosR S, RosaneseW M, LopesW R, SakamotoC A, da CostaA J (2013). Sexual transmission of Toxoplasma gondii in sheep. Vet Parasitol, 195(1–2): 47–56
doi: 10.1016/j.vetpar.2012.12.056 pmid: 23384578
|
| 65 |
LutchmayaS, Baron-CohenS, RaggattP, KnickmeyerR, ManningJ T (2004). 2nd to 4th digit ratios, fetal testosterone and estradiol. Early Hum Dev, 77(1–2): 23–28
doi: 10.1016/j.earlhumdev.2003.12.002 pmid: 15113628
|
| 66 |
MackD G, JohnsonJ J, RobertsF, RobertsC W, EstesR G, DavidC, GrumetF C, McLeodR (1999). HLA-class II genes modify outcome of Toxoplasma gondii infection. Int J Parasitol, 29(9): 1351–1358
doi: 10.1016/S0020-7519(99)00152-6 pmid: 10579423
|
| 67 |
McConkeyG A, MartinH L, BristowG C, WebsterJ P (2013). Toxoplasma gondii infection and behaviour- location, location, location? J Exp Biol, 216(Pt 1): 113–119
doi: 10.1242/jeb.074153 pmid: 23225873
|
| 68 |
MillerC M, BoulterN R, IkinR J, SmithN C (2009). The immunobiology of the innate response to Toxoplasma gondii. Int J Parasitol, 39(1): 23–39
doi: 10.1016/j.ijpara.2008.08.002 pmid: 18775432
|
| 69 |
MitraR, SapolskyR M, VyasA (2013). Toxoplasma gondii infection induces dendritic retraction in basolateral amygdala accompanied by reduced corticosterone secretion. Dis Model Mech, 6(2): 516–520
doi: 10.1242/dmm.009928 pmid: 23104989
|
| 70 |
MontoyaE R, TerburgD, BosP A, van HonkJ (2012). Testosterone, cortisol, and serotonin as key regulators of social aggression: A review and theoretical perspective. Motiv Emot, 36(1): 65–73
doi: 10.1007/s11031-011-9264-3 pmid: 22448079
|
| 71 |
MontoyaJ G, LiesenfeldO (2004). Toxoplasmosis. Lancet, 363(9425): 1965–1976
doi: 10.1016/S0140-6736(04)16412-X pmid: 15194258
|
| 72 |
MougeotF, RedpathS M, PiertneyS B (2006). Elevated spring testosterone increases parasite intensity in male red grouse. Behav Ecol, 17(1): 117–125
doi: 10.1093/beheco/arj005
|
| 73 |
MuehlenbeinM P, BribiescasR G (2005). Testosterone-mediated immune functions and male life histories. Am J Hum Biol, 17(5): 527–558
doi: 10.1002/ajhb.20419 pmid: 16136532
|
| 74 |
Nava-CastroK, Hernández-BelloR, Muñiz-HernándezS, Camacho-ArroyoI, Morales-MontorJ (2012). Sex steroids, immune system, and parasitic infections: facts and hypotheses. Ann N Y Acad Sci, 1262(1): 16–26
doi: 10.1111/j.1749-6632.2012.06632.x pmid: 22823431
|
| 75 |
NovotnáM, HavlícekJ, SmithA P, KolbekováP, SkallováA, KloseJ, GasováZ, PísackaM, SechovskáM, FlegrJ (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
doi: 10.1017/S003118200800485X pmid: 18752708
|
| 76 |
OktenliC, DoganciL, OzgurtasT, ArazR E, TanyukselM, MusabakU, SanisogluS Y, YesilovaZ, ErbilM K, InalA (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
doi: 10.1093/humrep/deh161 pmid: 14990538
|
| 77 |
PetittoJ M, McCarthyD B, RinkerC M, HuangZ, GettyT (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
doi: 10.1016/S0165-5728(96)00196-8 pmid: 9058775
|
| 78 |
PrandovszkyE, GaskellE, MartinH, DubeyJ P, WebsterJ P, McConkeyG A (2011). The neurotropic parasite Toxoplasma gondii increases dopamine metabolism. PLoS ONE, 6(9): e23866
doi: 10.1371/journal.pone.0023866 pmid: 21957440
|
| 79 |
PrastH, PhilippuA (2001). Nitric oxide as modulator of neuronal function. Prog Neurobiol, 64(1): 51–68
doi: 10.1016/S0301-0082(00)00044-7 pmid: 11250062
|
| 80 |
Robert-GangneuxF, DardéM L (2012). Epidemiology of and diagnostic strategies for toxoplasmosis. Clin Microbiol Rev, 25(2): 264–296
doi: 10.1128/CMR.05013-11 pmid: 22491772
|
| 81 |
RobertsC W, WalkerW, AlexanderJ (2001). Sex-associated hormones and immunity to protozoan parasites. Clin Microbiol Rev, 14(3): 476–488
doi: 10.1128/CMR.14.3.476-488.2001 pmid: 11432809
|
| 82 |
SchwarczR, HunterC A (2007). Toxoplasma gondii and schizophrenia: linkage through astrocyte-derived kynurenic acid?Schizophr Bull, 33(3): 652–653
doi: 10.1093/schbul/sbm030 pmid: 17434932
|
| 83 |
ShirbazouS, AbasianL, MeymandF 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 |
SkallováA, KodymP, FryntaD, FlegrJ (2006). The role of dopamine in Toxoplasma-induced behavioural alterations in mice: an ethological and ethopharmacological study. Parasitology, 133(Pt 5): 525–535
doi: 10.1017/S0031182006000886 pmid: 16882355
|
| 85 |
SohL J, VasudevanA, VyasA (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
doi: 10.1007/s00436-013-3545-6 pmid: 23907633
|
| 86 |
StahlW, DiasJ A, TurekG (1985). Hypothalamic-adenohypophyseal origin of reproductive failure in mice following chronic infection with Toxoplasma gondii. Proc Soc Exp Biol Med, 178(2): 246–249
doi: 10.3181/00379727-178-42006 pmid: 3918311
|
| 87 |
StahlW, DiasJ A, TurekG, KanedaY (1995). Etiology of ovarian dysfunction in chronic murine toxoplasmosis. Parasitol Res, 81(2): 114–120
doi: 10.1007/BF00931615 pmid: 7731917
|
| 88 |
StahlW, KanedaY (1998a). Impaired thyroid function in murine toxoplasmosis. Parasitology, 117(Pt 3): 217–222
doi: 10.1017/S003118209800300X pmid: 9774785
|
| 89 |
StahlW, KanedaY (1998b). Aetiology of thyroidal dysfunction in murine toxoplasmosis. Parasitology, 117(Pt 3): 223–227
doi: 10.1017/S0031182098003035 pmid: 9774786
|
| 90 |
StahlW, KanedaY, NoguchiT (1994). Reproductive failure in mice chronically infected with Toxoplasma gondii. Parasitol Res, 80(1): 22–28
doi: 10.1007/BF00932619 pmid: 8153121
|
| 91 |
StibbsH H (1985). Changes in brain concentrations of catecholamines and indoleamines in Toxoplasma gondii infected mice. Ann Trop Med Parasitol, 79(2): 153–157
pmid: 2420295
|
| 92 |
StutzA, KesslerH, KaschelM E, MeissnerM, DalpkeA H (2012). Cell invasion and strain dependent induction of suppressor of cytokine signaling-1 by Toxoplasma gondii. Immunobiology, 217(1): 28–36
doi: 10.1016/j.imbio.2011.08.008 pmid: 22015046
|
| 93 |
SullivanW J Jr, JeffersV (2012). Mechanisms of Toxoplasma gondii persistence and latency. FEMS Microbiol Rev, 36(3): 717–733
doi: 10.1111/j.1574-6976.2011.00305.x pmid: 22091606
|
| 94 |
SuzukiY, WongS Y, GrumetF C, FesselJ, MontoyaJ G, ZolopaA R, PortmoreA, Schumacher-PerdreauF, SchrappeM, KöppenS, RufB, BrownB W, RemingtonJ S (1996). Evidence for genetic regulation of susceptibility to toxoplasmic encephalitis in AIDS patients. J Infect Dis, 173(1): 265–268
doi: 10.1093/infdis/173.1.265 pmid: 8537674
|
| 95 |
TenterA M, HeckerothA R, WeissL M (2000). Toxoplasma gondii: from animals to humans. Int J Parasitol, 30(12–13): 1217–1258
doi: 10.1016/S0020-7519(00)00124-7 pmid: 11113252
|
| 96 |
van HonkJ, PeperJ S, SchutterD 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
doi: 10.1016/j.biopsych.2005.04.003 pmid: 15939408
|
| 97 |
VyasA (2013). Parasite-augmented mate choice and reduction in innate fear in rats infected by Toxoplasma gondii. J Exp Biol, 216(Pt 1): 120–126
doi: 10.1242/jeb.072983 pmid: 23225874
|
| 98 |
VyasA, KimS K, GiacominiN, BoothroydJ C, SapolskyR 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
doi: 10.1073/pnas.0608310104 pmid: 17404235
|
| 99 |
WagnerM S, WajnerS M, MaiaA L (2008). The role of thyroid hormone in testicular development and function. J Endocrinol, 199(3): 351–365
doi: 10.1677/JOE-08-0218 pmid: 18728126
|
| 100 |
WanderleyF S, PortoW J, CâmaraD R, da CruzN L, FeitosaB C, FreireR L, de MoraesE P, MotaR A (2013). Experimental vaginal infection of goats with semen contaminated with the “CPG” strain of Toxoplasma gondii. J Parasitol, 99(4): 610–613
doi: 10.1645/12-126.1 pmid: 23391103
|
| 101 |
WebsterJ 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
doi: 10.1017/S0031182000076460 pmid: 7831094
|
| 102 |
WebsterJ P (2007). The effect of Toxoplasma gondii on animal behavior: playing cat and mouse. Schizophr Bull, 33(3): 752–756
doi: 10.1093/schbul/sbl073 pmid: 17218613
|
| 103 |
WebsterJ P, KaushikM, BristowG C, McConkeyG 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
doi: 10.1242/jeb.074716 pmid: 23225872
|
| 104 |
WestA R, GallowayM P, GraceA A (2002). Regulation of striatal dopamine neurotransmission by nitric oxide: effector pathways and signaling mechanisms. Synapse, 44(4): 227–245
doi: 10.1002/syn.10076 pmid: 11984858
|
| 105 |
WittingP A (1979). Learning capacity and memory of normal and Toxoplasma-infected laboratory rats and mice. Z Parasitenkd, 61(1): 29–51
doi: 10.1007/BF00927085 pmid: 543216
|
| 106 |
WorthA R, LymberyA J, ThompsonR C (2013). Adaptive host manipulation by Toxoplasma gondii: fact or fiction? Trends Parasitol, 29(4): 150–155
doi: 10.1016/j.pt.2013.01.004 pmid: 23415732
|
| 107 |
XiaoJ, BukaS L, CannonT D, SuzukiY, ViscidiR P, TorreyE F, YolkenR 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
doi: 10.1016/j.micinf.2009.07.007 pmid: 19638313
|
| 108 |
XiaoJ, Jones-BrandoL, TalbotC C Jr, YolkenR H (2011). Differential effects of three canonical Toxoplasma strains on gene expression in human neuroepithelial cells. Infect Immun, 79(3): 1363–1373
doi: 10.1128/IAI.00947-10 pmid: 21149591
|
| 109 |
XiaoJ, KannanG, Jones-BrandoL, BrannockC, KrasnovaI N, CadetJ L, PletnikovM, YolkenR H (2012). Sex-specific changes in gene expression and behavior induced by chronic Toxoplasma infection in mice. Neuroscience, 206: 39–48
doi: 10.1016/j.neuroscience.2011.12.051 pmid: 22240252
|
| 110 |
XiaoJ, LiY, Jones-BrandoL, YolkenR H (2013). Abnormalities of neurotransmitter and neuropeptide systems in human neuroepithelioma cells infected by three Toxoplasma strains. J Neural Transm, 120(12): 1631–1639
doi: 10.1007/s00702-013-1064-3 pmid: 23821371
|
| 111 |
ZalcmanS, Green-JohnsonJ M, MurrayL, NanceD M, DyckD, AnismanH, GreenbergA H (1994). Cytokine-specific central monoamine alterations induced by interleukin-1, -2 and-6. Brain Res, 643(1–2): 40–49
doi: 10.1016/0006-8993(94)90006-X pmid: 7518332
|
| 112 |
ZghairKH, AL-QadhiBN, MahmoodSH (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
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