REVIEW

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

  • Amir ABDOLI , 1,2
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  • 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

Received date: 25 Aug 2013

Accepted date: 10 Dec 2013

Published date: 01 Apr 2014

Copyright

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg

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.

Cite this article

Amir ABDOLI . Toxoplasma, testosterone, and behavior manipulation: the role of parasite strain, host variations, and intensity of infection[J]. Frontiers in Biology, 2014 , 9(2) : 151 -160 . DOI: 10.1007/s11515-014-1291-5

Acknowledgments

The author would like to sincerely thank Professor Jaroslav Flegr (Charles University, Prague, Czech Republic) for their excellent comments and helpful suggestions. The author also expresses his sincere thanks to the unknown referees for valuable criticisms and suggestions.
Compliance with ethics guidelines
Amir Abdoli declares that he has no conflict of interest.
ƒThis manuscript is a review article and does not involve a research protocol requiring approval by the relevant institutional review board or ethics committee.
1
AbdoliA (2013). Toxoplasma gondii and neuropsychiatric diseases: strain hypothesis. Neurol Sci, 34(9): 1697–1698

DOI PMID

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 PMID

4
AchermannJ C, JamesonJ L (1999). Fertility and infertility: genetic contributions from the hypothalamic-pituitary-gonadal axis. Mol Endocrinol, 13(6): 812–818

DOI PMID

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 PMID

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 PMID

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 PMID

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 PMID

9
BerdoyM, WebsterJ P, MacdonaldD W (2000). Fatal attraction in rats infected with Toxoplasma gondii. Proc Biol Sci, 267(1452): 1591–1594

DOI PMID

10
BoothA, GrangerD A, MazurA, KivlighanK T (2006). Testosterone and social behavior. Soc Forces, 85(1): 167–191

DOI

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 PMID

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

13
DalimiA, AbdoliA (2012). Latent toxoplasmosis and human. Iran J Parasitol, 7(1): 1–17

PMID

14
DalimiA, AbdoliA (2013). Toxoplasma gondii and male reproduction impairment: a new aspect of toxoplasmosis research. Jundishapur J Microbiol, 6(8): e7184

DOI

15
DardéM L (2008). Toxoplasma gondii, “new” genotypes and virulence. Parasite, 15(3): 366–371

DOI PMID

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 PMID

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 PMID

18
DominguezJ M, HullE M (2005). Dopamine, the medial preoptic area, and male sexual behavior. Physiol Behav, 86(3): 356–368

DOI PMID

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 PMID

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 PMID

21
EiseneggerC, HaushoferJ, FehrE (2011). The role of testosterone in social interaction. Trends Cogn Sci, 15(6): 263–271

DOI PMID

22
FabianiS, PintoB, BruschiF (2013). Toxoplasmosis and neuropsychiatric diseases: can serological studies establish a clear relationship? Neurol Sci, 34(4): 417–425

DOI PMID

23
FlegrJ (2007). Effects of toxoplasma on human behavior. Schizophr Bull, 33(3): 757–760

DOI PMID

24
FlegrJ (2010). Influence of latent toxoplasmosis on the phenotype of intermediate hosts. Folia Parasitol (Praha), 57(2): 81–87

PMID

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 PMID

26
FlegrJ (2013b). How and why Toxoplasma makes us crazy. Trends Parasitol, 29(4): 156–163

DOI PMID

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 PMID

28
FlegrJ, LindováJ, KodymP (2008a). Sex-dependent toxoplasmosis-associated differences in testosterone concentration in humans. Parasitology, 135(4): 427–431

DOI PMID

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 PMID

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

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 PMID

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 PMID

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 PMID

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 PMID

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

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 PMID

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 PMID

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 PMID

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 PMID

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

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 PMID

43
HughesV L, RandolphS E (2001). Testosterone increases the transmission potential of tick-borne parasites. Parasitology, 123(Pt 4): 365–371

DOI PMID

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

45
HullE M, DuJ, LorrainD S, MatuszewichL (1997). Testosterone, preoptic dopamine, and copulation in male rats. Brain Res Bull, 44(4): 327–333

DOI PMID

46
HullE M, MuschampJ W, SatoS (2004). Dopamine and serotonin: influences on male sexual behavior. Physiol Behav, 83(2): 291–307

PMID

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

48
InnesE A (1997). Toxoplasmosis: comparative species susceptibility and host immune response. Comp Immunol Microbiol Infect Dis, 20(2): 131–138

DOI PMID

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 PMID

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

51
KaňkováS, KodymP, FlegrJ (2011). Direct evidence of Toxoplasma-induced changes in serum testosterone in mice. Exp Parasitol, 128(3): 181–183

DOI PMID

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 PMID

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 PMID

54
KankováŠ, SulcJ, NouzováK, FajfrlíkK, FryntaD, FlegrJ (2007a). Women infected with parasite Toxoplasma have more sons. Naturwissenschaften, 94(2): 122–127

DOI PMID

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

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 PMID

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 PMID

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 PMID

60
LimA, KumarV, Hari DassS A, VyasA (2013). Toxoplasma gondii infection enhances testicular steroidogenesis in rats. Mol Ecol, 22(1): 102–110

DOI PMID

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

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 PMID

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

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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

71
MontoyaJ G, LiesenfeldO (2004). Toxoplasmosis. Lancet, 363(9425): 1965–1976

DOI PMID

72
MougeotF, RedpathS M, PiertneyS B (2006). Elevated spring testosterone increases parasite intensity in male red grouse. Behav Ecol, 17(1): 117–125

DOI

73
MuehlenbeinM P, BribiescasR G (2005). Testosterone-mediated immune functions and male life histories. Am J Hum Biol, 17(5): 527–558

DOI PMID

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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

79
PrastH, PhilippuA (2001). Nitric oxide as modulator of neuronal function. Prog Neurobiol, 64(1): 51–68

DOI PMID

80
Robert-GangneuxF, DardéM L (2012). Epidemiology of and diagnostic strategies for toxoplasmosis. Clin Microbiol Rev, 25(2): 264–296

DOI PMID

81
RobertsC W, WalkerW, AlexanderJ (2001). Sex-associated hormones and immunity to protozoan parasites. Clin Microbiol Rev, 14(3): 476–488

DOI PMID

82
SchwarczR, HunterC A (2007). Toxoplasma gondii and schizophrenia: linkage through astrocyte-derived kynurenic acid?Schizophr Bull, 33(3): 652–653

DOI PMID

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 PMID

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 PMID

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 PMID

87
StahlW, DiasJ A, TurekG, KanedaY (1995). Etiology of ovarian dysfunction in chronic murine toxoplasmosis. Parasitol Res, 81(2): 114–120

DOI PMID

88
StahlW, KanedaY (1998a). Impaired thyroid function in murine toxoplasmosis. Parasitology, 117(Pt 3): 217–222

DOI PMID

89
StahlW, KanedaY (1998b). Aetiology of thyroidal dysfunction in murine toxoplasmosis. Parasitology, 117(Pt 3): 223–227

DOI PMID

90
StahlW, KanedaY, NoguchiT (1994). Reproductive failure in mice chronically infected with Toxoplasma gondii. Parasitol Res, 80(1): 22–28

DOI PMID

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

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 PMID

93
SullivanW J Jr, JeffersV (2012). Mechanisms of Toxoplasma gondii persistence and latency. FEMS Microbiol Rev, 36(3): 717–733

DOI PMID

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 PMID

95
TenterA M, HeckerothA R, WeissL M (2000). Toxoplasma gondii: from animals to humans. Int J Parasitol, 30(12–13): 1217–1258

DOI PMID

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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

102
WebsterJ P (2007). The effect of Toxoplasma gondii on animal behavior: playing cat and mouse. Schizophr Bull, 33(3): 752–756

DOI PMID

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 PMID

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 PMID

105
WittingP A (1979). Learning capacity and memory of normal and Toxoplasma-infected laboratory rats and mice. Z Parasitenkd, 61(1): 29–51

DOI PMID

106
WorthA R, LymberyA J, ThompsonR C (2013). Adaptive host manipulation by Toxoplasma gondii: fact or fiction? Trends Parasitol, 29(4): 150–155

DOI PMID

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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

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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