Toxoplasma gondii infection enhances testicular steroidogenesis in rats

Molecular Ecology

Volumn 22, Issue 1, 2013, Pages 102-110

  Lim, Audrey ^a   Kumar, Vineet ^a   Hari Dass, Shantala A ^a   Vyas, Ajai ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

anti predator behaviour; behavioural manipulation; mate choice; parasitism; sexual transmission; testosterone; trophic transmission

Indexed keywords

LUTEINIZING HORMONE RECEPTOR; MESSENGER RNA; TESTOSTERONE;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BIOSYNTHESIS; BLOOD; FEAR; GENE EXPRESSION REGULATION; GENETICS; HOST PARASITE INTERACTION; MALE; METABOLISM; ORCHIECTOMY; PARASITOLOGY; RAT; TESTIS; TOXOPLASMA; TOXOPLASMOSIS; WISTAR RAT;

ANIMALS; BEHAVIOR, ANIMAL; FEAR; GENE EXPRESSION REGULATION; HOST-PARASITE INTERACTIONS; MALE; ORCHIECTOMY; RATS; RATS, WISTAR; RECEPTORS, LH; RNA, MESSENGER; TESTIS; TESTOSTERONE; TOXOPLASMA; TOXOPLASMOSIS, ANIMAL;

PROTOZOA; RATTUS; TOXOPLASMA GONDII;

EID: 84872873503     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12042     Document Type: Article

References (42)

1. Able DJ, (1996) The contagion indicator hypothesis for parasite-mediated sexual selection. Proceedings of the National Academy of Sciences of the United States of America, 93, 2229-2233. (Pubitemid 26079911)
2. Aikey JL, Nyby JG, Anmuth DM, James PJ, (2002) Testosterone rapidly reduces anxiety in male house mice (Mus musculus). Hormones and Behavior, 42, 448-460. (Pubitemid 36071179)
3. Andersson M, Simmons LW, (2006) Sexual selection and mate choice. Trends in Ecology & Evolution, 21, 296-302. (Pubitemid 43850058)
4. Ardia DR, Broughton DR, Gleicher MJ, (2010) Short-term exposure to testosterone propionate leads to rapid bill color and dominance changes in zebra finches. Hormones and Behavior, 58, 526-532.
5. Azhar S, Reaven E, (2007) Regulation of Leydig cell cholesterol metabolism. In: Contemporary Endocrinology: The Leydig Cell in Health and Disease (eds, Payne AH, Hardy MP,), pp. 135-148. Humana Press Inc., Totowa, New Jersey.
6. Berdoy M, Webster JP, Macdonald DW, (2000) Fatal attraction in rats infected with Toxoplasma gondii. Proceedings. Biological sciences, 267, 1591-1594. (Pubitemid 30624132)
7. Bonisoli-Alquati A, Matteo A, Ambrosini R, et al,. (2011) Effects of egg testosterone on female mate choice and male sexual behavior in the pheasant. Hormones and Behavior, 59, 75-82.
8. Bottoni L, Massa R, Lea RW, Sharp PJ, (1993) Mate choice and reproductive success in the red-legged partridge (Alectoris rufa). Hormones and Behavior, 27, 308-317. (Pubitemid 23281953)
9. Chang C, Chen YT, Yeh SD, et al,. (2004) Infertility with defective spermatogenesis and hypotestosteronemia in male mice lacking the androgen receptor in Sertoli cells. Proceedings of the National Academy of Sciences of the United States of America, 101, 6876-6881. (Pubitemid 38596411)
10. Chen H, Ge RS, Zirkin BR, (2009) Leydig cells: from stem cells to aging. Molecular and Cellular Endocrinology, 306, 9-16.
11. Dass SA, Vasudevan A, Dutta D, et al,. (2011) Protozoan parasite Toxoplasma gondii manipulates mate choice in rats by enhancing attractiveness of males. PLoS One, 6, e27229.
12. Easterbrook JD, Kaplan JB, Glass GE, Pletnikov MV, Klein SL, (2007) Elevated testosterone and reduced 5-HIAA concentrations are associated with wounding and hantavirus infection in male Norway rats. Hormones and Behavior, 52, 474-481. (Pubitemid 47488259)
13. Ezenwa VO, Ekernas LS, Creel S, (2011) Unravelling complex associations between testosterone and parasite infection in the wild. Functional Ecology, 26, 123-133.
14. Flegr J, Lindova J, Kodym P, (2008) Sex-dependent toxoplasmosis- associated differences in testosterone concentration in humans. Parasitology, 135, 427-431. (Pubitemid 351651639)
15. Folstad I, Karter AK, (1992) Parasites, bright males and the immunocompetence handicap. American Society of Naturalists, 139, 603-622.
16. Hamilton WD, Zuk M, (1982) Heritable true fitness and bright birds: a role for parasites? Science, 218, 384-387. (Pubitemid 13283877)
17. Hermans EJ, Putman P, Baas JM, Koppeschaar HP, van Honk J, (2006) A single administration of testosterone reduces fear-potentiated startle in humans. Biological Psychiatry, 59, 872-874.
18. Hodkova H, Kodym P, Flegr J, (2007) Poorer results of mice with latent toxoplasmosis in learning tests: impaired learning processes or the novelty discrimination mechanism? Parasitology, 134, 1329-1337. (Pubitemid 47236796)
19. House PK, Vyas A, Sapolsky R, (2011) Predator cat odors activate sexual arousal pathways in brains of Toxoplasma gondii infected rats. PLoS One, 6, e23277.
20. Hrda S, Votypka J, Kodym P, Flegr J, (2000) Transient nature of Toxoplasma gondii-induced behavioral changes in mice. Journal of Parasitology, 86, 657-663. (Pubitemid 30646575)
21. Kankova S, Kodym P, Flegr J, (2011) Direct evidence of Toxoplasma-induced changes in serum testosterone in mice. Experimental Parasitology, 128, 181-183.
22. Kavaliers M, Choleris E, Colwell DD, (2001) Brief exposure to female odors "emboldens" male mice by reducing predator-induced behavioral and hormonal responses. Hormones and Behavior, 40, 497-509. (Pubitemid 33116604)
23. Kavaliers M, Choleris E, Pfaff DW, (2005) Genes, odours and the recognition of parasitized individuals by rodents. Trends in Parasitology, 21, 423-429. (Pubitemid 41116718)
24. King JA, De Oliveira WL, Patel N, (2005) Deficits in testosterone facilitate enhanced fear response. Psychoneuroendocrinology, 30, 333-340. (Pubitemid 40188188)
25. Lafferty KD, (1999) The evolution of trophic transmission. Parasitology Today, 15, 111-115. (Pubitemid 29341191)
26. Longpre KM, Katz LS, (2011) Estrous female goats use testosterone- dependent cues to assess mates. Hormones and Behavior, 59, 98-104.
27. Mitra R, Sapolsky RM, (2012) Short-term enrichment makes male rats more attractive, more defensive and alters hypothalamic neurons. PLoS One, 7, e36092.
28. Moshkin M, Gerlinskaya L, Morozova O, Bakhvalova V, Evsikov V, (2002) Behaviour, chemosignals and endocrine functions in male mice infected with tick-borne encephalitis virus. Psychoneuroendocrinology, 27, 603-608. (Pubitemid 34310621)
29. Parker KL, Schimmer BP, (1995) Transcriptional regulation of the genes encoding the cytochrome P-450 steroid hydroxylases. Vitamins and Hormones, 51, 339-370.
30. Payne AH, (2007) Steroidogenic enzymes in leydig cells. In: Contemporary Endocrinology: The Leydig Cell in Health and Disease (eds, Payne AH, Hardy MP,), pp. 157-171. Humana Press Inc., Totowa, New Jersey.
31. Payne AH, Hales DB, (2004) Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocrine Reviews, 25, 947-970. (Pubitemid 39657774)
32. Pfaffl MW, Horgan GW, Dempfle L, (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Research, 30, e36.
33. Poulin R, (1995) "Adaptive" changes in the behaviour of parasitized animals: a critical review. International Journal for Parasitology, 25, 1371-1383. (Pubitemid 3010442)
34. Roney JR, Hanson KN, Durante KM, Maestripieri D, (2006) Reading men's faces: women's mate attractiveness judgments track men's testosterone and interest in infants. Proceedings. Biological sciences, 273, 2169-2175. (Pubitemid 44318306)
35. Sapolsky RM, (1985) Stress-induced suppression of testicular function in the wild baboon: role of glucocorticoids. Endocrinology, 116, 2273-2278. (Pubitemid 15098055)
36. Stocco DM, (2000) Intramitochondrial cholesterol transfer. Biochimica et Biophysica Acta, 1486, 184-197. (Pubitemid 30336800)
37. Taylor GT, Haller J, Regan D, (1982) Female rats prefer an area vacated by a high testosterone male. Physiology & Behavior, 28, 953-958. (Pubitemid 12021472)
38. Vyas A, Sapolsky R, (2010) Manipulation of host behaviour by Toxoplasma gondii: what is the minimum a proposed proximate mechanism should explain? Folia Parasitologica, 57, 88-94.
39. Vyas A, Kim SK, Giacomini N, Boothroyd JC, Sapolsky RM, (2007) Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors. Proceedings of the National Academy of Sciences of the United States of America, 104, 6442-6447. (Pubitemid 47186113)
40. Webster JP, McConkey GA, (2010) Toxoplasma gondii-altered host behaviour: clues as to mechanism of action. Folia Parasitologica, 57, 95-104.
41. Wingfield JC, Jacobs J, Hillgarth N, (1997) Ecological constraints and the evolution of hormone-behavior interrelationships. Annals of the New York Academy of Sciences, 807, 22-41. (Pubitemid 27135484)
42. Zuk M, Kolluru GR, (1998) Exploitation of sexual signals by predators and parasitoids. The Quarterly Review of Biology, 73, 415-438. (Pubitemid 128652457)