The effect of adolescent testosterone on hippocampal BDNF and TrkB mRNA expression: Relationship with cell proliferation

BMC Neuroscience

Volumn 16, Issue 1, 2015, Pages

  Allen, Katherine M ^a,b,c   Purves Tyson, Tertia D ^a,b,c   Fung, Samantha J ^a,b,c   Shannon Weickert, Cynthia ^a,b,c  

^a SCHIZOPHRENIA RESEARCH INSTITUTE   (Australia)

^b NEUROSCIENCE RESEARCH AUSTRALIA   (Australia)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Adolescence; Neurogenesis; Neurotrophins; Schizophrenia; Sex steroids

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; MESSENGER RNA; TESTOSTERONE; BROXURIDINE; KI 67 ANTIGEN;

ADOLESCENT; ADULT; ANDROGEN THERAPY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; GONADECTOMY; HIPPOCAMPUS; MALE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; RAT; RHESUS MONKEY; SPRAGUE DAWLEY RAT; SUBGRANULAR ZONE; YOUNG ADULT; ANIMAL; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; HORMONE SUBSTITUTION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; ORCHIECTOMY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SPECIES DIFFERENCE; STEM CELL NICHE;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; BROMODEOXYURIDINE; HIPPOCAMPUS; HORMONE REPLACEMENT THERAPY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; KI-67 ANTIGEN; MACACA MULATTA; MALE; NEUROGENESIS; ORCHIECTOMY; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, TRKB; RNA, MESSENGER; SPECIES SPECIFICITY; STEM CELL NICHE; TESTOSTERONE;

EID: 84925126385     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/s12868-015-0142-x     Document Type: Article

References (66)

1. Galea LA, Wainwright SR, Roes MM, Duarte-Guterman P, Chow C, Hamson DK. Sex, hormones and neurogenesis in the hippocampus: hormonal modulation of neurogenesis and potential functional implications. J Neuroendocrinol. 2013;25(11):1039-61.
2. Spritzer MD, Galea LA. Testosterone and dihydrotestosterone, but not estradiol, enhance survival of new hippocampal neurons in adult male rats. Dev Neurobiol. 2007;67(10):1321-33.
3. Wainwright SR, Lieblich SE, Galea LA. Hypogonadism predisposes males to the development of behavioural and neuroplastic depressive phenotypes. Psychoneuroendocrinology. 2011;36(9):1327-41.
4. Allen KM, Fung SJ, Rothmond DA, Noble PL, Weickert CS. Gonadectomy increases neurogenesis in the male adolescent rhesus macaque hippocampus. Hippocampus. 2014;24(2):225-38.
5. Chen Z, Ye R, Goldman SA. Testosterone modulation of angiogenesis and neurogenesis in the adult songbird brain. Neuroscience. 2013;239:139-48.
6. Rasika S, Alvarez-Buylla A, Nottebohm F. BDNF mediates the effects of testosterone on the survival of new neurons in an adult brain. Neuron. 1999;22(1):53-62.
7. Aid T, Kazantseva A, Piirsoo M, Palm K, Timmusk T. Mouse and rat BDNF gene structure and expression revisited. J Neurosci Res. 2007;85(3):525-35.
8. Pruunsild P, Kazantseva A, Aid T, Palm K, Timmusk T. Dissecting the human BDNF locus: bidirectional transcription, complex splicing, and multiple promoters. Genomics. 2007;90(3):397-406.
9. Timmusk T, Palm K, Metsis M, Reintam T, Paalme V, Saarma M, et al. Multiple promoters direct tissue-specific expression of the rat BDNF gene. Neuron. 1993;10(3):475-89.
10. Wong J, Webster MJ, Cassano H, Weickert CS. Changes in alternative brain-derived neurotrophic factor transcript expression in the developing human prefrontal cortex. Eur J Neurosci. 2009;29(7):1311-22.
11. Bergami M, Rimondini R, Santi S, Blum R, Gotz M, Canossa M. Deletion of TrkB in adult progenitors alters newborn neuron integration into hippocampal circuits and increases anxiety-like behavior. Proc Natl Acad Sci U S A. 2008;105(40):15570-5.
12. Shelton DL, Sutherland J, Gripp J, Camerato T, Armanini MP, Phillips HS, et al. Human trks: molecular cloning, tissue distribution, and expression of extracellular domain immunoadhesins. J Neurosci. 1995;15(1 Pt 2):477-91.
13. Romanczyk TB, Weickert CS, Webster MJ, Herman MM, Akil M, Kleinman JE. Alterations in trkB mRNA in the human prefrontal cortex throughout the lifespan. Eur J Neurosci. 2002;15(2):269-80.
14. Luberg K, Wong J, Weickert CS, Timmusk T. Human TrkB gene: novel alternative transcripts, protein isoforms and expression pattern in the prefrontal cerebral cortex during postnatal development. J Neurochem. 2010;113(4):952-64.
15. Middlemas DS, Lindberg RA, Hunter T. trkB, a neural receptor protein-tyrosine kinase: evidence for a full-length and two truncated receptors. Mol Cell Biol. 1991;11(1):143-53.
16. Klein R, Conway D, Parada LF, Barbacid M. The trkB tyrosine protein kinase gene codes for a second neurogenic receptor that lacks the catalytic kinase domain. Cell. 1990;61(4):647-56.
17. Pan M, Zhang C. Stimulatory effect of gonadal hormones on fetal rat hippocampal neural proliferation requires neurotrophin receptor activation in vitro. Neurosci Lett. 2013;546:1-5.
18. Tervonen TA, Ajamian F, De Wit J, Verhaagen J, Castren E, Castren M. Overexpression of a truncated TrkB isoform increases the proliferation of neural progenitors. Eur J Neurosci. 2006;24(5):1277-85.
19. Islam O, Loo TX, Heese K. Brain-derived neurotrophic factor (BDNF) has proliferative effects on neural stem cells through the truncated TRK-B receptor, MAP kinase, AKT, and STAT-3 signaling pathways. Curr Neurovasc Res. 2009;6(1):42-53.
20. Richards AB, Morris RW, Ward S, Schmitz S, Rothmond DA, Noble PL, et al. Gonadectomy negatively impacts social behavior of adolescent male primates. Horm Behav. 2009;56(1):140-8.
21. Morris RW, Fung SJ, Rothmond DA, Richards B, Ward S, Noble PL, et al. The effect of gonadectomy on prepulse inhibition and fear-potentiated startle in adolescent rhesus macaques. Psychoneuroendocrinology. 2010;35(6):896-905.
22. Purves-Tyson TD, Handelsman DJ, Double KL, Owens SJ, Bustamante S, Weickert CS. Testosterone regulation of sex steroid-related mRNAs and dopamine-related mRNAs in adolescent male rat substantia nigra. BMC Neurosci. 2012;13:95.
23. Allan CM, Couse JF, Simanainen U, Spaliviero J, Jimenez M, Rodriguez K, et al. Estradiol induction of spermatogenesis is mediated via an estrogen receptor-{alpha} mechanism involving neuroendocrine activation of follicle-stimulating hormone secretion. Endocrinology. 2010;151(6):2800-10.
24. Singh J, O'Neill C, Handelsman DJ. Induction of spermatogenesis by androgens in gonadotropin-deficient (hpg) mice. Endocrinology. 1995;136(12):5311-21.
25. Zirkin BR, Santulli R, Awoniyi CA, Ewing LL. Maintenance of advanced spermatogenic cells in the adult rat testis: quantitative relationship to testosterone concentration within the testis. Endocrinology. 1989;124(6):3043-9.
26. Walker DM, Kirson D, Perez LF, Gore AC. Molecular profiling of postnatal development of the hypothalamus in female and male rats. Biol Reprod. 2012;87(6):129.
27. Saksena SK, Lau IF. Variations in serum androgens, estrogens, progestins, gonadotropins and prolactin levels in male-rats from prepubertal to advanced Age. Exp Aging Res. 1979;5(3):179-94.
28. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. 6th ed. San Diego, California: Elsevier; 2007.
29. Whitfield Jr HJ, Brady LS, Smith MA, Mamalaki E, Fox RJ, Herkenham M. Optimization of cRNA probe in situ hybridization methodology for localization of glucocorticoid receptor mRNA in rat brain: a detailed protocol. Cell Mol Neurobiol. 1990;10(1):145-57.
30. Paxinos G. The Rhesus Monkey Brain: In Stereotaxic Coordinates. London: Elsevier/Academic Press; 2009.
31. Ngwenya LB, Rosene DL, Peters A. An ultrastructural characterization of the newly generated cells in the adult monkey dentate gyrus. Hippocampus. 2008;18(2):210-20.
32. Santos AM, Calvente R, Tassi M, Carrasco MC, Martin-Oliva D, Marin-Teva JL, et al. Embryonic and postnatal development of microglial cells in the mouse retina. J Comp Neurol. 2008;506(2):224-39.
33. Burns JC, Christophel JJ, Collado MS, Magnus C, Carfrae M, Corwin JT. Reinforcement of cell junctions correlates with the absence of hair cell regeneration in mammals and its occurrence in birds. J Comp Neurol. 2008;511(3):396-414.
34. Okuno H, Tokuyama W, Li YX, Hashimoto T, Miyashita Y. Quantitative evaluation of neurotrophin and trk mRNA expression in visual and limbic areas along the occipito-temporo-hippocampal pathway in adult macaque monkeys. J Comp Neurol. 1999;408(3):378-98.
35. Fenner BM. Truncated TrkB: beyond a dominant negative receptor. Cytokine Growth Factor Rev. 2012;23(1-2):15-24.
36. Rose CR, Blum R, Pichler B, Lepier A, Kafitz KW, Konnerth A. Truncated TrkB-T1 mediates neurotrophin-evoked calcium signalling in glia cells. Nature. 2003;426(6962):74-8.
37. Donovan MH, Yamaguchi M, Eisch AJ. Dynamic expression of TrkB receptor protein on proliferating and maturing cells in the adult mouse dentate gyrus. Hippocampus. 2008;18(5):435-9.
38. Carrier N, Kabbaj M. Extracellular signal-regulated kinase 2 signaling in the hippocampal dentate gyrus mediates the antidepressant effects of testosterone. Biol Psychiatry. 2012;71(7):642-51.
39. Hill RA, Wu YW, Kwek P, van den Buuse M. Modulatory effects of sex steroid hormones on brain-derived neurotrophic factor-tyrosine kinase B expression during adolescent development in C57Bl/6 mice. J Neuroendocrinol. 2012;24(5):774-88.
40. Bimonte-Nelson HA, Singleton RS, Nelson ME, Eckman CB, Barber J, Scott TY, et al. Testosterone, but not nonaromatizable dihydrotestosterone, improves working memory and alters nerve growth factor levels in aged male rats. Exp Neurol. 2003;181(2):301-12.
41. Silhol M, Bonnichon V, Rage F, Tapia-Arancibia L. Age-related changes in brain-derived neurotrophic factor and tyrosine kinase receptor isoforms in the hippocampus and hypothalamus in male rats. Neuroscience. 2005;132(3):613-24.
42. Webster MJ, Herman MM, Kleinman JE, Shannon Weickert C. BDNF and trkB mRNA expression in the hippocampus and temporal cortex during the human lifespan. Gene Expression Patterns. 2006;6(8):941-51.
43. Dechant G, Barde YA. The neurotrophin receptor p75(NTR): novel functions and implications for diseases of the nervous system. Nat Neurosci. 2002;5(11):1131-6.
44. Fraley GS, Ulibarri C. Development of androgen receptor and p75(NTR) mRNAs and peptides in the lumbar spinal cord of the gerbil. Brain Res Dev Brain Res. 2002;137(2):101-14.
45. Tirassa P, Thiblin I, Agren G, Vigneti E, Aloe L, Stenfors C. High-dose anabolic androgenic steroids modulate concentrations of nerve growth factor and expression of its low affinity receptor (p75-NGFr) in male rat brain. J Neurosci Res. 1997;47(2):198-207.
46. Anagnostopoulou V, Pediaditakis I, Alkahtani S, Alarifi SA, Schmidt EM, Lang F, et al. Differential effects of dehydroepiandrosterone and testosterone in prostate and colon cancer cell apoptosis: the role of nerve growth factor (NGF) receptors. Endocrinology. 2013;154(7):2446-56.
47. Xu J, Gingras KM, Bengston L, Di Marco A, Forger NG. Blockade of endogenous neurotrophic factors prevents the androgenic rescue of rat spinal motoneurons. J Neurosci. 2001;21(12):4366-72.
48. Ho A, Villacis AJ, Svirsky SE, Foilb AR, Romeo RD. The pubertal-related decline in cellular proliferation and neurogenesis in the dentate gyrus of male rats is independent of the pubertal rise in gonadal hormones. Dev Neurobiol. 2011;75(5):743-52.
49. Brown JP, Couillard-Despres S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG. Transient expression of doublecortin during adult neurogenesis. J Comp Neurol. 2003;467(1):1-10.
50. Kohler SJ, Williams NI, Stanton GB, Cameron JL, Greenough WT. Maturation time of new granule cells in the dentate gyrus of adult macaque monkeys exceeds six months. Proc Natl Acad Sci U S A. 2011;108:10326-31.
51. Isgor C, Watson SJ. Estrogen receptor alpha and beta mRNA expressions by proliferating and differentiating cells in the adult rat dentate gyrus and subventricular zone. Neuroscience. 2005;134(3):847-56.
52. Hamson DK, Wainwright SR, Taylor JR, Jones BA, Watson NV, Galea LA. Androgens increase survival of adult-born neurons in the dentate gyrus by an androgen receptor-dependent mechanism in male rats. Endocrinology. 2013;154(9):3294-304.
53. Brannvall K, Bogdanovic N, Korhonen L, Lindholm D. 19-Nortestosterone influences neural stem cell proliferation and neurogenesis in the rat brain. Eur J Neurosci. 2005;21(4):871-8.
54. Hojo Y, Higo S, Ishii H, Ooishi Y, Mukai H, Murakami G, et al. Comparison between hippocampus-synthesized and circulation-derived sex steroids in the hippocampus. Endocrinology. 2009;150(11):5106-12.
55. Spritzer MD, Ibler E, Inglis W, Curtis MG. Testosterone and social isolation influence adult neurogenesis in the dentate gyrus of male rats. Neuroscience. 2011;195:180-90.
56. Barker JM, Galea LA. Repeated estradiol administration alters different aspects of neurogenesis and cell death in the hippocampus of female, but not male, rats. Neuroscience. 2008;152(4):888-902.
57. Hickson RC, Czerwinski SM, Falduto MT, Young AP. Glucocorticoid antagonism by exercise and androgenic-anabolic steroids. Med Sci Sports Exerc. 1990;22(3):331-40.
58. Viau V, Meaney MJ. The inhibitory effect of testosterone on hypothalamic-pituitary-adrenal responses to stress is mediated by the medial preoptic area. J Neurosci. 1996;16(5):1866-76.
59. Schoenfeld TJ, Gould E. Stress, stress hormones, and adult neurogenesis. Exp Neurol. 2012;233(1):12-21.
60. Mirescu C, Gould E. Stress and adult neurogenesis. Hippocampus. 2006;16(3):233-8.
61. Shors TJ, Mathew J, Sisti HM, Edgecomb C, Beckoff S, Dalla C. Neurogenesis and helplessness are mediated by controllability in males but not in females. Biol Psychiatry. 2007;62(5):487-95.
62. Falconer EM, Galea LA. Sex differences in cell proliferation, cell death and defensive behavior following acute predator odor stress in adult rats. Brain Res. 2003;975(1-2):22-36.
63. Reif A, Fritzen S, Finger M, Strobel A, Lauer M, Schmitt A, et al. Neural stem cell proliferation is decreased in schizophrenia, but not in depression. Mol Psychiatry. 2006;11(5):514-22.
64. Barbeau D, Liang JJ, Robitalille Y, Quirion R, Srivastava LK. Decreased expression of the embryonic form of the neural cell adhesion molecule in schizophrenic brains. Proc Natl Acad Sci U S A. 1995;92(7):2785-9.
65. Epp JR, Beasley CL, Galea LA. Increased hippocampal neurogenesis and p21 expression in depression: dependent on antidepressants, sex, age, and antipsychotic exposure. Neuropsychopharmacology. 2013;38(11):2297-306.
66. Lucassen PJ, Stumpel MW, Wang Q, Aronica E. Decreased numbers of progenitor cells but no response to antidepressant drugs in the hippocampus of elderly depressed patients. Neuropharmacology. 2010;58(6):940-9.