Gonadectomy increases neurogenesis in the male adolescent rhesus macaque hippocampus

Hippocampus

Volumn 24, Issue 2, 2014, Pages 225-238

  Allen, K M ^a,b,c   Fung, S J ^a,b,c   Rothmond, D A ^a,b   Noble, P L ^d   Shannon Weickert, C ^a,b,c  

^a SCHIZOPHRENIA RESEARCH INSTITUTE   (Australia)

^b NEUROSCIENCE RESEARCH AUSTRALIA   (Australia)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

^d NIMH IRP Non Human Primate Core   (United States)

Author keywords

Development; Neuronal survival; Schizophrenia; Sex steroids; Testosterone

Indexed keywords

TESTIS PEPTIDE HORMONE; TESTOSTERONE;

ADOLESCENCE; ADOLESCENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; GONADECTOMY; HIPPOCAMPUS; MALE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; RHESUS MONKEY; STEREOLOGY; SURVIVAL FACTOR;

DEVELOPMENT; NEURONAL SURVIVAL; SCHIZOPHRENIA; SEX STEROIDS; TESTOSTERONE;

ANIMALS; BROMODEOXYURIDINE; CELL COUNT; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION; HIPPOCAMPUS; KI-67 ANTIGEN; MACACA MULATTA; MALE; NEUROGENESIS; ORCHIECTOMY; PHOSPHOPYRUVATE HYDRATASE; RNA, MESSENGER; TESTOSTERONE; TUMOR SUPPRESSOR PROTEINS;

EID: 84892678689     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22217     Document Type: Article

References (103)

1. Abel KM, Drake R, Goldstein JM. 2010. Sex differences in schizophrenia. Int Rev Psychiatry 22:417-428.
2. Aizawa K, Ageyama N, Terao K, Hisatsune T. 2011. Primate-specific alterations in neural stem/progenitor cells in the aged hippocampus. Neurobiol Aging 32:140-150.
3. Aizawa K, Ageyama N, Yokoyama C, Hisatsune T. 2009. Age-dependent alteration in hippocampal neurogenesis correlates with learning performance of macaque monkeys. Exp Anim 58:403-407.
4. Akhondzadeh S, Rezaei F, Larijani B, Nejatisafa AA, Kashani L, Abbasi SH. 2006. Correlation between testosterone, gonadotropins and prolactin and severity of negative symptoms in male patients with chronic schizophrenia. Schizophr Res 84:405-410.
5. Aleman A, Kahn RS, Selten JP. 2003. Sex differences in the risk of schizophrenia-Evidence from meta-analysis. Arch Gen Psychiatry 60:565-571.
6. Altar CA, Jurata LW, Charles V, Lemire A, Liu P, Bukhman Y, Young TA, Bullard J, Yokoe H, Webster MJ, Knable MB, Brockman JA 2005. Deficient hippocampal neuron expression of proteasome, ubiquitin, and mitochondrial genes in multiple schizophrenia cohorts. Biol Psychiatry 58:85-96.
7. Amaral DG, Scharfman HE, Lavenex P. 2007. The dentate gyrus: Fundamental neuroanatomical organization (dentate gyrus for dummies). Prog Brain Res 163:3-22.
8. Amrein I, Isler K, Lipp HP. 2011. Comparing adult hippocampal neurogenesis in mammalian species and orders: Influence of chronological age and life history stage. Eur J Neurosci 34:978-987.
9. Barbeau D, Liang JJ, Robitalille Y, Quirion R, Srivastava LK. 1995. Decreased expression of the embryonic form of the neural cell adhesion molecule in schizophrenic brains. Proc Natl Acad Sci USA 92:2785-2789.
10. Barha CK, Brummelte S, Lieblich SE, Galea LA. 2011. Chronic restraint stress in adolescence differentially influences hypothalamic-pituitary-adrenal axis function and adult hippocampal neurogenesis in male and female rats. Hippocampus 21:1216-1227.
11. Bercovitch FB, Widdig A, Trefilov A, Kessler MJ, Berard JD, Schmidtke J, Nurnberg P, Krawczak M. 2003. A longitudinal study of age-specific reproductive output and body condition among male rhesus macaques, Macaca mulatta. Naturwissenschaften 90:309-312.
12. Bowen WH, Koch G. 1970. Determination of age in monkeys (Macaca irus) on the basis of dental development. Lab Anim 4:113-124.
13. Brannvall K, Bogdanovic N, Korhonen L, Lindholm D. 2005. 19-Nortestosterone influences neural stem cell proliferation and neurogenesis in the rat brain. Eur J Neurosci 21:871-878.
14. Brenhouse HC, Andersen SL. 2011. Developmental trajectories during adolescence in males and females: A cross-species understanding of underlying brain changes. Neurosci Biobehav Rev 35:1687-1703.
15. Buwalda B, van der Borght K, Koolhaas JM, McEwen BS. 2010. Testosterone decrease does not play a major role in the suppression of hippocampal cell proliferation following social defeat stress in rats. Physiol Behav 101:719-725.
16. Carrier N, Kabbaj M. 2012. Extracellular signal-regulated kinase 2 signaling in the hippocampal dentate gyrus mediates the antidepressant effects of testosterone. Biol Psychiatry 71:642-651.
17. Chen Z, Ye R, Goldman SA. 2013. Testosterone modulation of angiogenesis and neurogenesis in the adult songbird brain. Neuroscience 239:139-148.
18. Coe CL, Kramer M, Czeh B, Gould E, Reeves AJ, Kirschbaum C, Fuchs E. 2003. Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys. Biol Psychiatry 54:1025-1034.
19. Czéh B, Lucassen P. 2007. What causes the hippocampal volume decrease in depression? Eur Arch Psychiatry Clin Neurosci 257:250-260.
20. DeCarolis NA, Eisch AJ. 2010. Hippocampal neurogenesis as a target for the treatment of mental illness: A critical evaluation. Neuropharmacology 58:884-893.
21. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH. 1998. Neurogenesis in the adult human hippocampus. Nat Med 4:1313-1317.
22. Garcia A, Steiner B, Kronenberg G, Bick-Sander A, Kempermann G. 2004. Age-dependent expression of glucocorticoid- and mineralocorticoid receptors on neural precursor cell populations in the adult murine hippocampus. Aging Cell 3:363-371.
23. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H. 2006. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439:589-593.
24. Ge S, Yang CH, Hsu KS, Ming GL, Song H. 2007. A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 54:559-566.
25. Ge S, Sailor K, Ming G, Song H. 2008. Synaptic integration and plasticity of new neurons in the adult hippocampus. J Physiol 586:3759-3765.
26. Geinisman Y, Gundersen HJ, van der Zee E, West MJ. 1996. Unbiased stereological estimation of the total number of synapses in a brain region. J Neurocytol 25:805-819.
27. Gerdes J, Lemke H, Baisch H, Wacker HH, Schwab U, Stein H. 1984. Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J Immunol 133:1710-1715.
28. Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijdenbos A, Paus T, Evans AC, Rapoport JL. 1999. Brain development during childhood and adolescence: A longitudinal MRI study. Nat Neurosci 2:861-863.
29. Gogtay N, Nugent T, Herman D, Ordonez A. 2006. Dynamic mapping of normal human hippocampal development. Hippocampus 16:664-672.
30. Gould E, Tanapat P, McEwen BS, Flugge G, Fuchs E. 1998. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc Natl Acad Sci USA 95:3168-3171.
31. Gould E, Reeves AJ, Fallah M, Tanapat P, Gross CG, Fuchs E. 1999. Hippocampal neurogenesis in adult Old World primates. Proc Natl Acad Sci USA 96:5263-5267.
32. Gould E, Vail N, Wagers M, Gross CG. 2001. Inaugural article: Adult-generated hippocampal and neocortical neurons in macaques have a transient existence. Proc Natl Acad Sci USA 98:1-8.
33. Gundersen HJ, Jensen EB. 1987. The efficiency of systematic sampling in stereology and its prediction. J Microsc 147 (Part 3):229-263.
34. Hamson DK, Wainwright SR, Taylor JR, Jones BA, Watson NV, Galea LA. 2013. Androgens increase survival of adult-born neurons in the dentate gyrus by an androgen receptor-dependent mechanism in male rats. Endocrinology 154:3294-3304.
35. Hartog TE, Dittrich F, Pieneman AW, Jansen RF, Frankl-Vilches C, Lessmann V, Lilliehook C, Goldman SA, Gahr M. 2009. Brain-derived neurotrophic factor signaling in the HVC is required for testosterone-induced song of female canaries. J Neurosci 29:15511-15519.
36. He J, Crews FT. 2007. Neurogenesis decreases during brain maturation from adolescence to adulthood. Pharmacol Biochem Behav 86:327-333.
37. Heine VM, Maslam S, Joels M, Lucassen PJ. 2004. Prominent decline of newborn cell proliferation, differentiation, and apoptosis in the aging dentate gyrus, in absence of an age-related hypothalamus-pituitary-adrenal axis activation. Neurobiol Aging 25:361-375.
38. Ho A, Villacis AJ, Svirsky SE, Foilb AR, Romeo RD. 2011. 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 75:743-752.
39. Inta D, Alfonso J, von Engelhardt J, Kreuzberg MM, Meyer AH, van Hooft JA, Monyer H. 2008. Neurogenesis and widespread forebrain migration of distinct GABAergic neurons from the postnatal subventricular zone. Proc Natl Acad Sci USA 105:20994-20999.
40. Jabes A, Lavenex PB, Amaral DG, Lavenex P. 2010. Quantitative analysis of postnatal neurogenesis and neuron number in the macaque monkey dentate gyrus. Eur J Neurosci 31:273-285.
41. Jabes A, Lavenex PB, Amaral DG, Lavenex P. 2011. Postnatal development of the hippocampal formation: A stereological study in macaque monkeys. J Comp Neurol 519:1051-1070.
42. Kempermann G. 2011. Adult Neurogenesis 2: Stem Cells and Neuronal Development in the Adult Brain. New York: Oxford University Press.
43. Keuker JI, Luiten PG, Fuchs E. 2003. Preservation of hippocampal neuron numbers in aged rhesus monkeys. Neurobiol Aging 24:157-165.
44. Knoth R, Singec I, Ditter M, Pantazis G, Capetian P, Meyer RP, Horvat V, Volk B, Kempermann G. 2010. Murine features of neurogenesis in the human hippocampus across the lifespan from 0 to 100 years. PLoS One 5:e8809.
45. Ko YH, Jung SW, Joe SH, Lee CH, Jung HG, Jung IK, Kim SH, Lee MS. 2007. Association between serum testosterone levels and the severity of negative symptoms in male patients with chronic schizophrenia. Psychoneuroendocrinology 32:385-391.
46. Kohler SJ, Williams NI, Stanton GB, Cameron JL, Greenough WT. 2011. Maturation time of new granule cells in the dentate gyrus of adult macaque monkeys exceeds six months. Proc Natl Acad Sci USA 108:10326-10331.
47. Kordower JH, Chen EY, Morrison JH. 2010. Long-term gonadal hormone treatment and endogenous neurogenesis in the dentate gyrus of the adult female monkey. Exp Neurol 224:252-257.
48. Kornack DR, Rakic P. 1998. Changes in cell-cycle kinetics during the development and evolution of primate neocortex. Proc Natl Acad Sci USA 95:1242-1246.
49. Kornack DR, Rakic P. 1999. Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc Natl Acad Sci USA 96:5768-5773.
50. Kornack DR, Rakic P. 1999. Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc Natl Acad Sci USA 96:1-6.
51. Le Strat Y, Ramoz N, Gorwood P. 2009. The role of genes involved in neuroplasticity and neurogenesis in the observation of a gene-environment interaction (GxE) in schizophrenia. Curr Mol Med 9:506-518.
52. Leuner B, Gould E. 2010. Structural plasticity and hippocampal function. Annu Rev Psychol 61:111-140.
53. Louissaint A Jr, Rao S, Leventhal C, Goldman SA. 2002. Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron 34:945-960.
54. Lucas NN, Lee DW. 2009. BDNF increases BrdU-IR cells in the injured adult zebra finch hippocampus. Neuroreport 20:1066-1070.
55. MacLusky NJ, Walters MJ, Clark AS, Toran-Allerand CD. 1994. Aromatase in the cerebral cortex, hippocampus, and mid-brain: Ontogeny and developmental implications. Mol Cell Neurosci 5:691-698.
56. Manganas LN, Zhang X, Li Y, Hazel RD, Smith SD, Wagshul ME, Henn F, Benveniste H, Djuric PM, Enikolopov G, Maletic-Savatic M 2007. Magnetic resonance spectroscopy identifies neural progenitor cells in the live human brain. Science 318:980-985.
57. Mattai A, Hosanagar A, Weisinger B, Greenstein D, Stidd R, Clasen L, Lalonde F, Rapoport J, Gogtay N. 2011. Hippocampal volume development in healthy siblings of childhood-onset schizophrenia patients. Am J Psychiatry 168:427-435.
58. McClure RE, Barha CK, Galea LA. 2013. 17beta-Estradiol, but not estrone, increases the survival and activation of new neurons in the hippocampus in response to spatial memory in adult female rats. Horm Behav 63:144-157.
59. McGrath J, Saha S, Welham J, El Saadi O, MacCauley C, Chant D. 2004. A systematic review of the incidence of schizophrenia: The distribution of rates and the influence of sex, urbanicity, migrant status and methodology. BMC Med 2:13.
60. Mirescu C, Gould E. 2006. Stress and adult neurogenesis. Hippocampus 16:233-238.
61. Moore L, Kyaw M, Vercammen A, Lenroot R, Kulkarni J, Curtis J, O'Donnell M, Carr VJ, Shannon Weickert C, Weickert TW. 2013. Serum testosterone levels are related to cognitive function in men with schizophrenia. Psychoneuroendocrinology 38:1717-1728.
62. Morris RW, Fung SJ, Rothmond DA, Richards B, Ward S, Noble PL, Woodward RA, Weickert CS, Winslow JT. 2010. The effect of gonadectomy on prepulse inhibition and fear-potentiated startle in adolescent rhesus macaques. Psychoneuroendocrinology 35:896-905.
63. Ngwenya L, Peters A, Rosene DL. 2006. Maturational sequence of newly generated neurons in the dentate gyrus of the young adult rhesus monkey. J Comp Neurol 498:204-216.
64. Ngwenya LB, Rosene DL, Peters A. 2008. An ultrastructural characterization of the newly generated cells in the adult monkey dentate gyrus. Hippocampus 18:210-220.
65. Ormerod BK, Galea LA. 2003. Reproductive status influences the survival of new cells in the dentate gyrus of adult male meadow voles. Neurosci Lett 346:25-28.
66. Ottem EN, Bailey DJ, Jordan CL, Marc Breedlove S. 2012. With a little help from my friends: Androgens tap BDNF signaling pathways to alter neural circuits. Neuroscience 239:124-138.
67. Paxinos G. 2009. The Rhesus Monkey Brain: In Stereotaxic Coordinates. London: Elsevier/Academic Press.
68. Payne C, Machado CJ, Bliwise NG, Bachevalier J. 2010. Maturation of the hippocampal formation and amygdala in Macaca mulatta: A volumetric magnetic resonance imaging study. Hippocampus 20:922-935.
69. Pelletier G, Luu-The V, Labrie F. 1994. Immunocytochemical localization of 5 alpha-reductase in rat brain. Mol Cell Neurosci 5:394-399.
70. Perlman WR, Weickert CS, Akil M, Kleinman JE. 2004. Postmortem investigations of the pathophysiology of schizophrenia: The role of susceptibility genes. J Psychiatry Neurosci 29:287-293.
71. Rao MS, Hattiangady B, Shetty AK. 2006. The window and mechanisms of major age-related decline in the production of new neurons within the dentate gyrus of the hippocampus. Aging Cell 5:545-558.
72. Rasika S, Alvarez-Buylla A, Nottebohm F. 1999. BDNF mediates the effects of testosterone on the survival of new neurons in an adult brain. Neuron 22:53-62.
73. Reif A, Fritzen S, Finger M, Strobel A, Lauer M, Schmitt A, Lesch KP. 2006. Neural stem cell proliferation is decreased in schizophrenia, but not in depression. Mol Psychiatry 11:514-522.
74. Reif A, Schmitt A, Fritzen S, Lesch KP. 2007. Neurogenesis and schizophrenia: Dividing neurons in a divided mind? Eur Arch Psychiatry Clin Neurosci 257:290-299.
75. Richards AB, Morris RW, Ward S, Schmitz S, Rothmond DA, Noble PL, Woodward RA, Winslow JT, Weickert CS. 2009. Gonadectomy negatively impacts social behavior of adolescent male primates. Horm Behav 56:140-148.
76. Scharfman H, Goodman J, Macleod A, Phani S, Antonelli C, Croll S. 2005. Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp Neurol 192:348-356.
77. Schoenfeld TJ, Gould E. 2012. Stress, stress hormones, and adult neurogenesis. Exp Neurol 233:12-21.
78. Schwartz SM, Kemnitz JW. 1992. Age- and gender-related changes in body size, adiposity, and endocrine and metabolic parameters in free-ranging rhesus macaques. Am J Phys Anthropol 89:109-121.
79. Shin R, Kobayashi K, Hagihara H, Kogan JH, Miyake S, Tajinda K, Walton NM, Gross AK, Heusner CL, Chen Q, Tamura K, Miyakawa T, Matsumoto M 2013. The immature dentate gyrus represents a shared phenotype of mouse models of epilepsy and psychiatric disease. Bipolar Disord. In Press. doi: 10.1111/bdi.12064.
80. Shirayama Y, Hashimoto K, Suzuki Y, Higuchi T. 2002. Correlation of plasma neurosteroid levels to the severity of negative symptoms in male patients with schizophrenia. Schizophr Res 58:69-74.
81. Sisk CL, Foster DL. 2004. The neural basis of puberty and adolescence. Nat Neurosci 7:1040-1047.
82. Snyder JS, Kee N, Wojtowicz JM. 2001. Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. J Neurophysiol 85:2423-2431.
83. Snyder JS, Choe JS, Clifford MA, Jeurling SI, Hurley P, Brown A, Kamhi JF, Cameron HA. 2009. Adult-born hippocampal neurons are more numerous, faster maturing, and more involved in behavior in rats than in mice. J Neurosci 29:14484-14495.
84. Spalding KL, Bergmann O, Alkass K, Bernard S, Salehpour M, Huttner HB, Bostrom E, Westerlund I, Vial C, Buchholz BA, et al. 2013. Dynamics of hippocampal neurogenesis in adult humans. Cell 153:1219-1227.
85. Spear LP. 2000. The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24:417-463.
86. Spritzer MD, Galea LA. 2007. Testosterone and dihydrotestosterone, but not estradiol, enhance survival of new hippocampal neurons in adult male rats. Dev Neurobiol 67:1321-1333.
87. Spritzer MD, Ibler E, Inglis W, Curtis MG. 2011. Testosterone and social isolation influence adult neurogenesis in the dentate gyrus of male rats. Neuroscience 195:180-190.
88. Starka L, Pospisilova H, Hill M. 2009. Free testosterone and free dihydrotestosterone throughout the life span of men. J Steroid Biochem Mol Biol 116:118-120.
89. Steiner B, Zurborg S, Horster H, Fabel K, Kempermann G. 2008. Differential 24 h responsiveness of Prox1-expressing precursor cells in adult hippocampal neurogenesis to physical activity, environmental enrichment, and kainic acid-induced seizures. Neuroscience 154:521-529.
90. Taherianfard M, Shariaty M. 2004. Evaluation of serum steroid hormones in schizophrenic patients. Indian J Med Sci 58:3-9.
91. Tanapat P, Hastings NB, Reeves AJ, Gould E. 1999. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J Neurosci 19:5792-5801.
92. Thompson Ray M, Weickert CS, Wyatt E, Webster MJ. 2011. Decreased BDNF, trkB-TK+ and GAD67 mRNA expression in the hippocampus of individuals with schizophrenia and mood disorders. J Psychiatry Neurosci 36:195-203.
93. Toth E, Gersner R, Wilf-Yarkoni A, Raizel H, Dar DE, Richter-Levin G, Levit O, Zangen A. 2008. Age-dependent effects of chronic stress on brain plasticity and depressive behavior. J Neurochem 107:522-532.
94. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH. 2002. Functional neurogenesis in the adult hippocampus. Nature 415:1030-1034.
95. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:1-12.
96. von Bohlen und Halbach O. 2011. Immunohistological markers for proliferative events, gliogenesis, and neurogenesis within the adult hippocampus. Cell Tissue Res 345:1-19.
97. Wainwright SR, Lieblich SE, Galea LA. 2011. Hypogonadism predisposes males to the development of behavioural and neuroplastic depressive phenotypes. Psychoneuroendocrinology 36:1327-1341.
98. Walker DM, Kirson D, Perez LF, Gore AC. 2012. Molecular profiling of postnatal development of the hypothalamus in female and male rats. Biol Reprod 87:129.
99. Walton NM, Zhou Y, Kogan JH, Shin R, Webster M, Gross AK, Heusner CL, Chen Q, Miyake S, Tajinda K, Tamura K, Miyakawa T, Matsumoto M 2012. Detection of an immature dentate gyrus feature in human schizophrenia/bipolar patients. Transl Psychiatry 2:e135.
100. Weickert CS, Webster MJ, Colvin SM, Herman MM, Hyde TM, Weinberger DR, Kleinman JE. 2000. Localization of epidermal growth factor receptors and putative neuroblasts in human subependymal zone. J Comp Neurol 423:359-372.
101. West MJ. 1999. Stereological methods for estimating the total number of neurons and synapses: Issues of precision and bias. Trends Neurosci 22:51-61.
102. Yamasaki N, Maekawa M, Kobayashi K, Kajii Y, Maeda J, Soma M, Takao K, Tanda K, Ohira K, Toyama K, Kanzaki K, Fukunaga K, Sudo Y, Ichinose H, Ikeda M, Iwata N, Ozaki N, Suzuki H, Higuchi M, Suhara T, Yuasa S, Miyakawa T 2008. Alpha-CaMKII deficiency causes immature dentate gyrus, a novel candidate endophenotype of psychiatric disorders. Mol Brain 1:6.
103. Zhang Z, Yang R, Zhou R, Li L, Sokabe M, Chen L. 2010. Progesterone promotes the survival of newborn neurons in the dentate gyrus of adult male mice. Hippocampus 20:402-412.