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Erschienen in: Metabolic Brain Disease 2/2018

11.12.2017 | Original Article

Neuroanatomical and molecular correlates of cognitive and behavioural outcomes in hypogonadal males

verfasst von: O. B. Akinola, M. O. Gabriel

Erschienen in: Metabolic Brain Disease | Ausgabe 2/2018

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Abstract

Robust epidemiological, clinical and laboratory evidence supports emerging roles for the sex steroids in such domains as neurodevelopment, behaviour, learning and cognition. Regions of the mammalian brain that are involved in cognitive development and memory do not only express the classical nuclear androgen receptor, but also the non-genomic membrane receptor, which is a G protein-coupled receptor that mediates some rapid effects of the androgens on neurogenesis and synaptic plasticity. Under physiological conditions, hippocampal neurons do express the enzyme aromatase, and therefore actively aromatize testosterone to oestradiol. Although glial expression of the aromatase enzyme is minimal, increased expression following injury suggests a role for sex steroids in neuroprotection. It is therefore plausible to deduce that low levels of circulating androgens in males would perturb neuronal functions in relation to cognition and memory, as well as neural repair following injury. The present review is an overview of some roles of the sex steroids on cognitive function in males, and the neuroanatomical and molecular underpinnings of some behavioural and cognitive deficits characteristic of such genetic disorders noted for low androgen levels, including Klinefelter syndrome, Bardet-Biedl syndrome, Kallman syndrome and Prader-Willi syndrome. Recent literature in relation to some behavioural and cognitive changes secondary to surgical and pharmacological castration are also appraised.
Literatur
Zurück zum Zitat Akinola OB, Poluch S, Juliano SL (2013) Abnormal expression of cation-chloride cotransporters results in impaired migration during corticogenesis. In 43rd annual meeting of the Society for Neuroscience). San Diego, USA: Society for Neuroscience Akinola OB, Poluch S, Juliano SL (2013) Abnormal expression of cation-chloride cotransporters results in impaired migration during corticogenesis. In 43rd annual meeting of the Society for Neuroscience). San Diego, USA: Society for Neuroscience
Zurück zum Zitat Aksoy A, Karaguzel G, Akbulut U, Turk A (2011) Two sisters with Bardet-Biedl syndrome: brain abnormalities and unusual facial findings. Turk J Pediatr 53(4):460–463PubMed Aksoy A, Karaguzel G, Akbulut U, Turk A (2011) Two sisters with Bardet-Biedl syndrome: brain abnormalities and unusual facial findings. Turk J Pediatr 53(4):460–463PubMed
Zurück zum Zitat Anthoni H, Sucheston LE, Lewis BA, Tapia-Páez I, Fan X, Zucchelli M, Taipale M, Stein CM, Hokkanen ME, Castrén E, Pennington BF, Smith SD, Olson RK, Tomblin JB, Schulte-Körne G, Nöthen M, Schumacher J, Müller-Myhsok B, Hoffmann P, Gilger JW, Hynd GW, Nopola-Hemmi J, Leppanen PHT, Lyytinen H, Schoumans J, Nordenskjöld M, Spencer J, Stanic D, Boon WC, Simpson E, Mäkelä S, Gustafsson JÅ, Peyrard-Janvid M, Iyengar S, Kere J (2012) The aromatase gene CYP19A1: several genetic and functional lines of evidence supporting a role in reading, speech and language. Behav Genet 42(4):509–527. https://doi.org/10.1007/s10519-012-9532-3 PubMedPubMedCentralCrossRef Anthoni H, Sucheston LE, Lewis BA, Tapia-Páez I, Fan X, Zucchelli M, Taipale M, Stein CM, Hokkanen ME, Castrén E, Pennington BF, Smith SD, Olson RK, Tomblin JB, Schulte-Körne G, Nöthen M, Schumacher J, Müller-Myhsok B, Hoffmann P, Gilger JW, Hynd GW, Nopola-Hemmi J, Leppanen PHT, Lyytinen H, Schoumans J, Nordenskjöld M, Spencer J, Stanic D, Boon WC, Simpson E, Mäkelä S, Gustafsson JÅ, Peyrard-Janvid M, Iyengar S, Kere J (2012) The aromatase gene CYP19A1: several genetic and functional lines of evidence supporting a role in reading, speech and language. Behav Genet 42(4):509–527. https://​doi.​org/​10.​1007/​s10519-012-9532-3 PubMedPubMedCentralCrossRef
Zurück zum Zitat Aubele T, Kritzer MF (2012) Androgen influence on prefrontal dopamine systems in adult male rats: localization of cognate intracellular receptors in medial prefrontal projections to the ventral tegmental area and effects of gonadectomy and hormone replacement on glutamate-stimulated extracellular dopamine level. Cereb Cortex 22(8):1799–1812. https://doi.org/10.1093/cercor/bhr258 PubMedCrossRef Aubele T, Kritzer MF (2012) Androgen influence on prefrontal dopamine systems in adult male rats: localization of cognate intracellular receptors in medial prefrontal projections to the ventral tegmental area and effects of gonadectomy and hormone replacement on glutamate-stimulated extracellular dopamine level. Cereb Cortex 22(8):1799–1812. https://​doi.​org/​10.​1093/​cercor/​bhr258 PubMedCrossRef
Zurück zum Zitat Baker K, Northam GB, Chong WK, Banks T, Beales P, Baldeweg T (2011) Neocortical and hippocampal volume loss in a human ciliopathy: a quantitative MRI study in Bardet-Biedl syndrome. Am J Med Genet A 1:1–8CrossRef Baker K, Northam GB, Chong WK, Banks T, Beales P, Baldeweg T (2011) Neocortical and hippocampal volume loss in a human ciliopathy: a quantitative MRI study in Bardet-Biedl syndrome. Am J Med Genet A 1:1–8CrossRef
Zurück zum Zitat Bennouna-Greene V, Kremer S, Stoetzel C, Christmann D, Schuster C, Durand M, Verloes A, Sigaudy S, Holder-Espinasse M, Godet J, Brandt C, Marion V, Danion A, Dietemann JL, Dollfus H (2011) Hippocampal dysgenesis and variable neuropsychiatric phenotypes in patients with Bardet-Biedl syndrome underline complex CNS impact of primary cilia. Clin Genet 80(6):523–531. https://doi.org/10.1111/j.1399-0004.2011.01688.x PubMedCrossRef Bennouna-Greene V, Kremer S, Stoetzel C, Christmann D, Schuster C, Durand M, Verloes A, Sigaudy S, Holder-Espinasse M, Godet J, Brandt C, Marion V, Danion A, Dietemann JL, Dollfus H (2011) Hippocampal dysgenesis and variable neuropsychiatric phenotypes in patients with Bardet-Biedl syndrome underline complex CNS impact of primary cilia. Clin Genet 80(6):523–531. https://​doi.​org/​10.​1111/​j.​1399-0004.​2011.​01688.​x PubMedCrossRef
Zurück zum Zitat Buiting K (2010) Prader-Willi syndrome and Angelman syndrome. Am J Med Genet C Semin Med Genet 15:365–376CrossRef Buiting K (2010) Prader-Willi syndrome and Angelman syndrome. Am J Med Genet C Semin Med Genet 15:365–376CrossRef
Zurück zum Zitat Cappuccio F, Abate V, Bolognini I et al (2016) Impact of testicular cancer on survivors’ quality of life: systematic review. World Cancer Res J 3:e738 Cappuccio F, Abate V, Bolognini I et al (2016) Impact of testicular cancer on survivors’ quality of life: systematic review. World Cancer Res J 3:e738
Zurück zum Zitat Djankpa FT, Akinola OB, Juliano SL (2016) Regional distribution and cellular localization of KCC2 in ferret cortex. Proceedings of the, published by the in USU research days 2016). Bethesda: Uniformed Services University of the Health Sciences Djankpa FT, Akinola OB, Juliano SL (2016) Regional distribution and cellular localization of KCC2 in ferret cortex. Proceedings of the, published by the in USU research days 2016). Bethesda: Uniformed Services University of the Health Sciences
Zurück zum Zitat Farag TI, Teebi AS (1988) Bardet-Biedl and Laurence-moon syndromes in a mixed Arab population. Clin Genet 33(2):78–82 Farag TI, Teebi AS (1988) Bardet-Biedl and Laurence-moon syndromes in a mixed Arab population. Clin Genet 33(2):78–82
Zurück zum Zitat Farag TI, Teebi AS (1989) High incidence of Bardet Biedl syndrome among the Bedouin. Clin Genet 36(6):463–464PubMedCrossRef Farag TI, Teebi AS (1989) High incidence of Bardet Biedl syndrome among the Bedouin. Clin Genet 36(6):463–464PubMedCrossRef
Zurück zum Zitat Giedd JN, Clasen LS, Lenroot R et al (2006) Puberty-related influences on brain development. Mol Cell Endocrinol 255:154–162CrossRef Giedd JN, Clasen LS, Lenroot R et al (2006) Puberty-related influences on brain development. Mol Cell Endocrinol 255:154–162CrossRef
Zurück zum Zitat Hernando-Quintana N, Playan-Uson J, Crespo-Burillo JA, Marin-Cardenas MA, Gazulla J (2015) Ataxia and focal dystonia in Kallmann syndrome. Clin Case Rep 4:182–185PubMedPubMedCentralCrossRef Hernando-Quintana N, Playan-Uson J, Crespo-Burillo JA, Marin-Cardenas MA, Gazulla J (2015) Ataxia and focal dystonia in Kallmann syndrome. Clin Case Rep 4:182–185PubMedPubMedCentralCrossRef
Zurück zum Zitat Hogervorst E, Williams J, Budge M, Barnetson L, Combrinck M, Smith D (2001) Serum total testosterone is lower in men with Alzheimer’s disease. Neuroendocrinol Lett 22(3):163–168PubMed Hogervorst E, Williams J, Budge M, Barnetson L, Combrinck M, Smith D (2001) Serum total testosterone is lower in men with Alzheimer’s disease. Neuroendocrinol Lett 22(3):163–168PubMed
Zurück zum Zitat Honea RA, Holsen LM, Lepping RJ et al (2012) The neuroanatomy of genetic subtype differences in Prader-Willi syndrome. Am J Med Genet B Neuropsychiatr Genet 2:243–253CrossRef Honea RA, Holsen LM, Lepping RJ et al (2012) The neuroanatomy of genetic subtype differences in Prader-Willi syndrome. Am J Med Genet B Neuropsychiatr Genet 2:243–253CrossRef
Zurück zum Zitat Iwuala S, Olamoyegun M, Fasanmade O, Ohwovoriole A (2013) Bardet-Biedel syndrome: a case report and a review of literature. Nigerian. Endocr Pract 7:33–38 Iwuala S, Olamoyegun M, Fasanmade O, Ohwovoriole A (2013) Bardet-Biedel syndrome: a case report and a review of literature. Nigerian. Endocr Pract 7:33–38
Zurück zum Zitat Kim HJ, Casadesus G (2010) Estrogen-mediated effects on cognition and synaptic plasticity: what do estrogen receptor knockout models tell us? Biochim Biophys Acta 10:12 Kim HJ, Casadesus G (2010) Estrogen-mediated effects on cognition and synaptic plasticity: what do estrogen receptor knockout models tell us? Biochim Biophys Acta 10:12
Zurück zum Zitat Knorr JR, Ragland RL, Brown RS, Gelber N (1993) Kallmann syndrome: MR findings. AJNR Am J Neuroradiol 14(4):845–851PubMed Knorr JR, Ragland RL, Brown RS, Gelber N (1993) Kallmann syndrome: MR findings. AJNR Am J Neuroradiol 14(4):845–851PubMed
Zurück zum Zitat Laitinen EM, Vaaralahti K, Tommiska J et al (2011) Incidence, phenotypic features and molecular genetics of Kallmann syndrome in Finland. Orphanet J Rare Dis 6:1750–1172CrossRef Laitinen EM, Vaaralahti K, Tommiska J et al (2011) Incidence, phenotypic features and molecular genetics of Kallmann syndrome in Finland. Orphanet J Rare Dis 6:1750–1172CrossRef
Zurück zum Zitat Lasaite L, Ceponis J, Preiksa RT, Zilaitiene B (2017) Effects of two-years testosterone replacement therapy on cognition, emotions and quality of life in young and middle-aged hypogonadal men. Andrologia 49:22CrossRef Lasaite L, Ceponis J, Preiksa RT, Zilaitiene B (2017) Effects of two-years testosterone replacement therapy on cognition, emotions and quality of life in young and middle-aged hypogonadal men. Andrologia 49:22CrossRef
Zurück zum Zitat Lettieri A, Oleari R, Gimmelli J, ANDRé V, Cariboni A (2016) The role of semaphorin signaling in the etiology of hypogonadotropic hypogonadism. Minerva Endocrinol 41(2):266–278 Lettieri A, Oleari R, Gimmelli J, ANDRé V, Cariboni A (2016) The role of semaphorin signaling in the etiology of hypogonadotropic hypogonadism. Minerva Endocrinol 41(2):266–278
Zurück zum Zitat Liu PY, Erkkila K, Lue Y et al (2010) Genetic, hormonal, and metabolomic influences on social behaviour and sex preference of XXY mice. Am J Physiol Endocrinol Metab 299:22 Liu PY, Erkkila K, Lue Y et al (2010) Genetic, hormonal, and metabolomic influences on social behaviour and sex preference of XXY mice. Am J Physiol Endocrinol Metab 299:22
Zurück zum Zitat Lukoshe A, White T, Schmidt MN, van der Lugt A, Hokken-Koelega AC (2013) Divergent structural brain abnormalities between different genetic subtypes of children with Prader-Willi syndrome. J Neurodev Disord 5:1866–1955CrossRef Lukoshe A, White T, Schmidt MN, van der Lugt A, Hokken-Koelega AC (2013) Divergent structural brain abnormalities between different genetic subtypes of children with Prader-Willi syndrome. J Neurodev Disord 5:1866–1955CrossRef
Zurück zum Zitat Manara R, Salvalaggio A, Citton V, Palumbo V, D'Errico A, Elefante A, Briani C, Cantone E, Ottaviano G, Pellecchia MT, Greggio NA, Weis L, D'Agosto G, Rossato M, de Carlo E, Napoli E, Coppola G, di Salle F, Brunetti A, Bonanni G, Sinisi AA, Favaro A (2015) Brain anatomical substrates of mirror movements in Kallmann syndrome. NeuroImage 104:52–58. https://doi.org/10.1016/j.neuroimage.2014.09.067 PubMedCrossRef Manara R, Salvalaggio A, Citton V, Palumbo V, D'Errico A, Elefante A, Briani C, Cantone E, Ottaviano G, Pellecchia MT, Greggio NA, Weis L, D'Agosto G, Rossato M, de Carlo E, Napoli E, Coppola G, di Salle F, Brunetti A, Bonanni G, Sinisi AA, Favaro A (2015) Brain anatomical substrates of mirror movements in Kallmann syndrome. NeuroImage 104:52–58. https://​doi.​org/​10.​1016/​j.​neuroimage.​2014.​09.​067 PubMedCrossRef
Zurück zum Zitat Nand N, Mittal R, Yadav M, Venu S, Deshmukh AR (2016) Kallman Syndrome. J Assoc Physicians India 64(10):106–107PubMed Nand N, Mittal R, Yadav M, Venu S, Deshmukh AR (2016) Kallman Syndrome. J Assoc Physicians India 64(10):106–107PubMed
Zurück zum Zitat Obaydi H, Izmeth MGA, Rigby JC (1992) Kallmann's syndrome and mental handicap. J Intellect Disabil Res 36:457–460PubMedCrossRef Obaydi H, Izmeth MGA, Rigby JC (1992) Kallmann's syndrome and mental handicap. J Intellect Disabil Res 36:457–460PubMedCrossRef
Zurück zum Zitat Okoronkwo NC (2016) A rare classical presentation of Bardet-Biedl syndrome in a three-year-old male from south East Nigeria: a case report. Case Rep Clin Med 5:243CrossRef Okoronkwo NC (2016) A rare classical presentation of Bardet-Biedl syndrome in a three-year-old male from south East Nigeria: a case report. Case Rep Clin Med 5:243CrossRef
Zurück zum Zitat Poluch S, Akinola OB, Juliano SL (2012) The contribution of proliferative zones to gyral formation in a ferret model of lissencephaly in 42nd annual meeting of the Society for Neuroscience. Society for Neuroscience, New Orleans Poluch S, Akinola OB, Juliano SL (2012) The contribution of proliferative zones to gyral formation in a ferret model of lissencephaly in 42nd annual meeting of the Society for Neuroscience. Society for Neuroscience, New Orleans
Zurück zum Zitat Randy J (2011) An introduction to Behavioural endocrinology. Sinauer associates, Inc. Publishers, Ohio Randy J (2011) An introduction to Behavioural endocrinology. Sinauer associates, Inc. Publishers, Ohio
Zurück zum Zitat Resnick SM, Matsumoto AM, Stephens-Shields AJ, Ellenberg SS, Gill TM, Shumaker SA, Pleasants DD, Barrett-Connor E, Bhasin S, Cauley JA, Cella D, Crandall JP, Cunningham GR, Ensrud KE, Farrar JT, Lewis CE, Molitch ME, Pahor M, Swerdloff RS, Cifelli D, Anton S, Basaria S, Diem SJ, Wang C, Hou X, Snyder PJ (2017) Testosterone treatment and cognitive function in older men with low testosterone and age-associated memory impairment. JAMA 317(7):717–727. https://doi.org/10.1001/jama.2016.21044 PubMedPubMedCentralCrossRef Resnick SM, Matsumoto AM, Stephens-Shields AJ, Ellenberg SS, Gill TM, Shumaker SA, Pleasants DD, Barrett-Connor E, Bhasin S, Cauley JA, Cella D, Crandall JP, Cunningham GR, Ensrud KE, Farrar JT, Lewis CE, Molitch ME, Pahor M, Swerdloff RS, Cifelli D, Anton S, Basaria S, Diem SJ, Wang C, Hou X, Snyder PJ (2017) Testosterone treatment and cognitive function in older men with low testosterone and age-associated memory impairment. JAMA 317(7):717–727. https://​doi.​org/​10.​1001/​jama.​2016.​21044 PubMedPubMedCentralCrossRef
Zurück zum Zitat Simm PJ, Zacharin MR (2006) The psychosocial impact of Klinefelter syndrome--a 10 years review. J Pediatr Endocrinol Metab 19(4):499–505PubMed Simm PJ, Zacharin MR (2006) The psychosocial impact of Klinefelter syndrome--a 10 years review. J Pediatr Endocrinol Metab 19(4):499–505PubMed
Zurück zum Zitat Singh K, Kumar R, Prakash J, Krishna A (2015) Bardet-Biedl syndrome presenting with steroid sensitive nephrotic syndrome. Indian J Nephrol 25:300PubMedPubMedCentralCrossRef Singh K, Kumar R, Prakash J, Krishna A (2015) Bardet-Biedl syndrome presenting with steroid sensitive nephrotic syndrome. Indian J Nephrol 25:300PubMedPubMedCentralCrossRef
Zurück zum Zitat Sultan KT, Brown KN, Shi SH (2013) Production and organization of neocortical interneurons. Front Cell Neurosci 7:00221CrossRef Sultan KT, Brown KN, Shi SH (2013) Production and organization of neocortical interneurons. Front Cell Neurosci 7:00221CrossRef
Zurück zum Zitat Yague JG, Wang AC, Janssen WG et al (2008) Aromatase distribution in the monkey temporal neocortex and hippocampus. Brain Res 13:115–127CrossRef Yague JG, Wang AC, Janssen WG et al (2008) Aromatase distribution in the monkey temporal neocortex and hippocampus. Brain Res 13:115–127CrossRef
Metadaten
Titel
Neuroanatomical and molecular correlates of cognitive and behavioural outcomes in hypogonadal males
verfasst von
O. B. Akinola
M. O. Gabriel
Publikationsdatum
11.12.2017
Verlag
Springer US
Erschienen in
Metabolic Brain Disease / Ausgabe 2/2018
Print ISSN: 0885-7490
Elektronische ISSN: 1573-7365
DOI
https://doi.org/10.1007/s11011-017-0163-5

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