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Gender differences in doublecortin expression in the dentate gyrus of the Wistar rat during development

Year 2020, Volume: 14 Issue: 2, 111 - 116, 31.08.2020

Abstract

Objectives: Neurogenesis is the formation process of functional neurons from progenitor cells which continues during lifetime. Alterations in neurogenesis is associated with neurodegenerative disorders (ND). Different mechanisms underlie the ND in males and females which may be related to neurogenesis. In this study, we aimed to investigate the developmental process of neurogenesis in the hippocampus of male and female rats at different ages and shed light on the effect of gender difference on ND.
Methods: Brains were obtained from 7, 14, 21 days and 3-month-old male and female Wistar rats following intracardiac perfusion and processed for immunohistochemical and immunoflorescence staining. Doublecortin protein (DCX) was used as a marker of newly-born neuroblasts to determine neurogenesis.
Results: DCX immunoreactive (-ir) cells were dispersed throughout the granular and subgranular layers of DG in 7-days-old group in both genders. However, in the 14 and 21 days old groups, DCX-ir cells were observed only in the subgranular zone in the sections labelled with both immunohistochemistry (IHC) and immunoflourescent (IF) methods. In all age groups, female rats had a tendency to increase in DCX immunoreactivity when compared to that of male Wistar rats.
Conclusion: DCX-ir cells may be localized in different parts of DG during development. The number of newly born neurons showed a tendency to increase in female rats in all groups. Further studies are needed to understand the reason for differences in the normal developmental neurogenesis process between two genders.

Supporting Institution

Research Fund of the Marmara University

Project Number

SAG-K-081117-0608

References

  • Ming GL, Song H. Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 2011;70:687–702.
  • Altman J, Das GD. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 1965;124: 319–35.
  • Paton JA, Nottebohm FN. Neurons generated in the adult brain are recruited into functional circuits. Science 1984;225:1046–8.
  • Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992;255:1707–10.
  • Eriksson PS, Perfilieva E, Björk-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH. Neurogenesis in the adult human hippocampus. Nat Med 1998;4:1313–7.
  • Gage FH. Mammalian neural stem cells. Science 2000;287:1433–8.
  • Zhao C, Teng EM, Summers RG, Jr., Ming GL, Gage FH. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 2006;26:3–11.
  • Kempermann G, Jessberger S, Steiner B, Kronenberg G. Milestones of neuronal development in the adult hippocampus. Trends Neurosci 2004;27:447–52.
  • Gleeson JG, Lin PT, Flanagan LA, Walsh CA. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 1999;23:257–71.
  • Plumpe T, Ehninger D, Steiner B, Klempin F, Jessberger S, Brandt M, Römer B, Rodrigues GR, Kronenberg G, Kempermann G. Variability of doublecortin-associated dendrite maturation in adult hippocampal neurogenesis is independent of the regulation of precursor cell proliferation. BMC Neurosci 2006;7:77.
  • 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;467:1–10.
  • Levine S. Sex differences in the brain. Scientific American 1966;214: 84–90.
  • Sacher J, Neumann J, Okon-Singer H, Gotowiec S, Villringer A. Sexual dimorphism in the human brain: evidence from neuroimaging. Magn Reson Imaging 2013;31:366–75.
  • Bao AM, Swaab DF. Sex differences in the brain, behavior, and neuropsychiatric disorders. Neuroscientist 2010;16:550–65.
  • Baron-Cohen S, Lombardo MV, Auyeung B, Ashwin E, Chakrabarti B, Knickmeyer R. Why are autism spectrum conditions more prevalent in males? PLoS Biol 2011;9:e1001081.
  • Lenz KM, Nugent BM, Haliyur R, McCarthy MM. Microglia are essential to masculinization of brain and behavior. J Neurosci 2013; 33:2761–72.
  • Arnold AP, Chen X. What does the “four core genotypes” mouse model tell us about sex differences in the brain and other tissues? Front Neuroendocrinol 2009;30:1–9.
  • Phoenix CH. Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Horm Behav 2009;55:566.
  • Arnold AP, Breedlove SM. Organizational and activational effects of sex steroids on brain and behavior: a reanalysis. Horm Behav 1985; 19:469–98.
  • 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;975:22–36.
  • Hillerer KM, Neumann ID, Couillard-Despres S, Aigner L, Slattery DA. Sex-dependent regulation of hippocampal neurogenesis under basal and chronic stress conditions in rats. Hippocampus 2013;23: 476–87.
  • Cahill L. Why sex matters for neuroscience. Nature Rev Neurosci 2006;7:477–84.
  • Goldstein JM, Seidman LJ, Horton NJ, Makris N, Kennedy DN, Caviness VS Jr, Faraone SV, Tsuang MT. Normal sexual dimorphism of the adult human brain assessed by in vivo magnetic resonance imaging. Cereb Cortex 2001;11:490–7.
  • Madeira MD, Lieberman AR. Sexual dimorphism in the mammalian limbic system. Prog Neurobiol 1995;45:275–333.
  • Teyler TJ, Vardaris RM, Lewis D, Rawitch AB. Gonadal steroids: effects on excitability of hippocampal pyramidal cells. Science 1980; 209:1017–8.
  • Cooke BM, Woolley CS. Gonadal hormone modulation of dendrites in the mammalian CNS. J Neurobiol 2005;64:34–46.
  • Pazar A, Kolgazi M, Memisoglu A, Bahadir E, Sirvanci S, Yaman A, Yegen BÇ, Ozek E. The neuroprotective and anti-apoptotic effects of melatonin on hemolytic hyperbilirubinemia-induced oxidative brain damage. J Pineal Res 2016;60:74–83.
  • Goffinet AM, Rakic P. Mouse brain development. Results and problems in cell differentiation. Heidelberg: Springer; 2000.
  • Spritzer MD, Panning AW, Engelman SM, Prince WT, Casler AE, Georgakas JE, Jaeger ECB, Nelson LR, Roy EA, Wagner BA. Seasonal and sex differences in cell proliferation, neurogenesis, and cell death within the dentate gyrus of adult wild-caught meadow voles. Neuroscience 2017;360:155–65.
  • Spampanato J, Sullivan RK, Turpin FR, Bartlett PF, Sah P. Properties of doublecortin expressing neurons in the adult mouse dentate gyrus. PloS One 2012;7:e41029.
  • Moreno-Jiménez EP, Flor-García M, Terreros-Roncal J, Rábano A, Cafini F, Pallas-Bazarra N, Avila J, Llorens-Martin M. Adult hippocampal neurogenesis is abundant in neurologically healthy subjects and drops sharply in patients with Alzheimer’s disease. Nat Med 2019;25:554–60.
Year 2020, Volume: 14 Issue: 2, 111 - 116, 31.08.2020

Abstract

Project Number

SAG-K-081117-0608

References

  • Ming GL, Song H. Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 2011;70:687–702.
  • Altman J, Das GD. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 1965;124: 319–35.
  • Paton JA, Nottebohm FN. Neurons generated in the adult brain are recruited into functional circuits. Science 1984;225:1046–8.
  • Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992;255:1707–10.
  • Eriksson PS, Perfilieva E, Björk-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH. Neurogenesis in the adult human hippocampus. Nat Med 1998;4:1313–7.
  • Gage FH. Mammalian neural stem cells. Science 2000;287:1433–8.
  • Zhao C, Teng EM, Summers RG, Jr., Ming GL, Gage FH. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 2006;26:3–11.
  • Kempermann G, Jessberger S, Steiner B, Kronenberg G. Milestones of neuronal development in the adult hippocampus. Trends Neurosci 2004;27:447–52.
  • Gleeson JG, Lin PT, Flanagan LA, Walsh CA. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 1999;23:257–71.
  • Plumpe T, Ehninger D, Steiner B, Klempin F, Jessberger S, Brandt M, Römer B, Rodrigues GR, Kronenberg G, Kempermann G. Variability of doublecortin-associated dendrite maturation in adult hippocampal neurogenesis is independent of the regulation of precursor cell proliferation. BMC Neurosci 2006;7:77.
  • 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;467:1–10.
  • Levine S. Sex differences in the brain. Scientific American 1966;214: 84–90.
  • Sacher J, Neumann J, Okon-Singer H, Gotowiec S, Villringer A. Sexual dimorphism in the human brain: evidence from neuroimaging. Magn Reson Imaging 2013;31:366–75.
  • Bao AM, Swaab DF. Sex differences in the brain, behavior, and neuropsychiatric disorders. Neuroscientist 2010;16:550–65.
  • Baron-Cohen S, Lombardo MV, Auyeung B, Ashwin E, Chakrabarti B, Knickmeyer R. Why are autism spectrum conditions more prevalent in males? PLoS Biol 2011;9:e1001081.
  • Lenz KM, Nugent BM, Haliyur R, McCarthy MM. Microglia are essential to masculinization of brain and behavior. J Neurosci 2013; 33:2761–72.
  • Arnold AP, Chen X. What does the “four core genotypes” mouse model tell us about sex differences in the brain and other tissues? Front Neuroendocrinol 2009;30:1–9.
  • Phoenix CH. Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Horm Behav 2009;55:566.
  • Arnold AP, Breedlove SM. Organizational and activational effects of sex steroids on brain and behavior: a reanalysis. Horm Behav 1985; 19:469–98.
  • 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;975:22–36.
  • Hillerer KM, Neumann ID, Couillard-Despres S, Aigner L, Slattery DA. Sex-dependent regulation of hippocampal neurogenesis under basal and chronic stress conditions in rats. Hippocampus 2013;23: 476–87.
  • Cahill L. Why sex matters for neuroscience. Nature Rev Neurosci 2006;7:477–84.
  • Goldstein JM, Seidman LJ, Horton NJ, Makris N, Kennedy DN, Caviness VS Jr, Faraone SV, Tsuang MT. Normal sexual dimorphism of the adult human brain assessed by in vivo magnetic resonance imaging. Cereb Cortex 2001;11:490–7.
  • Madeira MD, Lieberman AR. Sexual dimorphism in the mammalian limbic system. Prog Neurobiol 1995;45:275–333.
  • Teyler TJ, Vardaris RM, Lewis D, Rawitch AB. Gonadal steroids: effects on excitability of hippocampal pyramidal cells. Science 1980; 209:1017–8.
  • Cooke BM, Woolley CS. Gonadal hormone modulation of dendrites in the mammalian CNS. J Neurobiol 2005;64:34–46.
  • Pazar A, Kolgazi M, Memisoglu A, Bahadir E, Sirvanci S, Yaman A, Yegen BÇ, Ozek E. The neuroprotective and anti-apoptotic effects of melatonin on hemolytic hyperbilirubinemia-induced oxidative brain damage. J Pineal Res 2016;60:74–83.
  • Goffinet AM, Rakic P. Mouse brain development. Results and problems in cell differentiation. Heidelberg: Springer; 2000.
  • Spritzer MD, Panning AW, Engelman SM, Prince WT, Casler AE, Georgakas JE, Jaeger ECB, Nelson LR, Roy EA, Wagner BA. Seasonal and sex differences in cell proliferation, neurogenesis, and cell death within the dentate gyrus of adult wild-caught meadow voles. Neuroscience 2017;360:155–65.
  • Spampanato J, Sullivan RK, Turpin FR, Bartlett PF, Sah P. Properties of doublecortin expressing neurons in the adult mouse dentate gyrus. PloS One 2012;7:e41029.
  • Moreno-Jiménez EP, Flor-García M, Terreros-Roncal J, Rábano A, Cafini F, Pallas-Bazarra N, Avila J, Llorens-Martin M. Adult hippocampal neurogenesis is abundant in neurologically healthy subjects and drops sharply in patients with Alzheimer’s disease. Nat Med 2019;25:554–60.
There are 31 citations in total.

Details

Primary Language English
Subjects Health Care Administration
Journal Section Original Articles
Authors

Özlem Tuğçe Çilingir-kaya 0000-0002-2591-9174

Sercan Yıldız This is me 0000-0002-2971-2402

Nişva Levent This is me 0000-0003-0525-2162

Esra Bihter Gürler 0000-0001-8259-521X

Ümit Şehirli 0000-0001-6261-4567

Serap Sirvancı 0000-0001-7683-4587

Project Number SAG-K-081117-0608
Publication Date August 31, 2020
Published in Issue Year 2020 Volume: 14 Issue: 2

Cite

APA Çilingir-kaya, Ö. T., Yıldız, S., Levent, N., Gürler, E. B., et al. (2020). Gender differences in doublecortin expression in the dentate gyrus of the Wistar rat during development. Anatomy, 14(2), 111-116.
AMA Çilingir-kaya ÖT, Yıldız S, Levent N, Gürler EB, Şehirli Ü, Sirvancı S. Gender differences in doublecortin expression in the dentate gyrus of the Wistar rat during development. Anatomy. August 2020;14(2):111-116.
Chicago Çilingir-kaya, Özlem Tuğçe, Sercan Yıldız, Nişva Levent, Esra Bihter Gürler, Ümit Şehirli, and Serap Sirvancı. “Gender Differences in Doublecortin Expression in the Dentate Gyrus of the Wistar Rat During Development”. Anatomy 14, no. 2 (August 2020): 111-16.
EndNote Çilingir-kaya ÖT, Yıldız S, Levent N, Gürler EB, Şehirli Ü, Sirvancı S (August 1, 2020) Gender differences in doublecortin expression in the dentate gyrus of the Wistar rat during development. Anatomy 14 2 111–116.
IEEE Ö. T. Çilingir-kaya, S. Yıldız, N. Levent, E. B. Gürler, Ü. Şehirli, and S. Sirvancı, “Gender differences in doublecortin expression in the dentate gyrus of the Wistar rat during development”, Anatomy, vol. 14, no. 2, pp. 111–116, 2020.
ISNAD Çilingir-kaya, Özlem Tuğçe et al. “Gender Differences in Doublecortin Expression in the Dentate Gyrus of the Wistar Rat During Development”. Anatomy 14/2 (August 2020), 111-116.
JAMA Çilingir-kaya ÖT, Yıldız S, Levent N, Gürler EB, Şehirli Ü, Sirvancı S. Gender differences in doublecortin expression in the dentate gyrus of the Wistar rat during development. Anatomy. 2020;14:111–116.
MLA Çilingir-kaya, Özlem Tuğçe et al. “Gender Differences in Doublecortin Expression in the Dentate Gyrus of the Wistar Rat During Development”. Anatomy, vol. 14, no. 2, 2020, pp. 111-6.
Vancouver Çilingir-kaya ÖT, Yıldız S, Levent N, Gürler EB, Şehirli Ü, Sirvancı S. Gender differences in doublecortin expression in the dentate gyrus of the Wistar rat during development. Anatomy. 2020;14(2):111-6.

Anatomy is the official journal of Turkish Society of Anatomy and Clinical Anatomy (TSACA).