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Postnatal changes in glucose transporter 3 expression in the dentate gyrus of the C57BL/6 mouse model

Abstract

In this study, we observed the ontogenetic changes in glucose transporter 3 (GLUT3) immunoreactivity, a major neuronal GLUT, in the dentate gyrus of mouse brains at various ages: postnatal day (P) 1, 7, 14, 28, and 56. At P1, cresyl violet staining showed abundant neurons in the dentate gyrus, whereas the granule cell layer was ill-defined. At P7, the granule cell layer was observed, and cresyl violet-positive cells were dispersed throughout the polymorphic layer. At P14, the granule cell layer was well-defined, and cresyl violet positive cells were detected abundantly in the polymorphic layer. At P28 and P56, cresyl violet-positive cells were observed in the granule cell layer, as well as in the polymorphic layer. At P1, GLUT3 immunoreactivity was detected in the dentate gyrus. At P7, GLUT3 immunoreactive cells were scattered in the polymorphic and molecular layer. However, at P14, GLUT3 immunoreactivity was observed in the polymorphic layer as well as subgranular zone of the dentate gyrus. At P28, GLUT3 immunoreactivity was detected in the polymorphic layer of the dentate gyrus. At P56, GLUT3 immunoreactivity was observed predominantly in the subgranular zone of the dentate gyrus. GLUT3 immunoreactive cells were mainly colocalized with doublecortin, which is a marker for differentiated neuroblasts, in the polymorphic layer and subgranular zone of dentate gyrus at P14 and P56. These results suggest that the expression of GLUT3 is closely associated with postnatal development of the dentate gyrus and adult neurogenesis.

References

  1. Pellegrini M, Mansouri A, Simeone A, Boncinelli E, Gruss P. Dentate gyrus formation requires Emx2. Development 1996; 122(12): 3893–3898.

    Google Scholar 

  2. Bayer SA. Development of the hippocampal region in the rat. II. Morphogenesis during embryonic and early postnatal life. J Comp Neurol 1980; 190(4): 115–134.

    Article  CAS  Google Scholar 

  3. Schlessinger AR, Cowan WM, Gottlieb DI. An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat. J Comp Neurol 1975; 159(4): 149- 175.

    Google Scholar 

  4. Ngwenya LB, Heyworth NC, Shwe Y, Moore TL, Rosene DL. Age-related changes in dentate gyrus cell numbers, neurogenesis, and associations with cognitive impairments in the rhesus monkey. Front Syst Neurosci 2015; 9: 102.

  5. Ortega-Martínez S. A new perspective on the role of the CREB family of transcription factors in memory consolidation via adult hippocampal neurogenesis. Front Mol Neurosci 2015; 8: 46.

    Article  Google Scholar 

  6. Siegel GJ, Agranoff BW, Wayne Albers R, Fisher SK, Uhler MD. Basic Neurochemistry: Molecular, Cellular and Medical Aspects. Lippincott-Raven, Philadelphia, 2005; pp 637-670.

    Google Scholar 

  7. Simpson IA, Dwyer D, Malide D, Moley KH, Travis A, Vannucci SJ. The facilitative glucose transporter GLUT3: 20 years of distinction. Am J Physiol Endocrinol Metab 2008; 295(4): E242-253.

    Google Scholar 

  8. Vannucci SJ, Maher F, Simpson IA. Glucose transporter proteins in brain: delivery of glucose to neurons and glia. Glia 1997; 21(3): 2–21.

    Article  CAS  Google Scholar 

  9. Guo X, Geng M, Du G. Glucose transporter 1, distribution in the brain and in neural disorders: its relationship with transport of neuroactive drugs through the blood-brain barrier. Biochem Genet 2005; 43(3-4): 175–187.

    Google Scholar 

  10. Maher F, Vannucci SJ, Simpson IA. Glucose transporter proteins in brain. FASEB J 1994; 8(13): 1003–1011.

    Google Scholar 

  11. Nehlig A, de Vasconcelos AP, Boyet S. Quantitative autoradiographic measurement of local cerebral glucose utilization in freely moving rats during postnatal development. J Neurosci 1988; 8(2): 2321–2333.

    Article  CAS  Google Scholar 

  12. Vannucci RC, Christensen MA, Stein DT. Regional cerebral glucose utilization in the immature rat: effect of hypoxiaischemia. Pediatr Res 1989; 26(3): 208–214.

    Article  CAS  Google Scholar 

  13. Altman J, Das GD. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 1965; 124(4): 319–335.

    Article  CAS  Google Scholar 

  14. Bayer SA, Altman J. Hippocampal development in the rat: cytogenesis and morphogenesis examined with autoradiography and low-level X-irradiation. J Comp Neurol 1974; 158(4): 55–79.

    Article  CAS  Google Scholar 

  15. Yoo DY, Yoo KY, Park JH, Choi JW, Kim W, Hwang IK, Won MH. Detailed differentiation of calbindin d-28k-immunoreactive cells in the dentate gyrus in C57BL/6 mice at early postnatal stages. Lab Anim Res 2011; 27(3): 153–159.

    Article  Google Scholar 

  16. Hebel R, Stromberg MW. Anatomy and Embryology of the Laboratory Rat. BioMed Verlag, W örthsee, 1986.

    Google Scholar 

  17. Vannucci SJ. Developmental expression of GLUT1 and GLUT3 glucose transporters in rat brain. J Neurochem 1994; 62(3): 240–246.

    CAS  PubMed  Google Scholar 

  18. Aghajanian GK, Bloom FE. The formation of synaptic junctions in developing rat brain: a quantitative electron microscopic study. Brain Res 1967; 6(2): 716–727.

    Article  CAS  Google Scholar 

  19. Ghosh A, Greenberg ME. Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science 1995; 268(5208): 239–247.

    Article  CAS  Google Scholar 

  20. Riccio A, Ahn S, Davenport CM, Blendy JA, Ginty DD. Mediation by a CREB family transcription factor of NGFdependent survival of sympathetic neurons. Science 1999; 286(5448): 2358–2361.

    Article  CAS  Google Scholar 

  21. Jin N, Qian W, Yin X, Zhang L, Iqbal K, Grundke-Iqbal I, Gong CX, Liu F. CREB regulates the expression of neuronal glucose transporter 3: a possible mechanism related to impaired brain glucose uptake in Alzheimer’s disease. Nucleic Acids Res 2013; 41(3): 3240–3256.

    Article  CAS  Google Scholar 

  22. Rajakumar A, Thamotharan S, Raychaudhuri N, Menon RK, Devaskar SU. Trans-activators regulating neuronal glucose transporter isoform-3 gene expression in mammalian neurons. J Biol Chem 2004; 279(25): 26768–26779.

    Article  CAS  Google Scholar 

  23. Rajakumar RA, Thamotharan S, Menon RK, Devaskar SU. Sp1 and Sp3 regulate transcriptional activity of the facilitative glucose transporter isoform-3 gene in mammalian neuroblasts and trophoblasts. J Biol Chem 1998; 273(42): 27474–27483.

    Article  CAS  Google Scholar 

  24. Reddy AB, Srivastava SK, Ramana KV. Aldose reductase inhibition prevents lipopolysaccharide-induced glucose uptake and glucose transporter 3 expression in RAW264.7 macrophages. Int J Biochem Cell Biol 2010; 42(3): 1039–1045.

    Article  CAS  Google Scholar 

  25. Hwang IK, Yoo KY, Yoo DY, Choi JW, Lee CH, Choi JH, Yoon YS, Won MH. Time-course of changes in phosphorylated CREB in neuroblasts and BDNF in the mouse dentate gyrus at early postnatal stages. Cell Mol Neurobiol 2011; 31(3): 669–674.

    Article  CAS  Google Scholar 

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Correspondence to In Koo Hwang.

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Jung, H.Y., Yim, H.S., Yoo, D.Y. et al. Postnatal changes in glucose transporter 3 expression in the dentate gyrus of the C57BL/6 mouse model. Lab Anim Res 32, 1–7 (2016). https://doi.org/10.5625/lar.2016.32.1.1

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