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Enhanced Adult Neural Stem Cell Population Following Bacterial Infection during Early Postnatal Life

  • Nisha Patro
  • Shrstha Sinha
  • Kavita Singh
  • Jyoti Chaudhary
  • I. K. Patro
Research Article
  • 17 Downloads

Abstract

Impaired adult hippocampal neurogenesis is a prominent feature of neurodegenerative disorders. The extent of neural stem cell (NSCs) generation in adult brain is highly adaptive and depends on both inflammatory signalling and glial cells. In this study, through immunohistochemical co-labelling of nestin and glial fibrillary acidic protein (GFAP), the authors have demonstrated an enhanced stem astrocyte density in subgranular zone of adult and ageing rats following neonatal lipopolysaccharide (LPS) exposure, which could be attributed as a regenerative attempt evoked to overcome the effects of bacterial infection. However, a second hit of LPS at 12 months of age might have killed the progenitors because of the persistent glial activation leading to a decline in stem astrocyte population. The enhanced density of NSCs is attributed to the activation of the toll-like receptor-4 (TLR-4) by LPS on their surface that in turn influences their proliferative potential. The information generated may be useful for therapeutically modulating the pathway in a way so that the TLR-4 activation following bacterial infection may be checked at a level when it triggers the activation of the innate immune response. Thus, the enhanced number of NSCs can generate a viable number of neurons that will mature and integrate in the hippocampal circuitry to compensate the loss due to bacterial infection.

Keywords

Adult neurogenesis Nestin GFAP Stem astrocytes Subgranular zone Neural stem cells Lipopolysaccharide 

Notes

Acknowledgements

The authors are thankful to Indian Council of Medical Research, Govt. of India, for financial assistance through a project grant (54/36/CFP/GER/2011-NCD-II). Facilities developed through the DBT-Human Resource Development and Bioinformatics Infrastructural facilities from Department of Biotechnology used in this study are also thankfully acknowledged.

Compliance with Ethical Standards

Conflict of interest

The authors have no conflict of interest to publish this manuscript.

References

  1. 1.
    Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319–335CrossRefGoogle Scholar
  2. 2.
    Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313–1317CrossRefGoogle Scholar
  3. 3.
    Limke TL, Rao MS (2002) Neural stem cells in aging and disease. J Cell Mol Med 6:475–496CrossRefGoogle Scholar
  4. 4.
    Spalding KL, Bergmann O, Alkass K, Bernard S, Salehpour M, Huttner HB, Bostrom E, Westerlund I, Vial C, Buchholz BA, Possnert G (2013) Dynamics of hippocampal neurogenesis in adult humans. Cell 153:1219–1227CrossRefGoogle Scholar
  5. 5.
    Ernst A, Frisen J (2015) Adult neurogenesis in humans—common and unique traits in mammals. PLoS Biol 13:e1002045.  https://doi.org/10.1371/journal.pbio.1002045 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Kempermann G, Song H, Gage FH (2015) Neurogenesis in the adult hippocampus. Cold Spring Harb Perspect Biol 7:a018812.  https://doi.org/10.1101/cshperspect.a018812 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Ming GL, Song H (2005) Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28:223–250CrossRefGoogle Scholar
  8. 8.
    Akers KG, Martinez-Canabal A, Restivo L, Yiu AP, De Cristofaro A, Hsiang HL, Wheeler AL, Guskjolen A, Niibori Y, Shoji H, Ohira K (2014) Hippocampal neurogenesis regulates forgetting during adulthood and infancy. Science 344:598–602CrossRefGoogle Scholar
  9. 9.
    Garcia AD, Doan NB, Imura T, Bush TG, Sofroniew MV (2004) GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci 7:1233CrossRefGoogle Scholar
  10. 10.
    Gonzalez-Perez O, Quinones-Hinojosa A (2012) Role of astrocytes as neural stem cells in adult brain. J Stem Cells 7:181–188PubMedPubMedCentralGoogle Scholar
  11. 11.
    Ihrie RA, Alvarez-Buylla A (2008) Cells in the astroglial lineage are neural stem cells. Cell Tissue Res 331:179–191CrossRefGoogle Scholar
  12. 12.
    Gonzalez-Perez O, Quinones-Hinojosa A (2010) A dose-dependent effect of EGF on migration and differentiation of adult subventricular zone astrocytes. Glia 58:975–983PubMedPubMedCentralGoogle Scholar
  13. 13.
    Balu DT, Lucki I (2009) Adult hippocampal neurogenesis: regulation, functional implications, and contribution to disease pathology. Neurosci Biobehav Rev 33:232–252CrossRefGoogle Scholar
  14. 14.
    Mu Y, Lee SW, Gage FH (2010) Signalling in adult neurogenesis. Curr Opin Neurobiol 20:416–423CrossRefGoogle Scholar
  15. 15.
    Liu H, Song N (2016) Molecular mechanism of adult neurogenesis and its association with human brain diseases. J Cent Nerv Syst Dis 8:5–11CrossRefGoogle Scholar
  16. 16.
    Monje ML, Toda H, Palmer TD (2003) Inflammatory blockade restores adult hippocampal neurogenesis. Science 302:1760–1765CrossRefGoogle Scholar
  17. 17.
    Ekdahl CT, Kokaia Z, Lindvall O (2009) Brain inflammation and adult neurogenesis: the dual role of microglia. Neuroscience 158:1021–1029CrossRefGoogle Scholar
  18. 18.
    Fujioka H, Akema T (2010) Lipopolysaccharide acutely inhibits proliferation of neural precursor cells in the dentate gyrus in adult rats. Brain Res 1352:35–42CrossRefGoogle Scholar
  19. 19.
    Gerber J, Bottcher T, Bering J, Bunkowski S, Brück W, Kuhnt U, Nau R (2003) Increased neurogenesis after experimental Streptococcus pneumoniae meningitis. J Neurosci Res 73:441–446CrossRefGoogle Scholar
  20. 20.
    Veena J, Rao BS, Srikumar BN (2011) Regulation of adult neurogenesis in the hippocampus by stress, acetylcholine and dopamine. J Nat Sci Biol Med 2:26–37CrossRefGoogle Scholar
  21. 21.
    Connor JR (2013) Metals and oxidative damage in neurological disorders. Springer, New YorkGoogle Scholar
  22. 22.
    Musaelyan K, Egeland M, Fernandes C, Pariante CM, Zunszain PA, Thuret S (2014) Modulation of adult hippocampal neurogenesis by early-life environmental challenges triggering immune activation. Neural Plast 2014:194396.  https://doi.org/10.1155/2014/194396 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Cameron HA, Glover LR (2015) Adult neurogenesis: beyond learning and memory. Annu Rev Psychol 66:53–81CrossRefGoogle Scholar
  24. 24.
    Cui K, Ashdown H, Luhesh GN, Boksa P (2009) Effects of prenatal immune activation on hippocampal neurogenesis in the rat. Schizophr Res 113(2–3):288–297CrossRefGoogle Scholar
  25. 25.
    Meyer U, Nyffeler M, Engler A, Urwlyer A, Schedlowski M, Knuesel I, Yee BK, Feldon J (2006) The time of prenatal immune challenge determines the specificity of inflammation mediated brain and behavioral pathology. J Neurosci 26:4752–4762CrossRefGoogle Scholar
  26. 26.
    Meyer U, Nyffeler M, Yee BK, Knuesel I, Feldon J (2008) Adult brain and behavioral pathological markers of prenatal immune challenge during early/middle and late foetal development in mice. Brain Behav Immun 22:469–486CrossRefGoogle Scholar
  27. 27.
    Mouihate A (2016) Prenatal activation of toll-like receptor-4 dampens adult hippocampal neurogenesis in an IL-6 dependent manner. Front cell Neurosci 10:173.  https://doi.org/10.3389/fncel.2016.00173 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Henry CJ, Huang Y, Wynne AM, Godbout JP (2009) Peripheral lipopolysaccharide (LPS) challenge promotes microglial hyperactivity in aged mice that is associated with exaggerated induction of both pro-inflammatory IL-1β and anti-inflammatory IL-10 cytokines. Brain Behav Immun 23(3):309–317CrossRefGoogle Scholar
  29. 29.
    Sharma A, Patro N, Patro IK (2016) Lipopolysaccharide-Induced apoptosis of astrocytes: therapeutic intervention by minocycline. Cell Mol Neurobiol 36:577–592CrossRefGoogle Scholar
  30. 30.
    Clark L, Chamberlain SR, Sahakian BJ (2009) Neurocognitive mechanisms in depression: implications for treatment. Annu Rev Neurosci 32:57–74CrossRefGoogle Scholar
  31. 31.
    Covacu R, Brundin L (2016) Endogenous spinal cord stem cells in multiple sclerosis and its animal model. J Neuroimmunol pii:S0165–5728(16)30403–9.  https://doi.org/10.1016/j.jneuroim.2016.11.006 CrossRefGoogle Scholar
  32. 32.
    Michalczyk K, Ziman M (2005) Nestin structure and predicted function in cellular cytoskeletal organisation. Histol Histopathol 20:665–671PubMedGoogle Scholar
  33. 33.
    O’callaghan JP (1991) Assessment of neurotoxicity: use of glial fibrillary acidic protein as a biomarker. Biomed Environ Sci 4:197–206PubMedGoogle Scholar
  34. 34.
    Raponi E, Agenes F, Delphin C, Assard N, Baudier J, Legraverend C, Deloulme JC (2007) S100B expression defines a state in which GFAP-expressing cells lose their neural stem cell potential and acquire a more mature developmental stage. Glia 55:165CrossRefGoogle Scholar
  35. 35.
    Steiner B, Klempin F, Wang L, Kott M, Kettenmann H, Kempermann G (2006) Type-2 cells as link between glial and neuronal lineage in adult hippocampal neurogenesis. Glia 54:805–814CrossRefGoogle Scholar
  36. 36.
    Patro N, Naik AA, Patro I (2015) Differential temporal expression of S100β in developing rat brain. Front Cell Neurosci 9:87.  https://doi.org/10.3389/fncel.2015.00087 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Horgusluoglu E, Nudelman K, Nho K, Saykin AJ (2017) Adult neurogenesis and neurodegenerative diseases: a systems biology perspective. Am J Med Genet B Neuropsychiatr Genet 174(1):93–112CrossRefGoogle Scholar
  38. 38.
    van den Berge SA, van Strien ME, Korecka JA, Dijkstra AA, Sluijs JA, Kooijman L, Eggers R, De Filippis L, Vescovi AL, Verhaagen J, van de Berg WD (2011) The proliferative capacity of the subventricular zone is maintained in the parkinsonian brain. Brain 134(11):3249–3263CrossRefGoogle Scholar
  39. 39.
    Winner B, Winkler J (2015) Adult neurogenesis in neurodegenerative diseases. Cold Spring Harb Perspect Biol 7:a021287.  https://doi.org/10.1101/cshperspect.a021287 CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Liu Z, Martin LJ (2006) The adult neural stem and progenitor cell niche is altered in amyotrophic lateral sclerosis mouse brain. J Comp Neurol 497:468–488CrossRefGoogle Scholar
  41. 41.
    Chi L, Ke Y, Luo C, Li B, Gozal D, Kalyanaraman B, Liu R (2006) Motor neuron degeneration promotes neural progenitor cell proliferation, migration and neurogenesis in the spinal cords of amyotrophic lateral sclerosis mice. Stem Cells 24(1):34–43CrossRefGoogle Scholar
  42. 42.
    Galan L, Gomez-Pinedo U, Vela-Souto A, Guerrero-Sola A, Barcia JA, Gutierrez AR, Martinez-Martinez A, Jiménez MS, García-Verdugo JM, Matias-Guiu J (2011) Subventricular zone in motor neuron disease with frontotemporal dementia. Neurosci Lett 499:9–13CrossRefGoogle Scholar
  43. 43.
    Goodell MA, Rando TA (2015) Stem cells and healthy aging. Science 350:1199–1204CrossRefGoogle Scholar
  44. 44.
    Artandi SE, Blau HM, de Haan G (2015) Stem cells and aging: what next. Stem Cell 16:578–581Google Scholar
  45. 45.
    Naninck EF, Hoeijmakers L, Kakava-Georgiadou N, Meesters A, Lazic SE, Lucassen PJ, Korosi A (2015) Chronic early life stress alters developmental and adult neurogenesis and impairs cognitive function in mice. Hippocampus 25:309–328CrossRefGoogle Scholar
  46. 46.
    Naik AA, Patro N, Seth P, Patro IK (2017) Intra-generational protein malnutrition impairs temporal astrogenesis in rat brain. Biol Open 6:931–942.  https://doi.org/10.1242/bio.23432 CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Kim JJ, Song EY, Kosten TA (2006) Stress effects in the hippocampus: synaptic plasticity and the memory. Stress 9:1–11CrossRefGoogle Scholar
  48. 48.
    Jin K, Minami M, Lan JQ, Mao XO, Batteur S, Simon RP, Greenberg DA (2001) Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc Natl Acad Sci USA 98(8):4710–4715CrossRefGoogle Scholar
  49. 49.
    Zhu DY, Liu SH, Sun HS, Lu YM (2003) Expression of inducible nitric oxide synthase after focal cerebral ischemia stimulates neurogenesis in the adult rodent dentate gyrus. J Neurosci 23:223–229CrossRefGoogle Scholar
  50. 50.
    Bernabeu R, Sharp FR (2000) NMDA and AMPA/kainate glutamate receptors modulate dentate neurogenesis and CA3 synapsin-1 in normal and ischemic hippocampus. J Cereb Blood Flow Metab 20:1669CrossRefGoogle Scholar
  51. 51.
    Zhang R, Zhang L, Zhang Z, Wang Y, Lu M, LaPointe M, Chopp M (2001) A nitric oxide donor induces neurogenesis and reduces functional deficits after stroke in rats. Ann Neurol 50:602–611CrossRefGoogle Scholar
  52. 52.
    Bhattacharyya BJ, Banisadr G, Jung H, Ren D, Cronshaw DG, Zou Y, Miller RJ (2008) The chemokine stromal cell-derived factor-1 regulates GABAergic inputs to neural progenitors in the postnatal dentate gyrus. J Neurosci 28:6720–6730CrossRefGoogle Scholar
  53. 53.
    Carpentier PA, Palmer TD (2009) Immune influence on adult neural stem cell regulation and function. Neuron 64(1):72–92CrossRefGoogle Scholar
  54. 54.
    Ye Y, Xu H, Zhang X, Li Z, Jia Y, He X, Huang JH (2014) Association between toll-like receptor 4 expression and neural stem cell proliferation in the hippocampus following traumatic brain injury in mice. Int J Mol Sci 15(7):12651–12664CrossRefGoogle Scholar

Copyright information

© The National Academy of Sciences, India 2018

Authors and Affiliations

  • Nisha Patro
    • 1
  • Shrstha Sinha
    • 1
    • 2
  • Kavita Singh
    • 1
  • Jyoti Chaudhary
    • 1
  • I. K. Patro
    • 1
    • 2
  1. 1.School of Studies in NeuroscienceJiwaji UniversityGwaliorIndia
  2. 2.School of Studies in ZoologyJiwaji UniversityGwaliorIndia

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