Modulation of Adult Hippocampal Neurogenesis by Early-life Environmental Challenges Triggering Immune Activation

Overview

Journal Neural Plast

Specialty Neurology

Date 2014 Jun 4

PMID 24891958

Citations 21

Authors

Ksenia Musaelyan

Martin Egeland

Cathy Fernandes

Carmine M Pariante

Patricia A Zunszain

Sandrine Thuret

Affiliations

Soon will be listed here.

Abstract

The immune system plays an important role in the communication between the human body and the environment, in early development as well as in adulthood. Per se, research has shown that factors such as maternal stress and nutrition as well as maternal infections can activate the immune system in the infant. A rising number of research studies have shown that activation of the immune system in early life can augment the risk of some psychiatric disorders in adulthood, such as schizophrenia and depression. The mechanisms of such a developmental programming effect are unknown; however some preliminary evidence is emerging in the literature, which suggests that adult hippocampal neurogenesis may be involved. A growing number of studies have shown that pre- and postnatal exposure to an inflammatory stimulus can modulate the number of proliferating and differentiating neural progenitors in the adult hippocampus, and this can have an effect on behaviours of relevance to psychiatric disorders. This review provides a summary of these studies and highlights the evidence supporting a neurogenic hypothesis of immune developmental programming.

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References

Bilbo S, Biedenkapp J, Der-Avakian A, Watkins L, Rudy J, Maier S . Neonatal infection-induced memory impairment after lipopolysaccharide in adulthood is prevented via caspase-1 inhibition. J Neurosci. 2005; 25(35):8000-9. PMC: 6725459. DOI: 10.1523/JNEUROSCI.1748-05.2005. View

Jiang P, Sun Y, Zhu T, Zhan C, Gu W, Yuan T . Endogenous neurogenesis in the hippocampus of developing rat after intrauterine infection. Brain Res. 2012; 1459:1-14. DOI: 10.1016/j.brainres.2012.03.058. View

Jiang P, Zhu T, Zhao W, Shen J, Yu Y, Xu J . The persistent effects of maternal infection on the offspring's cognitive performance and rates of hippocampal neurogenesis. Prog Neuropsychopharmacol Biol Psychiatry. 2013; 44:279-89. DOI: 10.1016/j.pnpbp.2013.03.007. View

Meyer U, Nyffeler M, Engler A, Urwyler A, Schedlowski M, Knuesel I . The time of prenatal immune challenge determines the specificity of inflammation-mediated brain and behavioral pathology. J Neurosci. 2006; 26(18):4752-62. PMC: 6674174. DOI: 10.1523/JNEUROSCI.0099-06.2006. View

Bilbo S, Levkoff L, Mahoney J, Watkins L, Rudy J, Maier S . Neonatal infection induces memory impairments following an immune challenge in adulthood. Behav Neurosci. 2005; 119(1):293-301. DOI: 10.1037/0735-7044.119.1.293. View

Marques A, OConnor T, Roth C, Susser E, Bjorke-Monsen A . The influence of maternal prenatal and early childhood nutrition and maternal prenatal stress on offspring immune system development and neurodevelopmental disorders. Front Neurosci. 2013; 7:120. PMC: 3728489. DOI: 10.3389/fnins.2013.00120. View

Zunszain P, Anacker C, Cattaneo A, Choudhury S, Musaelyan K, Myint A . Interleukin-1β: a new regulator of the kynurenine pathway affecting human hippocampal neurogenesis. Neuropsychopharmacology. 2011; 37(4):939-49. PMC: 3280640. DOI: 10.1038/npp.2011.277. View

Spalding K, Bergmann O, Alkass K, Bernard S, Salehpour M, Huttner H . Dynamics of hippocampal neurogenesis in adult humans. Cell. 2013; 153(6):1219-1227. PMC: 4394608. DOI: 10.1016/j.cell.2013.05.002. View

Rodriguez-Martinez G, Velasco I . Activin and TGF-β effects on brain development and neural stem cells. CNS Neurol Disord Drug Targets. 2012; 11(7):844-55. DOI: 10.2174/1871527311201070844. View

10.

Atladottir H, Thorsen P, Ostergaard L, Schendel D, Lemcke S, Abdallah M . Maternal infection requiring hospitalization during pregnancy and autism spectrum disorders. J Autism Dev Disord. 2010; 40(12):1423-30. DOI: 10.1007/s10803-010-1006-y. View

11.

Walker A, Nakamura T, Byrne R, Naicker S, Tynan R, Hunter M . Neonatal lipopolysaccharide and adult stress exposure predisposes rats to anxiety-like behaviour and blunted corticosterone responses: implications for the double-hit hypothesis. Psychoneuroendocrinology. 2009; 34(10):1515-25. DOI: 10.1016/j.psyneuen.2009.05.010. View

12.

Schwarz T, Ebert B, Lie D . Stem cell maintenance in the adult mammalian hippocampus: a matter of signal integration?. Dev Neurobiol. 2012; 72(7):1006-15. DOI: 10.1002/dneu.22026. View

13.

OConnor T, Winter M, Hunn J, Carnahan J, Pressman E, Glover V . Prenatal maternal anxiety predicts reduced adaptive immunity in infants. Brain Behav Immun. 2013; 32:21-8. PMC: 3686987. DOI: 10.1016/j.bbi.2013.02.002. View

14.

Walker A, Nakamura T, Hodgson D . Neonatal lipopolysaccharide exposure alters central cytokine responses to stress in adulthood in Wistar rats. Stress. 2010; 13(6):506-15. DOI: 10.3109/10253890.2010.489977. View

15.

Jarlestedt K, Naylor A, Dean J, Hagberg H, Mallard C . Decreased survival of newborn neurons in the dorsal hippocampus after neonatal LPS exposure in mice. Neuroscience. 2013; 253:21-8. PMC: 3824076. DOI: 10.1016/j.neuroscience.2013.08.040. View

16.

Giovanoli S, Engler H, Engler A, Richetto J, Voget M, Willi R . Stress in puberty unmasks latent neuropathological consequences of prenatal immune activation in mice. Science. 2013; 339(6123):1095-9. DOI: 10.1126/science.1228261. View

17.

Lin Y, Wang S . Prenatal lipopolysaccharide exposure increases depression-like behaviors and reduces hippocampal neurogenesis in adult rats. Behav Brain Res. 2013; 259:24-34. DOI: 10.1016/j.bbr.2013.10.034. View

18.

Teixeira C, Kron M, Masachs N, Zhang H, Lagace D, Martinez A . Cell-autonomous inactivation of the reelin pathway impairs adult neurogenesis in the hippocampus. J Neurosci. 2012; 32(35):12051-65. PMC: 3475414. DOI: 10.1523/JNEUROSCI.1857-12.2012. View

19.

Danese A, Moffitt T, Pariante C, Ambler A, Poulton R, Caspi A . Elevated inflammation levels in depressed adults with a history of childhood maltreatment. Arch Gen Psychiatry. 2008; 65(4):409-15. PMC: 2923056. DOI: 10.1001/archpsyc.65.4.409. View

20.

OConnor T, Moynihan J, Caserta M . Annual research review: The neuroinflammation hypothesis for stress and psychopathology in children--developmental psychoneuroimmunology. J Child Psychol Psychiatry. 2013; 55(6):615-31. PMC: 4029900. DOI: 10.1111/jcpp.12187. View