Trends in Neurosciences
Volume 35, Issue 12, December 2012, Pages 733-741
Journal home page for Trends in Neurosciences

Review
A vitamin for the brain

https://doi.org/10.1016/j.tins.2012.08.005Get rights and content

In the central nervous system (CNS) the function of retinoic acid, the active metabolite of vitamin A, is best understood from its action in guiding embryonic development; as development comes to completion, retinoic acid signaling declines. However, it is increasingly recognized that this signaling mechanism does not disappear in the adult brain but becomes more regionally focused and takes on new roles. These functions are often tied to processes of neural plasticity whether in the hippocampus, through homeostatic neural plasticity, the olfactory bulb or the hypothalamus. The role of retinoic acid in the control of plastic processes has led to suggestions of its involvement in neural disorders, both degenerative and psychiatric. This review presents a snapshot of developments in these areas over recent years.

Introduction

Since its discovery in 1913 [1], vitamin A has been closely tied to the function of the CNS, initially from the discovery of its requirement for vision and soon after from the importance of vitamin A in embryonic development in both the eye and brain. The primary mechanism by which vitamin A regulates CNS development, as well as much of its action in the body, is through its oxidation to the active metabolite, retinoic acid (RA; Figure 1). Its function in the embryonic CNS includes two crucial actions: (i) induction of neurogenesis and (ii) control of neuronal patterning [2]. The latter includes patterning along the anterior–posterior axis, where it may function as a morphogen, determining cell fate according to concentration. The concentration dependence of the effects of RA and its action in regulating patterning through the formation of gradients results in high embryonic sensitivity to disruption when RA levels are too low (deficiency syndrome) or too high (teratogenicity). A number of factors that shape the developing CNS later function in the adult brain to regulate neuroplasticity, and RA is no exception in its action on the adult hippocampus olfactory bulb, and hypothalamus. Because of its key roles in these processes, it is unsurprising that RA function is also implicated in several brain disorders. Some of the new findings in these fields are discussed below.

Section snippets

Neuronal plasticity homeostasis in the hippocampus

Hippocampal long-term potentiation (LTP) and long-term depression (LTD), believed to be essential components of hippocampal-dependent memory, are both dependent on vitamin A and RA [3]. Research on such synaptic effects has continued and recent studies in which a dominant-negative retinoic acid receptor (RAR)α was expressed in mouse forebrain revealed impaired LTP and AMPA receptor (AMPAR)-mediated synapse transmission in the hippocampus, together with reduced social recognition and spatial

RA as part of the seasonal switch in the hypothalamus

The hypothalamus is the primary region of the brain that regulates reproductive status, hormone release, feeding, and energy balance. Recent studies using a seasonal switch to manipulate hypothalamic function (Box 1) have pointed to a crucial role for RA in this region. Certainly many components of the RA signaling pathway are expressed in the hypothalamus (Figure 3) 31, 32, 33. Expression is predominantly localized to three main regions: the arcuate nucleus, known to regulate feeding behavior

Vitamin A for a healthy brain

The World Health Organization (WHO) includes vitamin A deficiency as a major cause of serious illnesses in developing countries [WHO (2002) The World Health Report, http://www.who.int/whr/2002/en/]. Such illnesses include blindness, and increases in susceptibility to malaria and diarrheal diseases, as well as fetal loss, low birth weight, and infant mortality. Its importance for neurological disorders is less well established at this time. Nevertheless, VAD studies in rodents have pointed to

Vitamin A in the brain: what the future may hold

Many questions remain unanswered regarding RA action in the brain (Box 2) and it is very likely that its influence extends beyond the brain regions detailed in this review. Hints of these roles in the cortex were revealed by studies indicating that RARβ is an intermediary between delta oscillations and the slow-wave sleep electroencephalogram [89], probably in part through modulation of dopamine signaling [90]. As already discussed, vitamin A is necessary for the rhythms of the brain and new

Acknowledgments

We thank Ashley Bird for assistance with Figure 1, Figure 2 and the Biological Sciences Research Council for financial support of part of this work (Grant BB/G014272/1).

References (113)

  • J.N. Griffin

    13-cis-Retinoic acid decreases hypothalamic cell number in vitro

    Neurosci. Res.

    (2010)
  • E.M. Rodriguez

    Hypothalamic tanycytes: a key component of brain–endocrine interaction

    Int. Rev. Cytol.

    (2005)
  • Q.Y. Meng

    Distribution of retinoic acid receptor-alpha immunoreactivity in the human hypothalamus

    Neuroscience

    (2011)
  • X.N. Chen

    The involvement of retinoic acid receptor-alpha in corticotropin-releasing hormone gene expression and affective disorders

    Biol. Psychiatry

    (2009)
  • L. Cai

    Chronic all-trans retinoic acid administration induced hyperactivity of HPA axis and behavioral changes in young rats

    Eur. Neuropsychopharmacol.

    (2010)
  • J.E. Balmer et al.

    Gene expression regulation by retinoic acid

    J. Lipid Res.

    (2002)
  • A. Toulouse

    Molecular cloning and characterization of human RAI1, a gene associated with schizophrenia

    Genomics

    (2003)
  • M.E. Modi et al.

    The oxytocin system in drug discovery for autism: animal models and novel therapeutic strategies

    Horm. Behav.

    (2012)
  • T. Munesue

    Two genetic variants of CD38 in subjects with autism spectrum disorder and controls

    Neurosci. Res.

    (2010)
  • M.A. Lane et al.

    Role of retinoid signalling in the adult brain

    Prog. Neurobiol.

    (2005)
  • S. van Neerven

    Inflammatory cytokine release of astrocytes in vitro is reduced by all-trans retinoic acid

    J. Neuroimmunol.

    (2010)
  • K. Ono

    Vitamin A exhibits potent antiamyloidogenic and fibril-destabilizing effects in vitro

    Exp. Neurol.

    (2004)
  • P. Rinaldi

    Plasma antioxidants are similarly depleted in mild cognitive impairment and in Alzheimer's disease

    Neurobiol. Aging

    (2003)
  • C.P. Maury et al.

    Immunodetection of protein composition in cerebral amyloid extracts in Alzheimer's disease: enrichment of retinol-binding protein

    J. Neurol. Sci.

    (1987)
  • J. Brouillette et al.

    Transthyretin: a key gene involved in the maintenance of memory capacities during aging

    Neurobiol. Aging

    (2008)
  • N. Etchamendy

    Vitamin A deficiency and relational memory deficit in adult mice: relationships with changes in brain retinoid signalling

    Behav. Brain Res.

    (2003)
  • G. Donmez

    SIRT1 suppresses beta-amyloid production by activating the alpha-secretase gene ADAM10

    Cell

    (2010)
  • K. Kitaoka

    Retinoic acid receptor antagonist LE540 attenuates wakefulness via the dopamine D1 receptor in mice

    Brain Res.

    (2011)
  • S. Kumar

    Alcohol and aldehyde dehydrogenases: retinoid metabolic effects in mouse knockout models

    Biochim. Biophys. Acta

    (2012)
  • J.L. Napoli

    Physiological insights into all-trans-retinoic acid biosynthesis

    Biochim. Biophys. Acta

    (2012)
  • D. Hazlerigg et al.

    New insights into ancient seasonal life timers

    Curr. Biol.

    (2008)
  • M. Maden

    Retinoic acid in the development, regeneration and maintenance of the nervous system

    Nat. Rev. Neurosci.

    (2007)
  • P. McCaffery

    Retinoic acid signaling and function in the adult hippocampus

    J. Neurobiol.

    (2006)
  • M. Nomoto

    Dysfunction of the RAR/RXR signaling pathway in the forebrain impairs hippocampal memory and synaptic plasticity

    Mol. Brain

    (2012)
  • H.L. Wang

    Decrease in calcium concentration triggers neuronal retinoic acid synthesis during homeostatic synaptic plasticity

    J. Neurosci.

    (2011)
  • T. Goodman

    Patterning of retinoic acid signaling and cell proliferation in the hippocampus

    Hippocampus

    (2012)
  • K.D. Shearer

    Astrocytes as a regulated source of retinoic acid for the brain

    Glia

    (2012)
  • Y.D. Fragoso

    High expression of retinoic acid receptors and synthetic enzymes in the human hippocampus

    Brain Struct. Funct.

    (2012)
  • N. Chen et al.

    All-trans-retinoic acid stimulates translation and induces spine formation in hippocampal neurons through a membrane-associated RARα

    FASEB J.

    (2008)
  • B. Maghsoodi

    Retinoic acid regulates RARα-mediated control of translation in dendritic RNA granules during homeostatic synaptic plasticity

    Proc. Natl. Acad. Sci. U. S. A.

    (2008)
  • M.E. Soden et al.

    Fragile X protein FMRP is required for homeostatic plasticity and regulation of synaptic strength by retinoic acid

    J. Neurosci.

    (2010)
  • D.L. Misner

    Vitamin A deprivation results in reversible loss of hippocampal long-term synaptic plasticity

    Proc. Natl. Acad. Sci. U. S. A.

    (2001)
  • S. Jacobs

    Retinoic acid is required early during adult neurogenesis in the dentate gyrus

    Proc. Natl. Acad. Sci. U. S. A.

    (2006)
  • E. Bonnet

    Retinoic acid restores adult hippocampal neurogenesis and reverses spatial memory deficit in vitamin A deprived rats

    PLoS ONE

    (2008)
  • W. Jiang

    Vitamin A deficiency impairs postnatal cognitive function via inhibition of neuronal calcium excitability in hippocampus

    J. Neurochem.

    (2012)
  • L.S. Fonzo

    Temporal patterns of lipoperoxidation and antioxidant enzymes are modified in the hippocampus of vitamin A-deficient rats

    Hippocampus

    (2009)
  • N.E. Rawson et al.

    Once and again: retinoic acid signaling in the developing and regenerating olfactory pathway

    J. Neurobiol.

    (2006)
  • C. Chatzi

    Retinoic acid functions as a key GABAergic differentiation signal in the basal ganglia

    PLoS Biol.

    (2011)
  • G.T. Haskell et al.

    Retinoic acid signaling identifies a distinct precursor population in the developing and adult forebrain

    J. Neurosci.

    (2005)
  • M.A. Marzinke

    Calmin expression in embryos and the adult brain, and its regulation by all-trans retinoic acid

    Dev. Dyn.

    (2010)
  • Cited by (0)

    View full text