Elsevier

Brain Research

Volume 190, Issue 1, 19 May 1980, Pages 195-214
Brain Research

Neurons switch from non-neuronal enolase to neuron-specific enolase during differentiation

https://doi.org/10.1016/0006-8993(80)91169-5Get rights and content

Abstract

The enolase (EC 4.2.1.11) isoenzymes, neuron-specific enolase (NSE,γγ) and non-neuronal enolase (NNE, αα), are markers for neurons and glia, respectively, in adult mammalian brain. In developing fetal and early postnatal brain, levels of non-neuronal enolase (NNE) are high. Neuron-specific enolase (NSE) appears only after neurogenesis begins in a given region and only slowly attains adult levels. Immunocytochemistry in developing rat and rhesus monkey brain reveals that proliferative zones that give rise to neurons are NNE(+). Thus, nerve cells must undergo a switch from NNE to NSE. In addition, study of neurons in cerebellum and neocortex reveals that they are NNE(+) during migration and only become NSE(+) in their final location, presumably after making full synaptic connections. Such migrating cells may contain hybrid enolase (άγ) and some (e.g. cerebellar stellate/basket cells) may not completely switch over to NSE even in the adult. Neuron-specific enolase is not only a specific molecular marker for mature nerve cells, but is closely correlated to the differentiated state.

Reference (44)

  • BockE.

    Nervous system specific proteins

    J. Neurochem.

    (1978)
  • BockE. et al.

    Demonstration of enolase activity connected to the brain specific protein 14-3-2

    Scand. J. Immunol.

    (1975)
  • BockE. et al.

    The nature of the two proteins of brain specific antigen 14-3-2

    J. Neurochem.

    (1978)
  • ChenShi-Han et al.

    Enolase: human tissue distribution and evidence for three different loci

    Ann. hum. Genet.

    (1976)
  • CiceroT.J. et al.

    Regional changes in CNS levels of the S-100 and 14-3-2 proteins during development and aging of the mouse

    J. Neurochem.

    (1972)
  • Dubois-DalcqM. et al.

    Protein-A peroxidase: a valuable tool for the localization of antigens

    J. Histochem. Cytochem.

    (1977)
  • FletcherL. et al.

    Enolase isoenzymes as markers of differentiation in teratocarcinoma cells and normal tissues of mouse

    Develop. Biol.

    (1978)
  • HeinsenH.

    Quantitative anatomical studies on the postnatal development of the cerebellum of the albino rat

    Anat. Embryol.

    (1977)
  • JacobsenM.

    Histogenesis and morphogenesis of the central nervous system

  • LebherzG. et al.

    Distribution of fructose diphosphate aldolase variants in biological systems

    Biochemistry

    (1969)
  • MarangosP.J. et al.

    Functional properties of neuronal and glial isoenzymes of brain enolase

    J. Neurochem.

    (1978)
  • MarangosP.J. et al.

    The developmental profile of neuronal and glial enolase in rat brain

    Neurosci. Abstr.

    (1978)
  • Cited by (302)

    • Designing anti-Zika virus peptides derived from predicted human-Zika virus protein-protein interactions

      2017, Computational Biology and Chemistry
      Citation Excerpt :

      A member of the enolase family, ENO2 promotes cell maturation in the central nervous system (Konstantinou et al., 2008). During early development, neuronal cells switch from ENO1 (non-neuronal enolase) to ENO2 in order to promote brain development (Schmechel et al., 1980) (Fig. 2). Interestingly, a similar interaction was reported by Munoz et al. where they describe an interaction between the Aedes aegypti enolase and Dengue virus NS5 protein (Muñoz et al., 2013).

    • Lactoferrin induced neuronal differentiation: A boon for brain tumours

      2015, International Journal of Developmental Neuroscience
      Citation Excerpt :

      However, the same was not true when checked for NF 200 at protein level (Fig. 3B). The other neuronal marker studied was the expression of neuron specific enolase (NSE) and was found to elevate with both the protein treatments confirming the neuronal differentiation (Schmechel et al., 1980). Our results showed that the differentiation induced by bLf was evident with the upregulation of neurofilaments and β-tubulin III along with the PI3K signalling at both the gene and protein level.

    • Delineating the regulation of energy homeostasis using hypothalamic cell models

      2015, Frontiers in Neuroendocrinology
      Citation Excerpt :

      Transformed hypothalamic neurons generally maintain their genetic diversity and distinct neuronal phenotypes despite the potential impact of SV40 T-Ag on gene expression, indicating that immortalization is insufficient to fully overwrite previous genetic programming. Also, hypothalamic models derived from adult mice (mHypoA-xx cell lines) still maintain the expression of fully differentiated and mature neuronal markers, notably NSE and NF, without detectable levels of the immature marker, doublecortin (DCX), suggesting the T-Ag is unable to promote dedifferentiation (Belsham et al., 2009; Hoffman and Lasek, 1975; Schmechel et al., 1980; Brown et al., 2003; Couillard-Despres et al., 2005). Most importantly, these hypothalamic models maintain regulated expression and secretion of a plethora of neuropeptides, including NPY, AgRP, and POMC.

    • Distribution of TMEM100 in the mouse and human gastrointestinal tract - A novel marker of enteric nerves

      2013, Neuroscience
      Citation Excerpt :

      For the most part these limitations are surmountable and in some tissues absence of expression or ectopic expression can provide important information. For example, studies of NSE expression have revealed important information about the processes of neuronal maturation, because a switch in expression from non-neuronal enolase (αα isoenzyme) to the neuron-specific isoenzyme (γγ, NSE) correlates with differentiation of precursor cells into mature neurons (Schmechel et al., 1980). The finding that HuC/D expression is high in small cell carcinomas and is immunogenic has led to the recognition of paraneoplastic enteropathies in which the enteric nervous system (ENS) is damaged by the anti-Hu or ANNA-1 antibodies (King et al., 1999).

    View all citing articles on Scopus
    View full text