Regulation of Neuronal Proliferation and Differentiation by Nitric Oxide

Overview

Journal Mol Neurobiol

Specialties Molecular Biology
Neurology

Date 2003 Jun 5

PMID 12777682

Citations 29

Authors

Sarah M Gibbs

Affiliations

Soon will be listed here.

Abstract

Many studies have revealed the free radical nitric oxide (NO) to be an important modulator of vascular and neuronal physiology. It also plays a developmental role in regulating synapse formation and patterning. Recent studies suggest that NO may also mediate the switch from proliferation to differentiation during neurogenesis. Many mechanisms of this response are conserved between neuronal precursor cells and the cells of the vascular system, where NO can inhibit the proliferative response of endothelial and smooth-muscle cells to injury. In cultured neuroblastoma cells, NO synthase (NOS) expression is increased in the presence of various growth factors and mitogens. Subsequent production of NO leads to cessation of cell division and the acquisition of a differentiated phenotype. The inhibitory action of NO on neuroblast proliferation has also been demonstrated in vivo for vertebrate and invertebrate nervous systems, as well as in the adult brain. Potential downstream effectors of NO include the second messenger cyclic GMP, activation of the tumor-suppressor genes p53 and Rb, and the cyclin-dependent kinase inhibitor p21. These studies highlight a new role for NO in the nervous system, as a coordinator of proliferation and patterning during neural development and adult neurogenesis.

Citing Articles

A specific, non-immune system-related isoform of the human inducible nitric oxide synthase is expressed during differentiation of human stem cells into various cell types.

Gather F, Ihrig-Biedert I, Kohlhas P, Krutenko T, Peitz M, Brustle O Cell Commun Signal. 2022; 20(1):47.

PMID: 35392923 PMC: 8991583. DOI: 10.1186/s12964-022-00855-x.

L-Arginine Exerts Excellent Anti-Stress Effects on Stress-Induced Shortened Lifespan, Cognitive Decline and Depression.

Pervin M, Unno K, Konishi T, Nakamura Y Int J Mol Sci. 2021; 22(2).

PMID: 33419170 PMC: 7825557. DOI: 10.3390/ijms22020508.

Nitric oxide and the brain. Part 1: Mechanisms of regulation, transport and effects on the developing brain.

Angelis D, Savani R, Chalak L Pediatr Res. 2020; 89(4):738-745.

PMID: 32563183 DOI: 10.1038/s41390-020-1017-0.

TRPC5 regulates axonal outgrowth in developing retinal ganglion cells.

Oda M, Yamamoto H, Matsumoto H, Ishizaki Y, Shibasaki K Lab Invest. 2019; 100(2):297-310.

PMID: 31844148 DOI: 10.1038/s41374-019-0347-1.

Human Dermal Fibroblast: A Promising Cellular Model to Study Biological Mechanisms of Major Depression and Antidepressant Drug Response.

Mesdom P, Colle R, Lebigot E, Trabado S, Deflesselle E, Feve B Curr Neuropharmacol. 2019; 18(4):301-318.

PMID: 31631822 PMC: 7327943. DOI: 10.2174/1570159X17666191021141057.

References

Gibbs S, Truman J . Nitric oxide and cyclic GMP regulate retinal patterning in the optic lobe of Drosophila. Neuron. 1998; 20(1):83-93. DOI: 10.1016/s0896-6273(00)80436-5. View

Yang W, Ando J, Korenaga R, Toyo-oka T, Kamiya A . Exogenous nitric oxide inhibits proliferation of cultured vascular endothelial cells. Biochem Biophys Res Commun. 1994; 203(2):1160-7. DOI: 10.1006/bbrc.1994.2304. View

Dyson N . The regulation of E2F by pRB-family proteins. Genes Dev. 1998; 12(15):2245-62. DOI: 10.1101/gad.12.15.2245. View

Morbidelli L, Chang C, Douglas J, Granger H, Ledda F, Ziche M . Nitric oxide mediates mitogenic effect of VEGF on coronary venular endothelium. Am J Physiol. 1996; 270(1 Pt 2):H411-5. DOI: 10.1152/ajpheart.1996.270.1.H411. View

Virgili M, Monti B, Lorusso A, Bentivogli M, Contestabile A . Developmental effects of in vivo and in vitro inhibition of nitric oxide synthase in neurons. Brain Res. 1999; 839(1):164-72. DOI: 10.1016/s0006-8993(99)01750-3. View

Sarkar R, Webb R, Stanley J . Nitric oxide inhibition of endothelial cell mitogenesis and proliferation. Surgery. 1995; 118(2):274-9. DOI: 10.1016/s0039-6060(05)80334-4. View

Weinberger B, Laskin D, Heck D, Laskin J . The toxicology of inhaled nitric oxide. Toxicol Sci. 2001; 59(1):5-16. DOI: 10.1093/toxsci/59.1.5. View

Hope B, Michael G, Knigge K, Vincent S . Neuronal NADPH diaphorase is a nitric oxide synthase. Proc Natl Acad Sci U S A. 1991; 88(7):2811-4. PMC: 51329. DOI: 10.1073/pnas.88.7.2811. View

Nawy S, Jahr C . Suppression by glutamate of cGMP-activated conductance in retinal bipolar cells. Nature. 1990; 346(6281):269-71. DOI: 10.1038/346269a0. View

10.

Assender J, Southgate K, Hallett M, Newby A . Inhibition of proliferation, but not of Ca2+ mobilization, by cyclic AMP and GMP in rabbit aortic smooth-muscle cells. Biochem J. 1992; 288 ( Pt 2):527-32. PMC: 1132042. DOI: 10.1042/bj2880527. View

11.

Hartzell H, Fischmeister R . Opposite effects of cyclic GMP and cyclic AMP on Ca2+ current in single heart cells. Nature. 1986; 323(6085):273-5. DOI: 10.1038/323273a0. View

12.

Bredt D, Hwang P, Glatt C, Lowenstein C, Reed R, Snyder S . Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature. 1991; 351(6329):714-8. DOI: 10.1038/351714a0. View

13.

Yan G, Ziff E . Nerve growth factor induces transcription of the p21 WAF1/CIP1 and cyclin D1 genes in PC12 cells by activating the Sp1 transcription factor. J Neurosci. 1997; 17(16):6122-32. PMC: 6568361. View

14.

Itoi K, Watson S . Regulation of nitric oxide synthase messenger RNA expression in the rat hippocampus by glucocorticoids. Neuroscience. 1998; 87(2):439-46. DOI: 10.1016/s0306-4522(98)00075-x. View

15.

Scholz N, de Vente J, Truman J, Graubard K . Neural network partitioning by NO and cGMP. J Neurosci. 2001; 21(5):1610-8. PMC: 6762929. View

16.

Peunova N, Enikolopov G . Nitric oxide triggers a switch to growth arrest during differentiation of neuronal cells. Nature. 1995; 375(6526):68-73. DOI: 10.1038/375068a0. View

17.

Cox R, Mariano T, Heck D, Laskin J, Stegeman J . Nitric oxide synthase sequences in the marine fish Stenotomus chrysops and the sea urchin Arbacia punctulata, and phylogenetic analysis of nitric oxide synthase calmodulin-binding domains. Comp Biochem Physiol B Biochem Mol Biol. 2001; 130(4):479-91. DOI: 10.1016/s1096-4959(01)00446-8. View

18.

Keilhoff G, Seidel B, Noack H, Tischmeyer W, Stanek D, Wolf G . Patterns of nitric oxide synthase at the messenger RNA and protein levels during early rat brain development. Neuroscience. 1996; 75(4):1193-201. DOI: 10.1016/0306-4522(96)00330-2. View

19.

Meffert M, Calakos N, Scheller R, Schulman H . Nitric oxide modulates synaptic vesicle docking fusion reactions. Neuron. 1996; 16(6):1229-36. DOI: 10.1016/s0896-6273(00)80149-x. View

20.

Hawkins R, Son H, Arancio O . Nitric oxide as a retrograde messenger during long-term potentiation in hippocampus. Prog Brain Res. 1999; 118:155-72. DOI: 10.1016/s0079-6123(08)63206-9. View