Opiate Analgesics As Negative Modulators of Adult Hippocampal Neurogenesis: Potential Implications in Clinical Practice

Overview

Journal Front Pharmacol

Date 2017 May 25

PMID 28536527

Citations 19

Authors

Valeria Bortolotto

Mariagrazia Grilli

Affiliations

Soon will be listed here.

Abstract

During the past decade, studies of the mechanisms and functional implications of adult hippocampal neurogenesis (ahNG) have significantly progressed. At present, it is proposed that adult born neurons may contribute to a variety of hippocampal-related functions, including specific cognitive aspects and mood regulation. Several groups focussed on the factors that regulate proliferation and fate determination of adult neural stem/progenitor cells (NSC/NPC), including clinically relevant drugs. Opiates were the first drugs shown to negatively impact neurogenesis in the adult mammalian hippocampus. Since that initial report, a vast array of information has been collected on the effect of opiate drugs, by either modulating proliferation of stem/progenitor cells or interfering with differentiation, maturation and survival of adult born neurons. The goal of this review is to critically revise the present state of knowledge on the effect of opiate drugs on the different developmental stages of ahNG, as well as the possible underlying mechanisms. We will also highlight the potential impact of deregulated hippocampal neurogenesis on patients undergoing chronic opiate treatment. Finally, we will discuss the differences in the negative impact on ahNG among clinically relevant opiate drugs, an aspect that may be potentially taken into account to avoid long-term deregulation of neural plasticity and its associated functions in the clinical practice.

Citing Articles

Drug-Induced Cognitive Impairment.

Reimers A, Odin P, Ljung H Drug Saf. 2024; 48(4):339-361.

PMID: 39718691 PMC: 11903592. DOI: 10.1007/s40264-024-01506-5.

Safety and Efficacy of Combined Injection of Pure-μ-Opioid Agonist with Tramadol as an Opioid Induction Agent for Opioid-Naïve Cancer Patients.

Sato T, Ono S, Sato T, Tanaka R, Kamo Y, Suzuki T Palliat Med Rep. 2024; 5(1):340-349.

PMID: 39144134 PMC: 11319850. DOI: 10.1089/pmr.2023.0061.

Potential role of hippocampal neurogenesis in spinal cord injury induced post-trauma depression.

Ma Y, Qiao Y, Gao X Neural Regen Res. 2024; 19(10):2144-2156.

PMID: 38488549 PMC: 11034606. DOI: 10.4103/1673-5374.392855.

Tapentadol: A Review of Experimental Pharmacology Studies, Clinical Trials, and Recent Findings.

Alshehri F Drug Des Devel Ther. 2023; 17:851-861.

PMID: 36974332 PMC: 10039632. DOI: 10.2147/DDDT.S402362.

Evaluation of the Negative Effects of Opium Tincture on Memory and Hippocampal Neurons in the Presence of Chicory Extract.

Bakhshayesh A, Eslami Farsani R, Seyedebrahimi R, Ababzadeh S, Heidari F, Farsani M Adv Biomed Res. 2023; 12:23.

PMID: 36926425 PMC: 10012026. DOI: 10.4103/abr.abr_210_21.

References

Mutso A, Radzicki D, Baliki M, Huang L, Banisadr G, Centeno M . Abnormalities in hippocampal functioning with persistent pain. J Neurosci. 2012; 32(17):5747-56. PMC: 3365570. DOI: 10.1523/JNEUROSCI.0587-12.2012. View

Ge S, Goh E, Sailor K, Kitabatake Y, Ming G, Song H . GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature. 2005; 439(7076):589-93. PMC: 1420640. DOI: 10.1038/nature04404. View

Canales J . Adult neurogenesis and the memories of drug addiction. Eur Arch Psychiatry Clin Neurosci. 2007; 257(5):261-70. DOI: 10.1007/s00406-007-0730-6. View

Bortolotto V, Cuccurazzu B, Canonico P, Grilli M . NF-κB mediated regulation of adult hippocampal neurogenesis: relevance to mood disorders and antidepressant activity. Biomed Res Int. 2014; 2014:612798. PMC: 3942292. DOI: 10.1155/2014/612798. View

van Praag H, Shubert T, Zhao C, Gage F . Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci. 2005; 25(38):8680-5. PMC: 1360197. DOI: 10.1523/JNEUROSCI.1731-05.2005. View

Gorman A, Elliott K, Inturrisi C . The d- and l-isomers of methadone bind to the non-competitive site on the N-methyl-D-aspartate (NMDA) receptor in rat forebrain and spinal cord. Neurosci Lett. 1997; 223(1):5-8. DOI: 10.1016/s0304-3940(97)13391-2. View

Sasikumar T, Qiang L, Burnett D, Greenlee W, Li C, Grilli M . A-ring modifications on the triazafluorenone core structure and their mGluR1 antagonist properties. Bioorg Med Chem Lett. 2010; 20(8):2474-7. DOI: 10.1016/j.bmcl.2010.03.004. View

Famitafreshi H, Karimian M, Fatima S . Synergistic Effects of Social Isolation and Morphine Addiction on Reduced Neurogenesis and BDNF Levels and the Resultant Deficits in Cognition and Emotional State in Male Rats. Curr Mol Pharmacol. 2016; 9(4):337-347. DOI: 10.2174/1874467209666160822102153. View

Dayer A, Ford A, Cleaver K, Yassaee M, Cameron H . Short-term and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol. 2003; 460(4):563-72. DOI: 10.1002/cne.10675. View

10.

Mandyam C, Norris R, Eisch A . Chronic morphine induces premature mitosis of proliferating cells in the adult mouse subgranular zone. J Neurosci Res. 2004; 76(6):783-94. DOI: 10.1002/jnr.20090. View

11.

Zhao C, Deng W, Gage F . Mechanisms and functional implications of adult neurogenesis. Cell. 2008; 132(4):645-60. DOI: 10.1016/j.cell.2008.01.033. View

12.

Smith K, Mattick R, Bruno R, Nielsen S, Cohen M, Campbell G . Factors associated with the development of depression in chronic non-cancer pain patients following the onset of opioid treatment for pain. J Affect Disord. 2015; 184:72-80. DOI: 10.1016/j.jad.2015.05.049. View

13.

Seri B, Garcia-Verdugo J, Collado-Morente L, McEwen B, Alvarez-Buylla A . Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol. 2004; 478(4):359-78. DOI: 10.1002/cne.20288. View

14.

Persson A, Thorlin T, Bull C, Zarnegar P, Ekman R, Terenius L . Mu- and delta-opioid receptor antagonists decrease proliferation and increase neurogenesis in cultures of rat adult hippocampal progenitors. Eur J Neurosci. 2003; 17(6):1159-72. DOI: 10.1046/j.1460-9568.2003.02538.x. View

15.

Kempermann G, Jessberger S, Steiner B, Kronenberg G . Milestones of neuronal development in the adult hippocampus. Trends Neurosci. 2004; 27(8):447-52. DOI: 10.1016/j.tins.2004.05.013. View

16.

Nugent F, Penick E, Kauer J . Opioids block long-term potentiation of inhibitory synapses. Nature. 2007; 446(7139):1086-90. DOI: 10.1038/nature05726. View

17.

Couillard-Despres S, Iglseder B, Aigner L . Neurogenesis, cellular plasticity and cognition: the impact of stem cells in the adult and aging brain--a mini-review. Gerontology. 2011; 57(6):559-64. DOI: 10.1159/000323481. View

18.

Maekawa M, Namba T, Suzuki E, Yuasa S, Kohsaka S, Uchino S . NMDA receptor antagonist memantine promotes cell proliferation and production of mature granule neurons in the adult hippocampus. Neurosci Res. 2009; 63(4):259-66. DOI: 10.1016/j.neures.2008.12.006. View

19.

Neumaier J, Mailheau S, Chavkin C . Opioid receptor-mediated responses in the dentate gyrus and CA1 region of the rat hippocampus. J Pharmacol Exp Ther. 1988; 244(2):564-70. View

20.

Dranovsky A, Hen R . Hippocampal neurogenesis: regulation by stress and antidepressants. Biol Psychiatry. 2006; 59(12):1136-43. PMC: 7537828. DOI: 10.1016/j.biopsych.2006.03.082. View