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Brain acid sphingomyelinase controls addiction-related behaviours in a sex-specific way.

Liubov S Kalinichenko, Iulia Zoicas, Anne-Marie Bienia, Clara Bühner, Julia Robinson, Joshua Kütemeyer, Annika Labonte, Thadshajiny Raveendran, Lena Warth, Irena Smaga, Malgorzata Filip, Volker Eulenburg, Cosima Rhein, Anna Fejtova, Erich Gulbins, Johannes Kornhuber, Christian P Müller

Neurobiology of disease March 1, 2025 DOI: 10.1016/j.nbd.2025.106800 via PubMed

Summary

Overexpression of acid sphingomyelinase (ASM) in the forebrain affects addiction-related behaviors differently in male and female mice. In males, forebrain ASM overexpression increased alcohol consumption in a free-choice paradigm and reduced conditioned place preference (CPP) for alcohol and cocaine, but not for amphetamine, ketamine, or high-fat/carbohydrate food. In females, it increased binge-like alcohol drinking while moderate consumption remained unchanged, and enhanced CPP for amphetamine but not other substances. These findings suggest ASM plays a sex-specific role in the reinforcing effects of certain addictive substances, offering potential molecular targets for drug- and sex-specific therapies.

Study at a glance

Characteristics Experimental study Peer reviewed
Population Male and female mice with forebrain ASM overexpression
Intervention forebrain ASM overexpression
Topics Addiction Ketamine Serotonin
Keywords Acid sphingomyelinase Alcohol Amphetamine Cocaine Conditioned place preference
Citations 4
Key finding Forebrain ASM overexpression alters alcohol consumption and conditioned place preference for alcohol, cocaine, and amphetamine in a sex-specific manner in mice.

Abstract

Addiction is a chronic and severe mental disorder with high gender- and sex-specificity. However, the pathogenesis of this disorder is not fully elucidated, and no targeted pharmacotherapy is available. A growing body of evidence points out the potential involvement of the ceramide system in the pathophysiology of addiction. A pathogenic pathway for several mental disorders based on the overexpression of an enzyme involved in ceramide formation, acid sphingomyelinase (ASM), was recently proposed. Here we show a crucial role of ASM specifically overexpressing in the forebrain for various types of addiction-related behaviours in a drug- and sex-specific way. In male mice, a forebrain ASM overexpression led to enhanced alcohol consumption in a free-choice paradigm. It also diminished the reinforcing properties of alcohol and cocaine, but not that of amphetamine, ketamine, or a natural reinforcer fat/carbohydrate-rich food in the conditioned place preference (CPP) test in males. In female mice, a forebrain ASM overexpression enhanced alcohol binge-like drinking, while moderate alcohol consumption was preserved. ASM overexpression in females contributed to CPP establishment for amphetamine, but not for other psychoactive substances. Altogether, this study shows a specific involvement of forebrain ASM in the development of conditioned reinforcing effects of different types of substances with addictive properties in a sex-specific way. Our data enlarge the current knowledge on the specific molecular mechanisms of dependence from various drugs of abuse and might serve as a basis for the development of drug- and sex-specific targeted therapy.

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