σ-1 receptor at the mitochondrial-associated endoplasmic reticulum membrane is responsible for mitochondrial metabolic regulation
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The mitochondria-associated endoplasmic reticulum (ER) membrane (MAM) is a small section of the outer mitochondrial membrane tethered to the ER by lipid and protein filaments. One such MAM protein is the σ-1 receptor, which contributes to multiple signaling pathways. We found that short interfering RNA-mediated knockdown of σ-1 reduced pregnenolone synthesis by 95% without affecting expression of the inner mitochondrial membrane resident enzyme, 3-β-hydroxysteroid dehydrogenase 2. To explore the underlying mechanism of this effect, we generated a series of σ-receptor ligands: 5,6-dimethoxy-3-methyl-N-phenyl-N-(3-(piperidin-1-yl)propyl)benzofuran-2-carboxamide (KSCM-1), 3-methyl-N-phenyl-N-(3-(piperidin-1-yl)propyl)benzofuran-2-carboxamide (KSCM-5), and 6-methoxy-3-methyl-N-phenyl-N-(3-(piperidin-1-yl) propyl)benzofuran-2-carboxamide (KSCM-11) specifically bound to σ-1 in the nanomolar range, whereas KSCM-5 and KSCM-11 also bound to σ-2. Treatment of cells with the KSCM ligands led to decreased cell viability, with KSCM-5 having the most potent effect followed by KSCM-11. KSCM-1 increased σ-1 expression by 4-fold and progesterone synthesis, whereas the other compounds decreased progesterone synthesis. These differences probably are caused by ligand molecular structure. For example, KSCM-1 has two methoxy substituents at C-5 and C-6 of the benzofuran ring, whereas KSCM-11 has one at C-6. KSCM ligands or σ-1 knockdown did not alter the expression of ER resident enzymes that synthesize steroids. However, coimmunoprecipitation of the σ-1 receptor pulled down voltage-dependent anion channel 2 (VDAC2), whose expression was enhanced by KSCM-1. VDAC2 plays a key role in cholesterol transport into the mitochondria, suggesting that the σ-1 receptor at the MAM coordinates with steroidogenic acute regulatory protein for cholesterol trafficking into the mitochondria for metabolic regulation.
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SIGMAR1 coimmunoprecipitates with VDAC2 in a steroidogenic cell model and disrupts mitochondrial cholesterol metabolism when its expression is reduced by siRNA.
“The first of these proteins, the sigma-1 receptor (SIGMAR1), was found to coimmunoprecipitate with VDAC2 in a steroidogenic cell model as well as disrupt mitochondrial cholesterol metabolism when its expression was reduced by short interfering RNA (siRNA) (157).”
From Adrenal Mitochondria and Steroidogenesis: From Individual Proteins to Functional Protein Assemblies (2016) · cites this paper as [157]
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- Authors
- Marriott, K.-S. C., Prasad, M., Thapliyal, V., & Bose, H. S.
- Affiliations
- Mercer University (US)
- ORCID
- Bose, Himangshu S.
- Venue
- The Journal of Pharmacology and Experimental Therapeutics
- Publisher
- Elsevier BV
- Published
- 2012-12
- Volume
- 343
- Issue
- 3
- Pages
- 578-586
- ISSN
- 0022-3565 (ISSN-L)
- PMC
- PMC3500540
- OpenAlex
- W2141684558
- Cited by
- 75
- References
- 50
- Citations by year
- 2026: 2 · 2025: 7 · 2024: 1 · 2023: 7 · 2021: 8 · 2020: 4 · 2019: 8 · 2018: 2 · 2017: 11 · 2016: 8 · 2015: 3 · 2014: 7 · 2013: 7
- FWCI
- 2.18
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Pharmacology and Experimental Therapeutics (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health
- National Institute on Drug Abuse (R03DA027086, DA027086)
- National Center on Minority Health and Health Disparities
- National Institute on Minority Health and Health Disparities (P20MD003941)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD057876, R01HD057876)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pharmacological Receptor Mechanisms and Effects
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Endoplasmic Reticulum Stress and Disease
- Keywords
- sigma-1 receptor, mitochondria-associated endoplasmic reticulum membranes, pregnenolone synthesis, progesterone secretion, sigma-1 receptor ligands, VDAC2, steroidogenic acute regulatory protein, sterol metabolism
- MeSH terms
- Sigma-1 Receptor, Animals, Benzofurans, Cell Line, Cholesterol, Dose-Response Relationship, Drug, Endoplasmic Reticulum, Leydig Cells, Ligands, Male, Piperidines, Pregnenolone, Protein Binding, Blotting, Western, Molecular Structure, Receptors, sigma, Mitochondrial Membranes, Mice, Gene Knockdown Techniques
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