Oleic acid is an endogenous ligand of TLX/NR2E1 that triggers hippocampal neurogenesis


Por: Kandel, P, Semerci, F, Mishra, R, Choi, W, Bajic, A, Baluya, D, Ma, LH, Chen, K, Cao, AC, Phongmekhin, T, Matinyan, N, Jimenez-Panizo, A, Chamakuri, S, Raji, IO, Chang, L, Fuentes-Prior, P, MacKenzie, KR, Benn, CL, Estebanez-Perpina, E, Venken, K, Moore, DD, Young, DW, Maletic-Savatic, M

Publicada: 29 mar 2022
Resumen:
Neural stem cells, the source of newborn neurons in the adult hippocampus, are intimately involved in learning and memory, mood, and stress response. Despite considerable progress in understanding the biology of neural stem cells and neurogenesis, regulating the neural stem cell population precisely has remained elusive because we have lacked the specific targets to stimulate their proliferation and neurogenesis. The orphan nuclear receptor TLX/NR2E1 governs neural stem and progenitor cell self-renewal and proliferation, but the precise mechanism by which it accomplishes this is not well understood because its endogenous ligand is not known. Here, we identify oleic acid (18:1 omega 9 monounsaturated fatty acid) as such a ligand. We first show that oleic acid is critical for neural stem cell survival. Next, we demonstrate that it binds to TLX to convert it from a transcriptional repressor to a transcriptional activator of cell-cycle and neurogenesis genes, which in turn increases neural stem cell mitotic activity and drives hippocampal neurogenesis in mice. Interestingly, oleic acid-activated TLX strongly up-regulates cell cycle genes while only modestly up-regulating neurogenic genes. We propose a model in which sufficient quantities of this endogenous ligand must bind to TLX to trigger the switch to proliferation and drive the progeny toward neuronal lineage. Oleic acid thus serves as a metabolic regulator of TLX activity that can be used to selectively target neural stem cells, paving the way for future therapeutic manipulations to counteract pathogenic impairments of neurogenesis.

Filiaciones:
Kandel, P:
 Baylor Coll Med, Integrat Mol & Biomed Sci Grad Program, Houston, TX 77030 USA

 Baylor Coll Med, Dept Pharmacol & Chem Biol, Houston, TX 77030 USA

Semerci, F:
 Baylor Coll Med, Dept Pediat Neurol, Houston, TX 77030 USA

 Texas Childrens Hosp, Jan & Duncan Neurol Res Inst, Houston, TX 77030 USA

Mishra, R:
 Baylor Coll Med, Dept Pediat Neurol, Houston, TX 77030 USA

 Texas Childrens Hosp, Jan & Duncan Neurol Res Inst, Houston, TX 77030 USA

Choi, W:
 Texas Childrens Hosp, Jan & Duncan Neurol Res Inst, Houston, TX 77030 USA

 Baylor Coll Med, Med Scientist Training Program, Houston, TX 77030 USA

 Tulane Univ, Dept Obstet & Gynecol, New Orleans, LA 70112 USA

Bajic, A:
 Texas Childrens Hosp, Jan & Duncan Neurol Res Inst, Houston, TX 77030 USA

 Baylor Coll Med, Dept Mol & Human Genet, Houston, TX 77030 USA

Baluya, D:
 Univ Texas MD Anderson Canc Ctr, Dept Intervent Radiol, Houston, TX 77030 USA

 Washington State Univ, Tissue Imaging Metabol & Prote Lab, Pullman, WA 99163 USA

Ma, LH:
 Baylor Coll Med, NMR & Drug Metab Adv Technol Cores, Houston, TX 77030 USA

Chen, K:
 Rice Univ, Dept Biosci, Houston, TX 77005 USA

 Univ Chicago, Pritzker Sch Med, Chicago, IL 60637 USA

Cao, AC:
 Rice Univ, Dept Chem, Houston, TX 77005 USA

 Univ Penn, Perelman Sch Med, Philadelphia, PA 19104 USA

Phongmekhin, T:
 Rice Univ, Dept Biosci, Houston, TX 77005 USA

Matinyan, N:
 Baylor Coll Med, Integrat Mol & Biomed Sci Grad Program, Houston, TX 77030 USA

 Baylor Coll Med, Verna & Marrs McLean Dept Biochem & Mol Biol, Houston, TX 77030 USA

Jimenez-Panizo, A:
 Univ Barcelona, Inst Biomed, Dept Biochem & Mol Biomed, Barcelona 08028, Spain

Chamakuri, S:
 Baylor Coll Med, Dept Pharmacol & Chem Biol, Houston, TX 77030 USA

 Baylor Coll Med, Dept Pathol & Immunol, Houston, TX 77030 USA

Raji, IO:
 Baylor Coll Med, Dept Pharmacol & Chem Biol, Houston, TX 77030 USA

 MIT, Koch Inst, Cambridge, MA 02142 USA

Chang, L:
 Baylor Coll Med, Dept Pharmacol & Chem Biol, Houston, TX 77030 USA

Fuentes-Prior, P:
 Biomed Res Inst St Pau, Mol Basis Dis, Barcelona 08025, Spain

MacKenzie, KR:
 Baylor Coll Med, Dept Pharmacol & Chem Biol, Houston, TX 77030 USA

 Baylor Coll Med, NMR & Drug Metab Adv Technol Cores, Houston, TX 77030 USA

 Baylor Coll Med, Dept Pathol & Immunol, Houston, TX 77030 USA

Benn, CL:
 Pfizer Regenerat Med, Cambridge CB21 6GP, England

 CSO LoQus23 Therapeut, Cambridge CB22 3AT, England

Estebanez-Perpina, E:
 Univ Barcelona, Inst Biomed, Dept Biochem & Mol Biomed, Barcelona 08028, Spain

Venken, K:
 Baylor Coll Med, Integrat Mol & Biomed Sci Grad Program, Houston, TX 77030 USA

 Baylor Coll Med, Verna & Marrs McLean Dept Biochem & Mol Biol, Houston, TX 77030 USA

Moore, DD:
 Baylor Coll Med, Integrat Mol & Biomed Sci Grad Program, Houston, TX 77030 USA

 Baylor Coll Med, Dept Mol & Cellular Biol, Houston, TX 77030 USA

Young, DW:
 Baylor Coll Med, Integrat Mol & Biomed Sci Grad Program, Houston, TX 77030 USA

 Baylor Coll Med, Dept Pharmacol & Chem Biol, Houston, TX 77030 USA

 Texas Childrens Hosp, Jan & Duncan Neurol Res Inst, Houston, TX 77030 USA

 Rice Univ, Dept Chem, Houston, TX 77005 USA

 Baylor Coll Med, Dept Pathol & Immunol, Houston, TX 77030 USA

 Biomed Res Inst St Pau, Mol Basis Dis, Barcelona 08025, Spain

 Baylor Coll Med, Ctr Drug Discovery, Houston, TX 77030 USA

Maletic-Savatic, M:
 Baylor Coll Med, Dept Pediat Neurol, Houston, TX 77030 USA

 Texas Childrens Hosp, Jan & Duncan Neurol Res Inst, Houston, TX 77030 USA

 Baylor Coll Med, Ctr Drug Discovery, Houston, TX 77030 USA

 Baylor Coll Med, Dept Neurosci, Houston, TX 77030 USA
ISSN: 00278424
Editorial
NATL ACAD SCIENCES, 2101 CONSTITUTION AVE NW, WASHINGTON, DC 20418 USA, Estados Unidos America
Tipo de documento: Article
Volumen: 119 Número: 13
Páginas:
WOS Id: 000780677900002
ID de PubMed: 35333654
imagen Green Published, Green

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