The evolutionary conserved miR-137/325 tandem mediates obesity-induced hypogonadism and metabolic comorbidities by repressing hypothalamic kisspeptin
Obesity-induced hypogonadism (OIH) is a prevalent, but often neglected condition in men, which aggravates the metabolic complications of overweight. While hypothalamic suppression of Kiss1-encoded kisspeptin has been suggested to contribute to OIH, the molecular mechanisms for such repression in obe...
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| Published in | Metabolism, clinical and experimental Vol. 157; p. 155932 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , |
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| Abstract | Obesity-induced hypogonadism (OIH) is a prevalent, but often neglected condition in men, which aggravates the metabolic complications of overweight. While hypothalamic suppression of Kiss1-encoded kisspeptin has been suggested to contribute to OIH, the molecular mechanisms for such repression in obesity, and the therapeutic implications thereof, remain unknown.
A combination of bioinformatic, expression and functional analyses was implemented, assessing the role of the evolutionary-conserved miRNAs, miR-137 and miR-325, in mediating obesity-induced suppression of hypothalamic kisspeptin, as putative mechanism of central hypogonadism and metabolic comorbidities. The implications of such miR-137/325-kisspeptin interplay for therapeutic intervention in obesity were also explored using preclinical OIH models.
MiR-137/325 repressed human KISS1 3’-UTR in-vitro and inhibited hypothalamic kisspeptin content in male rats, while miR-137/325 expression was up-regulated, and Kiss1/kisspeptin decreased, in the medio-basal hypothalamus of obese rats. Selective over-expression of miR-137 in Kiss1 neurons reduced Kiss1/ kisspeptin and partially replicated reproductive and metabolic alterations of OIH in lean mice. Conversely, interference of the repressive actions of miR-137/325 selectively on Kiss1 3’-UTR in vivo, using target-site blockers (TSB), enhanced kisspeptin content and reversed central hypogonadism in obese rats, together with improvement of glucose intolerance, insulin resistance and cardiovascular and inflammatory markers, despite persistent exposure to obesogenic diet. Reversal of OIH by TSB miR-137/325 was more effective than chronic kisspeptin or testosterone treatments in obese rats.
Our data disclose that the miR-137/325-Kisspeptin repressive interaction is a major player in the pathogenesis of obesity-induced hypogonadism and a putative druggable target for improved management of this condition and its metabolic comorbidities in men suffering obesity.
Up to half of the men suffering obesity display also central hypogonadism, an often neglected complication of overweight that can aggravate the clinical course of obesity and its complications. The mechanisms for such obesity-induced hypogonadism remain poorly defined. We show here that the evolutionary conserved miR137/miR325 tandem centrally mediates obesity-induced hypogonadism via repression of the reproductive-stimulatory signal, kisspeptin; this may represent an amenable druggable target for improved management of hypogonadism and other metabolic complications of obesity.
•Central hypogonadism is a prevalent condition in men with obesity, of as yet unknown mechanisms•Long-term obesity has been suggested to suppress Kiss1 neurons in the ARC of male rodents, via ill-defined molecular mechanisms•Hypothalamic miR-137/miR-325 are upregulated in obese male rats and repress Kiss1/kisspeptin•Blockade of this repressive interaction reverses central hypogonadism and metabolic comorbidities•This reversal is more effective than those induced by treatments with testosterone or kisspeptin |
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| AbstractList | Obesity-induced hypogonadism (OIH) is a prevalent, but often neglected condition in men, which aggravates the metabolic complications of overweight. While hypothalamic suppression of Kiss1-encoded kisspeptin has been suggested to contribute to OIH, the molecular mechanisms for such repression in obesity, and the therapeutic implications thereof, remain unknown.
A combination of bioinformatic, expression and functional analyses was implemented, assessing the role of the evolutionary-conserved miRNAs, miR-137 and miR-325, in mediating obesity-induced suppression of hypothalamic kisspeptin, as putative mechanism of central hypogonadism and metabolic comorbidities. The implications of such miR-137/325-kisspeptin interplay for therapeutic intervention in obesity were also explored using preclinical OIH models.
MiR-137/325 repressed human KISS1 3'-UTR in-vitro and inhibited hypothalamic kisspeptin content in male rats, while miR-137/325 expression was up-regulated, and Kiss1/kisspeptin decreased, in the medio-basal hypothalamus of obese rats. Selective over-expression of miR-137 in Kiss1 neurons reduced Kiss1/ kisspeptin and partially replicated reproductive and metabolic alterations of OIH in lean mice. Conversely, interference of the repressive actions of miR-137/325 selectively on Kiss1 3'-UTR in vivo, using target-site blockers (TSB), enhanced kisspeptin content and reversed central hypogonadism in obese rats, together with improvement of glucose intolerance, insulin resistance and cardiovascular and inflammatory markers, despite persistent exposure to obesogenic diet. Reversal of OIH by TSB miR-137/325 was more effective than chronic kisspeptin or testosterone treatments in obese rats.
Our data disclose that the miR-137/325-Kisspeptin repressive interaction is a major player in the pathogenesis of obesity-induced hypogonadism and a putative druggable target for improved management of this condition and its metabolic comorbidities in men suffering obesity.
Up to half of the men suffering obesity display also central hypogonadism, an often neglected complication of overweight that can aggravate the clinical course of obesity and its complications. The mechanisms for such obesity-induced hypogonadism remain poorly defined. We show here that the evolutionary conserved miR137/miR325 tandem centrally mediates obesity-induced hypogonadism via repression of the reproductive-stimulatory signal, kisspeptin; this may represent an amenable druggable target for improved management of hypogonadism and other metabolic complications of obesity. Obesity-induced hypogonadism (OIH) is a prevalent, but often neglected condition in men, which aggravates the metabolic complications of overweight. While hypothalamic suppression of Kiss1-encoded kisspeptin has been suggested to contribute to OIH, the molecular mechanisms for such repression in obesity, and the therapeutic implications thereof, remain unknown.BACKGROUNDObesity-induced hypogonadism (OIH) is a prevalent, but often neglected condition in men, which aggravates the metabolic complications of overweight. While hypothalamic suppression of Kiss1-encoded kisspeptin has been suggested to contribute to OIH, the molecular mechanisms for such repression in obesity, and the therapeutic implications thereof, remain unknown.A combination of bioinformatic, expression and functional analyses was implemented, assessing the role of the evolutionary-conserved miRNAs, miR-137 and miR-325, in mediating obesity-induced suppression of hypothalamic kisspeptin, as putative mechanism of central hypogonadism and metabolic comorbidities. The implications of such miR-137/325-kisspeptin interplay for therapeutic intervention in obesity were also explored using preclinical OIH models.METHODSA combination of bioinformatic, expression and functional analyses was implemented, assessing the role of the evolutionary-conserved miRNAs, miR-137 and miR-325, in mediating obesity-induced suppression of hypothalamic kisspeptin, as putative mechanism of central hypogonadism and metabolic comorbidities. The implications of such miR-137/325-kisspeptin interplay for therapeutic intervention in obesity were also explored using preclinical OIH models.MiR-137/325 repressed human KISS1 3'-UTR in-vitro and inhibited hypothalamic kisspeptin content in male rats, while miR-137/325 expression was up-regulated, and Kiss1/kisspeptin decreased, in the medio-basal hypothalamus of obese rats. Selective over-expression of miR-137 in Kiss1 neurons reduced Kiss1/ kisspeptin and partially replicated reproductive and metabolic alterations of OIH in lean mice. Conversely, interference of the repressive actions of miR-137/325 selectively on Kiss1 3'-UTR in vivo, using target-site blockers (TSB), enhanced kisspeptin content and reversed central hypogonadism in obese rats, together with improvement of glucose intolerance, insulin resistance and cardiovascular and inflammatory markers, despite persistent exposure to obesogenic diet. Reversal of OIH by TSB miR-137/325 was more effective than chronic kisspeptin or testosterone treatments in obese rats.RESULTSMiR-137/325 repressed human KISS1 3'-UTR in-vitro and inhibited hypothalamic kisspeptin content in male rats, while miR-137/325 expression was up-regulated, and Kiss1/kisspeptin decreased, in the medio-basal hypothalamus of obese rats. Selective over-expression of miR-137 in Kiss1 neurons reduced Kiss1/ kisspeptin and partially replicated reproductive and metabolic alterations of OIH in lean mice. Conversely, interference of the repressive actions of miR-137/325 selectively on Kiss1 3'-UTR in vivo, using target-site blockers (TSB), enhanced kisspeptin content and reversed central hypogonadism in obese rats, together with improvement of glucose intolerance, insulin resistance and cardiovascular and inflammatory markers, despite persistent exposure to obesogenic diet. Reversal of OIH by TSB miR-137/325 was more effective than chronic kisspeptin or testosterone treatments in obese rats.Our data disclose that the miR-137/325-Kisspeptin repressive interaction is a major player in the pathogenesis of obesity-induced hypogonadism and a putative druggable target for improved management of this condition and its metabolic comorbidities in men suffering obesity.CONCLUSIONSOur data disclose that the miR-137/325-Kisspeptin repressive interaction is a major player in the pathogenesis of obesity-induced hypogonadism and a putative druggable target for improved management of this condition and its metabolic comorbidities in men suffering obesity.Up to half of the men suffering obesity display also central hypogonadism, an often neglected complication of overweight that can aggravate the clinical course of obesity and its complications. The mechanisms for such obesity-induced hypogonadism remain poorly defined. We show here that the evolutionary conserved miR137/miR325 tandem centrally mediates obesity-induced hypogonadism via repression of the reproductive-stimulatory signal, kisspeptin; this may represent an amenable druggable target for improved management of hypogonadism and other metabolic complications of obesity.SIGNIFICANCE STATEMENTUp to half of the men suffering obesity display also central hypogonadism, an often neglected complication of overweight that can aggravate the clinical course of obesity and its complications. The mechanisms for such obesity-induced hypogonadism remain poorly defined. We show here that the evolutionary conserved miR137/miR325 tandem centrally mediates obesity-induced hypogonadism via repression of the reproductive-stimulatory signal, kisspeptin; this may represent an amenable druggable target for improved management of hypogonadism and other metabolic complications of obesity. Obesity-induced hypogonadism (OIH) is a prevalent, but often neglected condition in men, which aggravates the metabolic complications of overweight. While hypothalamic suppression of Kiss1-encoded kisspeptin has been suggested to contribute to OIH, the molecular mechanisms for such repression in obesity, and the therapeutic implications thereof, remain unknown. A combination of bioinformatic, expression and functional analyses was implemented, assessing the role of the evolutionary-conserved miRNAs, miR-137 and miR-325, in mediating obesity-induced suppression of hypothalamic kisspeptin, as putative mechanism of central hypogonadism and metabolic comorbidities. The implications of such miR-137/325-kisspeptin interplay for therapeutic intervention in obesity were also explored using preclinical OIH models. MiR-137/325 repressed human KISS1 3’-UTR in-vitro and inhibited hypothalamic kisspeptin content in male rats, while miR-137/325 expression was up-regulated, and Kiss1/kisspeptin decreased, in the medio-basal hypothalamus of obese rats. Selective over-expression of miR-137 in Kiss1 neurons reduced Kiss1/ kisspeptin and partially replicated reproductive and metabolic alterations of OIH in lean mice. Conversely, interference of the repressive actions of miR-137/325 selectively on Kiss1 3’-UTR in vivo, using target-site blockers (TSB), enhanced kisspeptin content and reversed central hypogonadism in obese rats, together with improvement of glucose intolerance, insulin resistance and cardiovascular and inflammatory markers, despite persistent exposure to obesogenic diet. Reversal of OIH by TSB miR-137/325 was more effective than chronic kisspeptin or testosterone treatments in obese rats. Our data disclose that the miR-137/325-Kisspeptin repressive interaction is a major player in the pathogenesis of obesity-induced hypogonadism and a putative druggable target for improved management of this condition and its metabolic comorbidities in men suffering obesity. Up to half of the men suffering obesity display also central hypogonadism, an often neglected complication of overweight that can aggravate the clinical course of obesity and its complications. The mechanisms for such obesity-induced hypogonadism remain poorly defined. We show here that the evolutionary conserved miR137/miR325 tandem centrally mediates obesity-induced hypogonadism via repression of the reproductive-stimulatory signal, kisspeptin; this may represent an amenable druggable target for improved management of hypogonadism and other metabolic complications of obesity. •Central hypogonadism is a prevalent condition in men with obesity, of as yet unknown mechanisms•Long-term obesity has been suggested to suppress Kiss1 neurons in the ARC of male rodents, via ill-defined molecular mechanisms•Hypothalamic miR-137/miR-325 are upregulated in obese male rats and repress Kiss1/kisspeptin•Blockade of this repressive interaction reverses central hypogonadism and metabolic comorbidities•This reversal is more effective than those induced by treatments with testosterone or kisspeptin |
| ArticleNumber | 155932 |
| Author | Perdices-Lopez, Cecilia Rodriguez-Sanchez, Ana B. Avendaño, María S. García-Redondo, Ana B. Guerrero-Ruiz, Yolanda Sobrino, Verónica Hernanz, Raquel Pitteloud, Nelly Briones, Ana M. Tena-Sempere, Manuel Correa-Sáez, Alejandro Lara-Chica, Maribel Calzado, Marco A. Garcia-Galiano, David Ruiz-Pino, Francisco Ruiz-Cruz, Miguel Pineda, Rafael Vázquez, María J. Sanchez-Tapia, María J. Barroso, Alexia Fernandez-Garcia, José C. |
| Author_xml | – sequence: 1 givenname: María S. surname: Avendaño fullname: Avendaño, María S. email: b22avhem@uco.es organization: Instituto Maimónides de Investigación Biomédica de Córdoba (IMIBIC), Córdoba, Spain – sequence: 2 givenname: Cecilia surname: Perdices-Lopez fullname: Perdices-Lopez, Cecilia organization: Instituto Maimónides de Investigación Biomédica de Córdoba (IMIBIC), Córdoba, Spain – sequence: 3 givenname: Yolanda surname: Guerrero-Ruiz fullname: Guerrero-Ruiz, Yolanda organization: Instituto Maimónides de Investigación Biomédica de Córdoba (IMIBIC), Córdoba, Spain – sequence: 4 givenname: Francisco surname: Ruiz-Pino fullname: Ruiz-Pino, Francisco organization: Instituto Maimónides de Investigación Biomédica de Córdoba (IMIBIC), Córdoba, Spain – sequence: 5 givenname: Ana B. surname: Rodriguez-Sanchez fullname: Rodriguez-Sanchez, Ana B. organization: Instituto Maimónides de Investigación Biomédica de Córdoba (IMIBIC), Córdoba, Spain – sequence: 6 givenname: María J. surname: Sanchez-Tapia fullname: Sanchez-Tapia, María J. organization: Instituto Maimónides de Investigación Biomédica de Córdoba (IMIBIC), Córdoba, Spain – sequence: 7 givenname: Verónica surname: Sobrino fullname: Sobrino, Verónica organization: Instituto Maimónides de Investigación Biomédica de Córdoba (IMIBIC), Córdoba, Spain – sequence: 8 givenname: Rafael surname: Pineda fullname: Pineda, Rafael organization: Instituto Maimónides de Investigación Biomédica de Córdoba (IMIBIC), Córdoba, Spain – sequence: 9 givenname: Alexia surname: Barroso fullname: Barroso, Alexia organization: Instituto Maimónides de Investigación Biomédica de Córdoba (IMIBIC), Córdoba, Spain – sequence: 10 givenname: Alejandro surname: Correa-Sáez fullname: Correa-Sáez, Alejandro organization: Instituto Maimónides de Investigación Biomédica de Córdoba (IMIBIC), Córdoba, Spain – sequence: 11 givenname: Maribel surname: Lara-Chica fullname: Lara-Chica, Maribel organization: Instituto Maimónides de Investigación Biomédica de Córdoba (IMIBIC), Córdoba, Spain – sequence: 12 givenname: José C. surname: Fernandez-Garcia fullname: Fernandez-Garcia, José C. organization: CIBER Fisiopatología de la Obesidad y Nutrición (CIBEROBN), Instituto de Salud Carlos III, Córdoba, Spain – sequence: 13 givenname: Ana B. surname: García-Redondo fullname: García-Redondo, Ana B. organization: Department of Pharmacology, Universidad Autónoma de Madrid, Madrid, Spain – sequence: 14 givenname: Raquel surname: Hernanz fullname: Hernanz, Raquel organization: Instituto Investigación Hospital Universitario La Paz (IdiPaz), Madrid, Spain – sequence: 15 givenname: Miguel surname: Ruiz-Cruz fullname: Ruiz-Cruz, Miguel organization: Instituto Maimónides de Investigación Biomédica de Córdoba (IMIBIC), Córdoba, Spain – sequence: 16 givenname: David surname: Garcia-Galiano fullname: Garcia-Galiano, David organization: Instituto Maimónides de Investigación Biomédica de Córdoba (IMIBIC), Córdoba, Spain – sequence: 17 givenname: Nelly surname: Pitteloud fullname: Pitteloud, Nelly organization: Department of Service of Endocrinology, Diabetes, and Metabolism, Faculty of Biology and Medicine, University of Lausanne, Lausanne University Hospital, Lausanne, Switzerland – sequence: 18 givenname: Marco A. surname: Calzado fullname: Calzado, Marco A. organization: Instituto Maimónides de Investigación Biomédica de Córdoba (IMIBIC), Córdoba, Spain – sequence: 19 givenname: Ana M. surname: Briones fullname: Briones, Ana M. organization: Department of Pharmacology, Universidad Autónoma de Madrid, Madrid, Spain – sequence: 20 givenname: María J. surname: Vázquez fullname: Vázquez, María J. organization: Instituto Maimónides de Investigación Biomédica de Córdoba (IMIBIC), Córdoba, Spain – sequence: 21 givenname: Manuel surname: Tena-Sempere fullname: Tena-Sempere, Manuel email: fi1tesem@uco.es organization: Instituto Maimónides de Investigación Biomédica de Córdoba (IMIBIC), Córdoba, Spain |
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| Keywords | Obesity Kiss1 miR-137 miR-325 Comorbidities Male hypogonadism Obesity-induced hypogonadism MicroRNAs Kisspeptins |
| Language | English |
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| SubjectTerms | Comorbidities Kiss1 Kisspeptins Male hypogonadism MicroRNAs miR-137 miR-325 Obesity Obesity-induced hypogonadism |
| Title | The evolutionary conserved miR-137/325 tandem mediates obesity-induced hypogonadism and metabolic comorbidities by repressing hypothalamic kisspeptin |
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