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AgRP neurons shape the sperm small RNA payload.

Iasim Tahiri1,2, Sergio R Llana1, Francisco Díaz-Castro1,3

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Paternal obesity alters sperm small noncoding RNAs, particularly transfer RNA-derived small RNAs (tsRNAs), via Agouti-related peptide (AgRP) neurons. This suggests AgRP neurons mediate metabolic epigenetic inheritance from fathers to offspring.

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Area of Science:

  • Epigenetics
  • Reproductive Biology
  • Metabolic Health

Background:

  • Paternal diet and obesity can influence offspring health through epigenetic mechanisms.
  • Sperm RNA, including small noncoding RNAs, is a potential mediator of these effects.
  • The role of specific neuronal pathways in mediating these paternal influences is not fully understood.

Purpose of the Study:

  • To investigate how activating hypothalamic Agouti-related peptide (AgRP) neurons, simulating obesity, affects the small noncoding RNA content of sperm.
  • To determine if these changes in sperm RNA are similar to those induced by dietary factors.
  • To explore the role of AgRP neurons in metabolic epigenetic inheritance.

Main Methods:

  • Utilized a mouse model to activate hypothalamic AgRP neurons, mimicking obesity-associated metabolic changes.
  • Analyzed the small noncoding RNA profile of sperm from treated and control mice.
  • Compared observed RNA alterations with those previously reported following high-fat diet interventions.

Main Results:

  • Activation of AgRP neurons led to significant changes in the sperm's small noncoding RNA payload.
  • Alterations were particularly pronounced in transfer RNA-derived small RNAs (tsRNAs).
  • The observed tsRNA changes mirrored those induced by short-term high-fat diets in previous studies.

Conclusions:

  • Hypothalamic AgRP neurons play a role in modifying sperm RNA content in response to metabolic challenges.
  • AgRP neuron-mediated changes in sperm tsRNAs suggest a common regulatory pathway linking paternal metabolic state to offspring epigenetics.
  • These findings highlight a potential mechanism for metabolic epigenetic inheritance influenced by paternal obesity and diet.