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A specific folate activates serotonergic neurons to control C. elegans behavior

Author

Listed:
  • Ria S. Peesapati

    (The University of Georgia)

  • Brianna L. Austin-Byler

    (The University of Georgia)

  • Fathima Zahra Nawaz

    (The University of Georgia)

  • Jonathan B. Stevenson

    (The University of Georgia)

  • Stanelle A. Mais

    (The University of Georgia)

  • Rabia N. Kaya

    (The University of Georgia)

  • Michael G. Hassan

    (The University of Georgia)

  • Nabraj Khanal

    (The University of Georgia)

  • Alexandra C. Wells

    (The University of Georgia)

  • Deena Ghiai

    (The University of Georgia)

  • Anish K. Garikapati

    (The University of Georgia)

  • Jacob Selhub

    (Tufts University)

  • Edward T. Kipreos

    (The University of Georgia)

Abstract

Folates are B-group vitamins that function in one-carbon metabolism. Here we show that a specific folate can activate serotonergic neurons in C. elegans to modulate behavior through a pathway that requires the folate receptor FOLR-1 and the GON-2 calcium channel. FOLR-1 and GON-2 physically interact in a heterologous system, and both are expressed in the HSN and NSM serotonergic neurons. Both the folate 10-formyl-THF and a non-metabolic pteroate induce increases in the number of Ca2+ transients in the HSN neurons and egg laying in an FOLR-1- and GON-2-dependent manner. FOLR-1 and GON-2 are required for the activation of the NSM neurons in response to 10-formyl-THF, and for full NSM-mediated stoppage of movement when starved animals encounter bacteria. Our results demonstrate that FOLR-1 acts independently of one-carbon metabolism and suggest that 10-formyl-THF acts as a dietary signal that activates serotonergic neurons to impact behavior through a pathway that involves calcium entry.

Suggested Citation

  • Ria S. Peesapati & Brianna L. Austin-Byler & Fathima Zahra Nawaz & Jonathan B. Stevenson & Stanelle A. Mais & Rabia N. Kaya & Michael G. Hassan & Nabraj Khanal & Alexandra C. Wells & Deena Ghiai & Ani, 2024. "A specific folate activates serotonergic neurons to control C. elegans behavior," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-52738-z
    DOI: 10.1038/s41467-024-52738-z
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    References listed on IDEAS

    as
    1. Marcel Grapp & Arne Wrede & Michaela Schweizer & Sabine Hüwel & Hans-Joachim Galla & Nicolas Snaidero & Mikael Simons & Johanna Bückers & Philip S. Low & Henning Urlaub & Jutta Gärtner & Robert Steinf, 2013. "Choroid plexus transcytosis and exosome shuttling deliver folate into brain parenchyma," Nature Communications, Nature, vol. 4(1), pages 1-13, October.
    2. Ji Ying Sze & Martin Victor & Curtis Loer & Yang Shi & Gary Ruvkun, 2000. "Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant," Nature, Nature, vol. 403(6769), pages 560-564, February.
    3. Olga A. Balashova & Alexios A. Panoutsopoulos & Olesya Visina & Jacob Selhub & Paul S. Knoepfler & Laura N. Borodinsky, 2024. "Noncanonical function of folate through folate receptor 1 during neural tube formation," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
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