دورية أكاديمية
Oxygen consumption rate of flatworms under the influence of wake- and sleep-promoting neurotransmitters.
| العنوان: | Oxygen consumption rate of flatworms under the influence of wake- and sleep-promoting neurotransmitters. |
|---|---|
| المؤلفون: | Omond SET; School of Agriculture, Biomedicine and Environment, La Trobe University, Melbourne, Australia., Barker RG; School of Agriculture, Biomedicine and Environment, La Trobe University, Melbourne, Australia., Sanislav O; School of Agriculture, Biomedicine and Environment, La Trobe University, Melbourne, Australia., Fisher PR; School of Agriculture, Biomedicine and Environment, La Trobe University, Melbourne, Australia., Annesley SJ; School of Agriculture, Biomedicine and Environment, La Trobe University, Melbourne, Australia., Lesku JA; School of Agriculture, Biomedicine and Environment, La Trobe University, Melbourne, Australia. |
| المصدر: | Journal of experimental zoology. Part A, Ecological and integrative physiology [J Exp Zool A Ecol Integr Physiol] 2024 May 27. Date of Electronic Publication: 2024 May 27. |
| Publication Model: | Ahead of Print |
| نوع المنشور: | Journal Article |
| اللغة: | English |
| بيانات الدورية: | Publisher: Wiley Periodicals, Inc Country of Publication: United States NLM ID: 101710204 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 2471-5646 (Electronic) Linking ISSN: 24715638 NLM ISO Abbreviation: J Exp Zool A Ecol Integr Physiol Subsets: MEDLINE |
| أسماء مطبوعة: | Original Publication: Hoboken, NJ : Wiley Periodicals, Inc., [2017] |
| مستخلص: | Flatworms are among the best studied animal models for regeneration; however, they also represent an emerging opportunity to investigate other biological processes as well. For instance, flatworms are nocturnal and sleep during the day, a state that is regulated by sleep/wake history and the action of the sleep-promoting neurotransmitter gamma-aminobutyric acid (or GABA). Sleep is widespread across the animal kingdom, where it serves many nonexclusive functions. Notably, sleep saves energy by reducing metabolic rate and by not doing something more energetically taxing. Whether the conservation of energy is apparent in sleeping flatworms is unclear. We measured the oxygen consumption rate (OCR) of flatworms dosed with either (1) GABA (n = 29) which makes flatworms inactive or (2) dopamine (n = 20) which stimulates flatworms to move, or (3) day and night neurotransmitter-free controls (n = 28 and 27, respectively). While OCR did not differ between the day and night, flatworms treated with GABA used less oxygen than those treated with dopamine, and less than the day-time control. Thus, GABA affected flatworm physiology, ostensibly by enforcing energy-conserving sleep. Evidence that dopamine increased metabolism was less strong. This work broadens our understanding of flatworm physiology and expands the phylogenetic applicability of energy conservation as a function of sleep. (© 2024 The Author(s). Journal of Experimental Zoology Part A: Ecological and Integrative Physiology published by Wiley Periodicals LLC.) |
| References: | Agilent. (2018). Seahorse XFe Analyzer: Operating Manual. Agilent Technologies. Aljbour, S. M., Zimmer, M., & Kunzmann, A. (2017). Cellular respiration, oxygen consumption, and trade‐offs of the jellyfish Cassiopea sp. in response to temperature change. Journal of Sea Research, 128, 92–97. Berger, R. J., & Phillips, N. H. (1995). Energy conservation and sleep. Behavioural Brain Research, 69, 65–73. Bounas, A., Komini, C., Toli, E. A., Talioura, A., Sotiropoulos, K., & Barboutis, C. (2024). Expression patterns of heat‐shock genes during stopover and the trade‐off between refueling and stress response in a passerine migrant. Journal of Comparative Physiology B, 194, 1–6. Brown, E. B., Klok, J., & Keene, A. C. (2022). Measuring metabolic rate in single flies during sleep and waking states via indirect calorimetry. Journal of Neuroscience Methods, 376, 109606. Bushey, D., Tononi, G., & Cirelli, C. (2015). Sleep‐ and wake‐dependent changes in neuronal activity and reactivity demonstrated in fly neurons using in vivo calcium imaging. Proceedings of the National Academy of Sciences, 112, 4785–4790. Calabrese, E. J., & Baldwin, L. A. (2003). Hormesis: The dose‐response revolution. Annual Review of Pharmacology and Toxicology, 43, 175–197. Davimes, J. G., Alagaili, A. N., Bhagwandin, A., Bertelsen, M. F., Mohammed, O. B., Bennett, N. C., Manger, P. R., & Gravett, N. (2018). Seasonal variations in sleep of free‐ranging Arabian oryx (Oryx leucoryx) under natural hyperarid conditions. Sleep, 41, zsy038. Ferretti, A., Rattenborg, N. C., Ruf, T., McWilliams, S. R., Cardinale, M., & Fusani, L. (2019). Sleeping unsafely tucked in to conserve energy in a nocturnal migratory songbird. Current Biology, 29, 2766–2772.e4. Freiberg, J., Lang, L., Kaernbach, C., & Keil, J. (2023). Characterization of the planarian surface electroencephalogram. BMC Neuroscience, 24, 29. Hadas, E., Ilan, M., & Shpigel, M. (2008). Oxygen consumption by a coral reef sponge. Journal of Experimental Biology, 211, 2185–2190. Hoffmann, F., Røy, H., Bayer, K., Hentschel, U., Pfannkuchen, M., Brümmer, F., & de Beer, D. (2008). Oxygen dynamics and transport in the Mediterranean sponge Aplysina aerophoba. Marine Biology, 153, 1257–1264. Hyman, L. H. (1925). Respiratory differences along the axis of the sponge Grantia. The Biological Bulletin, 48, 379–389. Joiner, W. J. (2016). Unraveling the evolutionary determinants of sleep. Current Biology, 26, R1073–R1087. Kaiser, W., & Steiner‐Kaiser, J. (1983). Neuronal correlates of sleep, wakefulness and arousal in a diurnal insect. Nature, 301, 707–709. Kanaya, H. J., Park, S., Kim, J., Kusumi, J., Krenenou, S., Sawatari, E., Sato, A., Lee, J., Bang, H., Kobayakawa, Y., Lim, C., & Itoh, T. Q. (2020). A sleep‐like state in Hydra unravels conserved sleep mechanisms during the evolutionary development of the central nervous system. Science Advances, 6, eabb9415. Keenan, L., Koopowitz, H., & Bernardo, K. (1979). Primitive nervous systems: action of aminergic drugs and blocking agents on activity in the ventral nerve cord of the flatworm Notoplana acticola. Journal of Neurobiology, 10, 397–407. Kelly, M. L., Collins, S. P., Lesku, J. A., Hemmi, J. M., Collin, S. P., & Radford, C. A. (2022). Energy conservation characterizes sleep in sharks. Biology Letters, 18, 20210259. Lesku, J. A., Roth II, T. C., Rattenborg, N. C., Amlaner, C. J., & Lima, S. L. (2009). History and future of comparative analyses in sleep research. Neuroscience & Biobehavioral Reviews, 33, 1024–1036. Lesku, J. A., & Schmidt, M. H. (2022). Energetic costs and benefits of sleep. Current Biology, 32, R656–R661. Lima, S. L., Rattenborg, N. C., Lesku, J. A., & Amlaner, C. J. (2005). Sleeping under the risk of predation. Animal Behaviour, 70, 723–736. Nitz, D. A., van Swinderen, B., Tononi, G., & Greenspan, R. J. (2002). Electrophysiological correlates of rest and activity in Drosophila melanogaster. Current Biology, 12, 1934–1940. Omond, S., Ly, L. M. T., Beaton, R., Storm, J. J., Hale, M. W., & Lesku, J. A. (2017). Inactivity is nycthemeral, endogenously generated, homeostatically regulated, and melatonin modulated in a free‐living platyhelminth flatworm. Sleep, 40, zsx124. Omond, S. E. T., Hale, M. W., & Lesku, J. A. (2022). Neurotransmitters of sleep and wakefulness in flatworms. Sleep, 45, zsac053. Osuma, E. A., Riggs, D. W., Gibb, A. A., & Hill, B. G. (2018). High throughput measurement of metabolism in planarians reveals activation of glycolysis during regeneration. Regeneration, 5, 78–86. Paskin, T. R., Jellies, J., Bacher, J., & Beane, W. S. (2014). Planarian phototactic assay reveals differential behavioral responses based on wavelength. PLoS One, 9, e114708. Preston, B. T., Capellini, I., McNamara, P., Barton, R. A., & Nunn, C. L. (2009). Parasite resistance and the adaptive significance of sleep. BMC Evolutionary Biology, 9, 7. Rattenborg, N. C., & Ungurean, G. (2023). The evolution and diversification of sleep. Trends in Ecology & Evolution, 38, 156–170. Ruppert, E. E., Fox, R. S., & Barnes, R. D. (2004). Invertebrate Zoology: A Functional Evolutionary Approach (7th ed.). Thomson, Brooks/Cole. Schmidt, M. H. (2014). The energy allocation function of sleep: A unifying theory of sleep, torpor, and continuous wakefulness. Neuroscience & Biobehavioral Reviews, 47, 122–153. Sharma, S., & Kavuru, M. (2010). Sleep and metabolism: An overview. International Journal of Endocrinology, 2010, 1–12. Siegel, J. M. (2005). Clues to the functions of mammalian sleep. Nature, 437, 1264–1271. Siegel, J. M. (2009). Sleep viewed as a state of adaptive inactivity. Nature Reviews Neuroscience, 10, 747–753. Stahl, B. A., Slocumb, M. E., Chaitin, H., DiAngelo, J. R., & Keene, A. C. (2017). Sleep‐dependent modulation of metabolic rate in Drosophila. Sleep, 40, zsx084. Stenberg, D. (2007). Neuroanatomy and neurochemistry of sleep. Cellular and Molecular Life Sciences, 64, 1187–1204. Strand, R., Whalan, S., Webster, N. S., Kutti, T., Fang, J. K. H., Luter, H. M., & Bannister, R. J. (2017). The response of a boreal deep‐sea sponge holobiont to acute thermal stress. Scientific Reports, 7, 1660. Ueno, T., Tomita, J., Kume, S., & Kume, K. (2012). Dopamine modulates metabolic rate and temperature sensitivity in Drosophila melanogaster. PLoS One, 7, e31513. Welsh, D. T., Dunn, R. J. K., & Meziane, T. (2009). Oxygen and nutrient dynamics of the upside down jellyfish (Cassiopea sp.) and its influence on benthic nutrient exchanges and primary production. Hydrobiologia, 635, 351–362. Winsky‐Sommerer, R. (2009). Role of GABAA receptors in the physiology and pharmacology of sleep. European Journal of Neuroscience, 29, 1779–1794. Zaid, E., Rainsford, F. W., Johnsson, R. D., Valcu, M., Vyssotski, A. L., Meerlo, P., & Lesku, J. A. (2024). Semelparous marsupials reduce sleep for sex. Current Biology, 34, 606–614.e3. Zepelin, H., & Rechtschaffen, A. (1974). Mammalian sleep, longevity, and energy metabolism. Brain, Behavior and Evolution, 10, 425–446. |
| معلومات مُعتمدة: | Australian Research Council |
| فهرسة مساهمة: | Keywords: Dugesia; GABA; Girardia; circadian; dopamine; planarian; platyhelminthes |
| تواريخ الأحداث: | Date Created: 20240527 Latest Revision: 20240527 |
| رمز التحديث: | 20240527 |
| DOI: | 10.1002/jez.2828 |
| PMID: | 38801005 |
| قاعدة البيانات: | MEDLINE |
| تدمد: | 2471-5646 |
|---|---|
| DOI: | 10.1002/jez.2828 |