Putative role of N-Arachidonoyl glycine (NAGly) Acute hyperphagia in BALB/c mice

  • Ramírez-Orozco Ricardo Ernesto Universidad Autónoma de Aguascalientes. Departamento de Nutrición; Aguascalientes, Ags., México.
  • Pedroza-García Karina Alejandra Universidad Autónoma de Aguascalientes. Departamento de Nutrición; Aguascalientes, Ags., México.
  • Masuoka David Universidad Autónoma de Aguascalientes. Departamento de Estomatología; Aguascalientes, Ags., México.
  • Camacho-Morales Alberto Universidad Autónoma de Nuevo León. Departamento de Bioquímica, Facultad de Medicina; Monterrey, N.L., México.
  • Álvarez-Miramontes Silvia Anahí Universidad Autónoma de Aguascalientes. Departamento de Nutrición; Aguascalientes, Ags., México.
  • Martínez-Miranda Christian Alejandro Universidad Autónoma de Aguascalientes. Departamento de Nutrición; Aguascalientes, Ags., México.

Abstract

Introduction: Obesity is a pandemic problem associated to development of chronic degenerative diseases. N-arachidonylglycine (NAGly) is speculated to participate in pain regulation, immunity and insulin secretion; some N-acyl amino acids induce hyperphagia; in light of this, NAGly metabolic functions related to energy homeostasis has not been clarified yet. We aim to elucidate the effect of NAGly administration on weight gain, food intake, diet preferences and inflammatory profile changes in a murine model. Methods: 8-week-old BALB/c mice (n=78) were allocated into 4 groups for either sex: control, vector, NAGly-LD (1nM) and NAGly-HD (10nM). NAGly was subcutaneous administered 5 consecutive days for 3 weeks. Mice were exposed to standard diet (SD), high-fat diet (HFD) and high-sugar diet (HSD) simultaneously; weight gain, food intake and diet preferences were evaluated for 21-days. Finally, cytokines were analyzed by enzyme-linked immunosorbent assay (ELISA). Results: final weight gain was found higher in those following NAGly [LD: 21.6±1.1 g and HD: 21.4±2.1 g, (p=0.001)]. NAGly groups consumed more food in the first days; NAGly groups consumed more HFD [5.06±1.60; (p=0.001)] and HSD [1.10±0.69; (p=0.001)]. Conclusion: Our data propose that subcutaneous NAGly promotes acute hyperphagia events. We propose that NAGly might play a role related to the hunger-satiety circuit.

References

Akiba, Y., Kato, S., Katsube, K. I., Nakamura, M., Takeuchi, K., Ishii, H., & Hibi, T. (2004). Transient receptor potential vanilloid subfamily 1 expressed in pancreatic islet β cells modulates insulin secretion in rats. Biochemical and Biophysical Research Communications, 321(1), 219–225. https://doi.org/10.1016/j.bbrc.2004.06.149
Artmann, A., Petersen, G., Hellgren, L. I., Boberg, J., Skonberg, C., Nellemann, C., Hansen, S. H., & Hansen, H. S. (2008). Influence of dietary fatty acids on endocannabinoid and N-acylethanolamine levels in rat brain, liver and small intestine. Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids, 1781(4), 200–212. https://doi.org/10.1016/j.bbalip.2008.01.006
Balvers, M. G. J., Verhoeckx, K. C. M., Plastina, P., Wortelboer, H. M., Meijerink, J., & Witkamp, R. F. (2010). Docosahexaenoic acid and eicosapentaenoic acid are converted by 3T3-L1 adipocytes to N-acyl ethanolamines with anti-inflammatory properties. Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids, 1801(10), 1107–1114. https://doi.org/10.1016/j.bbalip.2010.06.006
Becker, A. M., Callahan, D. J., Richner, J. M., Choi, J., DiPersio, J. F., Diamond, M. S., & Bhattacharya, D. (2015). GPR18 controls reconstitution of mouse small intestine intraepithelial lymphocytes following bone marrow transplantation. PLoS ONE, 10(7). https://doi.org/10.1371/journal.pone.0133854
Berge, K., Piscitelli, F., Hoem, N., Silvestri, C., Meyer, I., Banni, S., & Di Marzo, V. (2013). Chronic treatment with krill powder reduces plasma triglyceride and anandamide levels in mildly obese men. Lipids in Health and Disease, 12(1). https://doi.org/10.1186/1476-511X-12-78
Bradshaw, H. B., Rimmerman, N., Hu, S. S. J., Burstein, S., & Walker, J. M. (2009). Chapter 8 Novel Endogenous N-Acyl Glycines. Identification and Characterization. In Vitamins and Hormones (Vol. 81, Issue C, pp. 191–205). Vitam Horm. https://doi.org/10.1016/S0083-6729(09)81008-X
Brown, I., Wahle, K. W. J., Cascio, M. G., Smoum-Jaouni, R., Mechoulam, R., Pertwee, R. G., & Heys, S. D. (2011). Omega-3 N-acylethanolamines are endogenously synthesised from omega-3 fatty acids in different human prostate and breast cancer cell lines. Prostaglandins Leukotrienes and Essential Fatty Acids, 85(6), 305–310. https://doi.org/10.1016/j.plefa.2011.09.007
Burstein, S. H. (2014). The cannabinoid acids, analogs and endogenous counterparts. In Bioorganic and Medicinal Chemistry (Vol. 22, Issue 10, pp. 2830–2843). Elsevier Ltd. https://doi.org/10.1016/j.bmc.2014.03.038
Burstein, S. H., Huang, S. M., Petros, T. J., Rossetti, R. G., Walker, J. M., & Zurier, R. B. (2002). Regulation of anandamide tissue levels by N-arachidonylglycine. Biochemical Pharmacology, 64(7), 1147–1150. https://doi.org/10.1016/S0006-2952(02)01301-1
Console-Bram, L., Ciuciu, S. M., Zhao, P., Zipkin, R. E., Brailoiu, E., & Abood, M. E. (2017). N-arachidonoyl glycine, another endogenous agonist of GPR55. Biochemical and Biophysical Research Communications, 490(4), 1389–1393. https://doi.org/10.1016/j.bbrc.2017.07.038
De Vries, T. J., Shaham, Y., Homberg, J. R., Crombag, H., Schuurman, K., Dieben, J., Vanderschuren, L. J. M. J., & Schoffelmeer, A. N. M. (2001). A cannabinoid mechanism in relapse to cocaine seeking. Nature Medicine, 7(10), 1151–1154. https://doi.org/10.1038/nm1001-1151
Di Marzo, V., Bisogno, T., & De Petrocellis, L. (2007). Endocannabinoids and Related Compounds: Walking Back and Forth between Plant Natural Products and Animal Physiology. In Chemistry and Biology (Vol. 14, Issue 7, pp. 741–756). Chem Biol. https://doi.org/10.1016/j.chembiol.2007.05.014
Fattore, L., Martellotta, M. C., Cossu, G., Mascia, M. S., & Fratta, W. (1999). CB1 cannabinoid receptor agonist WIN 55, 212-2 decreases intravenous cocaine self-administration in rats. Behavioural Brain Research, 104(1–2), 141–146. https://doi.org/10.1016/S0166-4328(99)00059-5
Fernández-Ruiz, J., Lastres-Becker, I., Cabranes, A., González, S., & Ramos, J. A. (2002). Endocannabinoids and basal ganglia functionality. Prostaglandins Leukotrienes and Essential Fatty Acids, 66(2–3), 257–267. https://doi.org/10.1054/plef.2001.0350
Goldbach-Mansky, R. (2012). Immunology in clinic review series; focus on autoinflammatory diseases: Update on monogenic autoinflammatory diseases: The role of interleukin (IL)-1 and an emerging role for cytokines beyond IL-1. In Clinical and Experimental Immunology (Vol. 167, Issue 3, pp. 391–404). Clin Exp Immunol. https://doi.org/10.1111/j.1365-2249.2011.04533.x
Guindon, J., & Beaulieu, P. (2010). The Role of the Endogenous Cannabinoid System in Peripheral Analgesia. Current Molecular Pharmacology, 2(1), 134–139. https://doi.org/10.2174/1874467210902010134
Hansen, H. S., Rosenkilde, M. M., Holst, J. J., & Schwartz, T. W. (2012). GPR119 as a fat sensor. In Trends in Pharmacological Sciences (Vol. 33, Issue 7, pp. 374–381). Trends Pharmacol Sci. https://doi.org/10.1016/j.tips.2012.03.014
Hillard, C. J. (2000). Endocannabinoids and vascular function. Journal of Pharmacology and Experimental Therapeutics, 294(1), 27–32.
Huang, S. M., Bisogno, T., Petros, T. J., Chang, S. Y., Zavitsanos, P. A., Zipkin, R. E., Sivakumar, R., Coop, A., Maeda, D. Y., De Petrocellis, L., Burstein, S., Di Marzo, V., & Walker, J. M. (2001). Identification of a New Class of Molecules, the Arachidonyl Amino Acids, and Characterization of One Member That Inhibits Pain. Journal of Biological Chemistry, 276(46), 42639–42644. https://doi.org/10.1074/jbc.M107351200
Ikeda, Y., Iguchi, H., Nakata, M., Ioka, R. X., Tanaka, T., Iwasaki, S., Magoori, K., Takayasu, S., Yamamoto, T. T., Kodama, T., Yada, T., Sakurai, T., Yanagisawa, M., & Sakai, J. (2005). Identification of N-arachidonylglycine, U18666A, and 4-androstene-3,17- dione as novel insulin Secretagogues. Biochemical and Biophysical Research Communications, 333(3), 778–786. https://doi.org/10.1016/j.bbrc.2005.06.005
Inam, Q.-A., Ikram, H., Shireen, E., & Haleem, D. J. (2016). Effects of sugar rich diet on brain serotonin, hyperphagia and anxiety in animal model of both genders. Pakistan Journal of Pharmaceutical Sciences, 29(3), 757–763.
Jeong, H. J., Vandenberg, R. J., & Vaughan, C. W. (2010). N-arachidonyl-glycine modulates synaptic transmission in superficial dorsal horn. British Journal of Pharmacology, 161(4), 925–935. https://doi.org/10.1111/j.1476-5381.2010.00935.x
Kleiner, G., Marcuzzi, A., Zanin, V., Monasta, L., & Zauli, G. (2013). Cytokine levels in the serum of healthy subjects. Mediators of Inflammation, 2013. https://doi.org/10.1155/2013/434010
Lu, V. B., Puhl, H. L., & Ikeda, S. R. (2013). N-arachidonyl glycine does not activate G protein-coupled receptor 18 signaling via canonical pathways. Molecular Pharmacology, 83(1), 267–282. https://doi.org/10.1124/mol.112.081182
McHugh, D., Hu, S. S. J., Rimmerman, N., Juknat, A., Vogel, Z., Walker, J. M., & Bradshaw, H. B. (2010). N-arachidonoyl glycine, an abundant endogenous lipid, potently drives directed cellular migration through GPR18, the putative abnormal cannabidiol receptor. BMC Neuroscience, 11. https://doi.org/10.1186/1471-2202-11-44
McHugh, D., Page, J., Dunn, E., & Bradshaw, H. B. (2012). Δ 9-tetrahydrocannabinol and N-arachidonyl glycine are full agonists at GPR18 receptors and induce migration in human endometrial HEC-1B cells. British Journal of Pharmacology, 165(8), 2414–2424. https://doi.org/10.1111/j.1476-5381.2011.01497.x
McHugh, D., Roskowski, D., Xie, S., & Bradshaw, H. B. (2014). Δ9-THC and N-arachidonoyl glycine regulate BV-2 microglial morphology and cytokine release plasticity: Implications for signaling at GPR18. Frontiers in Pharmacology, 4 JAN. https://doi.org/10.3389/fphar.2013.00162
McHugh, M. P., & Cosgrave, C. H. (2010). To stretch or not to stretch: the role of stretching in injury prevention and performance. Scand J Med Sci Sports, 20(2), 169–181. https://doi.org/10.1111/j.1600-0838.2009.01058.x
Meijerink, J., Balvers, M., Plastina, P., & Witkamp, R. (2015). Omega-3 Polyunsaturated N-Acylethanolamines: A Link Between Diet and Cellular Biology. In The Endocannabinoidome: The World of Endocannabinoids and Related Mediators (pp. 15–32). Elsevier Inc. https://doi.org/10.1016/B978-0-12-420126-2.00002-X
Miller, S., Leishman, E., Oehler, O., Daily, L., Murataeva, N., Wager-Miller, J., Bradshaw, H., & Straiker, A. (2016). Evidence for a GPR18 role in diurnal regulation of intraocular pressure. Investigative Ophthalmology and Visual Science, 57(14), 6419–6426. https://doi.org/10.1167/iovs.16-19437
Morselli, E., Fuente-Martin, E., Finan, B., Kim, M., Frank, A., Garcia-Caceres, C., Navas, C. R., Gordillo, R., Neinast, M., Kalainayakan, S. P., Li, D. L., Gao, Y., Yi, C. X., Hahner, L., Palmer, B. F., Tschöp, M. H., & Clegg, D. J. (2014). Hypothalamic PGC-1α protects against high-fat diet exposure by regulating ERα. Cell Reports, 9(2), 633–645. https://doi.org/10.1016/j.celrep.2014.09.025
Palmer, B. F., & Clegg, D. J. (2015). The sexual dimorphism of obesity. In Molecular and Cellular Endocrinology (Vol. 402, pp. 113–119). Elsevier Ireland Ltd. https://doi.org/10.1016/j.mce.2014.11.029
Parolaro, D. (1999). Presence and functional regulation of cannabinoid receptors in immune cells. Life Sciences, 65(6–7), 637–644. https://doi.org/10.1016/S0024-3205(99)00286-6
Ramírez-Orozco, R. E., García-Ruiz, R., Morales, P., Villalón, C. M., Villafán-Bernal, J. R., & Marichal-Cancino, B. A. (2019). Potential metabolic and behavioural roles of the putative endocannabinoid receptors GPR18, GPR55 and GPR119 in feeding. Current Neuropharmacology, 17(10), 947–960. https://doi.org/10.2174/1570159x17666190118143014
Sheskin, T., Hanuš, L., Slager, J., Vogel, Z., & Mechoulam, R. (1997). Structural requirements for binding of anandamide-type compounds to the brain cannabinoid receptor. Journal of Medicinal Chemistry, 40(5), 659–667. https://doi.org/10.1021/jm960752x
Shi, H., Seeley, R. J., & Clegg, D. J. (2009). Sexual differences in the control of energy homeostasis. In Frontiers in Neuroendocrinology (Vol. 30, Issue 3, pp. 396–404). Front Neuroendocrinol. https://doi.org/10.1016/j.yfrne.2009.03.004
Takenouchi, R., Inoue, K., Kambe, Y., & Miyata, A. (2012). N-arachidonoyl glycine induces macrophage apoptosis via GPR18. Biochemical and Biophysical Research Communications, 418(2), 366–371. https://doi.org/10.1016/j.bbrc.2012.01.027
Voigt, R. G., Mellon, M. W., Katusic, S. K., Weaver, A. L., Matern, D., Mellon, B., Jensen, C. L., & Barbaresi, W. J. (2014). Dietary Docosahexaenoic Acid Supplementation in Children With Autism. Journal of Pediatric Gastroenterology and Nutrition, 58(6), 715–722. https://doi.org/10.1097/mpg.0000000000000260
WHO. (2020, April 1). Obesidad y sobrepeso. https://www.who.int/es/news-room/fact-sheets/detail/obesity-and-overweight
Wu, J., Zhu, C., Yang, L., Wang, Z., Wang, L., Wang, S., Gao, P., Zhang, Y., Jiang, Q., Zhu, X., & Shu, G. (2017). N-Oleoylglycine-Induced Hyperphagia Is Associated with the Activation of Agouti-Related Protein (AgRP) Neuron by Cannabinoid Receptor Type 1 (CB1R). Journal of Agricultural and Food Chemistry, 65(5), 1051–1057. https://doi.org/10.1021/acs.jafc.6b05281
Zhang, L., Han, W., Lin, C., Li, F., & de Araujo, I. E. (2018). Sugar metabolism regulates flavor preferences and portal glucose sensing. Frontiers in Integrative Neuroscience, 12. https://doi.org/10.3389/fnint.2018.00057
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Ernesto, R.-O. R., P.-G. K. Alejandra, M. David, C.-M. Alberto, Álvarez-M. S. Anahí, and M.-M. C. Alejandro. “Putative Role of N-Arachidonoyl Glycine (NAGly) Acute Hyperphagia in BALB/C Mice”. Emirates Journal of Food and Agriculture, Vol. 33, no. 3, Apr. 2021, pp. 245-52, doi:https://doi.org/10.9755/ejfa.2021.v33.i3.2657. Accessed 24 June 2021.
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Research Article