Serotonin-induced brain glycogenolysis in rainbow trout (Oncorhynchus mykiss)

Journal of Experimental Biology

Volumn 215, Issue 17, 2012, Pages 2969-2979

  Pérez Maceira, Jorge J ^a   Mancebo, María J ^a   Aldegunde, Manuel ^a  

^a UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

Author keywords

Brain; Glycogen; Serotonin; Trout

Indexed keywords

1 (2 METHOXYPHENYL) 4 (4 (2 PHTHALIMIDO)BUTYL)PIPERAZINE; 1 (5 (2 THENYLOXY) 1H INDOL 3 YL)PROPAN 2 AMINE; 1,2,3,5 TETRAHYDRO 5 METHYL 1 (3 PYRIDYLCARBAMOYL)PYRROLO[2,3 F]INDOLE; 1-(2-METHOXYPHENYL)-4-(4-(2-PHTHALIMIDO)BUTYL)PIPERAZINE; 1-(5-(2-THENYLOXY)-1H-INDOL-3-YL)PROPAN-2-AMINE; 2 (((3 (MORPHOLINYLMETHYL) 2H CHROMEN 8 YL)OXY)METHYL)MORPHOLINE; 2-(((3-(MORPHOLINYLMETHYL)-2H-CHROMEN-8-YL)OXY)METHYL)MORPHOLINE; 8,9 DICHLORO 2,3,4,4A TETRAHYDRO 1H PYRAZINO(1,2 A)QUINOXALIN 5(6H) ONE; 8,9-DICHLORO-2,3,4,4A-TETRAHYDRO-1H-PYRAZINO(1,2-A)QUINOXALIN-5(6H)-ONE; BENZOPYRAN DERIVATIVE; GLYCOGEN; GLYCOGEN PHOSPHORYLASE; INDOLE DERIVATIVE; MORPHOLINE DERIVATIVE; N TERT BUTYL 3 [4 (2 METHOXYPHENYL) 1 PIPERAZINYL] 2 PHENYLPROPIONAMIDE; PIPERAZINE DERIVATIVE; PYRAZINE DERIVATIVE; PYRIDINE DERIVATIVE; QUINOXALINE DERIVATIVE; SEROTONIN; SEROTONIN 1 AGONIST; SEROTONIN 1 ANTAGONIST; SEROTONIN 1 RECEPTOR; THIOPHENE DERIVATIVE;

ANIMAL; ARTICLE; BRAIN; DRUG EFFECT; ENZYMOLOGY; GLYCOGENOLYSIS; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; INTRAPERITONEAL DRUG ADMINISTRATION; METABOLISM; RAINBOW TROUT; TIME;

ANIMALS; BENZOPYRANS; BRAIN; GLYCOGEN; GLYCOGEN PHOSPHORYLASE, BRAIN FORM; GLYCOGENOLYSIS; INDOLES; INJECTIONS, INTRAPERITONEAL; INJECTIONS, INTRAVENTRICULAR; MORPHOLINES; ONCORHYNCHUS MYKISS; PIPERAZINES; PYRAZINES; PYRIDINES; QUINOXALINES; RECEPTORS, SEROTONIN, 5-HT1; SEROTONIN; SEROTONIN 5-HT1 RECEPTOR AGONISTS; SEROTONIN 5-HT1 RECEPTOR ANTAGONISTS; THIOPHENES; TIME FACTORS;

EID: 84865257279     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.070649     Document Type: Article

References (91)

1. Ahlander-Lüttgen, M., Madjid, N., Schött, P. A., Sandin, J. and Ogren, S. O. (2003). Analysis of the role of the 5-HT1B receptor in spatial and aversive learning in the rat. Neuropsychopharmacol. 28, 1642-1655.
2. Aldegunde, M. and Mancebo, M. (2006). Effects of neuropeptide Y on food intake and brain biogenic amines in the rainbow trout (Oncorhynchus mykiss). Peptides 27, 719-727.
3. Allee, S. J., Markham, M. R., Salazar, V. K. and Stoddard, P. K. (2008). Opposing actions of 5HT1A and 5HT2-like serotonin receptors on modulations of the electric signal waveform in the electric fish Brachyhypopomus pinnicaudatus. Horm. Behav. 53, 481-488.
4. Baños, N., Baró, J., Castejón, C., Navarro, I. and Gutiérrez, J. (1998). Influence of high-carbohydrate enriched diets on plasma insulin levels and insulin and IGF-I receptors in trout. Regul. Pept. 77, 55-62.
5. Baxter, L. R., Ackermann, R. F., Clark, E. C. and Baxter, J. E. (2001). Brain mediation of Anolis social dominance displays. I. Differential basal ganglia activation. Brain Behav. Evol. 57, 169-183.
6. Blasco, J., Fernández-Borrás, J., Marimon, I. and Requena, A. (1996). Plasma glucose kinetics and tissue uptake in brown trout in vivo: effect of an intravascular glucose load. J. Comp. Physiol. B 165, 534-541.
7. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
8. Brown, A. M. (2004). Brain glycogen re-awakened. J. Neurochem. 89, 537-552.
9. Brown, A. M. and Ransom, B. R. (2007). Astrocyte glycogen and brain energy metabolism. Glia 55, 1263-1271.
10. Bullock, T. H. (2004). The natural history of neuroglia: an agenda for comparative studies. Neuron Glia Biol. 1, 97-100.
11. Butt, C. H., Zhao, B., Duncan, M. J. and Debski, E. A. (2002). Sculpting the visual map: the distribution and function of serotonin-1A and serotonin-1B receptors in the optic tectum of the frog. Brain Res. 931, 21-31.
12. Cambray-Deakin, M., Pearce, B., Morrow, C. and Murphy, S. (1988). Effects of neurotransmitters on astrocyte glycogen stores in vitro. J. Neurochem. 51, 1852-1857.
13. Chen, Y., Peng, L., Zhang, X., Stolzenburg, J.-U. and Hertz, L. (1995). Further evidence that fluoxetine interacts with a 5-HT2c receptor in glial cells. Brain Res. Bull. 38, 153-159.
14. Choi, I. Y., Seaquist, E. R. and Gruetter, R. (2003). Effect of hypoglycemia on brain glycogen metabolism in vivo. J. Neurosci. Res. 72, 25-32.
15. Cowey, C. B., Knox, D., Walton, M. J. and Adron, J. W. (1977). The regulation of gluconeogenesis by diet and insulin in rainbow trout (Salmo gairdneri). Br. J. Nutr 38, 463-470.
16. Cruz, N. F. and Dienel, G. A. (2002). High glycogen levels in brains of rats with minimal environmental stimuli: implications for metabolic contributions of working astrocytes. J. Cereb. Blood Flow Metab. 22, 1476-1489.
17. Darvesh, A. S. and Gudelsky, G. A. (2003). Activation of 5-HT2 receptors induces glycogenosis in the rat brain. Eur. J. Pharmacol. 464, 135-140.
18. Darvesh, A. S., Shankaran, M. and Guldelsky, G. A. (2002). 3,4-Methylenedioxymethamphetamine produces glycogenolysis and increases the extracellular concentration of glucose in the rat brain. J. Pharmacol. Exp. Ther. 300 138-144.
19. De Deurwaerdere, P., Navailles, S., Berg, K. A., Clarke, W. P. and Spampinato, U. (2004). Constitutive activity of the serotonin2C receptor inhibits in vivo dopamine release in the rat striatum and nucleus accumbens. J. Neurosci. 24, 3235-3241.
20. Dietl, M. and Palacios, J. M. (1988). Autoradiographic studies of serotonin receptors. In The Serotonin Receptors (ed. E. Sanders-Bush), pp. 89-138. Clifton, NJ: Humana Press.
21. Egashira, N., Koushi, E., Mishima, K., Iwasaki, K., Oishi, R. and Fujiwara, M. (2007). 2,5-Dimethoxy-4-iodoamphetamine (DOI) inhibits A9-Tetrahydrocannabinol-induced catalepsy-like immobilization in mice. J. Pharmacol. Sci. 105, 361-366.
22. Filipenko, M. L., Beilina, A. G., Alekseyenko, O. V., Dolgov, V. V. and Kudryavtseva, N. N. (2002). Increase in expression of brain serotonin transporter and monoamine oxidase genes induced by repeated experience of social defeats in male mice. Biochemistry 67, 451-455.
23. Forsyth, R., Fray, A., Boutelle, M., Fillenz, M., Middleditch, C. and Burchell, A. (1996). A role for astrocytes in glucose delivery to neurons? Dev. Neurosci. 18, 360-370.
24. Foster, G. D., Youson, J. H. and Moon, T. W. (1993). Carbohydrate metabolism in the brain of the adult lamprey. J. Exp. Zool. 267, 27-32.
25. Frojdo, E. M., Westerlund, J. and Isomaa, B. (2002). Culturing and characterization of astrocytes isolated from juvenile rainbow trout (Oncorhynchus mykiss). Comp. Biochem. Physiol. 133A, 17-28.
26. Gesto, M., Soengas, J. L. and Míguez, J. M. (2008). Acute and prolonged stress responses of brain monoaminergic activity and plasma cortisol levels in rainbow trout are modified by PAHs (naphthalene, beta-naphthoflavone and benzo(a)pyrene) treatment. Aquat. Toxicol. 86, 341-351.
27. Ginawi, O. T., Al-Majed, A. A. and Al-Suwailem, A. K. (2005). NAN-190, a possible specific antagonist for methamphetamine. Regul. Toxicol. Pharmacol. 41, 122-127.
28. Hansley, S. H. and Cohen, J. L. (1992). Effects of serotonergic agonists and antagonists on ganglion cells in goldfish retina. Visual Neurosci. 9, 353-364.
29. Hanssonp, E. and Rönnbäck, L. (2004). Astrocytic receptors and second messenger systems. Adv. Mol. Cell Biol. 31, 475-501.
30. Herzog, R. I., Chan, O., Yu, S., Dziura, J., McNay, E. C. and Sherwin, R. S. (2008) Effect of acute and recurrent hypoglycemia on changes in brain glycogen concentration. Endocrinology 149, 1499-1504.
31. Hirst, W. D., Price, G. W., Rattray, M. and Wilkin, G. P. (1997). Identification of 5-hydroxytryptamine receptors positively coupled to adenylyl cyclase in rat cultured astrocytes. Br. J. Pharmacol. 120, 509-515.
32. Hirst, W. D., Cheung, N. Y., Rattray, M., Price, G. W. and Wilkin, G. P. (1998) Cultured astrocytes express messenger RNA for multiple serotonin receptor subtypes, without functional coupling of 5-HT1 receptor subtypes to adenylyl cyclase. Brain Res. Mol. Brain Res. 61, 90-99.
33. Ichikawa, J. and Meltzer, H. Y. (1995). DOI, a 5-HT2A/2C receptor agonist potentiates amphetamine-induced dopamine release in rat striatum. Brain Res. 698, 204-208.
34. Jacobs, B. L. and Azmitia, E. C. (1992). Structure and function of the brain serotonin system. Physiol. Rev. 72, 165-229.
35. Joseph, M. and Kennet, G. (1981). Brain tryptophan and 5-HT function in stress. Br. J. Pharmacol. 73, 267-271.
36. Keppler, D. and Decker, K. (1974). Glycogen determination with amyloglucosidase. In Methods of Enzymatic Analysis (ed. H. U. Bergmeyer), pp. 1127-1131. New York: Academic Press.
37. Khanbabian, M. V., Kirakosyan, M. P. and Sargsyan, R. Sh. (2002) Electrophysiological and pharmacological analysis of neuronal activity in the midbrain medial raphe nucleus after acute immobilization stress. Neurophysiol. 34, 147-149.
38. Kreke, N. and Dietrich, D. R. (2008). Physiological endpoints for potential SSRI interactions in fish. Crit. Rev. Toxicol. 38, 215-247.
39. Kroeze, W. K. and Roth, B. L. (2006). Molecular Biology and genomic organization of G-protein-Couple Serotonin Receptors. In The Serotonin Receptors: From Molecular Pharmacology to Human Therapeutics (ed. B. L. Roth), pp. 1-38. Totowa, NJ: Humana Press.
40. Kruger, L. and Maxwell, D. S. (1967). Comparative fine structure of vertebrate neuroglia: teleosts and reptiles. J. Comp. Neurol. 129, 115-142.
41. Li, B., Zhang, S., Zhang, H., Un, W., Cai, L., Hertz, L. and Peng, L. (2008) Fluoxetine-mediated 5-HT2B receptor stimulation in astrocytes causes EGF receptor transactivation and ERK phosphorylation. Psychopharmacology 201, 443-458.
42. Magistretti, P. J. (1988). Regulation of glycogenolysis by neurotransmitters in the central nervous system. Diabete. Metab. 14, 237-246.
43. Magistretti, P. J., Sorg, O. and Martin, J. (1993). Regulation of glycogen metabolism in astrocytes: physiological, pharmacological, and pathological aspects. In Astrocytes Pharmacology and Function (ed. S. Murphy), pp. 243-265. San Diego, CA: Academic Press.
44. Magnoni, L. J., Míguez, J. M. and Soengas, J. L. (2001). Glucagon effects on brain carbohydrate and ketone body metabolism of rainbow trout. J. Exp. Zool. 290, 662-71.
45. McEwen, B. S. (2007). Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol. Rev. 87, 873-904.
46. McLean, D. L. and Sillar, K. T. (2004). Divergent actions of serotonin receptor activation during fictive swimming in frog embryos. J. Comp. Physiol. A 190, 391-402.
47. Monzon-Mayor, M., Yanes, C., Jamest, J. L. and Sturrock R. R. (1990). An ultrastructural study of the development of astrocytes in the midbrain of the lizard. J. Anat. 170, 33-41.
48. Moon, T. W. (2001). Glucose intolerance in teleost fish: fact or fiction? Comp. Biochem. Physiol. 129B, 243-249.
49. Moon, T. W., Foster, G. D. and Plisetskaya, E. M. (1989). Changes in peptide hormones and liver enzymes in the rainbow trout deprived of food for 6 weeks. Can. J. Zool. 67, 2189-2193.
50. Morgan, W. W. and Rudeen, P. K. (1976). Temporal study of 5-hydroxyindoleacetic acid normalization during recovery from immobilization stress. Exp. Neurol. 51, 259-262.
51. Morgenthaler, F. D., Dee, M., Koski, A., Kraftsik, R., Henry, P.-G. and Gruetter, R. (2006). Biochemical quantification of total brain glycogen concentration in rats under different glycemic states. Neurochem. Int. 48, 616-622.
52. Norton, W. H., Folchert, A. and Bally-Cuif, L. (2008). Comparative analysis of serotonin receptor (HTR1A/HTR1B families) and transporter (slc6a4a/b) gene expression in the zebrafish brain. J. Comp. Neurol. 511, 521-542.
53. Ochi, T. and Goto, T. (2000). The antinociceptive effect induced by FR140423 is mediated through spinal 5-HT2A and 5-HT3 receptors. Eur. J. Pharmacol. 409, 167-172.
54. Osredkar, D., and Krzan, M. (2009). Expression of serotonin receptor subtypes in rat brain and astrocyte cell cultures: an age and tissue-dependent process. Periodicum Biologorum 111, 129-135.
55. Oz, G., Seaquist, E. R., Kumar, A., Criego, A. B., Benedict, L. E., Rao, J. P., Henry, P. G., Van De Moortele, P. F. and Gruetter, R. (2007). Human brain glycogen content and metabolism: implications on its role in brain energy metabolism. Am. J. Physiol. Endocrinol. Metab. 292, E946-E951.
56. Palacios, J. M., and Dietl, M. M. (1988). Autoradiographic studies of serotonin receptors. In The Serotonin Receptors (ed. E. Sanders-Bush), pp. 89-134. Clifton, NJ: Humana Press.
57. Papp, M. and Willmer, P. (1991). 8-OH-DPAT-induced place preference and place aversion: effects of PCPA and dopamine antagonists. Psychopharmacol. 103, 99-102.
58. Parent, A. (1981). Comparative anatomy of the serotoninergic systems. J. Physiol. (Paris) 77, 147-156.
59. Parent, A., Poitras, D., and Dubé, L. (1984). Comparative anatomy of central monoaminergic systems. In Handbook of Chemical Neuroanatomy (ed. A. Björklund and T. Hökfelt), pp. 409-439. Oxford: Elsevier.
60. Pellerin, L., Bouzier-Sore, A. K., Aubert, A., Serres, S., Merle, M., Costalat, R. and Magistretti, P. J. (2007). Activity-dependent regulation of energy metabolism by astrocytes: an update. Glia 55, 1251-1262.
61. Poblete, J. C. and Azmitia, E. C. (1995). Activation of glycogen phosphorylase by serotonin and 3,4-methylenedioxymethamphetamine in astroglial-rich primary cultures: involvement of the 5-HT2A receptor. Brain Res. 680, 9-15.
62. Polakof, S., Arjona, F. J., Sangiao-Alvarellos, S., Martín del Río, M. P., Mancera, J. M. and Soengas, J. L. (2006). Food deprivation alters osmoregulatory and metabolic responses to salinity acclimation in gilthead sea bream Sparus auratus. J. Comp. Physiol. B 176, 441-452.
63. Polakof, S., Míguez, J. M. and Soengas, J. L. (2008). Changes in food intake and glucosensing function of hypothalamus and hindbrain in rainbow trout subjected to hyperglycemic or hypoglycemic conditions. J. Comp. Physiol. A 194, 829-839.
64. Porter, J. T. and McCarthy, K. D. (1997). Astrocytic neurotransmitter receptors in situ and in vivo. Prog. Neurobiol. 51, 439-455.
65. Quach, T. T., Duchemin, A. M., Rose, C. and Schwartz, J.-C. (1982). Glycogenolysis induced by serotonin in brain: identification of a new class of receptor. Nature 298, 373-375.
66. Rodriguez de Fonseca, F., Navarro, M., Gomez, R., Escuredo, L., Nava, F., Fu, J., Murillo-RodrIguez, E., Giuffrida, A., LoVerme, J., Gaetani, S. et al. (2001). An anorexic lipid mediator regulated by feeding. Nature 414, 209-212.
67. Roots, B. I. (1986). Phylogenetic development of astrocytes. In Astrocytes, vol. 1 (ed. S. Fedoroff and A. Vernadakis), pp. 1-34. New York: Academic Press.
68. Ruibal, C., Soengas, J. L. and Aldegunde, M. (2002). Brain serotonin and the control of food intake in rainbow trout (Oncorhynchus mykiss): effects of changes in plasma glucose levels. J. Comp. Physiol. A 188, 479-484.
69. Samosudova, N. V., Reutov, V. P., and Larionova, N. P. (2010). Role of glycogen in processes of cerebellar glial cells under conditions of its damage with sodium nitrite. Bull. Exp. Biol. Med. 150, 247-250.
70. Sangiao-Alvarellos, S., Bouça, P., Miguez, J. M. and Soengas, J. L. (2003). Intracerebroventricular injections of noradrenaline affect brain energy metabolism of rainbow trout. Physiol. Biochem. Zool. 76, 663-671.
71. Sangiao-Alvarellos, S, Lapido, M., Míguez, J. M. and Soengas, J. L. (2004). Effects of central administration of arginine vasotocin on monoaminergic neurotransmitters and energy metabolism of rainbow trout brain. J. Fish Biol. 64, 1313-1329.
72. Sangiao-Alvarellos, S., Arjona, F. J., Míguez, J. M., Martín del Río, M. P., Soengas, J. L. and Mancera, J. M. (2006). Growth hormone and prolactin actions on osmoregulation and energy metabolism of gilthead sea bream (Sparus auratus). Comp. Biochem. Physiol. 144A, 491-500.
73. Schreiber, R., Selbach, K., Asmussen, M., Hesse, D. and de Vry, J. (2000). Effects of serotonin1/2 receptor agonists on dark-phase food and water intake in rats. Pharmacol. Biochem. Behav. 67, 291-305.
74. Singh, V. B., Corley, K. C., Krieg, R. J., Phan, T. H. and Boadle-Biber, M. C. (1994). Sound stress activation of tryptophan hydroxylase blocked by hypophysectomy and intracranial RU 38486. Eur. J. Pharmacol. 256, 177-184.
75. Soengas, J. L. and Aldegunde, M. (2002). Energy metabolism of fish brain. Comp. Biochem. Physiol. 131B, 271-296.
76. Soengas, J. L. and Aldegunde, M. (2004). Brain glucose and insulin: effects on food intake and brain biogenic amines of rainbow trout. J. Comp. Physiol. A 190, 641-649.
77. Soengas, J. L., Strong, E. F., Fuentes, J., Veira, J. A. R. and Andrés, M. D. (1996). Food deprivation and refeeding in Atlantic salmon, Salmo salar: effects on brain and liver carbohydrate and ketone bodies metabolism. Fish Physiol. Biochem. 15, 491-511.
78. Soengas, J. L., Strong, E. F. Andrés, M. D. and Aldegunde, M. (1998a). Dose-dependent effects of acute melatonin treatments on brain carbohydrate metabolism of rainbow trout. Fish Physiol. Biochem. 18, 311-319.
79. Soengas, J. L., Strong, E. F. and Andres, M. D. (1998b). Glucose, lactate, and β-hydroxybutyrate utilization by rainbow trout brain: changes during food deprivation. Physiol. Zool. 71, 285-293.
80. Summers, C. H. and Winberg, S. (2006). Interactions between the neural regulation of stress and aggression. J. Exp. Biol. 209, 4581-4589.
81. Swanson, R. A. and Choi, D. W. (1993). Glial glycogen stores affect neuronal survival during glucose deprivation in vitro. J. Cereb. Blood Flow Metab. 13, 162-169.
82. Swanson, R. A., Morton, M. M., Sagar, S. M. and Sharp, F. R. (1992). Sensory stimulation induces local cerebral glycogenolysis: demonstration by autoradiography. Neuroscience 51, 451-461.
83. Swedberg, M. D., Shannon, H. E., Nickel, B. and Goldberg, S. R. (1992). D-16949 (anpirtoline): a novel serotonergic (5-HT1B) psychotherapeutic agent assessed by its discriminative effects in the rat. J. Pharm. Exp. Ther. 263, 1015-1022.
84. Tubío, R. I., Pérez-Maceira, J. and Aldegunde, M. (2010). Homeostasis of glucose in the rainbow trout (Oncorhynchus mykiss Walbaum): the role of serotonin. J. Exp. Biol. 213, 1813-1821.
85. Verkhratsky, A. (2010). Physiology of neuronal-glial networking. Neurochem. Int. 57, 332-343.
86. Wender, R., Brown, A. M., Fern, R., Swanson, R. A., Farrell, K. and Ransom, B. R. (2000). Astrocytic glycogen influences axon function and survival during glucose deprivation in central white matter. J. Neurosci. 20, 6804-6810.
87. Winberg, S. and Lepage, O. (1998). Elevation of brain 5-HT activity, POMC expression, and plasma cortisol in socially subordinate rainbow trout. Am. J. Physiol. 274, R645-R654.
88. Winberg, S. and Nilsson, G. E. (1993). Roles of brain monoamine neurotransmitters in agonistic behaviour and stress reactions, with particular reference to fish. Comp. Biochem. Physiol. 10C, 597-614.
89. Winberg, S. and Nilsson, G. E. (1996). Multiple high affinity binding sites for [3H]serotonin in the brain of a teleost fish, the Arctic charr (Salvelinus alpinus). J. Exp. Biol. 199, 2429-2435.
90. Winberg, S., Nilsson, A., Hylland, P., Söderstöm, V. and Nilsson, G. E. (1997). Serotonin as a regulator of hypothalamic-pituitary- interrenal activity in teleost fish. Neurosci. Lett. 230, 113-116.
91. Xiaohu, Z., Peng, L., Chen, Y. and Hertz, L. (1993). Stimulation of glycogenolysis in astrocytes by fluoxetine, an antidepressant acting like 5-HT. Neuroreport 4, 1235-1238.