Skip to main content Accessibility help
×
Home
Hostname: page-component-78dcdb465f-cs4hf Total loading time: 0.324 Render date: 2021-04-19T04:39:21.974Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": false, "newCiteModal": false, "newCitedByModal": true }

Nutritional regulation of glucose-6-phosphatase gene expression in liver of the gilthead sea bream (Sparus aurata)

Published online by Cambridge University Press:  09 March 2007

A. Caseras
Affiliation:
Department de Bioquímica i Biologia Molecular, Facultat de Farmàcia, Universitat de Barcelona, Barcelona, Spain
I. Metón
Affiliation:
Department de Bioquímica i Biologia Molecular, Facultat de Farmàcia, Universitat de Barcelona, Barcelona, Spain
C. Vives
Affiliation:
Department de Bioquímica i Biologia Molecular, Facultat de Farmàcia, Universitat de Barcelona, Barcelona, Spain
M. Egea
Affiliation:
Department de Bioquímica i Biologia Molecular, Facultat de Farmàcia, Universitat de Barcelona, Barcelona, Spain
F. Fernández
Affiliation:
Department d'Ecologia, Facultat de Biologia, Universitat de Barcelona, Barcelona, Spain
I. V. Baanante
Affiliation:
Department de Bioquímica i Biologia Molecular, Facultat de Farmàcia, Universitat de Barcelona, Barcelona, Spain
Corresponding
Rights & Permissions[Opens in a new window]

Abstract

To examine the role of glucose-6-phosphatase (G6Pase) in glucose homeostasis in the diabetes-like experimental model of carnivorous fish, we analysed postprandial variations and the effect of starvation, ration size and diet composition on the regulation of G6Pase expression at the enzyme activity and mRNA level in the liver of gilthead sea bream (Sparus aurata). G6Pase expression increased in long-term starved or energy-restricted fish. In contrast to data reported for other fish species, short-term regulation of G6Pase expression was found in regularly fed S. aurata. G6Pase mRNA levels were lowest between 4 and 15 h after food intake, whereas minimal enzyme activity was observed 10–15 h postprandially. Alterations of plasma glucose levels affect G6Pase in mammals. However, the carbohydrate content of the diet did not affect hepatic expression of G6Pase in S. aurata, suggesting that a different molecular mechanism is involved in the control of G6Pase expression in fish. Although G6Pase was unaffected, high-carbohydrate low-protein diets increased glucokinase (GK) expression and thus allowed a metabolic adaptation favouring glycolysis over gluconeogenesis. Interestingly, only the nutritional conditions that promoted variations in the blood glucose levels resulted in changes in the hepatic expression of G6Pase. These findings indicate a concerted regulation of G6Pase and GK expression and suggest that the direction and rate of the glucose–glucose-6-phosphate substrate cycle flux is finely regulated in the liver of S. aurata, challenging the role attributed to deficient regulation of G6Pase or GK expression in the low ability of carnivorous fish to metabolize glucose.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2002

References

Argaud, D, Kirby, TL, Newgard, CB & Lange, AJ (1997) Stimulation of glucose-6-phosphatase gene expression by glucose and fructose-2,6-bisphosphate. Journal of Biological Chemistry 272, 1285412861.CrossRefGoogle ScholarPubMed
Argaud, D, Zhang, Q, Pan, W, Maitra, S, Pilkis, SJ & Lange, AJ (1996) Regulation of rat liver glucose-6-phosphatase gene expression in different nutritional and hormonal states. Gene structure and 5'-flanking sequence. Diabetes 45, 15631571.Google ScholarPubMed
Arion, WJ, Lange, AJ, Walls, HE & Ballas, LM (1980) Evidence for the participation of independent translocation for phosphate and glucose 6-phosphate in the microsomal glucose-6-phosphatase system. Interactions of the system with orthophosphate inorganic phosphate and carbamyl phosphate. Journal of Biological Chemistry 255, 1039610406.Google ScholarPubMed
Arion, WJ, Wallin, BK, Lange, AJ & Ballas, LM (1975) On the involvement of a glucose 6-phosphate transport system in the function of microsomal glucose-6-phosphatase. Molecular and Cellular Biochemistry 6, 7583.CrossRefGoogle ScholarPubMed
Baanante, IV, García de Frutos, P, Bonamusa, L & Fernández, F (1991) Regulation of fish glycolysis-gluconeogenesis, role of fructose 2,6-P2 and PFK-2. Comparative Biochemistry and Physiology 100B, 1117.Google Scholar
Bonamusa, L, García de Frutos, P, Fernández, F & Baanante, IV (1992) Nutritional effects on key glycolytic-gluconeogenic enzyme activities and metabolite levels in the liver of the teleost fish Sparus aurata. Molecular Marine Biology and Biotechnology 1, 113125.Google Scholar
Borrebaek, B, Waagbo, R, Christophersen, B, Tranulis, MA & Hemre, G-I (1993) Adaptable hexokinase with low affinity for glucose in the liver of Atlantic salmon (Salmo salar). Comparative Biochemistry and Physiology 106B, 833836.Google Scholar
Bradford, MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248254.CrossRefGoogle ScholarPubMed
Caseras, A, Metón, I, Fernández, F & Baanante, IV (2000) Glucokinase gene expression is nutritionally regulated in the liver of gilthead seabream (Sparus aurata). Biochimica et Biophysica Acta 1493, 135141.CrossRefGoogle Scholar
Chatelain, F, Pegorier, JP, Minassian, C, Bruni, N, Tarpin, S, Girard, J & Mithieux, G (1998) Development and regulation of glucose-6-phosphatase gene expression in rat liver intestine and kidney, in vivo and in vitro studies in cultured fetal hepatocytes Diabetes 47, 882889.CrossRefGoogle ScholarPubMed
Christiansen, DG & Klungsøyr, L (1987) Metabolic utilization of nutrients and the effects of insulin in fish. Comparative Biochemistry and Physiology 88B, 701711.Google Scholar
Cowey, CB & Walton, MJ (1989) Intermediary metabolism. In Fish Nutrition, pp. 260321 [Halver, JE, editor]. San Diego: Academic Press.Google Scholar
Foster, GD & Moon, TW (1991) Hypometabolism with fasting in the yellow perch (Perca flavescens), a study of enzymes, hepatocyte metabolism and tissue size. Physiological Zoology 64, 259275.CrossRefGoogle Scholar
Guignot, L & Mithieux, G (1999) Mechanisms by which insulin associated or not with glucose may inhibit hepatic glucose production in the rat. American Journal of Physiology 277, E984E989.Google ScholarPubMed
Herzig, S, Long, F, Jhala, US, Hedrick, S, Quinn, R, Bauer, A, Rudolph, D, Schutz, G, Yoon, C, Puigserver, P, Spiegelman, B & Montminy, M (2001) CREB regulates hepatic gluconeogenesis through the coactivator PGC-1. Nature 413, 179183.CrossRefGoogle ScholarPubMed
Massillon, D (2001) Regulation of glucose-6-phosphatase gene by glucose occurs by transcriptional and post-transcriptional mechanisms. Journal of Biological Chemistry 276, 40554062.CrossRefGoogle ScholarPubMed
Massillon, D, Barzilai, N, Chen, W, Hu, M & Rossetti, L (1996) Glucose regulates in vivo glucose-6-phosphatase gene expression in the liver of diabetic rats. Journal of Biological Chemistry 271, 98719874.CrossRefGoogle ScholarPubMed
Massillon, D, Chen, W, Barzilai, N, Prus-Wertheimer, D, Hawkins, M, Liu, R, Taub, R & Rossetti, L (1998) Carbon flux via the pentose phosphate pathway regulates the hepatic expression of the glucose-6-phosphatase and phosphoenolpyruvate carboxykinase genes in conscious rats. Journal of Biological Chemistry 273, 228234.CrossRefGoogle ScholarPubMed
Metón, I, Caseras, A, Fernández, F & Baanante, IV (2000) 6-Phosphofructo-2-kinase/fructose-2,6-bisphosphatase gene expression is regulated by diet composition and ration size in liver of gilthead sea bream Sparus aurata Biochimica et Biophysica Acta 1491, 220228.CrossRefGoogle ScholarPubMed
Metón, I, Caseras, A, Mediavilla, D, Fernández, F & Baanante, IV (1999a) Molecular cloning of a cDNA encoding 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase from liver of Sparus aurata, nutritional regulation of enzyme expression. Biochimica et Biophysica Acta 1444, 153165.CrossRefGoogle ScholarPubMed
Metón, I, Mediavilla, D, Caseras, A, Cantó, E, Fernández, F & Baanante, IV (1999b) Effect of diet composition and ration size on key enzyme activities of glycolysis-gluconeogenesis pentose phosphate pathway and amino acid metabolism in liver of gilthead sea bream (Sparus aurata). British Journal of Nutrition 82, 223232.Google Scholar
Minassian, C, Montano, S & Mithieux, G (1999) Regulatory role of glucose-6-phosphatase in the repletion of liver glycogen during refeeding in fasted rats. Biochimica et Biophysica Acta 1452, 172178.CrossRefGoogle ScholarPubMed
Morata, P, Vargas, AM, Sanchez-Medina, F, Garcia, M, Cardenete, G & Zamora, S (1982) Evolution of gluconeogenic enzyme activities during starvation in liver and kidney of the rainbow trout (Salmo gairdneri). Comparative Biochemistry and Physiology 71B, 6570.Google Scholar
Nordlie, RC, Foster, JD & Lange, AJ (1999) Regulation of glucose production by the liver. Annual Review of Nutrition 19, 379406.CrossRefGoogle ScholarPubMed
O'Brien, RM & Granner, DK (1996) Regulation of gene expression by insulin. Physiological Reviews 76, 11091161.CrossRefGoogle ScholarPubMed
Palmer, TN & Ryman, BE (1972) Studies on oral glucose tolerance tests in fish. Journal of Fish Biology 4, 311319.CrossRefGoogle Scholar
Panserat, S, Blin, C, Médale, F, Plagnes-Juan, E, Brèque, J, Krishnamoorthy, J & Kaushik, S (2000a) Molecular cloning tissue distribution and sequence analysis of complete glucokinase cDNAs from gilthead seabream (Sparus aurata), rainbow trout (Oncorynchus mykiss) and common carp (Cyprinus carpio). Biochimica et Biophysica Acta 1474, 6169.CrossRefGoogle Scholar
Panserat, S, Capilla, E, Gutierrez, J, Frappart, PO, Vachot, C, Plagnes-Juan, E, Aguirre, P, Brèque, J & Kaushik, S (2001) Glucokinase is highly induced and glucose-6-phosphatase poorly repressed in liver of rainbow trout (Oncorhynchus mykiss) by a single meal with glucose. Comparative Biochemistry and Physiology 128B, 275283.CrossRefGoogle Scholar
Panserat, S, Médale, F, Blin, C, Brèque, J, Vachot, C, Plagnes-Juan, E, Gomes, E, Krishnamoorthy, R & Kaushik, S (2000b) Hepatic glucokinase is induced by dietary carbohydrates in rainbow trout, gilthead seabream and common carp. American Journal of Physiology 278, R1164R1170.Google ScholarPubMed
Panserat, S, Médale, F, Brèque, J, Plagnes-Juan, E & Kaushik, S (2000c) Lack of significant long-term effect of dietary carbohydrates on hepatic glucose-6-phosphatase expression in rainbow trout (Oncorhynchus mykiss). Journal of Nutritional Biochemistry 11, 2229.CrossRefGoogle Scholar
Sambrook, J, Fritsch, EF & Maniatis, T (1989) Extraction, purification and analysis of messenger RNA from eukaryotic cells. In Molecular Cloning, a Laboratory Manual, 2nd ed., pp. 7.1–7.87 [Nolan, C, editor]. Cold Spring Harbour: Cold Spring Harbour Laboratory Press.Google Scholar
Seoane, J, Trinh, K, O'Doherty, RM, Gómez-Foix, AM, Lange, AJ, Newgard, CB & Guinovart, JJ (1997) Metabolic impact of adenovirus-mediated overexpression of the glucose-6-phosphatase catalytic subunit in hepatocytes. Journal of Biological Chemistry 272, 2697226977.CrossRefGoogle ScholarPubMed
Shikata, T, Kheyyali, D & Shimeno, S (1993) Effect of feeding rates on hepatopancreatic enzymes and body composition in common carp. Nippon Suisan Gakkaishi 59, 835839.CrossRefGoogle Scholar
Shimeno, S, Ming, D-C, & Takeda, M (1993) Metabolic response to dietary carbohydrate to lipid ratios in Oreochromis niloticus. Nippon Suisan Gakkaishi 59, 827833.CrossRefGoogle Scholar
Trinh, KY, O'Doherty, RM, Anderson, P, Lange, AJ & Newgard, CB (1998) Perturbation of fuel homeostasis caused by overexpression of the glucose-6-phosphatase catalytic subunit in liver of normal rats. Journal of Biological Chemistry 273, 3161531620.CrossRefGoogle ScholarPubMed
Van de Werve, G, Lange, AJ, Newgard, C, Méchin, M-C, Li, Y & Berteloot, A (2000) New lessons in the regulation of glucose metabolism taught by the glucose-6-phosphatase system. European Journal of Biochemistry 267, 15331549.CrossRefGoogle ScholarPubMed
Wilson, RP (1994) Utilization of dietary carbohydrate by fish. Aquaculture 124, 6780.CrossRefGoogle Scholar
Windham, WR (1997) Animal feed. In Official Methods of Analysis, 16th ed., pp. 4.14.46 [Cunnif, P, editor]. Gaithersburg, MD: AOAC International.Google Scholar
Wright, JR Jr, O'Hali, W, Yang, H, Han, X-X, & Bonen, A (1998) GLUT-4 deficiency and severe peripheral resistance to insulin in the teleost fish tilapia. General Comparative Endocrinology 111, 2027.CrossRefGoogle ScholarPubMed
Yoon, JC, Puigserver, P, Chen, G, Donovan, J, Wu, Z, Rhee, J, Adelmant, G, Stafford, J, Kahn, CR, Granner, DK, Newgard, CB & Spiegelman, BM (2001) Control of hepatic gluconeogenesis through the transcriptional coactivator PGC-1. Nature 413, 131138.CrossRefGoogle ScholarPubMed

Full text views

Full text views reflects PDF downloads, PDFs sent to Google Drive, Dropbox and Kindle and HTML full text views.

Total number of HTML views: 0
Total number of PDF views: 354 *
View data table for this chart

* Views captured on Cambridge Core between September 2016 - 19th April 2021. This data will be updated every 24 hours.

You have Access

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Nutritional regulation of glucose-6-phosphatase gene expression in liver of the gilthead sea bream (Sparus aurata)
Available formats
×

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

Nutritional regulation of glucose-6-phosphatase gene expression in liver of the gilthead sea bream (Sparus aurata)
Available formats
×

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

Nutritional regulation of glucose-6-phosphatase gene expression in liver of the gilthead sea bream (Sparus aurata)
Available formats
×
×

Reply to: Submit a response


Your details


Conflicting interests

Do you have any conflicting interests? *