Regulation of Rat Liver Glucose-6-Phosphatase Gene Expression in Different Nutritional and Hormonal States: Gene Structure and 5′-Flanking Sequence

Argaud, Doriane; Zhang, Qing; Pan, Wansong; Maitra, Subir; Pilkis, Simon J; Lange, Alex J

doi:10.2337/diab.45.11.1563

Cited by 168Glycogen Storage Diseases and MyoclonusMetabolism, Diabetes, and CancerBiochemical and Molecular Research

Regulation of Rat Liver Glucose-6-Phosphatase Gene Expression in Different Nutritional and Hormonal States: Gene Structure and 5′-Flanking Sequence

Argaud, Doriane, Zhang, Qing, Pan, Wansong, Maitra, Subir, Pilkis, Simon J, Lange, Alex J·1996·Diabetes

DOI 10.2337/diab.45.11.1563

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Abstract

The mRNA level of the catalytic subunit of rat liver glucose-6-phosphatase (Glu-6-Pase) was regulated by hormones commensurate with activity changes in vivo. Insulin exerts a dominant negative effect on the mRNA levels of Glu-6-Pase. Both mRNA levels and activities of the enzyme are low in the fed and refed state where insulin levels are elevated. Insulin administration to diabetic rats also decreases levels of mRNA and Glu-6-Pase activity. Insulin at a concentration of 1 nmol/l completely overcomes the stimulatory effect of glucocorticoids on Glu-6-Pase message levels in FAO hepatoma cells. The stimulatory response to glucocorticoid in FAO cells is biphasic, with maxima seen at 3 and 18 h after hormone addition (respectively 1.6- and 3.3-fold). 8-(4-chlorophenylthio)-cAMP (CPT-cAMP) causes a fourfold increase in Glu-6-Pase mRNA at 3 h in FAO cells. The gene of rat liver Glu-6-Pase is 13 kilobases in length and comprised of 5 exons. The exon-intron structure is completely conserved when compared with the mouse and human genes. A 0.5-kb 3′-untranslated region, which is present in rat and mouse liver Glu-6-Pase cDNA, is absent in the Glu-6-Pase gene reported here, indicating the possible duplication of either the terminal fifth exon or the entire gene. The promoter region contains a consensus core CCAAT element at position –207 and a TATAAA at position –31. Several possible response elements have been identified in the 5′-flanking region (from a HindIII site at position –1641). A consensus glucocorticoid response element is located at base pair –1552, a 9/10 match of the insulin response sequence is located at position –1449, and a 7/8 match of the cAMP response element is located at position –164.

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Starvation and diabetes cause a two- to threefold increase in gluconeogenic enzyme activity in the liver associated with a two- to fourfold increase in PEPCK and G-6-Pase mRNA.
“Starvation and diabetes cause a two- to threefold increase in gluconeogenic enzyme activity in the liver that is associated with a two- to fourfold increase in PEPCK and G-6-Pase mRNA (1).”
From Hypoglycemic effects of brassinosteroid in diet-induced obese mice (2012) · cites this paper as [1]

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Self-citation
Increasing fructose 2,6-bisphosphate overcomes hepatic insulin resistance of type 2 diabetes
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Self-citation
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“In contrast, the catalytic enzyme activity [13-16], protein content [16] and mRNA levels [13,14] are all increased in diabetic animals and presumably contribute to the prevailing hyperglycaemia.”
Background
Gossypol ameliorates liver fibrosis in diabetic rats induced by high-fat diet and streptozocin
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“…g6p syn = 1.16 · 10 −2 k1 = 1 k2 = 0.8 n1 = 3 Kglucagon = 100 pM k3 = 1 k4 = 15 keff = 0.3 Kglcext = 17 mM n2 = 20 k g6p deg k g6p deg = ln(2) 48 Leskes et al., 1971; Argaud et al., 1996; Massillon, 2001 Phosphofructokinase 1 k pfk1 syn k pfk1 syn = 7.8 · 10 −3 k pfk1 deg k pfk1 deg =…”
Influential
Differential regulation of the glucose-6-phosphatase TATA box by intestine-specific homeodomain proteins CDX1 and CDX2
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“In this study, we have investigated whether the Glc6Pase promoter could be regulated by CDX proteins, with a particular interest in the ATATAAAATG sequence located ‐31/‐25 bp upstream of the transcription start site, previously hypothesized to constitute the TATA box of the gene ( 24 ).”
Background
Several Transcription Factors Are Recruited to the Glucose-6-Phosphatase Gene Promoter in Response to Palmitate in Rat Hepatocytes and H4IIE Cells
Xu, C., Chakravarty, K., Kong, X., Tuy, T. T., Arinze, I., Bone, F., & Massillon, D. (2007) · Journal of Nutrition · doi:10.1093/jn/137.3.554 · Cited by 33 · see citing works
Diabetes Affects Similarly the Catalytic Subunit and Putative Glucose-6-phosphate Translocase of Glucose-6-phosphatase
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Natural products, an important resource for discovery of multitarget drugs and functional food for regulation of hepatic glucose metabolism
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Elements of the Glucocorticoid and Retinoic Acid Response Units Are Involved in cAMP-mediated Expression of the PEPCK Gene
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“Because G6Pase expression is increased by glucagon and decreased by insulin (2, 29), the decrease in steady-state levels of G6Pase is inappropriate and indicates that hormonal modulation of G6Pase is altered in sepsis.”
BackgroundResultInfluential
Inhibition by Insulin of Glucocorticoid-Induced Gene Transcription: Involvement of the Ligand-Binding Domain of the Glucocorticoid Receptor and Independence from the Phosphatidylinositol 3-Kinase and Mitogen-Activated Protein Kinase Pathways
Pierreux, C. E., Ursø, B., MEYTS, P. D., Rousseau, G. G., & Lemaigre, F. P. (1998) · Molecular Endocrinology · doi:10.1210/mend.12.9.0172 · Cited by 31 · see citing works
Physical exercise enhances hepatic insulin signaling and inhibits phosphoenolpyruvate carboxykinase activity in diabetes-prone Psammomys obesus
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Transcriptional activation of SHP by PPAR-γ in liver
Kim, H., Koh, Y.-K., Kim, T. H., Kwon, S., Im, S., Choi, H.-S., Kim, K., & Ahn, Y. (2007) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2007.05.171 · Cited by 28 · see citing works
Upregulation of Hepatic Glucose 6-Phosphatase Gene Expression in Rats Treated with an Inhibitor of Glucose-6-phosphate Translocase
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Selective stimulation of G-6-Pase catalytic subunit but not G-6-Ptransporter gene expression by glucagon in vivo and cAMP in situ
Hornbuckle, L. A., Everett, C. A., Martin, C. C., Gustavson, S. S., Svitek, C. A., Oeser, J. K., Neal, D. W., Cherrington, A. D., & O’Brien, R. M. (2004) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00455.2003 · Cited by 26 · see citing works
“The generation of the heterologous XMB vector that contains a minimal Xenopus 68 kDa albumin promoter ligated to the CAT reporter gene has previously been described (10), as have the CRE1 WT XMB, CRE1 MUT XMB and CRE2 WT XMB plasmids which contain multiple (3-4) copies of doublestranded complementary oligonucleotides…”
BackgroundMethod
Transcriptional regulation of glucose-6-phosphatase catalytic subunit promoter by insulin and glucose in the carnivorous fish, Sparus aurata
Salgado, M. C. D. O., Metón, I., Egea, M., & Baanante, I. V. (2004) · Journal of Molecular Endocrinology · doi:10.1677/jme.1.01552 · Cited by 27 · see citing works
“In rats, starvation and hormones that increase cAMP stimulate G6pc expression, whereas refeeding and insulin administration decrease it ( Argaud et al. 1996, Minassian et al. 1999).”
Background
Peroxyvanadium Compounds Inhibit Glucose-6-phosphatase Activity and Glucagon-Stimulated Hepatic Glucose Output in the Ratin Vivo
Westergaard, N., Brand, C. L., Lewinsky, R., Andersen, H. S., Carr, R. D., Burchell, A. N., & Lundgren, K. (1999) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1999.1181 · Cited by 26 · see citing works
Revealing Alteration in the Hepatic Glucose Metabolism of Genetically Improved Carp, Jayanti Rohu Labeo rohita Fed a High Carbohydrate Diet Using Transcriptome Sequencing
Rasal, K. D., Iquebal, M. A., Dixit, S., Vasam, M., Raza, M., Sahoo, L., Jaiswal, S., Nandi, S., Mahapatra, K. D., Rasal, A. R., et al. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21218180 · Cited by 25 · see citing works
FGF21 suppresses hepatic glucose production through the activation of atypical protein kinase Cι/λ
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Procyanidin A2, an anti-diabetic condensed tannin extracted from Wendlandia glabrata , reduces elevated G-6-Pase and mRNA levels in diabetic mice and increases glucose uptake in CC1 hepatocytes and C1C12 myoblast cells
Sheikh, Y., Chanu, M. B., Mondal, G., Manna, P., Chattoraj, A., Deka, D. C., Talukdar, N. C., & Borah, J. C. (2019) · RSC Advances · doi:10.1039/c9ra02397f · Cited by 26 · see citing works
A modest glucokinase overexpression in the liver promotes fed expression levels of glycolytic and lipogenic enzyme genes in the fasted state without altering SREBP-1c expression
Scott, D. K., Collier, J. J., Doan, T.-T. T., et al. (2003) · Molecular and Cellular Biochemistry · doi:10.1023/a:1027306122336 · Cited by 25 · see citing works
“In agreement with previous studies, glucose-6-phosphatase mRNA levels decreased from the fasted to the fed state [31].”
Result
Rapid reversal of the effects of the portal signal under hyperinsulinemic conditions in the conscious dog
Hsieh, P., Moore, M. C., Neal, D. W., Emshwiller, M., & Cherrington, A. D. (1999) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1999.276.5.e930 · Cited by 25 · see citing works
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Self-citation
Glucose-6-phosphatase Catalytic Enzyme Inhibitors: Synthesis and In Vitro Evaluation of Novel 4,5,6,7-Tetrahydrothieno[3,2-c]- and -[2,3-c]pyridines
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Background
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Authors: Argaud, D., Zhang, Q., Pan, W., Maitra, S., Pilkis, S. J., & Lange, A. J.
Affiliations: University of Minnesota (US)
ORCID: Zhang, Qing
Venue: Diabetes
Publisher: American Diabetes Association
Published: 1996-11-01
Volume: 45
Issue: 11
Pages: 1563-1571
ISSN: 0012-1797 (ISSN-L)
1939-327X
DOI: 10.2337/diab.45.11.1563
OpenAlex: W2057486586
Cited by: 168
References: 0
Citations by year: 2026: 1 · 2023: 3 · 2022: 5 · 2021: 1 · 2020: 5 · 2019: 2 · 2018: 5 · 2017: 4 · 2016: 5 · 2015: 3 · 2014: 4 · 2013: 8 · 2012: 6
FWCI: 8.40
Type: journal article
Language: en
Open access: closed
Locations: Diabetes (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5r01dk046562-05)
National Institute of Diabetes and Digestive and Kidney Diseases (DK-46562)
Topics: Health Sciences › Medicine › Rheumatology › Glycogen Storage Diseases and Myoclonus
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Biochemical and Molecular Research
Keywords: glucose-6-phosphatase, gene expression regulation, liver, insulin, glucocorticoids, cAMP response element, promoter, 5'-flanking region, exon-intron structure, 3' untranslated region, gene duplication, TATA box, hepatic gluconeogenesis, diabetic rats, Fao hepatoma cells
MeSH terms: Cyclic AMP, Amino Acid Sequence, Animals, Base Sequence, Cell Nucleus, Diabetes Mellitus, Experimental, Dietary Carbohydrates, Eating, Exons, Fasting, Glucocorticoids, Glucose-6-Phosphatase, Humans, Insulin, Introns, Liver, Liver Neoplasms, Experimental, Male, Molecular Sequence Data, Nutritional Status, Thionucleotides, Transcription, Genetic, Tumor Cells, Cultured, Genomic Library, Gene Expression Regulation, Enzymologic, Rats, Sprague-Dawley, Dinucleotide Repeats, Mice, Rats

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Regulation of Rat Liver Glucose-6-Phosphatase Gene Expression in Different Nutritional and Hormonal States: Gene Structure and 5′-Flanking Sequence

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