Retinoids synergize with insulin to induce hepatic Gck expression.

Hepatic GK (glucokinase) plays a key role in maintaining glucose homoeostasis. Many stimuli regulate GK activity by controlling its gene transcription. We hypothesized that endogenous lipophilic molecules modulate hepatic Gck expression. Lipophilic molecules were extracted from rat livers, saponified and re-constituted as an LE (lipophilic extract). LE synergized with insulin to induce primary hepatocyte, but not beta-cell, Gck expression in an SREBP-1c (sterol-regulatory-element-binding protein-1c)-independent manner. The dramatic induction of Gck mRNA resulted in a significant increase in GK activity. Subsequently, the active molecules were identified as retinol and retinal by MS after the purification of the active LE fractions. Retinoids synergized with insulin to induce Gck expression by the activation of both RAR [RA (retinoic acid) receptor] and RXR (retinoid X receptor). Inhibition of RAR activation completely abolished the effect of retinal. The hepatic GK specific activity and Gck mRNA levels of Zucker lean rats fed with a VAD [VA (vitamin A)-deficient] diet were significantly lower than those of rats fed with VAS (VA-sufficient) diet. Additionally, the hepatic Gck mRNA expression of Sprague-Dawley rats fed with a VAD diet was lower than that of rats fed with VA-marginal, -adequate or -supplemented diets. The reduced expression of Gck mRNA was increased after an intraperitoneal dose of RA in VAD rats. Furthermore, an intravenous injection of RA rapidly raised hepatic Gck expression in rats fed with a VAS control diet. Understanding the underlying mechanism that mediates the synergy may be helpful for developing a treatment strategy for patients with diabetes.

[1]  Guoxun Chen Liver lipid molecules induce PEPCK-C gene transcription and attenuate insulin action. , 2007, Biochemical and biophysical research communications.

[2]  K. Palczewski,et al.  Delivery of retinoid-based therapies to target tissues. , 2007, Biochemistry.

[3]  F. Hansmannel,et al.  Insulin induction of glucokinase and fatty acid synthase in hepatocytes: analysis of the roles of sterol-regulatory-element-binding protein-1c and liver X receptor. , 2006, The Biochemical journal.

[4]  A. Ross,et al.  All-trans-retinoic acid distribution and metabolism in vitamin A-marginal rats. , 2006, American journal of physiology. Gastrointestinal and liver physiology.

[5]  U. Smith,et al.  Retinol-binding protein 4 and insulin resistance in lean, obese, and diabetic subjects. , 2006, The New England journal of medicine.

[6]  J. Girard,et al.  Insulin regulation of glucokinase gene expression: Evidence against a role for sterol regulatory element binding protein 1 in primary hepatocytes , 2006, FEBS letters.

[7]  P. B. Jensen,et al.  The Nkx6.1 homeodomain transcription factor suppresses glucagon expression and regulates glucose-stimulated insulin secretion in islet beta cells. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[8]  H. Towle,et al.  Direct Role of ChREBP·Mlx in Regulating Hepatic Glucose-responsive Genes* , 2005, Journal of Biological Chemistry.

[9]  I. Rioja,et al.  Gene expression profiles in the rat streptococcal cell wall-induced arthritis model identified using microarray analysis , 2004, Arthritis research & therapy.

[10]  J. Grippo,et al.  Allosteric Activators of Glucokinase: Potential Role in Diabetes Therapy , 2003, Science.

[11]  D. Mangelsdorf,et al.  Activation of liver X receptor improves glucose tolerance through coordinate regulation of glucose metabolism in liver and adipose tissue , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[12]  A. Ross,et al.  Cloning of rat cytochrome P450RAI (CYP26) cDNA and regulation of its gene expression by all-trans-retinoic acid in vivo. , 2002, Archives of biochemistry and biophysics.

[13]  R. Hammer,et al.  Diminished Hepatic Response to Fasting/Refeeding and Liver X Receptor Agonists in Mice with Selective Deficiency of Sterol Regulatory Element-binding Protein-1c* , 2002, The Journal of Biological Chemistry.

[14]  Patrick Cramer,et al.  Structural basis of transcription: α-Amanitin–RNA polymerase II cocrystal at 2.8 Å resolution , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[15]  F. Matschinsky,et al.  Effect of retinoic acid on glucokinase activity and gene expression in neonatal and adult cultured hepatocytes. , 2001, Life sciences.

[16]  C. Newgard,et al.  Selection of insulinoma cell lines with resistance to interleukin-1beta- and gamma-interferon-induced cytotoxicity. , 2000, Diabetes.

[17]  I. Shimomura,et al.  Insulin selectively increases SREBP-1c mRNA in the livers of rats with streptozotocin-induced diabetes. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[18]  C. Newgard,et al.  Glucokinase Overexpression Restores Glucose Utilization and Storage in Cultured Hepatocytes from Male Zucker Diabetic Fatty Rats* , 1999, The Journal of Biological Chemistry.

[19]  M. Foretz,et al.  Sterol regulatory element binding protein-1c is a major mediator of insulin action on the hepatic expression of glucokinase and lipogenesis-related genes. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[20]  J. L. Napoli Interactions of retinoid binding proteins and enzymes in retinoid metabolism. , 1999, Biochimica et biophysica acta.

[21]  M. German,et al.  Effect of retinoic acid on glucokinase activity and gene expression and on insulin secretion in primary cultures of pancreatic islets. , 1999, Endocrinology.

[22]  M. Magnuson,et al.  Dual Roles for Glucokinase in Glucose Homeostasis as Determined by Liver and Pancreatic β Cell-specific Gene Knock-outs Using Cre Recombinase* , 1999, The Journal of Biological Chemistry.

[23]  A. Cornish-Bowden,et al.  Evolution and regulatory role of the hexokinases. , 1998, Biochimica et biophysica acta.

[24]  J. Girard,et al.  Effects of triiodothyronine and retinoic acid on glucokinase gene expression in neonatal rat hepatocytes , 1997, Molecular and Cellular Endocrinology.

[25]  A. Grupe,et al.  Transgenic knockouts reveal a critical requirement for pancreatic β cell glucokinase in maintaining glucose homeostasis , 1995, Cell.

[26]  G. Perret,et al.  Time- and dose-dependent kinetics of all-trans-retinoic acid in rats after oral or intravenous administration(s). , 1995, Drug metabolism and disposition: the biological fate of chemicals.

[27]  P. Lemotte,et al.  Different agonist- and antagonist-induced conformational changes in retinoic acid receptors analyzed by protease mapping , 1994, Molecular and Cellular Biology.

[28]  J. Beckmann,et al.  Familial hyperglycemia due to mutations in glucokinase. Definition of a subtype of diabetes mellitus. , 1993, The New England journal of medicine.

[29]  R. Blomhoff,et al.  Transport and storage of vitamin A , 1990, Science.

[30]  J. L. Napoli,et al.  Microsomes convert retinol and retinal into retinoic acid and interfere in the conversions catalyzed by cytosol. , 1990, Biochimica et biophysica acta.

[31]  T. Nouspikel,et al.  Transcriptional induction of glucokinase gene by insulin in cultured liver cells and its repression by the glucagon-cAMP system. , 1989, The Journal of biological chemistry.

[32]  C. Ucla,et al.  Differential expression and regulation of the glucokinase gene in liver and islets of Langerhans. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[33]  M. Magnuson,et al.  An alternate promoter in the glucokinase gene is active in the pancreatic beta cell. , 1989, The Journal of biological chemistry.

[34]  W. J. Arion,et al.  Factors underlying significant underestimations of glucokinase activity in crude liver extracts: physiological implications of higher cellular activity. , 1987, Archives of biochemistry and biophysics.

[35]  W. Sibrowski,et al.  Rapid action of insulin and cyclic AMP in the regulation of functional messenger RNA coding for glucokinase in rat liver. , 1984, The Journal of biological chemistry.

[36]  T. A. Venkitasubramanian,et al.  Early effects of feeding excess vitamin A: hepatic glycogen, blood lactic acid, plasma NEFA and glucose tolerance in rats. , 1968, Life sciences.

[37]  M. Lane,et al.  Studies on the function of vitamin A in metabolism. , 1957, The Journal of biological chemistry.

[38]  E. V. Mccollum,et al.  The Necessity of Certain Lipins in the Diet during Growth. , 1913 .

[39]  A. Ross,et al.  Chronic vitamin A status and acute repletion with retinyl palmitate are determinants of the distribution and catabolism of all-trans-retinoic acid in rats. , 2007, The Journal of nutrition.

[40]  M. Magnuson,et al.  The network of glucokinase-expressing cells in glucose homeostasis and the potential of glucokinase activators for diabetes therapy. , 2006, Diabetes.

[41]  A. Ross,et al.  Retinoid production and catabolism: role of diet in regulating retinol esterification and retinoic Acid oxidation. , 2003, The Journal of nutrition.

[42]  M. Sporn,et al.  The Retinoids : biology, chemistry, and medicine , 1994 .

[43]  L. Machlin Handbook of Vitamins , 1991 .

[44]  T. Moore Vitamin A and carotene: The vitamin A reserve of the adult human being in health and disease. , 1937, The Biochemical journal.

[45]  Guoxun Chen,et al.  Trace: Tennessee Research and Creative Exchange Nutrition Publications and Other Works Nutrition Central Role for Liver X Receptor in Insulin-mediated Activation of Srebp-1c Transcription and Stimulation of Fatty Acid Synthesis in Liver. Recommended Citation , 2022 .