Beta-adrenergic blockade increases GLUT4 and improves glycemic control in insulin-treated diabetic Wistar rats

Autonomic Neuroscience: Basic and Clinical

Volumn 193, Issue , 2015, Pages 108-116

  Alves Wagner, Ana Barbara ^a   Mori, Rosana Cristina ^a   Sabino Silva, Robinson ^b   Fatima, Luciana Alves ^a   da Silva Alves, Adilson ^a   Britto, Luiz Roberto ^a   D'Agord Schaan, Beatriz ^c   Machado, Ubiratan Fabres ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF UBERLÂNDIA   (Brazil)

^c HOSPITAL DE CLÍNICAS DE PORTO ALEGRE   (Brazil)

Author keywords

EDL; PKA; SHR; Soleus; TNF

Indexed keywords

ALLOXAN; BETA 2 ADRENERGIC RECEPTOR; CYCLIC AMP DEPENDENT PROTEIN KINASE; GLUCOSE; GLUCOSE TRANSPORTER 4; MESSENGER RNA; PROPRANOLOL; PROTEIN; RECOMBINANT HUMAN INSULIN; TUMOR NECROSIS FACTOR; ANTIDIABETIC AGENT; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; GLUCOSE BLOOD LEVEL; INSULIN; SLC2A4 PROTEIN, RAT;

ADRENERGIC SYSTEM; ALLOXAN-INDUCED DIABETES MELLITUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BETA ADRENERGIC RECEPTOR BLOCKING; CONTROLLED STUDY; DRUG EFFICACY; EXTENSOR DIGITORUM LONGUS MUSCLE; GLUCOSE HOMEOSTASIS; GLYCEMIC CONTROL; INSULIN TREATMENT; MALE; MONOTHERAPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; SOLEUS MUSCLE; SPONTANEOUSLY HYPERTENSIVE RAT; STRAIN DIFFERENCE; WISTAR RAT; ANIMAL; DIABETES MELLITUS, EXPERIMENTAL; DRUG EFFECTS; GLUCOSE BLOOD LEVEL; HOMEOSTASIS; METABOLISM; PHYSIOLOGY; SKELETAL MUSCLE; TREATMENT OUTCOME;

ADRENERGIC BETA-ANTAGONISTS; ANIMALS; BLOOD GLUCOSE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DIABETES MELLITUS, EXPERIMENTAL; GLUCOSE TRANSPORTER TYPE 4; HOMEOSTASIS; HYPOGLYCEMIC AGENTS; INSULIN; MALE; MUSCLE, SKELETAL; PROPRANOLOL; RATS, INBRED SHR; RATS, WISTAR; RECEPTORS, ADRENERGIC, BETA-2; RNA, MESSENGER; TREATMENT OUTCOME;

EID: 84947437819     PISSN: 15660702     EISSN: 18727484     Source Type: Journal    
DOI: 10.1016/j.autneu.2015.10.003     Document Type: Article

References (64)

1. Alves-Wagner A.B., De Freitas H.S., De Souza P.B., Seraphim P.M., Mori R.C., Machado U.F. Beta-adrenergic activity preserves GLUT4 protein in glycolytic fibers in fasting. Muscle Nerve 2009, 40:847-854.
2. Alves-Wagner A.B., Sabino-Silva R., Campello R.S., Mori R.C., Machado U.F. Decreased diabetes-induced glycemic impairment in WKY and SHR involves enhanced skeletal muscle Slc2a4/GLUT4 expression. Diabetol. Metab. Syndr. 2014, 6:97.
3. Bangalore S., Parkar S., Grossman E., Messerli F.H. A meta-analysis of 94, 492 patients with hypertension treated with beta blockers to determine the risk of new-onset diabetes mellitus. Am. J. Cardiol. 2007, 100:1254-1262.
4. Barnett A.H., Leslie D., Watkins P.J. Can insulin-treated diabetics be given beta-adrenergic blocking drugs?. Br. Med. J. 1980, 280:976-978.
5. Berne C., Fagius J., Pollare T., Hjemdahl P. The sympathetic response to euglycaemic hyperinsulinaemia. Evidence from microelectrode nerve recordings in healthy subjects. Diabetologia 1992, 35:873-879.
6. Cabassi A., Vinci S., Cantoni A.M., Quartieri F., Moschini L., Cavazzini S., Cavatorta A., Borghetti A. Sympathetic activation in adipose tissue and skeletal muscle of hypertensive rats. Hypertension 2002, 39:656-661.
7. Cabassi A., Vinci S., Quartieri F., Moschini L., Borghetti A. Norepinephrine reuptake is impaired in skeletal muscle of hypertensive rats in vivo. Hypertension 2001, 37:698-702.
8. Chellingsworth M.C., Kendall M.J., Wright A.D., Singh B.M., Pasi J. The effects of verapamil, diltiazem, nifedipine and propranolol on metabolic control in hypertensives with non-insulin dependent diabetes mellitus. J. Hum. Hypertens. 1989, 3:35-39.
9. Chen W.Q., Cai H., Zhang C., Ji X.P., Zhang Y. Is overall blockade superior to selective blockade of adrenergic receptor subtypes in suppressing left ventricular remodeling in spontaneously hypertensive rats?. Hypertens. Res. 2010, 33:1071-1081.
10. Chiasson J.L., Shikama H., Chu D.T., Exton J.H. Inhibitory effect of epinephrine on insulin-stimulated glucose uptake by rat skeletal muscle. J. Clin. Invest. 1981, 68:706-713.
11. Corrêa-Giannella M.L., Machado U.F. SLC2A4gene: a promising target for pharmacogenomics of insulin resistance. Pharmacogenomics 2013, 14:847-850.
12. Cryer P.E. Banting lecture. Hypoglycemia: the limiting factor in the management of IDDM. Diabetes 1994, 43:1378-1389.
13. Dangel V., Giray J., Ratge D., Wisser H. Regulation of beta-adrenoceptor density and mRNA levels in the rat heart cell-line H9c2. Biochem. J. 1996, 317(Pt 3):925-931.
14. DeFronzo R.A. Pathogenesis of type 2 diabetes mellitus. Med Clin North Am 2004, 88(787-835):ix.
15. Dimitrijević M., Pilipović I., Stanojević S., Mitić K., Radojević K., Pesić V., Leposavić G. Chronic propranolol treatment affects expression of adrenoceptors on peritoneal macrophages and their ability to produce hydrogen peroxide and nitric oxide. J. Neuroimmunol. 2009, 211:56-65.
16. Dong Z., Chai W., Wang W., Zhao L., Fu Z., Cao W., Liu Z. Protein kinase A mediates glucagon-like peptide 1-induced nitric oxide production and muscle microvascular recruitment. Am J Physiol Endocrinol Metab 2013, 304:E222-E228.
17. Dornhorst A., Powell S.H., Pensky J. Aggravation by propranolol of hyperglycaemic effect of hydrochlorothiazide in type II diabetics without alteration of insulin secretion. Lancet 1985, 1:123-126.
18. Ernberg M., Lundeberg T., Kopp S. Effect of propranolol and granisetron on experimentally induced pain and allodynia/hyperalgesia by intramuscular injection of serotonin into the human masseter muscle. Pain 2000, 84:339-346.
19. Franzellitti S., Buratti S., Valbonesi P., Capuzzo A., Fabbri E. The β-blocker propranolol affects cAMP-dependent signaling and induces the stress response in Mediterranean mussels, Mytilus galloprovincialis. Aquat. Toxicol. 2011, 101:299-308.
20. Freitas H.S., Schaan B.D., David-Silva A., Sabino-Silva R., Okamoto M.M., Alves-Wagner A.B., Mori R.C., Machado U.F. SLC2A2 gene expression in kidney of diabetic rats is regulated by HNF-1 alpha and HNF-3 beta. Mol. Cell. Endocrinol. 2009, 305:63-70.
21. Freitas H.S., Schaan B.D., Seraphim P.M., Nunes M.T., Machado U.F. Acute and short-term insulin-induced molecular adaptations of GLUT2 gene expression in the renal cortex of diabetic rats. Mol. Cell. Endocrinol. 2005, 237:49-57.
22. Fu Q., Xu B., Liu Y., Parikh D., Li J., Li Y., Zhang Y., Riehle C., Zhu Y., Rawlings T., Shi Q., Clark R.B., Chen X., Abel E.D., Xiang Y.K. Insulin inhibits cardiac contractility by inducing a Gi-biased β2-adrenergic signaling in hearts. Diabetes 2014, 63:2676-2689.
23. Furuya D.T., Neri E.A., Poletto A.C., Anhê G.F., Freitas H.S., Campello R.S., Rebouças N.A., Machado U.F. Identification of nuclear factor-κB sites in the Slc2a4 gene promoter. Mol. Cell. Endocrinol. 2013, 370:87-95.
24. Gerich J.E. Lilly lecture 1988. Glucose counterregulation and its impact on diabetes mellitus. Diabetes 1988, 37:1608-1617.
25. Gupta A.K., Dahlof B., Dobson J., Sever P.S., Wedel H., Poulter N.R., Investigators A.-S.C.O.T. Determinants of new-onset diabetes among 19,257 hypertensive patients randomized in the Anglo-Scandinavian Cardiac Outcomes Trial-Blood Pressure Lowering Arm and the relative influence of antihypertensive medication. Diabetes Care 2008, 31:982-988.
26. Haenni A., Lithell H. Treatment with a beta-blocker with beta 2-agonism improves glucose and lipid metabolism in essential hypertension. Metabolism 1994, 43:455-461.
27. Horinouchi T., Morishima S., Tanaka T., Suzuki F., Tanaka Y., Koike K., Miwa S., Muramatsu I. Different changes of plasma membrane beta-adrenoceptors in rat heart after chronic administration of propranolol, atenolol and bevantolol. Life Sci. 2007, 81:399-404.
28. Hoyer D., Hannon J.P., Martin G.R. Molecular, pharmacological and functional diversity of 5-HT receptors. Pharmacol Biochem Behav 2002, 71:533-554.
29. Hunt D.G., Ding Z., Ivy J.L. Clenbuterol prevents epinephrine from antagonizing insulin-stimulated muscle glucose uptake. J. Appl. Physiol. 2002, 1985(92):1285-1292.
30. Hupfeld C.J., Dalle S., Olefsky J.M. Beta-arrestin 1 down-regulation after insulin treatment is associated with supersensitization of beta 2 adrenergic receptor galpha s signaling in 3T3-L1 adipocytes. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:161-166.
31. Katayama S., Inaba M., Maruno Y., Morita T., Awata T., Oka Y. Glucose intolerance in spontaneously hypertensive and Wistar-Kyoto rats: enhanced gene expression and synthesis of skeletal muscle glucose transporter 4. Hypertens. Res. 1997, 20:279-286.
32. Kim Y.S., Sainz R.D., Molenaar P., Summers R.J. Characterization of beta 1- and beta 2-adrenoceptors in rat skeletal muscles. Biochem. Pharmacol. 1991, 42:1783-1789.
33. Kimura, H., Miyamoto, A., Ohshika, H. 1993. Down-regulation of beta-adrenoceptors and loss of Gs alpha subunit levels in ventricular myocardium of rats treated with isoproterenol. Life Sci. 53, PL171-176.
34. Kleinbaum J., Shamoon H. Effect of propranolol on delayed glucose recovery after insulin-induced hypoglycemia in normal and diabetic subjects. Diabetes Care 1984, 7:155-162.
35. Lager I. Adrenergic blockade and hypoglycaemia. Acta Med Scand Suppl 1983, 672:63-67.
36. Lang C.H., Nystrom G., Frost R.A. Beta-adrenergic blockade exacerbates sepsis-induced changes in tumor necrosis factor alpha and interleukin-6 in skeletal muscle and is associated with impaired translation initiation. J Trauma 2008, 64:477-486.
37. Lira E.C., Graca F.A., Goncalves D.A., Zanon N.M., Baviera A.M., Strindberg L., Lönnroth P., Migliorini R.H., Kettelhut I.C., Navegantes L.C. Cyclic adenosine monophosphate-phosphodiesterase inhibitors reduce skeletal muscle protein catabolism in septic rats. Shock 2007, 27:687-694.
38. Lynch G.S., Ryall J.G. Role of beta-adrenoceptor signaling in skeletal muscle: implications for muscle wasting and disease. Physiol. Rev. 2008, 88:729-767.
39. Matsui S., Yamane T., Kobayashi-Hattori K., Oishi Y. Calcitonin gene-related peptide regulates mitogen-activated protein kinase pathway to decrease transforming growth factor β1-induced hepatic plasminogen activator inhibitor-1 mRNA expression in HepG2 cells. Biosci. Biotechnol. Biochem. 2014, 78:787-790.
40. Mora S., Pessin J.E. The MEF2A isoform is required for striated muscle-specific expression of the insulin-responsive GLUT4 glucose transporter. J Biol Chem 2000, 275:16323-16328.
41. Moraes P.A., Yonamine C.Y., Pinto Junior D.C., Esteves J.V., Machado U.F., Mori R.C. Insulin acutely triggers transcription of Slc2a4 gene: participation of the AT-rich, E-box and NFKB-binding sites. Life Sci. 2014, 114:36-44.
42. Morisco C., Lembo G., Trimarco B. Insulin resistance and cardiovascular risk: new insights from molecular and cellular biology. Trends Cardiovasc Med 2006, 16:183-188.
43. Nonogaki K. New insights into sympathetic regulation of glucose and fat metabolism. Diabetologia 2000, 43:533-549.
44. Okamoto M.M., Anhê G.F., Sabino-Silva R., Marques M.F., Freitas H.S., Mori R.C., Melo K.F., Machado U.F. Intensive insulin treatment induces insulin resistance in diabetic rats by impairing glucose metabolism-related mechanisms in muscle and liver. J Endocrinol 2011, 211:55-64.
45. Oliver E., Martí D., Montó F., Flacco N., Moreno L., Barettino D., Ivorra M.D., D'Ocon P. The impact of alpha1-adrenoceptors up-regulation accompanied by the impairment of beta-adrenergic vasodilatation in hypertension. J Pharmacol Exp Ther 2009, 328:982-990.
46. Rashid S., Shi Z.Q., Niwa M., Mathoo J.M., Vandelangeryt M.L., Bilinski D., Lewis G.F., Vranic M. Beta-blockade, but not normoglycemia or hyperinsulinemia, markedly diminishes stress-induced hyperglycemia in diabetic dogs. Diabetes 2000, 49:253-262.
47. Reaven G.M. The metabolic syndrome: is this diagnosis necessary?. Am J Clin Nutr 2006, 83:1237-1247.
48. Roy D., Jóhannsson E., Bonen A., Marette A. Electrical stimulation induces fiber type-specific translocation of GLUT-4 to T tubules in skeletal muscle. Am J Physiol 1997, 273:E688-E694.
49. Ryan J.R., LaCorte W., Jain A., McMahon F.G. Hypertension in hypoglycemic diabetics treated with beta-adrenergic antagonists. Hypertension 1985, 7:443-446.
50. Sabino-Silva R., Alves-Wagner A.B., Burgi K., Okamoto M.M., Alves A.S., Lima G.A., Freitas H.S., Antunes V.R., Machado U.F. SGLT1 protein expression in plasma membrane of acinar cells correlates with the sympathetic outflow to salivary glands in diabetic and hypertensive rats. Am J Physiol Endocrinol Metab 2010, 299:E1028-E1037.
51. Saghizadeh M., Ong J.M., Garvey W.T., Henry R.R., Kern P.A. The expression of TNF alpha by human muscle. Relationship to insulin resistance. J Clin Invest 1996, 97:1111-1116.
52. Sato M., Dehvari N., Oberg A.I., Dallner O.S., Sandström A.L., Olsen J.M., Csikasz R.I., Summers R.J., Hutchinson D.S., Bengtsson T. Improving type 2 diabetes through a distinct adrenergic signaling pathway involving mTORC2 that mediates glucose uptake in skeletal muscle. Diabetes 2014, 63:4115-4129.
53. Sawicki P.T., Siebenhofer A. Betablocker treatment in diabetes mellitus. J. Intern. Med. 2001, 250:11-17.
54. Seraphim P.M., Nunes M.T., Giannocco G., Machado U.F. Age related obesity-induced shortening of GLUT4 mRNA poly(a) tail length in rat gastrocnemius skeletal muscle. Mol. Cell. Endocrinol. 2007, 276:80-87.
55. Shamoon H., Sherwin R. Beta-adrenergic blockade is more effective in suppressing adrenaline-induced glucose production in Type 1 (insulin-dependent) diabetes. Diabetologia 1984, 26:183-189.
56. Sivitz W.I., DeSautel S.L., Lee E.C., Pessin J.E. Time-dependent regulation of rat adipose tissue glucose transporter (GLUT4) mRNA and protein by insulin in streptozocin-diabetic and normal rats. Metabolism 1992, 41:1267-1272.
57. Spallone V., Maiello M.R., Cicconetti E., Menzinger G. Autonomic neuropathy and cardiovascular risk factors in insulin-dependent and non insulin-dependent diabetes. Diabetes Res. Clin. Pract. 1997, 34:169-179.
58. Tentolouris N., Argyrakopoulou G., Katsilambros N. Perturbed autonomic nervous system function in metabolic syndrome. Neruomol. Med. 2008, 10:169-178.
59. Torgan C.E., Brozinick J.T., Banks E.A., Cortez M.Y., Wilcox R.E., Ivy J.L. Exercise training and clenbuterol reduce insulin resistance of obese Zucker rats. Am J Physiol 1993, 264:E373-E379.
60. Vestri S., Okamoto M.M., de Freitas H.S., Aparecida Dos Santos R., Nunes M.T., Morimatsu M., Heimann J.C., Machado U.F. Changes in sodium or glucose filtration rate modulate expression of glucose transporters in renal proximal tubular cells of rat. J Membr Biol 2001, 182:105-112.
61. Waal-Manning H.J. Metabolic effects of beta-adrenoreceptor blockers. Drugs 1976, 11(SUPPL 1):121-126.
62. Winslow J.T., Insel T.R. Serotonergic modulation of the rat pup ultrasonic isolation call: studies with 5HT1 and 5HT2 subtype-selective agonists and antagonists. Psychopharmacology 1991, 105:513-520.
63. Wright A.D., Barber S.G., Kendall M.J., Poole P.H. Beta-adrenoceptor-blocking drugs and blood sugar control in diabetes mellitus. Br. Med. J. 1979, 1:159-161.
64. Ye J.M., Colquhoun E.Q. Altered muscle metabolism associated with vasoconstriction in spontaneously hypertensive rats. Am J Physiol 1998, 275:E1007-E1015.