Nitric oxide increases cyclic GMP levels, AMP-activated protein kinase (AMPK)α1-specific activity and glucose transport in human skeletal muscle

Diabetologia

Volumn 53, Issue 6, 2010, Pages 1142-1150

  Deshmukh, A S ^a   Long, Y C ^a   De Castro Barbosa, T ^a   Karlsson, H K R ^a   Glund, S ^a   Zavadoski, W J ^b   Gibbs, E M ^b,c   Koistinen, H A ^d,e   Wallberg Henriksson, H ^a   Zierath, J R ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b PFIZER INC   (United States)

^c Gibbs Biomedical Consultants   (United States)

^d HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^e MINERVA FOUNDATION INSTITUTE FOR MEDICAL RESEARCH   (Finland)

Author keywords

Contraction; Exercise; GLUT4; Spermine NONOate

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; CYCLIC GMP; GLUCOSE; GLYCOGEN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ALPHA1; INSULIN; N (2 AMINOETHYL) N (2 HYDROXY 2 NITROSOHYDRAZINO) 1,2 ETHYLENEDIAMINE; NITRIC OXIDE DONOR; PROTEIN SERINE THREONINE KINASE; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVITY; GLUCOSE TRANSPORT; GLYCOGEN SYNTHESIS; HUMAN; HUMAN TISSUE; MALE; MUSCLE BIOPSY; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; VASTUS LATERALIS MUSCLE;

AMP-ACTIVATED PROTEIN KINASES; ANALYSIS OF VARIANCE; BIOLOGICAL TRANSPORT; BLOTTING, WESTERN; CELLS, CULTURED; CYCLIC GMP; GLUCOSE; HUMANS; INSULIN; MALE; MIDDLE AGED; MUSCLE, SKELETAL; NITRIC OXIDE; NITRIC OXIDE DONORS; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SPERMINE;

EID: 77952092350     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-010-1716-x     Document Type: Article

References (41)

1. GK McConell BA Kingwell 2006 Does nitric oxide regulate skeletal muscle glucose uptake during exercise? Exerc Sport Sci Rev 34 36 41 10.1097/00003677-200601000-00008 16394813 (Pubitemid 44378460)
2. TW Balon JL Nadler 1994 Nitric oxide release is present from incubated skeletal muscle preparations J Appl Physiol 77 2519 2521 1:STN:280: DyaK2M3gsVaisg%3D%3D 7896585
3. CK Roberts RJ Barnard SH Scheck TW Balon 1997 Exercise-stimulated glucose transport in skeletal muscle is nitric oxide dependent Am J Physiol 273 E220 E225 1:CAS:528:DyaK2sXlt1Srtrw%3D 9252500
4. SJ Bradley BA Kingwell GK McConell 1999 Nitric oxide synthase inhibition reduces leg glucose uptake but not blood flow during dynamic exercise in humans Diabetes 48 1815 1821 10.2337/diabetes.48.9.1815 1:CAS:528:DyaK1MXmtVaitb4%3D 10480613 (Pubitemid 29415202)
5. S Moncada A Higgs 1993 The l-arginine-nitric oxide pathway N Engl J Med 329 2002 2012 10.1056/NEJM199312303292706 1:CAS:528:DyaK2cXhsF2ntrw%3D 7504210 (Pubitemid 24015045)
6. M Nakane HH Schmidt JS Pollock U Förstermann F Murad 1993 Cloned human brain nitric oxide synthase is highly expressed in skeletal muscle FEBS Lett 316 175 180 10.1016/0014-5793(93)81210-Q 1:CAS:528:DyaK3sXkvFWru7s%3D 7678401 (Pubitemid 23025053)
7. WJ Durham CW Yeckel SL Miller DC Gore RR Wolfe 2003 Exogenous nitric oxide increases basal leg glucose uptake in humans Metabolism 52 662 665 10.1016/S0026-0495(03)00062-3 1:CAS:528:DC%2BD3sXkt1Oqt7s%3D 12800088 (Pubitemid 36896298)
8. DC Henstridge BA Kingwell MF Formosa, et al. 2005 Effects of the nitric oxide donor, sodium nitroprusside, on resting leg glucose uptake in patients with type 2 diabetes Diabetologia 48 2602 2608 10.1007/s00125-005-0018-1 1:CAS:528:DC%2BD2MXht1Omu7%2FN 16273348 (Pubitemid 41738228)
9. TW Balon JL Nadler 1997 Evidence that nitric oxide increases glucose transport in skeletal muscle J Appl Physiol 82 359 363 1:CAS:528: DyaK2sXhsVeqt78%3D 9029239 (Pubitemid 27052084)
10. ME Young GK Radda B Leighton 1997 Nitric oxide stimulates glucose transport and metabolism in rat skeletal muscle in vitro Biochem J 322 223 228 1:CAS:528:DyaK2sXhslKru78%3D 9078265 (Pubitemid 27095544)
11. GJ Etgen Jr DA Fryburg EM Gibbs 1997 Nitric oxide stimulates skeletal muscle glucose transport through a calcium/contraction- and phosphatidylinositol-3-kinase-independent pathway Diabetes 46 1915 1919 10.2337/diabetes.46.11.1915 1:CAS:528:DyaK2sXntVKhsr0%3D 9356048 (Pubitemid 27456433)
12. EH Ohlstein KS Wood LJ Ignarro 1982 Purification and properties of heme-deficient hepatic soluble guanylate cyclase: effects of heme and other factors on enzyme activation by NO, NO-heme, and protoporphyrin IX Arch Biochem Biophys 218 187 198 10.1016/0003-9861(82)90335-6 1:CAS:528:DyaL38XlslOltrg%3D 6128958
13. N Jessen LJ Goodyear 2005 Contraction signaling to glucose transport in skeletal muscle J Appl Physiol 99 330 337 10.1152/japplphysiol.00175.2005 1:CAS:528:DC%2BD2MXmvFWkur0%3D 16036906 (Pubitemid 40934499)
14. YC Long JR Zierath 2006 AMP-activated protein kinase signaling in metabolic regulation J Clin Invest 116 1776 1783 10.1172/JCI29044 1:CAS:528:DC%2BD28XmvV2ltLw%3D 16823475 (Pubitemid 44033297)
15. Y Higaki MF Hirshman N Fujii, et al. 2001 Nitric oxide increases glucose uptake through a mechanism that is distinct from the insulin and contraction pathways in rat skeletal muscle Diabetes 50 241 247 10.2337/diabetes.50.2.241 1:CAS:528:DC%2BD3MXhtVOhu7c%3D 11272132 (Pubitemid 32127278)
16. VA Lira QA Soltow JH Long, et al. 2007 Nitric oxide increases GLUT4 expression and regulates AMPK signaling in skeletal muscle Am J Physiol Endocrinol Metab 293 E1062 E1068 10.1152/ajpendo.00045.2007 1:CAS:528: DC%2BD2sXht1WltbbO 17666490 (Pubitemid 47535838)
17. LG Fryer E Hajduch F Rencurel, et al. 2000 Activation of glucose transport by AMP-activated protein kinase via stimulation of nitric oxide synthase Diabetes 49 1978 1785 10.2337/diabetes.49.12.1978 1:CAS:528: DC%2BD3cXos1ejsr0%3D 11117997
18. ZP Chen KI Mitchelhill BJ Michell, et al. 1999 AMP-activated protein kinase phosphorylation of endothelial NO synthase FEBS Lett 443 285 289 10.1016/S0014-5793(98)01705-0 1:CAS:528:DyaK1MXht1Sgt7c%3D 10025949 (Pubitemid 29080812)
19. ZP Chen GK McConell BJ Michell, et al. 2000 AMPK signaling in contracting human skeletal muscle: acetyl-CoA carboxylase and NO synthase phosphorylation Am J Physiol Endocrinol Metab 279 E1202 E1206 1:CAS:528:DC%2BD3cXotFaqsbw%3D 11052978
20. JR Zierath 1995 In vitro studies of human skeletal muscle: hormonal and metabolic regulation of glucose transport Acta Physiol Scand Suppl 626 1 96 1:STN:280:DyaK28%2FovFWgtQ%3D%3D 8525841
21. JR Zierath D Galuska A Engstrom, et al. 1992 Human islet amyloid polypeptide at pharmacological levels inhibits insulin and phorbol ester-stimulated glucose transport in in vitro incubated human muscle strips Diabetologia 35 26 31 10.1007/BF00400848 1:CAS:528:DyaK38XisVyiu7g%3D 1541378
22. L Al-Khalili AV Chibalin K Kannisto, et al. 2003 Insulin action in cultured human skeletal muscle cells during differentiation: assessment of cell surface GLUT4 and GLUT1 content Cell Mol Life Sci 60 991 998 1:CAS:528:DC%2BD3sXlt1aitLc%3D 12827286 (Pubitemid 36735127)
23. W Niu C Huang Z Nawaz, et al. 2003 Maturation of the regulation of GLUT4 activity by p38 MAPK during L6 cell myogenesis J Biol Chem 278 17953 17962 10.1074/jbc.M211136200 1:CAS:528:DC%2BD3sXjs1Kitbo%3D 12637564 (Pubitemid 36799402)
24. HA Koistinen D Galuska AV Chibalin, et al. 2003 5-amino-imidazole carboxamide riboside increases glucose transport and cell-surface GLUT4 content in skeletal muscle from subjects with type 2 diabetes Diabetes 52 1066 1072 10.2337/diabetes.52.5.1066 1:CAS:528:DC%2BD3sXjsFGhtL0%3D 12716734 (Pubitemid 36523338)
25. BR Barnes JW Ryder TL Steiler, et al. 2002 Isoform-specific regulation of 5′ AMP-activated protein kinase in skeletal muscle from obese Zucker (fa/fa) rats in response to contraction Diabetes 51 2703 2708 10.2337/diabetes.51.9.2703 1:CAS:528:DC%2BD38Xmslertbc%3D 12196462
26. A Mulsch R Busse S Liebau, et al. 1988 LY 83583 interferes with the release of endothelium-derived relaxing factor and inhibits soluble guanylate cyclase J Pharmacol Exp Ther 247 1 283 288 1:STN:280:DyaL1M%2FhtFCluw%3D%3D 2902213
27. MA Rogers C Yamamoto DS King, et al. 1988 Improvement in glucose tolerance after 1 wk of exercise in patients with mild NIDDM Diabetes Care 11 613 618 10.2337/diacare.11.8.613 1:STN:280:DyaL1M7itVCquw%3D%3D 3065001
28. JP Kirwan TPJ Solomon DM Wojta MA Staten JO Holloszy 2009 Effects of 7 days of exercise training on insulin sensitivity and responsiveness in type 2 diabetes mellitus Am J Physiol Endocrinol Metab 297 E151 E156 10.1152/ajpendo.00210.2009 1:CAS:528:DC%2BD1MXovVKjt7k%3D 19383872
29. A Kirk P de Feo 2007 Strategies to enhance compliance to physical activity for patients with insulin resistance Appl Physiol Nutr Metab 32 549 556 10.1139/H07-023 17510696
30. DE Moller 2001 New drug targets for type 2 diabetes and the metabolic syndrome Nature 414 821 827 10.1038/414821a 1:CAS:528:DC%2BD38Xhtlyltw%3D%3D 11742415 (Pubitemid 34000786)
31. BA Kingwell M Formosa M Muhlmann, et al. 2002 Nitric oxide synthase inhibition reduces glucose uptake during exercise in individuals with type 2 diabetes more than in control subjects Diabetes 51 2572 2580 10.2337/diabetes.51.8.2572 1:CAS:528:DC%2BD38XlvFKhsrg%3D 12145173 (Pubitemid 34827409)
32. ME Young B Leighton 1998 Evidence for altered sensitivity of the nitric oxide/cGMP signalling cascade in insulin-resistant skeletal muscle Biochem J 329 73 79 1:CAS:528:DyaK1cXltFeiuw%3D%3D 9405277 (Pubitemid 28022292)
33. JF Wojtaszewski JB Birk C Frosig, et al. 2005 5′AMP activated protein kinase expression in human skeletal muscle: effects of strength training and type 2 diabetes J Physiol 564 563 573 10.1113/jphysiol.2005.082669 1:CAS:528:DC%2BD2MXjslGltr0%3D 15718261 (Pubitemid 40585054)
34. JF Wojtaszewski P Nielsen BF Hansen, et al. 2000 Isoform-specific and exercise intensity-dependent activation of 5′-AMP-activated protein kinase in human skeletal muscle J Physiol 528 221 226 10.1111/j.1469-7793.2000.t01-1- 00221.x 1:CAS:528:DC%2BD3cXnslWqt7c%3D 11018120
35. JT Treebak JB Birk AJ Rose, et al. 2007 AS160 phosphorylation is associated with activation of alpha2beta2gamma1- but not alpha2beta2gamma3-AMPK trimeric complex in skeletal muscle during exercise in humans Am J Physiol Endocrinol Metab 292 E715 E722 10.1152/ajpendo.00380.2006 1:CAS:528: DC%2BD2sXjsFeqtr8%3D 17077344 (Pubitemid 46411048)
36. 2, in mouse skeletal muscle PLoS ONE 3 e2102 10.1371/journal.pone.0002102 18461163 (Pubitemid 352025096)
37. VA Morrow F Foufelle JM Connell, et al. 2003 Direct activation of AMP-activated protein kinase stimulates nitric-oxide synthesis in human aortic endothelial cells J Biol Chem 278 31629 31639 10.1074/jbc.M212831200 1:CAS:528:DC%2BD3sXmsVOnt7o%3D 12791703 (Pubitemid 37048341)
38. TJ Stephens BJ Canny RJ Snow, et al. 2004 5′-Aminoimidazole-4- carboxyamide-ribonucleoside-activated glucose transport is not prevented by nitric oxide synthase inhibition in rat isolated skeletal muscle Clin Exp Pharmacol Physiol 31 419 423 10.1111/j.1440-1681.2004.04014.x 1:CAS:528:DC%2BD2cXms1eju7c%3D 15236627 (Pubitemid 39044120)
39. WG Roach JA Chavez CP Miinea, et al. 2007 Substrate specificity and effect on GLUT4 translocation of the Rab GTPase-activating protein Tbc1d1 Biochem J 403 353 358 10.1042/BJ20061798 1:CAS:528:DC%2BD2sXjsVWrtL8%3D 17274760 (Pubitemid 46596592)
40. H Sano S Kane E Sano, et al. 2003 Insulin-stimulated phosphorylation of a Rab GTPase-activating protein regulates GLUT4 translocation J Biol Chem 278 14599 14602 10.1074/jbc.C300063200 1:CAS:528:DC%2BD3sXjtVCmt7w%3D 12637568 (Pubitemid 36799780)
41. DC Henstridge BG Drew MF Formosa, et al. 2009 The effect of the nitric oxide donor sodium nitroprusside on glucose uptake in human primary skeletal muscle cells Nitric Oxide 21 126 131 10.1016/j.niox.2009.06.002 1:CAS:528:DC%2BD1MXps1WltbY%3D 19567271