Globular adiponectin controls insulin-mediated vasoreactivity in muscle through AMPKα2

Vascular Pharmacology

Volumn 78, Issue , 2016, Pages 24-35

  de Boer, Michiel P ^a,b   Meijer, Rick I ^a,b   Richter, Erik A ^c   van Nieuw Amerongen, Geerten P ^a,b   Sipkema, Pieter ^a,b   van Poelgeest, Erik M ^a,b   Aman, Jurjan ^a,b   Kokhuis, Tom J A ^d   Koolwijk, Pieter ^a,b   van Hinsbergh, Victor W M ^a,b   Smulders, Yvo M ^a,b   Serné, Erik H ^a,b   Eringa, Etto C ^a,b  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Animal models of human disease; Endothelium; Human; Insulin; Insulin resistance; Intracellular signaling; Microcirculation; Nitric oxide; Obesity

Indexed keywords

ADIPONECTIN; ENDOTHELIN 1; GLOBULAR ADIPONECTIN; GLUCOSE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ALPHA1; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ALPHA2; MITOGEN ACTIVATED PROTEIN KINASE 1; NEUTRAL INSULIN; UNCLASSIFIED DRUG; INSULIN; NITRIC OXIDE; PRKAA2 PROTEIN, HUMAN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY MASS; BODY WEIGHT; CAPILLARY DENSITY; CAPILLARY ENDOTHELIAL CELL; CONTINUOUS INFUSION; CONTROLLED STUDY; DIET RESTRICTION; FEMALE; FLUORESCENCE MICROSCOPY; GENE DELETION; GLUCOSE BLOOD LEVEL; GLUCOSE TRANSPORT; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; HYPERINSULINEMIA; IN VIVO STUDY; INSULIN INFUSION; INSULIN RESISTANCE; INSULIN SENSITIVITY; MALE; MOUSE; MUSCLE PERFUSION; NONHUMAN; NORMAL HUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; ANIMAL; BLOOD; C57BL MOUSE; COMPLICATION; ENDOTHELIUM CELL; METABOLISM; MIDDLE AGED; PHYSIOLOGY; VASODILATATION; WISTAR RAT;

ADIPONECTIN; ADULT; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ENDOTHELIAL CELLS; ENDOTHELIN-1; FEMALE; HUMANS; INSULIN; INSULIN RESISTANCE; MALE; MICE; MICE, INBRED C57BL; MIDDLE AGED; NITRIC OXIDE; OBESITY; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; VASODILATION;

EID: 84959152725     PISSN: 15371891     EISSN: 18793649     Source Type: Journal    
DOI: 10.1016/j.vph.2015.09.002     Document Type: Article

References (46)

1. Flegal K.M., Carroll M.D., Kit B.K., Ogden C.L. Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999-2010. JAMA 2012, 307:491-497.
2. Richter E.A., Ruderman N.B. AMPK and the biochemistry of exercise: implications for human health and disease. Biochem. J. 2009, 418:261-275.
3. Hardie D.G. AMPK: a target for drugs and natural products with effects on both diabetes and cancer. Diabetes 2013, 62:2164-2172.
4. Viollet B., Andreelli F., Jorgensen S.B., et al. The AMP-activated protein kinase alpha 2 catalytic subunit controls whole-body insulin sensitivity. J. Clin. Invest. 2003, 111:91-98.
5. Fisslthaler B., Fleming I. Activation and signaling by the AMP-activated protein kinase in endothelial cells. Circ. Res. 2009, 105:114-127.
6. Ouyang J., Parakhia R.A., Ochs R.S. Metformin activates AMP kinase through inhibition of AMP deaminase. J. Biol. Chem. 2011, 286:1-11.
7. Garcia-Prieto C.F., Pulido-Olmo H., Ruiz-Hurtado G., et al. Mild caloric restriction reduces blood pressure and activates endothelial AMPK-PI3K-Akt-eNOS pathway in obese Zucker rats. Vasc. Pharmacol. 2015, 65-66:3-12.
8. Zou M.H., Hou X.Y., Shi C.M., Nagata D., Walsh K., Cohen R.A. Modulation by peroxynitrite of Akt- and AMP-activated kinase-dependent Ser1179 phosphorylation of endothelial nitric oxide synthase. J. Biol. Chem. 2002, 277:32552-32557.
9. Frosig C., Jensen T.E., Jeppesen J., et al. AMPK and insulin action - responses to ageing and high fat diet. PLoS ONE 2013, 8.
10. Kubota T., Kubota N., Kumagai H., et al. Impaired insulin signaling in endothelial cells reduces insulin-induced glucose uptake by skeletal muscle. Cell Metab. 2011, 13:294-307.
11. Barrett E.J., Wang H., Upchurch C., Liu Z. Insulin regulates its own delivery to skeletal muscle by feed-forward actions on the vasculature. Am. J. Physiol. Endocrinol. Metab. 2011, 301(2):E252-63.
12. de Boer M.P., Meijer R.I., Wijnstok N.J., et al. Microvascular dysfunction: a potential mechanism in the pathogenesis of obesity-associated insulin resistance and hypertension. Microcirculation 2012, 19:5-18.
13. Clerk L.H., Vincent M.A., Jahn L.A., Liu Z., Lindner J.R., Barrett E.J. Obesity blunts insulin-mediated microvascular recruitment in human forearm muscle. Diabetes 2006, 55:1436-1442.
14. Eringa E.C., Stehouwer C.D., Merlijn T., Westerhof N., Sipkema P. Physiological concentrations of insulin induce endothelin-mediated vasoconstriction during inhibition of NOS or PI3-kinase in skeletal muscle arterioles. Cardiovasc. Res. 2002, 56:464-471.
15. Rattigan S., Clark M.G., Barrett E.J. Hemodynamic actions of insulin in rat skeletal muscle: evidence for capillary recruitment. Diabetes 1997, 46:1381-1388.
16. Sjoberg K.A., Rattigan S., Hiscock N., Richter E.A., Kiens B. A new method to study changes in microvascular blood volume in muscle and adipose tissue: real-time imaging in humans and rat. Am. J. Physiol. Heart Circ. Physiol. 2011, 301:H450-H458.
17. Eringa E.C., Stehouwer C.D.A., Nieuw Amerongen G.P., Ouwehand L., Westerhof N., Sipkema P. Vasoconstrictor effects of insulin in skeletal muscle arterioles are mediated by ERK1/2 activation in endothelium. Am. J. Physiol. Heart Circ. Physiol. 2004, 287:H2043-H2048.
18. Eringa E.C., Stehouwer C.D.A., Roos M.H., Westerhof N., Sipkema P. Selective resistance to vasoactive effects of insulin in muscle resistance arteries of obese Zucker (fa/fa) rats. Am. J. Physiol. Endocrinol. Metab. 2007, 293:E1134-E1139.
19. Zhao L., Chai W., Fu Z., et al. Globular adiponectin enhances muscle insulin action via microvascular recruitment and increased insulin delivery. Circ. Res. 2013, 112:1263-1271.
20. Hoeg L.D., Sjoberg K.A., Lundsgaard A.M., et al. Adiponectin concentration is associated with muscle insulin sensitivity, AMPK phosphorylation, and ceramide content in skeletal muscles of men but not women. J. Appl. Physiol. (1985) 2013, 114:592-601.
21. American Diabetes Association Diagnosis and Classification of Diabetes Mellitus Diabetes Care 2013, 36:S67-S74.
22. Meijer R.I., de Boer M.P., Groen M.R., et al. Insulin-induced microvascular recruitment in skin and muscle are related and both are associated with whole body glucose uptake. Microcirculation 2012, 19:494-500.
23. Bakker W., Sipkema P., Stehouwer C.D., et al. Protein kinase C theta activation induces insulin-mediated constriction of muscle resistance arteries. Diabetes 2008, 57:706-713.
24. Hattori Y., Suzuki M., Hattori S., Kasai K. Globular adiponectin upregulates nitric oxide production in vascular endothelial cells. Diabetologia 2003, 46:1543-1549.
25. Eringa E.C., Bradley E.A., Stehouwer C.D.A., et al. Activation of AMP-activated protein kinase by 5-aminoimidazole-4-carboxamide-1-beta-d-ribofuranoside in the muscle microcirculation increases nitric oxide synthesis and microvascular perfusion. Arterioscler. Thromb. Vasc. Biol. 2010, 30:1137-1142.
26. Aman J., van Bezu J., Damanafshan A., et al. Effective treatment of edema and endothelial barrier dysfunction with imatinib. Circulation 2012, 126:2728-2738.
27. Voshol P.J., Jong M.C., Dahlmans V.E.H., et al. In muscle-specific lipoprotein lipase-overexpressing mice, muscle triglyceride content is increased without inhibition of insulin-stimulated whole-body and muscle-specific glucose uptake. Diabetes 2001, 50:2585-2590.
28. Meijer R.I., Bakker W., Alta C.L., et al. Perivascular adipose tissue control of insulin-induced vasoreactivity in muscle is impaired in db/db mice. Diabetes 2013, 62:590-598.
29. Eringa E.C., Stehouwer C.D.A., Walburg K., et al. Physiological concentrations of insulin induce endothelin-dependent vasoconstriction of skeletal muscle resistance arteries in the presence of tumor necrosis factor-alpha: dependence on c-jun N-terminal kinase. Arterioscler. Thromb. Vasc. Biol. 2006, 26:274-280.
30. Chen Z., Peng I.C., Sun W., et al. AMP-activated protein kinase functionally phosphorylates endothelial nitric oxide synthase Ser633. Circ. Res. 2009, 104:496-505.
31. Xu M.J., Song P., Shirwany N., et al. Impaired expression of uncoupling protein 2 causes defective postischemic angiogenesis in mice deficient in AMP-activated protein kinase + | subunits. Arterioscler. Thromb. Vasc. Biol. 2011, 31:1757-1765.
32. Schisler J.C., Rubel C.E., Zhang C., Lockyer P., Cyr D.M., Patterson C. CHIP protects against cardiac pressure overload through regulation of AMPK. J. Clin. Invest. 2013, 123:3588-3599.
33. Scott J.-J., Ling N., Issa S.M., et al. Small molecule drug A-769662 and AMP synergistically activate naive AMPK independent of upstream kinase signaling. Chem. Biol. 2014, 21:619-627.
34. Eskildsen-Helmond Y.E.G., Mulvany M.J. Pressure-induced activation of extracellular signal-regulated kinase 1/2 in small arteries. Hypertension 2003, 41:891-897.
35. Kohlstedt K., Trouvain C., Boettger T., Shi L., Fisslthaler B., Fleming I. AMP-activated protein kinase regulates endothelial cell angiotensin-converting enzyme expression via p53 and the post-transcriptional regulation of microRNA-143/145. Circ. Res. 2013, 112:1150-1158.
36. Huang A., Sun D., Smith C.J., et al. In eNOS knockout mice skeletal muscle arteriolar dilation to acetylcholine is mediated by EDHF. Am. J. Physiol. Heart Circ. Physiol. 2000, 278:H762-H768.
37. Morrow V.A., Foufelle F., Connell J.M., Petrie J.R., Gould G.W., Salt I.P. Direct activation of AMP-activated protein kinase stimulates nitric-oxide synthesis in human aortic endothelial cells. J. Biol. Chem. 2003, 278:31629-31639.
38. Sharma K., Ramachandrarao S., Qiu G., et al. Adiponectin regulates albuminuria and podocyte function in mice. J. Clin. Invest. 2008, 118:1645-1656.
39. Ouedraogo R., Gong Y., Berzins B., et al. Adiponectin deficiency increases leukocyte-endothelium interactions via upregulation of endothelial cell adhesion molecules in vivo. J. Clin. Invest. 2007, 117:1718-1726.
40. Kim J.E., Song S.E., Kim Y.W., et al. Adiponectin inhibits palmitate-induced apoptosis through suppression of reactive oxygen species in endothelial cells: involvement of cAMP/protein kinase A and AMP-activated protein kinase. J. Endocrinol. 2010, 207:35-44.
41. Yudkin J.S., Eringa E., Stehouwer C.D. "Vasocrine" signalling from perivascular fat: a mechanism linking insulin resistance to vascular disease. Lancet 2005, 365:1817-1820.
42. O'Neill H.M., Maarbjerg S.J., Crane J.D., et al. AMP-activated protein kinase (AMPK) + |1 + |2 muscle null mice reveal an essential role for AMPK in maintaining mitochondrial content and glucose uptake during exercise. PNAS 2011, 108:16092-16097.
43. Vincent M.A., Barrett E.J., Lindner J.R., Clark M.G., Rattigan S. Inhibiting NOS blocks microvascular recruitment and blunts muscle glucose uptake in response to insulin. Am. J. Physiol. Endocrinol. Metab. 2003, 285:E123-E129.
44. Shankar R.R., Wu Y., Shen H.-Q., Zhu J.-S., Baron A.D. Mice with gene disruption of both endothelial and neuronal nitric oxide synthase exhibit insulin resistance. Diabetes 2000, 49.
45. Shemyakin A., Salehzadeh F., Bohm F., et al. Regulation of glucose uptake by endothelin-1 in human skeletal muscle in vivo and in vitro. J. Clin. Endocrinol. Metab. 2010, 95:2359-2366.
46. Chalothorn D., Faber J.E. Strain-dependent variation in collateral circulatory function in mouse hindlimb. Physiol. Genomics 2010, 42:469-479.