Rho-kinase inhibition ameliorates metabolic disorders through activation of AMPK pathway in mice

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Noda, Kazuki ^a   Nakajima, Sota ^a   Godo, Shigeo ^a   Saito, Hiroki ^a   Ikeda, Shohei ^a   Shimizu, Toru ^a   Enkhjargal, Budbazar ^a   Fukumoto, Yoshihiro ^a   Tsukita, Sohei ^a   Yamada, Tetsuya ^a   Katagiri, Hideki ^a   Shimokawa, Hiroaki ^a  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FASUDIL; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LEPTIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MESSENGER RNA; PROTEIN KINASE LKB1; TRIACYLGLYCEROL; AMPK ALPHA2 SUBUNIT, MOUSE; PROTEIN KINASE INHIBITOR; PROTEIN SERINE THREONINE KINASE; RHO KINASE; STK11 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DISEASE ASSOCIATION; DRUG TARGETING; ENERGY CONSUMPTION; ENERGY YIELD; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; FAT MASS; FATTY ACID OXIDATION; FEMALE; GLUCOSE INTOLERANCE; GLUCOSE METABOLISM; HYPERCHOLESTEROLEMIA; IN VITRO STUDY; LIPID DIET; LIVER; MALE; METABOLIC DISORDER; MOUSE; MUSCLE CELL; NONHUMAN; OBESITY; OXYGEN CONSUMPTION; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SKELETAL MUSCLE; WHITE ADIPOSE TISSUE; WILD TYPE; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; CELL LINE; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; ENERGY METABOLISM; GENE EXPRESSION; GENETICS; KNOCKOUT MOUSE; METABOLISM; SIGNAL TRANSDUCTION;

MUS;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CELL LINE; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; ENERGY METABOLISM; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION; MALE; METABOLIC DISEASES; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MUSCLE, SKELETAL; PHENOTYPE; PROTEIN KINASE INHIBITORS; PROTEIN-SERINE-THREONINE KINASES; RHO-ASSOCIATED KINASES; SIGNAL TRANSDUCTION;

EID: 84909606665     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0110446     Document Type: Article

References (51)

1. Despres JP, Lemieux I (2006) Abdominal obesity and metabolic syndrome. Nature 444: 881-887.
2. Shimokawa H, Morishige K, Miyata K, Kandabashi T, Eto Y, et al. (2001) Long-term inhibition of Rho-kinase induces a regression of arteriosclerotic coronary lesions in a porcine model in vivo. Cardiovasc Res 51: 169-177.
3. Shimokawa H, Takeshita A (2005) Rho-kinase is an important therapeutic target in cardiovascular medicine. Arterioscler Thromb Vasc Biol 25: 1767-1775.
4. Shimokawa H, Rashid M (2007) Development of Rho-kinase inhibitors for cardiovascular medicine. Trends Pharmacol Sci 28: 296-302.
5. Hara Y, Wakino S, Tanabe Y, Saito M, Tokuyama H, et al. (2001) Rho and Rho-kinase activity in adipocytes contributes to a vicious cycle in obesity that may involve mechanical stretch. Sci Signal 4: ra3.
6. Kikuchi Y, Yamada M, Imakiire T, Kushiyama T, Higashi K, et al. (2007) A Rho-kinase inhibitor, fasudil, prevents development of diabetes and nephropathy in insulin-resistant diabetic rats. J Endocrinol 192: 595-603.
7. Liu PY, Chen JH, Lin LJ, Liao JK (2007) Increased Rho kinase activity in a Taiwanese population with metabolic syndrome. J Am Coll Cardiol 49: 1619-1624.
8. Hardie DG (2007) AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol 8: 774-785.
9. Xiao B, Sanders MJ, Underwood E, Heath R, Mayer FV, et al. (2011) Structure of mammalian AMPK and its regulation by ADP. Nature 472: 230-233.
10. Canto C, Jiang LQ, Deshmukh AS, Mataki C, Coste A, et al. (2010) Interdependence of AMPK and SIRT1 for metabolic adaptation to fasting and exercise in skeletal muscle. Cell Metab 11: 213-219.
11. Yang YY, Huang YT, Lee TY, Chan CC, Yeh YC, et al. (2012) Rho-kinasedependent pathway mediates the hepatoprotective effects of sorafenib against ischemia/reperfusion liver injury in rats with nonalcoholic steatohepatitis. Liver Transpl 18: 1371-1383.
12. Gaidhu MP, Frontini A, Hung S, Pistor K, Cinti S, et al. (2011) Chronic AMPkinase activation with AICAR reduces adiposity by remodeling adipocyte metabolism and increasing leptin sensitivity. J Lipid Res 52: 1702-1711.
13. Yamauchi T, Kamon J, Minokoshi Y, Ito Y, Waki H, et al. (2002) Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMPactivated protein kinase. Nat Med 8: 1288-1295.
14. Kanazawa I, Yamaguchi T, Yano S, Yamauchi M, Sugimoto T (2009) Activation of AMP kinase and inhibition of Rho kinase induce the mineralization of osteoblastic MC3T3-E1 cells through endothelial NOS and BMP-2 expression. Am J Physiol Endocrinol Metab 296: E139-146.
15. Viollet B, Andreelli F, Jorgensen SB, Perrin C, Geloen A, et al. (2003) The AMP-activated protein kinase a2 catalytic subunit controls whole-body insulin sensitivity. J Clin Invest 111: 91-98.
16. Kobayashi K, Takahashi M, Matsushita N, Miyazaki J, Koike M, et al. (2004) Survival of developing motor neurons mediated by Rho GTPase signaling pathway through Rho-kinase. J Neurosci 24: 3480-3488.
17. Nakajima S, Ohashi J, Sawada A, Noda K, Fukumoto Y, et al. (2012) Essential role of bone marrow for microvascular endothelial and metabolic functions in mice. Circ Res 111: 87-96.
18. Tsukita S, Yamada T, Uno K, Takahashi K, Kaneko K, et al. (2012) Hepatic Glucokinase Modulates Obesity Predisposition by Regulating BAT Thermogenesis via Neural Signals. Cell Metab 16: 825-832.
19. Uno K, Katagiri H, Yamada T, Ishigaki Y, Ogihara T, et al. (2006) Neuronal pathway from the liver modulates energy expenditure and systemic insulin sensitivity. Science 312: 1656-1659.
20. Noda K, Hosoya M, Nakajima S, Ohashi J, Fukumoto Y, et al. (2012) Antiatherogenic effects of the combination therapy with olmesartan and azelnidipine in diabetic apolipoprotein E-deficient mice. Tohoku J Exp Med 228: 305-315.
21. Dai Y, Kiselak T, Clark J, Clore E, Zheng K, et al. (2013) Behavioral and metabolic characterization of heterozygous and homozygous POLG mutator mice. Mitochondrion 13: 282-291.
22. Uehata M, Ishizaki T, Satoh H, Ono T, Kawahara T, et al. (1997) Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389: 990-994.
23. Hong SP, Leiper FC, Woods A, Carling D, Carlson M (2003) Activation of yeast Snf1 and mammalian AMP-activated protein kinase by upstream kinases. Proc Natl Acad Sci USA 100: 8839-8843.
24. Woods A, Dickerson K, Heath R, Hong SP, Momcilovic M, et al. (2005) Ca2+/ calmodulin-dependent protein kinase kinase-b acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab 2: 21-33.
25. Herrero-Martin G, Hoyer-Hansen M, Garcia-Garcia C, Fumarola C, Farkas T, et al. (2009) TAK1 activates AMPK-dependent cytoprotective autophagy in TRAIL-treated epithelial cells. EMBO J 28: 677-685.
26. Ming XF, Viswambharan H, Barandier C, Ruffieux J, Kaibuchi K, et al. (2002) Rho GTPase/Rho kinase negatively regulates endothelial nitric oxide synthase phosphorylation through the inhibition of protein kinase B/Akt in human endothelial cells. Molecular and cellular biology 22: 8467-8477.
27. Furukawa N, Ongusaha P, Jahng WJ, Araki K, Choi CS, et al. (2005) Role of Rho-kinase in regulation of insulin action and glucose homeostasis. Cell Metab 2: 119-129.
28. Kanda T, Wakino S, Homma K, Yoshioka K, Tatematsu S, et al. (2006) Rhokinase as a molecular target for insulin resistance and hypertension. FASEB J 20: 169-171.
29. Lee DH, Shi J, Jeoung NH, Kim MS, Zabolotny JM, et al. (2009) Targeted disruption of ROCK1 causes insulin resistance in vivo. J Biol Chem 284: 11776-11780.
30. Huang H, Kong D, Byun KH, Ye C, Koda S, et al. (2012) Rho-kinase regulates energy balance by targeting hypothalamic leptin receptor signaling. Nature neuroscience 15: 1391-1398.
31. Lee SH, Huang H, Choi K, Lee DH, Shi J, et al. (2014) ROCK1 isoformspecific deletion reveals a role for diet-induced insulin resistance. Am J Physiol Endocrinol Metab 306: E332-343.
32. Oakhill JS, Scott JW, Kemp BE (2009) Structure and function of AMP-activated protein kinase. Acta Physiol (Oxf) 196: 3-14.
33. Su X, Gi YJ, Chakravarti D, Chan IL, Zhang A, et al. (2012) TAp63 is a master transcriptional regulator of lipid and glucose metabolism. Cell Metab 16: 511-525.
34. Mu J, Brozinick JT Jr, Valladares O, Bucan M, Birnbaum MJ (2001) A role for AMP-activated protein kinase in contraction-and hypoxia-regulated glucose transport in skeletal muscle. Mol Cell 7: 1085-1094.
35. Russell RR III, Li J, Coven DL, Pypaert M, Zechner C, et al. (2004) AMPactivated protein kinase mediates ischemic glucose uptake and prevents postischemic cardiac dysfunction, apoptosis, and injury. J Clin Invest 114: 495-503.
36. Musi N, Fujii N, Hirshman MF, Ekberg I, Froberg S, et al. (2001) AMPK is activated in muscle of subjects with type 2 diabetes during exercise. Diabetes 50: 921-927.
37. Jelenik T, Rossmeisl M, Kuda O, Jilkova ZM, Medrikova D, et al. (2010) AMPactivated protein kinase a2 subunit is required for the preservation of hepatic insulin sensitivity by n-3 polyunsaturated fatty acids. Diabetes 59: 2737-2746.
38. Lee WJ, Kim M, Park HS, Kim HS, Jeon MJ, et al. (2006) AMPK activation increases fatty acid oxidation in skeletal muscle by activating PPARa and PGC-1. Biochem Biophys Res Commun 340: 291-295.
39. Jager S, Handschin C, St-Pierre J, Spiegelman BM (2007) AMPK action in skeletal muscle via direct phosphorylation of PGC-1a. Proc Natl Acad Sci USA 104: 12017-12022.
40. Baur JA, Ungvari Z, Minor RK, Le Couteur DG, de Cabo R (2012) Are sirtuins viable targets for improving healthspan and lifespan? Nat Rev Drug Discov 11: 443-461.
41. Zhou G, Myers R, Li Y, Chen Y, Shen X, et al. (2001) Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest 108: 1167-1174.
42. Sun W, Lee TS, Zhu M, Gu C, Wang Y, et al. (2006) Statins activate AMPactivated protein kinase in vitro and in vivo. Circulation 114: 2655-2662.
43. Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, et al. (2006) Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444: 337-342.
44. Minokoshi Y, Kim YB, Peroni OD, Fryer LG, Muller C, et al. (2002) Leptin stimulates fatty-acid oxidation by activating AMP-activated protein kinase. Nature 415: 339-343.
45. Lin HZ, Yang SQ, Chuckaree C, Kuhajda F, Ronnet G, et al. (2000) Metformin reverses fatty liver disease in obese, leptin-deficient mice. Nat Med 6: 998-1003.
46. Stumvoll M, Nurjhan N, Perriello G, Dailey G, Gerich JE (1995) Metabolic effects of metformin in non-insulin-dependent diabetes mellitus. N Engl J Med 333: 550-554.
47. Ruperez M, Rodrigues-Diez R, Blanco-Colio LM, Sanchez-Lopez E, Rodriguez-Vita J, et al. (2007) HMG-CoA reductase inhibitors decrease angiotensin II-induced vascular fibrosis: role of RhoA/ROCK and MAPK pathways. Hypertension 50: 377-383.
48. Sattar N, Preiss D, Murray HM, Welsh P, Buckley BM, et al. (2010) Statins and risk of incident diabetes: a collaborative meta-analysis of randomised statin trials. Lancet 375: 735-742.
49. Hattori T, Shimokawa H, Higashi M, Hiroki J, Mukai Y, et al. (2004) Long-term inhibition of Rho-kinase suppresses left ventricular remodeling after myocardial infarction in mice. Circulation 109: 2234-2239.
50. Rockl KS, Hirshman MF, Brandauer J, Fujii N, Witters LA, et al. (2007) Skeletal muscle adaptation to exercise training: AMP-activated protein kinase mediates muscle fiber type shift. Diabetes 56: 2062-2069.
51. Davies SP, Reddy H, Caivano M, Cohen P (2000) Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351: 95-105.