Protective Roles of Endothelial AMP-Activated Protein Kinase Against Hypoxia-Induced Pulmonary Hypertension in Mice

Circulation Research

Volumn 119, Issue 2, 2016, Pages 197-209

  Omura, Junichi ^a   Satoh, Kimio ^a   Kikuchi, Nobuhiro ^a   Satoh, Taijyu ^a   Kurosawa, Ryo ^a   Nogi, Masamichi ^a   Otsuki, Tomohiro ^a   Kozu, Katsuya ^a   Numano, Kazuhiko ^a   Suzuki, Kota ^a   Sunamura, Shinichiro ^a   Tatebe, Shunsuke ^a   Aoki, Tatsuo ^a   Sugimura, Koichiro ^a   Miyata, Satoshi ^a   Hoshikawa, Yasushi ^b   Okada, Yoshinori ^b   Shimokawa, Hiroaki ^a  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b TOHOKU UNIVERSITY   (Japan)

Author keywords

cell proliferation; cytokines; inflammation; metformin; pulmonary hypertension

Indexed keywords

CASPASE 3; CD31 ANTIGEN; CYCLINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; FIBROBLAST GROWTH FACTOR 2; GAMMA INTERFERON; GROWTH FACTOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; METFORMIN; PLATELET DERIVED GROWTH FACTOR BB; PROTEIN P53; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE EXACERBATION; DOWN REGULATION; ENDOTHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA-INDUCED PULMONARY HYPERTENSION; IMMUNOHISTOCHEMISTRY; LUNG PARENCHYMA; MALE; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PULMONARY ARTERY SMOOTH MUSCLE CELL; PULMONARY HYPERTENSION; UPREGULATION; AGED; ANIMAL; C57BL MOUSE; CELL CULTURE; ENZYME ACTIVATION; ENZYMOLOGY; HYPERTENSION, PULMONARY; HYPOXIA; KNOCKOUT MOUSE; METABOLISM; MIDDLE AGED; PHYSIOLOGY; VASCULAR ENDOTHELIUM;

ADULT; AGED; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; ENZYME ACTIVATION; FEMALE; HUMANS; HYPERTENSION, PULMONARY; HYPOXIA; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED;

EID: 84970021233     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.115.308178     Document Type: Article

References (56)

1. Rabinovitch M, Guignabert C, Humbert M, Nicolls MR, Inflammation and immunity in the pathogenesis of pulmonary arterial hypertension. Circ Res 2014 115 165 175. doi: 10.1161/CIRCRESAHA.113.301141
2. Lai YC, Potoka KC, Champion HC, Mora AL, Gladwin MT, Pulmonary arterial hypertension: the clinical syndrome. Circ Res 2014 115 115 130. doi: 10.1161/CIRCRESAHA.115.301146
3. Zamanian RT, Kudelko KT, Sung YK, de Jesus Perez V, Liu J, Spiekerkoetter E, Current clinical management of pulmonary arterial hypertension. Circ Res 2014 115 131 147. doi: 10.1161/CIRCRESAHA.115.303827
4. Paulin R, Michelakis ED, The metabolic theory of pulmonary arterial hypertension. Circ Res 2014 115 148 164
5. Ryan JJ, Archer SL, The right ventricle in pulmonary arterial hypertension: disorders of metabolism, angiogenesis and adrenergic signaling in right ventricular failure. Circ Res 2014 115 176 188. doi: 10.1161/CIRCRESAHA.113.301129
6. Teichert-Kuliszewska K, Kutryk MJ, Kuliszewski MA, Karoubi G, Courtman DW, Zucco L, Granton J, Stewart DJ, Bone morphogenetic protein receptor-2 signaling promotes pulmonary arterial endothelial cell survival: implications for loss-of-function mutations in the pathogenesis of pulmonary hypertension. Circ Res 2006 98 209 217. doi: 10.1161/01.RES.0000200180.01710.e6
7. Archer SL, Weir EK, Wilkins MR, Basic science of pulmonary arterial hypertension for clinicians: new concepts and experimental therapies. Circulation 2010 121 2045 2066. doi: 10.1161/CIRCULATIONAHA.108.847707
8. Huertas A, Perros F, Tu L, Cohen-Kaminsky S, Montani D, Dorfmüller P, Guignabert C, Humbert M, Immune dysregulation and endothelial dysfunction in pulmonary arterial hypertension: a complex interplay. Circulation 2014 129 1332 1340. doi: 10.1161/CIRCULATIONAHA.113.004555
9. Tu L, Dewachter L, Gore B, Fadel E, Dartevelle P, Simonneau G, Humbert M, Eddahibi S, Guignabert C, Autocrine fibroblast growth factor-2 signaling contributes to altered endothelial phenotype in pulmonary hypertension. Am J Respir Cell Mol Biol 2011 45 311 322. doi: 10.1165/rcmb.2010-0317OC
10. Quinlan TR, Li D, Laubach VE, Shesely EG, Zhou N, Johns RA, eNOS-deficient mice show reduced pulmonary vascular proliferation and remodeling to chronic hypoxia. Am J Physiol Lung Cell Mol Physiol 2000 279 L641 L650
11. Tuder RM, Cool CD, Geraci MW, Wang J, Abman SH, Wright L, Badesch D, Voelkel NF, Prostacyclin synthase expression is decreased in lungs from patients with severe pulmonary hypertension. Am J Respir Crit Care Med 1999 159 1925 1932. doi: 10.1164/ajrccm.159.6.9804054
12. Ewart MA, Kennedy S, AMPK and vasculoprotection. Pharmacol Ther 2011 131 242 253. doi: 10.1016/j.pharmthera.2010.11.002
13. Fisslthaler B, Fleming I, Activation and signaling by the AMP-activated protein kinase in endothelial cells. Circ Res 2009 105 114 127. doi: 10.1161/CIRCRESAHA.109.201590
14. Noda K, Nakajima S, Godo S, Saito H, Ikeda S, Shimizu T, Enkhjargal B, Fukumoto Y, Tsukita S, Yamada T, Katagiri H, Shimokawa H, Rho-kinase inhibition ameliorates metabolic disorders through activation of AMPK pathway in mice. PLoS One 2014 9 e110446. doi: 10.1371/journal.pone.0110446
15. Shimizu T, Fukumoto Y, Tanaka S, Satoh K, Ikeda S, Shimokawa H, Crucial role of ROCK2 in vascular smooth muscle cells for hypoxia-induced pulmonary hypertension in mice. Arterioscler Thromb Vasc Biol 2013 33 2780 2791. doi: 10.1161/ATVBAHA.113.301357
16. Ikeda S, Satoh K, Kikuchi N, Miyata S, Suzuki K, Omura J, Shimizu T, Kobayashi K, Kobayashi K, Fukumoto Y, Sakata Y, Shimokawa H, Crucial role of rho-kinase in pressure overload-induced right ventricular hypertrophy and dysfunction in mice. Arterioscler Thromb Vasc Biol 2014 34 1260 1271. doi: 10.1161/ATVBAHA.114.303320
17. Elias-Al-Mamun M, Satoh K, Tanaka S-i, Shimizu T, Nergui S, Miyata S, Fukumoto Y, Shimokawa H, Combination therapy with fasudil and sildenafil ameliorates monocrotaline-induced pulmonary hypertension and survival in rats. Circ J 2014 78 967 976
18. Ido Y, Carling D, Ruderman N, Hyperglycemia-induced apoptosis in human umbilical vein endothelial cells: inhibition by the AMP-activated protein kinase activation. Diabetes 2002 51 159 167
19. Igata M, Motoshima H, Tsuruzoe K, Kojima K, Matsumura T, Kondo T, Taguchi T, Nakamaru K, Yano M, Kukidome D, Matsumoto K, Toyonaga T, Asano T, Nishikawa T, Araki E, Adenosine monophosphate-activated protein kinase suppresses vascular smooth muscle cell proliferation through the inhibition of cell cycle progression. Circ Res 2005 97 837 844. doi: 10.1161/01.RES.0000185823.73556.06
20. Eddahibi S, Guignabert C, Barlier-Mur AM, Dewachter L, Fadel E, Dartevelle P, Humbert M, Simonneau G, Hanoun N, Saurini F, Hamon M, Adnot S, Cross talk between endothelial and smooth muscle cells in pulmonary hypertension: critical role for serotonin-induced smooth muscle hyperplasia. Circulation 2006 113 1857 1864. doi: 10.1161/CIRCULATIONAHA.105.591321
21. Humbert M, Montani D, Perros F, Dorfmüller P, Adnot S, Eddahibi S, Endothelial cell dysfunction and cross talk between endothelium and smooth muscle cells in pulmonary arterial hypertension. Vascul Pharmacol 2008 49 113 118. doi: 10.1016/j.vph.2008.06.003
22. Ibe JC, Zhou Q, Chen T, Tang H, Yuan JX, Raj JU, Zhou G, Adenosine monophosphate-activated protein kinase is required for pulmonary artery smooth muscle cell survival and the development of hypoxic pulmonary hypertension. Am J Respir Cell Mol Biol 2013 49 609 618. doi: 10.1165/rcmb.2012-0446OC
23. Teng RJ, Du J, Afolayan AJ, Eis A, Shi Y, Konduri GG, AMP kinase activation improves angiogenesis in pulmonary artery endothelial cells with in utero pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 2013 304 L29 L42. doi: 10.1152/ajplung.00200.2012
24. Enkhjargal B, Godo S, Sawada A, Suvd N, Saito H, Noda K, Satoh K, Shimokawa H, Endothelial AMP-activated protein kinase regulates blood pressure and coronary flow responses through hyperpolarization mechanism in mice. Arterioscler Thromb Vasc Biol 2014 34 1505 1513. doi: 10.1161/ATVBAHA.114.303735
25. Satoh K, Fukumoto Y, Nakano M, Sugimura K, Nawata J, Demachi J, Karibe A, Kagaya Y, Ishii N, Sugamura K, Shimokawa H, Statin ameliorates hypoxia-induced pulmonary hypertension associated with down-regulated stromal cell-derived factor-1. Cardiovasc Res 2009 81 226 234. doi: 10.1093/cvr/cvn244
26. Zou MH, Wu Y, AMP-activated protein kinase activation as a strategy for protecting vascular endothelial function. Clin Exp Pharmacol Physiol 2008 35 535 545. doi: 10.1111/j.1440-1681.2007.04851.x
27. Sun W, Lee TS, Zhu M, Gu C, Wang Y, Zhu Y, Shyy JY, Statins activate AMP-activated protein kinase in vitro and in vivo. Circulation 2006 114 2655 2662. doi: 10.1161/CIRCULATIONAHA.106.630194
28. Zhou G, Myers R, Li Y, Chen Y, Shen X, Fenyk-Melody J, Wu M, Ventre J, Doebber T, Fujii N, Musi N, Hirshman MF, Goodyear LJ, Moller DE, Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest 2001 108 1167 1174. doi: 10.1172/JCI13505
29. Chandra SM, Razavi H, Kim J, Agrawal R, Kundu RK, de Jesus Perez V, Zamanian RT, Quertermous T, Chun HJ, Disruption of the apelin-APJ system worsens hypoxia-induced pulmonary hypertension. Arterioscler Thromb Vasc Biol 2011 31 814 820. doi: 10.1161/ATVBAHA.110.219980
30. Satoh K, Satoh T, Kikuchi N, Basigin mediates pulmonary hypertension by promoting inflammation and vascular smooth muscle cell proliferation. Circ Res 2014 115 738 750. doi: 10.1161/CIRCRESAHA.115.304563
31. Satoh K, Kagaya Y, Nakano M, Important role of endogenous erythropoietin system in recruitment of endothelial progenitor cells in hypoxia-induced pulmonary hypertension in mice. Circulation 2006 113 1442 1450. doi: 10.1161/CIRCULATIONAHA.105.583732
32. Viollet B, Andreelli F, Jørgensen SB, The AMP-activated protein kinase alpha 2 catalytic subunit controls whole-body insulin sensitivity. J Clin Invest 2003 111 91 98. doi: 10.1172/JCI16567
33. Kisanuki YY, Hammer RE, Miyazaki J, Williams SC, Richardson JA, Yanagisawa M, Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo. Dev Biol 2001 230 230 242. doi: 10.1006/dbio.2000.0106
34. Comhair SA, Xu W, Mavrakis L, Aldred MA, Asosingh K, Erzurum SC, Human primary lung endothelial cells in culture. Am J Respir Cell Mol Biol 2012 46 723 730. doi: 10.1165/rcmb.2011-0416TE
35. Nakano M, Satoh K, Fukumoto Y, Ito Y, Kagaya Y, Ishii N, Sugamura K, Shimokawa H, Important role of erythropoietin receptor to promote VEGF expression and angiogenesis in peripheral ischemia in mice. Circ Res 2007 100 662 669. doi: 10.1161/01.RES.0000260179.43672.fe
36. Cory AH, Owen TC, Barltrop JA, Cory JG, Use of an aqueous soluble tetrazolium/formazan assay for cell growth assays in culture. Cancer Commun 1991 3 207 212
37. Hoffman GR, Moerke NJ, Hsia M, Shamu CE, Blenis J, A high-throughput, cell-based screening method for siRNA and small molecule inhibitors of mTORC1 signaling using the In Cell Western technique. Assay Drug Dev Technol 2010 8 186 199. doi: 10.1089/adt.2009.0213
38. Reagan-Shaw S, Nihal M, Ahmad N, Dose translation from animal to human studies revisited. FASEB J 2008 22 659 661. doi: 10.1096/fj.07-9574LSF
39. Rattan R, Graham RP, Maguire JL, Giri S, Shridhar V, Metformin suppresses ovarian cancer growth and metastasis with enhancement of cisplatin cytotoxicity in vivo. Neoplasia 2011 13 483 491
40. Deng L, Blanco FJ, Stevens H, MicroRNA-143 activation regulates smooth muscle and endothelial cell crosstalk in pulmonary arterial hypertension. Circ Res 2015 117 870 883. doi: 10.1161/CIRCRESAHA.115.306806
41. Nagata D, Mogi M, Walsh K, AMP-activated protein kinase (AMPK) signaling in endothelial cells is essential for angiogenesis in response to hypoxic stress. J Biol Chem 2003 278 31000 31006. doi: 10.1074/jbc.M300643200
42. Shimokawa H, Satoh K, 2015 ATVB Plenary Lecture: translational research on rho-kinase in cardiovascular medicine. Arterioscler Thromb Vasc Biol 2015 35 1756 1769. doi: 10.1161/ATVBAHA.115.305353
43. Afolayan AJ, Eis A, Alexander M, Michalkiewicz T, Teng RJ, Lakshminrusimha S, Konduri GG, Decreased endothelial nitric oxide synthase expression and function contribute to impaired mitochondrial biogenesis and oxidative stress in fetal lambs with persistent pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 2016 310 L40 L49. doi: 10.1152/ajplung.00392.2014
44. Le Hiress M, Tu L, Ricard N, Phan C, Thuillet R, Fadel E, Dorfmüller P, Montani D, de Man F, Humbert M, Huertas A, Guignabert C, Proinflammatory signature of the dysfunctional endothelium in pulmonary hypertension. Role of the macrophage migration inhibitory factor/CD74 complex. Am J Respir Crit Care Med 2015 192 983 997. doi: 10.1164/rccm.201402-0322OC
45. Rabinovitch M, Molecular pathogenesis of pulmonary arterial hypertension. J Clin Invest 2012 122 4306 4313. doi: 10.1172/JCI60658
46. Izikki M, Guignabert C, Fadel E, Humbert M, Tu L, Zadigue P, Dartevelle P, Simonneau G, Adnot S, Maitre B, Raffestin B, Eddahibi S, Endothelial-derived FGF2 contributes to the progression of pulmonary hypertension in humans and rodents. J Clin Invest 2009 119 512 523. doi: 10.1172/JCI35070
47. Soon E, Holmes AM, Treacy CM, Doughty NJ, Southgate L, Machado RD, Trembath RC, Jennings S, Barker L, Nicklin P, Walker C, Budd DC, Pepke-Zaba J, Morrell NW, Elevated levels of inflammatory cytokines predict survival in idiopathic and familial pulmonary arterial hypertension. Circulation 2010 122 920 927. doi: 10.1161/CIRCULATIONAHA.109.933762
48. Budhiraja R, Tuder RM, Hassoun PM, Endothelial dysfunction in pulmonary hypertension. Circulation 2004 109 159 165. doi: 10.1161/01.CIR.0000102381.57477.50
49. Hattori Y, Suzuki K, Hattori S, Kasai K, Metformin inhibits cytokine-induced nuclear factor kappaB activation via AMP-activated protein kinase activation in vascular endothelial cells. Hypertension 2006 47 1183 1188. doi: 10.1161/01.HYP.0000221429.94591.72
50. Hashimoto-Kataoka T, Hosen N, Sonobe T, Interleukin-6/interleukin-21 signaling axis is critical in the pathogenesis of pulmonary arterial hypertension. Proc Natl Acad Sci USA 2015 112 E2677 E2686. doi: 10.1073/pnas.1424774112
51. Ruderman NB, Keller C, Richard AM, Saha AK, Luo Z, Xiang X, Giralt M, Ritov VB, Menshikova EV, Kelley DE, Hidalgo J, Pedersen BK, Kelly M, Interleukin-6 regulation of AMP-activated protein kinase. Potential role in the systemic response to exercise and prevention of the metabolic syndrome. Diabetes 2006 55(suppl 2) S48 S54. doi: 10.2337/db06-S007
52. Hawley SA, Fullerton MD, Ross FA, Schertzer JD, Chevtzoff C, Walker KJ, Peggie MW, Zibrova D, Green KA, Mustard KJ, Kemp BE, Sakamoto K, Steinberg GR, Hardie DG, The ancient drug salicylate directly activates AMP-activated protein kinase. Science 2012 336 918 922. doi: 10.1126/science.1215327
53. Pirkmajer S, Kulkarni SS, Tom RZ, Ross FA, Hawley SA, Hardie DG, Zierath JR, Chibalin AV, Methotrexate promotes glucose uptake and lipid oxidation in skeletal muscle via AMPK activation. Diabetes 2015 64 360 369. doi: 10.2337/db14-0508
54. Hardie DG, Ross FA, Hawley SA, AMP-activated protein kinase: a target for drugs both ancient and modern. Chem Biol 2012 19 1222 1236. doi: 10.1016/j.chembiol.2012.08.019
55. Smith SC, Benjamin EJ, Bonow RO, Braun LT, Creager MA, Franklin BA, Gibbons RJ, Grundy SM, Hiratzka LF, Jones DW, Lloyd-Jones DM, Minissian M, Mosca L, Peterson ED, Sacco RL, Spertus J, Stein JH, Taubert KA, AHA/ACCF secondary prevention and risk reduction therapy for patients with coronary and other atherosclerotic vascular disease: 2011 Update: A Guideline from the American Heart Association and American College of Cardiology Foundation. Circulation 2011 124 2458 2473
56. Agard C, Rolli-Derkinderen M, Dumas-de-La-Roque E, Rio M, Sagan C, Savineau JP, Loirand G, Pacaud P, Protective role of the antidiabetic drug metformin against chronic experimental pulmonary hypertension. Br J Pharmacol 2009 158 1285 1294. doi: 10.1111/j.1476-5381.2009.00445.x