Endothelial cell-specific liver kinase B1 deletion causes endothelial dysfunction and hypertension in mice in vivo

Circulation

Volumn 129, Issue 13, 2014, Pages 1428-1439

  Zhang, Wencheng ^a   Wang, Qilong ^a   Wu, Yue ^a,b   Moriasi, Cate ^a   Liu, Zhaoyu ^a   Dai, Xiaoyan ^a   Wang, Qiongxin ^a   Liu, Weimin ^b   Yuan, Zu Yi ^b   Zou, Ming Hui ^a,b,c  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b MEDICAL SCHOOL OF XI AN JIAOTONG UNIVERSITY   (China)

^c SHANDONG UNIVERSITY   (China)

Author keywords

AMP activated protein kinases; caveolin 1; hypertension; nitric oxide synthase type III

Indexed keywords

CAVEOLIN 1; ENDOTHELIAL NITRIC OXIDE SYNTHASE; LIVER ENZYME; LIVER KINASE B1; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN;

3' UNTRANSLATED REGION; ARTICLE; BLOOD PRESSURE; CELL SPECIFICITY; CONTROLLED STUDY; CROSS BREEDING; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HEART VENTRICLE HYPERTROPHY; HYPERTENSION; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STABILITY;

AMP-ACTIVATED PROTEIN KINASES; CAVEOLIN 1; HYPERTENSION; NITRIC OXIDE SYNTHASE TYPE III;

ADENYLATE KINASE; ANIMALS; BLOOD PRESSURE; CAVEOLIN 1; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; GENE DELETION; HYPERTENSION; MALE; MICE; MICE, KNOCKOUT; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION;

EID: 84898059358     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.113.004146     Document Type: Article

References (46)

1. Deanfield JE, Halcox JP, Rabelink TJ
2. Brunner H, Cockcroft JR, Deanfield J, Donald A, Ferrannini E, Halcox J, Kiowski W, lüscher TF, Mancia G, Natali A, Oliver JJ, Pessina AC, Rizzoni D, Rossi GP, Salvetti A, Spieker lE, Taddei S, Webb DJ; Working Group on Endothelins and Endothelial Factors of the European Society of Hypertension. Endothelial function and dysfunction, part II: association with cardiovascular risk factors and diseases: a statement by the Working Group on Endothelins and Endothelial Factors of the European Society of Hypertension. J Hypertens. 2005;23:233-246.
3. Versari D, Daghini E, Virdis A, Ghiadoni l, Taddei S. Endothelial dysfunction as a target for prevention of cardiovascular disease. Diabetes Care. 2009;32(suppl 2):S314-S321.
4. Palmer RM, Ferrige AG, Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature. 1987;327:524-526.
5. Huang PL, Huang Z, Mashimo H, Bloch KD, Moskowitz MA, Bevan JA, Fishman MC. Hypertension in mice lacking the gene for endothelial nitric oxide synthase. Nature. 1995;377:239-242.
6. Moroi M, Zhang L, Yasuda T, Virmani R, Gold HK, Fishman MC, Huang Pl. Interaction of genetic deficiency of endothelial nitric oxide, gender, and pregnancy in vascular response to injury in mice. J Clin Invest. 1998;101:1225-1232.
7. Lefer DJ, Jones SP, Girod WG, Baines A, Grisham MB, Cockrell AS, Huang Pl, Scalia R. leukocyte-endothelial cell interactions in nitric oxide synthase-deficient mice. Am J Physiol. 1999;276(pt 2):H1943-H1950.
8. Freedman JE, Sauter R, Battinelli EM, Ault K, Knowles C, Huang PL, Loscalzo J. Deficient platelet-derived nitric oxide and enhanced hemostasis in mice lacking the NOSIII gene. Circ Res. 1999;84:1416-1421.
9. Kuhlencordt PJ, Gyurko R, Han F, Scherrer-Crosbie M, Aretz TH, Hajjar R, Picard MH, Huang Pl. Accelerated atherosclerosis, aortic aneurysm formation, and ischemic heart disease in apolipoprotein E/endothelial nitric oxide synthase double-knockout mice. Circulation. 2001;104:448-454.
10. Li S, Couet J, Lisanti MP. Src tyrosine kinases, Galpha subunits, and H-Ras share a common membrane-anchored scaffolding protein, caveolin: caveolin binding negatively regulates the auto-activation of Src tyrosine kinases. J Biol Chem. 1996;271:29182-29190.
11. Carver LA, Schnitzer JE. Caveolae: mining little caves for new cancer targets. Nat Rev Cancer. 2003;3:571-581.
12. Drab M, Verkade P, Elger M, Kasper M, Lohn M, Lauterbach B, Menne J, Lindschau C, Mende F, Luft FC, Schedl A, Haller H, Kurzchalia TV. loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science. 2001;293:2449-2452.
13. Razani B, Engelman JA, Wang XB, Schubert W, Zhang XL, Marks CB, Macaluso F, Russell RG, Li M, Pestell RG, Di Vizio D, Hou H Jr, Kneitz B, Lagaud G, Christ GJ, Edelmann W, lisanti MP. Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J Biol Chem. 2001;276:38121-38138.
14. Giardiello FM, Trimbath JD. Peutz-Jeghers syndrome and management recommendations. Clin Gastroenterol Hepatol. 2006;4:408-415.
15. Katajisto P, Vallenius T, Vaahtomeri K, Ekman N, Udd l, Tiainen M, Mäkelä TP. The lKB1 tumor suppressor kinase in human disease. Biochim Biophys Acta. 2007;1775:63-75.
16. Alessi DR, Sakamoto K, Bayascas JR. lKB1-dependent signaling pathways. Annu Rev Biochem. 2006;75:137-163.
17. Shackelford DB, Shaw RJ. The lKB1-AMPK pathway: metabolism and growth control in tumour suppression. Nat Rev Cancer. 2009;9:563-575.
18. Ylikorkala A, Rossi DJ, Korsisaari N, Luukko K, Alitalo K, Henkemeyer M, Mäkelä TP. Vascular abnormalities and deregulation of VEGF in lkb1-deficient mice. Science. 2001;293:1323-1326.
19. londesborough A, Vaahtomeri K, Tiainen M, Katajisto P, Ekman N, Vallenius T, Mäkelä TP. lKB1 in endothelial cells is required for angiogenesis and TGFbeta-mediated vascular smooth muscle cell recruitment. Development. 2008;135:2331-2338.
20. Ohashi K, Ouchi N, Higuchi A, Shaw RJ, Walsh K. lKB1 deficiency in Tie2-Cre-expressing cells impairs ischemia-induced angiogenesis. J Biol Chem. 2010;285:22291-22298.
21. Gustafsson E, Brakebusch C, Hietanen K, Fässler R. Tie-1-directed expression of Cre recombinase in endothelial cells of embryoid bodies and transgenic mice. J Cell Sci. 2001;114(pt 4):671-676.
22. 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.
23. Alva JA, Zovein AC, Monvoisin A, Murphy T, Salazar A, Harvey Nl, Carmeliet P, Iruela-Arispe Ml. VE-Cadherin-Cre-recombinase transgenic mouse: a tool for lineage analysis and gene deletion in endothelial cells. Dev Dyn. 2006;235:759-767.
24. Bardeesy N, Sinha M, Hezel AF, Signoretti S, Hathaway NA, Sharpless NE, Loda M, Carrasco DR, DePinho RA. Loss of the lkb1 tumour suppressor provokes intestinal polyposis but resistance to transformation. Nature. 2002;419:162-167.
25. Zhang W, Wang Q, Song P, Zou MH. Liver kinase b1 is required for white adipose tissue growth and differentiation. Diabetes. 2013;62:2347-2358.
26. Liang B, Wang S, Wang Q, Zhang W, Viollet B, Zhu Y, Zou MH. Aberrant endoplasmic reticulum stress in vascular smooth muscle increases vascular contractility and blood pressure in mice deficient of AMP-activated protein kinase-α2 in vivo. Arterioscler Thromb Vasc Biol. 2013;33:595-604.
27. García-Cardeña G, Fan R, Stern DF, Liu J, Sessa WC. Endothelial nitric oxide synthase is regulated by tyrosine phosphorylation and interacts with caveolin-1. J Biol Chem. 1996;271:27237-27240.
28. Feron O, Belhassen L, Kobzik L, Smith TW, Kelly RA, Michel T. Endothelial nitric oxide synthase targeting to caveolae: specific interactions with caveolin isoforms in cardiac myocytes and endothelial cells. J Biol Chem. 1996;271:22810-22814.
29. Wang W, Fan J, Yang X, Fürer-Galban S, lopez de Silanes I, von Kobbe C, Guo J, Georas SN, Foufelle F, Hardie DG, Carling D, Gorospe M. AMP-activated kinase regulates cytoplasmic HuR. Mol Cell Biol. 2002;22:3425-3436.
30. lee S, Chen TT, Barber CL, Jordan MC, Murdock J, Desai S, Ferrara N, Nagy A, Roos KP, Iruela-Arispe Ml. Autocrine VEGF signaling is required for vascular homeostasis. Cell. 2007;130:691-703.
31. Goetz JG, Lajoie P, Wiseman SM, Nabi IR. Caveolin-1 in tumor progression: the good, the bad and the ugly. Cancer Metastasis Rev. 2008;27:715-735.
32. Xie Z, Dong Y, Zhang M, Cui MZ, Cohen RA, Riek U, Neumann D, Schlattner U, Zou MH. Activation of protein kinase C zeta by peroxynitrite regulates lKB1-dependent AMP-activated protein kinase in cultured endothelial cells. J Biol Chem. 2006;281:6366-6375.
33. Xie Z, Dong Y, Scholz R, Neumann D, Zou MH. Phosphorylation of lKB1 at serine 428 by protein kinase C-zeta is required for metformin-enhanced activation of the AMP-activated protein kinase in endothelial cells. Circulation. 2008;117:952-962.
34. Levy NS, Chung S, Furneaux H, Levy AP. Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. J Biol Chem. 1998;273:6417-6423.
35. Wang W, Furneaux H, Cheng H, Caldwell MC, Hutter D, liu Y, Holbrook N, Gorospe M. HuR regulates p21 mRNA stabilization by UV light. Mol Cell Biol. 2000;20:760-769.
36. Maurer F, Tierney M, Medcalf RL. An AU-rich sequence in the 3′-UTR of plasminogen activator inhibitor type 2 (PAI-2) mRNA promotes PAI-2 mRNA decay and provides a binding site for nuclear HuR. Nucleic Acids Res. 1999;27:1664-1673.
37. Schubert W, Frank PG, Woodman SE, Hyogo H, Cohen DE, Chow CW, lisanti MP. Microvascular hyperpermeability in caveolin-1 (-/-) knock-out mice. Treatment with a specific nitric-oxide synthase inhibitor, l-NAME, restores normal microvascular permeability in Cav-1 null mice. J Biol Chem. 2002;277:40091- 40098.
38. Fernández-Hernando C, Yu J, Suarez Y, Rahner C, Davalos A, Lasuncion MA, Sessa WC. Genetic evidence supporting a critical role of endothelial caveolin-1 during the progression of atherosclerosis. Cell Metab. 2009;10:48-54.
39. Chidlow JH Jr, Greer JJ, Anthoni C, Bernatchez P, Fernandez-Hernando C, Fernadez-Hernando C, Bruce M, Abdelbaqi M, Shukla D, Granger DN, Sessa WC, Kevil CG. Endothelial caveolin-1 regulates pathologic angiogenesis in a mouse model of colitis. Gastroenterology. 2009;136:575-84. e2.
40. Reihill JA, Ewart MA, Hardie DG, Salt IP. AMP-activated protein kinase mediates VEGF-stimulated endothelial NO production. Biochem Biophys Res Commun. 2007;354:1084-1088.
41. Davis BJ, Xie Z, Viollet B, Zou MH. Activation of the AMP-activated kinase by antidiabetes drug metformin stimulates nitric oxide synthesis in vivo by promoting the association of heat shock protein 90 and endothelial nitric oxide synthase. Diabetes. 2006;55:496-505.
42. Cheng KK, Lam KS, Wang Y, Huang Y, Carling D, Wu D, Wong C, Xu A. Adiponectin-induced endothelial nitric oxide synthase activation and nitric oxide production are mediated by APPl1 in endothelial cells. Diabetes. 2007;56:1387-1394.
43. Fisslthaler B, Fleming I. Activation and signaling by the AMP-activated protein kinase in endothelial cells. Circ Res. 2009;105:114-127.
44. 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.
45. Noga AA, Soltys CL, Barr AJ, Kovacic S, Lopaschuk GD, Dyck JR. Expression of an active lKB1 complex in cardiac myocytes results in decreased protein synthesis associated with phenylephrine-induced hypertrophy. Am J Physiol Heart Circ Physiol. 2007;292:H1460-H1469.
46. Calamaras TD, lee C, lan F, Ido Y, Siwik DA, Colucci WS. Post-translational modification of serine/threonine kinase lKB1 via adduction of the reactive lipid species 4-hydroxy-trans-2-nonenal (HNE) at lysine residue 97 directly inhibits kinase activity. J Biol Chem. 2012;287:42400-42406.