AMP-Activated protein kinase α1 in macrophages promotes collateral remodeling and arteriogenesis in mice in vivo

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 36, Issue 9, 2016, Pages 1868-1878

  Zhu, Huaiping ^a   Zhang, Miao ^b   Liu, Zhaoyu ^a   Xing, Junjie ^b   Moriasi, Cate ^a   Dai, Xiaoyan ^a   Zou, Ming Hui ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

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

Author keywords

AMP Activated protein kinases; Knockout; Macrophages; Mice; NF kappa B; Transforming growth factor beta

Indexed keywords

AMP ACTIVATED PROTEIN KINASE ALPHA1; AMP ACTIVATED PROTEIN KINASE ALPHA2; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; I KAPPA B KINASE ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; THREONINE; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; AMPK ALPHA1 SUBUNIT, MOUSE; AMPK ALPHA2 SUBUNIT, MOUSE; CHUK PROTEIN, MOUSE; I KAPPA B KINASE; RELA PROTEIN, MOUSE; TRANSCRIPTION FACTOR RELA; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIOLE; ARTERY LIGATION; ARTICLE; BLOOD FLOW; COLLATERAL ARTERY; CONTROLLED STUDY; ENZYME ACTIVATION; FEMORAL ARTERY; GENE INACTIVATION; HINDLIMB; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; TISSUE REPAIR; ANIMAL; C57BL MOUSE; COLLATERAL CIRCULATION; CONVALESCENCE; DEFICIENCY; DISEASE MODEL; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; GENOTYPE; HEK293 CELL LINE; HUMAN; ISCHEMIA; KNOCKOUT MOUSE; METABOLISM; PATHOPHYSIOLOGY; PHENOTYPE; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TIME FACTOR; VASCULAR REMODELING; VASCULARIZATION;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; COLLATERAL CIRCULATION; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; GENOTYPE; HEK293 CELLS; HINDLIMB; HUMANS; I-KAPPA B KINASE; ISCHEMIA; MACROPHAGES; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE, SKELETAL; NEOVASCULARIZATION, PHYSIOLOGIC; PHENOTYPE; PHOSPHORYLATION; RECOVERY OF FUNCTION; REGIONAL BLOOD FLOW; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSCRIPTION FACTOR RELA; TRANSFECTION; TRANSFORMING GROWTH FACTOR BETA; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR REMODELING;

EID: 84979695565     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.116.307743     Document Type: Article

References (45)

1. Carmeliet P, Mechanisms of angiogenesis and arteriogenesis. Nat Med 2000 6 389 395. doi: 10.1038/74651
2. Cai W, Schaper W, Mechanisms of arteriogenesis. Acta Biochim Biophys Sin (Shanghai) 2008 40 681 692
3. Heil M, Eitenmüller I, Schmitz-Rixen T, Schaper W, Arteriogenesis versus angiogenesis: Similarities and differences. J Cell Mol Med 2006 10 45 55
4. Fung E, Helisch A, Macrophages in collateral arteriogenesis. Front Physiol 2012 3 353. doi: 10.3389/fphys.2012.00353
5. Heil M, Schaper W, Cellular mechanisms of arteriogenesis. Exs 2005 181 191
6. Heil M, Schaper W, Insights into pathways of arteriogenesis. Curr Pharm Biotechnol 2007 8 35 42
7. Schaper W, Scholz D, Factors regulating arteriogenesis. Arterioscler Thromb Vasc Biol 2003 23 1143 1151. doi: 10.1161/01.ATV.0000069625.11230.96
8. Khmelewski E, Becker A, Meinertz T, Ito WD, Tissue resident cells play a dominant role in arteriogenesis and concomitant macrophage accumulation. Circ Res 2004 95 E56 E64. doi: 10.1161/01.RES.0000143013.04985.E7
9. Eitenmüller I, Volger O, Kluge A, Troidl K, Barancik M, Cai WJ, Heil M, Pipp F, Fischer S, Horrevoets AJ, Schmitz-Rixen T, Schaper W, The range of adaptation by collateral vessels after femoral artery occlusion. Circ Res 2006 99 656 662. doi: 10.1161/01.RES.0000242560.77512.dd
10. Chen Z, Rubin J, Tzima E, Role of PECAM-1 in arteriogenesis and specification of preexisting collaterals. Circ Res 2010 107 1355 1363. doi: 10.1161/CIRCRESAHA.110.229955
11. Takeda Y, Costa S, Delamarre E, Macrophage skewing by Phd2 haplodeficiency prevents ischaemia by inducing arteriogenesis. Nature 2011 479 122 126. doi: 10.1038/nature10507
12. Heil M, Schaper W, Influence of mechanical, cellular, and molecular factors on collateral artery growth (arteriogenesis). Circ Res 2004 95 449 458. doi: 10.1161/01.RES.0000141145.78900.44
13. la Sala A, Pontecorvo L, Agresta A, Rosano G, Stabile E, Regulation of collateral blood vessel development by the innate and adaptive immune system. Trends Mol Med 2012 18 494 501. doi: 10.1016/j.molmed.2012.06.007
14. Hardie DG, Carling D, The AMP-Activated protein kinase-fuel gauge of the mammalian cell? Eur J Biochem 1997 246 259 273
15. Hardie DG, Scott JW, Pan DA, Hudson ER, Management of cellular energy by the AMP-Activated protein kinase system. FEBS Lett 2003 546 113 120
16. Hardie DG, AMPK and autophagy get connected. EMBO J 2011 30 634 635. doi: 10.1038/emboj.2011.12
17. Kahn BB, Alquier T, Carling D, Hardie DG, AMP-Activated protein kinase: Ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab 2005 1 15 25. doi: 10.1016/j.cmet.2004.12.003
18. Takano-Ohmuro H, Mukaida M, Kominami E, Morioka K, Autophagy in embryonic erythroid cells: Its role in maturation. Eur J Cell Biol 2000 79 759 764. doi: 10.1078/0171-9335-00096
19. Hardie DG, The AMP-Activated protein kinase pathway-new players upstream and downstream. J Cell Sci 2004 117 pt 23 5479 5487. doi: 10.1242/jcs.01540
20. Hardie DG, AMP-Activated protein kinase: An energy sensor that regulates all aspects of cell function. Genes Dev 2011 25 1895 1908. doi: 10.1101/gad.17420111
21. He C, Zhu H, Li H, Zou MH, Xie Z, Dissociation of bcl-2-beclin1 complex by activated ampk enhances cardiac autophagy and protects against cardiomyocyte apoptosis in diabetes. Diabetes 2013 62 4 1270 1281. doi: 10.2337/db12-0533
22. Zhu H, Foretz M, Xie Z, Zhang M, Zhu Z, Xing J, Leclerc J, Gaudry M, Viollet B, Zou MH, PRKAA1/AMPK1 is required for autophagy-dependent mitochondrial clearance during erythrocyte maturation. Autophagy 2014 10 1522 1534. doi: 10.4161/auto.29197
23. Zhang Y, Lee TS, Kolb EM, Sun K, Lu X, Sladek FM, Kassab GS, Garland T Jr, Shyy JY, AMP-Activated protein kinase is involved in endothelial NO synthase activation in response to shear stress. Arterioscler Thromb Vasc Biol 2006 26 1281 1287. doi: 10.1161/01.ATV.0000221230.08596.98
24. 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
25. Zippel N, Malik RA, Frömel T, Popp R, Bess E, Strilic B, Wettschureck N, Fleming I, Fisslthaler B, Transforming growth factor-β-Activated kinase 1 regulates angiogenesis via AMP-Activated protein kinase-1 and redox balance in endothelial cells. Arterioscler Thromb Vasc Biol 2013 33 2792 2799. doi: 10.1161/ATVBAHA.113.301848
26. Xu MJ, Song P, Shirwany N, Liang B, Xing J, Viollet B, Wang X, Zhu Y, Zou MH, 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. doi: 10.1161/ATVBAHA.111.227991
27. 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
28. Qi D, Young LH, AMPK: Energy sensor and survival mechanism in the ischemic heart. Trends Endocrinol Metab 2015 26 422 429. doi: 10.1016/j.tem.2015.05.010
29. Simons M, Angiogenesis: Where do we stand now? Circulation 2005 111 1556 1566. doi: 10.1161/01.CIR.0000159345.00591.8F
30. Olieslagers S, Pardali E, Tchaikovski V, ten Dijke P, Waltenberger J, TGF-β1/ALK5-induced monocyte migration involves PI3K and p38 pathways and is not negatively affected by diabetes mellitus. Cardiovasc Res 2011 91 510 518. doi: 10.1093/cvr/cvr100
31. van Royen N, Hoefer I, Buschmann I, Heil M, Kostin S, Deindl E, Vogel S, Korff T, Augustin H, Bode C, Piek JJ, Schaper W, Exogenous application of transforming growth factor beta 1 stimulates arteriogenesis in the peripheral circulation. FASEB J 2002 16 432 434. doi: 10.1096/fj.01-0563fje
32. van Royen N, Piek JJ, Schaper W, Fulton WF, A critical review of clinical arteriogenesis research. J Am Coll Cardiol 2009 55 17 25. doi: 10.1016/j.jacc.2009.06.058
33. Cacicedo JM, Yagihashi N, Keaney JF Jr, Ruderman NB, Ido Y, AMPK inhibits fatty acid-induced increases in NF-kappaB transactivation in cultured human umbilical vein endothelial cells. Biochem Biophys Res Commun 2004 324 1204 1209. doi: 10.1016/j.bbrc.2004.09.177
34. Green CJ, Pedersen M, Pedersen BK, Scheele C, Elevated NF-κB activation is conserved in human myocytes cultured from obese type 2 diabetic patients and attenuated by AMP-Activated protein kinase. Diabetes 2011 60 2810 2819. doi: 10.2337/db11-0263
35. Salminen A, Hyttinen JM, Kaarniranta K, AMP-Activated protein kinase inhibits NF-κB signaling and inflammation: Impact on healthspan and lifespan. J Mol Med (Berl) 2011 89 667 676. doi: 10.1007/s00109-011-0748-0
36. Tirziu D, Jaba IM, Yu P, Larrivée B, Coon BG, Cristofaro B, Zhuang ZW, Lanahan AA, Schwartz MA, Eichmann A, Simons M, Endothelial nuclear factor-κB-dependent regulation of arteriogenesis and branching. Circulation 2012 126 2589 2600. doi: 10.1161/CIRCULATIONAHA.112.119321
37. Sweet DT, Chen Z, Givens CS, Owens AP 3rd, Rojas M, Tzima E, Endothelial Shc regulates arteriogenesis through dual control of arterial specification and inflammation via the notch and nuclear factor-κ-light-chain-enhancer of activated B-cell pathways. Circ Res 2013 113 32 39. doi: 10.1161/CIRCRESAHA.113.301407
38. Lähteenvuo JE, Lähteenvuo MT, Kivelä A, Rosenlew C, Falkevall A, Klar J, Heikura T, Rissanen TT, Vähäkangas E, Korpisalo P, Enholm B, Carmeliet P, Alitalo K, Eriksson U, Ylä-Herttuala S, Vascular endothelial growth factor-B induces myocardium-specific angiogenesis and arteriogenesis via vascular endothelial growth factor receptor-1-And neuropilin receptor-1-dependent mechanisms. Circulation 2009 119 845 856. doi: 10.1161/CIRCULATIONAHA.108.816454
39. Liu ZJ, Shirakawa T, Li Y, Soma A, Oka M, Dotto GP, Fairman RM, Velazquez OC, Herlyn M, Regulation of Notch1 and Dll4 by vascular endothelial growth factor in arterial endothelial cells: Implications for modulating arteriogenesis and angiogenesis. Mol Cell Biol 2003 23 14 25
40. Dixit M, Bess E, Fisslthaler B, Härtel FV, Noll T, Busse R, Fleming I, Shear stress-induced activation of the AMP-Activated protein kinase regulates FoxO1a and angiopoietin-2 in endothelial cells. Cardiovasc Res 2008 77 160 168. doi: 10.1093/cvr/cvm017
41. Fisslthaler B, Fleming I, Keserü B, Walsh K, Busse R, Fluid shear stress and NO decrease the activity of the hydroxy-methylglutaryl coenzyme A reductase in endothelial cells via the AMP-Activated protein kinase and FoxO1. Circ Res 2007 100 e12 e21. doi: 10.1161/01.RES.0000257747.74358.1c
42. Chen Z, Peng IC, Cui X, Li YS, Chien S, Shyy JY, Shear stress, SIRT1, and vascular homeostasis. Proc Natl Acad Sci USA 2010 107 10268 10273
43. Bonello S, Zähringer C, BelAiba RS, Djordjevic T, Hess J, Michiels C, Kietzmann T, Görlach A, Reactive oxygen species activate the HIF-1alpha promoter via a functional NFkappaB site. Arterioscler Thromb Vasc Biol 2007 27 755 761. doi: 10.1161/01.ATV.0000258979.92828.bc
44. van Uden P, Kenneth NS, Rocha S, Regulation of hypoxia-inducible factor-1alpha by NF-kappaB. Biochem J 2008 412 477 484. doi: 10.1042/BJ20080476
45. Nizet V, Johnson RS, Interdependence of hypoxic and innate immune responses. Nat Rev Immunol 2009 9 609 617. doi: 10.1038/nri2607