Deletion of BMAL1 in smooth muscle cells protects mice from abdominal aortic aneurysms

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 38, Issue 5, 2018, Pages 1063-1075

  Lutshumba, Jenny ^a   Liu, Shu ^a   Zhong, Yu ^a   Hou, Tianfei ^a   Daugherty, Alan ^a   Lu, Hong ^a   Guo, Zhenheng ^a,b   Gong, Ming C ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b LEXINGTON VA MEDICAL CENTER   (United States)

Author keywords

Abdominal; Aortic aneurysm; ARNTL transcription factor; Metalloproteases; Mice; Mineralocorticoid; Muscle; Receptors; Smooth; Vascular

Indexed keywords

ALDOSTERONE; ANGIOTENSIN II; DEOXYCORTICOSTERONE ACETATE; ELASTIN; MATRIX METALLOPROTEINASE; MESSENGER RNA; MINERALOCORTICOID RECEPTOR; TISSUE INHIBITOR OF METALLOPROTEINASE 4; TRANSCRIPTION FACTOR ARNTL; ARNTL PROTEIN, MOUSE; GELATINASE A; GELATINASE B; MMP2 PROTEIN, MOUSE; MMP9 PROTEIN, MOUSE; TISSUE INHIBITOR OF METALLOPROTEINASE; TISSUE INHIBITOR OF METALLOPROTEINASE-4;

ABDOMINAL AORTA; ABDOMINAL AORTIC ANEURYSM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA; APOPTOSIS; ARTICLE; BLOOD PRESSURE; CIRCADIAN RHYTHM; CONTROLLED STUDY; HYPERCHOLESTEROLEMIA; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; SALT INTAKE; SMOOTH MUSCLE CELL; UPREGULATION; ANIMAL; BINDING SITE; C57BL MOUSE; CHEMICALLY INDUCED; DEFICIENCY; DISEASE MODEL; GENETIC TRANSCRIPTION; GENETICS; KNOCKOUT MOUSE; LESIONS AND DEFECTS; METABOLISM; PATHOLOGY; PROMOTER REGION; VASCULAR SMOOTH MUSCLE;

ALDOSTERONE; ANGIOTENSIN II; ANIMALS; AORTA, ABDOMINAL; AORTIC ANEURYSM, ABDOMINAL; ARNTL TRANSCRIPTION FACTORS; BINDING SITES; DESOXYCORTICOSTERONE ACETATE; DILATATION, PATHOLOGIC; DISEASE MODELS, ANIMAL; ELASTIN; MALE; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PROMOTER REGIONS, GENETIC; SODIUM CHLORIDE, DIETARY; TISSUE INHIBITOR OF METALLOPROTEINASES; TRANSCRIPTION, GENETIC;

EID: 85060487668     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.117.310153     Document Type: Article

References (47)

1. Sakalihasan N, Limet R, Defawe OD. Abdominal aortic aneurysm. Lancet. 2005;365:1577–1589. doi: 10.1016/S0140-6736(05)66459-8.
2. Golledge J, Muller J, Daugherty A, Norman P. Abdominal aortic aneurysm: pathogenesis and implications for management. Arterioscler Thromb Vasc Biol. 2006;26:2605–2613. doi: 10.1161/01. ATV.0000245819.32762.cb.
3. Liu S, Xie Z, Daugherty A, Cassis LA, Pearson KJ, Gong MC, Guo Z. Mineralocorticoid receptor agonists induce mouse aortic aneurysm formation and rupture in the presence of high salt. Arterioscler Thromb Vasc Biol. 2013;33:1568–1579. doi: 10.1161/ATVBAHA.112.300820.
4. Thompson A, Cooper JA, Fabricius M, Humphries SE, Ashton HA, Hafez H. An analysis of drug modulation of abdominal aortic aneurysm growth through 25 years of surveillance. J Vasc Surg. 2010;52:55.e2–61.e2. doi: 10.1016/j.jvs.2010.02.012.
5. Golledge J, Hankey GJ, Yeap BB, Almeida OP, Flicker L, Norman PE. Reported high salt intake is associated with increased prevalence of abdominal aortic aneurysm and larger aortic diameter in older men. PLoS One. 2014;9:e102578. doi: 10.1371/journal.pone.0102578.
6. Green CB, Takahashi JS, Bass J. The meter of metabolism. Cell. 2008;134:728–742. doi: 10.1016/j.cell.2008.08.022.
7. Bunger MK, Wilsbacher LD, Moran SM, Clendenin C, Radcliffe LA, Hogenesch JB, Simon MC, Takahashi JS, Bradfield CA. Mop3 is an essential component of the master circadian pacemaker in mammals. Cell. 2000;103:1009–1017.
8. Mehta RH, Manfredini R, Hassan F, Sechtem U, Bossone E, Oh JK, Cooper JV, Smith DE, Portaluppi F, Penn M, Hutchison S, Nienaber CA, Isselbacher EM, Eagle KA; International Registry of Acute Aortic Dissection (IRAD) Investigators. Chronobiological patterns of acute aortic dissection. Circulation. 2002;106:1110–1115. doi: 10.1161/01. CIR.0000027568.39540.4B.
9. Reilly DF, Westgate EJ, FitzGerald GA. Peripheral circadian clocks in the vasculature. Arterioscler Thromb Vasc Biol. 2007;27:1694–1705. doi: 10.1161/ATVBAHA.107.144923.
10. Anea CB, Zhang M, Stepp DW, Simkins GB, Reed G, Fulton DJ, Rudic RD. Vascular disease in mice with a dysfunctional circadian clock. Circulation. 2009;119:1510–1517. doi: 10.1161/ CIRCULATIONAHA.108.827477.
11. Anea CB, Ali MI, Osmond JM, Sullivan JC, Stepp DW, Merloiu AM, Rudic RD. Matrix metalloproteinase 2 and 9 dysfunction underlie vascular stiffness in circadian clock mutant mice. Arterioscler Thromb Vasc Biol. 2010;30:2535–2543. doi: 10.1161/ATVBAHA.110.214379.
12. Cheng B, Anea CB, Yao L, Chen F, Patel V, Merloiu A, Pati P, Caldwell RW, Fulton DJ, Rudic RD. Tissue-intrinsic dysfunction of circadian clock confers transplant arteriosclerosis. Proc Natl Acad Sci USA. 2011;108:17147–17152. doi: 10.1073/pnas.1112998108.
13. Anea CB, Cheng B, Sharma S, Kumar S, Caldwell RW, Yao L, Ali MI, Merloiu AM, Stepp DW, Black SM, Fulton DJ, Rudic RD. Increased superoxide and endothelial NO synthase uncoupling in blood vessels of Bmal1-knockout mice. Circ Res. 2012;111:1157–1165. doi: 10.1161/ CIRCRESAHA.111.261750.
14. Curci JA. Digging in the “soil” of the aorta to understand the growth of abdominal aortic aneurysms. Vascular. 2009;17(suppl 1):S21–S29.
15. López-Candales A, Holmes DR, Liao S, Scott MJ, Wickline SA, Thompson RW. Decreased vascular smooth muscle cell density in medial degeneration of human abdominal aortic aneurysms. Am J Pathol. 1997;150:993–1007.
16. Humphrey JD, Schwartz MA, Tellides G, Milewicz DM. Role of mech-anotransduction in vascular biology: focus on thoracic aortic aneurysms and dissections. Circ Res. 2015;116:1448–1461. doi: 10.1161/ CIRCRESAHA.114.304936.
17. Storch KF, Paz C, Signorovitch J, Raviola E, Pawlyk B, Li T, Weitz CJ. Intrinsic circadian clock of the mammalian retina: importance for retinal processing of visual information. Cell. 2007;130:730–741. doi: 10.1016/j. cell.2007.06.045.
18. Zhang J, Zhong W, Cui T, Yang M, Hu X, Xu K, Xie C, Xue C, Gibbons GH, Liu C, Li L, Chen YE. Generation of an adult smooth muscle cell-targeted Cre recombinase mouse model. Arterioscler Thromb Vasc Biol. 2006;26:e23–e24. doi: 10.1161/01.ATV.0000202661.61837.93.
19. Xie Z, Su W, Liu S, Zhao G, Esser K, Schroder EA, Lefta M, Stauss HM, Guo Z, Gong MC. Smooth-muscle BMAL1 participates in blood pressure circadian rhythm regulation. J Clin Invest. 2015;125:324–336. doi: 10.1172/JCI76881.
20. Lu H, Howatt DA, Balakrishnan A, Graham MJ, Mullick AE, Daugherty A. Hypercholesterolemia induced by a PCSK9 gain-of-function mutation augments angiotensin II-induced abdominal aortic aneurysms in C57BL/6 mice-brief report. Arterioscler Thromb Vasc Biol. 2016;36:1753–1757. doi: 10.1161/ATVBAHA.116.307613.
21. Toth M, Sohail A, Fridman R. Assessment of gelatinases (MMP-2 and MMP-9) by gelatin zymography. Methods Mol Biol. 2012;878:121–135. doi: 10.1007/978-1-61779-854-2_8.
22. Liu S, Xie Z, Zhao Q, Pang H, Turk J, Calderon L, Su W, Zhao G, Xu H, Gong MC, Guo Z. Smooth muscle-specific expression of calcium-independent phospholipase A2β (iPLA2β) participates in the initiation and early progression of vascular inflammation and neointima formation. J Biol Chem. 2012;287:24739–24753. doi: 10.1074/jbc.M112.340216.
23. Xie Z, Gong MC, Su W, Turk J, Guo Z. Group VIA phospholipase A2 (iPLA2beta) participates in angiotensin II-induced transcriptional upregulation of regulator of g-protein signaling-2 in vascular smooth muscle cells. J Biol Chem. 2007;282:25278–25289. doi: 10.1074/jbc. M611206200.
24. Xie Z, Gong MC, Su W, Xie D, Turk J, Guo Z. Role of calcium-independent phospholipase A2beta in high glucose-induced activation of RhoA, Rho kinase, and CPI-17 in cultured vascular smooth muscle cells and vascular smooth muscle hypercontractility in diabetic animals. J Biol Chem. 2010;285:8628–8638. doi: 10.1074/jbc.M109.057711.
25. Xie Z, Liu D, Liu S, Calderon L, Zhao G, Turk J, Guo Z. Identification of a cAMP-response element in the regulator of G-protein signaling-2 (RGS2) promoter as a key cis-regulatory element for RGS2 transcriptional regulation by angiotensin II in cultured vascular smooth muscles. J Biol Chem. 2011;286:44646–44658. doi: 10.1074/jbc.M111.265462.
26. Su W, Xie Z, Guo Z, Duncan MJ, Lutshumba J, Gong MC. Altered clock gene expression and vascular smooth muscle diurnal contractile variations in type 2 diabetic db/db mice. Am J Physiol Heart Circ Physiol. 2012;302:H621–H633. doi: 10.1152/ajpheart.00825.2011.
27. Krug AW, Allenhöfer L, Monticone R, Spinetti G, Gekle M, Wang M, Lakatta EG. Elevated mineralocorticoid receptor activity in aged rat vascular smooth muscle cells promotes a proin-flammatory phenotype via extracellular signal-regulated kinase ½ mitogen-activated protein kinase and epidermal growth factor receptor-dependent pathways. Hypertension. 2010;55:1476–1483. doi: 10.1161/ HYPERTENSIONAHA.109.148783.
28. McCurley A, Pires PW, Bender SB, Aronovitz M, Zhao MJ, Metzger D, Chambon P, Hill MA, Dorrance AM, Mendelsohn ME, Jaffe IZ. Direct regulation of blood pressure by smooth muscle cell mineralocorticoid receptors. Nat Med. 2012;18:1429–1433. doi: 10.1038/nm.2891.
29. Longo GM, Xiong W, Greiner TC, Zhao Y, Fiotti N, Baxter BT. Matrix metalloproteinases 2 and 9 work in concert to produce aortic aneurysms. J Clin Invest. 2002;110:625–632. doi: 10.1172/JCI15334.
30. Baker AH, Edwards DR, Murphy G. Metalloproteinase inhibitors: biological actions and therapeutic opportunities. J Cell Sci. 2002;115(pt 19):3719–3727.
31. Brew K, Nagase H. The tissue inhibitors of metalloproteinases (TIMPs): an ancient family with structural and functional diversity. Biochim Biophys Acta. 2010;1803:55–71. doi: 10.1016/j.bbamcr.2010.01.003.
32. Steffens S, Winter C, Schloss MJ, Hidalgo A, Weber C, Soehnlein O. Circadian control of inflammatory processes in atherosclerosis and its complications. Arterioscler Thromb Vasc Biol. 2017;37:1022–1028. doi: 10.1161/ATVBAHA.117.309374.
33. Su W, Guo Z, Randall DC, Cassis L, Brown DR, Gong MC. Hypertension and disrupted blood pressure circadian rhythm in type 2 diabetic db/db mice. Am J Physiol Heart Circ Physiol. 2008;295:H1634–H1641. doi: 10.1152/ajpheart.00257.2008.
34. Nernpermpisooth N, Qiu S, Mintz JD, Suvitayavat W, Thirawarapan S, Rudic DR, Fulton DJ, Stepp DW. Obesity alters the peripheral circadian clock in the aorta and microcirculation. Microcirculation. 2015;22:257–266. doi: 10.1111/micc.12192.
35. Chen S, Ding Y, Zhang Z, Wang H, Liu C. Hyperlipidaemia impairs the circadian clock and physiological homeostasis of vascular smooth muscle cells via the suppression of Smarcd1. J Pathol. 2014;233:159–169. doi: 10.1002/path.4338.
36. Lin C, Tang X, Zhu Z, Liao X, Zhao R, Fu W, Chen B, Jiang J, Qian R, Guo D. The rhythmic expression of clock genes attenuated in human plaque-derived vascular smooth muscle cells. Lipids Health Dis. 2014;13:14. doi: 10.1186/1476-511X-13-14.
37. Anea CB, Zhang M, Chen F, Ali MI, Hart CM, Stepp DW, Kovalenkov YO, Merloiu AM, Pati P, Fulton D, Rudic RD. Circadian clock control of Nox4 and reactive oxygen species in the vasculature. PLoS One. 2013;8:e78626. doi: 10.1371/journal.pone.0078626.
38. Yang G, Chen L, Grant GR, Paschos G, Song WL, Musiek ES, Lee V, McLoughlin SC, Grosser T, Cotsarelis G, FitzGerald GA. Timing of expression of the core clock gene Bmal1 influences its effects on aging and survival. Sci Transl Med. 2016;8:324ra16.
39. Eskandari MK, Vijungco JD, Flores A, Borensztajn J, Shively V, Pearce WH. Enhanced abdominal aortic aneurysm in TIMP-1-deficient mice. J Surg Res. 2005;123:289–293. doi: 10.1016/j.jss.2004.07.247.
40. Basu R, Fan D, Kandalam V, Lee J, Das SK, Wang X, Baldwin TA, Oudit GY, Kassiri Z. Loss of Timp3 gene leads to abdominal aortic aneurysm formation in response to angiotensin II. J Biol Chem. 2012;287:44083–44096. doi: 10.1074/jbc.M112.425652.
41. Allaire E, Forough R, Clowes M, Starcher B, Clowes AW. Local overexpression of TIMP-1 prevents aortic aneurysm degeneration and rupture in a rat model. J Clin Invest. 1998;102:1413–1420. doi: 10.1172/JCI2909.
42. Xiong W, Knispel R, Mactaggart J, Baxter BT. Effects of tissue inhibitor of metalloproteinase 2 deficiency on aneurysm formation. J Vasc Surg. 2006;44:1061–1066. doi: 10.1016/j.jvs.2006.06.036.
43. Apte SS, Olsen BR, Murphy G. The gene structure of tissue inhibitor of metalloproteinases (TIMP)-3 and its inhibitory activities define the distinct TIMP gene family. J Biol Chem. 1995;270:14313–14318.
44. Greene J, Wang M, Liu YE, Raymond LA, Rosen C, Shi YE. Molecular cloning and characterization of human tissue inhibitor of metalloproteinase 4. J Biol Chem. 1996;271:30375–30380.
45. Young DA, Phillips BW, Lundy C, Nuttall RK, Hogan A, Schultz GA, Leco KJ, Clark IM, Edwards DR. Identification of an initiator-like element essential for the expression of the tissue inhibitor of metalloproteinases-4 (Timp-4) gene. Biochem J. 2002;364(pt 1):89–99.
46. Dollery CM, McEwan JR, Wang M, Sang QA, Liu YE, Shi YE. TIMP-4 is regulated by vascular injury in rats. Ann NY Acad Sci. 1999;878:740–741.
47. Ketsawatsomkron P, Keen HL, Davis DR, Lu KT, Stump M, De Silva TM, Hilzendeger AM, Grobe JL, Faraci FM, Sigmund CD. Protective role for tissue inhibitor of metalloproteinase-4, a novel peroxisome proliferator-activated receptor-γ target gene, in smooth muscle in deoxycorticosterone acetate-salt hypertension. Hypertension. 2016;67:214–222. doi: 10.1161/ HYPERTENSIONAHA.115.06391.