Discovery of shear-and side-specific mRNAs and miRNAs in human aortic valvular endothelial cells

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 301, Issue 3, 2011, Pages

  Holliday, Casey J ^a   Ankeny, Randall F ^a   Jo, Hanjoong ^a,b,c   Nerem, Robert M ^a  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Ewha Womans University   (South Korea)

Author keywords

Aortic valve; Endothelium; Microarray; MicroRNA; Shear stress

Indexed keywords

I KAPPA B ALPHA; MESSENGER RNA; MICRORNA; THROMBOSPONDIN 1;

AORTA VALVE; ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; SHEAR STRESS; SIGNAL TRANSDUCTION;

AORTIC VALVE; CELLS, CULTURED; ENDOTHELIAL CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; GENETIC MARKERS; HEMODYNAMICS; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MICRORNAS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYMERASE CHAIN REACTION; REGIONAL BLOOD FLOW; REPRODUCIBILITY OF RESULTS; STRESS, MECHANICAL; TIME FACTORS;

EID: 80052329754     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00117.2011     Document Type: Article

References (53)

1. American College of Cardiology; American Heart Association Task Force on Practice Guidelines (Writing Committee to revise the 1998 guidelines for the management of patients with valvular heart disease); Society of Cardiovascular Anesthesiologists, Bonow RO, Carabello BA, Chatterjee K, de Leon AC Jr, Faxon DP, Freed MD, Gaasch WH, Lytle BW, Nishimura RA, O'Gara PT, O'Rourke RA, Otto CM, Shah PM, Shanewise JS, Smith SC Jr, Jacobs AK, Adams CD, Anderson JL, Antman EM, Fuster V, Halperin JL, Hiratzka LF, Hunt SA, Lytle BW, Nishimura R, Page RL, Riegel B. ACC/AHA 2006 guidelines for the management of patients with valvular heart disease. Circulation 114: E84-E231, 2006.
2. Ando H, Kubin T, Schaper W, Schaper J. Cardiac microvascular endothelial cells express α-smooth muscle actin and show low NOSIII activity. Am J Physiol Heart Circ Physiol 276: H1755-H1768, 1999.
3. Bosse Y, Mathieu P, Pibarot P. Genomics: the next step to elucidate the etiology of calcific aortic valve stenosis. J Am Coll Cardiol 51: 1327-1336, 2008.
4. Bosse Y, Miqdad A, Fournier D, Pepin A, Pibarot P, Mathieu P. Refining molecular pathways leading to calcific aortic valve stenosis by studying gene expression profile of normal and calcified stenotic human aortic valves. Circ Cardiovasc Genet 2: 489-498, 2009.
5. Butcher JT, Penrod AM, Garcia AJ, Nerem RM. Unique morphology and focal adhesion development of valvular endothelial cells in static and fluid flow environments. Arterioscler Thromb Vasc Biol 24: 1429-1434, 2004.
6. Castilla MA, Moreno-Bueno G, Romero-Perez L, Van De Vijver K, Biscuola M, Lopez-Garcia MA, Prat J, Matias-Guiu X, Cano A, Oliva E, Palacios J. Micro-RNA signature of the epithelial-mesenchymal transition in endometrial carcinosarcoma. J Pathol 223: 72-80, 2011.
7. Chan KL, Teo K, Dumesnil JG, Ni A, Tam J; ASTRONOMER Investigators. Effect of lipid lowering with rosuvastatin on progression of aortic stenosis: results of the Aortic Stenosis Progression Observation: Measuring Effects of Rosuvastatin (ASTRONOMER) trial. Circulation 121: 306-314, 2010.
8. Cheng AM, Byrom MW, Shelton J, Ford LP. Antisense inhibition of human miRNAs and indications for an involvement of miRNA in cell growth and apoptosis. Nucleic Acids Res 33: 1290-1297, 2005.
9. Conway DE, Williams Marcie R, Eskin Suzanne G, McIntire Larry V. Endothelial cell responses to atheroprone flow are driven by two separate flow components: low time-average shear stress and fluid flow reversal. Am J Physiol Heart Circ Physiol 298: H367-H374, 2010.
10. Dimmeler S, Zeiher AM. Circulating microRNAs: novel biomarkers for cardiovascular diseases? Eur Heart J 31: 2705-2707, 2010.
11. Fang Y, Shi CZ, Manduchi E, Civelek M, Davies PF. MicroRNA-10a regulation of proinflammatory phenotype in athero-susceptible endothelium in vivo and in vitro. Proc Natl Acad Sci USA 107: 13450-13455, 2010.
12. Georges SA, Biery MC, Kim SY, Schelter JM, Guo J, Chang AN, Jackson AL, Carleton MO, Linsley PS, Cleary MA, Chau BN. Coordinated regulation of cell cycle Transcripts by p53-inducible microRNAs, miR-192 and miR-215. Cancer Res 68: 10105-10112, 2008.
13. Guo HL, Ingolia NT, Weissman JS, Bartel DP. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466: 835-846, 2010.
14. Helske S, Lindstedt KA, Laine M, Mayranpaa M, Werkkala K, Lommi J, Turto H, Kupari M, Kovanen PT. Induction of local angiotensin II-producing systems in stenotic aortic valves. J Am Coll Cardiol 44: 1859-1866, 2004.
15. Ishisaki A, Hiyashi H, Li AJ, Imamura T. Human umbilical vein endothelium-derived cells retain potential to differentiate into smooth muscle-like cells. J Biol Chem 278: 1303-1309, 2003.
16. Kaden JJ, Dempfle CE, Grobholz R, Fischer CS, Vocke DC, Kilic R, Sarikoc A, Pinol R, Hagl S, Lang S, Brueckmann M, Borggrefe M. Inflammatory regulation of extracellular matrix remodeling in calcific aortic valve stenosis. Cardiovasc Pathol 14: 80-87, 2005.
17. Kaden JJ, Dempfle CE, Grobholz R, Tran HT, Kilic R, Sarikoc A, Brueckmann M, Vahl C, Hagl S, Haase KK, Borggrefe M. Interleukin-1β promotes matrix metalloproteinase expression and cell proliferation in calcific aortic valve stenosis. Atherosclerosis 170: 205-211, 2003.
18. Levesque MJ, Nerem RM. The elongation and orientation of cultured endothelial cells in response to shear stress. J Biomech Eng 107: 341-347, 1985.
19. Li XX, Stark GR. NFκB-dependent signaling pathways. Exp Hematol 30: 285-296, 2002.
20. Lin MS, Chen WC, Huang JX, Gao HJ, Ye YL, Song ZY, Shen XY. MicroRNA expression profiles in human colorectal cancers with liver metastases. Oncol Rep 25: 739-747, 2011.
21. Lloyd-Jones D, Adams RJ, Brown TM, Carnethon M, Dai S, De Simone G, Ferguson TB, Ford E, Furie K, Gillespie C, Go A, Greenlund K, Haase N, Hailpern S, Ho PM, Howard V, Kissela B, Kittner S, Lackland D, Lisabeth L, Marelli A, McDermott MM, Meigs J, Mozaffarian D, Mussolino M, Nichol G, Roger VL, Rosamond W, Sacco R, Sorlie P, Roger VL, Thom T, Wasserthiel-Smoller S, Wong ND, Wylie-Rosett J; American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart disease and stroke statistics-2010 update: a report from the American Heart Association. Circulation 121: E46-E215, 2010.
22. Medici D, Shore EM, Lounev VY, Kaplan FS, Kalluri R, Olsen BR. Conversion of vascular endothelial cells into multipotent stem-like cells. Nat Med 16: 1400-1406, 2010.
23. Mirochnik Y, Kwiatek A, Volpert OV. Thrombospondin and apoptosis: molecular mechanisms and use for design of complementation treatments. Curr Drug Targets 9: 851-862, 2008.
24. Mohler ER. Mechanisms of aortic valve calcification. Am J Cardiol 94: 1396-1402, 2004.
25. Moschos SA, Williams AE, Perry MM, Birrell MA, Belvisi MG, Lindsay MA. Expression profiling in vivo demonstrates rapid changes in lung microRNA levels following lipopolysaccharide-induced inflammation but not in the anti-inflammatory action of glucocorticoids. BMC Genomics 8: 240, 2007.
26. Mowbray AL, Kang DH, Rhee SG, Kang SW, Jo H. Laminar shear stress up-regulates peroxiredoxins (PRX) in endothelial cells. J Biol Chem 283: 1622-1627, 2008.
27. Navon R, Wang H, Steinfeld I, Tsalenko A, Ben-Dor A, Yakhini Z. Novel rank-based statistical methods reveal micrornas with differential expression in multiple cancer types. PLos One 4: e8003, 2009.
28. Ni CW, Qiu H, Jo H. MicroRNA-663 upregulated by oscillatory shear stress plays a role in inflammatory response of endothelial cells. Am J Physiol Heart Circ Physiol 300: H1762-H1769, 2011.
29. Ni CW, Qiu Haiwei Rezvan Amir Kwon Kihwan Nam Douglas Son Dong Ju Visvader Jane E, Jo Hanjoong. Discovery of novel mechanosensitive genes in vivo using mouse carotid artery endothelium exposed to disturbed flow. Blood 116: E66-E73, 2010.
30. Nigam V, Sievers HH, Jensen BC, Sier HA, Simpson PC, Srivastava D, Mohamed SA. Altered microRNAs in bicuspid aortic valve: a comparison between stenotic and insufficient valves. J Heart Valve Dis 19: 459-465, 2010.
31. Nikiforova MN, Tseng GC, Steward D, Diorio D, Nikiforov YE. MicroRNA expression profiling of thyroid tumors: biological significance and diagnostic utility. J Clin Endocrinol Metab 93: 1600-1608, 2008.
32. Novo G, Fazio G, Visconti C, Carita P, Maira E, Fattouch K, Novo S. Atherosclerosis, degenerative aortic stenosis and statins. Curr Drug Targets 12: 115-121, 2011.
33. O'Brien KD, Reichenbach DD, Marcovina SM, Kuusisto J, Alpers CE, Otto CM. Apolipoproteins B, (a), and E accumulate in the morphologically early lesion of "degenerative" valvular aortic stenosis. Arterioscler Thromb Vasc Biol 16: 523-532, 1996.
34. Olsson M, Thyberg J, Nilsson J. Presence of oxidized low density lipoprotein in nonrheumatic stenotic aortic valves. Arterioscler Thromb Vasc Biol 19: 1218-1222, 1999.
35. Otto CM, Kuusisto J, Reichenbach DD, Gown AM, Obrien KD. Characterization of the early lesion of degenerative valvular aortic-stenosis-histological and immunohistochemical studies. Circulation 90: 844-853, 1994.
36. Padovani AM, Molina MF, Mann KK. Inhibition of liver X receptor/ retinoid X receptor-mediated transcription contributes to the proatherogenic effects of arsenic in macrophages in vitro. Arterioscler Thromb Vasc Biol 30: 1228-1236, 2010.
37. Papadaki M, Eskin SG. Effects of fluid shear stress on gene regulation of vascular cells. Biotechnol Prog 13: 209-221, 1997.
38. Paranya G, Vineberg S, Dvorin E, Kaushal S, Roth SJ, Rabkin E, Schoen FJ, Bischoff J. Aortic valve endothelial cells undergo transforming growth factor-β-mediated and non-transforming growth factor-β-mediated transdifferentiation in vitro. Am J Pathol 159: 1335-1343, 2001.
39. Qin XM, Wang XH, Wang Y, Tang ZH, Cui QH, Xi JZ, Li YSJ, Chien S, Wang NP. MicroRNA-19a mediates the suppressive effect of laminar flow on cyclin D1 expression in human umbilical vein endothelial cells. Proc Natl Acad Sci USA 107: 3240-3244, 2010.
40. Rajamannan NM, Subramaniam M, Rickard D, Stock SR, Donovan J, Springett M, Orszulak T, Fullerton DA, Tajik AJ, Bonow RO, Spelsberg T. Human aortic valve calcification is associated with an osteoblast phenotype. Circulation 107: 2181-2184, 2003.
41. Roberts WC, Ko JM. Frequency by decades of unicuspid, bicuspid, and tricuspid aortic valves in adults having isolated aortic valve replacement for aortic stenosis, with or without associated aortic regurgitation. Circulation 111: 920-925, 2005.
42. Rossebo AB, Pedersen TR, Allen C, Boman K, Chambers J, Egstrup K, Gerdts E, Gohlke-Barwolf C, Holme I, Kesaniemi VAY, Malbecq W, Nienaber C, Ray S, Skjaerpe T, Wachtell K, Willenheimer R. Design and baseline characteristics of the simvastatin and ezetimibe in aortic stenosis (SEAS) study. Am J Cardiol 99: 970-973, 2007.
43. Salloum FN, Chau VQ, Hoke NN, Abbate A, Varma A, Ockaili RA, Toldo S, Kukreja RC. Phosphodiesterase-5 inhibitor, tadalafil, protects against myocardial ischemia/reperfusion through protein-kinase G-dependent generation of hydrogen sulfide. Circulation 120: S31-S36, 2009.
44. Schmitz KJ, Helwig J, Bertram S, Sheu SY, Suttorp AC, Seggewiß J, Willscher E, Walz MK, Worm K, Schmid KW. Differential expression of microRNA-675, microRNA-139-3p and microRNA-335 in benign and malignant adrenocortical tumours. J Clin Pathol 64: 529-535, 2011.
45. Simmons CA, Grant GR, Manduchi E, Davies PF. Spatial heterogeneity of endothelial phenotypes correlates with side-specific vulnerability to calcification in normal porcine aortic valves. Circ Res 96: 792-799, 2005.
46. Song B, Wang Y, Kudo K, Gavin EJ, Xi YG, Ju JF. miR-192 regulates dihydrofolate reductase and cellular proliferation through the p53-microRNA circuit. Clin Cancer Res 14: 8080-8086, 2008.
47. Sucosky P, Balachandran K, Elhammali A, Jo H, Yoganathan AP. Altered shear stress stimulates upregulation of endothelial VCAM-1 and ICAM-1 in a BMP-4-and TGF-β1-dependent pathway. Arterioscler Thromb Vasc Biol 29: 254-260, 2009.
48. Thiene G, Basso C. Pathology and pathogenesis of infective endocarditis in native heart valves. Cardiovasc Pathol 15: 256-263, 2006.
49. Tombol Z, Eder K, Kovacs A, Szabo PM, Kulka J, Liko I, Zalatnai A, Racz G, Toth M, Patocs A, Falus A, Racz K, Igaz P. MicroRNA expression profiling in benign (sporadic and hereditary) and recurring adrenal pheochromocytomas. Mod Pathol 23: 1583-1595, 2010.
50. van Rooij E, Marshall WS, Olson EN. Toward microRNA-based therapeutics for heart disease. The sense in antisense. Circ Res 103: 919-928, 2008.
51. Wang KC, Garmire LX, Young A, Nguyen P, Trinh A, Subramaniam S, Wang NP, Shyy JYJ, Li YS, Chien S. Role of microRNA-23b in flow-regulation of Rb phosphorylation and endothelial cell growth. Proc Natl Acad Sci USA 107: 3234-3239, 2010.
52. Weinberg EJ, Mack PJ, Schoen FJ, Garcia-Cardena G, Mofrad MRK. Hemodynamic environments from opposing sides of human aortic valve leaflets evoke distinct endothelial phenotypes in vitro. Cardiovasc Eng 10: 5-11, 2010.
53. Zhang J, Zhang F, Didelot X, Bruce KD, Cagampang FR, Vatish M, Hanson M, Lehnert H, Ceriello A, Byrne CD. Maternal high fat diet during pregnancy and lactation alters hepatic expression of insulin like growth factor-2 and key microRNAs in the adult offspring. BMC Genomics 10: 478, 2009.