Reduced EGFR causes abnormal valvular differentiation leading to calcific aortic stenosis and left ventricular hypertrophy in C57BL/6J but not 129S1/SvImJ mice

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 297, Issue 1, 2009, Pages

  Barrick, Cordelia J ^a,b   Roberts, Reade B ^a   Rojas, Mauricio ^a,b   Rajamannan, Nalini M ^c   Suitt, Carolyn B ^b   O'Brien, Kevin D ^d   Smyth, Susan S ^e   Threadgill, David W ^a,b,f  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

^e UNIVERSITY OF KENTUCKY   (United States)

^f NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Aortic stenosis; Epidermal growth factor receptor aortic sclerosis; Hypertrophy; Valvulogenesis

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA STENOSIS; AORTA VALVE DISEASE; ARTERIOSCLEROSIS; ARTERY CALCIFICATION; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; HEART FAILURE; HEART LEFT VENTRICLE HYPERTROPHY; HISTOPATHOLOGY; INFLAMMATORY INFILTRATE; LIFESPAN; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ALLELES; ANIMALS; AORTIC VALVE STENOSIS; BLOOD PRESSURE; CALCINOSIS; ECHOCARDIOGRAPHY; FEMALE; HEART FAILURE; HEART FUNCTION TESTS; HEART VALVES; HYPERTROPHY, LEFT VENTRICULAR; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHENOTYPE; PHOSPHORYLATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SPECIES SPECIFICITY; SURVIVAL;

EID: 67650033075     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00866.2008     Document Type: Article

References (60)

1. Alipour MS, Shah PA. Diagnosis of aortic stenosis in the elderly: role of echocardiography. Am J Geriatr Cardiol 12: 201-206, 2003.
2. Barrick CJ, Rojas M, Schoonhoven R, Smyth SS, Threadgill DW. Cardiac response to pressure overload in 129S1/SvImJ and C57BL/6J mice: temporal- and background-dependent development of concentric left ventricular hypertrophy. Am J Physiol Heart Circ Physiol 292: H2119-H2130, 2007.
3. Barrick CJ, Yu M, Chao HH, Threadgill DW. Chronic pharmacologic inhibition of EGFR leads to cardiac dysfunction in C57BL/6J mice. Toxicol Appl Pharmacol 228: 315-325, 2008.
4. Bonow RO, Carabello B, de Leon AC Jr, Edmunds LH Jr, Fedderly BJ, Freed MD, Gaasch WH, McKay CR, Nishimura RA, O'Gara PT, O'Rourke RA, Rahimtoola SH, Ritchie JL, Cheitlin MD, Eagle KA, Gardner TJ, Garson A Jr, Gibbons RJ, Russell RO, Ryan TJ, Smith SC Jr. Guidelines for the management of patients with valvular heart disease: executive summary. A report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (Committee on Management of Patients with Valvular Heart Disease). Circulation 98: 1949-1984, 1998.
5. Bonow RO, Carabello BA, Kanu C, 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, Faxon DP, 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: a report of the 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): developed in collaboration with the Society of Cardiovascular Anesthesiologists: endorsed by the Society for Cardiovascular Angiography and Interventions and the Society of Thoracic Surgeons. Circulation 114: e84-e231, 2006.
6. Braunwald E. Valvular Heart Disease. New York: McGraw Hill, 1998.
7. Burris HA, 3rd Hurwitz HI, Dees EC, Dowlati A, Blackwell KL, O'Neil B, Marcom PK, Ellis MJ, Overmoyer B, Jones SF, Harris JL, Smith DA, Koch KM, Stead A, Mangum S, Spector NL. Phase I safety, pharmacokinetics, and clinical activity study of lapatinib (GW572016), a reversible dual inhibitor of epidermal growth factor receptor tyrosine kinases, in heavily pretreated patients with metastatic carcinomas. J Clin Oncol 23: 5305-5313, 2005.
8. Caira FC, Stock SR, Gleason TG, McGee EC, Huang J, Bonow RO, Spelsberg TC, McCarthy PM, Rahimtoola SH, Rajamannan NM. Human degenerative valve disease is associated with up-regulation of low-density lipoprotein receptor-related protein 5 receptor-mediated bone formation. J Am Coll Cardiol 47: 1707-1712, 2006.
9. Carlson FL. Histotechnology: A Self-Instructional Text. Chicago: ASCP Press, 1990.
10. Chen B, Bronson RT, Klaman LD, Hampton TG, Wang JF, Green PJ, Magnuson T, Douglas PS, Morgan JP, Neel BG. Mice mutant for Egfr and Shp2 have defective cardiac semilunar valvulogenesis. Nat Genet 24: 296-299, 2000.
11. Cripe L, Andelfinger G, Martin LJ, Shooner K, Benson DW. Bicuspid aortic valve is heritable. J Am Coll Cardiol 44: 138-143, 2004.
12. de la Pompa JL, Timmerman LA, Takimoto H, Yoshida H, Elia AJ, Samper E, Potter J, Wakeham A, Marengere L, Langille BL, Crabtree GR, Mak TW. Role of the NF-ATc transcription factor in morphogenesis of cardiac valves and septum. Nature 392: 182-186, 1998.
13. Delot EC. Control of endocardial cushion and cardiac valve maturation by BMP signaling pathways. Mol Genet Metab 80: 27-35, 2003.
14. Delot EC, Bahamonde ME, Zhao M, Lyons KM. BMP signaling is required for septation of the outflow tract of the mammalian heart. Development 130: 209-220, 2003.
15. Drolet MC, Roussel E, Deshaies Y, Couet J, Arsenault M. A high fat/high carbohydrate diet induces aortic valve disease in C57BL/6J mice. J Am Coll Cardiol 47: 850-855, 2006.
16. Feit LR. Genetics of congenital heart disease: strategies. Adv Pediatr 45: 267-292, 1998.
17. Garg V. Molecular genetics of aortic valve disease. Curr Opin Cardiol 21: 180-184, 2006.
18. Garg V, Muth AN, Ransom JF, Schluterman MK, Barnes R, King IN, Grossfeld PD, Srivastava D. Mutations in NOTCH1 cause aortic valve disease. Nature 437: 270-274, 2005.
19. Grazette LP, Boecker W, Matsui T, Semigran M, Force TL, Hajjar RJ, Rosenzweig A. Inhibition of ErbB2 causes mitochondrial dysfunction in cardiomyocytes: implications for herceptin-induced cardiomyopathy. J Am Coll Cardiol 44: 2231-2238, 2004.
20. Hagaman JR, John S, Xu L, Smithies O, Maeda N. An improved technique for tail-cuff blood pressure measurements with dark-tailed mice. Contemp Top Lab Anim Sci 44: 43-46, 2005.
21. Iivanainen AM, Lindroos M, Tilvis R, Heikkila J, Kupari M. Calcific degeneration of the aortic valve in old age: is the development of flow obstruction predictable? J Intern Med 239: 269-273, 1996.
22. Iivanainen AM, Lindroos M, Tilvis R, Heikkila J, Kupari M. Natural history of aortic valve stenosis of varying severity in the elderly. Am J Cardiol 78: 97-101, 1996.
23. Ishimori N, Li R, Kelmenson PM, Korstanje R, Walsh KA, Churchill GA, Forsman-Semb K, Paigen B. Quantitative trait loci analysis for plasma HDL-cholesterol concentrations and atherosclerosis susceptibility between inbred mouse strains C57BL/6J and 129S1/SvImJ. Arterioscler Thromb Vasc Biol 24: 161-166, 2004.
24. Iwamoto R, Yamazaki S, Asakura M, Takashima S, Hasuwa H, Miyado K, Adachi S, Kitakaze M, Hashimoto K, Raab G, Nanba D, Higashiyama S, Hori M, Klagsbrun M, Mekada E. Heparin-binding EGF-like growth factor and ErbB signaling is essential for heart function. Proc Natl Acad Sci USA 100: 3221-3226, 2003.
25. Jackson LF, Qiu TH, Sunnarborg SW, Chang A, Zhang C, Patterson C, Lee DC. Defective valvulogenesis in HB-EGF and TACE-null mice is associated with aberrant BMP signaling. EMBO J 22: 2704-2716, 2003.
26. Junker R, Kotthoff S, Vielhaber H, Halimeh S, Kosch A, Koch HG, Kassenbohmer R, Heineking B, Nowak-Gottl U. Infant methylenetetrahydrofolate reductase 677TT genotype is a risk factor for congenital heart disease. Cardiovasc Res 51: 251-254, 2001.
27. Knez I, Renner W, Maier R, Rehak P, Rienmuller R, Pilsl M, Stanger O, Mircic A, Dacar D, Szalay Z, Martinovic I, Vogt PR, Rigler B. Angiotensin-converting enzyme polymorphisms and their potential impact on left ventricular myocardial geometry after aortic valve surgery. J Heart Valve Dis 12: 687-695, 2003.
28. Kokubo H, Miyagawa-Tomita S, Tomimatsu H, Nakashima Y, Nakazawa M, Saga Y, Johnson RL. Targeted disruption of hesr2 results in atrioventricular valve anomalies that lead to heart dysfunction. Circ Res 95: 540-547, 2004.
29. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2[-Delta Delta C(T)] method. Methods 25: 402-408, 2001.
30. Luetteke NC, Phillips HK, Qiu TH, Copeland NG, Earp HS, Jenkins NA, Lee DC. The mouse waved-2 phenotype results from a point mutation in the EGF receptor tyrosine kinase. Genes Dev 8: 399-413, 1994.
31. Mohler ER, 3rd Chawla MK, Chang AW, Vyavahare N, Levy RJ, Graham L, Gannon FH. Identification and characterization of calcifying valve cells from human and canine aortic valves. J Heart Valve Dis 8: 254-260, 1999.
32. Mrosovsky N, Redlin U, Roberts RB, Threadgill DW. Masking in waved-2 mice: EGF receptor control of locomotion questioned. Chronobiol Int 22: 963-974, 2005.
33. Nair BG, Patel TB. Regulation of cardiac adenylyl cyclase by epidermal growth factor (EGF). Role of EGF receptor protein tyrosine kinase activity. Biochem Pharmacol 46: 1239-1245, 1993.
34. Nair BG, Rashed HM, Patel TB. Epidermal growth factor produces inotropic and chronotropic effects in rat hearts by increasing cyclic AMP accumulation. Growth Factors 8: 41-48, 1993.
35. Noma T, Lemaire A, Naga Prasad SV, Barki-Harrington L, Tilley DG, Chen J, Le Corvoisier P, Violin JD, Wei H, Lefkowitz RJ, Rockman HA. Beta-arrestin-mediated beta1-adrenergic receptor transactivation of the EGFR confers cardioprotection. J Clin Invest 117: 2445-2458, 2007.
36. Novaro GM, Sachar R, Pearce GL, Sprecher DL, Griffin BP. Association between apolipoprotein E alleles and calcific valvular heart disease. Circulation 108: 1804-1808, 2003.
37. O'Brien KD. Pathogenesis of calcific aortic valve disease: a disease process comes of age (and a good deal more). Arterioscler Thromb Vasc Biol 26: 1721-1728, 2006.
38. O'Brien KD, Kuusisto J, Reichenbach DD, Ferguson M, Giachelli C, Alpers CE, Otto CM. Osteopontin is expressed in human aortic valvular lesions. Circulation 92: 2163-2168, 1995.
39. 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.
40. O'Brien KE, O'Bryan CL, Saad R. Predictors of outcome in asymptomatic aortic stenosis. N Engl J Med 344: 227-228; author reply 228-229, 2001.
41. Orlowska-Baranowska E, Placha G, Gaciong Z, Baranowski R, Zakrzewski D, Michalek P, Hoffman P, Rawczynska-Englert I. Influence of ACE I/D genotypes on left ventricular hypertrophy in aortic stenosis: gender-related differences. J Heart Valve Dis 13: 574-581, 2004.
42. Ortlepp JR, Hoffmann R, Ohme F, Lauscher J, Bleckmann F, Hanrath P. The vitamin D receptor genotype predisposes to the development of calcific aortic valve stenosis. Heart 85: 635-638, 2001.
43. Otto CM, Kuusisto J, Reichenbach DD, Gown AM, O'Brien KD. Characterization of the early lesion of 'degenerative' valvular aortic stenosis. Histological and immunohistochemical studies. Circulation 90: 844-853, 1994.
44. Pareja M, Sanchez O, Lorita J, Soley M, Ramirez I. Activated epidermal growth factor receptor (ErbB1) protects the heart against stress-induced injury in mice. Am J Physiol Regul Integr Comp Physiol 285: R455-R462, 2003.
45. Peter M, Hoffmann A, Parker C, Luscher T, Burckhardt D. Progression of aortic stenosis. Role of age and concomitant coronary artery disease. Chest 103: 1715-1719, 1993.
46. Rajagopalan V, Zucker IH, Jones JA, Carlson M, Ma YJ. Cardiac ErbB-1/ErbB-2 mutant expression in young adult mice leads to cardiac dysfunction. Am J Physiol Heart Circ Physiol 295: H543-H554, 2008.
47. Rajamannan NM. Calcific aortic stenosis: a disease ready for prime time. Circulation 114: 2007-2009, 2006.
48. Rajamannan NM. Calcific aortic stenosis: medical and surgical management in the elderly. Curr Treat Options Cardiovasc Med 7: 437-442, 2005.
49. Rajamannan NM. Is it time for medical therapy for aortic valve disease? Expert Rev Cardiovasc Ther 2: 845-854, 2004.
50. Rajamannan NM, Gersh B, Bonow RO. Calcific aortic stenosis: from bench to the bedside: emerging clinical and cellular concepts. Heart 89: 801-805, 2003.
51. Rajamannan NM, Otto CM. Targeted therapy to prevent progression of calcific aortic stenosis. Circulation 110: 1180-1182, 2004.
52. 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.
53. Rivera-Feliciano J, Lee KH, Kong SW, Rajagopal S, Ma Q, Springer Z, Izumo S, Tabin CJ, Pu WT. Development of heart valves requires Gata4 expression in endothelial-derived cells. Development 133: 3607-3618, 2006.
54. Sibilia M, Wagner B, Hoebertz A, Elliott C, Marino S, Jochum W, Wagner EF. Mice humanised for the EGF receptor display hypomorphic phenotypes in skin, bone and heart. Development 130: 4515-4525, 2003.
55. Sibilia M, Wagner EF. Strain-dependent epithelial defects in mice lacking the EGF receptor. Science 269: 234-238, 1995.
56. Stewart BF, Siscovick D, Lind BK, Gardin JM, Gottdiener JS, Smith VE, Kitzman DW, Otto CM. Clinical factors associated with calcific aortic valve disease. Cardiovascular Health Study. J Am Coll Cardiol 29: 630-634, 1997.
57. Strunk KE, Amann V, Threadgill DW. Phenotypic variation resulting from a deficiency of epidermal growth factor receptor in mice is caused by extensive genetic heterogeneity that can be genetically and molecularly partitioned. Genetics 167: 1821-1832, 2004.
58. Threadgill DW, Dlugosz AA, Hansen LA, Tennenbaum T, Lichti U, Yee D, LaMantia C, Mourton T, Herrup K, Harris RC, et al. Targeted disruption of mouse EGF receptor: effect of genetic background on mutant phenotype. Science 269: 230-234, 1995.
59. Weiss RM, Ohashi M, Miller JD, Young SG, Heistad DD. Calcific aortic valve stenosis in old hypercholesterolemic mice. Circulation 114: 2065-2069, 2006.
60. Zhou HM, Weskamp G, Chesneau V, Sahin U, Vortkamp A, Horiuchi K, Chiusaroli R, Hahn R, Wilkes D, Fisher P, Baron R, Manova K, Basson CT, Hempstead B, Blobel CP. Essential role for ADAM19 in cardiovascular morphogenesis. Mol Cell Biol 24: 96-104, 2004.