Silencing of the Drosophila ortholog of SOX5 in heart leads to cardiac dysfunction as detected by optical coherence tomography

Human Molecular Genetics

Volumn 22, Issue 18, 2013, Pages 3798-3806

  Li, Airong ^a   Ahsen, Osman O ^c   Liu, Jonathan J ^c   Du, Chuang ^d   McKee, Mary L ^b   Yang, Yan ^a   Wasco, Wilma ^a   Newton Cheh, Christopher H ^b   O'Donnell, Christopher J ^e   Fujimoto, James G ^c   Zhou, Chao ^c,f   Tanzi, Rudolph E ^a  

^a Department of Neurology   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c Department of Electrical Engineering and Computer Science   (United States)

^d TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e and Blood Institute   (United States)

^f Lehigh University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR SOX5;

ARTICLE; DROSOPHILA; GENE SILENCING; HEART CYCLE; HEART DISEASE; HEART FUNCTION; HEART RATE; HEART VENTRICLE WALL; MUSCLE FIBRIL; NONHUMAN; OPTICAL COHERENCE TOMOGRAPHY; PRIORITY JOURNAL; WNT SIGNALING PATHWAY;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DROSOPHILA; DROSOPHILA PROTEINS; GENE SILENCING; HEART; HUMANS; IMAGING, THREE-DIMENSIONAL; MYOCARDIUM; MYOFIBRILS; SOX TRANSCRIPTION FACTORS; SOXD TRANSCRIPTION FACTORS; TOMOGRAPHY, OPTICAL COHERENCE; WING; WNT PROTEINS;

EID: 84881539014     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt230     Document Type: Article

References (81)

1. Remenyi, A., Lins, K., Nissen, L.J., Reinbold, R., Scholer, H.R. and Wilmanns, M. (2003) Crystal structure of a POU/HMG/DNA ternary complex suggests differential assembly of Oct4 and Sox2 on two enhancers. Genes Dev., 17, 2048-2059.
2. Wunderle, V.M., Critcher, R., Ashworth, A. and Goodfellow, P.N. (1996) Cloning and characterization of SOX5, a new member of the human SOX gene family. Genomics, 36, 354-358.
3. Smits, P., Li, P., Mandel, J., Zhang, Z., Deng, J.M., Behringer, R.R., de Crombrugghe, B. and Lefebvre, V. (2001) The transcription factors L-Sox5 and Sox6 are essential for cartilage formation. Dev. Cell, 1, 277-290.
4. Shim, S., Kwan, K.Y., Li, M., Lefebvre, V. and Sestan, N. (2012) Cis-regulatory control of corticospinal system development and evolution. Nature, 486, 74-79.
5. Martinez-Morales, P.L., Quiroga, A.C., Barbas, J.A. and Morales, A.V. (2010) SOX5 controls cell cycle progression in neural progenitors by interfering with the WNT-beta-catenin pathway. EMBORep., 11, 466-472.
6. Eijgelsheim, M., Newton-Cheh, C., Sotoodehnia, N., de Bakker, P.I., Muller, M., Morrison, A.C., Smith, A.V., Isaacs, A., Sanna, S., Dorr, M. et al. (2010) Genome-wide association analysis identifies multiple loci related to resting heart rate. Hum. Mol. Genet., 19, 3885-3894.
7. Pfeufer, A., vanNoord, C.,Marciante, K.D.,Arking, D.E.,Larson, M.G., Smith, A.V., Tarasov, K.V., Muller, M., Sotoodehnia, N., Sinner, M.F. et al. (2010) Genome-wide association study of PR interval. Nat. Genet., 42, 153-159.
8. Olesen, M.S., Holst, A.G., Jabbari, J., Nielsen, J.B., Christophersen, I.E., Sajadieh, A., Haunso, S. and Svendsen, J.H. (2012) Genetic loci on chromosomes 4q25, 7p31 and 12p12 are associated with onset of lone atrial fibrillation before the age of 40 years. Can. J. Cardiol., 28, 191-195.
9. Della-Morte, D., Beecham, A., Rundek, T., Wang, L., McClendon, M.S., Slifer, S., Blanton, S.H., Di Tullio, M.R. and Sacco, R.L. (2011)Afollow-up study for left ventricular mass on chromosome 12p11 identifies potential candidate genes. BMC Med. Genet., 12, 100.
10. Hersh, C.P., Silverman, E.K., Gascon, J., Bhattacharya, S., Klanderman, B.J., Litonjua, A.A., Lefebvre, V., Sparrow, D., Reilly, J.J. Anderson, W.H. et al. (2011) SOX5 is a candidate gene for chronic obstructive pulmonary disease susceptibility and is necessary for lung development. Am. J. Respir. Crit. Care Med., 183, 1482-1489.
11. Ocorr, K., Reeves, N.L., Wessells, R.J., Fink, M., Chen, H.S., Akasaka, T., Yasuda, S., Metzger, J.M., Giles, W., Posakony, J.W. et al. (2007) KCNQ potassium channel mutations cause cardiac arrhythmias in Drosophila that mimic the effects of aging. Proc. Natl Acad. Sci. USA, 104, 3943-3948.
12. Vigoreaux, J.O. (2001) Genetics of the Drosophila flight muscle myofibril: a window into the biology of complex systems. Bioessays, 23, 1047-1063.
13. Paternostro, G., Vignola, C., Bartsch, D.U., Omens, J.H., McCulloch, A.D. and Reed, J.C. (2001) Age-associated cardiac dysfunction in Drosophila melanogaster. Circ. Res., 88, 1053-1058.
14. Curtis, N.J., Ringo, J.M. and Dowse, H.B. (1999) Morphology of the pupal heart, adult heart and associated tissues in the fruit fly, Drosophila melanogaster. J. Morphol., 240, 225-235.
15. Nishimura, M., Ocorr, K., Bodmer, R. and Cartry, J. (2011) Drosophila as a model to study cardiac aging. Exp. Gerontol., 46, 326-330.
16. Huang, D., Swanson, E.A., Lin, C.P., Schuman, J.S., Stinson, W.G., Chang, W., Hee, M.R., Flotte, T., Gregory, K., Puliafito, C.A. et al. (1991) Optical coherence tomography. Science, 254, 1178-1181.
17. Drexler, W., Morgner, U., Ghanta, R.K., Kärtner, F.X., Schuman, J.S. and Fujimoto, J.G. (2001) Ultrahigh-resolution ophthalmic optical coherence tomography. Nat. Med., 7, 502-507.
18. Sakata, L.M., DeLeon-Ortega, J., Sakata, V. and Girkin, C.A. (2009) Optical coherence tomography of the retina and optic nerve -a review. Clin. Exp. Ophthalmol., 37, 90-99.
19. Geitzenauer, W., Hitzenberger, C.K. and Schmidt-Erfurth, U.M. (2011) Retinal optical coherence tomography: past, present and future perspectives. Br. J. Ophthalmol., 95, 171-177.
20. Tearney, G.J., Brezinski, M.E., Bouma, B.E., Boppart, S.A., Pitvis, C., Southern, J.F. and Fujimoto, J.G. (1997) In vivo endoscopic optical biopsy with optical coherence tomography. Science, 276, 2037-2039.
21. Bouma, B.E., Tearney, G.J., Compton, C.C. and Nishioka, N.S. (2000) High-resolution imaging of the human esophagus and stomach in vivo using optical coherence tomography. Gastrointest. Endosc., 51, 467-474.
22. Sivak, M.V., Kobayashi, K., Izatt, J.A., Rollins, A.M., Ung-runyawee, R., Chak, A., Wong, R.C.K., Isenberg, G.A. and Willis, J. (2000) High-resolution endoscopic imaging of the GI tract using optical coherence tomography. Gastrointest. Endosc., 51, 474-479.
23. Suter, M.J., Jillella, P.A., Vakoc, B.J., Halpern, E.F., Mino-Kenudson, M., Lauwers, G.Y., Bouma, B.E., Nishioka, N.S. and Tearney, G.J. (2010) Image-guided biopsy in the esophagus through comprehensive optical frequency domain imaging and laser marking: a study in living swine. Gastrointest. Endosc., 71, 346-353.
24. Li, X.D., Boppart, S.A., Van Dam, J., Mashimo, H., Mutinga, M., Drexler, W., Klein, M., Pitris, C., Krinsky, M.L., Brezinski, M.E. et al. (2000) Optical coherence tomography: advanced technology for the endoscopic imaging of Barrett's esophagus. Endoscopy, 32, 921-930.
25. Hatta, W., Uno, K., Koike, T., Yokosawa, S., Iijima, K., Imatani, A. and Shimosegawa, T. (2010) Optical coherence tomography for the staging of tumor infiltration in superficial esophageal squamous cell carcinoma. Gastrointest. Endosc., 71, 899-906.
26. Zhou, C., Tsai, T.H., Lee, H.C., Kirtane, T., Figueiredo, M., Tao, Y.K.K., Ahsen, O.O., Adler, D.C., Schmitt, J.M., Huang, Q. et al. (2012) Characterization of buried glands before and after radiofrequency ablation by using 3-dimensional optical coherence tomography (with videos). Gastrointest. Endosc., 76, 32-40.
27. Tearney, G.J., Brezinski, M.E., Southern, J.F., Bouma, B.E., Boppart, S.A. and Fujimoto, J.G. (1997) Optical biopsy in human gastrointestinal tissue using optical coherence tomography. Am. J. Gastroenterol., 92, 1800-1804.
28. Barlis, P., van Soest, G., Serruys, P.W. and Regar, E. (2009) Intracoronary optical coherence tomography and the evaluation of stents. Exp. Rev. Med. Devices, 6, 157-167.
29. Bezerra, H.G., Costa, M.A., Guagliumi, G., Rollins, A.M. and Simon, D.I. (2009) Intracoronary optical coherence tomography: a comprehensive review clinical and research applications. JACC Cardiovasc. Interv., 2, 1035-1046.
30. Jang, I.K., Bouma, B.E., Kang, D.H., Park, S.J., Park, S.W., Seung, K.B., Choi, K.B., Shishkov, M., Schlendorf, K., Pomerantsev, E. et al. (2002) Visualization of coronary atherosclerotic plaques in patients using optical coherence tomography: comparison with intravascular ultrasound. J. Am. Coll. Cardiol., 39, 604-609.
31. Gutierrez-Chico, J.L., Alegria-Barrero, E., Teijeiro-Mestre, R., Chan, P.H., Tsujioka, H., de Silva, R., Viceconte, N., Lindsay, A., Patterson, T., Foin, N. et al. (2012) Optical coherence tomography: from research to practice. Eur. Heart J. Cardiovasc. Imaging, 13, 370-384.
32. Wolf, M.J., Amrein, H., Izatt, J.A., Choma, M.A., Reedy, M.C. and Rockman, H.A. (2006) Drosophila as a model for the identification of genes causing adult human heart disease. Proc. Natl Acad. Sci. USA, 103, 1394-1399.
33. Choma, M.A., Izatt, S.D., Wessells, R.J., Bodmer, R. and Izatt, J.A. (2006) Images in cardiovascular medicine: in vivo imaging of the adult Drosophila melanogaster heart with real-time optical coherence tomography. Circulation, 114, e35-e36.
34. Allikian, M.J., Bhabha, G., Dospoy, P., Heydemann, A., Ryder, P., Earley, J.U., Wolf, M.J., Rockman, H.A. and McNally, E.M. (2007) Reduced life span with heart and muscle dysfunction in Drosophila sarcoglycan mutants. Hum. Mol. Genet., 16, 2933-2943.
35. Choma, M.A., Suter, M.J., Vakoc, B.J., Bouma, B.E. and Tearney, G.J. (2010) Heart wall velocimetry and exogenous contrast-based cardiac flow imaging in Drosophila melanogaster using Doppler optical coherence tomography. J. Biomed. Optics, 15, 056020.
36. Li, A., Zhou, C., Moore, J., Zhang, P., Tsai, T.H., Lee, H.C., Romano, D.M., McKee, M.L., Schoenfeld, D.A., Serra, M.J. et al. (2011) Changes in the expression of the Alzheimer's disease-associated presenilin gene in Drosophila heart leads to cardiac dysfunction. Curr. Alzheimer Res., 8, 313-322.
37. Choma, M.A., Suter, M.J., Vakoc, B.J., Bouma, B.E. and Tearney, G.J. (2011) Physiological homology between Drosophila melanogaster and vertebrate cardiovascular systems. Dis. Models Mech., 4, 411-420.
38. Brand, A.H. and Perrimon, N. (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development, 118, 401-415.
39. Fischer, J.A., Giniger, E., Maniatis, T. and Ptashne, M. (1988) Gal4 activates transcription in Drosophila. Nature, 332, 853-856.
40. Zikova, M., Da Ponte, J.P., Dastugue, B. and Jagla, K. (2003) Patterning of the cardiac outflow region in Drosophila. Proc. Natl Acad. Sci. USA, 100, 12189-12194.
41. Sturtevant, M.A. and Bier, E. (1995) Analysis of the genetic hierarchy guidingwing vein development in Drosophila. Development, 121, 785-801.
42. Paumard-Rigal, S., Zider, A., Vaudin, P. and Silber, J. (1998) Specific interactions between vestigial and scalloped are required to promote wing tissue proliferation in Drosophila melanogaster. Dev. Genes. Evol., 208, 440-446.
43. Eisenberg, L.M. and Eisenberg, C.A. (2006) Wnt signal transduction and the formation of the myocardium. Dev. Biol., 293, 305-315.
44. Liebner, S., Cattelino, A., Gallini, R., Rudini, N., Iurlaro, M., Piccolo, S. and Dejana, E. (2004) Beta-catenin is required for endothelial-mesenchymal transformation during heart cushion development in the mouse. J. Cell. Biol., 166, 359-367.
45. Zeitouni, B., Senatore, S., Severac, D., Aknin, C., Semeriva, M. and Perrin, L. (2007) Signallingpathways involvedinadultheart formation revealed by gene expression profiling in Drosophila. PLoS Genet., 3, 1907-1921.
46. Cooney, M.T., Vartiainen, E., Laatikainen, T., Juolevi, A., Dudina, A. and Graham, I.M. (2009) Elevated resting heart rate is an independent risk factor for cardiovascular disease in healthy men and women. Am. Heart J., 159, 612-619 e613.
47. Kannel, W.B., Kannel, C., Paffenbarger, R.S. Jr and Cupples, L.A. (1987) Heart rate and cardiovascular mortality: the Framingham study. Am. Heart J., 113, 1489-1494.
48. Benetos, A., Rudnichi, A., Thomas, F., Safar, M. and Guize, L. (1999) Influence of heart rate on mortality in a French population: role of age, gender and blood pressure. Hypertension, 33, 44-52.
49. Woodward, M., Webster, R., Murakami, Y., Barzi, F., Lam, T.H., Fang, X., Suh, I., Batty, G.D., Huxley, R. and Rodgers, A. (2012) The association between resting heart rate, cardiovascular disease and mortality: evidence from 112,680 men and women in 12 cohorts. Eur. J. Prev. Cardiol. doi:10.1177/2047487312452501.
50. Nauman, J., Janszky, I., Vatten, L.J. and Wisloff, U. (2011) Temporal changes in resting heart rate and deaths from ischemic heart disease. JAMA, 306, 2579-2587.
51. Fox, K., Ford, I., Steg, P.G., Tendera, M., Robertson, M. and Ferrari, R. (2008) Heart rate as a prognostic risk factor in patients with coronary artery disease and left-ventricular systolic dysfunction(BEAUTIFUL): a subgroup analysis of a randomised controlled trial. Lancet, 372, 817-821.
52. Fox, K. and Steg, P.G. (2008) Elevated heart rate proven to increase coronary events. Cardiovasc. J. Afr., 19, 276-278.
53. Diaz, A., Bourassa, M.G., Guertin, M.C. and Tardif, J.C. (2005) Long-term prognostic value of resting heart rate in patients with suspected or proven coronary artery disease. Eur. Heart J., 26, 967-974.
54. Jouven, X., Empana, J.P., Escolano, S., Buyck, J.F., Tafflet, M., Desnos, M. and Ducimetiere, P. (2009) Relation of heart rate at rest and long-term(20 years) death rate in initially healthy middle-aged men. Am. J. Cardiol., 103, 279-283.
55. Gosse, P. and Dallocchio, M. (1993) Left ventricular hypertrophy: epidemiological prognosis and associated critical factors. Eur. Heart J., 14 (Suppl. D), 16-21.
56. Haider, A.W., Larson, M.G., Benjamin, E.J. and Levy, D. (1998) Increased left ventricular mass and hypertrophy are associated with increased risk for sudden death. J. Am. Coll. Cardiol., 32, 1454-1459.
57. Levy, D., Garrison, R.J., Savage, D.D., Kannel, W.B. and Castelli, W.P. (1990) Prognostic implications of echocardiographically determined left ventricular mass in the Framingham Heart Study. N. Engl. J. Med., 322, 1561-1566.
58. Moller, J.E., Egstrup, K., Kober, L., Poulsen, S.H., Nyvad, O. and Torp-Pedersen, C. (2003) Prognostic importance of systolic and diastolic function after acute myocardial infarction. Am. Heart J., 145, 147-153.
59. Hillis, G.S., Moller, J.E., Pellikka, P.A., Gersh, B.J., Wright, R.S., Ommen, S.R., Reeder, G.S. and Oh, J.K. (2004) Noninvasive estimation of left ventricular filling pressure by E/e' is a powerful predictor of survival after acute myocardial infarction. J. Am. Coll. Cardiol., 43, 360-367.
60. Wang, M., Yip, G.W.,Wang, A.Y., Zhang, Y., Ho, P.Y., Tse, M.K., Yu, C.M. and Sanderson, J.E. (2005) Tissue Doppler imaging provides incremental prognostic value in patients with systemic hypertension and left ventricular hypertrophy. J. Hypertens., 23, 183-191.
61. Sharma, R., Pellerin, D., Gaze, D.C., Mehta, R.L., Gregson, H., Streather, C.P., Collinson, P.O. and Brecker, S.J. (2006) Mitral peak Doppler E-waveto peak mitral annulus velocity ratio is an accurate estimate of left ventricular filling pressure and predicts mortality in end-stage renal disease. J. Am. Soc. Echocardiogr., 19, 266-273.
62. Nagueh, S.F., Appleton, C.P., Gillebert, T.C., Marino, P.N., Oh, J.K., Smiseth, O.A., Waggoner, A.D., Flachskampf, F.A., Pellikka, P.A. and Evangelista, A. (2009) Recommendations for the evaluation of left ventricular diastolic function by echocardiography. J. Am. Soc. Echocardiogr., 22, 107-133.
63. Matsumura, Y., Elliott, P.M., Virdee, M.S., Sorajja, P., Doi, Y. and McKenna, W.J. (2002) Left ventricular diastolic function assessed using Doppler tissue imaging in patients with hypertrophic cardiomyopathy: relation to symptoms and exercise capacity. Heart, 87, 247-251.
64. Eckberg, D.L., Gault, J.H., Bouchard, R.L., Karliner, J.S. and Ross, J. (1973) Mechanics of left ventricular contraction in chronic severe mitral regurgitation. Circulation, 47, 1252-1259.
65. Kovick, R.B., Fogelman, A.M., Abbasi, A.S., Peter, J.B. and Pearce, M.L. (1975) Echocardiographic evaluation of posterior left-ventricular wall motion in muscular-dystrophy. Circulation, 52, 447-454.
66. Chikamori, T., Dickie, S., Poloniecki, J.D., Myers, M.J., Lavender, J.P. and Mckenna, W.J. (1990) Prognostic-significance of radionuclide-assessed diastolic function in hypertrophic cardiomyopathy. Am. J. Cardiol., 65, 478-482.
67. Pak, P.H., Maughan, W.L., Baughman, K.L. and Kass, D.A. (1996) Marked discordance between dynamic and passive diastolic pressure-volume relations in idiopathic hypertrophic cardiomyopathy. Circulation, 94, 52-60.
68. Galetta, F., Franzoni, F. and Santoro, G. (2004) Left ventricular diastolic function assessed using tissue Doppler imaging in elderly athletes. Int. J. Cardiol., 94, 339-340.
69. Zheng, Z., Wang, Z.M. and Delbono, O. (2002) Charge movement and transcription regulation of L-type calcium channel alpha(1S) in skeletal muscle cells. J. Physiol., 540, 397-409.
70. Benitah, J.P., Alvarez, J.L. and Gomez, A.M. (2010) L-type Ca(2+) current in ventricular cardiomyocytes. J. Mol. Cell. Cardiol., 48, 26-36.
71. Hua, L., Li, C., Xia, D., Qu, P., Li, Z., Zhang, W. and Feng, X. (2000) Relationship between hypertensive left ventricular hypertrophy and levels of endothelin and nitric oxide. Hypertens. Res., 23, 377-380.
72. Braam, B., de Roos, R., Bluyssen, H.,Kemmeren, P., Holstege, F., Joles, J.A. and Koomans, H. (2005) Nitric oxide-dependent and nitric oxide-independent transcriptional responses to high shear stress in endothelial cells. Hypertension, 45, 672-680.
73. Olsson, S.B., Cotoi, S. and Varnauskas, E. (1971) Monophasic action potential and sinus rhythm stability after conversion of atrial fibrillation. Acta Med. Scand., 190, 381-387.
74. Le Clerc, S., Limou, S., Coulonges, C., Carpentier, W., Dina, C., Taing, L., Delaneau, O., Labib, T., Sladek, R., Deveau, C. et al. (2009) Genomewide association study of a rapid progression cohort identifies new susceptibility alleles for AIDS (ANRS Genomewide Association Study 03). J. Infect. Dis., 200, 1194-1201.
75. Adkins, D.E., Aberg, K., McClay, J.L., Bukszar, J., Zhao, Z., Jia, P., Stroup, T.S., Perkins, D., McEvoy, J.P., Lieberman, J.A. et al. (2011) Genomewide pharmacogenomic study of metabolic side effects to antipsychotic drugs. Mol. Psychiatry, 16, 321-332.
76. Barber, M.J., Mangravite, L.M., Hyde, C.L., Chasman, D.I., Smith, J.D., McCarty, C.A., Li, X., Wilke, R.A., Rieder, M.J., Williams, P.T. et al. (2010) Genome-wide association of lipid-lowering response to statins in combined study populations. PLoS One, 5, e9763.
77. Daoud, H., Valdmanis, P.N., Gros-Louis, F., Belzil, V., Spiegelman, D., Henrion, E., Diallo, O., Desjarlais, A., Gauthier, J., Camu, W. et al. (2011) Resequencing of 29 candidate genes in patients with familial and sporadic amyotrophic lateral sclerosis. Arch. Neurol., 68, 587-593.
78. White, B., Pierce, M., Nassif, N., Cense, B., Park, B., Tearney, G., Bouma, B., Chen, T. and de Boer, J. (2003) In vivo dynamic human retinal blood flow imaging using ultra-high-speed spectral domain optical coherence tomography. Optics Express, 11, 3490-3497.
79. Leitgeb, R., Schmetterer, L., Drexler, W., Fercher, A., Zawadzki, R. and Bajraszewski, T. (2003) Real-time assessment of retinal blood flow with ultrafast acquisition by color Doppler Fourier domain optical coherence tomography. Optics Express, 11, 3116-3121.
80. Alayari, N.N., Vogler, G., Taghli-Lamallem, O., Ocorr, K., Bodmer, R. and Cammarato, A. (2009) Fluorescent labeling of Drosophila heart structures. J. Vis. Exp., 32, e1423.
81. Sullivan William, M.A. and Scott Hawley, R. (2000) Drosophila Protocols. Cold Spring Harbor Labroratory Press, Woodbury, NY, 245 pp.