A deleterious gene-by-environment interaction imposed by calcium channel blockers in Marfan syndrome

eLife

Volumn 4, Issue OCTOBER2015, 2015, Pages

  Doyle, Jefferson J ^a,b   Doyle, Alexander J ^a,c   Wilson, Nicole K ^a   Habashi, Jennifer P ^a   Bedja, Djahida ^a,d   Whitworth, Ryan E ^e   Lindsay, Mark E ^f   Schoenhoff, Florian ^a,g   Myers, Loretha ^a   Huso, Nick ^a   Bachir, Suha ^a   Squires, Oliver ^a   Rusholme, Benjamin ^a   Ehsan, Hamid ^b   Huso, David ^a   Thomas, Craig J ^h   Caulfield, Mark J ^c   Van Eyk, Jennifer E ^a   Judge, Daniel P ^a   Dietz, Harry C ^a,j,j   Farrar, Carrie ⁱ   Ravekes, Williams ^j   Lurman, Kira ^j   Holmes, Kathryn W ^j   Habashi, Jennifer ^j   Milewicz, Dianna M ^k   Prakash, Siddharth K ^k   Terry, Meghan ^k   Lemaire, Scott A ^l   Morris, Shaine A ^l   Volguina, Irina ^l   Maslen, Cheryl L ⁱ   Song, Howard K ⁱ   Silberbach, G Michael ⁱ   Pyeritz, Reed E ^m   Bavaria, Joseph E ^m   Milewski, Karianna ^m   Parker, Amber ^m   Devereux, Richard B ⁿ   Weinsaft, Jonathan W ⁿ   Roman, Mary J ⁿ   Latortue, Tanya ⁿ   Shohet, Ralph ^o   Kennedy, Fionna ^o   McDonnell, Nazli ^p   Griswold, Ben ^p   Asch, Federico M ^q   Weissman, Neil J ^q   Eagle, Kim A ^r   Tolunay, H Eser ^s   Desvigne Nickens, Patrice ^s   Stylianou, Mario P ^s   Mitchell, Megan ^s   Tseng, Hung ^t   Kroner, Barbara L ^e   Hendershot, Tabitha ^e   Whitworth, Ryan ^e   Ringer, Danny ^e   McCallion, Andy ^j   Loeys, Bart ^u   Van Laer, Lut ^u   Eriksson, Per ^v   Franco Cereceda, Anders ^v   Mertens, Luc ^w   Mittal, Seema ^w   Mohamed, Salah A ^x   Andelfinger, Gregor ^y   more..

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^d MACQUARIE UNIVERSITY   (Australia)

^e RTI INTERNATIONAL   (United States)

^f HARVARD MEDICAL SCHOOL   (United States)

^g UNIVERSITY OF BERN   (Switzerland)

^h NATIONAL INSTITUTES OF HEALTH   (United States)

ⁱ OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^j JOHNS HOPKINS UNIVERSITY   (United States)

^k UNIVERSITY OF TEXAS   (United States)

^l BAYLOR COLLEGE OF MEDICINE   (United States)

^m UNIVERSITY OF PENNSYLVANIA   (United States)

ⁿ WEILL CORNELL MEDICAL COLLEGE   (United States)

^o Cancer Center Program   (United States)

^p NATIONAL INSTITUTE ON AGING   (United States)

^q MEDSTAR RESEARCH INSTITUTE   (United States)

^r UNIVERSITY OF MICHIGAN   (United States)

^s NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^t National Institute of Arthritis   (United States)

^u UNIVERSITY OF ANTWERP   (Belgium)

^v KAROLINSKA INSTITUTE   (Sweden)

^w HOSPITAL FOR SICK CHILDREN   (Canada)

^x UNIVERSITY OF LÜBECK   (Germany)

^y UNIVERSITY OF MONTREAL   (Canada)

more..

Author keywords

[No Author keywords available]

Indexed keywords

AMLODIPINE; ANGIOTENSIN 1 RECEPTOR; CALCIUM CHANNEL BLOCKING AGENT; ENZASTAURIN; HYDRALAZINE; LOSARTAN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE C; VERAPAMIL; AGTR1A PROTEIN, MOUSE; ANTIHYPERTENSIVE AGENT; INDOLE DERIVATIVE; PROTEIN KINASE C BETA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; AORTA ANEURYSM; AORTA DISSECTION; AORTA ROOT; ARTICLE; BLOOD PRESSURE; CONTROLLED STUDY; ECHOCARDIOGRAPHY; FEMALE; FOLLOW UP; GENE EXPRESSION; GENOTYPE; GENOTYPE ENVIRONMENT INTERACTION; HEART RATE; HISTOLOGY; HUMAN; MALE; MARFAN SYNDROME; MOUSE; NONHUMAN; SCORING SYSTEM; WESTERN BLOTTING; ADULT; ANIMAL; C57BL MOUSE; CHILD; DISEASE MODEL; LONGITUDINAL STUDY; METABOLISM; PATHOLOGY; PRESCHOOL CHILD; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS; TREATMENT OUTCOME;

ADULT; ANIMALS; ANTIHYPERTENSIVE AGENTS; CALCIUM CHANNEL BLOCKERS; CHILD; CHILD, PRESCHOOL; DISEASE MODELS, ANIMAL; HUMANS; HYDRALAZINE; INDOLES; LONGITUDINAL STUDIES; MAP KINASE SIGNALING SYSTEM; MARFAN SYNDROME; MICE, INBRED C57BL; PROTEIN KINASE C BETA; RECEPTOR, ANGIOTENSIN, TYPE 1; SURVIVAL ANALYSIS; TREATMENT OUTCOME;

EID: 84946605554     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.08648     Document Type: Article

References (36)

1. Chen X, Rateri DL, Howatt DA, Balakrishnan A, Moorleghen JJ, Morris AJ, Charnigo R, Cassis LA, Daugherty A. 2013. Amlodipine reduces AngII-induced aortic aneurysms and atherosclerosis in hypercholesterolemic mice. PLOS ONE 8:e81743. doi: 10.1371/journal.pone.0081743.
2. Cohn RD, van Erp C, Habashi JP, Soleimani AA, Klein EC, Lisi MT, Gamradt M, ap Rhys CM, Holm TM, Loeys BL, Ramirez F, Judge DP, Ward CW, Dietz HC. 2007. Angiotensin II type 1 receptor blockade attenuates TGF-betainduced failure of muscle regeneration in multiple myopathic states. Nature Medicine 13:204-210. doi: 10.1038/ nm1536.
3. Cook JR, Clayton NP, Carta L, Galatioto J, Chiu E, Smaldone S, Nelson CA, Cheng SH, Wentworth BM, Ramirez F. 2015. Dimorphic effects of transforming growth factor-β signaling during aortic aneurysm progression in mice suggest a combinatorial therapy for Marfan syndrome. Arteriosclerosis, Thrombosis, and Vascular Biology 35: 911-917. doi: 10.1161/ATVBAHA.114.305150.
4. Deng C, Lu Q, Zhang Z, Rao T, Attwood J, Yung R, Richardson B. 2003. Hydralazine may induce autoimmunity by inhibiting extracellular signal-regulated kinase pathway signaling. Arthritis Rheum 48:746-756. doi: 10.1002/art.10833.
5. Doblinger E, Höcherl K, Mederle K, Kattler V, Walter S, Hansen PB, Jensen B, Castrop H. 2012. Angiotensin AT1 receptor-associated protein Arap1 in the kidney vasculature is suppressed by angiotensin II. American Journal of Physiology. Renal Physiology 302:F1313-F1324. doi: 10.1152/ajprenal.00620.2011.
6. Gallo EM, Loch DC, Habashi JP, Calderon JF, Chen Y, Bedja D, van Erp C, Gerber EE, Parker SJ, Sauls K, Judge DP, Cooke SK, Lindsay ME, Rouf R, Myers L, ap Rhys CM, Kent KC, Norris RA, Huso DL, Dietz HC. 2014. Angiotensin II-dependent TGF-β signaling contributes to Loeys-Dietz syndrome vascular pathogenesis. The Journal of Clinical Investigation 124:448-460. doi: 10.1172/JCI69666.
7. Gorelik G, Fang JY, Wu A, Sawalha AH, Richardson B. 2007. Impaired T cell protein kinase C delta activation decreases ERK pathway signaling in idiopathic and hydralazine-induced lupus. The Journal of Immunology 179: 5553-5563. doi: 10.4049/jimmunol.179.8.5553.
8. Graff JR, McNulty AM, Hanna KR, Konicek BW, Lynch RL, Bailey SN, Banks C, Capen A, Goode R, Lewis JE, Sams L, Huss KL, Campbell RM, Iversen PW, Neubauer BL, Brown TJ, Musib L, Geeganage S, Thornton D. 2005. The protein kinase Cbeta-selective inhibitor, Enzastaurin (LY317615.HCl), suppresses signaling through the AKT pathway, induces apoptosis, and suppresses growth of human colon cancer and glioblastoma xenografts. Cancer Research 65:7462-7469. doi: 10.1158/0008-5472.CAN-05-0071.
9. Habashi JP, Doyle JJ, Holm TM, Aziz H, Schoenhoff F, Bedja D, Chen Y, Modiri AN, Judge DP, Dietz HC. 2011. Angiotensin II type 2 receptor signaling attenuates aortic aneurysm in mice through ERK antagonism. Science 332:361-365. doi: 10.1126/science.1192152.
10. Habashi JP, Judge DP, Holm TM, Cohn RD, Loeys BL, Cooper TK, Myers L, Klein EC, Liu G, Calvi C, Podowski M, Neptune ER, Halushka MK, Bedja D, Gabrielson K, Rifkin DB, Carta L, Ramirez F, Huso DL, Dietz HC. 2006. Losartan, an AT1 antagonist, prevents aortic aneurysm in a mouse model of Marfan syndrome. Science 312: 117-121. doi: 10.1126/science.1124287.
11. Hartog AW, Franken R, Zwinderman AH, Groenink M, Mulder BJ. 2012. Current and future pharmacological treatment strategies with regard to aortic disease in Marfan syndrome. Expert Opinion on Pharmacotherapy 13: 647-662. doi: 10.1517/14656566.2012.665446.
12. Haskett D, Doyle JJ, Gard C, Chen H, Ball C, Estabrook MA, Encinas AC, Dietz HC, Utzinger U, Vande Geest JP, Azhar M. 2012. Altered tissue behavior of a non-aneurysmal descending thoracic aorta in the mouse model of Marfan syndrome. Cell and Tissue Research 347:267-277. doi: 10.1007/s00441-011-1270-y.
13. Holm TM, Habashi JP, Doyle JJ, Bedja D, Chen Y, van Erp C, Lindsay ME, Kim D, Schoenhoff F, Cohn RD, Loeys BL, Thomas CJ, Patnaik S, Marugan JJ, Judge DP, Dietz HC. 2011. Noncanonical TGFβ signaling contributes to aortic aneurysm progression in Marfan syndrome mice. Science 332:358-361. doi: 10.1126/science.1192149.
14. Lee SJ, KangJH, Choi SY, Suk KT, KimDJ, KwonOS. 2013. PKCδ as a regulator for TGFβ1-induced α-SMA production in a murine nonalcoholic steatohepatitis model. PLOS ONE 8:e55979. doi: 10.1371/journal.pone.0055979.
15. Li Z, Jimenez SA. 2011. Protein kinase Cδ and c-Abl kinase are required for transforming growth factor β induction of endothelial-mesenchymal transition in vitro. Arthritis Rheum 63:2473-2483. doi: 10.1002/art.30317.
16. Milewicz DM, Dietz HC, Miller DC. 2005. Treatment of aortic disease in patients with Marfan syndrome. Circulation 111:e150-e157. doi: 10.1161/01.CIR.0000155243.70456.F4.
17. Moran D. 1991. Voltage-dependent-L-type Ca2+ channels participate in regulating neural crest migration and differentiation. The American Journal of Anatomy 192:14-22. doi: 10.1002/aja.1001920103.
18. Mulsow JJ, Watson RW, Fitzpatrick JM, O'Connell PR. 2005. Transforming growth factor-beta promotes profibrotic behavior by serosal fibroblasts via PKC and ERK1/2 mitogen activated protein kinase cell signaling. Annals of Surgery 242:880-887. Discussion 887-889. doi: 10.1097/01.sla.0000189606.58343.cd.
19. Neptune ER, Frischmeyer PA, Arking DE, Myers L, Bunton TE, Gayraud B, Ramirez F, Sakai LY, Dietz HC. 2003. Dysregulation of TGF-beta activation contributes to pathogenesis in Marfan syndrome. Nature Genetics 33: 407-411. doi: 10.1038/ng1116.
20. Ng CM, Cheng A, Myers LA, Martinez-Murillo F, Jie C, Bedja D, Gabrielson KL, Hausladen JM, Mecham RP, Judge DP, Dietz HC. 2004. TGF-beta-dependent pathogenesis of mitral valve prolapse in a mouse model of Marfan syndrome. The Journal of Clinical Investigation 114:1586-1592. doi: 10.1172/JCI200422715.
21. Olivares Reyes JA, Shah BH, Hernández-Aranda J, García-Caballero A, Farshori MP, García-Sáinz JA, Catt KJ. 2005. Agonist-induced interactions between angiotensin AT1 and epidermal growth factor receptors. Molecular Pharmaceutics 68:356-364.
22. Olson ER, Shamhart PE, Naugle JE, Meszaros JG. 2008. Angiotensin II-induced extracellular signal-regulated kinase 1/2 activation is mediated by protein kinase Cdelta and intracellular calcium in adult rat cardiac fibroblasts. Hypertension 51:704-711. doi: 10.1161/HYPERTENSIONAHA.107.098459.
23. Ramachandran KV, Hennessey JA, Barnett AS, Yin X, Stadt HA, Foster E, Shah RA, Yazawa M, Dolmetsch RE, Kirby ML, Pitt GS. 2013. Calcium influx through L-type CaV1.2 Ca2+ channels regulates mandibular development. The Journal of Clinical Investigation 123:1638-1646. doi: 10.1172/JCI66903.
24. Rossi-Foulkes R, Roman MJ, Rosen SE, Kramer-Fox R, Ehlers KH, O'Loughlin JE, Davis JG, Devereux RB. 1999. Phenotypic features and impact of beta blocker or calcium antagonist therapy on aortic lumen size in the Marfan syndrome. The American Journal of Cardiology 83:1364-1368. doi: 10.1016/S0002-9149(99)00101-0.
25. Ruvolo PP, Zhou L, Watt JC, Ruvolo VR, Burks JK, Jiffar T, Kornblau S, Konopleva M, Andreeff M. 2011. Targeting PKC-mediated signal transduction pathways using enzastaurin to promote apoptosis in acute myeloid leukemiaderived cell lines and blast cells. Journal of Cellular Biochemistry 112:1696-1707. doi: 10.1002/jcb.23090.
26. Ryer EJ, Hom RP, Sakakibara K, Nakayama KI, Nakayama K, Faries PL, Liu B, Kent KC. 2006. PKCdelta is necessary for Smad3 expression and transforming growth factor beta-induced fibronectin synthesis in vascular smooth muscle cells. Arteriosclerosis, Thrombosis, and Vascular Biology 26:780-786. doi: 10.1161/01.ATV.0000209517. 00220.cd.
27. Salim MA, Alpert BS, Ward JC, Pyeritz RE. 1994. Effect of beta-adrenergic blockade on aortic root rate of dilation in the Marfan syndrome. The American Journal of Cardiology 74:629-633. doi: 10.1016/0002-9149(94)90762-5.
28. Shah BH, Catt KJ. 2002. Calcium-independent activation of extracellularly regulated kinases 1 and 2 by angiotensin II in hepatic C9 cells: roles of protein kinase Cdelta, Src/proline-rich tyrosine kinase 2, and epidermal growth receptor trans-activation. Molecular Pharmaceutics 61:343-351. doi: 10.1124/mol.61.2.343.
29. Shinmura K, Tamaki K, Ito K, Yan X, Yamamoto T, Katsumata Y, Matsuhashi T, Sano M, Fukuda K, Suematsu M, Ishii I. 2015. Indispensable role of endothelial nitric oxide synthase in caloric restriction-induced cardioprotection against ischemia-reperfusion injury. American Journal of Physiology. Heart and Circulatory Physiology 15: H894-H903. doi: 10.1152/ajpheart.00333.2014.
30. Shores J, Berger KR, Murphy EA, Pyeritz RE. 1994. Progression of aortic dilatation and the benefit of long-term beta-adrenergic blockade in Marfan's syndrome. The New England Journal of Medicine 330:1335-1341. doi: 10. 1056/NEJM199405123301902.
31. Silverman DI, Burton KJ, Gray J, Kouchoukos NT, Roman MJ, Boxer M, Devereux RB, Tsipouras P. 1995. Life expectancy in the Marfan syndrome. The American Journal of Cardiology 15:157-160. doi: 10.1016/S0002-9149 (00)80066-1.
32. Takahashi K, Matsumoto Y, Doe Z, Kanazawa M, Satoh K, Shimizu T, Sato A, Fukumoto Y, Shimokawa H. 2013. Combination therapy with atorvastatin and amlodipine suppresses angiotensin II-induced aortic aneurysm formation. PLOS ONE 8:e72558. doi: 10.1371/journal.pone.0072558.
33. Uchiyama-Tanaka Y, Matsubara H, Nozawa Y, Murasawa S, Mori Y, Kosaki A, Maruyama K, Masaki H, Shibasaki Y, Fujiyama S, Nose A, Iba O, Hasagawa T, Tateishi E, Higashiyama S, Iwasaka T. 2001. Angiotensin II signaling and HB-EGF shedding via metalloproteinase in glomerular mesangial cells. Kidney International 60:2153-2163. doi: 10.1046/j.1523-1755.2001.00067.x.
34. von Kodolitsch Y, Robinson PN. 2007. Marfan syndrome: an update of genetics, medical and surgical management. Heart 93:755-760. doi: 10.1136/hrt.2006.098798.
35. Williams A, Davies S, Stuart AG, Wilson DG, Fraser AG. 2008. Medical treatment of Marfan syndrome: a time for change. Heart 94:414-421. doi: 10.1136/hrt.2006.109454.
36. Wu X, Zhu M, Fletcher JA, Giobbie-Hurder A, Hodi FS. 2012. The protein kinase C inhibitor enzastaurin exhibits antitumor activity against uveal melanoma. PLOS ONE 7:e29622. doi: 10.1371/journal.pone.0029622.