Literature DB >> 19237664

Long-term cardiac-targeted RNA interference for the treatment of heart failure restores cardiac function and reduces pathological hypertrophy.

Lennart Suckau1, Henry Fechner, Elie Chemaly, Stefanie Krohn, Lahouaria Hadri, Jens Kockskämper, Dirk Westermann, Egbert Bisping, Hung Ly, Xiaomin Wang, Yoshiaki Kawase, Jiqiu Chen, Lifan Liang, Isaac Sipo, Roland Vetter, Stefan Weger, Jens Kurreck, Volker Erdmann, Carsten Tschope, Burkert Pieske, Djamel Lebeche, Heinz-Peter Schultheiss, Roger J Hajjar, Wolfgang C Poller.   

Abstract

BACKGROUND: RNA interference (RNAi) has the potential to be a novel therapeutic strategy in diverse areas of medicine. Here, we report on targeted RNAi for the treatment of heart failure, an important disorder in humans that results from multiple causes. Successful treatment of heart failure is demonstrated in a rat model of transaortic banding by RNAi targeting of phospholamban, a key regulator of cardiac Ca(2+) homeostasis. Whereas gene therapy rests on recombinant protein expression as its basic principle, RNAi therapy uses regulatory RNAs to achieve its effect. METHODS AND
RESULTS: We describe structural requirements to obtain high RNAi activity from adenoviral and adeno-associated virus (AAV9) vectors and show that an adenoviral short hairpin RNA vector (AdV-shRNA) silenced phospholamban in cardiomyocytes (primary neonatal rat cardiomyocytes) and improved hemodynamics in heart-failure rats 1 month after aortic root injection. For simplified long-term therapy, we developed a dimeric cardiotropic adeno-associated virus vector (rAAV9-shPLB) to deliver RNAi activity to the heart via intravenous injection. Cardiac phospholamban protein was reduced to 25%, and suppression of sacroplasmic reticulum Ca(2+) ATPase in the HF groups was rescued. In contrast to traditional vectors, rAAV9 showed high affinity for myocardium but low affinity for liver and other organs. rAAV9-shPLB therapy restored diastolic (left ventricular end-diastolic pressure, dp/dt(min), and tau) and systolic (fractional shortening) functional parameters to normal ranges. The massive cardiac dilation was normalized, and cardiac hypertrophy, cardiomyocyte diameter, and cardiac fibrosis were reduced significantly. Importantly, no evidence was found of microRNA deregulation or hepatotoxicity during these RNAi therapies.
CONCLUSIONS: Our data show for the first time the high efficacy of an RNAi therapeutic strategy in a cardiac disease.

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Year:  2009        PMID: 19237664      PMCID: PMC4298485          DOI: 10.1161/CIRCULATIONAHA.108.783852

Source DB:  PubMed          Journal:  Circulation        ISSN: 0009-7322            Impact factor:   29.690


  38 in total

1.  A mutation in the human phospholamban gene, deleting arginine 14, results in lethal, hereditary cardiomyopathy.

Authors:  Kobra Haghighi; Fotis Kolokathis; Anthony O Gramolini; Jason R Waggoner; Luke Pater; Roy A Lynch; Guo-Chang Fan; Dimitris Tsiapras; Rohan R Parekh; Gerald W Dorn; David H MacLennan; Dimitrios Th Kremastinos; Evangelia G Kranias
Journal:  Proc Natl Acad Sci U S A       Date:  2006-01-23       Impact factor: 11.205

2.  Recombinant adeno-associated virus serotype 9 leads to preferential cardiac transduction in vivo.

Authors:  Christina A Pacak; Cathryn S Mah; Bijoy D Thattaliyath; Thomas J Conlon; Melissa A Lewis; Denise E Cloutier; Irene Zolotukhin; Alice F Tarantal; Barry J Byrne
Journal:  Circ Res       Date:  2006-07-27       Impact factor: 17.367

3.  Construction of phospholamban antisense RNA recombinant adeno-associated virus vector and its effects in rat cardiomyocytes.

Authors:  Jiang Li; Shen-jiang Hu; Jian Sun; Zhao-hui Zhu; Xia Zheng; Guo-zhong Wang; Yu-mei Yao; Nai-yun Chen; Xiao-yan Zhao
Journal:  Acta Pharmacol Sin       Date:  2005-01       Impact factor: 6.150

4.  Gene transfer of a phospholamban-targeted antibody improves calcium handling and cardiac function in heart failure.

Authors:  Thomas Dieterle; Markus Meyer; Yusu Gu; Darrell D Belke; Eric Swanson; Mitsuo Iwatate; John Hollander; Kirk L Peterson; John Ross; Wolfgang H Dillmann
Journal:  Cardiovasc Res       Date:  2005-09-01       Impact factor: 10.787

5.  Restoration of mechanical and energetic function in failing aortic-banded rat hearts by gene transfer of calcium cycling proteins.

Authors:  Susumu Sakata; Djamel Lebeche; Naoya Sakata; Yuri Sakata; Elie R Chemaly; Li Fan Liang; Tsuyoshi Tsuji; Yoshiaki Takewa; Federica del Monte; Richard Peluso; Krisztina Zsebo; Dongtak Jeong; Woo Jin Park; Yoshiaki Kawase; Roger J Hajjar
Journal:  J Mol Cell Cardiol       Date:  2007-01-10       Impact factor: 5.000

6.  A signature pattern of stress-responsive microRNAs that can evoke cardiac hypertrophy and heart failure.

Authors:  Eva van Rooij; Lillian B Sutherland; Ning Liu; Andrew H Williams; John McAnally; Robert D Gerard; James A Richardson; Eric N Olson
Journal:  Proc Natl Acad Sci U S A       Date:  2006-11-15       Impact factor: 11.205

7.  Robust adenoviral and adeno-associated viral gene transfer to the in vivo murine heart: application to study of phospholamban physiology.

Authors:  Hunter C Champion; Dimitrios Georgakopoulos; Saptarsi Haldar; Lili Wang; Yibin Wang; David A Kass
Journal:  Circulation       Date:  2003-11-24       Impact factor: 29.690

8.  AAV-mediated knockdown of phospholamban leads to improved contractility and calcium handling in cardiomyocytes.

Authors:  Lourdes M Andino; Morihiko Takeda; Hideko Kasahara; Andrew Jakymiw; Barry J Byrne; Alfred S Lewin
Journal:  J Gene Med       Date:  2008-02       Impact factor: 4.565

9.  Chronic phospholamban inhibition prevents progressive cardiac dysfunction and pathological remodeling after infarction in rats.

Authors:  Yoshitaka Iwanaga; Masahiko Hoshijima; Yusu Gu; Mitsuo Iwatate; Thomas Dieterle; Yasuhiro Ikeda; Moto-o Date; Jacqueline Chrast; Masunori Matsuzaki; Kirk L Peterson; Kenneth R Chien; John Ross
Journal:  J Clin Invest       Date:  2004-03       Impact factor: 14.808

10.  The presence of Lys27 instead of Asn27 in human phospholamban promotes sarcoplasmic reticulum Ca2+-ATPase superinhibition and cardiac remodeling.

Authors:  Wen Zhao; Qunying Yuan; Jiang Qian; Jason R Waggoner; Anand Pathak; Guoxiang Chu; Bryan Mitton; Xiaoyin Sun; Jay Jin; Julian C Braz; Harvey S Hahn; Yehia Marreez; Faisal Syed; Piero Pollesello; Arto Annila; Hong-Sheng Wang; Jo El J Schultz; Jeffery D Molkentin; Stephen B Liggett; Gerald W Dorn; Evangelia G Kranias
Journal:  Circulation       Date:  2006-02-13       Impact factor: 29.690

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  90 in total

1.  CXCR4 gene transfer prevents pressure overload induced heart failure.

Authors:  Thomas J Larocca; Dongtak Jeong; Erik Kohlbrenner; Ahyoung Lee; Jiqiu Chen; Roger J Hajjar; Sima T Tarzami
Journal:  J Mol Cell Cardiol       Date:  2012-06-03       Impact factor: 5.000

Review 2.  Endogenous migration modulators as parent compounds for the development of novel cardiovascular and anti-inflammatory drugs.

Authors:  Wolfgang Poller; Madlen Rother; Carsten Skurk; Carmen Scheibenbogen
Journal:  Br J Pharmacol       Date:  2012-04       Impact factor: 8.739

3.  The rise of cardiovascular medicine.

Authors:  Eugene Braunwald
Journal:  Eur Heart J       Date:  2012-03-12       Impact factor: 29.983

Review 4.  Therapeutic potential of microRNAs in heart failure.

Authors:  Gerald W Dorn
Journal:  Curr Cardiol Rep       Date:  2010-05       Impact factor: 2.931

Review 5.  Calcium cycling proteins and their association with heart failure.

Authors:  L Hadri; R J Hajjar
Journal:  Clin Pharmacol Ther       Date:  2011-08-10       Impact factor: 6.875

6.  Intravascular AAV9 Administration for Delivering RNA Silencing Constructs to the CNS and Periphery.

Authors:  Brett D Dufour; Jodi L McBride
Journal:  Methods Mol Biol       Date:  2016

7.  Long noncoding RNA MALAT1-derived mascRNA is involved in cardiovascular innate immunity.

Authors:  Martina Gast; Blanche Schroen; Antje Voigt; Jan Haas; Uwe Kuehl; Dirk Lassner; Carsten Skurk; Felicitas Escher; Xiaomin Wang; Adelheid Kratzer; Katharina Michalik; Anna Papageorgiou; Tim Peters; Madlen Loebel; Sabrina Wilk; Nadine Althof; Kannanganattu V Prasanth; Hugo Katus; Benjamin Meder; Shinichi Nakagawa; Carmen Scheibenbogen; Heinz-Peter Schultheiss; Ulf Landmesser; Stefanie Dimmeler; Stephane Heymans; Wolfgang Poller
Journal:  J Mol Cell Biol       Date:  2016-01-27       Impact factor: 6.216

Review 8.  Cardiovascular gene therapy for myocardial infarction.

Authors:  Maria C Scimia; Anna M Gumpert; Walter J Koch
Journal:  Expert Opin Biol Ther       Date:  2013-12-16       Impact factor: 4.388

Review 9.  Non-coding RNAs in cardiovascular diseases: diagnostic and therapeutic perspectives.

Authors:  Wolfgang Poller; Stefanie Dimmeler; Stephane Heymans; Tanja Zeller; Jan Haas; Mahir Karakas; David-Manuel Leistner; Philipp Jakob; Shinichi Nakagawa; Stefan Blankenberg; Stefan Engelhardt; Thomas Thum; Christian Weber; Benjamin Meder; Roger Hajjar; Ulf Landmesser
Journal:  Eur Heart J       Date:  2018-08-01       Impact factor: 29.983

10.  microRNA-21 promotes cardiac fibrosis and development of heart failure with preserved left ventricular ejection fraction by up-regulating Bcl-2.

Authors:  Shuguang Dong; Wenhan Ma; Bohan Hao; Fen Hu; Lianhua Yan; Xiaofei Yan; Ya Wang; Zhijian Chen; Zhaohui Wang
Journal:  Int J Clin Exp Pathol       Date:  2014-01-15
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