Cardiomyopathies associated with the DES gene mutations: molecular pathogenesis and gene therapy approaches

Cover Page


Cite item

Full Text

Abstract

Cardiomyopathy (CMP) is a common group of cardiovascular disorders. Genetic (primary) cardiomyopathies are related to abnormalities in more than 100 genes, including the DES gene encoding desmin protein. Desmin is an essential member of the intermediate filaments, ensuring the structural and functional integrity of myocytes. Mutations in the DES gene result in desmin-related cardiomyopathy with progressive course and poor prognosis. By now, specific therapy for cardiomyopathy has not been developed. Existing conservative and surgical treatment modalities target the rate of heart failure progression and sudden cardiac death prevention but have limited efficacy. The development of gene therapy and genome editing could allow for creating effective and specific methods of gene-based therapy for desminopathies. A  number of studies have been published on the use of gene therapy for various genetic cardiomyopathies including those caused by the DES gene mutations, while genome editing has not been used yet. However, promising results have been obtained with CRISPR/Cas9 and TALEN editing systems to correct for “gain-of-function mutations” in some other genes, such as MYBPC3 and PLN. There is also evidence of the possibility to reduce the symptoms of desmin-related cardiomyopathy up to the normal function by knocking out the mutant DES allele, and preserved protein function provided by expression of the normal allele. We believe that genome editing approaches have an open perspective into the development of specific and effective methods to treat desminopathies.

About the authors

K. S. Kochergin-Nikitsky

Research Centre for Medical Genetics

Author for correspondence.
Email: KochNik.KS@gmail.com
ORCID iD: 0000-0002-0096-4542

Konstantin S. Kochergin-Nikitsky - PhD (in Biol.), Senior Research Fellow, Laboratory of Mutagenesis.

19/4-424 Novoyasenevskiy prospekt, Moscow, 117593, tel.: +7 (977) 830 94 95

Russian Federation

E. V. Zaklyazminskaya

Petrovsky National Research Center of Surgery;
Pirogov Russian National Research Medical University (RNRMU)

Email: helenezak@gmail.com
ORCID iD: 0000-0002-6244-9546

Elena V. Zaklyazminskaya - MD, PhD, Head of Laboratory of Medical Genetics Petrovsky NRCS; Associate Professor, Department of Cell Biology and Molecular Genetics, Medical-Biological Faculty RNRMU.

2 Abrikosovskiy pereulok, Moscow, 119991; 1 Ostrovityanova ul., Moscow, 117997

Russian Federation

A. V. Lavrov

Research Centre for Medical Genetics;
Pirogov Russian National Research Medical University (RNRMU)

Email: alexandervlavrov@gmail.com
ORCID iD: 0000-0003-4962-6947

Alexander V. Lavrov - MD, PhD, Leading Research Fellow, Laboratory of Genome Editing RCMG; Associate Professor, Department of Cell Biology and Molecular Genetics, Medical-Biological Faculty RNRMU.

1 Moskvorech'e ul., Moscow, 115522; 1 Ostrovityanova ul., Moscow, 117997

Russian Federation

S. A. Smirnikhina

Research Centre for Medical Genetics

Email: smirnikhinas@gmail.com
ORCID iD: 0000-0002-1558-3048

Svetlana A. Smirnikhina - MD, PhD, Head of the Laboratory of Genome Editing.

1 Moskvorech'e ul., Moscow, 115522

Russian Federation

References

  1. Cooper LT. Definition and classification of the cardiomyopathies [Internet]. Accessed at Apr. 15, 2018. Available from: http://www.upto-date.com/home.
  2. McCartan C, Mason R, Jayasinghe SR, Griffiths LR. Cardiomyopathy classification: ongoing debate in the genomics era. Bi-ochem Res Int. 2012;2012:796926. doi: 10.1155/2012/796926.
  3. Abelmann WH. Classification and natural history of primary myocardial disease. Prog Cardio-vasc Dis. 1984;27(2):73-94. doi: 10.1016/0033-0620(84)90020-3.
  4. Cecchi F, Tomberli B, Olivotto I. Clinical and molecular classification of cardiomyopathies. Glob Cardiol Sci Pract. 2012;2012(1 ):4. doi: 10.5339/gcsp.2012.4.
  5. Richardson P, McKenna W, Bristow M, Maisch B, Mautner B, O'Connell J, Olsen E, Thiene G, Goodwin J, Gyarfas I, Martin I, Nordet P. Report of the 1995 World Health Organization/International Society and Federation of Cardiology Task Force on the Definition and Classification of cardiomyopathies. Circulation. 1996;93(5): 841-2.
  6. Maron BJ. The 2006 American Heart Association classification of cardiomyopathies is the gold standard. Circ Heart Fail. 2008;1(1):72-5; discussion 76. doi: 10.1161/CIRCHEARTFAIL-URE.108.770826.
  7. Elliott P. The 2006 American Heart Association classification of cardiomyopathies is not the gold standard. Circ Heart Fail. 2008;1(1):77-9; discussion 80. doi: 10.1161/CIRCHEARTFAIL-URE.108.770511.
  8. Благова ОВ, Недоступ АВ. Классификация некоронарогенных заболеваний сердца: наш взгляд на проблему. Российский кардиологический журнал. 2017;(2):7-21. doi: 10.15829/1560-4071-2017-2-7-21. doi: 10.15829/1560-4071-2017-2-7-21].
  9. Charron P, Arad M, Arbustini E, Basso C, Bilinska Z, Elliott P, Helio T, Keren A, McKenna WJ, Monserrat L, Pankuweit S, Perrot A, Rapezzi C, Ristic A, Seggewiss H, van Langen I, Tavaz-zi L; European Society of Cardiology Working Group on Myocardial and Pericardial Diseases. Genetic counselling and testing in cardiomyopathies: a position statement of the European Society of Cardiology Working Group on Myocardial and Pericardial Diseases. Eur Heart J. 2010;31 (22):2715-26. doi: 10.1093/eurheartj/ehq271.
  10. Arbustini E, Narula N, Dec GW, Reddy KS, Greenberg B, Kushwaha S, Marwick T, Pinney S, Bellazzi R, Favalli V, Kramer C, Roberts R, Zoghbi WA, Bonow R, Tavazzi L, Fus-ter V, Narula J. The MOGE(S) Classification for a Phenotype-Genotype Nomenclature of Cardiomyopathy: Endorsed by the World Heart Federation. Glob Heart. 2013;8(4):355-82. doi: 10.1016/j.gheart.2013.11.001.
  11. Arbustini E, Narula N, Dec GW, Reddy KS, Greenberg B, Kushwaha S, Marwick T, Pinney S, Bellazzi R, Favalli V, Kramer C, Roberts R, Zoghbi WA, Bonow R, Tavazzi L, Fuster V, Narula J. The MOGE(S) classification for a phenotype-genotype nomenclature of cardiomyopathy: endorsed by the World Heart Federation. J Am Coll Cardiol. 2013;62(22):2046-72. doi: 10.1016/j.jacc.2013.08.1644.
  12. Arbustini E, Narula N, Tavazzi L, Serio A, Gras-so M, Favalli V, Bellazzi R, Tajik JA, Bonow RO, Fuster V, Narula J. The MOGE(S) classification of cardiomyopathy for clinicians. J Am Coll Cardiol. 2014;64(3):304-18. doi: 10.1016/j.jacc.2014.05.027.
  13. Westphal JG, Rigopoulos AG, Bakogiannis C, Ludwig SE, Mavrogeni S, Bigalke B, Doenst T, Pauschinger M, Tschope C, Schulze PC, Nout-sias M. The MOGE(S) classification for cardiomyopathies: current status and future outlook. Heart Fail Rev. 2017;22(6):743-52. doi: 10.1007/s10741-017-9641-4.
  14. Hazebroek MR, Moors S, Dennert R, van den Wijngaard A, Krapels I, Hoos M, Verdonschot J, Merken JJ, de Vries B, Wolffs PF, Crijns HJ, Brunner-La Rocca HP, Heymans S. Prognostic Relevance of Gene-Environment Interactions in Patients With Dilated Cardiomyopathy: Applying the MOGE(S) Classification. J Am Coll Cardiol. 2015;66(12):1313-23. doi: 10.1016/j.jacc.2015.07.023.
  15. Agarwal A, Yousefzai R, Jan MF, Cho C, Sheta-bi K, Bush M, Khandheria BK, Paterick TE, Trei-ber S, Sra J, Werner P, Allaqaband S, Bajwa T, Tajik AJ. Clinical application of WHF-MOGE(S) classification for hypertrophic cardiomyopathy. Glob Heart. 2015;10(3):209-19. doi: 10.1016/j.gheart.2015.01.001.
  16. Goldfarb LG, Dalakas MC. Tragedy in a heartbeat: malfunctioning desmin causes skeletal and cardiac muscle disease. J Clin Invest. 2009;119(7):1806-13. doi: 10.1172/JCI38027.
  17. Clemen CS, Herrmann H, Strelkov SV, Schroder R. Desminopathies: pathology and mechanisms. Acta Neuropathol. 2013;125(1): 47-75. doi: 10.1007/s00401-012-1057-6.
  18. Goldfarb LG, Olive M, Vicart P, Goebel HH. Intermediate filament diseases: desminopathy. Adv Exp Med Biol. 2008;642:131-64.
  19. Brodehl A, Gaertner-Rommel A, Milting H. Molecular insights into cardiomyopathies associated with desmin (DES) mutations. Bio-phys Rev. 2018;10(4):983-1006. doi: 10.1007/s12551-018-0429-0.
  20. Dalakas MC, Vasconcelos OM, Kaminska A, Kwiesciski H, Hilton-Jones D, Squier W, Gold-farb LG. Desmin myopathy: Distinct filamen-topathy caused by mutations in the desmin gene. Acta Myologica. 2002;21:138-43.
  21. Li D, Tapscoft T, Gonzalez O, Burch PE, Quinones MA, Zoghbi WA, Hill R, Bachinski LL, Mann DL, Roberts R. Desmin mutation responsible for idiopathic dilated cardiomyopathy. Circulation. 1999;100(5):461-4.
  22. Carmignac V, Sharma S, Arbogast S, Fischer D, Serreri C, Serria M, Stoltenburg G, Maurage CA, Herrmann H, Cuisset JM, Bar H, Ferreiro A. A homozygous desmin deletion causes an Emery-Dreifuss like recessive myopathy with desmin depletion. Neuromus-cul Disord. 2009; 19(8-9):600. doi: 10.1016/j.nmd.2009.06.179.
  23. Goldfarb LG, Park KY, Cervenakova L, Gorokhova S, Lee HS, Vasconcelos O, Nagle JW, Semi-no-Mora C, Sivakumar K, Dalakas MC. Missense mutations in desmin associated with familial cardiac and skeletal myopathy. Nat Genet. 1998;19(4):402-3. doi: 10.1038/1300.
  24. Arbustini E, Pasotti M, Pilotto A, Pellegrini C, Grasso M, Previtali S, Repetto A, Bellini O, Azan G, Scaffino M, Campana C, Piccolo G, Vigano M, Tavazzi L. Desmin accumulation restrictive cardiomyopathy and atrioventricular block associated with desmin gene defects. Eur J Heart Fail. 2006;8(5):477-83. doi: 10.1016/j.ejheart.2005.11.003.
  25. Munoz-Marmol AM, Strasser G, Isamat M, Coulombe PA, Yang Y, Roca X, Vela E, Mate JL, Coll J, Fernandez-Figueras MT, Navas-Palacios JJ, Ariza A, Fuchs E. A dysfunctional desmin mutation in a patient with severe generalized myopathy. Proc Natl Acad Sci U S A. 1998;95(19): 11312-7. doi: 10.1073/pnas.95.19.11312.
  26. Pinol-Ripoll G, Shatunov A, Cabello A, Lar-rode P, de la Puerta I, Pelegrin J, Ramos FJ, Olive M, Goldfarb LG. Severe infantile-onset cardiomyopathy associated with a homozygous deletion in desmin. Neuromuscul Disord. 2009;19(6):418-22. doi: 10.1016/j.nmd.2009.04.004.
  27. Schroder R, Vrabie A, Goebel HH. Primary desminopathies. J Cell Mol Med. 2007;11(3):416-26. doi: 10.1111/j.1582-4934.2007.00057.x.
  28. van Spaendonck-Zwarts KY, van Hessem L, Jongbloed JD, de Walle HE, Capetanaki Y, van der Kooi AJ, van Langen IM, van den Berg MP, van Tintelen JP. Desmin-related myopathy. Clin Genet. 2011;80(4):354-66. doi: 10.1111/j.1399-0004.2010.01512.x.
  29. Gallego-Delgado M, Delgado JF, Brossa-Loidi V, Palomo J, Marzoa-Rivas R, Perez-Villa F, Salazar-Mendiguchia J, Ruiz-Cano MJ, Gonzalez-Lopez E, Padron-Barthe L, Bornstein B, Alonso-Pulpon L, Garcia-Pavia P. Idiopathic Restrictive Cardiomyopathy Is Primarily a Genetic Disease. J Am Coll Cardiol. 2016;67(25):3021-3. doi: 10.1016/j.jacc.2016.04.024.
  30. Taylor MR, Slavov D, Ku L, Di Lenarda A, Si-nagra G, Carniel E, Haubold K, Boucek MM, Ferguson D, Graw SL, Zhu X, Cavanaugh J, Sucharov CC, Long CS, Bristow MR, Lavori P, Mestroni L; Familial Cardiomyopathy Registry; BEST (Beta-Blocker Evaluation of Survival Trial) DNA Bank. Prevalence of desmin mutations in dilated cardiomyopathy. Circulation. 2007; 115(10): 1244-51. doi: 10.1161/CIRCULATIONAHA.106.646778.
  31. Tesson F, Sylvius N, Pilotto A, Dubosq-Bidot L, Peuchmaurd M, Bouchier C, Benaiche A, Mangin L, Charron P, Gavazzi A, Tavazzi L, Arbusti-ni E, Komajda M. Epidemiology of desmin and cardiac actin gene mutations in a European population of dilated cardiomyopathy. Eur Heart J. 2000;21(22):1872-6. doi: 10.1053/euhj.2000.2245.
  32. Vajsar J, Becker LE, Freedom RM, Murphy EG. Familial desminopathy: myopathy with accumulation of desmin-type intermediate filaments. J Neurol Neurosurg Psychiatry. 1993;56(6):644-8. doi: 10.1136/jnnp.56.6.644.
  33. Goebel HH, Voit T, Warlo I, Jacobs K, Johannsen U, Muller CR. Rev Neurol (Paris). Immunohistologic and electron microscopic abnormalities of desmin and dystrophin in familial cardiomyopathy and myopathy. 1994;150(6-7):452-9.
  34. Dagvadorj A, Goudeau B, Hilton-Jones D, Blancato JK, Shatunov A, Simon-Casteras M, Squier W, Nagle JW, Goldfarb LG, Vicart P. Respiratory insufficiency in desminopathy patients caused by introduction of proline residues in desmin c-terminal alpha-helical segment. Muscle Nerve. 2003;27(6):669-75. doi: 10.1002/mus.10370.
  35. Milner DJ, Weitzer G, Tran D, Bradley A, Capetanaki Y. Disruption of muscle architecture and myocardial degeneration in mice lacking desmin. J Cell Biol. 1996;134(5):1255-70. doi: 10.1083/jcb.134.5.1255.
  36. Steinert PM, Roop DR. Molecular and cellular biology of intermediate filaments. Annu Rev Biochem. 1988;57:593-625. doi: 10.1146/an-nurev.bi.57.070188.003113.
  37. Fuchs E, Weber K. Intermediate filaments: structure, dynamics, function, and disease. Annu Rev Biochem. 1994;63:345-82. doi: 10.1146/annurev.bi.63.070194.002021.
  38. Paulin D, Li Z. Desmin: a major intermediate filament protein essential for the structural integrity and function of muscle. Exp Cell Res. 2004;301(1):1-7. doi: 10.1016/j.yex-cr.2004.08.004.
  39. McLendon PM, Robbins J. Desmin-related cardiomyopathy: an unfolding story. Am J Physiol Heart Circ Physiol. 2011;301(4):H 1220-8. doi: 10.1152/ajpheart.00601.2011.
  40. Capetanaki Y. Desmin cytoskeleton: a potential regulator of muscle mitochondrial behavior and function. Trends Cardiovasc Med. 2002;12(8):339-48. doi: 10.1016/S1050-1738(02)00184-6.
  41. Price MG. Molecular analysis of intermediate filament cytoskeleton - a putative load-bearing structure. Am J Physiol. 1984;246(4 Pt 2):H566-72.
  42. Li Z, Mericskay M, Agbulut O, Butler-Browne G, Carlsson L, Thornell LE, Babinet C, Paulin D. De-smin is essential for the tensile strength and integrity of myofibrils but not for myogenic commitment, differentiation, and fusion of skeletal muscle. J Cell Biol. 1997;139(1):129-44. doi: 10.1083/jcb.139.1.129.
  43. Balogh J, Merisckay M, Li Z, Paulin D, Arner A. Hearts from mice lacking desmin have a myopathy with impaired active force generation and unaltered wall compliance. Cardiovasc Res. 2002;53(2):439-50. doi: 10.1016/s0008-6363(01)00500-4.
  44. Milner DJ, Mavroidis M, Weisleder N, Capetanaki Y. Desmin cytoskeleton linked to muscle mitochondrial distribution and respiratory function. J Cell Biol. 2000;150(6):1283-98. doi: 10.1083/jcb.150.6.1283.
  45. Weisleder N, Taffet GE, Capetanaki Y. Bcl-2 overexpression corrects mitochondrial defects and ameliorates inherited desmin null cardiomyopathy. Proc Natl Acad Sci U S A. 2004;101(3): 769-74. doi: 10.1073/pnas.0303202101.
  46. Liu J, Tang M, Mestril R, Wang X. Aberrant protein aggregation is essential for a mutant desmin to impair the proteolytic function of the ubiquitin-proteasome system in cardiomyo-cytes. J Mol Cell Cardiol. 2006;40(4):451-4. doi: 10.1016/j.yjmcc.2005.12.011.
  47. Kostera-Pruszczyk A, Pruszczyk P, Kaminska A, Lee H-S, Goldfarb LG. Diversity of cardiomyopathy phenotypes caused by mutations in desmin. Int J Cardiol. 2008;131(1): 146-7. doi: 10.1016/j.ijcard.2007.08.095.
  48. Capetanaki Y, Papathanasiou S, Diokmetzi-dou A, Vatsellas G, Tsikitis M. Desmin related disease: a matter of cell survival failure. Curr Opin Cell Biol. 2015;32:113-20. doi: 10.1016/j.ceb.2015.01.004.
  49. Batonnet-Pichon S, Behin A, Cabet E, Delort F, Vicart P, Lilienbaum A. Myofibrillar Myopathies: New Perspectives from Animal Models to Potential Therapeutic Approaches. J Neuromuscul Dis. 2017;4(1):1-15. doi: 10.3233/JND-160203.
  50. Wahbi K, Behin A, Charron P, Dunand M, Richard P, Meune C, Vicart P, Laforet P, Stojkovic T, Becane HM, Kuntzer T, Duboc D. High cardiovascular morbidity and mortality in myofibrillar myopathies due to DES gene mutations: a 10-year longitudinal study. Neuromuscul Disord. 2012;22(3):211-8. doi: 10.1016/j.nmd.2011.10.019.
  51. Liebau G. Therapy of dilated cardiomyopathy with digitalis, diuretics and vasodilators. Herz. 1985;10(3):138-42. German.
  52. Hunt SA, Abraham WT, Chin MH, Feldman AM, Francis GS, Ganiats TG, Jessup M, Konstam MA, Mancini DM, Michl K, Oates JA, Rahko PS, Silver MA, Stevenson LW, Yan-cy CW, Antman EM, Smith SC Jr, Adams CD, Anderson JL, Faxon DP, Fuster V, Halperin JL, Hiratzka LF, Jacobs AK, Nishimura R, Orna-to JP, Page RL, Riegel B; American College of Cardiology; American Heart Association Task Force on Practice Guidelines; American College of Chest Physicians; International Society for Heart and Lung Transplantation; Heart Rhythm Society. ACC/AHA 2005 Guideline Update for the Diagnosis and Management of Chronic Heart Failure in the Adult: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (Writing Committee to Update the 2001 Guidelines for the Evaluation and Management of Heart Failure): developed in collaboration with the American College of Chest Physicians and the International Society for Heart and Lung Transplantation: endorsed by the Heart Rhythm Society. Circulation. 2005;112(12):e154-235. doi: 10.1161/CIRCU-LATIONAHA.105.167586.
  53. Барт БЯ, Беневская ВФ. Дилатационная кардиомиопатия: клиника, диагностика и лечение. Лечебное дело. 2005;(1):3-9.
  54. Colucci WS. Use of angiotensin converting enzyme inhibitors in heart failure with reduced ejection fraction [Internet]. Accessed at Sep. 29, 2018. Available from: https://www.upto-date.com/contents/use-of-angiotensin-converting-enzyme-inhibitors-in-heart-fail-ure-with-reduced-ejection-fraction.
  55. Dzau VJ. Tissue renin-angiotensin system in myocardial hypertrophy and failure. Arch Intern Med. 1993;153(8):937-42. doi: 10.1001/archinte.1993.00410080011002.
  56. Waagstein F. The role of beta-blockers in dilated cardiomyopathy. Curr Opin Cardiol. 1995; 10(3):322-31.
  57. Hjalmarson A, Waagstein F. The role of beta-blockers in the treatment of cardiomyopathy and ischaemic heart failure. Drugs. 1994;47 Suppl 4:31-9; discussion 39-40. doi: 10.2165/00003495-199400474-00006.
  58. Facchini E, Degiovanni A, Cavallino C, Lupi A, Rognoni A, Bongo AS. Beta-Blockers and Nitrates: Pharmacotherapy and Indications. Cardiovasc Hematol Agents Med Chem. 2015;13(1):25-30. doi: 10.2174/1871525713666141219114708.
  59. Colucci WS, Lynne SL. Use of digoxin in heart failure with reduced ejection fraction [Internet]. Accessed at Sep. 30, 2018. Available from: https://www.uptodate.com/contents/use-of-digoxin-in-heart-failure-with-reduced-ejection-fraction.
  60. Nguyen VQ, Celebi MM, Suleman A, Sander GE. Dilated Cardiomyopathy Treatment & Management [Internet]. Accessed at Sep. 27, 2018. Available from: https://emedicine.medscape.com/article/152696.
  61. Tang WH, Parameswaran AC, Maroo AP, Francis GS. Aldosterone receptor antagonists in the medical management of chronic heart failure. Mayo Clin Proc. 2005;80(12):1623-30. doi: 10.4065/80.12.1623.
  62. Kremastinos DT, Farmakis D. Iron overload cardiomyopathy in clinical practice. Circulation. 2011;124(20):2253-63. doi: 10.1161/CIRCULA-TIONAHA.111.050773.
  63. Reardon L, McKenna PJ, Viccellio P. Restrictive Cardiomyopathy Treatment & Management [Internet]. Accessed at Sep. 27, 2018. Available from: https://emedicine.medscape.com/arti-cle/153062.
  64. Dzau VJ, Liew CC, editors. Cardiovascular Genetics and Genomics for the Cardiologist. John Wiley & Sons; 2008. 316 p.
  65. Bott-Silverman C, Aksut B. Dilated and Restrictive Cardiomyopathies [Internet]. Accessed at Sep. 27, 2018. Available from: http://www. clevelandclinicmeded.com/medicalpubs/dis-easemanagement/cardiology/dilated-restric-tive-cardiomyopathy.
  66. Linde C. Heart. Implantable cardioverter-defibrillator treatment and resynchronisation in heart failure. 2004;90(2):231-4. doi: 10.1136/hrt.2003.019695.
  67. Bristow MR, Saxon LA, Boehmer J, Krueger S, Kass DA, De Marco T, Carson P, DiCarlo L, DeMets D, White BG, DeVries DW, Feldman AM; Comparison of Medical Therapy, Pacing, and Defibrillation in Heart Failure (COMPANION) Investigators. Cardiac-resynchronization therapy with or without an implantable defibrillator in advanced chronic heart failure. N Engl J Med. 2004;350(21):2140-50. doi: 10.1056/NEJMoa032423.
  68. Van Bommel RJ, Mollema SA, Borleffs CJ, Bertini M, Ypenburg C, Marsan NA, Delgado V, Van Der Wall EE, Schalij MJ, Bax JJ. Impaired renal function is associated with echocardiographic nonresponse and poor prognosis after cardiac resynchronization therapy. J Am Coll Cardiol. 2011;57(5):549-55. doi: 10.1016/j.jacc.2010.06.060.
  69. Moss AJ, Hall WJ, Cannom DS, Klein H, Brown MW, Daubert JP, Estes NA 3rd, Foster E, Greenberg H, Higgins SL, Pfeffer MA, Solomon SD, Wilber D, Zareba W; MADIT-CRT Trial Investigators. Cardiac-resynchronization therapy for the prevention of heart-failure events. N Engl J Med. 2009;361(14):1329-38. doi: 10.1056/NEJMoa0906431.
  70. Yue Y, Binalsheikh IM, Leach SB, Domeier TL, Duan D. Prospect of gene therapy for cardiomyopathy in hereditary muscular dystrophy. Expert Opin Orphan Drugs. 2016;4(2):169-83. doi: 10.1517/21678707.2016.1124039
  71. Lai Y, Yue Y, Liu M, Ghosh A, Engelhardt JF, Chamberlain JS, Duan D. Efficient in vivo gene expression by trans-splicing adeno-associat-ed viral vectors. Nat Biotechnol. 2005;23(11): 1435-9. doi: 10.1038/nbt1153.
  72. Ghosh A, Yue Y, Lai Y, Duan D. A hybrid vector system expands adeno-associated viral vector packaging capacity in a transgene independent manner. Mol Ther. 2008;16(1):124-30. doi: 10.1038/sj.mt.6300322.
  73. Bostick B, Shin JH, Yue Y, Duan D. AAV-microdystrophin therapy improves cardiac performance in aged female mdx mice. Mol Ther. 2011; 19( 10): 1826-32. doi: 10.1038/mt.2011.154.
  74. Bostick B, Shin JH, Yue Y, Wasala NB, Lai Y, Duan D. AAV micro-dystrophin gene therapy alleviates stress-induced cardiac death but not myocardial fibrosis in > 21-m-old mdx mice, an end-stage model of Duchenne muscular dystrophy cardiomyopathy. J Mol Cell Cardiol. 2012;53(2):217-22. doi: 10.1016/j.yjmcc.2012.05.002.
  75. Bostick B, Yue Y, Lai Y, Long C, Li D, Duan D. Adeno-associated virus serotype-9 microdystrophin gene therapy ameliorates electrocardiographic abnormalities in mdx mice. Hum Gene Ther. 2008;19(8):851-6. doi: 10.1089/hum.2008.058.
  76. Shin JH, Bostick B, Yue Y, Hajjar R, Duan D. SERCA2a gene transfer improves electrocardiographic performance in aged mdx mice. J Transl Med. 2011;9:132. doi: 10.1186/1479-5876-9-132.
  77. Hikoso S, Ikeda Y, Yamaguchi O, Takeda T, Hi-guchi Y, Hirotani S, Kashiwase K, Yamada M, Asahi M, Matsumura Y, Nishida K, Matsuzaki M, Hori M, Otsu K. Progression of heart failure was suppressed by inhibition of apoptosis signal-regulating kinase 1 via transcoronary gene transfer. J Am Coll Cardiol. 2007;50(5):453-62. doi: 10.1016/j.jacc.2007.03.053.
  78. Qiao C, Wang CH, Zhao C, Lu P, Awano H, Xiao B, Li J, Yuan Z, Dai Y, Martin CB, Li J, Lu Q, Xiao X. Muscle and heart function restoration in a limb girdle muscular dystrophy 2I (LG-MD2I) mouse model by systemic FKRP gene delivery. Mol Ther. 2014;22(11):1890-9. doi: 10.1038/mt.2014.141.
  79. Cannavo A, Komici K, Bencivenga L, D'amico ML, Gambino G, Liccardo D, Ferrara N, Ren-go G. GRK2 as a therapeutic target for heart failure. Expert Opin Ther Targets. 2018;22( 1): 75-83. doi: 10.1080/14728222.2018.1406925.
  80. Rengo G, Lymperopoulos A, Zincarelli C, Donniacuo M, Soltys S, Rabinowitz JE, Koch WJ. Myocardial adeno-associated virus serotype 6-betaARKct gene therapy improves cardiac function and normalizes the neurohormonal axis in chronic heart failure. Circulation. 2009;119(1):89-98. doi: 10.1161/CIRCULATIO-NAHA.108.803999.
  81. Raake PW, Schlegel P, Ksienzyk J, Reinko-ber J, Barthelmes J, Schinkel S, Pleger S, Mier W, Haberkorn U, Koch WJ, Katus HA, Most P, Muller OJ. AAV6.pARKct cardiac gene therapy ameliorates cardiac function and normalizes the catecholaminergic axis in a clinically relevant large animal heart failure model. Eur Heart J. 2013;34(19):1437-47. doi: 10.1093/eurheartj/ehr447.
  82. Williams ML, Hata JA, Schroder J, Ramper-saud E, Petrofski J, Jakoi A, Milano CA, Koch WJ. Targeted beta-adrenergic receptor kinase (betaARK1) inhibition by gene transfer in failing human hearts. Circulation. 2004;109(13):1590-3. doi: 10.1161/01.CIR.0000125521.40985.28.
  83. Kawada T, Nakazawa M, Toyo-Oka T. Somatic gene therapy of dilated cardiomyopathy. Nihon Yakurigaku Zasshi. 2002;119(1):37-44. Japanese. doi: 10.1254/fpj.119.37.
  84. Most P, Pleger ST, Volkers M, Heidt B, Boerries M, Weichenhan D, Loffler E, Janssen PM, Eckhart AD, Martini J, Williams ML, Katus HA, Remppis A, Koch WJ. Cardiac adenoviral S100A1 gene delivery rescues failing myocardium. J Clin Invest. 2004;114(11):1550-63. doi: 10.1172/JCI21454.
  85. Pleger ST, Shan C, Ksienzyk J, Bekeredjian R, Boekstegers P, Hinkel R, Schinkel S, Leuchs B, Ludwig J, Qiu G, Weber C, Raake P, Koch WJ, Katus HA, Muller OJ, Most P. Cardiac AAV9-S100A1 gene therapy rescues post-ischemic heart failure in a preclinical large animal model. Sci Transl Med. 2011;3(92):92ra64. doi: 10.1126/scitranslmed.3002097.
  86. Watanabe S, Ishikawa K, Fish K, Oh JG, Mot-loch LJ, Kohlbrenner E, Lee P, Xie C, Lee A, Liang L, Kho C, Leonardson L, McIntyre M, Wilson S, Samulski RJ, Kranias EG, Weber T, Akar FG, Hajjar RJ. Protein Phosphatase Inhibitor-1 Gene Therapy in a Swine Model of Nonischemic Heart Failure. J Am Coll Cardiol. 2017;70(14):1744-56. doi: 10.1016/j.jacc.2017.08.013.
  87. Mearini G, Stimpel D, Geertz B, Weinberger F, Kramer E, Schlossarek S, Mourot-Filia-tre J, Stoehr A, Dutsch A, Wijnker PJ, Braren I, Katus HA, Muller OJ, Voit T, Eschenhagen T, Carrier L. Mybpc3 gene therapy for neonatal cardiomyopathy enables long-term disease prevention in mice. Nat Commun. 2014;5:5515. doi: 10.1038/ncomms6515.
  88. del Monte F, Williams E, Lebeche D, Schmidt U, Rosenzweig A, Gwathmey JK, Lewandowski ED, Hajjar RJ. Improvement in survival and cardiac metabolism after gene transfer of sarcoplasmic reticulum Ca(2+)-ATPase in a rat model of heart failure. Circulation. 2001;104(12):1424-9.
  89. del Monte F, Lebeche D, Guerrero JL, Tsuji T, Doye AA, Gwathmey JK, Hajjar RJ. Abrogation of ventricular arrhythmias in a model of ischemia and reperfusion by targeting myocardial calcium cycling. Proc Natl Acad Sci U S A. 2004;101(15):5622-7. doi: 10.1073/pnas.0305778101.
  90. Pena JR, Szkudlarek AC, Warren CM, Heinrich LS, Gaffin RD, Jagatheesan G, del Monte F, Hajjar RJ, Goldspink PH, Solaro RJ, Wieczorek DF, Wolska BM. Neonatal gene transfer of Serca2a delays onset of hypertrophic remodeling and improves function in familial hypertrophic cardiomyopathy. J Mol Cell Cardiol. 2010;49(6):993-1002. doi: 10.1016/j.yjmcc.2010.09.010.
  91. Tsubata S, Bowles KR, Vatta M, Zintz C, Titus J, Muhonen L, Bowles NE, Towbin JA. Mutations in the human delta-sarcoglycan gene in familial and sporadic dilated cardiomyopathy. J Clin Invest. 2000;106(5):655-62. doi: 10.1172/JCI9224.
  92. Goehringer C, Rutschow D, Bauer R, Schinkel S, Weichenhan D, Bekeredjian R, Straub V, Klein-schmidt JA, Katus HA, Muller OJ Prevention of cardiomyopathy in delta-sarcoglycan knockout mice after systemic transfer of targeted adeno-associated viral vectors. Cardiovasc Res. 2009;82(3):404-10. doi: 10.1093/cvr/cvp061.
  93. He B, Tang RH, Weisleder N, Xiao B, Yuan Z, Cai C, Zhu H, Lin P, Qiao C, Li J, Mayer C, Li J, Ma J, Xiao X. Enhancing muscle membrane repair by gene delivery of MG53 ameliorates muscular dystrophy and heart failure in 6-Sarcoglycan-deficient hamsters. Mol Ther. 2012;20(4):727-35. doi: 10.1038/mt.2012.5.
  94. Prondzynski M, Mearini G, Carrier L. Gene therapy strategies in the treatment of hypertrophic cardiomyopathy. Pflugers Arch. 2019;471(5): 807-15. doi: 10.1007/s00424-018-2173-5.
  95. Heckmann MB, Bauer R, Jungmann A, Winter L, Rapti K, Strucksberg KH, Clemen CS, Li Z, Schroder R, Katus HA, Muller OJ. AAV9-me-diated gene transfer of desmin ameliorates cardiomyopathy in desmin-deficient mice. Gene Ther. 2016;23(8-9):673-9. doi: 10.1038/gt.2016.40.
  96. Pattison JS, Osinska H, Robbins J. Atg7 induces basal autophagy and rescues autophagic deficiency in CryABR120G cardiomyocytes. Circ Res. 2011;109(2):151-60. doi: 10.1161/CIRCRE-SAHA.110.237339.
  97. Maloyan A, Sayegh J, Osinska H, Chua BH, Robbins J. Manipulation of death pathways in desmin-related cardiomyopathy. Circ Res. 2010;106(9):1524-32. doi: 10.1161/CIRCRESA-HA.109.212639.
  98. Wang X, Klevitsky R, Huang W, Glasford J, Li F, Robbins J. AlphaB-crystallin modulates protein aggregation of abnormal desmin. Circ Res. 2003;93(10):998-1005. doi: 10.1161/01.RES.0000102401.77712.ED.
  99. Sanbe A, Daicho T, Mizutani R, Endo T, Mi-yauchi N, Yamauchi J, Tanonaka K, Glabe C, Tanoue A. Protective effect of geranylgerany-lacetone via enhancement of HSPB8 induction in desmin-related cardiomyopathy. PLoS One. 2009;4(4):e5351. doi: 10.1371/journal.pone.0005351.
  100. Karakikes I, Stillitano F, Nonnenmacher M, Tzi-mas C, Sanoudou D, Termglinchan V, Kong CW, Rushing S, Hansen J, Ceholski D, Kolokathis F, Kremastinos D, Katoulis A, Ren L, Cohen N, Gho JMIH, Tsiapras D, Vink A, Wu JC, Asselbergs FW, Li RA, Hulot JS, Kranias EG, Hajjar RJ. Correction of human phospholamban R14del mutation associated with cardiomyopathy using targeted nucleases and combination therapy. Nat Commun. 2015;6:6955. doi: 10.1038/ncomms7955.
  101. Jiang J, Wakimoto H, Seidman JG, Seidman CE. Allele-specific silencing of mutant Myh6 transcripts in mice suppresses hypertrophic cardiomyopathy. Science. 2013;342(6154):111-4. doi: 10.1126/science.1236921.
  102. McLaughlin HM, Kelly MA, Hawley PP, Dar-ras BT, Funke B, Picker J. Compound heterozygosity of predicted loss-of-function DES variants in a family with recessive desmin-opathy. BMC Med Genet. 2013;14:68. doi: 10.1186/1471-2350-14-68.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2019 Kochergin-Nikitsky K.S., Zaklyazminskaya E.V., Lavrov A.V., Smirnikhina S.A.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies