Mechano-signaling in Heart Failure

Overview

Journal Pflugers Arch

Specialty Physiology

Date 2014 Feb 18

PMID 24531746

Citations 21

Authors

Byambajav Buyandelger

Catherine Mansfield

Ralph Knoll

Affiliations

Soon will be listed here.

Abstract

Mechanosensation and mechanotransduction are fundamental aspects of biology, but the link between physical stimuli and biological responses remains not well understood. The perception of mechanical stimuli, their conversion into biochemical signals, and the transmission of these signals are particularly important for dynamic organs such as the heart. Various concepts have been introduced to explain mechanosensation at the molecular level, including effects on signalosomes, tensegrity, or direct activation (or inactivation) of enzymes. Striated muscles, including cardiac myocytes, differ from other cells in that they contain sarcomeres which are essential for the generation of forces and which play additional roles in mechanosensation. The majority of cardiomyopathy causing candidate genes encode structural proteins among which titin probably is the most important one. Due to its elastic elements, titin is a length sensor and also plays a role as a tension sensor (i.e., stress sensation). The recent discovery of titin mutations being a major cause of dilated cardiomyopathy (DCM) also underpins the importance of mechanosensation and mechanotransduction in the pathogenesis of heart failure. Here, we focus on sarcomere-related mechanisms, discuss recent findings, and provide a link to cardiomyopathy and associated heart failure.

Citing Articles

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References

Takawira D, Budinger G, Hopkinson S, Jones J . A dystroglycan/plectin scaffold mediates mechanical pathway bifurcation in lung epithelial cells. J Biol Chem. 2010; 286(8):6301-10. PMC: 3057847. DOI: 10.1074/jbc.M110.178988. View

Hayashi T, Arimura T, Itoh-Satoh M, Ueda K, Hohda S, Inagaki N . Tcap gene mutations in hypertrophic cardiomyopathy and dilated cardiomyopathy. J Am Coll Cardiol. 2004; 44(11):2192-201. DOI: 10.1016/j.jacc.2004.08.058. View

Laslett L, Alagona Jr P, Clark 3rd B, Drozda Jr J, Saldivar F, Wilson S . The worldwide environment of cardiovascular disease: prevalence, diagnosis, therapy, and policy issues: a report from the American College of Cardiology. J Am Coll Cardiol. 2012; 60(25 Suppl):S1-49. DOI: 10.1016/j.jacc.2012.11.002. View

Mosca S . Cardioprotective effects of stretch are mediated by activation of sarcolemmal, not mitochondrial, ATP-sensitive potassium channels. Am J Physiol Heart Circ Physiol. 2007; 293(2):H1007-12. DOI: 10.1152/ajpheart.00051.2007. View

Bos J, Poley R, Ny M, Tester D, Xu X, Vatta M . Genotype-phenotype relationships involving hypertrophic cardiomyopathy-associated mutations in titin, muscle LIM protein, and telethonin. Mol Genet Metab. 2005; 88(1):78-85. PMC: 2756511. DOI: 10.1016/j.ymgme.2005.10.008. View

Blair E, Redwood C, Ashrafian H, Oliveira M, Broxholme J, Kerr B . Mutations in the gamma(2) subunit of AMP-activated protein kinase cause familial hypertrophic cardiomyopathy: evidence for the central role of energy compromise in disease pathogenesis. Hum Mol Genet. 2001; 10(11):1215-20. DOI: 10.1093/hmg/10.11.1215. View

Knoll R, Iaccarino G, Tarone G, Hilfiker-Kleiner D, Bauersachs J, Leite-Moreira A . Towards a re-definition of 'cardiac hypertrophy' through a rational characterization of left ventricular phenotypes: a position paper of the Working Group 'Myocardial Function' of the ESC. Eur J Heart Fail. 2011; 13(8):811-9. DOI: 10.1093/eurjhf/hfr071. View

Miller M, Bang M, Witt C, Labeit D, Trombitas C, Watanabe K . The muscle ankyrin repeat proteins: CARP, ankrd2/Arpp and DARP as a family of titin filament-based stress response molecules. J Mol Biol. 2003; 333(5):951-64. DOI: 10.1016/j.jmb.2003.09.012. View

Bickham D, West T, Webb M, Woledge R, Curtin N, Ferenczi M . Millisecond-scale biochemical response to change in strain. Biophys J. 2011; 101(10):2445-54. PMC: 3218346. DOI: 10.1016/j.bpj.2011.10.007. View

10.

Knoll R, Hoshijima M, Hoffman H, Person V, Lorenzen-Schmidt I, Bang M . The cardiac mechanical stretch sensor machinery involves a Z disc complex that is defective in a subset of human dilated cardiomyopathy. Cell. 2003; 111(7):943-55. DOI: 10.1016/s0092-8674(02)01226-6. View

11.

Schmitz J, Jeneson J, van Oorschot J, Prompers J, Nicolay K, Hilbers P . Prediction of muscle energy states at low metabolic rates requires feedback control of mitochondrial respiratory chain activity by inorganic phosphate. PLoS One. 2012; 7(3):e34118. PMC: 3314597. DOI: 10.1371/journal.pone.0034118. View

12.

Takahashi K, Kakimoto Y, Toda K, Naruse K . Mechanobiology in cardiac physiology and diseases. J Cell Mol Med. 2013; 17(2):225-32. PMC: 3822585. DOI: 10.1111/jcmm.12027. View

13.

Lange S, Xiang F, Yakovenko A, Vihola A, Hackman P, Rostkova E . The kinase domain of titin controls muscle gene expression and protein turnover. Science. 2005; 308(5728):1599-603. DOI: 10.1126/science.1110463. View

14.

Linke W, Grutzner A . Pulling single molecules of titin by AFM--recent advances and physiological implications. Pflugers Arch. 2007; 456(1):101-15. DOI: 10.1007/s00424-007-0389-x. View

15.

Knoll R, Kostin S, Klede S, Savvatis K, Klinge L, Stehle I . A common MLP (muscle LIM protein) variant is associated with cardiomyopathy. Circ Res. 2010; 106(4):695-704. DOI: 10.1161/CIRCRESAHA.109.206243. View

16.

Olive M, Shatunov A, Gonzalez L, Carmona O, Moreno D, Quereda L . Transcription-terminating mutation in telethonin causing autosomal recessive muscular dystrophy type 2G in a European patient. Neuromuscul Disord. 2008; 18(12):929-33. PMC: 2592511. DOI: 10.1016/j.nmd.2008.07.009. View

17.

Hershberger R, Hedges D, Morales A . Dilated cardiomyopathy: the complexity of a diverse genetic architecture. Nat Rev Cardiol. 2013; 10(9):531-47. DOI: 10.1038/nrcardio.2013.105. View

18.

Ohlsson M, Hedberg C, Bradvik B, Lindberg C, Tajsharghi H, Danielsson O . Hereditary myopathy with early respiratory failure associated with a mutation in A-band titin. Brain. 2012; 135(Pt 6):1682-94. DOI: 10.1093/brain/aws103. View

19.

Pfeffer G, Elliott H, Griffin H, Barresi R, Miller J, Marsh J . Titin mutation segregates with hereditary myopathy with early respiratory failure. Brain. 2012; 135(Pt 6):1695-713. PMC: 3359754. DOI: 10.1093/brain/aws102. View

20.

Buyandelger B, Ng K, Miocic S, Gunkel S, Piotrowska I, Ku C . Genetics of mechanosensation in the heart. J Cardiovasc Transl Res. 2011; 4(3):238-44. PMC: 3098994. DOI: 10.1007/s12265-011-9262-6. View