The Role of Microtubules in Heart Failure

Main Article Content

Sidhi Laksono Purwowiyoto
Nadia Afiyani
Axel Jusuf
Hillary Kusharsamita

Abstract

Heart failure (HF) is a complex pathological state in which cardiac performance fails to match perfusion demand, commonly preceded by an enlargement of the heart known as cardiac hypertrophy. Pathological changes in the microtubule network (MTN) organization have been shown to increase cellular stiffness and lead to contractile dysfunction of cardiomyocytes. In this narrative review, we are focusing on the role of the microtubule and also its mechanism in the heart, especially in HF. We conducted literature research for published articles carried out from 2012 to 2022. Microtubules are polymers that serve as structural elements with the shape of long, rigid tubes that are highly dynamic. The stiffness of the myocardium is largely influenced by the MTN. Through various methods, the MTN is remodeled during cardiac hypertrophy and HF. Targeting microtubules for the treatment of HF might become a new approach to improve the outcome. While colchicine inhibits various microtubule-dependent cellular in interphase cells and proliferation, it needs further study for the safety of the adjusted dosage. Manipulating detyrosination of microtubules might be useful for restoring the function of failing myocytes although there are still very limited data on this.

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How to Cite
1.
Purwowiyoto SL, Afiyani N, Jusuf A, Kusharsamita H. The Role of Microtubules in Heart Failure. SEE J Cardiol [Internet]. 2023 Jul. 15 [cited 2024 May 20];4(1):22-8. Available from: https://seejca.eu/index.php/seejca/article/view/6045
Section
Molecular Cardiology

References

Li JM, Yao ZF, Zou YZ, Ge JB, Guan AL, Wu J, et al. The therapeutic potential of G-CSF in pressure overload induced ventricular reconstruction and heart failure in mice. Mol Biol Rep. 2012;39(1):5-12. https://doi.org/10.1007/s11033-011-0703-8 PMid:21431359 DOI: https://doi.org/10.1007/s11033-011-0703-8

Phyo SA, Uchida K, Chen CY, Caporizzo MA, Bedi K, Griffin J, et al. Transcriptional, post-transcriptional, and post-translational mechanisms rewrite the tubulin code during cardiac hypertrophy and failure. Front Cell Dev Biol. 2022;10:837486. https://doi.org/10.3389/fcell.2022.837486 PMid:35433678 DOI: https://doi.org/10.3389/fcell.2022.837486

Caporizzo MA, Chen CY, Bedi K, Margulies KB, Prosser BL. Microtubules increase diastolic stiffness in failing human cardiomyocytes and myocardium. Circulation. 2020;141(11):902-15. https://doi.org/10.1161/circulationaha.119.043930 PMid:31941365 DOI: https://doi.org/10.1161/CIRCULATIONAHA.119.043930

Borin D, Peña B, Chen SN, Long CS, Taylor MR, Mestroni L, et al. Altered microtubule structure, hemichannel localization and beating activity in cardiomyocytes expressing pathologic nuclear lamin A/C. Heliyon. 2020;6(1):e03175. https://doi.org/10.1016/j.heliyon.2020.e03175 PMid:32021920 DOI: https://doi.org/10.1016/j.heliyon.2020.e03175

Caporizzo MA, Prosser BL. The microtubule cytoskeleton in cardiac mechanics and heart failure. Nat Rev Cardiol. 2022;19(6):364-78. https://doi.org/10.1038/s41569-022-00692-y PMid: 35440741 DOI: https://doi.org/10.1038/s41569-022-00692-y

Goldblum RR, McClellan M, White K, Gonzalez SJ, Thompson BR, Vang HX, et al. Oxidative stress pathogenically remodels the cardiac myocyte cytoskeleton via structural alterations to the microtubule lattice. Dev Cell. 2021;56(15):2252-66.e6. https://doi.org/10.1016/j.devcel.2021.07.004 PMid:34343476 DOI: https://doi.org/10.1016/j.devcel.2021.07.004

Chen CY, Caporizzo MA, Bedi K, Vite A, Bogush AI, Robison P, et al. Suppression of detyrosinated microtubules improves cardiomyocyte function in human heart failure. Nat Med. 2018;24(8):1225-33. https://doi.org/10.1038/s41591-018-0046-2 PMid:29892068 DOI: https://doi.org/10.1038/s41591-018-0046-2

Caporizzo MA, Chen CY, Prosser BL. Cardiac microtubules in health and heart disease. Exp Biol Med (Maywood). 2019;244(15):1255-72. https://doi.org/10.1177/1535370219868960 PMid:31398994 DOI: https://doi.org/10.1177/1535370219868960

Gudimchuk NB, McIntosh JR. Regulation of microtubule dynamics, mechanics and function through the growing tip. Nat Rev Mol Cell Biol. 2021;22(12):777-95. https://doi.org/10.1038/s41580-021-00399-x PMid:34408299 DOI: https://doi.org/10.1038/s41580-021-00399-x

Roll-Mecak A. The tubulin code in microtubule dynamics and information encoding. Dev Cell. 2020;54(1):7-20. https://doi.org/10.1016/j.devcel.2020.06.008 PMid:32634400 DOI: https://doi.org/10.1016/j.devcel.2020.06.008

Zwetsloot AJ, Tut G, Straube A. Measuring microtubule dynamics. Essays Biochem. 2018;62(6):725-35. https://doi.org/10.1042/EBC20180035 PMid:30287587 DOI: https://doi.org/10.1042/EBC20180035

Sirajuddin M, Rice LM, Vale RD. Regulation of microtubule motors by tubulin isotypes and post-translational modifications. Nat Cell Biol. 2014;16(4):335-44. https://doi.org/10.1038/ncb2920 PMid:24633327 DOI: https://doi.org/10.1038/ncb2920

Scriven DR, Asghari P, Moore ED. Microarchitecture of the dyad. Cardiovasc Res. 2013;98(2):169-76. https://doi.org/10.1093/CVR/CVT025 PMid:23400762 DOI: https://doi.org/10.1093/cvr/cvt025

Vega AL, Yuan C, Votaw VS, Santana LF. Dynamic changes in sarcoplasmic reticulum structure in ventricular myocytes. J Biomed Biotechnol. 2011;2011:382586. https://doi.org/10.1155/2011/382586 PMid:22131804 DOI: https://doi.org/10.1155/2011/382586

Gross P, Johnson J, Romero CM, Eaton DM, Poulet C, Sanchez- Alonso J, et al. Interaction of the joining region in junctophilin-2 with the L-type Ca2+ channel is pivotal for cardiac dyad assembly and intracellular Ca2+ dynamics. Circ Res. 2021;128(1):92-114. https://doi.org/10.1161/CIRCRESAHA.119.315715 PMid:33092464 DOI: https://doi.org/10.1161/CIRCRESAHA.119.315715

Paschal BM, Shpetner HS, Vallee RB. MAP 1C is a microtubule- activated ATPase which translocates microtubules in vitro and has dynein-like properties. J Cell Biol. 1987;105(3):1273-82. https://doi.org/10.1083/JCB.105.3.1273 PMid:2958482 DOI: https://doi.org/10.1083/jcb.105.3.1273

Hu C, Tian Y, Xu H, Pan B, Terpstra EM, Wu P, et al. Inadequate ubiquitination-proteasome coupling contributes to myocardial ischemia-reperfusion injury. J Clin Invest. 2018;128(12):5294-306. https://doi.org/10.1172/JCI98287 PMid:30204128 DOI: https://doi.org/10.1172/JCI98287

Shaw RM, Fay AJ, Puthenveedu MA, von Zastrow M, Jan YN, Jan LY. Microtubule plus-end-tracking proteins target gap junctions directly from the cell interior to adherens junctions. Cell. 2007;128(3):547-60. https://doi.org/10.1016/J.CELL.2006.12.037 PMid:17289573 DOI: https://doi.org/10.1016/j.cell.2006.12.037

Macquart C, Jüttner R, Rodriguez BM, Le Dour C, Lefebvre F, Chatzifrangkeskou M, et al. Microtubule cytoskeleton regulates connexin 43 localization and cardiac conduction in cardiomyopathy caused by mutation in A-type lamins gene. Hum Mol Genet. 2019;28(24):4043-52. https://doi.org/10.1093/HMG/DDY227 PMid:29893868 DOI: https://doi.org/10.1093/hmg/ddy227

Smyth JW, Hong TT, Gao D, Vogan JM, Jensen BC, Fong TS, et al. Limited forward trafficking of connexin 43 reduces cell- cell coupling in stressed human and mouse myocardium. J Clin Invest. 2010;120(1):266-79. https://doi.org/10.1172/JCI39740 PMid:20038810 DOI: https://doi.org/10.1172/JCI39740

Denes LT, Kelley CP, Wang ET. Microtubule-based transport is essential to distribute RNA and nascent protein in skeletal muscle. Nat Commun. 2021;12(1):6079. https://doi.org/10.1038/S41467-021-26383-9 PMid:34707124 DOI: https://doi.org/10.1038/s41467-021-26383-9

Robison P, Caporizzo MA, Ahmadzadeh H, Bogush AI, Chen CY, Margulies KB, et al. Detyrosinated microtubules buckle and bear load in contracting cardiomyocytes. Science. 2016;352(6284):aaf0659. https://doi.org/10.1126/science.aaf0659 PMid:27102488 DOI: https://doi.org/10.1126/science.aaf0659

Caporizzo MA, Chen CY, Salomon AK, Margulies KB, Prosser BL. Microtubules provide a viscoelastic resistance to myocyte motion. Biophys J. 2018;115(9):1796-807. https://doi.org/10.1016/J.BPJ.2018.09.019 PMid:30322798 DOI: https://doi.org/10.1016/j.bpj.2018.09.019

Barmeyer A, Müllerleile K, Mortensen K, Meinertz T. Diastolic dysfunction in exercise and its role for exercise capacity. Heart Fail Rev. 2009;14(2):125-34. https://doi.org/10.1007/S10741-008-9105-Y PMid:18758943 DOI: https://doi.org/10.1007/s10741-008-9105-y

Lin Z, Gasic I, Chandrasekaran V, Peters N, Shao S, Mitchison TJ, et al. TTC5 mediates autoregulation of tubulin via mRNA degradation. Science. 2020;367(6473):100-4. https://doi.org/10.1126/science.aaz4352 PMid:31727855 DOI: https://doi.org/10.1126/science.aaz4352

Li L, Zhang Q, Zhang X, Zhang J, Wang X, Ren J, et al. Microtubule associated protein 4 phosphorylation leads to pathological cardiac remodeling in mice. EBioMedicine. 2018;37:221-35. https://doi.org/10.1016/j.ebiom.2018.10.017 PMid:30327268 DOI: https://doi.org/10.1016/j.ebiom.2018.10.017

Yu X, Chen X,Amrute-Nayak M,Allgeyer E, ZhaoA, Chenoweth H, et al. MARK4 controls ischaemic heart failure through microtubule detyrosination. Nature. 2021;594(7864):560-5. https://doi.org/10.1038/s41586-021-03573-5 PMid:34040253 DOI: https://doi.org/10.1038/s41586-021-03573-5

Imazio M, Nidorf M. Colchicine and the heart. Eur Heart J. 2021:42(28):2745-60. https://doi.org/10.1093/eurheartj/ehab221 PMid:33961006 DOI: https://doi.org/10.1093/eurheartj/ehab221

Fernández-Ruiz I. Targeting the cytoskeleton in heart failure. Nat Rev Cardiol. 2018;15:503. https://doi.org/10.1038/s41569-018-0056-2 DOI: https://doi.org/10.1038/s41569-018-0056-2

Leung YY, Hui LL, Kraus VB. Colchicine--update on mechanisms of action and therapeutic uses. Semin Arthritis Rheum. 2015;45(3):341-50. https://doi.org/10.1016/j.semarthrit.2015.06.013 PMid:26228647 DOI: https://doi.org/10.1016/j.semarthrit.2015.06.013

Chaldakov GN. Colchicine, a microtubule-disassembling drug, in the therapy of cardiovascular diseases. Cell Biol Int. 2018;42(8):1079-84. https://doi.org/10.1002/cbin.10988 PMid:29762881 DOI: https://doi.org/10.1002/cbin.10988

Fujisue K, Sugamura K, Kurokawa H, Matsubara J, Ishii M, Izumiya Y, et al. Colchicine improves survival, left ventricular remodeling, and chronic cardiac function after acute myocardial infarction. Circ J. 2017;81(8):1174-82. https://doi.org/10.1253/circj.CJ-16-0949 PMid:28420825 DOI: https://doi.org/10.1253/circj.CJ-16-0949

Robison P, Prosser BL. Microtubule mechanics in the working myocyte. J Physiol. 2017;595(12):3931-7. https://doi.org/10.1113/JP273046 PMid:28116814 DOI: https://doi.org/10.1113/JP273046

Chen CY, Salomon AK, Caporizzo MA, Curry S, Kelly NA, Bedi K, et al. Depletion of vasohibin 1 speeds contraction and relaxation in failing human cardiomyocytes. Circ Res. 2020;127(2):e14-27. https://doi.org/10.1161/CIRCRESAHA.119.315947 PMid:32272864 DOI: https://doi.org/10.1161/CIRCRESAHA.119.315947

Kerr JP, Robison P, Shi G, Bogush AI, Kempema AM, Hexum JK, et al. Detyrosinated microtubules modulate mechanotransduction in heart and skeletal muscle. Nat Commun. 2015;6:8526. https://doi.org/10.1038/ncomms9526 PMid:26446751 DOI: https://doi.org/10.1038/ncomms9526

Curry EA 3rd, Murry DJ, Yoder C, Fife K, Armstrong V, Nakshatri H, et al. Phase I dose escalation trial of feverfew with standardized doses of parthenolide in patients with cancer. Invest New Drugs. 2004;22(3):299-305. https://doi. org/10.1023/B:DRUG.0000026256.38560.be PMid:15122077 DOI: https://doi.org/10.1023/B:DRUG.0000026256.38560.be

Kurdi M, Bowers MC, Dado J, Booz GW. Parthenolide induces a distinct pattern of oxidative stress in cardiac myocytes. Free Radic Biol Med. 2007;42(4):474-81. https://doi.org/10.1016/j.freeradbiomed.2006.11.012 PMid:17275679 DOI: https://doi.org/10.1016/j.freeradbiomed.2006.11.012