Cardiomyocyte Microtubules: Control of Mechanics, Transport, and Remodeling

Literature Cited

1. 1. 

   Straub F. 1942. Actin. Stud. Inst. Med. Chem. Univ. Szeged 2:3–15
   [Google Scholar]
2. 2. 

   Szent-Györgyi A. 1942. Discussion. Stud. Inst. Med. Chem. Univ. Szeged 1:67–71
   [Google Scholar]
3. 3. 

   Huxley H, Hanson J. 1954. Changes in the cross-striations of muscle during contraction and stretch and their structural interpretation. Nature 173:973–76
   [Google Scholar]
4. 4. 

   Huxley AF, Niedergerke R. 1954. Structural changes in muscle during contraction; interference microscopy of living muscle fibres. Nature 173:971–73
   [Google Scholar]
5. 5. 

   Manton I, Clarke B 1952. An electron microscope study of the spermatozoid of sphagnum. J. Exp. Bot. 3:265–75
   [Google Scholar]
6. 6. 

   Fawcett DW, Porter KR. 1954. A study of the fine structure of ciliated epithelia. J. Morphol. 94:221–81
   [Google Scholar]
7. 7. 

   Page E. 1967. Tubular systems in Purkinje cells of the cat heart. J. Ultrastruct. Res. 17:72–83
   [Google Scholar]
8. 8. 

   Zebrowski DC, Vergarajauregui S, Wu CC, Piatkowski T, Becker R et al. 2015. Developmental alterations in centrosome integrity contribute to the post-mitotic state of mammalian cardiomyocytes. eLife 4:05563
   [Google Scholar]
9. 9. 

   Goldstein MA, Entman ML. 1979. Microtubules in mammalian heart muscle. J. Cell Biol. 80:183–95
   [Google Scholar]
10. 10. 

    Mandelkow EM, Mandelkow E, Milligan RA 1991. Microtubule dynamics and microtubule caps: a time-resolved cryo-electron microscopy study. J. Cell Biol. 114:977–91
    [Google Scholar]
11. 11. 

    Chrétien D, Fuller SD, Karsenti E. 1995. Structure of growing microtubule ends: two-dimensional sheets close into tubes at variable rates. J. Cell Biol. 129:1311–28
    [Google Scholar]
12. 12. 

    Mitchison T, Kirschner M. 1984. Dynamic instability of microtubule growth. Nature 312:237–42
    [Google Scholar]
13. 13. 

    Inoué S, Sato H. 1967. Cell motility by labile association of molecules. The nature of mitotic spindle fibers and their role in chromosome movement. J. Gen. Physiol. 50:Suppl.259–92
    [Google Scholar]
14. 14. 

    Aillaud C, Bosc C, Peris L, Bosson A, Heemeryck P et al. 2017. Vasohibins/SVBP are tubulin carboxypeptidases (TCPs) that regulate neuron differentiation. Science 358:1448–53
    [Google Scholar]
15. 15. 

    Robison P, Caporizzo MA, Ahmadzadeh H, Bogush AI, Chen CY et al. 2016. Detyrosinated microtubules buckle and bear load in contracting cardiomyocytes. Science 352:aaf0659
    [Google Scholar]
16. 16. 

    Redeker V. 2010. Mass spectrometry analysis of C-terminal posttranslational modifications of tubulins. Methods Cell Biol. 95:77–103
    [Google Scholar]
17. 17. 

    Chen CY, Caporizzo MA, Bedi K, Vite A, Bogush AI et al. 2018. Suppression of detyrosinated microtubules improves cardiomyocyte function in human heart failure. Nat. Med. 24:1225–33
    [Google Scholar]
18. 18. 

    Howes SC, Alushin GM, Shida T, Nachury MV, Nogales E. 2014. Effects of tubulin acetylation and tubulin acetyltransferase binding on microtubule structure. Mol. Biol. Cell 25:257–66
    [Google Scholar]
19. 19. 

    Xu Z, Schaedel L, Portran D, Aguilar A, Gaillard J et al. 2017. Microtubules acquire resistance from mechanical breakage through intralumenal acetylation. Science 356:328–32
    [Google Scholar]
20. 20. 

    Johnson V, Ayaz P, Huddleston P, Rice LM. 2011. Design, overexpression, and purification of polymerization-blocked yeast αβ-tubulin mutants. Biochemistry 50:8636–44
    [Google Scholar]
21. 21. 

    Ti SC, Wieczorek M, Kapoor TM. 2020. Purification of affinity tag-free recombinant tubulin from insect cells. STAR Protoc. 1:100011
    [Google Scholar]
22. 22. 

    Mallik R, Gross SP. 2004. Molecular motors: strategies to get along. Curr. Biol. 14:R971–82
    [Google Scholar]
23. 23. 

    Hendricks AG, Perlson E, Ross JL, Schroeder HW, Tokito M, Holzbaur EL 2010. Motor coordination via a tug-of-war mechanism drives bidirectional vesicle transport. Curr. Biol. 20:697–702
    [Google Scholar]
24. 24. 

    Shubeita GT, Tran SL, Xu J, Vershinin M, Cermelli S et al. 2008. Consequences of motor copy number on the intracellular transport of kinesin-1-driven lipid droplets. Cell 135:1098–107
    [Google Scholar]
25. 25. 

    Cai D, McEwen DP, Martens JR, Meyhofer E, Verhey KJ 2009. Single molecule imaging reveals differences in microtubule track selection between Kinesin motors. PLOS Biol 7:e1000216
    [Google Scholar]
26. 26. 

    Reed NA, Cai D, Blasius TL, Jih GT, Meyhofer E et al. 2006. Microtubule acetylation promotes kinesin-1 binding and transport. Curr. Biol. 16:2166–72
    [Google Scholar]
27. 27. 

    Tsutsui H, Ishihara K, Cooper G. 1993. Cytoskeletal role in the contractile dysfunction of hypertrophied myocardium. Science 260:682–87
    [Google Scholar]
28. 28. 

    Cooper G. 2000. Cardiocyte cytoskeleton in hypertrophied myocardium. Heart Fail. Rev. 5:187–201
    [Google Scholar]
29. 29. 

    Collins JF, Pawloski-Dahm C, Davis MG, Ball N, Dorn GW, Walsh RA. 1996. The role of the cytoskeleton in left ventricular pressure overload hypertrophy and failure. J. Mol. Cell. Cardiol. 28:1435–43
    [Google Scholar]
30. 30. 

    Wang X, Li F, Campbell SE, Gerdes AM. 1999. Chronic pressure overload cardiac hypertrophy and failure in guinea pigs: II. Cytoskeletal remodeling. J. Mol. Cell. Cardiol. 31:319–31
    [Google Scholar]
31. 31. 

    Konieczny P, Fuchs P, Reipert S, Kunz WS, Zeöld A et al. 2008. Myofiber integrity depends on desmin network targeting to Z-disks and costameres via distinct plectin isoforms. J. Cell Biol. 181:667–81
    [Google Scholar]
32. 32. 

    Gittes F, Mickey B, Nettleton J, Howard J 1993. Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape. J. Cell Biol. 120:923–34
    [Google Scholar]
33. 33. 

    Li T. 2008. A mechanics model of microtubule buckling in living cells. J. Biomech. 41:1722–29
    [Google Scholar]
34. 34. 

    Soheilypour M, Peyro M, Peter SJ, Mofrad MRK. 2015. Buckling behavior of individual and bundled microtubules. Biophys. J. 108:1718–26
    [Google Scholar]
35. 35. 

    Brangwynne CP, MacKintosh FC, Kumar S, Geisse NA, Talbot J et al. 2006. Microtubules can bear enhanced compressive loads in living cells because of lateral reinforcement. J. Cell Biol. 173:733–41
    [Google Scholar]
36. 36. 

    Helmes M, Najafi A, Palmer BM, Breel E, Rijnveld N et al. 2016. Mimicking the cardiac cycle in intact cardiomyocytes using diastolic and systolic force clamps; measuring power output. Cardiovasc. Res. 111:66–73
    [Google Scholar]
37. 37. 

    Caporizzo MA, Chen CY, Bedi K, Margulies KB, Prosser BL. 2020. Microtubules increase diastolic stiffness in failing human cardiomyocytes and myocardium. Circulation 141:902–15
    [Google Scholar]
38. 38. 

    Schuldt M, Pei J, Harakalova M, Dorsch LM, Schlossarek S et al. 2021. Proteomic and functional studies reveal detyrosinated tubulin as treatment target in sarcomere mutation-induced hypertrophic cardio-myopathy. Circ. Heart Fail. 14:e007022
    [Google Scholar]
39. 39. 

    Kreitzer G, Liao G, Gundersen GG. 1999. Detyrosination of tubulin regulates the interaction of intermediate filaments with microtubules in vivo via a kinesin-dependent mechanism. Mol. Biol. Cell 10:1105–18
    [Google Scholar]
40. 40. 

    Granzier HL, Irving TC. 1995. Passive tension in cardiac muscle: contribution of collagen, titin, microtubules, and intermediate filaments. Biophys. J. 68:1027–44
    [Google Scholar]
41. 41. 

    Caporizzo MA, Chen CY, Salomon AK, Margulies KB, Prosser BL. 2018. Microtubules provide a viscoelastic resistance to myocyte motion. Biophys. J. 115:1796–807
    [Google Scholar]
42. 42. 

    Caporizzo MA, Chen CY, Prosser BL. 2019. Cardiac microtubules in health and heart disease. Exp. Biol. Med. 244:1255–72
    [Google Scholar]
43. 43. 

    Harris TS, Baicu CF, Conrad CH, Koide M, Buckley JM et al. 2002. Constitutive properties of hypertrophied myocardium: cellular contribution to changes in myocardial stiffness. Am. J. Physiol. Heart Circ. Physiol. 282:H2173–82
    [Google Scholar]
44. 44. 

    Linke WA, Fernandez JM. 2002. Cardiac titin: molecular basis of elasticity and cellular contribution to elastic and viscous stiffness components in myocardium. J. Muscle Res. Cell Motil. 23:483–97
    [Google Scholar]
45. 45. 

    Bollen IAE, van der Meulen M, de Goede K, Kuster DWD, Dalinghaus M, van der Velden J. 2017. Cardiomyocyte hypocontractility and reduced myofibril density in end-stage pediatric cardiomyopathy. Front. Physiol. 8:1103
    [Google Scholar]
46. 46. 

    Witjas-Paalberends ER, Piroddi N, Stam K, van Dijk SJ, Oliviera VS et al. 2013. Mutations in MYH7 reduce the force generating capacity of sarcomeres in human familial hypertrophic cardiomyopathy. Cardiovasc. Res. 99:432–41
    [Google Scholar]
47. 47. 

    Zile MR, Green GR, Schuyler GT, Aurigemma GP, Miller DC, Cooper G. 2001. Cardiocyte cytoskeleton in patients with left ventricular pressure overload hypertrophy. J. Am. Coll. Cardiol. 37:1080–84
    [Google Scholar]
48. 48. 

    Swiatlowska P, Sanchez-Alonso JL, Wright PT, Novak P, Gorelik J. 2020. Microtubules regulate cardiomyocyte transversal Young's modulus. PNAS 117:2764–66
    [Google Scholar]
49. 49. 

    Fassett J, Xu X, Kwak D, Zhu G, Fassett EK et al. 2019. Adenosine kinase attenuates cardiomyocyte microtubule stabilization and protects against pressure overload-induced hypertrophy and LV dysfunction. J. Mol. Cell. Cardiol. 130:49–58
    [Google Scholar]
50. 50. 

    Tagawa H, Koide M, Sato H, Zile MR, Carabello BA, Cooper G. 1998. Cytoskeletal role in the transition from compensated to decompensated hypertrophy during adult canine left ventricular pressure overloading. Circ. Res. 82:751–61
    [Google Scholar]
51. 51. 

    Chen CY, Salomon AK, Caporizzo MA, Curry S, Kelly NA et al. 2020. Depletion of vasohibin 1 speeds contraction and relaxation in failing human cardiomyocytes. Circ. Res. 127:e14–27
    [Google Scholar]
52. 52. 

    Margulies KB, Prosser BL. 2021. Tubulin detyrosination: an emerging therapeutic target in hypertrophic cardiomyopathy. Circ. Heart Fail. 14:e008006
    [Google Scholar]
53. 53. 

    Sato H, Nagai T, Kuppuswamy D, Narishige T, Koide M et al. 1997. Microtubule stabilization in pressure overload cardiac hypertrophy. J. Cell Biol. 139:963–73
    [Google Scholar]
54. 54. 

    Liu Y, Morley M, Brandimarto J, Hannenhalli S, Hu Y et al. 2015. RNA-Seq identifies novel myocardial gene expression signatures of heart failure. Genomics 105:83–89
    [Google Scholar]
55. 55. 

    Doroudgar S, Hofmann C, Boileau E, Malone B, Riechert E et al. 2019. Monitoring cell-type-specific gene expression using ribosome profiling in vivo during cardiac hemodynamic stress. Circ. Res. 125:431–48
    [Google Scholar]
56. 56. 

    Takahashi M, Shiraishi H, Ishibashi Y, Blade KL, McDermott PJ et al. 2003. Phenotypic consequences of β1-tubulin expression and MAP4 decoration of microtubules in adult cardiocytes. Am. J. Physiol. Heart Circ. Physiol. 285:H2072–83
    [Google Scholar]
57. 57. 

    Li L, Zhang Q, Zhang X, Zhang J, Wang X et al. 2018. Microtubule associated protein 4 phosphorylation leads to pathological cardiac remodeling in mice. EBioMedicine 37:221–35
    [Google Scholar]
58. 58. 

    Chinnakkannu P, Samanna V, Cheng G, Ablonczy Z, Baicu CF et al. 2010. Site-specific microtubule-associated protein 4 dephosphorylation causes microtubule network densification in pressure overload cardiac hypertrophy. J. Biol. Chem. 285:21837–48
    [Google Scholar]
59. 59. 

    Hejnowicz Z, Rusin A, Rusin T. 2000. Tensile tissue stress affects the orientation of cortical microtubules in the epidermis of sunflower hypocotyl. J. Plant Growth Regul. 19:31–44
    [Google Scholar]
60. 60. 

    Kaverina I, Krylyshkina O, Beningo K, Anderson K, Wang YL, Small JV 2002. Tensile stress stimulates microtubule outgrowth in living cells. J. Cell Sci. 115:2283–91
    [Google Scholar]
61. 61. 

    Kabir AM, Inoue D, Hamano Y, Mayama H, Sada K, Kakugo A 2014. Biomolecular motor modulates mechanical property of microtubule. Biomacromolecules 15:1797–805
    [Google Scholar]
62. 62. 

    Peris L, Wagenbach M, Lafanechère L, Brocard J, Moore AT et al. 2009. Motor-dependent microtubule disassembly driven by tubulin tyrosination. J. Cell Biol. 185:1159–66
    [Google Scholar]
63. 63. 

    Schaedel L, John K, Gaillard J, Nachury MV, Blanchoin L, Théry M. 2015. Microtubules self-repair in response to mechanical stress. Nat. Mater. 14:1156–63
    [Google Scholar]
64. 64. 

    Portran D, Schaedel L, Xu Z, Théry M, Nachury MV. 2017. Tubulin acetylation protects long-lived microtubules against mechanical ageing. Nat. Cell Biol. 19:391–98
    [Google Scholar]
65. 65. 

    Vemu A, Szczesna E, Zehr EA, Spector JO, Grigorieff N et al. 2018. Severing enzymes amplify microtubule arrays through lattice GTP-tubulin incorporation. Science 361:eaau1504
    [Google Scholar]
66. 66. 

    Prosser BL, Ward CW, Lederer WJ. 2011. X-ROS signaling: rapid mechano-chemo transduction in heart. Science 333:1440–45
    [Google Scholar]
67. 67. 

    Khairallah RJ, Shi G, Sbrana F, Prosser BL, Borroto C et al. 2012. Microtubules underlie dysfunction in Duchenne muscular dystrophy. Sci. Signal. 5:ra56
    [Google Scholar]
68. 68. 

    Lyons JS, Joca HC, Law RA, Williams KM, Kerr JP et al. 2017. Microtubules tune mechanotransduction through NOX2 and TRPV4 to decrease sclerostin abundance in osteocytes. Sci. Signal. 10:eaan5748
    [Google Scholar]
69. 69. 

    Pratt SJP, Lee RM, Chang KT, Hernández-Ochoa EO, Annis DA et al. 2020. Mechanoactivation of NOX2-generated ROS elicits persistent TRPM8 Ca. PNAS 117:26008–19
    [Google Scholar]
70. 70. 

    Kim JC, Wang J, Son MJ, Woo SH 2017. Shear stress enhances Ca²⁺ sparks through Nox2-dependent mitochondrial reactive oxygen species generation in rat ventricular myocytes. Biochim. Biophys. Acta Mol. Cell Res. 1864:1121–31
    [Google Scholar]
71. 71. 

    Viner H, Nitsan I, Sapir L, Drori S, Tzlil S. 2019. Mechanical communication acts as a noise filter. iScience 14:58–68
    [Google Scholar]
72. 72. 

    Kerr JP, Robison P, Shi G, Bogush AI, Kempema AM et al. 2015. Detyrosinated microtubules modulate mechanotransduction in heart and skeletal muscle. Nat. Commun. 6:8526
    [Google Scholar]
73. 73. 

    Jiang F, Yin K, Wu K, Zhang M, Wang S et al. 2021. The mechanosensitive Piezo1 channel mediates heart mechano-chemo transduction. Nat. Commun. 12:869
    [Google Scholar]
74. 74. 

    Chen F, Barman S, Yu Y, Haigh S, Wang Y et al. 2014. Caveolin-1 is a negative regulator of NADPH oxidase-derived reactive oxygen species. Free Radic. Biol. Med. 73:201–13
    [Google Scholar]
75. 75. 

    Mundy DI, Machleidt T, Ying YS, Anderson RG, Bloom GS 2002. Dual control of caveolar membrane traffic by microtubules and the actin cytoskeleton. J. Cell Sci. 115:4327–39
    [Google Scholar]
76. 76. 

    Veteto AB, Peana D, Lambert MD, McDonald KS, Domeier TL. 2020. Transient receptor potential vanilloid-4 contributes to stretch-induced hypercontractility and time-dependent dysfunction in the aged heart. Cardiovasc. Res. 116:1887–96
    [Google Scholar]
77. 77. 

    Yan C, Wang F, Peng Y, Williams CR, Jenkins B et al. 2018. Microtubule acetylation is required for mechanosensation in Drosophila. Cell Rep 25:1051–65.e6
    [Google Scholar]
78. 78. 

    Jian Z, Han H, Zhang T, Puglisi J, Izu LT et al. 2014. Mechanochemotransduction during cardio-myocyte contraction is mediated by localized nitric oxide signaling. Sci. Signal. 7:ra27
    [Google Scholar]
79. 79. 

    Chiou KK, Rocks JW, Chen CY, Cho S, Merkus KE et al. 2016. Mechanical signaling coordinates the embryonic heartbeat. PNAS 113:8939–44
    [Google Scholar]
80. 80. 

    Scopacasa BS, Teixeira VP, Franchini KG. 2003. Colchicine attenuates left ventricular hypertrophy but preserves cardiac function of aortic-constricted rats. J. Appl. Physiol. 94:1627–33
    [Google Scholar]
81. 81. 

    Tsutsui H, Ishibashi Y, Takahashi M, Namba T, Tagawa H et al. 1999. Chronic colchicine administration attenuates cardiac hypertrophy in spontaneously hypertensive rats. J. Mol. Cell. Cardiol. 31:1203–13
    [Google Scholar]
82. 82. 

    Scarborough EA, Uchida K, Vogel M, Erlitzki N, Iyer M et al. 2021. Microtubules orchestrate local translation to enable cardiac growth. Nat. Commun. 12:1547
    [Google Scholar]
83. 83. 

    Russell B, Dix DJ 1992. Mechanisms for intracellular distribution of mRNA: in situ hybridization studies in muscle. Am. J. Physiol. 262:C1–8
    [Google Scholar]
84. 84. 

    Scholz D, McDermott P, Garnovskaya M, Gallien TN, Huettelmaier S et al. 2006. Microtubule-associated protein-4 (MAP-4) inhibits microtubule-dependent distribution of mRNA in isolated neonatal cardiocytes. Cardiovasc. Res. 71:506–16
    [Google Scholar]
85. 85. 

    Perhonen M, Sharp WW, Russell B. 1998. Microtubules are needed for dispersal of α-myosin heavy chain mRNA in rat neonatal cardiac myocytes. J. Mol. Cell. Cardiol. 30:1713–22
    [Google Scholar]
86. 86. 

    Lewis YE, Moskovitz A, Mutlak M, Heineke J, Caspi LH, Kehat I. 2018. Localization of transcripts, translation, and degradation for spatiotemporal sarcomere maintenance. J. Mol. Cell. Cardiol. 116:16–28
    [Google Scholar]
87. 87. 

    Sussman MA, Sakhi S, Barrientos P, Ito M, Kedes L. 1994. Tropomodulin in rat cardiac muscle. Localization of protein is independent of messenger RNA distribution during myofibrillar development. Circ. Res. 75:221–32
    [Google Scholar]
88. 88. 

    Rudolph F, Hüttemeister J, da Silva Lopes K, Jüttner R, Yu L et al. 2019. Resolving titin's lifecycle and the spatial organization of protein turnover in mouse cardiomyocytes. PNAS 116:25126–36
    [Google Scholar]
89. 89. 

    Fusco D, Accornero N, Lavoie B, Shenoy SM, Blanchard JM et al. 2003. Single mRNA molecules demonstrate probabilistic movement in living mammalian cells. Curr. Biol. 13:161–67
    [Google Scholar]
90. 90. 

    Bullock SL, Nicol A, Gross SP, Zicha D. 2006. Guidance of bidirectional motor complexes by mRNA cargoes through control of dynein number and activity. Curr. Biol. 16:1447–52
    [Google Scholar]
91. 91. 

    Macdonald PM, Struhl G. 1988. Cis-acting sequences responsible for anterior localization of bicoid mRNA in Drosophila embryos. Nature 336:595–98
    [Google Scholar]
92. 92. 

    Gavis ER, Lehmann R. 1992. Localization of nanos RNA controls embryonic polarity. Cell 71:301–13
    [Google Scholar]
93. 93. 

    Singer RH. 1993. RNA zipcodes for cytoplasmic addresses. Curr. Biol. 3:719–21
    [Google Scholar]
94. 94. 

    Jackson RJ. 1993. Cytoplasmic regulation of mRNA function: the importance of the 3′ untranslated region. Cell 74:9–14
    [Google Scholar]
95. 95. 

    Besse F, Ephrussi A. 2008. Translational control of localized mRNAs: restricting protein synthesis in space and time. Nat. Rev. Mol. Cell Biol. 9:971–80
    [Google Scholar]
96. 96. 

    Capri M, Santoni MJ, Thomas-Delaage M, Aït-Ahmed O. 1997. Implication of a 5′ coding sequence in targeting maternal mRNA to the Drosophila oocyte. Mech. Dev. 68:91–100
    [Google Scholar]
97. 97. 

    Serano TL, Cohen RS. 1995. A small predicted stem-loop structure mediates oocyte localization of Drosophila K10 mRNA. Development 121:3809–18
    [Google Scholar]
98. 98. 

    Thio GL, Ray RP, Barcelo G, Schüpbach T. 2000. Localization of gurken RNA in Drosophila oogenesis requires elements in the 5′ and 3′ regions of the transcript. Dev. Biol. 221:435–46
    [Google Scholar]
99. 99. 

    Wang T, Hamilla S, Cam M, Aranda-Espinoza H, Mili S. 2017. Extracellular matrix stiffness and cell contractility control RNA localization to promote cell migration. Nat. Commun. 8:896
    [Google Scholar]
100. 100. 

     Messitt TJ, Gagnon JA, Kreiling JA, Pratt CA, Yoon YJ, Mowry KL. 2008. Multiple kinesin motors coordinate cytoplasmic RNA transport on a subpopulation of microtubules in Xenopus oocytes. Dev. Cell 15:426–36
     [Google Scholar]
101. 101. 

     Goldspink P, Sharp W, Russell B. 1997. Localization of cardiac (alpha)-myosin heavy chain mRNA is regulated by its 3′ untranslated region via mechanical activity and translational block. J. Cell Sci. 110:Part 232969–78
     [Google Scholar]
102. 102. 

     Lécuyer E, Yoshida H, Parthasarathy N, Alm C, Babak T et al. 2007. Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. Cell 131:174–87
     [Google Scholar]
103. 103. 

     Fazal FM, Han S, Parker KR, Kaewsapsak P, Xu J et al. 2019. Atlas of subcellular RNA localization revealed by APEX-seq. Cell 178:473–90.e26
     [Google Scholar]
104. 104. 

     Medioni C, Mowry K, Besse F. 2012. Principles and roles of mRNA localization in animal development. Development 139:3263–76
     [Google Scholar]
105. 105. 

     Mingle LA, Okuhama NN, Shi J, Singer RH, Condeelis J, Liu G 2005. Localization of all seven messenger RNAs for the actin-polymerization nucleator Arp2/3 complex in the protrusions of fibroblasts. J. Cell Sci. 118:2425–33
     [Google Scholar]
106. 106. 

     Isaacs WB, Cook RK, Van Atta JC, Redmond CM, Fulton AB 1989. Assembly of vimentin in cultured cells varies with cell type. J. Biol. Chem. 264:17953–60
     [Google Scholar]
107. 107. 

     L'Ecuyer TJ, Noller JA, Fulton AB 1998. Assembly of tropomyosin isoforms into the cytoskeleton of avian muscle cells. Pediatr. Res. 43:813–22
     [Google Scholar]
108. 108. 

     Fulton AB, Alftine C. 1997. Organization of protein and mRNA for titin and other myofibril components during myofibrillogenesis in cultured chicken skeletal muscle. Cell Struct. Funct. 22:51–58
     [Google Scholar]
109. 109. 

     Isaacs WB, Fulton AB. 1987. Cotranslational assembly of myosin heavy chain in developing cultured skeletal muscle. PNAS 84:6174–78
     [Google Scholar]
110. 110. 

     Rui Y, Bai J, Perrimon N. 2010. Sarcomere formation occurs by the assembly of multiple latent protein complexes. PLOS Genet 6:e1001208
     [Google Scholar]
111. 111. 

     Lu MH, DiLullo C, Schultheiss T, Holtzer S, Murray JM et al. 1992. The vinculin/sarcomeric-alpha-actinin/alpha-actin nexus in cultured cardiac myocytes. J. Cell Biol. 117:1007–22
     [Google Scholar]
112. 112. 

     Montag J, Kraft T. 2020. Stochastic allelic expression as trigger for contractile imbalance in hypertrophic cardiomyopathy. Biophys. Rev. 12:1055–64
     [Google Scholar]
113. 113. 

     Yu JG, Thornell LE. 2002. Desmin and actin alterations in human muscles affected by delayed onset muscle soreness: a high resolution immunocytochemical study. Histochem. Cell Biol. 118:171–79
     [Google Scholar]
114. 114. 

     Yu JG, Russell B 2005. Cardiomyocyte remodeling and sarcomere addition after uniaxial static strain in vitro. J. Histochem. Cytochem. 53:839–44
     [Google Scholar]
115. 115. 

     Stout AL, Wang J, Sanger JM, Sanger JW 2008. Tracking changes in Z-band organization during myofibrillogenesis with FRET imaging. Cell Motil. Cytoskelet. 65:353–67
     [Google Scholar]
116. 116. 

     Yang H, Schmidt LP, Wang Z, Yang X, Shao Y et al. 2016. Dynamic myofibrillar remodeling in live cardiomyocytes under static stretch. Sci. Rep. 6:20674
     [Google Scholar]
117. 117. 

     Kislauskis EH, Zhu X, Singer RH. 1997. β-Actin messenger RNA localization and protein synthesis augment cell motility. J. Cell Biol. 136:1263–70
     [Google Scholar]
118. 118. 

     Tigchelaar W, de Jong AM, Bloks VW, van Gilst WH, de Boer RA, Silljé HH. 2016. Hypertrophy induced KIF5B controls mitochondrial localization and function in neonatal rat cardiomyocytes. J. Mol. Cell. Cardiol. 97:70–81
     [Google Scholar]
119. 119. 

     Willis MS, Schisler JC, Portbury AL, Patterson C. 2009. Build it up—tear it down: protein quality control in the cardiac sarcomere. Cardiovasc. Res. 81:439–48
     [Google Scholar]
120. 120. 

     Gupta I, Varshney NK, Khan S. 2018. Emergence of members of TRAF and DUB of ubiquitin proteasome system in the regulation of hypertrophic cardiomyopathy. Front. Genet. 9:336
     [Google Scholar]
121. 121. 

     Smyth JW, Hong TT, Gao D, Vogan JM, Jensen BC et al. 2010. Limited forward trafficking of connexin 43 reduces cell-cell coupling in stressed human and mouse myocardium. J. Clin. Investig. 120:266–79
     [Google Scholar]
122. 122. 

     Ponce-Balbuena D, Guerrero-Serna G, Valdivia CR, Caballero R, Diez-Guerra FJ et al. 2018. Cardiac Kir2.1 and Na_V1.5 channels traffic together to the sarcolemma to control excittability. Circ. Res. 122:1501–16
     [Google Scholar]
123. 123. 

     Pérez-Hernández M, Matamoros M, Alfayate S, Nieto-Marín P, Utrilla RG et al. 2018. Brugada syndrome trafficking-defective Nav1.5 channels can trap cardiac Kir2.1/2.2 channels. JCI Insight 3:e96291
     [Google Scholar]
124. 124. 

     Doroudgar S, Glembotski CC. 2013. New concepts of endoplasmic reticulum function in the heart: programmed to conserve. J. Mol. Cell. Cardiol. 55:85–91
     [Google Scholar]
125. 125. 

     Kaisto T, Metsikkö K. 2003. Distribution of the endoplasmic reticulum and its relationship with the sarcoplasmic reticulum in skeletal myofibers. Exp. Cell Res. 289:47–57
     [Google Scholar]
126. 126. 

     Balse E, Steele DF, Abriel H, Coulombe A, Fedida D, Hatem SN. 2012. Dynamic of ion channel expression at the plasma membrane of cardiomyocytes. Physiol. Rev. 92:1317–58
     [Google Scholar]
127. 127. 

     Steele DF, Eldstrom J, Fedida D. 2007. Mechanisms of cardiac potassium channel trafficking. J. Physiol. 582:17–26
     [Google Scholar]
128. 128. 

     Zadeh AD, Cheng Y, Xu H, Wong N, Wang Z et al. 2009. Kif5b is an essential forward trafficking motor for the Kv1.5 cardiac potassium channel. J. Physiol. 587:4565–74
     [Google Scholar]
129. 129. 

     Choi WS, Khurana A, Mathur R, Viswanathan V, Steele DF, Fedida D. 2005. Kv1.5 surface expression is modulated by retrograde trafficking of newly endocytosed channels by the dynein motor. Circ. Res. 97:363–71
     [Google Scholar]
130. 130. 

     Loewen ME, Wang Z, Eldstrom J, Dehghani Zadeh A, Khurana A et al. 2009. Shared requirement for dynein function and intact microtubule cytoskeleton for normal surface expression of cardiac potassium channels. Am. J. Physiol. Heart Circ. Physiol. 296:H71–83
     [Google Scholar]
131. 131. 

     Kirschner M, Mitchison T. 1986. Beyond self-assembly: from microtubules to morphogenesis. Cell 45:329–42
     [Google Scholar]
132. 132. 

     Mimori-Kiyosue Y, Tsukita S. 2003.. “ Search-and-capture” of microtubules through plus-end-binding proteins (+TIPs). J. Biochem. 134:321–26
     [Google Scholar]
133. 133. 

     Shaw RM, Fay AJ, Puthenveedu MA, von Zastrow M, Jan YN, Jan LY 2007. Microtubule plus-end-tracking proteins target gap junctions directly from the cell interior to adherens junctions. Cell 128:547–60
     [Google Scholar]
134. 134. 

     Hong TT, Smyth JW, Gao D, Chu KY, Vogan JM et al. 2010. BIN1 localizes the L-type calcium channel to cardiac T-tubules. PLOS Biol 8:e1000312
     [Google Scholar]
135. 135. 

     Patel MB, Stewart JM, Loud AV, Anversa P, Wang J et al. 1991. Altered function and structure of the heart in dogs with chronic elevation in plasma norepinephrine. Circulation 84:2091–100
     [Google Scholar]
136. 136. 

     Agullo-Pascual E, Lin X, Leo-Macias A, Zhang M, Liang FX et al. 2014. Super-resolution imaging reveals that loss of the C-terminus of connexin43 limits microtubule plus-end capture and Na_V1.5 localization at the intercalated disc. Cardiovasc. Res. 104:371–81
     [Google Scholar]
137. 137. 

     Basheer WA, Shaw RM. 2016. Connexin 43 and CaV1.2 ion channel trafficking in healthy and diseased myocardium. Circ. Arrhythm. Electrophysiol. 9:e001357
     [Google Scholar]
138. 138. 

     Meunier B, Quaranta M, Daviet L, Hatzoglou A, Leprince C. 2009. The membrane-tubulating potential of amphiphysin 2/BIN1 is dependent on the microtubule-binding cytoplasmic linker protein 170 (CLIP-170). Eur. J. Cell Biol. 88:91–102
     [Google Scholar]
139. 139. 

     D'Alessandro M, Hnia K, Gache V, Koch C, Gavriilidis C et al. 2015. Amphiphysin 2 orchestrates nucleus positioning and shape by linking the nuclear envelope to the actin and microtubule cytoskeleton. Dev. Cell 35:186–98
     [Google Scholar]
140. 140. 

     Terasaki M, Chen LB, Fujiwara K 1986. Microtubules and the endoplasmic reticulum are highly interdependent structures. J. Cell Biol. 103:1557–68
     [Google Scholar]
141. 141. 

     Nixon-Abell J, Obara CJ, Weigel AV, Li D, Legant WR et al. 2016. Increased spatiotemporal resolution reveals highly dynamic dense tubular matrices in the peripheral ER. Science 354:aaf3928
     [Google Scholar]
142. 142. 

     Vega AL, Yuan C, Votaw VS, Santana LF. 2011. Dynamic changes in sarcoplasmic reticulum structure in ventricular myocytes. J. Biomed. Biotechnol. 2011:382586
     [Google Scholar]
143. 143. 

     Drum BM, Yuan C, de la Mata A, Grainger N, Santana LF. 2020. Junctional sarcoplasmic reticulum motility in adult mouse ventricular myocytes. Am. J. Physiol. Cell Physiol. 318:C598–604
     [Google Scholar]
144. 144. 

     Osseni A, Sébastien M, Sarrault O, Baudet M, Couté Y et al. 2016. Triadin and CLIMP-63 form a link between triads and microtubules in muscle cells. J. Cell Sci. 129:3744–55
     [Google Scholar]
145. 145. 

     Takeshima H, Komazaki S, Nishi M, Iino M, Kangawa K. 2000. Junctophilins: a novel family of junctional membrane complex proteins. Mol. Cell 6:11–22
     [Google Scholar]
146. 146. 

     Gross P, Johnson J, Romero CM, Eaton DM, Poulet C et al. 2021. Interaction of the joining region in junctophilin-2 with the L-type Ca. Circ. Res. 128:92–114
     [Google Scholar]
147. 147. 

     Louch WE, Sejersted OM, Swift F. 2010. There goes the neighborhood: pathological alterations in T-tubule morphology and consequences for cardiomyocyte Ca²⁺ handling. J. Biomed. Biotechnol. 2010:503906
     [Google Scholar]
148. 148. 

     Guo A, Zhang C, Wei S, Chen B, Song LS 2013. Emerging mechanisms of T-tubule remodelling in heart failure. Cardiovasc. Res. 98:204–15
     [Google Scholar]
149. 149. 

     Song LS, Sobie EA, McCulle S, Lederer WJ, Balke CW, Cheng H. 2006. Orphaned ryanodine receptors in the failing heart. PNAS 103:4305–10
     [Google Scholar]
150. 150. 

     Guo Y, VanDusen NJ, Zhang L, Gu W, Sethi I et al. 2017. Analysis of cardiac myocyte maturation using CASAAV, a platform for rapid dissection of cardiac myocyte gene function in vivo. Circ. Res. 120:1874–88
     [Google Scholar]
151. 151. 

     Zhang C, Chen B, Guo A, Zhu Y, Miller JD et al. 2014. Microtubule-mediated defects in junctophilin-2 trafficking contribute to myocyte transverse-tubule remodeling and Ca²⁺ handling dysfunction in heart failure. Circulation 129:1742–50
     [Google Scholar]
152. 152. 

     Prins KW, Tian L, Wu D, Thenappan T, Metzger JM, Archer SL. 2017. Colchicine depolymerizes microtubules, increases junctophilin-2, and improves right ventricular function in experimental pulmonary arterial hypertension. J. Am. Heart Assoc. 6:e006195
     [Google Scholar]
153. 153. 

     Frisk M, Ruud M, Espe EK, Aronsen JM, Røe Å et al. 2016. Elevated ventricular wall stress disrupts cardiomyocyte t-tubule structure and calcium homeostasis. Cardiovasc. Res. 112:443–51
     [Google Scholar]
154. 154. 

     Sachse FB, Torres NS, Savio-Galimberti E, Aiba T, Kass DA et al. 2012. Subcellular structures and function of myocytes impaired during heart failure are restored by cardiac resynchronization therapy. Circ. Res. 110:588–97
     [Google Scholar]
155. 155. 

     Ibrahim M, Navaratnarajah M, Siedlecka U, Rao C, Dias P et al. 2012. Mechanical unloading reverses transverse tubule remodelling and normalizes local Ca²⁺-induced Ca²⁺ release in a rodent model of heart failure. Eur. J. Heart Fail. 14:571–80
     [Google Scholar]
156. 156. 

     Lee E, Marcucci M, Daniell L, Pypaert M, Weisz OA et al. 2002. Amphiphysin 2 (Bin1) and T-tubule biogenesis in muscle. Science 297:1193–96
     [Google Scholar]
157. 157. 

     Shinozaki-Narikawa N, Kodama T, Shibasaki Y 2006. Cooperation of phosphoinositides and BAR domain proteins in endosomal tubulation. Traffic 7:1539–50
     [Google Scholar]
158. 158. 

     Hall TE, Martel N, Ariotti N, Xiong Z, Lo HP et al. 2020. In vivo cell biological screening identifies an endocytic capture mechanism for T-tubule formation. Nat. Commun. 11:3711
     [Google Scholar]