1932

Abstract

Membrane contact sites between endoplasmic reticulum (ER) and plasma membrane (PM), or ER-PM junctions, are found in all eukaryotic cells. In excitable cells they play unique roles in organizing diverse forms of Ca2+ signaling as triggered by membrane depolarization. ER-PM junctions underlie crucial physiological processes such as excitation-contraction coupling, smooth muscle contraction and relaxation, and various forms of activity-dependent signaling and plasticity in neurons. In many cases the structure and molecular composition of ER-PM junctions in excitable cells comprise important regulatory feedback loops linking depolarization-induced Ca2+ signaling at these sites to the regulation of membrane potential. Here, we describe recent findings on physiological roles and molecular composition of native ER-PM junctions in excitable cells. We focus on recent studies that provide new insights into canonical forms of depolarization-induced Ca2+ signaling occurring at junctional triads and dyads of striated muscle, as well as the diversity of ER-PM junctions in these cells and in smooth muscle and neurons.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-physiol-032122-104610
2023-02-10
2024-06-18
Loading full text...

Full text loading...

/deliver/fulltext/physiol/85/1/annurev-physiol-032122-104610.html?itemId=/content/journals/10.1146/annurev-physiol-032122-104610&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Prinz WA, Toulmay A, Balla T. 2020. The functional universe of membrane contact sites. Nat. Rev. Mol. Cell Biol. 21:7–24
    [Google Scholar]
  2. 2.
    Henne WM, Liou J, Emr SD. 2015. Molecular mechanisms of inter-organelle ER-PM contact sites. Curr. Opin. Cell Biol. 35:123–30
    [Google Scholar]
  3. 3.
    Stefan CJ. 2020. Endoplasmic reticulum-plasma membrane contacts: principals of phosphoinositide and calcium signaling. Curr. Opin. Cell Biol. 63:125–34
    [Google Scholar]
  4. 4.
    Burgoyne T, Patel S, Eden ER 2015. Calcium signaling at ER membrane contact sites. Biochim. Biophys. Acta Mol. Cell Res. 1853:2012–17
    [Google Scholar]
  5. 5.
    Balla T. 2018. Ca2+ and lipid signals hold hands at endoplasmic reticulum-plasma membrane contact sites. J. Physiol. 596:2709–16
    [Google Scholar]
  6. 6.
    Dickson EJ. 2022. Phosphoinositide transport and metabolism at membrane contact sites. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1867:159107
    [Google Scholar]
  7. 7.
    Porter KR, Palade GE. 1957. Studies on the endoplasmic reticulum. III. Its form and distribution in striated muscle cells. J. Biophys. Biochem. Cytol. 3:269–300
    [Google Scholar]
  8. 8.
    Franzini-Armstrong C. 1970. Studies of the triad: I. Structure of the junction in frog twitch fibers. J. Cell Biol. 47:488–99
    [Google Scholar]
  9. 9.
    Bannister RA, Beam KG. 2013. CaV1.1: The atypical prototypical voltage-gated Ca2+ channel. Biochim. Biophys. Acta Biomembr. 1828:1587–97
    [Google Scholar]
  10. 10.
    Armstrong CM, Bezanilla FM, Horowicz P. 1972. Twitches in the presence of ethylene glycol bis(β-aminoethyl ether)-N,N′-tetracetic acid. Biochim. Biophys. Acta Bioenerg. 267:605–8
    [Google Scholar]
  11. 11.
    Gonzalez-Serratos H, Valle-Aguilera R, Lathrop DA, Garcia MC. 1982. Slow inward calcium currents have no obvious role in muscle excitation-contraction coupling. Nature 298:292–94
    [Google Scholar]
  12. 12.
    Nakai J, Dirksen RT, Nguyen HT, Pessah IN, Beam KG, Allen PD. 1996. Enhanced dihydropyridine receptor channel activity in the presence of ryanodine receptor. Nature 380:72–75
    [Google Scholar]
  13. 13.
    Dirksen RT, Beam KG. 1999. Role of calcium permeation in dihydropyridine receptor function. Insights into channel gating and excitation-contraction coupling. J. Gen. Physiol. 114:393–403
    [Google Scholar]
  14. 14.
    Polster A, Perni S, Filipova D, Moua O, Ohrtman JD et al. 2018. Junctional trafficking and restoration of retrograde signaling by the cytoplasmic RyR1 domain. J. Gen. Physiol. 150:293–306
    [Google Scholar]
  15. 15.
    Avila G, Dirksen RT. 2000. Functional impact of the ryanodine receptor on the skeletal muscle L-type Ca2+ channel. J. Gen. Physiol. 115:467–80
    [Google Scholar]
  16. 16.
    Franzini-Armstrong C, Pincon-Raymond M, Rieger F 1991. Muscle fibers from dysgenic mouse in vivo lack a surface component of peripheral couplings. Dev. Biol. 146:364–76
    [Google Scholar]
  17. 17.
    Takekura H, Nishi M, Noda T, Takeshima H, Franzini-Armstrong C. 1995. Abnormal junctions between surface membrane and sarcoplasmic reticulum in skeletal muscle with a mutation targeted to the ryanodine receptor. PNAS 92:3381–85
    [Google Scholar]
  18. 18.
    Samso M. 2017. A guide to the 3D structure of the ryanodine receptor type 1 by cryoEM. Protein Sci 26:52–68
    [Google Scholar]
  19. 19.
    Yan Z, Bai X, Yan C, Wu J, Li Z et al. 2015. Structure of the rabbit ryanodine receptor RyR1 at near-atomic resolution. Nature 517:50–55
    [Google Scholar]
  20. 20.
    Block BA, Imagawa T, Campbell KP, Franzini-Armstrong C. 1988. Structural evidence for direct interaction between the molecular components of the transverse tubule/sarcoplasmic reticulum junction in skeletal muscle. J. Cell Biol. 107:2587–600
    [Google Scholar]
  21. 21.
    Di Biase V, Franzini-Armstrong C. 2005. Evolution of skeletal type e–c coupling: a novel means of controlling calcium delivery. J. Cell Biol. 171:695–704
    [Google Scholar]
  22. 22.
    Emrich SM, Yoast RE, Trebak M. 2022. Physiological functions of CRAC channels. Annu. Rev. Physiol. 84:355–79
    [Google Scholar]
  23. 23.
    Prakriya M, Lewis RS. 2015. Store-operated calcium channels. Physiol. Rev. 95:1383–436
    [Google Scholar]
  24. 24.
    Lewis RS. 2020. Store-operated calcium channels: from function to structure and back again. Cold Spring Harb. Perspect. Biol. 12:a035055
    [Google Scholar]
  25. 25.
    Michelucci A, Garcia-Castaneda M, Boncompagni S, Dirksen RT. 2018. Role of STIM1/ORAI1-mediated store-operated Ca2+ entry in skeletal muscle physiology and disease. Cell Calcium 76:101–15
    [Google Scholar]
  26. 26.
    Takeshima H, Shimuta M, Komazaki S, Ohmi K, Nishi M et al. 1998. Mitsugumin29, a novel synaptophysin family member from the triad junction in skeletal muscle. Biochem. J. 331:Part 1317–22
    [Google Scholar]
  27. 27.
    Betz H, Becker CM, Grenningloh G, Hoch W, Knaus P et al. 1989. Homology and analogy in transmembrane channel design: lessons from synaptic membrane proteins. J. Protein Chem. 8:325
    [Google Scholar]
  28. 28.
    Chang CW, Hsiao YT, Jackson MB. 2021. Synaptophysin regulates fusion pores and exocytosis mode in chromaffin cells. J. Neurosci. 41:3563–78
    [Google Scholar]
  29. 29.
    Komazaki S, Nishi M, Kangawa K, Takeshima H. 1999. Immunolocalization of mitsugumin29 in developing skeletal muscle and effects of the protein expressed in amphibian embryonic cells. Dev. Dyn. 215:87–95
    [Google Scholar]
  30. 30.
    Nishi M, Komazaki S, Kurebayashi N, Ogawa Y, Noda T et al. 1999. Abnormal features in skeletal muscle from mice lacking mitsugumin29. J. Cell Biol. 147:1473–80
    [Google Scholar]
  31. 31.
    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]
  32. 32.
    Garbino A, van Oort RJ, Dixit SS, Landstrom AP, Ackerman MJ, Wehrens XH. 2009. Molecular evolution of the junctophilin gene family. Physiol. Genom. 37:175–86
    [Google Scholar]
  33. 33.
    Bennett HJ, Davenport JB, Collins RF, Trafford AW, Pinali C, Kitmitto A. 2013. Human junctophilin-2 undergoes a structural rearrangement upon binding PtdIns(3,4,5)P3 and the S101R mutation identified in hypertrophic cardiomyopathy obviates this response. Biochem. J. 456:205–17
    [Google Scholar]
  34. 34.
    Rossi D, Scarcella AM, Liguori E, Lorenzini S, Pierantozzi E et al. 2019. Molecular determinants of homo- and heteromeric interactions of Junctophilin-1 at triads in adult skeletal muscle fibers. PNAS 116:15716–24
    [Google Scholar]
  35. 35.
    Yang ZF, Panwar P, McFarlane CR, Tuinte WE, Campiglio M, Van Petegem F. 2022. Structures of the junctophilin/voltage-gated calcium channel interface reveal hot spot for cardiomyopathy mutations. PNAS 119:e2120416119
    [Google Scholar]
  36. 36.
    Jiang M, Hu J, White FKH, Williamson J, Klymchenko AS et al. 2019. S-Palmitoylation of junctophilin-2 is critical for its role in tethering the sarcoplasmic reticulum to the plasma membrane. J. Biol. Chem. 294:13487–501
    [Google Scholar]
  37. 37.
    Ito K, Komazaki S, Sasamoto K, Yoshida M, Nishi M et al. 2001. Deficiency of triad junction and contraction in mutant skeletal muscle lacking junctophilin type 1. J. Cell Biol. 154:1059–67
    [Google Scholar]
  38. 38.
    Komazaki S, Ito K, Takeshima H, Nakamura H. 2002. Deficiency of triad formation in developing skeletal muscle cells lacking junctophilin type 1. FEBS Lett. 524:225–29
    [Google Scholar]
  39. 39.
    Hirata Y, Brotto M, Weisleder N, Chu Y, Lin P et al. 2006. Uncoupling store-operated Ca2+ entry and altered Ca2+ release from sarcoplasmic reticulum through silencing of junctophilin genes. Biophys. J. 90:4418–27
    [Google Scholar]
  40. 40.
    Guarina L, Moghbel AN, Pourhosseinzadeh MS, Cudmore RH, Sato D et al. 2022. Biological noise is a key determinant of the reproducibility and adaptability of cardiac pacemaking and EC coupling. J. Gen. Physiol. 154:e202012613
    [Google Scholar]
  41. 41.
    King AN, Manning CF, Trimmer JS. 2014. A unique ion channel clustering domain on the axon initial segment of mammalian neurons. J. Comp. Neurol. 522:2594–608
    [Google Scholar]
  42. 42.
    Kirmiz M, Vierra NC, Palacio S, Trimmer JS. 2018. Identification of VAPA and VAPB as Kv2 channel-interacting proteins defining endoplasmic reticulum-plasma membrane junctions in mammalian brain neurons. J. Neurosci. 38:7562–84
    [Google Scholar]
  43. 43.
    Golini L, Chouabe C, Berthier C, Cusimano V, Fornaro M et al. 2011. Junctophilin 1 and 2 proteins interact with the L-type Ca2+ channel dihydropyridine receptors (DHPRs) in skeletal muscle. J. Biol. Chem. 286:43717–25
    [Google Scholar]
  44. 44.
    Nakada T, Kashihara T, Komatsu M, Kojima K, Takeshita T, Yamada M. 2018. Physical interaction of junctophilin and the CaV1.1 C terminus is crucial for skeletal muscle contraction. PNAS 115:4507–12
    [Google Scholar]
  45. 45.
    Phimister AJ, Lango J, Lee EH, Ernst-Russell MA, Takeshima H et al. 2007. Conformation-dependent stability of junctophilin 1 (JP1) and ryanodine receptor type 1 (RyR1) channel complex is mediated by their hyper-reactive thiols. J. Biol. Chem. 282:8667–77
    [Google Scholar]
  46. 46.
    Rufenach B, Van Petegem F. 2021. Structure and function of STAC proteins: calcium channel modulators and critical components of muscle excitation-contraction coupling. J. Biol. Chem. 297:100874
    [Google Scholar]
  47. 47.
    Shishmarev D. 2020. Excitation-contraction coupling in skeletal muscle: recent progress and unanswered questions. Biophys. Rev. 12:143–53
    [Google Scholar]
  48. 48.
    Perni S, Lavorato M, Beam KG. 2017. De novo reconstitution reveals the proteins required for skeletal muscle voltage-induced Ca2+ release. PNAS 114:13822–27
    [Google Scholar]
  49. 49.
    Di Maio A, Karko K, Snopko RM, Mejia-Alvarez R, Franzini-Armstrong C. 2007. T-tubule formation in cardiacmyocytes: Two possible mechanisms?. J. Muscle Res. Cell Motil. 28:231–41
    [Google Scholar]
  50. 50.
    Pinali C, Bennett H, Davenport JB, Trafford AW, Kitmitto A. 2013. Three-dimensional reconstruction of cardiac sarcoplasmic reticulum reveals a continuous network linking transverse-tubules: this organization is perturbed in heart failure. Circ. Res. 113:1219–30
    [Google Scholar]
  51. 51.
    Shiels HA, Galli GL. 2014. The sarcoplasmic reticulum and the evolution of the vertebrate heart. Physiology 29:456–69
    [Google Scholar]
  52. 52.
    Kawai M, Hussain M, Orchard CH. 1999. Excitation-contraction coupling in rat ventricular myocytes after formamide-induced detubulation. Am. J. Physiol. 277:H603–9
    [Google Scholar]
  53. 53.
    Del Villar SG, Voelker TL, Westhoff M, Reddy GR, Spooner HC et al. 2021. β-Adrenergic control of sarcolemmal CaV1.2 abundance by small GTPase Rab proteins. PNAS 118:e2017937118
    [Google Scholar]
  54. 54.
    Ito DW, Hannigan KI, Ghosh D, Xu B, Del Villar SG et al. 2019. β-Adrenergic-mediated dynamic augmentation of sarcolemmal CaV1.2 clustering and co-operativity in ventricular myocytes. J. Physiol. 597:2139–62
    [Google Scholar]
  55. 55.
    Dixon RE, Moreno CM, Yuan C, Opitz-Araya X, Binder MD et al. 2015. Graded Ca2+/calmodulin-dependent coupling of voltage-gated CaV1.2 channels. eLife 4:e05608
    [Google Scholar]
  56. 56.
    Scriven DR, Asghari P, Schulson MN, Moore ED. 2010. Analysis of CaV1.2 and ryanodine receptor clusters in rat ventricular myocytes. Biophys. J. 99:3923–29
    [Google Scholar]
  57. 57.
    Cheng H, Lederer WJ. 2008. Calcium sparks. Physiol. Rev. 88:1491–545
    [Google Scholar]
  58. 58.
    Tanskanen AJ, Greenstein JL, Chen A, Sun SX, Winslow RL. 2007. Protein geometry and placement in the cardiac dyad influence macroscopic properties of calcium-induced calcium release. Biophys. J. 92:3379–96
    [Google Scholar]
  59. 59.
    Franzini-Armstrong C, Protasi F, Ramesh V 1999. Shape, size, and distribution of Ca2+ release units and couplons in skeletal and cardiac muscles. Biophys. J. 77:1528–39
    [Google Scholar]
  60. 60.
    Dixon RE. 2021. Nanoscale organization, regulation, and dynamic reorganization of cardiac calcium channels. Front. Physiol. 12:810408
    [Google Scholar]
  61. 61.
    Wang MC, Collins RF, Ford RC, Berrow NS, Dolphin AC, Kitmitto A. 2004. The three-dimensional structure of the cardiac L-type voltage-gated calcium channel: comparison with the skeletal muscle form reveals a common architectural motif. J. Biol. Chem. 279:7159–68
    [Google Scholar]
  62. 62.
    Inoue M, Bridge JH. 2003. Ca2+ sparks in rabbit ventricular myocytes evoked by action potentials: involvement of clusters of L-type Ca2+ channels. Circ. Res. 92:532–38
    [Google Scholar]
  63. 63.
    Bers DM, Stiffel VM. 1993. Ratio of ryanodine to dihydropyridine receptors in cardiac and skeletal muscle and implications for E-C coupling. Am. J. Physiol. 264:C1587–93
    [Google Scholar]
  64. 64.
    Quayle JM, McCarron JG, Asbury JR, Nelson MT. 1993. Single calcium channels in resistance-sized cerebral arteries from rats. Am. J. Physiol. 264:H470–78
    [Google Scholar]
  65. 65.
    Dixon RE, Yuan C, Cheng EP, Navedo MF, Santana LF. 2012. Ca2+ signaling amplification by oligomerization of L-type CaV1.2 channels. PNAS 109:1749–54
    [Google Scholar]
  66. 66.
    Dixon RE, Navedo MF, Binder MD, Santana LF. 2022. Mechanisms and physiological implications of cooperative gating of clustered ion channels. Physiol. Rev. 102:1159–210
    [Google Scholar]
  67. 67.
    Ziman AP, Gomez-Viquez NL, Bloch RJ, Lederer WJ. 2010. Excitation-contraction coupling changes during postnatal cardiac development. J. Mol. Cell. Cardiol. 48:379–86
    [Google Scholar]
  68. 68.
    Kim HD, Kim DJ, Lee IJ, Rah BJ, Sawa Y, Schaper J. 1992. Human fetal heart development after mid-term: morphometry and ultrastructural study. J. Mol. Cell. Cardiol. 24:949–65
    [Google Scholar]
  69. 69.
    Jones PP, MacQuaide N, Louch WE. 2018. Dyadic plasticity in cardiomyocytes. Front. Physiol. 9:1773
    [Google Scholar]
  70. 70.
    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]
  71. 71.
    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]
  72. 72.
    Parton RG, Way M, Zorzi N, Stang E. 1997. Caveolin-3 associates with developing T-tubules during muscle differentiation. J. Cell Biol. 136:137–54
    [Google Scholar]
  73. 73.
    Bryant SM, Kong CHT, Watson JJ, Gadeberg HC, Roth DM et al. 2018. Caveolin-3 KO disrupts t-tubule structure and decreases t-tubular ICa density in mouse ventricular myocytes. Am. J. Physiol. Heart Circ. Physiol. 315:H1101–11
    [Google Scholar]
  74. 74.
    Lehnart SE, Wehrens XHT. 2022. The role of junctophilin proteins in cellular function. Physiol. Rev. 102:1211–61
    [Google Scholar]
  75. 75.
    Van Oort RJ, Garbino A, Wang W, Dixit SS, Landstrom AP et al. 2011. Disrupted junctional membrane complexes and hyperactive ryanodine receptors after acute junctophilin knockdown in mice. Circulation 123:979–88
    [Google Scholar]
  76. 76.
    Munro ML, Jayasinghe ID, Wang Q, Quick A, Wang W et al. 2016. Junctophilin-2 in the nanoscale organisation and functional signalling of ryanodine receptor clusters in cardiomyocytes. J. Cell Sci. 129:4388–98
    [Google Scholar]
  77. 77.
    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 Ca2+ channel is pivotal for cardiac dyad assembly and intracellular Ca2+ dynamics. Circ. Res. 128:92–114
    [Google Scholar]
  78. 78.
    Poulet C, Sanchez-Alonso J, Swiatlowska P, Mouy F, Lucarelli C et al. 2021. Junctophilin-2 tethers T-tubules and recruits functional L-type calcium channels to lipid rafts in adult cardiomyocytes. Cardiovasc. Res. 117:149–61
    [Google Scholar]
  79. 79.
    Wei S, Guo A, Chen B, Kutschke W, Xie YP et al. 2010. T-tubule remodeling during transition from hypertrophy to heart failure. Circ. Res. 107:520–31
    [Google Scholar]
  80. 80.
    Reynolds JO, Chiang DY, Wang W, Beavers DL, Dixit SS et al. 2013. Junctophilin-2 is necessary for T-tubule maturation during mouse heart development. Cardiovasc. Res. 100:44–53
    [Google Scholar]
  81. 81.
    Chen B, Guo A, Zhang C, Chen R, Zhu Y et al. 2013. Critical roles of junctophilin-2 in T-tubule and excitation-contraction coupling maturation during postnatal development. Cardiovasc. Res. 100:54–62
    [Google Scholar]
  82. 82.
    Landstrom AP, Weisleder N, Batalden KB, Bos JM, Tester DJ et al. 2007. Mutations in JPH2-encoded junctophilin-2 associated with hypertrophic cardiomyopathy in humans. J. Mol. Cell. Cardiol. 42:1026–35
    [Google Scholar]
  83. 83.
    Zhang HB, Li RC, Xu M, Xu SM, Lai YS et al. 2013. Ultrastructural uncoupling between T-tubules and sarcoplasmic reticulum in human heart failure. Cardiovasc. Res. 98:269–76
    [Google Scholar]
  84. 84.
    Guo A, Hall D, Zhang C, Peng T, Miller JD et al. 2015. Molecular determinants of calpain-dependent cleavage of junctophilin-2 protein in cardiomyocytes. J. Biol. Chem. 290:17946–55
    [Google Scholar]
  85. 85.
    Matsushita Y, Furukawa T, Kasanuki H, Nishibatake M, Kurihara Y et al. 2007. Mutation of junctophilin type 2 associated with hypertrophic cardiomyopathy. J. Hum. Genet. 52:543–48
    [Google Scholar]
  86. 86.
    Reynolds JO, Quick AP, Wang Q, Beavers DL, Philippen LE et al. 2016. Junctophilin-2 gene therapy rescues heart failure by normalizing RyR2-mediated Ca2+ release. Int. J. Cardiol. 225:371–80
    [Google Scholar]
  87. 87.
    Caldwell JL, Smith CE, Taylor RF, Kitmitto A, Eisner DA et al. 2014. Dependence of cardiac transverse tubules on the BAR domain protein amphiphysin II (BIN-1). Circ. Res. 115:986–96
    [Google Scholar]
  88. 88.
    Hou Y, Bai J, Shen X, de Langen O, Li A et al. 2021. Nanoscale organisation of ryanodine receptors and Junctophilin-2 in the failing human heart. Front. Physiol. 12:724372
    [Google Scholar]
  89. 89.
    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]
  90. 90.
    Hong TT, Smyth JW, Chu KY, Vogan JM, Fong TS et al. 2012. BIN1 is reduced and Cav1.2 trafficking is impaired in human failing cardiomyocytes. Heart Rhythm 9:812–20
    [Google Scholar]
  91. 91.
    Hong T, Yang H, Zhang SS, Cho HC, Kalashnikova M et al. 2014. Cardiac BIN1 folds T-tubule membrane, controlling ion flux and limiting arrhythmia. Nat. Med. 20:624–32
    [Google Scholar]
  92. 92.
    Fu Y, Shaw SA, Naami R, Vuong CL, Basheer WA et al. 2016. Isoproterenol promotes rapid ryanodine receptor movement to bridging integrator 1 (BIN1)-organized dyads. Circulation 133:388–97
    [Google Scholar]
  93. 93.
    De La Mata A, Tajada S, O'Dwyer S, Matsumoto C, Dixon RE et al. 2019. BIN1 induces the formation of T-tubules and adult-like Ca2+ release units in developing cardiomyocytes. Stem Cells 37:54–64
    [Google Scholar]
  94. 94.
    Li J, Agvanian S, Zhou K, Shaw RM, Hong T. 2020. Exogenous cardiac bridging integrator 1 benefits mouse hearts with pre-existing pressure overload-induced heart failure. Front. Physiol. 11:708
    [Google Scholar]
  95. 95.
    Lyon AR, Nikolaev VO, Miragoli M, Sikkel MB, Paur H et al. 2012. Plasticity of surface structures and β2-adrenergic receptor localization in failing ventricular cardiomyocytes during recovery from heart failure. Circ. Heart Fail. 5:357–65
    [Google Scholar]
  96. 96.
    Ohtsuka T, Nakanishi H, Ikeda W, Satoh A, Momose Y et al. 1998. Nexilin: a novel actin filament-binding protein localized at cell-matrix adherens junction. J. Cell Biol. 143:1227–38
    [Google Scholar]
  97. 97.
    Hassel D, Dahme T, Erdmann J, Meder B, Huge A et al. 2009. Nexilin mutations destabilize cardiac Z-disks and lead to dilated cardiomyopathy. Nat. Med. 15:1281–88
    [Google Scholar]
  98. 98.
    Spinozzi S, Liu C, Chen Z, Feng W, Zhang L et al. 2020. Nexilin is necessary for maintaining the transverse-axial tubular system in adult cardiomyocytes. Circ. Heart Fail. 13:e006935
    [Google Scholar]
  99. 99.
    Liu C, Spinozzi S, Feng W, Chen Z, Zhang L et al. 2020. Homozygous G650del nexilin variant causes cardiomyopathy in mice. JCI Insight 5:e138780
    [Google Scholar]
  100. 100.
    Aherrahrou Z, Schlossarek S, Stoelting S, Klinger M, Geertz B et al. 2016. Knock-out of nexilin in mice leads to dilated cardiomyopathy and endomyocardial fibroelastosis. Basic Res. Cardiol. 111:6
    [Google Scholar]
  101. 101.
    Wang H, Li Z, Wang J, Sun K, Cui Q et al. 2010. Mutations in NEXN, a Z-disc gene, are associated with hypertrophic cardiomyopathy. Am. J. Hum. Genet. 87:687–93
    [Google Scholar]
  102. 102.
    Liu C, Spinozzi S, Chen JY, Fang X, Feng W et al. 2019. Nexilin is a new component of junctional membrane complexes required for cardiac t-tubule formation. Circulation 140:55–66
    [Google Scholar]
  103. 103.
    Moore ED, Voigt T, Kobayashi YM, Isenberg G, Fay FS et al. 2004. Organization of Ca2+ release units in excitable smooth muscle of the guinea-pig urinary bladder. Biophys. J. 87:1836–47
    [Google Scholar]
  104. 104.
    Somlyo AP. 1985. Excitation-contraction coupling and the ultrastructure of smooth muscle. Circ. Res. 57:497–507
    [Google Scholar]
  105. 105.
    Nelson MT, Cheng H, Rubart M, Santana LF, Bonev AD et al. 1995. Relaxation of arterial smooth muscle by calcium sparks. Science 270:633–37
    [Google Scholar]
  106. 106.
    Wellman GC, Nelson MT. 2003. Signaling between SR and plasmalemma in smooth muscle: sparks and the activation of Ca2+-sensitive ion channels. Cell Calcium 34:211–29
    [Google Scholar]
  107. 107.
    Herrera GM, Heppner TJ, Nelson MT. 2001. Voltage dependence of the coupling of Ca2+ sparks to BKCa channels in urinary bladder smooth muscle. Am. J. Physiol. Cell Physiol. 280:C481–90
    [Google Scholar]
  108. 108.
    Gonzales AL, Amberg GC, Earley S. 2010. Ca2+ release from the sarcoplasmic reticulum is required for sustained TRPM4 activity in cerebral artery smooth muscle cells. Am. J. Physiol. Cell Physiol. 299:C279–88
    [Google Scholar]
  109. 109.
    Earley S, Waldron BJ, Brayden JE. 2004. Critical role for transient receptor potential channel TRPM4 in myogenic constriction of cerebral arteries. Circ. Res. 95:922–29
    [Google Scholar]
  110. 110.
    Leblanc N, Forrest AS, Ayon RJ, Wiwchar M, Angermann JE et al. 2015. Molecular and functional significance of Ca2+-activated Cl channels in pulmonary arterial smooth muscle. Pulm. Circ. 5:244–68
    [Google Scholar]
  111. 111.
    Pritchard HAT, Gonzales AL, Pires PW, Drumm BT, Ko EA et al. 2017. Microtubule structures underlying the sarcoplasmic reticulum support peripheral coupling sites to regulate smooth muscle contractility. Sci. Signal. 10:eaan2694
    [Google Scholar]
  112. 112.
    Pritchard HAT, Griffin CS, Yamasaki E, Thakore P, Lane C et al. 2019. Nanoscale coupling of junctophilin-2 and ryanodine receptors regulates vascular smooth muscle cell contractility. PNAS 116:21874–81
    [Google Scholar]
  113. 113.
    Saeki T, Suzuki Y, Yamamura H, Takeshima H, Imaizumi Y. 2019. A junctophilin-caveolin interaction enables efficient coupling between ryanodine receptors and BKCa channels in the Ca2+ microdomain of vascular smooth muscle. J. Biol. Chem. 294:13093–105
    [Google Scholar]
  114. 114.
    Suzuki Y, Yamamura H, Ohya S, Imaizumi Y. 2013. Caveolin-1 facilitates the direct coupling between large conductance Ca2+-activated K+ (BKCa) and Cav1.2 Ca2+ channels and their clustering to regulate membrane excitability in vascular myocytes. J. Biol. Chem. 288:36750–61
    [Google Scholar]
  115. 115.
    Krishnan V, Ali S, Gonzales AL, Thakore P, Griffin CS et al. 2022. STIM1-dependent peripheral coupling governs the contractility of vascular smooth muscle cells. eLife 11:e70278
    [Google Scholar]
  116. 116.
    Rosenbluth J. 1962. The fine structure of acoustic ganglia in the rat. J. Cell Biol. 12:329–59
    [Google Scholar]
  117. 117.
    Rosenbluth J. 1962. Subsurface cisterns and their relationship to the neuronal plasma membrane. J. Cell Biol. 13:405–21
    [Google Scholar]
  118. 118.
    Henkart M, Landis DM, Reese TS. 1976. Similarity of junctions between plasma membranes and endoplasmic reticulum in muscle and neurons. J. Cell Biol. 70:338–47
    [Google Scholar]
  119. 119.
    Wu Y, Whiteus C, Xu CS, Hayworth KJ, Weinberg RJ et al. 2017. Contacts between the endoplasmic reticulum and other membranes in neurons. PNAS 114:E4859–67
    [Google Scholar]
  120. 120.
    BRAIN Init. Cell Census Netw. 2021. A multimodal cell census and atlas of the mammalian primary motor cortex. Nature 598:86–102
    [Google Scholar]
  121. 121.
    Berridge MJ. 1998. Neuronal calcium signaling. Neuron 21:13–26
    [Google Scholar]
  122. 122.
    Manita S, Ross WN. 2009. Synaptic activation and membrane potential changes modulate the frequency of spontaneous elementary Ca2+ release events in the dendrites of pyramidal neurons. J. Neurosci. 29:7833–45
    [Google Scholar]
  123. 123.
    Berrout J, Isokawa M. 2009. Homeostatic and stimulus-induced coupling of the L-type Ca2+ channel to the ryanodine receptor in the hippocampal neuron in slices. Cell Calcium 46:30–38
    [Google Scholar]
  124. 124.
    Miyazaki K, Ross WN. 2013. Ca2+ sparks and puffs are generated and interact in rat hippocampal CA1 pyramidal neuron dendrites. J. Neurosci. 33:17777–88
    [Google Scholar]
  125. 125.
    Vierra NC, Kirmiz M, van der List D, Santana LF, Trimmer JS. 2019. Kv2.1 mediates spatial and functional coupling of L-type calcium channels and ryanodine receptors in mammalian neurons. eLife 8:e49953
    [Google Scholar]
  126. 126.
    Jacobs JM, Meyer T. 1997. Control of action potential-induced Ca2+ signaling in the soma of hippocampal neurons by Ca2+ release from intracellular stores. J. Neurosci. 17:4129–35
    [Google Scholar]
  127. 127.
    Irie T, Trussell LO. 2017. Double-nanodomain coupling of calcium channels, ryanodine receptors, and BK channels controls the generation of burst firing. Neuron 96:856–70.e4
    [Google Scholar]
  128. 128.
    Mandikian D, Bocksteins E, Parajuli LK, Bishop HI, Cerda O et al. 2014. Cell type-specific spatial and functional coupling between mammalian brain Kv2.1 K+ channels and ryanodine receptors. J. Comp. Neurol. 522:3555–74
    [Google Scholar]
  129. 129.
    Antonucci DE, Lim ST, Vassanelli S, Trimmer JS. 2001. Dynamic localization and clustering of dendritic Kv2.1 voltage-dependent potassium channels in developing hippocampal neurons. Neuroscience 108:69–81
    [Google Scholar]
  130. 130.
    Misonou H, Mohapatra DP, Trimmer JS. 2005. Kv2.1: a voltage-gated K+ channel critical to dynamic control of neuronal excitability. Neurotoxicology 26:743–52
    [Google Scholar]
  131. 131.
    Fakler B, Adelman JP. 2008. Control of KCa channels by calcium nano/microdomains. Neuron 59:873–81
    [Google Scholar]
  132. 132.
    Indriati DW, Kamasawa N, Matsui K, Meredith AL, Watanabe M, Shigemoto R. 2013. Quantitative localization of CaV2.1 (P/Q-type) voltage-dependent calcium channels in Purkinje cells: somatodendritic gradient and distinct somatic coclustering with calcium-activated potassium channels. J. Neurosci. 33:3668–78
    [Google Scholar]
  133. 133.
    Whitt JP, McNally BA, Meredith AL. 2018. Differential contribution of Ca2+ sources to day and night BK current activation in the circadian clock. J. Gen. Physiol. 150:259–75
    [Google Scholar]
  134. 134.
    Barbara JG. 2002. IP3-dependent calcium-induced calcium release mediates bidirectional calcium waves in neurones: functional implications for synaptic plasticity. Biochim. Biophys. Acta Proteins Proteom. 1600:12–18
    [Google Scholar]
  135. 135.
    Yamasaki-Mann M, Demuro A, Parker I. 2013. Cytosolic [Ca2+] regulation of InsP3-evoked puffs. Biochem. J. 449:167–73
    [Google Scholar]
  136. 136.
    Thillaiappan NB, Chavda AP, Tovey SC, Prole DL, Taylor CW. 2017. Ca2+ signals initiate at immobile IP3 receptors adjacent to ER-plasma membrane junctions. Nat. Commun. 8:1505
    [Google Scholar]
  137. 137.
    Ross CA, Meldolesi J, Milner TA, Satoh T, Supattapone S, Snyder SH. 1989. Inositol 1,4,5-trisphosphate receptor localized to endoplasmic reticulum in cerebellar Purkinje neurons. Nature 339:468–70
    [Google Scholar]
  138. 138.
    Takei K, Stukenbrok H, Metcalf A, Mignery GA, Sudhof TC et al. 1992. Ca2+ stores in Purkinje neurons: endoplasmic reticulum subcompartments demonstrated by the heterogeneous distribution of the InsP3 receptor, Ca2+-ATPase, and calsequestrin. J. Neurosci. 12:489–505
    [Google Scholar]
  139. 139.
    Kaufmann WA, Ferraguti F, Fukazawa Y, Kasugai Y, Shigemoto R et al. 2009. Large-conductance calcium-activated potassium channels in Purkinje cell plasma membranes are clustered at sites of hypolemmal microdomains. J. Comp. Neurol. 515:215–30
    [Google Scholar]
  140. 140.
    Benedeczky I, Molnar E, Somogyi P. 1994. The cisternal organelle as a Ca2+-storing compartment associated with GABAergic synapses in the axon initial segment of hippocampal pyramidal neurones. Exp. Brain Res. 101:216–30
    [Google Scholar]
  141. 141.
    Lipkin AM, Cunniff MM, Spratt PWE, Lemke SM, Bender KJ. 2021. Functional microstructure of Cav-mediated calcium signaling in the axon initial segment. J. Neurosci. 41:3764–76
    [Google Scholar]
  142. 142.
    Spacek J, Harris KM. 1997. Three-dimensional organization of smooth endoplasmic reticulum in hippocampal CA1 dendrites and dendritic spines of the immature and mature rat. J. Neurosci. 17:190–203
    [Google Scholar]
  143. 143.
    Nishi M, Sakagami H, Komazaki S, Kondo H, Takeshima H. 2003. Coexpression of junctophilin type 3 and type 4 in brain. Brain Res. Mol. Brain Res. 118:102–10
    [Google Scholar]
  144. 144.
    Nishi M, Hashimoto K, Kuriyama K, Komazaki S, Kano M et al. 2002. Motor discoordination in mutant mice lacking junctophilin type 3. Biochem. Biophys. Res. Commun. 292:318–24
    [Google Scholar]
  145. 145.
    Seixas AI, Holmes SE, Takeshima H, Pavlovich A, Sachs N et al. 2012. Loss of junctophilin-3 contributes to Huntington disease-like 2 pathogenesis. Ann. Neurol. 71:245–57
    [Google Scholar]
  146. 146.
    Kakizawa S, Kishimoto Y, Hashimoto K, Miyazaki T, Furutani K et al. 2007. Junctophilin-mediated channel crosstalk essential for cerebellar synaptic plasticity. EMBO J. 26:1924–33
    [Google Scholar]
  147. 147.
    Holmes SE, O'Hearn E, Rosenblatt A, Callahan C, Hwang HS et al. 2001. A repeat expansion in the gene encoding junctophilin-3 is associated with Huntington disease-like 2. Nat. Genet. 29:377–78
    [Google Scholar]
  148. 148.
    Wilburn B, Rudnicki DD, Zhao J, Weitz TM, Cheng Y et al. 2011. An antisense CAG repeat transcript at JPH3 locus mediates expanded polyglutamine protein toxicity in Huntington's disease-like 2 mice. Neuron 70:427–40
    [Google Scholar]
  149. 149.
    Lancaster B, Nicoll RA. 1987. Properties of two calcium-activated hyperpolarizations in rat hippocampal neurones. J. Physiol. 389:187–203
    [Google Scholar]
  150. 150.
    Adelman JP, Maylie J, Sah P. 2012. Small-conductance Ca2+-activated K+ channels: form and function. Annu. Rev. Physiol. 74:245–69
    [Google Scholar]
  151. 151.
    Akita T, Kuba K. 2000. Functional triads consisting of ryanodine receptors, Ca2+ channels, and Ca2+-activated K+ channels in bullfrog sympathetic neurons. Plastic modulation of action potential. J. Gen. Physiol. 116:697–720
    [Google Scholar]
  152. 152.
    Moriguchi S, Nishi M, Komazaki S, Sakagami H, Miyazaki T et al. 2006. Functional uncoupling between Ca2+ release and afterhyperpolarization in mutant hippocampal neurons lacking junctophilins. PNAS 103:10811–16
    [Google Scholar]
  153. 153.
    Tedoldi A, Ludwig P, Fulgenzi G, Takeshima H, Pedarzani P, Stocker M. 2020. Calcium-induced calcium release and type 3 ryanodine receptors modulate the slow afterhyperpolarising current, sIAHP, and its potentiation in hippocampal pyramidal neurons. PLOS ONE 15:e0230465
    [Google Scholar]
  154. 154.
    Luo T, Li L, Peng Y, Xie R, Yan N et al. 2021. The MORN domain of junctophilin2 regulates functional interactions with small-conductance Ca2+-activated potassium channel subtype2 (SK2). Biofactors 47:69–79
    [Google Scholar]
  155. 155.
    Sahu G, Wazen RM, Colarusso P, Chen SRW, Zamponi GW, Turner RW. 2019. Junctophilin proteins tether a Cav1-RyR2-KCa3.1 tripartite complex to regulate neuronal excitability. Cell Rep. 28:2427–42.e6
    [Google Scholar]
  156. 156.
    Perni S, Beam K. 2021. Neuronal junctophilins recruit specific Cav and RyR isoforms to ER-PM junctions and functionally alter CaV2.1 and CaV2.2. eLife 10:e64249
    [Google Scholar]
  157. 157.
    Vacher H, Mohapatra DP, Trimmer JS. 2008. Localization and targeting of voltage-dependent ion channels in mammalian central neurons. Physiol. Rev. 88:1407–47
    [Google Scholar]
  158. 158.
    Liu PW, Bean BP. 2014. Kv2 channel regulation of action potential repolarization and firing patterns in superior cervical ganglion neurons and hippocampal CA1 pyramidal neurons. J. Neurosci. 34:4991–5002
    [Google Scholar]
  159. 159.
    Guan D, Armstrong WE, Foehring RC. 2013. Kv2 channels regulate firing rate in pyramidal neurons from rat sensorimotor cortex. J. Physiol. 591:4807–25
    [Google Scholar]
  160. 160.
    Malin SA, Nerbonne JM. 2002. Delayed rectifier K+ currents, IK, are encoded by Kv2 alpha-subunits and regulate tonic firing in mammalian sympathetic neurons. J. Neurosci. 22:10094–105
    [Google Scholar]
  161. 161.
    Trimmer JS. 1991. Immunological identification and characterization of a delayed rectifier K+ channel polypeptide in rat brain. PNAS 88:10764–68
    [Google Scholar]
  162. 162.
    Trimmer JS. 2015. Subcellular localization of K+ channels in mammalian brain neurons: remarkable precision in the midst of extraordinary complexity. Neuron 85:238–56
    [Google Scholar]
  163. 163.
    Bishop HI, Cobb MM, Kirmiz M, Parajuli LK, Mandikian D et al. 2018. Kv2 ion channels determine the expression and localization of the associated AMIGO-1 cell adhesion molecule in adult brain neurons. Front. Mol. Neurosci. 11: https://doi.org/10.3389/fnmol.2018.00001
    [Crossref] [Google Scholar]
  164. 164.
    Du J, Tao-Cheng JH, Zerfas P, McBain CJ. 1998. The K+ channel, Kv2.1, is apposed to astrocytic processes and is associated with inhibitory postsynaptic membranes in hippocampal and cortical principal neurons and inhibitory interneurons. Neuroscience 84:37–48
    [Google Scholar]
  165. 165.
    Bishop HI, Guan D, Bocksteins E, Parajuli LK, Murray KD et al. 2015. Distinct cell- and layer-specific expression patterns and independent regulation of Kv2 channel subtypes in cortical pyramidal neurons. J. Neurosci. 35:14922–42
    [Google Scholar]
  166. 166.
    Fox PD, Haberkorn CJ, Akin EJ, Seel PJ, Krapf D, Tamkun MM. 2015. Induction of stable ER-plasma-membrane junctions by Kv2.1 potassium channels. J. Cell Sci. 128:2096–105
    [Google Scholar]
  167. 167.
    Johnson B, Leek AN, Sole L, Maverick EE, Levine TP, Tamkun MM. 2018. Kv2 potassium channels form endoplasmic reticulum/plasma membrane junctions via interaction with VAPA and VAPB. PNAS 115:E7331–40
    [Google Scholar]
  168. 168.
    Kirmiz M, Palacio S, Thapa P, King AN, Sack JT, Trimmer JS. 2018. Remodeling neuronal ER-PM junctions is a conserved nonconducting function of Kv2 plasma membrane ion channels. Mol. Biol. Cell 29:2410–32
    [Google Scholar]
  169. 169.
    Lim ST, Antonucci DE, Scannevin RH, Trimmer JS. 2000. A novel targeting signal for proximal clustering of the Kv2.1 K+ channel in hippocampal neurons. Neuron 25:385–97
    [Google Scholar]
  170. 170.
    Rost BR, Schneider-Warme F, Schmitz D, Hegemann P. 2017. Optogenetic tools for subcellular applications in neuroscience. Neuron 96:572–603
    [Google Scholar]
  171. 171.
    Murphy SE, Levine TP. 2016. VAP, a versatile access point for the endoplasmic reticulum: review and analysis of FFAT-like motifs in the VAPome. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1861:952–61
    [Google Scholar]
  172. 172.
    Park KS, Mohapatra DP, Misonou H, Trimmer JS. 2006. Graded regulation of the Kv2.1 potassium channel by variable phosphorylation. Science 313:976–79
    [Google Scholar]
  173. 173.
    Misonou H, Mohapatra DP, Park EW, Leung V, Zhen D et al. 2004. Regulation of ion channel localization and phosphorylation by neuronal activity. Nat. Neurosci. 7:711–18
    [Google Scholar]
  174. 174.
    Jegla T, Marlow HQ, Chen B, Simmons DK, Jacobo SM, Martindale MQ. 2012. Expanded functional diversity of Shaker K+ channels in cnidarians is driven by gene expansion. PLOS ONE 7:e51366
    [Google Scholar]
  175. 175.
    O'Dwyer SC, Palacio S, Matsumoto C, Guarina L, Klug NR et al. 2020. Kv2.1 channels play opposing roles in regulating membrane potential, Ca2+ channel function, and myogenic tone in arterial smooth muscle. PNAS 117:3858–66
    [Google Scholar]
  176. 176.
    Amberg GC, Santana LF. 2006. Kv2 channels oppose myogenic constriction of rat cerebral arteries. Am. J. Physiol. Cell Physiol. 291:C348–56
    [Google Scholar]
  177. 177.
    Vierra NC, O'Dwyer SC, Matsumoto C, Santana LF, Trimmer JS 2021. Regulation of neuronal excitation-transcription coupling by Kv2.1-induced clustering of somatic L-type Ca2+ channels at ER-PM junctions. PNAS 118:e2110094118
    [Google Scholar]
  178. 178.
    Venditti R, Wilson C, De Matteis MA. 2021. Regulation and physiology of membrane contact sites. Curr. Opin. Cell Biol. 71:148–57
    [Google Scholar]
  179. 179.
    Li C, Qian T, He R, Wan C, Liu Y, Yu H. 2021. Endoplasmic reticulum-plasma membrane contact sites: regulators, mechanisms, and physiological functions. Front. Cell Dev. Biol. 9:627700
    [Google Scholar]
  180. 180.
    English AR, Voeltz GK. 2013. Endoplasmic reticulum structure and interconnections with other organelles. Cold Spring Harb. Perspect. Biol. 5:a013227
    [Google Scholar]
  181. 181.
    Rog-Zielinska EA, Scardigli M, Peyronnet R, Zgierski-Johnston CM, Greiner J et al. 2021. Beat-by-beat cardiomyocyte T-tubule deformation drives tubular content exchange. Circ. Res. 128:203–15
    [Google Scholar]
  182. 182.
    Tao-Cheng JH. 2018. Activity-dependent decrease in contact areas between subsurface cisterns and plasma membrane of hippocampal neurons. Mol. Brain 11:23
    [Google Scholar]
/content/journals/10.1146/annurev-physiol-032122-104610
Loading
/content/journals/10.1146/annurev-physiol-032122-104610
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error