The junctophilin family of proteins: From bench to bedside

Trends in Molecular Medicine

Volumn 20, Issue 6, 2014, Pages 353-362

  Landstrom, Andrew P ^a   Beavers, David L ^a   Wehrens, Xander H T ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Calcium; Excitation contraction coupling; JPH; Junctophilin; Mutation

Indexed keywords

CALCIUM; JUNCTOPHILIN 1; JUNCTOPHILIN 2; JUNCTOPHILIN 3; JUNCTOPHILIN 4; NEUROTRANSMITTER RECEPTOR; PROTEIN; UNCLASSIFIED DRUG; JUNCTOPHILIN; JUNCTOPHILIN-2 PROTEIN, HUMAN; MEMBRANE PROTEIN; MUSCLE PROTEIN;

ALTERNATIVE RNA SPLICING; ARRHYTHMOGENESIS; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CARDIOMYOPATHY; CELL MATURATION; CELL ULTRASTRUCTURE; HEART MUSCLE; HUMAN; HUNTINGTON DISEASE LIKE SYNDROME; IN VITRO STUDY; INTRACELLULAR MEMBRANE; MUSCLE INJURY; MUTATION; MYOPATHY; NONHUMAN; PATHOGENESIS; PATHOPHYSIOLOGY; PHYLOGENY; PROTEIN EXPRESSION; REVIEW; SKELETAL MUSCLE; TRANSVERSE TUBULAR SYSTEM; CARDIAC MUSCLE; CHEMISTRY; GENETICS; METABOLISM; MUSCLE DISEASE; NERVE CELL; STRIATED MUSCLE;

CALCIUM SIGNALING; CARDIOMYOPATHIES; HUMANS; MEMBRANE PROTEINS; MUSCLE PROTEINS; MUSCLE, SKELETAL; MUSCLE, STRIATED; MUSCULAR DISEASES; MUTATION; MYOCARDIUM; NEURONS; PHYLOGENY;

EID: 84901610427     PISSN: 14714914     EISSN: 1471499X     Source Type: Journal    
DOI: 10.1016/j.molmed.2014.02.004     Document Type: Review

References (81)

1. Takeshima H., et al. Junctophilins: a novel family of junctional membrane complex proteins. Mol. Cell 2000, 6:11-22.
2. Weisleder N., et al. Immuno-proteomic approach to excitation-contraction coupling in skeletal and cardiac muscle: molecular insights revealed by the mitsugumins. Cell Calcium 2008, 43:1-8.
3. Nishi M., et al. Characterization of human junctophilin subtype genes. Biochem. Biophys. Res. Commun. 2000, 273:920-927.
4. Garbino A., et al. Molecular evolution of the junctophilin gene family. Physiol. Genomics 2009, 37:175-186.
5. Ma H., et al. MORN motifs in plant PIPKs are involved in the regulation of subcellular localization and phospholipid binding. Cell Res. 2006, 16:466-478.
6. Im Y.J., et al. The N-terminal membrane occupation and recognition nexus domain of Arabidopsis phosphatidylinositol phosphate kinase 1 regulates enzyme activity. J. Biol. Chem. 2007, 282:5443-5452.
7. van Oort R., et al. Disrupted junctional membrane complexes and hyperactive ryanodine receptors after acute junctophilin knockdown in mice. Circulation 2011, 123:979-988.
8. Bers D. Excitation-Contraction Coupling and Cardiac Contractile Force 2001, Kluwer Academic.
9. Bers D.M. Cardiac excitation-contraction coupling. Nature 2002, 415:198-205.
10. Catterall W.A. Excitation-contraction coupling in vertebrate skeletal muscle: a tale of two calcium channels. Cell 1991, 64:871-874.
11. Endo M. Calcium-induced calcium release in skeletal muscle. Physiol. Rev. 2009, 89:1153-1176.
12. Hodgkin A.L., Horowicz P. Potassium contractures in single muscle fibres. J. Physiol. 1960, 153:386-403.
13. Schneider M., Chandler W. Voltage dependent charge movement in skeletal muscle: a possible step in excitation-contraction coupling. Nature 1973, 242:244-246.
14. Curtis B.M., Catterall W.A. Purification of the calcium antagonist receptor of the voltage-sensitive calcium channel from skeletal muscle transverse tubules. Biochemistry 1984, 23:2113-2118.
15. Hoffmann R., Valencia A. Implementing the iHOP concept for navigation of biomedical literature. Bioinformatics 2005, 21:ii252-ii258.
16. Block B., et al. Structural evidence for direct interaction between the molecular components of the transverse tubule/sarcoplasmic reticulum junction in skeletal muscle. J. Cell Biol. 1988, 107:2587-2600.
17. 2+ release from sarcoplasmic reticulum through silencing of junctophilin genes. Biophys. J. 2006, 90:4418-4427.
18. 2+ channel dihydropyridine receptors (DHPRs) in skeletal muscle. J. Biol. Chem. 2011, 286:43717-43725.
19. Phimister A.J., et al. 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. 2007, 8667-8677.
20. 2+ loading in quiescent junctophilin 1 knock-out myotubes. J. Biol. Chem. 2010, 285:39171-39179.
21. Lee E.H., et al. Functional coupling between TRPC3 and RyR1 regulates the expressions of key triadic proteins. J. Biol. Chem. 2006, 281:10042-10048.
22. Gonzalez-Serratos H., et al. Na-Ca exchange studies in sarcolemmal skeletal muscle. Ann. N. Y. Acad. Sci. 1996, 779:556-560.
23. 2+ entry is not required for store refilling in skeletal muscle. Clin. Exp. Pharmacol. Physiol. 2013, 40:338-344.
24. 2+ entry in skeletal muscle. Pflugers Arch 2010, 460:813-823.
25. Stiber J.A., Rosenberg P.B. The role of store-operated calcium influx in skeletal muscle signaling. Cell Calcium 2011, 49:341-349.
26. Ito K., et al. Deficiency of triad junction and contraction in mutant skeletal muscle lacking junctophilin type 1. J. Cell Biol. 2001, 154:1059-1068.
27. Komazaki S., et al. Deficiency of triad formation in developing skeletal muscle cells lacking junctophilin type 1. FEBS Lett. 2002, 524:225-229.
28. Corona B.T., et al. Junctophilin damage contributes to early strength deficits and EC coupling failure after eccentric contractions. Am. J. Physiol. Cell Physiol. 2010, 298:C365-C376.
29. 2+-dependent proteolysis of junctophilin-1 and junctophilin-2 in skeletal and cardiac muscle. J. Physiol. 2013, 591:719-729.
30. Rayns D.G., et al. Surface features of striated muscle: I. Guinea-pig cardiac muscle. J. Cell Sci. 1968, 3:467-474.
31. Fawcett D.W., McNutt N.S. The ultrastructure of the cat myocardium: I. Ventricular papillary muscle. J. Cell Biol. 1969, 42:1-45.
32. Minamisawa S., et al. Junctophilin type 2 is associated with caveolin-3 and is down-regulated in the hypertrophic and dilated cardiomyopathies. Biochem. Biophys. Res. Commun. 2004, 325:852-856.
33. Galbiati F., et al. Caveolin-3 null mice show a loss of caveolae, changes in the microdomain distribution of the dystrophin-glycoprotein complex, and t-tubule abnormalities. J. Biol. Chem. 2001, 276:21425-21433.
34. Balijepalli R.C., Kamp T.J. Caveolae, ion channels and cardiac arrhythmias. Prog. Biophys. Mol. Biol. 2008, 98:149-160.
35. Ziman A.P., et al. Excitation-contraction coupling changes during postnatal cardiac development. J. Mol. Cell. Cardiol. 2010, 48:379-386.
36. Liang X., et al. Junctophilin 2 knockdown interfere with mitochondrium status in ESC-CMs and cardiogenesis of ES cells. J. Cell. Biochem. 2012, 113:2884-2894.
37. Landstrom A., et al. Junctophilin-2 expression silencing causes cardiocyte hypertrophy and abnormal intracellular calcium-handling. Circ. Heart Fail. 2011, 4:214-223.
38. Jayasinghe I.D., et al. Nanoscale organization of junctophilin-2 and ryanodine receptors within peripheral couplings of rat ventricular cardiomyocytes. Biophys. J. 2012, 102:L19-L21.
39. Reynolds J.O., et al. Junctophilin-2 is necessary for T-tubule maturation during mouse heart development. Cardiovasc. Res. 2013, 100:44-53.
40. Han J., et al. Morphogenesis of T-tubules in heart cells: the role of junctophilin-2. Sci. China Life Sci. 2013, 56:647-652.
41. Go A.S., et al. Heart disease and stroke statistics 2013 update: a report from the American Heart Association. Circulation 2013, 127:e6-e245.
42. 2+ channel and ryanodine receptor signaling in hypertrophy. PLoS Biol. 2007, 5:e21.
43. 2+ signalling apparatus in failing heart cells. Cardiovasc. Res. 2012, 95:430-438.
44. Landstrom A.P., et al. Mutations in JPH2-encoded junctophilin-2 associated with hypertrophic cardiomyopathy in humans. J. Mol. Cell. Cardiol. 2007, 42:1026-1035.
45. Landstrom A.P., Ackerman M.J. GWAS or Gee Whiz, PSAS or Pshaw: elucidating the biologic and clinical significance of genetic variation in cardiovascular disease. Heart Rhythm 2009, 6:1751-1753.
46. Landstrom A.P., Ackerman M.J. The Achilles' heel of cardiovascular genetic testing: distinguishing pathogenic mutations from background genetic noise. Clin. Pharmacol. Ther. 2011, 90:496.
47. Matsushita Y., et al. Mutation of junctophilin type 2 associated with hypertrophic cardiomyopathy. J. Hum. Genet. 2007, 52:543-548.
48. Landstrom A.P., Ackerman M.J. Beyond the cardiac myofilament: hypertrophic cardiomyopathy-associated mutations in genes that encode calcium-handling proteins. Curr. Mol. Med. 2012, 12:507-518.
49. Beavers D.L., et al. Mutation E169K in junctophilin-2 causes atrial fibrillation due to impaired RyR2 stabilization. J. Am. Coll. Cardiol. 2013, 62:2010-2019.
50. 2+ signalling in skeletal muscle. Biochem. J. 2010, 427:125-134.
51. Woo J.S., et al. Glutamate at position 227 of junctophilin-2 is involved in binding to TRPC3. Mol. Cell. Biochem. 2009, 328:25-32.
52. Woo J.S., et al. TRPC3-interacting triadic proteins in skeletal muscle. Biochem. J. 2008, 411:399-405.
53. 2+ entry via orai1. J. Biol. Chem. 2012, 287:14336-14348.
54. Nishi M., et al. Motor discoordination in mutant mice lacking junctophilin type 3. Biochem. Biophys. Res. Commun. 2002, 292:318-324.
55. Seixas A.I., et al. Loss of junctophilin-3 contributes to Huntington disease-like 2 pathogenesis. Ann. Neurol. 2012, 71:245-257.
56. Nishi M., et al. Coexpression of junctophilin type 3 and type 4 in brain. Mol. Brain Res. 2003, 118:102-110.
57. 2+ release and afterhyperpolarization in mutant hippocampal neurons lacking junctophilins. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:10811-10816.
58. Kakizawa S., et al. Functional crosstalk between cell-surface and intracellular channels mediated by junctophilins essential for neuronal functions. Cerebellum 2008, 7:385-391.
59. Mori F., et al. Developmental changes in expression of the three ryanodine receptor mRNAs in the mouse brain. Neurosci. Lett. 2000, 285:57-60.
60. Balschun D., et al. Deletion of the ryanodine receptor type 3 (RyR3) impairs forms of synaptic plasticity and spatial learning. EMBO J. 1999, 18:5264-5273.
61. Shimuta M., et al. Postsynaptic modulation of AMPA receptor-mediated synaptic responses and LTP by the type 3 ryanodine receptor. Mol. Cell. Neurosci. 2001, 17:921-930.
62. Kushnir A., et al. Ryanodine receptor studies using genetically engineered mice. FEBS Lett. 2010, 584:1956-1965.
63. De Crescenzo V., et al. Type 1 ryanodine receptor knock-in mutation causing central core disease of skeletal muscle also displays a neuronal phenotype. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:610-615.
64. Walker F.O. Huntington's disease. Lancet 2007, 369:218-228.
65. Gusella J., et al. A polymorphic DNA marker genetically linked to Huntington's disease. Nature 1983, 306:234-238.
66. Moore R.C., et al. Huntington disease phenocopy is a familial prion disease. Am. J. Hum. Genet. 2001, 69:1385-1388.
67. Margolis R., et al. A disorder similar to Huntington's disease is associated with a novel CAG repeat expansion. Ann. Neurol. 2001, 50:373-380.
68. Holmes S.E., et al. A repeat expansion in the gene encoding junctophilin-3 is associated with Huntington disease-like 2. Nat. Genet. 2001, 29:377-378.
69. Margolis R., et al. Huntington's disease-like 2 (HDL2) in North America and Japan. Ann. Neurol. 2004, 56:670-674.
70. Paradisi I., et al. Huntington disease-like 2 (HDL2) in Venezuela: frequency and ethnic origin. J. Hum. Genet. 2013, 58:3-6.
71. Stevanin G., et al. CAG/CTG repeat expansions at the Huntington's disease-like 2 locus are rare in Huntington's disease patients. Neurology 2002, 58:965-967.
72. Santos C., et al. Huntington disease-like 2: the first patient with apparent European ancestry. Clin. Genet. 2008, 73:480-485.
73. Rodrigues G., et al. Huntington's disease-like 2 in Brazil - report of 4 patients. Mov. Disord. 2008, 23:2244-2247.
74. Schneider S., et al. JPH3 repeat expansions cause a progressive akinetic-rigid syndrome with severe dementia and putaminal rim in a five-generation African-American family. Neurogenetics 2012, 13:133-140.
75. Rudnicki D.D., et al. Huntington's disease-like 2 is associated with CUG repeat-containing RNA foci. Ann. Neurol. 2007, 61:272-282.
76. Wilburn B., et al. An antisense CAG repeat transcript at JPH3 locus mediates expanded polyglutamine protein toxicity in Huntington's disease-like 2 mice. Neuron 2011, 70:427-440.
77. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32:1792-1797.
78. Dereeper A., et al. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 2008, 36:W465-W469.
79. Chevenet F., et al. TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics 2006, 7:439.
80. Matlin A.J., et al. Understanding alternative splicing: towards a cellular code. Nat. Rev. Mol. Cell Biol. 2005, 6:386-398.
81. Pan Q., et al. Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat. Genet. 2008, 40:1413-1415.