Calcium signaling in membrane repair

Seminars in Cell and Developmental Biology

Volumn 45, Issue , 2015, Pages 24-31

  Cheng, Xiping ^a   Zhang, Xiaoli ^a   Yu, Lu ^a   Xu, Haoxing ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Ca2+; Calcium sensor; Lysosomal exocytosis; Membrane repair; TRPML1

Indexed keywords

ANNEXIN; CADMIUM BINDING PROTEIN; CALCIUM CHANNEL; CALCIUM ION; CALPAIN; DYSFERLIN; ION CHANNEL; SYNAPTOTAGMIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL;

APOPTOSIS; BIOSENSOR; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL MEMBRANE; ENDOCYTOSIS; EXTRACELLULAR SPACE; HUMAN; LYSOSOME; MITOCHONDRION; NONHUMAN; REVIEW; ANIMAL; EXOCYTOSIS; METABOLISM; PHYSIOLOGY; WOUND HEALING;

ANIMALS; CALCIUM SIGNALING; CELL MEMBRANE; EXOCYTOSIS; HUMANS; LYSOSOMES; TRANSIENT RECEPTOR POTENTIAL CHANNELS; WOUND HEALING;

EID: 84949231181     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2015.10.031     Document Type: Review

References (128)

1. McNeil P.L., Kirchhausen T. An emergency response team for membrane repair. Nat. Rev. Mol. Cell Biol. 2005, 6(6):499-505.
2. Andrews N.W., Almeida P.E., Corrotte M. Damage control: cellular mechanisms of plasma membrane repair. Trends Cell Biol. 2014, 24(12):734-742.
3. Suetsugu S., Kurisu S., Takenawa T. Dynamic shaping of cellular membranes by phospholipids and membrane-deforming proteins. Physiol. Rev. 2014, 94(4):1219-1248.
4. McNeil P.L., et al. Patching plasma membrane disruptions with cytoplasmic membrane. J. Cell Sci. 2000, 113(Pt 11):1891-1902.
5. Kagawa H., et al. Expression of prothrombinase activity and CD9 antigen on the surface of small vesicles from stimulated human endothelial cells. Thromb. Res. 1995, 80(6):451-460.
6. 2+)-regulated exocytosis of lysosomes. Cell 2001, 106(2):157-169.
7. 2+-dependent endocytosis. J. Cell Biol. 2008, 180(5):905-914.
8. Idone V., Tam C., Andrews N.W. Two-way traffic on the road to plasma membrane repair. Trends Cell Biol. 2008, 18(11):552-559.
9. Tam C., et al. Exocytosis of acid sphingomyelinase by wounded cells promotes endocytosis and plasma membrane repair. J. Cell Biol. 2010, 189(6):1027-1038.
10. Jimenez A.J., et al. ESCRT machinery is required for plasma membrane repair. Science 2014, 343(6174):1247136.
11. Babiychuk E.B., et al. Blebbing confers resistance against cell lysis. Cell Death Differ. 2011, 18(1):80-89.
12. 2+) operates a switch between repair and lysis of streptolysin O-perforated cells. Cell Death Differ. 2009, 16(8):1126-1134.
13. Scheffer L.L., et al. Mechanism of Ca(2)(+)-triggered ESCRT assembly and regulation of cell membrane repair. Nat. Commun. 2014, 5:5646.
14. Draeger A., Monastyrskaya K., Babiychuk E.B. Plasma membrane repair and cellular damage control: the annexin survival kit. Biochem. Pharmacol. 2011, 81(6):703-712.
15. McNeil P. Membrane repair redux: redox of MG53. Nat. Cell Biol. 2009, 11(1):7-9.
16. Cai C., et al. MG53 nucleates assembly of cell membrane repair machinery. Nat. Cell Biol. 2009, 11(1):56-64.
17. Chakrabarti S., et al. Impaired membrane resealing and autoimmune myositis in synaptotagmin VII-deficient mice. J. Cell Biol. 2003, 162(4):543-549.
18. Prins D., Michalak M. Organellar calcium buffers. Cold Spring Harbor Perspect. Biol. 2011, 3(3):1-18.
19. Clapham D.E. Calcium signaling. Cell 2007, 131(6):1047-1058.
20. Cheng X., et al. The intracellular Ca(2)(+) channel MCOLN1 is required for sarcolemma repair to prevent muscular dystrophy. Nat. Med. 2014, 20(10):1187-1192.
21. Berridge M.J., Bootman M.D., Roderick H.L. Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 2003, 4(7):517-529.
22. Xu H., Martinoia E., Szabo I. Organellar channels and transporters. Cell Calcium 2015, 58(1):1-10.
23. 2+ clearance in the cytosol of adrenal chromaffin cells. Biophys. J. 1997, 73(1):532-545.
24. 2+] at the mouth of a calcium channel. J. Neurosci. 1997, 17(18):6961-6973.
25. Bauer P.J. The local Ca concentration profile in the vicinity of a Ca channel. Cell Biochem. Biophys. 2001, 35(1):49-61.
26. Strehler E.E., Treiman M. Calcium pumps of plasma membrane and cell interior. Curr. Mol. Med. 2004, 4(3):323-335.
27. Fill M., Copello J.A. Ryanodine receptor calcium release channels. Physiol. Rev. 2002, 82(4):893-922.
28. Lam A.K., Galione A. The endoplasmic reticulum and junctional membrane communication during calcium signaling. Biochim. Biophys. Acta 2013, 1833(11):2542-2559.
29. Prakriya M. Store-operated orai channels: structure and function. Curr. Top. Membr. 2013, 71:1-32.
30. Csordas G., et al. Structural and functional features and significance of the physical linkage between ER and mitochondria. J. Cell Biol. 2006, 174(7):915-921.
31. 2+ signalling in health and disease. Biochem. J. 2011, 439(3):349-374.
32. Lloyd-Evans E., et al. Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium. Nat. Med. 2008, 14(11):1247-1255.
33. Zhu M.X., et al. Two-pore channels for integrative Ca signaling. Commun. Integr. Biol. 2010, 3(1):12-17.
34. Tugba Durlu-Kandilci N., et al. TPC2 proteins mediate nicotinic acid adenine dinucleotide phosphate (NAADP)- and agonist-evoked contractions of smooth muscle. J. Biol. Chem. 2010, 285(32):24925-24932.
35. 2+) signaling and endolysosomal trafficking. Curr. Biol. 2010, 20(8):703-709.
36. Morgan A.J., Galione A. Two-pore channels (TPCs): current controversies. Bioessays 2014, 36(2):173-183.
37. Davis L.C., et al. NAADP activates two-pore channels on T cell cytolytic granules to stimulate exocytosis and killing. Curr. Biol. 2012, 22(24):2331-2337.
38. Morgan A.J., et al. TPC: the NAADP discovery channel?. Biochem. Soc. Trans. 2015, 43(3):384-389.
39. Lee H.C. Cyclic ADP-ribose and nicotinic acid adenine dinucleotide phosphate (NAADP) as messengers for calcium mobilization. J. Biol. Chem. 2012, 287(38):31633-31640.
40. 2+) stores in sea urchin eggs. J. Biol. Chem. 2007, 282(52):37730-37737.
41. Steinhardt R.A., Bi G., Alderton J.M. Cell membrane resealing by a vesicular mechanism similar to neurotransmitter release. Science 1994, 263(5145):390-393.
42. 2+ and proteolysis in lethal oxidative injury in endothelial cells. Am. J. Physiol. 1991, 261(5 Pt 1):C889-C896.
43. Shen D., et al. Lipid storage disorders block lysosomal trafficking by inhibiting a TRP channel and lysosomal calcium release. Nat. Commun. 2012, 3:731.
44. Dong X.P., Wang X., Xu H. TRP channels of intracellular membranes. J. Neurochem. 2010, 113(2):313-328.
45. Luzio J.P., Pryor P.R., Bright N.A. Lysosomes: fusion and function. Nat. Rev. Mol. Cell Biol. 2007, 8(8):622-632.
46. Luzio J.P., Bright N.A., Pryor P.R. The role of calcium and other ions in sorting and delivery in the late endocytic pathway. Biochem. Soc. Trans. 2007, 35(Pt 5):1088-1091.
47. 2+) in late endosome-lysosome heterotypic fusion and in the reformation of lysosomes from hybrid organelles. J. Cell Biol. 2000, 149(5):1053-1062.
48. Adler E.M., et al. Alien intracellular calcium chelators attenuate neurotransmitter release at the squid giant synapse. J. Neurosci. 1991, 11(6):1496-1507.
49. Burgoyne R.D., Clague M.J. Calcium and calmodulin in membrane fusion. Biochim. Biophys. Acta 2003, 1641(2-3):137-143.
50. Hai A., Spira M.E. On-chip electroporation, membrane repair dynamics and transient in-cell recordings by arrays of gold mushroom-shaped microelectrodes. Lab Chip 2012, 12(16):2865-2873.
51. McDade J.R., Michele D.E. Membrane damage-induced vesicle-vesicle fusion of dysferlin-containing vesicles in muscle cells requires microtubules and kinesin. Hum. Mol. Genet. 2013, 23(7):1677-1686.
52. Marg A., et al. Sarcolemmal repair is a slow process and includes EHD2. Traffic 2012, 13(9):1286-1294.
53. Cheng X., et al. Mucolipins: Intracellular TRPML1-3 channels. FEBS Lett. 2010, 584(10):2013-2021.
54. Grimm C., et al. Role of TRPML and two-pore channels in endolysosomal cation homeostasis. J. Pharmacol. Exp. Ther. 2012, 342(2):236-244.
55. Abe K., Puertollano R. Role of TRP channels in the regulation of the endosomal pathway. Physiology (Bethesda) 2011, 26(1):14-22.
56. Sun M., et al. Mucolipidosis type IV is caused by mutations in a gene encoding a novel transient receptor potential channel. Hum. Mol. Genet. 2000, 9(17):2471-2478.
57. Bassi M.T., et al. Cloning of the gene encoding a novel integral membrane protein, mucolipidin-and identification of the two major founder mutations causing mucolipidosis type IV. Am. J. Hum. Genet. 2000, 67(5):1110-1120.
58. Bargal R., et al. Identification of the gene causing mucolipidosis type IV. Nat. Genet. 2000, 26(1):118-123.
59. Dong X.P., et al. PI(3,5)P(2) controls membrane trafficking by direct activation of mucolipin Ca (2+) release channels in the endolysosome. Nat. Commun. 2010, 1:p38.
60. Zhang X., Li X., Xu H. Phosphoinositide isoforms determine compartment-specific ion channel activity. Proc. Natl. Acad. Sci. U.S.A. 2012, 109(28):11384-11389.
61. Grimm C., et al. Small molecule activators of TRPML3. Chem. Biol. 2010, 17(2):135-148.
62. Wang W., et al. Up-regulation of lysosomal TRPML1 channels is essential for lysosomal adaptation to nutrient starvation. Proc. Natl. Acad. Sci. U.S.A. 2015, 112(11):E1373-E1381.
63. Shen D., Wang X., Xu H. Pairing phosphoinositides with calcium ions in endolysosomal dynamics: phosphoinositides control the direction and specificity of membrane trafficking by regulating the activity of calcium channels in the endolysosomes. Bioessays 2011, 33(6):448-457.
64. Thompson E.G., et al. Lysosomal trafficking functions of mucolipin-1 in murine macrophages. BMC Cell Biol. 2007, 8:p54.
65. Vergarajauregui S., et al. Autophagic dysfunction in mucolipidosis type IV patients. Hum. Mol. Genet. 2008, 17(17):2723-2737.
66. Dong X.P., et al. Activating mutations of the TRPML1 channel revealed by proline-scanning mutagenesis. J. Biol. Chem. 2009, 284(46):32040-32052.
67. Samie M., et al. A TRP channel in the lysosome regulates large particle phagocytosis via focal exocytosis. Dev. Cell 2013, 26(5):511-524.
68. Kim H.J., et al. A novel mode of TRPML3 regulation by extracytosolic pH absent in the varitint-waddler phenotype. EMBO J. 2008, 27(8):1197-1205.
69. Miao Y., et al. A TRP channel senses lysosome neutralization by pathogens to trigger their expulsion. Cell 2015, 161(6):1306-1319.
70. Farah C.A., et al. Autophosphorylation of the C2 domain inhibits translocation of the novel protein kinase C (nPKC) Apl II. J. Neurochem. 2012, 123(3):360-372.
71. Schiavo G., Osborne S.L., Sgouros J.G. Synaptotagmins: more isoforms than functions?. Biochem. Biophys. Res. Commun. 1998, 248(1):1-8.
72. Sudhof T.C. Synaptotagmins: why so many?. J. Biol. Chem. 2002, 277(10):7629-7632.
73. 2+-triggered exocytosis. Curr. Opin. Cell Biol. 2010, 22(4):496-505.
74. Schapire A.L., Valpuesta V., Botella M.A. Plasma membrane repair in plants. Trends Plant Sci. 2009, 14(12):645-652.
75. Schapire A.L., et al. Arabidopsis synaptotagmin 1 is required for the maintenance of plasma membrane integrity and cell viability. Plant Cell 2008, 20(12):3374-3388.
76. Butz S., et al. The subcellular localizations of atypical synaptotagmins III and VI, synaptotagmin III is enriched in synapses and synaptic plasma membranes but not in synaptic vesicles. J. Biol. Chem. 1999, 274(26):18290-18296.
77. Sudhof T.C., Rizo J. Synaptotagmins: C2-domain proteins that regulate membrane traffic. Neuron 1996, 17(3):379-388.
78. Rao S.K., et al. Identification of SNAREs involved in synaptotagmin VII-regulated lysosomal exocytosis. J. Biol. Chem. 2004, 279(19):20471-20479.
79. Posey A.D., Demonbreun A., McNally E.M. Ferlin proteins in myoblast fusion and muscle growth. Curr. Top. Dev. Biol. 2011, 96:203-230.
80. Jimenez J.L., Bashir R. In silico functional and structural characterisation of ferlin proteins by mapping disease-causing mutations and evolutionary information onto three-dimensional models of their C2 domains. J. Neurol. Sci. 2007, 260(1-2):114-123.
81. Britton S., et al. The third human FER-1-like protein is highly similar to dysferlin. Genomics 2000, 68(3):313-321.
82. Achanzar W.E., Ward S. A nematode gene required for sperm vesicle fusion. J. Cell Sci. 1997, 110(Pt 9):1073-1081.
83. Lek A., et al. Phylogenetic analysis of ferlin genes reveals ancient eukaryotic origins. BMC Evol. Biol. 2010, 10:p231.
84. Han R., Campbell K.P. Dysferlin and muscle membrane repair. Curr. Opin. Cell Biol. 2007, 19(4):409-416.
85. Nalefski E.A., Falke J.J. The C2 domain calcium-binding motif: structural and functional diversity. Prot. Sci. 1996, 5(12):2375-2390.
86. Illa I., et al. Distal anterior compartment myopathy: a dysferlin mutation causing a new muscular dystrophy phenotype. Ann. Neurol. 2001, 49(1):130-134.
87. Bashir R., et al. A gene related to Caenorhabditis elegans spermatogenesis factor fer-1 is mutated in limb-girdle muscular dystrophy type 2B. Nat. Genet. 1998, 20(1):37-42.
88. Liu J., et al. Dysferlin, a novel skeletal muscle gene, is mutated in Miyoshi myopathy and limb girdle muscular dystrophy. Nat. Genet. 1998, 20(1):31-36.
89. Bansal D., et al. Defective membrane repair in dysferlin-deficient muscular dystrophy. Nature 2003, 423(6936):168-172.
90. Davis D.B., et al. Calcium-sensitive phospholipid binding properties of normal and mutant ferlin C2 domains. J. Biol. Chem. 2002, 277(25):22883-22888.
91. Lek A., et al. Calpains, cleaved mini-dysferlinC72, and L-type channels underpin calcium-dependent muscle membrane repair. J. Neurosci. 2013, 33(12):5085-5094.
92. Redpath G.M., et al. Calpain cleavage within dysferlin exon 40a releases a synaptotagmin-like module for membrane repair. Mol. Biol. Cell 2014, 25(19):3037-3048.
93. Doherty K.R., et al. Normal myoblast fusion requires myoferlin. Development 2005, 132(24):5565-5575.
94. Davis D.B., et al. Myoferlin, a candidate gene and potential modifier of muscular dystrophy. Hum. Mol. Genet. 2000, 9(2):217-226.
95. Demonbreun A.R., et al. Myoferlin regulation by NFAT in muscle injury, regeneration and repair. J. Cell Sci. 2010, 123(Pt 14):2413-2422.
96. 2+ signalling to membrane dynamics. Nat. Rev. Mol. Cell Biol. 2005, 6(6):449-461.
97. Moss S.E., Morgan R.O. The annexins. Genome Biol. 2004, 5(4):219.
98. Draeger A., Wray S., Babiychuk E.B. Domain architecture of the smooth-muscle plasma membrane: regulation by annexins. Biochem. J. 2005, 387(Pt 2):309-314.
99. Rambotti M.G., Spreca A., Donato R. Immunocytochemical localization of annexins V and VI in human placentae of different gestational ages. Cell Mol. Biol. Res. 1993, 39(6):579-588.
100. Diakonova M., et al. Localization of five annexins in J774 macrophages and on isolated phagosomes. J. Cell Sci. 1997, 110(Pt 10):1199-1213.
101. Zobiack N., et al. The annexin 2/S100A10 complex controls the distribution of transferrin receptor-containing recycling endosomes. Mol. Biol. Cell 2003, 14(12):4896-4908.
102. Mayran N., Parton R.G., Gruenberg J. Annexin II regulates multivesicular endosome biogenesis in the degradation pathway of animal cells. EMBO J. 2003, 22(13):3242-3253.
103. Merrifield C.J., et al. Endocytic vesicles move at the tips of actin tails in cultured mast cells. Nat. Cell Biol. 1999, 1(1):72-74.
104. Roostalu U., Strahle U. In vivo imaging of molecular interactions at damaged sarcolemma. Dev. Cell 2012, 22(3):515-529.
105. Carmeille R., et al. Annexin-A5 promotes membrane resealing in human trophoblasts. Biochim. Biophys. Acta 2015, 1853(9):2033-2044.
106. 2+-binding proteins. Biochemistry 1999, 38(23):7498-7508.
107. Missotten M., et al. Alix, a novel mouse protein undergoing calcium-dependent interaction with the apoptosis-linked-gene 2 (ALG-2) protein. Cell Death Differ. 1999, 6(2):124-129.
108. Katoh K., et al. The penta-EF-hand protein ALG-2 interacts directly with the ESCRT-I component TSG101, and Ca2+-dependently co-localizes to aberrant endosomes with dominant-negative AAA ATPase SKD1/Vps4B. Biochem. J. 2005, 391(Pt 3):677-685.
109. Satoh H., et al. ALG-2 interacts with the amino-terminal domain of annexin XI in a Ca(2+)-dependent manner. Biochem. Biophys. Res. Commun. 2002, 291(5):1166-1172.
110. 2+-dependent manner. Biochim. Biophys. Acta 2002, 1600(1-2):61-67.
111. Tarabykina S., et al. ALG-2, a multifunctional calcium binding protein?. Front. Biosci. 2004, 9:1817-1832.
112. Helm J.R., et al. Apoptosis-linked gene-2 (ALG-2)/Sec31 interactions regulate endoplasmic reticulum (ER)-to-Golgi transport: a potential effector pathway for luminal calcium. J. Biol. Chem. 2014, 289(34):23609-23628.
113. 2+-dependent interactor of mucolipin-1. J. Biol. Chem. 2009, 284(52):36357-36366.
114. Ono Y., Sorimachi H. Calpains: an elaborate proteolytic system. Biochim. Biophys. Acta 2012, 1824(1):224-236.
115. Nigro V., Savarese M. Genetic basis of limb-girdle muscular dystrophies: the 2014 update. Acta Myol. 2014, 33(1):1-12.
116. 2+)-triggered protease activity and cytoskeletal disassembly. J. Neurosci. 1991, 11(10):3257-3267.
117. Godell C.M., et al. Calpain activity promotes the sealing of severed giant axons. Proc. Natl. Acad. Sci. U.S.A. 1997, 94(9):4751-4756.
118. Mellgren R.L., et al. Calpain is required for the rapid, calcium-dependent repair of wounded plasma membrane. J. Biol. Chem. 2007, 282(4):2567-2575.
119. Mellgren R.L., et al. Calcium-dependent plasma membrane repair requires m- or mu-calpain, but not calpain-3, the proteasome, or caspases. Biochim. Biophys. Acta 2009, 1793(12):1886-1893.
120. Stohr H., et al. TMEM16B, a novel protein with calcium-dependent chloride channel activity, associates with a presynaptic protein complex in photoreceptor terminals. J. Neurosci. 2009, 29(21):6809-6818.
121. Yang Y.D., et al. TMEM16A confers receptor-activated calcium-dependent chloride conductance. Nature 2008, 455(7217):1210-1215.
122. Schroeder B.C., et al. Expression cloning of TMEM16A as a calcium-activated chloride channel subunit. Cell 2008, 134(6):1019-1029.
123. Caputo A., et al. TMEM16A, a membrane protein associated with calcium-dependent chloride channel activity. Science 2008, 322(5901):590-594.
124. 2+-activated Cl-channels. J. Physiol. 2009, 587(Pt 10):2127-2139.
125. Almaca J., et al. TMEM16 proteins produce volume-regulated chloride currents that are reduced in mice lacking TMEM16A. J. Biol. Chem. 2009, 284(42):28571-28578.
126. Galindo B.E., Vacquier V.D. Phylogeny of the TMEM16 protein family: some members are overexpressed in cancer. Int. J. Mol. Med. 2005, 16(5):919-924.
127. Mizuta K., et al. Molecular characterization of GDD1/TMEM16E, the gene product responsible for autosomal dominant gnathodiaphyseal dysplasia. Biochem. Biophys. Res. Commun. 2007, 357(1):126-132.
128. Duran C., et al. ANOs 3-7 in the anoctamin/Tmem16 Cl- channel family are intracellular proteins. Am. J. Physiol. Cell Physiol. 2012, 302(3):C482-C493.