Differential Regulation of Ion Channels Function by Proteolysis

Overview

Journal Biochim Biophys Acta Mol Cell Res

Publisher Elsevier

Specialties Biochemistry
Biophysics
Cell Biology

Date 2018 Jul 17

PMID 30009861

Citations 6

Authors

Liwei Wang

David I Yule

Affiliations

Soon will be listed here.

Abstract

Ion channels are pore-forming protein complexes in membranes that play essential roles in a diverse array of biological activities. Ion channel activity is strictly regulated at multiple levels and by numerous cellular events to selectively activate downstream effectors involved in specific biological activities. For example, ions, binding proteins, nucleotides, phosphorylation, the redox state, channel subunit composition have all been shown to regulate channel activity and subsequently allow channels to participate in distinct cellular events. While these forms of modulation are well documented and have been extensively reviewed, in this article, we will first review and summarize channel proteolysis as a novel and quite widespread mechanism for altering channel activity. We will then highlight the recent findings demonstrating that proteolysis profoundly alters Inositol 1,4,5 trisphosphate receptor activity, and then discuss its potential functional ramifications in various developmental and pathological conditions.

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References

Maes K, Missiaen L, Parys J, de Smet P, Sienaert I, Waelkens E . Mapping of the ATP-binding sites on inositol 1,4,5-trisphosphate receptor type 1 and type 3 homotetramers by controlled proteolysis and photoaffinity labeling. J Biol Chem. 2000; 276(5):3492-7. DOI: 10.1074/jbc.M006082200. View

Hirota J, Furuichi T, Mikoshiba K . Inositol 1,4,5-trisphosphate receptor type 1 is a substrate for caspase-3 and is cleaved during apoptosis in a caspase-3-dependent manner. J Biol Chem. 1999; 274(48):34433-7. DOI: 10.1074/jbc.274.48.34433. View

Shimizu N, Sato N, Kikuchi T, Ishizaki T, Kobayashi K, Kita K . A sustained increase in the intracellular Ca²⁺ concentration induces proteolytic cleavage of EAG2 channel. Int J Biochem Cell Biol. 2014; 59:126-34. DOI: 10.1016/j.biocel.2014.12.007. View

Yule D, Betzenhauser M, Joseph S . Linking structure to function: Recent lessons from inositol 1,4,5-trisphosphate receptor mutagenesis. Cell Calcium. 2010; 47(6):469-79. PMC: 3086728. DOI: 10.1016/j.ceca.2010.04.005. View

Dupont G, Combettes L, Bird G, Putney J . Calcium oscillations. Cold Spring Harb Perspect Biol. 2011; 3(3). PMC: 3039928. DOI: 10.1101/cshperspect.a004226. View

Michailidis I, Abele-Henckels K, Zhang W, Lin B, Yu Y, Geyman L . Age-related homeostatic midchannel proteolysis of neuronal L-type voltage-gated Ca²⁺ channels. Neuron. 2014; 82(5):1045-57. PMC: 4052215. DOI: 10.1016/j.neuron.2014.04.017. View

Kruger B, Albrecht E, Lerch M . The role of intracellular calcium signaling in premature protease activation and the onset of pancreatitis. Am J Pathol. 2000; 157(1):43-50. PMC: 1850214. DOI: 10.1016/S0002-9440(10)64515-4. View

Bansaghi S, Golenar T, Madesh M, Csordas G, RamachandraRao S, Sharma K . Isoform- and species-specific control of inositol 1,4,5-trisphosphate (IP3) receptors by reactive oxygen species. J Biol Chem. 2014; 289(12):8170-81. PMC: 3961646. DOI: 10.1074/jbc.M113.504159. View

Wang L, Alzayady K, Yule D . Proteolytic fragmentation of inositol 1,4,5-trisphosphate receptors: a novel mechanism regulating channel activity?. J Physiol. 2015; 594(11):2867-76. PMC: 4887670. DOI: 10.1113/JP271140. View

10.

Bezprozvanny I . The inositol 1,4,5-trisphosphate receptors. Cell Calcium. 2005; 38(3-4):261-72. DOI: 10.1016/j.ceca.2005.06.030. View

11.

Greka A, Navarro B, Oancea E, Duggan A, Clapham D . TRPC5 is a regulator of hippocampal neurite length and growth cone morphology. Nat Neurosci. 2003; 6(8):837-45. DOI: 10.1038/nn1092. View

12.

Hughey R, Bruns J, Kinlough C, Harkleroad K, Tong Q, Carattino M . Epithelial sodium channels are activated by furin-dependent proteolysis. J Biol Chem. 2004; 279(18):18111-4. DOI: 10.1074/jbc.C400080200. View

13.

Brocard C, Plantier V, Boulenguez P, Liabeuf S, Bouhadfane M, Viallat-Lieutaud A . Cleavage of Na(+) channels by calpain increases persistent Na(+) current and promotes spasticity after spinal cord injury. Nat Med. 2016; 22(4):404-11. DOI: 10.1038/nm.4061. View

14.

Alzayady K, Sebe-Pedros A, Chandrasekhar R, Wang L, Ruiz-Trillo I, Yule D . Tracing the Evolutionary History of Inositol, 1, 4, 5-Trisphosphate Receptor: Insights from Analyses of Capsaspora owczarzaki Ca2+ Release Channel Orthologs. Mol Biol Evol. 2015; 32(9):2236-53. PMC: 4540961. DOI: 10.1093/molbev/msv098. View

15.

Poirot O, Vukicevic M, Boesch A, Kellenberger S . Selective regulation of acid-sensing ion channel 1 by serine proteases. J Biol Chem. 2004; 279(37):38448-57. DOI: 10.1074/jbc.M407381200. View

16.

Meighan P, Meighan S, Rich E, Lane Brown R, Varnum M . Matrix metalloproteinase-9 and -2 enhance the ligand sensitivity of photoreceptor cyclic nucleotide-gated channels. Channels (Austin). 2012; 6(3):181-96. PMC: 3431585. DOI: 10.4161/chan.20904. View

17.

Antigny F, Konig S, Bernheim L, Frieden M . Inositol 1,4,5 trisphosphate receptor 1 is a key player of human myoblast differentiation. Cell Calcium. 2014; 56(6):513-21. DOI: 10.1016/j.ceca.2014.10.014. View

18.

Mound A, Vautrin-Glabik A, Foulon A, Botia B, Hague F, Parys J . Downregulation of type 3 inositol (1,4,5)-trisphosphate receptor decreases breast cancer cell migration through an oscillatory Ca signal. Oncotarget. 2017; 8(42):72324-72341. PMC: 5641133. DOI: 10.18632/oncotarget.20327. View

19.

Rajamani S, Anderson C, Valdivia C, Eckhardt L, Foell J, Robertson G . Specific serine proteases selectively damage KCNH2 (hERG1) potassium channels and I(Kr). Am J Physiol Heart Circ Physiol. 2005; 290(3):H1278-88. DOI: 10.1152/ajpheart.00777.2005. View

20.

Schulman J, Wright F, Kaufmann T, Wojcikiewicz R . The Bcl-2 protein family member Bok binds to the coupling domain of inositol 1,4,5-trisphosphate receptors and protects them from proteolytic cleavage. J Biol Chem. 2013; 288(35):25340-25349. PMC: 3757198. DOI: 10.1074/jbc.M113.496570. View