BK channel density is regulated by endoplasmic reticulum associated degradation and influenced by the SKN-1A/NRF1 transcription factor
Autoři:
Timothy P. Cheung aff001; Jun-Yong Choe aff002; Janet E. Richmond aff004; Hongkyun Kim aff001
Působiště autorů:
Center for Cancer Cell Biology, Immunology, and Infection, Department of Cell Biology and Anatomy, Chicago Medical School, Rosalind Franklin University of Medicine & Science, North Chicago, Illinois, United States of America
aff001; School of Graduate & Postdoctoral Studies, Rosalind Franklin University of Medicine & Science, North Chicago, Illinois, United States of America
aff002; Department of Biochemistry and Molecular Biology, Rosalind Franklin University of Medicine & Science, North Chicago, Illinois United States of America
aff003; Department of Biological Sciences, University of Illinois at Chicago, Chicago, Illinois, United States of America
aff004
Vyšlo v časopise:
BK channel density is regulated by endoplasmic reticulum associated degradation and influenced by the SKN-1A/NRF1 transcription factor. PLoS Genet 16(6): e32767. doi:10.1371/journal.pgen.1008829
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008829
Souhrn
Ion channels are present at specific levels within subcellular compartments of excitable cells. The regulation of ion channel trafficking and targeting is an effective way to control cell excitability. The BK channel is a calcium-activated potassium channel that serves as a negative feedback mechanism at presynaptic axon terminals and sites of muscle excitation. The C. elegans BK channel ortholog, SLO-1, requires an endoplasmic reticulum (ER) membrane protein for efficient anterograde transport to these locations. Here, we found that, in the absence of this ER membrane protein, SLO-1 channels that are seemingly normally folded and expressed at physiological levels undergo SEL-11/HRD1-mediated ER-associated degradation (ERAD). This SLO-1 degradation is also indirectly regulated by a SKN-1A/NRF1-mediated transcriptional mechanism that controls proteasome levels. Therefore, our data indicate that SLO-1 channel density is regulated by the competitive balance between the efficiency of ER trafficking machinery and the capacity of ERAD.
Klíčová slova:
Caenorhabditis elegans – Deletion mutation – Endoplasmic reticulum – Point mutation – Proteasomes – Scanning electron microscopy – Ubiquitin ligases – Calcium-activated potassium channels
Zdroje
1. Roberts WM, Jacobs RA, Hudspeth AJ. Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells. J Neurosci. 1990;10: 3664–84. Available: http://www.ncbi.nlm.nih.gov/pubmed/1700083 doi: 10.1523/JNEUROSCI.10-11-03664.1990 1700083
2. Robitaille R, Charlton MP. Presynaptic Calcium Signals and Transmitter by Calcium-activated Potassium Channels. J Neurosci. 1992; 297–305. doi: 10.1523/JNEUROSCI.12-01-00297.1992 1370323
3. Hu H, Shao LR, Chavoshy S, Gu N, Trieb M, Behrens R, et al. Presynaptic Ca2+-activated K+ channels in glutamatergic hippocampal terminals and their role in spike repolarization and regulation of transmitter release. J Neurosci. 2001;21: 9585–9597. 21/24/9585 [pii] doi: 10.1523/JNEUROSCI.21-24-09585.2001 11739569
4. Knot H. Ryanodine receptors regulate arterial wall and diameter in cerebral arteries of rat via K Ca channels. J Physiol. 1998; 211–221. Available: http://scholar.google.co.uk/scholar?hl=en&q=%22hj+knot%22&as_sdt=0,5&as_ylo=&as_vis=0#55
5. McManus OB, Helms LMH, Pallanck L, Ganetzky B, Swanson R, Leonard RJ. Functional role of the β subunit of high conductance calcium-activated potassium channels. Neuron. 1995;14: 645–650. doi: 10.1016/0896-6273(95)90321-6 7695911
6. Brenner R, Peréz GJ, Bonev a D, Eckman DM, Kosek JC, Wiler SW, et al. Vasoregulation by the beta1 subunit of the calcium-activated potassium channel. Nature. 2000;407: 870–876. doi: 10.1038/35038011 11057658
7. Tricarico D, Barbieri M, Camerino DC. Acetazolamide opens the muscular K(Ca)2+ channel: A novel mechanism of action that may explain the therapeutic effect of the drug in hypokalemic periodic paralysis. Ann Neurol. 2000;48: 304–312. doi: 10.1002/1531-8249(200009)48:3<304::AID-ANA4>3.0.CO;2-A 10976636
8. Girouard H, Bonev AD, Hannah RM, Meredith A, Aldrich RW, Nelson MT. Astrocytic endfoot Ca2+ and BK channels determine both arteriolar dilation and constriction. Proc Natl Acad Sci U S A. 2010;107: 3811–3816. doi: 10.1073/pnas.0914722107 20133576
9. Leo MD, Jaggar JH. Trafficking of BK channel subunits controls arterial contractility. Oncotarget. 2017;8: 106149–106150. doi: 10.18632/oncotarget.22280 29290926
10. Dennis Leo M, Bulley S, Bannister JP, Kuruvilla KP, Narayanan D, Jaggar JH. Angiotensin II stimulates internalization and degradation of arterial myocyte plasma membrane BK channels to induce vasoconstriction. Am J Physiol—Cell Physiol. 2015;309: C392–C402. doi: 10.1152/ajpcell.00127.2015 26179602
11. Holtzclaw JD, Grimm PR, Sansom SC. Role of BK channels in hypertension and potassium secretion. Curr Opin Nephrol Hypertens. 2011;20: 512–517. doi: 10.1097/MNH.0b013e3283488889 21670674
12. Davies AG, Pierce-Shimomura JT, Kim H, VanHoven MK, Thiele TR, Bonci A, et al. A Central Role of the BK Potassium Channel in Behavioral Responses to Ethanol in C. elegans. Cell. 2003;115: 655–666. doi: 10.1016/s0092-8674(03)00979-6 14675531
13. Bettinger JC, Davies AG. The role of the BK channel in ethanol response behaviors: Evidence from model organism and human studies. Front Physiol. 2014;5 AUG: 1–9. doi: 10.3389/fphys.2014.00001
14. Lee US, Cui J. Beta subunit-specific modulations of BK channel function by a mutation associated with epilepsy and dyskinesia. J Physiol. 2009;587: 1481–1498. doi: 10.1113/jphysiol.2009.169243 19204046
15. Deng PY, Klyachko VA. Genetic upregulation of BK channel activity normalizes multiple synaptic and circuit defects in a mouse model of fragile X syndrome. J Physiol. 2016;594: 83–97. doi: 10.1113/JP271031 26427907
16. Wang L, Kang H, Li Y, Shui Y, Yamamoto R, Sugai T, et al. Cognitive recovery by chronic activation of the large-conductance calcium-activated potassium channel in a mouse model of Alzheimer’s disease. Neuropharmacology. 2015;92: 8–15. doi: 10.1016/j.neuropharm.2014.12.033 25577958
17. Kim H, Oh KH. Protein Network Interacting with BK Channels. Int Rev Neurobiol. 2016;128: 127–161. doi: 10.1016/bs.irn.2016.03.003 27238263
18. Yuan P, Leonetti MD, Pico AR, Hsiung Y, MacKinnon R. Structure of the Human BK Channel Ca2+-Activation Apparatus at 3.0A Resolution. 2010;329: 182–186. doi: 10.1126/science.1190414.Structure
19. Wei A, Solaro C, Lingle C, Salkoff L. Calcium Sensitivity of BKType Kca Channels Determined by a Separable Domain. Neuron. 1994;13: 671–681. doi: 10.1016/0896-6273(94)90034-5 7917297
20. Oh KH, Kim H. BK channel clustering is required for normal behavioral alcohol sensitivity in C. elegans. Sci Rep. 2019;9: 10224. doi: 10.1038/s41598-019-46615-9 31308408
21. Oh K, Haney JJ, Wang X, Chuang CF, Richmond JE, Kim H. ERG-28 controls BK channel trafficking in the ER to regulate synaptic function and alcohol response in C. Elegans. Elife. 2017;6: 1–21. doi: 10.7554/eLife.24733 28168949
22. Gaynor EC, Heesen S, Graham TR, Aebi M, Emr SD. Signal-mediated Retrieval of a Membrane Protein from the Golgi to the ER in Yeast. 1994;127: 653–665.
23. Zerangue N, Malan MJ, Fried SR, Dazin PF, Jan YN, Jan LY, et al. Analysis of endoplasmic reticulum trafficking signals by combinatorial screening in mammalian cells. Proc Natl Acad Sci U S A. 2001;98: 2431–2436. doi: 10.1073/pnas.051630198 11226256
24. Gil G, Faust JR, Chin DJ, Goldstein JL, Brown MS. Membrane-bound domain of HMG CoA reductase is required for sterol-enhanced degradation of the enzyme. Cell. 1985;41: 249–258. doi: 10.1016/0092-8674(85)90078-9 3995584
25. Song BL, Sever N, DeBose-Boyd RA. Gp78, a membrane-anchored ubiquitin ligase, associates with Insig-1 and couples sterol-regulated ubiquitination to degradation of HMG CoA reductase. Mol Cell. 2005;19: 829–840. doi: 10.1016/j.molcel.2005.08.009 16168377
26. Foresti O, Ruggiano A, Hannibal-Bach HK, Ejsing CS, Carvalho P. Sterol homeostasis requires regulated degradation of squalene monooxygenase by the ubiquitin ligase Doa10/Teb4. Elife. 2013;2013: 1–17. doi: 10.7554/eLife.00953 23898401
27. Lehrbach NJ, Ruvkun G. Proteasome dysfunction triggers activation of SKN-1A/Nrf1 by the aspartic protease DDI-1. Elife. 2016;5: 1–19. doi: 10.7554/eLife.17721.001
28. Lehrbach NJ, Ruvkun G. Endoplasmic reticulum-associated SKN-1A/Nrf1 mediates a cytoplasmic unfolded protein response and promotes longevity. Elife. 2019;8: 1–25. doi: 10.7554/eLife.44425 30973820
29. Lehrbach NJ, Breen PC, Ruvkun G. Protein Sequence Editing of SKN-1A/Nrf1 by Peptide:N-Glycanase Controls Proteasome Gene Expression. Cell. 2019;177: 737–750.e15. doi: 10.1016/j.cell.2019.03.035 31002798
30. Darom A, Benin-Abu-Shach U, Brody L. RNF-121 Is an Endoplasmic Reticulum-Membrane E3 Ubiquitin Ligase Involved in the Regulation of Beta-Integrin. Mol Biol Cell. 2010;21: 1788–1798. doi: 10.1091/mbc.e09-09-0774 20357004
31. Hamamichi S, Rivas RN, Knight AL, Cao S, Caldwell KA, Caldwell GA. Hypothesis-based RNAi screening identifies neuroprotective genes in a Parkinson’s disease model. Proc Natl Acad Sci U S A. 2008;105: 728–733. doi: 10.1073/pnas.0711018105 18182484
32. Sasagawa Y, Yamanaka K, Ogura T. ER E3 ubiquitin ligase HRD-1 and its specific partner chaperone BiP play important roles in ERAD and developmental growth in Caenorhabditis elegans. Genes to Cells. 2007;12: 1063–1073. doi: 10.1111/j.1365-2443.2007.01108.x 17825049
33. Urano F, Calfon M, Yoneda T, Yun C, Kiraly M, Clark SG, et al. A survival pathway for Caenorhabditis elegans with a blocked unfolded protein response. J Cell Biol. 2002;158: 639–646. doi: 10.1083/jcb.200203086 12186849
34. He L, Skirkanich J, Moronetti L, Lewis R, Lamitina T. The cystic-fibrosis-associated ΔF508 mutation confers post-transcriptional destabilization on the C. elegans ABC transporter PGP-3. DMM Dis Model Mech. 2012;5: 930–939. doi: 10.1242/dmm.008987 22569626
35. Safra M, Ben-hamo S, Kenyon C, Henis-korenblit S. The ire-1 ER stress-response pathway is required for normal secretory-protein metabolism in C. elegans. 2013; 4136–4146. doi: 10.1242/jcs.123000 23843615
36. Oh K, Kim H. Aldicarb-induced Paralysis Assay to Determine Defects in Synaptic Transmission in Caenorhabditis elegans. BIO-PROTOCOL. 2017;7: 1–11. doi: 10.21769/BioProtoc.2400 28868330
37. Mahoney TR, Luo S, Nonet ML. Analysis of synaptic transmission in Caenorhabditis elegans using an aldicarb-sensitivity assay. 2006;1. doi: 10.1038/nprot.2006.281 17487159
38. Zhang Y, Niu X, Brelidze TI, Magleby KL. Ring of negative charge in BK channels facilitates block by intracellular Mg2+ and polyamines through electrostatics. J Gen Physiol. 2006;128: 185–202. doi: 10.1085/jgp.200609493 16847096
39. Omura T, Kaneko M, Onoguchi M, Koizumi S, Itami M, Ueyama M, et al. Novel functions of ubiquitin ligase HRD1 with transmembrane and proline-rich domains. J Pharmacol Sci. 2008;106: 512–519. doi: 10.1254/jphs.08005fp 18344614
40. Vashistha N, Neal SE, Singh A, Carroll SM, Hampton RY. Direct and essential function for Hrd3 in ER-associated degradation. Proc Natl Acad Sci. 2016;113: 5934–5939. doi: 10.1073/pnas.1603079113 27170191
41. Denic V, Quan EM, Weissman JS. A Luminal Surveillance Complex that Selects Misfolded Glycoproteins for ER-Associated Degradation. Cell. 2006;126: 349–359. doi: 10.1016/j.cell.2006.05.045 16873065
42. Schoebel S, Mi W, Stein A, Ovchinnikov S, Pavlovicz R, DImaio F, et al. Cryo-EM structure of the protein-conducting ERAD channel Hrd1 in complex with Hrd3. Nature. 2017;548: 352–355. doi: 10.1038/nature23314 28682307
43. Carvalho P, Goder V, Rapoport TA. Distinct Ubiquitin-Ligase Complexes Define Convergent Pathways for the Degradation of ER Proteins. Cell. 2006;126: 361–373. doi: 10.1016/j.cell.2006.05.043 16873066
44. Wu X, Rapoport TA. Mechanistic insights into ER-associated protein degradation. Curr Opin Cell Biol. 2018;53: 22–28. doi: 10.1016/j.ceb.2018.04.004 29719269
45. Zattas D, Adle DJ, Rubenstein EM, Hochstrasser M. N-terminal acetylation of the yeast Derlin Der1 is essential for Hrd1 ubiquitin-ligase activity toward luminal ER substrates. Mol Biol Cell. 2013;24: 890–900. doi: 10.1091/mbc.E12-11-0838 23363603
46. Lilley BN, Ploegh HL. A membrane protein required for dislocation of misfolded proteins from the ER. Nature. 2004;429: 834–840. doi: 10.1038/nature02592 15215855
47. Neal S, Jaeger PA, Duttke SH, Benner CK, Glass C, Ideker T, et al. The Dfm1 Derlin Is Required for ERAD Retrotranslocation of Integral Membrane Proteins. Mol Cell. 2018;69: 306–320.e4. doi: 10.1016/j.molcel.2017.12.012 29351849
48. Bodnar N, Rapoport TA. Molecular Mechanism of Substrate Processing by the Cdc48 ATPase Complex. Cell. 2017;169: 722–735.e9. doi: 10.1016/j.cell.2017.04.020 28475898
49. Ye Y, Tang WK, Zhang T, Xia D. A Mighty “Protein Extractor” of the Cell: Structure and Function of the p97/CDC48 ATPase. Front Mol Biosci. 2017;4: 1–20. doi: 10.3389/fmolb.2017.00001
50. Yamanaka K, Okubo Y, Suzaki T, Ogura T. Analysis of the two p97/VCP/Cdc48p proteins of Caenorhabditis elegans and their suppression of polyglutamine-induced protein aggregation. J Struct Biol. 2004;146: 242–250. doi: 10.1016/j.jsb.2003.11.017 15037255
51. Nowicka U, Zhang D, Walker O, Krutauz D, Castañeda CA, Chaturvedi A, et al. DNA-damage-inducible 1 protein (Ddi1) contains an uncharacteristic ubiquitin-like domain that binds ubiquitin. Structure. 2015;23: 542–557. doi: 10.1016/j.str.2015.01.010 25703377
52. Sivá M, Svoboda M, Veverka V, Trempe JF, Hofmann K, Kožíšek M, et al. Human DNA-Damage-Inducible 2 Protein Is Structurally and Functionally Distinct from Its Yeast Ortholog. Sci Rep. 2016;6: 1–15. doi: 10.1038/s41598-016-0001-8
53. Hill SE, Kauffman KJ, Krout M, Richmond JE, Melia TJ, Colón-Ramos DA. Maturation and Clearance of Autophagosomes in Neurons Depends on a Specific Cysteine Protease Isoform, ATG-4.2. Dev Cell. 2019;49: 251–26. doi: 10.1016/j.devcel.2019.02.013 30880001
54. Blackwell TK, Steinbaugh MJ, Hourihan JM, Ewald CY, Isik M. SKN-1/Nrf, stress responses, and aging in Caenorhabditis elegans. Free Radic Biol Med. 2015;88: 290–301. doi: 10.1016/j.freeradbiomed.2015.06.008 26232625
55. Koizumi S, Irie T, Hirayama S, Sakurai Y, Yashiroda H, Naguro I, et al. The aspartyl protease DDI2 activates Nrf1 to compensate for proteasome dysfunction. Elife. 2016;5: 1–10. doi: 10.7554/elife.18357 27528193
56. Johnson BM, DeBose-Boyd RA. Underlying Mechanisms for Sterol-Induced Ubiquitination and ER-Associated Degradation of HMG CoA Reductase. Semin Cell Dev Biol. 2018;81: 121–128. doi: 10.1016/j.semcdb.2017.10.019 29107682
57. Bodnar N, Rapoport T. Toward an understanding of the Cdc48/p97 ATPase. F1000Research. 2017;6: 1318. doi: 10.12688/f1000research.11683.1 28815021
58. Yamauchi S, Yamanaka K, Ogura T. Comparative analysis of expression of two p97 homologues in Caenorhabditis elegans. Biochem Biophys Res Commun. 2006;345: 746–753. doi: 10.1016/j.bbrc.2006.04.160 16701565
59. Badros A, Goloubeva O, Dalal JS, Can I, Thompson J, Rapoport AP, et al. Neurotoxicity of bortezomib therapy in multiple myeloma: A single-center experience and review of the literature. Cancer. 2007;110: 1042–1049. doi: 10.1002/cncr.22921 17654660
60. Jagannath S, Barlogie B, Berenson J, Siegel D, Irwin D, Richardson PG, et al. A phase 2 study of two doses of bortezomib in relapsed or refractory myeloma. Br J Haematol. 2004;127: 165–172. doi: 10.1111/j.1365-2141.2004.05188.x 15461622
61. Liu H, Xu R, Huang H. Peripheral neuropathy outcomes and efficacy of subcutaneous bortezomib when combined with thalidomide and dexamethasone in the treatment of multiple myeloma. Exp Ther Med. 2016;12: 3041–3046. doi: 10.3892/etm.2016.3738 27882113
62. Moreira MMC, Rodrigues AB, De Oliveira PP, De Aguiar MIF, Da Cunha GH, Pinto RMC, et al. Peripheral neuropathy in people with multiple myeloma. ACTA Paul Enferm. 2018;31: 439–445. doi: 10.1590/1982-0194201800061
63. Bentzen BH, Olesen SP, Rønn LCB, Grunnet M. BK channel activators and their therapeutic perspectives. Front Physiol. 2014;5: 1–12. doi: 10.3389/fphys.2014.00001
64. Goda AA, Siddique AB, Mohyeldin M, Ayoub NM, El Sayed KA. The Maxi-K (BK) channel antagonist penitrem a as a novel breast cancer-targeted therapeutic. Mar Drugs. 2018;16: 1–21. doi: 10.3390/md16050157 29751615
65. Arribere JA, Bell RT, Fu BXH, Artiles KL, Hartman PS, Fire AZ. Efficient marker-free recovery of custom genetic modifications with CRISPR/Cas9 in Caenorhabditis elegans. Genetics. 2014;198: 837–846. doi: 10.1534/genetics.114.169730 25161212
66. Richmond J. Synaptic function. WormBook. 2006; 1–15. doi: 10.1895/wormbook.1.69.1 18050398
67. Frøkjær-Jensen C, Davis MW, Sarov M, Taylor J, Flibotte S, LaBella M, et al. Random and targeted transgene insertion in Caenorhabditis elegans using a modified Mos1 transposon. Nat Methods. 2014;11: 529–534. doi: 10.1038/nmeth.2889 24820376
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