The Kv1.3 K+ channel in the immune system and its “precision pharmacology” using peptide toxins
Tóm tắt
Từ khóa
Tài liệu tham khảo
Asuncion XE, Sampaco A-RB, Adorna H, Magadia J, BoÒgolan VP, Lluisma A (2019) Predicting the molecular targets of conopeptides by using principal component analysis and multiclass logistic regression philippine. J Sci 148:237–245
Bartok A, Fehér K, Bodor A, Rákosi K, Tóth GK, Kövér KE, Panyi G, Varga Z (2015a) An engineered scorpion toxin analogue with improved Kv1.3 selectivity displays reduced conformational flexibility. Sci. Rep. 5:18397. https://doi.org/10.1038/srep18397
Bartok A, Panyi G, Varga Z (2015b) Potassium channel blocking peptide toxins from scorpion venom. In: Gopalakrishnakone P, Possani L, Schwartz EF, de la Vega RR (eds) Scorpion venoms, vol 4. Springer, Dordrecht, pp 493–527
Beeton C, Pennington MW, Wulff H, Singh S, Nugent D, Crossley G, Khaytin I, Calabresi PA, Chen CY, Gutman GA, Chandy KG (2005) Targeting effector memory T cells with a selective peptide inhibitor of Kv1.3 channels for therapy of autoimmune diseases. Mol Pharmacol 67:1369–1381
Cahalan MD, Chandy KG (2009) The functional network of ion channels in T lymphocytes. Immunol Rev 231:59–87. https://doi.org/10.1111/j.1600-065X.2009.00816.x
Chandy KG, Decoursey TE, Cahalan MD, McLaughlin C, Gupta S (1984) Voltage-gated potassium channels are required for human T lymphocyte activation. J Exp Med 160:369–385
Chandy KG, Norton RS (2017) Peptide blockers of Kv1.3 channels in T cells as therapeutics for autoimmune disease. Curr Opin Chem Biol 38:97–107. https://doi.org/10.1016/j.cbpa.2017.02.015
Chi V, Pennington MW, Norton RS, Tarcha EJ, Londono LM, Sims-Fahey B, Upadhyay SK, Lakey JT, Iadonato S, Wulff H, Beeton C, Chandy KG (2012) Development of a sea anemone toxin as an immunomodulator for therapy of autoimmune diseases. Toxicon 59:529–546
Chiang EY, Li T, Jeet S, Peng I, Zhang J, Lee WP, DeVoss J, Caplazi P, Chen J, Warming S, Hackos DH, Mukund S, Koth CM, Grogan JL (2017) Potassium channels Kv1.3 and KCa3.1 cooperatively and compensatorily regulate antigen-specific memory T cell functions. Nat Commun 8:14644. https://doi.org/10.1038/ncomms14644
Chighizola CB, Ong VH, Meroni PL (2017) The use of cyclosporine A in rheumatology: a 2016 comprehensive review. Clin Rev Allergy Immunol 52:401–423. https://doi.org/10.1007/s12016-016-8582-3
Cidad P, Miguel-Velado E, Ruiz-McDavitt C, Alonso E, Jimenez-Perez L, Asuaje A, Carmona Y, Garcia-Arribas D, Lopez J, Marroquin Y, Fernandez M, Roque M, Perez-Garcia MT, Lopez-Lopez JR (2015) Kv1.3 channels modulate human vascular smooth muscle cells proliferation independently of mTOR signaling pathway. Pflugers Arch 467:1711–1722. https://doi.org/10.1007/s00424-014-1607-y
Diochot S, Drici MD, Moinier D, Fink M, Lazdunski M (1999) Effects of phrixotoxins on the Kv4 family of potassium channels and implications for the role of Ito1 in cardiac electrogenesis. Br J Pharmacol 126:251–263. https://doi.org/10.1038/sj.bjp.0702283
Fernandez-Ballester G, Fernandez-Carvajal A, Ferrer-Montiel A (2020) Targeting thermo TRP ion channels: in silico preclinical approaches and opportunities. Expert Opin Ther Targets 24:1079–1097. https://doi.org/10.1080/14728222.2020.1820987
Feske S, Prakriya M, Rao A, Lewis RS (2005) A severe defect in CRAC Ca2+ channel activation and altered K+ channel gating in T cells from immunodeficient patients. J Exp Med 202:651–662
Feske S, Skolnik EY, Prakriya M (2012) Ion channels and transporters in lymphocyte function and immunity. Nat Rev Immunol 12:532–547. https://doi.org/10.1038/nri3233
Feske S, Wulff H, Skolnik EY (2015) Ion channels in innate and adaptive immunity. Annu Rev Immunol 33:291–353. https://doi.org/10.1146/annurev-immunol-032414-112212
Gordon D, Chen R, Chung SH (2013) Computational methods of studying the binding of toxins from venomous animals to biological ion channels: theory and applications. Physiol Rev 93:767–802. https://doi.org/10.1152/physrev.00035.2012
Gurrola GB, Hernandez-Lopez RA, Rodriguez de la Vega RC, Varga Z, Batista CV, Salas-Castillo SP, Panyi G, del Rio-Portilla F, Possani LD (2012) Structure, function, and chemical synthesis of Vaejovis mexicanus peptide 24: a novel potent blocker of Kv1.3 potassium channels of human T lymphocytes. Biochemistry 51:4049–4061. https://doi.org/10.1021/bi300060n
Halloran PF (2004) Immunosuppressive drugs for kidney transplantation. N Engl J Med 351:2715–2729. https://doi.org/10.1056/NEJMra033540
Jin L, Pan Y, Pham AC, Boyd BJ, Norton RS, Nicolazzo JA (2020) Prolonged plasma exposure of the Kv1.3-inhibitory peptide HsTX1[R14A] by subcutaneous administration of a poly(lactic-co-glycolic acid) (PLGA) microsphere formulation. J Pharm Sci. https://doi.org/10.1016/j.xphs.2020.10.014
Kaas Q, Craik DJ (2015) Bioinformatics-aided venomics. Toxins (Basel) 7:2159–2187. https://doi.org/10.3390/toxins7062159
Kalman K, Pennington MW, Lanigan MD, Nguyen A, Rauer H, Mahnir V, Paschetto K, Kem WR, Grissmer S, Gutman GA, Christian EP, Cahalan MD, Norton RS, Chandy KG (1998) ShK-Dap22, a potent Kv1.3-specific immunosuppressive polypeptide. J Biol Chem 273:32697–32707
Kim JH, Perfect JR (1989) Infection and cyclosporine. Rev Infect Dis 11:677–690. https://doi.org/10.1093/clinids/11.5.677
Kundu-Raychaudhuri S, Chen YJ, Wulff H, Raychaudhuri SP (2014) Kv1.3 in psoriatic disease: PAP-1, a small molecule inhibitor of Kv1.3 is effective in the SCID mouse psoriasis–xenograft model. J Autoimmun 55:63–72. https://doi.org/10.1016/j.jaut.2014.07.003
Lallana EC, Fadul CE (2011) Toxicities of immunosuppressive treatment of autoimmune neurologic diseases. Curr Neuropharmacol 9:468–477. https://doi.org/10.2174/157015911796557939
Lau C, Hunter MJ, Stewart A, Perozo E, Vandenberg JI (2018) Never at rest: insights into the conformational dynamics of ion channels from cryo-electron microscopy. J Physiol 596:1107–1119. https://doi.org/10.1113/JP274888
Lebrun B, Romi-Lebrun R, Martin-Eauclaire MF, Yasuda A, Ishiguro M, Oyama Y, Pongs O, Nakajima T (1997) A four-disulphide-bridged toxin, with high affinity towards voltage-gated K+ channels, isolated from Heterometrus spinnifer (Scorpionidae) venom. Biochem J 328(Pt 1):321–327
Legany N, Toldi G, Orban C, Megyes N, Bajnok A, Balog A (2016) Calcium influx kinetics, and the features of potassium channels of peripheral lymphocytes in primary Sjogren’s syndrome. Immunobiology 221:1266–1272. https://doi.org/10.1016/j.imbio.2016.06.004
Li M (1997) Use of a modified bacteriophage to probe the interactions between peptides and ion channel receptors in mammalian cells. Nat Biotechnol 15:559–563. https://doi.org/10.1038/nbt0697-559
Lund H, Krakauer M, Skimminge A, Sellebjerg F, Garde E, Siebner HR, Paulson OB, Hesse D, Hanson LG (2013) Blood-brain barrier permeability of normal appearing white matter in relapsing-remitting multiple sclerosis. PLoS ONE 8:e56375. https://doi.org/10.1371/journal.pone.0056375
Mak KK, Pichika MR (2019) Artificial intelligence in drug development: present status and future prospects. Drug Discov Today 24:773–780. https://doi.org/10.1016/j.drudis.2018.11.014
Matteson DR, Deutsch C (1984) K channels in T lymphocytes: a patch clamp study using monoclonal antibody adhesion. Nature 307:468–471
Matthies D, Bae C, Toombes GE, Fox T, Bartesaghi A, Subramaniam S, Swartz KJ (2018) Single-particle cryo-EM structure of a voltage-activated potassium channel in lipid nanodiscs. Elife 7:e37558. https://doi.org/10.7554/eLife.37558
Middleton RE, Warren VA, Kraus RL, Hwang JC, Liu CJ, Dai G, Brochu RM, Kohler MG, Gao YD, Garsky VM, Bogusky MJ, Mehl JT, Cohen CJ, Smith MM (2002) Two tarantula peptides inhibit activation of multiple sodium channels. Biochemistry 41:14734–14747. https://doi.org/10.1021/bi026546a
Mouhat S, Visan V, Ananthakrishnan S, Wulff H, Andreotti N, Grissmer S, Darbon H, De Waard M, Sabatier JM (2005) K+ channel types targeted by synthetic OSK1, a toxin from Orthochirus scrobiculosus scorpion venom. Biochem J 385:95–104
Mullard A (2019) 2018 FDA drug approvals. Nat Rev Drug Discov 18:85–89. https://doi.org/10.1038/d41573-019-00014-x
Nguyen HM, Grossinger EM, Horiuchi M, Davis KW, Jin LW, Maezawa I, Wulff H (2017) Differential Kv1.3, KCa3.1, and Kir2.1 expression in “classically” and “alternatively” activated microglia. Glia 65:106–121. https://doi.org/10.1002/glia.23078
Norton RS, Chandy KG (2017) Venom-derived peptide inhibitors of voltage-gated potassium channels. Neuropharmacology 127:124–138. https://doi.org/10.1016/j.neuropharm.2017.07.002
Oller-Salvia B, Sanchez-Navarro M, Giralt E, Teixido M (2016) Blood-brain barrier shuttle peptides: an emerging paradigm for brain delivery. Chem Soc Rev 45:4690–4707. https://doi.org/10.1039/c6cs00076b
Orlicka K, Barnes E, Culver EL (2013) Prevention of infection caused by immunosuppressive drugs in gastroenterology. Ther Adv Chronic Dis 4:167–185. https://doi.org/10.1177/2040622313485275
Panyi G, Vamosi G, Bodnar A, Gaspar R Jr, Damjanovich S (2004a) Looking through ion channels: recharged concepts in T cell signaling. Trends Immunol 25:565–569
Panyi G, Possani LD, Rodriguez de la Vega RC, Gaspar R, Varga Z (2006) K+ channel blockers: novel tools to inhibit T cell activation leading to specific immunosuppression. Curr Pharm Des 12:2199–2220
Pennington MW, Beeton C, Galea CA, Smith BJ, Chi V, Monaghan KP, Garcia A, Rangaraju S, Giuffrida A, Plank D, Crossley G, Nugent D, Khaytin I, Lefievre Y, Peshenko I, Dixon C, Chauhan S, Orzel A, Inoue T, Hu X, Moore RV, Norton RS, Chandy KG (2009) Engineering a stable and selective peptide blocker of the Kv1.3 channel in T lymphocytes. Mol Pharmacol 75:762–773
Rangaraju S, Gearing M, Jin LW, Levey A (2015) Potassium channel Kv1.3 is highly expressed by microglia in human Alzheimer’s disease. J Alzheimers Dis 44:797–808. https://doi.org/10.3233/JAD-141704
Rashid MH, Huq R, Tanner MR, Chhabra S, Khoo KK, Estrada R, Dhawan V, Chauhan S, Pennington MW, Beeton C, Kuyucak S, Norton RS (2014) A potent and Kv1.3-selective analogue of the scorpion toxin HsTX1 as a potential therapeutic for autoimmune diseases. Sci Rep 4:4509. https://doi.org/10.1038/srep04509
Rodriguez de la Vega RC, Possani LD (2004) Current views on scorpion toxins specific for K+-channels. Toxicon 43:865–875
Sanchez-Navarro M, Teixido M, Giralt E (2017) Jumping hurdles: peptides able to overcome biological barriers. Acc Chem Res 50:1847–1854. https://doi.org/10.1021/acs.accounts.7b00204
Schreiber SL, Crabtree GR (1992) The mechanism of action of cyclosporin A and FK506. Immunol Today 13:136–142. https://doi.org/10.1016/0167-5699(92)90111-J
Serrano-Albarras A, Cirera-Rocosa S, Sastre D, Estadella I, Felipe A (2019) Fighting rheumatoid arthritis: Kv1.3 as a therapeutic target. Biochem Pharmacol 165:214–220. https://doi.org/10.1016/j.bcp.2019.03.016
Smietana K, Siatkowski M, Moller M (2016) Trends in clinical success rates. Nat Rev Drug Discov 15:379–380. https://doi.org/10.1038/nrd.2016.85
Stauderman KA (2018) CRAC channels as targets for drug discovery and development. Cell Calcium 74:147–159. https://doi.org/10.1016/j.ceca.2018.07.005
Tajti G, Wai DCC, Panyi G, Norton RS (2020) The voltage-gated potassium channel KV1.3 as a therapeutic target for venom-derived peptides. Biochem Pharmacol. https://doi.org/10.1016/j.bcp.2020.114146
Takacs Z, Toups M, Kollewe A, Johnson E, Cuello LG, Driessens G, Biancalana M, Koide A, Ponte CG, Perozo E, Gajewski TF, Suarez-Kurtz G, Koide S, Goldstein SA (2009) A designer ligand specific for Kv1.3 channels from a scorpion neurotoxin-based library. Proc Natl Acad Sci USA 106:22211–22216
Tanner MR, Tajhya RB, Huq R, Gehrmann EJ, Rodarte KE, Atik MA, Norton RS, Pennington MW, Beeton C (2017) Prolonged immunomodulation in inflammatory arthritis using the selective Kv1.3 channel blocker HsTX1[R14A] and its PEGylated analog. Clin Immunol 180:45–57. https://doi.org/10.1016/j.clim.2017.03.014
Tarcha EJ, Olsen CM, Probst P, Peckham D, Munoz-Elias EJ, Kruger JG, Iadonato SP (2017) Safety and pharmacodynamics of dalazatide, a Kv1.3 channel inhibitor, in the treatment of plaque psoriasis: a randomized phase 1b trial. PLoS ONE 12:e0180762. https://doi.org/10.1371/journal.pone.0180762
Teisseyre A, Palko-Labuz A, Sroda-Pomianek K, Michalak K (2019) Voltage-gated potassium channel Kv1.3 as a target in therapy of cancer. Front Oncol 9:933. https://doi.org/10.3389/fonc.2019.00933
Tesauro D, Accardo A, Diaferia C, Milano V, Guillon J, Ronga L, Rossi F (2019) Peptide-based drug-delivery systems in biotechnological applications: recent advances and perspectives. Molecules. https://doi.org/10.3390/molecules24020351
Varga Z, Hajdu P, Panyi G (2010) Ion channels in T lymphocytes: an update on facts, mechanisms and therapeutic targeting in autoimmune diseases. Immunol Lett 130:19–25. https://doi.org/10.1016/j.imlet.2009.12.015
Varga Z, Gurrola-Briones G, Papp F, Rodriguez de la Vega RC, Pedraza-Alva G, Tajhya RB, Gaspar R, Cardenas L, Rosenstein Y, Beeton C, Possani LD, Panyi G (2012) Vm24, a natural immunosuppressive peptide, potently and selectively blocks Kv1.3 potassium channels of human T cells. Mol Pharmacol 82:372–382. https://doi.org/10.1124/mol.112.078006
Vennekamp J, Wulff H, Beeton C, Calabresi PA, Grissmer S, Hansel W, Chandy KG (2004) Kv1.3-blocking 5-phenylalkoxypsoralens: a new class of immunomodulators. Mol Pharmacol 65:1364–1374
Wang RE, Wang Y, Zhang Y, Gabrelow C, Zhang Y, Chi V, Fu Q, Luo X, Wang D, Joseph S, Johnson K, Chatterjee AK, Wright TM, Nguyen-Tran VT, Teijaro J, Theofilopoulos AN, Schultz PG, Wang F (2016) Rational design of a Kv1.3 channel-blocking antibody as a selective immunosuppressant. Proc Natl Acad Sci USA 113:11501–11506. https://doi.org/10.1073/pnas.1612803113
Wisedchaisri G, Tonggu L, El-Din TMG, McCord E, Zeng N, Catterall WA (2021) Structural basis for high-affinity trapping of the NaV1.7 channel in its resting state by tarantula toxin. Mol Cell 81:1–11. https://doi.org/10.1016/j.molcel.2020.10.039
Wulff H, Calabresi PA, Allie R, Yun S, Pennington M, Beeton C, Chandy KG (2003) The voltage-gated Kv1.3 K+ channel in effector memory T cells as new target for MS. J Clin Invest 111:1703–1713
Wulff H, Castle NA, Pardo LA (2009) Voltage-gated potassium channels as therapeutic targets. Nat Rev Drug Discov 8:982–1001. https://doi.org/10.1038/nrd2983
Zhao R, Dai H, Mendelman N, Cuello LG, Chill JH, Goldstein SA (2015) Designer and natural peptide toxin blockers of the KcsA potassium channel identified by phage display. Proc Natl Acad Sci USA 112:E7013-7021. https://doi.org/10.1073/pnas.1514728112
Zhao R, Kennedy K, De Blas GA, Orta G, Pavarotti MA, Arias RJ, de la Vega-Beltran JL, Li Q, Dai H, Perozo E, Mayorga LS, Darszon A, Goldstein SAN (2018) Role of human Hv1 channels in sperm capacitation and white blood cell respiratory burst established by a designed peptide inhibitor. Proc Natl Acad Sci USA 115:E11847–E11856. https://doi.org/10.1073/pnas.1816189115
