Antibody-guided photoablation of voltage-gated potassium currents

Journal of General Physiology

Volumn 142, Issue 3, 2013, Pages 315-324

  Sack, Jon T ^a,b,c   Stephanopoulos, Nicholas ^d   Austin, Daniel C ^a   Francis, Matthew B ^d   Trimmer, James S ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Protean Research   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MONOCLONAL ANTIBODY; PORPHYRIN; POTASSIUM CHANNEL BLOCKING AGENT; SHAL POTASSIUM CHANNEL;

ACTION POTENTIAL; ANIMAL; ARTICLE; CHEMISTRY; DRUG ANTAGONISM; DRUG EFFECT; IMMUNOLOGY; LIGHT; MOUSE; RADIATION EXPOSURE;

ACTION POTENTIALS; ANIMALS; ANTIBODIES, MONOCLONAL; LIGHT; MICE; PORPHYRINS; POTASSIUM CHANNEL BLOCKERS; SHAL POTASSIUM CHANNELS;

EID: 84883233942     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201311023     Document Type: Article

References (55)

1. Agostinis, P., K. Berg, K.A. Cengel, T.H. Foster, A.W. Girotti, S.O. Gollnick, S.M. Hahn, M.R. Hamblin, A. Juzeniene, D. Kessel, et al. 2011. Photodynamic therapy of cancer: an update. CA Cancer J. Clin. 61:250-281. http://dx.doi.org/10.3322/caac.20114
2. Alonso, C.M., A. Palumbo, A.J. Bullous, F. Pretto, D. Neri, and R.W. Boyle. 2010. Site-specific and stoichiometric conjugation of cationic porphyrins to antiangiogenic monoclonal antibodies. Bioconjug. Chem. 21:302-313. http://dx.doi.org/10.1021/bc9003537
3. Amarillo, Y., J.A. De Santiago-Castillo, K. Dougherty, J. Maffie, E. Kwon, M. Covarrubias, and B. Rudy. 2008. Ternary Kv4.2 channels recapitulate voltage-dependent inactivation kinetics of A-type K+ channels in cerebellar granule neurons. J. Physiol. 586:2093-2106. http://dx.doi.org/10.1113/jphysiol.2007.150540
4. Antonucci, D.E., S.T. Lim, S. Vassanelli, and J.S. Trimmer. 2001. Dynamic localization and clustering of dendritic Kv2.1 voltagedependent potassium channels in developing hippocampal neurons. Neuroscience. 108:69-81. http://dx.doi.org/10.1016/S0306- 4522(01)00476-6
5. Baumgart, F., A. Rossi, and A.S. Verkman. 2012. Light inactivation of water transport and protein-protein interactions of aquaporin- Killer Red chimeras. J. Gen. Physiol. 139:83-91. http://dx.doi.org/ 10.1085/jgp.201110712
6. Beck, S., T. Sakurai, B.K. Eustace, G. Beste, R. Schier, F. Rudert, and D.G. Jay. 2002. Fluorophore-assisted light inactivation: a highthroughput tool for direct target validation of proteins. Proteomics. 2:247-255. http://dx.doi.org/10.1002/1615-9861(200203)2:3247:: AID-PROT2473.0.CO;2-K
7. Beeton, C., H. Wulff, N.E. Standifer, P. Azam, K.M. Mullen, M.W. Pennington, A. Kolski-Andreaco, E. Wei, A. Grino, D.R. Counts, et al. 2006. Kv1.3 channels are a therapeutic target for T cell-mediated autoimmune diseases. Proc. Natl. Acad. Sci. USA. 103:17414-17419. http://dx.doi.org/10.1073/pnas.0605136103
8. Bonnett, R. 1995. Photosensitizers of the porphyrin and phthalocyanine series for photodynamic therapy. Chem. Soc. Rev. 24:19-33. http://dx.doi.org/10.1039/cs9952400019
9. Burkhalter, A., Y. Gonchar, R.L. Mellor, and J.M. Nerbonne. 2006. Differential expression of I(A) channel subunits Kv4.2 and Kv4.3 in mouse visual cortical neurons and synapses. J. Neurosci. 26:12274- 12282. http://dx.doi.org/10.1523/JNEUROSCI.2599-06.2006
10. Dallas, M.L., S.A. Deuchars, and J. Deuchars. 2010. Immunopharmacology: utilizing antibodies as ion channel modulators. Expert Rev Clin Pharmacol. 3:281-289. http://dx.doi.org/10.1586/ecp.10.18
11. DeCoursey, T.E., K.G. Chandy, S. Gupta, and M.D. Cahalan. 1984. Voltage-gated K+ channels in human T lymphocytes: a role in mitogenesis? Nature. 307:465-468. http://dx.doi.org/10.1038/307465a0
12. Endo, M., M. Fujitsuka, and T. Majima. 2007. Porphyrin lightharvesting arrays constructed in the recombinant tobacco mosaic virus scaffold. Chemistry. 13:8660-8666. http://dx.doi.org/10.1002/ chem.200700895
13. Gardoni, F., D. Mauceri, E. Marcello, C. Sala, M. Di Luca, and A. Jeromin. 2007. SAP97 directs the localization of Kv4.2 to spines in hippocampal neurons: regulation by CaMKII. J. Biol. Chem. 282:28691-28699. http://dx.doi.org/10.1074/jbc.M701899200
14. Gilmore, J.M., R.A. Scheck, A.P. Esser-Kahn, N.S. Joshi, and M.B. Francis. 2006. N-terminal protein modification through a biomimetic transamination reaction. Angew. Chem. Int. Ed. Engl. 45: 5307-5311. http://dx.doi.org/10.1002/anie.200600368
15. Gómez-Varela, D., E. Zwick-Wallasch, H. Knötgen, A. Sánchez, T. Hettmann, D. Ossipov, R. Weseloh, C. Contreras-Jurado, M. Rothe, W. Stühmer, and L.A. Pardo. 2007. Monoclonal antibody blockade of the human Eag1 potassium channel function exerts antitumor activity. Cancer Res. 67:7343-7349. http://dx.doi.org/ 10.1158/0008-5472.CAN-07-0107
16. Grissmer, S., B. Dethlefs, J.J. Wasmuth, A.L. Goldin, G.A. Gutman, M.D. Cahalan, and K.G. Chandy. 1990. Expression and chromosomal localization of a lymphocyte K+ channel gene. Proc. Natl. Acad. Sci. USA. 87:9411-9415. http://dx.doi.org/10.1073/pnas.87.23.9411
17. Guo, W., W.E. Jung, C. Marionneau, F. Aimond, H. Xu, K.A. Yamada, T.L. Schwarz, S. Demolombe, and J.M. Nerbonne. 2005. Targeted deletion of Kv4.2 eliminates I(to,f) and results in electrical and molecular remodeling, with no evidence of ventricular hypertrophy or myocardial dysfunction. Circ. Res. 97:1342-1350. http:// dx.doi.org/10.1161/01.RES.0000196559.63223.aa
18. Guo, J., H. Chen, H.L. Puhl III, and S.R. Ikeda. 2006. Fluorophoreassisted light inactivation produces both targeted and collateral effects on N-type calcium channel modulation in rat sympathetic neurons. J. Physiol. 576:477-492. http://dx.doi.org/10.1113/ jphysiol.2006.113068
19. Gutman, G.A., K.G. Chandy, S. Grissmer, M. Lazdunski, D. McKinnon, L.A. Pardo, G.A. Robertson, B. Rudy, M.C. Sanguinetti, W. Stühmer, and X. Wang. 2005. International Union of Pharmacology. LIII. Nomenclature and molecular relationships of voltage-gated potassium channels. Pharmacol. Rev. 57:473-508. http://dx.doi.org/10 .1124/pr.57.4.10
20. Hammond, R.S., L. Lin, M.S. Sidorov, A.M. Wikenheiser, and D.A. Hoffman. 2008. Protein kinase A mediates activity-dependent Kv4.2 channel trafficking. J. Neurosci. 28:7513-7519. http:// dx.doi.org/10.1523/JNEUROSCI.1951-08.2008
21. Jiang, Y., A. Lee, J. Chen, V. Ruta, M. Cadene, B.T. Chait, and R. MacKinnon. 2003. X-ray structure of a voltage-dependent K+ channel. Nature. 423:33-41. http://dx.doi.org/10.1038/nature01580
22. Kaczorowski, G.J., O.B. McManus, B.T. Priest, and M.L. Garcia. 2008. Ion channels as drug targets: The next GPCRs. J. Gen. Physiol. 131:399-405. http://dx.doi.org/10.1085/jgp.200709946
23. Kim, J., S.C. Jung, A.M. Clemens, R.S. Petralia, and D.A. Hoffman. 2007. Regulation of dendritic excitability by activity-dependent trafficking of the A-type K+ channel subunit Kv4.2 in hippocampal neurons. Neuron. 54:933-947. http://dx.doi.org/10.1016/j .neuron.2007.05.026
24. Lee, J., P. Yu, X. Xiao, and T. Kodadek. 2008. A general system for evaluating the efficiency of chromophore-assisted light inactivation (CALI) of proteins reveals Ru(II) tris-bipyridyl as an unusually efficient "warhead". Mol. Biosyst. 4:59-65. http://dx.doi.org/ 10.1039/b712307h
25. Lim, S.T., D.E. Antonucci, R.H. Scannevin, and J.S. Trimmer. 2000. A novel targeting signal for proximal clustering of the Kv2.1 K+ channel in hippocampal neurons. Neuron. 25:385-397. http:// dx.doi.org/10.1016/S0896-6273(00)80902-2
26. Lin, C.S., R.C. Boltz, J.T. Blake, M. Nguyen, A. Talento, P.A. Fischer, M.S. Springer, N.H. Sigal, R.S. Slaughter, M.L. Garcia, et al. 1993. Voltage-gated potassium channels regulate calcium-dependent pathways involved in human T lymphocyte activation. J. Exp. Med. 177:637-645. http://dx.doi.org/10.1084/jem.177.3.637
27. Menegola, M., and J.S. Trimmer. 2006. Unanticipated region- and cell-specific downregulation of individual KChIP auxiliary subunit isotypes in Kv4.2 knock-out mouse brain. J. Neurosci. 26:12137- 12142. http://dx.doi.org/10.1523/JNEUROSCI.2783-06.2006
28. Middendorf, T.R., and R.W. Aldrich. 2000. Effects of ultraviolet modification on the gating energetics of cyclic nucleotide-gated channels. J. Gen. Physiol. 116:253-282. http://dx.doi.org/10.1085/ jgp.116.2.253
29. Middendorf, T.R., R.W. Aldrich, and D.A. Baylor. 2000. Modification of cyclic nucleotide-gated ion channels by ultraviolet light. J. Gen. Physiol. 116:227-252. http://dx.doi.org/10.1085/jgp.116.2.227
30. Murakoshi, H., and J.S. Trimmer. 1999. Identification of the Kv2.1 K+ channel as a major component of the delayed rectifier K+ current in rat hippocampal neurons. J. Neurosci. 19:1728-1735.
31. Palumbo, A., F. Hauler, P. Dziunycz, K. Schwager, A. Soltermann, F. Pretto, C. Alonso, G.F. Hofbauer, R.W. Boyle, and D. Neri. 2011. A chemically modified antibody mediates complete eradication of tumours by selective disruption of tumour blood vessels. Br. J. Cancer. 104:1106-1115. http://dx.doi.org/10.1038/bjc.2011.78
32. Redmond, R.W., and J.N. Gamlin. 1999. A compilation of singlet oxygen yields from biologically relevant molecules. Photochem. Photobiol. 70:391-475.
33. Rhodes, K.J., and J.S. Trimmer. 2008. Antibody-based validation of CNS ion channel drug targets. J. Gen. Physiol. 131:407-413. http://dx.doi.org/10.1085/jgp.200709926
34. Rhodes, K.J., K.I. Carroll, M.A. Sung, L.C. Doliveira, M.M. Monaghan, S.L. Burke, B.W. Strassle, L. Buchwalder, M. Menegola, J. Cao, et al. 2004. KChIPs and Kv4 alpha subunits as integral components of A-type potassium channels in mammalian brain. J. Neurosci. 24:7903-7915. http://dx.doi.org/10.1523/ JNEUROSCI.0776-04.2004
35. Scheck, R.A., and M.B. Francis. 2007. Regioselective labeling of antibodies through N-terminal transamination. ACS Chem. Biol. 2:247-251. http://dx.doi.org/10.1021/cb6003959
36. Shi, G., A.K. Kleinklaus, N.V. Marrion, and J.S. Trimmer. 1994. Properties of Kv2.1 K+ channels expressed in transfected mammalian cells. J. Biol. Chem. 269:23204-23211.
37. Shibata, R., H. Misonou, C.R. Campomanes, A.E. Anderson, L.A. Schrader, L.C. Doliveira, K.I. Carroll, J.D. Sweatt, K.J. Rhodes, and J.S. Trimmer. 2003. A fundamental role for KChIPs in determining the molecular properties and trafficking of Kv4.2 potassium channels. J. Biol. Chem. 278:36445-36454. http://dx.doi.org/ 10.1074/jbc.M306142200
38. Sjoback, R., J. Nygren, and M. Kubista. 1998. Characterization of fluorescein-oligonucleotide conjugates and measurement of local electrostatic potential. Biopolymers. 46:445-453.
39. Smith, K., N. Malatesti, N. Cauchon, D. Hunting, R. Lecomte, J.E. van Lier, J. Greenman, and R.W. Boyle. 2011. Mono- and tri-cationic porphyrin-monoclonal antibody conjugates: photodynamic activity and mechanism of action. Immunology. 132:256-265. http://dx.doi.org/10.1111/j.1365-2567.2010.03359.x
40. Stephanopoulos, N., Z.M. Carrico, and M.B. Francis. 2009. Nanoscale integration of sensitizing chromophores and porphyrins with bacteriophage MS2. Angew. Chem. Int. Ed. Engl. 48:9498-9502. http://dx.doi.org/10.1002/anie.200902727
41. Stephanopoulos, N., G.J. Tong, S.C. Hsiao, and M.B. Francis. 2010. Dual-surface modified virus capsids for targeted delivery of photodynamic agents to cancer cells. ACS Nano. 4:6014-6020. http:// dx.doi.org/10.1021/nn1014769
42. Tarcha, E.J., V. Chi, E.J. Muñoz-Elías, D. Bailey, L.M. Londono, S.K. Upadhyay, K. Norton, A. Banks, I. Tjong, H. Nguyen, et al. 2012. Durable pharmacological responses from the peptide ShK-186, a specific Kv1.3 channel inhibitor that suppresses T cell mediators of autoimmune disease. J. Pharmacol. Exp. Ther. 342:642-653. http://dx.doi.org/10.1124/jpet.112.191890
43. Tiffany, A.M., L.N. Manganas, E. Kim, Y.P. Hsueh, M. Sheng, and J.S. Trimmer. 2000. PSD-95 and SAP97 exhibit distinct mechanisms for regulating K+ channel surface expression and clustering. J. Cell Biol. 148:147-158. http://dx.doi.org/10.1083/jcb.148.1.147
44. Tomé, J.P., M.G. Neves, A.C. Tomé, J.A. Cavaleiro, M. Soncin, M. Magaraggia, S. Ferro, and G. Jori. 2004. Synthesis and antibacterial activity of new poly-S-lysine-porphyrin conjugates. J. Med. Chem. 47:6649-6652. http://dx.doi.org/10.1021/jm040802v
45. Tour, O., R.M. Meijer, D.A. Zacharias, S.R. Adams, and R.Y. Tsien. 2003. Genetically targeted chromophore-assisted light inactivation. Nat. Biotechnol. 21:1505-1508. http://dx.doi.org/10.1038/nbt914
46. Trapani, J.G., and S.J. Korn. 2003. Control of ion channel expression for patch clamp recordings using an inducible expression system in mammalian cell lines. BMC Neurosci. 4:15. http://dx .doi.org/10.1186/1471-2202-4-15
47. Trimmer, J.S. 1991. Immunological identification and characterization of a delayed rectifier K+ channel polypeptide in rat brain. Proc. Natl. Acad. Sci. USA. 88:10764-10768. http://dx.doi.org/10.1073/ pnas.88.23.10764
48. Trimmer, J.S., I.S. Trowbridge, and V.D. Vacquier. 1985. Monoclonal antibody to a membrane glycoprotein inhibits the acrosome reaction and associated Ca2+ and H+ fluxes of sea urchin sperm. Cell. 40:697-703. http://dx.doi.org/10.1016/0092-8674(85)90218-1
49. Vacher, H., D.P. Mohapatra, and J.S. Trimmer. 2008. Localization and targeting of voltage-dependent ion channels in mammalian central neurons. Physiol. Rev. 88:1407-1447. http://dx.doi.org/ 10.1152/physrev.00002.2008
50. Vegh, R.B., K.M. Solntsev, M.K. Kuimova, S. Cho, Y. Liang, B.L. Loo, L.M. Tolbert, and A.S. Bommarius. 2011. Reactive oxygen species in photochemistry of the red fluorescent protein "Killer Red". Chem. Commun. (Camb.). 47:4887-4889. http://dx.doi.org/10.1039/ c0cc05713d
51. Verlhac, J., A. Gaudemer, and I. Kraljic. 1984. Water-soluble porphyrins and metalloporphyrins as photosensitizers in aerated aqueous solutions. I: Detection and determination of quantum yield of formation of singlet oxygen. Nouveau Journal de Chimie. 8:401-406.
52. Wilkinson, F., W.P. Helman, and A.B. Ross. 1993. Quantum yields for the photosensitized formation of the lowest electronically excited singlet state of molecular oxygen in solution. J. Phys. Chem. Ref. Data. 22:113-263.
53. Xu, S.Z., G. Boulay, R. Flemming, and D.J. Beech. 2006. E3- targeted anti-TRPC5 antibody inhibits store-operated calcium entry in freshly isolated pial arterioles. Am. J. Physiol. Heart Circ. Physiol. 291:H2653-H2659. http://dx.doi.org/10.1152/ajpheart .00495.2006
54. Yang, X.F., Y. Yang, Y.T. Lian, Z.H. Wang, X.W. Li, L.X. Cheng, J.P. Liu, Y.F. Wang, X. Gao, Y.H. Liao, et al. 2012. The antibody targeting the E314 peptide of human Kv1.3 pore region serves as a novel, potent and specific channel blocker. PLoS ONE. 7:e36379. http://dx.doi.org/10.1371/journal.pone.0036379
55. Zhou, B.Y., W. Ma, and X.Y. Huang. 1998. Specific antibodies to the external vestibule of voltage-gated potassium channels block current. J. Gen. Physiol. 111:555-563. http://dx.doi.org/10.1085/ jgp.111.4.55