Intracellular trafficking of the KV1.3 potassium channel is regulated by the prodomain of a matrix metalloprotease

Journal of Biological Chemistry

Volumn 288, Issue 9, 2013, Pages 6451-6464

  Nguyen, Hai M ^a   Galea, Charles A ^b   Schmunk, Galina ^a   Smith, Brian J ^c   Edwards, Robert A ^a   Norton, Raymond S ^b   Chandy, K George ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MONASH UNIVERSITY   (Australia)

^c LA TROBE UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL PROCESS; C TERMINUS; CELL FUNCTIONS; CHANNEL FUNCTIONS; CHANNEL REGULATION; COLORECTAL CANCER; DELETION ANALYSIS; INTRACELLULAR TRAFFICKING; MATRIX METALLOPROTEASE; METALLO-PROTEASE; METALLOPROTEASES; NMR STUDIES; PATCH CLAMPING; POTASSIUM CHANNELS; SECRETORY PATHWAYS; TOPOLOGICAL SIMILARITY; VOLTAGE-GATED POTASSIUM CHANNELS; WHOLE CELL;

CONFOCAL MICROSCOPY; PROTEINS;

POTASSIUM;

MATRIX METALLOPROTEASES 23; MATRIX METALLOPROTEINASE; POTASSIUM CHANNEL; POTASSIUM CHANNEL KCNE1; POTASSIUM CHANNEL KCNE2; POTASSIUM CHANNEL KCNE4; POTASSIUM CHANNEL KV1.3; POTASSIUM CHANNEL KV1.4; POTASSIUM CHANNEL KV3.3; POTASSIUM CHANNEL KV3.4; SOLVENT; UNCLASSIFIED DRUG; METALLOPROTEINASE; MMP23A PROTEIN, HUMAN; POTASSIUM CHANNEL KV1.2; TUMOR PROTEIN;

ALPHA HELIX; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHIMERA; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LOCALIZATION; INTRACELLULAR TRANSPORT; MEMBRANE BINDING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PATCH CLAMP; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REGULATORY MECHANISM; SECRETORY PATHWAY; SURFACE PROPERTY; ANIMAL; CELL STRAIN COS1; CHANNEL GATING; COLORECTAL TUMOR; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

ANIMALS; COLORECTAL NEOPLASMS; COS CELLS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; ION CHANNEL GATING; KV1.2 POTASSIUM CHANNEL; KV1.3 POTASSIUM CHANNEL; METALLOENDOPEPTIDASES; NEOPLASM PROTEINS; PATCH-CLAMP TECHNIQUES; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT;

MLCS; MLOWN;

EID: 84874771897     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.421495     Document Type: Article

References (56)

1. Mannello, F., and Medda, V. (2012) Nuclear localization of matrix metalloproteinases. Prog. Histochem. Cytochem. 47, 27-58
2. Nagase, H., Visse, R., and Murphy, G. (2006) Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc. Res. 69, 562-573
3. Page-McCaw, A., Ewald, A. J., and Werb, Z. (2007) Matrix metalloproteinases and the regulation of tissue remodelling. Nat. Rev. Mol. Cell Biol. 8, 221-233
4. Golubkov, V. S., Chernov, A. V., and Strongin, A. Y. (2011) Intradomain cleavage of inhibitory prodomain is essential to protumorigenic function of membrane type-1 matrix metalloproteinase (MT1-MMP) in vivo. J. Biol. Chem. 286, 34215-34223
5. Jozic, D., Bourenkov, G., Lim, N. H., Visse, R., Nagase, H., Bode, W., and Maskos, K. (2005) X-ray structure of human proMMP-1: new insights into procollagenase activation and collagen binding. J. Biol. Chem. 280, 9578-9585
6. Ohnishi, J., Ohnishi, E., Jin, M., Hirano, W., Nakane, D., Matsui, H., Kimura, A., Sawa, H., Nakayama, K., Shibuya, H., Nagashima, K., and Takahashi, T. (2001) Cloning and characterization of a rat ortholog of MMP-23 (matrix metalloproteinase-23), a unique type of membrane-anchored matrix metalloproteinase and conditioned switching of its expression during the ovarian follicular development. Mol. Endocrinol. 15, 747-764
7. Pei, D., Kang, T., and Qi, H. (2000) Cysteine array matrix metalloproteinase (CA-MMP)/MMP-23 is a type II transmembrane matrix metalloproteinase regulated by a single cleavage for both secretion and activation. J. Biol. Chem. 275, 33988-33997
8. Velasco, G., Pendás, A. M., Fueyo, A., Knäuper, V., Murphy, G., and López-Otín, C. (1999) Cloning and characterization of human MMP-23, a new matrix metalloproteinase predominantly expressed in reproductive tissues and lacking conserved domains in other family members. J. Biol. Chem. 274, 4570-4576
9. Pei, D. (1999) CA-MMP: a matrix metalloproteinase with a novel cysteine array, but without the classic cysteine switch. FEBS Lett. 457, 262-270
10. Rangaraju, S., Khoo, K. K., Feng, Z. P., Crossley, G., Nugent, D., Khaytin, I., Chi, V., Pham, C., Calabresi, P., Pennington, M. W., Norton, R. S., and Chandy, K. G. (2010) Potassium channel modulation by a toxin domain in matrix metalloprotease 23. J. Biol. Chem. 285, 9124-9136
11. Hamill, O. P., Marty, A., Neher, E., Sakmann, B., and Sigworth, F. J. (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 391, 85-100
12. Beeton, C., Smith, B. J., Sabo, J. K., Crossley, G., Nugent, D., Khaytin, I., Chi, V., Chandy, K. G., Pennington, M. W., and Norton, R. S. (2008) The D-diastereomer of ShK toxin selectively blocks voltage-gated K+ channels and inhibits T lymphocyte proliferation. J. Biol. Chem. 283, 988-997
13. Beeton, C., Wulff, H., Singh, S., Botsko, S., Crossley, G., Gutman, G. A., Cahalan, M. D., Pennington, M., and Chandy, K. G. (2003) A novel fluorescent toxin to detect and investigate KV1.3 channel up-regulation in chronically activated T lymphocytes. J. Biol. Chem. 278, 9928-9937
14. Gill, S. C., and von Hippel, P. H. (1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182, 319-326
15. Rovnyak, D., Frueh, D. P., Sastry, M., Sun, Z. Y., Stern, A. S., Hoch, J. C., and Wagner, G. (2004) Accelerated acquisition of high resolution tripleresonance spectra using non-uniform sampling and maximum entropy reconstruction. J. Magn Reson. 170, 15-21
16. Orekhov, V. Y., and Jaravine, V. A. (2011) Analysis of non-uniformly sampled spectra with multi-dimensional decomposition. Prog. Nucl. Magn Reson. Spectrosc. 59, 271-292
17. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR. 6, 277-293
18. Johnson, B. A. (2004) Using NMRView to visualize and analyze the NMR spectra of macromolecules. Methods Mol. Biol. 278, 313-352
19. Bahrami, A., Assadi, A. H., Markley, J. L., and Eghbalnia, H. R. (2009) Probabilistic interaction network of evidence algorithm and its application to complete labeling of peak lists from protein NMR spectroscopy. PLoS. Comput. Biol. 5, e1000307
20. Kay, L. E., Torchia, D. A., and Bax, A. (1989) Backbone dynamics of proteins as studied by 15Ninverse detected heteronuclearNMRspectroscopy: application to staphylococcal nuclease. Biochemistry 28, 8972-8979
21. Lin, D., Sze, K. H., Cui, Y., and Zhu, G. (2002) Clean SEA-HSQC: a method to map solvent exposed amides in large non-deuterated proteins with gradient-enhanced HSQC. J. Biomol. NMR 23, 317-322
22. Pintacuda, G., and Otting, G. (2002) Identification of protein surfaces by NMRmeasurements with a pramagnetic Gd(III) chelate. J. Am. Chem. Soc. 124, 372-373
23. Hess, B., Kutzner, C., van der Spoel, D., and Lindahl, E. (2008) GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Chem. Theory Comput. 4, 435-447
24. Monticelli, L., Kandasamy, S. K., Periole, X., Larson, R. G., Tieleman, D. P., and Marrink, S.-J. (2008) The MARTINI coarse-grained force field: extension to proteins. J. Chem. Theory Comput. 4, 819-834
25. Marrink, S. J., Risselada, H. J., Yefimov, S., Tieleman, D. P., and de Vries, A. H. (2007) The MARTINI force field: coarse grained model for biomolecular simulations. J. Phys. Chem. B. 111, 7812-7824
26. Bussi, G., Donadio, D., and Parrinello, M. (2007) Canonical sampling through velocity rescaling. J. Chem. Phys. 126, 014101
27. Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., and Haak, J. R. (1984) Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81, 3684-3690
28. Fiser, A., and Sali, A. (2003) Modeller: generation and refinement of homology- based protein structure models. Methods Enzymol. 374, 461-491
29. Grissmer, S., Nguyen, A. N., Aiyar, J., Hanson, D. C., Mather, R. J., Gutman, G. A., Karmilowicz, M. J., Auperin, D. D., and Chandy, K. G. (1994) Pharmacological characterization of five cloned voltage-gated K+ channels, types KV1.1, 1.2, 1.3, 1.5, and 3.1, stably expressed in mammalian cell lines. Mol. Pharmacol. 45, 1227-1234
30. Grunnet, M., Rasmussen, H. B., Hay-Schmidt, A., and Klaerke, D. A. (2003) The voltage-gated potassium channel subunit, KV1.3, is expressed in epithelia. Biochim. Biophys. Acta 1616, 85-94
31. Abdul, M., and Hoosein, N. (2002) Voltage-gated potassium ion channels in colon cancer. Oncol. Rep. 9, 961-964
32. Baeza-Delgado, C., Marti-Renom, M. A., and Mingarro, I. (April 14, 2012) Structure-based statistical analysis of transmembrane helices. Eur. Biophys. J. 10.1007/s00249-012-0813-9
33. Shen, Y., Delaglio, F., Cornilescu, G., and Bax, A. (2009) TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J. Biomol. NMR 44, 213-223
34. Shen, Y., and Bax, A. (2012) Identification of helix capping and β-turn motifs from NMR chemical shifts. J. Biomol. NMR 52, 211-232
35. Beswick, V., Roux, M., Navarre, C., Coïc, Y. M., Huynh-Dinh, T., Goffeau, A., Sanson, A., and Neumann, J. M. (1998) 1H- and 2H-NMR studies of a fragment of PMP1, a regulatory subunit associated with the yeast plasma membrane H+-ATPase. Conformational properties and lipid-peptide interactions. Biochimie 80, 451-459
36. Sharpe, H. J., Stevens, T. J., and Munro, S. (2010) A comprehensive comparison of transmembrane domains reveals organelle-specific properties. Cell 142, 158-169
37. Langelaan, D. N., Wieczorek, M., Blouin, C., and Rainey, J. K. (2010) Improved helix and kink characterization in membrane proteins allows evaluation of kink sequence predictors. J. Chem. Inf. Model. 50, 2213-2220
38. Cordes, F. S., Bright, J. N., and Sansom, M. S. (2002) Proline-induced distortions of transmembrane helices. J. Mol. Biol. 323, 951-960
39. Klammt, C., Maslennikov, I., Bayrhuber, M., Eichmann, C., Vajpai, N., Chiu, E. J., Blain, K. Y., Esquivies, L., Kwon, J. H., Balana, B., Pieper, U., Sali, A., Slesinger, P. A., Kwiatkowski, W., Riek, R., and Choe, S. (2012) Facile backbone structure determination of human membrane proteins byNMR spectroscopy. Nat. Methods 9, 834-839
40. Van Horn, W. D., Vanoye, C. G., and Sanders, C. R. (2011) Working model for the structural basis for KCNE1 modulation of the KCNQ1 potassium channel. Curr. Opin. Struct. Biol. 21, 283-291
41. Barrett, P. J., Song, Y., Van Horn, W. D., Hustedt, E. J., Schafer, J. M., Hadziselimovic, A., Beel, A. J., and Sanders, C. R. (2012) The amyloid precursor protein has a flexible transmembrane domain and binds cholesterol. Science 336, 1168-1171
42. Kanda, V. A., Lewis, A., Xu, X., and Abbott, G. W. (2011) KCNE1 and KCNE2 provide a checkpoint governing voltage-gated potassium channel α-subunit composition. Biophys. J. 101, 1364-1375
43. Kanda, V. A., Lewis, A., Xu, X., and Abbott, G. W. (2011) KCNE1 and KCNE2 inhibit forward trafficking of homomeric N-type voltage-gated potassium channels. Biophys. J. 101, 1354-1363
44. Kanda, V. A., and Abbott, G. W. (2012) KCNE Regulation of K+ channel trafficking - a Sisyphean task? Front Physiol. 3, 231
45. Solé, L., Roura-Ferrer, M., Pérez-Verdaguer, M., Oliveras, A., Calvo, M., Fernández-Fernández, J. M., and Felipe, A. (2009) KCNE4 suppresses KV1.3 currents by modulating trafficking, surface expression and channel gating. J. Cell Sci. 122, 3738-3748
46. Tapper, A. R., and George, A. L., Jr. (2000) MinK subdomains that mediate modulation of and association with KVLQT1. J. Gen. Physiol. 116, 379-390
47. Krogsgaard, M., Ma, M. W., Friedman, E. B., Vega-Saenz de Miera, E., Darvishian, F., Perez-Garcia, A., Berman, R. S., Shapiro, R. L., Christos, P. J., Osman, I., and Pavlick, A. C. (2011) An analysis of altered melanoma matrix metalloproteinase-23 (MMP-23) expression and response to immune biologic therapy. J. Clin. Oncol. 29, (suppl.) (Abstr. 8541)
48. Clancy, B. M., Johnson, J. D., Lambert, A. J., Rezvankhah, S., Wong, A., Resmini, C., Feldman, J. L., Leppanen, S., and Pittman, D. D. (2003) A gene expression profile for endochondral bone formation: oligonucleotide microarrays establish novel connections between known genes and BMP-2- induced bone formation in mouse quadriceps. Bone 33, 46-63
49. Fortunato, S. J., and Menon, R. (2002) Screening of novel matrix metalloproteinases (MMPs) in human fetal membranes. J. Assist. Reprod. Genet. 19, 483-486
50. Jones, G. C., Corps, A. N., Pennington, C. J., Clark, I. M., Edwards, D. R., Bradley, M. M., Hazleman, B. L., and Riley, G. P. (2006) Expression profiling of metalloproteinases and tissue inhibitors of metalloproteinases in normal and degenerate human achilles tendon. Arthritis Rheum. 54, 832-842
51. Okada, A., and Okada, Y. (2009) Progress of research in osteoarthritis. Metalloproteinases in osteoarthritis. Clin. Calcium 19, 1593-1601
52. Riddick, A. C., Shukla, C. J., Pennington, C. J., Bass, R., Nuttall, R. K., Hogan, A., Sethia, K. K., Ellis, V., Collins, A. T., Maitland, N. J., Ball, R. Y., and Edwards, D. R. (2005) Identification of degradome components associated with prostate cancer progression by expression analysis of human prostatic tissues. Br. J. Cancer 92, 2171-2180
53. Hegedüs, L., Cho, H., Xie, X., and Eliceiri, G. L. (2008) Additional MDAMB- 231 breast cancer cell matrix metalloproteinases promote invasiveness. J. Cell. Physiol. 216, 480-485
54. Scrideli, C. A., Carlotti, C. G., Jr., Okamoto, O. K., Andrade, V. S., Cortez, M. A., Motta, F. J., Lucio-Eterovic, A. K., Neder, L., Rosemberg, S., Oba- Shinjo, S. M., Marie, S. K., and Tone, L. G. (2008) Gene expression profile analysis of primary glioblastomas and non-neoplastic brain tissue: identification of potential target genes by oligonucleotide microarray and realtime quantitative PCR. J. Neurooncol. 88, 281-291
55. Davidson, R. K., Waters, J. G., Kevorkian, L., Darrah, C., Cooper, A., Donell, S. T., and Clark, I. M. (2006) Expression profiling of metalloproteinases and their inhibitors in synovium and cartilage. Arthritis Res. Ther. 8, R124
56. Wishart, D. S., Bigam, C. G., Holm, A., Hodges, R. S., and Sykes, B. D. (1995) 1H, 13C, and 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of nearest-neighbor effects. J. Biomol. NMR. 5, 67-81