Domain structure and function of matrix metalloprotease 23 (MMP23): role in potassium channel trafficking

Cellular and Molecular Life Sciences

Volumn 71, Issue 7, 2014, Pages 1191-1210

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

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c LA TROBE UNIVERSITY   (Australia)

Author keywords

Kv1.3; Matrix metalloprotease; MMP23 Pro domain; Potassium channel; Toxin domain; Trans membrane domain

Indexed keywords

CELL ADHESION MOLECULE; MATRIX METALLOPROTEINASE; POTASSIUM CHANNEL KV1.1; PROTEIN IMMUNOGLOBULIN LIKE CELL ADHESION MOLECULE; PROTEIN MATRIX METALLOPROTEINASE 23; PROTEIN TOXIN LIKE DOMAIN; UNCLASSIFIED DRUG; POTASSIUM; POTASSIUM CHANNEL;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; CELL MIGRATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME MECHANISM; ENZYME REGULATION; HUMAN; NONHUMAN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REVIEW; AMINO ACID SEQUENCE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; CATALYTIC DOMAIN; HUMANS; MATRIX METALLOPROTEINASES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; POTASSIUM; POTASSIUM CHANNELS; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT;

EID: 84902107047     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-013-1431-0     Document Type: Review

References (175)

1. Butler GS, Overall CM (2009) Updated biological roles for matrix metalloproteinases and new “intracellular” substrates revealed by degradomics. Biochemistry 48:10830–10845
2. Morrison CJ, Butler GS, Rodriguez D, Overall CM (2009) Matrix metalloproteinase proteomics: substrates, targets, and therapy. Curr Opin Cell Biol 21:645–653
3. Rodriguez D, Morrison CJ, Overall CM (2010) Matrix metalloproteinases: what do they not do? New substrates and biological roles identified by murine models and proteomics. Biochim Biophys Acta 1803:39–54
4. Gururajan R, Grenet J, Lahti JM, Kidd VJ (1998) Isolation and characterization of two novel metalloproteinase genes linked to the Cdc2L locus on human chromosome 1p36.3. Genomics 52:101–106
5. Gill SE, Parks WC (2008) Metalloproteinases and their inhibitors: regulators of wound healing. Int J Biochem Cell Biol 40:1334–1347
6. Mott JD, Werb Z (2004) Regulation of matrix biology by matrix metalloproteinases. Curr Opin Cell Biol 16:558–564
7. Nagase H, Visse R, Murphy G (2006) Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res 69:562–573
8. Page-McCaw A, Ewald AJ, Werb Z (2007) Matrix metalloproteinases and the regulation of tissue remodeling. Nat Rev Mol Cell Biol 8:221–233
9. Sternlicht MD, Werb Z (2001) How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 17:463–516
10. Vu TH, Werb Z (2000) Matrix metalloproteinases: effectors of development and normal physiology. Genes Dev 14:2123–2133
11. Hadler-Olsen E, Fadnes B, Sylte I, Uhlin-Hansen L, Winberg JO (2011) Regulation of matrix metalloproteinase activity in health and disease. FEBS J 278:28–45
12. Sbardella D, Fasciglione GF, Gioia M, Ciaccio C, Tundo GR, Marini S, Coletta M (2012) Human matrix metalloproteinases: an ubiquitarian class of enzymes involved in several pathological processes. Mol Aspects Med 33:119–208
13. Piperi C, Papavassiliou AG (2012) Molecular mechanisms regulating matrix metalloproteinases. Curr Top Med Chem 12:1095–1112
14. Mannello F, Medda V (2012) Nuclear localization of matrix metalloproteinases. Prog Histochem Cytochem 47:27–58
15. Murphy G, Nagase H (2011) Localizing matrix metalloproteinase activities in the pericellular environment. FEBS J 278:2–15
16. Bourboulia D, Stetler-Stevenson WG (2010) Matrix metalloproteinases (MMPs) and tissue inhibitors of metalloproteinases (TIMPs): positive and negative regulators in tumor cell adhesion. Semin Cancer Biol 20:161–168
17. Brew K, Nagase H (2010) The tissue inhibitors of metalloproteinases (TIMPs): an ancient family with structural and functional diversity. Biochim Biophys Acta 1803:55–71
18. Fu X, Parks WC, Heinecke JW (2008) Activation and silencing of matrix metalloproteinases. Semin Cell Dev Biol 19:2–13
19. Murphy G (2011) Tissue inhibitors of metalloproteinases. Genome Biol 12:233
20. Gustafsson T (2011) Vascular remodeling in human skeletal muscle. Biochem Soc Trans 39:1628–1632
21. Kraiem Z, Korem S (2000) Matrix metalloproteinases and the thyroid. Thyroid 10:1061–1069
22. Ortega N, Behonick D, Stickens D, Werb Z (2003) How proteases regulate bone morphogenesis. Ann NY Acad Sci 995:109–116
23. Parks WC, Shapiro SD (2001) Matrix metalloproteinases in lung biology. Respir Res 2:10–19
24. Clutterbuck AL, Asplin KE, Harris P, Allaway D, Mobasheri A (2009) Targeting matrix metalloproteinases in inflammatory conditions. Curr Drug Targets 10:1245–1254
25. Decock J, Thirkettle S, Wagstaff L, Edwards DR (2011) Matrix metalloproteinases: protective roles in cancer. J Cell Mol Med 15:1254–1265
26. Gialeli C, Theocharis AD, Karamanos NK (2011) Roles of matrix metalloproteinases in cancer progression and their pharmacological targeting. FEBS J 278:16–27
27. Hua H, Li M, Luo T, Yin Y, Jiang Y (2011) Matrix metalloproteinases in tumorigenesis: an evolving paradigm. Cell Mol Life Sci 68:3853–3868
28. Korpos E, Wu C, Sorokin L (2009) Multiple roles of the extracellular matrix in inflammation. Curr Pharm Des 15:1349–1357
29. Rucci N, Sanita P, Angelucci A (2011) Roles of metalloproteases in metastatic niche. Curr Mol Med 11:609–622
30. Siasos G, Tousoulis D, Kioufis S, Oikonomou E, Siasou Z, Limperi M, Papavassiliou AG, Stefanadis C (2012) Inflammatory mechanisms in atherosclerosis: the impact of matrix metalloproteinases. Curr Top Med Chem 12:1132–1148
31. Stellas D, Patsavoudi E (2012) Inhibiting matrix metalloproteinases, an old story with new potentials for cancer treatment. Anticancer Agents Med Chem 12:707–717
32. Aldonyte R, Brantly M, Block E, Patel J, Zhang J (2009) Nuclear localization of active matrix metalloproteinase-2 in cigarette smoke-exposed apoptotic endothelial cells. Exp Lung Res 35:59–75
33. Eguchi T, Kubota S, Kawata K, Mukudai Y, Uehara J, Ohgawara T, Ibaragi S, Sasaki A, Kuboki T, Takigawa M (2008) Novel transcription-factor-like function of human matrix metalloproteinase 3 regulating the CTGF/CCN2 gene. Mol Cell Biol 28:2391–2413
34. Ip YC, Cheung ST, Fan ST (2007) Atypical localization of membrane type 1-matrix metalloproteinase in the nucleus is associated with aggressive features of hepatocellular carcinoma. Mol Carcinog 46:225–230
35. Kwan JA, Schulze CJ, Wang W, Leon H, Sariahmetoglu M, Sung M, Sawicka J, Sims DE, Sawicki G, Schulz R (2004) Matrix metalloproteinase-2 (MMP-2) is present in the nucleus of cardiac myocytes and is capable of cleaving poly (ADP-ribose) polymerase (PARP) in vitro. FASEB J 18:690–692
36. Limb GA, Matter K, Murphy G, Cambrey AD, Bishop PN, Morris GE, Khaw PT (2005) Matrix metalloproteinase-1 associates with intracellular organelles and confers resistance to lamin A/C degradation during apoptosis. Am J Pathol 166:1555–1563
37. Marchenko ND, Marchenko GN, Weinreb RN, Lindsey JD, Kyshtoobayeva A, Crawford HC, Strongin AY (2004) Beta-catenin regulates the gene of MMP-26, a novel metalloproteinase expressed both in carcinomas and normal epithelial cells. Int J Biochem Cell Biol 36:942–956
38. Nguyen HM, Galea CA, Schmunk G, Smith BJ, Edwards RA, Norton RS, Chandy KG (2013) Intracellular trafficking of the Kv1.3 potassium channel is regulated by the prodomain of a matrix metalloprotease. J Biol Chem 288:6451–6464
39. Rangaraju S, Khoo KK, Feng ZP, Crossley G, Nugent D, Khaytin I, Chi V, Pham C, Calabresi P, Pennington MW, Norton RS, Chandy KG (2010) Potassium channel modulation by a toxin domain in matrix metalloprotease 23. J Biol Chem 285:9124–9136
40. Si-Tayeb K, Monvoisin A, Mazzocco C, Lepreux S, Decossas M, Cubel G, Taras D, Blanc JF, Robinson DR, Rosenbaum J (2006) Matrix metalloproteinase 3 is present in the cell nucleus and is involved in apoptosis. Am J Pathol 169:1390–1401
41. Wang W, Schulze CJ, Suarez-Pinzon WL, Dyck JR, Sawicki G, Schulz R (2002) Intracellular action of matrix metalloproteinase-2 accounts for acute myocardial ischemia and reperfusion injury. Circulation 106:1543–1549
42. Yang Y, Candelario-Jalil E, Thompson JF, Cuadrado E, Estrada EY, Rosell A, Montaner J, Rosenberg GA (2010) Increased intranuclear matrix metalloproteinase activity in neurons interferes with oxidative DNA repair in focal cerebral ischemia. J Neurochem 112:134–149
43. Zhao YG, Xiao AZ, Newcomer RG, Park HI, Kang T, Chung LW, Swanson MG, Zhau HE, Kurhanewicz J, Sang QX (2003) Activation of pro-gelatinase B by endometase/matrilysin-2 promotes invasion of human prostate cancer cells. J Biol Chem 278:15056–15064
44. Bode W, Maskos K (2011) Matrix metalloproteinases. In: Encyclopedia of inorganic and bioinorganic chemistry. Wiley, New York. doi:10.1002/9781119951438.eibc0495
45. Klein T, Bischoff R (2011) Physiology and pathophysiology of matrix metalloproteases. Amino Acids 41:271–290
46. Zitka O, Kukacka J, Krizkova S, Huska D, Adam V, Masarik M, Prusa R, Kizek R (2010) Matrix metalloproteinases. Curr Med Chem 17:3751–3768
47. Huxley-Jones J, Clarke TK, Beck C, Toubaris G, Robertson DL, Boot-Handford RP (2007) The evolution of the vertebrate metzincins; insights from Ciona intestinalis and Danio rerio. BMC Evol Biol 7:63
48. Fanjul-Fernandez M, Folgueras AR, Cabrera S, Lopez-Otin C (2010) Matrix metalloproteinases: evolution, gene regulation and functional analysis in mouse models. Biochim Biophys Acta 1803:3–19
49. Van Wart HE, Birkedal-Hansen H (1990) The cysteine switch: a principle of regulation of metalloproteinase activity with potential applicability to the entire matrix metalloproteinase gene family. Proc Natl Acad Sci USA 87:5578–5582
50. Ra HJ, Parks WC (2007) Control of matrix metalloproteinase catalytic activity. Matrix Biol 26:587–596
51. Ohnishi J, Ohnishi E, Jin M, Hirano W, Nakane D, Matsui H, Kimura A, Sawa H, Nakayama K, Shibuya H, Nagashima K, 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
52. Pei D (1999) CA-MMP: a matrix metalloproteinase with a novel cysteine array, but without the classic cysteine switch. FEBS Lett 457:262–270
53. Pei D, Kang T, 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
54. Velasco G, Pendas AM, Fueyo A, Knauper V, Murphy G, Lopez-Otin 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
55. Sounni NE, Noel A (2005) Membrane type-matrix metalloproteinases and tumor progression. Biochimie 87:329–342
56. Zucker S, Pei D, Cao J, Lopez-Otin C (2003) Membrane type-matrix metalloproteinases (MT-MMP). Curr Top Dev Biol 54:1–74
57. Koziol A, Martin-Alonso M, Clemente C, Gonzalo P, Arroyo AG (2012) Site-specific cellular functions of MT1-MMP. Eur J Cell Biol 91:889–895
58. Labrecque L, Nyalendo C, Langlois S, Durocher Y, Roghi C, Murphy G, Gingras D, Beliveau R (2004) Src-mediated tyrosine phosphorylation of caveolin-1 induces its association with membrane type 1 matrix metalloproteinase. J Biol Chem 279:52132–52140
59. Artym VV, Zhang Y, Seillier-Moiseiwitsch F, Yamada KM, Mueller SC (2006) Dynamic interactions of cortactin and membrane type 1 matrix metalloproteinase at invadopodia: defining the stages of invadopodia formation and function. Cancer Res 66:3034–3043
60. Cauwe B, Van den Steen PE, Opdenakker G (2007) The biochemical, biological, and pathological kaleidoscope of cell surface substrates processed by matrix metalloproteinases. Crit Rev Biochem Mol Biol 42:113–185
61. Gingras D, Michaud M, Di Tomasso G, Beliveau E, Nyalendo C, Beliveau R (2008) Sphingosine-1-phosphate induces the association of membrane-type 1 matrix metalloproteinase with p130Cas in endothelial cells. FEBS Lett 582:399–404
62. Gonzalo P, Guadamillas MC, Hernandez-Riquer MV, Pollan A, Grande-Garcia A, Bartolome RA, Vasanji A, Ambrogio C, Chiarle R, Teixido J, Risteli J, Apte SS, del Pozo MA, Arroyo AG (2010) MT1-MMP is required for myeloid cell fusion via regulation of Rac1 signaling. Dev Cell 18:77–89
63. Roghi C, Jones L, Gratian M, English WR, Murphy G (2010) Golgi reassembly stacking protein 55 interacts with membrane-type (MT) 1-matrix metalloprotease (MMP) and furin and plays a role in the activation of the MT1-MMP zymogen. FEBS J 277:3158–3175
64. Sakamoto T, Seiki M (2010) A membrane protease regulates energy production in macrophages by activating hypoxia-inducible factor-1 via a non-proteolytic mechanism. J Biol Chem 285:29951–29964
65. Smith-Pearson PS, Greuber EK, Yogalingam G, Pendergast AM (2010) Abl kinases are required for invadopodia formation and chemokine-induced invasion. J Biol Chem 285:40201–40211
66. Tapia T, Ottman R, Chakrabarti R (2011) LIM kinase1 modulates function of membrane type matrix metalloproteinase 1: implication in invasion of prostate cancer cells. Mol Cancer 10:6
67. Knauper V, Kramer S, Reinke H, Tschesche H (1990) Characterization and activation of procollagenase from human polymorphonuclear leucocytes. N-terminal sequence determination of the proenzyme and various proteolytically activated forms. Eur J Biochem 189:295–300
68. Nagase H, Suzuki K, Enghild JJ, Salvesen G (1991) Stepwise activation mechanisms of the precursors of matrix metalloproteinases 1 (tissue collagenase) and 3 (stromelysin). Biomed Biochim Acta 50:749–754
69. Nagase H, Suzuki K, Morodomi T, Enghild JJ, Salvesen G (1992) Activation mechanisms of the precursors of matrix metalloproteinases 1, 2 and 3. Matrix Suppl 1:237–244
70. Springman EB, Angleton EL, Birkedal-Hansen H, Van Wart HE (1990) Multiple modes of activation of latent human fibroblast collagenase: evidence for the role of a Cys73 active-site zinc complex in latency and a “cysteine switch” mechanism for activation. Proc Natl Acad Sci USA 87:364–368
71. Li SS (2005) Specificity and versatility of SH3 and other proline-recognition domains: structural basis and implications for cellular signal transduction. Biochem J 390:641–653
72. Saksela K, Permi P (2012) SH3 domain ligand binding: what’s the consensus and where’s the specificity? FEBS Lett 586:2609–2614
73. Gomis-Ruth FX, Trillo-Muyo S, Stocker W (2012) Functional and structural insights into astacin metallopeptidases. Biol Chem 393:1027–1041
74. Mohrlen F, Hutter H, Zwilling R (2003) The astacin protein family in Caenorhabditis elegans. Eur J Biochem 270:4909–4920
75. Rachamim T, Sher D (2012) What Hydra can teach us about chemical ecology—how a simple, soft organism survives in a hostile aqueous environment. Int J Dev Biol 56:605–611
76. Guevara T, Yiallouros I, Kappelhoff R, Bissdorf S, Stocker W, Gomis-Ruth FX (2010) Proenzyme structure and activation of astacin metallopeptidase. J Biol Chem 285:13958–13965
77. Maskos K (2005) Crystal structures of MMPs in complex with physiological and pharmacological inhibitors. Biochimie 87:249–263
78. Tallant C, Marrero A, Gomis-Ruth FX (2010) Matrix metalloproteinases: fold and function of their catalytic domains. Biochim Biophys Acta 1803:20–28
79. Andreini C, Banci L, Bertini I, Luchinat C, Rosato A (2004) Bioinformatic comparison of structures and homology-models of matrix metalloproteinases. J Proteome Res 3:21–31
80. Bode W, Gomis-Rüth F-X, Stöckler W (1993) Astacins, serralysins, snake venom and matrix metalloproteinases exhibit identical zinc-binding environments (HEXXHXXGXXH and Met-turn) and topologies and should be grouped into a common family, the ‘metzincins’. FEBS Lett 331:134–140
81. Stocker W, Grams F, Baumann U, Reinemer P, Gomis-Ruth FX, McKay DB, Bode W (1995) The metzincins–topological and sequential relations between the astacins, adamalysins, serralysins, and matrixins (collagenases) define a superfamily of zinc-peptidases. Protein Sci 4:823–840
82. Steffensen B, Wallon UM, Overall CM (1995) Extracellular matrix binding properties of recombinant fibronectin type II-like modules of human 72-kDa gelatinase/type IV collagenase. High affinity binding to native type I collagen but not native type IV collagen. J Biol Chem 270:11555–11566
83. Lambert E, Dasse E, Haye B, Petitfrere E (2004) TIMPs as multifacial proteins. Crit Rev Oncol Hematol 49:187–198
84. Marrero A, Duquerroy S, Trapani S, Goulas T, Guevara T, Andersen GR, Navaza J, Sottrup-Jensen L, Gomis-Ruth FX (2012) The crystal structure of human α2-macroglobulin reveals a unique molecular cage. Angew Chem Int Ed Engl 51:3340–3344
85. Sottrup-Jensen L (1989) α-macroglobulins: structure, shape, and mechanism of proteinase complex formation. J Biol Chem 264:11539–11542
86. Strickland DK, Ashcom JD, Williams S, Burgess WH, Migliorini M, Argraves WS (1990) Sequence identity between the alpha 2-macroglobulin receptor and low density lipoprotein receptor-related protein suggests that this molecule is a multifunctional receptor. J Biol Chem 265:17401–17404
87. Willenbrock F, Thomas DA, Amour A (2010) Kinetic analysis of the inhibition of matrix metalloproteinases: lessons from the study of tissue inhibitors of metalloproteinases. Methods Mol Biol 622:435–450
88. Murphy G, Knauper V (1997) Relating matrix metalloproteinase structure to function: why the “hemopexin” domain? Matrix Biol 15:511–518
89. Bode W (1995) A helping hand for collagenases: the haemopexin-like domain. Structure 3:527–530
90. Clark IM, Cawston TE (1989) Fragments of human fibroblast collagenase. Purification and characterization. Biochem J 263:201–206
91. Overall CM (2002) Molecular determinants of metalloproteinase substrate specificity: matrix metalloproteinase substrate binding domains, modules, and exosites. Mol Biotechnol 22:51–86
92. Chung L, Dinakarpandian D, Yoshida N, Lauer-Fields JL, Fields GB, Visse R, Nagase H (2004) Collagenase unwinds triple-helical collagen prior to peptide bond hydrolysis. EMBO J 23:3020–3030
93. Cavallaro U, Christofori G (2004) Cell adhesion and signalling by cadherins and Ig-CAMs in cancer. Nat Rev Cancer 4:118–132
94. Hohenester E (2008) Structural insight into Slit-Robo signalling. Biochem Soc Trans 36:251–256
95. Morlot C, Thielens NM, Ravelli RB, Hemrika W, Romijn RA, Gros P, Cusack S, McCarthy AA (2007) Structural insights into the Slit-Robo complex. Proc Natl Acad Sci USA 104:14923–14928
96. Rasmussen KK, Kulahin N, Kristensen O, Poulsen JC, Sigurskjold BW, Kastrup JS, Berezin V, Bock E, Walmod PS, Gajhede M (2008) Crystal structure of the Ig1 domain of the neural cell adhesion molecule NCAM2 displays domain swapping. J Mol Biol 382:1113–1120
97. Sanchez-Arrones L, Cardozo M, Nieto-Lopez F, Bovolenta P (2012) Cdon and Boc: two transmembrane proteins implicated in cell-cell communication. Int J Biochem Cell Biol 44:698–702
98. Law RH, Lukoyanova N, Voskoboinik I, Caradoc-Davies TT, Baran K, Dunstone MA, D’Angelo ME, Orlova EV, Coulibaly F, Verschoor S, Browne KA, Ciccone A, Kuiper MJ, Bird PI, Trapani JA, Saibil HR, Whisstock JC (2010) The structural basis for membrane binding and pore formation by lymphocyte perforin. Nature 468:447–451
99. Lopez JA, Brennan AJ, Whisstock JC, Voskoboinik I, Trapani JA (2012) Protecting a serial killer: pathways for perforin trafficking and self-defence ensure sequential target cell death. Trends Immunol 33:406–412
100. Voskoboinik I, Dunstone MA, Baran K, Whisstock JC, Trapani JA (2010) Perforin: structure, function, and role in human immunopathology. Immunol Rev 235:35–54
101. Faraco J, Bashir M, Rosenbloom J, Francke U (1995) Characterization of the human gene for microfibril-associated glycoprotein (MFAP2), assignment to chromosome 1p36.1-p35, and linkage to D1S170. Genomics 25:630–637
102. Tsang SW, Nguyen CQ, Hall DH, Chow KL (2007) mab-7 encodes a novel transmembrane protein that orchestrates sensory ray morphogenesis in C. elegans. Dev Biol 312:353–366
103. Pan T, Groger H, Schmid V, Spring J (1998) A toxin homology domain in an astacin-like metalloproteinase of the jellyfish Podocoryne carnea with a dual role in digestion and development. Dev Genes Evol 208:259–266
104. Yan L, Fei K, Zhang J, Dexter S, Sarras MP Jr (2000) Identification and characterization of Hydra metalloproteinase 2 (HMP2): a meprin-like astacin metalloproteinase that functions in foot morphogenesis. Development 127:129–141
105. Cotton J, Crest M, Bouet F, Alessandri N, Gola M, Forest E, Karlsson E, Castaneda O, Harvey AL, Vita C, Menez A (1997) A potassium-channel toxin from the sea anemone Bunodosoma granulifera, an inhibitor for Kv1 channels. Revision of the amino acid sequence, disulfide-bridge assignment, chemical synthesis, and biological activity. Eur J Biochem 244:192–202
106. Norton RS (2009) Structures of sea anemone toxins. Toxicon 54:1075–1088
107. Tudor JE, Pallaghy PK, Pennington MW, Norton RS (1996) Solution structure of ShK toxin, a novel potassium channel inhibitor from a sea anemone. Nat Struct Biol 3:317–320
108. 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
109. Tudor JE, Pennington MW, Norton RS (1998) Ionisation behaviour and solution properties of the potassium-channel blocker ShK toxin. Eur J Biochem 251:133–141
110. Lanigan MD, Kalman K, Lefievre Y, Pennington MW, Chandy KG, Norton RS (2002) Mutating a critical lysine in ShK toxin alters its binding configuration in the pore-vestibule region of the voltage-gated potassium channel, Kv1.3. Biochemistry 41:11963–11971
111. Pennington MW, Harunur Rashid M, Tajhya RB, Beeton C, Kuyucak S, Norton RS (2012) A C-terminally amidated analogue of ShK is a potent and selective blocker of the voltage-gated potassium channel Kv1.3. FEBS Lett 586:3996–4001
112. Alessandri-Haber N, Lecoq A, Gasparini S, Grangier-Macmath G, Jacquet G, Harvey AL, de Medeiros C, Rowan EG, Gola M, Menez A, Crest M (1999) Mapping the functional anatomy of BgK on Kv1.1, Kv1.2, and Kv1.3. Clues to design analogs with enhanced selectivity. J Biol Chem 274:35653–35661
113. Rauer H, Pennington M, Cahalan M, Chandy KG (1999) Structural conservation of the pores of calcium-activated and voltage-gated potassium channels determined by a sea anemone toxin. J Biol Chem 274:21885–21892
114. Dauplais M, Lecoq A, Song J, Cotton J, Jamin N, Gilquin B, Roumestand C, Vita C, de Medeiros CL, Rowan EG, Harvey AL, Menez A (1997) On the convergent evolution of animal toxins. Conservation of a diad of functional residues in potassium channel-blocking toxins with unrelated structures. J Biol Chem 272:4302–4309
115. Manganas LN, Wang Q, Scannevin RH, Antonucci DE, Rhodes KJ, Trimmer JS (2001) Identification of a trafficking determinant localized to the Kv1 potassium channel pore. Proc Natl Acad Sci USA 98:14055–14059
116. Vacher H, Mohapatra DP, Misonou H, Trimmer JS (2007) Regulation of Kv1 channel trafficking by the mamba snake neurotoxin dendrotoxin K. FASEB J 21:906–914
117. Zhu J, Watanabe I, Gomez B, Thornhill WB (2001) Determinants involved in Kv1 potassium channel folding in the endoplasmic reticulum, glycosylation in the Golgi, and cell surface expression. J Biol Chem 276:39419–39427
118. Li D, Takimoto K, Levitan ES (2000) Surface expression of Kv1 channels is governed by a C-terminal motif. J Biol Chem 275:11597–11602
119. Manganas LN, Akhtar S, Antonucci DE, Campomanes CR, Dolly JO, Trimmer JS (2001) Episodic ataxia type-1 mutations in the Kv1.1 potassium channel display distinct folding and intracellular trafficking properties. J Biol Chem 276:49427–49434
120. + channels by interaction with a family of membrane-associated guanylate kinases. Nature 378:85–88
121. + channel modulates its interaction with scaffold proteins. Proc Natl Acad Sci USA 104:13022–13027
122. Ogawa Y, Horresh I, Trimmer JS, Bredt DS, Peles E, Rasband MN (2008) Postsynaptic density-93 clusters Kv1 channels at axon initial segments independently of Caspr2. J Neurosci 28:5731–5739
123. McKeown L, Burnham MP, Hodson C, Jones OT (2008) Identification of an evolutionarily conserved extracellular threonine residue critical for surface expression and its potential coupling of adjacent voltage-sensing and gating domains in voltage-gated potassium channels. J Biol Chem 283:30421–30432
124. Klammt C, Maslennikov I, Bayrhuber M, Eichmann C, Vajpai N, Chiu EJ, Blain KY, Esquivies L, Kwon JH, Balana B, Pieper U, Sali A, Slesinger PA, Kwiatkowski W, Riek R, Choe S (2012) Facile backbone structure determination of human membrane proteins by NMR spectroscopy. Nat Methods 9:834–839
125. Van Horn WD, Vanoye CG, Sanders CR (2011) Working model for the structural basis for KCNE1 modulation of the KCNQ1 potassium channel. Curr Opin Struct Biol 21:283–291
126. Barrett PJ, Song Y, Van Horn WD, Hustedt EJ, Schafer JM, Hadziselimovic A, Beel AJ, Sanders CR (2012) The amyloid precursor protein has a flexible transmembrane domain and binds cholesterol. Science 336:1168–1171
127. + channel trafficking—a sisyphean task? Front Physiol 3:231
128. Kanda VA, Lewis A, Xu X, Abbott GW (2011) KCNE1 and KCNE2 provide a checkpoint governing voltage-gated potassium channel alpha-subunit composition. Biophys J 101:1364–1375
129. Sole L, Roura-Ferrer M, Perez-Verdaguer M, Oliveras A, Calvo M, Fernandez-Fernandez JM, Felipe A (2009) KCNE4 suppresses Kv1.3 currents by modulating trafficking, surface expression and channel gating. J Cell Sci 122:3738–3748
130. McCrossan ZA, Abbott GW (2004) The MinK-related peptides. Neuropharmacology 47:787–821
131. Tapper AR, George AL Jr (2000) MinK subdomains that mediate modulation of and association with KvLQT1. J Gen Physiol 116:379–390
132. Haerteis S, Krappitz M, Bertog M, Krappitz A, Baraznenok V, Henderson I, Lindstrom E, Murphy JE, Bunnett NW, Korbmacher C (2012) Proteolytic activation of the epithelial sodium channel (ENaC) by the cysteine protease cathepsin-S. Pflugers Arch 464:353–365
133. Kitamura K, Tomita K (2012) Proteolytic activation of the epithelial sodium channel and therapeutic application of a serine protease inhibitor for the treatment of salt-sensitive hypertension. Clin Exp Nephrol 16:44–48
134. Liedtke W (2008) Molecular mechanisms of TRPV4-mediated neural signaling. Ann NY Acad Sci 1144:42–52
135. Poole DP, Amadesi S, Veldhuis NA, Abogadie FC, Lieu T, Darby W, Liedtke W, Lew MJ, McIntyre P, Bunnett NW (2013) Protease-activated receptor 2 (PAR2) protein and transient receptor potential vanilloid 4 (TRPV4) protein coupling is required for sustained inflammatory signaling. J Biol Chem 288:5790–5802
136. Hanlon MR, Wallace BA (2002) Structure and function of voltage-dependent ion channel regulatory beta subunits. Biochemistry 41:2886–2894
137. + channel beta subunits in development and disease. Neurosci Lett 486:53–59
138. + channels by the sodium channel beta1 subunit. Proc Natl Acad Sci USA 109:18577–18582
139. Clancy BM, Johnson JD, Lambert AJ, Rezvankhah S, Wong A, Resmini C, Feldman JL, Leppanen S, Pittman DD (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
140. Davidson RK, Waters JG, Kevorkian L, Darrah C, Cooper A, Donell ST, Clark IM (2006) Expression profiling of metalloproteinases and their inhibitors in synovium and cartilage. Arthr Res Ther 8:R124
141. Fortunato SJ, Menon R (2002) Screening of novel matrix metalloproteinases (MMPs) in human fetal membranes. J Assist Reprod Genet 19:483–486
142. Hegedus L, Cho H, Xie X, Eliceiri GL (2008) Additional MDA-MB-231 breast cancer cell matrix metalloproteinases promote invasiveness. J Cell Physiol 216:480–485
143. Jones GC, Corps AN, Pennington CJ, Clark IM, Edwards DR, Bradley MM, Hazleman BL, Riley GP (2006) Expression profiling of metalloproteinases and tissue inhibitors of metalloproteinases in normal and degenerate human achilles tendon. Arthr Rheum 54:832–842
144. Okada A, Okada Y (2009) Progress of research in osteoarthritis. Metalloproteinases in osteoarthritis. Clin Calcium 19:1593–1601
145. Riddick AC, Shukla CJ, Pennington CJ, Bass R, Nuttall RK, Hogan A, Sethia KK, Ellis V, Collins AT, Maitland NJ, Ball RY, Edwards DR (2005) Identification of degradome components associated with prostate cancer progression by expression analysis of human prostatic tissues. Br J Cancer 92:2171–2180
146. Scrideli CA, Carlotti CG Jr, Okamoto OK, Andrade VS, Cortez MA, Motta FJ, Lucio-Eterovic AK, Neder L, Rosemberg S, Oba-Shinjo SM, Marie SK, Tone LG (2008) Gene expression profile analysis of primary glioblastomas and non-neoplastic brain tissue: identification of potential target genes by oligonucleotide microarray and real-time quantitative PCR. J Neurooncol 88:281–291
147. Riley G (2008) Tendinopathy—from basic science to treatment. Nat Clin Pract Rheumatol 4:82–89
148. Gajecka M, Yu W, Ballif BC, Glotzbach CD, Bailey KA, Shaw CA, Kashork CD, Heilstedt HA, Ansel DA, Theisen A, Rice R, Rice DP, Shaffer LG (2005) Delineation of mechanisms and regions of dosage imbalance in complex rearrangements of 1p36 leads to a putative gene for regulation of cranial suture closure. Eur J Hum Genet 13:139–149
149. Zhao S, Zhao Y, Niu P, Wang N, Tang Z, Zan L, Li K (2011) Molecular characterization of porcine MMP19 and MMP23B genes and its association with immune traits. Int J Biol Sci 7:1101–1113
150. Acevedo VD, Gangula RD, Freeman KW, Li R, Zhang Y, Wang F, Ayala GE, Peterson LE, Ittmann M, Spencer DM (2007) Inducible FGFR-1 activation leads to irreversible prostate adenocarcinoma and an epithelial-to-mesenchymal transition. Cancer Cell 12:559–571
151. Carrasco DR, Sukhdeo K, Protopopova M, Sinha R, Enos M, Carrasco DE, Zheng M, Mani M, Henderson J, Pinkus GS, Munshi N, Horner J, Ivanova EV, Protopopov A, Anderson KC, Tonon G, DePinho RA (2007) The differentiation and stress response factor XBP-1 drives multiple myeloma pathogenesis. Cancer Cell 11:349–360
152. Haldar M, Hancock JD, Coffin CM, Lessnick SL, Capecchi MR (2007) A conditional mouse model of synovial sarcoma: insights into a myogenic origin. Cancer Cell 11:375–388
153. Lam SH, Gong Z (2006) Modeling liver cancer using zebrafish: a comparative oncogenomics approach. Cell Cycle 5:573–577
154. Qi F, Song J, Yang H, Gao W, Liu NA, Zhang B, Lin S (2010) MMP23b promotes liver development and hepatocyte proliferation through the tumor necrosis factor pathway in zebrafish. Hepatology 52:2158–2166
155. Wajant H, Pfizenmaier K, Scheurich P (2003) Tumor necrosis factor signaling. Cell Death Differ 10:45–65
156. Schwabe RF, Brenner DA (2006) Mechanisms of Liver Injury. I. TNF-alpha-induced liver injury: role of IKK, JNK, and ROS pathways. Am J Physiol Gastrointest Liver Physiol 290:G583–G589
157. Wullaert A, van Loo G, Heyninck K, Beyaert R (2007) Hepatic tumor necrosis factor signaling and nuclear factor-kappaB: effects on liver homeostasis and beyond. Endocr Rev 28:365–386
158. Black RA, Rauch CT, Kozlosky CJ, Peschon JJ, Slack JL, Wolfson MF, Castner BJ, Stocking KL, Reddy P, Srinivasan S, Nelson N, Boiani N, Schooley KA, Gerhart M, Davis R, Fitzner JN, Johnson RS, Paxton RJ, March CJ, Cerretti DP (1997) A metalloproteinase disintegrin that releases tumor-necrosis factor-alpha from cells. Nature 385:729–733
159. Krogsgaard M, Ma W, Friedman EB, Vega-Saenz de Miera E, Darvishian F, Perez-Garcia RS, Berman RS, Sharpio RL, Christos PJ, Osman I, Pavlick AC (2011) An analysis of altered melanoma matrix metalloprotease-23 (MMP-23) expression and response to immune biologic therapy. J Clin Oncol 29(Suppl):8541
160. Bielanska J, Hernandez-Losa J, Moline T, Somoza R, Cajal SR, Condom E, Ferreres JC, Felipe A (2012) Increased voltage-dependent K(+) channel Kv1.3 and Kv1.5 expression correlates with leiomyosarcoma aggressiveness. Oncol Lett 4:227–230
161. + channels in human skeletal muscle sarcomas. Cancer Invest 30:203–208
162. Bielanska J, Hernandez-Losa J, Perez-Verdaguer M, Moline T, Somoza R, Ramon YCS, Condom E, Ferreres JC, Felipe A (2009) Voltage-dependent potassium channels Kv1.3 and Kv1.5 in human cancer. Curr Cancer Drug Targets 9:904–914
163. + channels Kv1.3 and Kv1.5 as tumor biomarkers for cancer detection and prevention. Curr Med Chem 19:661–674
164. + channels as therapeutic targets in oncology. Future Med Chem 2:745–755
165. Beeton C, Wulff H, Standifer NE, Azam P, Mullen KM, Pennington MW, Kolski-Andreaco A, Wei E, Grino A, Counts DR, Wang PH, LeeHealey CJ, Andrews BS, Sankaranarayanan A, Homerick D, Roeck WW, Tehranzadeh J, Stanhope KL, Zimin P, Havel PJ, Griffey S, Knaus HG, Nepom GT, Gutman GA, Calabresi PA, Chandy KG (2006) Kv1.3 channels are a therapeutic target for T cell-mediated autoimmune diseases. Proc Natl Acad Sci USA 103:17414–17419
166. Leanza L, Henry B, Sassi N, Zoratti M, Chandy KG, Gulbins E, Szabo I (2012) Inhibitors of mitochondrial Kv1.3 channels induce Bax/Bak-independent death of cancer cells. EMBO Mol Med 4:577–593
167. 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
168. Vacher H, Trimmer JS (2012) Trafficking mechanisms underlying neuronal voltage-gated ion channel localization at the axon initial segment. Epilepsia 53(Suppl 9):21–31
169. Patterson NL, Iyer RP, Bras LD, Li Y, Andrews TG, Aune GJ, Lange RA, Lindsey ML (2013) Using proteomics to uncover extracellular matrix interactions during cardiac remodeling. Proteomics Clin Appl. doi:10.1002/prca.201200100
170. Stegemann C, Didangelos A, Barallobre-Barreiro J, Langley SR, Mandal K, Jahangiri M, Mayr M (2013) Proteomic identification of matrix metalloproteinase substrates in the human vasculature. Circ Cardiovasc Genet 6:106–117
171. Austin KM, Covic L, Kuliopulos A (2013) Matrix metalloproteases and PAR1 activation. Blood 121:431–439
172. Haerteis S, Krappitz M, Diakov A, Krappitz A, Rauh R, Korbmacher C (2012) Plasmin and chymotrypsin have distinct preferences for channel activating cleavage sites in the gamma subunit of the human epithelial sodium channel. J Gen Physiol 140:375–389
173. Schrodinger LLC (2010) The PyMOL Molecular Graphics System, Version 1.3r1
174. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
175. Brodskii LI, Ivanov VV, Ia Kalaidzidis Ia L, Leontovich AM, Nikolaev VK, Feranchuk SI, Drachev VA (1995) GeneBee-NET: an Internet based server for biopolymer structure analysis. Biokhimiia 60:1221–1230