Membrane na+-pyrophosphatases can transport protons at low sodium concentrations

Journal of Biological Chemistry

Volumn 288, Issue 49, 2013, Pages 35126-35137

  Luoto, Heidi H ^a   Nordbo, Erika ^a   Baykov, Alexander A ^b   Lahti, Reijo ^a   Malinen, Anssi M ^a  

^a UNIVERSITY OF TURKU   (Finland)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

SODIUM;

LOW SODIUM; PHYSIOLOGICAL CONDITION; PYROPHOSPHATASES; TRANSPORT ACTIVITY;

ION EXCHANGE;

ASPARAGINE; DUAL SPECIFICITY PHOSPHATASE; GLUTAMINE; INORGANIC PYROPHOSPHATASE; PROTON; SERINE; SODIUM ION; SODIUM PYROPHOSPHATASE; UNCLASSIFIED DRUG; ARCHAEAL PROTEIN; BACTERIAL PROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; RECOMBINANT PROTEIN; SODIUM;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; BINDING SITE; BIOACCUMULATION; CATALYSIS; CELL PH; CHLOROBIUM; CHLOROBIUM LIMICOLA; CONTROLLED STUDY; ENZYME ACTIVITY; ESCHERICHIA COLI; HYDROLYSIS; MEMBRANE VESICLE; NONHUMAN; PRIORITY JOURNAL; PROTON TRANSPORT; SODIUM CELL LEVEL; SODIUM CONDUCTANCE; SODIUM TRANSPORT; ACTIVE TRANSPORT; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; GENETICS; KINETICS; METABOLISM; PROTEIN CONFORMATION; SITE DIRECTED MUTAGENESIS;

PROKARYOTA;

AMINO ACID SUBSTITUTION; ARCHAEAL PROTEINS; BACTERIAL PROTEINS; BACTERIAL PROTON-TRANSLOCATING ATPASES; BIOLOGICAL TRANSPORT, ACTIVE; CHLOROBIUM; INORGANIC PYROPHOSPHATASE; KINETICS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PROTEIN CONFORMATION; PROTONS; RECOMBINANT PROTEINS; SODIUM;

EID: 84894341827     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.510909     Document Type: Article

References (57)

1. Sato, H., Takino, T., Okada, Y., Cao, J., Shinagawa, A., Yamamoto, E., and Seiki, M. (1994) A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature 370, 61-65
2. Seiki, M. (2003) Membrane-type 1 matrix metalloproteinase. A key enzyme for tumor invasion. Cancer Lett. 194, 1-11
3. Itoh, Y., and Seiki, M. (2006) MT1-MMP.Apotent modifier of pericellular microenvironment. J. Cell. Physiol. 206, 1-8
4. Sabeh, F., Shimizu-Hirota, R., and Weiss, S. J. (2009) Protease-dependent versus -independent cancer cell invasion programs. Three-dimensional amoeboid movement revisited. J. Cell Biol. 185, 11-19
5. Hotary, K., Allen, E., Punturieri, A., Yana, I., and Weiss, S. J. (2000) Regulation of cell invasion and morphogenesis in a three-dimensional type I collagen matrix by membrane-type matrix metalloproteinases 1, 2, andJ. Cell Biol. 149, 1309-1323
6. Miller, M. C., Manning, H. B., Jain, A., Troeberg, L., Dudhia, J., Essex, D., Sandison, A., Seiki, M., Nanchahal, J., Nagase, H., and Itoh, Y. (2009) Membrane type 1 matrix metalloproteinase is a crucial promoter of synovial invasion in human rheumatoid arthritis. Arthritis Rheum. 60, 686-697
7. Filippov, S., Koenig, G. C., Chun, T. H., Hotary, K. B., Ota, I., Bugge, T. H., Roberts, J. D., Fay, W. P., Birkedal-Hansen, H., Holmbeck, K., Sabeh, F., Allen, E. D., and Weiss, S. J. (2005) MT1-matrix metalloproteinase directs arterial wall invasion and neointima formation by vascular smooth muscle cells. J. Exp. Med. 202, 663-671
8. Ohuchi, E., Imai, K., Fujii, Y., Sato, H., Seiki, M., and Okada, Y. (1997) Membrane type 1 matrix metalloproteinase digests interstitial collagens and other extracellular matrix macromolecules. J. Biol. Chem. 272, 2446-2451
9. Koshikawa, N., Giannelli, G., Cirulli, V., Miyazaki, K., and Quaranta, V. (2000) Role of cell surface metalloprotease MT1-MMP in epithelial cell migration over laminin-5. J. Cell Biol. 148, 615-624
10. Knäuper, V., Will, H., López-Otin, C., Smith, B., Atkinson, S. J., Stanton, H., Hembry, R. M., and Murphy, G. (1996) Cellular mechanisms for human procollagenase 3 (MMP 13) activation. Evidence that MT1 MMP (MMP 14) and gelatinase a (MMP 2) are able to generate active enzyme. J. Biol. Chem. 271, 17124-17131
11. Okada, Y., Morodomi, T., Enghild, J. J., Suzuki, K., Yasui, A., Nakanishi, I., Salvesen, G., and Nagase, H. (1990) Matrix metalloproteinase 2 from human rheumatoid synovial fibroblasts. Purification and activation of the precursor and enzymic properties. Eur. J. Biochem. 194, 721-730
12. Taniwaki, K., Fukamachi, H., Komori, K., Ohtake, Y., Nonaka, T., Sakamoto, T., Shiomi, T., Okada, Y., Itoh, T., Itohara, S., Seiki, M., and Yana, I. (2007) Stroma-derived matrix metalloproteinase (MMP)-2 promotes membrane type 1-MMP-dependent tumor growth in mice. Cancer Res. 67, 4311-4319
13. Kajita, M., Itoh, Y., Chiba, T., Mori, H., Okada, A., Kinoh, H., and Seiki, M. (2001) Membrane-type 1 matrix metalloproteinase cleaves CD44 and promotes cell migration. J. Cell Biol. 153, 893-904
14. Endo, K., Takino, T., Miyamori, H., Kinsen, H., Yoshizaki, T., Furukawa, M., and Sato, H. (2003) Cleavage of syndecan-1 by membrane type matrix metalloproteinase-1 stimulates cell migration. J. Biol. Chem. 278, 40764-40770
15. Ratnikov, B. I., Rozanov, D. V., Postnova, T. I., Baciu, P. G., Zhang, H., DiScipio, R. G., Chestukhina, G. G., Smith, J. W., Deryugina, E. I., and Strongin, A. Y. (2002) An alternative processing of integrin- (v) subunit in tumor cells by membrane type-1 matrix metalloproteinase. J. Biol. Chem. 277, 7377-7385
16. Takino, T., Miyamori, H., Watanabe, Y., Yoshioka, K., Seiki, M., and Sato, H. (2004) Membrane type 1 matrix metalloproteinase regulates collagendependent mitogen-activated protein/extracellular signal-related kinase activation and cell migration. Cancer Res. 64, 1044-1049
17. Yana, I., and Weiss, S. J. (2000) Regulation of membrane type-1 matrix metalloproteinase activation by proprotein convertases. Mol. Biol. Cell 11, 2387-2401
18. Will, H., Atkinson, S. J., Butler, G. S., Smith, B., and Murphy, G. (1996) The soluble catalytic domain of membrane type 1 matrix metalloproteinase cleaves the propeptide of progelatinase A and initiates autoproteolytic activation. Regulation by TIMP-2 and TIMP-3. J. Biol. Chem. 271, 17119-17123
19. Nakada, M., Yamada, A., Takino, T., Miyamori, H., Takahashi, T., Yamashita, J., and Sato, H. (2001) Suppression of membrane-type 1 matrix metalloproteinase (MMP)-mediated MMP-2 activation and tumor invasion by testican 3 and its splicing variant gene product, N-Tes. Cancer Res. 61, 8896-8902
20. Oh, J., Takahashi, R., Kondo, S., Mizoguchi, A., Adachi, E., Sasahara, R. M., Nishimura, S., Imamura, Y., Kitayama, H., Alexander, D. B., Ide, C., Horan, T. P., Arakawa, T., Yoshida, H., Nishikawa, S., Itoh, Y., Seiki, M., Itohara, S., Takahashi, C., and Noda, M. (2001) The membrane-anchored MMP inhibitor RECK is a key regulator of extracellular matrix integrity and angiogenesis. Cell 107, 789-800
21. Lehti, K., Lohi, J., Valtanen, H., and Keski-Oja, J. (1998) Proteolytic processing of membrane-type-1 matrix metalloproteinase is associated with gelatinase A activation at the cell surface. Biochem. J. 334, 345-353
22. Jiang, A., Lehti, K., Wang, X., Weiss, S. J., Keski-Oja, J., and Pei, D. (2001) Regulation of membrane-type matrix metalloproteinase 1 activity by dynamin-mediated endocytosis. Proc. Natl. Acad. Sci. U.S.A. 98, 13693-13698
23. Uekita, T., Itoh, Y., Yana, I., Ohno, H., and Seiki, M. (2001) Cytoplasmic tail-dependent internalization of membrane-type 1 matrix metalloproteinase is important for its invasion-promoting activity. J. Cell Biol. 155, 1345-1356
24. Remacle, A., Murphy, G., and Roghi, C. (2003) Membrane type I-matrix metalloproteinase (MT1-MMP) is internalised by two different pathways and is recycled to the cell surface. J. Cell Sci. 116, 3905-3916
25. Takino, T., Miyamori, H., Kawaguchi, N., Uekita, T., Seiki, M., and Sato, H. (2003) Tetraspanin CD63 promotes targeting and lysosomal proteolysis of membrane-type 1 matrix metalloproteinase. Biochem. Biophys. Res. Commun. 304, 160-166
26. Itoh, Y., Takamura, A., Ito, N., Maru, Y., Sato, H., Suenaga, N., Aoki, T., and Seiki, M. (2001) Homophilic complex formation of MT1-MMP facilitates proMMP-2 activation on the cell surface and promotes tumor cell invasion. EMBO J. 20, 4782-4793
27. Anilkumar, N., Uekita, T., Couchman, J. R., Nagase, H., Seiki, M., and Itoh, Y. (2005) Palmitoylation at Cys-574 is essential forMT1-MMPto promote cell migration. FASEB J. 19, 1326-1328
28. Sato, T., del Carmen Ovejero, M., Hou, P., Heegaard, A. M., Kumegawa, M., Foged, N. T., and Delaissé, J. M. (1997) Identification of the membrane- type matrix metalloproteinaseMT1-MMPin osteoclasts. J. Cell Sci. 110, 589-596
29. Nakahara, H., Howard, L., Thompson, E. W., Sato, H., Seiki, M., Yeh, Y., and Chen, W. T. (1997) Transmembrane/cytoplasmic domain-mediated membrane type 1-matrix metalloprotease docking to invadopodia is required for cell invasion. Proc. Natl. Acad. Sci. U.S.A. 94, 7959-7964
30. Wang, Y., and McNiven, M. A. (2012) Invasive matrix degradation at focal adhesions occurs via protease recruitment by a FAK-p130Cas complex. J. Cell Biol. 196, 375-385
31. Mori, H., Tomari, T., Koshikawa, N., Kajita, M., Itoh, Y., Sato, H., Tojo, H., Yana, I., and Seiki, M. (2002) CD44 directs membrane-type 1 matrix metalloproteinase to lamellipodia by associating with its hemopexin-like domain. EMBO J. 21, 3949-3959
32. Artym, V. V., Zhang, Y., Seillier-Moiseiwitsch, F., Yamada, K. M., and Mueller, S. C. (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
33. Itoh, Y., Ito, N., Nagase, H., and Seiki, M. (2008) The second dimer interface of MT1-MMP, the transmembrane domain, is essential for ProMMP-2 activation on the cell surface. J. Biol. Chem. 283, 13053-13062
34. Hotary, K. B., Allen, E. D., Brooks, P. C., Datta, N. S., Long, M. W., and Weiss, S. J. (2003) Membrane type I matrix metalloproteinase usurps tumor growth control imposed by the three-dimensional extracellular matrix. Cell 114, 33-45
35. Li, X. Y., Ota, I., Yana, I., Sabeh, F., and Weiss, S. J. (2008) Molecular dissection of the structural machinery underlying the tissue-invasive activity of membrane type-1 matrix metalloproteinase. Mol. Biol. Cell 19, 3221-3233
36. Itoh, Y., Ito, N., Nagase, H., Evans, R. D., Bird, S. A., and Seiki, M. (2006) Cell surface collagenolysis requires homodimerization of the membranebound collagenase MT1-MMP. Mol. Biol. Cell 17, 5390-5399
37. Itoh, Y., Palmisano, R., Anilkumar, N., Nagase, H., Miyawaki, A., and Seiki, M. (2011) Dimerization of MT1-MMP during cellular invasion detected by fluorescence resonance energy transfer. Biochem. J. 440, 319-326
38. Suenaga, N., Mori, H., Itoh, Y., and Seiki, M. (2005) CD44 binding through the hemopexin-like domain is critical for its shedding by membrane-type 1 matrix metalloproteinase. Oncogene 24, 859-868
39. Palmisano, R., and Itoh, Y. (2010) Analysis of MMP-dependent cell migration and invasion. Methods Mol. Biol. 622, 379-392
40. Itoh, Y., Ito, A., Iwata, K., Tanzawa, K., Mori, Y., and Nagase, H. (1998) Plasma membrane-bound tissue inhibitor of metalloproteinases (TIMP)-2 specifically inhibits matrix metalloproteinase 2 (gelatinase A) activated on the cell surface. J. Biol. Chem. 273, 24360-24367
41. English, W. R., Holtz, B., Vogt, G., Knäuper, V., and Murphy, G. (2001) Characterization of the role of the "MT-loop." An eight-amino acid inser- tion specific to progelatinase A (MMP2) activating membrane-type matrix metalloproteinases. J. Biol. Chem. 276, 42018-42026
42. Wehrle-Haller, B. (2012) Structure and function of focal adhesions. Curr. Opin. Cell Biol. 24, 116-124
43. Mori, H., Lo, A. T., Inman, J. L., Alcaraz, J., Ghajar, C. M., Mott, J. D., Nelson, C. M., Chen, C. S., Zhang, H., Bascom, J. L., Seiki, M., and Bissell, M. J. (2013) Transmembrane/cytoplasmic, rather than catalytic, domains of Mmp14 signal to MAPK activation and mammary branching morphogenesis via binding to integrin beta1. Development 140, 343-352
44. Gálvez, B. G., Matías-Román, S., Yáñez-Mó, M., Sánchez-Madrid, F., and Arroyo, A. G. (2002) ECM regulates MT1-MMP localization with -1 or -v-3 integrins at distinct cell compartments modulating its internalization and activity on human endothelial cells. J. Cell Biol. 159, 509-521
45. Weaver, A. M. (2006) Invadopodia. Specialized cell structures for cancer invasion. Clin. Exp. Metastasis 23, 97-105
46. Poincloux, R., Lizárraga, F., and Chavrier, P. (2009) Matrix invasion by tumour cells.Afocus on MT1-MMP trafficking to invadopodia. J. Cell Sci. 122, 3015-3024
47. Yamaguchi, H., Lorenz, M., Kempiak, S., Sarmiento, C., Coniglio, S., Symons, M., Segall, J., Eddy, R., Miki, H., Takenawa, T., and Condeelis, J. (2005) Molecular mechanisms of invadopodium formation. The role of the N-WASP-Arp2/3 complex pathway and cofilin. J. Cell Biol. 168, 441-452
48. Mueller, S. C., Ghersi, G., Akiyama, S. K., Sang, Q. X., Howard, L., Pineiro- Sanchez, M., Nakahara, H., Yeh, Y., and Chen, W. T. (1999) A novel protease-docking function of integrin at invadopodia. J. Biol. Chem. 274, 24947-24952
49. Zhang, W., Matrisian, L. M., Holmbeck, K., Vick, C. C., and Rosenthal, E. L. (2006) Fibroblast-derived MT1-MMP promotes tumor progression in vitro and in vivo. BMC Cancer 6, 52
50. Chun, T. H., Sabeh, F., Ota, I., Murphy, H., McDonagh, K. T., Holmbeck, K., Birkedal-Hansen, H., Allen, E. D., and Weiss, S. J. (2004) MT1-MMPdependent neovessel formation within the confines of the three-dimensional extracellular matrix. J. Cell Biol. 167, 757-767
51. Sakamoto, T., and Seiki, M. (2009) Cytoplasmic tail of MT1-MMP regulates macrophage motility independently from its protease activity. Genes Cells 14, 617-626
52. Sabeh, F., Fox, D., and Weiss, S. J. (2010) Membrane-type I matrix metalloproteinase- dependent regulation of rheumatoid arthritis synoviocyte function. J. Immunol. 184, 6396-6406
53. Devy, L., Huang, L., Naa, L., Yanamandra, N., Pieters, H., Frans, N., Chang, E., Tao, Q., Vanhove, M., Lejeune, A., van Gool, R., Sexton, D. J., Kuang, G., Rank, D., Hogan, S., Pazmany, C., Ma, Y. L., Schoonbroodt, S., Nixon, A. E., Ladner, R. C., Hoet, R., Henderikx, P., Tenhoor, C., Rabbani, S. A., Valentino, M. L., Wood, C. R., and Dransfield, D. T. (2009) Selective inhibition of matrix metalloproteinase-14 blocks tumor growth, invasion, and angiogenesis. Cancer Research 69, 1517-1526
54. Strongin, A. Y., Collier, I., Bannikov, G., Marmer, B. L., Grant, G. A., and Goldberg, G. I. (1995) Mechanism of cell surface activation of 72-kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease. J. Biol. Chem. 270, 5331-5338
55. Remacle, A. G., Golubkov, V. S., Shiryaev, S. A., Dahl, R., Stebbins, J. L., Chernov, A. V., Cheltsov, A. V., Pellecchia, M., and Strongin, A. Y. (2012) Novel MT1-MMP small-molecule inhibitors based on insights into hemopexin domain function in tumor growth. Cancer Res. 72, 2339-2349
56. Ingvarsen, S., Porse, A., Erpicum, C., Maertens, L., Jürgensen, H. J., Madsen, D. H., Melander, M. C., Gårdsvoll, H., Høyer-Hansen, G., Noel, A., Holmbeck, K., Engelholm, L. H., and Behrendt, N. (2013) Targeting a single function of the multifunctional matrix metalloprotease MT1- MMP. Impact on lymphangiogenesis. J. Biol. Chem. 288, 10195-10204
57. Fernandez-Catalan, C., Bode, W., Huber, R., Turk, D., Calvete, J. J., Lichte, A., Tschesche, H., and Maskos, K. (1998) Crystal structure of the complex formed by the membrane type 1-matrix metalloproteinase with the tissue inhibitor of metalloproteinases-2, the soluble progelatinase A receptor. EMBO J. 17, 5238-5248.