NaV1.5 Na+ channels allosterically regulate the NHE-1 exchanger and promote the activity of breast cancer cell invadopodia

Journal of Cell Science

Volumn 126, Issue 21, 2013, Pages 4835-4842

  Brisson, Lucie ^a   Driffort, Virginie ^a   Benoist, Lauriane ^a   Poet, Mallorie ^b   Counillon, Laurent ^b   Antelmi, Ester ^c   Rubino, Rosa ^c   Besson, Pierre ^a   Labbal, Fabien ^b   Chevalier, Stéphan ^a   Reshkin, Stephan J ^c   Gore, Jacques ^a   Roger, Sébastien ^a  

^a UNIVERSITÉ DE TOURS   (France)

^b UNIVERSITÉ CÔTE D'AZUR   (France)

^c UNIVERSITY OF BARI   (Italy)

Author keywords

Cancer cell invasiveness; Caveolae; Invadopodia; Na+ H+ exchanger type 1; SCN5A; Voltage gated Na+ channels

Indexed keywords

CATHEPSIN; CAVEOLIN 1; CORTACTIN; CYSTEINE; F ACTIN; PROTON; SODIUM CHANNEL NAV1.5; SODIUM PROTON EXCHANGE PROTEIN 1;

ACIDIFICATION; ALLOSTERISM; ANIMAL CELL; ARTICLE; BREAST CANCER; CANCER CELL; CELL INVASION; CELL PH; CELL STRUCTURE; CONTROLLED STUDY; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INVADOPODIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN POLYMERIZATION;

CANCER CELL INVASIVENESS; CAVEOLAE; INVADOPODIA; NA+/H+ EXCHANGER TYPE 1; SCN5A; VOLTAGE-GATED NA+ CHANNELS;

BREAST NEOPLASMS; CAVEOLIN 1; CELL LINE, TUMOR; CELL SURFACE EXTENSIONS; CORTACTIN; EXTRACELLULAR MATRIX; FEMALE; HUMANS; NAV1.5 VOLTAGE-GATED SODIUM CHANNEL; PHOSPHORYLATION; PROTEIN BINDING; SODIUM-HYDROGEN ANTIPORTER;

EID: 84887577488     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.123901     Document Type: Article

References (44)

1. Arber, S., Barbayannis, F. A., Hanser, H., Schneider, C., Stanyon, C. A., Bernard, O. and Caroni, P. (1998). Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature, 393, 805-809.
2. Baumgartner, M., Patel, H. and Barber, D. L. (2004). Na(+)/H(+) exchanger NHE1 as plasma membrane scaffold in the assembly of signaling complexes. Am. J. Physiol. 287, C844-C850.
3. Black, J. A. and Waxman, S. G. (2012). Sodium channels and microglial function. Exp. Neurol., 234, 302-315.
4. Bourguignon, L. Y., Singleton, P. A., Diedrich, F., Stern, R. and Gilad, E. (2004). CD44 interaction with Na+-H+ exchanger (NHE1) creates acidic microenvironments leading to hyaluronidase-2 and cathepsin B activation and breast tumor cell invasion. J. Biol. Chem., 279, 26991-27007.
5. Brisson, L., Gillet, L., Calaghan, S., Besson, P., Le Guennec, J. Y., Roger, S. and Gore, J. (2011). Na(V)1.5 enhances breast cancer cell invasiveness by increasing NHE1-dependent H(+) efflux in caveolae. Oncogene, 30, 2070-2076.
6. Brisson, L., Reshkin, S. J., Goré, J. and Roger, S. (2012). pH regulators in invadosomal functioning: proton delivery for matrix tasting. Eur. J. Cell Biol., 91, 847-860.
7. Busco, G., Cardone, R. A., Greco, M. R., Bellizzi, A., Colella, M., Antelmi, E., Mancini, M. T., Dell'Aquila, M. E., Casavola, V., Paradiso, A. et al. (2010). NHE1 promotes invadopodial ECM proteolysis through acidification of the peri-invadopodial space. FASEB J., 24, 3903-3915.
8. Caldieri, G. and Buccione, R. (2010). Aiming for invadopodia: organizing polarized delivery at sites of invasion. Trends Cell Biol., 20, 64-70.
9. Caldieri, G., Giacchetti, G., Beznoussenko, G., Attanasio, F., Ayala, I. and Buccione, R. (2009). Invadopodia biogenesis is regulated by caveolin-mediated modulation of membrane cholesterol levels. J. Cell. Mol. Med. 13 8B, 1728-1740.
10. Caldieri, G., Capestrano, M., Bicanova, K., Beznoussenko, G., Baldassarre, M. and Buccione, R. (2012). Polarised apical-like intracellular sorting and trafficking regulates invadopodia formation and degradation of the extracellular matrix in cancer cells. Eur. J. Cell Biol., 91, 961-968.
11. Callies, C., Fels, J., Liashkovich, I., Kliche, K., Jeggle, P., Kusche-Vihrog, K. and Oberleithner, H. (2011). Membrane potential depolarization decreases the stiffness of vascular endothelial cells. J. Cell Sci., 124, 1936-1942.
12. Cardone, R. A., Casavola, V. and Reshkin, S. J. (2005). The role of disturbed pH dynamics and the Na+/H+ exchanger in metastasis. Nat. Rev. Cancer, 5, 786-795.
13. Carrithers, M. D., Dib-Hajj, S., Carrithers, L. M., Tokmoulina, G., Pypaert, M., Jonas, E. A. and Waxman, S. G. (2007). Expression of the voltage-gated sodium channel NaV1.5 in the macrophage late endosome regulates endosomal acidification. J. Immunol., 178, 7822-7832.
14. Carrithers, M. D., Chatterjee, G., Carrithers, L. M., Offoha, R., Iheagwara, U., Rahner, C., Graham, M. and Waxman, S. G. (2009). Regulation of podosome formation in macrophages by a splice variant of the sodium channel SCN8A. J. Biol. Chem., 284, 8114-8126.
15. Catterall, W. A. (2012). Voltage-gated sodium channels at 60: structure, function and pathophysiology. J. Physiol., 590, 2577-2589.
16. Diaz, D., Delgadillo, D. M., Hernández-Gallegos, E., Ramírez-Domínguez, M. E., Hinojosa, L. M., Ortiz, C. S., Berumen, J., Camacho, J. and Gomora, J. C. (2007). Functional expression of voltage-gated sodium channels in primary cultures of human cervical cancer. J. Cell. Physiol., 210, 469-478.
17. Frantz, C., Barreiro, G., Dominguez, L., Chen, X., Eddy, R., Condeelis, J., Kelly, M. J., Jacobson, M. P. and Barber, D. L. (2008). Cofilin is a pH sensor for actin free barbed end formation: role of phosphoinositide binding. J. Cell Biol., 183, 865-879.
18. Fraser, S. P., Diss, J. K., Chioni, A. M., Mycielska, M. E., Pan, H., Yamaci, R. F., Pani, F., Siwy, Z., Krasowska, M., Grzywna, Z. et al. (2005). Voltage-gated sodium channel expression and potentiation of human breast cancer metastasis. Clin. Cancer Res., 11, 5381-5389.
19. Gawden-Bone, C., Zhou, Z., King, E., Prescott, A., Watts, C. and Lucocq, J. (2010). Dendritic cell podosomes are protrusive and invade the extracellular matrix using metalloproteinase MMP-14. J. Cell Sci., 123, 1427-1437.
20. Gillet, L., Roger, S., Besson, P., Lecaille, F., Gore, J., Bougnoux, P., Lalmanach, G. and Le Guennec, J. Y. (2009). Voltage-gated Sodium Channel Activity Promotes Cysteine Cathepsin-dependent Invasiveness and Colony Growth of Human Cancer Cells. J. Biol. Chem., 284, 8680-8691.
21. Harvey, R. D. and Calaghan, S. C. (2012). Caveolae create local signalling domains through their distinct protein content, lipid profile and morphology. J. Mol. Cell. Cardiol., 52, 366-375.
22. Hernandez-Plata, E., Ortiz, C. S., Marquina-Castillo, B., Medina-Martinez, I., Alfaro, A., Berumen, J., Rivera, M. and Gomora, J. C. (2012). Overexpression of NaV 1.6 channels is associated with the invasion capacity of human cervical cancer. Int. J. Cancer, 130, 2013-2023.
23. House, C. D., Vaske, C. J., Schwartz, A. M., Obias, V., Frank, B., Luu, T., Sarvazyan, N., Irby, R., Strausberg, R. L., Hales, T. G. et al. (2010). Voltage-gated Na+ channel SCN5A is a key regulator of a gene transcriptional network that controls colon cancer invasion. Cancer Res., 70, 6957-6967.
24. Jelassi, B., Chantôme, A., Alcaraz-Pérez, F., Baroja-Mazo, A., Cayuela, M. L., Pelegrin, P., Surprenant, A. and Roger, S. (2011). P2X(7) receptor activation enhances SK3 channels- and cystein cathepsin-dependent cancer cells invasiveness. Oncogene, 30, 2108-2122.
25. Jézéquel, P., Campone, M., Gouraud, W., Guérin-Charbonnel, C., Leux, C., Ricolleau, G. and Campion, L. (2012). bc-GenExMiner: an easy-to-use online platform for gene prognostic analyses in breast cancer. Breast Cancer Res. Treat., 131, 765-775.
26. Lacroix, J., Poët, M., Maehrel, C. and Counillon, L. (2004). A mechanism for the activation of the Na/H exchanger NHE-1 by cytoplasmic acidification and mitogens. EMBO Rep., 5, 91-96.
27. Linder, S. (2007). The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol., 17, 107-117.
28. Linder, S., Wiesner, C. and Himmel, M. (2011). Degrading devices: invadosomes in proteolytic cell invasion. Annu. Rev. Cell Dev. Biol., 27, 185-211.
29. MacGrath, S. M. and Koleske, A. J. (2012). Cortactin in cell migration and cancer at a glance. J. Cell Sci., 125, 1621-1626.
30. Magalhaes, M. A., Larson, D. R., Mader, C. C., Bravo-Cordero, J. J., Gil-Henn, H., Oser, M., Chen, X., Koleske, A. J. and Condeelis, J. (2011). Cortactin phosphorylation regulates cell invasion through a pH-dependent pathway. J. Cell Biol., 195, 903-920.
31. Milosavljevic, N., Duranton, C., Djerbi, N., Puech, P. H., Gounon, P., Lagadic-Gossmann, D., Dimanche-Boitrel, M. T., Rauch, C., Tauc, M., Counillon, L. et al. (2010). Nongenomic effects of cisplatin: acute inhibition of mechanosensitive transporters and channels without actin remodeling. Cancer Res., 70, 7514-7522.
32. Oser, M., Yamaguchi, H., Mader, C. C., Bravo-Cordero, J. J., Arias, M., Chen, X., Desmarais, V., van Rheenen, J., Koleske, A. J. and Condeelis, J. (2009). Cortactin regulates cofilin and N-WASp activities to control the stages of invadopodium assembly and maturation. J. Cell Biol., 186, 571-587.
33. Oser, M., Mader, C. C., Gil-Henn, H., Magalhaes, M., Bravo-Cordero, J. J., Koleske, A. J. and Condeelis, J. (2010). Specific tyrosine phosphorylation sites on cortactin regulate Nck1-dependent actin polymerization in invadopodia. J. Cell Sci., 123, 3662-3673.
34. Pope, B. J., Zierler-Gould, K. M., Kühne, R., Weeds, A. G. and Ball, L. J. (2004). Solution structure of human cofilin: actin binding, pH sensitivity, and relationship to actin-depolymerizing factor. J. Biol. Chem., 279, 4840-4848.
35. Roger, S., Besson, P. and Le Guennec, J. Y. (2003). Involvement of a novel fast inward sodium current in the invasion capacity of a breast cancer cell line. Biochim. Biophys. Acta, 1616, 107-111.
36. Roger, S., Potier, M., Vandier, C., Besson, P. and Le Guennec, J. Y. (2006). Voltagegated sodium channels: new targets in cancer therapy? Curr. Pharm. Des., 12, 3681-3695.
37. Roger, S., Rollin, J., Barascu, A., Besson, P., Raynal, P. I., Iochmann, S., Lei, M., Bougnoux, P., Gruel, Y. and Le Guennec, J. Y. (2007). Voltage-gated sodium channels potentiate the invasive capacities of human non-small-cell lung cancer cell lines. Int. J. Biochem. Cell Biol., 39, 774-786.
38. Schoumacher, M., Goldman, R. D., Louvard, D. and Vignjevic, D. M. (2010). Actin, microtubules, and vimentin intermediate filaments cooperate for elongation of invadopodia. J. Cell Biol., 189, 541-556.
39. Söderberg, O., Gullberg, M., Jarvius, M., Ridderstråle, K., Leuchowius, K. J., Jarvius, J., Wester, K., Hydbring, P., Bahram, F., Larsson, L. G. et al. (2006). Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods, 3, 995-1000.
40. Stock, C. and Schwab, A. (2009). Protons make tumor cells move like clockwork. Pflugers Arch., 458, 981-992.
41. Yamaguchi, H. and Oikawa, T. (2010). Membrane lipids in invadopodia and podosomes: key structures for cancer invasion and metastasis. Oncotarget, 1, 320-328.
42. Yamaguchi, H., Takeo, Y., Yoshida, S., Kouchi, Z., Nakamura, Y. and Fukami, K. (2009). Lipid rafts and caveolin-1 are required for invadopodia formation and extracellularmatrix degradation by human breast cancer cells. Cancer Res., 69, 8594-8602.
43. Yang, M., Kozminski, D. J., Wold, L. A., Modak, R., Calhoun, J. D., Isom, L. L. and Brackenbury, W. J. (2012). Therapeutic potential for phenytoin: targeting Na(v)1.5 sodium channels to reduce migration and invasion in metastatic breast cancer. Breast Cancer Res. Treat., 134, 603-615.
44. Yildirim, S., Altun, S., Gumushan, H., Patel, A. and Djamgoz, M. B. (2012). Voltagegated sodium channel activity promotes prostate cancer metastasis in vivo. Cancer Lett., 323, 58-61.