The function of vacuolar ATPase (V-ATPase) a subunit isoforms in invasiveness of MCF10a and MCF10CA1a human breast cancer cells

Journal of Biological Chemistry

Volumn 288, Issue 45, 2013, Pages 32731-32741

  Capecci, Joseph ^a   Forgac, Michael ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BREAST TUMOR CELLS; CANCER CELL LINES; HUMAN BREAST CANCER; HUMAN BREAST CANCER CELLS; METASTATIC POTENTIAL; SUBCELLULAR LOCALIZATIONS; TUMOR CELL INVASION; V-ATPASE INHIBITORS;

CELL CULTURE;

CELL MEMBRANES;

ADENOSINE TRIPHOSPHATASE; CONCANAMYCIN A; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VACUOLAR ADENOSINE TRIPHOSPHATASE;

ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CANCER CELL; CANCER CELL CULTURE; CELL INVASION; CELL MEMBRANE; CELL STRAIN MCF10A; CELL STRAIN MCF10CA1A; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOLYSIS; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; METASTASIS POTENTIAL; PLASMID; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

A SUBUNIT ISOFORMS; BIOENERGETICS; BREAST CANCER; INVASION; PROTON PUMPS; PROTON TRANSPORT; VACUOLAR ATPASE;

BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MEMBRANE; ENZYME INHIBITORS; FEMALE; HUMANS; ISOENZYMES; MACROLIDES; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; PROTEIN TRANSPORT; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 84887439107     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.503771     Document Type: Article

References (42)

1. Nguyen, D. X., Bos, P. D., and Massagué J. (2009) Metastasis. From dissemination to organ-specific colonization. Nat. Rev. Cancer 9, 274-284
2. Spano, D., and Zollo, M. (2012) Tumor microenvironment. A main actor in the metastasis process. Clin. Exp. Metastasis 29, 381-395
3. Gupta, G. P., and Massagué, J. (2006) Cancer metastasis. Building a framework. Cell 127, 679-695
4. Martínez-Zaguilán, R., Seftor, E. A., Seftor, R. E., Chu, Y. W., Gillies, R. J., and Hendrix, M. J. (1996) Acidic pH enhances the invasive behavior of human melanoma cells. Clin. Exp. Metastasis 14, 176-186
5. 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
6. Forgac, M. (2007) Vacuolar ATPases. Rotary proton pumps in physiology and pathophysiology. Nat. Rev. Mol. Cell Biol. 8, 917-929
7. Li, S. C., and Kane, P. M. (2009) The yeast lysosome-like vacuole. Endpoint and crossroads. Biochim. Biophys. Acta 1793, 650-663
8. Brown, D., Paunescu, T. G., Breton, S., and Marshansky, V. (2009) Regulation of the V-ATPase in kidney epithelial cells. Dual role in acid-base homeostasis and vesicle trafficking. J. Exp. Biol. 212, 1762-1772
9. Wang, Y., Toei, M., and Forgac, M. (2008) Analysis of the membrane topology of transmembrane segments in the C-terminal hydrophobic domain of the yeast vacuolar ATPase subunit a (Vph1p) by chemical modification. J. Biol. Chem. 283, 20696-20702
10. Kawasaki-Nishi, S., Bowers, K., Nishi, T., Forgac, M., and Stevens, T. H. (2001) The amino-terminal domain of the vacuolar proton-translocating ATPase a subunit controls targeting and in vivo dissociation, and the carboxyl-terminal domain affects coupling of proton transport and ATP hydrolysis. J. Biol. Chem. 276, 47411-47420
11. Toei, M., Saum, R., and Forgac, M. (2010) Regulation and isoform function of the V-ATPases. Biochemistry 49, 4715-4723
12. Morel, N., Dedieu, J. C., and Philippe, J. M. (2003) Specific sorting of the a1 isoform of the V-H+ATPase a subunit to nerve terminals where it associates with both synaptic vesicles and the presynaptic plasma membrane. J. Cell Sci. 116, 4751-4762
13. Toyomura, T., Murata, Y., Yamamoto, A., Oka, T., Sun-Wada, G. H., Wada, Y., and Futai, M. (2003) From lysosomes to the plasma membrane. Localization of vacuolar-type H+-ATPase with the a3 isoform during osteoclast differentiation. J. Biol. Chem. 278, 22023-22030
14. Hurtado-Lorenzo, A., Skinner, M., El Annan, J., Futai, M., Sun-Wada, G. H., Bourgoin, S., Casanova, J., Wildeman, A., Bechoua, S., Ausiello, D. A., Brown, D., and Marshansky, V. (2006) V-ATPase interacts with ARNO and Arf6 in early endosomes and regulates the protein degradative pathway. Nat. Cell Biol. 8, 124-136
15. Sun-Wada, G. H., Toyomura, T., Murata, Y., Yamamoto, A., Futai, M., and Wada, Y. (2006) The a3 isoform of V-ATPase regulates insulin secretion from pancreatic β-cells. J. Cell Sci. 119, 4531-4540
16. Frattini, A., Orchard, P. J., Sobacchi, C., Giliani, S., Abinun, M., Mattsson, J. P., Keeling, D. J., Andersson, A. K., Wallbrandt, P., Zecca, L., Notarangelo, L. D., Vezzoni, P., and Villa, A. (2000) Defects in TCIRG1 subunit of the vacuolar proton pump are responsible for a subset of human autosomal recessive osteopetrosis. Nat. Genet. 25, 343-346
17. Toyomura, T., Oka, T., Yamaguchi, C., Wada, Y., and Futai, M. (2000) Three subunit a isoforms of mouse vacuolar H+-ATPase. Preferential expression of the a3 isoform during osteoclast differentiation. J. Biol. Chem. 275, 8760-8765
18. Hu, Y., Nyman, J., Muhonen, P., Väänänen, H. K., and Laitala-Leinonen, T. (2005) Inhibition of the osteoclast V-ATPase by small interfering RNAs. FEBS Lett. 579, 4937-4942
19. Smith, A. N., Skaug, J., Choate, K. A., Nayir, A., Bakkaloglu, A., Ozen, S., Hulton, S. A., Sanjad, S. A., Al-Sabban, E. A., Lifton, R. P., Scherer, S. W., and Karet, F. E. (2000) Mutations in ATP6N1B, encoding a new kidney vacuolar proton pump 116-kD subunit, cause recessive distal renal tubular acidosis with preserved hearing. Nat. Genet. 26, 71-75
20. Oka, T., Murata, Y., Namba, M., Yoshimizu, T., Toyomura, T., Yamamoto, A., Sun-Wada, G. H., Hamasaki, N., Wada, Y., and Futai, M. (2001) a4, a unique kidney-specific isoform of mouse vacuolar H+-ATPase subunit a. J. Biol. Chem. 276, 40050-40054
21. Smith, A. N., Finberg, K. E., Wagner, C. A., Lifton, R. P., Devonald, M. A., Su, Y., Karet, F. E. (2001) Molecular cloning and characterization of Atp6n1b. A novel fourth murine vacuolar H+-ATPase a-subunit gene. J. Biol. Chem. 276, 42382-42388
22. Pietrement, C., Sun-Wada, G. H., Silva, N. D., McKee, M., Marshansky, V., Brown, D., Futai, M., and Breton, S. (2006) Distinct expression patterns of different subunit isoforms of the V-ATPase in the rat epididymis. Biol. Reprod. 74, 185-194
23. Sennoune, S. R., Bakunts, K., Martínez, G. M., Chua-Tuan, J. L., Kebir, Y., Attaya, M. N., and Martínez-Zaguilán, R. (2004) Vacuolar H+-ATPase in human breast cancer cells with distinct metastatic potential. Distribution and functional activity. Am. J. Physiol. Cell Physiol. 286, C1443-52
24. Hinton, A., Sennoune, S. R., Bond, S., Fang, M., Reuveni, M., Sahagian, G. G., Jay, D., Martinez-Zaguilan, R., and Forgac, M. (2009) Function of a subunit isoforms of the V-ATPase in pH homeostasis and in vitro invasion of MDA-MB231 human breast cancer cells. J. Biol. Chem. 284, 16400-16408
25. Soule, H. D., Vazguez, J., Long, A., Albert, S., and Brennan, M. (1973) A human cell line from a pleural effusion derived from a breast carcinoma. J. Natl. Cancer Inst. 51, 1409-1416
26. Cailleau, R., Young, R., Olivé, M., and Reeves, W. J. (1974) Breast tumor cell lines from pleural effusions. J. Natl. Cancer Inst. 53, 661-674
27. Chung, C., Mader, C. C., Schmitz, J. C., Atladottir, J., Fitchev, P., Cornwell, M. L., Koleske, A. J., Crawford, S. E., and Gorelick, F. (2011) The vacuolar- ATPase modulates matrix metalloproteinase isoforms in human pancreatic cancer. Lab. Invest. 91, 732-743
28. Nishisho, T., Hata, K., Nakanishi, M., Morita, Y., Sun-Wada, G. H., Wada, Y., Yasui, N., and Yoneda, T. (2011) The a3 isoform vacuolar type H+- ATPase promotes distant metastasis in the mouse B16 melanoma cells. Mol. Cancer Res. 9, 845-855
29. Michel, V., Licon-Munoz, Y., Trujillo, K., Bisoffi, M., and Parra, K. J. (2013) Inhibitors of vacuolar ATPase proton pumps inhibit human prostate cancer cell invasion and prostate-specific antigen expression and secretion. Int. J. Cancer 132, E1-E10
30. Soule, H. D., Maloney, T. M., Wolman, S. R., Peterson, W. D., Jr., Brenz, R., McGrath, C. M., Russo, J., Pauley, R. J., Jones, R. F., and Brooks, S. C. (1990) Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10. Cancer Res. 50, 6075-6086
31. Santner, S. J., Dawson, P. J., Tait, L., Soule, H. D., Eliason, J., Mohamed, A. N., Wolman, S. R., Heppner, G. H., and Miller, F. R. (2001) Malignant MCF10CA1 cell lines derived from premalignant human breast epithelial MCF10AT cells. Breast Cancer Res. Treat. 65, 101-110
32. Debnath, J., Muthuswamy, S. K., and Brugge, J. S. (2003) Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in threedimensional basement membrane cultures. Methods 30, 256-268
33. Partridge, J., and Flaherty, P. (2009) An in vitro FluoroBlok tumor invasion assay. J. Vis. Exp. 29, 1475
34. Dawson, P. J., Wolman, S. R., Tait, L., Heppner, G. H., and Miller F. R. (1996) MCF10AT. A model for the evolution of cancer from proliferative breast disease. Am. J. Pathol. 148, 313-319
35. Rojas, J. D., Sennoune, S. R., Maiti, D., Bakunts, K., Reuveni, M., Sanka, S. C., Martinez, G. M., Seftor, E. A., Meininger, C. J., Wu, G., Wesson, D. E., Hendrix, M. J., and Martínez-Zaguilán, R. (2006) Vacuolar-type H+- ATPases at the plasma membrane regulate pH and cell migration in microvascular endothelial cells. Am. J. Physiol. Heart Circ. Physiol. 291, 1147-1157
36. Gocheva, V., and Joyce, J. A. (2007) Cysteine cathepsins and the cutting edge of cancer invasion. Cell Cycle 6, 60-64
37. Gondi, C. S., and Rao, J. S. (2013) Cathepsin B as a cancer target. Expert Opin. Ther. Targets 17, 281-291
38. Robey, I. F., Baggett, B. K., Kirkpatrick, N. D., Roe, D. J., Dosescu, J., Sloane, B. F., Hashim, A. I., Morse, D. L., Raghunand, N., Gatenby, R. A., and Gillies, R. J (2009). Bicarbonate increases tumor pH and inhibits spontaneous metastases. Cancer Res. 69, 2260-2268
39. Cao, X., Yang, Q., Qin, J., Zhao, S., Li, X., Fan, J., Chen, W., Zhou, Y., Mao, H., and Yu, X. (2012) V-ATPase promotes transforming growth factor-β- induced epithelial-mesenchymal transition of rat proximal tubular epithelial cells. Am. J. Physiol. Renal Physiol. 302, 1121-1132
40. Wiedmann, R. M., von Schwarzenberg, K., Palamidessi, A., Schreiner, L., Kubisch, R., Liebl, J., Schempp, C., Trauner, D., Vereb, G., Zahler, S., Wagner, E., Müller, R., Scita, G., and Vollmar, A. M. (2012) The VATPase- inhibitor archazolid abrogates tumor metastasis via inhibition of endocytic activation of the Rho-GTPase Rac1. Cancer Res. 72, 5976-5987
41. Hendrix, A., Sormunen, R., Westbroek, W., Lambein, K., Denys, H., Sys, G., Braems, G., Van den Broecke, R., Cocquyt, V., Gespach, C., Bracke, M., and De Wever, O. (2013) Vacuolar H+ ATPase expression and activity is required for Rab27B-dependent invasive growth and metastasis of breast cancer. Int. J. Cancer 133, 843-854
42. Glunde, K., Guggino, S. E., Solaiyappan, M., Pathak, A. P., Ichikawa, Y., and Bhujwalla, Z. M. (2003) Extracellular acidification alters lysosomal trafficking in human breast cancer cells. Neoplasia 5, 533-545