HGF-induced invasion by prostate tumor cells requires anterograde lysosome trafficking and activity of Na+-H+ exchangers

Journal of Cell Science

Volumn 123, Issue 7, 2010, Pages 1151-1159

  Steffan, Joshua J ^a   Williams, Brittany C ^a   Welbourne, Tomas ^a   Cardelli, James A ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

Cathepsin secretion; Cell invasion; EIPA; Glycolysis; HGF; Lysosome trafficking; NHE1; ORP1L; Rab7; RILP

Indexed keywords

CATHEPSIN B; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN RILP; RAB7 PROTEIN; REGULATOR PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SCATTER FACTOR; SHORT HAIRPIN RNA; SODIUM PROTON EXCHANGE PROTEIN 1; SODIUM PROTON EXCHANGE PROTEIN 3; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL CULTURE; CANCER INVASION; CONTROLLED STUDY; HUMAN; HUMAN CELL; LYSOSOME; MICROTUBULE; PRIORITY JOURNAL; PROSTATE TUMOR; PROTEIN EXPRESSION; PROTEIN FUNCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; CATHEPSIN B; CELL LINE, TUMOR; CELL MOVEMENT; CLONING, MOLECULAR; CYTOPLASMIC STREAMING; HEPATOCYTE GROWTH FACTOR; HUMANS; LYSOSOMES; MALE; NEOPLASM INVASIVENESS; PROSTATIC NEOPLASMS; PROTON PUMP INHIBITORS; RAB GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; SODIUM-HYDROGEN ANTIPORTER; TRANSGENES;

EID: 77951165622     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.063644     Document Type: Article

References (63)

1. Acloque, H., Thiery, J. and Nieto, M. (2008). The physiology and pathology of the EMT. EMBO J. 9, 22-26.
2. Agarwal, S., Zerillo, C., Kolmakova, J., Christensen, J. G., Harris, L. N., Rimm, D. L., DiGiovanna, M. P. and Stern, D. F. (2009). Association of constitutively activated hepatocyte growth factor receptor (Met) with resistance to a dual EGFR//Her2 inhibitor in non-small-cell lung cancer cells. Br. J. Cancer 100, 941-949.
3. Benvenuti, S. and Comoglio, P. M. (2007). The MET receptor tyrosine kinase in invasion and metastasis. J. Cell. Physiol. 213, 316-325.
4. Bertola, A., Bonnafous, S., Cormont, M., Anty, R., Tanti, J.-F., Tran, A., Le Marchand-Brustel, Y. and Gual, P. (2007). Hepatocyte growth factor induces glucose uptake in 3T3-L1 adipocytes through a Gab1/phosphatidylinositol 3-kinase/Glut4 pathway. J. Biol. Chem. 282, 10325-10332.
5. Birchmeier, C., Birchmeier, W., Gherardi, E. and Vande Woude, G. F. (2003). Met, metastasis, motility and more. Nat. Rev. Mol. Cell Biol. 4, 915-925.
6. Boccaccio, C. and Comoglio, P. M. (2006). Invasive growth: a MET-driven genetic programme for cancer and stem cells. Nat. Rev. Cancer 6, 637-645.
7. Bourguignon, L. Y. (2008). Hyaluronan-mediated CD44 activation of RhoGTPase signaling and cytoskeleton function promotes tumor progression. Semin. Cancer Biol. 18, 251-259.
8. Bourguignon, L., Singleton, P., 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 breat tumor cell invasion. J. Biol. Chem. 279, 26991-27007.
9. Boussouar, F. and Benahmed, M. (1999). Epidermal growth factor regulates glucose metabolism through lactate dehydrogenase a messenger ribonucleic acid expression in cultured porcine Sertoli cells. Biol. Repro. 61, 1139-1145.
10. Cantalupo, G., Alifano, P., Roberti, V., Bruni, C. B. and Bucci, C. (2001). Rab-interacting lysosomal protein (RILP): the Rab7 effector required for transport to lysosomes. EMBO J. 20, 683-693.
11. Colella, R. and Casey, S. F. (2003). Decreased activity of cathepsins L + B and decreased invasive ability of PC3 prostate cancer cells. Biotech. Histochem. 78, 101-108.
12. Colella, R., Jackson, T. and Goodwyn, E. (2004). Matrigel invasion by the prostate cancer cell lines, PC3 and DU145, and cathepsin L+B activity. Biotech. Histochem. 79, 121-127.
13. Coleman, D. T., Bigelow, R. and Cardelli, J. A. (2009). Inhibition of fatty acid synthase by luteolin post-transcriptionally down-regulates c-Met expression independent of proteosomal/lysosomal degradation. Mol. Cancer Ther. 8, 214-224.
14. Cordonnier, M.-N., Dauzonne, D., Louvard, D. and Coudrier, E. (2001). Actin filaments and myosin I alpha cooperate with microtubules for the movement of lysosomes. Mol. Biol. Cell 12, 4013-4029.
15. + exchanger inhibitors on subcellular localisation of endocytic organelles and intracellular dynamics of protein trandsuction domains HIV-TAT peptide and octaarginine. J. Control. Release 116, 247-254.
16. Gentile, A., Trusolino, L. and Comoglio, P. M. (2008). The Met tyrosine kinase receptor in development and cancer. Cancer Met. Rev. 27, 85-94.
17. 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.
18. + exchange and growth factor-induced cytosolic pH changes. Role in cellular proliferation. Biochem. Biophys. Acta 988, 73-97.
19. + antiporter in the etiopathogenesis and treatment of cancer. Two faces of the same coin - one single nature. Biochem. Biophys. Acta 1756, 1-24.
20. Hsu, P. and Sabatini, D. M. (2008). Cancer cell metabolism: Warburg and beyond. Cell 134, 703-707.
21. Johansson, M., Lehto, M., Tanhuanpaa, K., Cover, T. L. and Olkkonen, V. M. (2005). The oxysterol-binding protein homologue ORP1L interacts with Rab7 and alters functional properties of late endocytic compartments. Mol. Biol. Cell 16, 5480-5492.
22. Johansson, M., Rocha, N., Zwart, W., Jordens, I., Janssen, L., Kuijl, C., Olkkonen, V. M. and Neefjes, J. (2007). Activation of endosomal dynein motors by stepwise assembly of Rab7-RILP-p150Glued, ORP1L, and the receptor {beta}lll spectrin. J. Cell Biol. 176, 459-471.
23. Jordens, I., Fernandez-Borja, M., Marsman, M., Dusseljee, S., Janssen, L., Calafat, J., Janssen, H., Wubbolts, R. and Neefjes, J. (2001). The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors. Curr. Biol. 11, 1680-1685.
24. Joyce, J. A. and Pollard, J. W. (2009). Microenvironmental regulation of metastasis. Nat. Rev. Cancer 9, 239-252.
25. + exchanger by hepatocyte growth factor in hepatocytes. Hepatology 22, 629-636.
26. 3 exchange in NIH-3T3 fibroblasts. J. Biol. Chem. 269, 4116-4124.
27. Kaplan, O., Firon, M., Vivi, A., Navon, G. and Tsarfaty, I. (2000). HGF/SF activates glycolysis and oxidative phosphorylation in DA3 murine mammary cancer cells. Neoplasia 2, 365-377.
28. Koblinski, J. E., Ahram, M. and Sloane, B. F. (2000). Unraveling the role of proteases in cancer. Clin. Chim. Acta 291, 113-135.
29. Levayer, R. and Lecuit, T. (2008). Breaking down EMT. Nat. Cell Biol. 10, 757-759.
30. Mantovani, A., Schioppa, T., Porta, C., Allavena, P. and Sica, A. (2006). Role of tumor-associated macrophages in tumor progression and invasion. Cancer Met. Rev. 25, 315-322.
31. Martinez-Zaguilan, R., Seftor, E. A., Seftor, R. E. B., Chu, Y., Gillies, R. J. and Hendrix, M. J. C. (1996). Acidic pH enhances the invasive behavior of human melanoma cells. Clin. Exp. Metastasis 14, 176-186.
32. + exchanger. Eur. J. Med. Chem. 38, 547-554.
33. Matsumoto, K. and Nakamura, T. (2006). Hepatocyte growth factor and the Met system as a mediator of tumor-stromal interactions. Int. J. Cancer 119, 477-483.
34. Matteoni, R. and Kreis, T. E. (1987). Translocation and clustering of endosomes and lysosomes depends on microtubules. J. Cell Biol. 105, 1253-1265.
35. Milligan, S. A., Burke, P., Coleman, D. T., Bigelow, R. L., Steffan, J. J., Carroll, J. L., Williams, B. J. and Cardelli, J. A. (2009). The green tea polyphenol EGCG potentiates the antiproliferative activity of c-Met and epidermal growth factor receptor inhibitors in non-small cell lung cancer cells. Clin. Cancer Res. 15, 4885-4894.
36. Moellering, R., Black, K., Krishnamurty, C., Baggett, B. K., Stafford, P., Rain, M., Gatenby, R. A. and Gillies, R. J. (2008). Acid treatment of melanoma cells selects for invasive phenotypes. Clin. Exp. Metastasis 25, 411-425.
37. Nomura, T. and Katunuma, N. (2005). Involvement of cathepsins in the invasion, metastasis and proliferation of cancer cells. J. Med. Invest. 52, 1-9.
38. Orian-Rousseau, V., Chen, L., Sleeman, J. P., Herrlich, P. and Ponta, H. (2002). CD44 is required for two consecutive steps in HGF/c-Met signaling. Genes Dev. 16, 3074-3086.
39. Orian-Rousseau, V., Morrison, H., Matzke, A., Kastilan, T., Pace, G., Herrlich, P. and Ponta, H. (2007). Hepatocyte growth factor-induced Ras activation requires ERM proteins linked to both CD44v6 and F-actin. Mol. Biol. Cell 18, 76-83.
40. + exhanger-1 induces cytoskeletal changes involving reciprocal RhoA and Rac1 signaling, resulting in motility and invasion in MDA-MB-435 cells. Breast Cancer Res. 6, R616-R628.
41. Pennacchietti, S., Michieli, P., Galluzzo, M., Mazzone, M., Giordano, S. and Comoglio, P. M. (2003). Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene. Cancer Cell 3, 347-361.
42. Perdomo, G., Martinez-Brocca, M. A., Bhatt, B. A., Brown, N. F., O'Doherty, R. M. and Garcia-Ocana, A. (2008). Hepatocyte growth factor is a novel stimulator of glucose uptake and metabolism in skeletal muscle cells. J. Biol. Chem. 283, 13700-13706.
43. Progida, C., Malerod, L., Stuffers, S., Brech, A., Bucci, C. and Stenmark, H. (2007). RILP is required for the proper morphology and function of late endosomes. J. Cell Sci. 120, 3729-3737.
44. + exchanger, NHE1: structure, regulation, and cellular actions. Annu. Rev. Pharmacol. Toxicol. 42, 527-552.
45. Rempel, S. A., Rosenblum, M. L., Mikkelsen, T., Yan, P.-S., Ellis, K. D., Golembieski, W. A., Sameni, M., Rozhin, J., Ziegler, G. and Sloane, B. F. (1994). Cathepsin B expression and localization in glioma progression and invasion. Cancer Res. 54, 6027-6031.
46. + exchanger-dependent intracellular alkalinization is an early event in malignant transformation and plays an essential role in the development of subsequent transformation-associated phenotypes. FASEB J. 14, 2185-2197.
47. Rocha, N., Kuijl, C., van der Kant, R., Janssen, L., Houben, D., Janssen, H., Zwart, W. and Neefjes, J. (2009). Cholesterol sensor ORP1L contacts the ER protein VAP to control Rab7-RILP-p150Glued and late endosome positioning. J. Cell Biol. 185, 1209-1225.
48. Rozhin, J., Sameni, M., Ziegler, G. H. and Sloane, B. F. (1994). Pericellular pH affects distribution and secretion of cathepsin b in malignant cells. Cancer Res. 54, 6517-6525.
49. Sawada, K., Radjabi, A. R., Shinomiya, N., Kistner, E., Kenny, H., Becker, A. R., Turkyilmaz, M. A., Salgia, R., Yamada, S. D., Vande Woude, G. F. et al. (2007). c-Met overexpression is a prognostic factor in ovarian cancer and an effective target for inhibition of peritoneal dissemination and invasion. Cancer Res. 67, 1670-1679.
50. Singh, S., Sadanandam, A. and Singh, R. (2007). Chemokines in tumor angiogenesis and metastasis. Cancer Met. Rev. 26, 453-467.
51. Singleton, P. A., Salgia, R., Moreno-Vinasco, L., Moitra, J., Sammani, S., Mirzapoiazova, T. and Garcia, J. G. N. (2007). CD44 regulates hepatocyte growth factor-mediated vascular integrity. J. Biol. Chem. 282, 30643-30657.
52. Steffan, J. J. and Cardelli, J. A. (2010). Thiazolidinediones induce Rab7-RILP-MAPK-dependent juxtanuclear lysosome aggregation and reduce tumor cell invasion. Traffic 11, 274-286.
53. + exchangers and RhoA regulate acidic extracellular pH-induced lysosome trafficking in prostate cancer cells. Traffic 10, 737-753.
54. Stock, C. and Schwab, A. (2006). Role of the Na/H exchanger NHE1 in cell migration. Acta Physiol. 187, 149-157.
55. + exchange activity. Hepatology 22, 588-597.
56. Swanson, J., Locke, A., Ansel, P. and Hollenbeck, P. (1992). Radial movement of lysosomes along microtubules in permeabilized macrophages. J. Cell Sci. 103, 201-209.
57. Taniguchi, K., Yonemura, Y., Nojima, N., Hirono, Y., Fushida, S., Fujimura, T., Miwa, K., Endo, Y., Yamamoto, H. and Watanabe, H. (1998). The relation between the growth patterns of gastric carcinoma and the expression of hepatocyte growth factor receptor (c-met), autocrine motility factor receptor, and urokinase-type plasminogen activator receptor. Cancer 82, 2112-2122.
58. Tsuji, T., Ibaragi, S. and Hu, G. (2009). Epithelial-mesenchymal transition and cell cooperativity in metastasis. Cancer Res. 69, 7135-7139.
59. Tu, C., Ortega-Cava, C. F., Chen, G., Fernandes, N. D., Cavallo-Medved, D., Sloane, B. F., Band, V. and Band, H. (2008). Lysosomal cathepsin B participates in the podosome-mediated extracellular matrix degradation and invasion via secreted lysosomes in v-Src fibroblasts. Cancer Res. 68, 9147-9156.
60. Turturro, F., Friday, E., Fowler, R., Surie, D. and Welbourne, T. (2004). Troglitazone acts on cellular pH and DNA synthesis through a peroxisome proliferator-activated receptor {gamma}-independent mechanism in breast cancer-derived cell lines. Clin. Cancer Res. 10, 7022-7030.
61. + pump activity as a potential target via distinct signaling mechanisms. Glia 39, 10-18.
62. Wang, T. and Hong, W. (2006). RILP interacts with VPS22 and VPS36 of ESCRT-II and regulates their membrane recruitment. Biochem. Biophys. Res. Commun. 350, 413-423.
63. Yilmaz, M. and Christofori, G. (2009). EMT, the cytoskeleton, and cancer cell invasion. Cancer Met. Rev. 28, 15-33.