The plasma membrane sialidase NEU3 regulates the malignancy of renal carcinoma cells by controlling β1 integrin internalization and recycling

Journal of Biological Chemistry

Volumn 287, Issue 51, 2012, Pages 42835-42845

  Tringali, Cristina ^a   Lupo, Barbara ^a   Silvestri, Ilaria ^a   Papini, Nadia ^a   Anastasia, Luigi ^b,c   Tettamanti, Guido ^c   Venerando, Bruno ^a,c  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c IRCCS POLICLINICO SAN DONATO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHAGY; CELL SURFACES; DOWN-REGULATION; DRUG RESISTANCE; EPIDERMAL GROWTH FACTOR RECEPTORS; FOCAL ADHESION KINASE; INTEGRINS; INTRACELLULAR CHANNEL; KEY ENZYMES; KEY REGULATORS; METALLOPROTEINASES; METASTATIC POTENTIAL; RAS-RELATED PROTEINS; RECYCLING PATHWAYS; RENAL CARCINOMA CELLS; RENAL CELL; SIALIDASES;

ADHESION; CELL DEATH; CELL MEMBRANES; CHLORINE COMPOUNDS; ENZYMES; GLYCOPROTEINS; MOLECULAR BIOLOGY; PROTEINS;

RECYCLING;

BETA1 INTEGRIN; CASPASE 3; CHLORIDE INTRACELLULAR CHANNEL PROTEIN 3; COLLAGEN TYPE 1; EPIDERMAL GROWTH FACTOR RECEPTOR; FIBRONECTIN; FOCAL ADHESION KINASE; GELATINASE A; GELATINASE B; INTERSTITIAL COLLAGENASE; MATRILYSIN; MEMBRANE PROTEIN; MESSENGER RNA; PROTEIN BAX; PROTEIN BCL 2; PROTEIN KINASE B; PROTEIN NEU3; RAB PROTEIN; RAB25 PROTEIN; SIALIDASE; UNCLASSIFIED DRUG;

ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; DOWN REGULATION; DRUG RESISTANCE; ENDOCYTOSIS; ENZYME ACTIVATION; GENE SILENCING; HUMAN; HUMAN CELL; INTERNALIZATION; INTRACELLULAR SIGNALING; KIDNEY CARCINOMA; METASTASIS POTENTIAL; MOLECULAR PATHOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS REGULATION; UPREGULATION;

ANTIGENS, CD29; CARCINOMA, RENAL CELL; CELL ADHESION; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL MEMBRANE; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; ENDOCYTOSIS; FOCAL ADHESION KINASE 1; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; GLYCOSPHINGOLIPIDS; HUMANS; KIDNEY NEOPLASMS; MATRIX METALLOPROTEINASE 1; MATRIX METALLOPROTEINASE 7; NEOPLASM INVASIVENESS; NEURAMINIDASE; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 84871110223     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.407718     Document Type: Article

References (42)

1. Cairns, P. (2010) Renal cell carcinoma. Cancer Biomark 9, 461-473
2. Finley, D. S., Pantuck, A. J., and Belldegrun, A. S. (2011) Tumor biology and prognostic factors in renal cell carcinoma. Oncologist 16, Suppl. 2, 4-13
3. Li, L., and Kaelin, W. G., Jr. (2011) New insights into the biology of renal cell carcinoma. Hematol. Oncol. Clin. North Am. 25, 667-686
4. Brenner, W., Greber, I., Gudejko-Thiel, J., Beitz, S., Schneider, E., Walenta, S., Peters, K., Unger, R., and Thüroff, J. W. (2008) Migration of renal carcinoma cells is dependent on protein kinase Cδ via β1 integrin and focal adhesion kinase. Int. J. Oncol. 32, 1125-1131
5. Hoon, D. S., Okun, E., Neuwirth, H., Morton, D. L., and Irie, R. F. (1993) Aberrant expression of gangliosides in human renal cell carcinomas. J. Urol. 150, 2013-2018
6. Senda, M., Ito, A., Tsuchida, A., Hagiwara, T., Kaneda, T., Nakamura, Y., Kasama, K., Kiso, M., Yoshikawa, K., Katagiri, Y., Ono, Y., Ogiso, M., Urano, T., Furukawa, K., Oshima, S., and Furukawa, K. (2007) Identification and expression of a sialyltransferase responsible for the synthesis of disialylgalactosylgloboside in normal and malignant kidney cells: downregulation of ST6GalNAc VI in renal cancers. Biochem. J. 402, 459-470
7. Biswas, S., Biswas, K., Richmond, A., Ko, J., Ghosh, S., Simmons, M., Rayman, P., Rini, B., Gill, I., Tannenbaum, C. S., and Finke, J. H. (2009) Elevated levels of select gangliosides in T cells from renal cell carcinoma patients is associated withTcell dysfunction. J. Immunol. 183, 5050-5058
8. Aoki, H., Satoh, M., Mitsuzuka, K., Ito, A., Saito, S., Funato, T., Endoh, M., Takahashi, T., and Arai, Y. (2004) Inhibition of motility and invasiveness of renal cell carcinoma induced by short interfering RNA transfection of β1,4GalNAc transferase. FEBS Lett. 567, 203-208
9. Ueno, S., Saito, S., Wada, T., Yamaguchi, K., Satoh, M., Arai, Y., and Miyagi, T. (2006) Plasma membrane-associated sialidase is up-regulated in renal cell carcinoma and promotes interleukin-6-induced apoptosis suppression and cell motility. J. Biol. Chem. 281, 7756-7764
10. Mandal, C., Tringali, C., Mondal, S., Anastasia, L., Chandra, S., Venerando, B., and Mandal, C. (2010) Down regulation of membrane-bound Neu3 constitutes a new potential marker for childhood acute lymphoblastic leukemia and induces apoptosis suppression of neoplastic cells. Int. J. Cancer 126, 337-349
11. Wada, T., Hata, K., Yamaguchi, K., Shiozaki, K., Koseki, K., Moriya, S., and Miyagi, T. (2007) A crucial role of plasma membrane-associated sialidase in the survival of human cancer cells. Oncogene 26, 2483-2490
12. Miyagi, T., Takahashi, K., Hata, K., Shiozaki, K., and Yamaguchi, K. (2012) Sialidase significance for cancer progression. Glycoconj. J. 29, 567-577
13. Tringali, C., Lupo, B., Cirillo, F., Papini, N., Anastasia, L., Lamorte, G., Colombi, P., Bresciani, R., Monti, E., Tettamanti, G., and Venerando, B. (2009) Silencing of membrane-associated sialidase Neu3 diminishes apoptosis resistance and triggers megakaryocytic differentiation of chronic myeloid leukemic cells K562 through the increase of ganglioside GM3. Cell Death Differ. 16, 164-174
14. Monti, E., Bassi, M. T., Papini, N., Riboni, M., Manzoni, M., Venerando, B., Croci, G., Preti, A., Ballabio, A., Tettamanti, G., and Borsani, G. (2000) Identification and expression of NEU3, a novel human sialidase associated to the plasma membrane. Biochem. J. 349, 343-351
15. Anastasia, L., Papini, N., Colazzo, F., Palazzolo, G., Tringali, C., Dileo, L., Piccoli, M., Conforti, E., Sitzia, C., Monti, E., Sampaolesi, M., Tettamanti, G., and Venerando, B. (2008) NEU3 sialidase strictly modulates GM3 levels in skeletal myoblasts C2C12 thus favoring their differentiation and protecting them from apoptosis. J. Biol. Chem. 283, 36265-36271
16. Miyagi, T., Wada, T., Yamaguchi, K., Hata, K., and Shiozaki, K. (2008) Plasma membrane-associated sialidase as a crucial regulator of transmembrane signalling. J Biochem. 144, 279-285
17. Sonnino, S., Nicolini, M., and Chigorno, V. (1996) Preparation of radiolabeled gangliosides. Glycobiology 6, 479-487
18. Steinberg, F., Heesom, K. J., Bass, M. D., and Cullen, P. J. (2012) SNX17 protects integrins from degradation by sorting between lysosomal and recycling pathways. J. Cell Biol. 197, 219-230
19. Papini, N., Anastasia, L., Tringali, C., Croci, G., Bresciani, R., Yamaguchi, K., Miyagi, T., Preti, A., Prinetti, A., Prioni, S., Sonnino, S., Tettamanti, G., Venerando, B., and Monti, E. (2004) The plasma membrane-associated sialidase MmNEU3 modifies the ganglioside pattern of adjacent cells supporting its involvement in cell-to-cell interactions. J. Biol. Chem. 279, 16989-16995
20. Sonnino, S., and Prinetti, A. (2010) Gangliosides as regulators of cell membrane organization and functions. Adv. Exp. Med. Biol. 688, 165-184
21. Hua, H., Li, M., Luo, T., Yin, Y., and Jiang, Y. (2011) Matrix metalloproteinases in tumorigenesis: an evolving paradigm. Cell Mol. Life Sci. 68, 3853-3868
22. Wang, F., Reierstad, S., and Fishman, D. A. (2006) Matrilysin over-expression in MCF-7 cells enhances cellular invasiveness and pro-gelatinase activation. Cancer Lett 236, 292-301
23. Mosesson, Y., Mills, G. B., and Yarden, Y. (2008) Derailed endocytosis: an emerging feature of cancer. Nat. Rev. Cancer 8, 835-850
24. Sonnino, S., and Prinetti, A. (2009) Sphingolipids and membrane environments for caveolin. FEBS Lett. 583, 597-606
25. Dozynkiewicz, M. A., Jamieson, N. B., Macpherson, I., Grindlay, J., van den Berghe, P. V., von Thun, A., Morton, J. P., Gourley, C., Timpson, P., Nixon, C., McKay, C. J., Carter, R., Strachan, D., Anderson, K., Sansom, O. J., Caswell, P. T., and Norman, J. C. (2012) Rab25 and CLIC3 collaborate to promote integrin recycling from late endosomes/lysosomes and drive cancer progression. Dev. Cell 22, 131-145
26. Wang, S., and Basson, M. D. (2011) Protein kinase B/AKT and focal adhesion kinase: two close signaling partners in cancer. Anticancer Agents Med. Chem. 11, 993-1002
27. Streuli, C. H., and Akhtar, N. (2009) Signal co-operation between integrins and other receptor systems. Biochem. J. 418, 491-506
28. Banumathy, G., and Cairns, P. (2010) Signaling pathways in renal cell carcinoma. Cancer Biol. Ther. 10, 658-664
29. Azim, H., Azim, H. A., Jr., and Escudier, B. (2010) Targeting mTOR in cancer: renal cell is just a beginning. Target Oncol. 5, 269-280
30. Wang, Y., Yamaguchi, K., Wada, T., Hata, K., Zhao, X., Fujimoto, T., and Miyagi, T. (2002) A close association of the ganglioside-specific sialidase Neu3 with caveolin in membrane microdomains. J. Biol. Chem. 277, 26252-26259
31. Rathinam, R., and Alahari, S. K. (2010) Important role of integrins in the cancer biology. Cancer Metastasis Rev. 29, 223-237
32. Schwartz, M. A., and Ginsberg, M. H. (2002) Networks and crosstalk: integrin signalling spreads. Nat. Cell Biol. 4, E65-68
33. Singh, R. D., Marks, D. L., Holicky, E. L., Wheatley, C. L., Kaptzan, T., Sato, S. B., Kobayashi, T., Ling, K., and Pagano, R. E. (2010) Gangliosides and β1-integrin are required for caveolae and membrane domains. Traffic 11, 348-360
34. Park, S. Y., Kwak, C. Y., Shayman, J. A., and Kim, J. H. (2012) Globoside promotes activation of ERK by interaction with the epidermal growth factor receptor. Biochim. Biophys. Acta 1820, 1141-1148
35. Zhao, J., and Guan, J. L. (2009) Signal transduction by focal adhesion kinase in cancer. Cancer Metastasis Rev. 28, 35-49
36. Saito, S., Orikasa, S., Satoh, M., Ohyama, C., Ito, A., and Takahashi, T. (1997) Expression of globo-series gangliosides in human renal cell carcinoma. Jpn. J. Cancer Res. 88, 652-659
37. Saito, S., Nojiri, H., Satoh, M., Ito, A., Ohyama, C., and Orikasa, S. (2000) Inverse relationship of expression between GM3 and globo-series ganglioside in human renal cell carcinoma. Tohoku J. Exp. Med. 190, 271-278
38. Mikhaylova, O., Stratton, Y., Hall, D., Kellner, E., Ehmer, B., Drew, A. F., Gallo, C. A., Plas, D. R., Biesiada, J., Meller, J., and Czyzyk-Krzeska, M. F. (2012) VHL-regulated MiR-204 suppresses tumor growth through inhibition of LC3B-mediated autophagy in renal clear cell carcinoma. Cancer Cell 21, 532-546
39. Hetz, C., and Glimcher, L. (2008) The daily job of night killers: alternative roles of the BCL-2 family in organelle physiology. Trends Cell Biol. 18, 38-44
40. Djavaheri-Mergny, M., Maiuri, M. C., and Kroemer, G. (2010) Cross talk between apoptosis and autophagy by caspase-mediated cleavage of Beclin 1. Oncogene 29, 1717-1719
41. Liang, X., De Vera, M. E., Buchser, W. J., Romo de Vivar Chavez, A., Loughran, P., Beer Stolz, D., Basse, P., Wang, T., Van Houten, B., Zeh, H. J., 3rd, and Lotze, M. T. (2012) Inhibiting Systemic Autophagy during Interleukin 2 Immunotherapy Promotes Long-term Tumor Regression. Cancer Res. 72, 2791-2801
42. Ramankulov, A., Lein, M., Johannsen, M., Schrader, M., Miller, K., and Jung, K. (2008) Plasma matrix metalloproteinase-7 as a metastatic marker and survival predictor in patients with renal cell carcinomas. Cancer Sci. 99, 1188-1194