Characterization of carbonic anhydrase ix interactome reveals proteins assisting its nuclear localization in hypoxic cells(393 views) Buanne P, Renzone G, Monteleone F, Vitale M, Monti SM, Sandomenico A, Garbi C, Montanaro D, Accardo M, Troncone G, Zatovicova M, Csaderova L, Supuran CT, Pastorekova S, Scaloni A, De Simone G, Zambrano N
J Proteome Res (ISSN: 1535-3893), 2013 Jan; 12(1): 282-292.
Keywords: Arm Repeat, Cancer, Heat Repeat, Hypoxia, Nuclear Export Signal, Nuclear Localization Signal, Carbonate Dehydratase Ix, Exportin 1, Karyopherin, Ubiquitin Protein Ligase, Article, Carboxy Terminal Sequence, Cell Nucleus, Cell Strain Hek293, Cell Surface, Cellular Distribution, Complex Formation, Cytoplasm, Down Regulation, Enzyme Analysis, Enzyme Binding, Enzyme Stability, Gene Overexpression, Genetic Transcription, Human, Hypoxic Cell, Kidney Carcinoma, Kidney Cell, Nucleotide Sequence, Priority Journal, Protein Domain, Protein Function, Protein Localization, Protein Phosphorylation, Protein Protein Interaction, Protein Stability, Protein Targeting, Antigens, Neoplasm, Carbonic Anhydrases, Renal Cell, Cell Hypoxia, Hek293 Cells, Protein Interaction Maps, Transcription Factors,
Affiliations: *** IBB - CNR ***
CEINGE Biotecnologie Avanzate SCaRL, Naples, Italy
Proteomics and Mass Spectrometry Laboratory, ISPAAM, CNR, Naples, Italy
Dipartimento di Medicina Molecolare e Biotecnologie Mediche, Universitä di Napoli Federico II, Italy
Istituto di Biostrutture e Bioimmagini, CNR, Naples, Italy
Dipartimento di Biologia e Patologia Cellulare e Molecolare, Universitä di Napoli Federico II, Italy
Department of Public Health, Section of Pathology, Seconda Universitä di Napoli, Italy
Dipartimento di Scienze Biomorfologiche e Funzionali, Universitä di Napoli Federico II, Italy
Department of Molecular Medicine, Institute of Virology, Slovak Academy of Sciences, Bratislava, Slovakia
Laboratorio di Chimica Bioinorganica, Universitä di Firenze, Italy
References: Supuran, C.T., Carbonic anhydrases: Novel therapeutic applications for inhibitors and activators (2008) Nat Rev. Drug Discov., 7 (2), pp. 168-18
Pastorek, J., Pastorekova, S., Callebaut, I., Mornon, J.P., Zelnik, V., Opavsky, R., Zat'ovicova, M., Stanbridge, E.J., Cloning and characterization of MN, a human tumorassociated protein with a domain homologous to carbonic anhydrase and a putative helix-loop-helix DNA binding segment (1994) Oncogene, 9 (10), pp. 2877-2888
Opavsky, R., Pastorekova, S., Zelnik, V., Gibadulinova, A., Stanbridge, E.J., Zavada, J., Kettmann, R., Pastorek, J., Human MN/CA9 gene, a novel member of the carbonic anhydrase family: Structure and exon to protein domain relationships (1996) Genomics, 33 (3), pp. 480-487
Hilvo, M., Baranauskiene, L., Salzano, A.M., Scaloni, A., Matulis, D., Innocenti, A., Scozzafava, A., Parkkila, S., Biochemical characterization of CA IX, one of the most active carbonic anhydrase isozymes (2008) J. Biol. Chem., 283 (41), pp. 27799-27809
Alterio, V., Hilvo, M., Di Fiore, A., Supuran, C.T., Pan, P., Parkkila, S., Scaloni, A., De Simone, G., Crystal structure of the catalytic domain of the tumor-associated human carbonic anhydrase IX (2009) Proc. Natl. Acad. Sci. U.S.A., 106 (38), pp. 16233-16238
Wykoff, C.C., Beasley, N.J., Watson, P.H., Turner, K.J., Pastorek, J., Sibtain, A., Wilson, G.D., Harris, A.L., Hypoxiainducible expression of tumor-associated carbonic anhydrases (2000) Cancer Res., 60 (24), pp. 7075-7083
Potter, C.P., Harris, A.L., Diagnostic, prognostic and therapeutic implications of carbonic anhydrases in cancer (2003) Br. J. Cancer, 89 (1), pp. 2-7
Svastova, E., Hulikova, A., Rafajova, M., Zat'ovicova, M., Gibadulinova, A., Casini, A., Cecchi, A., Pastorekova, S., Hypoxia activates the capacity of tumor-associated carbonic anhydrase IX to acidify extracellular pH (2004) FEBS Lett., 577 (3), pp. 439-445
Svastova, E., Witarski, W., Csaderova, L., Kosik, I., Skvarkova, L., Hulikova, A., Zatovicova, M., Pastorekova, S., Carbonic anhydrase IX interacts with bicarbonate transporters in lamellipodia and increases cell migration via its catalytic domain (2012) J. Biol. Chem., 287 (5), pp. 3392-3402
Swietach, P., Patiar, S., Supuran, C.T., Harris, A.L., Vaughan-Jones, R.D., The role of carbonic anhydrase 9 in regulating extracellular and intracellular ph in three-dimensional tumor cell growths (2009) J. Biol. Chem., 284 (30), pp. 20299-20310
Pastorekova, S., Parkkila, S., Zavada, J., Tumor-associated carbonic anhydrases and their clinical significance (2006) Adv. Clin. Chem., 42, pp. 167-216
Monti, S.M., Supuran, C.T., De Simone, G., Carbonic anhydrase IX as a target for designing novel anticancer drugs (2012) Curr. Med. Chem., 19 (6), pp. 821-830
Pastorekova, S., Zatovicova, M., Pastorek, J., Cancer-associated carbonic anhydrases and their inhibition (2008) Curr. Pharm. Des., 14 (7), pp. 685-698
Svastova, E., Zilka, N., Zat'ovicova, M., Gibadulinova, A., Ciampor, F., Pastorek, J., Pastorekova, S., Carbonic anhydrase IX reduces E-cadherin-mediated adhesion of MDCK cells via interaction with beta-catenin (2003) Exp. Cell Res., 290 (2), pp. 332-345
Zavadova, Z., Zavada, J., Carbonic anhydrase IX (CA IX) mediates tumor cell interactions with microenvironment (2005) Oncol. Rep., 13 (5), pp. 977-982
Zavada, J., Zavadova, Z., Pastorek, J., Biesova, Z., Jezek, J., Velek, J., Human tumour-associated cell adhesion protein MN/CA IX: Identification of M75 epitope and of the region mediating cell adhesion (2000) Br. J. Cancer, 82 (11), pp. 1808-1813
Ditte, P., Dequiedt, F., Svastova, E., Hulikova, A., Ohradanova-Repic, A., Zatovicova, M., Csaderova, L., Pastorek, J., Phosphorylation of carbonic anhydrase IX controls its ability to mediate extracellular acidification in hypoxic tumors (2011) Cancer Res., 71 (24), pp. 7558-7567
Dorai, T., Sawczuk, I.S., Pastorek, J., Wiernik, P.H., Dutcher, J.P., The role of carbonic anhydrase IX overexpression in kidney cancer (2005) Eur. J. Cancer, 41 (18), pp. 2935-2947
Caratu, G., Allegra, D., Bimonte, M., Schiattarella, G.G., D'ambrosio, C., Scaloni, A., Napolitano, M., Zambrano, N., Identification of the ligands of protein interaction domains through a functional approach (2007) Mol. Cell. Proteomics, 6 (2), pp. 333-345
Shevchenko, A., Wilm, M., Vorm, O., Mann, M., Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels (1996) Anal. Chem., 68 (5), pp. 850-858
Gallo, G., Renzone, G., Alduina, R., Stegmann, E., Weber, T., Lantz, A.E., Thykaer, J., Puglia, A.M., Differential proteomic analysis reveals novel links between primary metabolism and antibiotic production in Amycolatopsis balhimycina (2010) Proteomics, 10 (7), pp. 1336-1358
Vitale, M., Renzone, G., Matsuda, S., Scaloni, A., D'adamio, L., Zambrano, N., Proteomic characterization of a mouse model of familial danish dementia (2012) J. Biomed. Biotechnol., p. 728178
Picariello, G., Ferranti, P., Mamone, G., Roepstorff, P., Addeo, F., Identification of N-linked glycoproteins in human milk by hydrophilic interaction liquid chromatography and mass spectrometry (2008) Proteomics, 8 (18), pp. 3833-3847
D'ambrosio, C., Arena, S., Salzano, A.M., Renzone, G., Ledda, L., Scaloni, A., A proteomic characterization of water buffalo milk fractions describing PTM of major species and the identification of minor components involved in nutrient delivery and defense against pathogens (2008) Proteomics, 8 (17), pp. 3657-3666
Arena, S., Renzone, G., Novi, G., Paffetti, A., Bernardini, G., Santucci, A., Scaloni, A., Modern proteomic methodologies for the characterization of lactosylation protein targets in milk (2010) Proteomics, 10 (19), pp. 3414-3434
Szklarczyk, D., Franceschini, A., Kuhn, M., Simonovic, M., Roth, A., Minguez, P., Doerks, T., Von Mering, C., The STRING database in 2011: Functional interaction networks of proteins, globally integrated and scored (2011) Nucleic Acids Res., 39, pp. D561-D568
Huang Da, W., Sherman, B.T., Lempicki, R.A., Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources (2009) Nat. Protoc., 4 (1), pp. 44-57
Zat'ovicova, M., Tarabkova, K., Svastova, E., Gibadulinova, A., Mucha, V., Jakubickova, L., Biesova, Z., Pastorekova, S., Monoclonal antibodies generated in carbonic anhydrase IX-deficient mice recognize different domains of tumourassociated hypoxia-induced carbonic anhydrase IX (2003) J. Immunol. Methods, 282 (1-2), pp. 117-134
Fields, G.B., Noble, R.L., Solid phase peptide synthesis utilizing 9-fluorenylmethoxycarbonyl amino acids (1990) Int. J. Pept. Protein Res., 35 (3), pp. 161-214
Prigent, M., Barlat, I., Langen, H., Dargemont, C., IkappaBalpha and IkappaBalpha /NF-kappa B complexes are retained in the cytoplasm through interaction with a novel partner, RasGAP SH3-binding protein 2 (2000) J. Biol. Chem., 275 (46), pp. 36441-36449
Andrade, M.A., Petosa, C., O'donoghue, S.I., Muller, C.W., Bork, P., Comparison of ARM and HEAT protein repeats (2001) J. Mol. Biol., 309 (1), pp. 1-18
Henderson, B.R., Eleftheriou, A., A comparison of the activity, sequence specificity, and CRM1-dependence of different nuclear export signals (2000) Exp. Cell Res., 256 (1), pp. 213-224
Lee, B.J., Cansizoglu, A.E., Suel, K.E., Louis, T.H., Zhang, Z., Chook, Y.M., Rules for nuclear localization sequence recognition by karyopherin beta 2 (2006) Cell, 126 (3), pp. 543-558
Swinson, D.E., Jones, J.L., Richardson, D., Wykoff, C., Turley, H., Pastorek, J., Taub, N., O'byrne, K.J., Carbonic anhydrase IX expression, a novel surrogate marker of tumor hypoxia, is associated with a poor prognosis in non-small-cell lung cancer (2003) J. Clin. Oncol., 21 (3), pp. 473-482
Dungwa, J.V., Hunt, L.P., Ramani, P., Carbonic anhydrase IX up-regulation is associated with adverse clinicopathologic and biologic factors in neuroblastomas (2012) Hum. Pathol., 43 (10), pp. 1651-1660
Bikkavilli, R.K., Malbon, C.C., Wnt3a-stimulated LRP6 phosphorylation is dependent upon arginine methylation of G3BP2 (2012) J. Cell Sci., 125 (10), pp. 2446-2456
Campbell, M.G., Karbstein, K., Protein-protein interactions within late pre-40S ribosomes (2011) PLoS One, 6 (1), pp. e16194
Lee, J.E., Sweredoski, M.J., Graham, R.L., Kolawa, N.J., Smith, G.T., Hess, S., Deshaies, R.J., The steady-state repertoire of human SCF ubiquitin ligase complexes does not require ongoing Nedd8 conjugation (2011) Mol. Cell. Proteomics, 10 (5), pp. M110006460
Giri, D.K., Ali-Seyed, M., Li, L.Y., Lee, D.F., Ling, P., Bartholomeusz, G., Wang, S.C., Hung, M.C., Endosomal transport of ErbB-2: Mechanism for nuclear entry of the cell surface receptor (2005) Mol. Cell. Biol., 25 (24), pp. 11005-11018
Bryant, D.M., Stow, J.L., Nuclear translocation of cell-surface receptors: Lessons from fibroblast growth factor (2005) Traffic, 6 (10), pp. 947-954
Janiszewska, M., De Vito, C., Le Bitoux, M.A., Fusco, C., Stamenkovic, I., Transportin regulates nuclear import of CD44 (2010) J. Biol. Chem., 285 (40), pp. 30548-30557
Zatovicova, M., Jelenska, L., Hulikova, A., Csaderova, L., Ditte, Z., Ditte, P., Goliasova, T., Pastorekova, S., Carbonic anhydrase IX as an anticancer therapy target: Preclinical evaluation of internalizing monoclonal antibody directed to catalytic domain (2010) Curr. Pharm. Des., 16 (29), pp. 3255-3263
Makino, Y., Yogosawa, S., Kayukawa, K., Coin, F., Egly, J.M., Wang, Z., Roeder, R.G., Tamura, T., TATA-Binding protein-interacting protein 120, TIP120, stimulates three classes of eukaryotic transcription via a unique mechanism (1999) Mol. Cell. Biol., 19 (12), pp. 7951-7960
Aoki, T., Okada, N., Wakamatsu, T., Tamura, T.A., TBPinteracting protein 120B, which is induced in relation to myogenesis, binds to NOT3 (2002) Biochem. Biophys. Res. Commun., 296 (5), pp. 1097-1103
Shiraishi, S., Zhou, C., Aoki, T., Sato, N., Chiba, T., Tanaka, K., Yoshida, S., Tamura, T.A., TBP-interacting protein 120B (TIP120B)/cullin-associated and neddylation-dissociated 2 (CAND2) inhibits SCF-dependent ubiquitination of myogenin and accelerates myogenic differentiation (2007) J. Biol. Chem., 282 (12), pp. 9017-9028
Turner, J.G., Dawson, J., Sullivan, D.M., Nuclear export of proteins and drug resistance in cancer (2012) Biochem. Pharmacol., 83 (8), pp. 1021-1032
Zemp, I., Kutay, U., Nuclear export and cytoplasmic maturation of ribosomal subunits (2007) FEBS Lett., 581 (15), pp. 2783-2793
Groulx, I., Lee, S., Oxygen-dependent ubiquitination and degradation of hypoxia-inducible factor requires nuclear-cytoplasmic trafficking of the von Hippel-Lindau tumor suppressor protein (2002) Mol. Cell. Biol., 22 (15), pp. 5319-5336
Steinhoff, A., Pientka, F.K., Mockel, S., Kettelhake, A., Hartmann, E., Kohler, M., Depping, R., Cellular oxygen sensing: Importins and exportins are mediators of intracellular localisation of prolyl-4-hydroxylases PHD1 and PHD2 (2009) Biochem. Biophys. Res. Commun., 387 (4), pp. 705-711
Mylonis, I., Chachami, G., Samiotaki, M., Panayotou, G., Paraskeva, E., Kalousi, A., Georgatsou, E., Simos, G., Identification of MAPK phosphorylation sites and their role in the localization and activity of hypoxia-inducible factor-1alpha (2006) J. Biol. Chem., 281 (44), pp. 33095-33106
Koritzinsky, M., Wouters, B.G., Hypoxia and regulation of messenger RNA translation (2007) Methods Enzymol., 435, pp. 247-273
Supuran, C. T., Carbonic anhydrases: Novel therapeutic applications for inhibitors and activators (2008) Nat Rev. Drug Discov., 7 (2), pp. 168-18
Wykoff, C. C., Beasley, N. J., Watson, P. H., Turner, K. J., Pastorek, J., Sibtain, A., Wilson, G. D., Harris, A. L., Hypoxiainducible expression of tumor-associated carbonic anhydrases (2000) Cancer Res., 60 (24), pp. 7075-7083
Potter, C. P., Harris, A. L., Diagnostic, prognostic and therapeutic implications of carbonic anhydrases in cancer (2003) Br. J. Cancer, 89 (1), pp. 2-7
Monti, S. M., Supuran, C. T., De Simone, G., Carbonic anhydrase IX as a target for designing novel anticancer drugs (2012) Curr. Med. Chem., 19 (6), pp. 821-830
Fields, G. B., Noble, R. L., Solid phase peptide synthesis utilizing 9-fluorenylmethoxycarbonyl amino acids (1990) Int. J. Pept. Protein Res., 35 (3), pp. 161-214
Andrade, M. A., Petosa, C., O'donoghue, S. I., Muller, C. W., Bork, P., Comparison of ARM and HEAT protein repeats (2001) J. Mol. Biol., 309 (1), pp. 1-18
Henderson, B. R., Eleftheriou, A., A comparison of the activity, sequence specificity, and CRM1-dependence of different nuclear export signals (2000) Exp. Cell Res., 256 (1), pp. 213-224
Lee, B. J., Cansizoglu, A. E., Suel, K. E., Louis, T. H., Zhang, Z., Chook, Y. M., Rules for nuclear localization sequence recognition by karyopherin beta 2 (2006) Cell, 126 (3), pp. 543-558
Swinson, D. E., Jones, J. L., Richardson, D., Wykoff, C., Turley, H., Pastorek, J., Taub, N., O'byrne, K. J., Carbonic anhydrase IX expression, a novel surrogate marker of tumor hypoxia, is associated with a poor prognosis in non-small-cell lung cancer (2003) J. Clin. Oncol., 21 (3), pp. 473-482
Dungwa, J. V., Hunt, L. P., Ramani, P., Carbonic anhydrase IX up-regulation is associated with adverse clinicopathologic and biologic factors in neuroblastomas (2012) Hum. Pathol., 43 (10), pp. 1651-1660
Bikkavilli, R. K., Malbon, C. C., Wnt3a-stimulated LRP6 phosphorylation is dependent upon arginine methylation of G3BP2 (2012) J. Cell Sci., 125 (10), pp. 2446-2456
Campbell, M. G., Karbstein, K., Protein-protein interactions within late pre-40S ribosomes (2011) PLoS One, 6 (1), pp. e16194
Lee, J. E., Sweredoski, M. J., Graham, R. L., Kolawa, N. J., Smith, G. T., Hess, S., Deshaies, R. J., The steady-state repertoire of human SCF ubiquitin ligase complexes does not require ongoing Nedd8 conjugation (2011) Mol. Cell. Proteomics, 10 (5), pp. M110006460
Giri, D. K., Ali-Seyed, M., Li, L. Y., Lee, D. F., Ling, P., Bartholomeusz, G., Wang, S. C., Hung, M. C., Endosomal transport of ErbB-2: Mechanism for nuclear entry of the cell surface receptor (2005) Mol. Cell. Biol., 25 (24), pp. 11005-11018
Bryant, D. M., Stow, J. L., Nuclear translocation of cell-surface receptors: Lessons from fibroblast growth factor (2005) Traffic, 6 (10), pp. 947-954
Duda, D. M., Scott, D. C., Calabrese, M. F., Zimmerman, E. S., Zheng, N., Schulman, B. A., Structural regulation of cullin-RING ubiquitin ligase complexes (2011) Curr. Opin. Struct. Biol., 21 (2), pp. 257-264
Turner, J. G., Dawson, J., Sullivan, D. M., Nuclear export of proteins and drug resistance in cancer (2012) Biochem. Pharmacol., 83 (8), pp. 1021-1032
Characterization of carbonic anhydrase ix interactome reveals proteins assisting its nuclear localization in hypoxic cells