Role of hypoxia and EGF on expression, activity, localization and phosphorylation of carbonic anhydrase IX in MDA-MB-231 breast cancer cells

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1813, Issue 1, 2011, Pages 159-167

  Li, Ying ^a   Wang, Hai ^a   Tu, Chingkuang ^a   Shiverick, Kathleen T ^a   Silverman, David N ^a   Frost, Susan C ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

Carbonic anydrase IX; Dimerization; EGF; Hypoxia; Lipid raft; MDA MB 231 breast cancer cell

Indexed keywords

CARBONATE DEHYDRATASE IX; EPIDERMAL GROWTH FACTOR; GLYCOPROTEIN; PROTEIN KINASE B; TYROSINE;

ARTICLE; BREAST CANCER; CANCER CELL; CELL MEMBRANE; CONTROLLED STUDY; HYPOXIA; LIPID RAFT; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION;

ANOXIA; ANTIGENS, NEOPLASM; BREAST NEOPLASMS; CARBONIC ANHYDRASES; CELL LINE, TUMOR; EPIDERMAL GROWTH FACTOR; FEMALE; GLYCOSYLATION; HUMANS; IMMUNOBLOTTING; MEMBRANE MICRODOMAINS; PHOSPHORYLATION; PROTEIN MULTIMERIZATION; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 78650750585     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2010.09.018     Document Type: Article

References (63)

1. Supuran C.T. Carbonic anhydrase: novel therapeutic applications for inhibitors and activators. Nat. Rev. 2008, 7:168.
2. Potter C.P.S., Harris A.L. Diagnostic, prognostic and therapeutic implications of carbonic anhydrases in cancer. Br. J. Cancer 2003, 89:2.
3. Ivanov S., Liao S.-Y., Ivanova A., Danilkovitch-Miagkova A., Tarasova N., Weirich G., Merrill M.J., Proescholdt M.A., Oldfield E.H., Lee J., Zavada J., Waheed A., Sly W., Lerman M.I., Stanbridge E.J. Expression of hypoxia-inducible cell-surface transmembrane carbonic anhydrases in human cancer. Am. J. Pathol. 2001, 158:905.
4. Pastorek J., Pastoreková S., Callebaut I., Mornon J.P., Zelník V., Opavsky R., Zat'ovicová M., Liao S., Portetelle D., Stanbridge E.J., Závada J., Burny A., Kettmann R. Cloning and characterization of MN, a human tumor-associated protein with a domain homologous to carbonic anhydrase and a putative helix-loop-helix DNA binding segment. Oncogene 1994, 9:2877.
5. Wingo T., Tu C., Laipis P.J., Silverman D.N. The catalytic properties of human carbonic anhydrase IX. Biochem. Biophys. Res. Commun. 2001, 288:666.
6. Bui M.H.T., Seligson D., Han K.R., Pantuck A.J., Dorey F.J., Huang Y., Horvath S., Leibovich B.C., Chopra S., Liao S.-Y., Stanbridge E., Lerman M.I., Palotie A., Figlin R.A., Belldegrun A.S. Carbonic anhydrase IX is an independent predictor of survival in advanced renal clear cell carcinoma: implication fro prognosis and therapy. Clin. Cancer Res. 2003, 9:802.
7. Chia S.K., Wykoff C.C., Watson P.H., Han C., Leek R.D., Pastorek J., Gatter K.C., Ratcliffe P., Harris A.L. Prognostic significance of a novel hypoxia-regulated marker, carbonic anhydrase IX, in invasive breast cancer. J. Clin. Oncol. 2005, 19:3660.
8. Hussain S.A., Palmer D.H., Ganesan R., Hiller L., Gregory J., Murray P.G., Pastorek J., Young L., James N.D. Carbonic anhydrase IX, a marker of hypoxia: correlation with clinical outcome in transitional cell carcinoma of the bladder. Oncol. Rep. 2004, 11:1005.
9. Loncaster J.A., Harris A.L., Davidson S.E., Logue J.P., Hunter R.D., Wykoff C.C., Pastorek J., Ratcliffe P.J., Stratford I.J., West C.M.L. Carbonic anhydrase (CAIX) expression, a potential new intrinsic marker of hypoxia: correlations with tumor oxygen measurements and prognosis in locally advanced carcinoma of the cervix. Cancer Res. 2001, 61:6394.
10. Swinson D.E.B., Jones J.L., Richardson D., Wykoff C., Turley H., Pastorek J., Taub N., Harris A.L., O'Bryne 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. J. Clin. Oncol. 2003, 21:473.
11. Pastorekova S., Parkkila S., Parkkila A., Opavsky R., Zelnik V., Saarnio J., Pastorek J. Carbonic anhydrase IX, MN/CAIX: analysis of stomach complementary DNA sequence and expression in human and rat alimentary tracts. Gastroenterology 1997, 112:398.
12. Saarnio J., Parkkila S., Parkkila A.-K., Waheed A., Casey M.C., Zhou X.Y., Pastoreková S., Pastorek J., Karttunen T., Haukipuro K., Kairaluoma M.I., Sly W.S. Immunohistochemistry of carbonic anhydrase isozyme IX (MN/CA IX) in human gut reveals polarized expression in epithelial cells with the highest proliferative capacity. J. Histochem. Cytochem. 1998, 46:497.
13. Hussain S.A., Ganesan R., Reynolds G., Gross L., Stevens A., Pastorek J., Murray P.G., Perunovic B., Anwar M.S., Billingham L., James N.D., Spooner D., Poole C.J., Rea D.W., Palmer D.H. Hypoxia-regulated carbonic anhydrase IX expression is associated with poor survival in patients with invasive breast cancer. Br. J. Cancer 2007, 96:104.
14. Li Y., Wang H., Oosterwijk E., Tu C., Shiverick K.T., Silverman D.N., Frost S.C. Expression and activity of carbonic anhydrase IX is associated with metabolic dysfunction in MDA-MB-231 breast cancer cells. Cancer Investig. 2009, 27:613.
15. Dubois L., Lieuwes N.G., Maresca A., Thiry A., Supuran C.T., Scozzafava A., Wouters B.G., Lambin P. Imaging of CA IX with fluorescent labelled sulfonamides distinguishes hypoxic and (re)-oxygenated cells in a xenograft tumour model. Radiother. Oncol. 2009, 92:423.
16. Chiche J., Ilc K., Laferriere J., Trottier E., Dayan F., Mazure N.M., Brahimi-Horn M.C., Pouyssegur J. Hypoxia-inducible carbonic anhydrase IX and XII promote tumor cell growth by counteracting acidosis through the regulation of the intracellular pH. Cancer Res. 2009, 69:358.
17. Svastova E., Hulikova A., Rafajova M., Zatovicova M., Gibadulinova A., Casini A., Cecchi A., Scozzafava A., Supuran C.T., Pastorek J., Pastorekova S. Hypoxia activates the capacity of tumor-associated carbonic anhydrase IX to acidify extracellular pH. FEBS Lett. 2004, 577:439.
18. +-ATPase. Proc. Natl Acad. Sci. USA 1995, 92:5965.
19. Stubbs M., McSheehy P.M.J., Griffiths J.R., Bashford C.L. Causes and consequences of tumour acidity and implications for treatment. Mol. Med. Today 2000, 6:15.
20. Gatenby R.A., Gillies R.J. Why do cancers have high aerobic glycolysis?. Nat. Rev. Cancer 2004, 4:891.
21. Gatenby R.A., Smallbone K., Maini P.K., Rose F., Averill J., Nagle R.B., Worrall L., Gillies R.J. Cellular adaptations to hypoxia and acidosis during somatic evolution of breast cancer. Br. J. Cancer 2007, 97:646.
22. Sorlie T., Perou C.M., Tibshirani R., Aas R., Geisler S., Johnsen H., Hastie T., Eisen M.B., van de Rijn M., Jeffrey S.S., Thorsen T., Quist H., Matese J.C., Brown P.O., Botstein D., Lonning P.E., Borrensen-Dale A. Gene Expression Patterns of Breast Carcinomas Distinguish Tumor Subclasses with Clinical Implications. Proc. Natl Acad. Sci. USA 2001, 98:10869.
23. Neve R.M., Chin K., Fridlyand J., Yeh J., Baehner F.L., Fevr T., Clark L., Bayani N., Coppe J., Tong F., Speed T., Spellman P.T., DeVries S., Lapuk A., Wang N.J., Kuo W., Stilwell J.L., Pinkel D., Albertson D.G., Waldman F.M., McCormick F., Dickson R.B., Johnson M.D., Lippman M., Ethier S., Gazdar A., Gray J.W. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 2006, 10:515.
24. Dorai T., Sawczuk I.S., Pastorek J., Wiernik P.H., Dutcher J.P. The role of carbonic anhydrase IX overexpression in kidney cancer. Eur. J. Cancer 2005, 41:2935.
25. +-ATPase in human breast cancer cells with distinct metastatic potential: distribution and functional activity. Am. J. Physiol. 2004, 286:C1443-C1452.
26. Markwell M.A.K., Haas S.M., Lieber L.L., Tolbert N.E. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal. Biochem. 1978, 87:206.
27. Silverman D.N. Carbonic anhydrase: oxygen-18 exchange catalyzed by an enzyme with rate-contributing proton-transfer steps. Meth. Enzymol. 1982, 87:732.
28. Kumar A., Xiao Y.-P., Laipis P.J., Fletcher B.S., Frost S.C. Glucose deprivation enhances targeting of GLUT1 to lipid rafts in 3T3-L1 adipocytes. Am. J. Physiol. 2004, 286:E568-E576.
29. Pastorekova S., Zavadova Z., Kostal M., Babusikova O., Zavada J. A novel quasi-viral agent, MaTu, is a two-component system. Virology 1992, 187:620.
30. Kitzman H.H., McMahon R.J., Williams M.G., Frost S.C. Effect of glucose deprivation on GLUT1 expression in 3T3-L1 adipocytes. J. Biol. Chem. 1993, 268:1320.
31. Opavsky R., Pastoreková S., Zelník V., Gibadulinová A., Stanbridge E.J., Závada J., Kettmann R., Pastorek J. Human MN/CA9 Gene, a novel member of the carbonic anhydrase family: structure and exon to protein domain relationships. Genomics 1996, 33:480.
32. Maxwell P.H., Wiesener M.S., Chang G., Clifford S.C., Vaux E.C., Cockman M.E., Wykoff C.C., Pugh C.W., Maher E.R., Ratcliffe P.J. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999, 399:271.
33. Wykoff C.C., Beasley N.J.P., Watson P.H., Turner K.J., Pastorek J., Sibtain A., Wilson G.D., Turley H., Talks K.L., Maxwell P.H., Pugh C.W., Ratcliffe P.J., Harris A.L. Hypoxia-inducible expression of tumor-associated carbonic anhydrase. Cancer Res. 2000, 60:7075.
34. Greijer A.E., van der Groep P., Kemming D., Shvarts A., Semenza G.L., Meijer G.A., van de Wiel M.A., Belien J.A.M., van Diest P.J., van der Wall E. Up-regulation of gene expression by hypoxia is mediated predominantly by hypoxia-inducible factor 1 (HIF1). J. Pathol. 2005, 206:291.
35. Ratcliffe P.J., Pugh C.W., Maxwell P.H. Targeting tumors through the HIF system. Nat. Med. 2000, 6:1315.
36. Wykoff C.C., Beasley N., Watson P.H., Campo L., Chia S.K., English R., Pastorek J., Sly W.S., Ratcliffe P., Harris A.L. Expression of hypoxia-inducible and tumor-associated carbonic anhydrases in ductal carcinoma in situ of the breast. Am. J. Pathol. 2001, 158:1011.
37. Span P.M., Bussink J., Manders P., Beex L.V.A.M., Sweep C.G.J. Carbonic anhydrase-9 expression levels and prognosis in human breast cancer: association with treatment outcome. Br. J. Cancer 2003, 89:271.
38. Generali D., Fox S.B., Berruti A., Brizzi M.P., Campo L., Bonardi S., Wigfield S.M., Bruzzi P., Bersiga A., Allevi G., Milani M., Aguggini S., Dogliotti L., Bottini A., Harris A.L. Role of carbonic anhydrase IX expression in prediction of the efficacy and outcome of primary epirubicin/tamoxifen therapy for breast cancer. Endocr.-Relat. Cancer 2006, 13:921.
39. Trastour C., Benizri E., Ettore F., Ramaioli A., Chamorey E., Pouyssegur J., Berra E. HIF-1a and CA IX staining in invasive breast carcinomas: prognosis and treatment outcome. Int. J. Cancer 2007, 120:1451.
40. Cairns R., Papandreou I., Denko N. Overcoming physiologic barriers to cancer treatment by molecularly targeting the tumor microenvironment. Mol. Cancer Res. 2006, 4:61.
41. Tan E.Y., Yan M., Campo L., Han C., Takano E., Turley H., Candiloro I., Pezzella F., Gatter K.C., Millar E.K.A., O'Toole S.A., McNeil C.M., Crea P., Segara D., Sutherland R.L., Harris A.L., Fox S.B. The key hypoxia regulated gene CAIX is upregulated in basal-like breast tumours and is associated with resistance to chemotherapy. Br. J. Cancer 2009, 100:405.
42. Hsieh M.-J., Chen K.-S., Chiou H.-L., Hsieh Y.-S. Carbonic anhydrase XII promotes invasion and migration ability of MDA-MB-231 breast cancer cells through the p38 MAPK signaling pathway. Eur. J. Cell Biol. 2010, 89:598.
43. Hanahan D., Weinberg R.A. Hallmarks of Cancer. Cell 2000, 100:57.
44. Masramon L., Vendrell E., Tarafa G., Capella G., Miro R., Ribas M., Peinado M.A. Genetic instability and divergence of clonal populations in colon cancer cells in vitro. J. Cell Sci. 2006, 119:1477.
45. Hilvo M., Baranauskiene L., Salzano A.M., Scaloni A., Matulis D., Innocenti A., Scozzafava A., Monti S.M., Di Flore A., De Simone G., Lindfors M., Janis J., Valjakka J., Pastorekova S., Pastorek J., Kulomaa M.S., Mordlund H.R., Supuran C.T., Parkkila S. Biochemical characterization of CA IX, one of the most active carbonic anhydrase isozymes. J. Biol. Chem. 2008, 283:27799.
46. Alterio V., Hilvo M., Di Fiore A., Supuran C.T., Pan P., Parkkila S., Scaloni A., Pastorek J., Pastorekova S., Pedone C., Scozzafava A., Monti S.M., De Simone G. Crystal structure of the catalytic domain of the tumor-associated human carbonic anhydrase IX. Proc. Natl Acad. Sci. USA 2009, 106:16233.
47. De Simone G., Supuran C.T. Carbonic anhycrase IX: biochemical and crystallographic characterization of a novel antitumor target. Biochim. Biophys. Acta 2010, 1804:494.
48. Wong N.K., Easton R.L., Panico M., Sutton-Smith M., Morrison J.C., Lattanzio F.A., Morris H.R., Clark G.F., Dell A., Patankar M.S. Characterization of the oligosaccharides associated with the human ovarian tumor marker CA125. J. Biol. Chem. 2003, 278:28619.
49. Goetz J.A., Mechref Y., Kang P., Jeng M., Hovotny M.V. Glycomics profiling of invasive and non-invasive breast cancer cells. Glycoconj. J. 2009, 26:117.
50. McMahon R.J., Frost S.C. Nutrient control of GLUT1 processing and turnover in 3T3-L1 adipocytes. J. Biol. Chem. 1995, 270:12094.
51. Smart E.J., Ying Y., Mineo C., Anderson R.G.W. A detergent-free method for purifying caveolae membrane from tissue culture cells. Proc. Natl Acad. Sci. USA 1995, 92:10104.
52. Sun J., Nanjundan M., Pike L.J., Wiedmer T., Sims P.J. Plasma membrane phospholiid scramblase 1 is enriched in lipid rafts and interacts with the epidermal growth factor receptor. Biochemistry 2002, 41:6338.
53. Nanjundan M., Sun J., Zhao J., Zhou Q., Sims P.J., Weidmer T. Plasma membrane phospholipid scramblase I promotes EGF-dependent activation of c-Src through the epidermal growth factor receptor. J. Biol. Chem. 2008, 278:37413.
54. Chen X., Resh M.D. Cholesterol depletion from the plasma membrane triggers ligand-independent activation of the epidermal growth factor receptor. J. Biol. Chem. 2002, 277:49631.
55. Ringerike T., Blystad F.D., Lvey F.O., Madshus I.H., Stang E. Cholesterol is important in control of EGF receptor kinase activity but EGF receptors are not concentrated in caveolae. J. Cell Sci. 2002, 115:1331.
56. Teng D.H., Hu R., Lin H., Davis T., Iliev D., Frye C., Swedlund B., Hansen K.L., Vinson V.L., Gumpper K.L., Ellis L., El-Naggar A., Frazier M., Jasser S., Langford L.A., Lee J., Mills G.B., Pershouse M.A., Polllack R.E., Tornos C., Troncoso P., Yung W.K.A., Fujii G., Berson A., Bookstein R., Bolen J.B., Tavtigian S.V., Steck P.A. MMACI/PTEN mutations in primary tumor specimens and tumor cell lines. Cancer Res. 1997, 57:5221.
57. Lu Y., Lin Y., LaPushin R., Cuevas B., Fang X., Yu X.S., Davies M.A., Kahn H., Furui T., Mao M., Zinner R., Hung M., Steck P., Siminovitch K., Mills G.B. The Pten/MMAC/TEP tumor suppressor gene decreases cell growth and induces apoptosis and anoikis in breast cancer cells. Oncogene 1999, 18:7034.
58. Alvarez-Tejado M., Naranjo-Suarez S., Jimenez C., Carrera A.C., Landazuri M.O., del Peso L. Hypoxia Induces the Activation of the Phosphatidylinositol 3-Kinase/Akt Cell Survival Pathway in PC12 cells: Protective Role in Apoptosis. J. Biol. Chem. 2001, 276:22368.
59. Beitner-Johnson D., Rust R.T., Hsieh T.C., Millhorn D.E. Hypoxia activates Akt and induces phosphorylation of GSK-3 in PC12 cells. Cell. Signal. 2001, 13:23.
60. Mardilovich K., Shaw L.M. Hypoxia regulates insulin receptor substrate-2 expression to promote breast carcinoma cell survival and invasion. Cancer Res. 2009, 69:8894.
61. Rathmell J.C., Fox C.J., Plas D.R., Hammerman P.S., Cinalli R.M., Thompson C.B. Akt-directed glucose metabolism can prevent Bax conformation change and promote growth factor-independent survival. Mol. Cell. Biol. 2003, 23:7315.
62. DeBerardinis R.J., Lum J.J., Hatzivassiliou G., Thompson C.B. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab. 2008, 7:11.
63. Rubin D., Ismail-Beigi F. Distribution of Glut1 in detergent resistant (DRMs) and non-DRM domains: effect of treatment with azide. Am. J. Physiol. 2003, 285:C377-C383.