Generation and characterization of the first inhibitory antibody targeting tumour-associated carbonic anhydrase XII

Cancer Immunology, Immunotherapy

Volumn 60, Issue 5, 2011, Pages 649-658

  Battke, Christina ^a   Kremmer, Elisabeth ^a   Mysliwietz, Josef ^a   Gondi, Gabor ^a   Dumitru, Claudia ^b   Brandau, Sven ^b   Lang, Stephan ^b   Vullo, Daniela ^c   Supuran, Claudiu ^c   Zeidler, Reinhard ^d  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b UNIVERSITY HOSPITAL ESSEN   (Germany)

^c UNIVERSITY OF FLORENCE   (Italy)

^d UNIVERSITY OF MUNICH   (Germany)

Author keywords

Cancer treatment; Carbonic anhydrase; Hypoxia; Monoclonal antibody; Warburg effect

Indexed keywords

ACETAZOLAMIDE; CARBONATE DEHYDRATASE XII; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 6A10; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CANCER STEM CELL; CATALYSIS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; GROWTH INHIBITION; HEAD AND NECK CANCER; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; NONHUMAN; PRIORITY JOURNAL; RAT; TUMOR CELL; TUMOR SPHEROID;

ANIMALS; ANTIBODIES, MONOCLONAL; CARBONIC ANHYDRASE INHIBITORS; CARBONIC ANHYDRASES; CELL LINE, TUMOR; CELL PROLIFERATION; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION; HYDROGEN-ION CONCENTRATION; MEMBRANE PROTEINS; NEOPLASMS; RATS;

EID: 79955549517     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-011-0980-z     Document Type: Article

References (51)

1. O Warburg 1956 On respiratory impairment in cancer cells Science 124 269 270 13351639 1:STN:280:DyaG287gsVeksA%3D%3D
2. M Stubbs PM McSheehy JR Griffiths CL Bashford 2000 Causes and consequences of tumour acidity and implications for treatment Mol Med Today 6 15 19 10637570 10.1016/S1357-4310(99)01615-9 1:CAS:528:DC%2BD3cXms1alsg%3D%3D (Pubitemid 30010232)
3. N Oksala M Levula M Pelto-Huikko L Kytomaki JT Soini J Salenius M Kahonen PJ Karhunen R Laaksonen S Parkkila T Lehtimaki 2010 Carbonic anhydrases II and XII are up-regulated in osteoclast-like cells in advanced human atherosclerotic plaques-Tampere Vascular Study Ann Med 42 360 370 20509747 10.3109/07853890. 2010.486408 1:CAS:528:DC%2BC3cXnsVWitrk%3D
4. SY Liao S Ivanov A Ivanova S Ghosh MA Cote K Keefe M Coca-Prados EJ Stanbridge MI Lerman 2003 Expression of cell surface transmembrane carbonic anhydrase genes CA9 and CA12 in the human eye: overexpression of CA12 (CAXII) in glaucoma J Med Genet 40 257 261 12676895 10.1136/jmg.40.4.257 1:CAS:528:DC%2BD3sXjsleguro%3D (Pubitemid 36506438)
5. CT Supuran 2008 Carbonic anhydrases-an overview Curr Pharm Des 14 603 614 18336305 10.2174/138161208783877884 1:CAS:528:DC%2BD1cXls1ajsrs%3D (Pubitemid 351736439)
6. V Alterio M Hilvo A Di Fiore CT Supuran P Pan S Parkkila A Scaloni J Pastorek S Pastorekova C Pedone A Scozzafava SM Monti G De Simone 2009 Crystal structure of the catalytic domain of the tumor-associated human carbonic anhydrase IX Proc Natl Acad Sci USA 106 16233 16238 19805286 10.1073/pnas.0908301106 1:CAS:528:DC%2BD1MXht1Kqt7nL
7. DA Whittington A Waheed B Ulmasov GN Shah JH Grubb WS Sly DW Christianson 2001 Crystal structure of the dimeric extracellular domain of human carbonic anhydrase XII, a bitopic membrane protein overexpressed in certain cancer tumor cells Proc Natl Acad Sci USA 98 9545 9550 11493685 10.1073/pnas.161301298 1:CAS:528:DC%2BD3MXmtlCntbo%3D (Pubitemid 32769340)
8. CC Wykoff N Beasley PH Watson L Campo SK Chia R English J Pastorek WS Sly P Ratcliffe AL Harris 2001 Expression of the hypoxia-inducible and tumor-associated carbonic anhydrases in ductal carcinoma in situ of the breast Am J Pathol 158 1011 1019 11238049 10.1016/S0002-9440(10)64048-5 1:CAS:528:DC%2BD3MXitlOmsr4%3D (Pubitemid 32221793)
9. MJ Hsieh KS Chen HL Chiou YS Hsieh 2010 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 89 598 606 20434230 10.1016/j.ejcb.2010. 03.004 1:CAS:528:DC%2BC3cXotlWqu7s%3D
10. J Chiche K Ilc J Laferriere E Trottier F Dayan NM Mazure MC Brahimi-Horn J Pouyssegur 2009 Hypoxia-inducible carbonic anhydrase IX and XII promote tumor cell growth by counteracting acidosis through the regulation of the intracellular pH Cancer Res 69 358 368 19118021 10.1158/0008-5472.CAN-08-2470 1:CAS:528:DC%2BD1MXmvFKl
11. S Parkkila H Rajaniemi AK Parkkila J Kivela A Waheed S Pastorekova J Pastorek WS Sly 2000 Carbonic anhydrase inhibitor suppresses invasion of renal cancer cells in vitro Proc Natl Acad Sci USA 97 2220 2224 10688890 10.1073/pnas.040554897 1:CAS:528:DC%2BD3cXhslKht7Y%3D (Pubitemid 30134049)
12. E Svastova N Zilka M Zat'ovicova A Gibadulinova F Ciampor J Pastorek S Pastorekova 2003 Carbonic anhydrase IX reduces E-cadherin-mediated adhesion of MDCK cells via interaction with beta-catenin Exp Cell Res 290 332 345 14567991 10.1016/S0014-4827(03)00351-3 1:CAS:528:DC%2BD3sXotVCitLc%3D (Pubitemid 37272176)
13. O Tureci U Sahin E Vollmar S Siemer E Gottert G Seitz AK Parkkila GN Shah JH Grubb M Pfreundschuh WS Sly 1998 Human carbonic anhydrase XII: cDNA cloning, expression, and chromosomal localization of a carbonic anhydrase gene that is overexpressed in some renal cell cancers Proc Natl Acad Sci USA 95 7608 7613 9636197 10.1073/pnas.95.13.7608 1:CAS:528:DyaK1cXktFChu7g%3D (Pubitemid 28293300)
14. P Karhumaa S Parkkila O Tureci A Waheed JH Grubb G Shah A Parkkila K Kaunisto J Tapanainen WS Sly H Rajaniemi 2000 Identification of carbonic anhydrase XII as the membrane isozyme expressed in the normal human endometrial epithelium Mol Hum Reprod 6 68 74 10611263 10.1093/molehr/6.1.68 1:CAS:528:DC%2BD3cXptFCrsA%3D%3D (Pubitemid 30043591)
15. A Kivela S Parkkila J Saarnio TJ Karttunen J Kivela AK Parkkila A Waheed WS Sly JH Grubb G Shah O Tureci H Rajaniemi 2000 Expression of a novel transmembrane carbonic anhydrase isozyme XII in normal human gut and colorectal tumors Am J Pathol 156 577 584 10666387 10.1016/S0002-9440(10)64762-1 1:STN:280:DC%2BD3c7jt1yhug%3D%3D (Pubitemid 30643813)
16. DH Barnett S Sheng TH Charn A Waheed WS Sly CY Lin ET Liu BS Katzenellenbogen 2008 Estrogen receptor regulation of carbonic anhydrase XII through a distal enhancer in breast cancer Cancer Res 68 3505 3515 18451179 10.1158/0008-5472.CAN-07-6151 1:CAS:528:DC%2BD1cXltlSltL0%3D
17. P Hynninen L Vaskivuo J Saarnio H Haapasalo J Kivela S Pastorekova J Pastorek A Waheed WS Sly U Puistola S Parkkila 2006 Expression of transmembrane carbonic anhydrases IX and XII in ovarian tumours Histopathology 49 594 602 17163844 10.1111/j.1365-2559.2006.02523.x 1:STN:280:DC%2BD28jis1WlsA%3D%3D (Pubitemid 44924291)
18. Ilie MI, Hofman V, Ortholan C, Ammadi RE, Bonnetaud C, Havet K, Venissac N, Mouroux J, Mazure NM, Pouyssegur J, Hofman P (2010) Overexpression of carbonic anhydrase XII in tissues from resectable non-small cell lung cancers is a biomarker of good prognosis. Int J Cancer 128:1614-1623
19. S Ivanov SY Liao A Ivanova A Danilkovitch-Miagkova N Tarasova G Weirich MJ Merrill MA Proescholdt EH Oldfield J Lee J Zavada A Waheed W Sly MI Lerman EJ Stanbridge 2001 Expression of hypoxia-inducible cell-surface transmembrane carbonic anhydrases in human cancer Am J Pathol 158 905 919 11238039 10.1016/S0002-9440(10)64038-2 1:CAS:528:DC%2BD3MXitlOnu74%3D (Pubitemid 32221783)
20. M Leppilampi J Saarnio TJ Karttunen J Kivela S Pastorekova J Pastorek A Waheed WS Sly S Parkkila 2003 Carbonic anhydrase isozymes IX and XII in gastric tumors World J Gastroenterol 9 1398 1403 12854129 1:CAS:528:DC%2BD3sXoslajtr0%3D (Pubitemid 36992321)
21. S Parkkila AK Parkkila J Saarnio J Kivela TJ Karttunen K Kaunisto A Waheed WS Sly O Tureci I Virtanen H Rajaniemi 2000 Expression of the membrane-associated carbonic anhydrase isozyme XII in the human kidney and renal tumors J Histochem Cytochem 48 1601 1608 11101628 10.1177/002215540004801203 1:CAS:528:DC%2BD3MXit1eq
22. MA Proescholdt C Mayer M Kubitza T Schubert SY Liao EJ Stanbridge S Ivanov EH Oldfield A Brawanski MJ Merrill 2005 Expression of hypoxia-inducible carbonic anhydrases in brain tumors Neuro Oncology 7 465 475 16212811 10.1215/S1152851705000025 1:CAS:528:DC%2BD2MXht1SisLvI (Pubitemid 41555618)
23. B Ulmasov A Waheed GN Shah JH Grubb WS Sly C Tu DN Silverman 2000 Purification and kinetic analysis of recombinant CA XII, a membrane carbonic anhydrase overexpressed in certain cancers Proc Natl Acad Sci USA 97 14212 14217 11121027 10.1073/pnas.97.26.14212 1:CAS:528:DC%2BD3MXitVCntA%3D%3D (Pubitemid 32016556)
24. S Ashida I Nishimori M Tanimura S Onishi T Shuin 2002 Effects of von Hippel-Lindau gene mutation and methylation status on expression of transmembrane carbonic anhydrases in renal cell carcinoma J Cancer Res Clin Oncol 128 561 568 12384800 10.1007/s00432-002-0374-x 1:CAS:528: DC%2BD3sXksVyrsA%3D%3D (Pubitemid 35244932)
25. CJ Creighton KE Cordero JM Larios RS Miller MD Johnson AM Chinnaiyan ME Lippman JM Rae 2006 Genes regulated by estrogen in breast tumor cells in vitro are similarly regulated in vivo in tumor xenografts and human breast tumors Genome Biol 7 R28 16606439 10.1186/gb-2006-7-4-r28 (Pubitemid 43871882)
26. J Frasor F Stossi JM Danes B Komm CR Lyttle BS Katzenellenbogen 2004 Selective estrogen receptor modulators: discrimination of agonistic versus antagonistic activities by gene expression profiling in breast cancer cells Cancer Res 64 1522 1533 14973112 10.1158/0008-5472.CAN-03-3326 1:CAS:528:DC%2BD2cXhtleitLk%3D (Pubitemid 38235626)
27. T Mosmann 1983 Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays J Immunol Methods 65 55 63 6606682 10.1016/0022-1759(83)90303-4 1:STN:280:DyaL2c%2FovFSmtw%3D%3D (Pubitemid 14203433)
28. SF Ibrahim AH Diercks TW Petersen G van den Engh 2007 Kinetic analyses as a critical parameter in defining the side population (SP) phenotype Exp Cell Res 313 1921 1926 17428468 10.1016/j.yexcr.2007.02.025 1:CAS:528: DC%2BD2sXkslOiurg%3D (Pubitemid 46653868)
29. A Innocenti D Vullo J Pastorek A Scozzafava S Pastorekova I Nishimori CT Supuran 2007 Carbonic anhydrase inhibitors. Inhibition of transmembrane isozymes XII (cancer-associated) and XIV with anions Bioorg Med Chem Lett 17 1532 1537 17257840 10.1016/j.bmcl.2006.12.113 1:CAS:528:DC%2BD2sXit1yktLc%3D (Pubitemid 46290636)
30. D Vullo A Innocenti I Nishimori J Pastorek A Scozzafava S Pastorekova CT Supuran 2005 Carbonic anhydrase inhibitors. Inhibition of the transmembrane isozyme XII with sulfonamides-a new target for the design of antitumor and antiglaucoma drugs? Bioorg Med Chem Lett 15 963 969 15686894 10.1016/j.bmcl.2004.12.053 1:CAS:528:DC%2BD2MXos1eqsA%3D%3D (Pubitemid 40458631)
31. RG Khalifah 1971 The carbon dioxide hydration activity of carbonic anhydrase. I. Stop-flow kinetic studies on the native human isoenzymes B and C J Biol Chem 246 2561 2573 4994926 1:CAS:528:DyaE3MXhtlGmu7k%3D
32. CT Supuran 2008 Carbonic anhydrases: novel therapeutic applications for inhibitors and activators Nat Rev Drug Discov 7 168 181 18167490 10.1038/nrd2467 1:CAS:528:DC%2BD1cXhs1Khsr0%3D (Pubitemid 351194064)
33. CT Supuran A Scozzafava A Casini 2003 Carbonic anhydrase inhibitors Med Res Rev 23 146 189 12500287 10.1002/med.10025 1:CAS:528:DC%2BD3sXitVyksr4%3D (Pubitemid 36241096)
34. S Pastorekova M Zatovicova J Pastorek 2008 Cancer-associated carbonic anhydrases and their inhibition Curr Pharm Des 14 685 698 18336315 10.2174/138161208783877893 1:CAS:528:DC%2BD1cXls1ajs7s%3D (Pubitemid 351736449)
35. RL Jensen 2009 Brain tumor hypoxia: tumorigenesis, angiogenesis, imaging, pseudoprogression, and as a therapeutic target J Neurooncol 92 317 335 19357959 10.1007/s11060-009-9827-2 1:CAS:528:DC%2BD1MXkt1yitL4%3D
36. CT Supuran A Scozzafava 2007 Carbonic anhydrases as targets for medicinal chemistry Bioorg Med Chem 15 4336 4350 17475500 10.1016/j.bmc.2007.04.020 1:CAS:528:DC%2BD2sXlvFSjsr8%3D (Pubitemid 46777288)
37. P Swietach S Wigfield CT Supuran AL Harris RD Vaughan-Jones 2008 Cancer-associated, hypoxia-inducible carbonic anhydrase IX facilitates CO2 diffusion BJU Int 101 Suppl 4 22 24 18430118 10.1111/j.1464-410X.2008.07644.x 1:CAS:528:DC%2BD1cXnsVKqsrY%3D
38. P Swietach S Wigfield P Cobden CT Supuran AL Harris RD Vaughan-Jones 2008 Tumor-associated carbonic anhydrase 9 spatially coordinates intracellular pH in three-dimensional multicellular growths J Biol Chem 283 20473 20483 18482982 10.1074/jbc.M801330200 1:CAS:528:DC%2BD1cXotlOhsrk%3D
39. MP Deonarain CA Kousparou AA Epenetos 2009 Antibodies targeting cancer stem cells: a new paradigm in immunotherapy? MAbs 1 12 25 20046569 10.4161/mabs.1.1.7347
40. C Wu BA Alman 2008 Side population cells in human cancers Cancer Lett 268 1 9 18487012 10.1016/j.canlet.2008.03.048 1:CAS:528:DC%2BD1cXpt1Gku7Y%3D
41. JM Sung HJ Cho H Yi CH Lee HS Kim DK Kim AM Abd El-Aty JS Kim CP Landowski MA Hediger HC Shin 2008 Characterization of a stem cell population in lung cancer A549 cells Biochem Biophys Res Commun 371 163 167 18423378 10.1016/j.bbrc.2008.04.038 1:CAS:528:DC%2BD1cXlvVWgtrw%3D
42. P Vaupel A Mayer 2007 Hypoxia in cancer: significance and impact on clinical outcome Cancer Metastasis Rev 26 225 239 17440684 10.1007/s10555-007- 9055-1 1:CAS:528:DC%2BD2sXotFWrtLo%3D (Pubitemid 47101660)
43. AY Isa TH Ward CM West NJ Slevin JJ Homer 2006 Hypoxia in head and neck cancer Br J Radiol 79 791 798 16854964 10.1259/bjr/17904358 1:CAS:528: DC%2BD28Xht1ehsLjO (Pubitemid 44613678)
44. EP Hui AT Chan F Pezzella H Turley KF To TC Poon B Zee F Mo PM Teo DP Huang KC Gatter PJ Johnson AL Harris 2002 Coexpression of hypoxia-inducible factors 1alpha and 2alpha, carbonic anhydrase IX, and vascular endothelial growth factor in nasopharyngeal carcinoma and relationship to survival Clin Cancer Res 8 2595 2604 12171890 1:CAS:528:DC%2BD38XmvVahsL8%3D (Pubitemid 34856346)
45. M Kappler H Taubert HJ Holzhausen R Reddemann S Rot A Becker T Kuhnt K Dellas J Dunst D Vordermark G Hansgen M Bache 2008 Immunohistochemical detection of HIF-1alpha and CAIX in advanced head-and-neck cancer. Prognostic role and correlation with tumor markers and tumor oxygenation parameters Strahlenther Onkol 184 393 399 18956515 10.1007/s00066-008-1813-7
46. NJ Beasley CC Wykoff PH Watson R Leek H Turley K Gatter J Pastorek GJ Cox P Ratcliffe AL Harris 2001 Carbonic anhydrase IX, an endogenous hypoxia marker, expression in head and neck squamous cell carcinoma and its relationship to hypoxia, necrosis, and microvessel density Cancer Res 61 5262 5267 11431368 1:CAS:528:DC%2BD3MXltVCjs7s%3D (Pubitemid 32681562)
47. J Haapasalo M Hilvo K Nordfors H Haapasalo S Parkkila A Hyrskyluoto I Rantala A Waheed WS Sly S Pastorekova J Pastorek AK Parkkila 2008 Identification of an alternatively spliced isoform of carbonic anhydrase XII in diffusely infiltrating astrocytic gliomas Neuro Oncology 10 131 138 18322268 10.1215/15228517-2007-065 1:CAS:528:DC%2BD1cXls1Gjs7s%3D
48. JS Fang RD Gillies RA Gatenby 2008 Adaptation to hypoxia and acidosis in carcinogenesis and tumor progression Semin Cancer Biol 18 330 337 18455429 10.1016/j.semcancer.2008.03.011 1:CAS:528:DC%2BD1cXpsVGmsL8%3D
49. Q Ke M Costa 2006 Hypoxia-inducible factor-1 (HIF-1) Mol Pharmacol 70 1469 1480 16887934 10.1124/mol.106.027029 1:CAS:528:DC%2BD28XhtFygsbjI
50. AS Silva JA Yunes RJ Gillies RA Gatenby 2009 The potential role of systemic buffers in reducing intratumoral extracellular pH and acid-mediated invasion Cancer Res 69 2677 2684 19276380 10.1158/0008-5472.CAN-08-2394 1:CAS:528:DC%2BD1MXjtF2jsrk%3D
51. E Oosterwijk DJ Ruiter PJ Hoedemaeker EK Pauwels U Jonas J Zwartendijk SO Warnaar 1986 Monoclonal antibody G 250 recognizes a determinant present in renal-cell carcinoma and absent from normal kidney Int J Cancer 38 489 494 2428759 10.1002/ijc.2910380406 1:STN:280:DyaL2s%2FgslWrtg%3D%3D (Pubitemid 16006918)