Application of monoclonal antibody G250 recognizing carbonic anhydrase IX in renal cell carcinoma

International Journal of Molecular Sciences

Volumn 14, Issue 6, 2013, Pages 11402-11423

  Oosterwijk Wakka, Jeannette C ^a   Boerman, Otto C ^a   Mulders, Peter F A Mulders ^a   Oosterwijk, Egbert ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

CAIX; Clear cell renal cell carcinoma; G250; Girentuximab; Imaging; Monoclonal antibody; Radioimmunotherapy; RCC

Indexed keywords

ALPHA2A INTERFERON; CARBONATE DEHYDRATASE IX; FLUORODEOXYGLUCOSE F 18; GIRENTUXIMAB; GIRENTUXIMAB I 124; INDIUM 111; INTERLEUKIN 2; IODINE 131; LUTETIUM 177; PLACEBO; PROTEIN TYROSINE KINASE INHIBITOR; RHENIUM 186; YTTRIUM 90; ANTIGEN G250; CARBONATE DEHYDRATASE; G250 MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY; TUMOR ANTIGEN;

ADVANCED CANCER; BLOOD TOXICITY; CANCER ADJUVANT THERAPY; CANCER DIAGNOSIS; COMPUTER ASSISTED EMISSION TOMOGRAPHY; DRUG DISTRIBUTION; DRUG DOSE ESCALATION; DRUG MEGADOSE; DRUG TOLERABILITY; DRUG TUMOR LEVEL; HUMAN; ISOTOPE LABELING; KIDNEY CARCINOMA; LOW DRUG DOSE; METASTASIS; MOLECULAR CLONING; MULTIPLE CYCLE TREATMENT; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); POSITRON EMISSION TOMOGRAPHY; PROTEIN EXPRESSION; RADIOIMMUNOTHERAPY; REVIEW; SENSITIVITY AND SPECIFICITY; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; UNSPECIFIED SIDE EFFECT; ANIMAL; CARCINOMA, RENAL CELL; CLINICAL TRIAL (TOPIC); ENZYMOLOGY; KIDNEY NEOPLASMS; METABOLISM;

ANIMALIA;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, NEOPLASM; CARBONIC ANHYDRASES; CARCINOMA, RENAL CELL; CLINICAL TRIALS AS TOPIC; HUMANS; KIDNEY NEOPLASMS;

EID: 84878454886     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms140611402     Document Type: Review

References (67)

1. Jemal, A.; Siegel, R.; Ward, E.; Hao, Y.; Xu, J.; Thun, M.J. Cancer statistics, 2009. CA Cancer J. Clin. 2009, 59, 225-249
2. Patard, J.J.; Pignot, G.; Escudier, B.; Eisen, T.; Bex, A.; Sternberg, C.; Rini, B.; Roigas, J.; Choueiri, T.; Bukowski, R. et al. Icud-eau international consultation on kidney cancer 2010: Treatment of metastatic disease. Eur. Urol. 2011, 60, 684-690
3. Motzer, R.J.; Rini, B.I.; Bukowski, R.M.; Curti, B.D.; George, D.J.; Hudes, G.R.; Redman, B.G.; Margolin, K.A.; Merchan, J.R.; Wilding, G. et al. Sunitinib in patients with metastatic renal cell carcinoma. JAMA 2006, 295, 2516-2524
4. Escudier, B.; Eisen, T.; Stadler, W.M.; Szczylik, C.; Oudard, S.; Siebels, M.; Negrier, S.; Chevreau, C.; Solska, E.; Desai, A.A. et al. Sorafenib in advanced clear-cell renal-cell carcinoma. N. Engl. J. Med. 2007, 356, 125-134
5. Rixe, O.; Bukowski, R.M.; Michaelson, M.D.; Wilding, G.; Hudes, G.R.; Bolte, O.; Motzer, R.J.; Bycott, P.; Liau, K.F.; Freddo, J. et al. Axitinib treatment in patients with cytokine-refractory metastatic renal-cell cancer: A phase II study. Lancet Oncol. 2007, 8, 975-984
6. Sternberg, C.N.; Davis, I.D.; Mardiak, J.; Szczylik, C.; Lee, E.; Wagstaff, J.; Barrios, C.H.; Salman, P.; Gladkov, O.A.; Kavina, A. et al. Pazopanib in locally advanced or metastatic renal cell carcinoma: Results of a randomized phase III trial. J. Clin. Oncol. 2010, 28, 1061-1068
7. Escudier, B.; Bellmunt, J.; Negrier, S.; Bajetta, E.; Melichar, B.; Bracarda, S.; Ravaud, A.; Golding, S.; Jethwa, S.; Sneller, V. Phase III trial of bevacizumab plus interferon alfa-2a in patients with metastatic renal cell carcinoma (avoren): Final analysis of overall survival. J. Clin. Oncol. 2010, 28, 2144-2150
8. Coppin, C.; Kollmannsberger, C.; Le, L.; Porzsolt, F.; Wilt, T.J. Targeted therapy for advanced renal cell cancer (rcc): A cochrane systematic review of published randomised trials. BJU Int. 2011, 108, 1556-1563
9. Oosterwijk, E.; Ruiter, D.J.; Hoedemaeker, P.J.; Pauwels, E.K.; Jonas, U.; Zwartendijk, J.; Warnaar, S.O. Monoclonal antibody g250 recognizes a determinant present in renal-cell carcinoma and absent from normal kidney. Int. J. Cancer 1986, 38, 489-494
10. Uemura, H.; Nakagawa, Y.; Yoshida, K.; Saga, S.; Yoshikawa, K.; Hirao, Y.; Oosterwijk, E. Mn/ca ix/g250 as a potential target for immunotherapy of renal cell carcinomas. Br. J. Cancer 1999, 81, 741-746
11. Bismar, T.A.; Bianco, F.J.; Zhang, H.; Li, X.; Sarkar, F.H.; Sakr, W.A.; Grignon, D.J.; Che, M. Quantification of g250 mrna expression in renal epithelial neoplasms by real-time reverse transcription-pcr of dissected tissue from paraffin sections. Pathology 2003, 35, 513-517
12. Pastorek, J.; Pastorekova, S.; Callebaut, I.; Mornon, J.P.; Zelnik, V.; Opavsky, R.; Zat'ovicova, M.; Liao, S.; Portetelle, D.; Stanbridge, E.J. et al. 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, 2877-2888
13. Grabmaier, K.; Vissers, J.L.; de Weijert, M.C.; Oosterwijk-Wakka, J.C.; van Bokhoven, A.; Brakenhoff, R.H.; Noessner, E.; Mulders, P.A.; Merkx, G.; Figdor, C.G. et al. Molecular cloning and immunogenicity of renal cell carcinoma-associated antigen g250. Int. J. Cancer 2000, 85, 865-870
14. Grabmaier, K.; A de Weijert, M.C.; Verhaegh, G.W.; Schalken, J.A.; Oosterwijk, E. Strict regulation of caix(g250/mn) by hif-1alpha in clear cell renal cell carcinoma. Oncogene 2004, 23, 5624-5631
15. Gnarra, J.R.; Tory, K.; Weng, Y.; Schmidt, L.; Wei, M.H.; Li, H.; Latif, F.; Liu, S.; Chen, F.; Duh, F.M. et al. Mutations of the vhl tumour suppressor gene in renal carcinoma. Nat. Genet. 1994, 7, 85-90
16. Jaakkola, P.; Mole, D.R.; Tian, Y.M.; Wilson, M.I.; Gielbert, J.; Gaskell, S.J.; von Kriegsheim, A.; Hebestreit, H.F.; Mukherji, M.; Schofield, C.J. et al. Targeting of hif-alpha to the von hippel-lindau ubiquitylation complex by o2-regulated prolyl hydroxylation. Science 2001, 292, 468-472
17. Schofield, C.J.; Ratcliffe, P.J. Signalling hypoxia by hif hydroxylases. Biochem. Biophys. Res. Commun. 2005, 338, 617-626
18. 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. et al. Expression of hypoxia-inducible cell-surface transmembrane carbonic anhydrases in human cancer. Am. J. Pathol. 2001, 158, 905-919
19. Potter, C.; Harris, A.L. Hypoxia inducible carbonic anhydrase ix, marker of tumour hypoxia, survival pathway and therapy target. Cell Cycle 2004, 3, 164-167
20. Stillebroer, A.B.; Mulders, P.F.; Boerman, O.C.; Oyen, W.J.; Oosterwijk, E., Carbonic anhydrase ix in renal cell carcinoma: Implications for prognosis, diagnosis, and therapy. Eur. Urol. 2010, 58, 75-83
21. Poeppel, T.D.; Krause, B.J.; Heusner, T.A.; Boy, C.; Bockisch, A.; Antoch, G. Pet/ct for the staging and follow-up of patients with malignancies. Eur. J. Radiol. 2009, 70, 382-392
22. Patard, J.J. Incidental renal tumours. Curr. Opin. Urol. 2009, 19, 454-458
23. Van Dijk, J.; Zegveld, S.T.; Fleuren, G.J.; Warnaar, S.O. Localization of monoclonal antibody g250 and bispecific monoclonal antibody cd3/g250 in human renal-cell carcinoma xenografts: Relative effects of size and affinity. Int. J. Cancer 1991, 48, 738-743
24. Kranenborg, M.H.; Boerman, O.C.; de Weijert, M.C.; Oosterwijk-Wakka, J.C.; Corstens, F.H.; Oosterwijk, E. The effect of antibody protein dose of anti-renal cell carcinoma monoclonal antibodies in nude mice with renal cell carcinoma xenografts. Cancer 1997, 80, 2390-2397
25. Steffens, M.G.; Kranenborg, M.H.; Boerman, O.C.; Zegwaart-Hagemeier, N.E.; Debruyne, F.M.; Corstens, F.H.; Oosterwijk, E. Tumor retention of 186re-mag3, 111in-dtpa and 125i labeled monoclonal antibody g250 in nude mice with renal cell carcinoma xenografts. Cancer Biother. Radiopharm. 1998, 13, 133-139
26. Steffens, M.G.; Oosterwijk, E.; Kranenborg, M.H.; Manders, J.M.; Debruyne, F.M.; Corstens, F.H.; Boerman, O.C. In vivo and in vitro characterizations of three 99mtc-labeled monoclonal antibody g250 preparations. J. Nucl. Med. 1999, 40, 829-836
27. Van Dijk, J.; Oosterwijk, E.; van Kroonenburgh, M.J.; Jonas, U.; Fleuren, G.J.; Pauwels, E.K.; Warnaar, S.O. Perfusion of tumor-bearing kidneys as a model for scintigraphic screening of monoclonal antibodies. J. Nucl. Med. 1988, 29, 1078-1082
28. Oosterwijk, E.; Bander, N.H.; Divgi, C.R.; Welt, S.; Wakka, J.C.; Finn, R.D.; Carswell, E.A.; Larson, S.M.; Warnaar, S.O.; Fleuren, G.J. et al. Antibody localization in human renal cell carcinoma: A phase i study of monoclonal antibody g250. J. Clin. Oncol. 1993, 11, 738-750
29. Divgi, C.R.; Bander, N.H.; Scott, A.M.; O'Donoghue, J.A.; Sgouros, G.; Welt, S.; Finn, R.D.; Morrissey, F.; Capitelli, P.; Williams, J.M. et al. Phase i/ii radioimmunotherapy trial with iodine-131-labeled monoclonal antibody g250 in metastatic renal cell carcinoma. Clin. Cancer Res. 1998, 4, 2729-2739
30. Steffens, M.G.; Boerman, O.C.; Oosterwijk-Wakka, J.C.; Oosterhof, G.O.; Witjes, J.A.; Koenders, E.B.; Oyen, W.J.; Buijs, W.C.; Debruyne, F.M.; Corstens, F.H. et al. Targeting of renal cell carcinoma with iodine-131-labeled chimeric monoclonal antibody g250. J. Clin. Oncol. 1997, 15, 1529-1537
31. Steffens, M.G.; Boerman, O.C.; Oyen, W.J.; Kniest, P.H.; Witjes, J.A.; Oosterhof, G.O.; van Leenders, G.J.; Debruyne, F.M.; Corstens, F.H.; Oosterwijk, E. Intratumoral distribution of two consecutive injections of chimeric antibody g250 in primary renal cell carcinoma: Implications for fractionated dose radioimmunotherapy. Cancer Res. 1999, 59, 1615-1619
32. Brouwers, A.H.; Dorr, U.; Lang, O.; Boerman, O.C.; Oyen, W.J.; Steffens, M.G.; Oosterwijk, E.; Mergenthaler, H.G.; Bihl, H.; Corstens, F.H. 131I-cg250 monoclonal antibody immunoscintigraphy vs. [18F]fdg-pet imaging in patients with metastatic renal cell carcinoma: A comparative study. Nucl. Med. Commun. 2002, 23, 229-236
33. Brouwers, A.H.; Buijs, W.C.; Oosterwijk, E.; Boerman, O.C.; Mala, C.; de Mulder, P.H.; Corstens, F.H.; Mulders, P.F.; Oyen, W.J. Targeting of metastatic renal cell carcinoma with the chimeric monoclonal antibody g250 labeled with 131I or 111In: An intrapatient comparison. Clin. Cancer Res. 2003, 9, 3953S-3960S.
34. Divgi, C.R.; Pandit-Taskar, N.; Jungbluth, A.A.; Reuter, V.E.; Gonen, M.; Ruan, S.; Pierre, C.; Nagel, A.; Pryma, D.A.; Humm, J. et al. Preoperative characterisation of clear-cell renal carcinoma using iodine-124-labelled antibody chimeric g250 (124I-cg250) and pet in patients with renal masses: A phase i trial. Lancet Oncol. 2007, 8, 304-310
35. Divgi, C.R.; Uzzo, R.G.; Gatsonis, C.; Bartz, R.; Treutner, S.; Yu, J.Q.; Chen, D.; Carrasquillo, J.A.; Larson, S.; Bevan, P. et al. Positron emission tomography/computed tomography identification of clear cell renal cell carcinoma: Results from the redect trial. J. Clin. Oncol. 2013, 31, 187-194
36. Muselaers, C.H.; Boerman, O.C.; Oosterwijk, E.; Langenhuijsen, J.F.; Oyen, W.J.; Mulders, P.F. Indium-111-labeled girentuximab immunospect as a diagnostic tool in clear cell renal cell carcinoma. Eur. Urol. 2013, doi:10.1016/j.eururo.2013.02.022
37. Steffens, M.G.; Oosterwijk, E.; Zegwaart-Hagemeier, N.E.; van't Hof, M.A.; Debruyne, F.M.; Corstens, F.H.; Boerman, O.C. Immunohistochemical analysis of intratumoral heterogeneity of [131I]cg250 antibody uptake in primary renal cell carcinomas. Br. J. Cancer 1998, 78, 1208-1213
38. Durrbach, A.; Angevin, E.; Poncet, P.; Rouleau, M.; Chavanel, G.; Chapel, A.; Thierry, D.; Gorter, A.; Hirsch, R.; Charpentier, B.; et al. Antibody-mediated endocytosis of g250 tumor-associated antigen allows targeted gene transfer to human renal cell carcinoma in vitro. Cancer Gene Ther. 1999, 6, 564-571
39. Genega, E.M.; Ghebremichael, M.; Najarian, R.; Fu, Y.N.; Wang, Y.H.; Argani, P.; Grisanzio, C.; Signoretti, S. Carbonic anhydrase ix expression in renal neoplasms correlation with tumor type and grade. Am. J. Clin. Pathol. 2010, 134, 873-879
40. Van Schaijk, F.G.; Broekema, M.; Oosterwijk, E.; van Eerd, J.E.; McBride, B.J.; Goldenberg, D.M.; Corstens, F.H.; Boerman, O.C. Residualizing iodine markedly improved tumor targeting using bispecific antibody-based pretargeting. J. Nucl. Med. 2005, 46, 1016-1022
41. Brouwers, A.H.; van Eerd, J.E.; Frielink, C.; Oosterwijk, E.; Oyen, W.J.; Corstens, F.H.; Boerman, O.C. Optimization of radioimmunotherapy of renal cell carcinoma: Labeling of monoclonal antibody cg250 with 131I, 90Y, 177Lu, or 186Re. J. Nucl. Med. 2004, 45, 327-337
42. Steffens, M.G.; Boerman, O.C.; de Mulder, P.H.; Oyen, W.J.; Buijs, W.C.; Witjes, J.A.; van den Broek, W.J.; Oosterwijk-Wakka, J.C.; Debruyne, F.M.; Corstens, F.H. et al. Phase I radioimmunotherapy of metastatic renal cell carcinoma with 131I-labeled chimeric monoclonal antibody g250. Clin. Cancer Res. 1999, 5, 3268S-3274S.
43. Divgi, C.R.; O'Donoghue, J.A.; Welt, S.; O'Neel, J.; Finn, R.; Motzer, R.J.; Jungbluth, A.; Hoffman, E.; Ritter, G.; Larson, S.M. et al. Phase I clinical trial with fractionated radioimmunotherapy using 131I-labeled chimeric g250 in metastatic renal cancer. J. Nuclear Med. 2004, 45, 1412-1421
44. Brouwers, A.H.; Mulders, P.F.; de Mulder, P.H.; van den Broek, W.J.; Buijs, W.C.; Mala, C.; Joosten, F.B.; Oosterwijk, E.; Boerman, O.C.; Corstens, F.H. et al. Lack of efficacy of two consecutive treatments of radioimmunotherapy with 131I-cg250 in patients with metastasized clear cell renal cell carcinoma. J. Clin. Oncol. 2005, 23, 6540-6548
45. Stillebroer, A.B.; Boerman, O.C.; Desar, I.M.; Boers-Sonderen, M.J.; van Herpen, C.M.; Langenhuijsen, J.F.; Smith-Jones, P.M.; Oosterwijk, E.; Oyen, W.J.; Mulders, P.F. Phase 1 radioimmunotherapy study with lutetium 177-labeled anti-carbonic anhydrase IX monoclonal antibody girentuximab in patients with advanced renal cell carcinoma. Eur. Urol. 2012, doi:10.1016/j.eururo.2012.08.024
46. Davis, I.D.; Wiseman, G.A.; Lee, F.T.; Gansen, D.N.; Hopkins, W.; Papenfuss, A.T.; Liu, Z.; Moynihan, T.J.; Croghan, G.A.; Adjei, A.A.; et al. A phase i multiple dose, dose escalation study of cg250 monoclonal antibody in patients with advanced renal cell carcinoma. Cancer Immun. 2007, 7, 13
47. Bleumer, I.; Knuth, A.; Oosterwijk, E.; Hofmann, R.; Varga, Z.; Lamers, C.; Kruit, W.; Melchior, S.; Mala, C.; Ullrich, S.; et al. A phase ii trial of chimeric monoclonal antibody g250 for advanced renal cell carcinoma patients. Br. J. Cancer 2004, 90, 985-990
48. WILEX Ariser, adjuvant rencarex® immunotherapy phase iii trial to study efficacy in non-metastatic rcc. Available online: http://www.wilex.de/portfolio-english/rencarex/phase-iii-ariser/(accessed on 28 April 2013).
49. Davis, I.D.; Liu, Z.; Saunders, W.; Lee, F.T.; Spirkoska, V.; Hopkins, W.; Smyth, F.E.; Chong, G.; Papenfuss, A.T.; Chappell, B.; et al. A pilot study of monoclonal antibody cg250 and low dose subcutaneous il-2 in patients with advanced renal cell carcinoma. Cancer Immun. 2007, 7, 14
50. Bleumer, I.; Oosterwijk, E.; Oosterwijk-Wakka, J.C.; Voller, M.C.; Melchior, S.; Warnaar, S.O.; Mala, C.; Beck, J.; Mulders, P.F. A clinical trial with chimeric monoclonal antibody wx-g250 and low dose interleukin-2 pulsing scheme for advanced renal cell carcinoma. J. Urol. 2006, 175, 57-62
51. Siebels, M.; Rohrmann, K.; Oberneder, R.; Stahler, M.; Haseke, N.; Beck, J.; Hofmann, R.; Kindler, M.; Kloepfer, P.; Stief, C. A clinical phase I/II trial with the monoclonal antibody cg250 (rencarex(r)) and interferon-alpha-2a in metastatic renal cell carcinoma patients. World J. Urol. 2011, 29, 121-126
52. Brouwers, A.H.; Buijs, W.C.; Mulders, P.F.; de Mulder, P.H.; van den Broek, W.J.; Mala, C.; Oosterwijk, E.; Boerman, O.C.; Corstens, F.H.; Oyen, W.J. Radioimmunotherapy with [131I]cg250 in patients with metastasized renal cell cancer: Dosimetric analysis and immunologic response. Clin. Cancer Res. 2005, 11, 7178S-7186S.
53. Sharkey, R.M.; Behr, T.M.; Mattes, M.J.; Stein, R.; Griffiths, G.L.; Shih, L.B.; Hansen, H.J.; Blumenthal, R.D.; Dunn, R.M.; Juweid, M.E.; et al. Advantage of residualizing radiolabels for an internalizing antibody against the b-cell lymphoma antigen, cd22. Cancer Immunol. Immunother. 1997, 44, 179-188
54. Stillebroer, A.B.; Zegers, C.M.; Boerman, O.C.; Oosterwijk, E.; Mulders, P.F.; O'Donoghue, J.A.; Visser, E.P.; Oyen, W.J. Dosimetric analysis of 177Lu-cg250 radioimmunotherapy in renal cell carcinoma patients: Correlation with myelotoxicity and pretherapeutic absorbed dose predictions based on 111In-cg250 imaging. J. Nucl. Med. 2012, 53, 82-89
55. Surfus, J.E.; Hank, J.A.; Oosterwijk, E.; Welt, S.; Lindstrom, M.J.; Albertini, M.R.; Schiller, J.H.; Sondel, P.M. Anti-renal-cell carcinoma chimeric antibody g250 facilitates antibody-dependent cellular cytotoxicity with in vitro and in vivo interleukin-2-activated effectors. J. Immunother. Emphasis Tumor Immunol. 1996, 19, 184-191
56. Liu, Z.; Smyth, F.E.; Renner, C.; Lee, F.T.; Oosterwijk, E.; Scott, A.M. Anti-renal cell carcinoma chimeric antibody g250: Cytokine enhancement of in vitro antibody-dependent cellular cytotoxicity. Cancer Immunol. Immunother. 2002, 51, 171-177
57. Brouwers, A.H.; Frielink, C.; Oosterwijk, E.; Oyen, W.J.; Corstens, F.H.; Boerman, O.C. Interferons can upregulate the expression of the tumor associated antigen g250-mn/ca IX, a potential target for (radio)immunotherapy of renal cell carcinoma. Cancer Biother. Radiopharm. 2003, 18, 539-547
58. Bui, M.H.; Seligson, D.; Han, K.R.; Pantuck, A.J.; Dorey, F.J.; Huang, Y.; Horvath, S.; Leibovich, B.C.; Chopra, S.; Liao, S.Y.; et al. Carbonic anhydrase IX is an independent predictor of survival in advanced renal clear cell carcinoma: Implications for prognosis and therapy. Clin. Cancer Res. 2003, 9, 802-811
59. Bui, M.H.; Visapaa, H.; Seligson, D.; Kim, H.; Han, K.R.; Huang, Y.; Horvath, S.; Stanbridge, E.J.; Palotie, A.; Figlin, R.A.; et al. Prognostic value of carbonic anhydrase IX and ki67 as predictors of survival for renal clear cell carcinoma. J. Urol. 2004, 171, 2461-2466
60. Atkins, M.; Regan, M.; McDermott, D.; Mier, J.; Stanbridge, E.; Youmans, A.; Febbo, P.; Upton, M.; Lechpammer, M.; Signoretti, S. Carbonic anhydrase ix expression predicts outcome of interleukin 2 therapy for renal cancer. Clin. Cancer Res. 2005, 11, 3714-3721
61. Dudek, A.Z.; Yee, R.T.; Manivel, J.C.; Isaksson, R.; Yee, H.O. Carbonic anhydrase ix expression is associated with improved outcome of high-dose interleukin-2 therapy for metastatic renal cell carcinoma. Anticancer Res. 2010, 30, 987-992
62. Smith, I.; Procter, M.; Gelber, R.D.; Guillaume, S.; Feyereislova, A.; Dowsett, M.; Goldhirsch, A.; Untch, M.; Mariani, G.; Baselga, J.; et al. 2-year follow-up of trastuzumab after adjuvant chemotherapy in her2-positive breast cancer: A randomised controlled trial. Lancet 2007, 369, 29-36
63. Lamers, C.H.; Sleijfer, S.; Vulto, A.G.; Kruit, W.H.; Kliffen, M.; Debets, R.; Gratama, J.W.; Stoter, G.; Oosterwijk, E. Treatment of metastatic renal cell carcinoma with autologous t-lymphocytes genetically retargeted against carbonic anhydrase IX: First clinical experience. J. Clin. Oncol. 2006, 24, e20-e22
64. Lamers, C.H.; Sleijfer, S.; van Steenbergen, S.; van Elzakker, P.; van Krimpen, B.; Groot, C.; Vulto, A.; den Bakker, M.; Oosterwijk, E.; Debets, R.; et al. Treatment of metastatic renal cell carcinoma with caix car-engineered t cells: Clinical evaluation and management of on-target toxicity. Mol. Ther. 2013, 21, 904-912
65. Oosterwijk-Wakka, J.C.; Kats-Ugurlu, G.; Leenders, W.P.; Kiemeney, L.A.; Old, L.J.; Mulders, P.F.; Oosterwijk, E. Effect of tyrosine kinase inhibitor treatment of renal cell carcinoma on the accumulation of carbonic anhydrase IX-specific chimeric monoclonal antibody cg250. BJU Int. 2011, 107, 118-125
66. Muselaers, S.; Boerman, O.; Stillebroer, A.; Desar, I.; Sonderen, M.; van Herpen, C.; Oosterwijk, E.; Leenders, W.; Mulders, P.; Oyen, W. Sorafenib decreases indium-111-girentuximab tumor uptake in clear cell renal cell carcinoma patients. J. Nuc. Med. 2012, 53, 27
67. Murri-Plesko, M.T.; Hulikova, A.; Oosterwijk, E.; Scott, A.M.; Zortea, A.; Harris, A.L.; Ritter, G.; Old, L.; Bauer, S.; Swietach, P.; et al. Antibody inhibiting enzymatic activity of tumour-associated carbonic anhydrase isoform IX. Eur. J. Pharmacol. 2011, 657, 173-183.