Evaluation of Nonpeptidic Ligand Conjugates for SPECT Imaging of Hypoxic and Carbonic Anhydrase IX-Expressing Cancers

Bioconjugate Chemistry

Volumn 27, Issue 7, 2016, Pages 1762-1769

  Lv, Peng Cheng ^a,b   Putt, Karson S ^a   Low, Philip S ^a,b  

^a PURDUE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBONIC ANHYDRASE; CHELATION; DISEASES; GENE EXPRESSION; IONIZING RADIATION; LIGANDS;

ANTICANCER TREATMENT; CHEMOTHERAPEUTIC DRUGS; CLINICAL CARE; GENE EXPRESSION PATTERNS; IMAGING AGENT; LOCALISED; NONPEPTIDIC LIGANDS; PRIORI KNOWLEDGE; SPECT IMAGING; VASCULATURE;

TUMORS;

CARBONATE DEHYDRATASE IX; LIGAND; PROLINE DERIVATIVE; RHODAMINE; TECHNETIUM 99M; CARBONATE DEHYDRATASE INHIBITOR; MACROGOL; TECHNETIUM;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; CANCER CELL; CELL MEMBRANE; CHELATION; CHEMICAL STRUCTURE; CONJUGATE; DISTRIBUTION PARAMETERS; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; HYDROPHILICITY; HYPOXEMIA; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR STABILITY; MOUSE; NEOPLASM; NONHUMAN; PROTEIN EXPRESSION; RADIOACTIVITY; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; SURFACE AREA; SYNTHESIS; TIME; TUMOR XENOGRAFT; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL TRANSFORMATION; CHEMISTRY; GENE EXPRESSION REGULATION; HT-29 CELL LINE; MALE; METABOLISM; PROCEDURES; SINGLE PHOTON EMISSION COMPUTED TOMOGRAPHY; TISSUE DISTRIBUTION; TUMOR HYPOXIA;

ANIMALS; CARBONIC ANHYDRASE INHIBITORS; CARBONIC ANHYDRASE IX; CELL TRANSFORMATION, NEOPLASTIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HT29 CELLS; HUMANS; LIGANDS; MALE; MICE; POLYETHYLENE GLYCOLS; RHODAMINES; TECHNETIUM; TISSUE DISTRIBUTION; TOMOGRAPHY, EMISSION-COMPUTED, SINGLE-PHOTON; TUMOR HYPOXIA;

EID: 84979282978     PISSN: 10431802     EISSN: 15204812     Source Type: Journal    
DOI: 10.1021/acs.bioconjchem.6b00271     Document Type: Article

References (70)

1. Noman, M. Z., Hasmim, M., Messai, Y., Terry, S., Kieda, C., Janji, B., and Chouaib, S. (2015) Hypoxia: a key player in anti-tumor immune response. A review in the Theme: Cellular Responses to Hypoxia Am. J. Physiol Cell Physiol. 309 (9) C569-C579 10.1152/ajpcell.00207.2015
2. Scanlon, S. E. and Glazer, P. M. (2015) Multifaceted control of DNA repair pathways by the hypoxic tumor microenvironment DNA Repair 32, 180-189 10.1016/j.dnarep.2015.04.030
3. Span, P. N. and Bussink, J. (2015) Biology of hypoxia Semin. Nucl. Med. 45, 101-109 10.1053/j.semnuclmed.2014.10.002
4. Harris, B. H., Barberis, A., West, C. M., and Buffa, F. M. (2015) Gene Expression Signatures as Biomarkers of Tumour Hypoxia Clin Oncol (R Coll Radiol1). 27 (10) 547-560 10.1016/j.clon.2015.07.004
5. Harris, A. L. (2002) Hypoxia-a key regulatory factor in tumour growth Nat. Rev. Cancer 2 (1) 38-47 10.1038/nrc704
6. Yamada, S., Utsunomiya, T., Morine, Y., Imura, S., Ikemoto, T., Arakawa, Y., Kanamoto, M., Iwahashi, S., Saito, Y., and Takasu, C. et al. 2014, Expressions of hypoxia-inducible factor-1 and epithelial cell adhesion molecule are linked with aggressive local recurrence of hepatocellular carcinoma after radiofrequency ablation therapy Ann. Surg Oncol. 21, S436-S442 10.1245/s10434-014-3575-z
7. Karakashev, S. V. and Reginato, M. J. (2015) Progress toward overcoming hypoxia-induced resistance to solid tumor therapy Cancer Manage. Res. 7, 253-264 10.2147/CMAR.S58285
8. DeClerck, K. and Elble, R. C. (2010) The role of hypoxia and acidosis in promoting metastasis and resistance to chemotherapy Front. Biosci., Landmark Ed. 15, 213-225 10.2741/3616
9. Byers, L. A., Holsinger, F. C., Kies, M. S., William, W. N., El-Naggar, A. K., Lee, J. J., Hu, J., Lopez, A., Tran, H. T., and Yan, S. et al. 2010, Serum signature of hypoxia-regulated factors is associated with progression after induction therap4y in head and neck squamous cell cancer Mol. Cancer Ther. 9 (6) 1755-1763 10.1158/1535-7163.MCT-09-1047
10. Swinson, D. E., Jones, J. L., Richardson, D., Wykoff, C., Turley, H., Pastorek, J., Taub, N., Harris, A. L., and O'Byrne, K. J. (2003) 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. 21, 473-482 10.1200/JCO.2003.11.132
11. Kim, S. J., Rabbani, Z. N., Dewhirst, M. W., Vujaskovic, Z., Vollmer, R. T., Schreiber, E. G., Oosterwijk, E., and Kelley, M. J. (2005) Expression of HIF-1alpha, CA IX, VEGF, and MMP-9 in surgically resected non-small cell lung cancer Lung Cancer. 49, 325-335 10.1016/j.lungcan.2005.03.036
12. Ilie, M., Mazure, N. M., Hofman, V., Ammadi, R. E., Ortholan, C., Bonnetaud, C., Havet, K., Venissac, N., Mograbi, B., and Mouroux, J. et al. 2010, High levels of carbonic anhydrase IX in tumour tissue and plasma are biomarkers of poor prognostic in patients with non-small cell lung cancer Br. J. Cancer 102, 1627-1635 10.1038/sj.bjc.6605690
13. Saarnio, J., Parkkila, S., Parkkila, A. K., Haukipuro, K., Pastorekova, S., Pastorek, J., Kairaluoma, M. I., and Karttunen, T. J. (1998) Immunohistochemical study of colorectal tumors for expression of a novel transmembrane carbonic anhydrase, MN/CA IX, with potential value as a marker of cell proliferation Am. J. Pathol. 153, 279-285 10.1016/S0002-9440(10)65569-1
14. Korkeila, E., Talvinen, K., Jaakkola, P. M., Minn, H., Syrjanen, K., Sundstrom, J., and Pyrhonen, S. (2009) Expression of carbonic anhydrase IX suggests poor outcome in rectal cancer Br. J. Cancer 100, 874-880 10.1038/sj.bjc.6604949
15. Niemela, A. M., Hynninen, P., Mecklin, J. P., Kuopio, T., Kokko, A., Aaltonen, L., Parkkila, A. K., Pastorekova, S., Pastorek, J., and Waheed, A. et al. 2007, Carbonic anhydrase IX is highly expressed in hereditary nonpolyposis colorectal cancer Cancer Epidemiol., Biomarkers Prev. 16, 1760-1766 10.1158/1055-9965.EPI-07-0080
16. Chen, J., Rocken, C., Hoffmann, J., Kruger, S., Lendeckel, U., Rocco, A., Pastorekova, S., Malfertheiner, P., and Ebert, M. P. (2005) Expression of carbonic anhydrase 9 at the invasion front of gastric cancers Gut. 54, 920-927
17. Juhasz, M., Chen, J., Lendeckel, U., Kellner, U., Kasper, H. U., Tulassay, Z., Pastorekova, S., Malfertheiner, P., and Ebert, M. P. (2003) Expression of carbonic anhydrase IX in human pancreatic cancer Aliment. Pharmacol. Ther. 18, 837-846 10.1046/j.1365-2036.2003.01738.x
18. Chia, S. K., Wykoff, C. C., Watson, P. H., Han, C., Leek, R. D., Pastorek, J., Gatter, K. C., Ratcliffe, P., and Harris, A. L. (2001) Prognostic significance of a novel hypoxia-regulated marker, carbonic anhydrase IX, in invasive breast carcinoma J. Clin Oncol. 19, 3660-3668
19. Trastour, C., Benizri, E., Ettore, F., Ramaioli, A., Chamorey, E., Pouyssegur, J., and Berra, E. (2007) HIF-1alpha and CA IX staining in invasive breast carcinomas: prognosis and treatment outcome Int. J. Cancer 120, 1451-1458 10.1002/ijc.22436
20. Tan, E. Y., Yan, M., Campo, L., Han, C., Takano, E., Turley, H., Candiloro, I., Pezzella, F., Gatter, K. C., Millar, E. K., O'Toole, S. A., McNeil, C. M., Crea, P., Segara, D., Sutherland, R. L., Harris, A. L., and Fox, S. B. (2009) The key hypoxia regulated gene CAIX is upregulated in basal-like breast tumours and is associated with resistance to chemotherapy Br. J. Cancer 100, 405-411 10.1038/sj.bjc.6604844
21. Hussain, S. A., Ganesan, R., Reynolds, G., Gross, L., Stevens, A., Pastorek, J., Murray, P. G., Perunovic, B., Anwar, M. S., and Billingham, L. et al. 2007, Hypoxia-regulated carbonic anhydrase IX expression is associated with poor survival in patients with invasive breast cancer Br. J. Cancer 96, 104-109 10.1038/sj.bjc.6603530
22. Neumeister, V. M., Sullivan, C. A., Lindner, R., Lezon-Geyda, K., Li, J., Zavada, J., Martel, M., Glazer, P. M., Tuck, D. P., and Rimm, D. L. et al. 2012, Hypoxia-induced protein CAIX is associated with somatic loss of BRCA1 protein and pathway activity in triple negative breast cancer Breast Cancer Res. Treat. 136, 67-75 10.1007/s10549-012-2232-0
23. Loncaster, J. A., Harris, A. L., Davidson, S. E., Logue, J. P., Hunter, R. D., Wycoff, C. C., Pastorek, J., Ratcliffe, P. J., Stratford, I. J., and West, C. M. (2001) Carbonic anhydrase (CA IX) expression, a potential new intrinsic marker of hypoxia: correlations with tumor oxygen measurements and prognosis in locally advanced carcinoma of the cervix Cancer Res. 61, 6394-6399
24. Kim, J. Y., Shin, H. J., Kim, T. H., Cho, K. H., Shin, K. H., Kim, B. K., Roh, J. W., Lee, S., Park, S. Y., and Hwang, Y. J. et al. 2006, Tumor-associated carbonic anhydrases are linked to metastases in primary cervical cancer J. Cancer Res. Clin. Oncol. 132, 302-308 10.1007/s00432-005-0068-2
25. Lee, S., Shin, H. J., Han, I. O., Hong, E. K., Park, S. Y., Roh, J. W., Shin, K. H., Kim, T. H., and Kim, J. Y. (2007) Tumor carbonic anhydrase 9 expression is associated with the presence of lymph node metastases in uterine cervical cancer Cancer Sci. 98, 329-333 10.1111/j.1349-7006.2007.00396.x
26. Woelber, L., Kress, K., Kersten, J. F., Choschzick, M., Kilic, E., Herwig, U., Lindner, C., Schwarz, J., Jaenicke, F., and Mahner, S. et al. 2011, Carbonic anhydrase IX in tumor tissue and sera of patients with primary cervical cancer BMC Cancer 11, 12 10.1186/1471-2407-11-12
27. Hoskin, P. J., Sibtain, A., Daley, F. M., and Wilson, G. D. (2003) GLUT1 and CAIX as intrinsic markers of hypoxia in bladder cancer: relationship with vascularity and proliferation as predictors of outcome of ARCON Br. J. Cancer 89, 1290-1297 10.1038/sj.bjc.6601260
28. Klatte, T., Seligson, D. B., Rao, J. Y., Yu, H., de Martino, M., Kawaoka, K., Wong, S. G., Belldegrun, A. S., and Pantuck, A. J. (2009) Carbonic anhydrase IX in bladder cancer: a diagnostic, prognostic, and therapeutic molecular marker Cancer 115, 1448-1458 10.1002/cncr.24163
29. Choschzick, M., Oosterwijk, E., Muller, V., Woelber, L., Simon, R., Moch, H., and Tennstedt, P. (2011) Overexpression of carbonic anhydrase IX (CAIX) is an independent unfavorable prognostic marker in endometrioid ovarian cancer Virchows Arch. 459, 193-200 10.1007/s00428-011-1105-y
30. Nordfors, K., Haapasalo, J., Korja, M., Niemela, A., Laine, J., Parkkila, A. K., Pastorekova, S., Pastorek, J., Waheed, A., and Sly, W. S. et al. 2010, The tumour-associated carbonic anhydrases CA II, CA IX and CA XII in a group of medulloblastomas and supratentorial primitive neuroectodermal tumours: an association of CA IX with poor prognosis BMC Cancer 10, 148 10.1186/1471-2407-10-148
31. Proescholdt, M. A., Merrill, M. J., Stoerr, E. M., Lohmeier, A., Pohl, F., and Brawanski, A. (2012) Function of carbonic anhydrase IX in glioblastoma multiforme Neuro Oncol. 14, 1357-1366 10.1093/neuonc/nos216
32. Haapasalo, J. A., Nordfors, K. M., Hilvo, M., Rantala, I. J., Soini, Y., Parkkila, A. K., Pastorekova, S., Pastorek, J., Parkkila, S. M., and Haapasalo, H. K. (2006) Expression of carbonic anhydrase IX in astrocytic tumors predicts poor prognosis Clin. Cancer Res. 12, 473-477 10.1158/1078-0432.CCR-05-0848
33. Hoogsteen, I. J., Marres, H. A., Wijffels, K. I., Rijken, P. F., Peters, J. P., van den Hoogen, F. J., Oosterwijk, E., van der Kogel, A. J., and Kaanders, J. H. (2005) Colocalization of carbonic anhydrase 9 expression and cell proliferation in human head and neck squamous cell carcinoma Clin. Cancer Res. 11, 97-106
34. De Schutter, H., Landuyt, W., Verbeken, E., Goethals, L., Hermans, R., and Nuyts, S. (2005) The prognostic value of the hypoxia markers CA IX and GLUT 1 and the cytokines VEGF and IL 6 in head and neck squamous cell carcinoma treated by radiotherapy ± chemotherapy BMC Cancer 5, 42 10.1186/1471-2407-5-42
35. Koukourakis, M. I., Bentzen, S. M., Giatromanolaki, A., Wilson, G. D., Daley, F. M., Saunders, M. I., Dische, S., Sivridis, E., and Harris, A. L. (2006) Endogenous markers of two separate hypoxia response pathways (hypoxia inducible factor 2 alpha and carbonic anhydrase 9) are associated with radiotherapy failure in head and neck cancer patients recruited in the CHART randomized trial J. Clin. Oncol. 24, 727-735 10.1200/JCO.2005.02.7474
36. Eckert, A. W., Kappler, M., Schubert, J., and Taubert, H. (2012) Correlation of expression of hypoxia-related proteins with prognosis in oral squamous cell carcinoma patients Oral Maxillofac Surg. 16, 189-196 10.1007/s10006-012-0335-8
37. Eckert, A. W., Lautner, M. H., Schutze, A., Bolte, K., Bache, M., Kappler, M., Schubert, J., Taubert, H., and Bilkenroth, U. (2009) Co-expression of Hif1alpha and CAIX is associated with poor prognosis in oral squamous cell carcinoma patients J. Oral Pathol. Med. 39, 313-317 10.1111/j.1600-0714.2009.00829.x
38. Choi, S. W., Kim, J. Y., Park, J. Y., Cha, I. H., Kim, J., and Lee, S. (2008) Expression of carbonic anhydrase IX is associated with postoperative recurrence and poor prognosis in surgically treated oral squamous cell carcinoma Hum. Pathol. 39, 1317-1322 10.1016/j.humpath.2007.10.026
39. Maxwell, P. H., Wiesener, M. S., Chang, G. W., Clifford, S. C., Vaux, E. C., Cockman, M. E., Wykoff, C. C., Pugh, C. W., Maher, E. R., and Ratcliffe, P. J. (1999) The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis Nature 399, 271-275 10.1038/20459
40. Liao, S. Y., Aurelio, O. N., Jan, K., Zavada, J., and Stanbridge, E. J. (1997) Identification of the MN/CA9 protein as a reliable diagnostic biomarker of clear cell carcinoma of the kidney Cancer Res. 57, 2827-2831
41. Muriel Lopez, C., Esteban, E., Berros, J. P., Pardo, P., Astudillo, A., Izquierdo, M., Crespo, G., Sanmamed, M., Fonseca, P. J., and Martinez-Camblor, P. (2012) Prognostic factors in patients with advanced renal cell carcinoma Clin. Genitourin. Cancer 10, 262-270 10.1016/j.clgc.2012.06.005
42. Pastorekova, S., Parkkila, S., Parkkila, A. K., Opavsky, R., Zelnik, V., Saarnio, J., and Pastorek, J. (1997) Carbonic anhydrase IX, MN/CA IX: analysis of stomach complementary DNA sequence and expression in human and rat alimentary tracts Gastroenterology 112, 398-408 10.1053/gast.1997.v112.pm9024293
43. Supuran, C. T. (2012) Inhibition of carbonic anhydrase IX as a novel anticancer mechanism World J. Clin Oncol. 3 (7) 98-103 10.5306/wjco.v3.i7.98
44. Pastorek, J. and Pastorekova, S. (2015) Hypoxia-induced carbonic anhydrase IX as a target for cancer therapy: from biology to clinical use Semin. Cancer Biol. 31, 52-64 10.1016/j.semcancer.2014.08.002
45. Sneddon, D. and Poulsen, S. A. (2014) Agents described in the Molecular Imaging and Contrast Agent Database for imaging carbonic anhydrase IX expression J. Enzyme Inhib. Med. Chem. 29 (5) 753-763 10.3109/14756366.2013.848205
46. Tafreshi, N. K., Lloyd, M. C., Bui, M. M., Gillies, R. J., and Morse, D. L. (2014) Carbonic anhydrase IX as an imaging and therapeutic target for tumors and metastases Subcell. Biochem. 75, 221-254 10.1007/978-94-007-7359-2-12
47. Akurathi, V., Dubois, L., Lieuwes, N. G., Chitneni, S. K., Cleynhens, B. J., Vullo, D., Supuran, C. T., Verbruggen, A. M., Lambin, P., and Bormans, G. M. (2010) Synthesis and biological evaluation of a 99m Tc-labelled sulfonamide conjugate for in vivo visualization of carbonic anhydrase IX expression in tumor hypoxia Nucl. Med. Biol. 37 (5) 557-564 10.1016/j.nucmedbio.2010.02.006
48. Akurathi, V., Dubois, L., Celen, S., Lieuwes, N. G., Chitneni, S. K., Cleynhens, B. J., Innocenti, A., Supuran, C. T., Verbruggen, A. M., and Lambin, P. et al. 2014, Development and biological evaluation of 99mTc-sulfonamide derivatives for in vivo visualization of CA IX as surrogate tumor hypoxia markers Eur. J. Med. Chem. 71, 374-384 10.1016/j.ejmech.2013.10.027
49. Pan, J., Lau, J., Mesak, F., Hundal, N., Pourghiasian, M., Liu, Z., Benard, F., Dedhar, S., Supuran, C. T., and Lin, K. S. (2014) Synthesis and evaluation of 18F-labeled carbonic anhydrase IX inhibitors for imaging with positron emission tomography J. Enzyme Inhib. Med. Chem. 29 (2) 249-255 10.3109/14756366.2013.773994
50. Lau, J., Pan, J., Zhang, Z., Hundal-Jabal, N., Liu, Z., Benard, F., and Lin, K. S. (2014) Synthesis and evalulation of (18)F-labeled tertiary benzenesulfonamides for imaging carbonic anhydrase IX expression in tumours with positron emission tomography Bioorg. Med. Chem. Lett. 24 (14) 3064-3068 10.1016/j.bmcl.2014.05.021
51. Bao, B., Groves, K., Zhang, J., Handy, E., Kennedy, P., Cuneo, G., Supuran, C. T., Yared, W., Rajopadhye, M., and Peterson, J. D. (2012) In vivo imaging and quantification of carbonic anhydrase IX expression as an endogenous biomarker of tumor hypoxia PLoS One 7 (11) e50860 10.1371/journal.pone.0050860
52. Lv, P. C., Roy, J., Putt, K. S., and Low, P. S. (2016) Evaluation of a carbonic anhydrase IX-targeted near-infrared dye for fluorescence-guided surgery of hypoxic tumors Mol. Pharmaceutics 13 (5) 1618-1625 10.1021/acs.molpharmaceut.6b00065
53. Ahlskog, J. K., Dumelin, C. E., Trussel, S., Marlind, J., and Neri, D. (2009) In vivo targeting of tumor-associated carbonic anhydrases using acetazolamide derivatives Bioorg. Med. Chem. Lett. 19 (16) 4851-4856 10.1016/j.bmcl.2009.06.022
54. Muselaers, C. H., Rijpkema, M., Bos, D. L., Langenhuijsen, J. F., Oyen, W. J., Mulders, P. F., Oosterwijk, E., and Boerman, O. C. (2015) Radionuclide and Fluorescence Imaging of Clear Cell Renal Cell Carcinoma Using Dual Labeled Anti-Carbonic Anhydrase IX Antibody G250 J. Urol. 194 (2) 532-538 10.1016/j.juro.2015.02.041
55. Muselaers, C. H., Stillebroer, A. B., Rijpkema, M., Franssen, G. M., Oosterwijk, E., Mulders, P. F., Oyen, W. J., and Boerman, O. C. (2014) Optical imaging of renal cell carcinoma with anti-carbonic anhydrase IX monoclonal antibody Girentuximab J. Nucl. Med. 55 (6) 1035-1040 10.2967/jnumed.114.137356
56. Muselaers, C. H., Oosterwijk, E., Bos, D. L., Oyen, W. J., Mulders, P. F., and Boerman, O. C. (2014) Optimizaing lutetium 177-anti-carbonic anhydrase IX radioimmunotherapy in an intraperitoneal clear cell renal cell carcinoma xenograft model Mol. Imaging 13, 1-7
57. Cheal, S. M., Punzalan, B., Doran, M. G., Evans, M. J., Osborne, J. R., Lewis, J. S., Zanzonico, P., and Larson, S. M. (2014) Pairwise comparison of 89ZR- and 124I-labeled cG250 based on positron emission tomography imaging and nonlinear immunokinetic modeling: in vivo carbonic anhydrase IX receptor binding and internalization in mouse xenografts of clear-cell renal carcinoma Eur. J. Nucl. Med. Mol. Imaging 41 (5) 985-994 10.1007/s00259-013-2679-1
58. Hoeben, B. A., Kaanders, J. H., Franssen, G. M., Troost, E. G., Rijken, P. F., Oosterwijk, E., van Dongen, G. A., Oyen, W. J., Boerman, O. C., and Bussink, J. (2010) PET of hypoxia with 89Zr-labeled cG250-F(ab′)2 in head and neck tumors J. Nucl. Med. 51 (7) 1076-1083 10.2967/jnumed.109.073189
59. Li, J., Shi, L., Wang, C., Zhang, X., Jia, L., Li, X., Zhou, W., Qi, Y., and Zhang, L. (2011) Preliminary biological evaluation of 125I-labeled anti-carbonic anhydrase IX monoclonal antibody in the mice bearing HT-29 tumors Nucl. Med. Commun. 32 (12) 1190-1193 10.1097/MNM.0b013e32834bf3e1
60. Chrastina, A., Závada, J., Parkkila, S., Kaluz, S., Kaluzova, M., Rajcáni, J., Pastorek, J., and Pastoreková, S. (2003) Biodistribution and pharmacokinetics of 125I-labeled monoclonal antibody M75 specific for carbonic anhydrase IX, an intrinsic marker of hypoxia, in nude mice xenografted with human colorectal carcinoma Int. J. Cancer 105 (6) 873-881 10.1002/ijc.11142
61. Chrastina, A., Pastoreková, S., and Pastorek, J. (2003) Immunotargeting of human cervical carcinoma xenograft expressing CA IX tumor-associated antigen by 125I-labeled M75 monoclonal antibody Neoplasma 50 (1) 13-21
62. Muselaers, C. H., Stillebroer, A. B., Desar, I. M., Boers-Sonderen, M. J., van Herpen, C. M., de Weijert, M. C., Langenhuijsen, J. F., Oosterwijk, E., Leenders, W. P., and Boerman, O. C. et al. 2014, Tyrosine kinase inhibitor sorafenib decreases 111In-girentuximab uptake in patients with clear cell renal cell carcinoma J. Nucl. Med. 55 (2) 242-247 10.2967/jnumed.113.131110
63. Muselaers, C. H., Boerman, O. C., Oosterwijk, E., Langenhuijsen, J. F., Oyen, W. J., and Mulders, P. F. (2013) Indium-111-labeled girentuximab immunoSPECT as a diagnostic tool in clear cell renal cell carcinoma Eur. Urol. 63 (6) 1101-1106 10.1016/j.eururo.2013.02.022
64. Pryma, D. A., O'Donoghue, J. A., Humm, J. L., Jungbluth, A. A., Old, L. J., Larson, S. M., and Divgi, C. R. (2011) Correlation of in vivo and in vitro measures of carbonic anhydrase IX antigen expression in renal masses using antibody 124I-cG250 J. Nucl. Med. 52 (4) 535-540 10.2967/jnumed.110.083295
65. 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., and Corstens, F. H. et al. 1997, Targeting of renal cell carcinoma with iodine-131-labeled chimeric monoclonal antibody G250 J. Clin Oncol. 15 (4) 1529-1537
66. Divgi, C. R., Pandit-Taskar, N., Jungbluth, A. A., Reuter, V. E., Gönen, M., Ruan, S., Pierre, C., Nagel, A., Pryma, D. A., and Humm, J. et al. 2007, Preoperative characterization 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. 8 (4) 304-310 10.1016/S1470-2045(07)70044-X
67. Rami, M., Winum, J. Y., Innocenti, A., Montero, J. L., Scozzafava, A., and Supuran, C. T. (2008) Carbonic anhydrase inhibitors: copper(II) complexes of polyamino-polycarboxylamido aromatic/heterocyclic sulfonamides are very potent inhibitors of the tumor-associated isoforms of IX and XII Bioorg. Med. Chem. Lett. 18 (2) 836-841 10.1016/j.bmcl.2007.11.025
68. Pacchiano, F., Carta, F., McDonald, P. C., Lou, Y., Vullo, D., Scozzafava, A., Dedhar, S., and Supuran, C. T. (2011) Ureido-substituted benzenesulfonamides potently inhibit carbonic anhydrase IX and show antimetastatic activity in a model of breast cancer metastasis J. Med. Chem. 54 (6) 1896-1902 10.1021/jm101541x
69. Lau, J., Liu, Z., Lin, K. S., Pan, J., Zhang, Z., Vullo, D., Supuran, C. T., Perrin, D. M., and Benard, F. (2015) Trimeric radiofluorinated sulfonamide derivatives to achieve in vivo selectivity for carbonic anhydrase IX-targeted PET imaging J. Nucl. Med. 56 (9) 1434-1440 10.2967/jnumed.114.153288
70. Cherry, S. R., Sorenson, J. A., and Phelps, M. E. (2012) Physics in Nuclear Medicine, p 4, Elsevier Health Sciences, Philadelphia, PA.