Preclinical evaluation of the novel monoclonal antibody H6-11 for prostate cancer imaging

Molecular Pharmaceutics

Volumn 10, Issue 10, 2013, Pages 3655-3664

  Jin, Hongjun ^a   Xu, Mai ^a   Padakanti, Prashanth K ^a   Liu, Yongjian ^a   Lapi, Suzanne ^a   Tu, Zhude ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Glycosylation; MAb; O GlcNAc; PC 3; Positron emission tomography (PET); Prostate cancer; Tumor associated carbohydrate antigens (TACA)

Indexed keywords

EPITOPE; IODINE 125; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY H6 11; RADIOISOTOPE; UNCLASSIFIED DRUG; ZIRCONIUM 89;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY SPECIFICITY; ANTIGEN BINDING; ARTICLE; CANCER CELL CULTURE; CANCER DIAGNOSIS; CONTROLLED STUDY; DIAGNOSTIC VALUE; DRUG ACCUMULATION; FLUORESCENCE IMAGING; GLYCOSYLATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR PROBE; MOUSE; NONHUMAN; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROSTATE ADENOCARCINOMA; PROSTATE CANCER; TUMOR XENOGRAFT;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, TUMOR-ASSOCIATED, CARBOHYDRATE; CELL LINE, TUMOR; DIAGNOSTIC IMAGING; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GLYCOSYLATION; HUMANS; MALE; MICE; MICE, INBRED BALB C; POSITRON-EMISSION TOMOGRAPHY; PROSTATIC NEOPLASMS;

EID: 84888321789     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp400130w     Document Type: Article

References (56)

1. Tesarova, P.; Kalousova, M.; Trnkova, B.; Soukupova, J.; Argalasova, S.; Mestek, O.; Petruzelka, L.; Zima, T. Carbonyl and oxidative stress in patients with breast cancer-is there a relation to the stage of the disease? Neoplasma 2007, 54 (3), 219-224.
2. Kumar, S. R.; Sauter, E. R.; Quinn, T. P.; Deutscher, S. L. Thomsen-Friedenreich and Tn antigens in nipple fluid: Carbohydrate biomarkers for breast cancer detection. Clin. Cancer Res. 2005, 11 (19 Pt 1), 6868-6871.
3. Glinskii, O. V.; Sud, S.; Mossine, V. V.; Mawhinney, T. P.; Anthony, D. C.; Glinsky, G. V.; Pienta, K. J.; Glinsky, V. V. Inhibition of prostate cancer bone metastasis by synthetic TF antigen mimic/galectin-3 inhibitor lactulose-L-leucine. Neoplasia (New York, NY) 2012, 14 (1), 65-73.
4. Khabaz, M. N.; McClure, J.; McClure, S.; Stoddart, R. W. Glycophenotype of prostatic carcinomas. Folia Histochem. Cytobiol. 2010, 48 (4), 637-645.
5. Mariano, A.; Di Carlo, A.; Santonastaso, C.; Oliva, A.; D'Armiento, M.; Macchia, V. Expression of Lewis carbohydrate antigens and chromogranin A in human prostatic cancer. Int. J. Oncol. 2000, 17 (1), 167-171.
6. Marczynska, A.; Kulpa, J.; Lenko, J.; Bugajski, A.; Wojcik, E. CA-50 serum level in patients with prostate cancer. Urol. Res. 1990, 18 (3), 189-191.
7. Abel, P. D.; Cornell, C.; Buamah, P. K.; Williams, G. Assessment of serum CA 19.9 as a tumour marker in patients with carcinoma of the bladder and prostate. Br. J. Urol. 1987, 59 (5), 427-429.
8. Moore, L. E.; Pfeiffer, R. M.; Zhang, Z.; Lu, K. H.; Fung, E. T.; Bast, R. C., Jr. Proteomic biomarkers in combination with CA 125 for detection of epithelial ovarian cancer using prediagnostic serum samples from the Prostate, Lung, Colorectal, and Ovarian (PLCO) Cancer Screening Trial. Cancer 2012, 118 (1), 91-100.
9. Xu, M.; Yuan, Y.; Xia, Y.; Achilefu, S. Monoclonal antibody CC188 binds a carbohydrate epitope expressed on the surface of both colorectal cancer stem cells and their differentiated progeny. Clin. Cancer Res. 2008, 14 (22), 7461-7469.
10. Bergeron, A.; LaRue, H.; Fradet, Y. Biochemical analysis of a bladder-cancer-associated mucin: Structural features and epitope characterization. Biochem. J. 1997, 321 (Pt 3), 889-895.
11. Li, Q.; Anver, M. R.; Butcher, D. O.; Gildersleeve, J. C. Resolving conflicting data on expression of the Tn antigen and implications for clinical trials with cancer vaccines. Mol. Cancer Ther. 2009, 8 (4), 971-979.
12. Slovin, S. F.; Ragupathi, G.; Musselli, C.; Fernandez, C.; Diani, M.; Verbel, D.; Danishefsky, S.; Livingston, P.; Scher, H. I. Thomsen-Friedenreich (TF) antigen as a target for prostate cancer vaccine: Clinical trial results with TF cluster (c)-KLH plus QS21 conjugate vaccine in patients with biochemically relapsed prostate cancer. Cancer Immunol. Immunother. 2005, 54 (7), 694-702.
13. Martensson, S.; Bigler, S. A.; Brown, M.; Lange, P. H.; Brawer, M. K.; Hakomori, S. Sialyl-Lewisx and related carbohydrate antigens in the prostate. Hum. Pathol. 1995, 26 (7), 735-739.
14. Wang, C. C.; Huang, Y. L.; Ren, C. T.; Lin, C. W.; Hung, J. T.; Yu, J. C.; Yu, A. L.; Wu, C. Y.; Wong, C. H. Glycan microarray of Globo H and related structures for quantitative analysis of breast cancer. Proc Natl Acad Sci USA 2008, 105 (33), 11661-6.
15. Chang, W. W.; Lee, C. H.; Lee, P.; Lin, J.; Hsu, C. W.; Hung, J. T.; Lin, J. J.; Yu, J. C.; Shao, L. E.; Yu, J.; Wong, C. H.; Yu, A. L. Expression of Globo H and SSEA3 in breast cancer stem cells and the involvement of fucosyl transferases 1 and 2 in Globo H synthesis. Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (33), 11667-72.
16. Gilewski, T.; Ragupathi, G.; Bhuta, S.; Williams, L. J.; Musselli, C.; Zhang, X. F.; Bornmann, W. G.; Spassova, M.; Bencsath, K. P.; Panageas, K. S.; Chin, J.; Hudis, C. A.; Norton, L.; Houghton, A. N.; Livingston, P. O.; Danishefsky, S. J. Immunization of metastatic breast cancer patients with a fully synthetic globo H conjugate: A phase I trial. Proc. Natl. Acad. Sci. U.S.A. 2001, 98 (6), 3270-3275.
17. LaRue, H.; Parent-Vaugeois, C.; Bergeron, A.; Champetier, S.; Fradet, Y. Influence of spatial configuration on the expression of carcinoembryonic antigen and mucin antigens in human bladder cancer. Int. J. Cancer 1997, 71 (6), 986-992.
18. Xu, M.; Rettig, M. P.; Sudlow, G.; Wang, B.; Akers, W. J.; Cao, D.; Mutch, D. G.; DiPersio, J. F.; Achilefu, S. Preclinical evaluation of Mab CC188 for ovarian cancer imaging. Int. J. Cancer 2012, 131 (6), 1351-1359.
19. Urban, N.; Thorpe, J. D.; Bergan, L. A.; Forrest, R. M.; Kampani, A. V.; Scholler, N.; O'Briant, K. C.; Anderson, G. L.; Cramer, D. W.; Berg, C. D.; McIntosh, M. W.; Hartge, P.; Drescher, C. W. Potential role of HE4 in multimodal screening for epithelial ovarian cancer. J. Natl. Cancer Inst. 2011, 103 (21), 1630-1634.
20. Donadio, A. C.; Lobo, C.; Tosina, M.; de la Rosa, V.; Martin-Rufian, M.; Campos-Sandoval, J. A.; Mates, J. M.; Marquez, J.; Alonso, F. J.; Segura, J. A. Antisense glutaminase inhibition modifies the OGlcNAc pattern and flux through the hexosamine pathway in breast cancer cells. J. Cell Biochem. 2008, 103 (3), 800-811.
21. Havaki, S.; Kittas, C.; Marinos, E.; Dafni, U.; Sotiropoulou, C.; Voloudakis-Baltatzis, I.; Goutas, N.; Vassilaros, S. D.; Athanasiou, E.; Arvanitis, D. L. Ultrastructural immunostaining of infiltrating ductal breast carcinomas with the monoclonal antibody H: A comparative study with cytokeratin 8. Ultrastruct. Pathol. 2003, 27 (6), 393-407.
22. Firpo, M. A.; Gay, D. Z.; Granger, S. R.; Scaife, C. L.; DiSario, J. A.; Boucher, K. M.; Mulvihill, S. J. Improved diagnosis of pancreatic adenocarcinoma using haptoglobin and serum amyloid A in a panel screen. World J. Surg. 2009, 33 (4), 716-722.
23. Zhang, Z.; Yu, Y.; Xu, F.; Berchuck, A.; van Haaften-Day, C.; Havrilesky, L. J.; de Bruijn, H. W.; van der Zee, A. G.; Woolas, R. P.; Jacobs, I. J.; Skates, S.; Chan, D. W.; Bast, R. C., Jr. Combining multiple serum tumor markers improves detection of stage I epithelial ovarian cancer. Gynecol. Oncol. 2007, 107 (3), 526-531.
24. Chaturvedi, R.; Heimburg, J.; Yan, J.; Koury, S.; Sajjad, M.; Abdel-Nabi, H. H.; Rittenhouse-Olson, K. Tumor immunolocalization using 124I-iodine-labeled JAA-F11 antibody to Thomsen-Friedenreich alpha-linked antigen. Appl. Radiat. Isot. 2008, 66 (3), 278-287.
25. Lieberman, G.; Buscombe, J. R.; Hilson, A. J.; Reid, W. M.; Thakrar, D.; Maclean, A. B. Preoperative diagnosis of ovarian carcinoma with a novel monoclonal antibody. Am. J. Obstet. Gynecol. 2000, 183 (3), 534-540.
26. Tibben, J. G.; Massuger, L. F.; Claessens, R. A.; Schijf, C. P.; Pak, K. Y.; Strijk, S. P.; Kenemans, P.; Corstens, F. H. Tumour detection and localization using 99mTc-labelled OV-TL 3 Fab' in patients suspected of ovarian cancer. Nucl. Med. Commun. 1992, 13 (12), 885-893.
27. Xu, M.; Wright, W. D.; Higashikubo, R.; Roti, J. L. Chronic thermotolerance with continued cell proliferation. Int. J. Hyperthermia 1996, 12 (5), 645-660 discussion 661-662.
28. Thean, E. T.; Toh, B. H. Production and characterization of murine monoclonal antibody to human alpha-lactalbumin. Immunol. Cell Biol. 1989, 67 (Pt 1), 41-48.
29. Mandeville, R.; Dumas, F.; Amarouch, A.; Sidrac-Ghali, S.; Walker, M. C.; Zelechowska, M.; Ajdukovic, I.; Grouix, B. Affinity purification of a high molecular weight human breast cancer-associated antigen identified by the BCD-B4 monoclonal antibody. Hybridoma 1987, 6 (5), 441-451.
30. Xu, M.; Wang, F.; Gildersleeve, J. C.; Achilefu, S. MAb L9E10 to blood group H2 antigen binds to colon cancer stem cells and inhibits tumor cell migration and invasion. Hybridoma 2010, 29 (4), 355-359.
31. Jadvar, H.; Xiankui, L.; Shahinian, A.; Park, R.; Tohme, M.; Pinski, J.; Conti, P. S. Glucose metabolism of human prostate cancer mouse xenografts. Mol. Imaging 2005, 4 (2), 91-97.
32. Zheng, Q. H.; Gardner, T. A.; Raikwar, S.; Kao, C.; Stone, K. L.; Martinez, T. D.; Mock, B. H.; Fei, X.; Wang, J. Q.; Hutchins, G. D. [11C]Choline as a PET biomarker for assessment of prostate cancer tumor models. Bioorg. Med. Chem. 2004, 12 (11), 2887-2893.
33. Vosjan, M. J. W. D.; Perk, L. R.; Visser, G. W. M.; Budde, M.; Jurek, P.; Kiefer, G. E.; van Dongen, G. A. M. S. Conjugation and radiolabeling of monoclonal antibodies with zirconium-89 for PET imaging using the bifunctional chelate p-isothiocyanatobenzyldesferrioxamine. Nat. Protoc. 2010, 5 (4), 739-743.
34. Perk, L. R.; Vosjan, M. J. W. D.; Visser, G. W. M.; Budde, M.; Jurek, P.; Kiefer, G. E.; van Dongen, G. A. M. S. p-Isothiocyanatobenzyl-desferrioxamine: A new bifunctional chelate for facile radiolabeling of monoclonal antibodies with zirconium-89 for immuno-PET imaging. Eur. J. Nucl. Med. Mol. Imaging 2010, 37 (2), 250-259.
35. Pu, Y.; Wang, W. B.; Xu, M.; Tang, G. C.; Budansky, Y.; Sharanov, M.; Achilefu, S.; Eastham, J. A.; Alfano, R. R. Near infrared photonic finger imager for prostate cancer screening. Technol. Cancer Res. Treat. 2011, 10 (6), 507-517.
36. Girgis, M. D.; Kenanova, V.; Olafsen, T.; McCabe, K. E.; Wu, A. M.; Tomlinson, J. S. Anti-CA19-9 diabody as a PET imaging probe for pancreas cancer. J. Surg. Res. 2011, 170 (2), 169-78.
37. Jin, H.; Zangar, R. C. Protein modifications as potential biomarkers in breast cancer. Biomarker Insights 2009, 4, 191-200.
38. Rambaruth, N. D.; Greenwell, P.; Dwek, M. V. The lectin Helix pomatia agglutinin recognizes O-GlcNAc containing glycoproteins in human breast cancer. Glycobiology 2012, 22 (6), 839-848.
39. Lynch, T. P.; Ferrer, C. M.; Jackson, S. R.; Shahriari, K. S.; Vosseller, K.; Reginato, M. J. Critical role of O-Linked beta-Nacetylglucosamine transferase in prostate cancer invasion, angiogenesis, and metastasis. J. Biol. Chem. 2012, 287 (14), 11070-11081.
40. Krzeslak, A.; Forma, E.; Bernaciak, M.; Romanowicz, H.; Brys, M. Gene expression of O-GlcNAc cycling enzymes in human breast cancers. Clin. Exp. Med. 2012, 12 (1), 61-65.
41. Mi, W.; Gu, Y.; Han, C.; Liu, H.; Fan, Q.; Zhang, X.; Cong, Q.; Yu, W. O-GlcNAcylation is a novel regulator of lung and colon cancer malignancy. Biochim. Biophys. Acta 2011, 1812 (4), 514-519.
42. Sayat, R.; Leber, B.; Grubac, V.; Wiltshire, L.; Persad, S. OGlcNAc-glycosylation of beta-catenin regulates its nuclear localization and transcriptional activity. Exp. Cell Res. 2008, 314 (15), 2774-2787.
43. Cho, H.; Ackerstaff, E.; Carlin, S.; Lupu, M. E.; Wang, Y.; Rizwan, A.; O'Donoghue, J.; Ling, C. C.; Humm, J. L.; Zanzonico, P. B.; Koutcher, J. A. Noninvasive multimodality imaging of the tumor microenvironment: registered dynamic magnetic resonance imaging and positron emission tomography studies of a preclinical tumor model of tumor hypoxia. Neoplasia 2009, 11 (3), 247-259 2p following 259.
44. Uehara, H.; Miyagawa, T.; Tjuvajev, J.; Joshi, R.; Beattie, B.; Oku, T.; Finn, R.; Blasberg, R. Imaging experimental brain tumors with 1-aminocyclopentane carboxylic acid and alpha-aminoisobutyric acid: Comparison to fluorodeoxyglucose and diethylenetriaminepentaacetic acid in morphologically defined tumor regions. J. Cereb. Blood Flow Metab. 1997, 17 (11), 1239-53.
45. Wakefield, L. M.; Letterio, J. J.; Chen, T.; Danielpour, D.; Allison, R. S.; Pai, L. H.; Denicoff, A. M.; Noone, M. H.; Cowan, K. H.; O'Shaughnessy, J. A.; et al. Transforming growth factor-beta1 circulates in normal human plasma and is unchanged in advanced metastatic breast cancer. Clin. Cancer Res. 1995, 1 (1), 129-136.
46. Apostolopoulos, V.; Xing, P. X.; Trapani, J. A.; McKenzie, I. F. Production of anti-breast cancer monoclonal antibodies using a glutathione-S-transferase-MUC1 bacterial fusion protein. Br. J. Cancer 1993, 67 (4), 713-720.
47. Samih, N.; Hovsepian, S.; Notel, F.; Prorok, M.; Zattara-Cannoni, H.; Mathieu, S.; Lombardo, D.; Fayet, G.; El-Battari, A. The impact of N-and O-glycosylation on the functions of Glut-1 transporter in human thyroid anaplastic cells. Biochim. Biophys. Acta 2003, 1621 (1), 92-101.
48. Heffernan, M.; Lotan, R.; Amos, B.; Palcic, M.; Takano, R.; Dennis, J. W. Branching beta 1-6N-acetylglucosaminetransferases and polylactosamine expression in mouse F9 teratocarcinoma cells and differentiated counterparts. J. Biol. Chem. 1993, 268 (2), 1242-1251.
49. MacLean, G. D.; Reddish, M.; Koganty, R. R.; Wong, T.; Gandhi, S.; Smolenski, M.; Samuel, J.; Nabholtz, J. M.; Longenecker, B. M. Immunization of breast cancer patients using a synthetic sialyl-Tn glycoconjugate plus Detox adjuvant. Cancer Immunol. Immunother. 1993, 36 (4), 215-222.
50. Li, X.; Lu, F.; Wang, J. Z.; Gong, C. X. Concurrent alterations of O-GlcNAcylation and phosphorylation of tau in mouse brains during fasting. Eur. J. Neurosci. 2006, 23 (8), 2078-2086.
51. Robertson, L. A.; Moya, K. L.; Breen, K. C. The potential role of tau protein O-glycosylation in Alzheimer's disease. J. Alzheimer's Dis. 2004, 6 (5), 489-495.
52. Yao, P. J.; Coleman, P. D. Reduced O-glycosylated clathrin assembly protein AP180: Implication for synaptic vesicle recycling dysfunction in Alzheimer's disease. Neurosci. Lett. 1998, 252 (1), 33-36.
53. Caldwell, S. A.; Jackson, S. R.; Shahriari, K. S.; Lynch, T. P.; Sethi, G.; Walker, S.; Vosseller, K.; Reginato, M. J. Nutrient sensor OGlcNAc transferase regulates breast cancer tumorigenesis through targeting of the oncogenic transcription factor FoxM1. Oncogene 2010, 29 (19), 2831-2842.
54. Olafsen, T.; Wu, A. M. Antibody vectors for imaging. Semin. Nucl. Med. 2010, 40 (3), 167-181.
55. Wei, L. H.; Olafsen, T.; Radu, C.; Hildebrandt, I. J.; McCoy, M. R.; Phelps, M. E.; Meares, C.; Wu, A. M.; Czernin, J.; Weber, W. A. Engineered antibody fragments with infinite affinity as reporter genes for PET imaging. J. Nucl. Med. 2008, 49 (11), 1828-1835.
56. Wu, A. M.; Olafsen, T. Antibodies for molecular imaging of cancer. Cancer J. (Sudbury, MA) 2008, 14 (3), 191-197.