Antibody-based tumor vascular theranostics targeting endosialin/TEM1 in a new mouse tumor vascular model

Cancer Biology and Therapy

Volumn 15, Issue 4, 2014, Pages 443-451

  Li, Chunsheng ^b   Chacko, Ann Marie ^a,b   Hu, Jia ^a   Hasegawa, Kosei ^a   Swails, Jennifer ^a   Grasso, Luigi ^c   El Deiry, Wafik S ^a   Nicolaides, Nicholas ^c   Muzykantov, Vladimir R ^b   Divgi, Chaitanya R ^a   Coukos, George ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c Morphotek Inc   (United States)

Author keywords

Anti angiogenesis; Antibody therapy; CD248; Endosialin; ImmunoPET; TEM1; Tumor vasculature

Indexed keywords

ENDOSIALIN; FIREFLY LUCIFERASE; IMMUNOGLOBULIN G1 ANTIBODY; MORAB 004; MORAB 004 I 124; MORAB 004 I 125; RADIOPHARMACEUTICAL AGENT; UNCLASSIFIED DRUG; LEUKOCYTE ANTIGEN; MONOCLONAL ANTIBODY; RADIOACTIVE IODINE; TUMOR ENDOTHELIAL MARKER 1, MOUSE; TUMOR PROTEIN;

ANGIOGENESIS; ANGIOMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY SPECIFICITY; ARTICLE; BLOOD VESSEL GRAFT; CONTROLLED STUDY; ENDOTHELIUM CELL; HEMANGIOMA; MOLECULAR IMAGING; MOUSE; NONHUMAN; OVARY TUMOR; POSITRON EMISSION TOMOGRAPHY; PROTEIN EXPRESSION; RADIOIODINATION; TUMOR MODEL; TUMOR VASCULARIZATION; ANIMAL; METABOLISM; NEOPLASMS, EXPERIMENTAL; NUDE MOUSE; SCINTISCANNING; TISSUE DISTRIBUTION; TUMOR CELL LINE; VASCULAR ENDOTHELIUM; VASCULARIZATION; XENOGRAFT;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD; CELL LINE, TUMOR; ENDOTHELIUM, VASCULAR; HETEROGRAFTS; IODINE RADIOISOTOPES; MICE, NUDE; NEOPLASM PROTEINS; NEOPLASMS, EXPERIMENTAL; POSITRON-EMISSION TOMOGRAPHY; RADIOPHARMACEUTICALS; TISSUE DISTRIBUTION;

EID: 84897510637     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.27825     Document Type: Article

References (39)

1. Parker BS, Argani P, Cook BP, Liangfeng H, Chartrand SD, Zhang M, Saha S, Bardelli A, Jiang Y, St Martin TB, et al. Alterations in vascular gene expression in invasive breast carcinoma. Cancer Res 2004; 64:7857-66; PMID:15520192; http://dx.doi.org/10.1158/0008-5472.CAN-04-1976
2. Lu C, Bonome T, Li Y, Kamat AA, Han LY, Schmandt R, Coleman RL, Gershenson DM, Jaffe RB, Birrer MJ, et al. Gene alterations identified by expression profiling in tumor-associated endothelial cells from invasive ovarian carcinoma. Cancer Res 2007; 67:1757-68; PMID:17308118; http://dx.doi.org/10. 1158/0008-5472.CAN-06-3700
3. Buckanovich RJ, Sasaroli D, O'Brien-Jenkins A, Botbyl J, Hammond R, Katsaros D, Sandaltzopoulos R, Liotta LA, Gimotty PA, Coukos G. Tumor vascular proteins as biomarkers in ovarian cancer. J Clin Oncol 2007; 25:852-61; PMID:17327606; http://dx.doi.org/10.1200/JCO.2006.08.8583
4. St Croix B, Rago C, Velculescu V, Traverso G, Romans KE, Montgomery E, Lal A, Riggins GJ, Lengauer C, Vogelstein B, et al. Genes expressed in human tumor endothelium. Science 2000; 289:1197-202; PMID:10947988; http://dx.doi.org/10.1126/science.289.5482.1197
5. Bhati R, Patterson C, Livasy CA, Fan C, Ketelsen D, Hu Z, Reynolds E, Tanner C, Moore DT, Gabrielli F, et al. Molecular characterization of human breast tumor vascular cells. Am J Pathol 2008; 172:1381-90; PMID:18403594; http://dx.doi.org/10.2353/ajpath.2008.070988
6. Madden SL, Cook BP, Nacht M, Weber WD, Callahan MR, Jiang Y, Dufault MR, Zhang X, Zhang W, Walter-Yohrling J, et al. Vascular gene expression in nonneoplastic and malignant brain. Am J Pathol 2004; 165:601-8; PMID:15277233; http://dx.doi.org/10.1016/S0002-9440(10)63324-X
7. Ulahannan SV, Brahmer JR. Antiangiogenic agents in combination with chemotherapy in patients with advanced non-small cell lung cancer. Cancer Invest 2011; 29:325-37; PMID:21469981; http://dx.doi.org/10.3109/07357907.2011.554476
8. Mulder K, Scarfe A, Chua N, Spratlin J. The role of bevacizumab in colorectal cancer: understanding its benefits and limitations. Expert Opin Biol Ther 2011; 11:405-13; PMID:21281258; http://dx.doi.org/10.1517/14712598.2011. 557657
9. Merritt WM, Sood AK. Markers of angiogenesis in ovarian cancer. Dis Markers 2007; 23:419-31; PMID:18057525; http://dx.doi.org/10.1155/2007/257602
10. Lanza GM, Winter PM, Caruthers SD, Hughes MS, Hu G, Schmieder AH, Wickline SA. Theragnostics for tumor and plaque angiogenesis with perfluoro-carbon nanoemulsions. Angiogenesis 2010; 13:189-202; PMID:20411320; http://dx.doi.org/10.1007/s10456-010-9166-0
11. Street JM, Dear JW. The application of mass-spectrometry-based protein biomarker discovery to theragnostics. Br J Clin Pharmacol 2010; 69:367-78; PMID:20406221; http://dx.doi.org/10.1111/j.1365-2125.2009.03610.x
12. van Dongen GA, Visser GW, Lub-de Hooge MN, de Vries EG, Perk LR. Immuno-PET: a navigator in monoclonal antibody development and applications. Oncologist 2007; 12:1379-89; PMID:18165614; http://dx.doi.org/10.1634/ theoncologist.12-12-1379
13. Divgi CR, Pandit-Taskar N, Jungbluth AA, Reuter VE, Gönen M, Ruan S, Pierre C, Nagel A, Pryma DA, 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; 8:304-10; PMID:17395103; http://dx.doi.org/10.1016/S1470-2045(07) 70044-X
14. Becker R, Lenter MC, Vollkommer T, Boos AM, Pfaff D, Augustin HG, Christian S. Tumor stroma marker endosialin (Tem1) is a binding partner of metastasis-related protein Mac-2 BP/90K. FASEB J 2008; 22:3059-67; PMID:18490383; http://dx.doi.org/10.1096/fj.07-101386
15. Tomkowicz B, Rybinski K, Foley B, Ebel W, Kline B, Routhier E, Sass P, Nicolaides NC, Grasso L, Zhou Y. Interaction of endosialin/TEM1 with extracellular matrix proteins mediates cell adhesion and migration. Proc Natl Acad Sci U S A 2007; 104:17965-70; PMID:17986615; http://dx.doi.org/10.1073/ pnas.0705647104
16. Christian S, Ahorn H, Koehler A, Eisenhaber F, Rodi HP, Garin-Chesa P, Park JE, Rettig WJ, Lenter MC. Molecular cloning and characterization of endosialin, a C-type lectin-like cell surface receptor of tumor endothelium. J Biol Chem 2001; 276:7408-14; PMID:11084048; http://dx.doi.org/10.1074/jbc. M009604200
17. Rettig WJ, Garin-Chesa P, Healey JH, Su SL, Jaffe EA, Old LJ. Identification of endosialin, a cell surface glycoprotein of vascular endothelial cells in human cancer. Proc Natl Acad Sci U S A 1992; 89:10832-6; PMID:1438285; http://dx.doi.org/10.1073/pnas.89.22.10832
18. Christian S, Winkler R, Helfrich I, Boos AM, Besemfelder E, Schadendorf D, Augustin HG. Endosialin (Tem1) is a marker of tumor-associated myofibroblasts and tumor vessel-associated mural cells. Am J Pathol 2008; 172:486-94; PMID:18187565; http://dx.doi.org/10.2353/ajpath.2008.070623
19. Brady J, Neal J, Sadakar N, Gasque P. Human endosialin (tumor endothelial marker 1) is abundantly expressed in highly malignant and invasive brain tumors. J Neuropathol Exp Neurol 2004; 63:1274-83; PMID:15624764
20. Buckanovich RJ, Sasaroli D, O'brien-Jenkins A, Botbyl J, Conejo-Garcia JR, Benencia F, Liotta LA, Gimotty PA, Coukos G. Use of immuno-LCM to identify the in situ expression profile of cellular constituents of the tumor microenvironment. Cancer Biol Ther 2006; 5:635-42; PMID:16627987; http://dx.doi.org/10.4161/cbt.5.6.2676
21. Neri D, Bicknell R. Tumour vascular targeting. Nat Rev Cancer 2005; 5:436-46; PMID:15928674; http://dx.doi.org/10.1038/nrc1627
22. Carson-Walter EB, Watkins DN, Nanda A, Vogelstein B, Kinzler KW, St Croix B. Cell surface tumor endothelial markers are conserved in mice and humans. Cancer Res 2001; 61:6649-55; PMID:11559528
23. Walter-Yohrling J, Morgenbesser S, Rouleau C, Bagley R, Callahan M, Weber W, Teicher BA. Murine endothelial cell lines as models of tumor endothelial cells. Clin Cancer Res 2004; 10:2179-89; PMID:15041739; http://dx.doi.org/10. 1158/1078-0432.CCR-03-1013
24. Bagley RG, Rouleau C, St Martin T, Boutin P, Weber W, Ruzek M, Honma N, Nacht M, Shankara S, Kataoka S, et al. Human endothelial precursor cells express tumor endothelial marker 1/endosialin/ CD248. Mol Cancer Ther 2008; 7:2536-46; PMID:18723498; http://dx.doi.org/10.1158/1535-7163.MCT-08-0050
25. Simonavicius N, Robertson D, Bax DA, Jones C, Huijbers IJ, Isacke CM. Endosialin (CD248) is a marker of tumor-associated pericytes in high-grade glioma. Mod Pathol 2008; 21:308-15; PMID:18192970; http://dx.doi.org/10.1038/ modpathol.3801006
26. Wesseling P, Schlingemann RO, Rietveld FJ, Link M, Burger PC, Ruiter DJ. Early and extensive contribution of pericytes/vascular smooth muscle cells to microvascular proliferation in glioblastoma multiforme: an immuno-light and immuno-electron microscopic study. J Neuropathol Exp Neurol 1995; 54:304-10; PMID:7745429; http://dx.doi.org/10.1097/00005072-199505000-00003
27. MacFadyen JR, Haworth O, Roberston D, Hardie D, Webster MT, Morris HR, Panico M, Sutton-Smith M, Dell A, van der Geer P, et al. Endosialin (TEM1, CD248) is a marker of stromal fibroblasts and is not selectively expressed on tumour endothelium. FEBS Lett 2005; 579:2569-75; PMID:15862292; http://dx.doi.org/10.1016/j.febslet.2005.03.071
28. Davies G, Cunnick GH, Mansel RE, Mason MD, Jiang WG. Levels of expression of endothelial markers specific to tumour-associated endothelial cells and their correlation with prognosis in patients with breast cancer. Clin Exp Metastasis 2004; 21:31-7; PMID:15065600; http://dx.doi.org/10.1023/B:CLIN. 0000017168.83616.d0
29. Nanda A, Karim B, Peng Z, Liu G, Qiu W, Gan C, Vogelstein B, St Croix B, Kinzler KW, Huso DL. Tumor endothelial marker 1 (Tem1) functions in the growth and progression of abdominal tumors. Proc Natl Acad Sci U S A 2006; 103:3351-6; PMID:16492758; http://dx.doi.org/10.1073/pnas.0511306103
30. Conejo-Garcia JR, Buckanovich RJ, Benencia F, Courreges MC, Rubin SC, Carroll RG, Coukos G. Vascular leukocytes contribute to tumor vascularization. Blood 2005; 105:679-81; PMID:15358628; http://dx.doi.org/10.1182/blood-2004-05- 1906
31. Rettig WJ. Immunogenetics of cell surface antigens of human cancer. Curr Opin Immunol 1992; 4:630-40; PMID:1418731; http://dx.doi.org/10.1016/0952- 7915(92)90039-H
32. Zhou Y, Grasso L, Tomkowicz B, Ebel W, Routhier E, Phillips MD, Sass P, Old L, Nicolaides NC. Targeting endosialin/TEM1 as a novel anti-angiogenic agent for the treatment of neovascular disease and cancer. AACR poster 2008;http://www.morphotek.com/CorporateSite/media/Posters/Preclinical-MORAb-004- Study.pdf.
33. Hasegawa K, Pham L, O'Connor MK, Federspiel MJ, Russell SJ, Peng KW. Dual therapy of ovarian cancer using measles viruses expressing carcinoembryonic antigen and sodium iodide symporter. Clin Cancer Res 2006; 12:1868-75; PMID:16551872; http://dx.doi.org/10.1158/1078-0432.CCR-05-1803
34. Steplewski Z, Sun LK, Shearman CW, Ghrayeb J, Daddona P, Koprowski H. Biological activity of human-mouse IgG1, IgG2, IgG3, and IgG4 chimeric monoclonal antibodies with antitumor specificity. Proc Natl Acad Sci U S A 1988; 85:4852-6; PMID:3387441; http://dx.doi.org/10.1073/pnas.85.13.4852
35. Lindmo T, Boven E, Cuttitta F, Fedorko J, Bunn PA Jr. Determination of the immunoreactive fraction of radiolabeled monoclonal antibodies by linear extrapolation to binding at infinite antigen excess. J Immunol Methods 1984; 72:77-89; PMID:6086763; http://dx.doi.org/10.1016/0022-1759(84)90435-6
36. Rouleau C, Curiel M, Weber W, Smale R, Kurtzberg L, Mascarello J, Berger C, Wallar G, Bagley R, Honma N, et al. Endosialin protein expression and therapeutic target potential in human solid tumors: sarcoma versus carcinoma. Clin Cancer Res 2008; 14:7223-36; PMID:19010839; http://dx.doi.org/10.1158/1078- 0432.CCR-08-0499
37. Pryma DA, O'Donoghue JA, Humm JL, Jungbluth AA, Old LJ, Larson SM, Divgi CR. Correlation of in vivo and in vitro measures of carbonic anhydrase IX antigen expression in renal masses using antibody 124I-cG250. J Nucl Med 2011; 52:535-40; PMID:21421715; http://dx.doi.org/10.2967/jnumed.110.083295
38. O'Donoghue JA, Smith-Jones PM, Humm JL, Ruan S, Pryma DA, Jungbluth AA, Divgi CR, Carrasquillo JA, Pandit-Taskar N, Fong Y, et al. 124I-huA33 antibody uptake is driven by A33 antigen concentration in tissues from colorectal cancer patients imaged by immuno-PET. J Nucl Med 2011; 52:1878-85; PMID:22068895; http://dx.doi.org/10.2967/jnumed.111.095596
39. Chacko AM, Nayak M, Greineder CF, Delisser HM, Muzykantov VR. Collaborative enhancement of antibody binding to distinct PECAM-1 epitopes modulates endothelial targeting. PLoS One 2012; 7:e34958; PMID:22514693; http://dx.doi.org/10.1371/journal.pone.0034958