Evaluation of the novel folate receptor ligand [18F]fluoro-PEG-folate for macrophage targeting in a rat model of arthritis

Arthritis Research and Therapy

Volumn 15, Issue 2, 2013, Pages

  Gent, Yoony Y J ^a   Weijers, Karin ^a   Molthoff, Carla F M ^a   Windhorst, Albert D ^a   Huisman, Marc C ^a   Smith, Desirée E C ^a   Kularatne, Sumith A ^b   Jansen, Gerrit ^a   Low, Philip S ^b   Lammertsma, Adriaan A ^a   van der Laken, Conny J ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 METHYLTETRAHYDROFOLIC ACID; BOVINE SERUM ALBUMIN; FLUORO PEG FOLATE F 18; FOLATE RECEPTOR; FOLIC ACID; GLUCOSAMINE; N SEC BUTYL 1 (2 CHLOROPHENYL) N METHYL 3 ISOQUINOLINECARBOXAMIDE C 11; TRACER; UNCLASSIFIED DRUG; FLUORODEOXYGLUCOSE F 18; LIGAND; MACROGOL DERIVATIVE; POLY(ETHYLENE GLYCOL)-FOLATE; RADIOPHARMACEUTICAL AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DIAGNOSTIC IMAGING EQUIPMENT; DRUG ACTIVITY; DRUG BLOOD LEVEL; DRUG BONE LEVEL; DRUG DISTRIBUTION; DRUG PURITY; DRUG RECEPTOR BINDING; DRUG SYNTHESIS; DRUG TARGETING; DRUG UPTAKE; EX VIVO STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; KNEE ARTHRITIS; MACROPHAGE; MALE; NONHUMAN; POSITRON EMISSION TOMOGRAPHY; PROTEIN EXPRESSION; RAT; TISSUE DISTRIBUTION; ANALOGS AND DERIVATIVES; ANIMAL; DIAGNOSTIC USE; EXPERIMENTAL ARTHRITIS; IMAGE PROCESSING; IMMUNOHISTOCHEMISTRY; SCINTISCANNING; SYNOVITIS; SYNTHESIS; WISTAR RAT;

ANIMALS; ARTHRITIS, EXPERIMENTAL; FLUORODEOXYGLUCOSE F18; FOLIC ACID; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; LIGANDS; MACROPHAGES; MALE; POLYETHYLENE GLYCOLS; RADIOPHARMACEUTICALS; RATS; RATS, WISTAR; SYNOVITIS;

EID: 84874398867     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar4191     Document Type: Article

References (45)

1. Hamilton JA, Tak PP. The dynamics of macrophage lineage populations in inflammatory and autoimmune diseases. Arthritis Rheum 2009, 60:1210-1221. 10.1002/art.24505, 19404968.
2. Singh JA, Pando JA, Tomaszewski J, Schumacher HR. Quantitative analysis of immunohistologic features of very early rheumatoid synovitis in disease modifying antirheumatic drug- and corticosteroid-naive patients. J Rheumatol 2004, 31:1281-1285.
3. Nielen MM, van Schaardenburg D, Reesink HW, van de Stadt RJ, van der Horst-Bruinsma IE, de Koning MH, Habibuw MR, Vandenbroucke JP, Dijkmans BA. Specific autoantibodies precede the symptoms of rheumatoid arthritis: a study of serial measurements in blood donors. Arthritis Rheum 2004, 50:380-386. 10.1002/art.20018, 14872479.
4. Kraan MC, Versendaal H, Jonker M, Bresnihan B, Post WJ, Hart BA, Breedveld FC, Tak PP. Asymptomatic synovitis precedes clinically manifest arthritis. Arthritis Rheum 1998, 41:1481-1488. 10.1002/1529-0131(199808)41:8<1481::AID-ART19>3.0.CO;2-O, 9704648.
5. Brown AK, Conaghan PG, Karim Z, Quinn MA, Ikeda K, Peterfy CG, Hensor E, Wakefield RJ, O'Connor PJ, Emery P. An explanation for the apparent dissociation between clinical remission and continued structural deterioration in rheumatoid arthritis. Arthritis Rheum 2008, 58:2958-2967. 10.1002/art.23945, 18821687.
6. van der Laken CJ, Elzinga EH, Kropholler MA, Molthoff CF, van der Heijden JW, Maruyama K, Boellaard R, Dijkmans BA, Lammertsma AA, Voskuyl AE. Noninvasive imaging of macrophages in rheumatoid synovitis using 11C-(R)-PK11195 and positron emission tomography. Arthritis Rheum 2008, 58:3350-3355. 10.1002/art.23955, 18975347.
7. Gent YY, Voskuyl AE, Kloet RW, van Schaardenburg D, Hoekstra OS, Dijkmans BA, Lammertsma AA, van der Laken CJ. Macrophage positron emission tomography imaging as a biomarker for preclinical rheumatoid arthritis: findings of a prospective pilot study. Arthritis Rheum 2012, 64:62-66. 10.1002/art.30655, 21898356.
8. Salazar MD, Ratnam M. The folate receptor: what does it promise in tissue-targeted therapeutics?. Cancer Metastasis Rev 2007, 26:141-152. 10.1007/s10555-007-9048-0, 17333345.
9. Weitman SD, Lark RH, Coney LR, Fort DW, Frasca V, Zurawski VR, Kamen BA. Distribution of the folate receptor GP38 in normal and malignant cell lines and tissues. Cancer Res 1992, 52:3396-3401.
10. Parker N, Turk MJ, Westrick E, Lewis JD, Low PS, Leamon CP. Folate receptor expression in carcinomas and normal tissues determined by a quantitative radioligand binding assay. Anal Biochem 2005, 338:284-293. 10.1016/j.ab.2004.12.026, 15745749.
11. Xia W, Hilgenbrink AR, Matteson EL, Lockwood MB, Cheng JX, Low PS. A functional folate receptor is induced during macrophage activation and can be used to target drugs to activated macrophages. Blood 2009, 113:438-446.
12. van der Heijden JW, Oerlemans R, Dijkmans BA, Qi H, van der Laken CJ, Lems WF, Jackman AL, Kraan MC, Tak PP, Ratnam M, Jansen G. Folate receptor beta as a potential delivery route for novel folate antagonists to macrophages in the synovial tissue of rheumatoid arthritis patients. Arthritis Rheum 2009, 60:12-21. 10.1002/art.24219, 19116913.
13. Jansen G, van der Heijden JW, Dijkmans BA. Folate receptor β: a novel target for therapeutic intervention in rheumatoid arthritis?. Int J Clin Rheumatol 2009, 4:109-113.
14. Westerhof GR, Schornagel JH, Kathmann I, Jackman AL, Rosowsky A, Forsch RA, Hynes JB, Boyle FT, Peters GJ, Pinedo HM. Carrier- and receptor-mediated transport of folate antagonists targeting folate-dependent enzymes: correlates of molecular-structure and biological activity. Mol Pharmacol 1995, 48:459-471.
15. Nagayoshi R, Nakamura M, Ijiri K, Yoshida H, Komiya S, Matsuyama T. LY309887, antifolate via the folate receptor suppresses murine type II collagen-induced arthritis. Clin Exp Rheumatol 2003, 21:719-725.
16. Low PS, Henne WA, Doorneweerd DD. Discovery and development of folic-acid-based receptor targeting for imaging and therapy of cancer and inflammatory diseases. Acc Chem Res 2008, 41:120-129. 10.1021/ar7000815, 17655275.
17. Paulos CM, Turk MJ, Breur GJ, Low PS. Folate receptor-mediated targeting of therapeutic and imaging agents to activated macrophages in rheumatoid arthritis. Adv Drug Deliv Rev 2004, 56:1205-1217. 10.1016/j.addr.2004.01.012, 15094216.
18. van Dam GM, Themelis G, Crane LM, Harlaar NJ, Pleijhuis RG, Kelder W, Sarantopoulos A, de Jong JS, Arts HJ, van der Zee AG, Bart J, Low PS, Ntziachristos V. Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-alpha targeting: first in-human results. Nat Med 2011, 17:1315-1319. 10.1038/nm.2472, 21926976.
19. Muller C, Hohn A, Schubiger PA, Schibli R. Preclinical evaluation of novel organometallic 99mTc-folate and 99mTc-pteroate radiotracers for folate receptor-positive tumour targeting. Eur J Nucl Med Mol Imaging 2006, 33:1007-1016. 10.1007/s00259-006-0111-9, 16763819.
20. Turk MJ, Breur GJ, Widmer WR, Paulos CM, Xu LC, Grote LA, Low PS. Folate-targeted imaging of activated macrophages in rats with adjuvant-induced arthritis. Arthritis Rheum 2002, 46:1947-1955. 10.1002/art.10405, 12124880.
21. Henne WA, Rothenbuhler R, Ayala-Lopez W, Xia W, Varghese B, Low PS. Imaging sites of infection using a 99mTc-labeled folate conjugate targeted to folate receptor positive macrophages. Mol Pharm 2012, 9:1435-1440.
22. Matteson EL, Lowe VJ, Prendergast FG, Crowson CS, Moder KG, Morgenstern DE, Messmann RA, Low PS. Assessment of disease activity in rheumatoid arthritis using a novel folate targeted radiopharmaceutical Folatescan. Clin Exp Rheumatol 2009, 27:253-259.
23. Bettio A, Honer M, Muller C, Bruhlmeier M, Muller U, Schibli R, Groehn V, Schubiger AP, Ametamey SM. Synthesis and preclinical evaluation of a folic acid derivative labeled with 18F for PET imaging of folate receptor-positive tumors. J Nucl Med 2006, 47:1153-1160.
24. Ross TL, Honer M, Lam PY, Mindt TL, Groehn V, Schibli R, Schubiger PA, Ametamey SM. Fluorine-18 click radiosynthesis and preclinical evaluation of a new 18F-labeled folic acid derivative. Bioconjug Chem 2008, 19:2462-2470. 10.1021/bc800356r, 19053298.
25. Ross TL, Honer M, Muller C, Groehn V, Schibli R, Ametamey SM. A new 18F-labeled folic acid derivative with improved properties for the PET imaging of folate receptor-positive tumors. J Nucl Med 2010, 51:1756-1762. 10.2967/jnumed.110.079756, 20956469.
26. Fischer CR, Muller C, Reber J, Muller A, Kramer SD, Ametamey SM, Schibli R. [18F]fluoro-deoxy-glucose folate: a novel PET radiotracer with improved in vivo properties for folate receptor targeting. Bioconjug Chem 2012, 23:805-813. 10.1021/bc200660z, 22372827.
27. Harris JM, Martin NE, Modi M. Pegylation: a novel process for modifying pharmacokinetics. Clin Pharmacokinet 2001, 40:539-551. 10.2165/00003088-200140070-00005, 11510630.
28. Kropholler MA, Boellaard R, Elzinga EH, van der Laken CJ, Maruyama K, Kloet RW, Voskuyl AE, Dijkmans BA, Lammertsma AA. Quantification of (R)-[11C]PK11195 binding in rheumatoid arthritis. Eur J Nucl Med Mol Imaging 2009, 36:624-631. 10.1007/s00259-008-0987-7, 19043704.
29. Dijkstra CD, Dopp EA, Vogels IM, Van Noorden CJ. Macrophages and dendritic cells in antigen-induced arthritis. An immunohistochemical study using cryostat sections of the whole knee joint of rat. Scand J Immunol 1987, 26:513-523. 10.1111/j.1365-3083.1987.tb02285.x, 3479836.
30. de Jong HW, van Velden FH, Kloet RW, Buijs FL, Boellaard R, Lammertsma AA. Performance evaluation of the ECAT HRRT: an LSO-LYSO double layer high resolution, high sensitivity scanner. Phys Med Biol 2007, 52:1505-1526. 10.1088/0031-9155/52/5/019, 17301468.
31. AMIDE: Amide's a Medical Image Data Examiner. , http://amide.sourceforge.cet/
32. Dijkstra CD, Dopp EA, Joling P, Kraal G. The heterogeneity of mononuclear phagocytes in lymphoid organs: distinct macrophage subpopulations in the rat recognized by monoclonal antibodies ED1, ED2 and ED3. Immunology 1985, 54:589-599. 1453512, 3882559.
33. Lu Y, Stinnette TW, Westrick E, Klein PJ, Gehrke MA, Cross VA, Vlahov IR, Low PS, Leamon CP. Treatment of experimental adjuvant arthritis with a novel folate receptor-targeted folic acid-aminopterin conjugate. Arthritis Res Ther 2011, 13:R56. 10.1186/ar3304, 3132048, 21463515.
34. van der Wilt CL, Backus HH, Smid K, Comijn L, Veerman G, Wouters D, Voorn DA, Priest DG, Bunni MA, Mitchell F, Jackman AL, Jansen G, Peters GJ. Modulation of both endogenous folates and thymidine enhance the therapeutic efficacy of thymidylate synthase inhibitors. Cancer Res 2001, 61:3675-3681.
35. Smith DE, Kok RM, Teerlink T, Jakobs C, Smulders YM. Quantitative determination of erythrocyte folate vitamer distribution by liquid chromatography-tandem mass spectrometry. Clin Chem Lab Med 2006, 44:450-459.
36. Elnakat H, Ratnam M. Distribution, functionality and gene regulation of folate receptor isoforms: implications in targeted therapy. Adv Drug Deliv Rev 2004, 56:1067-1084. 10.1016/j.addr.2004.01.001, 15094207.
37. Pohlers D, Siegling A, Buchner E, Schmidt-Weber CB, Palombo-Kinne E, Emmrich F, Brauer R, Kinne RW. Expression of cytokine mRNA and protein in joints and lymphoid organs during the course of rat antigen-induced arthritis. Arthritis Res Ther 2005, 7:R445-R457. 10.1186/ar1689, 1174936, 15899031.
38. Simon J, Surber R, Kleinstauber G, Petrow PK, Henzgen S, Kinne RW, Brauer R. Systemic macrophage activation in locally-induced experimental arthritis. J Autoimmun 2001, 17:127-136. 10.1006/jaut.2001.0534, 11591121.
39. Johnson WJ, Muirhead KA, Meunier PC, Votta BJ, Schmitt TC, DiMartino MJ, Hanna N. Macrophage activation in rat models of inflammation and arthritis. Systemic activation precedes arthritis induction and progression. Arthritis Rheum 1986, 29:1122-1130. 10.1002/art.1780290910, 3489469.
40. van der Heijden JW, Dijkmans BA, Scheper RJ, Jansen G. Drug Insight: resistance to methotrexate and other disease-modifying antirheumatic drugs--from bench to bedside. Nat Clin Pract Rheumatol 2007, 3:26-34.
41. Nagai T, Kyo A, Hasui K, Takao S, Matsuyama T. Efficacy of an immunotoxin to folate receptor beta in the intra-articular treatment of antigen-induced arthritis. Arthritis Res Ther 2012, 14:R106. 10.1186/ar3831, 3446483, 22551402.
42. Naumann RW, Coleman RL. Management strategies for recurrent platinum-resistant ovarian cancer. Drugs 2011, 71:1397-1412. 10.2165/11591720-000000000-00000, 21812505.
43. Piscaer TM, Müller C, Mindt TL, Lubberts E, Verhaar JA, Krenning EP, Schibli R, De Jong M, Weinans H. Imaging of activated macrophages in experimental osteoarthritis using folate-targeted animal single-photon-emission computed tomography/computed tomography. Arthritis Rheum 2011, 63:1898-1907. 10.1002/art.30363, 21437875.
44. Ayala-Lopez W, Xia W, Varghese B, Low PS. Imaging of atherosclerosis in apoliprotein e knockout mice: targeting of a folate-conjugated radiopharmaceutical to activated macrophages. J Nucl Med 2010, 51:768-774. 10.2967/jnumed.109.071324, 20395331.
45. Jager NA, Teteloshvili N, Zeebregts CJ, Westra J, Bijl M. Macrophage folate receptor-beta (FR-beta) expression in auto-immune inflammatory rheumatic diseases: A forthcoming marker for cardiovascular risk?. Autoimmun Rev 2012, 11:621-626. 10.1016/j.autrev.2011.11.002, 22094710.