ACS Publications. Most Trusted. Most Cited. Most Read
Fluorine-18 Click Radiosynthesis and Preclinical Evaluation of a New 18F-Labeled Folic Acid Derivative
My Activity

Figure 1Loading Img
    Article

    Fluorine-18 Click Radiosynthesis and Preclinical Evaluation of a New 18F-Labeled Folic Acid Derivative
    Click to copy article linkArticle link copied!

    View Author Information
    Animal Imaging Center - PET, Center for Pharmaceutical Science of ETH, PSI and USZ, and Department of Chemistry and Applied Biosciences, ETH Zürich, 8093 Zürich, Switzerland, and Merck Eprova AG, 8200 Schaffhausen
    †Department of Chemistry and Applied Biosciences, ETH Zürich.
    ‡Merck Eprova AG.
    Other Access OptionsSupporting Information (1)

    Bioconjugate Chemistry

    Cite this: Bioconjugate Chem. 2008, 19, 12, 2462–2470
    Click to copy citationCitation copied!
    https://doi.org/10.1021/bc800356r
    Published November 24, 2008
    Copyright © 2008 American Chemical Society

    Abstract

    Click to copy section linkSection link copied!

    The folate receptor (FR) is highly expressed on most epithelial cancer cells, while normal cells show only restricted expression of FR. As a result, the FR is an ideal target for receptor-based molecular imaging and therapy of cancer and has become a promising target in oncology. To date, several folate-based chemotherapeutics and imaging probes such as radiopharmaceuticals for single photon emission computed tomography (SPECT) have been developed. However, an 18F-labeled folic acid derivative suitable for positron emission tomography (PET) imaging that can be routinely applied is still lacking. In this study, a new fluorinated and radiofluorinated folic acid derivative, 18/19F-click folate, was synthesized using click chemistry. In a convenient and very efficient two-step radiosynthesis, the isolated 18F-click folate was obtained in good radiochemical yields of 25−35% with a specific activity of 160 ± 70 GBq/μmol after ≤90 min synthesis time. The new compound was pharmacologically evaluated in vitro and in vivo. The affinity of the non-radioactive 19F-click folate to the FR was determined in displacement studies with FR expressing KB tumor cells using 3H-folic acid. In these in vitro binding studies, a nanomolar affinity with a Ki of 9.76 ± 3.13 nM was found for 19F-click folate. The 18F-labeled click folate derivative was then applied for in vivo PET studies and ex vivo biodistribution experiments using nude mice bearing KB tumor xenografts. The post mortem dissection experiments showed a high specific uptake of 18F-click folate derivative in FR-expressing tissues. Uptake in KB tumor xenografts and kidneys (FR-positive tissue) amounted to 3.13%ID/g (94% specific blockade) and 16.53%ID/g (75% specific blockade), respectively. PET imaging using 18F-click folate permitted a visualization of KB tumors, and blockade studies confirmed the specific accumulation of the radiotracer in vivo. However, strong hepatobiliary excretion of the new tracer led to elevated accumulation of radioactivity in the abdominal region. In conclusion, the click chemistry approach is convenient to accomplish and provided high radiochemical yields of 18F-click folate. The new tracer showed good in vitro but limited in vivo properties. Ultimately, the 18F-click folate emphasizes the potential of 18F-labeled folates for receptor-based tumor PET imaging.

    Copyright © 2008 American Chemical Society

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.

    Recommended

    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. Add or change your institution or let them know you’d like them to include access.

    Supporting Information

    Click to copy section linkSection link copied!

    1H and 13C NMR spectra of compound 3 and 5. Radio-HPLC chromatograms of quality control, plasma stability studies, and liver microsomes metabolite studies. This material is available free of charge via the Internet at http://pubs.acs.org.

    Terms & Conditions

    Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

    Click to copy section linkSection link copied!
    Citation Statements
    Explore this article's citation statements on scite.ai

    This article is cited by 69 publications.

    1. E. Johanna L. Stéen, Jesper T. Jørgensen, Christoph Denk, Umberto M. Battisti, Kamilla Nørregaard, Patricia E. Edem, Klas Bratteby, Vladimir Shalgunov, Martin Wilkovitsch, Dennis Svatunek, Christian B. M. Poulie, Lars Hvass, Marina Simón, Thomas Wanek, Raffaella Rossin, Marc Robillard, Jesper L. Kristensen, Hannes Mikula, Andreas Kjaer, Matthias M. Herth. Lipophilicity and Click Reactivity Determine the Performance of Bioorthogonal Tetrazine Tools in Pretargeted In Vivo Chemistry. ACS Pharmacology & Translational Science 2021, 4 (2) , 824-833. https://doi.org/10.1021/acsptsci.1c00007
    2. Silvan D. Boss, Cristina Müller, Klaudia Siwowska, Josephine I. Büchel, Raffaella M. Schmid, Viola Groehn, Roger Schibli, Simon M. Ametamey. Reduced 18F-Folate Conjugates as a New Class of PET Tracers for Folate Receptor Imaging. Bioconjugate Chemistry 2018, 29 (4) , 1119-1130. https://doi.org/10.1021/acs.bioconjchem.7b00775
    3. Qingshou Chen, Xiangjun Meng, Paul McQuade, Daniel Rubins, Shu-An Lin, Zhizhen Zeng, Hyking Haley, Patricia Miller, Dinko González Trotter, and Philip S. Low . Folate-PEG-NOTA-Al18F: A New Folate Based Radiotracer for PET Imaging of Folate Receptor-Positive Tumors. Molecular Pharmaceutics 2017, 14 (12) , 4353-4361. https://doi.org/10.1021/acs.molpharmaceut.7b00415
    4. Zhide Guo, Linyi You, Changrong Shi, Manli Song, Mengna Gao, Duo Xu, Chenyu Peng, Rongqiang Zhuang, Ting Liu, Xinhui Su, Jin Du, and Xianzhong Zhang . Development of a New FR-Targeting Agent 99mTc-HYNFA with Improved Imaging Contrast and Comparison of Multimerization and/or PEGylation Strategies for Radio-Folate Modification. Molecular Pharmaceutics 2017, 14 (11) , 3780-3788. https://doi.org/10.1021/acs.molpharmaceut.7b00536
    5. Qingshou Chen, Xiangjun Meng, Paul McQuade, Daniel Rubins, Shu-An Lin, Zhizhen Zeng, Hyking Haley, Patricia Miller, Dinko González Trotter, and Philip S. Low . Synthesis and Preclinical Evaluation of Folate-NOTA-Al18F for PET Imaging of Folate-Receptor-Positive Tumors. Molecular Pharmaceutics 2016, 13 (5) , 1520-1527. https://doi.org/10.1021/acs.molpharmaceut.5b00989
    6. Silvan D. Boss, Thomas Betzel, Cristina Müller, Cindy R. Fischer, Stephanie Haller, Josefine Reber, Viola Groehn, Roger Schibli, and Simon M. Ametamey . Comparative Studies of Three Pairs of α- and γ-Conjugated Folic Acid Derivatives Labeled with Fluorine-18. Bioconjugate Chemistry 2016, 27 (1) , 74-86. https://doi.org/10.1021/acs.bioconjchem.5b00644
    7. Jong Hwan Kim, Mihue Jang, Young-Je Kim, and Hyung Jun Ahn . Design and Application of Rolling Circle Amplification for a Tumor-Specific Drug Carrier. Journal of Medicinal Chemistry 2015, 58 (19) , 7863-7873. https://doi.org/10.1021/acs.jmedchem.5b01126
    8. Sumith A. Kularatne, Marie-José Bélanger, Xiangjun Meng, Brett M. Connolly, Amy Vanko, Donna L. Suresch, Ilonka Guenther, Shubing Wang, Philip S. Low, Paul McQuade, and Dinko González Trotter . Comparative Analysis of Folate Derived PET Imaging Agents with [18F]-2-Fluoro-2-deoxy-d-glucose Using a Rodent Inflammatory Paw Model. Molecular Pharmaceutics 2013, 10 (8) , 3103-3111. https://doi.org/10.1021/mp4001684
    9. Yong Liu, Janell Richardson, Thao Tran, Nour Al-Muhtasib, Teresa Xie, Venkata Mahidhar Yenugonda, Hannah G. Sexton, Amir H. Rezvani, Edward D. Levin, Niaz Sahibzada, Kenneth J. Kellar, Milton L. Brown, Yingxian Xiao, and Mikell Paige . Chemistry and Pharmacological Studies of 3-Alkoxy-2,5-Disubstituted-Pyridinyl Compounds as Novel Selective α4β2 Nicotinic Acetylcholine Receptor Ligands That Reduce Alcohol Intake in Rats. Journal of Medicinal Chemistry 2013, 56 (7) , 3000-3011. https://doi.org/10.1021/jm4000374
    10. Thomas Betzel, Cristina Müller, Viola Groehn, Adrienne Müller, Josefine Reber, Cindy R. Fischer, Stefanie D. Krämer, Roger Schibli, and Simon M. Ametamey . Radiosynthesis and Preclinical Evaluation of 3′-Aza-2′-[18F]fluorofolic Acid: A Novel PET Radiotracer for Folate Receptor Targeting. Bioconjugate Chemistry 2013, 24 (2) , 205-214. https://doi.org/10.1021/bc300483a
    11. Julian Willibald, Johannes Harder, Konstantin Sparrer, Karl-Klaus Conzelmann, and Thomas Carell . Click-Modified Anandamide siRNA Enables Delivery and Gene Silencing in Neuronal and Immune Cells. Journal of the American Chemical Society 2012, 134 (30) , 12330-12333. https://doi.org/10.1021/ja303251f
    12. Melpomeni Fani, Maria-Luisa Tamma, Guillaume P. Nicolas, Elisabeth Lasri, Christelle Medina, Isabelle Raynal, Marc Port, Wolfgang A. Weber, and Helmut R. Maecke . In Vivo Imaging of Folate Receptor Positive Tumor Xenografts Using Novel 68Ga-NODAGA-Folate Conjugates. Molecular Pharmaceutics 2012, 9 (5) , 1136-1145. https://doi.org/10.1021/mp200418f
    13. Cindy R. Fischer, Cristina Müller, Josefine Reber, Adrienne Müller, Stefanie D. Krämer, Simon M. Ametamey, and Roger Schibli . [18F]Fluoro-Deoxy-Glucose Folate: A Novel PET Radiotracer with Improved in Vivo Properties for Folate Receptor Targeting. Bioconjugate Chemistry 2012, 23 (4) , 805-813. https://doi.org/10.1021/bc200660z
    14. Kelly J. Kilpin, Emma L. Gavey, C. John McAdam, Christopher B. Anderson, Samuel J. Lind, Courtney C. Keep, Keith C. Gordon, and James D. Crowley . Palladium(II) Complexes of Readily Functionalized Bidentate 2-Pyridyl-1,2,3-triazole “Click” Ligands: A Synthetic, Structural, Spectroscopic, and Computational Study. Inorganic Chemistry 2011, 50 (13) , 6334-6346. https://doi.org/10.1021/ic200789b
    15. Kristin Michel, Katrin Büther, Marilyn P. Law, Stefan Wagner, Otmar Schober, Sven Hermann, Michael Schäfers, Burkhard Riemann, Carsten Höltke, and Klaus Kopka . Development and Evaluation of Endothelin-A Receptor (Radio)Ligands for Positron Emission Tomography. Journal of Medicinal Chemistry 2011, 54 (4) , 939-948. https://doi.org/10.1021/jm101110w
    16. Thomas L. Mindt, Cristina Müller, Florian Stuker, Jean-Frédéric Salazar, Alexander Hohn, Thomas Mueggler, Markus Rudin and Roger Schibli . A “Click Chemistry” Approach to the Efficient Synthesis of Multiple Imaging Probes Derived from a Single Precursor. Bioconjugate Chemistry 2009, 20 (10) , 1940-1949. https://doi.org/10.1021/bc900276b
    17. Laurène Wagner, Bibigul Kenzhebayeva, Batoul Dhaini, Samir Boukhlef, Albert Moussaron, Serge Mordon, Céline Frochot, Charlotte Collet, Samir Acherar. Folate-based radiotracers for nuclear imaging and radionuclide therapy. Coordination Chemistry Reviews 2022, 470 , 214702. https://doi.org/10.1016/j.ccr.2022.214702
    18. Kornelis S. M. van der Geest, Maria Sandovici, Pieter H. Nienhuis, Riemer H. J. A. Slart, Peter Heeringa, Elisabeth Brouwer, William F. Jiemy. Novel PET Imaging of Inflammatory Targets and Cells for the Diagnosis and Monitoring of Giant Cell Arteritis and Polymyalgia Rheumatica. Frontiers in Medicine 2022, 9 https://doi.org/10.3389/fmed.2022.902155
    19. Pejman Shahrokhi, Arezou Masteri Farahani, Mohammad Tamaddondar. Radiolabeled vitamins as the potential diagnostic probes for targeted tumor imaging. Bioorganic Chemistry 2022, 122 , 105717. https://doi.org/10.1016/j.bioorg.2022.105717
    20. Silvan D. Boss, Simon Mensah Ametamey. Development of Folate Receptor−Targeted PET Radiopharmaceuticals for Tumor Imaging—A Bench-to-Bedside Journey. Cancers 2020, 12 (6) , 1508. https://doi.org/10.3390/cancers12061508
    21. Weidong Yang, Cheng Wang, Gang Huang. Receptor-Targeted Radionuclide Imaging (RTRI) and Peptide Receptor Radionuclide Therapy (PRRT). 2019, 177-199. https://doi.org/10.1007/978-981-13-7458-6_12
    22. James C. Knight, Bart Cornelissen. Click Chemistry in Radiopharmaceutical Chemistry. 2019, 467-479. https://doi.org/10.1007/978-3-319-98947-1_26
    23. Kathrin Kettenbach, Laura Reffert, Hanno Schieferstein, Stefanie Pektor, Raphael Eckert, Matthias Miederer, Frank Rösch, Tobias Ross. Comparison Study of Two Differently Clicked 18F-Folates—Lipophilicity Plays a Key Role. Pharmaceuticals 2018, 11 (1) , 30. https://doi.org/10.3390/ph11010030
    24. James C. Knight, Bart Cornelissen. Preservation of Ligand Functionality by Click Chemistry. 2018, 251-262. https://doi.org/10.1007/978-3-319-67720-0_13
    25. Hema S. Krishnan, Longle Ma, Neil Vasdev, Steven H. Liang. 18 F‐Labeling of Sensitive Biomolecules for Positron Emission Tomography. Chemistry – A European Journal 2017, 23 (62) , 15553-15577. https://doi.org/10.1002/chem.201701581
    26. Christian Brand, Valerie A. Longo, Mike Groaning, Wolfgang A. Weber, Thomas Reiner. Development of a New Folate-Derived Ga-68-Based PET Imaging Agent. Molecular Imaging and Biology 2017, 19 (5) , 754-761. https://doi.org/10.1007/s11307-017-1049-y
    27. Ralf Schirrmacher, Björn Wängler, Justin Bailey, Vadim Bernard-Gauthier, Esther Schirrmacher, Carmen Wängler. Small Prosthetic Groups in 18 F-Radiochemistry: Useful Auxiliaries for the Design of 18 F-PET Tracers. Seminars in Nuclear Medicine 2017, 47 (5) , 474-492. https://doi.org/10.1053/j.semnuclmed.2017.07.001
    28. Sujuan Duan, Lu Guo, Dandan Shi, Mengmeng Shang, Dong Meng, Jie Li. Development of a novel folate-modified nanobubbles with improved targeting ability to tumor cells. Ultrasonics Sonochemistry 2017, 37 , 235-243. https://doi.org/10.1016/j.ultsonch.2017.01.013
    29. John F. Valliant. A Bridge Not Too Far: Linking Disciplines Through Molecular Imaging Probes. Journal of Nuclear Medicine Technology 2016, 44 (3) , 173-183. https://doi.org/10.2967/jnumed.109.068312
    30. Ganesan Vaidyanathan, Darryl McDougald, Jaeyeon Choi, Marek Pruszynski, Eftychia Koumarianou, Zhengyuan Zhou, Michael R. Zalutsky. N-Succinimidyl 3-((4-(4-[ 18 F]fluorobutyl)-1H-1,2,3-triazol-1-yl)methyl)-5-(guanidinomethyl)benzoate ([ 18 F]SFBTMGMB): a residualizing label for 18 F-labeling of internalizing biomolecules. Organic & Biomolecular Chemistry 2016, 14 (4) , 1261-1271. https://doi.org/10.1039/C5OB02258D
    31. Ragini Jenkins, Mary K. Burdette, Stephen H. Foulger. Mini-review: fluorescence imaging in cancer cells using dye-doped nanoparticles. RSC Advances 2016, 6 (70) , 65459-65474. https://doi.org/10.1039/C6RA10473H
    32. Ji Young Choi, Byung Chul Lee. Click Reaction: An Applicable Radiolabeling Method for Molecular Imaging. Nuclear Medicine and Molecular Imaging 2015, 49 (4) , 258-267. https://doi.org/10.1007/s13139-015-0377-6
    33. Punit Sharma, Rakesh Kumar, Abass Alavi. PET/Computed Tomography Using New Radiopharmaceuticals in Targeted Therapy. PET Clinics 2015, 10 (4) , 495-505. https://doi.org/10.1016/j.cpet.2015.05.007
    34. Lina Cui, Jianghong Rao. Chemical Methodology for Labelling and Bioconjugation. 2014, 25-53. https://doi.org/10.1002/9781118854754.ch2
    35. Jennifer Taylor. The Diagnostic Application of Radiolabelled Folate in the Detection of Folate Receptor–Positive Tumors. Journal of Medical Imaging and Radiation Sciences 2014, 45 (1) , 55-58. https://doi.org/10.1016/j.jmir.2013.11.002
    36. Kathrin Kettenbach, Hanno Schieferstein, Tobias L. Ross. 18 F-Labeling Using Click Cycloadditions. BioMed Research International 2014, 2014 , 1-16. https://doi.org/10.1155/2014/361329
    37. Yongjian Liu. Advances in Radiotracer Development for Molecular Imaging. 2014, 275-318. https://doi.org/10.1007/978-1-4939-0894-3_9
    38. Hanno Schieferstein, Tobias L. Ross. 18 F‐labeled folic acid derivatives for imaging of the folate receptor via positron emission tomography. Journal of Labelled Compounds and Radiopharmaceuticals 2013, 56 (9-10) , 432-440. https://doi.org/10.1002/jlcr.3104
    39. Marc Pretze, Doreen Pietzsch, Constantin Mamat. Recent Trends in Bioorthogonal Click-Radiolabeling Reactions Using Fluorine-18. Molecules 2013, 18 (7) , 8618-8665. https://doi.org/10.3390/molecules18078618
    40. Cristina Müller. Folate-Based Radiotracers for PET Imaging—Update and Perspectives. Molecules 2013, 18 (5) , 5005-5031. https://doi.org/10.3390/molecules18055005
    41. Yves Chapleur, Christine Vala, Françoise Chrétien, Sandrine Lamandé‐Langle. Toward Imaging Glycotools by Click Coupling. 2013, 183-210. https://doi.org/10.1002/9781118526996.ch7
    42. Hanno Schieferstein, Thomas Betzel, Cindy R Fischer, Tobias L Ross. 18 F-click labeling and preclinical evaluation of a new 18 F-folate for PET imaging. EJNMMI Research 2013, 3 (1) , 68. https://doi.org/10.1186/2191-219X-3-68
    43. Stefan Wagner, Klaus Kopka. Non-peptidyl 18F-Labelled PET Tracers as Radioindicators for the Noninvasive Detection of Cancer. 2013, 107-132. https://doi.org/10.1007/978-3-642-10853-2_3
    44. Berit Kühle, Cristina Müller, Tobias L. Ross. A Novel 68Ga-Labeled Pteroic Acid-Based PET Tracer for Tumor Imaging via the Folate Receptor. 2013, 257-267. https://doi.org/10.1007/978-3-642-27994-2_13
    45. Yoony YJ Gent, Karin Weijers, Carla FM Molthoff, Albert D Windhorst, Marc C Huisman, Desirée EC Smith, Sumith A Kularatne, Gerrit Jansen, Philip S Low, Adriaan A Lammertsma, Conny J van der Laken. Evaluation of the novel folate receptor ligand [18F]fluoro-PEG-folate for macrophage targeting in a rat model of arthritis. Arthritis Research & Therapy 2013, 15 (2) , R37. https://doi.org/10.1186/ar4191
    46. I. Al Jammaz, B. Al-Otaibi, S. Amer, N. Al-Hokbany, S. Okarvi. Novel synthesis and preclinical evaluation of folic acid derivatives labeled with 18F-[FDG] for PET imaging of folate receptor-positive tumors. Nuclear Medicine and Biology 2012, 39 (6) , 864-870. https://doi.org/10.1016/j.nucmedbio.2012.02.005
    47. Baohua Huang, Jolanta F. Kukowska-Latallo, Shengzhuang Tang, Hong Zong, Kali B. Johnson, Ankur Desai, Chris L. Gordon, Pascale R. Leroueil, James R. Baker. The facile synthesis of multifunctional PAMAM dendrimer conjugates through copper-free click chemistry. Bioorganic & Medicinal Chemistry Letters 2012, 22 (9) , 3152-3156. https://doi.org/10.1016/j.bmcl.2012.03.052
    48. James D. Crowley, David A. McMorran. “Click-Triazole” Coordination Chemistry: Exploiting 1,4-Disubstituted-1,2,3-Triazoles as Ligands. 2012, 31-83. https://doi.org/10.1007/7081_2011_67
    49. Uwe Ackermann, Duanne Sigmund, Shinn Dee Yeoh, Angela Rigopoulos, Graeme O'Keefe, Glenn Cartwright, Jonathan White, Andrew M. Scott, Henri J. Tochon‐Danguy. Synthesis of 2‐[(4‐[ 18 F]Fluorobenzoyloxy)methyl]‐1,4‐naphthalenedione from 2‐hydroxymethyl 1,4‐naphthoquinone and 4‐[ 18 F]fluorobenzoic acid using dicyclohexyl carbodiimide. Journal of Labelled Compounds and Radiopharmaceuticals 2011, 54 (13) , 788-794. https://doi.org/10.1002/jlcr.1932
    50. I. Al Jammaz, B. Al-Otaibi, S. Amer, S.M. Okarvi. Rapid synthesis and in vitro and in vivo evaluation of folic acid derivatives labeled with fluorine-18 for PET imaging of folate receptor-positive tumors. Nuclear Medicine and Biology 2011, 38 (7) , 1019-1028. https://doi.org/10.1016/j.nucmedbio.2011.03.004
    51. Cristina Müller, Iontcho R. Vlahov, Hari Krishna R. Santhapuram, Christopher P. Leamon, Roger Schibli. Tumor targeting using 67Ga-DOTA-Bz-folate — investigations of methods to improve the tissue distribution of radiofolates. Nuclear Medicine and Biology 2011, 38 (5) , 715-723. https://doi.org/10.1016/j.nucmedbio.2010.12.013
    52. Jie Lu, Yan Pang, Fang Xie, Hongjuan Guo, Yan Li, Zhi Yang, Xuebin Wang. Synthesis and in vitro/in vivo evaluation of 99mTc-labeled folate conjugates for folate receptor imaging. Nuclear Medicine and Biology 2011, 38 (4) , 557-565. https://doi.org/10.1016/j.nucmedbio.2010.11.007
    53. Hongjuan Guo, Fang Xie, Meilin Zhu, Yan Li, Zhi Yang, Xuebin Wang, Jie Lu. The synthesis of pteroyl-lys conjugates and its application as Technetium-99m labeled radiotracer for folate receptor-positive tumor targeting. Bioorganic & Medicinal Chemistry Letters 2011, 21 (7) , 2025-2029. https://doi.org/10.1016/j.bmcl.2011.02.014
    54. T. L. Ross, H. J. Wester. 18F: Labeling Chemistry and Labeled Compounds. 2011, 2021-2071. https://doi.org/10.1007/978-1-4419-0720-2_42
    55. Melpomeni Fani, Xuejuan Wang, Guillaume Nicolas, Christelle Medina, Isabelle Raynal, Marc Port, Helmut R. Maecke. Development of new folate-based PET radiotracers: preclinical evaluation of 68Ga-DOTA-folate conjugates. European Journal of Nuclear Medicine and Molecular Imaging 2011, 38 (1) , 108-119. https://doi.org/10.1007/s00259-010-1597-8
    56. Vincent Bouvet, Melinda Wuest, Frank Wuest. Copper-free click chemistry with the short-lived positron emitter fluorine-18. Organic & Biomolecular Chemistry 2011, 9 (21) , 7393. https://doi.org/10.1039/c1ob06034a
    57. Cristina Müller, Roger Schibli. Folic Acid Conjugates for Nuclear Imaging of Folate Receptor–Positive Cancer. Journal of Nuclear Medicine 2011, 52 (1) , 1-4. https://doi.org/10.2967/jnumed.110.076018
    58. Cristina Müller, Roger Schibli. Folate Receptor-Targeted Radionuclide Imaging Agents. 2011, 65-92. https://doi.org/10.1007/978-1-4419-8417-3_4
    59. Tobias L. Ross, Michael Honer, Cristina Müller, Viola Groehn, Roger Schibli, Simon M. Ametamey. A New 18 F-Labeled Folic Acid Derivative with Improved Properties for the PET Imaging of Folate Receptor–Positive Tumors. Journal of Nuclear Medicine 2010, 51 (11) , 1756-1762. https://doi.org/10.2967/jnumed.110.079756
    60. Zibo Li, Peter S. Conti. Radiopharmaceutical chemistry for positron emission tomography. Advanced Drug Delivery Reviews 2010, 62 (11) , 1031-1051. https://doi.org/10.1016/j.addr.2010.09.007
    61. Wu Xing, Wang Zhigang, Hu Bing, Ran Haitao, Li Pan, Xu Chuanshan, Zheng Yuanyi, Li Ao. Targeting an Ultrasound Contrast Agent to Folate Receptors on Ovarian Cancer Cells. Journal of Ultrasound in Medicine 2010, 29 (4) , 609-614. https://doi.org/10.7863/jum.2010.29.4.609
    62. Stephen Daniels, Siti Farah Md Tohid, Winnie Velanguparackel, Andrew D Westwell. The role and future potential of fluorinated biomarkers in positron emission tomography. Expert Opinion on Drug Discovery 2010, 5 (3) , 291-304. https://doi.org/10.1517/17460441003652967
    63. Dong Hyun Kim, Yearn Seong Choe, Byung-Tae Kim. Evaluation of 4-[18F]fluoro-1-butyne as a radiolabeled synthon for click chemistry with azido compounds. Applied Radiation and Isotopes 2010, 68 (2) , 329-333. https://doi.org/10.1016/j.apradiso.2009.11.003
    64. Simone Maschauer, Jürgen Einsiedel, Roland Haubner, Carsten Hocke, Matthias Ocker, Harald Hübner, Torsten Kuwert, Peter Gmeiner, Olaf Prante. Labeling and Glycosylation of Peptides Using Click Chemistry: A General Approach to 18 F‐Glycopeptides as Effective Imaging Probes for Positron Emission Tomography. Angewandte Chemie International Edition 2010, 49 (5) , 976-979. https://doi.org/10.1002/anie.200904137
    65. Simone Maschauer, Jürgen Einsiedel, Roland Haubner, Carsten Hocke, Matthias Ocker, Harald Hübner, Torsten Kuwert, Peter Gmeiner, Olaf Prante. Markierung und Glycosylierung von Peptiden mithilfe der Klick‐Chemie: ein allgemeiner Ansatz zur Synthese von 18 F‐Glycopeptiden, leistungsstarken Tracern für die Positronenemissionstomographie. Angewandte Chemie 2010, 122 (5) , 988-992. https://doi.org/10.1002/ange.200904137
    66. Matthias Glaser, Edward G. Robins. ‘Click labelling’ in PET radiochemistry. Journal of Labelled Compounds and Radiopharmaceuticals 2009, 52 (10) , 407-414. https://doi.org/10.1002/jlcr.1656
    67. Patrick Dupont, James Warwick. Kinetic modelling in small animal imaging with PET. Methods 2009, 48 (2) , 98-103. https://doi.org/10.1016/j.ymeth.2009.03.008
    68. Kim Serdons, Alfons Verbruggen, Guy M. Bormans. Developing new molecular imaging probes for PET. Methods 2009, 48 (2) , 104-111. https://doi.org/10.1016/j.ymeth.2009.03.010
    69. Kido Nwe, Martin W. Brechbiel. Growing Applications of “Click Chemistry” for Bioconjugation in Contemporary Biomedical Research. Cancer Biotherapy and Radiopharmaceuticals 2009, 24 (3) , 289-302. https://doi.org/10.1089/cbr.2008.0626

    Bioconjugate Chemistry

    Cite this: Bioconjugate Chem. 2008, 19, 12, 2462–2470
    Click to copy citationCitation copied!
    https://doi.org/10.1021/bc800356r
    Published November 24, 2008
    Copyright © 2008 American Chemical Society

    Article Views

    2914

    Altmetric

    -

    Citations

    Learn about these metrics

    Article Views are the COUNTER-compliant sum of full text article downloads since November 2008 (both PDF and HTML) across all institutions and individuals. These metrics are regularly updated to reflect usage leading up to the last few days.

    Citations are the number of other articles citing this article, calculated by Crossref and updated daily. Find more information about Crossref citation counts.

    The Altmetric Attention Score is a quantitative measure of the attention that a research article has received online. Clicking on the donut icon will load a page at altmetric.com with additional details about the score and the social media presence for the given article. Find more information on the Altmetric Attention Score and how the score is calculated.