Current status of radiopharmaceuticals for the theranostics of neuroendocrine neoplasms

Pharmaceuticals

Volumn 10, Issue 1, 2017, Pages

  Fani, Melpomeni ^a   Peitl, Petrakolenc ^b   Velikyan, Irina ^c  

^a UNIVERSITY HOSPITAL BASEL   (Switzerland)

^b UNIVERSITY MEDICAL CENTRE LJUBLJANA   (Slovenia)

^c UPPSALA UNIVERSITY   (Sweden)

Author keywords

CCK2; Exendin 4; Gastrin; GIP; GLP 1R; Neuroendocrine neoplasms; Radiolabeled peptides; Somatostatin receptor antagonists; Theranostics

Indexed keywords

CHOLECYSTOKININ; CHOLECYSTOKININ 2; CHOLECYSTOKININ B RECEPTOR; GASTRIC INHIBITORY POLYPEPTIDE RECEPTOR; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; HORMONE RECEPTOR; PEPTIDE DERIVATIVE; RADIOISOTOPE; RADIOLIGAND; RADIOPHARMACEUTICAL AGENT; RECEPTOR BLOCKING AGENT; SOMATOSTATIN DERIVATIVE; SOMATOSTATIN RECEPTOR; SOMATOSTATIN RECEPTOR ANTAGONIST; UNCLASSIFIED DRUG;

CLINICAL RESEARCH; DIAGNOSTIC TEST; DOSIMETRY; DRUG SYNTHESIS; EVIDENCE BASED MEDICINE; FEASIBILITY STUDY; HUMAN; IN VITRO STUDY; INSULINOMA; ISOTOPE LABELING; NEUROENDOCRINE TUMOR; NONHUMAN; PERSONALIZED MEDICINE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TARGETING; REVIEW; THYROID CANCER; TUMOR DIAGNOSIS;

EID: 85015669131     PISSN: None     EISSN: 14248247     Source Type: Journal    
DOI: 10.3390/ph10010030     Document Type: Review

References (133)

1. Carrasquillo, J.A.; Chen, C.C. Molecular imaging of neuroendocrine tumors. Semin. Oncol. 2010, 37, 662-679.
2. Bodei, L.; Sundin, A.; Kidd, M.; Prasad, V.; Modlin, I.M. The status of neuroendocrine tumor imaging: From darkness to light? Neuroendocrinology 2015, 101, 1-17.
3. Fani, M. Current and future radiopharmaceuticals in neuroendocrine tumor imaging In Diagnostic and Therapeutic Nuclear Medicine for Neuroendocrine Tumors; Taïeb, D., Pacak, K., Eds.; Springer: Cham, Switzerland, 2017; pp 141-162.
4. Oberg, K. Molecular imaging radiotherapy: Theranostics for personalized patient management of neuroendocrine tumors (nets). Theranostics 2012, 2, 448-458.
5. Werner, R.A.; Bluemel, C.; Allen-Auerbach, M.S.; Higuchi, T.; Herrmann, K. 68Gallium- and 90Yttrium-/177Lutetium: “Theranostic twins” for diagnosis and treatment of nets. Ann. Nucl. Med. 2015, 29, 1-7.
6. Velikyan, I. Radionuclides for imaging and therapy in oncology. In CancerTheranostics; Chen, X.; Wong, S., Eds.; Elsevier: Amsterdam, The Netherlands, 2014; pp 285-325.
7. Nicolas, G.; Giovacchini, G.; Muller-Brand, J.; Forrer, F. Targeted radiotherapy with radiolabeled somatostatin analogs. Endocrinol. Metab. Clin. N. Am. 2011, 40, 187-204.
8. Reubi, J.C. Somatostatin receptor sst1-sst5 expression in normal and neoplastic human tissues using receptor autoradiography with subtype-selective ligands. Eur. J. Nucl. Med. 2001, 28, 836-846.
9. Kwekkeboom, D.J.; Kam, B.L.; van Essen, M.; Teunissen, J.J.M.; van Eijck, C.H.J.; Valkema, R.; de Jong, M.; de Herder, W.W.; Krenning, E.P. Somatostatin receptor-based imaging and therapy of gastroenteropancreatic neuroendocrine tumors. Endocr. Relat. Cancer 2010, 17, R53-R73.
10. Ambrosini, V.; Campana, D.; Tomassetti, P.; Fanti, S. 68Ga-labelled peptides for diagnosis of gastroenteropancreatic net. Eur. J. Nucl. Med. Mol. Imaging 2012, 39 (Suppl 1), S52-S60.
11. Van Essen, M.; Krenning, E.P.; Kam, B.L.; de Jong, M.; Valkema, R.; Kwekkeboom, D.J. Peptide-receptor radionuclide therapy for endocrine tumors. Nat. Rev. Endocrinol. 2009, 5, 382-393.
12. Perrin, M.H.; Sutton, S.W.; Cervini, L.A.; Rivier, J.E.; Vale, W.W. Comparison of an agonist, urocortin, and an antagonist, astressin, as radioligands for characterization of corticotropin-releasing factor receptors. J. Pharmacol. Exp. Ther. 1999, 288, 729-734.
13. Sleight, A.J.; Stam, N.J.; Mutel, V.; Vanderheyden, P.M. Radiolabelling of the human 5-ht2a receptor with an agonist, a partial agonist and an antagonist: Effects on apparent agonist affinities. Biochem. Pharmacol. 1996, 51, 71-76.
14. Ginj, M.; Zhang, H.; Waser, B.; Cescato, R.; Wild, D.; Wang, X.; Erchegyi, J.; Rivier, J.; Macke, H.R.; Reubi, J.C. Radiolabeled somatostatin receptor antagonists are preferable to agonists for in vivo peptide receptor targeting of tumors. Proc. Natl. Acad. Sci. USA 2006, 103, 16436-16441.
15. Bass, R.T.; Buckwalter, B.L.; Patel, B.P.; Pausch, M.H.; Price, L.A.; Strnad, J.; Hadcock, J.R. Identification and characterization of novel somatostatin antagonists. Mol. Pharmacol. 1996, 50, 709-715.
16. Reubi, J.C.; Schaer, J.C.; Wenger, S.; Hoeger, C.; Erchegyi, J.; Waser, B.; Rivier, J. Sst3-selective potent peptidic somatostatin receptor antagonists. Proc. Natl. Acad. Sci. USA 2000, 97, 13973-13978.
17. Reubi, J.C.; Schär, J.-C.; Waser, B.; Wenger, S.; Heppeler, A.; Schmitt, J.S.; Mäcke, H.R. Affinity profiles for human somatostatin receptor subtypes sst1-sst5 of somatostatin radiotracers selected for scintigraphic and radiotherapeutic use. Eur. J. Nucl. Med. Mol. Imaging 2000, 27, 273-282.
18. Wang, X.; Fani, M.; Schulz, S.; Rivier, J.; Reubi, J.C.; Maecke, H.R. Comprehensive evaluation of a somatostatin-based radiolabelled antagonist for diagnostic imaging and radionuclide therapy. Eur. J. Nucl. Med. Mol. Imaging 2012, 39, 1876-1885.
19. Wadas, T.J.; Eiblmaier, M.; Zheleznyak, A.; Sherman, C.D.; Ferdani, R.; Liang, K.; Achilefu, S.; Anderson, C.J. Preparation and biological evaluation of 64cu-cb-te2a-sst2-ant, a somatostatin antagonist for pet imaging of somatostatin receptor-positive tumors. J. Nucl. Med. 2008, 49, 1819-1827.
20. Cescato, R.; Erchegyi, J.; Waser, B.; Piccand, V.; Maecke, H.R.; Rivier, J.E.; Reubi, J.C. Design and in vitro characterization of highly sst2-selective somatostatin antagonists suitable for radiotargeting. J. Med. Chem. 2008, 51, 4030-4037.
21. Hocart, S.J.; Jain, R.; Murphy, W.A.; Taylor, J.E.; Coy, D.H. Highly potent cyclic disulfide antagonists of somatostatin. J. Med. Chem. 1999, 42, 1863-1871.
22. Fani, M.; Del Pozzo, L.; Abiraj, K.; Mansi, R.; Tamma, M.L.; Cescato, R.; Waser, B.; Weber, W.A.; Reubi, J.C.; Maecke, H.R. Pet of somatostatin receptor-positive tumors using 64cu- and 68ga-somatostatin antagonists: The chelate makes the difference. J. Nucl. Med. 2011, 52, 1110-1118.
23. Fani, M.; Braun, F.; Waser, B.; Beetschen, K.; Cescato, R.; Erchegyi, J.; Rivier, J.E.; Weber, W.A.; Maecke, H.R.; Reubi, J.C. Unexpected sensitivity of sst2 antagonists to n-terminal radiometal modifications. J. Nucl. Med. 2012, 53, 1481-1489.
24. Antunes, P.; Ginj, M.; Zhang, H.; Waser, B.; Baum, R.P.; Reubi, J.C.; Maecke, H. Are radiogallium-labelled dota-conjugated somatostatin analogues superior to those labelled with other radiometals? Eur. J. Nucl. Med. Mol. Imaging 2007, 34, 982-993.
25. Dalm, S.U.; Nonnekens, J.; Doeswijk, G.N.; de Blois, E.; van Gent, D.C.; Konijnenberg, M.W.; de Jong, M. Comparison of the therapeutic response to treatment with a 177lu-labeled somatostatin receptor agonist and antagonist in preclinical models. J. Nucl. Med. 2016, 57, 260-265.
26. Nicolas, G.; Mansi, R.; Vomstein, S.; Kaufmann, J.; Bouterfa, H.; Maecke, H.; Wild, D.; Fani, M. Wider safety window with radiolabeled somatostatin receptor antagonists over agonists. J. Nucl. Med. 2015, 56, 335.
27. Nicolas, G.P.; Vomstein, S.; Bouterfa, H.; Maecke, H.R.; Wild, D.; Fani, M. Higher tumour uptake and residence time enhances the therapeutic index of the radiolabeled somatostatin antagonists over the agonists: The influence of the peptide mass. Eur. J. Nucl. Med. Mol. Imaging 2014, 41, S292.
28. Nicolas G.P.; Mansi, R.; McDougall Kaufmann, L.; Bouterfa, H.; Wild, D.; Fani, M. Biodistribution, pharmacokinetics and dosimetry of 177lu-, 90y- and 111in-labeled somatostatin receptor antagonist ops201 in comparison to the agonist 177lu-dota-tate: The mass effect. J. Nucl. Med. 2017, in press.
29. Cescato, R.; Waser, B.; Fani, M.; Reubi, J.C. Evaluation of 177lu-dota-sst2 antagonist versus 177lu-dota-sst2 agonist binding in human cancers in vitro. J. Nucl. Med. 2011, 52, 1886-1890.
30. Reubi, J.C.; Waser, B.; Maecke, H.R.; Rivier, J.E. Highly increased 125i-jr11 antagonist binding in vitro reveals novel indications for sst2 targeting in human cancers. J. Nucl. Med. 2017, 58, 300-306.
31. Wild, D.; Fani, M.; Behe, M.; Brink, I.; Rivier, J.E.; Reubi, J.C.; Maecke, H.R.; Weber, W.A. First clinical evidence that imaging with somatostatin receptor antagonists is feasible. J. Nucl. Med. 2011, 52, 1412-1417.
32. Wild, D.; Fani, M.; Fischer, R.; Del Pozzo, L.; Kaul, F.; Krebs, S.; Fischer, R.; Rivier, J.E.; Reubi, J.C.; Maecke, H.R. et al. Comparison of somatostatin receptor agonist and antagonist for peptide receptor radionuclide therapy: A pilot study. J. Nucl. Med. 2014, 55, 1248-1252.
33. Nicolas, G.; Schreiter, N.; Kaul, F.; Uiters, J.; Mena, R.; Bouterfa, H.; Maecke, H.; Fani, M.; Wild, D. Pet/ct with the somatostatin receptor antagonist 68ga-ops202 is twice as accurate as with the agonist 68ga-dotatoc for detecting liver metastases: Results of a phase 1/2 study in gastroenteropancreatic net patients. J. Nucl. Med. 2016, 57, 154.
34. Sandstrom, M.; Velikyan, I.; Garske-Roman, U.; Sorensen, J.; Eriksson, B.; Granberg, D.; Lundqvist, H.; Sundin, A.; Lubberink, M. Comparative biodistribution and radiation dosimetry of 68ga-dotatoc and 68gadotatate in patients with neuroendocrine tumors. J. Nucl. Med. 2013, 54, 1755-1759.
35. Körner, M.; Christ, E.; Wild, D.; Reubi, J.C. Glucagon-like peptide-1 receptor overexpression in cancer and its impact on clinical applications. Front. Endocrinol. 2012, 3, 158.
36. Korner, M.; Stockli, M.; Waser, B.; Reubi, J.C. Glp-1 receptor expression in human tumors and human normal tissues: Potential for in vivo targeting. J. Nucl. Med. 2007, 48, 736-743.
37. Reubi, J.C.; Waser, B. Concomitant expression of several peptide receptors in neuroendocrine tumours: Molecular basis for in vivo multireceptor tumour targeting. Eur. J. Nucl. Med. Mol. Imaging 2003, V30, 781-793.
38. De Herder, W.W.; Niederle, B.; Scoazec, J.Y.; Pauwels, S.; Klöppel, G.; Falconi, M.; Kwekkeboom, D.J.; Öberg, K.; Eriksson, B.; Wiedenmann, B. et al. Well-differentiated pancreatic tumor/carcinoma: Insulinoma. Neuroendocrinology 2006, 84, 183-188.
39. Soga, J.; Yakuwa, Y. Pancreatic endocrinomas: A statistical analysis of 1857 cases. J. Hepato-Biliary-Pancreat. Surg. 1994, 1, 522-529.
40. Öberg, K.; Eriksson, B. Endocrine tumours of the pancreas. Best Pract. Res. Clin. Gastroenterol. 2005, 19, 753-781.
41. Aisha, S.; Lubna, M.Z.; Huque, N. Recurrent insulinoma-Rare among the rarities. J. Coll. Phys. Surg. Pak. 2007, 17, 364-366.
42. Krenning, E.P.; Kwekkeboom, D.J.; Reubi, J.C.; van Hagen, P.M.; van Eijck, C.H.J.; Oei, H.Y.; Lamberts, S.W.J. 111in-octreotide scintigraphy in oncology. Metabolism 1992, 41, 83-86.
43. Krenning, E.P.; Kwekkeboom, D.J.; Bakker, W.H.; Breeman, W.A.; Kooij, P.P.; Oei, H.Y.; van Hagen, M.; Postema, P.T.; de Jong, M.; Reubi, J.C. et al. Somatostatin receptor scintigraphy with [111in-dtpa-d-phe1]- and [123i-tyr3]-octreotide: The rotterdam experience with more than 1000 patients. Eur. J. Nucl. Med. 1993, 20, 716-731.
44. Reubi, J.C. Peptide receptors as molecular targets for cancer diagnosis and therapy. Endocr. Rev. 2003, 24, 389-427.
45. Wild, D.; Christ, E.; Caplin, M.E.; Kurzawinski, T.R.; Forrer, F.; Brandle, M.; Seufert, J.; Weber, W.A.; Bomanji, J.; Perren, A. et al. Glucagon-like peptide-1 versus somatostatin receptor targeting reveals 2 distinct forms of malignant insulinomas. J. Nucl. Med. 2011, 52, 1073-1078.
46. Eriksson, O.; Velikyan, I.; Selvaraju, R.K.; Kandeel, F.; Johansson, L.; Antoni, G.; Eriksson, B.; Sörensen, J.; Korsgren, O. Detection of metastatic insulinoma by positron emission tomography with [68ga]exendin-4-a case report. J. Clin. Endocrinol. Metab. 2014, 99, 1519-1524.
47. Luo, Y.; Pan, Q.; Yao, S.; Yu, M.; Wu, W.; Xue, H.; Kiesewetter, D.O.; Zhu, Z.; Li, F.; Zhao, Y. et al. Glucagonlike peptide-1 receptor pet/ct with 68ga-nota-exendin-4 for detecting localized insulinoma: A prospective cohort study. J. Nucl. Med. 2016, 57, 715-720.
48. Sowa-Staszczak, A.; Trofimiuk-Muldner, M.; Stefanska, A.; Tomaszuk, M.; Buziak-Bereza, M.; Gilis-Januszewska, A.; Jabrocka-Hybel, A.; Glowa, B.; Malecki, M.; Bednarczuk, T.;et al. 99mtc labeled glucagonlike peptide-1-analogue (99mtc-glp1) scintigraphy in the management of patients with occult insulinoma. PLoS ONE 2016, 11, e0160714.
49. Okabayashi, T.; Shima, Y.; Sumiyoshi, T.; Kozuki, A.; Ito, S.; Ogawa, Y.; Kobayashi, M.; Hanazaki, K. Diagnosis and management of insulinoma. World J. Gastroenterol. 2013, 19, 829-837.
50. Gotthardt, M.; Lalyko, G.; van Eerd-Vismale, J.; Keil, B.; Schurrat, T.; Hower, M.; Laverman, P.; Behr, T.M.; Boerman, O.C.; Göke, B. et al. A new technique for in vivo imaging of specific glp-1 binding sites: First results in small rodents. Regul. Pept. 2006, 137, 162-167.
51. Wild, D.; Behe, M.; Wicki, A.; Storch, D.; Waser, B.; Gotthardt, M.; Keil, B.; Christofori, G.; Reubi, J.C.; Macke, H.R. [lys40(ahx-dtpa-111in)nh2]exendin-4, a very promising ligand for glucagon-like peptide-1 (glp-1) receptor targeting. J. Nucl. Med. 2006, 47, 2025-2033.
52. Gotthardt, M.; Fischer, M.; Naeher, I.; Holz, J.B.; Jungclas, H.; Fritsch, H.W.; Behe, M.; Goke, B.; Joseph, K.; Behr, T.M. Use of the incretin hormone glucagon-like peptide-1 (glp-1) for the detection of insulinomas: Initial experimental results. Eur. J. Nucl. Med. Mol. Imaging 2002, 29, 597-606.
53. Wild, D.; Macke, H.; Christ, E.; Gloor, B.; Reubi, J.C. Glucagon-like peptide 1-receptor scans to localize occult insulinomas. New Engl. J. Med. 2008, 359, 766-768.
54. Sowa-Staszczak, A.; Pach, D.; Mikolajczak, R.; Macke, H.; Jabrocka-Hybel, A.; Stefanska, A.; Tomaszuk, M.; Janota, B.; Gilis-Januszewska, A.; Malecki, M. et al. Glucagon-like peptide-1 receptor imaging with [lys40(ahx-hynic-99mtc/edda)nh2]-exendin-4 for the detection of insulinoma. Eur. J. Nucl. Med. Mol. Imaging 2013, 40, 524-531.
55. Christ, E.; Wild, D.; Forrer, F.; Brandle, M.; Sahli, R.; Clerici, T.; Gloor, B.; Martius, F.; Maecke, H.; Reubi, J.C. Glucagon-like peptide-1 receptor imaging for localization of insulinomas. J. Clin. Endocrinol. Metab. 2009, 94, 4398-4405.
56. Brom, M.; Joosten, L.; Oyen, W.J.G.; Gotthardt, M.; Boerman, O.C. Radiolabelled glp-1 analogues for in vivo targeting of insulinomas. Contrast Media Mol. Imaging 2012, 7, 160-166.
57. Brom, M.; Oyen, W.J.; Joosten, L.; Gotthardt, M.; Boerman, O.C. 68ga-labelled exendin-3, a new agent for the detection of insulinomas with pet. Eur. J. Nucl. Med. Mol. Imaging 2010, 37, 1345-1355.
58. Wild, D.; Wicki, A.; Mansi, R.; Behe, M.; Keil, B.; Bernhardt, P.; Christofori, G.; Ell, P.J.; Macke, H.R. Exendin-4-based radiopharmaceuticals for glucagonlike peptide-1 receptor pet/ct and spect/ct. J. Nucl. Med. 2010, 51, 1059-1067.
59. Selvaraju, R.K.; Velikyan, I.; Asplund, V.; Johansson, L.; Wu, Z.; Todorov, I.; Shively, J.; Kandeel, F.; Eriksson, B.; Korsgren, O. et al. Pre-clinical evaluation of [68ga]ga-do3a-vs-cys40-exendin-4 for imaging of insulinoma. Nucl. Med. Biol. 2014, 41, 471-476.
60. Wu, Z.; Liu, S.; Nair, I.; Omori, K.; Scott, S.; Todorov, I.; Shively, J.E.; Conti, P.S.; Li, Z.; Kandeel, F. (64)cu labeled sarcophagine exendin-4 for micropet imaging of glucagon like peptide-1 receptor expression. Theranostics 2014, 4, 770-777.
61. Wang, Y.; Lim, K.; Normandin, M.; Zhao, X.; Cline, G.W.; Ding, Y.S. Synthesis and evaluation of [18f]exendin (9-39) as a potential biomarker to measure pancreatic beta-cell mass. Nucl. Med. Biol. 2012, 39, 167-176.
62. Gao, H.; Niu, G.; Yang, M.; Quan, Q.; Ma, Y.; Murage, E.N.; Ahn, J.M.; Kiesewetter, D.O.; Chen, X. Pet of insulinoma using (1)(8)f-fbem-em3106b, a new glp-1 analogue. Mol. Pharm. 2011, 8, 1775-1782.
63. Kiesewetter, D.O.; Gao, H.; Ma, Y.; Niu, G.; Quan, Q.; Guo, N.; Chen, X. 18f-radiolabeled analogs of exendin-4 for pet imaging of glp-1 in insulinoma. Eur. J. Nucl. Med. Mol. Imaging 2012, 39, 463-473.
64. Luo, Y.; Yu, M.; Pan, Q.; Wu, W.; Zhang, T.; Kiesewetter, D.O.; Zhu, Z.; Li, F.; Chen, X.; Zhao, Y. 68ga-notaexendin-4 pet/ct in detection of occult insulinoma and evaluation of physiological uptake. Eur. J. Nucl. Med. Mol. Imaging 2015, 42, 531-532.
65. Christ, E.; Wild, D.; Antwi, K.; Waser, B.; Fani, M.; Schwanda, S.; Heye, T.; Schmid, C.; Baer, H.U.; Perren, A. et al. Preoperative localization of adult nesidioblastosis using 68ga-dota-exendin-4-pet/ct. Endocrine 2015, 50, 821-823.
66. Jodal, A.; Lankat-Buttgereit, B.; Brom, M.; Schibli, R.; Behe, M. A comparison of three (67/68)ga-labelled exendin-4 derivatives for beta-cell imaging on the glp-1 receptor: The influence of the conjugation site of nodaga as chelator. EJNMMI Res. 2014, 4, 31.
67. Selvaraju, R.K.; Velikyan, I.; Johansson, L.; Wu, Z.; Todorov, I.; Shively, J.; Kandeel, F.; Korsgren, O.; Eriksson, O. In vivo imaging of the glucagonlike peptide 1 receptor in the pancreas with 68ga-labeled do3aexendin-4. J. Nucl. Med. 2013, 54, 1458-1463.
68. Kirsi, M.; Yim, C.B.; Veronica, F.; Tamiko, I.; Viki-Veikko, E.; Johan, R.; Jori, J.; Tiina, S.; Tuula, T.; Marko, T. et al. 64cu- and 68ga-labelled [nle14,lys 40(ahx-nodaga)nh2]-exendin-4 for pancreatic beta cell imaging in rats. Mol. Imaging Biol. 2014, 16, 255-263.
69. Wu, Z.; Todorov, I.; Li, L.; Bading, J.R.; Li, Z.; Nair, I.; Ishiyama, K.; Colcher, D.; Conti, P.E.; Fraser, S.E. et al. In vivo imaging of transplanted islets with 64cu-do3a-vs-cys40-exendin-4 by targeting glp-1 receptor. Bioconjug.Chem. 2011, 22, 1587-1594.
70. Kiesewetter, D.O.; Guo, N.; Guo, J.; Gao, H.; Zhu, L.; Ma, Y.; Niu, G.; Chen, X. Evaluation of an [(18)f]alfnota analog of exendin-4 for imaging of glp-1 receptor in insulinoma. Theranostics 2012, 2, 999-1009.
71. Yue, X.; Kiesewetter, D.O.; Guo, J.; Sun, Z.; Zhang, X.; Zhu, L.; Niu, G.; Ma, Y.; Lang, L.; Chen, X. Development of a new thiol site-specific prosthetic group and its conjugation with [cys40]-exendin-4 for in vivo targeting of insulinomas. Bioconjug. Chem. 2013, 24, 1191-1200.
72. Yue, X.; Yan, X.; Wu, C.; Niu, G.; Ma, Y.; Jacobson, O.; Shen, B.; Kiesewetter, D.O.; Chen, X. One-pot twostep radiosynthesis of a new (18)f-labeled thiol reactive prosthetic group and its conjugate for insulinoma imaging. Mol. Pharm. 2014, 11, 3875-3884.
73. Wu, H.; Liang, S.; Liu, S.; Pan, Y.; Cheng, D.; Zhang, Y. 18f-radiolabeled glp-1 analog exendin-4 for pet/ct imaging of insulinoma in small animals. Nucl. Med. Commun. 2013, 34, 701-708.
74. Wu, Z.; Liu, S.; Hassink, M.; Nair, I.; Park, R.; Li, L.; Todorov, I.; Fox, J.M.; Li, Z.; Shively, J.E. et al. Development and evaluation of 18f-ttco-cys40-exendin-4: A pet probe for imaging transplanted islets. J. Nucl. Med. 2013, 54, 244-251.
75. Bauman, A.; Valverde, I.E.; Fischer, C.A.; Vomstein, S.; Mindt, T.L. Development of 68ga- and 89zr-labeled exendin-4 as potential radiotracers for the imaging of insulinomas by pet. J. Nucl. Med. 2015, 56, 1569-1574.
76. Janota, B.; Karczmarczyk, U.; Laszuk, E.; Garnuszek, P.; Mikolajczak, R. Oxidation of methionine-Is it limiting the diagnostic properties of 99mtc-labeled exendin-4, a glucagon-like peptide-1 receptor agonist? Nucl. Med. Rev. Cent. East. Eur. 2016, 19, 104-110.
77. Espes, D.; Selvaraju, R.; Velikyan, I.; Krajcovic, M.; Carlsson, P.O.; Eriksson, O. Quantification of beta-cell mass in intramuscular islet grafts using radiolabeled exendin-4. Transpl. Direct 2016, 2, e93.
78. Christ, E.; Wild, D.; Ederer, S.; Béhé, M.; Nicolas, G.; Caplin, M.E.; Brändle, M.; Clerici, T.; Fischli, S.; Stettler, C. et al. Glucagon-like peptide-1 receptor imaging for the localisation of insulinomas: A prospective multicentre imaging study. Lancet Diabetes Endocrinol. 2013, 1, 115-122.
79. Pach, D.; Sowa-Staszczak, A.; Jabrocka-Hybel, A.; Stefanska, A.; Tomaszuk, M.; Mikolajczak, R.; Janota, B.; Trofimiuk-Muldner, M.; Przybylik-Mazurek, E.; Hubalewska-Dydejczyk, A. Glucagon-like peptide-1 receptor imaging with [lys (40) (ahx-hynic-(99 m) tc/edda)nh 2]-exendin-4 for the diagnosis of recurrence or dissemination of medullary thyroid cancer: A preliminary report. Int. J. Endocrinol. 2013, 2013, 384508.
80. Velikyan, I. Prospective of 68ga-radiopharmaceutical development. Theranostics 2014, 4, 47-80.
81. Nalin, L.; Selvaraju, R.K.; Velikyan, I.; Berglund, M.; Andreasson, S.; Wikstrand, A.; Ryden, A.; Lubberink, M.; Kandeel, F.; Nyman, G. et al. Positron emission tomography imaging of the glucagon-like peptide-1 receptor in healthy and streptozotocin-induced diabetic pigs. Eur. J. Nucl. Med. Mol. Imaging 2014, 41, 1800-1810.
82. Ryden, A.; Nyman, G.; Nalin, L.; Andreasson, S.; Velikyan, I.; Korsgren, O.; Eriksson, O.; Jensen-Waern, M. Corrigendum to “cardiovascular side-effects and insulin secretion after intravenous administration of radiolabeled exendin-4 in pigs” [nucl med biol 43 (2016) 397-402]. Nucl. Med. Biol. 2016, 43, 742.
83. Selvaraju, R.; Bulenga, T.N.; Espes, D.; Lubberink, M.; Sörensen, J.; Eriksson, B.; Estrada, S.; Velikyan, I.; Eriksson, O. Dosimetry of [68ga]ga-do3a-vs-cys40-exendin-4 in rodents, pigs, non-human primates and human - repeated scanning in human is possible. Am. J. Nucl. Med. Mol. Imaging 2015, 5, 259-269.
84. Velikyan, I.; Bulenga, T.N.; Selvaraju, K.R.; Lubberink, M.; Espes, D.; Rosenstrom, U.; Eriksson, O. Dosimetry of [177lu]-do3a-vs-cys40-exendin-4-Impact on the feasibility of insulinoma internal radiotherapy. Am. J. Nucl. Med. Mol. Imaging 2015, 5, 109-126.
85. Rylova, S.N.; Waser, B.; Del Pozzo, L.; Tonnesmann, R.; Mansi, R.; Meyer, P.T.; Reubi, J.C.; Maecke, H.R. Approaches to improve the pharmacokinetics of radiolabeled glucagon-like peptide-1 receptor ligands using antagonistic tracers. J. Nucl. Med. 2016, 57, 1282-1288.
86. Mukai, E.; Toyoda, K.; Kimura, H.; Kawashima, H.; Fujimoto, H.; Ueda, M.; Temma, T.; Hirao, K.; Nagakawa, K.; Saji, H. et al. Glp-1 receptor antagonist as a potential probe for pancreatic β-cell imaging. Biochem. Biophys. Res. Commun. 2009, 389, 523-526.
87. Waser, B.; Reubi, J.C. Radiolabelled glp-1 receptor antagonist binds to glp-1 receptor-expressing human tissues. Eur. J. Nucl. Med. Mol. Imaging 2014, 41, 1166-1171.
88. Gotthardt, M.; van Eerd-Vismale, J.; Oyen, W.J.; de Jong, M.; Zhang, H.; Rolleman, E.; Maecke, H.R.; Béhé, M.; Boerman, O. Indication for different mechanisms of kidney uptake of radiolabeled peptides. J. Nucl. Med. 2007, 48, 596-601.
89. Laeppchen, T.; Toennesmann, R.; Meyer, P.; Maecke, H.; Rylova, S. Radioiodinated exendin-4 demonstrates superior pharmacokinetics compared to radiometalated analogs. J. Nucl. Med. 2016, 57, 1388.
90. Wicki, A.; Wild, D.; Storch, D.; Seemayer, C.; Gotthardt, M.; Behe, M.; Kneifel, S.; Mihatsch, M.J.; Reubi, J.C.; Macke, H.R. et al. [lys40(ahx-dtpa-111in)nh2]-exendin-4 is a highly efficient radiotherapeutic for glucagon-like peptide-1 receptor-targeted therapy for insulinoma. Clin. Cancer Res. 2007, 13, 3696-3705.
91. Reubi, J.C.; Schaer, J.C.; Waser, B. Cholecystokinin(cck)-a and cck-b/gastrin receptors in human tumors. Cancer Res. 1997, 57, 1377-1386.
92. Reubi, J.C.; Waser, B. Unexpected high incidence of cholecystokinin-b/gastrin receptors in human medullary thyroid carcinomas. Int. J. Cancer 1996, 67, 644-647.
93. Kebebew, E.; Kikuchi, S.; Duh, Q.Y.; Clark, O.H. Long-term results of reoperation and localizing studies in patients with persistent or recurrent medullary thyroid cancer. Arch. Surg. 2000, 135, 895-901.
94. Pacini, F.; Castagna, M.G.; Cipri, C.; Schlumberger, M. Medullary thyroid carcinoma. Clin. Oncol. (R. Coll. Radiol.) 2010, 22, 475-485.
95. Treglia, G.; Aktolun, C.; Chiti, A.; Frangos, S.; Giovanella, L.; Hoffmann, M.; Iakovou, I.; Mihailovic, J.; Krause, B.J.; Langsteger, W. et al. The 2015 revised american thyroid association guidelines for the management of medullary thyroid carcinoma: The “evidence-based” refusal to endorse them by eanm due to the “not evidence-based” marginalization of the role of nuclear medicine. Eur. J. Nucl. Med. Mol. Imaging 2016, 43, 1486-1490.
96. Wells, S.A., Jr.; Asa, S.L.; Dralle, H.; Elisei, R.; Evans, D.B.; Gagel, R.F.; Lee, N.; Machens, A.; Moley, J.F.; Pacini, F. et al. Revised american thyroid association guidelines for the management of medullary thyroid carcinoma. Thyroid 2015, 25, 567-610.
97. Moley, J.F. Medullary thyroid cancer. Surg. Clin. N. Am. 1995, 75, 405-420.
98. Gotthardt, M.; Behe, M.P.; Beuter, D.; Battmann, A.; Bauhofer, A.; Schurrat, T.; Schipper, M.; Pollum, H.; Oyen, W.J.; Behr, T.M. Improved tumour detection by gastrin receptor scintigraphy in patients with metastasised medullary thyroid carcinoma. Eur. J. Nucl. Med. Mol. Imaging 2006, 33, 1273-1279.
99. Gotthardt, M.; Behe, M.P.; Grass, J.; Bauhofer, A.; Rinke, A.; Schipper, M.L.; Kalinowski, M.; Arnold, R.; Oyen, W.J.; Behr, T.M. Added value of gastrin receptor scintigraphy in comparison to somatostatin receptor scintigraphy in patients with carcinoids and other neuroendocrine tumours. Endocr. Relat. Cancer 2006, 13, 1203-1211.
100. Behr, T.M.; Gratz, S.; Markus, P.M.; Dunn, R.M.; Hufner, M.; Schauer, A.; Fischer, M.; Munz, D.L.; Becker, H.; Becker, W. Anti-carcinoembryonic antigen antibodies versus somatostatin analogs in the detection of metastatic medullary thyroid carcinoma: Are carcinoembryonic antigen and somatostatin receptor expression prognostic factors? Cancer 1997, 80, 2436-2457.
101. De Jong, M.; Bakker, W.H.; Bernard, B.F.; Valkema, R.; Kwekkeboom, D.J.; Reubi, J.C.; Srinivasan, A.; Schmidt, M.; Krenning, E.P. Preclinical and initial clinical evaluation of 111in-labeled nonsulfated cck8 analog: A peptide for cck-b receptor-targeted scintigraphy and radionuclide therapy. J. Nucl. Med. 1999, 40, 2081-2087.
102. Kwekkeboom, D.J.; Bakker, W.H.; Kooij, P.P.; Erion, J.; Srinivasan, A.; de Jong, M.; Reubi, J.C.; Krenning, E.P. Cholecystokinin receptor imaging using an octapeptide dtpa-cck analogue in patients with medullary thyroid carcinoma. Eur. J. Nucl. Med. 2000, 27, 1312-1317.
103. Behr, T.M.; Behe, M.; Angerstein, C.; Gratz, S.; Mach, R.; Hagemann, L.; Jenner, N.; Stiehler, M.; Frank-Raue, K.; Raue, F. et al. Cholecystokinin-b/gastrin receptor binding peptides: Preclinical development and evaluation of their diagnostic and therapeutic potential. Clin. Cancer Res. 1999, 5, 3124s-3138s.
104. Behr, T.M.; Jenner, N.; Radetzky, S.; Behe, M.; Gratz, S.; Yucekent, S.; Raue, F.; Becker, W. Targeting of cholecystokinin-b/gastrin receptors in vivo: Preclinical and initial clinical evaluation of the diagnostic and therapeutic potential of radiolabelled gastrin. Eur. J. Nucl. Med. 1998, 25, 424-430.
105. Behr, T.M.; Jenner, N.; Behe, M.; Angerstein, C.; Gratz, S.; Raue, F.; Becker, W. Radiolabeled peptides for targeting cholecystokinin-b/gastrin receptor-expressing tumors. J. Nucl. Med. 1999, 40, 1029-1044.
106. Behe, M.; Becker, W.; Gotthardt, M.; Angerstein, C.; Behr, T.M. Improved kinetic stability of dtpa-dglu as compared with conventional monofunctional dtpa in chelating indium and yttrium: Preclinical and initial clinical evaluation of radiometal labelled minigastrin derivatives. Eur. J. Nucl. Med. Mol. Imaging 2003, 30, 1140-1146.
107. Behe, M.; Behr, T.M. Cholecystokinin-b (cck-b)/gastrin receptor targeting peptides for staging and therapy of medullary thyroid cancer and other cck-b receptor expressing malignancies. Biopolymers 2002, 66, 399-418.
108. Reubi, J.C.; Waser, B.; Schaer, J.C.; Laederach, U.; Erion, J.; Srinivasan, A.; Schmidt, M.A.; Bugaj, J.E. Unsulfated dtpa-and dota-cck analogs as specific high-affinity ligands for cck-b receptor-expressing human and rat tissues in vitro and in vivo. Eur. J. Nucl. Med. 1998, 25, 481-490.
109. Breeman, W.A.; Froberg, A.C.; de Blois, E.; van Gameren, A.; Melis, M.; de Jong, M.; Maina, T.; Nock, B.A.; Erion, J.L.; Macke, H.R. et al. Optimised labeling, preclinical and initial clinical aspects of cck-2 receptortargeting with 3 radiolabeled peptides. Nucl. Med. Biol. 2008, 35, 839-849.
110. Froberg, A.C.; de Jong, M.; Nock, B.A.; Breeman, W.A.; Erion, J.L.; Maina, T.; Verdijsseldonck, M.; de Herder, W.W.; van der Lugt, A.; Kooij, P.P. et al. Comparison of three radiolabelled peptide analogues for cck-2 receptor scintigraphy in medullary thyroid carcinoma. Eur. J. Nucl. Med. Mol. Imaging 2009, 36, 1265-1272.
111. Good, S.; Walter, M.A.; Waser, B.; Wang, X.; Muller-Brand, J.; Behe, M.P.; Reubi, J.C.; Maecke, H.R. Macrocyclic chelator-coupled gastrin-based radiopharmaceuticals for targeting of gastrin receptorexpressing tumours. Eur. J. Nucl. Med. Mol. Imaging 2008, 35, 1868-1877.
112. Nock, B.A.; Kaloudi, A.; Lymperis, E.; Giarika, A.; Kulkarni, H.R.; Klette, I.; Singh, A.; Krenning, E.P.; de Jong, M.; Maina, T. et al. Theranostic perspectives in prostate cancer with the gastrin-releasing peptide receptor antagonist neobomb1: Preclinical and first clinical results. J. Nucl. Med. 2017, 58, 75-80.
113. Mather, S.J.; McKenzie, A.J.; Sosabowski, J.K.; Morris, T.M.; Ellison, D.; Watson, S.A. Selection of radiolabeled gastrin analogs for peptide receptor-targeted radionuclide therapy. J. Nucl. Med. 2007, 48, 615-622.
114. Von Guggenberg, E.; Rangger, C.; Sosabowski, J.; Laverman, P.; Reubi, J.C.; Virgolini, I.J.; Decristoforo, C. Preclinical evaluation of radiolabeled dota-derivatized cyclic minigastrin analogs for targeting cholecystokinin receptor expressing malignancies. Mol. Imaging Biol. 2012, 14, 366-375.
115. Sosabowski, J.K.; Matzow, T.; Foster, J.M.; Finucane, C.; Ellison, D.; Watson, S.A.; Mather, S.J. Targeting of cck-2 receptor-expressing tumors using a radiolabeled divalent gastrin peptide. J. Nucl. Med. 2009, 50, 2082-2089.
116. Kolenc-Peitl, P.; Mansi, R.; Tamma, M.; Gmeiner-Stopar, T.; Sollner-Dolenc, M.; Waser, B.; Baum, R.P.; Reubi, J.C.; Maecke, H.R. Highly improved metabolic stability and pharmacokinetics of indium-111-dotagastrin conjugates for targeting of the gastrin receptor. J. Med. Chem. 2011, 54, 2602-2609.
117. Kolenc Peitl, P.; Tamma, M.; Kroselj, M.; Braun, F.; Waser, B.; Reubi, J.C.; Sollner Dolenc, M.; Maecke, H.R.; Mansi, R. Stereochemistry of amino acid spacers determines the pharmacokinetics of (111)in-dotaminigastrin analogues for targeting the cck2/gastrin receptor. Bioconjug. Chem. 2015, 26, 1113-1119.
118. Maina, T.; Konijnenberg, M.W.; KolencPeitl, P.; Garnuszek, P.; Nock, B.A.; Kaloudi, A.; Kroselj, M.; Zaletel, K.; Maecke, H.; Mansi, R. et al. Preclinical pharmacokinetics, biodistribution, radiation dosimetry and toxicity studies required for regulatory approval of a phase i clinical trial with (111)in-cp04 in medullary thyroid carcinoma patients. Eur. J. Pharm.Sci. 2016, 91, 236-242.
119. Kroselj, M.; Mansi, R.; Reubi, J.; Maecke, H.; Peitl, P.K. Comparison of dota-coupled minigastrin analogues and corresponding nle congeners. Eur. J. Nucl. Med. Mol. Imaging 2012; 39(Suppl. 1), S533-S534.
120. Aloj, L.; Aurilio, M.; Rinaldi, V.; D'Ambrosio, L.; Tesauro, D.; Peitl, P.K.; Maina, T.; Mansi, R.; von Guggenberg, E.; Joosten, L. et al. Comparison of the binding and internalization properties of 12 dotacoupled and (1)(1)(1)in-labelled cck2/gastrin receptor binding peptides: A collaborative project under cost action bm0607. Eur. J. Nucl. Med. Mol. Imaging 2011, 38, 1417-1425.
121. Laverman, P.; Joosten, L.; Eek, A.; Roosenburg, S.; Peitl, P.K.; Maina, T.; Macke, H.; Aloj, L.; von Guggenberg, E.; Sosabowski, J.K. et al. Comparative biodistribution of 12 (1)(1)(1)in-labelled gastrin/cck2 receptor-targeting peptides. Eur. J. Nucl. Med. Mol. Imaging 2011, 38, 1410-1416.
122. Ocak, M.; Helbok, A.; Rangger, C.; Peitl, P.K.; Nock, B.A.; Morelli, G.; Eek, A.; Sosabowski, J.K.; Breeman, W.A.; Reubi, J.C. et al. Comparison of biological stability and metabolism of cck2 receptor targeting peptides, a collaborative project under cost bm0607. Eur. J. Nucl. Med. Mol. Imaging 2011, 38, 1426-1435.
123. Behe, M.; Kluge, G.; Becker, W.; Gotthardt, M.; Behr, T.M. Use of polyglutamic acids to reduce uptake of radiometal-labeled minigastrin in the kidneys. J. Nucl. Med. 2005, 46, 1012-1015.
124. Konijnenberg, M.; Breeman, W.; de Blois, E.; Chan, H.; Boerman, O.; Laverman, P.; Kolenc-Peitl, P.; Melis, M.; de Jong, M. Therapeutic application of cck2r-targeting pp-f11: Influence of particle range, activity and peptide amount. EJNMMI Res. 2014, 4, 1-15.
125. Roosenburg, S.; Laverman, P.; Joosten, L.; Cooper, M.S.; Kolenc Peitl, P.; Foster, J.; Hudson, C.; Leyton, J.; Burnet, J.; Oyen, W. et al. Pet and spect imaging of a radiolabeled minigastrin analog conjugated with dota, nota and nodaga and labeled with cu, ga and in. Mol. Pharm. 2014,11, 3930-3937.
126. Kunikowska, J.; Ziemnicka, K.; Pawlak, D.; Ruchala, M.; Kolasa, A.; Janicka-Jedynska, M.; Wozniak, A.; Mikolajczak, R.; Krolicki, L. Medullary thyroid carcinoma-Pet/ct imaging with 68ga-labelled gastrin and somatostatin analogues. Endokrynol. Polska 2016, 67, 68-71.
127. Pawlak, D.; Rangger, C.; Kolenc Peitl, P.; Garnuszek, P.; Maurin, M.; Ihli, L.; Kroselj, M.; Maina, T.; Maecke, H.; Erba, P. et al. From preclinical development to clinical application: Kit formulation for radiolabelling the minigastrin analogue cp04 with in-111 for a first-in-human clinical trial. Eur. J. Pharm. Sci. 2016, 85, 1-9.
128. Behr, T.M.; Behe, M.P. Cholecystokinin-b/gastrin receptor-targeting peptides for staging and therapy of medullary thyroid cancer and other cholecystokinin-b receptor-expressing malignancies. Semin. Nucl. Med. 2002, 32, 97-109.
129. Wessels, B.W.; Konijnenberg, M.W.; Dale, R.G.; Breitz, H.B.; Cremonesi, M.; Meredith, R.F.; Green, A.J.; Bouchet, L.G.; Brill, A.B.; Bolch, W.E. et al. Mird pamphlet no. 20: The effect of model assumptions on kidney dosimetry and response-Implications for radionuclide therapy. J. Nucl. Med. 2008, 49, 1884-1899.
130. Mayo, K.E.; Miller, L.J.; Bataille, D.; Dalle, S.; Goke, B.; Thorens, B.; Drucker, D.J. International union of pharmacology. Xxxv. The glucagon receptor family. Pharmacol. Rev. 2003, 55, 167-194.
131. Waser, B.; Rehmann, R.; Sanchez, C.; Fourmy, D.; Reubi, J.C. Glucose-dependent insulinotropic polypeptide receptors in most gastroenteropancreatic and bronchial neuroendocrine tumors. J. Clin. Endocrinol. Metab. 2012, 97, 482-488.
132. Yaqub, T.; Tikhonova, I.G.; Lattig, J.; Magnan, R.; Laval, M.; Escrieut, C.; Boulegue, C.; Hewage, C.; Fourmy, D. Identification of determinants of glucose-dependent insulinotropic polypeptide receptor that interact with n-terminal biologically active region of the natural ligand. Mol. Pharmacol. 2010, 77, 547-558.
133. Gourni, E.; Waser, B.; Clerc, P.; Fourmy, D.; Reubi, J.C.; Maecke, H.R. The glucose-dependent insulinotropic polypeptide receptor: A novel target for neuroendocrine tumor imaging-first preclinical studies. J. Nucl. Med. 2014, 55, 976-982.