Nuclear Medicine and Biology
Volume 37, Issue 3 , Pages 277-288 , April 2010

Synthesis and evaluation of a technetium-99m labeled cytotoxic bombesin peptide conjugate for targeting bombesin receptor-expressing tumors

Received 15 September 2009 ,Revised 9 December 2009 ,Accepted 16 December 2009.

References 

  1. Anastasi A, Erspamer V, Bucci M. Isolation and structure of bombesin and alytesin, two analogous active peptides from the skin of the European amphibians Bombina and Alytes. Experientia. 1971;27:166–167
  2. Breeman WA, de Jong M, Erion JL, Bugaj JE, Srinivasan A, Bernard BF, et al. Preclinical comparison of 111In-labeled DTPA- or DOTA-bombesin analogs for receptor targeted scintigraphy and radionuclide therapy. J Nucl Med. 2002;43:1650–1656
  3. Shipp MA, Tarr GE, Chen CY, Switzer SN, Hersh LB, Stein H, et al. CD10/neutral endopeptidase 24.11 hydrolyzes bombesin-like peptides and regulates the growth of small cell carcinomas of the lung. Proc Natl Acad Sci U S A. 1991;88:10662–10666
  4. Faintuch BL, Teodoro R, Duatti A, Muramoto E, Faintuch S, Smith CJ. Radiolabeled bombesin analogs for prostate cancer diagnosis: preclinical studies. Nucl Med Biol. 2008;35:401–411
  5. Cai RZ, Reile H, Armatis P, Schally AV. Potent bombesin antagonists with C-terminal Leu-ψ(CH2-N)-Tac-NH2 or its derivatives. Proc Natl Acad Sci U S A. 1994;91:12664–12668
  6. Nakagawa T, Hocart SJ, Schumann M, Tapia JA, Mantey SA, Coy DH, et al. Identification of key amino acids in the gastrin-releasing peptide receptor (GRPR) responsible for high affinity binding of gastrin-releasing peptide (GRP). Biochem Pharmacol. 2005;69:579–593
  7. Parry JJ, Kelly TS, Andrews R, Rogers BE. In vitro and in vivo evaluation of 64Cu-labeled DOTA-linker-bombesin(7–14) analogues containing different amino acid linker moieties. Bioconjug Chem. 2007;18:1110–1117
  8. Smith CJ, Volkert WA, Hoffman TJ. Radiolabeled peptide conjugates for targeting of the bombesin receptor superfamily subtypes. Nucl Med Biol. 2005;32:733–740
  9. Fleischmann A, Waser B, Gebbers JO, Reubi JC. Gastrin-releasing peptide receptors in normal and neoplastic human uterus: involvement of multiple tissue compartments. J Clin Endocrinol Metab. 2005;90:4722–4729
  10. Fleischmann A, Läderach U, Friess H, Buechler MW, Reubi JC. Bombesin receptors in distinct tissue compartments of human pancreatic diseases. Lab Invest. 2000;80:1807–1817
  11. Reubi JC, Wenger S, Schmuckli-Maurer J, Schaer JC, Gugger M. Bombesin receptor subtypes in human cancers: detection with the universal radioligand 125I-[D-TYR6-β-ALA11, PHE13, NLE14] bombesin(6-14). Clin Cancer Res. 2002;8:1139–1146
  12. Garrison JC, Rold TL, Sieckman GL, Naz F, Sublett SV, Figueroa SD, et al. Evaluation of the pharmacokinetic effects of various linking group using the 111In-DOTA-X-BBN(7–14)NH2 structural paradigm in a prostate cancer model. Bioconjug Chem. 2008;19:1803–1812
  13. Zhang H, Chen J, Waldherr C, Hinni K, Waser B. Synthesis and evaluation of bombesin derivatives on the basis of pan-bombesin peptides with indium-111, leutetium-177, and yttrium-90 for targeting bombesin receptor-expressing tumors. Cancer Res. 2004;64:6707–6715
  14. Okarvi SM. Peptide-based radiopharmaceuticals and cytotoxic conjugates: potential tools against cancer. Cancer Treat Rev. 2008;34:13–26
  15. Schally AV, Nagy A. New approaches to treatment of various cancers based on cytotoxic analogs of LHRH, somatostatin and bombesin. Life Sci. 2003;72:2305–2320
  16. Schally AV, Nagy A. Cancer chemotherapy based on targeting of cytotoxic peptide conjugates to their receptors on tumors. Eur J Endocrinol. 1999;141:1–14
  17. Nagy A, Armatis P, Cai RZ, Szepeshazi K, Halmos G, Schally AV. Design, synthesis, and in vitro evaluation of cytotoxic analogs of bombesin-like peptides containing doxorubicin or its intensely potent derivative, 2-pyrrolinodoxorubicin. Proc Natl Acad Sci U S A. 1997;94:652–656
  18. Lantry LE, Cappelletti E, Maddalena ME, Fox JS, Feng W, Chen J, et al. Nunn A D. 177Lu-AMBA: synthesis and characterization of a selective 177Lu-labeled GRP-R agonist for systemic radiotherapy of prostate cancer. J Nucl Med. 2006;47:1144–1152
  19. Mantey SA, Weber HC, Sainz E, Akeson M, Ryant RR, Pradhan TK, et al. Discovery of a high affinity radioligand for the human orphan receptor, bombesin receptor subtype 3, which demonstrates that it has a unique pharmacology compared with other mammalian bombesin receptors. J Biol Chem. 1997;272:26062–26071
  20. Pradhan TK, Katsuno T, Taylor JE, Kim SH, Ryan RR, Mantey SA, et al. Identification of a unique ligand which has high affinity for all four bombesin receptor subtypes. Eur J Pharmacol. 1998;343:275–287
  21. Nagy A, Szoke B, Schally AV. Selective coupling of methotrexate to peptide hormone carriers through a γ-carboxamide linkage of its glutamic acid moiety: benzotriazol-1-yloxytris(dimethylamino)phosphonium hexafluorophosphate activation in salt coupling. Proc Natl Acad Sci. 1993;90:6373–6376
  22. Bertino JR. Ode to methotrexate. J Clin Oncol. 1993;11:5–14
  23. Ilgan S, Yang DJ, Higuchi T, Zareneyrizi F, Kim EE, Podoloff DA. Imaging tumor folate receptors using 111In-DTPA-methotrexate. Cancer Biother Radiopharm. 1998;13:177–184
  24. Reubi JC, Mäcke HR, Krenning EP. Candidates for peptide receptor radiotherapy today and in the future. J Nucl Med. 2005;46:67S–75S
  25. Grant GA. Synthetic peptides. New York: Oxford University Press; 2002;
  26. Okarvi SM. Synthesis, radiolabeling and in vitro and in vivo characterization of a technetium-99m-labeled alpha-M2 peptide as a tumor imaging agent. J Peptide Res. 2004;63:460–468
  27. Stalteri MA, Bansal S, Hider R, Mather SJ. Comparison of the stability of technetium-labeled peptides to challenge with cysteine. Bioconjug Chem. 1999;10:130–136
  28. Eisenwiener KP, Prata MIM, Buschmann I, Zhang HW, Santos AC, Wenger S, et al. a new chelator-coupled somatostatin analogue labeled with [67/68Ga] and [111In] for SPECT, PET, and targeted therapeutic applications of somatostatin receptor (hsst2) expressing tumors. Bioconjug Chem. 2002;13:530–541
  29. Okarvi SM, Jammaz IA. Preparation and in vitro and in vivo evaluation of technetium-99-labeled folate and methotrexate conjugates as tumor imaging agents. Cancer Biother Radiopharm. 2006;21:49–60
  30. Nakao R, Furutsuka K, Yamaguchi M, Suzuki K. Development and validation of a liquid chromatographic method for the analysis of positron emission tomography radiopharmaceuticals with Ru(bpy)32+-KMnO4. Anal Sci. 2007;23:151–155
  31. Nakao R, Furutsuka K, Yamaguchi M, Suzuki K. Sensitive determination of specific radioactivity of positron emission tomography radiopharmaceuticals by radio high-performance liquid chromatography with fluorescence detection. Nucl Med Biol. 2008;35:733–740
  32. Lundquist P, Wilking H, Höglund AU, Sandell J, Bergström M, Hartvig P, et al. Potential of [11C]DASB for measuring endogenous serotonin with PET: binding studies. Nucl Med Biol. 2005;32:129–136
  33. Siegrist W, Solca F, Stutz S, Giuffre L, Carrel S, Girard J, et al. Characterization of receptors for α-melanocyte-stimulating hormone on human melanoma cells. Cancer Res. 1989;49:6352–6358
  34. Guide for the Care and Use of Laboratory Animals. Washington, DC: National Academy Press; 1996;
  35. Mather SJ, Ellison D, Bard DS. In: Technetium-99m labelled hybrid receptor-binding peptides. Technetium and rhenium in chemistry and nuclear medicine. Padova (Italy): SG Editoriali; 1995;p. 491–497
  36. Lister-James J, McBride WJ, Buttram S, Civitello ER, Martel LJ, Pearson DA, et al. In: Technetium-99m chelate-containing receptor-binding peptides. Technetium and rhenium in chemistry and nuclear medicine. Padova (Italy): SG Editoriali; 1995;p. 269–274
  37. Yang YS, Zhang X, Xiong Z, Chen X. Comparative in vitro and in vivo evaluation of two 64Cu-labeled bombesin analogs in a mouse model of human prostate adenocarcinoma. Nucl Med Biol. 2006;33:371–380
  38. Hoffman TJ, Smith CJ. True radiotracers: Cu-64 targeting vectors based upon bombesin peptide. Nucl Med Biol. 2009;36:579–585
  39. Halmos G, Wittliff JL, Schally AV. Characterization of bombesin/gastrin-releasing peptide receptors in human breast cancer and their relationship to steroid receptor expression. Cancer Res. 1995;55:280–287
  40. Giacchetti S, Gauvillé C, De Crémoux P, Bertin L, Berthon P, Abita JP, et al. Characterization, in some human breast cancer cell lines, of gastrin-releasing peptide-like receptors which are absent in normal breast epithelial cells. Int J Cancer. 1990;46:293–298
  41. Reile H, Armatis PE, Schally AV. Characterization of high-affinity receptors for bombesin/gastrin releasing peptide on the human prostate cancer cell lines PC-3 and DU-145: internalization of receptor bound 125I-(Tyr4) bombesin by tumor cells. Prostate. 1994;25:29–38
  42. Horne DW, Reed KA. Transport of methotrexate into PC-3 human prostate cancer cells. Arch Biochem Biophys. 2001;394:39–44
  43. Deutsch JC, Elwood PC, Portillo RM, Macey MG, Kolhouse JF. Role of the membrane-associated folate binding protein (folate receptor) in methotrexate transport by human KB cells. Arch Biochem Biophys. 1989;274:327–337
  44. Hoffman TJ, Gali H, Smith CJ, Sieckman GL, Hayes DL, Owen NK, et al. Novel series of 111In-labeled bombesin analogs as potential radiopharmaceuticals for specific targeting of gastrin-releasing peptide receptors expressed on human prostate cancer cells. J Nucl Med. 2003;44:823–831
  45. De Jong M, Krenning EP. Molecular imaging and therapy of cancer using radiolabelled peptides. EJHP. 2005;01:20–21
  46. Rolleman EJ, Valkema R, de Jong M, Kooij PPM, Krenning EP. Safe and effective inhibition of renal uptake of radiolabelled octreotide by a combination of lysine and arginine. Eur J Nucl Med. 2003;30:9–15

PII: S0969-8051(09)00296-0

doi: 10.1016/j.nucmedbio.2009.12.006

Nuclear Medicine and Biology
Volume 37, Issue 3 , Pages 277-288 , April 2010