In vivo stabilization of a gastrin-releasing peptide receptor antagonist enhances pet imaging and radionuclide therapy of prostate cancer in preclinical studies

Theranostics

Volumn 6, Issue 1, 2016, Pages 104-117

  Chatalic, Kristell L S ^a   Konijnenberg, Mark ^a   Nonnekens, Julie ^a   de Blois, Erik ^a   Hoeben, Sander ^a   de Ridder, Corrina ^a   Brunel, Luc ^b   Fehrentz, Jean Alain ^b   Martinez, Jean ^b   van Gent, Dik C ^a   Nock, Berthold A ^c   Maina, Theodosia ^c   van Weerden, Wytske M ^a   Jong, Marion de ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b INSTITUT CHARLES GERHARDT   (France)

^c INSTITUTE OF NANOSCIENCE AND NANOTECHNOLOGY   (Greece)

Author keywords

Enzyme inhibition; GRPR; Neutral endopeptidase; PET imaging; Phosphoramidon; Prostate cancer; Radionuclide therapy; Theranostics

Indexed keywords

DOUBLE STRANDED DNA; GALLIUM 68 TETRAXETAN BETAALANYL BETAALANYL [HISTIDINYL DEXTRO PHENYL ALANYL GLUTAMINYL TRYPTOPHYL ALANYL VALYL GLYCYL HISTIDINYL LEUCYL AMINE]; LUTETIUM 177 TETRAXETAN BETAALANYL BETAALANYL [HISTIDINYL DEXTRO PHENYL ALANYL GLUTAMINYL TRYPTOPHYL ALANYL VALYL GLYCYL HISTIDINYL LEUCYL AMINE]; PHOSPHORAMIDON; RECEPTOR BLOCKING AGENT; TETRAXETAN BETA ALANINE BETA ALANINE [HISTIDINE DEXTRO PHENYLALANYLGLUTAMYLTRYPTOPHYLALANYLVALYLGLYCYLHISTIDYLSTATINYLLEUCYL AMINE] GA 68; TETRAXETAN BETA ALANINE BETA ALANINE [HISTIDINE DEXTRO PHENYLALANYLGLUTAMYLTRYPTOPHYLALANYLVALYLGLYCYLHISTIDYLSTATINYLLEUCYL AMINE] LU 177; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; BOMBESIN RECEPTOR; RADIOISOTOPE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; DRUG DISTRIBUTION; HUMAN; HUMAN CELL; IN VIVO STUDY; ISOTOPE LABELING; MALE; MOUSE; NONHUMAN; POSITRON EMISSION TOMOGRAPHY; PROSTATE CANCER; SENSITIVITY ANALYSIS; SURVIVAL RATE; TUMOR REGRESSION; TUMOR VOLUME; ANIMAL; ANTAGONISTS AND INHIBITORS; DISEASE MODEL; PROCEDURES; PROSTATIC NEOPLASMS; RADIOTHERAPY;

ANIMALS; ANTINEOPLASTIC AGENTS; DISEASE MODELS, ANIMAL; MALE; MICE; POSITRON-EMISSION TOMOGRAPHY; PROSTATIC NEOPLASMS; RADIOISOTOPES; RADIOTHERAPY; RECEPTORS, BOMBESIN;

EID: 84954547925     PISSN: None     EISSN: 18387640     Source Type: Journal    
DOI: 10.7150/thno.13580     Document Type: Article

References (49)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin. 2012; 62: 10-29.
2. Siegel R, DeSantis C, Virgo K, et al. Cancer treatment and survivorship statistics, 2012. CA Cancer J Clin. 2012; 62: 220-41.
3. Roivainen A, Kahkonen E, Luoto P, et al. Plasma pharmacokinetics, whole-body distribution, metabolism, and radiation dosimetry of 68Ga bombesin antagonist BAY 86-7548 in healthy men. J Nucl Med. 2013; 54: 867-72.
4. Kahkonen E, Jambor I, Kemppainen J, et al. In vivo imaging of prostate cancer using [68Ga]-labeled bombesin analog BAY86-7548. Clin Cancer Res. 2013; 19: 5434-43.
5. Afshar-Oromieh A, Malcher A, Eder M, et al. PET imaging with a [68Ga]gallium-labelled PSMA ligand for the diagnosis of prostate cancer: biodistribution in humans and first evaluation of tumour lesions. Eur J Nucl Med Mol Imaging. 2013; 40: 486-95.
6. Afshar-Oromieh A, Zechmann CM, Malcher A, et al. Comparison of PET imaging with a (68)Ga-labelled PSMA ligand and (18)F-choline-based PET/CT for the diagnosis of recurrent prostate cancer. Eur J Nucl Med Mol Imaging. 2014; 41: 11-20.
7. Tagawa ST, Milowsky MI, Morris M, et al. Phase II study of Lutetium-177-labeled anti-prostate-specific membrane antigen monoclonal antibody J591 for metastatic castration-resistant prostate cancer. Clin Cancer Res. 2013; 19: 5182-91.
8. Vallabhajosula S, Nikolopoulou A, Jhanwar YS, et al. Radioimmunotherapy of Metastatic Prostate Cancer with 177Lu-DOTA-huJ591 Anti Prostate Specific Membrane Antigen Specific Monoclonal Antibody. Curr Radiopharm. 2015; [Epub ahead of print].
9. Ananias HJ, van den Heuvel MC, Helfrich W, et al. Expression of the gastrin-releasing peptide receptor, the prostate stem cell antigen and the prostate-specific membrane antigen in lymph node and bone metastases of prostate cancer. Prostate. 2009; 69: 1101-8.
10. Markwalder R, Reubi JC. Gastrin-releasing peptide receptors in the human prostate: relation to neoplastic transformation. Cancer Res. 1999; 59: 1152-9.
11. Cescato R, Maina T, Nock B, et al. Bombesin receptor antagonists may be preferable to agonists for tumor targeting. J Nucl Med. 2008; 49: 318-26.
12. Basso N, Lezoche E, Speranza V. Studies with bombesin in man. World J Surg. 1979; 3: 579-85.
13. Bodei L, Ferrari M, Nunn A, et al. Lu-177-AMBA Bombesin analogue in hormone refractory prostate cancer patients: A phase I escalation study with single-cycle administrations. Eur J Nucl Med Mol Imaging. 2007; 34: S221-S221.
14. Chatalic KL, Franssen GM, van Weerden WM, et al. Preclinical comparison of Al18F-and 68Ga-labeled gastrin-releasing peptide receptor antagonists for PET imaging of prostate cancer. J Nucl Med. 2014; 55: 2050-6.
15. Shipp MA, Tarr GE, Chen CY, 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: 10662-6.
16. Erdos EG, Skidgel RA. Neutral endopeptidase 24.11 (enkephalinase) and related regulators of peptide hormones. Faseb j. 1989; 3: 145-51.
17. Roques BP, Noble F, Dauge V, et al. Neutral endopeptidase 24.11: structure, inhibition, and experimental and clinical pharmacology. Pharmacol Rev. 1993; 45: 87-146.
18. Nock BA, Maina T, Krenning EP, et al. "To serve and protect": enzyme inhibitors as radiopeptide escorts promote tumor targeting. J Nucl Med. 2014; 55: 121-7.
19. Marsouvanidis PJ, Nock BA, Hajjaj B, et al. Gastrin releasing peptide receptor-directed radioligands based on a bombesin antagonist: synthesis, (111)in-labeling, and preclinical profile. J Med Chem. 2013; 56: 2374-84.
20. Ali M, Hsieh W, Smyth D, et al. A simple and rapid method to quantify (68)Ga-hydroxides in a (68)Ga-DOTATATE formulation. Intern Med J. 2014; 44: 36-7.
21. Bolch WE, Eckerman KF, Sgouros G, et al. MIRD pamphlet No. 21: a generalized schema for radiopharmaceutical dosimetry-standardization of nomenclature. J Nucl Med. 2009; 50: 477-84.
22. Keenan MA, Stabin MG, Segars WP, et al. RADAR realistic animal model series for dose assessment. J Nucl Med. 2010; 51: 471-6.
23. Konijnenberg M, Breeman W, de Blois E, et al. Therapeutic application of CCK2R-targeting PP-F11: influence of particle range, activity and peptide amount. EJNMMI Research. 2014; 4: 1-15.
24. O'Donoghue JA, Bardies M, Wheldon TE. Relationships between tumor size and curability for uniformly targeted therapy with beta-emitting radionuclides. J Nucl Med. 1995; 36: 1902-9.
25. de Visser M, van Weerden WM, de Ridder CM, et al. Androgen-dependent expression of the gastrin-releasing peptide receptor in human prostate tumor xenografts. J Nucl Med. 2007; 48: 88-93.
26. de Blois E, Chan HS, Konijnenberg M, et al. Effectiveness of quenchers to reduce radiolysis of (111)In-or (177)Lu-labelled methionine-containing regulatory peptides. Maintaining radiochemical purity as measured by HPLC. Curr Top Med Chem. 2012; 12: 2677-85.
27. Sancho V, Di Florio A, Moody TW, et al. Bombesin receptor-mediated imaging and cytotoxicity: review and current status. Curr Drug Deliv. 2011; 8: 79-134.
28. Lantry LE, Cappelletti E, Maddalena ME, et al. 177Lu-AMBA: Synthesis and characterization of a selective 177Lu-labeled GRP-R agonist for systemic radiotherapy of prostate cancer. J Nucl Med. 2006; 47: 1144-52.
29. Johnson CV, Shelton T, Smith CJ, et al. Evaluation of combined (177)Lu-DOTA-8-AOC-BBN (7-14)NH(2) GRP receptor-targeted radiotherapy and chemotherapy in PC-3 human prostate tumor cell xenografted SCID mice. Cancer Biother Radiopharm. 2006; 21: 155-66.
30. Wild D, Frischknecht M, Zhang H, et al. Alpha-versus beta-particle radiopeptide therapy in a human prostate cancer model (213Bi-DOTA-PESIN and 213Bi-AMBA versus 177Lu-DOTA-PESIN). Cancer Res. 2011; 71: 1009-18.
31. Ginj M, Zhang H, Waser B, et al. Radiolabeled somatostatin receptor antagonists are preferable to agonists for in vivo peptide receptor targeting of tumors. Proc Natl Acad Sci U S A. 2006; 103: 16436-41.
32. Cescato R, Waser B, Fani M, et al. Evaluation of 177Lu-DOTA-sst2 antagonist versus 177Lu-DOTA-sst2 agonist binding in human cancers in vitro. J Nucl Med. 2011; 52: 1886-90.
33. Wild D, Fani M, Behe M, et al. First clinical evidence that imaging with somatostatin receptor antagonists is feasible. J Nucl Med. 2011; 52: 1412-7.
34. Dumont RA, Tamma M, Braun F, et al. Targeted radiotherapy of prostate cancer with a gastrin-releasing peptide receptor antagonist is effective as monotherapy and in combination with rapamycin. J Nucl Med. 2013; 54: 762-9.
35. Pernot M, Vanderesse R, Frochot C, et al. Stability of peptides and therapeutic success in cancer. Expert Opin Drug Metab Toxicol. 2011; 7: 793-802.
36. Adessi C, Soto C. Converting a peptide into a drug: strategies to improve stability and bioavailability. Curr Med Chem. 2002; 9: 963-78.
37. Vlieghe P, Lisowski V, Martinez J, et al. Synthetic therapeutic peptides: science and market. Drug Discov Today. 2010; 15: 40-56.
38. Shipp MA, Richardson NE, Sayre PH, et al. Molecular cloning of the common acute lymphoblastic leukemia antigen (CALLA) identifies a type II integral membrane protein. Proc Natl Acad Sci U S A. 1988; 85: 4819-23.
39. Erdos EG, Schulz WW, Gafford JT, et al. Neutral metalloendopeptidase in human male genital tract. Comparison to angiotensin I-converting enzyme. Lab Invest. 1985; 52: 437-47.
40. Sato Y, Itoh F, Hinoda Y, et al. Expression of CD10/neutral endopeptidase in normal and malignant tissues of the human stomach and colon. J Gastroenterol. 1996; 31: 12-7.
41. Oefner C, D'Arcy A, Hennig M, et al. Structure of human neutral endopeptidase (Neprilysin) complexed with phosphoramidon. J Mol Biol. 2000; 296: 341-9.
42. Marsouvanidis PJ, Melis M, de Blois E, et al. In vivo enzyme inhibition improves the targeting of [177Lu]DOTA-GRP(13-27) in GRPR-positive tumors in mice. Cancer Biother Radiopharm. 2014; 29: 359-67.
43. Osman I, Dai J, Mikhail M, et al. Loss of neutral endopeptidase and activation of protein kinase B (Akt) is associated with prostate cancer progression. Cancer. 2006; 107: 2628-36.
44. Albrecht M, Doroszewicz J, Gillen S, et al. Proliferation of prostate cancer cells and activity of neutral endopeptidase is regulated by bombesin and IL-1beta with IL-1beta acting as a modulator of cellular differentiation. Prostate. 2004; 58: 82-94.
45. Dawson LA, Maitland NJ, Turner AJ, et al. Stromal-epithelial interactions influence prostate cancer cell invasion by altering the balance of metallopeptidase expression. Br J Cancer. 2004; 90: 1577-82.
46. Usmani BA, Harden B, Maitland NJ, et al. Differential expression of neutral endopeptidase-24.11 (neprilysin) and endothelin-converting enzyme in human prostate cancer cell lines. Clin Sci (Lond). 2002; 103 Suppl 48: 314s-7s.
47. Ho ME, Quek SI, True LD, et al. Prostate cancer cell phenotypes based on AGR2 and CD10 expression. Mod Pathol. 2013; 26: 849-59.
48. van Gent DC, van der Burg M. Non-homologous end-joining, a sticky affair. Oncogene. 2007; 26: 7731-40.
49. Dalm SU, Martens JW, Sieuwerts AM, et al. In vitro and in vivo application of radiolabeled gastrin-releasing Peptide receptor ligands in breast cancer. J Nucl Med. 2015; 56: 752-7.