New enzyme-activated solubility-switchable contrast agent for magnetic resonance imaging: From synthesis to in vivo imaging

Journal of Medicinal Chemistry

Volumn 52, Issue 6, 2009, Pages 1576-1581

  Jastrzebska, Beata ^a,b   Lebel, Réjean ^a,b   Therriault, Hélène ^b   McIntyre, J Oliver ^c   Escher, Emanuel ^b   Guérin, Brigitte ^a,b   Paquette, Benoit ^b   Neugebauer, Witold A ^b   Lepage, Martin ^a,b  

^a UNIVERSITY OF SHERBROOKE   (Canada)

^b UNIVERSITÉ DE SHERBROOKE   (Canada)

^c VANDERBILT INGRAM CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GADOLINIUM PENTETATE; GADOTERIC ACID; GELATINASE A; MACROGOL; PROTEINASE;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTRAST ENHANCEMENT; CONTROLLED STUDY; DRUG SOLUBILITY; DRUG SYNTHESIS; ENZYME ACTIVATION; EXPERIMENTAL MODEL; HYDROPHOBICITY; IN VIVO STUDY; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING;

ANIMALS; CONTRAST MEDIA; HETEROCYCLIC COMPOUNDS; MAGNETIC RESONANCE IMAGING; MATRIX METALLOPROTEINASE 2; MICE; NEOPLASMS, EXPERIMENTAL; ORGANOMETALLIC COMPOUNDS; SOLUBILITY; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 64349083804     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm801411h     Document Type: Article

References (51)

1. Liotta, L. A.; Tryggvason, K.; Garbisa, S.; Hart, I.; Foltz, C. M.; Shafie, S. Metastatic potential correlates with enzymatic degradation of basement membrane collagen. Nature 1980, 284, 67-68.
2. Urbanski, S. J.; Edwards, D. R.; Maitland, A.; Leco, K. J.; Watson, A.; Kossakowska, A. E. Expression of metalloproteinases and their inhibitors in primary pulmonary carcinomas. Br. J. Cancer 1992, 66, 1188-1194.
3. Remacle, A. G.; Noël, A.; Duggan, C.; McDermott, E.; O'Higgins, N.; Foidart, J. M.; Duffy, M. Assay of matrix metalloproteinases types 1, 2, 3, and in breast cancer. Br. J. Cancer 1998, 77, 926-931.
4. Basset, P.; Bellocq, J. P.; Wolf, C.; Stoll, I.; Hutin, P.; Limacher, J. M.; Podhajcer, O. L.; Chenard, M. P.; Rio, M. C.; Chambon, P. A novel metalloproteinase gene specifically expressed in stromal cells of breast carcinomas. Nature 1990, 348, 699-704.
5. Parsons, S. L.; Watson, S. A.; Collins, H. M.; Griffin, N. R.; Clarke, P. A.; Steele, R. J. C. Gelatinase (MMP-2 and -9) expression in gastrointestinal malignancy. Br. J. Cancer 1998, 78, 1495-1502.
6. r 72,000) expression in human prostate: Bening and malignant tissue. Cancer Res. 1993, 53, 878-883.
7. MacDougall, J. R.; Bani, M. R.; Lin, Y.; Rak, J.; Kerbel, R. S. The 92-kDa gelatinase B is expressed by advanced stage melanoma cells: suppression by somatic cell hybridization with early stage melanoma cell. Cancer Res. 1995, 55, 4174-4181.
8. Gerhards, S.; Jung, K.; Koenig, F.; Daniltchenko, D.; Hauptmann, S.; Schnorr, D.; Loening, S. A. Excretion of matrix metalloproteinases 2 and 9 in urine is associated with a high stage and grade of bladder carcinoma. Urology 2001, 57, 675-679.
9. Schmalfeldt, B.; Prechtel, D.; Harting, K.; Spathe, K.; Rutke, S.; Konik, E.; Fridman, R.; Berger, U.; Schmitt, M.; Kuhn, W.; Lengyel, E. Increased expression of matrix metalloproteinases (MMP)-2, MMP-9, and the urokinase-type plasminogen activator is associated with progression from benign to advanced ovarian cancer. Clin. Cancer Res. 2001, 7, 2396-2404.
10. Koshiba, T.; Hosotani, R.; Wada, M.; Fujimoto, K.; Lee, J.; Doi, R.; Arii, S.; Imamura, M. Detection of matrix metalloproteinase activity in human pancreatic cancer. Surg. Today 1997, 27, 302-304.
11. Langers, A. M. J.; Sier, C. F. M.; Hawinkels, L. J. A. C.; Kubben, F. J. G. M.; van Duijn, W.; van der Reijden, J. J.; Lamers, C. B. H. W.; Hommes, D. W.; Verspaget, H. W. MMP-2 geno-phenotype is prognostic for colorectal cancer survival, whereas MMP-9 is not. Br. J. Cancer 2008, 98, 1820-1823.
12. Kusukawa, J.; Sasaquri, Y.; Shima, I.; Kameyama, T.; Morimatsu, M. Expression of matrix metalloproteinase-2 releated to lymph node metastasis of oral squamous cell carcinoma. A clinicopathologic study. Am. J. Clin. Pathol. 1993, 99, 18-23.
13. Sato, H.; Takino, T.; Okada, Y.; Cao, J.; Shinagawa, A.; Yamamoto, E.; Selki, M. A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature 1994, 370, 61-65.
14. Gilles, C.; Bassuk, J. A.; Pulyaeva, J.; Sage, E. H.; Foidart, J. M.; Thompson, E. W. SPARC/osteonectin induces matrix metalloprotein-ase-2 activation in human breast cancer cell lines. Cancer Res. 1998, 58, 5529-5536.
15. Jones, J. L.; Glynn, P.; Walker, R. A. Expression of MMP-2 and MMP-9, their inhibitors and the activator MT1-MMP in primary breast carcinomas. J. Pathol. 1999, 789, 161-168.
16. Overall, C. M.; Kleifeld, O. Validating matrix metalloproteinases as drug targets and anti-targets for cancer therapy. Nat. Rev. Cancer. 2006, 6, 227-239.
17. Bellin, M. F.; Vasile, M.; Morel-Precetti, S. Currently used non-specific extracellular MR contrast media. Eur. Radiol. 2003, 73, 2688-2698.
18. Moats, R. A.; Fraser, S. E.; Meade, T. J. A "smart" magnetic resonance imaging agent that reports on specific enzymatic activity. Angew. Chem., Int. Ed. Engl. 1997, 36, 726-728.
19. Louie, A. Y.; Hüber, M. M.; Ahrens, E. T.; Rothbächer, U.; Moats, R.; Jacobs, R. E.; Fraser, S. E.; Meade, T. J. In vivo visualization of gene expression using magnetic resonance imaging. Nat. Biotechnol. 2000, 18, 321-325.
20. Armitage, F. E.; Richardson, D. E.; Li, K. C. P. Polymeric contrast agent for magnetic resonance imaging: synthesis and characterization of gadolinium diethylenetriaminepentaacetic acid conjugated to polysac- charides. Bioconiueate Chem. 1990, 1, 365-374.
21. André, J. P.; Geraldes, C. F. G. C.; Martins, J. A.; Merbach, A. E.; Prata, M. I. M.; Santos, A. C.; de Lima, J. J. P.; Tóth, É. Lanthanide(III) complexes of DOTA-glycoconjugates: a potential new class of lectin- mediated medical imaging agents. Chem.-Eur. J. 2004, 70, 5804-5816.
22. Weissleder, R.; Bogdanov, A.; Tung, C. H.; Weinmann, H. J. Size optimization of synthetic graft copolymers for in vivo angiogenesis imaging. Bioconiueate Chem. 2001, 12, 213-219.
23. Lu, Z. R.; Wang, X. H.; Parker, D. L.; Goodrich, K. C.; Buswell, H. R. Poly(L-glutamic acid) Gd(III)-DOTA conjugate with a degrad-able spacer for magnetic resonance imaging. Bioconiugate Chem. 2003, 14, 715-719.
24. Lee, H. Y.; Jee, H. W.; Seo, S. M.; Kwak, B. K.; Khang, G.; Cho, S. H. Diethylenetriaminepentaacetic acid-gadolinium (DTPA-Gd)-conjugated polysuccinimide derivatives as magnetic resonance imaging contrast agents. Bioconiugate Chem. 2006, 17, 700-706.
25. Wiener, E. C.; Brechbiel, M. W.; Brothers, H.; Magin, R. L.; Gansow, O. A.; Tomalia, D. A.; Lauterbur, P. C. Dendrimer-based metal chelates, a new class of magnetic resonance imaging contrast agents. Maen. Reson. Med. 1994, 31, 1-8.
26. Wiener, E. C.; Konda, S.; Shadron, A.; Brechbiel, M.; Gansow, O. Targeting dendrimer-chelates to tumors and tumor cells expressing the high-affinity folate receptor. Invest. Radiol. 1997, 32, 748-754.
27. Kobayashi, H.; Kawamoto, S.; Saga, T.; Sato, N.; Hiraga, A.; Ishimori, T.; Konishi, J.; Togashi, K.; Brechbiel, M. W. Positive effects of polyethylene glycol conjugation to generation-4 polyamidoamine dendrimers as macromolecular MR contrast agents. Magn. Reson. Med. 2001, 46, 781-788.
28. Kobayashi, H.; Kawamoto, S.; Star, R. A.; Waldmann, T. A.; Tagaya, Y.; Brechbiel, M. W. Micro-magnetic resonance lymphangiography in mice using a novel dendrimer-based magnetic resonance imaging contrast agent. Cancer Res. 2003, 63, 271-276.
29. Schmiedl, U.; Ogan, M.; Paajanen, H.; Marotti, M.; Crooks, L. E.; Brito, A. C.; Brasch, R. C. Albumin labeled with Gd-DTPA as an intravascular, blood pool-enhancing agent for MR imaging: biodis- tribution and imaging studies. Radiology 1987, 162, 205-210.
30. Geninatti Crich, S.; Cabella, C.; Barge, A.; Belfiore, S.; Ghirelli, C.; Lattuada, L.; Lanzardo, S.; Mortillaro, A.; Tei, L.; Visigalli, M.; Forni, G.; Aime, S. In vitro and in vivo magnetic resonance detection of tumor cells by targeting glutamine transporters with Gd-based probes. J. Med. Chem. 2006, 49, 4926-4936.
31. Dirksen, A.; Langereis, S.; de Waal, B. F. M.; van Genderen, M. H. P.; Meijer, E. W.; de Lussanet, Q. G.; Hackeng, T. M. Design and synthesis of a bimodal target-specific contrast agent for angiogenesis. Org. Lett. 2004, 6, 4857-4860.
32. Bull, S. R.; Guler, M. O.; Bras, R. E.; Meade, T. J.; Stupp, S. I. Self-assembled peptide amphiphile nanofibers conjugated to MRI contrast agents. Nano Lett. 2005, 5, 1-4.
33. Lepage, M.; Dow, W. C.; Melchior, M.; You, Y.; Fingleton, B.; Quarles, C. C.; Pépin, C.; Gore, J. C.; Matrisian, L. M.; McIntyre, J. O. Non-invasive detection of matrix metalloproteinase activity in vivo using a novel MRI contrast agent with a solubility switch. Mol. Imaging 2007, 6, 393-403.
34. Chen, E. I.; Kridel, S. J.; Howard, E. W.; Li, W.; Godzik, A.; Smith, J. W. A unique substrate recognition profile for matrix metallopro-teinase-2. J. Biol. Chem. 2002, 277, 4485-4491.
35. Loncin, M. F.; Desreux, J. F.; Merciny, E. Coordination of lanthanides by 2 polyamino polycarboxylic macrocycles: formation of highly stable lanthanide complexes. Inorg. Chem. 1986, 25, 2646-2648.
36. Aime, S.; Botta, M.; Fasano, M.; Terreno, E. Lanthanide(III) chelates for NMR biomedical applications. Chem. Soc. Rev. 1998, 27, 19-29.
37. DeNardo, S. J.; Yao, Z. S.; Lam, K. S.; Song, A. M.; Burke, P. A.; Mirick, G. R.; Lamborn, K. R.; O'Donnel, L. R. T.; DeNardo, G. L. Effect of molecular size of pegylated peptide on the pharmacokinetics and tumor targeting in lymphoma-bearing mice. Clin. Cancer Res. 2003, 9, 3854s-3864s.
38. Hershfield, M. PEG-ADA replacement therapy for adenosine deaminase deficiency: an update after 8.5 years. Clin. Immunol. Immuno-pathol. 1995, 76, S228-S232.
39. Abuchowski, A.; McCoy, J. R.; Palczuk, N. C.; van Es, T.; Davis, F. F. Effect of covalent attachment of polyethylene glycol on immunogenicity and circulating life of bovine liver catalase. J. Biol. Chem. 1977, 252, 3582-3587.
40. Bukowski, R. M.; Tendler, C.; Cutler, D.; Rose, E.; Laughlin, M. M.; Statkevich, P. Treating cancer with PEG intron. Pharmacokinetic profile and dosing guidelines for an improved interferon-alpha-2b formulation. Cancer 2002, 95, 389-396.
41. Wilkinson, J.; Jackson, C. J. C.; Lang, G. M.; Holford-Strevens, V.; Sehon, A. H. Tolerance induction in mice by conjugates of monoclonal immunoglobulins and monomethoxypolyethylene glycol. Transfer of tolerance by T-cells and by T-cells extracts. J. Immunol. 1987, 139, 326-331.
42. Tsutsumi, Y.; Onda, M.; Nagata, S.; Lee, B.; Kreitman, R. J.; Pastan, I. Site-specific chemical modification with polyethylene glycol of recombinant immunotoxin anti-Tac(Fv)-PE38 (LMB-2) improves antitumor activity and reduces animal toxicity and immunogenicity. Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 8548-8553.
43. Schottelius, M.; Schwaiger, M.; Wester, H.-J. Rapid and high-yield solution-phase synthesis of DOTA-Tyr3-octreotide and DOTA-Tyr3- octreotate using unprotected DOTA. Tetrahedron Lett. 2003, 44, 2393-2396.
44. 3]bombesin in human prostate adenocarcinoma xenografts. J. Nucl. Med. 2004, 45, 1390-1397.
45. Woessner, J. F.; Nagase, H. Matrix Metalloproteinases and TIMPs; Oxford University Press: Oxford, U.K., 2000.
46. Molinspiration Cheminformatics Calculation of Molecular Properties and Drug-likeness. http://www.molinspiration.com (accessed April 2008).
47. Lebel, R.; Jastrzȩbska, B.; Therriault, H.; Cournoyer, M.-M.; McIntyre, J. O.; Neugebauer, W.; Escher, E.; Paquette, B.; Lepage, M. Novel solubility-switchable MRI agent allows the noninvasive detection of matrix metalloproteinase-2 activity activity in vivo in a mouse model. Magn. Reson. Med. 2008, 60, 1056-1065.
48. Kaiser, E.; Colescott, R. L.; Bossinger, C. D.; Cook, P. I. Color test for detection of free terminal amino groups in the solid-phase synthesis of peptides. Anal. Biochem. 1970, 34, 595-598.
49. Udenfriend, S.; Stein, S.; Böhlen, P.; Dairman, W.; Leimgruber, W.; Weigele, M. Fluorescamine: a reagent for assay of amino acids, peptides, proteins, and primary amines in the picomole range. Science 1972, 178, 871-872.
50. Lauer-Fields, J. L.; Sritharan, T.; Stack, M. S.; Nagase, H.; Fields, G. B. Selective hydrolysis of triple-helical substrates by matrix metalloproteinase-2 and -9. J. Biol. Chem. 2003, 278, 18140-18145.
51. Fields, G. B.; Van Wart, H. E.; Birkedal-Hansen, H. Sequence specificity of human skin fibroblast collagenase. Evidence for the role of collagen structure in determining the collagenase cleavage site. J. Biol. Chem. 1987, 262, 6221-6226.