Pre-Assembly of Near-Infrared Fluorescent Multivalent Molecular Probes for Biological Imaging

Bioconjugate Chemistry

Volumn 27, Issue 5, 2016, Pages 1400-1410

  Peck, Evan M ^a   Battles, Paul M ^a   Rice, Douglas R ^a   Roland, Felicia M ^a   Norquest, Kathryn A ^a   Smith, Bradley D ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; BONE; CHEMICAL STABILITY; ELECTROPHORESIS; ENERGY TRANSFER; FLUORESCENCE IMAGING; FLUORESCENCE MICROSCOPY; INFRARED DEVICES; LIGANDS; MOLECULAR IMAGING;

ASSEMBLY PROCESS; BINDING PROPERTIES; BIOLOGICAL IMAGING; IMINODIACETATE; MACROCYCLES; MODULAR ASSEMBLY; MOLECULAR PROBES; MULTIVALENT BINDING; NEAR-INFRARED FLUORESCENT; TUNABLES;

PROBES;

CARBOXYLIC ACID; DIGLYCINE; FLUORESCENT DYE; MACROCYCLIC COMPOUND; TRIETHYLENE GLYCOL; MACROGOL DERIVATIVE;

ABSORPTION SPECTROSCOPY; AGAR GEL ELECTROPHORESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASSOCIATION CONSTANT; CONTROLLED STUDY; CYCLOADDITION; ENERGY TRANSFER; EX VIVO STUDY; FLUORESCENCE IMAGING; FLUORESCENCE MICROSCOPY; FLUORESCENCE SPECTROSCOPY; GEL ELECTROPHORESIS; IN VIVO STUDY; LIVER MICROSOME; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; METABOLIC STABILITY; MOLECULAR IMAGING; MOLECULAR PROBE; MOUSE; NONHUMAN; PROTON NUCLEAR MAGNETIC RESONANCE; QUANTUM YIELD; RAT; ANIMAL; BONE; CHEMISTRY; CHO CELL LINE; CONFORMATION; CRICETULUS; DIAGNOSTIC IMAGING; INFRARED RADIATION; KINETICS; MATERIALS TESTING; MOLECULAR MODEL;

ANIMALS; BONE AND BONES; CHO CELLS; CRICETULUS; FLUORESCENT DYES; INFRARED RAYS; KINETICS; MACROCYCLIC COMPOUNDS; MATERIALS TESTING; MICE; MODELS, MOLECULAR; MOLECULAR CONFORMATION; POLYETHYLENE GLYCOLS;

EID: 84971287315     PISSN: 10431802     EISSN: 15204812     Source Type: Journal    
DOI: 10.1021/acs.bioconjchem.6b00173     Document Type: Article

References (63)

1. Srinivasarao, M., Galliford, C. V., and Low, P. S. (2015) Principles in the design of ligand-targeted cancer therapeutics and imaging agents Nat. Rev. Drug Discovery 14, 203-19 10.1038/nrd4519
2. Sim, N. and Parker, D. (2015) Critical design issues in the targeted molecular imaging of cell surface receptors Chem. Soc. Rev. 44, 2122-34 10.1039/C4CS00364K
3. Warram, J. M., de Boer, E., Sorace, A. G., Chung, T. K., Kim, H., Pleijhuis, R. G., van Dam, G. M., and Rosenthal, E. L. (2014) Antibody-based imaging strategies for cancer Cancer Metastasis Rev. 33, 809-22 10.1007/s10555-014-9505-5
4. Xu, S., Olenyuk, B. Z., Okamoto, C. T., and Hamm-Alvarez, S. F. (2013) Targeting receptor-mediated endocytotic pathways with nanoparticles: rationale and advances Adv. Drug Delivery Rev. 65, 121-38 10.1016/j.addr.2012.09.041
5. Kiessling, L. L., Gestwicki, J. E., and Strong, L. E. (2000) Synthetic multivalent ligands in the exploration of cell-surface interactions Curr. Opin. Chem. Biol. 4, 696-703 10.1016/S1367-5931(00)00153-8
6. Hlavacek, W. S., Percus, J. K., Percus, O. E., Perelson, A. S., and Wofsy, C. (2002) Retention of antigen on follicular dendritic cells and B lymphocytes through complement-mediated multivalent ligand-receptor interactions: theory and application to HIV treatment Math. Biosci. 176, 185-202 10.1016/S0025-5564(02)00091-3
7. Kitov, P. I. and Bundle, D. R. (2003) On the nature of the multivalency effect: a thermodynamic model J. Am. Chem. Soc. 125, 16271-84 10.1021/ja038223n
8. Vauquelin, G. and Charlton, S. J. (2013) Exploring avidity: understanding the potential gains in functional affinity and target residence time of bivalent and heterobivalent ligands Br. J. Pharmacol. 168, 1771-85 10.1111/bph.12106
9. Fischer, G., Lindner, S., Litau, S., Schirrmacher, R., Wangler, B., and Wangler, C. (2015) Next step toward optimization of GRP receptor avidities: determination of the minimal distance between BBN(7-14) units in peptide homodimers Bioconjugate Chem. 26, 1479-83 10.1021/acs.bioconjchem.5b00362
10. Guo, Z., He, B., Jin, H., Zhang, H., Dai, W., Zhang, L., Zhang, H., Wang, X., Wang, J., and Zhang, X. et al. 2014, Targeting efficiency of RGD-modified nanocarriers with different ligand intervals in response to integrin alphavbeta3 clustering Biomaterials 35, 6106-17 10.1016/j.biomaterials.2014.04.031
11. Hennig, R., Pollinger, K., Veser, A., Breunig, M., and Goepferich, A. (2014) Nanoparticle multivalency counterbalances the ligand affinity loss upon PEGylation J. Controlled Release 194, 20-7 10.1016/j.jconrel.2014.07.062
12. Lundquist, J. J. and Toone, E. J. (2002) The cluster glycoside effect Chem. Rev. 102, 555-78 10.1021/cr000418f
13. Care, B. R. and Soula, H. A. (2011) Impact of receptor clustering on ligand binding BMC Syst. Biol. 5, 48 10.1186/1752-0509-5-48
14. Martinez, A., Ortiz Mellet, C., and Garcia Fernandez, J. M. (2013) Cyclodextrin-based multivalent glycodisplays: covalent and supramolecular conjugates to assess carbohydrate-protein interactions Chem. Soc. Rev. 42, 4746-73 10.1039/c2cs35424a
15. Appelhans, D., Klajnert-Maculewicz, B., Janaszewska, A., Lazniewska, J., and Voit, B. (2015) Dendritic glycopolymers based on dendritic polyamine scaffolds: view on their synthetic approaches, characteristics and potential for biomedical applications Chem. Soc. Rev. 44, 3968-96 10.1039/C4CS00339J
16. Tassa, C., Shaw, S. Y., and Weissleder, R. (2011) Dextran-coated iron oxide nanoparticles: a versatile platform for targeted molecular imaging, molecular diagnostics, and therapy Acc. Chem. Res. 44, 842-52 10.1021/ar200084x
17. Montet, X., Funovics, M., Montet-Abou, K., Weissleder, R., and Josephson, L. (2006) Multivalent effects of RGD peptides obtained by nanoparticle display J. Med. Chem. 49, 6087-93 10.1021/jm060515m
18. Cheng, Z., Al Zaki, A., Hui, J. Z., Muzykantov, V. R., and Tsourkas, A. (2012) Multifunctional nanoparticles: cost versus benefit of adding targeting and imaging capabilities Science 338, 903-10 10.1126/science.1226338
19. Lammers, T., Kiessling, F., Hennink, W. E., and Storm, G. (2012) Drug targeting to tumors: principles, pitfalls and (pre-) clinical progress J. Controlled Release 161, 175-87 10.1016/j.jconrel.2011.09.063
20. Bae, Y. H. and Park, K. (2011) Targeted drug delivery to tumors: myths, reality and possibility J. Controlled Release 153, 198-205 10.1016/j.jconrel.2011.06.001
21. Fox, M. E., Szoka, F. C., and Frechet, J. M. (2009) Soluble polymer carriers for the treatment of cancer: the importance of molecular architecture Acc. Chem. Res. 42, 1141-51 10.1021/ar900035f
22. Dix, A. V., Moss, S. M., Phan, K., Hoppe, T., Paoletta, S., Kozma, E., Gao, Z. G., Durell, S. R., Jacobson, K. A., and Appella, D. H. (2014) Programmable nanoscaffolds that control ligand display to a G-protein-coupled receptor in membranes to allow dissection of multivalent effects J. Am. Chem. Soc. 136, 12296-303 10.1021/ja504288s
23. Dix, A. V., Conroy, J. L., George Rosenker, K. M., Sibley, D. R., and Appella, D. H. (2015) PNA-based multivalent scaffolds activate the dopamine D2 receptor ACS Med. Chem. Lett. 6, 425-9 10.1021/ml500478m
24. Selden, N. S., Todhunter, M. E., Jee, N. Y., Liu, J. S., Broaders, K. E., and Gartner, Z. J. (2012) Chemically programmed cell adhesion with membrane-anchored oligonucleotides J. Am. Chem. Soc. 134, 765-8 10.1021/ja2080949
25. Grunstein, D., Maglinao, M., Kikkeri, R., Collot, M., Barylyuk, K., Lepenies, B., Kamena, F., Zenobi, R., and Seeberger, P. H. (2011) Hexameric supramolecular scaffold orients carbohydrates to sense bacteria J. Am. Chem. Soc. 133, 13957-66 10.1021/ja2036767
26. Ornelas-Megiatto, C., Becher, T. B., and Megiatto, J. D. (2015) Interlocked systems in nanomedicine Curr. Top. Med. Chem. 15, 1236-56 10.2174/1568026615666150330111614
27. Kobayashi, H., Longmire, M. R., Ogawa, M., and Choyke, P. L. (2011) Rational chemical design of the next generation of molecular imaging probes based on physics and biology: mixing modalities, colors and signals Chem. Soc. Rev. 40, 4626-48 10.1039/c1cs15077d
28. Nguyen, Q. T. and Tsien, R. Y. (2013) Fluorescence-guided surgery with live molecular navigation - a new cutting edge Nat. Rev. Cancer 13, 653-62 10.1038/nrc3566
29. Chi, C., Du, Y., Ye, J., Kou, D., Qiu, J., Wang, J., Tian, J., and Chen, X. (2014) Intraoperative imaging-guided cancer surgery: from current fluorescence molecular imaging methods to future multi-modality imaging technology Theranostics 4, 1072-84 10.7150/thno.9899
30. Zhang, X., Wang, H., Ma, Z., and Wu, B. (2014) Effects of pharmaceutical PEGylation on drug metabolism and its clinical concerns Expert Opin. Drug Metab. Toxicol. 10, 1691-702 10.1517/17425255.2014.967679
31. Guo, Y., Yuan, H., Rice, W. L., Kumar, A. T., Goergen, C. J., Jokivarsi, K., and Josephson, L. (2012) The PEG-fluorochrome shielding approach for targeted probe design J. Am. Chem. Soc. 134, 19338-41 10.1021/ja309085b
32. Smith, B. D. (2015) Smart molecules for imaging, sensing and health (SMITH) Beilstein J. Org. Chem. 11, 2540-8 10.3762/bjoc.11.274
33. Peck, E. M., Liu, W., Spence, G. T., Shaw, S. K., Davis, A. P., Destecroix, H., and Smith, B. D. (2015) Rapid macrocycle threading by a fluorescent dye-polymer conjugate in water with nanomolar affinity J. Am. Chem. Soc. 137, 8668-71 10.1021/jacs.5b03573
34. Liu, W., Peck, E. M., Hendzel, K. D., and Smith, B. D. (2015) Sensitive structural control of macrocycle threading by a fluorescent squaraine dye flanked by polymer chains Org. Lett. 17, 5268-71 10.1021/acs.orglett.5b02633
35. Liu, W., Peck, E. M., and Smith, B. D. (2016) High affinity macrocycle threading by a near-infrared croconaine dye with flanking polymer chains J. Phys. Chem. B 120, 995-1001 10.1021/acs.jpcb.5b11961
36. White, A. G., Fu, N., Leevy, W. M., Lee, J. J., Blasco, M. A., and Smith, B. D. (2010) Optical imaging of bacterial infection in living mice using deep-red fluorescent squaraine rotaxane probes Bioconjugate Chem. 21, 1297-304 10.1021/bc1000998
37. Rice, D. R., White, A. G., Leevy, W. M., and Smith, B. D. (2015) Fluorescence imaging of interscapular brown adipose tissue in living mice J. Mater. Chem. B 3, 1979-1989 10.1039/C4TB01914H
38. Harris, J. M. and Chess, R. B. (2003) Effect of pegylation on pharmaceuticals Nat. Rev. Drug Discovery 2, 214-21 10.1038/nrd1033
39. Harmatys, K. M., Cole, E. L., and Smith, B. D. (2013) In vivo imaging of bone using a deep-red fluorescent molecular probe bearing multiple iminodiacetate groups Mol. Pharmaceutics 10, 4263-71 10.1021/mp400357v
40. Parkesh, R., Gowin, W., Lee, T. C., and Gunnlaugsson, T. (2006) Synthesis and evaluation of potential CT (computer tomography) contrast agents for bone structure and microdamage analysis Org. Biomol. Chem. 4, 3611-7 10.1039/b606976b
41. Jackson, S. N. and Woods, A. S. (2013) Imaging of noncovalent complexes by MALDI-MS J. Am. Soc. Mass Spectrom. 24, 1950-6 10.1007/s13361-013-0745-3
42. Gassensmith, J. J., Arunkumar, E., Barr, L., Baumes, J. M., DiVittorio, K. M., Johnson, J. R., Noll, B. C., and Smith, B. D. (2007) Self-assembly of fluorescent inclusion complexes in competitive media including the interior of living cells J. Am. Chem. Soc. 129, 15054-9 10.1021/ja075567v
43. Cole, E. L., Arunkumar, E., Xiao, S., Smith, B. A., and Smith, B. D. (2012) Water-soluble, deep-red fluorescent squaraine rotaxanes Org. Biomol. Chem. 10, 5769-73 10.1039/C2OB06783H
44. Hyun, H., Wada, H., Bao, K., Gravier, J., Yadav, Y., Laramie, M., Henary, M., Frangioni, J. V., and Choi, H. S. (2014) Phosphonated near-infrared fluorophores for biomedical imaging of bone Angew. Chem., Int. Ed. 53, 10668-72 10.1002/anie.201404930
45. Bao, K., Nasr, K. A., Hyun, H., Lee, J. H., Gravier, J., Gibbs, S. L., and Choi, H. S. (2015) Charge and hydrophobicity effects of NIR fluorophores on bone-specific imaging Theranostics 5, 609-17 10.7150/thno.11222
46. Sun, S., Blazewska, K. M., Kadina, A. P., Kashemirov, B. A., Duan, X., Triffitt, J. T., Dunford, J. E., Russell, R. G., Ebetino, F. H., and Roelofs, A. J. et al. 2016, Fluorescent bisphosphonate and carboxyphosphonate probes: a versatile imaging toolkit for applications in bone biology and biomedicine Bioconjugate Chem. 27, 329-40 10.1021/acs.bioconjchem.5b00369
47. Bhushan, K. R., Tanaka, E., and Frangioni, J. V. (2007) Synthesis of conjugatable bisphosphonates for molecular imaging of large animals Angew. Chem., Int. Ed. 46, 7969-71 10.1002/anie.200701216
48. Ventura, M., Boerman, O. C., de Korte, C., Rijpkema, M., Heerschap, A., Oosterwijk, E., Jansen, J. A., and Walboomers, X. F. (2014) Preclinical imaging in bone tissue engineering Tissue Eng., Part B 20, 578-95 10.1089/ten.teb.2013.0635
49. Anada, T., Takeda, Y., Honda, Y., Sakurai, K., and Suzuki, O. (2009) Synthesis of calcium phosphate-binding liposome for drug delivery Bioorg. Med. Chem. Lett. 19, 4148-50 10.1016/j.bmcl.2009.05.117
50. Singh, T., Kaur, V., Kumar, M., Kaur, P., Murthy, R. S., and Rawal, R. K. (2015) The critical role of bisphosphonates to target bone cancer metastasis: an overview J. Drug. Target 23, 1-15 10.3109/1061186X.2014.950668
51. Liu, X. M., Zhang, Y., Chen, F., Khutsishvili, I., Fehringer, E. V., Marky, L. A., Bayles, K. W., and Wang, D. (2012) Prevention of orthopedic device-associated osteomyelitis using oxacillin-containing biomineral-binding liposomes Pharm. Res. 29, 3169-79 10.1007/s11095-012-0812-7
52. Santos-Ferreira, I., Bettencourt, A., and Almeida, A. J. (2015) Nanoparticulate platforms for targeting bone infections: meeting a major therapeutic challenge Nanomedicine 10, 3131-45 10.2217/nnm.15.134
53. Schott, S., Vallet, S., Tower, R. J., Noor, S., Tiwari, S., Schem, C., and Busch, C. (2015) In vitro and in vivo toxicity of 5-FdU-alendronate, a novel cytotoxic bone-seeking duplex drug against bone metastasis Invest. New Drugs 33, 816-26 10.1007/s10637-015-0253-3
54. Kootala, S., Tokunaga, M., Hilborn, J., and Iwasaki, Y. (2015) Anti-resorptive functions of poly(ethylene sodium phosphate) on human osteoclasts Macromol. Biosci. 15, 1634-40 10.1002/mabi.201500166
55. Ossipov, D. A. (2015) Bisphosphonate-modified biomaterials for drug delivery and bone tissue engineering Expert Opin. Drug Delivery 12, 1443-58 10.1517/17425247.2015.1021679
56. Groger, D., Kerschnitzki, M., Weinhart, M., Reimann, S., Schneider, T., Kohl, B., Wagermaier, W., Schulze-Tanzil, G., Fratzl, P., and Haag, R. (2014) Selectivity in bone targeting with multivalent dendritic polyanion dye conjugates Adv. Healthcare Mater. 3, 375-85 10.1002/adhm.201300205
57. Mizrahi, D. M., Ziv-Polat, O., Perlstein, B., Gluz, E., and Margel, S. (2011) Synthesis, fluorescence and biodistribution of a bone-targeted near-infrared conjugate Eur. J. Med. Chem. 46, 5175-83 10.1016/j.ejmech.2011.08.040
58. Kubicek, V. and Lukes, I. (2010) Bone-seeking probes for optical and magnetic resonance imaging Future Med. Chem. 2, 521-31 10.4155/fmc.09.162
59. Brounts, S. H., Lee, J. S., Weinberg, S., Lan Levengood, S. K., Smith, E. L., and Murphy, W. L. (2013) High affinity binding of an engineered, modular peptide to bone tissue Mol. Pharmaceutics 10, 2086-90 10.1021/mp300662r
60. Bain, J. L., Bonvallet, P. P., Abou-Arraj, R. V., Schupbach, P., Reddy, M. S., and Bellis, S. L. (2015) Enhancement of the regenerative potential of anorganic bovine bone graft utilizing a polyglutamate-modified BMP2 peptide with improved binding to calcium-containing materials Tissue Eng., Part A 21, 2426-36 10.1089/ten.tea.2015.0160
61. Gray, B. P., Li, S., and Brown, K. C. (2013) From phage display to nanoparticle delivery: functionalizing liposomes with multivalent peptides improves targeting to a cancer biomarker Bioconjugate Chem. 24, 85-96 10.1021/bc300498d
62. Gray, B. P. and Brown, K. C. (2014) Combinatorial peptide libraries: mining for cell-binding peptides Chem. Rev. 114, 1020-81 10.1021/cr400166n
63. Ruzza, P., Marchiani, A., Antolini, N., and Calderan, A. (2012) Peptide-receptor ligands and multivalent approach Anti-Cancer Agents Med. Chem. 12, 416-27 10.2174/187152012800617849