Force spectroscopy of multivalent binding of riboflavin-conjugated dendrimers to riboflavin binding protein

Journal of Physical Chemistry B

Volumn 119, Issue 18, 2015, Pages 5785-5792

  Leistra, Abigail N ^a   Han, Jong Hyun ^a   Tang, Shengzhuang ^b   Orr, Bradford G ^b,c   Banaszak Holl, Mark M ^b,c   Choi, Seok Ki ^b,d   Sinniah, Kumar ^a  

^a CALVIN COLLEGE   (United States)

^b UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DENDRIMERS; LIGANDS; LOADING; MOBILE SECURITY; NANOPARTICLES; PROTEINS;

BINDING INTERACTION; CELLULAR INTERACTION; MULTIVALENT BINDING; MULTIVALENT INTERACTIONS; MULTIVALENT LIGANDS; RIBOFLAVIN BINDING PROTEIN; SINGLE MOLECULE FORCE SPECTROSCOPY; TARGETED DRUG DELIVERY SYSTEMS;

BINDING ENERGY;

CARRIER PROTEIN; DENDRIMER; NANOPARTICLE; PAMAM STARBURST; PROTEIN BINDING; RIBOFLAVIN; RIBOFLAVIN-BINDING PROTEIN;

ATOMIC FORCE MICROSCOPY; CALORIMETRY; CHEMICAL STRUCTURE; CHEMISTRY; KINETICS; SPECTROSCOPY; THERMODYNAMICS;

CALORIMETRY; DENDRIMERS; KINETICS; MEMBRANE TRANSPORT PROTEINS; MICROSCOPY, ATOMIC FORCE; MODELS, MOLECULAR; NANOPARTICLES; PROTEIN BINDING; RIBOFLAVIN; SPECTRUM ANALYSIS; THERMODYNAMICS;

EID: 84928978529     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/acs.jpcb.5b01028     Document Type: Article

References (49)

1. Kiessling, L. L.; Gestwicki, J. E.; Strong, L. E. Synthetic Multivalent Ligands as Probes of Signal Transduction Angew. Chem., Int. Ed. 2006, 45, 2348-2368
2. Mammen, M.; Choi, S. K.; Whitesides, G. M. Polyvalent Interactions in Biological Systems: Implications for Design and Use of Multivalent Ligands and Inhibitors Angew. Chem., Int. Ed. 1998, 37, 2754-2794
3. Roy, R. Syntheses and Some Applications of Chemically Defined Multivalent Glycoconjugates Curr. Opin. Struct. Biol. 1996, 6, 692-702
4. Fasting, C.; Schalley, C. A.; Weber, M.; Seitz, O.; Hecht, S.; Koksch, B.; Dernedde, J.; Graf, C.; Knapp, E.-W.; Haag, R. Multivalency as a Chemical Organization and Action Principle Angew. Chem., Int. Ed. 2012, 51, 10472-10498
5. Li, M.-H.; Choi, S. K.; Leroueil, P.; Baker, J. R. Evaluating Binding Avidities of Populations of Heterogeneous Multivalent Ligand-Functionalized Nanoparticles ACS Nano 2014, 8, 5600-5609
6. Majoros, I. J.; Williams, C. R.; Becker, A.; Baker, J. R., Jr. Methotrexate Delivery Via Folate Targeted Dendrimer-Based Nanotherapeutic Platform Wiley Interdiscip. Rev.: Nanomed. Nanobiotechnol. 2009, 1, 502-510
7. Patri, A. K.; Kukowska-Latallo, J. F.; Baker, J. J. R. Targeted Drug Delivery with Dendrimers: Comparison of the Release Kinetics of Covalently Conjugated Drug and Non-Covalent Drug Inclusion Complex Adv. Drug Delivery Rev. 2005, 57, 2203-2214
8. Paulos, C. M.; Turk, M. J.; Breur, G. J.; Low, P. S. Folate Receptor-Mediated Targeting of Therapeutic and Imaging Agents to Activated Macrophages in Rheumatoid Arthritis Adv. Drug Delivery Rev. 2004, 56, 1205-1217
9. Zhao, X.; Li, H.; Lee, R. J. Targeted Drug Delivery Via Folate Receptors Expert Opin. Drug Delivery 2008, 5, 309-319
10. Hong, S.; Leroueil, P. R.; Majoros, I. J.; Orr, B. G.; Baker, J. R., Jr.; Banaszak Holl, M. M. The Binding Avidity of a Nanoparticle-Based Multivalent Targeted Drug Delivery Platform Chem. Biol. (Oxford, U. K.) 2007, 14, 107-115
11. Silpe, J. E.; Sumit, M.; Thomas, T. P.; Huang, B.; Kotlyar, A.; van Dongen, M. A.; Banaszak Holl, M. M.; Orr, B. G.; Choi, S. K. Avidity Modulation of Folate-Targeted Multivalent Dendrimers for Evaluating Biophysical Models of Cancer Targeting Nanoparticles ACS Chem. Biol. 2013, 8, 2063-2071
12. Choi, S. K.; Myc, A.; Silpe, J. E.; Sumit, M.; Wong, P. T.; McCarthy, K.; Desai, A. M.; Thomas, T. P.; Kotlyar, A.; Banaszak Holl, M. M.; Orr, B. G.; Baker, J. R. Dendrimer-Based Multivalent Vancomycin Nanoplatform for Targeting the Drug-Resistant Bacterial Surface ACS Nano 2013, 7, 214-228
13. Plomp, M.; Malkin, A. J. Mapping of Proteomic Composition on the Surfaces of Bacillus Spores by Atomic Force Microscopy-Based Immunolabeling Langmuir 2008, 25, 403-409
14. Schotanus, M. P.; Aumann, K. S.; Sinniah, K. Using Force Spectroscopy to Investigate the Binding of Complementary DNA in the Presence of Intercalating Agents Langmuir 2002, 18, 5333-5336
15. Dufrene, Y. F.; Martinez-Martin, D.; Medalsy, I.; Alsteens, D.; Muller, D. J. Multiparametric Imaging of Biological Systems by Force-Distance Curve-Based AFM Nat. Methods 2013, 10, 847-854
16. Shukla, R.; Thomas, T. P.; Desai, A. M.; Kotlyar, A.; Park, S. J.; Baker, J. R., Jr. Her2 Specific Delivery of Methotrexate by Dendrimer Conjugated Anti-Her2Mab Nanotechnology 2008, 19, 295102
17. Thomas, T. P.; Shukla, R.; Kotlyar, A.; Liang, B.; Ye, J. Y.; Norris, T. B.; Baker, J. R., Jr. Dendrimer-Epidermal Growth Factor Conjugate Displays Superagonist Activity Biomacromolecules 2008, 9, 603-609
18. Kukowska-Latallo, J. F.; Candido, K. A.; Cao, Z.; Nigavekar, S. S.; Majoros, I. J.; Thomas, T. P.; Balogh, L. P.; Khan, M. K.; Baker, J. R., Jr. Nanoparticle Targeting of Anticancer Drug Improves Therapeutic Response in Animal Model of Human Epithelial Cancer Cancer Res. 2005, 65, 5317-5324
19. Tomalia, D. A.; Baker, H.; Dewald, J.; Hall, M.; Kallos, G.; Martin, S.; Roeck, J.; Ryder, J.; Smith, P. A New Class of Polymers: Starburst-Dendritic Macromolecules Polym. J. (Tokyo, Jpn.) 1985, 17, 117-132
20. Tomalia, D. A.; Naylor, A. M.; William, A.; Goddard, I. Starburst Dendrimers: Molecular-Level Control of Size, Shape, Surface Chemistry, Topology, and Flexibility from Atoms to Macroscopic Matter Angew. Chem., Int. Ed. 1990, 29, 138-175
21. van Dongen, M. A.; Orr, B. G.; Banaszak Holl, M. M. Diffusion NMR Study of Generation-Five Pamam Dendrimer Materials J. Phys. Chem. B 2014, 118, 7195-7202
22. Thomas, T. P.; Choi, S. K.; Li, M.-H.; Kotlyar, A.; Baker, J. R., Jr. Design of Riboflavin-Presenting Pamam Dendrimers as a New Nanoplatform for Cancer-Targeted Delivery Bioorg. Med. Chem. Lett. 2010, 20, 5191-5194
23. Witte, A. B.; Timmer, C. M.; Gam, J. J.; Choi, S. K.; Banaszak Holl, M. M.; Orr, B. G.; Baker, J. R., Jr.; Sinniah, K. Biophysical Characterization of a Riboflavin-Conjugated Dendrimer Platform for Targeted Drug Delivery Biomacromolecules 2012, 13, 507-516
24. Witte, A. B.; Leistra, A. N.; Wong, P. T.; Bharathi, S.; Refior, K.; Smith, P.; Kaso, O.; Sinniah, K.; Choi, S. K. Atomic Force Microscopy Probing of Receptor-Nanoparticle Interactions for Riboflavin Receptor Targeted Gold-Dendrimer Nanocomposites J. Phys. Chem. B 2014, 118, 2872-2882
25. Wong, P. T.; Tang, K.; Coulter, A.; Tang, S.; Baker, J. R., Jr.; Choi, S. K. Multivalent Dendrimer Vectors with DNA Intercalation Motifs for Gene Delivery Biomacromolecules 2014, 15, 4134-4145
26. Karande, A. A.; Sridhar, L.; Gopinath, K. S.; Adiga, P. R. Riboflavin Carrier Protein: A Serum and Tissue Marker for Breast Carcinoma Int. J. Cancer 2001, 95, 277-281
27. Johnson, T.; Ouhtit, A.; Gaur, R.; Fernando, A.; Schwarzenberger, P.; Su, J.; Ismail, M. F.; El-Sayyad, H. I.; Karande, A.; Elmageed, Z. A.; Rao, P.; Raj, M. Biochemical Characterization of Riboflavin Carrier Protein (RCP) in Prostate Cancer Front. Biosci., Landmark Ed. 2009, 14, 3634-3640
28. Hilgenbrink, A. R.; Low, P. S. Folate Receptor-Mediated Drug Targeting: From Therapeutics to Diagnostics J. Pharm. Sci. 2005, 94, 2135-2146
29. Lee, R. J.; Low, P. S. Folate-Mediated Tumor Cell Targeting of Liposome-Entrapped Doxorubicin in Vitro Biochim. Biophys. Acta, Biomembr. 1995, 1233, 134-144
30. Wong, P. T.; Choi, S. K. Mechanisms and Implications of Dual-Acting Methotrexate in Folate-Targeted Nanotherapeutic Delivery Int. J. Mol. Sci. 2015, 16, 1772-1790
31. Montet, X.; Funovics, M.; Montet-Abou, K.; Weissleder, R.; Josephson, L. Multivalent Effects of Rgd Peptides Obtained by Nanoparticle Display J. Med. Chem. 2006, 49, 6087-6093
32. Shukla, R.; Thomas, T. P.; Peters, J.; Kotlyar, A.; Myc, A.; Baker, J. R., Jr. Tumor Angiogenic Vasculature Targeting with PAMAM Dendrimer-RGD Conjugates Chem. Commun. (Cambridge, U. K.) 2005, 5739-5741
33. Temming, K.; Lacombe, M.; Schaapveld, R. Q. J.; Orfi, L.; Kéri, G.; Poelstra, K.; Molema, G.; Kok, R. J. Rational Design of Rgd-Albumin Conjugates for Targeted Delivery of the Vegf-R Kinase Inhibitor Ptk787 to Angiogenic Endothelium ChemMedChem 2006, 1, 1200-1203
34. Chen, Y.; Foss, C. A.; Byun, Y.; Nimmagadda, S.; Pullambhatla, M.; Fox, J. J.; Castanares, M.; Lupold, S. E.; Babich, J. W.; Mease, R. C. Radiohalogenated Prostate-Specific Membrane Antigen (Psma)-Based Ureas as Imaging Agents for Prostate Cancer J. Med. Chem. 2008, 51, 7933-7943
35. Raha, S.; Paunesku, T.; Woloschak, G. Peptide-Mediated Cancer Targeting of Nanoconjugates Wiley Interdiscip. Rev.: Nanomed. Nanobiotechnol. 2010, 3, 269-281
36. Plantinga, A.; Witte, A.; Li, M.-H.; Harmon, A.; Choi, S. K.; Banaszak Holl, M. M.; Orr, B. G.; Baker, J. R., Jr.; Sinniah, K. Bioanalytical Screening of Riboflavin Antagonists for Targeted Drug Delivery-a Thermodynamic and Kinetic Study ACS Med. Chem. Lett. 2011, 2, 363-367
37. Ratto, T. V.; Rudd, R. E.; Langry, K. C.; Balhorn, R. L.; McElfresh, M. W. Nonlinearly Additive Forces in Multivalent Ligand Binding to a Single Protein Revealed with Force Spectroscopy Langmuir 2006, 22, 1749-1757
38. Sulchek, T.; Friddle, R. W.; Noy, A. Strength of Multiple Parallel Biological Bonds Biophys. J. 2006, 90, 4686-4691
39. Zhang, Y.; Yu, Y.; Jiang, Z.; Xu, H.; Wang, Z.; Zhang, X.; Oda, M.; Ishizuka, T.; Jiang, D.; Chi, L.; Fuchs, H. Single-Molecule Study on Intermolecular Interaction between C60 and Porphyrin Derivatives: Toward Understanding the Strength of the Multivalency Langmuir 2009, 25, 6627-6632
40. Gomez-Casado, A.; Dam, H. H.; Yilmaz, M. D.; Florea, D.; Jonkheijm, P.; Huskens, J. Probing Multivalent Interactions in a Synthetic Host-Guest Complex by Dynamic Force Spectroscopy J. Am. Chem. Soc. 2011, 133, 10849-10857
41. Mullen, D. G.; Banaszak Holl, M. M. Heterogeneous Ligand-Nanoparticle Distributions: A Major Obstacle to Scientific Understanding and Commercial Translation Acc. Chem. Res. 2011, 44, 1135-1145
42. Vander Wal, M.; Kamper, S.; Headley, J.; Sinniah, K. Effects of Contact Force and Salt Concentration on the Unbinding of a DNA Duplex by Force Spectroscopy Langmuir 2005, 22, 882-886
43. Teulon, J. M.; Delcuze, Y.; Odorico, M.; Chen, S. W.; Parot, P.; Pellequer, J. L. Single and Multiple Bonds in (Strept)Avidin-Biotin Interactions J. Mol. Recognit. 2011, 24, 490-502
44. Evans, E. Energy Landscapes of Biomolecular Adhesion and Receptor Anchoring at Interfaces Explored with Dynamic Force Spectroscopy Faraday Discuss. 1998, 1-16
45. Evans, E. Probing the Relation between Force-Lifetime-and Chemistry in Single Molecular Bonds Annu. Rev. Biophys. Biomol. Struct. 2001, 30, 105-128
46. Bell, G. I. Models for the Specific Adhesion of Cells to Cells Science 1978, 200, 618-627
47. Krishnamurthy, V. M.; Estroff, L. A.; Whitesides, G. M. Multivalency in Ligand Design. Fragment-Based Approaches in Drug Discovery; Wiley-VCH Verlag GmbH & Co. KGaA: Weinheim, Germany, 2006; pp 11-53.
48. Wu, X. F.; Cai, Z. X.; Sun, S. G.; Huang, Q.; Ren, G. D.; He, L.; Ma, M. H. [Investigation of Interaction between Riboflavin and Riboflavin Binding Protein by Fluorescence Spectroscopy] Guangpuxue Yu Guangpu Fenxi 2012, 32, 719-722
49. Mullen, D. G.; Borgmeier, E. L.; Desai, A. M.; van Dongen, M. A.; Barash, M.; Cheng, X. M.; Baker, J. R., Jr.; Banaszak Holl, M. M. Isolation and Characterization of Dendrimers with Precise Numbers of Functional Groups Chem. Eur. J. 2010, 16, 10675-10678