Bromelain surface modification increases the diffusion of silica nanoparticles in the tumor extracellular matrix

ACS Nano

Volumn 8, Issue 10, 2014, Pages 9874-9883

  Parodi, Alessandro ^a,b   Haddix, Seth G ^a   Taghipour, Nima ^a   Scaria, Shilpa ^a   Taraballi, Francesca ^a,g   Cevenini, Armando ^a,c,d   Yazdi, Iman K ^a,e   Corbo, Claudia ^a,b   Palomba, Roberto ^a,b   Khaled, Sm Z ^a   Martinez, Jonathan O ^a,f   Brown, Brandon S ^a,f   Isenhart, Lucas ^a   Tasciotti, Ennio ^a  

^a HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^b IRCCS SDN   (Italy)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^d CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^e University of Houston   (United States)

^f UNIVERSITY OF TEXAS   (United States)

^g FONDAZIONE IRCCS POLICLINICO SAN MATTEO   (Italy)

Author keywords

Bromelain; cancer; cellular uptake; extracellular matrix digestion; mesoporous silica nanoparticle modification

Indexed keywords

BROMELAIN; CELL CULTURE; CONTROLLED DRUG DELIVERY; DISEASES; NANOPARTICLES; SILICA; TARGETED DRUG DELIVERY; TUMORS;

BIOLOGICAL BARRIER; CANCER; CELLULAR UPTAKE; DRUG DELIVERY SYSTEM; ENHANCED PENETRATION; ENZYMATIC COMPLEXES; EXTRACELLULAR MATRICES; MESOPOROUS SILICA NANOPARTICLES;

SILICA NANOPARTICLES;

BROMELAIN; NANOPARTICLE; SILICON DIOXIDE;

CHEMISTRY; DIFFUSION; EXTRACELLULAR MATRIX; INFRARED SPECTROSCOPY; NEOPLASM; PATHOLOGY; SURFACE PROPERTY; TRANSMISSION ELECTRON MICROSCOPY; VASCULARIZATION;

BROMELAINS; DIFFUSION; EXTRACELLULAR MATRIX; MICROSCOPY, ELECTRON, TRANSMISSION; NANOPARTICLES; NEOPLASMS; SILICON DIOXIDE; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; SURFACE PROPERTIES;

EID: 84908433122     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn502807n     Document Type: Article

References (45)

1. Rakesh, K. J.; Triantafyllos, S. Delivering Nanomedicine to Solid Tumors Nat. Rev. Clin. Oncol. 2010, 7, 653-664
2. Wong, C.; Stylianopoulos, T.; Cui, J.; Martin, J.; Chauhan, V. P.; Jiang, W.; Popović, Z.; Jain, R. K.; Bawendi, M. G.; Fukumura, D. Multistage Nanoparticle Delivery System for Deep Penetration into Tumor Tissue Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 2426-2431
3. Wang, A. Z.; Langer, R.; Farokhzad, O. C. Nanoparticle Delivery of Cancer Drugs Ann. Rev. Med. 2012, 63, 185-198
4. Shekhar, C. Lean and Mean: Nanoparticle-Based Delivery Improves Performance of Cancer Drugs Chem. Biol. 2009, 16, 349-350
5. Torchilin, V. Tumor Delivery of Macromolecular Drugs Based on the Epr Effect Adv. Drug Delivery Rev. 2011, 63, 131-135
6. Plopper, G. The Extracellular Matrix and Cellular Adhesion, in Cells; Lewin, B. C.; Cassimens, L.; Lingappa, V. R.; Plopper, G., Eds.; Jones and Bartlett: Sudbury, MA, 2007.
7. Hirsch, L. R.; Stafford, R.; Bankson, J.; Sershen, S.; Rivera, B.; Price, R.; Hazle, J.; Halas, N.; West, J. Nanoshell-Mediated near-Infrared Thermal Therapy of Tumors under Magnetic Resonance Guidance Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 13549-13554
8. Beyer, I.; Li, Z.; Persson, J.; Liu, Y.; van Rensburg, R.; Yumul, R.; Zhang, X. B.; Hung, M. C.; Lieber, A. Controlled Extracellular Matrix Degradation in Breast Cancer Tumors Improves Therapy by Trastuzumab Mol. Ther. 2011, 19, 479-489
9. Eikenes, L.; Bruland, Ø. S.; Brekken, C.; de Lange Davies, C. Collagenase Increases the Transcapillary Pressure Gradient and Improves the Uptake and Distribution of Monoclonal Antibodies in Human Osteosarcoma Xenografts Cancer Res. 2004, 64, 4768-4773
10. Stylianopoulos, T.; Poh, M.-Z.; Insin, N.; Bawendi, M. G.; Fukumura, D.; Munn, L. L.; Jain, R. K. Diffusion of Particles in the Extracellular Matrix: The Effect of Repulsive Electrostatic Interactions Biophys. J. 2010, 99, 1342-1349
11. Netti, P. A.; Berk, D. A.; Swartz, M. A.; Grodzinsky, A. J.; Jain, R. K. Role of Extracellular Matrix Assembly in Interstitial Transport in Solid Tumors Cancer Res. 2000, 60, 2497-2503
12. Mitragotri, S.; Lahann, J. Materials for Drug Delivery: Innovative Solutions to Address Complex Biological Hurdles Adv. Mater. 2012, 24, 3717-3723
13. Gullotti, E.; Yeo, Y. Extracellularly Activated Nanocarriers: A New Paradigm of Tumor Targeted Drug Delivery Mol. Pharmaceutics 2009, 6, 1041-1051
14. Kong, S. D.; Zhang, W.; Lee, J. H.; Brammer, K.; Lal, R.; Karin, M.; Jin, S. Magnetically Vectored Nanocapsules for Tumor Penetration and Remotely Switchable on-Demand Drug Release Nano Lett. 2010, 10, 5088-5092
15. Eikenes, L.; Tari, M.; Tufto, I.; Bruland, Ø. S.; de Lange Davies, C. Hyaluronidase Induces a Transcapillary Pressure Gradient and Improves the Distribution and Uptake of Liposomal Doxorubicin (Caelyx) in Human Osteosarcoma Xenografts Br. J. Cancer 2005, 93, 81-88
16. Ganesh, S.; Gonzalez-Edick, M.; Gibbons, D.; Van Roey, M.; Jooss, K. Intratumoral Coadministration of Hyaluronidase Enzyme and Oncolytic Adenoviruses Enhances Virus Potency in Metastatic Tumor Models Clin. Cancer Res. 2008, 14, 3933-3941
17. Maurer, H. Bromelain: Biochemistry, Pharmacology and Medical Use CMLS, Cell. Mol. Life Sci. 2001, 58, 1234-1245
18. Pavan, R.; Jain, S.; Shraddha; Kumar, A. Properties and Therapeutic Application of Bromelain: A Review Biotechnol. Res. Int. 2012, 2012 976203
19. El-Gharbawi, M.; Whitaker, J. R. Fractionation and Partial Characterization of the Proteolytic Enzymes of Stem Bromelain Biochemistry 1963, 2, 476-481
20. Harrach, T.; Eckert, K.; Schulze-Forster, K.; Nuck, R.; Grunow, D.; Maurer, H. R. Isolation and Partial Characterization of Basic Proteinases from Stem Bromelain J. Protein Chem. 1995, 14, 41-52
21. Lee, K. L.; Albee, K. L.; Bernasconi, R. J.; Edmunds, T. Complete Amino Acid Sequence of Ananain and a Comparison with Stem Bromelain and Other Plant Cysteine Proteases Biochem. J. 1997, 327 (Pt. 1) 199-202
22. Istrati, D.; Vizireanu, C.; Dima, F.; Dinicə, R. Effect of Marination with Proteolytic Enzymes on Quality of Beef Muscle St. Cerc. St. CICBIA 2012, 13, 81-89
23. Tochi, B. N.; Wang, Z.; Xu, S.-Y.; Zhang, W. Therapeutic Application of Pineapple Protease (Bromelain): A Review Pak. J. Nutr. 2008, 7, 513-520
24. Heinicke, R.; van der Wal, L.; Yokoyama, M. Effect of Bromelain (Ananase) on Human Platelet Aggregation Cell. Mol. Life Sci. 1972, 28, 844-845
25. Brien, S.; Lewith, G.; Walker, A.; Hicks, S. M.; Middleton, D. Bromelain as a Treatment for Osteoarthritis: A Review of Clinical Studies J. Evidence-Based Complementary Altern. Med. 2004, 1, 251-257
26. Braun, J.; Schneider, B.; Beuth, H. Therapeutic Use, Efficiency and Safety of the Proteolytic Pineapple Enzyme Bromelain-Pos in Children with Acute Sinusitis in Germany In Vivo 2005, 19, 417-421
27. Batkin, S.; Taussig, S.; Szekerezes, J. Antimetastatic Effect of Bromelain with or without Its Proteolytic and Anticoagulant Activity J. Cancer Res. Clin. Oncol. 1988, 114, 507-508
28. Chobotova, K.; Vernallis, A. B.; Majid, F. A. A. Bromelains Activity and Potential as an Anti-Cancer Agent: Current Evidence and Perspectives Cancer Lett. 2010, 290, 148-156
29. Chiang, Y.-D.; Lian, H.-Y.; Leo, S.-Y.; Wang, S.-G.; Yamauchi, Y.; Wu, K. C.-W. Controlling Particle Size and Structural Properties of Mesoporous Silica Nanoparticles Using the Taguchi Method J. Phys. Chem. C 2011, 115, 13158-13165
30. Maria Chong, A.; Zhao, X. Functionalization of Sba-15 with Aptes and Characterization of Functionalized Materials J. Phys. Chem. B 2003, 107, 12650-12657
31. Soares, P. A.; Vaz, A. F.; Correia, M. T.; Pessoa, A., Jr.; Carneiro-da-Cunha, M. G. Purification of Bromelain from Pineapple Wastes by Ethanol Precipitation Sep. Purif. Technol. 2012, 98, 389-395
32. Blanka, H. K.; Catherine, C. B.; Seher, G.-A.; Lucienne, J.-J. Induction of Oxidative Stress, Lysosome Activation and Autophagy by Nanoparticles in Human Brain-Derived Endothelial Cells Biochem. J. 2012, 441, 813-821
33. Wu, S.; Li, Z.; Han, J.; Han, S. Dual Colored Mesoporous Silica Nanoparticles with Ph Activable Rhodamine-Lactam for Ratiometric Sensing of Lysosomal Acidity Chem. Commun. 2011, 47, 11276-11278
34. Stern, S. T.; Adiseshaiah, P. P.; Crist, R. M. Autophagy and Lysosomal Dysfunction as Emerging Mechanisms of Nanomaterial Toxicity Part. Fibre Toxicol. 2012, 9, 20
35. Albini, A.; Mussi, V.; Parodi, A.; Ventura, A.; Principi, E.; Tegami, S.; Rocchia, M.; Francheschi, E.; Sogno, I.; Cammarota, R. Interactions of Single-Wall Carbon Nanotubes with Endothelial Cells Nanomedicine (N. Y., NY, U.S.) 2010, 6, 277-288
36. Monteiro-Riviere, N. A.; Inman, A. O.; Zhang, L. Limitations and Relative Utility of Screening Assays to Assess Engineered Nanoparticle Toxicity in a Human Cell Line Toxicol. Appl. Pharmacol. 2009, 234, 222-235
37. Khan, R. H.; Rasheedi, S.; Haq, S. K. Effect of pH, Temperature and Alcohols on the Stability of Glycosylated and Deglycosylated Stem Bromelain J. Biosci. 2003, 28, 709-714
38. Donovan, D.; Brown, N.; Bishop, E.; Lewis, C. Comparison of Three in Vitro Human Angiogenesis Assays with Capillaries Formed in Vivo Angiogenesis 2001, 4, 113-121
39. Ponce, M. L. In Vitro Matrigel Angiogenesis Assays. In Angiogenesis Protocols; Murray, J. C., Ed.; Humana Press: Totowa, NJ, 2001; pp 205-209.
40. Cukierman, E.; Khan, D. R. The Benefits and Challenges Associated with the Use of Drug Delivery Systems in Cancer Therapy Biochem. Pharmacol. 2010, 80, 762-770
41. Primeau, A. J.; Rendon, A.; Hedley, D.; Lilge, L.; Tannock, I. F. The Distribution of the Anticancer Drug Doxorubicin in Relation to Blood Vessels in Solid Tumors Clin. Cancer Res. 2005, 11, 8782-8788
42. Choi, I.-K.; Strauss, R.; Richter, M.; Yun, C.-O.; Lieber, A. Strategies to Increase Drug Penetration in Solid Tumors Front. Oncol. 2013, 3, 193
43. Minchinton, A. I.; Tannock, I. F. Drug Penetration in Solid Tumours Nat. Rev. Cancer 2006, 6, 583-592
44. Chau, Y.; Padera, R. F.; Dang, N. M.; Langer, R. Antitumor Efficacy of a Novel Polymer-Peptide-Drug Conjugate in Human Tumor Xenograft Models Int. J. Cancer 2006, 118, 1519-1526
45. Chau, Y.; Dang, N. M.; Tan, F. E.; Langer, R. Investigation of Targeting Mechanism of New Dextran-Peptide-Methotrexate Conjugates Using Biodistribution Study in Matrix-Metalloproteinase-Overexpressing Tumor Xenograft Model J. Pharm. Sci. 2006, 95, 542-551