Bimodal tumor-targeting from microenvironment responsive hyaluronan layer-by-layer (LbL) nanoparticles

ACS Nano

Volumn 8, Issue 8, 2014, Pages 8374-8382

  Dreaden, Erik C ^a,b   Morton, Stephen W ^a,b   Shopsowitz, Kevin E ^a,b   Choi, Jae Hyeok ^c,d   Deng, Zhou J ^a,b   Cho, Nam Joon ^c,d,e   Hammond, Paula T ^a,b  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^d NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^e Nanyang Technological University   (Singapore)

Author keywords

controlled delivery; nanomaterials; nanomedicine; polymer engineering; self assembly

Indexed keywords

CELL MEMBRANES; CONTROLLED DRUG DELIVERY; CYTOLOGY; DIAGNOSIS; DISEASES; HYALURONIC ACID; MEDICAL NANOTECHNOLOGY; NANOPARTICLES; NANOSTRUCTURED MATERIALS; SELF ASSEMBLY; STEM CELLS; TUMORS;

CANCER DIAGNOSTICS; CONTROLLED DELIVERY; ELECTROSTATIC COMPLEXES; FUNDAMENTAL BARRIERS; PARTICLE INTERFACE; POLYMER ENGINEERING; STRUCTURAL REORGANIZATION; TUMOR MICROENVIRONMENT;

TARGETED DRUG DELIVERY;

DRUG CARRIER; HERMES ANTIGEN; HYALURONIC ACID; NANOPARTICLE; POLYLYSINE;

ANIMAL; CELL HYPOXIA; CELL TRANSFORMATION; CHEMISTRY; METABOLISM; MOUSE; PH; TRANSPORT AT THE CELLULAR LEVEL; TUMOR CELL LINE; TUMOR MICROENVIRONMENT;

ANIMALS; ANTIGENS, CD44; BIOLOGICAL TRANSPORT; CELL HYPOXIA; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; DRUG CARRIERS; HYALURONIC ACID; HYDROGEN-ION CONCENTRATION; MICE; NANOPARTICLES; POLYLYSINE; TUMOR MICROENVIRONMENT;

EID: 84906706938     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn502861t     Document Type: Article

References (60)

1. Eliasof, S.; Lazarus, D.; Peters, C.; Case, R.; Cole, R.; Hwang, J.; Schluep, T.; Chao, J.; Lin, J.; Yen, Y. et al. Correlating Preclinical Animal Studies and Human Clinical Trials of a Multifunctional, Polymeric Nanoparticle Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 15127-15132
2. Akinc, A.; Zumbuehl, A.; Goldberg, M.; Leshchiner, E. S.; Busini, V.; Hossain, N.; Bacallado, S. A.; Nguyen, D. N.; Fuller, J.; Alvarez, R. et al. A Combinatorial Library of Lipid-Like Materials for Delivery of Rnai Therapeutics Nat. Biotechnol. 2008, 26, 561-569
3. Matsumura, Y.; Maeda, H. A New Concept for Macromolecular Therapeutics in Cancer Chemotherapy: Mechanism of Tumoritropic Accumulation of Proteins and the Antitumor Agent Smancs Cancer Res. 1986, 46, 6387-6392
4. Jain, R. K. Transport of Molecules in the Tumor Interstitium: A Review Cancer Res. 1987, 47, 3039-3051
5. Choi, C. H. J.; Alabi, C. A.; Webster, P.; Davis, M. E. Mechanism of Active Targeting in Solid Tumors with Transferrin-Containing Gold Nanoparticles Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 1235-1240
6. 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
7. Vogelstein, B.; Papadopoulos, N.; Velculescu, V. E.; Zhou, S.; Diaz, L. A.; Kinzler, K. W. Cancer Genome Landscapes Science 2013, 339, 1546-1558
8. Marusyk, A.; Almendro, V.; Polyak, K. Intra-Tumour Heterogeneity: A Looking Glass for Cancer? Nat. Rev. Cancer 2012, 12, 323-334
9. Greaves, M.; Maley, C. C. Clonal Evolution in Cancer Nature 2012, 481, 306-313
10. Park, S. Y.; xF; nen, M.; Kim, H. J.; Michor, F.; Polyak, K. Cellular and Genetic Diversity in the Progression of in Situ Human Breast Carcinomas to an Invasive Phenotype J. Clin. Invest. 2010, 120, 636-644
11. Maley, C. C.; Galipeau, P. C.; Finley, J. C.; Wongsurawat, V. J.; Li, X.; Sanchez, C. A.; Paulson, T. G.; Blount, P. L.; Risques, R.-A.; Rabinovitch, P. S. et al. Genetic Clonal Diversity Predicts Progression to Esophageal Adenocarcinoma Nat. Genet. 2006, 38, 468-473
12. Bedard, P. L.; Hansen, A. R.; Ratain, M. J.; Siu, L. L. Tumour Heterogeneity in the Clinic Nature 2013, 501, 355-364
13. Caruso, F.; Caruso, R. A.; Mohwald, H. Nanoengineering of Inorganic and Hybrid Hollow Spheres by Colloidal Templating Science 1998, 282, 1111-1114
14. Donath, E.; Sukhorukov, G. B.; Caruso, F.; Davis, S. A.; Möhwald, H. Novel Hollow Polymer Shells by Colloid Templated Assembly of Polyelectrolytes Angew. Chem., Int. Ed. 1998, 37, 2201-2205
15. Shutava, T. G.; Balkundi, S. S.; Vangala, P.; Steffan, J. J.; Bigelow, R. L.; Cardelli, J. A.; ONeal, D. P.; Lvov, Y. M. Layer-by-Layer-Coated Gelatin Nanoparticles as a Vehicle for Delivery of Natural Polyphenols ACS Nano 2009, 3, 1877-1885
16. Schneider, G.; Decher, G. From Functional Core/Shell Nanoparticles Prepared via Layer-by-Layer Deposition to Empty Nanospheres Nano Lett. 2004, 4, 1833-1839
17. Zahr, A.; de Villiers, M.; Pishko, M. Encapsulation of Drug Nanoparticles in Self-Assembled Macromolecular Nanoshells Langmuir 2005, 21, 403-410
18. Agarwal, A.; Lvov, Y.; Sawant, R.; Torchilin, V. Stable Nanocolloids of Poorly Soluble Drugs with High Drug Content Prepared Using the Combination of Sonication and Layer-by-Layer Technology J. Controlled Release 2008, 128, 255-260
19. Poon, Z.; Chang, D.; Zhao, X.; Hammond, P. T. Layer-by-Layer Nanoparticles with a Ph-Sheddable Layer for in Vivo Targeting of Tumor Hypoxia ACS Nano 2011, 5, 4284-4292
20. Poon, Z.; Lee, J. B.; Morton, S. W.; Hammond, P. T. Controlling in Vivo Stability and Biodistribution in Electrostatically Assembled Nanoparticles for Systemic Delivery Nano Lett. 2011, 11, 2096-2103
21. Hammond, P. T. Polyelectrolyte Multilayered Nanoparticles: Using Nanolayers for Controlled and Targeted Systemic Release Nanomedicine 2012, 7, 619-622
22. Morton, S.; Herlihy, K.; Shopsowitz, K.; Deng, Z.; Chu, K.; Bowerman, C.; Desimone, J.; Hammond, P. Scalable Manufacture of Built-to-Order Nanomedicine: Spray-Assisted Layer-by-Layer Functionalization of Print Nanoparticles Adv. Mater. 2013, 25, 4707-4713
23. Morton, S.; Poon, Z.; Hammond, P. The Architecture and Biological Performance of Drug-Loaded Lbl Nanoparticles Biomaterials 2013, 34, 5328-5335
24. Sukhishvili, S. A. Responsive Polymer Films and Capsules via Layer-by-Layer Assembly Curr. Opin. Colloid Interface Sci. 2005, 10
25. Luo, R.; Neu, B.; Venkatraman, S. Surface Functionalization of Nanoparticles to Control Cell Interactions and Drug Release Small 2012, 8, 2585-2594
26. Deng, Z. J.; Morton, S. W.; Ben-Akiva, E.; Dreaden, E. C.; Shopsowitz, K. E.; Hammond, P. T. Layer-by-Layer Nanoparticles for Systemic Codelivery of an Anticancer Drug and Sirna for Potential Triple-Negative Breast Cancer Treatment ACS Nano 2013, 7, 9571-9584
27. Morton, S. W.; Shah, N. J.; Quadir, M. A.; Deng, Z. J.; Poon, Z.; Hammond, P. T. Osteotropic Therapy Via Targeted Layer-by-Layer Nanoparticles Adv. Healthcare Mater. 2014, 3 (6) 867-875
28. Lee, J. B.; Hong, J.; Bonner, D. K.; Poon, Z.; Hammond, P. T. Self-Assembled RNA Interference Microsponges for Efficient Sirna Delivery Nat. Mater. 2012, 11, 316-322
29. Ye, C.; Drachuk, I.; Calabrese, R.; Dai, H.; Kaplan, D.; Tsukruk, V. Permeability and Micromechanical Properties of Silk Ionomer Microcapsules Langmuir 2012, 28, 12235-12244
30. Tan, Y.; Mundargi, R.; Chen, M.; Lessig, J.; Neu, B.; Venkatraman, S.; Wong, T. Layer-by-Layer Nanoparticles as an Efficient Sirna Delivery Vehicle for Sparc Silencing Small 2014, 10, 1790-1798
31. Caruso, F.; Spasova, M.; Susha, A.; Giersig, M.; Caruso, R. A. Magnetic Nanocomposite Particles and Hollow Spheres Constructed by a Sequential Layering Approach Chem. Mater. 2001, 13, 109-116
32. Drachuk, I.; Gupta, M. K.; Tsukruk, V. V. Biomimetic Coatings to Control Cellular Function through Cell Surface Engineering Adv. Funct. Mater. 2013, 23, 4437-4453
33. Wilson, J. T.; Cui, W.; Kozlovskaya, V.; Kharlampieva, E.; Pan, D.; Qu, Z.; Krishnamurthy, V. R.; Mets, J.; Kumar, V.; Wen, J. et al. Cell Surface Engineering with Polyelectrolyte Multilayer Thin Films J. Am. Chem. Soc. 2011, 133, 7054-7064
34. Mendelsohn, J.; Barrett, C.; Chan, V.; Pal, A.; Mayes, A.; Rubner, M. Fabrication of Microporous Thin Films from Polyelectrolyte Multilayers Langmuir 2000, 16, 5017-5023
35. Harris, J. J.; Bruening, M. L. Electrochemical and in Situ Ellipsometric Investigation of the Permeability and Stability of Layered Polyelectrolyte Films Langmuir 2000, 16, 2006-2013
36. Petrov, A. I.; Antipov, A. A.; Sukhorukov, G. B. Base-Acid Equilibria in Polyelectrolyte Systems: From Weak Polyelectrolytes to Interpolyelectrolyte Complexes and Multilayered Polyelectrolyte Shells Macromolecules 2003, 36, 10079-10086
37. Jain, R. K.; Stylianopoulos, T. Delivering Nanomedicine to Solid Tumors Nat. Rev. Clin. Oncol. 2010, 7, 653-664
38. De Bock, K.; Mazzone, M.; Carmeliet, P. Antiangiogenic Therapy, Hypoxia, and Metastasis: Risky Liaisons, or Not? Nat. Rev. Clin. Oncol. 2011, 8, 393-404
39. Hashimoto, D.; Hirota, M.; Yagi, Y.; Baba, H. Hyaluronate Carboxymethylcellulose-Based Bioresorbable Membrane (Seprafilm) Reduces Adhesion under the Incision to Make Unplanned Re-Laparotomy Safer Surg. Today 2012, 42, 863-867
40. Al-Hajj, M.; Wicha, M.; Benito-Hernandez, A.; Morrison, S.; Clarke, M. Prospective Identification of Tumorigenic Breast Cancer Cells Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 3983-3988
41. Alvero, A. B.; Chen, R.; Fu, H.-H.; Montagna, M.; Schwartz, P. E.; Rutherford, T.; Silasi, D.-A.; Steffensen, K. D.; Waldstrom, M.; Visintin, I. et al. Molecular Phenotyping of Human Ovarian Cancer Stem Cells Unravels the Mechanisms for Repair and Chemoresistance Cell Cycle 2009, 8, 158-166
42. Zhang, S.; Balch, C.; Chan, M. W.; Lai, H.-C.; Matei, D.; Schilder, J. M.; Yan, P. S.; Huang, T. H.-M.; Nephew, K. P. Identification and Characterization of Ovarian Cancer-Initiating Cells from Primary Human Tumors Cancer Res. 2008, 68, 4311-4320
43. Ricardo, S.; Vieira, A.; Gerhard, R.; Leitão, D.; Pinto, R.; Cameselle-Teijeiro, J.; Milanezi, F.; Schmitt, F.; Paredes, J. Breast Cancer Stem Cell Markers Cd44, Cd24 and Aldh1: Expression Distribution within Intrinsic Molecular Subtype J. Clin. Pathol. 2011, 64, 937-946
44. Choi, K.; Yoon, H.; Kim, J.-H.; Bae, S.; Park, R.-W.; Kang, Y.; Kim, I.-S.; Kwon, I.; Choi, K.; Jeong, S. et al. Smart Nanocarrier Based on Pegylated Hyaluronic Acid for Cancer Therapy ACS Nano 2011, 5, 8591-8599
45. Ganesh, S.; Iyer, A.; Gattacceca, F.; Morrissey, D.; Amiji, M. In Vivo Biodistribution of Sirna and Cisplatin Administered Using Cd44-Targeted Hyaluronic Acid Nanoparticles J. Controlled Release 2013, 172, 699-706
46. Cohen, K.; Emmanuel, R.; Kisin-Finfer, E.; Shabat, D.; Peer, D. Modulation of Drug Resistance in Ovarian Adenocarcinoma Using Chemotherapy Entrapped in Hyaluronan-Grafted Nanoparticle Clusters ACS Nano 2014, 8, 2183-2195
47. Scott, J. E. Supramolecular Organization of Extracellular Matrix Glycosaminoglycans, In Vitro and in the Tissues FASEB J. 1992, 6, 2639-2645
48. Burke, S.; Barrett, C. pH-Responsive Properties of Multilayered Poly(L-lysine)/Hyaluronic Acid Surfaces Biomacromolecules 2003, 4, 1773-1783
49. Bauer, S.; Arpa-Sancet, M.; Finlay, J.; Callow, M.; Callow, J.; Rosenhahn, A. Adhesion of Marine Fouling Organisms on Hydrophilic and Amphiphilic Polysaccharides Langmuir 2013, 29, 4039-4047
50. Mueller, M.; Fusenig, N. Friends or Foes-Bipolar Effects of the Tumour Stroma in Cancer Nat. Rev. Cancer 2004, 4, 839-849
51. Shiratori, S. S.; Rubner, M. F. pH-Dependent Thickness Behavior of Sequentially Adsorbed Layers of Weak Polyelectrolytes Macromolecules 2000, 33, 4213-4219
52. Burke, S. E.; Barrett, C. J. Swelling Behavior of Hyaluronic Acid/Polyallylamine Hydrochloride Multilayer Films Biomacromolecules 2005, 6, 1419-1428
53. Nel, A. E.; Mädler, L.; Velegol, D.; Xia, T.; Hoek, E. M. V.; Somasundaran, P.; Klaessig, F.; Castranova, V.; Thompson, M. Understanding Biophysicochemical Interactions at the Nano-Bio Interface Nat. Mater. 2009, 8, 543-557
54. Wilson, W.; Hay, M. Targeting Hypoxia in Cancer Therapy Nat. Rev. Cancer 2011, 11, 393-410
55. Olaku, V.; Matzke, A.; Mitchell, C.; Hasenauer, S.; Sakkaravarthi, A.; Pace, G.; Ponta, H.; Orian-Rousseau, V. C-Met Recruits Icam-1 as a Coreceptor to Compensate for the Loss of Cd44 in Cd44 Null Mice Mol. Biol. Cell 2011, 22, 2777-2786
56. Zöller, M. Cd44: Can a Cancer-Initiating Cell Profit from an Abundantly Expressed Molecule? Nat. Rev. Cancer 2011, 11, 254-267
57. Lopez, J.; Camenisch, T.; Stevens, M.; Sands, B.; McDonald, J.; Schroeder, J. Cd44 Attenuates Metastatic Invasion During Breast Cancer Progression Cancer Res. 2005, 65, 6755-6763
58. Tian, X.; Azpurua, J.; Hine, C.; Vaidya, A.; Myakishev-Rempel, M.; Ablaeva, J.; Mao, Z.; Nevo, E.; Gorbunova, V.; Seluanov, A. High-Molecular-Mass Hyaluronan Mediates the Cancer Resistance of the Naked Mole Rat Nature 2013, 499, 346-349
59. Cho, N.-J.; Frank, C.; Kasemo, B.; Höök, F. Quartz Crystal Microbalance with Dissipation Monitoring of Supported Lipid Bilayers on Various Substrates Nat. Protoc. 2010, 5, 1096-1106
60. Vinci, M.; Gowan, S.; Boxall, F.; Patterson, L.; Zimmermann, M.; Court, W.; Lomas, C.; Mendiola, M.; Hardisson, D.; Eccles, S. Advances in Establishment and Analysis of Three-Dimensional Tumor Spheroid-Based Functional Assays for Target Validation and Drug Evaluation BMC Biol. 2012, 10, 29