Biodistribution and pharmacokinetics of EGFR-targeted thiolated gelatin nanoparticles following systemic administration in pancreatic tumor-bearing mice

Molecular Pharmaceutics

Volumn 10, Issue 5, 2013, Pages 2031-2044

  Xu, Jing ^a   Gattacceca, Florence ^a,b   Amiji, Mansoor ^a  

^a NORTHEASTERN UNIVERSITY   (United States)

^b UNIV MONTPELLIER   (France)

Author keywords

active tumor targeting; biodistribution; epidermal growth factor receptor (EGFR) targeting; long circulation time; passive tumor targeting; pharmacokinetics; poly(ethylene glycol); population analysis; targeting efficiency; thiolated type B gelatin nanoparticles; two compartment model

Indexed keywords

ANTINEOPLASTIC AGENT; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR THIOLATED TYPE B GELATIN NANOPARTICLE; GELATIN; INDIUM 111; MACROGOL; UNCLASSIFIED DRUG; EGFR PROTEIN, HUMAN; GE11 PEPTIDE; INDIUM; MACROGOL DERIVATIVE; NANOPARTICLE; PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; AREA UNDER THE CURVE; ARTICLE; CHEMICAL MODIFICATION; CONTROLLED STUDY; CYTOTOXICITY; FEMALE; IN VIVO STUDY; MOUSE; NONHUMAN; PANCREAS ADENOCARCINOMA; PRIORITY JOURNAL; PROTEIN TARGETING; SIGNAL TRANSDUCTION; SURFACE PROPERTY; SYNTHESIS; ZETA POTENTIAL; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMISTRY; DRUG DELIVERY SYSTEM; DRUG SCREENING; HUMAN; METABOLISM; PANCREATIC NEOPLASMS; SCID MOUSE; TISSUE DISTRIBUTION; TUMOR CELL LINE; ULTRASTRUCTURE;

ANIMALS; CELL LINE, TUMOR; DRUG DELIVERY SYSTEMS; FEMALE; GELATIN; HUMANS; INDIUM RADIOISOTOPES; MICE; MICE, SCID; NANOPARTICLES; PANCREATIC NEOPLASMS; PEPTIDES; POLYETHYLENE GLYCOLS; RECEPTOR, EPIDERMAL GROWTH FACTOR; TISSUE DISTRIBUTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84877262163     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp400054e     Document Type: Article

References (75)

1. Xu, J.; Ganesh, S.; Amiji, M. Non-condensing polymeric nanoparticles for targeted gene and siRNA delivery Int. J. Pharmaceutics 2012, 427 (1) 21-34
2. Choi, S. W.; Lee, S. H.; Mok, H.; Park, T. G. Multifunctional siRNA delivery system: polyelectrolyte complex micelles of six-arm PEG conjugate of siRNA and cell penetrating peptide with crosslinked fusogenic peptide Biotechnol. Prog. 2010, 26 (1) 57-63
3. Kim, H. K.; Davaa, E.; Myung, C. S.; Park, J. S. Enhanced siRNA delivery using cationic liposomes with new polyarginine-conjugated PEG-lipid Int. J. Pharmaceutics 2010, 392 (1-2) 141-7
4. van Vlerken, L. E.; Duan, Z.; Little, S. R.; Seiden, M. V.; Amiji, M. M. Biodistribution and pharmacokinetic analysis of Paclitaxel and ceramide administered in multifunctional polymer-blend nanoparticles in drug resistant breast cancer model Mol. Pharmaceutics 2008, 5 (4) 516-26
5. Kommareddy, S.; Tiwari, S. B.; Amiji, M. M. Long-circulating polymeric nanovectors for tumor-selective gene delivery Technol. Cancer Res. Treat. 2005, 4 (6) 615-25
6. Monsky, W. L.; Fukumura, D.; Gohongi, T.; Ancukiewcz, M.; Weich, H. A.; Torchilin, V. P.; Yuan, F.; Jain, R. K. Augmentation of transvascular transport of macromolecules and nanoparticles in tumors using vascular endothelial growth factor Cancer Res. 1999, 59 (16) 4129-35
7. Cho, K.; Wang, X.; Nie, S.; Chen, Z. G.; Shin, D. M. Therapeutic nanoparticles for drug delivery in cancer Clin. Cancer Res. 2008, 14 (5) 1310-6
8. 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 (12 Pt 1) 6387-92
9. Napper, D. H. Polymeric stabilization of colloidal dispersions; Academic Press: London, 1983; p xvi.
10. Schafer, F. Q.; Buettner, G. R. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple Free Radical Biol. Med. 2001, 30 (11) 1191-212
11. Dong, L.; Xia, S.; Wu, K.; Huang, Z.; Chen, H.; Chen, J.; Zhang, J. A pH/enzyme-responsive tumor-specific delivery system for doxorubicin Biomaterials 2010, 31 (24) 6309-16
12. Bulmus, V.; Woodward, M.; Lin, L.; Murthy, N.; Stayton, P.; Hoffman, A. A new pH-responsive and glutathione-reactive, endosomal membrane-disruptive polymeric carrier for intracellular delivery of biomolecular drugs J. Controlled Release 2003, 93 (2) 105-20
13. Garcea, G.; Neal, C. P.; Pattenden, C. J.; Steward, W. P.; Berry, D. P. Molecular prognostic markers in pancreatic cancer: a systematic review Eur. J. Cancer 2005, 41 (15) 2213-36
14. Wagner, M.; Greten, F. R.; Weber, C. K.; Koschnick, S.; Mattfeldt, T.; Deppert, W.; Kern, H.; Adler, G.; Schmid, R. M. A murine tumor progression model for pancreatic cancer recapitulating the genetic alterations of the human disease Genes Dev. 2001, 15 (3) 286-93
15. Wagner, M.; Weber, C. K.; Bressau, F.; Greten, F. R.; Stagge, V.; Ebert, M.; Leach, S. D.; Adler, G.; Schmid, R. M. Transgenic overexpression of amphiregulin induces a mitogenic response selectively in pancreatic duct cells Gastroenterology 2002, 122 (7) 1898-912
16. Leach, S. D. Mouse models of pancreatic cancer: the fur is finally flying! Cancer Cell 2004, 5 (1) 7-11
17. Xiong, H. Q. Molecular targeting therapy for pancreatic cancer Cancer Chemother. Pharmacol. 2004, 54 (Suppl 1) S69-77
18. Kimura, K.; Sawada, T.; Komatsu, M.; Inoue, M.; Muguruma, K.; Nishihara, T.; Yamashita, Y.; Yamada, N.; Ohira, M.; Hirakawa, K. Antitumor effect of trastuzumab for pancreatic cancer with high HER-2 expression and enhancement of effect by combined therapy with gemcitabine Clin. Cancer Res. 2006, 12 (16) 4925-32
19. Safran, H.; Iannitti, D.; Ramanathan, R.; Schwartz, J. D.; Steinhoff, M.; Nauman, C.; Hesketh, P.; Rathore, R.; Wolff, R.; Tantravahi, U.; Hughes, T. M.; Maia, C.; Pasquariello, T.; Goldstein, L.; King, T.; Tsai, J. Y.; Kennedy, T. Herceptin and gemcitabine for metastatic pancreatic cancers that overexpress HER-2/neu Cancer Invest. 2004, 22 (5) 706-12
20. Yu, D.; Hung, M. C. Overexpression of ErbB2 in cancer and ErbB2-targeting strategies Oncogene 2000, 19 (53) 6115-21
21. Wilson, C. A.; Cajulis, E. E.; Green, J. L.; Olsen, T. M.; Chung, Y. A.; Damore, M. A.; Dering, J.; Calzone, F. J.; Slamon, D. J. HER-2 overexpression differentially alters transforming growth factor-beta responses in luminal versus mesenchymal human breast cancer cells Breast Cancer Res. 2005, 7 (6) R1058-79
22. Cheng, J.; Teply, B. A.; Sherifi, I.; Sung, J.; Luther, G.; Gu, F. X.; Levy-Nissenbaum, E.; Radovic-Moreno, A. F.; Langer, R.; Farokhzad, O. C. Formulation of functionalized PLGA-PEG nanoparticles for in vivo targeted drug delivery Biomaterials 2007, 28 (5) 869-76
23. Song, S.; Liu, D.; Peng, J.; Sun, Y.; Li, Z.; Gu, J. R.; Xu, Y. Peptide ligand-mediated liposome distribution and targeting to EGFR expressing tumor in vivo Int. J. Pharmaceutics 2008, 363 (1-2) 155-61
24. Gu, F.; Zhang, L.; Teply, B. A.; Mann, N.; Wang, A.; Radovic-Moreno, A. F.; Langer, R.; Farokhzad, O. C. Precise engineering of targeted nanoparticles by using self-assembled biointegrated block copolymers Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (7) 2586-91
25. Townsend, S. A.; Evrony, G. D.; Gu, F. X.; Schulz, M. P.; Brown, R. H., Jr.; Langer, R. Tetanus toxin C fragment-conjugated nanoparticles for targeted drug delivery to neurons Biomaterials 2007, 28 (34) 5176-84
26. Li, Z.; Zhao, R.; Wu, X.; Sun, Y.; Yao, M.; Li, J.; Xu, Y.; Gu, J. Identification and characterization of a novel peptide ligand of epidermal growth factor receptor for targeted delivery of therapeutics FASEB J. 2005, 19 (14) 1978-85
27. van Vlerken, L. E.; Vyas, T. K.; Amiji, M. M. Poly(ethylene glycol)-modified nanocarriers for tumor-targeted and intracellular delivery Pharm. Res. 2007, 24 (8) 1405-14
28. Vonhippel, P. H.; Wong, K. Y. Neutral Salts: The Generality of Their Effects on the Stability of Macromolecular Conformations Science 1964, 145 (3632) 577-80
29. Veis, A. The physical chemistry of gelatin Int. Rev. Connect Tissue Res. 1965, 3, 113-200
30. Anand, P.; Kunnumakkara, A. B.; Newman, R. A.; Aggarwal, B. B. Bioavailability of curcumin: problems and promises Mol. Pharmaceutics 2007, 4 (6) 807-18
31. Brandau, D. T.; Jones, L. S.; Wiethoff, C. M.; Rexroad, J.; Middaugh, C. R. Thermal stability of vaccines J. Pharm. Sci. 2003, 92 (2) 218-31
32. Hiraoka, Y.; Yamashiro, H.; Yasuda, K.; Kimura, Y.; Inamoto, T.; Tabata, Y. In situ regeneration of adipose tissue in rat fat pad by combining a collagen scaffold with gelatin microspheres containing basic fibroblast growth factor Tissue Eng. 2006, 12 (6) 1475-87
33. Abate-Shen, C.; Banach-Petrosky, W. A.; Sun, X.; Economides, K. D.; Desai, N.; Gregg, J. P.; Borowsky, A. D.; Cardiff, R. D.; Shen, M. M. Nkx3.1; Pten mutant mice develop invasive prostate adenocarcinoma and lymph node metastases Cancer Res. 2003, 63 (14) 3886-90
34. Beaujeux, R.; Laurent, A.; Wassef, M.; Casasco, A.; Gobin, Y. P.; Aymard, A.; Rufenacht, D.; Merland, J. J. Trisacryl gelatin microspheres for therapeutic embolization, II: preliminary clinical evaluation in tumors and arteriovenous malformations AJNR Am. J. Neuroradiol. 1996, 17 (3) 541-8
35. Laurent, A.; Beaujeux, R.; Wassef, M.; Rufenacht, D.; Boschetti, E.; Merland, J. J. Trisacryl gelatin microspheres for therapeutic embolization, I: development and in vitro evaluation AJNR Am. J. Neuroradiol. 1996, 17 (3) 533-40
36. Soules, M. R.; Dennis, L.; Bosarge, A.; Moore, D. E. The prevention of postoperative pelvic adhesions: an animal study comparing barrier methods with dextran 70 Am. J. Obstet. Gynecol. 1982, 143 (7) 829-34
37. Azarmi, S.; Huang, Y.; Chen, H.; McQuarrie, S.; Abrams, D.; Roa, W.; Finlay, W. H.; Miller, G. G.; Lobenberg, R. Optimization of a two-step desolvation method for preparing gelatin nanoparticles and cell uptake studies in 143B osteosarcoma cancer cells J. Pharm. Pharm. Sci. 2006, 9 (1) 124-32
38. Mohanty, B.; Bohidar, H. B. Systematic of alcohol-induced simple coacervation in aqueous gelatin solutions Biomacromolecules 2003, 4 (4) 1080-6
39. Kommareddy, S.; Amiji, M. Poly(ethylene glycol)-modified thiolated gelatin nanoparticles for glutathione-responsive intracellular DNA delivery Nanomedicine 2007, 3 (1) 32-42
40. Kommareddy, S.; Amiji, M. Preparation and evaluation of thiol-modified gelatin nanoparticles for intracellular DNA delivery in response to glutathione Bioconjugate Chem. 2005, 16 (6) 1423-32
41. Xu, J.; Amiji, M. Therapeutic gene delivery and transfection in human pancreatic cancer cells using epidermal growth factor receptor-targeted gelatin nanoparticles J. Vis. Exp. 2012, 59, e3612
42. Magadala, P.; Amiji, M. Epidermal growth factor receptor-targeted gelatin-based engineered nanocarriers for DNA delivery and transfection in human pancreatic cancer cells AAPS J. 2008, 10 (4) 565-76
43. Kommareddy, S.; Amiji, M. M. Cell Transfection and Analysis Using DNA-Loaded Gelatin Nanoparticles. CSH Protocols 2008, 10.1101pdb.prot4887.
44. Kommareddy, S.; Amiji, M. M. Intracellular trafficking studies using gold-encapsulated gelatin nanoparticles. CSH Protocols 2008, 10.1101pdb.prot4886.
45. Kommareddy, S.; Amiji, M. M. Preparation and loading of gelatin nanoparticles. CSH Protocols 2008, 10.1101pdb.prot4885.
46. Kommareddy, S.; Amiji, M. Biodistribution and pharmacokinetic analysis of long-circulating thiolated gelatin nanoparticles following systemic administration in breast cancer-bearing mice J. Pharm. Sci. 2007, 96 (2) 397-407
47. Kaul, G.; Amiji, M. Biodistribution and targeting potential of poly(ethylene glycol)-modified gelatin nanoparticles in subcutaneous murine tumor model J. Drug Target. 2004, 12 (9-10) 585-91
48. Park, K.; Kim, J. H.; Nam, Y. S.; Lee, S.; Nam, H. Y.; Kim, K.; Park, J. H.; Kim, I. S.; Choi, K.; Kim, S. Y.; Kwon, I. C. Effect of polymer molecular weight on the tumor targeting characteristics of self-assembled glycol chitosan nanoparticles J. Controlled Release 2007, 122 (3) 305-14
49. McNeil, S. E. Nanoparticle therapeutics: a personal perspective Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 2009, 1 (3) 264-71
50. Berz, D.; Miner, T.; McCormack, E.; Safran, H. HER family inhibitors in pancreatic cancer: current status and future directions Expert Opin. Ther. Targets 2007, 11 (3) 337-47
51. Arteaga, C. L. The epidermal growth factor receptor: from mutant oncogene in nonhuman cancers to therapeutic target in human neoplasia J. Clin. Oncol. 2001, 19 (18 Suppl) 32S-40S
52. Landsman, M. L.; Kwant, G.; Mook, G. A.; Zijlstra, W. G. Light-absorbing properties, stability, and spectral stabilization of indocyanine green J. Appl. Physiol. 1976, 40 (4) 575-83
53. Desmettre, T.; Devoisselle, J. M.; Mordon, S. Fluorescence properties and metabolic features of indocyanine green (ICG) as related to angiography Surv. Ophthalmol. 2000, 45 (1) 15-27
54. Simmons, R.; Shephard, R. J. Does indocyanine green obey Beer's law? J. Appl. Physiol. 1971, 30 (4) 502-7
55. Gathje, J.; Steuer, R. R.; Nicholes, K. R. Stability studies on indocyanine green dye J. Appl. Physiol. 1970, 29 (2) 181-5
56. Mordon, S.; Devoisselle, J. M.; Soulie-Begu, S.; Desmettre, T. Indocyanine green: physicochemical factors affecting its fluorescence in vivo Microvasc. Res. 1998, 55 (2) 146-52
57. Maarek, J. M.; Holschneider, D. P.; Harimoto, J. Fluorescence of indocyanine green in blood: intensity dependence on concentration and stabilization with sodium polyaspartate J. Photochem. Photobiol., B 2001, 65 (2-3) 157-64
58. Saxena, V.; Sadoqi, M.; Shao, J. Polymeric nanoparticulate delivery system for Indocyanine green: biodistribution in healthy mice Int. J. Pharmaceutics 2006, 308 (1-2) 200-4
59. Altinoglu, E. I.; Russin, T. J.; Kaiser, J. M.; Barth, B. M.; Eklund, P. C.; Kester, M.; Adair, J. H. Near-infrared emitting fluorophore-doped calcium phosphate nanoparticles for in vivo imaging of human breast cancer ACS Nano 2008, 2 (10) 2075-84
60. Kong, G.; Braun, R. D.; Dewhirst, M. W. Hyperthermia enables tumor-specific nanoparticle delivery: effect of particle size Cancer Res. 2000, 60 (16) 4440-5
61. Maeda, H. The enhanced permeability and retention (EPR) effect in tumor vasculature: the key role of tumor-selective macromolecular drug targeting Adv. Enzyme Regul. 2001, 41, 189-207
62. Maeda, H.; Fang, J.; Inutsuka, T.; Kitamoto, Y. Vascular permeability enhancement in solid tumor: various factors, mechanisms involved and its implications Int. Immunopharmacol. 2003, 3 (3) 319-28
63. Perry, J. L.; Reuter, K. G.; Kai, M. P.; Herlihy, K. P.; Jones, S. W.; Luft, J. C.; Napier, M.; Bear, J. E.; DeSimone, J. M. PEGylated PRINT nanoparticles: the impact of PEG density on protein binding, macrophage association, biodistribution, and pharmacokinetics Nano Lett. 2012, 12 (10) 5304-10
64. Li, C.; Wang, C.; Yang, H.; Zhao, X.; Wei, N.; Cui, J. Liposomal topotecan formulation with a low polyethylene glycol grafting density: pharmacokinetics and antitumour activity J. Pharm. Pharmacol. 2012, 64 (3) 372-82
65. Sun, X.; Rossin, R.; Turner, J. L.; Becker, M. L.; Joralemon, M. J.; Welch, M. J.; Wooley, K. L. An assessment of the effects of shell cross-linked nanoparticle size, core composition, and surface PEGylation on in vivo biodistribution Biomacromolecules 2005, 6 (5) 2541-54
66. Larson, T. A.; Joshi, P. P.; Sokolov, K. Preventing protein adsorption and macrophage uptake of gold nanoparticles via a hydrophobic shield ACS Nano 2012, 6 (10) 9182-90
67. Moghimi, S. M.; Hunter, A. C.; Andresen, T. L. Factors controlling nanoparticle pharmacokinetics: an integrated analysis and perspective Annu. Rev. Pharmacol. Toxicol. 2012, 52, 481-503
68. Saraogi, G. K.; Gupta, P.; Gupta, U. D.; Jain, N. K.; Agrawal, G. P. Gelatin nanocarriers as potential vectors for effective management of tuberculosis Int. J. Pharmaceutics 2010, 385 (1-2) 143-9
69. Jokerst, J. V.; Lobovkina, T.; Zare, R. N.; Gambhir, S. S. Nanoparticle PEGylation for imaging and therapy Nanomedicine (London) 2011, 6 (4) 715-28
70. Alexis, F.; Pridgen, E.; Molnar, L. K.; Farokhzad, O. C. Factors affecting the clearance and biodistribution of polymeric nanoparticles Mol. Pharmaceutics 2008, 5 (4) 505-15
71. Weissig, V.; Whiteman, K. R.; Torchilin, V. P. Accumulation of protein-loaded long-circulating micelles and liposomes in subcutaneous Lewis lung carcinoma in mice Pharm. Res. 1998, 15 (10) 1552-6
72. Kommareddy, S.; Amiji, M. Antiangiogenic gene therapy with systemically administered sFlt-1 plasmid DNA in engineered gelatin-based nanovectors Cancer Gene Ther. 2007, 14 (5) 488-98
73. Kaul, G.; Amiji, M. Tumor-targeted gene delivery using poly(ethylene glycol)-modified gelatin nanoparticles: in vitro and in vivo studies Pharm. Res. 2005, 22 (6) 951-61
74. Bhavsar, M. D.; Amiji, M. M. Gastrointestinal distribution and in vivo gene transfection studies with nanoparticles-in-microsphere oral system (NiMOS) J. Controlled Release 2007, 119 (3) 339-48
75. Korc, M. Pancreatic cancer-associated stroma production Am. J. Surg. 2007, 194 (4 Suppl) S84-6