Encapsulated cells for long-term secretion of soluble VEGF receptor 1: Material optimization and simulation of ocular drug response

European Journal of Pharmaceutics and Biopharmaceutics

Volumn 95, Issue , 2015, Pages 387-397

  Kontturi, Leena Stiina ^a   Collin, Estelle C ^b   Murtomäki, Lasse ^c   Pandit, Abhay S ^b   Yliperttula, Marjo ^a   Urtti, Arto ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^c AALTO UNIVERSITY   (Finland)

Author keywords

ARPE 19 cells; Cell encapsulation; Hydrogel; Pharmacokinetic pharmacodynamic modeling; Recombinant protein; Retinal neovascularization; Vascular endothelial growth factor inhibitor

Indexed keywords

COLLAGEN; HYALURONIC ACID; SOLUBLE VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR 1; UNCLASSIFIED DRUG; VASCULOTROPIN INHIBITOR; VASCULOTROPIN RECEPTOR 1; ANGIOGENESIS INHIBITOR; HYDROGEL;

ANTIANGIOGENIC THERAPY; ARTICLE; CELL DENSITY; CELL ENCAPSULATION; CELL ENGINEERING; CELL VIABILITY; CONTROLLED STUDY; CROSS LINKING; DRUG DELIVERY SYSTEM; DRUG RESPONSE; GENETIC ENGINEERING; HUMAN; HUMAN CELL; HYDROGEL; MEASUREMENT; PHARMACODYNAMICS; PROTEIN SECRETION; PROTEIN STRUCTURE; RETINA NEOVASCULARIZATION; SIMULATION; BIOLOGICAL MODEL; CELL LINE; CELL SURVIVAL; CYTOLOGY; DRUG ADMINISTRATION; PATHOLOGY; PHYSIOLOGY; RETINAL DISEASES; RETINAL PIGMENT EPITHELIUM; SECRETION (PROCESS); TIME FACTOR;

ANGIOGENESIS INHIBITORS; CELL LINE; CELL SURVIVAL; DRUG ADMINISTRATION SCHEDULE; DRUG DELIVERY SYSTEMS; HUMANS; HYDROGELS; MODELS, BIOLOGICAL; RETINAL DISEASES; RETINAL PIGMENT EPITHELIUM; TIME FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

EID: 84943808613     PISSN: 09396411     EISSN: 18733441     Source Type: Journal    
DOI: 10.1016/j.ejpb.2014.10.005     Document Type: Article

References (77)

1. C.M. Andreoli, and J.W. Miller Anti-vascular endothelial growth factor therapy for ocular neovascular disease Curr. Opin. Ophthalmol. 18 6 2007 502 508
2. M.V. Emerson, and A.K. Lauer Emerging therapies for the treatment of neovascular age-related macular degeneration and diabetic macular edema BioDrugs 21 4 2007 245 257
3. T.A. Ciulla, and P.J. Rosenfeld Antivascular endothelial growth factor therapy for neovascular age-related macular degeneration Curr. Opin. Ophthalmol. 20 3 2009 158 165 10.1097/ICU.0b013e32832d25b3
4. K.M. Farjo, and J.X. Ma The potential of nanomedicine therapies to treat neovascular disease in the retina J. Angiogenes Res. 8 2 2010 21 10.1186/2040-2384-2-21
5. E.M. Del Amo, and A. Urtti Current and future ophthalmic drug delivery systems. A shift to the posterior segment Drug Discov. Today 13 3-4 2008 135 143 10.1016/j.drudis.2007.11.002
6. Y.E. Choonara, V. Pillay, M.P. Danckwerts, T.R. Carmichael, and L.C. du Toit A review of implantable intravitreal drug delivery technologies for the treatment of posterior segment eye diseases J. Pharm. Sci. 99 5 2010 2219 2239 10.1002/jps.21987
7. E.S. Gragoudas, A.P. Adamis, E.T. Cunningham, M. Feinsod, and D.R. Guyer Pegaptanib for neovascular age-related macular degeneration N. Engl. J. Med. 351 2004 2805 2816
8. R.L. Avery, D.J. Pieramici, M.D. Rabena, A.A. Castellarin, M.A. Nasir, and M.J. Giust Intravitreal bevacizumab (Avastin) for neovascular age-related macular degeneration Ophthalmology 113 3 2006 363 372
9. P.J. Rosenfeld, D.M. Brown, J.S. Heier, D.S. Boyer, P.K. Kaiser, C.Y. Chung, R.Y. Kim, and MARINA Study Group Ranibizumab for neovascular age-related macular degeneration N. Engl. J. Med. 355 14 2006 1419 1431
10. J.A. Dixon, S.C. Oliver, J.L. Olson, and N. Mandava VEGF Trap-Eye for the treatment of neovascular age-related macular degeneration Expert Opin. Invest. Drugs 18 10 2009 1573 1580 10.1517/13543780903201684
11. F.T. Wu, M.O. Stefanini, F. Mac Gabhann, C.D. Kontos, B.H. Annex, and A.S. Popel A systems biology perspective on sVEGFR1: its biological function, pathogenic role and therapeutic use J. Cell. Mol. Med. 14 3 2010 528 552 10.1111/j.1582-4934.2009.00941
12. F. Lim, and A.M. Sun Microencapsulated islets as bioartificial endocrine pancreas Science 210 4472 1980 908 910
13. E.H. Nafea, A. Marson, L.A. Poole-Warren, and P.J. Martens Immunoisolating semi-permeable membranes for cell encapsulation: focus on hydrogels J. Control. Release 154 2 2011 110 122 10.1016/j.jconrel.2011.04.022
14. H. Uludag, P. De Vos, and P.A. Tresco Technology of mammalian cell encapsulation Adv. Drug Deliv. Rev. 42 1-2 2000 29 64
15. A. Acarregui, A. Murua, J.L. Pedraz, G. Orive, and R.M. Hernández A perspective on bioactive cell microencapsulation BioDrugs 26 5 2012 283 301 10.2165/11632640-000000000-00000
16. W. Tao, R. Wen, M.B. Goddard, S.D. Sherman, P.J. O'Rourke, P.F. Stabila, W.J. Bell, B.J. Dean, and et al. Encapsulated cell-based delivery of CNTF reduces photoreceptor degeneration in animal models of retinitis pigmentosa Invest. Ophthalmol. Vis. Sci. 43 10 2002 3292 3298
17. C.G. Thanos, W.J. Bell, P. O'Rourke, K. Kauper, S. Sherman, P. Stabila, and W. Tao Sustained secretion of ciliary neurotrophic factor to the vitreous, using the encapsulated cell therapy-based NT-501 intraocular device Tissue Eng. 10 11-12 2004 1617 1622
18. P.A. Sieving, R.C. Caruso, W. Tao, H.R. Coleman, D.J. Thompson, K.R. Fullmer, and R.A. Bush Ciliary neurotrophic factor (CNTF) for human retinal degeneration: phase I trial of CNTF delivered by encapsulated cell intraocular implants Proc. Natl. Acad. Sci. U.S.A. 103 10 2006 3896 3901
19. K. Zhang, J.J. Hopkins, J.S. Heier, D.G. Birch, L.S. Halperin, T.A. Albini, D.M. Brown, G.J. Jaffe, and et al. Ciliary neurotrophic factor delivered by encapsulated cell intraocular implants for treatment of geographic atrophy in age-related macular degeneration Proc. Natl. Acad. Sci. U.S.A. 108 15 2011 6241 6245 10.1073/pnas.101898710
20. K. Kauper, C. McGovern, S. Sherman, P. Heatherton, R. Rapoza, P. Stabila, B. Dean, A. Lee, and et al. Two-year intraocular delivery of ciliary neurotrophic factor by encapsulated cell technology implants in patients with chronic retinal degenerative diseases Invest. Ophthalmol. Vis. Sci. 53 12 2012 7484 7491 10.1167/iovs.12-9970
21. R.H. Li Materials for immunoisolated cell transplantation Adv. Drug Deliv. Rev. 33 1-2 1998 87 109
22. S. Lahooti, and M.V. Sefton Effect of an immobilization matrix and capsule membrane permeability on the viability of encapsulated HEK cells Biomaterials 21 10 2000 987 995
23. T. Taguchi, L. Xu, H. Kobayashi, A. Taniguchi, K. Kataoka, and J. Tanaka Encapsulation of chondrocytes in injectable alkali-treated collagen gels prepared using poly(ethylene glycol)-based 4-armed star polymer Biomaterials 26 11 2005 1247 1252
24. E.C. Collin, S. Grad, D.I. Zeugolis, C.S. Vinatier, J.R. Clouet, J.J. Guicheux, P. Weiss, M. Alini, and et al. An injectable vehicle for nucleus pulposus cell-based therapy Biomaterials 32 11 2011 2862 2870 10.1016/j.biomaterials.2011.01.018
25. L.S. Kontturi, E. Järvinen, V. Muhonen, E.C. Collin, A.S. Pandit, I. Kiviranta, M. Yliperttula, and A. Urtti An injectable type II collagen/hyaluronic acid/TGF1 hydrogel vehicle for chondrocyte delivery in cartilage tissue engineering Drug Deliv. Transl. Res. 2014 (January)
26. L.S. Kontturi, M. Yliperttula, P. Toivanen, A. Määttä, A.M. Määttä, and A. Urtti A laboratory-scale device for the straightforward production of uniform, small sized cell microcapsules with long-term cell viability J. Control. Release 152 3 2011 376 381 10.1016/j.jconrel.2011.03.005
27. S.S. Lee, C. Ghosn, Z. Yu, L.C. Zacharias, H. Kao, C. Lanni, N. Abdelfattah, B. Kuppermann, and et al. Vitreous VEGF clearance is increased after vitrectomy Invest. Ophthalmol. Vis. Sci. 51 4 2010 2135 2138 10.1167/iovs.09-3582
28. M. Funk, D. Karl, M. Georgopoulos, T. Benesch, S. Sacu, K. Polak, G.J. Zlabinger, and U. Schmidt-Erfurth Neovascular age-related macular degeneration: intraocular cytokines and growth factors and the influence of therapy with ranibizumab Ophthalmology 116 12 2009 2393 2399 10.1016/j.ophtha.2009.05.039
29. W.M. Chan, T.Y. Lai, K.P. Chan, H. Li, D.T. Liu, D.S. Lam, and C.P. Pang Changes in aqueous vascular endothelial growth factor and pigment epithelial-derived factor levels following intravitreal bevacizumab injections for choroidal neovascularization secondary to age-related macular degeneration or pathologic myopia Retina 28 9 2008 1308 1313 10.1097/IAE.0b013e31818358b2
30. O. Sawada, T. Miyake, M. Kakinoki, T. Sawada, H. Kawamura, and M. Ohji Aqueous vascular endothelial growth factor after intravitreal injection of pegaptanib or ranibizumab in patients with age-related macular degeneration Retina 30 7 2010 1034 1038 10.1097/IAE.0b013e3181ce74c
31. X. Wang, T. Sawada, M. Kakinoki, T. Miyake, H. Kawamura, Y. Saishin, P. Liu, and M. Ohji Aqueous vascular endothelial growth factor and ranibizumab concentrations after monthly and bimonthly intravitreal injections of ranibizumab for age-related macular degeneration Graefes Arch. Clin. Exp. Ophthalmol. 2013 (November 7)
32. M.I. Roh, S.J. Lim, J.M. Ahn, J.B. Lim, and O.W. Kwon Concentration of cytokines in age-related macular degeneration after consecutive intravitreal bevacizumab injection Graefes Arch. Clin. Exp. Ophthalmol. 248 5 2010 635 640 10.1007/s00417-009-1254-8
33. H. Funatsu, H. Yamashita, H. Noma, T. Mimura, S. Nakamura, K. Sakata, and S. Hori Aqueous humor levels of cytokines are related to vitreous levels and progression of diabetic retinopathy in diabetic patients Graefes Arch. Clin. Exp. Ophthalmol. 243 1 2005 3 8
34. H. Noma, H. Funatsu, T. Mimura, S. Harino, and S. Hori Aqueous humor levels of vasoactive molecules correlate with vitreous levels and macular edema in central retinal vein occlusion Eur. J. Ophthalmol. 20 2 2010 402 409
35. L.P. Aiello, R.L. Avery, P.G. Arrigg, B.A. Keyt, H.D. Jampel, S.T. Shah, L.R. Pasquale, H. Thieme, and et al. Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders N. Engl. J. Med. 331 22 1994 1480 1487
36. S.M. Ecker, J.C. Hines, S.M. Pfahler, and B.M. Glaser Aqueous cytokine and growth factor levels do not reliably reflect those levels found in the vitreous Mol. Vis. 17 2011 2856 2863
37. S.J. Bakri, M.R. Snyder, J.M. Reid, J.S. Pulido, and R.J. Singh Pharmacokinetics of intravitreal bevacizumab (Avastin) Ophthalmology 114 5 2007 855 859
38. J.B. Christoforidis, M.M. Carlton, M.V. Knopp, and G.H. Hinkle PET/CT imaging of I-124-radiolabeled bevacizumab and ranibizumab after intravitreal injection in a rabbit model Invest. Ophthalmol. Vis. Sci. 52 8 2011 5899 5903 10.1167/iovs.10-6862
39. S.J. Bakri, M.R. Snyder, J.M. Reid, J.S. Pulido, M.K. Ezzat, and R.J. Singh Pharmacokinetics of intravitreal ranibizumab (Lucentis) Ophthalmology 114 12 2007 2179 2182
40. J.B. Christoforidis, M.M. Williams, S. Kothandaraman, K. Kumar, F.J. Epitropoulos, and M.V. Knopp Pharmacokinetic properties of intravitreal I-124-aflibercept in a rabbit model using PET/CT Curr. Eye Res. 37 12 2012 1171 1174 10.3109/02713683.2012.727521
41. H. Kim, K.G. Csaky, C.C. Chan, P.M. Bungay, R.J. Lutz, R.L. Dedrick, P. Yuan, J. Rosenberg, and et al. The pharmacokinetics of rituximab following an intravitreal injection Exp. Eye Res. 82 5 2006 760 766
42. M. Brar, L. Cheng, R. Yuson, F. Mojana, W.R. Freeman, and P.S. Gill Ocular safety profile and intraocular pharmacokinetics of an antagonist of EphB4/EphrinB2 signalling Br. J. Ophthalmol. 94 12 2010 1668 1673 10.1136/bjo.2010.182881
43. H. Li, N. Lei, M. Zhang, Y. Li, H. Xiao, and X. Hao Pharmacokinetics of a long-lasting anti-VEGF fusion protein in rabbit Exp. Eye Res. 97 1 2012 154 159 10.1016/j.exer.2011.09.002
44. F.T. Wu, M.O. Stefanini, F. Mac Gabhann, and A.S. Popel A compartment model of VEGF distribution in humans in the presence of soluble VEGF receptor-1 acting as a ligand trap PLoS ONE 4 4 2009 e5108 10.1371/journal.pone.0005108
45. N. Papadopoulos, J. Martin, Q. Ruan, A. Rafique, M.P. Rosconi, E. Shi, E.A. Pyles, G.D. Yancopoulos, and et al. Binding and neutralization of vascular endothelial growth factor (VEGF) and related ligands by VEGF Trap, ranibizumab and bevacizumab Angiogenesis 15 2 2012 171 185 10.1007/s10456-011-9249-6
46. F. Mac Gabhann, and A.S. Popel Model of competitive binding of vascular endothelial growth factor and placental growth factor to VEGF receptors on endothelial cells Am. J. Physiol. Heart Circ. Physiol. 286 1 2004 H153 H164
47. J.L. Drury, and D.J. Mooney Hydrogels for tissue engineering: scaffold design variables and applications Biomaterials 24 24 2003 4337 4351
48. J.J. Schmidt, J. Rowley, and H.J. Kong Hydrogels used for cell-based drug delivery J. Biomed. Mater. Res. A 87 4 2008 1113 1122 10.1002/jbm.a.32287
49. C.G. Thanos, and D.F. Emerich On the use of hydrogels in cell encapsulation and tissue engineering system Adv. Drug Deliv. Rev. 62 7-8 2010 711 730
50. R.H. Li, D.H. Altreuter, and F.T. Gentile Transport characterization of hydrogel matrices for cell encapsulation Biotechnol. Bioeng. 50 4 1996 365 373
51. K.C. Dunn, A.E. Aotaki-Keen, F.R. Putkey, and L.M. Hjelmeland ARPE-19, a human retinal pigment epithelial cell line with differentiated properties Exp. Eye Res. 62 2 1996 155 169
52. J. Wikström, M. Elomaa, H. Syväjärvi, J. Kuokkanen, M. Yliperttula, P. Honkakoski, and A. Urtti Alginate-based microencapsulation of retinal pigment epithelial cell line for cell therapy Biomaterials 29 7 2008 869 876
53. L. Fjord-Larsen, P. Kusk, J. Tornøe, B. Juliusson, M. Torp, C.R. Bjarkam, M.S. Nielsen, A. Handberg, and et al. Long-term delivery of nerve growth factor by encapsulated cell biodelivery in the Göttingen minipig basal forebrain Mol. Ther. 18 12 2010 2164 2172 10.1038/mt.2010.154
54. L. Fjord-Larsen, P. Kusk, M. Torp, J.C.H. Sørensen, Ettru Kaare, C.R. Bjarkam, and et al. Encapsulated cell biodelivery of transposon-mediated high-dose NGF to the Göttingen mini pig basal forebrain Open Tissue Eng. Regener. Med. J. 5 2012 35 42
55. L.U. Wahlberg, G. Lind, P.M. Almqvist, P. Kusk, J. Tornøe, B. Juliusson, M. Söderman, E. Selldén, and et al. Targeted delivery of nerve growth factor via encapsulated cell biodelivery in Alzheimer disease: a technology platform for restorative neurosurgery J. Neurosurg. 117 2 2012 340 347 10.3171/2012.2.JNS11714
56. J.W. Streilein Ocular immune privilege: the eye takes a dim but practical view of immunity and inflammation J. Leukoc. Biol. 74 2 2003 179 185
57. J.W. Streilein Ocular immune privilege: therapeutic opportunities from an experiment of nature Nat. Rev. Immunol. 3 11 2003 879 889
58. A.W. Taylor Ocular immune privilege Eye 23 2009 1885 1889 10.1038/eye.2008.382
59. T. Lavé, N. Parrott, H.P. Grimm, A. Fleury, and M. Reddy Challenges and opportunities with modelling and simulation in drug discovery and drug development Xenobiotica 37 10-11 2007 1295 1310
60. I. Rajman PK/PD modelling and simulations: utility in drug development Drug Discov. Today 13 7-8 2008 341 346 10.1016/j.drudis.2008.01.003
61. M.W. Stewart Predicted biologic activity of intravitreal bevacizumab Retina 27 9 2007 1196 1200
62. M.W. Stewart, and P.J. Rosenfeld Predicted biological activity of intravitreal VEGF Trap Br. J. Ophthalmol. 92 5 2008 667 668 10.1136/bjo.2007.134874
63. M.W. Stewart, P.J. Rosenfeld, F.M. Penha, F. Wang, Z. Yehoshua, E. Bueno-Lopez, and P.F. Lopez Pharmacokinetic rationale for dosing every 2 weeks versus 4 weeks with intravitreal ranibizumab, bevacizumab, and aflibercept (vascular endothelial growth factor Trap-eye) Retina 32 3 2012 434 457 10.1097/IAE.0B013E31822C290F
64. Y. Chen, C. Wiesmann, G. Fuh, B. Li, H.W. Christinger, P. McKay, A.M. de Vos, and H.B. Lowman Selection and analysis of an optimized anti-VEGF antibody: crystal structure of an affinity-matured Fab in complex with antigen J. Mol. Biol. 293 4 1999 865 881
65. J. Holash, S. Davis, N. Papadopoulos, S.D. Croll, L. Ho, M. Russell, P. Boland, R. Leidich, and et al. VEGF-Trap: a VEGF blocker with potent antitumor effects Proc. Natl. Acad. Sci. U.S.A. 99 17 2002 11393 11398
66. S.C. Makrides Components of vectors for gene transfer and expression in mammalian cells Protein Expr. Purif. 17 2 1999 183 202
67. F.M. Wurm Production of recombinant protein therapeutics in cultivated mammalian cells Nat. Biotechnol. 22 11 2004 1393 1398
68. A. Rita Costa, M. Elisa Rodrigues, M. Henriques, J. Azeredo, and R. Oliveira Guidelines to cell engineering for monoclonal antibody production Eur. J. Pharm. Biopharm. 74 2 2010 127 138 10.1016/j.ejpb.2009.10.00
69. K.M. Sampat, and S.J. Garg Complications of intravitreal injections Curr. Opin. Ophthalmol. 21 3 2010 178 183 10.1097/ICU.0b013e328338679a
70. C.I. Sinapis, J.G. Routsias, A.I. Sinapis, D.I. Sinapis, G.D. Agrogiannis, A. Pantopoulou, S.E. Theocharis, S. Baltatzis, and et al. Pharmacokinetics of intravitreal bevacizumab (Avastin®) in rabbits Clin Ophthalmol. 5 2011 697 704 10.2147/OPTH.S19555
71. Y. Wang, D. Fei, M. Vanderlaan, and A. Song Biological activity of bevacizumab, a humanized anti-VEGF antibody in vitro Angiogenesis 7 4 2004 335 345
72. R.J. Campbell, C.M. Bell, E de L. Campbell, and S.S. Gill Systemic effects of intravitreal vascular endothelial growth factor inhibitors Curr. Opin. Ophthalmol. 24 3 2013 197 204 10.1097/ICU.0b013e32835f8bbe
73. B. Salmons, M. Löhr, and W.H. Günzburg Treatment of inoperable pancreatic carcinoma using a cell-based local chemotherapy: results of a phase I/II clinical trial J. Gastroenterol. 38 Suppl. 15 2003 78 84
74. J. Bloch, A.C. Bachoud-Lévi, N. Déglon, J.P. Lefaucheur, L. Winkel, S. Palfi, J.P. Nguyen, C. Bourdet, and et al. Neuroprotective gene therapy for Huntington's disease, using polymer-encapsulated cells engineered to secrete human ciliary neurotrophic factor: results of a phase I study Hum. Gene Ther. 15 10 2004 968 975
75. B. Buder, M. Alexander, R. Krishnan, D.W. Chapman, and J.R.T. Lakey Encapsulated islet transplantation: strategies and clinical trials Immune Netw. 13 6 2013 235 239 10.4110/in.2013.13.6.235
76. E.S. Farag, H.V. Vinters, and J. Bronstein Pathologic findings in retinal pigment epithelial cell implantation for Parkinson disease Neurology 73 14 2009 1095 1102 10.1212/WNL.0b013e3181bbff1c
77. R.E. Gross, R.L. Watts, R.A. Hauser, R.A. Bakay, H. Reichmann, R. von Kummer, W.G. Ondo, E. Reissig, and et al. Intrastriatal transplantation of microcarrier-bound human retinal pigment epithelial cells versus sham surgery in patients with advanced Parkinson's disease: a double-blind, randomised, controlled trial Lancet Neurol. 10 6 2011 509 519 10.1016/S1474-4422(11)70097-7