Fibrin As a Scaffold for Delivery of GDNF Overexpressing Stem Cells to the Adult Rat Brain

ACS Biomaterials Science and Engineering

Volumn 1, Issue 7, 2015, Pages 559-566

  Moloney, Teresa C ^a,b   Ní Fhlathartaigh, Mary ^a   Kulkarni, Mangesh ^a   Pandit, Abhay ^a   Dowd, Eilís ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

biomaterial; fibrin; neurodegeneration; neurotrophic factors; stem cells

Indexed keywords

FIBRIN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; NEUROTROPHIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN BINDING; ARTICLE; BIOCOMPATIBILITY; BIODEGRADABILITY; BONE MARROW DERIVED MESENCHYMAL STEM CELL; BRAIN TISSUE; CELL SURVIVAL; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; ENGRAFTMENT; FIBRIN POLYMERIZATION; IMMUNE RESPONSE; MALE; MESENCHYMAL STEM CELL; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STEM CELL; STEM CELL TRANSPLANTATION; SURVIVAL FACTOR; TISSUE SCAFFOLD;

EID: 84969130578     PISSN: None     EISSN: 23739878     Source Type: Journal    
DOI: 10.1021/acsbiomaterials.5b00049     Document Type: Article

References (58)

1. Olesen, J.; Gustavsson, A.; Svensson, M.; Wittchen, H. U.; Jonsson, B.; group, C. s.; European Brain, C. The economic cost of brain disorders in Europe Eur. J. Neurol 2012, 19, 155-162 10.1111/j.1468-1331.2011.03590.x
2. Kowal, S. L.; Dall, T. M.; Chakrabarti, R.; Storm, M. V.; Jain, A. The current and projected economic burden of Parkinson's disease in the United States Mov. Disord. 2013, 28, 311-318 10.1002/mds.25292
3. Johnson, S. J.; Diener, M. D.; Kaltenboeck, A.; Birnbaum, H. G.; Siderowf, A. D. An economic model of Parkinson's disease: implications for slowing progression in the United States Mov. Disord. 2013, 28, 319-326 10.1002/mds.25328
4. Lin, L. F.; Doherty, D. H.; Lile, J. D.; Bektesh, S.; Collins, F. GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons Science 1993, 260, 1130-1132 10.1126/science.8493557
5. Kirik, D.; Rosenblad, C.; Bjorklund, A. Preservation of a functional nigrostriatal dopamine pathway by GDNF in the intrastriatal 6-OHDA lesion model depends on the site of administration of the trophic factor Eur. J. Neurosci 2000, 12, 3871-3882 10.1046/j.1460-9568.2000.00274.x
6. Rosenblad, C.; Kirik, D.; Devaux, B.; Moffat, B.; Phillips, H. S.; Bjorklund, A. Protection and regeneration of nigral dopaminergic neurons by neurturin or GDNF in a partial lesion model of Parkinson's disease after administration into the striatum or the lateral ventricle Eur. J. Neurosci 1999, 11, 1554-1566 10.1046/j.1460-9568.1999.00566.x
7. Sullivan, A. M.; Opacka-Juffry, J.; Blunt, S. B. Long-term protection of the rat nigrostriatal dopaminergic system by glial cell line-derived neurotrophic factor against 6-hydroxydopamine in vivo Eur. J. Neurosci 1998, 10, 57-63 10.1046/j.1460-9568.1998.00016.x
8. Winkler, C.; Sauer, H.; Lee, C. S.; Bjorklund, A. Short-term GDNF treatment provides long-term rescue of lesioned nigral dopaminergic neurons in a rat model of Parkinson's disease J. Neurosci. 1996, 16, 7206-7215
9. Gill, S. S.; Patel, N. K.; Hotton, G. R.; O'Sullivan, K.; McCarter, R.; Bunnage, M.; Brooks, D. J.; Svendsen, C. N.; Heywood, P. Direct brain infusion of glial cell line-derived neurotrophic factor in Parkinson disease Nat. Med. 2003, 9, 589-595 10.1038/nm850
10. Love, S.; Plaha, P.; Patel, N. K.; Hotton, G. R.; Brooks, D. J.; Gill, S. S. Glial cell line-derived neurotrophic factor induces neuronal sprouting in human brain Nat. Med. 2005, 11, 703-704 10.1038/nm0705-703
11. Slevin, J. T.; Gerhardt, G. A.; Smith, C. D.; Gash, D. M.; Kryscio, R.; Young, B. Improvement of bilateral motor functions in patients with Parkinson disease through the unilateral intraputaminal infusion of glial cell line-derived neurotrophic factor J. Neurosurg. 2005, 102, 216-222 10.3171/jns.2005.102.2.0216
12. Lang, A. E.; Gill, S.; Patel, N. K.; Lozano, A.; Nutt, J. G.; Penn, R.; Brooks, D. J.; Hotton, G.; Moro, E.; Heywood, P.; Brodsky, M. A.; Burchiel, K.; Kelly, P.; Dalvi, A.; Scott, B.; Stacy, M.; Turner, D.; Wooten, V. G.; Elias, W. J.; Laws, E. R.; Dhawan, V.; Stoessl, A. J.; Matcham, J.; Coffey, R. J.; Traub, M. Randomized controlled trial of intraputamenal glial cell line-derived neurotrophic factor infusion in Parkinson disease Ann. Neurol. 2006, 59, 459-466 10.1002/ana.20737
13. Sherer, T. B.; Fiske, B. K.; Svendsen, C. N.; Lang, A. E.; Langston, J. W. Crossroads in GDNF therapy for Parkinson's disease Mov. Disord. 2006, 21, 136-141 10.1002/mds.20861
14. Bartholomew, A.; Sturgeon, C.; Siatskas, M.; Ferrer, K.; McIntosh, K.; Patil, S.; Hardy, W.; Devine, S.; Ucker, D.; Deans, R.; Moseley, A.; Hoffman, R. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo Exp. Hematol. 2002, 30, 42-48 10.1016/S0301-472X(01)00769-X
15. Di Nicola, M.; Carlo-Stella, C.; Magni, M.; Milanesi, M.; Longoni, P. D.; Matteucci, P.; Grisanti, S.; Gianni, A. M. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli Blood 2002, 99, 3838-3843 10.1182/blood.V99.10.3838
16. Moloney, T. C.; Dockery, P.; Windebank, A. J.; Barry, P. B.; Howard, L.; Dowd, E. Survival and immunogenicity of mesenchymal stem cells from the green fluorescent protein transgenic rat in the adult rat brain Neurorehab Neural Re 2010, 24, 645 10.1177/1545968309357745
17. Ohtaki, H.; Ylostalo, J. H.; Foraker, J. E.; Robinson, A. P.; Reger, R. L.; Shioda, S.; Prockop, D. J. Stem/progenitor cells from bone marrow decrease neuronal death in global ischemia by modulation of inflammatory/immune responses Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 14638-14643 10.1073/pnas.0803670105
18. Rossignol, J.; Boyer, C.; Thinard, R.; Remy, S.; Dugast, A. S.; Dubayle, D.; Dey, N. D.; Boeffard, F.; Delecrin, J.; Heymann, D.; Vanhove, B.; Anegon, I.; Naveilhan, P.; Dunbar, G. L.; Lescaudron, L. Mesenchymal stem cells induce a weak immune response in the rat striatum after allo or xenotransplantation J. Cell. Mol. Med. 2009, 13, 2547-2558 10.1111/j.1582-4934.2009.00657.x
19. Bartmann, C.; Rohde, E.; Schallmoser, K.; Purstner, P.; Lanzer, G.; Linkesch, W.; Strunk, D. Two steps to functional mesenchymal stromal cells for clinical application Transfusion 2007, 47, 1426-1435 10.1111/j.1537-2995.2007.01219.x
20. Digirolamo, C. M.; Stokes, D.; Colter, D.; Phinney, D. G.; Class, R.; Prockop, D. J. Propagation and senescence of human marrow stromal cells in culture: a simple colony-forming assay identifies samples with the greatest potential to propagate and differentiate Br. J. Haematol. 1999, 107, 275-281 10.1046/j.1365-2141.1999.01715.x
21. Pittenger, M. F.; Mackay, A. M.; Beck, S. C.; Jaiswal, R. K.; Douglas, R.; Mosca, J. D.; Moorman, M. A.; Simonetti, D. W.; Craig, S.; Marshak, D. R. Multilineage potential of adult human mesenchymal stem cells Science 1999, 284, 143-147 10.1126/science.284.5411.143
22. Zhang, Z.; Wang, X.; Wang, S. Isolation and characterization of mesenchymal stem cells derived from bone marrow of patients with Parkinson's disease In Vitro Cell. Dev. Biol.: Anim. 2008, 44, 169-177 10.1007/s11626-008-9093-1
23. Venkataramana, N. K.; Kumar, S. K.; Balaraju, S.; Radhakrishnan, R. C.; Bansal, A.; Dixit, A.; Rao, D. K.; Das, M.; Jan, M.; Gupta, P. K.; Totey, S. M. Open-labeled study of unilateral autologous bone-marrow-derived mesenchymal stem cell transplantation in Parkinson's disease Transl Res. 2010, 155, 62-70 10.1016/j.trsl.2009.07.006
24. Moloney, T. C.; Rooney, G. E.; Barry, F. P.; Howard, L.; Dowd, E. Potential of rat bone marrow-derived mesenchymal stem cells as vehicles for delivery of neurotrophins to the Parkinsonian rat brain Brain Res. 2010, 1359, 33-43 10.1016/j.brainres.2010.08.040
25. Hoban, D. B.; Newland, B.; Moloney, T. C.; Howard, L.; Pandit, A.; Dowd, E. The reduction in immunogenicity of neurotrophin overexpressing stem cells after intra-striatal transplantation by encapsulation in an in situ gelling collagen hydrogel Biomaterials 2013, 34, 9420-9429 10.1016/j.biomaterials.2013.08.073
26. Ren, Z.; Wang, J.; Wang, S.; Zou, C.; Li, X.; Guan, Y.; Chen, Z.; Zhang, Y. A. Autologous transplantation of GDNF-expressing mesenchymal stem cells protects against MPTP-induced damage in cynomolgus monkeys Sci. Rep. 2013, 3, 2786 10.1038/srep02786
27. Martino, M. M.; Briquez, P. S.; Ranga, A.; Lutolf, M. P.; Hubbell, J. A. Heparin-binding domain of fibrin(ogen) binds growth factors and promotes tissue repair when incorporated within a synthetic matrix Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 4563-4568 10.1073/pnas.1221602110
28. Moore, A. M.; Wood, M. D.; Chenard, K.; Hunter, D. A.; Mackinnon, S. E.; Sakiyama-Elbert, S. E.; Borschel, G. H. Controlled delivery of glial cell line-derived neurotrophic factor enhances motor nerve regeneration Journal of hand surgery 2010, 35, 2008-2017 10.1016/j.jhsa.2010.08.016
29. Taylor, S. J.; McDonald, J. W., 3rd; Sakiyama-Elbert, S. E. Controlled release of neurotrophin-3 from fibrin gels for spinal cord injury J. Controlled Release 2004, 98, 281-294 10.1016/j.jconrel.2004.05.003
30. Taylor, S. J.; Rosenzweig, E. S.; McDonald, J. W., 3rd; Sakiyama-Elbert, S. E. Delivery of neurotrophin-3 from fibrin enhances neuronal fiber sprouting after spinal cord injury J. Controlled Release 2006, 113, 226-235 10.1016/j.jconrel.2006.05.005
31. Wood, M. D.; MacEwan, M. R.; French, A. R.; Moore, A. M.; Hunter, D. A.; Mackinnon, S. E.; Moran, D. W.; Borschel, G. H.; Sakiyama-Elbert, S. E. Fibrin matrices with affinity-based delivery systems and neurotrophic factors promote functional nerve regeneration Biotechnol. Bioeng. 2010, 106, 970-979 10.1002/bit.22766
32. Wood, M. D.; Moore, A. M.; Hunter, D. A.; Tuffaha, S.; Borschel, G. H.; Mackinnon, S. E.; Sakiyama-Elbert, S. E. Affinity-based release of glial-derived neurotrophic factor from fibrin matrices enhances sciatic nerve regeneration Acta Biomater. 2009, 5, 959-968 10.1016/j.actbio.2008.11.008
33. Wood, M. D.; Sakiyama-Elbert, S. E. Release rate controls biological activity of nerve growth factor released from fibrin matrices containing affinity-based delivery systems J. Biomed. Mater. Res., Part A 2008, 84, 300-312 10.1002/jbm.a.31269
34. Breen, A.; Dockery, P.; O'Brien, T.; Pandit, A. Fibrin scaffold promotes adenoviral gene transfer and controlled vector delivery J. Biomed. Mater. Res., Part A 2009, 89, 876-884 10.1002/jbm.a.32039
35. Breen, A.; O'Brien, T.; Pandit, A. Fibrin as a delivery system for therapeutic drugs and biomolecules Tissue Eng., Part B 2009, 15, 201-214 10.1089/ten.teb.2008.0527
36. Breen, A.; Strappe, P.; Kumar, A.; O'Brien, T.; Pandit, A. Optimization of a fibrin scaffold for sustained release of an adenoviral gene vector J. Biomed. Mater. Res., Part A 2006, 78, 702-708 10.1002/jbm.a.30735
37. Breen, A. M.; Dockery, P.; O'Brien, T.; Pandit, A. S. The use of therapeutic gene eNOS delivered via a fibrin scaffold enhances wound healing in a compromised wound model Biomaterials 2008, 29, 3143-3151 10.1016/j.biomaterials.2008.04.020
38. Kulkarni, M.; Breen, A.; Greiser, U.; O'Brien, T.; Pandit, A. Fibrin-lipoplex system for controlled topical delivery of multiple genes Biomacromolecules 2009, 10, 1650-1654 10.1021/bm900248n
39. Kulkarni, M.; O'Loughlin, A.; Vazquez, R.; Mashayekhi, K.; Rooney, P.; Greiser, U.; O'Toole, E.; O'Brien, T.; Malagon, M. M.; Pandit, A. Use of a fibrin-based system for enhancing angiogenesis and modulating inflammation in the treatment of hyperglycemic wounds Biomaterials 2014, 35, 2001-2010 10.1016/j.biomaterials.2013.11.003
40. Kulkarni, M. M.; Greiser, U.; O'Brien, T.; Pandit, A. A temporal gene delivery system based on fibrin microspheres Mol. Pharmaceutics 2011, 8, 439-446 10.1021/mp100295z
41. Johnson, P. J.; Tatara, A.; McCreedy, D. A.; Shiu, A.; Sakiyama-Elbert, S. E. Tissue-engineered fibrin scaffolds containing neural progenitors enhance functional recovery in a subacute model of SCI Soft Matter 2010, 6, 5127-5137 10.1039/c0sm00173b
42. Johnson, P. J.; Tatara, A.; Shiu, A.; Sakiyama-Elbert, S. E. Controlled release of neurotrophin-3 and platelet-derived growth factor from fibrin scaffolds containing neural progenitor cells enhances survival and differentiation into neurons in a subacute model of SCI Cell transplantation 2010, 19, 89-101 10.3727/096368909X477273
43. Manning, C. N.; Schwartz, A. G.; Liu, W.; Xie, J.; Havlioglu, N.; Sakiyama-Elbert, S. E.; Silva, M. J.; Xia, Y.; Gelberman, R. H.; Thomopoulos, S. Controlled delivery of mesenchymal stem cells and growth factors using a nanofiber scaffold for tendon repair Acta Biomater. 2013, 9, 6905-6914 10.1016/j.actbio.2013.02.008
44. Wolberg, A. S. Thrombin generation and fibrin clot structure Blood Rev. 2007, 21, 131-142 10.1016/j.blre.2006.11.001
45. Liu, J.; Chen, Q.; Zhang, Z.; Zheng, Y.; Sun, X.; Cao, X.; Gong, A.; Cui, Y.; He, Q.; Jiang, P. Fibrin scaffolds containing ectomesenchymal stem cells enhance behavioral and histological improvement in a rat model of spinal cord injury Cells Tissues Organs 2013, 198, 35-46 10.1159/000351665
46. Wood, M. D.; Gordon, T.; Kim, H.; Szynkaruk, M.; Phua, P.; Lafontaine, C.; Kemp, S. W.; Shoichet, M. S.; Borschel, G. H. Fibrin gels containing GDNF microspheres increase axonal regeneration after delayed peripheral nerve repair Regener. Med. 2013, 8, 27-37 10.2217/rme.12.105
47. Kassam, A.; Nemoto, E.; Balzer, J.; Rao, G.; Welch, W. C.; Kuwabara, H.; Boada, F.; Horowitz, M. Effects of Tisseel fibrin glue on the central nervous system of nonhuman primates Ear, Nose, Throat J. 2004, 83, 246-248 250, 252 passim.
48. Ito, T.; Suzuki, A.; Imai, E.; Okabe, M.; Hori, M. Bone marrow is a reservoir of repopulating mesangial cells during glomerular remodeling J. Am. Soc. Nephrol. 2001, 12, 2625-2635
49. Okabe, M.; Ikawa, M.; Kominami, K.; Nakanishi, T.; Nishimune, Y. 'Green mice' as a source of ubiquitous green cells FEBS Lett. 1997, 407, 313-319 10.1016/S0014-5793(97)00313-X
50. Rooney, G. E.; Moran, C.; McMahon, S. S.; Ritter, T.; Maenz, M.; Flugel, A.; Dockery, P.; O'Brien, T.; Howard, L.; Windebank, A. J.; Barry, F. P. Gene-modified mesenchymal stem cells express functionally active nerve growth factor on an engineered poly lactic glycolic acid (PLGA) substrate Tissue Eng., Part A 2008, 14, 681-690 10.1089/tea.2007.0260
51. Rooney, G. E.; McMahon, S. S.; Ritter, T.; Garcia, Y.; Moran, C.; Madigan, N. N.; Flugel, A.; Dockery, P.; O'Brien, T.; Howard, L.; Windebank, A. J.; Barry, F. P. Neurotrophic factor-expressing mesenchymal stem cells survive transplantation into the contused spinal cord without differentiating into neural cells Tissue Eng., Part A 2009, 15, 3049-3059 10.1089/ten.tea.2009.0045
52. Moloney, T. C.; Dockery, P.; Windebank, A. J.; Barry, F. P.; Howard, L.; Dowd, E. Survival and immunogenicity of mesenchymal stem cells from the green fluorescent protein transgenic rat in the adult rat brain Neurorehabil Neural Repair 2010, 24, 645-656 10.1177/1545968309357745
53. Johnson, P. J.; Parker, S. R.; Sakiyama-Elbert, S. E. Fibrin-based tissue engineering scaffolds enhance neural fiber sprouting and delay the accumulation of reactive astrocytes at the lesion in a subacute model of spinal cord injury J. Biomed. Mater. Res., Part A 2010, 92, 152-163 10.1002/jbm.a.32343
54. Lorentz, K. M.; Kontos, S.; Frey, P.; Hubbell, J. A. Engineered aprotinin for improved stability of fibrin biomaterials Biomaterials 2011, 32, 430-438 10.1016/j.biomaterials.2010.08.109
55. Vu, T. H.; Werb, Z. Matrix metalloproteinases: effectors of development and normal physiology Genes Dev. 2000, 14, 2123-2133 10.1101/gad.815400
56. Ho, W.; Tawil, B.; Dunn, J. C.; Wu, B. M. The behavior of human mesenchymal stem cells in 3D fibrin clots: dependence on fibrinogen concentration and clot structure Tissue Eng. 2006, 12, 1587-1595 10.1089/ten.2006.12.1587
57. De Faveri, S.; Maggiolini, E.; Miele, E.; De Angelis, F.; Cesca, F.; Benfenati, F.; Fadiga, L. Bio-inspired hybrid microelectrodes: a hybrid solution to improve long-term performance of chronic intracortical implants Front. Neuroeng. 2014, 7, 7 10.3389/fneng.2014.00007
58. Wolberg, AS. Thrombin generation and fibrin clot structure Blood Rev. 2007, 21, 131-42 10.1016/j.blre.2006.11.001