Biocompatibility of a coacervate-based controlled release system for protein delivery to the injured spinal cord

Acta Biomaterialia

Volumn 11, Issue C, 2015, Pages 204-211

  Rauck, Britta M ^a,b   Novosat, Tabitha L ^c   Oudega, Martin ^a,c   Wang, Yadong ^a,b,d  

^a University of Pittsburgh   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

Biocompatibility; Growth factor delivery; Nervous tissue loss; Sonic hedgehog; Spinal cord injury

Indexed keywords

ETHYLENE; PATIENT REHABILITATION; POLYSACCHARIDES; PROTEINS; TISSUE;

COACERVATE; DELIVERY SYSTEMS; DIGLYCERIDE; GROWTH FACTOR DELIVERY; NERVOUS TISSUE LOSS; NERVOUS TISSUES; POLY(ETHYLENES); SONIC HEDGEHOGS; SPINAL CORD INJURY; TISSUE LOSS;

BIOCOMPATIBILITY;

DIACYLGLYCEROL DERIVATIVE; DRUG CARRIER; HEPARIN; POLY ETHYLENE ARGININYLASPARTATE DIGLYCERIDE; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG; DELAYED RELEASE FORMULATION; PEPTIDE; POLY(ETHYLENE ARGININYLASPARTATE DIGLYCERIDE); POLYESTER; SONIC HEDGEHOG PROTEIN, RAT;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DENSITY; CELL LOSS; CELLULAR IMMUNITY; COACERVATE BASED CONTROLLED RELEASE SYSTEM; COACERVATION; CONTROLLED DRUG RELEASE; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; EXCIPIENT COMPATIBILITY; EXPERIMENTAL SPINAL CORD CONTUSION; FEMALE; IMMUNOCYTOCHEMISTRY; MACROPHAGE; NERVE FIBER; NERVOUS TISSUE; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; RAT; SCAR FORMATION; SENSORIMOTOR FUNCTION; TREADMILL TEST; ANIMAL; AXON; CHEMISTRY; DELAYED RELEASE FORMULATION; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; SPINAL INJURIES; SPRAGUE DAWLEY RAT; SYNTHESIS;

ERINACEIDAE; RATTUS;

ANIMALS; AXONS; DELAYED-ACTION PREPARATIONS; FEMALE; HEDGEHOG PROTEINS; HEPARIN; MACROPHAGES; PEPTIDES; POLYESTERS; RATS; RATS, SPRAGUE-DAWLEY; SPINAL INJURIES;

EID: 84924971496     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2014.09.037     Document Type: Article

References (43)

1. Gumera C, Rauck B, Wang Y. Materials for central nervous system regeneration: bioactive cues. J Mater Chem 2011;21:7033-51.
2. Mocchetti I, Wrathall JR. Neurotrophic factors in central nervous system trauma. J Neurotrauma 1995;12:853-70.
3. Sayer FT, Oudega M, Hagg T. Neurotrophins reduce degeneration of injured ascending sensory and corticospinal motor axons in adult rat spinal cord. Exp Neurol 2002;175:282-96.
4. McTigue DM, Horner PJ, Stokes BT, Gage FH. Neurotrophin-3 and brain-derived neurotrophic factor induce oligodendrocyte proliferation and myelination of regenerating axons in the contused adult rat spinal cord. J Neurosci 1998;18:5354-65.
5. Bamber NI, Li H, Lu X, Oudega M, Aebischer P, Xu XM. Neurotrophins BDNF and NT-3 promote axonal re-entry into the distal host spinal cord through Schwann cell-seeded mini-channels. Eur J Neurosci 2001;13:257-68.
6. Bregman BS, McAtee M, Dai HN, Kuhn PL. Neurotrophic factors increase axonal growth after spinal cord injury and transplantation in the adult rat. Exp Neurol 1997;148:475-94.
7. Mantilla CB, Gransee HM, Zhan WZ, Sieck GC. Motoneuron BDNF/TrkB signaling enhances functional recovery after cervical spinal cord injury. Exp Neurol 2013;247:101-9.
8. Xu XM, Guenard V, Kleitman N, Aebischer P, Bunge MB. A combination of BDNF and NT-3 promotes supraspinal axonal regeneration into Schwann cell grafts in adult rat thoracic spinal cord. Exp Neurol 1995;134:261-72.
9. Parr AM, Tator CH. Intrathecal epidermal growth factor and fibroblast growth factor-2 exacerbate meningeal proliferative lesions associated with intrathecal catheters. Neurosurgery 2007;60:926-33 [discussion-33].
10. Chu H, Gao J, Wang Y. Design, synthesis, and biocompatibility of an arginine-based polyester. Biotechnol Prog 2012;28:257-64.
11. Chu H, Johnson NR, Mason NS, Wang Y. A [polycation:heparin] complex releases growth factors with enhanced bioactivity. J Control Release 2011;150:157-63.
12. Zern BJ, Chu H, Wang Y. Control growth factor release using a self-assembled [polycation:heparin] complex. PLoS One 2010;5:e11017.
13. Johnson NR, Wang Y. Controlled delivery of heparin-binding EGF-like growth factor yields fast and comprehensive wound healing. J Control Release 2013;166:124-9.
14. Johnson NR, Wang Y. Controlled delivery of sonic hedgehog morphogen and its potential for cardiac repair. PLoS One 2013;8:e63075.
15. Li H, Johnson NR, Usas A, Lu A, Poddar M, Wang Y, et al. Sustained release of bone morphogenetic protein 2 via coacervate improves the osteogenic potential of muscle-derived stem cells. Stem Cells Transl Med 2013;2:667-77.
16. Chu H, Gao J, Chen C-W, Huard J, Wang Y. Injectable fibroblast growth factor-2 coacervate for persistent angiogenesis. Proc Natl Acad Sci 2011;108:13444-9.
17. Marti E, Bovolenta P. Sonic hedgehog in CNS development: one signal, multiple outputs. Trends Neurosci 2002;25:89-96.
18. Basso DM, Beattie MS, Bresnahan JC. A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 1995;12:1-21.
19. Hagg T, Oudega M. Degenerative and spontaneous regenerative processes after spinal cord injury. J Neurotrauma 2006;23:264-80.
20. Fitch MT, Doller C, Combs CK, Landreth GE, Silver J. Cellular and molecular mechanisms of glial scarring and progressive cavitation: in vivo and in vitroanalysis of inflammation-induced secondary injury after CNS trauma. J Neurosci 1999;19:8182-98.
21. Leskovar A, Moriarty LJ, Turek JJ, Schoenlein IA, Borgens RB. The macrophage in acute neural injury: changes in cell numbers over time and levels of cytokine production in mammalian central and peripheral nervous systems. J Exp Biol 2000;203:1783-95.
22. Kigerl KA, Ankeny DP, Garg SK, Wei P, Guan Z, Lai W, et al. System xc - regulates microglia and macrophage glutamate excitotoxicity in vivo. Exp Neurol 2012;233:333-41.
23. Kigerl KA, Gensel JC, Ankeny DP, Alexander JK, Donnelly DJ, Popovich PG. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci 2009;29:13435-44.
24. Hausmann ON. Post-traumatic inflammation following spinal cord injury. Spinal Cord 2003;41:369-78.
25. Fawcett JW, Asher RA. The glial scar and central nervous system repair. Brain Res Bull 1999;49:377-91.
26. Fitch MT, Silver J. CNS injury, glial scars, and inflammation: inhibitory extracellular matrices and regeneration failure. Exp Neurol 2008;209:294-301.
27. Nishimaru H, Takizawa H, Kudo N. 5-Hydroxytryptamine-induced locomotor rhythm in the neonatal mouse spinal cord in vitro. Neurosci Lett 2000;280:187-90.
28. Cazalets JR, Sqalli-Houssaini Y, Clarac F. Activation of the central pattern generators for locomotion by serotonin and excitatory amino acids in neonatal rat. J Physiol 1992;455:187-204.
29. Takeoka A, Kubasak MD, Zhong H, Roy RR, Phelps PE. Serotonergic innervation of the caudal spinal stump in rats after complete spinal transection: effect of olfactory ensheathing glia. J Comp Neurol 2009;515:664-76.
30. Ritfeld GJ, Nandoe Tewarie RDS, Vajn K, Rahiem ST, Hurtado A, Wendell DF, et al. Bone marrow stromal cell-mediated tissue sparing enhances functional repair after spinal cord contusion in adult rats. Cell Transplant 2012;21:1561-75.
31. Ritfeld GJ, Rauck BM, Novosat TL, Park D, Patel P, Roos RA, et al. The effect of a polyurethane-based reverse thermal gel on bone marrow stromal cell transplant survival and spinal cord repair. Biomaterials 2014;35:1924-31.
32. Rabchevsky AG, Fugaccia I, Fletcher-Turner A, Blades DA, Mattson MP, Scheff SW. Basic fibroblast growth factor (bFGF) enhances tissue sparing and functional recovery following moderate spinal cord injury. J Neurotrauma 1999;16:817-30.
33. Basso DM. Neuroanatomical substrates of functional recovery after experimental spinal cord injury: implications of basic science research for human spinal cord injury. Phys Ther 2000;80:808-17.
34. Alvarez JI, Dodelet-Devillers A, Kebir H, Ifergan I, Fabre PJ, Terouz S, et al. The Hedgehog pathway promotes blood-brain barrier integrity and CNS immune quiescence. Science 2011;334:1727-31.
35. Straface G, Aprahamian T, Flex A, Gaetani E, Biscetti F, Smith RC, et al. Sonic hedgehog regulates angiogenesis and myogenesis during post-natal skeletal muscle regeneration. J Cell Mol Med 2009;13:2424-35.
36. Lai K, Kaspar BK, Gage FH, Schaffer DV. Sonic hedgehog regulates adult neural progenitor proliferation in vitro and in vivo. Nat Neurosci 2003;6:21-7.
37. Hashimoto M, Ishii K, Nakamura Y, Watabe K, Kohsaka S, Akazawa C. Neuroprotective effect of sonic hedgehog up-regulated in Schwann cells following sciatic nerve injury. J Neurochem 2008;107:918-27.
38. Bambakidis NC, Petrullis M, Kui X, Rothstein B, Karampelas I, Kuang Y, et al. Improvement of neurological recovery and stimulation of neural progenitor cell proliferation by intrathecal administration of Sonic hedgehog. J Neurosurg 2012;116:1114-20.
39. Bambakidis NC, Wang RZ, Franic L, Miller RH. Sonic hedgehog-induced neural precursor proliferation after adult rodent spinal cord injury. J Neurosurg 2003;99:70-5.
40. Bambakidis NC, Horn EM, Nakaji P, Theodore N, Bless E, Dellovade T, et al. Endogenous stem cell proliferation induced by intravenous hedgehog agonist administration after contusion in the adult rat spinal cord. J Neurosurg Spine 2009;10:171-6.
41. Lowry N, Goderie SK, Lederman P, Charniga C, Gooch MR, Gracey KD, et al. The effect of long-term release of Shh from implanted biodegradable microspheres on recovery from spinal cord injury in mice. Biomaterials 2012;33:2892-901.
42. Sirko S, Behrendt G, Johansson PA, Tripathi P, Costa M, Bek S, et al. Reactive glia in the injured brain acquire stem cell properties in response to sonic hedgehog. [Corrected]. Cell Stem Cell 2013;12:426-39.
43. Chu H, Chen C-W, Huard J, Wang Y. The effect of a heparin-based coacervate of fibroblast growth factor-2 on scarring in the infarcted myocardium. Biomaterials 2013;34:1747-56.