In vivo effects of L1 coating on inflammation and neuronal health at the electrode-tissue interface in rat spinal cord and dorsal root ganglion

Acta Biomaterialia

Volumn 8, Issue 10, 2012, Pages 3561-3575

  Kolarcik, C L ^a   Bourbeau, D ^b   Azemi, E ^a,c   Rost, E ^a   Zhang, L ^a   Lagenaur, C F ^b,c   Weber, D J ^b   Cui, X T ^a,c  

^a University of Pittsburgh   (United States)

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

^c UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Biocompatibility; Electrode; Interface; Neural prosthesis; Surface modification

Indexed keywords

BIOCOMPATIBILITY; CELL DEATH; COATED WIRE ELECTRODES; COATINGS; NEURONS; PROSTHETICS; TISSUE;

DORSAL ROOT GANGLIONS; ELECTRODE INTERFACE; ELECTRODE-TISSUE INTERFACE; IN-VIVO; MICROGLIA; NEURAL PROSTHETIC; NEUROFILAMENTS; RAT SPINAL CORD; SURFACE-MODIFICATION;

SURFACE TREATMENT;

EOSIN; HEMATOXYLIN; NERVE CELL ADHESION MOLECULE L1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN TISSUE; CELL ADHESION; CELL AGGREGATION; CELL CULTURE; CELL DENSITY; CONTROLLED STUDY; EMBRYO; GLIOSIS; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; MATERIAL COATING; MICROELECTRODE; MICROGLIA; NERVE CELL; NERVE CELL NECROSIS; NEUROFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN IMMOBILIZATION; RAT; SPINAL CORD; SPINAL GANGLION; TISSUE REACTION;

RATTUS;

EID: 84865526490     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2012.06.034     Document Type: Article

References (81)

1. R.M. Rothschild Neuroengineering tools/applications for bidirectional interfaces, brain-computer interfaces, and neuroprosthetic implants - a review of recent progress Front Neuroeng 3 2010 112
2. S.I. Ryu, and K.V. Shenoy Human cortical prostheses: lost in translation? Neurosurg Focus 27 2009 E5
3. Song YK, Patterson WR, Bull CW, Borton DA, Li Y, Nurmikko AV, et al. A brain implantable microsystem with hybrid RF/IR telemetry for advanced neuroengineering applications. Conf Proc IEEE Eng Med Biol Soc 2007;2007:445-8.
4. M. Morrell Brain stimulation for epilepsy: can scheduled or responsive neurostimulation stop seizures? Curr Opin Neurol 19 2006 164 168
5. T.L. Skarpaas, and M.J. Morrell Intracranial stimulation therapy for epilepsy Neurotherapeutics 6 2009 238 243
6. C. Pena, K. Bowsher, A. Costello, R. De Luca, S. Doll, and K. Li An overview of FDA medical device regulation as it relates to deep brain stimulation devices IEEE Trans Neural Syst Rehabil Eng 15 2007 421 424
7. J.M. Waltz Spinal cord stimulation: a quarter century of development and investigation. A review of its development and effectiveness in 1336 cases Stereotact Funct Neurosurg 69 1997 288 299
8. V.K. Mushahwar, D.M. Gillard, M.J. Gauthier, and A. Prochazka Intraspinal micro stimulation generates locomotor-like and feedback-controlled movements IEEE Trans Neural Syst Rehabil Eng 10 2002 68 81
9. C.T. Moritz, T.H. Lucas, S.I. Perlmutter, and E.E. Fetz Forelimb movements and muscle responses evoked by microstimulation of cervical spinal cord in sedated monkeys J Neurophysiol 97 2007 110 120
10. D.J. Weber, R.B. Stein, D.G. Everaert, and A. Prochazka Limb-state feedback from ensembles of simultaneously recorded dorsal root ganglion neurons J Neural Eng 4 2007 S168 S180
11. R.A. Gaunt, J.A. Hokanson, and D.J. Weber Microstimulation of primary afferent neurons in the L7 dorsal root ganglia using multielectrode arrays in anesthetized cats: thresholds and recruitment properties J Neural Eng 6 2009 055009
12. A.B. Schwartz Cortical neural prosthetics Annu Rev Neurosci 27 2004 487 507
13. A.B. Schwartz, X.T. Cui, D.J. Weber, and D.W. Moran Brain-controlled interfaces: movement restoration with neural prosthetics Neuron 52 2006 205 220
14. K.C. Cheung Implantable microscale neural interfaces Biomed Microdevices 9 2007 923 938
15. V.S. Polikov, P.A. Tresco, and W.M. Reichert Response of brain tissue to chronically implanted neural electrodes J Neurosci Methods 148 2005 1 18
16. S.S. Rao, and J.O. Winter Adhesion molecule-modified biomaterials for neural tissue engineering Front Neuroeng 2 2009 6
17. K.S. Straley, and S.C. Heilshorn Design and adsorption of modular engineered proteins to prepare customized, neuron-compatible coatings Front Neuroeng 2 2009 9
18. W.M. Grill, S.E. Norman, and R.V. Bellamkonda Implanted neural interfaces: biochallenges and engineered solutions Annu Rev Biomed Eng 11 2009 1 24
19. E. Azemi, W.R. Stauffer, M.S. Gostock, C.F. Lagenaur, and X.T. Cui Surface immobilization of neural adhesion molecule L1 for improving the biocompatibility of chronic neural probes: in vitro characterization Acta Biomater 4 2008 1208 1217
20. F. Panetsos, C. Avendano, P. Negredo, J. Castro, and V. Bonacasa Neural prostheses: electrophysiological and histological evaluation of central nervous system alterations due to long-term implants of sieve electrodes to peripheral nerves in cats IEEE Trans Neural Syst Rehabil Eng 16 2008 223 232
21. M.T. Pardue, E.B. Stubbs Jr., J.I. Perlman, K. Narfstrom, A.Y. Chow, and N.S. Peachey Immunohistochemical studies of the retina following long-term implantation with subretinal microphotodiode arrays Exp Eye Res 73 2001 333 343
22. N. Lago, E. Udina, A. Ramachandran, and X. Navarro Neurobiological assessment of regenerative electrodes for bidirectional interfacing injured peripheral nerves IEEE Trans Biomed Eng 54 2007 1129 1137
23. E. Azemi, C.F. Lagenaur, and X.T. Cui The surface immobilization of the neural adhesion molecule L1 on neural probes and its effect on neuronal density and gliosis at the probe/tissue interface Biomaterials 32 2011 681 692
24. P.F. Maness, and M. Schachner Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration Nat Neurosci 10 2007 19 26
25. C. Figge, G. Loers, M. Schachner, and T. Tilling Neurite outgrowth triggered by the cell adhesion molecule L1 requires activation and inactivation of the cytoskeletal protein cofilin Mol Cell Neurosci 2011
26. V. Lemmon, K.L. Farr, and C. Lagenaur L1-mediated axon outgrowth occurs via a homophilic binding mechanism Neuron 2 1989 1597 1603
27. C. Lagenaur, and V. Lemmon An L1-like molecule, the 8D9 antigen, is a potent substrate for neurite extension Proc Natl Acad Sci USA 84 1987 7753 7757
28. S. Kenwrick, A. Watkins, and E. De Angelis Neural cell recognition molecule L1: relating biological complexity to human disease mutations Hum Mol Genet 9 2000 879 886
29. H. Nishimune, C. Bernreuther, P. Carroll, S. Chen, M. Schachner, and C.E. Henderson Neural adhesion molecules L1 and CHL1 are survival factors for motoneurons J Neurosci Res 80 2005 593 599
30. L. Vutskits, Z. Djebbara-Hannas, H. Zhang, J.P. Paccaud, P. Durbec, and G. Rougon PSA-NCAM modulates BDNF-dependent survival and differentiation of cortical neurons Eur J Neurosci 13 2001 1391 1402
31. P. Hulley, M. Schachner, and H. Lubbert L1 neural cell adhesion molecule is a survival factor for fetal dopaminergic neurons J Neurosci Res 53 1998 129 134
32. I. Aubert, J.L. Ridet, and F.H. Gage Regeneration in the adult mammalian CNS: guided by development Curr Opin Neurobiol 5 1995 625 635
33. J.C. Xu, C. Bernreuther, Y.F. Cui, I. Jakovcevski, G. Hargus, and M.F. Xiao Transplanted L1 expressing radial glia and astrocytes enhance recovery after spinal cord injury J Neurotrauma 28 2011 1921 1937
34. Y.F. Cui, J.C. Xu, G. Hargus, I. Jakovcevski, M. Schachner, and C. Bernreuther Embryonic stem cell-derived L1 overexpressing neural aggregates enhance recovery after spinal cord injury in mice PLoS One 6 2011 e17126
35. A.A. Lavdas, J. Chen, F. Papastefanaki, S. Chen, M. Schachner, and R. Matsas Schwann cells engineered to express the cell adhesion molecule L1 accelerate myelination and motor recovery after spinal cord injury Exp Neurol 221 2010 206 216
36. Y. Takeda, Y. Murakami, H. Asou, and K. Uyemura The roles of cell adhesion molecules on the formation of peripheral myelin Keio J Med 50 2001 240 248
37. J.A. Mackintosh, D.A. Veal, and P. Karuso Fluoroprofile, a fluorescence-based assay for rapid and sensitive quantitation of proteins in solution Proteomics 5 2005 4673 4677
38. S. Musallam, M.J. Bak, P.R. Troyk, and R.A. Andersen A floating metal microelectrode array for chronic implantation J Neurosci Methods 160 2007 122 127
39. G.J. Brewer Serum-free B27/neurobasal medium supports differentiated growth of neurons from the striatum, substantia nigra, septum, cerebral cortex, cerebellum, and dentate gyrus J Neurosci Res 42 1995 674 683
40. P. Cheepsunthorn, L. Radov, S. Menzies, J. Reid, and J.R. Connor Characterization of a novel brain-derived microglial cell line isolated from neonatal rat brain Glia 35 2001 53 62
41. X. Luo, C. Matranga, S. Tan, N. Alba, and X.T. Cui Carbon nanotube nanoreservior for controlled release of anti-inflammatory dexamethasone Biomaterials 32 2011 6316 6323
42. D. Ito, Y. Imai, K. Ohsawa, K. Nakajima, Y. Fukuuchi, and S. Kohsaka Microglia-specific localisation of a novel calcium binding protein, Iba1 Brain Res Mol Brain Res 57 1998 1 9
43. N. Patro, A. Nagayach, and I.K. Patro Iba1 expressing microglia in the dorsal root ganglia become activated following peripheral nerve injury in rats Indian J Exp Biol 48 2010 110 116
44. K. Ohsawa, M. Neo, H. Matsuoka, H. Akiyama, H. Ito, and H. Kohno The expression of bone matrix protein mRNAs around beta-TCP particles implanted into bone J Biomed Mater Res 52 2000 460 466
45. D. Ito, K. Tanaka, S. Suzuki, T. Dembo, and Y. Fukuuchi Enhanced expression of Iba1, ionized calcium-binding adapter molecule 1, after transient focal cerebral ischemia in rat brain Stroke 32 2001 1208 1215
46. I. Mori, F. Goshima, T. Koshizuka, Y. Imai, S. Kohsaka, and N. Koide Iba1-expressing microglia respond to herpes simplex virus infection in the mouse trigeminal ganglion Brain Res Mol Brain Res 120 2003 52 56
47. R.J. Dumont, D.O. Okonkwo, S. Verma, R.J. Hurlbert, P.T. Boulos, and D.B. Ellegala Acute spinal cord injury, part I: pathophysiologic mechanisms Clin Neuropharmacol 24 2001 254 264
48. I. Paterniti, T. Genovese, C. Crisafulli, E. Mazzon, R. Di Paola, and M. Galuppo Treatment with green tea extract attenuates secondary inflammatory response in an experimental model of spinal cord trauma Naunyn Schmiedebergs Arch Pharmacol 380 2009 179 192
49. G. Majno, and I. Joris Apoptosis, oncosis, and necrosis. An overview of cell death Am J Pathol 146 1995 3 15
50. P. Nicotera, M. Ankarcrona, E. Bonfoco, S. Orrenius, and S.A. Lipton Neuronal necrosis and apoptosis: two distinct events induced by exposure to glutamate or oxidative stress Adv Neurol 72 1997 95 101
51. X.Z. Liu, X.M. Xu, R. Hu, C. Du, S.X. Zhang, and J.W. McDonald Neuronal and glial apoptosis after traumatic spinal cord injury J Neurosci 17 1997 5395 5406
52. M.S. Beattie, A.A. Farooqui, and J.C. Bresnahan Review of current evidence for apoptosis after spinal cord injury J Neurotrauma 17 2000 915 925
53. S. Amemiya, T. Kamiya, C. Nito, T. Inaba, K. Kato, and M. Ueda Anti-apoptotic and neuroprotective effects of edaravone following transient focal ischemia in rats Eur J Pharmacol 516 2005 125 130
54. C.A. Oyinbo Secondary injury mechanisms in traumatic spinal cord injury: a nugget of this multiply cascade Acta Neurobiol Exp (Wars) 71 2011 281 299
55. D.L. Bennett, G.J. Michael, N. Ramachandran, J.B. Munson, S. Averill, and Q. Yan A distinct subgroup of small DRG cells express GDNF receptor components and GDNF is protective for these neurons after nerve injury J Neurosci 18 1998 3059 3072
56. P. Hu, A.L. Bembrick, K.A. Keay, and E.M. McLachlan Immune cell involvement in dorsal root ganglia and spinal cord after chronic constriction or transection of the rat sciatic nerve Brain Behav Immun 21 2007 599 616
57. M. Hanani Satellite glial cells in sensory ganglia: from form to function Brain Res Brain Res Rev 48 2005 457 476
58. J.R. Keast, and T.M. Stephensen Glutamate and aspartate immunoreactivity in dorsal root ganglion cells supplying visceral and somatic targets and evidence for peripheral axonal transport J Comp Neurol 424 2000 577 587
59. J.N. Turner, W. Shain, D.H. Szarowski, M. Andersen, S. Martins, and M. Isaacson Cerebral astrocyte response to micromachined silicon implants Exp Neurol 156 1999 33 49
60. P.C. Georges, W.J. Miller, D.F. Meaney, E.S. Sawyer, and P.A. Janmey Matrices with compliance comparable to that of brain tissue select neuronal over glial growth in mixed cortical cultures Biophys J 90 2006 3012 3018
61. B. Amsden Curable, biodegradable elastomers:emerging biomaterials for drug delivery and tissue engineering Soft Matter 3 2007 1335 1348
62. G.N. Tew, K. Agrawal, and S.R. Bhatia New properties from PLA-PEO-PLA hydrogels Soft Matter 1 2005 253 258
63. Ware T, Simon D, Arreaga-Salas DE, Reeder J, Rennaker R, Keefer EW, et al. Fabrication of Responsive, Softening Neural Interfaces. Adv Funct Mater 2012:n/a-n/a.
64. J.R. Capadona, K. Shanmuganathan, D.J. Tyler, S.J. Rowan, and C. Weder Stimuli-responsive polymer nanocomposites inspired by the sea cucumber dermis Science 319 2008 1370 1374
65. J.P. Harris, J.R. Capadona, R.H. Miller, B.C. Healy, K. Shanmuganathan, and S.J. Rowan Mechanically adaptive intracortical implants improve the proximity of neuronal cell bodies J Neural Eng 8 2011 066011
66. J.P. Harris, A.E. Hess, S.J. Rowan, C. Weder, C.A. Zorman, and D.J. Tyler In vivo deployment of mechanically adaptive nanocomposites for intracortical microelectrodes J Neural Eng 8 2011 046010
67. A. Irintchev, and M. Schachner The Injured and Regenerating Nervous System: Immunoglobulin Superfamily Members as Key Players Neuroscientist 2011
68. C.G. Becker, B.C. Lieberoth, F. Morellini, J. Feldner, T. Becker, and M. Schachner L1.1 is involved in spinal cord regeneration in adult zebrafish J Neurosci 24 2004 7837 7842
69. T. Becker, B.C. Lieberoth, C.G. Becker, and M. Schachner Differences in the regenerative response of neuronal cell populations and indications for plasticity in intraspinal neurons after spinal cord transection in adult zebrafish Mol Cell Neurosci 30 2005 265 278
70. J. Chen, C. Bernreuther, M. Dihne, and M. Schachner Cell adhesion molecule l1-transfected embryonic stem cells with enhanced survival support regrowth of corticospinal tract axons in mice after spinal cord injury J Neurotrauma 22 2005 896 906
71. Y.F. Cui, G. Hargus, J.C. Xu, J.S. Schmid, Y.Q. Shen, and M. Glatzel Embryonic stem cell-derived L1 overexpressing neural aggregates enhance recovery in Parkinsonian mice Brain 133 2010 189 204
72. K.D. Barron Microglia: history, cytology, and reactions J Neurol Sci 207 2003 98
73. M. Schwartz Macrophages and microglia in central nervous system injury: are they helpful or harmful? J Cereb Blood Flow Metab 23 2003 385 394
74. M.V. Sofroniew, and H.V. Vinters Astrocytes: biology and pathology Acta Neuropathol 119 2010 7 35
75. D.H. Szarowski, M.D. Andersen, S. Retterer, A.J. Spence, M. Isaacson, and H.G. Craighead Brain responses to micro-machined silicon devices Brain Res 983 2003 23 35
76. C. Roonprapunt, W. Huang, R. Grill, D. Friedlander, M. Grumet, and S. Chen Soluble cell adhesion molecule L1-Fc promotes locomotor recovery in rats after spinal cord injury J Neurotrauma 20 2003 871 882
77. K. Webb, E. Budko, T.J. Neuberger, S. Chen, M. Schachner, and P.A. Tresco Substrate-bound human recombinant L1 selectively promotes neuronal attachment and outgrowth in the presence of astrocytes and fibroblasts Biomaterials 22 2001 1017 1028
78. W. He, G.C. McConnell, and R.V. Bellamkonda Nanoscale laminin coating modulates cortical scarring response around implanted silicon microelectrode arrays J Neural Eng 3 2006 316 326
79. A. Singh, G. Ehteshami, S. Massia, J. He, R.G. Storer, and G. Raupp Glial cell and fibroblast cytotoxicity study on plasma-deposited diamond-like carbon coatings Biomaterials 24 2003 5083 5089
80. R. Wadhwa, C.F. Lagenaur, and X.T. Cui Electrochemically controlled release of dexamethasone from conducting polymer polypyrrole coated electrode J Control Release 110 2006 531 541
81. Y. Zhong, and R.V. Bellamkonda Controlled release of anti-inflammatory agent alpha-MSH from neural implants J Control Release 106 2005 309 318