The effect of resveratrol on neurodegeneration and blood brain barrier stability surrounding intracortical microelectrodes

Biomaterials

Volumn 34, Issue 29, 2013, Pages 7001-7015

  Potter, Kelsey A ^a,b   Buck, Amy C ^a,b   Self, Wade K ^a,b   Callanan, Megan E ^a   Sunil, Smrithi ^a,b   Capadona, Jeffrey R ^a,b  

^a Case Western Reserve University   (United States)

^b LOUIS STOKES CLEVELAND VA MEDICAL CENTER   (United States)

Author keywords

Brain; Implantation; Microelectrode; Reactive oxygen species; Resveratrol

Indexed keywords

ANTI-OXIDATIVE ENZYMES; BIOLOGICAL MECHANISMS; BLOOD-BRAIN BARRIER; HISTOLOGICAL ANALYSIS; POST-IMPLANTATION; REACTIVE OXYGEN SPECIES; THERAPEUTIC TARGETS; TOLL-LIKE RECEPTOR 4;

ANIMALS; BLOOD; BRAIN; ION IMPLANTATION; MICROELECTRODES; OXYGEN; RESVERATROL; STABILITY;

NEURONS;

CATALASE; CD68 ANTIGEN; COPPER ZINC SUPEROXIDE DISMUTASE; GLIAL FIBRILLARY ACIDIC PROTEIN; REACTIVE OXYGEN METABOLITE; RESVERATROL; TOLL LIKE RECEPTOR 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD BRAIN BARRIER; CELL DENSITY; CELL POPULATION; CELL VIABILITY; CONTROLLED STUDY; DRUG EFFECT; HISTOPATHOLOGY; MALE; MEMBRANE PERMEABILITY; MICROELECTRODE; MICROGLIA; NERVE CELL; NERVE DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANIMALS; ANTIOXIDANTS; BLOOD-BRAIN BARRIER; ELECTRODES, IMPLANTED; MALE; MICROELECTRODES; NEURONS; RATS; REACTIVE OXYGEN SPECIES; STILBENES;

ANIMALIA; RATTUS;

EID: 84879600609     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.05.035     Document Type: Article

References (62)

1. Schwartz A.B. Cortical neural prosthetics. Annu Rev Neurosci 2004, 27:487-507.
2. Simeral J.D., Kim S.P., Black M.J., Donoghue J.P., Hochberg L.R. Neural control of cursor trajectory and click by a human with tetraplegia 1000 days after implant of an intracortical microelectrode array. JNeural Eng 2011, 8:025027.
3. Ludwig K.A., Miriani R.M., Langhals N.B., Joseph M.D., Anderson D.J., Kipke D.R. Using a common average reference to improve cortical neuron recordings from microelectrode arrays. JNeurophysiol 2009, 101:1679-1689.
4. Rennaker R.L., Miller J., Tang H., Wilson D.A. Minocycline increases quality and longevity of chronic neural recordings. JNeural Eng 2007, 4:L1-L5.
5. Saxena T., Karumbaiah L., Gaupp E.A., Patkar R., Patil K., Betancur M., et al. The impact of chronic blood-brain barrier breach on intracortical electrode function. Biomaterials 2013, 34:4703-4713.
6. Ward M.P., Rajdev P., Ellison C., Irazoqui P.P. Toward a comparison of microelectrodes for acute and chronic recordings. Brain Res 2009, 1282:183-200.
7. Williams J.C., Rennaker R.L., Kipke D.R. Long-term neural recording characteristics of wire microelectrode arrays implanted in cerebral cortex. Brain Res Prot 1999, 4:303-313.
8. Ludwig K.A., Uram J.D., Yang J., Martin D.C., Kipke D.R. Chronic neural recordings using silicon microelectrode arrays electrochemically deposited with a poly(3,4-ethylenedioxythiophene) (PEDOT) film. JNeural Eng 2006, 3:59-70.
9. Potter K.A., Buck A.C., Self W.K., Capadona J.R. Stab injury and device implantation within the brain results in inversely multiphasic neuroinflammatory and neurodegenerative responses. JNeural Eng 2012, 9.
10. Szarowski D. Brain responses to micro-machined silicon devices. Brain Res 2003, 983:23-35.
11. Ware T., Simon D., Arreaga-Salas D.E., Reeder J., Rennaker R., Keefer E.W., et al. Fabrication of responsive, softening neural interfaces. Adv Funct Mater 2012.
12. Zhong Y., Bellamkonda R. Controlled release of anti-inflammatory agent α-MSH from neural implants. JControl Release 2005, 106:309-318.
13. Skousen J., Merriam S., Srivannavit O., Perlin G., Wise K., Tresco P. Reducing surface area while maintaining implant penetrating profile lowers the brain foreign body response to chronically implanted planar silicon microelectrode arrays. Prog Brain Res 2011, 194C:167-180.
14. Harris J.P., Hess A.E., Rowan S.J., Weder C., Zorman C.A., Tyler D.J., et al. Invivo deployment of mechanically adaptive nanocomposites for intracortical microelectrodes. JNeural Eng 2011, 8:046010.
15. Capadona J.R., Tyler D.J., Zorman C.A., Rowan S.J., Weder C. Mechanically adaptive nanocomposites for neural interfacing. MRS Bull 2012, 37:581-589.
16. Kozai T.D.Y., Marzullo T.C., Hooi F., Langhals N.B., Majewska A.K., Brown E.B., et al. Reduction of neurovascular damage resulting from microelectrode insertion into the cerebral cortex using invivo two-photon mapping. JNeural Eng 2010, 7:046011.
17. Winslow B.D., Christensen M.B., Yang W.-K., Solzbacher F., Tresco P.A. Acomparison of the tissue response to chronically implanted Parylene-C-coated and uncoated planar silicon microelectrode arrays in rat cortex. Biomaterials 2010, 31:9163-9172.
18. Munoz-Fernandez M.A., Fresno M. The role of tumour necrosis factor, interlukin 6, interferon-y and inducible nitric oxide synthase in the development and pathology of the nervous system. Prog Neurobiol 1998, 56:307-340.
19. He W., McConnell G.C., Schneider T.M., Bellamkonda R.V. Anovel anti-inflammatory surface for neural electrodes. Adv Mater 2007, 19:3529-3533.
20. Gilgun-Sherki Y., Melamed E., Offen D. Oxidative stress induced-neurodegenerative diseases: the need for antioxidants that penetrate the blood brain barrier. Neuropharmacology 2001, 40:959-975.
21. Haorah J., Ramirez S.H., Schall K., Smith D., Pandya R., Persidsky Y. Oxidative stress activates protein tyrosine kinase and matrix metalloproteinases leading to blood-brain barrier dysfunction. JNeurochem 2007, 101:566-576.
22. Shukla V., Mishra S.K., Pant H.C. Oxidative stress in neurodegeneration. Adv Pharm Sci 2011, 2011:572634.
23. Sarker M.H., Fraser P.A. Evidence that bradykinin increases permeability of single cerebral microvessels via free radicals in the rat. JPhysiol 1994, 1994:36.
24. Sarker M.H., Hu D.-E., Fraser P.A. Acute effects of bradykinin on cerebral microvascular permeability in the anaesthetized rat. JPhysiol 2000, 528(1):177-187.
25. McArthur S., Cristante E., Paterno M., Christian H., Roncaroli F., Gillies G.E., et al. Annexin A1: a central player in the anti-inflammatory and neuroprotective role of microglia. JImmunol 2010, 185:6317-6328.
26. Alarcón de la Lastra C., Villegas I. Resveratrol as an anti-inflammatory and anti-aging agent: mechanisms and clinical implications. Mol Nutr Food Res 2005, 49:405-430.
27. Potter K.A., Simon J.S., Velagapudi B., Capadona J.R. Reduction of autofluorescence at the microelectrode-cortical tissue interface improves antibody detection. JNeurosci Methods 2012, 203:96-105.
28. Ates O., Cayli S., Altinoz E., Gurses I., Yucel N., Sener M., et al. Neuroprotection by resveratrol against traumatic brain injury in rats. Mol Cell Biochem 2007, 294:137-144.
29. Liu C., Shi Z., Fan L., Zhang C., Wang K., Wang B. Resveratrol improves neuron protection and functional recovery in rat model of spinal cord injury. Brain Res 2011, 1374:100-109.
30. Wenzel E., Somoza V. Metabolism and bioavailability of trans-resveratrol. Mol Nutr Food Res 2005, 49:472-481.
31. Gu Q., Schmued L.C., Sarkar S., Paule M.G., Raymick B. One-step labeling of degenerative neurons in unfixed brain tissue samples using Fluoro-Jade C. JNeurosci Methods 2012, 208:40-43.
32. Schmued L.C., Hopkins K.J. Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res 2000, 874:123-130.
33. McConnell G.C., Rees H.D., Levey A.I., Gutekunst C.-A., Gross R.E., Bellamkonda R.V. Implanted neural electrodes cause chronic, local inflammation that is correlated with local neurodegeneration. JNeural Eng 2009, 6:056003.
34. Fukui M., Choi H.J., Zhu B.T. Mechanism for the protective effect of resveratrol against oxidative stress-induced neuronal death. Free Radic Biol Med 2010, 49:800-813.
35. Leonard S.S., Xia C., Jiang B.-H., Stinefelt B., Klandorf H., Harris G.K., et al. Resveratrol scavenges reactive oxygen species and effects radical-induced cellular responses. Biochem Biophys Res Commun 2003, 309:1017-1026.
36. Zanetti M, d'Uscio L, Peterson TE, Katusic ZS, O'Brien T. Analysis of superoxide anion production in tissue. In: Fennel JP, Baker AH, editors. Methods in molecular medicine. p. 65-72.
37. Buzsáki G. Large-scale recording of neuronal ensembles. Nat Neurosci 2004, 7:446-451.
38. Federico A., Cardaioli E., Da Pozzo P., Formichi P., Gallus G.N., Radi E. Mitochondria, oxidative stress and neurodegeneration. JNeurol Sci 2012.
39. Cole J.T., Yarnell A., Kean W.S., Gold E., Lewis B., Ren M., et al. Craniotomy: true sham for traumatic brain injury, or a sham of a sham?. JNeurotrauma 2011, 28:359-369.
40. Ravikumar M., Jain S., Miller R.H., Capadona J.R., Selkirk S.M. An organotypic spinal cord slice culture model to quantify neurodegeneration. JNeurosci Methods 2012, 211:280-288.
41. Biran R., Martin D., Tresco P. Neuronal cell loss accompanies the brain tissue response to chronically implanted silicon microelectrode arrays. Exp Neurol 2005, 195:115-126.
42. Skaper S.D. The brain as a target for inflammatory processes and neuroprotective strategies. Ann N Y Acad Sci 2007, 1122:23-34.
43. Liu G.S., Zhang Z.S., Yang B., He W. Resveratrol attenuates oxidative damage and ameliorates cognitive impairment in the brain of senescence-accelerated mice. Life Sci 2012, 91:872-877.
44. Simao F., Matte A., Pagnussat A.S., Netto C.A., Salbego C.G. Resveratrol preconditioning modulates inflammatory response in the rat hippocampus following global cerebral ischemia. Neurochem Int 2012.
45. Brkenhielm E. Suppression of angiogenesis, tumor growth, and wound healing by resveratrol, a natural compound in red wine and grapes. FASEB 2001.
46. Sovak M. Grape extract, resveratrol, and its analogs: a review. JMed Food 2001, 4:93-105.
47. Mokni M., Elkahoui S., Limam F., Amri M., Aouani E. Effect of resveratrol on antioxidant enzyme activities in the brain of healthy rat. Neurochem Res 2007, 32:981-987.
48. Abbott N.J., Rönnbäck L., Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 2006, 7:41-53.
49. Aihara N., Tanno H., Hall J.J., Pitts L.H., Noble L.J. Immunocytochemical localization of immunoglobulins in the rat brain: relationship to the blood-brain barrier. JComp Neurol 1994, 342:481-496.
50. Goligorsky M.S. TLR4 and HMGB1: partners in crime?. Kidney Int 2011, 80:450-452.
51. Liew F.Y., Xu D., Brint E.K., O'Neill L.A. Negative regulation of toll-like receptor-mediated immune responses. Nat Rev Immunol 2005, 5:446-458.
52. McCoy C.E., O'Neill L.A.J. The role of TLRs in macrophages. Front Biosci 2008, 1:62-70.
53. Kim Y.T., Hitchcock R.W., Bridge M.J., Tresco P.A. Chronic response of adult rat brain tissue to implants anchored to the skull. Biomaterials 2004, 25:2229-2237.
54. Tate C.C., Tate M.C., LaPlaca M.C. Fibronectin and laminin increase in the mouse brain after controlled cortical impact injury. JNeurotrauma 2007, 24:226-230.
55. Kong Y., Le Y. Toll-like receptors in inflammation of the central nervous system. Int Immunopharmacol 2011, 11:1407-1414.
56. Sims G.P., Rowe D.C., Rietdijk S.T., Herbst R., Coyle A.J. HMGB1 and RAGE in inflammation and cancer. Ann Rev Immunol 2010, 28:367-388.
57. Redzic Z. Molecular biology of the blood-brain and the blood-cerebrospinal fluid barriers: similarities and differences. Fluids Barriers CNS 2011, 8:3.
58. Neher J.J., Neniskyte U., Brown G.C. Primary phagocytosis of neurons by inflamed microglia: potential roles in neurodegeneration. Front Pharm 2012, 3:27.
59. Chan W.H., Wu C.C., Yu J.S. Curcumin inhibits UV irradiation-induced oxidative stress and apoptotic biochemical changes in human epidermoid carcinoma A431 cells. JCell Biochem 2003, 90:327-338.
60. Pardo C.A., Xu Z., Borchelt D.R., Price D.L., Sisodia S.S., Cleveland D.W. Superoxide dismutase is an abundant component in cell bodies, dendrites and axons of motor neurons and in a subset of other neurons. Proc Natl Acad Sci 1995, 92:954-959.
61. Chan P.H. Reactive oxygen radicals in signaling and damage in the ischemic brain. JCereb Blood Flow Metab 2001, 21:2-14.
62. Warner D.S., Sheng H., Batinic-Haberle I. Oxidants, antioxidants and the ischemic brain. JExp Biol 2004, 207:3221-3231.