Delayed inflammatory mRNA and protein expression after spinal cord injury

Journal of Neuroinflammation

Volumn 8, Issue , 2011, Pages

  Byrnes, Kimberly R ^a,b   Washington, Patricia M ^a   Knoblach, Susan M ^c,d   Hoffman, Eric ^c,d   Faden, Alan I ^a,e  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^b UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^c CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

^d GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^e UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Chronic; Dpi; Galectin 3; Inflammation; Mac 2,; Microarray; Microglia; Nadph oxidase

Indexed keywords

CD53 ANTIGEN; CELL PROTEIN; DIPHENYLIODONIUM SALT; GALECTIN 3; MESSENGER RNA; PROGRANULIN; PROTEIN P22 PHOX; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; UNCLASSIFIED DRUG; PROTEIN PRECURSOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD53 GENE; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVITY; GALECTIN 3 GENE; GENE; GENE CLUSTER; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; GP91 PHOX GENE; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; MACROPHAGE; MALE; MICROARRAY ANALYSIS; MICROGLIA; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEOTIDE SEQUENCE; P22 PHOX GENE; PROGRANULIN GENE; PROTEIN EXPRESSION; RAT; RNA SEQUENCE; SEQUENCE ANALYSIS; SPINAL CORD INJURY; UPREGULATION; WESTERN BLOTTING; ANIMAL; DRUG ANTAGONISM; GENE EXPRESSION; GENE REGULATORY NETWORK; GENETICS; IMMUNOLOGY; INFLAMMATION; METABOLISM; MULTIGENE FAMILY; PATHOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; GALECTIN 3; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; INFLAMMATION; MACROPHAGES; MAGNETIC RESONANCE IMAGING; MALE; MICROARRAY ANALYSIS; MICROGLIA; MULTIGENE FAMILY; NADPH OXIDASE; PROTEIN PRECURSORS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SPINAL CORD INJURIES;

EID: 80053540582     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-8-130     Document Type: Article

References (64)

1. Dumont RJ, Okonkwo DO, Verma S, Hurlbert RJ, Boulos PT, Ellegala DB, Dumont AS. Acute spinal cord injury, part I: pathophysiologic mechanisms. Clin Neuropharmacol 2001, 24:254-264. 10.1097/00002826-200109000-00002, 11586110.
2. Tator CH. Experimental and clinical studies of the pathophysiology and management of acute spinal cord injury. J Spinal Cord Med 1996, 19:206-214.
3. Fitch MT, Doller C, Combs CK, Landreth GE, Silver J. Cellular and molecular mechanisms of glial scarring and progressive cavitation: In vivo and in vitro analysis of inflammation-induced secondary injury after cns trauma. J Neurosci 1999, 19:8182-8198.
4. Dusart I, Schwab ME. Secondary cell death and the inflammatory reaction after dorsal hemisection of the rat spinal cord. Eur J Neurosci 1994, 6:712-724. 10.1111/j.1460-9568.1994.tb00983.x, 8075816.
5. Popovich PG, Guan Z, McGaughy V, Fisher L, Hickey WF, Basso DM. The neuropathological and behavioral consequences of intraspinal microglial/macrophage activation. J Neuropathol Exp Neurol 2002, 61:623-633.
6. Teng YD, Choi H, Onario RC, Zhu S, Desilets FC, Lan S, Woodard EJ, Snyder EY, Eichler ME, Friedlander RM. Minocycline inhibits contusion-triggered mitochondrial cytochrome c release and mitigates functional deficits after spinal cord injury. Proc Natl Acad Sci USA 2004, 101:3071-3076. 10.1073/pnas.0306239101, 365746, 14981254.
7. Stirling DP, Khodarahmi K, Liu J, McPhail LT, McBride CB, Steeves JD, Ramer MS, Tetzlaff W. Minocycline treatment reduces delayed oligodendrocyte death, attenuates axonal dieback, and improves functional outcome after spinal cord injury. J Neurosci 2004, 24:2182-2190. 10.1523/JNEUROSCI.5275-03.2004, 14999069.
8. Demjen D, Klussmann S, Kleber S, Zuliani C, Stieltjes B, Metzger C, Hirt UA, Walczak H, Falk W, Essig M, et al. Neutralization of CD95 ligand promotes regeneration and functional recovery after spinal cord injury. Nat Med 2004, 10:389-395. 10.1038/nm1007, 15004554.
9. Beattie MS. Inflammation and apoptosis: linked therapeutic targets in spinal cord injury. Trends Mol Med 2004, 10:580-583. 10.1016/j.molmed.2004.10.006, 15567326.
10. Spranger M, Fontana A. Activation of microglia: a dangerous interlude in immune function in the brain. The Neuroscientist 1996, 2:293-305.
11. Gomes-Leal W, Corkill DJ, Freire MA, Picanco-Diniz CW, Perry VH. Astrocytosis, microglia activation, oligodendrocyte degeneration, and pyknosis following acute spinal cord injury. Exp Neurol 2004, 190:456-467. 10.1016/j.expneurol.2004.06.028, 15530884.
12. Smith ME, van der Maesen K, Somera FP. Macrophage and microglial responses to cytokines in vitro: phagocytic activity, proteolytic enzyme release, and free radical production. J Neurosci Res 1998, 54:68-78. 10.1002/(SICI)1097-4547(19981001)54:1<68::AID-JNR8>3.0.CO;2-F, 9778151.
13. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, Littman DR, Dustin ML, Gan WB. ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 2005, 8:752-758. 10.1038/nn1472, 15895084.
14. Popovich PG, Hickey WF. Bone marrow chimeric rats reveal the unique distribution of resident and recruited macrophages in the contused rat spinal cord. J Neuropathol Exp Neurol 2001, 60:676-685.
15. Byrnes KR, Garay J, Di Giovanni S, De Biase A, Knoblach SM, Hoffman EP, Movsesyan V, Faden AI. Expression of two temporally distinct microglia-related gene clusters after spinal cord injury. Glia 2006, 53:420-433. 10.1002/glia.20295, 16345062.
16. Popovich PG, Horner PJ, Mullin BB, Stokes BT. A quantitative spatial analysis of the blood-spinal cord barrier. I. Permeability changes after experimental spinal contusion injury. Exp Neurol 1996, 142:258-275. 10.1006/exnr.1996.0196, 8934558.
17. Cross AR, Segal AW. The NADPH oxidase of professional phagocytes--prototype of the NOX electron transport chain systems. Biochim Biophys Acta 2004, 1657:1-22.
18. Qin L, Liu Y, Wang T, Wei SJ, Block ML, Wilson B, Liu B, Hong JS. NADPH oxidase mediates lipopolysaccharide-induced neurotoxicity and proinflammatory gene expression in activated microglia. J Biol Chem 2004, 279:1415-1421.
19. Block ML, Zecca L, Hong JS. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci 2007, 8:57-69. 10.1038/nrn2038, 17180163.
20. Aldskogius H, Kozlova EN. Central neuron-glial and glial-glial interactions following axon injury. Prog Neurobiol 1998, 55:1-26. 10.1016/S0301-0082(97)00093-2, 9602498.
21. Cheret C, Gervais A, Lelli A, Colin C, Amar L, Ravassard P, Mallet J, Cumano A, Krause KH, Mallat M. Neurotoxic activation of microglia is promoted by a nox1-dependent NADPH oxidase. J Neurosci 2008, 28:12039-12051. 10.1523/JNEUROSCI.3568-08.2008, 19005069.
22. Peng J, Stevenson FF, Oo ML, Andersen JK. Iron-enhanced paraquat-mediated dopaminergic cell death due to increased oxidative stress as a consequence of microglial activation. Free Radic Biol Med 2009, 46:312-320. 10.1016/j.freeradbiomed.2008.10.045, 2654268, 19027846.
23. Gao HM, Jiang J, Wilson B, Zhang W, Hong JS, Liu B. Microglial activation-mediated delayed and progressive degeneration of rat nigral dopaminergic neurons: relevance to Parkinson's disease. J Neurochem 2002, 81:1285-1297. 10.1046/j.1471-4159.2002.00928.x, 12068076.
24. Min KJ, Pyo HK, Yang MS, Ji KA, Jou I, Joe EH. Gangliosides activate microglia via protein kinase C and NADPH oxidase. Glia 2004, 48:197-206. 10.1002/glia.20069, 15390122.
25. Pawate S, Shen Q, Fan F, Bhat NR. Redox regulation of glial inflammatory response to lipopolysaccharide and interferongamma. J Neurosci Res 2004, 77:540-551. 10.1002/jnr.20180, 15264224.
26. Doussiere J, Gaillard J, Vignais PV. The heme component of the neutrophil NADPH oxidase complex is a target for aryliodonium compounds. Biochemistry 1999, 38:3694-3703. 10.1021/bi9823481, 10090757.
27. O'Donnell BV, Tew DG, Jones OT, England PJ. Studies on the inhibitory mechanism of iodonium compounds with special reference to neutrophil NADPH oxidase. Biochem J 1993, 290(Pt 1):41-49. 1132380, 8439298.
28. Li J, Baud O, Vartanian T, Volpe JJ, Rosenberg PA. Peroxynitrite generated by inducible nitric oxide synthase and NADPH oxidase mediates microglial toxicity to oligodendrocytes. Proc Natl Acad Sci USA 2005, 102:9936-9941. 10.1073/pnas.0502552102, 1174990, 15998743.
29. Yakovlev AG, Faden AI. Sequential expression of c-fos protooncogene, TNF-alpha, and dynorphin genes in spinal cord following experimental traumatic injury. Mol Chem Neuropathol 1994, 23:179-190. 10.1007/BF02815410, 7702707.
30. Di Giovanni S, Faden AI, Yakovlev A, Duke-Cohan JS, Finn T, Thouin M, Knoblach S, De Biase A, Bregman BS, Hoffman EP. Neuronal plasticity after spinal cord injury: identification of a gene cluster driving neurite outgrowth. Faseb J 2005, 19:153-154.
31. Di Giovanni S, Knoblach SM, Brandoli C, Aden SA, Hoffman EP, Faden AI. Gene profiling in spinal cord injury shows role of cell cycle in neuronal death. Ann Neurol 2003, 53:454-468. 10.1002/ana.10472, 12666113.
32. Byrnes KR, Stoica BA, Fricke S, Di Giovanni S, Faden AI. Cell cycle activation contributes to post-mitotic cell death and secondary damage after spinal cord injury. Brain 2007, 130:2977-2992. 10.1093/brain/awm179, 17690131.
33. Donnelly DJ, Gensel JC, Ankeny DP, van Rooijen N, Popovich PG. An efficient and reproducible method for quantifying macrophages in different experimental models of central nervous system pathology. J Neurosci Methods 2009, 181:36-44. 10.1016/j.jneumeth.2009.04.010, 2737682, 19393692.
34. Fernandes DC, Wosniak J, Pescatore LA, Bertoline MA, Liberman M, Laurindo FR, Santos CX. Analysis of DHE-derived oxidation products by HPLC in the assessment of superoxide production and NADPH oxidase activity in vascular systems. Am J Physiol Cell Physiol 2007, 292:C413-422.
35. Iannotti C, Ping Zhang Y, Shields CB, Han Y, Burke DA, Xu XM. A neuroprotective role of glial cell line-derived neurotrophic factor following moderate spinal cord contusion injury. Exp Neurol 2004, 189:317-332. 10.1016/j.expneurol.2004.05.033, 15380482.
36. Byrnes KR, Stoica B, Riccio A, Pajoohesh-Ganji A, Loane DJ, Faden AI. Activation of metabotropic glutamate receptor 5 improves recovery after spinal cord injury in rodents. Ann Neurol 2009, 66:63-74. 10.1002/ana.21673, 19670441.
37. Sorce S, Krause KH. NOX enzymes in the central nervous system: from signaling to disease. Antioxid Redox Signal 2009, 10:2481-504.
38. Byrnes KR, Fricke ST, Faden AI. Neuropathological differences between rats and mice after spinal cord injury. J Magn Res Imag 2010, 32:836-46.
39. Totoiu MO, Keirstead HS. Spinal cord injury is accompanied by chronic progressive demyelination. J Comp Neurol 2005, 486:373-383. 10.1002/cne.20517, 15846782.
40. Naphade SB, Kigerl KA, Jakeman LB, Kostyk SK, Popovich PG, Kuret J. Progranulin expression is upregulated after spinal contusion in mice. Acta Neuropathol 2010, 119:123-133. 10.1007/s00401-009-0616-y, 19946692.
41. Grewal RP, Morgan TE, Finch CE. C1qB and clusterin mRNA increase in association with neurodegeneration in sporadic amyotrophic lateral sclerosis. Neurosci Lett 1999, 271:65-67. 10.1016/S0304-3940(99)00496-6, 10471215.
42. Natale JE, Ahmed F, Cernak I, Stoica B, Faden AI. Gene expression profile changes are commonly modulated across models and species after traumatic brain injury. J Neurotrauma 2003, 20:907-927. 10.1089/089771503770195777, 14588109.
43. Doverhag C, Hedtjarn M, Poirier F, Mallard C, Hagberg H, Karlsson A, Savman K. Galectin-3 contributes to neonatal hypoxic-ischemic brain injury. Neurobiol Dis 2010, 38:36-46. 10.1016/j.nbd.2009.12.024, 20053377.
44. Yan YP, Lang BT, Vemuganti R, Dempsey RJ. Galectin-3 mediates post-ischemic tissue remodeling. Brain Res 2009, 1288:116-124.
45. Ahmed Z, Mackenzie IR, Hutton ML, Dickson DW. Progranulin in frontotemporal lobar degeneration and neuroinflammation. J Neuroinflammation 2007, 4:7. 10.1186/1742-2094-4-7, 1805428, 17291356.
46. Philips T, De Muynck L, Thu HN, Weynants B, Vanacker P, Dhondt J, Sleegers K, Schelhaas HJ, Verbeek M, Vandenberghe R, et al. Microglial upregulation of progranulin as a marker of motor neuron degeneration. J Neuropathol Exp Neurol 2010, 69:1191-1200. 10.1097/NEN.0b013e3181fc9aea, 21107132.
47. 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, 29:13435-13444. 10.1523/JNEUROSCI.3257-09.2009, 2788152, 19864556.
48. Yin F, Banerjee R, Thomas B, Zhou P, Qian L, Jia T, Ma X, Ma Y, Iadecola C, Beal MF, et al. Exaggerated inflammation, impaired host defense, and neuropathology in progranulin-deficient mice. J Exp Med 2010, 207:117-128. S111-114, 10.1084/jem.20091568, 2812536, 20026663.
49. Pickford F, Marcus J, Camargo LM, Xiao Q, Graham D, Mo JR, Burkhardt M, Kulkarni V, Crispino J, Hering H, Hutton M. Progranulin is a chemoattractant for microglia and stimulates their endocytic activity. Am J Pathol 2011, 178:284-295. 10.1016/j.ajpath.2010.11.002, 21224065.
50. Youn BS, Bang SI, Kloting N, Park JW, Lee N, Oh JE, Pi KB, Lee TH, Ruschke K, Fasshauer M, et al. Serum progranulin concentrations may be associated with macrophage infiltration into omental adipose tissue. Diabetes 2009, 58:627-636. 2646061, 19056610.
51. Filer A, Bik M, Parsonage GN, Fitton J, Trebilcock E, Howlett K, Cook M, Raza K, Simmons DL, Thomas AM, et al. Galectin 3 induces a distinctive pattern of cytokine and chemokine production in rheumatoid synovial fibroblasts via selective signaling pathways. Arthritis Rheum 2009, 60:1604-1614. 10.1002/art.24574, 3116228, 19479862.
52. Narciso MS, Mietto Bde S, Marques SA, Soares CP, Mermelstein Cdos S, El-Cheikh MC, Martinez AM. Sciatic nerve regeneration is accelerated in galectin-3 knockout mice. Exp Neurol 2009, 217:7-15. 10.1016/j.expneurol.2009.01.008, 19416680.
53. Dhirapong A, Lleo A, Leung P, Gershwin ME, Liu FT. The immunological potential of galectin-1 and -3. Autoimmun Rev 2009, 8:360-363. 10.1016/j.autrev.2008.11.009, 19064001.
54. Goodman EB, Tenner AJ. Signal transduction mechanisms of C1q-mediated superoxide production. Evidence for the involvement of temporally distinct staurosporine-insensitive and sensitive pathways. J Immunol 1992, 148:3920-3928.
55. Karlsson A, Follin P, Leffler H, Dahlgren C. Galectin-3 activates the NADPH-oxidase in exudated but not peripheral blood neutrophils. Blood 1998, 91:3430-3438.
56. Fernandez GC, Ilarregui JM, Rubel CJ, Toscano MA, Gomez SA, Bompadre MB, Isturiz MA, Rabinovich GA, Palermo MS. Galectin-3 and soluble fibrinogen act in concert to modulate neutrophil activation and survival. Involvement of alternative MAPK-pathways. Glycobiology 2005, 15:519-27.
57. Lee JH, Woo JH, Woo SU, Kim KS, Park SM, Joe EH, Jou I. The 15-deoxy-delta 12,14-prostaglandin J2 suppresses monocyte chemoattractant protein-1 expression in IFN-gamma-stimulated astrocytes through induction of MAPK phosphatase-1. J Immunol 2008, 181:8642-8649.
58. Olefsky JM, Glass CK. Macrophages, inflammation, and insulin resistance. Annu Rev Physiol 2010, 72:219-246. 10.1146/annurev-physiol-021909-135846, 20148674.
59. Ni W, Zhan Y, He H, Maynard E, Balschi JA, Oettgen P. Ets-1 is a critical transcriptional regulator of reactive oxygen species and p47(phox) gene expression in response to angiotensin II. Circ Res 2007, 101:985-994. 10.1161/CIRCRESAHA.107.152439, 17872466.
60. Dusi S, Donini M, Lissandrini D, Mazzi P, Bianca VD, Rossi F. Mechanisms of expression of NADPH oxidase components in human cultured monocytes: role of cytokines and transcriptional regulators involved. Eur J Immunol 2001, 31:929-938. 10.1002/1521-4141(200103)31:3<929::AID-IMMU929>3.0.CO;2-M, 11241298.
61. Oh YT, Lee JY, Yoon H, Lee EH, Baik HH, Kim SS, Ha J, Yoon KS, Choe W, Kang I. Lipopolysaccharide induces hypoxia-inducible factor-1 alpha mRNA expression and activation via NADPH oxidase and Sp1-dependent pathway in BV2 murine microglial cells. Neurosci Lett 2008, 431:155-160. 10.1016/j.neulet.2007.11.033, 18164813.
62. Wu F, Tyml K, Wilson JX. iNOS expression requires NADPH oxidase-dependent redox signaling in microvascular endothelial cells. J Cell Physiol 2008, 217:207-214. 10.1002/jcp.21495, 2551742, 18481258.
63. Tang XN, Cairns B, Cairns N, Yenari MA. Apocynin improves outcome in experimental stroke with a narrow dose range. Neuroscience 2008, 154:556-562. 10.1016/j.neuroscience.2008.03.090, 2518451, 18511205.
64. Wang Q, Tompkins KD, Simonyi A, Korthuis RJ, Sun AY, Sun GY. Apocynin protects against global cerebral ischemia-reperfusion-induced oxidative stress and injury in the gerbil hippocampus. Brain Res 2006, 1090:182-189. 10.1016/j.brainres.2006.03.060, 16650838.