The temporal expression, cellular localization, and inhibition of the chemokines MIP-2 and MCP-1 after traumatic brain injury in the rat

Journal of Neurotrauma

Volumn 26, Issue 4, 2009, Pages 507-525

  Rhodes, Jonathan K J ^a   Sharkey, John ^c   Andrews, Peter J D ^b  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b WESTERN GENERAL HOSPITAL   (United Kingdom)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Brain; MCP 1=CCL2; MIP 2=CXCL2; trauma

Indexed keywords

DEXAMETHASONE; MACROPHAGE INFLAMMATORY PROTEIN 2; MONOCYTE CHEMOTACTIC PROTEIN 1; NEURON SPECIFIC NUCLEAR PROTEIN; TACROLIMUS;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; CELLULAR DISTRIBUTION; COHORT ANALYSIS; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; GLIA CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MALE; NERVE CELL; NONHUMAN; PROTEIN EXPRESSION; RAT; STAINING; TRAUMATIC BRAIN INJURY;

ANIMALS; ANTI-INFLAMMATORY AGENTS; BRAIN; BRAIN INJURIES; CHEMOKINE CCL2; CHEMOKINE CXCL2; DEXAMETHASONE; DISEASE MODELS, ANIMAL; DOWN-REGULATION; IMMUNOSUPPRESSIVE AGENTS; MALE; NERVE DEGENERATION; NERVE TISSUE PROTEINS; NEURONS; NUCLEAR PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; TACROLIMUS; TIME FACTORS; UP-REGULATION;

EID: 64849090434     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2008.0686     Document Type: Article

References (68)

1. Aihara, N., Hall, J.J., Pitts, L.H., Fukuda, K., and Noble, L.J. (1995). Altered immunoexpression of microglia and macro-phages after mild head injury. J. Neurotrauma 12, 53-63.
2. Alderson, P., and Roberts, I. (2000). Corticosteroids for acute traumatic brain injury. Cochrane Database Syst. Rev. CD000196.
3. Babcock, A.A., Kuziel, W.A., Rivest, S., and Owens, T. (2003). Chemokine expression by glial cells directs leukocytes to sites of axonal injury in the CNS. J. Neurosci. 23, 7922-7930.
4. Bell, M.D., Taub, D.D., and Perry, V.H. (1996). Overriding the brain's intrinsic resistance to leukocyte recruitment with in-traparenchymal injections of recombinant chemokines. Neu-roscience 74, 283-292.
5. Berman, J.W., Guida, M.P., Warren, J., Amat, J., and Brosnan, C.F. (1996). Localization of monocyte chemoattractant pep-tide-1 expression in the central nervous system in experimental autoimmune encephalomyelitis and trauma in the rat. J. Immunol. 156, 3017-3023.
6. Borger, P., Kauffman, H.F., Timmerman, J.A., Scholma, J., van den Berg, J.W., and Koeter, G.H. (2000). Cyclosporine, FK506, mycophenolate mofetil, and prednisolone differentially modulate cytokine gene expression in human airway-derived epithelial cells. Transplantation 69, 1408-1413.
7. Butcher, S.P., Henshall, D.C., Teramura, Y., Iwasaki, K., and Sharkey, J. (1997). Neuroprotective actions of FK506 in experimental stroke: in vivo evidence against an antiexcitotoxic mechanism. J. Neurosci. 17, 6939-6946.
8. Che, X., Ye, W., Panga, L., Wu, D.C., and Yang, G.Y. (2001). Monocyte chemoattractant protein-1 expressed in neurons and astrocytes during focal ischemia in mice. Brain Res. 902, 171-177.
9. Colotta, F., Borre, A., Wang, J.M., Tattanelli, M., Maddalena, F., Polentarutti, N., Peri, G., and Mantovani, A. (1992). Expression of a monocyte chemotactic cytokine by human mono-nuclear phagocytes. J. Immunol. 148, 760-765.
10. Cortez, S.C., McIntosh, T.K., and Noble, L.J. (1989). Experimental fluid percussion brain injury: vascular disruption and neuronal and glial alterations. Brain Res. 482, 271-282.
11. Cox, G. (1995). Glucocorticoid treatment inhibits apoptosis in human neutrophils. Separation of survival and activation outcomes. J. Immunol. 154, 4719-4725.
12. de Haij, S., Woltman, A.M., Bakker, A.C., Daha, M.R., and van Kooten, C. (2002). Production of inflammatory mediators by renal epithelial cells is insensitive to glucocorticoids. Br. J. Pharmacol. 137, 197-204.
13. Duffield, J.S. (2003). The inflammatory macrophage: a story of Jekyll and Hyde. Clin. Sci. (Lond.) 104, 27-38.
14. Ehrlich, L.C., Hu, S., Sheng, W.S., Sutton, R.L., Rockswold, G.L., Peterson, P.K., and Chao, C.C. (1998). Cytokine regulation of human microglial cell IL-8 production. J. Immunol. 160, 1944- 1948.
15. Fan, L., Young, P.R., Barone, F.C., Feuerstein, G.Z., Smith, D.H., and McIntosh, T.K. (1995). Experimental brain injury induces expression of interleukin-1 beta mRNA in the rat brain. Brain Res. Mol. Brain Res. 30, 125-130.
16. Galicich, J., and French, L. (1961). Use of dexamethasone in the treatment of cerebral edema resulting from brain tumors and brain surgery. Am. Pract. Dig. Treat. 12, 169-174.
17. Gilmour, P.S., Ziesenis, A., Morrison, E.R., Vickers, M.A., Drost, E.M., Ford, I., Karg, E., Mossa, C., Schroeppel, A., Ferron, G.A., Heyder, J., Greaves, M., MacNee, W., and Donaldson, K. (2004). Pulmonary and systemic effects of short-term inhalation exposure to ultrafine carbon black particles. Toxicol. Appl. Pharmacol. 195, 35-44.
18. Glabinski, A.R., Balasingam, V., Tani, M., Kunkel, S.L., Strieter, R.M., Yong, V.W., and Ransohoff, R.M. (1996). Chemokine monocyte chemoattractant protein-1 is expressed by astro-cytes after mechanical injury to the brain. J. Immunol. 156, 4363-4368.
19. Gourmala, N.G., Buttini, M., Limonta, S., Sauter, A., and Bod-deke, H.W. (1997). Differential and time-dependent expression of monocyte chemoattractant protein-1 mRNA by astrocytes and macrophages in rat brain: effects of ischemia and peripheral lipopolysaccharide administration. J. Neuroimmunol. 74, 35-44.
20. Grzybicki, D., Moore, S.A., Schelper, R., Glabinski, A.R., Ran-sohoff, R.M., and Murphy, S. (1998). Expression of monocyte chemoattractant protein (MCP-1) and nitric oxide synthase-2 following cerebral trauma. Acta Neuropathol. (Berl.) 95, 98- 103.
21. Harkness, K.A., Sussman, J.D., Davies-Jones, G.A., Greenwood, J., and Woodroofe, M.N. (2003). Cytokine regulation of MCP-1 expression in brain and retinal microvascular endothelial cells. J. Neuroimmunol. 142, 1-9.
22. Hausmann, E.H., Berman, N.E., Wang, Y.Y., Meara, J.B., Wood, G.W., and Klein, R.M. (1998). Selective chemokine mRNA expression following brain injury. Brain Res. 788, 49-59.
23. Hayashi, M., Luo, Y., Laning, J., Strieter, R.M., and Dorf, M.E. (1995). Production and function of monocyte chemoattractant protein-1 and other beta-chemokines in murine glial cells. J. Neuroimmunol. 60, 143-150.
24. Heasman, S.J., Giles, K.M., Ward, C., Rossi, A.G., Haslett, C., and Dransfield, I. (2003). Glucocorticoid-mediated regulation of granulocyte apoptosis and macrophage phagocytosis of apoptotic cells: implications for the resolution of inflammation. J. Endocrinol. 178, 29-36.
25. Held, H.D., Boettcher, S., Hamann, L., and Uhlig, S. (2001). Ventilation-induced chemokine and cytokine release is associated with activation of nuclear factor-kappaB and is blocked by steroids. Am. J. Respir. Crit. Care Med. 163, 711-716.
26. Hicks, R., Soares, H., Smith, D., and McIntosh, T. (1996). Temporal and spatial characterization of neuronal injury following lateral fluid-percussion brain injury in the rat. Acta Neuro-pathol. (Berl.) 91, 236-246.
27. Holmin, S., Mathiesen, T., Shetye, J., and Biberfeld, P. (1995). Intracerebral inflammatory response to experimental brain contusion. Acta Neurochir. (Wien.) 132, 110-119.
28. Holmin, S., Soderlund, J., Biberfeld, P., and Mathiesen, T. (1998). Intracerebral inflammation after human brain contusion. Neurosurgery 42, 291-298.
29. Johnston, B., and Butcher, E.C. (2002). Chemokines in rapid leukocyte adhesion triggering and migration. Semin. Immunol. 14, 83-92.
30. Kaplan, A., Matsue, H., Shibaki, A., Kawashima, T., Kobayashi, H., and Ohkawara, A. (1995). The effects of cyclosporin A and FK506 on proliferation and IL-8 production of cultured human keratinocytes. J. Dermatol. Sci. 10, 130-138.
31. Kim, J.S., Chopp, M., and Gautam, S.C. (1995). High dose methylprednisolone therapy reduces expression of JE/MCP-1 mRNA and macrophage accumulation in the ischemic rat brain. J. Neurol. Sci. 128, 28-35.
32. Kono, H., Fujii, H., Asakawa, M., Maki, A., Amemiya, H., Hirai, Y., Matsuda, M., and Yamamoto, M. (2004). Medium-chain triglycerides enhance secretory IgA expression in rat intestine after administration of endotoxin. Am. J. Physiol. Gastrointest. Liver Physiol. 286, G1081-G1089.
33. Kossmann, T., Stahel, P.F., Lenzlinger, P.M., Redl, H., Dubs, R.W., Trentz, O., Schlag, G., and Morganti-Kossmann, M.C. (1997). Interleukin-8 released into the cerebrospinal fluid after brain injury is associated with blood-brain barrier dysfunction and nerve growth factor production. J. Cereb. Blood Flow Metab. 17, 280-289.
34. Kubes, P., Hunter, J., and Granger, D.N. (1991). Effects of cy-closporin A and FK506 on ischemia/reperfusion-induced neutrophil infiltration in the cat. Dig. Dis. Sci. 36, 1469-1472.
35. Kurz, J.E., Parsons, J.T., Rana, A., Gibson, C.J., Hamm, R.J., and Churn, S.B. (2005). A significant increase in both basal and maximal calcineurin activity following fluid percussion injury in the rat. J. Neurotrauma. 22, 476-490.
36. McCarter, J.F., McGregor, A.L., Jones, P.A., and Sharkey, J. (2001). FK 506 protects brain tissue in animal models of stroke. Transplant. Proc. 33, 2390-2392.
37. McIntosh, T.K., Vink, R., Noble, L., Yamakami, I., Fernyak, S., Soares, H., and Faden, A.L. (1989). Traumatic brain injury in the rat: characterization of a lateral fluid-percussion model. Neuroscience 28, 233-244.
38. Minami, M., and Satoh, M. (2003). Chemokines and their receptors in the brain: pathophysiological roles in ischemic brain injury. Life Sci. 74, 321-327.
39. Muessel, M.J., Berman, N.E., and Klein, R.M. (2000). Early and specific expression of monocyte chemoattractant protein-1 in the thalamus induced by cortical injury. Brain Res. 870, 211-221.
40. Mukaida, N., Morita, M., Ishikawa, Y., Rice, N., Okamoto, S., Kasahara, T., and Matsushima, K. (1994). Novel mechanism of glucocorticoid-mediated gene repression. Nuclear factor-kappa B is target for glucocorticoid-mediated interleukin 8 gene repression. J. Biol. Chem. 269, 13289-13295.
41. Nishinaka, Y., Sugiyama, S., Yokota, M., Saito, H., and Ozawa, T. (1993). Protective effect of FK506 on ischemia/reperfusion-induced myocardial damage in canine heart. J. Cardiovasc. Pharmacol. 21, 448-454.
42. Nudel, U., Zakut, R., Shani, M., Neuman, S., Levy, Z., and Yaffe, D. (1983). The nucleotide sequence of the rat cytoplasmic beta-actin gene. Nucleic Acids Res. 11, 1759-1771.
43. Nygardas, P.T., Maatta, J.A., and Hinkkanen, A.E. (2000). Che-mokine expression by central nervous system resident cells and infiltrating neutrophils during experimental autoimmune encephalomyelitis in the BALB/c mouse. Eur. J. Immunol. 30, 1911-1918.
44. Okamoto, S., Mukaida, N., Yasumoto, K., Rice, N., Ishikawa, Y., Horiguchi, H., Murakami, S., and Matsushima, K. (1994). The interleukin-8 AP-1 and kappa B-like sites are genetic end targets of FK506-sensitive pathway accompanied by calcium mobilization. J. Biol. Chem. 269, 8582-8589.
45. Otto, V.I., Heinzel-Pleines, U.E., Gloor, S.M., Trentz, O., Koss-mann, T., and Morganti-Kossmann, M.C. (2000). sICAM-1 and TNF-alpha induce MIP-2 with distinct kinetics in astrocytes and brain microvascular endothelial cells. J. Neurosci. Res. 60, 733-742.
46. Otto, V.I., Stahel, P.F., Rancan, M., Kariya, K., Shohami, E., Yatsiv, I., Eugster, H.P., Kossmann, T., Trentz, O., and Morganti-Kossmann, M.C. (2001). Regulation of chemokines and chemokine receptors after experimental closed head injury. Neuroreport 12, 2059-2064.
47. Porcheray, F., Viaud, S., Rimaniol, A.C., Leone, C., Samah, B., Dereuddre-Bosquet, N., Dormont, D., and Gras, G. (2005). Macrophage activation switching: an asset for the resolution of inflammation. Clin. Exp. Immunol. 142, 481-489.
48. Rancan, M., Otto, V.I., Hans, V.H., Gerlach, I., Jork, R., Trentz, O., Kossmann, T., and Morganti-Kossmann, M.C. (2001). Upregulation of ICAM-1 and MCP-1 but not of MIP-2 and sensorimotor deficit in response to traumatic axonal injury in rats. J. Neurosci. Res. 63, 438-446.
49. Rhodes, J.K., Andrews, P.J., Holmes, M.C., and Seckl, J.R. (2002). Expression of interleukin-6 messenger RNA in a rat model of diffuse axonal injury. Neurosci. Lett. 19;335, 1-4.
50. Roberts, I., Yates, D., Sandercock, P., Farrell, B., Wasserberg, J., Lomas, G., Cottingham, R., Svoboda, P., Brayley, N., Ma-zairac, G., Laloe, V., Munoz-Sanchez, A., Arango, M., Hart-zenberg, B., Khamis, H., Yutthakasemsunt, S., Komolafe, E., Olldashi, F., Yadav, Y., Murillo-Cabezas, F., Shakur, H., and Edwards, P. (2004). Effect of intravenous corticosteroids on death within 14 days in 10008 adults with clinically significant head injury (MRC CRASH trial): randomised placebo-controlled trial. Lancet 364, 1321-1328.
51. Saitoh, O., Matsuse, R., Sugi, K., Nakagawa, K., Uchida, K., Maemura, K., Kojima, K., Hirata, I., and Katsu, K. (1997). Cyclosporine A inhibits interleukin-8 production in a human colon epithelial cell line (HT-29). J. Gastroenterol. 32, 605-610.
52. Sasakawa, Y., Sakuma, S., Higashi, Y., Sasakawa, T., Amaya, T., and Goto, T. (2000). FK506 suppresses neutrophil chemoat-tractant production by peripheral blood mononuclear cells. Eur. J. Pharmacol. 403, 281-288.
53. Savill, J.S., Wyllie, A.H., Henson, J.E., Walport, M.J., Henson, P.M., and Haslett, C. (1989). Macrophage phagocytosis of aging neutrophils in inflammation. Programmed cell death in the neutrophil leads to its recognition by macrophages. J. Clin. Invest. 83, 865-875.
54. Schramm, R., and Thorlacius, H. (2003). Staphylococcal entero-toxin B-induced acute inflammation is inhibited by dexameth-asone: important role of CXC chemokines KC and macrophage inflammatory protein 2. Infect. Immun. 71, 2542-2547.
55. Schwartz, D., Engelhard, D., Gallily, R., Matoth, I., and Brenner, T. (1998). Glial cells production of inflammatory mediators induced by Streptococcus pneumoniae: inhibition by pentox-ifylline, low-molecular-weight heparin and dexamethasone. J. Neurol. Sci. 155, 13-22.
56. Sharkey, J., and Butcher, S.P. (1994). Immunophilins mediate the neuroprotective effects of FK506 in focal cerebral ischaemia. Nature 371, 336-339.
57. Singleton, R.H., Stone, J.R., Okonkwo, D.O., Pellicane, A.J., and Povlishock, J.T. (2001). The immunophilin ligand FK506 attenuates axonal injury in an impact-acceleration model of traumatic brain injury. J. Neurotrauma 18, 607-614.
58. Soares, H.D., Hicks, R.R., Smith, D., and McIntosh, T.K. (1995). Inflammatory leukocytic recruitment and diffuse neuronal degeneration are separate pathological processes resulting from traumatic brain injury. J. Neurosci. 15, 8223-8233.
59. Stover, J.F., Schoning, B., Sakowitz, O.W., Woiciechowsky, C., and Unterberg, A.W. (2001). Effects of tacrolimus on hemispheric water content and cerebrospinal fluid levels of glu-tamate, hypoxanthine, interleukin-6, and tumor necrosis factor-alpha following controlled cortical impact injury in rats. J. Neurosurg. 94, 782-787.
60. Suzuki, S., Toledo-Pereyra, L.H., Rodriguez, F.J., and Cejalvo, D. (1993). Neutrophil infiltration as an important factor in liver ischemia and reperfusion injury. Modulating effects of FK506 and cyclosporine. Transplantation 55, 1265-1272.
61. Taupin, V., Toulmond, S., Serrano, A., Benavides, J., and Zavala, F. (1993). Increase in IL-6, IL-1 and TNF levels in rat brain following traumatic lesion. Influence of pre- and post-traumatic treatment with Ro5 4864, a peripheral-type (p site) benzodiazepine ligand. J. Neuroimmunol. 42, 177-185.
62. Tobler, A., Meier, R., Seitz, M., Dewald, B., Baggiolini, M., and Fey, M.F. (1992). Glucocorticoids downregulate gene expression of GM-CSF, NAP-1/IL-8, and IL-6, but not of M-CSF in human fibroblasts. Blood 79, 45-51.
63. Tsujikawa, A., Ogura, Y., Hiroshiba, N., Miyamoto, K., Kiryu, J., and Honda, Y. (1998). Tacrolimus (FK506) attenuates leukocyte accumulation after transient retinal ischemia. Stroke 29, 1431-1437.
64. Valles, A., Grijpink-Ongering, L., de Bree, F.M., Tuinstra, T., and Ronken, E. (2006). Differential regulation of the CXCR2 che-mokine network in rat brain trauma: implications for neu-roimmune interactions and neuronal survival. Neurobiol. Dis. 22, 312-322.
65. Wakita, H., Tomimoto, H., Akiguchi, I., and Kimura, J. (1998). Dose-dependent, protective effect of FK506 against white matter changes in the rat brain after chronic cerebral ischemia. Brain Res. 792, 105-113.
66. Xu, J., Fan, G., Chen, S., Wu, Y., Xu, X.M., and Hsu, C.Y. (1998). Methylprednisolone inhibition of TNF-alpha expression and NF-kB activation after spinal cord injury in rats. Brain Res. Mol. Brain Res. 59, 135-142.
67. Zawadzka, M., and Kaminska, B. (2005). A novel mechanism of FK506-mediated neuroprotection: downregulation of cytokine expression in glial cells. Glia 49, 36-51.
68. Zwijnenburg, P.J., Polfliet, M.M., Florquin, S., van den Berg, T.K., Dijkstra, C.D., van Deventer, S.J., Roord, J.J., van der, P.T., and van Furth, A.M. (2003). CXC-chemokines KC and macrophage inflammatory protein-2 (MIP-2) synergistically induce leukocyte recruitment to the central nervous system in rats. Immunol. Lett. 85, 1-4.