Increased circulating leukocyte numbers and altered macrophage phenotype correlate with the altered immune response to brain injury in metallothionein (MT) -I/II null mutant mice

Journal of Neuroinflammation

Volumn 8, Issue , 2011, Pages

  Pankhurst, Michael W ^a,b   Bennett, William ^a   Kirkcaldie, Matthew T K ^c   West, Adrian K ^a   Chung, Roger S ^a  

^a UNIVERSITY OF TASMANIA   (Australia)

^b UNIVERSITY OF OTAGO   (New Zealand)

^c UNIVERSITY OF TASMANIA   (Australia)

Author keywords

Alternatively activated macrophages; Brain injury; Cryolesion; Metallothionein

Indexed keywords

CD3 ANTIBODY; GAMMA INTERFERON; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; INTERLEUKIN 2; METALLOTHIONEIN; METALLOTHIONEIN I; METALLOTHIONEIN II; TRANSCRIPTION FACTOR FOXP3; CHEMOKINE; CYTOKINE; NEUROPROTECTIVE AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; BRAIN INJURY; CD3+ T LYMPHOCYTE; CD4 LYMPHOCYTE COUNT; CD4+ CD25+ T LYMPHOCYTE; CELL DEATH; CONTROLLED STUDY; DISEASE COURSE; FLOW CYTOMETRY; IMMUNE RESPONSE; IMMUNOASSAY; IMMUNOCYTOCHEMISTRY; IMMUNOMODULATION; LEUKOCYTE COUNT; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MALE; MOUSE; NERVE CELL; NEUROPROTECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE; ANIMAL; BLOOD; CYTOLOGY; GENETICS; IMMUNOLOGY; LEUKOCYTE; METABOLISM; MOUSE MUTANT; PATHOLOGY;

ANIMALS; ASTROCYTES; BRAIN INJURIES; CHEMOKINES; CYTOKINES; LEUKOCYTE COUNT; LEUKOCYTES; MACROPHAGES; MALE; METALLOTHIONEIN; MICE; MICE, KNOCKOUT; NEURONS; NEUROPROTECTIVE AGENTS;

EID: 82755195803     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-8-172     Document Type: Article

References (42)

1. Natale JE, Knight JB, Cheng Y, Rome JE, Gallo V. Metallothionein I and II mitigate age-dependent secondary brain injury. J Neurosci Res 2004, 78:303-314. 10.1002/jnr.20265, 15389833.
2. Penkowa M, Carrasco J, Giralt M, Moos T, Hidalgo J. CNS wound healing is severely depressed in metallothionein I and II-deficient mice. J Neurosci 1999, 19:2535-2545.
3. Potter EG, Cheng Y, Natale JE. Deleterious Effects of Minocycline After In Vivo Target Deprivation of Thalamocortical Neurons in the Immature, Metallothionein-deficient Mouse Brain. J Neurosci Res 2009, 87:1356-1368. 10.1002/jnr.21963, 19115404.
4. Dineley KE, Scanlon JM, Kress GJ, Stout AK, Reynolds IJ. Astrocytes are more resistant than neurons to the cytotoxic effects of increased [Zn2+](i). Neurobiol Dis 2000, 7:310-320. 10.1006/nbdi.2000.0303, 10964603.
5. Suzuki Y, Apostolova MD, Cherian MG. Astrocyte cultures from transgenic mice to study the role of metallothionein in cytotoxicity of tert-butyl hydroperoxide. Toxicology 2000, 145:51-62. 10.1016/S0300-483X(99)00220-6, 10771131.
6. Chung RS, Vickers JC, Chuah MI, West AK. Metallothionein-IIA promotes initial neurite elongation and postinjury reactive neurite growth and facilitates healing after focal cortical brain injury. J Neurosci 2003, 23:3336-3342.
7. Penkowa M, Giralt M, Moos T, Thomsen PS, Hernandez J, Hidalgo J. Impaired inflammatory response to glial cell death in genetically metallothionein-I- and -II-deficient mice. Exp Neurol 1999, 156:149-164. 10.1006/exnr.1998.7009, 10192786.
8. Potter EG, Cheng Y, Knight JB, Gordish-Dressman H, Natale JE. Metallothionein I and II attenuate the thalamic microglial response following traumatic axotomy in the immature brain. J Neurotrauma 2007, 24:28-42. 10.1089/neu.2006.0056.R1, 17263668.
9. Crowthers KC, Kline V, Giardina C, Lynes MA. Augmented humoral immune function in metallothionein-null mice. Toxicol Appl Pharmacol 2000, 166:161-172. 10.1006/taap.2000.8961, 10906280.
10. Canpolat E, Lynes MA. In vivo manipulation of endogenous metallothionein with a monoclonal antibody enhances a T-dependent humoral immune response. Toxicol Sci 2001, 62:61-70.
11. Lynes MA, Borghesi LA, Youn JH, Olson EA. Immunomodulatory activities of extracellular metallothionein. 1. Metallothionein effects on antibody-production. Toxicology 1993, 85:161-177. 10.1016/0300-483X(93)90040-Y, 8303711.
12. Mita M, Imura N, Kumazawa Y, Himeno S. Suppressed proliferative response of spleen T cells from metallothionein null mice. Microbiol Immunol 2002, 46:101-107.
13. Borghesi LA, Youn J, Olson EA, Lynes MA. Interactions of metallothionein with murine lymphocytes: Plasma membrane binding and proliferation. Toxicology 1996, 108:129-140. 10.1016/S0300-483X(95)03243-9, 8644111.
14. Emeny RT, Marusov G, Lawrence DA, Pederson-Lane J, Yin X, Lynes MA. Manipulations of metallothionein gene dose accelerate the response to Listeria monocytogenes. Chem Biol Interact 2009, 181:243-253. 10.1016/j.cbi.2009.06.018, 19576872.
15. Stirling DP, Yong VW. Dynamics of the inflammatory response after murine spinal cord injury revealed by flow cytometry. J Neurosci Res 2008, 86:1944-1958. 10.1002/jnr.21659, 18438914.
16. Czigner A, Mihaly A, Farkas O, Buki A, Krisztin-Peva B, Dobo E, Barzo P. Kinetics of the cellular immune response following closed head injury. Acta Neurochirurgica 2007, 149:281-289. 10.1007/s00701-006-1095-8, 17288002.
17. Clausen F, Lorant T, Lewen A, Hillered L. T lymphocyte trafficking: A novel target for neuroprotection in traumatic brain injury. J Neurotrauma 2007, 24:1295-1307. 10.1089/neu.2006.0258, 17711391.
18. Sroga JM, Jones TB, Kigerl KA, McGaughy VM, Popovich PG. Rats and mice exhibit distinct inflammatory reactions after spinal cord injury. J Comp Neurol 2003, 462:223-240. 10.1002/cne.10736, 12794745.
19. Bezzi P, Domercq M, Brambilla L, Galli R, Schols D, De Clercq E, Vescovi A, Bagetta G, Kollias G, Meldolesi J, Volterra A. CXCR4-activated astrocyte glutamate release via TNFa: amplification by microglia triggers neurotoxicity. Nat Neurosci 2001, 4:702-710. 10.1038/89490, 11426226.
20. Desagher S, Glowinski J, Premont J. Astrocytes protect neurons from hydrogen peroxide toxicity. J Neurosci 1996, 16:2553-2562.
21. Hu JR, Ferreira A, VanEldik LJ. S100 beta induces neuronal cell death through nitric oxide release from astrocytes. J Neurochem 1997, 69:2294-2301.
22. Mosmann TR, Cherwinski H, Bond MW, Giedlin MA, Coffman RL. 2 types of murine helper T-cell clone. 1. Definition according to profiles of lymphokine activities and secreted proteins. J Immunol 1986, 136:2348-2357.
23. Mills CD, Kincaid K, Alt JM, Heilman MJ, Hill AM. M-1/M-2 macrophages and the Th1/Th2 paradigm. J Immunol 2000, 164:6166-6173.
24. 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.
25. Huh S, Lee K, Yun HS, Paik DJ, Kim JM, Youn J. Functions of metallothionein generating interleukin-10-producing regulatory CD4(+) T cells potentiate suppression of collagen-induced arthritis. J Microbiol Biotech 2007, 17:348-358.
26. Masters BA, Kelly EJ, Quaife CJ, Brinster RL, Palmiter RD. Targeted disruption of metallothionein-i and metallothionein-II genes increases sensitivity to cadmium. Proc Natl Acad Sci USA 1994, 91:584-588. 10.1073/pnas.91.2.584, 42993, 8290567.
27. Ling CY, Sandor M, Suresh M, Fabry Z. Traumatic injury and the presence of antigen differentially contribute to T-cell recruitment in the CNS. J Neurosci 2006, 26:731-741. 10.1523/JNEUROSCI.3502-05.2006, 16421293.
28. Schmued LC, Stowers CC, Scallet AC, Xu LL. Fluoro-Jade C results in ultra high resolution and contrast labeling of degenerating neurons. Brain Res 2005, 1035:24-31. 10.1016/j.brainres.2004.11.054, 15713273.
29. Brettingham-Moore KH, Rao S, Juelich T, Shannon MF, Holloway AF. GM-CSF promoter chromatin remodelling and gene transcription display distinct signal and transcription factor requirements. Nucleic Acids Research 2005, 33:225-234. 10.1093/nar/gki161, 546149, 15647505.
30. Liesz A, Suri-Payer E, Veltkamp C, Doerr H, Sommer C, Rivest S, Giese T, Veltkamp R. Regulatory T cells are key cerebroprotective immunomodulators in acute experimental stroke. Nat Med 2009, 15:192-199. 10.1038/nm.1927, 19169263.
31. Byram SC, Carson MJ, DeBoy CA, Serpe CJ, Sanders VM, Jones KJ. CD4-positive T cell-mediated neuroprotection requires dual compartment antigen presentation. J Neurosci 2004, 24:4333-4339. 10.1523/JNEUROSCI.5276-03.2004, 2665301, 15128847.
32. DeFelipe J, Alonso-Nanclares L, Arellano JI. Microstructure of the neocortex: Comparative aspects. J Neurocytol 2002, 31:299-316. 10.1023/A:1024130211265, 12815249.
33. Youn J, Lynes MA. Metallothionein-induced suppression of cytotoxic T lymphocyte function: an important immunoregulatory control. Toxicol Sci 1999, 52:199-208. 10.1093/toxsci/52.2.199, 10630572.
34. Youn J, Borghesi LA, Olson EA, Lynes MA. Immunomodulatory activities of extracellular metallothionein. II. Effects on macrophage functions. J Toxicol Env Health 1995, 45:397-413.
35. Kukačka J, Vajtr D, Huska D, Prusa R, Houstava L, Samal F, Diopan V, Kotaska K, Kizek R. Blood metallothionein, neuron specific enolase, and protein S100B in patients with traumatic brain injury. Neuroendocrinol Lett 2006, 27:116-120.
36. Aydemir TB, Blanchard RK, Cousins RJ. Zinc supplementation of young men alters metallothionein, zinc transporter, and cytokine gene expression in leukocyte populations. Proc Natl Acad Sci USA 2006, 103:1699-1704. 10.1073/pnas.0510407103, 1413653, 16434472.
37. McClain CJ, Twyman DL, Ott LG, Rapp RP, Tibbs PA, Norton JA, Kasarskis EJ, Dempsey RJ, Young B. Serum and urine zinc response in head-injured patients. J Neurosurg 1986, 64:224-230. 10.3171/jns.1986.64.2.0224, 3944632.
38. Raes G, De Baetselier P, Noel W, Beschin A, Brombacher F, Hassanzadeh G. Differential expression of FIZZ1 and Ym1 in alternatively versus classically activated macrophages. J Leukocyte Biol 2002, 71:597-602.
39. Kwidzinski E, Bechmann I. IDO expression in the brain: a double-edged sword. J Mol Med 2007, 85:1351-1359. 10.1007/s00109-007-0229-7, 17594069.
40. Yadav MC, Burudi EME, Alirezaei M, Flynn CC, Lanigan CM, Fox HS. IFN-gamma-induced IDO and WRS expression in microglia is differentially regulated by IL-4. Glia 2007, 55:1385-1396. 10.1002/glia.20544, 2486430, 17661345.
41. Chung RS, Leung YK, Butler CW, Chen Y, Eaton ED, Pankhurst MW, West AK, Guillemin GJ. Metallothionein Treatment Attenuates Microglial Activation and Expression of Neurotoxic Quinolinic Acid Following Traumatic Brain Injury. Neurotox Res 2009, 15:381-389. 10.1007/s12640-009-9044-y, 19384571.
42. Malek TR. The Biology of Interleukin-2. Annu Rev Immunol 2008, 26:453-79. 10.1146/annurev.immunol.26.021607.090357, 18062768.