Differences in origin of reactive microglia in bone marrow chimeric mouse and rat after transient global ischemia

Journal of Neuropathology and Experimental Neurology

Volumn 70, Issue 6, 2011, Pages 481-494

  Lambertsen, Kate L ^a   Deierborg, Tomas ^b   Gregersen, Rikke ^a   Clausen, Bettina H ^a   Wirenfeldt, Martin ^a   Nielsen, Helle H ^a   Dalmau, Ishar ^a   Diemer, Nils H ^a   Dagnaes Hansen, Frederik ^d   Johansen, Flemming F ^c   Keating, Armand ^e   Finsen, Bente ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b LUND UNIVERSITY   (Sweden)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d AARHUS UNIVERSITY   (Denmark)

^e PRINCESS MARGARET HOSPITAL   (Canada)

Author keywords

Blood brain barrier; Bone marrow chimeras; Claudin 5; Green fluorescence protein; Hippocampal formation; Major histocompatibility complex class I; Transient global cerebral ischemia

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BONE MARROW CELL; CONTROLLED STUDY; HIPPOCAMPUS; MALE; MICROGLIA; NERVE FIBER DEGENERATION; NONHUMAN; PRIORITY JOURNAL; RAT; TRANSIENT ISCHEMIC ATTACK;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIGENS, CD11B; ANTIGENS, CD45; ANTIGENS, NEOPLASM; BONE MARROW; BONE MARROW CELLS; BONE MARROW TRANSPLANTATION; DISEASE MODELS, ANIMAL; GREEN FLUORESCENT PROTEINS; HISTOCOMPATIBILITY ANTIGENS CLASS I; ISCHEMIC ATTACK, TRANSIENT; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICROGLIA; ORGANIC CHEMICALS; RATS; RATS, INBRED LEW; RATS, WISTAR; TIME FACTORS;

EID: 79957472286     PISSN: 00223069     EISSN: 15546578     Source Type: Journal    
DOI: 10.1097/NEN.0b013e31821db3aa     Document Type: Article

References (65)

1. Theele DP, Streit WJ. A chronicle of microglial ontogeny. Glia 1993;7: 5-8
2. Dalmau I, Vela JM, Gonzalez B, et al. Expression of purine metabolismY related enzyme by microglial cells in the developing rat brain. J Comp Neurol 1998;398:333-46 (Pubitemid 28360038)
3. Bianchin MM, Capella HM, Chaves DL, et al. Nasu-Hakola disease (polycystic lipomembranous osteodysplasia with sclerosing leukoencephalopathyYPLOSL): A dementia associated with bone cystic lesions. From clinical to genetic and molecular aspects. Cell Mol Neurobiol 2004;24:1-24 (Pubitemid 38233726)
4. Takahashi K, Rochford CD, Neumann H. Clearance of apoptotic neurons without inflammation by microglial triggering receptor expressed on myeloid cells-2. J Exp Med 2005;201:647-57 (Pubitemid 40289554)
5. Finsen B, Lehrmann E, Castelanno B, et al. The role of microglial cells and brain macrophages in transient global cerebral ischemia. In: Ling E-A, Tan CK, eds. Tropical Issues in Microglial Research. Singapore, Singapore: Elsevier, 1996:297-318
6. Kreutzberg GW. Microglia: A sensor for pathological events in the CNS. Trends Neurosci 1996;19:312-18 (Pubitemid 26349059)
7. Nimmerjahn, A, Kirchhoff F, Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005; 308:1314-18 (Pubitemid 40746128)
8. Stoll G, Jander S. The role of microglia and macrophages in the patho-physiology of the CNS. Prog Neurobiol 1999;58:233-47 (Pubitemid 29193056)
9. Streit WJ, Walter SA, Pennell NA. Reactive microgliosis. Prog Neurobiol 1999;57:563-81 (Pubitemid 29148415)
10. Finsen BR, Jorgensen MB, Diemer NH, et al. Microglial MHC antigen expression after ischemic and kainic acid lesions of the adult rat hippocampus. Glia 1993;7:41-49
11. Zhang GX, Li J, Ventura E, et al. Parenchymal microglia of naive adult C57BL/6J mice express high levels of B7.1, B7.2, and MHC class II. Exp Mol Pathol 2002;73:35-45 (Pubitemid 34775456)
12. Lehrmann E, Molinari A, Speciale C, et al. Immunohistochemical visualization of newly formed quinolinate in the normal and excitotoxically lesioned rat striatum. Exp Brain Res 2001;141:389-97 (Pubitemid 33071184)
13. Raivich G, Banati R. Brain microglia and blood-derived macrophages: Molecular profiles and functional roles in multiple sclerosis and animal models of autoimmune demyelinating disease. Brain Res Brain Res Rev 2004;46:261-81 (Pubitemid 39574328)
14. Lambertsen KL, Clausen BH, Babcock AA, et al. Microglia protect neurons against ischemia by synthesis of tumor necrosis factor. J Neu-rosci 2009;29:1319-30
15. Bechmann I, Goldmann J, Kovac AD, et al. Circulating monocytic cells infiltrate layers of anterograde axonal degeneration where they transform into microglia. FASEB J 2005;19:647-49 (Pubitemid 40471273)
16. Clausen BH, Lambertsen KL, Babcock AA, et al. Interleukin-1A and tumor necrosis factor-> are expressed by different subsets of micro-glia and macrophages after ischemic stroke in mice. J Neuroinflamm 2008;5:46
17. Ladeby R, Wirenfeldt M, Dalmau I, et al. Proliferating resident microglia express the stem cell antigen CD34 in response to acute neural injury. Glia 2005;50:121-31 (Pubitemid 40695266)
18. Priller J, Flugel A, Wehner T, et al. Targeting gene-modified hema-topoietic cells to the central nervous system: Use of green fluorescent protein uncovers microglial engraftment. Nat Med 2001;7:1356-61 (Pubitemid 34007942)
19. Schilling M, Besselmann M, Leonhard C, et al. Microglial activation precedes and predominates over macrophage infiltration in transient focal cerebral ischemia: A study in green fluorescent protein transgenic bone marrow chimeric mice. Exp Neurol 2003;183:25-33 (Pubitemid 37075853)
20. Wirenfeldt M, Babcock AA, Ladeby R, et al. Reactive microgliosis engages distinct responses by microglial subpopulations after minor central nervous system injury. J Neurosci Res 2005;82:507-14 (Pubitemid 41579350)
21. Wirenfeldt M, Dissing-Olesen L, Babcock AA, et al. Population control of resident and immigrant microglia by mitosis and apoptosis. Am J Pathol 2007;171:617-31 (Pubitemid 47344694)
22. Lawson LJ, Perry VH, Gordon S. Turnover of resident microglia in the normal adult mouse brain. Neuroscience 1992;48:405-15
23. Vallieres L, Sawchenko PE. Bone marrowYderived cells that populate the adult mouse brain preserve their hematopoietic identity. J Neurosci 2003; 23:5197-207 (Pubitemid 36793248)
24. Massengale M, Wagers AJ, Vogel H, et al. Hematopoietic cells maintain hematopoietic fates upon entering the brain. J Exp Med 2005;201: 1579-89 (Pubitemid 40721003)
25. Soulet D, Rivest S. Bone-marrowYderived microglia: Myth or reality? Curr Opin Pharmacol 2008;8:257-68
26. Ajami B, Bennett JL, Krieger C, et al. Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat Neurosci 2007;10:1538-43 (Pubitemid 350175883)
27. Ginhoux F, Greter M, Leboeuf M, et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 2010; 330:841-45
28. Mildner A, Schmidt H, Nitsche M, et al. Microglia in the adult brain arise from Ly-6ChiCCR2+ monocytes only under defined host conditions. Nat Neurosci 2007;10:1544-53 (Pubitemid 350175884)
29. Ling EA. Electron microscopic study of macrophages appearing in a stab wound of the brain of rats following intravenous injection of carbon particles. Arch Histol Jpn 1979;42:41-50 (Pubitemid 9104840)
30. Albini TA, Wang RC, Reiser B, et al. Microglial stability and repopula-tion in the retina. Br J Ophthalmol 2005;89:901-3
31. + T cells compared. J Immunol 1995;154:4309-21
32. Lassmann H, Schmied M, Vass K, et al. Bone marrow derived elements and resident microglia in brain inflammation. Glia 1993;7:19-24
33. Matsumoto Y, Fujiwara M. Absence of donor-type major histocompa-tibility complex class I antigen-bearing microglia in the rat central nervous system of radiation bone marrow chimeras. J Neuroimmunol 1987; 17:71-82 (Pubitemid 18017111)
34. 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;60:676-85 (Pubitemid 32619790)
35. Jorgensen MB, Finsen BR, Jensen MB, et al. Microglial and astroglial reactions to ischemic and kainic acidYinduced lesions of the adult rat hippocampus. Exp Neurol 1993;120:70-88 (Pubitemid 23114031)
36. Deierborg T, Wieloch T, Diano S, et al. Overexpression of UCP2 protects thalamic neurons following global ischemia in the mouse. J Cereb Blood Flow Metab 2008;28:1186-95 (Pubitemid 351733358)
37. Jensen MB, Finsen B, Zimmer J. Morphological and immunophenotypic microglial changes in the denervated fascia dentate of adult rats: Correlation with blood-brain barrier damage and astroglial reactions. Exp Neurol 1997;143:103-16 (Pubitemid 27049135)
38. Abe T, Shimada S, Osako R. Chronic runt disease in rats: Clinical and pathologic studies. J Natl Cancer Inst 1969;43:459-67
39. Lubaroff DM, Silvers WK. Susceptibility of parental strain and F1 hybrid rats to runt disease. Transplantation 1970;10:302-8
40. von der Maase H, Overgaard J. Microcolony survival assay for jejunal crypt cells exposed to radiation alone and combined with cancer che-motherapeutic agentsVMethodological problems. Int J Radiat Biol Relat Stud Phys Chem Med 1983;43:45-56 (Pubitemid 13174452)
41. Olsson T, Wieloch T, Smith ML. Brain damage in a mouse model of global cerebral ischemia. Effect of NMDA receptor blockade. Brain Res 2003;982:260-69
42. Jorgensen MB, Diemer NH. Selective neuron loss after cerebral ischemia in the rat: Possible role of transmitter glutamate. Acta Neurol Scand 1982; 66:536-46 (Pubitemid 12037474)
43. Pulsinelli WA, Brierley JB, Plum F. Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann Neurol 1982;11:491-98 (Pubitemid 12158810)
44. Gregersen R, Lambertsen K, Finsen B. Microglia and macrophages are the major source of tumor necrosis factor in permanent middle cerebral artery occlusion in mice. J Cereb Blood Flow Metab 2000;20:53-65 (Pubitemid 30019830)
45. Lambertsen KL, Gregersen R, Drojdahl N, et al. A specific and sensitive method for visualization of tumor necrosis factor in the murine central nervous system. Brain Res Brain Res Protoc 2001;7:175-91 (Pubitemid 32448966)
46. Garcia-Ovejero D, Veiga S, Garcia-Segura LM, et al. Glial expression of estrogen and androgen receptors after rat brain injury. J Comp Neurol 2002;450:256-71 (Pubitemid 34809996)
47. Wellons JC 3rd, Sheng H, Laskowitz DT, et al. A comparison of strain-related susceptibility in two murine recovery models of global cerebral ischemia. Brain Res 2000;868:14-21 (Pubitemid 30332338)
48. Nadler JV, Perry BW, Gentry C, et al. Loss and reacquisition of hippo-campal synapses after selective destruction of CA3-CA4 afferents with kainic acid. Brain Res 1980;191:387-403 (Pubitemid 10103914)
49. Johansen FF, Tonder N, Zimmer J, et al. Short-term changes of parval-bumin and calbindin immunoreactivity in the rat hippocampus following cerebral ischemia. Neurosci Lett 1990;120:171-74
50. Kato H, Takahashi A, Itoyama Y. Cell cycle protein expression in proliferating microglia and astrocytes following transient global cerebral ischemia in the rat. Brain Res Bull 2003;60:215-21 (Pubitemid 36561542)
51. Inácio AR, Ruscher K, Leng L, et al. Macrophage migration inhibitory factor promotes cell death and aggravates neurologic deficits after experimental stroke. J Cereb Blood Flow Metab 2011;31:1093-106
52. Bolton SJ, Anthony DC, Perry VH. Loss of the tight junction proteins occludens-1 from cerebral vascular endothelium during neutrophil-induced blood-brain barrier breakdown in vivo. Neuroscience 1998;86:1245-57 (Pubitemid 28318549)
53. Willis CL, Meske DS, Davis TP. Protein kinase C activation modulates reversible increase in cortical blood-brain barrier permeability and tight junction protein expression during hypoxia and posthypoxic reoxygena-tion. J Cereb Blood Flow Metab 2010;30:1847-59
54. Ulvestad E, Williams K, Vedeler C, et al. Reactive microglia in multiple sclerosis lesions have an increased expression of receptors for the Fc part of IgG. J Neurol Sci 1994;121:125-31 (Pubitemid 24044876)
55. Peress NS, Fleit HB, Perillo E, et al. Identification of FcF RI, II and III on normal human brain ramified microglia and on microglia in senile plaques in Alzheimer's disease. J Neuroimmunol 1993;48:71-79
56. Suemitsu S, Watanabe M, Yokobayashi E, et al. FcF receptors contribute to pyramidal cell death in the mouse hippocampus following local kainic acid injection. Neuroscience 2010;166:819-31
57. Webster SD, Park M, Fonseca MI, et al. Structural and functional evidence for microglial expression of C1qR(P), the C1q receptor that enhances phagocytosis. J Leukoc Biol 2000;67:109-16 (Pubitemid 30046825)
58. Hickey WF, Vass K, Lassmann H. Bone marrowYderived elements in the central nervous system: An immunohistochemical and ultrastruc-tural survey of rat chimeras. J Neuropathol Exp Neurol 1992;51: 246-56
59. Chen J, Li Y, Wang L, et al. Therapeutic benefit of intracerebral transplantation of bone marrow stromal cells after cerebral ischemia in rats. J Neurol Sci 2001;189:49-57 (Pubitemid 32776649)
60. Furuya T, Tanaka R, Urabe T, et al. Establishment of modified chimeric mice using GFP bone marrow as a model for neurological disorders. Neuroreport 2003;14:629-31 (Pubitemid 36529004)
61. Cogle CR, Yachnis AT, Laywell ED, et al. Bone marrow transdiffer- entiation in brain after transplantation: A retrospective study. Lancet 2004;363:1432-37 (Pubitemid 38586719)
62. + cells differentiate into microglia and express recombinant therapeutic protein. Proc Natl Acad Sci USA 2004;101:3557-62 (Pubitemid 38338234)
63. Gelinas DS, DaSilva K, Fenili D, et al. Immunotherapy for Alzheimer's disease. Proc Natl Acad Sci USA 2004;101(Suppl 2):14657-62 (Pubitemid 39346739)
64. Salmaggi A, Maccagnano E, Musso A, et al. An Italian family with Nasu-Hakola disease. J Neurol 2003;250:878-80
65. Biffi A, De Palma M, Quattrini A, et al. Correction of metachromatic leukodystrophy in the mouse model by transplantation of genetically modified hematopoietic stem cells. J Clin Invest 2004;113:1118-29 (Pubitemid 38544097)