TREM2-transduced myeloid precursors mediate nervous tissue debris clearance and facilitate recovery in an animal model of multiple sclerosis

PLoS Medicine

Volumn 4, Issue 4, 2007, Pages 675-689

  Takahashi, Kazuya ^a,b   Prinz, Marco ^c   Stagi, Massimiliano ^a,b,d   Chechneva, Olga ^a   Neumann, Harald ^a,b,d  

^a UNIVERSITY OF BONN   (Germany)

^b EUROPEAN NEUROSCIENCE INSTITUTE   (Germany)

^c UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^d UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL RECEPTOR; TRIGGERING RECEPTOR EXPRESSED ON MYELOID CELLS 2; UNCLASSIFIED DRUG; CYTOKINE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN RECEPTOR; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; MEMBRANE PROTEIN; NOS2 PROTEIN, MOUSE; SYNTHETIC DNA; TREM2 PROTEIN, MOUSE;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CONTROLLED STUDY; FEMALE; GENETIC TRANSDUCTION; MOUSE; MULTIPLE SCLEROSIS; NERVOUS TISSUE; NONHUMAN; PHAGOCYTOSIS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TISSUE INJURY; ANIMAL; APOPTOSIS; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOTION; DISEASE MODEL; DRUG EFFECT; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENE THERAPY; GENE VECTOR; GENETICS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; LENTIVIRINAE; MICROGLIA; MONOCYTE; NERVE CELL; PATHOLOGY; PHYSIOLOGY; PROMOTER REGION; REPORTER GENE; TRANSPLANTATION;

ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOVEMENT; CELLS, CULTURED; CYTOKINES; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENES, REPORTER; GENES, SYNTHETIC; GENETIC THERAPY; GENETIC VECTORS; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; INTERLEUKIN-10; LENTIVIRUS; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICROGLIA; MONOCYTES; MULTIPLE SCLEROSIS; MYELOID CELLS; NEURONS; NITRIC OXIDE SYNTHASE TYPE II; PHAGOCYTOSIS; PROMOTER REGIONS, GENETIC; RECEPTORS, IMMUNOLOGIC; TRANSDUCTION, GENETIC;

EID: 34247500821     PISSN: 15491277     EISSN: 15491676     Source Type: Journal    
DOI: 10.1371/journal.pmed.0040124     Document Type: Article

References (49)

1. Hickey WF, Kimura H (1988) Perivascular microglial cells of the CNS are bone marrow-derived and present antigen in vivo. Science 239: 290-292.
2. Priller J, Flugel A, Wehner T, Boentert M, Haas CA, et al. (2001) Targeting gene-modified hematopoietic cells to the central nervous system: Use of green fluorescent protein uncovers microglial engraftment. Nat Med 7: 1356-1361.
3. Simard AR, Rivest S (2004) Bone marrow stem cells have the ability to populate the entire central nervous system into fully differentiated parenchymal microglia. FASEB J 18: 998-1000.
4. Flugel A, Bradl M, Kreutzberg GW, Graeber MB (2001) Transformation of donor-derived bone marrow precursors into host microglia during autoimmune CNS inflammation and during the retrograde response to axotomy. J Neurosci Res 66: 74-82.
5. Bechmann I, Goldmann J, Kovac AD, Kwidzinski E, Simburger E, et al. (2005) Circulating monocytic cells infiltrate layers of anterograde axonal degeneration where they transform into microglia. FASEB J. 19: 647-649
6. Malm TM, Koistinaho M, Parepalo M, Vatanen T, Ooka A, et al. (2005) Bone-marrow-derived cells contribute to the recruitment of microglial cells in response to beta-amyloid deposition in APP/PS1 double transgenic Alzheimer mice. Neurobiol Dis 18: 134-142.
7. Stalder AK, Ermini F, Bondolfi L, Krenger W, Burbach GJ, et al. (2005) Invasion of hematopoietic cells into the brain of amyloid precursor protein transgenic mice. J Neurosci 25: 11125-11132.
8. Santambrogio L, Belyanskaya SL, Fischer FR, Cipriani B, Brosnan CF, et al. (2001) Developmental plasticity of CNS microglia. Proc Natl Acad Sci U S A 98: 6295-6300.
9. Servet-Delprat C, Arnaud S, Jurdic P, Nataf S, Grasset MF, et al. (2002) Flt3+ macrophage precursors commit sequentially to osteoclasts, dendritic cells and microglia. BMC Immunol 3: 15.
10. Asheuer M, Pflumio F, Benhamida S, Dubart-Kupperschmitt A, Fouquet F, et al. (2004) Human CD34+ cells differentiate into microglia and express recombinant therapeutic protein. Proc Natl Acad Sci U S A 101: 3557-3562.
11. Voll RE, Herrmann M, Roth EA, Stach C, Kalden JR, et al. (1997) Immunosuppressive effects of apoptotic cells. Nature 390: 350-351.
12. Savill J, Dransfield I, Gregory C, Haslett C (2002) A blast from the past: Clearance of apoptotic cells regulates immune responses. Nat Rev Immunol 2: 965-975.
13. Serhan CN, Savill J (2005) Resolution of inflammation: The beginning programs the end. Nat Immunol 6: 1191-1197.
14. Takahashi K, Rochford CD, Neumann H (2005) Clearance of apoptotic neurons without inflammation by microglial triggering receptor expressed on myeloid cells-2. J Exp Med 201: 647-657.
15. Prat A, Antel J (2005) Pathogenesis of multiple sclerosis. Curr Opin Neurol 18: 225-230.
16. Carson MJ (2002) Microglia as liaisons between the immune and central nervous systems: Functional implications for multiple sclerosis. Glia 40: 218-231.
17. Heppner FL, Greter M, Marino D, Falsig J, Raivich G, et al. (2005) Experimental autoimmune encephalomyelitis repressed by microglial paralysis. Nat Med 11: 146-152.
18. Platten M, Steinman L (2005) Multiple sclerosis: Trapped in deadly glue. Nat Med 11: 252-253.
19. Willenbring H, Bailey AS, Foster M, Akkari Y, Dorrell C, et al. (2004) Myelomonocytic cells are sufficient for therapeutic cell fusion in liver. Nat Med 10: 744-748.
20. Prinz M, Garbe F, Schmidt H, Mildner A, Gutcher I, et al. (2006) Innate immunity mediated by TLR9 modulates pathogenicity in an animal model of multiple sclerosis. J Clin Invest 116: 456-464.
21. Colonna M (2003) TREMs in the immune system and beyond. Nat Rev Immunol 3: 445-453.
22. Matsuo A, Lee GC, Terai K, Takami K, Hickey WF, et al. (1997) Unmasking of an unusual myelin basic protein epitope during the process of myelin degeneration in humans: A potential mechanism for the generation of autoantigens. Am J Pathol 150: 1253-1266.
23. Paloneva J, Autti T, Raininko R, Partanen J, Salonen O, et al. (2001) CNS manifestations of Nasu-Hakola disease: A frontal dementia with bone cysts. Neurology 56: 1552-1558.
24. Paloneva J, Mandelin J, Kiialainen A, Bohling T, Prudlo J, et al. (2003) DAP12/TREM2 deficiency results in impaired osteoclast differentiation and osteoporotic features. J Exp Med 198: 669-675.
25. Paloneva J, Manninen T, Christman G, Hovanes K, Mandelin J, et al. (2002) Mutations in two genes encoding different subunits of a receptor signaling complex result in an identical disease phenotype. Am J Hum Genet 71: 656-662.
26. Schmid CD, Sautkulis LN, Danielson PE, Cooper J, Hasel KW, et al. (2002) Heterogeneous expression of the triggering receptor expressed on myeloid cells-2 on adult murine microglia. J Neurochem 83: 1309-1320.
27. Cella M, Buonsanti C, Strader C, Kondo T, Salmaggi A, et al. (2003) Impaired differentiation of osteoclasts in TREM-2-deficient individuals. J Exp Med 198: 645-651.
28. Turnbull IR, Gilfillan S, Cella M, Aoshi T, Miller M, et al. (2006) Cutting edge: TREM-2 attenuates macrophage activation. J Immunol 177: 3520-3524.
29. Bauer J, Sminia T, Wouterlood FG, Dijkstra CD (1994) Phagocytic activity of macrophages and microglial cells during the course of acute and chronic relapsing experimental autoimmune encephalomyelitis. J Neurosci Res 38: 365-375.
30. Kotter MR, Zhao C, van Rooijen N, Franklin RJ (2005) Macrophage-depletion induced impairment of experimental CNS remyelination is associated with a reduced oligodendrocyte progenitor cell response and altered growth factor expression. Neurobiol Dis 18: 166-175.
31. Zhao C, Fancy SP, Kotter MR, Li WW, Franklin RJ (2005) Mechanisms of CNS remyelination-The key to therapeutic advances. J Neurol Sci 233: 87-91.
32. Schwab ME (2004) Nogo and axon regeneration. Curr Opin Neurobiol 14: 118-124.
33. Kerschensteiner M, Bareyre FM, Buddeberg BS, Merkler D, Stadelmann C, et al. (2004) Remodeling of axonal connections contributes to recovery in an animal model of multiple sclerosis. J Exp Med 200: 1027-1038.
34. Jander S, Pohl J, D'Urso D, Gillen C, Stoll G (1998) Time course and cellular localization of interleukin-10 mRNA and protein expression in autoimmune inflammation of the rat central nervous system. Am J Pathol 152: 975-982.
35. Bettelli E, Das MP, Howard ED, Weiner HL, Sobel RA, et al. (1998) IL-10 is critical in the regulation of autoimmune encephalomyelitis as demonstrated by studies of IL-10- and IL-4-deficient and transgenic mice. J Immunol 161: 3299-3306.
36. McGeachy MJ, Stephens LA, Anderton SM (2005) Natural recovery and protection from autoimmune encephalomyelitis: Contribution of CD4+CD25+ regulatory cells within the central nervous system. J Immunol 175: 3025-3032.
37. Cua DJ, Hutchins B, LaFace DM, Stohlman SA, Coffman RL (2001) Central nervous system expression of IL-10 inhibits autoimmune encephalomyelitis. J Immunol 166: 602-608.
38. Bakker AB, Hoek RM, Cerwenka A, Blom B, Lucian L, et al. (2000) DAP12-deficient mice fail to develop autoimmunity due to impaired antigen priming. Immunity 13: 345-353.
39. Steinman L (2001) Multiple sclerosis: A two-stage disease. Nat Immunol 2: 762-764.
40. Zamvil SS, Steinman L (2003) Diverse targets for intervention during inflammatory and neurodegenerative phases of multiple sclerosis. Neuron 38: 685-688.
41. Arnold DL (2005) Changes observed in multiple sclerosis using magnetic resonance imaging reflect a focal pathology distributed along axonal pathways. J Neurol 252: v25-v29.
42. Lim ET, Sellebjerg F, Jensen CV, Altmann DR, Grant D, et al. (2005) Acute axonal damage predicts clinical outcome in patients with multiple sclerosis. Mult Scler 11: 532-536.
43. Evavold BD, Sloan-Lancaster J, Allen PM (1993) Tickling the TCR: Selective T-cell functions stimulated by altered peptide ligands. Immunol Today 14: 602-609.
44. Nicholson LB, Greer JM, Sobel RA, Lees MB, Kuchroo VK (1995) An altered peptide ligand mediates immune deviation and prevents autoimmune encephalomyelitis. Immunity 3: 397-405.
45. Youssef S, Stuve O, Patarroyo JC, Ruiz PJ, Radosevich JL, et al. (2002) The HMG-CoA reductase inhibitor, atorvastatin, promotes a Th2 bias and reverses paralysis in central nervous system autoimmune disease. Nature 420: 78-84.
46. Garren H, Ruiz PJ, Watkins TA, Fontoura P, Nguyen LT, et al. (2001) Combination of gene delivery and DNA vaccination to protect from and reverse Th1 autoimmune disease via deviation to the Th2 pathway. Immunity 15: 15-22.
47. Flugel A, Matsumuro K, Neumann H, Klinkert WE, Birnbacher R, et al. (2001) Anti-inflammatory activity of nerve growth factor in experimental autoimmune encephalomyelitis: Inhibition of monocyte transendothelial migration. Eur J Immunol 31: 11-22.
48. Pluchino S, Quattrini A, Brambilla E, Gritti A, Salani G, et al. (2003) Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature 422: 688-694.
49. Pluchino S, Zanotti L, Rossi B, Brambilla E, Ottoboni L, et al. (2005) Neurosphere-derived multipotent precursors promote neuroprotection by an immunomodulatory mechanism. Nature 436: 266-271.