Temporal changes in monocyte and macrophage subsets and microglial macrophages following spinal cord injury in the lys-egfp-ki mouse model

Journal of Neuroimmunology

Volumn 261, Issue 1-2, 2013, Pages 7-20

  Thawer, Sakina G ^a,b   Mawhinney, Leah ^a,b   Chadwick, Kristin ^a   De Chickera, Sonali N ^a   Weaver, Lynne C ^a   Brown, Arthur ^a,b   Dekaban, Gregory A ^a,b  

^a ROBARTS RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Classical inflammatory monocytes; Lys EGFP ki mouse; M1 M2 macrophage polarization; Non classical monocytes

Indexed keywords

CD86 ANTIGEN; GLYCOPROTEIN P 15095; L SELECTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; FEMALE; HEMATOGENOUS MACROPHAGE; MACROPHAGE; MALE; MICROGLIAL MACROPHAGE; MONOCYTE; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD INJURY;

CLASSICAL INFLAMMATORY MONOCYTES; LYS-EGFP-KI MOUSE; M1/M2 MACROPHAGE POLARIZATION; NON-CLASSICAL MONOCYTES;

ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; FLOW CYTOMETRY; GREEN FLUORESCENT PROTEINS; MACROPHAGES; MALE; MICE; MICE, TRANSGENIC; MICROGLIA; MONOCYTES; MURAMIDASE; SPINAL CORD INJURIES; TIME FACTORS;

EID: 84880790410     PISSN: 01655728     EISSN: 18728421     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2013.04.008     Document Type: Article

References (54)

1. Ankeny D.P., Guan Z., Popovich P.G. B cells produce pathogenic antibodies and impair recovery after spinal cord injury in mice. J. Clin. Invest. 2009, 119:2990-2999.
2. Auffray C., Fogg D., Garfa M., Elain G., Join-Lambert O., Kayal S., Sarnacki S., Cumano A., Lauvau G., Geissmann F. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 2007, 317:666-670.
3. Auffray C., Sieweke M.H., Geissmann F. Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu. Rev. Immunol. 2009, 27:669-692.
4. Bethea J.R., Dietrich W.D. Targeting the host inflammatory response in traumatic spinal cord injury. Curr. Opin. Neurol. 2002, 15:355-360.
5. Casella G., Berger R.L. Statistical Inference 2002, Duxbury Press, Pacific Grove, CA.
6. David S., Kroner A. Repertoire of microglial and macrophage responses after spinal cord injury. Nat. Rev. Neurosci. 2011, 12:388-399.
7. Davoust N., Vuaillat C., Androdias G., Nataf S. From bone marrow to microglia: barriers and avenues. Trends Immunol. 2008, 29:227-234.
8. de Rivero Vaccari J.P., Bastien D., Yurcisin G., Pineau I., Dietrich W.D., De Koninck Y., Keane R.W., Lacroix S. P2X4 receptors influence inflammasome activation after spinal cord injury. J. Neurosci. 2012, 32:3058-3066.
9. Dominguez P.M., Ardavin C. Differentiation and function of mouse monocyte-derived dendritic cells in steady state and inflammation. Immunol. Rev. 2010, 234:90-104.
10. Donovan J.A., Koretzky G.A. CD45 and the immune response. J. Am. Soc. Nephrol. 1993, 4:976-985.
11. Donnelly D.J., Popovich P.G. Inflammation and its role in neuroprotection, axonal regeneration and functional recovery after spinal cord injury. Exp. Neurol. 2008, 209:378-388.
12. Donnelly D.J., Longbrake E.E., Shawler T.M., Kigerl K.A., Lai W., Tovar C.A., Ransohoff R.M., Popovich P.G. Deficient CX3CR1 signaling promotes recovery after mouse spinal cord injury by limiting the recruitment and activation of Ly6Clo/iNOS+macrophages. J. Neurosci. 2011, 31:9910-9922.
13. Faust N., Varas F., Kelly L.M., Heck S., Graf T. Insertion of enhanced green fluorescent protein into the lysozyme gene creates mice with green fluorescent granulocytes and macrophages. Blood 2000, 96:719-726.
14. Geissmann F., Jung S., Littman D.R. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 2003, 19:71-82.
15. Geissmann F., Auffray C., Palframan R., Wirrig C., Ciocca A., Campisi L., Narni-Mancinelli E., Lauvau G. Blood monocytes: distinct subsets, how they relate to dendritic cells, and their possible roles in the regulation of T-cell responses. Immunol. Cell Biol. 2008, 86:398-408.
16. Gonzalez R., Glaser J., Liu M.T., Lane T.E., Keirstead H.S. Reducing inflammation decreases secondary degeneration and functional deficit after spinal cord injury. Exp. Neurol. 2003, 184:456-463.
17. Gordon S. Alternative activation of macrophages. Nat. Rev. Immunol. 2003, 3:23-35.
18. Gordon S., Taylor P.R. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 2005, 5:953-964.
19. Gris D., Marsh D.R., Oatway M.A., Chen Y., Hamilton E.F., Dekaban G.A., Weaver L.C. Transient blockade of the CD11d/CD18 integrin reduces secondary damage after spinal cord injury, improving sensory, autonomic, and motor function. J. Neurosci. 2004, 24:4043-4051.
20. Hawthorne A.L., Popovich P.G. Emerging concepts in myeloid cell biology after spinal cord injury. Neurotherapeutics 2011, 8:252-261.
21. Houser B.L., Tilburgs T., Hill J., Nicotra M.L., Strominger J.L. Two unique human decidual macrophage populations. J. Immunol. 2011, 186:2633-2642.
22. Joshi M., Fehlings M.G. Development and characterization of a novel, graded model of clip compressive spinal cord injury in the mouse: part 1. Clip design, behavioral outcomes, and histopathology. J. Neurotrauma 2002, 19:175-190.
23. Kigerl K.A., McGaughy V.M., Popovich P.G. Comparative analysis of lesion development and intraspinal inflammation in four strains of mice following spinal contusion injury. J. Comp. Neurol. 2006, 494:578-594.
24. Kigerl K.A., Gensel J.C., Ankeny D.P., Alexander J.K., Donnelly D.J., Popovich P.G. 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.
25. Kobayashi M., Jeschke M.G., Shigematsu K., Asai A., Yoshida S., Herndon D.N., Suzuki F. M2b monocytes predominated in peripheral blood of severely burned patients. J. Immunol. 2010, 185:7174-7179.
26. Koo G.C., Peppard J.R. Establishment of monoclonal anti-Nk-1.1 antibody. Hybridoma 1984, 3:301-303.
27. Lu J., Goh S.J., Tng P.Y., Deng Y.Y., Ling E.A., Moochhala S. Systemic inflammatory response following acute traumatic brain injury. Front. Biosci. 2009, 14:3795-3813.
28. Mantovani A., Locati M. Orchestration of macrophage polarization. Blood 2009, 114:3135-3136.
29. Mantovani A., Sica A., Sozzani S., Allavena P., Vecchi A., Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 2004, 25:677-686.
30. Martinez F.O., Helming L., Gordon S. Alternative activation of macrophages: an immunologic functional perspective. Annu. Rev. Immunol. 2009, 27:451-483.
31. Maurer M., Echtenacher B., Hultner L., Kollias G., Mannel D.N., Langley K.E., Galli S.J. The c-kit ligand, stem cell factor, can enhance innate immunity through effects on mast cells. J. Exp. Med. 1998, 188:2343-2348.
32. Mawhinney L.A., Thawer S.G., Lu W.Y., Rooijen N., Weaver L.C., Brown A., Dekaban G.A. Differential detection and distribution of microglial and hematogenous macrophage populations in the injured spinal cord of lys-EGFP-ki transgenic mice. J. Neuropathol. Exp. Neurol. 2012, 71:180-197.
33. Mosser D.M. The many faces of macrophage activation. J. Leukoc. Biol. 2003, 73:209-212.
34. Muller I., Munder M., Kropf P., Hansch G.M. Polymorphonuclear neutrophils and T lymphocytes: strange bedfellows or brothers in arms?. Trends Immunol. 2009, 30:522-530.
35. Pineau I., Lacroix S. Proinflammatory cytokine synthesis in the injured mouse spinal cord: multiphasic expression pattern and identification of the cell types involved. J. Comp. Neurol. 2007, 500:267-285.
36. Pineau I., Sun L., Bastien D., Lacroix S. Astrocytes initiate inflammation in the injured mouse spinal cord by promoting the entry of neutrophils and inflammatory monocytes in an IL-1 receptor/MyD88-dependent fashion. Brain Behav. Immun. 2010, 24:540-553.
37. Popovich P.G., Longbrake E.E. Can the immune system be harnessed to repair the CNS? Nature reviews. Neuroscience 2008, 9:481-493.
38. Randolph G.J., Jakubzick C., Qu C. Antigen presentation by monocytes and monocyte-derived cells. Curr. Opin. Immunol. 2008, 20:52-60.
39. Ransohoff R.M., Perry V.H. Microglial physiology: unique stimuli, specialized responses. Annu. Rev. Immunol. 2009, 27:119-145.
40. Rivollier A., He J., Kole A., Valatas V., Kelsall B.L. Inflammation switches the differentiation program of Ly6Chi monocytes from antiinflammatory macrophages to inflammatory dendritic cells in the colon. J. Exp. Med. 2012, 209:139-155.
41. Rosas-Ballina M., Tracey K.J. Cholinergic control of inflammation. J. Intern. Med. 2009, 265:663-679.
42. Saville L.R., Pospisil C.H., Mawhinney L.A., Bao F., Simedrea F.C., Peters A.A., O'Connell P.J., Weaver L.C., Dekaban G.A. A monoclonal antibody to CD11d reduces the inflammatory infiltrate into the injured spinal cord: a potential neuroprotective treatment. J. Neuroimmunol. 2004, 156:42-57.
43. Shechter R., London A., Varol C., Raposo C., Cusimano M., Yovel G., Rolls A., Mack M., Pluchino S., Martino G., Jung S., Schwartz M. Infiltrating blood-derived macrophages are vital cells playing an anti-inflammatory role in recovery from spinal cord injury in mice. PLoS Med. 2009, 6:e1000113.
44. Stirling D.P., Yong V.W. Dynamics of the inflammatory response after murine spinal cord injury revealed by flow cytometry. J. Neurosci. Res. 2008, 86:1944-1958.
45. Tacke F., Randolph G.J. Migratory fate and differentiation of blood monocyte subsets. Immunobiology 2006, 211:609-618.
46. Tacke F., Alvarez D., Kaplan T.J., Jakubzick C., Spanbroek R., Llodra J., Garin A., Liu J., Mack M., van Rooijen N., Lira S.A., Habenicht A.J., Randolph G.J. Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J. Clin. Invest. 2007, 117:185-194.
47. Templeton S.P., Kim T.S., O'Malley K., Perlman S. Maturation and localization of macrophages and microglia during infection with a neurotropic murine coronavirus. Brain Pathol. 2008, 18:40-51.
48. Tjoa T., Strausbaugh H.J., Maida N., Dazin P.F., Rosen S.D., Noble-Haeusslein L.J. The use of flow cytometry to assess neutrophil infiltration in the injured murine spinal cord. J. Neurosci. Methods 2003, 129:49-59.
49. Varin A., Gordon S. Alternative activation of macrophages: immune function and cellular biology. Immunobiology 2009, 214:630-641.
50. Wong K.L., Yeap W.H., Tai J.J., Ong S.M., Dang T.M., Wong S.C. The three human monocyte subsets: implications for health and disease. Immunol. Res. 2012, 53:41-57.
51. Wu L., Dakic A. Development of dendritic cell system. Cell. Mol. Immunol. 2004, 1:112-118.
52. Wu L., Liu Y.J. Development of dendritic-cell lineages. Immunity 2007, 26:741-750.
53. Zeyda M., Gollinger K., Kriehuber E., Kiefer F.W., Neuhofer A., Stulnig T.M. Newly identified adipose tissue macrophage populations in obesity with distinct chemokine and chemokine receptor expression. Int. J. Obes. 2010, 34:1684-1694.
54. Ziegler-Heitbrock L., Ancuta P., Crowe S., Dalod M., Grau V., Hart D.N., Leenen P.J., Liu Y.J., MacPherson G., Randolph G.J., Scherberich J., Schmitz J., Shortman K., Sozzani S., Strobl H., Zembala M., Austyn J.M., Lutz M.B. Nomenclature of monocytes and dendritic cells in blood. Blood 2010, 116:e74-80.