Cranial irradiation alters the brain's microenvironment and permits CCR2+ macrophage infiltration

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Morganti, Josh M ^a,b   Jopson, Timothy D ^a,b   Liu, Sharon ^b   Gupta, Nalin ^b   Rosi, Susanna ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; CD45 ANTIGEN; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CX3CR1; CLAUDIN 5; CYCLOOXYGENASE 2; JUNCTIONAL ADHESION MOLECULE A; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 2; MONOCYTE CHEMOTACTIC PROTEIN 3; MONOCYTE CHEMOTACTIC PROTEIN 5; OCCLUDIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ZONA OCCLUDIN 1; CCR2 PROTEIN, MOUSE; PRIMER DNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL ADHESION; CELL CYCLE ARREST; CELL INFILTRATION; CELLULAR DISTRIBUTION; CHEMOTAXIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME INDUCTION; GENE EXPRESSION; HIPPOCAMPUS; IMMUNE RESPONSE; IONIZING RADIATION; MACROPHAGE; MALE; MICROGLIA; MONOCYTE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RADIATION EXPOSURE; SKULL IRRADIATION; TUMOR MICROENVIRONMENT; ANIMAL; BLOOD BRAIN BARRIER; BRAIN NEOPLASMS; C57BL MOUSE; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; IMMUNOLOGY; NUCLEOTIDE SEQUENCE; PATHOLOGY; POLYMERASE CHAIN REACTION; RADIATION RESPONSE; SIGNAL TRANSDUCTION;

ANIMALS; BASE SEQUENCE; BLOOD-BRAIN BARRIER; BRAIN NEOPLASMS; CRANIAL IRRADIATION; DNA PRIMERS; ENZYME-LINKED IMMUNOSORBENT ASSAY; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; POLYMERASE CHAIN REACTION; RECEPTORS, CCR2; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT;

EID: 84898899415     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0093650     Document Type: Article

References (79)

1. Abayomi OK (1996) Pathogenesis of irradiation-induced cognitive dysfunction. Acta Oncol 35: 659-663.
2. Rola R, Raber J, Rizk A, Otsuka S, VandenBerg SR, et al. (2004) Radiation-induced impairment of hippocampal neurogenesis is associated with cognitive deficits in young mice. Experimental neurology 188: 316-330. (Pubitemid 38891593)
3. Mizumatsu S, Monje ML, Morhardt DR, Rola R, Palmer TD, et al. (2003) Extreme Sensitivity of Adult Neurogenesis to Low Doses of X-Irradiation. Cancer research 63: 4021.
4. Monje ML, Mizumatsu S, Fike JR, Palmer TD (2002) Irradiation induces neural precursor-cell dysfunction. Nat Med 8: 955-962. (Pubitemid 35033699)
5. Rosi S, Andres-Mach M, Fishman KM, Levy W, Ferguson RA, et al. (2008) Cranial irradiation alters the behaviorally induced immediate-early gene arc (activity-regulated cytoskeleton-associated protein). Cancer Res 68: 9763-9770.
6. Moravan MJ, Olschowka JA, Williams JP, O'Banion MK (2011) Cranial irradiation leads to acute and persistent neuroinflammation with delayed increases in T-cell infiltration and CD11c expression in C57BL/6 mouse brain. Radiation research 176: 459-473.
7. Linard C, Marquette C, Mathieu J, Pennequin A, Clarencon D, et al. (2004) Acute induction of inflammatory cytokine expression after gamma-irradiation in the rat: effect of an NF-kappaB inhibitor. Int J Radiat Oncol Biol Phys 58: 427-434. (Pubitemid 38142468)
8. Rosi S, Ferguson R, Fishman K, Allen A, Raber J, et al. (2012) The polyamine inhibitor alpha-difluoromethylornithine modulates hippocampus- dependent function after single and combined injuries. PLoS One 7: e31094.
9. Monje ML, Toda H, Palmer TD (2003) Inflammatory blockade restores adult hippocampal neurogenesis. Science 302: 1760-1765. (Pubitemid 37505739)
10. Belarbi K, Jopson T, Arellano C, Fike JR, Rosi S (2013) CCR2 deficiency prevents neuronal dysfunction and cognitive impairments induced by cranial irradiation. Cancer Res 73: 1201-1210.
11. Banisadr G, Gosselin RD, Mechighel P, Rostene W, Kitabgi P, et al. (2005) Constitutive neuronal expression of CCR2 chemokine receptor and its colocalization with neurotransmitters in normal rat brain: functional effect of MCP-1/CCL2 on calcium mobilization in primary cultured neurons. J Comp Neurol 492: 178-192. (Pubitemid 41443720)
12. Stamatovic SM, Shakui P, Keep RF, Moore BB, Kunkel SL, et al. (2005) Monocyte chemoattractant protein-1 regulation of blood-brain barrier permeability. J Cereb Blood Flow Metab 25: 593-606. (Pubitemid 40562932)
13. Semple BD, Bye N, Rancan M, Ziebell JM, Morganti-Kossmann MC (2010) Role of CCL2 (MCP-1) in traumatic brain injury (TBI): evidence from severe TBI patients and CCL22/2 mice. J Cereb Blood Flow Metab 30: 769-782.
14. Mildner A, Schmidt H, Nitsche M, Merkler D, Hanisch UK, et al. (2007) Microglia in the adult brain arise from Ly-6ChiCCR2+ monocytes only under defined host conditions. Nat Neurosci 10: 1544-1553. (Pubitemid 350175884)
15. Varol C, Yona S, Jung S (2009) Origins and tissue-context-dependent fates of blood monocytes. Immunology and cell biology 87: 30-38.
16. Saederup N, Cardona AE, Croft K, Mizutani M, Cotleur AC, et al. (2010) Selective Chemokine Receptor Usage by Central Nervous System Myeloid Cells in CCR2-Red Fluorescent Protein Knock-In Mice. PloS one 5: e13693.
17. Mizutani M, Pino PA, Saederup N, Charo IF, Ransohoff RM, et al. (2012) The fractalkine receptor but not CCR2 is present on microglia from embryonic development throughout adulthood. J Immunol 188: 29-36.
18. Auffray C, Fogg D, Garfa M, Elain G, Join-Lambert O, et al. (2007) Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 317: 666-670. (Pubitemid 47229966)
19. Geissmann F, Jung S, Littman DR (2003) Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19: 71-82. (Pubitemid 36859902)
20. Swirski FK, Libby P, Aikawa E, Alcaide P, Luscinskas FW, et al. (2007) Ly-6Chi monocytes dominate hypercholesterolemia-associated monocytosis and give rise to macrophages in atheromata. The Journal of clinical investigation 117: 195-205. (Pubitemid 46048466)
21. Prinz M, Priller J (2010) Tickets to the brain: role of CCR2 and CX3CR1 in myeloid cell entry in the CNS. J Neuroimmunol 224: 80-84.
22. Getts DR, Terry RL, Getts MT, Muller M, Rana S, et al. (2008) Ly6c+ "inflammatory monocytes" are microglial precursors recruited in a pathogenic manner in West Nile virus encephalitis. J Exp Med 205: 2319-2337.
23. Serbina NV, Pamer EG (2006) Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat Immunol 7: 311-317.
24. Auffray C, Sieweke MH, Geissmann F (2009) Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu Rev Immunol 27: 669-692.
25. Gordon S, Taylor PR (2005) Monocyte and macrophage heterogeneity. Nat Rev Immunol 5: 953-964. (Pubitemid 41746764)
26. Naert G, Rivest S (2012) Age-related changes in synaptic markers and monocyte subsets link the cognitive decline of APP(Swe)/PS1 mice. Front Cell Neurosci 6: 51.
27. Mildner A, Mack M, Schmidt H, Bruck W, Djukic M, et al. (2009) CCR2+Ly-6Chi monocytes are crucial for the effector phase of autoimmunity in the central nervous system. Brain 132: 2487-2500.
28. Westin K, Buchhave P, Nielsen H, Minthon L, Janciauskiene S, et al. (2012) CCL2 is associated with a faster rate of cognitive decline during early stages of Alzheimer's disease. PLoS One 7: e30525.
29. Naert G, Rivest S (2011) CC chemokine receptor 2 deficiency aggravates cognitive impairments and amyloid pathology in a transgenic mouse model of Alzheimer's disease. J Neurosci 31: 6208-6220.
30. Naert G, Rivest S (2012) Hematopoietic CC-chemokine receptor 2 (CCR2) competent cells are protective for the cognitive impairments and amyloid pathology in a transgenic mouse model of Alzheimer's disease. Mol Med 18: 297-313.
31. El Khoury J, Toft M, Hickman SE, Means TK, Terada K, et al. (2007) Ccr2 deficiency impairs microglial accumulation and accelerates progression of Alzheimer-like disease. Nat Med 13: 432-438. (Pubitemid 46559828)
32. Mildner A, Schlevogt B, Kierdorf K, Bottcher C, Erny D, et al. (2011) Distinct and non-redundant roles of microglia and myeloid subsets in mouse models of Alzheimer's disease. J Neurosci 31: 11159-11171.
33. Schilling M, Strecker J-K, Ringelstein EB, Schäbitz W-R, Kiefer R (2009) The role of CC chemokine receptor 2 on microglia activation and blood-borne cell recruitment after transient focal cerebral ischemia in mice. Brain research 1289: 79-84.
34. Zuurman MW, Heeroma J, Brouwer N, Boddeke HWGM, Biber K (2003) LPS-induced expression of a novel chemokine receptor (L-CCR) in mouse glial cells in vitro and in vivo. Glia 41: 327-336. (Pubitemid 36314146)
35. Olah M, Amor S, Brouwer N, Vinet J, Eggen B, et al. (2012) Identification of a microglia phenotype supportive of remyelination. Glia 60: 306-321.
36. Prinz M, Mildner A (2011) Microglia in the CNS: immigrants from another world. Glia 59: 177-187.
37. Kim SH, Lim DJ, Chung YG, Cho TH, Lim SJ, et al. (2002) Expression of TNF-alpha and TGF-beta 1 in the rat brain after a single high-dose irradiation. J Korean Med Sci 17: 242-248.
38. Morganti JM, Nash KR, Grimmig BA, Ranjit S, Small B, et al. (2012) The soluble isoform of CX3CL1 is necessary for neuroprotection in a mouse model of Parkinson's disease. J Neurosci 32: 14592-14601.
39. Cardona AE, Huang D, Sasse ME, Ransohoff RM (2006) Isolation of murine microglial cells for RNA analysis or flow cytometry. Nat Protoc 1: 1947-1951. (Pubitemid 46773316)
40. Varvel NH, Grathwohl SA, Baumann F, Liebig C, Bosch A, et al. (2012) Microglial repopulation model reveals a robust homeostatic process for replacing CNS myeloid cells. Proc Natl Acad Sci U S A 109: 18150-18155.
41. Ransohoff RM, Brown MA (2012) Innate immunity in the central nervous system. J Clin Invest 122: 1164-1171.
42. Andres RH, Choi R, Pendharkar AV, Gaeta X, Wang N, et al. (2011) The CCR2/CCL2 interaction mediates the transendothelial recruitment of intravascularly delivered neural stem cells to the ischemic brain. Stroke 42: 2923-2931.
43. Chen M, Zhao J, Luo C, Pandi SP, Penalva RG, et al. (2012) Para-inflammation-mediated retinal recruitment of bone marrow-derived myeloid cells following whole-body irradiation is CCL2 dependent. Glia 60: 833-842.
44. Szmydynger-Chodobska J, Strazielle N, Gandy JR, Keefe TH, Zink BJ, et al. (2012) Posttraumatic invasion of monocytes across the blood-cerebrospinal fluid barrier. J Cereb Blood Flow Metab 32: 93-104.
45. Semple BD, Kossmann T, Morganti-Kossmann MC (2010) Role of chemokines in CNS health and pathology: a focus on the CCL2/CCR2 and CXCL8/CXCR2 networks. J Cereb Blood Flow Metab 30: 459-473.
46. Nordal RA, Wong CS (2005) Molecular targets in radiation-induced blood-brain barrier disruption. Int J Radiat Oncol Biol Phys 62: 279-287. (Pubitemid 40591955)
47. Fauquette W, Amourette C, Dehouck MP, Diserbo M (2012) Radiation-induced blood-brain barrier damages: an in vitro study. Brain Res 1433: 114-126.
48. Dimitrijevic OB, Stamatovic SM, Keep RF, Andjelkovic AV (2006) Effects of the chemokine CCL2 on blood-brain barrier permeability during ischemiareperfusion injury. J Cereb Blood Flow Metab 26: 797-810.
49. Stamatovic SM, Sladojevic N, Keep RF, Andjelkovic AV (2012) Relocalization of junctional adhesion molecule A during inflammatory stimulation of brain endothelial cells. Mol Cell Biol 32: 3414-3427.
50. Roberts TK, Eugenin EA, Lopez L, Romero IA, Weksler BB, et al. (2012) CCL2 disrupts the adherens junction: implications for neuroinflammation. Lab Invest 92: 1213-1233.
51. Schellenberg AE, Buist R, Del Bigio MR, Toft-Hansen H, Khorooshi R, et al. (2012) Blood-brain barrier disruption in CCL2 transgenic mice during pertussis toxin-induced brain inflammation. Fluids and Barriers of the CNS 9: 10.
52. Wu G, Luo J, Rana JS, Laham R, Sellke FW, et al. (2006) Involvement of COX-2 in VEGF-induced angiogenesis via P38 and JNK pathways in vascular endothelial cells. Cardiovasc Res 69: 512-519. (Pubitemid 43098807)
53. Ferrara N, Gerber HP, LeCouter J (2003) The biology of VEGF and its receptors. Nat Med 9: 669-676. (Pubitemid 36749215)
54. Lee WH, Cho HJ, Sonntag WE, Lee YW (2011) Radiation attenuates physiological angiogenesis by differential expression of VEGF, Ang-1, tie-2 and Ang-2 in rat brain. Radiat Res 176: 753-760.
55. Kioi M, Vogel H, Schultz G, Hoffman RM, Harsh GR, et al. (2010) Inhibition of vasculogenesis, but not angiogenesis, prevents the recurrence of glioblastoma after irradiation in mice. The Journal of clinical investigation 120: 694-705.
56. Lerman OZ, Greives MR, Singh SP, Thanik VD, Chang CC, et al. (2010) Low-dose radiation augments vasculogenesis signaling through HIF-1-dependent and -independent SDF-1 induction. Blood 116: 3669-3676.
57. Shi C, Pamer EG (2011) Monocyte recruitment during infection and inflammation. Nature reviews Immunology 11: 762-774.
58. Takeshita Y, Ransohoff RM (2012) Inflammatory cell trafficking across the blood-brain barrier: chemokine regulation and in vitro models. Immunol Rev 248: 228-239.
59. Zlokovic BV (2008) The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 57: 178-201.
60. Man S, Tucky B, Cotleur A, Drazba J, Takeshita Y, et al. (2012) CXCL12-Induced Monocyte-Endothelial Interactions Promote Lymphocyte Transmigration Across an in Vitro Blood-Brain Barrier. Science Translational Medicine 4: 119ra114-119ra114.
61. Gilmore S (2003) Radiation-induced modulation of the microglial population in the normal and injured mature spinal cord. Experimental neurology 182: 169-179.
62. Austyn JM, Gordon S (1981) F4/80, a monoclonal antibody directed specifically against the mouse macrophage. Eur J Immunol 11: 805-815. (Pubitemid 12237981)
63. Lloyd CM, Phillips ARJ, Cooper GJS, Dunbar PR (2008) Three-colour fluorescence immunohistochemistry reveals the diversity of cells staining for macrophage markers in murine spleen and liver. Journal of immunological methods 334: 70-81.
64. Farina C, Aloisi F, Meinl E (2007) Astrocytes are active players in cerebral innate immunity. Trends Immunol 28: 138-145. (Pubitemid 46283692)
65. Ridet JL, Malhotra SK, Privat A, Gage FH (1997) Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci 20: 570-577. (Pubitemid 27508969)
66. Lee SC, Liu W, Dickson DW, Brosnan CF, Berman JW (1993) Cytokine production by human fetal microglia and astrocytes. Differential induction by lipopolysaccharide and IL-1 beta. J Immunol 150: 2659-2667. (Pubitemid 23127515)
67. Steiner J, Bernstein HG, Bogerts B, Gos T, Richter-Landsberg C, et al. (2008) S100B is expressed in, and released from, OLN-93 oligodendrocytes: Influence of serum and glucose deprivation. Neuroscience 154: 496-503.
68. Panagiotakos G, Alshamy G, Chan B, Abrams R, Greenberg E, et al. (2007) Long-Term Impact of Radiation on the Stem Cell and Oligodendrocyte Precursors in the Brain. PloS one 2: e588.
69. Brambilla R, Bracchi-Ricard V, Hu WH, Frydel B, Bramwell A, et al. (2005) Inhibition of astroglial nuclear factor kappaB reduces inflammation and improves functional recovery after spinal cord injury. J Exp Med 202: 145-156. (Pubitemid 41002917)
70. Babcock AA, Kuziel WA, Rivest S, Owens T (2003) Chemokine expression by glial cells directs leukocytes to sites of axonal injury in the CNS. J Neurosci 23: 7922-7930. (Pubitemid 37052361)
71. Semple BD, Frugier T, Morganti-Kossmann MC (2010) CCL2 modulates cytokine production in cultured mouse astrocytes. J Neuroinflammation 7: 67.
72. Mahad D, Callahan MK, Williams KA, Ubogu EE, Kivisakk P, et al. (2006) Modulating CCR2 and CCL2 at the blood-brain barrier: relevance for multiple sclerosis pathogenesis. Brain 129: 212-223. (Pubitemid 43063772)
73. Ljubimova NV, Levitman MK, Plotnikova ED, Eidus LK (1991) Endothelial cell population dynamics in rat brain after local irradiation. The British journal of radiology 64: 934-940.
74. Nguyen V, Gaber MW, Sontag MR, Kiani MF (2000) Late effects of ionizing radiation on the microvascular networks in normal tissue. Radiation research 154: 531-536.
75. Roth NM, Sontag MR, Kiani MF (1999) Early effects of ionizing radiation on the microvascular networks in normal tissue. Radiation research 151: 270-277. (Pubitemid 29109137)
76. Wu K-L, Tu B, Li Y-Q, Wong CS (2010) Role of Intercellular Adhesion Molecule-1 in Radiation-Induced Brain Injury. International Journal of Radiation Oncology*Biology*Physics 76: 220-228.
77. Ransohoff RM, Cardona AE (2010) The myeloid cells of the central nervous system parenchyma. Nature 468: 253-262.
78. Stasinopoulos I, O'Brien DR, Bhujwalla ZM (2009) Inflammation, but not hypoxia, mediated HIF-1alpha activation depends on COX-2. Cancer biology & therapy 8: 31-35.
79. Lund EL, H g A, Olsen MWB, Hansen LT, Engelholm SA, et al. (2004) Differential regulation of VEGF, HIF1a and angiopoietin-1, -2 and -4 by hypoxia and ionizing radiation in human glioblastoma. International Journal of Cancer 108: 833-838.