Absence of CCL2 is sufficient to restore hippocampal neurogenesis following cranial irradiation

Brain, Behavior, and Immunity

Volumn 30, Issue , 2013, Pages 33-44

  Lee, Star W ^a   Haditsch, Ursula ^a   Cord, Branden J ^a   Guzman, Raphael ^a,b   Kim, Soo Jeong ^a   Boettcher, Chotima ^c   Priller, Josef ^c   Ormerod, Brandi K ^d   Palmer, Theo D ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF BASEL   (Switzerland)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d University of Florida   (United States)

Author keywords

CCL2 MCP1; Hippocampus; Inflammation; Neurogenesis; Radiation

Indexed keywords

CD45 ANTIGEN; CHLORDANE; INTERLEUKIN 12P40; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; CELL ACTIVATION; CELL FUNCTION; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE RESPONSE; HIPPOCAMPUS; IMMUNOREACTIVITY; MALE; MICROGLIA; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; SKULL IRRADIATION; UPREGULATION;

ANIMALS; CELLS, CULTURED; CHEMOKINE CCL2; CRANIAL IRRADIATION; HIPPOCAMPUS; MALE; MICE; MICE, KNOCKOUT; MICROGLIA; NEURAL STEM CELLS; NEUROGENESIS; NEURONS;

EID: 84876856695     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2012.09.010     Document Type: Review

References (58)

1. Abayomi O.K. Pathogenesis of irradiation-induced cognitive dysfunction. Acta Oncol. 1996, 35:659-663.
2. Andjelkovic A.V., Kerkovich D., Shanley J., Pulliam L., Pachter J.S. Expression of binding sites for beta chemokines on human astrocytes. Glia 1999, 28:225-235.
3. Banisadr G., Queraud-Lesaux F., Boutterin M.C., Pelaprat D., Zalc B., Rostene W., Haour F., Parsadaniantz S.M. Distribution, cellular localization and functional role of CCR2 chemokine receptors in adult rat brain. J. Neurochem. 2002, 81:257-269.
4. Biswas S.K., Sodhi A. In vitro activation of murine peritoneal macrophages by monocyte chemoattractant protein-1: upregulation of CD11b, production of proinflammatory cytokines, and the signal transduction pathway. J. Interferon Cytokine Res. 2002, 22:527-538.
5. Bottazzi B., Walter S., Govoni D., Colotta F., Mantovani A. Monocyte chemotactic cytokine gene transfer modulates macrophage infiltration, growth, and susceptibility to IL-2 therapy of a murine melanoma. J. Immunol. 1992, 148:1280-1285.
6. Bu J., Akhtar N., Nishiyama A. Transient expression of the NG2 proteoglycan by a subpopulation of activated macrophages in an excitotoxic hippocampal lesion. Glia 2001, 34:296-310.
7. Butovsky O., Ziv Y., Schwartz A., Landa G., Talpalar A.E., Pluchino S., Martino G., Schwartz M. Microglia activated by IL-4 or IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol. Cell. Neurosci. 2006, 31:149-160.
8. Cameron H.A., Tanapat P., Gould E. Adrenal steroids and N-methyl-d-aspartate receptor activation regulate neurogenesis in the dentate gyrus of adult rats through a common pathway. Neuroscience 1998, 82:349-354.
9. Chen Y., Hallenbeck J.M., Ruetzler C., Bol D., Thomas K., Berman N.E., Vogel S.N. Overexpression of monocyte chemoattractant protein 1 in the brain exacerbates ischemic brain injury and is associated with recruitment of inflammatory cells. J. Cereb. Blood Flow Metab. 2003, 23:748-755.
10. Edman L.C., Mira H., Erices A., Malmersjo S., Andersson E., Uhlen P., Arenas E. Alpha-chemokines regulate proliferation, neurogenesis, and dopaminergic differentiation of ventral midbrain precursors and neurospheres. Stem Cells 2008, 26:1891-1900.
11. Ekdahl C.T., Claasen J.H., Bonde S., Kokaia Z., Lindvall O. Inflammation is detrimental for neurogenesis in adult brain. Proc. Natl. Acad. Sci. USA 2003, 100:13632-13637.
12. Ferreira A.M., Rollins B.J., Faunce D.E., Burns A.L., Zhu X., Dipietro L.A. The effect of MCP-1 depletion on chemokine and chemokine-related gene expression: evidence for a complex network in acute inflammation. Cytokine 2005, 30:64-71.
13. Filippov V., Kronenberg G., Pivneva T., Reuter K., Steiner B., Wang L.P., Yamaguchi M., Kettenmann H., Kempermann G. Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol. Cell. Neurosci. 2003, 23:373-382.
14. + T cells compared. J. Immunol. 1995, 154:4309-4321.
15. Francis F., Koulakoff A., Boucher D., Chafey P., Schaar B., Vinet M.C., Friocourt G., McDonnell N., Reiner O., Kahn A., McConnell S.K., Berwald-Netter Y., Denoulet P., Chelly J. Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 1999, 23:247-256.
16. Gage F.H., Kempermann G., Palmer T.D., Peterson D.A., Ray J. Multipotent progenitor cells in the adult dentate gyrus. J. Neurobiol. 1998, 36:249-266.
17. Gould E., Cameron H.A., Daniels D.C., Woolley C.S., McEwen B.S. Adrenal hormones suppress cell division in the adult rat dentate gyrus. J. Neurosci. 1992, 12:3642-3650.
18. Gu L., Okada Y., Clinton S.K., Gerard C., Sukhova G.K., Libby P., Rollins B.J. Absence of monocyte chemoattractant protein-1 reduces atherosclerosis in low density lipoprotein receptor-deficient mice. Mol. Cell 1998, 2:275-281.
19. Gu L., Tseng S., Horner R.M., Tam C., Loda M., Rollins B.J. Control of TH2 polarization by the chemokine monocyte chemoattractant protein-1. Nature 2000, 404:407-411.
20. Hayashi M., Luo Y., Laning J., Strieter R.M., Dorf M.E. Production and function of monocyte chemoattractant protein-1 and other beta-chemokines in murine glial cells. J. Neuroimmunol. 1995, 60:143-150.
21. Hughes P.M., Allegrini P.R., Rudin M., Perry V.H., Mir A.K., Wiessner C. Monocyte chemoattractant protein-1 deficiency is protective in a murine stroke model. J. Cereb. Blood Flow Metab. 2002, 22:308-317.
22. Imai Y., Ibata I., Ito D., Ohsawa K., Kohsaka S. A novel gene iba1 in the major histocompatibility complex class III region encoding an EF hand protein expressed in a monocytic lineage. Biochem. Biophys. Res. Commun. 1996, 224:855-862.
23. Ji J.F., He B.P., Dheen S.T., Tay S.S. Expression of chemokine receptors CXCR4, CCR2, CCR5 and CX3CR1 in neural progenitor cells isolated from the subventricular zone of the adult rat brain. Neurosci. Lett. 2004, 355:236-240.
24. Jones L.L., Yamaguchi Y., Stallcup W.B., Tuszynski M.H. NG2 is a major chondroitin sulfate proteoglycan produced after spinal cord injury and is expressed by macrophages and oligodendrocyte progenitors. J. Neurosci. 2002, 22:2792-2803.
25. Kalm M., Fukuda A., Fukuda H., Ohrfelt A., Lannering B., Bjork-Eriksson T., Blennow K., Marky I., Blomgren K. Transient inflammation in neurogenic regions after irradiation of the developing brain. Radiat. Res. 2009, 171:66-76.
26. Kronenberg G., Wang L.P., Synowitz M., Gertz K., Katchanov J., Glass R., Harms C., Kempermann G., Kettenmann H., Endres M. Nestin-expressing cells divide and adopt a complex electrophysiologic phenotype after transient brain ischemia. J. Cereb. Blood Flow Metab. 2005, 25:1613-1624.
27. Lee W.H., Sonntag W.E., Mitschelen M., Yan H., Lee Y.W. Irradiation induces regionally specific alterations in pro-inflammatory environments in rat brain. Int. J. Radiat. Biol. 2010, 86:132-144.
28. Limoli C.L., Giedzinski E., Rola R., Otsuka S., Palmer T.D., Fike J.R. Radiation response of neural precursor cells: linking cellular sensitivity to cell cycle checkpoints, apoptosis and oxidative stress. Radiat. Res. 2004, 161:17-27.
29. Liu X.S., Zhang Z.G., Zhang R.L., Gregg S.R., Wang L., Yier T., Chopp M. Chemokine ligand 2 (CCL2) induces migration and differentiation of subventricular zone cells after stroke. J. Neurosci. Res. 2007, 85:2120-2125.
30. Lu B., Rutledge B.J., Gu L., Fiorillo J., Lukacs N.W., Kunkel S.L., North R., Gerard C., Rollins B.J. Abnormalities in monocyte recruitment and cytokine expression in monocyte chemoattractant protein 1-deficient mice. J. Exp. Med. 1998, 187:601-608.
31. Luo Y., Laning J., Hayashi M., Hancock P.R., Rollins B., Dorf M.E. Serologic analysis of the mouse beta chemokine JE/monocyte chemoattractant protein-1. J. Immunol. 1994, 153:3708-3716.
32. Madsen T.M., Kristjansen P.E., Bolwig T.G., Wortwein G. Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience 2003, 119:635-642.
33. Matsushima K., Larsen C.G., DuBois G.C., Oppenheim J.J. Purification and characterization of a novel monocyte chemotactic and activating factor produced by a human myelomonocytic cell line. J. Exp. Med. 1989, 169:1485-1490.
34. + monocytes only under defined host conditions. Nat. Neurosci. 2007, 10:1544-1553.
35. Mizumatsu S., Monje M.L., Morhardt D.R., Rola R., Palmer T.D., Fike J.R. Extreme sensitivity of adult neurogenesis to low doses of X-irradiation. Cancer Res. 2003, 63:4021-4027.
36. Monje M.L., Mizumatsu S., Fike J.R., Palmer T.D. Irradiation induces neural precursor-cell dysfunction. Nat. Med. 2002, 8:955-962.
37. Monje M.L., Palmer T. Radiation injury and neurogenesis. Curr. Opin. Neurol. 2003, 16:129-134.
38. Monje M.L., Toda H., Palmer T.D. Inflammatory blockade restores adult hippocampal neurogenesis. Science 2003, 302:1760-1765.
39. Monje M.L., Vogel H., Masek M., Ligon K.L., Fisher P.G., Palmer T.D. Impaired human hippocampal neurogenesis after treatment for central nervous system malignancies. Ann. Neurol. 2007, 62:515-520.
40. Muessel M.J., Klein R.M., Wilson A.M., Berman N.E. Ablation of the chemokine monocyte chemoattractant protein-1 delays retrograde neuronal degeneration, attenuates microglial activation, and alters expression of cell death molecules. Brain Res. Mol. Brain Res. 2002, 103:12-27.
41. Ogata H., Takeya M., Yoshimura T., Takagi K., Takahashi K. The role of monocyte chemoattractant protein-1 (MCP-1) in the pathogenesis of collagen-induced arthritis in rats. J. Pathol. 1997, 182:106-114.
42. Okabe M., Ikawa M., Kominami K., Nakanishi T., Nishimune Y. 'Green mice' as a source of ubiquitous green cells. FEBS Lett. 1997, 407:313-319.
43. + T cell proliferation. J. Neuroimmunol. 2005, 163:73-83.
44. Palmer T.D., Willhoite A.R., Gage F.H. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 2000, 425:479-494.
45. Priller J., Flugel A., Wehner T., Boentert M., Haas C.A., Prinz M., Fernandez-Klett F., Prass K., Bechmann I., de Boer B.A., Frotscher M., Kreutzberg G.W., Persons D.A., Dirnagl U. Targeting gene-modified hematopoietic cells to the central nervous system: use of green fluorescent protein uncovers microglial engraftment. Nat. Med. 2001, 7:1356-1361.
46. Ramprasad M.P., Terpstra V., Kondratenko N., Quehenberger O., Steinberg D. Cell surface expression of mouse macrosialin and human CD68 and their role as macrophage receptors for oxidized low density lipoprotein. Proc. Natl. Acad. Sci. USA 1996, 93:14833-14838.
47. Saxe M.D., Battaglia F., Wang J.W., Malleret G., David D.J., Monckton J.E., Garcia A.D., Sofroniew M.V., Kandel E.R., Santarelli L., Hen R., Drew M.R. Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc. Natl. Acad. Sci. USA 2006, 103:17501-17506.
48. Semple B.D., Kossmann T., Morganti-Kossmann M.C. Role of chemokines in CNS health and pathology: a focus on the CCL2/CCR2 and CXCL8/CXCR2 networks. J. Cereb. Blood Flow Metab. 2010, 30:459-473.
49. Shors T.J., Miesegaes G., Beylin A., Zhao M., Rydel T., Gould E. Neurogenesis in the adult is involved in the formation of trace memories. Nature 2001, 410:372-376.
50. Shors T.J., Townsend D.A., Zhao M., Kozorovitskiy Y., Gould E. Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 2002, 12:578-584.
51. Stamatovic S.M., Keep R.F., Kunkel S.L., Andjelkovic A.V. Potential role of MCP-1 in endothelial cell tight junction 'opening': signaling via Rho and Rho kinase. J. Cell Sci. 2003, 116:4615-4628.
52. Thibeault I., Laflamme N., Rivest S. Regulation of the gene encoding the monocyte chemoattractant protein 1 (MCP-1) in the mouse and rat brain in response to circulating LPS and proinflammatory cytokines. J. Comp Neurol. 2001, 434:461-477.
53. Traynor T.R., Herring A.C., Dorf M.E., Kuziel W.A., Toews G.B., Huffnagle G.B. Differential roles of CC chemokine ligand 2/monocyte chemotactic protein-1 and CCR2 in the development of T1 immunity. J. Immunol. 2002, 168:4659-4666.
54. Turbic A., Leong S.Y., Turnley A.M. Chemokines and inflammatory mediators interact to regulate adult murine neural precursor cell proliferation, survival and differentiation. PLoS ONE 2011, 6:e25406.
55. van Praag H., Schinder A.F., Christie B.R., Toni N., Palmer T.D., Gage F.H. Functional neurogenesis in the adult hippocampus. Nature 2002, 415:1030-1034.
56. Vela J.M., Yanez A., Gonzalez B., Castellano B. Time course of proliferation and elimination of microglia/macrophages in different neurodegenerative conditions. J. Neurotrauma 2002, 19:1503-1520.
57. Villeda S.A., Luo J., Mosher K.I., Zou B., Britschgi M., Bieri G., Stan T.M., Fainberg N., Ding Z., Eggel A., Lucin K.M., Czirr E., Park J.S., Couillard-Despres S., Aigner L., Li G., Peskind E.R., Kaye J.A., Quinn J.F., Galasko D.R., Xie X.S., Rando T.A., Wyss-Coray T. The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature 2011, 477:90-94.
58. Weissleder R., Elizondo G., Wittenberg J., Lee A.S., Josephson L., Brady T.J. Ultrasmall superparamagnetic iron oxide: an intravenous contrast agent for assessing lymph nodes with MR imaging. Radiology 1990, 175:494-498.