Microglial CX3CR1 promotes adult neurogenesis by inhibiting Sirt 1/p65 signaling independent of CX3CL1

Acta Neuropathologica Communications

Volumn 4, Issue 1, 2016, Pages

  Sellner, Sabine ^a,g   Paricio Montesinos, Ricardo ^a,h,i   Spieß, Alena ^a   Masuch, Annette ^b,j   Erny, Daniel ^a   Harsan, Laura A ^c   Elverfeldt, Dominik V ^c   Schwabenland, Marius ^a   Biber, Knut ^b,d   Staszewski, Ori ^a   Lira, Sergio ^e   Jung, Steffen ^f   Prinz, Marco ^a   Blank, Thomas ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b Department of Psychiatry and Psychotherapy ^*  (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

^d UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^e MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^f WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^g LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^h MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

ⁱ CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^j UNIVERSITY MEDICINE GREIFSWALD   (Germany)

more..

Author keywords

Adult neurogenesis; Microglia; Morphometry; Sirtuin 1; Water maze

Indexed keywords

CHEMOKINE RECEPTOR CXCR1; CX3CL1 PROTEIN, MOUSE; DOUBLECORTIN PROTEIN; FRACTALKINE; MICROTUBULE ASSOCIATED PROTEIN; NEUROPEPTIDE; RELA PROTEIN, MOUSE; SIRT1 PROTEIN, MOUSE; SIRTUIN 1; TRANSCRIPTION FACTOR RELA;

ADULT STEM CELL; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CYTOLOGY; DRUG EFFECTS; GENETICS; HIPPOCAMPUS; MAZE TEST; MEMORY; METABOLISM; MICROGLIA; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; PHYSIOLOGY; SIGNAL TRANSDUCTION; STEM CELL NICHE; TRANSGENIC MOUSE;

ADULT STEM CELLS; ANIMALS; CHEMOKINE CX3CL1; HIPPOCAMPUS; MAZE LEARNING; MEMORY; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; MICROTUBULE-ASSOCIATED PROTEINS; NEURAL STEM CELLS; NEUROGENESIS; NEUROPEPTIDES; RECEPTORS, INTERLEUKIN-8A; SIGNAL TRANSDUCTION; SIRTUIN 1; STEM CELL NICHE; TRANSCRIPTION FACTOR RELA;

EID: 85028922208     PISSN: None     EISSN: 20515960     Source Type: Journal    
DOI: 10.1186/s40478-016-0374-8     Document Type: Article

References (62)

1. Al-Aoukaty A, Rolstad B, Giaid A, Maghazachi AA. MIP-3alpha, MIP-3beta and fractalkine induce the locomotion and the mobilization of intracellular calcium, and activate the heterotrimeric G proteins in human natural killer cells. Immunology. 1998;95:618-24
2. Jung S, Aliberti J, Graemmel P, Sunshine MJ, Kreutzberg GW, Sher A, Littman DR. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol. 2000;20:4106-14
3. Ginhoux F, Greter M, Leboeuf M, Nandi S, See P, Gokhan S, Mehler MF, Conway SJ, Ng LG, Stanley ER, et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science. 2010;330:841-5. doi:10.1126/science.1194637
4. Kierdorf K, Erny D, Goldmann T, Sander V, Schulz C, Perdiguero EG, Wieghofer P, Heinrich A, Riemke P, Holscher C, et al. Microglia emerge from erythromyeloid precursors via Pu.1-and Irf8-dependent pathways. Nat Neurosci. 2013;16:273-80. doi:10.1038/nn.3318
5. Schulz C, Gomez Perdiguero E, Chorro L, Szabo-Rogers H, Cagnard N, Kierdorf K, Prinz M, Wu B, Jacobsen SE, Pollard JW, et al. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science. 2012;336:86-90. doi:10.1126/science.1219179
6. Shemer A, Erny D, Jung S, Prinz M. Microglia plasticity during health and disease: an immunological perspective. Trends Immunol. 2015;36:614-24. doi:10.1016/j.it.2015.08.003
7. Paolicelli RC, Bolasco G, Pagani F, Maggi L, Scianni M, Panzanelli P, Giustetto M, Ferreira TA, Guiducci E, Dumas L, et al. Synaptic pruning by microglia is necessary for normal brain development. Science. 2011;333:1456-8. doi:10. 1126/science.1202529
8. Schafer DP, Lehrman EK, Kautzman AG, Koyama R, Mardinly AR, Yamasaki R, Ransohoff RM, Greenberg ME, Barres BA, Stevens B. Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron. 2012;74:691-705. doi:10.1016/j.neuron.2012.03.026
9. Hatori K, Nagai A, Heisel R, Ryu JK, Kim SU. Fractalkine and fractalkine receptors in human neurons and glial cells. J Neurosci Res. 2002;69:418-26. doi:10.1002/jnr.10304
10. Kim KW, Vallon-Eberhard A, Zigmond E, Farache J, Shezen E, Shakhar G, Ludwig A, Lira SA, Jung S. In vivo structure/function and expression analysis of the CX3C chemokine fractalkine. Blood. 2011;118:e156-67. doi:10.1182/ blood-2011-04-348946
11. Chapman GA, Moores K, Harrison D, Campbell CA, Stewart BR, Strijbos PJ. Fractalkine cleavage from neuronal membranes represents an acute event in the inflammatory response to excitotoxic brain damage. J Neurosci. 2000;20:RC87
12. Haskell CA, Cleary MD, Charo IF. Molecular uncoupling of fractalkinemediated cell adhesion and signal transduction. Rapid flow arrest of CX3CR1-expressing cells is independent of G-protein activation. J Biol Chem. 1999;274:10053-8
13. Bachstetter AD, Morganti JM, Jernberg J, Schlunk A, Mitchell SH, Brewster KW, Hudson CE, Cole MJ, Harrison JK, Bickford PC, et al. Fractalkine and CX 3 CR1 regulate hippocampal neurogenesis in adult and aged rats. Neurobiol Aging. 2011;32:2030-44. doi:10.1016/j.neurobiolaging.2009.11.022
14. Rogers JT, Morganti JM, Bachstetter AD, Hudson CE, Peters MM, Grimmig BA, Weeber EJ, Bickford PC, Gemma C. CX3CR1 deficiency leads to impairment of hippocampal cognitive function and synaptic plasticity. J Neurosci. 2011;31: 16241-50. doi:10.1523/JNEUROSCI.3667-11.201131/45/16241
15. Maggi L, Scianni M, Branchi I, D'Andrea I, Lauro C, Limatola C. CX(3)CR1 deficiency alters hippocampal-dependent plasticity phenomena blunting the effects of enriched environment. Front Cell Neurosci. 2011;5:22. doi:10. 3389/fncel.2011.00022
16. Xue J, Dong JH, Huang GD, Qu XF, Wu G, Dong XR. NF-kappaB signaling modulates radiationinduced microglial activation. Oncol Rep. 2014;31:2555-60 doi:10.3892/or.2014.3144
17. Hickman SE, Kingery ND, Ohsumi TK, Borowsky ML, Wang LC, Means TK, El Khoury J. The microglial sensome revealed by direct RNA sequencing. Nat Neurosci. 2013;16:1896-905. doi:10.1038/nn.3554
18. Benzing WC, Wujek JR, Ward EK, Shaffer D, Ashe KH, Younkin SG, Brunden KR. Evidence for glial-mediated inflammation in aged APP(SW) transgenic mice. Neurobiol Aging. 1999;20:581-9
19. Chen J, Zhou Y, Mueller-Steiner S, Chen LF, Kwon H, Yi S, Mucke L, Gan L. SIRT1 protects against microglia-dependent amyloid-beta toxicity through inhibiting NF-kappaB signaling. J Biol Chem. 2005;280:40364-74. doi:10. 1074/jbc.M509329200
20. Yeung F, Hoberg JE, Ramsey CS, Keller MD, Jones DR, Frye RA, Mayo MW. Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J. 2004;23:2369-80. doi:10.1038/sj.emboj.7600244
21. Cook DN, Chen SC, Sullivan LM, Manfra DJ, Wiekowski MT, Prosser DM, Vassileva G, Lira SA. Generation and analysis of mice lacking the chemokine fractalkine. Mol Cell Biol. 2001;21:3159-65. doi:10.1128/MCB. 21.9.3159-3165.2001
22. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods. 1984;11:47-60
23. Kumar R, Hunt CR, Gupta A, Nannepaga S, Pandita RK, Shay JW, Bachoo R, Ludwig T, Burns DK, Pandita TK. Purkinje cell-specific males absent on the first (mMof) gene deletion results in an ataxia-telangiectasia-like neurological phenotype and backward walking in mice. Proc Natl Acad Sci U S A. 2011;108:3636-41. doi:10.1073/pnas.1016524108
24. Park HR, Kong KH, Yu BP, Mattson MP, Lee J. Resveratrol inhibits the proliferation of neural progenitor cells and hippocampal neurogenesis. J Biol Chem. 2012;287:42588-600. doi:10.1074/jbc.M112.406413
25. Darcy MJ, Trouche S, Jin SX, Feig LA. Age-dependent role for Ras-GRF1 in the late stages of adult neurogenesis in the dentate gyrus. Hippocampus. 2014;24:315-25. doi:10.1002/hipo.22225
26. Dann A, Poeck H, Croxford AL, Gaupp S, Kierdorf K, Knust M, Pfeifer D, Maihoefer C, Endres S, Kalinke U, et al. Cytosolic RIG-I-like helicases act as negative regulators of sterile inflammation in the CNS. Nat Neurosci. 2012; 15:98-106. doi:10.1038/nn.2964
27. Mildner A, Schmidt H, Nitsche M, Merkler D, Hanisch UK, Mack M, Heikenwalder M, Bruck W, Priller J, Prinz M. Microglia in the adult brain arise from Ly-6ChiCCR2+ monocytes only under defined host conditions. Nat Neurosci. 2007;10:1544-53. doi:10.1038/nn2015
28. Goldmann T, Wieghofer P, Muller PF, Wolf Y, Varol D, Yona S, Brendecke SM, Kierdorf K, Staszewski O, Datta M, et al. A new type of microglia gene targeting shows TAK1 to be pivotal in CNS autoimmune inflammation. Nat Neurosci. 2013;16:1618-26. doi:10.1038/nn.3531
29. Raasch J, Zeller N, van Loo G, Merkler D, Mildner A, Erny D, Knobeloch KP, Bethea JR, Waisman A, Knust M, et al. IkappaB kinase 2 determines oligodendrocyte loss by non-cell-autonomous activation of NF-kappaB in the central nervous system. Brain. 2011;134:1184-98. doi:10.1093/brain/awq359
30. Fatt MP, Cancino GI, Miller FD, Kaplan DR. p63 and p73 coordinate p53 function to determine the balance between survival, cell death, and senescence in adult neural precursor cells. Cell Death Differ. 2014;21:1546-59. doi:10.1038/cdd.2014.61
31. Chal J, Oginuma M, Al Tanoury Z, Gobert B, Sumara O, Hick A, Bousson F, Zidouni Y, Mursch C, Moncuquet P, et al. Differentiation of pluripotent stem cells to muscle fiber to model Duchenne muscular dystrophy. Nat Biotechnol. 2015;33:962-9. doi:10.1038/nbt.3297
32. Fulmer CG, VonDran MW, Stillman AA, Huang Y, Hempstead BL, Dreyfus CF. Astrocyte-derived BDNF supports myelin protein synthesis after cuprizoneinduced demyelination. J Neurosci. 2014;34:8186-96. doi:10.1523/ JNEUROSCI.4267-13.2014
33. Farioli-Vecchioli S, Micheli L, Saraulli D, Ceccarelli M, Cannas S, Scardigli R, Leonardi L, Cina I, Costanzi M, Ciotti MT, et al. Btg1 is required to maintain the pool of stem and progenitor cells of the dentate gyrus and subventricular zone. Front Neurosci. 2012;6:124. doi:10.3389/fnins.2012.00124
34. Nistico R, Florenzano F, Mango D, Ferraina C, Grilli M, Di Prisco S, Nobili A, Saccucci S, D'Amelio M, Morbin M, et al. Presynaptic c-Jun N-terminal Kinase 2 regulates NMDA receptor-dependent glutamate release. Sci Rep. 2015;5: 9035. doi:10.1038/srep09035
35. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci. 1999;2:260-5. doi:10.1038/6365
36. Mildner A, Schlevogt B, Kierdorf K, Bottcher C, Erny D, Kummer MP, Quinn M, Bruck W, Bechmann I, Heneka MT, et al. Distinct and non-redundant roles of microglia and myeloid subsets in mouse models of Alzheimer's disease. J Neurosci. 2011;31:11159-71. doi:10.1523/JNEUROSCI.6209-10.2011
37. West MJ, Slomianka L, Gundersen HJ. Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat Rec. 1991;231:482-97. doi:10.1002/ar. 1092310411
38. Goldmann T, Zeller N, Raasch J, Kierdorf K, Frenzel K, Ketscher L, Basters A, Staszewski O, Brendecke SM, Spiess A, et al. USP18 lack in microglia causes destructive interferonopathy of the mouse brain. EMBO J. 2015;34:1612-29. doi:10.15252/embj.201490791
39. Harsan LA, David C, Reisert M, Schnell S, Hennig J, von Elverfeldt D, Staiger JF. Mapping remodeling of thalamocortical projections in the living reeler mouse brain by diffusion tractography. Proc Natl Acad Sci U S A. 2013;110: E1797-806. doi:10.1073/pnas.1218330110
40. Harsan LA, Paul D, Schnell S, Kreher BW, Hennig J, Staiger JF, von Elverfeldt D. In vivo diffusion tensor magnetic resonance imaging and fiber tracking of the mouse brain. NMR Biomed. 2010;23:884-96. doi:10.1002/nbm.1496
41. Kumar P, Periyasamy R, Das S, Neerukonda S, Mani I, Pandey KN. All-trans retinoic acid and sodium butyrate enhance natriuretic peptide receptor a gene transcription: role of histone modification. Mol Pharmacol. 2014;85: 946-57. doi:10.1124/mol.114.092221
42. Brown JP, Couillard-Despres S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG. Transient expression of doublecortin during adult neurogenesis. J Comp Neurol. 2003;467:1-10. doi:10.1002/cne.10874
43. Combadiere C, Salzwedel K, Smith ED, Tiffany HL, Berger EA, Murphy PM. Identification of CX3CR1. A chemotactic receptor for the human CX3C chemokine fractalkine and a fusion coreceptor for HIV-1. J Biol Chem. 1998; 273:23799-804
44. Sengupta N, Seto E. Regulation of histone deacetylase activities. J Cell Biochem. 2004;93:57-67. doi:10.1002/jcb.20179
45. Zupkovitz G, Tischler J, Posch M, Sadzak I, Ramsauer K, Egger G, Grausenburger R, Schweifer N, Chiocca S, Decker T, et al. Negative and positive regulation of gene expression by mouse histone deacetylase 1. Mol Cell Biol. 2006;26:7913-28. doi:10.1128/MCB.01220-06
46. Chen LF, Mu Y, Greene WC. Acetylation of RelA at discrete sites regulates distinct nuclear functions of NF-kappaB. EMBO J. 2002;21:6539-48
47. Cao D, Wang M, Qiu X, Liu D, Jiang H, Yang N, Xu RM. Structural basis for allosteric, substrate-dependent stimulation of SIRT1 activity by resveratrol. Genes Dev. 2015;29:1316-25. doi:10.1101/gad.265462.115
48. Solomon JM, Pasupuleti R, Xu L, McDonagh T, Curtis R, DiStefano PS, Huber LJ. Inhibition of SIRT1 catalytic activity increases p53 acetylation but does not alter cell survival following DNA damage. Mol Cell Biol. 2006;26:28-38. doi:10.1128/MCB.26.1.28-38.2006
49. Min KJ, Yang MS, Jou I, Joe EH. Protein kinase A mediates microglial activation induced by plasminogen and gangliosides. Exp Mol Med. 2004; 36:461-7. doi:10.1038/emm.2004.58
50. Liu TF, Yoza BK, El Gazzar M, Vachharajani VT, McCall CE. NAD +-dependent SIRT1 deacetylase participates in epigenetic reprogramming during endotoxin tolerance. J Biol Chem. 2011;286:9856-64. doi:10.1074/jbc.M110.196790
51. Koo JW, Duman RS. IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc Natl Acad Sci U S A. 2008;105:751-6. doi:10.1073/pnas.0708092105
52. Hellwig S, Brioschi S, Dieni S, Frings L, Masuch A, Blank T, Biber K. Altered microglia morphology and higher resilience to stress-induced depressionlike behavior in CX3CR1-deficient mice. Brain Behav Immun. 2015. Doi 10. 1016/j.bbi.2015.11.008
53. Pagani F, Paolicelli RC, Murana E, Cortese B, Di Angelantonio S, Zurolo E, Guiducci E, Ferreira TA, Garofalo S, Catalano M, et al. Defective microglial development in the hippocampus of Cx3cr1 deficient mice. Front Cell Neurosci. 2015;9:111. doi:10.3389/fncel.2015.00111
54. Reshef R, Kreisel T, Beroukhim Kay D, Yirmiya R. Microglia and their CX3CR1 signaling are involved in hippocampal-but not olfactory bulb-related memory and neurogenesis. Brain Behav Immun. 2014;41:239-50. doi:10. 1016/j.bbi.2014.04.009
55. Hundhausen C, Misztela D, Berkhout TA, Broadway N, Saftig P, Reiss K, Hartmann D, Fahrenholz F, Postina R, Matthews V, et al. The disintegrin-like metalloproteinase ADAM10 is involved in constitutive cleavage of CX3CL1 (fractalkine) and regulates CX3CL1-mediated cell-cell adhesion. Blood. 2003; 102:1186-95. doi:10.1182/blood-2002-12-3775
56. Ransohoff RM, Liu L, Cardona AE. Chemokines and chemokine receptors: multipurpose players in neuroinflammation. Int Rev Neurobiol. 2007;82:187-204. doi:10.1016/S0074-7742(07)82010-1
57. Liu Z, Condello C, Schain A, Harb R, Grutzendler J. CX3CR1 in microglia regulates brain amyloid deposition through selective protofibrillar amyloidbeta phagocytosis. J Neurosci. 2010;30:17091-101. doi:10.1523/JNEUROSCI. 4403-10.2010
58. Shan S, Hong-Min T, Yi F, Jun-Peng G, Yue F, Yan-Hong T, Yun-Ke Y, Wen-Wei L, Xiang-Yu W, Jun M, et al. New evidences for fractalkine/CX3CL1 involved in substantia nigral microglial activation and behavioral changes in a rat model of Parkinson's disease. Neurobiol Aging. 2011;32:443-58. doi:10. 1016/j.neurobiolaging.2009.03.004
59. Cambien B, Pomeranz M, Schmid-Antomarchi H, Millet MA, Breittmayer V, Rossi B, Schmid-Alliana A. Signal transduction pathways involved in soluble fractalkine-induced monocytic cell adhesion. Blood. 2001;97:2031-7
60. Ding XM, Pan L, Wang Y, Xu QZ. Baicalin exerts protective effects against lipopolysaccharide-induced acute lung injury by regulating the crosstalk between the CX3CL1-CX3CR1 axis and NF-kappaB pathway in CX3CL1-knockout mice. Int J Mol Med. 2016. Doi 10.3892/ijmm.2016.2456
61. Nakayama T, Watanabe Y, Oiso N, Higuchi T, Shigeta A, Mizuguchi N, Katou F, Hashimoto K, Kawada A, Yoshie O. Eotaxin-3/CC chemokine ligand 26 is a functional ligand for CX3CR1. J Immunol. 2010;185:6472-9. doi:10.4049/ jimmunol.0904126
62. Pope SM, Fulkerson PC, Blanchard C, Akei HS, Nikolaidis NM, Zimmermann N, Molkentin JD, Rothenberg ME. Identification of a cooperative mechanism involving interleukin-13 and eotaxin-2 in experimental allergic lung inflammation. J Biol Chem. 2005;280:13952-61. doi:10.1074/jbc.M406037200