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CD200 is up-regulated in R6/1 transgenic mouse model of Huntington's disease


Autoři: Andrea Comella Bolla aff001;  Tony Valente aff003;  Andres Miguez aff001;  Veronica Brito aff002;  Silvia Gines aff002;  Carme Solà aff003;  Marco Straccia aff001;  Josep M. Canals aff001
Působiště autorů: Stem Cells and Regenerative Medicine Laboratory, Production and Validation Center of Advanced Therapies (Creatio), Department of Biomedicine, Faculty of Medicine and Health Science, University of Barcelona, Barcelona, Spain aff001;  Neuroscience Institute, University of Barcelona, Barcelona, Spain aff002;  August Pi i Sunyer Biomedical Research Institute (IDIBAPS), Barcelona, Spain aff003;  Network Center for Biomedical Research in Neurodegenerative Diseases (CIBERNED), Madrid, Spain aff004;  Department of Cerebral Ischemia and Neurodegeneration, Institut d’Investigacions Biomèdiques de Barcelona–Consejo Superior de Investigaciones Científicas (IIBB–CSIC), Barcelona, Spain aff005;  Department of Biomedicine, Faculty of Medicine and Health Science, University of Barcelona, Barcelona, Spain aff006
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0224901

Souhrn

In Huntington’s disease (HD), striatal medium spiny neurons (MSNs) are particularly sensitive to the presence of a CAG repeat in the huntingtin (HTT) gene. However, there are many evidences that cells from the peripheral immune system and central nervous system (CNS) immune cells, namely microglia, play an important role in the etiology and the progression of HD. However, it remains unclear whether MSNs neurodegeneration is mediated by a non-cell autonomous mechanism. The homeostasis in the healthy CNS is maintained by several mechanisms of interaction between all brain cells. Neurons can control microglia activation through several inhibitory mechanisms, such as the CD200–CD200R1 interaction. Due to the complete lack of knowledge about the CD200–CD200R1 system in HD, we determined the temporal patterns of CD200 and CD200R1 expression in the neocortex, hippocampus and striatum in the HD mouse models R6/1 and HdhQ111/7 from pre-symptomatic to manifest stages. In order to explore any alteration in the peripheral immune system, we also studied the levels of expression of CD200 and CD200R1 in whole blood. Although CD200R1 expression was not altered, we observed and increase in CD200 gene expression and protein levels in the brain parenchyma of all the regions we examined, along with HD pathogenesis in R6/1 mice. Interestingly, the expression of CD200 mRNA was also up-regulated in blood following a similar temporal pattern. These results suggest that canonical neuronal–microglial communication through CD200–CD200R1 interaction is not compromised, and CD200 up-regulation in R6/1 brain parenchyma could represent a neurotrophic signal to sustain or extend neuronal function in the latest stages of HD as pro-survival mechanism.

Klíčová slova:

Blood – Central nervous system – Gene expression – Hippocampus – Microglial cells – Mouse models – Neostriatum – Neocortex


Zdroje

1. Yu S, Mulley J, Loesch D, Turner G, Donnelly A, Gedeon A, et al. A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington’s disease chromosomes. The Huntington’s Disease Collaborative Research Group. Cell. 1993. doi: 10.1016/0092-8674(93)90585-E

2. Reiner A, Albin RL, Anderson KD, D’Amato CJ, Penney JB, Young AB. Differential loss of striatal projection neurons in Huntington disease. Proc Natl Acad Sci U S A. 1988.

3. Gil JMAC, Mohapel P, Araújo IM, N Popovic, Li JY, Brundin P, et al. Reduced hippocampal neurogenesis in R6/2 transgenic Huntington’s disease mice. Neurobiol Dis. 2005. doi: 10.1016/j.nbd.2005.05.006 15951191

4. Pang TYC, Du X, Zajac MS, Howard ML, Hannan AJ. Altered serotonin receptor expression is associated with depression-related behavior in the R6/1 transgenic mouse model of Huntington’s disease. Hum Mol Genet. 2009. doi: 10.1093/hmg/ddn385 19008301

5. Brito V, Giralt A, Enriquez-Barreto L, Puigdellívol M, Suelves N, Zamora-Moratalla A, et al. Neurotrophin receptor p75NTR mediates Huntington’s disease-associated synaptic and memory dysfunction. J Clin Invest. 2014. doi: 10.1172/JCI74809 25180603

6. Ross CA, Aylward EH, Wild EJ, Langbehn DR, Long JD, Warner JH, et al. Huntington disease: natural history, biomarkers and prospects for therapeutics. Nat Rev Neurol. 2014;10: 204–16. doi: 10.1038/nrneurol.2014.24 24614516

7. Björkqvist M, Wild EJ, Thiele J, Silvestroni A, Andre R, Lahiri N, et al. A novel pathogenic pathway of immune activation detectable before clinical onset in Huntington’s disease. J Exp Med. 2008. doi: 10.1084/jem.20080178 18625748

8. Kwan W, Träger U, Davalos D, Chou A, Bouchard J, Andre R, et al. Mutant huntingtin impairs immune cell migration in Huntington disease. J Clin Invest. 2012. doi: 10.1172/JCI64484 23160193

9. Zwilling D, Huang S-Y, Sathyasaikumar K V, Notarangelo FM, Guidetti P, Wu H-Q, et al. Kynurenine 3-monooxygenase inhibition in blood ameliorates neurodegeneration. Cell. 2011. doi: 10.1016/j.cell.2011.05.020 21640374

10. Singhrao SK, Neal JW, Morgan BP, Gasque P. Increased complement biosynthesis by microglia and complement activation on neurons in Huntington’s disease. Exp Neurol. 1999. doi: 10.1006/exnr.1999.7170 10506508

11. Hong S, Beja-Glasser VF, Nfonoyim BM, Frouin A, Li S, Ramakrishnan S, et al. Complement and microglia mediate early synapse loss in Alzheimer mouse models. Science (80-). 2016. doi: 10.1126/science.aad8373 27033548

12. Politis M, Pavese N, Tai YF, Kiferle L, Mason SL, Brooks DJ, et al. Microglial activation in regions related to cognitive function predicts disease onset in Huntington’s disease: A multimodal imaging study. Hum Brain Mapp. 2011. doi: 10.1002/hbm.21008 21229614

13. Miguez A, Barriga GGD, Brito V, Straccia M, Giralt A, Ginés S, et al. Fingolimod (FTY720) enhances hippocampal synaptic plasticity and memory in Huntington’s disease by preventing p75NTR up-regulation and astrocyte-mediated inflammation. Hum Mol Genet. 2015. doi: 10.1093/hmg/ddv218 26063761

14. Crotti A, Benner C, Kerman BE, Gosselin D, Lagier-Tourenne C, Zuccato C, et al. Mutant Huntingtin promotes autonomous microglia activation via myeloid lineage-determining factors. Nat Neurosci. 2014. doi: 10.1038/nn.3668 24584051

15. Yirmiya R, Rimmerman N, Reshef R. Depression as a Microglial Disease. Trends in Neurosciences. 2015. doi: 10.1016/j.tins.2015.08.001 26442697

16. Epping EA, Paulsen JS. Depression in the early stages of Huntington disease. Neurodegener Dis Manag. 2011. doi: 10.2217/nmt.11.45 22942903

17. Paoli Andrea; Ciammola Andrea; Silani Vincenzo; Prunas Cecilia; Lucchiari Claudio; Zugno Elisa; Caletti Elisabetta RAB. Neuropsychiatric burden in Huntington’s disease. Brain Sci. 2017;7: 67. doi: 10.3390/brainsci7060067 28621715

18. Paixão S, Klein R. Neuron-astrocyte communication and synaptic plasticity. Current Opinion in Neurobiology. 2010. doi: 10.1016/j.conb.2010.04.008 20471242

19. Santello M, Bezzi P, Volterra A. TNFα Controls Glutamatergic Gliotransmission in the Hippocampal Dentate Gyrus. Neuron. 2011. doi: 10.1016/j.neuron.2011.02.003 21382557

20. Griffiths MR, Gasque P, Neal JW. The multiple roles of the innate immune system in the regulation of apoptosis and inflammation in the brain. Journal of Neuropathology and Experimental Neurology. 2009. doi: 10.1097/NEN.0b013e3181996688 19225414

21. Nimmerjahn A, Kirchhoff F, Helmchen F. Neuroscience: Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science (80-). 2005. doi: 10.1126/science.1110647

22. Biber K, Neumann H, Inoue K, Boddeke HWGM. Neuronal “On” and “Off” signals control microglia. Trends in Neurosciences. 2007. doi: 10.1016/j.tins.2007.08.007 17950926

23. Shrivastava K, Gonzalez P, Acarin L. The immune inhibitory complex CD200/CD200R is developmentally regulated in the mouse brain. J Comp Neurol. 2012;520: 2657–2675. doi: 10.1002/cne.23062 22323214

24. Chitnis T, Imitola J, Wang Y, Elyaman W, Chawla P, Sharuk M, et al. Elevated neuronal expression of CD200 protects Wlds mice from inflammation-mediated neurodegeneration. Am J Pathol. 2007. doi: 10.2353/ajpath.2007.060677 17456775

25. Koning N, Swaab DF, Hoek RM, Huitinga I. Distribution of the immune inhibitory molecules CD200 and CD200R in the normal central nervous system and multiple sclerosis lesions suggests neuron-glia and glia-glia interactions. J Neuropathol Exp Neurol. 2009;68: 159–167. doi: 10.1097/NEN.0b013e3181964113 19151626

26. Walker DG, Dalsing-Hernandez JE, Campbell NA, Lue LF. Decreased expression of CD200 and CD200 receptor in Alzheimer’s disease: A potential mechanism leading to chronic inflammation. Exp Neurol. 2009. doi: 10.1016/j.expneurol.2008.09.003 18938162

27. Yi MH, Zhang E, Kang JW, Shin YN, Byun JY, Oh SH, et al. Expression of CD200 in alternative activation of microglia following an excitotoxic lesion in the mouse hippocampus. Brain Res. 2012;1481. doi: 10.1016/j.brainres.2012.08.053 22975132

28. Chen Z, Ma X, Zhang J, Hu J, Gorczynski RM. Alternative splicing of CD200 is regulated by an exonic splicing enhancer and SF2/ASF. Nucleic Acids Res. 2010. doi: 10.1093/nar/gkq554 20558599

29. Chen Z, Chen DX, Kai Y, Khatri I, Lamptey B, Gorczynski RM. Identification of an expressed truncated form of CD200, CD200tr, which is a physiologic antagonist of CD200-induced suppression. Transplantation. 2008;68: 1116–1124. doi: 10.1097/TP.0b013e318186fec2 18946351

30. Vieites JM, De la Torre R, Ortega MA, Montero T, Peco JM, Sánchez-Pozo A, et al. Characterization of human cd200 glycoprotein receptor gene located on chromosome 3q12-13. Gene. 2003;311: 99–104. doi: 10.1016/s0378-1119(03)00562-6 12853143

31. Dentesano G, Straccia M, Ejarque-Ortiz A, Tusell JM, Serratosa J, Saura J, et al. Inhibition of CD200R1 expression by C/EBP beta in reactive microglial cells. J Neuroinflammation. 2012;9: 165. doi: 10.1186/1742-2094-9-165 22776069

32. Yi M-H, Zhang E, Kim J-J, Baek H, Shin N, Kim S, et al. CD200R/Foxp3-mediated signalling regulates microglial activation. Sci Rep. 2016;6: 34901. doi: 10.1038/srep34901 27731341

33. Lyons A, Minogue AM, Jones RS, Fitzpatrick O, Noonan J, Campbell VA, et al. Analysis of the Impact of CD200 on Phagocytosis. Mol Neurobiol. 2016. doi: 10.1007/s12035-016-0223-6 27830533

34. Wang C-Y, Hsieh Y-T, Fang K-M, Yang C-S, Tzeng S-F. Reduction of CD200 expression in glioma cells enhances microglia activation and tumor growth. J Neurosci Res. 2016;94: 1460–1471. doi: 10.1002/jnr.23922 27629530

35. Costello DA, Lyons A, Denieffe S, Browne TC, Cox FF, Lynch MA. Long term potentiation is impaired in membrane glycoprotein CD200-deficient mice: a role for Toll-like receptor activation. J Biol Chem. 2011;286: 34722–34732. doi: 10.1074/jbc.M111.280826 21835925

36. Denieffe S, Kelly RJ, McDonald C, Lyons A, Lynch MA. Classical activation of microglia in CD200-deficient mice is a consequence of blood brain barrier permeability and infiltration of peripheral cells. Brain Behav Immun. 2013;34: 86–97. doi: 10.1016/j.bbi.2013.07.174 23916893

37. Xie X, Luo X, Liu N, Li X, Lou F, Zheng Y, et al. Monocytes, microglia, and CD200-CD200R1 signaling are essential in the transmission of inflammation from the periphery to the central nervous system. J Neurochem. 2017;141: 222–235. doi: 10.1111/jnc.13972 28164283

38. Cox FF, Carney D, Miller AM, Lynch MA. CD200 fusion protein decreases microglial activation in the hippocampus of aged rats. Brain Behav Immun. 2012;26: 789–796. doi: 10.1016/j.bbi.2011.10.004 22041297

39. Webb M, Barclay AN. Localisation of the MRC OX‐2 Glycoprotein on the Surfaces of Neurones. J Neurochem. 1984. doi: 10.1111/j.1471-4159.1984.tb12844.x 6147390

40. Wright GJ, Jones M, Puklavec MJ, Brown MH, Barclay AN. The unusual distribution of the neuronal/lymphoid cell surface CD200 (OX2) glycoprotein is conserved in humans. Immunology. 2001;102: 173–179. doi: 10.1046/j.1365-2567.2001.01163.x 11260322

41. Stubelius A, Andersson A, Islander U, Carlsten H. Ovarian hormones in innate inflammation. Immunobiology. 2017;222: 878–883. doi: 10.1016/j.imbio.2017.05.007 28554684

42. Mangiarini L, Sathasivam K, Seller M, Cozens B, Harper A, Hetherington C, et al. Exon I of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell. 1996. doi: 10.1016/S0092-8674(00)81369-0

43. Giralt A, Rodrigo T, Martín ED, Gonzalez JR, Milà M, Ceña V, et al. Brain-derived neurotrophic factor modulates the severity of cognitive alterations induced by mutant huntingtin: Involvement of phospholipaseCγ activity and glutamate receptor expression. Neuroscience. 2009;158. doi: 10.1016/j.neuroscience.2008.11.024 19121372

44. Wheeler VC, Auerbach W, White JK, Srinidhi J, Auerbach A, Ryan A, et al. Length-dependent gametic CAG repeat instability in the Huntington’s disease knock-in mouse. Hum Mol Genet. 1999. doi: 10.1093/hmg/8.1.115 9887339

45. Straccia M, Dentesano G, Valente T, Pulido-Salgado M, Solà C, Saura J. CCAAT/Enhancer binding protein β regulates prostaglandin E synthase expression and prostaglandin E2 production in activated microglial cells. Glia. 2013. doi: 10.1002/glia.22542 23893854

46. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9: 671–675. doi: 10.1038/nmeth.2089 22930834

47. Pankratova S, Bjornsdottir H, Christensen C, Zhang L, Li S, Dmytriyeva O, et al. Immunomodulator CD200 Promotes Neurotrophic Activity by Interacting with and Activating the Fibroblast Growth Factor Receptor. Mol Neurobiol. 2016;53: 584–594. doi: 10.1007/s12035-014-9037-6 25502296

48. Puigdellívol M, Cherubini M, Brito V, Giralt A, Suelves N, Ballesteros J, et al. A role for Kalirin-7 in corticostriatal synaptic dysfunction in Huntington’s disease. Hum Mol Genet. 2015. doi: 10.1093/hmg/ddv426 26464483

49. Barclay AN. Different reticular elements in rat lymphoid tissue identified by localization of Ia, Thy-1 and MRC OX 2 antigens. Immunology. 1981.

50. Heneka MT, Kummer MP, Latz E. Innate immune activation in neurodegenerative disease. Nature Reviews Immunology. 2014. doi: 10.1038/nri3705 24962261

51. Masgrau R, Guaza C, Ransohoff RM, Galea E. Should We Stop Saying ‘Glia’ and ‘Neuroinflammation’? Trends in Molecular Medicine. 2017. doi: 10.1016/j.molmed.2017.04.005 28499701

52. Deckert M, Sedgwick JD, Fischer E, Schlüter D. Regulation of microglial cell responses in murine Toxoplasma encephalitis by CD200/CD200 receptor interaction. Acta Neuropathol. 2006;111: 548–558. doi: 10.1007/s00401-006-0062-z 16718351

53. Paoletti P, Vila I, Rife M, Lizcano JM, Alberch J, Gines S. Dopaminergic and Glutamatergic Signaling Crosstalk in Huntington’s Disease Neurodegeneration: The Role of p25/Cyclin-Dependent Kinase 5. J Neurosci. 2008. doi: 10.1523/jneurosci.3237-08.2008 18829967

54. Estrada-Sanchez AM, Burroughs CL, Cavaliere S, Barton SJ, Chen S, Yang XW, et al. Cortical Efferents Lacking Mutant huntingtin Improve Striatal Neuronal Activity and Behavior in a Conditional Mouse Model of Huntington’s Disease. J Neurosci. 2015. doi: 10.1523/jneurosci.2812-14.2015 25762686

55. Estrada-Sánchez AM, Montiel T, Segovia J, Massieu L. Glutamate toxicity in the striatum of the R6/2 Huntington’s disease transgenic mice is age-dependent and correlates with decreased levels of glutamate transporters. Neurobiol Dis. 2009. doi: 10.1016/j.nbd.2008.12.017 19168136

56. Hansson O, Petersen A, Leist M, Nicotera P, Castilho RF, Brundin P. Transgenic mice expressing a Huntington’s disease mutation are resistant to quinolinic acid-induced striatal excitotoxicity. Proc Natl Acad Sci. 2002. doi: 10.1073/pnas.96.15.8727 10411943

57. Stephan AH, Barres BA, Stevens B. The complement system: an unexpected role in synaptic pruning during development and disease. Annu Rev Neurosci. 2012. doi: 10.1146/annurev-neuro-061010-113810 22715882

58. Crook ZR, Housman D. Huntington’s Disease: Can Mice Lead the Way to Treatment? Neuron. 2011. doi: 10.1016/j.neuron.2010.12.035 21315254

59. Pouladi MA, Morton AJ, Hayden MR. Choosing an animal model for the study of Huntington’s disease. Nat Rev Neurosci. 2013;14: 708–721. doi: 10.1038/nrn3570 24052178

60. Möller T. Neuroinflammation in Huntington’s disease. J Neural Transm. 2010;117: 1001–1008. doi: 10.1007/s00702-010-0430-7 20535620

61. Holmannová D, Koláčková M, Kondělková K, Kuneš P, Krejsek J, Andrýs C. CD200/CD200R Paired Potent Inhibitory Molecules Regulating Immune and Inflammatory Responses; Part I: CD200/CD200R Structure, Activation, and Function. Acta Medica (Hradec Kral Czech Republic). 2012;55: 12–17. doi: 10.14712/18059694.2015.68 22696929

62. Holmannová D, Koláčková M, Kondělková K, Kuneš P, Krejsek J, Andrýs C. CD200/CD200R Paired Potent Inhibitory Molecules Regulating Immune and Inflammatory Responses; Part II: CD 200/CD200R Potential Clinical Applications. Acta Medica (Hradec Kral Czech Republic). 2012;55: 59–65. doi: 10.14712/18059694.2015.56 23101267

63. Ojo B, Rezaie P, Gabbott PL, Davies H, Colyer F, Cowley TR, et al. Age-related changes in the hippocampus (loss of synaptophysin and glial-synaptic interaction) are modified by systemic treatment with an NCAM-derived peptide, FGL. Brain Behav Immun. 2012;26: 778–788. doi: 10.1016/j.bbi.2011.09.013 21986303

64. Martin DSD, Walsh M, Miller A-M, Skerrett HE, Byrne P, Mandel A, et al. A novel phospholipid-based drug formulation, VP025, modulates age- and LPS-induced microglial activity in the rat. Neuroimmunomodulation. 2009;16: 400–410. doi: 10.1159/000228915 19609089

65. Lyons A, Downer EJ, Crotty S, Nolan YM, Mills KHG, Lynch MA. CD200 ligand receptor interaction modulates microglial activation in vivo and in vitro: a role for IL-4. J Neurosci. 2007;27: 8309–8313. doi: 10.1523/JNEUROSCI.1781-07.2007 17670977

66. Frank MG, Barrientos RM, Biedenkapp JC, Rudy JW, Watkins LR, Maier SF. mRNA up-regulation of MHC II and pivotal pro-inflammatory genes in normal brain aging. Neurobiol Aging. 2006;27: 717–722. doi: 10.1016/j.neurobiolaging.2005.03.013 15890435

67. Wang X-J, Zhang S, Yan Z-Q, Zhao Y-X, Zhou H-Y, Wang Y, et al. Impaired CD200-CD200R-mediated microglia silencing enhances midbrain dopaminergic neurodegeneration: roles of aging, superoxide, NADPH oxidase, and p38 MAPK. Free Radic Biol {&} Med. 2011;50: 1094–1106. doi: 10.1016/j.freeradbiomed.2011.01.032 21295135

68. Wang Y, Cao X, Ma H, Tan W, Zhang L, Li Z, et al. Prior stressor exposure delays the recovery of surgery-induced cognitive impairment and prolongs neuroinflammation in aged rats. Brain Res. 2016. doi: 10.1016/j.brainres.2016.07.045 27487302

69. Li Z, Liu F, Ma H, White PF, Yumul R, Jiang Y, et al. Age exacerbates surgery-induced cognitive impairment and neuroinflammation in Sprague-Dawley rats: the role of IL-4. Brain Res. 2017;1665: 65–73. doi: 10.1016/j.brainres.2017.04.004 28414034

70. Cao X-Z, Ma H, Wang J-K, Liu F, Wu B-Y, Tian A-Y, et al. Postoperative cognitive deficits and neuroinflammation in the hippocampus triggered by surgical trauma are exacerbated in aged rats. Prog neuro-psychopharmacology {&} Biol psychiatry. 2010;34: 1426–1432. doi: 10.1016/j.pnpbp.2010.07.027 20691747

71. Walker DG, Lue LF, Tang TM, Adler CH, Caviness JN, Sabbagh MN, et al. Changes in CD200 and intercellular adhesion molecule-1 (ICAM-1) levels in brains of Lewy body disorder cases are associated with amounts of Alzheimer’s pathology not α-synuclein pathology. Neurobiol Aging. 2017;54: 175–186. doi: 10.1016/j.neurobiolaging.2017.03.007 28390825

72. Sun F-J, Zhang C-Q, Chen X, Wei Y-J, Li S, Liu S-Y, et al. Downregulation of CD47 and CD200 in patients with focal cortical dysplasia type IIb and tuberous sclerosis complex. J Neuroinflammation. 2016;13: 85. doi: 10.1186/s12974-016-0546-2 27095555

73. Jurgens HA, Johnson RW. Environmental enrichment attenuates hippocampal neuroinflammation and improves cognitive function during influenza infection. Brain Behav Immun. 2012;26: 1006–1016. doi: 10.1016/j.bbi.2012.05.015 22687335

74. Jurgens HA, Amancherla K, Johnson RW. Influenza infection induces neuroinflammation, alters hippocampal neuron morphology, and impairs cognition in adult mice. J Neurosci. 2012;32: 3958–3968. doi: 10.1523/JNEUROSCI.6389-11.2012 22442063

75. Valente T, Serratosa J, Perpiñá U, Saura J, Solà C. Alterations in CD200-CD200R1 System during EAE Already Manifest at Presymptomatic Stages. Front Cell Neurosci. 2017. doi: 10.3389/fncel.2017.00129 28522962

76. Koning N, Bö L, Hoek RM, Huitinga I. Downregulation of macrophage inhibitory molecules in multiple sclerosis lesions. Ann Neurol. 2007;62: 504–514. doi: 10.1002/ana.21220 17879969

77. Ren Y, Ye M, Chen S, Ding J. CD200 Inhibits Inflammatory Response by Promoting KATP Channel Opening in Microglia Cells in Parkinson’s Disease. Med Sci Monit. 2016;22: 1733–1741. doi: 10.12659/MSM.898400 27213506

78. Sung Y-H, Kim S-C, Hong H-P, Park C-Y, Shin M-S, Kim C-J, et al. Treadmill exercise ameliorates dopaminergic neuronal loss through suppressing microglial activation in Parkinson’s disease mice. Life Sci. 2012;91: 1309–1316. doi: 10.1016/j.lfs.2012.10.003 23069581

79. Masocha W. Systemic lipopolysaccharide (LPS)-induced microglial activation results in different temporal reduction of CD200 and CD200 receptor gene expression in the brain. J Neuroimmunol. 2009;214: 78–82. doi: 10.1016/j.jneuroim.2009.06.022 19656578

80. Lyons A, McQuillan K, Deighan BF, O’Reilly JA, Downer EJ, Murphy AC, et al. Decreased neuronal CD200 expression in IL-4-deficient mice results in increased neuroinflammation in response to lipopolysaccharide. Brain Behav Immun. 2009. doi: 10.1016/j.bbi.2009.05.060 19501645

81. Elmore MRP, Burton MD, Conrad MS, Rytych JL, Van Alstine WG, Johnson RW. Respiratory Viral Infection in Neonatal Piglets Causes Marked Microglia Activation in the Hippocampus and Deficits in Spatial Learning. J Neurosci. 2014;34: 2120–2129. doi: 10.1523/JNEUROSCI.2180-13.2014 24501353

82. Frank MG, Baratta M V, Sprunger DB, Watkins LR, Maier SF. Microglia serve as a neuroimmune substrate for stress-induced potentiation of CNS pro-inflammatory cytokine responses. Brain Behav Immun. 2007;21: 47–59. doi: 10.1016/j.bbi.2006.03.005 16647243

83. Hernangómez M, Mestre L, Correa FG, Loría F, Mecha M, Iñigo PM, et al. CD200-CD200R1 interaction contributes to neuroprotective effects of anandamide on experimentally induced inflammation. Glia. 2012;60: 1437–1450. doi: 10.1002/glia.22366 22653796

84. Montiel M, Bonilla E, Valero N, Mosquera J, Espina LM, Quiroz Y, et al. Melatonin decreases brain apoptosis, oxidative stress, and CD200 expression and increased survival rate in mice infected by Venezuelan equine encephalitis virus. Antivir Chem Chemother. 2015;23: 99–108. doi: 10.1177/2040206616660851 27503577

85. Murray C, Sanderson DJ, Barkus C, Deacon RMJ, Rawlins JNP, Bannerman DM, et al. Systemic inflammation induces acute working memory deficits in the primed brain: Relevance for delirium. Neurobiol Aging. 2012;33: 603–616.e3. doi: 10.1016/j.neurobiolaging.2010.04.002 20471138

86. Blandino P, Barnum CJ, Solomon LG, Larish Y, Lankow BS, Deak T. Gene expression changes in the hypothalamus provide evidence for regionally-selective changes in IL-1 and microglial markers after acute stress. Brain Behav Immun. 2009;23: 958–968. doi: 10.1016/j.bbi.2009.04.013 19464360

87. Wang HT, Huang FL, Hu ZL, Zhang WJ, Qiao XQ, Huang YQ, et al. Early-Life Social Isolation-Induced Depressive-Like Behavior in Rats Results in Microglial Activation and Neuronal Histone Methylation that Are Mitigated by Minocycline. Neurotox Res. 2017;31: 505–520. doi: 10.1007/s12640-016-9696-3 28092020

88. Sorrells SF, Munhoz CD, Manley NC, Yen S, Sapolsky RM. Glucocorticoids increase excitotoxic injury and inflammation in the hippocampus of adult male rats. Neuroendocrinology. 2014;100: 129–140. doi: 10.1159/000367849 25228100

89. Masocha W. CD200 receptors are differentially expressed and modulated by minocycline in the brain during Trypanosoma brucei infection. J Neuroimmunol. 2010. doi: 10.1016/j.jneuroim.2010.05.033 20627327


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