CX3CR1 ablation ameliorates motor and respiratory dysfunctions and improves survival of a Rett syndrome mouse model

Brain, Behavior, and Immunity

Volumn 60, Issue , 2017, Pages 106-116

  Horiuchi, Makoto ^a   Smith, Lucas ^a   Maezawa, Izumi ^a,b   Jin, Lee Way ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

CX3CR1; MeCP2; Microglia; Rett syndrome

Indexed keywords

CHEMOKINE RECEPTOR CX3CR1; MESSENGER RNA; SOMATOMEDIN C; CX3CR1 PROTEIN, MOUSE; METHYL CPG BINDING PROTEIN 2; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ANIMAL MODEL; APNEA; ARTICLE; BODY SIZE; BONE MARROW CELL; BREATHING PATTERN; CELL COUNT; CELL SIZE; CONTROLLED STUDY; DISEASE COURSE; DOWN REGULATION; GENOTYPE; HIPPOCAMPAL CA2 REGION; LIFESPAN; MEDIAN SURVIVAL TIME; MICROGLIA; MOTOR COORDINATION; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; MOUSE; NONHUMAN; PEAK EXPIRATORY FLOW; PEAK INSPIRATORY FLOW; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; RESPIRATORY FAILURE; RETT SYNDROME; SOMATIC CELL; SURVIVAL RATE; WEIGHT GAIN; ANIMAL; BRAIN; DISEASE MODEL; GENETICS; KNOCKOUT MOUSE; METABOLISM; MORTALITY; MUTATION; NERVE CELL; TOXICITY AND INTOXICATION;

ANIMALS; BRAIN; CX3C CHEMOKINE RECEPTOR 1; DISEASE MODELS, ANIMAL; METHYL-CPG-BINDING PROTEIN 2; MICE, KNOCKOUT; MICROGLIA; MUTATION; NEURONS; NEUROTOXICITY SYNDROMES; REACTIVE OXYGEN SPECIES; RETT SYNDROME;

EID: 84983523631     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2016.02.014     Document Type: Article

References (55)

1. Abdala, A.P., Dutschmann, M., Bissonnette, J.M., Paton, J.F., Correction of respiratory disorders in a mouse model of Rett syndrome. Proc Natl Acad Sci U.S.A. 107 (2010), 18208–18213.
2. Alvarez-Saavedra, M., Saez, M.A., Kang, D., Zoghbi, H.Y., Young, J.I., Cell-specific expression of wild-type MeCP2 in mouse models of Rett syndrome yields insight about pathogenesis. Human Mol. Genet. 16 (2007), 2315–2325.
3. Amir, R.E., Van den Veyver, I.B., Wan, M., Tran, C.Q., Francke, U., Zoghbi, H.Y., Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat. Genet. 23 (1999), 185–188.
4. Baxter, R.C., IGF binding proteins in cancer: mechanistic and clinical insights. Nat. Rev. Cancer 14 (2014), 329–341.
5. Bilimoria, P.M., Stevens, B., Microglia function during brain development: new insights from animal models. Brain Res. 1617 (2015), 7–17.
6. Cardona, A.E., Pioro, E.P., Sasse, M.E., Kostenko, V., Cardona, S.M., Dijkstra, I.M., Huang, D., Kidd, G., Dombrowski, S., Dutta, R., Lee, J.C., Cook, D.N., Jung, S., Lira, S.A., Littman, D.R., Ransohoff, R.M., Control of microglial neurotoxicity by the fractalkine receptor. Nature Neurosci. 9 (2006), 917–924.
7. Castro, J., Garcia, R.I., Kwok, S., Banerjee, A., Petravicz, J., Woodson, J., Mellios, N., Tropea, D., Sur, M., Functional recovery with recombinant human IGF1 treatment in a mouse model of Rett Syndrome. Proc. Natl. Acad. Sci. U.S.A. 111 (2014), 9941–9946.
8. Chahrour, M., Zoghbi, H.Y., The story of Rett syndrome: from clinic to neurobiology. Neuron 56 (2007), 422–437.
9. Chahrour, M., Jung, S.Y., Shaw, C., Zhou, X., Wong, S.T., Qin, J., Zoghbi, H.Y., MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 320 (2008), 1224–1229.
10. Chao, H.T., Chen, H., Samaco, R.C., Xue, M., Chahrour, M., Yoo, J., Neul, J.L., Gong, S., Lu, H.C., Heintz, N., Ekker, M., Rubenstein, J.L., Noebels, J.L., Rosenmund, C., Zoghbi, H.Y., Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes. Nature 468 (2010), 263–269.
11. Chen, R.Z., Akbarian, S., Tudor, M., Jaenisch, R., Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat. Genet. 27 (2001), 327–331.
12. Collins, S.M., Surette, M., Bercik, P., The interplay between the intestinal microbiota and the brain. Nat. Rev. Microbiol. 10 (2012), 735–742.
13. Cronk, J.C., Derecki, N.C., Litvak, V., Kipnis, J., Unexpected cellular players in Rett syndrome pathology. Neurobiol. Dis., 2015.
14. Cronk, J.C., Derecki, N.C., Ji, E., Xu, Y., Lampano, A.E., Smirnov, I., Baker, W., Norris, G.T., Marin, I., Coddington, N., Wolf, Y., Turner, S.D., Aderem, A., Klibanov, A.L., Harris, T.H., Jung, S., Litvak, V., Kipnis, J., Methyl-CpG binding protein 2 regulates microglia and macrophage gene expression in response to inflammatory stimuli. Immunity 42 (2015), 679–691.
15. Deacon, R.M.J., Measuring motor coordination in mice. Jove J. Vis. Exp., 2013.
16. Derecki, N.C., Cronk, J.C., Lu, Z., Xu, E., Abbott, S.B., Guyenet, P.G., Kipnis, J., Wild-type microglia arrest pathology in a mouse model of Rett syndrome. Nature 484 (2012), 105–109.
17. Derecki, N.C., Cronk, J.C., Kipnis, J., The role of microglia in brain maintenance: implications for Rett syndrome. Trends Immunol. 34 (2013), 144–150.
18. Garg, S.K., Lioy, D.T., Cheval, H., McGann, J.C., Bissonnette, J.M., Murtha, M.J., Foust, K.D., Kaspar, B.K., Bird, A., Mandel, G., Systemic delivery of MeCP2 rescues behavioral and cellular deficits in female mouse models of rett syndrome. J Neurosci 33 (2013), 13612–13620.
19. Gonzales M.L., LaSalle, J.M., 2010. The role of MeCP2 in brain development and neurodevelopmental disorders. Current Psychiatry Reports.
20. Guy, J., Hendrich, B., Holmes, M., Martin, J.E., Bird, A., A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat. Genet. 27 (2001), 322–326.
21. Guy, J., Gan, J., Selfridge, J., Cobb, S., Bird, A., Reversal of neurological defects in a mouse model of Rett syndrome. Science 315 (2007), 1143–1147.
22. Harrison, J.K., Jiang, Y., Chen, S.Z., Xia, Y.Y., Maciejewski, D., McNamara, R.K., Streit, W.J., Salafranca, M.N., Adhikari, S., Thompson, D.A., Botti, P., Bacon, K.B., Feng, L.L., Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc. Natl. Acad. Sci. U.S.A. 95 (1998), 10896–10901.
23. Jin, L.W., Horiuchi, M., Wulff, H., Liu, X.B., Cortopassi, G.A., Erickson, J.D., Maezawa, I., Dysregulation of glutamine transporter SNAT1 in Rett syndrome microglia: a mechanism for mitochondrial dysfunction and neurotoxicity. J. Neurosci. 35 (2015), 2516–2529.
24. Katz, D.M., Dutschmann, M., Ramirez, J.M., Hilaire, G., Breathing disorders in Rett syndrome: progressive neurochemical dysfunction in the respiratory network after birth. Respir. Physiol. Neurobiol. 168 (2009), 101–108.
25. Khroyan, T.V., Zhang, J.X., Yang, L.Y., Zou, B.D., Xie, J., Pascual, C., Malik, A., Xie, J.L., Zaveri, N.T., Vazquez, J., Polgar, W., Toll, L., Fang, J.D., Xie, X.M., Rodent motor and neuropsychological behaviour measured in home cages using the integrated modular platform SmartCage (TM). Clin. Exp. Pharmacol. Physiol. 39 (2012), 614–622.
26. Kiyomoto, M., Shinoda, M., Okada-Ogawa, A., Noma, N., Shibuta, K., Tsuboi, Y., Sessle, B.J., Imamura, Y., Iwata, K., Fractalkine signaling in microglia contributes to ectopic orofacial pain following trapezius muscle inflammation. J. Neurosci. 33 (2013), 7667–7680.
27. Levitt, P., Campbell, D.B., The genetic and neurobiologic compass points toward common signaling dysfunctions in autism spectrum disorders. J. Clin. Invest. 119 (2009), 747–754.
28. Li, Y., Du, X.F., Liu, C.S., Wen, Z.L., Du, J.L., Reciprocal regulation between resting microglial dynamics and neuronal activity in vivo. Dev. Cell 23 (2012), 1189–1202.
29. 3CR1 signaling. Front. Cell. Neurosci., 8, 2014.
30. Lioy, D.T., Garg, S.K., Monaghan, C.E., Raber, J., Foust, K.D., Kaspar, B.K., Hirrlinger, P.G., Kirchhoff, F., Bissonnette, J.M., Ballas, N., Mandel, G., A role for glia in the progression of Rett's syndrome. Nature 475 (2011), 497–500.
31. Livak, K.J., Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25 (2001), 402–408.
32. Maezawa, I., Jin, L.W., Rett syndrome microglia damage dendrites and synapses by the elevated release of glutamate. J. Neurosci. 30 (2010), 5346–5356.
33. Maezawa, I., Calafiore, M., Wulff, H., Jin, L.W., Does microglial dysfunction play a role in autism and Rett syndrome?. Neuron. Glia Biol. 7 (2011), 85–97.
34. Moretti, P., Zoghbi, H.Y., MeCP2 dysfunction in Rett syndrome and related disorders. Curr. Opin. Genet. Dev. 16 (2006), 276–281.
35. Nagarajan, R.P., Patzel, K.A., Martin, M., Yasui, D.H., Swanberg, S.E., Hertz-Picciotto, I., Hansen, R.L., Van de Water, J., Pessah, I.N., Jiang, R., Robinson, W.P., LaSalle, J.M., MECP2 promoter methylation and X chromosome inactivation in autism. Autism Res. 1 (2008), 169–178.
36. Niess, J.H., Brand, S., Gu, X., Landsman, L., Jung, S., McCormick, B.A., Vyas, J.M., Boes, M., Ploegh, H.L., Fox, J.G., Littman, D.R., Reinecker, H.C., CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 307 (2005), 254–258.
37. Poupel, L., Boissonnas, A., Hermand, P., Dorgham, K., Guyon, E., Auvynet, C., Charles, F.S., Lesnik, P., Deterre, P., Combadiere, C., Pharmacological inhibition of the chemokine receptor, CX3CR1, reduces atherosclerosis in mice. Arteriosclerosis Thrombosis Vasc. Biol. 33 (2013), 2297–2305.
38. Ramocki, M.B., Peters, S.U., Tavyev, Y.J., Zhang, F., Carvalho, C.M., Schaaf, C.P., Richman, R., Fang, P., Glaze, D.G., Lupski, J.R., Zoghbi, H.Y., Autism and other neuropsychiatric symptoms are prevalent in individuals with MeCP2 duplication syndrome. Ann. Neurol. 66 (2009), 771–782.
39. Ridderstad Wollberg, A., Ericsson-Dahlstrand, A., Jureus, A., Ekerot, P., Simon, S., Nilsson, M., Wiklund, S.J., Berg, A.L., Ferm, M., Sunnemark, D., Johansson, R., Pharmacological inhibition of the chemokine receptor CX3CR1 attenuates disease in a chronic-relapsing rat model for multiple sclerosis. Proc. Natl. Acad. Sci. U.S.A. 111 (2014), 5409–5414.
40. Robinson, L., Guy, J., McKay, L., Brockett, E., Spike, R.C., Selfridge, J., De Sousa, D., Merusi, C., Riedel, G., Bird, A., Cobb, S.R., Morphological and functional reversal of phenotypes in a mouse model of Rett syndrome. Brain 135 (2012), 2699–2710.
41. Samaco, R.C., Hogart, A., LaSalle, J.M., Epigenetic overlap in autism-spectrum neurodevelopmental disorders: MECP2 deficiency causes reduced expression of UBE3A and GABRB3. Human Mol. Genet. 14 (2005), 483–492.
42. Schafer, D.P., Lehrman, E.K., Stevens, B., The “quad-partite” synapse: microglia-synapse interactions in the developing and mature CNS. Glia 61 (2013), 24–36.
43. Sheridan, G.K., Murphy, K.J., Neuron-glia crosstalk in health and disease: fractalkine and CX3CR1 take centre stage. Open Biol., 3, 2013, 130181.
44. Stearns, N.A., Schaevitz, L.R., Bowling, H., Nag, N., Berger, U.V., Berger-Sweeney, J., Behavioral and anatomical abnormalities in Mecp2 mutant mice: a model for Rett syndrome. Neuroscience 146 (2007), 907–921.
45. Ueno, M., Fujita, Y., Tanaka, T., Nakamura, Y., Kikuta, J., Ishii, M., Yamashita, T., Layer V cortical neurons require microglial support for survival during postnatal development. Nature Neurosci. 16 (2013), 543–551.
46. Viemari, J.C., Roux, J.C., Tryba, A.K., Saywell, V., Burnet, H., Pena, F., Zanella, S., Bevengut, M., Barthelemy-Requin, M., Herzing, L.B., Moncla, A., Mancini, J., Ramirez, J.M., Villard, L., Hilaire, G., Mecp2 deficiency disrupts norepinephrine and respiratory systems in mice. J. Neurosci. 25 (2005), 11521–11530.
47. Voituron, N., Hilaire, G., The benzodiazepine Midazolam mitigates the breathing defects of Mecp2-deficient mice. Respir. Physiol. Neurobiol. 177 (2011), 56–60.
48. Vrinten, D.H., Hamers, F.F.T., ‘CatWalk’ automated quantitative gait analysis as a novel method to assess mechanical allodynia in the rat; a comparison with von Frey testing. Pain 102 (2003), 203–209.
49. Wake, H., Moorhouse, A.J., Jinno, S., Kohsaka, S., Nabekura, J., Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. J. Neurosci. 29 (2009), 3974–3980.
50. Wang, J., et al. Wild-type microglia do not reverse pathology in mouse models of Rett syndrome. Nature, 521, 2015 E1-4.
51. Wu, J., Bie, B., Yang, H., Xu, J.J., Brown, D.L., Naguib, M., Suppression of central chemokine fractalkine receptor signaling alleviates amyloid-induced memory deficiency. Neurobiol. Aging 34 (2013), 2843–2852.
52. Yee, D., Jackson, J.G., Kozelsky, T.W., Figueroa, J.A., Insulin-like growth-factor binding protein-1 expression inhibits insulin-like growth factor-I action in Mcf-7 breast–cancer cells. Cell. Growth Differ. 5 (1994), 73–77.
53. Zanella, S., Mebarek, S., Lajard, A.M., Picard, N., Dutschniann, M., Hilaire, G., Oral treatment with desipramine improves breathing and life span in Rett syndrome mouse model. Respir. Physiol. Neurobiol. 160 (2008), 116–121.
54. Zhan, Y., Paolicelli, R.C., Sforazzini, F., Weinhard, L., Bolasco, G., Pagani, F., Vyssotski, A.L., Bifone, A., Gozzi, A., Ragozzino, D., Gross, C.T., Deficient neuron–microglia signaling results in impaired functional brain connectivity and social behavior. Nature Neurosci. 17 (2014), 400–406.
55. Zoghbi, H.Y., Postnatal neurodevelopmental disorders: meeting at the synapse?. Science 302 (2003), 826–830.