Early life stress perturbs the maturation of microglia in the developing hippocampus

Brain, Behavior, and Immunity

Volumn 57, Issue , 2016, Pages 79-93

  Delpech, Jean Christophe ^a   Wei, Lan ^a   Hao, Jin ^a   Yu, Xiaoqing ^a   Madore, Charlotte ^b   Butovsky, Oleg ^b   Kaffman, Arie ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Creb1; Early life stress; Hippocampus; Microglia; Phagocytosis; PU.1; RelA; Sp1

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; TRANSCRIPTION FACTOR PU 1; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR SP1;

AGE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN DEVELOPMENT; CELL COUNT; CELL DENSITY; CELL MIGRATION; CELL STRUCTURE; CONTROLLED STUDY; EARLY LIFE STRESS; EX VIVO STUDY; FEMALE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HIPPOCAMPUS; INFLAMMATION; JUVENILE ANIMAL; MALE; MATERNAL DEPRIVATION; MICROGLIA; MOUSE; NONHUMAN; PERINATAL PERIOD; PHAGOCYTOSIS; PRIORITY JOURNAL; PROMOTER REGION; ANIMAL; BAGG ALBINO MOUSE; GROWTH, DEVELOPMENT AND AGING; MENTAL STRESS; METABOLISM;

AGE FACTORS; ANIMALS; HIPPOCAMPUS; MATERNAL DEPRIVATION; MICE; MICE, INBRED BALB C; MICROGLIA; STRESS, PSYCHOLOGICAL;

EID: 84992170640     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2016.06.006     Document Type: Article

References (79)

1. Bellavance, M.A., Rivest, S., The HPA – immune axis and the immunomodulatory actions of glucocorticoids in the brain. Front. Immunol., 5, 2014, 136.
2. Bhatt, A., Fan, L.W., Pang, Y., Strategies for myelin regeneration: lessons learned from development. Neural Regener. Res. 9 (2014), 1347–1350.
3. Bilbo, S.D., Newsum, N.J., Sprunger, D.B., Watkins, L.R., Rudy, J.W., Maier, S.F., Differential effects of neonatal handling on early life infection-induced alterations in cognition in adulthood. Brain Behav. Immun. 21 (2007), 332–342.
4. Bolton, J.L., Huff, N.C., Smith, S.H., Mason, S.N., Foster, W.M., Auten, R.L., Bilbo, S.D., Maternal stress and effects of prenatal air pollution on offspring mental health outcomes in mice. Environ. Health Perspect. 121 (2013), 1075–1082.
5. Bredy, T.W., Grant, R.J., Champagne, D.L., Meaney, M.J., Maternal care influences neuronal survival in the hippocampus of the rat. Eur. J. Neurosci. 18 (2003), 2903–2909.
6. Butovsky, O., Jedrychowski, M.P., Moore, C.S., Cialic, R., Lanser, A.J., Gabriely, G., Koeglsperger, T., Dake, B., Wu, P.M., Doykan, C.E., Fanek, Z., Liu, L., Chen, Z., Rothstein, J.D., Ransohoff, R.M., Gygi, S.P., Antel, J.P., Weiner, H.L., Identification of a unique TGF-beta-dependent molecular and functional signature in microglia. Nat. Neurosci. 17 (2014), 131–143.
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. 31 (2006), 149–160.
8. Carrion, V.G., Haas, B.W., Garrett, A., Song, S., Reiss, A.L., Reduced hippocampal activity in youth with posttraumatic stress symptoms: an FMRI study. J. Pediatr. Psychol. 35 (2010), 559–569.
9. Chamak, B., Morandi, V., Mallat, M., Brain macrophages stimulate neurite growth and regeneration by secreting thrombospondin. J. Neurosci. Res. 38 (1994), 221–233.
10. Champagne, D.L., Bagot, R.C., van Hasselt, F., Ramakers, G., Meaney, M.J., de Kloet, E.R., Joels, M., Krugers, H., Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. J. Neurosci. 28 (2008), 6037–6045.
11. Chugani, D.C., Muzik, O., Juhasz, C., Janisse, J.J., Ager, J., Chugani, H.T., Postnatal maturation of human GABAA receptors measured with positron emission tomography. Ann. Neurol. 49 (2001), 618–626.
12. Chugani, H.T., Behen, M.E., Muzik, O., Juhasz, C., Nagy, F., Chugani, D.C., Local brain functional activity following early deprivation: a study of postinstitutionalized Romanian orphans. Neuroimage 14 (2001), 1290–1301.
13. Coelho, R., Viola, T.W., Walss-Bass, C., Brietzke, E., Grassi-Oliveira, R., Childhood maltreatment and inflammatory markers: a systematic review. Acta Psychiatr. Scand. 129 (2014), 180–192.
14. Cunningham, C.L., Martinez-Cerdeno, V., Noctor, S.C., Microglia regulate the number of neural precursor cells in the developing cerebral cortex. J. Neurosci. 33 (2013), 4216–4233.
15. Dalmau, I., Finsen, B., Zimmer, J., Gonzalez, B., Castellano, B., Development of microglia in the postnatal rat hippocampus. Hippocampus 8 (1998), 458–474.
16. Diz-Chaves, Y., Astiz, M., Bellini, M.J., Garcia-Segura, L.M., Prenatal stress increases the expression of proinflammatory cytokines and exacerbates the inflammatory response to LPS in the hippocampal formation of adult male mice. Brain Behav. Immun. 28 (2013), 196–206.
17. Diz-Chaves, Y., Pernia, O., Carrero, P., Garcia-Segura, L.M., Prenatal stress causes alterations in the morphology of microglia and the inflammatory response of the hippocampus of adult female mice. J. Neuroinflammation, 9, 2012, 71.
18. Eaton, S.L., Roche, S.L., Llavero Hurtado, M., Oldknow, K.J., Farquharson, C., Gillingwater, T.H., Wishart, T.M., Total protein analysis as a reliable loading control for quantitative fluorescent Western blotting. PLoS ONE, 8, 2013, e72457.
19. Erblich, B., Zhu, L., Etgen, A.M., Dobrenis, K., Pollard, J.W., Absence of colony stimulation factor-1 receptor results in loss of microglia, disrupted brain development and olfactory deficits. PLoS ONE, 6, 2011, e26317.
20. Faulkner, R.L., Low, L.K., Cheng, H.J., Axon pruning in the developing vertebrate hippocampus. Dev. Neurosci. 29 (2007), 6–13.
21. Feng, R., Desbordes, S.C., Xie, H., Tillo, E.S., Pixley, F., Stanley, E.R., Graf, T., PU.1 and C/EBPalpha/beta convert fibroblasts into macrophage-like cells. Proc. Natl. Acad. Sci. U.S.A. 105 (2008), 6057–6062.
22. Frank, M.G., Watkins, L.R., Maier, S.F., Stress- and glucocorticoid-induced priming of neuroinflammatory responses: potential mechanisms of stress-induced vulnerability to drugs of abuse. Brain Behav. Immun. 25:Suppl 1 (2011), S21–S28.
23. Garofalo, R., Cytokines in human milk. J. Pediatr. 156 (2010), S36–S40.
24. Garrett, A.S., Carrion, V., Kletter, H., Karchemskiy, A., Weems, C.F., Reiss, A., Brain activation to facial expressions in youth with PTSD symptoms. Depress Anxiety 29 (2012), 449–459.
25. Ghosh, S., Geahlen, R.L., Stress granules modulate SYK to cause microglial cell dysfunction in Alzheimer's Disease. EBioMedicine 2 (2015), 1785–1798.
26. Gomez-Gonzalez, B., Escobar, A., Prenatal stress alters microglial development and distribution in postnatal rat brain. Acta Neuropathol. 119 (2010), 303–315.
27. Hao, S., Dey, A., Yu, X., Stranahan, A.M., Dietary obesity reversibly induces synaptic stripping by microglia and impairs hippocampal plasticity. Brain Behav. Immun. 51 (2016), 230–239.
28. Helmeke, C., Ovtscharoff, W. Jr., Poeggel, G., Braun, K., Juvenile emotional experience alters synaptic inputs on pyramidal neurons in the anterior cingulate cortex. Cereb. Cortex 11 (2001), 717–727.
29. Herringa, R.J., Birn, R.M., Ruttle, P.L., Burghy, C.A., Stodola, D.E., Davidson, R.J., Essex, M.J., Childhood maltreatment is associated with altered fear circuitry and increased internalizing symptoms by late adolescence. Proc. Natl. Acad. Sci. U.S.A. 110 (2013), 19119–19124.
30. Hess, J., Denenberg, V.H., Zarrow, M.X., Pfeifer, D., Modification of the corticosterone response curve as a function of handling in infancy. Physiol. Behav. 4 (1969), 109–111.
31. Hodes, G.E., Pfau, M.L., Leboeuf, M., Golden, S.A., Christoffel, D.J., Bregman, D., Rebusi, N., Heshmati, M., Aleyasin, H., Warren, B.L., Lebonte, B., Horn, S., Lapidus, K.A., Stelzhammer, V., Wong, E.H., Bahn, S., Krishnan, V., Bolanos-Guzman, C.A., Murrough, J.W., Merad, M., Russo, S.J., Individual differences in the peripheral immune system promote resilience versus susceptibility to social stress. Proc. Natl. Acad. Sci. U.S.A. 111 (2014), 16136–16141.
32. Ivy, A.S., Rex, C.S., Chen, Y., Dube, C., Maras, P.M., Grigoriadis, D.E., Gall, C.M., Lynch, G., Baram, T.Z., Hippocampal dysfunction and cognitive impairments provoked by chronic early-life stress involve excessive activation of CRH receptors. J. Neurosci. 30 (2010), 13005–13015.
33. Jackowski, A., Perera, T.D., Abdallah, C.G., Garrido, G., Tang, C.Y., Martinez, J., Mathew, S.J., Gorman, J.M., Rosenblum, L.A., Smith, E.L., Dwork, A.J., Shungu, D.C., Kaffman, A., Gelernter, J., Coplan, J.D., Kaufman, J., Early-life stress, corpus callosum development, hippocampal volumetrics, and anxious behavior in male nonhuman primates. Psychiatry Res. 192 (2011), 37–44.
34. Johnson, J.D., Campisi, J., Sharkey, C.M., Kennedy, S.L., Nickerson, M., Greenwood, B.N., Fleshner, M., Catecholamines mediate stress-induced increases in peripheral and central inflammatory cytokines. Neuroscience 135 (2005), 1295–1307.
35. Kaffman, A., Krystal, J.H., New frontiers in animal research of psychiatric illness. Methods Mol. Biol. 829 (2012), 3–30.
36. Kaur, C., Wu, C.H., Wen, C.Y., Ling, E.A., The effects of subcutaneous injections of glucocorticoids on amoeboid microglia in postnatal rats. Arch. Histol. Cytol. 57 (1994), 449–459.
37. Kierdorf, K., Erny, D., Goldmann, T., Sander, V., Schulz, C., Perdiguero, E.G., Wieghofer, P., Heinrich, A., Riemke, P., Holscher, C., Muller, D.N., Luckow, B., Brocker, T., Debowski, K., Fritz, G., Opdenakker, G., Diefenbach, A., Biber, K., Heikenwalder, M., Geissmann, F., Rosenbauer, F., Prinz, M., Microglia emerge from erythromyeloid precursors via Pu.1- and Irf8-dependent pathways. Nat. Neurosci. 16 (2013), 273–280.
38. Kritas, S.K., Saggini, A., Cerulli, G., Caraffa, A., Antinolfi, P., Pantalone, A., Rosati, M., Tei, M., Speziali, A., Saggini, R., Conti, P., Corticotropin-releasing hormone, microglia and mental disorders. Int. J. Immunopathol. Pharmacol. 27 (2014), 163–167.
39. Lenz, K.M., McCarthy, M.M., A starring role for microglia in brain sex differences. Neuroscientist 21 (2015), 306–321.
40. Lenz, K.M., Nugent, B.M., Haliyur, R., McCarthy, M.M., Microglia are essential to masculinization of brain and behavior. J. Neurosci. 33 (2013), 2761–2772.
41. Levine, S., Haltmeyer, G., Karas, G., Denenberg, V.H., Physiological and behavioral effects of infantile stimulation. Physiol. Behav. 2 (1967), 55–59.
42. Liu, D., Diorio, J., Day, J.C., Francis, D.D., Meaney, M.J., Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat. Neurosci. 3 (2000), 799–806.
43. Loi, M., Mossink, J.C., Meerhoff, G.F., Den Blaauwen, J.L., Lucassen, P.J., Joels, M., Effects of early-life stress on cognitive function and hippocampal structure in female rodents. Neuroscience, 2015.
44. Maheu, F.S., Dozier, M., Guyer, A.E., Mandell, D., Peloso, E., Poeth, K., Jenness, J., Lau, J.Y., Ackerman, J.P., Pine, D.S., Ernst, M., A preliminary study of medial temporal lobe function in youths with a history of caregiver deprivation and emotional neglect. Cog. Affect. Behav. Neurosci. 10 (2010), 34–49.
45. McNamee, E.N., Griffin, E.W., Ryan, K.M., Ryan, K.J., Heffernan, S., Harkin, A., Connor, T.J., Noradrenaline acting at beta-adrenoceptors induces expression of IL-1beta and its negative regulators IL-1ra and IL-1RII, and drives an overall anti-inflammatory phenotype in rat cortex. Neuropharmacology 59 (2010), 37–48.
46. Meaney, M.J., Aitken, D.H., Viau, V., Sharma, S., Sarrieau, A., Neonatal handling alters adrenocortical negative feedback sensitivity and hippocampal type II glucocorticoid receptor binding in the rat. Neuroendocrinology 50 (1989), 597–604.
47. Miron, V.E., Boyd, A., Zhao, J.W., Yuen, T.J., Ruckh, J.M., Shadrach, J.L., van Wijngaarden, P., Wagers, A.J., Williams, A., Franklin, R.J., ffrench-Constant, C., M2 microglia and macrophages drive oligodendrocyte differentiation during CNS remyelination. Nat. Neurosci. 16 (2013), 1211–1218.
48. Ock, J., Lee, H., Kim, S., Lee, W.H., Choi, D.K., Park, E.J., Kim, S.H., Kim, I.K., Suk, K., Induction of microglial apoptosis by corticotropin-releasing hormone. J. Neurochem. 98 (2006), 962–972.
49. Pace, T.W., Wingenfeld, K., Schmidt, I., Meinlschmidt, G., Hellhammer, D.H., Heim, C.M., Increased peripheral NF-kappaB pathway activity in women with childhood abuse-related posttraumatic stress disorder. Brain Behav. Immun. 26 (2012), 13–17.
50. Paolicelli, R.C., Bolasco, G., Pagani, F., Maggi, L., Scianni, M., Panzanelli, P., Giustetto, M., Ferreira, T.A., Guiducci, E., Dumas, L., Ragozzino, D., Gross, C.T., Synaptic pruning by microglia is necessary for normal brain development. Science 333 (2011), 1456–1458.
51. Paresce, D.M., Ghosh, R.N., Maxfield, F.R., Microglial cells internalize aggregates of the Alzheimer's disease amyloid beta-protein via a scavenger receptor. Neuron 17 (1996), 553–565.
52. Park, S.D., Cheon, S.Y., Park, T.Y., Shin, B.Y., Oh, H., Ghosh, S., Koo, B.N., Lee, S.K., Intranuclear interactomic inhibition of NF-kappaB suppresses LPS-induced severe sepsis. Biochem. Biophys. Res. Commun. 464 (2015), 711–717.
53. Parkhurst, C.N., Yang, G., Ninan, I., Savas, J.N., Yates, J.R. 3rd, Lafaille, J.J., Hempstead, B.L., Littman, D.R., Gan, W.B., Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell 155 (2013), 1596–1609.
54. Pfaffl, M.W., A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res., 29, 2001, e45.
55. Poeggel, G., Helmeke, C., Abraham, A., Schwabe, T., Friedrich, P., Braun, K., Juvenile emotional experience alters synaptic composition in the rodent cortex, hippocampus, and lateral amygdala. Proc. Natl. Acad. Sci. U.S.A. 100 (2003), 16137–16142.
56. Rice, R.A., Spangenberg, E.E., Yamate-Morgan, H., Lee, R.J., Arora, R.P., Hernandez, M.X., Tenner, A.J., West, B.L., Green, K.N., Elimination of microglia improves functional outcomes following extensive neuronal loss in the hippocampus. J. Neurosci. 35 (2015), 9977–9989.
57. Roque, A., Ochoa-Zarzosa, A., Torner, L., Maternal separation activates microglial cells and induces an inflammatory response in the hippocampus of male rat pups, independently of hypothalamic and peripheral cytokine levels. Brain Behav. Immun., 2015.
58. Roy, A., Fung, Y.K., Liu, X., Pahan, K., Up-regulation of microglial CD11b expression by nitric oxide. J. Biol. Chem. 281 (2006), 14971–14980.
59. Schafer, D.P., Lehrman, E.K., Kautzman, A.G., Koyama, R., Mardinly, A.R., Yamasaki, R., Ransohoff, R.M., Greenberg, M.E., Barres, B.A., Stevens, B., Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74 (2012), 691–705.
60. Smith, A.M., Gibbons, H.M., Oldfield, R.L., Bergin, P.M., Mee, E.W., Faull, R.L., Dragunow, M., The transcription factor PU.1 is critical for viability and function of human brain microglia. Glia 61 (2013), 929–942.
61. Spinelli, S., Chefer, S., Carson, R.E., Jagoda, E., Lang, L., Heilig, M., Barr, C.S., Suomi, S.J., Higley, J.D., Stein, E.A., Effects of early-life stress on serotonin(1A) receptors in juvenile Rhesus monkeys measured by positron emission tomography. Biol. Psychiatry 67 (2010), 1146–1153.
62. Stevens, S.L., Shaw, T.E., Dykhuizen, E., Lessov, N.S., Hill, J.K., Wurst, W., Stenzel-Poore, M.P., Reduced cerebral injury in CRH-R1 deficient mice after focal ischemia: a potential link to microglia and atrocytes that express CRH-R1. J. Cereb. Blood Flow Metab. 23 (2003), 1151–1159.
63. Steward, O., Falk, P.M., Selective localization of polyribosomes beneath developing synapses: a quantitative analysis of the relationships between polyribosomes and developing synapses in the hippocampus and dentate gyrus. J. Comp. Neurol. 314 (1991), 545–557.
64. Takatsuru, Y., Nabekura, J., Ishikawa, T., Kohsaka, S., Koibuchi, N., Early-life stress increases the motility of microglia in adulthood. J. Physiol. Sci. 65 (2015), 187–194.
65. Takenouchi, T., Nakai, M., Iwamaru, Y., Sugama, S., Tsukimoto, M., Fujita, M., Wei, J., Sekigawa, A., Sato, M., Kojima, S., Kitani, H., Hashimoto, M., The activation of P2X7 receptor impairs lysosomal functions and stimulates the release of autophagolysosomes in microglial cells. J. Immunol. 182 (2009), 2051–2062.
66. 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. Nat. Neurosci. 16 (2013), 543–551.
67. Wakselman, S., Bechade, C., Roumier, A., Bernard, D., Triller, A., Bessis, A., Developmental neuronal death in hippocampus requires the microglial CD11b integrin and DAP12 immunoreceptor. J. Neurosci. 28 (2008), 8138–8143.
68. Wang, X.D., Su, Y.A., Wagner, K.V., Avrabos, C., Scharf, S.H., Hartmann, J., Wolf, M., Liebl, C., Kuhne, C., Wurst, W., Holsboer, F., Eder, M., Deussing, J.M., Muller, M.B., Schmidt, M.V., Nectin-3 links CRHR1 signaling to stress-induced memory deficits and spine loss. Nat. Neurosci. 16 (2013), 706–713.
69. Wei, L., David, A., Duman, R.S., Anisman, H., Kaffman, A., Early life stress increases anxiety-like behavior in Balb c mice despite a compensatory increase in levels of postnatal maternal care. Horm. Behav. 57 (2010), 396–404.
70. Wei, L., Hao, J., Kaffman, A., Early life stress inhibits expression of ribosomal RNA in the developing hippocampus. PLoS ONE, 9, 2014, e115283.
71. Wei, L., Hao, J., Lacher, R.K., Abbott, T., Chung, L., Colangelo, C.M., Kaffman, A., Early-life stress perturbs key cellular programs in the developing mouse hippocampus. Dev. Neurosci., 2015.
72. Wei, L., Meaney, M.J., Duman, R.S., Kaffman, A., Affiliative behavior requires juvenile, but not adult neurogenesis. J. Neurosci. 31 (2011), 14335–14345.
73. Wei, L., Simen, A., Mane, S., Kaffman, A., Early life stress inhibits expression of a novel innate immune pathway in the developing hippocampus. Neuropsychopharmacology 37 (2012), 567–580.
74. Wen, A.Y., Sakamoto, K.M., Miller, L.S., The role of the transcription factor CREB in immune function. J. Immunol. 185 (2010), 6413–6419.
75. Wohleb, E.S., Hanke, M.L., Corona, A.W., Powell, N.D., Stiner, L.M., Bailey, M.T., Nelson, R.J., Godbout, J.P., Sheridan, J.F., Beta-Adrenergic receptor antagonism prevents anxiety-like behavior and microglial reactivity induced by repeated social defeat. J. Neurosci. 31 (2011), 6277–6288.
76. Wohleb, E.S., McKim, D.B., Shea, D.T., Powell, N.D., Tarr, A.J., Sheridan, J.F., Godbout, J.P., Re-establishment of anxiety in stress-sensitized mice is caused by monocyte trafficking from the spleen to the brain. Biol. Psychiatry 75 (2014), 970–981.
77. Wohleb, E.S., Powell, N.D., Godbout, J.P., Sheridan, J.F., Stress-induced recruitment of bone marrow-derived monocytes to the brain promotes anxiety-like behavior. J. Neurosci. 33 (2013), 13820–13833.
78. Wu, C.H., Chien, H.F., Chang, C.Y., Chen, S.H., Huang, Y.S., Response of amoeboid and differentiating ramified microglia to glucocorticoids in postnatal rats: a lectin histochemical and ultrastructural study. Neurosci. Res. 40 (2001), 235–244.
79. Yeamans, C., Wang, D., Paz-Priel, I., Torbett, B.E., Tenen, D.G., Friedman, A.D., C/EBPalpha binds and activates the PU.1 distal enhancer to induce monocyte lineage commitment. Blood 110 (2007), 3136–3142.