A novel microglial subset plays a key role in myelinogenesis in developing brain

EMBO Journal

Volumn 36, Issue 22, 2017, Pages 3292-3308

  Wlodarczyk, Agnieszka ^a   Holtman, Inge R ^b   Krueger, Martin ^c   Yogev, Nir ^d   Bruttger, Julia ^d   Khorooshi, Reza ^a   Benmamar Badel, Anouk ^a,e   de Boer Bergsma, Jelkje J ^b   Martin, Nellie A ^f   Karram, Khalad ^d   Kramer, Isabella ^a   Boddeke, Erik WGM ^b   Waisman, Ari ^d   Eggen, Bart JL ^b   Owens, Trevor ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c UNIVERSITY OF LEIPZIG   (Germany)

^d UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^e UNIVERSITÉ DE LYON   (France)

^f ODENSE UNIVERSITY HOSPITAL   (Denmark)

Author keywords

CD11c; IGF1; microglia; myelinogenesis

Indexed keywords

SOMATOMEDIN C; BIOLOGICAL MARKER; GLYCOPROTEIN P 15095;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DEVELOPMENT; CELL DIFFERENTIATION; CELL EXPANSION; CELL FUNCTION; CELL MIGRATION; CELL SURVIVAL; CONTROLLED STUDY; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; MICROGLIA; MOUSE; MYELINATION; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM INFLAMMATION; NEWBORN; NONHUMAN; PERINATAL PERIOD; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; UPREGULATION; AGING; ANIMAL; BRAIN; C57BL MOUSE; CELL AGGREGATION; CYTOLOGY; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MYELIN SHEATH; NEUROECTODERM; PATHOLOGY; ULTRASTRUCTURE;

AGING; ANIMALS; ANIMALS, NEWBORN; BIOMARKERS; BRAIN; CD11C ANTIGEN; CELL AGGREGATION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INSULIN-LIKE GROWTH FACTOR I; MICE, INBRED C57BL; MICROGLIA; MYELIN SHEATH; NEURAL PLATE; NEUROGENESIS; UP-REGULATION;

EID: 85030459487     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201696056     Document Type: Article

References (57)

1. Ajami B, Bennett JL, Krieger C, Tetzlaff W, Rossi FM (2007) Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat Neurosci 10: 1538–1543
2. Anders S, Pyl PT, Huber W (2015) HTSeq–a Python framework to work with high-throughput sequencing data. Bioinformatics 31: 166–169
3. Askew K, Li K, Olmos-Alonso A, Garcia-Moreno F, Liang Y, Richardson P, Tipton T, Chapman MA, Riecken K, Beccari S, Sierra A, Molnar Z, Cragg MS, Garaschuk O, Perry VH, Gomez-Nicola D (2017) Coupled proliferation and apoptosis maintain the rapid turnover of microglia in the adult brain. Cell Rep 18: 391–405
4. Beck KD, Powell-Braxton L, Widmer HR, Valverde J, Hefti F (1995) Igf1 gene disruption results in reduced brain size, CNS hypomyelination, and loss of hippocampal granule and striatal parvalbumin-containing neurons. Neuron 14: 717–730
5. Bennett ML, Bennett FC, Liddelow SA, Ajami B, Zamanian JL, Fernhoff NB, Mulinyawe SB, Bohlen CJ, Adil A, Tucker A, Weissman IL, Chang EF, Li G, Grant GA, Hayden Gephart MG, Barres BA (2016) New tools for studying microglia in the mouse and human CNS. Proc Natl Acad Sci USA 113: E1738–E1746
6. Biber K, Owens T, Boddeke E (2014) What is microglia neurotoxicity (Not)? Glia 62: 841–854
7. Bruttger J, Karram K, Wortge S, Regen T, Marini F, Hoppmann N, Klein M, Blank T, Yona S, Wolf Y, Mack M, Pinteaux E, Muller W, Zipp F, Binder H, Bopp T, Prinz M, Jung S, Waisman A (2015) Genetic cell ablation reveals clusters of local self-renewing microglia in the mammalian central nervous system. Immunity 43: 92–106
8. Buchser WJ, Smith RP, Pardinas JR, Haddox CL, Hutson T, Moon L, Hoffman SR, Bixby JL, Lemmon VP (2012) Peripheral nervous system genes expressed in central neurons induce growth on inhibitory substrates. PLoS ONE 7: e38101
9. Butovsky O, Koronyo-Hamaoui M, Kunis G, Ophir E, Landa G, Cohen H, Schwartz M (2006) Glatiramer acetate fights against Alzheimer's disease by inducing dendritic-like microglia expressing insulin-like growth factor 1. Proc Natl Acad Sci USA 103: 11784–11789
10. Butovsky O, Jedrychowski MP, Moore CS, Cialic R, Lanser AJ, Gabriely G, Koeglsperger T, Dake B, Wu PM, Doykan CE, Fanek Z, Liu L, Chen Z, Rothstein JD, Ransohoff RM, Gygi SP, Antel JP, Weiner HL (2014) Identification of a unique TGF-beta-dependent molecular and functional signature in microglia. Nat Neurosci 17: 131–143
11. Camby I, Le Mercier M, Lefranc F, Kiss R (2006) Galectin-1: a small protein with major functions. Glycobiology 16: 137R–157R
12. Cravens PD, Kieseier BC, Hussain R, Herndon E, Arellano B, Ben LH, Timmons BC, Castro-Rojas C, Hartung HP, Hemmer B, Weber MS, Zamvil SS, Stuve O (2013) The neonatal CNS is not conducive for encephalitogenic Th1 T cells and B cells during experimental autoimmune encephalomyelitis. J Neuroinflammation 10: 67
13. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29: 15–21
14. Elmore MR, Najafi AR, Koike MA, Dagher NN, Spangenberg EE, Rice RA, Kitazawa M, Matusow B, Nguyen H, West BL, Green KN (2014) Colony-stimulating factor 1 receptor signaling is necessary for microglia viability, unmasking a microglia progenitor cell in the adult brain. Neuron 82: 380–397
15. Garcia-Gutierrez P, Juarez-Vicente F, Wolgemuth DJ, Garcia-Dominguez M (2014) Pleiotrophin antagonizes Brd2 during neuronal differentiation. J Cell Sci 127: 2554–2564
16. Ginhoux F, Greter M, Leboeuf M, Nandi S, See P, Gokhan S, Mehler MF, Conway SJ, Ng LG, Stanley ER, Samokhvalov IM, Merad M (2010) Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330: 841–845
17. Ginhoux F, Lim S, Hoeffel G, Low D, Huber T (2013) Origin and differentiation of microglia. Front Cell Neurosci 7: 45
18. Goldmann T, Wieghofer P, Muller PF, Wolf Y, Varol D, Yona S, Brendecke SM, Kierdorf K, Staszewski O, Datta M, Luedde T, Heikenwalder M, Jung S, Prinz M (2013) A new type of microglia gene targeting shows TAK1 to be pivotal in CNS autoimmune inflammation. Nat Neurosci 16: 1618–1626
19. Holtman IR, Noback M, Bijlsma M, Duong KN, van der Geest MA, Ketelaars PT, Brouwer N, Vainchtein ID, Eggen BJ, Boddeke HW (2015) Glia Open Access Database (GOAD): a comprehensive gene expression encyclopedia of glia cells in health and disease. Glia 63: 1495–1506
20. Horie H, Inagaki Y, Sohma Y, Nozawa R, Okawa K, Hasegawa M, Muramatsu N, Kawano H, Horie M, Koyama H, Sakai I, Takeshita K, Kowada Y, Takano M, Kadoya T (1999) Galectin-1 regulates initial axonal growth in peripheral nerves after axotomy. J Neurosci 19: 9964–9974
21. Huang DW, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44–57
22. Kettenmann H, Kirchhoff F, Verkhratsky A (2013) Microglia: new roles for the synaptic stripper. Neuron 77: 10–18
23. Khorooshi R, Owens T (2013) Detection and cellular localization of phospho-STAT2 in the central nervous system by immunohistochemical staining. Methods Mol Biol 967: 179–188
24. Khorooshi R, Morch MT, Holm TH, Berg CT, Dieu RT, Draeby D, Issazadeh-Navikas S, Weiss S, Lienenklaus S, Owens T (2015) Induction of endogenous Type I interferon within the central nervous system plays a protective role in experimental autoimmune encephalomyelitis. Acta Neuropathol 130: 107–118
25. Kierdorf K, Erny D, Goldmann T, Sander V, Schulz C, Perdiguero EG, Wieghofer P, Heinrich A, Riemke P, Holscher C, Muller DN, Luckow B, Brocker T, Debowski K, Fritz G, Opdenakker G, Diefenbach A, Biber K, Heikenwalder M, Geissmann F et al (2013) Microglia emerge from erythromyeloid precursors via Pu.1- and Irf8-dependent pathways. Nat Neurosci 16: 273–280
26. Krishnasamy S, Weng YC, Thammisetty SS, Phaneuf D, Lalancette-Hebert M, Kriz J (2017) Molecular imaging of nestin in neuroinflammatory conditions reveals marked signal induction in activated microglia. J Neuroinflammation 14: 45
27. Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9: 559
28. Liu X, Yao DL, Bondy CA, Brenner M, Hudson LD, Zhou J, Webster HD (1994) Astrocytes express insulin-like growth factor-I (IGF-I) and its binding protein, IGFBP-2, during demyelination induced by experimental autoimmune encephalomyelitis. Mol Cell Neurosci 5: 418–430
29. Liu JL, Grinberg A, Westphal H, Sauer B, Accili D, Karas M, LeRoith D (1998) Insulin-like growth factor-I affects perinatal lethality and postnatal development in a gene dosage-dependent manner: manipulation using the Cre/loxP system in transgenic mice. Mol Endocrinol 12: 1452–1462
30. Matcovitch-Natan O, Winter DR, Giladi A, Vargas Aguilar S, Spinrad A, Sarrazin S, Ben-Yehuda H, David E, Zelada Gonzalez F, Perrin P, Keren-Shaul H, Gury M, Lara-Astaiso D, Thaiss CA, Cohen M, Bahar Halpern K, Baruch K, Deczkowska A, Lorenzo-Vivas E, Itzkovitz S et al (2016) Microglia development follows a stepwise program to regulate brain homeostasis. Science 353: aad8670
31. McGraw J, McPhail LT, Oschipok LW, Horie H, Poirier F, Steeves JD, Ramer MS, Tetzlaff W (2004) Galectin-1 in regenerating motoneurons. Eur J Neurosci 20: 2872–2880
32. Mizutani M, Pino PA, Saederup N, Charo IF, Ransohoff RM, Cardona AE (2012) The fractalkine receptor but not CCR2 is present on microglia from embryonic development throughout adulthood. J Immunol 188: 29–36
33. de la Monte SM, Wands JR (2005) Review of insulin and insulin-like growth factor expression, signaling, and malfunction in the central nervous system: relevance to Alzheimer's disease. J Alzheimers Dis 7: 45–61
34. Mueller AM, Nassery A, Conlon H, Liu X, Jun E, Yoon BH, Cristofanilli M, Sadiq SA (2013) Effects of intraventricular methotrexate administration on Cuprizone-induced demyelination in mice. Front Mol Neurosci 6: 34
35. Nakashima K, Yanagisawa M, Arakawa H, Taga T (1999) Astrocyte differentiation mediated by LIF in cooperation with BMP2. FEBS Lett 457: 43–46
36. Netchine I, Azzi S, Le Bouc Y, Savage MO (2011) IGF1 molecular anomalies demonstrate its critical role in fetal, postnatal growth and brain development. Best Pract Res Clin Endocrinol Metab 25: 181–190
37. Paolicelli RC, Bolasco G, Pagani F, Maggi L, Scianni M, Panzanelli P, Giustetto M, Ferreira TA, Guiducci E, Dumas L, Ragozzino D, Gross CT (2011) Synaptic pruning by microglia is necessary for normal brain development. Science 333: 1456–1458
38. Prinz M, Priller J (2014) Microglia and brain macrophages in the molecular age: from origin to neuropsychiatric disease. Nat Rev Neurosci 15: 300–312
39. Quinta HR, Pasquini JM, Rabinovich GA, Pasquini LA (2014) Glycan-dependent binding of galectin-1 to neuropilin-1 promotes axonal regeneration after spinal cord injury. Cell Death Differ 21: 941–955
40. Remington LT, Babcock AA, Zehntner SP, Owens T (2007) Microglial recruitment, activation, and proliferation in response to primary demyelination. Am J Pathol 170: 1713–1724
41. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139–140
42. Roussos P, Katsel P, Davis KL, Siever LJ, Haroutunian V (2012) A system-level transcriptomic analysis of schizophrenia using postmortem brain tissue samples. Arch Gen Psychiatry 69: 1205–1213
43. Schafer DP, Lehrman EK, Kautzman AG, Koyama R, Mardinly AR, Yamasaki R, Ransohoff RM, Greenberg ME, Barres BA, Stevens B (2012) Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74: 691–705
44. Schulz C, Gomez Perdiguero E, Chorro L, Szabo-Rogers H, Cagnard N, Kierdorf K, Prinz M, Wu B, Jacobsen SE, Pollard JW, Frampton J, Liu KJ, Geissmann F (2012) A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 336: 86–90
45. Smith ME, Eller NL, McFarland HF, Racke MK, Raine CS (1999) Age dependence of clinical and pathological manifestations of autoimmune demyelination. Implications for multiple sclerosis. Am J Pathol 155: 1147–1161
46. Squarzoni P, Oller G, Hoeffel G, Pont-Lezica L, Rostaing P, Low D, Bessis A, Ginhoux F, Garel S (2014) Microglia modulate wiring of the embryonic forebrain. Cell Rep 8: 1271–1279
47. Starossom SC, Mascanfroni ID, Imitola J, Cao L, Raddassi K, Hernandez SF, Bassil R, Croci DO, Cerliani JP, Delacour D, Wang Y, Elyaman W, Khoury SJ, Rabinovich GA (2012) Galectin-1 deactivates classically activated microglia and protects from inflammation-induced neurodegeneration. Immunity 37: 249–263
48. Stevens B, Allen NJ, Vazquez LE, Howell GR, Christopherson KS, Nouri N, Micheva KD, Mehalow AK, Huberman AD, Stafford B, Sher A, Litke AM, Lambris JD, Smith SJ, John SW, Barres BA (2007) The classical complement cascade mediates CNS synapse elimination. Cell 131: 1164–1178
49. Stranges PB, Watson J, Cooper CJ, Choisy-Rossi CM, Stonebraker AC, Beighton RA, Hartig H, Sundberg JP, Servick S, Kaufmann G, Fink PJ, Chervonsky AV (2007) Elimination of antigen-presenting cells and autoreactive T cells by Fas contributes to prevention of autoimmunity. Immunity 26: 629–641
50. Suh HS, Zhao ML, Derico L, Choi N, Lee SC (2013) Insulin-like growth factor 1 and 2 (IGF1, IGF2) expression in human microglia: differential regulation by inflammatory mediators. J Neuroinflammation 10: 37
51. Takamori Y, Mori T, Wakabayashi T, Nagasaka Y, Matsuzaki T, Yamada H (2009) Nestin-positive microglia in adult rat cerebral cortex. Brain Res 1270: 10–18
52. Ueno M, Fujita Y, Tanaka T, Nakamura Y, Kikuta J, Ishii M, Yamashita T (2013) Layer V cortical neurons require microglial support for survival during postnatal development. Nat Neurosci 16: 543–551
53. Wlodarczyk A, Lobner M, Cedile O, Owens T (2014) Comparison of microglia and infiltrating CD11c(+) cells as antigen presenting cells for T cell proliferation and cytokine response. J Neuroinflammation 11: 57
54. Wlodarczyk A, Cédile O, Jensen KN, Jasson A, Mony JT, Khorooshi R, Owens T (2015) Pathologic and protective roles for microglial subsets and bone marrow- and blood-derived myeloid cells in central nervous system inflammation. Front Immunol 6: 463
55. Ye P, Li L, Richards RG, DiAugustine RP, D'Ercole AJ (2002) Myelination is altered in insulin-like growth factor-I null mutant mice. J Neurosci 22: 6041–6051
56. Yokoyama A, Yang L, Itoh S, Mori K, Tanaka J (2004) Microglia, a potential source of neurons, astrocytes, and oligodendrocytes. Glia 45: 96–104
57. Zhan Y, Paolicelli RC, Sforazzini F, Weinhard L, Bolasco G, Pagani F, Vyssotski AL, Bifone A, Gozzi A, Ragozzino D, Gross CT (2014) Deficient neuron-microglia signaling results in impaired functional brain connectivity and social behavior. Nat Neurosci 17: 400–406