IL-1β induces hypomyelination in the periventricular white matter through inhibition of oligodendrocyte progenitor cell maturation via FYN/MEK/ERK signaling pathway in septic neonatal rats

GLIA

Volumn 64, Issue 4, 2016, Pages 583-602

  Xie, Di ^a   Shen, Fengcai ^a,b   He, Shaoru ^a   Chen, Mengmeng ^a,b   Han, Qianpeng ^a   Fang, Ming ^a   Zeng, Hongke ^a   Chen, Chunbo ^a   Deng, Yiyu ^a  

^a GUANGDONG PROVINCIAL PEOPLE'S HOSPITAL   (China)

^b SHANTOU UNIVERSITY MEDICAL COLLEGE   (China)

Author keywords

FYN MEK ERK signaling pathway; IL 1 ; Microglia; PWMD; Sepsis

Indexed keywords

2',3' CYCLIC NUCLEOTIDE 3' PHOSPHODIESTERASE; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MYELIN BASIC PROTEIN; PROTEIN KINASE FYN; IL1B PROTEIN, RAT; IL1R1 PROTEIN, RAT; INTERLEUKIN 1 RECEPTOR TYPE I;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; ELECTRON MICROSCOPY; GENE EXPRESSION; HYPOMYELINATION; INHIBITION KINETICS; MICROGLIA; MYELIN SHEATH; MYELINATION; NERVE FIBER; NONHUMAN; OLIGODENDROGLIA; PERIVENTRICULAR WHITE MATTER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SEPSIS; SIGNAL TRANSDUCTION; UPREGULATION; WHITE MATTER; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN; CELL CULTURE; DISEASE MODEL; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEWBORN; PATHOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; ULTRASTRUCTURE;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; BRAIN; CELL PROLIFERATION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; MAP KINASE SIGNALING SYSTEM; MYELIN SHEATH; NEURAL STEM CELLS; NEUROGENESIS; OLIGODENDROGLIA; RATS, SPRAGUE-DAWLEY; RECEPTORS, INTERLEUKIN-1 TYPE I; SEPSIS; WHITE MATTER;

EID: 84958777007     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22950     Document Type: Article

References (53)

1. Ahlin K, Himmelmann K, Hagberg G, Kacerovsky M, Cobo T, Wennerholm UB, Jacobsson B. 2013. Cerebral palsy and perinatal infection in children born at term. Obstet Gynecol 122:41-49.
2. Alshaikh B, Yusuf K, Sauve R. 2013. Neurodevelopmental outcomes of very low birth weight infants with neonatal sepsis: Systematic review and meta-analysis. J Perinatol 33:558-564.
3. Baer AS, Syed YA, Kang SU, Mitteregger D, Vig R, Ffrench-Constant C, Franklin RJ, Altmann F, Lubec G, Kotter MR. 2009. Myelin-mediated inhibition of oligodendrocyte precursor differentiation can be overcome by pharmacological modulation of Fyn-RhoA and protein kinase C signalling. Brain 132:465-481.
4. Cai Z, Pang Y, Lin S, Rhodes PG. 2003. Differential roles of tumor necrosis factor-alpha and interleukin-1 beta in lipopolysaccharide-induced brain injury in the neonatal rat. Brain Res 975:37-47.
5. Cammer W. 2000. Effects of TNFalpha on immature and mature oligodendrocytes and their progenitors in vitro. Brain Res 864:213-219.
6. Cayre M, Courtès S, Martineau F, Giordano M, Arnaud K, Zamaron A, Durbec P. 2013. Netrin 1 contributes to vascular remodeling in the subventricular zone and promotes progenitor emigration after demyelination. Development 140:3107-3117.
7. Chew LJ, Coley W, Cheng Y, Gallo V. 2010. Mechanisms of regulation of oligodendrocyte development by p38 mitogen-activated protein kinase. J Neurosci 30:11011-11027.
8. Choi EK, Park D, Kim TK, Lee SH, Bae DK, Yang G, Yang YH, Kyung J, Kim D, Lee WR, Suh JG, Jeong ES, Kim SU, Kim YB. 2011. Animal models of periventricular leukomalacia. Lab Anim Res 27:77-84.
9. Colognato H, Ramachandrappa S, Olsen IM, ffrench-Constant C. 2004. Integrins direct Src family kinases to regulate distinct phases of oligodendrocyte development. J Cell Biol 167:365-375.
10. Czeh M, Gressens P, Kaindl AM. 2011. The yin and yang of microglia. Dev Neurosci 33:199-209.
11. Dammann O, Hagberg H, Leviton A. 2001. Is periventricular leukomalacia an axonopathy as well as an oligopathy? Pediatr Res 49:453-457.
12. Dammann O, Leviton A. 1997. Maternal intrauterine infection, cytokines, and brain damage in the preterm newborn. Pediatr Res 42:1-8.
13. Deng YY, Lu J, Ling EA, Kaur C. 2009. Monocyte chemoattractant protein-1 (MCP-1) produced via NF-kappaB signaling pathway mediates migration of amoeboid microglia in the periventricular white matter in hypoxic neonatal rats. Glia 57:604-621.
14. Deng YY, Lu J, Ling EA, Kaur C. 2010. Microglia-derived macrophage colony stimulating factor promotes generation of proinflammatory cytokines by astrocytes in the periventricular white matter in the hypoxic neonatal brain. Brain Pathol 20:909-925.
15. Deng Y, Lu J, Sivakumar V, Ling EA, Kaur C. 2008. Amoeboid microglia in the periventricular white matter induce oligodendrocyte damage through expression of proinflammatory cytokines via MAP kinase signaling pathway in hypoxic neonatal rats. Brain Pathol 18:387-400.
16. El Waly B, Macchi M, Cayre M, Durbec P. 2014. Oligodendrogenesis in the normal and pathological central nervous system. Front Neurosci 8:145.
17. Fancy SP, Baranzini SE, Zhao C, Yuk DI, Irvine KA, Kaing S, Sanai N, Franklin RJ, Rowitch DH. 2009. Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNS. Genes Dev 23:1571-1585.
18. Fancy SP, Zhao C, Franklin RJ. 2004. Increased expression of Nkx2.2 and Olig2 identifies reactive oligodendrocyte progenitor cells responding to demyelination in the adult CNS. Mol Cell Neurosci 27:247-254.
19. Favrais G, van de Looij Y, Fleiss B, Ramanantsoa N, Bonnin P, Stoltenburg-Didinger G, Lacaud A, Saliba E, Dammann O, Gallego J, Sizonenko S, Hagberg H, Lelièvre V, Gressens P. 2011. Systemic inflammation disrupts the developmental program of white matter. Ann Neurol 70:550-565.
20. Fyffe-Maricich SL, Karlo JC, Landreth GE, Miller RH. 2011. The ERK2 mitogen-activated protein kinase regulates the timing of oligodendrocyte differentiation. J Neurosci 31:843-850.
21. Galvin J, Eyermann C, Colognato H. 2010. Dystroglycan modulates the ability of insulin-like growth factor-1 to promote oligodendrocyte differentiation. J Neurosci Res 88:3295-3307.
22. Grehan S, Uhlar CM, Sim RB, Herbert J, Whitehead AS. 1997. Expression of a biologically active recombinant mouse IL-1 receptor antagonist and its use in vivo to modulate aspects of the acute phase response. J Immunol 159:369-378.
23. Haynes RL, Folkerth RD, Keefe RJ, Sung I, Swzeda LI, Rosenberg PA, Volpe JJ, Kinney HC. 2003. Nitrosative and oxidative injury to premyelinating oligodendrocytes in periventricular leukomalacia. J Neuropathol Exp Neurol. 62:441-450.
24. He LF, Chen HJ, Qian LH, Chen GY, Buzby JS. 2010. Curcumin protects pre-oligodendrocytes from activated microglia in vitro and in vivo. Brain Res 1339:60-69.
25. Hirayama A, Okoshi Y, Hachiya Y, Ozawa Y, Ito M, Kida Y, Imai Y, Kohsaka S, Takashima S. 2001. Early immunohistochemical detection of axonal damage and glial activation in extremely immature brains with periventricular leukomalacia. Clin Neuropathol 20:87-91.
26. Hristova M, Cuthill D, Zbarsky V, Acosta-Saltos A, Wallace A, Blight K, Buckley SM, Peebles D, Heuer H, Waddington SN, Raivich G. 2010. Activation and deactivation of periventricular white matter phagocytes during postnatal mouse development. Glia 58:11-28.
27. Kadhim H, Tabarki B, Verellen G, De Prez C, Rona AM, Sébire G. 2001. Inflammatory cytokines in the pathogenesis of periventricular leukomalacia. Neurology 56:1278-1284.
28. Kinney HC, Back SA. 1998. Human oligodendroglial development: Relationship to periventricular leukomalacia. Semin Pediatr Neurol 5:180-189.
29. Krämer EM, Klein C, Koch T, Boytinck M, Trotter J. 1999. Compartmentation of Fyn kinase with glycosylphosphatidylinositol-anchored molecules in oligodendrocytes facilitates kinase activation during myelination. J Biol Chem 274:29042-29049.
30. Kuypers E, Ophelders D, Jellema RK, Kunzmann S, Gavilanes AW, Kramer BW. 2012. White matter injury following fetal inflammatory response syndrome induced by chorioamnionitis and fetal sepsis: Lessons from experimental ovine models. Early Hum Dev 88:931-936.
31. Leviton A, Paneth N, Reuss ML, Susser M, Allred EN, Dammann O, Kuban K, Van Marter LJ, Pagano M, Hegyi T, Hiatt M, Sanocka U, Shahrivar F, Abiri M, Disalvo D, Doubilet P, Kairam R, Kazam E, Kirpekar M, Rosenfeld D, Schonfeld S, Share J, Collins M, Genest D, Shen-Schwarz S. 1999. Maternal infection, fetal inflammatory response, and brain damage in very low birth weight infants. Developmental Epidemiology Network Investigators. Pediatr Res 46:566-575.
32. Liu Z, Hu X, Cai J, Liu B, Peng X, Wegner M, Qiu M. 2007. Induction of oligodendrocyte differentiation by Olig2 and Sox10: Evidence for reciprocal interactions and dosage-dependent mechanisms. Dev Biol 302:683-693.
33. Malaeb S, Dammann O. 2009. Fetal inflammatory response and brain injury in the preterm newborn. J Child Neurol 24:1119-1126.
34. Menn B, Garcia-Verdugo JM, Yaschine C, Gonzalez-Perez O, Rowitch D, Alvarez-Buylla A. 2006. Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci 26:7907-7918.
35. Murugan M, Sivakumar V, Lu J, Ling EA, Kaur C. 2011. Expression of N-methyl D-aspartate receptor subunits in amoeboid microglia mediates production of nitric oxide via NF-κB signaling pathway and oligodendrocyte cell death in hypoxic postnatal rats. Glia 59:521-39.
36. Nishiyama A, Chang A, Trapp BD. 1999. NG2+ glial cells: A novel glial cell population in the adult brain. J Neuropathol Exp Neurol 58:1113-1124.
37. Osterhout DJ, Wolven A, Wolf RM, Resh MD, Chao MV. 1999. Morphological differentiation of oligodendrocytes requires activation of Fyn tyrosine kinase. J Cell Biol 145:1209-1218.
38. Pang Y, Cai Z, Rhodes PG. 2003. Disturbance of oligodendrocyte development, hypomyelination and white matter injury in the neonatal rat brain after intracerebral injection of lipopolysaccharide. Brain Res Dev Brain Res 140:205-214.
39. Pang Y, Rodts-Palenik S, Cai Z, Bennett WA, Rhodes PG. 2005. Suppression of glial activation is involved in the protection of IL-10 on maternal E. coli induced neonatal white matter injury. Brain Res Dev Brain Res 157:141-149.
40. Pérez MJ, Fernandez N, Pasquini JM. 2013. Oligodendrocyte differentiation and signaling after transferrin internalization: A mechanism of action. Exp Neurol 248:262-274.
41. Procianoy RS, Silveira RC. 2012. Association between high cytokine levels with white matter injury in preterm infants with sepsis. Pediatr Crit Care Med 13:183-187.
42. Rousset CI, Chalon S, Cantagrel S, Bodard S, Andres C, Gressens P, Saliba E. 2006. Maternal exposure to LPS induces hypomyelination in the internal capsule and programmed cell death in the deep gray matter in newborn rats. Pediatr Res 59:428-433.
43. Silveira RC, Procianoy RS, Dill JC, da Costa CS. 2008. Periventricular leukomalacia in very low birth weight preterm neonates with high risk for neonatal sepsis. J Pediatr (Rio J) 84:211-216.
44. Skranes JS, Nilsen G, Smevik O, Vik T, Brubakk AM. 1998. Cerebral MRI of very low birth weight children at 6 years of age compared with the findings at 1 year. Pediatr Radiol 28:471-475.
45. Vela JM, Molina-Holgado E, Arévalo-Martín A, Almazán G, Guaza C. 2002. Interleukin-1 regulates proliferation and differentiation of oligodendrocyte progenitor cells. Mol Cell Neurosci 20:489-502.
46. Volpe JJ. 2008. Postnatal sepsis, necrotizing entercolitis, and the critical role of systemic inflammation in white matter injury in premature infants. J Pediatr 153:160-163.
47. Wang X, Rousset CI, Hagberg H, Mallard C. 2006. Lipopolysaccharide-induced inflammation and perinatal brain injury. Semin Fetal Neonatal Med 11:343-353.
48. Xiao L, Guo D, Hu C, Shen W, Shan L, Li C, Liu X, Yang W, Zhang W, He C. 2012. Diosgenin promotes oligodendrocyte progenitor cell differentiation through estrogen receptor-mediated ERK1/2 activation to accelerate remyelination. Glia 60:1037-1052.
49. Xin M, Yue T, Ma Z, Wu FF, Gow A, Lu QR. 2005. Myelinogenesis and axonal recognition by oligodendrocytes in brain are uncoupled in Olig1-null mice. J Neurosci 25:1354-1365.
50. Ye F, Chen Y, Hoang T, Montgomery RL, Zhao XH, Bu H, Hu T, Taketo MM, van Es JH, Clevers H, Hsieh J, Bassel-Duby R, Olson EN, Lu QR. 2009. HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the beta-catenin-TCF interaction. Nat Neurosci 12:829-838.
51. Yoon BH, Park CW, Chaiworapongsa T. 2003. Intrauterine infection and the development of cerebral palsy. Bjog 110:124-127.
52. Younes-Rapozo V, Felgueiras LO, Viana NL, Fierro IM, Barja-Fidalgo C, Manhães AC, Barradas PC. 2009. A role for the MAPK/ERK pathway in oligodendroglial differentiation in vitro: stage specific effects on cell branching. Int J Dev Neurosci 27:757-768.
53. Zhou Q, Choi G, Anderson DJ. 2001. The bHLH transcription factor Olig2 promotes oligodendrocyte differentiation in collaboration with Nkx2.2. Neuron 31:791-807.