Interleukin-34 restores blood-brain barrier integrity by upregulating tight junction proteins in endothelial cells

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Jin, Shijie ^a   Sonobe, Yoshifumi ^a   Kawanokuchi, Jun ^a   Horiuchi, Hiroshi ^a   Cheng, Yi ^a   Wang, Yue ^a   Mizuno, Tetsuya ^a   Takeuchi, Hideyuki ^a   Suzumura, Akio ^a  

^a NAGOYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CLAUDIN 5; COLONY STIMULATING FACTOR 1 RECEPTOR; COLONY STIMULATING FACTOR RECEPTOR; INTERLEUKIN 34; OCCLUDIN; UNCLASSIFIED DRUG; CYTOKINE; INTERLEUKIN DERIVATIVE; INTERLEUKIN-34, MOUSE; TIGHT JUNCTION PROTEIN;

ANIMAL CELL; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CAPILLARY ENDOTHELIAL CELL; BRAIN NERVE CELL; EMBRYO; MICROGLIA; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SPINAL CORD NERVE CELL; UPREGULATION; ANIMAL; C57BL MOUSE; CAPILLARY PERMEABILITY; CELL CULTURE; ENDOTHELIUM CELL; GENETICS; IMMUNOLOGY; METABOLISM;

ANIMALS; BLOOD-BRAIN BARRIER; CAPILLARY PERMEABILITY; CELLS, CULTURED; CYTOKINES; ENDOTHELIAL CELLS; INTERLEUKINS; MICE; MICE, INBRED C57BL; TIGHT JUNCTION PROTEINS; UP-REGULATION;

EID: 84919740878     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0115981     Document Type: Article

References (35)

1. Lin H, Lee E, Hestir K, Leo C, Huang M, et al. (2008) Discovery of a cytokine and its receptor by functional screening of the extracellular proteome. Science 320: 807-811
2. Chihara T, Suzu S, Hassan R, Chutiwitoonchai N, Hiyoshi M, et al. (2010) IL-34 and M-CSF share the receptor Fms but are not identical in biological activity and signal activation. Cell Death Differ 17: 1917-1927
3. Wang Y, Szretter KJ, Vermi W, Gilfillan S, Rossini C, et al. (2012) IL-34 is a tissue-restricted ligand of CSF1R required for the development of Langerhans cells and microglia. Nat Immunol 13: 753-760
4. Greter M, Lelios I, Pelczar P, Hoeffel G, Price J, et al. (2012) Stroma-derived interleukin-34 controls the development and maintenance of langerhans cells and the maintenance of microglia. Immunity 37: 1050-1060.
5. Nakamichi Y, Mizoguchi T, Arai A, Kobayashi Y, Sato M, et al. (2012) Spleen serves as a reservoir of osteoclast precursors through vitamin D-induced IL-34 expression in osteopetrotic op/op mice. Proc Natl Acad Sci U S A 109: 10006-10011.
6. Mizuno T, Doi Y, Mizoguchi H, Jin S, Noda M, et al. (2011) Interleukin-34 selectively enhances the neuroprotective effects of microglia to attenuate oligomeric amyloid-b neurotoxicity. Am J Pathol 179: 2016-2027.
7. Luo J, Elwood F, Britschgi M, Villeda S, Zhang H, et al. (2013) Colony-stimulating factor 1 receptor (CSF1R) signaling in injured neurons facilitates protection and survival. J Exp Med 210: 157-172.
8. Risau W, Engelhardt B, Wekerle H (1990) Immune function of the blood-brain barrier: incomplete presentation of protein (auto-)antigens by rat brain microvascular endothelium in vitro. J Cell Biol 110: 1757-1766.
9. Abbott NJ, Romero IA (1996) Transporting therapeutics across the blood-brain barrier. Mol Med Today 2: 106-113.
10. Abbott NJ (2002) Astrocyte-endothelial interactions and blood-brain barrier permeability. J Anat 200: 629-638.
11. Begley DJ (2003) Understanding and circumventing the blood-brain barrier. Acta Paediatr Suppl 92: 83-91.
12. Hawkins BT, Davis TP (2005) The blood-brain barrier/neurovascular unit in health and disease. Pharmacol Rev 57: 173-185.
13. Zhong Z, Deane R, Ali Z, Parisi M, Shapovalov Y, et al. (2008) ALS-causing SOD1 mutants generate vascular changes prior to motor neuron degeneration. Nat Neurosci 11: 420-422.
14. Afonso PV, Ozden S, Prevost MC, Schmitt C, Seilhean D, et al. (2007) Human blood-brain barrier disruption by retroviral-infected lymphocytes: role of myosin light chain kinase in endothelial tightjunction disorganization. J Immunol 179: 2576-2583.
15. Fabry Z, Topham DJ, Fee D, Herlein J, Carlino JA, et al. (1995) TGF-beta 2 decreases migration of lymphocytes in vitro and homing of cells into the central nervous system in vivo. J Immunol 155: 325-332.
16. Fö rster C, Burek M, Romero IA, Weksler B, Couraud PO, et al. (2008) Differential effects of hydrocortisone and TNFalpha on tight junction proteins in an in vitro model of the human blood-brain barrier. J Physiol 586: 1937-1949.
17. Kebir H, Kreymborg K, Ifergan I, Dodelet-Devillers A, Cayrol R, et al. (2007) Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nat Med 13: 1173-1175.
18. Minagar A, Alexander JS (2003) Blood-brain barrier disruption in multiple sclerosis. Mult Scler 9: 540-549.
19. Minagar A, Long A, Ma T, Jackson T, Kelley R, et al. (2003) Interferon (IFN)-β1a and IFN-β1b Block IFN-?-Induced Disintegration of Endothelial Junction Integrity and Barrier. Endothelium 10: 299-307.
20. Mizuno T, Zhang G, Takeuchi H, Kawanokuchi J, Wang J, et al. (2008) Interferon-gamma directly induces neurotoxicity through a neuron specific, calcium-permeable complex of IFN-gamma receptor and AMPA GluR1 receptor. FASEB J 22: 1797-1806.
21. Tatsuta T, Naito M, Oh-hara T, Sugawara I, Tsuruo T (1992) Functional involvement of P-glycoprotein in blood-brain barrier. J Biol Chem 267: 20383-20391.
22. Sonobe Y, Takeuchi H, Kataoka K, Li H, Jin S, et al. (2009) Interleukin-25 expressed by brain capillary endothelial cells maintains blood-brain barrier function in a protein kinase Cepsilon-dependent manner. J Biol Chem 284: 31834-31842.
23. Endong L, Shijie J, Sonobe Y, Di M, Hua L, et al. (2011) The gap-junction inhibitor carbenoxolone suppresses the differentiation of Th17 cells through inhibition of IL-23 expression in antigen presenting cells. J Neuroimmunol 240-241: 58-64.
24. Conejo-Garcia JR, Buckanovich RJ, Benencia F, Courreges MC, Rubin SC, et al. (2005) Vascular leukocytes contribute to tumor vascularization. Blood 105: 679-681.
25. Blamire AM, Anthony DC, Rajagopalan B, Sibson NR, Perry VH, et al. (2000) Interleukin-1beta -induced changes in blood-brain barrier permeability, apparent diffusion coefficient, and cerebral blood volume in the rat brain: a magnetic resonance study. J Neurosci 20: 8153-8159.
26. Ransohoff RM, Brown MA (2012) Innate immunity in the central nervous system. J Clin Invest 122: 1164-1171.
27. Boström EA, Lundberg P (2013) The Newly Discovered Cytokine IL-34 Is Expressed in Gingival Fibroblasts, Shows Enhanced Expression by Pro-Inflammatory Cytokines, and Stimulates Osteoclast Differentiation. PloS one 8: e81665.
28. Wang Y, Colonna M (2014) Interkeukin-34, a cytokine crucial for the differentiation and maintenance of tissue resident macrophages and Langerhans cells. European journal of immunology.
29. Ma D, Doi Y, Jin S, Li E, Sonobe Y, et al. (2012) TGF-b induced by interleukin-34-stimulated microglia regulates microglial proliferation and attenuates oligomeric amyloid b neurotoxicity. Neuroscience letters 529: 86-91.
30. Nandi S, Gokhan S, Dai X-M, Wei S, Enikolopov G, et al. (2012) The CSF-1 receptor ligands IL-34 and CSF-1 exhibit distinct developmental brain expression patterns and regulate neural progenitor cell maintenance and maturation. Developmental biology 367: 100-113.
31. Mitrasinovic OM, Grattan A, Robinson CC, Lapustea NB, Poon C, et al. (2005) Microglia overexpressing the macrophage colony-stimulating factor receptor are neuroprotective in a microglialhippocampal organotypic coculture system. The Journal of neuroscience 25: 4442-4451.
32. Hao C, Guilbert L, Fedoroff S (1990) Production of colony-stimulating factor-1 (CSF-1) by mouse astroglia in vitro. Journal of neuroscience research 27: 314-323.
33. Kook S-Y, Hong HS, Moon M, Mook-Jung I (2013) Disruption of blood-brain barrier in Alzheimer disease pathogenesis. Tissue Barriers 1: e23993.
34. Zhong Y, Zhang B, Eum SY, Toborek M (2012) HIV-1 Tat triggers nuclear localization of ZO-1 via Rho signaling and cAMP response element-binding protein activation. J Neurosci 32: 143-150.
35. Tureci O, Koslowski M, Helftenbein G, Castle J, Rohde C, et al. (2011) Claudin-18 gene structure, regulation, and expression is evolutionary conserved in mammals. Gene 481: 83-92.