CXCL5 signaling is a shared pathway of neuroinflammation and blood-brain barrier injury contributing to white matter injury in the immature brain

Journal of Neuroinflammation

Volumn 13, Issue 1, 2016, Pages

  Wang, Lin Yu ^a,b   Tu, Yi Fang ^c,d   Lin, Yung Chieh ^c,d   Huang, Chao Ching ^c,e,f  

^a CHI MEI MEDICAL CENTER   (Taiwan)

^b CHIA NAN UNIVERSITY OF PHARMACY AND SCIENCE   (Taiwan)

^c NATIONAL CHENG KUNG UNIVERSITY HOSPITAL   (Taiwan)

^d NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^e TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^f TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Blood brain barrier; CXCL5; CXCR2; Hypoxic ischemia; Immature brain; Lipopolysaccharide; Neuroinflammation; Preterm infant; White matter injury

Indexed keywords

1 (2 BROMOPHENYL) 3 (2 HYDROXY 4 NITROPHENYL)UREA; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; GLIAL FIBRILLARY ACIDIC PROTEIN; MYELIN BASIC PROTEIN; CHEMOKINE RECEPTOR CXCR2; ECTODYSPLASIN A; GRANULOCYTE COLONY STIMULATING FACTOR; HYBRID PROTEIN; INTERLEUKIN 3; LIPOPOLYSACCHARIDE; MYELOPOIETIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; BLOOD BRAIN BARRIER INJURY; BRAIN INJURY; CONTROLLED STUDY; DRUG EFFECT; ENDOTHELIUM CELL; HYPOXIC ISCHEMIC ENCEPHALOPATHY; MICROGLIA; MYELINATION; NERVOUS SYSTEM INFLAMMATION; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SIGNAL TRANSDUCTION; UPREGULATION; WHITE MATTER INJURY; ANIMAL; BLOOD BRAIN BARRIER; BRAIN; CHEMICALLY INDUCED; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; ENCEPHALITIS; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; INJURIES; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; LEUKOENCEPHALOPATHIES; METABOLISM; NEWBORN; PATHOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TIME FACTOR;

ANIMALS; ANIMALS, NEWBORN; BLOOD-BRAIN BARRIER; BRAIN; CHEMOKINE CXCL5; DISEASE MODELS, ANIMAL; ECTODYSPLASINS; ENCEPHALITIS; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL FIBRILLARY ACIDIC PROTEIN; GRANULOCYTE COLONY-STIMULATING FACTOR; INJECTIONS, INTRAVENTRICULAR; INTERLEUKIN-3; LEUKOENCEPHALOPATHIES; LIPOPOLYSACCHARIDES; MICROGLIA; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, INTERLEUKIN-8B; RECOMBINANT FUSION PROTEINS; TIME FACTORS;

EID: 84953241498     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-015-0474-6     Document Type: Article

References (43)

1. Raines EW, Ferri N. Thematic review series: the immune system and atherogenesis. Cytokines affecting endothelial and smooth muscle cells in vascular disease. J Lipid Res. 2005;46:1081-92.
2. Charo IF, Ransohoff RM. The many roles of chemokines and chemokine receptors in inflammation. New Engl J Med. 2006;354:610-21.
3. Sepuru KM, Poluri KM, Rajarathnam K. Solution structure of CXCL5-a novel chemokine and adipokine implicated in inflammation and obesity. PLoS One. 2014;9:e93228.
4. Walz A, Schmutz P, Mueller C, Schnyder-Candrian S. Regulation and function of the CXC chemokine ENA-78 in monocytes and its role in disease. J Leukoc Biol. 1997;62:604-11.
5. Rovai LE, Herschman HR, Smith JB. The murine neutrophil-chemoattractant chemokines LIX, KC, and MIP-2 have distinct induction kinetics, tissue distributions, and tissue-specific sensitivities to glucocorticoid regulation in endotoxemia. J Leukoc Biol. 1998;64:494-502.
6. Chandrasekar B, Melby PC, Sarau HM, Raveendran M, Perla RP, Marelli-Berg FM, et al. Chemokine-cytokine cross-talk. The ELR+ CXC chemokine LIX (CXCL5) amplifies a proinflammatory cytokine response via a phosphatidylinositol 3-kinase-NF-kappa B pathway. J Biol Chem. 2003;278:4675-86.
7. Volpe JJ. Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol. 2009;8:110-24.
8. Kadhim H, Tabarki B, Verellen G, De Prez C, Rona AM, Sebire G. Inflammatory cytokines in the pathogenesis of periventricular leukomalacia. Neurology. 2001;56:1278-84.
9. Dammann O, Durums S, Leviton A. Do white cells matter in white matter damage? Trends Neurosci. 2001;24:320-4.
10. Volpe JJ. Systemic inflammation, oligodendroglial maturation and encephalopathy of prematurity. Ann Neurol. 2011;70:525-9.
11. Keelan JA, Yang J, Romero RJ, Chaiworapongsa T, Marvin KW, Sato TA, et al. Epithelial cell-derived neutrophil-activating peptide-78 is present in fetal membranes and amniotic fluid at increased concentrations with intra-amniotic infection and preterm delivery. Biol Reprod. 2004;70:253-9.
12. Deng LZ, Shi CH, Huang YM. Study on relations between the dynamic changes of serum HMGB1, ENA-78 levels and hypoxic-ischemic encephalopathy. Chin J Clinicians. 2010;4:1840-3.
13. Stichel H, Bäckström E, Hafström O, Nilsson S, Lappalainen U, Bry K. Inflammatory cytokines in gastric fluid at birth and the development of bronchopulmonary dysplasia. Acta Paediatr. 2011;100:1206-12.
14. MohanKumar K, Kaza N, Jagadeeswaran R, Garzon SA, Bansal A, Kurundkar AR, et al. Gut mucosal injury in neonates is marked by macrophage infiltration in contrast to pleomorphic infiltrates in adult: evidence from an animal model. Am J Physiol Gastrointest Liver Physiol. 2012;303:G93-102.
15. Back SA, Miller SP. Brain injury in premature neonates: a primary cerebral dysmaturation disorder? Ann Neurol. 2014;75:469-86.
16. Craig A, Luo NL, Beardsley DJ, Wingate-Pearse N, Walker DW, Hohimer AR, et al. Quantitative analysis of perinatal rodent oligodendrocyte lineage progression and its correlation with human. Exp Neurol. 2003;181:231-40.
17. Wang LW, Lin YC, Wang ST, Yeh TF, Huang CC. Hypoxic/ischemic and infectious events have cumulative effects on the risk of cerebral palsy in very-low-birth-weight preterm infants. Neonatology. 2014;106:209-15.
18. Wang LW, Tu YF, Huang CC, Ho CJ. JNK signaling is the shared pathway linking neuroinflammation, blood-brain barrier disruption, and oligodendroglial apoptosis in the white matter injury of the immature brain. J Neuroinflammation. 2012;9:175.
19. Viola A, Luster AD. Chemokines and their receptors: drug targets in immunity and inflammation. Annu Rev Pharmacol Toxicol. 2008;48:171-97.
20. Bento AF, Leite DF, Claudino RF, Hara DB, Leal PC, Calixto JB. The selective nonpeptide CXCR2 antagonist SB225002 ameliorates acute experimental colitis in mice. J Leukoc Biol. 2008;84:1213-21.
21. Lee HT, Chang YC, Tu YF, Huang CC. VEGF-A/VEGFR-2 signaling leading to CREB phosphorylation is a shared pathway underlying the protective effect of preconditioning on neurons and endothelial cells. J Neurosci. 2009;29:4356-68.
22. Paxions G, Watson C. The rat brain in stereotaxic coordinates. 6th ed. Amsterdam: Elsevier; 2007.
23. Wang LW, Chang YC, Chen SJ, Tseng CH, Liao NS, Huang CC, et al. TNFR1-JNK signaling is the shared pathway of neuroinflammation and neurovascular damage after LPS-sensitized hypoxic-ischemic injury in the immature brain. J Neuroinflammation. 2014;11:215.
24. Hung PL, Huang CC, Tu DG, Huang HM, Chang YC. Thyroxin treatment protects against white matter injury in the immature brain via brain-derived neurotrophic factor. Stroke. 2013;44:2275-83.
25. Svedin P, Hagberg H, Savman K, Zhu C, Mallard C. Matrix metalloproteinase-9 gene knock-out protects the immature brain after cerebral hypoxia-ischemia. J Neurosci. 2007;27:1511-8.
26. Muramatsu K, Fukuda A, Togari H, Wada Y, Nishino H. Vulnerability to cerebral hypoxic-ischemic insult in neonatal but not in adult rats is in parallel with disruption of the blood-brain barrier. Stroke. 1997;28:2281-8.
27. Wang LW, Chang YC, Lin CY, Wang ST, Hong JS, Huang CC. Low-dose lipopolysaccharide selectively sensitizes hypoxic-ischemia-induced white matter injury in the immature brain. Pediatr Res. 2010;68:41-7.
28. Chew LJ, Takanohashi A, Bell M. Microglia and inflammation: impact on developmental brain injuries. Ment Retard Dev Disabil Res Rev. 2006;12:105-12.
29. Hagberg H, Mallard C, Ferriero DM, Vannucci SJ, Levison SW, Vexler ZS, et al. The role of inflammation in perinatal brain injury. Nat Rev Neurol. 2015;11:192-208.
30. Moretti R, Pansiot J, Bettati D, Strazielle N, Ghersi-Egea JF, Damante G, et al. Blood-brain barrier dysfunction in disorders of the developing brain. Front Neurosci. 2015;9:40.
31. Beck GC, Yard BA, Breedijk AJ, Van Ackern K, Van Der Woude FJ. Release of CXC-chemokines by human lung microvascular endothelial cells (LMVEC) compared with macrovascular umbilical vein endothelial cells. Clin Exp Immunol. 1999;118:298-303.
32. Koch AE, Kunkel SL, Harlow LA, Mazarakis DD, Haines GK. Epithelial neutrophil activating peptide-78: a novel chemotactic cytokine for neutrophils in arthritis. J Clin Invest. 1994;94:1012-8.
33. Shin JH, Park YM, Kim DH, Moon GJ, Bang OY, Ohn T, et al. Ischemic brain extract increases SDF-1 expression in astrocytes through the CXCR2/miR-223/miR-27b pathway. Biochim Biophys Acta. 1839;2014:826-36.
34. Veenstra M, Ransohoff RM. Chemokine receptor CXCR2: physiology regulator and neuroinflammation controller? J Neuroimmunol. 2012;246:1-9.
35. Liu L, Darnall L, Hu T, Choi K, Lane TE, Ransohoff RM. Myelin repair is accelerated by inactivating CXCR2 on nonhematopoietic cells. J Neurosci. 2010;30:9074-83.
36. Lue H, Dewor M, Leng L, Bucala R, Bernhagen J. Activation of the JNK signalling pathway by macrophage migration inhibitory factor (MIF) and dependence on CXCR4 and CD74. Cell Signal. 2011;23:135-44.
37. Balamayooran G, Batra S, Cai S, Mei J, Worthen GS, Penn AL, et al. Role of CXCL5 in leukocyte recruitment to the lungs during secondhand smoke exposure. Am J Respir Cell Mol Biol. 2012;47:104-11.
38. Filipovic R, Jakovcevski I, Zecevic N. GRO-alpha and CXCR2 in the human fetal brain and multiple sclerosis lesions. Dev Neurosci. 2003;25:279-90.
39. Remmers M, Schmidt-Kastner R, Belayev L, Lin B, Busto R, Ginsberg MD. Protein extravasation and cellular uptake after high-dose human-albumin treatment of transient focal cerebral ischemia in rats. Brain Res. 1999;827:237-42.
40. Simard JM, Geng Z, Woo SK, Ivanova S, Tosun C, Melnichenko L, et al. Glibenclamide reduces inflammation, vasogenic edema, and caspase-3 activation after subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2009;29:317-30.
41. Del Bigio MR, Deck JHN, Davidson GS. Glial swelling with eosinophilia in human post-mortem brains: a change indicative of plasma extravasation. Acta Neuropathol. 2000;100:688-94.
42. Jensen MB, Finsen B, Zimmer J. Morphological and immunophenotypic microglial changes in the denervated fascia dentata of adult rats: correlation with blood-brain barrier damage and astroglial reactions. Exp Neurol. 1997;143:103-16.
43. Jorgensen MB, Finsen BR, Jensen MB, Castellano B, Diemer NH, Zimmer J. Microglial and astroglial reactions to ischemic and kainic acid-induced lesions of the adult rat hippocampus. Exp Neurol. 1993;120:70-88.