TLR2-mediated leukocyte trafficking to the developing brain

Journal of Leukocyte Biology

Volumn 101, Issue 1, 2017, Pages 297-305

  Mottahedin, Amin ^a   Smith, Peter Lawrence Phillip ^a   Hagberg, Henrik ^b,c   Ek, C Joakim ^a   Mallard, Carina ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c ST THOMAS HOSPITAL   (United Kingdom)

Author keywords

BBB; BCSFB; Inflammation; Meningitis; PAM3CSK4; Pleocytosis

Indexed keywords

CHEMOKINE; LIPOPOLYSACCHARIDE; MYELOID DIFFERENTIATION FACTOR 88; SUCROSE; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 6; TOLL LIKE RECEPTOR AGONIST; CYTOKINE; LIPOPEPTIDE; PAM(3)CSK(4) PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD CEREBROSPINAL FLUID BARRIER; BRAIN; BRAIN DEVELOPMENT; CELL INFILTRATION; CEREBROSPINAL FLUID; CHOROID PLEXUS; CONTROLLED STUDY; CYTOKINE RESPONSE; ENCEPHALITIS; FLOW CYTOMETRY; IMMUNOCOMPETENT CELL; LEUKOCYTE MIGRATION; MEDIAN EMINENCE; MONOCYTE; MOUSE; NEUTROPHIL; NEWBORN; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; SUBARACHNOID SPACE; AGONISTS; ANIMAL; BLOOD BRAIN BARRIER; C57BL MOUSE; CELL MOTION; CYTOLOGY; DRUG EFFECTS; EMBRYOLOGY; INFLAMMATION; LEUKOCYTE; METABOLISM; PATHOLOGY; PERMEABILITY;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; CELL MOVEMENT; CEREBROSPINAL FLUID; CYTOKINES; INFLAMMATION; LEUKOCYTES; LIPOPEPTIDES; LIPOPOLYSACCHARIDES; MICE, INBRED C57BL; MONOCYTES; MYELOID DIFFERENTIATION FACTOR 88; PERMEABILITY; SUCROSE; TOLL-LIKE RECEPTOR 1; TOLL-LIKE RECEPTOR 2;

EID: 85008502078     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.3A1215-568R     Document Type: Article

References (39)

1. Grether, J. K., Nelson, K. B. (1997) Maternal infection and cerebral palsy in infants of normal birth weight. JAMA 278, 207-211.
2. Strunk, T., Inder, T., Wang, X., Burgner, D., Mallard, C., Levy, O. (2014) Infection-induced inflammation and cerebral injury in preterm infants. Lancet Infect. Dis. 14, 751-762.
3. Sävman, K., Blennow, M., Gustafson, K., Tarkowski, E., Hagberg, H. (1998) Cytokine response in cerebrospinal fluid after birth asphyxia. Pediatr. Res. 43, 746-751.
4. Hagberg, H., Mallard, C., Ferriero, D. M., Vannucci, S. J., Levison, S. W., Vexler, Z. S., Gressens, P. (2015) The role of inflammation in perinatal brain injury. Nat. Rev. Neurol. 11, 192-208.
5. Shechter, R., London, A., Schwartz, M. (2013) Orchestrated leukocyte recruitment to immune-privileged sites: absolute barriers versus educational gates. Nat. Rev. Immunol. 13, 206-218.
6. Johansson, P. A., Dziegielewska, K. M., Liddelow, S. A., Saunders, N. R. (2008) The blood-CSF barrier explained: when development is not immaturity. BioEssays 30, 237-248.
7. Ek, C. J., Dziegielewska, K. M., Habgood, M. D., Saunders, N. R. (2012) Barriers in the developing brain and neurotoxicology. Neurotoxicology 33, 586-604.
8. Ek, C. J., D’Angelo, B., Baburamani, A. A., Lehner, C., Leverin, A. L., Smith, P. L., Nilsson, H., Svedin, P., Hagberg, H., Mallard, C. (2015) Brain barrier properties and cerebral blood flow in neonatal mice exposed to cerebral hypoxia-ischemia. J. Cereb. Blood Flow Metab. 35, 818-827.
9. Rosenberg, G. A. (2012) Neurological diseases in relation to the bloodbrain barrier. J. Cereb. Blood Flow Metab. 32, 1139-1151.
10. Akira, S., Uematsu, S., Takeuchi, O. (2006) Pathogen recognition and innate immunity. Cell 124, 783-801.
11. Eklind, S., Mallard, C., Leverin, A.-L., Gilland, E., Blomgren, K., Mattsby-Baltzer, I., Hagberg, H. (2001) Bacterial endotoxin sensitizes the immature brain to hypoxic-ischaemic injury. Eur. J. Neurosci. 13, 1101-1106.
12. Stridh, L., Mottahedin, A., Johansson, M. E., Valdez, R. C., Northington, F., Wang, X., Mallard, C. (2013) Toll-like receptor-3 activation increases the vulnerability of the neonatal brain to hypoxia-ischemia. J. Neurosci. 33, 12041-12051.
13. Stridh, L., Smith, P. L., Naylor, A. S., Wang, X., Mallard, C. (2011) Regulation of toll-like receptor 1 and-2 in neonatal mice brains after hypoxia-ischemia. J. Neuroinflammation 8, 45.
14. Du, X., Fleiss, B., Li, H., D’angelo, B., Sun, Y., Zhu, C., Hagberg, H., Levy, O., Mallard, C., Wang, X. (2011) Systemic stimulation of TLR2 impairs neonatal mouse brain development. PLoS One 6, e19583.
15. Hoffmann, O., Braun, J. S., Becker, D., Halle, A., Freyer, D., Dagand, E., Lehnardt, S., Weber, J. R. (2007) TLR2 mediates neuroinflammation and neuronal damage. J. Immunol. 178, 6476-6481.
16. Stridh, L., Ek, C. J., Wang, X., Nilsson, H., Mallard, C. (2013) Regulation of Toll-like receptors in the choroid plexus in the immature brain after systemic inflammatory stimuli. Transl. Stroke Res. 4, 220-227.
17. Hübschle, T., Mütze, J., Mühlradt, P. F., Korte, S., Gerstberger, R., Roth, J. (2006) Pyrexia, anorexia, adipsia, and depressed motor activity in rats during systemic inflammation induced by the Toll-like receptors-2 and-6 agonists MALP-2 and FSL-1. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290, R180-R187.
18. Roussarie, J. P., Ruffié, C., Brahic, M. (2007) The role of myelin in Theiler’s virus persistence in the central nervous system. PLoS Pathog. 3, e23.
19. Rose, S., Misharin, A., Perlman, H. (2012) A novel Ly6C/Ly6G-based strategy to analyze the mouse splenic myeloid compartment. Cytometry A 81, 343-350.
20. Denker, S. P., Ji, S., Dingman, A., Lee, S. Y., Derugin, N., Wendland, M. F., Vexler, Z. S. (2007) Macrophages are comprised of resident brain microglia not infiltrating peripheral monocytes acutely after neonatal stroke. J. Neurochem. 100, 893-904.
21. Faust, N., Varas, F., Kelly, L. M., Heck, S., Graf, T. (2000) Insertion of enhanced green fluorescent protein into the lysozyme gene creates mice with green fluorescent granulocytes and macrophages. Blood 96, 719-726.
22. van de Beek, D., de Gans, J., Tunkel, A. R., Wijdicks, E. F. M. (2006) Community-acquired bacterial meningitis in adults. N. Engl. J. Med. 354, 44-53.
23. Kim, K. S. (2010) Acute bacterial meningitis in infants and children. Lancet Infect. Dis. 10, 32-42.
24. Kułak, W., Okurowska-Zawada, B., Sienkiewicz, D., Paszko-Patej, G., Krajewska-Kułak, E. (2010) Risk factors for cerebral palsy in term birth infants. Adv. Med. Sci. 55, 216-221.
25. Syrogiannopoulos, G. A., Grivea, I. N., Anastassiou, E. D., Triga, M. G., Dimitracopoulos, G. O., Beratis, N. G. (2001) Sterile cerebrospinal fluid pleocytosis in young infants with urinary tract infection. Pediatr. Infect. Dis. J. 20, 927-930.
26. Doby, E. H., Stockmann, C., Korgenski, E. K., Blaschke, A. J., Byington, C. L. (2013) Cerebrospinal fluid pleocytosis in febrile infants 1-90 days with urinary tract infection. Pediatr. Infect. Dis. J. 32, 1024-1026.
27. Bi, D., Qiao, L., Bergelson, I., Ek, C. J., Duan, L., Zhang, X., Albertsson, A. M., Pettengill, M., Kronforst, K., Ninkovic, J., Goldmann, D., Janzon, A., Hagberg, H., Wang, X., Mallard, C., Levy, O. (2015) Staphylococcus epidermidis bacteremia induces brain injury in neonatal mice via Toll-like receptor 2-dependent and-independent pathways. J. Infect. Dis. 212, 1480-1490.
28. Jin, M. S., Kim, S. E., Heo, J. Y., Lee, M. E., Kim, H. M., Paik, S. G., Lee, H., Lee, J. O. (2007) Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated lipopeptide. Cell 130, 1071-1082.
29. Morr, M., Takeuchi, O., Akira, S., Simon, M. M., Mühlradt, P. F. (2002) Differential recognition of structural details of bacterial lipopeptides by Toll-like receptors. Eur. J. Immunol. 32, 3337-3347.
30. Medzhitov, R. (2008) Origin and physiological roles of inflammation. Nature 454, 428-435.
31. Serbina, N. V., Pamer, E. G. (2006) Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat. Immunol. 7, 311-317.
32. Auffray, C., Fogg, D., Garfa, M., Elain, G., Join-Lambert, O., Kayal, S., Sarnacki, S., Cumano, A., Lauvau, G., Geissmann, F. (2007) Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 317, 666-670.
33. Cros, J., Cagnard, N., Woollard, K., Patey, N., Zhang, S.-Y., Senechal, B., Puel, A., Biswas, S. K., Moshous, D., Picard, C., Jais, J.-P., D’Cruz, D., Casanova, J.-L., Trouillet, C., Geissmann, F. (2010) Human CD14dim monocytes patrol and sense nucleic acids and viruses via TLR7 and TLR8 receptors. Immunity 33, 375-386.
34. Parker, L. C., Whyte, M. K. B., Vogel, S. N., Dower, S. K., Sabroe, I. (2004) Toll-like receptor (TLR)2 and TLR4 agonists regulate CCR expression in human monocytic cells. J. Immunol. 172, 4977-4986.
35. Reichel, C. A., Puhr-Westerheide, D., Zuchtriegel, G., Uhl, B., Berberich, N., Zahler, S., Wymann, M. P., Luckow, B., Krombach, F. (2012) C-C motif chemokine CCL3 and canonical neutrophil attractants promote neutrophil extravasation through common and distinct mechanisms. Blood 120, 880-890.
36. Spanaus, K. S., Nadal, D., Pfister, H. W., Seebach, J., Widmer, U., Frei, K., Gloor, S., Fontana, A. (1997) C-X-C and C-C chemokines are expressed in the cerebrospinal fluid in bacterial meningitis and mediate chemotactic activity on peripheral blood-derived polymorphonuclear and mononuclear cells in vitro. J. Immunol. 158, 1956-1964.
37. Diab, A., Abdalla, H., Li, H. L., Shi, F. D., Zhu, J., Höjberg, B., Lindquist, L., Wretlind, B., Bakhiet, M., Link, H. (1999) Neutralization of macrophage inflammatory protein 2 (MIP-2) and MIP-1a attenuates neutrophil recruitment in the central nervous system during experimental bacterial meningitis. Infect. Immun. 67, 2590-2601.
38. Silva, M. T. (2010) When two is better than one: macrophages and neutrophils work in concert in innate immunity as complementary and cooperative partners of a myeloid phagocyte system. J. Leukoc. Biol. 87, 93-106.
39. Rivest, S. (2009) Regulation of innate immune responses in the brain. Nat. Rev. Immunol. 9, 429-439.