P-selectin-mediated monocyte-cerebral endothelium adhesive interactions link peripheral organ inflammation to sickness behaviors

Journal of Neuroscience

Volumn 33, Issue 37, 2013, Pages 14878-14888

  D'Mello, Charlotte ^a   Riazi, Kiarash ^a,c   Le, Tai ^a   Stevens, Katarzyna M ^a   Wang, Arthur ^b   McKay, Derek M ^b   Pittman, Quentin J ^a,c   Swain, Mark G ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; BILIRUBIN; INDUCIBLE NITRIC OXIDE SYNTHASE; MINOCYCLINE; PADGEM PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CHEMOTAXIS; COLITIS; CONTROLLED STUDY; CREMASTER MUSCLE; ENDOTHELIUM CELL; FLOW CYTOMETRY; FLUORESCENCE ANALYSIS; HEPATITIS; HIPPOCAMPUS; ILLNESS BEHAVIOR; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LEUKOCYTE; MALE; MICROGLIA; MICROSCOPY; MONOCYTE; MOUSE; NERVE EXCITABILITY; NONHUMAN; PRIORITY JOURNAL;

ALANINE TRANSAMINASE; ANIMALS; CELL ADHESION; CEREBRAL CORTEX; CHOLESTASIS; COLITIS; CYTOKINES; DINITROFLUOROBENZENE; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; FEMALE; HIPPOCAMPUS; ILLNESS BEHAVIOR; INFLAMMATION; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MONOCYTES; MURAMIDASE; P-SELECTIN; PENTYLENETETRAZOLE;

EID: 84883665716     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1329-13.2013     Document Type: Article

References (49)

1. Ahmed Z, Shaw G, Sharma VP, Yang C, McGowan E, Dickson DW (2007) Actin-binding proteins coronin-1a and IBA-1 are effective microglial markers for immunohistochemistry. J Histochem Cytochem 55:687-700. CrossRef Medline
2. Audoy-Rémus J, Richard JF, Soulet D, Zhou H, Kubes P, Vallières L (2008) Rod-shaped monocytes patrol the brain vasculature and give rise to perivascular macrophages under the influence of proinflammatory cytokines and angiopoietin-2. J Neurosci 28:10187-10199. CrossRef Medline
3. Biscaro B, Lindvall O, Tesco G, Ekdahl CT, Nitsch RM (2012) Inhibition of microglial activation protects hippocampal neurogenesis and improves cognitive deficits in a transgenic mouse model for Alzheimer's disease. Neurodegener Dis 9:187-198. CrossRef Medline
4. Burak KW, Le T, Swain MG (2002) Increased sensitivity to the locomotoractivating effects of corticotropin-releasing hormone in cholestatic rats. Gastroenterology 122:681-688. CrossRef Medline
5. Cabal-Hierro L, Lazo PS (2012) Signal transduction by tumor necrosis factor receptors. Cell Signal 24:1297-1305. CrossRef Medline
6. Cairo F, Nieri M, Gori AM, Rotundo R, Castellani S, Abbate R, Pini-Prato GP (2009) Periodontal variables may predict sub-clinical atherosclerosis and systemic inflammation in young adults: a cross-sectional study. Eur J Oral Implantol 2:125-133. Medline
7. Capuron L, Miller AH (2011) Immune system to brain signaling: neuropsychopharmacological implications. Pharmacol Ther 130:226-238. CrossRef Medline
8. Carvalho-Tavares J, Hickey MJ, Hutchison J, Michaud J, Sutcliffe IT, Kubes P (2000) A role for platelets and endothelial selectins in tumor necrosis factor-_ induced leukocyte recruitment in the brain microvasculature. Circ Res 87:1141-1148. CrossRef Medline
9. D'Mello C, Swain MG (2011) Liver-brain inflammation axis. Am J Physiol Gastrointest Liver Physiol 301:G749-G761. CrossRef Medline
10. D'Mello C, Le T, Swain MG (2009) Cerebral microglia recruit monocytes into the brain in response to tumor necrosis factor α signaling during peripheral organ inflammation. J Neurosci 29:2089-2102. CrossRef Medline
11. Dougados M, Ripert M, Hilliquin P, Brocq O, Brault Y, Logeart I (2012) Onset of action of etanercept in rheumatoid arthritis based on patientreported outcomes. Clin Exp Rheumatol 30:266-268. Medline
12. Fabene PF, et al. (2008) A role for leukocyte-endothelial adhesion mechanisms in epilepsy. Nat Med 14:1377-1383. CrossRef Medline
13. Faust N, Varas F, Kelly LM, 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. Medline
14. Feagan BG, Sandborn WJ, Hass S, Niecko T, White J (2007) Health-related quality of life during natalizumab maintenance therapy for Crohn's disease. Am J Gastroenterol 102:2737-2746. CrossRef Medline
15. Galic MA, Riazi K, Heida JG, Mouihate A, Fournier NM, Spencer SJ, Kalynchuk LE, Teskey GC, Pittman QJ (2008) Postnatal inflammation increases seizure susceptibility in adult rats. J Neurosci 28:6904-6913. CrossRef Medline
16. Getts DR, Terry RL, Getts MT, Müller M, Rana S, Shrestha B, Radford J, van Rooijen N, Campbell IL, King NJ (2008) Ly6C+"inflammatory monocytes" are microglial precursors recruited in a pathogenic manner in West Nile virus encephalitis. J Exp Med 205:2319-2337. CrossRef Medline
17. Gosselin D, Rivest S (2008) MyD88 signaling in brain endothelial cells is essential for the neuronal activity and glucocorticoid release during systemic inflammation. Mol Psychiatry 13:480-497. CrossRef Medline
18. Graff LA, Vincent N, Walker JR, Clara I, Carr R, Ediger J, Miller N, Rogala L, Rawsthorne P, Lix L, Bernstein CN (2011) A population-based study of fatigue and sleep difficulties in inflammatory bowel disease. Inflamm Bowel Dis 17:1882-1889. CrossRef Medline
19. Henry CJ, Huang Y, Wynne A, Hanke M, Himler J, Bailey MT, Sheridan JF, Godbout JP (2008) Minocycline attenuates lipopolysaccharide (LPS)- induced neuroinflammation, sickness behavior and anhedonia. J Neuroinflammation 5:15. CrossRef Medline
20. Hickey MJ, Sharkey KA, Sihota EG, Reinhardt PH, Macmicking JD, Nathan C, Kubes P (1997) Inducible nitric oxide synthase-deficient mice have enhanced leukocyte-endothelium interactions in endotoxemia. FASEB J 11:955-964. Medline
21. Hristov M, Weber C (2011) Differential role of monocyte subsets in atherosclerosis. Throm Haemost 106:757-762. CrossRef Medline
22. Hu Y, Wu DL, Luo CX, Zhu LJ, Zhang J, Wu HY, Zhu DY (2012) Hippocampal nitric oxide contributes to sex difference in affective behaviors. Proc Natl Acad Sci U S A 109:14224-14229. CrossRef Medline
23. Hunter MM, Wang A, Parhar KS, Johnston MJ, Van Rooijen N, Beck PL, McKay DM (2010) In vitro-derived alternatively activated macrophages reduce colonic inflammation in mice. Gastroenterology 138:1395-1405. CrossRef Medline
24. Kerfoot SM, D'Mello C, Nguyen H, Ajuebor MN, Kubes P, Le T, Swain MG (2006) TNF-α secreting monocytes are recruited into the brains of cholestatic mice. Hepatology 43:154-162. CrossRef Medline
25. Kim JV, Kang SS, Dustin ML, McGavern DB (2009) Myelomonocytic cell recruitment causes fatal CNS vascular injury during acute viral meningitis. Nature 457:191-195. CrossRef Medline
26. Kuno R, Wang J, Kawanokuchi J, Takeuchi H, Mizuno T, Suzumura A (2005) Autocrine activation of microglia by tumor necrosis factor-α. J Neuroimmunol 162:89-96. CrossRef Medline
27. Lee WY, Moriarty TJ, Wong CH, Zhou H, Strieter RM, van Rooijen N, Chaconas G, Kubes P (2010) An intravascular immune response to Borrelia burgdorferi involves Kupffer cells and iNKT cells. Nat Immunol 11:295-302. CrossRef Medline
28. Liu L, Cara DC, Kaur J, Raharjo E, Mullaly SC, Jongstra-Bilen J, Jongstra J, Kubes P (2005) LPS1 is an endothelial gatekeeper of leukocyte transendothelial migration. J Exp Med 201:409-418. CrossRef Medline
29. Loftus EV, Feagan BG, Colombel JF, Rubin DT, Wu EQ, Yu AP, Pollack PF, Chao J, Mulani P (2008) Effects of adalimumab maintenance therapy on healthrelated quality of life of patients with Crohn's disease: patient-reported outcomes of the CHARM trial. Am J Gastroenterol 103:3132-3141. CrossRef Medline
30. Lorton D, Lubahn CL, Zautra AJ, Bellinger DL (2008) Proinflammatory cytokines and sickness behavior in rheumatic diseases. Curr Pharm Des 14:1242-1260. CrossRef Medline
31. Mandhane SN, Aavula K, Rajamannar T (2007) Timed pentylenetetrazol infusion test: a comparative analysis with s.c.PTZ and MES models of anticonvulsant screening in mice. Seizure 16:636-644. CrossRef Medline
32. Månsson P, Zhang XW, Jeppsson B, Johnell O, Thorlacius H (2000) Critical role of P-selectin dependent rolling in tumor necrosis factor-α induced leukocyte adhesion and extravascular recruitment in vivo. Naunyn Schmiedebergs Arch Pharmacol 362:190-196. CrossRef Medline
33. Neuman M, Angulo P, Malkiewicz I, Jorgensen R, Shear N, Dickson ER, Haber J, Katz G, Lindor K (2002) Tumor necrosis factor-alpha and transforming growth factor-beta reflect severity of liver damage in primary biliary cirrhosis. J Gastroenterol Hepatol 17:196-202. CrossRef Medline
34. Nguyen H, Wang H, Le T, Ho W, Sharkey KA, Swain MG (2008) Downregulated hypothalamic 5-HT3 receptor expression and enhanced 5HT3 receptor antagonist mediated improvement in fatigue like behavior in cholestatic rats. Neurogastroenterol Motil 20:228-235. CrossRef Medline
35. Nguyen K, D'Mello C, Le T, Urbanski S, Swain MG (2012) Regulatory T cells suppress sickness behaviour development without altering liver injury in cholestatic mice. J Hepatol 56:626-631. CrossRef Medline
36. Putzki N, Yaldizli O, Tettenborn B, Diener HC (2009) Multiple sclerosis associated fatigue during natalizumab treatment. J Neurol Sci 285:109-113. CrossRef Medline
37. Revicki DA, Willian MK, Menter A, Gordon KB, Kimball AB, Leonardi CL, Langley RG, Kimel M, Okun M (2007) Impact of adalimumab treatment on patient-reported outcomes: results from a phase III clinical trial in patients with moderate to severe plaque psoriasis. J Dermatolog Treat 18:341-350. CrossRef Medline
38. Riazi K, Galic MA, Kuzmiski JB, Ho W, Sharkey KA, Pittman QJ (2008) Microglial activation and TNFα production mediate altered CNS excitability following peripheral inflammation. Proc Natl Acad Sci U S A 105: 17151-17156. CrossRef Medline
39. Rudick RA, et al. (2007) Health-related quality of life in multiple sclerosis: effects of natalizumab. Ann Neurol 62:335-346. CrossRef Medline
40. Sedgwick JD, Schwender S, Imrich H, Dörries R, Butcher GW, ter Meulen V (1991) Isolation and direct characterization of resident microglial cells from the normal and inflamed central nervous system. Proc Natl Acad Sci U S A 88:7438-7442. CrossRef Medline
41. Shafer RA, Murphy S (1997) Activated astrocytes induce nitric oxide synthase-2 in cerebral endothelium via tumor necrosis factor α. Glia 21: 370-379. CrossRef Medline
42. Shi C, Pamer EG (2011) Monocyte recruitment during infection and inflammation. Nat Rev Immunol 11:762-774. CrossRef Medline
43. Stirling DP, Liu S, Kubes P, Yong VW (2009) Depletion of Ly6G/GR-1 leukocytes after spinal cord injury in mice alters wound healing and worsens neurological outcome. J Neurosci 29:753-764. CrossRef Medline
44. Strand V, Khanna D (2010) The impact of rheumatoid arthritis and treatment on patients' lives. Clin Exp Rheumatol 28:S32-S40. Medline
45. Targan SR, Feagan BG, Fedorak RN, Lashner BA, Pannaccione R, Present DH, Spehlmann ME, Rutgeerts PJ, Tulassay Z, Volfova M, Wolf DC, Hernandez C, Bornstein J, Sandborn WJ (2007) Natalizumab for the treatment of active Crohn's disease: results of the ENCORE trial. Gastroenterology 132:1672-1683. CrossRef Medline
46. Tontsch U, Bauer HC (1989) Isolation, characterization and long term cultivation of porcine and murine cerebral capillary endothelial cells. Microvasc Res 37:148-161. CrossRef Medline
47. Wong ML, Rettori V, al-Shekhlee A, Bongiorno PB, Canteros G, McCann SM, Gold PW, Licinio J (1996) Inducible nitric oxide synthase gene expression in the brain during systemic inflammation. Nat Med 2:581-584. CrossRef Medline
48. Wu DC, Jackson-Lewis V, Vila M, Tieu K, Teismann P, Vadseth C, Choi DK, Ischiropoulos H, Przedborski S (2002) Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson disease. J Neurosci 22:1763-1771. Medline
49. Yenari MA, Xu L, Tang XN, Qiao Y, Giffard RG (2006) Microglia potentiate damage to blood-brain barrier constituents. Stroke 37:1087-1093. CrossRef Medline