Capillary and arteriolar pericytes attract innate leukocytes exiting through venules and 'instruct' them with pattern-recognition and motility programs

Nature Immunology

Volumn 14, Issue 1, 2013, Pages 41-51

  Stark, Konstantin ^a   Eckart, Annekathrin ^a   Haidari, Selgai ^a   Tirniceriu, Anca ^a   Lorenz, Michael ^a   Von Brühl, Marie Luise ^a   Gärtner, Florian ^a   Khandoga, Alexander Georg ^a   Legate, Kyle R ^a,b   Pless, Robert ^c   Hepper, Ingrid ^d   Lauber, Kirsten ^b   Walzog, Barbara ^d   Massberg, Steffen ^a,e  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c WASHINGTON UNIVERSITY   (United States)

^d LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^e DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOATTRACTANT; CHEMOKINE; INTERCELLULAR ADHESION MOLECULE 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL MOTILITY; CELL SURVIVAL; HUMAN; HUMAN CELL; IMMUNOSURVEILLANCE; INNATE IMMUNITY; LEUKOCYTE; MACROPHAGE; MOUSE; NEUTROPHIL; NONHUMAN; PATTERN RECOGNITION; PERICYTE; PRIORITY JOURNAL; UPREGULATION;

ANTIBODIES, BLOCKING; ARTERIOLES; CAPILLARIES; CELL COMMUNICATION; CELL MOVEMENT; CELLS, CULTURED; HUMANS; IMMUNITY, INNATE; INFLAMMATION MEDIATORS; INTERCELLULAR ADHESION MOLECULE-1; INTRAMOLECULAR OXIDOREDUCTASES; LEUKOCYTES; MACROPHAGE MIGRATION-INHIBITORY FACTORS; NEUTROPHIL ACTIVATION; PERICYTES; RECEPTORS, PATTERN RECOGNITION; UP-REGULATION; VENULES;

EID: 84871189221     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.2477     Document Type: Article

References (50)

1. Chen, G.Y. & Nunez, G. Sterile inflammation: sensing and reacting to damage. Nat. Rev. Immunol. 10, 826-837 (2010).
2. Kono, H. & Rock, K.L. How dying cells alert the immune system to danger. Nat. Rev. Immunol. 8, 279-289 (2008).
3. McDonald, B. & Kubes, P. Cellular and molecular choreography of neutrophil recruitment to sites of sterile inflammation. J. Mol. Med. 89, 1079-1088 (2011).
4. Zhang, Q. et al. Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 464, 104-107 (2010).
5. Peter, C., Wesselborg, S., Herrmann, M. & Lauber, K. Dangerous attraction: phagocyte recruitment and danger signals of apoptotic and necrotic cells. Apoptosis 15, 1007-1028 (2010).
6. Phillipson, M. & Kubes, P. The neutrophil in vascular inflammation. Nat. Med. 17, 1381-1390 (2011).
7. Ley, K., Laudanna, C., Cybulsky, M.I. & Nourshargh, S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 7, 678-689 (2007).
8. McDonald, B. et al. Intravascular danger signals guide neutrophils to sites of sterile inflammation. Science 330, 362-366 (2010).
9. Nourshargh, S., Hordijk, P.L. & Sixt, M. Breaching multiple barriers: leukocyte motility through venular walls and the interstitium. Nat. Rev. Mol. Cell Biol. 11, 366-378 (2010).
10. Woodfin, A. et al. The junctional adhesion molecule JAM-C regulates polarized transendothelial migration of neutrophils in vivo. Nat. Immunol. 12, 761-769 (2011).
11. Bajénoff, M. et al. Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes. Immunity 25, 989-1001 (2006).
12. Mempel, T.R., Henrickson, S.E. & Von Andrian, U.H. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 427, 154-159 (2004).
13. Friedl, P. & Weigelin, B. Interstitial leukocyte migration and immune function. Nat. Immunol. 9, 960-969 (2008).
14. Armulik, A., Abramsson, A. & Betsholtz, C. Endothelial/pericyte interactions. Circ. Res. 97, 512-523 (2005).
15. Armulik, A., Genove, G. & Betsholtz, C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev. Cell 21, 193-215 (2011).
16. Armulik, A. et al. Pericytes regulate the blood-brain barrier. Nature 468, 557-561 (2010).
17. Balabanov, R., Beaumont, T. & Dore-Duffy, P. Role of central nervous system microvascular pericytes in activation of antigen-primed splenic T-lymphocytes. J. Neurosci. Res. 55, 578-587 (1999).
18. Verbeek, M.M., Westphal, J.R., Ruiter, D.J. & de Waal, R.M. T lymphocyte adhesion to human brain pericytes is mediated via very late antigen-4/vascular cell adhesion molecule-1 interactions. J. Immunol. 154, 5876-5884 (1995).
19. Murfee, W.L., Skalak, T.C. & Peirce, S.M. Differential arterial/venous expression of NG2 proteoglycan in perivascular cells along microvessels: identifying a venule-specific phenotype. Microcirculation 12, 151-160 (2005).
20. Proebstl, D. et al. Pericytes support neutrophil subendothelial cell crawling and breaching of venular walls in vivo. J. Exp. Med. 209, 1219-1234 (2012).
21. Lebrin, F. et al. Thalidomide stimulates vessel maturation and reduces epistaxis in individuals with hereditary hemorrhagic telangiectasia. Nat. Med. 16, 420-428 (2010).
22. Zhu, X., Bergles, D.E. & Nishiyama, A. NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 135, 145-157 (2008).
23. Petrie, R.J., Doyle, A.D. & Yamada, K.M. Random versus directionally persistent cell migration. Nat. Rev. Mol. Cell Biol. 10, 538-549 (2009).
24. Edelman, D.A., Jiang, Y., Tyburski, J.G., Wilson, R.F. & Steffes, C.P. Lipopolysaccharide activation of pericyte's Toll-like receptor-4 regulates co-culture permeability. Am. J. Surg. 193, 730-735 (2007).
25. Franchi, L., Eigenbrod, T., Munoz-Planillo, R. & Nunez, G. The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat. Immunol. 10, 241-247 (2009).
26. Bernhagen, J. et al. MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment. Nat. Med. 13, 587-596 (2007).
27. Santos, L.L. et al. Macrophage migration inhibitory factor regulates neutrophil chemotactic responses in inflammatory arthritis in mice. Arthritis Rheum. 63, 960-970 (2011).
28. Cheng, Q. et al. Macrophage migration inhibitory factor increases leukocyte-endothelial interactions in human endothelial cells via promotion of expression of adhesion molecules. J. Immunol. 185, 1238-1247 (2010).
29. Gregory, J.L. et al. Reduced leukocyte-endothelial cell interactions in the inflamed microcirculation of macrophage migration inhibitory factor-deficient mice. Arthritis Rheum. 50, 3023-3034 (2004).
30. Al-Abed, Y. & VanPatten, S. MIF as a disease target: ISO-1 as a proof-of-concept therapeutic. Future Med. Chem. 3, 45-63 (2011).
31. Cvetkovic, I. et al. Critical role of macrophage migration inhibitory factor activity in experimental autoimmune diabetes. Endocrinology 146, 2942-2951 (2005).
32. Leng, L. et al. A small-molecule macrophage migration inhibitory factor antagonist protects against glomerulonephritis in lupus-prone NZB/NZW F1 and MRL/lpr mice. J. Immunol. 186, 527-538 (2010).
33. Hudson, J.D. et al. A proinflammatory cytokine inhibits p53 tumor suppressor activity. J. Exp. Med. 190, 1375-1382 (1999).
34. Afonso, P.V. et al. LTB4 is a signal-relay molecule during neutrophil chemotaxis. Dev. Cell 22, 1079-1091 (2012).
35. Auffray, C. et al. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 317, 666-670 (2007).
36. Baumann, R. et al. Macrophage migration inhibitory factor delays apoptosis in neutrophils by inhibiting the mitochondria-dependent death pathway. FASEB J. 17, 2221-2230 (2003).
37. Luster, A.D., Alon, R. & von Andrian, U.H. Immune cell migration in inflammation: present and future therapeutic targets. Nat. Immunol. 6, 1182-1190 (2005).
38. Foxman, E.F., Campbell, J.J. & Butcher, E.C. Multistep navigation and the combinatorial control of leukocyte chemotaxis. J. Cell Biol. 139, 1349-1360 (1997).
39. Miller, M.J., Wei, S.H., Parker, I. & Cahalan, M.D. Two-photon imaging of lymphocyte motility and antigen response in intact lymph node. Science 296, 1869-1873 (2002).
40. Sumen, C., Mempel, T.R., Mazo, I.B. & von Andrian, U.H. Intravital microscopy: visualizing immunity in context. Immunity 21, 315-329 (2004).
41. Zachariah, M.A. & Cyster, J.G. Neural crest-derived pericytes promote egress of mature thymocytes at the corticomedullary junction. Science 328, 1129-1135 (2010).
42. Schumann, K. et al. Immobilized chemokine fields and soluble chemokine gradients cooperatively shape migration patterns of dendritic cells. Immunity 32, 703-713 (2010).
43. Siffrin, V. et al. Differential immune cell dynamics in the CNS cause CD4+ T cell compartmentalization. Brain 132, 1247-1258 (2009).
44. Link, A. et al. Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells. Nat. Immunol. 8, 1255-1265 (2007).
45. Livak, K.J. & Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔCT) method. Methods 25, 402-408 (2001).
46. Faust, N., Varas, F., Kelly, L.M., Heck, S. & Graf, T. Insertion of enhanced green fluorescent protein into the lysozyme gene creates mice with green fluorescent granulocytes and macrophages. Blood 96, 719-726 (2000).
47. Jung, S. et al. Analysis of fractalkine receptor CX3CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol. Cell. Biol. 20, 4106-4114 (2000).
48. Li, J.L. et al. Intravital multiphoton imaging of immune responses in the mouse ear skin. Nat. Protoc. 7, 221-234 (2012).
49. Ng, L.G. et al. Visualizing the neutrophil response to sterile tissue injury in mouse dermis reveals a three-phase cascade of events. J. Invest. Dermatol. 131, 2058-2068 (2011).
50. Kreisel, D. et al. In vivo two-photon imaging reveals monocyte-dependent neutrophil extravasation during pulmonary inflammation. Proc. Natl. Acad. Sci. USA 107, 18073-18078 (2010).