Stromal cells differentially regulate neutrophil and lymphocyte recruitment through the endothelium

Immunology

Volumn 131, Issue 3, 2010, Pages 357-370

  McGettrick, Helen M ^a   Buckley, Christopher D ^a   Filer, Andrew ^a   Ed Rainger, G ^a   Nash, Gerard B ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

Endothelial cells; Fibroblasts; Lymphocytes; Migration; Neutrophils

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL ADHESION; CELL CONTACT; CELL CULTURE; CELL MIGRATION; ENDOTHELIUM CELL; FIBROBLAST; HUMAN; HUMAN CELL; LYMPHOCYTE; LYMPHOCYTE MIGRATION; NEUTROPHIL; PRIORITY JOURNAL; STROMA CELL;

CELL ADHESION; CELL COMMUNICATION; CELL MIGRATION ASSAYS; CELL MOVEMENT; CELLS, CULTURED; CHEMOKINE CXCL12; COCULTURE TECHNIQUES; ENDOTHELIUM; FIBROBLASTS; HEPARIN LYASE; HUMANS; LYMPHOCYTES; SKIN; SYNOVIAL MEMBRANE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 78649433128     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/j.1365-2567.2010.03307.x     Document Type: Article

References (73)

1. Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 2007; 7:678-89.
2. Luu NT, Rainger GE, Nash GB. Differential ability of exogenous chemotactic agents to disrupt transendothelial migration of flowing neutrophils. J Immunol 2000; 164:5961-9.
3. Tull SP, Yates CM, Maskrey BH et al. Omega-3 Fatty acids and inflammation: novel interactions reveal a new step in neutrophil recruitment. PLoS Biol 2009; 7:e1000177.
4. + T lymphocytes on tumour necrosis factor-a-activated vascular endothelium under flow. J Exp Med 1995; 181:1179-86.
5. Piali L, Weber C, LaRosa G, Mackay CR, Springer TA, Clark-Lewis I, Moser B. The chemokine receptor CXCR3 mediates rapid and shear-resistant adhesion-induction of effector T lymphocytes by the chemokines IP10 and Mig. Eur J Immunol 1998; 28:961-72.
6. Cinamon G, Shinder V, Alon R. Shear forces promote lymphocyte migration across vascular endothelium bearing apical chemokines. Nat Immunol 2001; 2:515-22.
7. McGettrick HM, Hunter K, Moss PA, Buckley CD, Rainger GE, Nash GB. Direct observations of the kinetics of migrating T cells suggest active retention by endothelial cells with continual bidirectional migration. J Leukoc Biol 2009; 85:97-107.
8. McGettrick HM, Smith E, Filer A et al. Fibroblasts from different sites may promote or inhibit recruitment of flowing lymphocytes by endothelial cells. Eur J Immunol 2009; 39:98-107.
9. Cinamon G, Grabovsky V, Winter E et al. Novel chemokine functions in lymphocyte migration through vascular endothelium under shear flow. J Leukoc Biol 2001; 69:860-6.
10. Pietschmann P, Cush JJ, Lipsky PE, Oppenheimer-Marks N. Identification of subsets of human T cells capable of enhanced transendothelial migration. J Immunol 1992; 149:1170-8.
11. + T cells that exhibit a transendothelial migratory capacity. J Immunol 1995; 154:3062-77.
12. Denton CP, Shi-Wen X, Sutton A, Abraham D, Black CM, Pearson JD. Scleroderma fibroblasts promote migration of mononuclear leukocytes across endothelial cell monolayers. Clin Exp Immunol 1998; 114:293-300.
13. Mul FP, Zuurbier AE, Janssen H et al. Sequential migration of neutrophils across monolayers of endothelial and epithelial cells. J Leukoc Biol 2000; 68:529-37.
14. Rainger GE, Nash GB. Cellular pathology of atherosclerosis: smooth muscle cells prime cocultured endothelial cells for enhanced leukocyte adhesion. Circ Res 2001; 88:615-22.
15. Edwards S, Lalor PF, Nash GB, Rainger GE, Adams DH. Lymphocyte traffic through sinusoidal endothelial cells is regulated by hepatocytes. Hepatology 2005; 41:451-9.
16. Lally F, Smith E, Filer A et al. A novel mechanism of neutrophil recruitment in a coculture model of the rheumatoid synovium. Arthritis Rheum 2005; 52:3460-649.
17. Smith E, McGettrick HM, Stone MA et al. Duffy antigen receptor for chemokines and CXCL5 are essential for the recruitment of neutrophils in a multicellular model of rheumatoid arthritis synovium. Arthritis Rheum 2008; 58:1968-73.
18. Bijuklic K, Jennings P, Kountchev J et al. Migration of leukocytes across an endothelium-epithelium bilayer as a model of renal interstitial inflammation. Am J Physiol 2007; 293:C486-92.
19. Buttrum SM, Hatton R, Nash GB. Selectin-mediated rolling of neutrophils on immobilized platelets. Blood 1993; 82:1165-74.
20. Rainger GE, Stone P, Morland CM, Nash GB. A novel system for investigating the ability of smooth muscle cells and fibroblasts to regulate adhesion of flowing leukocytes to endothelial cells. J Immunol Methods 2001; 255:73-82.
21. Salmon M, Scheel-Toellner D, Huissoon AP et al. Inhibition of T cell apoptosis in the rheumatoid synovium. J Clin Invest 1997; 99:439-46.
22. Cooke BM, Usami S, Perry I, Nash GB. A simplified method for culture of endothelial cells and analysis of adhesion of blood cells under conditions of flow. Microvas Res 1993; 45:33-45.
23. Chappell D, Jacob M, Rehm M, Stoeckelhuber M, Welsch U, Conzen P, Becker BF. Heparinase selectively sheds heparan sulphate from the endothelial glycocalyx. Biol Chem 2008; 389:79-82.
24. McGettrick HM, Lord JM, Wang KQ, Rainger GE, Buckley CD, Nash GB. Chemokine- and adhesion-dependent survival of neutrophils after transmigration through cytokine-stimulated endothelium. J Leukoc Biol 2006; 79:779-88.
25. Chakravorty SJ, McGettrick HM, Butler LM, Buckley CD, Rainger GE, Nash GB. An in vitro model for analysing neutrophil migration into and away from the sub-endothelial space: roles of flow and CD31. Biorheology 2006; 43:71-82.
26. Luu NT, Rainger GE, Nash GB. Kinetics of the different steps during neutrophil migration through cultured endothelial monolayers treated with tumour necrosis factor-alpha. J Vas Res 1999; 36:477-85.
27. Oppenheimer-Marks N, Lipsky PE. Migration of naive and memory T cells. Immunol Today 1997; 18:456-7.
28. Hardingham TE, Fosang AJ. Proteoglycans: many forms and many functions. FASEB J 1992; 6:861-70.
29. Taylor KR, Gallo RL. Glycosaminoglycans and their proteoglycans: host-associated molecular patterns for initiation and modulation of inflammation. FASEB J 2006; 20:9-22.
30. Szczepanek K, Kieda C, Cichy J. Differential binding of hyaluronan on the surface of tissue-specific endothelial cell lines. Acta Biochim Pol 2008; 55:35-42.
31. Butler LM, Rainger GE, Nash GB. A role for the endothelial glycosaminoglycan hyaluronan in neutrophil recruitment by endothelial cells cultured for prolonged periods. Exp Cell Res 2009; 315:3433-41.
32. Burger JA, Zvaifler NJ, Tsukada N, Firestein GS, Kipps TJ. Fibroblast-like synoviocytes support B-cell pseudoemperipolesis via a stromal cell-derived factor-1- and CD106 (VCAM-1)-dependent mechanism. J Clin Invest 2001; 107:305-15.
33. Fedyk ER, Jones D, Critchley HO, Phipps RP, Blieden TM, Springer TA. Expression of stromal-derived factor-1 is decreased by IL-1 and TNF and in dermal wound healing. J Immunol 2001; 166:5749-54.
34. + T cell migration within synovial tissue. Arthritis Rheum 2003; 48:2472-82.
35. Curbishley SM, Eksteen B, Gladue R, Lalor PF, Adams D. CXCR3 activation promotes lymphocyte transendothelial migration across human hepatic endothelium under fluid flow. Am J Pathol 2005; 167:887-99.
36. Filer A, Bik M, Parsonage GN et al. Galectin 3 induces a distinctive pattern of cytokine and chemokine production in rheumatoid synovial fibroblasts via selective signaling pathways. Arthritis Rheum 2009; 60:1604-14.
37. Holt AP, Haughton EL, Lalor PF, Filer A, Buckley CD, Adams DH. Liver myofibroblasts regulate infiltration and positioning of lymphocytes in human liver. Gastroenterology 2009; 136:705-14.
38. Koch AE, Kunkel SL, Shah MR et al. Growth-related gene product alpha. A chemotactic cytokine for neutrophils in rheumatoid arthritis. J Immunol 1995; 155:3660-6.
39. Nanki T, Nagasaka K, Hayashida K, Saita Y, Miyasaka N. Chemokines regulate IL-6 and IL-8 production by fibroblast-like synoviocytes from patients with rheumatoid arthritis. J Immunol 2001; 167:5381-5.
40. Proost P, Verpoest S, Van de BK et al. Synergistic induction of CXCL9 and CXCL11 by Toll-like receptor ligands and interferon-gamma in fibroblasts correlates with elevated levels of CXCR3 ligands in septic arthritis synovial fluids. J Leukoc Biol 2004; 75:777-84.
41. Ueno A, Yamamura M, Iwahashi M, Okamoto A, Aita T, Ogawa N, Makino H. The production of CXCR3-agonistic chemokines by synovial fibroblasts from patients with rheumatoid arthritis. Rheumat Int 2005; 25:361-7.
42. Shulman Z, Shinder V, Klein E et al. Lymphocyte crawling and transendothelial migration require chemokine triggering of high-affinity LFA-1 integrin. Immunity 2009; 30:384-96.
43. Shamri R, Grabovsky V, Gauguet JM et al. Lymphocyte arrest requires instantaneous induction of an extended LFA-1 conformation mediated by endothelium-bound chemokines. Nat Immunol 2005; 6:497-506.
44. Middleton J, Patterson AM, Gardner L, Schmutz C, Ashton BA. Leukocyte extravasation: chemokine transport and presentation by the endothelium. Blood 2002; 100:3853-60.
45. Arisaka T, Mitsumata M, Kawasumi M, Tohjima T, Hirose S, Yoshida Y. Effects of shear stress on glycosaminoglycan synthesis in vascular endothelial cells. Ann N Y Acad Sci 1995; 748:543-54.
46. Van Lint P, Libert C. Chemokine and cytokine processing by matrix metalloproteinases and its effect on leukocyte migration and inflammation. J Leukoc Biol 2007; 82:1375-81.
47. Li Q, Park PW, Wilson CL, Parks WC. Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury. Cell 2002; 111:635-46.
48. Khandoga A, Kessler JS, Hanschen M et al. Matrix metalloproteinase-9 promotes neutrophil and T cell recruitment and migration in the postischemic liver. J Leukoc Biol 2006; 79:1295-305.
49. Ranjbaran H, Wang Y, Manes TD et al. Heparin displaces interferon-gamma-inducible chemokines (IP-10, I-TAC, and Mig) sequestered in the vasculature and inhibits the transendothelial migration and arterial recruitment of T cells. Circulation 2006; 114:1293-300.
50. Colditz IG, Schneider MA, Pruenster M, Rot A. Chemokines at large: in-vivo mechanisms of their transport, presentation and clearance. Thromb Haemost 2007; 97:688-93.
51. Pruenster M, Mudde L, Bombosi P et al. The Duffy antigen receptor for chemokines transports chemokines and supports their promigratory activity. Nat Immunol 2009; 10:101-8.
52. Mohan K, Ding Z, Hanly J, Issekutz TB. IFN-gamma-inducible T cell alpha chemoattractant is a potent stimulator of normal human blood T lymphocyte transendothelial migration: differential regulation by IFN-gamma and TNF-alpha. J Immunol 2002; 168:6420-8.
53. + T cells are increased in multiple sclerosis and their ligands MIP-1alpha and IP-10 are expressed in demyelinating brain lesions. Proc Natl Acad Sci U S A 1999; 96:6873-8.
54. Ransohoff RM, Hamilton TA, Tani M et al. Astrocyte expression of mRNA encoding cytokines IP-10 and JE/MCP-1 in experimental autoimmune encephalomyelitis. FASEB J 1993; 7:592-600.
55. Goddard S, Williams A, Morland C, Qin S, Gladue R, Hubscher SG, Adams DH. Differential expression of chemokines and chemokine receptors shapes the inflammatory response in rejecting human liver transplants. Transplantation 2001; 72:1957-67.
56. Buckley CD, Amft N, Bradfield PF et al. Persistent induction of the chemokine receptor CXCR4 by TGF-beta 1 on synovial T cells contributes to their accumulation within the rheumatoid synovium. J Immunol 2000; 165:3423-9.
57. Pablos JL, Santiago B, Galindo M, Torres C, Brehmer MT, Blanco FJ, Garcia-Lazaro FJ. Synoviocyte-derived CXCL12 is displayed on endothelium and induces angiogenesis in rheumatoid arthritis. J Immunol 2003; 170:2147-52.
58. Burman A, Haworth O, Hardie DL et al. A chemokine-dependent stromal induction mechanism for aberrant lymphocyte accumulation and compromised lymphatic return in rheumatoid arthritis. J Immunol 2005; 174:1693-700.
59. Wang S, Voisin MB, Larbi KY et al. Venular basement membranes contain specific matrix protein low expression regions that act as exit points for emigrating neutrophils. J Exp Med 2006; 203:1519-32.
60. Shiwen X, Rajkumar V, Denton CP, Leask A, Abraham DJ. Pericytes display increased CCN2 expression upon culturing. J Cell Commun Signal 2009; 3:61-4.
61. Crisan M, Yap S, Casteilla L et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 2008; 3:301-13.
62. + perivascular cells and fibroblasts. Exp Hematol 2008; 36:642-54.
63. Dore-Duffy P, Katychev A, Wang X, Van Buren E. CNS microvascular pericytes exhibit multipotential stem cell activity. J Cereb Blood Flow Metab 2006; 26:613-24.
64. Rajkumar VS, Howell K, Csiszar K, Denton CP, Black CM, Abraham DJ. Shared expression of phenotypic markers in systemic sclerosis indicates a convergence of pericytes and fibroblasts to a myofibroblast lineage in fibrosis. Arthritis Res Ther 2005; 7:R1113-23.
65. Traktuev DO, Merfeld-Clauss S, Li J et al. A population of multipotent CD34-positive adipose stromal cells share pericyte and mesenchymal surface markers, reside in a periendothelial location, and stabilize endothelial networks. Circ Res 2008; 102:77-85.
66. Sims DE. Diversity within pericytes. Clin Exp Pharmacol Physiol 2000; 27:842-6.
67. Kunz-Schughart LA, Schroeder JA, Wondrak M, Van Rey F, Lehle K, Hofstaedter F, Wheatley DN. Potential of fibroblasts to regulate the formation of three-dimensional vessel-like structures from endothelial cells in vitro. Am J Physiol Cell Physiol 2006; 290:C1385-98.
68. Oberringer M, Meins C, Bubel M, Pohlemann T. A new in vitro wound model based on the co-culture of human dermal microvascular endothelial cells and human dermal fibroblasts. Biol Cell 2007; 99:197-207.
69. Sorrell JM, Baber MA, Caplan AI. Human dermal fibroblast subpopulations; differential interactions with vascular endothelial cells in coculture: nonsoluble factors in the extracellular matrix influence interactions. Wound Repair Regen 2008; 16:300-9.
70. Liu H, Chen B, Lilly B. Fibroblasts potentiate blood vessel formation partially through secreted factor TIMP-1. Angiogenesis 2008; 11:223-34.
71. Martin P, Leibovich SJ. Inflammatory cells during wound repair: the good, the bad and the ugly. Trends Cell Biol 2005; 15:599-607.
72. Carlos TM. Leukocyte recruitment at sites of tumor: dissonant orchestration. J Leukoc Biol 2001; 70:171-84.
73. Firestein GS. Invasive fibroblast-like synoviocytes in rheumatoid arthritis. Passive responders or transformed aggressors?. Arthritis Rheum 1996; 39:1781-90.