Intraluminal crawling versus interstitial neutrophil migration during inflammation

Molecular Immunology

Volumn 55, Issue 1, 2013, Pages 70-75

  Pick, Robert ^a   Brechtefeld, Doris ^a   Walzog, Barbara ^a  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

Author keywords

Inflammation; Integrins; Migration; Neutrophil; Signal transduction

Indexed keywords

CD11B ANTIGEN; CD18 ANTIGEN; GLYCOPROTEIN P 15095; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1;

CELL ADHESION; CELL FUNCTION; EXTRACELLULAR MATRIX; GRANULOCYTE; IN VIVO STUDY; INFLAMMATION; LEUKOCYTE MIGRATION; LEUKOCYTE MOTILITY; NEUTROPHIL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW;

ANIMALS; CELL ADHESION; CELL MOVEMENT; CHEMOTAXIS, LEUKOCYTE; EXTRACELLULAR FLUID; HUMANS; IMMUNE SYSTEM DISEASES; INFLAMMATION; LEUKOCYTE DISORDERS; MODELS, BIOLOGICAL; NEUTROPHILS; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

EID: 84875577658     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2012.12.008     Document Type: Review

References (84)

1. Abram C.L., Lowell C.A. The ins and outs of leukocyte integrin signaling. Annual Review of Immunology 2009, 27:339-362.
2. Anderson D.C., Schmalsteig F.C., Finegold M.J., Hughes B.J., Rothlein R., Miller L.J., Kohl S., Tosi M.F., Jacobs R.L., Waldrop T.C., et al. The severe and moderate phenotypes of heritable Mac-1, LFA-1 deficiency: their quantitative definition and relation to leukocyte dysfunction and clinical features. Journal of Infectious Diseases 1985, 152:668-689.
3. Borregaard N. Neutrophils, from marrow to microbes. Immunity 2010, 33:657-670.
4. Bowen T.J., Ochs H.D., Altman L.C., Price T.H., Van Epps D.E., Brautigan D.L., Rosin R.E., Perkins W.D., Babior B.M., Klebanoff S.J., Wedgwood R.J. Severe recurrent bacterial infections associated with defective adherence and chemotaxis in two patients with neutrophils deficient in a cell-associated glycoprotein. Journal of Pediatrics 1982, 101:932-940.
5. Carman C.V., Springer T.A. Integrin avidity regulation: are changes in affinity and conformation underemphasized?. Current Opinion in Cell Biology 2003, 15:547-556.
6. Carman C.V., Springer T.A. Trans-cellular migration: cell-cell contacts get intimate. Current Opinion in Cell Biology 2008, 20:533-540.
7. Chen G.Y., Nunez G. Sterile inflammation: sensing and reacting to damage. Nature Reviews Immunology 2010, 10:826-837.
8. Chesnutt B.C., Smith D.F., Raffler N.A., Smith M.L., White E.J., Ley K. Induction of LFA-1-dependent neutrophil rolling on ICAM-1 by engagement of E-selectin. Microcirculation 2006, 13:99-109.
9. Coxon A., Rieu P., Barkalow F.J., Askari S., Sharpe A.H., von Andrian U.H., Arnaout M.A., Mayadas T.N. A novel role for the beta 2 integrin CD11b/CD18 in neutrophil apoptosis: a homeostatic mechanism in inflammation. Immunity 1996, 5:653-666.
10. Deckert M., Tartare-Deckert S., Couture C., Mustelin T., Altman A. Functional and physical interactions of Syk family kinases with the Vav proto-oncogene product. Immunity 1996, 5:591-604.
11. Devreotes P.N., Zigmond S.H. Chemotaxis in eukaryotic cells: a focus on leukocytes and dictyostelium. Annual Review of Cell Biology 1988, 4:649-686.
12. Ding Z.M., Babensee J.E., Simon S.I., Lu H., Perrard J.L., Bullard D.C., Dai X.Y., Bromley S.K., Dustin M.L., Entman M.L., Smith C.W., Ballantyne C.M. Relative contribution of LFA-1 and Mac-1 to neutrophil adhesion and migration. Journal of Immunology 1999, 163:5029-5038.
13. Dixit N., Yamayoshi I., Nazarian A., Simon S.I. Migrational guidance of neutrophils is mechanotransduced via high-affinity LFA-1 and calcium flux. Journal of Immunology 2011, 187:472-481.
14. Evans R., Patzak I., Svensson L., De Filippo K., Jones K., McDowall A., Hogg N. Integrins in immunity. Journal of Cell Science 2009, 122:215-225.
15. Foxman E.F., Campbell J.J., Butcher E.C. Multistep navigation and the combinatorial control of leukocyte chemotaxis. Journal of Cell Biology 1997, 139:1349-1360.
16. Friedl P., Weigelin B. Interstitial leukocyte migration and immune function. Nature Immunology 2008, 9:960-969.
17. Frommhold D., Mannigel I., Schymeinsky J., Mocsai A., Poeschl J., Walzog B., Sperandio M. Spleen tyrosine kinase Syk is critical for sustained leukocyte adhesion during inflammation in vivo. BMC Immunology 2007, 8:31.
18. Furze R.C., Rankin S.M. The role of the bone marrow in neutrophil clearance under homeostatic conditions in the mouse. FASEB Journal 2008, 22:3111-3119.
19. Gakidis M.A., Cullere X., Olson T., Wilsbacher J.L., Zhang B., Moores S.L., Ley K., Swat W., Mayadas T., Brugge J.S. Vav GEFs are required for beta2 integrin-dependent functions of neutrophils. Journal of Cell Biology 2004, 166:273-282.
20. Germain R.N., Robey E.A., Cahalan M.D. A decade of imaging cellular motility and interaction dynamics in the immune system. Science 2012, 336:1676-1681.
21. Goldman D.W., Chang F.H., Gifford L.A., Goetzl E.J., Bourne H.R. Pertussis toxin inhibition of chemotactic factor-induced calcium mobilization and function in human polymorphonuclear leukocytes. Journal of Experimental Medicine 1985, 162:145-156.
22. Groesch T.D., Zhou F., Mattila S., Geahlen R.L., Post C.B. Structural basis for the requirement of two phosphotyrosine residues in signaling mediated by Syk tyrosine kinase. Journal of Molecular Biology 2006, 356:1222-1236.
23. Hepper I., Schymeinsky J., Weckbach L.T., Jakob S.M., Frommhold D., Sixt M., Laschinger M., Sperandio M., Walzog B. The mammalian actin-binding protein 1 is critical for spreading and intraluminal crawling of neutrophils under flow conditions. Journal of Immunology 2012, 188:4590-4601.
24. Hirsch E., Katanaev V.L., Garlanda C., Azzolino O., Pirola L., Silengo L., Sozzani S., Mantovani A., Altruda F., Wymann M.P. Central role for G protein-coupled phosphoinositide 3-kinase gamma in inflammation. Science 2000, 287:1049-1053.
25. Ionita M.G., van den Borne P., Catanzariti L.M., Moll F.L., de Vries J.P., Pasterkamp G., Vink A., de Kleijn D.P. High neutrophil numbers in human carotid atherosclerotic plaques are associated with characteristics of rupture-prone lesions. Arteriosclerosis, Thrombosis, and Vascular Biology 2010, 30:1842-1848.
26. Jakus Z., Simon E., Frommhold D., Sperandio M., Mocsai A. Critical role of phospholipase Cgamma2 in integrin and Fc receptor-mediated neutrophil functions and the effector phase of autoimmune arthritis. Journal of Experimental Medicine 2009, 206:577-593.
27. Kuwano Y., Spelten O., Zhang H., Ley K., Zarbock A. Rolling on E- or P-selectin induces the extended but not high-affinity conformation of LFA-1 in neutrophils. Blood 2010, 116:617-624.
28. Lammermann T., Bader B.L., Monkley S.J., Worbs T., Wedlich-Soldner R., Hirsch K., Keller M., Forster R., Critchley D.R., Fassler R., Sixt M. Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature 2008, 453:51-55.
29. Larbolette O., Wollscheid B., Schweikert J., Nielsen P.J., Wienands J. SH3P7 is a cytoskeleton adapter protein and is coupled to signal transduction from lymphocyte antigen receptors. Molecular and Cellular Biology 1999, 19:1539-1546.
30. Law C.L., Chandran K.A., Sidorenko S.P., Clark E.A. Phospholipase C-gamma1 interacts with conserved phosphotyrosyl residues in the linker region of Syk and is a substrate for Syk. Molecular and Cellular Biology 1996, 16:1305-1315.
31. Lefort C.T., Ley K. Neutrophil arrest by LFA-1 activation. Frontiers in Immunology 2012, 3:157.
32. Ley K., Laudanna C., Cybulsky M.I., Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nature Reviews Immunology 2007, 7:678-689.
33. Luo B.H., Carman C.V., Springer T.A. Structural basis of integrin regulation and signaling. Annual Review of Immunology 2007, 25:619-647.
34. Martin C., Burdon P.C., Bridger G., Gutierrez-Ramos J.C., Williams T.J., Rankin S.M. Chemokines acting via CXCR2 and CXCR4 control the release of neutrophils from the bone marrow and their return following senescence. Immunity 2003, 19:583-593.
35. Massena S., Christoffersson G., Hjertstrom E., Zcharia E., Vlodavsky I., Ausmees N., Rolny C., Li J.P., Phillipson M. A chemotactic gradient sequestered on endothelial heparan sulfate induces directional intraluminal crawling of neutrophils. Blood 2010, 116:1924-1931.
36. McDonald B., Pittman K., Menezes G.B., Hirota S.A., Slaba I., Waterhouse C.C., Beck P.L., Muruve D.A., Kubes P. Intravascular danger signals guide neutrophils to sites of sterile inflammation. Science 2010, 330:362-366.
37. Megens R.T., Kemmerich K., Pyta J., Weber C., Soehnlein O. Intravital imaging of phagocyte recruitment. Thrombosis and Haemostasis 2011, 105:802-810.
38. Mocsai A., Abram C.L., Jakus Z., Hu Y., Lanier L.L., Lowell C.A. Integrin signaling in neutrophils and macrophages uses adaptors containing immunoreceptor tyrosine-based activation motifs. Nature Immunology 2006, 7:1326-1333.
39. Mocsai A., Ruland J., Tybulewicz V.L. The SYK tyrosine kinase: a crucial player in diverse biological functions. Nature Reviews Immunology 2010, 10:387-402.
40. Mocsai A., Zhou M., Meng F., Tybulewicz V.L., Lowell C.A. Syk is required for integrin signaling in neutrophils. Immunity 2002, 16:547-558.
41. Moon K.D., Post C.B., Durden D.L., Zhou Q., De P., Harrison M.L., Geahlen R.L. Molecular basis for a direct interaction between the Syk protein-tyrosine kinase and phosphoinositide 3-kinase. Journal of Biological Chemistry 2005, 280:1543-1551.
42. Moser M., Legate K.R., Zent R., Fassler R. The tail of integrins, talin, and kindlins. Science 2009, 324:895-899.
43. Nathan C. Neutrophils and immunity: challenges and opportunities. Nature Reviews Immunology 2006, 6:173-182.
44. Nemeth T., Mocsai A. The role of neutrophils in autoimmune diseases. Immunology Letters 2012, 143:9-19.
45. Nishida N., Xie C., Shimaoka M., Cheng Y., Walz T., Springer T.A. Activation of leukocyte beta2 integrins by conversion from bent to extended conformations. Immunity 2006, 25:583-594.
46. Nourshargh S., Hordijk P.L., Sixt M. Breaching multiple barriers: leukocyte motility through venular walls and the interstitium. Nature Reviews Molecular Cell Biology 2010, 11:366-378.
47. Phillipson M., Heit B., Colarusso P., Liu L., Ballantyne C.M., Kubes P. Intraluminal crawling of neutrophils to emigration sites: a molecularly distinct process from adhesion in the recruitment cascade. Journal of Experimental Medicine 2006, 203:2569-2575.
48. Phillipson M., Heit B., Parsons S.A., Petri B., Mullaly S.C., Colarusso P., Gower R.M., Neely G., Simon S.I., Kubes P. Vav1 is essential for mechanotactic crawling and migration of neutrophils out of the inflamed microvasculature. Journal of Immunology 2009, 182:6870-6878.
49. Phillipson M., Kubes P. The neutrophil in vascular inflammation. Nature Medicine 2011, 17:1381-1390.
50. Pillay J., den Braber I., Vrisekoop N., Kwast L.M., de Boer R.J., Borghans J.A., Tesselaar K., Koenderman L. In vivo labeling with 2H2O reveals a human neutrophil lifespan of 5.4 days. Blood 2010, 116:625-627.
51. Pillay J., Kamp V.M., van Hoffen E., Visser T., Tak T., Lammers J.W., Ulfman L.H., Leenen L.P., Pickkers P., Koenderman L. A subset of neutrophils in human systemic inflammation inhibits T cell responses through Mac-1. Journal of Clinical Investigation 2012, 122:327-336.
52. Proebstl D., Voisin M.B., Woodfin A., Whiteford J., D'Acquisto F., Jones G.E., Rowe D., Nourshargh S. Pericytes support neutrophil subendothelial cell crawling and breaching of venular walls in vivo. Journal of Experimental Medicine 2012, 209:1219-1234.
53. Puga I., Cols M., Barra C.M., He B., Cassis L., Gentile M., Comerma L., Chorny A., Shan M., Xu W., Magri G., Knowles D.M., Tam W., Chiu A., Bussel J.B., Serrano S., Lorente J.A., Bellosillo B., Lloreta J., Juanpere N., Alameda F., Baro T., de Heredia C.D., Toran N., Catala A., Torrebadell M., Fortuny C., Cusi V., Carreras C., Diaz G.A., Blander J.M., Farber C.M., Silvestri G., Cunningham-Rundles C., Calvillo M., Dufour C., Notarangelo L.D., Lougaris V., Plebani A., Casanova J.L., Ganal S.C., Diefenbach A., Arostegui J.I., Juan M., Yague J., Mahlaoui N., Donadieu J., Chen K., Cerutti A. B cell-helper neutrophils stimulate the diversification and production of immunoglobulin in the marginal zone of the spleen. Nature Immunology 2012, 13:170-180.
54. Renkawitz J., Sixt M. Mechanisms of force generation and force transmission during interstitial leukocyte migration. EMBO Reports 2010, 11:744-750.
55. Sadhu C., Masinovsky B., Dick K., Sowell C.G., Staunton D.E. Essential role of phosphoinositide 3-kinase delta in neutrophil directional movement. Journal of Immunology 2003, 170:2647-2654.
56. Sasaki T., Irie-Sasaki J., Jones R.G., Oliveira-dos-Santos A.J., Stanford W.L., Bolon B., Wakeham A., Itie A., Bouchard D., Kozieradzki I., Joza N., Mak T.W., Ohashi P.S., Suzuki A., Penninger J.M. Function of PI3Kgamma in thymocyte development, T cell activation, and neutrophil migration. Science 2000, 287:1040-1046.
57. Saverymuttu S.H., Peters A.M., Keshavarzian A., Reavy H.J., Lavender J.P. The kinetics of 111indium distribution following injection of 111indium labelled autologous granulocytes in man. British Journal of Haematology 1985, 61:675-685.
58. Schulte D., Kuppers V., Dartsch N., Broermann A., Li H., Zarbock A., Kamenyeva O., Kiefer F., Khandoga A., Massberg S., Vestweber D. Stabilizing the VE-cadherin-catenin complex blocks leukocyte extravasation and vascular permeability. EMBO Journal 2011, 30:4157-4170.
59. Schymeinsky J., Gerstl R., Mannigel I., Niedung K., Frommhold D., Panthel K., Heesemann J., Sixt M., Quast T., Kolanus W., Mocsai A., Wienands J., Sperandio M., Walzog B. A fundamental role of mAbp1 in neutrophils: impact on beta(2) integrin-mediated phagocytosis and adhesion in vivo. Blood 2009, 114:4209-4220.
60. Schymeinsky J., Mocsai A., Walzog B. Neutrophil activation via beta2 integrins (CD11/CD18): molecular mechanisms and clinical implications. Thrombosis and Haemostasis 2007, 98:262-273.
61. Schymeinsky J., Sindrilaru A., Frommhold D., Sperandio M., Gerstl R., Then C., Mocsai A., Scharffetter-Kochanek K., Walzog B. The Vav binding site of the non-receptor tyrosine kinase Syk at Tyr 348 is critical for beta2 integrin (CD11/CD18)-mediated neutrophil migration. Blood 2006, 108:3919-3927.
62. Schymeinsky J., Then C., Sindrilaru A., Gerstl R., Jakus Z., Tybulewicz V.L., Scharffetter-Kochanek K., Walzog B. Syk-mediated translocation of PI3Kdelta to the leading edge controls lamellipodium formation and migration of leukocytes. PLoS ONE 2007, 2:e1132.
63. Schymeinsky J., Then C., Walzog B. The non-receptor tyrosine kinase Syk regulates lamellipodium formation and site-directed migration of human leukocytes. Journal of Cellular Physiology 2005, 204:614-622.
64. Servant G., Weiner O.D., Herzmark P., Balla T., Sedat J.W., Bourne H.R. Polarization of chemoattractant receptor signaling during neutrophil chemotaxis. Science 2000, 287:1037-1040.
65. Servant G., Weiner O.D., Neptune E.R., Sedat J.W., Bourne H.R. Dynamics of a chemoattractant receptor in living neutrophils during chemotaxis. Molecular Biology of the Cell 1999, 10:1163-1178.
66. Shi J., Fujieda H., Kokubo Y., Wake K. Apoptosis of neutrophils and their elimination by Kupffer cells in rat liver. Hepatology 1996, 24:1256-1263.
67. Simon S.I., Green C.E. Molecular mechanics and dynamics of leukocyte recruitment during inflammation. Annual Review of Biomedical Engineering 2005, 7:151-185.
68. Smith C.W., Marlin S.D., Rothlein R., Toman C., Anderson D.C. Cooperative interactions of LFA-1 and Mac-1 with intercellular adhesion molecule-1 in facilitating adherence and transendothelial migration of human neutrophils in vitro. Journal of Clinical Investigation 1989, 83:2008-2017.
69. Smith C.W., Rothlein R., Hughes B.J., Mariscalco M.M., Rudloff H.E., Schmalstieg F.C., Anderson D.C. Recognition of an endothelial determinant for CD 18-dependent human neutrophil adherence and transendothelial migration. Journal of Clinical Investigation 1988, 82:1746-1756.
70. Soehnlein O. Multiple roles for neutrophils in atherosclerosis. Circulation Research 2012, 110:875-888.
71. Suire S., Condliffe A.M., Ferguson G.J., Ellson C.D., Guillou H., Davidson K., Welch H., Coadwell J., Turner M., Chilvers E.R., Hawkins P.T., Stephens L. Gbetagammas and the Ras binding domain of p110gamma are both important regulators of PI(3)Kgamma signalling in neutrophils. Nature Cell Biology 2006, 8:1303-1309.
72. Summers C., Rankin S.M., Condliffe A.M., Singh N., Peters A.M., Chilvers E.R. Neutrophil kinetics in health and disease. Trends in Immunology 2010, 31:318-324.
73. Sundd P., Gutierrez E., Koltsova E.K., Kuwano Y., Fukuda S., Pospieszalska M.K., Groisman A., Ley K. 'Slings' enable neutrophil rolling at high shear. Nature 2012, 488:399-403.
74. Takeuchi O., Akira S. Pattern recognition receptors and inflammation. Cell 2010, 140:805-820.
75. Van Haastert P.J., Devreotes P.N. Chemotaxis: signalling the way forward. Nature Reviews Molecular Cell Biology 2004, 5:626-634.
76. Walzog B., Offermanns S., Zakrzewicz A., Gaehtgens P., Ley K. Beta2 integrins mediate protein tyrosine phosphorylation in human neutrophils. Journal of Leukocyte Biology 1996, 59:747-753.
77. Walzog B., Scharffetter-Kochanek K., Gaehtgens P. Impairment of neutrophil emigration in CD18-null mice. American Journal of Physiology 1999, 276:G1125-G1130.
78. Wang F., Herzmark P., Weiner O.D., Srinivasan S., Servant G., Bourne H.R. Lipid products of PI(3)Ks maintain persistent cell polarity and directed motility in neutrophils. Nature Cell Biology 2002, 4:513-518.
79. Wang S., Voisin M.B., Larbi K.Y., Dangerfield J., Scheiermann C., Tran M., Maxwell P.H., Sorokin L., Nourshargh S. Venular basement membranes contain specific matrix protein low expression regions that act as exit points for emigrating neutrophils. Journal of Experimental Medicine 2006, 203:1519-1532.
80. Willeke T., Schymeinsky J., Prange P., Zahler S., Walzog B. A role for Syk-kinase in the control of the binding cycle of the beta2 integrins (CD11/CD18) in human polymorphonuclear neutrophils. Journal of Leukocyte Biology 2003, 74:260-269.
81. Woodfin A., Voisin M.B., Beyrau M., Colom B., Caille D., Diapouli F.M., Nash G.B., Chavakis T., Albelda S.M., Rainger G.E., Meda P., Imhof B.A., Nourshargh S. The junctional adhesion molecule JAM-C regulates polarized transendothelial migration of neutrophils in vivo. Nature Immunology 2011, 12:761-769.
82. Wright S.D., Weitz J.I., Huang A.J., Levin S.M., Silverstein S.C., Loike J.D. Complement receptor type three (CD11b/CD18) of human polymorphonuclear leukocytes recognizes fibrinogen. Proceedings of the National Academy of Sciences of the United States of America 1988, 85:7734-7738.
83. Xu J., Wang F., Van Keymeulen A., Herzmark P., Straight A., Kelly K., Takuwa Y., Sugimoto N., Mitchison T., Bourne H.R. Divergent signals and cytoskeletal assemblies regulate self-organizing polarity in neutrophils. Cell 2003, 114:201-214.
84. Zarbock A., Lowell C.A., Ley K. Spleen tyrosine kinase Syk is necessary for E-selectin-induced alpha(L)beta(2) integrin-mediated rolling on intercellular adhesion molecule-1. Immunity 2007, 26:773-783.