The regulation of immune cell trafficking by the extracellular matrix

Current Opinion in Cell Biology

Volumn 36, Issue , 2015, Pages 54-61

  Hallmann, Rupert ^a   Zhang, Xueli ^a   Di Russo, Jacopo ^a   Li, Lixia ^a   Song, Jian ^a   Hannocks, Melanie Jane ^a   Sorokin, Lydia ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BASEMENT MEMBRANE; CELL MIGRATION; CELL STRUCTURE; EXTRACELLULAR MATRIX; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; IN VIVO STUDY; LEUKOCYTE MIGRATION; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; ANIMAL; CELL MOTION; IMMUNE SYSTEM; METABOLISM;

ANIMALS; BASEMENT MEMBRANE; CELL MOVEMENT; EXTRACELLULAR MATRIX; IMMUNE SYSTEM;

EID: 84937124634     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2015.06.006     Document Type: Review

References (51)

1. Hynes R.O. The extracellular matrix: not just pretty fibrils. Science 2009, 326:1216-1219.
2. Mouw J.K., Ou G., Weaver V.M. Extracellular matrix assembly: a multiscale deconstruction. Nat Rev Mol Cell Biol 2014, 15:771-785.
3. Kadler K.E., Hill A., Canty-Laird E.G. Collagen fibrillogenesis: fibronectin, integrins, and minor collagens as organizers and nucleators. Curr Opin Cell Biol 2008, 20:495-501.
4. Kalamajski S., Oldberg A. The role of small leucine-rich proteoglycans in collagen fibrillogenesis. Matrix Biol 2010, 29:248-253.
5. Schneiders F.I., Maertens B., Bose K., Li Y., Brunken W.J., Paulsson M., Smyth N., Koch M. Binding of netrin-4 to laminin short arms regulates basement membrane assembly. J Biol Chem 2007, 282:23750-23758.
6. Timpl R., Sasaki T., Kostka G., Chu M.L. Fibulins: a versatile family of extracellular matrix proteins. Nat Rev Mol Cell Biol 2003, 4:479-489.
7. Yan Q., Sage E.H. Sparc, a matricellular glycoprotein with important biological functions. J Histochem Cytochem 1999, 47:1495-1506.
8. Sasaki T., Larsson H., Tisi D., Claesson-Welsh L., Hohenester E., Timpl R. Endostatins derived from collagens XV and XVIII differ in structural and binding properties, tissue distribution and anti-angiogenic activity. J Mol Biol 2000, 301:1179-1190.
9. Bruckner P. Suprastructures of extracellular matrices: paradigms of functions controlled by aggregates rather than molecules. Cell Tissue Res 2010, 339:7-18.
10. Lokmic Z., Lammermann T., Sixt M., Cardell S., Hallmann R., Sorokin L. The extracellular matrix of the spleen as a potential organizer of immune cell compartments. Semin Immunol 2008, 20:4-13.
11. Kanchanawong P., Shtengel G., Pasapera A.M., Ramko E.B., Davidson M.W., Hess H.F., Waterman C.M. Nanoscale architecture of integrin-based cell adhesions. Nature 2010, 468:580-584.
12. Margadant C., Monsuur H.N., Norman J.C., Sonnenberg A. Mechanisms of integrin activation and trafficking. Curr Opin Cell Biol 2011, 23:607-614.
13. Huttenlocher A., Sandborg R.R., Horwitz A.F. Adhesion in cell migration. Curr Opin Cell Biol 1995, 7:697-706.
14. Scales T.M., Parsons M. Spatial and temporal regulation of integrin signalling during cell migration. Curr Opin Cell Biol 2011, 23:562-568.
15. 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.
16. Wolf K., Muller R., Borgmann S., Brocker E.B., Friedl P. Amoeboid shape change and contact guidance: T-lymphocyte crawling through fibrillar collagen is independent of matrix remodeling by MMPs and other proteases. Blood 2003, 102. 3269-3269.
17. Friedl P., Wolf K. Proteolytic and non-proteolytic migration of tumour cells and leucocytes. Biochem Soc Symp 2003,277-285.
18. Sabeh F., Shimizu-Hirota R., Weiss S.J. Protease-dependent versus -independent cancer cell invasion programs: three-dimensional amoeboid movement revisited. J Cell Biol 2009, 185:11-19.
19. Wolf K., Te Lindert M., Krause M., Alexander S., Te Riet J., Willis A.L., Hoffman R.M., Figdor C.G., Weiss S.J., Friedl P. Physical limits of cell migration: control by ECM space and nuclear deformation and tuning by proteolysis and traction force. J Cell Biol 2013, 201:1069-1084.
20. Renkawitz J., Schumann K., Weber M., Lammermann T., Pflicke H., Piel M., Polleux J., Spatz J.P., Sixt M. Adaptive force transmission in amoeboid cell migration. Nat Cell Biol 2009, 11:1438-1443.
21. Schiller H.B., Hermann M.R., Polleux J., Vignaud T., Zanivan S., Friedel C.C., Sun Z., Raducanu A., Gottschalk K.E., Thery M., Mann M., et al. Beta1- and alphav-class integrins cooperate to regulate myosin II during rigidity sensing of fibronectin-based microenvironments. Nat Cell Biol 2013, 15:625-636.
22. Swift J., Ivanovska I.L., Buxboim A., Harada T., Dingal P.C., Pinter J., Pajerowski J.D., Spinler K.R., Shin J.W., Tewari M., Rehfeldt F., et al. Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation. Science 2013, 341:1240104.
23. Harada T., Swift J., Irianto J., Shin J.W., Spinler K.R., Athirasala A., Diegmiller R., Dingal P.C., Ivanovska I.L., Discher D.E. Nuclear lamin stiffness is a barrier to 3D migration, but softness can limit survival. J Cell Biol 2014, 204:669-682.
24. Buxboim A., Swift J., Irianto J., Spinler K.R., Dingal P.C., Athirasala A., Kao Y.R., Cho S., Harada T., Shin J.W., Discher D.E. Matrix elasticity regulates lamin-A,C phosphorylation and turnover with feedback to actomyosin. Curr Biol 2014, 24:1909-1917.
25. Senior R.M., Gresham H.D., Griffin G.L., Brown E.J., Chung A.E. Entactin stimulates neutrophil adhesion and chemotaxis through interactions between its arg-gly-asp (RGD) domain and the leukocyte response integrin. J Clin Invest 1992, 90:2251-2257.
26. Adair-Kirk T.L., Atkinson J.J., Broekelmann T.J., Doi M., Tryggvason K., Miner J.H., Mecham R.P., Senior R.M. A site on laminin alpha 5, aqarsaaskvkvsmkf, induces inflammatory cell production of matrix metalloproteinase-9 and chemotaxis. J Immunol 2003, 171:398-406.
27. Heck L.W., Blackburn W.D., Irwin M.H., Abrahamson D.R. Degradation of basement membrane laminin by human neutrophil elastase and cathepsin g. Am J Pathol 1990, 136:1267-1274.
28. Pipoly D.J., Crouch E.C. Degradation of native type iv procollagen by human neutrophil elastase. Implications for leukocyte-mediated degradation of basement membranes. Biochemistry 1987, 26:5748-5754.
29. Huber A.R., Weiss S.J. Disruption of the subendothelial basement membrane during neutrophil diapedesis in an in vitro construct of a blood vessel wall. J Clin Invest 1989, 83:1122-1136.
30. Agrawal S., Anderson P., Durbeej M., van Rooijen N., Ivars F., Opdenakker G., Sorokin L.M. Dystroglycan is selectively cleaved at the parenchymal basement membrane at sites of leukocyte extravasation in experimental autoimmune encephalomyelitis. J Exp Med 2006, 203:1007-1019.
31. Marchesi V.T., Florey H.W. Electron micrographic observations on the emigration of leucocytes. Q J Exp Physiol Cogn Med Sci 1960, 45:343-348.
32. Burns A.R., Smith C.W., Walker D.C. Unique structural features that influence neutrophil emigration into the lung. Physiol Rev 2003, 83:309-336.
33. Huber A.R., Kunkel S.L., Todd R.F., Weiss S.J. Regulation of transendothelial neutrophil migration by endogenous interleukin-8. Science 1991, 254:99-102.
34. McKee K.K., Capizzi S., Yurchenco P.D. Scaffold-forming and adhesive contributions of synthetic laminin-binding proteins to basement membrane assembly. J Biol Chem 2009, 284:8984-8994.
35. McKee K.K., Harrison D., Capizzi S., Yurchenco P.D. Role of laminin terminal globular domains in basement membrane assembly. J Biol Chem 2007, 282:21437-21447.
36. Hohenester E., Yurchenco P.D. Laminins in basement membrane assembly. Cell Adh Migr 2013, 7:56-63.
37. Hynes R.O. Stretching the boundaries of extracellular matrix research. Nat Rev Mol Cell Biol 2014, 15:761-763.
38. 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. J Exp Med 2006, 203:1519-1532.
39. Hagedorn E.J., Ziel J.W., Morrissey M.A., Linden L.M., Wang Z., Chi Q., Johnson S.A., Sherwood D.R. The netrin receptor DCC focuses invadopodia-driven basement membrane transmigration in vivo. J Cell Biol 2013, 201:903-913.
40. Hiramatsu R., Matsuoka T., Kimura-Yoshida C., Han S.W., Mochida K., Adachi T., Takayama S., Matsuo I. External mechanical cues trigger the establishment of the anterior-posterior axis in early mouse embryos. Dev Cell 2013, 27:131-144.
41. Sixt M., Engelhardt B., Pausch F., Hallmann R., Wendler O., Sorokin L.M. Endothelial cell laminin isoforms, laminin 8 and 10, play decisive roles in in t-cell recruitment across the blood-brain-barrier in an experimental autoimmune encephalitis model (EAE). J Cell Biol 2001, 153:933-945.
42. Wu C., Ivars F., Anderson P., Hallmann R., Vestweber D., Nilsson P., Robenek H., Tryggvason K., Song J., Korpos E., Loser K., et al. Endothelial basement membrane laminin alpha5 selectively inhibits T lymphocyte extravasation into the brain. Nat Med 2009, 15:519-527.
43. Masocha W., Robertson B., Rottenberg M.E., Mhlanga J., Sorokin L., Kristensson K. Cerebral vessel laminins and IFN-gamma define trypanosoma brucei brucei penetration of the blood-brain barrier. J Clin Invest 2004, 114:689-694.
44. Hallmann R., Horn N., Selg M., Wendler O., Pausch F., Sorokin L.M. Expression and function of laminins in the embryonic and mature vasculature. Physiol Rev 2005, 85:979-1000.
45. Kenne E., Soehnlein O., Genov G., Rotzius P., Eriksson E.E., Lindbom L. Immune cell recruitment to inflammatory loci is impaired in mice deficient in basement membrane protein laminin {alpha}4. J Leukoc Biol 2010.
46. Shulman Z., Shinder V., Klein E., Grabovsky V., Yeger O., Geron E., Montresor A., Bolomini-Vittori M., Feigelson S.W., Kirchhausen T., Laudanna C., et al. Lymphocyte crawling and transendothelial migration require chemokine triggering of high-affinity LFA-1 integrin. Immunity 2009, 30:384-396.
47. Voisin M.B., Woodfin A., Nourshargh S. Monocytes and neutrophils exhibit both distinct and common mechanisms in penetrating the vascular basement membrane in vivo. Arterioscler Thromb Vasc Biol 2009, 29:1193-1199.
48. Song J., Wu C., Korpos E., Zhang X., Agrawal S.M., Wang Y., Faber C., Schafers M., Korner H., Opdenakker G., Hallmann R., et al. Focal MMP-2 and MMP-9 activity at the blood-brain barrier promotes chemokine-induced leukocyte migration. Cell Rep 2015, 10:1040-1054.
49. Korpos E., Kadri N., Kappelhoff R., Wegner J., Overall C.M., Weber E., Holmberg D., Cardell S., Sorokin L. The peri-islet basement membrane, a barrier to infiltrating leukocytes in type 1 diabetes in mouse and human. Diabetes 2013, 62:531-542.
50. Sorokin L. The impact of the extracellular matrix on inflammation. Nat Rev Immunol 2010, 10:712-723.
51. Durbeej M. Laminins. Cell Tissue Res 2010, 339:259-268.