Mature Human Thymocytes Migrate on Laminin-5 with Activation of Metalloproteinase-14 and Cleavage of CD44

Journal of Immunology

Volumn 172, Issue 3, 2004, Pages 1397-1406

  Vivinus Nebot, Mylène ^a,b   Rousselle, Patricia ^c   Breittmayer, Jean Philippe ^a   Cenciarini, Claire ^a   Berrih Aknin, Sonia ^d   Spong, Suzanne ^e   Nokelainen, Pasi ^e   Cottrez, Françoise ^a   Marinkovich, M Peter ^f   Bernard, Alain ^a,b,g  

^a INSERM   (France)

^b UNIVERSITY HOSPITAL OF NICE   (France)

^c INSTITUT DE BIOLOGIE ET CHIMIE DES PROTÉINES   (France)

^d CNRS   (France)

^e FIBROGEN INC   (United States)

^f STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g CENTRE HOSPITALIER UNIVERSITAIRE DE NICE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HERMES ANTIGEN; INTEGRIN RECEPTOR; KALININ; METALLOPROTEINASE; METALLOPROTEINASE 14; MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG;

ARTICLE; CELL INTERACTION; CELL MIGRATION; CELL SURFACE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IMMUNOADSORPTION; IN VITRO STUDY; INFANT; LYMPHOCYTE MIGRATION; MOLECULAR BIOLOGY; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; SUPERNATANT; THYMOCYTE; UPREGULATION;

EID: 9144231190     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.172.3.1397     Document Type: Article

References (75)

1. Wu, L., F. Livak, and H. T. Petrie. 1998. Molecular Biology of B-Cell and T-Cell Development. J. G. Monroe and E. V. Rothenberg, eds. Humana, Totowa, p. 235.
2. Savagner, P., B. Imhof, K. M. Yamada, and J. P. Thiery. 1986. Homing of hemopoietic precursor cells to the embryonic thymus: characterization of an invasive mechanism induced by chemotactic peptides. J. Cell Biol. 103:2715.
3. van Ewijk, W. 1991. T-cell differentiation is influenced by thymic microenvironments. Annu. Rev. Immunol. 9:591.
4. Dunon, D., and B. A. Imhof. 1993. Mechanisms of thymus horning. Blood 81:1.
5. Scollay, R., and D. I. Godfrey. 1995. Thymic emigration: conveyor belts or lucky dips? Immunol. Today 16:268.
6. Wilkinson, B., J. J. Owen. and E. J. Jenkinson. 1999. Factors regulating stem cell recruitment to the fetal thymus. J. Immunol. 162:3873.
7. Lind, E. F., S. E. Prockop, H. E. Porritt, and H. T. Petrie. 2001. Mapping precursor movement through the postnatal thymus reveals specific microenvironments supporting defined stages of early lymphoid development. J. Exp. Med. 194:127.
8. Ueno, T., K. Hara, M. Swope Willis, U. E. Höpken, D. H. D. Gray, K. Matsushima, M. Lipp, T. A. Springer, R. L. Boyd, O. Yoshie, and Y. Takahama. 2002. Role of CCR7 ligands in the emigration of newly generated T lymphocytes from the neonatal thymus. Immunity 16:205.
9. Vieira, J. L., L. R. de Souza, and W. Savino. 1994. Conceptual aspects of the thymic microenvironment. Immunol. Today 15:192.
10. Savino, W., A. Mendes-da-Cruz, J. S. Silva, M. Dardenne, and V. Cotta-de-Almeida. 2002. Intrathymic T-cell migration: a combinatorial interplay of extracellular matrix and chemokines? Trends Immunol. 23:305.
11. Tanchot, C., and B. Rocha. 1997. Peripheral selection of T cell repertoires: the role of continuous thymus output. J. Exp. Med. 186:1099.
12. Berzins, S. P., R. L. Boyd, and J. F. A. P. Miller. 1998. The role of the thymus and recent thymic emigrants in the maintenance of the adult peripheral lymphocyte pool. J. Exp. Med. 187:1839.
13. Berzins, S. P., D. I. Godfrey, J. F. A. P. Miller, and R. L. Boyd. 1999. A central role for thymic emigrants in peripheral T cell homeostasis. Proc. Natl. Acad. Sci. USA 96:9787.
14. Poulin, J. F., M. N. Viswanathan, J. M. Harris, K. V. Komanduri, E. Wieder, N. Ringuette, M. Jenkins, J. M. McCune, and R. P. Sekaly. 1999. Direct evidence for thymic function in adult humans. J. Exp. Med. 190:479.
15. Almeida, A. R., J. A. Borghans, and A. A. Freitas. 2001. T cell homeostasis: thymus regeneration and peripheral T cell restoration in mice with a reduced fraction of competent precursors. J. Exp. Med. 194:591.
16. Poznansky, M. C., I. T. Olszak. R. H. Evans, Z. Wang, R. B. Foxall, D. P. Olson, K. Weibrecht, A. D. Luster. and D. T. Scadden. 2002. Thymocyte emigration is mediated by active movement away from stroma-derived factors. J. Clin. Invest. 109:1101.
17. Petrie, H. T. 2002. Role of thymic organ structure and stromal composition in steady-state post-natal T-cell production. Immunol. Rev. 189:8.
18. Burgeson, R. E., M. Chiquet, R. Deutzmann, P. Ekblom, J. Engel, H. Kleinman, G. R. Martin, G. Meneguzzi, M. Paulsson, J. Sanes, et al. 1994. A new nomenclature for the laminins. Marix Biol. 14:209.
19. Ryan, M. C., A. M. Christiano, E. Engvall, U. M. Wewer, J. H. Miner, J. R. Sanes. and R. E. Burgeson. 1996. The functions of laminins: lessons from in vivo studies. Matrix Biol. 15:369.
20. Patel, D. D., L. P. Whichard, G. Radcliff, S. M. Denning, and B. F. Haynes. 1995. Characterization of human thymic epithelial cell surface antigens: phenotypic similarity of thymic epithelial cells to epidermal keratinocytes. J. Clin. Immunol. 15:80.
21. Kallunki, P., K. Sainio, R. Eddy, M. Byers, T. Kallunki, H. Sariola, K. Beck, H. Hirvonen, T. B. Shows, and K. Tryggvason. 1992. A truncated laminin chain homologous to the B2 chain: structure, spatial expression, and chromosomal assignments. J. Cell Biol. 119:679.
22. Virtanen, I., J. Lohi, T. Tani, H. Sariola, R. E. Burgeson, and V. P. Lehto. 1996. Laminin chains in the basement membranes of human thymus. Histochem. J. 28:643.
23. 4 integrins. J. Cell Biol. 144:563.
24. Kim, M. G., G. Lee, S. K. Lee, M. Lolkema, J. Yim, S. H. Hong, and R. H. Schwartz. 2000. Epithelial cell-specific laminin 5 is required for survival of early thymocytes. J. Immunol. 165:192.
25. 4/bullous pemphigoid antigen in a new stable anchoring contact (SAC) of keratinocytes: relation to hemidesmosomes. J. Cell Biol. 111:3141.
26. Miyazaki, K., Y. Kikkawa, A. Nakamura, H. Yusumitsu, and M. Umeda. 1993. A large cell-adhesive scatter factor secreted by human gastric carcinoma cells. Proc. Natl. Acad. Sci. USA 90:11767.
27. Giannelli, G., J. Falk-Marzillier, O. Schiraldi, W. G. Stetler-Stevenson, and V. Quantara. 1997. Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5. Science 277:225.
28. Koshikawa, N., G. Giannelli, V. Cirulli, K. Miyazaki, and V. Quaranta. 2000. Role of cell surface metalloprotease MTI-MMP in epithelial cell migration over laminin-5. J. Cell Biol. 148:615.
29. Amano, S., I. C. Scott, K. Takahara, M. Koch, M. F. Champliaud, D. R. Gerecke, D. R. Keene, D. L. Hudson, T. Nishiyama. S. Lee, et al. 2000. Bone morphogenetic protein 1 is an extracellular processing enzyme of the laminin-5 γ2 chain. J. Biol. Chem. 275:22728.
30. Sasaki, T., W. Gohring, K. Mann, C. Brakebusch, Y. Yamada, R. Fassler, and R. Timpl. 2001. Short arm region of laminin-5 γ2 chain: structure, mechanism of processing and binding to heparin and proteins. J. Mol. Biol. 314:751.
31. Veitch, D. P., P. Nokelainen, K. A. McGowan, T. Nguyen, N. E. Nguyen, R. Stephenson, W. N. Pappano, S. M. Spong, D. S. Greenspan, P. R. Findell, and M. P. Marinkovich. 2003. Mammalian tolloid metalloproteinase, and not matrix metalloproteinase 2 nor membrane type 1 metalloprotease, processes laminin-5 in keratinocytes and skin. J. Biol. Chem. 278:15661.
32. Sato, H. T. Takino, Y. Okada, J. Cao, A. Shinagawa, E. Yamamoto, and M. Seiki. 1994. A matrix metalloproteinase expressed on the surface of invasive tumor cells. Nature 370:61.
33. Sato, H., T. Takino, T. Kinoshita, K. Imai, Y. Okada, W. G. Stetler Stevenson, and M. Seiki. 1996. Cell surface binding and activation of gelatinase A induced by expression of membrane-type-1-matrix metalloproteinase (MTI-MMP). FEBS Lett. 385:238.
34. Butler, G. S., M. J. Butler, S. J. Atkinson, H. Will, T. Tamura, S. S. van Westrum, T. Crabbe, J. Clements, M. P. d'Ortho, and G. Murphy. 1998. The TIMP2 membrane type 1 metalloproteinase receptor regulates the concentration and efficient activation of progelatinase A: a kinetic study. J. Biol. Chem. 273:871.
35. Will, H., S. J. Atkinson, G. S. Butler, B. Smith, and G. Murphy. 1996. The soluble catalytic domain of membrane type 1 matrix metalloproteinase cleaves the propeptide of progelatinase A and initiates autoproteolytic activation: regulation by TIMP-2 and TIMP-3. J. Biol. Chem. 271:17119.
36. Itoh, Y., A. Ito, K. Iwata, K. Tanzawa, Y. Mori, and H. Nagase. 1998. Plasma membrane-bound tissue inhibitor of metalloproteinases (TIMP)-2 specifically inhibits matrix metalloproteinase 2 (gelatinase A) activated on the cell surface. J. Biol. Chem. 273:24360.
37. Werb, Z. 1997. ECM and cell surface proteolysis: regulating cellular ecology. Cell 91:439.
38. Murphy, G., and J. Gavrilovic. 1999. Proteolysis and cell migration: creating a path? Curr. Opin. Cell Biol. 11:614.
39. Nagase, H., and J. F. Woessner, Jr. 1999. Matrix metalloproteinases. J. Biol. Chem. 274:21491.
40. Hotary, K., E. Allen, A. Punturien, I. Yana, and S. J. Weiss. 2000. Regulation of cell invasion and morphogenesis in a three-dimensional type 1 collagen matrix by membrane-type matrix metalloproteinases 1, 2, and 3. J. Cell Biol. 149:1309.
41. Okamom, I., H. Kawano, H. Tsuiki, J. Sasaki, M. Nakao, M. Matsumoto. M. Suga, M. Ando, M. Nakajima, and H. Saya. 1999. CD44 cleavage induced by a membrane associated metalloproteinase plays a critical role in tumor cell migration. Oncogene 18:1435.
42. Kajita, M., Y. Itoh, T. Chiba, H. Mori, A. Okada, H. Kinoh, and M. Seiki. 2001. Membrane-type matrix metalloproteinase cleaves CD44 and promotes cell migration. J. Cell Biol. 153:893.
43. Mori, H., T. Tomari, N. Koshikawa, M. Kajita, Y. Itoh, H. Sato, H. Tojo, I. Yana, and M. Seiki. 2002. CD44 directs membrane-type 1 matrix metalloproteinase to lamellipodia by associating with its hemopexin-like domain. EMBO J. 21:3949.
44. Naot, D., R. V. Sionov, and D. Ish-Shalom. 1997. CD44: structure, function and association with the malignant process. Adv. Cancer Res. 71:241.
45. Patel, D. D., L. P. Hale, L. P. Wichard, G. Radcliff, C. R. Mackay, and B. F. Haynes. 1995. Expression of CD44 variant isoforms containing exon v9 on human thymic epithelial cells is a marker of thymic epithelial cell terminal differentiation. In Leukocyte Typing V, Vol. 2. Oxford University Press, New York, p. 1725.
46. Stauder, R., H.-J. Terpe, H. Stark, J. Thaler, C. R. Mackay, and U. Gunthert. 1995. Characterization and tissue distribution of CD44 variant isoforms in lymphoid and non-lymphoid human tissue. In Leukocyte Typing V, Vol. 2. Oxford University Press, New York, p. 1719.
47. Thomas, L., H. R. Byers, J. Vink, and I. Stamenkovic. 1992. CD44 regulates tumor cell migration on hyaluronate-coated substrate. J. Cell Biol. 118:971.
48. Henke, C. A., U. Roontga, D. J. Mickelson, J. R. Knutson, and J. B. Mc Carthy. 1996. CD44 related chondroitin sulfate proteoglycan, a cell surface receptor implicated with tumor cell invasion, mediates endothelial cell migration on fibrinogen and invasion into a fibrin matrix. J. Clin. Invest. 97:2541.
49. Marinkovich, M. P., G. P. Lunstrum, D. R. Keene, and R. E. Burgeson. 1992. The dermal-epidermal junction of human skin contains a novel laminin variant. J. Cell Biol. 119:695.
50. Rousselle, P., G. Lunstrum, D. R. Keene, and R. E. Burgeson. 1991. Kalinin: an epithelium specific basement membrane adhesion molecule that is a component of anchoring filaments. J. Cell Biol. 114:567.
51. Rousselle, P., and M. Aumailley. 1994. Kalinin is more efficient than laminin in promoting adhesion of primary keratinocytes and some other epihelial cells and has a different requirement for integrin receptors. J. Cell Biol. 125:205.
52. Marinkovich, M. P., G. P. Lunstrum, and R. E. Burgeson. 1992. The anchoring filament protein kalinin is synthesized and secreted as a high molecular weight precursor. J. Biol. Chem. 267:17900.
53. Moebius, U. 1989. T4 cluster report. In Leukocyte Typing IV: White Cell Differentiation Antigens. Oxford University Press, Oxford, p. 314.
54. Moebius, U. 1989. T8 cluster report. In Leukocyte Typing IV: White Cell Differentiation Antigens. Oxford University Press, Oxford, p. 342.
55. Wakkach, A., N. Fournier, V. Brun, J. P. Breittmayer, F. Cottrez, and H. Groux. 2003. Characterization of dendritic cells that induce tolerance and T regulatory I cell differentiation in vivo. Immunity 18:605.
56. Morodomi, T., Y. Ogata, Y. Sasaguri, M. Morimatsu, and H. Nagase. 1992. Purification and characterization of matrix metalloproteinase 9 from U937 monocytic leukemia and HT1080 fibrosarcoma cells. Biochem. J. 285:603.
57. Matsuyama, T., A. Yamada, J. Kay, K. M. Yamada, S. K. Akiyama, S. F. Schlossman, and C. Morimoto. 1989. Activation of CD4 cells by fibronectin and anti-CD3 antibody: a synergistic effect mediated by the VLA-5 fibronectin receptor complex. J. Exp. Med. 170:1133.
58. 1 integrin. Exp. Cell Res. 222:281.
59. Sonnenberg, A., P. W. Modderman, and F. Hogervorst. 1988. Laminin receptor on platelets is the integrin VLA-6. Nature 336:487.
60. 1 positive T lymphocytes. J. Cell Biol. 121:1141.
61. 1. J. Cell Sci. 108:831.
62. Bazil, V., and J. L. Strominger. 1994. Metalloprotease and serine protease are involved in cleavage of CD43, CD44, and CD16 from stimulated human granulocytes: induction of cleavage of L-selectin via CD16. J. Immunol. 152:1314.
63. Kutlesa, S., U. Siler, A. Speiser, J. T. Wessels, I. Virtanen, P. Rousselle, L. Sorokin, C. Müller, and G. Klein. 2002. Developmentally regulated interactions of human thymocytes with different laminin isoforms. Immunology 105:407.
64. Mojcik, C. K., D. R. Salomon, A. C. Chang, and E. M. Shevach. 1995. Differential expression of integrins on human thymocyte subpopulations. Blood 86:4206.
65. Bendelac, A., P. Matzinger, R. A. Seder, W. E. Paul, and R. H. Schwartz. 1992. Activation events during thymic selection. J. Exp. Med. 175:731.
66. Gabor, M., D. Godfrey, and R. Scollay. 1997. Recent thymic emigrants are distinct from most medullary thymocytes. Eur. J. Immunol. 27:2010.
67. Ushiki, T., and M. Takeda. 1997. Three-dimensional ultrastructure of the perivascular space in the rat thymus. Arch. Histol. Cytol. 60:89.
68. Kendall, M. D. 1989. The morphology of perivascular spaces in the thymus. Thymus 13:157.
69. Kikkawa, Y., M. Umeda, and K. Miyazaki. 1994. Marked stimulation of cell adhesion and motility by ladsin, a laminin-like scatter factor. J. Biochem. 116:862.
70. Zhang, K., and R. H. Kramer. 1996. Laminin 5 deposition promotes keratinocyte motility. Exp. Cell Res. 227:309.
71. Itoh, Y., A. Takamura, N. Ito, Y. Maru, H. Sato, N. Suenaga, T. Aoki, and M. Seiki. 2001. Homophilic complex formation of MTI-MMP facilitates proMMP-2 activation on the cell surface and promotes tumor cell invasion. EMBO J. 20:4782.
72. Madri, J. A., D. Graesser, and T. Haas. 1996. The roles of adhesion molecules and proteinases in lymphocyte transendothelial migration. Biochem. Cell Biol. 74:749.
73. Takabasbi, K., H. Eto, and K. K. Tanabe. 1999. Involvement of CD44 in matrix metalloproteinase-2 regulation in human melanoma cells. Int. J. Cancer 80:387.
74. 8 mediates epithelial homeostasis through MTI-MMP-dependent activation of TGF-B1. J. Cell Biol. 157:493.
75. Okamoto, I., Y. Kawano, D. Murakami, T. Sasayama, N. Araki, T. Miki, A. J. Wong, and H. Saya. 2001. Proteolytic release of CD44 intracellular domain and its role in the CD44 signaling pathway. J. Cell Biol. 155:755.