Soluble Axl is generated by ADAM10-dependent cleavage and associates with Gas6 in mouse serum

Molecular and Cellular Biology

Volumn 25, Issue 21, 2005, Pages 9324-9339

  Budagian, Vadim ^a   Bulanova, Elena ^a   Orinska, Zane ^a   Duitman, Erwin ^a   Brandt, Katja ^a   Ludwig, Andreas ^b   Hartmann, Dieter ^c   Lemke, Greg ^d   Saftig, Paul ^b   Bulfone Paus, Silvia ^a  

^a RESEARCH CENTER BORSTEL   (Germany)

^b UNIVERSITY OF KIEL   (Germany)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^d SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVITY OF DISINTEGRIN LIKE METALLOPROTEINASE 10; ILOMASTAT; MEMBRANE PROTEIN; METALLOPROTEINASE; METALLOPROTEINASE INHIBITOR; PHORBOL 13 ACETATE 12 MYRISTATE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN TYROSINE KINASE; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AUTOIMMUNITY; CELL FUNCTION; CELL MIGRATION; CELL TRANSFORMATION; COMPLEX FORMATION; DENDRITIC CELL; DNA CLEAVAGE; ENZYME PHOSPHORYLATION; GENE DELETION; IMMOBILIZED CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; VASCULAR ENDOTHELIUM;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ADAM PROTEINS; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; CELL LINE; CELL MOVEMENT; DENDRITIC CELLS; DIPEPTIDES; FEMALE; FIBROBLASTS; HYDROXAMIC ACIDS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, INBRED STRAINS; ONCOGENE PROTEINS; PHOSPHORYLATION; RECEPTOR PROTEIN-TYROSINE KINASES;

ANIMALIA; MURINAE;

EID: 27144492960     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.21.9324-9339.2005     Document Type: Article

References (70)

1. Abel, S., C. Hundhausen, R. Mentlein, A. Schulte, T. A. Berkhout, N. Broadway, D. Hartmann, R. Sedlacek, S. Dietrich, B. Muetze, B. Schuster, K.-J. Kallen, P. Saftig, S. Rose-John, and A. Ludwig. 2004. The transmembrane CXC-chemokine ligand 16 is induced by IFN-γ and TNF-α and shed by the activity of the disintegrin-like metalloproteinase ADAM10. J. Immunol. 172:6362-6372.
2. Allen, M. P., C. Zeng, K. Schneider, X. Xiong, M. K. Meintzer, P. Bellosta, C. Basilico, B. Varnum, K. A. Heidenreich, and M. E. Wiermann. 1999. Growth arrest-specific gene 6 (Gas6)/adhesion related kinase (Ark) signaling promotes gonadotropin-releasing hormone neuronal survival via extracellular signal-regulated kinase (ERK) and Akt. Mol. Endocrinol. 13:191-201.
3. Althoff, K., P. Reddy, N. Voltz, S. Rose-John, and J. Mullberg. 2000. Shedding of interleukin-6 receptor and tumor necrosis factor alpha. Eur. J. Biochem. 267:2624-2631.
4. Angelillo-Scherrer, A., P. G. de Frutos, C. Aparicio, E. Melis, P. Savi, F. Lupu, J. Arnout, M. Dewerchin, M. Hoylaerts, J. Herbert, D. Collen, B. Dahlback, and P. Carmeliet. 2001. Deficiency or inhibition of Gas6 causes platelet dysfunction and protects mice against thrombosis. Nat. Med. 7:215-221.
5. Angelillo-Scherrer, A., L. Burnier, N. Flores, P. Savi, M. DeMol, P. Schaeffer, J. M. Herbert, G. Lemke, S. P. Goff, G. K. Matsushima, H. S. Earp, C. Vesin, M. F. Hoylaerts, S. Plaisance, D. Collen, E. M. Conway, B. Wehrle-Haller, and P. Carmeliet. 2005. Role of Gas6 receptors in platelet signaling during thrombus stabilization and implications for antithrombotic therapy. J. Clin. Investig. 115:237-246.
6. Arribas, J., and J. Massague. 1995. Transforming growth factor-alpha and beta-amyloid precursor protein share a secretory mechanism. J. Cell Biol. 128:433-441.
7. Avanzi, G. C., M. Gallicchio, F. Bottarel, L. Gammaitoni, G. Cavalloni, D. Buonfiglio, M. Bragardo, G. Bellomo, E. Albano, R. Fantozzi, G. Garbarino, B. Varnum, M. Aglietta, G. Saglio, U. Dianzani, and C. Dianzani. 1998. GAS6 inhibits granulocyte adhesion to endothelial cells. Blood 91:2334-2340.
8. Bargmann, C. I., and R. A. Weinberg. 1988. Oncogenic activation of the neu-encoded receptor protein by point mutation and deletion. EMBO J. 7:2043-2052.
9. Bellosta, P., M. Costa, D. A. Lin, and C. Basilico. 1995. The receptor tyrosine kinase ARK mediates cell aggregation by homophilic binding. Mol. Cell. Biol. 15:614-625.
10. Bellosta, P., Q. Zhang, S. P. Goff, and C. Basilico. 1997. Signaling through the Ark tyrosine kinase receptor protects from apoptosis in the absence of growth stimulation. Oncogene 15:2387-2397.
11. Biscardi, J. S., F. Denhez, G. F. Buehler, D. A. Chesnutt, S. C. Baragona, J. P. O'Bryan, C. J. Der, J. J. Fiordalisi, D. W. Fults, and P. F. Maness. 1996. Rek, a gene expressed in retina and brain, encodes a receptor tyrosine kinase of the Axl/Tyro3 family. J. Biol. Chem. 271:29049-29059.
12. Black, R. A., C. T. Rauch, C. J. Kozlosky, J. J. Peschon, J. L. Slack, M. F. Wolfson, B. J. Castner, K. L. Stocking, P. Reddy, S. Srinivasan, M. Gerhart, R. Davis, J. N. Fitzner, R. S. Johnson, R. J. Paxton, C. J. March, and D. P. Cerretti. 1997. A metalloproteinase disintegrin that releases tumor-necrosis factor-α from cells. Nature 385:729-733.
13. Blobel, C. P. 1997. Metalloprotease-disintegrins: links to cell adhesion and cleavage of TNF α and Notch. Cell 90:589-592.
14. Blobel, C. P. 2005. ADAMs: key components in EGFR signaling and development. Nat. Rev. 6:32-43.
15. Brandt, K., R. Ruckert, D. C. Foster, and S. Bulfone-Paus. 2003. Interleukin-21 inhibits dendritic cell activation and maturation. Blood 102:4090-4098.
16. Brunelleschi, S., L. Penengo, M. M. Santoro, and G. Gaudino. 2002. Receptor tyrosine kinases as target for anti-cancer therapy. Curr. Pharm. Des. 8:1959-1972.
17. 2b fusion protein. Scand. J. Immunol. 55:484-492.
18. Budagian, V., E. Bulanova, Z. Orinska, A. Ludwig, S. Rose-John, P. Saftig, E. C. Borden, and S. Bulfone-Paus. 2004. Natural soluble interleukin-15Rα is generated by cleavage that involves the tumor necrosis factor-alpha-converting enzyme (TACE/ADAM17). J. Biol. Chem. 279:40368-40375.
19. Bulanova, E., V. Budagian, T. Pohl, H. Krause, H. Dürkop, R. Paus, and S. Bulfone-Paus. 2001. The IL-15Rα chain signals through association with Syk in human B cells. J. Immunol. 167:6292-6302.
20. Bulfone-Paus, S., E. Bulanova, T. Pohl, V. Budagian, H. Dürkop, R. Rückert, U. Kunzendorf, R. Paus, and H. Krause. 1999. Death deflected: IL-15 inhibits TNF-α-mediated apoptosis in fibroblasts by TRAF2 recruitment to the IL-15Rα chain. FASEB. J. 13:1575-1585.
21. Chilton, P. M., and R. Fernandez-Botran. 1993. Production of soluble IL-4 receptors by murine spleen cells is regulated by T cell activation and IL-4. J. Immunol. 151:5907-5917.
22. 2-terminally truncated HER-2/neu protein: relationship with shedding of the extracellular domain and with prognostic factors in breast cancer. Cancer Res. 58:5123-5129.
23. Costa, M., P. Bellosta, and C. Basilico. 1996. Cleavage and release of a soluble form of the receptor tyrosine kinase ARK in vitro and in vivo. J. Cell. Physiol. 168:737-744.
24. Demarchi, F., R. Verardo, B. Varnum, C. Brancolini, and C. Schneider. 2001. Gas6 anti-apoptotic signaling requires NF-κB activation. J. Biol. Chem. 278:31738-31744.
25. Dri, P., C. Gasparini, R. Menegazzi, R. Cramer, L. Alberi, G. Presani, S. Garbisa, and P. Patriarca. 2000. TNF-induced shedding of TNF receptors in human polymorphonuclear leukocytes: role of the 55-kDa TNF receptor and involvement of a membrane-bound and non-matrix metalloproteinase. J. Immunol. 165:2165-2172.
26. Faust, M., C. Ebensperger, A. S. Schulz, L. Schleithoff, H. Hameister, C. R. Bartram, and J. W. Janssen. 1992. The murine ufo receptor: molecular cloning, chromosomal localization and in situ expression analysis. Oncogene 7:1287-1293.
27. Fernandez-Bortran, R. 2000. Soluble cytokine receptors: novel immunotherapeutic agents. Expert Opin. Investig. Drugs 9:497-514.
28. Fortini, M. E. 2002. γ-Secretase-mediated proteolysis in cell-surface-receptor signaling. Nat. Rev. 3:673-684.
29. Fridell, Y. C., Y. Jin, L. A. Quilliam, A. Buchert, P. McCloskey, G. Spizz, B. Varnum, C. Der, and E. T. Liu. 1996. Differential activation of the Ras/extracellular-signal-regulated protein kinase pathway is responsible for the biological consequences induces by the Axl receptor tyrosine kinase. Mol. Cell. Biol. 16:135-145.
30. Fridell, Y. C., J. Villa, E. C. Attar, and E. T. Liu. 1998. GAS6 induces Axl-mediated chemotaxis of vascular smooth muscle cells. J. Biol. Chem. 273:7123-7126.
31. Goruppi, S., E. Ruaro, and C. Schneider. 1996. Gas6, the ligand of Axl tyrosine kinase receptor, has mitogenic and survival activities for serum starved NIH3T3 fibroblasts. Oncogene 12:471-480.
32. Goruppi, S., E. Ruaro, B. Varnum, and C. Schneider. 1997. Requirement of phosphatidylinositol 3-kinase-dependent pathway and Src for Gas6-Axl mitogenic and survival activities in NIH 3T3 fibroblasts. Mol. Cell. Biol. 17: 4442-4453.
33. Goruppi, S., C. Chiaruttini, M. E. Ruaro, B. Varnum, and C. Schneider. 2001. Gas6 induces growth, β-catenin stabilization, and T-cell factor transcriptional activation in contact-inhibited C57 mammary cells. Mol. Cell. Biol. 21:902-915.
34. Graham, D. K., T. L. Dawson, D. L. Mullaney, H. R. Snodgrass, and H. S. Earp. 1994. Cloning and mRNA expression analysis of a novel human protooncogene, c-mer. Cell Growth Differ. 5:647-657.
35. Guttridge, K. L., J. C. Luft, T. L. Dawson, E. Kozlowska, N. P. Mahajan, B. Varnum, and H. S. Earp. 2002. Mer receptor tyrosine kinase signaling. J. Biol. Chem. 277:24057-24088.
36. Hartmann, D., B. De Strooper, L. Serneels, K. Craessaerts, A. Herreman, W. Annaert, L. Umans, T. Lübke, A. L. Illert, K. von Figura, and P. Saftig. 2002. The disintegrin/metalloproteinase ADAM10 is essential for Notch signaling but not for α-secretase activity in fibroblasts. Hum. Mol. Genet. 11:2615-2624.
37. Heaney, M. L., and D. W. Golde. 1996. Soluble cytokine receptors. Blood 87:847-857.
38. Hundhausen, C., D. Misztela, T. A. Berkhout, N. Broadway, P. Saftig, K. Reiss, D. Hartmann, F. Fahrenholz, R. Postina, V. Matthews, K. J. Kallen, S. Rose-John, and A. Ludwig. 2003. The disintegrin-like metalloproteinase ADAM10 is involved in constitutive cleavage of CX3CL1 (fractalkine) and regulates CX3CL1-mediated cell-cell adhesion. Blood 102:1186-1195.
39. Hwang, C., M. Gatanaga, G. A. Granger, and T. Gatanaga. 1993. Mechanism of release of soluble forms of tumor necrosis factor/lymphotoxin receptors by phorbol myristate acetate-stimulated human THP-1 cells in vitro. J. Immunol. 151:5631-5638.
40. Jones, S. A., and S. Rose-John. 2002. The role of soluble receptors in cytokine biology: the agonistic properties of the sIL-6R/IL-6 complex. Biochim. Biophys. Acta 1592:251-263.
41. Lu, Q., M. Gore, Q. Zhang, T. Camenisch, S. Boast, F. Casagranda, C. Lai, M. K. Skinner, R. Klein, G. K. Matsushima, H. S. Earp, S. P. Goff, and G. Lemke. 1999. Tyro-3 family receptors are essential regulators of mammalian spermatogenesis. Nature 398:723-728.
42. Lu, Q., and G. Lemke. 2001. Homeostatic regulation of the immune system by receptor tyrosine kinases of the Tyro 3 family. Science 293:306-311.
43. Manfioletti, G., C. Brancolini, G. Avanzi, and C. Schneider. 1993. The protein encoded by a growth arrest-specific gene (gas6) is a new member of the vitamin K-dependent proteins related to protein S, a negative coregulator in the blood coagulation cascade. Mol. Cell. Biol. 3:4976-4985.
44. Mark, M. R., D. T. Scadden, Z. Wang, Q. Gu, A. Goddard, and P. J. Godowski. 1994. Rse, a novel receptor-type tyrosine kinase with homology to Axl/Ufo, is expressed at high levels in the brain. J. Biol. Chem. 269:10720-10728.
45. McCloskey, P., Y.-W. Fridell, E. Attar, J. Villa, Y. Jin, B. Varnum, and E. T. Liu. 1997. GAS6 mediates adhesion of cells expressing the receptor tyrosine kinase Axl. J. Biol. Chem. 272:23285-23291.
46. Melaragno, M. G., Y. C. Fridell, and B. C. Berk. 1999. The Gas6/Axl system. A novel regulator of vascular cell function. Trends Cardiovasc. Med. 9:250-253.
47. Nagai, K., H. Arai, M. Yanagita, T. Matsubara, H. Kanamori, T. Nakano, N. Iehara, A. Fukatsu, T. Kita, and T. Doi. 2003. Growth arrest-specific gene 6 is involved in glomerular hypertrophy in the early stage of diabetic nephropathy. J. Biol. Chem. 278:18229-18234.
48. Nagata, K., K. Ohashi, T. Nakano, H. Arita, C. Zong, H. Hanafusa, and K. Mizuno. 1996. Identification of the product of growth arrest-specific gene 6 as a common ligand for Axl, Sky, and Mer receptor tyrosine kinases. J. Biol. Chem. 271:30022-30027.
49. Nakano, T., Y. Ishimoto, J. Kishino, M. Umeda, K. Inoue, K. Nagata, K. Ohashi, K. Mizuno, and H. Arita. 1997. Cell adhesion to phosphatidylserine mediated by a product of growth arrest-specific gene 6. J. Biol. Chem. 272:29411-29414.
50. O'Bryan, J. P., Y.-W. Fridell, R. Koski, B. Varnum, and E. T. Liu. 1995. The transforming receptor tyrosine kinase, Axl, is post-translationally regulated by proteolytic cleavage. J. Biol. Chem. 270:551-557.
51. O'Donnell, K., I. C. Harkes, L. Dougherty, and I. P. Wicks. 1999. Expression of receptor tyrosine kinase Axl and its ligand Gas6 in rheumatoid arthritis. Am. J. Pathol. 154:1171-1180.
52. Paradies, N. E., and G. B. Grunwald. 1993. Purification and characterization of NCAD90, a soluble endogenous form of N-cadherin, which is generated by proteolysis during retinal development and retains adhesive and neuritepromoting function. J. Neurosci. Res. 36:33-45.
53. Peschon, J. J., J. L. Slack, P. Reddy, K. L. Stocking, S. W. Sunnarborg, D. C. Lee, W. E. Russell, B. J. Castner, R. S. Johnson, J. N. Fitzner, R. W. Boyce, N. Nelson, C. J. Kozlosky, M. F. Wolfson, C. T. Rauch, D. P. Cerretti, R. J. Paxton, C. J. March, and R. A. Black. 1998. An essential role for ectodomain shedding in mammalian development. Science 282:1281-1284.
54. Reiss, K., T. Maretzky, A. Ludwig, T. Tousseyn, B. De Strooper, D. Hartmann, and P. Saftig. 2005. ADAM10 cleavage of N-cadherin and regulation of cell-cell adhesion and β-catenin nuclear signaling. EMBO. J. 24:742-752.
55. Sahin, U., G. Weskamp, K. Kelly, H.-M. Zhou, S. Higashiyama, J. Peschon, D. Hartmann, P. Saftig, and C. P. Blobel. 2004. Distinct roles for ADAM10 and ADAM17 in ectodomain shedding of six EGFR ligands. J. Cell Biol. 164:769-779.
56. Sato, T. A., M. B. Widmer, F. D. Finkelman, H. Madani, C. A. Jacobs, K. H. Grabstein, and C. R. Maliszewski. 1993. Recombinant soluble murine IL-4 receptor can inhibit or enhance IgE responses in vivo. J. Immunol. 150:2717-2723.
57. Schlondorf, J., and C. P. Blobel. 1999. Metalloproteinase-disintegrins: modular proteins capable of promoting cell-cell interactions and triggering signals by protein-ectodomain shedding. J. Cell Sci. 112:3603-3617.
58. Schuermann, M. 1990. An expression vector system for stable expression of oncogenes. Nucleic Acids Res. 18:4945-4946.
59. Scott, R. S., E. J. McMahon, S. M. Pop, E. A. Reap, R. Caricchio, P. L. Cohen, H. P. Earp, and G. K. Matsushima. 2001. Phagocytosis and clearance of apoptotic cells is mediated by MER. Nature 411:207-211.
60. Six, E., D. Ndiaye, Y. Laabi, C. Brou, N. Gupta-Rossi, A. Israel, and F. Logeat. 2003. The Notch ligand Delta1 is sequentially cleaved by an ADAM protease and gamma-secretase. Proc. Natl. Acad. Sci. USA 100:7638-7643.
61. Slack, B. E., L. K. Ma, and C. C. Seah. 2001. Constitutive shedding of the amyloid precursor protein ectodomain is up-regulated by tumor necrosis factor-alpha converting enzyme. Biochem. J. 357:787-794.
62. Stenhoff, J., B. Dahlback, and S. Hafizi. 2004. Vitamin K-dependent Gas6 activates ERK kinase and stimulates growth of cardiac fibroblasts. Biochem. Biophys. Res. Commun. 319:871-878.
63. Sunnarborg, S. W., C. L. Hinkle, M. Srevenson, W. E. Russel, C. S. Raska, J. J. Reschon, B. J. Castner, M. J. Gerhart, R. J. Raxton, R. A. Black, and D. C. Lee. 2002. Tumor necrosis factor-alpha converting enzyme (TACE) regulates epidermal growth factor receptor ligand availability. J. Biol. Chem. 277:12838-12845.
64. Varnum, B. C., C. Young, G. Elliott, A. Garcia, T. D. Bartley, Y. W. Fridell, R. W. Hunt, G. Trail, C. Clogston, R. J. Toso, D. Yanagihara, L. Bennett, Sylber, L. A. Merewether, A. Tseng, E. Escobar, E. T. Liu, and H. K. Yamane. 1995. Axl receptor tyrosine kinase stimulated by the vitamin K-dependent protein encoded by growth-arrest-specific gene 6. Nature 373: 623-626.
65. Wang, L. H., B. Lin, S. M. Jong, D. Dixon, L. Ellis, R. A. Roth, and W. J. Rutter. 1987. Activation of transforming potential of the human insulin receptor gene. Proc. Natl. Acad. Sci. USA 84:5715-5729.
66. Wang, X., K. He, M. Gerhart, Y. Huang, J. Jiang, R. J. Paxton, S. Yang, C. Lu, R. K. Menon, R. A. Black, G. Baumann, and S. J. Frank. 2002. Metalloprotease-mediated GH receptor proteolysis and GHBP shedding. Determination of extracellular domain stem region cleavage site. J. Biol. Chem. 277:50510-50519.
67. Williams, A. F., and A. N. Barclay. 1988. The immunoglobulins superfamily-domains for cell surface recognition. Annu. Rev. Immunol. 6:381-405.
68. Yanagita, M., K. Ishii, H. Ozaki, H. Arai, T. Nakano, K. Ohashi, K. Mizuno, T. Kita, and T. Doi. 1999. Mechanism of inhibitory effect of warfarin on mesangial cell proliferation. J. Am. Soc. Nephrol. 10:2503-2509.
69. Yanagita, M., H. Arai, K. Ishii, T. Nakano, K. Ohashi, K. Mizuno, B. Varnum, A. Fukatsu, T. Doi, and T. Kita. 2001. Gas6 regulates mesangial cell proliferation through Axl in experimental glomerulonephritis. Am. J. Pathol. 158:1423-1432.
70. Yanagita, M., H. Arai, T. Nakano, K. Ohashi, K. Mizuno, A. Fukatsu, T. Doi, and T. Kita. 2001. Gas6 induces mesangial cell proliferation via latent transcription factor STAT3. J. Biol. Chem. 276:42364-42369.