Cleavage of mer tyrosine kinase (MerTK) from the cell surface contributes to the regulation of retinal phagocytosis

Journal of Biological Chemistry

Volumn 290, Issue 8, 2015, Pages 4941-4952

  Law, Ah Lai ^a,b,c   Parinot, Célia ^a,b,c   Chatagnon, Jonathan ^a,b,c   Gravez, Basile ^a,b,c   Sahel, José Alain ^a,b,c   Bhattacharya, Shomi S ^a,b,c,d,e   Nandrot, Emeline F ^a,b,c  

^a INSERM   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c CNRS   (France)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e CABIMER Andalusian Center for Molecular Biology and Regenerative Medicine CSIC University of Seville UPO   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ANTIGEN-ANTIBODY REACTIONS; CELL MEMBRANES; OPHTHALMOLOGY;

APICAL CELLS; CELL SURFACES; DAILY RHYTHM; EXTRACELLULAR; IN-VITRO; PHAGOCYTIC CAPACITY; RPE CELL; TYROSINE KINASE;

MACROPHAGES;

LACTADHERIN; MER TYROSINE KINASE; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; MERTK PROTEIN, MOUSE; ONCOPROTEIN;

ANIMAL TISSUE; ARTICLE; CELL SURFACE; CONTROLLED STUDY; ENZYME RELEASE; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MOUSE; NONHUMAN; PHAGOCYTOSIS; PHOTORECEPTOR OUTER SEGMENT; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN LOCALIZATION; RETINA CELL; ANIMAL; CELL LINE; CYTOLOGY; ENZYMOLOGY; GENETICS; METABOLISM; PHOTORECEPTOR CELL; PHYSIOLOGY; RETINAL PIGMENT EPITHELIUM;

ANIMALS; CELL LINE; MACROPHAGES; MICE; PHAGOCYTOSIS; PHOTORECEPTOR CELLS, VERTEBRATE; PROTO-ONCOGENE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; RETINAL PIGMENT EPITHELIUM;

EID: 84929096320     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.628297     Document Type: Article

References (51)

1. Rabinovitch, M. (1995) Professional and non-professional phagocytes: an introduction. Trends Cell Biol. 5, 85-87
2. Strauss, O. (2005) The retinal pigment epithelium in visual function. Physiol. Rev. 85, 845-881
3. Young, R.W., and Bok, D. (1969) Participation of the retinal pigment epithelium in the rod outer segment renewal process. J. Cell Biol. 42, 392-403
4. Bok, D., and Hall, M.O. (1971) The role of the pigment epithelium in the etiology of inherited retinal dystrophy in the rat. J. Cell Biol. 49, 664-682
5. LaVail, M.M. (1976) Rod outer segment disk shedding in rat retina: relationship to cyclic lighting. Science 194, 1071-1074
6. Young, R.W. (1977) The daily rhythm of shedding and degradation of cone outer segment membranes in the lizard retina. J. Ultrastruct. Res. 61, 172-185
7. Savill, J., Dransfield, I., Hogg, N., and Haslett, C. (1990) Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis. Nature 343, 170-173
8. Boesze-Battaglia, K., and Albert, A. D. (1992) Phospholipid distribution among bovine rod outer segment plasma membrane and disk membranes. Exp. Eye Res. 54, 821-823
9. Ruggiero, L., Connor, M.P., Chen, J., Langen, R., and Finnemann, S. C. (2012) Diurnal, localized exposure of phosphatidylserine by rod outer segment tips in wild-type but not Itgb5/or Mfge8/mouse retina. Proc. Natl. Acad. Sci. U.S.A. 109, 8145-8148
10. Ryeom, S. W., Silverstein, R. L., Scotto, A., and Sparrow, J.R. (1996) Binding of anionic phospholipids to retinal pigment epithelium may be mediated by the scavenger receptor CD36. J. Biol. Chem. 271, 20536-20539
11. Hanayama, R., Tanaka, M., Miwa, K., Shinohara, A., Iwamatsu, A., and Nagata, S. (2002) Identification of a factor that links apoptotic cells to phagocytes. Nature 417, 182-187
12. Nandrot, E. F., Anand, M., Almeida, D., Atabai, K., Sheppard, D., and Finnemann, S. C. (2007) Essential role for MFG-E8 as ligand for αvβ5 integrin in diurnal retinal phagocytosis. Proc. Natl. Acad. Sci. U.S.A. 104, 12005-12010
13. Finnemann, S. C., Bonilha, V. L., Marmorstein, A. D., and Rodriguez-Boulan, E. (1997) Phagocytosis of rod outer segments by retinal pigment epithelial cells requires α(v)β5 integrin for binding but not for internalization. Proc. Natl. Acad. Sci. U.S.A. 94, 12932-12937
14. Nandrot, E. F., Kim, Y., Brodie, S.E., Huang, X., Sheppard, D., and Finnemann, S. C. (2004) Loss of synchronized retinal phagocytosis and agerelated blindness in mice lacking αvβ5 integrin. J. Exp. Med. 200, 1539-1545
15. Ishimoto, Y., Ohashi, K., Mizuno, K., and Nakano, T. (2000) Promotion of the uptake of PS liposomes and apoptotic cells by a product of growth arrest-specific gene, gas6. J. Biochem. 127, 411-417
16. Manfioletti, G., Brancolini, C., Avanzi, G., and Schneider, C. (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. 13, 4976-4985
17. Hafizi, S., and Dahlbäck, B. (2006) Gas6 and protein S. Vitamin K-dependent ligands for the Axl receptor tyrosine kinase subfamily. FEBS J. 273, 5231-5244
18. Chen, J., Carey, K., and Godowski, P.J. (1997) Identification of Gas6 as a ligand for Mer, a neural cell adhesion molecule related receptor tyrosine kinase implicated in cellular transformation. Oncogene 14, 2033-2039
19. Prasad, D., Rothlin, C. V., Burrola, P., Burstyn-Cohen, T., Lu, Q., Garcia de Frutos, P., and Lemke, G. (2006) TAM receptor function in the retinal pigment epithelium. Mol. Cell. Neurosci. 33, 96-108
20. Hall, M.O., Prieto, A. L., Obin, M.S., Abrams, T.A., Burgess, B. L., Heeb, M.J., and Agnew, B. J. (2001) Outer segment phagocytosis by cultured retinal pigment epithelial cells requires Gas6. Exp. Eye Res. 73, 509-520
21. Hall, M.O., Obin, M.S., Heeb, M.J., Burgess, B. L., and Abrams, T.A. (2005) Both protein S and Gas6 stimulate outer segment phagocytosis by cultured rat retinal pigment epithelial cells. Exp. Eye Res. 81, 581-591
22. Burstyn-Cohen, T., Lew, E.D., Través, P. G., Burrola, P. G., Hash, J.C., and Lemke, G. (2012) Genetic dissection of TAM receptor-ligand interaction in retinal pigment epithelial cell phagocytosis. Neuron 76, 1123-1132
23. Duncan, J.L., LaVail, M.M., Yasumura, D., Matthes, M.T., Yang, H., Trautmann, N., Chappelow, A.V., Feng, W., Earp, H.S. , Matsushima, G. K., and Vollrath, D. (2003) An RCS-like retinal dystrophy phenotype in mer knockout mice. Invest. Ophthalmol. Vis. Sci. 44, 826-838
24. Nandrot, E., Dufour, E.M., Provost, A.C., Péquignot, M.O., Bonnel, S., Gogat, K., Marchant, D., Rouillac, C., Sépulchre de Condé, B., Bihoreau, M.T., Shaver, C., Dufier, J.L., Marsac, C., Lathrop, M., Menasche, M., and Abitbol, M.M. (2000) Homozygous deletion in the coding sequence of the c-mer gene in RCS rats unravels general mechanisms of physiological cell adhesion and apoptosis. Neurobiol. Dis. 7, 586-599
25. D'Cruz, P. M., Yasumura, D., Weir, J., Matthes, M.T., Abderrahim, H., LaVail, M.M., and Vollrath, D. (2000) Mutation of the receptor tyrosine kinase gene Mertk in the retinal dystrophic RCS rat. Hum. Mol. Genet. 9, 645-651
26. Scott, R.S., McMahon, E.J., Pop, S. M., Reap, E.A., Caricchio, R., Cohen, P.L., Earp, H.S. , and Matsushima, G. K. (2001) Phagocytosis and clearance of apoptotic cells is mediated by MER. Nature 411, 207-211
27. Vollrath, D., Feng, W., Duncan, J.L., Yasumura, D., D'Cruz, P. M., Chappelow, A., Matthes, M.T., Kay, M.A., and LaVail, M.M. (2001) Correction of the retinal dystrophy phenotype of the RCS rat by viral gene transfer of Mertk. Proc. Natl. Acad. Sci. U.S.A. 98, 12584-12589
28. Feng, W., Yasumura, D., Matthes, M.T., LaVail, M.M., and Vollrath, D. (2002) Mertk triggers uptake of photoreceptor outer segments during phagocytosis by cultured retinal pigment epithelial cells. J. Biol. Chem. 277, 17016-17022
29. Gal, A., Li, Y., Thompson, D.A., Weir, J., Orth, U., Jacobson, S.G., Apfelstedt-Sylla, E., and Vollrath, D. (2000) Mutations in MERTK, the human orthologue of the RCS rat retinal dystrophy gene, cause retinitis pigmentosa. Nat. Genet. 26, 270-271
30. McHenry, C. L., Liu, Y., Feng, W., Nair, A.R., Feathers, K. L., Ding, X., Gal, A., Vollrath, D., Sieving, P.A., and Thompson, D.A. (2004) MERTK arginine-844-cysteine in a patient with severe rod-cone dystrophy: loss of mutant protein function in transfected cells. Invest. Ophthalmol. Vis. Sci. 45, 1456-1463
31. Tschernutter, M., Jenkins, S.A., Waseem, N.H., Saihan, Z., Holder, G. E., Bird, A.C., Bhattacharya, S. S., Ali, R. R., and Webster, A.R. (2006) Clinical characterisation of a family with retinal dystrophy caused by mutation in the Mertk gene. Br. J. Ophthalmol. 90, 718-723
32. Cummings, C. T., Deryckere, D., Earp, H.S. , and Graham, D. K. (2013) Molecular pathways: MERTK signaling in cancer. Clin. Cancer Res. 19, 5275-5280
33. Cohen, P.L., Caricchio, R., Abraham, V., Camenisch, T. D., Jennette, J.C., Roubey, R.A., Earp, H.S. , Matsushima, G., and Reap, E.A. (2002) Delayed apoptotic cell clearance and lupus-like autoimmunity in mice lacking the c-mer membrane tyrosine kinase. J. Exp. Med. 196, 135-140
34. Cheong, H.S. , Lee, S. O., Choi, C.-B., Sung, Y.-K., Shin, H. D., and Bae, S.-C. (2007) MERTK polymorphisms associated with risk of haematological disorders among Korean SLE patients. Rheumatology 46, 209-214
35. Dickhout, J. G., Basseri, S., and Austin, R. C. (2008) Macrophage function and its impact on atherosclerotic lesion composition, progression, and stability: the good, the bad, and the ugly. Arterioscler. Thromb. Vasc. Biol. 28, 1413-1415
36. Wu, Y., Singh, S., Georgescu, M.-M., and Birge, R. B. (2005) A role for Mer tyrosine kinase inαvβ5 integrin-mediated phagocytosis of apoptotic cells. J. Cell Sci. 118, 539-553
37. Nandrot, E. F., Silva, K. E., Scelfo, C., and Finnemann, S. C. (2012) Retinal pigment epithelial cells use a MerTK-dependent mechanism to limit the phagocytic particle binding activity of αvβ5 integrin. Biol. Cell 104, 326-341
38. Rose-John, S., and Heinrich, P. C. (1994) Soluble receptors for cytokines and growth factors: generation and biological function. Biochem. J. 300, 281-290
39. Heaney, M. L., and Golde, D. W. (1996) Soluble cytokine receptors. Blood 87, 847-857
40. Costa, M., Bellosta, P., and Basilico, C. (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
41. Sather, S., Kenyon, K. D., Lefkowitz, J. B., Liang, X., Varnum, B. C., Henson, P. M., and Graham, D. K. (2007) A soluble form of the Mer receptor tyrosine kinase inhibits macrophage clearance of apoptotic cells and platelet aggregation. Blood 109, 1026-1033
42. Parinot, C., Rieu, Q., Chatagnon, J., Finnemann, S. C., and Nandrot, E. F. (2014) Large-scale purification of porcine or bovine photoreceptor outer segments for phagocytosis assays on retinal pigment epithelial cells. J. Vis. Exp. 94, e52100
43. Hall, M.O., and Abrams, T. (1987) Kinetic studies of rod outer segment binding and ingestion by cultured rat RPE cells. Exp. Eye Res. 45, 907-922
44. Rakoczy, P. E., Zhang, D., Robertson, T., Barnett, N. L., Papadimitriou, J., Constable, I. J., and Lai, C.-M. (2002) Progressive age-related changes similar to age-related macular degeneration in a transgenic mouse model. Am. J. Pathol. 161, 1515-1524
45. Gibbs, D., Kitamoto, J., and Williams, D. S. (2003) Abnormal phagocytosis by retinal pigmented epithelium that lacks myosin VIIa, the Usher syndrome 1B protein. Proc. Natl. Acad. Sci. U.S.A. 100, 6481-6486
46. Wavre-Shapton, S. T., Tolmachova, T., Lopes da Silva, M., da Silva, M., Futter, C. E., and Seabra, M. C. (2013) Conditional ablation of the choroideremia gene causes age-related changes in mouse retinal pigment epithelium. PLoS ONE 8, e57769
47. Finnemann, S. C., and Rodriguez-Boulan, E. (1999) Macrophage and retinal pigment epithelium phagocytosis: apoptotic cells and photoreceptors compete for αvβ3 and αvβ5 integrins, and protein kinase C regulates αvβ5 binding and cytoskeletal linkage. J. Exp. Med. 190, 861-874
48. Raposo, G., and Stoorvogel, W. (2013) Extracellular vesicles: exosomes, microvesicles, and friends. J. Cell Biol. 200, 373-383
49. Ling, L., Templeton, D., and Kung, H.J. (1996) Identification of the major autophosphorylation sites of Nyk/Mer, an NCAM-related receptor tyrosine kinase. J. Biol. Chem. 271, 18355-18362
50. Tibrewal, N., Wu, Y., D'mello, V., Akakura, R., George, T. C., Varnum, B., and Birge, R. B. (2008) Autophosphorylation docking site Tyr-867 in Mer receptor tyrosine kinase allows for dissociation of multiple signaling pathways for phagocytosis of apoptotic cells and down-modulation of lipopolysaccharide-inducible NF-κB transcriptional activation. J. Biol. Chem. 283, 3618-3627
51. Thorp, E., Vaisar, T., Subramanian, M., Mautner, L., Blobel, C., and Tabas, I. (2011) Shedding of the Mer tyrosine kinase receptor is mediated by ADAM17 protein through a pathway involving reactive oxygen species, protein kinase C∂, and p38 mitogen-activated protein kinase (MAPK). J. Biol. Chem. 286, 33335-33344