GRK6 deficiency in mice causes autoimmune disease due to impaired apoptotic cell clearance

Nature Communications

Volumn 4, Issue , 2013, Pages

  Nakaya, Michio ^a   Tajima, Mitsuru ^a   Kosako, Hidetaka ^b   Nakaya, Takeo ^c   Hashimoto, Akiko ^a   Watari, Kenji ^a   Nishihara, Hiroaki ^a   Ohba, Mina ^a   Komiya, Shiori ^a   Tani, Naoki ^b   Nishida, Motohiro ^a   Taniguchi, Hisaaki ^b   Sato, Yoji ^d   Matsumoto, Mitsuru ^b   Tsuda, Makoto ^a   Kuroda, Masahiko ^c   Inoue, Kazuhide ^a   Kurose, Hitoshi ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKUSHIMA   (Japan)

^c TOKYO MEDICAL UNIVERSITY   (Japan)

^d NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DOCK180 PROTEIN; ELMO PROTEIN; G PROTEIN COUPLED RECEPTOR KINASE; G PROTEIN COUPLED RECEPTOR KINASE 6; GIT1 PROTEIN; GULP1 PROTEIN; IRON; RAC1 PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; CYTOLOGY; DISEASE INCIDENCE; GENE EXPRESSION; HOMEOSTASIS; IMMUNE SYSTEM; IRON; PROTEIN; RODENT;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; AUTOIMMUNE DISEASE; CELL AGING; CELL MIGRATION; CONTROLLED STUDY; ERYTHROCYTE; HOMEOSTASIS; IMMUNE SYSTEM; IN VITRO STUDY; IN VIVO STUDY; IRON METABOLISM; MACROPHAGE; MOUSE; NONHUMAN; PHAGOCYTOSIS; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SPLEEN; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; APOPTOSIS; AUTOIMMUNE DISEASES; CELL AGING; CELL CYCLE PROTEINS; CYTOSKELETAL PROTEINS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ERYTHROCYTES; FEMALE; G-PROTEIN-COUPLED RECEPTOR KINASES; GTPASE-ACTIVATING PROTEINS; HUMANS; MACROPHAGES; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICROFILAMENT PROTEINS; NIH 3T3 CELLS; PHAGOCYTOSIS; PHOSPHORYLATION; RAC GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; SPLEEN;

EID: 84874604710     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms2540     Document Type: Article

References (47)

1. Peter, C., Wesselborg, S., Herrmann, M. & Lauber, K. Dangerous attraction: phagocyte recruitment and danger signals of apoptotic and necrotic cells. Apoptosis 15, 1007-1028 (2010)
2. Maderna, P. & Godson, C. Phagocytosis of apoptotic cells and the resolution of inflammation. Biochim. Biophys. Acta. 1639, 141-151 (2003) (Pubitemid 37421421)
3. Kinchen, J. M. et al. Two pathways converge at CED-10 to mediate actin rearrangement and corpse removal in C. elegans. Nature 434, 93-99 (2005) (Pubitemid 40349391)
4. Nagata, S., Hanayama, R. & Kawane, K. Autoimmunity and the clearance of dead cells. Cell 140, 619-630 (2010)
5. Mangahas, P. M. & Zhou, Z. Clearance of apoptotic cells in Caenorhabditis elegans. Semin. Cell Dev. Biol. 16, 295-306 (2005) (Pubitemid 40432130)
6. Albert, M. L., Kim, J. I. & Birge, R. B. alphavbeta5 integrin recruits the CrkIIDock180-rac1 complex for phagocytosis of apoptotic cells. Nat. Cell Biol. 2, 899-905 (2000)
7. Reddien, P. W. & Horvitz, H. R. The engulfment process of programmed cell death in Caenorhabditis elegans. Annu. Rev. Cell Dev. Biol. 20, 193-221 (2004) (Pubitemid 39488637)
8. Penn, R. B., Pronin, A. N. & Benovic, J. L. Regulation of G protein-coupled receptor kinases. Trends Cardiovasc. Med. 10, 81-89 (2000) (Pubitemid 32012684)
9. Premont, R. T. & Gainetdinov, R. R. Physiological roles of G protein-coupled receptor kinases and arrestins. Annu. Rev. Physiol. 69, 511-534 (2007) (Pubitemid 46457653)
10. Reiter, E. & Lefkowitz, R. J. GRKs and beta-arrestins: roles in receptor silencing, trafficking and signaling. Trends Endocrinol. Metab. 17, 159-165 (2006)
11. Moore, C. A., Milano, S. K. & Benovic, J. L. Regulation of receptor trafficking by GRKs and arrestins. Annu. Rev. Physiol. 69, 451-482 (2007) (Pubitemid 46457651)
12. Penela, P., Murga, C., Ribas, C., Lafarga, V. & Mayor, Jr F. The complex G protein-coupled receptor kinase 2 (GRK2) interactome unveils new physiopathological targets. Br. J. Pharmacol. 160, 821-832 (2010)
13. Gurevich, E. V., Tesmer, J. J., Mushegian, A. & Gurevich, V. V. G proteincoupled receptor kinases: more than just kinases and not only for GPCRs. Pharmacol. Ther. 133, 40-69 (2012)
14. Usui, I. et al. G protein-coupled receptor kinase 2 mediates endothelin-1-induced insulin resistance via the inhibition of both Galphaq/11 and insulin receptor substrate-1 pathways in 3T3-L1 adipocytes. Mol. Endocrinol. 19, 2760-2768 (2005) (Pubitemid 41577248)
15. Martini, J. S. et al. Uncovering G protein-coupled receptor kinase-5 as a histone deacetylase kinase in the nucleus of cardiomyocytes. Proc. Natl Acad. Sci. USA 105, 12457-12462 (2008)
16. Hoefen, R. J. & Berk, B. C. The multifunctional GIT family of proteins. J. Cell Sci. 119, 1469-1475 (2006) (Pubitemid 43732975)
17. Fehon, R. G., McClatchey, A. I. & Bretscher, A. Organizing the cell cortex: the role of ERM proteins. Nat. Rev. Mol. Cell Biol. 11, 276-287 (2010)
18. Gainetdinov, R. R., Premont, R. T., Caron, M. G. & Lefkowitz, R. J. Reply: receptor specificity of G-protein-coupled receptor kinases. Trends Pharmacol. Sci. 21, 366-367 (2000)
19. Simon, V., Robin, M. T., Legrand, C. & Cohen-Tannoudji, J. Endogenous G protein-coupled receptor kinase 6 triggers homologous beta-adrenergic receptor desensitization in primary uterine smooth muscle cells. Endocrinology 144, 3058-3066 (2003) (Pubitemid 36819908)
20. Penela, P. et al. G protein-coupled receptor kinase 2 positively regulates epithelial cell migration. EMBO J. 27, 1206-1218 (2008) (Pubitemid 351574750)
21. Nakaya, M., Tanaka, M., Okabe, Y., Hanayama, R. & Nagata, S. Opposite effects of rho family GTPases on engulfment of apoptotic cells by macrophages. J. Biol. Chem. 281, 8836-8842 (2006) (Pubitemid 43847990)
22. Hall, A. G proteins and small GTPases: distant relatives keep in touch. Science 280, 2074-2075 (1998) (Pubitemid 28366192)
23. Brugnera, E. et al. Unconventional Rac-GEF activity is mediated through the Dock180-ELMO complex. Nat. Cell Biol. 4, 574-582 (2002)
24. Park, S. Y. et al. Requirement of adaptor protein GULP during stabilin-2-mediated cell corpse engulfment. J. Biol. Chem. 283, 10593-10600 (2008)
25. Premont, R. T. et al. Beta2-adrenergic receptor regulation by GIT1, a G proteincoupled receptor kinase-associated ADP ribosylation factor GTPase-activating protein. Proc. Natl Acad. Sci. USA 95, 14082-14087 (1998) (Pubitemid 28549324)
26. Mandiyan, V., Andreev, J., Schlessinger, J. & Hubbard, S. R. Crystal structure of the ARF-GAP domain and ankyrin repeats of PYK2-associated protein beta. EMBO J. 18, 6890-6898 (1999) (Pubitemid 30000442)
27. Premont, R. T. et al. The GIT/PIX complex: an oligomeric assembly of GIT family ARF GTPase-activating proteins and PIX family Rac1/Cdc42 guanine nucleotide exchange factors. Cell Signal 16, 1001-1011 (2004) (Pubitemid 38798051)
28. Kosako, H. et al. Phosphoproteomics reveals new ERK MAP kinase targets and links ERK to nucleoporin-mediated nuclear transport. Nat. Struct. Mol. Biol. 16, 1026-1035 (2009)
29. Erwig, L. P. et al. Differential regulation of phagosome maturation in macrophages and dendritic cells mediated by Rho GTPases and ezrin-radixinmoesin (ERM) proteins. Proc. Natl Acad. Sci. USA 103, 12825-12830 (2006)
30. Matsui, T. et al. Rho-kinase phosphorylates COOH-terminal threonines of ezrin/radixin/moesin (ERM) proteins and regulates their head-to-tail association. J. Cell Biol. 140, 647-657 (1998) (Pubitemid 28134067)
31. Mangeat, P., Roy, C. & Martin, M. ERM proteins in cell adhesion and membrane dynamics. Trends Cell Biol. 9, 187-192 (1999) (Pubitemid 29192986)
32. Elliott, M. R. & Ravichandran, K. S. Clearance of apoptotic cells: implications in health and disease. J. Cell Biol. 189, 1059-1070 (2010)
33. Hanayama, R. et al. Autoimmune disease and impaired uptake of apoptotic cells in MFG-E8-deficient mice. Science 304, 1147-1150 (2004) (Pubitemid 38661849)
34. Peng, Y. & Elkon, K. B. Autoimmunity in MFG-E8-deficient mice is associated with altered trafficking and enhanced cross-presentation of apoptotic cell antigens. J. Clin. Invest. 121, 2221-2241 (2011)
35. Sallusto, F., Geginat, J. & Lanzavecchia, A. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu. Rev. Immunol. 22, 745-763 (2004) (Pubitemid 38680440)
36. Mukundan, L. et al. PPAR-delta senses and orchestrates clearance of apoptotic cells to promote tolerance. Nat. Med. 15, 1266-1272 (2009)
37. A-Gonzalez., N. et al. Apoptotic cells promote their own clearance and immune tolerance through activation of the nuclear receptor LXR. Immunity 31, 245-258 (2009)
38. McEvoy, L., Williamson, P. & Schlegel, R. A. Membrane phospholipid asymmetry as a determinant of erythrocyte recognition by macrophages. Proc. Natl Acad. Sci. USA 83, 3311-3315 (1986) (Pubitemid 16043026)
39. Connor, J., Pak, C. C. & Schroit, A. J. Exposure of phosphatidylserine in the outer leaflet of human red blood cells. Relationship to cell density, cell age, and clearance by mononuclear cells. J. Biol. Chem. 269, 2399-2404 (1994)
40. Kohyama, M. et al. Role for Spi-C in the development of red pulp macrophages and splenic iron homeostasis. Nature 457, 318-321 (2009)
41. Chow, A. et al. Bone marrow CD169 macrophages promote the retention of hematopoietic stem and progenitor cells in the mesenchymal stem cell niche. J. Exp. Med. 208, 261-271 (2011)
42. Hashimoto, D. et al. Pretransplant CSF-1 therapy expands recipient macrophages and ameliorates GVHD after allogeneic hematopoietic cell transplantation. J. Exp. Med. 208, 1069-1082 (2011)
43. Tolosano, E. et al. Enhanced splenomegaly and severe liver inflammation in haptoglobin/hemopexin double-null mice after acute hemolysis. Blood 100, 4201-4208 (2002) (Pubitemid 35402055)
44. Lafarga, V., Aymerich, I., Tapia, O., Mayor, Jr F. & Penela, P. A novel GRK2/ HDAC6 interaction modulates cell spreading and motility. EMBO J. 31, 856-869 (2012)
45. Ribas, C. et al. The G protein-coupled receptor kinase (GRK) interactome: role of GRKs in GPCR regulation and signaling. Biochim. Biophys. Acta. 1768, 913-922 (2007) (Pubitemid 46452540)
46. Cant, S. H. & Pitcher, J. A. G protein-coupled receptor kinase 2-mediated phosphorylation of ezrin is required for G protein-coupled receptor-dependent reorganization of the actin cytoskeleton. Mol. Biol. Cell 16, 3088-3099 (2005) (Pubitemid 40962582)
47. Oldenborg, P. A. et al. Role of CD47 as a marker of self on red blood cells. Science 288, 2051-2054 (2000).