Caenorhabditis elegans transthyretin-like protein TTR-52 mediates recognition of apoptotic cells by the CED-1 phagocyte receptor

Nature Cell Biology

Volumn 12, Issue 7, 2010, Pages 655-664

  Wang, Xiaochen ^a,b   Li, Weida ^b   Zhao, Dongfeng ^b   Liu, Bin ^b   Shi, Yong ^a   Chen, Baohui ^b   Yang, Hengwen ^a   Guo, Pengfei ^b   Geng, Xin ^a   Shang, Zhihong ^a   Peden, Erin ^a   Kage Nakadai, Eriko ^c   Mitani, Shohei ^c   Xue, Ding ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b NATIONAL INSTITUTE OF BIOLOGICAL SCIENCES   (China)

^c TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; CELL RECEPTOR; PHAGOCYTE RECEPTOR CED 1; PHAGOCYTE RECEPTOR CED 6; PHAGOCYTE RECEPTOR CED 7; PHOSPHATIDYLSERINE; TRANSTHYETIN LIKE PROTEIN TTR 52; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENDODERM; GENETIC CODE; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL;

CAENORHABDITIS ELEGANS;

EID: 77954242242     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb2068     Document Type: Article

References (54)

1. Savill, J., Dransfield, I., Gregory, C. & Haslett, C. A blast from the past: clearance of apop-totic cells regulates immune responses. Nat. Rev. Immunol. 2, 965-975 (2002).
2. Henson, P. M., Bratton, D. L. & Fadok, V. A. Apoptotic cell removal. Curr. Biol. 11, R795-R805 (2001).
3. Savill, J. & Fadok, V. Corpse clearance defines the meaning of cell death. Nature 407, 784-788 (2000).
4. 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).
5. Reddien, P. W. & Horvitz, H. R. CED-2/CrkII and CED-10/Rac control phagocytosis and cell migration in Caenorhabditis elegans. Nat. Cell Biol. 2, 131-136 (2000).
6. Wu, Y. C. & Horvitz, H. R. C. elegans phagocytosis and cell-migration protein CED-5 is similar to human DOCK180. Nature 392, 501-504 (1998).
7. Gumienny, T. L. et al. CED-12/ELMO, a novel member of the CrkII/Dock180/Rac pathway, is required for phagocytosis and cell migration. Cell 107, 27-41 (2001).
8. Zhou, Z., Caron, E., Hartwieg, E., Hall, A. & Horvitz, H. R. The C. elegans PH domain protein CED-12 regulates cytoskeletal reorganization via a Rho/Rac GTPase signaling pathway. Dev. Cell 1, 477-489 (2001).
9. Wu, Y. C., Tsai, M. C., Cheng, L. C., Chou, C. J. & Weng, N. Y. C. elegans CED-12 acts in the conserved crkII/DOCK180/Rac pathway to control cell migration and cell corpse engulfment. Dev. Cell 1, 491-502 (2001).
10. Zhou, Z., Hartwieg, E. & Horvitz, H. R. CED-1 is a transmembrane receptor that mediates cell corpse engulfment in C. elegans. Cell 104, 43-56 (2001).
11. Su, H. P. et al. Interaction of CED-6/GULP, an adapter protein involved in engulfment of apoptotic cells with CED-1 and CD91/low density lipoprotein receptor-related protein (LRP). J. Biol. Chem. 277, 11772-11779 (2002).
12. Hamon, Y. et al. Cooperation between engulfment receptors: the case of ABCA1 and MEGF10. PLoS ONE 1, e120 (2006).
13. Manaka, J. et al. Draper-mediated and phosphatidylserine-independent phagocytosis of apoptotic cells by Drosophila hemocytes/macrophages. J. Biol. Chem. 279, 48466-48476 (2004).
14. Kurant, E., Axelrod, S., Leaman, D. & Gaul, U. Six-microns-under acts upstream of Draper in the glial phagocytosis of apoptotic neurons. Cell 133, 498-509 (2008).
15. MacDonald, J. M. et al. The Drosophila cell corpse engulfment receptor Draper mediates glial clearance of severed axons. Neuron 50, 869-881 (2006).
16. Gardai, S. J. et al. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 123, 321-334 (2005).
17. Fadok, V. A. et al. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148, 2207-2216 (1992).
18. Gardai, S. J., Bratton, D. L., Ogden, C. A. & Henson, P. M. Recognition ligands on apoptotic cells: a perspective. J. Leukoc. Biol. 79, 896-903 (2006).
19. Wang, X. et al. C. elegans mitochondrial factor WAH-1 promotes phosphatidylserine externalization in apoptotic cells through phospholipid scramblase SCRM-1. Nature Cell Biol. 9, 541-549 (2007).
20. Zullig, S. et al. Aminophospholipid translocase TAT-1 promotes phosphatidylserine exposure during C. elegans apoptosis. Curr. Biol. 17, 994-999 (2007).
21. Venegas, V. & Zhou, Z. Two alternative mechanisms that regulate the presentation of apoptotic cell engulfment signal in Caenorhabditis elegans. Mol. Biol. Cell 18, 3180-3192 (2007).
22. Darland-Ransom, M. et al. Role of C. elegans TAT-1 protein in maintaining plasma membrane phosphatidylserine asymmetry. Science 320, 528-531 (2008).
23. Wang, X. et al. Cell corpse engulfment mediated by C. elegans phosphatidylserine receptor through CED-5 and CED-12. Science 302, 1563-1566 (2003).
24. Yu, X., Odera, S., Chuang, C. H., Lu, N. & Zhou, Z. C. elegans Dynamin mediates the signaling of phagocytic receptor CED-1 for the engulfment and degradation of apoptotic cells. Dev. Cell 10, 743-757 (2006).
25. Hoeppner, D. J., Hengartner, M. O. & Schnabel, R. Engulfment genes cooperate with ced-3 to promote cell death in Caenorhabditis elegans. Nature 412, 202-206 (2001).
26. Reddien, P. W., Cameron, S. & Horvitz, H. R. Phagocytosis promotes programmed cell death in C. elegans. Nature 412, 198-202 (2001).
27. Schreiber, G. The evolutionary and integrative roles of transthyretin in thyroid hormone homeostasis. J. Endocrinol. 175, 61-73 (2002).
28. Sonnhammer, E. L. & Durbin, R. Analysis of protein domain families in Caenorhabditis elegans. Genomics 46, 200-216 (1997).
29. Saverwyns, H. et al. Analysis of the transthyretin-like (TTL) gene family in Ostertagia ostertagi\comparison with other strongylid nematodes and Caenorhabditis elegans. Int. J. Parasitol. 38, 1545-1556 (2008).
30. Ellis, H. M. & Horvitz, H. R. Genetic control of programmed cell death in the nematode C. elegans. Cell 44, 817-829 (1986).
31. Conradt, B. & Horvitz, H. R. The TRA-1A sex determination protein of C. elegans regulates sexually dimorphic cell deaths by repressing the egl-1 cell death activator gene. Cell 98, 317-327 (1999).
32. Kennedy, B. P. et al. The gut esterase gene (ges-1) from the nematodes Caenorhabditis elegans and Caenorhabditis briggsae. J. Mol. Biol. 229, 890-908 (1993).
33. Robertson, A. G. & Thomson, J. N. Morphology of programmed cell death in the ventral nerve chord of C. elegans larvae. J. Embryol. Exp. Morphol. 67, 89 (1982).
34. Sulston, J. E., Schierenberg, E., White, J. G. & Thomson, J. N. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100, 64-119 (1983).
35. Yeung, T. et al. Membrane phosphatidylserine regulates surface charge and protein localization. Science 319, 210-213 (2008).
36. Shi, J., Heegaard, C. W., Rasmussen, J. T. & Gilbert, G. E. Lactadherin binds selectively to membranes containing phosphatidyl-L-serine and increased curvature. Biochim. Biophys. Acta 1667, 82-90 (2004).
37. Kritikou, E. A. et al. C. elegans GLA-3 is a novel component of the MAP kinase MPK-1 signaling pathway required for germ cell survival. Genes Dev. 20, 2279-2292 (2006).
38. Savill, J., Hogg, N., Ren, Y. & Haslett, C. Thrombospondin cooperates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis. J. Clin. Invest. 90, 1513-1522 (1992).
39. Anderson, H. A. et al. Serum-derived protein S binds to phosphatidylserine and stimulates the phagocytosis of apoptotic cells. Nat. Immunol. 4, 87-91 (2003).
40. 2-glycoprotein I in macrophage recognition. J. Biol. Chem. 272, 31113-31117 (1997).
41. Ishimoto, Y., Ohashi, K., Mizuno, K. & Nakano, T. Promotion of the uptake of PS lipo-somes and apoptotic cells by a product of growth arrest-specific gene, gas6. J. Biochem. (Tokyo) 127, 411-417 (2000).
42. Vandivier, R. W. et al. Role of surfactant proteins A, D, and C1q in the clearance of apoptotic cells in vivo and in vitro: calreticulin and CD91 as a common collectin receptor complex. J. Immunol. 169, 3978-3986 (2002).
43. Savill, J., Fadok, V., Henson, P. & Haslett, C. Phagocyte recognition of cells undergoing apoptosis. Immunol. Today 14, 131-136 (1993).
44. Gardai, S. J. et al. By binding SIRPα or calreticulin/CD91, lung collectins act as dual function surveillance molecules to suppress or enhance inflammation. Cell 115, 13-23 (2003).
45. Eneqvist, T., Lundberg, E., Nilsson, L., Abagyan, R. & Sauer-Eriksson, A. E. The tran-sthyretin-related protein family. Eur. J. Biochem. 270, 518-532 (2003).
46. Lundberg, E., Backstrom, S., Sauer, U. H. & Sauer-Eriksson, A. E. The transthyretin-related protein: structural investigation of a novel protein family. J. Struct. Biol. 155, 445-457 (2006).
47. Lee, Y. et al. Mouse transthyretin-related protein is a hydrolase which degrades 5-hydroxyisourate, the end product of the uricase reaction. Mol. Cells 22, 141-145 (2006).
48. Nam, K. H. & Li, J. The Arabidopsis transthyretin-like protein is a potential substrate of BRASSINOSTEROID-INSENSITIVE 1. Plant Cell 16, 2406-2417 (2004).
49. Fadeel, B. & Xue, D. The ins and outs of phospholipid asymmetry in the plasma membrane: roles in health and disease. Crit. Rev. Biochem. Mol. Biol. 44, 264-277 (2009).
50. Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71-94 (1974).
51. Riddle, D. L., Blumenthal, T., Meyer, B. J. & Preiss, J. R. (eds). C. elegans II (Cold Spring Harbor Laboratory Press, 1997).
52. Ellis, R. E., Jacobson, D. M. & Horvitz, H. R. Genes required for the engulfment of cell corpses during programmed cell death in Caenorhabditis elegans. Genetics 129, 79-94 (1991).
53. Parrish, J. et al. Mitochondrial endonuclease G is important for apoptosis in C. elegans. Nature 412, 90-94 (2001).
54. Geng, X. et al. Inhibition of CED-3 zymogen activation and apoptosis in Caenorhabditis elegans by caspase homolog CSP-3. Nat. Struct. Mol. Biol. 15, 1094-1101 (2008).