Draper acts through the JNK pathway to control synchronous engulfment of dying germline cells by follicular epithelial cells

Development (Cambridge)

Volumn 139, Issue 21, 2012, Pages 4029-4039

  Etchegaray, Jon Iker ^a   Timmons, Allison K ^a   Klein, Adam P ^a   Pritchett, Tracy L ^a   Welch, Elaine ^a   Meehan, Tracy L ^a   Li, Christy ^a   McCall, Kimberly ^a  

^a Boston University   (United States)

Author keywords

Cell death; Drosophila; Engulfment; Ovary

Indexed keywords

CASPASE; JANUS KINASE; RECEPTOR PROTEIN;

ARTICLE; CELL DEATH; DROSOPHILA MELANOGASTER; EGG; EPITHELIUM CELL; GERM CELL; NONHUMAN; OVARY; OVARY FOLLICLE; PHAGOCYTOSIS; PRIORITY JOURNAL;

ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EPITHELIAL CELLS; FEMALE; GERM CELLS; MAP KINASE SIGNALING SYSTEM; MEMBRANE PROTEINS; OVARIAN FOLLICLE; SIGNAL TRANSDUCTION;

EID: 84867264110     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.082776     Document Type: Article

References (57)

1. Adachi-Yamada, T., Nakamura, M., Irie, K., Tomoyasu, Y., Sano, Y., Mori, E., Goto, S., Ueno, N., Nishida, Y. and Matsumoto, K. (1999). p38 mitogenactivated protein kinase can be involved in transforming growth factor beta superfamily signal transduction in Drosophila wing morphogenesis. Mol. Cell. Biol. 19, 2322-2329.
2. Birge, R. B. and Ucker, D. S. (2008). Innate apoptotic immunity: the calming touch of death. Cell Death Differ. 15, 1096-1102.
3. Cuttell, L., Vaughan, A., Silva, E., Escaron, C. J., Lavine, M., Van Goethem, E., Eid, J. P., Quirin, M. and Franc, N. C. (2008). Undertaker, a Drosophila Junctophilin, links Draper-mediated phagocytosis and calcium homeostasis. Cell 135, 524-534.
4. Elliott, M. R. and Ravichandran, K. S. (2010). Clearance of apoptotic cells: implications in health and disease. J. Cell Biol. 189, 1059-1070.
5. Erwig, L. P. and Henson, P. M. (2008). Clearance of apoptotic cells by phagocytes. Cell Death Differ. 15, 243-250.
6. Fernandez, R., Takahashi, F., Liu, Z., Steward, R., Stein, D. and Stanley, E. R. (2000). The Drosophila shark tyrosine kinase is required for embryonic dorsal closure. Genes Dev. 14, 604-614.
7. Freeman, M. R., Delrow, J., Kim, J., Johnson, E. and Doe, C. Q. (2003). Unwrapping glial biology: Gcm target genes regulating glial development, diversification, and function. Neuron 38, 567-580.
8. Fullard, J. F., Kale, A. and Baker, N. E. (2009). Clearance of apoptotic corpses. Apoptosis 14, 1029-1037.
9. Giorgi, F. and Deri, P. (1976). Cell death in ovarian chambers of Drosophila melanogaster. J. Embryol. Exp. Morphol. 35, 521-533.
10. Hoeppner, D. J., Hengartner, M. O. and Schnabel, R. (2001). Engulfment genes cooperate with ced-3 to promote cell death in Caenorhabditis elegans. Nature 412, 202-206.
11. Hurwitz, M. E., Vanderzalm, P. J., Bloom, L., Goldman, J., Garriga, G. and Horvitz, H. R. (2009). Abl kinase inhibits the engulfment of apoptotic cells in Caenorhabditis elegans. PLoS Biol. 7, e1000099.
12. Ichimura, T., Asseldonk, E. J., Humphreys, B. D., Gunaratnam, L., Duffield, J. S. and Bonventre, J. V. (2008). Kidney injury molecule-1 is a phosphatidylserine receptor that confers a phagocytic phenotype on epithelial cells. J. Clin. Invest. 118, 1657-1668.
13. Igaki, T. (2009). Correcting developmental errors by apoptosis: lessons from Drosophila JNK signaling. Apoptosis 14, 1021-1028.
14. Igaki, T., Kanda, H., Yamamoto-Goto, Y., Kanuka, H., Kuranaga, E., Aigaki, T. and Miura, M. (2002). Eiger, a TNF superfamily ligand that triggers the Drosophila JNK pathway. EMBO J. 21, 3009-3018.
15. Inoue, S., Watanabe, H., Saito, H., Hiroi, M. and Tonosaki, A. (2000). Elimination of atretic follicles from the mouse ovary: a TEM and immunohistochemical study in mice. J. Anat. 196, 103-110.
16. Jones, P., Gardner, L., Menage, J., Williams, G. T. and Roberts, S. (2008). Intervertebral disc cells as competent phagocytes in vitro: implications for cell death in disc degeneration. Arthritis Res. Ther. 10, R86.
17. Kinchen, J. M. (2010). A model to die for: signaling to apoptotic cell removal in worm, fly and mouse. Apoptosis 15, 998-1006.
18. Kinchen, J. M. and Ravichandran, K. S. (2007). Journey to the grave: signaling events regulating removal of apoptotic cells. J. Cell Sci. 120, 2143-2149.
19. Kinchen, J. M., Cabello, J., Klingele, D., Wong, K., Feichtinger, R., Schnabel, H., Schnabel, R. and Hengartner, M. O. (2005). Two pathways converge at CED-10 to mediate actin rearrangement and corpse removal in C. elegans. Nature 434, 93-99.
20. King, R. C. (1970). Ovarian Development in Drosophila melanogaster. New York, NY: Academic Press.
21. Kuraishi, T., Nakagawa, Y., Nagaosa, K., Hashimoto, Y., Ishimoto, T., Moki, T., Fujita, Y., Nakayama, H., Dohmae, N., Shiratsuchi, A. et al. (2009). Pretaporter, a Drosophila protein serving as a ligand for Draper in the phagocytosis of apoptotic cells. EMBO J. 28, 3868-3878.
22. Kurant, E., Axelrod, S., Leaman, D. and Gaul, U. (2008). Six-microns-under acts upstream of Draper in the glial phagocytosis of apoptotic neurons. Cell 133, 498-509.
23. Laundrie, B., Peterson, J. S., Baum, J. S., Chang, J. C., Fileppo, D., Thompson, S. R. and McCall, K. (2003). Germline cell death is inhibited by P-element insertions disrupting the dcp-1/pita nested gene pair in Drosophila. Genetics 165, 1881-1888.
24. Li, W. and Baker, N. E. (2007). Engulfment is required for cell competition. Cell 129, 1215-1225.
25. Lleo, A., Selmi, C., Invernizzi, P., Podda, M. and Gershwin, M. E. (2008). The consequences of apoptosis in autoimmunity. J. Autoimmun. 31, 257-262.
26. Lu, Z., Elliott, M. R., Chen, Y., Walsh, J. T., Klibanov, A. L., Ravichandran, K. S. and Kipnis, J. (2011). Phagocytic activity of neuronal progenitors regulates adult neurogenesis. Nat. Cell Biol. 13, 1076-1083.
27. MacDonald, J. M., Beach, M. G., Porpiglia, E., Sheehan, A. E., Watts, R. J. and Freeman, M. R. (2006). The Drosophila cell corpse engulfment receptor Draper mediates glial clearance of severed axons. Neuron 50, 869-881.
28. Manaka, J., Kuraishi, T., Shiratsuchi, A., Nakai, Y., Higashida, H., Henson, P. and Nakanishi, Y. (2004). Draper-mediated and phosphatidylserineindependent phagocytosis of apoptotic cells by Drosophila hemocytes/macrophages. J. Biol. Chem. 279, 48466-48476.
29. Mangahas, P. M. and Zhou, Z. (2005). Clearance of apoptotic cells in Caenorhabditis elegans. Semin. Cell Dev. Biol. 16, 295-306.
30. Martín-Blanco, E., Gampel, A., Ring, J., Virdee, K., Kirov, N., Tolkovsky, A. M. and Martinez-Arias, A. (1998). Puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure in Drosophila. Genes Dev. 12, 557-570.
31. Mazzalupo, S. and Cooley, L. (2006). Illuminating the role of caspases during Drosophila oogenesis. Cell Death Differ. 13, 1950-1959.
32. McCall, K. (2004). Eggs over easy: cell death in the Drosophila ovary. Dev. Biol. 274, 3-14.
33. McPhee, C. K. and Baehrecke, E. H. (2010). The engulfment receptor Draper is required for autophagy during cell death. Autophagy 6, 1192-1193.
34. McPhee, C. K., Logan, M. A., Freeman, M. R. and Baehrecke, E. H. (2010). Activation of autophagy during cell death requires the engulfment receptor Draper. Nature 465, 1093-1096.
35. Monks, J., Smith-Steinhart, C., Kruk, E. R., Fadok, V. A. and Henson, P. M. (2008). Epithelial cells remove apoptotic epithelial cells during post-lactation involution of the mouse mammary gland. Biol. Reprod. 78, 586-594.
36. Moreno, E., Yan, M. and Basler, K. (2002). Evolution of TNF signaling mechanisms: JNK-dependent apoptosis triggered by Eiger, the Drosophila homolog of the TNF superfamily. Curr. Biol. 12, 1263-1268.
37. Morin, X., Daneman, R., Zavortink, M. and Chia, W. (2001). A protein trap strategy to detect GFP-tagged proteins expressed from their endogenous loci in Drosophila. Proc. Natl. Acad. Sci. USA 98, 15050-15055.
38. Navarre, W. W. and Zychlinsky, A. (2000). Pathogen-induced apoptosis of macrophages: a common end for different pathogenic strategies. Cell. Microbiol. 2, 265-273.
39. Neher, J. J., Neniskyte, U., Zhao, J. W., Bal-Price, A., Tolkovsky, A. M. and Brown, G. C. (2011). Inhibition of microglial phagocytosis is sufficient to prevent inflammatory neuronal death. J. Immunol. 186, 4973-4983.
40. Neniskyte, U., Neher, J. J. and Brown, G. C. (2011). Neuronal death induced by nanomolar amyloid is mediated by primary phagocytosis of neurons by microglia. J. Biol. Chem. 286, 39904-39913.
41. Nezis, I. P., Stravopodis, D. J., Papassideri, I., Robert-Nicoud, M. and Margaritis, L. H. (2000). Stage-specific apoptotic patterns during Drosophila oogenesis. Eur. J. Cell Biol. 79, 610-620.
42. Ohsawa, S., Sugimura, K., Takino, K., Xu, T., Miyawaki, A. and Igaki, T. (2011). Elimination of oncogenic neighbors by JNK-mediated engulfment in Drosophila. Dev. Cell 20, 315-328.
43. Overholtzer, M., Mailleux, A. A., Mouneimne, G., Normand, G., Schnitt, S. J., King, R. W., Cibas, E. S. and Brugge, J. S. (2007). A nonapoptotic cell death process, entosis, that occurs by cell-in-cell invasion. Cell 131, 966-979.
44. Parnaik, R., Raff, M. C. and Scholes, J. (2000). Differences between the clearance of apoptotic cells by professional and non-professional phagocytes. Curr. Biol. 10, 857-860.
45. Patel, V. A., Longacre, A., Hsiao, K., Fan, H., Meng, F., Mitchell, J. E., Rauch, J., Ucker, D. S. and Levine, J. S. (2006). Apoptotic cells, at all stages of the death process, trigger characteristic signaling events that are divergent from and dominant over those triggered by necrotic cells: Implications for the delayed clearance model of autoimmunity. J. Biol. Chem. 281, 4663-4670.
46. Patel, V. A., Lee, D. J., Feng, L., Antoni, A., Lieberthal, W., Schwartz, J. H., Rauch, J., Ucker, D. S. and Levine, J. S. (2010). Recognition of apoptotic cells by epithelial cells: conserved versus tissue-specific signaling responses. J. Biol. Chem. 285, 1829-1840.
47. Peterson, J. S., Barkett, M. and McCall, K. (2003). Stage-specific regulation of caspase activity in drosophila oogenesis. Dev. Biol. 260, 113-123.
48. Pritchett, T. L., Tanner, E. A. and McCall, K. (2009). Cracking open cell death in the Drosophila ovary. Apoptosis 14, 969-79.
49. Reddien, P. W., Cameron, S. and Horvitz, H. R. (2001). Phagocytosis promotes programmed cell death in C. elegans. Nature 412, 198-202.
50. Stronach, B. (2005). Dissecting JNK signaling, one KKKinase at a time. Dev. Dyn. 232, 575-584.
51. Tanner, E. A., Blute, T. A., Brachmann, C. B. and McCall, K. (2011). Bcl-2 proteins and autophagy regulate mitochondrial dynamics during programmed cell death in the Drosophila ovary. Development 138, 327-338.
52. Tran, D. H. and Berg, C. A. (2003). Bullwinkle and shark regulate dorsalappendage morphogenesis in Drosophila oogenesis. Development 130, 6273-6282.
53. Wiegand, U. K., Corbach, S., Prescott, A. R., Savill, J. and Spruce, B. A. (2001). The trigger to cell death determines the efficiency with which dying cells are cleared by neighbours. Cell Death Differ. 8, 734-746.
54. Wu, H., Wang, M. C. and Bohmann, D. (2009). JNK protects Drosophila from oxidative stress by trancriptionally activating autophagy. Mech. Dev. 126, 624-637.
55. Yvan-Charvet, L., Pagler, T. A., Seimon, T. A., Thorp, E., Welch, C. L., Witztum, J. L., Tabas, I. and Tall, A. R. (2010). ABCA1 and ABCG1 protect against oxidative stress-induced macrophage apoptosis during efferocytosis. Circ. Res. 106, 1861-1869.
56. Zhou, Z., Hartwieg, E. and Horvitz, H. R. (2001). CED-1 is a transmembrane receptor that mediates cell corpse engulfment in C. elegans. Cell 104, 43-56.
57. Ziegenfuss, J. S., Biswas, R., Avery, M. A., Hong, K., Sheehan, A. E., Yeung, Y. G., Stanley, E. R. and Freeman, M. R. (2008). Draper-dependent glial phagocytic activity is mediated by Src and Syk family kinase signalling. Nature 453, 935-939.