Epidermal Cells Are the Primary Phagocytes in the Fragmentation and Clearance of Degenerating Dendrites in Drosophila

Neuron

Volumn 81, Issue 3, 2014, Pages 544-560

  Han, Chun ^a,c   Song, Yuanquan ^a   Xiao, Hui ^b   Wang, Denan ^a   Franc, Nathalie C ^b   Yeh Jan, Lily ^a   Jan, Yuh Nung ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c School of Integrative Plant Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIGENS, CD36; DENDRITES; DROSOPHILA; DROSOPHILA PROTEINS; EPIDERMIS; EPITHELIAL CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LARVA; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; MUTATION; NERVE DEGENERATION; PHAGOCYTOSIS; PUPA; RECEPTORS, SCAVENGER; RNA INTERFERENCE; SENSORY RECEPTOR CELLS; TIME FACTORS;

EID: 84893438166     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.11.021     Document Type: Article

References (70)

1. Aldskogius H., Kozlova E.N. Central neuron-glial and glial-glial interactions following axon injury. Prog. Neurobiol. 1998, 55:1-26.
2. Allen L.A., Schlesinger L.S., Kang B. Virulent strains of Helicobacter pylori demonstrate delayed phagocytosis and stimulate homotypic phagosome fusion in macrophages. J.Exp. Med. 2000, 191:115-128.
3. Awasaki T., Ito K. Engulfing action of glial cells is required for programmed axon pruning during Drosophila metamorphosis. Curr. Biol. 2004, 14:668-677.
4. Awasaki T., Tatsumi R., Takahashi K., Arai K., Nakanishi Y., Ueda R., Ito K. Essential role of the apoptotic cell engulfment genes draper and ced-6 in programmed axon pruning during Drosophila metamorphosis. Neuron 2006, 50:855-867.
5. Babcock D.T., Brock A.R., Fish G.S., Wang Y., Perrin L., Krasnow M.A., Galko M.J. Circulating blood cells function as a surveillance system for damaged tissue in Drosophila larvae. Proc. Natl. Acad. Sci. USA 2008, 105:10017-10022.
6. Botelho R.J., Grinstein S. Phagocytosis. Curr. Biol. 2011, 21:R533-R538.
7. Braun A., Hoffmann J.A., Meister M. Analysis of the Drosophila host defense in domino mutant larvae, which are devoid of hemocytes. Proc. Natl. Acad. Sci. USA 1998, 95:14337-14342.
8. Carrasco-Marín E., Fernández-Prieto L., Rodriguez-Del Rio E., Madrazo-Toca F., Reinheckel T., Saftig P., Alvarez-Dominguez C. LIMP-2 links late phagosomal trafficking with the onset of the innate immune response to Listeria monocytogenes: a role in macrophage activation. J.Biol. Chem. 2011, 286:3332-3341.
9. Conradt B. With a little help from your friends: cells don't die alone. Nat. Cell Biol. 2002, 4:E139-E143.
10. Cuttell L., Vaughan A., Silva E., Escaron C.J., Lavine M., Van Goethem E., Eid J.P., Quirin M., Franc N.C. Undertaker, a Drosophila Junctophilin, links Draper-mediated phagocytosis and calcium homeostasis. Cell 2008, 135:524-534.
11. Doherty J., Logan M.A., Taşdemir O.E., Freeman M.R. Ensheathing glia function as phagocytes in the adult Drosophila brain. J.Neurosci. 2009, 29:4768-4781.
12. Dubois L., Lecourtois M., Alexandre C., Hirst E., Vincent J.P. Regulated endocytic routing modulates wingless signaling in Drosophila embryos. Cell 2001, 105:613-624.
13. Etchegaray J.I., Timmons A.K., Klein A.P., Pritchett T.L., Welch E., Meehan T.L., Li C., McCall K. Draper acts through the JNK pathway to control synchronous engulfment of dying germline cells by follicular epithelial cells. Development 2012, 139:4029-4039.
14. Franc N.C., Dimarcq J.L., Lagueux M., Hoffmann J., Ezekowitz R.A. Croquemort, a novel Drosophila hemocyte/macrophage receptor that recognizes apoptotic cells. Immunity 1996, 4:431-443.
15. Franc N.C., Heitzler P., Ezekowitz R.A., White K. Requirement for croquemort in phagocytosis of apoptotic cells in Drosophila. Science 1999, 284:1991-1994.
16. Frank-Cannon T.C., Alto L.T., McAlpine F.E., Tansey M.G. Does neuroinflammation fan the flame in neurodegenerative diseases?. Mol. Neurodegener. 2009, 4:47.
17. Fuentes-Medel Y., Logan M.A., Ashley J., Ataman B., Budnik V., Freeman M.R. Glia and muscle sculpt neuromuscular arbors by engulfing destabilized synaptic boutons and shed presynaptic debris. PLoS Biol. 2009, 7:e1000184.
18. Gong W.J., Golic K.G. Ends-out, or replacement, gene targeting in Drosophila. Proc. Natl. Acad. Sci. USA 2003, 100:2556-2561.
19. Hall S. The response to injury in the peripheral nervous system. J.Bone Joint Surg. Br. 2005, 87:1309-1319.
20. Han C., Jan L.Y., Jan Y.N. Enhancer-driven membrane markers for analysis of nonautonomous mechanisms reveal neuron-glia interactions in Drosophila. Proc. Natl. Acad. Sci. USA 2011, 108:9673-9678.
21. Han C., Wang D., Soba P., Zhu S., Lin X., Jan L.Y., Jan Y.N. Integrins regulate repulsion-mediated dendritic patterning of Drosophila sensory neurons by restricting dendrites in a 2D space. Neuron 2012, 73:64-78.
22. Huynh K.K., Eskelinen E.L., Scott C.C., Malevanets A., Saftig P., Grinstein S. LAMP proteins are required for fusion of lysosomes with phagosomes. EMBO J. 2007, 26:313-324.
23. Inoue S., Watanabe H., Saito H., Hiroi M., Tonosaki A. Elimination of atretic follicles from the mouse ovary: a TEM and immunohistochemical study in mice. J.Anat. 2000, 196:103-110.
24. Ishizaki Y., Voyvodic J.T., Burne J.F., Raff M.C. Control of lens epithelial cell survival. J.Cell Biol. 1993, 121:899-908.
25. Katayama H., Yamamoto A., Mizushima N., Yoshimori T., Miyawaki A. GFP-like proteins stably accumulate in lysosomes. Cell Struct. Funct. 2008, 33:1-12.
26. Kiehart D.P., Galbraith C.G., Edwards K.A., Rickoll W.L., Montague R.A. Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila. J.Cell Biol. 2000, 149:471-490.
27. Kim M.E., Shrestha B.R., Blazeski R., Mason C.A., Grueber W.B. Integrins establish dendrite-substrate relationships that promote dendritic self-avoidance and patterning in Drosophila sensory neurons. Neuron 2012, 73:79-91.
28. Kinchen J.M., Ravichandran K.S. Phagosome maturation: going through the acid test. Nat. Rev. Mol. Cell Biol. 2008, 9:781-795.
29. Krieger M. Charting the fate of the "good cholesterol": identification and characterization of the high-density lipoprotein receptor SR-BI. Annu. Rev. Biochem. 1999, 68:523-558.
30. Kuo C.T., Jan L.Y., Jan Y.N. Dendrite-specific remodeling ofDrosophila sensory neurons requires matrix metalloproteases, ubiquitin-proteasome, and ecdysone signaling. Proc. Natl. Acad. Sci. USA 2005, 102:15230-15235.
31. Kurant E., Axelrod S., Leaman D., Gaul U. Six-microns-under acts upstream of Draper in the glial phagocytosis of apoptotic neurons. Cell 2008, 133:498-509.
32. Kuronita T., Eskelinen E.L., Fujita H., Saftig P., Himeno M., Tanaka Y. A role for the lysosomal membrane protein LGP85 in the biogenesis and maintenance of endosomal and lysosomal morphology. J.Cell Sci. 2002, 115:4117-4131.
33. Lee H.H., Jan L.Y., Jan Y.N. Drosophila IKK-related kinase Ik2 and Katanin p60-like 1 regulate dendrite pruning of sensory neuron during metamorphosis. Proc. Natl. Acad. Sci. USA 2009, 106:6363-6368.
34. Li W., Baker N.E. Engulfment is required for cell competition. Cell 2007, 129:1215-1225.
35. Lorenzi R., Brickell P.M., Katz D.R., Kinnon C., Thrasher A.J. Wiskott-Aldrich syndrome protein is necessary for efficient IgG-mediated phagocytosis. Blood 2000, 95:2943-2946.
36. Luo L., O'Leary D.D. Axon retraction and degeneration in development and disease. Annu. Rev. Neurosci. 2005, 28:127-156.
37. MacDonald J.M., Beach M.G., Porpiglia E., Sheehan A.E., Watts R.J., Freeman M.R. The Drosophila cell corpse engulfment receptor Draper mediates glial clearance of severed axons. Neuron 2006, 50:869-881.
38. Majeed M., Krause K.H., Clark R.A., Kihlström E., Stendahl O. Localization of intracellular Ca2+ stores in HeLa cells during infection with Chlamydia trachomatis. J.Cell Sci. 1999, 112:35-44.
39. Makhijani K., Alexander B., Tanaka T., Rulifson E., Brückner K. The peripheral nervous system supports blood cell homing and survival in the Drosophila larva. Development 2011, 138:5379-5391.
40. Marín-Teva J.L., Dusart I., Colin C., Gervais A., van Rooijen N., Mallat M. Microglia promote the death of developing Purkinje cells. Neuron 2004, 41:535-547.
41. Meister M. Blood cells of Drosophila: cell lineages and role in host defence. Curr. Opin. Immunol. 2004, 16:10-15.
42. Miesenböck G., De Angelis D.A., Rothman J.E. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 1998, 394:192-195.
43. Nichols Z., Vogt R.G. The SNMP/CD36 gene family in Diptera, Hymenoptera and Coleoptera: Drosophila melanogaster, D. pseudoobscura, Anopheles gambiae, Aedes aegypti, Apis mellifera, and Tribolium castaneum. Insect Biochem. Mol. Biol. 2008, 38:398-415.
44. Parrish J.Z., Xu P., Kim C.C., Jan L.Y., Jan Y.N. The microRNA bantam functions in epithelial cells to regulate scaling growth of dendrite arbors in Drosophila sensory neurons. Neuron 2009, 63:788-802.
45. Philips J.A., Rubin E.J., Perrimon N. Drosophila RNAi screen reveals CD36 family member required for mycobacterial infection. Science 2005, 309:1251-1253.
46. Pulipparacharuvil S., Akbar M.A., Ray S., Sevrioukov E.A., Haberman A.S., Rohrer J., Krämer H. Drosophila Vps16A is required for trafficking to lysosomes and biogenesis of pigment granules. J.Cell Sci. 2005, 118:3663-3673.
47. Rabinovitch M. Professional and non-professional phagocytes: an introduction. Trends Cell Biol. 1995, 5:85-87.
48. Rieder S.E., Emr S.D. A novel RING finger protein complex essential for a late step in protein transport to the yeast vacuole. Mol. Biol. Cell 1997, 8:2307-2327.
49. 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. 1992, 90:1513-1522.
50. Saxena S., Caroni P. Mechanisms of axon degeneration: from development to disease. Prog. Neurobiol. 2007, 83:174-191.
51. Schwartz J.T., Allen L.A. Role of urease in megasome formation and Helicobacter pylori survival in macrophages. J.Leukoc. Biol. 2006, 79:1214-1225.
52. Silverstein R.L., Febbraio M. CD36, a scavenger receptor involved in immunity, metabolism, angiogenesis, and behavior. Sci. Signal. 2009, 2:re3.
53. Song J.W., Misgeld T., Kang H., Knecht S., Lu J., Cao Y., Cotman S.L., Bishop D.L., Lichtman J.W. Lysosomal activity associated with developmental axon pruning. J.Neurosci. 2008, 28:8993-9001.
54. Song Y., Ori-McKenney K.M., Zheng Y., Han C., Jan L.Y., Jan Y.N. Regeneration of Drosophila sensory neuron axons and dendrites is regulated by the Akt pathway involving Pten and microRNA bantam. Genes Dev. 2012, 26:1612-1625.
55. Stuart L.M., Ezekowitz R.A. Phagocytosis and comparative innate immunity: learning on the fly. Nat. Rev. Immunol. 2008, 8:131-141.
56. Stuart L.M., Deng J., Silver J.M., Takahashi K., Tseng A.A., Hennessy E.J., Ezekowitz R.A., Moore K.J. Response to Staphylococcus aureus requires CD36-mediated phagocytosis triggered by the COOH-terminal cytoplasmic domain. J.Cell Biol. 2005, 170:477-485.
57. Tao J., Rolls M.M. Dendrites have a rapid program of injury-induced degeneration that is molecularly distinct from developmental pruning. J.Neurosci. 2011, 31:5398-5405.
58. Tepass U., Fessler L.I., Aziz A., Hartenstein V. Embryonic origin of hemocytes and their relationship to cell death in Drosophila. Development 1994, 120:1829-1837.
59. Valacchi G., Sticozzi C., Lim Y., Pecorelli A. Scavenger receptor class B type I: a multifunctional receptor. Ann. N Y Acad. Sci. 2011, 1229:E1-E7.
60. Verkhusha V.V., Kuznetsova I.M., Stepanenko O.V., Zaraisky A.G., Shavlovsky M.M., Turoverov K.K., Uversky V.N. High stability of Discosoma DsRed as compared to Aequorea EGFP. Biochemistry 2003, 42:7879-7884.
61. Watts R.J., Schuldiner O., Perrino J., Larsen C., Luo L. Glia engulf degenerating axons during developmental axon pruning. Curr. Biol. 2004, 14:678-684.
62. Williams D.W., Truman J.W. Cellular mechanisms of dendrite pruning in Drosophila: insights from invivo time-lapse of remodeling dendritic arborizing sensory neurons. Development 2005, 132:3631-3642.
63. Williams D.W., Kondo S., Krzyzanowska A., Hiromi Y., Truman J.W. Local caspase activity directs engulfment of dendrites during pruning. Nat. Neurosci. 2006, 9:1234-1236.
64. Wood W., Turmaine M., Weber R., Camp V., Maki R.A., McKercher S.R., Martin P. Mesenchymal cells engulf and clear apoptotic footplate cells in macrophageless PU.1 null mouse embryos. Development 2000, 127:5245-5252.
65. Wucherpfennig T., Wilsch-Bräuninger M., González-Gaitán M. Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. J.Cell Biol. 2003, 161:609-624.
66. Young R.W., Bok D. Participation of the retinal pigment epithelium in the rod outer segment renewal process. J.Cell Biol. 1969, 42:392-403.
67. 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 2006, 10:743-757.
68. Zhang J., Shehabeldin A., da Cruz L.A., Butler J., Somani A.K., McGavin M., Kozieradzki I., dos Santos A.O., Nagy A., Grinstein S., et al. Antigen receptor-induced activation and cytoskeletal rearrangement are impaired in Wiskott-Aldrich syndrome protein-deficient lymphocytes. J.Exp. Med. 1999, 190:1329-1342.
69. Zhou Z., Yu X. Phagosome maturation during the removal of apoptotic cells: receptors lead the way. Trends Cell Biol. 2008, 18:474-485.
70. Zhou Z., Hartwieg E., Horvitz H.R. CED-1 is a transmembrane receptor that mediates cell corpse engulfment in C. elegans. Cell 2001, 104:43-56.