Defective phagocytic corpse processing results in neurodegeneration and can be rescued by TORC1 activation

Journal of Neuroscience

Volumn 36, Issue 11, 2016, Pages 3170-3183

  Etchegaray, Jon Iker ^a   Elguero, Emma J ^a   Tran, Jennifer A ^a   Sinatra, Vincent ^a   Feany, Mel B ^b   McCall, Kimberly ^a  

^a USA   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Autophagy; Cell death; Drosophila; Glia; Neurodegeneration; Phagocytosis

Indexed keywords

LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; RAB7 PROTEIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL; CAENORHABDITIS ELEGANS PROTEIN; DROSOPHILA PROTEIN; DRPR PROTEIN, DROSOPHILA; DRR-2 PROTEIN, C ELEGANS; GAL4 PROTEIN, DROSOPHILA; INITIATION FACTOR; MEMBRANE PROTEIN; TORC1 PROTEIN COMPLEX, DROSOPHILA; TRANSCRIPTION FACTOR;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; BIOACCUMULATION; CELL MATURATION; CELL PHAGOCYTOSIS; CELL VACUOLE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; FEMALE; GENE EXPRESSION REGULATION; GENE SILENCING; GLIA CELL; HISTOLOGY; HOMEOSTASIS; LIFESPAN; MALE; NERVE DEGENERATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSMISSION ELECTRON MICROSCOPY; TUNEL ASSAY; AGE; ANIMAL; BRAIN; DEFICIENCY; GENETICS; GLIA; LARVA; METABOLISM; NERVE CELL; NONMAMMALIAN EMBRYO; PATHOLOGY; PHAGOCYTOSIS; PHYSIOLOGY; RNA INTERFERENCE; TRANSGENIC ANIMAL; ULTRASTRUCTURE;

AGE FACTORS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; BRAIN; CAENORHABDITIS ELEGANS PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; EUKARYOTIC INITIATION FACTORS; GENE EXPRESSION REGULATION; LARVA; MEMBRANE PROTEINS; NERVE DEGENERATION; NEUROGLIA; NEURONS; PHAGOCYTOSIS; RNA INTERFERENCE; TRANSCRIPTION FACTORS;

EID: 84961262891     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1912-15.2016     Document Type: Article

References (52)

1. Awasaki T, Lai SL, Ito K, Lee T (2008) Organization and postembryonic development of glial cells in the adult central brain of Drosophila. J Neurosci 28:13742–13753. CrossRef Medline
2. Betz C, Hall MN (2013) Where is mTOR and what is it doing there? J Cell Biol 203:563–574. CrossRef Medline
3. Blander JM, Medzhitov R (2006) On regulation of phagosome maturation and antigen presentation. Nat Immunol 7:1029–1035. CrossRef Medline
4. Brand AH, Perrimon N (1993) Targeted gene-expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401–415. Medline
5. Cantoni C, Bollman B, Licastro D, Xie M, Mikesell R, Schmidt R, Yuede CM, Galimberti D, Olivecrona G, Klein RS, Cross AH, Otero K, Piccio L (2015) TREM2 regulates microglial cell activation in response to demyelination in vivo. Acta Neuropathol 129:429–447. CrossRef Medline
6. Celotto AM, Palladino MJ (2005) Drosophila: a “model” model system to study neurodegeneration. Mol Interventions 5:292–303.CrossRef
7. Chung WS, Clarke LE, Wang GX, Stafford BK, Sher A, Chakraborty C, Joung J, Foo LC, Thompson A, Chen C, Smith SJ, Barres BA (2013) Astrocytes mediate synapse elimination through MEGF10 and MERTK pathways. Nature 504:394–400. CrossRef Medline
8. Cunningham CL, Martínez-Cerdeño V, Noctor SC (2013) Microglia regulate the number of neural precursor cells in the developing cerebral cortex. J Neurosci 33:4216–4233. CrossRef Medline
9. Derecki NC, Cronk JC, Lu Z, Xu E, Abbott SB, Guyenet PG, Kipnis J (2012) Wild-type microglia arrest pathology in a mouse model of Rett syndrome. Nature 484:105–105. CrossRef Medline
10. Doherty J, Logan MA, Tasdemir OE, Freeman MR (2009) Ensheathing glia function as phagocytes in the adult Drosophila brain. J Neurosci 29: 4768–4781. CrossRef Medline
11. Doherty J, Sheehan AE, Bradshaw R, Fox AN, Lu TY, Freeman MR (2014) PI3K signaling and Stat92E converge to modulate glial responsiveness to axonal injury. PLoS Biol 12:e1001985. Medline
12. Draper I, Mahoney LJ, Mitsuhashi S, Pacak CA, Salomon RN, Kang PB (2014) Silencing of drpr leads to muscle and brain degeneration in adult Drosophila. Am J Pathol 184:2653–2661. CrossRef Medline
13. Edwards TN, Meinertzhagen IA (2010) The functional organisation of glia in the adult brain of Drosophila and other insects. Prog Neurobiol 90: 471–497. CrossRef Medline
14. Elliott MR, Ravichandran KS (2010) Clearance of apoptotic cells: implications in health and disease. J Cell Biol 189:1059–1070. CrossRef Medline
15. Etchegaray JI, Timmons AK, Klein AP, Pritchett TL, Welch E, Meehan TL, Li C, McCall K (2012) Draper acts through the JNK pathway to control synchronous engulfment of dying germline cells by follicular epithelial cells. Development 139:4029–4039. CrossRef Medline
16. Florey O, Kim SE, Sandoval CP, Haynes CM, Overholtzer M (2011) Autophagy machinery mediates macroendocytic processing and entotic cell death by targeting single membranes. Nat Cell Biol 13:1335–1118. Medline
17. Fratti RA, Backer JM, Gruenberg J, Corvera S, Deretic V (2001) Role of phosphatidylinositol 3-kinase and Rab5 effectors in phagosomal biogenesis and mycobacterial phagosome maturation arrest. J Cell Biol 154: 631–644. CrossRef Medline
18. Freeman MR, Delrow J, Kim J, Johnson E, Doe CQ (2003) Unwrapping glial biology: Gcm target genes regulating glial development, diversification, and function. Neuron 38:567–580. CrossRef Medline
19. Frost B, Hemberg M, Lewis J, Feany MB (2014) Tau promotes neurodegeneration through global chromatin relaxation. Nat Neurosci 17:357–366. CrossRef Medline
20. Fu R, Shen Q, Xu P, Luo JJ, Tang Y (2014) Phagocytosis of microglia in the central nervous system diseases. Mol Neurobiol 49:1422–1434. CrossRef Medline
21. Fullard JF, Kale A, Baker NE (2009) Clearance of apoptotic corpses. Apoptosis 14:1029–1037. CrossRef Medline
22. Gilbert LI (2012) Insect molecular biology and biochemistry, Ed 1. Waltham, MA: Elsevier/Academic.
23. Guerreiro R, Wojtas A, Bras J, Carrasquillo M, Rogaeva E, Majounie E, Cruchaga C, Sassi C, Kauwe JS, Younkin S, Hazrati L, Collinge J, Pocock J, Lashley T, Williams J, Lambert JC, Amouyel P, Goate A, Rademakers R, Morgan K, et al. (2013) TREM2 variants in Alzheimer’s disease. N Engl J Med 368:117–127. CrossRef Medline
24. Han CZ, Ravichandran KS (2011) Metabolic connections during apoptotic cell engulfment. Cell 147:1442–1445. CrossRef Medline
25. Hegde VR, Vogel R, Feany MB (2014) Glia are critical for the neuropathology of complex I deficiency in Drosophila. Hum Mol Genet 23:4686–4692. CrossRef Medline
26. Hochreiter-Hufford A, Ravichandran KS (2013) Clearing the dead: apoptotic cell sensing, recognition, engulfment, and digestion. Cold Spring Harbor Perspect Biol 5:a008748. CrossRef
27. Ito K, Shinomiya K, Ito M, Armstrong JD, Boyan G, Hartenstein V, Harzsch S, Heisenberg M, Homberg U, Jenett A, Keshishian H, Restifo LL, Rössler W, Simpson JH, Strausfeld NJ, Strauss R, Vosshall LB, Grp IBNW (2014) A systematic nomenclature for the Insect Brain. Neuron 81:755–765. CrossRef Medline
28. Jonsson T, Stefansson H, Steinberg S, Jonsdottir I, Jonsson PV, Snaedal J, Bjornsson S, Huttenlocher J, Levey AI, Lah JJ, Rujescu D, Hampel H, Giegling I, Andreassen OA, Engedal K, Ulstein I, Djurovic S, Ibrahim- Verbaas C, Hofman A, Ikram MA, et al. (2013) Variant of TREM2 associated with the risk of Alzheimer’s disease. N Engl J Med 368:107–116. CrossRef Medline
29. Kauwe JS, Bailey MH, Ridge PG, Perry R, Wadsworth ME, Hoyt KL, Staley LA, Karch CM, Harari O, Cruchaga C, Ainscough BJ, Bales K, Pickering EH, Bertelsen S, Fagan AM, Holtzman DM, Morris JC, Goate AM, Neuroimaging AD (2014) Genome-wide association study of CSF levels of 59 Alzheimer’s disease candidate proteins: significant associations with proteins involved in amyloid processing and inflammation. Plos Genet 10:e1004758. CrossRef.
30. Kinchen JM, Ravichandran KS (2010) Identification of two evolutionarily conserved genes regulating processing of engulfed apoptotic cells. Nature 464:778–782. CrossRef Medline
31. Kinchen JM, Doukoumetzidis K, Almendinger J, Stergiou L, Tosello- Trampont A, Sifri CD, Hengartner MO, Ravichandran KS (2008) A pathway for phagosome maturation during engulfment of apoptotic cells. Nat Cell Biol 10:556–566. CrossRef Medline
32. Kurant E, Axelrod S, Leaman D, Gaul U (2008) Six-microns-under acts upstream of draper in the glial phagocytosis of apoptotic neurons. Cell 133:498–509. CrossRef Medline
33. Li W, Zou W, Yang Y, Chai Y, Chen B, Cheng S, Tian D, Wang X, Vale RD, Ou G (2012) Autophagy genes function sequentially to promote apoptotic cell corpse degradation in the engulfing cell. J Cell Biol 197:27–35. CrossRef Medline
34. Logan MA, Hackett R, Doherty J, Sheehan A, Speese SD, Freeman MR (2012) Negative regulation of glial engulfment activity by Draper terminates glial responses to axon injury. Nat Neurosci 15:722–730. CrossRef Medline
35. Lu N, Zhou Z (2012) Membrane trafficking and phagosome maturation during the clearance of apoptotic cells. Int Rev Cel Mol Biol 293:269–309. CrossRef
36. Lu Z, Elliott MR, Chen Y, Walsh JT, Klibanov AL, Ravichandran KS, Kipnis J (2011) Phagocytic activity of neuronal progenitors regulates adult neurogenesis. Nat Cell Biol 13:1076–1083. CrossRef Medline
37. MacDonald JM, Beach MG, Porpiglia E, Sheehan AE, Watts RJ, Freeman MR (2006) The Drosophila cell corpse engulfment receptor draper mediates glial clearance of severed axons. Neuron 50:869–881. CrossRef Medline
38. Martinez J, Almendinger J, Oberst A, Ness R, Dillon CP, Fitzgerald P, Hengartner MO, Green DR (2011) Microtubule-associated protein 1 light chain 3 alpha (LC3)-associated phagocytosis is required for the efficient clearance of dead cells. Proc Natl Acad Sci U S A 108:17396–17401. CrossRef Medline
39. McGuire SE, Le PT, Osborn AJ, Matsumoto K, Davis RL (2003) Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302: 1765–1768. CrossRef Medline
40. McPhee CK, Logan MA, Freeman MR, Baehrecke EH (2010) Activation of autophagy during cell death requires the engulfment receptor Draper. Nature 465:1093–1096. Medline
41. Oldfors A, Sourander P, Armstrong DL, Percy AK, Witt-Engerström I, Hagberg BA (1990) Rett syndrome—Cerebellar Pathology. Pediatr Neurol 6:310–314. CrossRef Medline
42. Poon IK, Lucas CD, Rossi AG, Ravichandran KS (2014) Apoptotic cell clearance: basic biology and therapeutic potential. Nat Rev Immunol 14: 166–180. CrossRef Medline
43. Savill J, Dransfield I, Gregory C, Haslett C (2002) A blast from the past: clearance of apoptotic cells regulates immune responses. Nat Rev Immunol 2:965–975. CrossRef Medline
44. Scheib JL, Sullivan CS, Carter BD (2012) Jedi-1 and MEGF10 signal engulfment of apoptotic neurons through the tyrosine kinase Syk. J Neurosci 32:13022–13031. CrossRef Medline
45. Shulman JM, Shulman LM, Weiner WJ, Feany MB (2003) From fruit fly to bedside: translating lessons from Drosophila models of neurodegenerative disease. Curr Opin Neurol 16:443–449. Medline
46. Sierra A, Abiega O, Shahraz A, Neumann H (2013) Janus-faced microglia: beneficial and detrimental consequences of microglial phagocytosis. Front Cell Neurosci 7:6. Medline
47. Song Z, McCall K, Steller H (1997) DCP-1, a Drosophila cell death protease essential for development. Science 275:536–540. CrossRef Medline
48. Venkatachalam K, Long AA, Elsaesser R, Nikolaeva D, Broadie K, Montell C (2008) Motor deficit in a Drosophila model of mucolipidosis type IV due to defective clearance of apoptotic cells. Cell 135:838–851. CrossRef Medline
49. Wong CO, Li R, Montell C, Venkatachalam K (2012) Drosophila TRPML is required for TORC1 activation. Curr Biol 22:1616–1621. CrossRef Medline
50. Yu XM, Lu N, Zhou Z (2008) Phagocytic receptor CED-1 initiates a signaling pathway for degrading engulfed apoptotic cells. PLoS Biol 6:e61. Medline
51. Yvan-Charvet L, Pagler TA, Seimon TA, Thorp E, Welch CL, Witztum JL, Tabas I, Tall AR (2010) ABCA1 and ABCG1 protect against oxidative stress-induced macrophage apoptosis during efferocytosis. Circ Res 106: 1861–1869. CrossRef
52. Ziegenfuss JS, Doherty J, Freeman MR (2012) Distinct molecular pathways mediate glial activation and engulfment of axonal debris after axotomy. Nat Neurosci 15:979–987. CrossRef Medline