The c-Jun kinase signaling cascade promotes glial engulfment activity through activation of draper and phagocytic function

Cell Death and Differentiation

Volumn 20, Issue 9, 2013, Pages 1140-1148

  MacDonald, J M ^a   Doherty, J ^a   Hackett, R ^a   Freeman, M R ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

dJNK; Engulfment; neurodegeneration

Indexed keywords

CELL RECEPTOR; DRAPER RECEPTOR; DROSOPHILA PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE SLIPPER; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AXONAL INJURY; COMPLEX FORMATION; CONTROLLED STUDY; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; GLIA CELL; IN VIVO STUDY; NERVE FIBER DEGENERATION; NERVE FIBER TRANSECTION; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; APOPTOSIS; AXONS; AXOTOMY; BRAIN; BRAIN INJURIES; DROSOPHILA; DROSOPHILA PROTEINS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE KINASE 4; MAP KINASE KINASE KINASES; MEMBRANE PROTEINS; NEUROGLIA; PHAGOCYTOSIS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR AP-1;

EID: 84882276428     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2013.30     Document Type: Article

References (38)

1. Gumienny TL, Hengartner MO. How the worm removes corpses: the nematode C. Elegans as a model system to study engulfment. Cell Death Differ 2001; 8: 564-568.
2. Giorgi F, Deri P. Cell death in ovarian chambers of Drosophila melanogaster. J Embryol Exp Morphol 1976; 35: 521-533.
3. Sears HC, Kennedy CJ, Garrity PA. Macrophage-mediated corpse engulfment is required for normal Drosophila CNS morphogenesis. Development 2003; 130: 3557-3565.
4. Aldskogius H, Kozlova EN. Central neuron-glial and glial-glial interactions following axon injury. Prog Neurobiol 1998; 55: 1-26.
5. Sofroniew MV. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 2009; 32: 638-647.
6. Zamanian JL, Xu L, Foo LC, Nouri N, Zhou L, Giffard RG et al. Genomic analysis of reactive astrogliosis. J Neurosci 2012; 32: 6391-6410.
7. Murray M, Wang SD, Goldberger ME, Levitt P. Modification of astrocytes in the spinal cord following dorsal root or peripheral nerve lesions. Exp Neurol 1990; 110: 248-357.
8. Gerber YN, Sabourin JC, Rabano M, Vivanco MD, Perrin FE. Early functional deficit and microglial disturbances in a mouse model of amyotrophiclateral sclerosis. PLoS One 2012; 7: e36000.
9. Perry VH, Nicoll JA, Holmes CM. Microglia in neurodegenerative disease. Nat Rev Neurol 2010; 6: 193-201.
10. Loane DJ, Byrnes KR. Role of microglia in neurotrauma. Neurotherapeutics 2010; 7: 366-377.
11. Nedergaard M, Dirnagl U. Role of glial cells in cerebral ischemia. Glia 2005; 50: 281-286.
12. Freeman MR, Delrow J, Kim J, Johnson E, Doe CQ. Unwrapping glial biology: Gcm target genes regulating glial development, diversification, and function. Neuron 2003; 38: 567-580.
13. MacDonald JM, Beach MG, Porpiglia E, Sheehan AE, Watts RJ, Freeman MR. The Drosophila cell corpse engulfment receptor Draper mediates glial clearance of severed axons. Neuron 2006; 50: 869-881.
14. Zhou Z, Hartwieg E, Horvitz HR. CED-1 is a transmembrane receptor that mediates cell corpse engulfment in C. Elegans. Cell 2001; 104: 43-56.
15. Logan MA, Hackett R, Doherty J, Sheehan A, Speese SD, Freeman MR. Negative regulation of glial engulfment activity by Draper terminates glial responses to axon injury. Nat Neurosci 2012; 15: 722-730.
16. Ziegenfuss JS, Biswas R, Avery MA, Hong K, Sheehan AE, Yeung YG et al. Draperdependent glial phagocytic activity is mediated by Src and Syk family kinase signalling. Nature 2008; 453: 935-939.
17. Liu QA, Hengartner MO. Candidate adaptor protein CED-6 promotes the engulfment of apoptotic cells in C. Elegans. Cell 1998; 93: 961-972.
18. Martin-Blanco E, Gampel A, Ring J, Virdee K, Kirov N, Tolkovsky AM et al. Puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure in Drosophila. Genes Dev 1998; 12: 557-570.
19. Doherty J, Logan MA, Taşdemir OE, Freeman MR. Ensheathing glia function as phagocytes in the adult Drosophila brain. J Neurosci 2009; 29: 4768-4781.
20. Stronach B. Dissecting JNK signaling, one KKKinase at a time. Dev Dyn 2005; 232: 575-584.
21. Chatterjee N, Bohmann DA. Versatile FC31 based reporter system for measuring AP-1 and Nrf2 signaling in Drosophila and in tissue culture. PLoS One 2012; 7: e34063.
22. Ziegenfuss JS, Doherty J, Freeman MR. Distinct molecular pathways mediate glial activation and engulfment of axonal debris after axotomy. Nat Neurosci 2012; 15: 979-987.
23. Nagata K, Lamarche N, Hall A. A new rac target POSH is an SH3-containing scaffold protein involved in the JNK and NF-kB signalling pathways. EMBO J 1998; 17: 1395-1404.
24. Teramoto H, Coso OA, Miyata H, Igishi T, Miki T, Gutkind JS. Signaling from the small GTP-binding proteins Rac1 and Cdc42 to the c-Jun N-terminal kinase/stress-activated protein kinase pathway. A role for mixed lineage kinase 3/protein-tyrosine kinase 1, a novel member of the mixed lineage kinase family. J. Biol Chem 1996; 271: 27225-27228.
25. Tateno M, Nishida Y, Adachi-Yamada T. Regulation of JNK by Src during Drosophila development. Science 2000; 287: 324-327.
26. Ma W, Quirion R. Partial sciatic nerve ligation induces increase in the phosphorylation of extracellular signal-regulated kinase (ERK) and c-Jun N-terminal kinase (JNK) in astrocytes in the lumbar spinal dorsal horn and the gracile nucleus. Pain 2002; 99: 175-184.
27. Tang G, Xu Z, Goldman JE. Synergistic effects of the SAPK/JNK and the proteasome pathway on glial fibrillary acidic protein (GFAP) accumulation in Alexander disease. J Biol Chem 2006; 281: 38634-38643.
28. Gadea A, Schinelli S, Gallo V. Endothelin-1 regulates astrocyte proliferation and reactive gliosis via a JNK/c-Jun signaling pathway. J Neurosci 2008; 28: 2394-2408.
29. Kim KC, Hyun Joo S, Shin CY. CPEB1 modulates lipopolysaccharide-mediated iNOS induction in rat primary astrocytes. Biochem Biophys Res Commun 2011; 409: 687-692.
30. Yang DP, Kim J, Syed N, Tung YJ, Bhaskaran A, Mindos T et al. p38 MAPK activation promotes denervated Schwann cell phenotype and functions as a negative regulator of Schwann cell differentiation and myelination. J Neurosci 2012; 32: 7158-7168.
31. Barrette B, Calvo E, Valliè res N, Lacroix S. Transcriptional profiling of the injured sciatic nerve of mice carrying the Wld(S) mutant gene: identification of genes involved in neuroprotection, neuroinflammation, and nerve regeneration. Brain Behav Immun 2010; 24: 1254-1267.
32. Leiserson WM, Harkins EW, Keshishian H. Fray, a Drosophila serine/threonine kinase homologous to mammalian PASK, is required for axonal ensheathment. Neuron 2000; 28: 793-806.
33. Ito K, Urban J, Technau GM. Distribution, classification, and development of Drosophila glial cells in the late embryonic and early larval ventral nerve cord. Roux's Arch Dev Biol 1995; 204: 284-307.
34. Lee T, Luo L. Mosaic analysis with a repressible cell marker (MARCM) for Drosophila neural development. Trends Neurosci 2001; 24: 251-254.
35. Dobritsa AA, Van der Goes van Naters W, Warr CG, Steinbrecht RA, Carlson JR. Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 2003; 37: 827-841.
36. Dietzl G, Chen D, Schnorrer F, Su KC, Barinova Y, Fellner M et al. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 2007; 448: 151-156.
37. Vosshall LB, Wong AM, Axel R. An olfactory sensory map in the fly brain. Cell 2000; 102: 147-159.
38. Awasaki T, Tatsumi R, Takahashi K, Arai K, Nakanishi Y, Ueda R et al. Essential role of the apoptotic cell engulfment genes draper and ced-6 in programmed axon pruning during Drosophila metamorphosis. Neuron 2006; 50: 855-867