#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Maintenance of Glia in the Optic Lamina Is Mediated by EGFR Signaling by Photoreceptors in Adult Drosophila


Degeneration of the nervous system can be viewed as a failure to maintain cell survival or function in the nervous system. The late onset of neurodegeneration in humans indicates that the cell survival in the nervous system must be maintained throughout our lives. Neuronal survival is maintained by neurotrophic factors in adults; however, it is unclear whether glia survival is also maintained throughout adulthood. Here, we use the Drosophila visual system as a model to address the role played by adult neurons for the active maintenance of glia. We demonstrated that the adult photoreceptors secrete a signaling molecule, which is transported to the brain to act on the lamina glia and maintain its integrity. When this signaling pathway is blocked, the lamina glia undergoes a progressive and irreversible degeneration. The primary defect occurs in the trafficking from the late endosome and autophagosome to the lysosome. This defect leads to an accumulation of autophagosomes and subsequent cell degeneration as a result of autophagy. Our findings provide in vivo evidence for a novel aspect of the neuron-glia interaction and a novel role for EGFR signaling in regulating the maintenance and degeneration of the nervous system.


Vyšlo v časopise: Maintenance of Glia in the Optic Lamina Is Mediated by EGFR Signaling by Photoreceptors in Adult Drosophila. PLoS Genet 11(4): e32767. doi:10.1371/journal.pgen.1005187
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005187

Souhrn

Degeneration of the nervous system can be viewed as a failure to maintain cell survival or function in the nervous system. The late onset of neurodegeneration in humans indicates that the cell survival in the nervous system must be maintained throughout our lives. Neuronal survival is maintained by neurotrophic factors in adults; however, it is unclear whether glia survival is also maintained throughout adulthood. Here, we use the Drosophila visual system as a model to address the role played by adult neurons for the active maintenance of glia. We demonstrated that the adult photoreceptors secrete a signaling molecule, which is transported to the brain to act on the lamina glia and maintain its integrity. When this signaling pathway is blocked, the lamina glia undergoes a progressive and irreversible degeneration. The primary defect occurs in the trafficking from the late endosome and autophagosome to the lysosome. This defect leads to an accumulation of autophagosomes and subsequent cell degeneration as a result of autophagy. Our findings provide in vivo evidence for a novel aspect of the neuron-glia interaction and a novel role for EGFR signaling in regulating the maintenance and degeneration of the nervous system.


Zdroje

1. Sofroniew MV, Howe CL, Mobley WC. Nerve growth factor signaling, neuroprotection, and neural repair. Annual review of neuroscience. 2001;24:1217–81. 11520933

2. Mattson MP. Glutamate and neurotrophic factors in neuronal plasticity and disease. Annals of the New York Academy of Sciences. 2008;1144:97–112. doi: 10.1196/annals.1418.005 19076369

3. Zhu B, Pennack JA, McQuilton P, Forero MG, Mizuguchi K, Sutcliffe B, et al. Drosophila neurotrophins reveal a common mechanism for nervous system formation. PLoS biology. 2008;6(11):e284. doi: 10.1371/journal.pbio.0060284 19018662

4. Sutcliffe B, Forero MG, Zhu B, Robinson IM, Hidalgo A. Neuron-type specific functions of DNT1, DNT2 and Spz at the Drosophila neuromuscular junction. PloS one. 2013;8(10):e75902. doi: 10.1371/journal.pone.0075902 24124519

5. McIlroy G, Foldi I, Aurikko J, Wentzell JS, Lim MA, Fenton JC, et al. Toll-6 and Toll-7 function as neurotrophin receptors in the Drosophila melanogaster CNS. Nature neuroscience. 2013;16(9):1248–56. doi: 10.1038/nn.3474 23892553

6. Hidalgo A, Kinrade EF, Georgiou M. The Drosophila neuregulin vein maintains glial survival during axon guidance in the CNS. Developmental cell. 2001;1(5):679–90. 11709188

7. Althaus HH, Richter-Landsberg C. Glial cells as targets and producers of neurotrophins. International review of cytology. 2000;197:203–77. 10761118

8. Althaus HH, Kloppner S, Klopfleisch S, Schmitz M. Oligodendroglial cells and neurotrophins: a polyphonic cantata in major and minor. Journal of molecular neuroscience: MN. 2008;35(1):65–79. doi: 10.1007/s12031-008-9053-y 18327658

9. Sharif A, Legendre P, Prevot V, Allet C, Romao L, Studler JM, et al. Transforming growth factor alpha promotes sequential conversion of mature astrocytes into neural progenitors and stem cells. Oncogene. 2007;26(19):2695–706. 17057735

10. Lecca D, Ceruti S, Fumagalli M, Abbracchio MP. Purinergic trophic signalling in glial cells: functional effects and modulation of cell proliferation, differentiation, and death. Purinergic signalling. 2012;8(3):539–57. doi: 10.1007/s11302-012-9310-y 22528683

11. Stemerdink C, Jacobs JR. Argos and Spitz group genes function to regulate midline glial cell number in Drosophila embryos. Development. 1997;124(19):3787–96. 9367434

12. Bergmann A, Tugentman M, Shilo BZ, Steller H. Regulation of cell number by MAPK-dependent control of apoptosis: a mechanism for trophic survival signaling. Developmental cell. 2002;2(2):159–70. 11832242

13. Learte AR, Hidalgo A. The role of glial cells in axon guidance, fasciculation and targeting. Advances in experimental medicine and biology. 2007;621:156–66. doi: 10.1007/978-0-387-76715-4_12 18269218

14. Fischer JA, Eun SH, Doolan BT. Endocytosis, endosome trafficking, and the regulation of Drosophila development. Annual review of cell and developmental biology. 2006;22:181–206. 16776558

15. Marmor MD, Yarden Y. Role of protein ubiquitylation in regulating endocytosis of receptor tyrosine kinases. Oncogene. 2004;23(11):2057–70. 15021893

16. Sepp KJ, Schulte J, Auld VJ. Peripheral glia direct axon guidance across the CNS/PNS transition zone. Developmental biology. 2001;238(1):47–63. 11783993

17. van der Bliek AM, Meyerowitz EM. Dynamin-like protein encoded by the Drosophila shibire gene associated with vesicular traffic. Nature. 1991;351(6325):411–4. 1674590

18. Awasaki T, Ito K. Engulfing action of glial cells is required for programmed axon pruning during Drosophila metamorphosis. Current biology: CB. 2004;14(8):668–77. 15084281

19. Kitamoto T. Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. Journal of neurobiology. 2001;47(2):81–92. 11291099

20. Hill E, van Der Kaay J, Downes CP, Smythe E. The role of dynamin and its binding partners in coated pit invagination and scission. The Journal of cell biology. 2001;152(2):309–23. 11266448

21. Lin RC, Scheller RH. Mechanisms of synaptic vesicle exocytosis. Annual review of cell and developmental biology. 2000;16:19–49. 11031229

22. Shilo BZ. Signaling by the Drosophila epidermal growth factor receptor pathway during development. Experimental cell research. 2003;284(1):140–9. 12648473

23. Vivekanand P, Rebay I. Intersection of signal transduction pathways and development. Annual review of genetics. 2006;40:139–57. 16771628

24. Harris TJ, McCormick F. The molecular pathology of cancer. Nature reviews Clinical oncology. 2010;7(5):251–65. doi: 10.1038/nrclinonc.2010.41 20351699

25. Makki N, Thiel KW, Miller FJ Jr. The epidermal growth factor receptor and its ligands in cardiovascular disease. International journal of molecular sciences. 2013;14(10):20597–613. doi: 10.3390/ijms141020597 24132149

26. Staruschenko A, Palygin O, Ilatovskaya DV, Pavlov TS. Epidermal growth factors in the kidney and relationship to hypertension. American journal of physiology Renal physiology. 2013;305(1):F12–20. doi: 10.1152/ajprenal.00112.2013 23637204

27. Tomas A, Futter CE, Eden ER. EGF receptor trafficking: consequences for signaling and cancer. Trends in cell biology. 2014;24(1):26–34. doi: 10.1016/j.tcb.2013.11.002 24295852

28. Vieira AV, Lamaze C, Schmid SL. Control of EGF receptor signaling by clathrin-mediated endocytosis. Science. 1996;274(5295):2086–9. 8953040

29. Lloyd TE, Atkinson R, Wu MN, Zhou Y, Pennetta G, Bellen HJ. Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell. 2002;108(2):261–9. 11832215

30. Jekely G, Rorth P. Hrs mediates downregulation of multiple signalling receptors in Drosophila. EMBO reports. 2003;4(12):1163–8. 14608370

31. Treisman JE. Retinal differentiation in Drosophila. Wiley interdisciplinary reviews Developmental biology. 2013;2(4):545–57. doi: 10.1002/wdev.100 24014422

32. Huang Z, Shilo BZ, Kunes S. A retinal axon fascicle uses spitz, an EGF receptor ligand, to construct a synaptic cartridge in the brain of Drosophila. Cell. 1998;95(5):693–703. 9845371

33. Schlesinger A, Kiger A, Perrimon N, Shilo BZ. Small wing PLCgamma is required for ER retention of cleaved Spitz during eye development in Drosophila. Developmental cell. 2004;7(4):535–45. 15469842

34. Yogev S, Schejter ED, Shilo BZ. Drosophila EGFR signalling is modulated by differential compartmentalization of Rhomboid intramembrane proteases. The EMBO journal. 2008;27(8):1219–30. doi: 10.1038/emboj.2008.58 18369317

35. Yogev S, Schejter ED, Shilo BZ. Polarized secretion of Drosophila EGFR ligand from photoreceptor neurons is controlled by ER localization of the ligand-processing machinery. PLoS biology. 2010;8(10).

36. Reich A, Shilo BZ. Keren, a new ligand of the Drosophila epidermal growth factor receptor, undergoes two modes of cleavage. The EMBO journal. 2002;21(16):4287–96. 12169631

37. Golembo M, Yarnitzky T, Volk T, Shilo BZ. Vein expression is induced by the EGF receptor pathway to provide a positive feedback loop in patterning the Drosophila embryonic ventral ectoderm. Genes & development. 1999;13(2):158–62.

38. Kurada P, White K. Ras promotes cell survival in Drosophila by downregulating hid expression. Cell. 1998;95(3):319–29. 9814703

39. Bergmann A, Agapite J, McCall K, Steller H. The Drosophila gene hid is a direct molecular target of Ras-dependent survival signaling. Cell. 1998;95(3):331–41. 9814704

40. Fu LL, Cheng Y, Liu B. Beclin-1: autophagic regulator and therapeutic target in cancer. The international journal of biochemistry & cell biology. 2013;45(5):921–4.

41. Wei Y, Zou Z, Becker N, Anderson M, Sumpter R, Xiao G, et al. EGFR-mediated Beclin 1 phosphorylation in autophagy suppression, tumor progression, and tumor chemoresistance. Cell. 2013;154(6):1269–84. doi: 10.1016/j.cell.2013.08.015 24034250

42. Fung C, Chen X, Grandis JR, Duvvuri U. EGFR tyrosine kinase inhibition induces autophagy in cancer cells. Cancer biology & therapy. 2012;13(14):1417–24.

43. Romero-Calderon R, Uhlenbrock G, Borycz J, Simon AF, Grygoruk A, Yee SK, et al. A glial variant of the vesicular monoamine transporter is required to store histamine in the Drosophila visual system. PLoS genetics. 2008;4(11):e1000245. doi: 10.1371/journal.pgen.1000245 18989452

44. Lee T, Luo L. Mosaic analysis with a repressible cell marker (MARCM) for Drosophila neural development. Trends in neurosciences. 2001;24(5):251–4. 11311363

45. Suzuki K, Ohsumi Y. Current knowledge of the pre-autophagosomal structure (PAS). FEBS letters. 2010;584(7):1280–6. doi: 10.1016/j.febslet.2010.02.001 20138172

46. Heisenberg M. Separation of receptor and lamina potentials in the electroretinogram of normal and mutant Drosophila. The Journal of experimental biology. 1971;55(1):85–100. 5001616

47. Burg MG, Sarthy PV, Koliantz G, Pak WL. Genetic and molecular identification of a Drosophila histidine decarboxylase gene required in photoreceptor transmitter synthesis. The EMBO journal. 1993;12(3):911–9. 8096176

48. Gavin BA, Arruda SE, Dolph PJ. The role of carcinine in signaling at the Drosophila photoreceptor synapse. PLoS genetics. 2007;3(12):e206. 18069895

49. Rahman M, Ham H, Liu X, Sugiura Y, Orth K, Kramer H. Visual neurotransmission in Drosophila requires expression of Fic in glial capitate projections. Nature neuroscience. 2012;15(6):871–5. doi: 10.1038/nn.3102 22544313

50. Ziegler AB, Brusselbach F, Hovemann BT. Activity and coexpression of Drosophila black with ebony in fly optic lobes reveals putative cooperative tasks in vision that evade electroretinographic detection. The Journal of comparative neurology. 2013;521(6):1207–24. doi: 10.1002/cne.23247 23124681

51. Meinertzhagen IA, Sorra KE. Synaptic organization in the fly's optic lamina: few cells, many synapses and divergent microcircuits. Progress in brain research. 2001;131:53–69. 11420968

52. Strigini M, Cohen SM. Wingless gradient formation in the Drosophila wing. Current biology: CB. 2000;10(6):293–300. 10744972

53. Steele F, O'Tousa JE. Rhodopsin activation causes retinal degeneration in Drosophila rdgC mutant. Neuron. 1990;4(6):883–90. 2361011

54. Steele FR, Washburn T, Rieger R, O'Tousa JE. Drosophila retinal degeneration C (rdgC) encodes a novel serine/threonine protein phosphatase. Cell. 1992;69(4):669–76. 1316807

55. Robinson SW, Herzyk P, Dow JA, Leader DP. FlyAtlas: database of gene expression in the tissues of Drosophila melanogaster. Nucleic acids research. 2013;41(Database issue):D744–50. doi: 10.1093/nar/gks1141 23203866

56. Tsruya R, Schlesinger A, Reich A, Gabay L, Sapir A, Shilo BZ. Intracellular trafficking by Star regulates cleavage of the Drosophila EGF receptor ligand Spitz. Genes & development. 2002;16(2):222–34.

57. Wasserman JD, Urban S, Freeman M. A family of rhomboid-like genes: Drosophila rhomboid-1 and roughoid/rhomboid-3 cooperate to activate EGF receptor signaling. Genes & development. 2000;14(13):1651–63.

58. Zettl M, Adrain C, Strisovsky K, Lastun V, Freeman M. Rhomboid family pseudoproteases use the ER quality control machinery to regulate intercellular signaling. Cell. 2011;145(1):79–91. doi: 10.1016/j.cell.2011.02.047 21439629

59. O'Neill EM, Rebay I, Tjian R, Rubin GM. The activities of two Ets-related transcription factors required for Drosophila eye development are modulated by the Ras/MAPK pathway. Cell. 1994;78(1):137–47. 8033205

60. Frankfort BJ, Mardon G. Senseless represses nuclear transduction of Egfr pathway activation. Development. 2004;131(3):563–70. 14711872

61. Brunner D, Ducker K, Oellers N, Hafen E, Scholz H, Klambt C. The ETS domain protein pointed-P2 is a target of MAP kinase in the sevenless signal transduction pathway. Nature. 1994;370(6488):386–9. 8047146

62. Bardet PL, Kolahgar G, Mynett A, Miguel-Aliaga I, Briscoe J, Meier P, et al. A fluorescent reporter of caspase activity for live imaging. Proceedings of the National Academy of Sciences of the United States of America. 2008;105(37):13901–5. doi: 10.1073/pnas.0806983105 18779587

63. Hay BA, Wolff T, Rubin GM. Expression of baculovirus P35 prevents cell death in Drosophila. Development. 1994;120(8):2121–9. 7925015

64. Goyal L, McCall K, Agapite J, Hartwieg E, Steller H. Induction of apoptosis by Drosophila reaper, hid and grim through inhibition of IAP function. The EMBO journal. 2000;19(4):589–97. 10675328

65. Hay BA, Wassarman DA, Rubin GM. Drosophila homologs of baculovirus inhibitor of apoptosis proteins function to block cell death. Cell. 1995;83(7):1253–62. 8548811

66. Wang SL, Hawkins CJ, Yoo SJ, Muller HA, Hay BA. The Drosophila caspase inhibitor DIAP1 is essential for cell survival and is negatively regulated by HID. Cell. 1999;98(4):453–63. 10481910

67. Liu Z, Huang X. Lipid metabolism in Drosophila: development and disease. Acta biochimica et biophysica Sinica. 2013;45(1):44–50. doi: 10.1093/abbs/gms105 23257293

68. Rusten TE, Lindmo K, Juhasz G, Sass M, Seglen PO, Brech A, et al. Programmed autophagy in the Drosophila fat body is induced by ecdysone through regulation of the PI3K pathway. Developmental cell. 2004;7(2):179–92. 15296715

69. DeVorkin L, Gorski SM. Monitoring autophagic flux using Ref(2)P, the Drosophila p62 ortholog. Cold Spring Harbor protocols. 2014;2014(9):959–66. doi: 10.1101/pdb.prot080333 25183816

70. Pircs K, Nagy P, Varga A, Venkei Z, Erdi B, Hegedus K, et al. Advantages and limitations of different p62-based assays for estimating autophagic activity in Drosophila. PloS one. 2012;7(8):e44214. doi: 10.1371/journal.pone.0044214 22952930

71. Bjorkoy G, Lamark T, Brech A, Outzen H, Perander M, Overvatn A, et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. The Journal of cell biology. 2005;171(4):603–14. 16286508

72. Falchetti A, Di Stefano M, Marini F, Del Monte F, Gozzini A, Masi L, et al. Segregation of a M404V mutation of the p62/sequestosome 1 (p62/SQSTM1) gene with polyostotic Paget's disease of bone in an Italian family. Arthritis research & therapy. 2005;7(6):R1289–95.

73. Nezis IP. Selective autophagy in Drosophila. International journal of cell biology. 2012;2012:146767. doi: 10.1155/2012/146767 22567011

74. de Castro IP, Costa AC, Celardo I, Tufi R, Dinsdale D, Loh SH, et al. Drosophila ref(2)P is required for the parkin-mediated suppression of mitochondrial dysfunction in pink1 mutants. Cell death & disease. 2013;4:e873.

75. Kimura S, Noda T, Yoshimori T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy. 2007;3(5):452–60. 17534139

76. Nezis IP, Shravage BV, Sagona AP, Lamark T, Bjorkoy G, Johansen T, et al. Autophagic degradation of dBruce controls DNA fragmentation in nurse cells during late Drosophila melanogaster oogenesis. The Journal of cell biology. 2010;190(4):523–31. doi: 10.1083/jcb.201002035 20713604

77. Scott RC, Schuldiner O, Neufeld TP. Role and regulation of starvation-induced autophagy in the Drosophila fat body. Developmental cell. 2004;7(2):167–78. 15296714

78. Pulipparacharuvil S, Akbar MA, Ray S, Sevrioukov EA, Haberman AS, Rohrer J, et al. Drosophila Vps16A is required for trafficking to lysosomes and biogenesis of pigment granules. Journal of cell science. 2005;118(Pt 16):3663–73. 16046475

79. Lim A, Kraut R. The Drosophila BEACH family protein, blue cheese, links lysosomal axon transport with motor neuron degeneration. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2009;29(4):951–63.

80. Seglen PO, Grinde B, Solheim AE. Inhibition of the lysosomal pathway of protein degradation in isolated rat hepatocytes by ammonia, methylamine, chloroquine and leupeptin. European journal of biochemistry / FEBS. 1979;95(2):215–25. 456353

81. Chi C, Zhu H, Han M, Zhuang Y, Wu X, Xu T. Disruption of lysosome function promotes tumor growth and metastasis in Drosophila. The Journal of biological chemistry. 2010;285(28):21817–23. doi: 10.1074/jbc.M110.131714 20418542

82. Wucherpfennig T, Wilsch-Brauninger M, Gonzalez-Gaitan M. Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. The Journal of cell biology. 2003;161(3):609–24. 12743108

83. Entchev EV, Schwabedissen A, Gonzalez-Gaitan M. Gradient formation of the TGF-beta homolog Dpp. Cell. 2000;103(6):981–91. 11136982

84. Gonzalez-Gaitan M, Jackle H. Role of Drosophila alpha-adaptin in presynaptic vesicle recycling. Cell. 1997;88(6):767–76. 9118220

85. Hyttinen JM, Niittykoski M, Salminen A, Kaarniranta K. Maturation of autophagosomes and endosomes: a key role for Rab7. Biochimica et biophysica acta. 2013;1833(3):503–10. doi: 10.1016/j.bbamcr.2012.11.018 23220125

86. Yousefian J, Troost T, Grawe F, Sasamura T, Fortini M, Klein T. Dmon1 controls recruitment of Rab7 to maturing endosomes in Drosophila. Journal of cell science. 2013;126(Pt 7):1583–94. doi: 10.1242/jcs.114934 23418349

87. Zhang J, Schulze KL, Hiesinger PR, Suyama K, Wang S, Fish M, et al. Thirty-one flavors of Drosophila rab proteins. Genetics. 2007;176(2):1307–22. 17409086

88. Chan CC, Scoggin S, Wang D, Cherry S, Dembo T, Greenberg B, et al. Systematic discovery of Rab GTPases with synaptic functions in Drosophila. Current biology: CB. 2011;21(20):1704–15. doi: 10.1016/j.cub.2011.08.058 22000105

89. Ullrich O, Reinsch S, Urbe S, Zerial M, Parton RG. Rab11 regulates recycling through the pericentriolar recycling endosome. The Journal of cell biology. 1996;135(4):913–24. 8922376

90. Szatmari Z, Kis V, Lippai M, Hegedus K, Farago T, Lorincz P, et al. Rab11 facilitates cross-talk between autophagy and endosomal pathway through regulation of Hook localization. Molecular biology of the cell. 2014;25(4):522–31. doi: 10.1091/mbc.E13-10-0574 24356450

91. Le Droguen PM, Claret S, Guichet A, Brodu V. Microtubule-dependent apical restriction of recycling endosomes sustains adherens junctions during morphogenesis of the Drosophila tracheal system. Development. 2015;142(2):363–74. doi: 10.1242/dev.113472 25564624

92. Akbar MA, Ray S, Kramer H. The SM protein Car/Vps33A regulates SNARE-mediated trafficking to lysosomes and lysosome-related organelles. Molecular biology of the cell. 2009;20(6):1705–14. doi: 10.1091/mbc.E08-03-0282 19158398

93. Sriram V, Krishnan KS, Mayor S. deep-orange and carnation define distinct stages in late endosomal biogenesis in Drosophila melanogaster. The Journal of cell biology. 2003;161(3):593–607. 12743107

94. Lindmo K, Simonsen A, Brech A, Finley K, Rusten TE, Stenmark H. A dual function for Deep orange in programmed autophagy in the Drosophila melanogaster fat body. Experimental cell research. 2006;312(11):2018–27. 16600212

95. Takats S, Pircs K, Nagy P, Varga A, Karpati M, Hegedus K, et al. Interaction of the HOPS complex with Syntaxin 17 mediates autophagosome clearance in Drosophila. Molecular biology of the cell. 2014.

96. Kato K, Forero MG, Fenton JC, Hidalgo A. The glial regenerative response to central nervous system injury is enabled by pros-notch and pros-NFkappaB feedback. PLoS biology. 2011;9(8):e1001133. doi: 10.1371/journal.pbio.1001133 21912512

97. Han W, Lo HW. Landscape of EGFR signaling network in human cancers: biology and therapeutic response in relation to receptor subcellular locations. Cancer letters. 2012;318(2):124–34. doi: 10.1016/j.canlet.2012.01.011 22261334

98. Lo HW, Ali-Seyed M, Wu Y, Bartholomeusz G, Hsu SC, Hung MC. Nuclear-cytoplasmic transport of EGFR involves receptor endocytosis, importin beta1 and CRM1. Journal of cellular biochemistry. 2006;98(6):1570–83. 16552725

99. De Angelis Campos AC, Rodrigues MA, de Andrade C, de Goes AM, Nathanson MH, Gomes DA. Epidermal growth factor receptors destined for the nucleus are internalized via a clathrin-dependent pathway. Biochemical and biophysical research communications. 2011;412(2):341–6. doi: 10.1016/j.bbrc.2011.07.100 21821003

100. Demory ML, Boerner JL, Davidson R, Faust W, Miyake T, Lee I, et al. Epidermal growth factor receptor translocation to the mitochondria: regulation and effect. The Journal of biological chemistry. 2009;284(52):36592–604. doi: 10.1074/jbc.M109.000760 19840943

101. Yao Y, Wang G, Li Z, Yan B, Guo Y, Jiang X, et al. Mitochondrially localized EGFR is independent of its endocytosis and associates with cell viability. Acta biochimica et biophysica Sinica. 2010;42(11):763–70. doi: 10.1093/abbs/gmq090 20929928

102. Wagner B, Natarajan A, Grunaug S, Kroismayr R, Wagner EF, Sibilia M. Neuronal survival depends on EGFR signaling in cortical but not midbrain astrocytes. The EMBO journal. 2006;25(4):752–62. 16467848

103. Weihua Z, Tsan R, Huang WC, Wu Q, Chiu CH, Fidler IJ, et al. Survival of cancer cells is maintained by EGFR independent of its kinase activity. Cancer cell. 2008;13(5):385–93. doi: 10.1016/j.ccr.2008.03.015 18455122

104. Haberman AS, Akbar MA, Ray S, Kramer H. Drosophila acinus encodes a novel regulator of endocytic and autophagic trafficking. Development. 2010;137(13):2157–66. doi: 10.1242/dev.044230 20504956

105. Nemazanyy I, Blaauw B, Paolini C, Caillaud C, Protasi F, Mueller A, et al. Defects of Vps15 in skeletal muscles lead to autophagic vacuolar myopathy and lysosomal disease. EMBO molecular medicine. 2013;5(6):870–90. doi: 10.1002/emmm.201202057 23630012

106. Settembre C, Fraldi A, Jahreiss L, Spampanato C, Venturi C, Medina D, et al. A block of autophagy in lysosomal storage disorders. Human molecular genetics. 2008;17(1):119–29. 17913701

107. Wang D, Chan CC, Cherry S, Hiesinger PR. Membrane trafficking in neuronal maintenance and degeneration. Cellular and molecular life sciences: CMLS. 2013;70(16):2919–34. doi: 10.1007/s00018-012-1201-4 23132096

108. Paul I, Bhattacharya S, Chatterjee A, Ghosh MK. Current Understanding on EGFR and Wnt/beta-Catenin Signaling in Glioma and Their Possible Crosstalk. Genes & cancer. 2013;4(11–12):427–46.

109. Kalman B, Szep E, Garzuly F, Post DE. Epidermal growth factor receptor as a therapeutic target in glioblastoma. Neuromolecular medicine. 2013;15(2):420–34. doi: 10.1007/s12017-013-8229-y 23575987

110. Goffin JR, Zbuk K. Epidermal growth factor receptor: pathway, therapies, and pipeline. Clinical therapeutics. 2013;35(9):1282–303. doi: 10.1016/j.clinthera.2013.08.007 24054705

111. Zhu Y, Nern A, Zipursky SL, Frye MA. Peripheral visual circuits functionally segregate motion and phototaxis behaviors in the fly. Current biology: CB. 2009;19(7):613–9. doi: 10.1016/j.cub.2009.02.053 19303299

112. Silies M, Yuva Y, Engelen D, Aho A, Stork T, Klambt C. Glial cell migration in the eye disc. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2007;27(48):13130–9. 18045907

113. Han C, Jan LY, Jan YN. Enhancer-driven membrane markers for analysis of nonautonomous mechanisms reveal neuron-glia interactions in Drosophila. Proceedings of the National Academy of Sciences of the United States of America. 2011;108(23):9673–8. doi: 10.1073/pnas.1106386108 21606367

114. Awasaki T, Lai SL, Ito K, Lee T. Organization and postembryonic development of glial cells in the adult central brain of Drosophila. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2008;28(51):13742–53. doi: 10.1523/JNEUROSCI.4844-08.2008 19091965

115. Langevin J, Le Borgne R, Rosenfeld F, Gho M, Schweisguth F, Bellaiche Y. Lethal giant larvae controls the localization of notch-signaling regulators numb, neuralized, and Sanpodo in Drosophila sensory-organ precursor cells. Current biology: CB. 2005;15(10):955–62. 15916953

116. Queenan AM, Ghabrial A, Schupbach T. Ectopic activation of torpedo/Egfr, a Drosophila receptor tyrosine kinase, dorsalizes both the eggshell and the embryo. Development. 1997;124(19):3871–80. 9367443

117. Freeman M. Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell. 1996;87(4):651–60. 8929534

118. O'Keefe DD, Prober DA, Moyle PS, Rickoll WL, Edgar BA. Egfr/Ras signaling regulates DE-cadherin/Shotgun localization to control vein morphogenesis in the Drosophila wing. Developmental biology. 2007;311(1):25–39. 17888420

119. Chen GC, Lee JY, Tang HW, Debnath J, Thomas SM, Settleman J. Genetic interactions between Drosophila melanogaster Atg1 and paxillin reveal a role for paxillin in autophagosome formation. Autophagy. 2008;4(1):37–45. 17952025

120. Clifford RJ, Schupbach T. Coordinately and differentially mutable activities of torpedo, the Drosophila melanogaster homolog of the vertebrate EGF receptor gene. Genetics. 1989;123(4):771–87. 2515109

121. Contamine D, Petitjean AM, Ashburner M. Genetic resistance to viral infection: the molecular cloning of a Drosophila gene that restricts infection by the rhabdovirus sigma. Genetics. 1989;123(3):525–33. 2557263

122. McDonald JA, Pinheiro EM, Kadlec L, Schupbach T, Montell DJ. Multiple EGFR ligands participate in guiding migrating border cells. Developmental biology. 2006;296(1):94–103. 16712835

123. Mayer U, Nusslein-Volhard C. A group of genes required for pattern formation in the ventral ectoderm of the Drosophila embryo. Genes & development. 1988;2(11):1496–511.

124. Sevrioukov EA, He JP, Moghrabi N, Sunio A, Kramer H. A role for the deep orange and carnation eye color genes in lysosomal delivery in Drosophila. Molecular cell. 1999;4(4):479–86. 10549280

125. Chang YY, Neufeld TP. An Atg1/Atg13 complex with multiple roles in TOR-mediated autophagy regulation. Molecular biology of the cell. 2009;20(7):2004–14. doi: 10.1091/mbc.E08-12-1250 19225150

126. Cherry S, Jin EJ, Ozel MN, Lu Z, Agi E, Wang D, et al. Charcot-Marie-Tooth 2B mutations in rab7 cause dosage-dependent neurodegeneration due to partial loss of function. eLife. 2013;2:e01064. doi: 10.7554/eLife.01064 24327558

127. Chu WC, Lee YM, Henry Sun Y. FGF /FGFR signal induces trachea extension in the drosophila visual system. PloS one. 2013;8(8):e73878. doi: 10.1371/journal.pone.0073878 23991208

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2015 Číslo 4
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#