Changes in endolysosomal organization define a pre-degenerative state in the crumbs mutant Drosophila retina


Autoři: Rachel S. Kraut aff001;  Elisabeth Knust aff001
Působiště autorů: Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstrasse, Dresden, Germany aff001
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0220220

Souhrn

Mutations in the epithelial polarity gene crumbs (crb) lead to retinal degeneration in Drosophila and in humans. The overall morphology of the retina and its deterioration in Drosophila crb mutants has been well-characterized, but the cell biological origin of the degeneration is not well understood. Degenerative conditions in the retina and elsewhere in the nervous system often involve defects in degradative intracellular trafficking pathways. So far, however, effects of crb on the endolysosomal system, or on the spatial organization of these compartments in photoreceptor cells have not been described. We therefore asked whether photoreceptors in crb mutants exhibit alterations in endolysosomal compartments under pre-degenerative conditions, where the retina is still morphologically intact. Data presented here show that, already well before the onset of degeneration, Arl8, Rab7, and Atg8-carrying endolysosomal and autophagosomal compartments undergo changes in morphology and positioning with respect to each other in crb mutant retinas. We propose that these changes may be early signs of the degeneration-prone condition in crb retinas.

Klíčová slova:

Cell membranes – Drosophila melanogaster – Light – Lysosomes – Photoreceptors – Retina – Vesicles – Retinal degeneration


Zdroje

1. Bales KL, Gross AK. Aberrant protein trafficking in retinal degeneration: The initial phase of retinal remodelling. Exp Eye Res. 2016;150:71–80. doi: 10.1016/j.exer.2015.11.007 26632497

2. Cao J, Zhong MB, Toro CA, Zhang L, Cai D. Endo-lysosomal pathway and ubiquitin-proteasome system dysfunction in Alzheimer’s disease pathogenesis. Neuroscience Letters. 2019;703:68–78. doi: 10.1016/j.neulet.2019.03.016 30890471

3. Deal SL, Yamamoto S. Unraveling Novel Mechanisms of Neurodegeneration Through a Large-Scale Forward Genetic Screen in Drosophila. Front Genet. 2019;9. doi: 10.3389/fgene.2018.00700 30693015

4. Ugur B, Chen K, Bellen HJ. Drosophila tools and assays for the study of human diseases. Dis Model Mech. 2016;9:235–44. doi: 10.1242/dmm.023762 26935102

5. Millburn GH, Crosby MA, Gramates LS, Tweedie S. FlyBase portals to human disease research using Drosophila models. Dis Model Mech. 2016;9:245–52. doi: 10.1242/dmm.023317 26935103

6. Yamamoto S, Jaiswal M, Charng W-L, Gambin T, Karaca E, Mirzaa G, et al. A drosophila genetic resource of mutants to study mechanisms underlying human genetic diseases. Cell. 2014;159:200–14. doi: 10.1016/j.cell.2014.09.002 25259927

7. Chien S, Reiter LT, Bier E, Gribskov M. Homophila: human disease gene cognates in Drosophila. Nucleic Acids Res. 2002;30:149–51. doi: 10.1093/nar/30.1.149 11752278

8. Reiter LT, Potocki L, Chien S, Gribskov M, Bier E. A Systematic Analysis of Human Disease-Associated Gene Sequences In Drosophila melanogaster. Genome Res. 2001;11:1114–25. doi: 10.1101/gr.169101 11381037

9. Wangler MF, Yamamoto S, Chao H-T, Posey JE, Westerfield M, Postlethwait J, et al. Model Organisms Facilitate Rare Disease Diagnosis and Therapeutic Research. Genetics. 2017;207:9–27. doi: 10.1534/genetics.117.203067 28874452

10. Arikawa K, Hicks JL, Williams DS. Identification of actin filaments in the rhabdomeral microvilli of Drosophila photoreceptors. J Cell Biol. 1990;110:1993–8. doi: 10.1083/jcb.110.6.1993 2112548

11. Hardie RC, Raghu P. Visual transduction in Drosophila. Nature. 2001;413:186–93. doi: 10.1038/35093002 11557987

12. Satoh AK, Ready DF. Arrestin1 Mediates Light-Dependent Rhodopsin Endocytosis and Cell Survival: Current Biology. Curr Biol. 2005;15:1722–33. doi: 10.1016/j.cub.2005.08.064 16213818

13. Wang T, Montell C. Phototransduction and retinal degeneration in Drosophila. Pflugers Arch—Eur J Physiol. 2007;454:821–47.

14. Chinchore Y, Mitra A, Dolph PJ. Accumulation of Rhodopsin in Late Endosomes Triggers Photoreceptor Cell Degeneration. PLOS Genet. 2009;5:e1000377. doi: 10.1371/journal.pgen.1000377 19214218

15. Midorikawa R, Yamamoto-Hino M, Awano W, Hinohara Y, Suzuki E, Ueda R, et al. Autophagy-Dependent Rhodopsin Degradation Prevents Retinal Degeneration in Drosophila. J Neurosci. 2010;30:10703–19. doi: 10.1523/JNEUROSCI.2061-10.2010 20702701

16. Thakur R, Panda A, Coessens E, Raj N, Zadav S, Balakrishnan S, et al. Phospholipase D activity couples plasma membrane endocytosis with retromer dependent recycling. eLife Lens. e-Life. 2016;5. http://lens.elifesciences.org/18515/index.html. Accessed 29 Nov 2016.

17. Lawrence RE, Zoncu R. The lysosome as a cellular centre for signalling, metabolism and quality control. Nature Cell Biology. 2019;21:133. doi: 10.1038/s41556-018-0244-7 30602725

18. Galluzzi L, Baehrecke EH, Ballabio A, Boya P, Bravo-San Pedro JM, Cecconi F, et al. Molecular definitions of autophagy and related processes. EMBO J. 2017;36:1811–36. doi: 10.15252/embj.201796697 28596378

19. Nakamura S, Yoshimori T. New insights into autophagosome–lysosome fusion. J Cell Sci. 2017;130:1209–16. doi: 10.1242/jcs.196352 28302910

20. Korolchuk VI, Rubinsztein DC. Regulation of autophagy by lysosomal positioning. Autophagy. 2011;7:927–8. doi: 10.4161/auto.7.8.15862 21521941

21. Pu J, Guardia CM, Keren-Kaplan T, Bonifacino JS. Mechanisms and functions of lysosome positioning. J Cell Sci. 2016;129:4329–39. doi: 10.1242/jcs.196287 27799357

22. Wong YC, Holzbaur ELF. Autophagosome dynamics in neurodegeneration at a glance. J Cell Sci. 2015;128:1259–67. doi: 10.1242/jcs.161216 25829512

23. Cabukusta B, Neefjes J. Mechanisms of Lysosomal Positioning and Movement. Traffic. 2018;19:761–9. doi: 10.1111/tra.12587 29900632

24. Hofmann I, Munro S. An N-terminally acetylated Arf-like GTPase is localised to lysosomes and affects their motility. J Cell Sci. 2006;119:1494–503. doi: 10.1242/jcs.02958 16537643

25. Johnson DE, Ostrowski P, Jaumouillé V, Grinstein S. The position of lysosomes within the cell determines their luminal pH. J Cell Biol. 2016;212:677–92. doi: 10.1083/jcb.201507112 26975849

26. Khatter D, Sindhwani A, Sharma M. Arf-like GTPase Arl8: Moving from the periphery to the center of lysosomal biology. Cell Logist. 2015;5:e1086501. doi: 10.1080/21592799.2015.1086501 27057420

27. Mrakovic A, Kay JG, Furuya W, Brumell JH, Botelho RJ. Rab7 and Arl8 GTPases are Necessary for Lysosome Tubulation in Macrophages. Traffic. 2012;13:1667–79. doi: 10.1111/tra.12003 22909026

28. Wang S, Bellen HJ. The retromer complex in development and disease. Development. 2015;142:2392–6. doi: 10.1242/dev.123737 26199408

29. Lehmann M, Knust E, Hebbar S. Drosophila melanogaster: A Valuable Genetic Model Organism to Elucidate the Biology of Retinitis Pigmentosa. Methods Mol Biol. 2019;1834:221–49. doi: 10.1007/978-1-4939-8669-9_16 30324448

30. Chartier FJ-M, Hardy ÉJ-L, Laprise P. Crumbs limits oxidase-dependent signaling to maintain epithelial integrity and prevent photoreceptor cell death. J Cell Biol. 2012;198:991–8. doi: 10.1083/jcb.201203083 22965909

31. Johnson K, Grawe F, Grzeschik N, Knust E. Drosophila Crumbs Is Required to Inhibit Light-Induced Photoreceptor Degeneration. Current Biology. 2002;12:1675–80. doi: 10.1016/s0960-9822(02)01180-6 12361571

32. Spannl S, Kumichel A, Hebbar S, Kapp K, Gonzalez-Gaitan M, Winkler S, et al. The Crumbs_C isoform of Drosophila shows tissue- and stage-specific expression and prevents light-dependent retinal degeneration. Biol Open. 2017;6:165–75. doi: 10.1242/bio.020040 28202468

33. Bujakowska K, Audo I, Mohand-Saïd S, Lancelot M-E, Antonio A, Germain A, et al. CRB1 mutations in inherited retinal dystrophies. Hum Mutat. 2012;33:306–15. doi: 10.1002/humu.21653 22065545

34. Hollander AI den, Brink JB ten, Kok YJM de, Soest S van, Born LI van den, Driel MA van, et al. Mutations in a human homologue of Drosophila crumbs cause retinitis pigmentosa (RP12). Nature Genetics. 1999;23:217. doi: 10.1038/13848 10508521

35. Hollander AI den, Heckenlively JR, Born LI van den, Kok YJM de, Velde-Visser SD van der, Kellner U, et al. Leber Congenital Amaurosis and Retinitis Pigmentosa with Coats-like Exudative Vasculopathy Are Associated with Mutations in the Crumbs Homologue 1 (CRB1) Gene. The American Journal of Human Genetics. 2001;69:198–203. doi: 10.1086/321263 11389483

36. Pocha SM, Shevchenko A, Knust E. Crumbs regulates rhodopsin transport by interacting with and stabilizing myosin V. J Cell Biol. 2011;195:827–38. doi: 10.1083/jcb.201105144 22105348

37. Bulgakova NA, Knust E. The Crumbs complex: from epithelial-cell polarity to retinal degeneration. Journal of Cell Science. 2009;122:2587–96. doi: 10.1242/jcs.023648 19625503

38. Pellikka M, Tanentzapf G, Pinto M, Smith C, McGlade CJ, Ready DF, et al. Crumbs, the Drosophila homologue of human CRB1/RP12, is essential for photoreceptor morphogenesis. Nature. 2002;416:143–9. doi: 10.1038/nature721 11850625

39. Mollereau B, Wernet MF, Beaufils P, Killian D, Pichaud F, Kühnlein R, et al. A green fluorescent protein enhancer trap screen in Drosophila photoreceptor cells. Mechanisms of Development. 2000;93:151–60. doi: 10.1016/s0925-4773(00)00287-2 10781948

40. 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. J Cell Sci. 2005;118:3663–73. doi: 10.1242/jcs.02502 16046475

41. Muschalik N. Epithelial cell polarity and photoreceptor morphogensis in Drosophila Ph.D. Technische Universität Dresden; 2010.

42. Entchev EV, Schwabedissen A, González-Gaitán M. Gradient Formation of the TGF-β Homolog Dpp. Cell. 2000;103:981–92. doi: 10.1016/s0092-8674(00)00200-2 11136982

43. McDonald EC, Xie B, Workman M, Charlton-Perkins M, Terrell DA, Reischl J, et al. Separable transcriptional regulatory domains within Otd control photoreceptor terminal differentiation events. Dev Biol. 2010;347:122–32. doi: 10.1016/j.ydbio.2010.08.016 20732315

44. Johnson AE, Shu H, Hauswirth AG, Tong A, Davis GW. VCP-dependent muscle degeneration is linked to defects in a dynamic tubular lysosomal network in vivo. eLife. 2015;4:e07366.

45. Chang Y-Y, Neufeld TP. An Atg1/Atg13 Complex with Multiple Roles in TOR-mediated Autophagy Regulation. MBoC. 2009;20:2004–14. doi: 10.1091/mbc.E08-12-1250 19225150

46. Nichols R, Pak WL. Characterization of Drosophila melanogaster rhodopsin. J Biol Chem. 1985;260:12670–4. 3930500

47. Richard M, Roepman R, Aartsen WM, van Rossum AGSH, den Hollander AI, Knust E, et al. Towards understanding CRUMBS function in retinal dystrophies. Hum Mol Genet. 2006;15 Spec No 2:R235–243.

48. Riedel F, Gillingham AK, Rosa-Ferreira C, Galindo A, Munro S. An antibody toolkit for the study of membrane traffic in Drosophila melanogaster. Biology Open. 2016;:bio.018937.

49. Korolchuk VI, Saiki S, Lichtenberg M, Siddiqi FH, Roberts EA, Imarisio S, et al. Lysosomal positioning coordinates cellular nutrient responses. Nat Cell Biol. 2011;13:453–60. doi: 10.1038/ncb2204 21394080

50. Marwaha R, Arya SB, Jagga D, Kaur H, Tuli A, Sharma M. The Rab7 effector PLEKHM1 binds Arl8b to promote cargo traffic to lysosomes. J Cell Biol. 2017;216:1051–70. doi: 10.1083/jcb.201607085 28325809

51. Kraft C, Kijanska M, Kalie E, Siergiejuk E, Lee SS, Semplicio G, et al. Binding of the Atg1/ULK1 kinase to the ubiquitin-like protein Atg8 regulates autophagy. EMBO J. 2012;31:3691–703. doi: 10.1038/emboj.2012.225 22885598

52. Verbakel SK, van Huet RAC, Boon CJF, den Hollander AI, Collin RWJ, Klaver CCW, et al. Non-syndromic retinitis pigmentosa. Prog Retin Eye Res. 2018;66:157–86. doi: 10.1016/j.preteyeres.2018.03.005 29597005

53. Bahr BA, Bendiske J. The neuropathogenic contributions of lysosomal dysfunction. J Neurochem. 2002;83:481–9. doi: 10.1046/j.1471-4159.2002.01192.x 12390510

54. Martini-Stoica H, Xu Y, Ballabio A, Zheng H. The Autophagy–Lysosomal Pathway in Neurodegeneration: A TFEB Perspective. Trends in Neurosciences. 2016;39:221–34. doi: 10.1016/j.tins.2016.02.002 26968346

55. Nixon RA. Autophagy in neurodegenerative disease: friend, foe or turncoat? Trends in Neurosciences. 2006;29:528–35. doi: 10.1016/j.tins.2006.07.003 16859759

56. Xiong B, Bellen HJ. Rhodopsin homeostasis and retinal degeneration: lessons from the fly. Trends in Neurosciences. 2013;36:652–60. doi: 10.1016/j.tins.2013.08.003 24012059

57. Hollingsworth TJ, Gross AK. Defective Trafficking of Rhodopsin and Its Role in Retinal Degenerations. In: Jeon KW, editor. International Review of Cell and Molecular Biology. Academic Press; 2012. p. 1–44. doi: 10.1016/B978-0-12-394304-0.00006–3

58. Komeima K, Rogers BS, Campochiaro PA. Antioxidants slow photoreceptor cell death in mouse models of retinitis pigmentosa. Journal of Cellular Physiology. 2007;213:809–15. doi: 10.1002/jcp.21152 17520694

59. Moreno M-L, Mérida S, Bosch-Morell F, Miranda M, Villar VM. Autophagy Dysfunction and Oxidative Stress, Two Related Mechanisms Implicated in Retinitis Pigmentosa. Front Physiol. 2018;9:1008. doi: 10.3389/fphys.2018.01008 30093867

60. Song H, Vijayasarathy C, Zeng Y, Marangoni D, Bush RA, Wu Z, et al. NADPH Oxidase Contributes to Photoreceptor Degeneration in Constitutively Active RAC1 Mice. Invest Ophthalmol Vis Sci. 2016;57:2864–75. doi: 10.1167/iovs.15-18974 27233035

61. Ye ZW, Zhang J, Townsend DM, Tew KD. Oxidative stress, redox regulation and diseases of cellular differentiation. Biochim Biophys Acta. 2015;1850:1607–21. doi: 10.1016/j.bbagen.2014.11.010 25445706

62. Rodney GG, Pal R, Abo-Zahrah R. Redox regulation of autophagy in skeletal muscle. Free Radic Biol Med. 2016;98:103–12. doi: 10.1016/j.freeradbiomed.2016.05.010 27184957

63. Berger Z, Ravikumar B, Menzies FM, Oroz LG, Underwood BR, Pangalos MN, et al. Rapamycin alleviates toxicity of different aggregate-prone proteins. Hum Mol Genet. 2006;15:433–42. doi: 10.1093/hmg/ddi458 16368705

64. Menzies FM, Fleming A, Rubinsztein DC. Compromised autophagy and neurodegenerative diseases. Nat Rev Neurosci. 2015;16:345–57. doi: 10.1038/nrn3961 25991442

65. Osellame LD, Duchen MR. Defective quality control mechanisms and accumulation of damaged mitochondria link Gaucher and Parkinson diseases. Autophagy. 2013;9:81–80.

66. Singh R, Cuervo AM. Autophagy in the Cellular Energetic Balance. Cell Metabolism. 2011;13:495–504. doi: 10.1016/j.cmet.2011.04.004 21531332

67. Balderhaar HJ kleine, Ungermann C. CORVET and HOPS tethering complexes–coordinators of endosome and lysosome fusion. J Cell Sci. 2013;126:1307–16. doi: 10.1242/jcs.107805 23645161

68. Oyarzún JE, Lagos J, Vázquez MC, Valls C, De la Fuente C, Yuseff MI, et al. Lysosome motility and distribution: Relevance in health and disease. Biochimica et Biophysica Acta (BBA)—Molecular Basis of Disease. 2019;1865:1076–87.

69. Weiss S, Minke B. A new genetic model for calcium induced autophagy and ER-stress in Drosophila photoreceptor cells. Channels. 2015;9:14–20. doi: 10.4161/19336950.2014.981439 25664921

70. Jain N, Ganesh S. Emerging nexus between RAB GTPases, autophagy and neurodegeneration. Autophagy. 2016;12:900–4. doi: 10.1080/15548627.2016.1147673 26985808

71. Kast DJ, Dominguez R. The Cytoskeleton–Autophagy Connection. Current Biology. 2017;27:R318–26. doi: 10.1016/j.cub.2017.02.061 28441569

72. Xia H, Ready DF. Ectoplasm, Ghost in the R cell Machine? Dev Neurobiol. 2011;71:1246–57. doi: 10.1002/dneu.20898 21542135

73. Khanal I, Elbediwy A, Diaz de la Loza M del C, Fletcher GC, Thompson BJ. Shot and Patronin polarise microtubules to direct membrane traffic and biogenesis of microvilli in epithelia. J Cell Sci. 2016;129:2651–9. doi: 10.1242/jcs.189076 27231092

74. Mui UN, Lubczyk CM, Nam S-C. Role of Spectraplakin in Drosophila Photoreceptor Morphogenesis. PLOS ONE. 2011;6:e25965. doi: 10.1371/journal.pone.0025965 22022483

75. Dell’Angelica EC, Mullins C, Caplan S, Bonifacino JS. Lysosome-related organelles. Faseb J. 2000;14:1265–78. doi: 10.1096/fj.14.10.1265 10877819

76. Kretzschmar D, Poeck B, Roth H, Ernst R, Keller A, Porsch M, et al. Defective pigment granule biogenesis and aberrant behavior caused by mutations in the Drosophila AP-3beta adaptin gene ruby. Genetics. 2000;155:213–23. 10790396


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2019 Číslo 12