The unfolded protein response is required for dendrite morphogenesis

eLife

Volumn 4, Issue JUNE2015, 2015, Pages

  Wei, Xing ^a   Howell, Audrey S ^a   Dong, Xintong ^a   Taylor, Caitlin A ^a,b   Cooper, Roshni C ^a   Zhang, Jianqi ^c   Zou, Wei ^d   Sherwood, David R ^d   Shen, Kang ^a,b  

^a STANFORD UNIVERSITY   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN; UBIQUITIN PROTEIN LIGASE E3; X BOX BINDING PROTEIN 1; CAENORHABDITIS ELEGANS PROTEIN; DMA-1 PROTEIN, C ELEGANS; MEMBRANE PROTEIN; RIBONUCLEASE;

ARTICLE; CAENORHABDITIS ELEGANS; CELL COUNTING; CELL MIGRATION; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENDRITE; DOWN REGULATION; GENE MAPPING; GENE MUTATION; GENETIC TRANSFORMATION; HOMEOSTASIS; MOLECULAR CLONING; MORPHOGENESIS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FOLDING; TRANSGENE; UNFOLDED PROTEIN RESPONSE; UPREGULATION; ANIMAL; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; PROTEIN SYNTHESIS;

CAENORHABDITIS ELEGANS; MAMMALIA;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DENDRITES; ENDORIBONUCLEASES; MEMBRANE PROTEINS; MORPHOGENESIS; PROTEIN BIOSYNTHESIS; UNFOLDED PROTEIN RESPONSE;

EID: 84937047237     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.06963     Document Type: Article

References (75)

1. Arakawa H, Kudo H, Batrak V, Caldwell RB, Rieger MA, Ellwart JW, Buerstedde JM. 2008. Protein evolution by hypermutation and selection in the B cell line DT40. Nucleic Acids Research 36:e1. doi: 10.1093/nar/gkm616.
2. Askonas BA. 1975. Immunoglobulin formation in B lymphoid cells. Journal of Clinical Pathology Supplement (Association of Clinical Pathology) 6:8-12. doi: 10.1136/jcp.s1-6.1.8.
3. Bole DG, Dowin R, Doriaux M, Jamieson JD. 1989. Immunocytochemical localization of Bip to the rough endoplasmic-reticulum-evidence for protein sorting by selective retention. The Journal of Histochemistry and Cytochemistry 37:1817-1823. doi: 10.1177/37.12.2685110.
4. Brandizzi F, Barlowe C. 2013. Organization of the ER-Golgi interface for membrane traffic control. Nature Reviews. Molecular Cell Biology 14:382-392. doi: 10.1038/nrm3588.
5. Burga A, Casanueva MO, Lehner B. 2011. Predicting mutation outcome from early stochastic variation in genetic interaction partners. Nature 480:250-U133. doi: 10.1038/nature10665.
6. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, Harding HP, Clark SG, Ron D. 2002. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415:92-96. doi: 10.1038/415092a.
7. Chen B, Gilbert LA, Cimini BA, Schnitzbauer J, Zhang W, Li GW, Park J, Blackburn EH, Weissman JS, Qi LS, Huang B. 2013. Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell 155: 1479-1491. doi: 10.1016/j.cell.2013.12.001.
8. Coelho DS, Cairrao F, Zeng XM, Pires E, Coelho AV, Ron D, Ryoo HD, Domingos PM. 2013. Xbp1-Independent Ire1 signaling is required for photoreceptor differentiation and rhabdomere morphogenesis in Drosophila. Cell Reports 5:791-801. doi: 10.1016/j.celrep.2013.09.046.
9. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F. 2013. Multiplex genome engineering using CRISPR/Cas systems. Science 339:819-823. doi: 10.1126/science.1231143.
10. Cox JS, Walter P. 1996. A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 87:391-404. doi: 10.1016/S0092-8674(00)81360-4.
11. Credle JJ, Finer-Moore JS, Papa FR, Stroud RM, Walter P. 2005. On the mechanism of sensing unfolded protein in the endoplasmic reticulum. Proceedings of the National Academy of Sciences of USA 102:18773-18784. doi: 10.1073/pnas.0509487102.
12. Dalton RP, Lyons DB, Lomvardas S. 2013. Co-opting the unfolded protein response to elicit olfactory receptor feedback. Cell 155:321-332. doi: 10.1016/j.cell.2013.09.033.
13. Dimcheff DE, Askovic S, Baker AH, Johnson-Fowler C, Portis JL. 2003. Endoplasmic reticulum stress is a determinant of retrovirus-induced spongiform neurodegeneration. Journal of Virology 77:12617-12629. doi: 10.1128/JVI.77.23.12617-12629.2003.
14. Dong X, Liu OW, Howell AS, Shen K. 2013. An extracellular adhesion molecule complex patterns dendritic branching and morphogenesis. Cell 155:296-307. doi: 10.1016/j.cell.2013.08.059.
15. Fonseca SG, Gromada J, Urano F. 2011. Endoplasmic reticulum stress and pancreatic beta-cell death. Trends in Endocrinology and Metabolism 22:266-274.
16. Freiberg A, Machner MP, Pfeil W, Schubert WD, Heinz DW, Seckler R. 2004. Folding and stability of the leucinerich repeat domain of internalin B from Listeria monocytogenes. Journal of Molecular Biology 337:453-461. doi: 10.1016/j.jmb.2004.01.044.
17. Gardner BM, Walter P. 2011. Unfolded proteins are Ire1-activating ligands that directly induce the unfolded protein response. Science 333:1891-1894. doi: 10.1126/science.1209126.
18. Hanus C, Ehlers MD. 2008. Secretory outposts for the local processing of membrane cargo in neuronal dendrites. Traffic 9:1437-1445. doi: 10.1111/j.1600-0854.2008.00775.x.
19. Henis-Korenblit S, Zhang P, Hansen M, McCormick M, Lee SJ, Cary M, Kenyon C. 2010Insulin/IGF-1 signaling mutants reprogram ER stress response regulators to promote longevity. Proceedings of the National Academy of Sciences of USA 107:9730-9735. doi: 10.1073/pnas.1002575107.
20. Herndon RM. 1963. The fine structure of the Purkinje cell. The Journal of Cell Biology 18:167-180. doi: 10.1083/jcb.18.1.167.
21. Hollien J, Lin JH, Li H, Stevens N, Walter P, Weissman JS. 2009. Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. The Journal of Cell Biology 186:323-331. doi: 10.1083/jcb.200903014.
22. Hollien J, Weissman JS. 2006. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313:104-107. doi: 10.1126/science.1129631.
23. Holt CE, Schuman EM. 2013. The central dogma decentralized: new perspectives on RNA function and local translation in neurons. Neuron 80:648-657. doi: 10.1016/j.neuron.2013.10.036.
24. Iwakoshi NN, Lee AH, Vallabhajosyula P, Otipoby KL, Rajewsky K, Glimcher LH. 2003. Plasma cell differentiation and the unfolded protein response intersect at the transcription factor XBP-1. Nature Immunology 4:321-329. doi: 10.1038/ni907.
25. Iwawaki T, Akai R, Kohno K, Miura M. 2004. A transgenic mouse model for monitoring endoplasmic reticulum stress. Nature Medicine 10:98-102. doi: 10.1038/nm970.
26. Jan Y-N, Jan LY. 2010Branching out: mechanisms of dendritic arborization. Nature Reviews. Neuroscience 11: 316-328. doi: 10.1038/nrn2836.
27. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. 2012. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:816-821. doi: 10.1126/science.1225829.
28. Komiyama T, Sweeney LB, Schuldiner O, Garcia KC, Luo LQ. 2007. Graded expression of semaphorin-1a cell-autonomously directs dendritic targeting of olfactory projection neurons. Cell 128:399-410.doi: 10.1016/j.cell.2006.12.028.
29. Lai CW, Aronson DE, Snapp EL. 2010BiP availability distinguishes states of homeostasis and stress in the endoplasmic reticulum of living cells. Molecular Biology of the Cell 21:1909-1921. doi: 10.1091/mbc.E09-12-1066.
30. Lee AH, Iwakoshi NN, Glimcher LH. 2003. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Molecular and Cellular Biology 23:7448-7459. doi: 10.1128/MCB.23.21.7448-7459.2003.
31. Lefebvre JL, Kostadinov D, Chen WV, Maniatis T, Sanes JR. 2012. Protocadherins mediate dendritic self-avoidance in the mammalian nervous system. Nature 488:517-521. doi: 10.1038/nature11305.
32. Lin JH, Lavail MM. 2010Misfolded proteins and retinal dystrophies. Advances in Experimental Medicine and Biology 664:115-121. doi: 10.1007/978-1-4419-1399-9_14.
33. Liu OW, Shen K. 2012. The transmembrane LRR protein DMA-1 promotes dendrite branching and growth in C. elegans. Nature Neuroscience 15:57-63. doi: 10.1038/nn.2978.
34. MacNeil MA, Masland RH. 1998. Extreme diversity among amacrine cells: implications for function. Neuron 20: 971-982. doi: 10.1016/S0896-6273(00)80478-X.
35. Matthews BJ, Kim ME, Flanagan JJ, Hattori D, Clemens JC, Zipursky SL, Grueber WB. 2007. Dendrite selfavoidance is controlled by Dscam. Cell 129:593-604. doi: 10.1016/j.cell.2007.04.013.
36. Maurel M, Chevet E, Tavernier J, Gerlo S. 2014. Getting RIDD of RNA: IRE1 in cell fate regulation. Trends in Biochemical Sciences 39:245-254. doi: 10.1016/j.tibs.2014.02.008.
37. Mello C, Fire A. 1995. DNA transformation. Methods in Cell Biology 48:451-482.
38. Newbury S, Woollard A. 2004. The 5’-3’ exoribonuclease xrn-1 is essential for ventral epithelial enclosure during C. elegans embryogenesis. RNA 10:59-65. doi: 10.1261/rna.2195504.
39. Peng H, Long F, Liu X, Kim SK, Myers EW. 2008. Straightening Caenorhabditis elegans images. Bioinformatics 24: 234-242. doi: 10.1093/bioinformatics/btm569.
40. Polleux F, Morrow T, Ghosh A. 2000. Semaphorin 3A is a chemoattractant for cortical apical dendrites. Nature 404: 567-573. doi: 10.1038/35007001.
41. Ramóny Cajal S. 1911. Histology of the nervous system of man and vertebrates. New York: Oxford University Press.
42. Reimold AM, Iwakoshi NN, Manis J, Vallabhajosyula P, Szomolanyi-Tsuda E, Gravallese EM, Friend D, Grusby MJ, Alt F, Glimcher LH. 2001. Plasma cell differentiation requires the transcription factor XBP-1. Nature 412:300-307. doi: 10.1038/35085509.
43. Richardson CE, Kooistra T, Kim DH. 2010An essential role for XBP-1 in host protection against immune activation in C. elegans. Nature 463:1092-1095. doi: 10.1038/nature08762.
44. Rolls MM, Hall DH, Victor M, Stelzer EH, Rapoport TA. 2002. Targeting of rough endoplasmic reticulum membrane proteins and ribosomes in invertebrate neurons. Molecular Biology of the Cell 13:1778-1791. doi: 10.1091/mbc.01-10-0514.
45. Ron D, Walter P. 2007. Signal integration in the endoplasmic reticulum unfolded protein response. Nature Reviews. Molecular Cell Biology 8:519-529. doi: 10.1038/nrm2199.
46. Safra M, Ben-Hamo S, Kenyon C, Henis-Korenblit S. 2013. The ire-1 ER stress-response pathway is required for normal secretory-protein metabolism in C. elegans. Journal of Cell Science 126:4136-4146. doi: 10.1242/jcs.123000.
47. Sallese M, Pulvirenti T, Luini A. 2006. The physiology of membrane transport and endomembrane-based signalling. The EMBO Journal 25:2663-2673. doi: 10.1038/sj.emboj.7601172.
48. Salzberg Y, Diaz-Balzac CA, Ramirez-Suarez NJ, Attreed M, Tecle E, Desbois M, Kaprielian Z, Bulow HE. 2013. Skin-derived cues control arborization of sensory dendrites in Caenorhabditis elegans. Cell 155:308-320. doi: 10.1016/j.cell.2013.08.058.
49. Sanes JR, Zipursky SL. 2010Design principles of insect and vertebrate visual systems. Neuron 66:15-36. doi: 10.1016/j.neuron.201001.018.
50. Sarin S, Prabhu S, O’Meara MM, Pe’er I, Hobert O. 2008. Caenorhabditis elegans mutant allele identification by whole-genome sequencing. Nature Methods 5:865-867. doi: 10.1038/nmeth.1249.
51. Satoh D, Sato D, Tsuyama T, Saito M, Ohkura H, Rolls MM, Ishikawa F, Uemura T. 2008. Spatial control of branching within dendritic arbors by dynein-dependent transport of Rab5-endosomes. Nature Cell Biology 10: 1164-1171. doi: 10.1038/ncb1776.
52. Schmucker D, Clemens JC, Shu H, Worby CA, Xiao J, Muda M, Dixon JE, Zipursky SL. 2000. Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell 101:671-684. doi: 10.1016/S0092-8674(00)80878-8.
53. Schroder M, Kaufman RJ. 2005. The mammalian unfolded protein response. Annual Review of Biochemistry 74: 739-789. doi: 10.1146/annurev.biochem.73.011303.074134.
54. Schroeder NE, Androwski RJ, Rashid A, Lee H, Lee J, Barr MM. 2013. Dauer-specific dendrite arborization in C. elegans is regulated by KPC-1/Furin. Current Biology 23:1527-1535. doi: 10.1016/j.cub.2013.06.058.
55. Shen Z, Zhang X, Chai Y, Zhu Z, Yi P, Feng G, Li W, Ou G. 2014. Conditional knockouts generated by engineered CRISPR-Cas9 endonuclease reveal the roles of coronin in C. elegans neural development. Developmental Cell 30: 625-636. doi: 10.1016/j.devcel.2014.07.017.
56. Shim J, Umemura T, Nothstein E, Rongo C. 2004. The unfolded protein response regulates glutamate receptor export from the endoplasmic reticulum. Molecular Biology of the Cell 15:4818-4828. doi: 10.1091/mbc.E04-02-0108.
57. Smith CJ, O’Brien T, Chatzigeorgiou M, Spencer WC, Feingold-Link E, Husson SJ, Hori S, Mitani S, Gottschalk A, Schafer WR, Miller DM 2013. Sensory neuron fates are distinguished by a transcriptional switch that regulates dendrite branch stabilization. Neuron 79:266-280. doi: 10.1016/j.neuron.2013.05.009.
58. Smith CJ, Watson JD, Spencer WC, O’Brien T, Cha B, Albeg A, Treinin M, Miller DM III. 2010Time-lapse imaging and cell-specific expression profiling reveal dynamic branching and molecular determinants of a multi-dendritic nociceptor in C. elegans. Developmental Biology 345:18-33. doi: 10.1016/j.ydbio.201005.502.
59. Smith CJ, Watson JD, VanHoven MK, Colon-Ramos DA, Miller DM III. 2012. Netrin (UNC-6) mediates dendritic self-avoidance. Nature Neuroscience 15:731-737. doi: 10.1038/nn.3065.
60. Spieth J, Brooke G, Kuersten S, Lea K, Blumenthal T. 1993. Operons in C-elegans-polycistronic messenger-Rna precursors are processed by transsplicing of Sl2 to downstream coding regions. Cell 73:521-532. doi: 10.1016/0092-8674(93)90139-H.
61. Sulston JE, Horvitz HR. 1977. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Developmental Biology 56:110-156. doi: 10.1016/0012-1606(77)90158-0.
62. Thacker C, Sheps JA, Rose AM. 2006. Caenorhabditis elegans dpy-5 is a cuticle procollagen processed by a proprotein convertase. Cellular and Molecular Life Sciences 63:1193-1204. doi: 10.1007/s00018-006-6012-z.
63. Tom Dieck S, Hanus C, Schuman EM. 2014. SnapShot: local protein translation in dendrites. Neuron 81:958-958. doi: 10.1016/j.neuron.2014.02.009.
64. Travers KJ, Patil CK, Wodicka L, Lockhart DJ, Weissman JS, Walter P. 2000. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101:249-258. doi: 10.1016/S0092-8674(00)80835-1.
65. Tursun B, Cochella L, Carrera I, Hobert O. 2009. A toolkit and robust pipeline for the generation of fosmid-based reporter genes in C. elegans. PLOS ONE 4:e4625. doi: 10.1371/journal.pone.0004625.
66. Urano F, Calfon M, Yoneda T, Yun C, Kiraly M, Clark SG, Ron D. 2002. A survival pathway for Caenorhabditis elegans with a blocked unfolded protein response. The Journal of Cell Biology 158:639-646. doi: 10.1083/jcb.200203086.
67. Valdes P, Mercado G, Vidal RL, Molina C, Parsons G, Court FA, Martinez A, Galleguillos D, Armentano D, Schneider BL, Hetz C. 2014. Control of dopaminergic neuron survival by the unfolded protein response transcription factor XBP1. Proceedings of the National Academy of Sciences of USA 111:6804-6809. doi: 10.1073/pnas.1321845111.
68. Vandenberghe W, Nicoll RA, Bredt DS. 2005. Interaction with the unfolded protein response reveals a role for stargazin in biosynthetic AMPA receptor transport. The Journal of Neuroscience 25:1095-1102. doi: 10.1523/JNEUROSCI.3568-04.2005.
69. Walter P, Ron D. 2011. The unfolded protein response: from stress pathway to homeostatic regulation. Science 334:1081-1086. doi: 10.1126/science.1209038.
70. Wassle H, Peichl L, Boycott BB. 1981. Dendritic territories of cat retinal ganglion-cells. Nature 292:344-345. doi: 10.1038/292344a0.
71. Wojtowicz WM, Flanagan JJ, Millard SS, Zipursky SL. 2004. Alternative splicing of Drosophila Dscam generates axon guidance receptors that exhibit isoform-specific homophilic binding. Cell 118:619-633. doi: 10.1016/j.cell.2004.08.021.
72. Worby CA, Dixon JE. 2014. Unpacking the unfolded protein response. Cell 158:1221-1224. doi: 10.1016/j.cell.2014.08.025.
73. Yamagata M, Sanes JR. 2008. Dscam and Sidekick proteins direct lamina-specific synaptic connections in vertebrate retina. Nature 451:465-U466. doi: 10.1038/nature06469.
74. Yamagata M, Sanes JR. 2012. Expanding the Ig superfamily code for laminar specificity in retina: expression and role of contactins. Journal of Neuroscience 32:14402-14414. doi: 10.1523/JNEUROSCI.3193-12.2012.
75. Ye B, Zhang Y, Song W, Younger SH, Jan LY, Jan YN. 2007. Growing dendrites and axons differ in their reliance on the secretory pathway. Cell 130:717-729. doi: 10.1016/j.cell.2007.06.032.