-
Články
- Časopisy
- Kurzy
- Témy
- Kongresy
- Videa
- Podcasty
RAB-10-Dependent Membrane Transport Is Required for Dendrite Arborization
Dendrites are cellular extensions from neurons that gather information from other neurons or cues from the external environment to convey to the nervous system of an organism. Dendrites are often extensively branched, raising the question of how neurons supply plasma membrane and dendrite specific proteins from the source of synthesis inside the cell to developing dendrites. We have examined membrane trafficking in the PVD neuron in the nematode worm C. elegans to investigate how new membrane and dendrite proteins are trafficked. The PVD neuron is easy to visualize and has remarkably long and widely branched dendrites positioned along the skin of the worm, which transmits information about harsh touch and cold temperature to the nervous system. We have discovered that a key organizer of vesicle trafficking, the RAB-10 protein, localizes to membrane vesicles and is required to traffic these vesicles that contain plasma membrane and dendrite proteins to the growing PVD dendrite. Further, our work revealed that a complex of proteins, termed the exocyst, that helps fuse membrane vesicles at the plasma membrane, localizes with RAB-10 and is required for dendrite branching. Together, our work has revealed a novel mechanism for how neurons build dendrites that could be used to help repair damaged neurons in human diseases and during aging.
Vyšlo v časopise: RAB-10-Dependent Membrane Transport Is Required for Dendrite Arborization. PLoS Genet 11(9): e32767. doi:10.1371/journal.pgen.1005484
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005484Souhrn
Dendrites are cellular extensions from neurons that gather information from other neurons or cues from the external environment to convey to the nervous system of an organism. Dendrites are often extensively branched, raising the question of how neurons supply plasma membrane and dendrite specific proteins from the source of synthesis inside the cell to developing dendrites. We have examined membrane trafficking in the PVD neuron in the nematode worm C. elegans to investigate how new membrane and dendrite proteins are trafficked. The PVD neuron is easy to visualize and has remarkably long and widely branched dendrites positioned along the skin of the worm, which transmits information about harsh touch and cold temperature to the nervous system. We have discovered that a key organizer of vesicle trafficking, the RAB-10 protein, localizes to membrane vesicles and is required to traffic these vesicles that contain plasma membrane and dendrite proteins to the growing PVD dendrite. Further, our work revealed that a complex of proteins, termed the exocyst, that helps fuse membrane vesicles at the plasma membrane, localizes with RAB-10 and is required for dendrite branching. Together, our work has revealed a novel mechanism for how neurons build dendrites that could be used to help repair damaged neurons in human diseases and during aging.
Zdroje
1. Ye B, Zhang Y, Song W, Younger SH, Jan LY, et al. (2007) Growing dendrites and axons differ in their reliance on the secretory pathway. Cell 130 : 717–729. 17719548
2. Satoh D, Sato D, Tsuyama T, Saito M, Ohkura H, et al. (2008) Spatial control of branching within dendritic arbors by dynein-dependent transport of Rab5-endosomes. Nat Cell Biol 10 : 1164–1171. doi: 10.1038/ncb1776 18758452
3. Lee MC, Miller EA, Goldberg J, Orci L, Schekman R (2004) Bi-directional protein transport between the ER and Golgi. Annu Rev Cell Dev Biol 20 : 87–123. 15473836
4. Lazo OM, Gonzalez A, Ascano M, Kuruvilla R, Couve A, et al. (2013) BDNF regulates Rab11-mediated recycling endosome dynamics to induce dendritic branching. J Neurosci 33 : 6112–6122. doi: 10.1523/JNEUROSCI.4630-12.2013 23554492
5. Way JC, Chalfie M (1989) The mec-3 gene of Caenorhabditis elegans requires its own product for maintained expression and is expressed in three neuronal cell types. Genes Dev 3 : 1823–1833. 2576011
6. Chatzigeorgiou M, Yoo S, Watson JD, Lee WH, Spencer WC, et al. (2010) Specific roles for DEG/ENaC and TRP channels in touch and thermosensation in C. elegans nociceptors. Nat Neurosci 13 : 861–868. doi: 10.1038/nn.2581 20512132
7. Li W, Kang L, Piggott BJ, Feng Z, Xu XZ (2011) The neural circuits and sensory channels mediating harsh touch sensation in Caenorhabditis elegans. Nat Commun 2 : 315. doi: 10.1038/ncomms1308 21587232
8. Smith CJ, Watson JD, Spencer WC, O'Brien T, Cha B, et al. (2010) Time-lapse imaging and cell-specific expression profiling reveal dynamic branching and molecular determinants of a multi-dendritic nociceptor in C. elegans. Dev Biol 345 : 18–33. doi: 10.1016/j.ydbio.2010.05.502 20537990
9. Liu OW, Shen K (2012) The transmembrane LRR protein DMA-1 promotes dendrite branching and growth in C. elegans. Nat Neurosci 15 : 57–63.
10. 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 24120131
11. Salzberg Y, Diaz-Balzac CA, Ramirez-Suarez NJ, Attreed M, Tecle E, et al. (2013) Skin-derived cues control arborization of sensory dendrites in Caenorhabditis elegans. Cell 155 : 308–320. doi: 10.1016/j.cell.2013.08.058 24120132
12. Smith CJ, O'Brien T, Chatzigeorgiou M, Spencer WC, Feingold-Link E, et al. (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 23889932
13. Wang T, Liu Y, Xu XH, Deng CY, Wu KY, et al. (2011) Lgl1 activation of rab10 promotes axonal membrane trafficking underlying neuronal polarization. Dev Cell 21 : 431–444. doi: 10.1016/j.devcel.2011.07.007 21856246
14. Liu Y, Xu XH, Chen Q, Wang T, Deng CY, et al. (2013) Myosin Vb controls biogenesis of post-Golgi Rab10 carriers during axon development. Nat Commun 4 : 2005. doi: 10.1038/ncomms3005 23770993
15. Deng CY, Lei WL, Xu XH, Ju XC, Liu Y, et al. (2014) JIP1 mediates anterograde transport of Rab10 cargos during neuronal polarization. J Neurosci 34 : 1710–1723. doi: 10.1523/JNEUROSCI.4496-13.2014 24478353
16. Xu XH, Deng CY, Liu Y, He M, Peng J, et al. (2014) MARCKS regulates membrane targeting of Rab10 vesicles to promote axon development. Cell Res 24 : 576–594. doi: 10.1038/cr.2014.33 24662485
17. He B, Guo W (2009) The exocyst complex in polarized exocytosis. Curr Opin Cell Biol 21 : 537–542. doi: 10.1016/j.ceb.2009.04.007 19473826
18. Frische EW, Pellis-van Berkel W, van Haaften G, Cuppen E, Plasterk RH, et al. (2007) RAP-1 and the RAL-1/exocyst pathway coordinate hypodermal cell organization in Caenorhabditis elegans. EMBO J 26 : 5083–5092. 17989692
19. Babbey CM, Bacallao RL, Dunn KW (2010) Rab10 associates with primary cilia and the exocyst complex in renal epithelial cells. Am J Physiol Renal Physiol 299: F495–506. doi: 10.1152/ajprenal.00198.2010 20576682
20. Sano H, Eguez L, Teruel MN, Fukuda M, Chuang TD, et al. (2007) Rab10, a target of the AS160 Rab GAP, is required for insulin-stimulated translocation of GLUT4 to the adipocyte plasma membrane. Cell Metab 5 : 293–303. 17403373
21. Inoue M, Chang L, Hwang J, Chiang SH, Saltiel AR (2003) The exocyst complex is required for targeting of Glut4 to the plasma membrane by insulin. Nature 422 : 629–633. 12687004
22. Babbey CM, Ahktar N, Wang E, Chen CC, Grant BD, et al. (2006) Rab10 regulates membrane transport through early endosomes of polarized Madin-Darby canine kidney cells. Mol Biol Cell 17 : 3156–3175. 16641372
23. Schuck S, Gerl MJ, Ang A, Manninen A, Keller P, et al. (2007) Rab10 is involved in basolateral transport in polarized Madin-Darby canine kidney cells. Traffic 8 : 47–60. 17132146
24. Chen CC, Schweinsberg PJ, Vashist S, Mareiniss DP, Lambie EJ, et al. (2006) RAB-10 is required for endocytic recycling in the Caenorhabditis elegans intestine. Mol Biol Cell 17 : 1286–1297. 16394106
25. Glodowski DR, Chen CC, Schaefer H, Grant BD, Rongo C (2007) RAB-10 regulates glutamate receptor recycling in a cholesterol-dependent endocytosis pathway. Mol Biol Cell 18 : 4387–4396. 17761527
26. Shi A, Chen CC, Banerjee R, Glodowski D, Audhya A, et al. (2010) EHBP-1 functions with RAB-10 during endocytic recycling in Caenorhabditis elegans. Mol Biol Cell 21 : 2930–2943. doi: 10.1091/mbc.E10-02-0149 20573983
27. Arakawa H, Kudo H, Batrak V, Caldwell RB, Rieger MA, et al. (2008) Protein evolution by hypermutation and selection in the B cell line DT40. Nucleic Acids Res 36: e1. 18073192
28. Frokjaer-Jensen C, Davis MW, Sarov M, Taylor J, Flibotte S, et al. (2014) Random and targeted transgene insertion in Caenorhabditis elegans using a modified Mos1 transposon. Nat Methods 11 : 529–534. doi: 10.1038/nmeth.2889 24820376
29. Guo P, Hu T, Zhang J, Jiang S, Wang X (2010) Sequential action of Caenorhabditis elegans Rab GTPases regulates phagolysosome formation during apoptotic cell degradation. Proc Natl Acad Sci U S A 107 : 18016–18021. doi: 10.1073/pnas.1008946107 20921409
30. Grant B, Zhang Y, Paupard MC, Lin SX, Hall DH, et al. (2001) Evidence that RME-1, a conserved C. elegans EH-domain protein, functions in endocytic recycling. Nat Cell Biol 3 : 573–579. 11389442
31. Chen B, Jiang Y, Zeng S, Yan J, Li X, et al. (2010) Endocytic sorting and recycling require membrane phosphatidylserine asymmetry maintained by TAT-1/CHAT-1. PLoS Genet 6: e1001235. doi: 10.1371/journal.pgen.1001235 21170358
32. Woodman PG (2000) Biogenesis of the sorting endosome: the role of Rab5. Traffic 1 : 695–701. 11208157
33. Ullrich O, Reinsch S, Urbe S, Zerial M, Parton RG (1996) Rab11 regulates recycling through the pericentriolar recycling endosome. J Cell Biol 135 : 913–924. 8922376
34. Grosshans BL, Ortiz D, Novick P (2006) Rabs and their effectors: achieving specificity in membrane traffic. Proc Natl Acad Sci U S A 103 : 11821–11827. 16882731
35. Guo W, Roth D, Walch-Solimena C, Novick P (1999) The exocyst is an effector for Sec4p, targeting secretory vesicles to sites of exocytosis. EMBO J 18 : 1071–1080. 10022848
36. Jiu Y, Jin C, Liu Y, Holmberg CI, Jantti J (2012) Exocyst subunits Exo70 and Exo84 cooperate with small GTPases to regulate behavior and endocytic trafficking in C. elegans. PLoS One 7: e32077. doi: 10.1371/journal.pone.0032077 22389680
37. Armenti ST, Lohmer LL, Sherwood DR, Nance J (2014) Repurposing an endogenous degradation system for rapid and targeted depletion of C. elegans proteins. Development 141 : 4640–4647. doi: 10.1242/dev.115048 25377555
38. Grindstaff KK, Yeaman C, Anandasabapathy N, Hsu SC, Rodriguez-Boulan E, et al. (1998) Sec6/8 complex is recruited to cell-cell contacts and specifies transport vesicle delivery to the basal-lateral membrane in epithelial cells. Cell 93 : 731–740. 9630218
39. Tsuboi T, Ravier MA, Xie H, Ewart MA, Gould GW, et al. (2005) Mammalian exocyst complex is required for the docking step of insulin vesicle exocytosis. J Biol Chem 280 : 25565–25570. 15878854
40. Pereira-Leal JB, Seabra MC (2000) The mammalian Rab family of small GTPases: definition of family and subfamily sequence motifs suggests a mechanism for functional specificity in the Ras superfamily. J Mol Biol 301 : 1077–1087. 10966806
41. Shen Z, Zhang X, Chai Y, Zhu Z, Yi P, et al. (2014) Conditional knockouts generated by engineered CRISPR-Cas9 endonuclease reveal the roles of coronin in C. elegans neural development. Dev Cell 30 : 625–636. doi: 10.1016/j.devcel.2014.07.017 25155554
42. Miyabayashi T, Palfreyman MT, Sluder AE, Slack F, Sengupta P (1999) Expression and function of members of a divergent nuclear receptor family in Caenorhabditis elegans. Dev Biol 215 : 314–331. 10545240
43. Lerner DW, McCoy D, Isabella AJ, Mahowald AP, Gerlach GF, et al. (2013) A Rab10-dependent mechanism for polarized basement membrane secretion during organ morphogenesis. Dev Cell 24 : 159–168. doi: 10.1016/j.devcel.2012.12.005 23369713
44. Jones TA, Nikolova LS, Schjelderup A, Metzstein MM (2014) Exocyst-mediated membrane trafficking is required for branch outgrowth in Drosophila tracheal terminal cells. Dev Biol 390 : 41–50. doi: 10.1016/j.ydbio.2014.02.021 24607370
45. Chen S, Li L, Li J, Liu B, Zhu X, et al. (2014) SEC-10 and RAB-10 coordinate basolateral recycling of clathrin-independent cargo through endosomal tubules in Caenorhabditis elegans. Proc Natl Acad Sci U S A 111 : 15432–15437. doi: 10.1073/pnas.1408327111 25301900
46. Jiu Y, Hasygar K, Tang L, Liu Y, Holmberg CI, et al. (2014) par-1, atypical pkc, and PP2A/B55 sur-6 are implicated in the regulation of exocyst-mediated membrane trafficking in Caenorhabditis elegans. G3 (Bethesda) 4 : 173–183.
47. Murthy M, Teodoro RO, Miller TP, Schwarz TL (2010) Sec5, a member of the exocyst complex, mediates Drosophila embryo cellularization. Development 137 : 2773–2783. doi: 10.1242/dev.048330 20630948
48. Einstein G, Buranosky R, Crain BJ (1994) Dendritic pathology of granule cells in Alzheimer's disease is unrelated to neuritic plaques. J Neurosci 14 : 5077–5088. 8046469
49. McNeill TH, Brown SA, Rafols JA, Shoulson I (1988) Atrophy of medium spiny I striatal dendrites in advanced Parkinson's disease. Brain Res 455 : 148–152. 3416180
50. Aguirre-Chen C, Bulow HE, Kaprielian Z (2011) C. elegans bicd-1, homolog of the Drosophila dynein accessory factor Bicaudal D, regulates the branching of PVD sensory neuron dendrites. Development 138 : 507–518. doi: 10.1242/dev.060939 21205795
51. Rual JF, Ceron J, Koreth J, Hao T, Nicot AS, et al. (2004) Toward improving Caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library. Genome Res 14 : 2162–2168. 15489339
52. Inoue T, Sherwood DR, Aspock G, Butler JA, Gupta BP, et al. (2002) Gene expression markers for Caenorhabditis elegans vulval cells. Mech Dev 119 Suppl 1: S203–209. 14516686
53. Gallegos ME, Balakrishnan S, Chandramouli P, Arora S, Azameera A, et al. (2012) The C. elegans rab family: identification, classification and toolkit construction. PLoS One 7: e49387. doi: 10.1371/journal.pone.0049387 23185324
54. Hobert O (2002) PCR fusion-based approach to create reporter gene constructs for expression analysis in transgenic C. elegans. Biotechniques 32 : 728–730. 11962590
55. Iyer EP, Iyer SC, Sullivan L, Wang D, Meduri R, et al. (2013) Functional genomic analyses of two morphologically distinct classes of Drosophila sensory neurons: post-mitotic roles of transcription factors in dendritic patterning. PLoS One 8: e72434. doi: 10.1371/journal.pone.0072434 23977298
Štítky
Genetika Reprodukčná medicína
Článek The Chromatin Protein DUET/MMD1 Controls Expression of the Meiotic Gene during Male Meiosis inČlánek Tissue-Specific Gain of RTK Signalling Uncovers Selective Cell Vulnerability during Embryogenesis
Článok vyšiel v časopisePLOS Genetics
Najčítanejšie tento týždeň
2015 Číslo 9- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
-
Všetky články tohto čísla
- Retraction: RNAi-Dependent and Independent Control of LINE1 Accumulation and Mobility in Mouse Embryonic Stem Cells
- Signaling from Within: Endocytic Trafficking of the Robo Receptor Is Required for Midline Axon Repulsion
- A Splice Region Variant in Lowers Non-high Density Lipoprotein Cholesterol and Protects against Coronary Artery Disease
- The Chromatin Protein DUET/MMD1 Controls Expression of the Meiotic Gene during Male Meiosis in
- A NIMA-Related Kinase Suppresses the Flagellar Instability Associated with the Loss of Multiple Axonemal Structures
- Slit-Dependent Endocytic Trafficking of the Robo Receptor Is Required for Son of Sevenless Recruitment and Midline Axon Repulsion
- Expression of Concern: Protein Under-Wrapping Causes Dosage Sensitivity and Decreases Gene Duplicability
- Mutagenesis by AID: Being in the Right Place at the Right Time
- Identification of as a Genetic Modifier That Regulates the Global Orientation of Mammalian Hair Follicles
- Bridges Meristem and Organ Primordia Boundaries through , , and during Flower Development in
- Evaluating the Performance of Fine-Mapping Strategies at Common Variant GWAS Loci
- KLK5 Inactivation Reverses Cutaneous Hallmarks of Netherton Syndrome
- Differential Expression of Ecdysone Receptor Leads to Variation in Phenotypic Plasticity across Serial Homologs
- Receptor Polymorphism and Genomic Structure Interact to Shape Bitter Taste Perception
- Cognitive Function Related to the Gene Acquired from an LTR Retrotransposon in Eutherians
- Critical Function of γH2A in S-Phase
- Arabidopsis AtPLC2 Is a Primary Phosphoinositide-Specific Phospholipase C in Phosphoinositide Metabolism and the Endoplasmic Reticulum Stress Response
- XBP1-Independent UPR Pathways Suppress C/EBP-β Mediated Chondrocyte Differentiation in ER-Stress Related Skeletal Disease
- Integration of Genome-Wide SNP Data and Gene-Expression Profiles Reveals Six Novel Loci and Regulatory Mechanisms for Amino Acids and Acylcarnitines in Whole Blood
- A Genome-Wide Association Study of a Biomarker of Nicotine Metabolism
- Cell Cycle Regulates Nuclear Stability of AID and Determines the Cellular Response to AID
- A Genome-Wide Association Analysis Reveals Epistatic Cancellation of Additive Genetic Variance for Root Length in
- Tissue-Specific Gain of RTK Signalling Uncovers Selective Cell Vulnerability during Embryogenesis
- RAB-10-Dependent Membrane Transport Is Required for Dendrite Arborization
- Basolateral Endocytic Recycling Requires RAB-10 and AMPH-1 Mediated Recruitment of RAB-5 GAP TBC-2 to Endosomes
- Dynamic Contacts of U2, RES, Cwc25, Prp8 and Prp45 Proteins with the Pre-mRNA Branch-Site and 3' Splice Site during Catalytic Activation and Step 1 Catalysis in Yeast Spliceosomes
- ARID1A Is Essential for Endometrial Function during Early Pregnancy
- Predicting Carriers of Ongoing Selective Sweeps without Knowledge of the Favored Allele
- An Interaction between RRP6 and SU(VAR)3-9 Targets RRP6 to Heterochromatin and Contributes to Heterochromatin Maintenance in
- Photoreceptor Specificity in the Light-Induced and COP1-Mediated Rapid Degradation of the Repressor of Photomorphogenesis SPA2 in Arabidopsis
- Autophosphorylation of the Bacterial Tyrosine-Kinase CpsD Connects Capsule Synthesis with the Cell Cycle in
- Multimer Formation Explains Allelic Suppression of PRDM9 Recombination Hotspots
- Rescheduling Behavioral Subunits of a Fixed Action Pattern by Genetic Manipulation of Peptidergic Signaling
- A Gene Regulatory Program for Meiotic Prophase in the Fetal Ovary
- Cell-Autonomous Gβ Signaling Defines Neuron-Specific Steady State Serotonin Synthesis in
- Discovering Genetic Interactions in Large-Scale Association Studies by Stage-wise Likelihood Ratio Tests
- The RCC1 Family Protein TCF1 Regulates Freezing Tolerance and Cold Acclimation through Modulating Lignin Biosynthesis
- The AMPK, Snf1, Negatively Regulates the Hog1 MAPK Pathway in ER Stress Response
- The Parkinson’s Disease-Associated Protein Kinase LRRK2 Modulates Notch Signaling through the Endosomal Pathway
- Multicopy Single-Stranded DNA Directs Intestinal Colonization of Enteric Pathogens
- Recurrent Domestication by Lepidoptera of Genes from Their Parasites Mediated by Bracoviruses
- Three Different Pathways Prevent Chromosome Segregation in the Presence of DNA Damage or Replication Stress in Budding Yeast
- Identification of Four Mouse Diabetes Candidate Genes Altering β-Cell Proliferation
- The Intolerance of Regulatory Sequence to Genetic Variation Predicts Gene Dosage Sensitivity
- Synergistic and Dose-Controlled Regulation of Cellulase Gene Expression in
- Genome Sequence and Transcriptome Analyses of : Metabolic Tools for Enhanced Algal Fitness in the Prominent Order Prymnesiales (Haptophyceae)
- Ty3 Retrotransposon Hijacks Mating Yeast RNA Processing Bodies to Infect New Genomes
- FUS Interacts with HSP60 to Promote Mitochondrial Damage
- Point Mutations in Centromeric Histone Induce Post-zygotic Incompatibility and Uniparental Inheritance
- Genome-Wide Association Study with Targeted and Non-targeted NMR Metabolomics Identifies 15 Novel Loci of Urinary Human Metabolic Individuality
- Outer Hair Cell Lateral Wall Structure Constrains the Mobility of Plasma Membrane Proteins
- A Large-Scale Functional Analysis of Putative Target Genes of Mating-Type Loci Provides Insight into the Regulation of Sexual Development of the Cereal Pathogen
- A Genetic Selection for Mutants Reveals an Interaction between DNA Polymerase IV and the Replicative Polymerase That Is Required for Translesion Synthesis
- PLOS Genetics
- Archív čísel
- Aktuálne číslo
- Informácie o časopise
Najčítanejšie v tomto čísle- Arabidopsis AtPLC2 Is a Primary Phosphoinositide-Specific Phospholipase C in Phosphoinositide Metabolism and the Endoplasmic Reticulum Stress Response
- Bridges Meristem and Organ Primordia Boundaries through , , and during Flower Development in
- KLK5 Inactivation Reverses Cutaneous Hallmarks of Netherton Syndrome
- XBP1-Independent UPR Pathways Suppress C/EBP-β Mediated Chondrocyte Differentiation in ER-Stress Related Skeletal Disease
Prihlásenie#ADS_BOTTOM_SCRIPTS#Zabudnuté hesloZadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
- Časopisy