Caenorhabditis elegans screen reveals role of PAR-5 in RAB-11-recycling endosome positioning and apicobasal cell polarity (original) (raw)

• Apodaca, G. Endocytic traffic in polarized epithelial cells: role of the actin and microtubule cytoskeleton. Traffic 2, 149–159 (2001).
  CAS PubMed Google Scholar
• Iden, S. & Collard, J. G. Crosstalk between small GTPases and polarity proteins in cell polarization. Nat. Rev. Mol. Cell Biol. 9, 846–859 (2008).
  CAS PubMed Google Scholar
• Knust, E. & Bossinger, O. Composition and formation of intercellular junctions in epithelial cells. Science 298, 1955–1959 (2002).
  CAS PubMed Google Scholar
• Goldenring, J. R. et al. Rab11 is an apically located small GTP-binding protein in epithelial tissues. Am. J. Physiol. 270, G515–G525 (1996).
  CAS PubMed Google Scholar
• Rodriguez-Boulan, E., Kreitzer, G. & Musch, A. Organization of vesicular trafficking in epithelia. Nat. Rev. Mol. Cell Biol. 6, 233–247 (2005).
  CAS PubMed Google Scholar
• Mellman, I. & Nelson, W. J. Coordinated protein sorting, targeting and distribution in polarized cells. Nat. Rev. Mol. Cell Biol. 9, 833–845 (2008).
  CAS PubMed PubMed Central Google Scholar
• Bryant, D. M. & Mostov, K. E. From cells to organs: building polarized tissue. Nat. Rev. Mol. Cell Biol. 9, 887–901 (2008).
  CAS PubMed PubMed Central Google Scholar
• Suzuki, A. & Ohno, S. The PAR–aPKC system: lessons in polarity. J. Cell Sci. 119, 979–987 (2006).
  Article CAS PubMed Google Scholar
• Munro, E. PAR proteins and the cytoskeleton: a marriage of equals. Curr. Opinion Cell Biol. 18, 86–94 (2006).
  CAS PubMed Google Scholar
• Nance, J. & Zallen, J. A. Elaborating polarity: PAR proteins and the cytoskeleton. Development 138, 799–809 (2011).
  CAS PubMed PubMed Central Google Scholar
• Achilleos, A., Wehman, A. M. & Nance, J. PAR-3 mediates the initial clustering and apical localization of junction and polarity proteins during C. elegans intestinal epithelial cell polarization. Development 137, 1833–1842 (2010).
  CAS PubMed PubMed Central Google Scholar
• Totong, R., Achilleos, A. & Nance, J. PAR-6 is required for junction formation but not apicobasal polarization in C. elegans embryonic epithelial cells. Development 134, 1259–1268 (2007).
  CAS PubMed Google Scholar
• Daley, W. P. et al. ROCK1-directed basement membrane positioning coordinates epithelial tissue polarity. Development 139, 411–422 (2012).
  CAS PubMed PubMed Central Google Scholar
• Etienne-Manneville, S. & Hall, A. Rho GTPases in cell biology. Nature 420, 629–635 (2002).
  CAS PubMed Google Scholar
• Zerial, M. & McBride, H. Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2, 107–117 (2001).
  CAS PubMed Google Scholar
• Lundquist, E. A. Small GTPases (January 17, 2006), WormBook, ed. The C. elegans Research Community, WormBook,http://dx.doi.org/10.1895/wormbook.1.67.1,http://www.wormbook.org.
• Golachowska, M. R., Hoekstra, D. & van, I. S. C. Recycling endosomes in apical plasma membrane domain formation and epithelial cell polarity. Trends Cell Biol. 20, 618–626 (2010).
  CAS PubMed Google Scholar
• Shivas, J. M., Morrison, H. A., Bilder, D. & Skop, A. R. Polarity and endocytosis: reciprocal regulation. Trends Cell Biol. 20, 445–452 (2010).
  CAS PubMed PubMed Central Google Scholar
• Prekeris, R., Klumperman, J. & Scheller, R. H. A Rab11/Rip11 protein complex regulates apical membrane trafficking via recycling endosomes. Mol. Cell 6, 1437–1448 (2000).
  CAS PubMed Google Scholar
• Swiatecka-Urban, A. et al. Myosin Vb is required for trafficking of the cystic fibrosis transmembrane conductance regulator in Rab11a-specific apical recycling endosomes in polarized human airway epithelial cells. J. Biol. Chem. 282, 23725–23736 (2007).
  CAS PubMed Google Scholar
• Langevin, J. et al. Drosophila exocyst components Sec5, Sec6, and Sec15 regulate DE-Cadherin trafficking from recycling endosomes to the plasma membrane. Dev. Cell 9, 355–376 (2005).
  Google Scholar
• Ang, A. L. et al. Recycling endosomes can serve as intermediates during transport from the Golgi to the plasma membrane of MDCK cells. J. Cell Biol. 167, 531–543 (2004).
  CAS PubMed PubMed Central Google Scholar
• Wu, S., Mehta, S., Pichaud, F., Bellen, H. & Quiocho, F. Sec15 interacts with Rab11 via a novel domain and affects Rab11 localization in vivo. Nat. Struct. Mol. Biol. 12, 879–885 (2005).
  CAS PubMed Google Scholar
• Chen, C. C. et al. RAB-10 is required for endocytic recycling in the Caenorhabditis elegans intestine. Mol. Biol. Cell 17, 1286–1297 (2006).
  CAS PubMed PubMed Central Google Scholar
• Zhang, H. et al. Apicobasal domain identities of expanding tubular membranes depend on glycosphingolipid biosynthesis. Nat. Cell Biol. 13, 1189–1201 (2011).
  CAS PubMed PubMed Central Google Scholar
• Hermann, G. J. et al. Genetic analysis of lysosomal trafficking in Caenorhabditis elegans. Mol. Biol. Cell 16, 3273–3288 (2005).
  CAS PubMed PubMed Central Google Scholar
• Van Fürden, D., Johnson, K., Segbert, C. & Bossinger, O. The C. elegans ezrin–radixin–moesin protein ERM-1 is necessary for apical junction remodelling and tubulogenesis in the intestine. Developmental Biol. 272, 262–276 (2004).
  Google Scholar
• McGhee, J. D. The C. elegans intestine (March 27, 2007), WormBook, ed. The C. elegans Research Community, WormBook,http://dx.doi.org/10.1895/wormbook.1.133.1,http://www.wormbook.org.
• McGhee, J. D. The C. elegans intestine. WormBook 1–36 (2007).
• Nehrke, K. A reduction in intestinal cell pHi due to loss of the _Caenorhabditis elegans_Na+/H+ exchanger NHX-2 increases life span. J. Biol. Chem. 278, 44657–44666 (2003).
  CAS PubMed Google Scholar
• Casanova, J. E. et al. Association of Rab25 and Rab11a with the apical recycling system of polarized Madin–Darby canine kidney cells. Mol. Biol. Cell 10, 47–61 (1999).
  CAS PubMed PubMed Central Google Scholar
• Kamath, R. S. & Ahringer, J. Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30, 313–321 (2003).
  CAS PubMed Google Scholar
• Blum, H. Models for the Perception of Speech and Visual Forms 362–380 (MIT Press, 1967).
  Google Scholar
• Thomas, P. et al. PANTHER: a browsable database of gene products organized by biological function, using curated protein family and subfamily classification. Nucleic Acids Res. 31, 334–341 (2003).
  CAS PubMed PubMed Central Google Scholar
• Johnson, S. C. Hierarchical clustering schemes. Psychometrika 32, 241–254 (1967).
  CAS PubMed Google Scholar
• McGary, K. L., Lee, I. & Marcotte, E. M. Broad network-based predictability of Saccharomyces cerevisiae gene loss-of-function phenotypes. Genome Biol. 8, R258 (2007).
  PubMed PubMed Central Google Scholar
• Kardon, J. R. & Vale, R. D. Regulators of the cytoplasmic dynein motor. Nat. Rev. Mol. Cell Biol. 10, 854–865 (2009).
  CAS PubMed PubMed Central Google Scholar
• Horgan, C. P., Hanscom, S. R., Jolly, R. S., Futter, C. E. & McCaffrey, M. W. Rab11-FIP3 links the Rab11 GTPase and cytoplasmic dynein to mediate transport to the endosomal-recycling compartment. J. Cell Sci. 123, 181–191 (2010).
  CAS PubMed Google Scholar
• Arimoto, M. et al. The Caenorhabditis elegans JIP3 protein UNC-16 functions as an adaptor to link kinesin-1 with cytoplasmic dynein. J. Neurosci. 31, 2216–2224 (2011).
  CAS PubMed PubMed Central Google Scholar
• Balklava, Z., Pant, S., Fares, H. & Grant, B. D. Genome-wide analysis identifies a general requirement for polarity proteins in endocytic traffic. Nat. Cell Biol. 9, 1066–1073 (2007).
  CAS PubMed Google Scholar
• Guo, S. & Kemphues, K. J. par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed. Cell 81, 611–620 (1995).
  CAS PubMed Google Scholar
• Morton, D. et al. The Caenorhabditis elegans par-5 gene encodes a 14-3-3 protein required for cellular asymmetry in the early embryo. Dev. Biol. 241, 47–58 (2002).
  CAS PubMed Google Scholar
• Jin, J. et al. Proteomic, functional, and domain-based analysis of in vivo 14-3-3 binding proteins involved in cytoskeletal regulation and cellular organization. Curr. Biol. 14, 1436–1450 (2004).
  CAS PubMed Google Scholar
• Pozuelo Rubio, M. et al. 14-3-3-affinity purification of over 200 human phosphoproteins reveals new links to regulation of cellular metabolism, proliferation and trafficking. Biochem. J. 379, 395–408 (2004).
  PubMed PubMed Central Google Scholar
• Angrand, P. O. et al. Transgenic mouse proteomics identifies new 14-3-3-associated proteins involved in cytoskeletal rearrangements and cell signaling. Mol. Cell Proteomics 5, 2211–2227 (2006).
  CAS PubMed Google Scholar
• Hurd, T. et al. Phosphorylation-dependent binding of 14-3-3 to the polarity protein Par3 regulates cell polarity in mammalian epithelia. Curr. Biol. 13, 2082–2090 (2003).
  CAS PubMed Google Scholar
• Benton, R. & St Johnston, D. Drosophila PAR-1 and 14-3-3 inhibit Bazooka/PAR-3 to establish complementary cortical domains in polarized cells. Cell 115, 691–704 (2003).
  CAS PubMed Google Scholar
• Kusakabe, M. & Nishida, E. The polarity-inducing kinase Par-1 controls Xenopus gastrulation in cooperation with 14-3-3 and aPKC. EMBO J. 23, 4190–4201 (2004).
  CAS PubMed PubMed Central Google Scholar
• Berdichevsky, A., Viswanathan, M., Horvitz, H. R. & Guarente, L. C. elegans SIR-2.1 interacts with 14-3-3 proteins to activate DAF-16 and extend life span. Cell 125, 1165–1177 (2006).
  CAS PubMed Google Scholar
• Sato, T. et al. The Rab8 GTPase regulates apical protein localization in intestinal cells. Nature 448, 366–369 (2007).
  CAS PubMed Google Scholar
• Gohla, A. & Bokoch, G. M. 14-3-3 regulates actin dynamics by stabilizing phosphorylated cofilin. Curr. Biol. 12, 1704–1710 (2002).
  CAS PubMed Google Scholar
• Birkenfeld, J., Betz, H. & Roth, D. Identification of cofilin and LIM-domain-containing protein kinase 1 as novel interaction partners of 14-3-3ζ. Biochem. J. 369, 45–54 (2003).
  CAS PubMed PubMed Central Google Scholar
• Nagata-Ohashi, K. et al. A pathway of neuregulin-induced activation of cofilin-phosphatase Slingshot and cofilin in lamellipodia. J. Cell Biol. 165, 465–471 (2004).
  PubMed PubMed Central Google Scholar
• Ono, K., Parast, M., Alberico, C., Benian, G. & Ono, S. Specific requirement for two ADF/cofilin isoforms in distinct actin-dependent processes in Caenorhabditis elegans. J. Cell Sci. 116, 2073–2085 (2003).
  CAS PubMed Google Scholar
• Croce, A. et al. A novel actin barbed-end-capping activity in EPS-8 regulates apical morphogenesis in intestinal cells of Caenorhabditis elegans. Nat. Cell Biol. 6, 1173–1179 (2004).
  CAS PubMed Google Scholar
• Hüsken, K. et al. Maintenance of the intestinal tube in Caenorhabditis elegans: the role of the intermediate filament protein IFC-2. Differentiation 76, 881–896 (2008).
  PubMed Google Scholar
• Koppen, M. et al. Cooperative regulation of AJM-1 controls junctional integrity in Caenorhabditis elegans epithelia. Nat. Cell Biol. 3, 983–991 (2001).
  CAS PubMed Google Scholar
• Cowan, C. R. & Hyman, A. A. Asymmetric cell division in C. elegans: cortical polarity and spindle positioning. Annu. Rev. Cell Dev. Biol. 20, 427–453 (2004).
  CAS PubMed Google Scholar
• Boutros, M. & Ahringer, J. The art and design of genetic screens: RNA interference. Nat. Rev. Genetics 9, 554–566 (2008).
  CAS PubMed Google Scholar
• Provance, W. et al. Myosin-Vb functions as a dynamic tether for peripheral endocytic compartments during transferrin trafficking. BMC Cell Biol. 9, 44 (2008).
  PubMed PubMed Central Google Scholar
• Zenke, F. T. et al. p21-activated kinase 1 phosphorylates and regulates 14-3-3 binding to GEF-H1, a microtubule-localized Rho exchange factor. J. Biol. Chem. 279, 18392–18400 (2004).
  CAS PubMed Google Scholar
• Meek, S. E., Lane, W. S. & Piwnica-Worms, H. Comprehensive proteomic analysis of interphase and mitotic 14-3-3-binding proteins. J. Biol. Chem. 279, 32046–32054 (2004).
  CAS PubMed Google Scholar
• Chen, X. & Macara, I. G. Par-3 mediates the inhibition of LIM kinase 2 to regulate cofilin phosphorylation and tight junction assembly. J. Cell Biol. 172, 671–678 (2006).
  CAS PubMed PubMed Central Google Scholar
• Kligys, K. et al. The slingshot family of phosphatases mediates Rac1 regulation of cofilin phosphorylation, laminin-332 organization, and motility behavior of keratinocytes. J. Biol. Chem. 282, 32520–32528 (2007).
  CAS PubMed Google Scholar
• Rollason, R., Korolchuk, V., Hamilton, C., Jepson, M. & Banting, G. A CD317/tetherin-RICH2 complex plays a critical role in the organization of the subapical actin cytoskeleton in polarized epithelial cells. J. Cell Biol. 184, 721–736 (2009).
  CAS PubMed PubMed Central Google Scholar
• Torkko, J. M., Manninen, A., Schuck, S. & Simons, K. Depletion of apical transport proteins perturbs epithelial cyst formation and ciliogenesis. J. Cell Sci. 121, 1193–1203 (2008).
  CAS PubMed Google Scholar
• Desclozeaux, M. et al. Active Rab11 and functional recycling endosome are required for E-cadherin trafficking and lumen formation during epithelial morphogenesis. Am. J. Physiol. Cell Physiol. 295, C545–C556 (2008).
  CAS PubMed Google Scholar
• Cao, J., Albertson, R., Riggs, B., Field, C. M. & Sullivan, W. Nuf, a Rab11 effector, maintains cytokinetic furrow integrity by promoting local actin polymerization. J. Cell Biol. 182, 301–313 (2008).
  CAS PubMed PubMed Central Google Scholar
• Schuh, M. An actin-dependent mechanism for long-range vesicle transport. Nat. Cell Biol. 13, 1431–1436 (2011).
  CAS PubMed PubMed Central Google Scholar
• Rodal, A. A., Motola-Barnes, R. N. & Littleton, J. T. Nervous wreck and Cdc42 cooperate to regulate endocytic actin assembly during synaptic growth. J. Neurosci. 28, 8316–8325 (2008).
  CAS PubMed PubMed Central Google Scholar
• Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71–94 (1974).
  CAS PubMed PubMed Central Google Scholar
• Praitis, V., Casey, E., Collar, D. & Austin, J. Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics 157, 1217–1226 (2001).
  CAS PubMed PubMed Central Google Scholar
• Simmer, F. et al. Genome-wide RNAi of C. elegans using the hypersensitive rrf-3 strain reveals novel gene functions. PLoS Biol. 1, E12 (2003).
  PubMed PubMed Central Google Scholar
• Rolls, M. M., Hall, D. H., Victor, M., Stelzer, E.H. & Rapoport, T. A. Targeting of rough endoplasmic reticulum membrane proteins and ribosomes in invertebrate neurons. Mol. Biol. Cell 13, 1778–1791 (2002).
  CAS PubMed PubMed Central Google Scholar
• Chen, C. C. et al. RAB-10 is required for endocytic recycling in the Caenorhabditis elegans intestine. Mol. Biol. Cell 17, 1286–1297 (2006).
  CAS PubMed PubMed Central Google Scholar
• Berdichevsky, A., Viswanathan, M., Horvitz, H. R. & Guarente, L. C. elegans SIR-2.1 interacts with 14-3-3 proteins to activate DAF-16 and extend life span. Cell 125, 1165–1177 (2006).
  CAS PubMed Google Scholar
• Sato, T. et al. The Rab8 GTPase regulates apical protein localization in intestinal cells. Nature 448, 366–369 (2007).
  CAS PubMed Google Scholar
• Timmons, L., Court, D. L. & Fire, A. Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263, 103–112 (2001).
  CAS PubMed Google Scholar
• Kamath, R. S. & Ahringer, J. Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30, 313–321 (2003).
  CAS PubMed Google Scholar
• Gillingham, A. K., Pfeifer, A. C. & Munro, S. CASP, the alternatively spliced product of the gene encoding the CCAAT-displacement protein transcription factor, is a Golgi membrane protein related to giantin. Mol. Biol. Cell 13, 3761–3774 (2002).
  CAS PubMed PubMed Central Google Scholar
• Van Fürden, D., Johnson, K., Segbert, C. & Bossinger, O. The C. elegans ezrin–radixin–moesin protein ERM-1 is necessary for apical junction remodelling and tubulogenesis in the intestine. Dev. Biol. 272, 262–276 (2004).
  PubMed Google Scholar
• Poteryaev, D., Fares, H., Bowerman, B. & Spang, A. Caenorhabditis elegans SAND-1 is essential for RAB-7 function in endosomal traffic. EMBO J. 26, 301–312 (2007).
  CAS PubMed PubMed Central Google Scholar
• Hannak, E., Kirkham, M., Hyman, A. A. & Oegema, K. Aurora-A kinase is required for centrosome maturation in Caenorhabditis elegans. J. Cell Biol. 155, 1109–1116 (2001).
  CAS PubMed PubMed Central Google Scholar
• Croce, A. et al. A novel actin barbed-end-capping activity in EPS-8 regulates apical morphogenesis in intestinal cells of Caenorhabditis elegans. Nat. Cell Biol. 6, 1173 (2004).
  CAS PubMed Google Scholar
• Hoege, C. et al. LGL can partition the cortex of one-cell Caenorhabditis elegans embryos into two domains. Curr. Biol. 20, 1296–1303 (2010).
  CAS PubMed Google Scholar
• Schonegg, S. & Hyman, A. A. CDC-42 and RHO-1 coordinate acto-myosin contractility and PAR protein localization during polarity establishment in C. elegans embryos. Development 133, 3507–3516 (2006).
  CAS PubMed Google Scholar
• Aono, S., Legouis, R., Hoose, W. & Kemphues, K. PAR-3 is required for epithelial cell polarity in the distal spermatheca of C. elegans. Development 131, 2865–2874 (2004).
  CAS PubMed Google Scholar