Abstract
The development of a multicellular organism is mosdy controlled at the transcriptional level but it has also been shown to require the transport of membrane and proteins through the exocytic pathway to the plasma membrane and the extracellular medium. As they are transported in the different compartments making up this pathway, newly synthesized proteins are modified and dispatched to their final destinations. In this chapter, we will first outline how mutations in genes encoding key proteins of this pathway, such as components of the COPII coat, tethers, components of the SNARE machinery, glycosylation enzymes, etc, lead to severe developmental defects. In the second part, we will describe how specific steps of epithelial development, such as epithelial cell formation, establishment of polarity, junction formation and morphogen secretion, are controlled or regulated by the exocytic machinery.
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References
Dudu V, Pantazis P, Gonzalez-Gaitan M. Membrane traffic during embryonic development: Epithelial formation, cell fate decisions and differentiation. Curr Opi Cell Biol 2004; 16:407–14.
Emery G, Knoblich JA. Endosome dynamics during development. Curr Opi Cell Biol 2006; 18:407–15.
Aridor M, Hannan LA. Traffic jam: A compendium of human diseases that affect intracellular transport processes. Traffic 2000; 1:836–51.
Aridor M, Hannan LA. Traffic jams II: An update of diseases of intracellular transport. Traffic 2002; 3:781–90.
Mellman I, Warren G. The road taken: Past and future foundations of membrane traffic. Cell 2000; 100:99–112.
Aridor M. Visiting the ER: The endoplasmic reticulum as a target for therapeutics in traffic related diseases. Adv Drug Del Rev 2007; 59:759–81.
Boyadjiev SA, Fromme JC, Ben J et al. Cranio-lenticulo-sutural dysplasia is caused by a SEC23A mutation leading to abnormal endoplasmic-reticulum-to-Golgi trafficking. Nat Genet 2006; 38:1192–7.
Lang MR, Lapierre LA, Frotscher M et al. Secretory COPII coat component Sec23a is essential for craniofacial chondrocyte maturation. Nat Genet 2006; 38:1198–203.
Fromme JC, Ravazzola M, Hamamoto S et al. The genetic basis of a craniofacial disease provides insight into COPII coat assembly. Dev Cell 2007; 13:623–34.
Hughes H, Stephens DJ. Assembly, organization, and function of the COPII coat. Histochem Cell Biol 2008; 129(2):129–51.
Jones B, Jones EL, Bonney SA et al. Mutations in a Sari GTPase of COPII vesicles are associated with lipid absorption disorders. Nat Genet 2003; 34:29–31.
Shoulders CC, Stephens DJ, Jones B. The intracellular transport of chylomicrons requires the small GTPase, Sarlb. Curr Opi Lipid 2004; 15:191–7.
Ye B, Zhang Y, Song W et al. Growing dendrites and axons differ in their reliance on the secretory pathway. Cell 2007; 130:717–29.
Miller EA, Beilharz TH, Malkus PN et al. Multiple cargo binding sites on the COPII subunit Sec24p ensure capture of diverse membrane proteins into transport vesicles. Cell 2003; 114:497–509.
Appenzeller C, Andersson H, Kappeler F et al. The lectin ERGIC-53 is a cargo transport receptor for glycoproteins. Nat Cell Biol 1999; 1:330–4.
Hauri HP, Kappeler F, Andersson H et al. ERGIC-53 and traffic in the secretory pathway. J Cell Sci 2000; 113:587–96.
Nichols WC, Seligsohn U, Zivelin A et al. Mutations in the ER-Golgi intermediate compartment protein ERGIC-53 cause combined deficiency of coagulation factors V and VIII. Cell 1998; 93:61–70.
Zhang B, Cunningham MA, Nichols WC et al. Bleeding due to disruption of a cargo-specific ER-to-Golgi transport complex. Nat Genet 2003; 34:220–5.
Barlowe C. Signals for COPII-dependent export from the ER: What’s the ticket out? Trend Cell Biol 2003; 13:295–300.
Powers J, Barlowe C. Transport of axl2p depends on ervl4p, an ER-vesicle protein related to the Drosophila cornichon gene product. J Cell Biol 1998; 142:1209–22.
Roth S, Neuman-Silberberg FS, Barcelo G et al. cornichon and the EGF receptor signaling process are necessary for both anterior-posterior and dorsal-ventral pattern formation in Drosophila. Cell 1995; 81:967–78.
Bokel C, Dass S, Wilsch-Brauninger M et al. Drosophila Cornichon acts as cargo receptor for ER export of the TGFalpha-like growth factor Gurken. Development 2006; 133:459–70.
Rabouille C, Klumperman J. Opinion: The maturing role of COPI vesicles in intra-Golgi transport. Nat Rev Mol Cell Biol 2005; 6:812–7.
Gillingham AK, Munro S. The small G proteins of the ARF family and their regulators. Annu Rev Cell Dev Biol 2007; 23:579–611.
Short B, Haas A, Barr FA. Golgins and GTPases, giving identity and structure to the Golgi apparatus. Biochim Biophys Acta 2005; 1744:383–95.
Coutelis JB, Ephrussi A. Rab6 mediates membrane organization and determinant localization during Drosophila oogenesis. Development 2007; 134:1419–30.
Januschke J, Nicolas E, Compagnon J et al. Rab6 and the secretory pathway affect oocyte polarity in Drosophila. Development 2007; 134:3419–25.
Grigoriev I, Splinter D, Keijzer N et al. Rab6 regulates transport and targeting of exocytotic carriers. Dev Cell 2007; 13:305–14.
Matanis T, Akhmanova A, Wulf P et al. Bicaudal-D regulates COPI-independent Golgi-ER transport by recruiting the dynein-dynactin motor complex. Nat Cell Biol 2002; 4:986–92.
Oka T, Krieger M. Multi-component protein complexes and Golgi membrane trafficking. J Biochem 2005; 137:109–14.
Haas AK, Barr FA. COP sets TRAPP for vesicles. Dev Cell 2007; 12:326–7.
Morozova N, Liang Y, Tokarev AA et al. TRAPPII subunits are required for the specificity switch of a Ypt-Rab GEF. Nat Cell Biol 2006; 8:1263–9.
Ungar D, Oka T, Krieger M et al. Retrograde transport on the COG railway. Trend Cell Biol 2006; 16:113–20.
Sollner T, Whiteheart SW, Brunner M et al. SNAP receptors implicated in vesicle targeting and fusion. Nature 1993; 362:318–24.
Rothman JE. Mechanisms of intracellular protein transport. Nature 1994; 372:55–63.
Jahn R, Scheller RH. SNAREs—engines for membrane fusion. Nature Rev Mol Cell Biol 2006; 7:631–43.
Wu MN, Bellen HJ. Genetic dissection of synaptic transmission in Drosophila. Curr Opi Neurobiol 1997; 7:624–30.
Hepp R, Langley K. SNAREs during development. Cell Tissue Res 2001; 305:247–53.
Stewart BA. Membrane trafficking in Drosophila wing and eye development. Sem Cell Dev Biol 2002; 13:91–7.
Rao SS, Stewart BA, Rivlin PK et al. Two distinct effects on neurotransmission in a temperaturesensitive SNAP-25 mutant. EMBO J 2001; 20:6761–71.
Littleton JT. A genomic analysis of membrane trafficking and neurotransmitter release in Drosophila. J Cell Biol 2000; 150:F77–82.
Schulze KL, Broadie K, Perin MS et al. Genetic and electrophysiological studies of Drosophila syntaxin-1A demonstrate its role in nonneuronal secretion and neurotransmission. Cell 1995; 80:311–20.
Sharma N, Low SH, Misra S et al. Apical targeting of syntaxin 3 is essential for epithelial cell polarity. J Biol Chem 2006; 173:937–48.
Moussian B, Veerkamp J, Muller U et al. Assembly of the Drosophila larval exoskeleton requires controlled secretion and shaping of the apical plasma membrane. Matrix Biol 2007; 26:337–47.
Chae TH, Kim S, Marz KE et al. The hyh mutation uncovers roles for alpha Snap in apical protein localization and control of neural cell fate. Nat Genet 2004; 36:264–70.
Hong HK, Chakravarti A, Takahashi JS. The gene for soluble N-ethylmaleimide sensitive factor attachment protein alpha is mutated in hydrocephaly with hop gait (hyh) mice. Proc Natl Acad Sci (USA) 2004; 101:1748–53.
Bajjalieh S. Trafficking in cell fate. Nat Genet 2004; 36:216–7.
Sudhof TC, De Camilli P, Niemann H et al. Membrane fusion machinery: Insights from synaptic proteins. Cell 1993; 75:1–4.
Littleton JT, Bellen HJ. Presynaptic proteins involved in exocytosis in Drosophila melanogaster: A genetic analysis. Invert Neurosci 1995; 1:3–13.
Pilot F, Philippe JM, Lemmers C et al. Spatial control of actin organization at adherens junctions by a synaptotagmin-like protein Btsz. Nature 2006; 442:580–4.
Bretscher A, Edwards K, Fehon RG. ERM proteins and merlin: Integrators at the cell cortex. Nat Rev Mol Cell Biol 2002; 3:586–99.
Grunewald S. Congenital disorders of glycosylation: Rapidly enlarging group of (neuro)metabolic disorders. Early Hum Dev 2007; 83:825–30.
Leroy JG. Congenital disorders of N-glycosylation including diseases associated with O-as well as N-glycosylation defects. Pediatric Res 2006; 60:643–56.
Freeze HH. Congenital disorders of glycosylation: CDG-I, CDG-II, and beyond. Curr Mol Med 2007; 7:389–96.
Zeevaert R, Foulquier F, Jaeken J et al. Deficiencies in subunits of the Conserved Oligomeric Golgi (COG) complex define a novel group of Congenital Disorders of Glycosylation. Mol Genet Metab 2007; 93:15–21.
Chui D, Oh-Eda M, Liao YF et al. Alpha-mannosidase-II deficiency results in dyserythropoiesis and unveils an alternate pathway in oligosaccharide biosynthesis. Cell 1997; 90:157–67.
Akama TO, Nakagawa H, Wong NK et al. Essential and mutually compensatory roles of a-mannosidase II and a-mannosidase IIx in N-glycan processing in vivo in mice. PNAS USA 2006; 103:8983–8.
Chui D, Sellakumar G, Green R et al. Genetic remodeling of protein glycosylation in vivo induces autoimmune disease. PNAS USA 2001; 98:1142–7.
Green RS, Stone EL, Tenno M et al. Mammalian N-glycan branching protects against innate immune self-recognition and inflammation in autoimmune disease pathogenesis. Immunity 2007; 27:308–20.
Campbell RM, Metzler M, Granovsky M et al. Complex asparagine-linked oligosaccharides in Mgatl-null embryos. Glycobiology 1995; 5:535–43.
Mendelsohn R, Cheung P, Berger L et al. Complex N-glycan and metabolic control in tumor cells. Cancer Res 2007; 67:9771–80.
Lagana A, Goetz JG, Cheung P et al. Galectin binding to Mgat5-modified N-glycans regulates fibronectin matrix remodeling in tumor cells. Mol Cell Biol 2006; 26:3181–93.
Cheung P, Dennis JW. Mgat5 and Pten interact to regulate cell growth and polarity. Glycobiology 2007; 17:767–73.
Bruckner K, Perez L, Clausen H et al. Glycosyltransferase activity of Fringe modulates Notch-Delta interactions. Nature 2000; 406:411–5.
Munro S, Freeman M. The notch signalling regulator fringe acts in the Golgi apparatus and requires the glycosyltransferase signature motif DXD. Curr Biol 2000; 10:813–20.
Rampal R, Li AS, Moloney DJ et al. Lunatic fringe, manic fringe, and radical fringe recognize similar specificity determinants in O-fucosylated epidermal growth factor-like repeats. J Biol Chem 2005; 280:42454–63.
Favier B, Fliniaux I, Thelu J et al. Localisation of members of the notch system and the differentiation of vibrissa hair follicles: Receptors, ligands, and fringe modulators. Dev Dyn 2000; 218:426–37.
Moloney DJ, Panin VM, Johnston SH et al. Fringe is a glycosyltransferase that modifies Notch. Nature 2000; 406:369–75.
Aulehla A, Herrmann BG. Segmentation in vertebrates: Clock and gradient finally joined. Genes Dev 2004; 18:2060–7.
Serth K, Schuster-Gossler K, Cordes R et al. Transcriptional oscillation of lunatic fringe is essential for somitogenesis. Genes Dev 2003; 17:912–25.
Rabouille C, Warren G. The changes in the architecture of the Golgi apparatus during mitosis. In: Berger EG, Roth, eds. The Golgi Apparatus. Basel/Switzerland: Birkhauser Verlag, 1997.
Kondylis V, van Nispen tot Pannerden HE, Herpers B et al. The Golgi comprises a paired stack that is separated at G2 by modulation of the actin cytoskeleton through Abi and Scar/WAVE. Dev Cell 2007; 12:901–15.
Barr FA, Puype M, Vandekerckhove J et al. GRASP65, a protein involved in the stacking of Golgi cisternae. Cell 1997; 91:253–62.
Shorter J, Watson R, Giannakou ME et al. GRASP55, a second mammalian GRASP protein involved in the stacking of Golgi cisternae in a cell-free system. EMBO J 1999; 18:4949–60.
Kondylis V, Spoorendonk KM, Rabouille C. dGRASP localization and function in the early exocytic pathway in Drosophila S2 cells. Mol Biol Cell 2005; 16:4061–72.
Sütterlin C, Polishchuk RS, Pecot M et al. The Golgi-associated protein GRASP65 regulates spindle dynamics and is essential for cell division. Mol Biol Cell 2005; 16:3211–22.
Kinseth MA, Anjard C, Fuller D et al. The Golgi-associated protein GRASP is required for unconventional protein secretion during development. Cell 2007; 130:524–34.
Levi SK, Glick BS. GRASPing unconventional secretion. Cell 2007; 130:407–9.
Schotman H, Karhinen L, Rabouille C. The dGRASP mediated noncanonical integrin secretion is required for Drosophila epithelial remodelling. Dev Cell 2008; 14:171–82.
Bonifacino JS, Traub LM. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Bioch 2003; 72:395–447.
Bonifacino JS. The GGA proteins: Adaptors on the move. Nat Rev Mol Cell Biol 2004; 5:23–32.
Ponnambalam S, Baldwin SA. Constitutive protein secretion from the trans-Golgi network to the plasma membrane. Mol Memb Biol 2003; 20:129–39.
Bossard C, Bresson D, Polishchuk RS et al. Dimeric PKD regulates membrane fission to form transport carriers at the TGN. J Cell Biol 2007; 179:1123–31.
Maier D, Nagel AC, Gloc H et al. Protein kinase D regulates several aspects of development in Drosophila melanogaster. BMC Dev Biol 2007; 7:74–81.
Van Lint J, Rykx A, Maeda Y et al. Protein kinase D: An intracellular traffic regulator on the move. Trends Cell Biol 2002; 12:193–200.
Hsu SC, TerBush D, Abraham M et al. The exocyst complex in polarized exocytosis. Int Rev Cytol 2004; 233:243–65.
Guo W, Roth D, Walch-Solimena C et al. The exocyst is an effector for Sec4p, targeting secretory vesicles to sites of exocytosis. EMBO J 1999; 18:1071–80.
Walch-Solimena C, Collins RN, Novick PJ. Sec2p mediates nucleotide exchange on Sec4p and is involved in polarized delivery of post-Golgi vesicles. J Cell Biol 1997; 137:1495–509.
Grote E, Carr CM, Novick PJ. Ordering the final events in yeast exocytosis. J Cell Biol 2000; 151:439–52.
Grindstaff KK, Yeaman C, Anandasabapathy N et al. Sec6/8 complex is recruited to cell-cell contacts and specifies transport vesicle delivery to the basal-lateral membrane in epithelial cells. Cell 1998; 93:731–40.
Moskalenko S, Henry DO, Rosse C et al. The exocyst is a Ral effector complex. Nat Cell Biol 2002; 4:66–72.
Vega IE, Hsu SC. The exocyst complex associates with microtubules to mediate vesicle targeting and neurite outgrowth. J Neurosci 2001; 21:3839–48.
Inoue M, Chang L, Hwang J et al. The exocyst complex is required for targeting of Glut4 to the plasma membrane by insulin. Nature 2003; 422:629–33.
Sommer B, Oprins A, Rabouille C et al. The exocyst component Sec5 is present on endocytic vesicles in the oocyte of Drosophila melanogaster. J Cell Biol 2005; 169:953–63.
Foe VE, Odell GM, Edgar BA. Mitosis and morphogenesis in the Drosophila embryo. In: Bate M, Martinez-Arias A, eds. The Development of Drosophila melanogaster. Cold Spring Harbor: Cold Spring Harbor Laboratory, 1993:149–300.
Warn RM, Robert-Nicoud M. F-actin organization during the cellularization of the Drosophila embryo as revealed with a confocal laser scanning microscope. J Cell Sci 1990; 96:35–42.
Lecuit T, Samanta R, Wieschaus E. slam encodes a developmental regulator of polarized membrane growth during cleavage of the Drosophila embryo. Dev Cell 2002; 2:425–36.
Royou A, Field C, Sisson JC et al. Reassessing the role and dynamics of nonmuscle myosin II during furrow formation in early Drosophila embryos. Mol Biol Cell 2004; 15:838–50.
Sisson JC, Field C, Ventura R et al. Lava lamp, a novel peripheral golgi protein, is required for Drosophila melanogaster cellularization. J Cell Biol 2000; 151:905–18.
Young PE, Pesacreta TC, Kiehart DP. Dynamic changes in the distribution of cytoplasmic myosin during Drosophila embryogenesis. Development 1991; 111:1–14.
Field CM, Alberts BM. Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex. J Cell Biol 1995; 131:165–78.
Thomas GH, Williams JA. Dynamic rearrangement of the spectrin membrane skeleton during the generation of epithelial polarity in Drosophila. J Cell Sci 1999; 112:2843–52.
Adam JC, Pringle JR, Peifer M. Evidence for functional differentiation among Drosophila septins in cytokinesis and cellularization. Mol Biol Cell 2000; 11:3123–35.
Fares H, Peifer M, Pringle JR. Localization and possible functions of Drosophila septins. Mol Biol Cell 1995; 6:1843–59.
Afshar K, Stuart B, Wasserman SA. Functional analysis of the Drosophila diaphanous FH protein in early embryonic development. Development 2000; 127:1887–97.
Lecuit T. Polarized insertion of new membrane from a cytoplasmic reservoir during cleavage of the Drosophila embryo. J Cell Biol 2000; 150:849–60.
Chardin P, McCormick F. Brefeldin A: The advantage of being uncompetitive. Cell 1999; 97:153–5.
Frescas D, Mavrakis M, Lorenz H et al. The secretory membrane system in the Drosophila syncytial blastoderm embryo exists as functionally compartmentalized units around individual nuclei. J Cell Biol 2006; 173:219–30.
Burgess RW, Deitcher DL, Schwarz TL. The synaptic protein syntaxin 1 is required for cellularization of Drosophila embryos. J Cell Biol 1997; 138:861–75.
Fremion F, Astier M, Zaffran S et al. The heterotrimeric protein Go is required for the formation of heart epithelium in Drosophila. J Cell Biol 1999; 145:1063–76.
Nelson WJ. Cytoskeleton functions in membrane traffic in polarized epithelial cells. Semin Cell Biol 1991; 2:375–85.
Mays RW, Beck KA, Nelson WJ. Organization and function of the cytoskeleton in polarized epithelial cells: A component of the protein sorting machinery. Curr Opin Cell Biol 1994; 6:16–24.
Tanentzapf G, Tepass U. Interactions between the crumbs, lethal giant larvae and bazooka pathways in epithelial polarization. Nat Cell Biol 2003; 5:46–52.
Bilder D, Schober M, Perrimon N. Integrated activity of PDZ protein complexes regulates epithelial polarity. Nat Cell Biol 2003; 5:53–8.
Horne-Badovinac S, Bilder D. Mass transit: Epithelial morphogenesis in the Drosophila egg chamber. Dev Dyn 2005; 232:559–74.
Nelson WJ. Adaptation of core mechanisms to generate cell polarity. Nature 2003; 422:766–74.
Bilder D. Epithelial polarity and proliferation control: Links from the Drosophila neoplastic tumor suppressors. Genes Dev 2004; 18:1909–25.
Lehman K, Rossi G, Adamo JE et al. Yeast homologues of tomosyn and lethal giant larvae function in exocytosis and are associated with the plasma membrane SNARE, Sec9. J Cell Biol 1999; 146:125–40.
Mostov KE, Verges M, Altschuler Y. Membrane traffic in polarized epithelial cells. Curr Opi Cell Biol 2000; 12:483–90.
Low SH, Chapin SJ, Weimbs T et al. Differential localization of syntaxin isoforms in polarized Madin-Darby canine kidney cells. Mol Biol Cell 1996; 7:2007–18.
Musch A, Cohen D, Yeaman C et al. Mammalian homolog of Drosophila tumor suppressor lethal (2) giant larvae interacts with basolateral exocytic machinery in Madin-Darby canine kidney cells. Mol Biol Cell 2002; 13:158–68.
Fujita Y, Shirataki H, Sakisaka T et al. Tomosyn: A syntaxin-1-binding protein that forms a novel complex in the neurotransmitter release process. Neuron 1998; 20:905–15.
Vaccari T, Rabouille C, Ephrussi A. The Drosophila PAR-1 spacer domain is required for lateral membrane association and for polarization of follicular epithelial cells. Curr Biol 2005; 15:255–61.
Elbert M, Rossi G, Brennwald P. The yeast par-1 homologs kinl and kin2 show genetic and physical interactions with components of the exocytic machinery. Mol Biol Cell 2005; 16:532–49.
Tepass U, Gruszynski-DeFeo E, Haag TA et al. shotgun encodes Drosophila E-cadherin and is preferentially required during cell rearrangement in the neurectoderm and other morphogenetically active epithelia. Genes and Development 1996; 10:672–85.
Uemura T, Oda H, Kraut R et al. Zygotic Drosophila E-cadherin expression is required for processes of dynamic epithelial cell rearrangement in the Drosophila embryo. Gene Dev 1996; 10:659–71.
Muller HA, Wieschaus E. armadillo, bazooka, and Stardust are critical for early stages in formation of the zonula adherens and maintenance of the polarized blastoderm epithelium in Drosophila. J Cell Biol 1996; 134:149–63.
Tepass U, Theres C, Knust E. Crumbs encodes an EGF-like protein expressed on apical membranes of Drosophila epithelial cells and required for organization of epithelia. Cell 1990; 61:787–99.
Wodarz A, Hinz U, Engelbert M et al. Expression of crumbs confers apical character on plasma membrane domains of ectodermal epithelia of Drosophila. Cell 1995; 82:67–76.
Bhat MA, Izaddoost S, Lu Y et al. Discs Lost, a novel multi-PDZ domain protein, establishes and maintains epithelial polarity. Cell 1999; 96:833–45.
Pielage J, Stork T, Bunse I et al. The Drosophila cell survival gene discs lost encodes a cytoplasmic Codanin-1-like protein, not a homolog of tight junction PDZ protein Patj. Dev Cell 2003; 5:841–51.
Tepass U, Tanentzapf G, Ward R et al. Epithelial cell polarity and cell junctions in Drosophila. Annu Rev Genet 2001; 35:747–84.
Tsukita S, Furuse M, Itoh M. Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol 2001; 2:285–93.
Ebnet K, Suzuki A, Ohno S et al. Junctional adhesion molecules (JAMs): More molecules with dual functions? J Cell Sci 2004; 117:19–29.
Hirabayashi S, Tajima M, Yao I et al. JAM4, a junctional cell adhesion molecule interacting with a tight junction protein, MAGI-1. Mol Cell Biol 2003; 23:4267–82.
Van Itallie CM, Anderson JM. The molecular physiology of tight junction pores. Physiology 2004; 19:331–8.
Behr M, Riedel D, Schuh R. The claudin-like megatrachea is essential in septate junctions for the epithelial barrier function in Drosophila. Dev Cell 2003; 5:611–20.
Wu VM, Schulte J, Hirschi A et al. Sinuous is a Drosophila claudin required for septate junction organization and epithelial tube size control. J Cell Biol 2004; 164:313–23.
Baumgartner S, Littleton JT, Broadie K et al. A Drosophila neurexin is required for septate junction and blood-nerve barrier formation and function. Cell 1996; 87:1059–68.
Genova JL, Fehon RG. Neuroglian, Gliotactin, and the Na+/K+ ATPase are essential for septate junction function in Drosophila. J Cell Biol 2003; 161:979–89.
Faivre-Sarrailh C, Banerjee S, Li J et al. Drosophila contactin, a homolog of vertebrate contactin, is required for septate junction organization and paracellular barrier function. Development 2004; 131:4931–42.
Auld VJ, Fetter RD, Broadie K et al. Gliotactin, a novel transmembrane protein on peripheral glia, is required to form the blood-nerve barrier in Drosophila. Cell 1995; 81:757–67.
Schulte J, Tepass U, Auld VJ. Gliotactin, a novel marker of tricellular junctions, is necessary for septate junction development in Drosophila. J Cell Biol 2003; 161:991–1000.
Snow PM, Bieber AJ, Goodman CS. Fasciclin III: A novel homophilic adhesion molecule in Drosophila. Cell 1989; 59:313–23.
Knust, Bossinger. Composition and formation of intercellular junctions in epithelial cells. Science 2002; 298:1955–9.
Paul SM, Ternet M, Salvaterra PM et al. The Na+/K+ ATPase is required for septate junction function and epithelial tube-size control in the Drosophila tracheal system. Development 2003; 130:4963–74.
Huber AH, Stewart DB, Laurents DV et al. The cadherin cytoplasmic domain is unstructured in the absence of beta-catenin: A possible mechanism for regulating cadherin turnover. J Biol Chem 2001; 276:12301–9.
Chen YT, Stewart DB, Nelson WJ. Coupling assembly of the E-cadherin/beta-catenin complex to efficient endoplasmic reticulum exit and basal-lateral membrane targeting of E-cadherin in polarized MDCK cells. J Cell Biol 1999; 144:687–99.
Miranda KC, Joseph SR, Yap AS et al. Contextual binding of pl20ctn to E-cadherin at the basolateral plasma membrane in polarized epithelia. J Biol Chem 2003; 278:43480–8.
Lock JG, Hammond LA, Houghton F et al. E-cadherin transport from the trans-Golgi network in tubulovesicular carriers is selectively regulated by golgin-97. Traffic 2005; 6:1142–56.
Miranda KC, Khromykh T, Christy P et al. A dileucine motif targets E-cadherin to the basolateral cell surface in Madin-Darby canine kidney and LLC-PK1 epithelial cells. J Biol Chem 2001; 276:22565–72.
Blankenship JT, Fuller MT, Zallen JA. The Drosophila homolog of the Exo84 exocyst subunit promotes apical epithelial identity. J Cell Sci 2007; 120:3099–110.
Langevin J, Morgan MJ, Sibarita JB et al. Drosophila exocyst components Sec5, Sec6, and Seel5 regulate DE-Cadherin trafficking from recycling endosomes to the plasma membrane. Dev Cell 2005; 9:355–76.
Zallen JA, Wieschaus E. Patterned gene expression directs bipolar planar polarity in Drosophila. Developmental Cell 2004; 6:343–55.
Bertet C, Sulak L, Lecuit T. Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 2004; 429:667–71.
Lubarsky B, Krasnow MA. Tube morphogenesis: Making and shaping biological tubes. Cell 2003; 112:19–28.
Neumann M, Affolter M. Remodelling epithelial tubes through cell rearrangements: From cells to molecules. EMBO Rep 2006; 7:36–40.
Hynes RO. Integrins: Versatility, modulation, and signaling in cell adhesion. Cell 1992; 69:11–25.
Cohen LA, Guan JL. Mechanisms of focal adhesion kinase regulation. Curr Cancer Drug Targets 2005; 5:629–43.
Caswell PT, Norman JC. Integrin trafficking and the control of cell Migration. Traffic 2006; 7:14–21.
Le Borgne R, Bardin A, Schweisguth F. The roles of receptor and ligand endocytosis in regulating Notch signaling. Development 2005; 132:1751–62.
Knoblich JA. Sara splits the signal. Science 2006; 314:1094–6.
Somers WG, Chia W. Recycling polarity. Dev Cell 2005; 9:312–3.
Logan CY, Nusse R. The wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 2004; 20:781–810.
Ingham PW, McMahon AP. Hedgehog signaling in animal development: Paradigms and principles. Genes Dev 2001; 15:3059–87.
Vincent JP, Dubois L. Morphogen transport along epithelia, an integrated trafficking problem. Dev Cell 2002; 3:615–23.
Hausmann G, Banziger C, Basler K. Helping Wingless take flight: How WNT proteins are secreted. Nat Rev Mol Cell Biol 2007; 8:331–6.
Guerrero I, Chiang C. A conserved mechanism of Hedgehog gradient formation by lipid modifications. Trend Cell Biol 2006; 17:1–5.
Willert K, Brown JD, Danenberg E et al. Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 2003; 423:448–52.
Coudreuse D, Korswagen HC. The making of Wnt: New insights into Wnt maturation, sorting and secretion. Development 2007; 134:3–12.
Takada R, Satomi Y, Kurata T et al. Monounsaturated fatty acid modification of Wnt protein: Its role in Wnt secretion. Dev Cell 2006; 11:791–801.
Hofmann K. A superfamily of membrane-bound O-acyltransferases with implications for wnt signaling. Trend Biochem Sci 2000; 25:111–2.
Kadowaki T, Wilder E, Klingensmith J et al. The segment polarity gene porcupine encodes a putative multitransmembrane protein involved in Wingless processing. Genes Dev 1996; 10:3116–28.
van den Heuvel M, Harryman-Samos C, Klingensmith J et al. Mutations in the segment polarity genes wingless and porcupine impair secretion of the wingless protein. EMBO J 1993; 12:5293–302.
van den Heuvel M, Nusse R, Johnston P et al. Distribution of the wingless gene product in Drosophila embryos: A protein involved in cell-cell communication. Cell 1989; 59:739–49.
Amanai K, Jiang J. Distinct roles of Central missing and Dispatched in sending the Hedgehog signal. Development 2001; 128:5119–27.
Chamoun Z, Mann RK, Nellen D et al. Skinny hedgehog, an acyltransferase required for palmitoylation and activity of the hedgehog signal. Science 2001; 293:2080–4.
Lee JD, Treisman JE. Sightless has homology to transmembrane acyltransferases and is required to generate active Hedgehog protein. Curr Biol 2001; 11:1147–52.
Micchelli CA, The I, Selva E et al. Rasp, a putative transmembrane acyltransferase, is required for Hedgehog signaling. Development 2002; 129:843–51.
Panakova D, Sprong H, Marois E et al. Lipoprotein particles are required for Hedgehog and Wingless signalling. Nature 2005; 435:58–65.
Eaton S. Release and trafficking of lipid-linked morphogens. Curr Opi Gen Dev 2006; 16:17–22.
Bartscherer K, Pelte N, Ingelfinger D et al. Secretion of Wnt ligands requires Evi, a conserved transmembrane protein. Cell 2006; 125:523–33.
Banziger C, Soldini D, Schutt C et al. Wndess, a conserved membrane protein dedicated to the secretion of Wnt proteins from signaling cells. Cell 2006; 125:509–22.
Burke R, Nellen D, Bellotto M et al. Dispatched, a novel sterol-sensing domain protein dedicated to the release of cholesterol-modified hedgehog from signaling cells. Cell 1999; 99:803–15.
Zeng X, Goetz JA, Suber LM et al. A freely diffusible form of Sonic hedgehog mediates long-range signalling. Nature 2001; 411:716–20.
Coudreuse DY, Roel G, Betist MC et al. Wnt gradient formation requires retromer function in Wnt-producing cells. Science 2006; 312:921–4.
Prasad BC, Clark SG. Wnt signaling establishes anteroposterior neuronal polarity and requires retromer in C. elegans. Development 2006; 133:1757–66.
Belenkaya TY, Wu Y, Tang X et al. The retromer complex influences wnt secretion by recycling wntless from endosomes to the trans-Golgi network. Dev Cell 2008; 14:120–31.
Franch-Marro X, Wendler F, Guidato S et al. Wingless secretion requires endosome-to-Golgi retrieval of Wntless/Evi/Sprinter by the retromer complex. Nat Cell Biol 2008; 10:170–7.
Pan CL, Baum PD, Gu M et al. C. elegans AP-2 and Retromer Control Wnt Signaling by Regulating MIG-14/Wndess. Dev Cell 2008; 14:132–9.
Port F, Kuster M, Herr P et al. Wingless secretion promotes and requires retromer-dependent cycling of Wntless. Nat Cell Biol 2008; 10:178–85.
Yang PT, Lorenowicz M, Silhankova M et al. Wnt Signaling Requires Retromer-Dependent Recycling of MIG-14/Wntless in Wnt-Producing Cells. Dev Cell 2008; 14:140–7.
Eaton S. Retromer retrieves Wndess. Dev Cell 2008; 14:4–6.
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Schotman, H., Rabouille, C. (2009). The Exocytic Pathway and Development. In: Trafficking Inside Cells. Molecular Biology Intelligence Unit. Springer, New York, NY. https://doi.org/10.1007/978-0-387-93877-6_20
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