Advertisement

The Exocytic Pathway and Development

  • Hans Schotman
  • Catherine Rabouille
Part of the Molecular Biology Intelligence Unit book series (MBIU)

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.

Keywords

MDCK Cell Adherens Junction Septate Junction COPII Vesicle Exocyst Complex 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    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.CrossRefGoogle Scholar
  2. 2.
    Emery G, Knoblich JA. Endosome dynamics during development. Curr Opi Cell Biol 2006; 18:407–15.CrossRefGoogle Scholar
  3. 3.
    Aridor M, Hannan LA. Traffic jam: A compendium of human diseases that affect intracellular transport processes. Traffic 2000; 1:836–51.PubMedCrossRefGoogle Scholar
  4. 4.
    Aridor M, Hannan LA. Traffic jams II: An update of diseases of intracellular transport. Traffic 2002; 3:781–90.PubMedCrossRefGoogle Scholar
  5. 5.
    Mellman I, Warren G. The road taken: Past and future foundations of membrane traffic. Cell 2000; 100:99–112.PubMedCrossRefGoogle Scholar
  6. 6.
    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.CrossRefGoogle Scholar
  7. 7.
    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.PubMedCrossRefGoogle Scholar
  8. 8.
    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.PubMedCrossRefGoogle Scholar
  9. 9.
    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.PubMedCrossRefGoogle Scholar
  10. 10.
    Hughes H, Stephens DJ. Assembly, organization, and function of the COPII coat. Histochem Cell Biol 2008; 129(2):129–51.PubMedCrossRefGoogle Scholar
  11. 11.
    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.PubMedCrossRefGoogle Scholar
  12. 12.
    Shoulders CC, Stephens DJ, Jones B. The intracellular transport of chylomicrons requires the small GTPase, Sarlb. Curr Opi Lipid 2004; 15:191–7.CrossRefGoogle Scholar
  13. 13.
    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.PubMedCrossRefGoogle Scholar
  14. 14.
    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.PubMedCrossRefGoogle Scholar
  15. 15.
    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.PubMedCrossRefGoogle Scholar
  16. 16.
    Hauri HP, Kappeler F, Andersson H et al. ERGIC-53 and traffic in the secretory pathway. J Cell Sci 2000; 113:587–96.PubMedGoogle Scholar
  17. 17.
    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.PubMedCrossRefGoogle Scholar
  18. 18.
    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.PubMedCrossRefGoogle Scholar
  19. 19.
    Barlowe C. Signals for COPII-dependent export from the ER: What’s the ticket out? Trend Cell Biol 2003; 13:295–300.CrossRefGoogle Scholar
  20. 20.
    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.PubMedCrossRefGoogle Scholar
  21. 21.
    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.PubMedCrossRefGoogle Scholar
  22. 22.
    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.PubMedCrossRefGoogle Scholar
  23. 23.
    Rabouille C, Klumperman J. Opinion: The maturing role of COPI vesicles in intra-Golgi transport. Nat Rev Mol Cell Biol 2005; 6:812–7.PubMedCrossRefGoogle Scholar
  24. 24.
    Gillingham AK, Munro S. The small G proteins of the ARF family and their regulators. Annu Rev Cell Dev Biol 2007; 23:579–611.PubMedCrossRefGoogle Scholar
  25. 25.
    Short B, Haas A, Barr FA. Golgins and GTPases, giving identity and structure to the Golgi apparatus. Biochim Biophys Acta 2005; 1744:383–95.PubMedCrossRefGoogle Scholar
  26. 26.
    Coutelis JB, Ephrussi A. Rab6 mediates membrane organization and determinant localization during Drosophila oogenesis. Development 2007; 134:1419–30.PubMedCrossRefGoogle Scholar
  27. 27.
    Januschke J, Nicolas E, Compagnon J et al. Rab6 and the secretory pathway affect oocyte polarity in Drosophila. Development 2007; 134:3419–25.PubMedCrossRefGoogle Scholar
  28. 28.
    Grigoriev I, Splinter D, Keijzer N et al. Rab6 regulates transport and targeting of exocytotic carriers. Dev Cell 2007; 13:305–14.PubMedCrossRefGoogle Scholar
  29. 29.
    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.PubMedCrossRefGoogle Scholar
  30. 30.
    Oka T, Krieger M. Multi-component protein complexes and Golgi membrane trafficking. J Biochem 2005; 137:109–14.PubMedCrossRefGoogle Scholar
  31. 31.
    Haas AK, Barr FA. COP sets TRAPP for vesicles. Dev Cell 2007; 12:326–7.PubMedCrossRefGoogle Scholar
  32. 32.
    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.PubMedCrossRefGoogle Scholar
  33. 33.
    Ungar D, Oka T, Krieger M et al. Retrograde transport on the COG railway. Trend Cell Biol 2006; 16:113–20.CrossRefGoogle Scholar
  34. 34.
    Sollner T, Whiteheart SW, Brunner M et al. SNAP receptors implicated in vesicle targeting and fusion. Nature 1993; 362:318–24.PubMedCrossRefGoogle Scholar
  35. 35.
    Rothman JE. Mechanisms of intracellular protein transport. Nature 1994; 372:55–63.PubMedCrossRefGoogle Scholar
  36. 36.
    Jahn R, Scheller RH. SNAREs—engines for membrane fusion. Nature Rev Mol Cell Biol 2006; 7:631–43.CrossRefGoogle Scholar
  37. 37.
    Wu MN, Bellen HJ. Genetic dissection of synaptic transmission in Drosophila. Curr Opi Neurobiol 1997; 7:624–30.CrossRefGoogle Scholar
  38. 38.
    Hepp R, Langley K. SNAREs during development. Cell Tissue Res 2001; 305:247–53.PubMedCrossRefGoogle Scholar
  39. 39.
    Stewart BA. Membrane trafficking in Drosophila wing and eye development. Sem Cell Dev Biol 2002; 13:91–7.CrossRefGoogle Scholar
  40. 40.
    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.PubMedCrossRefGoogle Scholar
  41. 41.
    Littleton JT. A genomic analysis of membrane trafficking and neurotransmitter release in Drosophila. J Cell Biol 2000; 150:F77–82.PubMedCrossRefGoogle Scholar
  42. 42.
    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.PubMedCrossRefGoogle Scholar
  43. 43.
    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.Google Scholar
  44. 44.
    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.PubMedCrossRefGoogle Scholar
  45. 45.
    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.PubMedCrossRefGoogle Scholar
  46. 46.
    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.CrossRefGoogle Scholar
  47. 47.
    Bajjalieh S. Trafficking in cell fate. Nat Genet 2004; 36:216–7.PubMedCrossRefGoogle Scholar
  48. 48.
    Sudhof TC, De Camilli P, Niemann H et al. Membrane fusion machinery: Insights from synaptic proteins. Cell 1993; 75:1–4.PubMedGoogle Scholar
  49. 49.
    Littleton JT, Bellen HJ. Presynaptic proteins involved in exocytosis in Drosophila melanogaster: A genetic analysis. Invert Neurosci 1995; 1:3–13.PubMedCrossRefGoogle Scholar
  50. 50.
    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.PubMedCrossRefGoogle Scholar
  51. 51.
    Bretscher A, Edwards K, Fehon RG. ERM proteins and merlin: Integrators at the cell cortex. Nat Rev Mol Cell Biol 2002; 3:586–99.PubMedCrossRefGoogle Scholar
  52. 52.
    Grunewald S. Congenital disorders of glycosylation: Rapidly enlarging group of (neuro)metabolic disorders. Early Hum Dev 2007; 83:825–30.PubMedCrossRefGoogle Scholar
  53. 53.
    Leroy JG. Congenital disorders of N-glycosylation including diseases associated with O-as well as N-glycosylation defects. Pediatric Res 2006; 60:643–56.CrossRefGoogle Scholar
  54. 54.
    Freeze HH. Congenital disorders of glycosylation: CDG-I, CDG-II, and beyond. Curr Mol Med 2007; 7:389–96.PubMedCrossRefGoogle Scholar
  55. 55.
    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.PubMedCrossRefGoogle Scholar
  56. 56.
    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.PubMedCrossRefGoogle Scholar
  57. 57.
    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.PubMedCrossRefGoogle Scholar
  58. 58.
    Chui D, Sellakumar G, Green R et al. Genetic remodeling of protein glycosylation in vivo induces autoimmune disease. PNAS USA 2001; 98:1142–7.PubMedCrossRefGoogle Scholar
  59. 59.
    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.PubMedCrossRefGoogle Scholar
  60. 60.
    Campbell RM, Metzler M, Granovsky M et al. Complex asparagine-linked oligosaccharides in Mgatl-null embryos. Glycobiology 1995; 5:535–43.PubMedCrossRefGoogle Scholar
  61. 61.
    Mendelsohn R, Cheung P, Berger L et al. Complex N-glycan and metabolic control in tumor cells. Cancer Res 2007; 67:9771–80.PubMedCrossRefGoogle Scholar
  62. 62.
    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.PubMedCrossRefGoogle Scholar
  63. 63.
    Cheung P, Dennis JW. Mgat5 and Pten interact to regulate cell growth and polarity. Glycobiology 2007; 17:767–73.PubMedCrossRefGoogle Scholar
  64. 64.
    Bruckner K, Perez L, Clausen H et al. Glycosyltransferase activity of Fringe modulates Notch-Delta interactions. Nature 2000; 406:411–5.PubMedCrossRefGoogle Scholar
  65. 65.
    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.PubMedCrossRefGoogle Scholar
  66. 66.
    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.PubMedCrossRefGoogle Scholar
  67. 67.
    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.PubMedCrossRefGoogle Scholar
  68. 68.
    Moloney DJ, Panin VM, Johnston SH et al. Fringe is a glycosyltransferase that modifies Notch. Nature 2000; 406:369–75.PubMedCrossRefGoogle Scholar
  69. 69.
    Aulehla A, Herrmann BG. Segmentation in vertebrates: Clock and gradient finally joined. Genes Dev 2004; 18:2060–7.PubMedCrossRefGoogle Scholar
  70. 70.
    Serth K, Schuster-Gossler K, Cordes R et al. Transcriptional oscillation of lunatic fringe is essential for somitogenesis. Genes Dev 2003; 17:912–25.PubMedCrossRefGoogle Scholar
  71. 71.
    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.Google Scholar
  72. 72.
    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.PubMedCrossRefGoogle Scholar
  73. 73.
    Barr FA, Puype M, Vandekerckhove J et al. GRASP65, a protein involved in the stacking of Golgi cisternae. Cell 1997; 91:253–62.PubMedCrossRefGoogle Scholar
  74. 74.
    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.PubMedCrossRefGoogle Scholar
  75. 75.
    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.PubMedCrossRefGoogle Scholar
  76. 76.
    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.PubMedCrossRefGoogle Scholar
  77. 77.
    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.PubMedCrossRefGoogle Scholar
  78. 78.
    Levi SK, Glick BS. GRASPing unconventional secretion. Cell 2007; 130:407–9.PubMedCrossRefGoogle Scholar
  79. 79.
    Schotman H, Karhinen L, Rabouille C. The dGRASP mediated noncanonical integrin secretion is required for Drosophila epithelial remodelling. Dev Cell 2008; 14:171–82.PubMedCrossRefGoogle Scholar
  80. 80.
    Bonifacino JS, Traub LM. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Bioch 2003; 72:395–447.CrossRefGoogle Scholar
  81. 81.
    Bonifacino JS. The GGA proteins: Adaptors on the move. Nat Rev Mol Cell Biol 2004; 5:23–32.PubMedCrossRefGoogle Scholar
  82. 82.
    Ponnambalam S, Baldwin SA. Constitutive protein secretion from the trans-Golgi network to the plasma membrane. Mol Memb Biol 2003; 20:129–39.CrossRefGoogle Scholar
  83. 83.
    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.PubMedCrossRefGoogle Scholar
  84. 84.
    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.PubMedCrossRefGoogle Scholar
  85. 85.
    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.PubMedCrossRefGoogle Scholar
  86. 86.
    Hsu SC, TerBush D, Abraham M et al. The exocyst complex in polarized exocytosis. Int Rev Cytol 2004; 233:243–65.PubMedCrossRefGoogle Scholar
  87. 87.
    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.PubMedCrossRefGoogle Scholar
  88. 88.
    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.PubMedCrossRefGoogle Scholar
  89. 89.
    Grote E, Carr CM, Novick PJ. Ordering the final events in yeast exocytosis. J Cell Biol 2000; 151:439–52.PubMedCrossRefGoogle Scholar
  90. 90.
    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.PubMedCrossRefGoogle Scholar
  91. 91.
    Moskalenko S, Henry DO, Rosse C et al. The exocyst is a Ral effector complex. Nat Cell Biol 2002; 4:66–72.PubMedCrossRefGoogle Scholar
  92. 92.
    Vega IE, Hsu SC. The exocyst complex associates with microtubules to mediate vesicle targeting and neurite outgrowth. J Neurosci 2001; 21:3839–48.PubMedGoogle Scholar
  93. 93.
    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.PubMedCrossRefGoogle Scholar
  94. 94.
    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.PubMedCrossRefGoogle Scholar
  95. 95.
    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.Google Scholar
  96. 96.
    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.PubMedGoogle Scholar
  97. 97.
    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.PubMedCrossRefGoogle Scholar
  98. 98.
    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.PubMedCrossRefGoogle Scholar
  99. 99.
    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.PubMedCrossRefGoogle Scholar
  100. 100.
    Young PE, Pesacreta TC, Kiehart DP. Dynamic changes in the distribution of cytoplasmic myosin during Drosophila embryogenesis. Development 1991; 111:1–14.PubMedGoogle Scholar
  101. 101.
    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.PubMedCrossRefGoogle Scholar
  102. 102.
    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.PubMedGoogle Scholar
  103. 103.
    Adam JC, Pringle JR, Peifer M. Evidence for functional differentiation among Drosophila septins in cytokinesis and cellularization. Mol Biol Cell 2000; 11:3123–35.PubMedGoogle Scholar
  104. 104.
    Fares H, Peifer M, Pringle JR. Localization and possible functions of Drosophila septins. Mol Biol Cell 1995; 6:1843–59.PubMedGoogle Scholar
  105. 105.
    Afshar K, Stuart B, Wasserman SA. Functional analysis of the Drosophila diaphanous FH protein in early embryonic development. Development 2000; 127:1887–97.PubMedGoogle Scholar
  106. 106.
    Lecuit T. Polarized insertion of new membrane from a cytoplasmic reservoir during cleavage of the Drosophila embryo. J Cell Biol 2000; 150:849–60.PubMedCrossRefGoogle Scholar
  107. 107.
    Chardin P, McCormick F. Brefeldin A: The advantage of being uncompetitive. Cell 1999; 97:153–5.PubMedCrossRefGoogle Scholar
  108. 108.
    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.PubMedCrossRefGoogle Scholar
  109. 109.
    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.PubMedCrossRefGoogle Scholar
  110. 110.
    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.PubMedCrossRefGoogle Scholar
  111. 111.
    Nelson WJ. Cytoskeleton functions in membrane traffic in polarized epithelial cells. Semin Cell Biol 1991; 2:375–85.PubMedGoogle Scholar
  112. 112.
    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.PubMedCrossRefGoogle Scholar
  113. 113.
    Tanentzapf G, Tepass U. Interactions between the crumbs, lethal giant larvae and bazooka pathways in epithelial polarization. Nat Cell Biol 2003; 5:46–52.PubMedCrossRefGoogle Scholar
  114. 114.
    Bilder D, Schober M, Perrimon N. Integrated activity of PDZ protein complexes regulates epithelial polarity. Nat Cell Biol 2003; 5:53–8.PubMedCrossRefGoogle Scholar
  115. 115.
    Horne-Badovinac S, Bilder D. Mass transit: Epithelial morphogenesis in the Drosophila egg chamber. Dev Dyn 2005; 232:559–74.PubMedCrossRefGoogle Scholar
  116. 116.
    Nelson WJ. Adaptation of core mechanisms to generate cell polarity. Nature 2003; 422:766–74.PubMedCrossRefGoogle Scholar
  117. 117.
    Bilder D. Epithelial polarity and proliferation control: Links from the Drosophila neoplastic tumor suppressors. Genes Dev 2004; 18:1909–25.PubMedCrossRefGoogle Scholar
  118. 118.
    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.PubMedGoogle Scholar
  119. 119.
    Mostov KE, Verges M, Altschuler Y. Membrane traffic in polarized epithelial cells. Curr Opi Cell Biol 2000; 12:483–90.CrossRefGoogle Scholar
  120. 120.
    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.PubMedGoogle Scholar
  121. 121.
    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.PubMedCrossRefGoogle Scholar
  122. 122.
    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.PubMedCrossRefGoogle Scholar
  123. 123.
    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.PubMedCrossRefGoogle Scholar
  124. 124.
    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.PubMedCrossRefGoogle Scholar
  125. 125.
    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.PubMedCrossRefGoogle Scholar
  126. 126.
    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.PubMedCrossRefGoogle Scholar
  127. 127.
    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.PubMedCrossRefGoogle Scholar
  128. 128.
    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.PubMedCrossRefGoogle Scholar
  129. 129.
    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.PubMedCrossRefGoogle Scholar
  130. 130.
    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.PubMedCrossRefGoogle Scholar
  131. 131.
    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.PubMedCrossRefGoogle Scholar
  132. 132.
    Tepass U, Tanentzapf G, Ward R et al. Epithelial cell polarity and cell junctions in Drosophila. Annu Rev Genet 2001; 35:747–84.PubMedCrossRefGoogle Scholar
  133. 133.
    Tsukita S, Furuse M, Itoh M. Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol 2001; 2:285–93.PubMedCrossRefGoogle Scholar
  134. 134.
    Ebnet K, Suzuki A, Ohno S et al. Junctional adhesion molecules (JAMs): More molecules with dual functions? J Cell Sci 2004; 117:19–29.PubMedCrossRefGoogle Scholar
  135. 135.
    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.PubMedCrossRefGoogle Scholar
  136. 136.
    Van Itallie CM, Anderson JM. The molecular physiology of tight junction pores. Physiology 2004; 19:331–8.PubMedCrossRefGoogle Scholar
  137. 137.
    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.PubMedCrossRefGoogle Scholar
  138. 138.
    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.PubMedCrossRefGoogle Scholar
  139. 139.
    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.PubMedCrossRefGoogle Scholar
  140. 140.
    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.PubMedCrossRefGoogle Scholar
  141. 141.
    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.PubMedCrossRefGoogle Scholar
  142. 142.
    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.PubMedCrossRefGoogle Scholar
  143. 143.
    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.PubMedCrossRefGoogle Scholar
  144. 144.
    Snow PM, Bieber AJ, Goodman CS. Fasciclin III: A novel homophilic adhesion molecule in Drosophila. Cell 1989; 59:313–23.PubMedCrossRefGoogle Scholar
  145. 145.
    Knust, Bossinger. Composition and formation of intercellular junctions in epithelial cells. Science 2002; 298:1955–9.PubMedCrossRefGoogle Scholar
  146. 146.
    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.PubMedCrossRefGoogle Scholar
  147. 147.
    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.PubMedCrossRefGoogle Scholar
  148. 148.
    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.PubMedCrossRefGoogle Scholar
  149. 149.
    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.PubMedCrossRefGoogle Scholar
  150. 150.
    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.PubMedCrossRefGoogle Scholar
  151. 151.
    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.PubMedCrossRefGoogle Scholar
  152. 152.
    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.PubMedCrossRefGoogle Scholar
  153. 153.
    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.CrossRefGoogle Scholar
  154. 154.
    Zallen JA, Wieschaus E. Patterned gene expression directs bipolar planar polarity in Drosophila. Developmental Cell 2004; 6:343–55.PubMedCrossRefGoogle Scholar
  155. 155.
    Bertet C, Sulak L, Lecuit T. Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 2004; 429:667–71.PubMedCrossRefGoogle Scholar
  156. 156.
    Lubarsky B, Krasnow MA. Tube morphogenesis: Making and shaping biological tubes. Cell 2003; 112:19–28.PubMedCrossRefGoogle Scholar
  157. 157.
    Neumann M, Affolter M. Remodelling epithelial tubes through cell rearrangements: From cells to molecules. EMBO Rep 2006; 7:36–40.PubMedCrossRefGoogle Scholar
  158. 158.
    Hynes RO. Integrins: Versatility, modulation, and signaling in cell adhesion. Cell 1992; 69:11–25.PubMedCrossRefGoogle Scholar
  159. 159.
    Cohen LA, Guan JL. Mechanisms of focal adhesion kinase regulation. Curr Cancer Drug Targets 2005; 5:629–43.PubMedCrossRefGoogle Scholar
  160. 160.
    Caswell PT, Norman JC. Integrin trafficking and the control of cell Migration. Traffic 2006; 7:14–21.PubMedCrossRefGoogle Scholar
  161. 161.
    Le Borgne R, Bardin A, Schweisguth F. The roles of receptor and ligand endocytosis in regulating Notch signaling. Development 2005; 132:1751–62.PubMedCrossRefGoogle Scholar
  162. 162.
    Knoblich JA. Sara splits the signal. Science 2006; 314:1094–6.PubMedCrossRefGoogle Scholar
  163. 163.
    Somers WG, Chia W. Recycling polarity. Dev Cell 2005; 9:312–3.PubMedCrossRefGoogle Scholar
  164. 164.
    Logan CY, Nusse R. The wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 2004; 20:781–810.PubMedCrossRefGoogle Scholar
  165. 165.
    Ingham PW, McMahon AP. Hedgehog signaling in animal development: Paradigms and principles. Genes Dev 2001; 15:3059–87.PubMedCrossRefGoogle Scholar
  166. 166.
    Vincent JP, Dubois L. Morphogen transport along epithelia, an integrated trafficking problem. Dev Cell 2002; 3:615–23.PubMedCrossRefGoogle Scholar
  167. 167.
    Hausmann G, Banziger C, Basler K. Helping Wingless take flight: How WNT proteins are secreted. Nat Rev Mol Cell Biol 2007; 8:331–6.PubMedCrossRefGoogle Scholar
  168. 168.
    Guerrero I, Chiang C. A conserved mechanism of Hedgehog gradient formation by lipid modifications. Trend Cell Biol 2006; 17:1–5.CrossRefGoogle Scholar
  169. 169.
    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.PubMedCrossRefGoogle Scholar
  170. 170.
    Coudreuse D, Korswagen HC. The making of Wnt: New insights into Wnt maturation, sorting and secretion. Development 2007; 134:3–12.PubMedCrossRefGoogle Scholar
  171. 171.
    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.PubMedCrossRefGoogle Scholar
  172. 172.
    Hofmann K. A superfamily of membrane-bound O-acyltransferases with implications for wnt signaling. Trend Biochem Sci 2000; 25:111–2.PubMedCrossRefGoogle Scholar
  173. 173.
    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.PubMedCrossRefGoogle Scholar
  174. 174.
    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.PubMedGoogle Scholar
  175. 175.
    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.PubMedCrossRefGoogle Scholar
  176. 176.
    Amanai K, Jiang J. Distinct roles of Central missing and Dispatched in sending the Hedgehog signal. Development 2001; 128:5119–27.PubMedGoogle Scholar
  177. 177.
    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.PubMedCrossRefGoogle Scholar
  178. 178.
    Lee JD, Treisman JE. Sightless has homology to transmembrane acyltransferases and is required to generate active Hedgehog protein. Curr Biol 2001; 11:1147–52.PubMedCrossRefGoogle Scholar
  179. 179.
    Micchelli CA, The I, Selva E et al. Rasp, a putative transmembrane acyltransferase, is required for Hedgehog signaling. Development 2002; 129:843–51.PubMedGoogle Scholar
  180. 180.
    Panakova D, Sprong H, Marois E et al. Lipoprotein particles are required for Hedgehog and Wingless signalling. Nature 2005; 435:58–65.PubMedCrossRefGoogle Scholar
  181. 181.
    Eaton S. Release and trafficking of lipid-linked morphogens. Curr Opi Gen Dev 2006; 16:17–22.CrossRefGoogle Scholar
  182. 182.
    Bartscherer K, Pelte N, Ingelfinger D et al. Secretion of Wnt ligands requires Evi, a conserved transmembrane protein. Cell 2006; 125:523–33.PubMedCrossRefGoogle Scholar
  183. 183.
    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.PubMedCrossRefGoogle Scholar
  184. 184.
    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.PubMedCrossRefGoogle Scholar
  185. 185.
    Zeng X, Goetz JA, Suber LM et al. A freely diffusible form of Sonic hedgehog mediates long-range signalling. Nature 2001; 411:716–20.PubMedCrossRefGoogle Scholar
  186. 186.
    Coudreuse DY, Roel G, Betist MC et al. Wnt gradient formation requires retromer function in Wnt-producing cells. Science 2006; 312:921–4.PubMedCrossRefGoogle Scholar
  187. 187.
    Prasad BC, Clark SG. Wnt signaling establishes anteroposterior neuronal polarity and requires retromer in C. elegans. Development 2006; 133:1757–66.PubMedCrossRefGoogle Scholar
  188. 188.
    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.PubMedCrossRefGoogle Scholar
  189. 189.
    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.PubMedCrossRefGoogle Scholar
  190. 190.
    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.PubMedCrossRefGoogle Scholar
  191. 191.
    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.PubMedCrossRefGoogle Scholar
  192. 192.
    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.PubMedCrossRefGoogle Scholar
  193. 193.
    Eaton S. Retromer retrieves Wndess. Dev Cell 2008; 14:4–6.PubMedCrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2009

Authors and Affiliations

  1. 1.Cell Microscopy Centre Department of Cell Biology and Institute of BiomembraneUniversity Medical CenterUtrechtThe Netherlands

Personalised recommendations