Positive and negative regulation of developmental signaling by the endocytic pathway

Current Opinion in Genetics and Development

Volumn 23, Issue 4, 2013, Pages 391-398

  Wada, Yoh ^a   Sun Wada, Ge Hong ^b  

^a OSAKA UNIVERSITY   (Japan)

^b DOSHISHA WOMEN'S COLLEGE OF LIBERAL ARTS   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; BONE MORPHOGENETIC PROTEIN; CAVEOLIN; CELL SURFACE RECEPTOR; CHORDIN; CLATHRIN; DYNAMIN; EPIDERMAL GROWTH FACTOR; HOMOTYPIC FUSION AND VACUOLAR PROTEIN SORTING COMPLEX; LOW DENSITY LIPOPROTEIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; NOGGIN; RAB PROTEIN; RAB7 PROTEIN; SMAD ANCHOR FOR RECEPTOR ACTIVATION; SMAD1 PROTEIN; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD5 PROTEIN; TRANSFERRIN RECEPTOR; TRANSFORMING GROWTH FACTOR; UNCLASSIFIED DRUG; WNT PROTEIN;

CELL BUDDING; CELL EXPANSION; CELL MEMBRANE; CELL PROLIFERATION; CELL STRUCTURE; CELL SURFACE; CELLULAR DISTRIBUTION; EMBRYO DEVELOPMENT; ENDOCYTOSIS; ENDOSOME; INTERNALIZATION; LIGAND BINDING; LYSOSOME; MAMMAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; SPATIOTEMPORAL ANALYSIS; TRANSLATION REGULATION; WNT SIGNALING PATHWAY; ANIMAL; CYTOSOL; GENETICS; METABOLISM;

MAMMALIA;

ANIMALS; CYTOSOL; EMBRYONIC DEVELOPMENT; ENDOCYTOSIS; ENDOSOMES; LYSOSOMES; SIGNAL TRANSDUCTION;

EID: 84883445153     PISSN: 0959437X     EISSN: 18790380     Source Type: Journal    
DOI: 10.1016/j.gde.2013.04.002     Document Type: Review

References (46)

1. Wickner W. Membrane fusion: five lipids, four SNAREs, three chaperones, two nucleotides, and a Rab, all dancing in a ring on yeast vacuoles. Annu Rev Cell Dev Biol 2010, 26:115-136.
2. Arnold S.J., Robertson E.J. Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo. Nat Rev Mol Cell Biol 2009, 10:91-103.
3. Hartung A., Bitton-Worms K., Rechtman M.M., Wenzel V., Boergermann J.H., Hassel S., Henis Y.I., Knaus P. Different routes of bone morphogenic protein (BMP) receptor endocytosis influence BMP signaling. Mol Cell Biol 2006, 26:7791-7805.
4. Nohe A., Keating E., Underhill T.M., Knaus P., Petersen N.O. Dynamics and interaction of caveolin-1 isoforms with BMP-receptors. J Cell Sci 2005, 118:643-650.
5. Di Guglielmo G.M., Le Roy C., Goodfellow A.F., Wrana J.L. Distinct endocytic pathways regulate TGF-β receptor signalling and turnover. Nat Cell Biol 2003, 5:410-421.
6. Yamamoto H., Komekado H., Kikuchi A. Caveolin is necessary for Wnt-3a-dependent internalization of LRP6 and accumulation of β-catenin. Dev Cell 2006, 11:213-223.
7. Razani B., Engelman J.A., Wang X.B., Schubert W., Zhang X.L., Marks C.B., Macaluso F., Russell R.G., Li M., Pestell R.G., et al. Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J Biol Chem 2001, 276:38121-38138.
8. Schubert W., Sotgia F., Cohen A.W., Capozza F., Bonuccelli G., Bruno C., Minetti C., Bonilla E., Dimauro S., Lisanti M.P. Caveolin-1(-/-)- and caveolin-2(-/-)-deficient mice both display numerous skeletal muscle abnormalities, with tubular aggregate formation. Am J Pathol 2007, 170:316-333.
9. Penheiter S.G., Mitchell H., Garamszegi N., Edens M., Dore J.J., Leof E.B. Internalization-dependent and -independent requirements for transforming growth factor β receptor signaling via the Smad pathway. Mol Cell Biol 2002, 22:4750-4759.
10. Shi W., Chang C., Nie S., Xie S., Wan M., Cao X. Endofin acts as a Smad anchor for receptor activation in BMP signaling. J Cell Sci 2007, 120:1216-1224.
11. Vieira A.V., Lamaze C., Schmid S.L. Control of EGF receptor signaling by clathrin-mediated endocytosis. Science 1996, 274:2086-2089.
12. Seto E.S., Bellen H.J. Internalization is required for proper Wingless signaling in Drosophila melanogaster. J Cell Biol 2006, 173:95-106.
13. Blitzer J.T., Nusse R. A critical role for endocytosis in Wnt signaling. BMC Cell Biol 2006, 7:28.
14. Schwarz D.G., Griffin C.T., Schneider E.A., Yee D., Magnuson T. Genetic analysis of sorting nexins 1 and 2 reveals a redundant and essential function in mice. Mol Biol Cell 2002, 13:3588-3600.
15. Zheng B., Tang T., Tang N., Kudlicka K., Ohtsubo K., Ma P., Marth J.D., Farquhar M.G., Lehtonen E. Essential role of RGS-PX1/sorting nexin 13 in mouse development and regulation of endocytosis dynamics. Proc Natl Acad Sci U S A 2006, 103:16776-16781.
16. Radice G., Lee J.J., Costantini F. Hβ58, an insertional mutation affecting early postimplantation development of the mouse embryo. Development 1991, 111:801-811.
17. Komada M., Soriano P. Hrs, a FYVE finger protein localized to early endosomes, is implicated in vesicular traffic and required for ventral folding morphogenesis. Genes Dev 1999, 13:1475-1485.
18. Sugimoto M., Kondo M., Hirose M., Suzuki M., Mekada K., Abe T., Kiyonari H., Ogura A., Takagi N., Artzt K., et al. Molecular identification of t(w5): Vps52 promotes pluripotential cell differentiation through cell-cell interactions. Cell Rep 2012, 2:1363-1374.
19. Sun-Wada G.H., Murata Y., Yamamoto A., Kanazawa H., Wada Y., Futai M. Acidic endomembrane organelles are required for mouse postimplantation development. Dev Biol 2000, 228:315-325.
20. Jullien J., Gurdon J. Morphogen gradient interpretation by a regulated trafficking step during ligand-receptor transduction. Genes Dev 2005, 19:2682-2694.
21. Kim S., Wairkar Y.P., Daniels R.W., DiAntonio A. The novel endosomal membrane protein Ema interacts with the class C Vps-HOPS complex to promote endosomal maturation. J Cell Biol 2010, 188:717-734.
22. Shim J.H., Xiao C., Hayden M.S., Lee K.Y., Trombetta E.S., Pypaert M., Nara A., Yoshimori T., Wilm B., Erdjument-Bromage H., et al. CHMP5 is essential for late endosome function and down-regulation of receptor signaling during mouse embryogenesis. J Cell Biol 2006, 172:1045-1056.
23. Taelman V.F., Dobrowolski R., Plouhinec J.L., Fuentealba L.C., Vorwald P.P., Gumper I., Sabatini D.D., De Robertis E.M. Wnt signaling requires sequestration of glycogen synthase kinase 3 inside multivesicular endosomes. Cell 2010, 143:1136-1148.
24. Mesnard D., Guzman-Ayala M., Constam D.B. Nodal specifies embryonic visceral endoderm and sustains pluripotent cells in the epiblast before overt axial patterning. Development 2006, 133:2497-2505.
25. Yamamoto M., Saijoh Y., Perea-Gomez A., Shawlot W., Behringer R.R., Ang S.L., Hamada H., Meno C. Nodal antagonists regulate formation of the anteroposterior axis of the mouse embryo. Nature 2004, 428:387-392.
26. Takaoka K., Yamamoto M., Hamada H. Origin of body axes in the mouse embryo. Curr Opin Genet Dev 2007, 17:344-350.
27. Takaoka K., Yamamoto M., Hamada H. Origin and role of distal visceral endoderm, a group of cells that determines anterior-posterior polarity of the mouse embryo. Nat Cell Biol 2011, 13:743-752.
28. Yamashita M., Ying S.X., Zhang G.M., Li C., Cheng S.Y., Deng C.X., Zhang Y.E. Ubiquitin ligase Smurf1 controls osteoblast activity and bone homeostasis by targeting MEKK2 for degradation. Cell 2005, 121:101-113.
29. Bengtsson L., Schwappacher R., Roth M., Boergermann J.H., Hassel S., Knaus P. PP2A regulates BMP signalling by interacting with BMP receptor complexes and by dephosphorylating both the C-terminus and the linker region of Smad1. J Cell Sci 2009, 122:1248-1257.
30. Aoyama M., Sun-Wada G.-H., Yamamoto A., Yamamoto M., Hamada H., Wada Y. Spatial restriction of bone morphogenetic protein signaling in mouse gastrula through the mVam2-dependent endocytic pathway. Dev Cell 2012, 22:1163-1175.
31. Mishina Y., Suzuki A., Ueno N., Behringer R.R. Bmpr encodes a type I bone morphogenetic protein receptor that is essential for gastrulation during mouse embryogenesis. Genes Dev 1995, 9:3027-3037.
32. Gu Z., Reynolds E.M., Song J., Lei H., Feijen A., Yu L., He W., MacLaughlin D.T., Van Den Eijnden-van Raaij J., Donahoe P.K., et al. The type I serine/threonine kinase receptor ActRIA (ALK2) is required for gastrulation of the mouse embryo. Development 1999, 126:2551-2561.
33. Fukuda T., Scott G., Komatsu Y., Araya R., Kawano M., Ray M.K., Yamada M., Mishina Y. Generation of a mouse with conditionally activated signaling through the BMP receptor, ALK2. Genesis 2006, 44:159-167.
34. Enders A.C., Given R.L., Schlafke S. Differentiation and migration of endoderm in the rat and mouse at implantation. Anat Rec 1978, 190:65-77.
35. Kawamura N., Sun-Wada G.-H., Aoyama M., Harada A., Takasuga S., Sasaki T., Wada Y. Delivery of endosomes to lysosomes via microautophagy in the visceral endoderm of mouse embryos. Nat Commun 2012, 3:1071.
36. Rink J., Ghigo E., Kalaidzidis Y., Zerial M. Rab conversion as a mechanism of progression from early to late endosomes. Cell 2005, 122:735-749.
37. Takasuga S., Horie Y., Sasaki J., Sun-Wada G.H., Kawamura N., Iizuka R., Mizuno K., Eguchi S., Kofuji S., Kimura H., et al. Critical roles of type III phosphatidylinositol phosphate kinase in murine embryonic visceral endoderm and adult intestine. Proc Natl Acad Sci U S A 2013, 110:1726-1731.
38. Al-Nassar N.A., Bellairs R. An electron-microscopical analysis of embryonic chick tissues explanted in culture. Cell Tissue Res 1982, 225:415-426.
39. Gonnella P.A., Siminoski K., Murphy R.A., Neutra M.R. Transepithelial transport of epidermal growth factor by absorptive cells of suckling rat ileum. J Clin Invest 1987, 80:22-32.
40. Stern C.D., Downs K.M. The hypoblast (visceral endoderm): an evo-devo perspective. Development 2012, 139:1059-1069.
41. Zoncu R., Bar-Peled L., Efeyan A., Wang S., Sancak Y., Sabatini D.M. mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires the vacuolar H-ATPase. Science 2011, 334:678-683.
42. Sancak Y., Bar-Peled L., Zoncu R., Markhard A.L., Nada S., Sabatini D.M. Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 2010, 141:290-303.
43. Yamanaka Y., Lanner F., Rossant J. FGF signal-dependent segregation of primitive endoderm and epiblast in the mouse blastocyst. Development 2010, 137:715-724.
44. Murakami M., Ichisaka T., Maeda M., Oshiro N., Hara K., Edenhofer F., Kiyama H., Yonezawa K., Yamanaka S. mTOR is essential for growth and proliferation in early mouse embryos and embryonic stem cells. Mol Cell Biol 2004, 24:6710-6718.
45. Gangloff Y.G., Mueller M., Dann S.G., Svoboda P., Sticker M., Spetz J.F., Um S.H., Brown E.J., Cereghini S., Thomas G., et al. Disruption of the mouse mTOR gene leads to early postimplantation lethality and prohibits embryonic stem cell development. Mol Cell Biol 2004, 24:9508-9516.
46. Nada S., Hondo A., Kasai A., Koike M., Saito K., Uchiyama Y., Okada M. The novel lipid raft adaptor p18 controls endosome dynamics by anchoring the MEK-ERK pathway to late endosomes. EMBO J 2009, 28:477-489.