Spatial Restriction of Bone Morphogenetic Protein Signaling in Mouse Gastrula through the mVam2-Dependent Endocytic Pathway

Developmental Cell

Volumn 22, Issue 6, 2012, Pages 1163-1175

  Aoyama, Minako ^a   Sun Wada, Ge Hong ^b   Yamamoto, Akitsugu ^c   Yamamoto, Masamichi ^a,d   Hamada, Hiroshi ^a,d   Wada, Yoh ^a  

^a OSAKA UNIVERSITY   (Japan)

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

^c NAGAHAMA INSTITUTE OF BIO SCIENCE AND TECHNOLOGY   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; CELL PROTEIN; EPIDERMAL GROWTH FACTOR; SMAD1 PROTEIN; SMAD5 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; VAM2 PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COMPARTMENTALIZATION; CELL MATURATION; CELL MUTANT; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; ENDOCYTOSIS; ENDOSOME; GASTRULA; GASTRULATION; GENE LOCUS; INTERNALIZATION; LYSOSOME; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN TRANSPORT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; BODY PATTERNING; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; BONE MORPHOGENETIC PROTEINS; ENDOCYTOSIS; ENDOSOMES; EPIDERMAL GROWTH FACTOR; GASTRULA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC LOCI; MICE; SIGNAL TRANSDUCTION; SMAD1 PROTEIN; SMAD5 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; VESICULAR TRANSPORT PROTEINS;

EID: 84862143028     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2012.05.009     Document Type: Article

References (64)

1. Aoyama M., Agari K., Sun-Wada G.H., Futai M., Wada Y. Simple and straightforward construction of a mouse gene targeting vector using in vitro transposition reactions. Nucleic Acids Res. 2005, 33:e52.
2. Bache K.G., Stuffers S., Malerød L., Slagsvold T., Raiborg C., Lechardeur D., Wälchli S., Lukacs G.L., Brech A., Stenmark H. The ESCRT-III subunit hVps24 is required for degradation but not silencing of the epidermal growth factor receptor. Mol. Biol. Cell 2006, 17:2513-2523.
3. Bachiller D., Klingensmith J., Kemp C., Belo J.A., Anderson R.M., May S.R., McMahon J.A., McMahon A.P., Harland R.M., Rossant J., De Robertis E.M. The organizer factors Chordin and Noggin are required for mouse forebrain development. Nature 2000, 403:658-661.
4. Bachiller D., Klingensmith J., Shneyder N., Tran U., Anderson R., Rossant J., De Robertis E.M. The role of chordin/Bmp signals in mammalian pharyngeal development and DiGeorge syndrome. Development 2003, 130:3567-3578.
5. Beppu H., Kawabata M., Hamamoto T., Chytil A., Minowa O., Noda T., Miyazono K. BMP type II receptor is required for gastrulation and early development of mouse embryos. Dev. Biol. 2000, 221:249-258.
6. Bernard O., Ripoche M.A., Bennett D. Distribution of maternal immunoglobulins in the mouse uterus and embryo in the days after implantation. J. Exp. Med. 1977, 145:58-75.
7. Bielinska M., Narita N., Wilson D.B. Distinct roles for visceral endoderm during embryonic mouse development. Int. J. Dev. Biol. 1999, 43:183-205.
8. Brennan J., Lu C.C., Norris D.P., Rodriguez T.A., Beddington R.S., Robertson E.J. Nodal signalling in the epiblast patterns the early mouse embryo. Nature 2001, 411:965-969.
9. Cabrera M., Ostrowicz C.W., Mari M., LaGrassa T.J., Reggiori F., Ungermann C. Vps41 phosphorylation and the Rab Ypt7 control the targeting of the HOPS complex to endosome-vacuole fusion sites. Mol. Biol. Cell 2009, 20:1937-1948.
10. Chazaud C., Rossant J. Disruption of early proximodistal patterning and AVE formation in Apc mutants. Development 2006, 133:3379-3387.
11. Chazaud C., Yamanaka Y., Pawson T., Rossant J. Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2-MAPK pathway. Dev. Cell 2006, 10:615-624.
12. +-ATPase-mediated acidification for Wnt signaling. Science 2010, 327:459-463.
13. Di Pietro S.M., Dell'Angelica E.C. The cell biology of Hermansky-Pudlak syndrome: recent advances. Traffic 2005, 6:525-533.
14. Felici A., Wurthner J.U., Parks W.T., Giam L.R., Reiss M., Karpova T.S., McNally J.G., Roberts A.B. TLP, a novel modulator of TGF-beta signaling, has opposite effects on Smad2- and Smad3-dependent signaling. EMBO J. 2003, 22:4465-4477.
15. 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.
16. Hamada H., Meno C., Watanabe D., Saijoh Y. Establishment of vertebrate left-right asymmetry. Nat. Rev. Genet. 2002, 3:103-113.
17. 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.
18. Heining E., Bhushan R., Paarmann P., Henis Y.I., Knaus P. Spatial segregation of BMP/Smad signaling affects osteoblast differentiation in C2C12 cells. PLoS One 2011, 6:e25163.
19. Kaufman M.H. The Atlas of Mouse Development 1992, Academic Press Limited, London.
20. Kelly O.G., Pinson K.I., Skarnes W.C. The Wnt co-receptors Lrp5 and Lrp6 are essential for gastrulation in mice. Development 2004, 131:2803-2815.
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. +-ATPase assembly in murine cardiomyocytes. Circ. Res. 2010, 107:30-34.
23. Lambson R.O. An electron microscopic visualization of transport across rat visceral yolk sac. Am. J. Anat. 1966, 118:21-52.
24. Lawson K.A., Dunn N.R., Roelen B.A., Zeinstra L.M., Davis A.M., Wright C.V., Korving J.P., Hogan B.L. Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev. 1999, 13:424-436.
25. Le Roy C., Wrana J.L. Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Nat. Rev. Mol. Cell Biol. 2005, 6:112-126.
26. Lin T.P., Labosky P.A., Grabel L.B., Kozak C.A., Pitman J.L., Kleeman J., MacLeod C.L. The Pem homeobox gene is X-linked and exclusively expressed in extraembryonic tissues during early murine development. Dev. Biol. 1994, 166:170-179.
27. Lin X., Duan X., Liang Y.Y., Su Y., Wrighton K.H., Long J., Hu M., Davis C.M., Wang J., Brunicardi F.C., et al. PPM1A functions as a Smad phosphatase to terminate TGFbeta signaling. Cell 2006, 125:915-928.
28. Logan C.Y., Nusse R. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 2004, 20:781-810.
29. Meno C., Gritsman K., Ohishi S., Ohfuji Y., Heckscher E., Mochida K., Shimono A., Kondoh H., Talbot W.S., Robertson E.J., et al. Mouse Lefty2 and zebrafish antivin are feedback inhibitors of nodal signaling during vertebrate gastrulation. Mol. Cell 1999, 4:287-298.
30. 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.
31. Messler S., Kropp S., Episkopou V., Felici A., Würthner J., Lemke R., Jerabek-Willemsen M., Willecke R., Scheu S., Pfeffer K., Wurthner J.U. The TGF-β signaling modulators TRAP1/TGFBRAP1 and VPS39/Vam6/TLP are essential for early embryonic development. Immunobiology 2011, 216:343-350.
32. 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.
33. Miyazono K., Maeda S., Imamura T. BMP receptor signaling: transcriptional targets, regulation of signals, and signaling cross-talk. Cytokine Growth Factor Rev. 2005, 16:251-263.
34. Morkel M., Huelsken J., Wakamiya M., Ding J., van de Wetering M., Clevers H., Taketo M.M., Behringer R.R., Shen M.M., Birchmeier W. Beta-catenin regulates Cripto- and Wnt3-dependent gene expression programs in mouse axis and mesoderm formation. Development 2003, 130:6283-6294.
35. Morsut L., Yan K.P., Enzo E., Aragona M., Soligo S.M., Wendling O., Mark M., Khetchoumian K., Bressan G., Chambon P., et al. Negative control of Smad activity by ectodermin/Tif1gamma patterns the mammalian embryo. Development 2010, 137:2571-2578.
36. Nakamura N., Hirata A., Ohsumi Y., Wada Y. Vam2/Vps41p and Vam6/Vps39p are components of a protein complex on the vacuolar membranes and involved in the vacuolar assembly in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 1997, 272:11344-11349.
37. Nakamura N., Yamamoto A., Wada Y., Futai M. Syntaxin 7 mediates endocytic trafficking to late endosomes. J. Biol. Chem. 2000, 275:6523-6529.
38. Odorizzi G., Cowles C.R., Emr S.D. The AP-3 complex: a coat of many colours. Trends Cell Biol. 1998, 8:282-288.
39. Oliver G., Mailhos A., Wehr R., Copeland N.G., Jenkins N.A., Gruss P. Six3, a murine homologue of the sine oculis gene, demarcates the most anterior border of the developing neural plate and is expressed during eye development. Development 1995, 121:4045-4055.
40. Ostrowicz C.W., Bröcker C., Ahnert F., Nordmann M., Lachmann J., Peplowska K., Perz A., Auffarth K., Engelbrecht-Vandré S., Ungermann C. Defined subunit arrangement and rab interactions are required for functionality of the HOPS tethering complex. Traffic 2010, 11:1334-1346.
41. Perea-Gomez A., Vella F.D., Shawlot W., Oulad-Abdelghani M., Chazaud C., Meno C., Pfister V., Chen L., Robertson E., Hamada H., et al. Nodal antagonists in the anterior visceral endoderm prevent the formation of multiple primitive streaks. Dev. Cell 2002, 3:745-756.
42. Price A., Wickner W., Ungermann C. Proteins needed for vesicle budding from the Golgi complex are also required for the docking step of homotypic vacuole fusion. J. Cell Biol. 2000, 148:1223-1229.
43. Radisky D.C., Snyder W.B., Emr S.D., Kaplan J. Characterization of VPS41, a gene required for vacuolar trafficking and high-affinity iron transport in yeast. Proc. Natl. Acad. Sci. USA 1997, 94:5662-5666.
44. Raymond C.K., Howald-Stevenson I., Vater C.A., Stevens T.H. Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants. Mol. Biol. Cell 1992, 3:1389-1402.
45. Saga Y., Hata N., Kobayashi S., Magnuson T., Seldin M.F., Taketo M.M. MesP1: a novel basic helix-loop-helix protein expressed in the nascent mesodermal cells during mouse gastrulation. Development 1996, 122:2769-2778.
46. 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.
47. Shi Y., Massagué J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 2003, 113:685-700.
48. 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.
49. Soares M.L., Haraguchi S., Torres-Padilla M.E., Kalmar T., Carpenter L., Bell G., Morrison A., Ring C.J., Clarke N.J., Glover D.M., Zernicka-Goetz M. Functional studies of signaling pathways in peri-implantation development of the mouse embryo by RNAi. BMC Dev. Biol. 2005, 5:28.
50. Solter D., Damjanov I., Skreb N. Ultrastructure of mouse egg-cylinder. Z. Anat. Entwicklungsgesch. 1970, 132:291-298.
51. 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.
52. Takaoka K., Yamamoto M., Shiratori H., Meno C., Rossant J., Saijoh Y., Hamada H. The mouse embryo autonomously acquires anterior-posterior polarity at implantation. Dev. Cell 2006, 10:451-459.
53. 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.
54. Thomas P., Beddington R. Anterior primitive endoderm may be responsible for patterning the anterior neural plate in the mouse embryo. Curr. Biol. 1996, 6:1487-1496.
55. Varlet I., Collignon J., Robertson E.J. nodal expression in the primitive endoderm is required for specification of the anterior axis during mouse gastrulation. Development 1997, 124:1033-1044.
56. Wada Y., Ohsumi Y., Anraku Y. Genes for directing vacuolar morphogenesis in Saccharomyces cerevisiae. I. Isolation and characterization of two classes of vam mutants. J. Biol. Chem. 1992, 267:18665-18670.
57. Wilkinson D.G., Bhatt S., Herrmann B.G. Expression pattern of the mouse T gene and its role in mesoderm formation. Nature 1990, 343:657-659.
58. Yamaguchi T.P., Dumont D.J., Conlon R.A., Breitman M.L., Rossant J. flk-1, an flt-related receptor tyrosine kinase is an early marker for endothelial cell precursors. Development 1993, 118:489-498.
59. Yamamoto M., Meno C., Sakai Y., Shiratori H., Mochida K., Ikawa Y., Saijoh Y., Hamada H. The transcription factor FoxH1 (FAST) mediates Nodal signaling during anterior-posterior patterning and node formation in the mouse. Genes Dev. 2001, 15:1242-1256.
60. 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.
61. Yamamoto M., Beppu H., Takaoka K., Meno C., Li E., Miyazono K., Hamada H. Antagonism between Smad1 and Smad2 signaling determines the site of distal visceral endoderm formation in the mouse embryo. J. Cell Biol. 2009, 184:323-334.
62. Yamanaka Y., Lanner F., Rossant J. FGF signal-dependent segregation of primitive endoderm and epiblast in the mouse blastocyst. Development 2010, 137:715-724.
63. Zhou X., Sasaki H., Lowe L., Hogan B.L., Kuehn M.R. Nodal is a novel TGF-beta-like gene expressed in the mouse node during gastrulation. Nature 1993, 361:543-547.
64. Zou H., Wieser R., Massagué J., Niswander L. Distinct roles of type I bone morphogenetic protein receptors in the formation and differentiation of cartilage. Genes Dev. 1997, 11:2191-2203.