Hepatocyte growth factor–regulated tyrosine kinase substrate ( Hgs ) is involved in BMP signaling through phosphorylation of smads and TAK1 in early mouse embryo
dc.contributor.author | Miura, Shigeto | en_US |
dc.contributor.author | Mishina, Yuji | en_US |
dc.date.accessioned | 2011-11-10T15:35:51Z | |
dc.date.available | 2013-01-02T16:32:25Z | en_US |
dc.date.issued | 2011-11 | en_US |
dc.identifier.citation | Miura, Shigeto; Mishina, Yuji (2011). "Hepatocyte growth factor–regulated tyrosine kinase substrate ( Hgs ) is involved in BMP signaling through phosphorylation of smads and TAK1 in early mouse embryo." Developmental Dynamics 240(11): 2474-2481. <http://hdl.handle.net/2027.42/87001> | en_US |
dc.identifier.issn | 1058-8388 | en_US |
dc.identifier.issn | 1097-0177 | en_US |
dc.identifier.uri | https://hdl.handle.net/2027.42/87001 | |
dc.description.abstract | Hepatocyte growth factor–regulated tyrosine kinase substrate that is encoded by Hgs promotes degradation of ubiquitinated signaling molecule in the early endosome. We previously reported that a targeted mutation in Hgs results in embryonic lethality soon after gastrulation in the mouse. Here, we report that downstream target genes for BMP signaling were highly down‐regulated in the Hgs mutant embryos. We also showed that Hgs is required for phosphorylation of SMAD1/5/8 and TAK1/p38 to transduce BMP signaling. Furthermore, we found that HGS functions to localize TAK1 in early endosome for its activation. These results suggest that HGS is critical to localize TAK1 to early endosome for transducing BMP signaling for proper development. Our data revealed a new mechanism to modify BMP signaling by Hgs during early mouse development. Developmental Dynamics 240:2474–2481, 2011. © 2011 Wiley‐Liss, Inc. | en_US |
dc.publisher | Wiley‐Liss, Inc. | en_US |
dc.subject.other | Gastrulation | en_US |
dc.subject.other | Signal Transduction | en_US |
dc.subject.other | Endosome | en_US |
dc.title | Hepatocyte growth factor–regulated tyrosine kinase substrate ( Hgs ) is involved in BMP signaling through phosphorylation of smads and TAK1 in early mouse embryo | en_US |
dc.type | Article | en_US |
dc.rights.robots | IndexNoFollow | en_US |
dc.subject.hlbsecondlevel | Pediatrics | en_US |
dc.subject.hlbtoplevel | Health Sciences | en_US |
dc.description.peerreviewed | Peer Reviewed | en_US |
dc.contributor.affiliationum | Department of Biologic and Materials Sciences, School of Dentistry, University of Michigan, Ann Arbor, Michigan | en_US |
dc.contributor.affiliationum | Department of Biologic and Materials Sciences, School of Dentistry, University of Michigan, Ann Arbor, MI 48109‐1078 | en_US |
dc.contributor.affiliationother | Laboratory of Reproductive and Developmental Toxicology, National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina | en_US |
dc.identifier.pmid | 21953618 | en_US |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/87001/1/22750_ftp.pdf | |
dc.identifier.doi | 10.1002/dvdy.22750 | en_US |
dc.identifier.source | Developmental Dynamics | en_US |
dc.identifier.citedreference | Adhikari A, Xu M, Chen ZJ. 2007. Ubiquitin‐mediated activation of TAK1 and IKK. Oncogene 26: 3214 – 3226. | en_US |
dc.identifier.citedreference | Belo JA, Bouwmeester T, Leyns L, Kertesz N, Gallo M, Follettie M, De Robertis EM. 1997. Cerberus‐like is a secreted factor with neutralizing activity expressed in the anterior primitive endoderm of the mouse gastrula. Mech Dev 68: 45 – 57. | en_US |
dc.identifier.citedreference | Ben‐Haim N, Lu C, Guzman‐Ayala M, Pescatore L, Mesnard D, Bischofberger M, Naef F, Robertson EJ, Constam DB. 2006. The nodal precursor acting via activin receptors induces mesoderm by maintaining a source of its convertases and BMP4. Dev Cell 11: 313 – 323. | en_US |
dc.identifier.citedreference | Candia AF, Hu J, Crosby J, Lalley PA, Noden D, Nadeau JH, Wright CV. 1992. Mox‐1 and Mox‐2 define a novel homeobox gene subfamily and are differentially expressed during early mesodermal patterning in mouse embryos. Development 116: 1123 – 1136. | en_US |
dc.identifier.citedreference | Catron KM, Wang H, Hu G, Shen MM, Abate‐Shen C. 1996. Comparison of MSX‐1 and MSX‐2 suggests a molecular basis for functional redundancy. Mech Dev 55: 185 – 199. | en_US |
dc.identifier.citedreference | Chen X, Zankl A, Niroomand F, Liu Z, Katus HA, Jahn L, Tiefenbacher C. 2006. Upregulation of ID protein by growth and differentiation factor 5 (GDF5) through a smad‐dependent and MAPK‐independent pathway in HUVSMC. J Mol Cell Cardiol 41: 26 – 33. | en_US |
dc.identifier.citedreference | Chu GC, Dunn NR, Anderson DC, Oxburgh L, Robertson EJ. 2004. Differential requirements for Smad4 in TGFbeta‐dependent patterning of the early mouse embryo. Development 131: 3501 – 3512. | en_US |
dc.identifier.citedreference | Conlon FL, Lyons KM, Takaesu N, Barth KS, Kispert A, Herrmann B, Robertson EJ. 1994. A primary requirement for nodal in the formation and maintenance of the primitive streak in the mouse. Development 120: 1919 – 1928. | en_US |
dc.identifier.citedreference | Davis S, Miura S, Hill C, Mishina Y, Klingensmith J. 2004. BMP receptor IA is required in the mammalian embryo for endodermal morphogenesis and ectodermal patterning. Dev Biol 270: 47 – 63. | en_US |
dc.identifier.citedreference | Di‐Gregorio A, Sancho M, Stuckey DW, Crompton LA, Godwin J, Mishina Y, Rodriguez TA. 2007. BMP signalling inhibits premature neural differentiation in the mouse embryo. Development 134: 3359 – 3369. | en_US |
dc.identifier.citedreference | Du Y, Yip H. 2010. Effects of bone morphogenetic protein 2 on Id expression and neuroblastoma cell differentiation. Differentiation 79: 84 – 92. | en_US |
dc.identifier.citedreference | Ellmeier W, Weith A. 1995. Expression of the helix‐loop‐helix gene Id3 during murine embryonic development. Dev Dyn 203: 163 – 173. | en_US |
dc.identifier.citedreference | Gorvel JP, Chavrier P, Zerial M, Gruenberg J. 1991. rab5 controls early endosome fusion in vitro. Cell 64: 915 – 925. | en_US |
dc.identifier.citedreference | Gu Z, Nomura M, Simpson BB, Lei H, Feijen A, van den Eijnden‐van Raaij J, Donahoe PK, Li E. 1998. The type I activin receptor ActRIB is required for egg cylinder organization and gastrulation in the mouse. Genes Dev 12: 844 – 857. | en_US |
dc.identifier.citedreference | Itoh F, Divecha N, Brocks L, Oomen L, Janssen H, Calafat J, Itoh S, Dijke Pt P. 2002. The FYVE domain in Smad anchor for receptor activation (SARA) is sufficient for localization of SARA in early endosomes and regulates TGF‐beta/Smad signalling. Genes Cells 7: 321 – 331. | en_US |
dc.identifier.citedreference | Jadrich JL, O'Connor MB, Coucouvanis E. 2006. The TGF beta activated kinase TAK1 regulates vascular development in vivo. Development 133: 1529 – 1541. | en_US |
dc.identifier.citedreference | Jen Y, Manova K, Benezra R. 1996. Expression patterns of Id1, Id2, and Id3 are highly related but distinct from that of Id4 during mouse embryogenesis. Dev Dyn 207: 235 – 252. | en_US |
dc.identifier.citedreference | Kishigami S, Mishina Y. 2005. BMP signaling and early embryonic patterning. Cytokine Growth Factor Rev 16: 265 – 278. | en_US |
dc.identifier.citedreference | Kishigami S, Yoshikawa S, Castranio T, Okazaki K, Furuta Y, Mishina Y. 2004. BMP signaling through ACVRI is required for left‐right patterning in the early mouse embryo. Dev Biol 276: 185 – 193. | en_US |
dc.identifier.citedreference | Komada M, Soriano P. 1999. Hrs, a FYVE finger protein localized to early endosomes, is implicated in vesicular traffic and required for ventral folding morphogenesis. Genes Dev 13: 1475 – 1485. | en_US |
dc.identifier.citedreference | Komada M, Masaki R, Yamamoto A, Kitamura N. 1997. Hrs, a tyrosine kinase substrate with a conserved double zinc finger domain, is localized to the cytoplasmic surface of early endosomes. J Biol Chem 272: 20538 – 20544. | en_US |
dc.identifier.citedreference | Liu P, Wakamiya M, Shea MJ, Albrecht U, Behringer RR, Bradley A. 1999. Requirement for Wnt3 in vertebrate axis formation. Nat Genet 22: 361 – 365. | en_US |
dc.identifier.citedreference | Lloyd TE, Atkinson R, Wu MN, Zhou Y, Pennetta G, Bellen HJ. 2002. Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell 108: 261 – 269. | en_US |
dc.identifier.citedreference | Mahlapuu M, Ormestad M, Enerback S, Carlsson P. 2001. The forkhead transcription factor Foxf1 is required for differentiation of extra‐embryonic and lateral plate mesoderm. Development 128: 155 – 166. | en_US |
dc.identifier.citedreference | Mandal CC, Ghosh Choudhury G, Ghosh‐Choudhury N. 2009. Phosphatidylinositol 3 kinase/Akt signal relay cooperates with smad in bone morphogenetic protein‐2‐induced colony stimulating factor‐1 (CSF‐1) expression and osteoclast differentiation. Endocrinology 150: 4989 – 4998. | en_US |
dc.identifier.citedreference | Mishina Y, Suzuki A, Ueno N, Behringer RR. 1995. Bmpr encodes a type I bone morphogenetic protein receptor that is essential for gastrulation during mouse embryogenesis. Genes Dev 9: 3027 – 3037. | en_US |
dc.identifier.citedreference | Mishina Y. 2003. Function of bone morphogenetic protein signaling during mouse development. Front Biosci 8: d855 – 869. | en_US |
dc.identifier.citedreference | Miura S, Takeshita T, Asao H, Kimura Y, Murata K, Sasaki Y, Hanai JI, Beppu H, Tsukazaki T, Wrana JL, Miyazono K, Sugamura K. 2000. Hgs (Hrs), a FYVE domain protein, is involved in Smad signaling through cooperation with SARA. Mol Cell Biol 20: 9346 – 9355. | en_US |
dc.identifier.citedreference | Miura S, Davis S, Klingensmith J, Mishina Y. 2006. BMP signaling in the epiblast is required for proper recruitment of the prospective paraxial mesoderm and development of the somites. Development 133: 3767 – 3775. | en_US |
dc.identifier.citedreference | Miura S, Singh AP, Mishina Y. 2010. Bmpr1a is required for proper migration of the AVE through regulation of Dkk1 expression in the pre‐streak mouse embryo. Dev Biol 341: 246 – 254. | en_US |
dc.identifier.citedreference | Miyazono K, Miyazawa K. 2002. Id: a target of BMP signaling. Sci STKE 2002: pe40. | en_US |
dc.identifier.citedreference | Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe‐Nebenius D, Chambers I, Scholer H, Smith A. 1998. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95: 379 – 391. | en_US |
dc.identifier.citedreference | Ninomiya‐Tsuji J, Kishimoto K, Hiyama A, Inoue J, Cao Z, Matsumoto K. 1999. The kinase TAK1 can activate the NIK‐I kappaB as well as the MAP kinase cascade in the IL‐1 signalling pathway. Nature 398: 252 – 256. | en_US |
dc.identifier.citedreference | Park C, Afrikanova I, Chung YS, Zhang WJ, Arentson E, Fong Gh G, Rosendahl A, Choi K. 2004. A hierarchical order of factors in the generation of FLK1‐ and SCL‐expressing hematopoietic and endothelial progenitors from embryonic stem cells. Development 131: 2749 – 2762. | en_US |
dc.identifier.citedreference | Raiborg C, Bremnes B, Mehlum A, Gillooly DJ, D'Arrigo A, Stang E, Stenmark H. 2001. FYVE and coiled‐coil domains determine the specific localisation of Hrs to early endosomes. J Cell Sci 114: 2255 – 2263. | en_US |
dc.identifier.citedreference | Russ AP, Wattler S, Colledge WH, Aparicio SA, Carlton MB, Pearce JJ, Barton SC, Surani MA, Ryan K, Nehls MC, Wilson V, Evans MJ. 2000. Eomesodermin is required for mouse trophoblast development and mesoderm formation. Nature 404: 95 – 99. | en_US |
dc.identifier.citedreference | Sasaki Y, Sugamura K. 2001. Involvement of Hgs/Hrs in signaling for cytokine‐mediated c‐fos induction through interaction with TAK1 and Pak1. J Biol Chem 276: 29943 – 29952. | en_US |
dc.identifier.citedreference | Shibuya H, Iwata H, Masuyama N, Gotoh Y, Yamaguchi K, Irie K, Matsumoto K, Nishida E, Ueno N. 1998. Role of TAK1 and TAB1 in BMP signaling in early Xenopus development. EMBO J 17: 1019 – 1028. | en_US |
dc.identifier.citedreference | Spiro DJ, Boll W, Kirchhausen T, Wessling‐Resnick M. 1996. Wortmannin alters the transferrin receptor endocytic pathway in vivo and in vitro. Mol Biol Cell 7: 355 – 367. | en_US |
dc.identifier.citedreference | Toyoshima M, Tanaka N, Aoki J, Tanaka Y, Murata K, Kyuuma M, Kobayashi H, Ishii N, Yaegashi N, Sugamura K. 2007. Inhibition of tumor growth and metastasis by depletion of vesicular sorting protein Hrs: its regulatory role on E‐cadherin and beta‐catenin. Cancer Res 67: 5162 – 5171. | en_US |
dc.identifier.citedreference | Winnier G, Blessing M, Labosky PA, Hogan BL. 1995. Bone morphogenetic protein‐4 is required for mesoderm formation and patterning in the mouse. Genes Dev 9: 2105 – 2116. | en_US |
dc.identifier.citedreference | Yamaguchi K, Nagai S, Ninomiya‐Tsuji J, Nishita M, Tamai K, Irie K, Ueno N, Nishida E, Shibuya H, Matsumoto K. 1999. XIAP, a cellular member of the inhibitor of apoptosis protein family, links the receptors to TAB1‐TAK1 in the BMP signaling pathway. EMBO J 18: 179 – 187. | en_US |
dc.identifier.citedreference | Yamamoto M, Beppu H, Takaoka K, Meno C, Li E, Miyazono K, Hamada H. 2009. Antagonism between Smad1 and Smad2 signaling determines the site of distal visceral endoderm formation in the mouse embryo. J Cell Biol 184: 323 – 334. | en_US |
dc.identifier.citedreference | Yang YP, Klingensmith J. 2006. Roles of organizer factors and BMP antagonism in mammalian forebrain establishment. Dev Biol 296: 458 – 475. | en_US |
dc.identifier.citedreference | Yao J, Kim TW, Qin J, Jiang Z, Qian Y, Xiao H, Lu Y, Qian W, Gulen MF, Sizemore N, DiDonato J, Sato S, Akira S, Su B, Li X. 2007. Interleukin‐1 (IL‐1)‐induced TAK1‐dependent Versus MEKK3‐dependent NFkappaB activation pathways bifurcate at IL‐1 receptor‐associated kinase modification. J Biol Chem 282: 6075 – 6089. | en_US |
dc.identifier.citedreference | Ying QL, Nichols J, Chambers I, Smith A. 2003. BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self‐renewal in collaboration with STAT3. Cell 115: 281 – 292. | en_US |
dc.identifier.citedreference | Yu PB, Hong CC, Sachidanandan C, Babitt JL, Deng DY, Hoyng SA, Lin HY, Bloch KD, Peterson RT. 2008. Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat Chem Biol 4: 33 – 41. | en_US |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
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