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  • Original Paper
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Xmeis1, a protooncogene involved in specifying neural crest cell fate in Xenopus embryos

Abstract

Meis1 (Myeloid Ecotropic viral Integration Site 1) is a homeobox gene that was originally isolated as a common site of viral integration in myeloid tumors of the BXH-2 recombinant inbred mice strain. We previously isolated a Xenopus homolog of Meis1 (Xmeis1). Here we show that Xmeis1 may play a significant role in neural crest development. In developing Xenopus embryos, Xmeis1 displays a broad expression pattern, but strong expression is observed in tissue of neural cell fate, such as midbrain, hindbrain, the dorsal portion of the neural tube, and neural crest derived branchial arches. In animal cap explants, overexpression of Xmeis1b, an alternatively spliced form of Xmeis1, induces expression of neural crest marker genes in the absence of mesoderm. Moreover, Xmeis1b induces XGli-3 and XZic3, pre-pattern genes involved at the earliest stages of neural crest development, and like these two genes, can induce ectopic pigmented cell masses when overexpressed in developing embryos. Misexpression of Xmeis1b also induces ectopic expression of neural crest markers along the antero-posterior axis of the neural tube in developing Xenopus embryos. In contrast, Xmeis1a, another splice variant, is much less effective at inducing these effects. These data suggest that Xmeis1b is involved in neural crest cell fate specification during embryogenesis, and can functionally intersect with the Gli/Zic signal transduction pathway.

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References

  • Abu-Shaar M, Ryoo HD, Mann RS . 1999 Genes Dev. 13: 935–945

  • Berthelsen J, Zappanigna V, Mavillo F, Blasi F . 1998 EMBO J. 17: 1434–1445

  • Berthelsen J, Kilstrup-Nielsen C, Blasi F, Mavilio F, Zappavigna V . 1999 Genes Dev. 13: 946–953

  • Blatt C, Aberdam D, Schwartz R, Sachs L . 1988 EMBO J 7: 4283–4290

  • Bradley LC, Snape A, Bhatt S, Wilkinson DG . 1993 Mech. Dev. 40: 73–84

  • Brewster R, Lee J, Ruiz i Altaba A . 1998 Nature 393: 579–583

  • Burglin TR . 1997 Nucleic Acids Res. 25: 4173–4180

  • Casares F, Mann RS . 1998 Nature 392: 723–726

  • Chang CP, Shen WF, Rozenfeld S, Lawerence HJ, Largman C, Cleary ML . 1995 Genes Dev. 9: 663–674

  • Chang CP, Brocchieri L, Shen WF, Largman C, Cleary ML . 1996 Mol. Cell. Biol. 16: 1734–1745

  • Chang C, Jacobs Y, Nakamura T, Jenkins NA, Copeland NG, Cleary ML . 1997 Mol. Cell. Biol. 17: 5679–5687

  • Dahmane N, Lee J, Robins P, Heller P, Ruiz i Altaba A . 1997 Nature 389: 876–881

  • Ding Q, Motoyama J, Gasca S, Mo R, Sasaki H, Rossant J, Hui CC . 1998 Development 125: 2533–2543

  • Hardcastle Z, Papalopulu N . 2000 Development 127: 1303–1314

  • Harland RM . 1991 Methods Cell Biol. 36: 685–695

  • Hemmati-Brivanlou A, Melton DA . 1994 Cell 77: 273–281

  • Hopwood ND, Pluck A, Gurdon JB . 1989 Cell 59: 893–903

  • Jacobs Y, Schnabel CA, Cleary ML . 1999 Mol. Cell. Biol. 19: 5134–5142

  • Kamps MP, Murre C, Sun XH, Baltimore D . 1990 Cell 60: 547–555

  • Kawagoe H, Humphries RK, Blair A, Sutherland HJ, Hogge DE . 1999 Leukemia 13: 687–698

  • Kroon E, Krosl J, Thorsteinsdottir U, Baban S, Buchberg AM, Sauvageau G . 1998 EMBO J 17: 3714–3725

  • Kurant E, Pai C, Sharf R, Halachmi N, Henry Sun Y, Salzberg A . 1998 Development 125: 1037–1048

  • LaBonne C, Bronner-Fraser M . 1998 Development 125: 2867–2882

  • LaBonne C, Bronner-Fraser M . 1999 Ann. Rev. Cell Dev. Biol. 15: 81–112

  • Lawrence HJ, Rozenfeld S, Cruz C, Matsukuma K, Kwong A, Komuves L, Buchberg AM, Largman C . 1999 Leukemia 13: 1993–1999

  • Levine M, Hoey T . 1988 Cell 55: 537–540

  • Lu Q, Knoepfler PS, Scheele J, Wright DD, Kamps MP . 1995 Mol. Cell. Biol. 15: 3786–3795

  • Maeda R, Kobayashi A, Sekine R, Lin JJ, Kung H, Maeno M . 1997 Development 124: 2553–2560

  • Mancilla A, Mayor R . 1996 Dev. Biol. 177: 580–589

  • Marigo V, Johnson RL, Vortkamp A, Tabin CJ . 1996 Dev. Biol. 180: 273–283

  • Marine J-C, Bellefroid EJ, Pendeville H, Martial JA, Pieler T . 1997 Mech. Dev. 63: 211–225

  • Matise MP, Epstein DJ, Park HL, Platt KA, Joyner AL . 1998 Development 125: 2759–2770

  • Matise MP, Joyner AL . 1999 Oncogene 18: 7852–7859

  • Mayor R, Morgan R, Sargent MG . 1995 Development 121: 767–777

  • Mayor R, Young R, Vargas A . 1999 Curr. Topics Dev. Biol. 43: 85–113

  • McGinnis W, Krumlauf R . 1992 Cell 68: 283–302

  • McGrew LL, Lai CJ, Moon RT . 1995 Dev. Biol. 172: 337–342

  • McGrew LL, Hoppler S, Moon RT . 1997 Mech. Dev. 69: 105–114

  • Mercader N, Leonardo E, Azpiazu N, Serrano A, Morata G, Martinez C, Torres M . 1999 Nature 402: 425–429

  • Miyatani S, Winkles JA, Sargent TD, Dawid IB . 1986 J. Cell. Biol. 103: 1957–1965

  • Mizuseki K, Kishi M, Shiota K, Nakanishi S, Sasai Y . 1998 Neuron 21: 77–85

  • Moskow JJ, Bullrich F, Huebner K, Daar IO, Buchberg AM . 1995 Mol. Cell. Biol. 15: 5434–5443

  • Nakamura T, Largaespada DA, Shaughnessy Jr JD, Jenkins NA, Copeland NG . 1996 Nat. Genet. 12: 149–153

  • Nakata K, Nagai T, Aruga J, Mikoshiba K . 1997 Proc. Natl. Acad. Sci. USA 94: 11980–11985

  • Nakata K, Nagai T, Aruga J, Mikoshiba K . 1998 Mech. Dev. 75: 43–51

  • Nakata K, Koyabu Y, Aruga J, Mikoshiba K . 2000 Mech. Dev. 99: 83–91

  • Nieuwkoop PD, Faber J . 1967 Normal Table of Xenopus laevis Daudine:North-Holland, Amsterdam

    Google Scholar 

  • Neuteboom ST, Peltenberg LT, Van Dijk MA, Murre C . 1995 Proc. Natl. Acad. Sci. USA 92: 9166–9170

  • Nourse J, Mellentin JD, Galili N, Wilkinson J, Stanbridge E, Smith SD, Cleary ML . 1990 Cell 60: 535–545

  • Pai CY, Kuo TS, Jaw TJ, Kurant E, Chen CT, Bessarab DA, Salzberg A, Nenry Sun Y . 1998 Genes Dev. 12: 435–446

  • Papalopulu N, Clarke JD, Bradley L, Wilkinson D, Krumlauf R, Holder N . 1991 Development 113: 1145–1158

  • Perkins A, Kongsuwan K, Visvader J, Adams JM, Cory S . 1990 Proc. Natl. Acad. Sci. USA 87: 8398–8402

  • Phelan ML, Rambaldi I, Featherstone MS . 1995 Mol. Cell. Biol. 15: 3989–3997

  • Richter K, Grunz H, Dawid IB . 1988 Proc. Natl. Acad. Sci. USA 85: 8086–8090

  • Rieckhof GE, Casares F, Ryoo YD, Abu-Shaar M, Mann RS . 1997 Cell 91: 171–183

  • Ruiz i Altaba A . 1998 Development 125: 2203–2212

  • Ruiz i Altaba A . 1999a Development 126: 3205–3216

  • Ruiz i Altaba A . 1999b TIG 15: 418–425

  • Ryoo HD, Marty T, Casares F, Affolter M, Mann RS . 1999 Development 126: 5137–5145

  • Saint-Jeannet JP, He X, Varmus HE, Dawid IB . 1997 Proc. Natl. Acad. Sci. USA 94: 13713–13718

  • Salzberg A, D'Evelyn D, Schulze KL, Lee JK, Strumpf D, Tsai L, Bellen HJ . 1994 Neuron 13: 269–287

  • Salzberg A, Elias S, Nachaliel N, Bonstein L, Henig C, Frank D . 1999 Mech. Dev. 80: 3–13

  • Sasai Y, De Robertis EM . 1997 Dev. Biol. 182: 5–20

  • Sasaki H, Hui C, Nakafuku M, Kondoh H . 1997 Development 124: 1313–1322

  • Shanmugam K, Green NC, Rambaldi I, Saragovi HU, Featherstone MS . 1999 Mol. Cell. Biol. 19: 7577–7588

  • Shen WF, Montgomery JC, Rozenfeld S, Moskow JJ, Lawrence HJ, Buchberg AM, Largman C . 1997 Mol. Cell. Biol. 17: 6448–6458

  • Shen WF, Rozenfeld S, Kwong A, Komuves LG, Lawrence HJ, Largmen C . 1999 Mol. Cell. Biol. 19: 3051–3061

  • Steelman S, Moskow JJ, Muzynski K, North C, Druck T, Montgomery JC, Huebner K, Daar IO, Buchberg AM . 1997 Genome Res. 7: 142–156

  • Suzuki A, Nishimatsu S, Murakami K, Ueno N . 1993 Zool. Sci. 10: 175–178

  • Swift GH, Liu F, Rose SD, Bischof LJ, Steelman S, Buchberg AM, Wright CV, MacDonald RJ . 1998 Mol. Cell. Biol. 18: 5109–5120

  • Tada MA, O'Reilly J, Smith JC . 1997 Development 124: 2225–2234

  • Theil T, Frain M, Gilardi-Hebenstreit P, Flenniken A, Charnay P, Wilkinson DG . 1998 Development 125: 443–445

  • Thorsteinsdottir U, Sauvageau G, Hough MR, Dragowska W, Lansdorp PM, Lawrence HJ, Largman C, Humphries RK . 1997a Mol. Cell. Biol. 17: 495–505

  • Thorsteinsdottir U, Sauvageau G, Humphries RK . 1997b Hematol. Oncol. Clin. North. Am. 11: 1221–1237

  • Wallingford JB, Seufert DW, Virta VC, Vize PD . 1997 Curr. Biol. 7: 747–757

  • Wallingford JB . 1999 TIG 15: 385–388

  • Wicking C, Smyth I, Bale A . 1999 Oncogene 18: 7844–7851

  • Winning RS, Shea LJ, Marcus SJ, Sargent TD . 1991 Nucleic Acids Res. 19: 3709–3714

  • Wolda SL, Moody CJ, Moon RT . 1993 Dev. Biol. 155: 46–57

  • Yang S, Lockwood A, Hollett P, Ford R, Kao K . 1998 J. Biol. Chem. 273: 13746–13752

  • Zimmerman K, Shih J, Bars J, Collazo A, Anderson DJ . 1993 Development 119: 221–232

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Acknowledgements

We would like to thank Andy Golden, Lino Tessarollo, and Nancy Papalopulu for critical reading of the manuscript, and thank David Wilkinson (Krox-20), Igor Dawid (N-tubulin and eFGF), Thomas Sargent (XAP-2, XK81), Masazumi Tada (pSP64T-GR construct) for cDNAs. Activin A was obtained through NHPP, NIDDK and Dr Parlow. This project has been funded in whole or in part with funds from the National Cancer Institute, National Institute of Health, under contract No. NO1-CO-5600. R Maeda was supported by a JSPS Research Fellowship for Japanese Biomedical and Behavioral Researchers.

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Maeda, R., Mood, K., Jones, T. et al. Xmeis1, a protooncogene involved in specifying neural crest cell fate in Xenopus embryos. Oncogene 20, 1329–1342 (2001). https://doi.org/10.1038/sj.onc.1204250

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