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.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 50 print issues and online access
$259.00 per year
only $5.18 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
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
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
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.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
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
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/sj.onc.1204250