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

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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

G Oliver, A Mailhos, R Wehr, NG Copeland, NA Jenkins and P Gruss
Department of Molecular Cell Biology, Max Planck Institute of Biophysical Chemistry, Gottingen, Germany.

The Drosophila sine oculis homeobox-containing gene is known to play an essential role in controlling the initial events of pattern formation in the eye disc and is also required for the development of other parts of the fly visual system including the optic lobes. In this paper, we report the isolation of a sequence-related gene referred to as Six3. Based on its amino acid sequence, this gene can be included in the new Six/sine oculis subclass of homeobox genes. Early on, Six3 expression is restricted to the anterior neural plate including areas that later will give rise to ectodermal and neural derivatives. Later, once the longitudinal axis of the brain bends, Six3 mRNA is also found in structures derived from the anterior neural plate: ectoderm of nasal cavity, olfactory placode and Rathke's pouch, and also the ventral forebrain including the region of the optic recess, hypothalamus and optic vesicles. Based on this expression pattern, we conclude that Six3 is one of the most anterior homeobox gene reported to date. The high sequence similarity of Six3 with the Drosophila sine oculis, and its expression during eye development, suggests that this gene is the likely murine homologue. This finding supports the idea that mammals and insects share control genes such as eyeless/Pax6 (Halder, G., Callaerts, P. and Gehring, W. J. (1995) Science 267, 1788-1792), and also possibly other members of the regulatory cascade required for eye morphogenesis. In Small eye (Pax6) mouse mutants Six3 expression is not affected. Finally, based on the chromosomal localization and the expression pattern of the mouse Six3 gene, the human Six3 cognate could be a good candidate to be at least one of the genes affected in patients with holoprosencephaly type 2 due to an interstitial deletion of 2p21-p22. This region shares a homology with the distal region of mouse chromosome 17 where Six3 has been mapped.
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AJNR Am. J. Neuroradiol., June 1, 1999; 20(6): 1154 - 1157.
[Abstract] [Full Text]

S. Nishina, S. Kohsaka, Y. Yamaguchi, H. Handa, A. Kawakami, H. Fujisawa, and N. Azuma
PAX6 expression in the developing human eye
Br J Ophthalmol, June 1, 1999; 83(6): 723 - 727.
[Abstract] [Full Text]

J. I. Kim, T. Li, I.-C. Ho, M. J. Grusby, and L. H. Glimcher
Requirement for the c-Maf transcription factor in crystallin gene regulation and lens development
PNAS, March 30, 1999; 96(7): 3781 - 3785.
[Abstract] [Full Text] [PDF]

F. Loosli, S. Winkler, and J. Wittbrodt
Six3 overexpression initiates the formation of ectopic retina
Genes & Dev., March 15, 1999; 13(6): 649 - 654.
[Abstract] [Full Text]

B. Hauck, W. J. Gehring, and U. Walldorf
Functional analysis of an eye specific enhancer of the eyeless gene in Drosophila
PNAS, January 19, 1999; 96(2): 564 - 569.
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K. Kenyon, S. Moody, and M Jamrich
A novel fork head gene mediates early steps during Xenopus lens formation
Development, January 11, 1999; 126(22): 5107 - 5116.
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R. Chow, C. Altmann, R. Lang, and A Hemmati-Brivanlou
Pax6 induces ectopic eyes in a vertebrate
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M Rhinn, A Dierich, M Le Meur, and S Ang
Cell autonomous and non-cell autonomous functions of Otx2 in patterning the rostral brain
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T Theil, G Alvarez-Bolado, A Walter, and U Ruther
Gli3 is required for Emx gene expression during dorsal telencephalon development
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M Andreazzoli, G Gestri, D Angeloni, E Menna, and G Barsacchi
Role of Xrx1 in Xenopus eye and anterior brain development
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T Niimi, M Seimiya, U Kloter, S Flister, and W. Gehring
Direct regulatory interaction of the eyeless protein with an eye-specific enhancer in the sine oculis gene during eye induction in Drosophila
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K Hentges, K Thompson, and A Peterson
The flat-top gene is required for the expansion and regionalization of the telencephalic primordium
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R Chen, G Halder, Z Zhang, and G Mardon
Signaling by the TGF-beta homolog decapentaplegic functions reiteratively within the network of genes controlling retinal cell fate determination in Drosophila
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Y. Furuta and B. L.M. Hogan
BMP4 is essential for lens induction in the mouse embryo
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[Abstract] [Full Text]

F. Spitz, J. Demignon, A. Porteu, A. Kahn, J.-P. Concordet, D. Daegelen, and P. Maire
Expression of myogenin during embryogenesis is controlled by Six/sine oculis homeoproteins through a conserved MEF3 binding site
PNAS, November 24, 1998; 95(24): 14220 - 14225.
[Abstract] [Full Text] [PDF]

L. Yang, H. Zhang, G. Hu, H. Wang, C. Abate-Shen, and M. M. Shen
An Early Phase of Embryonic Dlx5 Expression Defines the Rostral Boundary of the Neural Plate
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M. K. Duncan, J. I. Haynes II, A. Cvekl, and J. Piatigorsky
Dual Roles for Pax-6: a Transcriptional Repressor of Lens Fiber Cell-Specific beta -Crystallin Genes
Mol. Cell. Biol., September 1, 1998; 18(9): 5579 - 5586.
[Abstract] [Full Text]

J. Toy, J.-M. Yang, G. S. Leppert, and O. H. Sundin
The Optx2 homeobox gene is expressed in early precursors of the eye and activates retina-specific genes
PNAS, September 1, 1998; 95(18): 10643 - 10648.
[Abstract] [Full Text] [PDF]

M. Treier, A. S. Gleiberman, S. M. O'Connell, D. P. Szeto, J. A. McMahon, A. P. McMahon, and M. G. Rosenfeld
Multistep signaling requirements for pituitary organogenesis in�vivo
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[Abstract] [Full Text]

H. Ogino and K. Yasuda
Induction of Lens Differentiation by Activation of a bZIP Transcription Factor, L-Maf
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[Abstract] [Full Text]

				O. Shaham, A. N. Smith, M. L. Robinson, M. M. Taketo, R. A. Lang, and R. Ashery-Padan Pax6 is essential for lens fiber cell differentiation Development, August 1, 2009; 136(15): 2567 - 2578. [Abstract] [Full Text] [PDF]

				F Lacbawan, B D Solomon, E Roessler, K El-Jaick, S Domene, J I Velez, N Zhou, D Hadley, J Z Balog, R Long, et al. Clinical spectrum of SIX3-associated mutations in holoprosencephaly: correlation between genotype, phenotype and function J. Med. Genet., June 1, 2009; 46(6): 389 - 398. [Abstract] [Full Text] [PDF]

				H. Zhang and E. Stavnezer Ski Regulates Muscle Terminal Differentiation by Transcriptional Activation of Myog in a Complex with Six1 and Eya3 J. Biol. Chem., January 30, 2009; 284(5): 2867 - 2879. [Abstract] [Full Text] [PDF]

				S. Domene, E. Roessler, K. B. El-Jaick, M. Snir, J. L. Brown, J. I. Velez, S. Bale, F. Lacbawan, M. Muenke, and B. Feldman Mutations in the human SIX3 gene in holoprosencephaly are loss of function Hum. Mol. Genet., December 15, 2008; 17(24): 3919 - 3928. [Abstract] [Full Text] [PDF]

				T. Wataya, S. Ando, K. Muguruma, H. Ikeda, K. Watanabe, M. Eiraku, M. Kawada, J. Takahashi, N. Hashimoto, and Y. Sasai Minimization of exogenous signals in ES cell culture induces rostral hypothalamic differentiation PNAS, August 19, 2008; 105(33): 11796 - 11801. [Abstract] [Full Text] [PDF]

				S. L. Lewis, P.-L. Khoo, R. A. De Young, K. Steiner, C. Wilcock, M. Mukhopadhyay, H. Westphal, R. V. Jamieson, L. Robb, and P. P. L. Tam Dkk1 and Wnt3 interact to control head morphogenesis in the mouse Development, May 15, 2008; 135(10): 1791 - 1801. [Abstract] [Full Text] [PDF]

				I. Appolloni, F. Calzolari, G. Corte, R. Perris, and P. Malatesta Six3 Controls the Neural Progenitor Status in the Murine CNS Cereb Cortex, March 1, 2008; 18(3): 553 - 562. [Abstract] [Full Text] [PDF]

				A. Lavado, O. V. Lagutin, and G. Oliver Six3 inactivation causes progressive caudalization and aberrant patterning of the mammalian diencephalon Development, February 1, 2008; 135(3): 441 - 450. [Abstract] [Full Text] [PDF]

				C. L. Andoniadou, M. Signore, E. Sajedi, C. Gaston-Massuet, D. Kelberman, A. J. Burns, N. Itasaki, M. Dattani, and J. P. Martinez-Barbera Lack of the murine homeobox gene Hesx1 leads to a posterior transformation of the anterior forebrain Development, April 15, 2007; 134(8): 1499 - 1508. [Abstract] [Full Text] [PDF]

				B. L. Krock, J. Bilotta, and B. D. Perkins Noncell-autonomous photoreceptor degeneration in a zebrafish model of choroideremia PNAS, March 13, 2007; 104(11): 4600 - 4605. [Abstract] [Full Text] [PDF]

				T. Harada, C. Harada, and L. F. Parada Molecular regulation of visual system development: more than meets the eye Genes & Dev., February 15, 2007; 21(4): 367 - 378. [Abstract] [Full Text] [PDF]

				M. K. Sharma, D. B. Mansur, G. Reifenberger, A. Perry, J. R. Leonard, K. D. Aldape, M. G. Albin, R. J. Emnett, S. Loeser, M. A. Watson, et al. Distinct Genetic Signatures among Pilocytic Astrocytomas Relate to Their Brain Region Origin Cancer Res., February 1, 2007; 67(3): 890 - 900. [Abstract] [Full Text] [PDF]

				T. Hirata, M. Nakazawa, O. Muraoka, R. Nakayama, Y. Suda, and M. Hibi Zinc-finger genes Fez and Fez-like function in the establishment of diencephalon subdivisions Development, October 15, 2006; 133(20): 3993 - 4004. [Abstract] [Full Text] [PDF]

				J. Chu, J. Ding, K. Jeays-Ward, S. M. Price, M. Placzek, and M. M. Shen Non-cell-autonomous role for Cripto in axial midline formation during vertebrate embryogenesis Development, December 15, 2005; 132(24): 5539 - 5551. [Abstract] [Full Text] [PDF]

				S. Bassham and J. H. Postlethwait The evolutionary history of placodes: a molecular genetic investigation of the larvacean urochordate Oikopleura dioica Development, October 1, 2005; 132(19): 4259 - 4272. [Abstract] [Full Text] [PDF]

				H. Ikeda, F. Osakada, K. Watanabe, K. Mizuseki, T. Haraguchi, H. Miyoshi, D. Kamiya, Y. Honda, N. Sasai, N. Yoshimura, et al. Generation of Rx+/Pax6+ neural retinal precursors from embryonic stem cells PNAS, August 9, 2005; 102(32): 11331 - 11336. [Abstract] [Full Text] [PDF]

				T. A. Rodriguez, S. Srinivas, M. P. Clements, J. C. Smith, and R. S. P. Beddington Induction and migration of the anterior visceral endoderm is regulated by the extra-embryonic ectoderm Development, June 1, 2005; 132(11): 2513 - 2520. [Abstract] [Full Text] [PDF]

				N. Nishioka, S. Nagano, R. Nakayama, H. Kiyonari, T. Ijiri, K. Taniguchi, W. Shawlot, Y. Hayashizaki, H. Westphal, R. R. Behringer, et al. Ssdp1 regulates head morphogenesis of mouse embryos by activating the Lim1-Ldb1 complex Development, June 1, 2005; 132(11): 2535 - 2546. [Abstract] [Full Text] [PDF]

				J. Kimura, Y. Suda, D. Kurokawa, Z. M. Hossain, M. Nakamura, M. Takahashi, A. Hara, and S. Aizawa Emx2 and Pax6 Function in Cooperation with Otx2 and Otx1 to Develop Caudal Forebrain Primordium That Includes Future Archipallium J. Neurosci., May 25, 2005; 25(21): 5097 - 5108. [Abstract] [Full Text] [PDF]

				L Pasquier, C Dubourg, M Gonzales, L Lazaro, V David, S Odent, and F Encha-Razavi First occurrence of aprosencephaly/atelencephaly and holoprosencephaly in a family with a SIX3 gene mutation and phenotype/genotype correlation in our series of SIX3 mutations J. Med. Genet., January 1, 2005; 42(1): e4 - e4. [Full Text] [PDF]

				N. Gotoh, M. Ito, S. Yamamoto, I. Yoshino, N. Song, Y. Wang, I. Lax, J. Schlessinger, M. Shibuya, and R. A. Lang Tyrosine phosphorylation sites on FRS2{alpha} responsible for Shp2 recruitment are critical for induction of lens and retina PNAS, December 7, 2004; 101(49): 17144 - 17149. [Abstract] [Full Text] [PDF]

				Y. Kida, Y. Maeda, T. Shiraishi, T. Suzuki, and T. Ogura Chick Dach1 interacts with the Smad complex and Sin3a to control AER formation and limb development along the proximodistal axis Development, September 1, 2004; 131(17): 4179 - 4187. [Abstract] [Full Text] [PDF]

				D. Kurokawa, N. Takasaki, H. Kiyonari, R. Nakayama, C. Kimura-Yoshida, I. Matsuo, and S. Aizawa Regulation of Otx2 expression and its functions in mouse epiblast and anterior neuroectoderm Development, July 15, 2004; 131(14): 3307 - 3317. [Abstract] [Full Text] [PDF]

				D. Kurokawa, H. Kiyonari, R. Nakayama, C. Kimura-Yoshida, I. Matsuo, and S. Aizawa Regulation of Otx2 expression and its functions in mouse forebrain and midbrain Development, July 15, 2004; 131(14): 3319 - 3331. [Abstract] [Full Text] [PDF]

				O. G. Kelly, K. I. Pinson, and W. C. Skarnes The Wnt co-receptors Lrp5 and Lrp6 are essential for gastrulation in mice Development, June 15, 2004; 131(12): 2803 - 2815. [Abstract] [Full Text] [PDF]

				K. J. Whitehead, N. W. Plummer, J. A. Adams, D. A. Marchuk, and D. Y. Li Ccm1 is required for arterial morphogenesis: implications for the etiology of human cavernous malformations Development, March 15, 2004; 131(6): 1437 - 1448. [Abstract] [Full Text] [PDF]

				C.-W. Chang, C.-W. Tsai, H.-F. Wang, H.-C. Tsai, H.-Y. Chen, T.-F. Tsai, H. Takahashi, H.-Y. Li, M.-J. Fann, C.-W. Yang, et al. Identification of a developmentally regulated striatum-enriched zinc-finger gene, Nolz-1, in the mammalian brain PNAS, February 24, 2004; 101(8): 2613 - 2618. [Abstract] [Full Text] [PDF]

				H. Ozaki, K. Nakamura, J.-i. Funahashi, K. Ikeda, G. Yamada, H. Tokano, H.-o. Okamura, K. Kitamura, S. Muto, H. Kotaki, et al. Six1 controls patterning of the mouse otic vesicle Development, February 1, 2004; 131(3): 551 - 562. [Abstract] [Full Text] [PDF]

				L. Zakin and E. M. De Robertis Inactivation of mouse Twisted gastrulation reveals its role in promoting Bmp4 activity during forebrain development Development, January 15, 2004; 131(2): 413 - 424. [Abstract] [Full Text] [PDF]

				M. E. Zuber, G. Gestri, A. S. Viczian, G. Barsacchi, and W. A. Harris Specification of the vertebrate eye by a network of eye field transcription factors Development, November 1, 2003; 130(21): 5155 - 5167. [Abstract] [Full Text] [PDF]