A wide-range phylogenetic analysis of Zic proteins: Implications for correlations between protein structure conservation and body plan complexity

Aruga, Jun; Kamiya, Akio; Takahashi, Hirokazu; Fujimi, Takahiko J.; Shimizu, Yuri; Ohkawa, K.; Yazawa, Shogo; Umesono, Yoshihiko; Noguchi, Hideki; Shimizu, Takashi; Saitou, Naruya; Mikoshiba, Katsuhiko; Sakaki, Yoshiyuki; Agata, Kiyokazu; Toyoda, Atsushi

doi:10.1016/j.ygeno.2006.02.011

Cited by 73 publications

(96 citation statements)

References 34 publications

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“…1D). These results are consistent with a recently proposed hypothesis that the single ancestral Zic gene in the vertebrate ancestor has gone through one tandem duplication, two genome duplications, and occasional disappearance (Aruga et al, 2006). According to the model, Zic4 and Zic5 are counterparts on different chromosomes that arose by genome quadruplication.…”

Section: Structure Of Xenopus Zic4supporting

confidence: 91%

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Xenopus Zic4: Conservation and diversification of expression profiles and protein function among the Xenopus Zic family

Fujimi

Mikoshiba

Aruga

2006

Developmental Dynamics

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We compared the expression and function of Xenopus Zic4 with those of the other four Xenopus laevis Zic family members (Zic1, Zic2, Zic3, and Zic5). Zic4 expression was detected mainly in the neural plate border, dorsal neural tube, and somites, and was similar to that of Zic1, which is adjacent to Zic4 on the same chromosome. Injection of wild-type or mutant Zic4 RNA caused the induction of neural crest marker gene expression, hyperplastic neural tissue, and ectopic pigment cell formation, indicating that Zic4 can induce neural and neural crest tissue, as can other Xenopus Zic genes. Deletion analysis showed that the zinc-finger domain is critical for many Zic4 functions, but the C-terminal region is differently involved in induction of two neural crest markers, Slug and Sox10. The protein function as determined by the animal cap explant assay was similar to that of Zic5, but different from those of Zic1, Zic2, and Zic3, suggesting that Xenopus Zic genes can be divided into two groups based on function. These results indicate that the five Xenopus Zic genes cooperatively regulate both neural and neural crest development, despite significantly diverged expression profiles and functions. Developmental Dynamics 235:3379 -3386, 2006.

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Section: Structure Of Xenopus Zic4supporting

confidence: 91%

“…The gene clustering profile and exon-intron boundaries in the ZF domains are conserved between Xenopus and mouse ( Fig. 1C; Aruga et al, 2006; data not shown). The neighbor-joining molecular phylogenetic tree indicates that the mammalian-amphibian common ancestor already possessed the five Zic genes (Fig.…”

Section: Structure Of Xenopus Zic4mentioning

confidence: 96%

Xenopus Zic4: Conservation and diversification of expression profiles and protein function among the Xenopus Zic family

Fujimi

Mikoshiba

Aruga

2006

Developmental Dynamics

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“…1 P and S). In contrast, the expression of the anterior-specific gene DjZicB (16) was not induced in the anterior blastema at regeneration day 1, but rather decreased to the same level as that in the posterior blastema at day 3 in Djptc(RNAi) (Fig. 1 Q and S).…”

Section: Resultsmentioning

confidence: 93%

Planarian Hedgehog/Patched establishes anterior–posterior polarity by regulating Wnt signaling

Yazawa

Umesono²,

Hayashi³

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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147

161

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Despite long-standing interest, the molecular mechanisms underlying the establishment of anterior-posterior (AP) polarity remain among the unsolved mysteries in metazoans. In the planarians (a family of flatworms), canonical Wnt/␤-catenin signaling is required for posterior specification, as it is in many animals. However, the molecular mechanisms regulating the posterior-specific induction of Wnt genes according to the AP polarity have remained unclear. Here, we demonstrate that Hedgehog (Hh) signaling is responsible for the establishment of AP polarity via its regulation of the transcription of Wnt family genes during planarian regeneration. We found that RNAi gene knockdown of Dugesia japonica patched (Djptc) caused ectopic tail formation in the anterior blastema of body fragments, resulting in bipolar-tails regeneration. In contrast, RNAi of hedgehog (Djhh) and gli (Djgli) caused bipolar-heads regeneration. We show that Patched-mediated Hh signaling was crucial for posterior specification, which is established by regulating the transcription of Wnt genes via downstream Gli activity. Moreover, differentiated cells were responsible for the posterior specification of undifferentiated stem cells through Wnt/␤-catenin signaling. Surprisingly, Djhh was expressed in neural cells all along the ventral nerve cords (along the AP axis), but not in the posterior blastema of body fragments, where the expression of Wnt genes was induced for posteriorization. We therefore propose that Hh signals direct head or tail regeneration according to the AP polarity, which is established by Hh signaling activity along the body's preexisting nervous system. body polarity ͉ regeneration ͉ anteroposterior axis ͉ neuron ͉ stem P lanarians are one of the most useful animals for investigation of the molecular and cellular mechanisms by which the anteriorposterior (AP) polarity of the body is established during regeneration. It is well known that planarians regenerate a head or a tail from the anterior and posterior ends, respectively, of the amputated stump, with maintenance of the original AP polarity. More than a century ago, T.H. Morgan reported one of the earliest descriptions of ''polarity'' in planarian regeneration (1), based on his findings that very thin cross-sectional fragments made by cutting along the AP axis regenerated bipolar two-headed planarians (2), termed ''Janus-heads'' (an allusion to the Roman god Janus; 3, 4). Since then, much effort has been focused on this fascinating maintenance of the original polarity, and its disruption, such as the induction of Janus-heads formation by treatment with colchicine or colcemid (5, 6), although the molecular mechanisms still remain unknown.Recently, canonical Wnt/␤-catenin signaling was shown to be required for posterior specification in planarians. Wnt/␤-catenin signaling is evolutionarily well conserved and plays a role in establishing the AP axis during development in several animal species. In the planarian Schmidtea mediterranea, gene knockdown by RNA interference (RNAi) of ...

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“…The Emx sequence was deposited in the DDBJ database with accession number AB439506. Tubifex Zic (Ttu-Zic, AB231870) and Tubifex Msx (Ttu-Msx, AB302957) cDNAs were previously described (Aruga et al 2006;Takahashi et al 2008). …”

Section: Pcr Cloning and Rt-pcr Analysismentioning

confidence: 99%

“…Recent molecular phylogenetic analyses have revealed that Zic family genes are found in a wide range of eumetazoans (Aruga et al 2006. Expression and functional analyses indicate that Zic zinc finger proteins commonly play roles in cell differentiation and proliferation in the early embryonic stages in Deuterostomia, Ecdysozoa, and Cnidaria (reviewed in Aruga 2004;Merzdorf 2007).…”

Section: Introductionmentioning

confidence: 99%

Expression pattern of annelid Zic in embryonic development of the oligochaete Tubifex tubifex

2008

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Embryonic expression of a Zic homologue (Ttu-Zic) was examined in the oligochaete annelid Tubifex tubifex. The body plan of T. tubifex is characterized by obvious segmentation in the ectoderm and mesoderm. Ttu-Zic expression is detected in the mesodermal germ band and a subset of micromere descendants. Ttu-Zic is transiently expressed in primary m-blast cells (i.e., founder cells of mesodermal segments) as early as the time of their birth from M teloblasts. During its development, each mesodermal segment experiences two additional phases of Ttu-Zic expression. Ttu-Zic expression in micromere descendants is seen on the anterior surfaces of embryos undergoing teloblastogenesis; subsequently, these cells proliferate to form bilateral clusters, which then become internalized. Finally, clusters of Ttu-Zic-expressing cells are found in the center of the prostomium, corresponding to the cerebral ganglion. The Ttu-Zic expression profile in the early embryogenesis of T. tubifex may be homologous to those of evolutionarily distant animals.

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A wide-range phylogenetic analysis of Zic proteins: Implications for correlations between protein structure conservation and body plan complexity

Cited by 73 publications

References 34 publications

Xenopus Zic4: Conservation and diversification of expression profiles and protein function among the Xenopus Zic family

Xenopus Zic4: Conservation and diversification of expression profiles and protein function among the Xenopus Zic family

Planarian Hedgehog/Patched establishes anterior–posterior polarity by regulating Wnt signaling

Expression pattern of annelid Zic in embryonic development of the oligochaete Tubifex tubifex

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