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Activin a Induces Craniofacial Cartilage from Undifferentiated Xenopus Ectoderm in Vitro

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Activin a Induces Craniofacial Cartilage from Undifferentiated Xenopus Ectoderm in Vitro Activin A induces craniofacial cartilage from undifferentiated Xenopus ectoderm in vitro Miho Furue*, Yasufumi Myoishi†, Yasuto Fukui†, Takashi Ariizumi‡, Tetsuji Okamoto†, and Makoto Asashima‡§¶ *Department of Biochemistry and Molecular Biology, Kanagawa Dental College, Yokosuka 238-8580, Japan; †Department of Molecular Oral Medicine and Maxillofacial Surgery, Division of Frontier Medical Science, Graduate School of Biomedical Sciences, Hiroshima University, Hiroshima 734-8853, Japan; and ‡Solution Oriented Research for Science and Technology͞Japan Science and Technology Corporation, and §Department of Life Sciences (Biology), Graduate School of Arts and Sciences, University of Tokyo, Tokyo 153-0041, Japan Communicated by Gordon H. Sato, Ministry of Fisheries of Eritrea, Massawa, Eritrea, October 3, 2002 (received for review December 27, 2001) Activin A has potent mesoderm-inducing activity in amphibian To confirm this hypothesis, we investigated the induction of embryos and induces various mesodermal tissues in vitro from the cartilage, which hitherto had not been identified in the activin- isolated presumptive ectoderm. By using a sandwich culture treated presumptive ectoderm. During chondrogenesis of method established to examine activin A activity, we previously craniofacial development, the mesoderm-derived or neural demonstrated that activin-treated ectoderm can function as both crest-derived mesenchyme cells initially migrate to the pharyn- a head and trunk-tail organizer, depending on the concentration of geal arches and condense (13–15). The mesenchyme cell con- activin A. By using activin A and undifferentiated presumptive densation proceeds to the commitment of chondrocytes, pro- ectoderm, it is theoretically possible to reproduce embryonic in- ducing type II collagen (Col2) and the large chondroitin-sulfate duction. Here, we test this hypothesis by studying the induction of proteoglycans. Finally, chondrocytes differentiate into the ma- cartilage tissue by using the sandwich-culture method. In the ture cartilage tissues, including infrarostral cartilage, Meckel’s sandwiched explants, the mesenchymal cell condensation ex- cartilage, palatoquadrate, and branchial arch cartilage. This pressed type II collagen and cartilage homeoprotein-1 mRNA, and study demonstrates that craniofacial cartilage can be induced by subsequently, cartilage was induced as they are in vivo. goosecoid (gsc) mRNA was prominently expressed in the cartilage in the using activin A and the presumptive ectoderm, and, therefore, explants. Xenopus distal-less 4 (X-dll4) mRNA was expressed represents an in vitro model to examine the craniofacial cartilage throughout the explants. In Xenopus embryos, gsc expression is induction mechanisms in vertebrates. restricted to the cartilage of the lower jaw, and X-dll4 is widely Materials and Methods expressed in the ventral head region, including craniofacial carti- lage. These finding suggest that the craniofacial cartilage, espe- Embryos. Eggs of general Xenopus laevis were prepared as cially lower jaw cartilage, was induced in the activin–treated described (8, 10, 16). In brief, both males and females were sandwiched explants. In addition, a normal developmental pattern injected with 600 units of gonadotropin (Gestron; Denka was recapitulated at the histological and genetic level. This work Seiyaku, Kawasaki, Japan), and fertilized eggs were obtained. also suggests that the craniofacial cartilage-induction pathway is The eggs were raised until the late blastula stage (stage 9; ref. downstream of activin A. This study presents a model system 17), then the jelly coat was removed with Steinberg’s solution suitable for the in vitro analysis of craniofacial cartilage induction (SS) containing 4.5% cysteine hydrochloride (pH 7.8). The in vertebrates. vitelline membranes were manually removed from stage-9 em- bryos with forceps. chondrogenesis ͉ differentiation ͉ development ͉ animal cap Sandwich Culture. Presumptive ectodermal sheets (0.4 mm ϫ 0.4 ͞ ctivin A is a crucial morphogen in the vertebrate body plan mm) cut from stage-9 embryos were treated with 100 ng ml A(1–5), as demonstrated by its potent mesoderm-inducing activin A in SS for 1 h. Presumptive ectoderm precultured for 0, activity on Xenopus undifferentiated presumptive ectoderm (6, 1,2,3,or4hinfreshSSwassandwiched between two 7). Activin A induces nearly every mesodermal tissue from untreated-presumptive ectoderm sheets (0.8 mm ϫ 0.8 mm) cut amphibian undifferentiated presumptive ectoderm in a dose- from stage-9 eggs (Fig. 1). The sandwiched explants were dependent manner, whereas untreated ectoderm forms an ir- cultured in SS containing 0.1% fatty acid-free BSA (Sigma) in regularly shaped epidermis (8–10). At low concentrations of 96-well plates (Sumitomo Bakelite, Tokyo) for 4 days at 20°C. On activin A, ventral mesoderm, such as blood-like cells, coelomic day 4, the culture medium was changed to fresh SS, and the epithelium, and mesenchyme are induced in the explants. At explants were cultured in 24-well plates (Sumitomo Bakelite) for intermediate concentrations, muscle and neural tissue are in- an additional 10 days. duced. At high concentrations, notochord, the most dorsal mesoderm, is induced. These activin A-induced tissues are Histological and Immunohistochemical Examination. The general indistinguishable at the histological and molecular levels from embryos and explants were fixed with cold acetone overnight at those found in normal embryos. The most characteristic prop- 4°C and then processed into paraffin for serial sectioning (6 ␮M). erty of activin A is the induction of organizer activity. Previously, The sections were deparaffinized and then stained with Alcian we established the sandwich culture method to examine activin blue and PAS and counterstained with hematoxylin for light A activity in this role, demonstrating that activin-treated pre- microscopy. For immunohistochemistry, the serial sections were sumptive ectoderm can function as a head or trunk-tail orga- immunostained with mouse anti-Col2 antibody (Research Di- nizer, depending on the activin A concentration and preculture agnostics, Flanders, NJ), visualized with peroxidase-conjugated period after the activin treatment (8, 11, 12). Activin A triggers Simple Stain MAX PO goat anti-mouse IgG (Nichirei, Tokyo) several gene-expression cascades in the presumptive ectoderm with a time course that mimics the sequence in normal embry- onal development (2, 12). Therefore, it is theoretically possible Abbreviations: SS, Steinberg’s solution; DIG, digoxigenin. to reproduce embryonic induction by using activin A and ¶To whom correspondence should be addressed at: Department of Life Sciences (Biology), undifferentiated presumptive ectoderm and design a fundamen- Graduate School of Arts and Sciences, University of Tokyo, 3-8-1 Komaba, Meguro-ku, tal embryonic form in vitro. Tokyo 153-8902, Japan. E-mail: [email protected]. 15474–15479 ͉ PNAS ͉ November 26, 2002 ͉ vol. 99 ͉ no. 24 www.pnas.org͞cgi͞doi͞10.1073͞pnas.242597399 Downloaded by guest on September 30, 2021 RNA Probe Preparation. Recombinant plasmids of X-dll4, Col2, Cart-1, and goosecoid (gsc; generously provided by E. De Rob- ertis, University of California, Los Angeles) were used as templates for the synthesis of RNA probes. The digoxigenin (DIG) or fluorescein-labeled RNA sense and antisense probes were prepared from template cDNA, according to the RNA- labeling kit instructions (Roche Molecular Biochemicals). In Situ Hybridization. The general embryos and explants were fixed with 4% (wt͞vol) paraformaldehyde in phosphate buffer for 24 h at 4°C and then processed into paraffin for serial sectioning (10 ␮m). Except for the Col2, the deparaffinized sections were stained with Alcian blue for 2 min and cleared with 15% (vol͞vol) acetic acid in methanol for 10 min. The sections were Fig. 1. Schematic diagram of the procedure and sandwich-culture method. hybridized with DIG or fluorescein-labeled antisense or sense RNA probes at 60°C for 16 h. Then, the slides were washed once with 2ϫ SSC͞50% (vol͞vol) formamide, two times with 2ϫ SSC, and 3-amino-9-ethylcarbazol (AEC, Nichirei). Nuclei were coun- and three times with 0.1ϫ SSC, at 60°C for 15 min per wash. The terstained with hematoxylin. DIG-labeled Col2 signal was detected according to DIG detec- tion kit instructions by using NBT͞BCIP (Roche Molecular RT-PCR. Total RNA was extracted from explants and embryos by Biochemicals). To enhance the signals in the embryos (except for the guanidine-thiocyanate-phenol-chloroform extraction the Col2), the DIG-labeled signals were detected with peroxi- ␮ method (18). Total RNA from entire explant samples and 1 g dase-labeled anti-DIG antibody, biotinyl-tyramide (NEN), al- of total RNA derived from the whole embryo, the head region kaline phosphatase-labeled streptavidin, and NBT͞BCIP including the branchial arches, and the trunk-tail region, were (Roche Molecular Biochemicals) with 5% (vol͞vol) polyvinyl treated with RNase-free DNase I (GIBCO͞BRL). RT-PCR (19) alcohol (Wako Pure Chemical). To analyze the signals in a was then performed according to the instruction of GIBCO section of the explant, DIG was detected by using tyramide signal RT-PCR applications. Each cDNA was amplified by PCR by amplification (TSA)-cyanine 3 system (NEN), and fluorescein using the following primer pairs and cycling conditions: Xenopus was detected by using the TSA-fluorescein system (NEN). The distal-less 4(X-dll4) (20), 5Ј-tgcattccaaccacatgcc-3Ј,5Ј-
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