Encyclopedia.com. Co-existence: the primitive endostyle and thyroid follicles are not mutually exclusive in this state. [49], respectively. Mol Biol Evol. Transcriptional Analysis of the Endostyle Reveals Pharyngeal Organ Functions in Ascidian. S5. Love, M.I. ; Huber, W.; Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. S2. However, the lung and its homolog (the swim bladder) are presumed to be a synapomorphy of Osteichthyes (bony vertebrates), and thus, the expression domain of Nkx2-1 in these respiratory organs was likely acquired after Osteichthyes and Chondrichthyes split from each other and likely does not reflect an ancestral condition of gnathostomes. ." B, B Sections were stained using hematoxylin and eosin. PeerJ. endostyle. ; et al. After full sinkage, the solution on the surface of the tissue was dried with Kimtech wiper (FIS: 06666) and the tissue was merged into the optimal cutting temperature compound (OCT, SAKURA Tissue-Tek. Staging of cyclostome and catshark embryos used in this study. Bars, 200 m. A Acquisition of the primitive endostyle, which originated from the pharyngeal endoderm with broad expression of Nkx2-1/2-4 and subordinate endostyle GRN. Under this sample-collecting strategy, the general expression profile of the endostyle samples was similar (. Kim, D.; Paggi, J.M. Serra M, Alysandratos KD, Hawkins F, McCauley KB, Jacob A, Choi J, et al. zoology, branch of biology that studies the members of the animal kingdom and animal life in general. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. Fig. It functions similarly to the thyroid found on vertebrates. Mts, L.; Korpos, E.; Dak, F.; Liu, Z.; Beier, D.R. The library construction and sequencing experiment were accomplished by the Novogene experimental department. Rinkevich, Y.; Voskoboynik, A.; Rosner, A.; Rabinowitz, C.; Paz, G.; Oren, M.; Douek, J.; Alfassi, G.; Moiseeva, E.; Ishizuka, K.J. Berlin: Springer-Verlag; 1992. In the mammalian thyroid, Nkx2-1 and Pax8 genes are known to be involved both in organogenesis and physiological function [19, 21]. Featured [5], Early beliefs of the endostyle included the idea by Muller in 1873 stating that the endostyle that reside in the ammocoete has extremely similar functions as the protochordate hypobranchial groove. A distinct cellular component, the dynein complex [, For all four categories, the highly expressed genes can describe the fundamental functional pathway in the endostyle. Temperature pre-balance was performed for 30 min before sectioning the frozen block. This is similar to the consistency and appearance of the ventral glandular tracts. What is the function of endostyle in Protochordates? and P.L. 2B, B, C). Fang Zongxi Center, MoE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China, Laoshan Laboratory, Qingdao 266237, China, Institute of Evolution & Marine Biodiversity, Ocean University of China, Qingdao 266003, China. The distributions of thyroid-related genes including Pax2/5/8 and Nkx2-1/2-4 orthologs in adult amphioxi and tunicates similarly do not extend to the entire endostyle in cross-sectional view. Meanwhile, different from gnathostomes, the broad pharyngeal expression of Nkx2-1/2-4 prior to the initiation of the development of endostyle and thyroid was shared in lamprey and hagfish. BMC Biology ; Nakanishi, R.; Sasakura, Y.; Ogasawara, M. Nkx2-1 and FoxE regionalize glandular (mucus-producing) and thyroid-equivalent traits in the endostyle of the chordate, Yamagishi, M.; Huang, T.; Hozumi, A.; Onuma, T.A. Iodine metabolism and thyroid-related functions in organisms lacking thyroid follicles: are thyroid hormones also vitamins? Integr Comp Biol. Development. The presence of this structure, which was described as a rudiment of the endostyle almost a century later [10], and the broad pharyngeal origin of hagfish thyroid follicles would be consistent with the classical assumption that considers the endostyle a plesiomorphic trait retained in cyclostomes (Fig. For DEG filtered in the middle part of the endostyle, only two genes were concluded, which may reflect that most genes have longitudinal even expression trends or transiting expression patterns across longitudinal levels under the current sample collecting strategy. Anyone you share the following link with will be able to read this content: Sorry, a shareable link is not currently available for this article. This suggests that the regulatory roles of Foxe1 in thyroid development may not be conserved among gnathostomes [19]. Neither of the above glandular regions are involved in iodine metabolism. https://www.encyclopedia.com/science/dictionaries-thesauruses-pictures-and-press-releases/endostyle-0, "endostyle Adults and the deposited eggs were maintained in the same laboratory tank, and the embryos were fixed with 4% paraformaldehyde and Bouins fixative for in situ hybridization and histological observation, respectively. Holley, M.C. S1A), the thyroid follicle is a common functional unit and an evolutionary novelty of vertebrates [3]. E, E, H, H Sections including thyroid primordia were stained via in situ hybridization of Tbx1/10A (E, E) and Lhx3/4A (H, H) with nuclear fast red in a previous study [17]. Paper should be a substantial original Article that involves several techniques or approaches, provides an outlook for Acquisition of the follicular thyroid gland enables the efficient uptake and storage of iodine, which is notoriously scarce in freshwater environments, likely contributing to the early radiation of aquatic vertebrates [8]. For example, the Nkx2-1/2-4 ortholog is not expressed in the thyroid-equivalent elements in the ascidian Ciona intestinalis, and the Pax2/5/8 ortholog is not expressed in part of the supporting elements in the cephalochordate Branchiostoma belcheri [12]. This work was supported by Grant-in-Aid for Scientific Research (A) 15H02416, Grant-in-Aid for Scientific Research on Innovative Areas (Research in a Proposed Research Area) 17H06385, and a Naito Grant for the Promotion of Focused Research (The Naito Foundation) to SK; Grant-in-Aid for JSPS Fellows 15J08671 and a Special Postdoctoral Researcher Program of RIKEN to WT; Grant-in-Aid for Scientific Research (C) 19K06794 to FS, Laboratory of Physiology, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, 277-8564, Japan, Evolutionary Morphology Laboratory, RIKEN Cluster for Pioneering Research (CPR), Kobe, 650-0047, Japan, Wataru Takagi,Fumiaki Sugahara,Juan Pascual-Anaya&Shigeru Kuratani, Division of Biology, Hyogo College of Medicine, Nishinomiya, 663-8501, Japan, Department of Molecular Biology and Biochemistry, Graduate School of Biomedical & Health Sciences, Hiroshima University, Hiroshima, 734-8553, Japan, Laboratory for Evolutionary Morphology, RIKEN Center for Biosystems Dynamics Research (BDR), Kobe, 650-0047, Japan, Shinnosuke Higuchi,Rie Kusakabe,Iori Sato&Shigeru Kuratani, Present Address: Department of Animal Biology, Faculty of Science, University of Mlaga, Mlaga, Spain, Present Address: Andalusian Centre for Nanomedicine and Biotechnology (BIONAND), Mlaga, Spain, Laboratory for Haptic Perception and Cognitive Physiology, RIKEN Center for Brain Science, Wako, 351-0198, Japan, Laboratory Research Support Section, Center for Cooperative Research Promotion, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, 277-8564, Japan, Faculty of Agriculture, University of Miyazaki, Gakuen-kibanadai-nishi, 889-2192, Japan, Aix-Marseille Universit, IBDM, CNRS UMR 7288, Marseille, France, Present address: Department of Molecular Craniofacial Embryology, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University (TMDU), Tokyo, 113-8549, Japan, You can also search for this author in For the convenience of sample collection, each endostyle was evenly divided into three continuous segments. Genes Dev. (July 1, 2023). Because of the regional thyroid hormone synthesis capacity and transformation into follicle thyroid-like cells during metamorphosis in ammocoetes, the endostyle is believed to be an evolutionary precursor of the thyroid gland [, In this research, high-quality RNA-seq results were obtained with three biological replicons. Disclaimer/Publishers Note: The statements, opinions and data contained in all publications are solely Food particles are trapped by mucus produced by the pharynx, and then transported toward the oesophagus. The total RNA was extracted from the frozen or fresh whole embryos using the ISOGEN reagent (Nippon Gene, Toyama, Japan). Paris M, Escriva H, Schubert M, Brunet F, Brtko J, Ciesielski F, et al. [3][4], The endostyle in larval lampreys (ammocoetes) metamorphoses into the thyroid gland in adults, and is regarded as being homologous to the thyroid gland in vertebrates due to its iodine-concentrating activity. Pick a style below, and copy the text for your bibliography. Kluge B, Renault N, Rohr KB. Twelve years of SAMtools and BCFtools. Zoologists study animals and their interactions with ecosystems. Evidence from cyclostomes for complex regionalization of the ancestral vertebrate brain. ." Nonaka, M.; Satake, H. Urochordate immunity. In mammals it stimulates the m, Secrecy ." "Endostyle - an overview | ScienceDirect Topics", "Endostyles and endostylar secretions: A comparative histochemical study", The Metamorphosis of the Endostyle (Thyroid Gland) of, https://en.wikipedia.org/w/index.php?title=Endostyle&oldid=1162204247, This page was last edited on 27 June 2023, at 16:50. [CDATA[ Privacy Although the general anatomy of the vertebrate thyroid gland is highly diverse (Additional file 1: Fig. Google Scholar. 3X; Additional file 1: Fig. An endostyle may have evolved secondarily at the base of crown lampreys in association with the filter-feeding larval stage. The food particles suspended in the water adhere to the mucus it produces. https://doi.org/10.3390/biology12020245, Jiang A, Zhang W, Wei J, Liu P, Dong B. Considering the monophyly of cyclostomes [16, 17], further studies on the development of the thyroid in hagfish, the other group of extant cyclostomes, may enhance our knowledge regarding the evolution of the vertebrate thyroid and endostyle by providing a clearer understanding of the last common ancestor (LCA) of vertebrates. K, L, M, O, P, Q, S, T, and U Transverse sections of hybridized embryos in the plane of the dashed lines. Discovery of fossil lamprey larva from the Lower Cretaceous reveals its three-phased life cycle. ; Lindskog, C.; Oksvold, P.; Mardinoglu, A.; Sivertsson, .; Kampf, C.; Sjstedt, E.; Asplund, A.; et al. Takagi, W.; Sugahara, F.; Higuchi, S.; Kusakabe, R.; Pascual-Anaya, J.; Sato, I.; Oisi, Y.; Ogawa, N.; Miyanishi, H.; Adachi, N.; et al. Eptatretus burgeri embryos were obtained as per a previous protocol [24, 40] and fixed as described previously [17, 25, 41]. Since the endostyle is found in all three branches of chordates, it is presumed to have arisen in the common ancestor of these taxa, along with a shift to internal feeding for extracting suspended food from the water. //. Because of the large number of ribonucleoproteins in the gland cells, the synthesis of protein and a protein material rich in -SS and -SH bridges. ; Vizzini, A.; Parrinello, N.; Cammarata, M. Voskoboynik, A.; Soen, Y.; Rinkevich, Y.; Rosner, A.; Ueno, H.; Reshef, R.; Ishizuka, K.J. In situ hybridization methods. Examples are the sebaceous and sw, https://www.encyclopedia.com/science/dictionaries-thesauruses-pictures-and-press-releases/endostyle, https://www.encyclopedia.com/science/dictionaries-thesauruses-pictures-and-press-releases/endostyle-0. 2016;4:e2771. There has been no definitive proof of secretory ability within this zone, despite the existence of an acidic mucosal material that accumulates on the surface of the cells. The endostyle serves as a filter-feeding and thyroid hormone-synthesizing function and is recognized as a prototype of the thyroid gland. The head kidney in fish is believed to be analogous to the mammalian bone marrow and the primary site of hematopoiesis. Fujita, H.; Nanba, H. Fine structure and its functional properties of the endostyle of ascidians, Sasaki, A.; Miyamoto, Y.; Satou, Y.; Satoh, N.; Ogasawara, M. Novel endostyle-specific genes in the ascidian. 2018;2:176171. Single-cell transcriptome analysis reveals thyrocyte diversity in the zebrafish thyroid gland. 9108). 2015;527:45965. It is an organ which assists chordates in filter-feeding. Ogasawara M. Overlapping expression of amphioxus homologs of the thyroid transcription factor-1 gene and thyroid peroxidase gene in the endostyle: insight into evolution of the thyroid gland. Marine D. The metamorphosis of the endostyle (thyroid gland) of ammocoetes branchialis (larval land-locked Petromyzon marinus (Jordan) or Petromyzon dorsatus (Wilder)). Comparative analysis of the mouse and human genes (Matn2 and MATN2) for matrilin-2, a filament-forming protein widely distributed in extracellular matrices. 2023 . Please let us know what you think of our products and services. ; Chen, S.Y. Osugi, T.; Sasakura, Y.; Satake, H. The ventral peptidergic system of the adult ascidian. Pascual-Anaya J, Sato I, Sugahara F, Higuchi S, Paps J, Ren Y, et al. Thus, numerous investigations into the endostyle ensued, only for the theory to be denied by future researchers. ; Kim, J.K.; et al. The conserved fertility factor SPACA4/Bouncer has divergent modes of action in vertebrate fertilization. In 1906, Stockard reported that the thyroid gland in hagfish, the sister cyclostome group of lampreys, develops through an endostyle-like primordium, strongly supporting the plesiomorphy of the lamprey endostyle. https://www.mdpi.com/openaccess. "endostyle You are accessing a machine-readable page. Genomic analysis of immunity in a Urochordate and the emergence of the vertebrate immune system: waiting for Godot. Type 1 cells in the endostyle contain enlarged, circular nuclei and a large nucleolus. CAS Although the presence of a rudimentary endostyle in these stem lampreys cannot be ruled out, these observations cast doubt on the prevailing view that the ammocoete larva best resembles the earliest vertebrates [36, 37]. 2018;4:5. Kusakabe R, Higuchi S, Tanaka M, Kadota M, Nishimura O, Kuratani S. Novel developmental bases for the evolution of hypobranchial muscles in vertebrates. The endostyle is an anatomical feature found in invertebrate chordates and larval lampreys. Development of the thyroid gland in the Eptatretus burgeri embryo. The molecular phylogenetic trees of vertebrate Pax2/5/8 and Hhex genes were inferred via the maximum-likelihood method using PhyML3.0 (http://www.atgc-montpellier.fr/phyml/download.php) with the JTT+G4 model. 1993;267:31836. It is found in adult urochordates and cephalochordates, as well as in the larvae of the vertebrate lampreys,[1] but has been transformed through evolutionary time into the thyroid in all other vertebrates. [4], Zone 2 is classified with ventral glandular tracts. Hagfish and lamprey Hox genes reveal conservation of temporal colinearity in vertebrates. The plasmids containing lamprey Nkx2-1/2-4 paralogues (Nkx2-1/2-4A, B, C) generated in a previous study were used for probe synthesis [25]. Maag, J.L.V. The band of cells in Zone 11 mimic but are vastly different from Zone 1 cells. In L. camtschaticum at Taharas stage 24 [27], the endostyle diverticulum was distinguishable by the broad medial expression of Nkx2-1/2-4A and Nkx2-1/2-4C genes in the pharynx (Fig. We described the early development of the thyroid and endostyle in two extant cyclostomes and found that the histological features and the regulatory gene expression of hagfish thyroid development are nearly identical to those in gnathostomes, namely direct development. [4], 2c cells, are richly granulated and very easily recognizable. Fredriksson, G.; fverholm, T.; Ericson, L.E. [4]. [4], Type 1 cells make up the cells of the gland cylinders. The endostyle is a longitudinal, ciliated, grooved organ on the ventral wall of the pharynx that secretes mucoproteins into the alimentary canal for filter feeding (Fig. 3A, A, V). The spatiotemporal expression patterns of Nkx2-1/2-4 shared by hagfish and lamprey are similar to those of orthologous genes during the endostyle development in non-vertebrate chordates [13]. they achieve sexual maturity and reproduce without losing the larval form. Evolution of the thyroid: Anterior-posterior regionalization of the Oikopleura endostyle revealed by Otx, Pax2/5/8, and Hox1 expression. Dorsal (A, D) and lateral views (G) of fixed embryos immersed in methyl benzoate prior to paraffin embedding. Gene expression profiling at early organogenesis reveals both common and diverse mechanisms in foregut patterning. It is generally considered to be an evolutionary precursor of the thyroid gland of vertebrates. Kinds of immune effector cells with certain markers were defined in the endostyle and subendostylar region bathed with circulatory cells. Wong for critical reading of the manuscript; S. Shibuya and K. Yamamoto for maintenance of aquarium tanks; S. Kuraku, Y. Hara, M. Kadota, K. Itomi, C. Tanegashima, K. Tatsumi, and O. Nishimura from the Phyloinformatics Team, RIKEN BDR, for gene sequence analyses. END, endostyle; THY, thyroid. Petersen, J.K. Ascidian suspension feeding. Chapter Sugahara F, Murakami Y, Adachi N, Kuratani S. Evolution of the regionalization and patterning of the vertebrate telencephalon: what can we learn from cyclostomes? Zoologists are interested in them because they provide evolutionary insight into the origins of vertebrates. 1988;5:10918. Kimura S, Hara Y, Pineau T, Fernandez-Salguero P, Fox CH, Ward JM, et al. ; Sinha, R.; Okamoto, J.; Mantalas, G.; et al. BMC Biol 20, 76 (2022). There is currently no evidence that ancestral species possessed an endostyle in the branches leading to these taxa. Encyclopedia.com. What Does a Zoologist Do? endostyle ( plural endostyles ) English Wikipedia has an article on: endostyle. It is found in adult urochordates and cephalochordates, as well as in the larvae of the vertebrate lampreys,[1] but has been transformed through evolutionary time into the thyroid in all other vertebrates. as, aortic sac; opm, vestigial oropharyngeal membrane; MHB, midbrain-hindbrain boundary; ma, mandibular arch; liv, liver; hyp, hypothalamus; ve, velum; pn, pronephros. The identification of monoiodotyrosine, diiodotyrosine and thyroxine in extracts of the endostyle of the ascidian, Barrington, E.J.W. Nilsson, M.; Fagman, H. Development of the thyroid gland. Davidson, A.J. The cryosection was pasted onto adhesion microscope slides and persevered at 80 C. [4], The secretory regions in which the endostyle are known for include the ventral glandular region and the dorsal glandular region. Nature. Thus, we propose the following alternative evolutionary scenario for the vertebrate thyroid and endostyle (Fig. Retrieved July 01, 2023 from Encyclopedia.com: https://www.encyclopedia.com/science/dictionaries-thesauruses-pictures-and-press-releases/endostyle. The thyroid hormones exert important pleiotropic effects on development, growth, energy metabolism, and metamorphosis. Eales JG. 2023 . Materials for secretion is accumulated in Zone 1 and 2. 2013;23:47583. All experiments and relevant methods were carried out in accordance with the approved guidelines and regulations of OUC-IACUC (No. chordate anatomy. ." Rubin, S.A.; Baron, C.S. The aim is to provide a snapshot of some of the http://ccb.jhu.edu/software/stringtie/index.shtml?t=manual#deseq, https://CRAN.R-project.org/package=pheatmap, https://www.ncbi.nlm.nih.gov/tools/primer-blast/, https://rdocumentation.org/packages/ggsignif/versions/0.6.4, https://bioinfogp.cnb.csic.es/tools/venny/index.html, https://www.proteinatlas.org/about/download, https://www.proteinatlas.org/humanproteome/tissue/tissue+specific, Supplemental Figure S4, Supplementary Table S2, Supplementary Figure S5B, Supplementary Table S3, https://www.mdpi.com/article/10.3390/biology12020245/s1, https://creativecommons.org/licenses/by/4.0/. Kluge, B.; Renault, N.; Rohr, K.B. You can help Wikipedia by expanding it. Interestingly, in this result, except for the generally acknowledged thyroid and digestive-related tissue (stomach and salivary), the parathyroid was reported for the first time as a highly similar organ, which needs further research and evidence in supporting the possible evolutionary lineage. [4], Zone 3 is classified by narrow ciliated bands nestled between glandular zones. The endostyle is also found in the filter-feeding ammocoete larvae of modern lampreys, and a portion of the epithelial cells of the ammocoete endostyle re-differentiates and transforms into thyroid follicles during metamorphosis [14] (Fig. Canestro, C.; Bassham, S.; Postlethwait, J.H. Thus, the lamprey endostyle was considered to represent a state of non-vertebrate chordates [1, 8]. Dashed lines indicate the boundary between stomodeum and pharynx. Google Scholar. ; Zon, L.I. Secrecy, according to sociologist Edward Shils, (19111995) is a form of concealment reinforced by sanctions against disclosure, apocrine gland A type of gland in which the apical part, from which the secretion is released, breaks down during the secretion process. Azumi, K.; De Santis, R.; De Tomaso, A.; Rigoutsos, I.; Yoshizaki, F.; Pinto, M.R. The tissue after fixation was washed with cooled PBS to wash off PFA and the tissue was transferred into 30% sucrose solution (made with PBS solution) in the flat-bottomed container. future research directions and describes possible research applications. As negative controls, sense strand probes were used for in situ hybridization in catshark and lamprey embryos. Expression profiles of the genes involved in thyroid development in modern cyclostomes. Google Scholar. Since the endostyle is found in all . ; Palmeri, K.J. The sequences of hagfish Pax2/5/8A, B, and Hhex, and lamprey Pax2/5/8B, and Hhex were obtained from the previously reported transcriptome data sets from the GenBank database (SRA accession numbers: SRX2541845-SRX2541849; SRX2847491-SRX2847498) [46]. You can help Wikipedia by expanding it. [4], The two zones in which secretory activity occurs include Zone 2 and 4. Delsuc, F.; Brinkmann, H.; Chourrout, D.; Philippe, H.J.N. However, the findings in hagfish thyroid development were solely based on this single study, and these have not been confirmed by modern molecular, genetic, and morphological data pertaining to hagfish thyroid development over the last century. Zool Lett. A Dictionary of Biology. Galliciotti, G.; Sonderegger, P. Neuroserpin. This contains alternate bands of ciliated and glandular cells. Whole-mount in situ hybridization of lamprey embryos from stages 23 to 26 (n = 8 biological replicates) and shark embryos at stage 24 (n = 3 biological replicates) was performed according to Kusakabe et al. [4], Cylinder opening cells are identified as type 2 cells. Before library construction, the quality of RNA was finally analyzed by Agilent 2100 bioanalysis. Google Scholar. The primers for qRT-PCR were designed utilizing the NCBI primer design tool (, OSGs in the endostyle were aligned against the zebrafish (, The transcriptional matrix of the endostyle and pharynx, gill, head kidney, and thymus were compared manually with the Venny online interactive tool (, Human tissue-enriched genes were obtained from the protein atlas (, The endostyle in the ascidian is longitudinally extended on the dorsal pharyngeal wall (, To comprehensively uncover the function of the endostyle, bulk RNA sequencing on the endostyle was conducted. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. WT, FS, SH1, RK, JP-A, IS, YO, NO, HM, and NA performed experiments. Anatomical and molecular reinvestigation of lamprey endostyle development provides new insight into thyroid gland evolution.

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