DOCSLIB.ORG

“Primordial Immune Complex”: Origins of MHC Class I and Antigen Receptors Revealed by Comparative Genomics

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
“Primordial Immune Complex”: Origins of MHC Class I and Antigen Receptors Revealed by Comparative Genomics Inferring the ''Primordial Immune Complex'': Origins of MHC Class I and Antigen Receptors Revealed by Comparative Genomics This information is current as of October 4, 2021. Yuko Ohta, Masanori Kasahara, Timothy D. O'Connor and Martin F. Flajnik J Immunol published online 6 September 2019 http://www.jimmunol.org/content/early/2019/09/05/jimmun ol.1900597 Downloaded from Supplementary http://www.jimmunol.org/content/suppl/2019/09/06/jimmunol.190059 Material 7.DCSupplemental http://www.jimmunol.org/ Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication by guest on October 4, 2021 *average Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 Copyright © 2019 by The American Association of Immunologists, Inc. All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. Published September 6, 2019, doi:10.4049/jimmunol.1900597 The Journal of Immunology Inferring the “Primordial Immune Complex”: Origins of MHC Class I and Antigen Receptors Revealed by Comparative Genomics Yuko Ohta,* Masanori Kasahara,† Timothy D. O’Connor,‡,x,{,‖ and Martin F. Flajnik* Comparative analyses suggest that the MHC was derived from a prevertebrate “primordial immune complex” (PIC). PIC duplicated twice in the well-studied two rounds of genome-wide duplications (2R) early in vertebrate evolution, generating four MHC paralogous regions (predominantly on human chromosomes [chr] 1, 6, 9, 19). Examining chiefly the amphibian Xenopus laevis, but also other vertebrates, we identified their MHC paralogues and mapped MHC class I, AgR, and “framework” genes. Most class I genes mapped to MHC paralogues, but a cluster of Xenopus MHC class Ib genes (xnc), which previously was mapped outside of the MHC paralogues, was surrounded by genes syntenic to mammalian CD1 genes, a region previously proposed as an MHC paralogue on human chr 1. Thus, this gene block is instead the result of a translocation that we call the translocated part of Downloaded from the MHC paralogous region (MHCtrans). Analyses of Xenopus class I genes, as well as MHCtrans, suggest that class I arose at 1R on the chr 6/19 ancestor. Of great interest are nonrearranging AgR-like genes mapping to three MHC paralogues; thus, PIC clearly contained several AgR precursor loci, predating MHC class I/II. However, all rearranging AgR genes were found on paralogues derived from the chr 19 precursor, suggesting that invasion of a variable (V) exon by the RAG transposon occurred after 2R. We propose models for the evolutionary history of MHC/TCR/Ig and speculate on the dichotomy between the jawless (lamprey and hagfish) and jawed vertebrate adaptive immune systems, as we found genes related to variable lymphocyte receptors http://www.jimmunol.org/ also map to MHC paralogues. The Journal of Immunology, 2019, 203: 000–000. he “2R hypothesis” has proposed that the early vertebrate (3, 4). Further analysis using the insulin/relaxin and neurotrophin/ genome experienced two rounds of genome-wide dupli- neurotrophin receptor family genes revealed that there are addi- T cations (1). Indeed, there are four paralogous clusters of tional regions containing paralogous genes in a similar order (5–7), genes in the genomes of all jawed vertebrates, first studied in humans and it has been suggested that the precursors of these regions and for homeobox and MHC genes (2, 3). When genes or genetic regions MHCpara were syntenic during the preduplication era, but some were are duplicated, some loci preserve their original function, whereas translocated over evolutionary time. These detached regions include others are modified (neofunctionalization or subfunctionalization) or sections of human chr 12, 14, and 15, and are generally shorter than by guest on October 4, 2021 may experience differential silencing. Other types of genome mod- the original regions; we refer to these detached regions as “minor ifications may occur, such as translocation of block regions, at times MHCpara,” and the original four regions as “major MHCpara.” blurring the origins of a particular genetic region. The MHC harbors many genes involved in adaptive and As mentioned, the MHC was one of the original gene clusters noted innate immunity (6, 8). Central to the adaptive immune system, for its paralogous regions (or “ohnologues”), found on human chro- the Ag-presenting MHC class I and class II molecules work in mosomes(chr)6(MHC),1,9,and19(MHCparalogues[MHCpara]) concert with Ag-processing (immunoproteasomes), peptide- transporting (TAP), peptide-editing (DM, TAPBP), and other *Department of Microbiology and Immunology, University of Maryland School molecules, to present antigenic peptides recognized by TCR. of Medicine, Baltimore, MD 21201; †Department of Pathology, Faculty of Med- Precursors of these genes were likely derived from the so-called icine and Graduate School of Medicine, Hokkaido University, Sapporo 060- 8638, Japan; ‡Institute for Genome Sciences, University of Maryland School primordial immune complex (PIC), predating the genome-wide of Medicine, Baltimore, MD, 21201; xProgram in Personalized and Genomic duplications in early vertebrates (9). Indeed, analysis of several in- Medicine, University of Maryland School of Medicine, Baltimore, MD, 21201; vertebrate deuterostome genomes [e.g., amphioxus (Branchiostoma {Marlene and Stewart Greenebaum Comprehensive Cancer Center, University of Maryland School of Medicine, Baltimore, MD, 21201; and ‖Department of Med- lanceolatum) (10), and a placozoan (Trichoplax adhaerens)(11)] icine, University of Maryland School of Medicine, Baltimore, MD 21201 revealed conserved synteny of proteasome and “framework” genes ORCID: 0000-0002-0276-1896 (T.D.O.). (i.e., nonimmune genes in MHC). To date, and unfortunately, no Received for publication May 23, 2019. Accepted for publication August 2, 2019. candidate class I/II genes have been detected in species derived from This project was supported by National Institutes of Health Grants AI140326-26 and ancestors predating the jawed vertebrates, and thus most genes AI02877 to Y.O. and M.F.F. strictly involved in adaptive immunity (based on MHC, Ig, TCR) Address correspondence and reprint requests to Dr. Martin F. Flajnik, University of seem to have appeared “suddenly” in a gnathostome ancestor. Be- Maryland, Baltimore, 655 West Baltimore Avenue, Room 3-056, Baltimore, MD cause both MHC and MHCpara are derived from a preduplicated 21201. E-mail address: mfl[email protected] precursor region in a common vertebrate ancestor (3, 6, 9), analysis The online version of this article contains supplemental material. of these regions from different extant vertebrates provides insight Abbreviations used in this article: chr, chromosome; FISH, fluorescence in situ hybrid- ization; huMHCpara,humanMHCpara; IgSF, Ig superfamily; L, long; LRR, leucine-rich into the evolutionary history of the MHC and its precursor. repeat; MHCpara,MHCparalogue;MHCtrans, translocated part of the MHC paralogous Previous work on the paralogous regions has focused only on region; NCBI, National Center for Biotechnology Information; NKC, NK complex; PIC, mammals. In this study, we took advantage of the published work in primordial immune complex; S, short; VLR, variable lymphocyte receptor. humans and focused on the genome of the amphibian Xenopus. Copyright Ó 2019 by The American Association of Immunologists, Inc. 0022-1767/19/$37.50 Previous studies showed that the Xenopus genome is relatively stable www.jimmunol.org/cgi/doi/10.4049/jimmunol.1900597 2 EMERGENCE OF Ag RECEPTORS AND MHC CLASS I INCLUDING CD1 and preserves some primordial features that were lost in other ver- content of the L chromosomes is most similar to the genome of tebrates (12), thus serving as a complementary model system to study the true diploid X. tropicalis. Although most housekeeping genome evolution. We used the true diploid Xenopus tropicalis (13) genes are present on both chromosomes, most class I (except a few and especially the tetraploid Xenopus laevis (14), in which the ge- class I–like genes), AgR, and AgR-like genes discussed in this report nomes have been recently sequenced and analyzed. In combination were diploidized and thus found only on the L chromosomes, and with comparative genomic analyses, we obtained evidence for the therefore we focused our analyses on the L chromosomes. timing of emergence of MHC class I/II and AgR genes. We further Xenopus MHC and identification of major and minor propose a model for the evolution of the human chr 1q21.1–23.3 MHCpara regions region, including the CD1 genes, and reflect on the dichotomy be- tween the jawed and jawless vertebrate adaptive immune systems. The Xenopus MHC was previously mapped by FISH to chr 8 (18) and now is precisely mapped to 8Lq21. To identify Xenopus MHCpara, we used sets of paralogous hallmark genes that were Materials and Methods originally used to identify the human MHCpara (huMHCpara) (3) Data mining (e.g., notch1, 2, 3, 4; pbx1, 2, 3, 4; rxra, b,
Load more

Recommended publications
  • Animal Evolution: Looking for the First Nervous System
    Dispatch R655 cellular or symbiotic functions, cannot genome reduction in the symbiont, 10. Nakabachi, A., Ishida, K., Hongoh, Y., Ohkuma, M., and Miyagishima, S. (2014). be lost without harmful or fatal results. HGT from various sources to the host Aphid gene of bacterial origin encodes a But these genes can be replaced, genome to maintain symbiont function, protein transported to an obligate and perhaps ever more easily as and now the targeting of protein endosymbiont. Curr. Biol. 24, R640–R641. 11. Moran, N.A., and Jarvik, T. (2010). Lateral the interaction networks of the products from host to symbiont has transfer of genes from fungi underlies endosymbiont reduce in complexity, even been found [4,10]. These make carotenoid production in aphids. Science 328, 624–627. thus reducing pressures on proteins clean separation of endosymbiont from 12. Jorgenson, M.A., Chen, Y., Yahashiri, A., to co-evolve. In a sense, when genes organelle more difficult to see, Popham, D.L., and Weiss, D.S. (2014). The are transferred from symbiont or prompting us not to look for the point bacterial septal ring protein RlpA is a lytic transglycosylase that contributes to rod organelle to the host nuclear genome when a symbiont ‘becomes’ an shape and daughter cell separation in and their proteins targeted back, this is organelle, but rather to ask, ‘Is there Pseudomonas aeruginosa. Mol. Microbiol. 93, 113–128. a compensatory change [4,9,14,17]. really anything so special about 13. Acuna, R., Padilla, B.E., Florez-Ramos, C.P., But other compensatory transfers that organelles?’ Rubio, J.D., Herrera, J.C., Benavides, P., affect a symbiont or organelle can also Lee, S.J., Yeats, T.H., Egan, A.N., Doyle, J.J., et al.
    [Show full text]
  • Basal Metazoans - Dirk Erpenbeck, Simion Paul, Michael Manuel, Paulyn Cartwright, Oliver Voigt and Gert Worheide
    EVOLUTION OF PHYLOGENETIC TREE OF LIFE - Basal Metazoans - Dirk Erpenbeck, Simion Paul, Michael Manuel, Paulyn Cartwright, Oliver Voigt and Gert Worheide BASAL METAZOANS Dirk Erpenbeck Ludwig-Maximilians Universität München, Germany Simion Paul and Michaël Manuel Université Pierre et Marie Curie in Paris, France. Paulyn Cartwright University of Kansas USA. Oliver Voigt and Gert Wörheide Ludwig-Maximilians Universität München, Germany Keywords: Metazoa, Porifera, sponges, Placozoa, Cnidaria, anthozoans, jellyfishes, Ctenophora, comb jellies Contents 1. Introduction on ―Basal Metazoans‖ 2. Phylogenetic relationships among non-bilaterian Metazoa 3. Porifera (Sponges) 4. Placozoa 5. Ctenophora (Comb-jellies) 6. Cnidaria 7. Cultural impact and relevance to human welfare Glossary Bibliography Biographical Sketch Summary Basal metazoans comprise the four non-bilaterian animal phyla Porifera (sponges), Cnidaria (anthozoans and jellyfishes), Placozoa (Trichoplax) and Ctenophora (comb jellies). The phylogenetic position of these taxa in the animal tree is pivotal for our understanding of the last common metazoan ancestor and the character evolution all Metazoa,UNESCO-EOLSS but is much debated. Morphological, evolutionary, internal and external phylogenetic aspects of the four phyla are highlighted and discussed. SAMPLE CHAPTERS 1. Introduction on “Basal Metazoans” In many textbooks the term ―lower metazoans‖ still refers to an undefined assemblage of invertebrate phyla, whose phylogenetic relationships were rather undefined. This assemblage may contain both bilaterian and non-bilaterian taxa. Currently, ―Basal Metazoa‖ refers to non-bilaterian animals only, four phyla that lack obvious bilateral symmetry, Porifera, Placozoa, Cnidaria and Ctenophora. ©Encyclopedia of Life Support Systems (EOLSS) EVOLUTION OF PHYLOGENETIC TREE OF LIFE - Basal Metazoans - Dirk Erpenbeck, Simion Paul, Michael Manuel, Paulyn Cartwright, Oliver Voigt and Gert Worheide These four phyla have classically been known as ―diploblastic‖ Metazoa.
    [Show full text]
  • Animal Evolution: Trichoplax, Trees, and Taxonomic Turmoil
    View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Dispatch R1003 Dispatches Animal Evolution: Trichoplax, Trees, and Taxonomic Turmoil The genome sequence of Trichoplax adhaerens, the founding member of the into the same major classes (C, E/F enigmatic animal phylum Placozoa, has revealed that a surprising level of and B) as do those described from genetic complexity underlies its extremely simple body plan, indicating either Amphimedon [4]. Consistent with that placozoans are secondarily simple or that there is an undiscovered a more derived position, however, morphologically complex life stage. Trichoplax has a number of Antp superclass Hox genes that are absent David J. Miller1 and Eldon E. Ball2 but no other axial differentiation, from the sponge Amphimedon. resembling an amoeba. Grell [3] who These include the ‘ParaHox’ gene With the recent or imminent release formally described these common but Trox-2 [5] and the extended Hox of the whole genome sequences of inconspicuous marine organisms as family gene Not [6] known from a number of key animal species, this belonging to a new phylum, assumed previous work. Particularly intriguing is an exciting time for the ‘evo-devo’ that their simplicity is primary, and is the discovery in Trichoplax of many community. In the last twelve months, that they therefore must represent genes associated with neuroendocrine whole genome analyses of the a key stage in animal evolution. This function across the Bilateria; in cnidarian Nematostella vectensis, view is still held by several prominent common with Amphimedon [7], many the choanoflagellate Monosiga Trichoplax biologists, but has always elements of the post-synaptic scaffold brevicollis and the cephalochordate been contentious; the view that it is are present, but so too are channel Branchiostoma floridae (commonly derived from a more complex ancestor and receptor proteins not known from known as amphioxus) have been has recently been gaining momentum sponges.
    [Show full text]
  • Implications for Proteasome Nuclear Localization Revealed by the Structure of the Nuclear Proteasome Tether Protein Cut8
    Implications for proteasome nuclear localization revealed by the structure of the nuclear proteasome tether protein Cut8 Kojiro Takedaa, Nam K. Tonthatb, Tiffany Gloverc, Weijun Xuc, Eugene V. Koonind, Mitsuhiro Yanagidaa, and Maria A. Schumacherb,1 aG0 Cell Unit; Okinawa Institute of Science and Technology (OIST); 1919-1 Tancha, Onna, Okinawa, Japan; bDepartment of Biochemistry, Duke University Medical Center, Room 243A Nanaline H. Duke Building, Box 3711, Durham, NC 27710; cDepartment of Biochemistry and Molecular Biology, University of Texas M. D. Anderson Cancer Center, Unit 1000, Houston, TX 77030; and dNational Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20892 Edited by Axel T. Brunger, Stanford University, Stanford, CA, and approved August 29, 2011 (received for review March 7, 2011) Degradation of nuclear proteins by the 26S proteasome is essential ultimately found to be a delay in the destruction of the mitotic for cell viability. In yeast, the nuclear envelope protein Cut8 med- cyclin and securin (13). However, the polyubiquitination of these iates nuclear proteasomal sequestration by an uncharacterized proteins was normal, suggesting a role for the proteasome. Sub- mechanism. Here we describe structures of Schizosaccharomyces sequent studies showed that Cut8 is responsible for sequestering pombe Cut8, which shows that it contains a unique, modular the 26S proteasome to the nucleus (10, 11). Cut8 was found to be fold composed of an extended N-terminal, lysine-rich segment localized to the nuclear envelope and overlapping the location that when ubiquitinated binds the proteasome, a dimer domain of the proteasome (17–21). An interaction between Cut8 and followed by a six-helix bundle connected to a flexible C tail.
    [Show full text]
  • Expression of Immunoproteasome Genes Is Regulated by Cell-Intrinsic
    www.nature.com/scientificreports OPEN Expression of immunoproteasome genes is regulated by cell-intrinsic and –extrinsic factors in human Received: 06 April 2016 Accepted: 06 September 2016 cancers Published: 23 September 2016 Alexandre Rouette1,2,*, Assya Trofimov1,2,3,*, David Haberl1, Geneviève Boucher1, Vincent-Philippe Lavallée1,2,4,5, Giovanni D’Angelo4,5, Josée Hébert1,2,4,5, Guy Sauvageau1,2,4,5, Sébastien Lemieux1,3 & Claude Perreault1,2,4 Based on transcriptomic analyses of thousands of samples from The Cancer Genome Atlas, we report that expression of constitutive proteasome (CP) genes (PSMB5, PSMB6, PSMB7) and immunoproteasome (IP) genes (PSMB8, PSMB9, PSMB10) is increased in most cancer types. In breast cancer, expression of IP genes was determined by the abundance of tumor infiltrating lymphocytes and high expression of IP genes was associated with longer survival. In contrast, IP upregulation in acute myeloid leukemia (AML) was a cell-intrinsic feature that was not associated with longer survival. Expression of IP genes in AML was IFN-independent, correlated with the methylation status of IP genes, and was particularly high in AML with an M5 phenotype and/or MLL rearrangement. Notably, PSMB8 inhibition led to accumulation of polyubiquitinated proteins and cell death in IPhigh but not IPlow AML cells. Co-clustering analysis revealed that genes correlated with IP subunits in non-M5 AMLs were primarily implicated in immune processes. However, in M5 AML, IP genes were primarily co-regulated with genes involved in cell metabolism and proliferation, mitochondrial activity and stress responses. We conclude that M5 AML cells can upregulate IP genes in a cell-intrinsic manner in order to resist cell stress.
    [Show full text]
  • The Phylogeography of the Placozoa Suggests a Taxonrich Phylum In
    Molecular Ecology (2010) 19, 2315–2327 doi: 10.1111/j.1365-294X.2010.04617.x The phylogeography of the Placozoa suggests a taxon-rich phylum in tropical and subtropical waters M. EITEL* and B. SCHIERWATER*† *Tiera¨rztliche Hochschule Hannover, ITZ, Ecology and Evolution, Bu¨nteweg 17d, D-30559 Hannover, Germany, †American Museum of Natural History, New York, Division of Invertebrate Zoology, 79 St at Central Park West, New York, NY 10024, USA Abstract Placozoa has been a key phylum for understanding early metazoan evolution. Yet this phylum is officially monotypic and with respect to its general biology and ecology has remained widely unknown. Worldwide sampling and sequencing of the mitochondrial large ribosomal subunit (16S) reveals a cosmopolitan distribution in tropical and subtropical waters of genetically different clades. We sampled a total of 39 tropical and subtropical locations worldwide and found 23 positive sites for placozoans. The number of genetically characterized sites was thereby increased from 15 to 37. The new sampling identified the first genotypes from two new oceanographic regions, the Eastern Atlantic and the Indian Ocean. We found seven out of 11 previously known haplotypes as well as five new haplotypes. One haplotype resembles a new genetic clade, increasing the number of clades from six to seven. Some of these clades seem to be cosmopolitan whereas others appear to be endemic. The phylogeography also shows that different clades occupy different ecological niches and identifies several euryoecious haplotypes with a cosmopolitic distribution as well as some stenoecious haplotypes with an endemic distribution. Haplotypes of different clades differ substantially in their phylogeographic distribution according to latitude.
    [Show full text]
  • Biophysical Analyses of the Oxygen Sensing Prolyl Hydroxylase from the Simplest Animal Trichoplax Adhaerens
    Journal name: Hypoxia Article Designation: Original Research Year: 2018 Volume: 6 Hypoxia Dovepress Running head verso: Lippl et al Running head recto: Biophysical analyses of the oxygen sensing PHDs from the simplest animal T. adhaerens open access to scientific and medical research DOI: http://dx.doi.org/10.2147/HP.S174655 Open Access Full Text Article ORIGINAL RESEARCH Born to sense: biophysical analyses of the oxygen sensing prolyl hydroxylase from the simplest animal Trichoplax adhaerens Kerstin Lippl Background: In humans and other animals, the chronic hypoxic response is mediated by Anna Boleininger hypoxia inducible transcription factors (HIFs) which regulate the expression of genes that Michael A McDonough counteract the effects of limiting oxygen. Prolyl hydroxylases (PHDs) act as hypoxia sensors Martine I Abboud for the HIF system in organisms ranging from humans to the simplest animal Trichoplax Hanna Tarhonskaya adhaerens. We report structural and biochemical studies on the T. adhaerens HIF prolyl hydroxy- Rasheduzzaman Chowdhury Methods: lase (TaPHD) that inform about the evolution of hypoxia sensing in animals. Christoph Loenarz Results: High resolution crystal structures (≤1.3 Å) of TaPHD, with and without its HIFα Christopher J Schofield substrate, reveal remarkable conservation of key active site elements between T. adhaerens and Chemistry Research Laboratory, human PHDs, which also manifest in kinetic comparisons. University of Oxford, Oxford, UK Conclusion: Conserved structural features of TaPHD and human PHDs include those appar- ently enabling the slow binding/reaction of oxygen with the active site Fe(II), the formation of a stable 2-oxoglutarate complex, and a stereoelectronically promoted change in conformation of the hydroxylated proline-residue.
    [Show full text]
  • Systema Naturae. the Classification of Living Organisms
    Systema Naturae. The classification of living organisms. c Alexey B. Shipunov v. 5.601 (June 26, 2007) Preface Most of researches agree that kingdom-level classification of living things needs the special rules and principles. Two approaches are possible: (a) tree- based, Hennigian approach will look for main dichotomies inside so-called “Tree of Life”; and (b) space-based, Linnaean approach will look for the key differences inside “Natural System” multidimensional “cloud”. Despite of clear advantages of tree-like approach (easy to develop rules and algorithms; trees are self-explaining), in many cases the space-based approach is still prefer- able, because it let us to summarize any kinds of taxonomically related da- ta and to compare different classifications quite easily. This approach also lead us to four-kingdom classification, but with different groups: Monera, Protista, Vegetabilia and Animalia, which represent different steps of in- creased complexity of living things, from simple prokaryotic cell to compound Nature Precedings : doi:10.1038/npre.2007.241.2 Posted 16 Aug 2007 eukaryotic cell and further to tissue/organ cell systems. The classification Only recent taxa. Viruses are not included. Abbreviations: incertae sedis (i.s.); pro parte (p.p.); sensu lato (s.l.); sedis mutabilis (sed.m.); sedis possi- bilis (sed.poss.); sensu stricto (s.str.); status mutabilis (stat.m.); quotes for “environmental” groups; asterisk for paraphyletic* taxa. 1 Regnum Monera Superphylum Archebacteria Phylum 1. Archebacteria Classis 1(1). Euryarcheota 1 2(2). Nanoarchaeota 3(3). Crenarchaeota 2 Superphylum Bacteria 3 Phylum 2. Firmicutes 4 Classis 1(4). Thermotogae sed.m. 2(5).
    [Show full text]
  • Global Diversity of the Placozoa
    Review Global Diversity of the Placozoa Michael Eitel1,2*, Hans-Ju¨ rgen Osigus1, Rob DeSalle3, Bernd Schierwater1,3,4 1 Stiftung Tiera¨rztliche Hochschule Hannover, Institut fu¨r Tiero¨kologie und Zellbiologie, Ecology and Evolution, Hannover, Germany, 2 The Swire Institute of Marine Science, Faculty of Science, School of Biological Sciences, The University of Hong Kong, Hong Kong, 3 Sackler Institute for Comparative Genomics and Division of Invertebrate Zoology, American Museum of Natural History, New York, New York, United States of America, 4 Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, Connecticut, United States of America ‘Urmetazoon’ ([7,33]; for a historical summary of placozoan Abstract: The enigmatic animal phylum Placozoa holds a research see [34–36]). More than a century after the discovery of key position in the metazoan Tree of Life. A simple Trichoplax adhaerens the phylum status of the Placozoa – as bauplan makes it appear to be the most basal metazoan envisioned by Schulze – was finally accepted. known and genetic evidence also points to a position It is important to note that animals described as Trichoplax close to the last common metazoan ancestor. Trichoplax adhaerens in Grell and colleagues’ studies might, although being adhaerens is the only formally described species in the morphologically highly similar to Schulze’s Trichoplax, actually phylum to date, making the Placozoa the only monotypic phylum in the animal kingdom. However, recent molec- belong to a different species. Given our current knowledge of ular genetic as well as morphological studies have placozoan diversity (see below) it is evident that the various studies identified a high level of diversity, and hence a potential of placozoans accomplished over the years have pooled a broad high level of taxonomic diversity, within this phylum.
    [Show full text]
  • The Evolution of the Mitochondrial Genomes of Calcareous Sponges and Cnidarians Ehsan Kayal Iowa State University
    Iowa State University Capstones, Theses and Graduate Theses and Dissertations Dissertations 2012 The evolution of the mitochondrial genomes of calcareous sponges and cnidarians Ehsan Kayal Iowa State University Follow this and additional works at: https://lib.dr.iastate.edu/etd Part of the Evolution Commons, and the Molecular Biology Commons Recommended Citation Kayal, Ehsan, "The ve olution of the mitochondrial genomes of calcareous sponges and cnidarians" (2012). Graduate Theses and Dissertations. 12621. https://lib.dr.iastate.edu/etd/12621 This Dissertation is brought to you for free and open access by the Iowa State University Capstones, Theses and Dissertations at Iowa State University Digital Repository. It has been accepted for inclusion in Graduate Theses and Dissertations by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. The evolution of the mitochondrial genomes of calcareous sponges and cnidarians by Ehsan Kayal A dissertation submitted to the graduate faculty in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Major: Ecology and Evolutionary Biology Program of Study Committee Dennis V. Lavrov, Major Professor Anne Bronikowski John Downing Eric Henderson Stephan Q. Schneider Jeanne M. Serb Iowa State University Ames, Iowa 2012 Copyright 2012, Ehsan Kayal ii TABLE OF CONTENTS ABSTRACT ..........................................................................................................................................
    [Show full text]
  • A Self-Marker-Like Protein Governs Hemocyte Allorecognition In
    Ema et al. Zoological Letters (2019) 5:34 https://doi.org/10.1186/s40851-019-0149-8 RESEARCH ARTICLE Open Access A self-marker-like protein governs hemocyte allorecognition in Halocynthia roretzi Masaki Ema1†, Taizo Okada1†, Miki Takahashi1†, Masato Uchiyama1†, Hideo Kubo2, Hideaki Moriyama3, Hitoshi Miyakawa4 and Midori Matsumoto1* Abstract Background: Self-incompatibility, fusion/non-fusion reactions, and contact reactions (CRs) have all been identified as allorecognition phenomena in ascidians. CR is a reaction characteristic of the hemocytes of Halocynthia roretzi, whereby they release phenol oxidase (PO) upon contact with non-self hemocytes. Thus, these cells may represent a primitive form of the vertebrate immune system. In the present study, we focused on the CR of H. roretzi hemocytes and sought to identify self-marker proteins that distinguish between self and non-self cells. Results: We initially generated a CR-inducing monoclonal antibody against the complete hemocyte membrane- protein complement (mAb11B16B10). This antibody was identified based on the differential induction of PO activity in individual organisms. The level of PO activity induced by this antibody in individual ascidians was consistent with the observed CR-induced PO activity. mAb11B16B10 recognized a series of 12 spots corresponding to a 100-kDa protein, with differing isoelectric points (pIs). A comparison of the 2D electrophoresis gels of samples from CR- reactive/non-reactive individuals revealed that some spots in this series in hemocytes were common to the CR- non-inducible individuals, but not to CR-inducible individuals. We cloned the corresponding gene and named it Halocynthia roretzi self-marker-like protein-1 (HrSMLP1). This gene is similar to the glycoprotein DD3–3 found in Dictyostelium, and is conserved in invertebrates.
    [Show full text]
  • Lack of Activity of Recombinant HIF Prolyl Hydroxylases
    RESEARCH ARTICLE Lack of activity of recombinant HIF prolyl hydroxylases (PHDs) on reported non-HIF substrates Matthew E Cockman1†*, Kerstin Lippl2†, Ya-Min Tian3†, Hamish B Pegg1, William D Figg Jnr2, Martine I Abboud2, Raphael Heilig4, Roman Fischer4, Johanna Myllyharju5‡, Christopher J Schofield2‡, Peter J Ratcliffe1,3‡* 1The Francis Crick Institute, London, United Kingdom; 2Chemistry Research Laboratory, Department of Chemistry, University of Oxford, Oxford, United Kingdom; 3Ludwig Institute for Cancer Research, Nuffield Department of Clinical Medicine, University of Oxford, Oxford, United Kingdom; 4Target Discovery Institute, Nuffield Department of Clinical Medicine, University of Oxford, Oxford, United Kingdom; 5Oulu Center for Cell-Matrix Research, Biocenter Oulu and Faculty of Biochemistry and Molecular Medicine, University of Oulu, Oulu, Finland Abstract Human and other animal cells deploy three closely related dioxygenases (PHD 1, 2 and 3) to signal oxygen levels by catalysing oxygen regulated prolyl hydroxylation of the transcription factor HIF. The discovery of the HIF prolyl-hydroxylase (PHD) enzymes as oxygen sensors raises a key question as to the existence and nature of non-HIF substrates, potentially transducing other biological responses to hypoxia. Over 20 such substrates are reported. We therefore sought to *For correspondence: characterise their reactivity with recombinant PHD enzymes. Unexpectedly, we did not detect [email protected] prolyl-hydroxylase activity on any reported non-HIF protein or peptide, using conditions supporting (MEC); robust HIF-a hydroxylation. We cannot exclude PHD-catalysed prolyl hydroxylation occurring under [email protected] (PJR) conditions other than those we have examined. However, our findings using recombinant enzymes †These authors contributed provide no support for the wide range of non-HIF PHD substrates that have been reported.
    [Show full text]