DOCSLIB.ORG

Myd88-Deficient Hydra Reveal an Ancient Function of TLR Signaling In

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
Myd88-Deficient Hydra Reveal an Ancient Function of TLR Signaling In MyD88-deficient Hydra reveal an ancient function of TLR signaling in sensing bacterial colonizers Sören Franzenburga,1, Sebastian Fraunea,1,2, Sven Künzelb, John F. Bainesb,c, Tomislav Domazet-Losoa, and Thomas C. G. Boscha,2 aZoological Institute, Christian Albrechts University, 24098 Kiel, Germany; bMax Planck Institute for Evolutionary Biology, 24306 Plön, Germany; and cInstitute for Experimental Medicine, Christian Albrechts University, 24105 Kiel, Germany Edited by Nancy A. Moran, Yale University, West Haven, CT, and approved October 4, 2012 (received for review August 13, 2012) Toll-like receptor (TLR) signaling is one of the most important Vertebrate homologs of Toll, the TLRs, are receptors of the signaling cascades of the innate immune system of vertebrates. immune system. Vertebrate TLRs are involved in eliminating Studies in invertebrates have focused on the fruit fly Drosophila pathogens and controlling commensal colonization (1, 14, 15) by melanogaster and the nematode Caenorhabditis elegans,and recognizing conserved microbe-associated molecular patterns there is little information regarding the evolutionary origin and (MAMPs) including lipopolysaccharides, flagellin, and peptido- ancestral function of TLR signaling. In Drosophila, members of the glycans (1, 16). Therefore, it was proposed that immune function κ Toll-like receptor family are involved in both embryonic develop- of TLR signaling involving NF- B and MyD88 has evolved ment and innate immunity. In C. elegans, a clear immune function within the bilaterians (17). However, recent genome projects in of the TLR homolog TOL-1 is controversial and central components the nonbilaterians Hydra magnipapillata (18) and Nematostella vectensis (19) revealed the presence of TLRs, MyD88, and NF- of vertebrate TLR signaling including the key adapter protein my- κ eloid differentiation primary response gene 88 (MyD88) and the B (20, 21). Their role in bacterial recognition and innate im- transcription factor NF-κB are not present. In basal metazoans such munity, however, remains to be shown (22). Cnidaria are a sister as the cnidarians Hydra magnipapillata and Nematostella vectensis, group to the Bilateria (19) and one of the earliest branches in the animal tree of life (Fig. 1A). The recent genome project of the all components of the vertebrate TLR signaling cascade are present, cnidarian H. magnipapillata identified a conserved TLR-signaling but their role in immunity is unknown. Here, we use a MyD88 loss- cascade (21, 23) (Fig. 1B and Table S1), making Hydra a suitable of-function approach in Hydra to demonstrate that recognition of model for addressing questions of the ancestral function of TLR bacteria is an ancestral function of TLR signaling and that this signaling. Is the TLR pathway involved in the defense against process contributes to both host-mediated recolonization by com- bacterial pathogens or in maintaining specific host–microbe mensal bacteria as well as to defense against bacterial pathogens. interactions? Does it affect the mechanisms and routes by which functionally diverse bacteria colonize their host? Is it involved in oll-like receptors (TLRs) are conserved throughout animal developmental processes such as axis formation? To gain insight Tevolution but appear to serve different functions in different into these questions, we performed MyD88 loss-of-function ex- model organisms. TLRs are transmembrane receptors with ex- periments in Hydra vulgaris [AEP strain (24)]. We used a com- tracellular leucin-rich repeat (LRR) motifs and an intracellular bination of microarray-based gene expression screening and 16S Toll/interleukin-1 receptor (TIR) domain. Upon stimulation of rRNA-gene sequencing to detect changes in both the Hydra tran- TLRs, the key adapter protein MyD88 associates with the cyto- scriptome and the associated microbiota. Further, we investigated solic part of the TLR through a homophilic interaction of the TIR the role of TLR signaling in pathogen defense against Pseudo- domains and then recruits the IL-1R–associated kinase (IRAK), monas aeruginosa. The patterns of differentially regulated host which subsequently associates with the TNFR-associated factor genes as well as changes in the bacterial colonization process and (TRAF). TRAF recruits the TGF-β activated kinase 1 (TAK1). pathogen susceptibility in MyD88-knockdown polyps point to a The kinase TAK1 induces a phosphorylation cascade finally leading role of TLR signaling in sensing of bacteria, be it associated com- to the nuclear translocation of the transcription factors NF-κB via mensals or pathogens. Thus, this functional analysis clearly identi- the inhibitor of kappa B-kinase (IKK) signalosome or c-Jun via the fies a role of TLR signaling in innate immunity in an animal at the c-Jun N-terminal kinase (JNK)/p38 branch of TLR signaling (1). base of metazoan evolution. The Toll pathway was initially identified to be essential in early embryonic development in Drosophila (2). In addition to its cru- Results – − cial role in the establishment of the dorsal ventral axis, Drosophila Generation of MyD88-Knockdown (MyD88 ) H. vulgaris (AEP). To ana- Toll was shown to be involved in muscle development (3) and lyze the function of TLR signaling in the basal metazoan Hydra, heart formation (4). Later on, it was discovered that Toll signaling we generated a stable transgenic H. vulgaris (AEP) line with in Drosophila also contributes to defense reactions against bac- drastically reduced expression levels of the universal adapter teria as well as to antifungal defense by regulating, among others, the expression of the antifungal peptide drosomycin in adult flies (5, 6). Further immunity functions have been identified for Toll- Author contributions: S. Franzenburg, S. Fraune, and T.C.G.B. designed research; S. Franzenburg 7 (7) and Toll-8 (8). Studies in the mosquito Aedes aegypti also and S. Fraune performed research; S.K. and J.F.B. contributed new reagents/analytic identified MyD88-dependent Toll signaling to mediate immune tools; S. Franzenburg, S. Fraune, and T.D.-L. analyzed data; and S. Franzenburg, S. Fraune, defenses against dengue viruses (9). One other invertebrate and T.C.G.B. wrote the paper. model system, the nematode Caenorhabditis elegans lacks central The authors declare no conflict of interest. proteins of the canonical TLR-signaling cascade (10). Only one This article is a PNAS Direct Submission. Toll homolog, termed TOL-1, was identified in C. elegans (10). Data deposition: The microarray data reported in this paper have been deposited in the The fact that TOL-1 mutants show strong developmental defects Gene Expression Omnibus (GEO) database, www.ncbi.nlm.nih.gov/geo (accession no. despite mutants for the putative signaling cascade displaying no GSE32383); and the 16S 454 data are deposited at the metagenome analysis server MG- developmental abnormalities led to the belief that TOL-1 in C. RAST (Project ID 1719). elegans might function as a cell–cell adhesion protein in neurons 1S. Franzenburg and S. Fraune contributed equally to this work. (10). Other reports state an additional involvement of TOL-1 in 2To whom correspondence may be addressed. E-mail: [email protected] or pathogen defense (11). In addition, a TIR-domain–containing [email protected]. protein called tir-1 is required for resistance to fungal and bac- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. terial infection in C. elegans (12, 13). 1073/pnas.1213110109/-/DCSupplemental. 19374–19379 | PNAS | November 20, 2012 | vol. 109 | no. 47 www.pnas.org/cgi/doi/10.1073/pnas.1213110109 Downloaded by guest on September 24, 2021 Neither line displayed any obvious developmental or behavioral abnormalities. Absence of Bacteria as Well as MyD88 Deficiency Influence Central Parts of the TLR-Signaling Cascade. To assess the transcriptional consequences of a MyD88 knockdown and identify potential downstream effector genes of the TLR-signaling cascade, we per- − formed microarray analyses. Expression levels of both MyD88 polyps as well as germ-free polyps (Fig. 1G) were compared with − control polyps. The MyD88 polyps combined with the germ- free polyps provided unique resources that allowed us to directly investigate the connection between TLR signaling and the reg- ulation of associated bacterial diversity. Statistical analysis was carried out by ANOVA with Student–Newman–Keuls (SNK) post hoc tests and false discovery rate (FDR) correction. The microarray data independently validate the successful MyD88 knockdown. Contig 11552, encoding for MyD88, shows a 4.29- − fold down-regulation (P < 0.001) in MyD88 polyps and is not differentially expressed in germ-free polyps (fold change 1.09, N.S.) (Table S1). To check for transcriptional changes of other putative members of the TLR cascade, the H. vulgaris (AEP) transcriptome (29) was screened for homologs of previously described members of the pathway. The majority of central cascade members are present in H. vulgaris (AEP) (Fig. 1A and Table S1). Various central components of the putative TLR cascade including members of the TRAF family of ubiquitin protein ligases, the kinase TAK1, MAP-kinase p38, and the JNK inhibitor JSP-1 show significantly decreased expression in germ-free and/or MyD88-deficient conditions (Table S1). We hypothesize therefore the existence of positive feedback loops of the putative effector transcription factors NF-κBandc-Jun on certain upstream pathway components, pointing toward a functional unity of
Load more

Recommended publications
  • The Polyp and the Medusa Life on the Move
    The Polyp and the Medusa Life on the Move Millions of years ago, unlikely pioneers sparked a revolution. Cnidarians set animal life in motion. So much of what we take for granted today began with Cnidarians. FROM SHAPE OF LIFE The Polyp and the Medusa Life on the Move Take a moment to follow these instructions: Raise your right hand in front of your eyes. Make a fist. Make the peace sign with your first and second fingers. Make a fist again. Open your hand. Read the next paragraph. What you just did was exhibit a trait we associate with all animals, a trait called, quite simply, movement. And not only did you just move your hand, but you moved it after passing the idea of movement through your brain and nerve cells to command the muscles in your hand to obey. To do this, your body needs muscles to move and nerves to transmit and coordinate movement, whether voluntary or involuntary. The bit of business involved in making fists and peace signs is pretty complex behavior, but it pales by comparison with the suites of thought and movement associated with throwing a curve ball, walking, swimming, dancing, breathing, landing an airplane, running down prey, or fleeing a predator. But whether by thought or instinct, you and all animals except sponges have the ability to move and to carry out complex sequences of movement called behavior. In fact, movement is such a basic part of being an animal that we tend to define animalness as having the ability to move and behave.
    [Show full text]
  • Course Outline for Biology Department Adeyemi College of Education
    COURSE CODE: BIO 111 COURSE TITLE: Basic Principles of Biology COURSE OUTLINE Definition, brief history and importance of science Scientific method:- Identifying and defining problem. Raising question, formulating Hypotheses. Designing experiments to test hypothesis, collecting data, analyzing data, drawing interference and conclusion. Science processes/intellectual skills: (a) Basic processes: observation, Classification, measurement etc (b) Integrated processes: Science of Biology and its subdivisions: Botany, Zoology, Biochemistry, Microbiology, Ecology, Entomology, Genetics, etc. The Relevance of Biology to man: Application in conservation, agriculture, Public Health, Medical Sciences etc Relation of Biology to other science subjects Principles of classification Brief history of classification nomenclature and systematic The 5 kingdom system of classification Living and non-living things: General characteristics of living things. Differences between plants and animals. COURSE OUTLINE FOR BIOLOGY DEPARTMENT ADEYEMI COLLEGE OF EDUCATION COURSE CODE: BIO 112 COURSE TITLE: Cell Biology COURSE OUTLINE (a) A brief history of the concept of cell and cell theory. The structure of a generalized plant cell and generalized animal cell, and their comparison Protoplasm and its properties. Cytoplasmic Organelles: Definition and functions of nucleus, endoplasmic reticulum, cell membrane, mitochondria, ribosomes, Golgi, complex, plastids, lysosomes and other cell organelles. (b) Chemical constituents of cell - salts, carbohydrates, proteins, fats
    [Show full text]
  • Hydra Effects in Stable Communities and Their Implications for System Dynamics
    Ecology, 97(5), 2016, pp. 1135–1145 © 2016 by the Ecological Society of America Hydra effects in stable communities and their implications for system dynamics MICHAEL H. CORTEZ,1,3 AND PETER A. ABRAMS2 1Department of Mathematics and Statistics, Utah State University, Logan, Utah 84322, USA 2Department of Ecology and Evolutionary Biology, University of Toronto, 25 Harbord St., Toronto, ON M5S 3G5, Canada Abstract. A hydra effect occurs when the mean density of a species increases in response to greater mortality. We show that, in a stable multispecies system, a species exhibits a hydra effect only if maintaining that species at its equilibrium density destabilizes the system. The stability of the original system is due to the responses of the hydra-effect species to changes in the other species’ densities. If that dynamical feedback is removed by fixing the density of the hydra-effect species, large changes in the community make-up (including the possibility of species extinction) can occur. This general result has several implications: (1) Hydra effects occur in a much wider variety of species and interaction webs than has previously been described, and may occur for multiple species, even in small webs; (2) conditions for hydra effects caused by predators (or diseases) often differ from those caused by other mortality factors; (3) introducing a specialist or a switching predator of a hydra-effect species often causes large changes in the community, which frequently involve extinction of other species; (4) harvest policies that attempt to maintain a constant density of a hydra-effect species may be difficult to implement, and, if successful, are likely to cause large changes in the densities of other species; and (5) trophic cascades and other indirect effects caused by predators of hydra-effect species can exhibit amplification of effects or unexpected directions of change.
    [Show full text]
  • How to Use Hydra As a Model System to Teach Biology in the Classroom PATRICIA BOSSERT1 and BRIGITTE GALLIOT*,2
    Int. J. Dev. Biol. 56: 637-652 (2012) doi: 10.1387/ijdb.123523pb www.intjdevbiol.com How to use Hydra as a model system to teach biology in the classroom PATRICIA BOSSERT1 and BRIGITTE GALLIOT*,2 1University of Stony Brook, New York, USA and 2 Department of Genetics and Evolution, University of Geneva, Switzerland ABSTRACT As scientists it is our duty to fight against obscurantism and loss of rational thinking if we want politicians and citizens to freely make the most intelligent choices for the future gen- erations. With that aim, the scientific education and training of young students is an obvious and urgent necessity. We claim here that Hydra provides a highly versatile but cheap model organism to study biology at any age. Teachers of biology have the unenviable task of motivating young people, who with many other motivations that are quite valid, nevertheless must be guided along a path congruent with a ‘syllabus’ or a ‘curriculum’. The biology of Hydra spans the history of biology as an experimental science from Trembley’s first manipulations designed to determine if the green polyp he found was plant or animal to the dissection of the molecular cascades underpinning, regenera- tion, wound healing, stemness, aging and cancer. It is described here in terms designed to elicit its wider use in classrooms. Simple lessons are outlined in sufficient detail for beginners to enter the world of ‘Hydra biology’. Protocols start with the simplest observations to experiments that have been pretested with students in the USA and in Europe. The lessons are practical and can be used to bring ‘life’, but also rational thinking into the study of life for the teachers of students from elementary school through early university.
    [Show full text]
  • OREGON ESTUARINE INVERTEBRATES an Illustrated Guide to the Common and Important Invertebrate Animals
    OREGON ESTUARINE INVERTEBRATES An Illustrated Guide to the Common and Important Invertebrate Animals By Paul Rudy, Jr. Lynn Hay Rudy Oregon Institute of Marine Biology University of Oregon Charleston, Oregon 97420 Contract No. 79-111 Project Officer Jay F. Watson U.S. Fish and Wildlife Service 500 N.E. Multnomah Street Portland, Oregon 97232 Performed for National Coastal Ecosystems Team Office of Biological Services Fish and Wildlife Service U.S. Department of Interior Washington, D.C. 20240 Table of Contents Introduction CNIDARIA Hydrozoa Aequorea aequorea ................................................................ 6 Obelia longissima .................................................................. 8 Polyorchis penicillatus 10 Tubularia crocea ................................................................. 12 Anthozoa Anthopleura artemisia ................................. 14 Anthopleura elegantissima .................................................. 16 Haliplanella luciae .................................................................. 18 Nematostella vectensis ......................................................... 20 Metridium senile .................................................................... 22 NEMERTEA Amphiporus imparispinosus ................................................ 24 Carinoma mutabilis ................................................................ 26 Cerebratulus californiensis .................................................. 28 Lineus ruber .........................................................................
    [Show full text]
  • Freshwater Jellyfish
    Freshwater Jellyfish Craspedacusta sowerbyi www.seagrant.psu.edu Species at a Glance While similar in appearance to its saltwater relative, the freshwater jellyfish is actually considered a member of the hydra family, and not a “true” jellyfish. It is widespread around the world and has been in the United States since the early 1900’s. Even though this jellyfish uses stinging cells to capture prey, these stingers are too small to penetrate Map courtesy of United States human skin and are not considered a threat to people. Geological Survey. FRESHWATER JELLYFISH Species Description Craspedacusta sowerbyi The freshwater jellyfish exists in two main forms throughout its life. In the juvenile phase, it is a small, 1 mm long gelatinous polyp that lacks tentacles. In this phase the jellyfish attaches to hard surfaces and forms colonies. The freshwater jellyfish is most easily identified in its adult phase, as it has many of the characteristics of a true jellyfish such as a small, bell-shaped transparent body that is 5-25 mm in diameter. A whorl of string-like tentacles surround the circular edge of the body in sets of three to seven. The tentacles contain hundreds of specialized stinging cells that aid in capturing prey and protecting against predators. Native HUCs HUC 8 Level Record Native & Introduced Ranges HUC 6 Level Record Non-specific State Record Originally from the Yangtze River valley in China, the fresh- Map created on 8/5/2017. water jellyfish can now be found on all continents worldwide. It was first reported in the United States in the early 1900’s, presumably introduced with the transport of stocked fish and aquatic plants.
    [Show full text]
  • H Size Determination in Hydra: the Roles of Growth and Budding
    t /. Embryol. exp. Morph. Vol. 30, l,pp. 1-19, 1973 Printed in Great Britain h Size determination in Hydra: The roles K of growth and budding By JOHN W. BISBEE1 ^ From the Department of Biology, University of Pittsburgh r P SUMMARY \~ Hydra pseudoligactis cultured at 9 °C for 3-4 weeks are one-and-a-half times larger than ^ those cultured at 18 °C. The size of Hydra is correlated with the numbers of epithelio- muscular and digestive cells in the distal portion of the animal and with the diameters of the k- epithelio-muscular cells in the peduncle. [ Counts of mitotic figures and tritiated-thymidine-labeled nuclei and determinations of T increase in mass of Hydra populations suggest that the difference caused by these tempera- y. tures does not affect mitosis. At 9 °C buds are initiated at a lower rate and take longer to develop than at 18 °C. The surface-areas of buds raised at the two temperatures are similar. T Because Hydra raised at the two temperatures have similar growth dynamics, the differences u in sizes of the animals cannot be due to growth rate. The observed effect of temperature on bud initiation and development is probably relevant to the increased size of animals raised at 9 "C, since these larger animals may be accumulating more cells while losing fewer to buds. INTRODUCTION The shape and size of Hydra seems to be a consequence of several dynamic processes. Growth, budding, cell sloughing, cell migration, and mesogleal metabolism have possible roles in Hydra morphogenesis (Burnett, 1961, 1966; Burnett & Hausman, 1969; Brien & Reniers-Decoen, 1949; Campbell, 1965, 1967 a, b, c, 1968; Shostak, Patel & Burnett, 1965; Shostak & Globus, 1966; Shostak, 1968).
    [Show full text]
  • Hydra Magnipapillata
    A Proposal to Construct a BAC Library from Hydra magnipapillata Submitted by Robert E. Steele and Hans R. Bode University of California, Irvine The importance of the organism to biomedical or biological research. Hydra has been the subject of experimental studies for over 200 years (Trembley, 1744). Its attractive features include (1) its ease of culture in the laboratory, (2) its simple structure, (3) a small number of cell types, (4) three cell lineages, each of which is a stem cell lineage, and (5) an extensive capacity for regeneration. Because of the tissue dynamics of an adult Hydra, the developmental processes governing pattern formation, morphogenesis, cell division, and cell differentiation are continuously active. Given its considerable capacity for regeneration as well as its being amenable to a variety of manipulations at the tissue and cell levels, most of the work up to the mid-1980s was focused on aspects of the developmental biology of Hydra. Primarily, these efforts involved gaining an understanding of formation and patterning of the single axis of the animal (Bode and Bode, 1984) as well as understanding the nature and control of cell division and differentiation of the stem cell lineages (Bode, 1996). With these aspects fairly well established, the emphasis shifted in the late 1980s to gaining an understanding of the molecular mechanisms underlying the elucidated developmental processes. Efforts were focused on looking for orthologues of genes affecting patterning and stem cell processes in bilaterians, which led to the isolation and characterization of >100 such genes. The variety of cell and tissue manipulations that had been developed proved, and are proving, valuable in sorting out the developmental roles of these genes with some precision.
    [Show full text]
  • CNIDARIA Corals, Medusae, Hydroids, Myxozoans
    FOUR Phylum CNIDARIA corals, medusae, hydroids, myxozoans STEPHEN D. CAIRNS, LISA-ANN GERSHWIN, FRED J. BROOK, PHILIP PUGH, ELLIOT W. Dawson, OscaR OcaÑA V., WILLEM VERvooRT, GARY WILLIAMS, JEANETTE E. Watson, DENNIS M. OPREsko, PETER SCHUCHERT, P. MICHAEL HINE, DENNIS P. GORDON, HAMISH J. CAMPBELL, ANTHONY J. WRIGHT, JUAN A. SÁNCHEZ, DAPHNE G. FAUTIN his ancient phylum of mostly marine organisms is best known for its contribution to geomorphological features, forming thousands of square Tkilometres of coral reefs in warm tropical waters. Their fossil remains contribute to some limestones. Cnidarians are also significant components of the plankton, where large medusae – popularly called jellyfish – and colonial forms like Portuguese man-of-war and stringy siphonophores prey on other organisms including small fish. Some of these species are justly feared by humans for their stings, which in some cases can be fatal. Certainly, most New Zealanders will have encountered cnidarians when rambling along beaches and fossicking in rock pools where sea anemones and diminutive bushy hydroids abound. In New Zealand’s fiords and in deeper water on seamounts, black corals and branching gorgonians can form veritable trees five metres high or more. In contrast, inland inhabitants of continental landmasses who have never, or rarely, seen an ocean or visited a seashore can hardly be impressed with the Cnidaria as a phylum – freshwater cnidarians are relatively few, restricted to tiny hydras, the branching hydroid Cordylophora, and rare medusae. Worldwide, there are about 10,000 described species, with perhaps half as many again undescribed. All cnidarians have nettle cells known as nematocysts (or cnidae – from the Greek, knide, a nettle), extraordinarily complex structures that are effectively invaginated coiled tubes within a cell.
    [Show full text]
  • Expansion of a Single Transposable Element Family Is BRIEF REPORT Associated with Genome-Size Increase and Radiation in the Genus Hydra
    Expansion of a single transposable element family is BRIEF REPORT associated with genome-size increase and radiation in the genus Hydra Wai Yee Wonga, Oleg Simakova,1, Diane M. Bridgeb, Paulyn Cartwrightc, Anthony J. Bellantuonod, Anne Kuhne, Thomas W. Holsteine, Charles N. Davidf, Robert E. Steeleg, and Daniel E. Martínezh,1 aDepartment of Molecular Evolution and Development, University of Vienna, 1010 Vienna, Austria; bDepartment of Biology, Elizabethtown College, Elizabethtown, PA 17022; cDepartment of Ecology & Evolutionary Biology, University of Kansas, Lawrence, KS 66045; dDepartment of Biological Sciences, Florida International University, Miami, FL 33199; eCentre for Organismal Biology, Heidelberg University, 69120 Heidelberg, Germany; fFaculty of Biology, Ludwig Maximilian University of Munich, 80539 Munich, Germany; gDepartment of Biological Chemistry, University of California, Irvine, CA 92617; and hDepartment of Biology, Pomona College, Claremont, CA 91711 Edited by W. Ford Doolittle, Dalhousie University, Halifax, NS, Canada, and approved October 8, 2019 (received for review July 9, 2019) Transposable elements are one of the major contributors to genome- Using transcriptome data, we searched for evidence of a ge- size differences in metazoans. Despite this, relatively little is known nome duplication event in the brown hydras. We found that 75% about the evolutionary patterns of element expansions and the (8,629 out of 11,543) of gene families had the same number of element families involved. Here we report a broad genomic sampling genes in both H. viridissima and H. vulgaris. Additionally, 84.7% within the genus Hydra, a freshwater cnidarian at the focal point of and 81.1% of the gene families contained a single gene from H.
    [Show full text]
  • Lists of Larval Worms from Marine Invertebrates of the Pacific Oc Ast of North America Hilda Lei Ching Hydra Enterprises
    View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by UNL | Libraries University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Faculty Publications from the Harold W. Manter Parasitology, Harold W. Manter Laboratory of Laboratory of Parasitology 1991 Lists of Larval Worms from Marine Invertebrates of the Pacific oC ast of North America Hilda Lei Ching Hydra Enterprises Follow this and additional works at: http://digitalcommons.unl.edu/parasitologyfacpubs Part of the Aquaculture and Fisheries Commons, Biodiversity Commons, Other Animal Sciences Commons, Parasitology Commons, and the Zoology Commons Ching, Hilda Lei, "Lists of Larval Worms from Marine Invertebrates of the Pacific oC ast of North America" (1991). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 771. http://digitalcommons.unl.edu/parasitologyfacpubs/771 This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Ching, Journal of the Helminthological Society of Washington (1991) 58(1). Copyright 1991, HELMSOC. Used by permission. J lIelminthol. Soc. Wash. 5'8(1). \ 991, pp. 57~8 Lists of Larval Worms from Marine Invertebrates of the Pacific Coast of North America HILDA LEI CHING Hydra Enterprises Ltd., P.O. Box 2184, Vancouver, British Columbia, Canada V6B 3V7 ABS"fRAcr: Immature stages of 73 digenetic trematodes are listed by their families, marine invertebrate hosts, and localities and then cross listed according to their molluscan hosts.
    [Show full text]
  • Developmental Signaling in Hydra: What Does It Take to Build a “Simple” Animal?
    Developmental Biology 248, 199–219 (2002) doi:10.1006/dbio.2002.0744 View metadata, citation and similar papers at core.ac.uk brought to you by CORE REVIEW provided by Elsevier - Publisher Connector Developmental Signaling in Hydra: What Does It Take to Build a “Simple” Animal? Robert E. Steele1 Department of Biological Chemistry and the Developmental Biology Center, University of California, Irvine, California 92697-1700 Developmental processes in multicellular animals depend on an array of signal transduction pathways. Studies of model organisms have identified a number of such pathways and dissected them in detail. However, these model organisms are all bilaterians. Investigations of the roles of signal transduction pathways in the early-diverging metazoan Hydra have revealed that a number of the well-known developmental signaling pathways were already in place in the last common ancestor of Hydra and bilaterians. In addition to these shared pathways, it appears that developmental processes in Hydra make use of pathways involving a variety of peptides. Such pathways have not yet been identified as developmental regulators in more recently diverged animals. In this review I will summarize work to date on developmental signaling pathways in Hydra and discuss the future directions in which such work will need to proceed to realize the potential that lies in this simple animal. © 2002 Elsevier Science (USA) “The cnidarians never stop pulling surprises.” tell us how animals were first assembled. Over the past 15 Colin Tudge years, Hydra has moved to center stage in such studies. The Variety of Life, 2000 THE EVOLUTIONARY CONTEXT OF INTRODUCTION HYDRA DEVELOPMENTAL BIOLOGY We know a lot about the developmental biology of a very From molecular phylogenetic studies, it is clear that the small number of animals.
    [Show full text]