Literature DB >> 27192936

Perturbation of gut bacteria induces a coordinated cellular immune response in the purple sea urchin larva.

Eric Ch Ho1,2, Katherine M Buckley1,2,3, Catherine S Schrankel1,3, Nicholas W Schuh1,2, Taku Hibino1, Cynthia M Solek1,2, Koeun Bae1, Guizhi Wang1, Jonathan P Rast1,2,3.   

Abstract

The purple sea urchin (Strongylocentrotus purpuratus) genome sequence contains a complex repertoire of genes encoding innate immune recognition proteins and homologs of important vertebrate immune regulatory factors. To characterize how this immune system is deployed within an experimentally tractable, intact animal, we investigate the immune capability of the larval stage. Sea urchin embryos and larvae are morphologically simple and transparent, providing an organism-wide model to view immune response at cellular resolution. Here we present evidence for immune function in five mesenchymal cell types based on morphology, behavior and gene expression. Two cell types are phagocytic; the others interact at sites of microbial detection or injury. We characterize immune-associated gene markers for three cell types, including a perforin-like molecule, a scavenger receptor, a complement-like thioester-containing protein and the echinoderm-specific immune response factor 185/333. We elicit larval immune responses by (1) bacterial injection into the blastocoel and (2) seawater exposure to the marine bacterium Vibrio diazotrophicus to perturb immune state in the gut. Exposure at the epithelium induces a strong response in which pigment cells (one type of immune cell) migrate from the ectoderm to interact with the gut epithelium. Bacteria that accumulate in the gut later invade the blastocoel, where they are cleared by phagocytic and granular immune cells. The complexity of this coordinated, dynamic inflammatory program within the simple larval morphology provides a system in which to characterize processes that direct both aspects of the echinoderm-specific immune response as well as those that are shared with other deuterostomes, including vertebrates.

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Year:  2016        PMID: 27192936      PMCID: PMC5073156          DOI: 10.1038/icb.2016.51

Source DB:  PubMed          Journal:  Immunol Cell Biol        ISSN: 0818-9641            Impact factor:   5.126


  58 in total

1.  Metchnikoff and the phagocytosis theory.

Authors:  Alfred I Tauber
Journal:  Nat Rev Mol Cell Biol       Date:  2003-11       Impact factor: 94.444

Review 2.  Evolutionary crossroads in developmental biology: sea urchins.

Authors:  David R McClay
Journal:  Development       Date:  2011-07       Impact factor: 6.868

3.  Diversity of animal immune receptors and the origins of recognition complexity in the deuterostomes.

Authors:  Katherine M Buckley; Jonathan P Rast
Journal:  Dev Comp Immunol       Date:  2014-10-30       Impact factor: 3.636

Review 4.  Echinoderm immunity.

Authors:  L Courtney Smith; Julie Ghosh; Katherine M Buckley; Lori A Clow; Nolwenn M Dheilly; Tor Haug; John H Henson; Chun Li; Cheng Man Lun; Audrey J Majeske; Valeria Matranga; Sham V Nair; Jonathan P Rast; David A Raftos; Mattias Roth; Sandro Sacchi; Catherine S Schrankel; Klara Stensvåg
Journal:  Adv Exp Med Biol       Date:  2010       Impact factor: 2.622

5.  Chitin-induced carbotype conversion in Vibrio vulnificus.

Authors:  Jana Neiman; Yunzhi Guo; Dean A Rowe-Magnus
Journal:  Infect Immun       Date:  2011-06-13       Impact factor: 3.441

Review 6.  Individual-specific repertoires of immune cells SRCR receptors in the purple sea urchin (S. Purpuratus).

Authors:  Z Pancer
Journal:  Adv Exp Med Biol       Date:  2001       Impact factor: 2.622

7.  The coelomic elements of sea urchins (Strongylocentrotus). I. The normal coelomocytes; their morphology and dynamics in hanging drops.

Authors:  P T Johnson
Journal:  J Invertebr Pathol       Date:  1969-01       Impact factor: 2.841

8.  The onset of phagocytosis and identity in the embryo of Lytechinus variegatus.

Authors:  J R Silva
Journal:  Dev Comp Immunol       Date:  2000-12       Impact factor: 3.636

9.  Cis-regulatory logic driving glial cells missing: self-sustaining circuitry in later embryogenesis.

Authors:  Andrew Ransick; Eric H Davidson
Journal:  Dev Biol       Date:  2012-04-15       Impact factor: 3.582

10.  Gut immunity in a protochordate involves a secreted immunoglobulin-type mediator binding host chitin and bacteria.

Authors:  Larry J Dishaw; Brittany Leigh; John P Cannon; Assunta Liberti; M Gail Mueller; Diana P Skapura; Charlotte R Karrer; Maria R Pinto; Rosaria De Santis; Gary W Litman
Journal:  Nat Commun       Date:  2016-02-15       Impact factor: 14.919

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  26 in total

1.  Toll-like receptor pathway evolution in deuterostomes.

Authors:  Michael G Tassia; Nathan V Whelan; Kenneth M Halanych
Journal:  Proc Natl Acad Sci U S A       Date:  2017-06-19       Impact factor: 11.205

2.  Echinoderm immunity: is the larval immune system immature?

Authors:  Masayuki Hirano
Journal:  Immunol Cell Biol       Date:  2016-08-16       Impact factor: 5.126

3.  Embryo, larval, and juvenile staging of Lytechinus pictus from fertilization through sexual maturation.

Authors:  Katherine T Nesbit; Amro Hamdoun
Journal:  Dev Dyn       Date:  2020-08-31       Impact factor: 3.780

4.  Ocean warming alters predicted microbiome functionality in a common sea urchin.

Authors:  Cecilia J Brothers; William J Van Der Pol; Casey D Morrow; Joseph A Hakim; Hyunmin Koo; James B McClintock
Journal:  Proc Biol Sci       Date:  2018-06-27       Impact factor: 5.349

5.  Early patterning of ABCB, ABCC, and ABCG transporters establishes unique territories of small molecule transport in embryonic mesoderm and endoderm.

Authors:  Catherine S Schrankel; Amro Hamdoun
Journal:  Dev Biol       Date:  2021-01-15       Impact factor: 3.582

6.  Pigmentation biosynthesis influences the microbiome in sea urchins.

Authors:  Gary M Wessel; Masato Kiyomoto; Adam M Reitzel; Tyler J Carrier
Journal:  Proc Biol Sci       Date:  2022-08-17       Impact factor: 5.530

Review 7.  Gastrulation in the sea urchin.

Authors:  David R McClay; Jacob Warner; Megan Martik; Esther Miranda; Leslie Slota
Journal:  Curr Top Dev Biol       Date:  2019-10-22       Impact factor: 4.897

8.  CRISPR/Cas9 mutagenesis reveals a role for ABCB1 in gut immune responses to Vibrio diazotrophicus in sea urchin larvae.

Authors:  Travis J Fleming; Catherine S Schrankel; Himanshu Vyas; Hannah D Rosenblatt; Amro Hamdoun
Journal:  J Exp Biol       Date:  2021-04-15       Impact factor: 3.312

9.  Lectins identify distinct populations of coelomocytes in Strongylocentrotus purpuratus.

Authors:  Wen-Yun Liao; Sebastian D Fugmann
Journal:  PLoS One       Date:  2017-11-10       Impact factor: 3.240

Review 10.  An Organismal Model for Gene Regulatory Networks in the Gut-Associated Immune Response.

Authors:  Katherine M Buckley; Jonathan P Rast
Journal:  Front Immunol       Date:  2017-10-23       Impact factor: 7.561

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