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

Dishaw, Larry J.; Leigh, Brittany A.; Cannon, John P.; Liberti, Assunta; Mueller, Mathias; Skapura, Diana P.; Karrer, Charlotte R.; Pinto, Maria Rosaria; Santis, Rosaria De; Litman, Gary W.

doi:10.1038/ncomms10617

Cited by 49 publications

(85 citation statements)

References 57 publications

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“…Among the genes expressed in B. schlosseri isolated cell populations, we found high enrichment for gene sets predominantly expressed in human HSC and myeloid populations, consistent with previous studies 21,[40][41][42][43][44][45] . In mammals, the Major Histocompatibility Complex (MHC) is the tissue-antigen that allows the immune system to recognize and tolerate 'self'.…”

Section: Evolution Of Hematopoietic and Cellular Immune Systemssupporting

confidence: 91%

Evolutionary Origin of the Mammalian Hematopoietic System Found in a Colonial Chordate

Rosental

Kowarsky

Seita

et al. 2017

Preprint

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SummaryHematopoiesis is an essential process that evolved in multicellular animals. At the heart of this process are hematopoietic stem cells (HSCs), which are multipotent, self-renewing and generate the entire repertoire of blood and immune cells throughout life. Here we studied the hematopoietic system of Botryllus schlosseri, a colonial tunicate that has vasculature, circulating blood cells, and interesting characteristics of stem cell biology and immunity. Self-recognition between genetically compatible B. schlosseri colonies leads to the formation of natural parabionts with shared circulation, whereas incompatible colonies reject each other. Using flow-cytometry, whole-transcriptome sequencing of defined cell populations, and diverse functional assays, we identified HSCs, progenitors, immuneeffector cells, the HSC niche, and demonstrated that self-recognition inhibits cytotoxic reaction. Our study implies that the HSC and myeloid lineages emerged in a common ancestor of tunicates and vertebrates and suggests that hematopoietic bone marrow and the B. schlosseri endostyle niche evolved from the same origin.All rights reserved. No reuse allowed without permission.(which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.The copyright holder for this preprint . http://dx.doi.org/10.1101/206318 doi: bioRxiv preprint first posted online Dec. 26, 2017; 3 Hematopoietic stem cells (HSCs) are multipotent, self-renewing cells that generate all mature blood and immune cell populations throughout life. In mammals, the blood-forming organ is the bone marrow, where HSCs reside in specialized niches that support their self-renewal and maintenance of an undifferentiated state. Since the identification of HSCs by prospective isolation 1 , several model systems have been studied to elucidate HSC biology [2][3][4][5][6][7][8] . While there are comprehensive studies on vertebrate HSC self-renewal, differentiation, physiological regulation and niche occupation, relatively little is known about their evolutionary origin and niches. To gain insight into the evolutionary origin of the mammalian hematopoietic and immune system, and identify fundamental cell and molecular mechanisms underlying HSCs homeostasis and regeneration we characterized the blood and immune system of the colonial tunicate Botryllus schlosseri.Tunicates are marine invertebrates in the phylum Chordata that share the chordate characteristics of a notochord, dorsal neural tube, and gill slits in their free-swimming larval stage, but lose most of these features during metamorphosis into sessile adults 9,10 . In B. schlosseri, after metamorphosis, a colony is formed via asexual reproduction consisting of multiple individuals, called zooids, through a stem-cell-mediated budding process that continues throughout life 11. Every week, the developed buds replace the parent zooids that undergo synchronized programmed cell death 12 (Movie S1). Each mature zooid has digestive and respiratory systems, a tub...

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Section: Evolution Of Hematopoietic and Cellular Immune Systemssupporting

confidence: 91%

Evolutionary Origin of the Mammalian Hematopoietic System Found in a Colonial Chordate

Rosental

Kowarsky

Seita

et al. 2017

Preprint

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“…Using the genome sequence as a foundation, we can now return to Metchnikoff's model of cellular immunology with a suite of modern molecular tools to address fundamental questions of animal immunity. This provides the opportunity to investigate both novel immune functions and those that are part of the deuterostome heritage shared with vertebrates 15 …”

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confidence: 99%

“…This provides the opportunity to investigate both novel immune functions and those that are part of the deuterostome heritage shared with vertebrates. 15 To characterize how the complex immune system encoded in the genome functions, we focus here on the larval stage of the purple sea urchin that has a well-characterized biphasic life history. 16 In this species, free-living embryos undergo gastrulation by 48 h post fertilization (hpf).…”

mentioning

confidence: 99%

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

Buckley

Schrankel

et al. 2016

Immunol Cell Biol

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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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“…A recent review gives a comprehensive overview of the experiments done across all phyla, from which Figure has been derived, after addition of supplementary references. That review presents cases where memory was investigated, but not always firmly proven (for instance see below the case of Dscam) because certain experiments were never confirmed or never repeated, and some conflicting results remain.…”

Section: Second Extension Of the Notion Of Immunological Memory: Whicmentioning

confidence: 99%

Immunological memory: What's in a name?

Pradeu

Pasquier

2018

Immunological Reviews

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Immunological memory is one of the core topics of contemporary immunology. Yet there are many discussions about what this concept precisely means, which components of the immune system display it, and in which phyla it exists. Recent years have seen the multiplication of claims that immunological memory can be found in "innate" immune cells and in many phyla beyond vertebrates (including invertebrates, plants, but also bacteria and archaea), as well as the multiplication of concepts to account for these phenomena, such as "innate immune memory" or "trained immunity". The aim of this critical review is to analyze these recent claims and concepts, and to distinguish ideas that have often been misleadingly associated, such as memory, adaptive immunity, and specificity. We argue that immunological memory is a gradual and multidimensional phenomenon, irreducible to any simple dichotomy, and we show why adopting this new view matters from an experimental and therapeutic point of view.

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

Cited by 49 publications

References 57 publications

Evolutionary Origin of the Mammalian Hematopoietic System Found in a Colonial Chordate

Evolutionary Origin of the Mammalian Hematopoietic System Found in a Colonial Chordate

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

Immunological memory: What's in a name?

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