The acute transcriptional response of the coral Acropora millepora to immune challenge: expression of GiMAP/IAN genes links the innate immune responses of corals with those of mammals and plants

Weiss, Yvonne; Fôret, Sylvain; Hayward, David C.; Ainsworth, Tracy D.; King, Rob; Ball, Eldon E.; Miller, David J.

doi:10.1186/1471-2164-14-400

Cited by 49 publications

(69 citation statements)

References 62 publications

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“…GIMAP4 has been earlier localized to the water soluble 25 and microsomal 6 fractions of the cytoplasm, ER and Golgi 1 . GIMAPs are related to septin GTPases known to interact with microtubules and membranes 18 .…”

Section: Resultsmentioning

confidence: 99%

Tubulin‐ and actin‐associating GIMAP4 is required for IFN‐γ secretion during Th cell differentiation

et al. 2014

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Although GTPase of the immunity-associated protein (GIMAP) family are known to be most highly expressed in the cells of the immune system, their function and role remain still poorly characterized. Small GTPases in general are known to be involved in many cellular processes in a cell type-specific manner and to contribute to specific differentiation processes. Among GIMAP family, GIMAP4 is the only member reported to have true GTPase activity, and its transcription is found to be differentially regulated during early human CD4+ T helper (Th) lymphocyte differentiation. GIMAP4 has been previously connected mainly with T- and B-cell development and survival and T-cell apoptosis. Here we show GIMAP4 to be localized into cytoskeletal elements and with the component of the trans golgi network, which suggests it to have a function in cellular transport processes. We demonstrate that depletion of GIMAP4 with RNAi results in downregulation of endoplasmic reticulum localizing chaperone VMA21. Most importantly, we discovered that GIMAP4 regulates secretion of cytokines in early differentiating human CD4+ Th lymphocytes and in particular the secretion of interferon-γ also affecting its downstream targets.

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Section: Resultsmentioning

confidence: 99%

Tubulin‐ and actin‐associating GIMAP4 is required for IFN‐γ secretion during Th cell differentiation

et al. 2014

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“…GiMAP is also called IAN (immune associated nucleotide binding protein). GiMAPs are ancient in origin, and have been lost in some animal lineages yet undergone expansions in others (Weiss et al, 2013). GiAMPs have been found to play an important role in plant defense and in regulating T-cell development and in maintaining T-cell homeostasis for normal immune function in mammals (Nitta and Takahama, 2007; Reuber and Ausubel, 1996).…”

Section: Discussionmentioning

confidence: 99%

“…GiAMPs have been found to play an important role in plant defense and in regulating T-cell development and in maintaining T-cell homeostasis for normal immune function in mammals (Nitta and Takahama, 2007; Reuber and Ausubel, 1996). Recently, it has been demonstrated that GiMAPs appeared as the most prominent immune factors in the coral Acropora millepora , a basal metazoan, after challenge with the bacterial cell wall-derived muramyl dipeptide and polyinosinic:polycytidylic acid (Weiss et al, 2013). Still, except for mammals, a clear immune role for GiMAPs in the metazoa has not been documented.…”

Section: Discussionmentioning

confidence: 99%

Pathogen-associated molecular patterns activate expression of genes involved in cell proliferation, immunity and detoxification in the amebocyte-producing organ of the snail Biomphalaria glabrata

Zhang

Loker

Sullivan

2016

Developmental & Comparative Immunology

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The anterior pericardial wall of the snail Biomphalaria glabrata has been identified as a site of hemocyte production, hence has been named the amebocyte-producing organ (APO). A number of studies have shown that exogenous abiotic and biotic substances, including pathogen associated molecular patterns (PAMPs), are able to stimulate APO mitotic activity and/or enlarge its size, implying a role for the APO in innate immunity. The molecular mechanisms underlying such responses have not yet been explored, in part due to the difficulty in obtaining sufficient APO tissue for gene expression studies. By using a modified RNA extraction technique and microarray technology, we investigated transcriptomic responses of APOs dissected from snails at 24 hours post-injection with two bacterial PAMPs, lipopolysaccharide (LPS) and peptidoglycan (PGN), or with fucoidan (FCN), which may mimic fucosyl-rich glycan PAMPs on sporocysts of Schistosoma mansoni. Based upon the number of genes differentially expressed, LPS exhibited the strongest activity, relative to saline-injected controls. A concurrent activation of genes involved in cell proliferation, immune response and detoxification metabolism was observed. A gene encoding checkpoint 1 kinase, a key regulator of mitosis, was highly expressed after stimulation by LPS. Also, seven different aminoacyl-tRNA synthetases that play an essential role in protein synthesis were found to be highly expressed. In addition to stimulating genes involved in cell proliferation, the injected substances, especially LPS, also induced expression of a number of immune-related genes including arginase, peptidoglycan recognition protein short form, tumor necrosis factor receptor, ficolin, calmodulin, bacterial permeability increasing proteins and E3 ubiquitin-protein ligase. Importantly, significant up-regulation was observed in four GiMAP (GTPase of immunity-associated protein) genes, a result which provides the first evidence suggesting an immune role of GiMAP in protostome animals. Moreover, altered expression of genes encoding cytochrome P450, glutathione-S-transferase, multiple drug resistance protein as well as a large number of genes encoding enzymes associated with degradation and detoxification metabolism was elicited in response to the injected substances.

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“…Yet, the mechanisms of immune response in corals are just beginning to be studied systematically (Palmer and Traylor-Knowles 2012). Genome and transcriptome analyses from various coral species, including the staghorn corals Acropora digitifera (Shinzato et al 2011), Acropora millepora (Miller et al 2007;Weiss et al 2013), and Acropora cervicornis (Libro et al 2013), the cauliflower coral Pocillopora damicornis (Vidal-Dupiol et al 2013), and the mountainous star coral Orbicella faveolata (previously Montastraea faveolata) (Schwarz et al 2008), have revealed the presence of a variety of conserved immune-type genes predicted to participate in the three functional compartments of any immune reaction, i.e., immune recognition, intracellular signaling, and effector response.…”

Section: Introductionmentioning

confidence: 99%

The immunotranscriptome of the Caribbean reef-building coral Pseudodiploria strigosa

Ocampo

Zárate-Potes

Pizarro³

et al. 2015

Immunogenetics

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The viability of coral reefs worldwide has been seriously compromised in the last few decades due in part to the emergence of coral diseases of infectious nature. Despite important efforts to understand the etiology and the contribution of environmental factors associated to coral diseases, the mechanisms of immune response in corals are just beginning to be studied systematically. In this study, we analyzed the set of conserved immune response genes of the Caribbean reef-building coral Pseudodiploria strigosa by Illumina-based transcriptome sequencing and annotation of healthy colonies challenged with whole live Gram-positive and Gram-negative bacteria. Searching the annotated transcriptome with immune-related terms yielded a total of 2782 transcripts predicted to encode conserved immune-related proteins that were classified into three modules: (a) the immune recognition module, containing a wide diversity of putative pattern recognition receptors including leucine-rich repeat-containing proteins, immunoglobulin superfamily receptors, representatives of various lectin families, and scavenger receptors; (b) the intracellular signaling module, containing components from the Toll-like receptor, transforming growth factor, MAPK, and apoptosis signaling pathways; and (3) the effector module, including the C3 and factor B complement components, a variety of proteases and protease inhibitors, and the melanization-inducing phenoloxidase. P. strigosa displays a highly variable and diverse immune recognition repertoire that has likely contributed to its resilience to coral diseases.

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The acute transcriptional response of the coral Acropora millepora to immune challenge: expression of GiMAP/IAN genes links the innate immune responses of corals with those of mammals and plants

Cited by 49 publications

References 62 publications

Tubulin‐ and actin‐associating GIMAP4 is required for IFN‐γ secretion during Th cell differentiation

Tubulin‐ and actin‐associating GIMAP4 is required for IFN‐γ secretion during Th cell differentiation

Pathogen-associated molecular patterns activate expression of genes involved in cell proliferation, immunity and detoxification in the amebocyte-producing organ of the snail Biomphalaria glabrata

The immunotranscriptome of the Caribbean reef-building coral Pseudodiploria strigosa

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