Amphibians as a model to study the role of immune cell heterogeneity in host and mycobacterial interactions

Paiola, Matthieu; Dimitrakopoulou, Dionysia; Pavelka, Martin S.; Robert, Jacques

doi:10.1016/j.dci.2022.104594

Cited by 6 publications

(6 citation statements)

References 185 publications

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“…In X. laevis , T cells produced in tadpoles appear functionally limited in terms of Ag recognition (i.e., TCR repertoire is limited in both gene usage and N-region diversity) ( 9 ). Such an assumption is based mainly on reverse genetic approaches and in vitro studies because in vivo assays to assess T cell responsiveness are limited in ectothermic vertebrates.…”

Section: Discussionmentioning

confidence: 99%

“…Innate T cells, memory T cells, and neonatal T cells are typically activated by innate or “stress” stimuli such as cytokines and NK and pathogen recognition receptor activation ( 8 , 64 , 70–76 ). Similarly to mammals, it is likely that such intrinsic differences between tadpole and adult T cells is related to ontogenesis and their different progenitor origins ( 9 ).…”

Section: Discussionmentioning

confidence: 99%

“…During early mammalian development, iT cells are represented by a variety of populations, including γδ T cell subtypes, MHC class I–like restricted mucosal-associated invariant T and invariant NKT cells, as well as innate-like CD4 and CD8 T cells known as virtual memory T cells ( 7 , 8 ). As recently reviewed ( 9 ), tadpole T cells might represent a distinct population from their adult counterparts. In tadpoles, first peripheral T cells are detected at 8 postconception weeks and at day 15 after hatching (stage 52), respectively (reviewed in 2 , 10 ).…”

Section: Introductionmentioning

confidence: 97%

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Larval T Cells Are Functionally Distinct from Adult T Cells in Xenopus laevis

Paiola,

McGuire,

Lopez Ruiz

et al. 2023

ImmunoHorizons

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The amphibian Xenopus laevis tadpole provides a unique comparative experimental organism for investigating the roles of innate-like T (iT) cells in tolerogenic immunity during early development. Unlike mammals and adult frogs, where conventional T cells are dominant, tadpoles rely mostly on several prominent distinct subsets of iT cells interacting with cognate nonpolymorphic MHC class I–like molecules. In the present study, to investigate whole T cell responsiveness ontogenesis in X. laevis, we determined in tadpoles and adult frogs the capacity of splenic T cells to proliferate in vivo upon infection with two different pathogens, ranavirus FV3 and Mycobacterium marinum, as well as in vitro upon PHA stimulation using the thymidine analogous 5-ethynyl-2′-deoxyuridine and flow cytometry. We also analyzed by RT-quantitative PCR T cell responsiveness upon PHA stimulation. In vivo tadpole splenic T cells showed limited capacity to proliferate, whereas the in vitro proliferation rate was higher than adult T cells. Gene markers for T cell activation and immediate-early genes induced upon TCR activation were upregulated with similar kinetics in tadpole and adult splenocytes. However, the tadpole T cell signature included a lower amplitude in the TCR signaling, which is a hallmark of mammalian memory-like T cells and iT or “preset” T cells. This study suggests that reminiscent of mammalian neonatal T cells, tadpole T cells are functionally different from their adult counterpart.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 97%

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Larval T Cells Are Functionally Distinct from Adult T Cells in Xenopus laevis

Paiola,

McGuire,

Lopez Ruiz

et al. 2023

ImmunoHorizons

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“…Presumably because of developmental constraints, X. laevis tadpoles exhibit a more active disease tolerance toward mycobacteria that is dominated by iT cell responses and is minimally inflammatory (reviewed in [136]). By contrast, adult frogs elicit robust pro-inflammatory responses against mycobacteria, which are driven by conventional T cells.…”

Section: (C) Mycobacteriamentioning

confidence: 99%

The amphibian immune system

Ruiz

Robert

2023

Phil. Trans. R. Soc. B

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Amphibians are at the forefront of bridging the evolutionary gap between mammals and more ancient, jawed vertebrates. Currently, several diseases have targeted amphibians and understanding their immune system has importance beyond their use as a research model. The immune system of the African clawed frog, Xenopus laevis , and that of mammals is well conserved. We know that several features of the adaptive and innate immune system are very similar for both, including the existence of B cells, T cells and innate-like T cells. In particular, the study of the immune system at early stages of development is benefitted by studying X. laevis tadpoles. The tadpoles mainly rely on innate immune mechanisms including pre-set or innate-like T cells until after metamorphosis. In this review we lay out what is known about the innate and adaptive immune system of X. laevis including the lymphoid organs as well as how other amphibian immune systems are similar or different. Furthermore, we will describe how the amphibian immune system responds to some viral, bacterial and fungal insults. This article is part of the theme issue ‘Amphibian immunity: stress, disease and ecoimmunology’.

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“…Elevated temperatures can alter those communities at the larval stages. For example, leopard frog tadpoles ( R. pipiens ) raised at an elevated temperature of 28°C (slightly higher than the medium preferred temperature of 20–25°C) [ 85 ] had strikingly different microbial communities from those raised at 18°C, and the warm tadpoles had a greater abundance of members of the potentially pathogenic genus Mycobacterium ([ 86 ], reviewed in [ 87 ]). A shift in the gut microbiome was also detected within a very short time (1–4 days) in tadpoles of green frogs ( Rana clamitans ) and American bullfrogs ( Rana catesbeiana ) when the acclimation temperature of 24°C was shifted to 29°C [ 88 ].…”

Section: Effects Of Natural Stressors On Tadpolesmentioning

confidence: 99%

Heat stress and amphibian immunity in a time of climate change

Rollins‐Smith

Sage

2023

Phil. Trans. R. Soc. B

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As a class of vertebrates, amphibians, are at greater risk for declines or extinctions than any other vertebrate group, including birds and mammals. There are many threats, including habitat destruction, invasive species, overuse by humans, toxic chemicals and emerging diseases. Climate change which brings unpredictable temperature changes and rainfall constitutes an additional threat. Survival of amphibians depends on immune defences functioning well under these combined threats. Here, we review the current state of knowledge of how amphibians respond to some natural stressors, including heat and desiccation stress, and the limited studies of the immune defences under these stressful conditions. In general, the current studies suggest that desiccation and heat stress can activate the hypothalamus pituitary–interrenal axis, with possible suppression of some innate and lymphocyte-mediated responses. Elevated temperatures can alter microbial communities in amphibian skin and gut, resulting in possible dysbiosis that fosters reduced resistance to pathogens. This article is part of the theme issue ‘Amphibian immunity: stress, disease and ecoimmunology’.

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Amphibians as a model to study the role of immune cell heterogeneity in host and mycobacterial interactions

Cited by 6 publications

References 185 publications

Larval T Cells Are Functionally Distinct from Adult T Cells in Xenopus laevis

Larval T Cells Are Functionally Distinct from Adult T Cells in Xenopus laevis

The amphibian immune system

Heat stress and amphibian immunity in a time of climate change

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