Ancient T-independence of Mucosal IgX/A: Gut Microbiota Unaffected by Larval Thymectomy in Xenopus Laevis

Overview

Journal Mucosal Immunol

Publisher Elsevier

Specialty Allergy & Immunology

Date 2012 Aug 30

PMID 22929561

Citations 27

Authors

S Mashoof

A Goodroe

C C Du

J O Eubanks

N Jacobs

J M Steiner

I Tizard

J S Suchodolski

M F Criscitiello

Affiliations

Soon will be listed here.

Abstract

Many studies address the influence of the gut microbiome on the immune system, but few dissect the effect of T cells on gut microbiota and mucosal responses. We have employed larval thymectomy in Xenopus to study the gut microbiota with and without the influence of T lymphocytes. Pyrosequencing of 16S ribosomal RNA genes was used to assess the relative abundance of bacterial groups present in the stomach, small and large intestine. Clostridiaceae was the most abundant family throughout the gut, while Bacteroidaceae, Enterobacteriaceae, and Flavobacteriaceae also were well represented. Unifrac analysis revealed no differences in microbiota distribution between thymectomized and unoperated frogs. This is consistent with immunization data showing that levels of the mucosal immunoglobulin IgX are not altered significantly by thymectomy. This study in Xenopus represents the oldest organisms that exhibit class switch to a mucosal isotype and is relevant to mammalian immunology, as IgA appears to have evolved from IgX based upon phylogeny, genomic synteny, and function.

Citing Articles

The role of family and environment in determining the skin bacterial communities of captive aquatic frogs, Xenopus laevis.

Chapman P, Hudson D, Morgan X, Beck C FEMS Microbiol Ecol. 2024; 100(11).

PMID: 39317670 PMC: 11503959. DOI: 10.1093/femsec/fiae131.

Sex, health status and habitat alter the community composition and assembly processes of symbiotic bacteria in captive frogs.

Liu S, Imad S, Hussain S, Xiao S, Yu X, Cao H BMC Microbiol. 2024; 24(1):34.

PMID: 38262927 PMC: 10804495. DOI: 10.1186/s12866-023-03150-y.

Immunonutrition: facilitating mucosal immune response in teleost intestine with amino acids through oxidant-antioxidant balance.

Hissen K, He W, Wu G, Criscitiello M Front Immunol. 2023; 14:1241615.

PMID: 37841275 PMC: 10570457. DOI: 10.3389/fimmu.2023.1241615.

The adaptive microbiome hypothesis and immune interactions in amphibian mucus.

Woodhams D, McCartney J, Walke J, Whetstone R Dev Comp Immunol. 2023; 145:104690.

PMID: 37001710 PMC: 10249470. DOI: 10.1016/j.dci.2023.104690.

Evolutionary analyses of polymeric immunoglobulin receptor (pIgR) in the mammals reveals an outstanding mutation rate in the lagomorphs.

Neves F, de Sousa-Pereira P, Melo-Ferreira J, Esteves P, Pinheiro A Front Immunol. 2022; 13:1009387.

PMID: 36466819 PMC: 9716071. DOI: 10.3389/fimmu.2022.1009387.

References

Gravenor I, Horton T, Ritchie P, Flint E, Horton J . Ontogeny and thymus-dependence of T cell surface antigens in Xenopus: flow cytometric studies on monoclonal antibody-stained thymus and spleen. Dev Comp Immunol. 1995; 19(6):507-23. DOI: 10.1016/0145-305x(95)00030-w. View

Du C, Mashoof S, Criscitiello M . Oral immunization of the African clawed frog (Xenopus laevis) upregulates the mucosal immunoglobulin IgX. Vet Immunol Immunopathol. 2011; 145(1-2):493-8. PMC: 3273591. DOI: 10.1016/j.vetimm.2011.10.019. View

Lauer A, Simon M, Banning J, Lam B, Harris R . Diversity of cutaneous bacteria with antifungal activity isolated from female four-toed salamanders. ISME J. 2007; 2(2):145-57. DOI: 10.1038/ismej.2007.110. View

Macpherson A, Gatto D, Sainsbury E, Harriman G, Hengartner H, Zinkernagel R . A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science. 2000; 288(5474):2222-6. DOI: 10.1126/science.288.5474.2222. View

Kroese F, Ammerlaan W, Deenen G, Adams S, Herzenberg L, Kantor A . A dual origin for IgA plasma cells in the murine small intestine. Adv Exp Med Biol. 1995; 371A:435-40. DOI: 10.1007/978-1-4615-1941-6_91. View

Zhou J, Huang H, Meng K, Shi P, Wang Y, Luo H . Molecular and biochemical characterization of a novel xylanase from the symbiotic Sphingobacterium sp. TN19. Appl Microbiol Biotechnol. 2009; 85(2):323-33. DOI: 10.1007/s00253-009-2081-x. View

Benckert J, Schmolka N, Kreschel C, Zoller M, Sturm A, Wiedenmann B . The majority of intestinal IgA+ and IgG+ plasmablasts in the human gut are antigen-specific. J Clin Invest. 2011; 121(5):1946-55. PMC: 3083800. DOI: 10.1172/JCI44447. View

Criscitiello M, Ohta Y, Saltis M, McKinney E, Flajnik M . Evolutionarily conserved TCR binding sites, identification of T cells in primary lymphoid tissues, and surprising trans-rearrangements in nurse shark. J Immunol. 2010; 184(12):6950-60. PMC: 3222143. DOI: 10.4049/jimmunol.0902774. View

Nocker A, Burr M, Camper A . Genotypic microbial community profiling: a critical technical review. Microb Ecol. 2007; 54(2):276-89. DOI: 10.1007/s00248-006-9199-5. View

10.

Dunn-Walters D, Boursier L, Spencer J . Hypermutation, diversity and dissemination of human intestinal lamina propria plasma cells. Eur J Immunol. 1997; 27(11):2959-64. DOI: 10.1002/eji.1830271131. View

11.

Spiess S, Kuhrober A, Schirmbeck R, Arden B, Reimann J . Diversity of functional T-cell receptor delta-chain transcripts from bone marrow cells of athymic nude mice. Immunology. 1993; 78(2):252-9. PMC: 1421803. View

12.

Kuczynski J, Costello E, Nemergut D, Zaneveld J, Lauber C, Knights D . Direct sequencing of the human microbiome readily reveals community differences. Genome Biol. 2010; 11(5):210. PMC: 2898070. DOI: 10.1186/gb-2010-11-5-210. View

13.

Huse S, Dethlefsen L, Huber J, Welch D, Relman D, Sogin M . Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet. 2008; 4(11):e1000255. PMC: 2577301. DOI: 10.1371/journal.pgen.1000255. View

14.

Li J, Barreda D, Zhang Y, Boshra H, Gelman A, LaPatra S . B lymphocytes from early vertebrates have potent phagocytic and microbicidal abilities. Nat Immunol. 2006; 7(10):1116-24. DOI: 10.1038/ni1389. View

15.

Horton T, Ritchie P, Watson M, Horton J . NK cell evolution: studies on Xenopus. Biochem Soc Trans. 1997; 25(2):263S. DOI: 10.1042/bst025263s. View

16.

Soloff R, Wang T, Lybarger L, Dempsey D, Chervenak R . Transcription of the TCR-beta locus initiates in adult murine bone marrow. J Immunol. 1995; 154(8):3888-901. View

17.

Horton T, Ritchie P, Watson M, Horton J . NK-like activity against allogeneic tumour cells demonstrated in the spleen of control and thymectomized Xenopus. Immunol Cell Biol. 1996; 74(4):365-73. DOI: 10.1038/icb.1996.64. View

18.

Cooper M, Raymond D, Peterson R, South M, GOOD R . The functions of the thymus system and the bursa system in the chicken. J Exp Med. 1966; 123(1):75-102. PMC: 2138128. DOI: 10.1084/jem.123.1.75. View

19.

Tochinai S . Demonstration of thymus-independent immune system in Xenopus laevis. Response to polyvinylpyrrolidone. Immunology. 1976; 31(1):125-8. PMC: 1445089. View

20.

Guy-Grand D, Azogui O, Celli S, Darche S, Nussenzweig M, Kourilsky P . Extrathymic T cell lymphopoiesis: ontogeny and contribution to gut intraepithelial lymphocytes in athymic and euthymic mice. J Exp Med. 2003; 197(3):333-41. PMC: 2193840. DOI: 10.1084/jem.20021639. View