Investigating the effects of radiation, T cell depletion, and bone marrow transplantation on murine gut microbiota

. 2024 ; 15 () : 1324403. [epub] 20240605

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38903788

Microbiome research has gained much attention in recent years as the importance of gut microbiota in regulating host health becomes increasingly evident. However, the impact of radiation on the microbiota in the murine bone marrow transplantation model is still poorly understood. In this paper, we present key findings from our study on how radiation, followed by bone marrow transplantation with or without T cell depletion, impacts the microbiota in the ileum and caecum. Our findings show that radiation has different effects on the microbiota of the two intestinal regions, with the caecum showing increased interindividual variation, suggesting an impaired ability of the host to regulate microbial symbionts, consistent with the Anna Karenina principle. Additionally, we observed changes in the ileum composition, including an increase in bacterial taxa that are important modulators of host health, such as Akkermansia and Faecalibaculum. In contrast, radiation in the caecum was associated with an increased abundance of several common commensal taxa in the gut, including Lachnospiraceae and Bacteroides. Finally, we found that high doses of radiation had more substantial effects on the caecal microbiota of the T-cell-depleted group than that of the non-T-cell-depleted group. Overall, our results contribute to a better understanding of the complex relationship between radiation and the gut microbiota in the context of bone marrow transplantation and highlight the importance of considering different intestinal regions when studying microbiome responses to environmental stressors.

Zobrazit více v PubMed

Aguilera M., Cerdà-Cuéllar M., Martínez V. (2015). Antibiotic-induced dysbiosis alters host-bacterial interactions and leads to colonic sensory and motor changes in mice. Gut Microbes 6:10–23. doi: 10.4161/19490976.2014.990790 PubMed DOI PMC

Benjamini Y., Hochberg Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B (Methodological) 57, 289–300. doi: 10.1111/j.2517-6161.1995.tb02031.x DOI

Biagi E., Zama D., Nastasi C., Consolandi C., Fiori J., Rampelli S., et al. . (2015). Gut microbiota trajectory in pediatric patients undergoing hematopoietic SCT. Bone Marrow Transplant. 50, 992–998. doi: 10.1038/bmt.2015.16, PMID: PubMed DOI

Biagi E., Zama D., Rampelli S., Turroni S., Brigidi P., Consolandi C., et al. . (2019). Early gut microbiota signature of aGvHD in children given allogeneic hematopoietic cell transplantation for hematological disorders. BMC Med. Genet. 12:49. doi: 10.1186/s12920-019-0494-7, PMID: PubMed DOI PMC

Callahan B. J., McMurdie P. J., Rosen M. J., Han A. W., Johnson A. J. A., Holmes S. P. (2016). DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583. doi: 10.1038/nmeth.3869, PMID: PubMed DOI PMC

Cani P. D., Depommier C., Derrien M., Everard A., de Vos W. M. (2022). Akkermansia muciniphila: paradigm for next-generation beneficial microorganisms. Nat. Rev. Gastroenterol. Hepatol. 19, 625–637. doi: 10.1038/s41575-022-00631-9, PMID: PubMed DOI

Čížková D., Ďureje Ľ., Piálek J., Kreisinger J. (2021). Experimental validation of small mammal gut microbiota sampling from faeces and from the caecum after death. Heredity 127, 141–150. doi: 10.1038/s41437-021-00445-6, PMID: PubMed DOI PMC

Cui M., Xiao H., Li Y., Zhou L., Zhao S., Luo D., et al. . (2017). Faecal microbiota transplantation protects against radiation-induced toxicity. EMBO Mol. Med. 9, 448–461. doi: 10.15252/emmm.201606932, PMID: PubMed DOI PMC

Daniele N., Scerpa M. C., Caniglia M., Ciammetti C., Rossi C., Bernardo M. E., et al. . (2012). Overview of T-cell depletion in haploidentical stem cell transplantation. Blood Transfus. 10, 264–272. doi: 10.2450/2012.0106-11, PMID: PubMed DOI PMC

Doki N., Suyama M., Sasajima S., Ota J., Igarashi A., Mimura I., et al. . (2017). Clinical impact of pre-transplant gut microbial diversity on outcomes of allogeneic hematopoietic stem cell transplantation. Ann. Hematol. 96, 1517–1523. doi: 10.1007/s00277-017-3069-8, PMID: PubMed DOI

Douglas G. M., Maffei V. J., Zaneveld J. R., Yurgel S. N., Brown J. R., Taylor C. M., et al. . (2020). PICRUSt2 for prediction of metagenome functions. Nat. Biotechnol. 38, 685–688. doi: 10.1038/s41587-020-0548-6, PMID: PubMed DOI PMC

Edgar R. C., Haas B. J., Clemente J. C., Quince C., Knight R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200. doi: 10.1093/bioinformatics/btr381, PMID: PubMed DOI PMC

Eriguchi Y., Takashima S., Oka H., Shimoji S., Nakamura K., Uryu H., et al. . (2012). Graft-versus-host disease disrupts intestinal microbial ecology by inhibiting Paneth cell production of α-defensins. Blood 120, 223–231. doi: 10.1182/blood-2011-12-401166, PMID: PubMed DOI

Fredricks D. N. (2019). The gut microbiota and graft-versus-host disease. J. Clin. Invest. 129, 1808–1817. doi: 10.1172/JCI125797 PubMed DOI PMC

Guo H., Chou W. C., Lai Y., Liang K., Tam J. W., Brickey W. J., et al. . (2020). Multi-omics analyses of radiation survivors identify radioprotective microbes and metabolites. Science 370:eaay9097. doi: 10.1126/science.aay9097, PMID: PubMed DOI PMC

Ho V. T., Soiffer R. J. (2001). The history and future of T-cell depletion as graft-versus-host disease prophylaxis for allogeneic hematopoietic stem cell transplantation. Blood 98, 3192–3204. doi: 10.1182/blood.V98.12.3192 PubMed DOI

Holler E., Butzhammer P., Schmid K., Hundsrucker C., Koestler J., Peter K., et al. . (2014). Metagenomic analysis of the stool microbiome in patients receiving allogeneic stem cell transplantation: loss of diversity is associated with use of systemic antibiotics and more pronounced in gastrointestinal graft-versus-host disease. Biol. Blood Marrow Transplant. 20, 640–645. doi: 10.1016/j.bbmt.2014.01.030, PMID: PubMed DOI PMC

Ingham A. C., Kielsen K., Cilieborg M. S., Lund O., Holmes S., Aarestrup F. M., et al. . (2019). Specific gut microbiome members are associated with distinct immune markers in pediatric allogeneic hematopoietic stem cell transplantation. Microbiome 7:131. doi: 10.1186/s40168-019-0745-z, PMID: PubMed DOI PMC

Ingham A. C., Kielsen K., Mordhorst H., Ifversen M., Aarestrup F. M., Müller K. G., et al. . (2021). Microbiota long-term dynamics and prediction of acute graft-versus-host disease in pediatric allogeneic stem cell transplantation. Microbiome 9:148. doi: 10.1186/s40168-021-01100-2, PMID: PubMed DOI PMC

Jenq R. R., Ubeda C., Taur Y., Menezes C. C., Khanin R., Dudakov J. A., et al. . (2012). Regulation of intestinal inflammation by microbiota following allogeneic bone marrow transplantation. J. Exp. Med. 209, 903–911. doi: 10.1084/jem.20112408, PMID: PubMed DOI PMC

Jiang H., Lei R., Ding S. W., Zhu S. (2014). Skewer: a fast and accurate adapter trimmer for next-generation sequencing paired-end reads. BMC Bioinformatics 15:182. doi: 10.1186/1471-2105-15-182, PMID: PubMed DOI PMC

Kastl A. J., Terry N. A., Wu G. D., Albenberg L. G. (2020). The structure and function of the human small intestinal microbiota: current understanding and future directions. Cell. Mol. Gastroenterol. Hepatol. 9, 33–45. doi: 10.1016/j.jcmgh.2019.07.006, PMID: PubMed DOI PMC

Katiraei S., van Diepen J. A., Tavares L. P., Hoving L. R., Pronk A., Verschueren I., et al. . (2022). Bone marrow transplantation induces changes in the gut microbiota that chronically increase the cytokine response pattern of splenocytes. Sci. Rep. 12:6883. doi: 10.1038/s41598-022-10637-7, PMID: PubMed DOI PMC

Kaysen A., Heintz-Buschart A., Muller E. E. L., Narayanasamy S., Wampach L., Laczny C. C., et al. . (2017). Integrated meta-omic analyses of the gastrointestinal tract microbiome in patients undergoing allogeneic hematopoietic stem cell transplantation. Transl. Res. 186, 79–94.e1. doi: 10.1016/j.trsl.2017.06.008, PMID: PubMed DOI

Klindworth A., Pruesse E., Schweer T., Peplies J., Quast C., Horn M., et al. . (2013). Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 41:e1. doi: 10.1093/nar/gks808, PMID: PubMed DOI PMC

Kouidhi S., Souai N., Zidi O., Mosbah A., Lakhal A., Ben Othmane T., et al. . (2021). High throughput analysis reveals changes in gut microbiota and specific fecal Metabolomic signature in hematopoietic stem cell transplant patients. Microorganisms 9:1845. doi: 10.3390/microorganisms9091845, PMID: PubMed DOI PMC

Liu J., Liu C., Yue J. (2021). Radiotherapy and the gut microbiome: facts and fiction. Radiat. Oncol. 16:9. doi: 10.1186/s13014-020-01735-9 PubMed DOI PMC

Lu W., Qian L., Fang Z., Wang H., Zhu J., Lee Y. K., et al. . (2022). Probiotic strains alleviated OVA-induced food allergy in mice by regulating the gut microbiota and improving the level of indoleacrylic acid in fecal samples. Food Funct. 13, 3704–3719. doi: 10.1039/d1fo03520g, PMID: PubMed DOI

Mähler Convenor M., Berard M., Feinstein R., Gallagher A., Illgen-Wilcke B., Pritchett-Corning K., et al. . (2014). FELASA recommendations for the health monitoring of mouse, rat, hamster, guinea pig and rabbit colonies in breeding and experimental units. Lab. Anim. 48, 178–192. doi: 10.1177/0023677213516312, PMID: PubMed DOI

Mancini N., Greco R., Pasciuta R., Barbanti M. C., Pini G., Morrow O. B., et al. . (2017). Enteric microbiome markers as early predictors of clinical outcome in allogeneic hematopoietic stem cell transplant: results of a prospective study in adult patients. Open Forum Infect. Dis. 4:ofx215. doi: 10.1093/ofid/ofx215, PMID: PubMed DOI PMC

McArtor D. B., Lubke G. H., Bergeman C. S. (2017). Extending multivariate distance matrix regression with an effect size measure and the asymptotic null distribution of the test statistic. Psychometrika 82, 1052–1077. doi: 10.1007/s11336-016-9527-8 PubMed DOI PMC

Miltiadous O., Waters N. R., Andrlová H., Dai A., Nguyen C. L., Burgos da Silva M., et al. . (2022). Early intestinal microbial features are associated with CD4 T-cell recovery after allogeneic hematopoietic transplant. Blood 139, 2758–2769. doi: 10.1182/blood.2021014255, PMID: PubMed DOI PMC

Morjaria S., Schluter J., Taylor B. P., Littmann E. R., Carter R. A., Fontana E., et al. . (2019). Antibiotic-induced shifts in fecal microbiota density and composition during hematopoietic stem cell transplantation. Infect. Immun. 87, e00206–e00219. doi: 10.1128/IAI.00206-19, PMID: PubMed DOI PMC

Moudra A., Niederlova V., Novotny J., Schmiedova L., Kubovciak J., Matejkova T., et al. . (2021). Phenotypic and clonal stability of antigen-inexperienced memory-like T cells across the genetic background, hygienic status, and aging. J. Immunol. 206, 2109–2121. doi: 10.4049/jimmunol.2001028, PMID: PubMed DOI PMC

Parada Venegas D., de la Fuente M. K., Landskron G., González M. J., Quera R., Dijkstra G., et al. . (2019). Short chain fatty acids (SCFAs)-mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases. Front. Immunol. 10:277: 277. doi: 10.3389/fimmu.2019.00277, PMID: PubMed DOI PMC

Payen M., Nicolis I., Robin M., Michonneau D., Delannoye J., Mayeur C., et al. . (2020). Functional and phylogenetic alterations in gut microbiome are linked to graft-versus-host disease severity. Blood Adv. 4, 1824–1832. doi: 10.1182/bloodadvances.2020001531, PMID: PubMed DOI PMC

Peled J. U., Gomes A. L. C., Devlin S. M., Littmann E. R., Taur Y., Sung A. D., et al. . (2020). Microbiota as predictor of mortality in allogeneic hematopoietic-cell transplantation. N. Engl. J. Med. 382, 822–834. doi: 10.1056/NEJMoa1900623, PMID: PubMed DOI PMC

Quast C., Pruesse E., Yilmaz P., Gerken J., Schweer T., Yarza P., et al. . (2013). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596. doi: 10.1093/nar/gks1219, PMID: PubMed DOI PMC

Sen T., Thummer R. P. (2022). The impact of human microbiotas in hematopoietic stem cell and organ transplantation. Front. Immunol. 13:932228. doi: 10.3389/fimmu.2022.932228 (Accessed: 9 June 2023), PMID: PubMed DOI PMC

Song Q., Cheng S. W., Li D., Cheng H., Lai Y. S., Han Q., et al. . (2022). Gut microbiota mediated hypoglycemic effect of Astragalus membranaceus polysaccharides in db/db mice. Front. Pharmacol. 13:1043527. doi: 10.3389/fphar.2022.1043527, PMID: PubMed DOI PMC

Staffas A., Burgos da Silva M., van den Brink M. R. M. (2017). The intestinal microbiota in allogeneic hematopoietic cell transplant and graft-versus-host disease. Blood 129, 927–933. doi: 10.1182/blood-2016-09-691394 PubMed DOI PMC

Styczyński J., Tridello G., Koster L., Iacobelli S., van Biezen A., van der Werf S., et al. . (2020). Death after hematopoietic stem cell transplantation: changes over calendar year time, infections and associated factors. Bone Marrow Transplant. 55, 126–136. doi: 10.1038/s41409-019-0624-z, PMID: PubMed DOI PMC

Taur Y., Xavier J. B., Lipuma L., Ubeda C., Goldberg J., Gobourne A., et al. . (2012). Intestinal domination and the risk of bacteremia in patients undergoing allogeneic hematopoietic stem cell transplantation. Clin. Infect. Dis. 55, 905–914. doi: 10.1093/cid/cis580, PMID: PubMed DOI PMC

Wang Q., Garrity G. M., Tiedje J. M., Cole J. R. (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261–5267. doi: 10.1128/AEM.00062-07, PMID: PubMed DOI PMC

Ward T., Larson J., Meulemans J., Hillmann B., Lynch J., Sidiropoulos D., et al. . (2017). BugBase predicts organism-level microbiome phenotypes. bioRxiv 2017:133462. doi: 10.1101/133462 DOI

Weber D., Hiergeist A., Weber M., Dettmer K., Wolff D., Hahn J., et al. . (2019). Detrimental effect of broad-spectrum antibiotics on intestinal microbiome diversity in patients after allogeneic stem cell transplantation: lack of commensal sparing antibiotics. Clin. Infect. Dis. 68, 1303–1310. doi: 10.1093/cid/ciy711, PMID: PubMed DOI

Ye Y., Doak T. G. (2009). A parsimony approach to biological pathway reconstruction/inference for genomes and metagenomes. PLoS Comput. Biol. 5:e1000465. doi: 10.1371/journal.pcbi.1000465 PubMed DOI PMC

Zagato E., Pozzi C., Bertocchi A., Schioppa T., Saccheri F., Guglietta S., et al. . (2020). Endogenous murine microbiota member Faecalibaculum rodentium and its human homologue protect from intestinal tumour growth. Nat. Microbiol. 5, 511–524. doi: 10.1038/s41564-019-0649-5, PMID: PubMed DOI PMC

Zama D., Bossù G., Leardini D., Muratore E., Biagi E., Prete A., et al. . (2020). Insights into the role of intestinal microbiota in hematopoietic stem-cell transplantation. Ther. Adv. Hematol. 11:96961. doi: 10.1177/2040620719896961, PMID: PubMed DOI PMC

Zaneveld J. R., McMinds R., Vega Thurber R. (2017). Stress and stability: applying the Anna Karenina principle to animal microbiomes. Nat. Microbiol. 2:17121. doi: 10.1038/nmicrobiol.2017.121 PubMed DOI

Zoetendal E. G., Raes J., van den Bogert B., Arumugam M., Booijink C. C. G. M., Troost F. J., et al. . (2012). The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates. ISME J. 6, 1415–1426. doi: 10.1038/ismej.2011.212, PMID: PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...