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Home / Equine Research Bank / Front Vet Sci / The Role of Intestinal Microbial Metabolites in the Immunity...
Frontiers in veterinary science2022; 9; 832062; doi: 10.3389/fvets.2022.832062

The Role of Intestinal Microbial Metabolites in the Immunity of Equine Animals Infected With Horse Botflies.

Abstract: The microbiota and its metabolites play an important role in regulating the host metabolism and immunity. However, the underlying mechanism is still not well studied. Thus, we conducted the LC-MS/MS analysis and RNA-seq analysis on with and without horse botfly infestation to determine the metabolites produced by intestinal microbiota in feces and differentially expressed genes (DEGs) related to the immune response in blood and attempted to link them together. The results showed that parasite infection could change the composition of microbial metabolites. These identified metabolites could be divided into six categories, including compounds with biological roles, bioactive peptides, endocrine-disrupting compounds, pesticides, phytochemical compounds, and lipids. The three pathways involving most metabolites were lipid metabolism, amino acid metabolism, and biosynthesis of other secondary metabolites. The significant differences between the host with and without parasites were shown in 31 metabolites with known functions, which were related to physiological activities of the host. For the gene analysis, we found that parasite infection could alarm the host immune response. The gene of "cathepsin W" involved in innate and adaptive immune responses was upregulated. The two genes of the following functions were downregulated: "protein S100-A8" and "protein S100-A9-like isoform X2" involved in chemokine and cytokine production, the toll-like receptor signaling pathway, and immune and inflammatory responses. GO and KEGG analyses showed that immune-related functions of defense response and Th17 cell differentiation had significant differences between the host with and without parasites, respectively. Last, the relationship between metabolites and genes was determined in this study. The purine metabolism and pyrimidine metabolism contained the most altered metabolites and DEGs, which mainly influenced the conversion of ATP, ADP, AMP, GTP, GMP, GDP, UTP, UDP, UMP, dTTP, dTDP, dTMP, and RNA. Thus, it could be concluded that parasitic infection can change the intestinal microbial metabolic activity and enhance immune response of the host through the pathway of purine and pyrimidine metabolism. This results will be a valuable contribution to understanding the bidirectional association of the parasite, intestinal microbiota, and host.
Copyright © 2022 Hu, Tang, Wang, Qi, Ente, Li, Zhang, Li and Chu.
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Publication Date: 2022-06-22 PubMed ID: 35812868PubMed Central: PMC9257286DOI: 10.3389/fvets.2022.832062Google Scholar: Lookup
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  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research focuses on understanding how infection by horse botflies influences the composition of intestinal microbial metabolites in horses and subsequently affects their immune response.

Objective and Methodology

  • The study aims to understand the role that intestinal microbial metabolites play in the immunity of equine animals infected with horse botflies.
  • The authors used liquid chromatography-mass spectrometry and RNA-sequencing to analyze samples from horses with and without botfly infestation.
  • The metabolites produced by intestinal microbiota found in feces and differentially expressed genes (DEGs) contributing to the immune response in blood were meticulously studied.

Findings on Metabolites

  • The research indicates that parasite infection can alter the composition of microbial metabolites.
  • These metabolites were sorted into six categories: compounds with biological roles, bioactive peptides, endocrine-disrupting compounds, pesticides, phytochemical compounds, and lipids.
  • From these categories, most metabolites played a part in three distinct pathways: lipid metabolism, amino acid metabolism, and biosynthesis of other secondary metabolites.
  • 31 metabolites with known functions displayed significant differences in hosts with parasites compared to those without, indicating a correlation between parasite infestation and changes in physiological activities.

Findings on Gene Analysis

  • The study found that the host’s immune response could be alerted by parasite infection.
  • The “cathepsin W” gene, which plays a role in innate and adaptive immune responses, was upregulated.
  • Conversely, two genes associated with chemokine and cytokine production and the toll-like receptor signaling pathway (“protein S100-A8” and “protein S100-A9-like isoform X2”) were downregulated.
  • The variances in immune-related functions of defense response and Th17 cell differentiation between hosts with and without parasites were also noteworthy.

Conclusion

  • The study determined the relationship between metabolites and genes, noting that purine metabolism and pyrimidine metabolism showed the most alterations in metabolites and DEGs.
  • These changes primarily influenced the conversion of several nucleotides, including ATP, ADP, AMP, GTP, GMP, GDP, UTP, UDP, UMP, dTTP, dTDP, dTMP, and RNA.
  • Overall, the findings confirm that parasitic infection can affect the intestinal microbial metabolic activity and bolster the host’s immunity via the pathway of purine and pyrimidine metabolism.
  • This research provides significant insight into the interaction between parasites, intestinal microbiota, and their host, contributing valuable knowledge to the field.

Cite This Article

APA
Hu D, Tang Y, Wang C, Qi Y, Ente M, Li X, Zhang D, Li K, Chu H. (2022). The Role of Intestinal Microbial Metabolites in the Immunity of Equine Animals Infected With Horse Botflies. Front Vet Sci, 9, 832062. https://doi.org/10.3389/fvets.2022.832062

Publication

Frontiers in veterinary science
ISSN: 2297-1769
NlmUniqueID: 101666658
Country: Switzerland
Language: English
Volume: 9
Pages: 832062
PII: 832062

Researcher Affiliations

Hu, Dini
  • Key Laboratory of Non-invasive Research Technology for Endangered Species, School of Ecology and Nature Conservation, Beijing Forestry University, Beijing, China.
Tang, Yujun
  • Xinjiang Research Centre for Breeding Przewalski's Horse, Ürümqi, China.
Wang, Chen
  • Altay Management Station of Mt. Kalamaili Ungulate Nature Reserve, Altay, China.
Qi, Yingjie
  • Altay Management Station of Mt. Kalamaili Ungulate Nature Reserve, Altay, China.
Ente, Make
  • Xinjiang Research Centre for Breeding Przewalski's Horse, Ürümqi, China.
Li, Xuefeng
  • Xinjiang Research Centre for Breeding Przewalski's Horse, Ürümqi, China.
Zhang, Dong
  • Key Laboratory of Non-invasive Research Technology for Endangered Species, School of Ecology and Nature Conservation, Beijing Forestry University, Beijing, China.
Li, Kai
  • Key Laboratory of Non-invasive Research Technology for Endangered Species, School of Ecology and Nature Conservation, Beijing Forestry University, Beijing, China.
Chu, Hongjun
  • Institute of Forest Ecology, Xinjiang Academy of Forestry, Ürümqi, China.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

This article includes 85 references
  1. Zumpt F. Myiasis in Man and Animals in the Old World: Textbook For Physicians, Veterinarians and Zoologist. .
  2. Soulsby E. Helminths, Arthropods and Protozoa of Domesticated Animals, 7th ed. .
  3. Li K, Wu Z, Hu DF, Cao J, Wang C. A report on nw causative agent (Gasterophilus spp.) of the myiasis of Przewalski's horse occurred in China. Chin J Anim Vet Sci (2007) 38:837–40.
    doi: 10.3321/j.issn:0366-6964.2007.08.015google scholar: lookup
  4. Sequeira JL, Tostes RA, Oliveira-Sequeira TC. Prevalence and macro- and microscopic lesions produced by Gasterophilus nasalis (Diptera: Oestridae) in the Botucatu Region, SP, Brazil.. Vet Parasitol 2001 Dec 13;102(3):261-6.
    doi: 10.1016/S0304-4017(01)00536-2pubmed: 11777606google scholar: lookup
  5. Xing J, Li P, Yan W Y. The dynamic observation on the immunological function of rat infected with Trichinella spiralis. Chin J Parasit Dis Control (2005) 18:26–7.
    doi: 10.3969/j.issn.1673-5234.2005.01.008google scholar: lookup
  6. Wang J, Cui J, Wang ZQ. Serum IgG levels in the mice experimentally infected with Trichinella spp. J Pathogen Biol (2007) 2:266–7.
    doi: 10.3969/j.issn.1673-5234.2007.04.008google scholar: lookup
  7. Valdes AM, Walter J, Segal E, Spector TD. Role of the gut microbiota in nutrition and health.. BMJ 2018 Jun 13;361:k2179.
    doi: 10.1136/bmj.k2179pmc: PMC6000740pubmed: 29899036google scholar: lookup
  8. Tilg H, Zmora N, Adolph TE, Elinav E. The intestinal microbiota fuelling metabolic inflammation.. Nat Rev Immunol 2020 Jan;20(1):40-54.
    doi: 10.1038/s41577-019-0198-4pubmed: 31388093google scholar: lookup
  9. Fan Y, Pedersen O. Gut microbiota in human metabolic health and disease.. Nat Rev Microbiol 2021 Jan;19(1):55-71.
    doi: 10.1038/s41579-020-0433-9pubmed: 32887946google scholar: lookup
  10. Becker L, Spear ET, Sinha SR, Haileselassie Y, Habtezion A. Age-Related Changes in Gut Microbiota Alter Phenotype of Muscularis Macrophages and Disrupt Gastrointestinal Motility.. Cell Mol Gastroenterol Hepatol 2019;7(1):243-245.e2.
    doi: 10.1016/j.jcmgh.2018.09.001pmc: PMC6305843pubmed: 30585161google scholar: lookup
  11. Hu D, Chao Y, Li Y, Peng X, Wang C, Wang Z, Zhang D, Li K. Effect of Gender Bias on Equine Fecal Microbiota.. J Equine Vet Sci 2021 Feb;97:103355.
    doi: 10.1016/j.jevs.2020.103355pubmed: 33478764google scholar: lookup
  12. Martín-Mateos R, Albillos A. The Role of the Gut-Liver Axis in Metabolic Dysfunction-Associated Fatty Liver Disease.. Front Immunol 2021;12:660179.
    doi: 10.3389/fimmu.2021.660179pmc: PMC8085382pubmed: 33936094google scholar: lookup
  13. Caffaratti C, Plazy C, Mery G, Tidjani AR, Fiorini F, Thiroux S, Toussaint B, Hannani D, Le Gouellec A. What We Know So Far about the Metabolite-Mediated Microbiota-Intestinal Immunity Dialogue and How to Hear the Sound of This Crosstalk.. Metabolites 2021 Jun 21;11(6).
    doi: 10.3390/metabo11060406pmc: PMC8234899pubmed: 34205653google scholar: lookup
  14. Louis P, Flint HJ. Formation of propionate and butyrate by the human colonic microbiota.. Environ Microbiol 2017 Jan;19(1):29-41.
    doi: 10.1111/1462-2920.13589pubmed: 27928878google scholar: lookup
  15. Yang W, Yu T, Huang X, Bilotta AJ, Xu L, Lu Y, Sun J, Pan F, Zhou J, Zhang W, Yao S, Maynard CL, Singh N, Dann SM, Liu Z, Cong Y. Intestinal microbiota-derived short-chain fatty acids regulation of immune cell IL-22 production and gut immunity.. Nat Commun 2020 Sep 8;11(1):4457.
    doi: 10.1038/s41467-020-18262-6pmc: PMC7478978pubmed: 32901017google scholar: lookup
  16. Belenguer A, Duncan SH, Holtrop G, Anderson SE, Lobley GE, Flint HJ. Impact of pH on lactate formation and utilization by human fecal microbial communities.. Appl Environ Microbiol 2007 Oct;73(20):6526-33.
    doi: 10.1128/AEM.00508-07pmc: PMC2075063pubmed: 17766450google scholar: lookup
  17. Errea A, Cayet D, Marchetti P, Tang C, Kluza J, Offermanns S, Sirard JC, Rumbo M. Lactate Inhibits the Pro-Inflammatory Response and Metabolic Reprogramming in Murine Macrophages in a GPR81-Independent Manner.. PLoS One 2016;11(11):e0163694.
    doi: 10.1371/journal.pone.0163694pmc: PMC5112849pubmed: 27846210google scholar: lookup
  18. Castagnetti C, Mariella J, Pirrone A, Cinotti S, Mari G, Peli A. Expression of interleukin-1β, interleukin-8, and interferon-γ in blood samples obtained from healthy and sick neonatal foals.. Am J Vet Res 2012 Sep;73(9):1418-27.
    doi: 10.2460/ajvr.73.9.1418pubmed: 22924724google scholar: lookup
  19. Fossum C, Hjertner B, Olofsson KM, Lindberg R, Ahooghalandari P, Camargo MM, Bröjer J, Edner A, Nostell K. Expression of tlr4, md2 and cd14 in equine blood leukocytes during endotoxin infusion and in intestinal tissues from healthy horses.. Vet Immunol Immunopathol 2012 Dec 15;150(3-4):141-8.
    doi: 10.1016/j.vetimm.2012.09.005pubmed: 23036528google scholar: lookup
  20. Vinther AM, Skovgaard K, Heegaard PM, Andersen PH. Dynamic expression of leukocyte innate immune genes in whole blood from horses with lipopolysaccharide-induced acute systemic inflammation.. BMC Vet Res 2015 Jun 16;11:134.
    doi: 10.1186/s12917-015-0450-5pmc: PMC4467047pubmed: 26076814google scholar: lookup
  21. Migdał A, Migdał Ł, Oczkowicz M, Okólski A, Chełmońska-Soyta A. Influence of Age and Immunostimulation on the Level of Toll-Like Receptor Gene (TLR3, 4, and 7) Expression in Foals.. Animals (Basel) 2020 Oct 26;10(11).
    doi: 10.3390/ani10111966pmc: PMC7692595pubmed: 33114637google scholar: lookup
  22. Zarski LM, Weber PSD, Lee Y, Soboll Hussey G. Transcriptomic Profiling of Equine and Viral Genes in Peripheral Blood Mononuclear Cells in Horses during Equine Herpesvirus 1 Infection.. Pathogens 2021 Jan 7;10(1).
    doi: 10.3390/pathogens10010043pmc: PMC7825769pubmed: 33430330google scholar: lookup
  23. Uzcanga GL, Bubis J. Dominant IgM synthesis against the soluble form of the prevailing variant surface glycoprotein from TeAp-N/D1 Trypanosoma equiperdum throughout the experimental acute infections of horses with non-tsetse transmitted Trypanozoon parasites.. J Immunoassay Immunochem 2020 Jul 3;41(4):745-760.
    doi: 10.1080/15321819.2020.1778029pubmed: 32522083google scholar: lookup
  24. Jürgenschellert L, Krücken J, Austin CJ, Lightbody KL, Bousquet E, von Samson-Himmelstjerna G. Investigations on the occurrence of tapeworm infections in German horse populations with comparison of different antibody detection methods based on saliva and serum samples.. Parasit Vectors 2020 Sep 10;13(1):462.
    doi: 10.1186/s13071-020-04318-5pmc: PMC7488081pubmed: 32912340google scholar: lookup
  25. Tzelos T, Geyer KK, Mitchell MC, McWilliam HEG, Kharchenko VO, Burgess STG, Matthews JB. Characterisation of serum IgG(T) responses to potential diagnostic antigens for equine cyathostominosis.. Int J Parasitol 2020 Apr;50(4):289-298.
    doi: 10.1016/j.ijpara.2020.01.004pubmed: 32171845google scholar: lookup
  26. Mukhopadhyay D, Arranz-Solís D, Saeij JPJ. Influence of the Host and Parasite Strain on the Immune Response During Toxoplasma Infection.. Front Cell Infect Microbiol 2020;10:580425.
    doi: 10.3389/fcimb.2020.580425pmc: PMC7593385pubmed: 33178630google scholar: lookup
  27. Vyas A. Mechanisms of Host Behavioral Change in Toxoplasma gondii Rodent Association.. PLoS Pathog 2015 Jul;11(7):e1004935.
    doi: 10.1371/journal.ppat.1004935pmc: PMC4512725pubmed: 26203656google scholar: lookup
  28. Tedford E, McConkey G. Neurophysiological Changes Induced by Chronic Toxoplasma gondii Infection.. Pathogens 2017 May 17;6(2).
    doi: 10.3390/pathogens6020019pmc: PMC5488653pubmed: 28513566google scholar: lookup
  29. Marra CM. Central nervous system infection with Toxoplasma gondii.. Handb Clin Neurol 2018;152:117-122.
    doi: 10.1016/B978-0-444-63849-6.00009-8pubmed: 29604970google scholar: lookup
  30. Schlüter D, Barragan A. Advances and Challenges in Understanding Cerebral Toxoplasmosis.. Front Immunol 2019;10:242.
    doi: 10.3389/fimmu.2019.00242pmc: PMC6401564pubmed: 30873157google scholar: lookup
  31. Brosnahan M. Eosinophils of the horse: part II: eosinophils in clinical diseases. Equine Vet Educ (2020) 32:590–602.
    doi: 10.1111/eve.13262pubmed: 0google scholar: lookup
  32. Steuer AE, Stewart JC, Barker VD, Adams AA, Nielsen MK. Cytokine and goblet cell gene expression in equine cyathostomin infection and larvicidal anthelmintic therapy.. Parasite Immunol 2020 Jun;42(6):e12709.
    doi: 10.1111/pim.12709pubmed: 32145074google scholar: lookup
  33. Peachey LE, Molena RA, Jenkins TP, Di Cesare A, Traversa D, Hodgkinson JE, Cantacessi C. The relationships between faecal egg counts and gut microbial composition in UK Thoroughbreds infected by cyathostomins.. Int J Parasitol 2018 May;48(6):403-412.
    doi: 10.1016/j.ijpara.2017.11.003pmc: PMC5946844pubmed: 29432771google scholar: lookup
  34. Walshe N, Duggan V, Cabrera-Rubio R, Crispie F, Cotter P, Feehan O, Mulcahy G. Removal of adult cyathostomins alters faecal microbiota and promotes an inflammatory phenotype in horses.. Int J Parasitol 2019 May;49(6):489-500.
    doi: 10.1016/j.ijpara.2019.02.003pubmed: 30986403google scholar: lookup
  35. Peachey LE, Castro C, Molena RA, Jenkins TP, Griffin JL, Cantacessi C. Dysbiosis associated with acute helminth infections in herbivorous youngstock - observations and implications.. Sci Rep 2019 Jul 31;9(1):11121.
    doi: 10.1038/s41598-019-47204-6pmc: PMC6668452pubmed: 31366962google scholar: lookup
  36. Costa MC, Stämpfli HR, Allen-Vercoe E, Weese JS. Development of the faecal microbiota in foals.. Equine Vet J 2016 Nov;48(6):681-688.
    doi: 10.1111/evj.12532pubmed: 26518456google scholar: lookup
  37. Hu D, Chao Y, Zhang B, Wang C, Qi Y, Ente M, Zhang D, Li K, Mok KM. Effects of Gasterophilus pecorum infestation on the intestinal microbiota of the rewilded Przewalski's horses in China.. PLoS One 2021;16(5):e0251512.
    doi: 10.1371/journal.pone.0251512pmc: PMC8112688pubmed: 33974667google scholar: lookup
  38. Hu D, Yang J, Qi Y, Li B, Li K, Mok KM. Metagenomic Analysis of Fecal Archaea, Bacteria, Eukaryota, and Virus in Przewalski's Horses Following Anthelmintic Treatment.. Front Vet Sci 2021;8:708512.
    doi: 10.3389/fvets.2021.708512pmc: PMC8416479pubmed: 34490397google scholar: lookup
  39. Labuda LA, Adegnika AA, Rosa BA, Martin J, Ateba-Ngoa U, Amoah AS, Lima HM, Meurs L, Mbow M, Manurung MD, Zinsou JF, Smits HH, Kremsner PG, Mitreva M, Yazdanbakhsh M. A Praziquantel Treatment Study of Immune and Transcriptome Profiles in Schistosoma haematobium-Infected Gabonese Schoolchildren.. J Infect Dis 2020 Nov 13;222(12):2103-2113.
    doi: 10.1093/infdis/jiz641pmc: PMC7661769pubmed: 31844885google scholar: lookup
  40. Jiminez J, Timsit E, Orsel K, van der Meer F, Guan LL, Plastow G. Whole-Blood Transcriptome Analysis of Feedlot Cattle With and Without Bovine Respiratory Disease.. Front Genet 2021;12:627623.
    doi: 10.3389/fgene.2021.627623pmc: PMC7982659pubmed: 33763112google scholar: lookup
  41. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A. Full-length transcriptome assembly from RNA-Seq data without a reference genome.. Nat Biotechnol 2011 May 15;29(7):644-52.
    doi: 10.1038/nbt.1883pmc: PMC3571712pubmed: 21572440google scholar: lookup
  42. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research.. Bioinformatics 2005 Sep 15;21(18):3674-6.
    doi: 10.1093/bioinformatics/bti610pubmed: 16081474google scholar: lookup
  43. Kanehisa M, Goto S. KEGG: kyoto encyclopedia of genes and genomes.. Nucleic Acids Res 2000 Jan 1;28(1):27-30.
    doi: 10.1093/nar/28.1.27pmc: PMC102409pubmed: 10592173google scholar: lookup
  44. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome.. BMC Bioinformatics 2011 Aug 4;12:323.
    doi: 10.1186/1471-2105-12-323pmc: PMC3163565pubmed: 21816040google scholar: lookup
  45. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.. Genome Biol 2014;15(12):550.
    doi: 10.1186/s13059-014-0550-8pmc: PMC4302049pubmed: 25516281google scholar: lookup
  46. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data.. Bioinformatics 2010 Jan 1;26(1):139-40.
    doi: 10.1093/bioinformatics/btp616pmc: PMC2796818pubmed: 19910308google scholar: lookup
  47. Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, Kong L, Gao G, Li CY, Wei L. KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases.. Nucleic Acids Res 2011 Jul;39(Web Server issue):W316-22.
    doi: 10.1093/nar/gkr483pmc: PMC3125809pubmed: 21715386google scholar: lookup
  48. Tsuchida S, Hattori T, Sawada A, Ogata K, Watanabe J, Ushida K. Fecal metabolite analysis of Japanese macaques in Yakushima by LC-MS/MS and LC-QTOF-MS.. J Vet Med Sci 2021 Jul 10;83(6):1012-1015.
    doi: 10.1292/jvms.21-0076pmc: PMC8267200pubmed: 33952783google scholar: lookup
  49. Zheng X, Xie G, Zhao A, Zhao L, Yao C, Chiu NH, Zhou Z, Bao Y, Jia W, Nicholson JK, Jia W. The footprints of gut microbial-mammalian co-metabolism.. J Proteome Res 2011 Dec 2;10(12):5512-22.
    doi: 10.1021/pr2007945pubmed: 21970572google scholar: lookup
  50. Kobayashi A, Tsuchida S, Hattori T, Ogata K, Ueda A, Yamada T, Murata K, Nakamura H, Ushida K. Metabolomic LC-MS/MS analyses and meta 16S rRNA gene analyses on cecal feces of Japanese rock ptarmigans reveal fundamental differences between semi-wild and captive raised individuals.. J Vet Med Sci 2020 Aug 28;82(8):1165-1172.
    doi: 10.1292/jvms.20-0003pmc: PMC7468055pubmed: 32581149google scholar: lookup
  51. Du L, Sun Y, Wang Q, Wang L, Zhang Y, Li S, Jin H, Yan S, Xiao X. Integrated metabolomics and 16S rDNA sequencing to investigate the mechanism of immune-enhancing effect of health Tonic oral liquid.. Food Res Int 2021 Jun;144:110323.
    doi: 10.1016/j.foodres.2021.110323pubmed: 34053528google scholar: lookup
  52. Vollmer M, Esders S, Farquharson FM, Neugart S, Duncan SH, Schreiner M, Louis P, Maul R, Rohn S. Mutual Interaction of Phenolic Compounds and Microbiota: Metabolism of Complex Phenolic Apigenin-C- and Kaempferol-O-Derivatives by Human Fecal Samples.. J Agric Food Chem 2018 Jan 17;66(2):485-497.
    doi: 10.1021/acs.jafc.7b04842pubmed: 29236499google scholar: lookup
  53. Dono A, Patrizz A, McCormack RM, Putluri N, Ganesh BP, Kaur B, McCullough LD, Ballester LY, Esquenazi Y. Glioma induced alterations in fecal short-chain fatty acids and neurotransmitters.. CNS Oncol 2020 Jun;9(2):CNS57.
    doi: 10.2217/cns-2020-0007pmc: PMC7341178pubmed: 32602743google scholar: lookup
  54. Marques JG, Shokry E, Frivolt K, Werkstetter KJ, Brückner A, Schwerd T, Koletzko S, Koletzko B. Metabolomic Signatures in Pediatric Crohn's Disease Patients with Mild or Quiescent Disease Treated with Partial Enteral Nutrition: A Feasibility Study.. SLAS Technol 2021 Apr;26(2):165-177.
    doi: 10.1177/2472630320969147pmc: PMC7985853pubmed: 33207993google scholar: lookup
  55. Zhang W, Jiang S, Qian D, Shang EX, Duan JA. Analysis of interaction property of calycosin-7-O-β-D-glucoside with human gut microbiota.. J Chromatogr B Analyt Technol Biomed Life Sci 2014 Jul 15;963:16-23.
    doi: 10.1016/j.jchromb.2014.05.015pubmed: 24922599google scholar: lookup
  56. Martinez-Guryn K, Hubert N, Frazier K, Urlass S, Musch MW, Ojeda P, Pierre JF, Miyoshi J, Sontag TJ, Cham CM, Reardon CA, Leone V, Chang EB. Small Intestine Microbiota Regulate Host Digestive and Absorptive Adaptive Responses to Dietary Lipids.. Cell Host Microbe 2018 Apr 11;23(4):458-469.e5.
    doi: 10.1016/j.chom.2018.03.011pmc: PMC5912695pubmed: 29649441google scholar: lookup
  57. Li S, Wang C, Wu Z. Dietary L-arginine supplementation of tilapia (Oreochromis niloticus) alters the microbial population and activates intestinal fatty acid oxidation.. Amino Acids 2022 Mar;54(3):339-351.
    doi: 10.1007/s00726-021-03018-3pubmed: 34212252google scholar: lookup
  58. Fuhr JE, Stidham JD. Inhibitory effect of cyclic adenosine 2',3'-monophosphate on leucine incorporation by L5178Y cells.. J Cell Physiol 1980 Apr;103(1):71-5.
    doi: 10.1002/jcp.1041030111pubmed: 6159364google scholar: lookup
  59. Fiet J, Gueux B, Raux-Demay MC, Kuttenn F, Vexiau P, Gourmelen M, Couillin P, Mornet E, Villette JM, Brerault JL. [21-deoxycortisol. A new marker of virilizing adrenal hyperplasia caused by 21-hydroxylase deficiency].. Presse Med 1989 Dec 2;18(40):1965-9.
    pubmed: 2531882
  60. Burgess EA, Hunt KE, Kraus SD, Rolland RM. Adrenal responses of large whales: Integrating fecal aldosterone as a complementary biomarker to glucocorticoids.. Gen Comp Endocrinol 2017 Oct 1;252:103-110.
    doi: 10.1016/j.ygcen.2017.07.026pubmed: 28757434google scholar: lookup
  61. Miller LJ, Lauderdale LK, Walsh MT, Bryant JL, Mitchell KA, Granger DA, Mellen JD. Reference intervals and values for fecal cortisol, aldosterone, and the ratio of cortisol to dehydroepiandrosterone metabolites in four species of cetaceans.. PLoS One 2021;16(8):e0250331.
    doi: 10.1371/journal.pone.0250331pmc: PMC8404979pubmed: 34460862google scholar: lookup
  62. Elfiky AA. Novel Guanosine Derivatives as Anti-HCV NS5b Polymerase: A QSAR and Molecular Docking Study.. Med Chem 2019;15(2):130-137.
    doi: 10.2174/1573406414666181015152511pubmed: 30324891google scholar: lookup
  63. Elfiky AA. Novel guanosine derivatives against Zika virus polymerase in silico.. J Med Virol 2020 Jan;92(1):11-16.
    doi: 10.1002/jmv.25573pmc: PMC7166851pubmed: 31436327google scholar: lookup
  64. Zheng X, Chen T, Jiang R, Zhao A, Wu Q, Kuang J, Sun D, Ren Z, Li M, Zhao M, Wang S, Bao Y, Li H, Hu C, Dong B, Li D, Wu J, Xia J, Wang X, Lan K, Rajani C, Xie G, Lu A, Jia W, Jiang C, Jia W. Hyocholic acid species improve glucose homeostasis through a distinct TGR5 and FXR signaling mechanism.. Cell Metab 2021 Apr 6;33(4):791-803.e7.
    doi: 10.1016/j.cmet.2020.11.017pubmed: 33338411google scholar: lookup
  65. Srinivasan S, Torres AG, Ribas de Pouplana L. Inosine in Biology and Disease.. Genes (Basel) 2021 Apr 19;12(4).
    doi: 10.3390/genes12040600pmc: PMC8072771pubmed: 33921764google scholar: lookup
  66. Jacques F, Rippa S, Perrin Y. Physiology of L-carnitine in plants in light of the knowledge in animals and microorganisms.. Plant Sci 2018 Sep;274:432-440.
    doi: 10.1016/j.plantsci.2018.06.020pubmed: 30080631google scholar: lookup
  67. Xu LL, Berg LJ, Jamin Keith D, Townsend SD. An effective reagent to functionalize alcohols with phosphocholine.. Org Biomol Chem 2020 Jan 28;18(4):767-770.
    doi: 10.1039/C9OB02582Kpmc: PMC7047658pubmed: 31912847google scholar: lookup
  68. Stamper GF, Morollo AA, Ringe D. Reaction of alanine racemase with 1-aminoethylphosphonic acid forms a stable external aldimine.. Biochemistry 1998 Jul 21;37(29):10438-45.
    doi: 10.1021/bi980692spubmed: 9671513google scholar: lookup
  69. Alvarado R, To J, Lund ME, Pinar A, Mansell A, Robinson MW, O'Brien BA, Dalton JP, Donnelly S. The immune modulatory peptide FhHDM-1 secreted by the helminth Fasciola hepatica prevents NLRP3 inflammasome activation by inhibiting endolysosomal acidification in macrophages.. FASEB J 2017 Jan;31(1):85-95.
    doi: 10.1096/fj.201500093rpubmed: 27682204google scholar: lookup
  70. Zhang XX, Cwiklinski K, Hu RS, Zheng WB, Sheng ZA, Zhang FK, Elsheikha HM, Dalton JP, Zhu XQ. Complex and dynamic transcriptional changes allow the helminth Fasciola gigantica to adjust to its intermediate snail and definitive mammalian hosts.. BMC Genomics 2019 Oct 12;20(1):729.
    doi: 10.1186/s12864-019-6103-5pmc: PMC6790025pubmed: 31606027google scholar: lookup
  71. Nian YY, Chen BK, Wang JJ, Zhong WT, Fang Y, Li Z, Zhang QS, Yan DC. Transcriptome analysis of Procambarus clarkii infected with infectious hypodermal and haematopoietic necrosis virus.. Fish Shellfish Immunol 2020 Mar;98:766-772.
    doi: 10.1016/j.fsi.2019.11.027pubmed: 31734284google scholar: lookup
  72. Chu C, Parkhurst CN, Zhang W, Zhou L, Yano H, Arifuzzaman M, Artis D. The ChAT-acetylcholine pathway promotes group 2 innate lymphoid cell responses and anti-helminth immunity.. Sci Immunol 2021 Mar 5;6(57).
    doi: 10.1126/sciimmunol.abe3218pmc: PMC8577047pubmed: 33674322google scholar: lookup
  73. O'Leary CE, Feng X, Cortez VS, Locksley RM, Schneider C. Interrogating the Small Intestine Tuft Cell-ILC2 Circuit Using In Vivo Manipulations.. Curr Protoc 2021 Mar;1(3):e77.
    doi: 10.1002/cpz1.77pmc: PMC8082719pubmed: 33740294google scholar: lookup
  74. Li S, Zhang N, Liu S, Li J, Liu L, Wang X, Li X, Gong P, Zhang X. Protective Immunity Against Neospora caninum Infection Induced by 14-3-3 Protein in Mice.. Front Vet Sci 2021;8:638173.
    doi: 10.3389/fvets.2021.638173pmc: PMC7965954pubmed: 33748214google scholar: lookup
  75. Borghi SM, Fattori V, Carvalho TT, Tatakihara VLH, Zaninelli TH, Pinho-Ribeiro FA, Ferraz CR, Staurengo-Ferrari L, Casagrande R, Pavanelli WR, Cunha FQ, Cunha TM, Pinge-Filho P, Verri WA. Experimental Trypanosoma cruzi Infection Induces Pain in Mice Dependent on Early Spinal Cord Glial Cells and NFκB Activation and Cytokine Production.. Front Immunol 2020;11:539086.
    doi: 10.3389/fimmu.2020.539086pmc: PMC7870690pubmed: 33574810google scholar: lookup
  76. Wu X, Thylur RP, Dayanand KK, Punnath K, Norbury CC, Gowda DC. IL-4 Treatment Mitigates Experimental Cerebral Malaria by Reducing Parasitemia, Dampening Inflammation, and Lessening the Cytotoxicity of T Cells.. J Immunol 2021 Jan 1;206(1):118-131.
    doi: 10.4049/jimmunol.2000779pubmed: 33239419google scholar: lookup
  77. Han HJ, Kim JH. Establishment of a TLR3 homozygous knockout human induced pluripotent stem cell line using CRISPR/Cas9.. Stem Cell Res 2021 Apr;52:102187.
    doi: 10.1016/j.scr.2021.102187pubmed: 33582546google scholar: lookup
  78. Maldonado Rivera JE, Hecker YP, Burucúa MM, Cirone KM, Cheuquepán FA, Fiorani F, Dorsch MA, Colque LA, Cantón GJ, Marin MS, Moore DP. Innate and humoral immune parameters at delivery in colostrum and calves from heifers experimentally infected with Neospora caninum.. Mol Immunol 2021 Apr;132:53-59.
    doi: 10.1016/j.molimm.2021.01.016pubmed: 33545625google scholar: lookup
  79. Sun S, Jiang H, Li Q, Liu Y, Gao Q, Liu W, Qin Y, Feng Y, Peng X, Xu G, Shen Q, Fan X, Ding J, Zhu L. Safety and Transcriptome Analysis of Live Attenuated Brucella Vaccine Strain S2 on Non-pregnant Cynomolgus Monkeys Without Abortive Effect on Pregnant Cynomolgus Monkeys.. Front Vet Sci 2021;8:641022.
    doi: 10.3389/fvets.2021.641022pmc: PMC7985263pubmed: 33768120google scholar: lookup
  80. Ortiz Wilczyñski JM, Olexen CM, Errasti AE, Schattner M, Rothlin CV, Correale J, Carrera Silva EA. GAS6 signaling tempers Th17 development in patients with multiple sclerosis and helminth infection.. PLoS Pathog 2020 Dec;16(12):e1009176.
    doi: 10.1371/journal.ppat.1009176pmc: PMC7785232pubmed: 33347509google scholar: lookup
  81. Kong D, Li X, Zhang B, Yan C, Tang R, Zheng K. The characteristics of CD4(+)T-helper cell subset differentiation in experimental Clonorchis sinensis-infected FVB mice.. Iran J Basic Med Sci 2020 Dec;23(12):1538-1543.
    doi: 10.22038/ijbms.2020.39436.9350pmc: PMC7811812pubmed: 33489026google scholar: lookup
  82. Alberghina D, Piccione G, Amorini AM, D'Urso S, Longo S, Picardi M, Tavazzi B, Lazzarino G. Modulation of circulating purines and pyrimidines by physical exercise in the horse.. Eur J Appl Physiol 2011 Mar;111(3):549-56.
    doi: 10.1007/s00421-010-1673-6pubmed: 20931219google scholar: lookup
  83. Harkness RA. Purine metabolism in the horse--are evolutionary differences linked to muscular performance?. Equine Vet J 1986 Jan;18(1):5-6.
    doi: 10.1111/j.2042-3306.1986.tb03525.xpubmed: 3948830google scholar: lookup
  84. Castejón F, Trigo P, Muñoz A, Riber C. Uric acid responses to endurance racing and relationships with performance, plasma biochemistry and metabolic alterations.. Equine Vet J Suppl 2006 Aug;(36):70-3.
    doi: 10.1111/j.2042-3306.2006.tb05516.xpubmed: 17402395google scholar: lookup
  85. Xu F, Pang Y, Nie Q, Zhang Z, Ye C, Jiang C, Wang Y, Liu H. Development and evaluation of a simultaneous strategy for pyrimidine metabolome quantification in multiple biological samples.. Food Chem 2022 Mar 30;373(Pt A):131405.
    doi: 10.1016/j.foodchem.2021.131405pubmed: 34742045google scholar: lookup

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