Animal Bioscience

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
권호 표지
DOI QR코드

DOI QR Code

β-Carotene prevents weaning-induced intestinal inflammation by modulating gut microbiota in piglets

  • Li, Ruonan (College of Animal Science and Technology, Jilin Agricultural University) ;
  • Li, Lingqian (College of Animal Science and Technology, Jilin Agricultural University) ;
  • Hong, Pan (College of Animal Science and Technology, Jilin Agricultural University) ;
  • Lang, Wuying (College of Animal Science and Technology, Jilin Agricultural University) ;
  • Hui, Junnan (College of Animal Science and Technology, Jilin Agricultural University) ;
  • Yang, Yu (College of Animal Science and Technology, Jilin Agricultural University) ;
  • Zheng, Xin (College of Animal Science and Technology, Jilin Agricultural University)
  • Received : 2019.06.17
  • Accepted : 2019.12.11
  • Published : 2021.07.01
Download PDF
⟨ Previous Next ⟩

Abstract

Objective: Weaning is an important stage in the life of young mammals, which is associated with intestinal inflammation, gut microbiota disorders, and even death. β-Carotene displays anti-inflammatory and antioxidant activities, which can prevent the development of inflammatory diseases. However, whether β-carotene can affect intestinal microbiota remains unclear. Methods: Twenty-four piglets were distributed into four groups: the normal suckling group (Con), the weaning group (WG), the weaning+β-carotene (40 mg/kg) group (LCBC), and the weaning+β-carotene (80 mg/kg) group (HCBC). The serum, jejunum, colon, and faeces were collected separately from each group. The effects of β-carotene on the phenotype, overall structure, and composition of gut microbiota were assessed in weaning piglets. Results: The results showed that β-carotene improved the growth performance, intestinal morphology and relieved inflammation. Furthermore, β-carotene significantly decreased the species from phyla Bacteroidetes and the genus Prevotella, and Blautia, and increased the species from the phyla Firmicutes and the genera p-75-a5, and Parabacteroides compared to the WG group. Spearman's correlation analysis showed that Prevotella and Blautia were positively correlated, and Parabacteroides and Synergistes were negatively correlated with the levels of interleukin-1β (IL-1β), IL-6, and tumour necrosis factor-α (TNF-α), while p-75-a5 showed negative correlation with IL-6 in serum samples from piglets. Conclusion: These findings indicate that β-carotene could alleviate weaning-induced intestinal inflammation by modulating gut microbiota in piglets. Prevotella may be a potential target of β-carotene in alleviating the weaning-induced intestinal inflammation in piglets.

Keywords

Acknowledgement

This work was supported by the National Natural Science Foundation of China (Grant Nos. 31672511); the Key science and technology projects in Jilin province (Grant Nos. 20170201004NY).

References

  1. Campbell JM, Crenshaw JD, Polo J. The biological stress of early weaned piglets. J Anim Sci Biotechnol 2013;4:19. https://doi.org/10.1186/2049-1891-4-19
  2. Ren W, Wang P, Yan J, et al. Melatonin alleviates weanling stress in mice: involvement of intestinal microbiota. J Pineal Res 2018;64:e12448. https://doi.org/10.1111/jpi.12448
  3. Kamada N, Seo SU, Chen GY, Nunez G. Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol 2013;13:321-35. https://doi.org/10.1038/nri3430
  4. Meale SJ, Li S, Azevedo P, et al. Weaning age influences the severity of gastrointestinal microbiome shifts in dairy calves. Sci Rep 2017;7:198. https://doi.org/10.1038/s41598-017-00223-7
  5. Gresse R, Chaucheyras-durand F, Fleury MA, Van de Wiele T, Forano E, Blanquet-diot S. Gut microbiota dysbiosis in postweaning piglets: understanding the keys to health. Trends Microbiol 2017;25:851-73. https://doi.org/10.1016/j.tim.2017.05.004
  6. Li R, Yang Y, Hong P, et al. β-Carotene attenuates weaning-induced apoptosis via inhibition of PERK-CHOP and IRE1-JNK/p38 MAPK signalling pathways in piglet jejunum. J Anim Physiol Anim Nutr 2020;104:280-90. https://doi.org/10.1111/jpn.13216
  7. Chew BP. Vitamin A and β-carotene on host defense. J Dairy Sci 1987;70:2732-43. https://doi.org/10.3168/jds.S0022-0302(87)80346-6
  8. Nishida K, Sugimoto M, Ikeda S, Kume S. Effects of supplemental β-carotene on mucosal IgA induction in the jejunum and ileum of mice after weaning. Br J Nutr 2014;111:247-53. https://doi.org/10.1017/S0007114513002195
  9. Bai S-K, Lee S-J, Na H-J, et al. β-Carotene inhibits inflammatory gene expression in lipopolysaccharide-stimulated macrophages by suppressing redox-based NF-κB activation. Exp Mol Med 2005;37:323-34. https://doi.org/10.1038/emm.2005.42
  10. Lee H, Ko GP. Antiviral effect of vitamin A on norovirus infection via modulation of the gut microbiome. Sci Rep 2016;6:25835. https://doi.org/10.1038/srep25835
  11. Hill GM, Cromwell GL, Crenshaw TD, et al. Growth promotion effects and plasma changes from feeding high dietary concentrations of zinc and copper to weanling pigs (regional study). J Anim Sci 2000;78:1010-6. https://doi.org/10.2527/2000.7841010x
  12. Ren W, Luo W, Wu M, et al. Dietary L-glutamine supplementation improves pregnancy outcome in mice infected with type-2 porcine circovirus. Amino Acids 2013;45:479-88. https://doi.org/10.1007/s00726-011-1134-5
  13. Caporaso JG, Kuczynski J, Stombaugh J, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010;7:335-6. https://doi.org/10.1038/nmeth.f.303
  14. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010;26:2460-1. https://doi.org/10.1093/bioinformatics/btq461
  15. Chao A, Yang MC. Stopping rules and estimation for recapture debugging with unequal failure rates. Biometrika 1993;80:193-201. http://dx.doi.org/10.1093/biomet/80.1.193
  16. Shannon CE. A mathematical theory of communication. Bell Syst Tech J 1948;27:379-423. https://doi.org/10.1002/j.1538-7305.1948.tb01338.x
  17. Xu J, Xu C, Chen X, et al. Regulation of an antioxidant blend on intestinal redox status and major microbiota in early weaned piglets. Nutrition 2014;30:584-9. https://doi.org/10.1016/j.nut.2013.10.018
  18. Kaminogawa S. Effects of food components on intestinal flora, intestinal immune system and their mutualism. Biosci Microflora 2010;29:69-82. https://doi.org/10.12938/bifidus.29.69
  19. Pie S, Lalles JP, Blazy F, Laffitte J, Seve B, Oswald IP. Weaning is associated with an upregulation of expression of inflammatory cytokines in the intestine of piglets. J Nutr 2004;134:641-7. https://doi.org/10.1093/jn/134.3.641
  20. Bhosale P, Bernstein PS. Vertebrate and invertebrate carotenoidbinding proteins. Arch Biochem Biophys 2007;458:121-7. https://doi.org/10.1016/j.abb.2006.10.005
  21. Dufour E, HaertlE T. Binding of retinoids and β-carotene to β-lactoglobulin. Influence of protein modifications. Biochim Biophys Acta (BBA)-Protein Struct Mol Enzymol 1991;1079:316-20. https://doi.org/10.1016/0167-4838(91)90075-B
  22. Hoffmann A, Baltimore D. Circuitry of nuclear factor κB signaling. Immunol Rev 2006;210:171-86. https://doi.org/10.1111/j.0105-2896.2006.00375.x
  23. Li R, Hong P, Zheng X. β-Carotene attenuates lipopolysaccharide-induced inflammation via inhibition of the NF-κB, JAK2/STAT3 and JNK/p38 MAPK signaling pathways in macrophages. Anim Sci J 2019;90:140-8. https://doi.org/10.1111/asj.13108
  24. Galdiero M, Vitiello M, D'Isanto M, Raieta K, Galdiero E. STAT1 and STAT3 phosphorylation by porins are independent of JAKs but are dependent on MAPK pathway and plays a role in U937 cells production of interleukin-6. Cytokine 2006;36:218-28. https://doi.org/10.1016/j.cyto.2006.12.003
  25. Leclercq S, Matamoros S, Cani PD, et al. Intestinal permeability, gut-bacterial dysbiosis, and behavioral markers of alcohol-dependence severity. Proc Natl Acad Sci USA 2014;111:E4485-E93. https://doi.org/10.1073/pnas.1415174111
  26. Scher JU, Andrew S, Longman RS, et al. Expansion of intestinal Prevotella copricorrelates with enhanced susceptibility to arthritis. Elife 2013;2:e01202. http://dx.doi.org/10.7554/eLife.01202.001
  27. Lavy A, Naveh Y, Coleman R, Mokady S, Werman MJ. Dietary Dunaliella bardawil, a beta-carotene-rich alga, protects against acetic acid-induced small bowel inflammation in rats. Inflamm Bowel Dis 2003;9:372-9. https://doi.org/10.1097/00054725-200311000-00005
  28. Arpaia N, Campbell C, Fan X, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 2013;504:451-5. https://doi.org/10.1038/nature12726
  29. Kverka M, Zakostelska Z, Klimesova K, et al. Oral administration of Parabacteroides distasonis antigens attenuates experimental murine colitis through modulation of immunity and microbiota composition. Clin Exp Immunol 2011;163:250-9. https://doi.org/10.1111/j.1365-2249.2010.04286.x
  30. Walker AW, Sanderson JD, Churcher C, et al. High-throughput clone library analysis of the mucosa-associated microbiota reveals dysbiosis and differences between inflamed and non-inflamed regions of the intestine in inflammatory bowel disease. BMC Microbiol 2011;11:7. https://doi.org/10.1186/1471-2180-11-7
  31. Pajarillo EAB, Chae J-P, Balolong MP, Kim HB, Kang D-K. Assessment of fecal bacterial diversity among healthy piglets during the weaning transition. J Gen Appl Microbiol 2014;60:140-6. https://doi.org/10.2323/jgam.60.140
  32. Hofer U. Microbiome: pro-inflammatory Prevotella? Nat Rev Microbiol 2014;12:5. https://doi.org/10.1038/nrmicro3180
  33. Larsen JM. The immune response to Prevotella bacteria in chronic inflammatory disease. Immunology 2017;151:363-74. https://doi.org/10.1111/imm.12760
  34. Thingholm L, Ruhlemann M, Wang J, et al. Sucrase-isomaltase 15Phe IBS risk variant in relation to dietary carbohydrates and faecal microbiota composition. Gut 2019:68:177-8. http://dx.doi.org/10.1136/gutjnl-2017-315841

피인용 문헌

  1. Gut microbiota regulation and anti‐inflammatory effect of β‐carotene in dextran sulfate sodium‐stimulated ulcerative colitis in rats vol.86, pp.5, 2021, https://doi.org/10.1111/1750-3841.15684
  2. Role of Food Antioxidants in Modulating Gut Microbial Communities: Novel Understandings in Intestinal Oxidative Stress Damage and Their Impact on Host Health vol.10, pp.10, 2021, https://doi.org/10.3390/antiox10101563
  3. Anti-Inflammatory and Anticancer Effects of Microalgal Carotenoids vol.19, pp.10, 2021, https://doi.org/10.3390/md19100531
  4. Understanding of the Site-Specific Microbial Patterns towards Accurate Identification for Patients with Diarrhea-Predominant Irritable Bowel Syndrome vol.9, pp.3, 2021, https://doi.org/10.1128/spectrum.01255-21