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Research Paper

Regulation of colonic neuropeptide Y expression by the gut microbiome in patients with ulcerative colitis and its association with anxiety- and depression-like behavior in mice

ORCID Icon, , , , ORCID Icon & ORCID Icon
Article: 2319844 | Received 25 May 2023, Accepted 13 Feb 2024, Published online: 25 Feb 2024

References

  • Feuerstein JD, Moss AC, Farraye FA. Ulcerative colitis. Mayo Clin Proc. 2019;94(7):1357–19. doi:10.1016/j.mayocp.2019.01.018.
  • Roman AL. Comorbidity in inflammatory bowel disease. World J Gastroenterol. 2011;17(22):2723–2733. doi:10.3748/wjg.v17.i22.2723.
  • Addolorato G, Capristo E, Stefanini GF, Gasbarrini G. Inflammatory bowel disease: a study of the association between anxiety and depression, physical morbidity, and nutritional status. Scand J Gastroenterol. 1997;32(10):1013–21. doi:10.3109/00365529709011218.
  • Magni G, Bernasconi G, Mauro P, D’Odorico A, Sturniolo GC, Canton G, Martin A. Psychiatric diagnoses in ulcerative colitis. A controlled study. Br J Psychiatry. 1991;158(3):413–415. doi:10.1192/bjp.158.3.413.
  • Robertson DA, Ray J, Diamond I, Edwards JG. Personality profile and affective state of patients with inflammatory bowel disease. Gut. 1989;30(5):623–6. doi:10.1136/gut.30.5.623.
  • Panara AJ, Yarur AJ, Rieders B, Proksell S, Deshpande AR, Abreu MT, Sussman DA. The incidence and risk factors for developing depression after being diagnosed with inflammatory bowel disease: a cohort study. Aliment Pharmacol Ther. 2014;39(8):802–810. doi:10.1111/apt.12669.
  • Nahon S, Lahmek P, Durance C, Olympie A, Lesgourgues B, Colombel JF, Gendre JP. Risk factors of anxiety and depression in inflammatory bowel disease. Inflamm Bowel Dis. 2012;18(11):2086–2091. doi:10.1002/ibd.22888.
  • Martin-Subero M, Anderson G, Kanchanatawan B, Berk M, Maes M. Comorbidity between depression and inflammatory bowel disease explained by immune-inflammatory, oxidative, and nitrosative stress; tryptophan catabolite; and gut–brain pathways. CNS Spectr. 2016;21(2):184–198. doi:10.1017/S1092852915000449.
  • Jang HM, Lee KE, Lee HJ, Kim DH. Immobilization stress-induced Escherichia coli causes anxiety by inducing NF-κB activation through gut microbiota disturbance. Sci Rep. 2018;8(1):13897. doi:10.1038/s41598-018-31764-0.
  • Jang HM, Kim JK, Joo MK, Shin YJ, Lee CK, Kim HJ, Kim DH. Transplantation of fecal microbiota from patients with inflammatory bowel disease and depression alters immune response and behavior in recipient mice. Sci Rep. 2021;11(1):20406. doi:10.1038/s41598-021-00088-x.
  • Kilincarslan S, Evrensel A. The effect of fecal microbiota transplantation on psychiatric symptoms among patients with inflammatory bowel disease: an experimental study. Actas Esp Psiquiatr. 2020;48:1–7.
  • Kurokawa S, Kishimoto T, Mizuno S, Masaoka T, Naganuma M, Liang KC, Kitazawa M, Nakashima M, Shindo C, Suda W. et al. The effect of fecal microbiota transplantation on psychiatric symptoms among patients with irritable bowel syndrome, functional diarrhea and functional constipation: an open-label observational study. J Affect Disord. 2018;235:506–12. doi:10.1016/j.jad.2018.04.038.
  • De Palma G, Collins SM, Bercik P. The microbiota-gut-brain axis in functional gastrointestinal disorders. Gut Microbes. 2014;5(3):419–29. doi:10.4161/gmic.29417.
  • Carding S, Verbeke K, Vipond DT, Corfe BM, Owen LJ. Dysbiosis of the gut microbiota in disease. Microb Ecol Health Dis. 2015;26(8):26191. doi:10.3402/mehd.v26.26191.
  • Baumgart DC, Carding SR. Inflammatory bowel disease: cause and immunobiology. Lancet. 2007;369(9573):1627–40. doi:10.1016/S0140-6736(07)60750-8.
  • Carroll IM, Chang YH, Park J, Sartor RB, Ringel Y. Luminal and mucosal-associated intestinal microbiota in patients with diarrhea-predominant irritable bowel syndrome. Gut Pathog. 2010;2(1):19. doi:10.1186/1757-4749-2-19.
  • Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A. 2007;104(34):13780–5. doi:10.1073/pnas.0706625104.
  • De Palma G, Nadal I, Medina M, Donat E, Ribes-Koninckx C, Calabuig M, Sanz Y. Intestinal dysbiosis and reduced immunoglobulin-coated bacteria associated with coeliac disease in children. BMC Microbiol. 2010;10(1):63. doi:10.1186/1471-2180-10-63.
  • Shen XJ, Rawls JF, Randall T, Burcal L, Mpande CN, Jenkins N, Jovov B, Abdo Z, Sandler RS, Keku TO. et al. Molecular characterization of mucosal adherent bacteria and associations with colorectal adenomas. Gut Microbes. 2010;1(3):138–47. doi:10.4161/gmic.1.3.12360.
  • Foster JA, McVey Neufeld KA. Gut–brain axis: how the microbiome influences anxiety and depression. Trends Neurosci. 2013;36(5):305–312. doi:10.1016/j.tins.2013.01.005.
  • Jiang C, Li G, Huang P, Liu Z, Zhao B. The gut microbiota and alzheimer’s disease. J Alzheimers Dis. 2017;58(1):1–15. doi:10.3233/JAD-161141.
  • Qian Y, Yang X, Xu S, Wu C, Song Y, Qin N, Chen SD, Xiao Q. Alteration of the fecal microbiota in Chinese patients with Parkinson’s disease. Brain Behav Immun. 2018;70:194–202. doi:10.1016/j.bbi.2018.02.016.
  • Cryan JF, Dinan TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci. 2012;13(10):701–12. doi:10.1038/nrn3346.
  • Carabotti M, Scirocco A, Maselli MA, Severi C. The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems. Ann Gastroenterol. 2015;28:203–209.
  • Houser MC, Tansey MG. The gut-brain axis: is intestinal inflammation a silent driver of Parkinson’s disease pathogenesis? NPJ Parkinsons Dis. 2017;3(1):3. doi:10.1038/s41531-016-0002-0.
  • Sharon G, Sampson TR, Geschwind DH, Mazmanian SK. The central nervous system and the gut microbiome. Cell. 2016;167(4):915–32. doi:10.1016/j.cell.2016.10.027.
  • Mayer EA, Savidge T, Shulman RJ. Brain–gut microbiome interactions and functional bowel disorders. Gastroenterol. 2014;146(6):1500–1512. doi:10.1053/j.gastro.2014.02.037.
  • Fung TC, Olson CA, Hsiao EY. Interactions between the microbiota, immune and nervous systems in health and disease. Nat Neurosci. 2017;20(2):145–55. doi:10.1038/nn.4476.
  • Kormos V, Gaszner B. Role of neuropeptides in anxiety, stress, and depression: from animals to humans. Neuropeptides. 2013;47(6):401–19. doi:10.1016/j.npep.2013.10.014.
  • Belzung C, Yalcin I, Griebel G, Surget A, Leman S. Neuropeptides in psychiatric diseases: an overview with a particular focus on depression and anxiety disorders. CNS Neurol Disord Drug Targets. 2006;5(2):135–145. doi:10.2174/187152706776359682.
  • McGonigle P. Peptide therapeutics for CNS indications. Biochem Pharmacol. 2012;83(5):559–66. doi:10.1016/j.bcp.2011.10.014.
  • Holzer P, Reichmann F, Farzi A. Neuropeptide Y, peptide YY and pancreatic polypeptide in the gut–brain axis. Neuropeptides. 2012;46(6):261–274. doi:10.1016/j.npep.2012.08.005.
  • Holzer P, Farzi A. Neuropeptides and the microbiota-gut-brain axis. Adv Exp Med Biol. 2014;817:195–219.
  • Druce MR, Small CJ, Bloom SR. Minireview: gut peptides regulating satiety. Endocrinol. 2004;145(6):2660–2665. doi:10.1210/en.2004-0089.
  • Lach G, Schellekens H, Dinan TG, Cryan JF. Anxiety, depression, and the microbiome: a role for gut peptides. Neurotherapeut. 2018;15(1):36–59. doi:10.1007/s13311-017-0585-0.
  • Wei P, Keller C, Li L. Neuropeptides in gut-brain axis and their influence on host immunity and stress. Comput Struct Biotechnol J. 2020;18:843–51. doi:10.1016/j.csbj.2020.02.018.
  • Ge L, Liu S, Li S, Yang J, Hu G, Xu C, Song W. Psychological stress in inflammatory bowel disease: psychoneuroimmunological insights into bidirectional gut–brain communications. Front Immunol. 2022;13:1016578. doi:10.3389/fimmu.2022.1016578.
  • Sonali S, Ray B, Ahmed Tousif H, Rathipriya AG, Sunanda T, Mahalakshmi AM, Rungratanawanich W, Essa MM, Qoronfleh MW, Chidambaram SB. et al. Mechanistic insights into the link between gut dysbiosis and major depression: an extensive review. Cells. 2022;11(8):11. doi:10.3390/cells11081362.
  • Stogner KA, Holmes PV. Neuropeptide-Y exerts antidepressant-like effects in the forced swim test in rats. Eur J Pharmacol. 2000;387(2):R9–10. doi:10.1016/S0014-2999(99)00800-6.
  • Bannon AW, Seda J, Carmouche M, Francis JM, Norman MH, Karbon B, McCaleb ML. Behavioral characterization of neuropeptide Y knockout mice. Brain Res. 2000;868(1):79–87. doi:10.1016/S0006-8993(00)02285-X.
  • Kastin AJ, Akerstrom V. Nonsaturable entry of neuropeptide Y into brain. Am J Physiol. 1999;276(3):E479–82. doi:10.1152/ajpendo.1999.276.3.E479.
  • Jang HM, Kim JK, Joo MK, Shin YJ, Lee KE, Lee CK, Kim HJ, Kim DH. Enterococcus faecium and pediococcus acidilactici deteriorate Enterobacteriaceae-induced depression and colitis in mice. Sci Rep. 2022;12(1):9389. doi:10.1038/s41598-022-13629-9.
  • Joo MK, Ma X, Yoo JW, Shin YJ, Kim HJ, Kim DH. Patient-derived Enterococcus mundtii and its capsular polysaccharides cause depression through the downregulation of NF-κB-involved serotonin and BDNF expression. Microbes Infect. 2023;25(6):105116. doi:10.1016/j.micinf.2023.105116.
  • Farzi A, Reichmann F, Holzer P. The homeostatic role of neuropeptide Y in immune function and its impact on mood and behaviour. Acta Physiol (Oxf). 2015;213(3):603–627. doi:10.1111/apha.12445.
  • Gelfo F, Tirassa P, De Bartolo P, Croce N, Bernardini S, Caltagirone C, Petrosini L, Angelucci F. NPY intraperitoneal injections produce antidepressant-like effects and downregulate BDNF in the rat hypothalamus. CNS Neurosci Ther. 2012;18(6):487–492. doi:10.1111/j.1755-5949.2012.00314.x.
  • Bonacina J, Suarez N, Hormigo R, Fadda S, Lechner M, Saavedra L. A genomic view of food-related and probiotic enterococcus strains. DNA Res. 2017;24:11–24. doi:10.1093/dnares/dsw043.
  • Young V, Chang E, Meyer F, Sogin M, Schmidt T, Tiedje J. The role of the gut microbiota in ulcerative colitis. Nat Prec. 2010. doi:10.1038/npre.2010.5254.1.
  • Shreiner AB, Kao JY, Young VB. The gut microbiome in health and in disease. Curr Opin Gastroenterol. 2015;31(1):69–75. doi:10.1097/MOG.0000000000000139.
  • Kamada N, Seo SU, Chen GY, Nunez G. Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol. 2013;13(5):321–35. doi:10.1038/nri3430.
  • Leclercq S, Matamoros S, Cani PD, Neyrinck AM, Jamar F, Starkel P, Windey K, Tremaroli V, Bäckhed F, Verbeke K. et al. Intestinal permeability, gut-bacterial dysbiosis, and behavioral markers of alcohol-dependence severity. Proc Natl Acad Sci U S A. 2014;111(42):E4485–93. doi:10.1073/pnas.1415174111.
  • Alenghat T, Osborne LC, Saenz SA, Kobuley D, Ziegler CG, Mullican SE, Choi I, Grunberg S, Sinha R, Wynosky-Dolfi M. et al. Histone deacetylase 3 coordinates commensal-bacteria-dependent intestinal homeostasis. Nature. 2013;504(7478):153–7. doi:10.1038/nature12687.
  • Dayama G, Priya S, Niccum DE, Khoruts A, Blekhman R. Interactions between the gut microbiome and host gene regulation in cystic fibrosis. Genome Med. 2020;12(1):12. doi:10.1186/s13073-020-0710-2.
  • Nichols RG, Davenport ER. The relationship between the gut microbiome and host gene expression: a review. Hum Genet. 2021;140(5):747–60. doi:10.1007/s00439-020-02237-0.
  • Enman NM, Sabban EL, McGonigle P, Van Bockstaele EJ. Targeting the neuropeptide Y system in stress-related psychiatric disorders. Neurobiol Stress. 2015;1:33–43. doi:10.1016/j.ynstr.2014.09.007.
  • Ruohonen ST, Savontaus E, Rinne P, Rosmaninho-Salgado J, Cavadas C, Ruskoaho H, Koulu M, Pesonen U. Stress-induced hypertension and increased sympathetic activity in mice overexpressing neuropeptide Y in noradrenergic neurons. Neuroendocrinol. 2009;89(3):351–360. doi:10.1159/000188602.
  • Chen DL, Dai YC, Zheng L, Chen YL, Zhang YL, Tang ZP. Features of the gut microbiota in ulcerative colitis patients with depression: a pilot study. Med (Baltimore). 2021;100(7):e24845. doi:10.1097/MD.0000000000024845.
  • McGuinness AJ, Davis JA, Dawson SL, Loughman A, Collier F, O’Hely M, Simpson CA, Green J, Marx W, Hair C. et al. A systematic review of gut microbiota composition in observational studies of major depressive disorder, bipolar disorder and schizophrenia. Mol Psychiatry. 2022;27(4):1920–1935. doi:10.1038/s41380-022-01456-3.
  • Jiang H, Ling Z, Zhang Y, Mao H, Ma Z, Yin Y, Wang W, Tang W, Tan Z, Shi J. et al. Altered fecal microbiota composition in patients with major depressive disorder. Brain Behav Immun. 2015;48:186–94. doi:10.1016/j.bbi.2015.03.016.
  • Zhou Y, Chen C, Yu H, Yang Z. Fecal microbiota changes in patients with postpartum depressive disorder. Front Cell Infect Microbiol. 2020;10:10. doi:10.3389/fcimb.2020.567268.
  • Lesniewska V, Rowland I, Cani PD, Neyrinck AM, Delzenne NM, Naughton PJ. Effect on components of the intestinal microflora and plasma neuropeptide levels of feeding lactobacillus delbrueckii , bifidobacterium lactis , and inulin to adult and elderly rats. Appl Environ Microbiol. 2006;72(10):6533–6538. doi:10.1128/AEM.00915-06.
  • Wang W, Xu T, Chen X, Dong K, Du C, Sun J, Shi C, Li X, Yang Y, Li H. et al. NPY receptor 2 mediates NPY antidepressant effect in the mPFC of LPS rat by suppressing NLRP3 signaling pathway. Mediators Inflamm. 2019;2019:1–12. doi:10.1155/2019/7898095.
  • Smialowska M, Domian H, Zieba B, Strosznajder L. Effect of lipopolysaccharide induced inflammation on neuropeptide Y neurons in mouse hippocampus. Acta Neurobiol Exp (Wars). 2009;69(3):317.
  • Haghshenas B, Nami Y, Abdullah N, Radiah D, Rosli R, Khosroushahi AY. Anti-proliferative effects of enterococcus strains isolated from fermented dairy products on different cancer cell lines. J Funct Foods. 2014;11:363–74. doi:10.1016/j.jff.2014.10.002.
  • Seishima J, Iida N, Kitamura K, Yutani M, Wang Z, Seki A, Yamashita T, Sakai Y, Honda M, Yamashita T. et al. Gut-derived enterococcus faecium from ulcerative colitis patients promotes colitis in a genetically susceptible mouse host. Genome Biol. 2019;20(1):20. doi:10.1186/s13059-019-1879-9.
  • Sava IG, Heikens E, Huebner J. Pathogenesis and immunity in enterococcal infections. Clin Microbiol Infect. 2010;16(6):533–40. doi:10.1111/j.1469-0691.2010.03213.x.
  • Golińska E. Virulence factors of enterococcus strains isolated from patients with inflammatory bowel disease. World J Gastroenterol. 2013;19(23):3562. doi:10.3748/wjg.v19.i23.3562.
  • Lin L, Zhang J. Role of intestinal microbiota and metabolites on gut homeostasis and human diseases. BMC Immunol. 2017;18(1):2. doi:10.1186/s12865-016-0187-3.
  • Gonzalez-Santana A, Diaz Heijtz R. Bacterial peptidoglycans from microbiota in neurodevelopment and behavior. Trends Mol Med. 2020;26(8):729–43. doi:10.1016/j.molmed.2020.05.003.
  • Wu L, Luo Y. Bacterial quorum-sensing systems and their role in intestinal bacteria-host crosstalk. Front Microbiol. 2021;12:611413. doi:10.3389/fmicb.2021.611413.
  • Pascale A, Marchesi N, Govoni S, Barbieri A. Targeting the microbiota in pharmacology of psychiatric disorders. Pharmacol Res. 2020;157:104856. doi:10.1016/j.phrs.2020.104856.
  • Jang HM, Lee HJ, Jang SE, Han MJ, Kim DH. Evidence for interplay among antibacterial-induced gut microbiota disturbance, neuro-inflammation, and anxiety in mice. Mucosal Immunol. 2018;11(5):1386–97. doi:10.1038/s41385-018-0042-3.
  • Tejada-Simon MV, Pestka JJ. Proinflammatory cytokine and nitric oxide induction in murine macrophages by cell wall and cytoplasmic extracts of lactic acid bacteria. J Food Protect. 1999;62(12):1435–44. doi:10.4315/0362-028X-62.12.1435.
  • Yang YI, Wang YY, Ahn JH, Kim BH, Choi JH. CCL2 overexpression is associated with paclitaxel resistance in ovarian cancer cells via autocrine signaling and macrophage recruitment. Biomed Pharmacother. 2022;153:113474. doi:10.1016/j.biopha.2022.113474.