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Research Paper

Antibiotic-induced gut dysbiosis elicits gut-brain axis relevant multi-omic signatures and behavioral and neuroendocrine changes in a nonhuman primate model

Shivdeep S. Hayera Department of Biology, University of Nebraska at Omaha, Omaha, NE, USA;b Callitrichid Research Center, University of Nebraska at Omaha, Omaha, NE, USA;c Nebraska Food for Health Center, University of Nebraska-Lincoln, Lincoln, NE, USAView further author information
,
Mackenzie Conrina Department of Biology, University of Nebraska at Omaha, Omaha, NE, USA;b Callitrichid Research Center, University of Nebraska at Omaha, Omaha, NE, USAView further author information
,
Jeffrey A. Frenchb Callitrichid Research Center, University of Nebraska at Omaha, Omaha, NE, USA;c Nebraska Food for Health Center, University of Nebraska-Lincoln, Lincoln, NE, USA;d Program in Neuroscience and Behavior, University of Nebraska at Omaha, Omaha, NE, USAView further author information
,
Andrew K. Bensonc Nebraska Food for Health Center, University of Nebraska-Lincoln, Lincoln, NE, USA;e Department of Food Science and Technology, University of Nebraska-Lincoln, Lincoln, NE, USAView further author information
,
Sophie Alvarezf Proteomics and Metabolomics Facility, Nebraska Center for Biotechnology, University of Nebraska-Lincoln, Lincoln, NE, USAView further author information
,
Kathryn Cooperg School of Interdisciplinary Informatics, College of Information Science and Technology, University of Nebraska at Omaha, Omaha, NE, USAView further author information
,
Anne Fischerf Proteomics and Metabolomics Facility, Nebraska Center for Biotechnology, University of Nebraska-Lincoln, Lincoln, NE, USAView further author information
,
Zahraa Wajih Alsafwanig School of Interdisciplinary Informatics, College of Information Science and Technology, University of Nebraska at Omaha, Omaha, NE, USAView further author information
,
William Gasperg School of Interdisciplinary Informatics, College of Information Science and Technology, University of Nebraska at Omaha, Omaha, NE, USAView further author information
,
Mallory J. Suhr Van Hautec Nebraska Food for Health Center, University of Nebraska-Lincoln, Lincoln, NE, USA;e Department of Food Science and Technology, University of Nebraska-Lincoln, Lincoln, NE, USAView further author information
,
Haley R. Hassenstaba Department of Biology, University of Nebraska at Omaha, Omaha, NE, USA;b Callitrichid Research Center, University of Nebraska at Omaha, Omaha, NE, USAView further author information
,
Shayda Azadmanesha Department of Biology, University of Nebraska at Omaha, Omaha, NE, USA;b Callitrichid Research Center, University of Nebraska at Omaha, Omaha, NE, USAView further author information
,
Missy Briardya Department of Biology, University of Nebraska at Omaha, Omaha, NE, USA;b Callitrichid Research Center, University of Nebraska at Omaha, Omaha, NE, USAView further author information
,
Skyler Gerbersa Department of Biology, University of Nebraska at Omaha, Omaha, NE, USA;b Callitrichid Research Center, University of Nebraska at Omaha, Omaha, NE, USAView further author information
,
Aliyah Jabenisa Department of Biology, University of Nebraska at Omaha, Omaha, NE, USA;b Callitrichid Research Center, University of Nebraska at Omaha, Omaha, NE, USAView further author information
,
Jennifer L. Thompsona Department of Biology, University of Nebraska at Omaha, Omaha, NE, USA;b Callitrichid Research Center, University of Nebraska at Omaha, Omaha, NE, USAView further author information
&
Jonathan B. Claytona Department of Biology, University of Nebraska at Omaha, Omaha, NE, USA;b Callitrichid Research Center, University of Nebraska at Omaha, Omaha, NE, USA;c Nebraska Food for Health Center, University of Nebraska-Lincoln, Lincoln, NE, USA;e Department of Food Science and Technology, University of Nebraska-Lincoln, Lincoln, NE, USA;h Department of Pathology and Microbiology, University of Nebraska Medical Center, Omaha, NE, USA;i Primate Microbiome Project, University of Nebraska-Lincoln, Lincoln, NE, USACorrespondence[email protected]
ORCID Iconhttps://orcid.org/0000-0003-3709-3362View further author information
ORCID Icon show all
Article: 2305476 | Received 02 Jun 2023, Accepted 10 Jan 2024, Published online: 29 Jan 2024

References

  • Cheung SG, Goldenthal AR, Uhlemann A-C, Mann JJ, Miller JM, Sublette ME. Systematic review of gut microbiota and major depression. Front Psychiatry. 2019;10:34. doi:10.3389/fpsyt.2019.00034.
  • Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S. Host-gut microbiota metabolic interactions. Sci. 2012;336(6086):1262–26. doi:10.1126/science.1223813.
  • Brown CT, Davis-Richardson AG, Giongo A, Gano KA, Crabb DB, Mukherjee N, Casella G, Drew JC, Ilonen J, Knip M. et al. Gut microbiome metagenomics analysis suggests a functional model for the development of autoimmunity for type 1 diabetes. PloS ONE. 2011;6(10):e25792. doi:10.1371/journal.pone.0025792.
  • Borre YE, O’Keeffe GW, Clarke G, Stanton C, Dinan TG, Cryan JF. Microbiota and neurodevelopmental windows: implications for brain disorders. Trends Mol Med. 2014;20(9):509–518. doi:10.1016/j.molmed.2014.05.002.
  • Thomas CM, Hong T, van Pijkeren JP, Hemarajata P, Trinh DV, Hu W, Britton RA, Kalkum M, Versalovic J. Histamine derived from probiotic lactobacillus reuteri suppresses TNF via modulation of PKA and ERK signaling. PloS ONE. 2012;7(2):e31951. doi:10.1371/journal.pone.0031951.
  • Barrett E, Ross RP, O’Toole PW, Fitzgerald GF, Stanton C. γ-Aminobutyric acid production by culturable bacteria from the human intestine. J Appl Microbiol. 2012;113(2):411–417. doi:10.1111/j.1365-2672.2012.05344.x.
  • Kawashima K, Misawa H, Moriwaki Y, Fujii YX, Fujii T, Horiuchi Y, Yamada T, Imanaka T, Kamekura M. Ubiquitous expression of acetylcholine and its biological functions in life forms without nervous systems. Life Sci. 2007;80(24–25):2206–2209. doi:10.1016/j.lfs.2007.01.059.
  • Rosin S, Xia K, Azcarate-Peril MA, Carlson AL, Propper CB, Thompson AL, Grewen K, Knickmeyer RC. A preliminary study of gut microbiome variation and HPA axis reactivity in healthy infants. Psychoneuroendocrinology. 2021;124:105046. doi:10.1016/j.psyneuen.2020.105046.
  • Hantsoo L, Jašarević E, Criniti S, McGeehan B, Tanes C, Sammel MD, Elovitz MA, Compher C, Wu G, Epperson CN. Childhood adversity impact on gut microbiota and inflammatory response to stress during pregnancy. Brain Behav Immun. 2019;75:240–250. doi:10.1016/j.bbi.2018.11.005.
  • Michels N, Van de Wiele T, Fouhy F, O’Mahony S, Clarke G, Keane J. Gut microbiome patterns depending on children’s psychosocial stress: reports versus biomarkers. Brain, Behav, Immun. 2019;80:751–762. doi:10.1016/j.bbi.2019.05.024.
  • Hayer SS, Hwang S, Clayton JB. Antibiotic-induced gut dysbiosis and cognitive, emotional, and behavioral changes in rodents: a systematic review and meta-analysis. Front Neurosci. 2023;17:1237177. doi:10.3389/fnins.2023.1237177.
  • Messaoudi M, Lalonde R, Violle N, Javelot H, Desor D, Nejdi A, Bisson J-F, Rougeot C, Pichelin M, Cazaubiel M. et al. Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects. Br J Nutr. 2011;105(5):755–764. doi:10.1017/S0007114510004319.
  • Liu Y, Sanderson D, Firoz Mian M, Neufeld K-A, Forsythe P. Loss of vagal integrity disrupts immune components of the microbiota-gut-brain axis and inhibits the effect of lactobacillus rhamnosus on behavior and the corticosterone stress response. Neuropharmacology. 2021;195:108682. doi:10.1016/j.neuropharm.2021.108682.
  • Petersen C, Round JL. Defining dysbiosis and its influence on host immunity and disease. Cell Microbiol. 2014;16(7):1024–1033. doi:10.1111/cmi.12308.
  • Yang Y, Jobin C. Microbial imbalance and intestinal pathologies: connections and contributions. Dis Model Mech. 2014;7(10):1131–1142. doi:10.1242/dmm.016428.
  • Hawrelak JA, Myers SP. The causes of intestinal dysbiosis: a review. Altern Med Rev. 2004;9:180–197.
  • Zimmermann P, Curtis N. The effect of antibiotics on the composition of the intestinal microbiota - a systematic review. J Infect. 2019;79(6):471–489. doi:10.1016/j.jinf.2019.10.008.
  • Hao W-Z, Li X-J, Zhang P-W, Chen J-X. A review of antibiotics, depression, and the gut microbiome. Psychiatry Res. 2020;284:112691. doi:10.1016/j.psychres.2019.112691.
  • Sarkar A, Harty S, Lehto SM, Moeller AH, Dinan TG, Dunbar RIM, Cryan JF, Burnet PWJ. The microbiome in psychology and cognitive neuroscience. Trends Cogn Sci. 2018;22(7):611–636. doi:10.1016/j.tics.2018.04.006.
  • Zheng P, Wu J, Zhang H, Perry SW, Yin B, Tan X, Chai T, Liang W, Huang Y, Li Y. et al. The gut microbiome modulates gut–brain axis glycerophospholipid metabolism in a region-specific manner in a nonhuman primate model of depression. Mol Psychiatry. 2020;26(6):2380–2392. doi:10.1038/s41380-020-0744-2.
  • Burkart JM, Finkenwirth C. Marmosets as model species in neuroscience and evolutionary anthropology. Neurosci Res (N Y). 2015;93:8–19. doi:10.1016/j.neures.2014.09.003.
  • Smith TE, French JA. Psychosocial stress and urinary cortisol excretion in marmoset monkeys. Physiology & Behavior. 1997;62(2):225–232. doi:10.1016/S0031-9384(97)00103-0.
  • Sousa MBCD, de Sousa MBC, de Menezes Galvão AC, Sales CJR, de Castro DC, Galvão-Coelho NL. Endocrine and cognitive adaptations to cope with stress in immature common marmosets (Callithrix jacchus): sex and age matter. Front Psychiatry. 2015;6:6. doi:10.3389/fpsyt.2015.00160.
  • Miller CT, Freiwald WA, Leopold DA, Mitchell JF, Silva AC, Wang X. Marmosets: a neuroscientific model of human social behavior. Neuron. 2016;90:219–233. doi:10.1016/j.neuron.2016.03.018.
  • Malukiewicz J, Cartwright RA, Dergam JA, Igayara CS. The effects of Host Taxon, hybridization, and environment on the gut microbiome of callithrix marmosets. bioRxiv. 2019.
  • Rao S, Kupfer Y, Pagala M, Chapnick E, Tessler S. Systemic absorption of oral vancomycin in patients with Clostridium difficile infection. Scand J Infect Dis. 2011;43(5):386–388. doi:10.3109/00365548.2010.544671.
  • Carnicle JM, Tran TV, McKissack SS. Systemic contact dermatitis following oral neomycin therapy. Baylor Univ Med Center Proc. 2020;34(1):89–90. doi:10.1080/08998280.2020.1805671.
  • Sylvia KE, Jewell CP, Rendon NM, St John EA, Demas GE. Sex-specific modulation of the gut microbiome and behavior in Siberian hamsters. Brain Behav Immun. 2017;60:51–62. doi:10.1016/j.bbi.2016.10.023.
  • Dalgic N, Sancar M, Bayraktar B, Dincer E, Pelit S. Ertapenem for the treatment of urinary tract infections caused by extended-spectrum β-lactamase-producing bacteria in children. Scand J Infect Dis. 2011;43(5):339–343. doi:10.3109/00365548.2011.553241.
  • Zhu L, Clayton JB, Suhr Van Haute MJ, Yang Q, Hassenstab HR, Mustoe AC, Knights D, Benson AK, French JA. Sex bias in gut microbiome transmission in newly paired marmosets (Callithrix jacchus). mSystems. 2020;5(2):5. doi:10.1128/mSystems.00910-19.
  • French JA, Brewer KJ, Schaffner CM, Schalley J, Hightower-Merritt D, Smith TE, Bell SM. Urinary steroid and gonadotropin excretion across the reproductive cycle in female Wied’s black tufted-ear marmosets (callithrix kuhli). Am J Primatol. 1996;40(3):231–245. doi:10.1002/(SICI)1098-2345(1996)40:3<231:AID-AJP2>3.0.CO;2-Z.
  • Glymour MM, Weuve J, Berkman LF, Kawachi I, Robins JM. When is baseline adjustment useful in analyses of change? An example with education and cognitive change. Am J Epidemiol. 2005;162(3):267–278. doi:10.1093/aje/kwi187.
  • Jang H-M, Lee H-J, Jang S-E, Han MJ, Kim D-H. Evidence for interplay among antibacterial-induced gut microbiota disturbance, neuro-inflammation, and anxiety in mice. Mucosal Immunol. 2018;11(5):1386–1397. doi:10.1038/s41385-018-0042-3.
  • Fröhlich EE, Farzi A, Mayerhofer R, Reichmann F, Jačan A, Wagner B, Zinser E, Bordag N, Magnes C, Fröhlich E. et al. Cognitive impairment by antibiotic-induced gut dysbiosis: analysis of gut microbiota-brain communication. Brain Behav Immun. 2016;56:140–155. doi:10.1016/j.bbi.2016.02.020.
  • Reyes REN, Al Omran AJ, Davies DL, Asatryan L. Antibiotic-induced disruption of commensal microbiome linked to increases in binge-like ethanol consumption behavior. Brain Res. 2020;1747:147067. doi:10.1016/j.brainres.2020.147067.
  • Hoban AE, Moloney RD, Golubeva AV, McVey Neufeld KA, O’Sullivan O, Patterson E, Stanton C, Dinan TG, Clarke G, Cryan JF. Behavioural and neurochemical consequences of chronic gut microbiota depletion during adulthood in the rat. Neuroscience. 2016;339:463–477. doi:10.1016/j.neuroscience.2016.10.003.
  • Brennan CA, Garrett WS. Fusobacterium nucleatum — symbiont, opportunist and oncobacterium. Nat Rev Microbiol. 2019;17(3):156–166. doi:10.1038/s41579-018-0129-6.
  • Han YW. Fusobacterium nucleatum: a commensal-turned pathogen. Curr Opin Microbiol. 2015;23:141–147. doi:10.1016/j.mib.2014.11.013.
  • Simpson CA, Adler C, du Plessis MR, Landau ER, Dashper SG, Reynolds EC, Schwartz OS, Simmons JG. Oral microbiome composition, but not diversity, is associated with adolescent anxiety and depression symptoms. Physiology & Behavior. 2020;226:113126. doi:10.1016/j.physbeh.2020.113126.
  • Wingfield B, Lapsley C, McDowell A, Miliotis G, McLafferty M, O’Neill SM, Coleman S, McGinnity TM, Bjourson AJ, Murray EK. Variations in the oral microbiome are associated with depression in young adults. Sci Rep. 2021;11(1):15009. doi:10.1038/s41598-021-94498-6.
  • Qin Q, Liu H, Yang Y, Wang Y, Xia C, Tian P, Wei J, Li S, Chen T. Probiotic Supplement Preparation Relieves Test Anxiety by Regulating Intestinal Microbiota in College Students. Dis Markers. 2021;2021:5597401. doi:10.1155/2021/5597401.
  • Zhu L, Yang Q, Suhr Van Haute MJ, Kok CR. Captive common marmosets (Callithrix jacchus) are colonized throughout their lives by a community of bifidobacterium species with species-specific genomic content that can support adaptation to distinct metabolic niches. MBio. 2021;12(4):10–128. doi:10.1128/mBio.01153-21.
  • Messaoudi M, Violle N, Bisson J-F, Desor D, Javelot H, Rougeot C. Beneficial psychological effects of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in healthy human volunteers. Gut Microbes. 2011;2(4):256–261. doi:10.4161/gmic.2.4.16108.
  • Allen AP, Hutch W, Borre YE, Kennedy PJ, Temko A, Boylan G, Murphy E, Cryan JF, Dinan TG, Clarke G. Bifidobacterium longum 1714 as a translational psychobiotic: modulation of stress, electrophysiology and neurocognition in healthy volunteers. Transl Psychiatry. 2016;6(11):e939. doi:10.1038/tp.2016.191.
  • Cavanaugh J, Carp SB, Rock CM, French JA. Oxytocin modulates behavioral and physiological responses to a stressor in marmoset monkeys. Psychoneuroendocrinology. 2016;66:22–30. doi:10.1016/j.psyneuen.2015.12.027.
  • Taylor SE, Klein LC, Lewis BP, Gruenewald TL, Gurung RA, Updegraff JA. Biobehavioral responses to stress in females: tend-and-befriend, not fight-or-flight. Psychol Rev. 2000;107(3):411–429. doi:10.1037/0033-295X.107.3.411.
  • Cohen S, Wills TA. Stress, social support, and the buffering hypothesis. Psychol Bull. 1985;98(2):310–357. doi:10.1037/0033-2909.98.2.310.
  • Rukstalis M, French JA. Vocal buffering of the stress response: exposure to conspecific vocalizations moderates urinary cortisol excretion in isolated marmosets. Horm Behav. 2005;47(1):1–7. doi:10.1016/j.yhbeh.2004.09.004.
  • Smith TE, McGreer-Whitworth B, French JA. Close proximity of the heterosexual partner reduces the physiological and behavioral consequences of novel-cage housing in black tufted-ear marmosets (callithrix kuhli). Horm Behav. 1998;34(3):211–222. doi:10.1006/hbeh.1998.1469.
  • Mustoe AC, Taylor JH, Birnie AK, Huffman MC, French JA. Gestational cortisol and social play shape development of marmosets’ HPA functioning and behavioral responses to stressors. Dev Psychobiol. 2014;56(6):1229–1243. doi:10.1002/dev.21203.
  • Olavarría-Ramírez L, Cooney-Quane J, Murphy G, McCafferty CP, Cryan JF, Dockray S. A systematic review of the effects of gut microbiota depletion on social and anxiety-related behaviours in adult rodents: implications for translational research. Neurosci Biobehav Rev. 2023;145:105013. doi:10.1016/j.neubiorev.2022.105013.
  • Klein LC, Corwin EJ. Seeing the unexpected: how sex differences in stress responses may provide a new perspective on the manifestation of psychiatric disorders. Curr Psychiatry Rep. 2002;4(6):441–448. doi:10.1007/s11920-002-0072-z.
  • Ågmo A, Smith AS, Birnie AK, French JA. Behavioral characteristics of pair bonding in the black tufted-ear marmoset (Callithrix penicillata). Behaviour. 2012;149(3–4):407–440. doi:10.1163/156853912X638454.
  • Ross CN, Adams J, Gonzalez O, Dick E, Giavedoni L, Hodara VL, Phillips K, Rigodanzo AD, Kasinath B, Tardif SD. Cross-sectional comparison of health-span phenotypes in young versus geriatric marmosets. Am J Primatol. 2019;81(2):e22952. doi:10.1002/ajp.22952.
  • Ross CN, French JA, Patera KJ. Intensity of aggressive interactions modulates testosterone in male marmosets. Physiology & Behavior. 2004;83(3):437–445. doi:10.1016/j.physbeh.2004.08.036.
  • Ross CN, French JA. Female marmosets’ behavioral and hormonal responses to unfamiliar intruders. Am J Primatol. 2011;73(10):1072–1081. doi:10.1002/ajp.20975.
  • Emile N, Barros M. Recognition of a 3D snake model and its 2D photographic image by captive black tufted-ear marmosets (Callithrix penicillata). Anim Cogn. 2009;12(5):725–732. doi:10.1007/s10071-009-0234-z.
  • Nedley N, Ramirez FE. Nedley depression hit hypothesis: identifying depression and its causes. Am J Lifestyle Med. 2016;10(6):422–428. doi:10.1177/1559827614550779.
  • Silva YP, Bernardi A, Frozza RL. The role of short-chain fatty acids from gut microbiota in gut-brain communication. Front Endocrinol. 2020;11:11. doi:10.3389/fendo.2020.00025.
  • O’Riordan KJ, Collins MK, Moloney GM, Knox EG, Aburto MR, Fülling C, Morley SJ, Clarke G, Schellekens H, Cryan JF. Short chain fatty acids: microbial metabolites for gut-brain axis signalling. Mol Cell Endocrinol. 2022;546:111572. doi:10.1016/j.mce.2022.111572.
  • Mertens KL, Kalsbeek A, Soeters MR, Eggink HM. Bile acid signaling pathways from the Enterohepatic Circulation to the central nervous system. Front Neurosci. 2017;11:617. doi:10.3389/fnins.2017.00617.
  • Wei W, Wang H-F, Zhang Y, Zhang Y-L, Niu B-Y, Yao S-K. Altered metabolism of bile acids correlates with clinical parameters and the gut microbiota in patients with diarrhea-predominant irritable bowel syndrome. World J Gastroenterol. 2020;26(45):7153–7172. doi:10.3748/wjg.v26.i45.7153.
  • Ridlon JM, Harris SC, Bhowmik S, Kang D-J, Hylemon PB. Consequences of bile salt biotransformations by intestinal bacteria. Gut Microbes. 2016;7(1):22–39. doi:10.1080/19490976.2015.1127483.
  • Guzior DV, Quinn RA. Review: microbial transformations of human bile acids. Microbiome. 2021;9(1):140. doi:10.1186/s40168-021-01101-1.
  • Feng L, Zhou N, Li Z, Fu D, Guo Y, Gao X, Liu X. Co-occurrence of gut microbiota dysbiosis and bile acid metabolism alteration is associated with psychological disorders in Crohn’s disease. FASEB J. 2022;36(1):e22100. doi:10.1096/fj.202101088RRR.
  • Golubeva AV, Joyce SA, Moloney G, Burokas A, Sherwin E, Arboleya S, Flynn I, Khochanskiy D, Moya-Pérez A, Peterson V. et al. Microbiota-related changes in bile acid & tryptophan metabolism are associated with gastrointestinal dysfunction in a mouse model of autism. EBioMedicine. 2017;24:166–178. doi:10.1016/j.ebiom.2017.09.020.
  • Aaldijk E, Vermeiren Y. The role of serotonin within the microbiota-gut-brain axis in the development of Alzheimer’s disease: a narrative review. Ageing Res Rev. 2022;75:101556. doi:10.1016/j.arr.2021.101556.
  • Oldendorf WH. Brain uptake of radiolabeled amino acids, amines, and hexoses after arterial injection. Am J Physiol. 1971;221(6):1629–1639. doi:10.1152/ajplegacy.1971.221.6.1629.
  • Clarke G, Grenham S, Scully P, Fitzgerald P, Moloney RD, Shanahan F, Dinan TG, Cryan JF. The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Mol Psychiatry. 2013;18(6):666–673. doi:10.1038/mp.2012.77.
  • Sobko T, Liang S, Cheng WHG, Tun HM. Impact of outdoor nature-related activities on gut microbiota, fecal serotonin, and perceived stress in preschool children: the Play&Grow randomized controlled trial. Sci Rep. 2020;10(1):10. doi:10.1038/s41598-020-78642-2.
  • Petroff OAC. Book review: GABA and glutamate in the human brain. Neuroscientist. 2002;8(6):562–573. doi:10.1177/1073858402238515.
  • Meeder E, Matzaraki V, Vadaq N, van de Wijer L, van der Ven A, Schellekens A. Unbiased metabolomics links fatty acid pathways to psychiatric symptoms in people living with HIV. J Clin Med Res. 2021;10(23):10. doi:10.3390/jcm10235466.
  • Yang J, Zheng P, Li Y, Wu J, Tan X, Zhou J, Sun Z, Chen X, Zhang G, Zhang H. et al. Landscapes of bacterial and metabolic signatures and their interaction in major depressive disorders. Sci Adv. 2020;6(49):6. doi:10.1126/sciadv.aba8555.
  • Liang S, Sin ZY, Yu J, Zhao S, Xi Z, Bruzzone R, Tun HM. Multi-cohort analysis of depression-associated gut bacteria sheds insight on bacterial biomarkers across populations. Cell Mol Life Sci. 2023;80(1):80. doi:10.1007/s00018-022-04650-2.
  • Neis E, Dejong C, Rensen S. The role of microbial amino acid metabolism in Host metabolism. Nutrients. 2015;7(4):2930–2946. doi:10.3390/nu7042930.
  • Perna AF, Anishchenko E, Vigorito C, Zacchia M, Trepiccione F, D’Aniello S, Ingrosso D. Zebrafish, a Novel Model System to study uremic toxins: the case for the sulfur amino acid lanthionine. Int J Mol Sci. 2018;19(5):1323. doi:10.3390/ijms19051323.
  • Wang W-W, Zhang Y, Huang X-B, You N, Zheng L, Li J. Fecal microbiota transplantation prevents hepatic encephalopathy in rats with carbon tetrachloride-induced acute hepatic dysfunction. World J Gastroenterol. 2017;23(38):6983–6994. doi:10.3748/wjg.v23.i38.6983.
  • Lane H-Y, Lin C-H, Green MF, Hellemann G, Huang C-C, Chen P-W, Tun R, Chang Y-C, Tsai GE. Add-on treatment of benzoate for schizophrenia: a randomized, double-blind, placebo-controlled trial of D-amino acid oxidase inhibitor. JAMA Psychiarty. 2013;70(12):1267–1275. doi:10.1001/jamapsychiatry.2013.2159.

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