Increased butyrate priming in the gut stalls microbiome associated-gastrointestinal inflammation and hepatic metabolic reprogramming in a mouse model of Gulf War Illness
Open accessAbstract
Most of the associated pathologies in Gulf War Illness (GWI) have been ascribed to chemical and pharmaceutical exposures during the war. Since an increased number of veterans complain of gastrointestinal (GI), neuroinflammatory and metabolic complications as they age and there are limited options for a cure, the present study was focused to assess the role of butyrate, a short chain fatty acid for attenuating GWI-associated GI and metabolic complications. Results in a GWI-mouse model of permethrin and pyridostigmine bromide (PB) exposure showed that oral butyrate restored gut homeostasis and increased GPR109A receptor copies in the small intestine (SI). Claudin-2, a protein shown to be upregulated in conditions of leaky gut was significantly decreased following butyrate administration. Butyrate decreased TLR4 and TLR5 expressions in the liver concomitant to a decrease in TLR4 activation. GW-chemical exposure showed no clinical signs of liver disease but a significant alteration of metabolic markers such as SREBP1c, PPAR-α, and PFK was evident. Liver markers for lipogenesis and carbohydrate metabolism that were significantly upregulated following GW chemical exposure were attenuated by butyrate priming in vivo and in human primary hepatocytes. Further, Glucose transporter Glut-4 that was shown to be elevated following liver complications were significantly decreased in these mice after butyrate administration. Finally, use of TLR4 KO mice completely attenuated the liver metabolic changes suggesting the central role of these receptors in the GWI pathology. In conclusion, we report a butyrate specific mechanistic approach to identify and treat increased metabolic abnormalities in GWI veterans with systemic inflammation, chronic fatigue, GI disturbances, metabolic complications and weight gain.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Alterations in the microbiota may lead to leaky gut and endotoxemia, exacerbating neuroinflammation and activation of Toll-like receptors (specifically TLR4) in the small intestine and brain.
“Alhasson (67) observed simultaneous intestinal inflammation and neuroinflammation in a mouse model of Gulf War disease, suggesting that alterations in the microbiota may lead to leaky gut and endotoxemia, exacerbating neuroinflammation and activation of Toll-like receptors (specifically, TLR4) in the small intestine and brain.”
From Modulation of the gut–brain axis via the gut microbiota: a new era in treatment of amyotrophic lateral sclerosis (2023) · cites this paper as [67]
Activation of TLR4 due to changes in gut microbiota composition and gut permeability leads to the release of pro-inflammatory cytokines and endotoxins from astrocytes and microglia.
“In addition, activation of TLR4 due to changes in gut microbiota composition and gut permeability further leads to the release of pro-inflammatory cytokines, endotoxins (LSP) (67), etc., from astrocytes and from the microglia themselves.”
From Modulation of the gut–brain axis via the gut microbiota: a new era in treatment of amyotrophic lateral sclerosis (2023) · cites this paper as [67]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity
Henao-Mejia, J., Elinav, E., Jin, C., Hao, L., Mehal, W. Z., Strowig, T., Thaiss, C. A., Kau, A. L., Eisenbarth, S. C., Jurczak, M. J., et al. (2012) · Nature · doi:10.1038/nature10809 · Cited by 2,435 · see citing works
Singh, N., Gurav, A., Sivaprakasam, S., Brady, E., Padia, R., Shi, H., Thangaraju, M., Prasad, P. D., Manicassamy, S., Munn, D. H., et al. (2014) · Immunity · doi:10.1016/j.immuni.2013.12.007 · Cited by 2,368 · see citing works
Chang, P. V., Hao, L., Offermanns, S., & Medzhitov, R. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1322269111 · Cited by 2,175 · see citing works
Badman, M. K., Pissios, P., Kennedy, A. R., Koukos, G., Flier, J. S., & Maratos-Flier, E. (2007) · Cell Metabolism · doi:10.1016/j.cmet.2007.05.002 · Cited by 1,495 · see citing works
Butyrate inhibits inflammatory responses through NFκB inhibition: implications for Crohn's disease
Segain, J.-P., de la Blétière, D. R., Bourreille, A., Leray, V., Gervois, N., Rosales, C., Ferrier, L., Bonnet, C., Blottière, H. M., & Galmiche, J.-P. (2000) · Gut · doi:10.1136/gut.47.3.397 · Cited by 1,325 · see citing works
PAMP s and DAMP s: signal 0s that spur autophagy and immunity
Tang, D., Kang, R., Coyne, C. B., Zeh, H. J., & Lotze, M. T. (2012) · Immunological Reviews · doi:10.1111/j.1600-065x.2012.01146.x · Cited by 1,250 · see citing works
Microbiota metabolite short chain fatty acids, GPCR, and inflammatory bowel diseases
Sun, M., Wu, W. H., Liu, Z., & Cong, Y. (2016) · Journal of Gastroenterology · doi:10.1007/s00535-016-1242-9 · Cited by 1,071 · see citing works
The interaction of hepatic lipid and glucose metabolism in liver diseases
Bechmann, L. P., Hannivoort, R. A., Gerken, G., Hotamışlıgil, G. S., Trauner, M., & Canbay, A. E. (2011) · Journal of Hepatology · doi:10.1016/j.jhep.2011.08.025 · Cited by 992 · see citing works
LeBlanc, J. G., Chain, F., Martín, R., Bermúdez‐Humarán, L. G., Courau, S., & Langella, P. (2017) · Microbial Cell Factories · doi:10.1186/s12934-017-0691-z · Cited by 881 · see citing works
Lipotoxicity and the gut-liver axis in NASH pathogenesis
Marra, F., & Svegliati-Baroni, G. (2018) · Journal of Hepatology · doi:10.1016/j.jhep.2017.11.014 · Cited by 847 · see citing works
Imhann, F., Vich Vila, A., Bonder, M. J., Fu, J., Gevers, D., Visschedijk, M. C., Spekhorst, L. M., Alberts, R., Franke, L., van Dullemen, H. M., et al. (2018) · Gut · doi:10.1136/gutjnl-2016-312135 · Cited by 788 · see citing works
Carey, E. J., Ali, A. H., & Lindor, K. D. (2015) · The Lancet · doi:10.1016/s0140-6736(15)00154-3 · Cited by 735 · see citing works
Zheng, L., Kelly, C. J., Battista, K. D., Schaefer, R., Lanis, J. M., Alexeev, E. E., Wang, R. X., Onyiah, J. C., Kominsky, D. J., & Colgan, S. P. (2017) · The Journal of Immunology · doi:10.4049/jimmunol.1700105 · Cited by 549 · see citing works
Activation of Toll-like receptor 4 is associated with insulin resistance in adipocytes
Song, M. J., Kim, K. H., Yoon, J. M., & Kim, J. B. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.05.170 · Cited by 454 · see citing works
White, R. F., Steele, L., O'Callaghan, J. P., Sullivan, K. A., Binns, J. H., Golomb, B. A., Bloom, F. E., Bunker, J. A., Crawford, F., Graves, J. C., et al. (2015) · Cortex · doi:10.1016/j.cortex.2015.08.022 · Cited by 433 · see citing works
Self-citationMetabolic endotoxemia with obesity: Is it real and is it relevant?
Boutagy, N. E., McMillan, R. P., Frisard, M. I., & Hulver, M. W. (2016) · Biochimie · doi:10.1016/j.biochi.2015.06.020 · Cited by 413 · see citing works
NF-κB controls energy homeostasis and metabolic adaptation by upregulating mitochondrial respiration
Mauro, C., Leow, S. C., Ansó, E., Rocha, S., Thotakura, A. K., Tornatore, L., Moretti, M., Smaele, E. D., Beg, A. A., Tergaonkar, V., et al. (2011) · Nature Cell Biology · doi:10.1038/ncb2324 · Cited by 393 · see citing works
Metabolic features of chronic fatigue syndrome
Naviaux, R. K., Naviaux, J. C., Li, K., Bright, A. T., Alaynick, W. A., Wang, L., Baxter, A., Nathan, N., Anderson, W. H., & Gordon, E. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1607571113 · Cited by 393 · see citing works
Oishi, Y., Spann, N. J., Link, V. M., Muse, E. D., Strid, T., Edillor, C., Kolar, M. J., Matsuzaka, T., Hayakawa, S., Tao, J., et al. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2016.11.009 · Cited by 342 · see citing works
Giloteaux, L., Goodrich, J. K., Walters, W. A., Levine, S. M., Ley, R. E., & Hanson, M. R. (2016) · Microbiome · doi:10.1186/s40168-016-0171-4 · Cited by 339 · see citing works
Leptin secretion and leptin receptor in the human stomach
Sobhani, I., Bado, A., Vissuzaine, C., Buyse, M., Kermorgant, S., Laigneau, J.-P., Attoub, S., Lehy, T., Hénin, D., Mignon, M., et al. (2000) · Gut · doi:10.1136/gut.47.2.178 · Cited by 336 · see citing works
Sappington, P. L., Yang, R., Yang, H., Tracey, K. J., Delude, R. L., & Fink, M. P. (2002) · Gastroenterology · doi:10.1053/gast.2002.35391 · Cited by 319 · see citing works
Claudin-2 as a mediator of leaky gut barrier during intestinal inflammation
Luettig, J., Rosenthal, R., Barmeyer, C., & Jd, S. (2015) · Tissue Barriers · doi:10.4161/21688370.2014.977176 · Cited by 281 · see citing works
Hedgehog Controls Hepatic Stellate Cell Fate by Regulating Metabolism
Chen, Y., Choi, S. S., Michelotti, G., Chan, I. S., Swiderska-Syn, M., Karaca, G., Xie, G., Moylan, C. A., Garibaldi, F., Premont, R., et al. (2012) · Gastroenterology · doi:10.1053/j.gastro.2012.07.115 · Cited by 279 · see citing works
Mechanisms of triglyceride accumulation in activated macrophages
Feingold, K. R., Shigenaga, J. K., Kazemi, M. R., McDonald, C. M., Patzek, S. M., Cross, A. S., Moser, A. H., & Grünfeld, C. (2012) · Journal of Leukocyte Biology · doi:10.1189/jlb.1111537 · Cited by 249 · see citing works
ChREBP: A Glucose-activated Transcription Factor Involved in the Development of Metabolic Syndrome
Iizuka, K., & Horikawa, Y. (2008) · Endocrine Journal · doi:10.1507/endocrj.k07e-110 · Cited by 222 · see citing works
Nagy‐Szakal, D., Williams, B. L., Mishra, N., Che, X., Lee, B., Bateman, L., Klimas, N. G., Komaroff, A. L., Levine, S. M., Montoya, J. G., et al. (2017) · Microbiome · doi:10.1186/s40168-017-0261-y · Cited by 221 · see citing works
Butyrate inhibits interleukin-17 and generates Tregs to ameliorate colorectal colitis in rats
Zhang, M., Zhou, Q., Dorfman, R. G., Huang, X., Fan, T., Zhang, H., Zhang, J., & Yu, C. (2016) · BMC Gastroenterology · doi:10.1186/s12876-016-0500-x · Cited by 210 · see citing works
Milić, S., & Štimac, D. (2012) · Digestive Diseases · doi:10.1159/000336669 · Cited by 191 · see citing works
Hepatic expression and cellular distribution of the glucose transporter family
Karim, S. (2012) · World Journal of Gastroenterology · doi:10.3748/wjg.v18.i46.6771 · Cited by 190 · see citing works
Schreuder, T. C. M. A., Verwer, B. J., van Nieuwkerk, C. M., & Mulder, C. J. J. (2008) · World Journal of Gastroenterology · doi:10.3748/wjg.14.2474 · Cited by 189 · see citing works
Parihar, V. K., Hattiangady, B., Shuai, B., & Shetty, A. K. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.158 · Cited by 176 · see citing works
Chiu, C.-C., Ching, Y.-H., Li, Y.-P., Liu, J.-Y., Huang, Y.-T., Huang, Y.-W., Yang, S.-S., Huang, W.-C., & Chuang, H.-L. (2017) · Nutrients · doi:10.3390/nu9111220 · Cited by 160 · see citing works
O'Callaghan, J. P., Kelly, K. A., Locker, A. R., Miller, D. B., & Lasley, S. M. (2015) · Journal of Neurochemistry · doi:10.1111/jnc.13088 · Cited by 154 · see citing works
Self-citationAlhasson, F. A., Das, S., Seth, R. K., Dattaroy, D., Chandrashekaran, V., Ryan, C. N., Chan, L. S., Testerman, T. L., Burch, J. B., Hofseth, L. J., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0172914 · Cited by 152 · see citing works
Self-citationKhan, S., & Jena, G. (2014) · Food and Chemical Toxicology · doi:10.1016/j.fct.2014.08.010 · Cited by 137 · see citing works
Chatterjee, S., Ganini, D., Tokar, E. J., Kumar, A., Das, S., Corbett, J. T., Kadiiska, M. B., Waalkes, M. P., Diehl, A. M., & Mason, R. P. (2012) · Journal of Hepatology · doi:10.1016/j.jhep.2012.11.035 · Cited by 134 · see citing works
Self-citationAnderson‐Baucum, E. K., Hill, A. A., & Hasty, A. H. (2012) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.112.250142 · Cited by 118 · see citing works
Duodenal Leptin Stimulates Cholecystokinin Secretion
Guilmeau, S., Buyse, M., Tsocas, A., Laigneau, J., & Bado, A. (2003) · Diabetes · doi:10.2337/diabetes.52.7.1664 · Cited by 110 · see citing works
Reichardt, F., Chassaing, B., Nezami, B. G., Li, G., Tabatabavakili, S., Mwangi, S. M., Uppal, K., Liang, B., Vijay–Kumar, M., Jones, D. P., et al. (2016) · The Journal of Physiology · doi:10.1113/jp273269 · Cited by 109 · see citing works
Competitive inhibition of histone deacetylase activity by trichostatin A and butyrate
Sekhavat, A., Sun, J., & Davie, J. (2007) · Biochemistry and Cell Biology · doi:10.1139/o07-145 · Cited by 108 · see citing works
Khan, S., & Jena, G. (2015) · Epigenomics · doi:10.2217/epi.15.20 · Cited by 101 · see citing works
Sullivan, K. A., Krengel, M., Bradford, W., Stone, C., Thompson, T. A., Heeren, T., & White, R. F. (2017) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2017.11.002 · Cited by 100 · see citing works
Self-citationInstitute of Medicine (2000) · National Academies Press eBooks · doi:10.17226/9953 · Cited by 94 · see citing works
Koslik, H. J., Hamilton, G., & Golomb, B. A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0092887 · Cited by 87 · see citing works
Insights into the Hexose Liver Metabolism—Glucose versus Fructose
Geidl-Flueck, B., & Gerber, P. (2017) · Nutrients · doi:10.3390/nu9091026 · Cited by 85 · see citing works
Doycheva, I., Watt, K. D. S., Rifai, G., Mrad, R. A., López, R., Zein, N. N., Carey, W. D., & Alkhouri, N. (2017) · Digestive Diseases and Sciences · doi:10.1007/s10620-017-4492-3 · Cited by 83 · see citing works
Koo, B., Michalovicz, L. T., Calderazzo, S. M., Kelly, K. A., Sullivan, K. A., Killiany, R., & O'Callaghan, J. P. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.08.003 · Cited by 82 · see citing works
Self-citationChandrashekaran, V., Seth, R. K., Dattaroy, D., Alhasson, F. A., Ziolenka, J., Carson, J. A., Berger, F. G., Kalyanaraman, B., Diehl, A. M., & Chatterjee, S. (2017) · Redox Biology · doi:10.1016/j.redox.2017.05.005 · Cited by 72 · see citing works
Self-citationCholinergic Autonomic Dysfunction in Veterans With Gulf War Illness
Haley, R. W., Charuvastra, E., Shell, W. E., Buhner, D. M., Marshall, W. W., Biggs, M. M., Hopkins, S., Wolfe, G. I., & Vernino, S. A. (2012) · JAMA Neurology · doi:10.1001/jamaneurol.2013.596 · Cited by 71 · see citing works
Seth, R. K., Kumar, A., Das, S., Kadiiska, M. B., Michelotti, G. A., Diehl, A. M., & Chatterjee, S. (2013) · Toxicological Sciences · doi:10.1093/toxsci/kft104 · Cited by 67 · see citing works
Self-citationAbdullah, L. I., Evans, J. E., Joshi, U., Crynen, G. C., Reed, J. M., Mouzon, B., Baumann, S., Montague, H., Zakirova, Z., Emmerich, T., et al. (2016) · Toxicology · doi:10.1016/j.tox.2016.10.012 · Cited by 65 · see citing works
Self-citationGulf War illness (GWI) as a neuroimmune disease
Georgopoulos, A. P., James, L. M., Carpenter, A. F., Engdahl, B. E., Leuthold, A. C., & Lewis, S. M. (2017) · Experimental Brain Research · doi:10.1007/s00221-017-5050-0 · Cited by 65 · see citing works
Tang, Y., & Chen, A. (2010) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2010.00956.x · Cited by 60 · see citing works
Morris, G., Berk, M., Carvalho, A. F., Caso, J. R., Sanz, Y., & Maes, M. H. J. (2016) · Current Pharmaceutical Design · doi:10.2174/1381612822666160914182822 · Cited by 56 · see citing works
Nonalcoholic Fatty Liver Disease
Sweet, P. H., Khoo, T., & Nguyen, S. (2017) · Primary Care Clinics in Office Practice · doi:10.1016/j.pop.2017.07.003 · Cited by 56 · see citing works
Fatigue, endocrinopathies, and metabolic disorders
Kaltsas, G., Vgontzas, A., & Chrousos, G. (2010) · PM&R · doi:10.1016/j.pmrj.2010.04.011 · Cited by 54 · see citing works
Zakirova, Z., Crynen, G. C., Hassan, S., Abdullah, L. I., Horne, L., Mathura, V. S., Crawford, F., & Ait‐Ghezala, G. (2016) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2015.00071 · Cited by 53 · see citing works
Kerr, K. J. (2015) · Reviews on Environmental Health · doi:10.1515/reveh-2015-0032 · Cited by 49 · see citing works
Therapeutic Opportunities in Damage-Associated Molecular Pattern-Driven Metabolic Diseases
García‐Martinez, I., Shaker, M. E., & Mehal, W. Z. (2015) · Antioxidants and Redox Signaling · doi:10.1089/ars.2015.6383 · Cited by 44 · see citing works
Kelsall, H. L., McKenzie, D. P., Sim, M. R., Leder, K. S., Forbes, A. B., & Dwyer, T. (2009) · American Journal of Epidemiology · doi:10.1093/aje/kwp238 · Cited by 42 · see citing works
Complications, symptoms, quality of life and pregnancy in cholestatic liver disease
Zakharia, K., Tabibian, A., Lindor, K. D., & Tabibian, J. H. (2018) · Liver International · doi:10.1111/liv.13591 · Cited by 42 · see citing works
Razolli, D. S., Moraes, J. C., Morari, J., de Moura, R. F., Vinolo, M. A. R., & Velloso, L. A. (2014) · Endocrinology · doi:10.1210/en.2014-1552 · Cited by 40 · see citing works
Chandrashekaran, V., Das, S., Seth, R. K., Dattaroy, D., Alhasson, F. A., Michelotti, G. A., Nagarkatti, M., Nagarkatti, P. S., Diehl, A. M., & Chatterjee, S. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2015.10.009 · Cited by 40 · see citing works
Self-citationCoker, W. J. (1996) · Journal of The Royal Naval Medical Service · doi:10.1136/jrnms-82-141 · Cited by 32 · see citing works
Coughlin, S. S. (2011) · The Open Epidemiology Journal · doi:10.2174/1874297101104010140 · Cited by 31 · see citing works
Fatigue in type 1 diabetes: A systematic review of Observational studies
Jensen, Ø., Bernklev, T., & Jelsness‐Jørgensen, L. (2016) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2016.11.002 · Cited by 30 · see citing works
Supporting a Neuroimmune Basis of Gulf War Illness
O'Callaghan, J. P., Michalovicz, L. T., & Kelly, K. A. (2016) · EBioMedicine · doi:10.1016/j.ebiom.2016.10.037 · Cited by 27 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Seth RK, Kumar A, Das S, Kadiiska MB, Michelotti G, Diehl AM,, 2013b Environmental toxin-linked nonalcoholic steatohepatitis and hepatic metabolic reprogramming in obese mice. Toxicol. Sci 134 (2), 291– 303. 10.1093/toxsciAftl04 Epub 2013 May 2. 23640861 PMC3707434 · DOI
Cited by
Sorted by citations
Gut microbiota: An underestimated and unintended recipient for pesticide-induced toxicity
Yuan, X., Pan, Z., Jin, C., Ni, Y., Fu, Z., & Jin, Y. (2019) · Chemosphere · doi:10.1016/j.chemosphere.2019.04.088 · Cited by 187 · see citing works
Alrafas, H. R., Busbee, P. B., Chitrala, K. N., Nagarkatti, M., & Nagarkatti, P. S. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9061796 · Cited by 90 · see citing works
Self-citationGulf War Illness: Mechanisms Underlying Brain Dysfunction and Promising Therapeutic Strategies
Dickey, B. R., Madhu, L. N., & Shetty, A. K. (2020) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2020.107716 · Cited by 74 · see citing works
Michalovicz, L. T., Kelly, K. A., Sullivan, K. A., & O'Callaghan, J. P. (2020) · Neuropharmacology · doi:10.1016/j.neuropharm.2020.108073 · Cited by 59 · see citing works
Self-citationGut microbiome: An intermediary to neurotoxicity
Dempsey, J. L., Little, M., & Cui, J. Y. (2019) · NeuroToxicology · doi:10.1016/j.neuro.2019.08.005 · Cited by 62 · see citing works
Seth, R. K., Maqsood, R., Mondal, A., Bose, D., Kimono, D. A., Holland, L. A., Janulewicz, P. A., Klimas, N. G., Horner, R. D., Sullivan, K. A., et al. (2019) · Viruses · doi:10.3390/v11100968 · Cited by 55 · see citing works
Self-citationCrosstalk between PPARs and gut microbiota in NAFLD
Wu, L., Li, J., Feng, J., Ji, J., Yu, Q., Li, Y., Zheng, Y., Dai, W., Wu, J., & Guo, C. (2021) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2021.111255 · Cited by 52 · see citing works
The Gut-Microbiome in Gulf War Veterans: A Preliminary Report
Janulewicz, P. A., Seth, R. K., Carlson, J. M., Ajama, J., Quinn, E. K., Heeren, T., Klimas, N. G., Lasley, S. M., Horner, R. D., Sullivan, K. A., et al. (2019) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph16193751 · Cited by 51 · see citing works
Self-citationKimono, D. A., Sarkar, S., Albadrani, M. S., Seth, R. K., Bose, D., Mondal, A., Li, Y., Kar, A. N., Nagarkatti, M., Nagarkatti, P. S., et al. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.01229 · Cited by 48 · see citing works
Self-citationMichalovicz, L. T., Locker, A. R., Kelly, K. A., Miller, J. V., Barnes, Z. M., FLETCHER, M. A., Miller, D. B., Klimas, N. G., Morris, M., Lasley, S. M., et al. (2018) · NeuroToxicology · doi:10.1016/j.neuro.2018.10.006 · Cited by 46 · see citing works
Self-citationFotschki, B., Juśkiewicz, J., Jurgoński, A., Amarowicz, R., Opyd, P., Bez, J., Muranyi, I. S., Petersen, I. L., & Laparra, J. M. (2020) · Nutrients · doi:10.3390/nu12092781 · Cited by 45 · see citing works
Janulewicz, P. A., Krengel, M., Quinn, E. K., Heeren, T., Toomey, R., Killiany, R., Zundel, C. G., Ajama, J., O'Callaghan, J. P., Steele, L., et al. (2018) · Brain Sciences · doi:10.3390/brainsci8110198 · Cited by 44 · see citing works
Self-citationPesticides: Unintended Impact on the Hidden World of Gut Microbiota
Ali, A., & AlHussaini, K. I. (2024) · Metabolites · doi:10.3390/metabo14030155 · Cited by 43 · see citing works
Kang, G.-U., Jung, D.-R., Lee, Y. H., Jeon, S. Y., Han, H. S., Chong, G. O., & Shin, J. (2020) · Cancers · doi:10.3390/cancers12123800 · Cited by 41 · see citing works
Hong, D., Zhang, C., Wu, W., Lu, X., & Zhang, L. (2023) · Frontiers in Neurology · doi:10.3389/fneur.2023.1133546 · Cited by 38 · see citing works
Trageser, K. J., Sebastian-Valverde, M., Naughton, S. X., & Pasinetti, G. M. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.00704 · Cited by 36 · see citing works
Kimono, D. A., Bose, D., Seth, R. K., Mondal, A., Saha, P., Janulewicz, P. A., Sullivan, K. A., Lasley, S. M., Horner, R. D., Klimas, N. G., et al. (2020) · Neuroscience Insights · doi:10.1177/2633105520942480 · Cited by 38 · see citing works
Self-citationGuo, J., Wang, Y., Jiang, P., Yao, H., Zhao, C., Hu, X., Cao, Y., Zhang, N., Fu, Y., & Shen, H. (2019) · Microbial Pathogenesis · doi:10.1016/j.micpath.2019.103792 · Cited by 32 · see citing works
Effects of a high fat diet on gut microbiome dysbiosis in a mouse model of Gulf War Illness
Angoa‐Pérez, M., Zagorac, B., Francescutti, D. M., Winters, A. D., Greenberg, J. M., Ahmad, M. M., Manning, S. D., Gulbransen, B. D., Theis, K. R., & Kuhn, D. M. (2020) · Scientific Reports · doi:10.1038/s41598-020-66833-w · Cited by 32 · see citing works
A review of pre-clinical models for Gulf War Illness
Ribeiro, A. C. R., & Deshpande, L. S. (2021) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2021.107936 · Cited by 32 · see citing works
Bose, D., Saha, P., Mondal, A., Fanelli, B. C., Seth, R. K., Janulewicz, P. A., Sullivan, K. A., Lasley, S. M., Horner, R. D., Colwell, R. R., et al. (2020) · Nutrients · doi:10.3390/nu12092764 · Cited by 30 · see citing works
Self-citationZhang, L., Huang, S., & Yuan, Y. (2024) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-024-05807-1 · Cited by 29 · see citing works
Impact of occupational exposure on human microbiota
Lai, P. S., & Christiani, D. C. (2018) · Current Opinion in Allergy and Clinical Immunology · doi:10.1097/aci.0000000000000502 · Cited by 28 · see citing works
Attaluri, S., Upadhya, R., Kodali, M., Madhu, L. N., Upadhya, D., Shuai, B., & Shetty, A. K. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.853000 · Cited by 26 · see citing works
Saha, P., Skidmore, P. T., Holland, L. A., Mondal, A., Bose, D., Seth, R. K., Sullivan, K. A., Janulewicz, P. A., Horner, R. D., Klimas, N. G., et al. (2021) · Brain Sciences · doi:10.3390/brainsci11070905 · Cited by 24 · see citing works
Self-citationChemical exposures and suspected impact on Gulf War Veterans
Elhaj, R., & Reynolds, J. M. (2023) · Military Medical Research · doi:10.1186/s40779-023-00449-9 · Cited by 20 · see citing works
Krengel, M., Sullivan, K. A., Heboyan, V., Zundel, C. G., Wilson, C., Klimas, N. G., & Coughlin, S. S. (2021) · Life Sciences · doi:10.1016/j.lfs.2021.119623 · Cited by 18 · see citing works
Self-citationBose, D., Mondal, A., Saha, P., Kimono, D. A., Sarkar, S., Seth, R. K., Janulewicz, P. A., Sullivan, K. A., Horner, R. D., Klimas, N. G., et al. (2020) · Brain Sciences · doi:10.3390/brainsci10080532 · Cited by 18 · see citing works
Self-citationDysbiosis in gastrointestinal pathophysiology: Role of the gut microbiome in Gulf War Illness
Slevin, E., 小山, 幸., Harrison, K., Wan, Y., Klaunig, J. E., Wu, C., Shetty, A. K., & Meng, F. (2023) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.17631 · Cited by 16 · see citing works
Distinct respiratory microbiota associates with lung cancer clinicopathological characteristics
Zheng, X., Lu, X., & Hu, Y. (2023) · Frontiers in Oncology · doi:10.3389/fonc.2023.847182 · Cited by 17 · see citing works
The Health of Gulf War and Gulf Era Veterans Over Time
Dursa, E. K., Cao, G., Porter, B., Culpepper, W. J., & Schneiderman, A. (2021) · Journal of Occupational and Environmental Medicine · doi:10.1097/jom.0000000000002331 · Cited by 17 · see citing works
Niacin for Parkinson's disease
Seamon, M., Purohit, S. B., Giri, B., Baban, B., Morgan, J. C., Chong, R. K. Y., & Wakade, C. G. (2019) · Clinical and Experimental Neuroimmunology · doi:10.1111/cen3.12553 · Cited by 16 · see citing works
Zhu, Z., Zuo, S., Zhu, Z., Wang, C., Du, Y., & Chen, F. (2025) · International Immunopharmacology · doi:10.1016/j.intimp.2025.114091 · Cited by 15 · see citing works
Michalovicz, L. T., Kelly, K. A., Miller, D. B., Sullivan, K. A., & O'Callaghan, J. P. (2021) · Life Sciences · doi:10.1016/j.lfs.2021.119962 · Cited by 15 · see citing works
Self-citationKeating, J. A., Shaughnessy, C., Baubie, K., Kates, A., Putman-Buehler, N., Watson, L., Dominguez, N., Watson, K. E., Cook, D. B., Rabago, D., et al. (2019) · BMJ Open · doi:10.1136/bmjopen-2019-031114 · Cited by 14 · see citing works
Host gut resistome in Gulf War chronic multisymptom illness correlates with persistent inflammation
Bose, D., Chatterjee, S., Older, E. A., Seth, R. K., Janulewicz, P. A., Saha, P., Mondal, A., Carlson, J. M., Decho, A. W., Sullivan, K. A., et al. (2022) · Communications Biology · doi:10.1038/s42003-022-03494-7 · Cited by 14 · see citing works
Self-citationKozlova, E. V., Carabelli, B., Bishay, A. E., Liu, R., Denys, M. E., Macbeth, J. C., Piamthai, V., Crawford, M. S., McCole, D. F., Nieden, N. I. Z., et al. (2021) · Life Sciences · doi:10.1016/j.lfs.2021.120153 · Cited by 14 · see citing works
Keating, D., Zundel, C. G., Abreu, M., Krengel, M., Aenlle, K. K., Nichols, M. D., Toomey, R., Chao, L. L., Golier, J. A., Abdullah, L. I., et al. (2021) · Life Sciences · doi:10.1016/j.lfs.2021.119903 · Cited by 12 · see citing works
Self-citationKimono, D. A. (2021) · Military Medical Research · doi:10.1186/s40779-021-00341-4 · Cited by 12 · see citing works
Self-citationMote, R. S., Carpenter, J. M., Dockman, R. L., Steinberger, A. J., Suen, G., Norberg, T., Harn, D. A., Wagner, J. J., & Filipov, N. M. (2020) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph17197081 · Cited by 11 · see citing works
Angoa‐Pérez, M., Zagorac, B., Francescutti, D. M., Theis, K. R., & Kuhn, D. M. (2021) · Life Sciences · doi:10.1016/j.lfs.2021.119675 · Cited by 11 · see citing works
Hodgin, K. S., Jones, C. L., & Younger, J. (2022) · Journal of Occupational and Environmental Medicine · doi:10.1097/jom.0000000000002625 · Cited by 11 · see citing works
François, S., Mondot, S., Gerard, Q., Bel, R., Knoertzer, J., Berriche, A., Cavallero, S., Baati, R., Orset, C., Bo, G. D., et al. (2022) · Biomedicines · doi:10.3390/biomedicines10051167 · Cited by 10 · see citing works
Host gut microbiome and potential therapeutics in Gulf War Illness: A short review
Chatterjee, S., Bose, D., & Seth, R. K. (2021) · Life Sciences · doi:10.1016/j.lfs.2021.119717 · Cited by 9 · see citing works
Self-citationKates, A., Keating, J. A., Baubie, K., Putman-Buehler, N., Watson, L., Godfrey, J. J., Deblois, C. L., Suen, G., Cook, D. B., Rabago, D., et al. (2022) · PLoS ONE · doi:10.1371/journal.pone.0268479 · Cited by 10 · see citing works
Experimental Models of Gulf War Illness, a Chronic Neuropsychiatric Disorder in Veterans
Reddy, D. S., Wu, X. Y., Singh, T., & Neff, M. (2023) · Current Protocols · doi:10.1002/cpz1.707 · Cited by 7 · see citing works
Crisis in the gut: navigating gastrointestinal challenges in Gulf War Illness with bioengineering
Collier, C. A., Salikhova, A., Sabir, S., Foncerrada, S., & Raghavan, S. A. (2024) · Military Medical Research · doi:10.1186/s40779-024-00547-2 · Cited by 8 · see citing works
The Role of the Microbiome in Allergy, Asthma, and Occupational Lung Disease
Peer, A., & Samuelson, D. R. (2024) · Current Allergy and Asthma Reports · doi:10.1007/s11882-024-01156-8 · Cited by 5 · see citing works
Role of microbiota in pain: From bench to bedside
Ren, H., Cao, B., Xu, Q., Zhao, R., Li, H., & Wei, B. (2025) · iMetaOmics. · doi:10.1002/imo2.58 · Cited by 6 · see citing works
Environmental Pollutants That Can Be Metabolized by the Host (Gut Microbiota)
El-Dalatony, M. M., & Li, X. (2020) · Springer eBooks · doi:10.1007/978-981-15-4759-1_5 · Cited by 4 · see citing works
Trivedi, A., Bose, D., Moffat, K. S., Pearson, E., Walsh, D. M., Cohen, D. E., Skupsky, J., Chao, L. L., Golier, J. A., Janulewicz, P. A., et al. (2024) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph21081102 · Cited by 3 · see citing works
Self-citationWu, Y. H., Liu, J. L., Ren, Y., & Zou, C. (2026) · Experimental Dermatology · doi:10.1111/exd.70261 · Cited by 2 · see citing works
Contributions of the gut microbiota to Gulf War Illness susceptibility: Findings from a mouse model
Chaudhari, D. S., Francescutti, D. M., Winters, A. D., Koka, O., Kracht, D. J., Greenberg, J. M., Theis, K. R., & Angoa‐Pérez, M. (2024) · Life Sciences · doi:10.1016/j.lfs.2024.123244 · Cited by 2 · see citing works
Donatini, B. (2021) · JOURNAL OF CASE REPORTS AND STUDIES · doi:10.15744/2348-9820.9.205
Gut-Brain Axis and Colorectal Cancer: Neuroimmune Interactions
Prasad, A., Acharya, S., Singh, A., Raj, U., & Sharma, A. (2025) · Cancer drug discovery and develogment/Cancer drug discovery and development · doi:10.1007/978-3-031-86065-2_12
- Authors
- Seth, R. K., Kimono, D., Alhasson, F., Sarkar, S., Albadrani, M., Lasley, S. K., Horner, R., Janulewicz, P., Nagarkatti, M., Nagarkatti, P., Sullivan, K., & Chatterjee, S.
- Affiliations
- University of South Carolina (US)
- Boston University (US)
- Corresponding author
- Chatterjee, Saurabh
- ORCID
- Venue
- Toxicology and Applied Pharmacology
- Publisher
- Elsevier BV
- Published
- 2018-07
- Volume
- 350
- Pages
- 64-77
- ISSN
- 0041-008X (ISSN-L)
- PMC
- PMC6121708
- OpenAlex
- W2800481810
- Cited by
- 55
- References
- 68
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 6 · 2023: 5 · 2022: 5 · 2021: 12 · 2020: 12 · 2019: 8 · 2018: 3
- FWCI
- 3.11
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Toxicology and Applied Pharmacology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Gulf War Illness Research (W81XWH-13-2-0072)
- University of South Carolina School of Medicine
- University of Georgia college of veterinary medicine
- University of South Carolina
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Life Sciences › Immunology and Microbiology › Immunology › Immunotoxicology and immune responses
- Keywords
- Gulf War illness, butyrate, short-chain fatty acids, gastrointestinal inflammation, gut microbiota, permethrin, pyridostigmine bromide, GPR109A, TLR4, TLR5, claudin-2, leaky gut, SREBP-1c, PPARα, lipogenesis, glucose transporter 4, hepatocytes, chronic fatigue, veterans
- MeSH terms
- Cellular Reprogramming Techniques, Gastrointestinal Microbiome, Animals, Butyrates, Cells, Cultured, Disease Models, Animal, Gastritis, Humans, Insecticides, Male, Mice, Inbred C57BL, Mice, Transgenic, Mice, Knockout, Persian Gulf Syndrome, Hepatocytes, Permethrin, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review