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Frontiers in microbiology2019; 10; 723; doi: 10.3389/fmicb.2019.00723

Beyond Gut Instinct: Metabolic Short-Chain Fatty Acids Moderate the Pathogenesis of Alphaherpesviruses.

Abstract: Short-chain fatty acids (SCFA), such as sodium butyrate (SB), sodium propionate (SPr), and sodium acetate (SAc), are metabolic end-products of the fermentation of dietary fibers. They are linked with multiple beneficial effects on the general mammalian health, based on the sophisticated interplay with the host immune response. Equine herpesvirus 1 (EHV1) is a major pathogen, which primarily replicates in the respiratory epithelium, and disseminates through the body via a cell-associated viremia in leukocytes, even in the presence of neutralizing antibodies. Infected monocytic CD172a cells and T-lymphocytes transmit EHV1 to the endothelium of the endometrium or central nervous system (CNS), causing reproductive or neurological disorders. Here, we questioned whether SCFA have a potential role in shaping the pathogenesis of EHV1 during the primary replication in the URT, during the cell-associated viremia, or at the level of the endothelium of the pregnant uterus and/or CNS. First, we demonstrated the expression of SCFA receptors, FFA2 and FFA3, within the epithelium of the equine respiratory tract, at the cell surface of immune cells, and equine endothelium. Subsequently, EHV1 replication was evaluated in the URT, in the presence or absence of SB, SPr, or SAc. In general, we demonstrated that SCFA do not affect the number of viral plaques or virus titer upon primary viral replication. Only SB and SPr were able to reduce the plaque latitudes. Similarly, pretreatment of monocytic CD172a cells and T-lymphocytes with different concentrations of SCFA did not alter the number of infected cells. When endothelial cells were treated with SB, SPr, or SAc, prior to the co-cultivation with EHV1-inoculated mononuclear cells, we observed a reduced number of adherent immune cells to the target endothelium. This was associated with a downregulation of endothelial adhesion molecules ICAM-1 and VCAM-1 in the presence of SCFA, which ultimately lead to a significant reduction of the EHV1 endothelial plaques. These results indicate that physiological concentrations of SCFA may affect the pathogenesis of EHV1, mainly at the target endothelium, in favor of the fitness of the horse. Our findings may have significant implications to develop innovative therapies, to prevent the devastating clinical outcome of EHV1 infections.
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Publication Date: 2019-04-05 PubMed ID: 31024501PubMed Central: PMC6460668DOI: 10.3389/fmicb.2019.00723Google 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 the role of short-chain fatty acids (SCFAs) in influencing the pathogenesis of Equine Herpesvirus 1 (EHV1), a major disease agent in horses. The study demonstrates that SCFAs do not affect primary viral replication, but they can reduce the adhesion of immune cells to the endothelium, thereby reducing the spread of the virus.

Experiment Setup and Findings

  • The study primarily dealt with three types of SCFAs – sodium butyrate (SB), sodium propionate (SPr), and sodium acetate (SAc). These acids are produced by the fermentation of dietary fibers and have a significant impact on general mammalian health primarily due to their interaction with the immune response.
  • The research concentrated on the role of these SCFAs on EHV1, a virus that initially replicates in the respiratory epithelium of horses and spreads through the body by associating with leukocytes. The virus can cause reproductive or neurological disorders in horses when transmitted to the endometrium or central nervous system (CNS) by infected monocytic CD172a cells and T-lymphocytes.
  • The study confirmed the presence of SCFA receptors, FFA2 and FFA3, within the epithelial cells of the equine respiratory tract, immune cells, and equine endothelium. The replication of EHV1 in these cells was then evaluated with or without the presence of the SCFAs. The results showed that the SCFAs did not affect the viral plaques or virus titer during primary viral replication, though SB and SPr were observed to reduce plaque sizes.
  • When monocytic CD172a cells and T-lymphocytes were pretreated with SCFAs, the number of infected cells remained unaltered. However, when endothelial cells were treated with the SCFAs prior to exposure to EHV1-inoculated mononuclear cells, a reduction in the number of immune cells adhering to the target endothelium was observed. This was linked to a reduction in endothelial adhesion molecules ICAM-1 and VCAM-1 in the presence of SCFAs, resulting in a significant reduction of EHV1 endothelial plaques.

Implications and Conclusions

  • These findings suggest that SCFAs, at physiological concentrations, could play a role in altering the pathogenesis of EHV1, mainly at the level of the target endothelium. This would benefit the horse’s health by impeding the spread of the virus within the body
  • The research has implications for potential therapeutic development. Utilizing SCFAs could pave the way for innovative therapies to prevent the severe outcomes of EHV1 infections in horses.

Cite This Article

APA
Poelaert KCK, Van Cleemput J, Laval K, Descamps S, Favoreel HW, Nauwynck HJ. (2019). Beyond Gut Instinct: Metabolic Short-Chain Fatty Acids Moderate the Pathogenesis of Alphaherpesviruses. Front Microbiol, 10, 723. https://doi.org/10.3389/fmicb.2019.00723

Publication

Frontiers in microbiology
ISSN: 1664-302X
NlmUniqueID: 101548977
Country: Switzerland
Language: English
Volume: 10
Pages: 723
PII: 723

Researcher Affiliations

Poelaert, Katrien C K
  • Laboratory of Virology, Department of Virology, Immunology and Parasitology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium.
Van Cleemput, Jolien
  • Laboratory of Virology, Department of Virology, Immunology and Parasitology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium.
  • 301 Schultz Laboratory, Department of Molecular Biology, Princeton University, Princeton, NJ, United States.
Laval, Kathlyn
  • 301 Schultz Laboratory, Department of Molecular Biology, Princeton University, Princeton, NJ, United States.
Descamps, Sarah
  • Laboratory of Virology, Department of Virology, Immunology and Parasitology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium.
Favoreel, Herman W
  • Laboratory of Virology, Department of Virology, Immunology and Parasitology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium.
Nauwynck, Hans J
  • Laboratory of Virology, Department of Virology, Immunology and Parasitology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium.

References

This article includes 71 references
  1. Abrahamsson TR, Jakobsson HE, Andersson AF, Björkstén B, Engstrand L, Jenmalm MC. Low gut microbiota diversity in early infancy precedes asthma at school age.. Clin Exp Allergy 2014 Jun;44(6):842-50.
    doi: 10.1111/cea.12253pubmed: 24330256google scholar: lookup
  2. Anderson JW, Baird P, Davis RH Jr, Ferreri S, Knudtson M, Koraym A, Waters V, Williams CL. Health benefits of dietary fiber.. Nutr Rev 2009 Apr;67(4):188-205.
    doi: 10.1111/j.1753-4887.2009.00189.xpubmed: 19335713google scholar: lookup
  3. Ang Z, Ding JL. GPR41 and GPR43 in Obesity and Inflammation - Protective or Causative?. Front Immunol 2016;7:28.
    doi: 10.3389/fimmu.2016.00028pmc: PMC4734206pubmed: 26870043google scholar: lookup
  4. Argenzio RA. Functions of the equine large intestine and their interrelationship in disease.. Cornell Vet 1975 Jul;65(3):303-30.
    pubmed: 237739
  5. Biddle AS, Black SJ, Blanchard JL. An in vitro model of the horse gut microbiome enables identification of lactate-utilizing bacteria that differentially respond to starch induction.. PLoS One 2013;8(10):e77599.
    doi: 10.1371/journal.pone.0077599pmc: PMC3788102pubmed: 24098591google scholar: lookup
  6. Bisgaard H, Li N, Bonnelykke K, Chawes BL, Skov T, Paludan-Müller G, Stokholm J, Smith B, Krogfelt KA. Reduced diversity of the intestinal microbiota during infancy is associated with increased risk of allergic disease at school age.. J Allergy Clin Immunol 2011 Sep;128(3):646-52.e1-5.
    doi: 10.1016/j.jaci.2011.04.060pubmed: 21782228google scholar: lookup
  7. Bruzzese E, Callegari ML, Raia V, Viscovo S, Scotto R, Ferrari S, Morelli L, Buccigrossi V, Lo Vecchio A, Ruberto E, Guarino A. Disrupted intestinal microbiota and intestinal inflammation in children with cystic fibrosis and its restoration with Lactobacillus GG: a randomised clinical trial.. PLoS One 2014;9(2):e87796.
    doi: 10.1371/journal.pone.0087796pmc: PMC3929570pubmed: 24586292google scholar: lookup
  8. Burkhardt JK, Echeverri CJ, Nilsson T, Vallee RB. Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution.. J Cell Biol 1997 Oct 20;139(2):469-84.
    doi: 10.1083/jcb.139.2.469pmc: PMC2139801pubmed: 9334349google scholar: lookup
  9. Chow J, Lee SM, Shen Y, Khosravi A, Mazmanian SK. Host-bacterial symbiosis in health and disease.. Adv Immunol 2010;107:243-74.
    doi: 10.1016/B978-0-12-381300-8.00008-3pmc: PMC3152488pubmed: 21034976google scholar: lookup
  10. Comalada M, Bailón E, de Haro O, Lara-Villoslada F, Xaus J, Zarzuelo A, Gálvez J. The effects of short-chain fatty acids on colon epithelial proliferation and survival depend on the cellular phenotype.. J Cancer Res Clin Oncol 2006 Aug;132(8):487-97.
    doi: 10.1007/s00432-006-0092-xpubmed: 16788843google scholar: lookup
  11. Cummings JH, Pomare EW, Branch WJ, Naylor CP, Macfarlane GT. Short chain fatty acids in human large intestine, portal, hepatic and venous blood.. Gut 1987 Oct;28(10):1221-7.
    doi: 10.1136/gut.28.10.1221pmc: PMC1433442pubmed: 3678950google scholar: lookup
  12. Daly K, Stewart CS, Flint HJ, Shirazi-Beechey SP. Bacterial diversity within the equine large intestine as revealed by molecular analysis of cloned 16S rRNA genes. FEMS Microbiol. Ecol. 38 141–151.
    doi: 10.1111/j.1574-6941.2001.tb00892.xgoogle scholar: lookup
  13. Dauphinee SM, Karsan A. Lipopolysaccharide signaling in endothelial cells.. Lab Invest 2006 Jan;86(1):9-22.
    doi: 10.1038/labinvest.3700366pubmed: 16357866google scholar: lookup
  14. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, Collini S, Pieraccini G, Lionetti P. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa.. Proc Natl Acad Sci U S A 2010 Aug 17;107(33):14691-6.
    doi: 10.1073/pnas.1005963107pmc: PMC2930426pubmed: 20679230google scholar: lookup
  15. Dedoni S, Olianas MC, Onali P. Synergistic interaction of histone deacetylase inhibitors with interferon-β in inducing apoptosis of human neuroblastoma cells. FASEB J. 30 715 12.
  16. den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud DJ, Bakker BM. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism.. J Lipid Res 2013 Sep;54(9):2325-40.
    doi: 10.1194/jlr.R036012pmc: PMC3735932pubmed: 23821742google scholar: lookup
  17. Dicks LMT, Botha M, Dicks E, Botes M. The equine gastro-intestinal tract: an overview of the microbiota, disease and treatment. Livest. Sci. 160 69–81.
    doi: 10.1016/j.livsci.2013.11.025google scholar: lookup
  18. Didonna A, Opal P. The promise and perils of HDAC inhibitors in neurodegeneration.. Ann Clin Transl Neurol 2015 Jan;2(1):79-101.
    doi: 10.1002/acn3.147pmc: PMC4301678pubmed: 25642438google scholar: lookup
  19. Dougal K, de la Fuente G, Harris PA, Girdwood SE, Pinloche E, Geor RJ, Nielsen BD, Schott HC 2nd, Elzinga S, Newbold CJ. Characterisation of the faecal bacterial community in adult and elderly horses fed a high fibre, high oil or high starch diet using 454 pyrosequencing.. PLoS One 2014;9(2):e87424.
    doi: 10.1371/journal.pone.0087424pmc: PMC3913607pubmed: 24504261google scholar: lookup
  20. Edington N, Bridges CG, Patel JR. Endothelial cell infection and thrombosis in paralysis caused by equid herpesvirus-1: equine stroke.. Arch Virol 1986;90(1-2):111-24.
    doi: 10.1007/BF01314149pubmed: 3015074google scholar: lookup
  21. Edington N, Smyth B, Griffiths L. The role of endothelial cell infection in the endometrium, placenta and foetus of equid herpesvirus 1 (EHV-1) abortions.. J Comp Pathol 1991 May;104(4):379-87.
    doi: 10.1016/S0021-9975(08)80148-Xpubmed: 1651960google scholar: lookup
  22. Esposito K, Giugliano D. Whole-grain intake cools down inflammation.. Am J Clin Nutr 2006 Jun;83(6):1440-1; author reply 1441-2.
    doi: 10.1093/ajcn/83.6.1440pubmed: 16762958google scholar: lookup
  23. Faure E, Equils O, Sieling PA, Thomas L, Zhang FX, Kirschning CJ, Polentarutti N, Muzio M, Arditi M. Bacterial lipopolysaccharide activates NF-kappaB through toll-like receptor 4 (TLR-4) in cultured human dermal endothelial cells. Differential expression of TLR-4 and TLR-2 in endothelial cells.. J Biol Chem 2000 Apr 14;275(15):11058-63.
    doi: 10.1074/jbc.275.15.11058pubmed: 10753909google scholar: lookup
  24. Franklin ST, Young JW, Nonnecke BJ. Effects of ketones, acetate, butyrate, and glucose on bovine lymphocyte proliferation.. J Dairy Sci 1991 Aug;74(8):2507-14.
    doi: 10.3168/jds.S0022-0302(91)78428-2pubmed: 1918530google scholar: lookup
  25. Friedman HM, Macarak EJ, MacGregor RR, Wolfe J, Kefalides NA. Virus infection of endothelial cells.. J Infect Dis 1981 Feb;143(2):266-73.
    doi: 10.1093/infdis/143.2.266pubmed: 6260874google scholar: lookup
  26. Goehring LS, van Winden SC, van Maanen C, Sloet van Oldruitenborgh-Oosterbaan MM. Equine herpesvirus type 1-associated myeloencephalopathy in The Netherlands: a four-year retrospective study (1999-2003).. J Vet Intern Med 2006 May-Jun;20(3):601-7.
    pubmed: 16734096doi: 10.1892/0891-6640(2006)20[601:ehtami]2.0.co;2google scholar: lookup
  27. Goodrum F, Bughio F. Viral infection at the endothelium.. Oncotarget 2015 Sep 29;6(29):26541-2.
    doi: 10.18632/oncotarget.5246pmc: PMC4694926pubmed: 26309089google scholar: lookup
  28. Gosselin J, Flamand L, D'Addario M, Hiscott J, Menezes J. Infection of peripheral blood mononuclear cells by herpes simplex and Epstein-Barr viruses. Differential induction of interleukin 6 and tumor necrosis factor-alpha.. J Clin Invest 1992 Jun;89(6):1849-56.
    doi: 10.1172/JCI115789pmc: PMC295883pubmed: 1318324google scholar: lookup
  29. Gray SG, Ekström TJ. The human histone deacetylase family.. Exp Cell Res 2001 Jan 15;262(2):75-83.
    doi: 10.1006/excr.2000.5080pubmed: 11139331google scholar: lookup
  30. Gryspeerdt AC, Vandekerckhove AP, Garré B, Barbé F, Van de Walle GR, Nauwynck HJ. Differences in replication kinetics and cell tropism between neurovirulent and non-neurovirulent EHV1 strains during the acute phase of infection in horses.. Vet Microbiol 2010 May 19;142(3-4):242-53.
    doi: 10.1016/j.vetmic.2009.10.015pubmed: 19926232google scholar: lookup
  31. Hijiya N, Miyake K, Akashi S, Matsuura K, Higuchi Y, Yamamoto S. Possible involvement of toll-like receptor 4 in endothelial cell activation of larger vessels in response to lipopolysaccharide.. Pathobiology 2002;70(1):18-25.
    doi: 10.1159/000066000pubmed: 12415188google scholar: lookup
  32. Imoto Y, Kato A, Takabayashi T, Sakashita M, Norton JE, Suh LA, Carter RG, Weibman AR, Hulse KE, Stevens W, Harris KE, Peters AT, Grammer LC, Tan BK, Welch K, Conley DB, Kern RC, Fujieda S, Schleimer RP. Short-chain fatty acids induce tissue plasminogen activator in airway epithelial cells via GPR41&43.. Clin Exp Allergy 2018 May;48(5):544-554.
    doi: 10.1111/cea.13119pmc: PMC5987538pubmed: 29431874google scholar: lookup
  33. Jang HK, Albrecht RA, Buczynski KA, Kim SK, Derbigny WA, O'Callaghan DJ. Mapping the sequences that mediate interaction of the equine herpesvirus 1 immediate-early protein and human TFIIB.. J Virol 2001 Nov;75(21):10219-30.
    doi: 10.1128/JVI.75.21.10219-10230.2001pmc: PMC114596pubmed: 11581390google scholar: lookup
  34. Janis C. THE EVOLUTIONARY STRATEGY OF THE EQUIDAE AND THE ORIGINS OF RUMEN AND CECAL DIGESTION.. Evolution 1976 Dec;30(4):757-774.
    doi: 10.1111/j.1558-5646.1976.tb00957.xpubmed: 28563331google scholar: lookup
  35. Julliand V. Impact of nutrition on the gastro-intestinal tract in horses. .
  36. Karlin S, Mocarski ES, Schachtel GA. Molecular evolution of herpesviruses: genomic and protein sequence comparisons.. J Virol 1994 Mar;68(3):1886-902.
    pmc: PMC236651pubmed: 8107249doi: 10.1128/jvi.68.3.1886-1902.1994google scholar: lookup
  37. Kolb H, Mandrup-Poulsen T. The global diabetes epidemic as a consequence of lifestyle-induced low-grade inflammation.. Diabetologia 2010 Jan;53(1):10-20.
    doi: 10.1007/s00125-009-1573-7pubmed: 19890624google scholar: lookup
  38. La Bonnardiere C, Laude H. High interferon titer in newborn pig intestine during experimentally induced viral enteritis.. Infect Immun 1981 Apr;32(1):28-31.
    pmc: PMC350581pubmed: 6163724doi: 10.1128/iai.32.1.28-31.1981google scholar: lookup
  39. Laval K, Favoreel HW, Nauwynck HJ. Equine herpesvirus type 1 replication is delayed in CD172a+ monocytic cells and controlled by histone deacetylases.. J Gen Virol 2015 Jan;96(Pt 1):118-130.
    doi: 10.1099/vir.0.067363-0pubmed: 25239765google scholar: lookup
  40. Laval K, Favoreel HW, Poelaert KC, Van Cleemput J, Nauwynck HJ. Equine Herpesvirus Type 1 Enhances Viral Replication in CD172a+ Monocytic Cells upon Adhesion to Endothelial Cells.. J Virol 2015 Nov;89(21):10912-23.
    doi: 10.1128/JVI.01589-15pmc: PMC4621108pubmed: 26292328google scholar: lookup
  41. Laval K, Van Cleemput J, Poelaert KC, Brown IK, Nauwynck HJ. Replication of neurovirulent equine herpesvirus type 1 (EHV-1) in CD172a(+) monocytic cells.. Comp Immunol Microbiol Infect Dis 2017 Feb;50:58-62.
    doi: 10.1016/j.cimid.2016.11.006pubmed: 28131380google scholar: lookup
  42. Leys C, Ley C, Klein O, Bernard P, Licata L. Detecting outliers: do not use standard deviation around the mean, use absolute deviation around the median. J. Exp. Soc. Psychol. 49 764–766.
    doi: 10.1016/j.jesp.2013.03.013google scholar: lookup
  43. Li M, van Esch BCAM, Wagenaar GTM, Garssen J, Folkerts G, Henricks PAJ. Pro- and anti-inflammatory effects of short chain fatty acids on immune and endothelial cells.. Eur J Pharmacol 2018 Jul 15;831:52-59.
    doi: 10.1016/j.ejphar.2018.05.003pubmed: 29750914google scholar: lookup
  44. Lunn DP, Davis-Poynter N, Flaminio MJ, Horohov DW, Osterrieder K, Pusterla N, Townsend HG. Equine herpesvirus-1 consensus statement.. J Vet Intern Med 2009 May-Jun;23(3):450-61.
    doi: 10.1111/j.1939-1676.2009.0304.xpubmed: 19645832google scholar: lookup
  45. Marsland BJ, Trompette A, Gollwitzer ES. The Gut-Lung Axis in Respiratory Disease.. Ann Am Thorac Soc 2015 Nov;12 Suppl 2:S150-6.
    doi: 10.1513/AnnalsATS.201503-133AWpubmed: 26595731google scholar: lookup
  46. Menzel T, Lührs H, Zirlik S, Schauber J, Kudlich T, Gerke T, Gostner A, Neumann M, Melcher R, Scheppach W. Butyrate inhibits leukocyte adhesion to endothelial cells via modulation of VCAM-1.. Inflamm Bowel Dis 2004 Mar;10(2):122-8.
    doi: 10.1097/00054725-200403000-00010pubmed: 15168812google scholar: lookup
  47. Morrison DJ, Preston T. Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism.. Gut Microbes 2016 May 3;7(3):189-200.
    doi: 10.1080/19490976.2015.1134082pmc: PMC4939913pubmed: 26963409google scholar: lookup
  48. Muylle S, Simoens P, Lauwers H. Ageing horses by an examination of their incisor teeth: an (im)possible task?. Vet Rec 1996 Mar 30;138(13):295-301.
    doi: 10.1136/vr.138.13.295pubmed: 8730689google scholar: lookup
  49. Nugent J, Birch-Machin I, Smith KC, Mumford JA, Swann Z, Newton JR, Bowden RJ, Allen GP, Davis-Poynter N. Analysis of equid herpesvirus 1 strain variation reveals a point mutation of the DNA polymerase strongly associated with neuropathogenic versus nonneuropathogenic disease outbreaks.. J Virol 2006 Apr;80(8):4047-60.
    doi: 10.1128/JVI.80.8.4047-4060.2006pmc: PMC1440451pubmed: 16571821google scholar: lookup
  50. Nusinzon I, Horvath CM. Interferon-stimulated transcription and innate antiviral immunity require deacetylase activity and histone deacetylase 1.. Proc Natl Acad Sci U S A 2003 Dec 9;100(25):14742-7.
    doi: 10.1073/pnas.2433987100pmc: PMC299790pubmed: 14645718google scholar: lookup
  51. Park J, Kim M, Kang SG, Jannasch AH, Cooper B, Patterson J, Kim CH. Short-chain fatty acids induce both effector and regulatory T cells by suppression of histone deacetylases and regulation of the mTOR-S6K pathway.. Mucosal Immunol 2015 Jan;8(1):80-93.
    doi: 10.1038/mi.2014.44pmc: PMC4263689pubmed: 24917457google scholar: lookup
  52. Pluznick J. A novel SCFA receptor, the microbiota, and blood pressure regulation.. Gut Microbes 2014 Mar-Apr;5(2):202-7.
    doi: 10.4161/gmic.27492pmc: PMC4063845pubmed: 24429443google scholar: lookup
  53. Poelaert KCK, Van Cleemput J, Laval K, Favoreel HW, Couck L, Van den Broeck W, Azab W, Nauwynck HJ. Equine Herpesvirus 1 Bridles T Lymphocytes To Reach Its Target Organs.. J Virol 2019 Apr 1;93(7).
    doi: 10.1128/JVI.02098-18pmc: PMC6430527pubmed: 30651370google scholar: lookup
  54. Poelaert KCK, Van Cleemput J, Laval K, Favoreel HW, Soboll Hussey G, Maes RK, Nauwynck HJ. Abortigenic but Not Neurotropic Equine Herpes Virus 1 Modulates the Interferon Antiviral Defense.. Front Cell Infect Microbiol 2018;8:312.
    doi: 10.3389/fcimb.2018.00312pmc: PMC6144955pubmed: 30258819google scholar: lookup
  55. Reed LJ, Muench H. A simple method of estimating fifty percent endpoints. Am. J. Epidemiol. 27 493–497.
    doi: 10.1093/oxfordjournals.aje.a118408google scholar: lookup
  56. Reichert N, Choukrallah MA, Matthias P. Multiple roles of class I HDACs in proliferation, differentiation, and development.. Cell Mol Life Sci 2012 Jul;69(13):2173-87.
    doi: 10.1007/s00018-012-0921-9pubmed: 22286122google scholar: lookup
  57. Schilderink R, Verseijden C, de Jonge WJ. Dietary inhibitors of histone deacetylases in intestinal immunity and homeostasis.. Front Immunol 2013;4:226.
    doi: 10.3389/fimmu.2013.00226pmc: PMC3730085pubmed: 23914191google scholar: lookup
  58. Smith JS, Rajagopal S. The β-Arrestins: Multifunctional Regulators of G Protein-coupled Receptors.. J Biol Chem 2016 Apr 22;291(17):8969-77.
    doi: 10.1074/jbc.R115.713313pmc: PMC4861465pubmed: 26984408google scholar: lookup
  59. Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly-Y M, Glickman JN, Garrett WS. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis.. Science 2013 Aug 2;341(6145):569-73.
    doi: 10.1126/science.1241165pmc: PMC3807819pubmed: 23828891google scholar: lookup
  60. Smith RH, Zhao Y, O'Callaghan DJ. The equine herpesvirus type 1 immediate-early gene product contains an acidic transcriptional activation domain.. Virology 1994 Aug 1;202(2):760-70.
    doi: 10.1006/viro.1994.1398pubmed: 8030239google scholar: lookup
  61. Springer TA. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm.. Cell 1994 Jan 28;76(2):301-14.
    doi: 10.1016/0092-8674(94)90337-9pubmed: 7507411google scholar: lookup
  62. Trompette A, Gollwitzer ES, Yadava K, Sichelstiel AK, Sprenger N, Ngom-Bru C, Blanchard C, Junt T, Nicod LP, Harris NL, Marsland BJ. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis.. Nat Med 2014 Feb;20(2):159-66.
    doi: 10.1038/nm.3444pubmed: 24390308google scholar: lookup
  63. Van de Walle GR, Favoreel HW, Nauwynck HJ, Pensaert MB. Antibody-induced internalization of viral glycoproteins and gE-gI Fc receptor activity protect pseudorabies virus-infected monocytes from efficient complement-mediated lysis.. J Gen Virol 2003 Apr;84(Pt 4):939-947.
    doi: 10.1099/vir.0.18663-0pubmed: 12655095google scholar: lookup
  64. Van de Walle GR, Goupil R, Wishon C, Damiani A, Perkins GA, Osterrieder N. A single-nucleotide polymorphism in a herpesvirus DNA polymerase is sufficient to cause lethal neurological disease.. J Infect Dis 2009 Jul 1;200(1):20-5.
    doi: 10.1086/599316pubmed: 19456260google scholar: lookup
  65. van der Meulen K, Vercauteren G, Nauwynck H, Pensaert M. A local epidemic of equine herpesvirus 1-induced neurological disorders in Belgium. Vlaams Diergeneeskundig Tijdschrift 72 366–372.
  66. van Der Meulen KM, Nauwynck HJ, Bí¶®rt W, Pensaert MB. Replication of equine herpesvirus type 1 in freshly isolated equine peripheral blood mononuclear cells and changes in susceptibility following mitogen stimulation.. J Gen Virol 2000 Jan;81(Pt 1):21-5.
    doi: 10.1099/0022-1317-81-1-21pubmed: 10640538google scholar: lookup
  67. Vandekerckhove AP, Glorieux S, Gryspeerdt AC, Steukers L, Duchateau L, Osterrieder N, Van de Walle GR, Nauwynck HJ. Replication kinetics of neurovirulent versus non-neurovirulent equine herpesvirus type 1 strains in equine nasal mucosal explants.. J Gen Virol 2010 Aug;91(Pt 8):2019-2028.
    doi: 10.1099/vir.0.019257-0pubmed: 20427565google scholar: lookup
  68. Wajner M, Santos KD, Schlottfeldt JL, Rocha MP, Wannmacher CM. Inhibition of mitogen-activated proliferation of human peripheral lymphocytes in vitro by propionic acid.. Clin Sci (Lond) 1999 Jan;96(1):99-103.
    doi: 10.1042/cs0960099pubmed: 9857112google scholar: lookup
  69. Zapolska-Downar D, Siennicka A, Kaczmarczyk M, Kołodziej B, Naruszewicz M. Butyrate inhibits cytokine-induced VCAM-1 and ICAM-1 expression in cultured endothelial cells: the role of NF-kappaB and PPARalpha.. J Nutr Biochem 2004 Apr;15(4):220-8.
    doi: 10.1016/j.jnutbio.2003.11.008pubmed: 15068815google scholar: lookup
  70. Zeuke S, Ulmer AJ, Kusumoto S, Katus HA, Heine H. TLR4-mediated inflammatory activation of human coronary artery endothelial cells by LPS.. Cardiovasc Res 2002 Oct;56(1):126-34.
    doi: 10.1016/S0008-6363(02)00512-6pubmed: 12237173google scholar: lookup
  71. Zhou B, Margariti A, Zeng L, Xu Q. Role of histone deacetylases in vascular cell homeostasis and arteriosclerosis.. Cardiovasc Res 2011 Jun 1;90(3):413-20.
    doi: 10.1093/cvr/cvr003pubmed: 21233251google scholar: lookup

Citations

This article has been cited 9 times.
  1. He H, Fan X, Shen H, Gou H, Zhang C, Liu Z, Zhang B, Wuri N, Zhang J, Liao M, Geri L. Butyrate limits the replication of porcine epidemic diarrhea virus in intestine epithelial cells by enhancing GPR43-mediated IFN-III production. Front Microbiol 2023;14:1091807.
    doi: 10.3389/fmicb.2023.1091807pubmed: 36744090google scholar: lookup
  2. Zhang S, Wang T, Zhang D, Wang X, Zhang Z, Lim C, Lee S. Probiotic characterization of Lactiplantibacillus plantarum HOM3204 and its restoration effect on antibiotic-induced dysbiosis in mice. Lett Appl Microbiol 2022 Jun;74(6):949-958.
    doi: 10.1111/lam.13683pubmed: 35231139google scholar: lookup
  3. Tobin D, Vige R, Calder PC. Review: The Nutritional Management of Multiple Sclerosis With Propionate. Front Immunol 2021;12:676016.
    doi: 10.3389/fimmu.2021.676016pubmed: 34394076google scholar: lookup
  4. Machado MG, Sencio V, Trottein F. Short-Chain Fatty Acids as a Potential Treatment for Infections: a Closer Look at the Lungs. Infect Immun 2021 Aug 16;89(9):e0018821.
    doi: 10.1128/IAI.00188-21pubmed: 34097474google scholar: lookup
  5. Laval K, Poelaert KCK, Van Cleemput J, Zhao J, Vandekerckhove AP, Gryspeerdt AC, Garré B, van der Meulen K, Baghi HB, Dubale HN, Zarak I, Van Crombrugge E, Nauwynck HJ. The Pathogenesis and Immune Evasive Mechanisms of Equine Herpesvirus Type 1. Front Microbiol 2021;12:662686.
    doi: 10.3389/fmicb.2021.662686pubmed: 33746936google scholar: lookup
  6. Pascoal LB, Rodrigues PB, Genaro LM, Gomes ABDSP, Toledo-Teixeira DA, Parise PL, Bispo-Dos-Santos K, Simeoni CL, Guimarães PV, Buscaratti LI, Elston JGA, Marques-Souza H, Martins-de-Souza D, Ayrizono MLS, Velloso LA, Proenca-Modena JL, Moraes-Vieira PMM, Mori MAS, Farias AS, Vinolo MAR, Leal RF. Microbiota-derived short-chain fatty acids do not interfere with SARS-CoV-2 infection of human colonic samples. Gut Microbes 2021 Jan-Dec;13(1):1-9.
    doi: 10.1080/19490976.2021.1874740pubmed: 33550892google scholar: lookup
  7. Balta I, Stef L, Pet I, Ward P, Callaway T, Ricke SC, Gundogdu O, Corcionivoschi N. Antiviral activity of a novel mixture of natural antimicrobials, in vitro, and in a chicken infection model in vivo. Sci Rep 2020 Oct 6;10(1):16631.
    doi: 10.1038/s41598-020-73916-1pubmed: 33024252google scholar: lookup
  8. Xie Q, Li Q, Fang H, Zhang R, Tang H, Chen L. Gut-Derived Short-Chain Fatty Acids and Macrophage Modulation: Exploring Therapeutic Potentials in Pulmonary Fungal Infections. Clin Rev Allergy Immunol 2024 Jun;66(3):316-327.
    doi: 10.1007/s12016-024-08999-zpubmed: 38965168google scholar: lookup
  9. Lv J, Qi P, Yan X, Bai L, Zhang L. Structure and Metabolic Characteristics of Intestinal Microbiota in Tibetan and Han Populations of Qinghai-Tibet Plateau and Associated Influencing Factors. Microorganisms 2023 Oct 28;11(11).
    doi: 10.3390/microorganisms11112655pubmed: 38004668google scholar: lookup
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