The mechanisms of nerve injury caused by viral infection in the occurrence of gastrointestinal motility disorder-related diseases

  • Ouyang A, Locke GR 3. rd. Overview of neurogastroenterology-gastrointestinal motility and functional GI disorders: classification, prevalence, and epidemiology. Gastroenterol Clin North Am. 2007;36:485 – 98, vii.

  • Mittal R, Vaezi MF. Esophageal motility Disorders and gastroesophageal reflux disease. N Engl J Med. 2020;383:1961–72.

    CAS 
    PubMed 

    Google Scholar 

  • Thapar N, Saliakellis E, Benninga MA, Borrelli O, Curry J, Faure C, et al. Paediatric intestinal pseudo-obstruction: evidence and Consensus-based Recommendations from an ESPGHAN-Led Expert Group. J Pediatr Gastroenterol Nutr. 2018;66:991–1019.

    PubMed 

    Google Scholar 

  • De Giorgio R, Ricciardiello L, Naponelli V, Selgrad M, Piazzi G, Felicani C et al. Chronic intestinal pseudo-obstruction related to viral infections. Transplant Proc. 2010;42:9–14.

  • Camilleri M. Gastrointestinal motility disorders in neurologic disease. J Clin Invest. 2021;131.

  • Black CJ, Drossman DA, Talley NJ, Ruddy J, Ford AC. Functional gastrointestinal disorders: advances in understanding and management. Lancet. 2020;396:1664–74.

    CAS 
    PubMed 

    Google Scholar 

  • Nurko S. Motility Disorders in Children. Pediatr Clin North Am. 2017;64:593–612.

    PubMed 

    Google Scholar 

  • Ford AC, Mahadeva S, Carbone MF, Lacy BE, Talley NJ. Functional dyspepsia. Lancet. 2020;396:1689–702.

    CAS 
    PubMed 

    Google Scholar 

  • Vaezi MF, Pandolfino JE, Yadlapati RH, Greer KB, Kavitt RT. ACG clinical guidelines: diagnosis and management of Achalasia. Am J Gastroenterol. 2020;115:1393–411.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Nehra AK, Sheedy SP, Johnson CD, Flicek KT, Venkatesh SK, Heiken JP, et al. Imaging Rev Gastrointest Motil Disorders Radiographics. 2022;42:2014–36.

    Google Scholar 

  • Brun P, Qesari M, Marconi PC, Kotsafti A, Porzionato A, Macchi V, et al. Herpes simplex virus type 1 infects enteric neurons and triggers gut dysfunction via macrophage recruitment. Front Cell Infect Microbiol. 2018;8:74.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Naik RD, Vaezi MF, Gershon AA, Higginbotham T, Chen JJ, Flores E, et al. Association of Achalasia with active varicella zoster virus infection of the Esophagus. Gastroenterology. 2021;161:719–21e2.

    PubMed 

    Google Scholar 

  • Ye L, Bae M, Cassilly CD, Jabba SV, Thorpe DW, Martin AM et al. Enteroendocrine cells sense bacterial tryptophan catabolites to activate enteric and vagal neuronal pathways. Cell Host Microbe. 2021;29:179 – 96.e9.

  • Geng ZH, Zhu Y, Li QL, Zhao C, Zhou PH. Enteric nervous system: the Bridge between the Gut Microbiota and Neurological Disorders. Front Aging Neurosci. 2022;14:810483.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Rao M, Gershon MD. The bowel and beyond: the enteric nervous system in neurological disorders. Nat Rev Gastroenterol Hepatol. 2016;13:517–28.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lake JI, Heuckeroth RO. Enteric nervous system development: migration, differentiation, and disease. Am J Physiol Gastrointest Liver Physiol. 2013;305:G1–24.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Giuffre M, Moretti R, Campisciano G, da Silveira ABM, Monda VM, Comar M et al. You talking to me? Says the enteric nervous system (ENS) to the microbe. How intestinal microbes interact with the ENS. J Clin Med. 2020;9.

  • Pawolski V, Schmidt MHH. Neuron-Glia Interaction in the developing and adult enteric nervous system. Cells. 2020;10.

  • Ngwainmbi J, De DD, Smith TH, El-Hage N, Fitting S, Kang M, et al. Effects of HIV-1 Tat on enteric neuropathogenesis. J Neurosci. 2014;34:14243–51.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Brun P, Scarpa M, Marchiori C, Conti J, Kotsafti A, Porzionato A, et al. Herpes simplex virus type 1 engages toll like receptor 2 to Recruit Macrophages during infection of enteric neurons. Front Microbiol. 2018;9:2148.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Gershon AA, Chen J, Gershon MD. Use of Saliva to identify varicella zoster virus infection of the gut. Clin Infect Dis. 2015;61:536–44.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Marasco G, Lenti MV, Cremon C, Barbaro MR, Stanghellini V, Di Sabatino A, et al. Implications of SARS-CoV-2 infection for neurogastroenterology. Neurogastroenterol Motil. 2021;33:e14104.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Goldstein RS, Kinchington PR. Varicella zoster virus neuronal latency and Reactivation Modeled in Vitro. Curr Top Microbiol Immunol. 2023;438:103–34.

    CAS 
    PubMed 

    Google Scholar 

  • Kennedy PG, Rovnak J, Badani H, Cohrs RJ. A comparison of herpes simplex virus type 1 and varicella-zoster virus latency and reactivation. J Gen Virol. 2015;96:1581–602.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Gershon AA, Chen J, Gershon MD. A model of lytic, latent, and reactivating varicella-zoster virus infections in isolated enteric neurons. J Infect Dis. 2008;197(Suppl 2):61–5.

    Google Scholar 

  • Chen JJ, Gershon AA, Li Z, Cowles RA, Gershon MD. Varicella zoster virus (VZV) infects and establishes latency in enteric neurons. J Neurovirol. 2011;17:578–89.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Gan L, Wang M, Chen JJ, Gershon MD, Gershon AA. Infected peripheral blood mononuclear cells transmit latent varicella zoster virus infection to the guinea pig enteric nervous system. J Neurovirol. 2014;20:442–56.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Chen JJ, Gershon AA, Li ZS, Lungu O, Gershon MD. Latent and lytic infection of isolated guinea pig enteric ganglia by varicella zoster virus. J Med Virol. 2003;70(Suppl 1):71–8.

    Google Scholar 

  • Brun P, Conti J, Zatta V, Russo V, Scarpa M, Kotsafti A, et al. Persistent herpes simplex virus type 1 infection of enteric neurons triggers CD8(+) T cell response and gastrointestinal neuromuscular dysfunction. Front Cell Infect Microbiol. 2021;11:615350.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Amlie-Lefond C, Gilden D. Varicella Zoster Virus: A Common cause of stroke in children and adults. J Stroke Cerebrovasc Dis. 2016;25:1561–9.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Wilson AC, Mohr I. A cultured affair: HSV latency and reactivation in neurons. Trends Microbiol. 2012;20:604–11.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Gershon AA, Chen J, Davis L, Krinsky C, Cowles R, Reichard R, et al. Latency of varicella zoster virus in dorsal root, cranial, and enteric ganglia in vaccinated children. Trans Am Clin Climatol Assoc. 2012;123:17–33. discussion – 5.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Gershon MD, Gershon AA. VZV infection of keratinocytes: production of cell-free infectious virions in vivo. Curr Top Microbiol Immunol. 2010;342:173–88.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Gesser RM, Koo SC. Oral inoculation with herpes simplex virus type 1 infects enteric neuron and mucosal nerve fibers within the gastrointestinal tract in mice. J Virol. 1996;70:4097–102.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Guedia J, Brun P, Bhave S, Fitting S, Kang M, Dewey WL, et al. HIV-1 Tat exacerbates lipopolysaccharide-induced cytokine release via TLR4 signaling in the enteric nervous system. Sci Rep. 2016;6:31203.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Gesser RM, Valyi-Nagy T, Altschuler SM, Fraser NW. Oral-oesophageal inoculation of mice with herpes simplex virus type 1 causes latent infection of the vagal sensory ganglia (nodose ganglia). J Gen Virol. 1994;75(Pt 9):2379–86.

    PubMed 

    Google Scholar 

  • Julio-Pieper M, López-Aguilera A, Eyzaguirre-Velásquez J, Olavarría-Ramírez L, Ibacache-Quiroga C, Bravo JA et al. Gut susceptibility to viral Invasion: contributing roles of Diet, Microbiota and Enteric Nervous System to Mucosal Barrier Preservation. Int J Mol Sci. 2021;22.

  • Narita M, Kimura K, Tanimura N, Arai S, Uchimura A. Immunohistochemical demonstration of spread of Aujeszky’s disease virus to the porcine central nervous system after intestinal inoculation. J Comp Pathol. 1998;118:329–36.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Pfannkuche H, Konrath A, Buchholz I, Richt JA, Seeger J, Müller H, et al. Infection of the enteric nervous system by Borna disease virus (BDV) upregulates expression of calbindin D-28k. Vet Microbiol. 2008;127:275–85.

    CAS 
    PubMed 

    Google Scholar 

  • Khoury-Hanold W, Yordy B, Kong P, Kong Y, Ge W, Szigeti-Buck K, et al. Viral spread to enteric neurons links genital HSV-1 infection to toxic megacolon and lethality. Cell Host Microbe. 2016;19:788–99.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Gershon M, Gershon A. Varicella-Zoster Virus and the enteric nervous system. J Infect Dis. 2018;218:113–s9.

    Google Scholar 

  • Ku CC, Padilla JA, Grose C, Butcher EC, Arvin AM. Tropism of varicella-zoster virus for human tonsillar CD4(+) T lymphocytes that express activation, memory, and skin homing markers. J Virol. 2002;76:11425–33.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Sen N, Mukherjee G, Sen A, Bendall SC, Sung P, Nolan GP, et al. Single-cell mass cytometry analysis of human tonsil T cell remodeling by varicella zoster virus. Cell Rep. 2014;8:633–45.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hoffmann M, Kleine-Weber H, Schroeder S, Krüger N, Herrler T, Erichsen S et al. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell. 2020;181:271 – 80.e8.

  • Fenrich M, Mrdenovic S, Balog M, Tomic S, Zjalic M, Roncevic A, et al. SARS-CoV-2 dissemination through peripheral nerves explains multiple Organ Injury. Front Cell Neurosci. 2020;14:229.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kariyawasam JC, Jayarajah U, Riza R, Abeysuriya V, Seneviratne SL. Gastrointestinal manifestations in COVID-19. Trans R Soc Trop Med Hyg. 2021;115:1362–88.

    CAS 
    PubMed 

    Google Scholar 

  • Shinu P, Morsy MA, Deb PK, Nair AB, Goyal M, Shah J, et al. SARS CoV-2 Organotropism Associated Pathogenic Relationship of Gut-Brain Axis and Illness. Front Mol Biosci. 2020;7:606779.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Esposito G, Pesce M, Seguella L, Sanseverino W, Lu J, Sarnelli G. Can the enteric nervous system be an alternative entrance door in SARS-CoV2 neuroinvasion? Brain Behav Immun. 2020;87:93–4.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Spencer NJ, Hu H. Enteric nervous system: sensory transduction, neural circuits and gastrointestinal motility. Nat Rev Gastroenterol Hepatol. 2020;17:338–51.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Ra SH, Kwon JS, Kim JY, Cha HH, Lee HJ, Jung J, et al. Frequency of putative enteric zoster diagnosed using saliva samples in patients with abdominal pain: a prospective study. Infect Dis (Lond). 2021;53:713–8.

    CAS 
    PubMed 

    Google Scholar 

  • Cipriani G, Gibbons SJ, Kashyap PC, Farrugia G. Intrinsic gastrointestinal macrophages: their phenotype and role in gastrointestinal motility. Cell Mol Gastroenterol Hepatol. 2016;2:120–30.e1.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Brun P, Giron MC, Zoppellaro C, Bin A, Porzionato A, De Caro R, et al. Herpes simplex virus type 1 infection of the rat enteric nervous system evokes small-bowel neuromuscular abnormalities. Gastroenterology. 2010;138:1790–801.

    CAS 
    PubMed 

    Google Scholar 

  • Barbara G, Cremon C, Pallotti F, De Giorgio R, Stanghellini V, Corinaldesi R. Postinfectious irritable bowel syndrome. J Pediatr Gastroenterol Nutr. 2009;48(Suppl 2):95–7.

    Google Scholar 

  • Egan KP, Wu S, Wigdahl B, Jennings SR. Immunological control of herpes simplex virus infections. J Neurovirol. 2013;19:328–45.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Braun J. Flaviviruses hit a moving target. Cell. 2018;175:1175–6.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Facco M, Brun P, Baesso I, Costantini M, Rizzetto C, Berto A, et al. T cells in the myenteric plexus of achalasia patients show a skewed TCR repertoire and react to HSV-1 antigens. Am J Gastroenterol. 2008;103:1598–609.

    PubMed 

    Google Scholar 

  • Mohammed FS, Krogel N. Post-COVID-19 Achalasia? Dig Dis Sci. 2023;68:333–4.

    PubMed 

    Google Scholar 

  • Gaber CE, Cotton CC, Eluri S, Lund JL, Farrell TM, Dellon ES. Autoimmune and viral risk factors are associated with achalasia: a case-control study. Neurogastroenterol Motil. 2022;34:e14312.

    PubMed 

    Google Scholar 

  • Robertson CS, Martin BA, Atkinson M. Varicella-zoster virus DNA in the oesophageal myenteric plexus in achalasia. Gut. 1993;34:299–302.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Boeckxstaens GE. Achalasia: virus-induced euthanasia of neurons? Am J Gastroenterol. 2008;103:1610–2.

    PubMed 

    Google Scholar 

  • Kahrilas PJ, Boeckxstaens G. The spectrum of achalasia: lessons from studies of pathophysiology and high-resolution manometry. Gastroenterology. 2013;145:954–65.

    PubMed 

    Google Scholar 

  • Jia X, Chen S, Zhuang Q, Tan N, Zhang M, Cui Y, et al. Achalasia: the current clinical dilemma and possible pathogenesis. J Neurogastroenterol Motil. 2023;29:145–55.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Amin I, Younas S, Afzal S, Shahid M, Idrees M. Herpes simplex virus type 1 and host antiviral Immune responses: an update. Viral Immunol. 2019;32:424–9.

    CAS 
    PubMed 

    Google Scholar 

  • Zhang F, Lau RI, Liu Q, Su Q, Chan FKL, Ng SC. Gut microbiota in COVID-19: key microbial changes, potential mechanisms and clinical applications. Nat Rev Gastroenterol Hepatol. 2023;20:323–37.

    PubMed 

    Google Scholar 

  • Nagata N, Takeuchi T, Masuoka H, Aoki R, Ishikane M, Iwamoto N, et al. Human gut microbiota and its metabolites Impact Immune responses in COVID-19 and its complications. Gastroenterology. 2023;164:272–88.

    CAS 
    PubMed 

    Google Scholar 

  • Zuo T, Wu X, Wen W, Lan P. Gut microbiome alterations in COVID-19. Genomics Proteom Bioinf. 2021;19:679–88.

    Google Scholar 

  • Dhar D, Mohanty A. Gut microbiota and Covid-19- possible link and implications. Virus Res. 2020;285:198018.

    CAS 
    PubMed 

    Google Scholar 

  • Yeoh YK, Zuo T, Lui GC, Zhang F, Liu Q, Li AY, et al. Gut microbiota composition reflects disease severity and dysfunctional immune responses in patients with COVID-19. Gut. 2021;70:698–706.

    CAS 
    PubMed 

    Google Scholar 

  • Ben Haij N, Leghmari K, Planès R, Thieblemont N, Bahraoui E. HIV-1 Tat protein binds to TLR4-MD2 and signals to induce TNF-α and IL-10. Retrovirology. 2013;10:123.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Anitha M, Vijay-Kumar M, Sitaraman SV, Gewirtz AT, Srinivasan S. Gut microbial products regulate murine gastrointestinal motility via Toll-like receptor 4 signaling. Gastroenterology. 2012;143:1006-16.e4.

  • Planès R, Ben Haij N, Leghmari K, Serrero M, BenMohamed L, Bahraoui E. HIV-1 Tat protein activates both the MyD88 and TRIF pathways to induce tumor necrosis factor alpha and Interleukin-10 in human monocytes. J Virol. 2016;90:5886–98.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Galligan JJ. HIV, opiates, and enteric neuron dysfunction. Neurogastroenterol Motil. 2015;27:449–54.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • White JP, Xiong S, Malvin NP, Khoury-Hanold W, Heuckeroth RO, Stappenbeck TS et al. Intestinal dysmotility syndromes following systemic infection by Flaviviruses. Cell. 2018;175:1198 – 212.e12.

  • Leave a Reply

    Your email address will not be published. Required fields are marked *