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Research Paper

Ascorbate deficiency increases progression of shigellosis in guinea pigs and mice infection models

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Article: 2271597 | Received 20 Apr 2023, Accepted 12 Oct 2023, Published online: 24 Oct 2023

References

  • Lozano R, Naghavi M, Foreman K, Lim S, Shibuya K, Aboyans V, Abraham J, Adair T, Aggarwal R, Ahn SY, et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the global burden of disease study 2010. Lancet. 2012;380(9859):2095–18. doi:10.1016/S0140-6736(12)61728-0.
  • Tacconelli E, Carrara E, Savoldi A, Harbarth S, Mendelson M, Monnet DL, Pulcini C, Kahlmeter G, Kluytmans J, Carmeli Y, et al. Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis. Lancet Infect Dis. 2017;18(3):318–327. doi:10.1016/S1473-3099(17)30753-3.
  • Marteyn BS. Shigella vaccine development: the model matters. JSM Trop Med Res. 2016;2:1011–1014.
  • Water and Sanitation-Related Diseases and the Environment: Challenges, Interventions, and Preventive Measures. Edited by Janine M. H. Selendy. Hoboken (New Jersey): Wiley-Blackwell. $139.95 (paper). xvii + 497 p. + 16 pl.; ill.; index. ISBN: 978-0-470-52785-6. [Two DVDs are included.] 2011. Q Rev Biology 2013; 88:238–238.
  • Mahbub MM, Ahsan CR, Yasmin M, Nessa J. Analysis of different prognostic indicators for malnutrition and Shigella flexneri infection among the children in Bangladesh. Indian J Microbiol. 2012;52(3):400–405. doi:10.1007/s12088-012-0247-1.
  • Ferdous F, Das SK, Ahmed S, Farzana FD, Latham JR, Chisti MJ, Ud-Din AIMS, Azmi IJ, Talukder KA, Faruque ASG. Severity of diarrhea and malnutrition among under five-year-old children in rural Bangladesh. Am J Tropical Medicine Hyg. 2013;89(2):223–228. doi:10.4269/ajtmh.12-0743.
  • Hossain S, Biswas R, Kabir I, Sarker S, Dibley M, Fuchs G, Mahalanabis D. Single dose vitamin a treatment in acute shigellosis in Bangladeshi children: randomised double blind controlled trial. Bmj. 1998;316(7129):422–426. doi:10.1136/bmj.316.7129.422.
  • Roy SK, Raqib R, Khatun W, Azim T, Chowdhury R, Fuchs GJ, Sack DA. Zinc supplementation in the management of shigellosis in malnourished children in Bangladesh. Eur J Clin Nutr. 2008;62(7):849–855. doi:10.1038/sj.ejcn.1602795.
  • WHO. Guidelines for the control of shigellosis, including epidemics due to Shigella dysenteriae type 1. 2005.
  • Fontaine A, Arondel J, Sansonetti PJ. Role of Shiga toxin in the pathogenesis of bacillary dysentery, studied by using a tox- mutant of Shigella dysenteriae 1. Infect Immun. 1988;56(12):3099–3109. doi:10.1128/iai.56.12.3099-3109.1988.
  • Medeiros PHQS, Bolick DT, Ledwaba SE, Kolling GL, Costa DVS, Oriá RB, Lima AÂM, Barry EM, Guerrant RL. A bivalent vaccine confers immunogenicity and protection against Shigella flexneri and enterotoxigenic Escherichia coli infections in mice. NPJ Vaccines. 2020;5(1):30. doi:10.1038/s41541-020-0180-y.
  • Mitchell PS, Roncaioli JL, Turcotte EA, Goers L, Chavez RA, Lee AY, Lesser CF, Rauch I, Vance RE. NAIP–NLRC4-deficient mice are susceptible to shigellosis. Elife. 2020;9:e59022. doi:10.7554/eLife.59022.
  • Shim D-H, Suzuki T, Chang S-Y, Park S-M, Sansonetti PJ, Sasakawa C, Kweon M-N. New animal model of shigellosis in the Guinea pig: its usefulness for protective efficacy studies. J Immunol. 2007;178(4):2476–2482. doi:10.4049/jimmunol.178.4.2476.
  • Brunner K, Samassa F, Sansonetti PJ, Phalipon A. Shigella-mediated immunosuppression in the human gut: subversion extends from innate to adaptive immune responses. Hum Vaccines Immunother. 2019;15(6):1317–1325. doi:10.1080/21645515.2019.1594132.
  • Levine MM, Kotloff KL, Barry EM, Pasetti MF, Sztein MB. Clinical trials of Shigella vaccines: two steps forward and one step back on a long, hard road. Nat Rev Microbiol. 2007;5(7):540–553. doi:10.1038/nrmicro1662.
  • Wenzel H, Kaminski RW, Clarkson KA, Maciel M, Smith MA, Zhang W, Oaks EV. Improving chances for successful clinical outcomes with better preclinical models. Vaccine. 2017;35(49):6798–6802. doi:10.1016/j.vaccine.2017.08.030.
  • McArthur MA, Maciel M, Pasetti MF. Human immune responses against Shigella and enterotoxigenic E. coli: Current advances and the path forward. Vaccine. 2017;35(49):6803–6806. doi:10.1016/j.vaccine.2017.05.034.
  • Honjo S, Takasaka M, Fujiwara T, Imaizumi K, Ogawa H. Shigellosis in cynomolgus monkeys (MACACA IRUS). Jpn J Medical Sci Biol. 1969;22(3):149–162. doi:10.7883/yoken1952.22.149.
  • Lind J A treatise of the scurvy in three parts. 1753;
  • Bollet AJ. Scurvy and chronic diarrhea in Civil war troops: were they both nutritional deficiency syndromes? J Hist Med All Sci. 1992;47(1):49–67. doi:10.1093/jhmas/47.1.49.
  • Moya‐Alvarez V, Koyembi JJ, Kayé LM, Mbecko J, Sanke‐Waîgana H, Djorie SG, Nyasenu YT, Mad‐Bondo D, Kongoma J, Nakib S, et al. Vitamin C levels in a Central‐African mother–infant cohort: does hypovitaminosis C increase the risk of enteric infections? Maternal Child Nutr. 2021;17(4):e13215. doi:10.1111/mcn.13215.
  • Anderson MC, Chaze T, Coïc Y-M, Injarabian L, Jonsson F, Lombion N, Selimoglu-Buet D, Souphron J, Ridley C, Vonaesch P, et al. MUB40 binds to lactoferrin and stands as a specific neutrophil marker. Cell Chem Biol. 2018;25(4):483–493.e9. doi:10.1016/j.chembiol.2018.01.014.
  • Marteyn BS, Karimova G, Fenton AK, Gazi AD, West N, Touqui L, Prevost M-C, Betton J-M, Poyraz O, Ladant D, et al. Zape is a novel cell division protein interacting with FtsZ and modulating the Z-Ring dynamics. Mbio. 2014;5(2):e00022–14. doi:10.1128/mBio.00022-14.
  • Tinevez J-Y, Arena ET, Anderson M, Nigro G, Injarabian L, André A, Ferrari M, Campbell-Valois F-X, Devin A, Shorte SL, et al. Shigella-mediated oxygen depletion is essential for intestinal mucosa colonization. Nat Microbiol. 2019;4(11):2001–2009. doi:10.1038/s41564-019-0525-3.
  • Mortensen A, Hasselholt S, Tveden-Nyborg P, Lykkesfeldt J. Guinea pig ascorbate status predicts tetrahydrobiopterin plasma concentration and oxidation ratio in vivo. Nutr Res New York N Y. 2013;33(10):859–867. doi:10.1016/j.nutres.2013.07.006.
  • Injarabian L, Scherlinger M, Devin A, Ransac S, Lykkesfeldt J, Marteyn BS. Ascorbate maintains a low plasma oxygen level. Sci Rep-Uk. 2020;10(1):10659. doi:10.1038/s41598-020-67778-w.
  • Padayatty SJ, Levine M. Vitamin C: the known and the unknown and goldilocks. Oral Dis. 2016;22(6):463–493. doi:10.1111/odi.12446.
  • Buck A, Aichler M, Huber K, Walch A. Chapter five in situ metabolomics in cancer by mass spectrometry imaging. Adv Cancer Res. 2017;134:117–132.
  • Aichler M, Walch A. MALDI imaging mass spectrometry: current frontiers and perspectives in pathology research and practice. Lab Investig. 2015;95(4):422–431. doi:10.1038/labinvest.2014.156.
  • Maeda N, Hagihara H, Nakata Y, Hiller S, Wilder J, Reddick R. Aortic wall damage in mice unable to synthesize ascorbic acid. Proc Natl Acad Sci. 2000;97(2):841–846. doi:10.1073/pnas.97.2.841.
  • Carr AC, Lykkesfeldt J. Discrepancies in global vitamin C recommendations: a review of RDA criteria and underlying health perspectives. Crit Rev Food Sci Nutr. 2021;61(5):742–755. doi:10.1080/10408398.2020.1744513.
  • Preston AM, Rodríguez C, Rivera CE. Plasma ascorbate in a population of children: influence of age, gender, vitamin C intake, BMI and smoke exposure. P R Health Sci J. 2006;25:137–142.
  • Jensen PØ, Lykkesfeldt J, Bjarnsholt T, Hougen HP, Høiby N, Ciofu O. Poor antioxidant status exacerbates oxidative stress and inflammatory response to Pseudomonas aeruginosa lung infection in Guinea pigs. Basic Clin Pharmacol Toxicol. 2012;110(4):353–358. doi:10.1111/j.1742-7843.2011.00822.x.
  • Hasselholt S, Tveden-Nyborg P, Lykkesfeldt J. Distribution of vitamin C is tissue specific with early saturation of the brain and adrenal glands following differential oral dose regimens in guinea pigs. Br J Nutr. 2015;113(10):1539–1549. doi:10.1017/S0007114515000690.
  • Arena ET, Campbell-Valois F-X, Tinevez J-Y, Nigro G, Sachse M, Moya-Nilges M, Nothelfer K, Marteyn B, Shorte SL, Sansonetti PJ. Bioimage analysis of Shigella infection reveals targeting of colonic crypts. Proc National Acad Sci. 2015;112(25):E3282–90. doi:10.1073/pnas.1509091112.
  • Phalipon A, Kaufmann M, Michetti P, Cavaillon JM, Huerre M, Sansonetti P, Kraehenbuhl JP. Monoclonal immunoglobulin a antibody directed against serotype-specific epitope of Shigella flexneri lipopolysaccharide protects against murine experimental shigellosis. J Exp Medicine. 1995;182(3):769–778. doi:10.1084/jem.182.3.769.
  • Boullier S, Tanguy M, Kadaoui KA, Caubet C, Sansonetti P, Corthésy B, Phalipon A. Secretory IgA-mediated neutralization of Shigella flexneri prevents intestinal tissue destruction by down-regulating inflammatory circuits. J Immunol Baltim Md 1950. 2009;183(9):5879–5885. doi:10.4049/jimmunol.0901838.
  • Zychlinsky A, Prevost MC, Sansonetti PJ. Shigella flexneri induces apoptosis in infected macrophages. Nature. 1992;358(6382):167–169. doi:10.1038/358167a0.
  • Nothelfer K, Arena ET, Pinaud L, Neunlist M, Mozeleski B, Belotserkovsky I, Parsot C, Dinadayala P, Burger-Kentischer A, Raqib R, et al. B lymphocytes undergo TLR2-dependent apoptosis upon Shigella infection. J Exp Medicine. 2014;211(6):1215–1229. doi:10.1084/jem.20130914.
  • Salgado-Pabón W, Celli S, Arena ET, Nothelfer K, Roux P, Sellge G, Frigimelica E, Bousso P, Sansonetti PJ, Phalipon A. Shigella impairs T lymphocyte dynamics in vivo. P Natl Acad Sci USA. 2013;110(12):4458–4463. doi:10.1073/pnas.1300981110.
  • Konradt C, Frigimelica E, Nothelfer K, Puhar A, Salgado-Pabon W, di BV, Scott-Algara D, Rodrigues CD, Sansonetti PJ, Phalipon A. The Shigella flexneri type three secretion system effector IpgD inhibits T cell migration by manipulating host phosphoinositide metabolism. Cell Host Microbe. 2011;9(4):263–272. doi:10.1016/j.chom.2011.03.010.
  • Luchetti G, Roncaioli JL, Chavez RA, Schubert AF, Kofoed EM, Reja R, Cheung TK, Liang Y, Webster JD, Lehoux I, et al. Shigella ubiquitin ligase IpaH7.8 targets gasdermin D for degradation to prevent pyroptosis and enable infection. Cell Host Microbe. 2021;29(10):1521–1530.e10. doi:10.1016/j.chom.2021.08.010.
  • Heskett CW, Teafatiller T, Hennessey C, Gareau MG, Marchant JS, Said HM, Subramanian VS. Enteropathogenic Escherichia coli infection inhibits intestinal ascorbic acid uptake via dysregulation of its transporter expression. Dig Dis Sci. 2021;66(7):2250–2260. doi:10.1007/s10620-020-06389-x.
  • Ang A, Pullar JM, Currie MJ, Vissers MCM. Vitamin C and immune cell function in inflammation and cancer. Biochem Soc Trans. 2018;46(5):1147–1159. doi:10.1042/BST20180169.
  • Carr AC, Maggini S. Vitamin C and immune function. Nutrients. 2017;9(11):1211. doi:10.3390/nu9111211.
  • Morante-Palacios O, Godoy-Tena G, Calafell-Segura J, Ciudad L, Martínez-Cáceres EM, Sardina JL, Ballestar E. Vitamin C enhances NF-κB-driven epigenomic reprogramming and boosts the immunogenic properties of dendritic cells. Nucleic Acids Res. 2022;50(19):10981–10994. doi:10.1093/nar/gkac941.
  • Anderson MC, Vonaesch P, Saffarian A, Marteyn BS, Sansonetti PJ. Shigella sonnei encodes a functional T6SS used for interbacterial competition and niche occupancy. Cell Host Microbe. 2017;21(6):769–776.e3. doi:10.1016/j.chom.2017.05.004.
  • Monceaux V, Chiche-Lapierre C, Chaput C, Witko-Sarsat V, Prevost M-C, Taylor CT, Ungeheuer M-N, Sansonetti PJ, Marteyn BS. Anoxia and glucose supplementation preserve neutrophil viability and function. Blood. 2016;128(7):993–1002. doi:10.1182/blood-2015-11-680918.
  • Marteyn B, West NP, Browning DF, Cole JA, Shaw JG, Palm F, Mounier J, Prévost M-C, Sansonetti P, Tang CM. Modulation of Shigella virulence in response to available oxygen in vivo. Nature. 2010;465(7296):355–358. doi:10.1038/nature08970.