Relationship between E. coli, Enterobacter spp. and S. aureus isolated from intestinal microflora and blood proteins associated with the immune system and infectious diseases during 3-day dry immersion
- Authors: Komissarova D.V.1, Larina I.M.1, Pastushkova L.H.1, Kashirina D.N.1, Usanova N.A.1, Ilyin V.K.1
-
Affiliations:
- State Scientific Center of the Russian Federation — Institute of Medical and Biological Problems of the Russian Academy of Sciences
- Issue: Vol 14, No 5 (2024)
- Pages: 951-960
- Section: ORIGINAL ARTICLES
- URL: https://journal-vniispk.ru/2220-7619/article/view/284808
- DOI: https://doi.org/10.15789/2220-7619-RBE-17615
- ID: 284808
Cite item
Full Text
Abstract
“Dry” immersion is one of the methods for simulating some factors of a space flight. Volunteer-derived intestinal microbiota previously studied by “dry” immersion showed profoundly deteriorated state of microflora and blood protein composition. The study was aimed to analyze mechanisms underlying a positive correlation with amount of intestinal E. coli, and negative correlation between S. aureus and Enterobacter spp. with the number of human blood proteins assessed by proteomics methods based on mass spectrometry, in a 3-day experiment “dry” female immersion. 6 female volunteers aged from 25 to 40 years took part in the 3-days “dry” immersion experiment. During the experiment, the subjects did not take any drugs that could affect the microflora. Fecal samples were collected once per 1–2 days before the onset of the experiment and once on days 1–3 after the end of the “dry” immersion, number of microorganisms in the above-mentioned samples was assessed. Capillary blood samples were obtained by puncture of the terminal phalanx of the ring finger 2 days before the onset of the experiment, on day 1, 2 and 3 during dry immersion and 2 days afterwards. The relationship between the level of proteins in the samples and the number of intestinal microorganisms was described using a regression model in which the blood specific protein was a dependent variable, and the number of microorganisms was an independent variable. The STATISTICA 12.0 program was used for data processing. When analyzing the data obtained, 30 proteins were identified, which positively correlated with the amount of E. coli and negatively correlated with the amount of S. aureus and Enterobacter spp. While considering the events in which these proteins are involved in the human body, they were divided into several groups. In the current study, there were examined 6 proteins associated with infectious diseases (PSMA2, PSMC3, PSME2, NCKAP1, LTF, ENO1) and 10 immune-related proteins (the above-mentioned proteins, as well as CCT2, APOB, FGB, CA1, STOM). Thus, it is necessary to continue close examination of the mechanisms underlying this relationship in the interest of ensuring spaceflight medical safety.
Keywords
Full Text
##article.viewOnOriginalSite##About the authors
Daria V. Komissarova
State Scientific Center of the Russian Federation — Institute of Medical and Biological Problems of the Russian Academy of Sciences
Author for correspondence.
Email: d.komisarova@yandex.ru
PhD (Biology), Leading Researcher, Head of Laboratory of Ecological and Hygienic Aspects of Habitability
Russian Federation, MoscowI. M. Larina
State Scientific Center of the Russian Federation — Institute of Medical and Biological Problems of the Russian Academy of Sciences
Email: d.komisarova@yandex.ru
DSc (Medicine), Professor, Leading Researcher, Head of Laboratory of Proteomics
Russian Federation, MoscowL. H. Pastushkova
State Scientific Center of the Russian Federation — Institute of Medical and Biological Problems of the Russian Academy of Sciences
Email: d.komisarova@yandex.ru
DSc (Biology), Leading Researcher, Laboratory of Proteomics
Russian Federation, MoscowD. N. Kashirina
State Scientific Center of the Russian Federation — Institute of Medical and Biological Problems of the Russian Academy of Sciences
Email: d.komisarova@yandex.ru
PhD (Biology), Senior Researcher, Laboratory of Proteomics
Russian Federation, MoscowN. A. Usanova
State Scientific Center of the Russian Federation — Institute of Medical and Biological Problems of the Russian Academy of Sciences
Email: d.komisarova@yandex.ru
Senior Researcher, Laboratory of Human Microbial Ecology
Russian Federation, MoscowV. K. Ilyin
State Scientific Center of the Russian Federation — Institute of Medical and Biological Problems of the Russian Academy of Sciences
Email: d.komisarova@yandex.ru
DSc (Medicine), Professor, RAS Corresponding Member, Head of Department of Sanitary and Hygienic Safety of Humans in Artificial Habitats, Leading Researcher, Head of Laboratory of Human Microbial Ecology
Russian Federation, MoscowReferences
- Афонин Б.В., Седова Е.А. Состояние пищеварительной системы человека при моделировании эффектов невесомости в условиях иммерсии // Авиакосмическая и экологическая медицина. 2009. Т. 43, № 1. С. 48–52. [Afonin B.V., Sedova E.A. The state of the human digestive system when modeling the effects of weightlessness under immersion conditions. Aviakosmicheskaya i ekologicheskaya meditsina = Aerospace and Environmental Medicine, 2009, vol. 43, no. 1, pp. 48–52. (In Russ.)]
- Афонин Б.В., Седова Е.А., Тихонова Г.А., Соловьева А.А., Валуев В.А. Оценка функциональных изменений печени при моделировании гемодинамических эффектов невесомости в антиортостатическом положении // Авиакосмическая и экологическая медицина. 2014. Т. 48, № 5. С. 17–22. [Afonin B.V., Sedova E.A., Tikhonova G.A., Solovyova A.A., Valuev V.A. Assessment of functional changes in the liver when modeling the hemodynamic effects of weightlessness in an anti-orthostatic position. Aviakosmicheskaya i ekologicheskaya meditsina = Aerospace and Environmental Medicine, 2014, vol. 48, no. 4, pp. 17–22. (In Russ.)]
- Балмасова И.П., Сепиашвили Р.И. Кишечные инфекции, воспаление и аутоиммунитет. Лимфоидный аппарат кишечника во взаимодействии с кишечной микрофлорой // Журнал микробиологии, эпидемиологии и иммунобиологии. 2013. № 2. C. 113–123. [Balmasova I.P., Sepiashvili R.I. Intestinal infections, inflammation and autoimmunity. Intestinal lymphoid apparatus in interaction with intestinal microflora. Zhurnal mikrobiologii, epidemiologii i mmunobiologii = Journal of Microbiology, Epidemiology and Immunobiology, 2013, no. 2, pp. 113–123. (In Russ.)]
- Гаус О.В., Беляков Д.Г. Современные взгляды на роль кишечной микробиоты в формировании патологии кишечника. // Русский медицинский журнал. 2021. № 5. С. 10–16. [Gaus O.V., Belyakov D.G. Modern views on the role of intestinal microbiota in the formation of intestinal pathology. Russkii meditsinskii zhurnal = Russian Medical Journal, 2021, no. 4, pp. 10–16. (In Russ.)]
- Ильин В.К., Афонин Б.В., Комиссарова Д.В., Шеф К.А., Агуреев А.Н., Усанова Н.А., Валуев В.А., Дзех С.А. Исследование влияния изменений микрофлоры кишечника и профилактического приема пробиотиков на функциональное состояние желудка в изоляционном эксперименте SIRIUS-18/19 // Авиакосмическая и экологическая медицина. 2021. Т. 55, № 1. С. 70–75. [Ilyin V.K., Afonin B.V., Komissarova D.V., Shef K.A., Agureev A.N., Usanova N.A., Valuev V.A., Dzekh S.A. Study of the influence of changes in intestinal microflora and prophylactic administration of probiotics on the functional state of the stomach in the SIRIUS-18/19 isolation experiment. Aviakosmicheskaya i ekologicheskaya meditsina = Aerospace and Environmental Medicine, 2021, vol. 55, no. 1, pp. 70–75. (In Russ.)] doi: 10.21687/0233-528X-2021-55-1-70-75
- Ильин В.К., Рыкова М.П., Антропова Е.Н., Соловьева З.О., Скедина М.А., Ковалева А.А. Исследование физиологических и микробиологических особенностей пародонта человека в эксперименте «сухая» иммерсия // Авиакосмическая и экологическая медицина. 2020. Т. 54, № 5. С. 112–117. [Ilyin V.K., Rykova M.P., Antropova E.N., Solovieva Z.O., Skedina M.A., Kovaleva A.A. Study of physiological and microbiological features of the human periodontium in the experiment «dry» immersion. Aviakosmicheskaya i ekologicheskaya meditsina = Aerospace and Environmental Medicine, 2020, vol. 54, no. 4, pp. 112–117. (In Russ.)] doi: 10.21687/0233-528X-2020-54-4-112-117
- Каширина Д.Н., Пастушкова Л.Х., Бржозовский А.Г., Кононихин А.С., Николаев Е.Н., Ларина И.М. Эффекты 3-суточного иммерсионного воздействия на протеом крови женщин // Авиакосмическая и экологическая медицина. 2023. Т. 57, № 2. С.47–56. [Kashirina D.N., Pastushkova L.Kh., Brzhozovsky A.G., Kononikhin A.S., Nikolaev E.N., Larina I.M. Effects of 3-day immersion on the blood proteome of women. Aviakosmicheskaya i ekologicheskaya meditsina = Aerospace and Environmental Medicine, 2023, vol. 57, no. 2, pp. 47–56. (In Russ.)] doi: 10.21687/0233-528X-2023-57-2-47-56
- Комиссарова Д.В., Ильин В.К., Припутневич Т.В., Муравьева В.В., Жигалова К.Н. Пребиотические и пробиотические способы коррекции микрофлоры влагалища у женщин участниц наземных экспериментов, моделирующих отдельные факторы космического полета // Бюллетень Оренбургского научного центра УрО РАН. 2023. № 2. С. 74–76. [Komissarova D.V., Ilyin V.K., Priputnevich T.V., Muravyova V.V., Zhigalova K.N. Prebiotic and probiotic methods for correcting vaginal microflora in female participants in ground-based experiments simulating individual factors of space flight. Byulleten’ Orenburgskogo nauchnogo tsentra UrO RAN = Bulletin of the Orenburg Federal Research Сenter UB RAS, 2023, no. 2, pp. 74–76. (In Russ.)] doi: 10.24411/2304-9081-2023-12007
- Костюкевич О.И., Былова Н.А., Симбирцев А.С. Роль кишечной микробиоты в развитии заболеваний печени и желчевыводящих путей // Русский медицинский журнал. 2016. № 11. С. 713–720. [Kostyukevich O.I., Bylova N.A., Simbirtsev A.S. The role of intestinal microbiota in the development of liver and biliary tract diseases. Russkii meditsinskii zhurnal = Russian Medical Journal, 2016. no. 11, pp. 713–720. (In Russ.)]
- Кулаичев А.П. Методы и средства комплексного статистического анализа данных: учеб. пособие. 5-е изд., перераб. и доп. М.: ИНФРА-М, 2017. 484 с. [Kulaichev A.P. Methods and means of complex statistical data analysis: tutorial. 5th ed., revised. Moscow: INFRA-M, 2017. 484 p. (In Russ.)]
- Морозов А.М., Минакова Ю.Е., Протченко И.Г. Влияние микрофлоры на синтез витаминов (обзор литературы) // Вестник новых медицинских технологий. 2019. № 6. С. 167–171. [Morozov A.M., Minakova Yu.E., Protchenko I.G. The influence of microflora on the synthesis of vitamins (review). Vestnik novykh meditsinskikh tekhnologii = Journal of New Medical Technologies, 2019, no. 6, pp. 167–171. (In Russ.)]
- Оришак Е.А., Нилова Л.Ю., Авалуева Е.Б., Бойцов А.Г. Условно-патогенные микроорганизмы при дисбактериозе кишечника // Ученые записки СПбГМУ им. И.П. Павлова. 2010. № 2. C. 24–27. [Orishak E.A., Nilova L.Yu., Avalueva E.B., Boytsov A.G. Opportunistic pathogenic microorganisms in intestinal dysbiosis. Uchenye zapiski SPbGMU im. I.P. Pavlova = Scientific Notes of Pavlov First St. Petersburg State Medical University, 2010, no. 2, pp. 24–27. (In Russ.)]
- Пастушкова Л.Х., Пахарукова Н.А., Новоселова Н.М., Доброхотов И.В., валеева О.А., Кусто М.А., Ларина И.М. Прямое протеомное профилирование мочи и сыворотки крови человека в эксперименте с 5-суточной «сухой» иммерсией. // Авиакосмическая и экологическая медицина. 2012. Т. 46, № 5. С. 31–37. [Pastushkova L.Kh., Pakharukova N.A., Novoselova N.M., Dobrokhotov I.V., Valeeva O.A., Cousteau M.A., Larina I.M. Direct proteomic profiling of human urine and serum in an experiment with a 5-day “dry” immersion. Aviakosmicheskaya i ekologicheskaya meditsina = Aerospace and Environmental Medicine, 2012, vol. 46, no. 4, pp. 31–37. (In Russ.)]
- Ткаченко Е.И. Парадигма дисбиоза в современной гастроэнтерологии. Роль микробиоты в лечении и профилактике заболеваний в XXI веке // Экспериментальная и клиническая гастроэнтерология. 2014, № 5 (105). C. 4–8. [Tkachenko E.I. The paradigm of dysbiosis in modern gastroenterology. The role of microbiota in the treatment and prevention of diseases in the 21st century. Eksperimental’naia i klinicheskaia gastroenterologiia = Experimental & Clinical Gastroenterology, 2014, no. 5 (105), pp. 4–8. (In Russ.)]
- Томиловская Е.С., Рукавишников И.В., Амирова Л.Е., Шигуева Т.А., Савеко А.А., Китов В.В., Васильева Г.Ю., Пономарев С.А., Смирнова Т.А., Козловская И.Б., Орлов О.И. 21-суточная «сухая» иммерсия: особенности проведения и основные итоги. // Авиакосмическая и экологическая медицина. 2020. Т. 54, № 5. С. 5–14. [Tomilovskaya E.S., Rukavishnikov I.V., Amirova L.E., Shigueva T.A., Saveko A.A., Kitov V.V., Vasilyeva G.Yu., Ponomarev S.A., Smirnova T. .A., Kozlovskaya I.B., Orlov O.I. 21-day “dry” immersion: features and main results. Aviakosmicheskaya i ekologicheskaya meditsina = Aerospace and Environmental Medicine, 2020, vol. 54, no. 4, pp. 5–14. (In Russ.)] doi: 10.21687/0233-528X-2020-54-4-5-14
- Усик М. Клетки под давлением // Biomolecula.ru: сайт (дата публикации: 08.12.2015) [Usik M. Cells under pressure. Biomolecule.ru: web-site (publication date: 08.12.2015) (In Russ.)] URL: https://biomolecula.ru/articles/kletki-pod-davleniem
- Benos D.J., Awayda M.S., Ismailov I.I., Johnson J.P. Structure and function of amiloride-sensitive Na+ channels. J. Membr. Biol.,1995, no. 143, pp. 1–18. doi: 10.1007/BF00232519
- Capello M., Ferri-Borgogno S., Riganti C., Chattaragada M. Samuel, Principe M., Roux C., Zhou W., Petricoin E.F., Cappello P., Novelli F. Targeting the Warburg effect in cancer cells through ENO1 knockdown rescues oxidative phosphorylation and induces growth arrest. Oncotarget, 2016, vol. 7, pp. 5598–5612. doi: 10.18632/oncotarget.6798
- Castro C.N., Rosenzwajg M., Carapito R., Shahrooei M., Konantz M., Khan A., Miao Z., Groß M., Tranchant T., Radosavljevic M., Paul N., Stemmelen T., Pitoiset F., Hirschler A., Nespola B., Molitor A., Rolli V., Pichot A., Faletti L.E., Rinaldi B., Friant S., Mednikov M., Karauzum H., Aman M.J., Carapito C., Lengerke C., Ziaee V., Eyaid W., Ehl S., Alroqi F., Parvaneh N., Bahram S. NCKAP1L defects lead to a novel syndrome combining immunodeficiency, lymphoproliferation, and hyperinflammation. J. Exp. Med., 2020, vol. 217, no. 12: e20192275. doi: 10.1084/jem.20192275 PMID: 32766723; PMCID: PMC7526481
- Chen J., Ge J.,. Zhang W., Xie X., Zhong X., Tang S. NCKAP1 is a Prognostic Biomarker for Inhibition of Cell Growth in Clear Cell Renal Cell Carcinoma. Front. Genet, 2022, vol. 13. doi: 10.3389/fgene.2022.764957
- Chung I.-C., Huang W.-Ch., Huang Y.-Ts., Chen M.-L., Tsai A.-W., Wu P.-Y., Yuan T.-T. Unrevealed roles of extracellular enolase1 (ENO1) in promoting glycolysis and procancer activities in multiple myeloma via hypoxia-inducible factor 1α. Oncology. Reports, 2023, vol. 50, no. 5. doi: 10.3892/or.2023.8642
- Devarajan P., Scaramuzzino D.A., Morrow J.S. Ankyrin binds to two distinct cytoplasmic domains of Na,K-ATPase alpha subunit. PNAS, 1995, no. 91, pp. 2965–2969. doi: 10.1073/pnas.91.8.2965
- Ebstein F., Küry S., Most V., Rosenfelt C., Scott-Boyer M.P., van Woerden G.M., Besnard T., Papendorf J.J., Studencka-Turski M., Wang T., Hsieh T.C., Golnik R., Baldridge D., Forster C., de Konink C., Teurlings S.M.W., Vignard V., van Jaarsveld R.H., Ades L., Cogné B., Mignot C., Deb W., Jongmans M.C.J., Cole F.S., van den Boogaard M.H., Wambach J.A., Wegner D.J., Yang S., Hannig V., Brault J.A., Zadeh N., Bennetts B., Keren B., Gélineau A.C., Powis Z., Towne M., Bachman K., Seeley A., Beck A.E., Morrison J., Westman R., Averill K., Brunet T., Haasters J., Carter M.T., Osmond M., Wheeler P.G., Forzano F., Mohammed S., Trakadis Y., Accogli A., Harrison R., Guo Y., Hakonarson H., Rondeau S., Baujat G., Barcia G., Feichtinger R.G., Mayr J.A., Preisel M., Laumonnier F., Kallinich T., Knaus A., Isidor B., Krawitz P., Völker U., Hammer E., Droit A., Eichler E.E., Elgersma Y., Hildebrand P.W., Bolduc F., Krüger E., Bézieau S. PSMC3 proteasome subunit variants are associated with neurodevelopmental delay and type I interferon production. Sci. Transl. Med., 2023, vol. 15, no. 698: eabo3189. doi: 10.1126/scitranslmed.abo3189
- Kardoush M.I., Ward B.J., Ndao M. Serum Carbonic Anhydrase 1 is a Biomarker for Diagnosis of Human Schistosoma mansoni Infection. Am. J. Trop. Med. Hyg., 2017, vol. 96, no. 4, pp. 842–849. doi: 10.4269/ajtmh.16-0021
- Kashirinа D., Brzhozovskiy A., Sun W., Pastushkova L., Popova O., Rusanov V., Nikolaev E., Larina I., Kononikhin A. Proteomic characterization of dry blood spots of healthy women during simulation the microgravity effects using dry immersion. Front. Physiol., 2022, no. 12: 75329. doi: 10.3389/fphys.2021.753291
- Kim K., Loessner M.J. Enterobacter sakazakii Invasion in Human Intestinal Caco-2 Cells Requires the Host Cell Cytoskeleton and Is Enhanced by Disruption of Tight Junction. Infect. Immun., 2008, vol. 76, no. 2. doi: 10.1128/iai.00937-07
- Kishimoto N., Yamamoto K., Iga N., Kirihara C., Abe T., Takamune N., Misumi S. Alpha-enolase in viral target cells suppresses the human immunodeficiency virus type 1 integration. Retrovirology, 2020, vol. 17: 31. doi: 10.1186/s12977-020-00539-9
- Makogonenko E., Tsurupa G., Ingham K., Medved L. Interaction of Fibrin(ogen) with Fibronectin: Further Characterization and Localization of the Fibronectin-Binding Site. Biochemistry, 2002, vol. 41, no. 25, pp. 7907–7913. doi: 10.1021/bi025770x
- Meier F., Brunner A.D., Koch S., Koch H., Lubeck M., Krause M., Goedecke N., Decker J., Kosinski T., Park M., Bache N., Hoerning O., Cox J., Räther O., Mann M. Online Parallel Accumulation-Serial Fragmentation (PASEF) with a novel trapped ion mobility mass spectrometer. Mol. Cell. Proteomics, 2018, vol. 17, no. 12, pp. 2534–2545. doi: 10.1074/mcp.TIR118.000900
- Mergani A., Wanes D., Schecker N., Branitzki-Heinemann K., Naim H.Y., von Köckritz-Blickwede M. Staphylococcus aureus Infection Influences the Function of Intestinal Cells by Altering the Lipid Raft-Dependent Sorting of Sucrase-Isomaltase. Front. Cell. Dev. Biol., 2021, no. 9. doi: 10.3389/fcell.2021.699970
- Nandi D., Tahiliani P., Kumar A., Chandu D. The ubiquitin-proteasome system. J. Biosci., 2006, vol. 31, pp. 137–155. doi: 10.1007/BF02705243
- Peterson M.M., Mack J.L., Hall P.R., Alsup A.A., Alexander S.M., Sully E.K., Sawires Y.S., Cheung A.L., Otto M., Gresham H.D. Apolipoprotein B Is an innate barrier against invasive Staphylococcus aureus infection. Cell. Host. Microbe., 2008, vol. 4, no. 6, pp. 555–566. doi: 10.1016/j.chom.2008.10.001
- Ruetz T., Cornick S., Guttman J.A. The Spectrin Cytoskeleton Is Crucial for Adherent and Invasive Bacterial Pathogenesis. PLoS One, 2011, vol. 6, no. 5: e19940. doi: 10.1371/journal.pone.0019940
- Scheld W.M., Strunk R.W., Balian G., Calderone R.A. Microbial adhesion to fibronectin in vitro correlates with production of endocarditis in rabbits. Proc. Soc. Exp. Biol. Med., 1988, vol. 180, no. 3, pp. 474–482. doi: 10.3181/00379727-180-42205
- Shui W., Gilmore S.A., Sheu L., Liu J., Keasling J.D., Bertozzi C.R. Quantitative proteomic profiling of host-pathogen interactions: the macrophage response to Mycobacterium tuberculosis lipids. J. Proteome Res., 2009, vol. 8, no. 1, pp. 282–289. doi: 10.1021/pr800422e
- Srinivasan Y., Elmer L., Davis J., Bennett V., Angelides K. Ankyrin and spectrin associate with voltage-dependent sodium channels in brain. Nature, 1988, no. 333, pp. 177–180.
- Suzuki M., Miyazaki K., Ikeda M., Kawaguchi Y., Sakai O. F-actin network may regulate a Cl– channel in renal proximal tubule cells. J. Membr. Biol., 1993, no. 134, pp. 31–39. doi: 10.1007/BF00233473
- Vozandychova V., Stojkova P., Hercik K., Rehulka P., Stulik J. The Ubiquitination System within Bacterial Host–Pathogen Interactions. Microorganisms, 2021, no. 9: 638. doi: 10.3390/microorganisms9030638
- Wada T., Aiba Y., Shimizu K., Takagi T., Miwa A., Koga Y. The Therapeutic Effect of Bovine Lactoferrin in the Host Infected with Helicobacter pylori. Scand. J. Gastroenterol., 1999, vol. 34, no. 3, pp. 238–243. doi: 10.1080/00365529950173627
- Xu Y.Y., Samaranayake Y.H., Samaranayake L.P., Nikawa H. In vitro susceptibility of Candida species to lactoferrin. Med. Mycol., 1999, vol. 37, no. 1, pp. 35–41. doi: 10.1046/j.1365-280x.1999.00198.x
- Yu F., He M., Li J., Wang H., Chen S., Zhang X., Zhang H., Duan G., Zhang R. Differential expression of α-enolase in clinical gastric tissues and cultured normal/cancer cells in response to Helicobacter pylori infection and cagA transfection. Medicina, 2022, vol. 58, no. 10. doi: 10.3390/medicina58101453
Supplementary files
