In vitro interaction of hormone-conditioned neutrophils with commensal and uropathogenic Escherichia coli biofilms
- Authors: Maslennikova I.L.1, Nekrasova I.V.1, Orlova E.G.1, Gorbunova O.L.1, Shirshev S.V.2
-
Affiliations:
- Institute of Ecology and Genetics of Microrganisms Ural Branch Russian Academy of Science
- Institute of Ecology and Genetics of Microorganisms Ural Branch Russian Academy of Science
- Issue: Vol 10, No 1 (2020)
- Pages: 64-72
- Section: ORIGINAL ARTICLES
- Submitted: 12.02.2019
- Accepted: 10.06.2019
- Published: 05.04.2020
- URL: https://iimmun.ru/iimm/article/view/1146
- DOI: https://doi.org/10.15789/2220-7619-IVI-1146
- ID: 1146
Cite item
Full Text
Abstract
The aim of the work was to examine an interaction between neutrophils conditioned with chorionic gonadotropin, estriol, kisspeptin, leptin, ghrelin and commensal and uropathogenic Escherichia coli biofilms. Peripheral blood neutrophils isolated from healthy non-pregnant women in the first phase of the menstrual cycle (n = 8) were cultured in vitro for 1 hour together with hormones at concentration corresp onding to their level in the first and third trimester of pregnancy. An interaction of neutrophils with commensal E. coli TG1 and uropathogenic E. coli DL82 (UPEC) biofilms was assessed 1 hour later. The biofilm biomass, activity of myeloperoxidase and cathepsin G was measured spectrophotometrically on a microplate reader Synergy H1 (BioTec, USA). Neutrophils conditioned with chorionic gonadotropin (10; 100 IU/ml), estriol (2; 20 ng/ml) and leptin (10 ng/ml) were found to enhance their potential to destroy solely opsonized commensal E. coli biofilm, without affecting the UPEC biofilm. The biomass of non-opsonized biofilm of commensal E. coli TG1 decreased after interaction with neutrophils conditioned with estriol (2 ng/ml), kisspeptin (9.6 pM) and ghrelin (0.83 ng/ml). In contrast, non-opsonized UPEC biofilm was more destroyed by neutrophils exposed to low- vs. high-dose chorionic gonadotropin (10 IU/ml and 100 IU/ml, respectively) or control group. Myeloperoxidase secretion increased when UPEC interacted with neutrophils conditioned with estriol at concentration of 2 ng/ml. Comparing the two E. coli strains allowed to find that chorionic gonadotropin (10 IU/ml) and estriol (20 ng/ml) enhanced activity of neutrophil myeloperoxidase after interaction with UPEC biofilms to a greater extent than with E. coli TG1 biofilms. Estriol (20 ng/ml) and kisspeptin (9 pM) reduced activity of neutrophil cathepsin G after interaction with UPEC biofilms.
Keywords
About the authors
I. L. Maslennikova
Institute of Ecology and Genetics of Microrganisms Ural Branch Russian Academy of Science
Author for correspondence.
Email: I.Maslennikova1974@gmail.com
ORCID iD: 0000-0002-2776-8023
Irina L. Maslennikova - PhD (Biology), Senior Researcher, Laboratory of Immunoregulation.
614081, Perm, Goleva str., 13, Phone: +7 922 317-87-77 (mobile)
РоссияI. V. Nekrasova
Institute of Ecology and Genetics of Microrganisms Ural Branch Russian Academy of Science
Email: nirina5@mail.ru
Nekrasova I.V., PhD (Biology), Researcher, Laboratory of Immunoregulation.
Perm
РоссияE. G. Orlova
Institute of Ecology and Genetics of Microrganisms Ural Branch Russian Academy of Science
Email: orlova_katy@mail.ru
Orlova E.G., PhD, MD (Biology), Leading Researcher, Laboratory of Immunoregulation.
Perm
РоссияO. L. Gorbunova
Institute of Ecology and Genetics of Microrganisms Ural Branch Russian Academy of Science
Email: olia15_77@mail.ru
Gorbunova O.L., PhD (Biology), Researcher, Laboratory of Immunoregulation.
Perm
РоссияS. V. Shirshev
Institute of Ecology and Genetics of Microorganisms Ural Branch Russian Academy of Science
Email: shirshev@iegm.ru
PhD, MD (Medicine), Professor, Head of Laboratory of Immunoregulation.
Perm
РоссияReferences
- Горбунова О.Л., Ширшев С.В. Комплексное исследование иммуномодулирующей активности кисспептина // Российский иммунологический журнал. 2014. Т. 8, № 3. С. 288—290.
- Данилов В.С., Зарубина А.П., Ерошников Г.Е., Соловьева Л.Н., Карташев Ф.В., Завильгельский Г.Б. Сенсорные биолюминесцентные системы на основе lux-оперонов разных видов люминесцентных бактерий // Вестник Московского университета. Серия 16: Биология. 2002. № 3. С. 20.
- Куклина Е.М., Ширшев С.В. Регуляция окислительной активности нейтрофилов хорионическим гонадотропином. Роль женских половых стероидных гормонов // Известия Российской академии наук. Серия биологическая. 2003. № 4. С. 399—404.
- Некрасова И.В., Ширшев С.В. Женские половые стероидные гормоны в регуляции ферментативной активности нейтрофилов // Доклады академии наук. 2013. Т. 453, № 6. С. 690—693.
- Орлова Е.Г., Ширшев С.В. модуляция лептином функциональной активности нейтрофилов и моноцитов периферической крови женщин // Цитокины и воспаление. 2007. Т. 6, № 3. С. 44—48.
- Чеботарь И.В., Маянский А.Н., Кончакова Е.Д. Нейтрофилы и бактериальные биопленки: диалектика взаимоотношений // Журнал микробиологии, эпидемиологии и иммунобиологии. 2013. № 6. С. 105—112.
- Шипицына Е.В., Хуснутдинова Т.А., Савичева А.М., Айвазян Т.А. Инфекции мочевыводящих путей в акушерстве и гинекологии // Журнал акушерства и женских болезней. 2015. № 6. С. 91—104.
- Ширшев С.В., Масленникова И.Л., Некрасова И.В. Влияние секретируемых метаболитов Escherichia coli на функциональную активность нейтрофилов человека на фоне действия эстриола // Журнал микробиологии, эпидемиологии и иммунобиологии. 2014. № 5. С. 65—70.
- Ширшев С.В., Орлова Е.Г., Сабанцева Ю.П. Роль грелина в регуляции фагоцитарной и микробицидной активности нейтрофилов // Вестник Пермского университета. Серия: Биология. 2015. № 4. С. 378—381.
- Cole L.A. hCG, the wonder of today’s science. Reprod. Biol. Endocrinol., 2012, vol. 10, no. 24. doi: 10.1186/1477-7827-10-24
- Coote J.G. The RTX toxins of Gram-negative bacterial pathogens: modulators of the host immune system. Rev. Med. Microbiol., 1996, vol. 7, no. 1,pp. 53-62. doi: 10.1097/00013542-199601000-00006
- Dapunt U., Hansch G.M., Arciola C.R. Innate immune response in implant-associated infections: neutrophils against biofilms. Materials (Basel), 2016, vol. 9, no. 5: E387. doi: 10.3390/ma9050387
- Donlan R.M. Biofilm formation: a clinically relevant microbiological process. Clin. Infect. Dis, 2001, vol. 33, no. 8, pp. 1387—1392. doi: 10.1086/322972
- Eberly A.R., Floyd K.A., Beebout C.J., Colling S.J., Fitzgerald M.J., Stratton C.W., Schmitz J.E., Hadjifrangiskou M. Biofilm formation by uropathogenic Escherichia coli is favored under oxygen conditions that mimic the bladder environment. Int. J. Mol. Sci, 2017, vol. 18, no. 10: E2077. doi: 10.3390/ijms18102077
- Fattahi S., Kafil H.S., Nahai M.R., Asgharzadeh M., Nori R., Aghazadeh M. Relationship of biofilm formation and different virulence genes in uropathogenic Escherichia coli isolates from Northwest Iran. GMS Hyg. Infect. Control, 2015, vol. 10:11 doi: 10.3205/dgkh000254
- Fuglsang J., Skjaerbaek C., Espelund U., Frystyk J., Fisker S., Flyvbjerg A., Ovesen P. Ghrelin and its relationship to growth hormones during normal pregnancy. Clin. Endocrinol. (Oxf), 2005, vol. 62, no. 5, pp. 554—559. doi: 10.1111/j.1365-2265.2005.02257.x
- Gajewski M., Rzodkiewicz P., Gajewska J., Wojtecka-Eukasik E. The effect of leptin on the respiratory burst of human neutrophils cultured in synovial fluid. Reumatologia, 2015, vol. 53, no. 1, pp. 21—25. doi: 10.5114/reum.2015.50553
- Gargan R.A., Brumfitt W., Hamilton-Miller J.M. Pre-opsonisation of Escherichia coli induces resistance to neutrophil killing in serum and urine: relationship to growth phase. J. Med. Microbiol., 1991, vol. 35, no. 1, pp. 12—17.
- Hall-Stoodley L., Costerton J.W., Stoodley P. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol., 2004, vol. 2, no. 2, pp. 95—108.
- Hardie L., Trayhurn P., Abramovich D., Fowler P. Circulating leptin in women: a longitudinal study in the menstrual cycle and during pregnancy. Clin. Endocrinol. (Oxf)., 1997, vol. 47, no. 1, pp. 101—106. doi: 10.1046/j.1365-2265.1997.2441017.x
- Hashemizadeh Z., Kalantar-Neyestanaki D., Mansouri S. Association between virulence profile, biofilm formation and phylogenetic groups of Escherichia coli causing urinary tract infection and the commensal gut microbiota: a comparative analysis. Microb. Pathog., 2017, vol. 110, pp. 540—545. doi: 10.1016/j.micpath.2017.07.046
- Hattori N. Expression, regulation and biological actions of growth hormone (GH) and ghrelin in the immune system. Growth Horm. IGF Res., 2009, vol. 19, no. 3, pp. 187-97. doi: 10.1016/j.ghir.2008.12.001
- Hirschfeld J. Dynamic interactions of neutrophils and biofilms. J. Oral. Microbiol., 2014, vol. 17, no. 6:26102. doi: 10.3402/jom.v6.26102
- Horikoshi Y., Matsumoto H., Takatsu Y., Ohtaki T., Kitada C., Usuki S., Fujino M. Dramatic elevation of plasma metastin concentrations in human pregnancy: metastin as a novel placenta-derived hormone in humans. J. Clin. Endocrinol. Metab., 2003, vol. 88, no. 2, pp. 914-919. doi: 10.1210/jc.2002-021235
- Jesaitis A.J., Franklin M.J., Berglund D., Sasaki M., Lord C.I., Bleazard J.B., Duffy J.E., Beyenal H., Lewandowski Z. Compromised host defense on Pseudomonas aeruginosa biofilms: characterization of neutrophil and biofilm interactions. J. Immunol., 2003, vol. 171, no. 8, pp. 4329-4339. doi: 10.4049/jimmunol.171.8.4329
- Kase N.G., Reyniak J.V. Endocrinology of pregnancy. Mt. Sinai J. Med., 1985, vol. 52, no. 1, pp. 11-34.
- Kazemnia A., Ahmadi M., Dilmaghani M. Antibiotic resistance pattern of different Escherichia coli phylogenetic groups isolated from human urinary tract infection and avian colibacillosis. Iran Biomed. J, 2014, vol. 18, no. 4, pp. 219-224. doi: 10.6091/ibj.1394.2014
- Khan M.A., Philip L.M., Cheung G., Vadakepeedika S., Grasemann H., Sweezey N., Palaniyar N. Regulating NETosis: Increasing pH Promotes NADPH Oxidase-Dependent NETosis. Front. Med. (Lausanne), 2018, vol. 5, pp. 19. doi: 10.3389/fmed.2018.00019
- Koca С., §ahin Kavakli H., Alici O. Immunomodulatory role of leptin treatment in experimental sepsis caused by gram negative bacteria. Turk. J. Med. Sci, 2011, vol. 41, no. 2, pp. 251-258. doi: 10.3906/sag-1009-1109
- Lassek C., Burghartz M., Chaves-Moreno D., Otto A., Hentschker C., Fuchs S., Bernhardt J., Jauregui R., Neubauer R., Becher D., Pieper D.H., Jahn M., Jahn D., Riedel K. A metaproteomics approach to elucidate host and pathogen protein expression during catheter-associated urinary tract infections (CAUTIs). Mol. Cell Proteomics, 2015, vol. 14, no. 4, pp. 989-1008. doi: 10.1074/mcp.M114.043463
- Lee J.H., Subhadra B., Son Y.J., Kim D.H., Park H.S., Kim J.M., Koo S.H., Oh M.H., Kim H.J., Choi C.H. Phylogenetic group distributions, virulence factors and antimicrobial resistance properties of uropathogenic Escherichia coli strains isolated from patients with urinary tract infections in South Korea. Lett. Appl. Microbiol., 2016, vol. 62, no. 1, pp. 84-90. doi: 10.1111/lam.12517
- Li B., Zeng M., Zheng H., Huang C., He W., Lu G., Li X., Chen Y., Xie R. Effects of ghrelin on the apoptosis of human neutrophils in vitro. Int. J. Mol. Med., 2016, vol. 38, no. 3, pp. 794-802. doi: 10.3892/ijmm.2016.2668
- Lichtenberger P., Hooton T.M. Antimicrobial prophylaxis in women with recurrent urinary tract infections. Int. J. Antimicrob. Agent, 2011, vol. 38, pp. 36-41. doi: 10.1016/j.ijantimicag.2011.09.005
- Luthje P., Brauner A. Virulence factors of uropathogenic E. coli and their interaction with the host. Adv. Microb. Physiol., 2014, vol. 65,pp. 337-372. doi: 10.1016/bs.ampbs.2014.08.006
- Luthje P., Brauner H., Ramos N.L., Ovregaard A., Glaser R., Hirschberg A.L., Aspenstrom P., Brauner A. Estrogen supports urothelial defense mechanisms. Sci. Transl. Med, 2013, vol. 5, no. 190, pp. 190ra80. doi: 10.1126/scitranslmed.3005574
- Mann R., Mediati D.G., Duggin I.G., Harry E.J., Bottomley A.L. Metabolic adaptations of uropathogenic E. coli in the urinary tract. Front. Cell Infect. Microbiol., 2017, vol. 7, pp. 241. doi: 10.3389/fcimb.2017.00241
- Matuszkiewicz-Rowinska J., MaEyszko J., Wieliczko M. Urinary tract infections in pregnancy: old and new unresolved diagnostic and therapeutic problems. Arch. Med. Sci., 2015, vol. 11, no. 1, pp. 67-77. doi: 10.5114/aoms.2013.39202
- Molero L., Garcia-Duran M., Diaz-Recasens J., Rico L., Casado S., Lopez-Farre A. Expression of estrogen receptor subtypes and neuronal nitric oxide synthase in neutrophils from women and men: regulation by estrogen. Cardiovasc. Res., 2002, vol. 56, no. 1, pp. 43-51.
- Ohtaki T., Shintani Y., Honda S., Matsumoto H., Hori A., Kanehashi K., Terao Y., Kumano S., Takatsu Y., Masuda Y., Ishibashi Y., Watanabe T., Asada M., Yamada T., Suenaga M., Kitada C., Usuki S., Kurokawa T., Onda H., Nishimura O., Fujino M. Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature, 2001, vol. 411, no. 6837, pp. 613-617.
- Oliveira F.A., Paludo K.S., Arend L.N., Farah S.M., Pedrosa F.O., Souza E.M., Surek M., Picheth G., Fadel-Picheth C.M. Virulence characteristics and antimicrobial susceptibility of uropathogenic Escherichia coli strains. Genet. Mol. Res., 2011, vol. 10, no. 4, pp. 4114-4125. doi: 10.4238/2011
- Olson P.D., Hruska K.A., Hunstad D.A. Androgens enhance male urinary tract infection severity in a new model. J. Am. Soc. Nephrol, 2016, vol. 27, no. 6, pp. 1625-1634. doi: 10.1681/ASN.2015030327
- O'Toole G.F., Kaplan H.B., Kolter R. Biofilm formation as microbial development. Ann. Rev. Microbiol., 2000, vol. 54, pp. 49-79. doi: 10.1146/annurev.micro.54.1.49
- Pham C.T., Ivanovich J.L., Raptis S.Z., Zehnbauer B., Ley T.J. Papillon-Lefe'vre syndrome: Correlating the molecular, cellular, and clinical consequences of cathepsin C/dipeptidyl peptidase I deficiency in humans. J. Immunol, 2004, vol. 173, no. 12, pp. 7277-7281. doi: 10.4049/jimmunol.173.12.7277
- Phan Q.T., Sipka T., Gonzalez C., Levraud J.P., Lutfalla G., Nguyen-Chi M. Neutrophils use superoxide to control bacterial infection at a distance. PLoS Pathog, 2018, vol. 14, no. 7: e1007157. doi: 10.1371/journal.ppat.1007157
- Ramos N.L., Sekikubo M., Dzung D.T., Kosnopfel C., Kironde F., Mirembe F., Brauner A. Uropathogenic Escherichia coli isolates from pregnant women in different countries. J. Clin. Microbiol., 2012, vol. 50, no. 11, pp. 3569-3574. doi: 10.1128/JCM.01647-12
- Rosen D.A., Hooton T.M., Stamm W.E., Humphrey P.A., Hultgren S.J. Detection of intracellular bacterial communities in human urinary tract infection. PLoS Med., 2007, vol. 4, no. 12: e329. doi: 10.1371/journal.pmed.0040329
- Schwab S., Jobin K., Kurts C. Urinary tract infection: recent insight into the evolutionary arms race between uropathogenic Escherichia coli and our immune system. Nephrol. Dial. Transplant., 2017, vol. 32, no. 12, pp. 1977-1983. doi: 10.1093/ndt/gfx022
- Schwartz D.J., Kalas V., Pinkner J.S., Chen S.L., Spaulding C.N., Dodson K.W., Hultgren S.J. Positively selected FimH residues enhance virulence during urinary tract infection by altering FimH conformation. Proc. Natl. Acad. Sci. USA, 2013, vol. 110, no. 39, pp. 15530-15537. doi: 10.1073/pnas.1315203110
- Shirai F., Kawaguchi M., Yutsudo M., Dohi Y. Human peripheral blood polymorphonuclear leukocytes at the ovulatory period are in an activated state. Mol. Cell Endocrinol., 2002, vol. 196, no. 1-2, pp. 21-28. doi: 10.1016/S0303-7207(02)00228-9
- Soto S.M., Smithson A., Martinez J.A., Horcajada J.P., Mensa J., Vila J. Biofilm formation in uropathogenic Escherichia coli strains: relationship with prostatitis, urovirulence factors and antimicrobial resistance. J. Urol, 2007, vol. 177, no. 1, pp. 365-368. doi: 10.1016/j.juro.2006.08.081
- Stroh P., Gunther F., Meyle E., Prior B., Wagner C., Hansch G.M. Host defence against Staphylococcus aureus biofilms by polymorphonuclear neutrophils: oxygen radical production but not phagocytosis depends on opsonisation with immunoglobulin G. Immunobiology, 2011, vol. 216, no. 3, pp. 351-357. doi: 10.1016/j.imbio.2010.07.009
- Sun Z., Dragon S., Becker A., Gounni A.S. Leptin inhibits neutrophil apoptosis in children via ERK/NF-KB-dependent pathways. PLoS One, 2013, vol. 8, no. 1: e55249. doi: 10.1371/journal.pone.0055249
- Ujioka T., Matsukawa A., Tanaka N., Matsuura K., Yoshinaga M., Okamura H. Interleukin-8 as an essential factor in the human chorionic gonadotropin-induced rabbit ovulatory process: interleukin-8 induces neutrophil accumulation and activation in ovulation. Biol. Reprod., 1998, vol. 58, no. 2, pp. 526-530.
- Van Gennip M., Christensen L.D., Alhede M., Qvortrup K., Jensen P.0., Heiby N., Givskov M., Bjarnsholt T. Interactions between polymorphonuclear leukocytes and Pseudomonas aeruginosa biofilms on silicone implants in vivo. Infect. Immun., 2012, vol. 80, no. 8, pp. 2601-2607. doi: 10.1128/IAI.06215-11
- Vejborg R.M., Hancock V., Schembri M.A., Klemm P. Comparative genomics of Escherichia coli strains causing urinary tract infections. Appl. Environ. Microbiol, 2011, vol. 77, no. 10, pp. 3268-3278. doi: 10.1128/AEM.02970-10
- Vethanayagam R.R., Almyroudis N.G., Grimm M.J., Lewandowski D.C., Pham C.T., Blackwell T.S., Petraitiene R., Petraitis V., Walsh T.J., Urban C.F., Segal B.H. Role of NADPH oxidase versus neutrophil proteases in antimicrobial host defense. PLoS One, 2011, vol. 6, no. 12: e28149. doi: 10.1371/journal.pone.0028149
- Yang W.L., Ma G., Zhou M., Aziz M., Yen H.T., Mavropoulos S., Ojamaa K., Wang P. Combined administration of human ghrelin and human growth hormone attenuates organ injury and improves survival in aged septic rats. Mol. Med., 2016, vol. 22, pp. 124-135. doi: 10.2119/molmed.2015.00255
- Yu Y., Sikorski P., Bowman-Gholston C., Cacciabeve N., Nelson K.E., Pieper R. Diagnosing inflammation and infection in the urinary system via proteomics. J. Transl. Med., 2015, vol. 13, pp. 111. doi: 10.1186/s12967-015-0475-3