Infection of Bat Epithelial Cells Depends on the Invasion Factors InlA and InlB

Overview

Journal Pathogens

Date 2020 Oct 27

PMID 33105852

Citations 4

Authors

Olga Povolyaeva

Yaroslava Chalenko

Egor Kalinin

Olga Kolbasova

Elena Pivova

Denis Kolbasov

Sergey Yurkov

Svetlana Ermolaeva

Affiliations

Soon will be listed here.

Abstract

is a widespread facultative intracellular pathogen. The range of natural hosts that supporting persistence in the environment has not been fully established yet. In this study, we were interested in the potential of to infect cells of bats, which are being increasingly recognized as a reservoir for microorganisms that are pathogenic to humans and domestic animals. A stable epithelial cell line was developed from the kidneys of , a small bat widely distributed across Europe. The wild-type strain EGDe infected this cell line with an invasion efficiency of 0.0078 ± 0.0009%. Once it entered bat cells, doubled within about 70 minutes. When lacked either of the major invasion factors, InlA and InlB, invasion efficiency decreased by a factor of 10 and 25 respectively ( < 0.000001). The obtained results suggest that bat epithelial cells are susceptible to infection and that invasion of bat cells depends on the major invasion factors InlA and InlB. These results constitute the first report on in vitro studies of infection in bats.

Citing Articles

Molecular Survey of Protist Enteroparasites in Bats (Order Chiroptera) from Portugal.

Lopez-Lopez P, Cruz A, Santos-Silva S, Rivero-Juarez A, Rebelo H, Mesquita J Acta Parasitol. 2025; 70(1):24.

PMID: 39853462 DOI: 10.1007/s11686-024-00985-x.

Natural Isoforms of Virulence Factor Inlb Differ in c-Met Binding Efficiency and Differently Affect Uptake and Survival Listeria in Macrophage.

Chalenko Y, Slonova D, Kechko O, Kalinin E, Mitkevich V, Ermolaeva S Int J Mol Sci. 2023; 24(8).

PMID: 37108418 PMC: 10139187. DOI: 10.3390/ijms24087256.

An overview of bats microbiota and its implication in transmissible diseases.

Federici L, Masulli M, De Laurenzi V, Allocati N Front Microbiol. 2022; 13:1012189.

PMID: 36338090 PMC: 9631491. DOI: 10.3389/fmicb.2022.1012189.

Comparison of Selected Phenotypic Features of Persistent and Sporadic Strains of Sampled from Fish Processing Plants.

Wiktorczyk-Kapischke N, Walecka-Zacharska E, Skowron K, Kijewska A, Bernaciak Z, Bauza-Kaszewska J Foods. 2022; 11(10).

PMID: 35627065 PMC: 9140201. DOI: 10.3390/foods11101492.

Invasion Into Sheep Kidney Epithelial Cells Depends on InlB, and Invasion Efficiency Is Modulated by Phylogenetically Defined InlB Isoforms.

Chalenko Y, Kolbasova O, Pivova E, Abdulkadieva M, Povolyaeva O, Kalinin E Front Microbiol. 2022; 13:825076.

PMID: 35197955 PMC: 8859113. DOI: 10.3389/fmicb.2022.825076.

References

Portnoy D, Jacks P, Hinrichs D . Role of hemolysin for the intracellular growth of Listeria monocytogenes. J Exp Med. 1988; 167(4):1459-71. PMC: 2188911. DOI: 10.1084/jem.167.4.1459. View

Schipper J, Chanson J, Chiozza F, Cox N, Hoffmann M, Katariya V . The status of the world's land and marine mammals: diversity, threat, and knowledge. Science. 2008; 322(5899):225-30. DOI: 10.1126/science.1165115. View

Calisher C, Childs J, Field H, Holmes K, Schountz T . Bats: important reservoir hosts of emerging viruses. Clin Microbiol Rev. 2006; 19(3):531-45. PMC: 1539106. DOI: 10.1128/CMR.00017-06. View

Regan E, Harrison G, Butler S, McLAUCHLIN J, Thomas M, Mitchell S . Primary cutaneous listeriosis in a veterinarian. Vet Rec. 2005; 157(7):207. DOI: 10.1136/vr.157.7.207. View

Camejo A, Carvalho F, Reis O, Leitao E, Sousa S, Cabanes D . The arsenal of virulence factors deployed by Listeria monocytogenes to promote its cell infection cycle. Virulence. 2011; 2(5):379-94. DOI: 10.4161/viru.2.5.17703. View

Brook C, Dobson A . Bats as 'special' reservoirs for emerging zoonotic pathogens. Trends Microbiol. 2015; 23(3):172-80. PMC: 7126622. DOI: 10.1016/j.tim.2014.12.004. View

OSullivan D, Klaenhammer T . High- and low-copy-number Lactococcus shuttle cloning vectors with features for clone screening. Gene. 1993; 137(2):227-31. DOI: 10.1016/0378-1119(93)90011-q. View

Ortega F, Koslover E, Theriot J . cell-to-cell spread in epithelia is heterogeneous and dominated by rare pioneer bacteria. Elife. 2019; 8. PMC: 6363384. DOI: 10.7554/eLife.40032. View

Nakamura S, Settai S, Hayashidani H, Urabe T, Namai S, Une Y . Outbreak of yersiniosis in Egyptian rousette bats (Rousettus aegyptiacus) caused by Yersinia pseudotuberculosis serotype 4b. J Comp Pathol. 2012; 148(4):410-3. DOI: 10.1016/j.jcpa.2012.07.007. View

10.

Lecuit M, Ohayon H, Braun L, Mengaud J, Cossart P . Internalin of Listeria monocytogenes with an intact leucine-rich repeat region is sufficient to promote internalization. Infect Immun. 1997; 65(12):5309-19. PMC: 175764. DOI: 10.1128/iai.65.12.5309-5319.1997. View

11.

Lingnau A, Domann E, Hudel M, Bock M, Nichterlein T, Wehland J . Expression of the Listeria monocytogenes EGD inlA and inlB genes, whose products mediate bacterial entry into tissue culture cell lines, by PrfA-dependent and -independent mechanisms. Infect Immun. 1995; 63(10):3896-903. PMC: 173548. DOI: 10.1128/iai.63.10.3896-3903.1995. View

12.

Zaytseva E, Ermolaeva S, Somov G . Low genetic diversity and epidemiological significance of Listeria monocytogenes isolated from wild animals in the far east of Russia. Infect Genet Evol. 2007; 7(6):736-42. DOI: 10.1016/j.meegid.2007.07.006. View

13.

Banerjee M, Copp J, Vuga D, Marino M, Chapman T, van der Geer P . GW domains of the Listeria monocytogenes invasion protein InlB are required for potentiation of Met activation. Mol Microbiol. 2004; 52(1):257-71. DOI: 10.1111/j.1365-2958.2003.03968.x. View

14.

Mounier J, RYTER A, Sansonetti P . Intracellular and cell-to-cell spread of Listeria monocytogenes involves interaction with F-actin in the enterocytelike cell line Caco-2. Infect Immun. 1990; 58(4):1048-58. PMC: 258581. DOI: 10.1128/iai.58.4.1048-1058.1990. View

15.

Weis J, SEELIGER H . Incidence of Listeria monocytogenes in nature. Appl Microbiol. 1975; 30(1):29-32. PMC: 187108. DOI: 10.1128/am.30.1.29-32.1975. View

16.

Hayashidani H, Kanzaki N, Kaneko Y, Okatani A, Taniguchi T, Kaneko K . Occurrence of yersiniosis and listeriosis in wild boars in Japan. J Wildl Dis. 2002; 38(1):202-5. DOI: 10.7589/0090-3558-38.1.202. View

17.

Lecuit M, Vandormael-Pournin S, Lefort J, Huerre M, Gounon P, Dupuy C . A transgenic model for listeriosis: role of internalin in crossing the intestinal barrier. Science. 2001; 292(5522):1722-5. DOI: 10.1126/science.1059852. View

18.

Parida S, Domann E, Rohde M, Muller S, Darji A, Hain T . Internalin B is essential for adhesion and mediates the invasion of Listeria monocytogenes into human endothelial cells. Mol Microbiol. 1998; 28(1):81-93. DOI: 10.1046/j.1365-2958.1998.00776.x. View

19.

Khelef N, Lecuit M, Bierne H, Cossart P . Species specificity of the Listeria monocytogenes InlB protein. Cell Microbiol. 2006; 8(3):457-70. DOI: 10.1111/j.1462-5822.2005.00634.x. View

20.

Marona P, Gorka J, Kotlinowski J, Majka M, Jura J, Miekus K . C-Met as a Key Factor Responsible for Sustaining Undifferentiated Phenotype and Therapy Resistance in Renal Carcinomas. Cells. 2019; 8(3). PMC: 6468372. DOI: 10.3390/cells8030272. View