Borrelia burgdorferi strain and host sex influence pathogen prevalence and abundance in the tissues of a laboratory rodent host
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
R01 AI097137
NIAID NIH HHS - United States
R01 AI142572
NIAID NIH HHS - United States
R01 AI181007
NIAID NIH HHS - United States
PubMed
36112076
PubMed Central
PMC12359074
DOI
10.1111/mec.16694
Knihovny.cz E-zdroje
- Klíčová slova
- Borrelia burgdorferi, Lyme borreliosis, pathogen abundance, pathogen life history, tick-borne disease,
- MeSH
- Borrelia burgdorferi komplex * MeSH
- Borrelia burgdorferi * genetika MeSH
- hlodavci MeSH
- klíšťata * MeSH
- klíště * MeSH
- lymeská nemoc * epidemiologie veterinární MeSH
- myši inbrední C3H MeSH
- myši MeSH
- prevalence MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- myši MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Experimental infections with different pathogen strains give insight into pathogen life history traits. The purpose of the present study was to compare variation in tissue infection prevalence and spirochete abundance among strains of Borrelia burgdorferi in a rodent host (Mus musculus, C3H/HeJ). Male and female mice were experimentally infected via tick bite with one of 12 strains. Ear tissue biopsies were taken at days 29, 59 and 89 postinfection, and seven tissues were collected at necropsy. The presence and abundance of spirochetes in the mouse tissues were measured by quantitative polymerase chain reaction. To determine the frequencies of our strains in nature, their multilocus sequence types were matched to published data sets. For the infected mice, 56.6% of the tissues were infected with B. burgdorferi. The mean spirochete load in the mouse necropsy tissues varied 4.8-fold between the strains. The mean spirochete load in the ear tissue biopsies decreased rapidly over time for some strains. The percentage of infected tissues in male mice (65.4%) was significantly higher compared to female mice (50.5%). The mean spirochete load in the seven tissues was 1.5× higher in male mice compared to female mice; this male bias was 15.3× higher in the ventral skin. Across the 11 strains, the mean spirochete loads in the infected mouse tissues were positively correlated with the strain-specific frequencies in their tick vector populations. The study suggests that laboratory-based estimates of pathogen abundance in host tissues can predict the strain composition of this important tick-borne pathogen in nature.
Biology Centre Institute of Parasitology Czech Academy of Sciences České Budějovice Czechia
Department of Biology University of Pennsylvania Philadelphia Pennsylvania USA
Faculty of Science University of South Bohemia České Budějovice Czechia
Zobrazit více v PubMed
Acevedo MA, Dillemuth FP, Flick AJ, Faldyn MJ, & Elderd BD (2019). Virulence-driven trade-offs in disease transmission: A meta-analysis. Evolution, 73(4), 636–647. 10.1111/evo.13692 PubMed DOI
Anderson RM, & May RM (1982). Coevolution of hosts and parasites. Parasitology, 16. PubMed
Arroyo-Mendoza M, Peraza K, Olson J, Adler-Moore JP, & Buckley NE (2020). Effect of testosterone and estrogen supplementation on the resistance to systemic Candida albicans infection in mice. Heliyon, 6(7), e04437. 10.1016/j.heliyon.2020.e04437 PubMed DOI PMC
Balmer O, & Tanner M (2011). Prevalence and implications of multiple-strain infections. The Lancet Infectious Diseases, 11(11), 868–878. 10.1016/S1473-3099(11)70241-9 PubMed DOI
Barthold SW, Beck DS, Hansen GM, Terwilliger GA, & Moody KD (1990). Lyme borreliosis in selected strains and ages of laboratory mice. The Journal of Infectious Diseases, 162(1), 133–138. 10.1093/infdis/162.1.133 PubMed DOI
Baum E, Hue F, & Barbour AG (2012). Experimental infections of the reservoir species PubMed DOI PMC
Belli A, Sarr A, Rais O, Rego ROM, & Voordouw MJ (2017). Ticks infected via co-feeding transmission can transmit Lyme borreliosis to vertebrate hosts. Scientific Reports, 7(1), 5006. 10.1038/s41598-017-05231-1 PubMed DOI PMC
Benoit VM, Petrich A, Alugupalli KR, Marty-Roix R, Moter A, Leong JM, & Boyartchuk VL (2010). Genetic control of the innate immune response to PubMed DOI PMC
Benten WPM, Ulrich P, Kühn-Velten WN, Vohr H-W, & Wunderlich F (1997). Testosterone-induced susceptibility to Plasmodium chabaudi malaria: Persistence after withdrawal of testosterone. Journal of Endocrinology, 153(2), 275–281. 10.1677/joe.0.1530275 PubMed DOI
Cobey S. (2014). Pathogen evolution and the immunological niche. Annals of the New York Academy of Sciences, 1320(1), 1–15. 10.1111/nyas.12493 PubMed DOI PMC
Courtney JW, Kostelnik LM, Zeidner NS, & Massung RF (2004). Multiplex real-time PCR for detection of PubMed DOI PMC
Dai J, Wang P, Adusumilli S, Booth CJ, Narasimhan S, Anguita J, & Fikrig E (2009). Antibodies against a tick protein, Salp15, protect mice from the Lyme disease agent. Cell Host and Microbe, 6(5), 482–492. 10.1016/j.chom.2009.10.006 PubMed DOI PMC
De Roode JC, Yates AJ, & Altizer S (2008). Virulence-transmission trade-offs and population divergence in virulence in a naturally occurring butterfly parasite. Proceedings of the National Academy of Sciences of the United States of America, 105(21), 7489–7494. 10.1073/pnas.0710909105 PubMed DOI PMC
Derdáková M, Dudiò V, Brei B, Brownstein JS, Schwartz I, & Fish D (2004). Interaction and transmission of two PubMed DOI PMC
Devevey G, & Brisson D (2012). The effect of spatial heterogenity on the aggregation of ticks on white-footed mice. Parasitology, 139(7), 915–925. 10.1017/S003118201200008X PubMed DOI PMC
Dolan MC, Piesman J, Schneider BS, Schriefer M, Brandt K, & Zeidner NS (2004). Comparison of disseminated and nondisseminated strains of PubMed DOI PMC
Durand J, Jacquet M, Rais O, Gern L, & Voordouw MJ (2017). Fitness estimates from experimental infections predict the long-term strain structure of a vector-borne pathogen in the field. Scientific Reports, 7(1). 10.1038/s41598-017-01821-1 PubMed DOI PMC
Dykhuizen DE, Sandigursky S, Nadelman RB, Nowakowski J, Brisson D, Wormser GP, & Schwartz I (2008). The propensity of different PubMed DOI PMC
Earnhart CG, Buckles EL, Dumler JS, & Marconi RT (2005). Demonstration of PubMed DOI PMC
Ehrlich GD, Hu FZ, Shen K, Stoodley P, & Post JC (2005). Bacterial plurality as a general mechanism driving persistence in chronic infections. Clinical Orthopaedics and Related Research, 437, 20–24. PubMed PMC
Embers ME, Ramamoorthy R, & Philipp MT (2004). Survival strategies of PubMed DOI
Forbes ML, Horsey E, Hiller NL, Buchinsky FJ, Hayes JD, Compliment JM, Hillman T, Ezzo S, Shen K, Keefe R, Barbadora K, Post JC, Hu FZ, & Ehrlich GD (2008). Strain-specific virulence phenotypes of PubMed DOI PMC
Genné D, Rossel M, Sarr A, Battilotti F, Rais O, Rego ROM, & Voordouw MJ (2021). Competition between strains of PubMed DOI PMC
Genné D, Sarr A, Gomez-Chamorro A, Durand J, Cayol C, Rais O, & Voordouw MJ (2018). Competition between strains of PubMed DOI PMC
Genné D, Sarr A, Rais O, & Voordouw MJ (2019). Competition between strains of PubMed DOI PMC
Gern L, Schaible UE, & Simon MM (1993). Mode of inoculation of the Lyme disease agent PubMed DOI
Golde WT, Gollobin P, & Rodriguez LL (2005). A rapid, simple, and humane method for submandibular bleeding of mice using a lancet. Lab Animal, 34(9), 39–43. 10.1038/laban1005-39 PubMed DOI
Hanincová K, Ogden NH, Diuk-Wasser M, Pappas CJ, Iyer R, Fish D, Schwartz I, & Kurtenbach K (2008). Fitness variation of PubMed DOI PMC
Haven J, Magori K, & Park AW (2012). Ecological and inhost factors promoting distinct parasite life-history strategies in Lyme borreliosis. Epidemics, 4(3), 152–157. 10.1016/j.epidem.2012.07.001 PubMed DOI
Horká H, Cerná-Kýcková K, Skallová A, & Kopecký J (2009). Tick saliva affects both proliferation and distribution of PubMed DOI
Hovius JWR, van Dam AP, & Fikrig E (2007). Tick-host-pathogen interactions in Lyme borreliosis. Trends in Parasitology, 23(9), 434–438. 10.1016/j.pt.2007.07.001 PubMed DOI
Hughes VL, & Randolph SE (2001). Testosterone increases the transmission potential of tick-borne parasites. Parasitology, 123(4), 365–371. 10.1017/S0031182001008599 PubMed DOI
Hyde JA (2017). PubMed DOI PMC
Jacquet M, Durand J, Rais O, & Voordouw MJ (2015). Cross-reactive acquired immunity influences transmission success of the Lyme disease pathogen, PubMed DOI
Jacquet M, Margos G, Fingerle V, & Voordouw MJ (2016). Comparison of the lifetime host-to-tick transmission between two strains of the Lyme disease pathogen PubMed DOI PMC
Kazimírová M, & Štibrániová I (2013). Tick salivary compounds: Their role in modulation of host defences and pathogen transmission. Frontiers in Cellular and Infection Microbiology, 3, 43. 10.3389/fcimb.2013.00043 PubMed DOI PMC
Klein SL (2004). Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunology, 26(6–7), 247–264. 10.1111/j.0141-9838.2004.00710.x PubMed DOI
Klein SL, & Flanagan KL (2016). Sex differences in immune responses. Nature Reviews Immunology, 16(10), 626–638. 10.1038/nri.2016.90 PubMed DOI
Kurtenbach K, Hanincová K, Tsao JI, Margos G, Fish D, & Ogden NH (2006). Fundamental processes in the evolutionary ecology of Lyme borreliosis. Nature Reviews Microbiology, 4(9), 660–669. 10.1038/nrmicro1475 PubMed DOI
Liang FT, Yan J, Mbow ML, Sviat SL, Gilmore RD, Mamula M, & Fikrig E (2004). PubMed DOI PMC
Lin YP, Tan X, Caine JA, Castellanos M, Chaconas G, Coburn J, & Leong JM (2020). Strain-specific joint invasion and colonization by Lyme disease spirochetes is promoted by outer surface protein C. PLoS Pathogens, 16(5), 1–29. 10.1371/journal.ppat.1008516 PubMed DOI PMC
Machácková M, Oborník M, & Kopecký J (2006). Effect of salivary gland extract from PubMed
Margos G, Tsao JI, Castillo-Ramírez S, Girard YA, Hamer SA, Hoen AG, Lane RS, Raper SL, & Ogden NH (2012). Two boundaries separate PubMed DOI PMC
Margos G, Vollmer SA, Ogden NH, & Fish D (2011). Population genetics, taxonomy, phylogeny and evolution of PubMed DOI PMC
Massad E. (1987). Transmission rates and the evolution of pathogenicity. Evolution, 41(5), 1127–1130. 10.2307/2409198 PubMed DOI
Ogden NH, Feil EJ, Leighton PA, Lindsay LR, Margos G, Mechai S, Michel P, & Moriarty TJ (2015). Evolutionary aspects of emerging Lyme disease in Canada. Applied and Environmental Microbiology, 81(21), 7350–7359. 10.1128/AEM.01671-15 PubMed DOI PMC
Ogden NH, Margos G, Aanensen DM, Drebot MA, Feil EJ, Hanincová K, Schwartz I, Tyler S, & Lindsay LR (2011). Investigation of genotypes of PubMed DOI PMC
Pechová J, Stĕpánová G, Kovár L, & Kopecký J (2002). Tick salivary gland extract-activated transmission of PubMed
Perkins SE, Cattadori IM, Tagliapietra V, Rizzoli AP, & Hudson PJ (2003). Empirical evidence for key hosts in persistence of a tick-borne disease. International Journal for Parasitology, 33(9), 909–917. 10.1016/s0020-7519(03)00128-0 PubMed DOI
Piesman J, & Gern L (2004). Lyme borreliosis in Europe and North America. Parasitology, 129(S1), S191–S220. 10.1017/s0031182003004694 PubMed DOI
R Core Team. (2021). R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/
Råberg L. (2012). Infection intensity and infectivity of the tick-borne pathogen PubMed DOI
Råberg L, Hagström, Andersson M, Bartkova S, Scherman K, Strandh M, & Tschirren B (2017). Evolution of antigenic diversity in the tick-transmitted bacterium PubMed DOI
Roehrig JT, Piesman J, Hunt AR, Keen MG, Happ CM, & Johnson BJB (1992). The hamster immune response to tick-transmitted PubMed
Rudolf I, Sikutová S, Kopecký J, & Hubálek Z (2010). Salivary gland extract from engorged PubMed DOI
Rynkiewicz EC, Brown J, Tufts DM, Huang C-I, Kampen H, Bent SJ, Fish D, & Diuk-Wasser MA (2017). Closely-related PubMed DOI PMC
Sasaki M, Fujii Y, Iwamoto M, & Ikadai H (2013). Effect of Sex Steroids on Babesia microti Infection in Mice. The American Journal of Tropical Medicine and Hygiene, 88(2), 367–375. 10.4269/ajtmh.2012.12-0338 PubMed DOI PMC
Schmid-Hempel P. (2021). Evolutionary parasitology: The integrated study of infections, immunology, ecology, and genetics (2nd ed.). Oxford University Press. 10.1093/oso/9780198832140.001.0001 DOI
Seinost G, Dykhuizen DE, Dattwyler RJ, Golde WT, Dunn JJ, Wang IN, Wormser GP, Schriefer ME, & Luft BJ (1999). Four clones of PubMed DOI PMC
Sertour N, Cotté V, Garnier M, Malandrin L, Ferquel E, & Choumet V (2018). Infection kinetics and tropism of PubMed DOI PMC
Shih C-M, Pollack RJ, Telford SR, & Spielman A (1992). Delayed dissemination of Lyme disease spirochetes from the site of deposition in the skin of mice. Journal of Infectious Diseases, 166(4), 827–831. 10.1093/infdis/166.4.827 PubMed DOI
Šimo L, Kazimirova M, Richardson J, & Bonnet SI (2017). The essential role of tick salivary glands and saliva in tick feeding and pathogen transmission. Frontiers in Cellular and Infection Microbiology, 7, 281. 10.3389/fcimb.2017.00281 PubMed DOI PMC
Stanek G, & Reiter M (2011). The expanding Lyme PubMed DOI
Steere AC, Strle F, Wormser GP, Hu LT, Branda JA, Hovius JWR, Li X, & Mead PS (2016). Lyme borreliosis. Nature Reviews Disease Primers, 2(1), 1–19. 10.1038/nrdp.2016.90 PubMed DOI PMC
Tonetti N, Voordouw MJ, Durand J, Monnier S, & Gern L (2015). Genetic variation in transmission success of the Lyme borreliosis pathogen PubMed DOI
Trigunaite A, Dimo J, & Jørgensen TN (2015). Suppressive effects of androgens on the immune system. Cellular Immunology, 294(2), 87–94. 10.1016/j.cellimm.2015.02.004 PubMed DOI
Tschirren B, Andersson M, Scherman K, Westerdahl H, Mittl PRE, & Råberg L (2013). Polymorphisms at the innate immune receptor PubMed DOI PMC
Tyler S, Tyson S, Dibernardo A, Drebot M, Feil EJ, Graham M, Knox NC, Lindsay LR, Margos G, Mechai S, Van Domselaar G, Thorpe HA, & Ogden NH (2018). Whole genome sequencing and phylogenetic analysis of strains of the agent of Lyme disease PubMed DOI PMC
Voordouw MJ, Lachish S, & Dolan MC (2015). The Lyme disease pathogen has no effect on the survival of its rodent reservoir host. PLOS ONE, 10(2), e0118265. 10.1371/journal.pone.0118265 PubMed DOI PMC
Wang G, Ojaimi C, Wu H, Saksenberg V, Iyer R, Liveris D, McClain SA, Wormser GP, & Schwartz I (2002). Disease severity in a murine model of Lyme borreliosis is associated with the genotype of the infecting PubMed DOI PMC
Wang G, Ojaimi C, Wu H, Saksenberg V, Iyer R, McClain SA, Wormser GP, & Schwartz I (2001). Impact of genotypic variation of DOI
Wang IN, Dykhuizen DE, Qiu W, Dunn JJ, Bosler EM, & Luft BJ (1999). Genetic diversity of PubMed DOI PMC
Wooten RM, & Weis JJ (2001). Host-pathogen interactions promoting inflammatory Lyme arthritis: Use of mouse models for dissection of disease processes. Current Opinion in Microbiology, 4(3), 274–279. 10.1016/S1369-5274(00)00202-2 PubMed DOI
Yang L, Weis JH, Eichwald E, Kolbert CP, Persing DH, & Weis JJ (1994). Heritable susceptibility to severe PubMed DOI PMC
Zawada SG, von Fricken ME, Weppelmann TA, Sikaroodi M, & Gillevet PM (2020). Optimization of tissue sampling for PubMed DOI PMC
Zeidner NS, Schneider BS, Nuncio MS, Gern L, & Piesman J (2002). Coinoculation of PubMed DOI
Zhong X, Nouri M, & Råberg L (2019). Colonization and pathology of PubMed DOI