FREE SHIPPING over $40
OVER 10000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Frontiers in cellular and infection microbiology2022; 12; 932137; doi: 10.3389/fcimb.2022.932137

Host and Species-Specificities of Pattern Recognition Receptors Upon Infection With Leptospira interrogans.

Abstract: Leptospirosis is a zoonotic infectious disease affecting all vertebrates. It is caused by species of the genus Leptospira, among which are the highly pathogenic L. interrogans. Different mammals can be either resistant or susceptible to the disease which can present a large variety of symptoms. Humans are mostly asymptomatic after infection but can have in some cases symptoms varying from a flu-like syndrome to more severe forms such as Weil's disease, potentially leading to multiorgan failure and death. Similarly, cattle, pigs, and horses can suffer from acute forms of the disease, including morbidity, abortion, and uveitis. On the other hand, mice and rats are resistant to leptospirosis despite chronical colonization of the kidneys, excreting leptospires in urine and contributing to the transmission of the bacteria. To this date, the immune mechanisms that determine the severity of the infection and that confer susceptibility to leptospirosis remain enigmatic. To our interest, differential immune sensing of leptospires through the activation of or escape from pattern recognition receptors (PRRs) by microbe-associated molecular patterns (MAMPs) has recently been described. In this review, we will summarize these findings that suggest that in various hosts, leptospires differentially escape recognition by some Toll-like and NOD-like receptors, including TLR4, TLR5, and NOD1, although TLR2 and NLRP3 responses are conserved independently of the host. Overall, we hypothesize that these innate immune mechanisms could play a role in determining host susceptibility to leptospirosis and suggest a central, yet complex, role for TLR4.
Copyright © 2022 Bonhomme and Werts.
Get Full Text
Publication Date: 2022-07-22 PubMed ID: 35937697PubMed Central: PMC9353586DOI: 10.3389/fcimb.2022.932137Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article
  • Review
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research investigates the role of innate immune mechanisms in differentiating host susceptibility to Leptospirosis, including the interactions between Leptospira interrogans and pattern recognition receptors (PRRs). It suggests a potentially key role for Toll-like receptor 4 (TLR4) in this process.

Introduction to Leptospirosis

  • Leptospirosis is a zoonotic disease affecting all vertebrates, caused by species of the genus Leptospira, particular the pathogenic strain Leptospira interrogans.
  • Various mammals exhibit different levels of resistance or susceptibility to Leptospirosis, with a range of symptoms from asymptomatic infections to severe conditions like Weil’s disease, which can lead to multiorgan failure and death. Particularly, humans are mostly asymptomatic but in some cases may exhibit symptoms similar to a flu-like syndrome.
  • The immune mechanisms that determine the infection severity and susceptibility to leptospirosis are currently not well understood.

Differential Immune Responses to Leptospirosis

  • Mice and rats have been noted to exhibit resistance to the disease, despite chronic colonization of their kidneys and excretion of leptospires, the bacteria that causes the disease, in their urine. This contributes to the transmission of the bacteria.
  • Livestock animals like cattle, pigs, and horses can suffer from acute forms of Leptospirosis, including symptoms such as morbidity, abortion, and uveitis.
  • Recent studies have highlighted the differential immune sensing of the bacteria through the activation or avoidance of pattern recognition receptors (PRRs) by microbe-associated molecular patterns (MAMPs).

Role of Specific Toll-Like and NOD-Like Receptors

  • Current findings suggest that, within a variety of hosts, leptospires may escape recognition by certain Toll-like and NOD-like receptors, including TLR4, TLR5, and NOD1.
  • However, response to TLR2 and NLRP3 seem to be conserved regardless of the host. This suggests that these two receptors play a role in the innate immune response to leptospirosis.
  • The research highlights a potentially central role for TLR4 in determining susceptibility to Leptospirosis, but acknowledges that this is a complex interaction and requires further examination.

Cite This Article

APA
Bonhomme D, Werts C. (2022). Host and Species-Specificities of Pattern Recognition Receptors Upon Infection With Leptospira interrogans. Front Cell Infect Microbiol, 12, 932137. https://doi.org/10.3389/fcimb.2022.932137

Publication

Frontiers in cellular and infection microbiology
ISSN: 2235-2988
NlmUniqueID: 101585359
Country: Switzerland
Language: English
Volume: 12
Pages: 932137

Researcher Affiliations

Bonhomme, Delphine
  • Institut Pasteur, Université de Paris, CNRS UMR2001, INSERM U1306, Unité de Biologie et Génétique de la Paroi Bactérienne, Paris, France.
Werts, Catherine
  • Institut Pasteur, Université de Paris, CNRS UMR2001, INSERM U1306, Unité de Biologie et Génétique de la Paroi Bactérienne, Paris, France.

MeSH Terms

  • Animals
  • Cattle
  • Horses
  • Humans
  • Leptospira
  • Leptospira interrogans
  • Leptospirosis / microbiology
  • Mammals
  • Mice
  • Mice, Inbred C57BL
  • Rats
  • Receptors, Pattern Recognition
  • Swine
  • Toll-Like Receptor 4

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

This article includes 142 references
  1. Ackermann K, Kenngott R, Settles M, Gerhards H, Maierl J, Wollanke B. In Vivo Biofilm Formation of Pathogenic Leptospira Spp. In the Vitreous Humor of Horses With Recurrent Uveitis. Microorganisms 9, 1915 (2021).
    doi: 10.3390/microorganisms9091915pmc: PMC8464839pubmed: 34576809google scholar: lookup
  2. Adler B. Leptospira and Leptospirosis. Berlin, Heidelberg: Springer Berlin Heidelberg (2015).
    doi: 10.1007/978-3-662-45059-8google scholar: lookup
  3. Akino Mercy C S, Natarajaseenivasan K. Htlr2 Interacting Peptides of Pathogenic Leptospiral Outer Membrane Proteins. Microbial Pathogenesis 155 (2021), 104895.
    doi: 10.1016/j.micpath.2021.104895pubmed: 33878396google scholar: lookup
  4. Andersen-Nissen E, Smith K D, Bonneau R, Strong R K, Aderem A. A Conserved Surface on Toll-Like Receptor 5 Recognizes Bacterial Flagellin. A RT I C L E 204 (2007), 11.
    doi: 10.1084/jem.20061400pmc: PMC2118731pubmed: 17283206google scholar: lookup
  5. Anwar M A, Panneerselvam S, Shah M, Choi S. Insights Into the Species-Specific TLR4 Signaling Mechanism in Response to Rhodobacter Sphaeroides Lipid A Detection. Sci. Rep. 5 (2015), 7657.
    doi: 10.1038/srep07657pmc: PMC4288214pubmed: 25563849google scholar: lookup
  6. Bauernfeind F G, Horvath G, Stutz A, Alnemri E S, MacDonald K, Speert D. Cutting Edge: NF-κb Activating Pattern Recognition and Cytokine Receptors License NLRP3 Inflammasome Activation by Regulating NLRP3 Expression. J. Immunol. 183 (2009), 787–791.
    doi: 10.4049/jimmunol.0901363pmc: PMC2824855pubmed: 19570822google scholar: lookup
  7. Belperron A A, Bockenstedt L K. Natural Antibody Affects Survival of the Spirochete Borrelia Burgdorferi Within Feeding Ticks. Infect. Immun. 69 (2001), 6456–6462.
    doi: 10.1128/IAI.69.10.6456-6462.2001pmc: PMC98781pubmed: 11553590google scholar: lookup
  8. Bens M, Vimont S, Ben Mkaddem S, Chassin C, Goujon J-M, Balloy V. Flagellin/TLR5 Signalling Activates Renal Collecting Duct Cells and Facilitates Invasion and Cellular Translocation of Uropathogenic E Scherichia Coli: TLR5 Signalling in Renal Collecting Duct Cells. Cell Microbiol. 16 (2014), 1503–1517.
    doi: 10.1111/cmi.12306pubmed: 24779433google scholar: lookup
  9. Bertin J, Nir W-J, Fischer C M, Tayber O V, Errada P R, Grant J R. Human CARD4 Protein Is a Novel CED-4/Apaf-1 Cell Death Family Member That Activates NF-κb. J. Biol. Chem. 274 (1999), 12955–12958.
    doi: 10.1074/jbc.274.19.12955pubmed: 10224040google scholar: lookup
  10. Bonhomme D, Santecchia I, Vernel-Pauillac F, Caroff M, Germon P, Murray G. Leptospiral LPS Escapes Mouse TLR4 Internalization and TRIF−associated Antimicrobial Responses Through O Antigen and Associated Lipoproteins. PloS Pathogens 16 (2020), e1008639.
    doi: 10.1371/journal.ppat.1008639pmc: PMC7757799pubmed: 33362240google scholar: lookup
  11. Bonhomme D, Werts C. Purification of LPS From Leptospira. In Leptospira Spp, pp. 53–65, New York, NY: Springer US (2020).
    doi: 10.1007/978-1-0716-0459-5_6pubmed: 32632859google scholar: lookup
  12. Botos I, Segal D M, Davies D R. The Structural Biology of Toll-Like Receptors. Structure 19 (2011), 447–459.
    doi: 10.1016/j.str.2011.02.004pmc: PMC3075535pubmed: 21481769google scholar: lookup
  13. Brough D, Le Feuvre R A, Wheeler R D, Solovyova N, Hilfiker S, Rothwell N J. Ca 2+ Stores and Ca 2+ Entry Differentially Contribute to the Release of IL-1β and IL-1α From Murine Macrophages. J. Immunol. 170 (2003), 3029–3036.
    doi: 10.4049/jimmunol.170.6.3029pubmed: 12626557google scholar: lookup
  14. Cameron C E. Leptospiral Structure, Physiology, and Metabolism. In Leptospira and Leptospirosis, pp. 21–41, Berlin, Heidelberg: Springer Berlin Heidelberg (2015).
    doi: 10.1007/978-3-662-45059-8_3google scholar: lookup
  15. Carneiro L A M, Travassos L H, Girardin S E. Nod-Like Receptors in Innate Immunity and Inflammatory Diseases. Ann. Med. 39 (2007), 581–593.
    doi: 10.1080/07853890701576172pubmed: 18038361google scholar: lookup
  16. Charon N W, Lawrence C W, O’Brien S. Movement of Antibody-Coated Latex Beads Attached to the Spirochete Leptospira Interrogans. Proc. Natl. Acad. Sci. U.S.A. 78 (1981), 7166–7170.
    doi: 10.1073/pnas.78.11.7166pmc: PMC349217pubmed: 6947280google scholar: lookup
  17. Chassin C, Picardeau M, Goujon J-M, Bourhy P, Quellard N, Darche S. TLR4- and TLR2-Mediated B Cell Responses Control the Clearance of the Bacterial Pathogen, Leptospira Interrogans. J. Immunol. 183 (2009), 2669–2677.
    doi: 10.4049/jimmunol.0900506pubmed: 19635914google scholar: lookup
  18. Chen C, Zibiao H, Ming Z, Shiyi C, Ruixia L, Jie W. Expression Pattern of Toll-Like Receptors (TLRs) in Different Organs and Effects of Lipopolysaccharide on the Expression of TLR 2 and 4 in Reproductive Organs of Female Rabbit. Dev. Comp. Immunol. 46 (2014), 341–348.
    doi: 10.1016/j.dci.2014.05.008pubmed: 24858029google scholar: lookup
  19. Cinco M, Banfi E, Panfili E. Heterogeneity of Lipopolysaccharide Banding Patterns in Leptospira Spp. Microbiol. 132 (1986), 1135–1138.
    doi: 10.1099/00221287-132-4-1135pubmed: 3760822google scholar: lookup
  20. Costa F, Hagan J E, Calcagno J, Kane M, Torgerson P, Martinez-Silveira M S. Global Morbidity and Mortality of Leptospirosis: A Systematic Review. PloS Negl. Trop. Diseases 9 (2015), e0003898.
    doi: 10.1371/journal.pntd.0003898pmc: PMC4574773pubmed: 26379143google scholar: lookup
  21. Costa F, Zeppelini C G, Ribeiro G S, Santos N, Reis R B, Martins R D. Household Rat Infestation in Urban Slum Populations: Development and Validation of a Predictive Score for Leptospirosis. PloS Negl. Trop. Dis. 15 (2021), e0009154.
    doi: 10.1371/journal.pntd.0009154pmc: PMC7959339pubmed: 33657101google scholar: lookup
  22. Cullen P A, Haake D A, Bulach D M, Zuerner R L, Adler B. LipL21 is a Novel Surface-Exposed Lipoprotein of Pathogenic Leptospira Species. Infect Immun. 71 (2003), 2414–2421.
    doi: 10.1128/IAI.71.5.2414-2421.2003pmc: PMC153295pubmed: 12704111google scholar: lookup
  23. Delude R L, Savedra R Jr, Zhao H, Thieringer R, Yamamoto S, Fenton M J. CD14 Enhances Cellular Responses to Endotoxin Without Imparting Ligand-Specific Recognition. Proc Natl Acad Sci U. S. A. 92 (1995), 9288–9292.
    doi: 10.1073/pnas.92.20.9288pmc: PMC40970pubmed: 7568119google scholar: lookup
  24. Desai S, van Treeck U, Lierz M, Espelage W, Zota L, Sarbu A. Resurgence of Field Fever in a Temperate Country: An Epidemic of Leptospirosis Among Seasonal Strawberry Harvesters in Germany in 2007. Clin. Infect. Dis. 48 (2009), 691–697.
    doi: 10.1086/597036pubmed: 19193108google scholar: lookup
  25. Dick M S, Sborgi L, Rühl S, Hiller S, Broz P. ASC Filament Formation Serves as a Signal Amplification Mechanism for Inflammasomes. Nat. Commun. 7 (2016), 11929.
    doi: 10.1038/ncomms11929pmc: PMC4917984pubmed: 27329339google scholar: lookup
  26. Donnelly M A, Steiner T S. Two Nonadjacent Regions in Enteroaggregative Escherichia Coli Flagellin Are Required for Activation of Toll-Like Receptor 5. J. Biol. Chem. 277 (2002), 40456–40461.
    doi: 10.1074/jbc.M206851200pubmed: 12185085google scholar: lookup
  27. Dyevoich A M, Disher N S, Haro M A, Haas K M. A TLR4–TRIF-Dependent Signaling Pathway is Required for Protective Natural Tumor-Reactive IgM Production by B1 Cells. Cancer Immunol. Immunother. 69 (2020), 2113–2124.
    doi: 10.1007/s00262-020-02607-7pmc: PMC7529868pubmed: 32448982google scholar: lookup
  28. Ellis W, Bryson D, Neill S, McParland P, Malone F. Possible Involvement of Leptospires in Abortion, Stillbirths and Neonatal Deaths in Sheep. Vet. Rec. 112 (1983), 291–293.
    doi: 10.1136/vr.112.13.291pubmed: 6845608google scholar: lookup
  29. Ellis W, Bryson D, O’Brien J, Neill S. Leptospiral Infection in Aborted Equine Foetuses. Equine Vet J. 15 (1983), 321–324.
    doi: 10.1111/j.2042-3306.1983.tb01811.xpubmed: 6357776google scholar: lookup
  30. Ellis W, McParland P, Bryson D, Cassells J. Prevalence of Leptospira Infection in Aborted Pigs in Northern Ireland. Vet. Rec. 118 (1986), 63–65.
    doi: 10.1136/vr.118.3.63pubmed: 3952941google scholar: lookup
  31. Ellis W, O’Brien J, Bryson D, Mackie D. Bovine Leptospirosis: Some Clinical Features of Serovar Hardjo Infection. Vet. Rec. 117 (1985), 101–104.
    doi: 10.1136/vr.117.5.101pubmed: 4049693google scholar: lookup
  32. Ellis W, Songer J, Montgomery J, Cassells J. Prevalence of Leptospira Interrogans Serovar Hardjo in the Genital and Urinary Tracts of non-Pregnant Cattle. Vet. Rec. 118 (1986), 11–13.
    doi: 10.1136/vr.118.1.11pubmed: 3511601google scholar: lookup
  33. Erridge C, Bennett-Guerrero E, Poxton I R. Structure and Function of Lipopolysaccharides. Microbes Infect. 4 (2002), 837–851.
    doi: 10.1016/S1286-4579(02)01604-0pubmed: 12270731google scholar: lookup
  34. Eshghi A, Henderson J, Trent M S, Picardeau M. Leptospira Interrogans lpxD Homologue Is Required for Thermal Acclimatization and Virulence. Infect Immun. 83 (2015), 4314–4321.
    doi: 10.1128/IAI.00897-15pmc: PMC4598399pubmed: 26283339google scholar: lookup
  35. Faber E, Tedin K, Speidel Y, Brinkmann M M, Josenhans C. Functional Expression of TLR5 of Different Vertebrate Species and Diversification in Intestinal Pathogen Recognition. Sci. Rep. 8 (2018), 11287.
    doi: 10.1038/s41598-018-29371-0pmc: PMC6062626pubmed: 30050158google scholar: lookup
  36. Fanton d’Andon M, Quellard N, Fernandez B, Ratet G, Lacroix-Lamandé S, Vandewalle A. Leptospira Interrogans Induces Fibrosis in the Mouse Kidney Through Inos-Dependent, TLR- and NLR-Independent Signaling Pathways. PloS Negl. Trop. Diseases 8 (2014), e2664.
    doi: 10.1371/journal.pntd.0002664pmc: PMC3907306pubmed: 24498450google scholar: lookup
  37. Ferrer M F, Scharrig E, Charo N, Rípodas A L, Drut R, Carrera Silva E A. Macrophages and Galectin 3 Control Bacterial Burden in Acute and Subacute Murine Leptospirosis That Determines Chronic Kidney Fibrosis. Front. Cell Infect. Microbiol. 8 (2018).
    doi: 10.3389/fcimb.2018.00384pmc: PMC6218566pubmed: 30425972google scholar: lookup
  38. Forstnerič V, Ivičak-Kocjan K, Ljubetič A, Jerala R, Benčina M. Distinctive Recognition of Flagellin by Human and Mouse Toll-Like Receptor 5. PloS One 11 (2016), e0158894.
    doi: 10.1371/journal.pone.0158894pmc: PMC4938411pubmed: 27391968google scholar: lookup
  39. Franchi L, Eigenbrod T, Núñez G. Cutting Edge: TNF-α Mediates Sensitization to ATP and Silica via the NLRP3 Inflammasome in the Absence of Microbial Stimulation. J. Immunol. 183 (2009), 792–796.
    doi: 10.4049/jimmunol.0900173pmc: PMC2754237pubmed: 19542372google scholar: lookup
  40. Frey E A. Soluble CD14 Participates in the Response of Cells to Lipopolysaccharide. J. Exp. Med. 176 (1992), 1665–1671.
    doi: 10.1084/jem.176.6.1665pmc: PMC2119444pubmed: 1281215google scholar: lookup
  41. Fritz J H, Ferrero R L, Philpott D J, Girardin S E. Nod-Like Proteins in Immunity, Inflammation and Disease. Nat. Immunol. 7 (2006), 1250–1257.
    doi: 10.1038/ni1412pubmed: 17110941google scholar: lookup
  42. Gibson K H, Trajtenberg F, Wunder E A, Brady M R, San Martin F, Mechaly A. An Asymmetric Sheath Controls Flagellar Supercoiling and Motility in the Leptospira Spirochete. eLife 9 (2020), e53672.
    doi: 10.7554/eLife.53672pmc: PMC7065911pubmed: 32157997google scholar: lookup
  43. Girardin S E, Boneca I G, Viala J, Chamaillard M, Labigne A, Thomas G. Nod2 Is a General Sensor of Peptidoglycan Through Muramyl Dipeptide (MDP) Detection. J. Biol. Chem. 278 (2003), 8869–8872.
    doi: 10.1074/jbc.C200651200pubmed: 12527755google scholar: lookup
  44. Girardin S E, Jéhanno M, Mengin-Lecreulx D, Sansonetti P J, Alzari P M, Philpott D J. Identification of the Critical Residues Involved in Peptidoglycan Detection by Nod1. J. Biol. Chem. 280 (2005), 38648–38656.
    doi: 10.1074/jbc.M509537200pubmed: 16172124google scholar: lookup
  45. Gomes C K, Guedes M, Potula H-H, Dellagostin O A, Gomes-Solecki M. Sex Matters: Male Hamsters Are More Susceptible to Lethal Infection With Lower Doses of Pathogenic Leptospira Than Female Hamsters. Infect. Immun. 86 (2018), e00369–e00318.
    doi: 10.1128/IAI.00369-18pmc: PMC6204738pubmed: 30012637google scholar: lookup
  46. Guo Y, Ding C, Zhang B, Xu J, Xun M, Xu J. Inhibitory Effect of BMAP-28 on Leptospiral Lipopolysaccharide-Induced TLR2-Dependent Immune Response in Bovine Cells. Jundishapur J. Microbiol. 9 (2016).
    doi: 10.5812/jjm.33926pmc: PMC5013549pubmed: 27635213google scholar: lookup
  47. Guo Y, Fukuda T, Nakamura S, Bai L, Xu J, Kuroda K. Interaction Between Leptospiral Lipopolysaccharide and Toll-Like Receptor 2 in Pig Fibroblast Cell Line, and Inhibitory Effect of Antibody Against Leptospiral Lipopolysaccharide on Interaction. Asian-Australasian J. Anim. Sci. 28 (2015), 273.
    doi: 10.5713/ajas.14.0440pmc: PMC4283174pubmed: 25557825google scholar: lookup
  48. Haake D A, Chao G, Zuerner R L, Barnett J K, Barnett D, Mazel M. The Leptospiral Major Outer Membrane Protein LipL32 is a Lipoprotein Expressed During Mammalian Infection. Infect immun. 68 (2000), 2276–2285.
    doi: 10.1128/IAI.68.4.2276-2285.2000pmc: PMC97414pubmed: 10722630google scholar: lookup
  49. Haake D A, Zückert W R. The Leptospiral Outer Membrane. Curr. Top. Microbiol. Immunol. 387 (2015), 187–221.
    doi: 10.1007/978-3-662-45059-8_8pmc: PMC4419373pubmed: 25388136google scholar: lookup
  50. Hailman E, Lichenstein H S, Wurfel M M, Miller D S, Johnson D A, Kelley M. Lipopolysaccharide (LPS)-Binding Protein Accelerates the Binding of LPS to CD14. J. Exp. Med. 179 (1994), 269–277.
    doi: 10.1084/jem.179.1.269pmc: PMC2191344pubmed: 7505800google scholar: lookup
  51. Hamond C, Silveira C S, Buroni F, Suanes A, Nieves C, Salaberry X. Leptospira Interrogans Serogroup Pomona Serovar Kennewicki Infection in Two Sheep Flocks With Acute Leptospirosis in Uruguay. Transbound Emerg. Dis. 66 (2019), 1186–1194.
    doi: 10.1111/tbed.13133pubmed: 30685885google scholar: lookup
  52. Hathaway S C, Blackmore D K. Ecological Aspects of the Epidemiology of Infection With Leptospires of the Ballum Serogroup in the Black Rat ( Rattus Rattus ) and the Brown Rat ( Rattus Norvegicus ) in New Zealand. J. Hyg. 87 (1981), 427–436.
    doi: 10.1017/S0022172400069679pmc: PMC2134120pubmed: 7310125google scholar: lookup
  53. Hayashi F, Smith K D, Ozinsky A, Hawn T R, Yi E C, Goodlett D R. The Innate Immune Response to Bacterial Flagellin is Mediated by Toll-Like Receptor 5. Nature 410 (2001), 1099–1103.
    doi: 10.1038/35074106pubmed: 11323673google scholar: lookup
  54. He Y, Hara H, Núñez G. Mechanism and Regulation of NLRP3 Inflammasome Activation. Trends Biochem. Sci. 41 (2016), 1012–1021.
    doi: 10.1016/j.tibs.2016.09.002pmc: PMC5123939pubmed: 27669650google scholar: lookup
  55. Heuser E, Fischer S, Ryll R, Mayer-Scholl A, Hoffmann D, Spahr C. Survey for Zoonotic Pathogens in Norway Rat Populations From Europe: Survey for Zoonotic Pathogens in Norway Rat Populations From Europe. Pest Manag Sci. 73 (2017), 341–348.
    doi: 10.1002/ps.4339pubmed: 27299665google scholar: lookup
  56. Holzapfel M, Bonhomme D, Cagliero J, Vernel-Pauillac F, Fanton d’Andon M, Bortolussi S. Escape of TLR5 Recognition by Leptospira Spp.: A Rationale for Atypical Endoflagella. Front. Immunol. 149 (2020), e229.
    doi: 10.3389/fimmu.2020.02007pmc: PMC7431986pubmed: 32849665google scholar: lookup
  57. Holzapfel M, Taraveau F, Djelouadji Z. Serological and Molecular Detection of Pathogenic Leptospira in Domestic and Stray Cats on Reunion Island, French Indies. Epidemiol. Infect. (2021), 1–28.
    doi: 10.1017/S095026882100176Xpmc: PMC8569831pubmed: 34372952google scholar: lookup
  58. Hsu S-H, Chang M-Y, Lin S-M, Ko Y-C, Chou L-F, Tian Y-C. Peptidoglycan Mediates Leptospira Outer Membrane Protein Loa22 to Toll-Like Receptor 2 for Inflammatory Interaction: A Novel Innate Immune Recognition. Sci. Rep. 11 (2021), 1064.
    doi: 10.1038/s41598-020-79662-8pmc: PMC8115183pubmed: 33441663google scholar: lookup
  59. Hsu S-H, Hung C-C, Chang M-Y, Ko Y-C, Yang H-Y, Hsu H-H. Active Components of Leptospira Outer Membrane Protein LipL32 to Toll-Like Receptor 2. Sci. Rep. 7 (2017), 1–16.
    doi: 10.1038/s41598-017-08743-ypmc: PMC5566480pubmed: 28827637google scholar: lookup
  60. Hsu S-H, Lo Y-Y, Tung J-Y, Ko Y-C, Sun Y-J, Hung C-C. Leptospiral Outer Membrane Lipoprotein LipL32 Binding on Toll-Like Receptor 2 of Renal Cells As Determined With an Atomic Force Microscope. Biochemistry 49 (2010), 5408–5417.
    doi: 10.1021/bi100058wpubmed: 20513152google scholar: lookup
  61. Jin M S, Lee J-O. Structures of the Toll-Like Receptor Family and Its Ligand Complexes. Immun. 29 (2008), 182–191.
    doi: 10.1016/j.immuni.2008.07.007pubmed: 18701082google scholar: lookup
  62. Kang J Y, Nan X, Jin M S, Youn S-J, Ryu Y H, Mah S. Recognition of Lipopeptide Patterns by Toll-Like Receptor 2-Toll-Like Receptor 6 Heterodimer. Immun. 31 (2009), 873–884.
    doi: 10.1016/j.immuni.2009.09.018pubmed: 19931471google scholar: lookup
  63. Kawai T, Akira S. The Role of Pattern-Recognition Receptors in Innate Immunity: Update on Toll-Like Receptors. Nat. Immunol. 11 (2010), 373–384.
    doi: 10.1038/ni.1863pubmed: 20404851google scholar: lookup
  64. Keestra A M, de Zoete M R, van Aubel R A, van Putten J P. Functional Characterization of Chicken TLR5 Reveals Species-Specific Recognition of flagellin. Mol. Immunol. 45 (2008), 1298–1307.
    doi: 10.1016/j.molimm.2007.09.013pubmed: 17964652google scholar: lookup
  65. Keestra A M, de Zoete M R, van Aubel R A M H, van Putten J P M. The Central Leucine-Rich Repeat Region of Chicken TLR16 Dictates Unique Ligand Specificity and Species-Specific Interaction With TLR2. J. Immunol. 178 (2007), 7110–7119.
    doi: 10.4049/jimmunol.178.11.7110pubmed: 17513760google scholar: lookup
  66. Kobayashi K, Inohara N, Hernandez L D, Galán J E, Núñez G, Janeway C A. RICK/Rip2/CARDIAK Mediates Signalling for Receptors of the Innate and Adaptive Immune Systems. Nat 416 (2002), 194–199.
    doi: 10.1038/416194apubmed: 11894098google scholar: lookup
  67. Ko A I, Goarant C, Picardeau M. Leptospira: The Dawn of the Molecular Genetics Era for an Emerging Zoonotic Pathogen. Nat. Rev. Microbiol. 7 (2009), 736–747.
    doi: 10.1038/nrmicro2208pmc: PMC3384523pubmed: 19756012google scholar: lookup
  68. Lacroix-Lamande S, Fanton d’Andon M, Michel E, Ratet G, Philpott D J, Girardin S E. Downregulation of the Na/K-ATPase Pump by Leptospiral Glycolipoprotein Activates the NLRP3 Inflammasome. J. Immunol. 188 (2012), 2805–2814.
    doi: 10.4049/jimmunol.1101987pubmed: 22323544google scholar: lookup
  69. Larsson C, Santa Rosa C, Larsson M, Birgel E, Fernandes W, Paim G. Laboratory and Clinical Features of Experimental Feline Leptospirosis. Int. J. Zoonoses 12 (1985), 111–119.
    pubmed: 4077410
  70. Lawlor K E, Vince J E. Ambiguities in NLRP3 Inflammasome Regulation: Is There a Role for Mitochondria?. Biochim. Biophys. Acta (BBA) - Gen. Subj. 1840 (2014), 1433–1440.
    doi: 10.1016/j.bbagen.2013.08.014pubmed: 23994495google scholar: lookup
  71. Leonvizcaino L, Demendoza M, Garrido F. Incidence of Abortions Caused by Leptospirosis in Sheep and Goats in Spain. Comp. Immunol Microbiol. Infect. Diseases 10 (1987), 149–153.
    doi: 10.1016/0147-9571(87)90009-9pubmed: 3304822google scholar: lookup
  72. Lilenbaum W, Varges R, Brandão F Z, Cortez A, de Souza S O, Brandão P E. Detection of Leptospira Spp. In Semen and Vaginal Fluids of Goats and Sheep by Polymerase Chain Reaction. Theriogenology 69 (2008), 837–842.
    doi: 10.1016/j.theriogenology.2007.10.027pubmed: 18291518google scholar: lookup
  73. Li S, Wang M, Ojcius D M, Zhou B, Hu W, Liu Y. Leptospira Interrogans Infection Leads to IL-1β and IL-18 Secretion From a Human Macrophage Cell Line Through Reactive Oxygen Species and Cathepsin B Mediated-NLRP3 Inflammasome Activation. Microbes Infect. 20 (2018), 254–260.
    doi: 10.1016/j.micinf.2018.01.010pubmed: 29432801google scholar: lookup
  74. Li S, Wang M, Ojcius D M, Zhou B, Hu W, Liu Y. Corrigendum to “Leptospira Interrogans Infection Leads to IL-1β and IL-18 Secretion From a Human Macrophage Cell Line Through Reactive Oxygen Species and Cathepsin B Mediated-NLRP3 Inflammasome Activation” [Microbe Infect, (2018) 254–260]. Microbes Infect. 23 (2021), 104756.
    doi: 10.1016/j.micinf.2020.09.002pubmed: 32988716google scholar: lookup
  75. Lo Y-Y, Hsu S-H, Ko Y-C, Hung C-C, Chang M-Y, Hsu H-H. Essential Calcium-Binding Cluster of Leptospira LipL32 Protein for Inflammatory Responses Through the Toll-Like Receptor 2 Pathway. J. Biol. Chem. 288 (2013), 12335–12344.
    doi: 10.1074/jbc.M112.418699pmc: PMC3636917pubmed: 23486465google scholar: lookup
  76. Lourdault K, Aviat F, Picardeau M. Use of Quantitative Real-Time PCR for Studying the Dissemination of Leptospira Interrogans in the Guinea Pig Infection Model of Leptospirosis. J. Med. Microbiol. 58 (2009), 648–655.
    doi: 10.1099/jmm.0.008169-0pubmed: 19369528google scholar: lookup
  77. Lozano-Aponte J, Scior T, Ambrosio F N M, González-Melchor M, Alexander C. Exploring Electrostatic Patterns of Human, Murine, Equine and Canine TLR4/MD-2 Receptors. Innate Immun. 26 (2020), 364–380.
    doi: 10.1177/1753425919894628pmc: PMC7903528pubmed: 31874581google scholar: lookup
  78. Magalhaes J G, Philpott D J, Nahori M, Jéhanno M, Fritz J, Bourhis L. Murine Nod1 But Not its Human Orthologue Mediates Innate Immune Detection of Tracheal Cytotoxin. EMBO Rep. 6 (2005), 1201–1207.
    doi: 10.1038/sj.embor.7400552pmc: PMC1369207pubmed: 16211083google scholar: lookup
  79. Malkiel S, Kuhlow C J, Mena P, Benach J L. The Loss and Gain of Marginal Zone and Peritoneal B Cells Is Different in Response to Relapsing Fever and Lyme Disease Borrelia. J. Immunol. 182 (2009), 498–506.
    doi: 10.4049/jimmunol.182.1.498pubmed: 19109181google scholar: lookup
  80. Malmström J, Beck M, Schmidt A, Lange V, Deutsch E W, Aebersold R. Proteome-Wide Cellular Protein Concentrations of the Human Pathogen Leptospira Interrogans. Nat 460 (2009), 762–765.
    doi: 10.1038/nature08184pmc: PMC2723184pubmed: 19606093google scholar: lookup
  81. Matsui M, Roche L, Geroult S, Soupé-Gilbert M-E, Monchy D, Huerre M. Cytokine and Chemokine Expression in Kidneys During Chronic Leptospirosis in Reservoir and Susceptible Animal Models. PloS One 11 (2016), e0156084.
    doi: 10.1371/journal.pone.0156084pmc: PMC4878748pubmed: 27219334google scholar: lookup
  82. Medzhitov R, Preston-Hurlburt P, Janeway C A. A Human Homologue of the Drosophila Toll Protein Signals Activation of Adaptive Immunity. Nat 388 (1997), 394–397.
    doi: 10.1038/41131pubmed: 9237759google scholar: lookup
  83. Meng J, Drolet J R, Monks B G, Golenbock D T. MD-2 Residues Tyrosine 42, Arginine 69, Aspartic Acid 122, and Leucine 125 Provide species-specificity for Lipid IVA. J. Biol. Chem. 285 (2010), 27935–27943.
    doi: 10.1074/jbc.M110.134668pmc: PMC2934660pubmed: 20592019google scholar: lookup
  84. Metcalfe H J, La Ragione R M, Smith D G E, Werling D. Functional Characterisation of Bovine TLR5 Indicates Species-Specific Recognition of Flagellin. Vet Immunol. Immunopathol. 157 (2014), 197–205.
    doi: 10.1016/j.vetimm.2013.12.006pmc: PMC3969226pubmed: 24461722google scholar: lookup
  85. Miller D K, Ayala J M, Egger L A, Raju S M, Yamin T T, Ding G J. Purification and Characterization of Active Human Interleukin-1 Beta-Converting Enzyme From THP.1 Monocytic Cells. J. Biol. Chem. 268 (1993), 18062–18069.
    doi: 10.1016/S0021-9258(17)46811-6pubmed: 8349684google scholar: lookup
  86. Moinet M, Wilkinson D A, Aberdein D, Russell J C, Vallée E, Collins-Emerson J M. Of Mice, Cattle, and Men: A Review of the Eco-Epidemiology of Leptospira Borgpetersenii Serovar Ballum. TropicalMed 6 (2021), 189.
    doi: 10.3390/tropicalmed6040189pmc: PMC8544700pubmed: 34698305google scholar: lookup
  87. Monte L G, Jorge S, Xavier M A, Leal F M A, Amaral M G, Seixas F K. Molecular Characterization of Virulent Leptospira Interrogans Serogroup Icterohaemorrhagiae Isolated From Cavia Aperea. Acta Tropica 126 (2013), 164–166.
    doi: 10.1016/j.actatropica.2013.02.009pubmed: 23435256google scholar: lookup
  88. Moore G E, Guptill L F, Glickman N W, Caldanaro R J, Aucoin D, Glickman L T. Canine Leptospirosis, United States 2002–2004. Emerg. Infect. Dis. 12 (2006), 501–503.
    doi: 10.3201/eid1203.050809pmc: PMC3291439pubmed: 16704794google scholar: lookup
  89. Muñoz-Planillo R, Kuffa P, Martínez-Colón G, Smith B L, Rajendiran T M, Núñez G. K+ Efflux Is the Common Trigger of NLRP3 Inflammasome Activation by Bacterial Toxins and Particulate Matter. Immun. 38 (2013), 1142–1153.
    doi: 10.1016/j.immuni.2013.05.016pmc: PMC3730833pubmed: 23809161google scholar: lookup
  90. Nagel A, Vázquez C L, Etulain J, Blanco F C, Gravisaco M J, Gómez R M. Bovine Macrophages Responses to the Infection With Virulent and Attenuated Leptospira Interrogans Serovar Pomona. Vet Microbiol. 233 (2019), 124–132.
    doi: 10.1016/j.vetmic.2019.04.033pubmed: 31176398google scholar: lookup
  91. Nahori M-A, Fournié-Amazouz E, Que-Gewirth N S, Balloy V, Chignard M, Raetz C R H. Differential TLR Recognition of Leptospiral Lipid A and Lipopolysaccharide in Murine and Human Nells. J. Immunol. 175 (2005), 6022.
    doi: 10.4049/jimmunol.175.9.6022pubmed: 16237097google scholar: lookup
  92. Nair N, Guedes M S, Hajjar A M, Werts C, Gomes-Solecki M. Role of TLR4 in Persistent Leptospira Interrogans Infection: A Comparative In Vivo Study in Mice. Front. Immunol. 11 (2021).
    doi: 10.3389/fimmu.2020.572999pmc: PMC7843520pubmed: 33519799google scholar: lookup
  93. Nally J E, Fishbein M C, Blanco D R, Lovett M A. Lethal Infection of C3H/HeJ and C3H/SCID Mice With an Isolate of Leptospira Interrogans Serovar Copenhageni. Infect. Immun. 73 (2005), 7014–7017.
    doi: 10.1128/IAI.73.10.7014-7017.2005pmc: PMC1230959pubmed: 16177383google scholar: lookup
  94. Nalubamba K S, Gossner A G, Dalziel R G, Hopkins J. Differential Expression of Pattern Recognition Receptors in Sheep Tissues and Leukocyte Subsets. Vet Immunol. Immunopathol. 118 (2007), 252–262.
    doi: 10.1016/j.vetimm.2007.05.018pubmed: 17604125google scholar: lookup
  95. Netea M G, Nold-Petry C A, Nold M F, Joosten L A, Opitz B, van de Meer J H. Differential Requirement for the Activation of the Inflammasome for Processing and Release of IL-1␤ in Monocytes and Macrophages. Blood 113 (2009), 2324–2335.
    doi: 10.1182/blood-2008-03-146720pmc: PMC2652374pubmed: 19104081google scholar: lookup
  96. Novak A, Pupo E, van’t Veld E, Rutten V P M G, Broere F, Sloots A. Activation of Canine, Mouse and Human TLR2 and TLR4 by Inactivated Leptospira Vaccine Strains. Front. Immunol. 13 (2022).
    doi: 10.3389/fimmu.2022.823058pmc: PMC8978998pubmed: 35386703google scholar: lookup
  97. Osvaldova A, Woodman S, Patterson N, Offord V, Mwangi D, Gibson A J. Replacement of Two Aminoacids in the Bovine Toll-Like Receptor 5 TIR Domain With Their Human Counterparts Partially Restores Functional Response to Flagellin. Dev. Comp. Immunol. 47 (2014), 90–94.
    doi: 10.1016/j.dci.2014.07.002pubmed: 25020193google scholar: lookup
  98. Paiva-Cardoso M das N, Arent Z, Gilmore C, Hartskeerl R, Ellis W A. Altodouro, a New Leptospira Serovar of the Pomona Serogroup Isolated From Rodents in Northern Portugal. Infect Genet. Evolution. 13 (2013), 211–217.
    doi: 10.1016/j.meegid.2012.09.013pubmed: 23070280google scholar: lookup
  99. Panda S, Ding J L. Natural Antibodies Bridge Innate and Adaptive Immunity. JI 194 (2015), 13–20.
    doi: 10.4049/jimmunol.1400844pubmed: 25527792google scholar: lookup
  100. Park B S, Song D H, Kim H M, Choi B-S, Lee H, Lee J-O. The Structural Basis of Lipopolysaccharide Recognition by the TLR4–MD-2 Complex. Nat 458 (2009), 1191–1195.
    doi: 10.1038/nature07830pubmed: 19252480google scholar: lookup
  101. Patra K P, Choudhury B, Matthias M M, Baga S, Bandyopadhya K, Vinetz J M. Comparative Analysis of Lipopolysaccharides of Pathogenic and Intermediately Pathogenic Leptospira Species. BMC Microbiol. 15 (2015), 244.
    doi: 10.1186/s12866-015-0581-7pmc: PMC4628369pubmed: 26518696google scholar: lookup
  102. Pena-Moctezuma A, Bulach D M, Kalambaheti T, Adler B. Comparative Analysis of the LPS Biosynthetic Loci of the Genetic Subtypes of Serovar Hardjo: Leptospira Interrogans Subtype Hardjoprajitno and Leptospira Borgpetersenii Subtype Hardjobovis. FEMS Microbiol. Lett. 177 (1999), 319–326.
    doi: 10.1111/j.1574-6968.1999.tb13749.xpubmed: 10474199google scholar: lookup
  103. Pereira M M, Andrade J, Marchevsky R S, Ribeiro dos Santos R. Morphological Characterization of Lung and Kidney Lesions Inc3h/HeJ Mice Infected With Leptospira Interrogans Serovar Icterohaemorrhagiae: Defect of CD4+ and CD8+ T-Cells are Prognosticators of the Disease Progression. Exp. Toxicol Pathol. 50 (1998), 191–198.
    doi: 10.1016/S0940-2993(98)80083-3pubmed: 9681649google scholar: lookup
  104. Poltorak A. Defective LPS Signaling in C3H/HeJ and C57BL/10ScCr Mice: Mutations in Tlr4 Gene. Sci. 282 (1998), 2085–2088.
    doi: 10.1126/science.282.5396.2085pubmed: 9851930google scholar: lookup
  105. Que-Gewirth N L S, Ribeiro A A, Kalb S R, Cotter R J, Bulach D M, Adler B. A Methylated Phosphate Group and Four Amide-Linked Acyl Chains in Leptospira Interrogans Lipid A: The Membrane Anchor of an Unusual Lipopolysaccharide That Activates TLR2. J. Biol. Chem. 279 (2004), 25420–25429.
    doi: 10.1074/jbc.M400598200pmc: PMC2556802pubmed: 15044492google scholar: lookup
  106. Raddi G, Morado D R, Yan J, Haake D A, Yang X F, Liu J. Three-Dimensional Structures of Pathogenic and Saprophytic Leptospira Species Revealed by Cryo-Electron Tomography. J. Bacteriol. 194 (2012), 1299–1306.
    doi: 10.1128/JB.06474-11pmc: PMC3294836pubmed: 22228733google scholar: lookup
  107. Rajeev S, Toka F N, Shiokawa K. Potential Use of a Canine Whole Blood Culture System to Evaluate the Immune Response to Leptospira. Comp. Immunol Microbiol. Infect. Diseases 73 (2020), 101546.
    doi: 10.1016/j.cimid.2020.101546pubmed: 32916553google scholar: lookup
  108. Ranoa D R E, Kelley S L, Tapping R I. Human Lipopolysaccharide-Binding Protein (LBP) and CD14 Independently Deliver Triacylated Lipoproteins to Toll-Like Receptor 1 (TLR1) and TLR2 and Enhance Formation of the Ternary Signaling Complex. J. Biol. Chem. 288 (2013), 9729.
    doi: 10.1074/jbc.M113.453266pmc: PMC3617275pubmed: 23430250google scholar: lookup
  109. Ratet G, Santecchia I, Fanton d’Andon M, Vernel-Pauillac F, Wheeler R, Lenormand P. LipL21 Lipoprotein Binding to Peptidoglycan Enables Leptospira Interrogans to Escape NOD1 and NOD2 Recognition. PloS Pathogens 13 (2017), e1006725.
    doi: 10.1371/journal.ppat.1006725pmc: PMC5764436pubmed: 29211798google scholar: lookup
  110. Ratet G, Veyrier F J, Fanton d’Andon M, Kammerscheit X, Nicola M-A, Picardeau M. Live Imaging of Bioluminescent Leptospira Interrogans in Mice Reveals Renal Colonization as a Stealth Escape From the Blood Defenses and Antibiotics. PloS Negl. Trop. Diseases 8 (2014), e3359.
    doi: 10.1371/journal.pntd.0003359pmc: PMC4256284pubmed: 25474719google scholar: lookup
  111. Ren S-X, Fu G, Jiang X-G, Zeng R, Miao Y-G, Xu H. Unique Physiological and Pathogenic Features of Leptospira Interrogans Revealed by Whole-Genome Sequencing. Nat 422 (2003), 888–893.
    doi: 10.1038/nature01597pubmed: 12712204google scholar: lookup
  112. Rietschel E T, Kirikae T, Schade F U, Mamat U, Schmidt G, Loppnow H. Bacterial Endotoxin: Molecular Relationships of Structure to Activity and Function. FASEB J. 8 (1994), 217–225.
    doi: 10.1096/fasebj.8.2.8119492pubmed: 8119492google scholar: lookup
  113. Rigby C. Natural Infections of Guinea-Pigs. Lab. Anim. 10 (1976), 119–142.
    doi: 10.1258/002367776781071503pubmed: 180326google scholar: lookup
  114. Ristow P, Bourhy P, McBride FW da C, Figueira C P, Huerre M, Ave P. The OmpA-Like Protein Loa22 is Rssential for Leptospiral Virulence. PloS Pathogens 3 (2007), e97.
    doi: 10.1371/journal.ppat.0030097pmc: PMC1914066pubmed: 17630832google scholar: lookup
  115. Ritter J M, Lau C, Craig S B, Goarant C, Nilles E J, Ko A I. A Large Leptospirosis Outbreak Following Successive Severe Floods in Fij. Am. J. Trop. Med. Hygiene 99 (2018), 849–851.
    doi: 10.4269/ajtmh.18-0335pmc: PMC6159581pubmed: 30141390google scholar: lookup
  116. Ryu J-K, Kim S J, Rah S-H, Kang J I, Jung H E, Lee D. Reconstruction of LPS Transfer Cascade Reveals Structural Determinants Within LBP, CD14, and TLR4-MD2 for Efficient LPS Recognition and Transfer. Immun. 46 (2017), 38–50.
    doi: 10.1016/j.immuni.2016.11.007pubmed: 27986454google scholar: lookup
  117. Sansonetti P J, Phalipon A, Arondel J, Thirumalai K, Banerjee S, Akira S. Caspase-1 Activation of IL-1␤ and IL-18 Are Essential for Shigella Flexneri–Induced Inflammation. Immunity 12 (2000), 581–590.
    doi: 10.1016/S1074-7613(00)80209-5pubmed: 10843390google scholar: lookup
  118. Sebek Z, Grulich I, Valova M. To the Knowledge of the Common Hamster (Cricetus Cricetus Linné, 1758; Rodentia) as a Host of Leptospirosis in Czechoslovajia. Folia Parasitol. (Praha) 34 (1987), 97–105.
    pubmed: 3596398
  119. Sellati T J, Bouis D A, Caimano M J, Feulner J A, Ayers C, Lien E. Activation of Human Monocytic Cells by Borrelia Burgdorferi and Treponema Pallidum is Facilitated by CD14 and Correlates With Surface Exposure of Spirochetal Lipoproteins. J. Immunol. 163 (1999), 2049–2056.
    pubmed: 10438943
  120. Sellati T J, Bouis D A, Kitchens R L, Darveau R P, Pugin J, Ulevitch R J. Treponema Pallidum and Borrelia Burgdorferi Lipoproteins and Synthetic Lipopeptides Activate Monocytic Cells via a CD14-Dependent Pathway Distinct From That Used by Lipopolysaccharide. J. Immunol. 160 (1998), 5455–5464.
    pubmed: 9605148
  121. Senavirathna I, Rathish D, Agampodi S. Cytokine Response in Human Leptospirosis With Different Clinical Outcomes: A Systematic Review. BMC Infect. Dis. 20 (2020), 268.
    doi: 10.1186/s12879-020-04986-9pmc: PMC7137275pubmed: 32264832google scholar: lookup
  122. Slamti L, de Pedro M A, Guichet E, Picardeau M. Deciphering Morphological Determinants of the Helix-Shaped Leptospira. J. Bacteriol. 193 (2011), 6266–6275.
    doi: 10.1128/JB.05695-11pmc: PMC3209227pubmed: 21926230google scholar: lookup
  123. Smith K D, Andersen-Nissen E, Hayashi F, Strobe K, Bergman M A, Barrett S L R. Toll-Like Receptor 5 Recognizes a Conserved Site on Flagellin Required for Protofilament Formation and Bacterial Motility. Nat. Immunol. 4 (2003), 1247–1253.
    doi: 10.1038/ni1011pubmed: 14625549google scholar: lookup
  124. Subharat S, Wilson P, Heuer C, Collins-Emerson J. Investigation of Localisation of Leptospira Spp. In Uterine and Fetal Tissues of non-Pregnant and Pregnant Farmed Deer. null 58 (2010), 281–285.
    doi: 10.1080/00480169.2010.69755pubmed: 21151213google scholar: lookup
  125. Su Q, Chen Y, Wang B, Zhang Q, He H. Genetic Characterization of Toll-Like Receptors in the Brown Rat and Their Association With Pathogen Infections. Integr. Zool. 0 (2021), 1–11.
    doi: 10.1111/1749-4877.12555pubmed: 34003606google scholar: lookup
  126. Tahoun A, Jensen K, Corripio-Miyar Y, McAteer S, Smith D G E, McNeilly T N. Host Species Adaptation of TLR5 Signalling and Flagellin Recognition. Sci. Rep. 7 (2017), 17677.
    doi: 10.1038/s41598-017-17935-5pmc: PMC5732158pubmed: 29247203google scholar: lookup
  127. Teghanemt A, Zhang D, Levis E N, Weiss J P, Gioannini T L. Molecular Basis of Reduced Potency of Underacylated Endotoxins. J. Immunol. 175 (2005), 4669–4676.
    doi: 10.4049/jimmunol.175.7.4669pubmed: 16177114google scholar: lookup
  128. Vincent A T, Schiettekatte O, Goarant C, Neela V K, Bernet E, Thibeaux R. Revisiting the Taxonomy and Evolution of Pathogenicity of the Genus Leptospira Through the Prism of Genomics. PloS Negl. Trop. Dis. 13 (2019), e0007270.
    doi: 10.1371/journal.pntd.0007270pmc: PMC6532842pubmed: 31120895google scholar: lookup
  129. Vinh T, Adler B, Faine S. Ultrastructure and Chemical Composition of Lipopolysaccharide Extracted From Leptospira Interrogans Serovar Copenhageni. J. Gen. Microbiol. 132 (1986), 103–109.
    doi: 10.1099/00221287-132-1-103pubmed: 3711857google scholar: lookup
  130. Viriyakosol S, Matthias M A, Swancutt M A, Kirkland T N, Vinetz J M. Toll-Like Receptor 4 Protects Against Lethal Leptospira Interrogans Serovar Icterohaemorrhagiae Infection and Contributes to In Vivo Control of Leptospiral Burden. IAI 74 (2006), 887–895.
    doi: 10.1128/IAI.74.2.887-895.2006pmc: PMC1360355pubmed: 16428731google scholar: lookup
  131. Vollmer W, Blanot D, De Pedro M A. Peptidoglycan Structure and Architecture. FEMS Microbiol. Rev. 32 (2008), 149–167.
    doi: 10.1111/j.1574-6976.2007.00094.xpubmed: 18194336google scholar: lookup
  132. Wang H, Mao L, Meng G. The NLRP3 Inflammasome Activation in Human or Mouse Cells, Sensitivity Causes Puzzle. Protein Cell. 4 (2013), 565–568.
    doi: 10.1007/s13238-013-3905-0pmc: PMC4875544pubmed: 23794000google scholar: lookup
  133. Werling D, Jann O C, Offord V, Glass E J, Coffey T J. Variation Matters: TLR Structure and Species-Specific Pathogen Recognition. Trends Immunol. 30 (2009), 124–130.
    doi: 10.1016/j.it.2008.12.001pubmed: 19211304google scholar: lookup
  134. Werts C, Tapping R I, Mathison J C, Chuang T-H, Kravchenko V, Saint Girons I. Leptospiral Lipopolysaccharide Activates Cells Through a TLR2-Dependent Mechanism. Nat. Immunol. 2 (2001), 346–352.
    doi: 10.1038/86354pubmed: 11276206google scholar: lookup
  135. Wooten R M, Morrison T B, Weis J H, Wright S D, Thieringer R, Weis J J. The Role of CD14 in Signaling Mediated by Outer Membrane Lipoproteins of Borrelia Burgdorferi. J. Immunol. 160 (1998), 5485–5492.
    pubmed: 9605151
  136. Wright S, Ramos R, Tobias P, Ulevitch R, Mathison J. CD14, a Receptor for Complexes of Lipopolysaccharide (LPS) and LPS Binding Protein. Sci. 249 (1990), 1431–1433.
    doi: 10.1126/science.1698311pubmed: 1698311google scholar: lookup
  137. Xia B, Sun L, Fan X, Xiao H, Zhu Y, Qin J. A New Model of Self-Resolving Leptospirosis in Mice Infected With a Strain of Leptospira Interrogans Serovar Autumnalis Harboring LPS Signaling Only Through TLR4. Emerg. Microbes Infect. 6 (2017), e36.
    doi: 10.1038/emi.2017.16pmc: PMC5520481pubmed: 28536433google scholar: lookup
  138. Yamin T-T, Ayala J M, Miller D K. Activation of the Native 45-kDa Precursor Form of Interleukin-1-Converting Enzyme. J. Biol. Chem. 271 (1996), 13273–13282.
    doi: 10.1074/jbc.271.22.13273pubmed: 8662843google scholar: lookup
  139. Yang C-W, Hung C-C, Wu M-S, Tian Y-C, Chang C-T, Pan M-J. Toll-Like Receptor 2 Mediates Early Inflammation by Leptospiral Outer Membrane Proteins in Proximal Tubule Cells. Kidney Int. 69 (2006), 815–822.
    doi: 10.1038/sj.ki.5000119pubmed: 16437059google scholar: lookup
  140. Yoon S-I, Kurnasov O, Natarajan V, Hong M, Gudkov A V, Osterman A L. Structural Basis of TLR5-Flagellin Recognition and Signaling. Sci. 335 (2012), 859–864.
    doi: 10.1126/science.1215584pmc: PMC3406927pubmed: 22344444google scholar: lookup
  141. Zhang W, Xie X, Wu D, Jin X, Liu R, Hu X. Doxycycline Attenuates Leptospira-Induced IL-1β by Suppressing NLRP3 Inflammasome Priming. Front. Immunol. 8 (2017).
    doi: 10.3389/fimmu.2017.00857pmc: PMC5522854pubmed: 28791016google scholar: lookup
  142. Zhu A, Wei L, Hu S, Yang C, Chen C, Zhou Z. Characterisation and Functional Analysis of Canine TLR5. Innate Immun. 26 (2020), 451–458.
    doi: 10.1177/1753425920901862pmc: PMC7491235pubmed: 31986950google scholar: lookup

Citations

This article has been cited 12 times.
  1. Giraud-Gatineau A, Dagbo K, Pětrošová H, Werts C, Veyrier FJ, Picardeau M. Shaping the future of Leptospira serotyping. J Med Microbiol 2025 Sep;74(9).
    doi: 10.1099/jmm.0.002059pubmed: 40938636google scholar: lookup
  2. Chinchilla D, Sánchez I, Montero D, Picardeau M, Gutiérrez R. In-house isolation protocol from human serum samples demonstrates the circulating of a broad diversity of Leptospira serogroups in Costa Rica. Sci Rep 2025 Mar 20;15(1):9614.
    doi: 10.1038/s41598-025-93301-0pubmed: 40113886google scholar: lookup
  3. Dai D, Dong C, Kong F, Wang S, Wang S, Wang W, Li S. Dietary supplementation of S cutellariae radix flavonoid extract improves lactation performance in dairy cows by regulating gastrointestinal microbes, antioxidant capacity and immune function. Anim Nutr 2025 Mar;20:499-508.
    doi: 10.1016/j.aninu.2024.11.019pubmed: 40092352google scholar: lookup
  4. Garcia LE, Lin Z, Culos S, Catherine Muenker M, Johnson EE, Wang Z, Lopez-Giraldez F, Giraud-Gatineau A, Jackson A, Picardeau M, Goodlett DR, Townsend JP, Pětrošová H, Wunder EA Jr. DMEM and EMEM are suitable surrogate media to mimic host environment and expand leptospiral pathogenesis studies using in vitro tools. bioRxiv 2025 Jan 24;.
    doi: 10.1101/2025.01.22.634353pubmed: 39896660google scholar: lookup
  5. Papadopoulos S, Hardy D, Vernel-Pauillac F, Tichit M, Boneca IG, Werts C. Myocarditis and neutrophil-mediated vascular leakage but not cytokine storm associated with fatal murine leptospirosis. EBioMedicine 2025 Feb;112:105571.
    doi: 10.1016/j.ebiom.2025.105571pubmed: 39889371google scholar: lookup
  6. Kirkimbayeva Z, Biyashev B, Yermagambetova S, Kuzembekova G, Abdeliev B. A retrospective study of animal leptospirosis in Kazakhstan. J Adv Vet Anim Res 2024 Jun;11(2):439-448.
    doi: 10.5455/javar.2024.k793pubmed: 39101084google scholar: lookup
  7. Giraud-Gatineau A, Nieves C, Harrison LB, Benaroudj N, Veyrier FJ, Picardeau M. Evolutionary insights into the emergence of virulent Leptospira spirochetes. PLoS Pathog 2024 Jul;20(7):e1012161.
    doi: 10.1371/journal.ppat.1012161pubmed: 39018329google scholar: lookup
  8. Giraud-Gatineau A, Nieves C, Harrison LB, Benaroudj N, Veyrier FJ, Picardeau M. Evolutionary insights into the emergence of virulent Leptospira spirochetes. bioRxiv 2024 Apr 2;.
    doi: 10.1101/2024.04.02.587687pubmed: 38617210google scholar: lookup
  9. Yang QF, Shu CM, Ji QY. Diagnosis of pulmonary hemorrhagic leptospirosis complicated by invasive pulmonary aspergillosis complemented by metagenomic next-generation sequencing: a case report. Front Med (Lausanne) 2024;11:1365096.
    doi: 10.3389/fmed.2024.1365096pubmed: 38500954google scholar: lookup
  10. Petakh P, Oksenych V, Kamyshna I, Boisak I, Lyubomirskaya K, Kamyshnyi O. Exploring the complex interplay: gut microbiome, stress, and leptospirosis. Front Microbiol 2024;15:1345684.
    doi: 10.3389/fmicb.2024.1345684pubmed: 38476949google scholar: lookup
  11. Zheng X, He P, Zhong R, Chen G, Xia J, Li C. Weil's Disease in an HIV-Infected Patient: A Case Report and Literature Review. Diagnostics (Basel) 2023 Oct 16;13(20).
    doi: 10.3390/diagnostics13203218pubmed: 37892039google scholar: lookup
  12. Sripattanakul S, Boonchuay K, Prapong T, Wajjwalku W, Katzenmeier G, Haltrich D, Hongprayoon R, Prapong S. Leptospiral Leucine-Rich Repeat Protein-Based Lateral Flow for Assessment of Canine Leptospiral Immunoglobulin G. Trop Med Infect Dis 2022 Dec 10;7(12).
    doi: 10.3390/tropicalmed7120427pubmed: 36548682google scholar: lookup
Subscribe to our newsletter
Join 99,658 horse owners like you who receive our email updates on horse health and nutrition.