1887

Microbial Genomics logo

Volume 8, Issue 7

Novel internalin P homologs in Open Access

Abstract

() is a bacterial pathogen that causes listeriosis in immunocompromised individuals, particularly pregnant women. Several virulence factors support the intracellular lifecycle of and facilitate cell-to-cell spread, allowing it to occupy multiple niches within the host and cross-protective barriers, including the placenta. One family of virulence factors, internalins, contributes to pathogenicity by inducing specific uptake and conferring tissue tropism. Over 25 internalins have been identified thus far, but only a few have been extensively studied. Internalins contain leucine-rich repeat (LRR) domains that enable protein-protein interactions, allowing to bind host proteins. Notably, other species express internalins but cannot colonize human hosts, prompting questions regarding the evolution of internalins within the genus . Internalin P (InlP) promotes placental colonization through interaction with the host protein afadin. Although prior studies of InlP have begun to elucidate its role in pathogenesis, there remains a lack of information regarding homologs in other species. Here, we have used a computational evolutionary approach to identify InlP homologs in additional species. We found that () and () encode InlP homologs. We also found InlP-like homologs in and the recently identified species . All newly identified homologs lack the full-length LRR6 and LRR7 domains found in ’s InlP. These findings are informative regarding the evolution of one key virulence factor, InlP, and serve as a springboard for future evolutionary studies of pathogenesis as well as mechanistic studies of internalins.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): inlp , internalin , Listeria , molecular evolution , phylogeny and placenta
© 2022 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000828
2022-07-29
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/mgen/8/7/mgen000828.html?itemId=/content/journal/mgen/10.1099/mgen.0.000828&mimeType=html&fmt=ahah

References

  1. Goldenberg RL, Culhane JF, Iams JD, Romero R. Epidemiology and causes of preterm birth. Lancet 2008; 371:75–84 [View Article] [PubMed]
     [Google Scholar]
  2. Lowe DE, Robbins JR, Bakardjiev AI. Animal and human tissue models of vertical Listeria monocytogenes transmission and implications for other pregnancy-associated infections. Infect Immun 2018; 86:e00801-17 [View Article] [PubMed]
     [Google Scholar]
  3. Morrison HA, Lowe D, Robbins JR, Bakardjiev AI. In vivo virulence characterization of pregnancy-associated Listeria monocytogenes Infections. Infect Immun 2018; 86:e00397-18 [View Article] [PubMed]
     [Google Scholar]
  4. Orsi RH, Wiedmann M. Characteristics and distribution of Listeria spp., including Listeria species newly described since 2009. Appl Microbiol Biotechnol 2016; 100:5273–5287 [View Article] [PubMed]
     [Google Scholar]
  5. Vázquez-Boland JA, Kuhn M, Berche P, Chakraborty T, Domínguez-Bernal G et al. Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 2001; 14:584–640 [View Article] [PubMed]
     [Google Scholar]
  6. Matereke LT, Okoh AI. Listeria monocytogenes virulence, antimicrobial resistance and environmental persistence: a review. Pathogens 2020; 9:E528 [View Article] [PubMed]
     [Google Scholar]
  7. Listeria (Listeriosis). https://www.cdc.gov/listeria/index.html
  8. Listeria During Pregnancy. https://americanpregnancy.org/healthy-pregnancy/pregnancy-concerns/listeria-during-pregnancy
  9. Lecuit M, Nelson DM, Smith SD, Khun H, Huerre M et al. Targeting and crossing of the human maternofetal barrier by Listeria monocytogenes: role of internalin interaction with trophoblast E-cadherin. Proc Natl Acad Sci U S A 2004; 101:6152–6157 [View Article] [PubMed]
     [Google Scholar]
  10. Le Monnier A, Join-Lambert OF, Jaubert F, Berche P, Kayal S. Invasion of the placenta during murine listeriosis. Infect Immun 2006; 74:663–672 [View Article] [PubMed]
     [Google Scholar]
  11. Le Monnier A, Autret N, Join-Lambert OF, Jaubert F, Charbit A et al. ActA is required for crossing of the fetoplacental barrier by Listeria monocytogenes. Infect Immun 2007; 75:950–957 [View Article] [PubMed]
     [Google Scholar]
  12. Faralla C, Rizzuto GA, Lowe DE, Kim B, Cooke C et al. Inlp, a new virulence factor with strong placental tropism. Infect Immun 2016; 84:3584–3596 [View Article] [PubMed]
     [Google Scholar]
  13. Faralla C, Bastounis EE, Ortega FE, Light SH, Rizzuto G et al. Listeria monocytogenes InlP interacts with afadin and facilitates basement membrane crossing. PLoS Pathog 2018; 14:e1007094 [View Article] [PubMed]
     [Google Scholar]
  14. Ireton K, Mortuza R, Gyanwali GC, Gianfelice A, Hussain M. Role of internalin proteins in the pathogenesis of Listeria monocytogenes. Mol Microbiol 2021; 116:1407–1419 [View Article] [PubMed]
     [Google Scholar]
  15. Kobe B, Kajava AV. The leucine-rich repeat as a protein recognition motif. Curr Opin Struct Biol 2001; 11:725–732 [View Article] [PubMed]
     [Google Scholar]
  16. Kobe B, Deisenhofer J. The leucine-rich repeat: a versatile binding motif. Trends Biochem Sci 1994; 19:415–421 [View Article] [PubMed]
     [Google Scholar]
  17. Hain T, Chatterjee SS, Ghai R, Kuenne CT, Billion A et al. Pathogenomics of Listeria spp. Int J Med Microbiol 2007; 297:541–557 [View Article] [PubMed]
     [Google Scholar]
  18. Glaser P, Frangeul L, Buchrieser C, Rusniok C, Amend A et al. Comparative genomics of Listeria species. Science 2001; 294:849–852 [View Article] [PubMed]
     [Google Scholar]
  19. Gouin E, Mengaud J, Cossart P. The virulence gene cluster of Listeria monocytogenes is also present in Listeria ivanovii, an animal pathogen, and Listeria seeligeri, a nonpathogenic species. Infect Immun 1994; 62:3550–3553 [View Article] [PubMed]
     [Google Scholar]
  20. Burke JT, Chen SZ, Sosinski LM, Johnston JB, Ravi J. MolEvolvR: A web-app for characterizing proteins using molecular evolution and phylogeny. Genomics 2022 [View Article]
     [Google Scholar]
  21. O’Leary NA et al. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res 2016; 44:D733–D745
     [Google Scholar]
  22. Karp PD, Billington R, Caspi R, Fulcher CA, Latendresse M et al. The BioCyc collection of microbial genomes and metabolic pathways. Brief Bioinform 2019; 20:1085–1093 [View Article] [PubMed]
     [Google Scholar]
  23. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 2011; 7:539 [View Article] [PubMed]
     [Google Scholar]
  24. Stothard P. The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences. Biotechniques 2000; 28:1102–1104 [View Article] [PubMed]
     [Google Scholar]
  25. Campanella JJ, Bitincka L, Smalley J. MatGAT: an application that generates similarity/identity matrices using protein or DNA sequences. BMC Bioinformatics 2003; 4:29 [View Article] [PubMed]
     [Google Scholar]
  26. Lassmann T, Sonnhammer ELL. Kalign--an accurate and fast multiple sequence alignment algorithm. BMC Bioinformatics 2005; 6:298 [View Article] [PubMed]
     [Google Scholar]
  27. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ. Jalview Version 2--a multiple sequence alignment editor and analysis workbench. Bioinformatics 2009; 25:1189–1191 [View Article] [PubMed]
     [Google Scholar]
  28. Yu G, Smith DK, Zhu H, Guan Y, Lam T. T. ggtree: an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol 2017; 8:28–36
     [Google Scholar]
  29. Paradis E, Schliep K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 2019; 35:526–528 [View Article] [PubMed]
     [Google Scholar]
  30. Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G et al. SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res 2018; 46:W296–W303 [View Article] [PubMed]
     [Google Scholar]
  31. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN et al. The Protein data bank. Nucleic Acids Res 2000; 28:235–242 [View Article] [PubMed]
     [Google Scholar]
  32. Pettersen EF, Goddard TD, Huang CC, Meng EC, Couch GS et al. UCSF ChimeraX: Structure visualization for researchers, educators, and developers. Protein Sci 2021; 30:70–82 [View Article] [PubMed]
     [Google Scholar]
  33. Boerlin P, Rocourt J, Grimont F, Grimont PAD, Jacquet C et al. Listeria ivanovii subsp. londoniensis subsp. nov. Int J Syst Bacteriol 1992; 42:69–73 [View Article]
     [Google Scholar]
  34. Hupfeld M, Trasanidou D, Ramazzini L, Klumpp J, Loessner MJ et al. A functional type II-A CRISPR-Cas system from Listeria enables efficient genome editing of large non-integrating bacteriophage. Nucleic Acids Res 2018; 46:6920–6933 [View Article] [PubMed]
     [Google Scholar]
  35. Rocourt J, Hof H, Schrettenbrunner A, Malinverni R, Bille J. Acute purulent Listeria seelingeri meningitis in an immunocompetent adult. Schweiz Med Wochenschr 1986; 116:248–251 [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000828
Loading
Novel internalin P homologs in Listeria
M Gen 8, 000828 (2022); https://doi.org/10.1099/mgen.0.000828
/content/journal/mgen/10.1099/mgen.0.000828
/content/journal/mgen/10.1099/mgen.0.000828
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error