Student or educator? Sign up with your school email and get 6 months of Pro free.
CoChat
Sign Up
Cited by 23Urinary Tract Infections ManagementReproductive tract infections researchUrinary Bladder and Prostate Research

The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.

Gardnerella Exposures Alter Bladder Gene Expression and Augment Uropathogenic Escherichia coli Urinary Tract Infection in Mice

Open access
Gilbert, Nicole M., O’Brien, Valerie P., Waller, Chevaughn, Batourina, Ekatherina, Mendelsohn, Cathy Lee, Lewis, Amanda L.·2022·Frontiers in Cellular and Infection Microbiology
DOI 10.3389/fcimb.2022.909799PMC PMC9245024
Open this paper in CoChat — free accountOpen PDF

Abstract

The anaerobic actinobacterium Gardnerella was first isolated from the bladder by suprapubic aspiration more than 50 years ago. Since then, Gardnerella has been increasingly recognized as a common and often abundant member of the female urinary microbiome (urobiome). Some studies even suggest that the presence of Gardnerella is associated with urological disorders in women. We recently reported that inoculation of Gardnerella into the bladders of mice results in urothelial exfoliation. Here, we performed whole bladder RNA-seq in our mouse model to identify additional host pathways involved in the response to Gardnerella bladder exposure. The transcriptional response to Gardnerella reflected the urothelial turnover that is a consequence of exfoliation while also illustrating the activation of pathways involved in inflammation and immunity. Additional timed exposure experiments in mice provided further evidence of a potentially clinically relevant consequence of bladder exposure to Gardnerella—increased susceptibility to subsequent UTI caused by uropathogenic Escherichia coli. Together, these data provide a broader picture of the bladder’s response to Gardnerella and lay the groundwork for future studies examining the impact of Gardnerella on bladder health.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3389/fcimb.2022.909799

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Figures

Figure 1 Gardnerella exposures alter the bladder transcriptome. (A) Schematic of the urinary tract exposure model used for RNA-seq. Female C57BL/6 mice were given intravesical “urinary tract exposures” of either PBS or Gardnerella via transurethral catheterization. Each mouse received two exposures that were administered 12 h apart. Bladders were collected 12 h after the second exposure and processed for RNA-seq. Gardnerella-exposed bladders were compared to PBS-exposed control bladders to identify differentially expressed genes and for gene set enrichment analyses. (B) MA-plot indicates genes that had altered expression in Gardnerella compared to PBS bladders. Red dots denote genes that were significantly differentially expressed after false discovery rate (FDR) correction for multiple comparisons. Genes discussed in the text are indicated by name.
Figure 1 Gardnerella exposures alter the bladder transcriptome. (A) Schematic of the urinary tract exposure model used for RNA-seq. Female C57BL/6 mice were given intravesical “urinary tract exposures” of either PBS or Gardnerella via transurethral catheterization. Each mouse received two exposures that were administered 12 h apart. Bladders were collected 12 h after the second exposure and processed for RNA-seq. Gardnerella-exposed bladders were compared to PBS-exposed control bladders to identify differentially expressed genes and for gene set enrichment analyses. (B) MA-plot indicates genes that had altered expression in Gardnerella compared to PBS bladders. Red dots denote genes that were significantly differentially expressed after false discovery rate (FDR) correction for multiple comparisons. Genes discussed in the text are indicated by name.CC BY · PubMed Central
Figure 2 Gene set enrichment analysis identifies pathways upregulated by Gardnerella exposures. Graphs depict the top 15 gene sets from the Gene Ontology (A, B) and KEGG (C) databases that were significantly enriched in the bladders of mice exposed to Gardnerella relative to PBS controls.
Figure 2 Gene set enrichment analysis identifies pathways upregulated by Gardnerella exposures. Graphs depict the top 15 gene sets from the Gene Ontology (A, B) and KEGG (C) databases that were significantly enriched in the bladders of mice exposed to Gardnerella relative to PBS controls.CC BY · PubMed Central
Figure 3 Gardnerella exposures result in urothelial exfoliation and proliferation. (A) Scanning electron micrographs of bladders collected 12 h after two exposures (the model used for RNA-seq, see Figure 1 schematic) to PBS (panel I) or Gardnerella (II–IV). (I) Intact superficial umbrella cells; (II) umbrella cell with membrane blebbing; (III) region of exfoliation with smaller underlying intermediate cells visible at the luminal interface; (IV) exfoliating umbrella cell marked by an asterisk. Scale bars = 10 μm. (B) Immunofluorescence microscopy of urothelial differentiation markers in bladder sections from mice exposed to PBS (I) or Gardnerella (II and III). Keratin 5 (K5) in green labels, basal cells; P63 in red labels, basal and intermediate cells; and cytokeratin 20 (CK20) in white labels, the apical surface of fully differentiated umbrella cells. Scale bars = 50 μm. (C) Counts of CK20-positive (+) and CK20-negative (−) cells on the urothelial surface, adjacent to the lumen. **** p < 0.001, Fisher’s exact test. The graph was generated by plotting the %CK20 positivity, with each dot representing an individual microscopy image of the ×20 field of view. ** p < 0.01, Mann–Whitney U test. Box plot denotes the 25th and 75th percentiles with a line at the median and whiskers from min to max. (D) Panoramic assembly of bladder sections stained for Ki67 in red. Scale bars = 200 μm. (E) Representative images of immunofluorescence microscopy used for Ki67+ enumeration. (F, G) Tables show the counts of Ki67-positive (+) and Ki67-negative (−) cells of superficial and intermediate cells combined (F) or only superficial cells (G) in each experimental group. *** p < 0.001, **** p < 0.0001, Fisher’s exact test. Graphs were generated by plotting the %Ki67 positivity, with each dot representing an individual microscopy image as in (B). Box plot denotes the 25th and 75th percentiles with a line at the median and whiskers from min to max.
Figure 3 Gardnerella exposures result in urothelial exfoliation and proliferation. (A) Scanning electron micrographs of bladders collected 12 h after two exposures (the model used for RNA-seq, see Figure 1 schematic) to PBS (panel I) or Gardnerella (II–IV). (I) Intact superficial umbrella cells; (II) umbrella cell with membrane blebbing; (III) region of exfoliation with smaller underlying intermediate cells visible at the luminal interface; (IV) exfoliating umbrella cell marked by an asterisk. Scale bars = 10 μm. (B) Immunofluorescence microscopy of urothelial differentiation markers in bladder sections from mice exposed to PBS (I) or Gardnerella (II and III). Keratin 5 (K5) in green labels, basal cells; P63 in red labels, basal and intermediate cells; and cytokeratin 20 (CK20) in white labels, the apical surface of fully differentiated umbrella cells. Scale bars = 50 μm. (C) Counts of CK20-positive (+) and CK20-negative (−) cells on the urothelial surface, adjacent to the lumen. **** p < 0.001, Fisher’s exact test. The graph was generated by plotting the %CK20 positivity, with each dot representing an individual microscopy image of the ×20 field of view. ** p < 0.01, Mann–Whitney U test. Box plot denotes the 25th and 75th percentiles with a line at the median and whiskers from min to max. (D) Panoramic assembly of bladder sections stained for Ki67 in red. Scale bars = 200 μm. (E) Representative images of immunofluorescence microscopy used for Ki67+ enumeration. (F, G) Tables show the counts of Ki67-positive (+) and Ki67-negative (−) cells of superficial and intermediate cells combined (F) or only superficial cells (G) in each experimental group. *** p < 0.001, **** p < 0.0001, Fisher’s exact test. Graphs were generated by plotting the %Ki67 positivity, with each dot representing an individual microscopy image as in (B). Box plot denotes the 25th and 75th percentiles with a line at the median and whiskers from min to max.CC BY · PubMed Central
Figure 4 Preexposure to Gardnerella increases acute UPEC bacteriuria and persistent infection. (A) Schematic of the mouse experiment time course. Dots on the timeline indicate when urine was collected for CFU enumeration. Data are from five independent mouse experiments. (B) SEM images of bladders collected 6 h after UPEC infection from mice preexposed to PBS (top) or Gardnerella (bottom). Asterisks mark exfoliating umbrella cells. Scale bars = 20 μm. Refer to Supplementary Figure S3 for additional bladder SEM images. (C) Acute UPEC titers in urine collected 6 hpi, with each dot representing an individual mouse (107 n = 20 per group; 106 PBS n = 24, Gardnerella n = 25). * p < 0.05, Mann–Whitney U test. Box plot denotes the 25th and 75th percentiles with a line at the median and whiskers from min to max. (D, E) Time course of UPEC bacteriuria after a 107 CFU inoculation. Red symbols indicate mice that had UPEC bacteriuria >104 CFU/ml in each weekly urine sample. (F) UPEC titers in bladder homogenates collected 28 dpi. Each dot represents an individual mouse (n = 10 per group). Red symbols indicate mice that had UPEC bacteriuria >104 CFU/ml in each weekly urine sample. LOD, limit of detection. *** p < 0.001, Mann–Whitney U test. Box plot denotes the 25th and 75th percentiles with a line at the median and whiskers from min to max.
Figure 4 Preexposure to Gardnerella increases acute UPEC bacteriuria and persistent infection. (A) Schematic of the mouse experiment time course. Dots on the timeline indicate when urine was collected for CFU enumeration. Data are from five independent mouse experiments. (B) SEM images of bladders collected 6 h after UPEC infection from mice preexposed to PBS (top) or Gardnerella (bottom). Asterisks mark exfoliating umbrella cells. Scale bars = 20 μm. Refer to Supplementary Figure S3 for additional bladder SEM images. (C) Acute UPEC titers in urine collected 6 hpi, with each dot representing an individual mouse (107 n = 20 per group; 106 PBS n = 24, Gardnerella n = 25). * p < 0.05, Mann–Whitney U test. Box plot denotes the 25th and 75th percentiles with a line at the median and whiskers from min to max. (D, E) Time course of UPEC bacteriuria after a 107 CFU inoculation. Red symbols indicate mice that had UPEC bacteriuria >104 CFU/ml in each weekly urine sample. (F) UPEC titers in bladder homogenates collected 28 dpi. Each dot represents an individual mouse (n = 10 per group). Red symbols indicate mice that had UPEC bacteriuria >104 CFU/ml in each weekly urine sample. LOD, limit of detection. *** p < 0.001, Mann–Whitney U test. Box plot denotes the 25th and 75th percentiles with a line at the median and whiskers from min to max.CC BY · PubMed Central

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Show all 1 references

Research works printed but not linked: 65

  1. Birch, 1981, Ureaplasma Urealyticum in the Upper Urinary Tracts of Renal Allograft Recipients, J. Infect. Dis., 144, 123, 10.1093/infdis/144.2.123 · DOI
  2. Borsodi, 2021, Signaling Pathways Mediating Bradykinin-Induced Contraction in Murine and Human Detrusor Muscle, Front. Med. (Lausanne), 8, 10.3389/fmed.2021.745638 · DOI
  3. Briselden, 1990, Longitudinal Study of the Biotypes of Gardnerella Vaginalis, J. Clin. Microbiol., 28, 2761, 10.1128/jcm.28.12.2761-2764.1990 · DOI
  4. Brown, 2021, Assessing the Concordance Between Urogenital and Vaginal Microbiota: Can Urine Specimens Be Used as a Proxy for Vaginal Samples, Front. Cell Infect. Microbiol., 11, 10.3389/fcimb.2021.671413 · DOI
  5. Cao, 2010, Keratin 6 Expression Correlates to Areas of Squamous Differentiation in Multiple Independent Isolates of As(+3)-Induced Bladder Cancer, J. Appl. Toxicol., 30, 416, 10.1002/jat.1513 · DOI
  6. Cole, 2021, The Pediatric Urobiome in Genitourinary Conditions: A Narrative Review, Pediatr. Nephrol, 10.1007/s00467-021-05274-7 · DOI
  7. Conover, 2015, Establishment and Characterization of UTI and CAUTI in a Mouse Model, J. Vis. Exp., 100, 10.3791/52892 · DOI
  8. Dalghi, 2020, The Urothelium: Life in a Liquid Environment, Physiol. Rev., 100, 1621, 10.1152/physrev.00041.2019 · DOI
  9. Dong, 2015, The Actions of Neurotensin in Rat Bladder Detrusor Contractility, Sci. Rep., 5, 11192, 10.1038/srep11192 · DOI
  10. Fairley, 1983, Unconventional Bacteria in Urinary Tract Disease: Gardnerella Vaginalis, Kidney Int., 23, 862, 10.1038/ki.1983.107 · DOI
  11. Foxman, 2014, Urinary Tract Infection Syndromes: Occurrence, Recurrence, Bacteriology, Risk Factors, and Disease Burden, Infect. Dis. Clin. North Am., 28, 1, 10.1016/j.idc.2013.09.003 · DOI
  12. Gardner, 1954, New Etiologic Agent in Nonspecific Bacterial Vaginitis, Science, 120, 853, 10.1126/science.120.3125.853 · DOI
  13. Gardner, 1955, Haemophilus Vaginalis Vaginitis: A Newly Defined Specific Infection Previously Classified Non-Specific Vaginitis, Am. J. Obstet. Gynecol., 69, 962, 10.1016/0002-9378(55)90095-8 · DOI
  14. Garofalo, 2022, Whole-Person, Urobiome-Centric Therapy for Uncomplicated Urinary Tract Infection, Antibiot. (Basel), 11, 10.3390/antibiotics11020218 · DOI · Paper page
  15. Gatta, 2019, Hyper-Activation of STAT3 Sustains Progression of Non-Papillary Basal-Type Bladder Cancer via FOSL1 Regulome, Cancers (Basel), 11, 10.3390/cancers11091219 · DOI
  16. Gilbert, 1986, Bacteriuria Due to Ureaplasmas and Other Fastidious Organisms During Pregnancy: Prevalence and Significance, Pediatr. Infect. Dis., 5, S239, 10.1097/00006454-198611010-00007 · DOI
  17. Gilbert, 2019, Covert Pathogenesis: Transient Exposures to Microbes as Triggers of Disease, PLoS Pathog., 15, 10.1371/journal.ppat.1007586 · DOI
  18. Gilbert, 2017, Transient Microbiota Exposures Activate Dormant Escherichia Coli Infection in the Bladder and Drive Severe Outcomes of Recurrent Disease, PLoS Pathog., 13, 10.1371/journal.ppat.1006238 · DOI
  19. Gottschick, 2017, The Urinary Microbiota of Men and Women and its Changes in Women During Bacterial Vaginosis and Antibiotic Treatment, Microbiome, 5, 99, 10.1186/s40168-017-0305-3 · DOI
  20. Hannan, 2010, Early Severe Inflammatory Responses to Uropathogenic E. Coli Predispose to Chronic and Recurrent Urinary Tract Infection, PLoS Pathog., 6, 10.1371/journal.ppat.1001042 · DOI
  21. Hillebrand, 2002, Urinary Tract Infections in Pregnant Women With Bacterial Vaginosis, Am. J. Obstet. Gynecol., 186, 916, 10.1067/mob.2002.123987 · DOI
  22. Hilt, 2014, Urine Is Not Sterile: Use of Enhanced Urine Culture Techniques to Detect Resident Bacterial Flora in the Adult Female Bladder, J. Clin. Microbiol., 52, 871, 10.1128/JCM.02876-13 · DOI
  23. Hooton, 1989, Association Between Bacterial Vaginosis and Acute Cystitis in Women Using Diaphragms, Arch. Intern. Med., 149, 1932, 10.1001/archinte.1989.00390090014003 · DOI
  24. Hugenholtz, 2022, Urine and Vaginal Microbiota Compositions of Postmenopausal and Premenopausal Women Differ Regardless of Recurrent Urinary Tract Infection and Renal Transplant Status, Sci. Rep., 12, 2698, 10.1038/s41598-022-06646-1 · DOI
  25. Jacobs, 2017, Microorganisms Identified in the Maternal Bladder: Discovery of the Maternal Bladder Microbiota, AJP Rep., 7, e188, 10.1055/s-0037-1606860 · DOI
  26. Jones, 2021, The Urobiome, Urinary Tract Infections, and the Need for Alternative Therapeutics, Microb. Pathog., 161, 105295, 10.1016/j.micpath.2021.105295 · DOI
  27. Klein, 2020, Urinary Tract Infections: Microbial Pathogenesis, Host-Pathogen Interactions and New Treatment Strategies, Nat. Rev. Microbiol., 18, 211, 10.1038/s41579-020-0324-0 · DOI
  28. Kline, 2016, Gram-Positive Uropathogens, Polymicrobial Urinary Tract Infection, and the Emerging Microbiota of the Urinary Tract, Microbiol. Spectr., 4, 10.1128/microbiolspec.UTI-0012-2012 · DOI
  29. Komesu, 2019, Defining the Relationship Between Vaginal and Urinary Microbiomes, Am. J. Obstet. Gynecol, 222, 154.e1, 10.1016/j.ajog.2019.08.011 · DOI
  30. Krohn, 1989, Comparison of Methods for Diagnosing Bacterial Vaginosis Among Pregnant Women, J. Clin. Microbiol., 27, 1266, 10.1128/jcm.27.6.1266-1271.1989 · DOI
  31. Kudelski, 2021, Enhanced Expression But Decreased Specific Activity of Matrix Metalloproteinase 10 (MMP-10) in Comparison With Matrix Metalloproteinase 3 (MMP-3) in Human Urinary Bladder Carcinoma, J. Clin. Med., 10, 10.3390/jcm10163683 · DOI
  32. Lacerda Mariano, 2020, The Immune Response to Infection in the Bladder, Nat. Rev. Urol, 17, 439, 10.1038/s41585-020-0350-8 · DOI
  33. Lee, 2021, Trefoil Factor 1 Suppresses Epithelial-Mesenchymal Transition Through Inhibition of TGF-Beta Signaling in Gastric Cancer Cells, J. Cancer Prev., 26, 137, 10.15430/JCP.2021.26.2.137 · DOI
  34. Leopold, 1953, Heretofore Undescribed Organism Isolated From the Genitourinary System, U S Armed Forces Med. J., 4, 263
  35. Lewis, 2013, Degradation, Foraging, and Depletion of Mucus Sialoglycans by the Vagina-Adapted Actinobacterium Gardnerella Vaginalis, J. Biol. Chem., 288, 12067, 10.1074/jbc.M113.453654 · DOI
  36. Lin, 2015, Role of Hypoxia Inducible Factor-1alpha (HIF-1alpha) in Innate Defense Against Uropathogenic Escherichia Coli Infection, PloS Pathog., 11, 10.1371/journal.ppat.1004818 · DOI
  37. Lu, 2021, N6-Methyladenosine-Related Non-Coding RNAs Are Potential Prognostic and Immunotherapeutic Responsiveness Biomarkers for Bladder Cancer, EPMA J., 12, 589, 10.1007/s13167-021-00259-w · DOI
  38. Marceau, 1997, The Kinin B1 Receptor: An Inducible G Protein Coupled Receptor, Can. J. Physiol. Pharmacol., 75, 725, 10.1139/y97-049 · DOI
  39. McDonald, 1982, Ureaplasma Urealyticum in Patients With Acute Symptoms of Urinary Tract Infection, J. Urol, 128, 517, 10.1016/S0022-5347(17)53025-6 · DOI
  40. McDowall, 1981, Anaerobic and Other Fastidious Microorganisms in Asymptomatic Bacteriuria in Pregnant Women, J. Infect. Dis., 144, 114, 10.1093/infdis/144.2.114 · DOI
  41. Mcfadyen, 1968, Suprapubic Aspiration of Urine in Pregnancy, Lancet, 1, 1112, 10.1016/S0140-6736(68)90185-2 · DOI
  42. Morrill, 2020, Gardnerella Vaginalis as a Cause of Bacterial Vaginosis: Appraisal of the Evidence From In Vivo Models, Front. Cell Infect. Microbiol., 10, 10.3389/fcimb.2020.00168 · DOI
  43. Mulvey, 2001, Establishment of a Persistent Escherichia Coli Reservoir During the Acute Phase of a Bladder Infection, Infect. Immun., 69, 4572, 10.1128/IAI.69.7.4572-4579.2001 · DOI
  44. Mulvey, 2000, Bad Bugs and Beleaguered Bladders: Interplay Between Uropathogenic Escherichia Coli and Innate Host Defenses, Proc. Natl. Acad. Sci. U.S.A., 97, 8829, 10.1073/pnas.97.16.8829 · DOI
  45. Mysorekar, 2006, Mechanisms of Uropathogenic Escherichia Coli Persistence and Eradication From the Urinary Tract, Proc. Natl. Acad. Sci. U.S.A., 103, 14170, 10.1073/pnas.0602136103 · DOI
  46. Nicolle, 1982, The Association of Urinary Tract Infection With Sexual Intercourse, J. Infect. Dis., 146, 579, 10.1093/infdis/146.5.579 · DOI
  47. O'Brien, 2020, Recurrent Escherichia Coli Urinary Tract Infection Triggered by Gardnerella Vaginalis Bladder Exposure in Mice, J. Vis. Exp, 2020, 10.3791/61967 · DOI
  48. Pearce, 2014, The Female Urinary Microbiome: A Comparison of Women With and Without Urgency Urinary Incontinence, MBio, 5, e01283, 10.1128/mBio.01283-14 · DOI
  49. Pearce, 2015, The Female Urinary Microbiome in Urgency Urinary Incontinence, Am. J. Obstet. Gynecol., 213, 10.1016/j.ajog.2015.07.009 · DOI
  50. Price, 2020, The Urobiome of Continent Adult Women: A Cross-Sectional Study, BJOG, 127, 193, 10.1111/1471-0528.15920 · DOI
  51. Putonti, 2021, Genome Investigation of Urinary Gardnerella Strains and Their Relationship to Isolates of the Vaginal Microbiota, mSphere, 6, 10.1128/mSphere.00154-21 · DOI
  52. Ravel, 2011, Vaginal Microbiome of Reproductive-Age Women, Proc. Natl. Acad. Sci. U.S.A., 4680, 10.1073/pnas.1002611107 · DOI · Paper page
  53. Schwartz, 2015, Uropathogenic Escherichia Coli Superinfection Enhances the Severity of Mouse Bladder Infection, PLoS Pathog., 11, 10.1371/journal.ppat.1004599 · DOI
  54. Schwebke, 2014, Role of Gardnerella Vaginalis in the Pathogenesis of Bacterial Vaginosis: A Conceptual Model, J. Infect. Dis., 210, 338, 10.1093/infdis/jiu089 · DOI
  55. Somji, 2011, Comparison of Expression Patterns of Keratin 6, 7, 16, 17, and 19 Within Multiple Independent Isolates of As(+3)- and Cd (+2)-Induced Bladder Cancer : Keratin 6, 7, 16, 17, and 19 in Bladder Cancer, Cell Biol. Toxicol., 27, 381, 10.1007/s10565-010-9169-z · DOI
  56. Sumati, 2009, Association of Urinary Tract Infection in Women With Bacterial Vaginosis, J. Glob. Infect. Dis., 1, 151, 10.4103/0974-777X.56254 · DOI
  57. Tate, 2021, Pparg Signaling Controls Bladder Cancer Subtype and Immune Exclusion, Nat. Commun., 12, 6160, 10.1038/s41467-021-26421-6 · DOI
  58. Tessarz, 2008, The TREM-1/DAP12 Pathway, Immunol. Lett., 116, 111, 10.1016/j.imlet.2007.11.021 · DOI
  59. Vaneechoutte, 2019, Emended Description of Gardnerella Vaginalis and Description of Gardnerella Leopoldii Sp. Nov., Gardnerella Piotii Sp. Nov. And Gardnerella Swidsinskii Sp. Nov., With Delineation of 13 Genomic Species Within the Genus Gardnerella, Int. J. Syst. Evol. Microbiol., 69, 679, 10.1099/ijsem.0.003200 · DOI
  60. Veranic, 2004, What Determines Differentiation of Urothelial Umbrella Cells, Eur. J. Cell Biol., 83, 27, 10.1078/0171-9335-00351 · DOI
  61. Wright, 2005, Uropathogenic Escherichia Coli Flagella Aid in Efficient Urinary Tract Colonization, Infect. Immun., 73, 7657, 10.1128/IAI.73.11.7657-7668.2005 · DOI
  62. Wu, 2021, Analysis of the Expression and Prognostic Value of Annexin Family Proteins in Bladder Cancer, Front. Genet., 12, 10.3389/fgene.2021.731625 · DOI
  63. Xu, 1999, Multiorgan Autonomic Dysfunction in Mice Lacking the Beta2 and the Beta4 Subunits of Neuronal Nicotinic Acetylcholine Receptors, J. Neurosci., 19, 9298, 10.1523/JNEUROSCI.19-21-09298.1999 · DOI
  64. Zhang, 2021, Gene Regulatory Networks Analysis of Muscle-Invasive Bladder Cancer Subtypes Using Differential Graphical Model, BMC Genomics, 22, 863, 10.1186/s12864-021-08113-z · DOI
  65. Zinnemann, 1963, The Taxonomic Position of “Haemophilus vaginalis” (Corynebacterium vaginale), J Pathol Bacteriol, 85, 213, 10.1002/path.1700850120 · DOI

Cited by

Metadata

Authors
Gilbert, N. M., O’Brien, V. P., Waller, C., Batourina, E., Mendelsohn, C. L., & Lewis, A. L.
Affiliations
  • Washington University in St. Louis (US)
  • Columbia University Irving Medical Center (US)
  • University of California San Diego (US)
Corresponding author
Gilbert, Nicole M.
ORCID
Venue
Frontiers in Cellular and Infection Microbiology
Publisher
Frontiers Media SA
Published
2022-06-16
Volume
12
Pages
909799-909799
ISSN
2235-2988 (ISSN-L)
DOI
10.3389/fcimb.2022.909799
PMC
PMC9245024
OpenAlex
W4283027576
Cited by
23
References
1
Citations by year
2026: 7 · 2025: 6 · 2024: 5 · 2023: 4 · 2022: 1
FWCI
2.82
Type
journal article
Language
en
Open access
Licence
Locations
  • Frontiers in Cellular and Infection Microbiology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Digital Commons@Becker (Washington University School of Medicine) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Science Foundation (1143954)
  • American Heart Association
  • National Institutes of Health (DGE-1143954, CA013696, DK104309)
  • Washington University School of Medicine in St. Louis
  • Center for Cellular Imaging, Washington University
  • National Cancer Institute (P30CA013696)
  • National Institute of Allergy and Infectious Diseases (R21AI152049, AI152049, AI114635, R01AI114635)
  • National Institute of Diabetes and Digestive and Kidney Diseases (DK092586, R03DK132442, K01DK110225, R21DK092586, DK110225, U54DK104309)
  • National Center for Research Resources (C06-RR-015502)
Topics
  • Health Sciences › Medicine › Urology › Urinary Tract Infections Management
  • Life Sciences › Immunology and Microbiology › Microbiology › Reproductive tract infections research
  • Health Sciences › Medicine › Urology › Urinary Bladder and Prostate Research
Keywords
Gardnerella, uropathogenic Escherichia coli, urinary tract infection, urinary microbiome, inflammation, host immune response, mouse model
MeSH terms
Animals, Urinary Bladder, Escherichia coli Infections, Female, Humans, Urinary Tract Infections, Gene Expression, Gardnerella, Mice, Uropathogenic Escherichia coli

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Data sources

Bibliographic data: Semantic Scholar, OpenAlex, Crossref.

Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.