HIV-associated penile anaerobes disrupt epithelial barrier integrity

April 16, 2025 by
HIV-associated penile anaerobes disrupt 
epithelial barrier integrity
Aber Maurine
Lane B. Buchanan1, Zhongtian Shao1, Ronald M. Galiwango2,3, Shirley Constable1, David Zuanazzi1, Victoria Menya Biribawa4, Henry Rogers Ssemunywa4, Annemarie Namuniina4, Brenda Okech4, Gabriella Edfeldt5,6, Annelie Tjernlund5, Aaron A. R. Tobian7, Daniel E. Park8, Tony Pham8, Maliha Aziz8, Juan E. Salazar8, Sydney Nelson8, Cindy M. Liu8, Rupert Kaul3, Jessica L. Prodger1,9*

Affiliations:

1Department of Microbiology and Immunology, Schulich School of Medicine and Dentistry, Western University, London, Ontario, Canada
2Rakai Health Sciences Program, Rakai, Uganda
3Department of Medicine, University Health Network, Toronto, Ontario, Canada
4Uganda Virus Research Institute, International AIDS Vaccine Initiative, Entebbe, Uganda
5Department of Medicine Solna, Karolinska Institutet, Stockholm, Sweden
6Department of Microbiology, Tumor and Cell Biology, Karolinska Institutet, Stockholm, Sweden
7Department of Pathology, Johns Hopkins University School of Medicine, Johns Hopkins University, Baltimore, Maryland, United States of America
8Department of Environmental and Occupational Health, Milken Institute School of Public Health, George Washington University, Washington, D.C., United States of America
9Department of Epidemiology and Biostatistics, Schulich School of Medicine and Dentistry, Western University, London, Ontario, Canada

*Corresponding author


Background 

Abstract Specific anaerobic taxa within the penile microbiome—the Bacteria Associated with Seroconversion, Inflammation and Immune Cells (BASIC) species—enhance HIV-1 susceptibility, in part by recruiting susceptible cells to the inner foreskin. However, their effect on epithelial barrier integrity has not been described. Using foreskin tissues and penile swabs from 116 males undergoing voluntary medical male circum cision, we assessed the relationship between BASIC species and foreskin epithe lial thickness, junction protein expression, and cellular proliferation. The absolute abundance of BASIC species was associated with reduced tissue expression of the epithelial junction proteins claudin-1 and E-cadherin, and with elevated soluble E-cadherin in penile secretions, suggesting proteolytic cleavage. These effects were not seen in participants with a high abundance of control taxa without high levels of BASIC species. The BASIC species Prevotella bivia, but not Peptostreptococcus anaerobius or Dialister micraerophilus, was shown to directly degrade recombinant human E-cadherin and to increase the release of soluble E-cadherin from foreskin epithelial cells in vitro. In vivo BASIC species absolute abundance was also linked to a thicker nucleated epithelium and increased keratinocyte proliferation, with no change in stratum corneum thickness. Therefore, BASIC species may enhance penile HIV susceptibility by directly disrupting epithelial integrity, in addition to previously described target cell recruitment. 


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