Hunter W Kuhn, Madeleine R Smither, Rachel J Jin, Christina A Collins, Hongming Ma, Jason Sina, Joseph P Gaut, Michael S Diamond, David A Hunstad
{"title":"LDL受体介导的大肠杆菌α-溶血素内吞作用介导肾上皮毒性。","authors":"Hunter W Kuhn, Madeleine R Smither, Rachel J Jin, Christina A Collins, Hongming Ma, Jason Sina, Joseph P Gaut, Michael S Diamond, David A Hunstad","doi":"10.1073/pnas.2505482122","DOIUrl":null,"url":null,"abstract":"<p><p>The α-hemolysin (HlyA) of uropathogenic <i>Escherichia coli</i> (UPEC) is a pore-forming toxin (PFT) that is thought to function by disrupting the host cell plasma membrane. Although CD18 (LFA-1) has been implicated as a receptor on myeloid cells, the mechanisms underlying HlyA cytotoxicity to epithelial cells are poorly defined. Here, we show that HlyA secretion by UPEC markedly intensifies renal tubular epithelial injury in a murine model of ascending pyelonephritis. A CRISPR-Cas9 loss-of-function screen in renal collecting duct cells revealed an unexpected requirement for clathrin-mediated endocytosis in HlyA-induced cytotoxicity. Following internalization, HlyA triggered lysosomal permeabilization, resulting in protease leakage, cytoplasmic acidification, and mitochondrial impairment, culminating in rapid epithelial cell death-a pathway distinct from canonical membrane-disrupting mechanisms of other PFTs. Moreover, we identify the low-density lipoprotein receptor (LDLR) as a critical epithelial receptor for HlyA; genetic ablation or competitive inhibition of the HlyA-LDLR interaction fully abrogated cytotoxicity. Our findings detail a paradigm for HlyA function in which epithelial toxicity relies on LDLR-mediated endocytic uptake rather than plasma membrane poration. These mechanistic insights illuminate potential therapeutic strategies to attenuate HlyA-mediated tissue damage during UPEC infections.</p>","PeriodicalId":20548,"journal":{"name":"Proceedings of the National Academy of Sciences of the United States of America","volume":"122 24","pages":"e2505482122"},"PeriodicalIF":9.1000,"publicationDate":"2025-06-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12184420/pdf/","citationCount":"0","resultStr":"{\"title\":\"LDL receptor-mediated endocytosis of <i>Escherichia coli</i> α-hemolysin mediates renal epithelial toxicity.\",\"authors\":\"Hunter W Kuhn, Madeleine R Smither, Rachel J Jin, Christina A Collins, Hongming Ma, Jason Sina, Joseph P Gaut, Michael S Diamond, David A Hunstad\",\"doi\":\"10.1073/pnas.2505482122\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>The α-hemolysin (HlyA) of uropathogenic <i>Escherichia coli</i> (UPEC) is a pore-forming toxin (PFT) that is thought to function by disrupting the host cell plasma membrane. Although CD18 (LFA-1) has been implicated as a receptor on myeloid cells, the mechanisms underlying HlyA cytotoxicity to epithelial cells are poorly defined. Here, we show that HlyA secretion by UPEC markedly intensifies renal tubular epithelial injury in a murine model of ascending pyelonephritis. A CRISPR-Cas9 loss-of-function screen in renal collecting duct cells revealed an unexpected requirement for clathrin-mediated endocytosis in HlyA-induced cytotoxicity. Following internalization, HlyA triggered lysosomal permeabilization, resulting in protease leakage, cytoplasmic acidification, and mitochondrial impairment, culminating in rapid epithelial cell death-a pathway distinct from canonical membrane-disrupting mechanisms of other PFTs. Moreover, we identify the low-density lipoprotein receptor (LDLR) as a critical epithelial receptor for HlyA; genetic ablation or competitive inhibition of the HlyA-LDLR interaction fully abrogated cytotoxicity. Our findings detail a paradigm for HlyA function in which epithelial toxicity relies on LDLR-mediated endocytic uptake rather than plasma membrane poration. These mechanistic insights illuminate potential therapeutic strategies to attenuate HlyA-mediated tissue damage during UPEC infections.</p>\",\"PeriodicalId\":20548,\"journal\":{\"name\":\"Proceedings of the National Academy of Sciences of the United States of America\",\"volume\":\"122 24\",\"pages\":\"e2505482122\"},\"PeriodicalIF\":9.1000,\"publicationDate\":\"2025-06-17\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12184420/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Proceedings of the National Academy of Sciences of the United States of America\",\"FirstCategoryId\":\"103\",\"ListUrlMain\":\"https://doi.org/10.1073/pnas.2505482122\",\"RegionNum\":1,\"RegionCategory\":\"综合性期刊\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2025/6/12 0:00:00\",\"PubModel\":\"Epub\",\"JCR\":\"Q1\",\"JCRName\":\"MULTIDISCIPLINARY SCIENCES\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Proceedings of the National Academy of Sciences of the United States of America","FirstCategoryId":"103","ListUrlMain":"https://doi.org/10.1073/pnas.2505482122","RegionNum":1,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2025/6/12 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"MULTIDISCIPLINARY SCIENCES","Score":null,"Total":0}
The α-hemolysin (HlyA) of uropathogenic Escherichia coli (UPEC) is a pore-forming toxin (PFT) that is thought to function by disrupting the host cell plasma membrane. Although CD18 (LFA-1) has been implicated as a receptor on myeloid cells, the mechanisms underlying HlyA cytotoxicity to epithelial cells are poorly defined. Here, we show that HlyA secretion by UPEC markedly intensifies renal tubular epithelial injury in a murine model of ascending pyelonephritis. A CRISPR-Cas9 loss-of-function screen in renal collecting duct cells revealed an unexpected requirement for clathrin-mediated endocytosis in HlyA-induced cytotoxicity. Following internalization, HlyA triggered lysosomal permeabilization, resulting in protease leakage, cytoplasmic acidification, and mitochondrial impairment, culminating in rapid epithelial cell death-a pathway distinct from canonical membrane-disrupting mechanisms of other PFTs. Moreover, we identify the low-density lipoprotein receptor (LDLR) as a critical epithelial receptor for HlyA; genetic ablation or competitive inhibition of the HlyA-LDLR interaction fully abrogated cytotoxicity. Our findings detail a paradigm for HlyA function in which epithelial toxicity relies on LDLR-mediated endocytic uptake rather than plasma membrane poration. These mechanistic insights illuminate potential therapeutic strategies to attenuate HlyA-mediated tissue damage during UPEC infections.
期刊介绍:
The Proceedings of the National Academy of Sciences (PNAS), a peer-reviewed journal of the National Academy of Sciences (NAS), serves as an authoritative source for high-impact, original research across the biological, physical, and social sciences. With a global scope, the journal welcomes submissions from researchers worldwide, making it an inclusive platform for advancing scientific knowledge.