Research Overview

The Lencer laboratory studies the cell and molecular biology of vesicular transport in polarized epithelial cells and regulation of ion transport in the intestine. These studies relate to how intestinal epithelial cells interact with the luminal and sub-epithelial micro-environment, and to the biology of bacterial pathogenesis and host defense at mucosal surfaces.

The lab has discovered how some enteric bacterial toxins breech the intestinal epithelial barrier and enter host epithelial cells to cause disease. These toxins hijack the cellular and molecular mechanisms of retrograde membrane transport to move from the luminal cell surface into the endoplasmic reticulum (ER) of affected cells, the total reverse of protein biosynthesis.

In another project, the lab studies the cell and molecular biology of the MHC Class I-like IgG receptor FcRn. FcRn transports IgG across mucosal surfaces where it may function in immune surveillance and host defense.

In a third area of interest, the lab aims to understand the mechanisms and regulation of intestinal Cl- secretion, the initial ion transport event in secretory diarrhea.

The Lencer Lab is also conducting research projects on oral and pulmonary delivery of protein therapeutics and on clotrimazole for the treatment of inflammatory bowel disease.

Research Background

Wayne Lencer received his MD degree from Boston University School of Medicine. He completed an internship and residency at Boston City Hospital, a clinical and research fellowship at Harvard Medical School/Boston Children's Hospital and a fellowship in cell biology and biophysics at Massachusetts General Hospital, HMS and University of California San Francisco.

Dr. Lencer is the recipient of the Samuel J. Meltzer Basic Research Award from the American Digestive Health Foundation and a Harvard Medical School Teaching Award.

Education

Medical School

Boston University School of Medicine
1977 Boston MA

Internship

Boston City Hospital
1978 Boston MA

Residency

Boston City Hospital
1980 Boston MA

Fellowship

Boston Children's Hospital
1987 Boston MA

Publications

  1. SLO co-opts host cell glycosphingolipids to access cholesterol-rich lipid rafts for enhanced pore formation and cytotoxicity. mBio. 2025 Jan 21; e0377724. View Abstract
  2. Presentation of the 2024 AGA Distinguished Achievement Award in Basic Science to Jerrold R. Turner, MD, PhD, AGAF. Gastroenterology. 2024 Jun 07. View Abstract
  3. Bacterial Sphingolipids Exacerbate Colitis by Inhibiting ILC3-derived IL-22 Production. Cell Mol Gastroenterol Hepatol. 2024; 18(2):101350. View Abstract
  4. IRE1a recognizes a structural motif in cholera toxin to activate an unfolded protein response. J Cell Biol. 2024 07 01; 223(7). View Abstract
  5. Protocol for measuring transcytosis and recycling of IgG in intestinal epithelial Caco-2 cells and primary human intestinal organoids. STAR Protoc. 2023 05 25; 4(2):102335. View Abstract
  6. The epithelial-specific ER stress sensor ERN2/IRE1ß enables host-microbiota crosstalk to affect colon goblet cell development. J Clin Invest. 2022 09 01; 132(17). View Abstract
  7. Structural basis for acyl chain control over glycosphingolipid sorting and vesicular trafficking. Cell Rep. 2022 07 12; 40(2):111063. View Abstract
  8. Depletion of the apical endosome in response to viruses and bacterial toxins provides cell-autonomous host defense at mucosal surfaces. Cell Host Microbe. 2022 02 09; 30(2):216-231.e5. View Abstract
  9. Intestinal goblet cells sample and deliver lumenal antigens by regulated endocytic uptake and transcytosis. Elife. 2021 10 22; 10. View Abstract
  10. Cholera Toxin as a Probe for Membrane Biology. Toxins (Basel). 2021 08 03; 13(8). View Abstract
  11. Small-molecule modulators of INAVA cytosolic condensate and cell-cell junction assemblies. J Cell Biol. 2021 09 06; 220(9). View Abstract
  12. Ceramide structure dictates glycosphingolipid nanodomain assembly and function. Nat Commun. 2021 06 16; 12(1):3675. View Abstract
  13. Evolution and function of the epithelial cell-specific ER stress sensor IRE1ß. Mucosal Immunol. 2021 11; 14(6):1235-1246. View Abstract
  14. Extracellular cyclic dinucleotides induce polarized responses in barrier epithelial cells by adenosine signaling. Proc Natl Acad Sci U S A. 2020 11 03; 117(44):27502-27508. View Abstract
  15. A Quantitative Single-cell Flow Cytometry Assay for Retrograde MembraneTrafficking Using Engineered Cholera Toxin. Bio Protoc. 2020 Aug 05; 10(15):e3707. View Abstract
  16. Everything Illuminated-Clostridium perfringens ß-toxin. Cell Host Microbe. 2020 07 08; 28(1):5-6. View Abstract
  17. Structured clustering of the glycosphingolipid GM1 is required for membrane curvature induced by cholera toxin. Proc Natl Acad Sci U S A. 2020 06 30; 117(26):14978-14986. View Abstract
  18. Conjugation of peptides to short-acyl-chain ceramides for delivery across mucosal cell barriers. Bioorg Med Chem Lett. 2020 04 15; 30(8):127014. View Abstract
  19. IRE1ß negatively regulates IRE1a signaling in response to endoplasmic reticulum stress. J Cell Biol. 2020 Feb 03; 219(2). View Abstract
  20. A quantitative single-cell assay for retrograde membrane traffic enables rapid detection of defects in cellular organization. Mol Biol Cell. 2020 03 19; 31(7):511-519. View Abstract
  21. A modified cholera toxin B subunit containing an ER retention motif enhances colon epithelial repair via an unfolded protein response. FASEB J. 2019 12; 33(12):13527-13545. View Abstract
  22. INAVA-ARNO complexes bridge mucosal barrier function with inflammatory signaling. Elife. 2018 10 25; 7. View Abstract
  23. Transcytosis Assay for Transport of Glycosphingolipids across MDCK-II Cells. Bio Protoc. 2018 10 20; 8(20). View Abstract
  24. Transcytosis Assay for Transport of Glycosphingolipids across MDCK-II Cells. Bio Protoc. 2018 Oct 20; 8(20):e2018. View Abstract
  25. CRISPR Screen Reveals that EHEC's T3SS and Shiga Toxin Rely on Shared Host Factors for Infection. mBio. 2018 06 19; 9(3). View Abstract
  26. Mucosal absorption of therapeutic peptides by harnessing the endogenous sorting of glycosphingolipids. Elife. 2018 05 31; 7. View Abstract
  27. Advances in Evaluation of Chronic Diarrhea in Infants. Gastroenterology. 2018 Jun; 154(8):2045-2059.e6. View Abstract
  28. Retraction Notice to: The Unfolded Protein Response Element IRE1a Senses Bacterial Proteins Invading the ER to Activate RIG-I and Innate Immune Signaling. Cell Host Microbe. 2018 04 11; 23(4):571. View Abstract
  29. Membrane Transport across Polarized Epithelia. Cold Spring Harb Perspect Biol. 2017 Sep 01; 9(9). View Abstract
  30. Hepatic FcRn regulates albumin homeostasis and susceptibility to liver injury. Proc Natl Acad Sci U S A. 2017 04 04; 114(14):E2862-E2871. View Abstract
  31. A targeted RNAi screen identifies factors affecting diverse stages of receptor-mediated transcytosis. J Cell Biol. 2017 02; 216(2):511-525. View Abstract
  32. Aquaporin-3 mediates hydrogen peroxide-dependent responses to environmental stress in colonic epithelia. Proc Natl Acad Sci U S A. 2017 01 17; 114(3):568-573. View Abstract
  33. Glycolipid Crosslinking Is Required for Cholera Toxin to Partition Into and Stabilize Ordered Domains. Biophys J. 2016 Dec 20; 111(12):2547-2550. View Abstract
  34. CellMapper: rapid and accurate inference of gene expression in difficult-to-isolate cell types. Genome Biol. 2016 09 29; 17(1):201. View Abstract
  35. Opening CFTR in the Intestine: Flushing on Demand. Cell Mol Gastroenterol Hepatol. 2016 May; 2(3):256. View Abstract
  36. Microbial sphingomyelinase induces RhoA-mediated reorganization of the apical brush border membrane and is protective against invasion. Mol Biol Cell. 2016 Apr 01; 27(7):1120-30. View Abstract
  37. Electrophysiological Studies into the Safety of the Anti-diarrheal Drug Clotrimazole during Oral Rehydration Therapy. PLoS Negl Trop Dis. 2015 Sep; 9(9):e0004098. View Abstract
  38. Congenital chloride-losing diarrhea in a Mexican child with the novel homozygous SLC26A3 mutation G393W. Front Physiol. 2015; 6:179. View Abstract
  39. Innate immunity at mucosal surfaces: the IRE1-RIDD-RIG-I pathway. Trends Immunol. 2015 Jul; 36(7):401-9. View Abstract
  40. FcRn: The Architect Behind the Immune and Nonimmune Functions of IgG and Albumin. J Immunol. 2015 May 15; 194(10):4595-603. View Abstract
  41. Microtubule motors power plasma membrane tubulation in clathrin-independent endocytosis. Traffic. 2015 Jun; 16(6):572-90. View Abstract
  42. 4-Phenylbutyrate attenuates the ER stress response and cyclic AMP accumulation in DYT1 dystonia cell models. PLoS One. 2014; 9(11):e110086. View Abstract
  43. Remodeling of the intestinal brush border underlies adhesion and virulence of an enteric pathogen. mBio. 2014 Aug 19; 5(4). View Abstract
  44. Mechanism for adhesion G protein-coupled receptor GPR56-mediated RhoA activation induced by collagen III stimulation. PLoS One. 2014; 9(6):e100043. View Abstract
  45. Unsaturated glycoceramides as molecular carriers for mucosal drug delivery of GLP-1. J Control Release. 2014 Feb 10; 175:72-8. View Abstract
  46. Neonatal Fc receptor expression in dendritic cells mediates protective immunity against colorectal cancer. Immunity. 2013 Dec 12; 39(6):1095-107. View Abstract
  47. Fc-fusion proteins and FcRn: structural insights for longer-lasting and more effective therapeutics. Crit Rev Biotechnol. 2015 Jun; 35(2):235-54. View Abstract
  48. Ganglioside GM1-mediated transcytosis of cholera toxin bypasses the retrograde pathway and depends on the structure of the ceramide domain. J Biol Chem. 2013 Sep 06; 288(36):25804-25809. View Abstract
  49. Multivalent immune complexes divert FcRn to lysosomes by exclusion from recycling sorting tubules. Mol Biol Cell. 2013 Aug; 24(15):2398-405. View Abstract
  50. The unfolded protein response element IRE1a senses bacterial proteins invading the ER to activate RIG-I and innate immune signaling. Cell Host Microbe. 2013 May 15; 13(5):558-569. View Abstract
  51. A single native ganglioside GM1-binding site is sufficient for cholera toxin to bind to cells and complete the intoxication pathway. mBio. 2012 Oct 30; 3(6). View Abstract
  52. Lipid sorting by ceramide structure from plasma membrane to ER for the cholera toxin receptor ganglioside GM1. Dev Cell. 2012 Sep 11; 23(3):573-86. View Abstract
  53. The immunologic functions of the neonatal Fc receptor for IgG. J Clin Immunol. 2013 Jan; 33 Suppl 1:S9-17. View Abstract
  54. Cross-presentation of IgG-containing immune complexes. Cell Mol Life Sci. 2013 Apr; 70(8):1319-34. View Abstract
  55. Insights on the trafficking and retro-translocation of glycosphingolipid-binding bacterial toxins. Front Cell Infect Microbiol. 2012; 2:51. View Abstract
  56. Eliciting mucosal immunity. N Engl J Med. 2011 Sep 22; 365(12):1151-3. View Abstract
  57. To translocate or not: that is the problem. Cell Host Microbe. 2011 Sep 15; 10(3):179-80. View Abstract
  58. Discovery of dual-action membrane-anchored modulators of incretin receptors. PLoS One. 2011; 6(9):e24693. View Abstract
  59. Intracellular phosphatidylserine is essential for retrograde membrane traffic through endosomes. Proc Natl Acad Sci U S A. 2011 Sep 20; 108(38):15846-51. View Abstract
  60. TorsinA participates in endoplasmic reticulum-associated degradation. Nat Commun. 2011 Jul 12; 2:393. View Abstract
  61. Neonatal Fc receptor for IgG (FcRn) regulates cross-presentation of IgG immune complexes by CD8-CD11b+ dendritic cells. Proc Natl Acad Sci U S A. 2011 Jun 14; 108(24):9927-32. View Abstract
  62. The zebrafish dag1 mutant: a novel genetic model for dystroglycanopathies. Hum Mol Genet. 2011 May 01; 20(9):1712-25. View Abstract
  63. Functional analysis of VopF activity required for colonization in Vibrio cholerae. mBio. 2010 Dec 07; 1(5). View Abstract
  64. Intoxication of zebrafish and mammalian cells by cholera toxin depends on the flotillin/reggie proteins but not Derlin-1 or -2. J Clin Invest. 2010 Dec; 120(12):4399-4409. View Abstract
  65. Neonatal Fc receptor: from immunity to therapeutics. J Clin Immunol. 2010 Nov; 30(6):777-89. View Abstract
  66. Cholera toxin: an intracellular journey into the cytosol by way of the endoplasmic reticulum. Toxins (Basel). 2010 03; 2(3):310-25. View Abstract
  67. Selective translocation of the Bordetella pertussis adenylate cyclase toxin across the basolateral membranes of polarized epithelial cells. J Biol Chem. 2010 Apr 02; 285(14):10662-70. View Abstract
  68. N-terminal extension of the cholera toxin A1-chain causes rapid degradation after retrotranslocation from endoplasmic reticulum to cytosol. J Biol Chem. 2010 Feb 26; 285(9):6145-52. View Abstract
  69. An FcRn-dependent role for anti-flagellin immunoglobulin G in pathogenesis of colitis in mice. Gastroenterology. 2009 Nov; 137(5):1746-56.e1. View Abstract
  70. Immune and non-immune functions of the (not so) neonatal Fc receptor, FcRn. Semin Immunopathol. 2009 Jul; 31(2):223-36. View Abstract
  71. The recycling and transcytotic pathways for IgG transport by FcRn are distinct and display an inherent polarity. J Cell Biol. 2009 May 18; 185(4):673-84. View Abstract
  72. N-Glycan Moieties in Neonatal Fc Receptor Determine Steady-state Membrane Distribution and Directional Transport of IgG. J Biol Chem. 2009 Mar 27; 284(13):8292-300. View Abstract
  73. Ceramide activates JNK to inhibit a cAMP-gated K+ conductance and Cl- secretion in intestinal epithelia. FASEB J. 2009 Jan; 23(1):259-70. View Abstract
  74. Patching a leaky intestine. N Engl J Med. 2008 Jul 31; 359(5):526-8. View Abstract
  75. Dependence of antibody-mediated presentation of antigen on FcRn. Proc Natl Acad Sci U S A. 2008 Jul 08; 105(27):9337-42. View Abstract
  76. Attenuated endocytosis and toxicity of a mutant cholera toxin with decreased ability to cluster ganglioside GM1 molecules. Infect Immun. 2008 Apr; 76(4):1476-84. View Abstract
  77. Conversion of apical plasma membrane sphingomyelin to ceramide attenuates the intoxication of host cells by cholera toxin. Cell Microbiol. 2008 Jan; 10(1):67-80. View Abstract
  78. Derlin-1 facilitates the retro-translocation of cholera toxin. Mol Biol Cell. 2008 Mar; 19(3):877-84. View Abstract
  79. Ca2+-dependent calmodulin binding to FcRn affects immunoglobulin G transport in the transcytotic pathway. Mol Biol Cell. 2008 Jan; 19(1):414-23. View Abstract
  80. The HA proteins of botulinum toxin disrupt intestinal epithelial intercellular junctions to increase toxin absorption. Cell Microbiol. 2008 Feb; 10(2):355-64. View Abstract
  81. Rafting with cholera toxin: endocytosis and trafficking from plasma membrane to ER. FEMS Microbiol Lett. 2007 Jan; 266(2):129-37. View Abstract
  82. How the controller is controlled - neonatal Fc receptor expression and immunoglobulin G homeostasis. Immunology. 2007 Feb; 120(2):145-7. View Abstract
  83. IgG transport across mucosal barriers by neonatal Fc receptor for IgG and mucosal immunity. Springer Semin Immunopathol. 2006 Dec; 28(4):397-403. View Abstract
  84. Neonatal Fc receptor for IgG regulates mucosal immune responses to luminal bacteria. J Clin Invest. 2006 Aug; 116(8):2142-2151. View Abstract
  85. Protein disulfide isomerase-like proteins play opposing roles during retrotranslocation. J Cell Biol. 2006 Jun 19; 173(6):853-9. View Abstract
  86. Myosin light chain phosphorylation regulates barrier function by remodeling tight junction structure. J Cell Sci. 2006 May 15; 119(Pt 10):2095-106. View Abstract
  87. The Cdc42 inhibitor secramine B prevents cAMP-induced K+ conductance in intestinal epithelial cells. Biochem Pharmacol. 2006 Jun 14; 71(12):1720-6. View Abstract
  88. The viral E3 ubiquitin ligase mK3 uses the Derlin/p97 endoplasmic reticulum-associated degradation pathway to mediate down-regulation of major histocompatibility complex class I proteins. J Biol Chem. 2006 Mar 31; 281(13):8636-44. View Abstract
  89. A biochemical method for tracking cholera toxin transport from plasma membrane to Golgi and endoplasmic reticulum. Methods Mol Biol. 2006; 341:127-39. View Abstract
  90. Antibodies in the breakdown lane. Nat Biotechnol. 2005 Oct; 23(10):1232-4. View Abstract
  91. Raft trafficking of AB5 subunit bacterial toxins. Biochim Biophys Acta. 2005 Dec 30; 1746(3):314-21. View Abstract
  92. Calnexin and ERp57 facilitate the assembly of the neonatal Fc receptor for IgG with beta 2-microglobulin in the endoplasmic reticulum. J Immunol. 2005 Jul 15; 175(2):967-76. View Abstract
  93. Role of p97 AAA-ATPase in the retrotranslocation of the cholera toxin A1 chain, a non-ubiquitinated substrate. J Biol Chem. 2005 Jul 29; 280(30):28127-32. View Abstract
  94. Characterization of the porcine neonatal Fc receptor--potential use for trans-epithelial protein delivery. Immunology. 2005 Apr; 114(4):542-53. View Abstract
  95. Signal transduction by bacterial proteins. J Pediatr Gastroenterol Nutr. 2005 Apr; 40 Suppl 1:S33-4. View Abstract
  96. Endocytosis of cholera toxin by human enterocytes is developmentally regulated. Am J Physiol Gastrointest Liver Physiol. 2005 Aug; 289(2):G332-41. View Abstract
  97. Entry of protein toxins into mammalian cells by crossing the endoplasmic reticulum membrane: co-opting basic mechanisms of endoplasmic reticulum-associated degradation. Curr Top Microbiol Immunol. 2005; 300:149-68. View Abstract
  98. Ganglioside GD1a restores infectibility to mouse cells lacking functional receptors for polyomavirus. J Virol. 2005 Jan; 79(1):615-8. View Abstract
  99. A passionate kiss, then run: exocytosis and recycling of IgG by FcRn. Trends Cell Biol. 2005 Jan; 15(1):5-9. View Abstract
  100. Trafficking of cholera toxin-ganglioside GM1 complex into Golgi and induction of toxicity depend on actin cytoskeleton. Am J Physiol Cell Physiol. 2004 Nov; 287(5):C1453-62. View Abstract
  101. Pulmonary delivery of an erythropoietin Fc fusion protein in non-human primates through an immunoglobulin transport pathway. Proc Natl Acad Sci U S A. 2004 Jun 29; 101(26):9763-8. View Abstract
  102. Human neonatal Fc receptor mediates transport of IgG into luminal secretions for delivery of antigens to mucosal dendritic cells. Immunity. 2004 Jun; 20(6):769-83. View Abstract
  103. Retrograde transport of cholera toxin from the plasma membrane to the endoplasmic reticulum requires the trans-Golgi network but not the Golgi apparatus in Exo2-treated cells. EMBO Rep. 2004 Jun; 5(6):596-601. View Abstract
  104. Cholera toxin toxicity does not require functional Arf6- and dynamin-dependent endocytic pathways. Mol Biol Cell. 2004 Aug; 15(8):3631-41. View Abstract
  105. Retrograde transport of cholera toxin into the ER of host cells. Int J Med Microbiol. 2004 Apr; 293(7-8):491-4. View Abstract
  106. Paneth cell cryptdins act in vitro as apical paracrine regulators of the innate inflammatory response. J Biol Chem. 2004 May 07; 279(19):19902-7. View Abstract
  107. Bidirectional transepithelial IgG transport by a strongly polarized basolateral membrane Fcgamma-receptor. Mol Biol Cell. 2004 Apr; 15(4):1746-59. View Abstract
  108. Diarrhea-associated HIV-1 APIs potentiate muscarinic activation of Cl- secretion by T84 cells via prolongation of cytosolic Ca2+ signaling. Am J Physiol Cell Physiol. 2004 May; 286(5):C998-C1008. View Abstract
  109. The intracellular voyage of cholera toxin: going retro. Trends Biochem Sci. 2003 Dec; 28(12):639-45. View Abstract
  110. Gangliosides that associate with lipid rafts mediate transport of cholera and related toxins from the plasma membrane to endoplasmic reticulm. Mol Biol Cell. 2003 Dec; 14(12):4783-93. View Abstract
  111. Gangliosides are receptors for murine polyoma virus and SV40. EMBO J. 2003 Sep 01; 22(17):4346-55. View Abstract
  112. Claudin-8 expression in Madin-Darby canine kidney cells augments the paracellular barrier to cation permeation. J Biol Chem. 2003 May 09; 278(19):17350-9. View Abstract
  113. Distribution of the IgG Fc receptor, FcRn, in the human fetal intestine. Pediatr Res. 2003 Feb; 53(2):295-301. View Abstract
  114. Role of ubiquitination in retro-translocation of cholera toxin and escape of cytosolic degradation. EMBO Rep. 2002 Dec; 3(12):1222-7. View Abstract
  115. The heavy chain of neonatal Fc receptor for IgG is sequestered in endoplasmic reticulum by forming oligomers in the absence of beta2-microglobulin association. Biochem J. 2002 Nov 01; 367(Pt 3):703-14. View Abstract
  116. Receptor-mediated immunoglobulin G transport across mucosal barriers in adult life: functional expression of FcRn in the mammalian lung. J Exp Med. 2002 Aug 05; 196(3):303-10. View Abstract
  117. Functional reconstitution of human FcRn in Madin-Darby canine kidney cells requires co-expressed human beta 2-microglobulin. J Biol Chem. 2002 Aug 02; 277(31):28038-50. View Abstract
  118. Cryptdin 3 forms anion selective channels in cytoplasmic membranes of human embryonic kidney cells. Am J Physiol Gastrointest Liver Physiol. 2002 May; 282(5):G757-65. View Abstract
  119. Uncoupling of the cholera toxin-G(M1) ganglioside receptor complex from endocytosis, retrograde Golgi trafficking, and downstream signal transduction by depletion of membrane cholesterol. J Biol Chem. 2002 May 03; 277(18):16249-56. View Abstract
  120. Research agenda for pediatric gastroenterology, hepatology and nutrition: secretion and diarrhea. Report of the North American Society for Pediatric Gastroenterology, Hepatology and Nutrition for the Children's Digestive Health and Nutrition Foundation. J Pediatr Gastroenterol Nutr. 2002; 35 Suppl 3:S246-9. View Abstract
  121. Characterization of receptor-mediated signal transduction by Escherichia coli type IIa heat-labile enterotoxin in the polarized human intestinal cell line T84. Infect Immun. 2001 Dec; 69(12):7205-12. View Abstract
  122. Vibrio cholerae-induced cellular responses of polarized T84 intestinal epithelial cells are dependent on production of cholera toxin and the RTX toxin. Infect Immun. 2001 Oct; 69(10):6310-7. View Abstract
  123. A cholera toxin B-subunit variant that binds ganglioside G(M1) but fails to induce toxicity. J Biol Chem. 2001 Oct 05; 276(40):36939-45. View Abstract
  124. A mutant cholera toxin B subunit that binds GM1- ganglioside but lacks immunomodulatory or toxic activity. Proc Natl Acad Sci U S A. 2001 Jul 17; 98(15):8536-41. View Abstract
  125. The multiple roles of major histocompatibility complex class-I-like molecules in mucosal immune function. Acta Odontol Scand. 2001 Jun; 59(3):139-44. View Abstract
  126. Microbes and microbial Toxins: paradigms for microbial-mucosal toxins. V. Cholera: invasion of the intestinal epithelial barrier by a stably folded protein toxin. Am J Physiol Gastrointest Liver Physiol. 2001 May; 280(5):G781-6. View Abstract
  127. Protein disulfide isomerase acts as a redox-dependent chaperone to unfold cholera toxin. Cell. 2001 Mar 23; 104(6):937-48. View Abstract
  128. MHC class I-related neonatal Fc receptor for IgG is functionally expressed in monocytes, intestinal macrophages, and dendritic cells. J Immunol. 2001 Mar 01; 166(5):3266-76. View Abstract
  129. Cryptdin-3 induces novel apical conductance(s) in Cl- secretory, including cystic fibrosis, epithelia. Am J Physiol Cell Physiol. 2001 Feb; 280(2):C296-302. View Abstract
  130. Microbial invasion across the intestinal epithelial barrier. Pediatr Res. 2001 Jan; 49(1):4-5. View Abstract
  131. Association of protease activity in Vibrio cholerae vaccine strains with decreases in transcellular epithelial resistance of polarized T84 intestinal epithelial cells. Infect Immun. 2000 Nov; 68(11):6487-92. View Abstract
  132. Floating cholera toxin into epithelial cells: functional association with caveolae-like detergent-insoluble membrane microdomains. Int J Med Microbiol. 2000 Oct; 290(4-5):403-8. View Abstract
  133. Heterogeneity of detergent-insoluble membranes from human intestine containing caveolin-1 and ganglioside G(M1). Am J Physiol Gastrointest Liver Physiol. 2000 Jun; 278(6):G895-904. View Abstract
  134. Salmonella pathogenesis: the trojan horse or the New York shuttle? Gastroenterology. 2000 Apr; 118(4):803-5. View Abstract
  135. Bidirectional FcRn-dependent IgG transport in a polarized human intestinal epithelial cell line. J Clin Invest. 1999 Oct; 104(7):903-11. View Abstract
  136. Floating the molecular machinery for t-cell activation. Gastroenterology. 1999 Aug; 117(2):503-5. View Abstract
  137. Membrane traffic and the cellular uptake of cholera toxin. Biochim Biophys Acta. 1999 Jul 08; 1450(3):177-90. View Abstract
  138. Antigen presentation by intestinal epithelial cells. Immunol Lett. 1999 Jun 15; 69(1):7-11. View Abstract
  139. Anthrax toxin entry into polarized epithelial cells. Infect Immun. 1999 Jun; 67(6):3026-30. View Abstract
  140. Structural basis for the differential toxicity of cholera toxin and Escherichia coli heat-labile enterotoxin. Construction of hybrid toxins identifies the A2-domain as the determinant of differential toxicity. J Biol Chem. 1999 Feb 12; 274(7):3962-9. View Abstract
  141. Mucosal vaccination: "all politics are local". Gastroenterology. 1999 Feb; 116(2):497-9. View Abstract
  142. The potassium channel and how it works. Gastroenterology. 1999 Jan; 116(1):216-7. View Abstract
  143. Differential activity of cholera toxin and E. coli enterotoxin: construction and purification of mutant and hybrid derivatives. Biochem Soc Trans. 1998 Nov; 26(4):S364. View Abstract
  144. Distinct Ca2+- and cAMP-dependent anion conductances in the apical membrane of polarized T84 cells. Am J Physiol. 1998 08; 275(2):C484-95. View Abstract
  145. Paneth cells: on the front line or in the backfield? Gastroenterology. 1998 Jun; 114(6):1343-5. View Abstract
  146. Ganglioside structure dictates signal transduction by cholera toxin and association with caveolae-like membrane domains in polarized epithelia. J Cell Biol. 1998 May 18; 141(4):917-27. View Abstract
  147. Acid secretion, ulcer disease, and cell biology. Gastroenterology. 1998 Mar; 114(3):607-8. View Abstract
  148. The antifungal antibiotic, clotrimazole, inhibits chloride secretion by human intestinal T84 cells via blockade of distinct basolateral K+ conductances. Demonstration of efficacy in intact rabbit colon and in an in vivo mouse model of cholera. J Clin Invest. 1997 Dec 15; 100(12):3111-20. View Abstract
  149. Induction of epithelial chloride secretion by channel-forming cryptdins 2 and 3. Proc Natl Acad Sci U S A. 1997 Aug 05; 94(16):8585-9. View Abstract
  150. Proteolytic activation of cholera toxin and Escherichia coli labile toxin by entry into host epithelial cells. Signal transduction by a protease-resistant toxin variant. J Biol Chem. 1997 Jun 13; 272(24):15562-8. View Abstract
  151. Surface expression, polarization, and functional significance of CD73 in human intestinal epithelia. J Clin Invest. 1997 Jun 01; 99(11):2588-601. View Abstract
  152. The antifungal antibiotic, clotrimazole, inhibits Cl- secretion by polarized monolayers of human colonic epithelial cells. J Clin Invest. 1996 Nov 01; 98(9):2066-75. View Abstract
  153. Role of the glycocalyx in regulating access of microparticles to apical plasma membranes of intestinal epithelial cells: implications for microbial attachment and oral vaccine targeting. J Exp Med. 1996 Sep 01; 184(3):1045-59. View Abstract
  154. Carboxy-terminal vesicular stomatitis virus G protein-tagged intestinal Na+-dependent glucose cotransporter (SGLT1): maintenance of surface expression and global transport function with selective perturbation of transport kinetics and polarized expression. J Biol Chem. 1996 Mar 29; 271(13):7738-44. View Abstract
  155. Targeting of cholera toxin and Escherichia coli heat labile toxin in polarized epithelia: role of COOH-terminal KDEL. J Cell Biol. 1995 Nov; 131(4):951-62. View Abstract
  156. Transcytosis of cholera toxin subunits across model human intestinal epithelia. Proc Natl Acad Sci U S A. 1995 Oct 24; 92(22):10094-8. View Abstract
  157. Signal transduction by cholera toxin: processing in vesicular compartments does not require acidification. Am J Physiol. 1995 Oct; 269(4 Pt 1):G548-57. View Abstract
  158. The A2b adenosine receptor mediates cAMP responses to adenosine receptor agonists in human intestinal epithelia. J Biol Chem. 1995 Feb 03; 270(5):2387-94. View Abstract
  159. Bacterial and host interactions during the biogenesis, toxicity and immunogenicity of Escherichia coli heat-labile enterotoxin. Biochem Soc Trans. 1994 May; 22(2):306-9. View Abstract
  160. Heterologous expression of delta F508 CFTR results in decreased sialylation of membrane glycoconjugates. Am J Physiol. 1994 Feb; 266(2 Pt 1):C360-6. View Abstract
  161. Monoclonal immunoglobulin A antibodies directed against cholera toxin prevent the toxin-induced chloride secretory response and block toxin binding to intestinal epithelial cells in vitro. Infect Immun. 1993 Dec; 61(12):5271-8. View Abstract
  162. Entry of cholera toxin into polarized human intestinal epithelial cells. Identification of an early brefeldin A sensitive event required for A1-peptide generation. J Clin Invest. 1993 Dec; 92(6):2941-51. View Abstract
  163. Mechanism of cholera toxin action on a polarized human intestinal epithelial cell line: role of vesicular traffic. J Cell Biol. 1992 Jun; 117(6):1197-1209. View Abstract
  164. Cl- secretion in a model intestinal epithelium induced by a neutrophil-derived secretagogue. J Clin Invest. 1992 Jun; 89(6):1938-44. View Abstract
  165. Endocytosis of water channels in rat kidney: cell specificity and correlation with in vivo antidiuresis. Am J Physiol. 1990 Dec; 259(6 Pt 1):C920-32. View Abstract
  166. Endocytic vesicles from renal papilla which retrieve the vasopressin-sensitive water channel do not contain a functional H+ ATPase. J Cell Biol. 1990 Aug; 111(2):379-89. View Abstract
  167. [Characterization of proton pump and osmotic water transport in endocytic vesicles from rat kidney proximal tubule]. Sheng Li Xue Bao. 1990 Apr; 42(2):105-13. View Abstract
  168. FITC-dextran as a probe for endosome function and localization in kidney. Am J Physiol. 1990 Feb; 258(2 Pt 1):C309-17. View Abstract
  169. Interaction of cholera toxin with cloned human goblet cells in monolayer culture. Am J Physiol. 1990 Jan; 258(1 Pt 1):G96-102. View Abstract
  170. Functional colocalization of water channels and proton pumps in endosomes from kidney proximal tubule. J Gen Physiol. 1989 May; 93(5):885-902. View Abstract
  171. Endosomes from kidney collecting tubule cells contain the vasopressin-sensitive water channel. Nature. 1988 May 19; 333(6170):268-9. View Abstract
  172. Differential binding kinetics of cholera toxin to intestinal microvillus membrane during development. Infect Immun. 1987 Dec; 55(12):3126-30. View Abstract
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