Wayne I. Lencer

Wayne I. Lencer, MD

Chief, Division of Gastroenterology, Hepatology and Nutrition; Harry Schwachman Chair in Pediatric Gastroenterology

Professor of Pediatrics, Harvard Medical School

  • Contact: 617-355-6058

  • Fax: 617-730-0404

Medical Services

Specialties

  • Diarrheal Diseases
  • Gastroenterology
  • Intestinal Normal Physiology and Failure

Departments

  • Gastroenterology, Hepatology and Nutrition
  • Medicine
To schedule an appointment: Call 617-355-6058 or Request an Appointment

Experience and Education

Education

Medical School

Boston University School of Medicine, 1977

Boston, MA

Internship

Boston City Hospital, 1977-1978

Boston, MA

Residency

Boston City Hospital, 1978-1980

Boston, MA

Fellowship

Boston Children's Hospital, 1984-1987

Boston, MA

Certifications

  • Pediatrics, Pediatric Gastroenterology

Research

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. Dr. Lencer is Director of the Harvard Digestive Diseases Center.


Publications

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  1. Saslowsky DE, Thiagarajah JR, McCormick BA, Lee JC, Lencer WI. Microbial sphingomyelinase induces RhoA-mediated reorganization of the apical brush border membrane and is protective against invasion. Mol Biol Cell. 2016 Apr 1; 27(7):1120-30.
  2. Lexmond WS, Rufo PA, Fiebiger E, Lencer WI. Electrophysiological Studies into the Safety of the Anti-diarrheal Drug Clotrimazole during Oral Rehydration Therapy. PLoS Negl Trop Dis. 2015 Sep; 9(9):e0004098.
  3. Reimold FR, Balasubramanian S, Doroquez DB, Shmukler BE, Zsengeller ZK, Saslowsky D, Thiagarajah JR, Stillman IE, Lencer WI, Wu BL, Villalpando-Carrion S, Alper SL. Congenital chloride-losing diarrhea in a Mexican child with the novel homozygous SLC26A3 mutation G393W. Front Physiol. 2015; 6:179.
  4. Lencer WI, DeLuca H, Grey MJ, Cho JA. Innate immunity at mucosal surfaces: the IRE1-RIDD-RIG-I pathway. Trends Immunol. 2015 Jul; 36(7):401-9.
  5. Pyzik M, Rath T, Lencer WI, Baker K, Blumberg RS. FcRn: The Architect Behind the Immune and Nonimmune Functions of IgG and Albumin. J Immunol. 2015 May 15; 194(10):4595-603.
  6. Day CA, Baetz NW, Copeland CA, Kraft LJ, Han B, Tiwari A, Drake KR, De Luca H, Chinnapen DJ, Davidson MW, Holmes RK, Jobling MG, Schroer TA, Lencer WI, Kenworthy AK. Microtubule motors power plasma membrane tubulation in clathrin-independent endocytosis. Traffic. 2015 Jun; 16(6):572-90.
  7. Cho JA, Zhang X, Miller GM, Lencer WI, Nery FC. 4-Phenylbutyrate attenuates the ER stress response and cyclic AMP accumulation in DYT1 dystonia cell models. PLoS One. 2014; 9(11):e110086.
  8. Zhou X, Massol RH, Nakamura F, Chen X, Gewurz BE, Davis BM, Lencer WI, Waldor MK. Remodeling of the intestinal brush border underlies adhesion and virulence of an enteric pathogen. MBio. 2014; 5(4).
  9. Luo R, Jeong SJ, Yang A, Wen M, Saslowsky DE, Lencer WI, Araç D, Piao X. Mechanism for adhesion G protein-coupled receptor GPR56-mediated RhoA activation induced by collagen III stimulation. PLoS One. 2014; 9(6):e100043.
  10. te Welscher YM, Chinnapen DJ, Kaoutzani L, Mrsny RJ, Lencer WI. Unsaturated glycoceramides as molecular carriers for mucosal drug delivery of GLP-1. J Control Release. 2014 Feb 10; 175:72-8.
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  11. Baker K, Rath T, Flak MB, Arthur JC, Chen Z, Glickman JN, Zlobec I, Karamitopoulou E, Stachler MD, Odze RD, Lencer WI, Jobin C, Blumberg RS. Neonatal Fc receptor expression in dendritic cells mediates protective immunity against colorectal cancer. Immunity. 2013 Dec 12; 39(6):1095-107.
  12. Rath T, Baker K, Dumont JA, Peters RT, Jiang H, Qiao SW, Lencer WI, Pierce GF, Blumberg RS. Fc-fusion proteins and FcRn: structural insights for longer-lasting and more effective therapeutics. Crit Rev Biotechnol. 2015 Jun; 35(2):235-54.
  13. Saslowsky DE, te Welscher YM, Chinnapen DJ, Wagner JS, Wan J, Kern E, Lencer WI. 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 6; 288(36):25804-9.
  14. Weflen AW, Baier N, Tang QJ, Van den Hof M, Blumberg RS, Lencer WI, Massol RH. Multivalent immune complexes divert FcRn to lysosomes by exclusion from recycling sorting tubules. Mol Biol Cell. 2013 Aug; 24(15):2398-405.
  15. Cho JA, Lee AH, Platzer B, Cross BC, Gardner BM, De Luca H, Luong P, Harding HP, Glimcher LH, Walter P, Fiebiger E, Ron D, Kagan JC, Lencer WI. 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):558-69.
  16. Jobling MG, Yang Z, Kam WR, Lencer WI, Holmes RK. A single native ganglioside GM1-binding site is sufficient for cholera toxin to bind to cells and complete the intoxication pathway. MBio. 2012; 3(6).
  17. Chinnapen DJ, Hsieh WT, te Welscher YM, Saslowsky DE, Kaoutzani L, Brandsma E, D'Auria L, Park H, Wagner JS, Drake KR, Kang M, Benjamin T, Ullman MD, Costello CE, Kenworthy AK, Baumgart T, Massol RH, Lencer WI. 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.
  18. Rath T, Kuo TT, Baker K, Qiao SW, Kobayashi K, Yoshida M, Roopenian D, Fiebiger E, Lencer WI, Blumberg RS. The immunologic functions of the neonatal Fc receptor for IgG. J Clin Immunol. 2013 Jan; 33 Suppl 1:S9-17.
  19. Baker K, Rath T, Lencer WI, Fiebiger E, Blumberg RS. Cross-presentation of IgG-containing immune complexes. Cell Mol Life Sci. 2013 Apr; 70(8):1319-34.
  20. Cho JA, Chinnapen DJ, Aamar E, te Welscher YM, Lencer WI, Massol R. Insights on the trafficking and retro-translocation of glycosphingolipid-binding bacterial toxins. Front Cell Infect Microbiol. 2012; 2:51.
  21. Lencer WI, von Andrian UH. Eliciting mucosal immunity. N Engl J Med. 2011 Sep 22; 365(12):1151-3.
  22. Lencer WI, Tweten RK. To translocate or not: that is the problem. Cell Host Microbe. 2011 Sep 15; 10(3):179-80.
  23. Fortin JP, Chinnapen D, Beinborn M, Lencer W, Kopin AS. Discovery of dual-action membrane-anchored modulators of incretin receptors. PLoS One. 2011; 6(9):e24693.
  24. Uchida Y, Hasegawa J, Chinnapen D, Inoue T, Okazaki S, Kato R, Wakatsuki S, Misaki R, Koike M, Uchiyama Y, Iemura S, Natsume T, Kuwahara R, Nakagawa T, Nishikawa K, Mukai K, Miyoshi E, Taniguchi N, Sheff D, Lencer WI, Taguchi T, Arai H. Intracellular phosphatidylserine is essential for retrograde membrane traffic through endosomes. Proc Natl Acad Sci U S A. 2011 Sep 20; 108(38):15846-51.
  25. Nery FC, Armata IA, Farley JE, Cho JA, Yaqub U, Chen P, da Hora CC, Wang Q, Tagaya M, Klein C, Tannous B, Caldwell KA, Caldwell GA, Lencer WI, Ye Y, Breakefield XO. TorsinA participates in endoplasmic reticulum-associated degradation. Nat Commun. 2011; 2:393.
  26. Baker K, Qiao SW, Kuo TT, Aveson VG, Platzer B, Andersen JT, Sandlie I, Chen Z, de Haar C, Lencer WI, Fiebiger E, Blumberg RS. 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.
  27. Gupta V, Kawahara G, Gundry SR, Chen AT, Lencer WI, Zhou Y, Zon LI, Kunkel LM, Beggs AH. The zebrafish dag1 mutant: a novel genetic model for dystroglycanopathies. Hum Mol Genet. 2011 May 1; 20(9):1712-25.
  28. Tam VC, Suzuki M, Coughlin M, Saslowsky D, Biswas K, Lencer WI, Faruque SM, Mekalanos JJ. Functional analysis of VopF activity required for colonization in Vibrio cholerae. MBio. 2010; 1(5).
  29. Saslowsky DE, Cho JA, Chinnapen H, Massol RH, Chinnapen DJ, Wagner JS, De Luca HE, Kam W, Paw BH, Lencer WI. 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.
  30. Kuo TT, Baker K, Yoshida M, Qiao SW, Aveson VG, Lencer WI, Blumberg RS. Neonatal Fc receptor: from immunity to therapeutics. J Clin Immunol. 2010 Nov; 30(6):777-89.
  31. Wernick NL, Chinnapen DJ, Cho JA, Lencer WI. Cholera toxin: an intracellular journey into the cytosol by way of the endoplasmic reticulum. Toxins (Basel). 2010 Mar; 2(3):310-25.
  32. Eby JC, Ciesla WP, Hamman W, Donato GM, Pickles RJ, Hewlett EL, Lencer WI. Selective translocation of the Bordetella pertussis adenylate cyclase toxin across the basolateral membranes of polarized epithelial cells. J Biol Chem. 2010 Apr 2; 285(14):10662-70.
  33. Wernick NL, De Luca H, Kam WR, Lencer WI. 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.
  34. Kobayashi K, Qiao SW, Yoshida M, Baker K, Lencer WI, Blumberg RS. An FcRn-dependent role for anti-flagellin immunoglobulin G in pathogenesis of colitis in mice. Gastroenterology. 2009 Nov; 137(5):1746-56.e1.
  35. Baker K, Qiao SW, Kuo T, Kobayashi K, Yoshida M, Lencer WI, Blumberg RS. Immune and non-immune functions of the (not so) neonatal Fc receptor, FcRn. Semin Immunopathol. 2009 Jul; 31(2):223-36.
  36. Tzaban S, Massol RH, Yen E, Hamman W, Frank SR, Lapierre LA, Hansen SH, Goldenring JR, Blumberg RS, Lencer WI. 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.
  37. Kuo TT, de Muinck EJ, Claypool SM, Yoshida M, Nagaishi T, Aveson VG, Lencer WI, Blumberg RS. 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.
  38. Saslowsky DE, Tanaka N, Reddy KP, Lencer WI. Ceramide activates JNK to inhibit a cAMP-gated K+ conductance and Cl- secretion in intestinal epithelia. FASEB J. 2009 Jan; 23(1):259-70.
  39. Lencer WI. Patching a leaky intestine. N Engl J Med. 2008 Jul 31; 359(5):526-8.
  40. Qiao SW, Kobayashi K, Johansen FE, Sollid LM, Andersen JT, Milford E, Roopenian DC, Lencer WI, Blumberg RS. Dependence of antibody-mediated presentation of antigen on FcRn. Proc Natl Acad Sci U S A. 2008 Jul 8; 105(27):9337-42.
  41. Wolf AA, Jobling MG, Saslowsky DE, Kern E, Drake KR, Kenworthy AK, Holmes RK, Lencer WI. 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.
  42. Saslowsky DE, Lencer WI. 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.
  43. Bernardi KM, Forster ML, Lencer WI, Tsai B. Derlin-1 facilitates the retro-translocation of cholera toxin. Mol Biol Cell. 2008 Mar; 19(3):877-84.
  44. Dickinson BL, Claypool SM, D'Angelo JA, Aiken ML, Venu N, Yen EH, Wagner JS, Borawski JA, Pierce AT, Hershberg R, Blumberg RS, Lencer WI. Ca2+-dependent calmodulin binding to FcRn affects immunoglobulin G transport in the transcytotic pathway. Mol Biol Cell. 2008 Jan; 19(1):414-23.
  45. Matsumura T, Jin Y, Kabumoto Y, Takegahara Y, Oguma K, Lencer WI, Fujinaga Y. The HA proteins of botulinum toxin disrupt intestinal epithelial intercellular junctions to increase toxin absorption. Cell Microbiol. 2008 Feb; 10(2):355-64.
  46. Chinnapen DJ, Chinnapen H, Saslowsky D, Lencer WI. Rafting with cholera toxin: endocytosis and trafficking from plasma membrane to ER. FEMS Microbiol Lett. 2007 Jan; 266(2):129-37.
  47. Qiao SW, Lencer WI, Blumberg RS. How the controller is controlled - neonatal Fc receptor expression and immunoglobulin G homeostasis. Immunology. 2007 Feb; 120(2):145-7.
  48. Yoshida M, Masuda A, Kuo TT, Kobayashi K, Claypool SM, Takagawa T, Kutsumi H, Azuma T, Lencer WI, Blumberg RS. IgG transport across mucosal barriers by neonatal Fc receptor for IgG and mucosal immunity. Springer Semin Immunopathol. 2006 Dec; 28(4):397-403.
  49. Yoshida M, Kobayashi K, Kuo TT, Bry L, Glickman JN, Claypool SM, Kaser A, Nagaishi T, Higgins DE, Mizoguchi E, Wakatsuki Y, Roopenian DC, Mizoguchi A, Lencer WI, Blumberg RS. Neonatal Fc receptor for IgG regulates mucosal immune responses to luminal bacteria. J Clin Invest. 2006 Aug; 116(8):2142-2151.
  50. Forster ML, Sivick K, Park YN, Arvan P, Lencer WI, Tsai B. Protein disulfide isomerase-like proteins play opposing roles during retrotranslocation. J Cell Biol. 2006 Jun 19; 173(6):853-9.
  51. Shen L, Black ED, Witkowski ED, Lencer WI, Guerriero V, Schneeberger EE, Turner JR. Myosin light chain phosphorylation regulates barrier function by remodeling tight junction structure. J Cell Sci. 2006 May 15; 119(Pt 10):2095-106.
  52. Pelish HE, Ciesla W, Tanaka N, Reddy K, Shair MD, Kirchhausen T, Lencer WI. The Cdc42 inhibitor secramine B prevents cAMP-induced K+ conductance in intestinal epithelial cells. Biochem Pharmacol. 2006 Jun 14; 71(12):1720-6.
  53. Wang X, Ye Y, Lencer W, Hansen TH. 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.
  54. De Luca HE, Lencer WI. A biochemical method for tracking cholera toxin transport from plasma membrane to Golgi and endoplasmic reticulum. Methods Mol Biol. 2006; 341:127-39.
  55. Blumberg RS, Lencer WI. Antibodies in the breakdown lane. Nat Biotechnol. 2005 Oct; 23(10):1232-4.
  56. Lencer WI, Saslowsky D. Raft trafficking of AB5 subunit bacterial toxins. Biochim Biophys Acta. 2005 Dec 30; 1746(3):314-21.
  57. Zhu X, Peng J, Chen D, Liu X, Ye L, Iijima H, Kadavil K, Lencer WI, Blumberg RS. 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.
  58. Kothe M, Ye Y, Wagner JS, De Luca HE, Kern E, Rapoport TA, Lencer WI. 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.
  59. Stirling CM, Charleston B, Takamatsu H, Claypool S, Lencer W, Blumberg RS, Wileman TE. Characterization of the porcine neonatal Fc receptor--potential use for trans-epithelial protein delivery. Immunology. 2005 Apr; 114(4):542-53.
  60. Lencer WI. Signal transduction by bacterial proteins. J Pediatr Gastroenterol Nutr. 2005 Apr; 40 Suppl 1:S33-4.
  61. Lu L, Khan S, Lencer W, Walker WA. Endocytosis of cholera toxin by human enterocytes is developmentally regulated. Am J Physiol Gastrointest Liver Physiol. 2005 Aug; 289(2):G332-41.
  62. Gilbert J, Dahl J, Riney C, You J, Cui C, Holmes R, Lencer W, Benjamin T. Ganglioside GD1a restores infectibility to mouse cells lacking functional receptors for polyomavirus. J Virol. 2005 Jan; 79(1):615-8.
  63. Lord JM, Roberts LM, Lencer WI. 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.
  64. Lencer WI, Blumberg RS. A passionate kiss, then run: exocytosis and recycling of IgG by FcRn. Trends Cell Biol. 2005 Jan; 15(1):5-9.
  65. Badizadegan K, Wheeler HE, Fujinaga Y, Lencer WI. 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.
  66. Bitonti AJ, Dumont JA, Low SC, Peters RT, Kropp KE, Palombella VJ, Stattel JM, Lu Y, Tan CA, Song JJ, Garcia AM, Simister NE, Spiekermann GM, Lencer WI, Blumberg RS. 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.
  67. Yoshida M, Claypool SM, Wagner JS, Mizoguchi E, Mizoguchi A, Roopenian DC, Lencer WI, Blumberg RS. 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.
  68. Feng Y, Jadhav AP, Rodighiero C, Fujinaga Y, Kirchhausen T, Lencer WI. 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.
  69. Massol RH, Larsen JE, Fujinaga Y, Lencer WI, Kirchhausen T. Cholera toxin toxicity does not require functional Arf6- and dynamin-dependent endocytic pathways. Mol Biol Cell. 2004 Aug; 15(8):3631-41.
  70. Lencer WI. Retrograde transport of cholera toxin into the ER of host cells. Int J Med Microbiol. 2004 Apr; 293(7-8):491-4.
  71. Lin PW, Simon PO, Gewirtz AT, Neish AS, Ouellette AJ, Madara JL, Lencer WI. Paneth cell cryptdins act in vitro as apical paracrine regulators of the innate inflammatory response. J Biol Chem. 2004 May 7; 279(19):19902-7.
  72. Claypool SM, Dickinson BL, Wagner JS, Johansen FE, Venu N, Borawski JA, Lencer WI, Blumberg RS. Bidirectional transepithelial IgG transport by a strongly polarized basolateral membrane Fcgamma-receptor. Mol Biol Cell. 2004 Apr; 15(4):1746-59.
  73. Rufo PA, Lin PW, Andrade A, Jiang L, Rameh L, Flexner C, Alper SL, Lencer WI. 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.
  74. Lencer WI, Tsai B. The intracellular voyage of cholera toxin: going retro. Trends Biochem Sci. 2003 Dec; 28(12):639-45.
  75. Fujinaga Y, Wolf AA, Rodighiero C, Wheeler H, Tsai B, Allen L, Jobling MG, Rapoport T, Holmes RK, Lencer WI. 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.
  76. Tsai B, Gilbert JM, Stehle T, Lencer W, Benjamin TL, Rapoport TA. Gangliosides are receptors for murine polyoma virus and SV40. EMBO J. 2003 Sep 1; 22(17):4346-55.
  77. Yu AS, Enck AH, Lencer WI, Schneeberger EE. Claudin-8 expression in Madin-Darby canine kidney cells augments the paracellular barrier to cation permeation. J Biol Chem. 2003 May 9; 278(19):17350-9.
  78. Shah U, Dickinson BL, Blumberg RS, Simister NE, Lencer WI, Walker WA. Distribution of the IgG Fc receptor, FcRn, in the human fetal intestine. Pediatr Res. 2003 Feb; 53(2):295-301.
  79. Rodighiero C, Tsai B, Rapoport TA, Lencer WI. Role of ubiquitination in retro-translocation of cholera toxin and escape of cytosolic degradation. EMBO Rep. 2002 Dec; 3(12):1222-7.
  80. Zhu X, Peng J, Raychowdhury R, Nakajima A, Lencer WI, Blumberg RS. 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 1; 367(Pt 3):703-14.
  81. Spiekermann GM, Finn PW, Ward ES, Dumont J, Dickinson BL, Blumberg RS, Lencer WI. Receptor-mediated immunoglobulin G transport across mucosal barriers in adult life: functional expression of FcRn in the mammalian lung. J Exp Med. 2002 Aug 5; 196(3):303-10.
  82. Claypool SM, Dickinson BL, Yoshida M, Lencer WI, Blumberg RS. Functional reconstitution of human FcRn in Madin-Darby canine kidney cells requires co-expressed human beta 2-microglobulin. J Biol Chem. 2002 Aug 2; 277(31):28038-50.
  83. Yue G, Merlin D, Selsted ME, Lencer WI, Madara JL, Eaton DC. 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.
  84. Wolf AA, Fujinaga Y, Lencer WI. 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 3; 277(18):16249-56.
  85. Lencer WI, Barrett K, Colgan S, Cohen MB, Duggan CP, Kotelchuck M, Rhoads JM. 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.
  86. Wimer-Mackin S, Holmes RK, Wolf AA, Lencer WI, Jobling MG. 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.
  87. Fullner KJ, Lencer WI, Mekalanos JJ. 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.
  88. Rodighiero C, Fujinaga Y, Hirst TR, Lencer WI. A cholera toxin B-subunit variant that binds ganglioside G(M1) but fails to induce toxicity. J Biol Chem. 2001 Oct 5; 276(40):36939-45.
  89. Aman AT, Fraser S, Merritt EA, Rodigherio C, Kenny M, Ahn M, Hol WG, Williams NA, Lencer WI, Hirst TR. 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.
  90. Blumberg RS, van de Wal Y, Claypool S, Corazza N, Dickinson B, Nieuwenhuis E, Pitman R, Spiekermann G, Zhu X, Colgan S, Lencer WI. The multiple roles of major histocompatibility complex class-I-like molecules in mucosal immune function. Acta Odontol Scand. 2001 Jun; 59(3):139-44.
  91. Lencer WI. 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.
  92. Tsai B, Rodighiero C, Lencer WI, Rapoport TA. Protein disulfide isomerase acts as a redox-dependent chaperone to unfold cholera toxin. Cell. 2001 Mar 23; 104(6):937-48.
  93. Zhu X, Meng G, Dickinson BL, Li X, Mizoguchi E, Miao L, Wang Y, Robert C, Wu B, Smith PD, Lencer WI, Blumberg RS. MHC class I-related neonatal Fc receptor for IgG is functionally expressed in monocytes, intestinal macrophages, and dendritic cells. J Immunol. 2001 Mar 1; 166(5):3266-76.
  94. Merlin D, Yue G, Lencer WI, Selsted ME, Madara JL. 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.
  95. Lencer WI. Microbial invasion across the intestinal epithelial barrier. Pediatr Res. 2001 Jan; 49(1):4-5.
  96. Mel SF, Fullner KJ, Wimer-Mackin S, Lencer WI, Mekalanos JJ. 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.
  97. Badizadegan K, Wolf AA, Rodighiero C, Jobling M, Hirst TR, Holmes RK, Lencer WI. 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.
  98. Badizadegan K, Dickinson BL, Wheeler HE, Blumberg RS, Holmes RK, Lencer WI. 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.
  99. Lencer WI, Neutra MR. Salmonella pathogenesis: the trojan horse or the New York shuttle? Gastroenterology. 2000 Apr; 118(4):803-5.
  100. Dickinson BL, Badizadegan K, Wu Z, Ahouse JC, Zhu X, Simister NE, Blumberg RS, Lencer WI. Bidirectional FcRn-dependent IgG transport in a polarized human intestinal epithelial cell line. J Clin Invest. 1999 Oct; 104(7):903-11.
  101. Lencer WI. Floating the molecular machinery for t-cell activation. Gastroenterology. 1999 Aug; 117(2):503-5.
  102. Lencer WI, Hirst TR, Holmes RK. Membrane traffic and the cellular uptake of cholera toxin. Biochim Biophys Acta. 1999 Jul 8; 1450(3):177-90.
  103. Blumberg RS, Lencer WI, Zhu X, Kim HS, Claypool S, Balk SP, Saubermann LJ, Colgan SP. Antigen presentation by intestinal epithelial cells. Immunol Lett. 1999 Jun 15; 69(1):7-11.
  104. Beauregard KE, Wimer-Mackin S, Collier RJ, Lencer WI. Anthrax toxin entry into polarized epithelial cells. Infect Immun. 1999 Jun; 67(6):3026-30.
  105. Rodighiero C, Aman AT, Kenny MJ, Moss J, Lencer WI, Hirst TR. 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.
  106. Lencer WI. Mucosal vaccination: "all politics are local". Gastroenterology. 1999 Feb; 116(2):497-9.
  107. Lencer WI, Alper SL. The potassium channel and how it works. Gastroenterology. 1999 Jan; 116(1):216-7.
  108. Rodighiero C, Aman AT, Lencer WI, Hirst TR. 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.
  109. Merlin D, Jiang L, Strohmeier GR, Nusrat A, Alper SL, Lencer WI, Madara JL. Distinct Ca2+- and cAMP-dependent anion conductances in the apical membrane of polarized T84 cells. Am J Physiol. 1998 Aug; 275(2 Pt 1):C484-95.
  110. Lencer WI. Paneth cells: on the front line or in the backfield? Gastroenterology. 1998 Jun; 114(6):1343-5.
  111. Wolf AA, Jobling MG, Wimer-Mackin S, Ferguson-Maltzman M, Madara JL, Holmes RK, Lencer WI. 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.
  112. Lencer WI. Acid secretion, ulcer disease, and cell biology. Gastroenterology. 1998 Mar; 114(3):607-8.
  113. Rufo PA, Merlin D, Riegler M, Ferguson-Maltzman MH, Dickinson BL, Brugnara C, Alper SL, Lencer WI. 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.
  114. Lencer WI, Cheung G, Strohmeier GR, Currie MG, Ouellette AJ, Selsted ME, Madara JL. Induction of epithelial chloride secretion by channel-forming cryptdins 2 and 3. Proc Natl Acad Sci U S A. 1997 Aug 5; 94(16):8585-9.
  115. Lencer WI, Constable C, Moe S, Rufo PA, Wolf A, Jobling MG, Ruston SP, Madara JL, Holmes RK, Hirst TR. 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.
  116. Strohmeier GR, Lencer WI, Patapoff TW, Thompson LF, Carlson SL, Moe SJ, Carnes DK, Mrsny RJ, Madara JL. Surface expression, polarization, and functional significance of CD73 in human intestinal epithelia. J Clin Invest. 1997 Jun 1; 99(11):2588-601.
  117. Rufo PA, Jiang L, Moe SJ, Brugnara C, Alper SL, Lencer WI. The antifungal antibiotic, clotrimazole, inhibits Cl- secretion by polarized monolayers of human colonic epithelial cells. J Clin Invest. 1996 Nov 1; 98(9):2066-75.
  118. Frey A, Giannasca KT, Weltzin R, Giannasca PJ, Reggio H, Lencer WI, Neutra MR. 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 1; 184(3):1045-59.
  119. Turner JR, Lencer WI, Carlson S, Madara JL. 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.
  120. Lencer WI, Constable C, Moe S, Jobling MG, Webb HM, Ruston S, Madara JL, Hirst TR, Holmes RK. 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.
  121. Lencer WI, Moe S, Rufo PA, Madara JL. Transcytosis of cholera toxin subunits across model human intestinal epithelia. Proc Natl Acad Sci U S A. 1995 Oct 24; 92(22):10094-8.
  122. Lencer WI, Strohmeier G, Moe S, Carlson SL, Constable CT, Madara JL. Signal transduction by cholera toxin: processing in vesicular compartments does not require acidification. Am J Physiol. 1995 Oct; 269(4 Pt 1):G548-57.
  123. Strohmeier GR, Reppert SM, Lencer WI, Madara JL. The A2b adenosine receptor mediates cAMP responses to adenosine receptor agonists in human intestinal epithelia. J Biol Chem. 1995 Feb 3; 270(5):2387-94.
  124. Hirst TR, Nashar TO, Eaglestone S, Lencer WI, Webb HM, Yu J. 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.
  125. Dosanjh A, Lencer W, Brown D, Ausiello DA, Stow JL. Heterologous expression of delta F508 CFTR results in decreased sialylation of membrane glycoconjugates. Am J Physiol. 1994 Feb; 266(2 Pt 1):C360-6.
  126. Apter FM, Lencer WI, Finkelstein RA, Mekalanos JJ, Neutra MR. 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.
  127. Lencer WI, de Almeida JB, Moe S, Stow JL, Ausiello DA, Madara JL. 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.
  128. Lencer WI, Delp C, Neutra MR, Madara JL. 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.
  129. Madara JL, Parkos C, Colgan S, MacLeod RJ, Nash S, Matthews J, Delp C, Lencer W. Cl- secretion in a model intestinal epithelium induced by a neutrophil-derived secretagogue. J Clin Invest. 1992 Jun; 89(6):1938-44.
  130. Lencer WI, Brown D, Ausiello DA, Verkman AS. 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.
  131. Lencer WI, Verkman AS, Arnaout MA, Ausiello DA, Brown D. 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.
  132. Shi LB, Ye RG, Lencer WI, Verkman AS. [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.
  133. Lencer WI, Weyer P, Verkman AS, Ausiello DA, Brown D. FITC-dextran as a probe for endosome function and localization in kidney. Am J Physiol. 1990 Feb; 258(2 Pt 1):C309-17.
  134. Lencer WI, Reinhart FD, Neutra MR. Interaction of cholera toxin with cloned human goblet cells in monolayer culture. Am J Physiol. 1990 Jan; 258(1 Pt 1):G96-102.
  135. Ye RG, Shi LB, Lencer WI, Verkman AS. Functional colocalization of water channels and proton pumps in endosomes from kidney proximal tubule. J Gen Physiol. 1989 May; 93(5):885-902.
  136. Verkman AS, Lencer WI, Brown D, Ausiello DA. Endosomes from kidney collecting tubule cells contain the vasopressin-sensitive water channel. Nature. 1988 May 19; 333(6170):268-9.
  137. Lencer WI, Chu SH, Walker WA. Differential binding kinetics of cholera toxin to intestinal microvillus membrane during development. Infect Immun. 1987 Dec; 55(12):3126-30.
  138. Rubin S, Salomon M, Walleigh L, Lencer W, Bauchner H, Shalen W, Klein K, Summergrad P. Unionization of house staff. N Engl J Med. 1979 Nov 8; 301(19):1068.
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