Jerrold R Turner

University of Chicago, Chicago, Illinois, United States

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Publications (219)2219.25 Total impact

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    ABSTRACT: Multi-organ failure contributes to mortality in bacterial sepsis. Platelet and immune cell activation contribute to organ injury during sepsis, but the mechanisms by which bacterial virulence factors initiate these responses remain poorly defined. We demonstrate that during lethal sepsis, Staphylococcus aureus α-toxin simultaneously alters platelet activation and promotes neutrophil inflammatory signaling through interactions with its cellular receptor ADAM10. Platelet intoxication prevents endothelial barrier repair and facilitates formation of injurious platelet-neutrophil aggregates, contributing to lung and liver injury that is mitigated by ADAM10 deletion on platelets and myeloid lineage cells. While platelet- or myeloid-specific ADAM10 knockout does not alter sepsis mortality, double-knockout animals are highly protected. These results define a pathway by which a single bacterial toxin utilizes a widely expressed receptor to coordinate progressive, multi-organ disease in lethal sepsis. As an expression-enhancing ADAM10 polymorphism confers susceptibility to severe human sepsis, these studies highlight the importance of understanding molecular host-microbe interactions. Copyright © 2015 Elsevier Inc. All rights reserved.
    Cell host & microbe 06/2015; 17(6):775-787. DOI:10.1016/j.chom.2015.05.011 · 12.33 Impact Factor
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    ABSTRACT: The members of the large family of claudin proteins regulate ion and water flux across the tight junction. Many claudins, e.g. claudins 2 and 15, accomplish this by forming size- and charge-selective paracellular channels. Claudins also appear to be essential for genesis of tight junction strands and recruitment of other proteins to these sites. What is less clear is whether claudins also form the paracellular seal. While this seal is defective when claudins are disrupted, some results, including ultrastructural and biochemical data, suggest that lipid structures are an important component of tight junction strands and may be responsible for the paracellular seal. This review highlights the current knowledge of claudins to barrier function and tight junction structure and suggests a model by which claudins and other tight junction proteins can drive assembly and stabilization of a lipid-based strand structure. Copyright © 2015 Elsevier Ltd. All rights reserved.
    Seminars in Cell and Developmental Biology 05/2015; 42. DOI:10.1016/j.semcdb.2015.04.008 · 6.27 Impact Factor
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    ABSTRACT: Background & aims: The mechanisms of tissue destruction during progression of celiac disease are poorly defined. It is not clear how tissue stress and adaptive immunity contribute to the activation of intraepithelial cytotoxic T cells and the development of villous atrophy. We analyzed epithelial cells and intraepithelial cytotoxic T cells in family members of patients with celiac disease, who were without any signs of adaptive antigluten immunity, and in potential celiac disease patients, who have antibodies against tissue transglutaminase 2 in the absence of villous atrophy. Methods: We collected blood and intestinal biopsy specimens from 268 patients at tertiary medical centers in the United States and Italy from 2004 to 2012. All subjects had normal small intestinal histology. Study groups included healthy individuals with no family history of celiac disease or antibodies against tissue transglutaminase 2 (controls), healthy family members of patients with celiac disease, and potential celiac disease patients. Intraepithelial cytotoxic T cells were isolated and levels of inhibitory and activating natural killer (NK) cells were measured by flow cytometry. Levels of heat shock protein (HSP) and interleukin 15 were measured by immunohistochemistry, and ultrastructural alterations in intestinal epithelial cells (IECs) were assessed by electron microscopy. Results: IECs from subjects with a family history of celiac disease, but not from subjects who already had immunity to gluten, expressed higher levels of HS27, HSP70, and interleukin-15 than controls; their IECs also had ultrastructural alterations. Intraepithelial cytotoxic T cells from relatives of patients with celiac disease expressed higher levels of activating NK receptors than cells from controls, although at lower levels than patients with active celiac disease, and without loss of inhibitory receptors for NK cells. Intraepithelial cytotoxic T cells from potential celiac disease patients failed to up-regulate activating NK receptors. Conclusions: A significant subset of healthy family members of patients with celiac disease with normal intestinal architecture had epithelial alterations, detectable by immunohistochemistry and electron microscopy. The adaptive immune response to gluten appears to act in synergy with epithelial stress to allow intraepithelial cytotoxic T cells to kill epithelial cells and induce villous atrophy in patients with active celiac disease.
    Gastroenterology 05/2015; 149(3). DOI:10.1053/j.gastro.2015.05.013 · 16.72 Impact Factor
  • H. Aimee Kwak · Jerrold R. Turner
    Gastroenterology 05/2015; DOI:10.1053/j.gastro.2015.05.018 · 16.72 Impact Factor
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    ABSTRACT: Excess circulating iron is stored in the liver, and requires reduction of non-Tf-bound-iron (NTBI) and transferrin (Tf)-iron at the plasma membrane and endosomes respectively by ferrireductase (FR) proteins for transport across biological membranes through divalent metal transporters. Here, we report that prion-protein (PrP(C)), a ubiquitously expressed glycoprotein most abundant on neuronal cells, functions as a FR partner for divalent-metal transporter-1 (DMT1) and ZIP14. Thus, absence of PrP(C) in PrP-knock-out (PrP(-/-)) mice resulted in markedly reduced liver iron stores, a deficiency that was not corrected by chronic or acute administration of iron by the oral or intra-peritoneal routes. Likewise, preferential radiolabeling of circulating NTBI with (59)Fe revealed significantly reduced uptake and storage of NTBI by the liver of PrP(-/-) mice relative to matched PrP(+/+) controls. However, uptake, storage, and utilization of ferritin-bound iron that does not require reduction for uptake was increased in PrP(-/-) mice, indicating a compensatory response to the iron-deficiency. Expression of exogenous PrP(C) in HepG2-cells increased uptake and storage of ferric-iron (Fe(3+)), not ferrous-iron (Fe(2+)) from the medium, supporting the function of PrP(C) as a plasma membrane FR. Co-expression of PrP(C) with ZIP14 and DMT1 in HepG2 cells increased uptake of Fe(3+) significantly, and surprisingly, increased the ratio of N-terminally truncated PrP(C) forms lacking the FR domain relative to full-length PrP(C). Together, these observations indicate that PrP(C) promotes, and possibly regulates the uptake of NTBI through DMT1 and Zip14 via its FR activity. Implications of these observations for neuronal iron homeostasis under physiological and pathological conditions are discussed. Copyright © 2015. Published by Elsevier Inc.
    Free Radical Biology and Medicine 04/2015; 84. DOI:10.1016/j.freeradbiomed.2015.03.037 · 5.74 Impact Factor
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    ABSTRACT: Substance P (SP), neurokinin-1 receptors (NK-1Rs) are expressed in mesenteric preadipocytes and SP binding activates proinflammatory signalling in these cells. We evaluated the expression levels of SP (Tac-1), NK-1R (Tacr-1), and NK-2R (Tacr-2) mRNA in preadipocytes isolated from patients with Inflammatory Bowel Disease (IBD) and examined their responsiveness to SP compared to control human mesenteric preadipocytes. The Aim of our study is to investigate the effects of the neuropeptide SP on cytokine expression in preadipocytes of IBD vs control patients and evaluate the potential effects of these cells on IBD pathophysiology via SP-NK-R interactions.
    03/2015; 245(4). DOI:10.1016/j.jcmgh.2015.03.003
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    ABSTRACT: Intraepithelial lymphocytes that express the γδ T cell receptor (γδ IELs) limit pathogen translocation across the intestinal epithelium by unknown mechanisms. We investigated whether γδ IEL migration and interaction with epithelial cells promote mucosal barrier maintenance during enteric infection. Salmonella typhimurium or Toxoplasma gondii were administered to γδ T cell-deficient (Tcrd KO), CD103-deficient (CD103 KO), or control TcrdEGFP C57BL/6 reporter mice. Intravital microscopy was used to visualize migration of GFP-tagged γδ T cells within the small intestinal mucosa of mice infected with DsRed-labeled S typhimurium. Mixed bone marrow chimeras were generated to assess the effects of γδ IEL migration on early pathogen invasion and chronic systemic infection. Morphometric analyses of intravital video microscopy data showed that γδ IELs rapidly localized to and remained near epithelial cells in direct contact with bacteria. Within 1 hr, greater numbers of T gondii or S typhimurium were present within mucosae of mice with migration-defective occludin KO γδ T cells, compared with controls. Pathogen invasion in Tcrd KO mice was quantitatively similar to that in mice with occludin-deficient γδ T cells, whereas invasion in CD103 KO mice, which have increased migration of γδ T cells into the lateral intercellular space, was reduced by 63%. Consistent with a role of γδ T cell migration in early host defense, systemic salmonellosis developed more rapidly and with greater severity in mice with occludin-deficient γδ IELs, relative to those with wild-type or CD103 KO γδ IELs. In mice, intraepithelial migration to epithelial cells in contact with pathogens is essential to γδ IEL surveillance and immediate host defense. γδ IEL occludin is required for early surveillance that limits systemic disease. Copyright © 2015 AGA Institute. Published by Elsevier Inc. All rights reserved.
    Gastroenterology 03/2015; 148(7). DOI:10.1053/j.gastro.2015.02.053 · 16.72 Impact Factor
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    ABSTRACT: In vitro, infection of polarized human intestinal epithelial cells by Coxsackievirus B3 (CVB3) depends on virus interaction with decay accelerating factor (DAF), a receptor expressed on the apical cell surface. Although mice are highly susceptible to CVB3 infection when virus is delivered by intraperitoneal injection, infection by the enteral route is very inefficient. Murine DAF, unlike human DAF, does not bind virus, and we hypothesized that the absence of an accessible receptor on the intestinal surface is an important barrier to infection by the oral route. We generated transgenic mice that express human DAF specifically on intestinal epithelium, and measured their susceptibility to infection by a DAF-binding CVB3 isolate. Human DAF permitted CVB3 to bind to the intestinal surface ex vivo, and to infect polarized monolayers of small-intestinal epithelial cells derived from DAF-transgenic mice. However, expression of human DAF did not facilitate infection by the enteral route, either in immunocompetent animals or in animals deficient in the interferon alpha/beta receptor. These results indicate that the absence of an apical receptor on intestinal epithelium is not the major barrier to infection of mice by the oral route. CVB3 infection of human intestinal epithelial cells depends on DAF at the apical cell surface, and expression of human DAF on murine intestinal epithelial cells permits their infection in vitro. However, expression of human DAF on the intestinal surface of transgenic mice did not facilitate infection by the oral route. Although the role of intestinal DAF in human infection has not been directly examined, these results suggest that DAF is not the critical factor in mice. Copyright © 2015, American Society for Microbiology. All Rights Reserved.
    Journal of Virology 02/2015; 89(8). DOI:10.1128/JVI.03468-14 · 4.44 Impact Factor
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    ABSTRACT: In Inflammatory Bowel Disease (IBD), obesity is associated with worsening of the course of disease. Here we examined the role obesity in the development of colitis and studied mesenteric fat-epithelial cell interactions in patients with IBD. We combined the diet-induce obesity (DIO) with the Trinitrobenzene Sulfonic Acid (TNBS) colitis mouse model to create groups with obesity, colitis, and their combination. Changes in the mesenteric fat and intestine were assessed by histology, myeloperoxidase (MPO) assay and cytokine mRNA expression by real-time PCR. Medium from human mesenteric fat and cultured preadipocytes was obtained from obese and IBD patients. Histological analysis showed inflammatory cell infiltrate and increased histological damage in the intestine and mesenteric fat of obese mice with colitis compared to all other groups. Obesity also increased the expression of proinflammatory cytokines including IL-1β, TNFα, MCP-1 and KC while it decreased the TNBS-induced increases in IL-2 and IFNγ in mesenteric adipose and intestinal tissues. Human mesenteric fat isolated from obese and IBD patients demonstrated differential release of adipokines and growth factors compared to controls. Fat conditioned media reduced adiponectin receptor 1 (AdipoR1) expression in human NCM460 colonic epithelial cells. AdipoR1 intracolonic silencing in mice exacerbated TNBS-induced colitis. In conclusion, obesity worsens the outcome of experimental colitis and obesity and IBD-associated changes in adipose tissue promote differential mediator release in mesenteric fat that modulate colonocyte responses and may affect the course of colitis. Our results also suggest an important role for AdipoR1 for the fat-intestinal axis in the regulation of inflammation during colitis. Copyright © 2014, American Journal of Physiology- Gastrointestinal and Liver Physiology.
    AJP Gastrointestinal and Liver Physiology 01/2015; 308(7):ajpgi.00269.2014. DOI:10.1152/ajpgi.00269.2014 · 3.80 Impact Factor
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    ABSTRACT: Tight junctions create a paracellular barrier that is essential for survival of complex organisms. In many cases tight junctions define separate, generally sterile, tissue compartments. In the skin and gut, tight junctions must also seal the paracellular space to prevent microbiota from accessing the internal milieu. This is a relatively simple task in the integument, where an absolute barrier is effective. However, intestinal epithelial tight junctions are charged with the far more complex task of supporting paracellular transport of water, ions, and nutrients while providing a barrier to microbial translocation. The delicate nature of this balance, which is disrupted in disease, makes the intestine a unique organ in which to explore the complexities of tight junction permeability and barrier regulation. Here we review recent progress in understanding the molecular determinants of barrier function and events responsible for regulation, and dysregulation, of tight junction permeability.
    Seminars in Cell and Developmental Biology 09/2014; 36. DOI:10.1016/j.semcdb.2014.09.022 · 6.27 Impact Factor
  • Peng Chen · Peter Stärkel · Jerrold R. Turner · Samuel B. Ho · Bernd Schnabl
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    ABSTRACT: Unlabelled: Intestinal barrier dysfunction is an important contributor to alcoholic liver disease (ALD). Translocated microbial products trigger an inflammatory response in the liver and contribute to steatohepatitis. Our aim was to investigate mechanisms of barrier disruption after chronic alcohol feeding. A Lieber-DeCarli model was used to induce intestinal dysbiosis, increased intestinal permeability, and liver disease in mice. Alcohol feeding for 8 weeks induced intestinal inflammation in the jejunum, which is characterized by an increased number of tumor necrosis factor alpha (TNF-α)-producing monocytes and macrophages. These findings were confirmed in duodenal biopsies from patients with chronic alcohol abuse. Intestinal decontamination with nonabsorbable antibiotics restored eubiosis, decreased intestinal inflammation and permeability, and reduced ALD in mice. TNF-receptor I (TNFRI) mutant mice were protected from intestinal barrier dysfunction and ALD. To investigate whether TNFRI on intestinal epithelial cells mediates intestinal barrier dysfunction and ALD, we used TNFRI mutant mice carrying a conditional gain-of-function allele for this receptor. Reactivation of TNFRI on intestinal epithelial cells resulted in increased intestinal permeability and liver disease that is similar to wild-type mice after alcohol feeding, suggesting that enteric TNFRI promotes intestinal barrier dysfunction. Myosin light-chain kinase (MLCK) is a downstream target of TNF-α and was phosphorylated in intestinal epithelial cells after alcohol administration. Using MLCK-deficient mice, we further demonstrate a partial contribution of MLCK to intestinal barrier dysfunction and liver disease after chronic alcohol feeding. Conclusion: Dysbiosis-induced intestinal inflammation and TNFRI signaling in intestinal epithelial cells mediate a disruption of the intestinal barrier. Therefore, intestinal TNFRI is a crucial mediator of ALD.
    Hepatology 09/2014; 61(3). DOI:10.1002/hep.27489 · 11.06 Impact Factor
  • Gastrointestinal Endoscopy 09/2014; 80(3):516–517. DOI:10.1016/j.gie.2014.07.022 · 5.37 Impact Factor
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    ABSTRACT: Approximately half of all adult burn patients are intoxicated at the time of their injury and have worsened clinical outcomes compared to those without prior alcohol exposure. This study tested the hypothesis that intoxication alters the gut-liver axis leading to increased pulmonary inflammation mediated by burn-induced IL-6 in the liver. To this end, C57BL/6 mice were given 1.2 g/kg ethanol 30 minutes prior to a 15% total body surface area burn. To restore gut barrier function, a specific myosin light chain kinase inhibitor [membrane-permeant inhibitor of kinase (PIK)] was administered 30 minutes after injury which we have demonstrated to reduce bacterial translocation from the gut. Limiting bacterial translocation with PIK attenuated hepatic damage as measured by a 47% reduction in serum alanine aminotransferase (p<0.05) as well as a 33% reduction in hepatic IL-6 mRNA expression (p<0.05) compared to intoxicated burned mice without PIK. This mitigation of hepatic damage was associated with a 49% decline in pulmonary neutrophil infiltration (p<0.05) and decreased alveolar wall thickening compared to matched controls. These results were reproduced by prophylactically reducing the bacterial load in the intestines with oral antibiotics before intoxication and burn. Overall these data suggest the gut-liver axis is deranged when intoxication precedes burn and that limiting bacterial translocation in this setting attenuates hepatic damage and pulmonary inflammation.
    AJP Gastrointestinal and Liver Physiology 08/2014; 307(7). DOI:10.1152/ajpgi.00185.2014 · 3.80 Impact Factor
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    ABSTRACT: Previous studies have shown a correlation between pretransplant conditioning intensity, intestinal barrier loss, and graft-versus-host disease (GVHD) severity. However, because irradiation and other forms of pretransplant conditioning have pleiotropic effects, the precise role of intestinal barrier loss in GVHD pathogenesis remains unclear. We developed GVHD models that allowed us to isolate the specific contributions of distinct pretransplant variables. Intestinal damage was required for the induction of minor mismatch [major histocompatibility complex (MHC)-matched] GVHD, but was not necessary for major mismatch GVHD, demonstrating fundamental pathogenic distinctions between these forms of disease. Moreover, recipient natural killer (NK) cells prevented minor mismatch GVHD by limiting expansion and target organ infiltration of alloreactive T cells via a perforin-dependent mechanism, revealing an immunoregulatory function of MHC-matched recipient NK cells in GVHD. Minor mismatch GVHD required MyD88-mediated Toll-like receptor 4 (TLR4) signaling on donor cells, and intestinal damage could be bypassed by parenteral lipopolysaccharide (LPS) administration, indicating a critical role for the influx of bacterial components triggered by intestinal barrier loss. In all, the data demonstrate that pretransplant conditioning plays a dual role in promoting minor mismatch GVHD by both depleting recipient NK cells and inducing intestinal barrier loss.
    Science translational medicine 07/2014; 6(243):243ra87. DOI:10.1126/scitranslmed.3008941 · 15.84 Impact Factor
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    ABSTRACT: Abnormal bacterial adherence and internalization in enterocytes have been documented in Crohn disease, celiac disease, surgical stress, and intestinal obstruction and are associated with low-level interferon (IFN)-γ production. How commensals gain access to epithelial soma through densely packed microvilli rooted on the terminal web (TW) remains unclear. We investigated molecular and ultrastructural mechanisms of bacterial endocytosis, focusing on regulatory roles of IFN-γ and myosin light chain kinase (MLCK) in TW myosin phosphorylation and brush border fanning. Mouse intestines were sham operated on or obstructed for 6 hours by loop ligation with intraluminally administered ML-7 (a MLCK inhibitor) or Y27632 (a Rho-associated kinase inhibitor). After intestinal obstruction, epithelial endocytosis and extraintestinal translocation of bacteria were observed in the absence of tight junctional damage. Enhanced TW myosin light chain phosphorylation, arc formation, and brush border fanning coincided with intermicrovillous bacterial penetration, which were inhibited by ML-7 and neutralizing anti-IFN-γ but not Y27632. The phenomena were not seen in mice genetically deficient for long MLCK-210 or IFN-γ. Stimulation of human Caco-2BBe cells with IFN-γ caused MLCK-dependent TW arc formation and brush border fanning, which preceded caveolin-mediated bacterial internalization through cholesterol-rich lipid rafts. In conclusion, epithelial MLCK-activated brush border fanning by IFN-γ promotes adherence and internalization of normally noninvasive enteric bacteria. Transcytotic commensal penetration may contribute to initiation or relapse of chronic inflammation.
    American Journal Of Pathology 06/2014; 184(8). DOI:10.1016/j.ajpath.2014.05.003 · 4.59 Impact Factor
  • Digestive disease week, Chicago; 05/2014
  • Gastroenterology 05/2014; 146(5):S-521. DOI:10.1016/S0016-5085(14)61887-4 · 16.72 Impact Factor
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    ABSTRACT: BACKGROUND & AIMS: Expression of the tight junction protein claudin-2 (cldn2), which forms a pore that mediates paracellular Na+ and water flux, is increased in colitis. We have shown that cldn2-/- mice are partially protected from adoptive transfer (AT) colitis, as demonstrated by reductions in stool Na+ and water content as well as mucosal cytokines. In vitro studies have shown that dephosphorylation of S408 within the occludin C-terminus drives assembly of a protein complex that includes cldn2 and disrupts pore function. CK2 is the primary kinase that phosphorylates S408, and in vitro studies have shown that CK2 inhibition can restore epithelial barrier function following IL-13-induced cldn2 expression in epithelial monolayers. However, some data suggest that CK2 may contribute to epithelial homeostasis in DSS colitis. Our aim was to determine whether in vivo CK2 inhibition could be beneficial in colitis. METHODS: Colitis was induced by AT or DSS using established methods in wild type (WT), cldn2-/-, and Rag1-/- mice. The orally-bioavailable CK2 inhibitor CX4945 was delivered daily by gavage. RESULTS: CX4945 markedly improved distal colonic histopathology in DSS-treated mice. DSS treatment resulted in complete loss of surface epithelium, mucin depletion, and diffuse ulceration within the distal colon of mice treated with daily saline gavage, while CX4945-treated mice demonstrated intact surface epithelium, normal goblet cell maturation, and only minor damage. Consistent with this, colonic permeability to 4kD dextran was 1.9±0.2-fold less in CX4945 treated mice (P<0.05). CX4945 also delayed DSS-induced weight loss and disease progression. Effects of CX4945 were similar in WT and cldn2-/- mice, indicating that CK2 inhibition limits DSS colitis by a cldn2- independent mechanism and that CK2 activity is not essential for epithelial homeostasis. To assess the effect of CK2 inhibition in an IBD-relevant model of immune mediated colitis, Rag1-/- and cldn2 -/-Rag1-/- mice were treated with CX4945 beginning 10 days after CD4+CD45Rbhi AT. CX4945 reduced increases in stool Na+ and water content, colonic 4kD dextran permeability (2.1±0.5-fold less in CX4945-treated mice) , mucosal cytokine production, weight loss, histopathology in Rag1-/- mice (P<0.05), but had no benefit in cldn2 -/-Rag1-/- mice; parameters were similar in CX4945-treated Rag1-/- mice and either CX4945-treated or saline-treated cldn2 -/-Rag1-/- mice. CONCLUSIONS: In vivo cldn2- mediated pore function can be inhibited by CK2 inhibition and that this can be an effective therapeutic target in experimental IBD. The data also remove concerns that CK2 activity is essential for mucosal homeostasis in colitis and, conversely, indicate that CK2 inhibition can limit intestinal damage by both cldn2-dependent and cldn2-independent mechanisms. Clinical trials of CK2 inhibitors are indicated in IBD.
    Gastroenterology 05/2014; 146(5):S-80. DOI:10.1016/S0016-5085(14)60288-2 · 16.72 Impact Factor
  • Matthew A. Odenwald · Aaron L. Hecht · Jerrold R. Turner
    Gastroenterology 05/2014; 146(5):S-36. DOI:10.1016/S0016-5085(14)60125-6 · 16.72 Impact Factor
  • Gastroenterology 05/2014; 146(5):S-823. DOI:10.1016/S0016-5085(14)62986-3 · 16.72 Impact Factor

Publication Stats

8k Citations
2,219.25 Total Impact Points


  • 2002–2015
    • University of Chicago
      • Department of Pathology
      Chicago, Illinois, United States
  • 2013
    • The University of Chicago Medical Center
      • Department of Pathology
      Chicago, Illinois, United States
  • 2012
    • Medical College of Wisconsin
      • Department of Pathology
      Milwaukee, Wisconsin, United States
  • 2005–2011
    • University of Illinois at Chicago
      • Department of Medicine (Chicago)
      Chicago, Illinois, United States
    • Johns Hopkins University
      Baltimore, Maryland, United States
    • The University of Calgary
      • Department of Biological Sciences
      Calgary, Alberta, Canada
  • 2009
    • University of Pittsburgh
      • Department of Cell Biology and Physiology
      Pittsburgh, Pennsylvania, United States
    • University of Tuebingen
      Tübingen, Baden-Württemberg, Germany
  • 2007
    • Harvard University
      Cambridge, Massachusetts, United States
  • 2000–2001
    • Wayne State University
      • Department of Pathology
      Detroit, MI, United States