Joseph F Urban

Sun Yat-Sen University, Shengcheng, Guangdong, China

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Publications (211)1421.95 Total impact

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    ABSTRACT: We examined the role of innate cells in acquired resistance to the natural murine parasitic nematode, Nippostrongylus brasiliensis. Macrophages obtained from lungs as late as 45 d after N. brasiliensis inoculation were able to transfer accelerated parasite clearance to naive recipients. Primed macrophages adhered to larvae in vitro and triggered increased mortality of parasites. Neutrophil depletion in primed mice abrogated the protective effects of transferred macrophages and inhibited their in vitro binding to larvae. Neutrophils in parasite-infected mice showed a distinct transcriptional profile and promoted alternatively activated M2 macrophage polarization through secretory factors including IL-13. Differentially activated neutrophils in the context of a type 2 immune response therefore prime a long-lived effector macrophage phenotype that directly mediates rapid nematode damage and clearance.
    Nature immunology. 08/2014;
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    ABSTRACT: How the immune system adapts to malnutrition to sustain immunity at barrier surfaces, such as the intestine, remains unclear. Vitamin A deficiency is one of the most common micronutrient deficiencies and is associated with profound defects in adaptive immunity. Here, we found that type 3 innate lymphoid cells (ILC3s) are severely diminished in vitamin A-deficient settings, which results in compromised immunity to acute bacterial infection. However, vitamin A deprivation paradoxically resulted in dramatic expansion of interleukin-13 (IL-13)-producing ILC2s and resistance to nematode infection in mice, which revealed that ILCs are primary sensors of dietary stress. Further, these data indicate that, during malnutrition, a switch to innate type 2 immunity may represent a powerful adaptation of the immune system to promote host survival in the face of ongoing barrier challenges.
    Science 01/2014; 343(6169):432-7. · 31.20 Impact Factor
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    ABSTRACT: Parasitic enteric nematodes induce a type 2 immune response characterized by increased production of Th2 cytokines, IL-4 and IL-13, and recruitment of alternatively activated macrophages (M2) to the site of infection. Nematode infection is associated with changes in epithelial permeability and inhibition of sodium-linked glucose absorption, but the role of M2 in these effects is unknown. Clodronate-containing liposomes were administered prior to and during nematode infection to deplete macrophages and prevent the development of M2 in response to infection with Nippostrongylus brasiliensis. The inhibition of epithelial glucose absorption that is associated with nematode infection involved a macrophage-dependent reduction in SGLT1 activity, with no change in receptor expression, and a macrophage-independent down-regulation of GLUT2 expression. The reduced transport of glucose into the enterocyte is compensated partially by an up-regulation of the constitutive GLUT1 transporter consistent with stress-induced activation of HIF-1α. Thus, nematode infection results in a "lean" epithelial phenotype that features decreased SGLT1 activity, decreased expression of GLUT2 and an emergent dependence on GLUT1 for glucose uptake into the enterocyte. Macrophages do not play a role in enteric nematode infection-induced changes in epithelial barrier function. There is a greater contribution, however, of paracellular absorption of glucose to supply the energy demands of host resistance. These data provide further evidence of the ability of macrophages to alter glucose metabolism of neighboring cells.
    PLoS ONE 01/2014; 9(1):e84763. · 3.53 Impact Factor
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    ABSTRACT: Liver X receptors (LXR) play an integral role in cholesterol metabolism and the inflammatory response. High-fat (HF) diets and microbial infection can antagonize the LXR pathway leading to accumulation of cholesteryl-esters (CE) and increased expression of pro-inflammatory mediators in macrophages. The probiotic bacteria Lactobacillus paracasei possesses cholesterol lowering and immune modulating properties. Therefore, the present study sought to model whether daily feeding of L. paracasei to juvenile Ossabaw pigs fed a HF diet could modulate cholesterol metabolism and the LXR/inflammatory axis in lipopolysacharide (LPS)-stimulated alveolar macrophages (AM). The results showed that AM from pigs fed a HF diet had significantly higher concentrations of CE compared to AM from pigs fed a control (C) diet, but not in pigs fed a HF diet with L. paracasei (HFPB). Ex vivo LPS stimulation of AM opposed LXR agonist-mediated transcription of cholesterol metabolism related genes: ABCA1, CH25H and PPARγ in pigs on the C diet, and LXRα, ABCA1, ABCG1, CH25H and PPARγ in pigs on the HF diet. This effect was abrogated for all these genes except LXRα in AM from pigs given L. paracasei. Protein analysis of culture supernatants revealed that AM from HFPB-fed pigs had significantly lower LPS-induced protein expression of IL-1β than AM from HF-fed pigs. Moreover, AM from pigs fed the C diet and given L. paracasei, had significantly higher mRNA levels of IL-8, and IL-6, in response to LPS. These data demonstrated a role for L. paracasei in modulating AM cholesterol metabolism and the response to LPS.
    The Journal of nutritional biochemistry 09/2013; · 4.29 Impact Factor
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    ABSTRACT: Typical clinical biomarker analyses on urine and plasma samples from human dietary interventions do not provide adequate information about diet-induced metabolic changes taking place in tissues. The aim of this study was to show how a large-scale non-targeted metabolomic approach can be used to reveal metabolite groups for generating new hypotheses of obesity-related metabolic disturbances produced in an animal model. A large spectrum of metabolites in the semi-polar region, including small water soluble molecules like betaine and dihydroxyindole, and a wide range of bile acids as well as various lipid species were detected. The high fat diet influenced metabolic homeostasis of Ossabaw pigs, especially the lipid metabolome, throughout all the analyzed sample types, including plasma, urine, bile, liver, pancreas, brain cortex, intestinal jejunum and proximal colon. However, even dramatic metabolic changes in tissues were not necessarily observed in plasma and urine. Metabolite profiling involving multiple sample types was shown to be a feasible method for the examination of a wide spectrum of metabolic species extending from small water soluble metabolites to an array of bile acids and lipids, thus pointing to the pathways of metabolism affected by the dietary treatment.
    Journal of Proteome Research 06/2013; · 5.06 Impact Factor
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    ABSTRACT: Heligmosomoides bakeri is a nematode with parasitic development exclusively in the small intestine of infected mice that induces a potent STAT6-dependent Th2 immune response. We previously demonstrated that host protective expulsion of adult H. bakeri from a challenge infection was delayed in selenium (Se) deficient mice. In order to explore mechanisms associated with the delayed expulsion, three-week old female Balb/c mice were placed on a Torula yeast-based diet with or without 0.2 ppm Se, and inoculated five weeks later with H. bakeri infective third-stage larvae (L3), anthelmintic-treated two weeks later, rested, re-inoculated with L3, and evaluated at various times after re-inoculation. Analysis of gene expression in parasite-induced cysts and surrounding tissue isolated from the intestine of infected mice showed that the local tissue Th2 response was decreased in Se deficient mice compared to Se adequate mice. In addition, adult worms recovered from Se deficient mice had higher ATP levels than worms from Se adequate mice indicating greater metabolic activity in the face of a sub-optimal Se-dependent local immune response. Notably, the process of worm expulsion was restored within two to four days after feeding a Se-adequate diet to Se-deficient mice. Expulsion was associated with an increased local expression of Th2-associated genes in the small intestine, intestinal glutathione peroxidase activity, secreted Relm-β protein, anti-H. bakeri IgG1 production, and reduced worm fecundity and ATP-dependent metabolic activity.
    Infection and immunity 05/2013; · 4.21 Impact Factor
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    ABSTRACT: SerpinB2, a member of the serine protease inhibitor family, is expressed by macrophages and is significantly upregulated by inflammation. Recent studies implicated a role for SerpinB2 in the control of Th1 and Th2 immune responses, but the mechanisms of these effects are unknown. In this study, we used mice deficient in SerpinB2 (SerpinB2(-/-)) to investigate its role in the host response to the enteric nematode, Heligmosomoides bakeri. Nematode infection induced a STAT6-dependent increase in intestinal SerpinB2 expression. The H. bakeri-induced upregulation of IL-4 and IL-13 expression was attenuated in SerpinB2(-/-) mice coincident with an impaired worm clearance. In addition, lack of SerpinB2 in mice resulted in a loss of the H. bakeri-induced smooth muscle hypercontractility and a significant delay in infection-induced increase in mucosal permeability. Th2 immunity is generally linked to a CCL2-mediated increase in the infiltration of macrophages that develop into the alternatively activated phenotype (M2). In H. bakeri-infected SerpinB2(-/-) mice, there was an impaired infiltration and alternative activation of macrophages accompanied by a decrease in the intestinal CCL2 expression. Studies in macrophages isolated from SerpinB2(-/-) mice showed a reduced CCL2 expression, but normal M2 development, in response to stimulation of Th2 cytokines. These data demonstrate that the immune regulation of SerpinB2 expression plays a critical role in the development of Th2-mediated protective immunity against nematode infection by a mechanism involving CCL2 production and macrophage infiltration.
    The Journal of Immunology 04/2013; · 5.52 Impact Factor
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    ABSTRACT: Obesity is associated with a chronic low grade inflammation characterized by increased levels of pro-inflammatory cytokines that are implicated in disrupted metabolic homeostasis. Parasitic nematode infection induces a polarized Th2 cytokine response and has been explored to treat autoimmune diseases. We investigated the effects of nematode infection against obesity and the associated metabolic dysfunction. Infection of RIP2-Opa1KO mice or C57BL/6 mice fed a high-fat diet (HFD) with Nippostrongyrus brasiliensis decreased weight gain and was associated with improved glucose metabolism. Infection in HFD obese mice reduced body weight and adipose tissue mass, ameliorated hepatic steatosis associated with a decreased expression of key lipogenic enzymes/mediators, and improved glucose metabolism accompanied by changes in the profile of metabolic hormones. The infection resulted in a phenotypic change in adipose tissue macrophages characterized by up-regulation of alternative activation markers. The IL-13 activation of STAT6 signaling pathway was required for the infection-induced attenuation of steatosis but not for improved glucose metabolism, whereas weight loss was attributed to both IL-13/STAT6-dependent and -independent mechanisms. Parasitic nematode infection has both preventive and therapeutic effects against the development of obesity and associated features of metabolic dysfunction in mice.
    Infection and immunity 03/2013; · 4.21 Impact Factor
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    ABSTRACT: Type 2 immunity is essential for host protection against nematode infection but is detrimental in allergic inflammation or asthma. There is a major research focus on the effector molecules and specific cell types involved in the initiation of type 2 immunity. Recent work has implicated an important role of epithelial-derived cytokines, IL-25 and IL-33, acting on innate immune cells that are believed to be the initial sources of type 2 cytokines IL-4/IL-5/IL-13. The identities of the cell types that mediate the effects of IL-25/IL-33, however, remain to be fully elucidated. In the present study, we demonstrate that macrophages as IL-25/IL-33-responsive cells play an important role in inducing type 2 immunity using both in vitro and in vivo approaches. Macrophages produced type 2 cytokines IL-5 and IL-13 in response to the stimulation of IL-25/IL-33 in vitro, or were the IL-13-producing cells in mice administrated with exogenous IL-33 or infected with Heligmosomoides bakeri. In addition, IL-33 induced alternative activation of macrophages primarily through autocrine IL-13 activating the IL-4Rα-STAT6 pathway. Moreover, depletion of macrophages attenuated the IL-25/IL-33-induced type 2 immunity in mice, while adoptive transfer of IL-33-activated macrophages into mice with a chronic Heligmosomoides bakeri infection induced worm expulsion accompanied by a potent type 2 protective immune response. Thus, macrophages represent a unique population of the innate immune cells pivotal to type 2 immunity and a potential therapeutic target in controlling type 2 immunity-mediated inflammatory pathologies.
    PLoS ONE 01/2013; 8(3):e59441. · 3.53 Impact Factor
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    ABSTRACT: IL-33 is a recently identified cytokine member of the IL-1 family. The biological activities of IL-33 are associated with promotion of Th2 and inhibition of Th1/Th17 immune responses. Exogenous IL-33 induces a typical "type 2" immune response in the gastrointestinal tract, yet the underlying mechanism(s) remain(s) to be fully elucidated. In addition, the role of IL-33 in the regulation of gastrointestinal function is not known. The current study investigated IL-33-dependent intestinal immunity and function in mice. Exogenous IL-33 induced a polarized type 2 cytokine response in the intestine that was entirely MyD88-dependent, but STAT6- and IL-13-independent. Mice injected with recombinant IL-33 exhibited intestinal smooth muscle hypercontractility, decreased epithelial responses to acetylcholine and glucose, and increased mucosal permeability. IL-33 effects on the intestinal epithelial function were STAT6-dependent, and both IL-4 and IL-13 appeared to play a role. The effects on smooth muscle function, however, were attributable to both STAT6-dependent and -independent mechanisms. In addition, IL-13 induction of insulin-like growth factor-1 was implicated in IL-33-induced smooth muscle hypertrophy. Finally, alternative activation of macrophages induced by IL-33 revealed a novel pathway that is IL-4-, IL-13-, and STAT6-independent. Thus, manipulating IL-33 or related signaling pathways represents a potential therapeutic strategy for treating inflammatory diseases associated with dysregulated intestinal function.
    AJP Gastrointestinal and Liver Physiology 12/2012; · 3.65 Impact Factor
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    ABSTRACT: OBJECTIVES:: Diarrhea is a leading cause of mortality and morbidity in children less than five years of age in impoverished regions of the world. Our aim was to compare the fecal microbiota of healthy children to children with clinical diarrhea in a population from a tropical highland in Colombia, South America. Our hypothesis was that a reduced prevalence of inherent Lactobacillus and Bifidobacterium species would be associated with enteric viral and bacterial pathogens. METHODS:: Children between 1 and 5 years of age from two different locations were evaluated for presence of clinical diarrhea. Nucleic acid, isolated from fecal samples, was used to determine by molecular protocols the abundance of inherent bacterial species and presence of enteric pathogens compared to clinically healthy children. The effect of host demographic factors on incidence of diarrhea was also analyzed. RESULTS:: The composition of the fecal microbiota was affected by host demographic factors: age, health status, location, and gender. In partial support of our hypothesis, the relative abundance of commensal Bifidobacterium and Lactobacillus species were inversely correlated with incidence of diarrhea regardless of location. CONCLUSION:: Our results suggested that changes in fecal microbiota composition of children with clinical diarrhea is associated with certain demographic factors that should be considered before designing a prophylactic intervention. Delivery of certain Lactobacillus species and Bifidobacterium species or a diet rich in bifidogenic components that promote growth of Bifidobacterium species could provide a prophylactic effect to ameliorate the impact of diarrhea in children at risk.
    Journal of pediatric gastroenterology and nutrition 12/2012; · 2.18 Impact Factor
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    ABSTRACT: Nematode infections in ruminants are a major impediment to the profitable production of meat and dairy products, especially for small farms. Gastrointestinal parasitism not only negatively impacts weight gain and milk yield, but is also a major cause of mortality in small ruminants. The current parasite control strategy involves heavy use of anthelmintics that has resulted in the emergence of drug-resistant parasite strains. This, in addition to increasing consumer demand for animal products that are free of drug residues has stimulated development of alternative strategies, including selective breeding of parasite resistant ruminants. The development of protective immunity and manifestations of resistance to nematode infections relies upon the precise expression of the host genome that is often confounded by mechanisms simultaneously required to control multiple nematode species as well as ecto- and protozoan parasites, and microbial and viral pathogens. Understanding the molecular mechanisms underlying these processes represents a key step toward development of effective new parasite control strategies. Recent progress in characterizing the transcriptome of both hosts and parasites, utilizing high-throughput microarrays and RNA-seq technology, has led to the recognition of unique interactions and the identification of genes and biological pathways involved in the response to parasitism. Innovative use of the knowledge gained by these technologies should provide a basis for enhancing innate immunity while limiting the polarization of acquired immunity can negatively affect optimal responses to co-infection. Strategies for parasite control that use diet and vaccine/adjuvant combination could be evaluated by monitoring the host transcriptome for induction of appropriate mechanisms for imparting parasite resistance. Knowledge of different mechanisms of host immunity and the critical regulation of parasite development, physiology, and virulence can also selectively identify targets for parasite control. Comparative transcriptome analysis, in concert with genome-wide association (GWS) studies to identify quantitative trait loci (QTLs) affecting host resistance, represents a promising molecular technology to evaluate integrated control strategies that involve breed and environmental factors that contribute to parasite resistance and improved performance. Tailoring these factors to control parasitism without severely affecting production qualities, management efficiencies, and responses to pathogenic co-infection will remain a challenge. This review summarizes recent progress and limitations of understanding regulatory genetic networks and biological pathways that affect host resistance and susceptibility to nematode infection in ruminants.
    Veterinary Parasitology 06/2012; 190(1-2):1-11. · 2.38 Impact Factor
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    ABSTRACT: The extensive similarities between helminth proteins and allergens are thought to contribute to helminth-driven allergic sensitization. The objective of this study was to investigate the cross-reactivity between a major glutathione-S transferase allergen of cockroach (Bla g 5) and the glutathione-S transferase of Wuchereria bancrofti (WbGST), a major lymphatic filarial pathogen of humans. We compared the molecular and structural similarities between Bla g 5 and WbGST by in silico analysis and by linear epitope mapping. The levels of IgE, IgG, and IgG(4) antibodies were measured in filarial-infected and filarial-uninfected patients. Mice were infected with Heligmosomoides bakeri, and their skin was tested for cross-reactive allergic responses. These 2 proteins are 30% identical at the amino acid level with remarkable similarity in the N-terminal region and overall structural conservation based on predicted 3-dimensional models. Filarial infection was associated with IgE, IgG, and IgG(4) anti-Bla g 5 antibody production, with a significant correlation between antibodies (irrespective of isotype) to Bla g 5 and WbGST (P< .0003). Preincubation of sera from cockroach-allergic subjects with WbGST partially depleted (by 50%-70%) anti-Bla g 5 IgE, IgG, and IgG(4) antibodies. IgE epitope mapping of Bla g 5 revealed that 2 linear N-terminal epitopes are highly conserved in WbGST corresponding to Bla g 5 peptides partially involved in the inhibition of WbGST binding. Finally, mice infected with H bakeri developed anti-HbGST IgE and showed immediate-type skin test reactivity to Bla g 5. These data demonstrate that helminth glutathione-S transferase and the aeroallergen Bla g 5 share epitopes that can induce allergic cross-sensitization.
    The Journal of allergy and clinical immunology 04/2012; 130(1):248-56.e9. · 12.05 Impact Factor
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    ABSTRACT: Helminth parasites ensure their survival by regulating host immunity through mechanisms that dampen inflammation. These properties have recently been exploited therapeutically to treat human diseases. The biocomplexity of the intestinal lumen suggests that interactions between the parasite and the intestinal microbiota would also influence inflammation. In this study, we characterized the microbiota in the porcine proximal colon in response to Trichuris suis (whipworm) infection using 16S rRNA gene-based and whole-genome shotgun (WGS) sequencing. A 21-day T. suis infection in four pigs induced a significant change in the composition of the proximal colon microbiota compared to that of three parasite-naive pigs. Among the 15 phyla identified, the abundances of Proteobacteria and Deferribacteres were changed in infected pigs. The abundances of approximately 13% of genera were significantly altered by infection. Changes in relative abundances of Succinivibrio and Mucispirillum, for example, may relate to alterations in carbohydrate metabolism and niche disruptions in mucosal interfaces induced by parasitic infection, respectively. Of note, infection by T. suis led to a significant shift in the metabolic potential of the proximal colon microbiota, where 26% of all metabolic pathways identified were affected. Besides carbohydrate metabolism, lysine biosynthesis was repressed as well. A metabolomic analysis of volatile organic compounds (VOCs) in the luminal contents showed a relative absence in infected pigs of cofactors for carbohydrate and lysine biosynthesis, as well as an accumulation of oleic acid, suggesting altered fatty acid absorption contributing to local inflammation. Our findings should facilitate development of strategies for parasitic control in pigs and humans.
    Infection and immunity 04/2012; 80(6):2150-7. · 4.21 Impact Factor
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    ABSTRACT: Helminths induce potent T helper 2 (TH2)-type immune responses that can mediate worm expulsion, but the role of this response in controlling the acute tissue damage caused by migrating multicellular parasites through vital tissues remains uncertain. We used a helminth infection model in which parasitic nematode larvae migrate transiently through the lung, resulting in hemorrhage and inflammation. We found that IL-17 initially contributed to inflammation and lung damage, whereas subsequent IL-4 receptor (IL-4R) signaling reduced elevations in IL-17 mRNA levels, enhanced the expression of insulin-like growth factor 1 (IGF-1) and IL-10 and stimulated the development of M2 macrophages, all of which contributed to the rapid resolution of tissue damage. These studies indicate an essential role for TH2-type immune responses in mediating acute wound healing during helminth infection.
    Nature medicine 01/2012; 18(2):260-6. · 27.14 Impact Factor
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    ABSTRACT: Helminth infection in pigs serves as an excellent model for the study of the interaction between human malnutrition and parasitic infection and could have important implications in human health. We had observed that pigs infected with Trichuris suis for 21 days showed significant changes in the proximal colon microbiota. In this study, interactions between worm burden and severity of disruptions to the microbial composition and metabolic potentials in the porcine proximal colon microbiota were investigated using metagenomic tools. Pigs were infected by a single dose of T. suis eggs for 53 days. Among infected pigs, two cohorts were differentiated that either had adult worms or were worm-free. Infection resulted in a significant change in the abundance of approximately 13% of genera detected in the proximal colon microbiota regardless of worm status, suggesting a relatively persistent change over time in the microbiota due to the initial infection. A significant reduction in the abundance of Fibrobacter and Ruminococcus indicated a change in the fibrolytic capacity of the colon microbiota in T. suis infected pigs. In addition, ∼10% of identified KEGG pathways were affected by infection, including ABC transporters, peptidoglycan biosynthesis, and lipopolysaccharide biosynthesis as well as α-linolenic acid metabolism. Trichuris suis infection modulated host immunity to Campylobacter because there was a 3-fold increase in the relative abundance in the colon microbiota of infected pigs with worms compared to naïve controls, but a 3-fold reduction in worm-free infected pigs compared to controls. The level of pathology observed in infected pigs with worms compared to worm-free infected pigs may relate to the local host response because expression of several Th2-related genes were enhanced in infected pigs with worms versus those worm-free. Our findings provided insight into the dynamics of the proximal colon microbiota in pigs in response to T. suis infection.
    PLoS ONE 01/2012; 7(4):e35470. · 3.53 Impact Factor
  • Gastroenterology 01/2011; 140(5). · 12.82 Impact Factor
  • Gastroenterology 01/2011; 140(5). · 12.82 Impact Factor
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    ABSTRACT: The pathogenesis of a Citrobacter rodentium infection was evaluated in mice fed diets with a single deficiency in either selenium or vitamin E or with a double deficiency in both selenium and vitamin E compared to mice on nutritionally adequate diets. Mice fed the selenium- and vitamin E-deficient diet for 6 weeks had increased loads of C. rodentium in the colon and spleen, which were not observed in mice fed either of the singly deficient diets or the adequate diet. Infected mice fed the doubly deficient diet had increased colon crypt hyperplasia and an influx of infiltrating cells along with gross changes to crypt architecture, including ulceration and denuding of the epithelial layer. Cytokine and chemokine mRNA levels in the colon were measured by real-time PCR. Expression of proinflammatory cytokines and chemokines was upregulated on day 12 after infection with C. rodentium in mice fed the doubly deficient diet compared to mice fed the control diet. Heme oxygenase 1, an enzyme upregulated by oxidative stress, also was more highly induced in infected mice fed the doubly deficient diet. Production of C. rodentium antigen-specific IgM and IgG antibodies was not affected by feeding the doubly deficient diet. The results indicated that selenium and vitamin E play an important role in host resistance and in the pathology induced by C. rodentium, an infection that mimics disease caused by common food-borne bacterial pathogens in humans.
    Infection and immunity 01/2011; 79(4):1471-8. · 4.21 Impact Factor
  • Gastroenterology 01/2011; 140(5). · 12.82 Impact Factor

Publication Stats

10k Citations
1,421.95 Total Impact Points

Institutions

  • 2013
    • Sun Yat-Sen University
      Shengcheng, Guangdong, China
  • 2005–2013
    • University of Maryland, Baltimore
      • Department of Medicine
      Baltimore, Maryland, United States
  • 2012
    • University of California, San Diego
      • Center for Research in Biological Systems (CRBS)
      San Diego, CA, United States
  • 2006–2012
    • Rutgers New Jersey Medical School
      • • Department of Medicine (RWJ Medical School)
      • • New Jersey Medical School
      • • Department of Medicine
      Newark, NJ, United States
  • 2002–2012
    • Agricultural Research Service
      Kerrville, Texas, United States
  • 1996–2011
    • United States Department of Agriculture
      • Agricultural Research Service (ARS)
      Washington, D. C., DC, United States
  • 1988–2010
    • Maryland Department Of Agriculture
      Annapolis, Maryland, United States
  • 2008–2009
    • Le Centre de Recherche en Nutrition Humaine Rhône-Alpes
      Rhône-Alpes, France
    • The Rockefeller University
      New York City, New York, United States
    • Southern University Agricultural Research and Extension Center
      Baton Rouge, Louisiana, United States
    • George Washington University
      • Department of Microbiology, Immunology, and Tropical Medicine
      Washington, D. C., DC, United States
  • 2003–2009
    • University of Iowa
      • Department of Internal Medicine
      Iowa City, IA, United States
    • Cincinnati Children's Hospital Medical Center
      • Division of Emergency Medicine
      Cincinnati, OH, United States
  • 1991–2009
    • National Institute of Allergy and Infectious Diseases
      • Laboratory of Parasitic Diseases (LPD)
      Maryland, United States
  • 2005–2008
    • Walter Reed National Military Medical Center
      Washington, Washington, D.C., United States
  • 1984–2006
    • Uniformed Services University of the Health Sciences
      • • Department of Microbiology & Immunology
      • • Department of Pediatrics
      • • Department of Medicine
      • • Department of Pathology
      Bethesda, MD, United States
  • 2000–2004
    • University of Cincinnati
      Cincinnati, Ohio, United States
  • 1996–2003
    • Michigan State University
      • • Department of Microbiology and Molecular Genetics
      • • College of Veterinary Medicine
      East Lansing, MI, United States