Microbiologist — Division of Microbiology
Robert Wagner, Ph.D.
Dr. Robert Wagner worked in a clinical laboratory as a medical technologist while earning a Bachelor of Science from Eastern Illinois University. He then acquired a Master of Science in chemistry from Illinois State University. His education was supplemented by membership in The American Society of Clinical Pathologists and the American Chemical Society. He was awarded a Ph.D. in microbiology and immunology from the University of Missouri. He was a member of the American Society for Microbiology, with which he continues to be affiliated. He was awarded a U.S. Department of Agriculture National Needs Fellowship for that training and was honored at the American Academy of Science.
Dr. Wagner then worked on the molecular genetics of human hypobetalipoproteinemia at the Lipid Research Center at Washington University Medical School. He was associated with the American Heart Association during his two-year tenure at Washington University.
Dr. Wagner worked at the University of Wisconsin Veterinary Medical School Pathobiology Division on the pathogenesis and host response to Listeria monocytogenes infections, where he was active in the American Society for Microbiology, the Society for Leukocyte Biology, and the American Association of Immunologists. He then moved to the University of Washington’s School of Medicine and studied host-parasite relationships with a eukaryotic pathogen, Candida albicans, and worked in collaboration with the Ross Products Division of Abbott Laboratories on probiotics in infant formulas.
Dr. Wagner began his tenure at FDA’s National Center for Toxicological Research (NCTR) in 1997. By request of FDA’s Center for Veterinary Medicine (CVM), he characterized probiotic competitive-exclusion products and developed an in vitro assay of antimicrobial drug-residue effects on intestinal-microbiota colonization resistance. He presented at FDA’s Center for Food Safety and Applied Nutrition (CFSAN) Food Advisory Committee on Probiotics in September of 2000, which aimed to define the role of FDA in regulating probiotic products. Research discussions with CFSAN and CVM led to a study in gnotobiotic mice of interactions between the human-intestinal microbiota and the pathogen Salmonella enterica, yielding an important discovery that the infection leads to immunosuppression of the mice. Dr. Wagner initiated a gnotobiotic research program at NCTR, which was essential to accomplish the Salmonella immunosuppression project. He was a co-principal investigator on a Cooperative Research and Development Agreements with the Pfizer Animal Health Company to study the effects of Ceftiofur and Ceftriaxone on the bovine intestinal microbiome.
Dr. Wagner’s laboratory collaborated with FDA’s Office of Women’s Health to study effects of probiotic bacteria, phytoestrogens, and nanotechnology products on vaginal epithelial responses to Candida albicans. Dr. Wagner also participated in FDA’s Live Microbial Ingredients Working Group.
Dr. Wagner’s research focuses on host defense against infections at mucosal interfaces. Recently, his research has expanded to study the effects of FDA-regulated products on mucosal infections. His laboratory studied the mechanism of microbiota suppression of Salmonella enterica immunosuppression. In this study, changes in lymphocyte activation and traffic in mucosa-associated lymphoid tissues of mice orally infected with S. enterica with and without treatment with enteric bacteria were evaluated by qRT-Polymerase chain reaction (PCR) and immunohistochemistry. Enteric bacteria increased T- and B-lymphocyte activation and reduced apoptosis and inflammatory responses to S. enterica. The results of this study are consistent with prevention of S. enterica-induced clonal deletion of T-cells by the influence of probiotic bacteria in mucosal lymphoid tissues of mice.
His laboratory investigated intestinal microbiome influences on epithelial cell responses to Clostridioides difficile infection, providing insight into the mechanisms of fecal microbiota transplantation. His research group developed a novel apparatus that provides oxygen to human cells and an anaerobic environment to the bacteria. The roles of representative strains of commensal bacteria in suppressing or enhancing C. difficile disease were explored using quantitative real-time PCR measurements of messenger ribonucleic acid concentrations and flow cytometric measurements of cell stress. The results of the study suggest that live microbial therapeutic products containing organisms such as Clostridium scindens and Blautia hansenii may be useful alternatives to fecal transplantation as therapies for C. difficile disease.
Dr. Wagner’s laboratory studied human vaginal-epithelial cell interactions with nanoparticles for intravaginal drug delivery. Nanoparticles consisting of polylactic acid-co-glycolic acid (PLGA)-polyethylene glycol (PEG) that could improve targeting of microbicidal drugs for sexually transmitted diseases by intravaginal inoculation in this study aggravate vaginal-epithelial cell proinflammatory responses to Candida albicans. The results showed that mucous-penetrating nanoparticle drug-delivery vehicles cause intracellular damage to vaginal-epithelial cells by several mechanisms and that their use for intravaginal drug delivery may exacerbate inflammation in active yeast infections by increased inflammatory recruitment.
Dr. Wagner and his research team also evaluated intravaginal drug-delivery nanoparticles effects on murine inflammation during vaginal candidiasis. Fluorescently labelled PLGA-PEG nanoparticles induced cytotoxicity and inflammation in mice infected with C. albicans. The nanoparticles induced oxidative effects, disruption of intracellular metabolic responses, and DNA damage in vaginal epithelial tissues of the mice. The nanoparticles also transited vaginal mucosal tissues and were found in other organs of the mice, including, livers, kidneys, and lungs. This study will enhance their understanding of nanoparticle effects on candidiasis.
His laboratory also investigated vaginal-microbiota disruption by silver nanoparticles in feminine hygiene products. A healthy, diverse vaginal microbiota — which may be adversely affected by contact with nanosilver — is essential for prevention of bacterial and fungal vaginoses and sexually transmitted diseases. A model vaginal microbiota in a vaginal-epithelial cell-culture model showed that silver nanomaterials found in some feminine hygiene products disrupt the composition of the vaginal microbiota as shown using conventional microbiological techniques and next-generation 16S ribosomal DNA sequencing. This work will provide an estimation of the impact of silver nanoparticles on the survival of microbiota relative to their capacity to maintain a protective level of colonization resistance in the vaginal environment.
Dr. Wagner and his laboratory staff are currently investigating the mechanisms involved in the microvascular coagulation-induced pathology in lungs that occur during human coronavirus infections. Using human lung epithelial and endothelial cell lines and human ACE2 transgenic mice, his laboratory is measuring the effects of infection with Human Coronavirus NL-63 on regulation of complement and coagulation cascades and inflammation. These studies have potential to reveal biomarkers for additional treatment options for COVID-19 and help to better understand immunization and establishment of long-lasting immunity to coronavirus infections.
Professional Societies/National and International Groups
American Society for Microbiology
2012 – 2022
Intravaginal Poly-(D, L-lactic-co-Glycolic Acid)-(Polyethylene Glycol) Drug-Delivery Nanoparticles Induce Pro-Inflammatory Responses with Candida albicans Infection in a Mouse Model.
Lina T.T., Johnson S.J., and Wagner R.D.
PLoS One. 2020, 15(10): e0240789. https://doi.org/10.1371/journal.pone.0240789.
Polyethylene Glycol-Functionalized Poly (Lactic Acid-co-Glycolic Acid) and Graphene Oxide Nanoparticles Induce Pro-Inflammatory and Apoptotic Responses in Candida albicans-Infected Vaginal Epithelial Cells.
Wagner R.D., Johnson S.J., Danielsen Z.Y., Lim J.H., Mudalige T., and Linder S.
PLoS One. 2017, 12 (4): e0175250. https://doi.org/10.1371/journal.pone.0175250.
A Metallo-β-Lactamase is Responsible for the Degradation of Ceftiofur by the Bovine Intestinal Bacterium Bacillus cereus P41.
Erickson B., Elkins C., Mullis L., Heinze T., Wagner R., and Cerniglia C.
Veterinary Microbiology. 2014, 172 (3-4):499-504.
Probiotic Lactobacillus and Estrogen Effects on Vaginal Epithelial Gene Expression Responses to Candida albicans.
Wagner R. and Johnson S.
J Biomed Sci. 2012, 19:58-66.
Protection of Vaginal Epithelial Cells with Probiotic Lactobacilli and the Effect of Estrogen Against Infection by Candida albicans.
Wagner R., Johnson S., and Tucker D.
Open J Med Microbiol. 2012, 2:54-64.
Bovine Intestinal Bacteria Inactivate and Degrade Ceftiofur and Ceftriaxone with Multiple β-Lactamases.
Wagner R., Johnson S., Cerniglia C., and Erickson B.
Antimicrob Agents Chemother. 2011, 55(11):4990-4998.
Probiotic Bacteria are Antagonistic to Salmonella enterica and Campylobacter jejuni and Influence Host Lymphocyte Responses in Human Microbiota-Associated Immunodeficient and Immunocompetent Mice.
Wagner R., Johnson S., and Kurniasih-Rubin D.
Mol Nutr Food Res. 2009, 53(3):377-388.
Vancomycin-Resistant Lactococcus lactis Isolated from a Competitive Exclusion Product Can Transfer the vanA Gene to Staphylococus aureus.
Wagner R., Kurniasih-Rubin D., and Johnson S.
Open Food Sci J. 2008, 2:72-76.
An In Vitro Model of Colonization Resistance by the Enteric Microbiota: Effects of Antimicrobial Agents Used in Food-Producing Animals.
Wagner R., Johnson S., and Cerniglia C.
Antimicrob Agents Chemother. 2008, 52(4):1230-1237.
Enhanced Production of Phospholipase C and Perfringolysin O (Alpha and Theta Toxins) in a Gatifloxacin-Resistant Strain of Clostridium perfringens.
Rafii F., Park M., Bryant A., Johnson S., and Wagner R.
Antimicrob Agents Chemother. 2008, 52(3):895-900.
Effects of Microbiota on GI Health: Gnotobiotic Research.
Adv Exper Med Biol. 2008, 635:41-56.
Efficacy and Food Safety Considerations of Poultry: Competitive Exclusion Products.
Mol Nutr Food Res. 2006, 50(11):1061-1071.
Phenotypic and Genotypic Characterization of Competitive Exclusion Products for Use in Poultry.
Wagner R., Paine D., and Cerniglia C.
J Appl Microbiol. 2003, 94(6):1098-107.
Biotherapeutic Effects of Probiotic Bacteria on Candidiasis in Immunodeficient Mice.
Wagner R., Warner T., Pierson C., Farmer J., Roberts L., Dohnalek M., Hilty M., and Balish E.
Infect Immun. 1997, 65:4165-4172.
J Food Protect. 2002, 65(5):746-51.
B Cell “Knockout” Mice are Resistant to Mucosal and Systemic Candidiasis of Endogenous Origin, but Susceptible to Experimental Systemic Candidiasis.
Wagner R., Vazquez-Torres A., Jones-Carson J., Warner T., and Balish E.
J Infect Dis. 1996, 174(3):589-97.
Recombinant Interleukin-12 Enhances Resistance of Mice to Listeria monocytogenes Infection.
Wagner R., Steinberg H., Brown J., and Czuprynski C.
Microb Pathog. 1994, 17(3):175-86.
Contact information for all lab members:
Shemedia J. Johnson, M.S.
Marufa Rumman, Ph.D.
- Contact Information
- Robert Wagner
- (870) 543-7121
ExpertiseApproachDomainTechnology & DisciplineToxicology