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Animal Enteric Viruses: Gene Expression, Epidemiology and Their ANIMAL ENTERIC VIRUSES: GENE EXPRESSION, EPIDEMIOLOGY AND THEIR ROLE IN SHELLFISH AND ENVIRONMENTAL CONTAMINATION DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Verónica P. Costantini, BS ******* The Ohio State University 2007 Dissertation Committee: Distinguished University Professor Dr. Linda J Saif, Adviser Professor Dr. Daral J. Jackwood Associate Professor Dr John H Hughes Approved by Adviser Graduate Program in Veterinary Preventive Medicine Copyright by Verónica Costantini 2007 ABSTRACT Acute gastroenteritis (AGE) is one of the most common diseases worldwide. Seven to 41 percent of these are food-borne disease. Each year, foodborne diseases cause 76 million illnesses, more than 300,000 hospitalizations and 5,000 deaths in the U.S, indicating that 1 in 4 Americans develop disease and at least 1 in 1000 is hospitalized. Only 20-30% of these illnesses are attributed to known pathogens, and viral agents are estimated to account for more than 2/3 of these. Among viruses, noroviruses (NoVs) are estimated to cause 82% of the foodborne illnesses. HuNoVs have been detected in fruits, vegetables, ready-to-eat foods and seafood worldwide. Ten to 70% of outbreaks are associated with seafood and contamination occurs at pre- and post-harvest. However, no data has been collected to determine viral contamination in commercial shellfish harvesting areas throughout the U.S. coasts. In addition, although the identification of related animal enteric caliciviruses and recombinants have raised concerns for human infection or co-infection with different strains, the presence of animal strains in shellfish with potential risk for humans has not been studied. We determined the occurrence of human and animal enteric caliciviruses (HECV and AECV, respectively) in U.S. market oysters. Oysters were collected from 45 different bays along the U.S. coasts during summer and winter of 2002- 2003. Twenty-percent of the samples were positive for HuNoVs GII, phylogenetically ii similar to NoV GII US 95/96 subset (GII.4). Animal enteric caliciviruses were detected in 10 samples (22%). Seven of these were positive for porcine NoV (PoNoV) GII and one sample was positive for PoSaV GIII. Bovine NoVs (BoNoVs) were detected in two samples and confirmed by sequencing as NoV GIII. Different seasonal and state distributions were detected and HECV and AECV strains were simultaneously detected in oysters from the same bay during the same season. Our results confirm the presence of HuNoV GII.4 in oysters purchased from markets supplied by licensed shippers that harvest them from bays on the East, West and Gulf coasts approved for human consumption. The simultaneous detection of HECV and AECV raises concerns for possible human infection or co-infection with HECV and AECV strains, favoring the opportunity for recombination and emergence of new strains relevant for the control of the disease. The major source of contamination of water and food is the discharge of treated or partially treated waste into open waters. Similarly for agriculture, the causative agents of many infectious diseases are excreted by the fecal route from animals with acute and chronic infections, but also sometimes from clinically healthy animals. Several candidate environmentally superior technologies (cESTs) have been developed for the treatment of animal wastes to reduce their impact on the environment. We determined the presence of swine enteric viruses [PoNoV, PoSaV, rotaviruses (RV)-group A, B and C] in fresh feces or manure and evaluated the effects of different cESTs on their detection and viability. Porcine SaVs were detected in 97% of the samples by RTPCR, ELISA or both techniques, iii whereas for PoNoVs 20% of the samples were positive by RTPCR. The RV-A and RV-C were detected in 67% and 44% of the samples by seminested-RTPCR and/or ELISA. After treatment PoSaV RNA was only detected in the Conventional Waste Management (CWM), and not from the cESTs. Rotavirus-A and -C RNA was detected in 4/5 and 3/4 cESTs after treatment, but infectious particles were not detected by cell culture immunofluorescense, nor were clinical signs or seroconversion detected in Gn pigs inoculated with post treatment samples. Thus only RV-A/C RNA, but no viral infectivity was detected after treatment. This is the first study to evaluate the impact of different waste treatment technologies on virus detection and viability in swine manure. The fact that RNA virus (PoSaV and PoNoV) was not detected after treatment and/or Gn pigs were not infected by post-treatment samples suggests that infectious virus would not be present in the field after treatment. However their utility should be evaluated together with their ability to reduce the impact of other factors (organic and inorganic residues) on the environment. In general, efforts to prevent contamination and to develop effective treatments to inactivate HuNoV, as well as many molecular and immunological studies, have been hampered by the lack of a cell culture system to assay infectivity of enteric NoVs. Only PoSaV/Cowden strain and a murine NoV can be propagated in cell culture. The PoSaV/Cowden strain was adapted to serial propagation in an LLC-PK cell line by adding on intestinal content preparation (IC), derived from uninfected Gn pigs to cell culture. Bile acids were identified as active factors in IC essential for growth of PoSaV/Cowden in cell iv culture by activating the Protein Kinase A (PKA) signaling pathway and down-regulating Interferon (IFN) mediated STAT1 activation. However in this case, the fact that the IC showed higher levels of activity than individual BA suggests that other components of the IC might inhibit STAT1 activation by other mechanisms or other undefined mechanisms mediated by IC or BA contribute to PoSaV/Cowden replication that will be applicable to other SaVs and NoVs. We measured gene expression profiles of LLC-PK cells in response to PoSaV/Cowden infection in the presence of IC at early and late time points post- infection. Based on the criteria of a ≥ 1.5-fold change, at 4h PI, 29 genes were differentially up-regulated and, at 8h PI, 83 genes were up-regulated and 7 were down-regulated in virus- infected cells compared to mock-infected cells. Genes clustered mainly into classes involved in cell cycle, cell proliferation and apoptosis, protein metabolism, immune and stress response and signal transduction. The late up-regulation of immune response genes and the absence of other intermediates in IFN responses suggest a block or delay of the IFN response. The late up-regulation of genes involved in apoptosis suggests that PoSaV/Cowden strain may trigger apoptosis for cell release or spread. This represents the first global study of cellular gene expression altered by calicivirus infection in cell culture, and shows an overview of the general changes in gene expression. Our findings may serve as a foundation for further analysis at the functional level to understand the mechanism of SaV infection with potential extension to NoVs. v Dedicated to my Father who always encouraged me to follow ahead, to my Mother who always let me fly and to my Sister and Brother who always were there for me Dedicada a mi Padre, que siempre me animó a seguir, a mi Madre que siempre me dejó volar y a mis Hermanos quienes siempre estuvieron ahi por mi. vi AKNOWLEDGMENTS I thank my adviser, Dr. Linda J. Saif for her guidance and support through this process. I thank to my committee members Dr. Daral Jackwood and Dr. John H. Hughes for their helpful suggestions and contributions to this work I also would like to thank Dr. Viviana Parreño for opening the door to this opportunity, and Dr Armando Hoet and Dr. Paul Nielsen for encourage me to follow this journey. I am greatly thankful to Dr. Menira Dias e Souza, Dr. Marli Azevedo, Dr. Myung Guk Han and Dr. Fabienne Loisy for their friendship and for sharing their knowledge. Special thanks to the Calicivirus group: Dr. Sonia M. Cheetham, Dr. Qiuhong Wang and Dr Christopher Thomas for all their help. Thanks to all my former and present lab colleagues: Peggy Lewis, Dr. Ana Gonzales, Dr. Anastasia Vlasova, Dr. Kostanini Alekseev, Dr. Kwonil Jung, Dr. Jason Zhang, Dr. Li Guohua, Dr. Trang Van Nguyen, Mrs Wei Zhang, Mrs Ana Clara Azevedo, for understanding and companionship during this time. Thanks to Hannah Gehman, Robin Weimer and Mary Decker for their help, company and dedication to the Food Animal Health Research Program. vii VITA March 8th, 1973 Born-Buenos Aires, Argentina 1991 – 1997 Diploma in Biochemistry Universidad de Morón, Buenos Aires, Argentina April 1996 – Dec 1996 Technical assistant in clinical Hospital de Campo de Mayo Campo de Mayo, Buenos Aires, Argentina April 1997 – March 1999 Technical Assistant National Institute of Agro Technology Institute for Virology Castelar, Buenos Aires, Argentina March 1999– Aug 2000 Research Fellowship National Institute of Agro Technology Institute for Virology Castelar, Buenos Aires, Argentina Sept 2000 – Dec 2001 Visiting Scholar Food Animal Health Research program Ohio Agricultural Research and Development Center Department of Veterinary Preventive Medicine The Ohio State University, Wooster, OH. Jan 2002 – Jun 2002 Junior Research National Institute of Agro Technology Institute for Virology Castelar, Buenos Aires, Argentina July 2002 – present Graduate Research Associate Food Animal Health Research Program Department of Veterinary Preventive Medicine Ohio Agricultural Research and Development Center The Ohio State University, Wooster, Ohio viii PUBLICATIONS 1. Costantini V., Azevedo A.C, Li X., Williams M.C., Michel F.C. and Saif L.J. Effect of different swine waste treatment technologies on detection and viability of swine enteric viruses. Appl and Environm Microbiol 2007 Jun 29; [Epub ahead of print]. 2. Souza M., Cheetham S., Azevedo M.S.P., Costantini V.
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