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View on Enteric Caliciviruses And IMMUNE RESPONSES TO HUMAN NOROVIRUS AND HUMAN NOROVIRUS VIRUS-LIKE PARTICLES IN GNOTOBIOTIC PIGS AND CALVES DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Menira B. L. Dias e Souza, M.S. ***** The Ohio State University 2007 Dissertation Committee: Distinguished University Professor Dr. Linda J. Saif, Adviser Associate Professor Dr. John H. Hughes Approved by Adjunct Assistant Professor Dr. Lijuan Yuan _______________________ Adviser Graduate Program in Veterinary Preventive Medicine ABSTRACT The Caliciviridae family is constituted of four distinct genera: Norovirus, Sapovirus, Lagovirus, and Vesivirus. The Noroviruses (NoVs) are classified within 5 genogroups (GI-V) and at least 27 genotypes, based on the partial capsid, and regions A-D of the RNA dependent RNA polymerase. Caliciviruses (CV) infect various hosts and cause a wide spectrum of diseases. The human noroviruses (HuNoV) are transmitted by the fecal-oral route and constitute the leading cause of epidemic food and water-borne non-bacterial gastroenteritis worldwide. They are generally highly stable in the environment, which contributes to their dissemination and consequently to disease impact. The HuNoV disease is characterized by nausea, vomiting and abdominal cramps. These symptoms are usually self-limiting and cease within 24-48 hrs. However, these agents are responsible for great disease burden in both developed and developing countries, affecting people of all ages. The determinants of susceptibility and/or resistance to HuNoV are not completely understood; however recently, the histo-blood group type and secretor status were identified as genetic factors associated with risk of Norwalk-virus infection and disease. Numerous HuNoV outbreaks have been detected in the past decade and the most ii common sources are contaminated food and water, with secondary person-to-person transmission also being a common cause. These outbreaks take place in various settings such as: day-care centers, hospitals, cruise ships and schools. Outbreaks are also common among certain populations that live in close contact and in isolation such as the military personnel and elderly persons in nursing homes, causing high morbidity and low mortality. Therefore, the use of an efficacious and safe vaccine against HuNoV, especially among these populations would be of great benefit. The SaV and NoV have great genetic diversity and are fastidious viruses that do not grow in routine cell culture, except for the murine norovirus (MNV), and the porcine enteric calicivirus (PECV). Their extensive genetic diversity and fastidious character contribute to the diagnose confusion and limited knowledge about these viruses replication strategies, pathogenesis and host immune responses. However; recently, important progresses has been made with the in vitro growth of GI and GII HuNoV strains, using a 3-dimensional organoid model of human intestinal epithelium, and the successful replication of the HuNoV GII.4-HS66 strain in the gnotobiotic (Gn) pig model. Therefore, the use of experimental animal models constitutes an alternative for the study of HuNoV and is an important tool for a better understanding of HuNoV replication, pathogenesis, virus-host interactions and host immune responses to these agents. Our first objective was to evaluate the antibody and cytokine immune responses, both locally (intestine) and systemically to the GII.4 HuNoV-HS66 strain using the gnotobiotic (Gn) pig model. Low antibody titers and antibody-secreting cell (ASC) numbers were elicited in the HuNoV-HS66-inculated pigs, but 65% of the pigs seroconverted. A higher Th1 (high IL-12 but low and transient IFN-γ), but also low Th2 iii (IL-4 and IL-10), low transient pro-inflammatory (IL-6) cytokine and delayed innate (IFN-α) responses were induced by the HuNoV-HS66 in the serum of the Gn pigs. Intestinal IFN-α and IL-12 (late) were also significantly elevated after infection. Higher numbers of Th1 (IL-12 and IFN-γ) cytokine-secreting cells (CSC) were elicited when compared to Th2 (IL-4) and pro-inflammatory (IL-6) cytokines. Our second objective was to evaluate the potential of the Gn calf as an alternative model to study the pathogenesis and host immune responses after oral inoculation with the HuNoV-HS66 strain. Isotype-specific (IgM, IgA and IgG) antibody levels and the concentrations of the pro-inflammatory (TNF-α), Th1 (IL-12 and IFN-γ) and Th2 (IL-4) and Th2/T-reg (IL-10) cytokines were determined, at selected post-inoculation days (PIDs) in the serum, fecal samples and IC of the Gn calves, together with the CSC numbers in the intestine, mesenteric lymph nodes, spleen and blood at PID 28. The HuNoV-HS66 caused diarrhea and intestinal lesions, mainly in the proximal part of the intestine of one of the calves euthanized at PID 3. Viral shedding was detected from post- inoculation day 1-6 and 67% of the animals seroconverted with HuNoV-HS66-specific IgA and IgG antibodies. Both Th1 (IL-12 and IFN-γ) and Th2/T-reg (IL-10) cytokines, but also pro-inflammatory (TNF-α) were induced in the serum and fecal samples of the HuNoV-HS66-inoculated calves. Our third objective was to evaluate the antibody and cytokine immune responses in Gn pigs, both locally and systemically, to a HuNoV GII.4 (HS66 strain) virus-like particle (VLP) vaccine using 1 oral and 2 IN doses (250 μg/dose), in conjunction with the mucosal adjuvants, ISCOM or mLT, compared to controls (each adjuvant alone). We also evaluated the protection induced by both vaccination regimens to homologous viral iv challenge in pigs of A+/H+ phenotype. A 100% seroconversion rate was observed in the vaccinated pigs, regardless of the vaccine regimen, and 100% of coproconversion was detected in the VLP+ISCOM pigs compared to 75% of the VLP+mLT group. However, only 57% of the control pigs shed virus post-challenge. Pre-challenge, the VLP+ISCOM vaccine induced higher IgA and IgG ASC both systemically and locally and IgA and IgG in IC, whereas the VLP+mLT induced higher systemic Th1 and Th2 CSC numbers and highest Th1 (IFN-γ) cytokine responses in IC. Thus, the VLP+mLT vaccine induced a balanced Th1/Th2 response, whereas the VLP+ISCOM induced a more Th2 biased response, but both vaccine regimens induced high levels of protection against virus shedding and diarrhea In summary, this was the first study to delineate in detail both local and systemic immune responses to a GII.4 HuNoV (HS66 strain) using the Gn pig and calf model and to describe the pathogenesis of this strain in Gn calves. This was also the first study to evaluate the immunogenicity and protective potential of GII HuNoV VLP vaccines and also the protection induced by these vaccines after viral homologous challenge of the Gn pigs. v Dedicated to my husband Murillo for making me a better person and for embracing my dreams as if they were his own To my family and friends for their unconditional love and support through this journey vi ACKNOWLEDGMENTS I thank my adviser, Dr. Linda J. Saif for her guidance; support and constructive criticism that helped me grow intellectually through this process Thanks to my committee members Dr. John H. Hughes and Dr. Lijuan Yuan for their helpful suggestions and contributions to this work I also would like to thank Dr. Divina Cardoso for introducing me to the scientific world I am greatly thankful to Dr. Marli Azevedo, Dr. Ana Gonzales and Veronica Costantini for their friendship and for sharing their knowledge Special thanks to Dr. Sonia M. Cheetham and Kwonil Jung for their contributions to this work I also thank Dr. Juliet Hanson, Peggy Lewis, Richard McCormick, Janet McCormick, Greg Meyers and Todd Root for technical support and for their dedication to the Food Animal Health Research Program Thanks to all my former and present lab colleagues Dr. Anastasia Vlasova, Dr. Kostanini Alekseev, Dr. Jason Zhang, Dr. Li Guohua, Wei Zhang, Dr. Myung Guk Han and Dr. Qiuhong Wang for all their help, understanding and companionship vii VITA October 29th, 1973 Born - Brasilia, DF, Brasil 1991-1996 B.S in Biological Sciences, Catholic University of Goias Goiania, Goias, Brasil 1996-1998 Lab. Technician at PADRAO Clinical Laboratory Goiania, Goias, Brasil 1999-2001 M.S Tropical Medicine, Federal University of Goias Goiania, Goias, Brasil 2002- present Graduate Research Associate Food Animal Health Research Program Ohio Agricultural Research and Development Center Department of Veterinary Preventive Medicine The Ohio State University Wooster, Ohio PUBLICATIONS 1. Cheetham, S., Souza, M., Meulia, T., Grimes, S., Han, M.G. and Saif L. J. (2007) Binding patterns of human norovirus-like particles to buccal and intestinal tissues of gnotobiotic pigs in relation to A/H histo-blood group antigen expression. J Virol 81, 3535-3544. 2. Cheetham, S., Souza, M., Meulia, T., Grimes, S., Han, M.G. and Saif L. J. (2006) Pathogenesis of a genogroup II human norovirus in gnotobiotic pigs. J Virol 80, 10372- 10381. 3. Wang, Q., M., Souza, J.A. Funk., W. Zhang, and L.J. Saif. (2006) Prevalence of noroviruses and sapoviruses in swine of various ages determined by reverse transcription- PCR and microwell hybridization assays. J Clin Microbiol 44, 2057-2062. 4. Wang, Q., M.G. Han, S. Cheetham, M. Souza, J.A. Funk, and L.J.Saif. (2005). Porcine noroviruses related to human noroviruses. Emerg Infect Dis 11, 1874-1881. viii 5. Costa, P.S.S., Cardoso, D.D.C., Grisi, S.F.F.E., Silva, P.A., Fiaccadori, F.S., Souza, M.,B.L.D., and Santos, R. A. T. (2004). Manifestacoes clinicas e epidemiologicas das infeccoes por Rotavirus A. Pediatria (USP), Brasil, 26, 151-158. 6. Costa, P.S.S., Cardoso, D.D.P., Grisi, S.J.F.E., Silva, P.A., Fiaccadori, F.S., Souza, M.B.
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