B

Commissioned Paper: Comparison of
Immunity to Pathogens in Humans,
Chimpanzees, and Macaques

The following paper was commissioned by the Committee on the Use of Chimpanzees in Biomedical and Behavioral Research. The responsibility for the content of this paper rests with the authors and does not necessarily represent the views of the Institute of Medicine or its committees and convening bodies.

By: Nancy L. Haigwood, Ph.D.
Professor of Microbiology and Immunology Director
Oregon National Primate Research Center

Christopher M. Walker, Ph.D.
Professor of Pediatrics
Nationwide Children’s Hospital
The Ohio State University



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B Commissioned Paper: Comparison of Immunity to Pathogens in Humans, Chimpanzees, and Macaques The following paper was commissioned by the Committee on the Use of Chimpanzees in Biomedical and Behavioral Research. The responsibility for the content of this paper rests with the authors and does not neces- sarily represent the views of the Institute of Medicine or its committees and convening bodies. By: Nancy L. Haigwood, Ph.D. Professor of Microbiology and Immunology Director Oregon National Primate Research Center Christopher M. Walker, Ph.D. Professor of Pediatrics Nationwide Children’s Hospital The Ohio State University 91

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92 ASSESSING THE NECESSITY OF THE CHIMPANZEE INTRODUCTION The purpose of this white paper is to compare genetic and functional features of immunity and the response to infection in humans and major nonhuman primate species currently used in biomedical research. The search for appropriate disease models has been stimulated by the need to understand the most intractable of the persistent and lethal pathogens, as well as chronic diseases and conditions that are determined by the genet- ic makeup of the individual. Because the outcome of infection is gov- erned by carefully coordinated innate and adaptive immune responses, and pathogens have evolved strategies to evade these defenses, use of animal models that recapitulate key features of human infection is criti- cal. Successful nonhuman primate models closely emulate human im- munity, inflammation, and disease sequelae. They can also provide a critical pathway to clinical testing of risky prevention or treatment strate- gies for serious human diseases. Some past successes of infectious diseases research in nonhuman primates are described. However, the primary objective of the paper is to identify conditions that either support or limit use of these animals for the study of human viral, bacterial, or parasitic infections. A survey of the published literature reveals that the common chimpanzee (Pan trog- lodytes) is the only great ape used in infectious disease research. With few exceptions there is usually no alternative, because lower species are not permissive for infection or fail to replicate key features of disease. Most studies involve very small numbers of chimpanzees to ensure safe translation of vaccines or therapeutics to humans, or provide incontro- vertible evidence for basic mechanisms of immune control and evasion that cannot be obtained in human subjects. Various monkey species, pri- marily the Asian macaques (Macaca species), have served as models for infection with human viruses and microbes. Alternatively, monkey path- ogens like the simian immunodeficiency viruses (SIV) provide a reliable model of human infection with closely related viruses like human immu- nodeficiency virus (HIV). Infection studies with human and monkey vi- ruses have facilitated advances in vaccine development and studies of immunity and pathogenesis relevant to humans. Sequencing of the human, chimpanzee, and macaque genomes has provided unprecedented insight into the evolutionary relationship be- tween these species, especially for genes that regulate host defense and susceptibility to infection. Here we also provide examples of gene fami- lies involved in immunity that have been largely conserved since specia-

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93 APPENDIX B tion, and others that have undergone rapid evolution because of selective pressure by infectious diseases. How these adaptive changes might affect modeling of human infectious diseases in monkeys and great apes is dis- cussed. Contemporary examples of primate infectious disease models that replicate most if not all features of human infection and immunity are provided. Where infection models are not perfectly matched in hu- mans and nonhuman primates, differences have provided insight into key features of the relationship between the pathogen and its human host. Finally, several practical advantages of nonhuman primate models are also reviewed. The include the ability to (1) infect with clonal or ge- netically modified pathogens, (2) modify the immune response to identi- fy protective mechanisms, (3) sample at the earliest times after infection, often before symptoms are apparent in humans, and (4) access organs or tissues that are the primary site of infection. The latter is particularly im- portant because blood, which is often the only compartment available for human sampling, may not adequately reflect immunity at the site of in- fection. Advances in adapting the most sophisticated technologies to nonhuman primates, including methods to monitor immunity, and under- stand molecular aspects of infection using genomic and proteomic ap- proaches, has the potential to provide new insight into vaccination and infection with known and emerging pathogens. CHIMPANZEES Historical and Current Examples of Human Infectious Disease Research in Chimpanzees Chimpanzees have been used for over 100 years to model human vi- ral, bacterial, and parasitic infections. This long history has revealed that chimpanzees are often uniquely permissive for infection with some med- ically important human pathogens. These animals can also provide a more faithful model of human disease than lower nonhuman primates. Studies in chimpanzees, particularly with hepatotropic viruses, have pro- vided critical insight into host defense mechanisms and facilitated devel- opment of vaccines that have changed global public health. Yet for other pathogens key features of immunity and infection outcome differ be- tween humans and chimpanzees. In these instances, the host-pathogen interaction is influenced by adaptations that are species-specific despite a strikingly close genetic relationship.

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94 ASSESSING THE NECESSITY OF THE CHIMPANZEE The promise and limitations of chimpanzees as an infectious disease model were first recognized in a 1904 publication from Albert Grunbaum who transmitted the Eberth-Gaffky bacillus (Salmonella typhi) to two animals (Grunbaum, 1904). The bacillus, isolated 10 years earlier, was the suspected cause of enteric fever. Efforts to satisfy Koch’s third postu- late by transmission of disease to rats, rabbits, and monkeys had failed. Infection of chimpanzees was successful, but with much milder disease symptoms than expected. The author noted “the virulence of my cultures was not sufficient to produce a fatal result in the two instances in which they were given the opportunity to do so” (Grunbaum, 1904). That the chimpanzee might not be suitable for S. typhi vaccine development was highlighted in a 1914 publication (Nichols, 1914). The author, a propo- nent of a killed vaccine, critiqued an earlier study where such an ap- proach had failed. “The authors found that a whole killed vaccine did not protect chimpanzees. But they used tremendous infecting doses—the contents of a whole Kolle flask. The problems must be settled, as some of them already have been settled, by actual experience with large num- bers of men kept under close observation” (Nichols, 1914). Infectious disease research involving chimpanzees published in the last 30-40 years fits into three broad categories. They include (1) identi- fication and characterization of infectious agents that are serious public health threats; (2) characterization of protective immunity and how it is subverted; and (3) development of strategies to prevent or treat human infections. All published experimental infection studies used human pathogens and not closely related (and thus potentially different) chim- panzee pathogens as a model. Here, factors that determine the suitability of chimpanzees for research on infectious diseases are reviewed. Malar- ia, respiratory syncytial virus (RSV), HIV, and the hepatitis viruses are used as case studies. Malaria Malaria vaccine research is made difficult by complexities of the parasite life cycle and selection of antigens to either interrupt transmis- sion of infection or protect from disease after a mosquito bite (Good and Doolan, 2010). That irradiated P. falciparum sporozoites prevent disease was established several decades ago, but this approach is not easily scaled for human vaccination (Hoffman and Doolan, 2000). A small pilot study demonstrating protection of chimpanzees by a recombinant liver stage antigen derived from the sporozoites (Daubersies et al., 2000,

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95 APPENDIX B 2008) laid the foundation for a recent human clinical trial of this concept (ClinicalTrials.gov NCT00509158). Nevertheless, malaria is exceptional because human challenge studies are permissible and studies in lower- order species can provide guidance for vaccine development. Many ma- laria trials that are either underway or completed involved parasite chal- lenge of vaccinated human volunteers followed by co-artemether eradication therapy if necessary (as an example see Porter et al., 2011). Recent studies have also included sophisticated analyses of humoral and cellular immune responses with goal of identifying protective correlates in human volunteers (Good, 2011). While chimpanzees have been used sparingly to date, there is increasing concern that no successful vaccine has emerged from the concepts tested to date. If progress requires identi- fication of new antigens and a better understanding of immunity, espe- cially in the liver (Good, 2011), the place of the chimpanzee in malaria research may be reconsidered. Chimpanzees have also been critically important for the in vivo gen- eration of malaria parasites that are recombinants between drug-resistant and drug-sensitive strains in order to map drug resistance genes and thereby better understand the metabolism of these pathogens and to de- velop improved drugs. Several studies that used parasites generated by this approach have been published recently (Hayton et al., 2008; Nguitragool et al., 2011; Sa et al., 2009). Respiratory Syncytial Virus RSV was first isolated from captive chimpanzees with upper respira- tory tract disease (Blount et al., 1956) but was quickly identified as a human virus (Chanock and Finberg, 1957; Chanock et al., 1957). It is now recognized as the most important viral agent of severe respiratory tract disease in infants and children worldwide (Hall et al., 2009; Nair et al., 2010). RSV is also an important cause of morbidity and mortality in the elderly and in profoundly immunosuppressed individuals. Protection of vulnerable infants and young children from severe airway disease by a licensed monoclonal antibody against the RSV F protein, as well as the protection in the general population afforded by prior infection, suggests that active vaccination is also feasible (Graham, 2011). Progress over the past 4 decades was slowed by an unfortunate clinical trial of a formalin inactivated RSV vaccine that worsened disease and resulted in two deaths upon natural infection with the virus (Kapikian et al., 1969). There is a general consensus that the vaccine failed to induce potent neu-

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96 ASSESSING THE NECESSITY OF THE CHIMPANZEE tralizing antibody responses, provoked heightened lymphoproliferative responses, and was associated with eosinophilia and immune complex deposition in airways. Rodent and monkey models have demonstrated Th2 responses and eosinophilia using formalin-inactivated vaccines, but the precise mechanisms of immunopathogenesis remain undefined (re- viewed in Graham, 2011). With the failure of this killed vaccine, devel- opment of live-attenuated RSV vaccines was initiated. Chimpanzees are the only experimental animal in which RSV repli- cation and pathogenicity approach that of humans. Small numbers of chimpanzees were used to demonstrate the safety of live-attenuated vac- cines as well as identifying candidates that were sufficiently attenuated to move forward into clinical trials (e.g., Clinicaltrials.gov NCT00767416) (Crowe et al., 1993, 1994; Teng et al., 2000; Whitehead et al., 1999). Importantly, the body temperature of the chimpanzee is the same as that of humans. Other available nonhuman primates have higher body tem- peratures and so chimpanzees are uniquely suited for pre-clinical evalua- tion of temperature-sensitive vaccine candidates, which comprise all of the candidates evaluated in clinical trials to date. In addition, the chim- panzee experiments added to a body of evidence that both live attenuated vaccines and vectored vaccines are not associated with enhanced disease. A series of clinical trials have been initiated in infants and young chil- dren to evaluate safety, attenuation, and immunogenicity of several live RSV vaccines (for instance, see ClinicalTrials.gov NCT00767416). It is too soon to know if live RSV vaccines that are sufficiently attenuated to be well tolerated in young infants (Karron et al., 2005) will be sufficient- ly immunogenic to prevent severe RSV disease. Alternate approaches involving recombinant viral vectors (such as attenuated parainfluenza virus type 3; see ClinicalTrials.gov NCT00686075), virus-like particles (ClinicalTrials.gov NCT01290419), and subunit proteins are at various stages of development and evaluation. RSV subunit vaccines are consid- ered unsuitable for use in RSV-naïve individuals, based on studies in mice, cotton rats, and African green monkeys. However, the evolutionary distance relative to humans, reduced permissiveness to RSV replication, and lack of disease may limit the predictive value of these models (Graham, 2011). Until the significant medical need for an RSV vaccine is fully met, it is difficult to exclude the possibility that chimpanzees will be required to answer questions about mechanisms and duration of immune protection and disease potentiation.

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97 APPENDIX B The Human Immunodeficiency Virus Susceptibility of chimpanzees to persistent HIV infection was first reported in 1984, a little more than 1 year after discovery of the virus (Alter et al., 1984). Successful infection of two animals, and persistence of lymphadenopathy for several weeks in one of them, suggested that the chimpanzee would be valuable for further studies of acquired immune deficiency syndrome (AIDS) (Alter et al., 1985). This study, and all oth- er early studies of immunity and vaccine development, used viruses like HIVIIIb and HIVSF2 that adapted in culture to use CXCR4 as a co-receptor for cell entry. These viruses did initiate infection in chimpanzees, but viremia was usually low or short-lived and immunodeficiency was not observed (with one notable exception described below). Several studies of the early studies with CXCR4 adapted viruses nonetheless provided insight into the nature of antiviral immunity in infected chimpanzees (Nara et al., 1987), including the development of neutralizing antibodies (Prince et al., 1987), proliferative responses, and lack of CD4+ T cell im- pairment (Eichberg et al., 1987). Important advances were made in un- derstanding mucosal routes of HIV-1 transmission using chimpanzees (Fultz et al., 1986), as well as the now better-appreciated issue of superinfection (Fultz et al., 1987). Some success in protecting animals from infection with the CXCR4-dependent HIV strains was achieved by active and passive vaccination. Sterilizing immunity was induced by immunization with recombinant subunit envelope glycoproteins, but only with the CXCR4-utilizing virus HIVIIIB matched to the envelope immunogen (Berman et al., 1988). The vaccine was not fully protective when a different strain belonging to the same subtype, HIVSF2, was used (El-Amad et al., 1995). Passive transfer of HIVIG at a higher dose even- tually showed protection against HIVIIIB (Prince et al., 1991), as did one of the first neutralizing monoclonal antibodies directed against the HIV envelope (Emini et al., 1990). The interpretation of vaccine and anti- body-based protection work in chimpanzees was complicated by the ob- servation that chimpanzees were mostly resistant to infection with primary human HIV isolate that required the CCR5 chemokine receptor for cell entry. This discovery brought pause to the vaccine field, since none of the vaccines in testing could elicit neutralizing antibodies against the primary isolates that required CCR5 for infection. Later attempts to block infection using a human monoclonal against a primary HIV-1 chal- lenge were also less successful, though they showed some effect in re- ducing acute phase viremia (Conley et al., 1996).

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98 ASSESSING THE NECESSITY OF THE CHIMPANZEE Notably, one chimpanzee did develop immunodeficiency after more than a decade of subclinical infection with two prototype strains of CXCR4-adapted HIV (Novembre et al., 1997). Isolation of a pathogenic virus from this animal sparked a debate on the role of chimpanzees in HIV vaccine research. Specifically, it was proposed that a pathogenic virus could facilitate a direct test of vaccines designed to slow CD4+ T cell loss and immunodeficiency, if not infection (Cohen, 1999; Letvin, 1998). Vaccinated chimpanzees were never challenged with this virus in the face of persuasive ethical and scientific arguments (Cohen, 1999; Prince and Andrus, 1998). From the scientific perspective, there was considerable doubt about whether very rapid CD4+ T cell loss observed after transmission of the virus to new animals was representative of hu- man disease. Moreover, because immunodeficiency was not a consistent finding, there were also practical concerns with design of a study involv- ing two or three animals per group. These experimental infections with the pathogenic HIV strain were perhaps the last conducted at a primate research facility in the United States. No new HIV infection studies in chimpanzees have been published in the past decade. Studies on the origin of human HIV infection are beginning to yield insight into a host-virus relationship so finely tuned that it cannot be re- capitulated in an animal with 99 percent genetic identity. It is now appar- ent that HIV originated from a chimpanzee simian immunodeficiency virus (SIVcpz) introduced into human populations by zoonotic infection at least three times since the beginning of the 20th century (Keele et al., 2009a). Most simian retroviruses, including those from monkeys, are restricted from growth in human cells by species-specific factors (see section below on Monkey-human models of infection). SIVcpz is no ex- ception, as Vpu and Nef proteins had to adapt to neutralize human tetherin, a protein that is induced by interferon and restricts virus release from infected cells (Lim et al., 2010; Sauter et al., 2009). Adaptations like this one may explain attenuation of HIV infectivity for chimpanzees and perhaps limit its value as a model for vaccine development. The Hepatitis Viruses Chimpanzees are currently used to study the host response to four hepatitis viruses (HAV, HBV, HCV, and HEV) and to develop or refine approaches for prevention and treatment of the liver disease that they cause. Prevention and treatment of transmissible hepatitis in humans has been a public health priority for over 60 years. Progress toward isolation

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99 APPENDIX B of the agent(s) responsible for the disease burden was slow, in part be- cause hepatotropic viruses are fastidious and not easily propogated in cell culture. By the 1960s there was strong clinical, epidemiological, and immunological evidence for two distinct forms of transmissible hepatitis in humans (Krugman and Giles, 1972). Type A (or infectious) hepatitis had a short incubation period and was self-limited. Type B (or serum) hepatitis had a longer incubation period and was characterized by the prolonged presence of the Australia antigen (hepatitis B surface antigen; HBsAg) in serum. Use of chimpanzees in hepatitis research predated the discovery of the viruses that caused type A and B hepatitis. Sporadic outbreaks of liver disease in chimpanzee colonies with occasional zoono- tic transmission indicated that the animals might be susceptible to infec- tion with human viruses (Maynard et al., 1972a). Transmission of type A (Dienstag et al., 1975; Maynard et al., 1975) and B (Barker et al., 1973; Maynard et al., 1972b) hepatitis to chimpanzees facilitated characteriza- tion of both viruses and rapid development of diagnostics and highly ef- fective vaccines. Chimpanzee research provided critical proof that HBV infection was preventable by vaccination with HBsAg purified from the serum of human carriers (Buynak et al., 1976a, 1976b; Purcell and Gerin, 1975), and for the transition to a safer recombinant subunit vaccine (McAleer et al., 1984). Attenuated and inactivated vaccines were also shown to prevent HAV infection of chimpanzees (Feinstone et al., 1983; Provost et al., 1983; Purcell et al., 1992). The principle that a vaccine can prevent disease when administered as post-exposure prophylaxis was also established using HAV-infected chimpanzees (Purcell et al., 1992). Universal childhood vaccination against HAV and HBV is now recom- mended in the United States. Chimpanzees were also critically important to the discovery of the agent causing a third major form of human hepatitis. Studies published in 1975 concluded that unidentified type C hepatitis virus(es) were respon- sible for post-transfusion hepatitis in subjects not infected with HAV or HBV (Feinstone et al., 1975; Prince et al., 1974). The infectious nature of non-A, non-B hepatitis was not established by experimental transmis- sion of liver disease to uninfected humans, an approach used to define features of type A and B hepatitis in the highly controversial Willowbrook experiments (Krugman, 1986). Instead, evidence that the disease was caused by a small, enveloped RNA virus was obtained by physico-chemical analysis of patient serum that transmitted persistent hepatitis to chimpanzees (Alter et al., 1978; Bradley et al., 1983, 1985; Tabor et al., 1978). Serum that was titrated and serially passaged in

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100 ASSESSING THE NECESSITY OF THE CHIMPANZEE chimpanzees provided the pedigreed material from which the HCV ge- nome was eventually cloned as described in 1989 (Choo et al., 1989). All four hepatitis viruses remain significant public health problems today. A box summarizing research objectives of contemporary hepatitis virus research using chimpanzees is provided (Box 1). As described in detail below, HAV, HBV, HCV, and HEV all cause robust infection in chimpanzees. These viruses can cause the same spectrum of liver disease observed in humans, although in both species most infections tend to clinically mild and/or slowly progressive. BOX 1 Major Uses of Chimpanzees in Infectious Disease Research • Characterize and identify new infectious agents, especially those that cannot be propagated in lower species or cell culture. • Define mechanisms of protective innate and adaptive immunity and pathogen evasion strategies. This is particularly important in settings where early phases of acute infection are not easily identified in humans, or infected tissues are not accessibly for studies of immunity. • Establish that new concepts for vaccination or therapy of infection are safe and effective before translation to humans. • Determine if reagents critical to development of therapeutics like clonal viruses or parasites replicate in a host closely related to humans. Enteric Hepatitis Viruses HAV and HEV cause acute hepatitis and self-limited infection in humans and chimpanzees. Although liver disease may be somewhat milder in chimpanzees, the kinetics and magnitude of virus replication, onset of liver disease, and histopathological changes in the liver are simi- lar to those in HAV-infected humans (Dienstag et al., 1975, 1976). The course of HEV infection in chimpanzees is variable, ranging from low viremia with no obvious liver disease to high viremia with biochemical and histological evidence of hepatitis (Li et al., 2006; McCaustland et al., 2000). This may be similar to the spectrum of disease in HEV-infected humans (McCaustland et al., 2000). HAV and HEV infections are pre- ventable by vaccination. The efficacy of a subunit HEV vaccine was ap-

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101 APPENDIX B proximately 90 percent in two large human trials in Nepal and China, but there is uncertainty about the durability of protective immunity as cur- rently formulated and how (or if) it will be deployed where needed (Shrestha et al., 2007; Wedemeyer and Pischke, 2011; Zhu et al., 2010). Thus it is likely that endemic and epidemic HEV will remain a cause of serious liver disease in developing countries (Aggarwal, 2011). HEV immunity and pathogenesis are still very poorly understood (Aggarwal, 2011). For HAV, socioeconomic development accompanied by improved sanitation and opportunity for vaccination has changed epidemiology in regions where the virus is still endemic, as illustrated by a recent out- break in South Korea (Kim and Lee, 2010; Kwon, 2009). Under these circumstances, HAV infection shifts from the first to the second and third decades of life with an associated increase in the severity of disease. This situation has highlighted a gap in knowledge about mechanisms of im- munity and hepatocellular injury caused by HAV. Very recent studies in chimpanzees provided insight into patterns of innate immunity and host gene expression immediately after infection with HAV and HEV, with the goal of understanding the pathogenesis of these infections and how they compare to responses elicited by HCV that often establishes a per- sistent infection (Lanford et al., 2011; Yu et al., 2010a). Follow up stud- ies of adaptive immunity to these viruses in animals should be anticipated. Similar studies in humans will be difficult, if not impossible, because infections with these small RNA viruses are often not sympto- matic for several weeks and access to liver may be challenging as there is typically no medical need for liver biopsy. HBV Worldwide, approximately 500 million people are infected with HBV. Hepadnaviruses are widespread in nature and chimpanzees do har- bor indigenous strains of HBV that can be distinguished from human viruses based on genomic signatures despite overall identity of about 90 percent (Barker et al., 1975a, 1975b; Dienstag et al., 1976; Guidotti et al., 1999; Hu et al., 2000; Rizzetto et al., 1981). Chimpanzees are never- theless highly susceptible to challenge with human HBV. Chimpanzees develop persistent and resolved infections after challenge with the virus (Barker et al., 1975a, 1975b). The incubation period preceding symptoms is long and biochemical evidence of acute hepatitis is associated with parenchymal inflammation, as in man. The magnitude and general pat- tern of viremia and antigenemia during the acute and chronic phases of infection are also similar between the species (Barker et al., 1975a, 1975b; Kwon and Lok, 2011). Severe progressive hepatitis and cirrhosis

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156 ASSESSING THE NECESSITY OF THE CHIMPANZEE Parham, P., L. Abi-Rached, L. Matevosyan, A. K. Moesta, P. J. Norman, A. M. Older Aguilar, and L. A. Guethlein. 2010. Primate-specific regulation of natural killer cells. Journal Med Primatol 39:194-212. Patel, V., A. Valentin, V. Kulkarni, M. Rosati, C. Bergamaschi, R. Jalah, C. Alicea, J. T. Minang, M. T. Trivett, C. Ohlen, J. Zhao, M. Robert-Guroff, A. S. Khan, R. Draghia-Akli, B. K. Felber, and G. N. Pavlakis. 2010. Long- lasting humoral and cellular immune responses and mucosal dissemination after intramuscular DNA immunization. Vaccine 28:4827-4836. Patterson, L. J., N. Malkevitch, J. Pinczewski, D. Venzon, Y. Lou, B. Peng, C. Munch, M. Leonard, E. Richardson, K. Aldrich, V. S. Kalyanaraman, G. N. Pavlakis, and M. Robert-Guroff. 2003. Potent, persistent induction and modulation of cellular immune responses in rhesus macaques primed with Ad5hr-simian immunodeficiency virus (SIV) env/rev, gag, and/or nef vaccines and boosted with SIV gp120. J Virol 77:8607-8620. Penna, A., M. Pilli, A. Zerbini, A. Orlandini, S. Mezzadri, L. Sacchelli, G. Missale, and C. Ferrari. 2007. Dysfunction and functional restoration of HCV-specific CD8 responses in chronic hepatitis C virus infection. Hepatology 45:588-601. Permar, S. R., S. A. Klumpp, K. G. Mansfield, W. K. Kim, D. A. Gorgone, M. A. Lifton, K. C. Williams, J. E. Schmitz, K. A. Reimann, M. K. Axthelm, F. P. Polack, D. E. Griffin, and N. L. Letvin. 2003. Role of CD8(+) lymphocytes in control and clearance of measles virus infection of rhesus monkeys. J Virol 77:4396-4400. Permar, S. R., S. A. Klumpp, K. G. Mansfield, A. A. Carville, D. A. Gorgone, M. A. Lifton, J. E. Schmitz, K. A. Reimann, F. P. Polack, D. E. Griffin, and N. L. Letvin. 2004. Limited contribution of humoral immunity to the clearance of measles viremia in rhesus monkeys. J Infect Dis 190:998-1005. Permar, S. R., S. S. Rao, Y. Sun, S. Bao, A. P. Buzby, H. H. Kang, and N. L. Letvin. 2007. Clinical measles after measles virus challenge in simian immunodeficiency virus-infected measles virus-vaccinated rhesus monkeys. J Infect Dis 196:1784-1793. Pitcher, C. J., S. I. Hagen, J. M. Walker, R. Lum, B. L. Mitchell, V. C. Maino, M. K. Axthelm, and L. J. Picker. 2002. Development and homeostasis of T cell memory in rhesus macaque. J Immunol 168:29-43. Polacino, P., K. Larsen, L. Galmin, J. Suschak, Z. Kraft, L. Stamatatos, D. Anderson, S. W. Barnett, R. Pal, K. Bost, A. H. Bandivdekar, C. J. Miller, and S. L. Hu. 2008. Differential pathogenicity of SHIV infection in pig-tailed and rhesus macaques. J Med Primatol 37(Suppl 2):13-23. Poland, J. D., C. H. Calisher, T. P. Monath, W. G. Downs, and K. Murphy. 1981. Persistence of neutralizing antibody 30-35 years after immunization with 17D yellow fever vaccine. B World Health Org 59:895-900. Porter, D. W., F. M. Thompson, T. K. Berthoud, C. L. Hutchings, L. Andrews, S. Biswas, I. Poulton, E. Prieur, S. Correa, R. Rowland, T. Lang, J. Williams, S. C. Gilbert, R. E. Sinden, S. Todryk, and A. V. Hill. 2011. A

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