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Latent Virus Infections in Primate Tissues with Special Reference to Simian Viruses G

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Latent Virus Infections in Primate Tissues with Special Reference to Simian Viruses G BACTERIOLOGICAL REVIEWS, Sept., 1968, p. 185-205 Vol. 32, No. 3 Copyright"@ 1968 American Society for Microbiology Printed in U.S.A. Latent Virus Infections in Primate Tissues with Special Reference to Simian Viruses G. D. HSIUNG Yale University School of Medicine and Veterans Administration Hospital, West Haven, Connecticut 06516 INTRODUCTION................................................................ 185 CLASSIFICATION OF SIMIAN VIRUSES BASED ON PHYSICOCHEMICAL PROPERTES. 186 BRIEF DESCRIPTIONS OF THE MAJOR SIMIAN VIRUS GROUPS . .186 DNA Viruses ..186 Papovavirus group ..186 Adenovirus group ..187 Herpesvirus group ..187 Poxvirus group ..187 RNA Viruses ..187 Picornavirus group. 187 Reovirus group ..192 Myxovirus group ..192 Pseudomyxovirus group ..193 EPIDEMIOLOGICAL ASPECTs OF LATENT VIRUS INFECTIONS IN SIMIAN TISSUES. 193 Detection ofLatent Infection in Cell Cultures by Prolonged Cultivationv... 194 Incidence of Virus Infections in "Normal" Monkey Kidney Cell Cultures. 194 Comparison of Virus Types Recoveredfrom Tissues ofMonkeys With or Without Quar- antine. 195 Mixed Infections.196 Distribution of Virus Types According to Conditions ofMonkey Shipment.197 Acquisition of Parainfluenza Virus Antibody in Monkeys During Captivity.198 POSSIBLE ORIGIN OF VIRUS INFECTION IN KINEY TISuEs.199 Model Study in Viremia and Viruria in Monkeys.199 Experimentally Induced Latent Infection ofSV40.199 Persistent Infection ofSV5 Group of Viruses in Monkeys after Intranasal Inoculation.. 200 LATENT VIRUS INFECTIONS IN HUMAN KIDNEY TIssuEs.200 CONCLUDING REMARKS.201 LITERATURE CITED.201 INTRODUCTION scope of this review. Furthermore, certain viral In recent years, there have been increasing agents have even been recovered from germ-free numbers of reports concerning the recognition of animals (4, 79). Thus, one cannot be assured that latent virus infections in tissues of primates as the organs of any animal species are microbiolog- well as nonprimates. The original isolation of ically sterile. adenovirus from adenoid tissues (87) and the sub- While searching for the viral etiology of human sequent recovery of adenovirus in tonsils (26), Kuru disease, Gajdusek and associates (30, 83) cytomegalovirus in adenoids (86), and several isolated 47 strains of viruses from a total of nine other virus types in kidney tissues (8, 22, 63) chimpanzees which had been experimentally in- are well-documented instances of latent virus oculated with Kuru 1 to 3 years previously. Some infections in tissues of man. Various methods of these isolates were identified as adenovirus, have been used for the detection of hidden reovirus, and foamy virus. All virus isolates were viruses in human tissues and these methods have obtained from tissue explants from chimpanzee been reviewed by Melnick et al. (68, 70). organs, such as brain, spinal cord, spleen, and Latent virus infections have also been recog- kidney. It became evident that some of these ani- nized in cell cultures derived from tissues of non- mals had been latently infected by these viruses primates. These include the isolation of cyto- prior to the inoculations of Kuru. megalovirus from the salivary glands of guinea Simian tissues have been of special interest, pigs and mice (38, 94), of herpesvirus from dog since monkey kidney cell cultures are commonly (95) and horse (51) kidney cell cultures, of adeno- used in the studies of animal viruses and in the virus from avian (16) and swine (11) kidney tis- preparation of virus vaccines for human use. As a sues, and of many others which are beyond the result of the extensive use of primate cell cultures, 185 186 HSIUNG BACTERIOL. REV. a great number of simian viruses have been re- determination by membrane filtration was em- covered from a variety of monkeys, baboons, and phasized (6). It was shown that SV5, measles, and marmosets (9, 12, 14, 15, 24, 25, 29, 40, 41, 47, foamy virus did not pass through a membrane 52, 56-58, 60, 65, 66, 72, 88, 89, 98, 99, 100). filter having a 100 nm limiting pore diameter; These indigenous viruses have caused consider- thus, these were considered large viruses. SVl1 able frustration and economic loss to workers in and SV12, which passed through the 100-nm filter terms of contaminated virus stocks and rejected with some reduction in infectivity titer, were in cultures. In this paper, I have reviewed the avail- the medium range; SV16 and SV40 passed able data, although in many instances the infor- through both 100- and 50-nm filters and were con- mation is rather limited regarding latent virus in- sidered small viruses. Thus, the use of membrane fections in primate tissues with special reference filtration has facilitated the grouping of unknown to viruses isolated from the monkey kidney tissues viruses (44). of apparently healthy animals. A brief descrip- The use of electron microscopy has led to tionoftheclassification of simian viruses and some highly detailed studies of the morphological struc- of the physicochemical and biological properties ture and the size of some simian viruses, especially ofthe major virus groups is also included. In addi- SV40 (31, 34). The fine structure of other simian tion, attempts have been made to elucidate the viruses has been described. These include simian origin of virus infections in primates, the mech- adenoviruses (2, 28), enteroviruses (3, 39), myxo- anism of viral persistence in kidney tissues, and viruses (19), foamy virus (61), and Yaba poxvirus the problems in the control of virus infections in (21). Based upon physicochemical properties, primate cell cultures. such as nucleic acid type and ether sensitivity, and on the results obtained by ultrafiltration and CLASSIFICATION OF SIMIAN VIRUSES electron microscopy, the classification of simian Simian viruses are, by defintion, a group of viruses has been proposed (45) in a manner simi- viruses isolated from tissues or excreta of pri- lar to that described for other animal viruses (1, mates other than man. The isolation of virus-like 44). This classification includes the DNA and agents from monkey kidney tissue cultures was RNA viruses, as shown in Table 1. In the DNA first reported by Rustigian et al. in 1955 (89). virus group, there are four major subgroups: the S-ubsequently, as a result of the extensive use of simian papovavirus, adenovirus, herpesvirus, monkey kidney cell cultures, especially in the and poxvirus. Similarly, there are four major sub- preparation of virus vaccines, a great number of groups among the RNA viruses: the simian pi- simian viruses have been recovered as endogenous cornavirus, reovirus, myxovirus, and pseudo- tissue contaminants by Hull and associates (56- myxovirus (monkey measles and foamy agents). 58). Since such a large number of viral agents have been isolated from monkeys, Hull et al. have BRIEF DESCRIPTIONS OF THE MAJOR designated all viruses isolated from simian origin SIMIAN VIRus GROUPS as "SV" with serial numbers, irrespective of their Recognition and characterization of simian properties or taxonomic order (56). In the mean- viruses in cell cultures are ofpractical importance, time, Malherbe and Harwin of South Africa since monkey tissues often harbor a variety of isolated several viral agents from vervet monkeys viruses. Some of the physicochemical properties and designated them "SA" with serial numbers, of the major simian virus groups are summarized indicating simian viruses isolated from South in Table 1. Methods used for recognition of each African monkeys (65, 66). simian virus group have been reported by various On the basis of certain biological properties, investigators and are described briefly below. especially cytopathic effect (CPE), simian viruses Some of the simian viruses, for example, the pox- were originally divided into four groups by Hull virus, were not recognized as latent virus infections et al. (57). Other biological properties, including in primate tissues. But, for completeness in listing plaque morphology, host-cell susceptibility, and the simian virus groups, the poxvirus group is hemagglutinin production, have also been used included. For a detailed discussion on the classifi- for grouping these viruses (54, 81). cation of the major groups of animal viruses, the More recently, the physicochemical properties reader is referred to Andrewes (1) and to Melnick of certain simian viruses have been studied. Infec- and McCombs (71). tious deoxyribonucleic acid (DNA) was obtained from SV40-infected cultures soon after the virus DNA Viruses was discovered (32), and infectious ribonucleic acid (RNA) has been successfully extracted from Papovavirus groups. SV40 or the vacuolating several strains of simian enterovirus (39). During virus of monkeys was found to be a small DNA, our study characterizing the simian viruses, size ether-resistant virus (52). This virus was first VOL. 32, 1968 LATENT VIRUS INFECTIONS IN PRIMATE TISSUES 187 isolated from kidney cell cultures derived from bodies to the B virus, and the percentage rose to rhesus and cynomolgus monkeys by Sweet and 60 to 70% when the monkeys were confined in Hilleman (98) and was isolated from patas mon- "gang-cages." Other studies indicated that 100% keys in our laboratory (52). Subsequently, SV40 of the experimental monkeys showed B virus was also isolated from kidney tissues of African antibody rise when the monkeys were housed green monkeys (47). In rhesus monkey cells, together over a period of 6 weeks (67). SV40 produced intranuclear inclusions, although Herpes T or Herpesvirus tamarinus, a new mem- CPE generally was not apparent (52). In patas, ber of the herpesvirus group, was isolated from African green monkey, and baboon cell cultures, marmoset, a New World monkey obtained from SV40 induced extensive vacuolations in the cyto- South America (41, 72). Although herpes T was plasm of infected cells (Fig. 1, Bi). Intranuclear highly pathogenic to marmosets, it did not pro- inclusions of a basophilic Feulgen-positive nature duce disease when inoculated into rhesus or green were observed in infected monkey cells regardless monkeys or baboons (72). of monkey species (Fig. 1, B2). Nonsimian cells Both herpes B and T grew readily in cultures of were generally resistant to SV40 infection (52).
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