Nomenclature and classification of herpesviruses: a proposal

Terminology Nomenclature and classification of herpesviruses: a proposal BERNARD ROIZMAN 1 & GUY DE-THE 2 The system for naming and classifying herpesviruses proposed in this memorandum is intended for consideration by other workers before a final proposal is made to the Inter- national Commission for Nomenclature of Viruses. The proposal is to classify the herpes- viruses in species and subspecies. The virus species should carry the name of the family, super-family, suborder, or order naturally infected by this virus. The second part of the name of the virus should be a numerical designation for each type of virus infecting that unit. The subspecies (representing closely related but clearly biologically different herpes- viruses isolated from a given unit of animal classification) should be designated with a consecutive letter in addition to the numerical species designation. The present nomenclature and classification of herpesviruses is bordering on disastrous as a conse- quence of the superimposition of numerous illogical schemes, and the nomenclature is under review by the International Commission for Nomenclature of Viruses. This memorandum proposes a system of nomenclature and classification for consideration by other workers before a final proposal is made to the International Commission. Herpesviruses were originally known by the disease they were associated with, some of them being known as the viruses of herpes zoster, herpes simplex, Aujeszky's disease, and, more recently, of Marek's disease. That this terminology is unsatisfactory is self- evident from the fact that herpesviruses are notori- ously variable in the diseases they induce; it is appa- rent that the virus of herpes zoster is also the virus of varicella and that the virus of bovine mammalitis also causes lumpy skin disease. Andrewes (1962) un- doubtedly recognized this problem and proposed that herpesviruses should be known by their hosts. Thus herpes simplex became herpesvirus hominis, and pseudorabies became herpesvirus suis and so on. This new nomenclature of herpesviruses gave rise to problems almost at once for three entirely different reasons. The first and least serious is that the no- menclature did not provide for a hierarchy. A less 1 Professor, Departments of Microbiology and Biophysics, The University of Chicago, Chicago, Ill., USA. ' Chief, Biological Carcinogenesis Unit, International Agency for Research on Cancer, Lyon, France. trivial reason stems from the fact that a virus may have more than one natural host with entirely diffe- rent binominal names. A good example is herpes T virus, a corruption of herpesvirus tamarinus, found in the New World monkey Tamarinus nigricollis, but also in Oediponidas oedipus, Saguinus oedipus, Saimiri sciureus, and Aotus tritigatus (Holmes et al., 1964; Melnick et al. 1964; Hunt & Melendez, 1966; Melen- dez et al., 1966; Daniel et al., 1967). Perhaps the most valid condemnation of this classification is that, while it allowed one herpesvirus per host, it did not take into account the fact that most of the species studied thoroughly up to now have yielded more than one herpesvirus. Man, a striking example, is afflicted by at least four herpesviruses. Of these, only one- the virus of herpes simplex-was given the name of herpesvirus hominis, leaving the others-the viruses of herpes zoster and cytomegalic inclusion-to be known by the diseases with which they are associated. However, even this nomenclature is not rigidly ad- hered to since the newest herpesvirus of man is named after its discoverers, Epstein and Barr. Clear- ly, we cannot have a nomenclature in which viruses are named after one of their native hosts, the diseases they produce, or their discoverers, arbi- trarily and at random. CRITERIA FOR THE NOMENCLATURE EMPLOYED IN THIS PROPOSAL The criteria are based on the following consider- ations: 2830 -547- TERMINOLOGY (1) Ideally the name assigned to a virus should be easy to remember and use. The latter requirement in particular suggests that current nomenclature should not be abandoned altogether but that rather it should be modified into a comprehensive scheme. (2) The identity of a virus within a group is fre- quently denoted by a serotype number. Herpes- viruses are at present denoted by the name of the disease, that of the discoverer, or that of one of the species in which they are found: objections have been raised against each of these systems. However, there is merit in identifying the virus not only by a number but also by the host in which it is found, but here again, problems arise because one virus can infect naturally more than one species or in fact more than one family. Thus, there is convincing evidence that the virus associated with Burkitt's lymphoma in man (or a very close relative) infects chimpanzees and possibly other Old World monkeys (Gerber & Birch, 1967; Gerber & Rosen- blum, 1968; Landon et al., 1968; Rauscher, 1968; Levy et al., 1971). Herpes T virus infects naturally two families of New World monkeys, whereas herpes B virus infects not only Old World monkeys but also man. (Is infection ofman by the bite of a pet monkey so different from transmission of tubercle bacilli from cow to man via milk?) Another objection to giving herpesvirus the name of the species in which the virus is found is that ultimately, if everyspecies yields only one herpesvirus, the herpesvirus nomen- clature will border on absurdity. We propose that herpesviruses should be designated by the name of the family, suborder, or order of the animals in which the virus is naturally endemic. (3) The most widely accepted criteria for a hier- archy in classifications of animal viruses are based on composition, symmetry, and structure of the virus (Lwoff & Tournier, 1966). In keeping with this precedent, we have considered a classification based on the base composition of the DNA-an indisputable structural characteristic of the virus. However, in order to operate such a classification the laboratories engaged in characterization of herpesvirus isolates would require much analytical equipment, and it is clear from an analysis of the available data that the biological properties of the virus cannot be predicted from the base composition of its DNA. We should also point out that the segregation of herpesviruses into groups based on DNA-DNA homology is also not very promising since with one exception (Kief et al., 1972) no herpes- viruses have been reported to share common nucleo- tide sequences (Zur Hausen & Schulte-Holthausen, 1970; Gravell, 1971; Bachenheimer et al., 1972). The present criterion for the classification of herpesviruses is based on the degree of cell asso- ciation of the virus as proposed by Melnick et al. (1964). The difficulty inherent in this classification is illustrated by Marek's disease herpesvirus, which, on the basis of its growth in chick embryo cells (Biggs, 1968; Churchill, 1968), would be classified in the group B, whereas based on its growth in feather follicle cells (Nazerian & Witter, 1970) the same virus could readily be classified into the A group. Sooner or later, the same case will be made for the viruses currently associated with varicella, cytomegalic inclusion disease, and Burkitt's lympho- ma. We propose that this classification should be phased out and that, except for the differentiation into species and subspecies, the more extensive classification of herpesviruses into genera be post- poned until more information for suitable criteria becomes available. It should be emphasized that the herpesvirus nomenclature we propose is inde- pendent of, and will not prejudice, a more compre- hensive classification of this group in the future. THE PROPOSAL We propose a nomenclature and partial classi- fication consisting of species and subspecies, as shown in Table 1. Species The name of the species shall be in two parts. The first part shall be after the family, superfamily, suborder, or order containing the smallest known unit which harbours all the species naturally infected by the virus with the widest host range; the second part shall be a consecutive numerical designation, one for each species of virus infecting that unit. Operational differentiation of species shall be on the basis of immunological properties. Both the name and numerical designation must be given even if a family, superfamily, suborder, or order have yielded only one herpesvirus. Subspecies Immunologically closely related but clearly bio- logically different herpesviruses isolated from a given unit of animal classification should be designated with a consecutive letter to indicate the subspecies in addition to the numerical species designation. The 548 NOMENCLATURE AND CLASSIFICATION OF HERPESVIRUSES Table 1. Proposed nomenclature and classification for herpesviruses Formal name Common name Species Subspecies Present names-synonyms herpesvirus primatis a herpesvirus primatis herpesvirus primatis herpesvirus primatis herpesvirus primatis b Herpesvirus primatis c herpesvirus primatis d herpesvirus primatis herpesvirus primatis herpesvirus salientis e herpesvirus salientis herpesvirus galli f herpesvirus galli herpesvirus galli herpesvirus canis ,herpesvirus felis h herpesvirus bovis i herpesvirus bovis herpesvirus bovis herpesvirus muris herpesvirus equi k herpesvirus equi herpesvirus laporis m herpesvirus laporis herpesvirus caviidae" herpesvirus columbi 0 herpesvirus anseri P herpesvirus suis q primate herpesvirus primate herpesvirus primate herpesvirus primate herpesvirus primate herpesvirus primate herpesvirus primate herpesvirus primate herpesvirus primate herpesvirus frog herpesvirus frog herpesvirus poultry herpesvirus poultry herpesvirus poultry herpesvirus canine herpesvirus feline herpesvirus bovine herpesvirus bovine herpesvirus bovine herpesvirus murine herpesvirus equine herpesvirus equine herpesvirus lapine herpesvirus lapine herpesvirus guinea-pig herpesvirus pigeon herpesvirus duck herpesvirus porcine herpesvirus 2 3 4 5 6 7 8 1 2 1 1 2 1 1 1 1 2 2 1 2 1 1 1 1 A B unknown uncertain uncertain unknown unknown unknown unknown unknown unknown A B unknown unknown unknown A A unknown unknown unknown unknown unknown unknown unknown unknown herpes simplex virus type (subtype) 1 herpesvirus hominis type 1 herpes simplex type (subtype) 2 herpesvirus hominis type 2 herpes zoster (varicella) virus herpes cytomegalovirus human cytomegalovirus Epstein-Barr virus Burkitt's lymphoma herpesviruis B virus, herpesvirus simiae T virus herpes saimiri virus vervet monkey herpesvirus Lucke adenocarcinoma herpesvirus FV4 Marek's disease herpesvirus turkey herpesvirus infectious laryngotracheitis canine herpesvirus feline rhinotracheitis virus infectious bovine rhinotracheitis virus infectious postular vulvovaginitis bovine mammilitis (Allerton) virus lumpy skin disease virus murine cytomegalovirus equine abortion viruses equine coital exanthemia virus herpesvirus sylvilagus herpes Ill virus of Andrewes guinea-pig cytomegalovirus pigeon herpesvirus duck herpesvirus pseudorabies herpesvirus suis Auzetzky's disease virus a After order Primatis. b Has been isolated from chimpanzees in captivity. c Infects man. d Infects two families of New World monkeys. e After order Salientia. f After order Galliformes. g After superfamily Canoideae. h After superfamily Feloideae. After superfamily Bovideae. After superfamily Muroideae. k After family Equidae. I Exact number of subtypes uncertain. m After family Lepideae. n After family Caviideae. 0 After order Columbiformes. P After order Anseriformes. q After suborder Suideae but pseudorabies infects naturally not only pigs, but also sheep, cows, and goats. Should it be named after the order Artiodactyla ? 549 550 TERMINOLOGY absence ofa subspecies designation shall indicate that none is known. It would be expected that the extent ofDNA-DNA homology between subspecies would be greater than that between species. In keeping with this design, there is no apparent homo- logy between the DNAs of the herpesviruses of herpes simplex and of Burkitt's lymphoma (herpes- virus primatis 1 and 4) (Zur Hausen & Schulte- Holthausen, 1970). On the other hand, approxi- mately 47% of the nucleotide sequence of the subspecies of herpes simplex (herpesvirus primatis 1/A and 1/B) are homologous and show only a. minimal amount (15%) of unmatched base pairs (Bachenheimer et al., 1972; Kieff et al., 1972). RtSUMtI NOMENCLATURE ET CLASSIFICATION DES VIRUS HERPES: UNE PROPOSITION Le systeme de designation et de classification des virus herpes propose dans ce memorandum a e 6tabli a l'intention d'autres chercheurs, en attendant qu'une pro- position definitive soit faite a la Commission internatio- nale pour la nomenclature des virus. On se propose de classer les virus herpes en especes et sous-esp6ces. Les especes de virus devraient porter le nom de la famille, superfamille, sous-ordre ou ordre infect6 naturellement par ce virus. La seconde partie du nom du virus devrait etre un nombre different pour chaque type de virus infectant cette unite. Les sous- especes (representant des virus herpes tres proches mais diffdrents du point de vue biologique et isol6s d'une unite donnee de classification animale) devraient etre design6es par un nombre consecutif ajoute a la d6signation nume- rique des especes. REFERENCES Andrewes, C. H. (1962) Advanc. Virus Res., 9, 271-296 Bachenheimer, S. L. et al. (1972) Comparative studies of DNAs of Marek's disease and herpes simplex virus. In: Biggs, P. M. et al., ed., Oncogenesis andherpesviruses, Lyon, International Agency for Research on Cancer Biggs, P. M. (1968) Curr. Top. Microbiol. Immunol., 43, 93-125 Churchill, A. E. (1968) J. nat. Cancer Inst., 41, 939-950 Daniel, M. D. et al. (1967) Arch. ges. Virusforsch., 22, 324-331 Gerber, P. & Birch, S. M. (1967) Proc. nat. Acad. Sci. (Wash.), 58, 478-484 Gerber, P. & Rosenblunm, E. N. (1968) Proc. Soc. exp. Biol. (N.Y.), 128, 541 Gravell, M. (1971) Virology, 43, 730-733 Holmes, A. W. et al. (1964) J. ImmunoL., 92, 602-61R Hunt, R. 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