Retroviruses of Fish, Reptiles, and Molluscs

Poulet, Frederique M.; Bowser, Paul R.; Casey, James W.

doi:10.1007/978-1-4899-1730-0_1

Cited by 25 publications

(34 citation statements)

References 72 publications

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“…The molecular events leading to the seasonal induction and regression of WDS are not known but likely include complex interactions of host factors, e.g., hormonally regulated changes in viral gene expression and variations in the immune response of fish at different water temperatures (5). This tenet is supported by (i) the presence of retroviral type C particles in regressing tumors but not in developing tumors; (ii) observations that the gene expression pattern of WDSV changes both quantitatively and qualitatively during the course of the disease, with low levels of multiply spliced RNA transcripts produced in developing tumors and high levels of spliced and unspliced viral transcripts produced in regressing tumors (6)(7)(8); and (iii) the experimental transmission of lesions to walleye and sauger (Stizostedion canadense) fingerlings using cell-free extracts from regressing tumors but not developing tumors (9)(10)(11)(12)(13)(14). Experimental transmission studies typically have produced the benign skin tumors observed on feral walleye, but importantly, they have also resulted in the generation of invasive tumors (13,15).…”

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confidence: 98%

Squamous epithelial proliferation induced by walleye dermal sarcoma retrovirus cyclin in transgenic mice

Lairmore

Stanley

Weber

et al. 2000

Proc. Natl. Acad. Sci. U.S.A.

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Walleye dermal sarcoma (WDS) is a common disease of walleye fish in the United States and Canada. These proliferative lesions are present autumn through winter and regress in the spring. Walleye dermal sarcoma virus (WDSV), a retrovirus distantly related to other members of the family Retroviridae, has been etiologically linked to the development of WDS. We have reported that the D-cyclin homologue [retroviral (rv) cyclin] encoded by WDSV rescues yeast conditionally deficient for cyclin synthesis from growth arrest and that WDSV-cyclin mRNA is present in developing tumors. These data strongly suggest that the rv-cyclin plays a central role in the development of WDS. To test the ability of the WDSV rv-cyclin to induce cell proliferation, we have generated transgenic mice expressing the rv-cyclin in squamous epithelia from the bovine keratin-5 promoter. The transgenic animals were smaller than littermates, had reduced numbers of hair follicles, and transgenic females did not lactate properly. Following injury the transgenic animals developed severe squamous epithelial hyperplasia and dysplasia with ultrastructural characteristics of neoplastic squamous epithelium. Immunocytochemistry studies demonstrated that the hyperplastic epithelium stained positive for cytokeratin and were abnormally differentiated. Furthermore, the rv-cyclin protein was detected in the thickened basal cell layers of the proliferating lesions. These data are the first to indicate that the highly divergent WDSV rv-cyclin is a very potent stimulator of eukaryotic cell proliferation and to demonstrate the potential of a cyclin homologue encoded by a retrovirus to induce hyperplastic skin lesions. Knowledge concerning mechanisms of cell cycle control and cancer has been greatly enhanced through the study of oncogenic animal viruses. Walleye dermal sarcoma (WDS) is a cutaneous tumor that was first reported on feral walleye fish (Stizostedion vitreum) from Oneida Lake in New York by Walker (1) who later reported the presence of type C retroviral particles, walleye dermal sarcoma virus (WDSV) in lesions (2). The sarcoma is neither a rare nor a geographically limited disease, as up to 27% of the walleye population of Oneida Lake have tumors in some years and the disease has been reported on walleyes throughout the higher latitudes of North America (3, 4). One of the remarkable characteristics of WDS is its seasonal induction and regression. Tumors are observed from late fall through early spring when they regress; lesions are absent in the summer months. The molecular events leading to the seasonal induction and regression of WDS are not known but likely include complex interactions of host factors, e.g., hormonally regulated changes in viral gene expression and variations in the immune response of fish at different water temperatures (5). This tenet is supported by (i) the presence of retroviral type C particles in regressing tumors but not in developing tumors; (ii) observations that the gene expression pattern of WDSV changes both quantitatively a...

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mentioning

confidence: 98%

Squamous epithelial proliferation induced by walleye dermal sarcoma retrovirus cyclin in transgenic mice

Lairmore

Stanley

Weber

et al. 2000

Proc. Natl. Acad. Sci. U.S.A.

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“…There is goblet cell hyperplasia at the interface with the normal dermis. 45,69 Two retroviruses, walleye epidermal hyperplasia retrovirus 1 and 2, have been characterized from spontaneous lesions and fully sequenced. 37,52 Transmission trials using cell-free filtrates derived from spontaneous lesions known to harbor both viruses were successful.…”

Section: Walleye Dermal Sarcomamentioning

confidence: 99%

Pathology of Tumors in Fish Associated With Retroviruses

2013

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Thirteen proliferative diseases in fish have been associated in the literature with 1 or more retroviruses. Typically, these occur as seasonal epizootics affecting farmed and wild fish, and most lesions resolve spontaneously. Spontaneous resolution and lifelong resistance to reinfection are 2 features of some piscine retrovirus-induced tumors that have stimulated research interest in this field. The purpose of this review is to present the reader with the epidemiological and morphological features of proliferative diseases in fish that have been associated with retroviruses by 1 or more of the following methods: detection of C-type retroviruslike particles or reverse transcriptase activity in tumor tissues; successful tumor transmission trials using well-characterized, tumor-derived, cell-free inocula; or molecular characterization of the virus from spontaneous and experimentally induced tumors. Two of the diseases included in this review, European smelt spawning papillomatosis and bicolor damselfish neurofibromatosis, at one time were attributed to a retroviral etiology, but both are now believed to involve additional viral agents based on more recent investigations. We include the latter 2 entities to update the reader about these developments. Keywords fishes, piscine, neoplasms, Retroviridae, tumor virus infections, oncogenic virusesMembers of several virus families have been implicated in the etiology of tumors in fish. The literature contains numerous publications in which members of virus families Herpesviridae, Papillomaviridae, and Retroviridae are associated with the development of tumors in fish. In this report, we review the epidemiological, gross, microscopic, and ultrastructural features of 13 piscine tumors reported in the literature for which there is evidence of a retroviral involvement. In some instances, the evidence supporting a retroviral association is compelling and includes viral sequencing and successful transmission trials using a well-characterized inoculum. In other instances, a retroviral association is based on detection of retrovirus-like particles or reverse transcriptase activity in tissues from proliferative lesions. These viruses have been the subject of several reviews. 4,48,49 For this review, we have accessed archival materials primarily from the archived Registry of Tumors in Lower Animals as well as cases from the Aquatic Animal Health Program at the College of Veterinary Medicine, Cornell University.Before evaluating a lesion, any case of a fish tumor must be considered in light of the fish as an ectotherm. Much of the biology of fish is affected by water temperature and seasonality of various physiological processes. It is well known that the immune response in fish is modified by changes in water temperature and other physiological stressors, such as spawning activity. 39 A review of the case records of most fish disease diagnostic laboratories will show the largest number of neoplastic cases to occur in the spring, a time of changing water temperature and a tim...

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“…Lesions are present in late fall through early spring, when they regress ( Fig. 1) (2,11,25,60). WDS of feral walleyes is a multifocal, benign skin lesion that can first be seen in the fall as firm, vascularized tumors (Fig.…”

Section: Wds and Epidermal Hyperplasiamentioning

confidence: 99%

“…These experiments demonstrate that WDSV has the potential to induce lethal tumors and suggest that tumor regression arose from an adaptive process that benefits both the virus (regressing tumors release copious numbers of virions) and host. Tumors of other organs have not been observed in experimental fingerlings or feral adults (60). WEH has also been experimentally transmitted to walleye fingerlings by intramuscular injection of cell-free filtrates from hyperplastic lesions (7).…”

Section: Wds and Epidermal Hyperplasiamentioning

confidence: 99%

Comparative Pathogenesis of Epsilonretroviruses

Holzschu

LaPierre

Lairmore

2003

J Virol

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Experimental models using mammalian and avian oncogenic retroviruses have led to key advances in the understanding of cell proliferation and oncogenesis and basic principles in cell biology. Since the discovery in 1911 of Rous sarcoma virus (65,66), more than 30 oncogenes have been identified in acutely transforming simple retroviruses (reviewed in references 17 and 62). Retrovirally transduced oncogenes include transcription factors, growth-stimulating factors, receptor molecules, protein tyrosine kinases, protein serine/threonine kinases, and membrane-associated G proteins (62). Each of these retrovirus-encoded oncogenes has a highly conserved cellular counterpart, and many of their human homologs have been implicated in cancers. In contrast to the simple retroviruses, oncogenic complex retroviruses, e.g., human T-cell lymphotropic virus type 1, do not contain typical oncogenes but contain unique regulatory and accessory genes that are believed to promote cancer through their ability to alter cellular gene regulation (1). These studies have contributed greatly to our understanding of eucaryotic cell cycle regulation and cell proliferation, but these processes are still far from understood. Therefore, it is important to continue to develop new research venues for the study of cell proliferation, including new systems to study retrovirus-induced oncogenesis. Piscine and other retroviruses of lower vertebrates represent an untapped resource of model systems to investigate mechanisms of oncogenesis. At least 13 proliferative lesions of fish are tentatively attributed to retroviruses based on the observation of retrovirus-like particles and, in some cases, reverse transcriptase activity in lesions. Interestingly, seven of these lesions are seasonal; i.e., they develop and regress annually, thereby providing unique experimental models for tumor development and naturally occurring tumor death (Table 1) (25). This review focuses on the skin lesions of walleyes (Stizostedion vitreum), i.e., walleye dermal sarcoma (WDS) and walleye epidermal hyperplasia (WEH) and on their associated epsilonretroviruses, WDS virus (WDSV) and WEH viruses 1 and 2 (WEHV1 and WEHV2). WDS AND EPIDERMAL HYPERPLASIAWDS and WEH were first reported on fish from Oneida Lake in New York by Walker (76), who later observed type C retrovirus-like particles in lesions (75, 76). Subsequently, WDS and WEH have been reported on walleyes throughout North America (9, 79). Both WDS and WEH are common in areas of endemicity; nearly 30% of the adult walleyes collected during the spring spawning run from Oneida Lake present WDS in some years, while approximately 10% present WEH. Lesions are present in late fall through early spring, when they regress ( Fig. 1) (2,11,25,60). WDS of feral walleyes is a multifocal, benign skin lesion that can first be seen in the fall as firm, vascularized tumors (Fig. 1). In contrast, WEH is a multifocal hyperproliferative skin disease that can first be seen in the fall as sharply delimited plaques of thickened epidermis (Fig. 1)...

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Retroviruses of Fish, Reptiles, and Molluscs

Cited by 25 publications

References 72 publications

Squamous epithelial proliferation induced by walleye dermal sarcoma retrovirus cyclin in transgenic mice

Squamous epithelial proliferation induced by walleye dermal sarcoma retrovirus cyclin in transgenic mice

Pathology of Tumors in Fish Associated With Retroviruses

Comparative Pathogenesis of Epsilonretroviruses

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