Isolation and tissue distribution of type-C virus and viral components from a gibbon ape (Hylobates lar) with lymphocytic leukemia

Gallo, Robert C.; Gallagher, Robert E.; Wong‐Staal, Flossie; Aoki, Tadao; Markham, Phillip D.; Schetters, H.; Ruscetti, Francis W.; Valerio, Marion G.; Walling, M. J.; O'Keeffe, Roderic; Saxinger, W. C.; Smith, R G; Gillespie, David; Reitz, M. S.

doi:10.1016/0042-6822(78)90255-6

Cited by 86 publications

(43 citation statements)

References 26 publications

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“…WMV isolated from the woolly monkey exists as a mixture of a replication-defective acute transforming virus and its associated replication-competent helper virus (10). Replication-competent WMV is related to GALV as supported by immunological (11) and serological tests (9), antigenic similarities in some gene products (7,12,13), and high RNA sequence homology (5,7). Since the woolly monkey from which WMV was isolated was reported to have been in contact with a gibbon for the 3 months before its death, WMV is likely the product of a single horizontal transmission of GALV from a gibbon to a woolly monkey.…”

Section: Importancementioning

confidence: 99%

“…The first was isolated from an animal with lymphocytic leukemia in a colony at the San Francisco Medical Center (strain SF) (1,2). GALV was later isolated from gibbons displaying malignant tumors, notably an individual gibbon with granulocytic leukemia, at the Southeast Asia Treaty Organization Medical Research Laboratory in Bangkok, Thailand (strain SEATO) (3,4), and another gibbon with lymphocytic leukemia from a colony on Hall's Island, near Bermuda (strain GALV-H) (5,6). The Brain strain was isolated from two healthy gibbons injected with brain extracts from human patients with kuru and from an uninoculated cage mate (7).…”

Section: Importancementioning

confidence: 99%

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Episodic Diversifying Selection Shaped the Genomes of Gibbon Ape Leukemia Virus and Related Gammaretroviruses

Alfano

Kolokotronis

Tsangaras

et al. 2016

J Virol

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Gibbon ape leukemia viruses (GALVs) are part of a larger group of pathogenic gammaretroviruses present across phylogenetically diverse host species of Australasian mammals. Despite the biomedical utility of GALVs as viral vectors and in cancer gene therapy, full genome sequences have not been determined for all of the five identified GALV strains, nor has a comprehensive evolutionary analysis been performed. We therefore generated complete genomic sequences for each GALV strain using hybridization capture and high-throughput sequencing. The four strains of GALV isolated from gibbons formed a monophyletic clade that was closely related to the woolly monkey virus (WMV), which is a GALV strain that likely originated in a gibbon host. The GALV-WMV clade in turn formed a sister group to the koala retroviruses (KoRVs). Genomic signatures of episodic diversifying selection were detected among the gammaretroviruses with concentration in the env gene across the GALV strains that were particularly oncogenic and KoRV strains that were potentially exogenous, likely reflecting their adaptation to the host immune system. In vitro studies involving vectors chimeric between GALV and KoRV-B established that variable regions A and B of the surface unit of the envelope determine which receptor is used by a viral strain to enter host cells. IMPORTANCEThe gibbon ape leukemia viruses (GALVs) are among the most medically relevant retroviruses due to their use as viral vectors for gene transfer and in cancer gene therapy. Despite their importance, full genome sequences have not been determined for the majority of primate isolates, nor has comprehensive evolutionary analysis been performed, despite evidence that the viruses are facing complex selective pressures associated with cross-species transmission. Using hybridization capture and high-throughput sequencing, we report here the full genome sequences of all the GALV strains and demonstrate that diversifying selection is acting on them, particularly in the envelope gene in functionally important domains, suggesting that host immune pressure is shaping GALV evolution. G ibbon ape leukemia virus (GALV) is an exogenous gammaretrovirus associated with hematopoietic neoplasms in captive colonies of white-handed gibbon (Hylobates lar). Five strains of GALV have been isolated from gibbons. The first was isolated from an animal with lymphocytic leukemia in a colony at the San Francisco Medical Center (strain SF) (1, 2). GALV was later isolated from gibbons displaying malignant tumors, notably an individual gibbon with granulocytic leukemia, at the Southeast Asia Treaty Organization Medical Research Laboratory in Bangkok, Thailand (strain SEATO) (3, 4), and another gibbon with lymphocytic leukemia from a colony on Hall's Island, near Bermuda (strain GALV-H) (5, 6). The Brain strain was isolated from two healthy gibbons injected with brain extracts from human patients with kuru and from an uninoculated cage mate (7). The SEATO strain has been shown to cause chronic myelogenous leukemia...

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Section: Importancementioning

confidence: 99%

Section: Importancementioning

confidence: 99%

Episodic Diversifying Selection Shaped the Genomes of Gibbon Ape Leukemia Virus and Related Gammaretroviruses

Alfano

Kolokotronis

Tsangaras

et al. 2016

J Virol

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“…In the early 1970s Kawakami et al (1972) had discovered gibbon ape leukemia virus (GALV), and linked it to chronic myeloid leukemia in that species. Later in the 1970s, we discovered a variant of that virus which caused T-cell leukemia (Gallo et al, 1978). Bovine leukemia virus (BLV) was discovered (Ferrer et al, 1975;Kettmann et al, 1975), and it was noted that BLV replicated at very low levels, thus putting to rest the notion of 'extensive viremia always precedes animal retrovirus-induced leukemia's'.…”

Section: Why the Consensus Against The Possible Existence Of Human Rementioning

confidence: 99%

“…First, most animal leukemias caused by retroviruses are lymphocytic leukemias and of these T-cell leukemias predominate. Second, the first and to this date only leukemia of nonhuman primates is caused by a retrovirus, namely the leukemia of gibbon apes caused by GALV (Kawakami et al, 1972;Gallo et al, 1978), and a particular strain of this virus which we isolated caused T-cell leukemia (Gallo et al, 1978). Third, fortune dictated that we would end up focusing on human T-cell malignancies because on our discovery of IL-2 which allowed us to grow significant numbers of such cells in liquid culture through many cell cycles.…”

Section: A Focus On T-cell Malignanciesmentioning

confidence: 99%

History of the discoveries of the first human retroviruses: HTLV-1 and HTLV-2

Gallo¹

2005

Oncogene

162

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“…The library was screened with homologous cDNA and cDNA synthesized on mRNA of another cutaneous T-cell lymphoma line that is negative for HTLV (14,15 (16), SEZ 2 (2), and MJ and MI (13) are five HTLV-producing human mature neoplastic T-cell lines. HUT 78 is a virus-negative mature human neoplastic T-cell line that is at a stage of differentiation similar to the virus-positive T-cell lines (14,15 (20); UCD 144, a gibbon T-lymphocyte line constitutively producing TCGF (21,22) and infected with the gibbon ape leukemia type C retrovirus (GaLV), and 6G-1, another GaLV-infected gibbon T-lymphocyte line (23) but not producing TCGF. AMML cells were fresh leukemic cells of a patient with acute myelogenous leukemia.…”

mentioning

confidence: 99%

Abundant transcription of a cellular gene in T cells infected with human T-cell leukemia-lymphoma virus.

Manzari¹,

Gallo²,

Franchini³

et al. 1983

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

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Human T-cell leukemialymphoma virus (HTLV) is a type C retrovirus associated with a subtype of mature T-cell malignancy in humans. HTLV also infects normal human cord blood mature T lymphocytes in vitro and induces a number of phenotypic changes in these cells, including their continuous growth and partial or complete independence of T-cell growth factor (TCGF). As part of our initial study designed to analyze gene(s) specifically activated by HTLV infection, we have isolated a recombinant DNA clone by differential screening of a cDNA library made from mRNA of a human T-cell lymphoma cell line producing HTLV. This cDNA identifies a single-copy gene in all human DNAs and a single mRNA species of 2.3 Idlobases expressed at several hundred copies per cell in five HTLV-positive neoplastic T-cell lines. In addition, cord blood T lymphocytes infected with HTLV, but not the uninfected counterparts, express high levels of mRNA from this gene. A survey of different human hematopoietic cell types showed that this gene is expressed at low or undetectable levels (<10 copies) in human T, B, myeloid, or erythroid cell lines; in moderate amounts in lymphoid precursor (immature) cell lines; and in high amounts in lectin-activated mature T-cells, comparable to those of HTLV-infected T-cell lines. The precise function of this gene has not yet been determined.Human T-cell leukemia-lymphoma virus (HTLV) is a unique exogenous retrovirus associated with a subtype ofmature T-cell malignancy in man (1-4). Extensive seroepidemiological studies (5-9) indicate that HTLV is present worldwide but is more prevalent in certain areas, including southwest Japan, the Caribbean, certain parts of South America, and the southeastern United States. There are now at least a dozen isolates of HTLV obtained from patients from different parts of the world (unpublished data). The isolates were obtained from neoplastic mature T-cell lines grown in suspension culture by addition of T-cell growth factor (TCGF) (10). Some ofthese lines eventually became autonomous producers of TCGF (11). Recent experiments indicate that some strains of HTLV can immortalize normal cord blood T lymphocytes in vitro (refs. 12 and 13; unpublished data), resulting in cell cultures that are completely or partially independent of TCGF. This result suggests a role of HTLV in modulation of specific steps in T-cell proliferation, possibly involving TCGF.To study the genes that are expressed at high levels in HTLVinfected cells, we constructed a cDNA library from mRNA of a cutaneous T-cell lymphoma line producing HTLV. The library was screened with homologous cDNA and cDNA synthesized on mRNA of another cutaneous T-cell lymphoma line that is negative for HTLV (14,15). From these experiments we identified a gene that is expressed at high levels in all HTLV-infected cells examined, including five neoplastic lines and two samples of normal cord blood T lymphocytes infected and transformed by HTLV in vitro. Studies on the expression of this gene in a variety of uninfected human...

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Isolation and tissue distribution of type-C virus and viral components from a gibbon ape (Hylobates lar) with lymphocytic leukemia

Cited by 86 publications

References 26 publications

Episodic Diversifying Selection Shaped the Genomes of Gibbon Ape Leukemia Virus and Related Gammaretroviruses

Episodic Diversifying Selection Shaped the Genomes of Gibbon Ape Leukemia Virus and Related Gammaretroviruses

History of the discoveries of the first human retroviruses: HTLV-1 and HTLV-2

Abundant transcription of a cellular gene in T cells infected with human T-cell leukemia-lymphoma virus.

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