The LTR enhancer of ERV-9 human endogenous retrovirus is active in oocytes and progenitor cells in transgenic zebrafish and humans

Wenhu Pi, Zhongan Yang, Jian Wang, Ling Ruan, Xiuping Yu, Jianhua Ling, Sanford Krantz, Carlos M Isales, Simon J. Conway, Shuo Lin, Dorothy Tuan Lo

Research output: Contribution to journalArticle

29 Citations (Scopus)

Abstract

The solitary LTRs of ERV-9 human endogenous retrovirus are middle repetitive DNAs associated with 3,000-4,000 human gene loci including the β-globin gene locus where the ERV-9 LTR is juxtaposed to the locus control region (β-LCR) far upstream of the globin genes. The ERV-9 LTRs are conserved during primate evolution, but their function in the primate genomes is unknown. Here, we show that in transgenic zebrafish harboring the β-globin ERV-9 LTR coupled to the GFP gene, the LTR enhancer was active and initiated synthesis of GFP mRNA in oocytes but not in spermatozoa, and GFP expression in the embryos was maternally inherited. The LTR enhancer was active also in stem/progenitor cell regions of adult tissues of transgenic zebrafish. In human tissues, ERV-9 LTR enhancer was active also in oocytes and stem/progenitor cells but not in spermatozoa and a number of differentiated, adult somatic cells. Transcriptional analyses of the human β-globin gene locus showed that the β-globin ERV-9 LTR enhancer initiated RNA synthesis from the LTR in the direction of the downstream β locus control region and globin genes in ovary and erythroid progenitor cells. The findings suggest that, during oogenesis, ERV-9 LTR enhancers in the human genome could activate the cis-linked gene loci to synthesize maternal mRNAs required for early embryogenesis. Alternatively, the ERV-9 LTR enhancers, in initiating RNA syntheses into the downstream genomic DNAs, could transcriptionally potentiate and preset chromatin structure of the cis-linked gene loci in oocytes and adult stem/progenitor cells.

Original languageEnglish (US)
Pages (from-to)805-810
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume101
Issue number3
DOIs
StatePublished - Jan 20 2004

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Endogenous Retroviruses
Zebrafish
Oocytes
Stem Cells
Globins
Genes
Locus Control Region
Primates
Spermatozoa
Stored Messenger RNA
RNA
Oogenesis
Erythroid Precursor Cells
Adult Stem Cells
DNA
Human Genome
Chromatin
Embryonic Development
Ovary
Embryonic Structures

ASJC Scopus subject areas

  • General

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The LTR enhancer of ERV-9 human endogenous retrovirus is active in oocytes and progenitor cells in transgenic zebrafish and humans. / Pi, Wenhu; Yang, Zhongan; Wang, Jian; Ruan, Ling; Yu, Xiuping; Ling, Jianhua; Krantz, Sanford; Isales, Carlos M; Conway, Simon J.; Lin, Shuo; Tuan Lo, Dorothy.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 101, No. 3, 20.01.2004, p. 805-810.

Research output: Contribution to journalArticle

Pi, Wenhu ; Yang, Zhongan ; Wang, Jian ; Ruan, Ling ; Yu, Xiuping ; Ling, Jianhua ; Krantz, Sanford ; Isales, Carlos M ; Conway, Simon J. ; Lin, Shuo ; Tuan Lo, Dorothy. / The LTR enhancer of ERV-9 human endogenous retrovirus is active in oocytes and progenitor cells in transgenic zebrafish and humans. In: Proceedings of the National Academy of Sciences of the United States of America. 2004 ; Vol. 101, No. 3. pp. 805-810.
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AU - Pi, Wenhu

AU - Yang, Zhongan

AU - Wang, Jian

AU - Ruan, Ling

AU - Yu, Xiuping

AU - Ling, Jianhua

AU - Krantz, Sanford

AU - Isales, Carlos M

AU - Conway, Simon J.

AU - Lin, Shuo

AU - Tuan Lo, Dorothy

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AB - The solitary LTRs of ERV-9 human endogenous retrovirus are middle repetitive DNAs associated with 3,000-4,000 human gene loci including the β-globin gene locus where the ERV-9 LTR is juxtaposed to the locus control region (β-LCR) far upstream of the globin genes. The ERV-9 LTRs are conserved during primate evolution, but their function in the primate genomes is unknown. Here, we show that in transgenic zebrafish harboring the β-globin ERV-9 LTR coupled to the GFP gene, the LTR enhancer was active and initiated synthesis of GFP mRNA in oocytes but not in spermatozoa, and GFP expression in the embryos was maternally inherited. The LTR enhancer was active also in stem/progenitor cell regions of adult tissues of transgenic zebrafish. In human tissues, ERV-9 LTR enhancer was active also in oocytes and stem/progenitor cells but not in spermatozoa and a number of differentiated, adult somatic cells. Transcriptional analyses of the human β-globin gene locus showed that the β-globin ERV-9 LTR enhancer initiated RNA synthesis from the LTR in the direction of the downstream β locus control region and globin genes in ovary and erythroid progenitor cells. The findings suggest that, during oogenesis, ERV-9 LTR enhancers in the human genome could activate the cis-linked gene loci to synthesize maternal mRNAs required for early embryogenesis. Alternatively, the ERV-9 LTR enhancers, in initiating RNA syntheses into the downstream genomic DNAs, could transcriptionally potentiate and preset chromatin structure of the cis-linked gene loci in oocytes and adult stem/progenitor cells.

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