Analysis of the human immunodeficiency virus-1 RNA packageome
- Matthew J. Eckwahl1,
- Helene Arnion1,
- Siarhei Kharytonchyk2,
- Trinity Zang3,4,5,
- Paul D. Bieniasz3,4,5,
- Alice Telesnitsky2 and
- Sandra L. Wolin1,6,7
- 1Department of Cell Biology, Yale School of Medicine, New Haven, Connecticut 06536, USA
- 2Department of Microbiology and Immunology, University of Michigan, Ann Arbor, Michigan 48109, USA
- 3Aaron Diamond AIDS Research Center, The Rockefeller University, New York, New York 10016, USA
- 4Laboratory of Retrovirology, The Rockefeller University, New York, New York 10016, USA
- 5Howard Hughes Medical Institute, The Rockefeller University, New York, New York 10016, USA
- 6Department of Molecular Biophysics and Biochemistry, Yale School of Medicine, New Haven, Connecticut 06536, USA
- 7Yale Cancer Center, Yale School of Medicine, New Haven, Connecticut 06520, USA
- Corresponding author: sandra.wolin{at}yale.edu
Abstract
All retroviruses package cellular RNAs into virions. Studies of murine leukemia virus (MLV) revealed that the major host cell RNAs encapsidated by this simple retrovirus were LTR retrotransposons and noncoding RNAs (ncRNAs). Several classes of ncRNAs appeared to be packaged by MLV shortly after synthesis, as precursors to tRNAs, small nuclear RNAs, and small nucleolar RNAs were all enriched in virions. To determine the extent to which the human immunodeficiency virus (HIV-1) packages similar RNAs, we used high-throughput sequencing to characterize the RNAs within infectious HIV-1 virions produced in CEM-SS T lymphoblastoid cells. We report that the most abundant cellular RNAs in HIV-1 virions are 7SL RNA and transcripts from numerous divergent and truncated members of the long interspersed element (LINE) and short interspersed element (SINE) families of retrotransposons. We also detected precursors to several tRNAs and small nuclear RNAs as well as transcripts derived from the ribosomal DNA (rDNA) intergenic spacers. We show that packaging of a pre-tRNA requires the nuclear export receptor Exportin 5, indicating that HIV-1 recruits at least some newly made ncRNAs in the cytoplasm. Together, our work identifies the set of RNAs packaged by HIV-1 and reveals that early steps in HIV-1 assembly intersect with host cell ncRNA biogenesis pathways.
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Article published online ahead of print. Article and publication date are at http://www.rnajournal.org/cgi/doi/10.1261/rna.057299.116.
- Received May 1, 2016.
- Accepted May 15, 2016.
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