Evidence map›Paper›PMID 24810616›Full record

ArticlePLoS genetics2014

Paternal poly (ADP-ribose) metabolism modulates retention of inheritable sperm histones and early embryonic gene expression.

Motomasa Ihara, Mirella L Meyer-Ficca, N Adrian Leu, Shilpa Rao, Fan Li, Brian D Gregory, Irina A Zalenskaya, Richard M Schultz, Ralph G Meyer

Open access · goldAbstract read
In one paragraph

Article in PLoS genetics, 2014. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 45 papers.

0numbers the graph read from it
0cells of the map it votes in
45citing papers in PubMed
4.0field-weighted citation impact, top 5% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

45 citing papers in PubMed, 92 citations in OpenAlex.

  1. Review
  2. Review
  3. Article
  4. Article
  5. Review
  6. International journal of molecular sciences · 2024
    Article
  7. Article
  8. Review
  9. Article
  10. Review
  11. Article
  12. Article
  13. Article
  14. Review
  15. Review
  16. Review
  17. Metabolism in Male Reproductive Aging.Advances in geriatric medicine and research · 2021
    Article
  18. Review
  19. Review
  20. Article
4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

9 authors at 2 institutions in 1 country.

Motomasa IharaDepartment of Animal Biology and Center for Animal Transgenesis and Germ Cell Research, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America; Department of Biology, School of Arts and Sciences, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America.
Mirella L Meyer-FiccaDepartment of Animal Biology and Center for Animal Transgenesis and Germ Cell Research, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America.
N Adrian LeuDepartment of Animal Biology and Center for Animal Transgenesis and Germ Cell Research, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America.
Shilpa RaoSchool of Medicine, Microarray Core Facility, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America.
Fan LiDepartment of Biology, School of Arts and Sciences, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America; School of Arts and Sciences, Penn Genome Frontiers Institute, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America.
Brian D GregoryDepartment of Biology, School of Arts and Sciences, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America; School of Arts and Sciences, Penn Genome Frontiers Institute, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America.
Irina A ZalenskayaCONRAD, Department of Obstetrics and Gynecology, Eastern Virginia Medical School, Norfolk, Virginia, United States of America.
Richard M SchultzDepartment of Biology, School of Arts and Sciences, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America.
Ralph G MeyerDepartment of Animal Biology and Center for Animal Transgenesis and Germ Cell Research, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America.
University of Pennsylvania · USEastern Virginia Medical School · US

Funding

Translational Research Support CoreP30ES013508 · NIEHS · UNIVERSITY OF PENNSYLVANIA · PI Rebecca A Simmons · 2006 to 2026
$35.3M
Research Project 4: Epigenetic Regulation of Retrotransposon Silencing and Male Fertility in the MouseP50HD068157 · NICHD · UNIVERSITY OF PENNSYLVANIA · PI Suneeta Senapati · 2014 to 2026
$16.3M
PROJECT 4: TARGETING ADP-RIBOSE POLYMER DEPENDENT EPIGENETIC EVENTS IN MALE LINEU54HD068157 · NICHD · UNIVERSITY OF PENNSYLVANIA · PI COUTIFARIS, CHRISTOS · 2011 to 2013
$4.8M
PROTEIN PHOSPHORYLATION IN PREIMPLANTATION DEVELOPMENTR01HD022681 · NICHD · UNIVERSITY OF PENNSYLVANIA · PI SCHULTZ, RICHARD MORRIS · 1987 to 2017
$3.6M
GENE EXPRESSION IN THE PREIMPLANTATION EMBRYOR37HD022681 · NICHD · UNIVERSITY OF PENNSYLVANIA · PI SCHULTZ, RICHARD M · 1997 to 2006
$2.2M
ADP-Ribose Polymer Metabolism in SpermatogenesisR01HD048837 · NICHD · UNIVERSITY OF PENNSYLVANIA · PI MEYER, RALPH G · 2005 to 2009
$1.4M
NICHD NIH HHS HD022681NICHD NIH HHS HD48837NICHD NIH HHS P50 HD068157NICHD NIH HHS R01 HD022681NICHD NIH HHS R01 HD048837NICHD NIH HHS R37 HD022681NICHD NIH HHS U54 HD068157NICHD NIH HHS U54HD068157NIEHS NIH HHS P30 ES013508NIEHS NIH HHS P30-ES013508
6 · The paper itself

Abstract

To achieve the extreme nuclear condensation necessary for sperm function, most histones are replaced with protamines during spermiogenesis in mammals. Mature sperm retain only a small fraction of nucleosomes, which are, in part, enriched on gene regulatory sequences, and recent findings suggest that these retained histones provide epigenetic information that regulates expression of a subset of genes involved in embryo development after fertilization. We addressed this tantalizing hypothesis by analyzing two mouse models exhibiting abnormal histone positioning in mature sperm due to impaired poly(ADP-ribose) (PAR) metabolism during spermiogenesis and identified altered sperm histone retention in specific gene loci genome-wide using MNase digestion-based enrichment of mononucleosomal DNA. We then set out to determine the extent to which expression of these genes was altered in embryos generated with these sperm. For control sperm, most genes showed some degree of histone association, unexpectedly suggesting that histone retention in sperm genes is not an all-or-none phenomenon and that a small number of histones may remain associated with genes throughout the genome. The amount of retained histones, however, was altered in many loci when PAR metabolism was impaired. To ascertain whether sperm histone association and embryonic gene expression are linked, the transcriptome of individual 2-cell embryos derived from such sperm was determined using microarrays and RNA sequencing. Strikingly, a moderate but statistically significant portion of the genes that were differentially expressed in these embryos also showed different histone retention in the corresponding gene loci in sperm of their fathers. These findings provide new evidence for the existence of a linkage between sperm histone retention and gene expression in the embryo.

Indexed as

Gene Expression Regulation, DevelopmentalAnimalsChromatinEmbryo, MammalianFemaleHistonesMaleMiceOligonucleotide Array Sequence AnalysisPoly Adenosine Diphosphate RiboseRNA, MessengerSpermatozoaChromatinHistonesPoly Adenosine Diphosphate RiboseRNA, Messenger

Identifiers

PMID24810616
PMCPMC4014456
OpenAlexW2082444663

What OpenQuestion holds

Textmetadata
LicenceCC BY
Read underepoch 390

Registered trials

None linked

Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.