Evidence map›Paper›PMID 23446454›Full record

ArticleBiology of reproduction2013

Disruption of a spermatogenic cell-specific mouse enolase 4 (eno4) gene causes sperm structural defects and male infertility.

Noriko Nakamura, Qunsheng Dai, Jason Williams, Eugenia H Goulding, William D Willis, Paula R Brown, Edward M Eddy

Open access · bronzeAbstract read
In one paragraph

Article in Biology of reproduction, 2013. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 52 papers, 1 of them a synthesis that pooled it.

0numbers the graph read from it
0cells of the map it votes in
52citing papers in PubMed, 1 pooled it
3.4field-weighted citation impact, top 7% 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

52 citing papers in PubMed, 1 synthesis or guideline pooled it, 100 citations in OpenAlex.

  1. Pooled it
  2. Enolase-1 and Inflammation.Biomolecules · 2026
    Review
  3. Article
  4. Article
  5. Review
  6. Article
  7. Review
  8. Article
  9. The Ultrastructure and Composition of Bovine Spermatozoa.Advances in anatomy, embryology, and cell biology · 2025
    Review
  10. Article
  11. Article
  12. Neuron-Specific Enolase-What Are We Measuring?International journal of molecular sciences · 2024
    Review
  13. Article
  14. Article
  15. Article
  16. Article
  17. Review
  18. Article
  19. ENO1 and Cancer.Molecular therapy oncolytics · 2022
    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

7 authors at 2 institutions in 1 country.

Noriko NakamuraGamete Biology Group, Laboratory of Reproductive and Developmental Toxicology, National Institute of Environmental Health Sciences, National Institutes of Health, Research Triangle Park, NC 27709, USA.
Qunsheng Dai
Jason Williams
Eugenia H Goulding
William D Willis
Paula R Brown
Edward M Eddy
National Institute of Environmental Health Sciences · USNational Institutes of Health · US

Funding

Protein Microcharacterization ZICES102488 · NIEHS · NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES · PI WILLIAMS, JASON · 2009 to 2025
$19.2M
Gene Expression In Spermatogenic CellsZIAES070076 · NIEHS · NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES · PI EDDY, EDWARD MITCHELL · 2009 to 2014
$12.6M
GERM CELL-SPECIFIC MOLECULES OF SPERMATOZOAZ01ES070076 · NIEHS · NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES · PI EDDY, EDWARD MITCHELL · 1985 to 2008
$4.6M
Intramural NIH HHS Z01 ES070076
6 · The paper itself

Abstract

Sperm utilize glycolysis to generate ATP required for motility, and several spermatogenic cell-specific glycolytic isozymes are associated with the fibrous sheath (FS) in the principal piece of the sperm flagellum. We used proteomics and molecular biology approaches to confirm earlier reports that a novel enolase is present in mouse sperm. We then found that a pan-enolase antibody, but not antibodies to ENO2 and ENO3, recognized a protein in the principal piece of the mouse sperm flagellum. Database analyses identified two previously uncharacterized enolase family-like candidate genes, 64306537H0Rik and Gm5506. Northern analysis indicated that 64306537H0Rik (renamed Eno4) was transcribed in testes of mice by Postnatal Day 12. To determine the role of ENO4, we generated mice using embryonic stem cells in which an Eno4 allele was disrupted by a gene trap containing a beta galactosidase (beta-gal) reporter (Eno4(+/Gt)). Expression of beta-gal occurred in the testis, and male mice homozygous for the gene trap allele (Eno4(Gt/Gt)) were infertile. Epididymal sperm numbers were 2-fold lower and sperm motility was reduced substantially in Eno4(Gt/Gt) mice compared to wild-type mice. Sperm from Eno4(Gt/Gt) mice had a coiled flagellum and a disorganized FS. The Gm5506 gene encodes a protein identical to ENO1 and also is transcribed at a low level in testis. We conclude that ENO4 is required for normal assembly of the FS and provides most of the enolase activity in sperm and that Eno1 and/or Gm5506 may encode a minor portion of the enolase activity in sperm.

Indexed as

AnimalsFemaleGene ExpressionInfertility, MaleMaleMiceMice, Inbred C57BLMice, TransgenicMutagenesisOrgan SpecificityPhosphopyruvate HydrataseSpermatogenesisSpermatozoaenolase 4 protein, mousePhosphopyruvate Hydratase

Identifiers

PMID23446454
PMCPMC4013874
OpenAlexW2103195924

What OpenQuestion holds

Textmetadata
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.