Role of Disulfide Bonds on DNA Packaging Forces in Bull Sperm Chromatin

James M. Hutchison, Donald C. Rau, Jason E. DeRouchey

Research output: Contribution to journalArticlepeer-review

22 Scopus citations

Abstract

Short arginine-rich proteins called protamines mediate the near crystalline DNA packaging in most vertebrate sperm cells. Protamines are synthesized during spermiogenesis and condense the paternal genome into a transcriptionally inactive state in late-stage spermatids. Protamines from eutherian mammals, including bulls and humans, also contain multiple cysteine residues that form intra- and interprotamine sulfur-sulfur bonds during the final stages of sperm maturation. Although the cross-linked protamine network is known to stabilize the resulting nucleoprotamine structure, little is known about the role of disulfide bonds on DNA condensation in the mammalian sperm. Using small angle x-ray scattering, we show that isolated bull nuclei achieve slightly lower DNA packing densities compared to salmon nuclei despite salmon protamine lacking cysteine residues. Surprisingly, reduction of the intermolecular sulfur-sulfur bonds of bull protamine results in tighter DNA packing. Complete reduction of the intraprotamine disulfide bonds ultimately leads to decondensation, suggesting that disulfide-mediated secondary structure is also critical for proper protamine function. Lastly, comparison of multiple bull collections showed some to have aberrant x-ray scattering profiles consistent with incorrect disulfide bond formation. Together, these observations shed light on the biological functions of disulfide linkages for in vivo DNA packaging in sperm chromatin.

Original languageEnglish
Pages (from-to)1925-1933
Number of pages9
JournalBiophysical Journal
Volume113
Issue number9
DOIs
StatePublished - Nov 7 2017

Bibliographical note

Funding Information:
Acknowledgment is made by J.E.D. to the National Science Foundation (CAREER Award MCB-1453168 ) and by D.C.R. to the Intramural Research Programs of the Eunice Kennedy Shriver National Institute of Child Health and Human Development for support of this work.

Publisher Copyright:
© 2017 Biophysical Society

ASJC Scopus subject areas

  • Biophysics

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