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Published ahead of print on December 12, 2002, doi:10.1164/rccm.200206-518OC

Am. J. Respir. Crit. Care Med., Volume 167, Number 4, February 2003, 570-579

A more recent version of this article appeared on February 15, 2003
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Submitted on June 5, 2002
Accepted on December 11, 2002

Post-Lipopolysaccharide Oxidative Damage of Mitochondrial DNA

Hagir B Suliman1, Martha S Carraway1, and Claude A Piantadosi1*

1 Medicine, Duke University Medical Center, Durham, NC, USA

* To whom correspondence should be addressed. E-mail: Piant001{at}mc.duke.edu.

Selected structural and functional alterations of mitochondria induced by bacterial lipopolysaccharide (LPS) were investigated on the basis of the hypothesis that LPS initiates hepatic mitochondrial DNA (mtDNA) damage by oxidative mechanisms. After a single intraperitoneal injection of E coli LPS, liver mtDNA copy number decreased by Southern analysis within 24 hours relative to the nuclear 18S rRNA (p<0.05). LPS induced a novel oxidant- dependent 3.8Kb mtDNA deletion in the region coding for NADH dehydrogenase subunits ND1 and 2 and cytochrome c oxidase subunit I (COX I) that correlated with mitochondrial glutathione (GSH) depletion. Expression of mt-mRNA and transcription of mt-RNA were suppressed, whereas mRNA expression increased for selected nuclear-encoded mitochondrial proteins. Resolution of mtDNA damage was mediated by importation of transcription-factor A (Tfam) protein, a central regulator of mtDNA copy number, accompanied by binding of mitochondrial protein extract to the Tfam-DNA binding site. Hence, mtDNA integrity and transcriptional capacity after LPS appeared to be re-instated by mitochondrial biogenesis. These data provide the first link between LPS-mediated hepatic injury and a specific oxidative mtDNA deletion, which inhibits mitochondrial transcription and is restored by activation of mechanisms that lead to biogenesis.
Key words: mitochondria, sepsis, reactive oxygen species, glutathione




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