Localization of the 16S mitochondrial rRNA in the nucleus of mammalian spermatogenic cells

Villegas, Jaime Eduardo Bernal; Araya, Pamela; Bustos‐Obregón, Eduardo; Burzio, Luis O.

doi:10.1093/molehr/8.11.977

Cited by 42 publications

(38 citation statements)

References 38 publications

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“…Cells cultured in 8-well chamber slides (Lab-Tek, NUNC) for 24 to 48 h or resting or PHA-stimulated human lymphocytes, were fixed in 4% p-formaldehyde for 10 min (2). ISH was done as described, using oligonucleotide probes labeled at the 3Ј end with digoxigenin-11-dUTP (2,22). For double FISH, cells were hybridized with dig-labeled probe 1 and biotin-labeled probe 3.…”

Section: Methodsmentioning

confidence: 99%

Expression of a family of noncoding mitochondrial RNAs distinguishes normal from cancer cells

Burzio

Villota

Villegas

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

113

198

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We reported the presence in human cells of a noncoding mitochondrial RNA that contains an inverted repeat (IR) of 815 nucleotides (nt) covalently linked to the 5 end of the mitochondrial 16S RNA (16S mtrRNA). The transcript contains a stem-loop structure and is expressed in human proliferating cells but not in resting cells. Here, we demonstrate that, in addition to this transcript, normal human proliferating cells in culture express 2 antisense mitochondrial transcripts. These transcripts also contain stem-loop structures but strikingly they are down-regulated in tumor cell lines and tumor cells present in 17 different tumor types. The differential expression of these transcripts distinguishes normal from tumor cells and might contribute a unique vision on cancer biology and diagnostics.differential expression in cancer ͉ RNAs with stem-loop structures R ecently, we described a novel human mitochondrial transcript of 2,374 nt that contains a long inverted repeat (IR) linked to the 5Ј end of the 16S mitochondrial rRNA (16S mtrRNA) (1, 2), which we designated noncoding mitochondrial RNA or ncmtRNA (2). The IR generates a stem-loop structure with an 820-bp doublestranded region and a 40-nt loop (2). In situ hybridization (ISH) showed that the ncmtRNA is overexpressed in several tumor cell lines but not in nondividing cells, suggesting that the ncmtRNA may play a role in cell proliferation (2).Because the results described before were obtained using tumor cell lines (2), we asked whether the ncmtRNA (from now on, sense ncmtRNA, SncmtRNA) is expressed in normal proliferating cells. Here we show that ISH of human umbilical vein endothelial cells (HUVEC), foreskin keratinocytes (HFK) (3), and human tonsil endothelial cells (HUTEC) (4) also express the SncmtRNA. However, and in striking contrast with tumor cell lines, ISH of normal proliferating cells revealed expression of antisense transcripts. These molecules were identified as 2 unique transcripts containing IRs linked to the 5Ј region of the antisense 16S mtRNA transcribed from the L-strand of the mtDNA (1, 2). We named these transcripts antisense ncmtRNA-1 (ASncmtRNA-1) and antisense ncmtRNA-2 (ASncmtRNA-2). Finally, we show that the antisense transcripts are also expressed in proliferating cells present in normal human tissues but are down-regulated in cells present in human tumors of different types and patients.

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Section: Methodsmentioning

confidence: 99%

Expression of a family of noncoding mitochondrial RNAs distinguishes normal from cancer cells

Burzio

Villota

Villegas

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

113

198

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“…Additionally, 16S mitochondrial rRNA are localized in the nucleus of mouse spermatogenic cells and human spermatozoa (Villegas et al 2002) indicating that these rRNAs may form ribosomes in the nucleus. Protein translation takes place in the nuclei of HeLa cells (Iborra et al 2001) via 80S ribosomes, which raises the possibility that unexpected cellular loci may control atypical translation processes.…”

Section: S]methionine (Met)-[mentioning

confidence: 99%

Mammalian sperm translate nuclear-encoded proteins by mitochondrial-type ribosomes

Gur¹,

Breitbart²

2006

Genes Dev.

318

254

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It is widely accepted that spermatozoa are translationally silent. The present study demonstrates, for the first time, incorporation of labeled amino acids into polypeptides during sperm capacitation, which was completely inhibited by mitochondrial translation inhibitors but not by the cytoplasmic translation inhibitor. Unlike 80S cytoplasmic ribosomes, 55S mitochondrial ribosomes were present in polysomal fractions, indicating that these ribosomes are actively involved in protein translation in spermatozoa. Inhibition of protein translation significantly reduced sperm motility, capacitation and in vitro fertilization rate. Thus, contrary to the accepted dogma, nuclear genes are expressed as proteins in sperm during their residence in the female reproductive tract until fertilization.Supplemental material is available at http://genesdev.org.

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“…Mitochondrially-derived ribosomes also form on germinal granules, structures very similar to polar granules, that are present in Xenopus germ plasm [70,71]. Recently, 16S rRNA was found outside the mitochondria in human testis, localized to the nuclei of spermatogenic cells, which suggests that mitochondrial ribosomes may have a function in the mammalian germline [72].…”

Section: Mitochondrial Rrna and Germ Cell Specificationmentioning

confidence: 99%

Tudor and its domains: germ cell formation from a Tudor perspective

Thomson

Lasko

2005

Cell Res

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In many metazoan species, germ cell formation requires the germ plasm, a specialized cytoplasm which often contains electron dense structures. Genes required for germ cell formation in Drosophila have been isolated predominantly in screens for maternal-effect mutations. One such gene is tudor (tud); without proper tud function germ cell formation does not occur. Unlike other genes involved in Drosophila germ cell specification tud is dispensable for other somatic functions such as abdominal patterning. It is not known how TUD contributes at a molecular level to germ cell formation but in tud mutants, polar granule formation is severely compromised, and mitochondrially encoded ribosomal RNAs do not localize to the polar granule. TUD is composed of 11 repeats of the protein motif called the Tudor domain. There are similar proteins to TUD in the germ line of other metazoan species including mice. Probable vertebrate orthologues of Drosophila genes involved in germ cell specification will be discussed.

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Localization of the 16S mitochondrial rRNA in the nucleus of mammalian spermatogenic cells

Cited by 42 publications

References 38 publications

Expression of a family of noncoding mitochondrial RNAs distinguishes normal from cancer cells

Expression of a family of noncoding mitochondrial RNAs distinguishes normal from cancer cells

Mammalian sperm translate nuclear-encoded proteins by mitochondrial-type ribosomes

Tudor and its domains: germ cell formation from a Tudor perspective

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