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The evolution and expression of the snaR family of small non-coding RNAs.

Parrott AM, Tsai M, Batchu P, Ryan K, Ozer HL, Tian B, Mathews MB - Nucleic Acids Res. (2010)

Bottom Line: We recently identified the snaR family of small non-coding RNAs that associate in vivo with the nuclear factor 90 (NF90/ILF3) protein.The major human species, snaR-A, is an RNA polymerase III transcript with restricted tissue distribution and orthologs in chimpanzee but not rhesus macaque or mouse.We infer that snaR evolved from the left monomer of the primate-specific Alu SINE family via ASR and CAS in conjunction with major primate speciation events, and suggest that snaRs participate in tissue- and species-specific regulation of cell growth and translation.

View Article: PubMed Central - PubMed

Affiliation: Department of Biochemistry and Molecular Biology, New Jersey Medical School, UMDNJ, Newark, New Jersey, USA.

ABSTRACT
We recently identified the snaR family of small non-coding RNAs that associate in vivo with the nuclear factor 90 (NF90/ILF3) protein. The major human species, snaR-A, is an RNA polymerase III transcript with restricted tissue distribution and orthologs in chimpanzee but not rhesus macaque or mouse. We report their expression in human tissues and their evolution in primates. snaR genes are exclusively in African Great Apes and some are unique to humans. Two novel families of snaR-related genetic elements were found in primates: CAS (catarrhine ancestor of snaR), limited to Old World Monkeys and apes; and ASR (Alu/snaR-related), present in all monkeys and apes. ASR and CAS appear to have spread by retrotransposition, whereas most snaR genes have spread by segmental duplication. snaR-A and snaR-G2 are differentially expressed in discrete regions of the human brain and other tissues, notably including testis. snaR-A is up-regulated in transformed and immortalized human cells, and is stably bound to ribosomes in HeLa cells. We infer that snaR evolved from the left monomer of the primate-specific Alu SINE family via ASR and CAS in conjunction with major primate speciation events, and suggest that snaRs participate in tissue- and species-specific regulation of cell growth and translation.

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snaR molecular evolution from FLAM C via ASR and CAS. (A) Schematic of syntenic regions of chromosome 19 in rhesus macaque (56.819–56.825 Mb), human (55.798–55.804 Mb) and orangutan (52.171–52.174 Mb), containing ∼1.9 Kb repeats (open boxes). CAS elements and snaR-F are indicated in green and AluSx in gray, with direction of transcription indicated by arrows. (B) Clustal-X alignment of selected snaR genes and CAS elements from humans (Hs), chimpanzee (Pt), orangutan (Pa) and rhesus macaque (Mm). Internal expansions ε1 and ε2 and a putative Pol III B box are indicated. The putative CAS Pol III A box is in a dashed box and is based on the tRNA consensus displayed below the alignment: invariant nucleotides are in red (27). (C) Clustal-X alignment of selected primate CAS, ASR and Alu elements. Deletions δ1 and δ2 are indicated. Elements are annotated in Supplementary Data 3. Alu Pol III A and B boxes are shown and their consensus sequences (74) displayed below the alignment; putative CAS Pol III A box is dashed and compared to a tRNA A box consensus displayed above the alignment. (D) Schematic of the major molecular deletions (in red) and expansions (in green) inferred to have occurred during the evolution of ASR, CAS, snaR-12 and snaR genes from FLAM C. Pol III A and B boxes are represented by gray and black boxes, respectively. Schematics A and D are modified from (32).
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Figure 3: snaR molecular evolution from FLAM C via ASR and CAS. (A) Schematic of syntenic regions of chromosome 19 in rhesus macaque (56.819–56.825 Mb), human (55.798–55.804 Mb) and orangutan (52.171–52.174 Mb), containing ∼1.9 Kb repeats (open boxes). CAS elements and snaR-F are indicated in green and AluSx in gray, with direction of transcription indicated by arrows. (B) Clustal-X alignment of selected snaR genes and CAS elements from humans (Hs), chimpanzee (Pt), orangutan (Pa) and rhesus macaque (Mm). Internal expansions ε1 and ε2 and a putative Pol III B box are indicated. The putative CAS Pol III A box is in a dashed box and is based on the tRNA consensus displayed below the alignment: invariant nucleotides are in red (27). (C) Clustal-X alignment of selected primate CAS, ASR and Alu elements. Deletions δ1 and δ2 are indicated. Elements are annotated in Supplementary Data 3. Alu Pol III A and B boxes are shown and their consensus sequences (74) displayed below the alignment; putative CAS Pol III A box is dashed and compared to a tRNA A box consensus displayed above the alignment. (D) Schematic of the major molecular deletions (in red) and expansions (in green) inferred to have occurred during the evolution of ASR, CAS, snaR-12 and snaR genes from FLAM C. Pol III A and B boxes are represented by gray and black boxes, respectively. Schematics A and D are modified from (32).

Mentions: To determine whether similar elements exist in lower primates, we conducted a BLAT search for the orangutan Pa19 clone sequence against the rhesus macaque genome. Similarity (85.5% identity over 297 bp) was identified with a segment on macaque chromosome 19. This macaque segment is part of a larger sequence that is demarcated by a SINE, AluSx, into three tandem repeats of ∼1.9 Kb (Figure 3A and Supplementary Figure S3; Supplementary Data S2). These repeats are conserved, at least partially, in other primates. A syntenic triple tandem repeat is present on human chromosome 19 (Figure 3A). Orthology corresponding to ∼1.5 repeats was found on orangutan chromosome 19 (at 52.170–52.174 Mb; Supplementary Figure S3), and with ‘undescribed’ portions of the draft orangutan genome. Similarly, orthology was observed on chimpanzee chromosome 19 (at 56.280–56.284 Mb) and with unassigned genomic sequences (not shown).Figure 3.


The evolution and expression of the snaR family of small non-coding RNAs.

Parrott AM, Tsai M, Batchu P, Ryan K, Ozer HL, Tian B, Mathews MB - Nucleic Acids Res. (2010)

snaR molecular evolution from FLAM C via ASR and CAS. (A) Schematic of syntenic regions of chromosome 19 in rhesus macaque (56.819–56.825 Mb), human (55.798–55.804 Mb) and orangutan (52.171–52.174 Mb), containing ∼1.9 Kb repeats (open boxes). CAS elements and snaR-F are indicated in green and AluSx in gray, with direction of transcription indicated by arrows. (B) Clustal-X alignment of selected snaR genes and CAS elements from humans (Hs), chimpanzee (Pt), orangutan (Pa) and rhesus macaque (Mm). Internal expansions ε1 and ε2 and a putative Pol III B box are indicated. The putative CAS Pol III A box is in a dashed box and is based on the tRNA consensus displayed below the alignment: invariant nucleotides are in red (27). (C) Clustal-X alignment of selected primate CAS, ASR and Alu elements. Deletions δ1 and δ2 are indicated. Elements are annotated in Supplementary Data 3. Alu Pol III A and B boxes are shown and their consensus sequences (74) displayed below the alignment; putative CAS Pol III A box is dashed and compared to a tRNA A box consensus displayed above the alignment. (D) Schematic of the major molecular deletions (in red) and expansions (in green) inferred to have occurred during the evolution of ASR, CAS, snaR-12 and snaR genes from FLAM C. Pol III A and B boxes are represented by gray and black boxes, respectively. Schematics A and D are modified from (32).
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Figure 3: snaR molecular evolution from FLAM C via ASR and CAS. (A) Schematic of syntenic regions of chromosome 19 in rhesus macaque (56.819–56.825 Mb), human (55.798–55.804 Mb) and orangutan (52.171–52.174 Mb), containing ∼1.9 Kb repeats (open boxes). CAS elements and snaR-F are indicated in green and AluSx in gray, with direction of transcription indicated by arrows. (B) Clustal-X alignment of selected snaR genes and CAS elements from humans (Hs), chimpanzee (Pt), orangutan (Pa) and rhesus macaque (Mm). Internal expansions ε1 and ε2 and a putative Pol III B box are indicated. The putative CAS Pol III A box is in a dashed box and is based on the tRNA consensus displayed below the alignment: invariant nucleotides are in red (27). (C) Clustal-X alignment of selected primate CAS, ASR and Alu elements. Deletions δ1 and δ2 are indicated. Elements are annotated in Supplementary Data 3. Alu Pol III A and B boxes are shown and their consensus sequences (74) displayed below the alignment; putative CAS Pol III A box is dashed and compared to a tRNA A box consensus displayed above the alignment. (D) Schematic of the major molecular deletions (in red) and expansions (in green) inferred to have occurred during the evolution of ASR, CAS, snaR-12 and snaR genes from FLAM C. Pol III A and B boxes are represented by gray and black boxes, respectively. Schematics A and D are modified from (32).
Mentions: To determine whether similar elements exist in lower primates, we conducted a BLAT search for the orangutan Pa19 clone sequence against the rhesus macaque genome. Similarity (85.5% identity over 297 bp) was identified with a segment on macaque chromosome 19. This macaque segment is part of a larger sequence that is demarcated by a SINE, AluSx, into three tandem repeats of ∼1.9 Kb (Figure 3A and Supplementary Figure S3; Supplementary Data S2). These repeats are conserved, at least partially, in other primates. A syntenic triple tandem repeat is present on human chromosome 19 (Figure 3A). Orthology corresponding to ∼1.5 repeats was found on orangutan chromosome 19 (at 52.170–52.174 Mb; Supplementary Figure S3), and with ‘undescribed’ portions of the draft orangutan genome. Similarly, orthology was observed on chimpanzee chromosome 19 (at 56.280–56.284 Mb) and with unassigned genomic sequences (not shown).Figure 3.

Bottom Line: We recently identified the snaR family of small non-coding RNAs that associate in vivo with the nuclear factor 90 (NF90/ILF3) protein.The major human species, snaR-A, is an RNA polymerase III transcript with restricted tissue distribution and orthologs in chimpanzee but not rhesus macaque or mouse.We infer that snaR evolved from the left monomer of the primate-specific Alu SINE family via ASR and CAS in conjunction with major primate speciation events, and suggest that snaRs participate in tissue- and species-specific regulation of cell growth and translation.

View Article: PubMed Central - PubMed

Affiliation: Department of Biochemistry and Molecular Biology, New Jersey Medical School, UMDNJ, Newark, New Jersey, USA.

ABSTRACT
We recently identified the snaR family of small non-coding RNAs that associate in vivo with the nuclear factor 90 (NF90/ILF3) protein. The major human species, snaR-A, is an RNA polymerase III transcript with restricted tissue distribution and orthologs in chimpanzee but not rhesus macaque or mouse. We report their expression in human tissues and their evolution in primates. snaR genes are exclusively in African Great Apes and some are unique to humans. Two novel families of snaR-related genetic elements were found in primates: CAS (catarrhine ancestor of snaR), limited to Old World Monkeys and apes; and ASR (Alu/snaR-related), present in all monkeys and apes. ASR and CAS appear to have spread by retrotransposition, whereas most snaR genes have spread by segmental duplication. snaR-A and snaR-G2 are differentially expressed in discrete regions of the human brain and other tissues, notably including testis. snaR-A is up-regulated in transformed and immortalized human cells, and is stably bound to ribosomes in HeLa cells. We infer that snaR evolved from the left monomer of the primate-specific Alu SINE family via ASR and CAS in conjunction with major primate speciation events, and suggest that snaRs participate in tissue- and species-specific regulation of cell growth and translation.

Show MeSH
Related in: MedlinePlus