Human pericentromeric tandemly repeated DNA is transcribed at the end of oocyte maturation and is associated with membraneless mitochondria-associated structures

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Human pericentromeric tandemly repeated DNA is transcribed at the end of oocyte maturation and is associated with membraneless mitochondria-associated structures. / Dobrynin, M. A.; Korchagina, N. M.; Prjibelski, A. D.; Shafranskaya, D.; Ostromyshenskii, D. I.; Shunkina, K.; Stepanova, I.; Kotova, A. V.; Podgornaya, O. I.; Enukashvily, N. I.

In: Scientific Reports, Vol. 10, No. 1, 19634, 12.11.2020.

Research output: Contribution to journal › Article › peer-review

BibTeX

@article{958207b120154603beae7fc4a66f3c56,

title = "Human pericentromeric tandemly repeated DNA is transcribed at the end of oocyte maturation and is associated with membraneless mitochondria-associated structures",

abstract = "Most of the human genome is non-coding. However, some of the non-coding part is transcriptionally active. In humans, the tandemly repeated (TR) pericentromeric non-coding DNA—human satellites 2 and 3 (HS2, HS3)—are transcribed in somatic cells. These transcripts are also found in pre- and post-implantation embryos. The aim of this study was to analyze HS2/HS3 transcription and cellular localization of transcripts in human maturating oocytes. The maternal HS2/HS3 TR transcripts transcribed from both strands were accumulated in the ooplasm in GV-MI oocytes as shown by DNA–RNA FISH (fluorescence in-situ hybridization). The transcripts{\textquoteright} content was higher in GV oocytes than in somatic cumulus cells according to real-time PCR. Using bioinformatics analysis, we demonstrated the presence of polyadenylated HS2 and HS3 RNAs in datasets of GV and MII oocyte transcriptomes. The transcripts shared a high degree of homology with HS2, HS3 transcripts previously observed in cancer cells. The HS2/HS3 transcripts were revealed by a combination of FISH and immunocytochemical staining within membraneless RNP structures that contained DEAD-box helicases DDX5 and DDX4. The RNP structures were closely associated with mitochondria, and are therefore similar to membraneless bodies described previously only in oogonia. These membraneless structures may be a site for spatial sequestration of RNAs and proteins in both maturating oocytes and cancer cells.",

keywords = "MESSENGER-RNA, SATELLITE DNA, BOVINE OOCYTES, TRANSCRIPTIONAL ACTIVITY, LAMPBRUSH CHROMOSOMES, SPLICING FACTORS, MOUSE OOCYTES, LOCALIZATION, PROTEIN, EXPRESSION",

author = "Dobrynin, {M. A.} and Korchagina, {N. M.} and Prjibelski, {A. D.} and D. Shafranskaya and Ostromyshenskii, {D. I.} and K. Shunkina and I. Stepanova and Kotova, {A. V.} and Podgornaya, {O. I.} and Enukashvily, {N. I.}",

note = "Funding Information: The work was supported by a grant from Russian Science Foundation (№19-74-20102). P.A.D. and S.D. were supported by St. Petersburg University, Russia (project ID 51555422). Publisher Copyright: {\textcopyright} 2020, The Author(s). Copyright: Copyright 2020 Elsevier B.V., All rights reserved.",

year = "2020",

month = nov,

day = "12",

doi = "10.1038/s41598-020-76628-8",

language = "English",

volume = "10",

journal = "Scientific Reports",

issn = "2045-2322",

publisher = "Nature Publishing Group",

number = "1",

}

RIS

TY - JOUR

T1 - Human pericentromeric tandemly repeated DNA is transcribed at the end of oocyte maturation and is associated with membraneless mitochondria-associated structures

AU - Dobrynin, M. A.

AU - Korchagina, N. M.

AU - Prjibelski, A. D.

AU - Shafranskaya, D.

AU - Ostromyshenskii, D. I.

AU - Shunkina, K.

AU - Stepanova, I.

AU - Kotova, A. V.

AU - Podgornaya, O. I.

AU - Enukashvily, N. I.

N1 - Funding Information: The work was supported by a grant from Russian Science Foundation (№19-74-20102). P.A.D. and S.D. were supported by St. Petersburg University, Russia (project ID 51555422). Publisher Copyright: © 2020, The Author(s). Copyright: Copyright 2020 Elsevier B.V., All rights reserved.

PY - 2020/11/12

Y1 - 2020/11/12

N2 - Most of the human genome is non-coding. However, some of the non-coding part is transcriptionally active. In humans, the tandemly repeated (TR) pericentromeric non-coding DNA—human satellites 2 and 3 (HS2, HS3)—are transcribed in somatic cells. These transcripts are also found in pre- and post-implantation embryos. The aim of this study was to analyze HS2/HS3 transcription and cellular localization of transcripts in human maturating oocytes. The maternal HS2/HS3 TR transcripts transcribed from both strands were accumulated in the ooplasm in GV-MI oocytes as shown by DNA–RNA FISH (fluorescence in-situ hybridization). The transcripts’ content was higher in GV oocytes than in somatic cumulus cells according to real-time PCR. Using bioinformatics analysis, we demonstrated the presence of polyadenylated HS2 and HS3 RNAs in datasets of GV and MII oocyte transcriptomes. The transcripts shared a high degree of homology with HS2, HS3 transcripts previously observed in cancer cells. The HS2/HS3 transcripts were revealed by a combination of FISH and immunocytochemical staining within membraneless RNP structures that contained DEAD-box helicases DDX5 and DDX4. The RNP structures were closely associated with mitochondria, and are therefore similar to membraneless bodies described previously only in oogonia. These membraneless structures may be a site for spatial sequestration of RNAs and proteins in both maturating oocytes and cancer cells.

AB - Most of the human genome is non-coding. However, some of the non-coding part is transcriptionally active. In humans, the tandemly repeated (TR) pericentromeric non-coding DNA—human satellites 2 and 3 (HS2, HS3)—are transcribed in somatic cells. These transcripts are also found in pre- and post-implantation embryos. The aim of this study was to analyze HS2/HS3 transcription and cellular localization of transcripts in human maturating oocytes. The maternal HS2/HS3 TR transcripts transcribed from both strands were accumulated in the ooplasm in GV-MI oocytes as shown by DNA–RNA FISH (fluorescence in-situ hybridization). The transcripts’ content was higher in GV oocytes than in somatic cumulus cells according to real-time PCR. Using bioinformatics analysis, we demonstrated the presence of polyadenylated HS2 and HS3 RNAs in datasets of GV and MII oocyte transcriptomes. The transcripts shared a high degree of homology with HS2, HS3 transcripts previously observed in cancer cells. The HS2/HS3 transcripts were revealed by a combination of FISH and immunocytochemical staining within membraneless RNP structures that contained DEAD-box helicases DDX5 and DDX4. The RNP structures were closely associated with mitochondria, and are therefore similar to membraneless bodies described previously only in oogonia. These membraneless structures may be a site for spatial sequestration of RNAs and proteins in both maturating oocytes and cancer cells.

KW - MESSENGER-RNA

KW - SATELLITE DNA

KW - BOVINE OOCYTES

KW - TRANSCRIPTIONAL ACTIVITY

KW - LAMPBRUSH CHROMOSOMES

KW - SPLICING FACTORS

KW - MOUSE OOCYTES

KW - LOCALIZATION

KW - PROTEIN

KW - EXPRESSION

UR - http://www.scopus.com/inward/record.url?scp=85095870016&partnerID=8YFLogxK

UR - https://www.mendeley.com/catalogue/765bfba7-dc06-31f6-9653-1fb4cc4a2c8e/

U2 - 10.1038/s41598-020-76628-8

DO - 10.1038/s41598-020-76628-8

M3 - Article

C2 - 33184340

AN - SCOPUS:85095870016

VL - 10

JO - Scientific Reports

JF - Scientific Reports

SN - 2045-2322

IS - 1

M1 - 19634

ER -

ID: 71075365