Unraveling Mitochondrial PiRNAs in Mouse Embryonic Gonadal Cells

Overview

Journal Sci Rep

Specialty Science

Date 2022 Jun 24

PMID 35750721

Authors

Odei Barrenada

Eduardo Larriba

Daniel Fernandez-Perez

Miguel Angel Brieno-Enriquez

Jesus Del Mazo Martinez

Affiliations

Soon will be listed here.

Abstract

Although mitochondria are widely studied organelles, the recent interest in the role of mitochondrial small noncoding RNAs (sncRNAs), miRNAs, and more recently, piRNAs, is providing new functional perspectives in germ cell development and differentiation. piRNAs (PIWI-interacting RNAs) are single-stranded sncRNAs of mostly about 20-35 nucleotides, generated from the processing of pre-piRNAs. We leverage next-generation sequencing data obtained from mouse primordial germ cells and somatic cells purified from early-differentiating embryonic ovaries and testis from 11.5 to 13.5 days postcoitum. Using bioinformatic tools, we elucidate (i) the origins of piRNAs as transcribed from mitochondrial DNA fragments inserted in the nucleus or from the mitochondrial genome; (ii) their levels of expression; and (iii) their potential roles, as well as their association with genomic regions encoding other sncRNAs (such as tRNAs and rRNAs) and the mitochondrial regulatory region (D-loop). Finally, our results suggest how nucleo-mitochondrial communication, both anterograde and retrograde signaling, may be mediated by mitochondria-associated piRNAs.

Citing Articles

Analysis of somatic piRNAs in the malaria mosquito reveals atypical classes of genic small RNAs.

Funikov S, Rezvykh A, Akulenko N, Liang J, Sharakhov I, Kalmykova A RNA Biol. 2025; 22(1):1-16.

PMID: 39916410 PMC: 11834523. DOI: 10.1080/15476286.2025.2463812.

Guidelines for mitochondrial RNA analysis.

Jusic A, Erpapazoglou Z, Dalgaard L, Lakkisto P, de Gonzalo-Calvo D, Benczik B Mol Ther Nucleic Acids. 2024; 35(3):102262.

PMID: 39091381 PMC: 11292373. DOI: 10.1016/j.omtn.2024.102262.

A landscape of mouse mitochondrial small non-coding RNAs.

Siniscalchi C, Di Palo A, Petito G, Senese R, Manfrevola F, De Leo I PLoS One. 2024; 19(1):e0293644.

PMID: 38165955 PMC: 10760717. DOI: 10.1371/journal.pone.0293644.

Mitochondrial Non-Coding RNAs Are Potential Mediators of Mitochondrial Homeostasis.

Sun W, Lu Y, Zhang H, Zhang J, Fang X, Wang J Biomolecules. 2022; 12(12).

PMID: 36551291 PMC: 9775270. DOI: 10.3390/biom12121863.

References

Zuo Y, Zou Q, Lin J, Jiang M, Liu X . 2lpiRNApred: a two-layered integrated algorithm for identifying piRNAs and their functions based on LFE-GM feature selection. RNA Biol. 2020; 17(6):892-902. PMC: 7549647. DOI: 10.1080/15476286.2020.1734382. View

Su J, Concilla A, Zhang D, Zhao F, Shen F, Zhang H . PIWI-interacting RNAs: Mitochondria-based biogenesis and functions in cancer. Genes Dis. 2021; 8(5):603-622. PMC: 8278532. DOI: 10.1016/j.gendis.2020.09.006. View

Kwon C, Tak H, Rho M, Chang H, Kim Y, Kim K . Detection of PIWI and piRNAs in the mitochondria of mammalian cancer cells. Biochem Biophys Res Commun. 2014; 446(1):218-23. DOI: 10.1016/j.bbrc.2014.02.112. View

Stein C, Genzor P, Mitra S, Elchert A, Ipsaro J, Benner L . Decoding the 5' nucleotide bias of PIWI-interacting RNAs. Nat Commun. 2019; 10(1):828. PMC: 6381166. DOI: 10.1038/s41467-019-08803-z. View

Le Thomas A, Fejes Toth K, Aravin A . To be or not to be a piRNA: genomic origin and processing of piRNAs. Genome Biol. 2014; 15(1):204. PMC: 4053809. DOI: 10.1186/gb4154. View

Zheng K, Xiol J, Reuter M, Eckardt S, Leu N, McLaughlin K . Mouse MOV10L1 associates with Piwi proteins and is an essential component of the Piwi-interacting RNA (piRNA) pathway. Proc Natl Acad Sci U S A. 2010; 107(26):11841-6. PMC: 2900664. DOI: 10.1073/pnas.1003953107. View

Yan Z, Hu H, Jiang X, Maierhofer V, Neb E, He L . Widespread expression of piRNA-like molecules in somatic tissues. Nucleic Acids Res. 2011; 39(15):6596-607. PMC: 3159465. DOI: 10.1093/nar/gkr298. View

Fu H, Feng J, Liu Q, Sun F, Tie Y, Zhu J . Stress induces tRNA cleavage by angiogenin in mammalian cells. FEBS Lett. 2008; 583(2):437-42. DOI: 10.1016/j.febslet.2008.12.043. View

Blumental-Perry A, Jobava R, Bederman I, Degar A, Kenche H, Guan B . Retrograde signaling by a mtDNA-encoded non-coding RNA preserves mitochondrial bioenergetics. Commun Biol. 2020; 3(1):626. PMC: 7603330. DOI: 10.1038/s42003-020-01322-4. View

10.

Liu Y, Dou M, Song X, Dong Y, Liu S, Liu H . The emerging role of the piRNA/piwi complex in cancer. Mol Cancer. 2019; 18(1):123. PMC: 6688334. DOI: 10.1186/s12943-019-1052-9. View

11.

Kozomara A, Birgaoanu M, Griffiths-Jones S . miRBase: from microRNA sequences to function. Nucleic Acids Res. 2018; 47(D1):D155-D162. PMC: 6323917. DOI: 10.1093/nar/gky1141. View

12.

Izumi N, Shoji K, Sakaguchi Y, Honda S, Kirino Y, Suzuki T . Identification and Functional Analysis of the Pre-piRNA 3' Trimmer in Silkworms. Cell. 2016; 164(5):962-73. PMC: 4856147. DOI: 10.1016/j.cell.2016.01.008. View

13.

Nishimura T, Nagamori I, Nakatani T, Izumi N, Tomari Y, Kuramochi-Miyagawa S . PNLDC1, mouse pre-piRNA Trimmer, is required for meiotic and post-meiotic male germ cell development. EMBO Rep. 2018; 19(3). PMC: 5836094. DOI: 10.15252/embr.201744957. View

14.

Chuma S, Hosokawa M, Tanaka T, Nakatsuji N . Ultrastructural characterization of spermatogenesis and its evolutionary conservation in the germline: germinal granules in mammals. Mol Cell Endocrinol. 2008; 306(1-2):17-23. DOI: 10.1016/j.mce.2008.11.009. View

15.

Wenda J, Homolka D, Yang Z, Spinelli P, Sachidanandam R, Pandey R . Distinct Roles of RNA Helicases MVH and TDRD9 in PIWI Slicing-Triggered Mammalian piRNA Biogenesis and Function. Dev Cell. 2017; 41(6):623-637.e9. PMC: 5481186. DOI: 10.1016/j.devcel.2017.05.021. View

16.

Dong Y, Yoshitomi T, Hu J, Cui J . Long noncoding RNAs coordinate functions between mitochondria and the nucleus. Epigenetics Chromatin. 2017; 10(1):41. PMC: 5569521. DOI: 10.1186/s13072-017-0149-x. View

17.

Spinelli J, Haigis M . The multifaceted contributions of mitochondria to cellular metabolism. Nat Cell Biol. 2018; 20(7):745-754. PMC: 6541229. DOI: 10.1038/s41556-018-0124-1. View

18.

Kim K . PIWI Proteins and piRNAs in the Nervous System. Mol Cells. 2019; 42(12):828-835. PMC: 6939654. DOI: 10.14348/molcells.2019.0241. View

19.

Sharp P . The centrality of RNA. Cell. 2009; 136(4):577-80. DOI: 10.1016/j.cell.2009.02.007. View

20.

Tsuzuki T, Nomiyama H, Setoyama C, Maeda S, Shimada K . Presence of mitochondrial-DNA-like sequences in the human nuclear DNA. Gene. 1983; 25(2-3):223-9. DOI: 10.1016/0378-1119(83)90226-3. View