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Citations to this article

Expression of Piwi protein MIWI2 defines a distinct population of multiciliated cells
Gregory A. Wasserman, … , Dónal O’Carroll, Matthew R. Jones
Gregory A. Wasserman, … , Dónal O’Carroll, Matthew R. Jones
Published September 18, 2017
Citation Information: J Clin Invest. 2017;127(10):3866-3876. https://doi.org/10.1172/JCI94639.
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Concise Communication Cell biology Pulmonology Article has an altmetric score of 64

Expression of Piwi protein MIWI2 defines a distinct population of multiciliated cells

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Abstract

P-element–induced wimpy testes (Piwi) proteins are known for suppressing retrotransposon activation in the mammalian germline. However, whether Piwi protein or Piwi-dependent functions occur in the mammalian soma is unclear. Contrary to germline-restricted expression, we observed that Piwi-like Miwi2 mRNA is indeed expressed in epithelial cells of the lung in adult mice and that it is induced during pneumonia. Further investigation revealed that MIWI2 protein localized to the cytoplasm of a discrete population of multiciliated airway epithelial cells. Isolation and next-generation sequencing of MIWI2-positive multiciliated cells revealed that they are phenotypically distinct from neighboring MIWI2-negative multiciliated cells. Mice lacking MIWI2 exhibited an altered balance of airway epithelial cells, demonstrating fewer multiciliated cells and an increase in club cells. During pneumococcal pneumonia, Miwi2-deficient mice exhibited increased expression of inflammatory mediators and increased immune cell recruitment, leading to enhanced bacterial clearance. Taken together, our data delineate MIWI2-dependent functions outside of the germline and demonstrate the presence of distinct subsets of airway multiciliated cells that can be discriminated by MIWI2 expression. By demonstrating roles for MIWI2 in airway cell identity and pulmonary innate immunity, these studies elucidate unanticipated physiological functions for Piwi proteins in somatic tissues.

Authors

Gregory A. Wasserman, Aleksander D. Szymaniak, Anne C. Hinds, Kazuko Yamamoto, Hirofumi Kamata, Nicole M.S. Smith, Kristie L. Hilliard, Claudia Carrieri, Adam T. Labadorf, Lee J. Quinton, Xingbin Ai, Xaralabos Varelas, Felicia Chen, Joseph P. Mizgerd, Alan Fine, Dónal O’Carroll, Matthew R. Jones

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Total citations by year

Year: 2025 2024 2023 2022 2021 2019 2018 Total
Citations: 1 2 2 1 4 2 1 13
Citation information
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Citations to this article (13)

Title and authors Publication Year
Somatic Miwi2 modulates mitochondrial function in airway multiciliated cells and exacerbates influenza pathogenesis
Vasquez JH, Yuan J, Leow CJ, Crossey E, Shao F, Carty S, Dominguez VA, Lo M, Mizgerd JP, Fetterman JL, Lau NC, Fine A, Jones MR
iScience 2025
Integrative role of small non-coding RNAs in viral immune response: a systematic review.
Suleiman AA, Al-Chalabi R, Shaban SA
Molecular Biology Reports 2024
Somatic piRNA and PIWI-mediated post-transcriptional gene regulation in stem cells and disease
Patel MZ, Jiang Y, Kakumani PK
Frontiers in Cell and Developmental Biology 2024
Innate immune responses in pneumonia
Korkmaz FT, Traber KE
Pneumonia 2023
The emerging role of the piRNA/PIWI complex in respiratory tract diseases.
Yao Y, Li Y, Zhu X, Zhao C, Yang L, Huang X, Wang L
Respiratory Research 2023
Respiratory syncytial virus infection changes the piwi-interacting RNA content of airway epithelial cells
Corsello T, Kudlicki AS, Liu T, Casola A
Frontiers in Molecular Biosciences 2022
piRNAs and endo-siRNAs: Small molecules with large roles in the nervous system
MC Ow, SE Hall
Neurochemistry International 2021
PIWI-mediated control of tissue-specific transposons is essential for somatic cell differentiation
D Li, DH Taylor, JC van Wolfswinkel
Cell Reports 2021
Mammalian antiviral systems directed by small RNA
T Takahashi, SM Heaton, NF Parrish, CB Wilen
PLoS pathogens 2021
A Census of the Lung: CellCards from LungMAP
Sun X, Perl AK, Li R, Bell SM, Sajti E, Kalinichenko VV, Kalin TV, Misra RS, Deshmukh H, Clair G, Kyle J, Crotty Alexander LE, Masso Silva J, Kitzmiller JA, Wikenheiser-Brokamp KA, Deutsch G, Guo M, Du Y, Morley MP, Valdez MJ, Yu HV, Jin K, Bardes EE, Zepp JA, Neithamer T, Basil MC, Zacharias WJ, Verheyden J, Young R, Bandyopadhyay G, Lin S, Ansong C, Adkins J, Salomonis N, Arronow B, Xu Y, Pryhuber G, Whitsett J, Morrisey EE
Developmental Cell 2021
Non-lytic clearance of influenza B virus from infected cells preserves epithelial barrier function
RE Dumm, JK Fiege, BM Waring, CT Kuo, RA Langlois, NS Heaton
Nature Communications 2019
Roles of interleukin-11 during acute bacterial pneumonia
KE Traber, EL Dimbo, EM Symer, FT Korkmaz, MR Jones, JP Mizgerd, LJ Quinton, H Fehrenbach
PloS one 2019
Integrative Physiology of Pneumonia
LJ Quinton, AJ Walkey, JP Mizgerd
Physiological reviews 2018

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