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Article

Distinct Roles of NANOS1 and NANOS3 in the Cell Cycle and NANOS3-PUM1-FOXM1 Axis to Control G2/M Phase in a Human Primordial Germ Cell Model

by
Erkut Ilaslan
1,*,
Krystyna Kwiatkowska
1,
Maciej Jerzy Smialek
1,2,
Marcin Piotr Sajek
1,3,4,
Zaneta Lemanska
1,
Matisa Alla
1,
Damian Mikolaj Janecki
1,†,
Jadwiga Jaruzelska
1 and
Kamila Kusz-Zamelczyk
1,*
1
Institute of Human Genetics, Polish Academy of Sciences, 60-479 Poznan, Poland
2
Biozentrum, University of Basel, 4056 Basel, Switzerland
3
RNA Bioscience Initiative, University of Colorado School of Medicine, Aurora, CO 80045, USA
4
Department of Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Aurora, CO 80045, USA
*
Authors to whom correspondence should be addressed.
†
Current address: Institute of Bioorganic Chemistry, Polish Academy of Sciences, 61-704 Poznan, Poland.
Int. J. Mol. Sci. 2022, 23(12), 6592; https://doi.org/10.3390/ijms23126592
Submission received: 20 May 2022 / Revised: 7 June 2022 / Accepted: 10 June 2022 / Published: 13 June 2022
(This article belongs to the Special Issue RNA-Binding Proteins and Their Emerging Roles in Cancer 2.0)
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Abstract

Nanos RNA-binding proteins are critical factors of germline development throughout the animal kingdom and their dysfunction causes infertility. During evolution, mammalian Nanos paralogues adopted divergent roles in germ cell biology. However, the molecular basis behind this divergence, such as their target mRNAs, remains poorly understood. Our RNA-sequencing analysis in a human primordial germ cell model-TCam-2 cell line revealed distinct pools of genes involved in the cell cycle process downregulated upon NANOS1 and NANOS3 overexpression. We show that NANOS1 and NANOS3 proteins influence different stages of the cell cycle. Namely, NANOS1 is involved in the G1/S and NANOS3 in the G2/M phase transition. Many of their cell cycle targets are known infertility and cancer-germ cell genes. Moreover, NANOS3 in complex with RNA-binding protein PUM1 causes 3′UTR-mediated repression of FOXM1 mRNA encoding a transcription factor crucial for G2/M phase transition. Interestingly, while NANOS3 and PUM1 act as post-transcriptional repressors of FOXM1, FOXM1 potentially acts as a transcriptional activator of NANOS3, PUM1, and itself. Finally, by utilizing publicly available RNA-sequencing datasets, we show that the balance between FOXM1-NANOS3 and FOXM1-PUM1 expression levels is disrupted in testis cancer, suggesting a potential role in this disease.
Keywords: NANOS1; NANOS3; PUM1; FOXM1; human primordial germ cells; cell cycle; germ cell cancer NANOS1; NANOS3; PUM1; FOXM1; human primordial germ cells; cell cycle; germ cell cancer

Share and Cite

MDPI and ACS Style

Ilaslan, E.; Kwiatkowska, K.; Smialek, M.J.; Sajek, M.P.; Lemanska, Z.; Alla, M.; Janecki, D.M.; Jaruzelska, J.; Kusz-Zamelczyk, K. Distinct Roles of NANOS1 and NANOS3 in the Cell Cycle and NANOS3-PUM1-FOXM1 Axis to Control G2/M Phase in a Human Primordial Germ Cell Model. Int. J. Mol. Sci. 2022, 23, 6592. https://doi.org/10.3390/ijms23126592

AMA Style

Ilaslan E, Kwiatkowska K, Smialek MJ, Sajek MP, Lemanska Z, Alla M, Janecki DM, Jaruzelska J, Kusz-Zamelczyk K. Distinct Roles of NANOS1 and NANOS3 in the Cell Cycle and NANOS3-PUM1-FOXM1 Axis to Control G2/M Phase in a Human Primordial Germ Cell Model. International Journal of Molecular Sciences. 2022; 23(12):6592. https://doi.org/10.3390/ijms23126592

Chicago/Turabian Style

Ilaslan, Erkut, Krystyna Kwiatkowska, Maciej Jerzy Smialek, Marcin Piotr Sajek, Zaneta Lemanska, Matisa Alla, Damian Mikolaj Janecki, Jadwiga Jaruzelska, and Kamila Kusz-Zamelczyk. 2022. "Distinct Roles of NANOS1 and NANOS3 in the Cell Cycle and NANOS3-PUM1-FOXM1 Axis to Control G2/M Phase in a Human Primordial Germ Cell Model" International Journal of Molecular Sciences 23, no. 12: 6592. https://doi.org/10.3390/ijms23126592

APA Style

Ilaslan, E., Kwiatkowska, K., Smialek, M. J., Sajek, M. P., Lemanska, Z., Alla, M., Janecki, D. M., Jaruzelska, J., & Kusz-Zamelczyk, K. (2022). Distinct Roles of NANOS1 and NANOS3 in the Cell Cycle and NANOS3-PUM1-FOXM1 Axis to Control G2/M Phase in a Human Primordial Germ Cell Model. International Journal of Molecular Sciences, 23(12), 6592. https://doi.org/10.3390/ijms23126592

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