Cyclic AMP induces reversible EPAC1 condensates that regulate histone transcription

Liliana Felicia Iannucci, Anna Maria D’Erchia, Ernesto Picardi, Daniela Bettio, Filippo Conca, Nicoletta Concetta Surdo, Giulietta Benedetto, Deborah Musso, Cristina Arrigoni, Marco Lolicato, Mauro Vismara, Francesca Grisan, Leonardo Salviati, Luciano Milanesi, Graziano Pesole and Konstantinos Lefkimmiatis ()
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Liliana Felicia Iannucci: University of Pavia
Anna Maria D’Erchia: University of Bari “Aldo Moro”
Ernesto Picardi: University of Bari “Aldo Moro”
Daniela Bettio: University of Padova
Filippo Conca: University of Pavia
Nicoletta Concetta Surdo: Veneto Institute of Molecular Medicine
Giulietta Benedetto: Veneto Institute of Molecular Medicine
Deborah Musso: University of Pavia
Cristina Arrigoni: University of Pavia
Marco Lolicato: University of Pavia
Mauro Vismara: University of Pavia
Francesca Grisan: Veneto Institute of Molecular Medicine
Leonardo Salviati: University of Padova
Luciano Milanesi: National Research Council of Italy
Graziano Pesole: University of Bari “Aldo Moro”
Konstantinos Lefkimmiatis: University of Pavia

Nature Communications, 2023, vol. 14, issue 1, 1-16

Abstract: Abstract The second messenger cyclic AMP regulates many nuclear processes including transcription, pre-mRNA splicing and mitosis. While most functions are attributed to protein kinase A, accumulating evidence suggests that not all nuclear cyclic AMP-dependent effects are mediated by this kinase, implying that other effectors may be involved. Here we explore the nuclear roles of Exchange Protein Activated by cyclic AMP 1. We find that it enters the nucleus where forms reversible biomolecular condensates in response to cyclic AMP. This phenomenon depends on intrinsically disordered regions present at its amino-terminus and is independent of protein kinase A. Finally, we demonstrate that nuclear Exchange Protein Activated by cyclic AMP 1 condensates assemble at genomic loci on chromosome 6 in the proximity of Histone Locus Bodies and promote the transcription of a histone gene cluster. Collectively, our data reveal an unexpected mechanism through which cyclic AMP contributes to nuclear spatial compartmentalization and promotes the transcription of specific genes.

Date: 2023
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DOI: 10.1038/s41467-023-41088-x

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