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Article ; Online: Monitoring Transcription Factor Oligomerization in Single Living Cells by Number and Brightness Analysis.

Cammarota, Eugenia / Mazza, Davide

Methods in molecular biology (Clifton, N.J.)

2019 Volume 2038, Page(s) 223–237

Abstract: One key step in the activation of inducible transcription factors is their homooligomerization, which can be measured in individual living cells by a fluorescence microscopy technique called Number and Brightness analysis (N&B). In this chapter we ... ...

Abstract	One key step in the activation of inducible transcription factors is their homooligomerization, which can be measured in individual living cells by a fluorescence microscopy technique called Number and Brightness analysis (N&B). In this chapter we describe how to acquire and analyze confocal microscopy time-series to provide information about transcription factor oligomerization in living cells using this technique.
MeSH term(s)	Animals ; Cell Line ; Gene Expression Regulation ; Humans ; Microscopy, Confocal ; Molecular Imaging/methods ; Protein Multimerization ; Single-Cell Analysis/methods ; Time Factors ; Transcription Factors/genetics ; Transcription Factors/metabolism ; Transcriptional Activation
Chemical Substances	Transcription Factors
Language	English
Publishing date	2019-08-12
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-4939-9674-2_15
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Article ; Online: Transcription factor binding kinetics and transcriptional bursting: What do we really know?

Mazzocca, Matteo / Colombo, Emanuele / Callegari, Andrea / Mazza, Davide

Current opinion in structural biology

2021 Volume 71, Page(s) 239–248

Abstract: In eukaryotes, transcription is a discontinuous process with mRNA being generated in bursts, after the binding of transcription factors (TFs) to regulatory elements on the genome. Live-cell single-molecule microscopy has highlighted that transcriptional ... ...

Abstract	In eukaryotes, transcription is a discontinuous process with mRNA being generated in bursts, after the binding of transcription factors (TFs) to regulatory elements on the genome. Live-cell single-molecule microscopy has highlighted that transcriptional bursting can be controlled by tuning TF/DNA binding kinetics. Yet the timescales of these two processes seem disconnected with TF/DNA interactions typically lasting orders of magnitude shorter than transcriptional bursts. To test models that could reconcile these discrepancies, reliable measurements of TF binding kinetics are needed, also accounting for the current limitations in performing these single-molecule measurements at specific regulatory elements. Here, we review the recent studies linking TF binding kinetics to transcriptional bursting and outline some current and future challenges that need to be addressed to provide a microscopic description of transcriptional regulation kinetics.
MeSH term(s)	Binding Sites ; Gene Expression Regulation ; Kinetics ; Protein Binding ; Transcription Factors/genetics ; Transcription Factors/metabolism ; Transcription, Genetic
Chemical Substances	Transcription Factors
Language	English
Publishing date	2021-09-01
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	1068353-7
ISSN	1879-033X ; 0959-440X
ISSN (online)	1879-033X
ISSN	0959-440X
DOI	10.1016/j.sbi.2021.08.002
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Zs.A 3206: Show issues

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Article ; Online: The needle and the haystack: single molecule tracking to probe the transcription factor search in eukaryotes.

Mazzocca, Matteo / Fillot, Tom / Loffreda, Alessia / Gnani, Daniela / Mazza, Davide

Biochemical Society transactions

2021 Volume 49, Issue 3, Page(s) 1121–1132

Abstract: Transcription factors (TFs) regulate transcription of their target genes by identifying and binding to regulatory regions of the genome among billions of potential non-specific decoy sites, a task that is often presented as a 'needle in the haystack' ... ...

Abstract	Transcription factors (TFs) regulate transcription of their target genes by identifying and binding to regulatory regions of the genome among billions of potential non-specific decoy sites, a task that is often presented as a 'needle in the haystack' challenge. The TF search process is now well understood in bacteria, but its characterization in eukaryotes needs to account for the complex organization of the nuclear environment. Here we review how live-cell single molecule tracking is starting to shed light on the TF search mechanism in the eukaryotic cell and we outline the future challenges to tackle in order to understand how nuclear organization modulates the TF search process in physiological and pathological conditions.
MeSH term(s)	Animals ; Binding Sites/genetics ; Cell Nucleus/genetics ; Cell Nucleus/metabolism ; Eukaryota/genetics ; Eukaryota/metabolism ; Gene Expression Regulation ; Genome/genetics ; Humans ; Protein Binding ; Regulatory Sequences, Nucleic Acid/genetics ; Single Molecule Imaging/methods ; Transcription Factors/metabolism
Chemical Substances	Transcription Factors
Language	English
Publishing date	2021-05-18
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	184237-7
ISSN	1470-8752 ; 0300-5127
ISSN (online)	1470-8752
ISSN	0300-5127
DOI	10.1042/BST20200709
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Zs.A 944: Show issues

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Article ; Online: PML restrains p53 activity and cellular senescence in clear cell renal cell carcinoma.

Simoni, Matilde / Menegazzi, Chiara / Fracassi, Cristina / Biffi, Claudia C / Genova, Francesca / Tenace, Nazario Pio / Lucianò, Roberta / Raimondi, Andrea / Tacchetti, Carlo / Brugarolas, James / Mazza, Davide / Bernardi, Rosa

EMBO molecular medicine

2024

Abstract: Clear-cell renal cell carcinoma (ccRCC), the major subtype of RCC, is frequently diagnosed at late/metastatic stage with 13% 5-year disease-free survival. Functional inactivation of the wild-type p53 protein is implicated in ccRCC therapy resistance, but ...

Abstract	Clear-cell renal cell carcinoma (ccRCC), the major subtype of RCC, is frequently diagnosed at late/metastatic stage with 13% 5-year disease-free survival. Functional inactivation of the wild-type p53 protein is implicated in ccRCC therapy resistance, but the detailed mechanisms of p53 malfunction are still poorly characterized. Thus, a better understanding of the mechanisms of disease progression and therapy resistance is required. Here, we report a novel ccRCC dependence on the promyelocytic leukemia (PML) protein. We show that PML is overexpressed in ccRCC and that PML depletion inhibits cell proliferation and relieves pathologic features of anaplastic disease in vivo. Mechanistically, PML loss unleashed p53-dependent cellular senescence thus depicting a novel regulatory axis to limit p53 activity and senescence in ccRCC. Treatment with the FDA-approved PML inhibitor arsenic trioxide induced PML degradation and p53 accumulation and inhibited ccRCC expansion in vitro and in vivo. Therefore, by defining non-oncogene addiction to the PML gene, our work uncovers a novel ccRCC vulnerability and lays the foundation for repurposing an available pharmacological intervention to restore p53 function and chemosensitivity.
Language	English
Publishing date	2024-05-10
Publishing country	England
Document type	Journal Article
ZDB-ID	2467145-9
ISSN	1757-4684 ; 1757-4676
ISSN (online)	1757-4684
ISSN	1757-4676
DOI	10.1038/s44321-024-00077-3
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Zs.A 6784: Show issues

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Article ; Online: Combinatorial allosteric modulation of agonist response in a self-interacting G-protein coupled receptor.

Patrone, Marco / Cammarota, Eugenia / Berno, Valeria / Tornaghi, Paola / Mazza, Davide / Degano, Massimo

Communications biology

2020 Volume 3, Issue 1, Page(s) 27

Abstract: The structural plasticity of G-protein coupled receptors (GPCRs) enables the long-range transmission of conformational changes induced by specific orthosteric site ligands and other pleiotropic factors. Here, we demonstrate that the ligand binding cavity ...

Abstract	The structural plasticity of G-protein coupled receptors (GPCRs) enables the long-range transmission of conformational changes induced by specific orthosteric site ligands and other pleiotropic factors. Here, we demonstrate that the ligand binding cavity in the sphingosine 1-phosphate receptor S1PR1, a class A GPCR, is in allosteric communication with both the β-arrestin-binding C-terminal tail, and a receptor surface involved in oligomerization. We show that S1PR1 oligomers are required for full response to different agonists and ligand-specific association with arrestins, dictating the downstream signalling kinetics. We reveal that the active form of the immunomodulatory drug fingolimod, FTY720-P, selectively harnesses both these intramolecular networks to efficiently recruit β-arrestins in a stable interaction with the receptor, promoting deep S1PR1 internalization and simultaneously abrogating ERK1/2 phosphorylation. Our results define a molecular basis for the efficacy of fingolimod for people with multiple sclerosis, and attest that GPCR signalling can be further fine-tuned by the oligomeric state.
MeSH term(s)	Allosteric Regulation ; Cell Line ; Cell Membrane/metabolism ; Fingolimod Hydrochloride/chemistry ; Fingolimod Hydrochloride/pharmacology ; Humans ; Kinetics ; Models, Molecular ; Phosphorylation ; Proprotein Convertases/chemistry ; Proprotein Convertases/metabolism ; Protein Binding ; Protein Conformation ; Protein Multimerization ; Protein Transport ; Receptors, G-Protein-Coupled/agonists ; Receptors, G-Protein-Coupled/chemistry ; Receptors, G-Protein-Coupled/metabolism ; Serine Endopeptidases/chemistry ; Serine Endopeptidases/metabolism ; Signal Transduction ; Structure-Activity Relationship ; beta-Arrestins/chemistry ; beta-Arrestins/metabolism
Chemical Substances	Receptors, G-Protein-Coupled ; beta-Arrestins ; Proprotein Convertases (EC 3.4.21.-) ; Serine Endopeptidases (EC 3.4.21.-) ; membrane-bound transcription factor peptidase, site 1 (EC 3.4.21.112) ; Fingolimod Hydrochloride (G926EC510T)
Language	English
Publishing date	2020-01-15
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	2399-3642
ISSN (online)	2399-3642
DOI	10.1038/s42003-020-0752-4
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Article ; Online: PML modulates epigenetic composition of chromatin to regulate expression of pro-metastatic genes in triple-negative breast cancer.

Fracassi, Cristina / Ugge', Martina / Abdelhalim, Mohamed / Zapparoli, Ettore / Simoni, Matilde / Magliulo, Daniela / Mazza, Davide / Lazarevic, Dejan / Morelli, Marco J / Collas, Philippe / Bernardi, Rosa

Nucleic acids research

2023 Volume 51, Issue 20, Page(s) 11024–11039

Abstract: The promyelocytic leukemia (PML) protein organizes nuclear aggregates known as PML nuclear bodies (PML-NBs), where many transcription factors localize to be regulated. In addition, associations of PML and PML-NBs with chromatin are described in various ... ...

Abstract	The promyelocytic leukemia (PML) protein organizes nuclear aggregates known as PML nuclear bodies (PML-NBs), where many transcription factors localize to be regulated. In addition, associations of PML and PML-NBs with chromatin are described in various cell types, further implicating PML in transcriptional regulation. However, a complete understanding of the functional consequences of PML association to DNA in cellular contexts where it promotes relevant phenotypes is still lacking. We examined PML chromatin association in triple-negative breast cancer (TNBC) cell lines, where it exerts important oncogenic functions. We find that PML associates discontinuously with large heterochromatic PML-associated domains (PADs) that contain discrete gene-rich euchromatic sub-domains locally depleted of PML. PML promotes heterochromatic organization in PADs and expression of pro-metastatic genes embedded in these sub-domains. Importantly, this occurs outside PML-NBs, suggesting that nucleoplasmic PML exerts a relevant gene regulatory function. We also find that PML plays indirect regulatory roles in TNBC cells by promoting the expression of pro-metastatic genes outside PADs. Our findings suggest that PML is an important transcriptional regulator of pro-oncogenic metagenes in TNBC cells, via transcriptional regulation and epigenetic organization of heterochromatin domains that embed regions of local transcriptional activity.
MeSH term(s)	Humans ; Cell Nucleus/metabolism ; Chromatin/genetics ; Chromatin/metabolism ; Epigenesis, Genetic ; Nuclear Proteins/genetics ; Nuclear Proteins/metabolism ; Promyelocytic Leukemia Protein/genetics ; Promyelocytic Leukemia Protein/metabolism ; Transcription Factors/genetics ; Transcription Factors/metabolism ; Triple Negative Breast Neoplasms/genetics ; Triple Negative Breast Neoplasms/metabolism ; Cell Line, Tumor
Chemical Substances	Chromatin ; Nuclear Proteins ; Promyelocytic Leukemia Protein ; Transcription Factors ; PML protein, human (143220-95-5)
Language	English
Publishing date	2023-10-11
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	186809-3
ISSN	1362-4962 ; 1362-4954 ; 0301-5610 ; 0305-1048
ISSN (online)	1362-4962 ; 1362-4954
ISSN	0301-5610 ; 0305-1048
DOI	10.1093/nar/gkad819
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Zs.A 1067: Show issues

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Article ; Online: Chromatin organization drives the search mechanism of nuclear factors.

Mazzocca, Matteo / Loffreda, Alessia / Colombo, Emanuele / Fillot, Tom / Gnani, Daniela / Falletta, Paola / Monteleone, Emanuele / Capozi, Serena / Bertrand, Edouard / Legube, Gaelle / Lavagnino, Zeno / Tacchetti, Carlo / Mazza, Davide

Nature communications

2023 Volume 14, Issue 1, Page(s) 6433

Abstract: Nuclear factors rapidly scan the genome for their targets, but the role of nuclear organization in such search is uncharted. Here we analyzed how multiple factors explore chromatin, combining live-cell single-molecule tracking with multifocal structured ... ...

Abstract	Nuclear factors rapidly scan the genome for their targets, but the role of nuclear organization in such search is uncharted. Here we analyzed how multiple factors explore chromatin, combining live-cell single-molecule tracking with multifocal structured illumination of DNA density. We find that factors displaying higher bound fractions sample DNA-dense regions more exhaustively. Focusing on the tumor-suppressor p53, we demonstrate that it searches for targets by alternating between rapid diffusion in the interchromatin compartment and compact sampling of chromatin dense regions. Efficient targeting requires balanced interactions with chromatin: fusing p53 with an exogenous intrinsically disordered region potentiates p53-mediated target gene activation at low concentrations, but leads to condensates at higher levels, derailing its search and downregulating transcription. Our findings highlight the role of disordered regions on factors search and showcase a powerful method to generate traffic maps of the eukaryotic nucleus to dissect how its organization guides nuclear factors action.
MeSH term(s)	Tumor Suppressor Protein p53/genetics ; Tumor Suppressor Protein p53/metabolism ; Chromatin/genetics ; Chromatin/metabolism ; DNA/metabolism ; Chromosomes/metabolism ; Transcriptional Activation ; Cell Nucleus/genetics ; Cell Nucleus/metabolism
Chemical Substances	Tumor Suppressor Protein p53 ; Chromatin ; DNA (9007-49-2)
Language	English
Publishing date	2023-10-13
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-023-42133-5
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Article ; Online: Scc2/Nipbl hops between chromosomal cohesin rings after loading.

Rhodes, James / Mazza, Davide / Nasmyth, Kim / Uphoff, Stephan

eLife

2017 Volume 6

Abstract: The cohesin complex mediates DNA-DNA interactions both between (sister chromatid cohesion) and within chromosomes (DNA looping). It has been suggested that intra-chromosome loops are generated by extrusion of DNAs through the lumen of cohesin's ring. ... ...

Abstract	The cohesin complex mediates DNA-DNA interactions both between (sister chromatid cohesion) and within chromosomes (DNA looping). It has been suggested that intra-chromosome loops are generated by extrusion of DNAs through the lumen of cohesin's ring. Scc2 (Nipbl) stimulates cohesin's ABC-like ATPase and is essential for loading cohesin onto chromosomes. However, it is possible that the stimulation of cohesin's ATPase by Scc2 also has a post-loading function, for example driving loop extrusion. Using fluorescence recovery after photobleaching (FRAP) and single-molecule tracking in human cells, we show that Scc2 binds dynamically to chromatin, principally through an association with cohesin. Scc2's movement within chromatin is consistent with a 'stop-and-go' or 'hopping' motion. We suggest that a low diffusion coefficient, a low stoichiometry relative to cohesin, and a high affinity for chromosomal cohesin enables Scc2 to move rapidly from one chromosomal cohesin complex to another, performing a function distinct from loading.
MeSH term(s)	Cell Cycle Proteins/metabolism ; Cell Line ; Chromatin/metabolism ; Chromosomal Proteins, Non-Histone/metabolism ; Humans ; Microscopy, Confocal ; Optical Imaging ; Proteins/metabolism ; Single Molecule Imaging ; Cohesins
Chemical Substances	Cell Cycle Proteins ; Chromatin ; Chromosomal Proteins, Non-Histone ; NIPBL protein, human ; Proteins
Language	English
Publishing date	2017-09-15
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.30000
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Article ; Online: HNF4α, SP1 and c-myc are master regulators of CNS autoimmunity.

Colombo, Emanuela / Di Dario, Marco / Menon, Ramesh / Valente, Maria Maddalena / Bassani, Claudia / Sarno, Nicole / Mazza, Davide / Montini, Federico / Moiola, Lucia / Comi, Giancarlo / Martinelli, Vittorio / Farina, Cinthia

Journal of autoimmunity

2023 Volume 138, Page(s) 103053

Abstract: Hepatocyte nuclear factor 4 α (HNF4α), a transcription factor (TF) essential for embryonic development, has been recently shown to regulate the expression of inflammatory genes. To characterize HNF4a function in immunity, we measured the effect of HNF4α ... ...

Abstract	Hepatocyte nuclear factor 4 α (HNF4α), a transcription factor (TF) essential for embryonic development, has been recently shown to regulate the expression of inflammatory genes. To characterize HNF4a function in immunity, we measured the effect of HNF4α antagonists on immune cell responses in vitro and in vivo. HNF4α blockade reduced immune activation in vitro and disease severity in the experimental model of multiple sclerosis (MS). Network biology studies of human immune transcriptomes unraveled HNF4α together with SP1 and c-myc as master TF regulating differential expression at all MS stages. TF expression was boosted by immune cell activation, regulated by environmental MS risk factors and higher in MS immune cells compared to controls. Administration of compounds targeting TF expression or function demonstrated non-synergic, interdependent transcriptional control of CNS autoimmunity in vitro and in vivo. Collectively, we identified a coregulatory transcriptional network sustaining neuroinflammation and representing an attractive therapeutic target for MS and other inflammatory disorders.
MeSH term(s)	Humans ; Autoimmunity/genetics ; Gene Expression Regulation ; Gene Regulatory Networks ; Hepatocyte Nuclear Factor 4/genetics ; Hepatocyte Nuclear Factor 4/metabolism ; Multiple Sclerosis/genetics ; Multiple Sclerosis/immunology ; Transcriptome ; Genes, myc
Chemical Substances	Hepatocyte Nuclear Factor 4 ; SP1 protein, human ; HNF4A protein, human
Language	English
Publishing date	2023-05-24
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	639452-8
ISSN	1095-9157 ; 0896-8411
ISSN (online)	1095-9157
ISSN	0896-8411
DOI	10.1016/j.jaut.2023.103053
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Zs.A 2368: Show issues

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Article ; Online: Measuring Mobility in Chromatin by Intensity-Sorted FCS.

Di Bona, Melody / Mancini, Michael A / Mazza, Davide / Vicidomini, Giuseppe / Diaspro, Alberto / Lanzanò, Luca

Biophysical journal

2019 Volume 116, Issue 6, Page(s) 987–999

Abstract: The architectural organization of chromatin can play an important role in genome regulation by affecting the mobility of molecules within its surroundings via binding interactions and molecular crowding. The diffusion of molecules at specific locations ... ...

Abstract	The architectural organization of chromatin can play an important role in genome regulation by affecting the mobility of molecules within its surroundings via binding interactions and molecular crowding. The diffusion of molecules at specific locations in the nucleus can be studied by fluorescence correlation spectroscopy (FCS), a well-established technique based on the analysis of fluorescence intensity fluctuations detected in a confocal observation volume. However, detecting subtle variations of mobility between different chromatin regions remains challenging with currently available FCS methods. Here, we introduce a method that samples multiple positions by slowly scanning the FCS observation volume across the nucleus. Analyzing the data in short time segments, we preserve the high temporal resolution of single-point FCS while probing different nuclear regions in the same cell. Using the intensity level of the probe (or a DNA marker) as a reference, we efficiently sort the FCS segments into different populations and obtain average correlation functions that are associated to different chromatin regions. This sorting and averaging strategy renders the method statistically robust while preserving the observation of intranuclear variations of mobility. Using this approach, we quantified diffusion of monomeric GFP in high versus low chromatin density regions. We found that GFP mobility was reduced in heterochromatin, especially within perinucleolar heterochromatin. Moreover, we found that modulation of chromatin compaction by ATP depletion, or treatment with solutions of different osmolarity, differentially affected the ratio of diffusion in both regions. Then, we used the approach to probe the mobility of estrogen receptor-α in the vicinity of an integrated multicopy prolactin gene array. Finally, we discussed the coupling of this method with stimulated emission depletion FCS for performing FCS at subdiffraction spatial scales.
MeSH term(s)	Chromatin/metabolism ; Diffusion ; Green Fluorescent Proteins/metabolism ; HeLa Cells ; Humans ; Movement ; Spectrometry, Fluorescence/methods ; Transcription Factors/metabolism
Chemical Substances	Chromatin ; Transcription Factors ; Green Fluorescent Proteins (147336-22-9)
Language	English
Publishing date	2019-02-14
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	218078-9
ISSN	1542-0086 ; 0006-3495
ISSN (online)	1542-0086
ISSN	0006-3495
DOI	10.1016/j.bpj.2019.02.003
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