Extracellular vesicle-packaged miRNA release after short-term exposure to particulate matter is associated with increased coagulation

Laura Pergoli, Laura Cantone, Chiara Favero, Laura Angelici, Simona Iodice, Eva Pinatel, Mirjam Hoxha, Laura Dioni, Marilena Letizia, Benedetta Albetti, Letizia Tarantini, Federica Rota, Pier Alberto Bertazzi, Amedea Silvia Tirelli, Vincenza Dolo, Andrea Cattaneo, Luisella Vigna, Cristina Battaglia, Michele Carugno, Matteo BonziniAngela Cecilia Pesatori, Valentina Bollati

Research output: Contribution to journalArticle

22 Citations (Scopus)

Abstract

Background: Exposure to particulate matter (PM) is associated with increased incidence of cardiovascular disease and increased coagulation, but the molecular mechanisms underlying these associations remain unknown. Obesity may increase susceptibility to the adverse effects of PM exposure, exacerbating the effects on cardiovascular diseases. Extracellular vesicles (EVs), which travel in body fluids and transfer microRNAs (miRNAs) between tissues, might play an important role in PM-induced cardiovascular risk. We sought to determine whether the levels of PM with an aerodynamic diameter≤10μm (PM10) are associated with changes in fibrinogen levels, EV release, and the miRNA content of EVs (EV-miRNAs), investigating 1630 overweight/obese subjects from the SPHERE Study. Results: Short-term exposure to PM10 (Day before blood drawing) was associated with an increased release of EVs quantified by nanoparticle tracking analysis, especially EVs derived from monocyte/macrophage components (CD14+) and platelets (CD61+) which were characterized by flow cytometry. We first profiled miRNAs of 883 subjects by the QuantStudio™ 12K Flex Real Time PCR System and the top 40 EV-miRNAs were validated through custom miRNA plates. Nine EV-miRNAs (let-7c-5p; miR-106a-5p; miR-143-3p; miR-185-5p; miR-218-5p; miR-331-3p; miR-642-5p; miR-652-3p; miR-99b-5p) were downregulated in response to PM10 exposure and exhibited putative roles in cardiovascular disease, as highlighted by integrated network analysis. PM10 exposure was significantly associated with elevated fibrinogen levels, and five of the nine downregulated EV-miRNAs were mediators between PM10 exposure and fibrinogen levels. Conclusions: Research on EVs opens a new path to the investigation of the adverse health effects of air pollution exposure. EVs have the potential to act both as markers of PM susceptibility and as potential molecular mechanism in the chain of events connecting PM exposure to increased coagulation, which is frequently linked to exposure and CVD development.

Original languageEnglish
Article number32
JournalParticle and Fibre Toxicology
Volume14
Issue number1
DOIs
Publication statusPublished - Aug 24 2017

Fingerprint

Particulate Matter
Coagulation
MicroRNAs
Fibrinogen
Cardiovascular Diseases
Flow cytometry
Extracellular Vesicles
Macrophages
Down-Regulation
Body fluids
Electric network analysis
Platelets
Real time systems
Air pollution
Chemical vapor deposition
Aerodynamics
Air Pollution
Computer Systems
Blood
Body Fluids

Keywords

  • Air pollution
  • Cardiovascular disease
  • Extracellular vesicles
  • Fibrinogen
  • MicroRNAs

ASJC Scopus subject areas

  • Toxicology
  • Health, Toxicology and Mutagenesis

Cite this

Extracellular vesicle-packaged miRNA release after short-term exposure to particulate matter is associated with increased coagulation. / Pergoli, Laura; Cantone, Laura; Favero, Chiara; Angelici, Laura; Iodice, Simona; Pinatel, Eva; Hoxha, Mirjam; Dioni, Laura; Letizia, Marilena; Albetti, Benedetta; Tarantini, Letizia; Rota, Federica; Bertazzi, Pier Alberto; Tirelli, Amedea Silvia; Dolo, Vincenza; Cattaneo, Andrea; Vigna, Luisella; Battaglia, Cristina; Carugno, Michele; Bonzini, Matteo; Pesatori, Angela Cecilia; Bollati, Valentina.

In: Particle and Fibre Toxicology, Vol. 14, No. 1, 32, 24.08.2017.

Research output: Contribution to journalArticle

Pergoli, L, Cantone, L, Favero, C, Angelici, L, Iodice, S, Pinatel, E, Hoxha, M, Dioni, L, Letizia, M, Albetti, B, Tarantini, L, Rota, F, Bertazzi, PA, Tirelli, AS, Dolo, V, Cattaneo, A, Vigna, L, Battaglia, C, Carugno, M, Bonzini, M, Pesatori, AC & Bollati, V 2017, 'Extracellular vesicle-packaged miRNA release after short-term exposure to particulate matter is associated with increased coagulation', Particle and Fibre Toxicology, vol. 14, no. 1, 32. https://doi.org/10.1186/s12989-017-0214-4
Pergoli, Laura ; Cantone, Laura ; Favero, Chiara ; Angelici, Laura ; Iodice, Simona ; Pinatel, Eva ; Hoxha, Mirjam ; Dioni, Laura ; Letizia, Marilena ; Albetti, Benedetta ; Tarantini, Letizia ; Rota, Federica ; Bertazzi, Pier Alberto ; Tirelli, Amedea Silvia ; Dolo, Vincenza ; Cattaneo, Andrea ; Vigna, Luisella ; Battaglia, Cristina ; Carugno, Michele ; Bonzini, Matteo ; Pesatori, Angela Cecilia ; Bollati, Valentina. / Extracellular vesicle-packaged miRNA release after short-term exposure to particulate matter is associated with increased coagulation. In: Particle and Fibre Toxicology. 2017 ; Vol. 14, No. 1.
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abstract = "Background: Exposure to particulate matter (PM) is associated with increased incidence of cardiovascular disease and increased coagulation, but the molecular mechanisms underlying these associations remain unknown. Obesity may increase susceptibility to the adverse effects of PM exposure, exacerbating the effects on cardiovascular diseases. Extracellular vesicles (EVs), which travel in body fluids and transfer microRNAs (miRNAs) between tissues, might play an important role in PM-induced cardiovascular risk. We sought to determine whether the levels of PM with an aerodynamic diameter≤10μm (PM10) are associated with changes in fibrinogen levels, EV release, and the miRNA content of EVs (EV-miRNAs), investigating 1630 overweight/obese subjects from the SPHERE Study. Results: Short-term exposure to PM10 (Day before blood drawing) was associated with an increased release of EVs quantified by nanoparticle tracking analysis, especially EVs derived from monocyte/macrophage components (CD14+) and platelets (CD61+) which were characterized by flow cytometry. We first profiled miRNAs of 883 subjects by the QuantStudio™ 12K Flex Real Time PCR System and the top 40 EV-miRNAs were validated through custom miRNA plates. Nine EV-miRNAs (let-7c-5p; miR-106a-5p; miR-143-3p; miR-185-5p; miR-218-5p; miR-331-3p; miR-642-5p; miR-652-3p; miR-99b-5p) were downregulated in response to PM10 exposure and exhibited putative roles in cardiovascular disease, as highlighted by integrated network analysis. PM10 exposure was significantly associated with elevated fibrinogen levels, and five of the nine downregulated EV-miRNAs were mediators between PM10 exposure and fibrinogen levels. Conclusions: Research on EVs opens a new path to the investigation of the adverse health effects of air pollution exposure. EVs have the potential to act both as markers of PM susceptibility and as potential molecular mechanism in the chain of events connecting PM exposure to increased coagulation, which is frequently linked to exposure and CVD development.",
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T1 - Extracellular vesicle-packaged miRNA release after short-term exposure to particulate matter is associated with increased coagulation

AU - Pergoli, Laura

AU - Cantone, Laura

AU - Favero, Chiara

AU - Angelici, Laura

AU - Iodice, Simona

AU - Pinatel, Eva

AU - Hoxha, Mirjam

AU - Dioni, Laura

AU - Letizia, Marilena

AU - Albetti, Benedetta

AU - Tarantini, Letizia

AU - Rota, Federica

AU - Bertazzi, Pier Alberto

AU - Tirelli, Amedea Silvia

AU - Dolo, Vincenza

AU - Cattaneo, Andrea

AU - Vigna, Luisella

AU - Battaglia, Cristina

AU - Carugno, Michele

AU - Bonzini, Matteo

AU - Pesatori, Angela Cecilia

AU - Bollati, Valentina

PY - 2017/8/24

Y1 - 2017/8/24

N2 - Background: Exposure to particulate matter (PM) is associated with increased incidence of cardiovascular disease and increased coagulation, but the molecular mechanisms underlying these associations remain unknown. Obesity may increase susceptibility to the adverse effects of PM exposure, exacerbating the effects on cardiovascular diseases. Extracellular vesicles (EVs), which travel in body fluids and transfer microRNAs (miRNAs) between tissues, might play an important role in PM-induced cardiovascular risk. We sought to determine whether the levels of PM with an aerodynamic diameter≤10μm (PM10) are associated with changes in fibrinogen levels, EV release, and the miRNA content of EVs (EV-miRNAs), investigating 1630 overweight/obese subjects from the SPHERE Study. Results: Short-term exposure to PM10 (Day before blood drawing) was associated with an increased release of EVs quantified by nanoparticle tracking analysis, especially EVs derived from monocyte/macrophage components (CD14+) and platelets (CD61+) which were characterized by flow cytometry. We first profiled miRNAs of 883 subjects by the QuantStudio™ 12K Flex Real Time PCR System and the top 40 EV-miRNAs were validated through custom miRNA plates. Nine EV-miRNAs (let-7c-5p; miR-106a-5p; miR-143-3p; miR-185-5p; miR-218-5p; miR-331-3p; miR-642-5p; miR-652-3p; miR-99b-5p) were downregulated in response to PM10 exposure and exhibited putative roles in cardiovascular disease, as highlighted by integrated network analysis. PM10 exposure was significantly associated with elevated fibrinogen levels, and five of the nine downregulated EV-miRNAs were mediators between PM10 exposure and fibrinogen levels. Conclusions: Research on EVs opens a new path to the investigation of the adverse health effects of air pollution exposure. EVs have the potential to act both as markers of PM susceptibility and as potential molecular mechanism in the chain of events connecting PM exposure to increased coagulation, which is frequently linked to exposure and CVD development.

AB - Background: Exposure to particulate matter (PM) is associated with increased incidence of cardiovascular disease and increased coagulation, but the molecular mechanisms underlying these associations remain unknown. Obesity may increase susceptibility to the adverse effects of PM exposure, exacerbating the effects on cardiovascular diseases. Extracellular vesicles (EVs), which travel in body fluids and transfer microRNAs (miRNAs) between tissues, might play an important role in PM-induced cardiovascular risk. We sought to determine whether the levels of PM with an aerodynamic diameter≤10μm (PM10) are associated with changes in fibrinogen levels, EV release, and the miRNA content of EVs (EV-miRNAs), investigating 1630 overweight/obese subjects from the SPHERE Study. Results: Short-term exposure to PM10 (Day before blood drawing) was associated with an increased release of EVs quantified by nanoparticle tracking analysis, especially EVs derived from monocyte/macrophage components (CD14+) and platelets (CD61+) which were characterized by flow cytometry. We first profiled miRNAs of 883 subjects by the QuantStudio™ 12K Flex Real Time PCR System and the top 40 EV-miRNAs were validated through custom miRNA plates. Nine EV-miRNAs (let-7c-5p; miR-106a-5p; miR-143-3p; miR-185-5p; miR-218-5p; miR-331-3p; miR-642-5p; miR-652-3p; miR-99b-5p) were downregulated in response to PM10 exposure and exhibited putative roles in cardiovascular disease, as highlighted by integrated network analysis. PM10 exposure was significantly associated with elevated fibrinogen levels, and five of the nine downregulated EV-miRNAs were mediators between PM10 exposure and fibrinogen levels. Conclusions: Research on EVs opens a new path to the investigation of the adverse health effects of air pollution exposure. EVs have the potential to act both as markers of PM susceptibility and as potential molecular mechanism in the chain of events connecting PM exposure to increased coagulation, which is frequently linked to exposure and CVD development.

KW - Air pollution

KW - Cardiovascular disease

KW - Extracellular vesicles

KW - Fibrinogen

KW - MicroRNAs

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