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Article ; Online: An Emerging Role for Type I Interferons as Critical Regulators of Blood Coagulation.

Ryan, Tristram A J / O'Neill, Luke A J

2023 Volume 12, Issue 5

Abstract: Type I interferons (IFNs) are central mediators of anti-viral and anti-bacterial host defence. Detection of microbes by innate immune cells via pattern recognition receptors (PRRs), including Toll-like receptors (TLRs) and cGAS-STING, induces the ... ...

Abstract	Type I interferons (IFNs) are central mediators of anti-viral and anti-bacterial host defence. Detection of microbes by innate immune cells via pattern recognition receptors (PRRs), including Toll-like receptors (TLRs) and cGAS-STING, induces the expression of type I IFN-stimulated genes. Primarily comprising the cytokines IFN-α and IFN-β, type I IFNs act via the type I IFN receptor in an autocrine or exocrine manner to orchestrate rapid and diverse innate immune responses. Growing evidence pinpoints type I IFN signalling as a fulcrum that not only induces blood coagulation as a core feature of the inflammatory response but is also activated by components of the coagulation cascade. In this review, we describe in detail recent studies identifying the type I IFN pathway as a modulator of vascular function and thrombosis. In addition, we profile discoveries showing that thrombin signalling via protease-activated receptors (PARs), which can synergize with TLRs, regulates the host response to infection via induction of type I IFN signalling. Thus, type I IFNs can have both protective (via maintenance of haemostasis) and pathological (facilitating thrombosis) effects on inflammation and coagulation signalling. These can manifest as an increased risk of thrombotic complications in infection and in type I interferonopathies such as systemic lupus erythematosus (SLE) and STING-associated vasculopathy with onset in infancy (SAVI). We also consider the effects on coagulation of recombinant type I IFN therapies in the clinic and discuss pharmacological regulation of type I IFN signalling as a potential mechanism by which aberrant coagulation and thrombosis may be treated therapeutically.
MeSH term(s)	Antiviral Agents ; Blood Coagulation ; Cytokines/metabolism ; Immunity, Innate ; Interferon Type I/metabolism ; Humans
Chemical Substances	Antiviral Agents ; Cytokines ; Interferon Type I
Language	English
Publishing date	2023-02-28
Publishing country	Switzerland
Document type	Journal Article ; Review ; Research Support, Non-U.S. Gov't
ZDB-ID	2661518-6
ISSN	2073-4409 ; 2073-4409
ISSN (online)	2073-4409
ISSN	2073-4409
DOI	10.3390/cells12050778
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Article ; Online: An Emerging Role for Type I Interferons as Critical Regulators of Blood Coagulation

Tristram A. J. Ryan / Luke A. J. O’Neill

Cells, Vol 12, Iss 778, p

2023 Volume 778

Abstract	Type I interferons (IFNs) are central mediators of anti-viral and anti-bacterial host defence. Detection of microbes by innate immune cells via pattern recognition receptors (PRRs), including Toll-like receptors (TLRs) and cGAS-STING, induces the expression of type I IFN-stimulated genes. Primarily comprising the cytokines IFN-α and IFN-β, type I IFNs act via the type I IFN receptor in an autocrine or exocrine manner to orchestrate rapid and diverse innate immune responses. Growing evidence pinpoints type I IFN signalling as a fulcrum that not only induces blood coagulation as a core feature of the inflammatory response but is also activated by components of the coagulation cascade. In this review, we describe in detail recent studies identifying the type I IFN pathway as a modulator of vascular function and thrombosis. In addition, we profile discoveries showing that thrombin signalling via protease-activated receptors (PARs), which can synergize with TLRs, regulates the host response to infection via induction of type I IFN signalling. Thus, type I IFNs can have both protective (via maintenance of haemostasis) and pathological (facilitating thrombosis) effects on inflammation and coagulation signalling. These can manifest as an increased risk of thrombotic complications in infection and in type I interferonopathies such as systemic lupus erythematosus (SLE) and STING-associated vasculopathy with onset in infancy (SAVI). We also consider the effects on coagulation of recombinant type I IFN therapies in the clinic and discuss pharmacological regulation of type I IFN signalling as a potential mechanism by which aberrant coagulation and thrombosis may be treated therapeutically.
Keywords	type I interferons ; blood coagulation ; IFN-α ; IFN-β ; thrombin ; PARs ; Biology (General) ; QH301-705.5
Subject code	570
Language	English
Publishing date	2023-02-01T00:00:00Z
Publisher	MDPI AG
Document type	Article ; Online
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Article ; Online: Innate immune signaling and immunothrombosis: New insights and therapeutic opportunities.

Ryan, Tristram A J / O'Neill, Luke A J

European journal of immunology

2022 Volume 52, Issue 7, Page(s) 1024–1034

Abstract: Activation of the coagulation cascade is a critical, evolutionarily conserved mechanism that maintains hemostasis by rapidly forming blood clots in response to blood-borne infections and damaged blood vessels. Coagulation is a key component of innate ... ...

Abstract	Activation of the coagulation cascade is a critical, evolutionarily conserved mechanism that maintains hemostasis by rapidly forming blood clots in response to blood-borne infections and damaged blood vessels. Coagulation is a key component of innate immunity since it prevents bacterial dissemination and can provoke inflammation. The term immunothrombosis describes the process by which the innate immune response drives aberrant coagulation, which can result in a lethal condition termed disseminated intravascular coagulation, often seen in sepsis. In this review, we describe the recently uncovered molecular mechanisms underlying inflammasome- and STING-driven immunothrombosis induced by bacterial and viral infections, culminating in tissue factor (TF) activation and release. Current anticoagulant therapeutics, while effective, are associated with a life-threatening bleeding risk, requiring the urgent development of new treatments. Targeting immunothrombosis may provide a safer option. Thus, we highlight preclinical tools which target TF and/or block canonical (NLRP3) or noncanonical (caspase-11) inflammasome activation as well as STING-driven TF release and discuss clinically approved drugs which block key immunothrombotic processes and, therefore, may be redeployed as safer anticoagulants.
MeSH term(s)	Blood Coagulation ; Hemostasis ; Humans ; Immunity, Innate ; Inflammasomes ; Thromboinflammation
Chemical Substances	Inflammasomes
Language	English
Publishing date	2022-05-24
Publishing country	Germany
Document type	Journal Article ; Review ; Research Support, Non-U.S. Gov't
ZDB-ID	120108-6
ISSN	1521-4141 ; 0014-2980
ISSN (online)	1521-4141
ISSN	0014-2980
DOI	10.1002/eji.202149410
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Article ; Online: Immunothrombosis and the molecular control of tissue factor by pyroptosis: prospects for new anticoagulants.

Ryan, Tristram A J / Preston, Roger J S / O'Neill, Luke A J

The Biochemical journal

2022 Volume 479, Issue 6, Page(s) 731–750

Abstract: The interplay between innate immunity and coagulation after infection or injury, termed immunothrombosis, is the primary cause of disseminated intravascular coagulation (DIC), a condition that occurs in sepsis. Thrombosis associated with DIC is the ... ...

Abstract	The interplay between innate immunity and coagulation after infection or injury, termed immunothrombosis, is the primary cause of disseminated intravascular coagulation (DIC), a condition that occurs in sepsis. Thrombosis associated with DIC is the leading cause of death worldwide. Interest in immunothrombosis has grown because of COVID-19, the respiratory disease caused by SARS-CoV-2, which has been termed a syndrome of dysregulated immunothrombosis. As the relatively new field of immunothrombosis expands at a rapid pace, the focus of academic and pharmacological research has shifted from generating treatments targeted at the traditional 'waterfall' model of coagulation to therapies better directed towards immune components that drive coagulopathies. Immunothrombosis can be initiated in macrophages by cleavage of the non-canonical inflammasome which contains caspase-11. This leads to release of tissue factor (TF), a membrane glycoprotein receptor that forms a high-affinity complex with coagulation factor VII/VIIa to proteolytically activate factors IX to IXa and X to Xa, generating thrombin and leading to fibrin formation and platelet activation. The mechanism involves the post-translational activation of TF, termed decryption, and release of decrypted TF via caspase-11-mediated pyroptosis. During aberrant immunothrombosis, decryption of TF leads to thromboinflammation, sepsis, and DIC. Therefore, developing therapies to target pyroptosis have emerged as an attractive concept to counteract dysregulated immunothrombosis. In this review, we detail the three mechanisms of TF control: concurrent induction of TF, caspase-11, and NLRP3 (signal 1); TF decryption, which increases its procoagulant activity (signal 2); and accelerated release of TF into the intravascular space via pyroptosis (signal 3). In this way, decryption of TF is analogous to the two signals of NLRP3 inflammasome activation, whereby induction of pro-IL-1β and NLRP3 (signal 1) is followed by activation of NLRP3 (signal 2). We describe in detail TF decryption, which involves pathogen-induced alterations in the composition of the plasma membrane and modification of key cysteines on TF, particularly at the location of the critical, allosterically regulated disulfide bond of TF in its 219-residue extracellular domain. In addition, we speculate towards the importance of identifying new therapeutics to block immunothrombotic triggering of TF, which can involve inhibition of pyroptosis to limit TF release, or the direct targeting of TF decryption using cysteine-modifying therapeutics.
MeSH term(s)	Anticoagulants/pharmacology ; Anticoagulants/therapeutic use ; COVID-19/drug therapy ; Humans ; Inflammation/complications ; Pyroptosis ; SARS-CoV-2 ; Thromboinflammation ; Thromboplastin/metabolism ; Thrombosis
Chemical Substances	Anticoagulants ; Thromboplastin (9035-58-9)
Language	English
Publishing date	2022-03-03
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2969-5
ISSN	1470-8728 ; 0006-2936 ; 0306-3275 ; 0264-6021
ISSN (online)	1470-8728
ISSN	0006-2936 ; 0306-3275 ; 0264-6021
DOI	10.1042/BCJ20210522
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Article ; Online: Macrophage fumarate hydratase restrains mtRNA-mediated interferon production.

Hooftman, Alexander / Peace, Christian G / Ryan, Dylan G / Day, Emily A / Yang, Ming / McGettrick, Anne F / Yin, Maureen / Montano, Erica N / Huo, Lihong / Toller-Kawahisa, Juliana E / Zecchini, Vincent / Ryan, Tristram A J / Bolado-Carrancio, Alfonso / Casey, Alva M / Prag, Hiran A / Costa, Ana S H / De Los Santos, Gabriela / Ishimori, Mariko / Wallace, Daniel J /

Venuturupalli, Swamy / Nikitopoulou, Efterpi / Frizzell, Norma / Johansson, Cecilia / Von Kriegsheim, Alexander / Murphy, Michael P / Jefferies, Caroline / Frezza, Christian / O'Neill, Luke A J

Nature

2023 Volume 615, Issue 7952, Page(s) 490–498

Abstract: Metabolic rewiring underlies the effector functions of ... ...

Abstract	Metabolic rewiring underlies the effector functions of macrophages
MeSH term(s)	Humans ; Argininosuccinate Synthase/metabolism ; Argininosuccinic Acid/metabolism ; Aspartic Acid/metabolism ; Cell Respiration ; Cytosol/metabolism ; Fumarate Hydratase/antagonists & inhibitors ; Fumarate Hydratase/genetics ; Fumarate Hydratase/metabolism ; Fumarates/metabolism ; Interferon-beta/biosynthesis ; Interferon-beta/immunology ; Lipopolysaccharides/pharmacology ; Lipopolysaccharides/metabolism ; Lupus Erythematosus, Systemic/enzymology ; Macrophages/enzymology ; Macrophages/immunology ; Macrophages/metabolism ; Membrane Potential, Mitochondrial ; Metabolomics ; Mitochondria/genetics ; Mitochondria/metabolism ; RNA, Mitochondrial/metabolism
Chemical Substances	Argininosuccinate Synthase (EC 6.3.4.5) ; Argininosuccinic Acid (2387-71-5) ; Aspartic Acid (30KYC7MIAI) ; RIGI protein, human (EC 3.6.1.-) ; Fumarate Hydratase (EC 4.2.1.2) ; Fumarates ; IFIH1 protein, human (EC 3.6.1.-) ; Interferon-beta (77238-31-4) ; Lipopolysaccharides ; RNA, Mitochondrial ; TLR7 protein, human
Language	English
Publishing date	2023-03-08
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	120714-3
ISSN	1476-4687 ; 0028-0836
ISSN (online)	1476-4687
ISSN	0028-0836
DOI	10.1038/s41586-023-05720-6
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Zs.A 26: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (1.OG) ab Jg. 2022: Lesesaal (EG)
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Article ; Online: Publisher Correction: Dimethyl fumarate and 4-octyl itaconate are anticoagulants that suppress Tissue Factor in macrophages via inhibition of Type I Interferon.

Ryan, Tristram A J / Hooftman, Alexander / Rehill, Aisling M / Johansen, Matt D / O' Brien, Eóin C / Toller-Kawahisa, Juliana E / Wilk, Mieszko M / Day, Emily A / Weiss, Hauke J / Sarvari, Pourya / Vozza, Emilio G / Schramm, Fabian / Peace, Christian G / Zotta, Alessia / Miemczyk, Stefan / Nalkurthi, Christina / Hansbro, Nicole G / McManus, Gavin / O'Doherty, Laura /

Gargan, Siobhan / Long, Aideen / Dunne, Jean / Cheallaigh, Clíona Ní / Conlon, Niall / Carty, Michael / Fallon, Padraic G / Mills, Kingston H G / Creagh, Emma M / O' Donnell, James S / Hertzog, Paul J / Hansbro, Philip M / McLoughlin, Rachel M / Wygrecka, Małgorzata / Preston, Roger J S / Zasłona, Zbigniew / O'Neill, Luke A J

Nature communications

2023 Volume 14, Issue 1, Page(s) 4374

Language	English
Publishing date	2023-07-20
Publishing country	England
Document type	Published Erratum
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-023-40034-1
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Article ; Online: Correction to "Lung SPLUNC1 Peptide Derivatives in the Lipid Membrane Headgroup Kill Gram-Negative Planktonic and Biofilm Bacteria".

Jakkampudi, Tanvi / Lin, Qiao / Mitra, Saheli / Vijai, Aishwarya / Qin, Weiheng / Kang, Ann / Chen, Jespar / Ryan, Emma / Wang, Runxuan / Gong, Yuqi / Heinrich, Frank / Song, Junming / Di, Yuan-Pu Peter / Tristram-Nagle, Stephanie

Biomacromolecules

2024

Language	English
Publishing date	2024-04-19
Publishing country	United States
Document type	Published Erratum
ISSN	1526-4602
ISSN (online)	1526-4602
DOI	10.1021/acs.biomac.4c00501
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Dimethyl fumarate and 4-octyl itaconate are anticoagulants that suppress Tissue Factor in macrophages via inhibition of Type I Interferon.

Ryan, Tristram A J / Hooftman, Alexander / Rehill, Aisling M / Johansen, Matt D / Brien, Eóin C O' / Toller-Kawahisa, Juliana E / Wilk, Mieszko M / Day, Emily A / Weiss, Hauke J / Sarvari, Pourya / Vozza, Emilio G / Schramm, Fabian / Peace, Christian G / Zotta, Alessia / Miemczyk, Stefan / Nalkurthi, Christina / Hansbro, Nicole G / McManus, Gavin / O'Doherty, Laura /

Gargan, Siobhan / Long, Aideen / Dunne, Jean / Cheallaigh, Clíona Ní / Conlon, Niall / Carty, Michael / Fallon, Padraic G / Mills, Kingston H G / Creagh, Emma M / Donnell, James S O' / Hertzog, Paul J / Hansbro, Philip M / McLoughlin, Rachel M / Wygrecka, Małgorzata / Preston, Roger J S / Zasłona, Zbigniew / O'Neill, Luke A J

Nature communications

2023 Volume 14, Issue 1, Page(s) 3513

Abstract: Excessive inflammation-associated coagulation is a feature of infectious diseases, occurring in such conditions as bacterial sepsis and COVID-19. It can lead to disseminated intravascular coagulation, one of the leading causes of mortality worldwide. ... ...

Abstract	Excessive inflammation-associated coagulation is a feature of infectious diseases, occurring in such conditions as bacterial sepsis and COVID-19. It can lead to disseminated intravascular coagulation, one of the leading causes of mortality worldwide. Recently, type I interferon (IFN) signaling has been shown to be required for tissue factor (TF; gene name F3) release from macrophages, a critical initiator of coagulation, providing an important mechanistic link between innate immunity and coagulation. The mechanism of release involves type I IFN-induced caspase-11 which promotes macrophage pyroptosis. Here we find that F3 is a type I IFN-stimulated gene. Furthermore, F3 induction by lipopolysaccharide (LPS) is inhibited by the anti-inflammatory agents dimethyl fumarate (DMF) and 4-octyl itaconate (4-OI). Mechanistically, inhibition of F3 by DMF and 4-OI involves suppression of Ifnb1 expression. Additionally, they block type I IFN- and caspase-11-mediated macrophage pyroptosis, and subsequent TF release. Thereby, DMF and 4-OI inhibit TF-dependent thrombin generation. In vivo, DMF and 4-OI suppress TF-dependent thrombin generation, pulmonary thromboinflammation, and lethality induced by LPS, E. coli, and S. aureus, with 4-OI additionally attenuating inflammation-associated coagulation in a model of SARS-CoV-2 infection. Our results identify the clinically approved drug DMF and the pre-clinical tool compound 4-OI as anticoagulants that inhibit TF-mediated coagulopathy via inhibition of the macrophage type I IFN-TF axis.
MeSH term(s)	Humans ; Anticoagulants ; Thromboplastin ; Dimethyl Fumarate/pharmacology ; Dimethyl Fumarate/therapeutic use ; Escherichia coli ; Inflammation ; Lipopolysaccharides ; Staphylococcus aureus ; Thrombin ; COVID-19 ; SARS-CoV-2 ; Thrombosis ; Macrophages ; Caspases ; Interferon Type I
Chemical Substances	Anticoagulants ; 4-octyl itaconate ; Thromboplastin (9035-58-9) ; Dimethyl Fumarate (FO2303MNI2) ; Lipopolysaccharides ; Thrombin (EC 3.4.21.5) ; Caspases (EC 3.4.22.-) ; Interferon Type I
Language	English
Publishing date	2023-06-14
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/s41467-023-39174-1
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Article ; Online: Lung SPLUNC1 Peptide Derivatives in the Lipid Membrane Headgroup Kill Gram-Negative Planktonic and Biofilm Bacteria.

Biomacromolecules

2023 Volume 24, Issue 6, Page(s) 2804–2815

Abstract: SPLUNC1 (short palate lung and nasal epithelial clone 1) is a multifunctional host defense protein found in human respiratory tract with antimicrobial properties. In this work, we compare the biological activities of four SPLUNC1 antimicrobial peptide ( ... ...

Abstract	SPLUNC1 (short palate lung and nasal epithelial clone 1) is a multifunctional host defense protein found in human respiratory tract with antimicrobial properties. In this work, we compare the biological activities of four SPLUNC1 antimicrobial peptide (AMP) derivatives using paired clinical isolates of the Gram-negative (G(-)) bacteria
MeSH term(s)	Humans ; Bacteria ; Biofilms ; Gram-Negative Bacteria ; Lipids ; Lung ; Microbial Sensitivity Tests ; Peptides
Chemical Substances	Lipids ; Peptides ; BPIFA1 protein, human
Language	English
Publishing date	2023-05-24
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ISSN	1526-4602
ISSN (online)	1526-4602
DOI	10.1021/acs.biomac.3c00218
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Book ; Online: Ejecta Evolution Following a Planned Impact into an Asteroid

Kareta, Theodore / Thomas, Cristina / Li, Jian-Yang / Knight, Matthew M. / Moskovitz, Nicholas / Rozek, Agata / Bannister, Michele T. / Ieva, Simone / Snodgrass, Colin / Pravec, Petr / Ryan, Eileen V. / Ryan, William H. / Fahnestock, Eugene G. / Rivkin, Andrew S. / Chabot, Nancy / Fitzsimmons, Alan / Osip, David / Lister, Tim / Sarid, Gal /

Hirabayashi, Masatoshi / Farnham, Tony / Tancredi, Gonzalo / Michel, Patrick / Wainscoat, Richard / Weryk, Rob / Burrati, Bonnie / Pittichova, Jana / Ridden-Harper, Ryan / Tan, Nicole J. / Tristram, Paul / Brown, Tyler / Bonavita, Mariangela / Burgdorf, Martin / Khalouei, Elahe / Longa, Penelope / Rabus, Markus / Sajadian, Sedighe / Jorgensen, Uffe Graae / Dominik, Martin / Kikwaya, Jean-Baptiste / Epifani, Elena Mazzotta / Dotto, Elisabetta / Deshapriya, J. D. Prasanna / Hasselmann, Pedro H. / Dall'Ora, Massimo / Abe, Lyu / Guillot, Tristan / Mekarnia, Djamel / Agabi, Abdelkrim / Bendjoya, Philippe / Suarez, Olga / Triaud, Amaury / Gasparetto, Thomas / Gunther, Maximillian N. / Kueppers, Michael / Merin, Bruno / Chatelain, Joseph / Gomez, Edward / Usher, Helen / Stoddard-Jones, Cai / Bartnik, Matthew / Bellaver, Michael / Chetan, Brenna / Dugan, Emma / Fallon, Tori / Fedewa, Jeremy / Gerhard, Caitlyn / Jacobson, Seth A. / Painter, Shane / Peterson, David-Michael / Rodriguez, Joseph E. / Smith, Cody / Sokolovsky, Kirill V. / Sullivan, Hannah / Townley, Kate / Watson, Sarah / Webb, Levi / Trigo-Rodrıguez, Josep M. / Llenas, Josep M. / Perez-Garcıa, Ignacio / Castro-Tirado, A. J. / Vincent, Jean-Baptiste / Migliorini, Alessandra / Lazzarin, Monica / La Forgia, Fiorangela / Ferrari, Fabio / Polakis, Tom / Skiff, Brian

The First Five Weeks

2023

Abstract: The impact of the DART spacecraft into Dimorphos, moon of the asteroid Didymos, changed Dimorphos' orbit substantially, largely from the ejection of material. We present results from twelve Earth-based facilities involved in a world-wide campaign to ... ...

Abstract	The impact of the DART spacecraft into Dimorphos, moon of the asteroid Didymos, changed Dimorphos' orbit substantially, largely from the ejection of material. We present results from twelve Earth-based facilities involved in a world-wide campaign to monitor the brightness and morphology of the ejecta in the first 35 days after impact. After an initial brightening of ~1.4 magnitudes, we find consistent dimming rates of 0.11-0.12 magnitudes/day in the first week, and 0.08-0.09 magnitudes/day over the entire study period. The system returned to its pre-impact brightness 24.3-25.3 days after impact through the primary ejecta tail remained. The dimming paused briefly eight days after impact, near in time to the appearance of the second tail. This was likely due to a secondary release of material after re-impact of a boulder released in the initial impact, through movement of the primary ejecta through the aperture likely played a role. Comment: 16 pages, 5 Figures, accepted in the Astrophysical Journal Letters (ApJL) on October 16, 2023
Keywords	Astrophysics - Earth and Planetary Astrophysics
Subject code	306
Publishing date	2023-10-18
Publishing country	us
Document type	Book ; Online
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