Senolytics in idiopathic pulmonary fibrosis: Results from a first-in-human, open-label, pilot study

Cellular senescence is a key mechanism that drives age-related diseases, but has yet to be targeted therapeutically in humans. Idiopathic pulmonary fibrosis (IPF) is a progressive, fatal cellular senescence-associated disease. Selectively ablating senescent cells using dasatinib plus quercetin (DQ)...

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Vydané v:EBioMedicine Ročník 40; s. 554 - 563
Hlavní autori: Justice, Jamie N., Nambiar, Anoop M., Tchkonia, Tamar, LeBrasseur, Nathan K., Pascual, Rodolfo, Hashmi, Shahrukh K., Prata, Larissa, Masternak, Michal M., Kritchevsky, Stephen B., Musi, Nicolas, Kirkland, James L.
Médium: Journal Article
Jazyk:English
Vydavateľské údaje: Netherlands Elsevier B.V 01.02.2019
Elsevier
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ISSN:2352-3964, 2352-3964
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Abstract Cellular senescence is a key mechanism that drives age-related diseases, but has yet to be targeted therapeutically in humans. Idiopathic pulmonary fibrosis (IPF) is a progressive, fatal cellular senescence-associated disease. Selectively ablating senescent cells using dasatinib plus quercetin (DQ) alleviates IPF-related dysfunction in bleomycin-administered mice. A two-center, open-label study of intermittent DQ (D:100 mg/day, Q:1250 mg/day, three-days/week over three-weeks) was conducted in participants with IPF (n = 14) to evaluate feasibility of implementing a senolytic intervention. The primary endpoints were retention rates and completion rates for planned clinical assessments. Secondary endpoints were safety and change in functional and reported health measures. Associations with the senescence-associated secretory phenotype (SASP) were explored. Fourteen patients with stable IPF were recruited. The retention rate was 100% with no DQ discontinuation; planned clinical assessments were complete in 13/14 participants. One serious adverse event was reported. Non-serious events were primarily mild-moderate, with respiratory symptoms (n = 16 total events), skin irritation/bruising (n = 14), and gastrointestinal discomfort (n = 12) being most frequent. Physical function evaluated as 6-min walk distance, 4-m gait speed, and chair-stands time was significantly and clinically-meaningfully improved (p < .05). Pulmonary function, clinical chemistries, frailty index (FI-LAB), and reported health were unchanged. DQ effects on circulat.ing SASP factors were inconclusive, but correlations were observed between change in function and change in SASP-related matrix-remodeling proteins, microRNAs, and pro-inflammatory cytokines (23/48 markers r ≥ 0.50). Our first-in-humans open-label pilot supports study feasibility and provides initial evidence that senolytics may alleviate physical dysfunction in IPF, warranting evaluation of DQ in larger randomized controlled trials for senescence-related diseases. ClinicalTrials.gov identifier: NCT02874989 (posted 2016–2018).
AbstractList Cellular senescence is a key mechanism that drives age-related diseases, but has yet to be targeted therapeutically in humans. Idiopathic pulmonary fibrosis (IPF) is a progressive, fatal cellular senescence-associated disease. Selectively ablating senescent cells using dasatinib plus quercetin (DQ) alleviates IPF-related dysfunction in bleomycin-administered mice.BACKGROUNDCellular senescence is a key mechanism that drives age-related diseases, but has yet to be targeted therapeutically in humans. Idiopathic pulmonary fibrosis (IPF) is a progressive, fatal cellular senescence-associated disease. Selectively ablating senescent cells using dasatinib plus quercetin (DQ) alleviates IPF-related dysfunction in bleomycin-administered mice.A two-center, open-label study of intermittent DQ (D:100 mg/day, Q:1250 mg/day, three-days/week over three-weeks) was conducted in participants with IPF (n = 14) to evaluate feasibility of implementing a senolytic intervention. The primary endpoints were retention rates and completion rates for planned clinical assessments. Secondary endpoints were safety and change in functional and reported health measures. Associations with the senescence-associated secretory phenotype (SASP) were explored.METHODSA two-center, open-label study of intermittent DQ (D:100 mg/day, Q:1250 mg/day, three-days/week over three-weeks) was conducted in participants with IPF (n = 14) to evaluate feasibility of implementing a senolytic intervention. The primary endpoints were retention rates and completion rates for planned clinical assessments. Secondary endpoints were safety and change in functional and reported health measures. Associations with the senescence-associated secretory phenotype (SASP) were explored.Fourteen patients with stable IPF were recruited. The retention rate was 100% with no DQ discontinuation; planned clinical assessments were complete in 13/14 participants. One serious adverse event was reported. Non-serious events were primarily mild-moderate, with respiratory symptoms (n = 16 total events), skin irritation/bruising (n = 14), and gastrointestinal discomfort (n = 12) being most frequent. Physical function evaluated as 6-min walk distance, 4-m gait speed, and chair-stands time was significantly and clinically-meaningfully improved (p < .05). Pulmonary function, clinical chemistries, frailty index (FI-LAB), and reported health were unchanged. DQ effects on circulat.ing SASP factors were inconclusive, but correlations were observed between change in function and change in SASP-related matrix-remodeling proteins, microRNAs, and pro-inflammatory cytokines (23/48 markers r ≥ 0.50).FINDINGSFourteen patients with stable IPF were recruited. The retention rate was 100% with no DQ discontinuation; planned clinical assessments were complete in 13/14 participants. One serious adverse event was reported. Non-serious events were primarily mild-moderate, with respiratory symptoms (n = 16 total events), skin irritation/bruising (n = 14), and gastrointestinal discomfort (n = 12) being most frequent. Physical function evaluated as 6-min walk distance, 4-m gait speed, and chair-stands time was significantly and clinically-meaningfully improved (p < .05). Pulmonary function, clinical chemistries, frailty index (FI-LAB), and reported health were unchanged. DQ effects on circulat.ing SASP factors were inconclusive, but correlations were observed between change in function and change in SASP-related matrix-remodeling proteins, microRNAs, and pro-inflammatory cytokines (23/48 markers r ≥ 0.50).Our first-in-humans open-label pilot supports study feasibility and provides initial evidence that senolytics may alleviate physical dysfunction in IPF, warranting evaluation of DQ in larger randomized controlled trials for senescence-related diseases. ClinicalTrials.gov identifier: NCT02874989 (posted 2016-2018).INTERPRETATIONOur first-in-humans open-label pilot supports study feasibility and provides initial evidence that senolytics may alleviate physical dysfunction in IPF, warranting evaluation of DQ in larger randomized controlled trials for senescence-related diseases. ClinicalTrials.gov identifier: NCT02874989 (posted 2016-2018).
Cellular senescence is a key mechanism that drives age-related diseases, but has yet to be targeted therapeutically in humans. Idiopathic pulmonary fibrosis (IPF) is a progressive, fatal cellular senescence-associated disease. Selectively ablating senescent cells using dasatinib plus quercetin (DQ) alleviates IPF-related dysfunction in bleomycin-administered mice. A two-center, open-label study of intermittent DQ (D:100 mg/day, Q:1250 mg/day, three-days/week over three-weeks) was conducted in participants with IPF (n = 14) to evaluate feasibility of implementing a senolytic intervention. The primary endpoints were retention rates and completion rates for planned clinical assessments. Secondary endpoints were safety and change in functional and reported health measures. Associations with the senescence-associated secretory phenotype (SASP) were explored. Fourteen patients with stable IPF were recruited. The retention rate was 100% with no DQ discontinuation; planned clinical assessments were complete in 13/14 participants. One serious adverse event was reported. Non-serious events were primarily mild-moderate, with respiratory symptoms (n = 16 total events), skin irritation/bruising (n = 14), and gastrointestinal discomfort (n = 12) being most frequent. Physical function evaluated as 6-min walk distance, 4-m gait speed, and chair-stands time was significantly and clinically-meaningfully improved (p < .05). Pulmonary function, clinical chemistries, frailty index (FI-LAB), and reported health were unchanged. DQ effects on circulat.ing SASP factors were inconclusive, but correlations were observed between change in function and change in SASP-related matrix-remodeling proteins, microRNAs, and pro-inflammatory cytokines (23/48 markers r ≥ 0.50). Our first-in-humans open-label pilot supports study feasibility and provides initial evidence that senolytics may alleviate physical dysfunction in IPF, warranting evaluation of DQ in larger randomized controlled trials for senescence-related diseases. ClinicalTrials.gov identifier: NCT02874989 (posted 2016-2018).
AbstractBackgroundCellular senescence is a key mechanism that drives age-related diseases, but has yet to be targeted therapeutically in humans. Idiopathic pulmonary fibrosis (IPF) is a progressive, fatal cellular senescence-associated disease. Selectively ablating senescent cells using dasatinib plus quercetin (DQ) alleviates IPF-related dysfunction in bleomycin-administered mice. MethodsA two-center, open-label study of intermittent DQ (D:100 mg/day, Q:1250 mg/day, three-days/week over three-weeks) was conducted in participants with IPF ( n = 14) to evaluate feasibility of implementing a senolytic intervention. The primary endpoints were retention rates and completion rates for planned clinical assessments. Secondary endpoints were safety and change in functional and reported health measures. Associations with the senescence-associated secretory phenotype (SASP) were explored. FindingsFourteen patients with stable IPF were recruited. The retention rate was 100% with no DQ discontinuation; planned clinical assessments were complete in 13/14 participants. One serious adverse event was reported. Non-serious events were primarily mild-moderate, with respiratory symptoms ( n = 16 total events), skin irritation/bruising (n = 14), and gastrointestinal discomfort ( n = 12) being most frequent. Physical function evaluated as 6-min walk distance, 4-m gait speed, and chair-stands time was significantly and clinically-meaningfully improved ( p < .05). Pulmonary function, clinical chemistries, frailty index (FI-LAB), and reported health were unchanged. DQ effects on circulat.ing SASP factors were inconclusive, but correlations were observed between change in function and change in SASP-related matrix-remodeling proteins, microRNAs, and pro-inflammatory cytokines (23/48 markers r ≥ 0.50). InterpretationOur first-in-humans open-label pilot supports study feasibility and provides initial evidence that senolytics may alleviate physical dysfunction in IPF, warranting evaluation of DQ in larger randomized controlled trials for senescence-related diseases. ClinicalTrials.gov identifier: NCT02874989 (posted 2016–2018).
Cellular senescence is a key mechanism that drives age-related diseases, but has yet to be targeted therapeutically in humans. Idiopathic pulmonary fibrosis (IPF) is a progressive, fatal cellular senescence-associated disease. Selectively ablating senescent cells using dasatinib plus quercetin (DQ) alleviates IPF-related dysfunction in bleomycin-administered mice. A two-center, open-label study of intermittent DQ (D:100 mg/day, Q:1250 mg/day, three-days/week over three-weeks) was conducted in participants with IPF (n = 14) to evaluate feasibility of implementing a senolytic intervention. The primary endpoints were retention rates and completion rates for planned clinical assessments. Secondary endpoints were safety and change in functional and reported health measures. Associations with the senescence-associated secretory phenotype (SASP) were explored. Fourteen patients with stable IPF were recruited. The retention rate was 100% with no DQ discontinuation; planned clinical assessments were complete in 13/14 participants. One serious adverse event was reported. Non-serious events were primarily mild-moderate, with respiratory symptoms (n = 16 total events), skin irritation/bruising (n = 14), and gastrointestinal discomfort (n = 12) being most frequent. Physical function evaluated as 6-min walk distance, 4-m gait speed, and chair-stands time was significantly and clinically-meaningfully improved (p < .05). Pulmonary function, clinical chemistries, frailty index (FI-LAB), and reported health were unchanged. DQ effects on circulat.ing SASP factors were inconclusive, but correlations were observed between change in function and change in SASP-related matrix-remodeling proteins, microRNAs, and pro-inflammatory cytokines (23/48 markers r ≥ 0.50). Our first-in-humans open-label pilot supports study feasibility and provides initial evidence that senolytics may alleviate physical dysfunction in IPF, warranting evaluation of DQ in larger randomized controlled trials for senescence-related diseases. ClinicalTrials.gov identifier: NCT02874989 (posted 2016–2018).
Author Tchkonia, Tamar
Masternak, Michal M.
LeBrasseur, Nathan K.
Justice, Jamie N.
Kritchevsky, Stephen B.
Prata, Larissa
Pascual, Rodolfo
Nambiar, Anoop M.
Hashmi, Shahrukh K.
Musi, Nicolas
Kirkland, James L.
AuthorAffiliation d Internal Medicine – Pulmonary, Critical Care, Allergy, Immunologic Medicine, Wake Forest School of Medicine, 1 Medical Center Blvd, Winston-Salem, NC 27157, United States
b Division of Pulmonary Diseases and Critical Care Medicine, Department of Internal Medicine, University of Texas Health Sciences Center at San Antonio (UTHSCSA) and South Texas Veterans Health Care System, San Antonio, TX 78229, United States
f Barshop Institute for Longevity and Aging Studies, Center for Healthy Aging, University of Texas Health Sciences Center at San Antonio and South Texas Veterans Health Care System, San Antonio, TX 78229, United States
g San Antonio Geriatric Research, Education and Clinical Center, South Texas Veterans Health Care System, San Antonio, TX 78229, United States
a Sticht Center for Healthy Aging and Alzheimer's Prevention, Internal Medicine – Gerontology and Geriatric Medicine, Wake Forest School of Medicine (WFSM), 1 Medical Center Blvd, Winston-Salem, NC 27157, United States
e Burne
AuthorAffiliation_xml – name: d Internal Medicine – Pulmonary, Critical Care, Allergy, Immunologic Medicine, Wake Forest School of Medicine, 1 Medical Center Blvd, Winston-Salem, NC 27157, United States
– name: a Sticht Center for Healthy Aging and Alzheimer's Prevention, Internal Medicine – Gerontology and Geriatric Medicine, Wake Forest School of Medicine (WFSM), 1 Medical Center Blvd, Winston-Salem, NC 27157, United States
– name: b Division of Pulmonary Diseases and Critical Care Medicine, Department of Internal Medicine, University of Texas Health Sciences Center at San Antonio (UTHSCSA) and South Texas Veterans Health Care System, San Antonio, TX 78229, United States
– name: f Barshop Institute for Longevity and Aging Studies, Center for Healthy Aging, University of Texas Health Sciences Center at San Antonio and South Texas Veterans Health Care System, San Antonio, TX 78229, United States
– name: c Robert and Arlene Kogod Center on Aging, Mayo Clinic, Rochester, MN 55905, United States
– name: e Burnett School of Biomedical Sciences, University of Central Florida, Orlando, FL 32827, United States
– name: g San Antonio Geriatric Research, Education and Clinical Center, South Texas Veterans Health Care System, San Antonio, TX 78229, United States
Author_xml – sequence: 1
  givenname: Jamie N.
  surname: Justice
  fullname: Justice, Jamie N.
  email: jnjustic@wakehealth.edu
  organization: Sticht Center for Healthy Aging and Alzheimer's Prevention, Internal Medicine – Gerontology and Geriatric Medicine, Wake Forest School of Medicine (WFSM), 1 Medical Center Blvd, Winston-Salem, NC 27157, United States
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  givenname: Anoop M.
  surname: Nambiar
  fullname: Nambiar, Anoop M.
  email: Nambiar@uthscsa.edu
  organization: Division of Pulmonary Diseases and Critical Care Medicine, Department of Internal Medicine, University of Texas Health Sciences Center at San Antonio (UTHSCSA) and South Texas Veterans Health Care System, San Antonio, TX 78229, United States
– sequence: 3
  givenname: Tamar
  surname: Tchkonia
  fullname: Tchkonia, Tamar
  email: Tchkonia.Tamar@mayo.edu
  organization: Robert and Arlene Kogod Center on Aging, Mayo Clinic, Rochester, MN 55905, United States
– sequence: 4
  givenname: Nathan K.
  surname: LeBrasseur
  fullname: LeBrasseur, Nathan K.
  email: LeBrasseur.Nathan@mayo.edu
  organization: Robert and Arlene Kogod Center on Aging, Mayo Clinic, Rochester, MN 55905, United States
– sequence: 5
  givenname: Rodolfo
  surname: Pascual
  fullname: Pascual, Rodolfo
  email: rpascual@wakehealth.edu
  organization: Internal Medicine – Pulmonary, Critical Care, Allergy, Immunologic Medicine, Wake Forest School of Medicine, 1 Medical Center Blvd, Winston-Salem, NC 27157, United States
– sequence: 6
  givenname: Shahrukh K.
  surname: Hashmi
  fullname: Hashmi, Shahrukh K.
  email: Hashmi.Shahrukh@mayo.edu
  organization: Robert and Arlene Kogod Center on Aging, Mayo Clinic, Rochester, MN 55905, United States
– sequence: 7
  givenname: Larissa
  surname: Prata
  fullname: Prata, Larissa
  email: prata.larissa@mayo.edu
  organization: Robert and Arlene Kogod Center on Aging, Mayo Clinic, Rochester, MN 55905, United States
– sequence: 8
  givenname: Michal M.
  orcidid: 0000-0002-8483-930X
  surname: Masternak
  fullname: Masternak, Michal M.
  email: michal.masternak@ucf.edu
  organization: Burnett School of Biomedical Sciences, University of Central Florida, Orlando, FL 32827, United States
– sequence: 9
  givenname: Stephen B.
  surname: Kritchevsky
  fullname: Kritchevsky, Stephen B.
  email: skritche@wakehealth.edu
  organization: Sticht Center for Healthy Aging and Alzheimer's Prevention, Internal Medicine – Gerontology and Geriatric Medicine, Wake Forest School of Medicine (WFSM), 1 Medical Center Blvd, Winston-Salem, NC 27157, United States
– sequence: 10
  givenname: Nicolas
  surname: Musi
  fullname: Musi, Nicolas
  email: Musi@uthscsa.edu
  organization: Barshop Institute for Longevity and Aging Studies, Center for Healthy Aging, University of Texas Health Sciences Center at San Antonio and South Texas Veterans Health Care System, San Antonio, TX 78229, United States
– sequence: 11
  givenname: James L.
  surname: Kirkland
  fullname: Kirkland, James L.
  email: Kirkland.James@mayo.edu
  organization: Robert and Arlene Kogod Center on Aging, Mayo Clinic, Rochester, MN 55905, United States
BackLink https://www.ncbi.nlm.nih.gov/pubmed/30616998$$D View this record in MEDLINE/PubMed
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Keywords Translation
Idiopathic pulmonary fibrosis
Cellular senescence
Aging
Clinical trial
Senolytics
Interstitial lung disease
Language English
License This is an open access article under the CC BY license.
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Drs. Justice and Nambiar contributed equally to this work.
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Snippet Cellular senescence is a key mechanism that drives age-related diseases, but has yet to be targeted therapeutically in humans. Idiopathic pulmonary fibrosis...
AbstractBackgroundCellular senescence is a key mechanism that drives age-related diseases, but has yet to be targeted therapeutically in humans. Idiopathic...
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StartPage 554
SubjectTerms Advanced Basic Science
Aging
Cellular senescence
Clinical trial
Idiopathic pulmonary fibrosis
Internal Medicine
Interstitial lung disease
Research paper
Senolytics
Translation
Title Senolytics in idiopathic pulmonary fibrosis: Results from a first-in-human, open-label, pilot study
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https://dx.doi.org/10.1016/j.ebiom.2018.12.052
https://www.ncbi.nlm.nih.gov/pubmed/30616998
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https://pubmed.ncbi.nlm.nih.gov/PMC6412088
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