Repeated Administration of Cisplatin Transforms Kidney Fibroblasts through G2/M Arrest and Cellular Senescence

Cisplatin is a potent chemotherapeutic used for the treatment of many types of cancer, but it has nephrotoxic side effects leading to acute kidney injury and subsequently chronic kidney disease (CKD). Previous work has focused on acute kidney tubular injury induced by cisplatin, whereas the chronic...

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Published inCells (Basel, Switzerland) Vol. 11; no. 21; p. 3472
Main Authors Yu, Jia-Bin, Lee, Dong-Sun, Padanilam, Babu J, Kim, Jinu
Format Journal Article
LanguageEnglish
Published Switzerland MDPI AG 01.11.2022
MDPI
Subjects
Actin
Aging
Animals
Antibodies
Apoptosis
Cancer
Cell adhesion
Cell cycle
Cell Line, Tumor
Cell size
Cells
Cellular Senescence
Cisplatin
Cisplatin - metabolism
Cisplatin - pharmacology
Complications
Complications and side effects
Cyclin-dependent kinase inhibitor p21
Fibroblasts
Fibroblasts - metabolism
Fibronectin
Fibronectins - metabolism
G2 Phase Cell Cycle Checkpoints
Genetic transformation
Health aspects
Hypertrophy
Kidney - metabolism
Kidney diseases
kidney fibroblast
Kidneys
Laboratories
Life sciences
Metastasis
myofibroblast
p21
Paclitaxel
Phenotypes
Rats
Renal Insufficiency, Chronic - metabolism
Senescence
Smooth muscle
β-Galactosidase
South Korea
United States > US
senescence
kidney fibroblast
cell cycle
myofibroblast
lamin B1
cisplatin
p21
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Abstract Cisplatin is a potent chemotherapeutic used for the treatment of many types of cancer, but it has nephrotoxic side effects leading to acute kidney injury and subsequently chronic kidney disease (CKD). Previous work has focused on acute kidney tubular injury induced by cisplatin, whereas the chronic sequelae post-injury has not been well-explored. In the present study, we established a kidney fibroblast model of CKD induced by repeated administration of cisplatin (RAC) as a clinically relevant model. In NRK-49F rat kidney fibroblasts, RAC upregulated α-smooth muscle actin (α-SMA) and fibronectin proteins, suggesting that RAC induces kidney fibroblast-to-myofibroblast transformation. RAC also enhanced cell size, including the cell attachment surface area, nuclear area, and cell volume. Furthermore, RAC induced p21 expression and senescence-associated β-galactosidase activity, suggesting that kidney fibroblasts exposed to RAC develop a senescent phenotype. Inhibition of p21 reduced cellular senescence, hypertrophy, and myofibroblast transformation induced by RAC. Intriguingly, after RAC, kidney fibroblasts were arrested at the G2/M phase. Repeated treatment with paclitaxel as an inducer of G2/M arrest upregulated p21, α-SMA, and fibronectin in the kidney fibroblasts. Taken together, these data suggest that RAC transforms kidney fibroblasts into myofibroblasts through G2/M arrest and cellular senescence.
AbstractList Cisplatin is a potent chemotherapeutic used for the treatment of many types of cancer, but it has nephrotoxic side effects leading to acute kidney injury and subsequently chronic kidney disease (CKD). Previous work has focused on acute kidney tubular injury induced by cisplatin, whereas the chronic sequelae post-injury has not been well-explored. In the present study, we established a kidney fibroblast model of CKD induced by repeated administration of cisplatin (RAC) as a clinically relevant model. In NRK-49F rat kidney fibroblasts, RAC upregulated α-smooth muscle actin (α-SMA) and fibronectin proteins, suggesting that RAC induces kidney fibroblast-to-myofibroblast transformation. RAC also enhanced cell size, including the cell attachment surface area, nuclear area, and cell volume. Furthermore, RAC induced p21 expression and senescence-associated β-galactosidase activity, suggesting that kidney fibroblasts exposed to RAC develop a senescent phenotype. Inhibition of p21 reduced cellular senescence, hypertrophy, and myofibroblast transformation induced by RAC. Intriguingly, after RAC, kidney fibroblasts were arrested at the G2/M phase. Repeated treatment with paclitaxel as an inducer of G2/M arrest upregulated p21, α-SMA, and fibronectin in the kidney fibroblasts. Taken together, these data suggest that RAC transforms kidney fibroblasts into myofibroblasts through G2/M arrest and cellular senescence.
Audience Academic
Author Padanilam, Babu J
Kim, Jinu
Yu, Jia-Bin
Lee, Dong-Sun
AuthorAffiliation 1 Interdisciplinary Graduate Program in Advanced Convergence Technology & Science, Jeju National University, Jeju 63243, Korea
3 Jeju Microbiome Research Center, Jeju National University, Jeju 63243, Korea
6 Department of Anatomy, Jeju National University College of Medicine, Jeju 63243, Korea
2 Subtropical/Tropical Organism Gene Bank, Jeju National University, Jeju 63243, Korea
4 Faculty of Biotechnology, College of Applied Life Sciences, SARI, Jeju National University, Jeju 63243, Korea
5 Department of Urology, Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA
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– name: 6 Department of Anatomy, Jeju National University College of Medicine, Jeju 63243, Korea
– name: 1 Interdisciplinary Graduate Program in Advanced Convergence Technology & Science, Jeju National University, Jeju 63243, Korea
– name: 5 Department of Urology, Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA
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  fullname: Yu, Jia-Bin
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/36359868$$D View this record in MEDLINE/PubMed
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Issue 21
Keywords senescence
kidney fibroblast
cell cycle
myofibroblast
lamin B1
cisplatin
p21
Language English
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  contributor:
    fullname: Kim
– volume: 4
  start-page: 1798
  year: 2009
  ident: ref_39
  article-title: Protocols to detect senescence-associated beta-galactosidase (SA-betagal) activity, a biomarker of senescent cells in culture and in vivo
  publication-title: Nat. Protoc.
  doi: 10.1038/nprot.2009.191
  contributor:
    fullname: Erusalimsky
SSID ssj0000816105
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Snippet Cisplatin is a potent chemotherapeutic used for the treatment of many types of cancer, but it has nephrotoxic side effects leading to acute kidney injury and...
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SubjectTerms Actin
Aging
Animals
Antibodies
Apoptosis
Cancer
Cell adhesion
Cell cycle
Cell Line, Tumor
Cell size
Cells
Cellular Senescence
Cisplatin
Cisplatin - metabolism
Cisplatin - pharmacology
Complications
Complications and side effects
Cyclin-dependent kinase inhibitor p21
Fibroblasts
Fibroblasts - metabolism
Fibronectin
Fibronectins - metabolism
G2 Phase Cell Cycle Checkpoints
Genetic transformation
Health aspects
Hypertrophy
Kidney - metabolism
Kidney diseases
kidney fibroblast
Kidneys
Laboratories
Life sciences
Metastasis
myofibroblast
p21
Paclitaxel
Phenotypes
Rats
Renal Insufficiency, Chronic - metabolism
Senescence
Smooth muscle
β-Galactosidase
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Title Repeated Administration of Cisplatin Transforms Kidney Fibroblasts through G2/M Arrest and Cellular Senescence
URI https://www.ncbi.nlm.nih.gov/pubmed/36359868
https://www.proquest.com/docview/2734618117
https://pubmed.ncbi.nlm.nih.gov/PMC9655665
https://doaj.org/article/41735ffd62134e098a1607a9c60c320d
Volume 11
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