Cited by 192Cell death mechanisms and regulationLiver physiology and pathologyGenetics, Aging, and Longevity in Model Organisms

Necroptosis contributes to chronic inflammation and fibrosis in aging liver

Open access
Mohammed, Sabira, Thadathil, Nidheesh, Selvarani, Ramasamy, Nicklas, Evan H., Wang, Dawei, Miller, Benjamin F., Richardson, Arlan, Deepa, Sathyaseelan S.·2021·Aging Cell

Published version of a preprint

Abstract

Inflammaging, characterized by an increase in low‐grade chronic inflammation with age, is a hallmark of aging and is strongly associated with various age‐related diseases, including chronic liver disease (CLD) and hepatocellular carcinoma (HCC). Because necroptosis is a cell death pathway that induces inflammation through the release of DAMPs, we tested the hypothesis that age‐associated increase in necroptosis contributes to chronic inflammation in aging liver. Phosphorylation of MLKL and MLKL oligomers, markers of necroptosis, as well as phosphorylation of RIPK3 and RIPK1 were significantly upregulated in the livers of old mice relative to young mice and this increase occurred in the later half of life (i.e., after 18 months of age). Markers of M1 macrophages, expression of pro‐inflammatory cytokines (TNFα, IL6 and IL1β), and markers of fibrosis were all significantly upregulated in the liver with age and the change in necroptosis paralleled the changes in inflammation and fibrosis. Hepatocytes and liver macrophages isolated from old mice showed elevated levels of necroptosis markers as well as increased expression of pro‐inflammatory cytokines relative to young mice. Short‐term treatment with the necroptosis inhibitor, necrostatin‐1s (Nec‐1s), reduced necroptosis, markers of M1 macrophages, fibrosis, and cell senescence as well as reducing the expression of pro‐inflammatory cytokines in the livers of old mice. Thus, our data show for the first time that liver aging is associated with increased necroptosis and necroptosis contributes to chronic inflammation in the liver, which in turn appears to contribute to liver fibrosis and possibly CLD.

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Written from the paper’s full text.

TL;DR

In aging mouse liver, necroptosis markers increase primarily after 18 months and parallel increases in M1 macrophages, pro-inflammatory cytokines, and fibrosis markers. Short-term necrostatin-1s treatment in old mice reduces necroptosis, inflammation, fibrosis, and senescence markers, suggesting necroptosis contributes to age-related chronic liver inflammation.

Key findings

  • Necroptosis markers increased with age in liver: late apoptotic/necroptotic cells were 3.3-fold higher at 18 months and 4.6-fold higher at 24 months vs. 7 months; MLKL oligomers increased 2-fold at 18 months and 5-fold at 24 months; plasma HMGB1 increased 4-fold at 18 months and 7-fold at 24 months.
  • Inflammation increased with age: CD45+ immune cells were 67.9% ± 6.84% in old vs. 32.86% ± 0.92% in young mice; F4/80+ macrophages were 27.9% ± 1.8% vs. 16.6% ± 1.6%; M1 macrophages were 9.03% ± 0.59% vs. 2.45% ± 0.18%; TNFα, IL6, and IL-1β transcripts increased 2–3 fold at 18–24 months.
  • Isolated old hepatocytes showed increased TNFα (4-fold), IL6 (4-fold), IL-1β (40-fold), and MCP1/CCL2 (4-fold); isolated old macrophages showed increased IL-1β (3.5-fold) and MCP-1 (5.6-fold).
  • Fibrosis markers increased with age: TGFβ 1.5–2 fold, desmin 3–4 fold, Col1α1/Col3α1 2.5 fold, hydroxyproline 1.5–1.9 fold, and picrosirius red staining 2.7 fold; 30-day Nec-1s treatment reduced necroptosis markers, M1 macrophage markers, TNFα, serum ALT, fibrosis markers, and p16/p21 transcripts in old mice.

Methods

  • Male C57BL/6 wild-type mice at 7, 12, 18, and 22–24 months of age (n = 5–10/group) were obtained from the National Institute on Aging; liver tissue, isolated hepatocytes, macrophages, and liver sinusoidal endothelial cells were analyzed.
  • Main assays included Annexin V/propidium iodide flow cytometry, western blotting for necroptosis and inflammation proteins, RT-PCR, immunofluorescence, magnetic-activated cell sorting, hydroxyproline assay, picrosirius red staining, and serum ALT measurement.
  • Old mice were treated with the RIPK1 inhibitor necrostatin-1s (Nec-1s) for 30 days; statistical analysis used ordinary one-way ANOVA with Tukey’s post hoc test and Student’s t test, with p < 0.05 considered significant.

Limitations

  • Stated: the authors cannot rule out off-target effects of Nec-1s and call for future studies using other pharmacological necroptosis inhibitors or genetic knockout models of Ripk3 or Mlkl.
  • Stated: long-term Nec-1s treatment is needed to assess feasibility for inflammaging and aging, and future studies will address in vitro effects of DAMPs on inflammatory cytokine production by different liver cell types.
  • Evident from the text: the study is primarily correlational for age-related associations, uses only male C57BL/6 mice, and tests short-term Nec-1s in old mice rather than lifespan or healthspan outcomes.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1111/acel.13512

Cites

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Statistics

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Claims the paper makes

0 of 38 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    Protein levels of TNFα and IL-1β are significantly increased in livers of 18- and 24-month-old mice relative to 7- or 12-month-old mice.

    “The changes in protein levels of TNFα and IL‐1β also were significantly increased in the livers of 18‐ and 24‐month‐old mice relative to 7‐ or 12‐month old mice (Figure 3f).”
    Quote in the paperSubstantial claim
  • Findingown data

    Necrosis is increased at 12 months relative to 7-month-old mice.

    “however, necrosis was increased at 12 months relative to 7‐month‐old mice.”
    Quote in the paperSubstantial claim
  • Findingown data

    The total immune cell population (CD45+ cells) is significantly increased in livers of old mice (67.9% ± 6.84%) relative to young mice (32.86% ± 0.92%).

    “Flow cytometry analysis showed that the total immune cell population (percentage of CD45+ cells), was significantly increased in the livers of old mice (67.9% ± 6.84%) relative to young mice (32.86% ± 0.92%) (Figure 3a).”
    Quote in the paperSubstantial claim
  • Findingown data

    Circulating HMGB1 levels are significantly elevated at 18 months (fourfold) and 24 months (sevenfold) of age relative to 7- or 12-month-old mice.

    “Circulating levels of HMGB1 are significantly elevated at 18 months (fourfold) and 24 months (sevenfold) of age relative to 7‐ or 12‐month‐old mice (Figure 1f).”
    Quote in the paperSubstantial claim
  • Findingown data

    Ripk1 transcript levels are similar in hepatocytes of old and young mice.

    “Mlkl and Ripk3 transcript levels are also significantly elevated (7.5‐fold and eightfold), whereas Ripk1 transcript levels were similar, in the hepatocytes of old mice relative to young mice (Figure S1d).”
    Quote in the paperNot a substantial claim
  • May combine two claims. 40
  • Classified as probably not a substantial claim. 26
  • May combine two claims.

    Findingown data

    Transcript levels of TNFα (fourfold), IL6 (fourfold), IL-1β (40-fold), and MCP1/CCL2 (fourfold) are significantly increased in hepatocytes isolated from old mice relative to young mice.

    “Transcript levels were significantly increased for TNFα (fourfold), IL6 (fourfold) and IL‐1β (40‐fold) and MCP1/CCL2 (fourfold) in the hepatocytes isolated from old mice relative to hepatocytes from young mice (Figure 3h).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    The percent of liver cells undergoing early apoptosis (Annexin V positive) is significantly increased with age, starting from 12 months (2.5-fold), and remains elevated at 18 (2.7-fold) and 24 months (2.2-fold).

    “The early apoptotic cell population was significantly higher in the liver starting from 12 months of age (2.5‐fold) and remained elevated at 18 (2.7‐fold) and 24 months of age (2.2‐fold)”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Transcript levels of F4/80 and MCP-1 are similar in 7- and 12-month-old mice, whereas they are significantly increased (twofold for F4/80 and fivefold and sixfold for MCP-1) in 18- and 24-month-old mice.

    “Transcript levels of F4/80 and monocyte chemoattractant protein‐1 (MCP‐1) were similar in 7‐ and 12‐month‐old mice, whereas the levels are significantly increased (twofold for F4/80 and fivefold and sixfold for MCP‐1) in 18‐ and 24‐month‐old mice. (Figure S2a).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    P-MLKL and MLKL levels are both significantly elevated (twofold) in hepatocytes isolated from old mice relative to young mice.

    “levels of P‐MLKL and MLKL were both significantly elevated (twofold) in the hepatocytes isolated from old mice relative to young mice (Figure 2b).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Expression of M1 macrophage markers at 24 months is similar to 18 months, except for CD11c, which is increased between 18 and 24 months.

    “Expression of M1 macrophage markers at 24 months was similar to those at 18‐months, except for CD11c, which was increased between 18 and 24 months of age (Figure S2b).”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    P-RIPK3 and RIPK3 levels are significantly elevated in hepatocytes from old mice (twofold and 1.4-fold respectively).

    “Levels of P‐RIPK3 and RIPK3 are significantly elevated in the hepatocytes from old mice (twofold and 1.4‐fold respectively)”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    P-MLKL and P-RIPK3 levels show a slight reduction at 24 months relative to 18 months, but this is not statistically significant.

    “The levels of P‐MLKL and P‐RIPK3 showed a slight reduction at 24 months relative to 18 months, however, this was not statistically significant.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Findingown data

    The M2 macrophage population (CD45+CD11b+Ly6G-F4/80+CD206+ cells) is reduced in livers of old mice (5.06 ± 0.12) relative to young mice (6.48 ± 0.56), but this reduction did not reach statistical significance.

    “The M2 macrophage population (CD45+CD11b+Ly6G‐ F4/80+ CD206+ cells) was reduced in the livers of old mice (5.06 ± 0.12) relative to young mice (6.48 ± 0.56), however, this reduction did not reach statistical significance (Figure 3d).”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    Picrosirius red staining in old mice liver is significantly higher (2.7-fold) relative to young mice, suggesting increased collagen levels.

    “Consistent with this, picrosirius red (PSR) staining in the old mice liver was significantly higher (2.7‐fold) relative to young mice, suggesting increased levels of collagen in old mice liver (Figure 4e).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Nec-1s treatment had no effect on body weight or liver weight of old WT mice, indicating no obvious negative effect.

    “Nec‐1s treatment had no effect on the body weight or liver weight of old WT mice (Figure S3a and Figure S3b), indicating no obvious negative effect of Nec‐1s on old mice.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    Serum ALT levels are significantly increased in old mice (2.2-fold) relative to young mice, and Nec-1s treatment significantly reduced serum ALT levels in old mice to levels comparable to young mice.

    “We found a significant increase in the serum levels of ALT in the old mice (2.2‐fold) relative to young mice, and Nec‐1s treatment significantly reduced serum ALT levels in old mice to levels comparable to young mice (Figure 5f).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Protein expression of F4/80 (fourfold) and CD68 (fivefold) is significantly increased in livers of old mice, and these are significantly reduced by Nec-1s treatment to levels similar to young liver.

    “protein expression of expression of F4/80 (fourfold) and CD68 (fivefold) was significantly increased in the livers of old mice, which were significantly reduced by Nec‐1s treatment to levels similar to young liver as shown by immunofluorescence staining (Figure 5d).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Expression of CD206 protein (M2 macrophage marker) is significantly reduced (80%) in livers of old mice relative to young mice, and Nec-1s had no effect on CD206 expression in old mice.

    “In contrast, the expression of CD206 protein (M2 macrophage marker) was significantly reduced (80%) in the livers of old mice relative to young mice and Nec‐1s had no effect on CD206 expression in the livers of old mice (Figure 5d).”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    Nec-1s treatment significantly reduced necroptosis, with P-MLKL and MLKL oligomer levels reduced to levels seen in young mice.

    “Nec‐1s treatment significantly reduced necroptosis as predicted, that is, the levels of PMLKL and MLKL oligomers were reduced to the levels seen in young mice (Figure 5a, b).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    While P-MLKL expression was similar at 18 and 24 months, MLKL oligomer levels were significantly increased from 18 to 24 months.

    “While the expression of P‐MLKL was similar at 18 and 24 months, MLKL oligomer levels were significantly increased from 18 to 24 months.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Transcript levels of pro-inflammatory cytokines TNFα, IL6, and IL-1β, which were elevated in livers of old WT mice, are significantly reduced by Nec-1s treatment and are comparable to young mice.

    “Similarly, levels of transcripts for pro‐inflammatory cytokines TNFα, IL6 and IL‐1β, which were elevated in the livers of old WT mice, were significantly reduced by Nec‐1s treatment and were comparable to the levels in young mice (Figure S3g).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Nec-1s treatment of old mice resulted in reduced M1 macrophages and reduced expression of pro-inflammatory cytokines.

    “we observed that Nec‐1s treatment of old mice resulted in reduced M1 macrophages and the expression of pro‐inflammatory cytokines.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Total macrophage content and pro-inflammatory M1 macrophages increase with age, whereas anti-inflammatory M2 macrophages decline with age.

    “the total macrophage content as well as pro‐inflammatory M1 macrophages increase with age, whereas anti‐inflammatory M2 macrophages decline with age.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Pro-inflammatory cytokine/chemokine expression (TNFα, IL6, IL1β, and CCL2) is increased in isolated hepatocytes and isolated macrophages (IL1β and CCL2), but not in LSECs from old mice.

    “We also found that pro‐inflammatory cytokine/chemokine expression (e.g., TNFα, IL6, IL1β, and CCL2) were increased in isolated hepatocytes, isolated macrophages (IL1β and CCL2), but not in LSECs from old mice.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingcitation

    There is a strong age-related association between necroptosis and inflammation in the liver, as both increase in the latter half of life, around 18 months of age.

    “We observed a strong age‐related association between necroptosis and inflammation in liver as both increase in the latter half of life, around 18 months of age when mice began to exhibit some age‐associated pathologies (Stahl et al., 2020).”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Necroptosis increases with age in white adipose tissue of mice and is reduced by interventions that delay aging (dietary restriction or Ames dwarf mice).

    “Previously, we reported that necroptosis increases with age in the white adipose tissue of mice and is reduced by interventions that delay aging (dietary restriction or in Ames dwarf mice) (Deepa et al., 2018; Royce et al., 2019).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Deepa et al., 2018

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    • cites Royce et al., 2019

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  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Necroptosis has emerged as a novel mode of cell death in various chronic liver diseases such as NAFLD and NASH, conditions also associated with aging in liver.

    “Necroptosis has emerged as a novel mode of cell death in various chronic liver diseases such as nonalcoholic fatty liver disease (NAFLD) and nonalcoholic steatohepatitis (NASH), conditions that are also associated with aging in liver (Saeed & Jun, 2014).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Saeed & Jun, 2014

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  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Necroptosis is initiated by necroptotic stimuli such as TNFα, oxidative stress or mTOR/Akt pathway, which sequentially phosphorylate and activate RIPK1 and RIPK3 that in turn phosphorylate MLKL.

    “However, necroptosis is also initiated by necroptotic stimuli [e.g., TNFα, oxidative stress or mTOR/Akt pathway (Royce et al., 2019), which sequentially phosphorylate and activate receptor‐interacting protein kinase 1(RIPK1) and RIPK3 that in turn phosphorylate the pseudokinase mixed lineage kinase domain‐like (MLKL) protein.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Royce et al., 2019

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  • Classified as probably not a substantial claim.

    Premisecitation

    DAMPs released from damaged or dying hepatocytes are one of the proposed mediators of chronic inflammation in the liver.

    “Damage‐associated molecular patterns (DAMPs, example, HMGB1, mitochondrial DNA, nuclear DNA, ATP etc.) released from damaged or dying hepatocytes are one of the proposed mediators of chronic inflammation in the liver (Brenner et al., 2013).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Brenner et al., 2013

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  • May combine two claims.

    Premisecitation

    Necroptosis and inflammation are increased in livers of Sod1-/- mice, and blocking necroptosis reduced inflammation in their livers.

    “Recently, we found that necroptosis and inflammation are increased in the livers of a mouse model of accelerated aging (mice deficient in the antioxidant enzyme, Cu/Zn superoxide dismutase, Sod1‐/‐ mice) and blocking necroptosis reduced inflammation in the livers of Sod1‐/‐ mice (Mohammed et al., 2021).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Mohammed et al., 2021

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  • May combine two claims.

    Interpretationown data

    The changes in circulating HMGB1 levels parallel the changes in necroptosis markers in the liver, supporting that necroptosis increases with age in liver.

    “The changes in circulating HMGB1 levels parallel the changes in the necroptosis markers in the liver, providing additional data supporting that necroptosis increases with age in liver.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationown data

    Chronic inflammation in the liver appears to contribute to liver fibrosis and possibly CLD.

    “Thus, our data show for the first time that liver aging is associated with increased necroptosis and necroptosis contributes to chronic inflammation in the liver, which in turn appears to contribute to liver fibrosis and possibly CLD.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Chronic hepatic inflammation is a major driver of liver fibrosis.
  • Classified as probably not a substantial claim.

    Premisecitation

    Absence of caspase-8 switches cell death from apoptosis to necroptosis.

    “Absence of caspase‐8, an initiator of extrinsic apoptosis, switches cell death from apoptosis to necroptosis (Fritsch et al., 2019).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Fritsch et al., 2019

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  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    For mouse MLKL, tetramers fail to translocate to the plasma membrane and octamer formation is required for pore formation in the membrane.

    “For mouse MLKL, tetramers fail to translocate to the plasma membrane and octamer formation is required for pore formation in the membrane (Huang et al., 2017).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Huang et al., 2017

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  • May combine two claims.

    Premisecitation

    Nec-1s effectively blocks necroptosis and reduces inflammation in the liver as well as in other tissues.

    “Mice were treated with Nec‐1s (RIPK1 inhibitor) for 30 days, which has been shown to effectively block necroptosis and reduce inflammation in the liver as well as in other tissues (Mohammed et al., 2021).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Mohammed et al., 2021

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  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Necroptosis most likely evolved as an alternative form of cell death to kill cells infected by viral pathogens and to promote inflammatory and immune responses to limit the spread of viruses.

    “Necroptosis most likely evolved as an alternative form of cell death to kill cells infected by viral pathogens and to promote inflammatory and immune responses to limit the spread of the viruses (Dondelinger et al., 2016).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Dondelinger et al., 2016

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  • May combine two claims.

    Interpretationown data

    Short-term Nec-1s treatment can exert its effect on M1 macrophages and reduce age-associated hepatic inflammation and thereby liver damage and fibrosis.

    “Thus, our data shows that short‐term Nec‐1s treatment can exert its effect on the M1 macrophages and reduce age‐associated hepatic inflammation and thereby liver damage and fibrosis.”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation

    HMGB1 is a DAMP that has been shown to be released by hepatic necroptosis and is associated with acute liver injury and chronic liver disease.

    “a DAMP that has been shown to be released by hepatic necroptosis and is associated with acute liver injury and chronic liver disease (Wen et al., 2020).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Wen et al., 2020

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  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Hepatocytes constitute 80% of the liver mass and are reported to undergo cell death in CLD.

    “Hepatocytes constitute 80% of the liver mass and are reported to undergo cell death in CLD (Shojaie et al., 2020)”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Shojaie et al., 2020

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  • Classified as probably not a substantial claim.

    Premisecitation

    Kupffer cells are reported to undergo necroptosis.

    “Because Kupffer cells are reported to undergo necroptosis (Blériot et al., 2015), necroptosis in liver macrophages in aging was assessed.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Blériot et al., 2015

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    Premisecitation

    Nec-1s is a specific and potent inhibitor of RIPK1 with no reported off-target effects.

    “Nec‐1s is a specific and potent inhibitor of RIPK1 (Takahashi et al., 2012) with no reported off target effects.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Takahashi et al., 2012

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  • May combine two claims.

    Premisecitation

    Chronic liver disease, especially fibrosis, increases with age in the livers of mice and humans and is associated with increased inflammation.

    “CLD, especially fibrosis has been reported to increase with age in the livers of mice and humans (Kim et al., 2015) and is associated with increased inflammation.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Kim et al., 2015

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  • May combine two claims.

    Premisecitation

    Blocking necroptosis genetically (Ripk3-/-) in mice fed a methionine-deficient diet or pharmacologically (RIPA56) in mice fed a high-fat diet reduced liver fibrosis.

    “These data are consistent with previous reports showing that blocking necroptosis genetically (Ripk3‐/‐ ) in mice fed a methionine‐deficient diet or pharmacologically (RIPA56) in mice fed a high‐fat diet reduced liver fibrosis (Gautheron et al., 2014; Majdi et al., 2020).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Gautheron et al., 2014

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    • cites Majdi et al., 2020

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  • Classified as probably not a substantial claim.

    Premisecitation

    DAMPs are factors known to initiate macrophage activation and polarization.

    “Because DAMPs are one of the factors that are known initiate macrophages activation and polarization (Lee et al., 2020)”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Lee et al., 2020

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  • May combine two claims.

    Premisecitation

    Exposure to chronic inflammation alters macrophage function, leading to a reduced ability to remove cells and increased production of inflammatory cytokines.

    “Exposure to chronic inflammation has been shown to alter macrophage function leading to a reduction in their ability to remove cells, such as bacteria and senescent cells, and increase their production of inflammatory cytokines (Thevaranjan et al., 2017).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Thevaranjan et al., 2017

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  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    RIPK1 is involved in apoptosis as well as cell survival pathways such as NF-kB, Akt, and JNK.

    “In addition to necroptosis, RIPK1 is also involved in apoptosis as well as cell survival pathways such as NF‐kB, Akt, and JNK (Mifflin et al., 2020).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Mifflin et al., 2020

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Several FDA-approved anti-cancer drugs such as Sorafenib and Dabrafenib have been identified as anti-necroptotic agents.

    “several FDA‐approved anti‐cancer drugs such as Sorafenib and Dabrafenib have been identified as anti‐necroptotic agents (Fulda, 2018).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Fulda, 2018

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Nec-1s treatment reduces inflammation associated with necroptosis in multiple sclerosis and amyotrophic lateral sclerosis.

    “Nec‐1s treatment has been reported to reduce inflammation associated with necroptosis in multiple sclerosis and amyotrophic lateral sclerosis (Mifflin et al., 2020).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Mifflin et al., 2020

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  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    TGFβ is a major player in the induction of fibrosis and is produced by several liver cells such as LSEC, Kupffer cells, platelets, hepatocytes and macrophages.

    “Transforming growth factor beta (TGFβ) is a major player in the induction of fibrosis and is produced by several liver cells such as LSEC, Kupffer cells, platelets, hepatocytes and macrophages (Fabregat and Caballero‐Díaz, 2018).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Fabregat and Caballero‐Díaz, 2018

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Liver sinusoidal endothelial cells are known to produce inflammatory cytokines in chronic liver diseases.

    “Liver sinusoidal endothelial cells (LSEC) are known to produce inflammatory cytokines in chronic liver diseases (Wang & Peng, 2021)”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Wang & Peng, 2021

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  • Classified as probably not a substantial claim.

    Premisecitation

    Hepatocytes are also reported to produce pro-inflammatory cytokines.

    “Because hepatocytes are also reported to produce pro‐inflammatory cytokines (Stahl et al., 2020), we measured the expression of pro‐inflammatory cytokines in isolated hepatocytes.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Stahl et al., 2020

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  • May combine two claims.

    Premisecitation

    Short-term Nec-1s treatment effectively reduced necroptosis and inflammation in the livers of Sod1-/- mice.

    “Short‐term Nec‐1s treatment effectively reduced necroptosis and inflammation in the livers of Sod1‐/‐ mice (Mohammed et al., 2021).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Mohammed et al., 2021

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Therapeutic applications of RIPK1 inhibitors for the treatment of a variety of human diseases are being tested in clinical trials.

    “Currently, therapeutic applications of RIPK1 inhibitors for the treatment of a variety of human diseases are being tested in clinical trials (Mifflin et al., 2020).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Mifflin et al., 2020

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  • May combine two claims.

    Interpretationown data

    The study's data provide strong support for necroptosis playing a role in inflammaging in the liver and in the age-related increase in chronic liver disease.

    “In summary, our data proved strong support for necroptosis playing a role in inflammaging in the liver and the age‐related increase in CLD.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Chronic inflammation increases with age (inflammaging) and is associated with a large number of age-related diseases.
    • Rests on an assumption: Necroptosis is a cell death pathway that can induce inflammation through the release of DAMPs from necroptotic cells.
  • Classified as probably not a substantial claim.

    Premisecitation

    Macrophages play an important role in the removal of senescent cells.

    “macrophages, which play an important role in removal of senescent cells (Kale et al., 2020).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Kale et al., 2020

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    p16 and p21 have been reported to increase with age.

    “we assessed changes in cell senescence by measuring p16 and p21 expression, which have been reported to increase with age (Franceschi & Campisi, 2014).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Franceschi & Campisi, 2014

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    All procedures were approved by the Institutional Animal Care and Use Committee at the University of Oklahoma Health Sciences Center.

    “All procedures were approved by the Institutional Animal Care and Use Committee at the University of Oklahoma Health Sciences Center (OUHSC).”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    The purity of isolated hepatocytes was checked by real-time PCR and western blotting for liver cell-specific markers.

    “The purity of the isolated hepatocytes was checked by real‐time PCR and western blotting for the expression of liver cell specific markers: albumin (hepatocytes), F4/80 (macrophages), Clec4f (Kupffer cells), CD31 (endothelial cells) and desmin (hepatic stellate cells).”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Necroptosis has dual effects in cancer, either promoting or reducing tumor growth depending on the type of cancer.

    “Necroptosis has been reported to exhibit dual effects in cancer, that is, necroptosis can either promote or reduce tumor growth depending on the type of cancer (Gong et al., 2019).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Gong et al., 2019

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    The purity of isolated fractions was checked by real-time PCR and western blotting for cell-specific markers.

    “The purity of the isolated fractions was checked by real‐time PCR and western blotting for cell specific markers.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S2 (checkable).

    Interpretationreasoning

    Necroptosis is a potential therapeutic target for treating chronic liver diseases associated with aging.

    “Thus, necroptosis is a potential therapeutic target for treating chronic liver diseases associated with aging.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: Chronic inflammation increases with age (inflammaging) and is associated with a large number of age-related diseases.
    • Rests on an assumption: Necroptosis is a cell death pathway that can induce inflammation through the release of DAMPs from necroptotic cells.
56 of 56
  • The paper relies on this without support.

    Chronic hepatic inflammation is a major driver of liver fibrosis.

    “Chronic hepatic inflammation is a major driver of liver fibrosis, and the trans differentiation of quiescent hepatic stellate cells (HSCs) drives fibrogenesis.”
  • The paper relies on this without support.

    Desmin is a protein produced by activated HSCs and is strongly upregulated in liver fibrosis.

    “Desmin, a protein produced by activated HSCs, which is strongly upregulated in liver fibrosis was threefold to fourfold higher at 18‐ and 24‐month relative to 7‐ or 12‐month (Figure 4b).”
  • The paper relies on this without support.

    Total collagen content (hydroxyproline) is an indicator of the severity of fibrosis.

    “Next, we assessed total collagen content by measuring concentration of hydroxyproline (OHP) because total collagen content is an indicator of the severity of fibrosis.”
  • The paper relies on this without support.

    M1 macrophages play a more pro-inflammatory role in liver injury and M2 macrophages exert an anti-inflammatory effect.

    “Macrophages are categorized into M1 or M2 phenotypes: M1 macrophages play a more pro‐inflammatory role in liver injury and M2 macrophages exert an anti‐inflammatory effect.”
  • The paper relies on this without support.

    Phosphorylation of MLKL leads to its oligomerization, which binds to and disrupts the cell membrane releasing DAMPs that initiate and exacerbate inflammation.

    “Phosphorylation of MLKL leads to its oligomerization, which then binds to and disrupts the cell membrane releasing cellular components including the DAMPs that initiate and exacerbate the inflammatory process.”
  • The paper relies on this without support.

    DAMPs released from necroptotic cells bind to PRRs such as TLRs on innate immune cells resulting in induction of pro-inflammatory cytokines.

    “DAMPs released from necroptotic cells bind to pattern recognition receptors (PRRs) such as toll‐like receptors (TLRs) on innate immune cells resulting in the induction of pro‐inflammatory cytokines.”
  • The paper relies on this without support.

    Cell death by apoptosis is associated with limited release of DAMPs and is less inflammatory in nature.

    “In contrast, cell death by apoptosis is associated with limited release of DAMPs and therefore is less inflammatory in nature.”
  • The paper relies on this without support.

    Chronic inflammation increases with age (inflammaging) and is associated with a large number of age-related diseases.

    “Although it is well established that chronic inflammation increases with age (inflammaging) and is associated with a large number of age‐related diseases, the pathways/processes responsible for inflammaging are unknown.”
  • The paper relies on this without support.

    The pathways/processes responsible for inflammaging are unknown.

    “the pathways/processes responsible for inflammaging are unknown.”
  • The paper relies on this without support.

    Necroptosis is a cell death pathway that can induce inflammation through the release of DAMPs from necroptotic cells.

    “because necroptosis is a cell death pathway that can induce inflammation through the release of DAMPs from the necroptotic cells.”
  • The paper relies on this without support.

    RIPK1 is involved in apoptosis as well as necroptosis.

    “Because RIPK1 is involved in apoptosis as well as necroptosis, the effect of Nec‐1s on inflammation could also arise from alterations in apoptosis.”
  • The paper relies on this without support.

    Virus-induced necroptosis occurs through activation of the RIPK3-MLKL pathway, which is independent of RIPK1.

    “because virus‐induced necroptosis occurs through the activation of RIPK3‐MLKL pathway, which is independent of RIPK1.”
12 of 12

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • In the livers of old mice aged 18 months and older, there was a significant upregulation of phosphorylated MLKL and MLKL oligomers, markers associated with necroptosis.

    “On the other hand, in the livers of old mice (specifically, those aged 18 months and older), there was a significant upregulation of phosphorylated MLKL and MLKL oligomers, which are markers associated with necroptosis.”
  • In the livers of old mice, short-term treatment with the necroptosis inhibitor necrostatin-1s reduced necroptosis, M1 macrophage markers, cellular senescence, fibrosis, and pro-inflammatory cytokines.

    “In the livers of old mice, short-term treatment with the necroptosis inhibitor necrostatin-1s (Nec-1s) reduced necroptosis, M1 macrophage markers, cellular senescence, fibrosis, and pro-inflammatory cytokines.241”
  • Liver aging has been linked to an increase in necroptosis, and this process contributes to chronic liver inflammation, which in turn appears to be involved in the development of liver fibrosis.

    “Focus on liver, its aging has been linked to an increase in necroptosis, and this process has been found to contribute to chronic liver inflammation, which in turn appears to be involved in the development of liver fibrosis.241”
  • Heightened levels of CD45+ and F4/80+ cells have been described in the livers of 24-month-old male C57BL/6 mice and Fischer rats.

    “Heightened levels of CD45 + and F4/80 + cells have been described in the livers of 24-month-old male C57BL/6 mice [59] and Fischer rats [60].”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Figure 3 labels CD206-positive macrophages as both M1 and M2

    Minor

    The Figure 3 caption calls the CD206-positive population M1, while the Results identify the same CD206-positive population as M2.

1 of 1

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Authors
Mohammed, S., Thadathil, N., Selvarani, R., Nicklas, E. H., Wang, D., Miller, B. F., Richardson, A., & Deepa, S. S.
Affiliations
  • OU Health Stephenson Cancer Center (US)
  • Department of Biochemistry and Molecular Biology Oklahoma City OK USA
  • Oklahoma Medical Research Foundation (US)
  • Oklahoma City VA Medical Center (US)
Corresponding author
Deepa, Sathyaseelan S.
Venue
Aging Cell
Publisher
Wiley
Published
2021-11-11
Volume
20
Issue
12
Pages
e13512-e13512
ISSN
  • 1474-9718 (ISSN-L)
  • 1474-9726
OpenAlex
W3213621514
Cited by
192
References
125
Citations by year
2026: 44 · 2025: 39 · 2024: 45 · 2023: 43 · 2022: 19 · 2021: 2
FWCI
9.26
Type
journal article
Language
en
Open access
Locations
  • Aging Cell (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
National Institutes of Health (R01AG059718, R01AG057424)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
  • Health Sciences › Medicine › Hepatology › Liver physiology and pathology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
Keywords
necroptosis, inflammaging, liver aging, chronic liver disease, liver fibrosis, hepatocyte senescence, M1 macrophages, inflammatory cytokines, MLKL phosphorylation, RIPK3, RIPK1, necrostatin-1, hepatocellular carcinoma
MeSH terms
Necroptosis, Aging, Chronic Disease, Fibrosis, Inflammation, Liver

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-10.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-10.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

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