Cytotoxicity of TNFα is regulated by integrin‐mediated matrix signaling
Open accessAbstract
Cytokines of the tumor necrosis factor (TNF) family regulate inflammation and immunity, and a subset of this family can also induce cell death in a context-dependent manner. Although TNFalpha is cytotoxic to certain tumor cell lines, it induces apoptosis in normal cells only when NFkappaB signaling is blocked. Here we show that the matricellular protein CCN1/CYR61 can unmask the cytotoxic potential of TNFalpha without perturbation of NFkappaB signaling or de novo protein synthesis, leading to rapid apoptosis in the otherwise resistant primary human fibroblasts. CCN1 acts through binding to integrins alpha(v)beta(5), alpha(6)beta(1), and syndecan-4, triggering the generation of reactive oxygen species (ROS) through a Rac1-dependent mechanism via 5-lipoxygenase and the mitochondria, leading to the biphasic activation of JNK necessary for apoptosis. Mice with the genomic Ccn1 locus replaced with an apoptosis-defective Ccn1 allele are substantially resistant to TNFalpha-induced apoptosis in vivo. These results indicate that CCN1 may act as a physiologic regulator of TNFalpha cytotoxicity, providing the contextual cues from the extracellular matrix for TNFalpha-mediated cell death.
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Ccn1DM/DM mice were backcrossed to C57BL/6 more than 20 times.
“Ccn1DM/DM mice were developed in our laboratory and backcrossed to C57BL/6 (The Jackson Laboratory) more than 20 times (82).”
From Senescent hepatic stellate cells promote liver regeneration through IL-6 and ligands of CXCR2 (2022) · cites this paper as [82]
The “Generation of Ccn1 dm/dm mice and apoptosis in vivo” section describes producing the mice using C57/BL6 blastocysts and intercrossing germline chimeras. It does not report backcrossing them to C57BL/6, let alone doing so more than 20 times; searches for the backcross count and genetic background found no supporting passage. Page numbers are unavailable in our copy. (LLM, conf=0.86)
Experimental — accuracy not yet measuredCCN1's ability to cause robust and sustained reactive oxygen species accumulation underlies some of its unique activities as a matrix cell-adhesion molecule.
“The ability of CCN1 to trigger the accumulation of a robust and sustained level of reactive oxygen species underlies some of its unique activities as a matrix cell-adhesion molecule.”
From CCN1/CYR61: the very model of a modern matricellular protein (2011) · cites this paper as [62]
CCN1 binds HSPGs with high affinity, which serve as co-receptors with integrins in some contexts; syndecan-4 is the critical HSPG for CCN1 functions where examined.
“CCN1 binds HSPGs with high affinity, which serve as co-receptors with integrins in some contexts [13,55]. Where examined, syndecan-4 has been identified as the HSPG critical for CCN1 functions [61,62].”
From CCN1/CYR61: the very model of a modern matricellular protein (2011) · cites this paper as [62]
CCN1's synergism with TNFα requires interaction with both αvβ5 and α6β1; mutants defective for either binding are incapable of functional synergism, but combining the two mutants reconstitutes wild-type activity.
“However, the synergism of CCN1 with TNFα (see below) requires its interaction with both αvβ5 and α6β1. Interestingly, whereas CCN1 mutants defective for either binding αvβ5 or α6β1 are each incapably of functional synergism with TNFα, a combination of these two mutants can fully reconstitute wild-type activity [62].”
From CCN1/CYR61: the very model of a modern matricellular protein (2011) · cites this paper as [62]
Cell adhesion to CCN1 enables TNF-α to induce apoptosis without inhibiting NF-κB signaling or de novo protein synthesis, converting TNF-α from a survival-enhancing factor into a potent apoptotic agent.
“Remarkably, cell adhesion to CCN1 enables TNF-α to induce apoptosis without inhibiting NF-κB signaling or de novo protein synthesis, thus converting TNF-α from a survival-enhancing factor into a potent apoptotic agent [62].”
From CCN1/CYR61: the very model of a modern matricellular protein (2011) · cites this paper as [62]
Although CCN1 is a cell-adhesion molecule, these activities are observed when CCN1 is presented to cells either as an adhesion substrate or as a soluble factor.
“Although CCN1 is a cell-adhesion molecule, these activities are observed when CCN1 is presented to cells either as an adhesion substrate or as a soluble factor.”
From CCN1/CYR61: the very model of a modern matricellular protein (2011) · cites this paper as [62]
Mechanistically, CCN1 acts by binding integrins α6β1, αvβ5 and syndecan-4, leading to generation of reactive oxygen species via 5-lipoxygenase and mitochondria.
“Mechanistically, CCN1 acts by binding integrins α6β1, αvβ5 and syndecan-4, leading to the generation of reactive oxygen species (ROS) via 5-lipoxygenase and mitochondria (Fig. 2) [62].”
From CCN1/CYR61: the very model of a modern matricellular protein (2011) · cites this paper as [62]
Dermal apoptosis induced upon direct subcutaneous injection of TNF-α is also substantially reduced in Ccn1dm/dm mice compared with wild-type mice.
“Dermal apoptosis induced upon direct subcutaneous injection of TNF-α is also substantially reduced in Ccn1dm/dm mice compared with wild-type mice.”
From CCN1/CYR61: the very model of a modern matricellular protein (2011) · cites this paper as [62]
The importance of CCN1 in TNF-α- and FasL-induced apoptosis in vivo has been demonstrated using knockin mice (Ccn1dm/dm) in which the genomic Ccn1 locus has been replaced by an apoptosis-defective Ccn1 allele with mutations at the α6β1-HSPG-binding sites.
“The importance of CCN1 in TNF-α- and FasL-induced apoptosis in vivo has been demonstrated using knockin mice (Ccn1dm/dm) in which the genomic Ccn1 locus has been replaced by an apoptosis-defective Ccn1 allele with mutations at the α6β1–HSPG-binding sites [62,101,106].”
From CCN1/CYR61: the very model of a modern matricellular protein (2011) · cites this paper as [62]
In each of these experimental models for TNF-α- or Fas-mediated apoptosis, Ccn1dm/dm mice consistently show a >60% reduction in apoptosis compared with wild-type mice.
“In each of these experimental models for TNF-α- or Fas-mediated apoptosis, Ccn1dm/dm mice consistently show a >60% reduction in apoptosis compared with wild-type mice [62,106].”
From CCN1/CYR61: the very model of a modern matricellular protein (2011) · cites this paper as [62]
In contrast to the embryonic lethality of Ccn1-null mice, these knockin mice are viable, fertile, and do not exhibit any obvious developmental defects.
“In contrast to the embryonic lethality of Ccn1-null mice, these knockin mice are viable, fertile, and do not exhibit any obvious developmental defects.”
From CCN1/CYR61: the very model of a modern matricellular protein (2011) · cites this paper as [62]
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Self-citation
- Authors
- Chen, C., Young, J. L., Monzon, R. I., Chen, N., Todorović, V., & Lau, L. F.
- Affiliations
- University of Illinois Chicago (US)
- Corresponding author
- Lau, Lester F
- Venue
- The EMBO Journal
- Published
- 2007-02-22
- Volume
- 26
- Issue
- 5
- Pages
- 1257-1267
- ISSN
- 0261-4189 (ISSN-L)
- 1460-2075
- PMC
- PMC1817641
- OpenAlex
- W2132681046
- Cited by
- 143
- References
- 52
- Citations by year
- 2026: 2 · 2025: 7 · 2023: 1 · 2022: 5 · 2021: 8 · 2020: 16 · 2019: 4 · 2018: 5 · 2017: 3 · 2016: 12 · 2015: 10 · 2014: 12 · 2013: 6 · 2012: 10
- FWCI
- 4.76
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- The EMBO Journal (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- American Heart Association (T32 HL07829)
- National Institutes of Health (T32 HL07829)
- National Heart, Lung, and Blood Institute (T32 HL-07829, T32HL007829)
- National Cancer Institute (R01CA046565, CA-46565)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Connective Tissue Growth Factor Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Signaling Pathways in Disease
- Keywords
- TNF-α, integrin signaling, extracellular matrix, apoptosis, fibroblasts, reactive oxygen species, Rac1, 5-lipoxygenase, JNK activation, NF-κB, syndecan-4, tumor necrosis factor family
- MeSH terms
- Animals, Cells, Cultured, Fibroblasts, Humans, Infant, Newborn, Models, Biological, Mutation, Tumor Necrosis Factor-alpha, Signal Transduction, Integrins, NF-kappa B, Apoptosis, Reactive Oxygen Species, Immediate-Early Proteins, Mice, Knockout, NADPH Oxidases, RNA, Small Interfering, JNK Mitogen-Activated Protein Kinases, Mice, Caspase 3, Cysteine-Rich Protein 61
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.
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.
What counts as a claim ›How we measure confidence ›How we check this ›
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