RGS5–TGFβ–Smad2/3 axis switches pro- to anti-apoptotic signaling in tumor-residing pericytes, assisting tumor growth

Regulator-of-G-protein-signaling-5 (RGS5), a pro-apoptotic/anti-proliferative protein, is a signature molecule of tumor-associated pericytes, highly expressed in several cancers, and is associated with tumor growth and poor prognosis. Surprisingly, despite the negative influence of intrinsic RGS5 ex...

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Published inCell death and differentiation Vol. 28; no. 11; pp. 3052 - 3076
Main Authors Dasgupta, Shayani, Ghosh, Tithi, Dhar, Jesmita, Bhuniya, Avishek, Nandi, Partha, Das, Arnab, Saha, Akata, Das, Juhina, Guha, Ipsita, Banerjee, Saptak, Chakravarti, Mohona, Dasgupta, Partha Sarathi, Alam, Neyaz, Chakrabarti, Jayanta, Majumdar, Subrata, Chakrabarti, Pinak, Storkus, Walter J., Baral, Rathindranath, Bose, Anamika
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.11.2021
Nature Publishing Group
Subjects
1-Phosphatidylinositol 3-kinase
13/1
13/109
13/2
13/21
13/31
13/51
13/89
13/95
14
631/67/2328
631/67/327
96/100
AKT protein
Animals
Apoptosis
Bax protein
Biochemistry
Biomedical and Life Sciences
Caspase
Cell Biology
Cell Cycle Analysis
Female
G protein-coupled receptors
Growth regulators
Humans
Life Sciences
Medical prognosis
Mice
Mitochondria
Neoplasms - genetics
p53 Protein
Pericytes
Pericytes - metabolism
RGS Proteins - metabolism
Signal Transduction
Smad2 protein
Smad2 Protein - metabolism
Smad4 protein
Stem Cells
Transfection
Tumor microenvironment
Tumors
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Abstract Regulator-of-G-protein-signaling-5 (RGS5), a pro-apoptotic/anti-proliferative protein, is a signature molecule of tumor-associated pericytes, highly expressed in several cancers, and is associated with tumor growth and poor prognosis. Surprisingly, despite the negative influence of intrinsic RGS5 expression on pericyte survival, RGS5 high pericytes accumulate in progressively growing tumors. However, responsible factor(s) and altered-pathway(s) are yet to report. RGS5 binds with Gαi/q and promotes pericyte apoptosis in vitro, subsequently blocking GPCR-downstream PI3K-AKT signaling leading to Bcl2 downregulation and promotion of PUMA-p53-Bax-mediated mitochondrial damage. However, within tumor microenvironment (TME), TGFβ appeared to limit the cytocidal action of RGS5 in tumor-residing RGS5 high pericytes. We observed that in the presence of high RGS5 concentrations, TGFβ–TGFβR interactions in the tumor-associated pericytes lead to the promotion of pSmad2–RGS5 binding and nuclear trafficking of RGS5, which coordinately suppressed RGS5–Gαi/q and pSmad2/3–Smad4 pairing. The RGS5–TGFβ–pSmad2 axis thus mitigates both RGS5- and TGFβ-dependent cellular apoptosis, resulting in sustained pericyte survival/expansion within the TME by rescuing PI3K-AKT signaling and preventing mitochondrial damage and caspase activation. This study reports a novel mechanism by which TGFβ fortifies and promotes survival of tumor pericytes by switching pro- to anti-apoptotic RGS5 signaling in TME. Understanding this altered RGS5 signaling might prove beneficial in designing future cancer therapy.
AbstractList Regulator-of-G-protein-signaling-5 (RGS5), a pro-apoptotic/anti-proliferative protein, is a signature molecule of tumor-associated pericytes, highly expressed in several cancers, and is associated with tumor growth and poor prognosis. Surprisingly, despite the negative influence of intrinsic RGS5 expression on pericyte survival, RGS5highpericytes accumulate in progressively growing tumors. However, responsible factor(s) and altered-pathway(s) are yet to report. RGS5 binds with Gαi/q and promotes pericyte apoptosis in vitro, subsequently blocking GPCR-downstream PI3K-AKT signaling leading to Bcl2 downregulation and promotion of PUMA-p53-Bax-mediated mitochondrial damage. However, within tumor microenvironment (TME), TGFβ appeared to limit the cytocidal action of RGS5 in tumor-residing RGS5highpericytes. We observed that in the presence of high RGS5 concentrations, TGFβ–TGFβR interactions in the tumor-associated pericytes lead to the promotion of pSmad2–RGS5 binding and nuclear trafficking of RGS5, which coordinately suppressed RGS5–Gαi/q and pSmad2/3–Smad4 pairing. The RGS5–TGFβ–pSmad2 axis thus mitigates both RGS5- and TGFβ-dependent cellular apoptosis, resulting in sustained pericyte survival/expansion within the TME by rescuing PI3K-AKT signaling and preventing mitochondrial damage and caspase activation. This study reports a novel mechanism by which TGFβ fortifies and promotes survival of tumor pericytes by switching pro- to anti-apoptotic RGS5 signaling in TME. Understanding this altered RGS5 signaling might prove beneficial in designing future cancer therapy.
Regulator-of-G-protein-signaling-5 (RGS5), a pro-apoptotic/anti-proliferative protein, is a signature molecule of tumor-associated pericytes, highly expressed in several cancers, and is associated with tumor growth and poor prognosis. Surprisingly, despite the negative influence of intrinsic RGS5 expression on pericyte survival, RGS5 pericytes accumulate in progressively growing tumors. However, responsible factor(s) and altered-pathway(s) are yet to report. RGS5 binds with Gαi/q and promotes pericyte apoptosis in vitro, subsequently blocking GPCR-downstream PI3K-AKT signaling leading to Bcl2 downregulation and promotion of PUMA-p53-Bax-mediated mitochondrial damage. However, within tumor microenvironment (TME), TGFβ appeared to limit the cytocidal action of RGS5 in tumor-residing RGS5 pericytes. We observed that in the presence of high RGS5 concentrations, TGFβ-TGFβR interactions in the tumor-associated pericytes lead to the promotion of pSmad2-RGS5 binding and nuclear trafficking of RGS5, which coordinately suppressed RGS5-Gαi/q and pSmad2/3-Smad4 pairing. The RGS5-TGFβ-pSmad2 axis thus mitigates both RGS5- and TGFβ-dependent cellular apoptosis, resulting in sustained pericyte survival/expansion within the TME by rescuing PI3K-AKT signaling and preventing mitochondrial damage and caspase activation. This study reports a novel mechanism by which TGFβ fortifies and promotes survival of tumor pericytes by switching pro- to anti-apoptotic RGS5 signaling in TME. Understanding this altered RGS5 signaling might prove beneficial in designing future cancer therapy.
Regulator-of-G-protein-signaling-5 (RGS5), a pro-apoptotic/anti-proliferative protein, is a signature molecule of tumor-associated pericytes, highly expressed in several cancers, and is associated with tumor growth and poor prognosis. Surprisingly, despite the negative influence of intrinsic RGS5 expression on pericyte survival, RGS5 high pericytes accumulate in progressively growing tumors. However, responsible factor(s) and altered-pathway(s) are yet to report. RGS5 binds with Gαi/q and promotes pericyte apoptosis in vitro, subsequently blocking GPCR-downstream PI3K-AKT signaling leading to Bcl2 downregulation and promotion of PUMA-p53-Bax-mediated mitochondrial damage. However, within tumor microenvironment (TME), TGFβ appeared to limit the cytocidal action of RGS5 in tumor-residing RGS5 high pericytes. We observed that in the presence of high RGS5 concentrations, TGFβ–TGFβR interactions in the tumor-associated pericytes lead to the promotion of pSmad2–RGS5 binding and nuclear trafficking of RGS5, which coordinately suppressed RGS5–Gαi/q and pSmad2/3–Smad4 pairing. The RGS5–TGFβ–pSmad2 axis thus mitigates both RGS5- and TGFβ-dependent cellular apoptosis, resulting in sustained pericyte survival/expansion within the TME by rescuing PI3K-AKT signaling and preventing mitochondrial damage and caspase activation. This study reports a novel mechanism by which TGFβ fortifies and promotes survival of tumor pericytes by switching pro- to anti-apoptotic RGS5 signaling in TME. Understanding this altered RGS5 signaling might prove beneficial in designing future cancer therapy.
Author Bhuniya, Avishek
Saha, Akata
Baral, Rathindranath
Majumdar, Subrata
Nandi, Partha
Chakravarti, Mohona
Storkus, Walter J.
Banerjee, Saptak
Chakrabarti, Jayanta
Bose, Anamika
Dhar, Jesmita
Alam, Neyaz
Dasgupta, Partha Sarathi
Chakrabarti, Pinak
Ghosh, Tithi
Dasgupta, Shayani
Das, Arnab
Das, Juhina
Guha, Ipsita
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/34012071$$D View this record in MEDLINE/PubMed
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Copyright The Author(s), under exclusive licence to ADMC Associazione Differenziamento e Morte Cellulare 2021
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The Author(s), under exclusive licence to ADMC Associazione Differenziamento e Morte Cellulare 2021.
Copyright_xml – notice: The Author(s), under exclusive licence to ADMC Associazione Differenziamento e Morte Cellulare 2021
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PublicationSubtitle Official journal of the ADMC Associazione Differenziamento e Morte Cellulare
PublicationTitle Cell death and differentiation
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Snippet Regulator-of-G-protein-signaling-5 (RGS5), a pro-apoptotic/anti-proliferative protein, is a signature molecule of tumor-associated pericytes, highly expressed...
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AKT protein
Animals
Apoptosis
Bax protein
Biochemistry
Biomedical and Life Sciences
Caspase
Cell Biology
Cell Cycle Analysis
Female
G protein-coupled receptors
Growth regulators
Humans
Life Sciences
Medical prognosis
Mice
Mitochondria
Neoplasms - genetics
p53 Protein
Pericytes
Pericytes - metabolism
RGS Proteins - metabolism
Signal Transduction
Smad2 protein
Smad2 Protein - metabolism
Smad4 protein
Stem Cells
Transfection
Tumor microenvironment
Tumors
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Title RGS5–TGFβ–Smad2/3 axis switches pro- to anti-apoptotic signaling in tumor-residing pericytes, assisting tumor growth
URI https://link.springer.com/article/10.1038/s41418-021-00801-3
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Volume 28
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