Literature DB >> 20051384

Inactivation of the tumour suppressor, PTEN, in smooth muscle promotes a pro-inflammatory phenotype and enhances neointima formation.

Seth B Furgeson1, Peter A Simpson, Insun Park, Vicki Vanputten, Henrick Horita, Christopher D Kontos, Raphael A Nemenoff, Mary C M Weiser-Evans.   

Abstract

AIMS: Phosphatase and tensin homolog (PTEN) is implicated as a negative regulator of vascular smooth muscle cell (SMC) proliferation and injury-induced vascular remodelling. We tested if selective depletion of PTEN only in SMC is sufficient to promote SMC phenotypic modulation, cytokine production, and enhanced neointima formation. METHODS AND
RESULTS: Smooth muscle marker expression and induction of pro-inflammatory cytokines were compared in cultured SMC expressing control or PTEN-specific shRNA. Compared with controls, PTEN-deficient SMC exhibited increased phosphoinositide 3-kinase (PI3K)/protein kinase B (Akt)/mammalian target of rapamycin (mTOR) signalling and nuclear factor kappa-light-chain-enhancer of activated B cells (NF-kappaB) activity, reduced expression of SM markers (SM-alpha-actin and calponin), and increased production of stromal cell-derived factor-1alpha (SDF-1alpha), monocyte chemotactic protein-1 (MCP-1), interleukin-6 (IL-6), and chemokine (C-X-C motif) ligand 1 (KC/CXCL1) under basal conditions. PI3K/Akt or mTOR inhibition reversed repression of SM marker expression, whereas PI3K/Akt or NF-kappaB inhibition blocked cytokine induction mediated by PTEN depletion. Carotid ligation in mice with genetic reduction of PTEN specifically in SMC (SMC-specific PTEN heterozygotes) resulted in enhanced neointima formation, increased SMC hyperplasia, reduced SM-alpha-actin and calponin expression, and increased NF-kappaB and cytokine expression compared with wild-types. Lesion formation in SMC-specific heterozygotes was similar to lesion formation in global PTEN heterozygotes, indicating that inactivation of PTEN exclusively in SMC is sufficient to induce considerable increases in neointima formation.
CONCLUSION: PTEN activation specifically in SMC is a common upstream regulator of multiple downstream events involved in pathological vascular remodelling, including proliferation, de-differentiation, and production of multiple cytokines.

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Year:  2010        PMID: 20051384      PMCID: PMC2856191          DOI: 10.1093/cvr/cvp425

Source DB:  PubMed          Journal:  Cardiovasc Res        ISSN: 0008-6363            Impact factor:   10.787


  45 in total

1.  Platelet-derived growth factor-BB-mediated activation of Akt suppresses smooth muscle-specific gene expression through inhibition of mitogen-activated protein kinase and redistribution of serum response factor.

Authors:  Nihal Kaplan-Albuquerque; Chrystelle Garat; Christina Desseva; Peter L Jones; Raphael A Nemenoff
Journal:  J Biol Chem       Date:  2003-07-25       Impact factor: 5.157

2.  Crucial role of stromal cell-derived factor-1alpha in neointima formation after vascular injury in apolipoprotein E-deficient mice.

Authors:  Andreas Schober; Sandra Knarren; Michael Lietz; Elisa A Lin; Christian Weber
Journal:  Circulation       Date:  2003-10-27       Impact factor: 29.690

3.  Unique, highly proliferative growth phenotype expressed by embryonic and neointimal smooth muscle cells is driven by constitutive Akt, mTOR, and p70S6K signaling and is actively repressed by PTEN.

Authors:  Peter M Mourani; Pamela J Garl; Janet M Wenzlau; Todd C Carpenter; Kurt R Stenmark; Mary C M Weiser-Evans
Journal:  Circulation       Date:  2004-03-01       Impact factor: 29.690

4.  Neointimal smooth muscle cells display a proinflammatory phenotype resulting in increased leukocyte recruitment mediated by P-selectin and chemokines.

Authors:  Ute Zeiffer; Andreas Schober; Michael Lietz; Elisa A Liehn; Wolfgang Erl; Neil Emans; Zhong-qun Yan; Christian Weber
Journal:  Circ Res       Date:  2004-02-12       Impact factor: 17.367

5.  Strain-dependent vascular remodeling phenotypes in inbred mice.

Authors:  K J Harmon; L L Couper; V Lindner
Journal:  Am J Pathol       Date:  2000-05       Impact factor: 4.307

6.  The mTOR/p70 S6K1 pathway regulates vascular smooth muscle cell differentiation.

Authors:  Kathleen A Martin; Eva M Rzucidlo; Bethany L Merenick; Diane C Fingar; David J Brown; Robert J Wagner; Richard J Powell
Journal:  Am J Physiol Cell Physiol       Date:  2003-10-30       Impact factor: 4.249

7.  Regulation of monocyte chemoattractant protein-1 by the oxidized lipid, 13-hydroperoxyoctadecadienoic acid, in vascular smooth muscle cells via nuclear factor-kappa B (NF-kappa B).

Authors:  Roopashree S Dwarakanath; Saurabh Sahar; Marpadga A Reddy; Daniela Castanotto; John J Rossi; Rama Natarajan
Journal:  J Mol Cell Cardiol       Date:  2004-04       Impact factor: 5.000

8.  Perlecan-induced suppression of smooth muscle cell proliferation is mediated through increased activity of the tumor suppressor PTEN.

Authors:  Pamela J Garl; Janet M Wenzlau; Heather A Walker; John M Whitelock; Mercedes Costell; Mary C M Weiser-Evans
Journal:  Circ Res       Date:  2003-12-01       Impact factor: 17.367

9.  Regulation of SM22 alpha expression by arginine vasopressin and PDGF-BB in vascular smooth muscle cells.

Authors:  Nihal Kaplan-Albuquerque; Chrystelle Garat; Vicki Van Putten; Raphael A Nemenoff
Journal:  Am J Physiol Heart Circ Physiol       Date:  2003-06-26       Impact factor: 4.733

Review 10.  Nuclear factor kappaB: a potential therapeutic target in atherosclerosis and thrombosis.

Authors:  Claudia Monaco; Ewa Paleolog
Journal:  Cardiovasc Res       Date:  2004-03-01       Impact factor: 10.787

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  39 in total

Review 1.  LKB1 signaling in advancing cell differentiation.

Authors:  Lina Udd; Tomi P Mäkelä
Journal:  Fam Cancer       Date:  2011-09       Impact factor: 2.375

2.  Immune modulation of vascular resident cells by Axl orchestrates carotid intima-media thickening.

Authors:  Janice Gerloff; Vyacheslav A Korshunov
Journal:  Am J Pathol       Date:  2012-05       Impact factor: 4.307

3.  PTEN hamartoma of soft tissue: a distinctive lesion in PTEN syndromes.

Authors:  Kyle C Kurek; Emily Howard; L B Tennant; Joseph Upton; Ahmad I Alomari; Patricia E Burrows; Kim Chalache; David J Harris; Cameron C Trenor; Charis Eng; Steven J Fishman; John B Mulliken; Antonio R Perez-Atayde; Harry P W Kozakewich
Journal:  Am J Surg Pathol       Date:  2012-05       Impact factor: 6.394

4.  Ca2+/calmodulin-dependent protein kinase II-γ (CaMKIIγ) negatively regulates vascular smooth muscle cell proliferation and vascular remodeling.

Authors:  Fatima Z Saddouk; Li-Yan Sun; Yong Feng Liu; Miao Jiang; Diane V Singer; Johannes Backs; Dee Van Riper; Roman Ginnan; John J Schwarz; Harold A Singer
Journal:  FASEB J       Date:  2015-11-13       Impact factor: 5.191

5.  TRPV1 attenuates intracranial arteriole remodeling through inhibiting VSMC phenotypic modulation in hypertension.

Authors:  Ming-Jie Zhang; Yun Liu; Zi-Cheng Hu; Yi Zhou; Yan Pi; Lu Guo; Xu Wang; Xue Chen; Jing-Cheng Li; Li-Li Zhang
Journal:  Histochem Cell Biol       Date:  2016-10-24       Impact factor: 4.304

6.  Integrative Analysis of miRNA and inflammatory gene expression after acute particulate matter exposure.

Authors:  Valeria Motta; Laura Angelici; Francesco Nordio; Valentina Bollati; Serena Fossati; Fabio Frascati; Valentina Tinaglia; Pier Alberto Bertazzi; Cristina Battaglia; Andrea A Baccarelli
Journal:  Toxicol Sci       Date:  2013-01-28       Impact factor: 4.849

7.  Serum response factor regulates expression of phosphatase and tensin homolog through a microRNA network in vascular smooth muscle cells.

Authors:  Henrick N Horita; Peter A Simpson; Allison Ostriker; Seth Furgeson; Vicki Van Putten; Mary C M Weiser-Evans; Raphael A Nemenoff
Journal:  Arterioscler Thromb Vasc Biol       Date:  2011-09-22       Impact factor: 8.311

8.  Small RNA sequencing reveals microRNAs that modulate angiotensin II effects in vascular smooth muscle cells.

Authors:  Wen Jin; Marpadga A Reddy; Zhuo Chen; Sumanth Putta; Linda Lanting; Mitsuo Kato; Jung Tak Park; Manasa Chandra; Charles Wang; Rajendra K Tangirala; Rama Natarajan
Journal:  J Biol Chem       Date:  2012-03-19       Impact factor: 5.157

9.  PTEN deletion drives aberrations of DNA methylome and transcriptome in different stages of prostate cancer.

Authors:  Chao Wang; Yaping Feng; Chengyue Zhang; David Cheng; Renyi Wu; Yuqing Yang; Davit Sargsyan; Dibyendu Kumar; Ah-Ng Kong
Journal:  FASEB J       Date:  2019-11-29       Impact factor: 5.191

10.  Pulmonary hypertension secondary to left-heart failure involves peroxynitrite-induced downregulation of PTEN in the lung.

Authors:  Yazhini Ravi; Karuppaiyah Selvendiran; Shan K Naidu; Sarath Meduru; Lucas A Citro; Balázs Bognár; Mahmood Khan; Tamás Kálai; Kálmán Hideg; Periannan Kuppusamy; Chittoor B Sai-Sudhakar
Journal:  Hypertension       Date:  2013-01-21       Impact factor: 10.190

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