Prosaposin is a biomarker of mesenchymal glioblastoma and regulates mesenchymal transition through the TGF‐β1/Smad signaling pathway

Jiang, Yang; Zhou, Jinpeng; Hou, Dianqi; Luo, Peng; Gao, Huiling; Ma, Yanju; Chen, Yin‐Sheng; Li, Long; Zou, Dan; Zhang, Haiying; Zhang, Ye; Jing, Zhitao

doi:10.1002/path.5278

Title: Prosaposin is a biomarker of mesenchymal glioblastoma and regulates mesenchymal transition through the TGF‐β1/Smad signaling pathway

Abstract

Abstract Mesenchymal glioblastoma (GBM) is the most aggressive subtype of GBM. Our previous study found that neurotrophic factor prosaposin (PSAP) is highly expressed and secreted in glioma and can promote the growth of glioma. The role of PSAP in mesenchymal GBM is still unclear. In this study, bioinformatic analysis, western blotting and RT‐qPCR were used to detect the expression of PSAP in different GBM subtypes. Human glioma cell lines and patient‐derived glioma stem cells were studied in vitro and in vivo , revealing that mesenchymal GBM expressed and secreted the highest level of PSAP among four subtypes of GBM, and PSAP could promote GBM invasion and epithelial–mesenchymal transition (EMT)‐like processes in vivo and in vitro . Bioinformatic analysis and western blotting showed that PSAP mainly played a regulatory role in GBM invasion and EMT‐like processes via the TGF‐β1/Smad signaling pathway. In conclusion, the overexpression and secretion of PSAP may be an important factor causing the high invasiveness of mesenchymal GBM. PSAP is therefore a potential target for the treatment of mesenchymal GBM. © 2019 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd

Authors:

Jiang, Yang ^[1]; Zhou, Jinpeng ^[2]; Hou, Dianqi ^[3]; Luo, Peng ^[2]; Gao, Huiling ^[4]; Ma, Yanju ^[5]; Chen, Yin‐Sheng ^[6]; Li, Long ^[2]; Zou, Dan ^[7]; Zhang, Haiying ^[8]; Zhang, Ye ^[7];

^[2]

Department of Neurosurgery The First Hospital of China Medical University Shenyang City PR China, Department of Neurosurgery Shanghai General Hospital, Shanghai Jiao Tong University School of Medicine Shanghai PR China
Department of Neurosurgery The First Hospital of China Medical University Shenyang City PR China
Department of Neurosurgery Shanghai General Hospital, Shanghai Jiao Tong University School of Medicine Shanghai PR China
College of Life and Health Sciences, Northeastern University Shenyang PR China
Department of Medical Oncology Cancer Hospital of China Medical University Shenyang PR China
Department of Neurosurgery/Neuro‐oncology SunYat‐sen University Cancer Center, State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine Guangzhou PR China
The First laboratory of cancer institute, the First Hospital of China Medical University Shenyang City PR China
International Education College, Liaoning University of Traditional Chinese Medicine Shenyang City PR China

Publication Date:: Tue May 21 00:00:00 EDT 2019

Sponsoring Org.:: USDOE

OSTI Identifier:: 1514753

Resource Type:: Publisher's Accepted Manuscript

Journal Name:: Journal of Pathology

Additional Journal Information:: Journal Name: Journal of Pathology Journal Volume: 249 Journal Issue: 1; Journal ID: ISSN 0022-3417

Publisher:: Wiley Blackwell (John Wiley & Sons)

Country of Publication:: United Kingdom

Language:: English

Citation Formats


                    Jiang, Yang, Zhou, Jinpeng, Hou, Dianqi, Luo, Peng, Gao, Huiling, Ma, Yanju, Chen, Yin‐Sheng, Li, Long, Zou, Dan, Zhang, Haiying, Zhang, Ye, and Jing, Zhitao. Prosaposin is a biomarker of mesenchymal glioblastoma and regulates mesenchymal transition through the TGF‐β1/Smad signaling pathway.  United Kingdom: N. p., 2019. 
Web.  doi:10.1002/path.5278.

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                    Jiang, Yang, Zhou, Jinpeng, Hou, Dianqi, Luo, Peng, Gao, Huiling, Ma, Yanju, Chen, Yin‐Sheng, Li, Long, Zou, Dan, Zhang, Haiying, Zhang, Ye, & Jing, Zhitao. Prosaposin is a biomarker of mesenchymal glioblastoma and regulates mesenchymal transition through the TGF‐β1/Smad signaling pathway.  United Kingdom.  https://doi.org/10.1002/path.5278

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                    Jiang, Yang, Zhou, Jinpeng, Hou, Dianqi, Luo, Peng, Gao, Huiling, Ma, Yanju, Chen, Yin‐Sheng, Li, Long, Zou, Dan, Zhang, Haiying, Zhang, Ye, and Jing, Zhitao. Tue .  
"Prosaposin is a biomarker of mesenchymal glioblastoma and regulates mesenchymal transition through the TGF‐β1/Smad signaling pathway".  United Kingdom.  https://doi.org/10.1002/path.5278.

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@article{osti_1514753,

  title        = {Prosaposin is a biomarker of mesenchymal glioblastoma and regulates mesenchymal transition through the TGF‐β1/Smad signaling pathway},

  author       = {Jiang, Yang and Zhou, Jinpeng and Hou, Dianqi and Luo, Peng and Gao, Huiling and Ma, Yanju and Chen, Yin‐Sheng and Li, Long and Zou, Dan and Zhang, Haiying and Zhang, Ye and Jing, Zhitao},

  abstractNote = {Abstract Mesenchymal glioblastoma (GBM) is the most aggressive subtype of GBM. Our previous study found that neurotrophic factor prosaposin (PSAP) is highly expressed and secreted in glioma and can promote the growth of glioma. The role of PSAP in mesenchymal GBM is still unclear. In this study, bioinformatic analysis, western blotting and RT‐qPCR were used to detect the expression of PSAP in different GBM subtypes. Human glioma cell lines and patient‐derived glioma stem cells were studied in vitro and in vivo , revealing that mesenchymal GBM expressed and secreted the highest level of PSAP among four subtypes of GBM, and PSAP could promote GBM invasion and epithelial–mesenchymal transition (EMT)‐like processes in vivo and in vitro . Bioinformatic analysis and western blotting showed that PSAP mainly played a regulatory role in GBM invasion and EMT‐like processes via the TGF‐β1/Smad signaling pathway. In conclusion, the overexpression and secretion of PSAP may be an important factor causing the high invasiveness of mesenchymal GBM. PSAP is therefore a potential target for the treatment of mesenchymal GBM. © 2019 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd},

  doi          = {10.1002/path.5278},

  journal      = {Journal of Pathology},

  number       = 1,

  volume       = 249,

  place        = {United Kingdom},

  year         = {Tue May 21 00:00:00 EDT 2019},

  month        = {Tue May 21 00:00:00 EDT 2019}

}

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Title: Prosaposin is a biomarker of mesenchymal glioblastoma and regulates mesenchymal transition through the TGF‐β1/Smad signaling pathway

Abstract

Citation Formats

Tumour-infiltrating CD4+ and CD8+ lymphocytes as predictors of clinical outcome in glioma journal, April 2014

MiR-181b suppresses proliferation of and reduces chemoresistance to temozolomide in U87 glioma stem cells journal, November 2010

Prosaposin facilitates sortilin-independent lysosomal trafficking of progranulin journal, September 2015

Hypoxia-Inducible Factors Regulate Tumorigenic Capacity of Glioma Stem Cells journal, June 2009

The MicroRNA-23b/27b/24 Cluster Promotes Breast Cancer Lung Metastasis by Targeting Metastasis-suppressive Gene Prosaposin journal, June 2014

Integrated Genomic Analysis Identifies Clinically Relevant Subtypes of Glioblastoma Characterized by Abnormalities in PDGFRA, IDH1, EGFR, and NF1 journal, January 2010

Prosaposin is a novel androgen-regulated gene in prostate cancer cell line LNCaP journal, January 2007

Stevioside attenuates isoproterenol-induced mouse myocardial fibrosis through inhibition of the myocardial NF-κB/TGF-β1/Smad signaling pathway journal, January 2019

Prosaposin Facilitates Sciatic Nerve Regeneration In Vivo journal, May 1996

Temozolomide sensitizes stem-like cells of glioma spheres to TRAIL-induced apoptosis via upregulation of casitas B-lineage lymphoma (c-Cbl) protein journal, July 2015

GPR56/ADGRG1 Inhibits Mesenchymal Differentiation and Radioresistance in Glioblastoma journal, November 2017

TGF-β promotes glioma cell growth via activating Nodal expression through Smad and ERK1/2 pathways journal, January 2014

HMGB1 induces lung fibroblast to myofibroblast differentiation through NF-κB-mediated TGF-β1 release journal, March 2017

Glioblastoma: new therapeutic strategies to address cellular and genomic complexity journal, December 2017

Protein precipitation of diluted samples in SDS-containing buffer with acetone leads to higher protein recovery and reproducibility in comparison with TCA/acetone approach journal, May 2016

A novel interaction of PAK4 with PPARγ to regulate Nox1 and radiation-induced epithelial-to-mesenchymal transition in glioma journal, May 2017

FAT1 modulates EMT and stemness genes expression in hypoxic glioblastoma: FAT1 as a novel regulator of stemness and EMT in glioblastoma journal, October 2017

Bivalent Chromatin Domains in Glioblastoma Reveal a Subtype-Specific Signature of Glioma Stem Cells journal, March 2018

Identification of prosaposin and transgelin as potential biomarkers for gallbladder cancer using quantitative proteomics journal, April 2014

Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis journal, March 2006

Targeting glioma stem cells through combined BMI1 and EZH2 inhibition journal, October 2017

Sphingolipid activator proteins: proteins with complex functions in lipid degradation and skin biogenesis journal, June 2001

TGF-β-mediated repression of MST1 by DNMT1 promotes glioma malignancy journal, October 2017

Saposins: structure, function, distribution, and molecular genetics. journal, September 1992

Prosaposin is an AR-target gene and its neurotrophic domain upregulates AR expression and activity in prostate stromal cells journal, May 2008

Prosaposin, a regulator of estrogen receptor alpha, promotes breast cancer growth journal, August 2012

Mechano-Signal Transduction in Mesenchymal Stem Cells Induces Prosaposin Secretion to Drive the Proliferation of Breast Cancer Cells journal, September 2017

The protective role of prosaposin and its receptors in the nervous system journal, October 2014

Prosaposin promotes the proliferation and tumorigenesis of glioma through toll-like receptor 4 (TLR4)-mediated NF-κB signaling pathway journal, November 2018

Prosaposin down-modulation decreases metastatic prostate cancer cell adhesion, migration, and invasion journal, January 2010

A multigene predictor of outcome in glioblastoma journal, October 2009

TGF-β1 Induces EMT in Bovine Mammary Epithelial Cells Through the TGFβ1/Smad Signaling Pathway journal, January 2017

Cancer stem cells in glioblastoma journal, June 2015

TGF-β Family Signaling in Tumor Suppression and Cancer Progression journal, February 2017

Development of a prosaposin-derived therapeutic cyclic peptide that targets ovarian cancer via the tumor microenvironment journal, March 2016

ARL2 overexpression inhibits glioma proliferation and tumorigenicity via down-regulating AXL journal, May 2018

S100A4 Is a Biomarker and Regulator of Glioma Stem Cells That Is Critical for Mesenchymal Transition in Glioblastoma journal, August 2017

Autophagy induction impairs migration and invasion by reversing EMT in glioblastoma cells journal, May 2015

Mesenchymal Differentiation Mediated by NF-κB Promotes Radiation Resistance in Glioblastoma journal, September 2013

Prosaposin-derived peptide alleviates ischaemia-induced hearing loss journal, December 2012

TGFβ1 Promotes Gemcitabine Resistance through Regulating the LncRNA-LET/NF90/miR-145 Signaling Axis in Bladder Cancer journal, January 2017

Astilbin Inhibits High Glucose-Induced Inflammation and Extracellular Matrix Accumulation by Suppressing the TLR4/MyD88/NF-κB Pathway in Rat Glomerular Mesangial Cells journal, October 2018

Krüppel-like Transcription Factor KLF10 Suppresses TGFβ-Induced Epithelial-to-Mesenchymal Transition via a Negative Feedback Mechanism journal, March 2017

Serum prosaposin levels are increased in patients with advanced prostate cancer journal, May 2011

Mesenchymal stem cells in breast cancer: response to chemical and mechanical stimuli journal, November 2017

Mesenchymal glioblastoma constitutes a major ceRNA signature in the TGF-β pathway journal, January 2018

Wnt5a Drives an Invasive Phenotype in Human Glioblastoma Stem-like Cells journal, December 2016

TSC22D1 and PSAP predict clinical outcome of tamoxifen treatment in patients with recurrent breast cancer journal, February 2008

Amplification and overexpression of prosaposin in prostate cancer journal, January 2005

Bone Marrow–Derived Gr1 + Cells Can Generate a Metastasis-Resistant Microenvironment Via Induced Secretion of Thrombospondin-1 journal, April 2013

NFAT1-regulated IL6 signalling contributes to aggressive phenotypes of glioma journal, December 2017

Prosaposin activates the androgen receptor and potentiates resistance to endocrine treatment in breast cancer journal, September 2015

TGF-β2 initiates autophagy via Smad and non-Smad pathway to promote glioma cells’ invasion journal, November 2017

Tumour-infiltrating CD4+ and CD8+ lymphocytes as predictors of clinical outcome in glioma
journal, April 2014

MiR-181b suppresses proliferation of and reduces chemoresistance to temozolomide in U87 glioma stem cells
journal, November 2010

Prosaposin facilitates sortilin-independent lysosomal trafficking of progranulin
journal, September 2015

Hypoxia-Inducible Factors Regulate Tumorigenic Capacity of Glioma Stem Cells
journal, June 2009

The MicroRNA-23b/27b/24 Cluster Promotes Breast Cancer Lung Metastasis by Targeting Metastasis-suppressive Gene Prosaposin
journal, June 2014

Integrated Genomic Analysis Identifies Clinically Relevant Subtypes of Glioblastoma Characterized by Abnormalities in PDGFRA, IDH1, EGFR, and NF1
journal, January 2010

Prosaposin is a novel androgen-regulated gene in prostate cancer cell line LNCaP
journal, January 2007

Stevioside attenuates isoproterenol-induced mouse myocardial fibrosis through inhibition of the myocardial NF-κB/TGF-β1/Smad signaling pathway
journal, January 2019

Prosaposin Facilitates Sciatic Nerve Regeneration In Vivo
journal, May 1996

Temozolomide sensitizes stem-like cells of glioma spheres to TRAIL-induced apoptosis via upregulation of casitas B-lineage lymphoma (c-Cbl) protein
journal, July 2015

GPR56/ADGRG1 Inhibits Mesenchymal Differentiation and Radioresistance in Glioblastoma
journal, November 2017

TGF-β promotes glioma cell growth via activating Nodal expression through Smad and ERK1/2 pathways
journal, January 2014

HMGB1 induces lung fibroblast to myofibroblast differentiation through NF-κB-mediated TGF-β1 release
journal, March 2017

Glioblastoma: new therapeutic strategies to address cellular and genomic complexity
journal, December 2017

Protein precipitation of diluted samples in SDS-containing buffer with acetone leads to higher protein recovery and reproducibility in comparison with TCA/acetone approach
journal, May 2016

A novel interaction of PAK4 with PPARγ to regulate Nox1 and radiation-induced epithelial-to-mesenchymal transition in glioma
journal, May 2017

FAT1 modulates EMT and stemness genes expression in hypoxic glioblastoma: FAT1 as a novel regulator of stemness and EMT in glioblastoma
journal, October 2017

Bivalent Chromatin Domains in Glioblastoma Reveal a Subtype-Specific Signature of Glioma Stem Cells
journal, March 2018

Identification of prosaposin and transgelin as potential biomarkers for gallbladder cancer using quantitative proteomics
journal, April 2014

Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis
journal, March 2006

Targeting glioma stem cells through combined BMI1 and EZH2 inhibition
journal, October 2017

Sphingolipid activator proteins: proteins with complex functions in lipid degradation and skin biogenesis
journal, June 2001

TGF-β-mediated repression of MST1 by DNMT1 promotes glioma malignancy
journal, October 2017

Saposins: structure, function, distribution, and molecular genetics.
journal, September 1992

Prosaposin is an AR-target gene and its neurotrophic domain upregulates AR expression and activity in prostate stromal cells
journal, May 2008

Prosaposin, a regulator of estrogen receptor alpha, promotes breast cancer growth
journal, August 2012

Mechano-Signal Transduction in Mesenchymal Stem Cells Induces Prosaposin Secretion to Drive the Proliferation of Breast Cancer Cells
journal, September 2017

The protective role of prosaposin and its receptors in the nervous system
journal, October 2014

Prosaposin promotes the proliferation and tumorigenesis of glioma through toll-like receptor 4 (TLR4)-mediated NF-κB signaling pathway
journal, November 2018

Prosaposin down-modulation decreases metastatic prostate cancer cell adhesion, migration, and invasion
journal, January 2010

A multigene predictor of outcome in glioblastoma
journal, October 2009

TGF-β1 Induces EMT in Bovine Mammary Epithelial Cells Through the TGFβ1/Smad Signaling Pathway
journal, January 2017

Cancer stem cells in glioblastoma
journal, June 2015

TGF-β Family Signaling in Tumor Suppression and Cancer Progression
journal, February 2017

Development of a prosaposin-derived therapeutic cyclic peptide that targets ovarian cancer via the tumor microenvironment
journal, March 2016

ARL2 overexpression inhibits glioma proliferation and tumorigenicity via down-regulating AXL
journal, May 2018

S100A4 Is a Biomarker and Regulator of Glioma Stem Cells That Is Critical for Mesenchymal Transition in Glioblastoma
journal, August 2017

Autophagy induction impairs migration and invasion by reversing EMT in glioblastoma cells
journal, May 2015

Mesenchymal Differentiation Mediated by NF-κB Promotes Radiation Resistance in Glioblastoma
journal, September 2013

Prosaposin-derived peptide alleviates ischaemia-induced hearing loss
journal, December 2012

TGFβ1 Promotes Gemcitabine Resistance through Regulating the LncRNA-LET/NF90/miR-145 Signaling Axis in Bladder Cancer
journal, January 2017

Astilbin Inhibits High Glucose-Induced Inflammation and Extracellular Matrix Accumulation by Suppressing the TLR4/MyD88/NF-κB Pathway in Rat Glomerular Mesangial Cells
journal, October 2018

Krüppel-like Transcription Factor KLF10 Suppresses TGFβ-Induced Epithelial-to-Mesenchymal Transition via a Negative Feedback Mechanism
journal, March 2017

Serum prosaposin levels are increased in patients with advanced prostate cancer
journal, May 2011

Mesenchymal stem cells in breast cancer: response to chemical and mechanical stimuli
journal, November 2017

Mesenchymal glioblastoma constitutes a major ceRNA signature in the TGF-β pathway
journal, January 2018

Wnt5a Drives an Invasive Phenotype in Human Glioblastoma Stem-like Cells
journal, December 2016

TSC22D1 and PSAP predict clinical outcome of tamoxifen treatment in patients with recurrent breast cancer
journal, February 2008

Amplification and overexpression of prosaposin in prostate cancer
journal, January 2005

Bone Marrow–Derived Gr1 ⁺ Cells Can Generate a Metastasis-Resistant Microenvironment Via Induced Secretion of Thrombospondin-1
journal, April 2013

NFAT1-regulated IL6 signalling contributes to aggressive phenotypes of glioma
journal, December 2017

Prosaposin activates the androgen receptor and potentiates resistance to endocrine treatment in breast cancer
journal, September 2015

TGF-β2 initiates autophagy via Smad and non-Smad pathway to promote glioma cells’ invasion
journal, November 2017