The prolyl isomerase Pin1 regulates the NF-κB signaling pathway and interleukin-8 expression in glioblastoma

Atkinson, G P; Nozell, S E; Harrison, D K; Stonecypher, M S; Chen, D; Benveniste, E N

doi:10.1038/onc.2009.232

Cited by 75Signaling Pathways in DiseaseGlioma Diagnosis and TreatmentNF-κB Signaling Pathways

The prolyl isomerase Pin1 regulates the NF-κB signaling pathway and interleukin-8 expression in glioblastoma

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Atkinson, G P, Nozell, S E, Harrison, D K, Stonecypher, M S, Chen, D, Benveniste, E N·2009·Oncogene

DOI 10.1038/onc.2009.232PMC PMC5987556

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Abstract

The brain tumor glioblastoma (GBM) remains one of the most aggressive and devastating tumors despite decades of effort to find more effective treatments. A hallmark of GBM is the constitutive activation of the nuclear factor kappa-light-chain-enhancer of activated B cells (NF-kappaB) signaling pathway, which regulates cell proliferation, inflammation, migration and apoptosis. The prolyl isomerase, Pin1, has been found to bind directly to the NF-kappaB protein, p65, and cause increases in NF-kappaB promoter activity in a breast cancer model. We now present evidence that this interaction occurs in GBM and that it has important consequences on NF-kappaB signaling. We demonstrate that Pin1 levels are enhanced in primary GBM tissues compared with controls, and that this difference in Pin1 expression affects the migratory capacity of GBM-derived cells. Pin1 knockdown decreases the amount of activated, phosphorylated p65 in the nucleus, resulting in inhibition of the transcriptional program of the IL-8 gene. Through the use of microarray, we also observed changes in the expression levels of other NF-kappaB regulated genes due to Pin1 knockdown. Taken together, these data suggest that Pin1 is an important regulator of NF-kappaB in GBM, and support the notion of using Pin1 as a therapeutic target in the future.

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Pin1 regulates the functions of transcription factors NFAT, STAT3, and NF-κB that play important roles in the immune system.
“It has been reported that Pin1 regulates the functions of transcription factors, such as NFAT [2], STAT3 [3], and NF-κB [4] that play important roles in the immune system.”
From Prolyl Isomerase Pin1 Protects Mice from Endotoxin Shock (2011) · cites this paper as [4]

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PIN1 Inhibition Suppresses Osteoclast Differentiation and Inflammatory Responses
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Regulation of mitochondrial apoptosis by Pin1 in cancer and neurodegeneration
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Regulation of AU-Rich Element RNA Binding Proteins by Phosphorylation and the Prolyl Isomerase Pin1
Shen, Z.-J., & Malter, J. S. (2015) · Biomolecules · doi:10.3390/biom5020412 · Cited by 36 · see citing works
Roles of Pin1 as a Key Molecule for EMT Induction by Activation of STAT3 and NF-κB in Human Gallbladder Cancer
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Role of Pin1 Protein in the Pathogenesis of Nonalcoholic Steatohepatitis in a Rodent Model
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Targeting Pin1 for Modulation of Cell Motility and Cancer Therapy
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Downregulation of microRNA-370 in esophageal squamous-cell carcinoma is associated with cancer progression and promotes cancer cell proliferation via upregulating PIN1
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Roles of peptidyl-prolyl isomerase Pin1 in disease pathogenesis
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Pin1 and Alzheimer's disease
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Sensitizing effect of juglone is mediated by down regulation of Notch1 signaling pathway in trastuzumab-resistant SKBR3 cells
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Pinning Down the Transcription: A Role for Peptidyl-Prolyl cis-trans Isomerase Pin1 in Gene Expression
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Prolyl Isomerase Pin1 Protects Mice from Endotoxin Shock
Akiyama, H., Misawa, T., Ono, M., Uchida, C., & Uchida, T. (2011) · PLoS ONE · doi:10.1371/journal.pone.0014656 · Cited by 17 · see citing works
“It has been reported that Pin1 regulates the functions of transcription factors, such as NFAT [2], STAT3 [3], and NF-kB [4] that play important roles in the immune system.”
Background
Association between PIN1 promoter polymorphisms and risk of nasopharyngeal carcinoma
Lü, Y., Huang, G., Pu, X.-X., He, Y.-X., Li, B.-B., Liu, X., Dong, Z., & He, Z. (2012) · Molecular Biology Reports · doi:10.1007/s11033-012-2454-6 · Cited by 17 · see citing works
Pin1 Plays Essential Roles in NASH Development by Modulating Multiple Target Proteins
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Peptidyl-prolyl isomerase Pin1 deficiency attenuates angiotensin II-induced abdominal aortic aneurysm formation in ApoE−/− mice
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Cytoplasmic Pin1 expression is correlated with poor prognosis in colorectal cancer
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Chronic Inflammation Pathway NF-κB Cooperates with Epigenetic Reprogramming to Drive the Malignant Progression of Glioblastoma
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The Multiple Roles of Peptidyl Prolyl Isomerases in Brain Cancer
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Prolyl isomerase Pin1 promotes extracellular matrix production in hepatic stellate cells through regulating formation of the Smad3-TAZ complex
Aoyama, S., Kido, Y., Kanamoto, M., Naito, M., Nakanishi, M., Kanna, M., Yamamotoya, T., Asano, T., & Nakatsu, Y. (2023) · Experimental Cell Research · doi:10.1016/j.yexcr.2023.113544 · Cited by 11 · see citing works
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Metabolic Management of Cancer
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Loss of Pin1 Suppresses Hedgehog-Driven Medulloblastoma Tumorigenesis
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Design and Synthesis of Oligopeptidic Parvulin Inhibitors
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Targeting Pin1 to overcome immunosuppressive tumor microenvironment in MSS colorectal cancer
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Self-citation
The −842G/C Polymorphisms of PIN1 Contributes to Cancer Risk: A Meta-Analysis of 10 Case-Control Studies
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The proline isomerase Pin1 inhibitors PiB and juglone protect rats against lipopolysaccharide-induced respiratory inflammation
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The expression of prolyl isomerase Pin1 is expanded in the skin of patients with atopic dermatitis and facilitates IL ‐33 expression in HaCaT cells
Kanamoto, M., Takahagi, S., Aoyama, S., Kido, Y., Nakanishi, M., Naito, M., Kanna, M., Yamamotoya, T., Tanaka, A., Hide, M., et al. (2022) · The Journal of Dermatology · doi:10.1111/1346-8138.16633 · Cited by 2 · see citing works
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Pin1 as a Central Modulator of Wnt/β-Catenin Signaling in Pulmonary Fibrosis: Interplay with EBV-LMP1 and Therapeutic Implications
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Investigating hyperactive NF-κB in glioma progression
Jeong, J. (2026) · Scholarship@Western (Western University)
Targeting The Peptidyl-Prolyl Isomerase Pin1 in Glioblastoma
Stewart, R. C. (2025) · Scholarship@Western (Western University)
Knockdown of Pin1 leads to reduced angiogenic potential and tumorigenicity in glioblastoma cells
Atabay, K. D., Yıldız, M. T., Avşar, T., Karabay, A., & Kılıç, T. (2015) · Oncology Letters · doi:10.3892/ol.2015.3512 · Cited by 6 · see citing works
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Authors: Atkinson, G. P., Nozell, S. E., Harrison, D. K., Stonecypher, M. S., Chen, D., & Benveniste, E. N.
Affiliations: University of Alabama at Birmingham (US)
Corresponding author: Benveniste, E N
ORCID: Nozell, S E
Harrison, D K
Stonecypher, M S
Benveniste, E N
Venue: Oncogene
Publisher: Springer Science and Business Media LLC
Published: 2009-08-10
Volume: 28
Issue: 42
Pages: 3735-3745
ISSN: 0950-9232 (ISSN-L)
1476-5594
DOI: 10.1038/onc.2009.232
PMC: PMC5987556
OpenAlex: W2092950531
Cited by: 75
References: 55
Citations by year: 2026: 1 · 2025: 3 · 2024: 2 · 2023: 2 · 2022: 5 · 2021: 5 · 2020: 7 · 2019: 2 · 2018: 5 · 2017: 6 · 2016: 2 · 2015: 9 · 2014: 5 · 2013: 3 · 2012: 6
FWCI: 2.42
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Oncogene (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: American Cancer Society
University of Alabama at Birmingham
National Institutes of Health
Comprehensive Cancer Center, University of Alabama at Birmingham
National Cancer Institute (CA 13148-31, CA97247, R01CA158534, R01CA194414, P30CA013148, P50CA097247)
National Institute of Allergy and Infectious Diseases (T32-AI0705, T32AI007051)
National Institute of Neurological Disorders and Stroke (R01NS045290, NS-54158, R21NS054158)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Signaling Pathways in Disease
Health Sciences › Medicine › Genetics › Glioma Diagnosis and Treatment
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › NF-κB Signaling Pathways
Keywords: Pin1, peptidyl-prolyl isomerase, NF-κB signaling, glioblastoma, interleukin-8, p65 phosphorylation, tumor cell migration, therapeutic target
MeSH terms: NIMA-Interacting Peptidylprolyl Isomerase, Animals, Brain Neoplasms, Cell Movement, Glioblastoma, Humans, Phosphorylation, Promoter Regions, Genetic, RNA, Messenger, Tetracycline, Signal Transduction, Gene Expression Regulation, Neoplastic, Interleukin-8, NF-kappa B, Peptidylprolyl Isomerase, Cell Line, Tumor, Mice, Transcription Factor RelA, Inverted Repeat Sequences, Gene Knockdown Techniques

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The prolyl isomerase Pin1 regulates the NF-κB signaling pathway and interleukin-8 expression in glioblastoma

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