Co-Localization of Insulin-Like Growth Factor Binding Protein-1, Casein Kinase-2β, and Mechanistic Target of Rapamycin in Human Hepatocellular Carcinoma Cells as Demonstrated by Dual Immunofluorescence and in Situ Proximity Ligation Assay
Insulin-like growth factor binding protein (IGFBP)–1 influences fetal growth by modifying insulin-like growth factor–I (IGF-I) bioavailability. IGFBP-1 phosphorylation, which markedly increases its affinity for IGF-I, is regulated by mechanistic target of rapamycin (mTOR) and casein kinase (CSNK)–2....
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Published in | The American journal of pathology Vol. 188; no. 1; pp. 111 - 124 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
Elsevier Inc
01.01.2018
American Society for Investigative Pathology |
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Abstract | Insulin-like growth factor binding protein (IGFBP)–1 influences fetal growth by modifying insulin-like growth factor–I (IGF-I) bioavailability. IGFBP-1 phosphorylation, which markedly increases its affinity for IGF-I, is regulated by mechanistic target of rapamycin (mTOR) and casein kinase (CSNK)–2. However, the underlying molecular mechanisms remain unknown. We examined the cellular localization and potential interactions of IGFBP-1, CSNK-2β, and mTOR as a prerequisite for protein–protein interaction. Analysis of dual immunofluorescence images indicated a potential perinuclear co-localization between IGFBP-1 and CSNK-2β and a nuclear co-localization between CSNK-2β and mTOR. Proximity ligation assay (PLA) indicated proximity between IGFBP-1 and CSNK-2β as well as mTOR and CSNK-2β but not between mTOR and IGFBP-1. Three-dimensional rendering of the PLA images validated that IGFBP-1 and CSNK-2β interactions were in the perinuclear region and mTOR and CSNK-2β interactions were also predominantly perinuclear rather than nuclear as indicated by mTOR and CSNK-2β co-localization. Compared with control, hypoxia and rapamycin treatment showed markedly amplified PLA signals for IGFBP-1 and CSNK-2β (approximately 18-fold, P = 0.0002). Stable isotope labeling with multiple reaction monitoring–mass spectrometry demonstrated that hypoxia and rapamycin treatment increased IGFBP-1 phosphorylation at Ser98/Ser101/Ser119/Ser174 but most considerably (106-fold) at Ser169. We report interactions between CSNK-2β and IGFBP-1 as well as mTOR and CSNK-2β, providing strong evidence of a mechanistic link between mTOR and IGF-I signaling, two critical regulators of cell growth via CSNK-2. |
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AbstractList | Insulin-like growth factor binding protein (IGFBP)–1 influences fetal growth by modifying insulin-like growth factor–I (IGF-I) bioavailability. IGFBP-1 phosphorylation, which markedly increases its affinity for IGF-I, is regulated by mechanistic target of rapamycin (mTOR) and casein kinase (CSNK)–2. However, the underlying molecular mechanisms remain unknown. We examined the cellular localization and potential interactions of IGFBP-1, CSNK-2β, and mTOR as a prerequisite for protein–protein interaction. Analysis of dual immunofluorescence images indicated a potential perinuclear co-localization between IGFBP-1 and CSNK-2β and a nuclear co-localization between CSNK-2β and mTOR. Proximity ligation assay (PLA) indicated proximity between IGFBP-1 and CSNK-2β as well as mTOR and CSNK-2β but not between mTOR and IGFBP-1. Three-dimensional rendering of the PLA images validated that IGFBP-1 and CSNK-2β interactions were in the perinuclear region and mTOR and CSNK-2β interactions were also predominantly perinuclear rather than nuclear as indicated by mTOR and CSNK-2β co-localization. Compared with control, hypoxia and rapamycin treatment showed markedly amplified PLA signals for IGFBP-1 and CSNK-2β (approximately 18-fold,
P
= 0.0002). Stable isotope labeling with multiple reaction monitoring–mass spectrometry demonstrated that hypoxia and rapamycin treatment increased IGFBP-1 phosphorylation at Ser98/Ser101/Ser119/Ser174 but most considerably (106-fold) at Ser169. We report interactions between CSNK-2β and IGFBP-1 as well as mTOR and CSNK-2β, providing strong evidence of a mechanistic link between mTOR and IGF-I signaling, two critical regulators of cell growth via CSNK-2. Insulin-like growth factor binding protein (IGFBP)-1 influences fetal growth by modifying insulin-like growth factor-I (IGF-I) bioavailability. IGFBP-1 phosphorylation, which markedly increases its affinity for IGF-I, is regulated by mechanistic target of rapamycin (mTOR) and casein kinase (CSNK)-2. However, the underlying molecular mechanisms remain unknown. We examined the cellular localization and potential interactions of IGFBP-1, CSNK-2β, and mTOR as a prerequisite for protein-protein interaction. Analysis of dual immunofluorescence images indicated a potential perinuclear co-localization between IGFBP-1 and CSNK-2β and a nuclear co-localization between CSNK-2β and mTOR. Proximity ligation assay (PLA) indicated proximity between IGFBP-1 and CSNK-2β as well as mTOR and CSNK-2β but not between mTOR and IGFBP-1. Three-dimensional rendering of the PLA images validated that IGFBP-1 and CSNK-2β interactions were in the perinuclear region and mTOR and CSNK-2β interactions were also predominantly perinuclear rather than nuclear as indicated by mTOR and CSNK-2β co-localization. Compared with control, hypoxia and rapamycin treatment showed markedly amplified PLA signals for IGFBP-1 and CSNK-2β (approximately 18-fold, P = 0.0002). Stable isotope labeling with multiple reaction monitoring-mass spectrometry demonstrated that hypoxia and rapamycin treatment increased IGFBP-1 phosphorylation at Ser98/Ser101/Ser119/Ser174 but most considerably (106-fold) at Ser169. We report interactions between CSNK-2β and IGFBP-1 as well as mTOR and CSNK-2β, providing strong evidence of a mechanistic link between mTOR and IGF-I signaling, two critical regulators of cell growth via CSNK-2. Insulin-like growth factor binding protein (IGFBP)-1 influences fetal growth by modifying insulin-like growth factor-I (IGF-I) bioavailability. IGFBP-1 phosphorylation, which markedly increases its affinity for IGF-I, is regulated by mechanistic target of rapamycin (mTOR) and casein kinase (CSNK)-2. However, the underlying molecular mechanisms remain unknown. We examined the cellular localization and potential interactions of IGFBP-1, CSNK-2β, and mTOR as a prerequisite for protein-protein interaction. Analysis of dual immunofluorescence images indicated a potential perinuclear co-localization between IGFBP-1 and CSNK-2β and a nuclear co-localization between CSNK-2β and mTOR. Proximity ligation assay (PLA) indicated proximity between IGFBP-1 and CSNK-2β as well as mTOR and CSNK-2β but not between mTOR and IGFBP-1. Three-dimensional rendering of the PLA images validated that IGFBP-1 and CSNK-2β interactions were in the perinuclear region and mTOR and CSNK-2β interactions were also predominantly perinuclear rather than nuclear as indicated by mTOR and CSNK-2β co-localization. Compared with control, hypoxia and rapamycin treatment showed markedly amplified PLA signals for IGFBP-1 and CSNK-2β (approximately 18-fold, P = 0.0002). Stable isotope labeling with multiple reaction monitoring-mass spectrometry demonstrated that hypoxia and rapamycin treatment increased IGFBP-1 phosphorylation at Ser98/Ser101/Ser119/Ser174 but most considerably (106-fold) at Ser169. We report interactions between CSNK-2β and IGFBP-1 as well as mTOR and CSNK-2β, providing strong evidence of a mechanistic link between mTOR and IGF-I signaling, two critical regulators of cell growth via CSNK-2. |
Author | Biggar, Kyle Jansson, Thomas Dhruv, Manthan R. Li, Shawn S.-C. Singal, Sahil S. Shehab, Majida A. Gupta, Madhulika B. Nygard, Karen |
AuthorAffiliation | Department of Biochemistry, University of Western Ontario, London, Ontario, Canada Biotron Laboratory, University of Western Ontario, London, Ontario, Canada Department of Obstetrics & Gynecology, University of Colorado Anschutz Medical Campus, Aurora, Colorado, Canada Department of Pediatrics, University of Western Ontario, London, Ontario, Canada Institute of Biochemistry, Carleton University, Ottawa, Ontario, Canada Children’s Health Research Institute, London, Ontario, Canada |
AuthorAffiliation_xml | – name: Department of Obstetrics & Gynecology, University of Colorado Anschutz Medical Campus, Aurora, Colorado, Canada – name: Department of Pediatrics, University of Western Ontario, London, Ontario, Canada – name: Department of Biochemistry, University of Western Ontario, London, Ontario, Canada – name: Children’s Health Research Institute, London, Ontario, Canada – name: Institute of Biochemistry, Carleton University, Ottawa, Ontario, Canada – name: Biotron Laboratory, University of Western Ontario, London, Ontario, Canada |
Author_xml | – sequence: 1 givenname: Sahil S. surname: Singal fullname: Singal, Sahil S. organization: Department of Biochemistry, University of Western Ontario, London, Ontario, Canada – sequence: 2 givenname: Karen surname: Nygard fullname: Nygard, Karen organization: Biotron Laboratory, University of Western Ontario, London, Ontario, Canada – sequence: 3 givenname: Manthan R. surname: Dhruv fullname: Dhruv, Manthan R. organization: Department of Pediatrics, University of Western Ontario, London, Ontario, Canada – sequence: 4 givenname: Kyle surname: Biggar fullname: Biggar, Kyle organization: Department of Biochemistry, University of Western Ontario, London, Ontario, Canada – sequence: 5 givenname: Majida A. surname: Shehab fullname: Shehab, Majida A. organization: Department of Pediatrics, University of Western Ontario, London, Ontario, Canada – sequence: 6 givenname: Shawn S.-C. surname: Li fullname: Li, Shawn S.-C. organization: Department of Biochemistry, University of Western Ontario, London, Ontario, Canada – sequence: 7 givenname: Thomas surname: Jansson fullname: Jansson, Thomas organization: Department of Obstetrics & Gynecology, University of Colorado Anschutz Medical Campus, Aurora, Colorado, Canada – sequence: 8 givenname: Madhulika B. surname: Gupta fullname: Gupta, Madhulika B. email: mbgupta@uwo.ca organization: Department of Biochemistry, University of Western Ontario, London, Ontario, Canada |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29037858$$D View this record in MEDLINE/PubMed |
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CitedBy_id | crossref_primary_10_1210_jc_2018_00820 crossref_primary_10_1152_ajpendo_00220_2020 crossref_primary_10_1096_fj_202100397R crossref_primary_10_1016_j_mce_2021_111400 crossref_primary_10_1038_s41374_020_0420_9 crossref_primary_10_3892_br_2018_1069 crossref_primary_10_1016_j_mce_2020_110865 crossref_primary_10_1093_biolre_ioy249 crossref_primary_10_1369_00221554221112702 crossref_primary_10_1016_j_snb_2021_131126 |
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Snippet | Insulin-like growth factor binding protein (IGFBP)–1 influences fetal growth by modifying insulin-like growth factor–I (IGF-I) bioavailability. IGFBP-1... Insulin-like growth factor binding protein (IGFBP)-1 influences fetal growth by modifying insulin-like growth factor-I (IGF-I) bioavailability. IGFBP-1... |
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SubjectTerms | Carcinoma, Hepatocellular - metabolism Carcinoma, Hepatocellular - pathology Casein Kinase II - metabolism Fluorescent Antibody Technique Hep G2 Cells Humans Insulin-Like Growth Factor Binding Protein 1 - metabolism Liver Neoplasms - metabolism Liver Neoplasms - pathology Phosphorylation Signal Transduction - physiology TOR Serine-Threonine Kinases - metabolism |
Title | Co-Localization of Insulin-Like Growth Factor Binding Protein-1, Casein Kinase-2β, and Mechanistic Target of Rapamycin in Human Hepatocellular Carcinoma Cells as Demonstrated by Dual Immunofluorescence and in Situ Proximity Ligation Assay |
URI | https://dx.doi.org/10.1016/j.ajpath.2017.09.009 https://www.ncbi.nlm.nih.gov/pubmed/29037858 https://www.proquest.com/docview/1952111753/abstract/ https://pubmed.ncbi.nlm.nih.gov/PMC5745526 |
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