Insulin-Like Growth Factor Binding Protein-3 Binds to Histone 3
Abstract
:1. Introduction
2. Results
3. Discussion
4. Material and Methods
4.1. Cell Lines
4.2. Cell Fractionation and Lysis
4.3. Whole Cell Lysis
4.4. Ligand Blotting
4.5. Ligand Dot Blot
4.6. Far-Western Blot Analyses
4.7. Co-Immunoprecipitation
4.8. Western Blot Analysis
4.9. Protein Estimation
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Foulstone, E.J.; Savage, P.B.; Crown, A.L.; Holly, J.M.; Stewart, C.E. Role of insulin-like growth factor binding protein-3 (IGFBP-3) in the differentiation of primary human adult skeletal myoblasts. J. Cell. Physiol. 2003, 195, 70–79. [Google Scholar] [CrossRef] [PubMed]
- Schedlich, L.J.; Le Page, S.L.; Firth, S.M.; Briggs, L.J.; Jans, D.A.; Baxter, R.C. Nuclear import of insulin-like growth factor-binding protein-3 and -5 is mediated by the importin beta subunit. J. Biol. Chem. 2000, 275, 23462–23470. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Micutkova, L.; Hermann, M.; Offterdinger, M.; Hess, M.W.; Matscheski, A.; Pircher, H.; Muck, C.; Ebner, H.L.; Laich, A.; Ferrando-May, E.; et al. Analysis of the cellular uptake and nuclear delivery of insulin-like growth factor binding protein-3 in human osteosarcoma cells. Int. J. Cancer 2012, 130, 1544–1557. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Granata, R.; Trovato, L.; Garbarino, G.; Taliano, M.; Ponti, R.; Sala, G.; Ghidoni, R.; Ghigo, E. Dual effects of IGFBP-3 on endothelial cell apoptosis and survival: Involvement of the sphingolipid signaling pathways. FASEB J. 2004, 18, 1456–1458. [Google Scholar] [CrossRef]
- Grkovic, S.; O’Reilly, V.C.; Han, S.; Hong, M.; Baxter, R.C.; Firth, S.M. IGFBP-3 binds GRP78, stimulates autophagy and promotes the survival of breast cancer cells exposed to adverse microenvironments. Oncogene 2013, 32, 2412–2420. [Google Scholar] [CrossRef] [Green Version]
- Lin, M.Z.; Marzec, K.A.; Martin, J.L.; Baxter, R.C. The role of insulin-like growth factor binding protein-3 in the breast cancer cell response to DNA-damaging agents. Oncogene 2014, 33, 85–96. [Google Scholar] [CrossRef] [Green Version]
- Chua, M.W.; Lin, M.Z.; Martin, J.L.; Baxter, R.C. Involvement of the insulin-like growth factor binding proteins in the cancer cell response to DNA damage. J. Cell Commun. Signal. 2015, 9, 167–176. [Google Scholar] [CrossRef] [Green Version]
- Shrivastav, S.V.; Bhardwaj, A.; Pathak, K.A.; Shrivastav, A. Insulin-Like Growth Factor Binding Protein-3 (IGFBP-3): Unraveling the Role in Mediating IGF-Independent Effects Within the Cell. Front. Cell Dev. Biol. 2020, 8, 286. [Google Scholar] [CrossRef]
- Butt, A.J.; Fraley, K.A.; Firth, S.M.; Baxter, R.C. IGF-binding protein-3-induced growth inhibition and apoptosis do not require cell surface binding and nuclear translocation in human breast cancer cells. Endocrinology 2002, 143, 2693–2699. [Google Scholar] [CrossRef]
- Shang, Y.; Baumrucker, C.R.; Green, M.H. Signal relay by retinoic acid receptors alpha and beta in the retinoic acid-induced expression of insulin-like growth factor-binding protein-3 in breast cancer cells. J. Biol. Chem. 1999, 274, 18005–18010. [Google Scholar] [CrossRef] [Green Version]
- Gucev, Z.S.; Oh, Y.; Kelley, K.M.; Rosenfeld, R.G. Insulin-like growth factor binding protein 3 mediates retinoic acid- and transforming growth factor beta2-induced growth inhibition in human breast cancer cells. Cancer Res. 1996, 56, 1545–1550. [Google Scholar] [PubMed]
- Kansra, S.; Ewton, D.Z.; Wang, J.; Friedman, E. IGFBP-3 mediates TGF beta 1 proliferative response in colon cancer cells. Int. J. Cancer 2000, 87, 373–378. [Google Scholar] [CrossRef]
- Rajah, R.; Lee, K.W.; Cohen, P. Insulin-like growth factor binding protein-3 mediates tumor necrosis factor-alpha-induced apoptosis: Role of Bcl-2 phosphorylation. Cell Growth Differ. 2002, 13, 163–171. [Google Scholar] [PubMed]
- Lopez-Bermejo, A.; Buckway, C.K.; Devi, G.R.; Hwa, V.; Plymate, S.R.; Oh, Y.; Rosenfeld, R.G. Characterization of insulin-like growth factor-binding protein-related proteins (IGFBP-rPs) 1, 2, and 3 in human prostate epithelial cells: Potential roles for IGFBP-rP1 and 2 in senescence of the prostatic epithelium. Endocrinology 2000, 141, 4072–4080. [Google Scholar] [CrossRef]
- Goossens, K.; Esquenet, M.; Swinnen, J.V.; Manin, M.; Rombauts, W.; Verhoeven, G. Androgens decrease and retinoids increase the expression of insulin-like growth factor-binding protein-3 in LNcaP prostatic adenocarcinoma cells. Mol. Cell. Endocrinol. 1999, 155, 9–18. [Google Scholar] [CrossRef]
- Krishnan, A.V.; Peehl, D.M.; Feldman, D. Inhibition of prostate cancer growth by vitamin D: Regulation of target gene expression. J. Cell. Biochem. 2003, 88, 363–371. [Google Scholar] [CrossRef]
- Boyle, B.J.; Zhao, X.Y.; Cohen, P.; Feldman, D. Insulin-like growth factor binding protein-3 mediates 1 alpha,25-dihydroxyvitamin d(3) growth inhibition in the LNCaP prostate cancer cell line through p21/WAF1. J. Urol. 2001, 165, 1319–1324. [Google Scholar] [CrossRef]
- Ingermann, A.R.; Yang, Y.F.; Han, J.; Mikami, A.; Garza, A.E.; Mohanraj, L.; Fan, L.; Idowu, M.; Ware, J.L.; Kim, H.S.; et al. Identification of a novel cell death receptor mediating IGFBP-3-induced anti-tumor effects in breast and prostate cancer. J. Biol. Chem. 2010, 285, 30233–30246. [Google Scholar] [CrossRef] [Green Version]
- Burrows, C.; Holly, J.M.; Laurence, N.J.; Vernon, E.G.; Carter, J.V.; Clark, M.A.; McIntosh, J.; McCaig, C.; Winters, Z.E.; Perks, C.M. Insulin-like growth factor binding protein 3 has opposing actions on malignant and nonmalignant breast epithelial cells that are each reversible and dependent upon cholesterol-stabilized integrin receptor complexes. Endocrinology 2006, 147, 3484–3500. [Google Scholar] [CrossRef] [Green Version]
- Lee, K.W.; Liu, B.; Ma, L.; Li, H.; Bang, P.; Koeffler, H.P.; Cohen, P. Cellular internalization of insulin-like growth factor binding protein-3: Distinct endocytic pathways facilitate re-uptake and nuclear localization. J. Biol. Chem. 2004, 279, 469–476. [Google Scholar] [CrossRef] [Green Version]
- Weinzimer, S.A.; Gibson, T.B.; Collett-Solberg, P.F.; Khare, A.; Liu, B.; Cohen, P. Transferrin is an insulin-like growth factor-binding protein-3 binding protein. J. Clin. Endocrinol. Metab. 2001, 86, 1806–1813. [Google Scholar] [CrossRef] [PubMed]
- Huang, S.S.; Ling, T.Y.; Tseng, W.F.; Huang, Y.H.; Tang, F.M.; Leal, S.M.; Huang, J.S. Cellular growth inhibition by IGFBP-3 and TGF-beta1 requires LRP-1. FASEB J. 2003, 17, 2068–2081. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Leal, S.M.; Liu, Q.; Huang, S.S.; Huang, J.S. The type V transforming growth factor beta receptor is the putative insulin-like growth factor-binding protein 3 receptor. J. Biol. Chem. 1997, 272, 20572–20576. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mishra, S.; Raz, A.; Murphy, L.J. Insulin-like growth factor binding protein-3 interacts with autocrine motility factor/phosphoglucose isomerase (AMF/PGI) and inhibits the AMF/PGI function. Cancer Res. 2004, 64, 2516–2522. [Google Scholar] [CrossRef] [Green Version]
- Li, C.; Harada, A.; Oh, Y. IGFBP-3 sensitizes antiestrogen-resistant breast cancer cells through interaction with GRP78. Cancer Lett. 2012, 325, 200–206. [Google Scholar] [CrossRef]
- Ikonen, M.; Liu, B.; Hashimoto, Y.; Ma, L.; Lee, K.W.; Niikura, T.; Nishimoto, I.; Cohen, P. Interaction between the Alzheimer’s survival peptide humanin and insulin-like growth factor-binding protein 3 regulates cell survival and apoptosis. Proc. Natl. Acad. Sci. USA 2003, 100, 13042–13047. [Google Scholar] [CrossRef] [Green Version]
- Wu, C.; Yao, G.; Zou, M.; Chen, G.; Wang, M.; Liu, J.; Wang, J.; Xu, D. N-Acetylgalactosaminyltransferase 14, a novel insulin-like growth factor binding protein-3 binding partner. Biochem. Biophys. Res. Commun. 2007, 357, 360–365. [Google Scholar] [CrossRef]
- Oufattole, M.; Lin, S.W.; Liu, B.; Mascarenhas, D.; Cohen, P.; Rodgers, B.D. Ribonucleic acid polymerase II binding subunit 3 (Rpb3), a potential nuclear target of insulin-like growth factor binding protein-3. Endocrinology 2006, 147, 2138–2146. [Google Scholar] [CrossRef] [Green Version]
- Liu, B.; Lee, H.Y.; Weinzimer, S.A.; Powell, D.R.; Clifford, J.L.; Kurie, J.M.; Cohen, P. Direct functional interactions between insulin-like growth factor-binding protein-3 and retinoid X receptor-alpha regulate transcriptional signaling and apoptosis. J. Biol. Chem. 2000, 275, 33607–33613. [Google Scholar] [CrossRef] [Green Version]
- Chan, S.S.; Schedlich, L.J.; Twigg, S.M.; Baxter, R.C. Inhibition of adipocyte differentiation by insulin-like growth factor-binding protein-3. Am. J. Physiol. Endocrinol. Metab. 2009, 296, E654–E663. [Google Scholar] [CrossRef] [Green Version]
- Moreno-Santos, I.; Castellano-Castillo, D.; Lara, M.F.; Fernandez-Garcia, J.C.; Tinahones, F.J.; Macias-Gonzalez, M. IGFBP-3 Interacts with the Vitamin D Receptor in Insulin Signaling Associated with Obesity in Visceral Adipose Tissue. Int. J. Mol. Sci. 2017, 18, 2349. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Holden, P.; Horton, W.A. Crude subcellular fractionation of cultured mammalian cell lines. BMC Res. Notes 2009, 2, 243. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Herrmann, C.; Avgousti, D.C.; Weitzman, M.D. Differential Salt Fractionation of Nuclei to Analyze Chromatin-associated Proteins from Cultured Mammalian Cells. Bio-Protocol 2017, 7, e2175. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Forcob, S.; Bulic, A.; Jonsson, F.; Lipps, H.J.; Postberg, J. Differential expression of histone H3 genes and selective association of the variant H3.7 with a specific sequence class in Stylonychia macronuclear development. Epigenetics Chromatin 2014, 7, 4. [Google Scholar] [CrossRef] [Green Version]
- Chakraborty, S.; Nguyen, P.K.; Ruyer-Quil, C.; Bontozoglou, V. Extreme solitary waves on falling liquid films. J. Fluid Mech. 2014, 745, 564–591. [Google Scholar] [CrossRef]
- Ruiz-Carrillo, A.; Jorcano, J.L. An octamer of core histones in solution: Central role of the H3-H4 tetramer in the self-assembly. Biochemistry 1979, 18, 760–768. [Google Scholar] [CrossRef]
- Thomas, J.O.; Butler, P.J. Characterization of the octamer of histones free in solution. J. Mol. Biol. 1977, 116, 769–781. [Google Scholar] [CrossRef]
- Eickbush, T.H.; Moudrianakis, E.N. The histone core complex: An octamer assembled by two sets of protein-protein interactions. Biochemistry 1978, 17, 4955–4964. [Google Scholar] [CrossRef]
- Chung, S.Y.; Hill, W.E.; Doty, P. Characterization of the histone core complex. Proc. Natl. Acad. Sci. USA 1978, 75, 1680–1684. [Google Scholar] [CrossRef] [Green Version]
- Annunziato, A.T. DNA Packaging: Nulceosomes and Chromatin. Nat. Educ. 2008, 1, 26. [Google Scholar]
- Forbes, B.E.; McCarthy, P.; Norton, R.S. Insulin-like growth factor binding proteins: A structural perspective. Front. Endocrinol. (Lausanne) 2012, 3, 38. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhao, Y.; Yin, P.; Bach, L.A.; Duan, C. Several acidic amino acids in the N-domain of insulin-like growth factor-binding protein-5 are important for its transactivation activity. J. Biol. Chem. 2006, 281, 14184–14191. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhong, Y.; Duan, C. Lamprey IGF-Binding Protein-3 Has IGF-Dependent and -Independent Actions. Front. Endocrinol. (Lausanne) 2016, 7, 174. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Baxter, R.C. Insulin-like growth factor binding protein-3 (IGFBP-3): Novel ligands mediate unexpected functions. J. Cell Commun. Signal. 2013, 7, 179–189. [Google Scholar] [CrossRef] [Green Version]
- Kastner, P.; Mark, M.; Chambon, P. Nonsteroid nuclear receptors: What are genetic studies telling us about their role in real life? Cell 1995, 83, 859–869. [Google Scholar] [CrossRef] [Green Version]
- Ikezoe, T.; Tanosaki, S.; Krug, U.; Liu, B.; Cohen, P.; Taguchi, H.; Koeffler, H.P. Insulin-like growth factor binding protein-3 antagonizes the effects of retinoids in myeloid leukemia cells. Blood 2004, 104, 237–242. [Google Scholar] [CrossRef] [Green Version]
- Pon, C.K.; Firth, S.M.; Baxter, R.C. Involvement of insulin-like growth factor binding protein-3 in peroxisome proliferator-activated receptor gamma-mediated inhibition of breast cancer cell growth. Mol. Cell. Endocrinol. 2015, 399, 354–361. [Google Scholar] [CrossRef]
- Jia, Q.; Xiao-li, M.; Xin, W.; Hong, C.; Bing-Ren, H. Insulin-like growth factor binding protein-3 interacts with the thyroid hormone receptor alpha1 and modulates transcription of thyroid hormone responsive gene. Zhongguo Yi Xue Ke Xue Yuan Xue Bao 2011, 33, 156–161. [Google Scholar]
- Alessi, D.R.; James, S.R.; Downes, C.P.; Holmes, A.B.; Gaffney, P.R.; Reese, C.B.; Cohen, P. Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Balpha. Curr. Biol. 1997, 7, 261–269. [Google Scholar] [CrossRef] [Green Version]
- Gui, Y.; Murphy, L.J. Insulin-like growth factor (IGF)-binding protein-3 (IGFBP-3) binds to fibronectin (FN): Demonstration of IGF-I/IGFBP-3/fn ternary complexes in human plasma. J. Clin. Endocrinol. Metab. 2001, 86, 2104–2110. [Google Scholar]
- Grulich-Henn, J.; Spiess, S.; Heinrich, U.; Schonberg, D.; Bettendorf, M. Ligand blot analysis of insulin-like growth factor-binding proteins using biotinylated insulin-like growth factor-I. Horm. Res. 1998, 49, 1–7. [Google Scholar] [CrossRef] [PubMed]
- Towbin, H.; Staehelin, T.; Gordon, J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc. Natl. Acad. Sci. USA 1979, 76, 4350–4354. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Bhardwaj, A.; Pathak, K.A.; Shrivastav, A.; Varma Shrivastav, S. Insulin-Like Growth Factor Binding Protein-3 Binds to Histone 3. Int. J. Mol. Sci. 2021, 22, 407. https://doi.org/10.3390/ijms22010407
Bhardwaj A, Pathak KA, Shrivastav A, Varma Shrivastav S. Insulin-Like Growth Factor Binding Protein-3 Binds to Histone 3. International Journal of Molecular Sciences. 2021; 22(1):407. https://doi.org/10.3390/ijms22010407
Chicago/Turabian StyleBhardwaj, Apurva, Kumar Alok Pathak, Anuraag Shrivastav, and Shailly Varma Shrivastav. 2021. "Insulin-Like Growth Factor Binding Protein-3 Binds to Histone 3" International Journal of Molecular Sciences 22, no. 1: 407. https://doi.org/10.3390/ijms22010407
APA StyleBhardwaj, A., Pathak, K. A., Shrivastav, A., & Varma Shrivastav, S. (2021). Insulin-Like Growth Factor Binding Protein-3 Binds to Histone 3. International Journal of Molecular Sciences, 22(1), 407. https://doi.org/10.3390/ijms22010407