Stimulation of Fibronectin Matrix Assembly by Lysine Acetylation
Abstract
:1. Introduction
2. Materials and Methods
2.1. Fibronectin, Inhibitors, and Antibodies
2.2. Mesangial Cell Culture
2.3. Generation of Cells Expressing β1 Integrin Lysine Mutations
2.4. Isolation of FN Matrix and Immunoblotting
2.5. Cell Attachment and Ligand Binding Assays
2.6. Matrix Contraction Assay
2.7. Immunofluorescence Microscopy
2.8. Acetyl-lysine Immunoprecipitation
2.9. TIRF Microscopy
2.10. Statistical Analysis
3. Results
3.1. Effects of Deacetylase Inhibitors on FN Matrix Assembly
3.2. Mimetics of Acetylated and Non-Acetylated Lysine in β1 Integrin
3.3. β1 Integrin Acetylation in SBHA-Treated Cells
3.4. Effects of Increased Acetylation on Cell Attachment to FN
3.5. Differential Recruitment of Kindlin-2 to Focal Adhesions
3.6. Effects of Acetylation on Integrin Activity and Cell Contractility
3.7. Stimulation of Lysine Acetylation Enhances the Effects of β1(K794Q) on FN Matrix Assembly
4. Discussion
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Schroeder, E.B.; Powers, J.D.; O’Connor, P.J.; Nichols, G.A.; Xu, S.; Desai, J.R.; Karter, A.J.; Morales, L.S.; Newton, K.M.; Pathak, R.D.; et al. Prevalence of chronic kidney disease among individuals with diabetes in the SUPREME-DM Project, 2005–2011. J. Diabetes Complicat. 2015, 29, 637–643. [Google Scholar] [CrossRef] [PubMed]
- Brosius, F.C., III. New insights into the mechanisms of fibrosis and sclerosis in diabetic nephropathy. Rev. Endocr. Metab. Disord. 2008, 9, 245–254. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Dixon, A.J.; Burns, J.; Dunnill, M.S.; McGee, J.O. Distribution of fibronectin in normal and diseased human kidneys. J. Clin. Pathol. 1980, 33, 1021–1028. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Miller, C.G.; Pozzi, A.; Zent, R.; Schwarzbauer, J.E. Effects of high glucose on integrin activity and fibronectin matrix assembly by mesangial cells. Mol. Biol. Cell 2014, 25, 2342–2350. [Google Scholar] [CrossRef]
- Singh, P.; Carraher, C.; Schwarzbauer, J.E. Assembly of fibronectin extracellular matrix. Annu. Rev. Cell Dev. Biol. 2010, 26, 397–419. [Google Scholar] [CrossRef][Green Version]
- Sottile, J.; Hocking, D.C. Fibronectin polymerization regulates the composition and stability of extracellular matrix fibrils and cell-matrix adhesions. Mol. Biol. Cell 2002, 13, 3546–3559. [Google Scholar] [CrossRef][Green Version]
- Dallas, S.L.; Sivakumar, P.; Jones, C.J.; Chen, Q.; Peters, D.M.; Mosher, D.F.; Humphries, M.J.; Kielty, C.M. Fibronectin regulates latent transforming growth factor-beta (TGF beta) by controlling matrix assembly of latent TGF beta-binding protein-1. J. Biol. Chem. 2005, 280, 18871–18880. [Google Scholar] [CrossRef][Green Version]
- Velling, T.; Risteli, J.; Wennerberg, K.; Mosher, D.F.; Johansson, S. Polymerization of type I and III collagens is dependent on fibronectin and enhanced by integrins alpha 11beta 1 and alpha 2beta 1. J. Biol. Chem. 2002, 277, 37377–37381. [Google Scholar] [CrossRef][Green Version]
- Filla, M.S.; Dimeo, K.D.; Tong, T.; Peters, D.M. Disruption of fibronectin matrix affects type IV collagen, fibrillin and laminin deposition into extracellular matrix of human trabecular meshwork (HTM) cells. Exp. Eye Res. 2017, 165, 7–19. [Google Scholar] [CrossRef]
- Miller, C.G.; Budoff, G.; Prenner, J.L.; Schwarzbauer, J.E. Minireview: Fibronectin in retinal disease. Exp. Biol. Med. 2017, 242, 1–7. [Google Scholar] [CrossRef][Green Version]
- Wynn, T.A. Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases. J. Clin. Investig. 2007, 117, 524–529. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Xue, C.; Mei, C.L. Polycystic Kidney Disease and Renal Fibrosis. Adv. Exp. Med. Biol. 2019, 1165, 81–100. [Google Scholar] [CrossRef] [PubMed]
- Pietrocola, F.; Galluzzi, L.; Bravo-San Pedro, J.M.; Madeo, F.; Kroemer, G. Acetyl coenzyme A: A central metabolite and second messenger. Cell Metab. 2015, 21, 805–821. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Kouzarides, T. Acetylation: A regulatory modification to rival phosphorylation? EMBO J. 2000, 19, 1176–1179. [Google Scholar] [CrossRef]
- Yang, X.J. Lysine acetylation and the bromodomain: A new partnership for signaling. Bioessays 2004, 26, 1076–1087. [Google Scholar] [CrossRef]
- Kosanam, H.; Thai, K.; Zhang, Y.; Advani, A.; Connelly, K.A.; Diamandis, E.P.; Gilbert, R.E. Diabetes induces lysine acetylation of intermediary metabolism enzymes in the kidney. Diabetes 2014, 63, 2432–2439. [Google Scholar] [CrossRef][Green Version]
- Liu, R.; Zhong, Y.; Li, X.; Chen, H.; Jim, B.; Zhou, M.M.; Chuang, P.Y.; He, J.C. Role of transcription factor acetylation in diabetic kidney disease. Diabetes 2014, 63, 2440–2453. [Google Scholar] [CrossRef][Green Version]
- Deb, D.K.; Bao, R.; Li, Y.C. Critical role of the cAMP-PKA pathway in hyperglycemia-induced epigenetic activation of fibrogenic program in the kidney. FASEB J. 2017, 31, 2065–2075. [Google Scholar] [CrossRef][Green Version]
- Huang, X.Z.; Wen, D.; Zhang, M.; Xie, Q.; Ma, L.; Guan, Y.; Ren, Y.; Chen, J.; Hao, C.M. Sirt1 activation ameliorates renal fibrosis by inhibiting the TGF-beta/Smad3 pathway. J. Cell. Biochem. 2014, 115, 996–1005. [Google Scholar] [CrossRef]
- Wen, D.; Huang, X.; Zhang, M.; Zhang, L.; Chen, J.; Gu, Y.; Hao, C.M. Resveratrol attenuates diabetic nephropathy via modulating angiogenesis. PLoS ONE 2013, 8, e82336. [Google Scholar] [CrossRef]
- Joo, E.E.; Yamada, K.M. MYPT1 regulates contractility and microtubule acetylation to modulate integrin adhesions and matrix assembly. Nat. Commun. 2014, 5, 3510. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Choudhary, C.; Kumar, C.; Gnad, F.; Nielsen, M.L.; Rehman, M.; Walther, T.C.; Olsen, J.V.; Mann, M. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 2009, 325, 834–840. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Wilson, C.L.; Schwarzbauer, J.E. The alternatively spliced V region contributes to the differential incorporation of plasma and cellular fibronectins into fibrin clots. J. Cell Biol. 1992, 119, 923–933. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Chen, X.; Moeckel, G.; Morrow, J.D.; Cosgrove, D.; Harris, R.C.; Fogo, A.B.; Zent, R.; Pozzi, A. Lack of integrin alpha1beta1 leads to severe glomerulosclerosis after glomerular injury. Am. J. Pathol. 2004, 165, 617–630. [Google Scholar] [CrossRef]
- Chen, X.; Abair, T.D.; Ibanez, M.R.; Su, Y.; Frey, M.R.; Dise, R.S.; Polk, D.B.; Singh, A.B.; Harris, R.C.; Zent, R.; et al. Integrin alpha1beta1 controls reactive oxygen species synthesis by negatively regulating epidermal growth factor receptor-mediated Rac activation. Mol. Cell Biol. 2007, 27, 3313–3326. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Girod, P.A.; Zahn-Zabal, M.; Mermod, N. Use of the chicken lysozyme 5’ matrix attachment region to generate high producer CHO cell lines. Biotechnol. Bioeng. 2005, 91, 1–11. [Google Scholar] [CrossRef]
- Loc, P.V.; Stratling, W.H. The matrix attachment regions of the chicken lysozyme gene co-map with the boundaries of the chromatin domain. EMBO J. 1988, 7, 655–664. [Google Scholar] [CrossRef]
- Fassler, R.; Pfaff, M.; Murphy, J.; Noegel, A.A.; Johansson, S.; Timpl, R.; Albrecht, R. Lack of beta 1 integrin gene in embryonic stem cells affects morphology, adhesion, and migration but not integration into the inner cell mass of blastocysts. J. Cell Biol. 1995, 128, 979–988. [Google Scholar] [CrossRef][Green Version]
- Wierzbicka-Patynowski, I.; Mao, Y.; Schwarzbauer, J.E. Analysis of fibronectin matrix assembly. Curr. Protoc. Cell Biol. 2004, 25. [Google Scholar] [CrossRef]
- O’Toole, T.E.; Katagiri, Y.; Faull, R.J.; Peter, K.; Tamura, R.; Quaranta, V.; Loftus, J.C.; Shattil, S.J.; Ginsberg, M.H. Integrin cytoplasmic domains mediate inside-out signal transduction. J. Cell Biol. 1994, 124, 1047–1059. [Google Scholar] [CrossRef]
- Midwood, K.S.; Valenick, L.V.; Hsia, H.C.; Schwarzbauer, J.E. Coregulation of fibronectin signaling and matrix contraction by tenascin-C and syndecan-4. Mol. Biol. Cell 2004, 15, 5670–5677. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Corbett, S.A.; Schwarzbauer, J.E. Requirements for alpha(5)beta(1) integrin-mediated retraction of fibronectin-fibrin matrices. J. Biol. Chem. 1999, 274, 20943–20948. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Soto-Ribeiro, M.; Kastberger, B.; Bachmann, M.; Azizi, L.; Fouad, K.; Jacquier, M.C.; Boettiger, D.; Bouvard, D.; Bastmeyer, M.; Hytonen, V.P.; et al. beta1D integrin splice variant stabilizes integrin dynamics and reduces integrin signaling by limiting paxillin recruitment. J. Cell Sci. 2019, 132. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Brahme, N.N.; Calderwood, D.A. Cell adhesion: A FERM grasp of the tail sorts out integrins. Curr. Biol. 2012, 22, R692–R694. [Google Scholar] [CrossRef][Green Version]
- Faull, R.J.; Kovach, N.L.; Harlan, J.M.; Ginsberg, M.H. Affinity modulation of integrin alpha 5 beta 1: Regulation of the functional response by soluble fibronectin. J. Cell Biol. 1993, 121, 155–162. [Google Scholar] [CrossRef]
- Walraven, M.; Hinz, B. Therapeutic approaches to control tissue repair and fibrosis: Extracellular matrix as a game changer. Matrix Biol. 2018, 71, 205–224. [Google Scholar] [CrossRef]
- Chen, K.H.; Hung, C.C.; Hsu, H.H.; Jing, Y.H.; Yang, C.W.; Chen, J.K. Resveratrol ameliorates early diabetic nephropathy associated with suppression of augmented TGF-beta/smad and ERK1/2 signaling in streptozotocin-induced diabetic rats. Chem. Biol. Interact. 2011, 190, 45–53. [Google Scholar] [CrossRef]
- Calderwood, D.A. Integrin activation. J. Cell Sci. 2004, 117, 657–666. [Google Scholar] [CrossRef][Green Version]
- Hynes, R.O. The emergence of integrins: A personal and historical perspective. Matrix Biol. 2004, 23, 333–340. [Google Scholar] [CrossRef][Green Version]
- Harburger, D.S.; Bouaouina, M.; Calderwood, D.A. Kindlin-1 and -2 directly bind the C-terminal region of beta integrin cytoplasmic tails and exert integrin-specific activation effects. J. Biol. Chem. 2009, 284, 11485–11497. [Google Scholar] [CrossRef][Green Version]
- Sun, Z.; Costell, M.; Fassler, R. Integrin activation by talin, kindlin and mechanical forces. Nat. Cell Biol. 2019, 21, 25–31. [Google Scholar] [CrossRef] [PubMed]
- Theodosiou, M.; Widmaier, M.; Bottcher, R.T.; Rognoni, E.; Veelders, M.; Bharadwaj, M.; Lambacher, A.; Austen, K.; Muller, D.J.; Zent, R.; et al. Kindlin-2 cooperates with talin to activate integrins and induces cell spreading by directly binding paxillin. Elife 2016, 5, e10130. [Google Scholar] [CrossRef] [PubMed]
- Qu, H.; Tu, Y.; Shi, X.; Larjava, H.; Saleem, M.A.; Shattil, S.J.; Fukuda, K.; Qin, J.; Kretzler, M.; Wu, C. Kindlin-2 regulates podocyte adhesion and fibronectin matrix deposition through interactions with phosphoinositides and integrins. J. Cell Sci. 2011, 124, 879–891. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Anthis, N.J.; Wegener, K.L.; Ye, F.; Kim, C.; Goult, B.T.; Lowe, E.D.; Vakonakis, I.; Bate, N.; Critchley, D.R.; Ginsberg, M.H.; et al. The structure of an integrin/talin complex reveals the basis of inside-out signal transduction. EMBO J. 2009, 28, 3623–3632. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Li, H.; Deng, Y.; Sun, K.; Yang, H.; Liu, J.; Wang, M.; Zhang, Z.; Lin, J.; Wu, C.; Wei, Z.; et al. Structural basis of kindlin-mediated integrin recognition and activation. Proc. Natl. Acad. Sci. USA 2017, 114, 9349–9354. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Brunner, M.; Millon-Fremillon, A.; Chevalier, G.; Nakchbandi, I.A.; Mosher, D.; Block, M.R.; Albiges-Rizo, C.; Bouvard, D. Osteoblast mineralization requires beta1 integrin/ICAP-1-dependent fibronectin deposition. J. Cell Biol. 2011, 194, 307–322. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Destaing, O.; Planus, E.; Bouvard, D.; Oddou, C.; Badowski, C.; Bossy, V.; Raducanu, A.; Fourcade, B.; Albiges-Rizo, C.; Block, M.R. beta1A integrin is a master regulator of invadosome organization and function. Mol. Biol. Cell 2010, 21, 4108–4119. [Google Scholar] [CrossRef][Green Version]
- Liu, W.; Draheim, K.M.; Zhang, R.; Calderwood, D.A.; Boggon, T.J. Mechanism for KRIT1 release of ICAP1-mediated suppression of integrin activation. Mol. Cell 2013, 49, 719–729. [Google Scholar] [CrossRef][Green Version]
- Cluzel, C.; Saltel, F.; Lussi, J.; Paulhe, F.; Imhof, B.A.; Wehrle-Haller, B. The mechanisms and dynamics of (alpha)v(beta)3 integrin clustering in living cells. J. Cell Biol. 2005, 171, 383–392. [Google Scholar] [CrossRef][Green Version]
- Hansen, B.K.; Gupta, R.; Baldus, L.; Lyon, D.; Narita, T.; Lammers, M.; Choudhary, C.; Weinert, B.T. Analysis of human acetylation stoichiometry defines mechanistic constraints on protein regulation. Nat. Commun. 2019, 10, 1055. [Google Scholar] [CrossRef][Green Version]
- Coussen, F.; Choquet, D.; Sheetz, M.P.; Erickson, H.P. Trimers of the fibronectin cell adhesion domain localize to actin filament bundles and undergo rearward translocation. J. Cell Sci. 2002, 115, 2581–2590. [Google Scholar] [PubMed]
- Cavalcanti-Adam, E.A.; Volberg, T.; Micoulet, A.; Kessler, H.; Geiger, B.; Spatz, J.P. Cell spreading and focal adhesion dynamics are regulated by spacing of integrin ligands. Biophys. J. 2007, 92, 2964–2974. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Changede, R.; Xu, X.; Margadant, F.; Sheetz, M.P. Nascent Integrin Adhesions Form on All Matrix Rigidities after Integrin Activation. Dev. Cell 2015, 35, 614–621. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Filippakopoulos, P.; Knapp, S. Targeting bromodomains: Epigenetic readers of lysine acetylation. Nat. Rev. Drug Discov. 2014, 13, 337–356. [Google Scholar] [CrossRef]
- Kouzarides, T. Chromatin modifications and their function. Cell 2007, 128, 693–705. [Google Scholar] [CrossRef][Green Version]
- Impens, F.; Radoshevich, L.; Cossart, P.; Ribet, D. Mapping of SUMO sites and analysis of SUMOylation changes induced by external stimuli. Proc. Natl. Acad. Sci. USA 2014, 111, 12432–12437. [Google Scholar] [CrossRef][Green Version]
- Pastino, A.K.; Greco, T.M.; Mathias, R.A.; Cristea, I.M.; Schwarzbauer, J.E. Stimulatory effects of advanced glycation endproducts (AGEs) on fibronectin matrix assembly. Matrix Biol. 2017, 59, 39–53. [Google Scholar] [CrossRef][Green Version]
- Hadden, M.J.; Advani, A. Histone Deacetylase Inhibitors and Diabetic Kidney Disease. Int. J. Mol. Sci. 2018, 19, 2630. [Google Scholar] [CrossRef]
- Mann, B.S.; Johnson, J.R.; Cohen, M.H.; Justice, R.; Pazdur, R. FDA approval summary: Vorinostat for treatment of advanced primary cutaneous T-cell lymphoma. Oncologist 2007, 12, 1247–1252. [Google Scholar] [CrossRef]
© 2020 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
Vega, M.E.; Kastberger, B.; Wehrle-Haller, B.; Schwarzbauer, J.E. Stimulation of Fibronectin Matrix Assembly by Lysine Acetylation. Cells 2020, 9, 655. https://doi.org/10.3390/cells9030655
Vega ME, Kastberger B, Wehrle-Haller B, Schwarzbauer JE. Stimulation of Fibronectin Matrix Assembly by Lysine Acetylation. Cells. 2020; 9(3):655. https://doi.org/10.3390/cells9030655
Chicago/Turabian StyleVega, Maria E., Birgit Kastberger, Bernhard Wehrle-Haller, and Jean E. Schwarzbauer. 2020. "Stimulation of Fibronectin Matrix Assembly by Lysine Acetylation" Cells 9, no. 3: 655. https://doi.org/10.3390/cells9030655