Mimicking the Bioactivity of Fibroblast Growth Factor-2 Using Supramolecular Nanoribbons

Rubert Pérez, Charles M.; Álvarez, Zaida; Chen, Feng; Aytun, Taner; Stupp, Samuel I.

doi:10.1021/acsbiomaterials.7b00347

Title: Mimicking the Bioactivity of Fibroblast Growth Factor-2 Using Supramolecular Nanoribbons

Journal Article · Sun Aug 06 00:00:00 EDT 2017 · ACS Biomaterials Science & Engineering

DOI:https://doi.org/10.1021/acsbiomaterials.7b00347· OSTI ID:1821894

Rubert Pérez, Charles M. ^[1]; Álvarez, Zaida ^[1]; Chen, Feng ^[1]; Aytun, Taner ^[2];

^[3]

Northwestern Univ., Chicago, IL (United States)
Northwestern Univ., Evanston, IL (United States)
Northwestern Univ., Chicago, IL (United States); Northwestern Univ., Evanston, IL (United States)

Fibroblast growth factor (FGF-2) is a multifunctional growth factor that has pleiotropic effects in different tissues and organs. In particular, FGF-2 has a special role in angiogenesis, an important process in development, wound healing, cell survival, and differentiation. Therefore, incorporating biological agents like FGF-2 within therapeutic biomaterials is a potential strategy to create angiogenic bioactivity for the repair of damaged tissue caused by trauma or complications that arise from age and/or disease. However, the use of growth factors as therapeutic agents can be costly and does not always bring about efficient tissue repair due to rapid clearance from the targeted site. An alternative would be a stable supramolecular nanostructure with the capacity to activate the FGF-2 receptor that can also assemble into a scaffold deliverable to tissue. We report here on peptide amphiphiles that incorporate a peptide known to activate the FGF-2 receptor and peptide domains that drive its self-assembly into supramolecular nanoribbons. These FGF2-PA nanoribbons displayed the ability to increase the proliferation and migration of the human umbilical vein endothelial cells (HUVECs) in vitro to the same extent as the native FGF-2 protein at certain concentrations. We confirmed that this activity was specific to the FGFR1 signaling pathway by tracking the phosphorylation of downstream signaling effectors such ERK1/2 and pH3. These results indicated the specificity of FGF2-PA nanoribbons in activating the FGF-2 signaling pathway and its potential application as a supramolecular scaffold that can be used in vivo as an alternative to the encapsulation and delivery of the native FGF-2 protein.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Northwestern Univ., Evanston, IL (United States); Energy Frontier Research Centers (EFRC) (United States). Center for Bio-Inspired Energy Science (CBES)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: FG02-00ER45810

OSTI ID:: 1821894

Alternate ID(s):: OSTI ID: 1846790

Journal Information:: ACS Biomaterials Science & Engineering, Vol. 3, Issue 9; ISSN 2373-9878

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (58)

PERSPECTIVE ARTICLE: Growth factors and cytokines in wound healing: Growth factors and cytokines in wound healing Barrientos, Stephan; Stojadinovic, Olivera; Golinko, Michael S. Wound Repair and Regeneration, Vol. 16, Issue 5 https://doi.org/10.1111/j.1524-475X.2008.00410.x	journal	September 2008
Cytokines, chemokines and growth factors in wound healing: Mediators of wound healing Behm, B.; Babilas, P.; Landthaler, M. Journal of the European Academy of Dermatology and Venereology, Vol. 26, Issue 7 https://doi.org/10.1111/j.1468-3083.2011.04415.x	journal	December 2011
Designing Regenerative Biomaterial Therapies for the Clinic Pashuck, E. T.; Stevens, M. M. Science Translational Medicine, Vol. 4, Issue 160 https://doi.org/10.1126/scitranslmed.3002717	journal	November 2012
Design of growth factor sequestering biomaterials Belair, David G.; Le, Ngoc Nhi; Murphy, William L. Chem. Commun., Vol. 50, Issue 99 https://doi.org/10.1039/C4CC04317K	journal	January 2014
Design principles for therapeutic angiogenic materials Briquez, Priscilla S.; Clegg, Lindsay E.; Martino, Mikaël M. Nature Reviews Materials, Vol. 1, Issue 1 https://doi.org/10.1038/natrevmats.2015.6	journal	January 2016
Design properties of hydrogel tissue-engineering scaffolds Zhu, Junmin; Marchant, Roger E. Expert Review of Medical Devices, Vol. 8, Issue 5 https://doi.org/10.1586/erd.11.27	journal	September 2011
Growth factor delivery-based tissue engineering: general approaches and a review of recent developments Lee, Kangwon; Silva, Eduardo A.; Mooney, David J. Journal of The Royal Society Interface, Vol. 8, Issue 55 https://doi.org/10.1098/rsif.2010.0223	journal	June 2010
Cell-demanded release of VEGF from synthetic, biointeractive cell ingrowth matrices for vascularized tissue growth Zisch, Andreas H.; Lutolf, Matthias P.; Ehrbar, Martin The FASEB Journal, Vol. 17, Issue 15 https://doi.org/10.1096/fj.02-1041fje	journal	December 2003
Dual independent delivery of pro-angiogenic growth factors from starPEG-heparin hydrogels Zieris, A.; Chwalek, K.; Prokoph, S. Journal of Controlled Release, Vol. 156, Issue 1 https://doi.org/10.1016/j.jconrel.2011.06.042	journal	November 2011
Heparin Mimetic Peptide Nanofibers Promote Angiogenesis Mammadov, Rashad; Mammadov, Busra; Toksoz, Sila Biomacromolecules, Vol. 12, Issue 10 https://doi.org/10.1021/bm200957s	journal	October 2011
Therapeutic angiogenesis in cardiology using protein formulations Post, M. Cardiovascular Research, Vol. 49, Issue 3 https://doi.org/10.1016/S0008-6363(00)00216-9	journal	February 2001
Engineering vascularized tissue Jain, Rakesh K.; Au, Patrick; Tam, Josh Nature Biotechnology, Vol. 23, Issue 7 https://doi.org/10.1038/nbt0705-821	journal	July 2005
Clinical Trials in Coronary Angiogenesis: Issues, Problems, Consensus: An Expert Panel Summary Simons, Michael; Bonow, Robert O.; Chronos, Nicolas A. Circulation, Vol. 102, Issue 11 https://doi.org/10.1161/01.CIR.102.11.e73	journal	September 2000
Peptides Targeting Angiogenesis Related Growth Factor Receptors D'Andrea, Luca; Del Gatto, Annarita; De Rosa, Lucia Current Pharmaceutical Design, Vol. 15, Issue 21 https://doi.org/10.2174/138161209788682235	journal	July 2009
Complexity in biomaterials for tissue engineering Place, Elsie S.; Evans, Nicholas D.; Stevens, Molly M. Nature Materials, Vol. 8, Issue 6 https://doi.org/10.1038/nmat2441	journal	June 2009
Supramolecular design of self-assembling nanofibers for cartilage regeneration Shah, Ramille N.; Shah, Nirav A.; Del Rosario Lim, Marc M. Proceedings of the National Academy of Sciences, Vol. 107, Issue 8 https://doi.org/10.1073/pnas.0906501107	journal	February 2010
Targeting angiogenesis: Structural characterization and biological properties of a de novo engineered VEGF mimicking peptide D'Andrea, L. D.; Iaccarino, G.; Fattorusso, R. Proceedings of the National Academy of Sciences, Vol. 102, Issue 40 https://doi.org/10.1073/pnas.0505047102	journal	September 2005
The Powerful Functions of Peptide-Based Bioactive Matrices for Regenerative Medicine Rubert Pérez, Charles M.; Stephanopoulos, Nicholas; Sur, Shantanu Annals of Biomedical Engineering, Vol. 43, Issue 3 https://doi.org/10.1007/s10439-014-1166-6	journal	November 2014
Supramolecular nanostructures that mimic VEGF as a strategy for ischemic tissue repair Webber, M. J.; Tongers, J.; Newcomb, C. J. Proceedings of the National Academy of Sciences, Vol. 108, Issue 33 https://doi.org/10.1073/pnas.1016546108	journal	August 2011
Tissue-Factor Targeted Peptide Amphiphile Nanofibers as an Injectable Therapy To Control Hemorrhage Morgan, Courtney E.; Dombrowski, Amanda W.; Rubert Pérez, Charles M. ACS Nano, Vol. 10, Issue 1 https://doi.org/10.1021/acsnano.5b06025	journal	December 2015
Instructive Nanofiber Scaffolds with VEGF Create a Microenvironment for Arteriogenesis and Cardiac Repair Lin, Y. -D.; Luo, C. -Y.; Hu, Y. -N. Science Translational Medicine, Vol. 4, Issue 146 https://doi.org/10.1126/scitranslmed.3003841	journal	August 2012
Gel Scaffolds of BMP-2-Binding Peptide Amphiphile Nanofibers for Spinal Arthrodesis Lee, Sungsoo S.; Hsu, Erin L.; Mendoza, Marco Advanced Healthcare Materials, Vol. 4, Issue 1 https://doi.org/10.1002/adhm.201400129	journal	April 2014
Spatial regulation of receptor tyrosine kinases in development and cancer Casaletto, Jessica B.; McClatchey, Andrea I. Nature Reviews Cancer, Vol. 12, Issue 6 https://doi.org/10.1038/nrc3277	journal	May 2012
Fibroblast Growth Factors: Biology, Function, and Application for Tissue Regeneration Yun, Ye-Rang; Won, Jong Eun; Jeon, Eunyi Journal of Tissue Engineering, Vol. 1, Issue 1 https://doi.org/10.4061/2010/218142	journal	January 2010
Controlled Growth Factor Delivery for Tissue Engineering Tayalia, Prakriti; Mooney, David J. Advanced Materials, Vol. 21, Issue 32-33 https://doi.org/10.1002/adma.200900241	journal	September 2009
Fibroblast growth factor signalling: from development to cancer Turner, Nicholas; Grose, Richard Nature Reviews Cancer, Vol. 10, Issue 2 https://doi.org/10.1038/nrc2780	journal	February 2010
Role of fibroblast growth factor signaling in vascular formation and maintenance: orchestrating signaling networks as an integrated system: Role of fibroblast growth factor signaling in vascular formation and maintenance Murakami, Masahiro; Sakurai, Takashi Wiley Interdisciplinary Reviews: Systems Biology and Medicine, Vol. 4, Issue 6 https://doi.org/10.1002/wsbm.1190	journal	August 2012
Basic Fibroblast Growth Factor (Fgf2) Is Necessary for Cell Proliferation and Neurogenesis in the Developing Cerebral Cortex Raballo, Rossana; Rhee, Julianne; Lyn-Cook, Richard The Journal of Neuroscience, Vol. 20, Issue 13 https://doi.org/10.1523/JNEUROSCI.20-13-05012.2000	journal	July 2000
Fibroblast Growth Factor-2 Signaling in Neurogenesis and Neurodegeneration Woodbury, Maya E.; Ikezu, Tsuneya Journal of Neuroimmune Pharmacology, Vol. 9, Issue 2 https://doi.org/10.1007/s11481-013-9501-5	journal	September 2013
The enhancement of mature vessel formation and cardiac function in infarcted hearts using dual growth factor delivery with self-assembling peptides Kim, Ji Hyun; Jung, Youngmee; Kim, Sang-Heon Biomaterials, Vol. 32, Issue 26 https://doi.org/10.1016/j.biomaterials.2011.05.003	journal	September 2011
Regenerative Therapies for Central Nervous System Diseases: a Biomaterials Approach Tam, Roger Y.; Fuehrmann, Tobias; Mitrousis, Nikolaos Neuropsychopharmacology, Vol. 39, Issue 1 https://doi.org/10.1038/npp.2013.237	journal	September 2013
Receptor- and heparin-binding domains of basic fibroblast growth factor. Baird, A.; Schubert, D.; Ling, N. Proceedings of the National Academy of Sciences, Vol. 85, Issue 7 https://doi.org/10.1073/pnas.85.7.2324	journal	April 1988
Synthetic peptide F2A4-K-NS mimics fibroblast growth factor-2 in vitro and is angiogenic in vivo Lin, X.; Takahashi, K.; Campion, S. International Journal of Molecular Medicine https://doi.org/10.3892/ijmm.17.5.833	journal	May 2006
Peptide-amphiphile nanofibers: A versatile scaffold for the preparation of self-assembling materials Hartgerink, J. D.; Beniash, E.; Stupp, S. I. Proceedings of the National Academy of Sciences, Vol. 99, Issue 8, p. 5133-5138 https://doi.org/10.1073/pnas.072699999	journal	April 2002
A self-assembly pathway to aligned monodomain gels Zhang, Shuming; Greenfield, Megan A.; Mata, Alvaro Nature Materials, Vol. 9, Issue 7 https://doi.org/10.1038/nmat2778	journal	June 2010
Energy landscapes and functions of supramolecular systems Tantakitti, Faifan; Boekhoven, Job; Wang, Xin Nature Materials, Vol. 15, Issue 4 https://doi.org/10.1038/nmat4538	journal	January 2016
25th Anniversary Article: Supramolecular Materials for Regenerative Medicine Boekhoven, Job; Stupp, Samuel I. Advanced Materials, Vol. 26, Issue 11 https://doi.org/10.1002/adma.201304606	journal	February 2014
Self-assembly for the synthesis of functional biomaterials Stephanopoulos, Nicholas; Ortony, Julia H.; Stupp, Samuel I. Acta Materialia, Vol. 61, Issue 3 https://doi.org/10.1016/j.actamat.2012.10.046	journal	February 2013
Selective Differentiation of Neural Progenitor Cells by High-Epitope Density Nanofibers Silva, Gabriel A.; Czeisler, Catherine; Niece, Krista L. Science, Vol. 303, Issue 5662, p. 1352-1355 https://doi.org/10.1126/science.1093783	journal	February 2004
Self-Assembling Nanofibers Inhibit Glial Scar Formation and Promote Axon Elongation after Spinal Cord Injury Tysseling-Mattiace, V. M.; Sahni, V.; Niece, K. L. Journal of Neuroscience, Vol. 28, Issue 14 https://doi.org/10.1523/JNEUROSCI.0143-08.2008	journal	April 2008
β1-Integrin and Integrin Linked Kinase Regulate Astrocytic Differentiation of Neural Stem Cells Pan, Liuliu; North, Hilary A.; Sahni, Vibhu PLoS ONE, Vol. 9, Issue 8 https://doi.org/10.1371/journal.pone.0104335	journal	August 2014
Bioactive Nanofibers Instruct Cells to Proliferate and Differentiate During Enamel Regeneration Huang, Zhan; Sargeant, Timothy D.; Hulvat, James F. Journal of Bone and Mineral Research, Vol. 23, Issue 12 https://doi.org/10.1359/jbmr.080705	journal	December 2008
Bone regeneration mediated by biomimetic mineralization of a nanofiber matrix Mata, Alvaro; Geng, Yanbiao; Henrikson, Karl J. Biomaterials, Vol. 31, Issue 23 https://doi.org/10.1016/j.biomaterials.2010.04.013	journal	August 2010
Bone regeneration with low dose BMP-2 amplified by biomimetic supramolecular nanofibers within collagen scaffolds Lee, Sungsoo S.; Huang, Brian J.; Kaltz, Stuart R. Biomaterials, Vol. 34, Issue 2 https://doi.org/10.1016/j.biomaterials.2012.10.005	journal	January 2013
A bioactive self-assembled membrane to promote angiogenesis Chow, Lesley W.; Bitton, Ronit; Webber, Matthew J. Biomaterials, Vol. 32, Issue 6 https://doi.org/10.1016/j.biomaterials.2010.10.048	journal	February 2011
Peptide amphiphile nanostructure–heparin interactions and their relationship to bioactivity Rajangam, Kanya; Arnold, Michael S.; Rocco, Mark A. Biomaterials, Vol. 29, Issue 23 https://doi.org/10.1016/j.biomaterials.2008.04.008	journal	August 2008
Cell death versus cell survival instructed by supramolecular cohesion of nanostructures Newcomb, Christina J.; Sur, Shantanu; Ortony, Julia H. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4321	journal	February 2014
Direct Observation of Morphological Tranformation from Twisted Ribbons into Helical Ribbons Pashuck, E. Thomas; Stupp, Samuel I. Journal of the American Chemical Society, Vol. 132, Issue 26 https://doi.org/10.1021/ja100613w	journal	July 2010
Reversible helical unwinding transition of a self-assembling peptide amphiphile Hamley, Ian W.; Dehsorkhi, Ashkan; Castelletto, Valeria Soft Matter, Vol. 9, Issue 39 https://doi.org/10.1039/c3sm51725j	journal	January 2013
Identification and concerted function of two receptor binding surfaces on basic fibroblast growth factor required for mitogenesis. Springer, B. A.; Pantoliano, M. W.; Barbera, F. A. Journal of Biological Chemistry, Vol. 269, Issue 43 https://doi.org/10.1016/S0021-9258(18)47101-3	journal	October 1994
Using circular dichroism spectra to estimate protein secondary structure Greenfield, Norma J Nature Protocols, Vol. 1, Issue 6, p. 2876-2890 https://doi.org/10.1038/nprot.2006.202	journal	January 2007
Structural basis for fibroblast growth factor receptor activation Mohammadi, Moosa; Olsen, Shaun K.; Ibrahimi, Omar A. Cytokine & Growth Factor Reviews, Vol. 16, Issue 2 https://doi.org/10.1016/j.cytogfr.2005.01.008	journal	April 2005
Crystal Structure of a Ternary FGF-FGFR-Heparin Complex Reveals a Dual Role for Heparin in FGFR Binding and Dimerization Schlessinger, Joseph; Plotnikov, Alexander N.; Ibrahimi, Omar A. Molecular Cell, Vol. 6, Issue 3 https://doi.org/10.1016/S1097-2765(00)00073-3	journal	September 2000
Controllable self-assembled laminated nanoribbons from dipeptide-amphiphile bearing azobenzene moiety Lin, Yiyang; Qiao, Yan; Tang, Peifeng Soft Matter, Vol. 7, Issue 6 https://doi.org/10.1039/c0sm01050b	journal	January 2011
Self-assembly of a peptide amphiphile: transition from nanotape fibrils to micelles Miravet, Juan F.; Escuder, Beatriu; Segarra-Maset, Maria Dolores Soft Matter, Vol. 9, Issue 13 https://doi.org/10.1039/c3sm27899a	journal	January 2013
Exploring mechanisms of FGF signalling through the lens of structural biology Goetz, Regina; Mohammadi, Moosa Nature Reviews Molecular Cell Biology, Vol. 14, Issue 3 https://doi.org/10.1038/nrm3528	journal	February 2013
Phosphorylation of histone H3: a balancing act between chromosome condensation and transcriptional activation Nowak, Scott J.; Corces, Victor G. Trends in Genetics, Vol. 20, Issue 4 https://doi.org/10.1016/j.tig.2004.02.007	journal	April 2004
Fibroblast Growth Factor Signaling Pathway in Endothelial Cells Is Activated by BMPER to Promote Angiogenesis Esser, Jennifer S.; Rahner, Susanne; Deckler, Meike Arteriosclerosis, Thrombosis, and Vascular Biology, Vol. 35, Issue 2 https://doi.org/10.1161/ATVBAHA.114.304345	journal	February 2015

Cited By (6)

Dynamic and Responsive Growth Factor Delivery from Electrospun and Hydrogel Tissue Engineering Materials Bruggeman, Kiara F.; Williams, Richard J.; Nisbet, David R. Advanced Healthcare Materials, Vol. 7, Issue 1 https://doi.org/10.1002/adhm.201700836	journal	November 2017
Supramolecular scaffolds enabling the controlled assembly of functional molecular units Ishiwari, Fumitaka; Shoji, Yoshiaki; Fukushima, Takanori Chemical Science, Vol. 9, Issue 8 https://doi.org/10.1039/c7sc04340f	journal	January 2018
The design and biomedical applications of self-assembled two-dimensional organic biomaterials Zhang, Xiaoyuan; Gong, Coucong; Akakuru, Ozioma Udochukwu Chemical Society Reviews, Vol. 48, Issue 23 https://doi.org/10.1039/c8cs01003j	journal	January 2019
Minimalistic supramolecular proteoglycan mimics by co-assembly of aromatic peptide and carbohydrate amphiphiles Brito, Alexandra; Abul-Haija, Yousef M.; da Costa, Diana Soares Chemical Science, Vol. 10, Issue 8 https://doi.org/10.1039/c8sc04361b	journal	January 2019
Synergistic effects of dual-presenting VEGF- and BDNF-mimetic peptide epitopes from self-assembling peptide hydrogels on peripheral nerve regeneration Lu, Jiaju; Yan, Xiaoqing; Sun, Xun Nanoscale, Vol. 11, Issue 42 https://doi.org/10.1039/c9nr04521j	journal	January 2019
Peptide-Based Functional Biomaterials for Soft-Tissue Repair Hosoyama, Katsuhiro; Lazurko, Caitlin; Muñoz, Marcelo Frontiers in Bioengineering and Biotechnology, Vol. 7 https://doi.org/10.3389/fbioe.2019.00205	journal	August 2019

Similar Records

Fibroblast growth factor 2 inhibits up-regulation of bone morphogenic proteins and their receptors during osteoblastic differentiation of human mesenchymal stem cells

Journal Article · Fri Nov 02 00:00:00 EDT 2012 · Biochemical and Biophysical Research Communications · OSTI ID:1821894

Biver, Emmanuel; Soubrier, Anne-Sophie; Thouverey, Cyril; +4 more

Supramolecular Assembly of Peptide Amphiphiles

Journal Article · Wed Sep 06 00:00:00 EDT 2017 · Accounts of Chemical Research · OSTI ID:1821894

Hendricks, Mark P.; Sato, Kohei; Palmer, Liam C.; +1 more

Supramolecular Nanostructure Activates TrkB Receptor Signaling of Neuronal Cells by Mimicking Brain-Derived Neurotrophic Factor

Journal Article · Thu Sep 13 00:00:00 EDT 2018 · Nano Letters · OSTI ID:1821894

Edelbrock, Alexandra N.; Àlvarez, Zaida; Simkin, Dina; +5 more

Related Subjects

36 MATERIALS SCIENCE
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
99 GENERAL AND MISCELLANEOUS
supramolecular biomaterials
peptide amphiphiles
nanoribbons
fibroblast growth factor-2
mimetic peptide
nanostructures
cell signaling
peptides and proteins
two dimensional materials
bioactivity
Nanostructures
Cell signaling
Peptides and proteins
Two dimensional materials
Bioactivity

Title: Mimicking the Bioactivity of Fibroblast Growth Factor-2 Using Supramolecular Nanoribbons

Citation Formats

References (58)

Cited By (6)

Similar Records

Related Subjects