Physical and biological regulation of neuron regenerative growth and network formation on recombinant dragline silks
Abstract
In this paper, recombinant spider silks produced in transgenic goat milk were studied as cell culture matrices for neuronal growth. Major ampullate spidroin 1 (MaSp1) supported neuronal growth, axon extension and network connectivity, with cell morphology comparable to the gold standard poly-lysine. In addition, neurons growing on MaSp1 films had increased neural cell adhesion molecule (NCAM) expression at both mRNA and protein levels. The results indicate that MaSp1 films present useful surface charge and substrate stiffness to support the growth of primary rat cortical neurons. Moreover, a putative neuron-specific surface binding sequence GRGGL within MaSp1 may contribute to the biological regulation of neuron growth. These findings indicate that MaSp1 could regulate neuron growth through its physical and biological features. Finally, this dual regulation mode of MaSp1 could provide an alternative strategy for generating functional silk materials for neural tissue engineering.
- Authors:
-
- Tufts Univ., Medford, MA (United States). Dept. of Biomedical Engineering
- Utah State Univ., Logan, UT (United States). Dept. of Biology
- Publication Date:
- Research Org.:
- Utah State Univ., Logan, UT (United States); Tufts Univ., Medford, MA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC): National Institutes of Health (NIH); USDOE
- OSTI Identifier:
- 1344119
- Alternate Identifier(s):
- OSTI ID: 1365582
- Grant/Contract Number:
- SC0004791; IIP-1318194; R01 EB014283; P41 EB002520; R01 EY020856
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Biomaterials
- Additional Journal Information:
- Journal Volume: 48; Journal ID: ISSN 0142-9612
- Publisher:
- Elsevier
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; Biomaterial; Neural cell; Silk; Recombinant protein; Tissue engineering
Citation Formats
An, Bo, Tang-Schomer, Min D., Huang, Wenwen, He, Jiuyang, Jones, Justin A., Lewis, Randolph V., and Kaplan, David L. Physical and biological regulation of neuron regenerative growth and network formation on recombinant dragline silks. United States: N. p., 2015.
Web. doi:10.1016/j.biomaterials.2015.01.044.
An, Bo, Tang-Schomer, Min D., Huang, Wenwen, He, Jiuyang, Jones, Justin A., Lewis, Randolph V., & Kaplan, David L. Physical and biological regulation of neuron regenerative growth and network formation on recombinant dragline silks. United States. https://doi.org/10.1016/j.biomaterials.2015.01.044
An, Bo, Tang-Schomer, Min D., Huang, Wenwen, He, Jiuyang, Jones, Justin A., Lewis, Randolph V., and Kaplan, David L. Wed .
"Physical and biological regulation of neuron regenerative growth and network formation on recombinant dragline silks". United States. https://doi.org/10.1016/j.biomaterials.2015.01.044. https://www.osti.gov/servlets/purl/1344119.
@article{osti_1344119,
title = {Physical and biological regulation of neuron regenerative growth and network formation on recombinant dragline silks},
author = {An, Bo and Tang-Schomer, Min D. and Huang, Wenwen and He, Jiuyang and Jones, Justin A. and Lewis, Randolph V. and Kaplan, David L.},
abstractNote = {In this paper, recombinant spider silks produced in transgenic goat milk were studied as cell culture matrices for neuronal growth. Major ampullate spidroin 1 (MaSp1) supported neuronal growth, axon extension and network connectivity, with cell morphology comparable to the gold standard poly-lysine. In addition, neurons growing on MaSp1 films had increased neural cell adhesion molecule (NCAM) expression at both mRNA and protein levels. The results indicate that MaSp1 films present useful surface charge and substrate stiffness to support the growth of primary rat cortical neurons. Moreover, a putative neuron-specific surface binding sequence GRGGL within MaSp1 may contribute to the biological regulation of neuron growth. These findings indicate that MaSp1 could regulate neuron growth through its physical and biological features. Finally, this dual regulation mode of MaSp1 could provide an alternative strategy for generating functional silk materials for neural tissue engineering.},
doi = {10.1016/j.biomaterials.2015.01.044},
journal = {Biomaterials},
number = ,
volume = 48,
place = {United States},
year = {Wed Feb 11 00:00:00 EST 2015},
month = {Wed Feb 11 00:00:00 EST 2015}
}
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Works referenced in this record:
New perspectives in cell adhesion: RGD and integrins
journal, October 1987
- Ruoslahti, E.; Pierschbacher, M.
- Science, Vol. 238, Issue 4826
Isolation of a clone encoding a second dragline silk fibroin. Nephila clavipes dragline silk is a two-protein fiber.
journal, September 1992
- Hinman, M. B.; Lewis, R. V.
- Journal of Biological Chemistry, Vol. 267, Issue 27
Enhanced neurite growth from mammalian neurons in three-dimensional salmon fibrin gels
journal, April 2007
- Ju, Yo-El; Janmey, Paul A.; McCormick, Margaret E.
- Biomaterials, Vol. 28, Issue 12
Nanocomposites of poly(vinylidene fluoride) with multiwalled carbon nanotubes
journal, March 2010
- Huang, Wenwen; Edenzon, Kyle; Fernandez, Luis
- Journal of Applied Polymer Science, Vol. 115, Issue 6
Native-sized recombinant spider silk protein produced in metabolically engineered Escherichia coli results in a strong fiber
journal, July 2010
- Xia, X. -X.; Qian, Z. -G.; Ki, C. S.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 32
Nephila clavipes Flagelliform Silk-Like GGX Motifs Contribute to Extensibility and Spacer Motifs Contribute to Strength in Synthetic Spider Silk Fibers
journal, May 2013
- Adrianos, Sherry L.; Teulé, Florence; Hinman, Michael B.
- Biomacromolecules, Vol. 14, Issue 6
Combining flagelliform and dragline spider silk motifs to produce tunable synthetic biopolymer fibers
journal, October 2011
- Teulé, Florence; Addison, Bennett; Cooper, Alyssa R.
- Biopolymers, Vol. 97, Issue 6
Regulators of Neurite Outgrowth: Role of Cell Adhesion Molecules
journal, April 2004
- Kiryushko, Darya; Berezin, Vladimir; Bock, Elisabeth
- Annals of the New York Academy of Sciences, Vol. 1014, Issue 1
The structure and properties of spider silk
journal, January 1986
- Gosline, John M.; DeMont, M. Edwin; Denny, Mark W.
- Endeavour, Vol. 10, Issue 1
Untangling spider silk evolution with spidroin terminal domains
journal, January 2010
- Garb, Jessica E.; Ayoub, Nadia A.; Hayashi, Cheryl Y.
- BMC Evolutionary Biology, Vol. 10, Issue 1
Matrices with Compliance Comparable to that of Brain Tissue Select Neuronal over Glial Growth in Mixed Cortical Cultures
journal, April 2006
- Georges, Penelope C.; Miller, William J.; Meaney, David F.
- Biophysical Journal, Vol. 90, Issue 8
An Essential Role for the C-Terminal Domain of A Dragline Spider Silk Protein in Directing Fiber Formation
journal, June 2006
- Ittah, Shmulik; Cohen, Shulamit; Garty, Shai
- Biomacromolecules, Vol. 7, Issue 6
Prion protein recruits its neuronal receptor NCAM to lipid rafts to activate p59fyn and to enhance neurite outgrowth
journal, April 2005
- Santuccione, Antonella; Sytnyk, Vladimir; Leshchyns'ka, Iryna
- Journal of Cell Biology, Vol. 169, Issue 2
Arg-Gly-Asp: A versatile cell recognition signal
journal, February 1986
- Ruoslahti, Erkki; Pierschbacher, Michael D.
- Cell, Vol. 44, Issue 4
The Collagen-binding A-domains of Integrins α 1 β 1 and α 2 β 1 Recognize the Same Specific Amino Acid Sequence, GFOGER, in Native (Triple-helical) Collagens
journal, January 2000
- Knight, C. Graham; Morton, Laurence F.; Peachey, Anthony R.
- Journal of Biological Chemistry, Vol. 275, Issue 1
Binding properties of a cell adhesion molecule from neural tissue.
journal, January 1982
- Rutishauser, U.; Hoffman, S.; Edelman, G. M.
- Proceedings of the National Academy of Sciences, Vol. 79, Issue 2
Strength in the Periphery: Growth Cone Biomechanics and Substrate Rigidity Response in Peripheral and Central Nervous System Neurons
journal, February 2012
- Koch, Daniel; Rosoff, William J.; Jiang, Jiji
- Biophysical Journal, Vol. 102, Issue 3
The treatment of TBI with human marrow stromal cells impregnated into collagen scaffold: Functional outcome and gene expression profile
journal, January 2011
- Qu, Changsheng; Mahmood, Asim; Liu, Xian Shuang
- Brain Research, Vol. 1371
Structural characterization of a homophilic binding site in the neural cell adhesion molecule.
journal, September 1993
- Rao, Y.; Wu, X. F.; Yip, P.
- Journal of Biological Chemistry, Vol. 268, Issue 27
Silk Hydrogels as Soft Substrates for Neural Tissue Engineering
journal, April 2013
- Hopkins, Amy M.; De Laporte, Laura; Tortelli, Federico
- Advanced Functional Materials, Vol. 23, Issue 41
Hypotheses that correlate the sequence, structure, and mechanical properties of spider silk proteins
journal, March 1999
- Hayashi, Cheryl Y.; Shipley, Nichola H.; Lewis, Randolph V.
- International Journal of Biological Macromolecules, Vol. 24, Issue 2-3
Liquid crystalline spinning of spider silk
journal, March 2001
- Vollrath, Fritz; Knight, David P.
- Nature, Vol. 410, Issue 6828
Differential distribution of aggrecan isoforms in perineuronal nets of the human cerebral cortex
journal, February 2009
- Virgintino, Daniela; Perissinotto, Daniela; Girolamo, Francesco
- Journal of Cellular and Molecular Medicine, Vol. 13, Issue 9b
Bioengineered sequential growth factor delivery stimulates brain tissue regeneration after stroke
journal, November 2013
- Wang, Yuanfei; Cooke, Michael J.; Sachewsky, Nadia
- Journal of Controlled Release, Vol. 172, Issue 1
Film-Based Implants for Supporting Neuron-Electrode Integrated Interfaces for The Brain
journal, November 2013
- Tang-Schomer, Min D.; Hu, Xiao; Hronik-Tupaj, Marie
- Advanced Functional Materials, Vol. 24, Issue 13
Charge-Tunable Autoclaved Silk-Tropoelastin Protein Alloys That Control Neuron Cell Responses
journal, March 2013
- Hu, Xiao; Tang-Schomer, Min D.; Huang, Wenwen
- Advanced Functional Materials, Vol. 23, Issue 31
A biomaterials approach to peripheral nerve regeneration: bridging the peripheral nerve gap and enhancing functional recovery
journal, November 2011
- Daly, W.; Yao, L.; Zeugolis, D.
- Journal of The Royal Society Interface, Vol. 9, Issue 67
Inducing β-Sheets Formation in Synthetic Spider Silk Fibers by Aqueous Post-Spin Stretching
journal, June 2011
- An, Bo; Hinman, Michael B.; Holland, Gregory P.
- Biomacromolecules, Vol. 12, Issue 6
Reproducing Natural Spider Silks’ Copolymer Behavior in Synthetic Silk Mimics
journal, November 2012
- An, Bo; Jenkins, Janelle E.; Sampath, Sujatha
- Biomacromolecules, Vol. 13, Issue 12
Regenerative potential of silk conduits in repair of peripheral nerve injury in adult rats
journal, January 2012
- Huang, W.; Begum, R.; Barber, T.
- Biomaterials, Vol. 33, Issue 1
Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration
journal, December 2006
- Maness, Patricia F.; Schachner, Melitta
- Nature Neuroscience, Vol. 10, Issue 1
An Engineered α1 Integrin-binding Collagenous Sequence
journal, October 2010
- Seo, Neungseon; Russell, Brooke H.; Rivera, Jose J.
- Journal of Biological Chemistry, Vol. 285, Issue 40
Ankyrin binding activity shared by the neurofascin/L1/NrCAM family of nervous system cell adhesion molecules.
journal, November 1994
- Davis, J. Q.; Bennett, V.
- Journal of Biological Chemistry, Vol. 269, Issue 44
Making recombinant extracellular matrix proteins
journal, May 2008
- Ruggiero, Florence; Koch, Manuel
- Methods, Vol. 45, Issue 1
Stem cell-based tissue engineering with silk biomaterials
journal, December 2006
- Wang, Yongzhong; Kim, Hyeon-Joo; Vunjak-Novakovic, Gordana
- Biomaterials, Vol. 27, Issue 36
Spider Silk Constructs Enhance Axonal Regeneration and Remyelination in Long Nerve Defects in Sheep
journal, February 2011
- Radtke, Christine; Allmeling, Christina; Waldmann, Karl-Heinz
- PLoS ONE, Vol. 6, Issue 2
Design and Characterization of a Synthetically Accessible, Photodegradable Hydrogel for User-Directed Formation of Neural Networks
journal, June 2014
- McKinnon, Daniel D.; Brown, Tobin E.; Kyburz, Kyle A.
- Biomacromolecules, Vol. 15, Issue 7
Recombinant spider silk matrices for neural stem cell cultures
journal, November 2012
- Lewicka, Michalina; Hermanson, Ola; Rising, Anna U.
- Biomaterials, Vol. 33, Issue 31
Tunable Self-Assembly of Genetically Engineered Silk–Elastin-like Protein Polymers
journal, November 2011
- Xia, Xiao-Xia; Xu, Qiaobing; Hu, Xiao
- Biomacromolecules, Vol. 12, Issue 11
Spider dragline silk proteins in transgenic tobacco leaves: accumulation and field production: Spider silk proteins in tobacco
journal, August 2004
- Menassa, Rima; Zhu, Hong; Karatzas, Costas N.
- Plant Biotechnology Journal, Vol. 2, Issue 5
Interactions between Spider Silk and Cells – NIH/3T3 Fibroblasts Seeded on Miniature Weaving Frames
journal, August 2010
- Kuhbier, Joern W.; Allmeling, Christina; Reimers, Kerstin
- PLoS ONE, Vol. 5, Issue 8
Spider Silk: Ancient Ideas for New Biomaterials
journal, September 2006
- Lewis, Randolph V.
- Chemical Reviews, Vol. 106, Issue 9
The injured brain interacts reciprocally with neural stem cells supported by scaffolds to reconstitute lost tissue
journal, October 2002
- Park, Kook In; Teng, Yang D.; Snyder, Evan Y.
- Nature Biotechnology, Vol. 20, Issue 11
Activation of the FGF receptor underlies neurite outgrowth stimulated by L1, N-CAM, and N-cadherin
journal, September 1994
- Williams, Emma J.; Furness, Josie; Walsh, Frank S.
- Neuron, Vol. 13, Issue 3
NeurphologyJ: An automatic neuronal morphology quantification method and its application in pharmacological discovery
journal, January 2011
- Ho, Shinn-Ying; Chao, Chih-Yuan; Huang, Hui-Ling
- BMC Bioinformatics, Vol. 12, Issue 1
Structure of a protein superfiber: spider dragline silk.
journal, September 1990
- Xu, M.; Lewis, R. V.
- Proceedings of the National Academy of Sciences, Vol. 87, Issue 18
Spider silk fibres in artificial nerve constructs promote peripheral nerve regeneration
journal, June 2008
- Allmeling, C.; Jokuszies, A.; Reimers, K.
- Cell Proliferation, Vol. 41, Issue 3
Production of synthetic spider dragline silk protein in Pichia pastoris
journal, January 1997
- Fahnestock, S. R.; Bedzyk, L. A.
- Applied Microbiology and Biotechnology, Vol. 47, Issue 1
The role of terminal domains during storage and assembly of spider silk proteins
journal, November 2011
- Eisoldt, Lukas; Thamm, Christopher; Scheibel, Thomas
- Biopolymers, Vol. 97, Issue 6
The homophilic binding site of the neural cell adhesion molecule NCAM is directly involved in promoting neurite outgrowth from cultured neural retinal cells.
journal, May 1994
- Sandig, M.; Rao, Y.; Siu, C. H.
- Journal of Biological Chemistry, Vol. 269, Issue 20
Recombinant spider silk as matrices for cell culture
journal, December 2010
- Widhe, Mona; Bysell, Helena; Nystedt, Sara
- Biomaterials, Vol. 31, Issue 36
The influence of specific binding of collagen–silk chimeras to silk biomaterials on hMSC behavior
journal, January 2013
- An, Bo; DesRochers, Teresa M.; Qin, Guokui
- Biomaterials, Vol. 34, Issue 2
The Neural Cell Adhesion Molecule NCAM Is an Alternative Signaling Receptor for GDNF Family Ligands
journal, June 2003
- Paratcha, Gustavo; Ledda, Fernanda; Ibáñez, Carlos F.
- Cell, Vol. 113, Issue 7
Spider Silk Fibers Spun from Soluble Recombinant Silk Produced in Mammalian Cells
journal, January 2002
- Lazaris, A.
- Science, Vol. 295, Issue 5554
Mechanical and Physical Properties of Recombinant Spider Silk Films Using Organic and Aqueous Solvents
journal, July 2014
- Tucker, Chauncey L.; Jones, Justin A.; Bringhurst, Heidi N.
- Biomacromolecules, Vol. 15, Issue 8
Neural responses to electrical stimulation on patterned silk films: Electrical Stimulation on Patterned Silk Films
journal, July 2013
- Hronik-Tupaj, Marie; Raja, Waseem Khan; Tang-Schomer, Min
- Journal of Biomedical Materials Research Part A, Vol. 101A, Issue 9
Cell adhesion and motility depend on nanoscale RGD clustering
journal, May 2000
- Maheshwari, G.; Brown, G.; Lauffenburger, D. A.
- Journal of Cell Science, Vol. 113, Issue 10
Works referencing / citing this record:
Three-dimensional hyaluronic acid hydrogel-based models for in vitro human iPSC-derived NPC culture and differentiation
journal, January 2017
- Wu, Shaohua; Xu, Ranjie; Duan, Bin
- Journal of Materials Chemistry B, Vol. 5, Issue 21
Chitosan/gelatin porous scaffolds assembled with conductive poly(3,4-ethylenedioxythiophene) nanoparticles for neural tissue engineering
journal, January 2017
- Wang, Shuping; Sun, Changkai; Guan, Shui
- Journal of Materials Chemistry B, Vol. 5, Issue 24
In vitro bioengineered model of cortical brain tissue
journal, August 2015
- Chwalek, Karolina; Tang-Schomer, Min D.; Omenetto, Fiorenzo G.
- Nature Protocols, Vol. 10, Issue 9
Bioactive Silk‐Based Nerve Guidance Conduits for Augmenting Peripheral Nerve Repair
journal, September 2018
- Magaz, Adrián; Faroni, Alessandro; Gough, Julie E.
- Advanced Healthcare Materials, Vol. 7, Issue 23
Intracellular Pathways Involved in Bone Regeneration Triggered by Recombinant Silk-Silica Chimeras
journal, September 2017
- Martín-Moldes, Zaira; Ebrahimi, Davoud; Plowright, Robyn
- Advanced Functional Materials, Vol. 28, Issue 27
Mimicking the Brain Extracellular Matrix in Vitro : A Review of Current Methodologies and Challenges
journal, July 2019
- Rauti, Rossana; Renous, Noa; Maoz, Ben M.
- Israel Journal of Chemistry
Tissue Engineered Neural Constructs Composed of Neural Precursor Cells, Recombinant Spidroin and PRP for Neural Tissue Regeneration
journal, February 2019
- Baklaushev, V. P.; Bogush, V. G.; Kalsin, V. A.
- Scientific Reports, Vol. 9, Issue 1
Nerve guidance conduit design based on self-rolling tubes
journal, January 2020
- Aigner, T. B.; Haynl, C.; Salehi, S.
- Materials Today Bio, Vol. 5
Biomedical Applications of Recombinant Silk-Based Materials
journal, February 2018
- Aigner, Tamara Bernadette; DeSimone, Elise; Scheibel, Thomas
- Advanced Materials, Vol. 30, Issue 19
Tissue Engineered Neural Constructs Composed of Neural Precursor Cells, Recombinant Spidroin and PRP for Neural Tissue Regeneration
journal, February 2019
- Baklaushev, V. P.; Bogush, V. G.; Kalsin, V. A.
- Scientific Reports, Vol. 9, Issue 1
Effect of Silk Fibroin on Neuroregeneration After Traumatic Brain Injury
journal, December 2018
- Moisenovich, M. M.; Plotnikov, E. Y.; Moysenovich, A. M.
- Neurochemical Research, Vol. 44, Issue 10
Design of Multistimuli Responsive Hydrogels Using Integrated Modeling and Genetically Engineered Silk-Elastin-Like Proteins
journal, April 2016
- Huang, Wenwen; Tarakanova, Anna; Dinjaski, Nina
- Advanced Functional Materials, Vol. 26, Issue 23
Predicting rates of in vivo degradation of recombinant spider silk proteins: Integrated modelling and experimental approach for predicting protein degradation
journal, May 2017
- Dinjaski, Nina; Ebrahimi, Davoud; Qin, Zhao
- Journal of Tissue Engineering and Regenerative Medicine, Vol. 12, Issue 1