BMHP1-derived self-assembling peptides: Hierarchically assembled structures with self-healing propensity and potential for tissue engineering applications

ACS Nano

Volumn 5, Issue 3, 2011, Pages 1845-1859

  Gelain, Fabrizio ^a,b,c   Silva, Diego ^a,b   Caprini, Andrea ^a,b   Taraballi, Francesca ^a,b   Natalello, Antonino ^b,d   Villa, Omar ^a,b   Nam, Ki Tae ^e,f   Zuckermann, Ronald N ^e   Doglia, Silvia Maria ^b,d   Vescovi, Angelo ^a,b,c  

^a OSPEDALE NIGUARDA CA GRANDA   (Italy)

^b UNIVERSITY OF MILANO BICOCCA   (Italy)

^c CASA SOLLIEVO DELLA SOFFERENZA HOSPITAL   (Italy)

^d UdR Milan Bicocca ^*  (Italy)

^e LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^f Seoul National University   (South Korea)

Author keywords

biotinylation; neural stem cell; self assembling peptide; self healing scaffold

Indexed keywords

BIO-INSPIRED; BIOTINYLATIONS; BONE MARROW; FTIR; FUNCTIONAL MOTIFS; FUNCTIONALIZATIONS; FUNCTIONALIZED; HOMING PEPTIDE; HYBRID PEPTIDES; IN-VITRO; IN-VIVO EXPERIMENTS; MATERIAL SCIENCE; MICRO-SCALES; NANOSTRUCTURE MORPHOLOGIES; NERVOUS TISSUES; NEURAL STEM CELL; ORGANIZED STRUCTURE; POTENTIAL APPLICATIONS; REGENERATIVE MEDICINE; SECONDARY STRUCTURES; SELF-ASSEMBLED; SELF-ASSEMBLING; SELF-ASSEMBLING PEPTIDE; SELF-ASSEMBLING PEPTIDES; SELF-HEALING; SELF-HEALING SCAFFOLD; TISSUE ENGINEERING APPLICATIONS; TWISTED RIBBON;

ANIMAL CELL CULTURE; CELL CULTURE; EXPERIMENTS; PEPTIDES; SELF ASSEMBLY; STEM CELLS; X RAY DIFFRACTION;

SCAFFOLDS (BIOLOGY);

NERVE GROWTH FACTOR;

ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECT; FEASIBILITY STUDY; HUMAN; METHODOLOGY; NERVE CELL; NEURAL STEM CELL; PHYSIOLOGY; SYNTHESIS; TISSUE ENGINEERING;

CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; FEASIBILITY STUDIES; HUMANS; NERVE GROWTH FACTORS; NEURAL STEM CELLS; NEURONS; TISSUE ENGINEERING;

EID: 79952937011     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn102663a     Document Type: Article

References (57)

1. Tibbitt, M. W.; Anseth, K. S. Hydrogels as Extracellular Matrix Mimics for 3d Cell Culture Biotechnol. Bioeng. 2009, 103, 655-663
2. Hamidi, M.; Azadi, A.; Rafiei, P. Hydrogel Nanoparticles in Drug Delivery Adv. Drug Delivery Rev. 2008, 60, 1638-1649
3. Nisbet, D. R.; Crompton, K. E.; Horne, M. K.; Finkelstein, D. I.; Forsythe, J. S. Neural Tissue Engineering of the CNS Using Hydrogels J. Biomed. Mater. Res. B 2008, 87, 251-263
4. Anumolu, S. S.; Desantis, A. S.; Menjoge, A. R.; Hahn, R. A.; Beloni, J. A.; Gordon, M. K.; Sinko, P. J. Doxycycline Loaded Poly(ethylene glycol) Hydrogels for Healing Vesicant-Induced Ocular Wounds Biomaterials 2010, 31, 964-974
5. Negredo, E.; Puig, J.; Aldea, D.; Medina, M.; Estany, C.; Perez-Alvarez, N.; Rodriguez-Fumaz, C.; Munoz-Moreno, J. A.; Higueras, C.; Gonzalez-Mestre, V et al. Four-Year Safety with Polyacrylamide Hydrogel To Correct Antiretroviral-Related Facial Lipoatrophy AIDS Res. Hum. Retroviruses 2009, 25, 451-455
6. Bader, R. A.; Rochefort, W. E. Rheological Characterization of Photopolymerized Poly(vinyl alcohol) Hydrogels for Potential Use in Nucleus Pulposus Replacement J. Biomed. Mater. Res. A 2008, 86, 494-501 (Pubitemid 351969648)
7. Bhattarai, N.; Gunn, J.; Zhang, M. Chitosan-Based Hydrogels for Controlled, Localized Drug Delivery Adv. Drug Delivery Rev. 2010, 62, 83-99
8. Ho, S. T.; Cool, S. M.; Hui, J. H.; Hutmacher, D. W. The Influence of Fibrin Based Hydrogels on the Chondrogenic Differentiation of Human Bone Marrow Stromal Cells Biomaterials 2010, 31, 38-47
9. Kleinman, H. K.; McGarvey, M. L.; Hassell, J. R.; Star, V. L.; Cannon, F. B.; Laurie, G. W.; Martin, G. R. Basement Membrane Complexes with Biological Activity Biochemistry 1986, 25, 312-318 (Pubitemid 16053790)
10. Kisiday, J.; Jin, M.; Kurz, B.; Hung, H.; Semino, C.; Zhang, S.; Grodzinsky, A. J. Self-Assembling Peptide Hydrogel Fosters Chondrocyte Extracellular Matrix Production and Cell Division: Implications for Cartilage Tissue Repair Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 9996-10001 (Pubitemid 34831161)
11. Gelain, F.; Bottai, D.; Vescovi, A.; Zhang, S. Designer Self-Assembling Peptide Nanofiber Scaffolds for Adult Mouse Neural Stem Cell 3-Dimensional Cultures PLoS ONE 2006, 1, e119
12. Zhang, S.; Gelain, F.; Zhao, X. Designer Self-Assembling Peptide Nanofiber Scaffolds for 3d Tissue Cell Cultures Semin. Cancer Biol. 2005, 15, 413-420 (Pubitemid 41140309)
13. Ellis-Behnke, R. G.; Liang, Y. X.; You, S. W.; Tay, D. K.; Zhang, S.; So, K. F.; Schneider, G. E. Nano Neuro Knitting: Peptide Nanofiber Scaffold for Brain Repair and Axon Regeneration with Functional Return of Vision Proc Natl Acad Sci U S A 2006, 103, 5054-5059
14. Rajagopal, K.; Schneider, J. P. Self-Assembling Peptides and Proteins for Nanotechnological Applications Curr Opin Struct Biol 2004, 14, 480-486 (Pubitemid 39099286)
15. Zhang, S.; Holmes, T.; Lockshin, C.; Rich, A. Spontaneous Assembly of a Self-Complementary Oligopeptide To Form a Stable Macroscopic Membrane Proc. Natl. Acad. Sci. U.S.A. 1993, 90, 3334-3338 (Pubitemid 23111360)
16. Gazit, E. Self-Assembled Peptide Nanostructures: The Design of Molecular Building Blocks and Their Technological Utilization Chem. Soc. Rev. 2007, 36, 1263-1269
17. Holmes, T. C.; de Lacalle, S.; Su, X.; Liu, G.; Rich, A.; Zhang, S. Extensive Neurite Outgrowth and Active Synapse Formation on Self-Assembling Peptide Scaffolds Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 6728-6733 (Pubitemid 30412782)
18. Gelain, F.; Unsworth, L. D.; Zhang, S. Slow and Sustained Release of Active Cytokines from Self-Assembling Peptide Scaffolds J. Controlled Release 2010, 145, 231-239
19. Ellis-Behnke, R. G.; Liang, Y. X.; Tay, D. K.; Kau, P. W.; Schneider, G. E.; Zhang, S.; Wu, W.; So, K. F. Nano Hemostat Solution: Immediate Hemostasis at the Nanoscale Nanomedicine 2006, 2, 207-215 (Pubitemid 44895530)
20. Segers, V. F.; Lee, R. T. Local Delivery of Proteins and the Use of Self-Assembling Peptides Drug Discovery Today 2007, 12, 561-568 (Pubitemid 47031660)
21. Silva, G. A.; Czeisler, C.; Niece, K. L.; Beniash, E.; Harrington, D. A.; Kessler, J. A.; Stupp, S. I. Selective Differentiation of Neural Progenitor Cells by High-Epitope Density Nanofibers Science 2004, 303, 1352-1355 (Pubitemid 38269424)
22. Tysseling, V. M.; Sahni, V.; Pashuck, E. T.; Birch, D.; Hebert, A.; Czeisler, C.; Stupp, S. I.; Kessler, J. A. Self-Assembling Peptide Amphiphile Promotes Plasticity of Serotonergic Fibers Following Spinal Cord Injury J. Neurosci. Res. 2010, 88, 3161-3170
23. Taraballi, F.; Campione, M.; Sassella, A.; Vescovi, A.; Paleari, A.; Hwang, W.; Gelain, F. Effect of Functionalization on the Self-Assembling Propensity of Beta-Sheet Forming Peptides Soft Matter 2009, 5, 660-668
24. Jitrapakdee, S.; Wallace, J. C. The Biotin Enzyme Family: Conserved Structural Motifs and Domain Rearrangements Curr. Protein Pept. Sci. 2003, 4, 217-229 (Pubitemid 36656735)
25. Lei, Y.; Li, H.; Zhang, R.; Han, S. Theoretical Study of Cooperativity in Biotin J. Phys. Chem. B 2007, 111, 14370-14377
26. Freitag, S.; Le Trong, I.; Klumb, L. A.; Chu, V.; Chilkoti, A.; Stayton, P. S.; Stenkamp, R. E. X-ray Crystallographic Studies of Streptavidin Mutants Binding to Biotin Biomol. Eng. 1999, 16, 13-19 (Pubitemid 30184834)
27. Saggio, I.; Laufer, R. Biotin Binders Selected from a Random Peptide Library Expressed on Phage Biochem. J. 1993, 295, 903
28. Zhao, X.; Zhang, S. Molecular Designer Self-Assembling Peptides Chem. Soc. Rev. 2006, 35, 1105-1110 (Pubitemid 44611723)
29. DSouza, S. E.; Ginsberg, M. H.; Plow, E. F. Arginyl-Glycyl-Aspartic Acid (RGD): A Cell Adhesion Motif Trends Biochem. Sci. 1991, 16, 246-250 (Pubitemid 121004445)
30. Genove, E.; Shen, C.; Zhang, S.; Semino, C. E. The Effect of Functionalized Self-Assembling Peptide Scaffolds on Human Aortic Endothelial Cell Function Biomaterials 2005, 26, 3341-3351 (Pubitemid 39647267)
31. Schneider, J. P.; Pochan, D. J.; Ozbas, B.; Rajagopal, K.; Pakstis, L.; Kretsinger, J. Responsive Hydrogels from the Intramolecular Folding and Self-Assembly of a Designed Peptide J. Am. Chem. Soc. 2002, 124, 15030-15037 (Pubitemid 36014111)
32. Aulisa, L.; Dong, H.; Hartgerink, J. D. Self-Assembly of Multidomain Peptides: Sequence Variation Allows Control over Cross-Linking and Viscoelasticity Biomacromolecules 2009, 10, 2694-2698
33. Castelletto, V.; Hamley, I. W.; Cenker, C.; Olsson, U. Influence of Salt on the Self-Assembly of Two Model Amyloid Heptapeptides J. Phys. Chem. B 2010, 114, 8002-8008
34. Veerman, C.; Sagis, L. M.; Heck, J.; van der Linden, E. Mesostructure of Fibrillar Bovine Serum Albumin Gels Int. J. Biol. Macromol. 2003, 31, 139-146 (Pubitemid 36144033)
35. Reches, M.; Gazit, E. Casting Metal Nanowires within Discrete Self-Assembled Peptide Nanotubes Science 2003, 300, 625-627 (Pubitemid 36520583)
36. Joshi, K. B.; Verma, S. Sequence Shuffle Controls Morphological Consequences in a Self-Assembling Tetrapeptide J. Pept. Sci. 2008, 14, 118-126 (Pubitemid 351284907)
37. Aggeli, A.; Nyrkova, I. A.; Bell, M.; Harding, R.; Carrick, L.; McLeish, T. C.; Semenov, A. N.; Boden, N. Hierarchical Self-Assembly of Chiral Rodlike Molecules as a Model for Peptide β-Sheet Tapes, Ribbons, Fibrils, and Fibers Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 11857-11862 (Pubitemid 32959792)
38. Zhang, S.; Marini, D. M.; Hwang, W.; Santoso, S. Design of Nanostructured Biological Materials through Self-Assembly of Peptides and Proteins Curr. Opin. Chem. Biol. 2002, 6, 865-871 (Pubitemid 35449349)
39. Sunde, M.; Serpell, L. C.; Bartlam, M.; Fraser, P. E.; Pepys, M. B.; Blake, C. C. Common Core Structure of Amyloid Fibrils by Synchrotron X-ray Diffraction J. Mol. Biol. 1997, 273, 729-739 (Pubitemid 27488813)
40. Perutz, M. F.; Finch, J. T.; Berriman, J.; Lesk, A. Amyloid Fibers Are Water-Filled Nanotubes Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 5591-5595 (Pubitemid 34411593)
41. Burley, S. K.; Petsko, G. A. Aromatic-Aromatic Interaction: A Mechanism of Protein Structure Stabilization Science 1985, 229, 23-28
42. Gsponer, J.; Haberthur, U.; Caflisch, A. The Role of Side-Chain Interactions in the Early Steps of Aggregation: Molecular Dynamics Simulations of an Amyloid-Forming Peptide from the Yeast Prion Sup35 Proc. Natl. Acad. Sci. U.S.A 2003, 100, 5154-5159 (Pubitemid 36542674)
43. Barth, A. Infrared Spectroscopy of Proteins Biochim. Biophys. Acta 2007, 1767, 1073-1101 (Pubitemid 47313388)
44. Susi, H.; Byler, D. M. Resolution-Enhanced Fourier Transform Infrared Spectroscopy of Enzymes Methods Enzymol. 1986, 130, 290-311
45. Natalello, A.; Prokorov, V. V.; Tagliavini, F.; Morbin, M.; Forloni, G.; Beeg, M.; Manzoni, C.; Colombo, L.; Gobbi, M.; Salmona, M et al. Conformational Plasticity of the Gerstmann-Straussler-Scheinker Disease Peptide as Indicated by Its Multiple Aggregation Pathways J. Mol. Biol. 2008, 381, 1349-1361
46. Fabian, H.; Naumann, D.; Misselwitz, R.; Ristau, O.; Gerlach, D.; Welfle, H. Secondary Structure of Streptokinase in Aqueous Solution: A Fourier Transform Infrared Spectroscopic Study Biochemistry 1992, 31, 6532-6538
47. Arrondo, J. L.; Goni, F. M. Structure and Dynamics of Membrane Proteins as Studied by Infrared Spectroscopy Prog. Biophys. Mol. Biol. 1999, 72, 367-405
48. Li, S. C.; Goto, N. K.; Williams, K. A.; Deber, C. M. α-Helical, but Not β-Sheet, Propensity of Proline Is Determined by Peptide Environment Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 6676-6681 (Pubitemid 26230368)
49. Vescovi, A. L.; Parati, E. A.; Gritti, A.; Poulin, P.; Ferrario, M.; Wanke, E.; Frolichsthal-Schoeller, P.; Cova, L.; Arcellana-Panlilio, M.; Colombo, A et al. Isolation and Cloning of Multipotential Stem Cells from the Embryonic Human CNS and Establishment of Transplantable Human Neural Stem Cell Lines by Epigenetic Stimulation Exp. Neurol. 1999, 156, 71-83 (Pubitemid 29152984)
50. Taraballi, F.; Natalello, A.; Campione, M.; Villa, O.; Doglia, S. M.; Paleari, A.; Gelain, F. Glycine-Spacers Influence Functional Motifs Exposure and Self-Assembling Propensity of Functionalized Substrates Tailored for Neural Stem Cell Cultures Front Neuroeng. 2010, 3, 1
51. Saha, K.; Keung, A. J.; Irwin, E. F.; Li, Y.; Little, L.; Schaffer, D. V.; Healy, K. E. Substrate Modulus Directs Neural Stem Cell Behavior Biophys. J. 2008, 95, 4426-4438
52. Zuckermann, R. N.; Kodadek, T. Peptoids as Potential Therapeutics Curr. Opin. Mol. Therapy 2009, 11, 299-307
53. Trapp, B. D.; Peterson, J.; Ransohoff, R. M.; Rudick, R.; Mork, S.; Bo, L. Axonal Transection in the Lesions of Multiple Sclerosis N. Engl. J. Med. 1998, 338, 278-285 (Pubitemid 28065253)
54. Pochan, D. J.; Schneider, J. P.; Kretsinger, J.; Ozbas, B.; Rajagopal, K.; Haines, L. Thermally Reversible Hydrogels via Intramolecular Folding and Consequent Self-Assembly of a de Novo Designed Peptide J. Am. Chem. Soc. 2003, 125, 11802-11803 (Pubitemid 37175398)
55. Davis, M. E.; Hsieh, P. C.; Takahashi, T.; Song, Q.; Zhang, S.; Kamm, R. D.; Grodzinsky, A. J.; Anversa, P.; Lee, R. T. Local Myocardial Insulin-like Growth Factor 1 (Igf-1) Delivery with Biotinylated Peptide Nanofibers Improves Cell Therapy for Myocardial Infarction Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 8155-8160 (Pubitemid 43801068)
56. Sedman, V. L.; Adler-Abramovich, L.; Allen, S.; Gazit, E.; Tendler, S. J. Direct Observation of the Release of Phenylalanine from Diphenylalanine Nanotubes J. Am. Chem. Soc. 2006, 128, 6903-6908 (Pubitemid 43830577)
57. Jun, S.; Hong, Y.; Imamura, H.; Ha, B. Y.; Bechhoefer, J.; Chen, P. Self-Assembly of the Ionic Peptide EAK16: The Effect of Charge Distributions on Self-Assembly Biophys. J. 2004, 87, 1249-1259 (Pubitemid 39095101)