Beta hairpin peptide hydrogels as an injectable solid vehicle for neurotrophic growth factor delivery

Biomacromolecules

Volumn 16, Issue 9, 2015, Pages 2672-2683

  Lindsey, Stephan ^a   Piatt, Joseph H ^a   Worthington, Peter ^a,b   Sönmez, Cem ^c   Satheye, Sameer ^b   Schneider, Joel P ^c   Pochan, Darrin J ^b   Langhans, Sigrid A ^a  

^a NEMOURS ALFRED I DUPONT HOSPITAL FOR CHILDREN   (United States)

^b UNIVERSITY OF DELAWARE   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHIBIOUS VEHICLES; BIODEGRADATION; CELL SIGNALING; ENZYME INHIBITION; NON NEWTONIAN FLOW; PEPTIDES; SHEAR FLOW; SHEAR THINNING;

BRAIN-DERIVED NEUROTROPHIC FACTORS; FUNCTIONAL CAPABILITIES; GROWTH FACTOR DELIVERY; GROWTH FACTOR RELEASE; NERVE GROWTH FACTOR; SIGNALING PATHWAYS; SPINAL CORD INJURIES (SCI); SUSTAINED RELEASE;

HYDROGELS;

BRAIN DERIVED NEUROTROPHIC FACTOR; DRUG VEHICLE; MAX8 PEPTIDE; NEUROTROPHIC FACTOR; PEPTIDE; UNCLASSIFIED DRUG; DRUG CARRIER; HYDROGEL; NERVE GROWTH FACTOR;

ANIMAL CELL; ARTICLE; BIOLOGICAL ACTIVITY; CELL CULTURE; CONTINUOUS CULTURE; CONTROLLED STUDY; CROSS LINKING; DRUG DELIVERY SYSTEM; EMBRYO; ENCAPSULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; HYDROGEL; MOUSE; NERVE CELL PLASTICITY; NEURITE; NONHUMAN; PC12 CELL LINE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; SUSTAINED DRUG RELEASE; WESTERN BLOTTING; ANIMAL; CHEMISTRY; HUMAN; PHARMACOLOGY; RAT;

ANIMALS; DRUG CARRIERS; HUMANS; HYDROGELS; NERVE GROWTH FACTOR; PC12 CELLS; PEPTIDES; RATS;

EID: 84941670929     PISSN: 15257797     EISSN: 15264602     Source Type: Journal    
DOI: 10.1021/acs.biomac.5b00541     Document Type: Article

References (53)

1. Awad, B. I.; Carmody, M. A.; Steinmetz, M. P. Potential Role of Growth Factors in the Management of Spinal Cord Injury. World Neurosurg 2015, 83, 120 10.1016/j.wneu.2013.01.042
2. Macaya, D.; Spector, M. Injectable hydrogel materials for spinal cord regeneration: a review Biomed. Mater. 2012, 7 (1) 012001 10.1088/1748-6041/7/1/012001
3. Branco, M. C.; Schneider, J. P. Self-assembling materials for therapeutic delivery Acta Biomater. 2009, 5 (3) 817-31 10.1016/j.actbio.2008.09.018
4. Kobsa, S.; Saltzman, W. M. Bioengineering approaches to controlled protein delivery Pediatr. Res. 2008, 63 (5) 513-9 10.1203/PDR.0b013e318165f14d
5. Lin, C. C.; Metters, A. T. Hydrogels in controlled release formulations: network design and mathematical modeling Adv. Drug Delivery Rev. 2006, 58 (12-13) 1379-408 10.1016/j.addr.2006.09.004
6. Sonmez, C.; Nagy, K. J.; Schneider, J. P. Design of self-assembling peptide hydrogelators amenable to bacterial expression Biomaterials 2015, 37, 62-72 10.1016/j.biomaterials.2014.10.011
7. Segers, V. F.; Lee, R. T. Local delivery of proteins and the use of self-assembling peptides Drug Discovery Today 2007, 12 (13-14) 561-8 10.1016/j.drudis.2007.05.003
8. 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 (50) 15030-7 10.1021/ja027993g
9. 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 (39) 11802-3 10.1021/ja0353154
10. Micklitsch, C. M.; Medina, S. H.; Yucel, T.; Nagy-Smith, K. J.; Pochan, D. J.; Schneider, J. P. Influence of Hydrophobic Face Amino Acids on the Hydrogelation of β-Hairpin Peptide Amphiphiles Macromolecules 2015, 48 (5) 1281-1288 10.1021/ma5024796
11. Rajagopal, K.; Ozbas, B.; Pochan, D. J.; Schneider, J. P. Probing the importance of lateral hydrophobic association in self-assembling peptide hydrogelators Eur. Biophys. J. 2006, 35 (2) 162-9 10.1007/s00249-005-0017-7
12. Rajagopal, K.; Lamm, M. S.; Haines-Butterick, L. A.; Pochan, D. J.; Schneider, J. P. Tuning the pH responsiveness of beta-hairpin peptide folding, self-assembly, and hydrogel material formation Biomacromolecules 2009, 10 (9) 2619-25 10.1021/bm900544e
13. Ozbas, B.; Rajagopal, K.; Schneider, J. P.; Pochan, D. J. Semiflexible chain networks formed via self-assembly of beta-hairpin molecules Phys. Rev. Lett. 2004, 93, 268106 10.1103/PhysRevLett.93.268106
14. Galler, K. M.; Aulisa, L.; Regan, K. R.; D'Souza, R. N.; Hartgerink, J. D. Self-assembling multidomain peptide hydrogels: designed susceptibility to enzymatic cleavage allows enhanced cell migration and spreading J. Am. Chem. Soc. 2010, 132 (9) 3217-23 10.1021/ja910481t
15. Aimetti, A. A.; Tibbitt, M. W.; Anseth, K. S. Human neutrophil elastase responsive delivery from poly(ethylene glycol) hydrogels Biomacromolecules 2009, 10 (6) 1484-9 10.1021/bm9000926
16. Yang, J.; Jacobsen, M. T.; Pan, H.; Kopecek, J. Synthesis and characterization of enzymatically degradable PEG-based peptide-containing hydrogels Macromol. Biosci. 2010, 10 (4) 445-54 10.1002/mabi.200900295
17. Giano, M. C.; Pochan, D. J.; Schneider, J. P. Controlled biodegradation of self-assembling beta-hairpin peptide hydrogels by proteolysis with matrix metalloproteinase-13 Biomaterials 2011, 32 (27) 6471-7 10.1016/j.biomaterials.2011.05.052
18. Li, Y.; Rodrigues, J.; Tomas, H. Injectable and biodegradable hydrogels: gelation, biodegradation and biomedical applications Chem. Soc. Rev. 2012, 41 (6) 2193-221 10.1039/C1CS15203C
19. Tavano, L.; Vivacqua, M.; Carito, V.; Muzzalupo, R.; Caroleo, M. C.; Nicoletta, F. Doxorubicin loaded magneto-niosomes for targeted drug delivery Colloids Surf., B 2013, 102, 803-7 10.1016/j.colsurfb.2012.09.019
20. Collier, J. H.; Segura, T. Evolving the use of peptides as components of biomaterials Biomaterials 2011, 32 (18) 4198-204 10.1016/j.biomaterials.2011.02.030
21. Li, L.; Teller, S.; Clifton, R. J.; Jia, X.; Kiick, K. L. Tunable mechanical stability and deformation response of a resilin-based elastomer Biomacromolecules 2011, 12 (6) 2302-10 10.1021/bm200373p
22. Agrawal, C. M.; Ray, R. B. Biodegradable polymeric scaffolds for musculoskeletal tissue engineering J. Biomed. Mater. Res. 2001, 55 (2) 141-50 10.1002/1097-4636(200105)55:2<141::AID-JBM1000>3.0.CO;2-J
23. Hatefi, A.; Amsden, B. Biodegradable injectable in situ forming drug delivery systems J. Controlled Release 2002, 80 (1-3) 9-28 10.1016/S0168-3659(02)00008-1
24. Farokhzad, O. C.; Langer, R. Impact of nanotechnology on drug delivery ACS Nano 2009, 3 (1) 16-20 10.1021/nn900002m
25. Haines-Butterick, L.; Rajagopal, K.; Branco, M.; Salick, D.; Rughani, R.; Pilarz, M.; Lamm, M. S.; Pochan, D. J.; Schneider, J. P. Controlling hydrogelation kinetics by peptide design for three-dimensional encapsulation and injectable delivery of cells Proc. Natl. Acad. Sci. U. S. A. 2007, 104 (19) 7791-6 10.1073/pnas.0701980104
26. Pakstis, L. M.; Ozbas, B.; Hales, K. D.; Nowak, A. P.; Deming, T. J.; Pochan, D. Effect of chemistry and morphology on the biofunctionality of self-assembling diblock copolypeptide hydrogels Biomacromolecules 2004, 5 (2) 312-8 10.1021/bm034249v
27. Yan, C.; Altunbas, A.; Yucel, T.; Nagarkar, R. P.; Schneider, J. P.; Pochan, D. J. Injectable solid hydrogel: mechanism of shear-thinning and immediate recovery of injectable beta-hairpin peptide hydrogels Soft Matter 2010, 6 (20) 5143-5156 10.1039/c0sm00642d
28. Sathaye, S.; Mbi, A.; Sonmez, C.; Chen, Y.; Blair, D. L.; Schneider, J. P.; Pochan, D. J. Rheology of peptide- and protein-based physical hydrogels: Are everyday measurements just scratching the surface? Wiley Interdiscip Rev. Nanomed Nanobiotechnol 2015, 7 (1) 34-68 10.1002/wnan.1299
29. Altunbas, A.; Lee, S. J.; Rajasekaran, S. A.; Schneider, J. P.; Pochan, D. J. Encapsulation of curcumin in self-assembling peptide hydrogels as injectable drug delivery vehicles Biomaterials 2011, 32 (25) 5906-14 10.1016/j.biomaterials.2011.04.069
30. Drubin, D. G.; Feinstein, S. C.; Shooter, E. M.; Kirschner, M. W. Nerve growth factor-induced neurite outgrowth in PC12 cells involves the coordinate induction of microtubule assembly and assembly-promoting factors J. Cell Biol. 1985, 101 (5) 1799-807 10.1083/jcb.101.5.1799
31. Lindsey, S.; Jiang, J.; Woulfe, D.; Papoutsakis, E. T. Platelets from mice lacking the aryl hydrocarbon receptor exhibit defective collagen-dependent signaling J. Thromb. Haemostasis 2014, 12 (3) 383-94 10.1111/jth.12490
32. Lindsey, S.; Papoutsakis, E. T. The aryl hydrocarbon receptor (AHR) transcription factor regulates megakaryocytic polyploidization Br. J. Haematol. 2011, 152 (4) 469-84 10.1111/j.1365-2141.2010.08548.x
33. Lindsey, S.; Huang, W.; Wang, H.; Horvath, E.; Zhu, C.; Eklund, E. A. Activation of SHP2 protein-tyrosine phosphatase increases HoxA10-induced repression of the genes encoding gp91(PHOX) and p67(PHOX) J. Biol. Chem. 2007, 282 (4) 2237-49 10.1074/jbc.M608642200
34. Lee, S. J.; Lindsey, S.; Graves, B.; Yoo, S.; Olson, J. M.; Langhans, S. A. Sonic hedgehog-induced histone deacetylase activation is required for cerebellar granule precursor hyperplasia in medulloblastoma PLoS One 2013, 8 (8) e71455 10.1371/journal.pone.0071455
35. Branco, M. C.; Pochan, D. J.; Wagner, N. J.; Schneider, J. P. Macromolecular diffusion and release from self-assembled beta-hairpin peptide hydrogels Biomaterials 2009, 30 (7) 1339-47 10.1016/j.biomaterials.2008.11.019
36. Branco, M. C.; Pochan, D. J.; Wagner, N. J.; Schneider, J. P. The effect of protein structure on their controlled release from an injectable peptide hydrogel Biomaterials 2010, 31 (36) 9527-34 10.1016/j.biomaterials.2010.08.047
37. Altunbas, A.; Pochan, D. J. Peptide-based and polypeptide-based hydrogels for drug delivery and tissue engineering Top Curr. Chem. 2012, 310, 135-67 10.1007/128
38. Boyce, V. S.; Mendell, L. M. Neurotrophins and spinal circuit function Front. Neural Circuits 2014, 8, 59 10.3389/fncir.2014.00059
39. Tsang, S. W.; Zhao, M.; Wu, J.; Sung, J. J.; Bian, Z. X. Nerve growth factor-mediated neuronal plasticity in spinal cord contributes to neonatal maternal separation-induced visceral hypersensitivity in rats Eur. J. Pain 2012, 16 (4) 463-72 10.1016/j.ejpain.2011.07.005
40. Cao, X.; Tang, C.; Luo, Y. Effect of nerve growth factor on neuronal apoptosis after spinal cord injury in rats Chin. J. Traumatol. 2002, 5 (3) 131-5
41. Vavrek, R.; Girgis, J.; Tetzlaff, W.; Hiebert, G. W.; Fouad, K. BDNF promotes connections of corticospinal neurons onto spared descending interneurons in spinal cord injured rats Brain 2006, 129 (6) 1534-45 10.1093/brain/awl087
42. Yucel, T.; Micklitsch, C. M.; Schneider, J. P.; Pochan, D. J. Direct Observation of Early-Time Hydrogelation in beta-Hairpin Peptide Self-Assembly Macromolecules 2008, 41 (15) 5763-5772 10.1021/ma702840q
43. Greene, L. A.; Tischler, A. S. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor Proc. Natl. Acad. Sci. U. S. A. 1976, 73 (7) 2424-8 10.1073/pnas.73.7.2424
44. Vaudry, D.; Stork, P. J.; Lazarovici, P.; Eiden, L. E. Signaling pathways for PC12 cell differentiation: making the right connections Science 2002, 296 (5573) 1648-9 10.1126/science.1071552
45. Leoni, C.; Menegon, A.; Benfenati, F.; Toniolo, D.; Pennuto, M.; Valtorta, F. Neurite extension occurs in the absence of regulated exocytosis in PC12 subclones Mol. Biol. Cell 1999, 10 (9) 2919-31 10.1091/mbc.10.9.2919
46. Connolly, J. L.; Greene, L. A.; Viscarello, R. R.; Riley, W. D. Rapid, sequential changes in surface morphology of PC12 pheochromocytoma cells in response to nerve growth factor J. Cell Biol. 1979, 82 (3) 820-7 10.1083/jcb.82.3.820
47. Jiang, J.; Papoutsakis, E. T. Stem-cell niche based comparative analysis of chemical and nano-mechanical material properties impacting ex vivo expansion and differentiation of hematopoietic and mesenchymal stem cells Adv. Healthcare Mater. 2013, 2 (1) 25-42 10.1002/adhm.201200169
48. Migliorini, E.; Ban, J.; Grenci, G.; Andolfi, L.; Pozzato, A.; Tormen, M.; Torre, V.; Lazzarino, M. Nanomechanics controls neuronal precursors adhesion and differentiation Biotechnol. Bioeng. 2013, 110 (8) 2301-10 10.1002/bit.24880
49. Oger, J.; Arnason, B. G.; Pantazis, N.; Lehrich, J.; Young, M. Synthesis of nerve growth factor by L and 3T3 cells in culture Proc. Natl. Acad. Sci. U. S. A. 1974, 71 (4) 1554-8 10.1073/pnas.71.4.1554
50. Gelain, F.; Unsworth, L. D.; Zhang, S. Slow and sustained release of active cytokines from self-assembling peptide scaffolds J. Controlled Release 2010, 145 (3) 231-9 10.1016/j.jconrel.2010.04.026
51. Annabi, N.; Tamayol, A.; Uquillas, J. A.; Akbari, M.; Bertassoni, L. E.; Cha, C.; Camci-Unal, G.; Dokmeci, M. R.; Peppas, N. A.; Khademhosseini, A. 25th anniversary article: Rational design and applications of hydrogels in regenerative medicine Adv. Mater. 2014, 26 (1) 85-123 10.1002/adma.201303233
52. Lee, M.; Chen, T. T.; Iruela-Arispe, M. L.; Wu, B. M.; Dunn, J. C. Modulation of protein delivery from modular polymer scaffolds Biomaterials 2007, 28 (10) 1862-70 10.1016/j.biomaterials.2006.12.006
53. Koutsopoulos, S.; Unsworth, L. D.; Nagai, Y.; Zhang, S. Controlled release of functional proteins through designer self-assembling peptide nanofiber hydrogel scaffold Proc. Natl. Acad. Sci. U. S. A. 2009, 106 (12) 4623-8 10.1073/pnas.0807506106