Specific immobilization of biotinylated fusion proteins NGF and Sema3A utilizing a photo-cross-linkable diazirine compound for controlling neurite extension

Bioconjugate Chemistry

Volumn 24, Issue 9, 2013, Pages 1515-1526

  McCormick, Aleesha M ^a   Wijekoon, Asanka ^a   Leipzig, Nic D ^a  

^a The University of Akron   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS; CHITOSAN; FOURIER TRANSFORM INFRARED SPECTROSCOPY; NEURONS; RECOMBINANT PROTEINS;

CHITOSAN FILM; CROSS-LINKABLE; CROSSLINKER; DIAZIRINES; DORSAL ROOT GANGLIONS; FUSION PROTEINS; NERVE GROWTH FACTOR; NEURITE EXTENSION; SPECIFIC IMMOBILIZATION; SULFHYDRYL;

IONS;

AMINE; AZIRINE DERIVATIVE; BIOTIN; CHITOSAN; HYBRID PROTEIN; IMMOBILIZED PROTEIN; MALEIMIDE; N MCEP DIAZIRINE; NERVE GROWTH FACTOR; SEMAPHORIN 3A; STREPTAVIDIN; THIOL DERIVATIVE; UNCLASSIFIED DRUG;

ADSORPTION; ANIMAL CELL; ARTICLE; BIOTINYLATION; CARBON NUCLEAR MAGNETIC RESONANCE; CELL REGENERATION; COMPLEX FORMATION; CONTROLLED STUDY; CROSS LINKING; FLUORESCENCE; IN VITRO STUDY; INFRARED SPECTROSCOPY; LIMIT OF QUANTITATION; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NERVOUS SYSTEM; NONHUMAN; PHOTOCHEMISTRY; PHOTOREACTIVITY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN IMMOBILIZATION; PROTON NUCLEAR MAGNETIC RESONANCE; PURIFICATION; SPINAL GANGLION; ULTRAVIOLET RADIATION;

ANIMALS; AZIRINES; BIOTINYLATION; CELLS, CULTURED; CHICKENS; CHITOSAN; CROSS-LINKING REAGENTS; GANGLIA, SPINAL; IMMOBILIZED PROTEINS; MICE; NERVE GROWTH FACTOR; NEURITES; RECOMBINANT FUSION PROTEINS; SEMAPHORIN-3A;

EID: 84884368863     PISSN: 10431802     EISSN: 15204812     Source Type: Journal    
DOI: 10.1021/bc400058n     Document Type: Article

References (70)

1. Buchthal, F. and Kuhl, V. (1979) Nerve conduction, tactile sensibility, and the electromyogram after suture or compression of peripheral nerve: a longitudinal study in man J. Neurol. Neurosurg. Psychiatry 42, 436-451 (Pubitemid 9158949)
2. Raivich, G. and Makwana, M. (2007) The making of successful axonal regeneration: genes, molecules and signal transduction pathways Brain Res. Rev. 53, 287-311 (Pubitemid 46177235)
3. Tohda, C. and Kuboyama, T. (2011) Current and future therapeutic strategies for functional repair of spinal cord injury Pharmacol. Ther. 132, 57-71
4. McCormick, A. M. and Leipzig, N. D. (2012) Neural regenerative strategies incorporating biomolecular axon guidance signals Annals Biomedical Engineering 40, 578-597
5. Levi-Montalcini, R. (1987) The nerve growth factor: thirty-five years later Biosci. Rep. 7, 681-699 (Pubitemid 18027449)
6. Heumann, R., Korsching, S., Bandtlow, C., and Thoenen, H. (1987) Changes of nerve growth factor synthesis in nonneuronal cells in response to sciatic nerve transection J. Cell Biol. 104, 1623-1631 (Pubitemid 17104532)
7. Whittemore, S. R., Ebendal, T., Larkfors, L., Olson, L., Seiger, A., Stromberg, I., and Persson, H. (1986) Development and regional expression of beta nerve growth factor messenger RNA and protein in the rat central nervous system Proc. Natl. Acad. Sci. U. S. A. 83, 817-821 (Pubitemid 16035566)
8. Luo, Y., Raible, D., and Raper, J. A. (1993) Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones Cell 75, 217-227 (Pubitemid 23320286)
9. Giger, R. J., Wolfer, D. P., De Wit, G. M., and Verhaagen, J. (1996) Anatomy of rat semaphorin III/collapsin-1 mRNA expression and relationship to developing nerve tracts during neuroembryogenesis J. Comp. Neurol. 375, 378-392 (Pubitemid 26374779)
10. Tang, X. Q., Heron, P., Mashburn, C., and Smith, G. M. (2007) Targeting sensory axon regeneration in adult spinal cord J. Neurosci. 27, 6068-6078 (Pubitemid 46849754)
11. Bagri, A., Cheng, H. J., Yaron, A., Pleasure, S. J., and Tessier-Lavigne, M. (2003) Stereotyped pruning of long hippocampal axon branches triggered by retraction inducers of the semaphorin family Cell 113, 285-299 (Pubitemid 36556112)
12. Wang, J., Onoshima, D., Aki, M., Okamoto, Y., Kaji, N., Tokeshi, M., and Baba, Y. (2011) Label-free detection of DNA-binding proteins based on microfluidic solid-state molecular beacon sensor Anal. Chem. 83, 3528-3532
13. Sorribas, H., Padeste, C., and Tiefenauer, L. (2002) Photolithographic generation of protein micropatterns for neuron culture applications Biomaterials 23, 893-900 (Pubitemid 33108965)
14. Shi, P., Nedelec, S., Wichterle, H., and Kam, L. C. (2010) Combined microfluidics/protein patterning platform for pharmacological interrogation of axon pathfinding Lab Chip 10, 1005-1010
15. Ganesan, R., Kratz, K., and Lendlein, A. (2010) Multicomponent protein patterning of material surfaces J. Mater. Chem. 20, 7322-7331
16. Jonkheijm, P., Weinrich, D., Kohn, M., Engelkamp, H., Christianen, P. C., Kuhlmann, J., Maan, J. C., Nusse, D., Schroeder, H., Wacker, R., Breinbauer, R., Niemeyer, C. M., and Waldmann, H. (2008) Photochemical surface patterning by the thiol-ene reaction Angew. Chem., Int. Ed. Engl. 47, 4421-4424
17. Vaisocherova, H., Zhang, Z., Yang, W., Cao, Z., Cheng, G., Taylor, A. D., Piliarik, M., Homola, J., and Jiang, S. (2009) Functionalizable surface platform with reduced nonspecific protein adsorption from full blood plasma - material selection and protein immobilization optimization Biosens. Bioelectron. 24, 1924-1930
18. Aizawa, Y., Leipzig, N., Zahir, T., and Shoichet, M. (2008) The effect of immobilized platelet derived growth factor AA on neural stem/progenitor cell differentiation on cell-adhesive hydrogels Biomaterials 29, 4676-4683
19. Leipzig, N. D., Wylie, R. G., Kim, H., and Shoichet, M. S. (2011) Differentiation of neural stem cells in three-dimensional growth factor-immobilized chitosan hydrogel scaffolds Biomaterials 32, 57-64
20. Yu, L. M., Miller, F. D., and Shoichet, M. S. (2010) The use of immobilized neurotrophins to support neuron survival and guide nerve fiber growth in compartmentalized chambers Biomaterials 31, 6987-6999
21. Adams, D. N., Kao, E. Y., Hypolite, C. L., Distefano, M. D., Hu, W. S., and Letourneau, P. C. (2005) Growth cones turn and migrate up an immobilized gradient of the laminin IKVAV peptide J. Neurobiol. 62, 134-147 (Pubitemid 39636384)
22. Van der Meijden, B. and Robinson, J. A. (2011) Synthesis and application of photoproline-a photoactivatable derivative of proline ARKIVOC vi, 130-136
23. Yu, L. M., Wosnick, J. H., and Shoichet, M. S. (2008) Miniaturized system of neurotrophin patterning for guided regeneration J. Neurosci. Methods 171, 253-263
24. Ben-Zvi, A., Yagil, Z., Hagalili, Y., Klein, H., Lerman, O., and Behar, O. (2006) Semaphorin 3A and neurotrophins: a balance between apoptosis and survival signaling in embryonic DRG neurons J. Neurochem. 96, 585-597
25. Gomes, A. F. and Gozzo, F. C. (2010) Chemical cross-linking with a diazirine photoactivatable cross-linker investigated by MALDI- and ESI-MS/MS J. Mass Spectrom. 45, 892-899
26. Dubinsky, L., Krom, B. P., and Meijler, M. M. (2012) Diazirine based photoaffinity labeling Bioorg. Med. Chem. 20, 554-570
27. Blencowe, A. and Hayes, W. (2005) Development and application of diazirines in biological and synthetic macromolecular systems Soft Matter 1, 178-205 (Pubitemid 41411307)
28. Weber, T. and Brunner, J. (1995) 2-(Tributylstannyl)-4-[3- (trifluoromethyl)-3H-diazirin-3-yl]benzyl alcohol: a building block for photolabeling and cross-linking reagent of very high specific radioactivity J. Am. Chem. Soc. 117, 3084-3095
29. Chee, G. L., Yalowich, J. C., Bodner, A., Wu, X., and Hasinoff, B. B. (2010) A diazirine-based photoaffinity etoposide probe for labeling topoisomerase II Bioorg. Med. Chem. 18, 830-838
30. Brunner, J., Senn, H., and Richards, F. M. (1980) 3-Trifluoromethyl-3- phenyldiazirine. A new carbene generating group for photolabeling reagents J. Biol. Chem. 255, 3313-3318
31. Chevolot, Y., Martins, J., Milosevic, N., Leonard, D., Zeng, S., Malissard, M., Berger, E. G., Maier, P., Mathieu, H. J., Crout, D. H., and Sigrist, H. (2001) Immobilisation on polystyrene of diazirine derivatives of mono- and disaccharides: biological activities of modified surfaces Bioorg. Med. Chem. 9, 2943-2953
32. Luo, Y. and Shoichet, M. S. (2004) A photolabile hydrogel for guided three-dimensional cell growth and migration Nat. Mater. 3, 249-253
33. Lee, S. H., Moon, J. J., and West, J. L. (2008) Three-dimensional micropatterning of bioactive hydrogels via two-photon laser scanning photolithography for guided 3D cell migration Biomaterials 29, 2962-2968
34. Wylie, R. G., Ahsan, S., Aizawa, Y., Maxwell, K. L., Morshead, C. M., and Shoichet, M. S. (2011) Spatially controlled simultaneous patterning of multiple growth factors in three-dimensional hydrogels Nat. Mater. 10, 799-806
35. Rusmini, F., Zhong, Z., and Feijen, J. (2007) Protein immobilization strategies for protein biochips Biomacromolecules 8, 1775-1789 (Pubitemid 47009952)
36. Weiden, P. L., Breitz, H. B., Press, O., Appelbaum, J. W., Bryan, J. K., Gaffigan, S., Stone, D., Axworthy, D., Fisher, D., and Reno, J. (2000) Pretargeted radioimmunotherapy (PRIT) for treatment of non-Hodgkin's lymphoma (NHL): initial phase I/II study results Cancer Biother. Radiopharm. 15, 15-29 (Pubitemid 30108614)
37. Knox, S. J., Goris, M. L., Tempero, M., Weiden, P. L., Gentner, L., Breitz, H., Adams, G. P., Axworthy, D., Gaffigan, S., Bryan, K., Fisher, D. R., Colcher, D., Horak, I. D., and Weiner, L. M. (2000) Phase II trial of yttrium-90-DOTA-biotin pretargeted by NR-LU-10 antibody/streptavidin in patients with metastatic colon cancer Clin. Cancer Res. 6, 406-414 (Pubitemid 30111457)
38. Forero, A., Weiden, P. L., Vose, J. M., Knox, S. J., LoBuglio, A. F., Hankins, J., Goris, M. L., Picozzi, V. J., Axworthy, D. B., Breitz, H. B., Sims, R. B., Ghalie, R. G., Shen, S., and Meredith, R. F. (2004) Phase 1 trial of a novel anti-CD20 fusion protein in pretargeted radioimmunotherapy for B-cell non-Hodgkin lymphoma Blood 104, 227-236 (Pubitemid 38879862)
39. Chinol, M., Casalini, P., Maggiolo, M., Canevari, S., Omodeo, E. S., Caliceti, P., Veronese, F. M., Cremonesi, M., Chiolerio, F., Nardone, E., Siccardi, A. G., and Paganelli, G. (1998) Biochemical modifications of avidin improve pharmacokinetics and biodistribution, and reduce immunogenicity Br. J. Cancer 78, 189-197 (Pubitemid 28302255)
40. Marshall, D., Pedley, R. B., Boden, J. A., Boden, R., Melton, R. G., and Begent, R. H. (1996) Polyethylene glycol modification of a galactosylated streptavidin clearing agent: effects on immunogenicity and clearance of a biotinylated anti-tumour antibody Br. J. Cancer 73, 565-572 (Pubitemid 26068858)
41. Meyer, D. L., Schultz, J., Lin, Y., Henry, A., Sanderson, J., Jackson, J. M., Goshorn, S., Rees, A. R., and Graves, S. S. (2001) Reduced antibody response to streptavidin through site-directed mutagenesis Protein Sci. 10, 491-503 (Pubitemid 32221140)
42. Wylie, R. G. and Shoichet, M. S. (2011) Three-dimensional spatial patterning of proteins in hydrogels Biomacromolecules 12, 3789-3796
43. Khatwani, S. L., Kang, J. S., Mullen, D. G., Hast, M. A., Beese, L. S., Distefano, M. D., and Taton, T. A. (2012) Covalent protein-oligonucleotide conjugates by copper-free click reaction Bioorg. Med. Chem. 20, 4532-4539
44. Soundrarajan, N., Sokalingam, S., Raghunathan, G., Budisa, N., Paik, H. J., Yoo, T. H., and Lee, S. G. (2012) Conjugation of proteins by installing BIO-orthogonally reactive groups at their N-termini PLoS One 7, e46741
45. Begum, A. A., Radhakrishnan, R., and Nazeer, K. P. (2011) Study of structure-property relationship on sulfuric acid crosslinked chitosan membranes Malaysian Polymer Journal 6, 27-38
46. Kumirska, J., Czerwicka, M., Kaczynski, Z., Bychowska, A., Brzozowski, K., Thoming, J., and Stepnowski, P. (2010) Application of spectroscopic methods for structural analysis of chitin and chitosan Mar. Drugs 8, 1567-1636
47. Zhang, Z. and Cui, H. (2012) Biodegradability and biocompatibility study of poly(chitosan-g-lactic acid) scaffolds Molecules 17, 3243-3258
48. Liao, S., Lin, M., and Hung, C. (2004) A kinetic study of thermal degradations of chitosan/polycaprolactam blends Macromol. Res. 12, 466-473 (Pubitemid 39524067)
49. Welzel, P. B. (2002) Investigation of adsorption-induced structural changes of proteins at solid/liquid interfaces by differential scanning calorimetry Thermochim. Acta 382, 175-188
50. Heron, P. M., Sutton, B. M., Curinga, G. M., Smith, G. M., and Snow, D. M. (2007) Localized gene expression of axon guidance molecules in neuronal co-cultures J. Neurosci. Methods 159, 203-214 (Pubitemid 44908649)
51. Bernfield, M., Kokenyesi, R., Kato, M., Hinkes, M. T., Spring, J., Gallo, R. L., and Lose, E. J. (1992) Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans Annu. Rev. Cell Biol. 8, 365-393 (Pubitemid 23001002)
52. Rutishauser, U., Acheson, A., Hall, A. K., Mann, D. M., and Sunshine, J. (1988) The neural cell adhesion molecule (NCAM) as a regulator of cell-cell interactions Science 240, 53-57
53. Nimni, M. E. (1997) Polypeptide growth factors: targeted delivery systems Biomaterials 18, 1201-1225 (Pubitemid 27390300)
54. Uebersax, L., Merkle, H. P., and Meinel, L. (2009) Biopolymer-based growth factor delivery for tissue repair: from natural concepts to engineered systems Tiss. Eng. Part B Rev. 15, 263-289
55. Steffensky, M., Steinbach, K., Schwarz, U., and Schlosshauer, B. (2006) Differential impact of semaphorin 3E and 3A on CNS axons Int. J. Dev. Neurosci. 24, 65-72 (Pubitemid 43287949)
56. Dontchev, V. D. and Letourneau, P. C. (2002) Nerve growth factor and semaphorin 3A signaling pathways interact in regulating sensory neuronal growth cone motility J. Neurosci. 22, 6659-6669 (Pubitemid 35386422)
57. Masters, K. S. (2011) Covalent growth factor immobilization strategies for tissue repair and regeneration Macromol. Biosci. 11, 1149-1163
58. Ito, Y. (2008) Covalently immobilized biosignal molecule materials for tissue engineering Soft Matter 4, 46-56
59. Zhong, X. and Rescorla, F. J. (2012) Cell surface adhesion molecules and adhesion-initiated signaling: understanding of anoikis resistance mechanisms and therapeutic opportunities Cell. Signalling 24, 393-401
60. Markus, A., Patel, T. D., and Snider, W. D. (2002) Neurotrophic factors and axonal growth Curr. Opin. Neurobiol. 12, 523-531 (Pubitemid 35284087)
61. Madduri, S., Papaloizos, M., and Gander, B. (2009) Synergistic effect of GDNF and NGF on axonal branching and elongation in vitro Neurosci. Res. 65, 88-97
62. Klimaschewski, L., Nindl, W., Feurle, J., Kavakebi, P., and Kostron, H. (2004) Basic fibroblast growth factor isoforms promote axonal elongation and branching of adult sensory neurons in vitro Neuroscience 126, 347-353 (Pubitemid 38780810)
63. Gallo, G. and Letourneau, P. C. (1998) Localized sources of neurotrophins initiate axon collateral sprouting J. Neurosci. 18, 5403-5414 (Pubitemid 28311956)
64. Atwal, J. K., Massie, B., Miller, F. D., and Kaplan, D. R. (2000) The TrkB-Shc site signals neuronal survival and local axon growth via MEK and P13-kinase Neuron 27, 265-277
65. Aoki, K., Nakamura, T., and Matsuda, M. (2004) Spatio-temporal regulation of Rac1 and Cdc42 activity during nerve growth factor-induced neurite outgrowth in PC12 cells J. Biol. Chem. 279, 713-719 (Pubitemid 38044876)
66. MacInnis, B. L. and Campenot, R. B. (2002) Retrograde support of neuronal survival without retrograde transport of nerve growth factor Science 295, 1536-1539 (Pubitemid 34174011)
67. MacInnis, B. L., Senger, D. L., and Campenot, R. B. (2003) Spatial requirements for TrkA kinase activity in the support of neuronal survival and axon growth in rat sympathetic neurons Neuropharmacology 45, 995-1010 (Pubitemid 37297925)
68. Liu, B. P. and Strittmatter, S. M. (2001) Semaphorin-mediated axonal guidance via Rho-related G proteins Curr. Opin. Cell Biol. 13, 619-626 (Pubitemid 32817022)
69. Castellani, V. and Rougon, G. (2002) Control of semaphorin signaling Curr. Opin. Neurobiol. 12, 532-541 (Pubitemid 35284088)
70. Brown, J. A. and Bridgman, P. C. (2009) Disruption of the cytoskeleton during Semaphorin 3A induced growth cone collapse correlates with differences in actin organization and associated binding proteins Dev. Neurobiol. 69, 633-646