Enzymatic engineering of polysialic acid on cells in vitro and in vivo using a purified bacterial polysialyltransferase

Journal of Biological Chemistry

Volumn 287, Issue 39, 2012, Pages 32770-32779

  El Maarouf, Abderrahman ^a   Yaw, Damali Moyo Lee ^a   Lindhout, Theresa ^b   Pearse, Damien D ^c   Wakarchuk, Warren ^b,d   Rutishauser, Urs ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b UNIVERSITY OF GUELPH   (Canada)

^c UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^d NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT BRAIN; CELL MIGRATION; CELL SURFACE PROTEINS; CELL TYPES; CELLULAR PROCESS; CEREBRAL CORTEX; CHINESE HAMSTER OVARY CELLS; DONOR SUBSTRATES; EXTRACELLULAR ENVIRONMENTS; IN-VITRO; IN-VIVO; MOUSE EMBRYONIC STEM CELLS; NEISSERIA MENINGITIDIS; NEURAL CELL ADHESION MOLECULES; NEURITE OUTGROWTH; POLYSIALIC ACID; POLYSIALYLATION; RAT SCHWANN CELL; SPINAL CORDS; STRIATUM; STX GENES;

ANIMALS; BRAIN; CELL ADHESION; CELL CULTURE; CELL MEMBRANES; GENE EXPRESSION; NEURONS; PURIFICATION; TISSUE;

CELL ENGINEERING;

POLYSIALIC ACID; POLYSIALYLTRANSFERASE; SIALYLTRANSFERASE; UNCLASSIFIED DRUG;

ADULT ANIMAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL ADHESION; CELL MIGRATION; CHICKEN; CHO CELL; CONTROLLED STUDY; CORPUS STRIATUM; DRUG ACTIVITY; EMBRYONIC STEM CELL; ENZYME ENGINEERING; FIBROBLAST; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NEISSERIA MENINGITIDIS; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; RAT; SCHWANN CELL; SPINAL CORD;

ANIMALS; BACTERIAL PROTEINS; CHICKENS; CHO CELLS; CRICETINAE; CRICETULUS; METABOLIC ENGINEERING; MICE; NEISSERIA MENINGITIDIS; RATS; RATS, INBRED F344; SIALIC ACIDS; SIALYLTRANSFERASES;

BACTERIA (MICROORGANISMS); CRICETULUS GRISEUS; NEISSERIA MENINGITIDIS; RATTUS; VERTEBRATA;

EID: 84866534476     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.377614     Document Type: Article

References (36)

1. Eckhardt, M., Mühlenhoff, M., Bethe, A., Koopman, J., Frosch, M., and Gerardy-Schahn, R. (1995) Molecular characterization of eukaryotic polysialyltransferase-1. Nature 373, 715-718
2. Johnson, C. P., Fujimoto, I., Rutishauser, U., and Leckband, D. E. (2005) Direct evidence that neural cell adhesion molecule (NCAM) polysialylation increases intermembrane repulsion and abrogates adhesion. J. Biol. Chem. 280, 137-145 (Pubitemid 40164974)
3. Fujimoto, I., Bruses, J. L., and Rutishauser, U. (2001) Regulation of cell adhesion by polysialic acid: effects on cadherin, immunoglobulin cell adhesion molecule, and integrin function and independence from neural cell adhesion molecule binding or signaling activity. J. Biol. Chem. 276, 31745-31751
4. Rutishauser, U. (2008) Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat. Rev. Neurosci. 9, 26-35
5. Angata, K., Huckaby, V., Ranscht, B., Terskikh, A., Marth, J. D., and Fukuda, M. (2007) Polysialic acid-directed migration and differentiation of neural precursors are essential for mouse brain development. Mol. Cell. Biol. 27, 6659-6668 (Pubitemid 47483620)
6. Weinhold, B., Seidenfaden, R., Röckle, I., Mühlenhoff, M., Schertzinger, F., Conzelmann, S., Marth, J. D., Gerardy-Schahn, R., and Hildebrandt, H. (2005) Genetic ablation of polysialic acid causes severe neurodevelopmental defects rescued by deletion of the neural cell adhesion molecule. J. Biol. Chem. 280, 42971-42977 (Pubitemid 43049260)
7. Tomasiewicz, H., Ono, K., Yee, D., Thompson, C., Goridis, C., Rutishauser, U., and Magnuson, T. (1993) Genetic deletion of a neural cell adhesion molecule variant (N-CAM-180) produces distinct defects in the central nervous system. Neuron 11, 1163-1174 (Pubitemid 24015289)
8. Cremer, H., Lange, R., Christoph, A., Plomann, M., Vopper, G., Roes, J., Brown, R., Baldwin, S., Kraemer, P., Scheff, S. (1994) Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature 367, 455-459 (Pubitemid 24046046)
9. Daston, M. M., Bastmeyer, M., Rutishauser, U., and O'Leary, D. D. (1996) Spatially restricted increase in polysialic acid enhances corticospinal axon branching related to target recognition and innervation. J. Neurosci. 16, 5488-5497 (Pubitemid 26277877)
10. Tang, J., Landmesser, L., and Rutishauser, U. (1992) Polysialic acid influences specific pathfinding by avian motoneurons. Neuron 8, 1031-1044
11. Tang, J., Rutishauser, U., and Landmesser, L. (1994) Polysialic acid regulates growth cone behavior during sorting of motor axons in the plexus region. Neuron 13, 405-414 (Pubitemid 24275097)
12. Yin, X., Watanabe, M., and Rutishauser, U. (1995) Effect of polysialic acid on the behavior of retinal ganglion cell axons during growth into the optic tract and tectum. Development 121, 3439-3446
13. Seki, T., and Rutishauser, U. (1998) Removal of polysialic acid-neural cell adhesion molecule induces aberrant mossy fiber innervation and ectopic synaptogenesis in the hippocampus. J. Neurosci. 18, 3757-3766 (Pubitemid 28225683)
14. El Maarouf, A., and Rutishauser, U. (2003) Removal of polysialic acid induces aberrant pathways, synaptic vesicle distribution, and terminal arborization of retinotectal axons. J. Comp. Neurol. 460, 203-211 (Pubitemid 36512931)
15. Theodosis, D. T., Rougon, G., and Poulain, D. A. (1991) Retention of embryonic features by an adult neuronal system capable of plasticity: polysialylated neural cell adhesion molecule in the hypothalamoneurohypophysial system. Proc. Natl. Acad. Sci. U.S.A. 88, 5494-5498 (Pubitemid 21914771)
16. El Maarouf, A., and Rutishauser, U. (2005) in Neuroglycobiology (Fukuda, M., Rutishauser, U., and Schnaar, R. L., eds) pp. 39-57, Oxford University Press, London
17. El Maarouf, A., Petridis, A. K., and Rutishauser, U. (2006) Use of polysialic acid in repair of the central nervous system. Proc. Natl. Acad. Sci. U.S.A. 103, 16989-16994 (Pubitemid 44737365)
18. El Maarouf, A., and Rutishauser, U. (2010) Use of PSA-NCAM in repair of the central nervous system. Adv. Exp. Med. Biol. 663, 137-147
19. Zhang, Y., Ghadiri-Sani, M., Zhang, X., Richardson, P. M., Yeh, J., and Bo, X. (2007) Induced expression of polysialic acid in the spinal cord promotes regeneration of sensory axons. Mol. Cell. Neurosci. 35, 109-119 (Pubitemid 46636307)
20. Zhang, Y., Zhang, X., Yeh, J., Richardson, P., and Bo, X. (2007) Engineered expression of polysialic acid enhances Purkinje cell axonal regeneration in L1/GAP-43 double transgenic mice. Eur. J. Neurosci. 25, 351-361
21. Lavdas, A. A., Franceschini, I., Dubois-Dalcq, M., and Matsas, R. (2006) Schwann cells genetically engineered to express PSA show enhanced migratory potential without impairment of their myelinating ability in vitro. Glia 53, 868-878
22. Gravvanis, A. I., Lavdas, A. A., Papalois, A., Tsoutsos, D. A., and Matsas, R. (2007) The beneficial effect of genetically engineered Schwann cells with enhanced motility in peripheral nerve regeneration: review. Acta Neurochir. Suppl. 100, 51-56
23. Papastefanaki, F., Chen, J., Lavdas, A. A., Thomaidou, D., Schachner, M., and Matsas, R. (2007) Grafts of Schwann cells engineered to express PSA-NCAM promote functional recovery after spinal cord injury. Brain 130, 2159-2174 (Pubitemid 47236630)
24. Ghosh, M., Tuesta, L. M., Puentes, R., Patel, S., Melendez, K., El Maarouf, A., Rutishauser, U., and Pearse, D. D. (2012) Extensive cell migration, axon regeneration, and improved function with polysialic acid-modified Schwann cells after spinal cord injury. Glia 60, 979-992
25. Cho, J. W., and Troy, F. A., 2nd (1994) Polysialic acid engineering: synthesis of polysialylated neoglycosphingolipids by using the polysialyltransferase from neuroinvasive Escherichia coli K1. Proc. Natl. Acad. Sci. U.S.A. 91, 11427-11431
26. Willis, L. M., Gilbert, M., Karwaski, M. F., Blanchard, M. C., and Wakarchuk, W. W. (2008) Characterization of the α-2,8- polysialyltransferase from Neisseria meningitidis with synthetic acceptors, and the development of a self-priming polysialyltransferase fusion enzyme. Glycobiology 18, 177-186 (Pubitemid 351168256)
27. Lindhout, T., Iqbal, U., Willis, L. M., Reid, A. N., Li, J., Liu, X., Moreno, M., and Wakarchuk, W. W. (2011) Site-specific enzymatic polysialylation of therapeutic proteins using bacterial enzymes. Proc. Natl. Acad. Sci. U.S.A. 108, 7397-7402
28. Karwaski, M. F., Wakarchuk, W. W., and Gilbert, M. (2002) High-level expression of recombinant Neisseria CMP-sialic acid synthetase in Escherichia coli. Protein Expr. Purif. 25, 237-240 (Pubitemid 35307505)
29. Morley, T. J., and Withers, S. G. (2010) Chemoenzymatic synthesis and enzymatic analysis of 8-modified cytidine monophosphate-sialic acid and sialyl lactose derivatives. J. Am. Chem. Soc. 132, 9430-9437
30. Wichterle, H., Lieberam, I., Porter, J. A., and Jessell, T. M. (2002) Directed differentiation of embryonic stem cells into motor neurons. Cell 110, 385-397
31. Wichterle, H., and Peljto, M. (2008) Differentiation of mouse embryonic stem cells to spinal motor neurons. Curr. Protoc. Stem. Cell Biol. Chapter 1, Unit 1H 1 1-1H 1 9
32. Li, X. J., Hu, B. Y., Jones, S. A., Zhang, Y. S., Lavaute, T., Du, Z. W., and Zhang, S. C. (2008) Directed differentiation of ventral spinal progenitors and motor neurons from human embryonic stem cells by small molecules. Stem Cells 26, 886-893
33. Vimr, E. R., McCoy, R. D., Vollger, H. F., Wilkison, N. C., and Troy, F. A. (1984) Use of prokaryotic-derived probes to identify poly(sialic acid) in neonatal neuronal membranes. Proc. Natl. Acad. Sci. U.S.A. 81, 1971-1975 (Pubitemid 14146588)
34. Hoffman, S., and Edelman, G. M. (1983) Kinetics of homophilic binding by embryonic and adult forms of the neural cell adhesion molecule. Proc. Natl. Acad. Sci. U.S.A. 80, 5762-5766 (Pubitemid 14249908)
35. Rutishauser, U., and Landmesser, L. (1996) Polysialic acid in the vertebrate nervous system: a promoter of plasticity in cell-cell interactions. Trends Neurosci. 19, 422-427 (Pubitemid 26302074)
36. Franz, C. K., Rutishauser, U., and Rafuse, V. F. (2005) Polysialylated neural cell adhesion molecule is necessary for selective targeting of regenerating motor neurons. J. Neurosci. 25, 2081-2091 (Pubitemid 40289413)