Improved stem cell-derived motoneuron survival, migration, sprouting, and innervation with enhanced expression of polysialic acid

Cell Transplantation

Volumn 24, Issue 5, 2015, Pages 797-809

  El Maarouf, Abderrahman ^a   Moyo Lee Yaw, Damali ^a   Rutishauser, Urs ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Cell engineering; Innervation; Motor neurons; Polysialylation; Stem cells; Transplantation

Indexed keywords

GREEN FLUORESCENT PROTEIN; POLYSIALIC ACID; POLYSIALYLTRANSFERASE; SIALYLTRANSFERASE; UNCLASSIFIED DRUG; SIALIC ACID DERIVATIVE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL POPULATION; CELL SURVIVAL; COCULTURE; CONTROLLED STUDY; EMBRYO; EMBRYOID BODY; EMBRYONIC STEM CELL; FAST MUSCLE; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; INNERVATION; MALE; MOTONEURON; MOUSE; MUSCLE DENERVATION; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVE ENDING; NERVE FIBER; NERVE FIBER GROWTH; NERVE SPROUTING; NEURAL STEM CELL; NEURAL STEM CELL TRANSPLANTATION; NEURITE; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; SCHWANN CELL; SCIATIC NERVE; STEM CELL CULTURE; UPREGULATION; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; CELL MOTION; CYTOLOGY; METABOLISM; PATHOLOGY; STEM CELL TRANSPLANTATION; TRANSGENIC MOUSE;

ANIMALS; AXONS; CELL MOVEMENT; CELL SURVIVAL; EMBRYONIC STEM CELLS; MICE; MICE, TRANSGENIC; MOTOR NEURONS; NEURITES; SCIATIC NERVE; SIALIC ACIDS; SIALYLTRANSFERASES; STEM CELL TRANSPLANTATION;

EID: 84928945795     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368914X679228     Document Type: Article

References (30)

1. Acheson, A.; Sunshine, J. L.; Rutishauser, U. NCAM polysialic acid can regulate both cell-cell and cell-substrate interactions. J. Cell Biol. 114(1):143–153; 1991.
2. Alderson, K.; Pestronk, A.; Yee, W. C.; Drachman, D. B. Silver cholinesterase immunocytochemistry: A new neuro-muscular junction stain. Muscle Nerve 12(1):9–14; 1989.
3. Angata, K.; Huckaby, V.; Ranscht, B.; Terskikh, A.; Marth, J. D.; Fukuda, M. Polysialic acid-directed migration and differentiation of neural precursors are essential for mouse brain development. Mol. Cell. Biol. 27(19):6659–6668; 2007.
4. Battista, D.; Ganat, Y.; El Maarouf, A.; Studer, L.; Rutishauser, U. Enhancement of polysialic acid expression improves function of embryonic stem-derived dopamine neuron grafts in Parkinsonian mice. Stem Cells Transl. Med. 3(1):108–113; 2013.
5. Boisseau, S.; Nedelec, J.; Poirier, V.; Rougon, G.; Simonneau, M. Analysis of high PSA N-CAM expression during mammalian spinal cord and peripheral nervous system development. Development 112(1):69–82; 1991.
6. Deshpande, D. M.; Kim, Y. S.; Martinez, T.; Carmen, J.; Dike, S.; Shats, I.; Rubin, L. L.; Drummond, J.; Krishnan, C.; Hoke, A.; Maragakis, N.; Shefner J.; Rothstein, J. D.; Kerr, D. A. Recovery from paralysis in adult rats using embryonic stem cells. Ann. Neurol. 60(1):32–44; 2006.
7. El Maarouf, A.; Moyo-Lee Yaw, D.; Lindhout, T.; Pearse, D. D.; Wakarchuk, W.; Rutishauser, U. Enzymatic engineering of polysialic acid on cells in vitro and in vivo using a purified bacterial polysialyltransferase. J. Biol. Chem. 287(39):32770–32779; 2012.
8. El Maarouf, A.; Petridis, A. K.; Rutishauser, U. Use of polysialic acid in repair of the central nervous system. Proc. Natl. Acad. Sci. USA 103(45):16989–16994; 2006.
9. El Maarouf, A.; Rutishauser, U. Removal of polysialic acid induces aberrant pathways, synaptic vesicle distribution, and terminal arborization of retinotectal axons. J. Comp. Neurol. 460(2):203–211; 2003.
10. El Maarouf, A.; Rutishauser, U. Use of PSA-NCAM in repair of the central nervous system. Adv. Exp. Med. Biol. 663:137–147; 2010.
11. Franz, C. K.; Rutishauser, U.; Rafuse, V. F. Intrinsic neuro-nal properties control selective targeting of regenerating motoneurons. Brain 131(6):1492–1505; 2008.
12. Franz, C. K.; Rutishauser, U.; Rafuse, V. F. Polysialylated neural cell adhesion molecule is necessary for selective targeting of regenerating motor neurons. J. Neurosci. 25(8): 2081–2091; 2005.
13. Gascon, E.; Vutskits, L.; Jenny, B.; Durbec, P.; Kiss, J. Z. PSA-NCAM in postnatally generated immature neurons of the olfactory bulb: A crucial role in regulating p75 expression and cell survival. Development 134(6):1181–1190; 2007.
14. Gascon, E.; Vutskits, L.; Kiss, J. Z. The role of PSA-NCAM in adult neurogenesis. Adv. Exp. Med. Biol. 663:127–136; 2010.
15. Ghosh, M.; Tuesta, L. M.; Puentes, R.; Patel, S.; Melendez, K.; El Maarouf, A.; Rutishauser, U.; Pearse, D. D. Extensive cell migration, axon regeneration, and improved function with polysialic acid-modified Schwann cells after spinal cord injury. Glia 60(6):979–992; 2012.
16. Li, X. J.; Hu, B. Y.; Jones, S. A.; Zhang, Y. S.; Lavaute, T.; Du, Z. W.; Zhang, S. C. Directed differentiation of ventral spinal progenitors and motor neurons from human embryonic stem cells by small molecules. Stem Cells 26(4): 886–893; 2008.
17. Liu, Y.; Namba, T.; Liu, J.; Suzuki, R.; Shioda, S.; Seki, T. Glial fibrillary acidic protein-expressing neural progenitors give rise to immature neurons via early intermediate progenitors expressing both glial fibrillary acidic protein and neuronal markers in the adult hippocampus. Neuroscience 166(1):241–251; 2010.
18. MacDonald, S. C.; Fleetwood, I. G.; Hochman, S.; Dodd, J. G.; Cheng, G. K.; Jordan, L. M.; Brownstone, R. M. Functional motor neurons differentiating from mouse multi-potent spinal cord precursor cells in culture and after transplantation into transected sciatic nerve. J. Neurosurg. 98(5): 1094–1103; 2003.
19. Palmgren, B.; Jiao, Y.; Novozhilova, E.; Stupp, S. I.; Olivius, P. Survival, migration and differentiation of mouse tau-GFP embryonic stem cells transplanted into the rat auditory nerve. Exp. Neurol. 235(2):599–609; 2012.
20. Pestronk, A.; Drachman, D. B. A new stain for quantitative measurement of sprouting at neuromuscular junctions. Muscle Nerve 1(1):70–74; 1978.
21. Petridis, A. K.; El-Maarouf, A.; Rutishauser, U. Polysialic acid regulates cell contact-dependent neuronal differentiation of progenitor cells from the subventricular zone. Dev. Dyn. 230(4):675–684; 2004.
22. Rutishauser, U. Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat. Rev. Neurosci. 9(1):26–35; 2008.
23. Rutishauser, U.; Landmesser, L. Polysialic acid in the vertebrate nervous system: a promoter of plasticity in cell-cell interactions. Trends Neurosci. 19(10):422–427; 1996.
24. Soundararajan, P.; Miles, G. B.; Rubin, L. L.; Brownstone, R. M.; Rafuse, V. F. Motoneurons derived from embryonic stem cells express transcription factors and develop pheno-types characteristic of medial motor column neurons. J. Neurosci. 26(12):3256–3268; 2006.
25. Tang, J.; Landmesser, L. Reduction of intramuscular nerve branching and synaptogenesis is correlated with decreased motoneuron survival. J. Neurosci. 13(7):3095–3103; 1993.
26. Tang, J.; Landmesser, L.; Rutishauser, U. Polysialic acid influences specific pathfinding by avian motoneurons. Neuron 8(6):1031–1044; 1992.
27. Tang, J.; Rutishauser, U.; Landmesser, L. Polysialic acid regulates growth cone behavior during sorting of motor axons in the plexus region. Neuron 13(2):405–414; 1994.
28. Wichterle, H.; Lieberam, I.; Porter, J. A.; Jessell, T. M. Directed differentiation of embryonic stem cells into motor neurons. Cell 110(3):385–397; 2002.
29. Wichterle, H.; Peljto, M. Differentiation of mouse embryonic stem cells to spinal motor neurons. Curr. Protoc. Stem Cell Biol. 1(1H):1–9; 2008.
30. Yohn, D. C.; Miles, G. B.; Rafuse, V. F.; Brownstone, R. M. Transplanted mouse embryonic stem-cell-derived motoneurons form functional motor units and reduce muscle atrophy. J. Neurosci. 28(47):12409–12418; 2008.