Human dental pulp stem cells can differentiate into Schwann cells and promote and guide neurite outgrowth in an aligned tissue-engineered collagen construct in vitro

FASEB Journal

Volumn 28, Issue 4, 2014, Pages 1634-1643

  Martens, Wendy ^a   Sanen, Kathleen ^a   Georgiou, Melanie ^b,c   Struys, Tom ^a   Bronckaers, Annelies ^a   Ameloot, Marcel ^a   Phillips, James ^b,c   Lambrichts, Ivo ^a  

^a HASSELT UNIVERSITY   (Belgium)

^b OPEN UNIVERSITY   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Cellular hydrogel; Glial cell; Myelination; Nerve repair; Neural regeneration

Indexed keywords

COLLAGEN TYPE 1; NEUROTROPHIC FACTOR;

ADULT; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL STRUCTURE; CELL SURVIVAL; CONTROLLED STUDY; DENTAL PULP STEM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; GLIAL CELL CULTURE; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOPHENOTYPING; MYELINATION; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; SCHWANN CELL; SPINAL GANGLION; STEM CELL; TISSUE ENGINEERING; TOOTH PULP; TRANSMISSION ELECTRON MICROSCOPY;

CELLULAR HYDROGEL; GLIAL CELL; MYELINATION; NERVE REPAIR; NEURAL REGENERATION;

ADOLESCENT; ANIMALS; ANIMALS, NEWBORN; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELLS, CULTURED; COLLAGEN; DENTAL PULP; GANGLIA, SPINAL; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; IMMUNOHISTOCHEMISTRY; LAMININ; MICROSCOPY, ELECTRON, TRANSMISSION; MYELIN SHEATH; NESTIN; NEURITES; RATS; RATS, SPRAGUE-DAWLEY; SCHWANN CELLS; STEM CELLS; TISSUE ENGINEERING; YOUNG ADULT;

EID: 84901068695     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-243980     Document Type: Article

References (52)

1. Deumens, R., Bozkurt, A., Meek, M. F., Marcus, M. A., Joosten, E. A., Weis, J., and Brook, G. A. (2010) Repairing injured peripheral nerves: bridging the gap. Progr. Neurobiol. 92, 245-276
2. Hall, S. M. (1986) The effect of inhibiting Schwann cell mitosis on the re-innervation of acellular autografts in the peripheral nervous system of the mouse. Neuropathol. Appl. Neurobiol. 12, 401-414
3. Ichihara, S., Inada, Y., and Nakamura, T. (2008) Artificial nerve tubes and their application for repair of peripheral nerve injury: an update of current concepts. Injury 39(Suppl. 4), 29-39
4. Bell, J. H., and Haycock, J. W. (2012) Next generation nerve guides: materials, fabrication, growth factors, and cell delivery. Tissue Eng. B Rev. 18, 116-128
5. Gu, X., Ding, F., Yang, Y., and Liu, J. (2011) Construction of tissue engineered nerve grafts and their application in peripheral nerve regeneration. Progr. Neurobiol. 93, 204-230
6. Nectow, A. R., Marra, K. G., and Kaplan, D. L. (2012) Biomaterials for the development of peripheral nerve guidance conduits. Tissue Eng. B Rev. 18, 40-50
7. Aurand, E. R., Lampe, K. J., and Bjugstad, K. B. (2012) Defining and designing polymers and hydrogels for neural tissue engineering. Neurosci. Res. 72, 199-213
8. Geckil, H., Xu, F., Zhang, X., Moon, S., and Demirci, U. (2010) Engineering hydrogels as extracellular matrix mimics. Nanomedicine 5, 469-484
9. Brown, R. A., and Phillips, J. B. (2007) Cell responses to biomimetic protein scaffolds used in tissue repair and engineering. Int. Rev. Cytol. 262, 75-150
10. Georgiou, M., Bunting, S. C., Davies, H. A., Loughlin, A. J., Golding, J. P., and Phillips, J. B. (2013) Engineered neural tissue for peripheral nerve repair. Biomaterials 34, 7335-7343
11. Ren, Z., Wang, Y., Peng, J., Zhao, Q., and Lu, S. (2012) Role of stem cells in the regeneration and repair of peripheral nerves. Rev. Neurosci. 23, 135-143
12. Terenghi, G., Wiberg, M., and Kingham, P. J. (2009) Chapter 21: use of stem cells for improving nerve regeneration. Int. Rev. Neurobiol. 87, 393-403
13. Javazon, E. H., Beggs, K. J., and Flake, A. W. (2004) Mesenchymal stem cells: paradoxes of passaging. Exp. Hematol. 32, 414-425
14. Ross, J. J., and Verfaillie, C. M. (2008) Evaluation of neural plasticity in adult stem cells. Phil. Trans. R. Soc. Lond. 363, 199-205
15. Gronthos, S., Mankani, M., Brahim, J., Robey, P. G., and Shi, S. (2000) Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc. Natl. Acad. Sci. U. S. A. 97, 13625-13630
16. Chai, Y., Jiang, X., Ito, Y., Bringas, P., Jr., Han, J., Rowitch, D. H., Soriano, P., McMahon, A. P., and Sucov, H. M. (2000) Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development 127, 1671-1679
17. Graham, A., Begbie, J., and McGonnell, I. (2004) Significance of the cranial neural crest. Dev. Dyn. 229, 5-13
18. Miletich, I., and Sharpe, P. T. (2004) Neural crest contribution to mammalian tooth formation. Birth Defects Res. C Embryo Today 72, 200-212
19. Thesleff, I., and Aberg, T. (1999) Molecular regulation of tooth development. Bone 25, 123-125
20. Papaccio, G., Graziano, A., d'Aquino, R., Graziano, M. F., Pirozzi, G., Menditti, D., De Rosa, A., Carinci, F., and Laino, G. (2006) Long-term cryopreservation of dental pulp stem cells (SBP-DPSCs) and their differentiated osteoblasts: a cell source for tissue repair. J. Cell. Physiol. 208, 319-325
21. Huang, A. H., Snyder, B. R., Cheng, P. H., and Chan, A. W. (2008) Putative dental pulp-derived stem/stromal cells promote proliferation and differentiation of endogenous neural cells in the hippocampus of mice. Stem Cells 26, 2654-2663
22. Martens, W., Bronckaers, A., Politis, C., Jacobs, R., and Lambrichts, I. (2013) Dental stem cells and their promising role in neural regeneration: an update. Clin. Oral Invest. 17, 1969-1983
23. Nosrat, I. V., Smith, C. A., Mullally, P., Olson, L., and Nosrat, C. A. (2004) Dental pulp cells provide neurotrophic support for dopaminergic neurons and differentiate into neurons in vitro; implications for tissue engineering and repair in the nervous system. Eur. J. Neurosci. 19, 2388-2398
24. Nosrat, I. V., Widenfalk, J., Olson, L., and Nosrat, C. A. (2001) Dental pulp cells produce neurotrophic factors, interact with trigeminal neurons in vitro, and rescue motoneurons after spinal cord injury. Dev. Biol. 238, 120-132
25. Arthur, A., Shi, S., Zannettino, A. C., Fujii, N., Gronthos, S., and Koblar, S. A. (2009) Implanted adult human dental pulp stem cells induce endogenous axon guidance. Stem Cells 27, 2229-2237
26. Arthur, A., Rychkov, G., Shi, S., Koblar, S. A., and Gronthos, S. (2008) Adult human dental pulp stem cells differentiate toward functionally active neurons under appropriate environmental cues. Stem Cells 26, 1787-1795
27. Gronthos, S., Brahim, J., Li, W., Fisher, L. W., Cherman, N., Boyde, A., DenBesten, P., Robey, P. G., and Shi, S. (2002) Stem cell properties of human dental pulp stem cells. J. Dental Res. 81, 531-535
28. Kiraly, M., Porcsalmy, B., Pataki, A., Kadar, K., Jelitai, M., Molnar, B., Hermann, P., Gera, I., Grimm, W. D., Ganss, B., Zsembery, A., and Varga, G. (2009) Simultaneous PKC and cAMP activation induces differentiation of human dental pulp stem cells into functionally active neurons. Neurochem. Int. 55, 323-332
29. Struys, T., Moreels, M., Martens, W., Donders, R., Wolfs, E., and Lambrichts, I. (2011) Ultrastructural and immunocytochemical analysis of multilineage differentiated human dental pulp-and umbilical cord-derived mesenchymal stem cells. Cells Tissues Organs 193, 366-378
30. Dezawa, M., Takahashi, I., Esaki, M., Takano, M., and Sawada, H. (2001) Sciatic nerve regeneration in rats induced by transplantation of in vitro differentiated bone-marrow stromal cells. Eur. J. Neurosci. 14, 1771-1776
31. Wei, Y., Zhou, J., Zheng, Z., Wang, A., Ao, Q., Gong, Y., and Zhang, X. (2009) An improved method for isolating Schwann cells from postnatal rat sciatic nerves. Cell Tissue Res. 337, 361-369
32. Bretschneider, A., Burns, W., and Morrison, A. (1981) "Pop-off" technic. The ultrastructure of paraffin-embedded sections. Am. J. Clin. Pathol. 76, 450-453
33. Phillips, J. B., and Brown, R. A. (2004) Self-aligning tissue growth guide. International Patent WO2004087231
34. Brown, R. A., Wiseman, M., Chuo, C. B., Cheema, U., and Nazhat, S. N. (2005) Ultrarapid engineering of biomimetic materials and tissues: fabrication of nano-and microstructures by plastic compression. Adv. Func. Mater. 15, 1762-1770
35. Phillips, J. B., and Brown, R. (2011) Micro-structured materials and mechanical cues in 3D collagen gels. Methods Mol. Biol. 695, 183-196
36. East, E., Golding, J. P., and Phillips, J. B. (2009) A versatile 3D culture model facilitates monitoring of astrocytes undergoing reactive gliosis. J. Tissue Eng. Regen. Med. 3, 634-646
37. Wright, K. E., Liniker, E., Loizidou, M., Moore, C., Macrobert, A. J., and Phillips, J. B. (2009) Peripheral neural cell sensitivity to mTHPC-mediated photodynamic therapy in a 3D in vitro model. Br. J. Cancer 101, 658-665
38. Kingham, P. J., Kalbermatten, D. F., Mahay, D., Armstrong, S. J., Wiberg, M., and Terenghi, G. (2007) Adipose-derived stem cells differentiate into a Schwann cell phenotype and promote neurite outgrowth in vitro. Exp. Neurol. 207, 267-274
39. Mantovani, C., Terenghi, G., and Shawcross, S. G. (2012) Isolation of adult stem cells and their differentiation to Schwann cells. Methods Mol. Biol. 916, 47-57
40. Ibarretxe, G., Crende, O., Aurrekoetxea, M., Garcia-Murga, V., Etxaniz, J., and Unda, F. (2012) Neural crest stem cells from dental tissues: a new hope for dental and neural regeneration. Stem Cells Int. 2012, 103503
41. Pierdomenico, L., Bonsi, L., Calvitti, M., Rondelli, D., Arpinati, M., Chirumbolo, G., Becchetti, E., Marchionni, C., Alviano, F., Fossati, V., Staffolani, N., Franchina, M., Grossi, A., and Bagnara, G. P. (2005) Multipotent mesenchymal stem cells with immunosuppressive activity can be easily isolated from dental pulp. Transplantation 80, 836-842
42. Deng, W., Obrocka, M., Fischer, I., and Prockop, D. J. (2001) In vitro differentiation of human marrow stromal cells into early progenitors of neural cells by conditions that increase intracellular cyclic AMP. Biochem. Biophys. Res. Commun. 282, 148-152
43. Woodbury, D., Schwarz, E. J., Prockop, D. J., and Black, I. B. (2000) Adult rat and human bone marrow stromal cells differentiate into neurons. J. Neurosci. Res. 61, 364-370
44. Fraichard, A., Chassande, O., Bilbaut, G., Dehay, C., Savatier, P., and Samarut, J. (1995) In vitro differentiation of embryonic stem cells into glial cells and functional neurons. J. Cell Sci. 108(Pt. 10), 3181-3188
45. Gage, F. H., Coates, P. W., Palmer, T. D., Kuhn, H. G., Fisher, L. J., Suhonen, J. O., Peterson, D. A., Suhr, S. T., and Ray, J. (1995) Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain. Proc. Natl. Acad. Sci. U. S. A. 92, 11879-11883
46. Sakai, K., Yamamoto, A., Matsubara, K., Nakamura, S., Naruse, M., Yamagata, M., Sakamoto, K., Tauchi, R., Wakao, N., Imagama, S., Hibi, H., Kadomatsu, K., Ishiguro, N., and Ueda, M. (2012) Human dental pulp-derived stem cells promote locomotor recovery after complete transection of the rat spinal cord by multiple neuro-regenerative mechanisms. J. Clin. Invest. 122, 80-90
47. Frostick, S. P., Yin, Q., and Kemp, G. J. (1998) Schwann cells, neurotrophic factors, and peripheral nerve regeneration. Microsurgery 18, 397-405
48. Ribeiro-Resende, V. T., Koenig, B., Nichterwitz, S., Oberhoffner, S., and Schlosshauer, B. (2009) Strategies for inducing the formation of bands of Bungner in peripheral nerve regeneration. Biomaterials 30, 5251-5259
49. East, E., de Oliveira, D. B., Golding, J. P., and Phillips, J. B. (2010) Alignment of astrocytes increases neuronal growth in three-dimensional collagen gels and is maintained following plastic compression to form a spinal cord repair conduit. Tissue Eng. 16, 3173-3184
50. Lietz, M., Dreesmann, L., Hoss, M., Oberhoffner, S., and Schlosshauer, B. (2006) Neuro tissue engineering of glial nerve guides and the impact of different cell types. Biomaterials 27, 1425-1436
51. Phillips, J. B., Bunting, S. C., Hall, S. M., and Brown, R. A. (2005) Neural tissue engineering: a self-organizing collagen guidance conduit. Tissue Eng. 11, 1611-1617
52. Sherman, D. L., and Brophy, P. J. (2005) Mechanisms of axon ensheathment and myelin growth. Nat. Rev. Neurosci. 6, 683-690