Schwann-spheres derived from injured peripheral nerves in adult mice - their in vitro characterization and therapeutic potential

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Takagi, Takehiko ^a   Ishii, Ken ^a   Shibata, Shinsuke ^a   Yasuda, Akimasa ^a   Sato, Momoka ^a,b   Nagoshi, Narihito ^c   Saito, Harukazu ^c   Okano, Hirotaka J ^a   Toyama, Yoshiaki ^a   Okano, Hideyuki ^a   Nakamura, Masaya ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b KEIO UNIVERSITY   (Japan)

^c NATIONAL HOSPITAL ORGANIZATION MURAYAMA MEDICAL CENTER   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ACTIN; CELL PROTEIN; NESTIN; PROTEIN MUSASHI1; PROTEIN P75; TRANSCRIPTION FACTOR PAX3; TRANSCRIPTION FACTOR SOX10; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; ENHANCED GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL ISOLATION; CELL LINEAGE; CELL RENEWAL; CONTROLLED STUDY; CULTURE TECHNIQUE; FEMALE; IN VITRO STUDY; MOUSE; MYELINATION; NERVE CELL CULTURE; NERVE FIBER GROWTH; NEURAL STEM CELL; NONHUMAN; PERIPHERAL NERVE; PERIPHERAL NERVE INJURY; SCHWANN CELL; SCIATIC NERVE; AGING; ANIMAL; C57BL MOUSE; CELL PROLIFERATION; GENE EXPRESSION REGULATION; GENETICS; INJURY; METABOLISM; MULTICELLULAR SPHEROID; MYELIN SHEATH; NEURITE; PATHOLOGY; STEM CELL; TRANSPLANTATION;

MUS;

AGING; ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL PROLIFERATION; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; MICE; MICE, INBRED C57BL; MYELIN SHEATH; NEURITES; RNA, MESSENGER; SCHWANN CELLS; SCIATIC NERVE; SPHEROIDS, CELLULAR; STEM CELLS;

EID: 79959603521     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021497     Document Type: Article

References (54)

1. Morrison SJ, White PM, Zock C, Anderson DJ, (1999) Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells. Cell 96: 737-749.
2. Mirsky R, Jessen KR, Brennan A, Parkinson D, Dong Z, et al. (2002) Schwann cells as regulators of nerve development. J Physiol Paris 96: 17-24.
3. Jessen KR, Mirsky R, (2005) The origin and development of glial cells in peripheral nerves. Nat Rev Neurosci 6: 671-682.
4. Toma JG, Akhavan M, Fernandes KJ, Barnabe-Heider F, Sadikot A, et al. (2001) Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat Cell Biol 3: 778-784.
5. Wong CE, Paratore C, Dours-Zimmermann MT, Rochat A, Pietri T, et al. (2006) Neural crest-derived cells with stem cell features can be traced back to multiple lineages in the adult skin. J Cell Biol 175: 1005-1015.
6. Kawaguchi A, Miyata T, Sawamoto K, Takashita N, Murayama A, et al. (2001) Nestin-EGFP transgenic mice: visualization of the self-renewal and multipotency of CNS stem cells. Mol Cell Neurosci 17: 259-273.
7. Hisahara S, Araki T, Sugiyama F, Yagami K, Suzuki M, et al. (2000) Targeted expression of baculovirus p35 caspase inhibitor in oligodendrocytes protects mice against autoimmune-mediated demyelination. EMBO J 19: 341-348.
8. Kawamoto S, Niwa H, Tashiro F, Sano S, Kondoh G, et al. (2000) A novel reporter mouse strain that expresses enhanced green fluorescent protein upon Cre-mediated recombination. FEBS Lett 470: 263-268.
9. Kohyama J, Kojima T, Takatsuka E, Yamashita T, Namiki J, et al. (2008) Epigenetic regulation of neural cell differentiation plasticity in the adult mammalian brain. Proc Natl Acad Sci U S A 105: 18012-18017.
10. Nagoshi N, Shibata S, Kubota Y, Nakamura M, Nagai Y, et al. (2008) Ontogeny and multipotency of neural crest-derived stem cells in mouse bone marrow, dorsal root ganglia, and whisker pad. Cell Stem Cell 2: 392-403.
11. Aguayo AJ, David S, Bray GM, (1981) Influences of the glial environment on the elongation of axons after injury: transplantation studies in adult rodents. J Exp Biol 95: 231-240.
12. Yoshida S, Shimmura S, Nagoshi N, Fukuda K, Matsuzaki Y, et al. (2006) Isolation of multipotent neural crest-derived stem cells from the adult mouse cornea. Stem Cells 24: 2714-2722.
13. Hoshikawa S, Ogata T, Fujiwara S, Nakamura K, Tanaka S, (2008) A novel function of RING finger protein 10 in transcriptional regulation of the myelin-associated glycoprotein gene and myelin formation in Schwann cells. PLoS One 3: e3464.
14. Vukojevic K, Petrovic D, Saraga-Babic M Nestin expression in glial and neuronal progenitors of the developing human spinal ganglia. Gene Expr Patterns 10: 144-151.
15. Kuhlbrodt K, Herbarth B, Sock E, Hermans-Borgmeyer I, Wegner M, (1998) Sox10, a novel transcriptional modulator in glial cells. J Neurosci 18: 237-250.
16. Stolt CC, Lommes P, Friedrich RP, Wegner M, (2004) Transcription factors Sox8 and Sox10 perform non-equivalent roles during oligodendrocyte development despite functional redundancy. Development 131: 2349-2358.
17. Agudo M, Woodhoo A, Webber D, Mirsky R, Jessen KR, et al. (2008) Schwann cell precursors transplanted into the injured spinal cord multiply, integrate and are permissive for axon growth. Glia 56: 1263-1270.
18. Molteni R, Zheng JQ, Ying Z, Gomez-Pinilla F, Twiss JL, (2004) Voluntary exercise increases axonal regeneration from sensory neurons. Proc Natl Acad Sci U S A 101: 8473-8478.
19. Fortun J, Hill CE, Bunge MB, (2009) Combinatorial strategies with Schwann cell transplantation to improve repair of the injured spinal cord. Neurosci Lett 456: 124-132.
20. Hood B, Levene HB, Levi AD, (2009) Transplantation of autologous Schwann cells for the repair of segmental peripheral nerve defects. Neurosurg Focus 26: E4.
21. Kulbatski I, Mothe AJ, Parr AM, Kim H, Kang CE, et al. (2008) Glial precursor cell transplantation therapy for neurotrauma and multiple sclerosis. Prog Histochem Cytochem 43: 123-176.
22. Xu XM, Zhang SX, Li H, Aebischer P, Bunge MB, (1999) Regrowth of axons into the distal spinal cord through a Schwann-cell-seeded mini-channel implanted into hemisected adult rat spinal cord. Eur J Neurosci 11: 1723-1740.
23. Takami T, Oudega M, Bates ML, Wood PM, Kleitman N, et al. (2002) Schwann cell but not olfactory ensheathing glia transplants improve hindlimb locomotor performance in the moderately contused adult rat thoracic spinal cord. J Neurosci 22: 6670-6681.
24. Grimpe B, Pressman Y, Lupa MD, Horn KP, Bunge MB, et al. (2005) The role of proteoglycans in Schwann cell/astrocyte interactions and in regeneration failure at PNS/CNS interfaces. Mol Cell Neurosci 28: 18-29.
25. Plant GW, Bates ML, Bunge MB, (2001) Inhibitory proteoglycan immunoreactivity is higher at the caudal than the rostral Schwann cell graft-transected spinal cord interface. Mol Cell Neurosci 17: 471-487.
26. Chau CH, Shum DK, Li H, Pei J, Lui YY, et al. (2004) Chondroitinase ABC enhances axonal regrowth through Schwann cell-seeded guidance channels after spinal cord injury. FASEB J 18: 194-196.
27. Fouad K, Schnell L, Bunge MB, Schwab ME, Liebscher T, et al. (2005) Combining Schwann cell bridges and olfactory-ensheathing glia grafts with chondroitinase promotes locomotor recovery after complete transection of the spinal cord. J Neurosci 25: 1169-1178.
28. Weidner N, Blesch A, Grill RJ, Tuszynski MH, (1999) Nerve growth factor-hypersecreting Schwann cell grafts augment and guide spinal cord axonal growth and remyelinate central nervous system axons in a phenotypically appropriate manner that correlates with expression of L1. J Comp Neurol 413: 495-506.
29. Jones LL, Oudega M, Bunge MB, Tuszynski MH, (2001) Neurotrophic factors, cellular bridges and gene therapy for spinal cord injury. J Physiol 533: 83-89.
30. Golden KL, Pearse DD, Blits B, Garg MS, Oudega M, et al. (2007) Transduced Schwann cells promote axon growth and myelination after spinal cord injury. Exp Neurol 207: 203-217.
31. Pearse DD, Pereira FC, Marcillo AE, Bates ML, Berrocal YA, et al. (2004) cAMP and Schwann cells promote axonal growth and functional recovery after spinal cord injury. Nat Med 10: 610-616.
32. Casella GT, Bunge RP, Wood PM, (1996) Improved method for harvesting human Schwann cells from mature peripheral nerve and expansion in vitro. Glia 17: 327-338.
33. Haastert K, Mauritz C, Chaturvedi S, Grothe C, (2007) Human and rat adult Schwann cell cultures: fast and efficient enrichment and highly effective non-viral transfection protocol. Nat Protoc 2: 99-104.
34. Iwashita Y, Fawcett JW, Crang AJ, Franklin RJ, Blakemore WF, (2000) Schwann cells transplanted into normal and X-irradiated adult white matter do not migrate extensively and show poor long-term survival. Exp Neurol 164: 292-302.
35. Hill CE, Moon LD, Wood PM, Bunge MB, (2006) Labeled Schwann cell transplantation: cell loss, host Schwann cell replacement, and strategies to enhance survival. Glia 53: 338-343.
36. Biernaskie J, Sparling JS, Liu J, Shannon CP, Plemel JR, et al. (2007) Skin-derived precursors generate myelinating Schwann cells that promote remyelination and functional recovery after contusion spinal cord injury. J Neurosci 27: 9545-9559.
37. McKenzie IA, Biernaskie J, Toma JG, Midha R, Miller FD, (2006) Skin-derived precursors generate myelinating Schwann cells for the injured and dysmyelinated nervous system. J Neurosci 26: 6651-6660.
38. Cummings BJ, Uchida N, Tamaki SJ, Salazar DL, Hooshmand M, et al. (2005) Human neural stem cells differentiate and promote locomotor recovery in spinal cord-injured mice. Proc Natl Acad Sci U S A 102: 14069-14074.
39. Nakamura M, Okano H, Toyama Y, Dai HN, Finn TP, et al. (2005) Transplantation of embryonic spinal cord-derived neurospheres support growth of supraspinal projections and functional recovery after spinal cord injury in the neonatal rat. J Neurosci Res 81: 457-468.
40. Ogawa Y, Sawamoto K, Miyata T, Miyao S, Watanabe M, et al. (2002) Transplantation of in vitro-expanded fetal neural progenitor cells results in neurogenesis and functional recovery after spinal cord contusion injury in adult rats. J Neurosci Res 69: 925-933.
41. Iwanami A, Kaneko S, Nakamura M, Kanemura Y, Mori H, et al. (2005) Transplantation of human neural stem cells for spinal cord injury in primates. J Neurosci Res 80: 182-190.
42. Fernandes KJ, McKenzie IA, Mill P, Smith KM, Akhavan M, et al. (2004) A dermal niche for multipotent adult skin-derived precursor cells. Nat Cell Biol 6: 1082-1093.
43. Li L, Mignone J, Yang M, Matic M, Penman S, et al. (2003) Nestin expression in hair follicle sheath progenitor cells. Proc Natl Acad Sci U S A 100: 9958-9961.
44. Amoh Y, Li L, Katsuoka K, Penman S, Hoffman RM, (2005) Multipotent nestin-positive, keratin-negative hair-follicle bulge stem cells can form neurons. Proc Natl Acad Sci U S A 102: 5530-5534.
45. Amoh Y, Li L, Campillo R, Kawahara K, Katsuoka K, et al. (2005) Implanted hair follicle stem cells form Schwann cells that support repair of severed peripheral nerves. Proc Natl Acad Sci U S A 102: 17734-17738.
46. Amoh Y, Kanoh M, Niiyama S, Hamada Y, Kawahara K, et al. (2009) Human hair follicle pluripotent stem (hfPS) cells promote regeneration of peripheral-nerve injury: an advantageous alternative to ES and iPS cells. J Cell Biochem 107: 1016-1020.
47. Amoh Y, Li L, Katsuoka K, Hoffman RM, (2008) Multipotent hair follicle stem cells promote repair of spinal cord injury and recovery of walking function. Cell Cycle 7: 1865-1869.
48. Liu F, Uchugonova A, Kimura H, Zhang C, Zhao M, et al. (2011) The bulge area is the major hair follicle source of nestin-expressing pluripotent stem cells which can repair the spinal cord compared to the dermal papilla. Cell Cycle 10: 830-839.
49. Kumagai G, Okada Y, Yamane J, Nagoshi N, Kitamura K, et al. (2009) Roles of ES cell-derived gliogenic neural stem/progenitor cells in functional recovery after spinal cord injury. PLoS One 4: e7706.
50. Tsuji O, Miura K, Okada Y, Fujiyoshi K, Mukaino M, et al. (2010) Therapeutic potential of appropriately evaluated safe-induced pluripotent stem cells for spinal cord injury. Proceedings of the National Academy of Sciences of the United States of America 107: 12704-12709.
51. Widera D, Heimann P, Zander C, Imielski Y, Heidbreder M, et al. (2011) Schwann Cells can be reprogrammed to multipotency by culture. Stem Cells Dev. (in press).
52. Takahashi K, Yamanaka S, (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676.
53. Wernig M, Zhao JP, Pruszak J, Hedlund E, Fu D, et al. (2008) Neurons derived from reprogrammed fibroblasts functionally integrate into the fetal brain and improve symptoms of rats with Parkinson's disease. Proc Natl Acad Sci U S A 105: 5856-5861.
54. Miura K, Okada Y, Aoi T, Okada A, Takahashi K, et al. (2009) Variation in the safety of induced pluripotent stem cell lines. Nat Biotechnol 27: 743-745.