Embryonic and adult stem cells promote raphespinal axon outgrowth and improve functional outcome following spinal hemisection in mice

European Journal of Neuroscience

Volumn 30, Issue 5, 2009, Pages 833-846

  Boido, Marina ^a   Rupa, Rosita ^a   Garbossa, Diego ^a   Fontanella, Marco ^a   Ducati, Alessandro ^a   Vercelli, Alessandro ^a  

^a Department of Anatomy Pharmacology and Forensic Medicine ^*  (Italy)

Author keywords

Cell therapy; CNS repair; Serotonergic axons; Spinal cord injury

Indexed keywords

SEROTONIN;

ADULT STEM CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; EMBRYONIC STEM CELL; FUNCTIONAL ASSESSMENT; MALE; MESENCHYMAL STEM CELL; MOTOR PERFORMANCE; MOUSE; NERVE FIBER GROWTH; NERVE REGENERATION; NEURAL STEM CELL; NEUROMERE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAPHE NUCLEUS; SPINAL CORD HEMISECTION; SPINAL CORD INJURY; STEM CELL TRANSPLANTATION; TREATMENT OUTCOME;

ANALYSIS OF VARIANCE; ANIMALS; AXONS; CELL DIFFERENTIATION; CELL SURVIVAL; CELLS, CULTURED; EMBRYONIC STEM CELLS; FLUORESCENT ANTIBODY TECHNIQUE; GLIOSIS; LUMBAR VERTEBRAE; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MICE; MICE, INBRED C57BL; RECOVERY OF FUNCTION; SEROTONIN; SPINAL CORD INJURIES;

EID: 69549124124     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2009.06879.x     Document Type: Article

References (86)

1. Ankeny, D.P., McTigue, D.M. Jakeman, L.B. (2004) Bone marrow transplants provide tissue protection and directional guidance for axons after contusive spinal cord injury in rats. Exp. Neurol., 190, 17 31.
2. Aoki, M., Fujito, Y., Satomi, H., Kurosawa, Y. Kasaba, T. (1986) The possible role of collateral sprouting in the functional restitution of corticospinal connections after spinal hemisection. Neurosci. Res., 3, 617 627.
3. Barami, K. Diaz, F.G. (2000) Cellular transplantation and spinal cord injury. Neurosurgery, 47, 691 700.
4. Bareyre, F.M., Kerschensteiner, M., Raineteau, O., Mettenleiter, T.C., Weinmann, O. Schwab, M.E. (2004) The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nat. Neurosci., 7, 269 277.
5. Basso, D.M., Fisher, L.C., Anderson, A.J., Jakeman, L.B., McTigue, D.M. Popovich, P.G. (2006) Basso Mouse Scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. J. Neurotrauma, 23, 635 659.
6. Ben-Hur, T., Ben-Menachem, O., Furer, V., Einstein, O., Mizrachi-Kol, R. Grigoriadis, N. (2003) Effects of proinflammatory cytokines on the growth fate, and motility of multipotential neural precursor cells. Mol. Cell. Neurosci., 24, 623 631.
7. Blanchart, A., De Carlos, J.A. López-Mascaraque, L. (2006) Time frame of mitral cell development in the mice olfactory bulb. J. Comp. Neurol., 496, 529 543.
8. Bowker, R.M., Westlund, K.N., Sullivan, M.C. Coulter, J.D. (1982) Organization of descending serotonergic projections to the spinal cord. Prog. Brain Res., 57, 239 265.
9. Cao, Q.L., Howard, R.M., Dennison, J.B. Whittemore, S.R. (2002) Differentiation of engrafted neuronal-restricted precursor cells is inhibited in the traumatically injured spinal cord. Exp. Neurol., 177, 349 359.
10. Collombet, J.M., Masqueliez, C., Four, E., Burckhart, M.F., Bernabé, D., Baubichon, D. Lallement, G. (2006) Early reduction of NeuN antigenicity induced by soman poisoning in mice can be used to predict delayed neuronal degeneration in the hippocampus. Neurosci. Lett., 398, 337 342.
11. Coutts, M. Keirstead, H.S. (2008) Stem cells for the treatment of spinal cord injury. Exp. Neurol., 209, 368 377.
12. Crigler, L., Robey, R.C., Asawachaicharn, A., Gaupp, D. Phinney, D.G. (2006) Human mesenchymal stem cell subpopulations express a variety of neuro-regulatory molecules and promote neuronal cell survival and neuritogenesis. Exp. Neurol., 198, 54 64.
13. Dahlstrom, A. Fuxe, K. (1964) Localization of monoamines in the lower brain stem. Experientia, 20, 398 399.
14. Davies, S.J., Fitch, M.T., Memberg, S.P., Hall, A.K., Raisman, G. Silver, J. (1997) Regeneration of adult axons in white matter tracts of the central nervous system. Nature, 390, 680 683.
15. Dumont, R.J., Okonkwo, D.O., Verna, S., Hurlbert, R.J., Boulos, P.T., Ellegala, D.B. Dumont, A.S. (2001) Acute spinal cord injury, Part I: pathophysiologic mechanisms. Clin. Neuropharmacol., 24, 254 264.
16. Eidelberg, E., Walden, J.G. Nguyen, L.H. (1981) Locomotor control in macaque monkeys. Brain, 104, 647 663.
17. Faden, A.I., Gannon, A. Basbaum, A.I. (1988) Use of serotonin immunocytochemistry as a marker of injury severity after experimental spinal trauma in rats. Brain Res., 450, 94 100.
18. Fawcett, J.W. Asher, R.A. (1999) The glial scar and central nervous system repair. Brain Res. Bull., 49, 377 391.
19. Feraboli-Lohnherr, D., Orsal, D., Yakovleff, A., Gimenez y Ribotta, M. Privat, A. (1997) Recovery of locomotor activity in the adult chronic spinal rat after sublesional transplantation of embryonic nervous cells: specific role of serotonergic neurons. Exp. Brain Res., 113, 443 454.
20. Fernandez, E., Mannino, S., Tufo, T., Pallini, R., Lauretti, L., Albanese, A. Denaro, L. (2006) The adult "paraplegic" rat: treatment with cell graftings. Surg. Neurol., 65, 223 237.
21. Forni, P.E., Scuoppo, C., Imayoshi, I., Taulli, R., Dastrù, W., Sala, V., Betz, U.A., Muzzi, P., Martinuzzi, D., Vercelli, A.E., Kageyama, R. Ponzetto, C. (2006) High levels of Cre expression in neuronal progenitors cause defects in brain development leading to microencephaly and hydrocephaly. J. Neurosci., 26, 9593 9602.
22. Garbossa, D., Fontanella, M., Fronda, C., Benevello, C., Muraca, G., Ducati, A. Vercelli, A. (2006) New strategies for repairing the injured spinal cord: role of stem cells. Neurol. Res., 28, 500 504.
23. Garcìa-Sevilla, J.A., Ferrer-Alcòn, M., Martìn, M., Kieffer, B.L. Maldonado, R. (2004) Neurofilament proteins and cAMP pathway in brains of mu-, delta- or kappa-opioid receptor gene knock-out mice: effects of chronic morphine administration. Neuropharmacology, 46, 519 530.
24. Goldstein, B., Little, J.W. Harris, R.M. (1997) Axonal sprouting following incomplete spinal cord injury: an experimental model. J. Spinal Cord Med., 20, 200 206.
25. Hadjiconstantinou, M., Panula, P., Lackovic, Z. Neff, N.H. (1984) Spinal cord serotonin: a biochemical and immunohistochemical study following transaction. Brain Res., 322, 245 254.
26. Han, S.S., Kang, D.Y., Mujtaba, T., Rao, M.S. Fischer, I. (2002) Grafted lineage-restricted precursors differentiate exclusively into neurons in the adult spinal cord. Exp. Neurol., 177, 360 375.
27. Han, S.S., Liu, Y., Tyler-Polsz, C., Rao, M.S. Fischer, I. (2004) Transplantation of glial-restricted precursor cells into the adult spinal cord: survival, glial-specific differentiation, and preferential migration in white matter. Glia, 45, 1 16.
28. Harel, N.Y. Strittmatter, S.M. (2006) Can regenerating axons recapitulate developmental guidance during recovery from spinal cord injury? Nat. Rev. Neurosci., 7, 603 616.
29. Hashimoto, T. Fukuda, N. (1991) Contribution of serotonin neurons to the functional recovery after spinal cord injury in rats. Brain Res., 539, 263 270.
30. Hill, C.E., Proschel, C., Noble, M., Mayer-Proschel, M., Gensel, J.C., Beattie, M.S. Bresnahan, J.C. (2004) Acute transplantation of glial-restricted precursor cells into spinal cord contusion injuries: survival, differentiation, and effects on lesion environment and axonal regeneration. Exp. Neurol., 190, 289 310.
31. Hockfield, S. McKay, R.D. (1985) Identification of major cell classes in the developing mammalian nervous system. J. Neurosci., 5, 3310 3328.
32. Hofstetter, C.P., Schwarz, E.J., Hess, D., Widenfalk, J., El Manira, A., Prockop, D.J. Olson, L. (2002) Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc. Natl Acad. Sci. USA, 99, 2199 2204.
33. Hofstetter, C.P., Holmström, N.A., Lilja, J.A., Schweinhardt, P., Hao, J., Spenger, C., Wiesenfeld-Hallin, Z., Kurpad, S.N., Frisén, J. Olson, L. (2005) Allodynia limits the usefulness of intraspinal neural stem cell grafts; directed differentiation improves outcome. Nat. Neurosci., 8, 346 353.
34. Hornung, J.P. (2003) The human raphe nuclei and the serotonergic system. J. Chem. Neuroanat., 26, 331 343.
35. Jones, L.L., Sajed, D. Tuszynski, M.H. (2003) Axonal regeneration through regions of chondroitin sulfate proteoglycan deposition after spinal cord injury: a balance of permissiveness and inhibition. J. Neurosci., 23, 9276 9288.
36. Kakulas, B.A. (1999) A review of the neuropathology of human spinal cord injury with emphasis on special features. J. Spinal Cord Med., 22, 119 124.
37. Karimi-Abdolrezaee, S., Eftekharpour, E., Wang, J., Morshead, C.M. Fehlings, M.G. (2006) Delayed transplantation of adult neural precursor cells promotes remyelination and functional neurological recovery after spinal cord injury. J. Neurosci., 26, 3377 3389.
38. Kiehn, O. (2006) Locomotor circuits in the mammalian spinal cord. Annu. Rev. Neurosci., 29, 279 306.
39. Le Blanc, K. (2003) Immunomodulatory effects of fetal and adult mesenchymal stem cells. Cytotherapy, 5, 485 489. (Pubitemid 38028708)
40. Lepore, A.C. Fischer, I. (2005) Lineage-restricted neural precursors survive, migrate, and differentiate following transplantation into the injured adult spinal cord. Exp. Neurol., 194, 230 242.
41. Lepore, A.C., Bakshi, A., Swanger, S.A., Rao, M.S. Fischer, I. (2005) Neural precursor cells can be delivered into the injured cervical spinal cord by intrathecal injection at the lumbar cord. Brain Res., 1045, 206 216.
42. López-Vales, R., Forés, J., Navarro, X. Verdú, E. (2007) Chronic transplantation of olfactory ensheathing cells promotes partial recovery after complete spinal cord transection in the rat. Glia, 55, 303 311.
43. Lu, P. Tuszynski, M.H. (2005) Can bone marrow-derived stem cells differentiate into functional neurons? Exp. Neurol., 193, 273 278.
44. Lu, J., Féron, F., Mackay-Sim, A. Waite, P.M. (2002) Olfactory ensheathing cells promote locomotor recovery after delayed transplantation into transected spinal cord. Brain, 125, 14 21.
45. Lu, P., Jones, L. Tuszynski, M.H. (2005) BDNF-expressing marrow stromal cells support extensive axonal growth at sites of spinal cord injury. Exp. Neurol., 191, 344 360.
46. Lu, P., Jones, L.L. Tuszynski, M.H. (2007) Axon regeneration through scars and into sites of chronic spinal cord injury. Exp. Neurol., 203, 8 21.
47. Maier, I.C. Schwab, M.E. (2006) Sprouting, regeneration and circuit formation in the injured spinal cord: factors and activity. Philos. Trans. R. Soc. Lond. B Biol. Sci., 361, 1611 1634.
48. Mareschi, K., Novara, M., Rustichelli, D., Ferrero, I., Guido, D., Carbone, E., Medico, E., Madon, E., Vercelli, A. Fagioli, F. (2006) Neural differentiation of human mesenchymal stem cells: evidence for expression of neural markers and eag K+ channel types. Exp. Hematol., 34, 1563 1572.
49. McDonald, J.W. Sadowsky, C. (2002) Spinal-cord injury. Lancet, 359, 417 425.
50. McGraw, J., Hiebert, G.W. Steeves, J.D. (2001) Modulating astrogliosis after neurotrauma. J. Neurosci. Res., 63, 109 115.
51. Metz, G.A., Dietz, V., Schwab, M.E. van de Meent, H. (1998) The effects of unilateral pyramidal tract section on hindlimb motor performance in the rat. Behav. Brain Res., 96, 37 46.
52. Mitsui, T., Shumsky, J.S., Lepore, A.C., Murray, M. Fischer, I. (2005) Transplantation of neuronal and glial restricted precursors into contused spinal cord improves bladder and motor functions, decreases thermal hypersensitivity, and modifies intraspinal circuitry. J. Neurosci., 25, 9624 9636.
53. Mujtaba, T., Piper, D.R., Kalyani, A., Groves, A.K., Lucero, M.T. Rao, M.S. (1999) Lineage-restricted neural precursors can be isolated from both the mouse neural tube and cultured ES cells. Dev. Biol., 214, 113 127.
54. Mullen, R.J., Buck, C.R. Smith, A.M. (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development, 116, 201 211.
55. Müllner, A., Gonzenbach, R.R., Weinmann, O., Schnell, L., Liebscher, T. Schwab, M.E. (2008) Lamina-specific restoration of serotonergic projections after Nogo-A antibody treatment of spinal cord injury in rats. Eur. J. Neurosci., 27, 326 333.
56. Neuhuber, B., Himes, B.T., Shumsky, J.S., Gallo, G. Fischer, I. (2005) Axon growth and recovery of function supported by human bone marrow stromal cells in the injured spinal cord exhibit donor variations. Brain Res., 1035, 73 85.
57. Okabe, M., Ikawa, M., Kominami, K., Nakanishi, T. Nishimune, Y. (1997) 'Green mice' as a source of ubiquitous green cells. FEBS Lett., 407, 313 319.
58. Okada, S., Ishii, K., Yamane, J., Iwanami, A., Ikegami, T., Katoh, H., Iwamoto, Y., Nakamura, M., Miyoshi, H., Okano, H.J., Contag, C.H., Toyama, Y. Okano, H. (2005) In vivo imaging of engrafted neural stem cells: its application in evaluating the optimal timing of transplantation for spinal cord injury. FASEB J., 19, 1839 1841.
59. Okano, H. (2002) Stem cell biology of the central nervous system. J. Neurosci. Res., 69, 698 707.
60. Pearse, D.D. Bunge, M.B. (2006) Designing cell- and gene-based regeneration strategies to repair the injured spinal cord. J. Neurotrauma, 23, 438 452.
61. Pfeifer, K., Vroemen, M., Blesch, A. Weidner, N. (2004) Adult neural progenitor cells provide a permissive guiding substrate for corticospinal axon growth following spinal cord injury. Eur. J. Neurosci., 20, 1695 1704.
62. Phinney, D.G. Isakova, I. (2005) Plasticity and therapeutic potential of mesenchymal stem cells in the nervous system. Curr. Pharm. Des., 11, 1255 1265.
63. Pitsikas, N., Brambilla, A., Besozzi, C., Bonali, P., Fodritto, F., Grippa, N., Scandroglio, A. Borsini, F. (2001) Effects of cerestat and NBQX on functional and morphological outcomes in rat focal cerebral ischemia. Pharmacol. Biochem. Behav., 68, 443 447.
64. Rabchevsky, A.G. Smith, G.M. (2001) Therapeutic interventions following mammalian spinal cord injury. Arch. Neurol., 58, 721 726.
65. Raineteau, O. Schwab, M.E. (2001) Plasticity of motor systems after incomplete spinal cord injury. Nat. Rev. Neurosci., 2, 263 273.
66. Rao, M.S. (1999) Multipotent and restricted precursors in the central nervous system. Anat. Rec., 257, 137 148.
67. Rouiller, E.M., Liang, F.Y., Moret, V. Wiesendanger, M. (1991) Trajectory of redirected corticospinal axons after unilateral lesion of the sensorimotor cortex in neonatal rat; a phaseolus vulgaris-leucoagglutinin (PHA-L) tracing study. Exp. Neurol., 114, 53 65.
68. Sadowsky, C., Volshteyn, O., Schultz, L. McDonald, J.W. (2002) Spinal cord injury. Disabil. Rehabil., 24, 680 687.
69. Schmidt, B.J. Jordan, L.M. (2000) The role of serotonin in reflex modulation and locomotor rhythm production in the mammalian spinal cord. Brain Res. Bull., 53, 689 710.
70. Schwab, M.E. (2002) Repairing the injured spinal cord. Science, 295, 1029 1031.
71. Schwab, M.E. (2004) Nogo and axon regeneration. Curr. Opin. Neurobiol., 14, 118 124.
72. Silver, J. Miller, J.H. (2004) Regeneration beyond the glial scar. Nat. Rev. Neurosci., 5, 146 156.
73. Soares, S., Barnat, M., Salim, C., von Boxberg, Y., Ravaille-Veron, M. Nothias, F. (2007) Extensive structural remodeling of the injured spinal cord revealed by phosphorylated MAP1B in sprouting axons and degenerating neurons. Eur. J. Neurosci., 26, 1446 1461.
74. Spitkovsky, D. Hescheler, J. (2008) Adult mesenchymal stromal stem cells for therapeutic applications. Minim. Invasive Ther. Allied Technol., 17, 79 90.
75. Takamatsu, H., Tatsumi, M., Nitta, S., Ichise, R., Muramatsu, K., Iida, M., Nishimura, S. Umemura, K. (2002) Time courses of progress to the chronic stage of middle cerebral artery occlusion models in rats. Exp. Brain Res., 146, 95 102.
76. Terada, N., Hamazaki, T., Oka, M., Hoki, M., Mastalerz, D.M., Nakano, Y., Meyer, E.M., Morel, L., Petersen, B.E. Scott, E.W. (2002) Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nature, 416, 542 545.
77. Terada, N., Ohno, N., Murata, S., Katoh, R., Stallcup, W.B. Ohno, S. (2006) Immunohistochemical study of NG2 chondroitin sulfate proteoglycan expression in the small and large intestines. Histochem. Cell Biol., 126, 483 490.
78. Tettoni, L., Gheorghita-Baechler, F., Bressoud, R., Welker, E. Innocenti, G.M. (1998) Constant and variable aspects of axonal phenotype in cerebral cortex. Cereb. Cortex, 8, 543 552.
79. Thuret, S., Moon, L.D.F. Gage, F.H. (2006) Therapeutic interventions after spinal cord injury. Nat. Rev. Neurosci., 7, 628 643.
80. Vercelli, A., Mereuta, O.M., Garbossa, D., Muraca, G., Mareschi, K., Rustichelli, D., Ferrero, I., Mazzini, L., Madon, E. Fagioli, F. (2008) Human mesenchymal stem cell transplantation extends survival, improves motor performance and decreases neuroinflammation in mouse model of amyotrophic lateral sclerosis. Neurobiol. Dis., 31, 395 405.
81. Weydt, P., Hongso, Y., Kliot, M. Moller, T. (2003) Assessing disease onset and progression in the SOD1 mouse model of ALS. Neuroreport, 14, 1051 1054.
82. Wiedenmann, B. Franke, W.W. (1985) Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles. Cell, 41, 1017 1028.
83. Wu, S., Suzuki, Y., Ejiri, Y., Noda, T., Bai, H., Kitada, M., Kataoka, K., Ohta, M., Chou, H. Ide, C. (2003) Bone marrow stromal cells enhance differentiation of cocultured neurosphere cells and promote regeneration of injured spinal cord. J. Neurosci. Res., 72, 343 351.
84. Wurmser, A.E. Gage, F.H. (2002) Stem cells: cell fusion causes confusion. Nature, 416, 485 487.
85. Wyatt, T.A., Lincoln, T.M. Pryzwansky, K.B. (1991) Vimentin is transiently co-localized with and phosphorylated by cyclic GMP-dependent protein kinase in formyl-peptide-stimulated neutrophils. J. Biol. Chem., 266, 21274 21280.
86. Zhang, L., Schallert, T., Zhang, Z.G., Jiang, Q., Arniego, P., Li, Q., Lu, M. Chopp, M. (2002) A test for detecting long-term sensorimotor dysfunction in the mouse after focal cerebral ischemia. J. Neurosci. Methods, 117, 207 214.