Exogenous adult postmortem neural precursors attenuate secondary degeneration and promote myelin sparing and functional recovery following experimental spinal sord injury

Cell Transplantation

Volumn 24, Issue 4, 2015, Pages 703-719

  Carelli, Stephana ^a   Giallongo, Toniella ^a   Marfia, Giovanni ^a   Merli, Davide ^a   Ottobrini, Luisa ^d   Degrassi, Anna ^c   Basso, Michele D ^b   Di Giulio, Anna Maria ^a   Gorio, Alfredo ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^c BU Oncology   (Italy)

^d UNIVERSITY OF MILAN   (Italy)

Author keywords

Animal behavior; Inflammation; Neural stem cells; Regenerative medicine; Spinal cord injury (SCI); Transplantation

Indexed keywords

BETA TUBULIN; MICROTUBULE ASSOCIATED PROTEIN 2; MYELIN; ERYTHROPOIETIN; ERYTHROPOIETIN RECEPTOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CADAVER; CELL HOMING; CELL INVASION; CELL SURVIVAL; DEGENERATION; EXPERIMENTAL SPINAL CORD INJURY; INFLAMMATORY CELL; MALE; MOUSE; NEURAL STEM CELL TRANSPLANTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; REGENERATIVE MEDICINE; ALLOTRANSPLANTATION; ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; CELL CULTURE; CELL MOTION; CONVALESCENCE; CYTOLOGY; FLUORESCENCE IMAGING; HINDLIMB; METABOLISM; MYELIN SHEATH; NEURAL STEM CELL; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PHYSIOLOGY; RADIOGRAPHY; SPINAL CORD INJURIES; TRANSGENIC MOUSE; TRANSPLANTATION;

ANIMALIA;

ANIMALS; BEHAVIOR, ANIMAL; CELL MOVEMENT; CELLS, CULTURED; ERYTHROPOIETIN; HINDLIMB; MAGNETIC RESONANCE IMAGING; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYELIN SHEATH; NEURAL STEM CELLS; OPTICAL IMAGING; RECEPTORS, ERYTHROPOIETIN; RECOVERY OF FUNCTION; SPINAL CORD INJURIES; TRANSPLANTATION, HOMOLOGOUS;

EID: 84927593167     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368914X685140     Document Type: Article

References (43)

1. Abematsu, M.; Smith, I.; Nakashima, K. Mechanisms of neural stem cell fate determination: Extracellular cues and intracellular programs. Curr. Stem Cell Res. Ther. 1:267- 277; 2006.
2. Ballermann, M.; Fouad, K. Spontaneous locomotor recovery in spinal cord injured rats is accompanied by anatomical plasticity of reticulospinal fibers. Eur. J. Neurosci. 23:1988-1996; 2006.
3. Basso, D. M.; Fisher, L. C.; Anderson, A. J.; Jakeman, L. B.; Mctigue, D. M.; Popovich, P. G. Basso Mouse Scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. J. Neurotrauma 23:635-659; 2006.
4. Bottai, D.; Cigognini, D.; Madaschi, L.; Adami, R.; Nicora, E.; Menarini, M.; Di Giulio, A. M.; Gorio, A. Embryonic stem cells promote motor recovery and affect inflammatory cell infiltration in spinal cord injured mice. Exp. Neurol. 223:452-463; 2010.
5. Bottai, D.; Madaschi, L.; Di Giulio, A. M.; Gorio, A. Viability-dependent promoting action of adult neural precursors in spinal cord injury. Mol.Med. 14:634-644; 2008.
6. Cao, Q. L.; Howard, R. M; Dennison, J. B.; Whittemore, S. R. Differentiation of engrafted neuronal-restricted precursor cells is inhibited in the traumatically injured spinal cord. Exp. Neurol. 177:349-359; 2002.
7. Cho, G. W.; Koh, S. H.; Kim, M. H.; Yoo, A. R.; Noh, M. Y.; Oh, S.; Kim, S. H. The neuroprotective effect of erythropoietin-transduced human mesenchymal stromal cells in an animal model of ischemic stroke. Brain Res. 1353:1-13; 2010.
8. Coggeshall, R. E. A consideration of neural counting methods. Trends Neurosci. 15:9-13; 1992.
9. Cummings, B. J.; Uchida, N.; Tamaki, S. J.; Salazar, D. L.; Hooshmand, M.; Summers R.; Gage, F. H.; Anderson, A. J. Human neural stem cells differentiate and promote locomotor recovery in spinal cord-injured mice. Proc. Natl. Acad. Sci. USA 102:14069-14074; 2005.
10. Fehlings, M. G.; Cadotte, D. W.; Fehlings, L. N. A series of systematic reviews on the treatment of acute spinal cord injury: A foundation for best medical practice. J. Neurotrauma 28:1329-1333; 2011.
11. Furlan, J. C.; Noonan V.; Cadotte, D. W.; Fehlings, M. G.; Timing of decompressive surgery of spinal cord after traumatic spinal cord injury: An evidence-based examination of pre-clinical and clinical studies. J. Neurotrauma 28:1371- 1399; 2011.
12. Gorio, A.; Gokmen, N.; Erbayraktar, S.; Yilmaz, O.; Madaschi, L.; Cichetti, C.; Di Giulio, A. M.; Vardar, E.; Cerami, A.; Brines, M. Recombinant human erythropoietin counteracts secondary injury and markedly enhances neurological recovery from experimental spinal cord trauma. Proc. Natl. Acad. Sci. USA 99:9450-9455; 2002.
13. Gorio, A.; Madaschi, L.; Di Stefano, B.; Carelli, S.; Di Giulio, A. M.; De Biasi, S.; Coleman, T.; Cerami, A.; Brines, M. Methylprednisolone neutralizes the beneficial effects of erythropoietin in experimental spinal cord injury. Proc. Natl. Acad. Sci USA 102:16379-16784; 2005.
14. Gorio, A.; Madaschi, L.; Zadra, G.; Marfia, G.; Cavalieri, B.; Bertini, R.; Di Giulio, A. M. Reparixin, an inhibitor of CXCR2 function, attenuates inflammatory responses and promotes recovery of function after traumatic lesion to the spinal cord. J. Pharmacol. Exp. Ther. 322:973-981; 2007.
15. Gorio, A.; Torrente, Y.; Madaschi, L.; Di Stefano, A. B.; Pisati, F.; Marchesi, C.; Belicchi, M.; Di Giulio, A. M.; Bresolin, N. Fate of autologous dermal stem cells transplanted into the spinal cord after traumatic injury (TSCI). Neuroscience 125:179-189; 2004.
16. Gris, D.; Marsh, D.R.; Oatway, M.A.; Chen, Y.; Hamilton, E.F; Dekaban, G.A.; Weaver L.C. Transient blockade of the CD11d/CD18 integrin reduces secondary damage after spinal cord injury, improving sensory, autonomic, and motor function. J. Neurosci. 24:4043-4051; 2004.
17. Gritti, A.; Bonfanti, L.; Doetsch, F.; Caille, I.; Alvarez Buylla, A.; Lim, D. A.; Galli, R.; Verdugo, J. M.; Herrera, D. G.; Vescovi, A. L. Multipotent neural stem cells reside into the rostral extension and olfactory bulb of adult rodents. J. Neurosci. 22:437-445; 2002.
18. Hansen, C. N.; Fisher, L. C.; Deibert, R. J.; Jakeman L. B.; Zhang, H.; Noble-Haeusslein, L.; White, S.; Basso, D. M. Elevated MMP-9 in the lumbar cord early after thoracic spinal cord injury impedes motor relearning in mice. J. Neurosci. 33:13101-13111; 2013.
19. 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. Allodynia limits the usefulness of intraspinal neural stem cell grafts: Directed differentiation improves outcome. Nat. Neurosci. 8:346- 353; 2005.
20. Horan, P. K.; Melnicoff, M. J.; Jensen, B. D.; Slezak, S. E. Fluorescent cell labeling for in vivo and in vitro cell tracking. Methods Cell Biol. 33:469-490; 1990.
21. Horn, K. P.; Busch, S. A.; Hawthorne, A. L.; van Rooijen, N.; Silver, J. Another barrier to regeneration in the CNS: Activated macrophages induce extensive retraction of dystrophic axons through direct physical interactions. J. Neurosci. 28:9330-9341; 2008.
22. Li, Y.; Chopp, M. Marrow stromal cell transplantation in stroke and traumatic brain injury. Neurosci. Lett. 456:120- 123; 2009.
23. Marfia, G.; Madaschi, L.; Marra, F.; Menarini, M.; Bottai, D.; Formenti, A.; Bellardita, C.; Di Giulio, A. M.; Carelli, S.; Gorio, A. Adult neural precursors isolated from post mortem brain yield mostly neurons: An erythropoietindependent process. Neurobiol. Dis. 43:86-98; 2011.
24. Martino, G.; Pluchino, S. The therapeutic potential of neural stem cells. Nat. Rev. Neurosci. 7:395-406; 2006.
25. Mori, S.; Matsui, T.; Kuze, B.; Asanome, M.; Nakajima, K.; Matsuyama, K. Cerebellar-induced locomotion: Reticulospinal control of spinal rhythm generating mechanism in cats. Ann. N. Y. Acad. Sci. 860:94-105; 1998.
26. Ponce, L. L.; Navarro, J. C.; Ahmed, O.; Robertson, C. S. Erythropoietin neuroprotection with traumatic brain injury. Pathophysiology 20:31-38; 2013.
27. Popovich, P. G.; Guan, Z.; Wei, P.; Huitinga, I.; van Rooijen, N.; Stokes, B. T. Depletion of hematogenous macrophages promotes partial hindlimb recovery and neuroanatomical repair after experimental spinal cord injury. Exp. Neurol. 158:351-365; 1999.
28. Popovich, P. G.; Wei, P.; Stokes, B. T. Cellular inflammatory response after spinal cord injury in Sprague-Dawley and Lewis rats. J. Comp. Neurol. 377:443-464; 1997.
29. Romanko, M. J.; Zhu, C.; Bahr, B. A.; Blomgren, K.; Levison, S. W. Death effector activation in the subventricular zone subsequent to perinatal hypoxia/ischemia. J. Neurochem. 103:1121-1131; 2007.
30. Sahni, V.; Kessler, J. A. Stem cell therapies for spinal cord injury. Nat. Rev. Neurol. 6:363-372; 2010.
31. Scheff, S. W.; Rabchevsky, A. G.; Fugaccia, I.; Main, J. A.; Lumpp, Jr., J. E. Experimental modeling of spinal cord injury: Characterization of a force defined injury device. J. Neurotrauma 20:179-193; 2003.
32. Schlayer, H. J.; Laaff, H.; Peters, T.; Woort-Menker, M.; Estler, H. C.; Karck, U.; Schaefer, H. E.; Decker, K. Involvement of tumor necrosis factor in endotoxin-triggered neutrophil adherence to sinusoidal endothelial cells of mouse liver and its modulation in acute phase. J. Hepatol. 7:239- 249; 1988.
33. Sekhon, L. H.; Fehlings, M. G. Epidemiology, demographics, and pathophysiology of acute spinal cord injury. Spine 26:S2-S12; 2001.
34. Setoguchi, T.; Nakashima, K.; Takizawa, T.; Yanagisawa, M.; Ochiai, W.; Okabe, M.; Yone K.; Komiya, S.; Taga, T. Treatment of spinal cord injury by transplantation of fetal neural precursor cells engineered to express BMP inhibitor. Exp. Neurol. 189:33-44; 2004.
35. Taoka, Y.; Okajima, K. Spinal cord injury in the rat. Prog. Neurobiol. 56:341-358; 1998.
36. Taoka, Y.; Okajima, K.; Uchiba, M.; Murakami, K.; Kushimoto, S.; Johno, M.; Naruo, M.; Okabe, H.; Takatsuki, K. Role of neutrophils in spinal cord injury in the rat. Neuroscience 79:1177-1182; 1997.
37. Thuret, S.; Moon, L. D.; Gage, F. H. Therapeutic interventions after spinal cord injury. Nat. Rev. Neurosci. 7:628- 643; 2006.
38. Vitellaro-Zuccarello, L.; Mazzetti, S.; Bosisio, P.; Monti, C.; De Biasi, S. Distribution of Aquaporin 4 in rodent spinal cord: Relationship with astrocyte markers and chondroitin sulfate proteoglycans. Glia 51:148-159; 2005.
39. Vitellaro-Zuccarello, L.; Mazzetti, S.; Madaschi, L.; Bosisio, P.; Fontana, E.; Gorio, A.; De Biasi, S. Chronic erythropoietin-mediated effects on the expression of astrocyte markers in a rat model of contusive spinal cord injury. Neuroscience 151:452-466; 2008.
40. Vitellaro-Zuccarello, L.; Mazzetti, S.; Madaschi, L.; Bosisio, P.; Gorio, A.; De Biasi S. Erythropoietin-mediated preservation of the white matter in rat spinal cord injury. Neuroscience 144:865-877; 2007.
41. Wallace, P. K.; Tario, Jr., J. D.; Fisher, J. L.; Wallace, S. S.; Ernstoff, M. S.; Muirhead, K. A. Tracking antigen-driven responses by flow cytometry: Monitoring proliferation by dye dilution. Cytometry 73A:1019-1034; 2008.
42. Whetstone, W. D.; Hsu, J. Y.; Eisenberg, M.; Werb, Z.; Noble-Haeusslein, L. J. Blood-spinal cord barrier after spinal cord injury: Relation to revascularization and wound healing. J. Neurosci. Res. 74:227-239; 2003.
43. Windle, W. F.; Clemente, C. D.; Chambers, W. W. Inhibition of formation of a glial barrier as a means of permitting a peripheral nerve to grow into the brain. J. Comp. Neurol. 96:359-369; 1952.