Peripheral nerve transplantation combined with acidic fibroblast growth factor and chondroitinase induces regeneration and improves urinary function in complete spinal cord transected adult mice

PLoS ONE

Volumn 10, Issue 10, 2015, Pages

  DePaul, Marc A ^a   Lin, Ching Yi ^b   Silver, Jerry ^a   Lee, Yu Shang ^b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; FIBROBLAST GROWTH FACTOR 1; N ACETYLGALACTOSAMINE 4 SULFATASE; SEROTONIN; TYROSINE 3 MONOOXYGENASE; CHONDROITIN ABC LYASE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLADDER SPHINCTER; BLADDER WEIGHT; CONTROLLED STUDY; CYSTOMETRY; ELECTROMYOGRAPHY; FEMALE; HISTOPATHOLOGY; MICTURITION; MOUSE; NERVE FIBER; NERVE REGENERATION; NERVE TRANSPLANTATION; NONHUMAN; ORGAN WEIGHT; SPINAL CORD REGENERATION; SPINAL CORD TRANSSECTION; URINARY DYSFUNCTION; URINARY TRACT FUNCTION; URODYNAMICS; ANIMAL; BLADDER; C57BL MOUSE; CONVALESCENCE; DISEASE MODEL; DRUG EFFECTS; HUMAN; INNERVATION; METABOLISM; PATHOPHYSIOLOGY; PERIPHERAL NERVE; PHYSIOLOGY; RAT; SPINAL CORD INJURIES; TRANSPLANTATION;

ANIMALS; CHONDROITIN ABC LYASE; DISEASE MODELS, ANIMAL; ELECTROMYOGRAPHY; FEMALE; FIBROBLAST GROWTH FACTOR 1; HUMANS; MICE; MICE, INBRED C57BL; NERVE REGENERATION; PERIPHERAL NERVES; RATS; RECOVERY OF FUNCTION; SPINAL CORD INJURIES; TYROSINE 3-MONOOXYGENASE; URINARY BLADDER; URINATION; URODYNAMICS;

EID: 84947216249     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0139335     Document Type: Article

References (66)

1. Filbin MT. Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat Rev Neurosci. 2003; 4: 703-713. doi: 10.1038/nrn1195 PMID: 12951563
2. Cregg JM, DePaul MA, Filous AR, Lang BT, Tran A, Silver J. Functional regeneration beyond the glial scar. Exp Neurol. 2014; 253: 197-207. doi: 10.1016/j.expneurol.2013.12.024 PMID: 24424280
3. Park KK, Liu K, Hu Y, Smith PD, Wang C, Cai B, et al. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science. 2008; 322: 963-966. doi: 10.1126/science.1161566 PMID: 18988856
4. Smith PD, Sun F, Park KK, Cai B, Wang C, Kuwako K, et al. SOCS3 deletion promotes optic nerve regeneration in vivo. Neuron. Elsevier; 2009; 64: 617-623. doi: 10.1016/j.neuron.2009.11.021
5. Fitch MT, Doller C, Combs CK, Landreth GE, Silver J. Cellular and molecular mechanisms of glial scarring and progressive cavitation: in vivo and in vitro analysis of inflammation-induced secondary injury after CNS trauma. Journal of Neuroscience. 1999; 19: 8182-8198. PMID: 10493720
6. Tuszynski MH, Gabriel K, Gage FH, Suhr S, Meyer S, Rosetti A. Nerve growth factor delivery by gene transfer induces differential outgrowth of sensory, motor, and noradrenergic neurites after adult spinal cord injury. Exp Neurol. 1996; 137: 157-173. doi: 10.1006/exnr.1996.0016 PMID: 8566208
7. Bradbury EJ, Moon LDF, Popat RJ, King VR, Bennett GS, Patel PN, et al. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature. 2002; 416: 636-640. doi: 10.1038/416636a PMID: 11948352
8. Lee Y-S, Lin C-Y, Jiang H-H, DePaul MA, Lin VW, Silver J. Nerve regeneration restores supraspinal control of bladder function after complete spinal cord injury. Journal of Neuroscience. 2013; 33: 10591-10606. doi: 10.1523/JNEUROSCI.1116-12.2013 PMID: 23804083
9. Lu P, Yang H, Jones LL, Filbin MT, Tuszynski MH. Combinatorial therapy with neurotrophins and cAMP promotes axonal regeneration beyond sites of spinal cord injury. Journal of Neuroscience. 2004; 24: 6402-6409. doi: 10.1523/JNEUROSCI.1492-04.2004 PMID: 15254096
10. Fouad K, Schnell L, Bunge MB, Schwab ME, Liebscher T, Pearse DD. Combining Schwann cell bridges and olfactory-ensheathing glia grafts with chondroitinase promotes locomotor recovery after complete transection of the spinal cord. Journal of Neuroscience. 2005; 25: 1169-1178. doi: 10.1523/JNEUROSCI.3562-04.2005 PMID: 15689553
11. Farooque M, Isaksson J, Olsson Y. White matter preservation after spinal cord injury in ICAM-1/Pselectin-deficient mice. Acta Neuropathol. 2001; 102: 132-140.PMID: 11563627
12. Lee JK, Geoffroy CG, Chan AF, Tolentino KE, Crawford MJ, Leal MA, et al. Assessing spinal axon regeneration and sprouting in Nogo-, MAG-, and OMgp-deficient mice. Neuron. 2010; 66: 663-670. doi: 10.1016/j.neuron.2010.05.002 PMID: 20547125
13. Goldshmit Y, Galea MP, Wise G, Bartlett PF, Turnley AM. Axonal regeneration and lack of astrocytic gliosis in EphA4-deficient mice. Journal of Neuroscience. 2004; 24: 10064-10073. doi: 10.1523/JNEUROSCI.2981-04.2004 PMID: 15537875
14. Wrathall JR, Pettegrew RK, Harvey F. Spinal cord contusion in the rat: production of graded, reproducible, injury groups. Exp Neurol. 1985; 88: 108-122. doi: 10.1016/0014-4886(85)90117-7 PMID: 3979505
15. Ma M, Basso DM, Walters P, Stokes BT, Jakeman LB. Behavioral and histological outcomes following graded spinal cord contusion injury in the C57Bl/6 mouse. Exp Neurol. 2001; 169: 239-254. doi: 10.1006/exnr.2001.7679 PMID: 11358439
16. Sroga JM, Jones TB, Kigerl KA, McGaughy VM, Popovich PG. Rats and mice exhibit distinct inflammatory reactions after spinal cord injury. J Comp Neurol. 2003; 462: 223-240. doi: 10.1002/cne.10736 PMID: 12794745
17. Cheng CL, de Groat WC. The role of capsaicin-sensitive afferent fibers in the lower urinary tract dysfunction induced by chronic spinal cord injury in rats. Exp Neurol. 2004; 187: 445-454. doi: 10.1016/j. expneurol.2004.02.014 PMID: 15144870
18. Fowler CJ, Griffiths D, de Groat WC. The neural control of micturition. Nat Rev Neurosci. Nature Publishing Group; 2008; 9: 453-466. doi: 10.1038/nrn2401
19. Kakizaki H, de Groat WC. Reorganization of somato-urethral reflexes following spinal cord injury in the rat. J Urol. 1997; 158: 1562-1567. doi: 10.1016/S0022-5347(01)64280-0 PMID: 9302174
20. Kadekawa K, Yoshiyama M, Majima T, Wada N, Shimizu T, Tyagi P, et al. Characterization of bladder and external urethral sphincter activity in mice with or without spinal cord injury-A comparison study with rats. In: International Continence Society, Montreal, CA. 2015. Volume 241, Abstract 16979, p. 49.
21. Anderson KD. Targeting recovery: priorities of the spinal cord-injured population. J Neurotrauma. 2004; 21: 1371-1383. PMID: 15672628
22. Weld KJ, Dmochowski RR. Association of level of injury and bladder behavior in patients with post-traumatic spinal cord injury. Urology. 2000; 55: 490-494. doi: 10.1016/S0090-4295(99)00553-1 PMID: 10736489
23. Cheng H, Cao Y, Olson L. Spinal cord repair in adult paraplegic rats: partial restoration of hind limb function. Science. 1996; 273: 510-513. PMID: 8662542
24. Lee Y-S, Hsiao I, Lin VW. Peripheral nerve grafts and aFGF restore partial hindlimb function in adult paraplegic rats. J Neurotrauma. 2002; 19: 1203-1216. doi: 10.1089/08977150260338001 PMID: 12427329
25. Kuo H-S, Tsai M-J, Huang M-C, Chiu C-W, Tsai C-Y, Lee M-J, et al. Acid fibroblast growth factor and peripheral nerve grafts regulate Th2 cytokine expression, macrophage activation, polyamine synthesis, and neurotrophin expression in transected rat spinal cords. Journal of Neuroscience. 2011; 31: 4137-4147. doi: 10.1523/JNEUROSCI.2592-10.2011 PMID: 21411654
26. Chang H-Y, Cheng C-L, Chen J-JJ, de Groat WC. Serotonergic drugs and spinal cord transections indicate that different spinal circuits are involved in external urethral sphincter activity in rats. Am J Physiol Renal Physiol. 2007; 292: F1044-53. doi: 10.1152/ajprenal.00175.2006 PMID: 17047164
27. Sławińska U, Majczyński H, Djavadian R. Recovery of hindlimb motor functions after spinal cord transection is enhanced by grafts of the embryonic raphe nuclei. Exp Brain Res. 2000; 132: 27-38. PMID: 10836633
28. Lee Y-S, Lin C-Y, Caiozzo VJ, Robertson RT, Yu J, Lin VW. Repair of spinal cord transection and its effects on muscle mass and myosin heavy chain isoform phenotype. J Appl Physiol. 2007; 103: 1808-1814. doi: 10.1152/japplphysiol.00588.2007 PMID: 17717118
29. Cheng H, Olson L. A new surgical technique that allows proximodistal regeneration of 5-HT fibers after complete transection of the rat spinal cord. Exp Neurol. 1995; 136: 149-161. doi: 10.1006/exnr.1995. 1092 PMID: 7498405
30. Kuscha V, Barreiro-Iglesias A, Becker CG, Becker T. Plasticity of tyrosine hydroxylase and serotonergic systems in the regenerating spinal cord of adult zebrafish. J Comp Neurol. Wiley Subscription Services, Inc., A Wiley Company; 2012; 520: 933-951. doi: 10.1002/cne.22739
31. Sasaki S, Isa T, Pettersson L-G, Alstermark B, Naito K, Yoshimura K, et al. Dexterous finger movements in primate without monosynaptic corticomotoneuronal excitation. Journal of Neurophysiology. American Physiological Society; 2004; 92: 3142-3147. doi: 10.1152/jn.00342.2004
32. Cajal SY. Degeneration and Regeneration of the Nervous System. London: Press; 1928.
33. Kanno H, Pearse DD, Ozawa H, Itoi E, Bunge MB. Schwann cell transplantation for spinal cord injury repair: its significant therapeutic potential and prospectus. Rev Neurosci. 2015. doi: 10.1515/revneuro-2014-0068
34. Stamegna JC, Felix MS, Roux-Peyronnet J, Rossi V, Féron F, Gauthier P, et al. Nasal OEC transplantation promotes respiratory recovery in a subchronic rat model of cervical spinal cord contusion. Exp Neurol. 2011; 229: 120-131. doi: 10.1016/j.expneurol.2010.07.002 PMID: 20633558
35. Ramón-Cueto A, Plant GW, Avila J, Bunge MB. Long-distance axonal regeneration in the transected adult rat spinal cord is promoted by olfactory ensheathing glia transplants. J Neurosci. 1998; 18: 3803-3815. PMID: 9570810
36. Yoshihara T, Ohta M, Itokazu Y, Matsumoto N, Dezawa M, Suzuki Y, et al. Neuroprotective effect of bone marrow-derived mononuclear cells promoting functional recovery from spinal cord injury. J Neurotrauma. 2007; 24: 1026-1036. doi: 10.1089/neu.2007.132R PMID: 17600518
37. Filous AR, Miller JH, Coulson-Thomas YM, Horn KP, Alilain W, Silver J. Immature astrocytes promote CNS axonal regeneration when combined with chondroitinase ABC. Dev Neurobiol. Wiley Subscription Services, Inc., A Wiley Company; 2010; 70: 826-841. doi: 10.1002/dneu.20820
38. Chu T, Zhou H, Li F, Wang T, Lu L, Feng S. Astrocyte transplantation for spinal cord injury: current status and perspective. Brain Res Bull. 2014; 107: 18-30. doi: 10.1016/j.brainresbull.2014.05.003 PMID: 24878447
39. Busch SA, Hamilton JA, Horn KP, Cuascut FX, Cutrone R, Lehman N, et al. Multipotent adult progenitor cells prevent macrophage-mediated axonal dieback and promote regrowth after spinal cord injury. Journal of Neuroscience. 2011; 31: 944-953. doi: 10.1523/JNEUROSCI.3566-10.2011 PMID: 21248119
40. Lu P, Wang Y, Graham L, McHale K, Gao M, Wu D, et al. Long-distance growth and connectivity of neural stem cells after severe spinal cord injury. Cell. Elsevier; 2012; 150: 1264-1273. doi: 10.1016/j.cell. 2012.08.020
41. +) from spinal cord injury patients improve functional recovery and tissue sparing in an acute spinal cord injury rat model. Cell Transplant. Cognizant Communication Corporation; 2013; 22: 393-412. doi: 10.3727/096368912X656081
42. Antonic A, Sena ES, Lees JS, Wills TE, Skeers P, Batchelor PE, et al. Stem cell transplantation in traumatic spinal cord injury: a systematic review and meta-analysis of animal studies. Plos Biol. 2013; 11: e1001738. doi: 10.1371/journal.pbio.1001738 PMID: 24358022
43. David S, Aguayo AJ. Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats. Science. 1981; 214: 931-933. doi: 10.1126/science.6171034 PMID: 6171034
44. Munz M, Rasminsky M, Aguayo AJ, Vidal-Sanz M, Devor MG. Functional activity of rat brainstem neurons regenerating axons along peripheral nerve grafts. Brain Res. 1985; 340: 115-125. PMID: 4027637
45. Gauthier P, Réga P, Lammari-Barreault N, Polentes J. Functional reconnections established by central respiratory neurons regenerating axons into a nerve graft bridging the respiratory centers to the cervical spinal cord. J Neurosci Res. 2002; 70: 65-81. doi: 10.1002/jnr.10379 PMID: 12237865
46. Levi ADO, Dancausse H, Li X, Duncan S, Horkey L, Oliviera M. Peripheral nerve grafts promoting central nervous system regeneration after spinal cord injury in the primate. J Neurosurg. 2002; 96: 197-205. doi: 10.3171/spi.2002.96.2.0197 PMID: 12450283
47. Houle JD, Tom VJ, Mayes D, Wagoner G, Phillips N, Silver J. Combining an autologous peripheral nervous system "bridge" and matrix modification by chondroitinase allows robust, functional regeneration beyond a hemisection lesion of the adult rat spinal cord. Journal of Neuroscience. Society for Neuroscience; 2006; 26: 7405-7415. doi: 10.1523/JNEUROSCI.1166-06.2006
48. Cheng H, Liao K-K, Liao S-F, Chuang T-Y, Shih Y-H. Spinal cord repair with acidic fibroblast growth factor as a treatment for a patient with chronic paraplegia. Spine. 2004; 29: E284-8. PMID: 15247588
49. Tabakow P, Raisman G, Fortuna W, Czyz M, Huber J, Li D, et al. Functional regeneration of supraspinal connections in a patient with transected spinal cord following transplantation of bulbar olfactory ensheathing cells with peripheral nerve bridging. Cell Transplant. 2014; 23: 1631-1655. doi: 10.3727/096368914X685131 PMID: 25338642
50. Tsai EC, Krassioukov AV, Tator CH. Corticospinal Regeneration into Lumbar Grey Matter Correlates with Locomotor Recovery after Complete Spinal Cord Transection and Repair with Peripheral Nerve Grafts, Fibroblast Growth Factor 1, Fibrin Glue, and Spinal Fusion. J Neuropathol Exp Neurol. 2005; 64: 230. PMID: 15804055
51. Powers CJ, McLeskey SW, Wellstein A. Fibroblast growth factors, their receptors and signaling. Endocr Relat Cancer. 2000; 7: 165-197. PMID: 11021964
52. Spyrou GE, Naylor IL. The effect of basic fibroblast growth factor on scarring. Br J Plast Surg. 2002; 55: 275-282. PMID: 12160530
53. Eto H, Suga H, Aoi N, Kato H, Doi K, Kuno S, et al. Therapeutic potential of fibroblast growth factor-2 for hypertrophic scars: upregulation of MMP-1 and HGF expression. Lab Invest. 2012; 92: 214-223. doi: 10.1038/labinvest.2011.127 PMID: 21946856
54. Tan EM, Rouda S, Greenbaum SS, Moore JH, Fox JW, Sollberg S. Acidic and basic fibroblast growth factors down-regulate collagen gene expression in keloid fibroblasts. Am J Pathol. American Society for Investigative Pathology; 1993; 142: 463-470.
55. Lee Y-S, Baratta J, Yu J, Lin VW, Robertson RT. aFGF promotes axonal growth in rat spinal cord organotypic slice co-cultures. J Neurotrauma. 2002; 19: 357-367. doi: 10.1089/089771502753594927 PMID: 11939503
56. Guest JD, Hesse D, Schnell L, Schwab ME, Bunge MB, Bunge RP. Influence of IN-1 antibody and acidic FGF-fibrin glue on the response of injured corticospinal tract axons to human Schwann cell grafts. J Neurosci Res. 1997; 50: 888-905. PMID: 9418975
57. Kang W, Balordi F, Su N, Chen L, Fishell G, Hébert JM. Astrocyte activation is suppressed in both normal and injured brain by FGF signaling. Proc Natl Acad Sci USA. 2014; 111: E2987-95. doi: 10.1073/pnas.1320401111 PMID: 25002516
58. Goldshmit Y, Sztal TE, Jusuf PR, Hall TE, Nguyen-Chi M, Currie PD. Fgf-dependent glial cell bridges facilitate spinal cord regeneration in zebrafish. J Neurosci. Soc Neuroscience; 2012; 32: 7477-7492.
59. Deng L-X, Deng P, Ruan Y, Xu ZC, Liu N-K, Wen X, et al. A novel growth-promoting pathway formed by GDNF-overexpressing Schwann cells promotes propriospinal axonal regeneration, synapse formation, and partial recovery of function after spinal cord injury. Journal of Neuroscience. 2013; 33: 5655-5667. doi: 10.1523/JNEUROSCI.2973-12.2013 PMID: 23536080
60. Alilain W, Horn KP, Hu H, Dick TE, Silver J. Functional regeneration of respiratory pathways after spinal cord injury. Nature. 2011; 475: 196-200. doi: 10.1038/nature10199 PMID: 21753849
61. Starkey ML, Bartus K, Barritt AW, Bradbury EJ. Chondroitinase ABC promotes compensatory sprouting of the intact corticospinal tract and recovery of forelimb function following unilateral pyramidotomy in adult mice. Eur J Neurosci. 2012; 36: 3665-3678. doi: 10.1111/ejn.12017 PMID: 23061434
62. Grimpe B, Pressman Y, Lupa MD, Horn KP, Bunge MB, Silver J. The role of proteoglycans in Schwann cell/astrocyte interactions and in regeneration failure at PNS/CNS interfaces. Mol Cell Neurosci. 2005; 28: 18-29. doi: 10.1016/j.mcn.2004.06.010 PMID: 15607938
63. Milbreta U, Boxberg von Y, Mailly P, Nothias F, Soares S. Astrocytic and vascular remodeling in the injured adult rat spinal cord after chondroitinase ABC treatment. J Neurotrauma. 2014; 31: 803-818. doi: 10.1089/neu.2013.3143 PMID: 24380419
64. Massey JM, Hubscher CH, Wagoner MR, Decker JA, Amps J, Silver J, et al. Chondroitinase ABC digestion of the perineuronal net promotes functional collateral sprouting in the cuneate nucleus after cervical spinal cord injury. Journal of Neuroscience. 2006; 26: 4406-4414. doi: 10.1523/JNEUROSCI. 5467-05.2006 PMID: 16624960
65. Bartus K, James ND, Didangelos A, Bosch KD, Verhaagen J, Yáñez-Muñoz RJ, et al. Large-scale chondroitin sulfate proteoglycan digestion with chondroitinase gene therapy leads to reduced pathology and modulates macrophage phenotype following spinal cord contusion injury. Journal of Neuroscience. 2014; 34: 4822-4836. doi: 10.1523/JNEUROSCI.4369-13.2014 PMID: 24695702
66. Kigerl KA, Gensel JC, Ankeny DP, Alexander JK, Donnelly DJ, Popovich PG. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. Journal of Neuroscience. 2009; 29: 13435-13444. doi: 10.1523/JNEUROSCI.3257-09.2009 PMID: 19864556