Acute stimulation of transplanted neurons improves motoneuron survival, axon growth, and muscle reinnervation

Journal of Neurotrauma

Volumn 30, Issue 12, 2013, Pages 1062-1069

  Grumbles, Robert M ^a   Liu, Yang ^a   Thomas, Christie M ^a   Wood, Patrick M ^a   Thomas, Christine K ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

axon regeneration; electrical stimulation; motoneuron transplantation; muscle denervation

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL SURVIVAL; CELL TRANSPLANTATION; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; DENERVATION; ELECTROSTIMULATION; FEMALE; GASTROCNEMIUS MUSCLE; MUSCLE INJURY; MUSCLE REINNERVATION; NERVE CELL STIMULATION; NERVE FIBER GROWTH; NONHUMAN; RAT; SCIATIC NERVE; TIBIAL NERVE;

ANIMALS; AXONS; AXOTOMY; CELL SURVIVAL; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; FEMALE; MOTOR NEURONS; MUSCLE, SKELETAL; NERVE REGENERATION; NEURODEGENERATIVE DISEASES; RATS; RATS, INBRED F344; SCIATIC NERVE; SPINAL CORD INJURIES;

EID: 84879328024     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2012.2797     Document Type: Article

References (87)

1. Bradley, W.G., Good, P., Rasool, C.G., and Adelman, L.S. (1983). Morphometric and biochemical studies of peripheral nerves in amyotrophic lateral sclerosis. Ann. Neurol. 14, 267-277. (Pubitemid 13051229)
2. Kim, W.K., Liu, X., Sandner, J., Pasmantier, M., Andrews, J., Rowland, L.P., and Mitsumoto, H. (2009). Study of 962 patients indicates progressive muscular atrophy is a form of ALS. Neurology 73, 1686-1692.
3. Thomas, C.K., and Zijdewind, I. (2006). Fatigue of muscles weakened by death of motoneurons. Muscle Nerve 33, 21-41. (Pubitemid 43062984)
4. Tovar Y Romo, L.B., Santa-Cruz, L.D., and Tapia, R. (2009). Experimental models for the study of neurodegeneration in amyotrophic lateral sclerosis. Mol. Neurodegener. 20, 31.
5. van Damme, P., and Robberecht, W. (2009). Recent advances in motor neuron disease. Curr. Opin. Neurol. 22, 486-492.
6. Kühnlein, P., Gdynia, H.J., Sperfeld, A.D., Lindner-Pfleghar, B., Ludolph, A.C., Prosiegel, M., and Riecker, A. (2008). Diagnosis and treatment of bulbar symptoms in amyotrophic lateral sclerosis. Nat. Clin. Pract. Neurol. 4, 366-374. (Pubitemid 352003288)
7. Rowland, L.P., and Shneider, N.A. (2001). Amyotrophic lateral sclerosis. N. Engl. J Med. 344, 1688-1700. (Pubitemid 32479968)
8. Bunge, R.P., Puckett, W.R., and Hiester, E.D. (1997). Observations on the pathology of several types of human spinal cord injury, with emphasis on the astrocyte response to penetrating injuries. Adv. Neurol. 72, 305-315.
9. Carlstedt, T. (2008). Root repair review: basic science background and clinical outcome. Restorative Neurol. Neurosci. 26, 225-241.
10. Collazos-Castro, J.E., Soto, V.M., Gutierrez-Davila, M., and Nieto-Sampedro, M. (2005). Motoneuron loss associated with chronic locomotion impairments after spinal cord contusion in the rat. J. Neurotrauma 22, 544-558. (Pubitemid 40726982)
11. Dietz, V., and Curt, A. (2006). Neurological aspects of spinal-cord repair: promises and challenges. Lancet Neurol. 5, 688-694. (Pubitemid 44062418)
12. Grumbles, R.M., Brunschwig, J.P., and Thomas, C.K. (1999). Motoneuron death after human spinal cord injury. J. Neurotrauma 16, 997.
13. Milhorat, T.H., Capocelli, A.L., Jr., Anzil, A.P., Kotzen, R.M., and Milhorat, R.H. (1995). Pathological basis of spinal cord cavitation in syringomyelia: analysis of 105 autopsy cases. J. Neurosurg. 82, 802-812.
14. Thomas, C.K. (1997). Contractile properties of human thenar muscles paralyzed by spinal cord injury. Muscle Nerve 20, 788-799. (Pubitemid 27250664)
15. Blesch, A., and Tuszynski, M.H. (2009). Spinal cord injury: plasticity, regeneration and the challenge of translational drug development. Trends Neurosci. 32, 41-47.
16. Gowing, G., and Svendsen, C.N. (2011). Stem cell transplantation for motor neuron disease: current approaches and future perspectives. Neurotherapeutics 8, 591-606.
17. Lindvall, O., Barker, R.A., Brustle, O., Isacson, O., and Svendsen, C.N. (2012). Clinical translation of stem cells in neurodegenerative disorders. Cell Stem Cell 10, 151-155.
18. Lu, P., Wang, Y., Graham, L., McHale, K., Gao, M., Wu, D., Brock, J., Blesch, A., Rosenzweig, E.S., Havton, L.A., Zheng, B., Conner, J.M., Marsala, M., and Tuszynski, M.H. (2012). Long-distance growth and connectivity of neural stem cells after severe spinal cord injury. Cell 150, 1264-1273.
19. Allan, C.H. (2000). Functional results of primary nerve repair. Hand Clin. 16, 67-72. (Pubitemid 30117164)
20. Hoke, A., and Brushart, T. (2010). Introduction to special issue: challenges and opportunities for regeneration in the peripheral nervous system. Exp. Neurol. 223, 1-4.
21. Terzis, J.K., Vekris, M.D., and Soucacos, P.N. (1999). Outcomes of brachial plexus reconstruction in 204 patients with devastating paralysis. Plast. Reconstr. Surg. 104, 1221-1240. (Pubitemid 29466265)
22. Young, J.Z. (1942). The functional repair of nervous tissue. Physiol. Rev. 22, 318-374.
23. Roytta, M., and Salonen, V. (1988). Long-term endoneurial changes after nerve transection. Acta Neuropathol. 76, 35-45.
24. Li, H., Terenghi, G., and Hall, S.M. (1997). Effects of delayed reinnervation on the expression of c-erbB receptors by chronically denervated rat Schwann cells in vivo. Glia 20, 333-347. (Pubitemid 27335751)
25. Richardson, P.M. (2009). Peripheral nerve regeneration: an overview, in: Encyclopedia Neuroscience. L.R.Squire (ed). Academic Press: New York, pps. 557-560.
26. Weinberg, H.J., and Spencer, P.S. (1978). The fate of Schwann cells isolated from axonal contact. J Neurocytol. 7, 555-569. (Pubitemid 9040730)
27. Gutmann, E. and Zelena, J. (1962). Morphological changes in the denervated muscle, in: The Denervated Muscle. E. Gutmann (ed). Publishing House of the Czechoslovak Academy of Sciences: Prague, pps. 57-102.
28. Lu, D.X., Huang, S.K., and Carlson, B.M. (1997). Electron microscopic study of long-term denervated rat skeletal muscle. Anat. Rec. 248, 355-365. (Pubitemid 27280142)
29. Schmalbruch, H., Al Amood, W.S., and Lewis, D.M. (1991). Morphology of long-term denervated rat soleus muscle and the effect of chronic electrical stimulation. J. Physiol. 441, 233-241.
30. Kern, H., Boncompagni, S., Rossini, K., Mayr, W., Fano, G., Zanin, M.E., Podhorska-Okolow, M., Protasi, F., and Carraro, U. (2004). Long-term denervation in humans causes degeneration of both contractile and excitation-contraction coupling apparatus, which is reversible by functional electrical stimulation (FES): a role for myofiber regeneration? J Neuropathol. Exp. Neurol. 63, 919-931. (Pubitemid 39202495)
31. Mortimer, J.T. (1981). Motor prostheses, in: Handbook of Physiology-A critical, comprehensive presentation of physiological knowledge and concepts. J.M. Brookhart, V.B. Brooks, S.R. Geiger, and V.B. Mountcastle (eds). American Physiological Society: Bethesda, MD, pps. 155-187.
32. Erb, D.E., Mora, R.J., and Bunge, R.P. (1993). Reinnervation of adult rat gastrocnemius muscle by embryonic motoneurons transplanted into the axotomized tibial nerve. Exp. Neurol. 124, 372-376. (Pubitemid 24041785)
33. Thomas, C.K., Erb, D.E., Grumbles, R.M., and Bunge, R.P. (2000). Embryonic cord transplants in peripheral nerve restore skeletal muscle function. J. Neurophysiol. 84, 591-595. (Pubitemid 30490078)
34. Thomas, C.K., Sesodia, S., Erb, D.E., and Grumbles, R.M. (2003). Properties of medial gastrocnemius motor units and muscle fibers reinnervated by embryonic ventral spinal cord cells. Exp. Neurol. 180, 25-31. (Pubitemid 36379004)
35. Brundin, P., Karlsson, J., Emgard, M., Schierle, G.S., Hansson, O., Petersen, A., and Castilho, R.F. (2000). Improving the survival of grafted dopaminergic neurons: a review over current approaches. Cell Transplant. 9, 179-195. (Pubitemid 30252685)
36. Grumbles, R.M., Casella, G.T.B., Rudinsky, M.J., Godfrey, S., Wood, P.M., and Thomas, C.K. (2005). The immunophilin ligand FK506, but not the P38 kinase inhibitor SB203580, improves function of adult rat muscle reinnervated from transplants of embryonic neurons. Neuroscience 130, 619-630. (Pubitemid 39601435)
37. Hu, Z., Ulfendahl, M., and Olivius, N.P. (2004). Central migration of neuronal tissue and embryonic stem cells following transplantation along the adult auditory nerve. Brain Res. 1026, 68-73. (Pubitemid 39336417)
38. Kakinohana, O., Cizkova, D., Tomori, Z., Hedlund, E., Marsala, S., Isacson, O., and Marsala, M. (2004). Region-specific cell grafting into cervical and lumbar spinal cord in rat: a qualitative and quantitative stereological study. Exp. Neurol. 190, 122-132. (Pubitemid 39335712)
39. Lowry, N., Goderie, S.K., Adamo, M., Lederman, P., Charniga, C., Gill, J., Silver, J., and Temple, S. (2008). Multipotent embryonic spinal cord stem cells expanded by endothelial factors and Shh/RA promote functional recovery after spinal cord injury. Exp. Neurol. 209, 510-522. (Pubitemid 351174140)
40. Webber, D.J., Bradbury, E.J., McMahon, S.B., and Minger, S.L. (2007). Transplanted neural progenitor cells survive and differentiate but achieve limited functional recovery in the lesioned adult rat spinal cord. Regen. Med. 2, 929-945.
41. Casella, G.T.B., Almeida, V.W., Grumbles, R.M., Yang, L., and Thomas, C.K. (2010). Neurotrophic factors improve muscle reinnervation from embryonic neurons. Muscle Nerve 42, 788-797.
42. Grumbles, R.M., Sesodia, S., Wood, P.M., and Thomas, C.K. (2009). Neurotrophic factors improve motoneuron survival and function of muscle reinnervated by embryonic neurons. J. Neuropathol. Exp. Neurol. 68, 736-746.
43. Goldberg, J.L., Espinosa, J.S., Xu, Y., Davidson, N., Kovacs, G.T., and Barres, B.A. (2002). Retinal ganglion cells do not extend axons by default: promotion by neurotrophic signaling and electrical activity. Neuron 33, 689-702. (Pubitemid 34219241)
44. Brunet, N., Tarabal, O., Portero-Otin, M., Oppenheim, R.W., Esquerda, J.E., and Caldero, J. (2007). Survival and death of mature avian motoneurons in organotypic slice culture: trophic requirements for survival and different types of degeneration. J. Comp. Neurol. 501, 669-690.
45. Hegarty, J.L., Kay, A.R., and Green, S.H. (1997). Trophic support of cultured spiral ganglion neurons by depolarization exceeds and is additive with that by neurotrophins or cAMP and requires elevation of [Ca2 +[i within a set range. J Neurosci. 17, 1959-1970. (Pubitemid 27106755)
46. Koike, T., Martin, D.P., and Johnson, E.M., Jr. (1989). Role of Ca2 + channels in the ability of membrane depolarization to prevent neuronal death induced by trophic-factor deprivation: evidence that levels of internal Ca2 + determine nerve growth factor dependence of sympathetic ganglion cells. Proc. Natl. Acad. Sci. U. S. A. 86, 6421-6425. (Pubitemid 19210663)
47. Mao, Z., Bonni, A., Xia, F., Nadal-Vicens, M., and Greenberg, M.E. (1999). Neuronal activity-dependent cell survival mediated by transcription factor MEF2. Science 286, 785-790.
48. Perez-Garcia, M.J., Cena, V., de Pablo, Y., Llovera, M., Comella, J.X., and Soler, R.M. (2004). Glial cell line-derived neurotrophic factor increases intracellular calcium concentration. Role of calcium/calmodulin in the activation of the phosphatidylinositol 3-kinase pathway. J Biol. Chem. 279, 6132-6142. (Pubitemid 38220646)
49. Garyantes, T.K., and Regehr, W.G. (1992). Electrical activity increases growth cone calcium but fails to inhibit neurite outgrowth from rat sympathetic neurons. J Neurosci. 12, 96-103.
50. Johnson, E.M., Jr., Koike, T., and Franklin, J. (1992). A "calcium setpoint hypothesis" of neuronal dependence on neurotrophic factor. Exp. Neurol. 115, 163-166.
51. Kater, S.B., and Mills, L.R. (1991). Regulation of growth cone behavior by calcium. J Neurosci. 11, 891-899.
52. Ming, G., Henley, J., Tessier-Lavigne, M., Song, H., and Poo, M. (2001). Electrical activity modulates growth cone guidance by diffusible factors. Neuron 29, 441-452. (Pubitemid 32206482)
53. Furber, S., Oppenheim, R.W., and Prevette, D. (1987). Naturallyoccurring neuron death in the ciliary ganglion of the chick embryo following removal of preganglionic input: evidence for the role of afferents in ganglion cell survival. J Neurosci. 7, 1816-1832. (Pubitemid 17119804)
54. Okado, N., and Oppenheim, R.W. (1984). Cell death of motoneurons in the chick embryo spinal cord. IX. The loss of motoneurons following removal of afferent inputs. J. Neurosci. 4, 1639-1652. (Pubitemid 14058680)
55. Pineda, R.H., Svoboda, K.R., Wright, M.A., Taylor, A.D., Novak, A.E., Gamse, J.T., Eisen, J.S., and Ribera, A.B. (2006). Knockdown of Nav1.6a Na + channels affects zebrafish motoneuron development. Development 133, 3827-3836. (Pubitemid 44650961)
56. Flavell, S.W., and Greenberg, M.E. (2008). Signaling mechanisms linking neuronal activity to gene expression and plasticity of the nervous system. Annu. Rev. Neurosci. 31, 563-590.
57. Spitzer, N.C. (2006). Electrical activity in early neuronal development. Nature 444, 707-712. (Pubitemid 44949593)
58. Al-Majed, A.A., Neumann, C.M., Brushart, T.M., and Gordon, T. (2000). Brief electrical stimulation promotes the speed and accuracy of motor axonal regeneration. J. Neurosci. 20, 2602-2608. (Pubitemid 30220347)
59. Grumbles, R.M., Wood, P., Rudinsky, M., Gomez, A.M., and Thomas, C.K. (2002). Muscle reinnervation with delayed or immediate transplant of embryonic ventral spinal cord cells into adult rat peripheral nerve. Cell Transplant. 11, 241-250. (Pubitemid 34665824)
60. Emgard, M., Blomgren, K., and Brundin, P. (2002). Characterisation of cell damage and death in embryonic mesencephalic tissue: a study on ultrastructure, vital stains and protease activity. Neuroscience 115, 1177-1187. (Pubitemid 35351707)
61. Mullen, R.J., Buck, C.R., and Smith, A.M. (1992). NeuN, a neuronal specific nuclear protein in vertebrates. Development 116, 201-211.
62. Basgen, J.M., Nicholas, S.B., Mauer, M., Rozen, S., and Nyengaard, J.R. (2006). Comparison of methods for counting cells in the mouse glomerulus. Nephron Exp. Nephrol. 103, e139-e148. (Pubitemid 44114507)
63. Grumbles, R.M., Almeida, V.W., and Thomas, C.K. (2008). Embryonic neurons transplanted into the tibial nerve reinnervate muscle and reduce atrophy but NCAM expression persists. Neurol. Res. 30, 183-189. (Pubitemid 351768839)
64. Deshmukh, M., and Johnson, E.M., Jr. (1998). Evidence of a novel event during neuronal death: development of competence-to-die in response to cytoplasmic cytochrome c. Neuron 21, 695-705. (Pubitemid 28498779)
65. Festjens, N., Vanden, B.T., and Vandenabeele, P. (2006). Necrosis, a well-orchestrated form of cell demise: signalling cascades, important mediators and concomitant immune response. Biochim. Biophys. Acta. 1757, 1371-1387. (Pubitemid 44472550)
66. Perez-Garcia, M.J., Gou-Fabregas, M., de Pablo, Y., Llovera, M., Comella, J.X., and Soler, R.M. (2008). Neuroprotection by neurotrophic factors and membrane depolarization is regulated by calmodulin kinase IV. J. Biol. Chem. 283, 4133-4144.
67. Wiegert, J.S., and Bading, H. (2011). Activity-dependent calcium signaling and ERK-MAP kinases in neurons: a link to structural plasticity of the nucleus and gene transcription regulation. Cell Calcium 49, 296-305.
68. Fields, R.D., Eshete, F., Stevens, B., and Itoh, K. (1997). Action potential-dependent regulation of gene expression: temporal specificity in Ca, cAMP-responsive element binding proteins, and mitogen-Activated protein kinase signaling. J. Neurosci. 17, 7252-7266. (Pubitemid 27413257)
69. Emgard, M., Hallin, U., Karlsson, J., Bahr, B.A., Brundin, P., and Blomgren, K. (2003). Both apoptosis and necrosis occur early after intracerebral grafting of ventral mesencephalic tissue: a role for protease activation. J. Neurochem. 86, 1223-1232. (Pubitemid 37022198)
70. Coleman, M. (2005). Axon degeneration mechanisms: commonality amid diversity. Nat. Rev. Neurosci. 6, 889-898. (Pubitemid 41568730)
71. Schlaepfer, W.W., and Bunge, R.P. (1973). Effects of calcium ion concentration on the degeneration of amputated axons in tissue culture. J. Cell Biol. 59, 456-470.
72. Xie, X.Y., and Barrett, J.N. (1991). Membrane resealing in cultured rat septal neurons after neurite transection: evidence for enhancement by Ca(2 + )-triggered protease activity and cytoskeletal disassembly. J. Neurosci. 11, 3257-3267.
73. Gitler, D., and Spira, M.E. (1998). Real time imaging of calciuminduced localized proteolytic activity after axotomy and its relation to growth cone formation. Neuron 20, 1123-1135. (Pubitemid 28293130)
74. Kamber, D., Erez, H., and Spira, M.E. (2009). Local calcium-dependent mechanisms determine whether a cut axonal end assembles a retarded endbulb or competent growth cone. Exp. Neurol. 219, 112-125.
75. Spira, M.E., Oren, R., Dormann, A., and Gitler, D. (2003). Critical calpain-dependent ultrastructural alterations underlie the transformation of an axonal segment into a growth cone after axotomy of cultured Aplysia neurons. J. Comp. Neurol. 457, 293-312. (Pubitemid 36158286)
76. Reimer, M.M., Kuscha, V., Wyatt, C., Sorensen, I., Frank, R.E., Knuwer, M., Becker, T., and Becker, C.G. (2009). Sonic hedgehog is a polarized signal for motor neuron regeneration in adult zebrafish. J. Neurosci. 29, 15,073-15,082.
77. Cosker, K.E., Courchesne, S.L., and Segal, R.A. (2008). Action in the axon: generation and transport of signaling endosomes. Curr. Opin. Neurobiol. 18, 270-275.
78. Hamburger, V. (1980). Trophic interactions in neurogenesis: a personal historical account. Annu. Rev. Neurosci. 3, 269-278.
79. Li, X.M., Dong, X.P., Luo, S.W., Zhang, B., Lee, D.H., Ting, A.K., Neiswender, H., Kim, C.H., Carpenter-Hyland, E., Gao, T.M., Xiong, W.C., and Mei, L. (2008). Retrograde regulation of motoneuron differentiation by muscle beta-catenin. Nat. Neurosci. 11, 262-268. (Pubitemid 351311800)
80. Pazyra-Murphy, M.F., Hans, A., Courchesne, S.L., Karch, C., Cosker, K.E., Heerssen, H.M., Watson, F.L., Kim, T., Greenberg, M.E., and Segal, R.A. (2009). A retrograde neuronal survival response: targetderived neurotrophins regulate MEF2D and bcl-w. J Neurosci. 29, 6700-6709.
81. Pratt, K.G., and Aizenman, C.D. (2007). Homeostatic regulation of intrinsic excitability and synaptic transmission in a developing visual circuit. J. Neurosci. 27, 8268-8277. (Pubitemid 47219613)
82. Puls, I., Jonnakuty, C., LaMonte, B.H., Holzbaur, E.L., Tokito, M., Mann, E., Floeter, M.K., Bidus, K., Drayna, D., Oh, S.J., Brown, R.H., Jr., Ludlow, C.L., and Fischbeck, K.H. (2003). Mutant dynactin in motor neuron disease. Nat. Genet. 33, 455-456. (Pubitemid 36390002)
83. Bernstein, M., and Lichtman, J.W. (1999). Axonal atrophy: the retraction reaction. Curr. Opin. Neurobiol. 9, 364-370. (Pubitemid 29267609)
84. Shimada, Y., and Fischman, D.A. (1973). Morphological and physiological evidence for the development of functional neuromuscular junctions in vitro. Dev. Biol. 31, 200-225.
85. Yumoto, N., Kim, N., and Burden, S.J. (2012). Lrp4 is a retrograde signal for presynaptic differentiation at neuromuscular synapses. Nature 489, 438-442.
86. Grumbles, R.M., Almeida, V.W., Casella, G.T.B., Wood, P.M., Hemstapat, K., and Thomas, C.K. (2012). Motoneuron replacement for reinnervation of skeletal muscle in adult rats. J Neuropathol. Exp. Neurol. 71, 921-930.
87. Mauritz, K.H., and Peckham, H.P. (1987). Restoration of grasping functions in quadriplegic patients by Functional Electrical Stimulation (FES). Int. J. Rehabil. Res. 10, 57-61.