Embryonic neurons transplanted into the tibial nerve reinnervate muscle and reduce atrophy but NCAM expression persists

Neurological Research

Volumn 30, Issue 2, 2008, Pages 183-189

  Grumbles, Robert M ^a   Almeida, Vania W ^a   Thomas, Christine K ^a  

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

Author keywords

Denervated muscle; Functional reinnervation; Motoneuron transplantation; Neural cell adhesion molecule

Indexed keywords

GLYCOGEN; NERVE CELL ADHESION MOLECULE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; CELL TRANSPLANTATION; CONFERENCE PAPER; CONTROLLED STUDY; FEMALE; FISCHER 344 RAT; GASTROCNEMIUS MUSCLE; MUSCLE ATROPHY; MUSCLE DENERVATION; MUSCLE REINNERVATION; NERVE CELL; NONHUMAN; PROTEIN EXPRESSION; RAT; TIBIAL NERVE;

ANALYSIS OF VARIANCE; ANIMALS; CELL TRANSPLANTATION; ELECTROMYOGRAPHY; EMBRYO, MAMMALIAN; FEMALE; GLYCOGEN; MUSCLE DENERVATION; MUSCLE FIBERS; MUSCULAR ATROPHY; NERVE REGENERATION; NEURAL CELL ADHESION MOLECULES; NEURONS; RATS; RATS, INBRED F344; SPINAL CORD; TIBIAL NERVE;

EID: 44449169338     PISSN: 01616412     EISSN: None     Source Type: Journal    
DOI: 10.1179/174313208X281073     Document Type: Conference Paper

References (49)

1. Bowden REM, Gutman E. Denervation and reinnervation of human voluntary muscles. Brain 1944; 67: 273-313
2. Gutmann E, Young JZ. The re-innervation of muscle after various periods of atrophy. J Anat 1944; 78: 15-43
3. Sunderland S. Nerve and Nerve Injuries, Baltimore, MD: The Williams & Wilkins Company, 1968
4. Finkelstein DI, Dooley PC, Luff AR. Recovery of muscle after different periods of denervation and treatments. Muscle Nerve 1993; 16: 769-777
5. Fu SY, Gordon T. Contributing factors to poor functional recovery after delayed nerve repair: prolonged denervation. J Neurosci 1995; 15: 3886-3895
6. Dantes M, McComas A. The extent and time course of motoneuron involvement in amyotrophic lateral sclerosis. Muscle Nerve 1991; 14: 416-421
7. Collazos-Castro JE, Soto VM, Gutierrez-Davila M, et al. Motoneuron loss associated with chronic locomotion impairments after spinal cord contusion in the rat. J Neurotrauma 2005; 22: 544-558
8. Thomas CK, Zaidner EY, Calancie B, et al. Muscle weakness, paralysis, and atrophy after human cervical spinal cord injury. Exp Neurol 1997; 148: 414-423
9. Thomas CK. Contractile properties of human thenar muscles paralyzed by spinal cord injury. Muscle Nerve 1997; 20: 788-799
10. Belegu V, Oudega M, Gary DS, et al. Restoring function after spinal cord injury: Promoting spontaneous regeneration with stem cells and activity-based therapies. Neurosurg Clin N Am 2007; 18: 143-168
11. Myckatyn TM, Mackinnon SE, McDonald JW. Stem cell transplantation and other novel techniques for promoting recovery from spinal cord injury. Transpl Immunol 2004; 12: 343-358
12. Enzmann GU, Benton RL, Talbott JF, et al. Functional considerations of stem cell transplantation therapy for spinal cord repair. J Neurotrauma 2006; 23: 479-495
13. Thomas CK, Grumbles RM. Muscle atropy after human spinal cord injury. Biocybernet Biomed Eng 2005; 25: 39-45
14. Kern H, Salmons S, Mayr W, et al. Recovery of long-term denervated human muscles induced by electrical stimulation. Muscle Nerve 2005; 31: 98-101
15. Gutmann E and Zelena J. Morphological changes in the denervated muscle. In: Gutmann E, ed. The Denervated Muscle, Prague: Publishing House of the Czechoslovak Academy of Sciences, 1962: pp. 57-102
16. Lu DX, Huang SK, Carlson BM. Electron microscopic study of long-term denervated rat skeletal muscle. Anat Rec 1997; 248: 355-365
17. Borisov AB, Dedkov EI, Carlson BM. Interrelations of myogenic response, progressive atrophy of muscle fibers, and cell death in denervated skeletal muscle. Anat Rec 2001; 264: 203-218
18. Siu PM, Alway SE. Mitochondria-associated apoptotic signalling in denervated rat skeletal muscle. J Physiol 2005; 565: 309-323
19. Schmalbruch H, Al-Amood WS, Lewis DM. Morphology of long-term denervated rat soleus muscle and the effect of chronic electrical stimulation. J Physiol 1991; 441: 233-241
20. Kernell D. The Motoneurone and its Muscle Fibres (Monographs of the Physiological Society), New York: Oxford University Press Inc., 2006
21. Erb DE, Mora RJ, Bunge RP. Reinnervation of adult rat gastrocnemius muscle by embryonic motoneurons transplanted into the axotomized tibial nerve. Exp Neurol 1993; 124: 372-376
22. Thomas CK, Erb DE, Grumbles RM, et al. Embryonic cord transplants in peripheral nerve restore skeletal muscle function. J Neurophysiol 2000; 84: 591-595
23. Thomas CK, Sesodia S, Erb DE, et al. Properties of medial gastrocnemius motor units and muscle fibers reinnervated by embryonic ventral spinal cord cells. Exp Neurol 2003; 180: 25-31
24. Edström L, Kugelberg E. Histochemical composition, distribution of fibres and fatiguability of single motor units. Anterior tibial muscle of the rat. J Neurol Neurosurg Psychiatry 1968; 31: 424-433
25. Sanes JR, Schachner M, Covault J. Expression of several adhesive macromolecules (N-CAM, L1, J1, NILE, uvomorulin, laminin, fibronectin, and a heparan sulfate proteoglycan) in embryonic, adult, and denervated adult skeletal muscle. J Cell Biol 1986; 102: 420-431
26. Cashman NR, Covault J, Wollman RL, et al. Neural cell adhesion molecule in normal, denervated, and myopathic human muscle. Ann Neurol 1987; 21: 481-489
27. Covault J, Sanes JR. Neural cell adhesion molecule (N-CAM) accumulates in denervated and paralyzed skeletal muscles. Proc Natl Acad Sci USA 1985; 82: 4544-4548
28. Grumbles RM, Wood P, Rudinsky M, et al. Muscle reinnervation with delayed or immediate transplant of embryonic ventral spinal cord cells into adult rat peripheral nerve. Cell Transplant 2002; 11: 241-250
29. Burke RE, Levine DN, Tsairis P, et al. Physiological types and histochemical profiles in motor units of the cat gastrocnemius. J Physiol 1973; 234: 723-748
30. Tötösy de Zepetnek JE, Zung HV, Erdebil S, et al. Motor-unit categorization based on contractile and histochemical properties: A glycogen depletion analysis of normal and reinnervated rat tibialis anterior muscle. J Neurophysiol 1992; 67: 1404-1415
31. Pearse AGE. Histochemistry - Theoretical and Applied, Boston, MA: Little, Brown & Company, 1961
32. Kugelberg E, Edström L, Abbruzzese M. Mapping of motor units in experimentally reinnervated rat muscle. Interpretation of histochemical and atrophic fibre patterns in neurogenic lesions. J Neurol Neurosurg Psychiatry 1970; 33: 319-329
33. Thomas CK, Stein RB, Gordon T, et al. Patterns of reinnervation and motor unit recruitment in human hand muscles after complete ulnar and median nerve section and resuture. J Neurol Neurosurg Psychiatry 1987; 50: 259-268
34. Pierotti DJ, Roy RR, Bodine-Fowler SC, et al. Mechanical and morphological properties of chronically inactive cat tibialis anterior motor units. J Physiol 1991; 444: 175-192
35. Davis HL, Kiernan JA. Neurotrophic effects of sciatic nerve extract on denervated extensor digitorum longus muscle in the rat. Exp Neurol 1980; 69: 124-134
36. Al-Majed AA, Neumann CM, Brushart TM, et al. Brief electrical stimulation promotes the speed and accuracy of motor axonal regeneration. J Neurosci 2000; 20: 2602-2608
37. Hopkins WG, Brown MC, Keynes RJ. Nerve growth from nodes of Ranvier in inactive muscle. Brain Res 1981; 222: 125-128
38. Dennis MJ, Miledi R. Non-transmitting neuromuscular junctions during an early stage of end-plate reinnervation. J Physiol 1974; 239: 553-570
39. Krnjevic K, Miledi R. Presynaptic failure of neuromuscular propagation in rats. J Physiol 1959; 149: 1-22
40. Smith DO. Mechanisms of action potential propagation failure at sites of axon branching in the crayfish. J Physiol 1980; 301: 243-259
41. Hintz CS, Chi MM, Fell RD, et al. Metabolite changes in individual rat muscle fibers during stimulation. Am J Physiol 1982; 242: C218-C228
42. Moore SE, Walsh FS. Nerve dependent regulation of neural cell adhesion molecule expression in skeletal muscle. Neuroscience 1986; 18: 499-505
43. Jamali AA, Afshar P, Abrams RA, et al. Differential expression of neural cell adhesion molecule (NCAM) after tenotomy in rabbit skeletal muscle. J Orthop Res 2002; 20: 364-369
44. Andersson AM, Olsen M, Zhernosekov D, et al. Age-related changes in expression of the neural cell adhesion molecule in skeletal muscle: A comparative study of newborn, adult and aged rats. Biochem J 1993; 290: 641-648
45. Biral D, Adami N, Caccavale S, et al. Reinnervation events in long-term denervated rat muscles. Basic Appl Myol 2007; 17: 66-67
46. Tews DS, Goebel HH, Schneider I, et al. Expression profile of stress proteins, intermediate filaments, and adhesion molecules in experimentally denervated and reinnervated rat facial muscle. Exp Neurol 1997; 146: 125-134
47. Gosztonyi G, Naschold U, Grozdanovic Z, et al. Expression of Leu-19 (CD56, N-CAM) and nitric oxide synthase (NOS) I in denervated and reinnervated human skeletal muscle. Microsc Res Tech 2001; 55: 187-197
48. Kern H, Hofer C, Modlin M, et al. Denervated muscles in humans: Limitations and problems of currently used functional electrical stimulation training protocols. Artif Organs 2002; 26: 216-218
49. Mortimer JT. Motor prostheses. In: Brookhart JM, Brooks VB, Geiger SR, Mountcastle VB, eds. Handbook of Physiology: A Critical, Comprehensive Presentation of Physiological Knowledge and Concepts, Bethesda, MD: American Physiological Society, 1981: pp. 155-187