A double-transgenic mouse used to track migrating Schwann cells and regenerating axons following engraftment of injured nerves

Experimental Neurology

Volumn 207, Issue 1, 2007, Pages 128-138

  Hayashi, Ayato ^a   Koob, Jason W ^a   Liu, Daniel Z ^a   Tong, Alice Y ^a   Hunter, Daniel A ^a   Parsadanian, Alexander ^a   Mackinnon, Susan E ^a   Myckatyn, Terence M ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cold preservation; Live imaging; Nerve allograft; Nerve regeneration; Schwann cell migration; Transgenic mouse

Indexed keywords

GREEN FLUORESCENT PROTEIN;

ALLOGRAFT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; IMAGING SYSTEM; MOUSE; NERVE FIBER REGENERATION; NERVE INJURY; NONHUMAN; PRIORITY JOURNAL; SCHWANN CELL;

ANIMALS; AXONS; CELL MOVEMENT; CELL-FREE SYSTEM; FLUORESCENT DYES; GREEN FLUORESCENT PROTEINS; LUMINESCENT AGENTS; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; NERVE REGENERATION; NEUROMUSCULAR JUNCTION; SCHWANN CELLS; SCIATIC NERVE; TIME FACTORS; TRANSPLANTATION, HOMOLOGOUS;

EID: 34548281577     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2007.06.004     Document Type: Article

References (48)

1. Ahmed Z., Underwood S., and Brown R.A. Nerve guide material made from fibronectin: assessment of in vitro properties. Tissue Eng. 9 2 (2003 Apr) 219-231
2. Best T.J., Mackinnon S.E., Evans P.J., Hunter D., and Midha R. Peripheral nerve revascularization: histomorphometric study of small- and large-caliber grafts. J. Reconstr. Microsurg. 15 (1999) 183-190
3. Best T.J., Mackinnon S.E., Midha R., Hunter D.A., and Evans P.J. Revascularization of peripheral nerve autografts and allografts. Plast. Reconstr. Surg. 104 (1999) 152-160
4. Breidenbach W.C., and Terzis J.K. The blood supply of vascularized nerve grafts. J. Reconstr. Microsurg. 3 (1986) 43-58
5. Brenner M.J., Tung T.H., Mackinnon S.E., Myckatyn T.M., Hunter D.A., and Mohanakumar T. Anti-CD40 ligand monoclonal antibody induces a permissive state, but not tolerance, for murine peripheral nerve allografts. Exp. Neurol. 186 (2004) 59-69
6. Chiu D.T., and Strauch B. A prospective clinical evaluation of autogenous vein grafts used as a nerve conduit for distal sensory nerve defects of 3 cm or less. Plast. Reconstr. Surg. 86 (1990) 928-934
7. Dailey A.T., Avellino A.M., Benthem L., Silver J., and Kliot M. Complement depletion reduces macrophage infiltration and activation during Wallerian degeneration and axonal regeneration. J. Neurosci. 18 (1998) 6713-6722
8. Dedkov E.I., Kostrominova T.Y., Borisov A.B., and Carlson B.M. Survival of Schwann cells in chronically denervated skeletal muscles. Acta Neuropathol. (Berl.) 103 (2002) 565-574
9. Dong Z., Brennan A., Liu N., Yarden Y., Lefkowitz G., Mirsky R., and Jessen K.R. Neu differentiation factor is a neuron-glia signal and regulates survival, proliferation, and maturation of rat Schwann cell precursors. Neuron 15 (1995) 585-596
10. Feng G., Mellor R.H., Bernstein M., Keller-Peck C., Nguyen Q.T., Wallace M., Nerbonne J.M., Lichtman J.W., and Sanes J.R. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28 (2000) 41-51
11. Fornaro M., Tos P., Geuna S., Giacobini-Robecchi M.G., and Battiston B. Confocal imaging of Schwann-cell migration along muscle-vein combined grafts used to bridge nerve defects in the rat. Microsurgery 21 (2001) 153-155
12. Fox I.K., Jaramillo A., Hunter D.A., Rickman S.R., Mohanakumar T., and Mackinnon S.E. Prolonged cold-preservation of nerve allografts. Muscle Nerve 31 (2005) 59-69
13. Garratt A.N., Britsch S., and Birchmeier C. Neuregulin, a factor with many functions in the life of a Schwann cell. BioEssays 22 (2000) 987-996
14. Gundersen H.J. The nucleator. J. Microsc. 151 (1988) 3-21
15. Hadlock T., Elisseeff J., Langer R., Vacanti J., and Cheney M. A tissue-engineered conduit for peripheral nerve repair. Arch. Otolaryngol. Head Neck Surg. 124 (1998) 1081-1086
16. Hayworth C.R., Moody S.E., Chodosh L.A., Krieg P., Rimer M., and Thompson W.J. Induction of neuregulin signaling in mouse Schwann cells in vivo mimics responses to denervation. J. Neurosci. 26 (2006) 6873-6884
17. Hobson M.I. Increased vascularisation enhances axonal regeneration within an acellular nerve conduit. Ann. R Coll. Surg. Engl. 84 (2002) 47-53
18. Jessen K.R., and Mirsky R. The origin and development of glial cells in peripheral nerves. Nat. Rev., Neurosci. 6 (2005) 671-682
19. Kang H., Tian L., and Thompson W. Terminal Schwann cells guide the reinnervation of muscle after nerve injury. J. Neurocytol. 32 (2003) 975-985
20. Lundborg G. Intraneural microcirculation. Orthop. Clin. North Am. 19 (1988) 1-12
21. Lyons D.A., Pogoda H.M., Voas M.G., Woods I.G., Diamond B., Nix R., Arana N., Jacobs J., and Talbot W.S. erbb3 and erbb2 are essential for Schwann cell migration and myelination in zebrafish. Curr. Biol. 15 (2005) 513-524
22. Michailov G.V., Sereda M.W., Brinkmann B.G., Fischer T.M., Haug B., Birchmeier C., Role L., Lai C., Schwab M.H., and Nave K.A. Axonal neuregulin-1 regulates myelin sheath thickness. Science 304 (2004) 700-703
23. Mirsky R., Jessen K.R., Brennan A., Parkinson D., Dong Z., Meier C., Parmantier E., and Lawson D. Schwann cells as regulators of nerve development. J. Physiol. (Paris) 96 (2002) 17-24
24. Mosahebi A., Wiberg M., and Terenghi G. Addition of fibronectin to alginate matrix improves peripheral nerve regeneration in tissue-engineered conduits. Tissue Eng. 9 2 (2003 (Apr)) 209-218
25. Myckatyn T.M., and MacKinnon S.E. A review of research endeavors to optimize peripheral nerve reconstruction. Neurol. Res. 26 (2004) 124-138
26. Myckatyn T.M., Mackinnon S.E., Hunter D.A., Brakefield D., and Parsadanian A. A novel model for the study of peripheral-nerve regeneration following common nerve injury paradigms. J. Reconstr. Microsurg. 20 (2004) 533-544
27. Nguyen Q.T., Sanes J.R., and Lichtman J.W. Pre-existing pathways promote precise projection patterns. Nat. Neurosci. 5 (2002) 861-867
28. Nichols C.M., Brenner M.J., Fox I.K., Tung T.H., Hunter D.A., Rickman S.R., and Mackinnon S.E. Effects of motor versus sensory nerve grafts on peripheral nerve regeneration. Exp. Neurol. 190 (2004) 347-355
29. Ozcan G., Shenaq S., and Spira M. Study of microcirculation of rat femoral nerve and development of a new vascularized nerve graft model. J. Reconstr. Microsurg. 7 (1991) 133-138
30. Pan Y.A., Misgeld T., Lichtman J.W., and Sanes J.R. Effects of neurotoxic and neuroprotective agents on peripheral nerve regeneration assayed by time-lapse imaging in vivo. J. Neurosci. 23 (2003) 11479-11488
31. Perry V.H., Brown M.C., and Gordon S. The macrophage response to central and peripheral nerve injury. A possible role for macrophages in regeneration. J. Exp. Med. 165 (1987) 1218-1223
32. Redett R., Jari R., Crawford T., Chen Y.G., Rohde C., and Brushart T.M. Peripheral pathways regulate motoneuron collateral dynamics. J. Neurosci. 25 (2005) 9406-9412
33. Reichert F., Saada A., and Rotshenker S. Peripheral nerve injury induces Schwann cells to express two macrophage phenotypes: phagocytosis and the galactose-specific lectin MAC-2. J. Neurosci. 14 (1994) 3231-3245
34. Seckel B.R., Ryan S.E., Simons J.E., Gagne R.G., and Watkins Jr. E. Vascularized versus nonvascularized nerve grafts: an experimental structural comparison. Plast. Reconstr. Surg. 78 (1986) 211-220
35. Snider W.D., Zhou F.Q., Zhong J., and Markus A. Signaling the pathway to regeneration. Neuron 35 (2002) 13-16
36. Sulaiman O.A., and Gordon T. Transforming growth factor-beta and forskolin attenuate the adverse effects of long-term Schwann cell denervation on peripheral nerve regeneration in vivo. Glia 37 (2002) 206-218
37. Sulaiman O.A., Midha R., Munro C.A., Matsuyama T., Al-Majed A., and Gordon T. Chronic Schwann cell denervation and the presence of a sensory nerve reduce motor axonal regeneration. Exp. Neurol. 176 (2002) 342-354
38. Taveggia C., Zanazzi G., Petrylak A., Yano H., Rosenbluth J., Einheber S., Xu X., Esper R.M., Loeb J.A., Shrager P., Chao M.V., Falls D.L., Role L., and Salzer J.L. Neuregulin-1 type III determines the ensheathment fate of axons. Neuron 47 (2005) 681-694
39. Terzis J.K., Skoulis T.G., and Soucacos P.N. Vascularized nerve grafts. A review. Int. Angiol. 14 (1995) 264-277
40. Tseng C.Y., Hu G., Ambron R.T., and Chiu D.T. Histologic analysis of Schwann cell migration and peripheral nerve regeneration in the autogenous venous nerve conduit (AVNC). J. Reconstr. Microsurg. 19 (2003) 331-340
41. Ulkur E., Yuksel F., Acikel C., Okar I., and Celikoz B. Comparison of functional results of nerve graft, vein graft, and vein filled with muscle graft in end-to-side neurorrhaphy. Microsurgery 23 (2003) 40-48
42. Varejao A.S., Cabrita A.M., Geuna S., Patricio J.A., Azevedo H.R., Ferreira A.J., and Meek M.F. Functional assessment of sciatic nerve recovery: biodegradable poly (DLLA-epsilon-CL) nerve guide filled with fresh skeletal muscle. Microsurgery 23 (2003) 346-353
43. Walsh M.K., and Lichtman J.W. In vivo time-lapse imaging of synaptic takeover associated with naturally occurring synapse elimination. Neuron 37 (2003) 67-73
44. Weber R.V., and Mackinnon S.E. Bridging the neural gap. Clin. Plast. Surg. 32 (2005) 605-616 (viii)
45. Witzel C., Rohde C., and Brushart T.M. Pathway sampling by regenerating peripheral axons. J. Comp. Neurol. 485 (2005) 183-190
46. Yin Q., Kemp G.J., Yu L.G., Wagstaff S.C., and Frostick S.P. Expression of Schwann cell-specific proteins and low-molecular-weight neurofilament protein during regeneration of sciatic nerve treated with neurotrophin-4. Neuroscience 105 (2001) 779-783
47. Zhu J.Y., Huang Y.T., Zhu Q.S., and Lu R. Expression of adenovirus-mediated neurotrophin-3 gene in Schwann cells of sciatic nerve in rats. Chin. J. Traumatol. 6 (2003) 75-80
48. Zuo Y., Lubischer J.L., Kang H., Tian L., Mikesh M., Marks A., Scofield V.L., Maika S., Newman C., Krieg P., and Thompson W.J. Fluorescent proteins expressed in mouse transgenic lines mark subsets of glia, neurons, macrophages, and dendritic cells for vital examination. J. Neurosci. 24 (2004) 10999-11009