GDNF preconditioning can overcome Schwann cell phenotypic memory

Experimental Neurology

Volumn 265, Issue , 2015, Pages 1-7

  Marquardt, Laura M ^a   Sakiyama Elbert, Shelly E ^a,b  

^a WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Growth factors; Microdevices; Muscle and cutaneous phenotype; Neurite extension; Peripheral nerve regeneration

Indexed keywords

GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; MESSENGER RNA;

ADULT; ANIMAL CELL; ARTICLE; CELL CULTURE EQUIPMENT; CELL FUNCTION; CELL INTERACTION; CONTROLLED STUDY; GDNF GENE; GENE EXPRESSION; MALE; MICROFLUIDICS; NERVE CELL CULTURE; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; SCHWANN CELL; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE; COCULTURE; DRUG EFFECTS; LEWIS RAT; PHYSIOLOGY; PROCEDURES; SPRAGUE DAWLEY RAT;

ANIMALS; CELLS, CULTURED; COCULTURE TECHNIQUES; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; MALE; PHENOTYPE; RATS; RATS, INBRED LEW; RATS, SPRAGUE-DAWLEY; SCHWANN CELLS;

EID: 84925259613     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2014.12.003     Document Type: Article

References (49)

1. Arthur-Farraj P., Makwana M., Wilton D., Latouche-Hartman M., Acosta A., Cuthill D., Bherens A., Mirsky R., Raivich G., Jessen K.R. In injured nerves, C-Jun in Schwann cells controls demyelination, neuronal survival, axonal re-growth and functional recovery. J. Peripher. Nerv. Syst. 2009, 14:9-10.
2. Arthur-Farraj P.J., Latouche M., Wilton D.K., Quintes S., Chabrol E., Banerjee A., Woodhoo A., Jenkins B., Rahman M., Turmaine M., Wicher G.K., Mitter R., Greensmith L., Behrens A., Raivich G., Mirsky R., Jessen K.R. c-Jun reprograms Schwann cells of injured nerves to generate a repair cell essential for regeneration. Neuron 2012, 75:633-647.
3. Banker G., Goslin K. Culturing nerve cells. Cellular and Molecular Neuroscience 1998, 2nd ed.
4. Brenner M.J., Hess J.R., Myckatyn T.M., Hayashi A., Hunter D.A., Mackinnon S.E. Repair of motor nerve gaps with sensory nerve inhibits regeneration in rats. Laryngoscope 2006, 116:1685-1692.
5. Brewer G.J., Torricelli J.R. Isolation and culture of adult neurons and neurospheres. Nat. Protoc. 2007, 2:1490-1498.
6. Brushart T.M.E. Preferential reinnervation of motor nerves by regenerating motor axons. J. Neurosci. 1988, 8:1026-1031.
7. Brushart T.M., Gerber J., Kessens P., Chen Y.G., Royall R.M. Contributions of pathway and neuron to preferential motor reinnervation. J. Neurosci. 1998, 18:8674-8681.
8. Brushart T.M., Aspalter M., Griffin J.W., Redett R., Hameed H., Zhou C., Wright M., Vyas A., Hoke A. Schwann cell phenotype is regulated by axon modality and central-peripheral location, and persists in vitro. Exp. Neurol. 2013, 247:272-281.
9. Eide L., McMurray C.T. Culture of adult mouse neurons. BioTech. 2005, 38:99-104.
10. Fox I.K., Schwetye K.E., Keune J.D., Brenner M.J., Yu J.W., Hunter D.A., Wood P.M., Mackinnon S.E. Schwann-cell injection of cold-preserved nerve allografts. Microsurgery 2005, 25:502-507.
11. Franz C.K., Rutishauser U., Rafuse V.F. Polysialylated neural cell adhesion molecule is necessary for selective targeting of regenerating motor neurons. J. Neurosci. 2005, 25:2081-2091.
12. Gingras M., Gagnon V., Minotti S., Durham H.D., Berthod F. Optimized protocols for isolation of primary motor neurons, astrocytes and microglia from embryonic mouse spinal cord. J. Neurosci. Methods 2007, 163:111-118.
13. Goldberg J.L. How does an axon grow?. Genes Dev. 2003, 17:941-958.
14. Graber D.J., Harris B.T. Purification and culture of spinal motor neurons from rat embryos. Cold Spring Harb. Protoc. 2013, 2013:319-326.
15. Guenard V., Kleitman N., Morrissey T.K., Bunge R.P., Aebischer P. Syngeneic Schwann-cells derived from adult nerves seeded in semipermeable guidance channels enhance peripheral-nerve regeneration. J. Neurosci. 1992, 12:3310-3320.
16. He Q.R., Man L.L., Ji Y.H., Ding F. Comparison in the biological characteristics between primary cultured sensory and motor Schwann cells. Neurosci. Lett. 2012, 521:57-61.
17. Hoke A., Griffin J.W. The effects of GDNF on Schwann cells and unmyelinated axons. Neurol. 1997, 48:5107.
18. Hoke A., Bell R., Zochodne D.W. GDNF and its receptors are upregulated in the denervated distal stump of injured sciatic nerves. Neurology 1998, 50:A28.
19. Hoke A., Cheng C., Zochodne D.W. Expression of glial cell line-derived neurotrophic factor family of growth factors in peripheral nerve injury in rats. Neuroreport 2000, 11:1651-1654.
20. Hoke A., Gordon T., Zochodne D.W., Sulaiman O.A.R. A decline in glial cell-line-derived neurotrophic factor expression is associated with impaired regeneration after long-term Schwann cell denervation. Exp. Neurol. 2002, 173:77-85.
21. Hoke A., Ho T., Crawford T.O., LeBel C., Hilt D., Griffin J.W. Glial cell line-derived neurotrophic factor alters axon Schwann cell units and promotes myelination in unmyelinated nerve fibers. J. Neurosci. 2003, 23:561-567.
22. Hoke A., Redett R., Hameed H., Jari R., Zhou C., Li Z.B., Griffin J.W., Brushart T.M. Schwann cells express motor and sensory phenotypes that regulate axon regeneration. J. Neurosci. 2006, 26:9646-9655.
23. Iwase T., Jung C.G., Bae H., Zhang M., Soliven B. Glial cell line-derived neurotrophic factor-induced signaling in Schwann cells. J. Neurochem. 2005, 94:1488-1499.
24. Jesuraj N.J., Nguyen P.K., Wood M.D., Moore A.M., Borschel G.H., Mackinnon S.E., Sakiyama-Elbert S.E. Differential gene expression in motor and sensory Schwann cells in the rat femoral nerve. J. Neurosci. Res. 2012, 90:96-104.
25. Jesuraj N.J., Marquardt L.M., Kwasa J.A., Sakiyama-Elbert S.E. Glial cell line-derived neurotrophic factor promotes increased phenotypic marker expression in femoral sensory and motor-derived Schwann cell cultures. Exp. Neurol. 2014, 257C:10-18.
26. Jesuraj N.J., Santosa K.B., Macewan M.R., Moore A.M., Kasukurthi R., Ray W.Z., Flagg E.R., Hunter D.A., Borschel G.H., Johnson P.J., Mackinnon S.E., Sakiyama-Elbert S.E. Schwann cells seeded in acellular nerve grafts improve functional recovery. Muscle Nerve 2014, 49:267-276.
27. Klemke R.L., Cai S., Giannini A.L., Gallagher P.J., deLanerolle P., Cheresh D.A. Regulation of cell motility by mitogen-activated protein kinase. J. Cell Biol. 1997, 137:481-492.
28. Leach M.K., Feng Z.Q., Gertz C.C., Tuck S.J., Regan T.M., Naim Y., Vincent A.M., Corey J.M. The culture of primary motor and sensory neurons in defined media on electrospun poly-l-lactide nanofiber scaffolds. Journal of visualized experiments: JoVE 2011, 48:2389.
29. Lin Y.C., Ramadan M., Hronik-Tupaj M., Kaplan D.L., Philips B.J., Sivak W., Rubin J.P., Marra K.G. Spatially controlled delivery of neurotrophic factors in silk fibroin-based nerve conduits for peripheral nerve repair. Ann. Plast. Surg. 2011, 67:147-155.
30. Lu X., Kim-Han J.S., O'Malley K.L., Sakiyama-Elbert S.E. A microdevice platform for visualizing mitochondrial transport in aligned dopaminergic axons. J. Neurosci. Methods 2012, 209:35-39.
31. Madison R.D., Archibald S.J., Brushart T.M. Reinnervation accuracy of the rat femoral nerve by motor and sensory neurons. J. Neurosci. 1996, 16:5698-5703.
32. Magill C.K., Moore A.M., Yan Y., Tong A.Y., Macewan M.R., Yee A., Hayashi A., Hunter D.A., Ray W.Z., Johnson P.J., Parsadanian A., Myckatyn T.M., Mackinnon S.E. The differential effects of pathway- versus target-derived glial cell line-derived neurotrophic factor on peripheral nerve regeneration. J. Neurosurgery 2010, 113:102.
33. Martini R., Xin Y., Schmitz B., Schachner M. The L2/Hnk-1 carbohydrate epitope is involved in the preferential outgrowth of motor neurons on ventral roots and motor nerves. Eur. J. Neurosci. 1992, 4:628-639.
34. Meintanis S., Thomaidou D., Jessen K.R., Mirsky R., Matsas R. The neuron-glia signal beta-neuregulin promotes Schwann cell motility via the MAPK pathway. Glia 2001, 34:39-51.
35. Moradzadeh A., Borschel G.H., Luciano J.P., Whitlock E.L., Hayashi A., Hunter D.A., Mackinnon a.S.E. The impact of motor and sensory nerve architecture on nerve regeneration. Exp. Neurol. 2009, 212:370-376.
36. Morgan L., Jessen K.R., Mirsky R. The effects of cAMP on differentiation of cultured Schwann cells: progression from an early phenotype (04+) to a myelin phenotype (P0+, GFAP-, N-CAM-, NGF-receptor-) depends on growth inhibition. J. Cell Biol. 1991, 112:457-467.
37. Nichols C.M., Brenner M.J., Fox I.K., Tung T.H., Hunter D.A., Rickman S.R., Mackinnon S.E. Effect of motor versus sensory nerve grafts on peripheral nerve regeneration. Exp. Neurol. 2004, 190:347-355.
38. Oda Y., Okada Y., Katsuda S., Ikeda K., Nakanishi I. A simple method for the Schwann-cell preparation from newborn rat sciatic-nerves. J. Neurosci. Methods 1989, 28:163-169.
39. Paratcha G., Ledda F., Ibanez C.F. The neural cell adhesion molecule NCAM is an alternative signaling receptor for GDNF family ligands. Cell 2003, 113:867-879.
40. Parrinello S., Napoli I., Ribeiro S., Digby P.W., Fedorova M., Parkinson D.B., Doddrell R.D.S., Nakayama M., Adams R.H., Lloyd A.C. EphB signaling directs peripheral nerve regeneration through Sox2-dependent Schwann cell sorting. Cell 2010, 143:145-155.
41. Redett R., Jari R., Crawford T., Chen Y.G., Rohde C., Brushart T.M. Peripheral pathways regulate motoneuron collateral dynamics. J. Neurosci. 2005, 25:9406-9412.
42. Ribeiro-Resende V.T., Koenig B., Nichterwitz S., Oberhoffner S., Schlosshauer B. Strategies for inducing the formation of bands of Bungner in peripheral nerve regeneration. Biomaterials 2009, 30:5251-5259.
43. Sakamoto T., Kawazoe Y., Shen J.S., Takeda Y., Arakawa Y., Ogawa J., Oyanagi K., Ohashi T., Watanabe K., Inoue K., Eto Y., Watabe K. Adenoviral gene transfer of GDNF, BDNF and TGF beta 2, but not CNTF, cardiotrophin-1 or IGF1, protects injured adult motoneurons after facial nerve avulsion. J. Neurosci. Res. 2003, 72:54-64.
44. Shakhbazau A., Martinez J.A., Xu Q.G., Kawasoe J., van Minnen J., Midha R. Evidence for a systemic regulation of neurotrophin synthesis in response to peripheral nerve injury. J. Neurochem. 2013, 122:501-511.
45. Taylor A.M., Blurton-Jones M., Rhee S.W., Cribbs D.H., Cotman C.W., Jeon N.L. A microfluidic culture platform for CNS axonal injury, regeneration and transport. Nat. Methods 2005, 2:599-605.
46. Vyas A., Li Z.B., Aspalter M., Feiner J., Hoke A., Zhou C.H., O'Daly A., Abdullah M., Rohde C., Brushart T.M. An in vitro model of adult mammalian nerve repair. Exp. Neurol. 2010, 223:112-118.
47. Wood M.D., Borschel G.H., Sakiyama-Elbert S.E. Controlled release of glial-derived neurotrophic factor from fibrin matrices containing an affinity-based delivery system. J. Biomed. Mater. Res. Part A 2009, 89A:909-918.
48. Wood M.D., Moore A.M., Hunter D.A., Tuffaha S., Borschel G.H., Mackinnon S.E., Sakiyama-Elbert S.E. Affinity-based release of glial-derived neurotrophic factor from fibrin matrices enhances sciatic nerve regeneration. Acta Biomater. 2009, 5:959-968.
49. Woodhoo A., Alonso M.B.D., Droggiti A., Turmaine M., D'Antonio M., Parkinson D.B., Wilton D.K., Al-Shawi R., Al-Shawi R., Simons P., Shen J., Guillemot F., Radtke F., Meijer D., Feltri M.L., Wrabetz L., Mirsky R., Jessen K.R. Notch controls embryonic Schwann cell differentiation, postnatal myelination and adult plasticity. Nat. Neurosci. 2009, 12:839-U846.