Hyperglycaemia inhibits Schwann cell proliferation and migration and restricts regeneration of axons and Schwann cells from adult murine DRG

Molecular and Cellular Neuroscience

Volumn 37, Issue 2, 2008, Pages 298-311

  Gumy, Laura F ^a   Bampton, Edward T W ^a   Tolkovsky, Aviva M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Apoptosis; Diabetic neuropathy; Dorsal root ganglion neurons; Hyperglycaemia; Regeneration; Schwann cells

Indexed keywords

BROXURIDINE; NEU DIFFERENTIATION FACTOR; NEUREGULIN BETA1; RETINOBLASTOMA PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE SEVERITY; EXPLANT; GROWTH RATE; HYPERGLYCEMIA; MOUSE; NERVE FIBER; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SCHWANN CELL; SPINAL GANGLION;

ANIMALS; BROMODEOXYURIDINE; CELL DIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; DIABETIC NEUROPATHIES; G1 PHASE; GANGLIA, SPINAL; GLUCOSE; GROWTH CONES; HYPERGLYCEMIA; MICE; MICE, KNOCKOUT; MYELIN SHEATH; NERVE REGENERATION; NEUREGULIN-1; RATS; RETINOBLASTOMA PROTEIN; SCHWANN CELLS; WALLERIAN DEGENERATION;

MURINAE;

EID: 38649110117     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2007.10.004     Document Type: Article

References (75)

1. Almhanna K., Wilkins P.L., Bavis J.R., Harwalkar S., and Berti-Mattera L.N. Hyperglycemia triggers abnormal signaling and proliferative responses in Schwann cells. Neurochem. Res. 27 (2002) 1341-1347
2. Anderson C.N., and Tolkovsky A.M. A role for MAPK/ERK in sympathetic neuron survival: protection against a p53-dependent, JNK-independent induction of apoptosis by cytosine arabinoside. J. Neurosci. 19 (1999) 664-673
3. Atanasoski S., Boller D., De Ventura L., Koegel H., Boentert M., Young P., Werner S., and Suter U. Cell cycle inhibitors p21 and p16 are required for the regulation of Schwann cell proliferation. Glia 53 (2006) 147-157
4. Bampton E.T.W., and Taylor J.S. Effects of Schwann cell secreted factors on PC12 cell neuritogenesis and survival. J. Neurobiol. 63 (2005) 29-48
5. Benn S.C., Perrelet D., Kato A.C., Scholz J., Decosterd I., Mannion R.J., Bakowska J.C., and Woolf C.J. Hsp27 upregulation and phosphorylation is required for injured sensory and motor neuron survival. Neuron 36 (2002) 45-56
6. Brooks R.F. Continuous protein synthesis is required to maintain the probability of entry into S phase. Cell 12 (1977) 311-317
7. Buchkovich K., Duffy L.A., and Harlow E. The retinoblastoma protein is phosphorylated during specific phases of the cell cycle. Cell 58 (1989) 1097-1105
8. Carroll S.L., Miller M.L., Frohnert P.W., Kim S.S., and Corbett J.A. Expression of neuregulins and their putative receptors, ErbB2 and ErbB3, is induced during Wallerian degeneration. J. Neurosci. 17 (1997) 1642-1659
9. Chen P.L., Scully P., Shew J.Y., Wang J.Y., and Lee W.H. Phosphorylation of the retinoblastoma gene product is modulated during the cell cycle and cellular differentiation. Cell 58 (1989) 1193-1198
10. Chen Y.Y., McDonald D., Cheng C., Magnowski B., Durand J., and Zochodne D.W. Axon and Schwann cell partnership during nerve regrowth. J. Neuropathol. Exp. Neurol. 64 (2005) 612-622
11. Cheng C., and Zochodne D.W. Sensory neurons with activated capsase-3 survive long-term experimental diabetes. Diabetes 52 (2003) 2363-2371
12. Cheng L., Esch F.S., Marchionni M.A., and Mudge A.W. Control of Schwann cell survival and proliferation: autocrine factors and neuregulins. Mol. Cell. Neurosci. 12 (1998) 141-156
13. DeCaprio J.A., Ludlow J.W., Lynch D., Furukawa Y., Griffin J., Piwnica-Worms H., Huang C.M., and Livingston D.M. The product of the retinoblastoma susceptibility gene has properties of a cell cycle regulatory element. Cell 58 (1989) 1085-1095
14. Delaney C.L., Russell J.W., Cheng H.L., and Feldman E.L. Insulin-like growth factor-I and over-expression of Bcl-xL prevent glucose-mediated apoptosis in Schwann cells. J. Neuropathol. Exp. Neurol. 60 (2001) 147-160
15. Dobrowsky R.T., Rouen S., and Yu C. Altered neurotrophism in diabetic neuropathy: spelunking the caves of peripheral nerve. J. Pharmacol. Exp. Ther. 313 (2005) 485-491
16. Driscoll B., T'Ang A., Hu Y.H., Yan C.L., Fu Y., Luo Y., Wu K.J., Wen S., Shi X.H., Barsky L., Weinberg K., Murphree A.L., and Fung Y.K. Discovery of a regulatory motif that controls the exposure of specific upstream cyclin-dependent kinase sites that determine both conformation and growth suppressing activity of pRb. J. Biol. Chem. 274 (1999) 9463-9471
17. Dyck P.J., Lais A., Karnes J.L., O'Brien P., and Rizza R. Fiber loss is primary and multifocal in sural nerves in diabetic polyneuropathy. Ann. Neurol. 19 (1986) 425-439
18. Ekstrom A.R., and Tomlinson D.R. Impaired nerve regeneration in streptozotocin-diabetic rats. Effects of treatment with an aldose reductase inhibitor. J. Neurol. Sci. 93 (1989) 231-237
19. Fawcett J.W., and Keynes R.J. Peripheral nerve regeneration. Annu. Rev. Neurosci. 13 (1990) 43-60
20. Harrisingh M.C., Perez-Nadales E., Parkinson D.B., Malcolm D.S., Mudge A.W., and Lloyd A.C. The Ras/Raf/ERK signalling pathway drives Schwann cell dedifferentiation. EMBO J. 23 (2004) 3061-3071
21. Hoke A., Redett R., Hameed H., Jari R., Zhou C., Li Z.B., Griffin J.W., and Brushart T.M. Schwann cells express motor and sensory phenotypes that regulate axon regeneration. J. Neurosci. 26 (2006) 9646-9655
22. Jessen K.R., and Mirsky R. Schwann cells and their precursors emerge as major regulators of nerve development. Trends Neurosci. 22 (1999) 402-410
23. Kalichman M.W., Powell H.C., and Mizisin A.P. Reactive, degenerative, and proliferative Schwann cell responses in experimental galactose and human diabetic neuropathy. Acta Neuropathol. (Berl.) 95 (1998) 47-56
24. Kamiya H., Zhang W., and Sima A.A.F. Apoptotic stress is counterbalanced by survival elements preventing programmed cell death of dorsal root ganglions in subacute type 1 diabetic BB/Wor rats. Diabetes 54 (2005) 3288-3295
25. Kannan K., and Jain S.K. Effect of high glucose on cellular proliferation and lipid peroxidation in cultured Vero cells. Horm. Metab. Res. 26 (1994) 322-325
26. Kennedy J.M., and Zochodne D.W. The regenerative deficit of peripheral nerves in experimental diabetes: its extent, timing and possible mechanisms. Brain 123 (2000) 2118-2129
27. Kennedy J.M., and Zochodne D.W. Experimental diabetic neuropathy with spontaneous recovery: is there irreparable damage?. Diabetes 54 (2005) 830-837
28. Kennedy J.M., and Zochodne D.W. Impaired peripheral nerve regeneration in diabetes mellitus. J. Peripher. Nerv. Syst. 10 (2005) 144-157
29. Kishi M., Tanabe J., Schmelzer J.D., and Low P.A. Morphometry of dorsal root ganglion in chronic experimental diabetic neuropathy. Diabetes 51 (2002) 819-824
30. Lee K.F., Li E., Huber L.J., Landis S.C., Sharpe A.H., Chao M.V., and Jaenisch R. Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system. Cell 69 (1992) 737-749
31. Li Y., Tennekoon G.I., Birnbaum M., Marchionni M.A., and Rutkowski J.L. Neuregulin signaling through a PI3K/Akt/Bad pathway in Schwann cell survival. Mol. Cell. Neurosci. 17 (2001) 761-767
32. Liu R.Y., and Snider W.D. Different signaling pathways mediate regenerative versus developmental sensory axon growth. J. Neurosci. 21 RC64 (2001) 1-5
33. Mahanthappa N.K., Anton E.S., and Matthew W.D. Glial growth factor 2, a soluble neuregulin, directly increases Schwann cell motility and indirectly promotes neurite outgrowth. J. Neurosci. 16 (1996) 4673-4683
34. Martin C.L., Albers J., Herman W.H., Cleary P., Waberski B., Greene D.A., Stevens M.J., and Feldman E.L. Neuropathy among the diabetes control and complications trial cohort 8 years after trial completion. Diabetes Care 29 (2006) 340-344
35. Meier C., Parmantier E., Brennan A., Mirsky R., and Jessen K.R. Developing Schwann cells acquire the ability to survive without axons by establishing an autocrine circuit involving insulin-like growth factor, neurotrophin-3, and platelet-derived growth factor-BB. J. Neurosci. 19 (1999) 3847-3859
36. Meintanis S., Thomaidou D., Jessen K.R., Mirsky R., and Matsas R. The neuron-glia signal beta-neuregulin promotes Schwann cell motility via the MAPK pathway. Glia 34 (2001) 39-51
37. Mitchell P.J., Perez-Nadales E., Malcolm D.S., and Lloyd A.C. Dissecting the contribution of p16(INK4A) and the Rb family to the Ras transformed phenotype. Mol. Cell. Biol. 23 (2003) 2530-2542
38. Morrissey T.K., Levi A.D., Nuijens A., Sliwkowski M.X., and Bunge R.P. Axon-induced mitogenesis of human Schwann cells involves heregulin and p185erbB2. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 1431-1435
39. Nave K.A., and Salzer J.L. Axonal regulation of myelination by neuregulin 1. Curr. Opin. Neurobiol. 16 (2006) 492-500
40. Ortega A., Malumbres M., and Barbacid M. Cyclin D-dependent kinases, INK4 inhibitors, and cancer. Biochim. Biophys. Acta 1602 (2002) 73-87
41. Park S.H., Choi H.J., Lee J.H., Woo C.H., Kim J.H., and Han H.J. High glucose inihibit renal proximal tubule proliferation and involves PKC, oxidative stress and TGF-beta1. Kidney Int. 59 (2001) 1695-1705
42. Patel T.D., Jackman A., Rice F.L., Kucera J., and Snider W.D. Development of sensory neurons in the absence of NGF/TrkA signaling in vivo. Neuron 25 (2000) 345-357
43. Patel T.D., Kramer I., Kucera J., Niederkofler V., Jessell T.M., Arber S., and Snider W.D. Peripheral NT3 signaling is required for ETS protein expression and central patterning of proprioceptive sensory afferents. Neuron 38 (2003) 403-416
44. Perkins B.A., Greene D.A., and Bril V. Glycemic control is related to the morphological severity of diabetic sensorimotor polyneuropathy. Diabetes Care 24 (2001) 748-752
45. Petratos S., Butzkueven H., Shipham K., Cooper H., Bucci T., Reid K., Lopes E., Emery B., Cheema S.S., and Kilpatrick T.J. Schwann cell apoptosis in the postnatal axotomized sciatic nerve is mediated via NGF through the low-affinity neurotrophin receptor. J. Neuropathol. Exp. Neurol. 62 (2003) 398-411
46. Rahmatullah M., Schroering A., Rothblum K., Stahl R.C., Urban B., and Carey D.J. Synergistic regulation of Schwann cell proliferation by heregulin and forskolin. Mol. Cell. Biol. 18 (1998) 6245-6252
47. Rosner B.I., Hang T., and Tranquillo R.T. Schwann cell behavior in three-dimensional collagen gels: evidence for differential mechano-transduction and the influence of TGF-beta 1 in morphological polarization and differentiation. Exp. Neurol. 195 (2005) 81-91
48. Russell J.W., Sullivan K.A., Windebank A.J., Herrmann D.N., and Feldman E.L. Neurons undergo apoptosis in animal and cell culture models of diabetes. Neurobiol. Dis. 6 (1999) 347-363
49. Russell J.W., Golovoy D., Vincent A.M., Mahendru P., Olzmann J.A., Mentzer A., and Feldman E.L. High glucose-induced oxidative stress and mitochondrial dysfunction in neurons. FASEB J. 16 (2002) 1738-1748
50. Saito H., Sango K., Horie H., Ikeda H., Ishigatsubo Y., Ishikawa Y., and Inoue S. Enhanced neural regeneration from transected vagus nerve terminal in diabetic mice in vitro. Neuroreport 10 (1999) 1025-1028
51. Sango K., Horie H., Saito H., Ajiki K., Tokashiki A., Takeshita K., Ishigatsubo Y., Kawano H., and Ishikawa Y. Diabetes is not a potent inducer of neuronal cell death in mouse sensory ganglia, but it enhances neurite regeneration in vitro. Life Sci. 71 (2002) 2351-2368
52. Schmeichel A.M., Schmelzer J.D., and Low P.A. Oxidative injury and apoptosis of dorsal root ganglion neurons in chronic experimental diabetic neuropathy. Diabetes 52 (2003) 165-171
53. Sharma A.K., and Thomas P.K. Peripheral nerve regeneration in experimental diabetes. J. Neurol. Sci. 24 (1975) 417-424
54. Sima A.A., Bril V., Nathaniel V., McEwen T.A., Brown M.B., Lattimer S.A., and Greene D.A. Regeneration and repair of myelinated fibers in sural-nerve biopsy specimens from patients with diabetic neuropathy treated with sorbinil. N. Engl. J. Med. 319 (1988) 548-555
55. Sinnreich M., Taylor B.V., and Dyck P.J. Diabetic neuropathies. Classification, clinical features, and pathophysiological basis. Neurologist 11 (2005) 63-79
56. Snider W.D., and Silos-Santiago I. Dorsal root ganglion neurons require functional neurotrophin receptors for survival during development. Philos. Trans. R. Soc. Lond., B Biol. Sci. 351 (1996) 395-403
57. Spravchikov N., Sizyakov G., Gartsbein M., Accili D., Tennenbaum T., and Wertheimer E. Glucose effects on skin keratinocytes: implications for diabetes skin complications. Diabetes 50 (2001) 1627-1635
58. Srinivasan S., Stevens M., and Wiley J.W. Diabetic peripheral neuropathy: evidence for apoptosis and associated mitochondrial dysfunction. Diabetes 49 (2000) 1932-1938
59. Syroid D.E., Maycox P.J., Soilu-Hanninen M., Petratos S., Bucci T., Burrola P., Murray S., Cheema S., Lee K.F., Lemke G., and Kilpatrick T.J. Induction of postnatal schwann cell death by the low-affinity neurotrophin receptor in vitro and after axotomy. J. Neurosci. 20 (2000) 5741-5747
60. Tabernero A., Stewart H.J.S., Jessen K.R., and Mirsky R. The neuron-glia signal beta neuregulin induces sustained CREB phosphorylation on serine 133 in cultured rat Schwann cells. Mol. Cell. Neurosci. 10 (1998) 309-322
61. Tan W., Rouen S., Barkus K.M., Dremina Y.S., Hui D., Christianson J.A., Wright D.E., Yoon S.O., and Dobrowsky R.T. Nerve growth factor blocks the glucose-induced down-regulation of caveolin-1 expression in Schwann cells via p75 neurotrophin receptor signaling. J. Biol. Chem. 278 (2003) 23151-23162
62. Tantuwaya V.S., Bailey S.B., Schmidt R.E., Villadiego A., Tong J.X., and Rich K.M. Peripheral nerve regeneration through silicone chambers in streptozocin-induced diabetic rats. Brain Res. 759 (1997) 58-66
63. NTR) in Schwann cells is implicated in remyelination and motor recovery after peripheral nerve injury. Glia 55 (2007) 1199-1208
64. Torigoe K., Tanaka H.F., Takahashi A., Awaya A., and Hashimoto K. Basic behaviour of migratory Schwann cells in peripheral nerve regeneration. Exp. Neurol. 137 (1996) 301-308
65. Trial, Diabetes Control and Complications. The absence of a glycemic threshold for the development of long-term complications: the perspective of the Diabetes Control and Complications Trial. Diabetes 45 (1996) 1289-1298
66. Triolo D., Dina G., Lorenzetti I., Malaguti M., Morana P., Del Carro U., Comi G., Messing A., Quattrini A., and Previtali S.C. Loss of glial fibrillary acidic protein (GFAP) impairs Schwann cell proliferation and delays nerve regeneration after damage. J. Cell Sci. 119 (2006) 3981-3993
67. Vincent A.M., McLean L.L., Backus C., and Feldman E.L. Short-term hyperglycemia produces oxidative damage and apoptosis in neurons. FASEB J. 19 (2005) 638-640
68. Vincent A.M., Stevens M.J., Backus C., McLean L.L., and Feldman E.L. Cell culture modeling to test therapies against hyperglycemia-mediated oxidative stress and injury. Antioxid. Redox Signal. 7 (2005) 1494-1506
69. Vogelbaum M.A., Tong J.X., and Rich K.M. Developmental regulation of apoptosis in dorsal root ganglion neurons. J. Neurosci. 18 (1998) 8928-8935
70. White F.A., Keller-Peck C.R., Knudson C.M., Korsmeyer S.J., and Snider W.D. Widespread elimination of naturally occurring neuronal death in Bax-deficient mice. J. Neurosci. 18 (1998) 1428-1439
71. Xue L., Borutaite V., and Tolkovsky A.M. Inhibition of mitochondrial permeability transition and release of cytochrome c by anti-apoptotic nucleoside analogues. Biochem. Pharmacol. 64 (2002) 441-449
72. Yamauchi J., Chan J.R., Miyamoto Y., Tsujimoto G., and Shooter E.M. The neurotrophin-3 receptor TrkC directly phosphorylates and activates the nucleotide exchange factor Dbs to enhance Schwann cell migration. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 5198-5203
73. Yamauchi J., Miyamoto Y., Tanoue A., Shooter E.M., and Chan J.R. Ras activation of a Rac1 exchange factor, Tiam1, mediates neurotrophin-3-induced Schwann cell migration. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 14889-14894
74. Zochodne D.W. Diabetes mellitus and the peripheral nervous system: manifestations and mechanisms. Muscle Nerve 36 (2007) 144-166
75. Zochodne D.W., Verge V.M., Cheng C., Sun H., and Johnston J. Does diabetes target ganglion neurones? Progressive sensory neurone involvement in long-term experimental diabetes. Brain 124 (2001) 2319-2334