A model for sealing plasmalemmal damage in neurons and other eukaryotic cells

Journal of Neuroscience

Volumn 30, Issue 47, 2010, Pages 15790-15800

  Spaeth, Christopher S ^a   Boydston, Elaine A ^a,b   Figard, Lauren R ^a,c   Zuzek, Aleksej ^a   Bittner, George D ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c Molecular and Cellular Biology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; KT 5720; MELATONIN;

ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL INTERACTION; CELL MEMBRANE; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVATION; EUKARYOTIC CELL; HIPPOCAMPUS; NERVE CELL LESION; NERVE REGENERATION; NERVE TRANSECTION; NEURITE; OXIDATION; PRIORITY JOURNAL;

ANIMALS; CELL LINE, TUMOR; CELL MEMBRANE; EUKARYOTIC CELLS; HIPPOCAMPUS; MODELS, NEUROLOGICAL; NEURONS; RATS;

EID: 78649402456     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4155-10.2010     Document Type: Article

References (79)

1. Agresti A (1996) An introduction to categorical data analysis, pp 60-64. New York: Wiley.
2. Arellano M, Valdivieso MH, Calonge TM, Coll PM, Duran A, Perez P (1999) Schizosaccharomyces pombe protein kinase C homologues, pck1p and pck2p, are targets of rho1p and rho2p and differentially regulate cell integrity. J Cell Sci 112:3569-3578.
3. Ballinger ML, Blanchette AR, Krause TL, Smyers ME, Fishman HM, Bittner GD (1997) Delaminating myelin membranes help seal the cut ends of severed earthworm giant axons. J Neurobiol 33:945-960.
4. Bansal D, Campbell KP (2004) Dysferlin and the plasma membrane repair pathway in muscular dystrophy. Trends Cell Biol 14:206-213.
5. Barros F, Gómez-Varela D, Viloria CG, Palomero T, Giráldez T, de la Peña P (2009) Modulation of human erg K+ channel gating by activation of a G protein-coupled receptor and protein kinase C. J Physiol 511:333-346.
6. Bittner GD, Fishman HM (2000) Axonal sealing following injury. In: Axonal regeneration in the central nervous system (Ingoglia N, Murray M, eds), pp 337-370. New York: Dekker.
7. Blanchette AR, Ballinger ML, Fishman HM, Bittner GD (1999) Calcium entry initiates processes that restore a barrier to dye entry in severed earthworm giant axons. Neurosci Lett 272:147-150.
8. Bonanomi D, Rusconi L, Colombo CA, Benfenati F, Valtorta F (2007) Synaptophysin I selectively specifies the exocytic pathway of synaptobrevin 2/VAMP2. Biochem J 404:525-534.
9. Bottenstein JE, Sato GH (1979) Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc Natl Acad Sci U S A 76:514-517.
10. Branham MT, Bustos MA, De Blas GA, Rehmann H, Zarelli VE, Treviño CL, Darszon A, Mayorga LS, Tomes CN (2009) Epac activates the small G proteins Rap1 and Rab3A to achieve exocytosis. J Biol Chem 284:24825-24839.
11. Britt JM, Kane JR, Spaeth CS, Zuzek A, Robinson GL, Gbanaglo MY, Estler CJ, Boydston EA, Schallert T, Bittner GD (2010) Polyethylene glycol rapidly restores axonal integrity and improves the rate of motor behavior recovery after sciatic crush injury. J Neurophysiol 104:695-703.
12. 2+-independent neurotransmission. J Neurophysiol 98:794-806.
13. Cai C, Masumiya H, Weisleder N, Matsuda N, Nishi M, Hwang M, Ko JK, Lin P, Thornton A, Zhao X, Pan Z, Komazaki S, Brotto M, Takeshima H, Ma J (2009a) MG53 nucleates assembly of cell membrane repair machinery. Nat Cell Biol 11:56-64.
14. Cai C, Weisleder N, Ko JK, Komazaki S, Sunada Y, Nishi M, Takeshima H, Ma J (2009b) Membrane repair defects in muscular dystrophy are linked to altered interaction between MG53, caveolin-3 and dysferlin. J Biol Chem 284:15894-15902.
15. Cai D, Qiu J, Cao Z, McAtee M, Bregman BS, Filbin MT (2001) Neuronal cyclic AMP controls the developmental loss in ability of axons to regenerate. J Neurosci 21:4731-4739.
16. Chierzi S, Ratto GM, Verma P, Fawcett JW (2005) The ability of axons to regenerate their growth cones depends on axonal type and age, and is regulated by calcium, cAMP and ERK. Eur J Neurosci 21:2051-2062. (Pubitemid 40695229)
17. Christensen AE, Selheim F, de Rooij J, Dremier S, Schwede F, Dao KK, Martinez A, Maenhaut C, Bos JL, Genieser HG, Døskeland SO (2003) cAMP analog mapping of Epac1 and cAMP kinase. J Biol Chem 278:35394-35402.
18. Circu ML, Moyer MP, Harrison L, Aw TY (2009) Contribution of glutathione status to oxidant-induced mitochondrial DNA damage in colonic epithelial cells. Free Rad Biol Med 47:1190-1198.
19. Dalton GD, Dewey WL (2006) Protein kinase inhibitor peptide (PKI): a family of endogenous neuropeptides that modulate neuronal cAMP-dependent protein kinase function. Neuropeptides 40:23-34.
20. Davies SP, Reddy H, Caivano M, Cohen P (2000) Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351:95-105.
21. Deák F, Ok-Ho Shin OH, Tang J, Hanson P, Ubach J, Jahn R, Rizo J, Kavalali ET, Südhof TS (2006) Rabphilin regulates SNARE-dependent repriming of synaptic vesicles for fusion. EMBO J 25:2856-2866.
22. Detrait E, Eddleman CS, Yoo S, Fukuda M, Nguyen MP, Bittner GD, Fishman HM (2000a) Axolemmal repair requires proteins that mediate synaptic vesicle fusion. J Neurobiol 44:382-391.
23. 2+ and synaptotagmin. J Neurosci Res 62:566-573.
24. Dunn TA, Storm DR, Feller MB (2009) Calcium-dependent increases in protein kinase-A activity in mouse retinal ganglion cells are mediated by multiple adenylate cyclases. PLoS One 4:e7877.
25. Eddleman CS, Ballinger ML, Smyers ME, Godell CM, Fishman HM, Bittner GD (1997) Repair of plasmalemmal lesions by vesicles. Proc Natl Acad Sci U S A 94:4745-4750.
26. 2+ and axolemmal injury. J Neurosci 18:4029-4041.
27. Eddleman CS, Bittner GD, Fishman HM (2000) Barrier permeability at cut axonal ends progressively decreases until an ionic seal is formed. Biophys J 79:1883-1890.
28. Enserink JM, Christensen AE, de Rooij J, van Triest M, Schwede F, Genieser HG, Døskeland SO, Blank JL, Bos JL (2002) Anovel Epac-specific cAMP analog demonstrates independent regulation of Rap1 and ERK. Nat Cell Biol 4:901-906.
29. Fishman HM, Bittner GD (2003) Vesicle-mediated restoration of a plasmalemmal barrier after axonal injury. News Physiol Sci 18:115-118.
30. 2+ sensor in pancreatic beta-cells: involvement of cAMP-GEFII·Rim2·Piccolo complex in cAMP-dependent exocytosis. J Biol Chem 277:50497-50502.
31. Garcia EP, McPherson PS, Chilcote TJ, Takei K, De Camilli P (1995) rbSec1A and B colocalize with syntaxin 1 and SNAP-25 throughout the axon, but are not in a stable complex with syntaxin. J Cell Biol 129:105-120.
32. Gatlin JC, Estrada-Bernal A, Sanford SD, Pfenninger KH (2006) Myristoylated, alanine-rich C-kinase substrate phosphorylation regulates growth cone adhesion and pathfinding. Mol Biol Cell 17:5115-5130.
33. Gerhart J, Kirchner M (1997) Cells, embryos and evolution, p 642. Malden, MA: Blackwell Science.
34. Godell CM, Smyers ME, Eddleman CS, Ballinger ML, Fishman HM, Bittner GD (1997) Calpain activity promotes the sealing of severed giant axons. Proc Natl Acad Sci U S A 94:4751-4756.
35. Hannila SS, Filbin MT (2008) The role of cyclic AMP signaling in promoting axonal regeneration after spinal cord injury. Exp Neurol 209:321-332.
36. Hatakeyama H, Takahashi N, Kishimoto T, Nemoto T, Kasai H (2007) Two cAMP pathways differentially regulate exocytosis of large dense core and small vesicles in mouse β cells. J Physiol 582:1087-1098.
37. Hochbaum D, Hong K, Barila G, Ribeiro-Neto F, Altschuler DL (2008) Epac, in synergy with cAMP-dependent protein kinase (PKA), is required for cAMP-mediated mitogenesis. J Biol Chem 283:4464-4468.
38. Kandel ER, Schwartz, JH, Jessel T (1991) Principles of neural science, Ed 3. New York: McGraw-Hill.
39. Korshunova I, Novitskaya V, Kiryushko D, Pedersen N, Kolkova K, Kropotova E, Mosevitsky M, Rayko M, Morrow JS, Ginzburg I, Berezin V, Bock E (2007) GAP-43 regulates NCAM-180 mediated neurite outgrowth. J Neurochem 100:1599-1612. (Pubitemid 46376203)
40. Krause TL, Fishman HM, Ballinger ML, Bittner GD (1994) Extent and mechanism of sealing in transected giant axons of squid and earthworms. J Neurosci 14:6638-6651.
41. Kwan EP, Xie L, Sheu L, Ohtsuka T, Gaisano HY (2007) Interaction between Munc13-1 and RIM is critical for glucagon-like peptide-1 mediated rescue of exocytotic defects in Munc13-1 deficient pancreatic beta-cells. Diabetes 56:2579-2588.
42. Lichstein JW, Ballinger ML, Blanchette AR, Fishman HM, Bittner GD (2000) Structural changes at cut ends of earthworm giant axons in the interval between dye barrier formation and neuritic outgrowth. J Comp Neurol 416:143-157.
43. Liu XF, Xie X, Miki T (2006) Inhibition of protein kinase C zeta blocks the attachment of stable microtubules to kinetochores leading to abnormal chromosome alignment. Cell Signal 18:2314-2323.
44. Loewy AD, Schader RE (1977) A quantitative study of retrograde neuronal changes in Clarke's column. J Comp Neurol 171:65-81.
45. Lucas JH, Gross GW, Emery DG, Gardner CR (1985) Neuronal survival or death after dendrite transection close to the perikaryon: correlation with electrophysiologic, morphologic, and ultrastructural changes. Cent Nerv Syst Trauma 2:231-255.
46. Lucas JH, Emery DG, Higgins ML, Gross GW (1990) Neuronal survival and dynamics of ultrastructural damage after dendrotomy in low calcium. J Neurotrauma 7:169-192.
47. McNeil P (2009) Membrane repair redux: redox of MG53. Nat Cell Biol 11:7-9.
48. Mellgren RL, Zhang W, Miyake K, McNeil PL (2007) Calpain is required for the rapid, calcium-dependent repair of wounded plasma membrane. J Biol Chem 282:2567-2575.
49. 2+-dependent synaptic activity. J Neurosci 26:11670-11681.
50. Millán-Plano S, Piedrafita E, Miana-Mena FJ, Fuentes-Broto L, Martínez-Ballarín E, López-Pingarrón L, Sáenz MA, García JJ (2010) Melatonin and structurally-related compounds protect synaptosomal membranes from free radical damage. Int J Mol Sci 11:312-328.
51. Miller MW, Mooney SM, Middleton FA (2006) Transforming growth factor β1 and ethanol affect transcription and translation of genes and proteins required for cell adhesion molecules in B104 neuroblastoma cells. J Neurochem 97:1182-1190.
52. Murray AJ, Shewan DA (2008) Epac mediates cyclic AMP-dependent axon growth, guidance and regeneration. Mol Cell Neurosci 38:578-588.
53. Nagy G, Reim K, Matti U, Brose N, Binz T, Rettig J, Neher E, Sørensen JB (2004) Regulation of releasable vesicle pool sizes by protein kinase A-dependent phosphorylation of SNAP-25. Neuron 41:417-429.
54. Nehrt A, Haman K, Ouyang H, Shi (2010) Polyethylene glycol enhances axolemmal resealing following transection in cultured cells and in ex vivo spinal cord. J Neurotrauma 27:151-161.
55. Nguyen MP, Bittner GD, Fishman HM (2005) Critical interval of somal calcium transient after neurite transection determines B104 cell survival. J Neurosci Res 81:805-816.
56. Qiu J, Cai D, Dai H, McAtee M, Hoffman PN, Bregman BS, Filbin MT (2002) Spinal axon regeneration induced by elevation of cyclic AMP. Neuron 34:895-903.
57. 2+-regulated exocytosis of lysosomes. Cell 106:157-169.
58. Ramon y Cajal S (1928) Degeneration and regeneration in the nervous system. New York: Hoffner.
59. Schlaepfer WW (1973) Effects of nerve constriction on oxygenated excised segments of rat peripheral nerve. J Neuropathol Exp Neurol 32:203-217.
60. Schlaepfer WW, Bunge RP (1973) Effects of calcium ion concentration on the degeneration of amputated axons in tissue culture. J Cell Biol 59:456-470.
61. 2+-dependent exocytosis through both PKA and Epac2 in mouse melanotrophs from pituitary slices. J Physiol 567:799-813.
62. SiskováZ, Baron W, de Vries H, Hoekstra D (2006) Fibronectin impedes "myelin" sheet-directed flow in oligodendrocytes: a role for a beta 1 integrin-mediated PKC signaling pathway in vesicular trafficking. Mol Cell Neurosci 33:150-159.
63. Sivasankaran R, Pei J, Wang KC, Zhang YP, Shields CB, Xu XM, He Z (2004) PKC mediates inhibitory effects of myelin and chondroitin sulfate proteoglycans on axonal regeneration. Nat Neurosci 7:261-268. (Pubitemid 38280450)
64. Spira ME, Benbassat D, Dormann A (1993) Resealing of the proximal and distal cut ends of transected axons: electrophysiological and ultrastructural analysis. J Neurobiol 24:300-316.
65. Steinberg SF (2008) Structural basis of protein kinase C isoform function. Physiol Rev 88:1341-1378.
66. Steinhardt RA, Bi G, Alderton JM (1994) Cell membrane resealing by a vesicular mechanism similar to neurotransmitter release. Science 263:390-393.
67. Ster J, de Bock F, Bertaso F, Abitbol K, Daniel H, Bockaert J, Fagni L (2009) Epac mediates PACAP-dependent long-term depression in the hippocampus. J Physiol 587:101-113.
68. Südhof TC, Rothman JE (2009) Membrane fusion: grappling with SNARE proteins. Science 323:474-477.
69. + channels in B104 neuronal cell line. Neurosci Lett 340:123-126.
70. Tao-Cheng JH, Du J, McBain CJ (2000) Snap-25 is polarized to axons and abundant along the axolemma: an immunogold study of intact neurons. J Neurocytol 29:67-77.
71. Toda M, Shirao T, Uyemura K (1999) Suppression of an actin-binding protein, drebrin, by antisense transfection attenuates neurite outgrowth in neuroblastoma B104 cells. Brain Res Dev Brain Res 114:193-200.
72. Togo T, Alderton JM, Steinhardt RA (2003) Long-term potentiation of exocytosis and cell membrane repair in fibroblasts. Mol Biol Cell 14:93-106.
73. Tsai SY, Yang LY, Wu CH, Chang SF, Hsu CY, Wei CP, Leu SJ, Liaw J, Lee YH, Tsai MD (2007) Injury-induced Janus kinase/protein kinase C-dependent phosphorylation of growth-associated protein 43 and signal transducer and activator of transcription 3 for neurite growth in dorsal root ganglion. J Neurosci Res 85:321-331.
74. Uberall F, Giselbrecht S, Hellbert K, Fresser F, Bauer B, Gschwendt M, Grunicke HH, Baier G (1997) Conventional PKC-alpha, novel PKC-epsilon and PKC-theta, but not atypical PKC-lambda are MARCKS kinases in intact NIH 3T3 fibroblasts. J Biol Chem 272:4072-4078.
75. van Diepen MT, Spencer GE, van Minnen J, Gouwenberg Y, Bouwman J, Smit AB, van Kesteren RE (2005) The molluscan RING-finger protein L-TRIM is essential for neuronal outgrowth. Mol Cell Neurosci 29:74-81.
76. 2+-regulated proteins. J Neurosci Res 74:541-551.
77. 2+ concentration. J Neurobiol 60:137-153.
78. 2+ increases and by cAMP. J Neurosci 19:2432-2441.
79. Yoshihara M, Suzuki K, Kidokoro Y (2000) Two independent pathways mediated by cAMP and protein kinase A enhance spontaneous transmitter release at Drosophila neuromuscular junctions. J Neurosci 20:8315-8322.