Prevention of thrombin-induced motoneuron degeneration with different neurotrophic factors in highly enriched cultures

Journal of Neurobiology

Volumn 38, Issue 4, 1999, Pages 571-580

  Turgeon, Victoria L ^a,c   Houenou, Lucien J ^a,b  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b Prosper Pharmaceuticals   (United States)

^c FURMAN UNIVERSITY   (United States)

Author keywords

Cell death; Development; Motoneuron; Receptor; Thrombin; Trophic factor

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CILIARY NEUROTROPHIC FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; NERVE GROWTH FACTOR; NEUROTROPHIC FACTOR; THROMBIN;

ANIMAL CELL; ARTICLE; BRAIN PROTECTION; CELL PROTECTION; CHICK EMBRYO; CONTROLLED STUDY; EMBRYO; HORMONE ACTION; MOTONEURON; NERVE CELL CULTURE; NERVE CELL DEGENERATION; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL CULTURE TECHNIQUES; CELL DEATH; CELLS, CULTURED; CHICK EMBRYO; CILIARY NEUROTROPHIC FACTOR; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; HUMANS; KINETICS; MOTOR NEURONS; NERVE GROWTH FACTORS; NERVE TISSUE PROTEINS; RECEPTOR, PAR-1; RECEPTORS, THROMBIN; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; THROMBIN;

EID: 0033036882     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4695(199903)38:4<571::AID-NEU11>3.0.CO;2-6     Document Type: Article

References (48)

1. Akaaboune M, Ma J, Festoff BW, Greenberg BD, Hantai D. 1994.) Neurotrophic regulation of mouse muscle β-amyloid protein precursor and α1-antichymotrypsin as revealed by axotomy. J Neurobiol 25:503-514.
2. Arakawa Y, Sendtner M, Thoenen H. 1990. Survival effect of ciliary neurotrophic factor (CNTF) on chick embryonic motoneurons in culture: comparison with other neurotrophic factors and cytokines. J Neurosci 10:3507-3515.
3. Brass LF. 1986. Regulation of phosphoinositide hydrolysis pathway in thrombin-stimulated platelets by a pertussis toxin-sensitive guanine nucleotide-binding protein. J Biol Chem 261:16833-16847.
4. Clarke PG, Oppenheim RW. 1995. Neuron death in vertebrate development: in vitro methods. Methods Cell Biol 46:277-321.
5. Dohrman U, Edgard D, Sendtner M, Thoenen H. 1986. Muscle derived factors that support and promote fiber outgrowth from embryonic chick spinal motor neurons in culture. Dev Biol 118:209-211.
6. Festoff BW, Rao JS, Hantaï D. 1991. Plasminogen activators and inhibitors in the neuromuscular system: III. The serpin protease nexin I is synthesized by muscle and localized at neuromuscular synapses. J Cell Physiol 147: 76-86.
7. Festoff BW, Smirnova IV, Ma J, Citron BA. 1996. Thrombin, its receptor and protease nexin I, its potent serpin, in the nervous system. Semin Thromb Hemost 22:267-271.
8. Grabham PW, Grand RJ, Gallimore PH. 1989. Purification of a serum factor which reverses dibutyrl cAMP induced differentiation. Cell Signal 1:269-281.
9. Gurwitz D, Cunningham DD. 1988. Thrombin modulates and reverses neuroblastoma neurite outgrowth. Proc Natl Acad Sci USA 85:3440-3444.
10. Gurwitz D, Cunningham DD. 1990. Neurite outgrowth activity of protease nexin-1 on neuroblastoma cells requires thrombin inhibition. J Cell Physiol 142:155-162.
11. Hamburger V. 1975. Cell death in the development of the lateral motor column of the chick embryo. J Comp Neurol 264:145-157.
12. Hamburger V, Hamilton HL. 1951. A series of normal stages in the development of the chick embryo. J Morphol 88:49-92.
13. Henderson CE, Camu W, Mettling C, Gouin A, Poulsen K, Karihaloo M, Rullamas J, Evans T, McMahan SB, Armanini MP, Berkemeir L, Philips HS, Rosenthal A. 1993. Neurotrophins promote motor neuron survival and are present in embryonic limb bud. Nature 363:266-270.
14. Henderson CE, Phillips HS, Pollock RA, Davies AM, Lemeulle C, Armanini M, Simpson LC, Moffet B, Vandlen RA, Koliatsos VE, Rosenthal A. 1994. GDNF: a potent survival factor for motoneurons present in peripheral nerve and muscle. Science 266:1062-1064.
15. Houenou LJ, Li L, Lo AC, Yan Q, Oppenheim RW. 1994. Naturally occurring and axotomy-induced motoneuron death and its prevention by neurotrophic agents: a comparison between chick and mouse. Prog Brain Res 102: 209-218.
16. Houenou LJ, McManaman JL, Prevette D, Oppenheim RW. 1991. Regulation of putative muscle-derived neurotrophic factors by muscle activity and innervation: in vivo and in vitro studies. J Neurosci 11:2829-2837.
17. Houenou LJ, Oppenheim RW, Li L, Lo AC, Prevette D. 1996. Regulation of spinal motoneuron survival by GDNF during development and following injury. Cell Tissue Res 286:219-223.
18. Houenou LJ, Turner PL, Li L, Oppenheim RW, Festoff BW. 1995. A serine protease inhibitor, protease nexin I, rescues motoneurons from naturally occurring and axotomy-induced cell death. Proc Natl Acad Sci USA 92:895-899.
19. Jalink K, van Corven EJ, Hengeveld T, Morii N, Narumiya S, Moolenaar WH. 1994. Inhibition of lysophosphatidate-and thrombin-induced neurite retraction and neuronal cell rounding by ADP ribosylation of the smal GTP-binding protein Rho. J Cell Biol 126:801-810.
20. Kahan C 1992. Coordinate, biphasic activation of p44 mitogen-activated protein kinase and S6 kinase by growth factors in hamster fibroblasts. J Biol Chem 267:13369-13375.
21. Koch CA, Anderson D, Moran EF, Ellis C, Pawson T. 1991. SH2 and SH3 domains: elements that control interactions of cytoplasmic signaling proteins. Science 252:668-674.
22. Li L, Houenou LJ, Wu W, Lei M, Prevette DM, Oppenehim RW. 1996. Mode of spinal motoneuron death following injury in adult mice: an EM study. Soc Neurosci Abstr 22:1182.
23. Li L, Oppenheim RW, Lei M, Houenou LJ. 1994. Neurotrophic agents prevent motoneuron death following sciatic nerve section in the neonatal mouse. J Neurobiol 25:759-766.
24. Li L, Wutian W, Leu-Fen HL, Lei M, Oppenheim RW, Houenou LJ. 1995. Rescue of adult mouse motoneurons from injury-induced cell death by glial cell line-derived neurotrophic factor. Proc Natl Acad Sci USA 92:9771-9775.
25. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. 1951. Protein measurement with Folin phenol reagent. J Biol Chem 193:265-275.
26. Medema RH, Bos JL. 1993. The role of p21 ras in receptor tyrosine kinase signaling. Crit Rev Oncol 4:615-661.
27. Milligan CE, Oppenheim RW, Schwartz LM. 1994. Motoneurons deprived of trophic support in vitro require new gene expression to undergo programmed cell death. J Neurobiol 25:1107-1110.
28. Milligan CE, Prevette D, Yaginuma H, Homma S, Cardwell C, Fritz LC, Tomaselli KJ, Oppenheim RW, Schwartz L. 1995. Peptide inhibitors of the ICE protease family arrest programmed cell death of motoneurons in vivo and in vitro. Neuron 15:385-393.
29. Neff NT, Prevette D, Houenou LJ, Lewis ME, Glicksman MA, Yin QW, Oppenheim RW. 1993. Insulin-like growth factors: putative muscle-derived trophic agents that promote motoneuron survival. J Neurobiol 24:1578-1588.
30. Oppenheim RW. 1989. The neurotrophic theory and naturally occurring motoneuron death. Trends Neurosci 12: 252-255.
31. Oppenheim RW. 1991. Cell death during development of the nervous system. Annu Rev Neurosci 14:453-501.
32. Oppenheim RW, Cole T, Prevette D. 1989. Early regional variations in motoneuron numbers arise by differential proliferation in the chick embryo spinal cord. Dev Biol 133:468-474.
33. Oppenheim RW, Houenou LJ, Johnson JE, Lin L-F, Li L, Lo AC, Newsome AL, Prevette DM, Wang S. 1995. Developing motor neurons rescued from programmed and axotomy-induced cell death by GDNF. Nature 373: 344-346.
34. Oppenheim RW, Prevette D, Haverkamp LJ, Houenou L, Yin Q-W, McManaman J. 1993. Biological studies of a putative avian muscle-derived neurotrophic factor that prevents naturally occurring motoneuron death in vivo. J Neurobiol 24:1065-1079.
35. Oppenheim RW, Prevette D, Yin QW, Collins F, MacDonald J. 1991. Control of embryonic motoneuron survival in vivo by ciliary neurotrophic factor. Science 257: 1616-1618.
36. Oppenheim RW, Yin QW, Prevette D, Yan Q. 1992. Brain-derived neurotrophic factor rescues developing avian motoneurons from cell death. Nature 360:755-757.
37. Seiler SM, Michel IM, Fenton JW II. 1992. Involvement of the "tethered-ligand" receptor in thrombin inhibition of platelet adenylate cyclase. Biochem Biophys Res Commun 182:1296-1302.
38. Smirnova IV, Zhang SX, Citron BA, Arnold PM, Festoff BW. 1998. Thrombin is a death signal that activates intracellular death protease pathways in motor neurons. J Neurobiol 36:64-80.
39. Stahl N, Yancopoulos GD. 1993. The alphas, betas and kinases of cytokine receptor complexes. Cell 74:587-590.
40. Stefanis L, Troy CM, Haiquing Q, Lloyd A. 1997. Inhibitors of trypsin-like serine proteases inhibit processing of the caspase nedd-2 and protect PC12 cells and sympathetic neurons from death evoked by withdrawal of trophic support. J Neurochem 69:1425-1437.
41. Stöckli KA, Lottspeich F, Sendtner M, Masiakowski P, Carroll P, Götz R, Lindholm D, Thoenen H. 1989. Molecular cloning, expression and regional distribution of rat ciliary neurotrophic factor. Nature 342:920-923.
42. Suidan HS, Stone SR, Hemmings BA, Monard D. 1992. Thrombin causes neurite retraction in neuronal cells through activation of cell surface receptors. Neuron 8:363-375.
43. Turgeon VL, Houenou LJ. 1997. The role of thrombin-like (serine) proteases in the development, plasticity and pathology of the nervous system. Brain Res Rev 25:85-95.
44. Turgeon VL, Lloyd ED, Wang S, Festoff BW, Houenou LJ. 1998. Thrombin perturbs neurite outgrowth and induces apoptotic cell death in enriched chick spinal motoneuron cultures through caspase activation. J Neurosci 18:6882-6891.
45. Vu TH, Hung DT, Wheaton VI, Coughlin SR. 1991. Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell 64:1057-1068.
46. Yaginuma H, Shiga T, Homma S, Ishihara R, Oppenheim RW. 1990. Identification of early developing axon projections from spinal interneurons in the chick embryo with a neuron specific β-tubulin antibody: evidence for a new "pioneer" pathway in the spinal cord. Development 108:705-716.
47. Yan Q, Matheson C, Lopez O. 1995. In vivo neurotrophic effects of GDNF on neonatal and adult facial motor neurons. Nature 373:341-344.
48. Zurn AD, Nick H, Monard D. 1988. A glial-derived nexin promotes neurite outgrowth in cultured chick sympathetic neurons. Dev Neurosci 10:17-24.