A molecular mechanism for synapse elimination: Novel inhibition of locally generated thrombin delays synapse loss in neonatal mouse muscle

Developmental Biology

Volumn 179, Issue 2, 1996, Pages 447-457

  Zoubine, M N ^b   Ma, J Y ^b   Smirnova, I V ^b   Citron, B A ^b   Festoff, B W ^a  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

PROTEINASE; PROTHROMBIN; THROMBIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; HISTOCHEMISTRY; MOUSE; NERVE ENDING; NEUROMUSCULAR SYNAPSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; SYNAPSE;

ANIMALIA; HIRUDINIDA;

EID: 0039534893     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1996.0274     Document Type: Article

References (68)

1. Akaaboune, M., Hantaï, D., Smirnova, I. V., and Festoff, B. W. (1995). Expression of protease nexin I in mouse skeletal muscle during development. Soc. Neurosci. Abstr. 21, 800.
2. Appel, S. H., and Festoff, B. W. (1971). Biochemical dysfunction and dementia. Contemp. Neurol. Ser. 9, 133-149.
3. Baker, J. B., Low, D. A., Simmer, R. L., and Cunningham, D. D. (1980). Protease-nexin: A cellular component that links thrombin and plasminogen activator and mediates their binding to cells. Cell 21, 37-45.
4. Balice-Gordon, R. J., Breedlove, S. M., Bernstein, S., and Lichtman, J. W. (1990). Neuromuscular junctions shrink and expand as muscle fiber size is manipulated: In vivo observations in the androgen-sensitive bulbocavernosus muscle of mice. J. Neurosci. 10, 2660-2671.
5. Balice-Gordon, R. J., Chua, C. K., Nelson, C. C., and Lichtman, J. W. (1993). Gradual loss of synaptic cartels precedes axon withdrawal at developing neuromuscular junctions. Neuron 11, 801-815.
6. Balice-Gordon, R. J., and Lichtman, J. W. (1990). In vivo visualization of the growth of pre-and postsynaptic elements of neuromuscular junctions in the mouse. J. Neurosci. 10, 894-908.
7. Balice-Gordon, R. J., and Lichtman, J. W. (1994). Long-term synapse loss induced by focal blockade of postsynaptic receptors. Nature 372, 519-524.
8. Beecher, K. L., Andersen, T. T., Fenton, J. W., and Festoff, B. W. (1994). Thrombin receptor peptides induce shape change in neonatal murine astrocytes in culture. J. Neurosci. Res. 37, 108-115.
9. Benzakour, O., Kanthou, C., Lupu, F., Dennehy, U., Goodwin, C., Scully, M. F., Kakkar, V. V., and Cooper, D. N. (1995). Prothrombin cleavage by human vascular smooth muscle cells: A potential alternative pathway to the coagulation cascade. J. Cell. Biochem. 59, 514-528.
10. Bleuel, A., De Gasparo, M., Whitebread, S., Püttner, I., and Monard, D. (1995). Regulation of protease nexin-1 expression in cultured Schwann cells is mediated by angiotensin II receptors. J. Neurosci. 15, 750-761.
11. Changeux, J. P., and Danchin, A. (1976). Selective stabilization of developing synapses as a mechanism for the specification of neuronal networks. Nature 264, 705-712.
12. Colman, H., and Lichtman, J. W. (1993). Interactions between nerve and muscle: Synapse elimination at the developing neuromuscular junction. Dev. Biol. 156, 1-10.
13. Connold, A. L., Evers, J. V., and Vrbova, G. (1986). Effect of low calcium and protease inhibitors on synapse elimination during postnatal development in the rat soleus muscle. Brain Res. 393, 99-107.
14. Cunningham, D. D., Pulliam, L., and Vaughan, P. J. (1993). Protease nexin-1 and thrombin: Injury-related processes in the brain. Thrombos. Haemostas. 70, 168-171.
15. Degen, S. J., Schaefer, L. A., Jamison, C. S., Grant, S. G., Fitzgibbon, J. J., Pai, J. A., and Elliott, R. W. (1990). Characterization of the cDNA coding for mouse prothrombin and localization of the gene on mouse chromosome 2. DNA Cell Biol. 9, 487-498.
16. DeKosky, S. T., and Scheff, S. W. (1990). Synapse loss in frontal cortex biopsies in Alzheimer's disease: Correlation with cognitive severity. Ann. Neurol. 27, 457-464.
17. Dennis, M. J. (1981). Development of the neuromuscular junction: Inductive interactions between cells. Ann. Rev. Neurosci 4, 43.
18. Dihanich, M., Kaser, M., Reinhard, E., Cunningham, D., and Monard, D. (1991). Prothrombin mRNA is expressed by cells of the nervous system. Neuron 6, 575-581.
19. Donovan, F. M., Vaughan, P. J., and Cunningham, D. D. (1994). Regulation of protease nexin-1 target protease specificity by collagen type IV. J. Biol. Chem. 269, 17199-17205.
20. English, A. W., and Schwartz, G. (1995). Both basic fibroblast growth factor and ciliary neurotrophic factor promote the retention of polyneuronal innervation of developing skeletal muscle fibers. Dev. Biol. 169, 57-64.
21. Farrell, D. H., Wagner, S. L., Yuan, R. H., and Cunningham, D. D. (1988). Localization of protease nexin-1 on the fibroblast extracellular matrix. J. Cell Physiol. 134, 179-188.
22. Fenton, J. W. (1986). Thrombin. Ann. N.Y. Acad. Sci. 485, 5-15.
23. Fenton, J. W. (1989). Thrombin interactions with hirudin. Semin. Thromb. Hemostas. 15, 265-268.
24. Fenton, J. W., Villanueva, G. B., Ofosu, F. A., and Maraganore, J. M. (1991). Thrombin inhibition by hirudin: How hirudin inhibits thrombin. Haemostasis 21(Suppl. 1), 27-31.
25. Fenton, J. W. (1988). Regulation of thrombin generation and functions. Semin. Thromb. Hemostas. 14, 234-240.
26. Festoff, B. W. (1980). Neuromuscular junction macromolecules in the pathogenesis of amyotrophic leteral sclerosis. Med. Hypotheses 6, 121-131.
27. Festoff, B. W. (1987). Proteases, their inhibitors and the extracellular matrix: Factors in nerve-muscle development and maintenance. Adv. Exp. Med. Biol. 209, 25-39.
28. Festoff, B. W. (1992). Protease cascade dysregulation and synaptic degeneration in amyotrophic lateral sclerosis. In "Handbook of Amyotrophic Lateral Sclerosis" (R. A. Smith, Ed.), Vol. 12, pp. 661-685. Dekker, New York.
29. Festoff, B. W., Nelson, P. G., and Brenneman, D. E. (1996). Prevention of activity-dependent neuronal death: Vasoactive intestinal polypeptide stimulates astrocytes to secrete the thrombin-inhibiting, neurotrophic serpin, protease nexin I. J. Neurobiol. 30, 255-266.
30. Festoff, B. W., Rao, J. S., and 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.
31. Hall, Z. W., and Sanes, J. R. (1993). Synaptic structure and development: The neuromuscular junction. Cell 72(Suppl.), 99-121.
32. Hantaï, D., Rao, J. S., Kahler, C., and Festoff, B. W. (1989). Decrease in plasminogen activator correlates with synapse elimination during neonatal development of mouse skeletal muscle. Proc. Natl. Acad. Sci. USA 86, 362-366.
33. Ho, G. J., Smirnova, I. V., Akaaboune, M., Hantai, D., and Festoff, B. W. (1994). Serine proteases and their serpin inhibitors in Alzheimer's disease. Biomed. Pharmacother. 48, 296-304.
34. Hung, D. T., Vu, T. K., Wheaton, V. I., Ishii, K., and Coughlin, S. R. (1992). Cloned platelet thrombin receptor is necessary for thrombin-induced platelet activation. J. Clin. Invest. 89, 1350-1353.
35. Ishii, K., Gerszten, R., Zheng, Y. W., Welsh, J. B., Turck, C. W., and Coughlin, S. R. (1995). Determinants of thrombin receptor cleavage. Receptor domains involved, specificity, and role of the P3 aspartate. J. Biol. Chem. 270, 16435-16440.
36. Jalink, K., and Moolenaar, W. H. (1992). Thrombin receptor activation causes rapid neural cell rounding and neurite retraction independent of classic second messengers. J. Cell Biol. 118, 411-419.
37. Jalink, K., van Corven, E. J., Hengeveld, T., Morii, N., Narumiya, S., and Moolenaar, W. H. (1994). Inhibition of lysophosphatidate-and thrombin-induced neurite retraction and neuronal cell rounding by ADP ribosylation of the small GTP-binding protein Rho. J. Cell Biol. 126, 801-810.
38. Lichtman, J. W., and Balice-Gordon, R. J. (1990). Understanding synaptic competition in theory and in practice [Review]. J. Neurobiol. 21, 99-106.
39. Liu, Y., Fields, R. D., Festoff, B. W., and Nelson, P. G. (1994a). Proteolytic action of thrombin is required for electrical activity-dependent synapse reduction. Proc. Natl. Acad. Sci. USA 91, 10300-10304.
40. Liu, Y., Fields, R. D., Fitzgerald, S., Festoff, B. W., and Nelson, P. G. (1994b). Proteolytic activity, synapse elimination, and the Hebb synapse. J. Neurobiol. 25, 325-335.
41. Ma, J., Yang, S. X., Ho, G. J., and Festoff, B. W. (1994). Insulin-like growth factor binding protein-1 at mouse neuromuscular synapses. Synapse 17, 225-229.
42. Monard, D. (1993). Tinkering with certain blood components can engender distinct functions in the nervous system [Review]. Perspect. Dev. Neurobiol. 1, 165-168.
43. Monard, D., Reinhard, E., Meier, R., Sommer, J., Farmer, L., Rovelli, G., and Ortmann, R. (1990). Steps in establishing a biological relevance for glia-derived nexin. In "Serine Proteases and Their Serpin Inhibitors in the Nervous System: Regulation in Development and in Degenerative and Malignant Disease" (B. W. Festoff, Ed.), pp. 275-281. Plenum, New York.
44. Nelson, P. G., Fields, R. D., Yu, C., and Liu, Y. (1993). Synapse elimination from the mouse neuromuscular junction in vitro: A non-Hebbian activity-dependent process. J. Neurobiol. 24, 1517-1530.
45. Nelson, P. G., Yadav, K., Fitzgerald, S., and Brenneman, D. E. (1994). Activation of mouse skeletal muscle in vitro produces increased secretion of thrombin. Soc. Neurosci. Abstr. 20, 1089.
46. Niclou, S., Suidan, H. S., Brown-Luedi, M., and Monard, D. (1994). Expression of the thrombin receptor mRNA in rat brain. Cell. Mol. Biol. 40, 421-428.
47. O'Brien, R., Ostberg, A., and Vrbova, G. (1978). Observation on the elimination of polyneuronal innervation in developing mammalian skeletal muscle. J. Physiol. 282, 571-582.
48. O'Brien, R. A., Ostberg, A. J., and Vrbova, G. (1984). Protease inhibitors reduce the loss of nerve terminals induced by activity and calcium in developing rat soleus muscles in vitro. Neuroscience 12, 637-646.
49. Pouyssegur, J., L'Allemain, G., Lenormand, P., Pages, G., Pavirani, A., Rasmussen, U., Van Obberghen-Schilling, E., and Vouret-Craviari, V. (1993). Alpha-thrombin receptor and MAP kinases in the control of cell growth. Nouv. Rev. Francaise Hematol. 35, 263-264.
50. Purves, D., and Lichtman, J. W. (1980). Elimination of synapses in the developing nervous system. Science 210, 153-157.
51. Riley, D. (1977). Spontaneous elimination of nerve terminals from the endplates of developing skeletal myofibers. Brain Res. 134, 279-285.
52. Rosing, J., and Tans, G. (1988). Meizothrombin, a major product of factor Xa-catalyzed prothrombin activation. Thrombos. Haemostas. 60, 355-360.
53. Rovelli, G., Stone, S. R., Preissner, K. T., and Monard, D. (1990). Specific interaction of vitronectin with the cell-secreted protease inhibitor glia-derived nexin and its thrombin complex. Eur. J. Biochem. 192, 797-803.
54. Sasaki, S., and Maruyama, S. (1994). Synapse loss in anterior horn neurons in amyotrophic lateral sclerosis. Acta Neuropathol. 88, 222-227.
55. Scott, R. W., Bergman, B. L., Bajpai, A., Hersh, R. T., Rodriguez, H., Jones, B. N., Barreda, C., Watts, S., and Baker, J. B. (1985). Protease nexin. Properties and a modified purification procedure. J. Biol. Chem. 260, 7029-7034.
56. Siegel, S. (1956). "Nonparametric Statistics for the Behavioral Sciences." McGraw-Hill, New York.
57. Siman, R., Baudry, M., and Lynch, G. S. (1987). Calcium-activated protease as possible mediator of synaptic plasticity. In "Synaptic Function" (G. M. Edelman, W. E. I. Gall, and W. M. Cowan, Eds.), pp. 519-548. Wiley, New York.
58. Smirnova, I. V., Ho, G. J., Fenton, J. W. L, and Festoff, B. W. (1994). Extravascular proteolysis and the nervous system: Serine protease/serpin balance. Semin. Thromb. Hemostas. 20, 426-432.
59. Stone, S. R., Nick, H., Hofsteenge, J., and Monard, D. (1987). Glial-derived neurite-promoting factor is a slow-binding inhibitor of trypsin, thrombin, and urokinase. Arch. Biochem. Biophys. 252, 237-244.
60. Suidan, H. S., Stone, S. R., Hemmings, B. A., and Monard, D. (1992). Thrombin causes neurite retraction in neuronal cells through activation of cell surface receptors. Neuron 8, 363-375.
61. Terry, R. D., Masliah, E., Salmon, D. P., Butters, N., DeTeresa, R., Hill, R., Hansen, L. A., and Katzman, R. (1991). Physical basis of cognitive alterations in Alzheimer's disease: Synapse loss is the major correlate of cognitive impairment. Ann. Neurol. 30, 572-580.
62. Tian, W. H., Festoff, B. W., Blot, S., Diaz, J., and Hantaï, D. (1995). Synaptic transmission blockade increases plasminogen activator activity in mouse skeletal muscle poisoned with botulinum toxin type A. Synapse 20, 24-32.
63. Van Essen, D. C. (1982). "Neuromuscular Synapse Elimination," pp. 333-376. Plenum, New York.
64. Van Essen, D. C., Gordon, H., Soha, J. M., and Fraser, S. E. (1990). Synaptic dynamics at the neuromuscular junction: Mechanisms and models. J. Neurobiol. 21, 223-249.
65. Verdière-Sahuqué, M., Akaaboune, M., Lachkar, S., Festoff, B. W., Jandrot Peruss, M., Garcia, L., Barlovatz-Meimon, G., and Hantaï, D. (1996). Myoblast fusion promotes the appearance of active protease nexin I on human muscle cell surfaces. Exp. Cell Res. 222, 70-76.
66. Vrbová, G., and Fisher, T. J. (1989). The effect of inhibiting the calcium activated neutral protease, on the motor unit size after partial denervation of the rat soleus muscle. Eur. J. Neurosci. 1, 616-625.
67. Vu, T. K., Hung, D. T., Wheaton, V. I., and Coughlin, S. R. (1991). Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell 64, 1057-1068.
68. Witting, J. I., Miller, T. M., and Fenton, J. W. d. (1987). Human alpha-and gamma-thrombin specificity with tripeptide p-nitro-analide substrates under physiologically relevant conditions. Thromb. Res. 46, 567-574.