Thrombin perturbs neurite outgrowth and induces apoptotic cell death in enriched chick spinal motoneuron cultures through caspase activation

Journal of Neuroscience

Volumn 18, Issue 17, 1998, Pages 6882-6891

  Houenou, Lucien J ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Caspases; PAR 1; Serine proteases; Spinal motoneuron cultures; Thrombin

Indexed keywords

SERINE PROTEINASE; THROMBIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CHICK EMBRYO; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; GROWTH REGULATION; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SPINAL CORD MOTONEURON;

EID: 17344365478     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.18-17-06882.1998     Document Type: Article

References (59)

1. Abraham CR, Selkoe D, Potter H (1988) Immunochemical identification of the serine protease inhibitor alpha-1-antichymotrypsin in the brain amyloid deposits of Alzheimer's disease. Cell 52:487-501.
2. Arakawa Y, Scndtner M, Thoenen H (1990) Survival effect of ciliary neurotrophic factor (CNTF) on chick motoneurons in culture: comparison with other neurotrophic factors and cytokines. J Neurosci 10:3507-3515.
3. Baker JB, Low DA, Simmer RL, Cunningham DD (1980) Proteasenexin: a cellular component that links thrombin and plasminogen activator and mediates their binding to cells. Cell 21:37-45.
4. Barinaga M (1996) Forging a path to cell death. Science 273:735-737.
5. Beecher KL, Anderson TT, Fenton II JW, Festoff BW (1994) Thrombin receptor peptides induce shape changes in neonatal murine astrocytes in culture. J Neurosci Res 37:108-115.
6. Brun A, Englund E (1981) Regional pattern of degeneration in Alzheimer's disease: neuronal loss and histopathological grading. Histopathology 5:549-564.
7. Cavanaugh K, Gurwitz D, Cunningham DD, Bradshaw R (1990) Reciprocal modulation of astrocyte stellation by thrombin and protease nexin-1. J Neurochem 54:1735-1743.
8. Chu-Wang IW, Oppenheim RW (1978) Cell death of motoneurons in the chick embryo spinal cord. II. A quantitative and qualitative analysis of degeneration in the ventral root, including evidence for axon outgrowth and limb innervation prior to cell death. J Comp Neurol 177:59-85.
9. Coleman PD, Flood DG (1987) Neuron numbers and dendritic extent in normal aging and Alzheimer's disease. Neurobiol Aging 8:521-545.
10. Cunningham DD, Van Nostrand WE, Farrell DH, Campell CH (1987) Proteases in biological control and biotechnology. New York: Liss.
11. Dihanich M, Kaser M, Reinhard E, Cunningham D, Monard D (1991) Prothrombin mRNA is expressed by cells of the nervous system. Neuron 6:575-581.
12. 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.
13. Donovan FM, Pike CJ, Cunningham DD (1997) Thrombin induces apoptosis in cultured neurons and astrocytes via a pathway requiring tyrosine kinase and RhoA activities. J Neurosci 17:5316-5326.
14. Ericson J, Thor S, Edlund T, Jessell TM, Yamada T (1992) Early stages of motor neuron differentiation revealed by expression of homeobox gene Islet-1. Science 256:1555-1560.
15. Festoff BW, Reddy RB, VanBecelaere M, Smirnova I, Chao J (1994) Activation of serpins and their cognate proteases in muscle after crush injury. J Cell Physiol 159:11-18.
16. 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.
17. Gavrieli Y, Sherman Y, Ben-Saan SA (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119:493-501.
18. Grabham PW, Gallimore PH, Grand RJ (1992) Vitronectin is the major serum protein essential for NGF-mediated neurite outgrowth from PC12 cells. Exp Cell Res 202:337-344.
19. Gurwitz D, Cunningham DD (1988) Thrombin modulates and reverses neuroblastoma neurite outgrowth. Proc Natl Acad Sci USA 85:3440-3444.
20. Gurwitz D, Cunningham DD (1990) Neurite outgrowth activity of protease nexin-1 on neuroblastoma cells requires thrombin inhibition. J Cell Physiol 142:155-162.
21. Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88:49-92.
22. Ho GJ, Smirnova IV, Akaaboune M, Hantai D, Festoff BW (1994) Serine proteases and their serpin inhibitors in Alzheimer's disease. Biomed Pharmacother 48:296-304.
23. Houenou LJ, Turner PL, Li L, Oppenheim RW, Festoff BW (1995) A serine protease inhibitor, protease nexin 1, rescues motoneurons from naturally occurring and axotomy-induced cell death. Proc Natl Acad Sci USA 92:895-899.
24. Ishii K, Hein L, Kobilka B, Coughlin SR (1993) Kinetics of thrombin receptor cleavage on intact cells. Relation to signaling. J Biol Chem 268:9780-9786.
25. Oppenheim RW (1991) Cell death during development of the nervous system. Annu Rev Neurosci 14:453-501.
26. Perraud F, Besnard F, Sensenbrenner M, Labourdette G (1987) Thrombin is a potent mitogen for rat astroblasts but not for oligodendroblasts and neuroblasts in primary culture. Int J Dev Neurosci 5:181-188.
27. Rao JS, Rayford A, Mortantz RA, Festoff BW, Sawaya R (1993) Increased levels of plasminogen activator inhibitor-1 (PA-1) in human brain tumors. J Neuro-Oncol 17:215:221.
28. Reinhard E, Suidan HS, Pavlik A, Monard D (1994) Glia-derived nexin/ protease nexin-1 is expressed by a subset of neurons in the rat brain. J Neurosci Res 37:256-270.
29. Robinson DG, Ehlers U, Herken R, Herrmann B, Mayer F, Shürmann F-W (1987) Methods of preparation for electron microscopy. New York: Springer.
30. Salcedo RM, Festoff BW, Citron BA (1998) Quantitative reversetranscription PCR to gauge increased protease-activated receptor 1 (PAR-1) mRNA copy numbers in the wobbler mutant mouse. J Mol Neurosci, in press.
31. Seiler SM, Michel IM, Fenton II JW (1992) Involvement of the "tethered-ligand" receptor in thrombin inhibition of platelet adenylate cyclase. Biochem Res Commun 182:1296-1302.
32. Shea TB (1995) Inhibition of neuronal surface proteases decreases the requirement for GAP-43 in neurite outgrowth. Dev Brain Res 87:87-90.
33. Shea TB, Cressman CM, Spencer MJ, Beerman ML, Nixon RA (1995) Enhancement of neurite outgrowth following calpain inhibition is mediated by protein kinase C. J Neurochem 65:517-527.
34. Siman R, Noszek JC, Kegerise C (1989) Calpain I activation is specifically related to excitatory amino acid induction of hippocampal damage. J Neurosci 9:1579-1590.
35. Smirnova IV, Ho GJ, Fenton II JW, Festoff BW (1994) Extravascular proteolysis and the nervous system: serine protease/serpin balance. Semin Thromb Hemost 20:426-432.
36. Smirnova IV, Zhang SX, Citron BA, Arnold PM, Festoff BW (1998a) Thrombin is a death signal that activates intracellular death protease pathways in motor neurons. J Neurobiol, in press.
37. Smirnova IV, Vamos S, Wiegmann T, Citron BA, Arnold PM, Festoff BW (1998b) Calcium mobilization and protease-activated receptor cleavage after thrombin stimulation in motor neurons. J Mol Neurosci, in press.
38. 2+ homeostasis and sensitivity to glucose deprivation-induced injury. J Neurosci 15:5840-5850.
39. Smith-Swintowsky VL, Cheo-Isaacs CT, D'Andrea MR, Santulli RJ, Darrow AL, Andrade-Gordon P (1997) Protease-activated receptor-2 (PAR-2) is present in the rat hippocampus and is associated with neurodegeneration. J Neurochem 69:1890-1896.
40. Stefanis L, Park DS, Yan CYI, Farinelli SE, Troy CM, Shelanski ML, Greene LA (1996) Induction of CPP32 like activity in PC12 cells by withdrawal of trophic support: dissociation from apoptosis. J Biol Chem 271:30663-30671.
41. Stefanis L, Troy CM, Haiqing Q, Greene LA (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.
42. Stone SR, Hofsteenge J (1986) Kinetics of the inhibition of thrombin by hirudin. Biochemistry 25:4622-4628.
43. Struss D, Storck J, Zimmerman RE (1992) The inhibition of thrombin and chymotrypsin by heparin-cofactor III. Thomb Res 68:45-56.
44. 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.
45. Swash M, Schwartz MS (1992) What do we really know about amyotrophic lateral sclerosis? J Neural Sci 113:4-16.
46. Tanaka H, Agata A, Obata K (1989) A new membrane antigen revealed by monoclonal antibodies is associated with motoneuron axonal pathways. Dev Biol 132:419-435.
47. Tanaka H, Matsui T, Agata A, Tomura M, Kubota I, McFarland KC, Kohr B, Lee A, Phillips HS, Shelton DL (1991) Molecular cloning and expression of a novel adhesion molecule, SCI. Neuron 7:535-545.
48. Tsirka SE, Gualandris A, Amaral DG, Strickland S (1995) Excitotoxin-induced neuronal degeneration and seizure are mediated by tissue plasminogen activator. Nature 377:340-344.
49. 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.
50. Vaughan PJ, Cunningham DD (1993) Regulation of protease nexin-1 synthesis and secretion in cultured brain cells by injury-related factors. J Biol Chem 268:3720-3727.
51. Vaughan PJ, Pike CJ, Cotman CW, Cunningham DD (1995) Thrombin receptor activation protects neurons and astrocytes from cell death produced by environmental insults. J Neurosci 15:5389-5401.
52. 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.
53. Wagner SL, Geddes JW, Cotman CW, Lau AL, Gurwitz D, Jackson PJ, Cunningham DD (1989) Protease nexin-1, an antithrombin with neurite outgrowth activity, is reduced in Alzheimer's disease. Proc Natl Acad Sci USA 86:8284-8288.
54. Walz DA, Anderson GF, Ciaglowski RE, Aiken M, Fenton II JW (1985) Thrombin-elicited contractile responses of aortic smooth muscle. Proc Soc Exp Biol Med 180:518-526.
55. Weinstein JR, Gold SJ, Cunningham DD, Gall CM (1995) Cellular localization of thrombin receptor mRNA in rat brain: expression by mesencephalic dopaminergic neurons and codistribution with prothrombin mRNA. J Neurosci 15:2906-2919.
56. Wijsman JH, Jonker RR, Keizer R, van de Velde CJ, Cornellisse CJ, van Dierendonck JH (1993) A new method to detect apoptosis in paraffin sections: in situ end-labeling of fragmented DNA. J Histochem Cytochem 41:7-12.
57. Wyllie AH (1981) Cell death: a new classification separating apoptosis from necrosis. In: Cell death in biology and pathology (Bowen ID, Lockstein RA, eds), pp 9-34. New York: Chapman and Hall.
58. Yanagihara Y, Brengman JM, Mushynski WE (1990) Differential vulnerability of microtubule components in cerebral ischemia. Acta Neuropathol (Berl) 80:499-505.
59. Zurn AD, Nick H, Monard D (1988) A glia-derived nexin promotes neurite outgrowth in cultured chick sympathetic neurons. Dev Neurosci 10:17-24.