Cell-surface actin binds plasminogen and modulates neurotransmitter release from catecholaminergic cells

Journal of Neuroscience

Volumn 26, Issue 50, 2006, Pages 13017-13024

  Miles, Lindsey A ^a   Andronicos, Nicholas M ^a   Baik, Nagyung ^a   Parmer, Robert J ^b  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Actin; Catecholamine; Chromaffin cell; Nicotinic; Plasminogen; Release

Indexed keywords

ACTIN; BETA ACTIN; CARBOXYPEPTIDASE B; HORMONE PRECURSOR; LYSINE DERIVATIVE; MONOCLONAL ANTIBODY; PLASMIN; PLASMINOGEN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CATECHOLAMINE NERVE CELL; CATECHOLAMINE RELEASE; CELL SURFACE; CONTROLLED STUDY; HUMAN; NEUROTRANSMITTER RELEASE; NONHUMAN; PLASMINOGEN ACTIVATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; RADIOASSAY; RAT; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ACTINS; ANIMALS; CATECHOLAMINES; CATTLE; CELL MEMBRANE; CELLS, CULTURED; CHROMAFFIN CELLS; HUMANS; NEUROTRANSMITTER AGENTS; PC12 CELLS; PLASMINOGEN; PLASMINOGEN ACTIVATORS; PROTEIN BINDING; RATS;

EID: 33845612415     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2070-06.2006     Document Type: Article

References (64)

1. Andronicos NM, Ranson M (2001) The topology of plasminogen binding and activation on the surface of human breast cancer cells. Br J Cancer 85:909-916.
2. Bachvaroff RJ, Miller F, Rapaport FT (1980) Appearance of cyoskeletal components on the surface of leukemia cells and of lymphocytes transformed by mitogens and Epstein-Barr virus. J Immunol 131:370-377.
3. Baranes D, Lederfein D, Huang YY, Chen M, Bailey CH, Kandel ER (1998) Tissue plasminogen activator contributes to the late phase of LTP and to synaptic growth in the hippocampal mossy fiber pathway. Neuron 21:813-825.
4. Beebe DP, Miles LA, Plow EF (1989) A linear amino acid sequence involved in the interaction of t-PA with its endothelial cell receptor. Blood 74:2034-2037.
5. Carmeliet P, Schoonjans L, Kieckens L, Ream B, Degen J, Bronson R, De Vos R, Van den Oord JJ, Collen D, Mulligan RC (1994) Physiological consequences of loss of plasminogen activator gene function in mice. Nature 368:419-424.
6. Castellino FJ, McCance SG (1997) The kringle domains of human plasminogen. Ciba Found Symp 212:46-60.
7. Chen-Liu LW, Strickland S (1997) Neuronal death in the hippocampus is promoted by plasmin-catalyzed degradation of laminin. Cell 91:917-925.
8. Colombo B, Longhi R, Marinzi C, Magni F, Cattoretti G, Yoo S-H, Curnis F, Corti A (2002) Cleavage of chromogranin A N-terminal domain by plasmin provides a new mechanism for regulating cell adhesion. J Biol Chem 277:45911-45919.
9. Deutsch DG, Mertz ET (1970) Plasminogen: Purification from human plasma by affinity chromatography. Science 170:1995-1996.
10. Dudani AK, Ganz PR (1996) Endothelial cell surface actin serves as a binding site for plasminogen, tissue plasminogen activator and lipoprotein(a). Br J Haematol 95:168-178.
11. Dudani AK, Ben Tchavtchavadze M, Porter S, Tackaberry E (2005) Angiostatin and plasminogen share binding to endothelial cell surface actin. Biochem Cell Biol 83:28-35.
12. Emerson DL, Arnaud P, Galbraith RM (1983) Evidence of increased Gc: actin complexes in pregnant serum: a possible result of trophoblast embolism. Am J Reprod Immunol 4:185-189.
13. Felez J, Miles LA, Fabregas P, Jardi M, Plow EF, Lijnen RJ (1996) Characterization of cellular binding sites and interactive regions within reactants required for enhancement of plasminogen activation by tPA on the surface of leukocytic cells. Thromb Haemost 76:577-584.
14. Fowler B, Mackman N, Parmer RJ, Miles LA (1998) Binding of human single chain urokinase to Chinese hamster ovary cells and cloning of hamster u-PAR. Thromb Haemost 80:148-154.
15. Frey U, Muller M, Kuhl D (1996) A different form of long-lasting potentiation revealed in tissue plasminogen activator mutant mice. J Neurosci 16:2057-2063.
16. Friedman GC, Seeds NW (1995) Tissue plasminogen activator mRNA expression in granule neurons coincides with their migration in the developing cerebellum. J Comp Neurol 360:658-670.
17. Greene LA, Tischler AS (1976) Establishment of a noradrenergic clonal cell line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci USA 73:2424-2428.
18. Gualandris A, Jones TE, Strickland S, Tsirka SE (1996) Membrane depolarization induces calcium-dependent secretion of tissue plasminogen activator. J Neurol Sci 16:2220-2225.
19. Hao Z, Guo C, Jiang X, Krueger S, Pietri T, Dufour S, Cone RE, O'Rourke J (2006) New transgenic evidence for a system of sympathetic axons able to express tissue plasminogen activator (t-PA) within arterial/arteriolar walls. Blood 108:200-202.
20. Hawley SB, Green MA, Miles LA (2000) Discriminating between cell surface and intracellular plasminogen- binding proteins: heterogeneity in profibrinolytic plasminogen-binding proteins on monocytoid cells. Thromb Haemost 84:882-890.
21. Hawley SB, Tamura T, Miles LA (2001) Purification, cloning, and characterization of a profibrinolytic plasminogen-binding protein, TIP49a. J Biol Chem 276:179-186.
22. Herschman HR, Ferguson GD, Feldman JD, Farias-Eisner R, Vician L (2000) Searching for depolarization-induced genes that modulate synaptic plasticity and neurotrophin-induced genes that mediate neuronal differentiation. Neurochem Res 25:591-602.
23. Hoover-Plow J, Skomorovska-Prokvolit O, Welsh S (2001) Selective behaviors altered in plasminogen-deficient mice are reconstituted with intracerebroventricular injection of plasminogen. Brain Res 898:256-264.
24. Huang YY, Bach ME, Lipp HP, Zhuo M, Wolfer DP, Hawkins RD, Schoonjans L, Kandel ER, Godfraind JM, Mulligan R, Collen D, Carmeliet P (1996) Mice lacking the gene encoding tissue-type plasminogen activator show a selective interference with late-phase long-term potentiation in both Schaffer collateral and mossy fiber pathways. Proc Natl Acad Sci USA 93:8699-8704.
25. Jacobson GR, Rosenbusch JP (1976) ATP binding to a protease-resistant core of actin. Proc Natl Acad Sci USA 73:2742-2746.
26. Jiang Q, Taupenot L, Mahata SK, Mahata M, O'Connor DT, Miles LA, Parmer RJ (2001) Proteolytic cleavage of chromogranin A (CgA) by plasmin. Selective liberation of a specific bioactive CgA fragment that regulates catecholamine release. J Biol Chem 276:25022-25029.
27. Jiang Q, Yasothornsrikul S, Taupenot L, Miles LA, Parmer RJ (2002) The local chromaffin cell plasminogen/plasmin system and the regulation of catecholamine secretion. Ann NY Acad Sci 971:445-449.
28. Jiang X, Wang Y, Hand AR, Gillies C, Cone RE, Kirk J, O'Rourke J (2002) Storage and release of tissue plasminogen activator by sympathetic axons in resistance vessel walls. Microvasc Res 64:438-447.
29. Kabsch W, Vandekerckhove J (1992) Structure and function of actin. Annu Rev Biophys Biomol Struct 21:49-76.
30. Laemmli UK (1970) Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227:680-685.
31. Lind SE, Smith CJ (1991) Actin accelerates plasmin generation by tissue plasminogen activator. J Biol Chem 266:17673-17678.
32. Lind SE, Smith CJ (1993) Actin stimulates plasmin generation by tissue and urokinase-type plasminogen activators. Arch Biochem Biophys 307:138-145.
33. Markus G, De Pasquale JL, Wissler FC (1978) Quantitative determination of the binding of epsilon-aminocaproic acid to native plasminogen. J Biol Chem 253:727-732.
34. Mejean C, Roustan C, Benyamin Y (1987) Anti-actin antibodies. Detection and quantitation of total and skeletal muscle actin in human plasma using a competitive ELISA. J Immunol Methods 99:129-135.
35. Miles LA, Hawley SB, Parmer RJ (2002) Chromaffin cell plasminogen receptors. Ann NY Acad Sci 971:454-459.
36. Mornet D, Bertrand R, Pantel P, Audemard E, Kassab R (1981) Structure of the actin-myosin interface. Nature 292:301-306.
37. Moroianu J, Fett JW, Riordan JF, Vallee BL (1993) Actin is a surface component of calf pulmonary artery endothelial cells in culture. Proc Natl Acad Sci USA 90:3815-3819.
38. Muench MO, Ratcliffe JV, Nakanishi M, Ishimoto H, Jaffe RB (2003) Isolation of definitive zone and chromaffin cells based upon expression of CD56 (neural cell adhesion molecule) in the human fetal adrenal gland. J Clin Endocrinol Metab 88:3921-3930.
39. Muesch A, Hartmann E, Rohde K, Rubartelli A, Sitia R, Rapoport TA (1990) A novel pathway for secretory proteins ? Trends Biochem Sci 15:86-88.
40. Muhlrad A, Kudryashov D, Michael PY, Bobkov AA, Almo SC, Reisler E (2004) Cofilin induced conformational changes in F-actin expose subdomain 2 to proteolysis. J Mol Biol 342:1559-1567.
41. Owen MJ, Auger J, Barber BH, Edwards AJ, Walsh FS, Crumpton MJ (1978) Actin may be present on the lymphocyte surface. Proc Natl Acad Sci USA 75:4484-4488.
42. Pang PT, Teng HK, Zaitsev E, Woo NT, Sakata K, Zhen S, Teng KK, Yung WH, Hempstead BL, Lu B (2004) Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity. Science 306:487-491.
43. Parmer RJ, Miles LA (1998) Targeting of tissue plasminogen activator to the regulated pathway of secretion. Trends Cardiovasc Med 8:306-312.
44. Parmer RJ, Xi X-P, Wu H-J, Helman LJ, Petz LN (1993) Secretory Protein Traffic. Chromogranin A contains a dominant signal for the regulated pathway. J Clin Invest 92:1042-1054.
45. Parmer RJ, Mahata M, Mahata S, Sebald MT, O'Connor DT, Miles LA (1997) Tissue plasminogen activator (t-PA) is targeted to the regulated secretory pathway: Catecholamine storage vesicles as a reservoir for the rapid release of t-PA. J Biol Chem 272:1976-1982.
46. Parmer RJ, Mahata M, Gong Y, Mahata S, Jiang Q, O'Connor DT, Xi X-P, Miles LA (2000) Processing of chromogranin A by plasmin provides a novel mechanism for regulating catecholamine secretioin. J Clin Invest 106:907-915.
47. Pittman RN, Ivins JK, Buettner HM (1989) Neuronal plasminogen activators: Cell surface binding sites and involvement in neurite outgrowth. J Neurosci 9:4269-4286.
48. Qian Z, Gilbert ME, Colicos MA, Kandel ER, Kuhl D (1993) Tissue-type plasminogen activator is induced as an immediate-early gene during seizure, kindling and long-term potentiation. Nature 361:453-457.
49. Ranson M, Andronicos NM, O'Mullane MJ, Baker MS (1998) Increased plasminogen binding is associated with metastatic breast cancer cells: differential expression of plasminogen binding proteins. Br J Cancer 77:1586-1597.
50. Rubenstein P, Ruppert T, Sandra A (1982) Selective isoactin release from cultured embryonic skeletal muscle cells. J Cell Biol 92:164-169.
51. Salles FJ, Strickland S (2002) Localization and regulation of the tissue plasminogen activator-plasmin system in the hippocampus. J Neurosci 22:2125-2134.
52. Sanders SK, Craig SW (1983) A lymphocyte cell surface molecule that is antigenically related to actin. J Immunol 131:370-377.
53. Sappino A-P, Madani R, huarte J, Belin D, Kiss JZ, Wohlwend A, Vassalli J-D (1993) Extracellular proteolysis in the adult murine brain. J Clin Invest 92:679-685.
54. Seeds NW, Basham ME, Ferguson JE (2003) Absence of tissue plasminogen activator gene or activity impairs mouse cerebellar motor learning. J Neurosci 23:7368-7375.
55. Thorstensson R, Utter G, Norberg R (1982) Further characterization of the Ca2+-dependent F-actin-depolymerizing protein of human serum. Eur J Biochem 126:11-16.
56. Tsirka SE, Rogove AD, Strickland S (1996) Neuronal cell death and tPA. Nature 384:123-124.
57. Tsirka SE, Rogove AD, Bugge TH, Degen JL, Strickland S (1997a) An extracellular proteolytic cascade promotes neuronal degeneration in the mouse hippocampus. J Neurosci 17:543-552.
58. Tsirka SE, Bugge TH, Degen JL, Strickland S (1997b) Neuronal death in the central nervous system demonstrates a non-fibrin substrate for plasmin. Proc Natl Acad Sci USA 94:9779-9781.
59. Violand BN, Sodetz JM, Castellino FJ (1975) The effect of epsilon-amino caproic acid on the gross conformation of plasminogen and plasmin. Arch Biochem Biophys 170:300-305.
60. Waller A, Pipkorn D, Sutton KL, Linderman JJ, Omann GM (2001) Validation of flow cytometric competitive binding protocols and characterization of fluorescently labeled ligands. Cytometry 45:102-114.
61. Wang H, Schultz R, Hong J, Cundiff DL, Jiang K, Soff GA (2004) Cell surface-dependent generation of angiostatin4.5. Cancer Res 64:162-168.
62. Wang H, Doll JA, Jiang K, Cundiff DL, Czarnecki JS, Wilson M, Ridge KM, Soff GA (2006) Differential binding of plasminogen, plasmin, and angiostatin4.5 to cell surface beta-actin: implications for cancer-mediated angiogenesis. Cancer Res 66:7211-7215.
63. Wang N, Zhang L, Miles L, Hoover-Plow J (2004) Plasminogen regulates pro-opiomelanocortin processing. J Thromb Haemost 2:785-796.
64. Zhang L, Seiffert D, Fowler BJ, Jenkins GR, Thinnes TC, Loskutoff DJ, Parmer RJ, Miles LA (2002) Plasminogen has a broad extrahepatic distribution. Thromb Haemost 87:493-501.