Activation of ERK signaling upon alternative protease nexin-1 internalization mediated by syndecan-1

Journal of Cellular Biochemistry

Volumn 99, Issue 3, 2006, Pages 936-951

  Li, Xiaobiao ^a   Herz, Joachim ^b   Monard, Denis ^a  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

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

Author keywords

ERK signaling; Internalization; LRP1; PN 1; Syndecan 1

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; LIPOPROTEIN RECEPTOR RELATED PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEASE NEXIN I; PROTEOHEPARAN SULFATE; RAS PROTEIN; SERINE PROTEINASE INHIBITOR; SYNDECAN 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVATION; ENZYME MECHANISM; GENE OVEREXPRESSION; INTERNALIZATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEOGLYCAN SYNTHESIS; RNA INTERFERENCE; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION;

AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBROBLASTS; HEPARAN SULFATE PROTEOGLYCANS; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE; MICE, KNOCKOUT; PROTEASE NEXINS; RAS PROTEINS; RECEPTORS, CELL SURFACE; RECEPTORS, LDL; RNA, SMALL INTERFERING; SERPIN E2; SYNDECAN-1; THROMBIN; TUMOR SUPPRESSOR PROTEINS;

EID: 33749495693     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.20881     Document Type: Article

References (74)

1. Al Haideri M, Goldberg IJ, Galeano NF, Gleeson A, Vogel T, Gorecki M, Sturley SL, Deckelbaum RJ. 1997. Heparan sulfate proteoglycan-mediated uptake of apolipoprotein E-triglyceride-rich lipoprotein particles: A major pathway at physiological particle concentrations. Biochemistry 36:12766-12772.
2. Baker JB, Low DA, Simmer RL, Cunningham DD. 1980. Protease-nexin: A cellular component that links thrombin and plasminogen activator and mediates their binding to cells. Cell 21:37-45.
3. Barbareschi M, Maisonneuve P, Aldovini D, Cangi MG, Pecciarini L, Angelo MF, Veronese S, Caffo O, Lucenti A, Palma PD, Galligioni E, Doglioni C. 2003. High syndecan-1 expression in breast carcinoma is related to an aggressive phenotype and to poorer prognosis. Cancer 98:474-483.
4. Beauvais DM, Rapraeger AC. 2003. Syndecan-1-mediated cell spreading requires signaling by alphavbeta3 integrins in human breast carcinoma cells. Exp Cell Res 286:219-232.
5. Beauvais DM, Burbach BJ, Rapraeger AC. 2004. The syndecan-1 ectodomain regulates alphavbeta3 integrin activity in human mammary carcinoma cells. J Cell Biol 167:171-181.
6. Beisiegel U, Weber W, Bengtsson-Olivecrona G. 1991. Lipoprotein lipase enhances the binding of chylomicrons to low density lipoprotein receptor-related protein. Proc Natl Acad Sci USA 88:8342-8346.
7. Bernfield M, Gotte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J, Zako M. 1999. Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 68:729-777.
8. Bleuel A, Monard D. 1995. Regulation of protease nexin-1 and angiotensin II receptor subtype 1 expression: Inverse relationship in experimental models of nerve injury. J Neurosci Res 42:562-57 0.
9. Bornfeldt KE, Krebs EG. 1999. Crosstalk between protein kinase A and growth factor receptor signaling pathways in arterial smooth muscle. Cell Signal 11:465-477.
10. Bouton MC, Richard B, Rossignol P, Philippe M, Guillin MC, Michel JB, Jandrot-Perrus M. 2003. The serpin protease-nexin 1 is present in rat aortic smooth muscle cells and is upregulated in L-NAME hypertensive rats. Arterioscler Thromb Vasc Biol 23:142-147.
11. Buchholz M, Biebl A, Neebetae A, Wagner M, Iwamura T, Leder G, Adler G, Gress TM. 2003. SERPINE2 (protease nexin I) promotes extracellular matrix production and local invasion of pancreatic tumors in vivo. Cancer Res 63:4945-4951.
12. Carey DJ, Bendt KM, Stahl RC. 1996. The cytoplasmic domain of syndecan-1 is required for cytoskeleton association but not detergent insolubility. Identification of essential cytoplasmic domain residues. J Biol Chem 271:15253-15260.
13. Chen LM, Hodge GB, Guarda LA, Welch JL, Greenberg NM, Chai KX. 2001. Down-regulation of prostasin serine protease: A potential invasion suppressor in prostate cancer. Prostate 48:93-103.
14. Chen LM, Zhang X, Chai KX. 2004. Regulation of prostasin expression and function in the prostate. Prostate 59:1-12.
15. Chen Y, Shi-Wen X, van Beek J, Kennedy L, McLeod M, Renzoni EA, Bou-Gharios G, Wilcox-Adelman S, Goetinck PF, Eastwood M, Black CM, Abraham DJ, Leask A. 2005. Matrix contraction by dermal fibroblasts requires transforming growth factor-{beta}/activin-linked kinase 5, heparan sulfate-containing proteoglycans, and MEK/ERK: Insights into pathological scarring in chronic fibrotic disease. Am J Pathol 167:1699-1711.
16. Conejo JR, Kleeff J, Koliopanos A, Matsuda K, Zhu ZW, Goecke H, Bicheng N, Zimmermann A, Korc M, Friess H, Buchler MW. 2000. Syndecan-1 expression is up-regulated in pancreatic but not in other gastrointestinal cancers. Int J Cancer 88:12-20.
17. Crisp RJ, Knauer DJ, Knauer MF. 2000. Roles of the heparin and low density lipid receptor-related protein-binding sites of protease nexin 1 (PN1) in urokinase-PN1 complex catabolism. The PN1 heparin-binding site mediates complex retention and degradation but not cell surface binding or internalization. J Biol Chem 275:19628-19637.
18. El Shemerly MY, Besser D, Nagasawa M, Nagamine Y. 1997. 12-O-Tetradecanoylphorbol-13-acetate activates the Ras/extracellular signal-regulated kinase (ERK) signaling pathway upstream of SOS involving serine phosphorylation of She in NIH3T3 cells. J Biol Chem 272:30599-30602.
19. Fernandez-Borja M, Bellido D, Vilella E, Olivecrona G, Vilaro S. 1996. Lipoprotein lipase-mediated uptake of lipoprotein in human fibroblasts: Evidence for an LDL receptor-independent internalization pathway. J Lipid Res 37:464-481.
20. Field PA, Gibbons GF. 2000. Decreased hepatic expression of the low-density lipoprotein (LDL) receptor and LDL receptor-related protein in aging rats is associated with delayed clearance of chylomicrons from the circulation. Metabolism 49:492-498.
21. Fuki W, Kuhn KM, Lomazov IR, Rothman VL, Tuszynski GP, Iozzo RV, Swenson TL, Fisher EA, Williams KJ. 1997. The syndecan family of proteoglycans. Novel receptors mediating internalization of atherogenic lipoproteine in vitro. J Clin Invest 100:1611-1622.
22. Fuki IV, Iozzo RV, Williams KJ. 2000a. Perlecan heparan sulfate proteoglycan: A novel receptor that mediates a distinct pathway for ligand catabolism. J Biol Chem 275:25742-25750.
23. Fuki IV, Meyer ME, Williams KJ. 2000b. Transmembrane and cytoplasmic domains of syndecan mediate a multi-step endocytic pathway involving detergent-insoluble membrane rafts. Biochem J 351(Pt 3):607-612.
24. Gilardoni MB, Ceschin DG, Sahores MM, Oviedo M, Gehrau RC, Chiabrando GA. 2003. Decreased expression of the low-density lipoprotein receptor-related protein-1 (LRP-1) in rats with prostate cancer. J Histochem Cytochem 51:1575-1580.
25. Giulietti A, Overbergh L, Valckx D, Decallonne B, Bouillon R, Mathieu C. 2001. An overview of real-time quantitative PCR: Applications to quantify cytokine gene expression. Methods 25:386-401.
26. Goldstein JL, Brown MS. 1977. Atherosclerosis: The low-density lipoprotein receptor hypothesis. Metabolism 26:1257-1275.
27. Goretzki L, Mueller BM. 1997. Receptor-mediated endocytosis of urokinase-type plasminogen activator is regulated by cAMP-dependent protein kinase. J Cell Sci 110(Pt 12):1395-1402.
28. Herndon ME, Stipp CS, Lander AD. 1999. Interactions of neural glycosaminoglycans and proteoglycans with protein ligands: Assessment of selectivity, heterogeneity and the participation of core proteins in binding. Glycobiology 9:143-155.
29. Herz J, Strickland DK. 2001. LRP: A multifunctional scavenger and signaling receptor. J Clin Invest 108:779-784.
30. Herz J, Goldstein JL, Strickland DK, Ho YK, Brown MS. 1991. 39-kDa protein modulates binding of ligands to low density lipoprotein receptor-related protein/alpha 2-macroglobulin receptor. J Biol Chem 266:21232-21238.
31. Howard EW, Knauer DJ. 1986. Biosynthesis of protease nexin-I. J Biol Chem 261:14184-14190.
32. Howard EW, Knauer DJ. 1987. Characterization of the receptor for protease nexin-I: Protease complexes on human fibroblasts. J Cell Physiol 131:276-283.
33. Ito M, Feng J, Tsujino S, Inagaki N, Inagaki M, Tanaka J, Ichikawa K, Hartshorne DJ, Nakano T. 1997. Interaction of smooth muscle myosin phosphatase with phospholipids. Biochemistry 36:7607-7614.
34. Ji ZS, Brecht WJ, Miranda RD, Hussain MM, Innerarity TL, Mahley RW. 1993. Role of heparan sulfate proteoglycans in the binding and uptake of apolipoprotein E-enriched remnant lipoproteine by cultured cells. J Biol Chem 268:10160-10167.
35. Kang DE, Pietrzik CU, Baum L, Chevallier N, Merriam DE, Kounnas MZ, Wagner SL, Troncoso JC, Kawas CH, Katzman R, Koo EH. 2000. Modulation of amyloid beta-protein clearance and Alzheimer's disease susceptibility by the LDL receptor-related protein pathway. J Clin Invest 106:1159-1166.
36. Kesaniemi YA, Witztum JL, Steinbrecher UP. 1983. Receptor-mediated catabolism of low density lipoprotein in man. Quantitation using glucosylated low density lipoprotein. J Clin Invest 71:950-959.
37. Knauer MF, Hawley SB, Knauer DJ. 1997a. Identification of a binding site in protease nexin I (PN1) required for the receptor mediated internalization of PN1-thrombin complexes. J Biol Chem 272:12261-12264.
38. Knauer MF, Kridel SJ, Hawley SB, Knauer DJ. 1997b. The efficient catabolism of thrombin-protease nexin 1 complexes is a synergistic mechanism that requires both the LDL receptor-related protein and cell surface heparins. J Biol Chem 272:29039-29045.
39. Knauer DJ, Majumdar D, Fong PC, Knauer MF. 2000. SERPIN regulation of factor XIa. The novel observation that protease nexin 1 in the presence of heparin is a more potent inhibitor of factor XIa than C1 inhibitor. J Biol Chem 275:37340-37346.
40. Kowal RC, Herz J, Goldstein JL, Esser V, Brown MS. 1989. Low density lipoprotein receptor-related protein mediates uptake of cholesteryl esters derived from apoprotein E-enriched lipoproteins. Proc Natl Acad Sci USA 86:5810-5814.
41. Laprise P, Langlois MJ, Boucher MJ, Jobin C, Rivard N. 2004. Down-regulation of MEK/ERK signaling by E-cadherin-dependent PI3K/Akt pathway in differentiating intestinal epithelial cells. J Cell Physiol 199:32-39.
42. Li Y, van Kerkhof P, Marzolo MP, Strous GJ, Bu G. 2001. Identification of a major cyclic AMP-dependent protein kinase A phosphorylation site within the cytoplasmic tail of the low-density lipoprotein receptor-related protein: Implication for receptor-mediated endocytosis. Mol Cell Biol 21:1185-1195.
43. Llorente A, Prydz K, Sprangers M, Skretting G, Kolset SO, Sandvig K. 2001. Proteoglycan synthesis is increased in cells with impaired clathrin-dependent endocytosis. J Cell Sci 114:335-343.
44. Llorente-Cortes V, Otero-Vinas M, Badimon L. 2002. Differential role of heparan sulfate proteoglycans on aggregated LDL uptake in human vascular smooth muscle cells and mouse embryonic fibroblasts. Arterioscler Thromb Vasc Biol 22:1905-1911.
45. Ma Z, Thomas KS, Webb DJ, Moravec R, Salicioni AM, Mars WM, Gonias SL. 2002. Regulation of Rac1 activation by the low density lipoprotein receptor-related protein. J Cell Biol 159:1061-1070.
46. Makarova A, Mikhailenko I, Bugge TH, List K, Lawrence DA, Strickland DK. 2003. The low density lipoprotein receptor-related protein modulates protease activity in the brain by mediating the cellular internalization of both neuroserpin and neuroserpin-tissue-type plasminogen activator complexes. J Biol Chem 278:50250-50258.
47. Matsuzaki H, Kobayashi H, Yagyu T, Wakahara K, Kondo T, Kurita N, Sekino H, Inagaki K, Suzuki M, Kanayama N, Terao T. 2005. Reduced syndecan-1 expression stimulates heparin-binding growth factor-mediated invasion in ovarian cancer cells in a urokinase-independent mechanism. Oncol Rep 14:449-457.
48. McPherson PS, Kay BK, Hussain NK. 2001. Signaling on the endocytic pathway. Traffic 2:375-384.
49. Meier R, Spreyer P, Ortmann R, Harel A, Monard D. 1989. Induction of glia-derived nexin after lesion of a peripheral nerve. Nature 342:548-550.
50. Monard D. 1993. Tinkering with certain blood components can engender distinct functions in the nervous system. Perspect Dev Neurobiol 1:165-168.
51. Nick H, Hofsteenge J, Shaw E, Rovelli G, Monard D. 1990. Functional sites of glia-derived nexin (GDN): Importance of the site reacting with the protease. Biochemistry 29:2417-2421.
52. Nykjaer A, Willnow TE. 2002. The low-density lipoprotein receptor gene family: A cellular Swiss army knife? Trends Cell Biol 12:273-280.
53. Park PW, Pier GB, Preston MJ, Goldberger O, Fitzgerald ML, Bernfield M. 2000. Syndecan-1 shedding is enhanced by LasA, a secreted virulence factor of Pseudomonas aeruginosa. J Biol Chem 275:3057-3064.
54. Ranganathan S, Liu CX, Migliorini MM, Von Arnim CA, Peltan ID, Mikhailenko I, Hyman BT, Strickland DK. 2004. Serine and threonine phosphorylation of the low density lipoprotein receptor-related protein by protein kinase C alpha regulates endocytosis and association with adaptor molecules. J Biol Chem 279:40536-40544.
55. Rauch BH, Millette E, Kenagy RD, Daum G, Fischer JW, Clowes AW. 2005. Syndecan-4 is required for thrombin-induced migration and proliferation in human vascular smooth muscle cells. J Biol Chem 280:17507-17511.
56. Richard B, Arocas V, Guillin MC, Michel JB, Jandrot-Perrus M, Bouton MC. 2004. Protease nexin-1: A cellular serpin down-regulated by thrombin in rat aortic smooth muscle cells. J Cell Physiol 201:138-145.
57. Roberts MS, Woods AJ, Shaw PE, Norman JC. 2003. ERK1 associates with alpha(v)beta 3 integrin and regulates cell spreading on vitronectin. J Biol Chem 278:1975-1985.
58. Seo T, St Clair RW. 1997. Heparan sulfate proteoglycans mediate internalization and degradation of beta-VLDL and promote cholesterol accumulation by pigeon macrophages. J Lipid Res 38:765-779.
59. Shisheva A, Buxton J, Czech MP. 1994. Differential intracellular localizations of GDP dissociation inhibitor isoforms. Insulin-dependent redistribution of GDP dissociation inhibitor-2 in 3T3-L1 adipocytes. J Biol Chem 269:23865-23868.
60. Shisheva A, Rusin B, Ikonomov OC, DeMarco C, Sbrissa D. 2001. Localization and insulin-regulated relocation of phosphoinositide 5-kinase PIKfyve in 3T3-L1 adipocytes. J Biol Chem 276:11859-11869.
61. Sommer J, Gloor SM, Rovelli GF, Hofsteenge J, Nick H, Meier R, Monard D. 1987. cDNA sequence coding for a rat glia-derived nexin and its homology to members of the serpin superfamily. Biochemistry 26:6407-6410.
62. Sommer J, Meyhack B, Rovelli G, Buergi R, Monard D. 1989. Synthesis of glia-derived nexin in yeast. Gene 85:453-459.
63. Stone SR, Hofsteenge J. 1986. Kinetics of the inhibition of thrombin by hirudin. Biochemistry 25:4622-4628.
64. Stork PJ, Schmitt JM. 2002. Crosstalk between cAMP and MAP kinase signaling in the regulation of cell proliferation. Trends Cell Biol 12:258-266.
65. Takayama Y, May P, Anderson RG, Herz J. 2005. Low density lipoprotein receptor-related protein 1 (LRP1) controls endocytosis and c-CBL-mediated ubiquitination of the platelet-derived growth factor receptor beta (PDGFR beta). J Biol Chem 280:18504-18510.
66. Teis D, Huber LA. 2003. The odd couple: Signal transduction and endocytosis. Cell Mol Life Sci 60:2020-2033.
67. Utani A, Momota Y, Endo H, Kasuya Y, Beck K, Suzuki N, Nomizu M, Shinkai H. 2003. Laminin alpha 3 LG4 module induces matrix metalloproteinase-1 through mitogen-activated protein kinase signaling. J Biol Chem 278:34483-34490.
68. van Der GP. 2002. Phosphorylation of LRP1: Regulation of transport and signal transduction. Trends Cardiovasc Med 12:160-165.
69. Vassiliou G, Stanley KK. 1994. Exogenous receptor-associated protein binds to two distinct sites on human fibroblasts but does not bind to the glycosaminoglycan residues of heparan sulfate proteoglycans. J Biol Chem 269:15172-15178.
70. Viklund L, Loo BM, Hermonen J, El Darwish K, Jalkanen M, Salmivirta M. 2002. Expression and characterization of minican, a recombinant syndecan-1 with extensively truncated core protein. Biochem Biophys Res Commun 290:146-152.
71. Williams KJ, Fless GM, Petrie KA, Snyder ML, Brocia RW, Swenson TL. 1992. Mechanisms by which lipoprotein lipase alters cellular metabolism of lipoprotein(a), low density lipoprotein, and nascent lipoproteins. Roles for low density lipoprotein receptors and heparan sulfate proteoglycans. J Biol Chem 267:13284-13292.
72. Willnow TE, Herz J. 1994. Genetic deficiency in low density lipoprotein receptor-related protein confers cellular resistance to Pseudomonas exotoxin A. Evidence that this protein is required for uptake and degradation of multiple ligands. J Cell Sci 107(Pt 3):719-726.
73. Wilsie LC, Orlando RA. 2003. The low density lipoprotein receptor-related protein complexes with cell surface heparan sulfate proteoglycans to regulate proteoglycan-mediated lipoprotein catabolism. J Biol Chem 278:15758-15764.
74. Zhu Y, Hui DY. 2003. Apolipoprotein E binding to low density lipoprotein receptor-related protein-1 inhibits cell migration via activation of cAMP-dependent protein kinase A. J Biol Chem 278:36257-36263.