Apoptosis of human endothelial cells is accompanied by proteolytic processing of latent TGF-β binding proteins and activation of the TGF-β

Cell Death and Differentiation

Volumn 12, Issue 7, 2005, Pages 815-826

  Solovyan, Victor T ^a   Keski Oja, J ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Anoikis; Cell matrix interactions; Endothelial cell; Extracellular matrix; LTBP; Programmed cell death; Staurosporine

Indexed keywords

BINDING PROTEIN; LATENCY ASSOCIATED PEPTIDE; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA BINDING PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL LINE; CELL PROTECTION; CONTROLLED STUDY; EMBRYO; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; FEEDBACK SYSTEM; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN SECRETION; PROTEIN TARGETING;

ANOIKIS; APOPTOSIS; CASPASES; CELLS, CULTURED; CULTURE MEDIA, CONDITIONED; CYSTEINE PROTEINASE INHIBITORS; DNA-BINDING PROTEINS; ENDOTHELIAL CELLS; EXTRACELLULAR MATRIX; GENES, REPORTER; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LATENT TGF-BETA BINDING PROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; SMAD PROTEINS; STAUROSPORINE; TRANS-ACTIVATORS; TRANSFORMING GROWTH FACTOR BETA;

EID: 21744437609     PISSN: 13509047     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.cdd.4401618     Document Type: Article

References (53)

1. Webb SJ, Harrison DJ and Wyllie AH (1997) Apoptosis: an overview of the process and its relevance in disease. Adv. Pharmacol. 41: 1-34
2. Earnshaw WC, Martins LM and Kaufmann SH (1999) Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu. Rev. Biochem. 68: 383-424
3. Nagata S (2000) Apoptotic DNA fragmentation. Exp. Cell Res. 256: 12-18
4. Pollman MJ, Naumovski L and Gibbons GH (1999) Vascular cell apoptosis: cell type-specific modulation by transforming growth factor-β1 in endothelial cells versus smooth muscle cells. Circulation 99: 2019-2026
5. Hyman KM, Seghezzi G, Pintucci G, Stellari G, Kim JH, Grossi EA, Galloway AC and Mignatti P (2002) Transforming growth factor-β1 induces apoptosis in vascular endothelial cells by activation of mitogen-activated protein kinase. Surgery 132: 173-179
6. Emmanuel C, Foo E, Medbury HJ, Matthews J, Comis A and Zoellner H (2002) Synergistic induction of apoptosis in human endothelial cells by tumour necrosis factor-α and transforming growth factor-β. Cytokine 18: 237-241
7. Ackermann EJ, Taylor JK, Narayana R and Bennett CF (1999) The role of antiapoptotic Bcl-2 family members in endothelial apoptosis elucidated with antisense oligonucleotides. J. Biol. Chem. 274: 11245-11252
8. Stoneman VE and Bennett MR (2004) Role of apoptosis in atherosclerosis and its therapeutic implications. Clin. Sci. 107: 343-354
9. Chavakis E and Dimmeler S (2002) Regulation of endothelial cell survival and apoptosis during angiogenesis. Arterioscler. Thromb. Vasc. Biol. 22: 887-893
10. Annes JP, Munger JS and Rifkin DB (2003) Making sense of latent TGF-β activation. J. Cell Sci. 116: 217-224
11. Taipale J, Saharinen J and Keski-Oja J (1998) Extracellular matrix-associated transforming growth factor-β: role in cancer cell growth and invasion. Adv. Cancer Res. 75: 87-134
12. Kanzaki T., Olofsson A, Moren A, Wernstedt C, Hellman U, Miyazono K, Claesson-Welsh L and Heldin CH (1990) TGF-β1 binding protein: a component of the large latent complex of TGF-β1 with multiple repeat sequences. Cell 61: 1051-1061
13. Saharinen J, Hyytiänen M, Taipale J and Keski-Oja J (1999) Latent transforming growth factor-β binding proteins (LTBPs) - structural extracellular matrix proteins for targeting TGF-β action. Cytokine Growth Factor Rev. 10: 99-117
14. Taipale J, Miyazono K, Heldin CH and Keski-Oja J (1994) Latent transforming growth factor-β associates to fibroblast extracellular matrix via latent TGF-β binding protein. J. Cell Biol. 124: 171-181
15. Koli K, Saharinen J, Hyytiäinen M, Penttinen C and Keski-Oja J (2001) Latency, activation, and binding proteins of TGF-β. Microsc. Res. Tech. 52: 354-362
16. Schultz-Cherry S and Murphy-Ullrich JE (1993) Thrombospondin causes activation of latent transforming growth factor-β secreted by endothelial cells by a novel mechanism. J. Cell Biol. 122: 923-932
17. 6 binds and activates latent TGF-β1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell 96: 319-328
18. 6-mediated activation of latent TGF-β requires the latent TGF-β binding protein-1. J. Cell Biol. 165: 723-734
19. Lyons RM, Keski-Oja J and Moses HL (1988) Proteolytic activation of latent transforming growth factor-β from fibroblast-conditioned medium. J. Cell Biol. 106: 1659-1665
20. Sato Y and Rifkin DB (1989) Inhibition of endothelial cell movement by pericytes and smooth muscle cells: activation of a latent transforming growth factor-β1-like molecule by plasmin during co-culture. J. Cell Biol. 109: 309-315
21. Karsdal MA, Larsen L, Engsig MT, Lou H, Ferreras M, Lochter A, Delaisse JM and Foged NT (2002) Matrix metalloproteinase-dependent activation of latent transforming growth factor-β controls the conversion of osteoblasts into osteocytes by blocking osteoblast apoptosis. J. Biol. Chem. 277: 44061-44067
22. Yu Q and Stamenkovic I (2000) Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-β and promotes tumor invasion and angiogenesis. Genes Dev. 14: 163-176
23. Guo M, Mathieu PA, Linebaugh B, Sloane BF and Reiners JJJr (2002) Phorbol ester activation of a proteolytic cascade capable of activating latent transforming growth factor-β: a process initiated by the exocytosis of cathepsin B. J. Biol. Chem. 277: 14829-14837
24. Taipale J, Lohi J, Saarinen J, Kovanen PT and Keski-Oja J (1995) Human mast cell chymase and leukocyte elastase release latent transforming growth factor-β1 from the extracellular matrix of cultured human epithelial and endothelial cells. J. Biol. Chem. 270: 4689-4696
25. Abe M, Harpel JG, Metz CN, Nunes I, Loskutoff DJ and Rifkin DB (1994) An assay for transforming growth factor-β using cells transfected with a plasminogen activator inhibitor-1 promoter-luciferase construct. Anal. Biochem. 216: 276-284
26. Guimond A, Sulea T, Pen A, Ear P and O'Connor-McCourt MD (2002) Site-directed mutagenesis of the type II TGF-β receptor indicates a ligand-binding site distinct from that of the type II activin receptor. FEBS Lett. 515: 13-19
27. Blobe GC, Schiemann WP and Lodish HF (2000) Role of transforming growth factor-β in human disease. New Engl. J. Med. 342: 1350-1358
28. Teder P, Vandivier RW, Jiang D, Liang J, Cohn L, Pure E, Henson PM and Noble PW (2002) Resolution of lung inflammation by CD44. Science 296: 155-158
29. Huynh ML, Fadok VA and Henson PM (2002) Phosphatidylserine-dependent ingestion of apoptotic cells promotes TGF-β1 secretion and the resolution of inflammation. J. Clin. Invest. 109: 41-50
30. Lawrence T, Gilroy DW, Colville-Nash PR and Willoughby DA (2001) Possible new role for NF-κB in the resolution of inflammation. Nat. Med. 7: 1291-1297
31. Ewan KB, Henshall-Powell RL, Ravani SA, Pajares MJ, Arteaga C, Warters R, Akhurst RJ and Barcellos-Hoff MH (2002) Transforming growth factor-β1 mediates cellular response to DNA damage in situ. Cancer Res. 62: 5627-5631
32. Hodge S, Hodge G, Flower R, Reynolds PN, Scicchitano R and Holmes M (2002) Up-regulation of production of TGF-β and IL-4 and down-regulation of IL-6 by apoptotic human bronchial epithelial cells. Immunol. Cell Biol. 80: 537-543
33. Chen W, Jin W, Tian H, Sicurello P, Frank M, Orenstein JM and Wahl SM (2001) Requirement for transforming growth factor-β1 in controlling T cell apoptosis. J. Exp. Med. 194: 439-453
34. Brionne T, Tesseur CI, Masliah E and Wyss-Coray T (2003) Loss of TGF-β1 leads to increased neuronal cell death and microgliosis in mouse brain. Neuron 40: 1133-1145
35. Krieglstein K, Richter S, Farkas L, Schuster N, Dunker N, Oppenheim RW and Unsicker K (2000) Reduction of endogenous transforming growth factors-β prevents ontogenetic neuron death. Nat. Neurosci. 3: 1085-1090
36. Dai C, Yang J and Liu Y (2003) Transforming growth factor-β1 potentiates renal tubular epithelial cell death by a mechanism independent of smad signalling. J. Biol. Chem. 278: 12537-12545
37. Barna G, Sebestyen A, Chinopoulos CC, Nagy K, Mihalik R, Paku S and Kopper L (2002) TGF-β1 kills lymphoma cells using mitochondrial apoptotic pathway with the help of caspase-8. Anticancer Res. 22: 3867-3872
38. Ramachandra M, Atencio I, Rahman A, Vaillancourt M, Zou A, Avanzini J, Wills K, Bookstein R and Shabram P (2002) Restoration of transforming growth factor-β signalling by functional expression of smad4 induces anoikis. Cancer Res. 62: 6045-6051
39. Valderrama-Carvajal H, Cocolakis E, Lacerte A, Lee EH, Krystal G, Ali S and Lebrun JJ (2002) Activin/TGF-β induce apoptosis through Smad-dependent expression of the lipid phosphatase SHIP. Nat. Cell Biol. 4: 963-969
40. Zhu Y, Yang GY, Ahlemeyer B, Pang L, Che XM, Culmsee C, Klumpp S and Krieglstein J (2002) Transforming growth factor-β1 increases bad phosphorylation and protects neurons against damage. J. Neurosci. 22: 3898-3909
41. Rosen K, Coll ML, Li A and Filmus J (2001) Transforming growth factor-α prevents detachment-induced inhibition of c-Src kinase activity, Bcl-XL downregulation, and apoptosis of intestinal epithelial cells. J. Biol. Chem. 276: 37273-37279
42. Saharinen J and Keski-Oja J (2000) Specific sequence motif of 8-Cys repeats of TGF-β binding proteins, LTBPs, creates a hydrophobic interaction surface for binding of small latent TGF-β. Mol. Biol. Cell 11: 2691-2704
43. Ryoo HD, Gorenc T and Steller H (2004) Apoptotic cells can induce compensatory cell proliferation through the JNK and the Wingless signalling pathways. Dev. Cell. 7: 491-501
44. Koli K, Wempe F, Sterner-Kock A, Kantola A, Komor M, Hofmann WK, von Melchner H and Keski-Oja J (2004) Disruption of LTBP-4 function reduces TGF-β activation and enhances BMP-4 signaling in the lung. J. Cell Biol. 167: 123-133
45. Miyazono K, Olofsson A, Colosetti P and Heldin CH (1991) A role of the latent TGF-β1-binding protein in the assembly and secretion of TGF-β1. EMBO J. 10: 1091-1101
46. Dallas SL, Rosser JL, Mundy GR and Bonewald LF (2002) Proteolysis of latent transforming growth factor-β (TGF-β)-binding protein-1 by osteoclasts. A cellular mechanism for release of TGF-β from bone matrix. J. Biol. Chem. 277: 21352-21360
47. Persson U, Izumi H, Souchelnytskyi S, Itoh S, Grimsby S, Engstrom U, Heldin CH, Funa K and ten Dijke P (1998) The L45 loop in type I receptors for TGF-β family members is a critical determinant in specifying Smad isoform activation. FEBS Lett. 434: 83-87
48. Hedman K, Kurkinen M., Alitalo K, Vaheri A, Johansson S and Höök M (1979) Isolation of the pericellular matrix of human fibroblast cultures. J. Cell Biol. 81: 83-91
49. Brunetti M, Martelli N, Manarini S, Mascetra N, Musiani P, Cerletti C, Aiello FB and Evangelista V (2000) Polymorphonuclear leukocyte apoptosis is inhibited by platelet-released mediators, role of TGF-β1. Thromb. Haemost. 84: 478-483
50. Schlapbach R, Spanaus KS, Malipiero U, Lens S, Tasinato A, Tschopp J and Fontana A (2000) TGF-β1 induces the expression of the FLICE-inhibitory protein and inhibits Fas-mediated apoptosis of microglia. Eur. J. Immunol. 30: 3680-3688
51. Saile B, Matthes NE, Armouche H, Neubauer K and Ramadori G (2001) The bcl, NFkappaB and p53/p21WAF1 systems are involved in spontaneous apoptosis and in the anti-apoptotic effect of TGF-β or TNF-α on activated hepatic stellate cells. Eur. J. Cell Biol. 80: 554-561
52. Shin I, Bakin AV, Rodeck U, Brunet A and Arteaga CL (2001) Transforming growth factor β enhances epithelial cell survival via Akt-dependent regulation of FKHRL1. Mol. Biol. Cell. 12: 3328-3339
53. Chua CC, Chua BH, Chen Z, Landy C and Hamdy RC (2002) TGF-β1 inhibits multiple caspases induced by TNF-α in murine osteoblastic MC3T3-E1 cells. Biochim. Biophys. Acta 1593: 1-8