Antiapoptotic activities of Bcl-2 correlate with vascular maturation and transcriptional modulation of human endothelial cells

Endothelium: Journal of Endothelial Cell Research

Volumn 15, Issue 1-2, 2008, Pages 59-71

  Enis, David R ^a   Dunmore, Benjamin ^b   Johnson, Nicola ^b   Pober, Jordan S ^a   Print, Cristin G ^c  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Apoptosis; Bcl 2; Endothelial Cell (EC); Vascular Maturation; Vascular Smooth Muscle Cell (VSMC)

Indexed keywords

CASPASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; HYPOCALCIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MATRIX METALLOPROTEINASE 14; OSTEOCALCIN; PROTEIN BCL 2; RNA; SOMATOMEDIN BINDING PROTEIN 2; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTOME; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME;

APOPTOSIS; ARTICLE; CELL MATURATION; CONTROLLED STUDY; ENDOTHELIUM CELL; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; MUTANT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRANSCRIPTION REGULATION; WILD TYPE;

ANIMALS; APOPTOSIS; BLOOD VESSELS; CELL CULTURE TECHNIQUES; CELLS, CULTURED; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, SCID; MODELS, GENETIC; MUSCLE, SMOOTH, VASCULAR; MUTATION; ORGAN CULTURE TECHNIQUES; PROTO-ONCOGENE PROTEINS C-BCL-2; RETROVIRIDAE; TRANSCRIPTION, GENETIC; TRANSDUCTION, GENETIC; TRANSFECTION; TRANSPLANTATION, HETEROLOGOUS; UMBILICAL VEINS;

MUS;

EID: 46049101237     PISSN: 10623329     EISSN: 10292373     Source Type: Journal    
DOI: 10.1080/10623320802092393     Document Type: Article

References (47)

1. Affara, M., Dunmore, B. J., Savoie, S., Imoto, S., Tamada, Y., Araki, H., Charnock-Jones, D. S., Miyano, S. and Print, C. G. (2007) Understanding endothelial cell apoptosis: What can the transcriptome, glycome and proteome reveal?. Philosophical Transactions of the Royal Society B, 362, pp. 1469-1487.
2. Baldi, P. and Long, A. D. (2001) A Bayesian framework for the analysis of microarray expression data: Regularized t-test and statistical inferences of gene changes. Bioinformatics, 17, pp. 509-519.
3. Beissbarth, T. and Speed, T. P. (2004) GOstat: Find statistically overrepresented gene ontologies within a group of genes. Bioinformatics, 20, pp. 1464-1465.
4. Bellas, R. E., Lee, J. S. and Sonenshein, G. E. (1995) Expression of a constitutive NF-kappa B-like activity is essential for proliferation of cultured bovine vascular smooth muscle cells. Journal of Clinical Investigation, 96, pp. 2521-2527.
5. Bostrom, K., Tsao, D., Shen, S., Wang, Y. and Demer, L. L. (2001) Matrix GLA protein modulates differentiation induced by bone morphogenetic protein-2 in C3H10T1/2 cells. Journal of Biological Chemistry, 276, pp. 14044-14052.
6. Cheng, E. H.-Y., Kirsch, D. G., Clem, R. J., Ravi, R., Kastan, M. B., Bedi, A., Ueno, K. and Hardwick, J. M. (1997) Conversion of Bcl-2 to a Bax-like death effector by caspases. Science, 278, pp. 1966-1968.
7. Choi, J., Choi, K., Benveniste, E. N., Hong, Y.-S., Lee, J.-H., Kim, J. and Park, K. (2005) Bcl-2 promotes invasion and lung metastasis by inducing matrix metalloproteinase-2. Cancer Res, 65, pp. 5554-5560.
8. Cory, S. and Adams, J. M. (2005) Killing cancer cells by flipping the Bcl-2/Bax switch. Cancer Cell, 8, pp. 5-6.
9. de Moissac, D., Mustapha, S., Greenberg, A. H. and Kirshenbaum, L. A. (1998) Bcl-2 activates the transcription factor NFkappaB through the degradation of the cytoplasmic inhibitor IkappaBalpha. Journal of Biological Chemistry, 273, pp. 23946-23951.
10. Duval, H., Harris, M., Li, J., Johnson, N. and Print, C. (2003) New insights into the function and regulation of endothelial cell apoptosis. Angiogenesis, 6, pp. 171-183.
11. Duval, H., Johnson, N., Li, J., Evans, A., Chen, S., Licence, D., Skepper, J., Charnock-Jones, D. S., Smith, S. and Print, C. (2007) Vascular development is disrupted by endothelial cell-specific expression of the anti-apoptotic protein Bcl-2. Angiogenesis, 10, pp. 55-68.
12. Enis, D. R., Shepherd, B. R., Wang, Y., Qasim, A., Shanahan, C. M., Weissberg, P. L., Kashgarian, M., Pober, J. S. and Schechner, J. S. (2005) Induction, differentiation, and remodeling of blood vessels after transplantation of Bcl-2-transduced endothelial cells. Proceedings of the National Academy of Sciences of the United States of America, 102, pp. 425-430.
13. Filippov, S., Koenig, G. C., Chun, T. H., Hotary, K. B., Ota, I., Bugge, T. H., Roberts, J. D., Fay, W. P., Birkedal-Hansen, H. Holmbeck, K. et al. (2005) MT1-matrix metalloproteinase directs arterial wall invasion and neointima formation by vascular smooth muscle cells. Journal of Experimental Medicine, 202, pp. 663-671.
14. Gimbrone Jr., M. A. (1976) Culture of vascular endothelium. Progress in Hemostasis and Thrombosis, 3, pp. 1-28.
15. Gross, A., McDonnell, J. M. and Korsmeyer, S. J. (1999) BCL-2 family members and the mitochondria in apoptosis. Genes and Development, 13, pp. 1899-1911.
16. Hsieh, T., Gordon, R. E., Clemmons, D. R., Busby Jr., W. H. and Duan, C. (2003) Regulation of vascular smooth muscle cell responses to insulin-like growth factor (IGF)-I by local IGF-binding proteins. Journal of Biological Chemistry, 278, pp. 42886-42892.
17. Iervolino, A., Trisciuoglio, D., Ribatti, D., Candiloro, A., Biroccio, A., Zupi, G. and Del Bufalo, D. (2002) Bcl-2 overexpression in human melanoma cells increases angiogenesis through VEGF mRNA stabilization and HIF-1-mediated transcriptional activity. FASEB Journal, 16, pp. 1453-1455.
18. Ilan, N., Mahooti, S. and Madri, J. A. (1998) Distinct signal transduction pathways are utilized during the tube formation and survival phases of in vitro angiogenesis. Journal of Cell Science, 111, pp. 3621-3631.
19. Johnson, N. A., Sengupta, S., Saidi, S. A., Lessan, K., Charnock-Jones, S. D., Scott, L., Stephens, R., Freeman, T. C., Tom, B. D. Harris, M. et al. (2004) Endothelial cells preparing to die by apoptosis initiate a program of transcriptome and glycome regulation. FASEB Journal, 18, pp. 188-190.
20. Kahn, J., Mehraban, F., Ingle, G., Xin, X., Bryant, J. E., Vehar, G., Schoenfeld, J., Grimaldi, C. J., Peale, F. Draksharapu, A. et al. (2000) Gene expression profiling in an in vitro model of angiogenesis. American Journal of Pathology, 156, pp. 1887-1900.
21. Karl, E., Warner, K., Zeitlin, B., Kaneko, T., Wurtzel, L., Jin, T., Chang, J., Wang, S., Wang, C. Y. Strieter, R. M. et al. (2005) Bcl-2 acts in a proangiogenic signaling pathway through nuclear factor-kappaB and CXC chemokines. Cancer Research, 65, pp. 5063-5069.
22. Kuwana, T., Mackey, M. R., Perkins, G., Ellisman, M. H., Latterich, M., Schneiter, R., Green, D. R. and Newmeyer, D. D. (2002) Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell, 111, pp. 331-342.
23. Li, C. and Wong, W. H. (2001) Model-based analysis of oligonucleotide arrays: Expression index computation and outlier detection. Proceedings of the National Academy of Sciences of the United States of America, 98, pp. 31-36.
24. Linette, G. P., Li, Y., Roth, K. and Korsmeyer, S. J. (1996) Cross talk between cell death and cell cycle progression: BCL-2 regulates NFAT-mediated activation. Proceedings of the National Academy of Sciences of the United States of America, 93, pp. 9545-9552.
25. Lum, J. J., DeBerardinis, R. J. and Thompson, C. B. (2005) Autophagy in metazoans: Cell survival in the land of plenty. Nature Reviews in Molecular and Cellular Biology, 6, pp. 439-448.
26. Madge, L. A., Sierra-Honigmann, M. R. and Pober, J. S. (1999) Apoptosis-inducing agents cause rapid shedding of tumor necrosis factor receptor 1 (TNFR1). A nonpharmacological explanation for inhibition of TNF-mediated activation. Journal of Biological Chemistry, 274, pp. 13643-13649.
27. Massaad, C. A., Portier, B. P. and Taglialatela, G. (1999) Inhibition of transcription factor activity by nuclear compartment-associated Bcl-2. Journal of Biological Chemistry, 279, pp. 54470-54478.
28. Nor, J. E., Christensen, J., Mooney, D. J. and Polverini, P. J. (1999) Vascular endothelial growth factor (VEGF)-mediated angiogenesis is associated with enhanced endothelial cell survival and induction of Bcl-2 expression. American Journal of Pathology, 154, pp. 375-384.
29. Ohtsu, H., Dempsey, P. J., Frank, G. D., Brailoiu, E., Higuchi, S., Suzuki, H., Nakashima, H., Eguchi, K. and Eguchi, S. (2006) ADAM17 mediates epidermal growth factor receptor transactivation and vascular smooth muscle cell hypertrophy induced by angiotensin II. Arteriosclerosis, Thrombosis, and Vascular Biology, 26, pp. e133-e137.
30. Proudfoot, D. and Shanahan, C. M. (2006) Molecular mechanisms mediating vascular calcification: Role of matrix Gla protein. Nephrology (Carlton), 11, pp. 455-461.
31. Rivard, A., Principle, N. and Andres, V. (2000) Age-dependent increase in c-fos activity and cyclin A expression in vascular smooth muscle cells. A potential link between aging, smooth muscle cell proliferation and atherosclerosis. Cardiovascular Research, 54, pp. 1026-1034.
32. Rosenkilde, M. M. and Schwartz, T. W. (2004) The chemokine system-a major regulator of angiogenesis in health and disease. APMIS, 112, pp. 481-495.
33. Saidi, S. A., Holland, C. M., Kreil, D. P., MacKay, D. J., Charnock-Jones, D. S., Print, C. G. and Smith, S. K. (2004) Independent component analysis of microarray data in the study of endometrial cancer. Oncogene, 23, pp. 6677-6683.
34. Schechner, J. S., Nath, A. K., Zheng, L., Kluger, M. S., Hughes, C. C., Sierra-Honigmann, M. R., Lorber, M. I., Tellides, G., Kashgarian, M. Bothwell, A. L. et al. (2000) In vivo formation of complex microvessels lined by human endothelial cells in an immunodeficient mouse. Proceedings of the National Academy of Sciences of the United States of America, 97, pp. 9191-9196.
35. Strasser, A. (2005) The role of BH3-only proteins in the immune system. Nature Reviews in Immunology, 5, pp. 189-200.
36. Thornton, S. C., Mueller, S. N. and Levine, E. M. (1983) Human endothelial cells: Use of heparin in cloning and long-term serial cultivation. Science, 222, pp. 623-625.
37. Vadigepalli, R., Chakravarthula, P., Zak, D. E., Schwaber, J. S. and Gonye, G. E. (2003) PAINT: A promoter analysis and interaction network generation tool for gene regulatory network identification. OMICS, 7, pp. 235-252.
38. Vailhe, B., Vittet, D. and Feige, J. J. (2001) In vitro models of vasculogenesis and angiogenesis. Laboratory Investigation, 81, pp. 439-452.
39. Vaux, D. L., Cory, S. and Adams, J. M. (1988) Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature, 335, pp. 440-442.
40. Yana, I., Sagara, H., Takaki, S., Takatsu, K., Nakamura, K., Nakao, K., Katsuki, M., Taniguchi, S., Aoki, T. Sato, H. et al. (2007) Crosstalk between neovessels and mural cells directs the site-specific expression of MT1-MMP to endothelial tip cells. Journal of Cell Science, 120, pp. 1607-1614.
41. Yin, X. M., Oltvai, Z. N. and Korsmeyer, S. J. (1994) BH1 and BH2 domains of Bcl-2 are required for inhibition of apoptosis and heterodimerization with Bax. Nature, 369, pp. 321-323.
42. Zuckerbraun, B. S., McCloskey, C. A., Mahidhara, R. S., Kim, P. K., Taylor, B. S. and Tzeng, E. (2003) Overexpression of mutated IkappaBalpha inhibits vascular smooth muscle cell proliferation and intimal hyperplasia formation. Journal of Vascular Surgery, 38, pp. 812-819.
43. Zhang, F., Hackett, N. R., Lam, G., Cheng, J., Pergolizzi, R., Luo, L., Shmelkov, S. V., Edelberg, J., Crystal, R. G. and Rafii, S. (2003) Green fluorescent protein selectively induces HSP70-mediated up-regulation of COX-2 expression in endothelial cells. Blood, 102, pp. 2115-2121.
44. Zheng, L., Ben, L. H., Pober, J. S. and Bothwell, A. L. (2002) Porcine endothelial cells, unlike human endothelial cells, can be killed by human CTL via Fas ligand and cannot be protected by Bcl-2. Journal of Immunology, 169, pp. 6850-6855.
45. Zheng, L., Dengler, T. J., Kluger, M. S., Madge, L. A., Schechner, J. S., Maher, S. E., Pober, J. S. and Bothwell, A. L. (2000) Cytoprotection of human umbilical vein endothelial cells against apoptosis and CTL-mediated lysis provided by caspase-resistant Bcl-2 without alterations in growth or activation responses. Journal of Immunology, 164, pp. 4665-4671.
46. Zheng, L., Gibson, T. F., Schechner, J. S., Pober, J. S. and Bothwell, A. L. (2004) Bcl-2 transduction protects human endothelial cell synthetic microvessel grafts from allogeneic T cells in vivo. Journal of Immunology, 173, pp. 3020-3026.
47. Zhou, J., Callapina, M., Goodall, G. J. and Brune, B. (2004) Functional integrity of nuclear factor κ B, phosphatidylinositol 3'-kinase, and mitogen-activated protein kinase signaling allows tumor necrosis factor α-evoked Bcl-2 expression to provoke internal ribosome entry site-dependent translation of hypoxia-inducible factor 1alpha. Cancer Research, 64, pp. 9041-9048.