Differential effects of shear stress and cyclic strain on Sp1 phosphorylation by protein kinase Cζ modulates membrane type 1-matrix metalloproteinase in endothelial cells

Endothelium: Journal of Endothelial Cell Research

Volumn 15, Issue 1-2, 2008, Pages 33-42

  Kim, Ji Il ^a,b   Cordova, Alfredo C ^a   Hirayama, Yo ^a   Madri, Joseph A ^a   Sumpio, Bauer E ^a,c  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b The Catholic University of Korea College of Medicine   (South Korea)

^c West Haven Campus   (United States)

Author keywords

Hemodynamic Forces; MMP; PKC; sp1 phosphorylation

Indexed keywords

EARLY GROWTH RESPONSE FACTOR 1; MATRIX METALLOPROTEINASE 14; PROTEIN KINASE C INHIBITOR; PROTEIN KINASE C ZETA; TRANSCRIPTION FACTOR SP1;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; EXPOSURE; IMMUNOPRECIPITATION; INHIBITION KINETICS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SHEAR STRESS; WESTERN BLOTTING;

ANIMALS; CELL CULTURE TECHNIQUES; CELLS, CULTURED; CULTURE MEDIA, SERUM-FREE; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; ISOENZYMES; MALE; MATRIX METALLOPROTEINASE 14; MODELS, BIOLOGICAL; PHOSPHORYLATION; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; SP1 TRANSCRIPTION FACTOR; STRESS; STRESS, MECHANICAL;

EID: 46049093008     PISSN: 10623329     EISSN: 10292373     Source Type: Journal    
DOI: 10.1080/10623320802092260     Document Type: Article

References (66)

1. Akai, Y., Homma, T., Burns, K. D., Yasuda, T., Badr, K. F. and Harris, R. C. (1994) Mechanical stretch/relaxation of cultured rat mesangial cells induces protooncogenes and cyclooxygenase. American Journal of Physiology, 267, pp. C482-C490.
2. Armstrong, S. A., Barry, D. A., Leggett, R. W. and Mueller, C. R. (1997) Casein kinase II-mediated phosphorylation of the C terminus of Sp1 decreases its DNA binding activity. Journal of Biological Chemistry, 272, pp. 13489-13495.
3. Azizkhan, J. C., Jensen, D. E., Pierce, A. J. and Wade, M. (1993) Transcription from TATA-less promoters: Dihydrofolate reductase as a model. Critical Reviews in Eukaryotic Gene Expression, 3, pp. 229-254.
4. Birkedal-Hansen, H. (1995) Proteolytic remodeling of extracellular matrix. Current Opinions in Cell Biology, 7, pp. 728-735.
5. Black, A. R., Jensen, D., Lin, S. Y. and Azizkhan, J. C. (1999) Growth/ cell cycle regulation of Sp1 phosphorylation. Journal of Biological Chemistry, 274, pp. 1207-1215.
6. Carmeliet, P. and Jain, R. K. (2000) Angiogenesis in cancer and other diseases. Nature, 407, pp. 249-257.
7. Cenni, V., Doppler, H., Sonnenburg, E. D., Maraldi, N., Newton, A. C. and Toker, A. (2002) Regulation of novel protein kinase C epsilon by phosphorylation. Biochemical Journal, 363, pp. 537-545.
8. Chou, M. M., Hou, W., Johnson, J., Graham, L. K., Lee, M. H., Chen, C. S., Newton, A. C., Schaffhausen, B. S. and Toker, A. (1998) Regulation of protein kinase C zeta by PI 3-kinase and PDK-1. Current Biology, 8, pp. 1069-1077.
9. Chun, R. F., Semmes, O. J., Neuveut, C. and Jeang, K. T. (1998) Modulation of Sp1 phosphorylation by human immunodeficiency virus type 1 Tat. J Virol, 72, pp. 2615-2629.
10. Cook, T., Gebelein, B. and Urrutia, R. (1999) Sp1 and its likes: biochemical and functional predictions for a growing family of zinc finger transcription factors. Annals of the New York Academy of Sciences, 880, pp. 94-102.
11. Courey, A. J. and Tjian, R. (1988) Analysis of Sp1 in vivo reveals multiple transcriptional domains, including a novel glutamine-rich activation motif. Cell, 55, pp. 887-898.
12. Courey, A. J., Holtzman, D. A., Jackson, S. P. and Tjian, R. (1989) Synergistic activation by the glutamine-rich domains of human transcription factor Sp1. Cell, 59, pp. 827-836.
13. Cuschieri, J., Umanskiy, K. and Solomkin, J. (2004) PKC-zeta is essential for endotoxin-induced macrophage activation. Journal of Surgical Research, 121, pp. 76-83.
14. Dardik, A., Chen, L., Frattini, J., Asada, H., Aziz, F., Kudo, F. A. and Sumpio, B. E. (2005) Differential effects of orbital and laminar shear stress on endothelial cells. Journal of Vascular Surgery, 41, pp. 869-880.
15. Davies, P. F., Barbee, K. A., Volin, M. V., Robotewskyj, A., Chen, J., Joseph, L., Griem, M. L., Wernick, M. N., Jacobs, E. Polacek, D. C. et al. (1997) Spatial relationships in early signaling events of flow-mediated endothelial mechanotransduction. Annual Reviews in Physiology, 59, pp. 527-549.
16. Eichholtz, T., de Bont, D. B., de Widt, J., Liskamp, R. M. and Ploegh, H. L. (1993) A myristoylated pseudosubstrate peptide, a novel protein kinase C inhibitor. Journal of Biological Chemistry, 268, pp. 1982-1986.
17. Fojas, de Borja, P., Collins, N. K., Du, P., Azizkhan-Clifford, J. and Mudryj, M. (2001) Cyclin A-CDK phosphorylates Sp1 and enhances Sp1-mediated transcription. EMBO Journal, 20, pp. 5737-5747.
18. Friedl, P. and Wolf, K. (2003) Tumour-cell invasion and migration: diversity and escape mechanisms. Nature Reviews in Cancer, 3, pp. 362-374.
19. Graesser, D., Mahooti, S. and Madri, J. A. (2000) Distinct roles for matrix metalloproteinase-2 and alpha4 integrin in autoimmune T cell extravasation and residency in brain parenchyma during experimental autoimmune encephalomyelitis. Journal of Neuroimmunology, 109, pp. 121-131.
20. Graesser, D., Mahooti, S., Haas, T., Davis, S., Clark, R. B. and Madri, J. A. (1998) The interrelationship of alpha4 integrin and matrix metalloproteinase-2 in the pathogenesis of experimental autoimmune encephalomyelitis. Laboratory Investigation, 78, pp. 1445-1458.
21. Gschwendt, M., Dieterich, S., Rennecke, J., Kittstein, W., Mueller, H. J. and Johannes, F. J. (1996) Inhibition of protein kinase C mu by various inhibitors. Differentiation from protein kinase c isoenzymes. FEBS Letters, 392, pp. 77-80.
22. Haas, T. L., Davis, S. J. and Madri, J. A. (1998) Three-dimensional type I collagen lattices induce coordinate expression of matrix metalloproteinases MT1-MMP and MMP-2 in microvascular endothelial cells. Journal of Biological Chemistry, 273, pp. 3604-3610.
23. Haas, T. L., Milkiewicz, M., Davis, S. J., Zhou, A. L., Egginton, S., Brown, M. D., Madri, J. A. and Hudlicka, O. (2000) Matrix metalloproteinase activity is required for activity-induced angiogenesis in rat skeletal muscle. American Journal of Physiology Heart Circualatory Physiology, 279, pp. H1540-H1547.
24. Haas, T. L., Stitelman, D., Davis, S. J., Apte, S. S. and Madri, J. A. (1999) Egr-1 mediates extracellular matrix-driven transcription of membrane type 1 matrix metalloproteinase in endothelium. Journal of Biological Chemistry, 274, pp. 22679-22685.
25. Haidweger, E., Novy, M. and Rotheneder, H. (2001) Modulation of Sp1 activity by a cyclin A/CDK complex. Journal of Molecular Biology, 306, pp. 201-212.
26. Hanahan, D. and Folkman, J. (1996) Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell, 86, pp. 353-364.
27. Hiraoka, N., Allen, E., Apel, I. J., Gyetko, M. R. and Weiss, S. J. (1998) Matrix metalloproteinases regulate neovascularization by acting as pericellular fibrinolysins. Cell, 95, pp. 365-377.
28. Hudlicka, O. (1998) Is physiological angiogenesis in skeletal muscle regulated by changes in microcirculation?. Microcirculation, 5, pp. 5-23.
29. Ihn, H., Ihn, Y. and Trojanowska, M. (2001) Spl phosphorylation induced by serum stimulates the human alpha2(I) collagen gene expression. Journal of Investigative Dermatology, 117, pp. 301-308.
30. Inoue, M., Kishimoto, A., Takai, Y. and Nishizuka, Y. (1977) Studies on a cyclic nucleotide-independent protein kinase and its proenzyme in mammalian tissues. II. Proenzyme and its activation by calcium-dependent protease from rat brain. Journal of Biological Chemistry, 252, pp. 7610-7616.
31. Jackson, S., Gottlieb, T. and Hartley, K. (1993) Phosphorylation of transcription factor Sp1 by the DNA-dependent protein kinase. Advances in Second Messenger and Phosphoprotein Research, 28, pp. 279-286.
32. Keranen, L. M., Dutil, E. M. and Newton, A. C. (1995) Protein kinase C is regulated in vivo by three functionally distinct phosphorylations. Current Biology, 5, pp. 1394-1403.
33. Khachigian, L. M., Lindner, V., Williams, A. J. and Collins, T. (1996) Egr-1-induced endothelial gene expression: A common theme in vascular injury. Science, 271, pp. 1427-1431.
34. Kishimoto, A., Takai, Y., Mori, T., Kikkawa, U. and Nishizuka, Y. (1980) Activation of calcium and phospholipid-dependent protein kinase by diacylglycerol, its possible relation to phosphatidylinositol turnover. Journal of Biological Chemistry, 255, pp. 2273-2276.
35. Liu, W. S. and Heckman, C. A. (1998) The sevenfold way of PKC regulation. Cell Signaling, 10, pp. 529-542.
36. Madri, J. A. and Williams, S. K. (1983) Capillary endothelial cell cultures: Phenotypic modulation by matrix components. Journal of Cell Biology, 97, pp. 153-165.
37. McQuibban, G. A., Butler, G. S., Gong, J. H., Bendall, L., Power, C., Clark-Lewis, I. and Overall, C. M. (2001) Matrix metalloproteinase activity inactivates the CXC chemokine stromal cell-derived factor-1. Journal of Biological Chemistry, 276, pp. 43503-43508.
38. McQuibban, G. A., Gong, J. H., Tam, E. M., McCulloch, C. A., Clark-Lewis, I. and Overall, C. M. (2000) Inflammation dampened by gelatinase A cleavage of monocyte chemoattractant protein-3. Science, 289, pp. 1202-1206.
39. McQuibban, G. A., Gong, J. H., Wong, J. P., Wallace, J. L., Clark-Lewis, I. and Overall, C. M. (2002) Matrix metalloproteinase processing of monocyte chemoattractant proteins generates CC chemokine receptor antagonists with anti-inflammatory properties in vivo. Blood, 100, pp. 1160-1167.
40. Merchant, J. L., Du, M. and Todisco, A. (1999) Sp1 phosphorylation by Erk 2 stimulates DNA binding. Biochemical Biophysical Research Communication, 254, pp. 454-461.
41. Mignatti, P. and Rifkin, D. B. (1996) Plasminogen activators and angiogenesis. Current Topics in Microbiology Immunology, 213, pp. 33-50.
42. Nakanishi, H., Brewer, K. A. and Exton, J. H. (1993) Activation of the zeta isozyme of protein kinase C by phosphatidylinositol 3,4,5-trisphosphate. Journal of Biological Chemistry, 268, pp. 13-16.
43. Nishizuka, Y. (1995) Protein kinase C and lipid signaling for sustained cellular responses. FASEB Journal, 9, pp. 484-496.
44. Overall, C. M. and Lopez-Otin, C. Strategies for MMP inhibition in cancer: Innovations for the post-trial era. Nature Reviews in Cancer, 2, pp. 657-672.
45. Pal, S., Claffey, K. P., Cohen, H. T. and Mukhopadhyay, D. (1998) Activation of Sp1-mediated vascular permeability factor/vascular endothelial growth factor transcription requires specific interaction with protein kinase C zeta. Journal of Biological Chemistry, 273, pp. 26277-26280.
46. Pal, S., Datta, K., Khosravi-Far, R. and Mukhopadhyay, D. (2001) Role of protein kinase Czeta in Ras-mediated transcriptional activation of vascular permeability factor/vascular endothelial growth factor expression. Journal of Biological Chemistry, 276, pp. 2395-2403.
47. Pan, M. R. and Hung, W. C. (2002) Nonsteroidal anti-inflammatory drugs inhibit matrix metalloproteinase-2 via suppression of the ERK/ Sp1-mediated transcription. Journal of Biological Chemistry, 277, pp. 32775-32780.
48. Pascal, E. and Tjian, R. (1991) Different activation domains of Sp1 govern formation of multimers and mediate transcriptional synergism. Genes and Development, 5, pp. 1646-1656.
49. Philipsen, S. and Suske, G. (1999) A tale of three fingers: The family of mammalian Sp/XKLF transcription factors. Nucleic Acids Research, 27, pp. 2991-3000.
50. Rafty, L. A. and Khachigian, L. M. (2001) Sp1 phosphorylation regulates inducible expression of platelet-derived growth factor B-chain gene via atypical protein kinase C-zeta. Nucleic Acids Research, 29, pp. 1027-1033.
51. Risau, W. (1997) Mechanisms of angiogenesis. Nature, 386, pp. 671-674.
52. Rohlff, C., Ahmad, S., Borellini, F., Lei, J. and Glazer, R. I. (1997) Modulation of transcription factor Sp1 by cAMP-dependent protein kinase. Journal of Biological Chemistry, 272, pp. 21137-21141.
53. Sato, H., Okada, Y. and Seiki, M. (1997) Membrane-type matrix metalloproteinases (MT-MMPs) in cell invasion. Thrombosis and Haemostasis, 78, pp. 497-500.
54. Sato, H., Takino, T., Okada, Y., Cao, J., Shinagawa, A., Yamamoto, E. and Seiki, M. (1994) A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature, 370, pp. 61-65.
55. Schwachtgen, J. L., Houston, P., Campbell, C., Sukhatme, V. and Braddock, M. (1998) Fluid shear stress activation of egr-1 transcription in cultured human endothelial and epithelial cells is mediated via the extracellular signal-related kinase 1/2 mitogen-activated protein kinase pathway. Journal of Clinical Investigation, 101, pp. 2540-2549.
56. Standaert, M. L., Galloway, L., Karnam, P., Bandyopadhyay, G., Moscat, J. and Farese, R. V. (1997) Protein kinase C-zeta as a downstream effector of phosphatidylinositol 3-kinase during insulin stimulation in rat adipocytes. Potential role in glucose transport. Journal of Biological Chemistry, 272, pp. 30075-30082.
57. Stempka, L., Girod, A., Muller, H. J., Rincke, G., Marks, F., Gschwendt, M. and Bossemeyer, D. (1997) Phosphorylation of protein kinase Cdelta (PKCdelta) at threonine 505 is not a prerequisite for enzymatic activity. Expression of rat PKCdelta and an alanine 505 mutant in bacteria in a functional form. Journal of Biological Chemistry, 272, pp. 6805-6811.
58. Strongin, A. Y., Collier, I., Bannikov, G., Marmer, B. L., Grant, G. A. and Goldberg, G. I. (1995) Mechanism of cell surface activation of 72-kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease. Journal of Biological Chemistry, 270, pp. 5331-5338.
59. Sun, R., Gao, P., Chen, L., Ma, D., Wang, J., Oppenheim, J. J. and Zhang, N. (2005) Protein kinase C zeta is required for epidermal growth factor-induced chemotaxis of human breast cancer cells. Cancer Research, 65, pp. 1433-1441.
60. Tam, E. M., Morrison, C. J., Wu, Y. I., Stack, M. S. and Overall, C. M. (2004) Membrane protease proteomics: Isotope-coded affinity tag MS identification of undescribed MT1-matrix metalloproteinase substrates. Proceedings of the National Academy of Sciences of the United States of America, 101, pp. 6917-6922.
61. Toker, A. (1998) Signaling through protein kinase C. Frontiers in Biosciences, 3, pp. D1134-D1147.
62. Van, Den, Steen, P. E., Wuyts, A., Husson, S. J., Proost, P., Van Damme, J. and Opdenakker, G. (2003) Gelatinase B/MMP-9 and neutrophil collagenase/MMP-8 process the chemokines human GCP-2/CXCL6, ENA-78/CXCL5 and mouse GCP-2/LIX and modulate their physiological activities. European Journal of Biochemistry, 270, pp. 3739-3749.
63. Woessner Jr., J. F. (1994) The family of matrix metalloproteinases. Annals of the New York Academy of Sciences, 732, pp. 11-21.
64. Yamaguchi, S., Yamaguchi, M., Yatsuyanagi, E., Yun, S. S., Nakajima, N., Madri, J. A. and Sumpio, B. E. (2002) Cyclic strain stimulates early growth response gene product 1-mediated expression of membrane type 1 matrix metalloproteinase in endothelium. Laboratory Investigation, 82, pp. 949-956.
65. Yun, S., Dardik, A., Haga, M., Yamashita, A., Yamaguchi, S., Koh, Y., Madri, J. A. and Sumpio, B. E. (2002) Transcription factor Sp1 phosphorylation induced by shear stress inhibits membrane type 1-matrix metalloproteinase expression in endothelium. Journal of Biological Chemistry, 277, pp. 34808-34814.
66. Zhang, K., McQuibban, G. A., Silva, C. G. S., Johnston, J. B., Holden, J., Clark-Lewis, I., Overall, C. M. and Power, C. (2003) HIV-induced metalloproteinase processing of the chemokine stromal cell derived factor-1 causes neurodegeneration. Nature Neuroscience, 6, pp. 1064-1071.