Activated pericyte attenuates endothelial functions: Nitric oxide - cGMP rescues activated pericyte-associated endothelial dysfunctions

Biochemistry and Cell Biology

Volumn 85, Issue 6, 2007, Pages 709-720

  Majumder, Syamantak ^a   Tamilarasan, K P ^a   Kolluru, Gopi Krishna ^a   Muley, Ajit ^a   Nair, C Madhavan ^a   Omanakuttan, Athira ^a   Murty, K V G K ^a   Chatterjee, Suvro ^a  

^a ANNA UNIVERSITY   (India)

Author keywords

cGMP; Endothelial cells; Hepatic stellate cells; Nitric oxide

Indexed keywords

BIOCHEMISTRY; ENDOTHELIAL CELLS; LIVER; MATHEMATICAL MODELS; PATHOGENS;

ANGIOGENESIS; ENDOTHELIAL DYSFUNCTIONS; HEPATIC STELLATE CELLS; PATHOGENESIS;

NITRIC OXIDE;

8 BROMO CYCLIC GMP; CYCLIC GMP; GUANYLATE CYCLASE; NITRIC OXIDE; PHOSPHODIESTERASE INHIBITOR; SILDENAFIL;

ANGIOGENESIS; ARTICLE; CELL ACTIVATION; CELL MEMBRANE PERMEABILITY; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; CULTURE MEDIUM; EGG YOLK; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; PERICYTE; PROTEIN STRUCTURE; STELLATE CELL; WOUND HEALING;

ANIMALS; CELL LINE; CELL MEMBRANE PERMEABILITY; CELL MOVEMENT; CELL PROLIFERATION; CELL SURFACE EXTENSIONS; CHICKENS; CULTURE MEDIA, CONDITIONED; CYCLIC GMP; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIAL CELLS; ENZYME INHIBITORS; GUANYLATE CYCLASE; HEPATOCYTES; HUMANS; HYDROLYSIS; NEOVASCULARIZATION, PHYSIOLOGIC; NITRIC OXIDE; PERICYTES; SOLUBILITY; WOUND HEALING;

EID: 38849195415     PISSN: 08298211     EISSN: None     Source Type: Journal    
DOI: 10.1139/O07-140     Document Type: Article

References (42)

1. Antonelli-Orlidge, A., Saunders, K.B., Smith, S.R., and D'Amore, P.A. 1989. An aActivated form of transforming growth factor beta is produced by cocultures of endothelial cells and pericytes. Proc. Natl. Acad. Sci. U.S.A. 86: 4544-4548. doi:10.1073/pnas.86.12.4544.
2. Armulik, A., Abramsson, A., and Betsholtz, C. 2005. Endothelial/pericyte interactions. Circ. Res. 97: 512-523. doi:10.1161/01.RES.0000182903. 16652.d7.
3. Bergers, G., and Song, S. 2005. The role of pericytes in blood vessel formation and maintenance. Neuro-oncol. 7: 452-464. doi:10.1215/ S1152851705000232.
4. Bergers, G., Song, S., Meyer-Morse, N., Bergsland, E., and Hanahan, D. 2003. Benefits of targeting both pericytes and endothelial cells in the tumor vasculature with kinase inhibitors. J. Clin. Invest. 111: 1287-1295. doi:10.1172/JCI200317929.
5. Binétruy-Tournaire, R., Demangel, C., Malavaud, B., Vassy, R., Rouyre, S., Kraemer, M., Plouët, J., Derbin, C., Perret, G., and Mazié, J.C. 2000. Identification of a peptide blocking vascular endothelial growth factor (VEGF)-mediated angiogenesis. EMBO J. 3;19(7):1525-1533.
6. Camenisch, G., Pisabarro, M.T., Sherman, D., Kowalski, J., Nagel, M., Hass, P., et al. 2002. ANGPTL3 stimulates endothelial cell adhesion and migration via integrin alpha vbeta 3 and induces blood vessel formation in vivo. J. Biol. Chem. 277: 17281-17290. doi:10.1074/jbc.M109768200.
7. Deibert, P., Rössle, M., Opitz, O., Schmieg-Kurz, A.K., Blum, H., and Kreisel, W. 2006. Comparable effects of Sildenafil, Vardenafil, and Tadalafil-the three licensed inhibitors of phosphodiesterase 5-on portal haemodynamics. Z. Gastroenterol. 44: 10. doi:10.1055/s-2006-950798.
8. Dentelli, P., Del Sorbo, L., Rosso, A., Molinar, A., Garbarino, G., Camussi, G., Pegoraro, L., and Brizzi, M.F. 1999. Human IL-3 stimulates endothelial cell motility and promotes in vivo new vessel formation. J. Immunol. 163: 2151-2159.
9. Dodge, A.B., and D'Amore, P.A. 1992. Cell-cell interactions in diabetic angiopathy. Diabetes Care, 15: 1168-1180. doi:10.2337/diacare.15.9.1168.
10. Egginton, S., Hudlicka, O., Brown, M.D., Graciotti, L., and Granata, A.L. 1996. In vivo pericyte-endothelial cell interaction during angiogenesis in adult cardiac and skeletal muscle. Microvasc. Res. 51: 213-228. doi:10.1006/mvre.1996.0022.
11. Fiorucci, S., Antonelli, E., Morelli, O., Mencarelli, A., Casini, A., Mello, T., et al. 2001. NCX-1000, a NO-releasing derivative of ursodeoxycholic acid, selectively delivers NO to the liver and protects against development of portal hypertension. Proc. Natl. Acad. Sci. U.S.A. 98: 8897-8902. doi:10.1073/pnas.151136298.
12. Friedman, S.L. 2004. Mechanisms of disease: Mechanisms of hepatic fibrosis and therapeutic implications. Nat. Clin. Pract. Gastroenterol. Hepatol. 1: 98-105. doi:10.1038/ncpgasthep0055.
13. Geerts, A. 2001. History, heterogeneity, developmental biology and functions of quiescent hepatic stellate cells. Semin. Liver Dis. 21: 311-335. doi:10.1055/s-2001-17550.
14. Haefliger, I.O., Chen, Q., and Anderson, D.R. 1997. Effect of oxygen on relaxation of retinal pericytes by sodium nitroprusside. Graefes Arch. Clin. Exp. Ophthalmol. 235: 388-392. doi:10.1007/BF00937289.
15. Harrison, D.G. 1997. Cellular and molecular mechanisms of endothelial cell dysfunction. J. Clin. Invest. 100: 2153-2157.
16. Herman, I.M., Newcomb, P.M., Coughlin, J.E., and Jacobson, S. 1987. Characterization of microvascular cell cultures from normotensive and hypertensive rat brains: pericyte-endothelial cell interactions in vitro. Tissue Cell, 19: 197-206. doi:10.1016/0040-8166(87)90005-X.
17. Kashiwagi, S., Izumi, Y., Gohongi, T., Demou, Z.N., Xu, L., Huang, P.L., et al. 2005. NO mediates mural cell recruitment and vessel morphogenesis in murine melanomas and tissue-engineered blood vessels. J. Clin. Invest. 115: 1816-1827. doi:10.1172/JCI24015.
18. Kim, K.Y., Choi, I., and Kim, S.S. 2000. Progression of hepatic stellate cell activation is associated with the level of oxidative stress rather than cytokines during CCl4-induced fibrogenesis. Mol. Cells, 10: 289-300.
19. Kondo, T., Hosoya, K., Hori, S., Tomi, M., Ohtsuki, S., and Terasaki, T. 2005. PKC/MAPK signaling suppression by retinal pericyte conditioned media prevents retinal endothelial cell proliferation. J. Cell. Physiol. 203: 378-386. doi:10.1002/jcp.20237.
20. Lee, J.S., Kang Decker, N., Chatterjee, S., Yao, J., Friedman, S., and Shah, V. 2005. Mechanisms of nitric oxide interplay with Rho GTPase family members in modulation of actin membrane dynamics in pericytes and fibroblasts. Am. J. Pathol. 166: 1861-1870.
21. Lee, J.S., Semela, D., Iredale, J., and Shah, V.H. 2007. Sinusoidal remodeling and angiogenesis: a new function for the liver-specific pericyte? Hepatology, 45: 817-825. doi:10.1002/hep.21564.
22. Loureiro-Silva, M.R., Cadelina, G.W., Iwakiri, Y., and Groszmann, R.J. 2003. A liver-specific nitric oxide donor improves the intrahepatic vascular response to both portal blood flow increase and methoxamine in cirrhotic rats. J. Hepatol. 39: 1072-1075. doi:10.1016/j.jhep.2003.09.018.
23. Mandarino, L.J., Sundarraj, N., Finlayson, J., and Hassell, H.R. 1993. Regulation of fibronectin and laminin synthesis by retinal capillary endothelial cells and pericytes in vitro. Exp. Eye Res. 57: 609-621. doi:10.1006/exer.1993.1166.
24. Nims, R.W., Cook, J.C., Krishna, M.C., Christodoulou, D., Poore, C.M., Miles, A.M., Grisham, M.B., and Wink, D.A. 1996. Colorimetric assays for nitric oxide and nitrogen oxide species formed from nitric oxide stock solutions and donor compounds. Methods Enzymol. 268: 93-105.
25. Pearse, D.B., Shimoda, L.A., Verin, A.D., Bogatcheva, N., Moon, C., Ronnett, G.V., Welsh, L.E., and Becker, P.M. 2003. Effect of cGMP on lung microvascular endothelial barrier dysfunction following hydrogen peroxide. Endothelium, 10: 309-317. doi:10.1080/714007541.
26. Perri, R.E., Langer, D.A., Chatterjee, S., Gibbons, S.J., Gadgil, J., Cao, S., Farrugia, G., and Shah, V.H. 2006. Defects in cGMP-PKG pathway contribute to impaired NO-dependent responses in hepatic stellate cells upon activation. Am. J. Physiol. Gastrointest. Liver Physiol. 290: G535-G542. doi:10.1152/ajpgi.00297.2005.
27. Reichenberger, F., Voswinckel, R., Steveling, E., Enke, B., Kreckel, A., Olschewski, H., et al. 2006. Sildenafil treatment for portopulmonary hypertension. Eur. Respir. J. 28: 563-567. doi:10.1183/09031936.06. 00030206.
28. Reynaert, H., Thompson, M.G., Thomas, T., and Geerts, A. 2002. Hepatic stellate cells: role in microcirculation and pathophysiology of portal hypertension. Gut, 50: 571-81. doi:10.1136/gut.50.4.571.
29. Rucker, H.K., Wynder, H.J., and Thomas, W.E. 2000. Cellular mechanisms of CNS pericytes. Brain Res. Bull. 51: 363-369. doi:10.1016/S0361-9230(99) 00260-9.
30. Sato, Y., and Rifkin, D.B. 1989. Inhibition of endothelial cell movement by pericyte 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. doi:10.1083/jcb.109.1.309.
31. Shah, V. 2004. Molecular mechanisms in the pathogenesis of cirrhotic portal hypertension: focus on nitric oxide. J. Gastroenterol. Hepatol. 19: S145. doi:10.1111/j.1440-1746.2004.03666.x.
32. Shah, V.H., and Kamath, P. 2006. Management of portal hypertension. Postgrad. Med. 119: 14-18.
33. Shah, V., Haddad, F.G., Garcia-Cardena, G., Frangos, J.A., Mennone, A., Groszmann, R.J., and Sessa, W.C. 1997. Liver sinusoidal endothelial cells are responsible for nitric oxide modulation of resistance in the hepatic sinusoids. J. Clin. Invest. 100: 2923-2930.
34. Shah, V., Toruner, M., Haddad, F., Cadelina, G., Papapetropoulos, A., Choo, K., Sessa, W.C., and Groszmann, R.J. 1999. Impaired endothelial nitric oxide synthase activity associated with enhanced caveolin binding in experimental cirrhosis in the rat. Gastroenterology, 117: 1222-1228. doi:10.1016/S0016-5085(99)70408-7.
35. Shepro, D., and Morel, N.M. 1993. Pericyte physiology. FASEB J. 7: 1031-1038.
36. Sims, D.E. 1991. Recent advances in pericyte biology-implications for health and disease. Can. J. Cardiol. 7: 431-443.
37. Soff, G.A., Cornwell, T.L., Cundiff, D.L., Gately, S., and Lincoln, T.M. 1997. Smooth muscle cell expression of type I cyclic GMP-dependent protein kinase is suppressed by continuous exposure to nitrovasodilators, theophylline, cyclic GMP, and cyclic AMP. J. Clin. Invest. 100: 2580-2587.
38. Staton, C.A., Stribbling, S.M., Tazzyman, S., Hughes, R., Brown, N.J., and Lewis, C.E. 2004. Current methods for assaying angiogenesis in vitro and in vivo. Int. J. Exp. Pathol. 85: 233-248. doi:10.1111/j.0959-9673.2004. 00396.x.
39. Vistica, D.T., Skehan, P., Scudiero, D., Monks, A., Pittman, A., and Boyd, M.R. 1991. Tetrazolium-based assays for cellular viability: a critical examination of selected parameters affecting formazan production. Cancer Res. 51: 2515-2520.
40. Wang, X., Tang, X., Gong, X., Albanis, E., Friedman, S.L., and Mao, Z. 2004. Regulation of hepatic stellate cell activation and growth by transcription factor myocyte enhancer factor 2. Gastroenterology, 127: 1174-1188. doi:10.1053/j.gastro.2004.07.007.
41. Xu, L., Hui, A., Albanis, E., Arther, M., O'Byrne, S., Blaner, W., et al. 2005. Human hepatic stellate cell lines, LX-1 and LX-2: new tools for analysis of hepatic fibrosis. Gut, 54: 142-151. doi:10.1136/gut.2004.042127.
42. Yamagishi, S., and Imaizumi, T. 2005. Pericyte biology and diseases. Int. J. Tissue React. 27: 125-135.