Effects of simulated microgravity on human umbilical vein endothelial cell angiogenesis and role of the PI3K-Akt-eNOS signal pathway

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Shi, Fei ^a   Wang, Yong Chun ^a   Zhao, Tian Zhi ^a   Zhang, Shu ^a   Du, Ting Yuan ^a   Yang, Chang Bin ^a   Li, Ying Hui ^b   Sun, Xi Qing ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b Chinese Astronaut Research and Training Center   (China)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; N(G) NITROARGININE METHYL ESTER; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B;

ANGIOGENESIS; ARTICLE; CAVEOLA; CELL MIGRATION; CELL ULTRASTRUCTURE; CONTROLLED STUDY; CULTURE MEDIUM; DOWN REGULATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; INCUBATION TIME; MICROGRAVITY; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SIMULATION; TRANSMISSION ELECTRON MICROSCOPY; UMBILICAL VEIN ENDOTHELIAL CELL; UPREGULATION; WESTERN BLOTTING;

CAVEOLAE; CELL MOVEMENT; COLLAGEN; DRUG COMBINATIONS; ENZYME ACTIVATION; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; LAMININ; NEOVASCULARIZATION, PHYSIOLOGIC; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEOGLYCANS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; UP-REGULATION; WEIGHTLESSNESS SIMULATION;

EID: 84863773753     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040365     Document Type: Article

References (50)

1. Crawford-Young SJ, (2006) Effects of microgravity on cell cytoskeleton and embryogenesis. Int J Dev Biol50: 183-191.
2. Convertino VA, (2009) Status of cardiovascular issues related to space flight: Implications for future research directions. Respir Physiol Neurobiol 169: S34-S37.
3. Cines DB, Pollak ES, Buck CA, Loscalzo J, Zimmerman GA, et al. (1998) Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood 91: 3527-3561.
4. Carlsson SI, Bertilaccio MT, Ballabio E, Maier JA, (2003) Endothelial stress by gravitational unloading: effects on cell growth and cytoskeletal organization. Biochim Biophys Acta 1642: 173-179.
5. Infanger M, Ulbrich C, Baatout S, Wehland M, Kreutz R, et al. (2007) Modeled gravitational unloading induced downregulation of endothelin-1 in human endothelial cells. J Cell Biochem101: 1439-1455.
6. Morbidelli L, Monici M, Marziliano N, Cogoli A, Fusi F, et al. (2005) Simulated hypogravity impairs the angiogenic response of endothelium by up-regulating apoptotic signals. Biochem Biophys Res Commun 334: 491-499.
7. Coupe M, Fortrat JO, Larina I, Gauquelin-Koch G, Gharib C, et al. (2009) Cardiovascular deconditioning: From autonomic nervous system to microvascular dysfunctions. Respir Physiol Neuro boil 169: S10-S12.
8. Griffoni C, Di MS, Fantozzi L, Zanetti C, Pippia P, et al. (2011) Modification of proteins secreted by endothelial cells during modeled low gravity exposure. J Cell Biochem 112: 265-272.
9. Folkman J, (1995) Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med1: 27-31.
10. Bussolino F, Mantovani A, Persico G, (1997) Molecular mechanisms of blood vessel formation. Trends Biochem Sci 22: 251-256.
11. Mariotti M, Maier JA, (2008) Gravitational unloading induces an anti-angiogenic phenotype in human microvascular endothelial cells. J Cell Biochem 104: 129-135.
12. Huang PL, Huang Z, Mashimo H, Bloch KD, Moskowitz MA, et al. (1995) Hypertension in mice lacking the gene for endothelial nitric oxide synthase. Nature 377: 239-242.
13. Rudic RD, Shesely EG, Maeda N, Smithies O, Segal SS, et al. (1998) Direct evidence for the importance of endothelium-derived nitric oxide invascular remodeling. J Clin Invest 101: 731-736.
14. Murohara T, Asahara T, Silver M, Bauters C, Masuda H, et al. (1998) Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J Clin Invest 101: 2567-2578.
15. Siamwala JH, Majumder S, Tamilarasan KP, Muley A, Reddy SH, et al. (2010) Simulated microgravity promotes nitric oxide-supported angiogenesis via the iNOS-cGMP-PKG pathway in macrovascular endothelial cells. FEBS Letters 584: 3415-3423.
16. Goetze S, Bungenstock A, Czupalla C, Eilers F, Stawowy P, et al. (2002) Leptin induces endothelial cell migration through Akt, which is inhibited by PPAR gamma-ligands. Hypertension 40: 748-754.
17. Uruno A, Sugawara A, Kanatsuka H, Arima S, Taniyama Y, et al. (2004) Hepatocyte growth factor stimulates nitric oxide production through endothelial nitric oxide synthase activation by the phosphoinositide 3-kinase/Akt pathway and possibly by mitogen-activated protein kinase kinase in vascular endothelial cells. Hypertens Res 27: 887-895.
18. Kim I, Moon SO, Han CY, Pak YK, Moon SK, et al. (2001) The angiopoietin-tie 2 system in coronary artery endothelium preventsoxidized low-density lipoprotein-induced apoptosis. Cardiovasc Res 49: 872-881.
19. DimmelerS, Fleming I, Fisslthler B, Hermann C, Busse R, et al. (1999) Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399: 601-605.
20. Fisslthaler B, Dimmeler S, Hermann C, Busse R, Fleming I, (2000) Phosphorylation and activation of the endothelial nitric oxide synthase by fluid shear stress. Acta Physiol Scand 168: 81-88.
21. Kraft TF, van Loon JJ, Kiss JZ, (2000) Plastid position in Arabidopsis columella cells is similar in microgravity and on a random-positioning machine. Planta 211: 415-422.
22. Kacena MA, Todd P, Gerstenfeld LC, Landis WJ, (2002) Experiments with osteoblasts cultured under varying orientations with respect to the gravity vector. Cytotechnology 39: 147-154.
23. Barjaktarovic Z, Nordheim A, Lamkemeyer T, Fladerer C, Madlung J, et al. (2007) Time-course of changes in amounts of specific proteins uponexposure to hyper-g, 2-D clinorotation, and 3-D random positioning of Arabidopsis cell cultures. J Exp Bot 58: 4357-4363.
24. Wang YC, Zhang S, Du TY, Wang B, Sun XQ, (2009) Clinorotation upregulates inducible nitric oxide synthase by inhibiting AP-1 activation in human umbilical vein endothelial cells. J Cell Biochem 107: 357-363.
25. Miura S, Fujino M, Matsuo Y, Kawamura A, Tanigawa H, et al. (2003) High density lipoprotein-induced angiogenesis requires the activation of Ras/MAP kinase in human coronary artery endothelial cells. Arterioscler Thromb Vasc Biol 23: 802-808.
26. Miura S, Matsuo Y, Saku K, (2003) Transactivation of KDR/Flk-1 by the B2 receptor induces tube formation in human coronary endothelial cells. Hypertension 41: 1118-1123.
27. Leavesley DI, Schwartz MA, Rosenfeld M, Cheresh DA, (1993) Integrin beta1- and beta 3- mediated endothelial cell migration is triggered through distinct signaling mechanisms. J Cell Biol 121: 163-170.
28. Dhillon B, Badiwala MV, Li SH, Li RK, Weisel RD, et al. (2003) Caveolin: A key target for modulating nitric oxide availability in health and disease. Mol Cell Bio chem 247: 101-109.
29. Dayanir V, Meyer RD, Lashkari K, Rahimi N, (2001) Identification of tyrosine residues in vascular endothelial growth factor receptor-2/FLK-1 involved in activation of phosphatidylinositol 3-kinase and cell proliferation. J Bio chem 276: 17686-17692.
30. Lee SJ, Namkoong S, Kim YM, Kim CK, Lee H, et al. (2006) Fractalkine stimulates angiogenesis by activating the Raf-/MMK/ERK-and PI3K/Akt/eNOS-dependent signal pathway. Am J Physiol Heart Circ Physiol 291: H2836-H2846.
31. Infanger M, Kossmehl P, Shakibaei M, Baatout S, Witzing A, et al. (2006) Induction of three-dimensional assembly and increase in apoptosisof human endothelial cells by simulated microgravity: impact of vascular endothelial growth factor. Apoptosis 11: 749-764.
32. Grimm D, Infanger M, Westphal K, Ulbrich C, Pietsch J, et al. (2009) A delayed type of three-dimensional growth of human endothelial cells under simulated weightlessness. Tissue Eng: Part A 15: 2267-2275.
33. Siamwala JH, Reddy SH, Majumder S, Kolluru GK, Muley A, et al. (2010) Simulated microgravity perturbs actin polymerizationto promote nitric oxide-associated migrationin human immortalized Ea.hy926 cells. Protoplasma 242: 3-12.
34. Namkoong S, Chung BH, Ha KS, Lee H, Kwon YG, et al. (2008) Microscopic technique for the detection of nitric oxide-dependent angiogenesis in an animal model. Methods Enzymol 441: 393-402.
35. Sessa WC, (2009) Molecular control of blood flow and angiogenesis: role of nitric oxide. J Thromb Haemost 7: 35-37.
36. Namkoong S, Lee SJ, Kim CK, Kim YM, Chung HT, et al. (2005) Prostaglandin E2 stimulates angiogenesis by activating the nitric oxide/cGMP pathway in human umbilical vein endothelial cells. Exp Mol Med 37: 588-600.
37. Dulak J, Jozkowicz (2002) A Nitric oxide and angiogenic activity of endothelial cells: direct or VEGF-dependent effect? Cardiovasc Res 56: 487-488.
38. Murohara T, Asahara T, Silver M, Bauters C, Masuda H, et al. (1998) Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J Clin Invest 10: 2567-2578.
39. Ziche M, Morbidelli L, Choudhuri R, Zhang HT, Donnini S, et al. (1997) Nitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not basic fibroblast growth factor-induced angiogenesis. J Clin Invest 99: 2625-2634.
40. Chung BH, Kim JD, Kim CK, Kim JH, Won MH, et al. (2008) Icariin stimulates angiogenesis by activating the MEK/ERK- and PI3K/Akt/eNOS-dependent signal pathways in human endothelial cells. Biochem Biophys Res Commun 376: 404-408.
41. Shaul PW, Anderson RGW, (1998) Role of plasmalemmal caveolae in signal transduction. Am J Physiol Lung Cell Mol Physiol 275: L843-L851.
42. Beardsley A, Fang K, Mertz H, Castranova V, Friend S, et al. (2005) Loss of caveolin-1 polarity impedes endothelial cell. J Biol Chem 280: 3541-3547.
43. Bernatchez P, Sharma A, Bauer PM, Marin E, Sessa WC, (2011) A noninhibitory mutant of the caveolin-1 scaffolding domain enhances eNOS-derived NO synthesis and vasodilation in mice. J Clin Invest 121: 3747-3755.
44. Garcia-Cardena G, Martasek P, Masters BS, Skidd PM, Couet J, et al. (1997) Dissecting the interaction between nitric oxide synthase (NOS) and caveolin. Functional significance of the noscaveolin binding domain in vivo. J Biol Chem 272: 25437-25440.
45. Michel JB, Feron O, Sacks D, Michel T, (1997) Reciprocal regulation of endothelial nitric-oxide synthase by Ca2+-calmodulin and caveolin. J Biol Chem 272: 15583-15586.
46. Spisni E, Bianco MC, Griffoni C, et al. (2003) Mechanosensing role of caveolae and caveolar constituents in human endothelial cells. J Cell Physiol 197: 198-204.
47. Spisni E, Toni M, Strillacci A, Galleri G, Santi S, et al. (2006) Caveolae and caveolae constituents in mechanosensing. Effect of modeled microgravity on cultured human endothelial cells. Cell Biochem Biophys 46: 155-164.
48. Kureishi Y, Luo Z, Shiojima I, Bialik A, Fulton D, et al. (2000) The HMG-CoA reductase inhibitor simvastatin activates the protein kinase Akt and promotes angiogenesis in normocholesterolemic animals. Nat Med 6: 1004-1010.
49. Fulton D, Gratton JP, McCabe TJ, Fontana J, Fujio Y, et al. (1999) Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 399: 597-601.
50. Igarashi J, Bernier SG, Michel T, (2001) Sphingosine 1-phosphate and activation of endothelial nitric-oxide synthase. Differential regulation of Akt and MAP kinase pathways by EDG and bradykinin receptors in vascular endothelial cells. J Biol Chem 276: 12420-12426.