Tipping off endothelial tubes: nitric oxide drives tip cells

Angiogenesis

Volumn 18, Issue 2, 2015, Pages 175-189

  Priya, Mani Krishna ^a   Sahu, Giriraj ^b   Soto Pantoja, David R ^c   Goldy, Naga ^a   Sundaresan, Abaya Meenakshi ^a   Jadhav, Vivek ^a   Barathkumar, T R ^a   Saran, Uttara ^a   Jaffar Ali, B M ^d   Roberts, David D ^c   Bera, Amal Kanti ^b   Chatterjee, Suvro ^a  

^a ANNA UNIVERSITY   (India)

^b INDIAN INSTITUTE OF TECHNOLOGY MADRAS   (India)

^c NATIONAL CANCER INSTITUTE   (United States)

^d PONDICHERRY UNIVERSITY   (India)

Author keywords

Cyclic guanosine monophosphate; Endothelial nitric oxide synthase; Nitric oxide; Stalk cell; Tip cell

Indexed keywords

CYCLIC GMP; ENDOTHELIAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; SMALL INTERFERING RNA;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CELL GROWTH; CELL MIGRATION; CELLULAR DISTRIBUTION; CHORIOALLANTOIS; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME SYNTHESIS; MOLECULAR IMAGING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; BOVINE; CHICKEN; GENETICS; HUMAN; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; TRANSFORMED CELL LINE;

ANIMALS; CATTLE; CELL LINE, TRANSFORMED; CHICKENS; CYCLIC GMP; HUMANS; NEOVASCULARIZATION, PHYSIOLOGIC; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORYLATION; RNA, SMALL INTERFERING; UP-REGULATION;

EID: 84925461641     PISSN: 09696970     EISSN: 15737209     Source Type: Journal    
DOI: 10.1007/s10456-014-9455-0     Document Type: Article

References (43)

1. Pyriochou A, Zhou Z, Koika V, Petrou C, Cordopatis P, Sessa WC, Papapetropoulos A (2007) The phosphodiesterase 5 inhibitor sildenafil stimulates angiogenesis through a protein kinase G/MAPK pathway. J Cell Physiol 211:197–204
2. Gerhardt H, Golding M, Fruttiger M, Ruhrberg C, Lundkvist A, Abramsson A, Jeltsch M, Mitchell C, Alitalo K, Shima D, Betsholtz C (2003) VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol 161:1163–1177
3. Strasser GA, Kaminker JS, Tessier-Lavigne M (2010) Microarray analysis of retinal endothelial tip cells identifies CXCR4 as a mediator of tip cell morphology and branching. Blood 115:5102–5110
4. Suchting S, Freitas C, le Noble F, Benedito R, Bréant C, Duarte A, Eichmann A (2007) The notch ligand delta-like 4 negatively regulates endothelial tip cell formation and vessel branching. Proc Natl Acad Sci USA 104:3225–3230
5. Tammela T, Zarkada G, Wallgard E, Murtomäki A, Suchting S, Wirzenius M, Waltari M, Hellström M, Schomber T, Peltonen R, Freitas C et al (2008) Blocking VEGFR-3 suppresses angiogenic sprouting and vascular network formation. Nature 454:656–660
6. Ziche M, Morbidelli L, Choudhuri R, Zhang HT, Donnini S, Granger HJ, Bicknell R (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
7. Fukumura D, Gohongi T, Kadambi A, Izumi Y, Ang J, Yun CO, Buerk DG, Huang PL, Jain RK (2001) Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability. Proc Natl Acad Sci USA 98:2604–2609
8. Ziche M, Morbidelli L (2000) Nitric oxide and angiogenesis. J Neurooncol 50:139–148
9. Ridnour LA, Isenberg JS, Espey MG, Thomas DD, Roberts DD, Wink DA (2005) Nitric oxide regulates angiogenesis through a functional switch involving thrombospondin-1. Proc Natl Acad Sci USA 102:13147–13152
10. Sinha S, Sridhara SR, Srinivasan S, Muley A, Majumder S, Kuppusamy M, Gupta R, Chatterjee S (2011) NO (nitric oxide): the ring master. Eur J Cell Biol 90:58–71
11. Jones RA, Wang Z, Dookie S, Griffin M (2013) The role of TG2 in ECV304-related vasculogenic mimicry. Amino Acids 44:89–101
12. Ryan US (1984) Isolation and culture of pulmonary endothelial cells. Environ Health Perspect 56:103–114
13. Chung-Welch N, Shepro D, Dunham B, Hechtman HB (1988) Prostacyclin and prostaglandin E2 secretions by bovine pulmonary microvessel endothelial cells are altered by changes in culture conditions. J Cell Physiol 135:224–234
14. Siamwala JH, Veeriah V, Priya MK, Rajendran S, Saran U, Sinha S, Nagarajan S, Pradeep T, Chatterjee S (2012) Nitric oxide rescues thalidomide mediated teratogenicity. Sci Rep 2:679
15. Mukhopadhyay S, Shah M, Patel K, Sehgal PB (2006) Monocrotaline pyrrole induced megalocytosis of lung and breast epithelial cells: disruption of plasma membrane and Golgi dynamics and an enhanced unfolded protein response. Toxicol Appl Pharmacol 211:209–220
16. Fleming I, Busse R (1999) Signal transduction of eNOS activation. Cardiovasc Res 43:532–541
17. Sessa WC, Garcia-Cardena G, Liu J, Keh A, Pollock JS, Bradley J, Thiru S, Braverman IM, Desai KM (1995) The Golgi association of endothelial nitric oxide synthase is necessary for the efficient synthesis of nitric oxide. J Biol Chem 270:17641–17644
18. Zhang Q, Church JE, Jagnandan D, Catravas JD, Sessa WC, Fulton D (2006) Functional relevance of Golgi- and plasma membrane-localized endothelial NOS synthase in reconstituted endothelial cells. Arterioscler Thromb Vasc Biol 26:1015–1021
19. McCabe TJ, Fulton D, Roman LJ, Sessa WC (2000) Enhanced electron flux and reduced calmodulin dissociation may explain “calcium-independent” eNOS activation by phosphorylation. J Biol Chem 275:6123–6128
20. Murohara T, Witzenbichler B, Spyridopoulos I, Asahara T, Ding B, Sullivan A, Losordo DW, Isner JM (1999) Role of endothelial nitric oxide synthase in endothelial cell migration. Arterioscler Thromb Vasc Biol 19:1156–1161
21. Guo J-P, Murohara T, Panday MM, Lefer AM (1996) Nitric oxide promotes endothelial cell proliferation: role in inhibiting restenosis. Circulation 92:I–750. Abstract
22. van der Zee R, Murohara T, Luo Z et al (1997) Vascular endothelial growth factor/vascular permeability factor augments nitric oxide release from quiescent rabbit and human vascular endothelium. Circulation 95:1030–1037
23. Hood JD, Meininger CJ, Ziche M, Granger HJ (1998) VEGF upregulates ecNOS message, protein, and NO production in human endothelial cells. Am J Physiol 274:H1054–H1058
24. Genís L, Gonzalo P, Tutor AS, Gálvez BG, Martínez-Ruiz A, Zaragoza C, Lamas S, Tryggvason K, Apte SS, Arroyo AG (2007) Functional interplay between endothelial nitric oxide synthase and membrane type 1–matrix metalloproteinase in migrating endothelial cells. Blood 110:2916–2923
25. Fulton D, Gratton JP, McCabe TJ, Fontana J, Fujio Y, Walsh K, Franke TF, Papapetropoulos A, Sessa WC (1999) Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 399:597–601
26. Scotland RS, Morales-Ruiz M, Chen Y, Yu J, Rudic RD, Fulton D, Gratton JP, Sessa WC (2002) Functional reconstitution of endothelial nitric oxide synthase reveals the importance of serine 1179 in endothelium-dependent vasomotion. Circ Res 90:904–910
27. Erwin PA, Lin AJ, Golan DE, Michel T (2005) Receptor-regulated dynamic s-nitrosylation of endothelial nitric-oxide synthase in vascular endothelial cells. J Biol Chem 280:19888–19894
28. Ando A, Yang A, Mori K, Yamada H, Yamada E, Takahashi K, Saikia J, Kim M, Melia M, Fishman M, Huang P, Campochiaro PA (2002) Nitric oxide is proangiogenic in the retina and choroid. J Cell Physiol 191:116–124
29. Tsutsui M, Shimokawa H, Morishita T, Nakashima Y, Yanagihara N (2006) Development of genetically engineered mice lacking all three nitric oxide synthases. J Pharmacol Sci 102:147–154
30. Bulotta S, Cerullo A, Barsacchi R, De Palma C, Rotiroti D, Clementi E, Borgese N (2006) Endothelial nitric oxide synthase is segregated from caveolin-1 and localizes to the leading edge of migrating cells. Exp Cell Res 312:877–889
31. Chatterjee S, Cao S, Peterson TE, Simari RD, Shah V (2003) Inhibition of GTP-dependent vesicle trafficking impairs internalization of plasmalemmal eNOS and cellular nitric oxide production. J Cell Sci 116(Pt 17):3645–3655
32. Lassalle P, Molet S, Janin A, Heyden JV, Tavernier J, Fiers W, Devos R, Tonnel AB (1996) ESM-1 is a novel human endothelial cell-specific molecule expressed in lung and regulated by cytokines. J Biol Chem 271:20458–20464
33. Roudnicky F, Poyet C, Wild P, Krampitz S, Negrini F, Huggenberger R, Rogler A, Stöhr R, Hartmann A, Provenzano M, Otto VI, Detmar M (2013) Endocan is upregulated on tumor vessels in invasive bladder cancer where it mediates VEGF-A-induced angiogenesis. Cancer Res 73:1097–1106
34. Feron O, Belhassen L, Kobzik L, Smith TW, Kelly RA, Michel T (1996) Endothelial nitric oxide synthase targeting to caveolae: specific interactions with caveolin isoforms in cardiac myocytes and endothelial cells. J Biol Chem 271:22810–22814
35. Ju H, Zou R, Venema VJ, Venema RC (1997) Direct interaction of endothelial nitric-oxide synthase and caveolin-1 inhibits synthase activity. J Biol Chem 72:18522–18525
36. Brouet A, Sonveaux P, Dessy C, Moniotte S, Balligand JL, Feron O (2001) Hsp90 and caveolin are key targets for the proangiogenic nitric oxide—mediated effects of statins. Circ Res 89:866–873
37. Bernatchez PN, Bauer PM, Yu J, Prendergast JS, He P, Sessa WC (2005) Dissecting the molecular control of endothelial NO synthase by caveolin-1 using cell-permeable peptides. Proc Natl Acad Sci USA 102:761–766
38. Papapetropoulos A, Garcia-Cardena G, Madri JA, Sessa WC (1997) Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J Clin Invest 100:3131–3139
39. Bussolati B, Dunk C, Grohman M, Kontos CD, Mason J, Ahmed A (2001) Vascular endothelial growth factor receptor-1 modulates vascular endothelial growth factor-mediated angiogenesis via nitric oxide. Am J Pathol 159:993–1008
40. Nausch LW, Ledoux J, Bonev AD, Nelson MT, Dostmann WR (2008) Differential patterning of cGMP in vascular smooth muscle cells revealed by single GFP-linked biosensors. Proc Natl Acad Sci USA 105:365–370
41. Senthilkumar A, Smith RD, Khitha J, Arora N, Veerareddy S et al (2007) Sildenafil promotes ischemia-induced angiogenesis through a PKG-dependent pathway. Arterioscler Thromb Vasc Biol 27:1947–1954
42. Aicher A, Heeschen C, Feil S, Hofmann F, Mendelsohn ME, Feil R, Dimmeler S (2009) cGMP-dependent protein kinase I is crucial for angiogenesis and postnatal vasculogenesis. PLoS One 4:e4879
43. Zhang R, Wang L, Zhang L, Chen J, Zhu Z, Zhang Z, Chopp M (2003) Nitric oxide enhances angiogenesis via the synthesis of vascular endothelial growth factor and cGMP after stroke in the rat. Circ Res 92:308–313