Arsenic requires sphingosine-1-phosphate type 1 receptors to induce angiogenic genes and endothelial cell remodeling

American Journal of Pathology

Volumn 174, Issue 5, 2009, Pages 1949-1958

  Straub, Adam C ^a   Klei, Linda R ^a   Stolz, Donna B ^b   Barchowsky, Aaron ^a,c  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 2 (3 OCTYLPHENYLCARBAMOYL)ETHYL PHOSPHATE; ARSENIC; DRINKING WATER; GUANOSINE TRIPHOSPHATASE; PERTUSSIS TOXIN; RAC1 PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SPHINGOSINE 1 PHOSPHATE RECEPTOR; SPHINGOSINE 1 PHOSPHATE RECEPTOR INHIBITOR; UNCLASSIFIED DRUG; DRUG DERIVATIVE; HEME OXYGENASE 1; HMOX1 PROTEIN, HUMAN; IL8 PROTEIN, HUMAN; INTERLEUKIN 8; LYSOPHOSPHOLIPID; MESSENGER RNA; RAC PROTEIN; SMALL INTERFERING RNA; SPHINGOSINE; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE 1-PHOSPHATE; SUPEROXIDE;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARSENIC POISONING; ARTICLE; CANCER RISK; CAPILLARY PROLIFERATION; CARDIOVASCULAR DISEASE; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; IN VIVO STUDY; ISCHEMIC HEART DISEASE; LIVER SINUSOID; MALE; MICROVASCULARIZATION; MOUSE; NONHUMAN; PERIPHERAL VASCULAR DISEASE; PORTAL HYPERTENSION; PRIORITY JOURNAL; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; LIVER; METABOLISM; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UMBILICAL VEIN; VASCULAR ENDOTHELIUM; VASCULARIZATION;

ANIMALS; ARSENIC; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; HEME OXYGENASE-1; INTERLEUKIN-8; LIVER; LYSOPHOSPHOLIPIDS; MALE; MICE; MICE, INBRED C57BL; NEOVASCULARIZATION, PHYSIOLOGIC; PERTUSSIS TOXIN; RAC GTP-BINDING PROTEINS; RECEPTORS, LYSOSPHINGOLIPID; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; SPHINGOSINE; SUPEROXIDES; UMBILICAL VEINS;

EID: 65649086447     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2009.081016     Document Type: Article

References (60)

1. Yuan Y, Marshall G, Ferreccio C, Steinmaus C, Selvin S, Liaw J, Bates MN, Smith AH: Acute myocardial infarction mortality in comparison with lung and bladder cancer mortality in arsenic-exposed region II of Chile from 1950 to 2000. Am J Epidemiol 2007, 166:1381-1391
2. Wang CH, Hsiao CK, Chen CL, Hsu LI, Chiou HY, Chen SY, Hsueh YM, Wu MM, Chen CJ: A review of the epidemiologic literature on the role of environmental arsenic exposure and cardiovascular diseases. Toxicol Appl Pharmacol 2007, 222:315-326 (Pubitemid 47198277)
3. Chen Y, Factor-Litvak P, Howe GR, Graziano JH, Brandt-Rauf P, Parvez F, van Geen A, Ahsan H: Arsenic exposure from drinking water. Dietary intakes of B vitamins and folate, and risk of high blood pressure in Bangladesh: a population-based, cross-sectional study. Am J Epidemiol 2007, 165:541-552
4. Kwok RK, Mendola P, Liu ZY, Savitz DA, Heiss G, Ling HL, Xia Y, Lobdell D, Zeng D, Thorp Jr JM, Creason JP, Mumford JL: Drinking water arsenic exposure and blood pressure in healthy women of reproductive age in Inner Mongolia. China Toxicol Appl Pharmacol 2007, 222:337-343 (Pubitemid 47202018)
5. Hordijk PL: Regulation of NADPH oxidases: the role of Rac proteins. Circ Res 2006, 98:453-462 (Pubitemid 43755303)
6. Lee MY, Griendling KK: Redox signaling, vascular function, and hypertension. Antioxid Redox Signal 2008, 10:1045-1059
7. Smith KR, Klei LR, Barchowsky A: Arsenite stimulates plasma membrane NADPH oxidase in vascular endothelial cells. Am J Physiol 2001, 280:L442-L449 (Pubitemid 32473194)
8. Qian Y, Liu KJ, Chen Y, Flynn DC, Castranova V, Shi X: Cdc42 regulates arsenic-induced NADPH oxidase activation and cell migration through actin filament reorganization. J Biol Chem 2005, 280: 3875-3884 (Pubitemid 40223857)
9. Lynn S, Gurr JR, Lai HT, Jan KY: NADH oxidase activation is involved in arsenite-induced oxidative DNA damage in human vascular smooth muscle cells. Circ Res 2000, 86:514-519 (Pubitemid 30165042)
10. Tan W, Palmby TR, Gavard J, Amornphimoltham P, Zheng Y, Gutkind JS: An essential role for Rac1 in endothelial cell function and vascular development. FASEB J 2008, 22: 1829-1838
11. Klei LR, Barchowsky A: Positive signaling interactions between arsenic and ethanol for angiogenic gene induction in human microvascular endothelial cells. Toxicol Sci 2008, 102:319-327
12. Straub AC, Stolz DB, Ross MA, Hernandez-Zavala A, Soucy NV, Klei LR, Barchowsky A: Arsenic stimulates sinusoidal endothelial cell capillarization and vessel remodeling in mouse liver. Hepatology 2007, 45:205-212 (Pubitemid 46144380)
13. Basu P, Ghosh RN, Grove LE, Klei L, Barchowsky A: Angiogenic potential of 3-nitro-4-hydroxy benzene arsonic acid (roxarsone). Environ Health Perspect 2008, 116:520-523
14. Soucy NV, Ihnat MA, Kamat CD, Hess L, Post MJ, Klei LR, Clark C, Barchowsky A: Arsenic stimulates angiogenesis and tumorigenesis in vivo. Toxicol Sci 2003, 76:271-279 (Pubitemid 38035420)
15. Soucy NV, Mayka D, Klei LR, Nemec AA, Bauer JA, Barchowsky A: Neovascularization and angiogenic gene expression following chronic arsenic exposure in mice. Cardiovasc Toxicol 2005, 5:29-42 (Pubitemid 40655441)
16. Kamat CD, Green DE, Curilla S, Warnke L, Hamilton JW, Sturup S, Clark C, Ihnat MA: Role of HIF signaling on tumorigenesis in response to chronic low-dose arsenic administration. Toxicol Sci 2005, 86:248-257 (Pubitemid 41418637)
17. Liu B, Pan SG, Dong XS, Qiao HQ, Jiang HC, Krissansen GW, Sun XY: Opposing effects of arsenic trioxide on hepatocellular carcinomas in mice. Cancer Science 2006, 97:675-681 (Pubitemid 44056616)
18. DeLeve LD: Hepatic microvasculature in liver injury. Semin Liver Dis 2007, 27:390-400 (Pubitemid 350071839)
19. Elvevold K, Smedsrod B, Martinez I: The liver sinusoidal endothelial cell: a cell type of controversial and confusing identity. Am J Physiol Gastrointest Liver Physiol 2008, 294:G391-G400
20. Le Couteur DG, Cogger VC, McCuskey RS, de Cabo R, Smedsrod B, Sorensen KK, Warren A, Fraser R: Age-related changes in the liver sinusoidal endothelium: a mechanism for dyslipidemia. Ann NY Acad Sci 2007, 1114:79-87 (Pubitemid 350070372)
21. Straub AC, Clark KA, Ross MA, Chandra AG, Li S, Gao X, Pagano PJ, Stolz DB, Barchowsky A: Arsenic-stimulated liver sinusoidal capillarization in mice requires NADPH oxidase-generated superoxide. J Clin Invest 2008, 118:3980-3989
22. Straub AC, Stolz DB, Vin H, Ross MA, Soucy NV, Klei LR, Barchowsky A: Low level arsenic promotes progressive inflammatory angiogenesis and liver blood vessel remodeling in mice. Toxicol Appl Pharmacol 2007, 222:327-336 (Pubitemid 47198271)
23. Seglen PO: Preparation of isolated rat liver cells. Methods Cell Biol 1976, 13:29-83
24. Ross MA, Sander CM, Kleeb TB, Watkins SC, Stolz DB: Spatiotemporal expression of angiogenesis growth factor receptors during the revascularization of regenerating rat liver. Hepatology 2001, 34:1135-1148 (Pubitemid 33096586)
25. Barchowsky A, Dudek EJ, Treadwell MD, Wetterhahn KE: Arsenic induces oxidant stress and NF-kappaB activation in cultured aortic endothelial cells. Free Radic Biol Med 1996, 21:783-790 (Pubitemid 26365274)
26. Gao Y, Dickerson JB, Guo F, Zheng J, Zheng Y: Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc Natl Acad Sci USA 2004, 101:7618-7623 (Pubitemid 38658078)
27. Balthasar S, Samulin J, Ahlgren H, Bergelin N, Lundqvist M, Toescu EC, Eggo MC, Tornquist K: Sphingosine 1-phosphate receptor expression profile and regulation of migration in human thyroid cancer cells. Biochem J 2006, 398:547-556 (Pubitemid 44453400)
28. Skaznik-Wikiel ME, Kaneko-Tarui T, Kashiwagi A, Pru JK: Sphingosine- 1-phosphate receptor expression and signaling correlate with uterine prostaglandin-endoperoxide synthase 2 expression and angiogenesis during early pregnancy. Biol Reprod 2006, 74:569-576 (Pubitemid 43271362)
29. Barchowsky A, Klei LR, Dudek EJ, Swartz HM, James PE: Stimulation of reactive oxygen, but not reactive nitrogen species, in vascular endothelial cells exposed to low levels of arsenite. Free Radic Biol Med 1999, 27:1405-1412 (Pubitemid 30001503)
30. Davis MD, Clemens JJ, Macdonald TL, Lynch KR: Sphingosine 1-phosphate analogs as receptor antagonists. J Biol Chem 2005, 280:9833-9841 (Pubitemid 40395829)
31. Peters SL, Alewijnse AE: Sphingosine-1-phosphate signaling in the cardiovascular system. Curr Opin Pharmacol 2007, 7:186-192 (Pubitemid 46404742)
32. Lin CI, Chen CN, Lin PW, Lee H: Sphingosine 1-phosphate regulates inflammation-related genes in human endothelial cells through S1P1 and S1P3. Biochem Biophys Res Commun 2007, 355:895-901 (Pubitemid 46366912)
33. Chae SS, Paik JH, Furneaux H, Hla T: Requirement for sphingosine 1-phosphate receptor-1 in tumor angiogenesis demonstrated by in vivo RNA interference. J Clin Invest 2004, 114:1082-1089 (Pubitemid 39578697)
34. Richard DE, Vouret-Craviari V, Pouyssegur J: Angiogenesis and Gprotein- coupled receptors: signals that bridge the gap. Oncogene 2001, 20:1556-1562 (Pubitemid 32336843)
35. Brinkmann V: Sphingosine 1-phosphate receptors in health and disease: mechanistic insights from gene deletion studies and reverse pharmacology. Pharmacol Ther 2007, 115:84-105 (Pubitemid 46990553)
36. Gonzalez E, Kou R, Michel T: Rac1 modulates sphingosine 1-phosphate- mediated activation of phosphoinositide 3-kinase/Akt signaling pathways in vascular endothelial cells. J Biol Chem 2006, 281: 3210-3216 (Pubitemid 43845932)
37. Allende ML, Yamashita T, Proia RL: G-protein-coupled receptor S1P1 acts within endothelial cells to regulate vascular maturation. Blood 2003, 102:3665-3667 (Pubitemid 37409386)
38. Barchowsky A, Roussel RR, Klei LR, James PE, Ganju N, Smith KR, Dudek EJ: Low levels of arsenic trioxide stimulate proliferative signals in primary vascular cells without activating stress effector pathways. Toxicol Appl Pharmacol 1999, 159:65-75 (Pubitemid 29404762)
39. Catarzi S, Giannoni E, Favilli F, Meacci E, Iantomasi T, Vincenzini MT: Sphingosine 1-phosphate stimulation of NADPH oxidase activity: relationship with platelet-derived growth factor receptor and c-Src kinase. Biochim Biophys Acta 2007, 1770:872-883 (Pubitemid 46617027)
40. Roztocil E, Nicholl SM, Davies MG: Sphingosine-1-phosphate-induced oxygen free radical generation in smooth muscle cell migration requires Galpha12/13 protein-mediated phospholipase C activation. J Vasc Surg 2007, 46:1253-1259 (Pubitemid 350267071)
41. Ushio-Fukai M, Tang Y, Fukai T, Dikalov SI, Ma Y, Fujimoto M, Quinn MT, Pagano PJ, Johnson C, Alexander RW: Novel role of gp91(phox)-containing NAD(P)H oxidase in vascular endothelial growth factor-induced signaling and angiogenesis. Circ Res 2002, 91:1160-1167 (Pubitemid 36076365)
42. Ushio-Fukai M, Alexander RW: Reactive oxygen species as mediators of angiogenesis signaling: role of NAD(P)H oxidase. Mol Cell Biochem 2004, 264:85-97 (Pubitemid 39366107)
43. Kitchin KT, Wallace K: The role of protein binding of trivalent arsenicals in arsenic carcinogenesis and toxicity. J Inorg Biochem 2008, 102:532-539
44. Lu M, Wang H, Wang Z, Li XF, Le XC: Identification of reactive cysteines in a protein using arsenic labeling and collision-induced dissociation tandem mass spectrometry. J Proteome Res 2008, 7:3080-3090
45. Carter DE, Aposhian HV, Gandolfi AJ: The metabolism of inorganic arsenic oxides, gallium arsenide, and arsine: a toxicochemical review. Toxicol Appl Pharmacol 2003, 193:309-334 (Pubitemid 37543540)
46. Kokkola T, Savinainen JR, Monkkonen KS, Retamal MD, Laitinen JT: S-nitrosothiols modulate G protein-coupled receptor signaling in a reversible and highly receptor-specific manner. BMC Cell Biol 2005, 6:21 (Pubitemid 41357615)
47. Wess J, Han SJ, Kim SK, Jacobson KA, Li JH: Conformational changes involved in G-protein-coupled-receptor activation. Trends Pharmacol Sci 2008, 29:616-625
48. Ozawa K, Whalen EJ, Nelson CD, Mu Y, Hess DT, Lefkowitz RJ, Stamler JS: S-nitrosylation of beta-arrestin regulates beta-adrenergic receptor trafficking. Mol Cell 2008, 31:395-405
49. Fujiwara Y, Osborne DA, Walker MD, Wang DA, Bautista DA, Liliom K, Van Brocklyn JR, Parrill AL, Tigyi G: Identification of the hydrophobic ligand binding pocket of the S1P1 receptor. J Biol Chem 2007, 282:2374-2385 (Pubitemid 47076755)
50. Leclerc PC, Lanctot PM, Auger-Messier M, Escher E, Leduc R, Guillemette G: S-nitrosylation of cysteine 289 of the AT1 receptor decreases its binding affinity for angiotensin II. Br J Pharmacol 2006, 148:306-313 (Pubitemid 43801178)
51. Albini A, Tosetti F, Benelli R, Noonan DM: Tumor inflammatory angiogenesis and its chemoprevention. Cancer Res 2005, 65:10637-10641 (Pubitemid 41713327)
52. Ramsauer M, D'Amore PA: Getting Tie(2)d up in angiogenesis. J Clin Invest 2002, 110:1615-1617
53. Pi J, Qu W, Reece JM, Kumagai Y, Waalkes MP: Transcription factor Nrf2 activation by inorganic arsenic in cultured keratinocytes: involvement of hydrogen peroxide. Exp Cell Res 2003, 290:234-245 (Pubitemid 37272168)
54. He X, Chen MG, Lin GX, Ma Q: Arsenic induces NAD(P)H-quinone oxidoreductase I by disrupting the Nrf2 x Keap1 x Cul3 complex and recruiting Nrf2 x Maf to the antioxidant response element enhancer. J Biol Chem 2006, 281:23620-23631 (Pubitemid 44274137)
55. Alam J, Cook JL: Transcriptional regulation of the heme oxygenase-1 gene via the stress response element pathway. Curr Pharm Des 2003, 9:2499-2511 (Pubitemid 37236369)
56. Gong P, Stewart D, Hu B, Vinson C, Alam J: Multiple basic-leucine zipper proteins regulate induction of the mouse heme oxygenase-1 gene by arsenite. Arch Biochem Biophys 2002, 405:265-274 (Pubitemid 35191741)
57. Ikeda H, Yatomi Y, Yanase M, Satoh H, Maekawa H, Ogata I, Ozaki Y, Takuwa Y, Mochida S, Fujiwara K: Biological activities of novel lipid mediator sphingosine 1-phosphate in rat hepatic stellate cells. Am J Physiol Gastrointest Liver Physiol 2000, 279:G304-G310
58. Krump-Konvalinkova V, Yasuda S, Rubic T, Makarova N, Mages J, Erl W, Vosseler C, Kirkpatrick CJ, Tigyi G, Siess W: Stable knock-down of the sphingosine 1-phosphate receptor S1P1 influences multiple functions of human endothelial cells. Arterioscler Thromb Vasc Biol 2005, 25: 546-552 (Pubitemid 40315676)
59. Hla T, Venkataraman K, Michaud J: The vascular S1P gradient- Cellular sources and biological significance. Biochim Biophys Acta 2008, 1781:477-482
60. Venkataraman K, Lee YM, Michaud J, Thangada S, Ai Y, Bonkovsky HL, Parikh NS, Habrukowich C, Hla T: Vascular endothelium as a contributor of plasma sphingosine 1-phosphate. Circ Res 2008, 102:669-676