PAI-1-dependent endothelial cell death determines severity of radiation-induced intestinal injury

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Abderrahmani, Rym ^a   François, Agnes ^a   Buard, Valerie ^a   Tarlet, Georges ^a   Blirando, Karl ^a   Hneino, Mohammad ^a   Vaurijoux, Aurelie ^a   Benderitter, Marc ^a   Sabourin, Jean Christophe ^b   Milliat, Fabien ^a  

^a INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE IRSN   (France)

^b ROUEN UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN KINASE B; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PTEN PROTEIN, MOUSE; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; ENDOTHELIUM CELL; ENZYME ACTIVATION; GENETIC DISORDER; HUMAN; HUMAN CELL; IN VIVO STUDY; INTESTINE INJURY; IRRADIATION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; RADIATION INJURY; RADIOSENSITIVITY; VASCULAR ENDOTHELIUM; ANIMAL; C57BL MOUSE; CELL CULTURE; DRUG ANTAGONISM; GENETICS; INJURY; INTESTINE; METABOLISM; MOUSE MUTANT; RADIATION EXPOSURE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; UMBILICAL VEIN ENDOTHELIAL CELL;

MUS;

ANIMALS; APOPTOSIS; CELLS, CULTURED; ENDOTHELIAL CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INTESTINES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84860363257     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035740     Document Type: Article

References (52)

1. Bentzen SM, (2006) Preventing or reducing late side effects of radiation therapy: radiobiology meets molecular pathology. Nat Rev Cancer 6: 702-713.
2. Stone HB, Coleman CN, Anscher MS, McBride WH, (2003) Effects of radiation on normal tissue: consequences and mechanisms. Lancet Oncol 4: 529-536.
3. Denham JW, Hauer-Jensen M, (2002) The radiotherapeutic injury-a complex 'wound'. Radiother Oncol 63: 129-145.
4. Kohler HP, Grant PJ, (2000) Plasminogen-activator inhibitor type 1 and coronary artery disease. N Engl J Med 342: 1792-1801.
5. Eitzman DT, McCoy RD, Zheng X, Fay WP, Shen T, et al. (1996) Bleomycin-induced pulmonary fibrosis in transgenic mice that either lack or overexpress the murine plasminogen activator inhibitor-1 gene. J Clin Invest 97: 232-237.
6. Eitzman DT, Westrick RJ, Xu Z, Tyson J, Ginsburg D, (2000) Plasminogen activator inhibitor-1 deficiency protects against atherosclerosis progression in the mouse carotid artery. Blood 96: 4212-4215.
7. Hattori N, Degen JL, Sisson TH, Liu H, Moore BB, et al. (2000) Bleomycin-induced pulmonary fibrosis in fibrinogen-null mice. J Clin Invest 106: 1341-1350.
8. Takeshita K, Hayashi M, Iino S, Kondo T, Inden Y, et al. (2004) Increased expression of plasminogen activator inhibitor-1 in cardiomyocytes contributes to cardiac fibrosis after myocardial infarction. Am J Pathol 164: 449-456.
9. Wang J, Boerma M, Fu Q, Hauer-Jensen M, (2007) Significance of endothelial dysfunction in the pathogenesis of early and delayed radiation enteropathy. World J Gastroenterol 13: 3047-3055.
10. Artman T, Schilling D, Gnann J, Molls M, Multhoff G, et al. (2010) Irradiation-induced regulation of plasminogen activator inhibitor type-1 and vascular endothelial growth factor in six human squamous cell carcinoma lines of the head and neck. Int J Radiat Oncol Biol Phys 76: 574-582.
11. Hageman J, Eggen BJ, Rozema T, Damman K, Kampinga HH, et al. (2005) Radiation and transforming growth factor-beta cooperate in transcriptional activation of the profibrotic plasminogen activator inhibitor-1 gene. Clin Cancer Res 11: 5956-5964.
12. Milliat F, Sabourin JC, Tarlet G, Holler V, Deutsch E, et al. (2008) Essential role of plasminogen activator inhibitor type-1 in radiation enteropathy. Am J Pathol 172: 691-701.
13. Zhao W, O'Malley Y, Robbins ME, (1999) Irradiation of rat mesangial cells alters the expression of gene products associated with the development of renal fibrosis. Radiat Res 152: 160-169.
14. Zhao W, Spitz DR, Oberley LW, Robbins ME, (2001) Redox modulation of the pro-fibrogenic mediator plasminogen activator inhibitor-1 following ionizing radiation. Cancer Res 61: 5537-5543.
15. Brown NJ, Nakamura S, Ma L, Nakamura I, Donnert E, et al. (2000) Aldosterone modulates plasminogen activator inhibitor-1 and glomerulosclerosis in vivo. Kidney Int 58: 1219-1227.
16. Oikawa T, Freeman M, Lo W, Vaughan DE, Fogo A, (1997) Modulation of plasminogen activator inhibitor-1 in vivo: a new mechanism for the anti-fibrotic effect of renin-angiotensin inhibition. Kidney Int 51: 164-172.
17. Vozenin-Brotons MC, Milliat F, Linard C, Strup C, Francois A, et al. (2004) Gene expression profile in human late radiation enteritis obtained by high-density cDNA array hybridization. Radiat Res 161: 299-311.
18. Collins-Underwood JR, Zhao W, Sharpe JG, Robbins ME, (2008) NADPH oxidase mediates radiation-induced oxidative stress in rat brain microvascular endothelial cells. Free Radic Biol Med 45: 929-938.
19. Scharpfenecker M, Kruse JJ, Sprong D, Russell NS, Ten Dijke P, et al. (2009) Ionizing radiation shifts the PAI-1/ID-1 balance and activates notch signaling in endothelial cells. Int J Radiat Oncol Biol Phys 73: 506-513.
20. Paris F, Fuks Z, Kang A, Capodieci P, Juan G, et al. (2001) Endothelial apoptosis as the primary lesion initiating intestinal radiation damage in mice. Science 293: 293-297.
21. Potten CS, Merritt A, Hickman J, Hall P, Faranda A, (1994) Characterization of radiation-induced apoptosis in the small intestine and its biological implications. Int J Radiat Biol 65: 71-78.
22. Balsara RD, Ploplis VA, (2008) Plasminogen activator inhibitor-1: the double-edged sword in apoptosis. Thromb Haemost 100: 1029-1036.
23. Lademann UA, Romer MU, (2008) Regulation of programmed cell death by plasminogen activator inhibitor type 1 (PAI-1). Thromb Haemost 100: 1041-1046.
24. Schneider DJ, Chen Y, Sobel BE, (2008) The effect of plasminogen activator inhibitor type 1 on apoptosis. Thromb Haemost 100: 1037-1040.
25. Soeda S, Oda M, Ochiai T, Shimeno H, (2001) Deficient release of plasminogen activator inhibitor-1 from astrocytes triggers apoptosis in neuronal cells. Brain Res Mol Brain Res 91: 96-103.
26. Bajou K, Peng H, Laug WE, Maillard C, Noel A, et al. (2008) Plasminogen activator inhibitor-1 protects endothelial cells from FasL-mediated apoptosis. Cancer Cell 14: 324-334.
27. Chen Y, Budd RC, Kelm RJ Jr, Sobel BE, Schneider DJ, (2006) Augmentation of proliferation of vascular smooth muscle cells by plasminogen activator inhibitor type 1. Arterioscler Thromb Vasc Biol 26: 1777-1783.
28. Chen Y, Kelm RJ Jr, Budd RC, Sobel BE, Schneider DJ, (2004) Inhibition of apoptosis and caspase-3 in vascular smooth muscle cells by plasminogen activator inhibitor type-1. J Cell Biochem 92: 178-188.
29. Balsara RD, Castellino FJ, Ploplis VA, (2006) A novel function of plasminogen activator inhibitor-1 in modulation of the AKT pathway in wild-type and plasminogen activator inhibitor-1-deficient endothelial cells. J Biol Chem 281: 22527-22536.
30. Ploplis VA, Balsara R, Sandoval-Cooper MJ, Yin ZJ, Batten J, et al. (2004) Enhanced in vitro proliferation of aortic endothelial cells from plasminogen activator inhibitor-1-deficient mice. J Biol Chem 279: 6143-6151.
31. Abderrahmani R, Francois A, Buard V, Benderitter M, Sabourin JC, et al. (2009) Effects of pharmacological inhibition and genetic deficiency of plasminogen activator inhibitor-1 in radiation-induced intestinal injury. Int J Radiat Oncol Biol Phys 74: 942-948.
32. Andreyev J, (2005) Gastrointestinal complications of pelvic radiotherapy: are they of any importance? Gut 54: 1051-1054.
33. Rotolo JA, Maj JG, Feldman R, Ren D, Haimovitz-Friedman A, et al. (2008) Bax and Bak do not exhibit functional redundancy in mediating radiation-induced endothelial apoptosis in the intestinal mucosa. Int J Radiat Oncol Biol Phys 70: 804-815.
34. Bhanja P, Saha S, Kabarriti R, Liu L, Roy-Chowdhury N, et al. (2009) Protective role of R-spondin1, an intestinal stem cell growth factor, against radiation-induced gastrointestinal syndrome in mice. PLoS One 4: e8014.
35. Burdelya LG, Krivokrysenko VI, Tallant TC, Strom E, Gleiberman AS, et al. (2008) An agonist of toll-like receptor 5 has radioprotective activity in mouse and primate models. Science 320: 226-230.
36. Cho CH, Kammerer RA, Lee HJ, Yasunaga K, Kim KT, et al. (2004) Designed angiopoietin-1 variant, COMP-Ang1, protects against radiation-induced endothelial cell apoptosis. Proc Natl Acad Sci U S A 101: 5553-5558.
37. Maxhimer JB, Soto-Pantoja DR, Ridnour LA, Shih HB, Degraff WG, et al. (2009) Radioprotection in normal tissue and delayed tumor growth by blockade of CD47 signaling. Sci Transl Med 1: 3ra7.
38. Qiu W, Carson-Walter EB, Liu H, Epperly M, Greenberger JS, et al. (2008) PUMA regulates intestinal progenitor cell radiosensitivity and gastrointestinal syndrome. Cell Stem Cell 2: 576-583.
39. Schuller BW, Binns PJ, Riley KJ, Ma L, Hawthorne MF, et al. (2006) Selective irradiation of the vascular endothelium has no effect on the survival of murine intestinal crypt stem cells. Proc Natl Acad Sci U S A 103: 3787-3792.
40. Schuller BW, Rogers AB, Cormier KS, Riley KJ, Binns PJ, et al. (2007) No significant endothelial apoptosis in the radiation-induced gastrointestinal syndrome. Int J Radiat Oncol Biol Phys 68: 205-210.
41. Brown M, (2008) What causes the radiation gastrointestinal syndrome?: overview. Int J Radiat Oncol Biol Phys 70: 799-800.
42. Gudkov AV, Gleiberman A, (2008) In regard to Schuller,et Al. (Int J Radiat Oncol Biol Phys 2007;68:205-210). Int J Radiat Oncol Biol Phys 70: 800-801; author reply 802-803.
43. Zheng H, Wang J, Koteliansky VE, Gotwals PJ, Hauer-Jensen M, (2000) Recombinant soluble transforming growth factor beta type II receptor ameliorates radiation enteropathy in mice. Gastroenterology 119: 1286-1296.
44. Bajou K, Noel A, Gerard RD, Masson V, Brunner N, et al. (1998) Absence of host plasminogen activator inhibitor 1 prevents cancer invasion and vascularization. Nat Med 4: 923-928.
45. Soff GA, Sanderowitz J, Gately S, Verrusio E, Weiss I, et al. (1995) Expression of plasminogen activator inhibitor type 1 by human prostate carcinoma cells inhibits primary tumor growth, tumor-associated angiogenesis, and metastasis to lung and liver in an athymic mouse model. J Clin Invest 96: 2593-2600.
46. Stefansson S, Petitclerc E, Wong MK, McMahon GA, Brooks PC, et al. (2001) Inhibition of angiogenesis in vivo by plasminogen activator inhibitor-1. J Biol Chem 276: 8135-8141.
47. Chen SC, Henry DO, Reczek PR, Wong MK, (2008) Plasminogen activator inhibitor-1 inhibits prostate tumor growth through endothelial apoptosis. Mol Cancer Ther 7: 1227-1236.
48. Devy L, Blacher S, Grignet-Debrus C, Bajou K, Masson V, et al. (2002) The pro- or antiangiogenic effect of plasminogen activator inhibitor 1 is dose dependent. Faseb J 16: 147-154.
49. Bonnaud S, Niaudet C, Pottier G, Gaugler MH, Millour J, et al. (2007) Sphingosine-1-phosphate protects proliferating endothelial cells from ceramide-induced apoptosis but not from DNA damage-induced mitotic death. Cancer Res 67: 1803-1811.
50. Bonnaud S, Niaudet C, Legoux F, Corre I, Delpon G, et al. (2010) Sphingosine-1-phosphate activates the AKT pathway to protect small intestines from radiation-induced endothelial apoptosis. Cancer Res 70: 9905-9915.
51. Fujio Y, Walsh K, (1999) Akt mediates cytoprotection of endothelial cells by vascular endothelial growth factor in an anchorage-dependent manner. J Biol Chem 274: 16349-16354.
52. Jin YP, Fishbein MC, Said JW, Jindra PT, Rajalingam R, et al. (2004) Anti-HLA class I antibody-mediated activation of the PI3K/Akt signaling pathway and induction of Bcl-2 and Bcl-xL expression in endothelial cells. Hum Immunol 65: 291-302.