Constitutively active endothelial Notch4 causes lung arteriovenous shunts in mice

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 298, Issue 2, 2010, Pages

  Miniati, Doug ^a,b   Jelin, Eric B ^a,b   Ng, Jennifer ^a,c   Wu, Jianfeng ^b   Carlson, Timothy R ^a,d   Wu, Xiaoqing ^a,e   Looney, Mark R ^a   Wang, Rong A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NEW YORK MEDICAL COLLEGE   (United States)

^d Two Prudential Plaza   (United States)

^e Data Virtuoso Inc   (United States)

Author keywords

Endothelium; Notch; Pulmonary; Vascular

Indexed keywords

NOTCH4 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIAL GAS; ARTERIOVENOUS MALFORMATION; ARTICLE; ENDOTHELIUM CELL; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; LUNG BLOOD VESSEL; LUNG HEMORRHAGE; MORBIDITY; MORTALITY; MOUSE; NONHUMAN; PATHOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY ARTERIOVENOUS FISTULA; RESPIRATORY FAILURE; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALS; ARTERIOVENOUS MALFORMATIONS; EMBRYO, MAMMALIAN; ENDOTHELIUM, VASCULAR; HUMANS; LUNG; MICE; MODELS, ANIMAL; MUTATION; PROTO-ONCOGENE PROTEINS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; TISSUE CULTURE TECHNIQUES;

EID: 74949129155     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00188.2009     Document Type: Article

References (44)

1. Bedogni B, Warneke JA, Nickoloff BJ, Giaccia AJ, Powell MB. Notch1 is an effector of Akt and hypoxia in melanoma development. J Clin Invest 118: 3660-3670, 2008.
2. Bernstein HS, Brook MM, Silverman NH, Bristow J. Development of pulmonary arteriovenous fistulae in children after cavopulmonary shunt. Circulation 92: II309-II314, 1995.
3. Braren R, Hu H, Kim YH, Beggs HE, Reichardt LF, Wang R. Endothelial FAK is essential for vascular network stability, cell survival, and lamellipodial formation. J Cell Biol 172: 151-162, 2006.
4. Braverman IM, Keh A, Jacobson BS. Ultrastructure and three-dimensional organization of the telangiectases of hereditary hemorrhagic telangiectasia. J Invest Dermatol 95: 422-427, 1990.
5. Carlson TR, Yan Y, Wu X, Lam MT, Tang GL, Beverly LJ, Messina LM, Capobianco AJ, Werb Z, Wang R. Endothelial expression of constitutively active Notch4 elicits reversible arteriovenous malformations in adult mice. Proc Natl Acad Sci USA 102: 9884-9889, 2005.
6. Chao HS, Chern MS, Chen YC, Chang SC. Recurrence of pulmonary arteriovenous malformations in a female with hereditary hemorrhagic telangiectasia. Am J Med Sci 327: 294-298, 2004.
7. Cottin V, Chinet T, Lavole A, Corre R, Marchand E, Reynaud-Gaubert M, Plauchu H, Cordier JF. Pulmonary arteriovenous malformations in hereditary hemorrhagic telangiectasia: a series of 126 patients. Medicine 86: 1-17, 2007.
8. Cottin V, Dupuis-Girod S, Lesca G, Cordier JF. Pulmonary vascular manifestations of hereditary hemorrhagic telangiectasia (rendu-osler disease). Respiration 74: 361-378, 2007.
9. Fallon MB. Mechanisms of pulmonary vascular complications of liver disease: hepatopulmonary syndrome. J Clin Gastroenterol 39: S138-S142, 2005.
10. Fallon MB, Abrams GA, McGrath JW, Hou Z, Luo B. Common bile duct ligation in the rat: a model of intrapulmonary vasodilatation and hepatopulmonary syndrome. Am J Physiol Gastrointest Liver Physiol 272: G779-G784, 1997.
11. Freedom RM, Yoo SJ, Perrin D. The biological "scrabble" of pulmonary arteriovenous malformations: considerations in the setting of cavopulmonary surgery. Cardiol Young 14: 417-437, 2004.
12. Graudal N, Leth P, Marbjerg L, Galloe AM. Characteristics of cirrhosis undiagnosed during life: a comparative analysis of 73 undiagnosed cases and 149 diagnosed cases of cirrhosis, detected in 4929 consecutive autopsies. J Intern Med 230: 165-171, 1991.
13. Kim YH, Hu H, Guevara-Gallardo S, Lam MT, Fong SY, Wang RA. Artery and vein size is balanced by Notch and ephrin B2/EphB4 during angiogenesis. Development 135: 3755-3764, 2008.
14. Kluppel M, Wrana JL. Turning it up a Notch: cross-talk between TGF beta and Notch signaling. Bioessays 27: 115-118, 2005.
15. Krebs LT, Shutter JR, Tanigaki K, Honjo T, Stark KL, Gridley T. Haploinsufficient lethality and formation of arteriovenous malformations in Notch pathway mutants. Genes Dev 18: 2469-2473, 2004.
16. Krebs LT, Xue Y, Norton CR, Shutter JR, Maguire M, Sundberg JP, Gallahan D, Closson V, Kitajewski J, Callahan R, Smith GH, Stark KL, Gridley T. Notch signaling is essential for vascular morphogenesis in mice. Genes Dev 14: 1343-1352, 2000.
17. Lacombe P, Lagrange C, Beauchet A, El Hajjam M, Chinet T, Pelage JP. Diffuse pulmonary arteriovenous malformations in hereditary hemorrhagic telangiectasia: long-term results of embolization according to the extent of lung involvement. Chest 31: 31, 2008.
18. Lai EC. Notch signaling: control of cell communication and cell fate. Development 131: 965-973, 2004.
19. Lange PA, Stoller JK. The hepatopulmonary syndrome. Effect of liver transplantation. Clin Chest Med 17: 115-123, 1996.
20. Lawson ND, Scheer N, Pham VN, Kim CH, Chitnis AB, Campos-Ortega JA, Weinstein BM. Notch signaling is required for arterial-venous differentiation during embryonic vascular development. Development 128: 3675-3683, 2001.
21. Li JL, Sainson RC, Shi W, Leek R, Harrington LS, Preusser M, Biswas S, Turley H, Heikamp E, Hainfellner JA, Harris AL. Delta-like 4 Notch ligand regulates tumor angiogenesis, improves tumor vascular function, and promotes tumor growth in vivo. Cancer Res 67: 11244-11253, 2007.
22. Lobov IB, Renard RA, Papadopoulos N, Gale NW, Thurston G, Yancopoulos GD, Wiegand SJ. Delta-like ligand 4 (Dll4) is induced by VEGF as a negative regulator of angiogenic sprouting. Proc Natl Acad Sci USA 104: 3219-3224, 2007.
23. Ma X, Reddy VM, Riemer RK. Notch signaling is involved in development of pulmonary arteriovenous malformations after cavopulmonary anastomosis (Abstract). Circulation 112: II-10, 2005.
24. Malhotra SP, Reddy VM, Thelitz S, He YP, Hanley FL, Suleman S, Riemer RK. Cavopulmonary anastomosis induces pulmonary expression of the angiotensin II receptor family. J Thorac Cardiovasc Surg 123: 655-660, 2002.
25. Malhotra SP, Reddy VM, Thelitz S, He YP, McMullan DM, Hanley FL, Riemer RK. The role of oxidative stress in the development of pulmonary arteriovenous malformations after cavopulmonary anastomosis. J Thorac Cardiovasc Surg 124: 479-485, 2002.
26. Malhotra SP, Riemer RK, Thelitz S, He YP, Hanley FL, Reddy VM. Superior cavopulmonary anastomosis suppresses the activity and expression of pulmonary angiotensin-converting enzyme. J Thorac Cardiovasc Surg 122: 464-469, 2001.
27. Metzger RJ, Klein OD, Martin GR, Krasnow MA. The branching programme of mouse lung development. Nature 453: 745-750, 2008.
28. Mumtaz MA, Fraga CH, Nicholls CM, Desai S, Vasilyev N, Joshi R, Mee RB, Duncan BW. Increased expression of vascular endothelial growth factor messenger RNA in lungs of rats after cavopulmonary anastomosis. J Thorac Cardiovasc Surg 129: 209-210, 2005.
29. Murphy PA, Lam MT, Wu X, Kim TN, Vartanian SM, Bollen AW, Carlson TR, Wang RA. Endothelial Notch4 signaling induces hallmarks of brain arteriovenous malformations in mice. Proc Natl Acad Sci USA 105: 10901-10906, 2008.
30. Murphy PA, Lu G, Shiah S, Bollen AW, Wang RA. Endothelial Notch signaling is upregulated in human brain arteriovenous malformations and a mouse model of the disease. Lab Invest 89: 971-982, 2009.
31. Park SO, Lee YJ, Seki T, Hong KH, Fliess N, Jiang Z, Park A, Wu X, Kaartinen V, Roman BL, Oh SP. ALK5- and TGFBR2-independent role of ALK1 in the pathogenesis of hereditary hemorrhagic telangiectasia type 2. Blood 111: 633-642, 2008.
32. Rodriguez-Roisin R, Krowka MJ. Hepatopulmonary syndrome - a liver-induced lung vascular disorder. N Engl J Med 358: 2378-2387, 2008.
33. Sahlgren C, Gustafsson MV, Jin S, Poellinger L, Lendahl U. Notch signaling mediates hypoxia-induced tumor cell migration and invasion. Proc Natl Acad Sci USA 105: 6392-6397, 2008.
34. Schenk P, Fuhrmann V, Madl C, Funk G, Lehr S, Kandel O, Muller C. Hepatopulmonary syndrome: prevalence and predictive value of various cut offs for arterial oxygenation and their clinical consequences. Gut 51: 853-859, 2002.
35. Shah MJ, Rychik J, Fogel MA, Murphy JD, Jacobs ML. Pulmonary AV malformations after superior cavopulmonary connection: resolution after inclusion of hepatic veins in the pulmonary circulation. Ann Thorac Surg 63: 960-963, 1997.
36. Sho E, Nanjo H, Sho M, Kobayashi M, Komatsu M, Kawamura K, Xu C, Zarins CK, Masuda H. Arterial enlargement, tortuosity, and intimal thickening in response to sequential exposure to high and low wall shear stress. J Vasc Surg 39: 601-612, 2004.
37. Srinivasan S, Hanes MA, Dickens T, Porteous ME, Oh SP, Hale LP, Marchuk DA. A mouse model for hereditary hemorrhagic telangiectasia (HHT) type 2. Hum Mol Genet 12: 473-482, 2003.
38. Srivastava D, Preminger T, Lock JE, Mandell V, Keane JF, Mayer JE Jr, Kozakewich H, Spevak PJ. Hepatic venous blood and the development of pulmonary arteriovenous malformations in congenital heart disease. Circulation 92: 1217-1222, 1995.
39. Starnes SL, Duncan BW, Fraga CH, Desai SY, Jones TK, Mathur SK, Rosenthal GL, Lupinetti FM. Rat model of pulmonary arteriovenous malformations after right superior cavopulmonary anastomosis. Am J Physiol Heart Circ Physiol 283: H2151-H2156, 2002.
40. Uyttendaele H, Ho J, Rossant J, Kitajewski J. Vascular patterning defects associated with expression of activated Notch4 in embryonic endothelium. Proc Natl Acad Sci USA 98: 5643-5648, 2001.
41. Uyttendaele H, Marazzi G, Wu G, Yan Q, Sassoon D, Kitajewski J. Notch4/int-3, a mammary proto-oncogene, is an endothelial cell-specific mammalian Notch gene. Development 122: 2251-2259, 1996.
42. Villa N, Walker L, Lindsell CE, Gasson J, Iruela-Arispe ML, Weinmaster G. Vascular expression of Notch pathway receptors and ligands is restricted to arterial vessels. Mech Dev 108: 161-164, 2001.
43. Zhang J, Luo B, Tang L, Wang Y, Stockard CR, Kadish I, Groen TV, Grizzle WE, Ponnazhagan S, Fallon MB. Pulmonary angiogenesis in rat experimental hepatopulmonary syndrome. Gastroenterology 136: 1070-1080, 2008.
44. Zhang M, Luo B, Chen SJ, Abrams GA, Fallon MB. Endothelin-1 stimulation of endothelial nitric oxide synthase in the pathogenesis of hepatopulmonary syndrome. Am J Physiol Gastrointest Liver Physiol 277: G944-G952, 1999.