Real-time imaging of de novo arteriovenous malformation in a mouse model of hereditary hemorrhagic telangiectasia

Journal of Clinical Investigation

Volumn 119, Issue 11, 2009, Pages 3487-3496

  Sung, Ok Park ^a,b   Wankhede, Mamta ^c   Young, Jae Lee ^a,d   Choi, Eun Jung ^a,b   Fliess, Naime ^a,b   Choe, Se Woon ^c   Oh, Seh Hoon ^a   Walter, Glenn ^a   Raizada, Mohan K ^a   Sorg, Brian S ^c   Oh, S Paul ^a,b,d  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c University of Florida   (United States)

^d Gachon University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN RECEPTOR LIKE KINASE 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTERIOVENOUS MALFORMATION; ARTERY BLOOD FLOW; ARTICLE; BLOOD VESSEL; CONTROLLED STUDY; ENVIRONMENTAL FACTOR; FLUORESCENCE; GENE DELETION; GENE MUTATION; IMAGING; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; RENDU OSLER WEBER DISEASE; SKINFOLD;

ACTIVIN RECEPTORS, TYPE I; ANIMALS; ARTERIOVENOUS MALFORMATIONS; BLOOD VESSELS; DIAGNOSTIC IMAGING; DISEASE MODELS, ANIMAL; FEMALE; HOMEOSTASIS; MALE; MICE; MUTATION; TELANGIECTASIA, HEREDITARY HEMORRHAGIC;

EID: 70449392400     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI39482     Document Type: Article

References (46)

1. NIH. 2009. NINDS Arteriovenous Malformation Information Page. http://www.ninds.nih.gov/ disorders/avms/detail-avms.htm.
2. Shovlin, C.L., et al. 2000. Diagnostic criteria for hereditary hemorrhagic telangiectasia (Rendu-Osler-Weber syndrome). Am. J. Med. Genet. 91:66-67. (Pubitemid 30127562)
3. Abdalla, S.A., and Letarte, M. 2006. Hereditary haemorrhagic telangiectasia: current views on genetics and mechanisms of disease. J. Med. Genet. 43:97-110. (Pubitemid 43262964)
4. Geisthoff, U.W., et al. 2007. Health-related quality of life in hereditary hemorrhagic telangiectasia. Otolaryngol. Head Neck Surg. 136:726-733.
5. Geisthoff, U.W., Fiorella, M.L., and Fiorella, R. 2006. Treatment of recurrent epistaxis in HHT. Curr. Pharm. Des. 12:1237-1242.
6. Lesnik, G.T., et al. 2007. Septectomy and septal dermoplasty for the treatment of severe transfusion-dependent epistaxis in patients with hereditary hemorrhagic telangiectasia and septal perforation. Am. J. Rhinol. 21:312-315.
7. McAllister, K.A., et al. 1994. Endoglin, a TGF-beta binding protein of endothelial cells, is the gene for hereditary haemorrhagic telangiectasia type 1. Nat. Genet. 8:345-351. (Pubitemid 24375599)
8. Johnson, D.W., et al. 1996. Mutations in the activin receptor-like kinase 1 gene in hereditary haemorrhagic telangiectasia type 2. Nat. Genet. 13:189-195. (Pubitemid 26000439)
9. Cole, S.G., Begbie, M.E., Wallace, G.M., and Shovlin, C.L. 2005. A new locus for hereditary haemorrhagic telangiectasia (HHT3) maps to chromosome 5. J. Med. Genet. 42:577-582. (Pubitemid 40993833)
10. Bayrak-Toydemir, P., et al. 2006. A fourth locus for hereditary hemorrhagic telangiectasia maps to chromosome 7. Am. J. Med. Genet. A. 140:2155-2162. (Pubitemid 44522429)
11. Gallione, C.J., et al. 2004. A combined syndrome of juvenile polyposis and hereditary haemorrhagic telangiectasia associated with mutations in MADH4 (SMAD4). Lancet. 363:852-859.
12. Chang, H., Brown, C.W., and Matzuk, M.M. 2002. Genetic analysis of the mammalian transforming growth factor-beta superfamily. Endocr. Rev. 23:787-823. (Pubitemid 35454589)
13. McDonald, J.E., et al. 2000. Clinical manifestations in a large hereditary hemorrhagic telangiectasia (HHT) type 2 kindred. Am. J. Med. Genet. 93:320-327.
14. Sadick, H., et al. 2006. Hereditary hemorrhagic telangiectasia: an update on clinical manifestations and diagnostic measures. Wien. Klin. Wochenschr. 118:72-80.
15. Park, S.O., et al. 2008. ALK5- and TGFBR2-independent role of ALK1 in the pathogenesis of hereditary hemorrhagic telangiectasia type 2 (HHT2). Blood. 111:633-642.
16. Hong, K.H., et al. 2008. Genetic ablation of the BMPR2 gene in pulmonary endothelium is sufficient to predispose to pulmonary arterial hypertension. Circulation. 118:722-730.
17. Badea, T.C., Wang, Y., and Nathans, J. 2003. A noninvasive genetic/pharmacologic strategy for visualizing cell morphology and clonal relationships in the mouse. J. Neurosci. 23:2314-2322. (Pubitemid 36368919)
18. Seki, T., Yun, J., and Oh, S.P. 2003. Arterial endothelium-specific activin receptor-like kinase 1 expression suggests its role in arterialization and vascular remodeling. Circ. Res. 93:682-689. (Pubitemid 37222165)
19. Menger, M.D., Laschke, M.W., and Vollmar, B. 2002. Viewing the microcirculation through the window: some twenty years experience with the hamster dorsal skinfold chamber. Eur. Surg. Res. 34:83-91. (Pubitemid 34195702)
20. Sorg, H., Krueger, C., and Vollmar, B. 2007. Intravital insights in skin wound healing using the mouse dorsal skin fold chamber. J. Anat. 211:810-818. (Pubitemid 350182608)
21. Sorg, B.S., et al. 2008. Spectral imaging facilitates visualization and measurements of unstable and abnormal microvascular oxygen transport in tumors. J. Biomed. Opt. 13:014026.
22. Sorg, B.S., Moeller, B.J., Donovan, O., Cao, Y., and Dewhirst, M.W. 2005. Hyperspectral imaging of hemoglobin saturation in tumor microvasculature and tumor hypoxia development. J. Biomed. Opt. 10:44004. (Pubitemid 43328906)
23. Braverman, I.M., Keh, A., and Jacobson, B.S. 1990. Ultrastructure and three-dimensional organization of the telangiectases of hereditary hemorrhagic telangiectasia. J. Invest. Dermatol. 95:422-427. (Pubitemid 20331987)
24. Murphy, P.A., et al. 2008. Endothelial Notch4 signaling induces hallmarks of brain arteriovenous malformations in mice. Proc. Natl. Acad. Sci. U. S. A. 105:10901-10906.
25. Croix, C.S., Zipfel, W.R., and Watkins, S.C. 2007. Potential solutions for confocal imaging of living animals. Biotechniques. 43:14-19.
26. Padera, T.P., Stoll, B.R., So, P.T., and Jain, R.K. 2002. Conventional and high-speed intravital multiphoton laser scanning microscopy of microvasculature, lymphatics, and leukocyte-endothelial interactions. Mol. Imaging. 1:9-15.
27. Tozer, G.M., et al. 2005. Intravital imaging of tumour vascular networks using multi-photon fluorescence microscopy. Adv. Drug Deliv. Rev. 57:135-152.
28. Werkmeister, E., Kerdjoudj, H., Marchal, L., Stoltz, J.F., and Dumas, D. 2007. Multiphoton microscopy for blood vessel imaging: new non-invasive tools (Spectral, SHG, FLIM). Clin. Hemorheol. Microcirc. 37:77-88. (Pubitemid 47015814)
29. Braiman-Wiksman, L., Solomonik, I., Spira, R., and Tennenbaum, T. 2007. Novel insights into wound healing sequence of events. Toxicol. Pathol. 35:767-779. (Pubitemid 47613607)
30. Eming, S.A., Krieg, T., and Davidson, J.M. 2007. Inflammation in wound repair: molecular and cellular mechanisms. J. Invest. Dermatol. 127:514-525. (Pubitemid 46271017)
31. Sadick, H., Naim, R., Sadick, M., Hormann, K., and Riedel, F. 2005. Plasma level and tissue expression of angiogenic factors in patients with hereditary hemorrhagic telangiectasia. Int. J. Mol. Med. 15:591-596.
32. Sadick, H., Naim, R., Gossler, U., Hormann, K., and Riedel, F. 2005. Angiogenesis in hereditary hemorrhagic telangiectasia: VEGF165 plasma concentration in correlation to the VEGF expression and microvessel density. Int. J. Mol. Med. 15:15-19.
33. Shao, E.S., Lin, L., Yao, Y., and Bostrom, K.I. 2009. Expression of vascular endothelial growth factor is coordinately regulated by the activin-like kinase receptors 1 and 5 in endothelial cells. Blood. Online publication ahead of print. doi:10.1182/blood- 2009-01-199166.
34. David, L., et al. 2008. Bone morphogenetic protein-9 is a circulating vascular quiescence factor. Circ. Res. 102:914-922. (Pubitemid 351591550)
35. Scharpfenecker, M., et al. 2007. BMP-9 signals via ALK1 and inhibits bFGF-induced endothelial cell proliferation and VEGF-stimulated angiogenesis. J. Cell Sci. 120:964-972. (Pubitemid 46638511)
36. Kurstin, R. 2002. Using thalidomide in a patient with epithelioid leiomyosarcoma and Osler-Weber- Rendu disease. Oncology (Williston Park). 16:21-24.
37. Perez-Encinas, M., Rabunal Martinez, M.J., and Bello Lopez, J.L. 2002. Is thalidomide effective for the treatment of gastrointestinal bleeding in hereditary hemorrhagic telangiectasia? Haematologica. 87:ELT34.
38. Mitchell, A., et al. 2008. Bevacizumab reverses need for liver transplantation in hereditary hemorrhagic telangiectasia. Liver Transpl. 14:210-213. (Pubitemid 351267278)
39. Seki, T., Hong, K.H., Yun, J., Kim, S.J., and Oh, S.P. 2004. Isolation of a regulatory region of activin receptor-like kinase 1 gene sufficient for arterial endothelium-specific expression. Circ. Res. 94:e72-e77.
40. Seki, T., Hong, K.H., and Oh, S.P. 2006. Nonoverlapping expression patterns of ALK1 and ALK5 reveal distinct roles of each receptor in vascular development. Lab. Invest. 86:116-129. (Pubitemid 43117592)
41. Gridley, T. 2007. Notch signaling in vascular development and physiology. Development. 134:2709-2718. (Pubitemid 47305050)
42. Roca, C., and Adams, R.H. 2007. Regulation of vascular morphogenesis by Notch signaling. Genes Dev. 21:2511-2524. (Pubitemid 47607663)
43. Carlson, T.R., et al. 2005. Endothelial expression of constitutively active Notch4 elicits reversible arteriovenous malformations in adult mice. Proc. Natl. Acad. Sci. U. S. A. 102:9884-9889.
44. Hellstrom, M., et al. 2007. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature. 445:776-780. (Pubitemid 46279716)
45. Shonat, R.D., Wachman, E.S., Niu, W., Koretsky, A.P., and Farkas, D.L. 1997. Near-simultaneous hemoglobin saturation and oxygen tension maps in mouse brain using an AOTF microscope. Biophys. J. 73:1223-1231. (Pubitemid 27360712)
46. Unthank, J.L., Lash, J.M., Nixon, J.C., Sidner, R.A., and Bohlen, H.G. 1993. Evaluation of carbocyanine- labeled erythrocytes for microvascular measurements. Microvasc. Res. 45:193-210. (Pubitemid 223041415)