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BioMed Research International
Volume 2014, Article ID 368082, 13 pages
http://dx.doi.org/10.1155/2014/368082
Research Article

Notch1 and 4 Signaling Responds to an Increasing Vascular Wall Shear Stress in a Rat Model of Arteriovenous Malformations

1Australian School of Advanced Medicine, Macquarie University, 2 Technology Place, North Ryde, Sydney, NSW 2109, Australia
2Department of Neurosurgery, The 9th Medical Clinical College of Beijing University, Beijing 100038, China

Received 27 September 2013; Accepted 11 December 2013; Published 20 January 2014

Academic Editor: Robert M. Starke

Copyright © 2014 Jian Tu et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. M. Starke, C. Yen, D. Ding, and J. P. Sheehan, “A practical grading scale for predicting outcome after radiosurgery for arteriovenous malformations: analysis of 1012 treated patients,” Journal of Neurosurgery, vol. 119, no. 4, pp. 981–987, 2013. View at Google Scholar
  2. S. Yamada, F. S. Brauer, A. R. T. Colohan et al., “Concept of arteriovenous malformation compartments and surgical management,” Neurological Research, vol. 26, no. 3, pp. 288–300, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Morgan and M. Winder, “Haemodynamics of arteriovenous malformations of the brain and consequences of resection: a review,” Journal of Clinical Neuroscience, vol. 8, no. 3, pp. 216–224, 2001. View at Publisher · View at Google Scholar · View at Scopus
  4. W. L. Young, “Intracranial arteriovenous malformations. pathophysiology and hemodynamics,” in Vascular Malformations of the Central Nervous System, J. J. Jafar, I. A. Awad, and R. H. Rosenwasser, Eds., pp. 95–126, Lippincott Williams & Wilkins, Philadelphia, Pa, USA, 1999. View at Google Scholar
  5. T. Hashimoto, R. Mesa-Tejada, C. M. Quick et al., “Evidence of increased endothelial cell turnover in brain arteriovenous malformations,” Neurosurgery, vol. 49, no. 1, pp. 124–132, 2001. View at Google Scholar · View at Scopus
  6. G. R. Sutherland, M. E. King, C. G. Drake, S. J. Peerless, and W. C. Vezina, “Platelet aggregation within cerebral arteriovenous malformations,” Journal of Neurosurgery, vol. 68, no. 2, pp. 198–204, 1988. View at Google Scholar · View at Scopus
  7. M. R. Harrigan, N. Ole-Schmidt, P. M. Black et al., “Angiogenic factors in the central nervous system,” Neurosurgery, vol. 53, no. 3, pp. 639–661, 2003. View at Google Scholar · View at Scopus
  8. P. A. Murphy, G. Lu, S. Shiah, A. W. Bollen, and R. A. Wang, “Endothelial Notch signaling is upregulated in human brain arteriovenous malformations and a mouse model of the disease,” Laboratory Investigation, vol. 89, no. 9, pp. 971–982, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. Q. Zhuge, M. Zhong, W. Zheng et al., “Notch-1 signalling is activated in brain arteriovenous malformations in humans,” Brain, vol. 132, no. 12, pp. 3231–3241, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. T. R. Carlson, Y. Yan, X. Wu et al., “Endothelial expression of constitutively active Notch4 elicits reversible arteriovenous malformations in adult mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 28, pp. 9884–9889, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. L. T. Krebs, C. Starling, A. V. Chervonsky, and T. Gridley, “Notch1 activation in mice causes arteriovenous malformations phenocopied by EphrinB2 and EphB4 mutants,” Genesis, vol. 48, no. 3, pp. 146–150, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. P. A. Murphy, M. T. Y. Lam, X. Wu et al., “Endothelial Notch4 signaling induces hallmarks of brain arteriovenous malformations in mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 31, pp. 10901–10906, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. P. A. Murphy, T. N. Kim, G. Lu, A. W. Bollen, C. B. Schaffer, and R. A. Wang, “Notch4 normalization reduces blood vessel size in arteriovenous malformations,” Science Translational Medicine, vol. 4, no. 117, p. 117ra8, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. S. S. Nijjar, H. A. Crosby, L. Wallace, S. G. Hubscher, and A. J. Strain, “Notch receptor expression in adult human liver: a possible role in bile duct formation and hepatic neovascularization,” Hepatology, vol. 34, no. 6, pp. 1184–1192, 2001. View at Publisher · View at Google Scholar · View at Scopus
  15. V. Lindner, C. Booth, I. Prudovsky, D. Small, T. Maciag, and L. Liaw, “Members of the Jagged/Notch gene families are expressed in injured arteries and regulate cell phenotype via alterations in cell matrix and cell-cell interaction,” American Journal of Pathology, vol. 159, no. 3, pp. 875–883, 2001. View at Google Scholar · View at Scopus
  16. N. Villa, L. Walker, C. E. Lindsell, J. Gasson, M. L. Iruela-Arispe, and G. Weinmaster, “Vascular expression of Notch pathway receptors and ligands is restricted to arterial vessels,” Mechanisms of Development, vol. 108, no. 1-2, pp. 161–164, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. S. P. Herbert and D. Y. R. Stainier, “Molecular control of endothelial cell behaviour during blood vessel morphogenesis,” Nature Reviews Molecular Cell Biology, vol. 12, no. 9, pp. 551–564, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. Z. Liu, A. Turkoz, E. N. Jackson et al., “Notch1 loss of heterozygosity causes vascular tumors and lethal hemorrhage in mice,” Journal of Clinical Investigation, vol. 121, no. 2, pp. 800–808, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. M. H. De Angelis, J. McIntyre II, and A. Gossler, “Maintenance of somite borders in mice requires the Delta homologue Dll1,” Nature, vol. 386, no. 6626, pp. 717–721, 1997. View at Google Scholar · View at Scopus
  20. A. Duarte, M. Hirashima, R. Benedito et al., “Dosage-sensitive requirement for mouse Dll4 in artery development,” Genes and Development, vol. 18, no. 20, pp. 2474–2478, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. N. W. Gale, M. G. Dominguez, I. Noguera et al., “Haploinsufficiency of delta-like 4 ligand results in embryonic lethality due to major defects in arterial and vascular development,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 45, pp. 15949–15954, 2004. View at Publisher · View at Google Scholar · View at Scopus
  22. F. A. High, M. L. Min, W. S. Pear, K. M. Loomes, K. H. Kaestner, and J. A. Epstein, “Endothelial expression of the Notch ligand Jagged1 is required for vascular smooth muscle development,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 6, pp. 1955–1959, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. Y. Xue, X. Gao, C. E. Lindsell et al., “Embryonic lethality and vascular defects in mice lacking the Notch ligand Jagged1,” Human Molecular Genetics, vol. 8, no. 5, pp. 723–730, 1999. View at Google Scholar · View at Scopus
  24. I. N. King, I. S. Kathiriya, M. Murakami et al., “Hrt and Hes negatively regulate Notch signaling through interactions with RBP-Jκ,” Biochemical and Biophysical Research Communications, vol. 345, no. 1, pp. 446–452, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. A. Limbourg, M. Ploom, D. Elligsen et al., “Notch ligand delta-like 1 is essential for postnatal arteriogenesis,” Circulation Research, vol. 100, no. 3, pp. 363–371, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. National Health and Medical Research Council, “Australian code of practice for the care and use of animals for scientific purposes,” 7th ed., 2004, http://www.nhmrc.gov.au/_files_nhmrc/publications/attachments/ea16.pdf.
  27. R. Yassari, T. Sayama, B. S. Jahromi et al., “Angiographic, hemodynamic and histological characterization of an arteriovenous fistula in rats,” Acta Neurochirurgica, vol. 146, no. 5, pp. 495–504, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. K. P. Storer, J. Tu, M. A. Stoodley, and R. I. Smee, “Expression of endothelial adhesion molecules after radiosurgery in an animal model of arteriovenous malformation,” Neurosurgery, vol. 67, no. 4, pp. 976–983, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Karunanyaka, J. Tu, A. Watling, K. P. Storer, A. Windsor, and M. A. Stoodley, “Endothelial molecular changes in a rodent model of arteriovenous malformation: laboratory investigation,” Journal of Neurosurgery, vol. 109, no. 6, pp. 1165–1172, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. J. Tu, Z. Hu, and Z. Chen, “Endothelial gene expression and molecular changes in response to radiosurgery in in vitro and in vivo models of cerebral arteriovenous malformations,” BioMed Research International, vol. 2013, Article ID 408253, 10 pages, 2013. View at Publisher · View at Google Scholar
  31. K. Storer, J. Tu, A. Karunanayaka et al., “Coadministration of low-dose lipopolysaccharide and soluble tissue factor induces thrombosis after radiosurgery in an animal arteriovenous malformation model,” Neurosurgery, vol. 61, no. 3, pp. 604–610, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. W. L. Young, E. Gao, G. J. Hademenos, and T. F. Massoud, “Use of modeling for the study of cerebral arteriovenous malformations,” in Intracranial Arteriovenous Malformations, P. E. Stieg, H. H. Batjer, and L. Samson, Eds., pp. 49–71, Informa Healthcare, New York, NY, USA, 2007. View at Google Scholar
  33. J. Tu, Z. Hu, and Z. Chen, “A combination of radiosurgery and soluble tissue factor enhances vascular targeting for experimental glioblastoma,” BioMed Research International, vol. 2013, Article ID 390714, 11 pages, 2013. View at Publisher · View at Google Scholar
  34. J. Tu and N. F. Jufri, “Estrogen signaling through estrogen receptor beta and G-protein-coupled estrogen receptor 1 in human cerebral vascular endothelial cells: implications for cerebral aneurysms,” BioMed Research International, vol. 2013, Article ID 524324, 9 pages, 2013. View at Publisher · View at Google Scholar
  35. J. L. Hintze, “Analysis of variance,” in Number Cruncher Statistical Systems (NCSS) 97-USer’s Guide-I, pp. 205–278, Kaysville, Utah, USA, 1997. View at Google Scholar
  36. G. J. Hademenos and T. F. Massoud, “The physics of intracranial arteriovenous malformations,” in The Physics of Cerebrovascular Diseases, pp. 238–290, Springer, New York, NY, USA, 1998. View at Google Scholar
  37. P. Fogarty-Mack, J. Pile-Spellman, L. Hacein-Bey et al., “The effect of arteriovenous malformations on the distribution of intracerebral arterial pressures,” American Journal of Neuroradiology, vol. 17, no. 8, pp. 1443–1449, 1996. View at Google Scholar · View at Scopus
  38. D. H. Duong, W. L. Young, M. C. Vang et al., “Feeding artery pressure and venous drainage pattern are primary determinants of hemorrhage from cerebral arteriovenous malformations,” Stroke, vol. 29, no. 6, pp. 1167–1176, 1998. View at Google Scholar · View at Scopus
  39. B. Larrivée, C. Prahst, E. Gordon et al., “ALK1 signaling inhibits angiogenesis by cooperating with the notch pathway,” Developmental Cell, vol. 22, no. 3, pp. 489–500, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. G. G. Leblanc, E. Golanov, I. A. Awad, and W. L. Young, “Biology of vascular malformations of the brain,” Stroke, vol. 40, no. 12, pp. e694–e702, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Jarriault, C. Brou, F. Logeat, E. H. Schroeter, R. Kopan, and A. Israel, “Signalling downstream of activated mammalian notch,” Nature, vol. 377, no. 6547, pp. 355–358, 1995. View at Google Scholar · View at Scopus
  42. J. J. Hofmann and M. L. Iruela-Arispe, “Notch signaling in blood vessels: who is talking to whom about what?” Circulation Research, vol. 100, no. 11, pp. 1556–1568, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. J. J. Hofmann and M. Luisa Iruela-Arispe, “Notch expression patterns in the retina: an eye on receptor-ligand distribution during angiogenesis,” Gene Expression Patterns, vol. 7, no. 4, pp. 461–470, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Hellström, L.-K. Phng, J. J. Hofmann et al., “Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis,” Nature, vol. 445, no. 7129, pp. 776–780, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. G.-R. Dou, L. Wang, Y.-S. Wang, and H. Han, “Notch signaling in ocular vasculature development and diseases,” Molecular Medicine, vol. 18, no. 1, pp. 47–55, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. D. Nichol and H. Stuhlmann, “EGFL7: a unique angiogenic signaling factor in vascular development and disease,” Blood, vol. 119, no. 6, pp. 1345–1352, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. M. Vikkula, L. M. Boon, J. B. Mulliken, and B. R. Olsen, “Molecular basis of vascular anomalies,” Trends in Cardiovascular Medicine, vol. 8, no. 7, pp. 281–292, 1998. View at Publisher · View at Google Scholar · View at Scopus
  48. R. L. Jeffree and M. A. Stoodley, “Postnatal development of arteriovenous malformations,” Pediatric Neurosurgery, vol. 45, no. 4, pp. 296–304, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. K. R. Bulsara, M. J. Alexander, A. T. Villavicencio et al., “De novo cerebral arteriovenous malformation: case report,” Neurosurgery, vol. 50, no. 5, pp. 1137–1141, 2002. View at Publisher · View at Google Scholar · View at Scopus
  50. O. A. Harris, S. D. Chang, B. T. Harris, and J. R. Adler, “Acquired cerebral arteriovenous malformation induced by an anaplastic astrocytoma: an interesting case,” Neurological Research, vol. 22, no. 5, pp. 473–477, 2000. View at Google Scholar · View at Scopus