Table of Contents Author Guidelines Submit a Manuscript
Table of Contents Alerts

To receive news and publication updates for International Journal of Endocrinology, enter your email address in the box below.

International Journal of Endocrinology
Volume 2015, Article ID 834137, 7 pages
http://dx.doi.org/10.1155/2015/834137
Research Article

Gremlin, a Bone Morphogenetic Protein Antagonist, Is a Crucial Angiogenic Factor in Pituitary Adenoma

Kenta Koketsu, Daizo Yoshida, Kyongsong Kim, Yudo Ishii, Shigeyuki Tahara, Akira Teramoto, and Akio Morita

Department of Neurosurgery, Nippon Medical School, Tokyo 113-8602, Japan

Received 27 September 2014; Revised 10 February 2015; Accepted 16 February 2015

Academic Editor: Amelie Bonnefond

Copyright © 2015 Kenta Koketsu 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. W. Lederle, M. Palmowski, and F. Kiessling, “Imaging in the age of molecular medicine: monitoring of anti-angiogenic treatments,” Current Pharmaceutical Biotechnology, vol. 13, no. 4, pp. 595–608, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. A. G. Linkous and E. M. Yazlovitskaya, “Novel therapeutic approaches for targeting tumor angiogenesis,” Anticancer Research, vol. 32, no. 1, pp. 1–12, 2012. View at Google Scholar · View at Scopus
  3. B. Shan, C. Schaaf, A. Schmidt et al., “Curcumin suppresses HIF1A synthesis and VEGFA release in pituitary adenomas,” Journal of Endocrinology, vol. 214, no. 3, pp. 389–398, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. J. Yang, Z. Xiao, T. Li, X. Gu, and B. Fan, “Erythropoietin promotes the growth of pituitary adenomas by enhancing angiogenesis,” International Journal of Oncology, vol. 40, no. 4, pp. 1230–1237, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. Q. Zhang, Y. Zhang, S. Z. Wang et al., “Reduced expression of tissue factor pathway inhibitor-2 contributes to apoptosis and angiogenesis in cervical cancer,” Journal of Experimental & Clinical Cancer Research, vol. 31, no. 1, article 1, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. X. Zhao, D. C. Li, H. Zhao et al., “A study of the suppressive effect on human pancreatic adenocarcinoma cell proliferation and angiogenesis by stable plasmid-based siRNA silencing of c-Src gene expression,” Oncology Reports, vol. 27, no. 3, pp. 628–636, 2012. View at Google Scholar
  7. J. T. Zhang, Y. Z. Fan, C. Q. Chen, Z. M. Zhao, and W. Sun, “Norcantharidin: a potential antiangiogenic agent for gallbladder cancers in vitro and in vivo,” International Journal of Oncology, vol. 40, no. 5, pp. 1501–1514, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. C. Onofri, M. Losa, E. Uhl, G. K. Stalla, and U. Renner, “Immunohistochemical analysis of VEGF-C/VEGFR-3 system and lymphatic vessel extent in normal and adenomatous human pituitary tissues,” Experimental and Clinical Endocrinology and Diabetes, vol. 116, no. 3, pp. 152–157, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. C. Onofri, M. Theodoropoulou, M. Losa et al., “Localization of vascular endothelial growth factor (VEGF) receptors in normal and adenomatous pituitaries: detection of a non-endothelial function of VEGF in pituitary tumours,” Journal of Endocrinology, vol. 191, no. 1, pp. 249–261, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. H. Horiguchi, L. Jin, K. H. Ruebel, B. W. Scheithauer, and R. V. Lloyd, “Regulation of VEGF-A, VEGFR-I, thrombospondin-1, -2, and -3 expression in a human pituitary cell line (HP75) by TGFβ1, bFGF, and EGF,” Endocrine, vol. 24, no. 2, pp. 141–146, 2004. View at Publisher · View at Google Scholar · View at Scopus
  11. M. C. Zatelli, D. Piccin, C. Vignali et al., “Pasireotide, a multiple somatostatin receptor subtypes ligand, reduces cell viability in non-functioning pituitary adenomas by inhibiting vascular endothelial growth factor secretion,” Endocrine-Related Cancer, vol. 14, no. 1, pp. 91–102, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. C. S. Kim, H. Ying, M. C. Willingham, and S. Y. Cheng, “The pituitary tumor-transforming gene promotes angiogenesis in a mouse model of follicular thyroid cancer,” Carcinogenesis, vol. 28, no. 5, pp. 932–939, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. D. S. Kim, J. A. Franklyn, K. Boelaert, M. C. Eggo, J. C. Watkinson, and C. J. McCabe, “Pituitary tumor transforming gene (PTTG) stimulates thyroid cell proliferation via a vascular endothelial growth factor/kinase insert domain receptor/inhibitor of DNA binding-3 autocrine pathway,” Journal of Clinical Endocrinology and Metabolism, vol. 91, no. 11, pp. 4603–4611, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. D. S. Kim, J. A. Franklyn, A. L. Stratford et al., “Pituitary tumor-transforming gene regulates multiple downstream angiogenic genes in thyroid cancer,” The Journal of Clinical Endocrinology & Metabolism, vol. 91, no. 3, pp. 1119–1128, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. J. Xu, S. Zhang, C. You, X. Wang, and Q. Zhou, “Microvascular density and vascular endothelial growth factor have little correlation with prognosis of craniopharyngioma,” Surgical Neurology, vol. 66, supplement 1, pp. S30–S34, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. H. Stabile, S. Mitola, E. Moroni et al., “Bone morphogenic protein antagonist Drm/gremlin is a novel proangiogenic factor,” Blood, vol. 109, no. 5, pp. 1834–1840, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. C. Ravelli, S. Mitola, M. Corsini, and M. Presta, “Involvement of alpha(v)beta (3) integrin in gremlin-induced angiogenesi,” Angiogenesis, vol. 16, no. 1, pp. 235–243, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. L. Claesson-Welsh, “Gremlin: vexing VEGF receptor agonist,” Blood, vol. 116, no. 18, pp. 3386–3387, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. D. Maiolo, S. Mitola, D. Leali et al., “Role of nanomechanics in canonical and noncanonical pro-angiogenic ligand/VEGF receptor-2 activation,” Journal of the American Chemical Society, vol. 134, no. 35, pp. 14573–14579, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. E. Tzahor, H. Kempf, R. C. Mootoosamy et al., “Antagonists of Wnt and BMP signaling promote the formation of vertebrate head muscle,” Genes and Development, vol. 17, no. 24, pp. 3087–3099, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. M. S. Mulvihill, Y.-W. Kwon, S. Lee et al., “Gremlin is overexpressed in lung adenocarcinoma and increases cell growth and proliferation in normal lung cells,” PLoS ONE, vol. 7, no. 8, Article ID e42264, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. J. Heinke, M. Juschkat, A. Charlet et al., “Antagonism and synergy between extracellular BMP modulators Tsg and BMPER balance blood vessel formation,” Journal of Cell Science, vol. 126, no. 14, pp. 3082–3094, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. M.-H. Chen, Y.-C. Yeh, Y.-M. Shyr et al., “Expression of gremlin 1 correlates with increased angiogenesis and progression-free survival in patients with pancreatic neuroendocrine tumors,” Journal of Gastroenterology, vol. 48, no. 1, pp. 101–108, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. E. Gazzerro, R. C. Pereira, V. Jorgetti, S. Olson, A. N. Economides, and E. Canalis, “Skeletal overexpression of gremlin impairs bone formation and causes osteopenia,” Endocrinology, vol. 146, no. 2, pp. 655–665, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. O. Michos, A. Gonçalves, J. Lopez-Rios et al., “Reduction of BMP4 activity by gremlin 1 enables ureteric bud outgrowth and GDNF/WNT11 feedback signalling during kidney branching morphogenesis,” Development, vol. 134, no. 13, pp. 2397–2405, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. E. Gazzerro, A. Smerdel-Ramoya, S. Zanotti et al., “Conditional deletion of gremlin causes a transient increase in bone formation and bone mass,” The Journal of Biological Chemistry, vol. 282, no. 43, pp. 31549–31557, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. D. C. Genetos, C. A. Toupadakis, L. F. Raheja et al., “Hypoxia decreases sclerostin expression and increases Wnt signaling in osteoblasts,” Journal of Cellular Biochemistry, vol. 110, no. 2, pp. 457–467, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Mitola, C. Ravelli, E. Moroni et al., “Gremlin is a novel agonist of the major proangiogenic receptor VEGFR2,” Blood, vol. 116, no. 18, pp. 3677–3680, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. J. B. Sneddon, H. H. Zhen, K. Montgomery et al., “Bone morphogenetic protein antagonist gremlin 1 is wideley expressed by cancer-associated stromal cells and can promote tumor cell proliferation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 40, pp. 14842–14847, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. V. Dolan, M. Murphy, P. Alarcon, H. R. Brady, and C. Hensey, “Gremlin—a putative pathogenic player in progressive renal disease,” Expert Opinion on Therapeutic Targets, vol. 7, no. 4, pp. 523–526, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. D. W. P. Lappin, R. McMahon, M. Murphy, and H. R. Brady, “Gremlin: an example of the re-emergence of developmental programmes in diabetic nephropathy,” Nephrology Dialysis Transplantation, vol. 17, supplement 9, pp. 65–67, 2002. View at Publisher · View at Google Scholar · View at Scopus
  32. Y. Zhang and Q. Zhang, “Bone morphogenetic protein-7 and Gremlin: new emerging therapeutic targets for diabetic nephropathy,” Biochemical and Biophysical Research Communications, vol. 383, no. 1, pp. 1–3, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. D. W. Walsh, S. A. Roxburgh, P. McGettigan et al., “Co-regulation of Gremlin and Notch signalling in diabetic nephropathy,” Biochimica et Biophysica Acta—Molecular Basis of Disease, vol. 1782, no. 1, pp. 10–21, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. V. Dolan, M. Murphy, D. Sadlier et al., “Expression of gremlin, a bone morphogenetic protein antagonist, in human diabetic nephropathy,” American Journal of Kidney Diseases, vol. 45, no. 6, pp. 1034–1039, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. R. Kane, L. Stevenson, C. Godson, A. W. Stitt, and C. O'Brien, “Gremlin gene expression in bovine retinal pericytes exposed to elevated glucose,” British Journal of Ophthalmology, vol. 89, no. 12, pp. 1638–1642, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. C. Gaston-Massuet, C. L. Andoniadou, M. Signore et al., “Increased Wingless (Wnt) signaling in pituitary progenitor/stem cells gives rise to pituitary tumors in mice and humans,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 28, pp. 11482–11487, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Giles, F. Madec, S. Friedrichsen et al., “Wnt signaling in estrogen-induced lactotroph proliferation,” Journal of Cell Science, vol. 124, no. 4, pp. 540–547, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. M. S. Elston and R. J. Clifton-Bligh, “Identification of Wnt family inhibitors: a pituitary tumor directed whole genome approach,” Molecular and Cellular Endocrinology, vol. 326, no. 1-2, pp. 48–54, 2010. View at Publisher · View at Google Scholar · View at Scopus