Sprouty1, a new target of the angiostatic agent 16K prolactin, negatively regulates angiogenesis
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  • 作者:Céline Sabatel (1)
    Anne M Cornet (1)
    Sébastien P Tabruyn (1)
    Ludovic Malvaux (1)
    Karolien Castermans (1)
    Joseph A Martial (1)
    Ingrid Struman (1)
  • 刊名:Molecular Cancer
  • 出版年:2010
  • 出版时间:December 2010
  • 年:2010
  • 卷:9
  • 期:1
  • 全文大小:1652KB
  • 参考文献:1. Ferrara N, Kerbel RS: Angiogenesis as a therapeutic target. / Nature 2005,438(7070):967-74. CrossRef
    2. McKay MM, Morrison DK: Integrating signals from RTKs to ERK/MAPK. / Oncogene 2007,26(22):3113-121. CrossRef
    3. Hacohen N, Kramer S, Sutherland D, Hiromi Y, Krasnow MA: sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. / Cell 1998,92(2):253-63. CrossRef
    4. Minowada G, Jarvis LA, Chi CL, Neubuser A, Sun X, Hacohen N, Krasnow MA, Martin GR: Vertebrate Sprouty genes are induced by FGF signaling and can cause chondrodysplasia when overexpressed. / Development 1999,126(20):4465-475.
    5. Mason JM, Morrison DJ, Basson MA, Licht JD: Sprouty proteins: multifaceted negative-feedback regulators of receptor tyrosine kinase signaling. / Trends Cell Biol 2006,16(1):45-4. CrossRef
    6. Cabrita MA, Christofori G: Sprouty proteins, masterminds of receptor tyrosine kinase signaling. / Angiogenesis 2008,11(1):53-2. CrossRef
    7. Edwin F, Anderson K, Ying C, Patel TB: Intermolecular interactions of Sprouty proteins and their implications in development and disease. / Mol Pharmacol 2009,76(4):679-91. CrossRef
    8. Taniguchi K, Ishizaki T, Ayada T, Sugiyama Y, Wakabayashi Y, Sekiya T, Nakagawa R, Yoshimura A: Sprouty4 deficiency potentiates Ras-independent angiogenic signals and tumor growth. / Cancer Sci 2009,100(9):1648-654. CrossRef
    9. Taniguchi K, Sasaki K, Watari K, Yasukawa H, Imaizumi T, Ayada T, Okamoto F, Ishizaki T, Kato R, Kohno R, / et al.: Suppression of Sproutys has a therapeutic effect for a mouse model of ischemia by enhancing angiogenesis. / PLoS One 2009,4(5):e5467. CrossRef
    10. Struman I, Bentzien F, Lee H, Mainfroid V, D'Angelo G, Goffin V, Weiner RI, Martial JA: Opposing actions of intact and N-terminal fragments of the human prolactin/growth hormone family members on angiogenesis: an efficient mechanism for the regulation of angiogenesis. / Proc Natl Acad Sci USA 1999,96(4):1246-251. CrossRef
    11. Nguyen NQ, Tabruyn SP, Lins L, Lion M, Cornet AM, Lair F, Rentier-Delrue F, Brasseur R, Martial JA, Struman I: Prolactin/growth hormone-derived antiangiogenic peptides highlight a potential role of tilted peptides in angiogenesis. / Proc Natl Acad Sci USA 2006,103(39):14319-4324. CrossRef
    12. Kim J, Luo W, Chen DT, Earley K, Tunstead J, Yu-Lee LY, Lin SH: Antitumor activity of the 16-kDa prolactin fragment in prostate cancer. / Cancer Res 2003,63(2):386-93.
    13. Bentzien F, Struman I, Martini JF, Martial J, Weiner R: Expression of the antiangiogenic factor 16 K hPRL in human HCT116 colon cancer cells inhibits tumor growth in Rag1(-/-) mice. / Cancer Res 2001,61(19):7356-362.
    14. Nguyen NQ, Cornet A, Blacher S, Tabruyn SP, Foidart JM, Noel A, Martial JA, Struman I: Inhibition of tumor growth and metastasis establishment by adenovirus-mediated gene transfer delivery of the antiangiogenic factor 16 K hPRL. / Mol Ther 2007,15(12):2094-100. CrossRef
    15. Kinet V, Nguyen NQ, Sabatel C, Blacher S, Noel A, Martial JA, Struman I: Antiangiogenic liposomal gene therapy with 16 K human prolactin efficiently reduces tumor growth. / Cancer Lett 2009,284(2):222-28. CrossRef
    16. Pan H, Nguyen NQ, Yoshida H, Bentzien F, Shaw LC, Rentier-Delrue F, Martial JA, Weiner R, Struman I, Grant MB: Molecular targeting of antiangiogenic factor 16 K hPRL inhibits oxygen-induced retinopathy in mice. / Invest Ophthalmol Vis Sci 2004,45(7):2413-419. CrossRef
    17. Hilfiker-Kleiner D, Kaminski K, Podewski E, Bonda T, Schaefer A, Sliwa K, Forster O, Quint A, Landmesser U, Doerries C, / et al.: A cathepsin D-cleaved 16 kDa form of prolactin mediates postpartum cardiomyopathy. / Cell 2007,128(3):589-00. CrossRef
    18. Clapp C, Weiner RI: A specific, high affinity, saturable binding site for the 16-kilodalton fragment of prolactin on capillary endothelial cells. / Endocrinology 1992,130(3):1380-386. CrossRef
    19. Martini JF, Piot C, Humeau LM, Struman I, Martial JA, Weiner RI: The antiangiogenic factor 16 K PRL induces programmed cell death in endothelial cells by caspase activation. / Mol Endocrinol 2000,14(10):1536-549. CrossRef
    20. Tabruyn SP, Sorlet CM, Rentier-Delrue F, Bours V, Weiner RI, Martial JA, Struman I: The antiangiogenic factor 16 K human prolactin induces caspase-dependent apoptosis by a mechanism that requires activation of nuclear factor-kappaB. / Mol Endocrinol 2003,17(9):1815-823. CrossRef
    21. Tabruyn SP, Nguyen NQ, Cornet AM, Martial JA, Struman I: The antiangiogenic factor, 16-kDa human prolactin, induces endothelial cell cycle arrest by acting at both the G0-G1 and the G2-M phases. / Mol Endocrinol 2005,19(7):1932-942. CrossRef
    22. D'Angelo G, Martini JF, Iiri T, Fantl WJ, Martial J, Weiner RI: 16 K human prolactin inhibits vascular endothelial growth factor-induced activation of Ras in capillary endothelial cells. / Mol Endocrinol 1999,13(5):692-04. CrossRef
    23. Tabruyn SP, Sabatel C, Nguyen NQ, Verhaeghe C, Castermans K, Malvaux L, Griffioen AW, Martial JA, Struman I: The angiostatic 16 K human prolactin overcomes endothelial cell anergy and promotes leukocyte infiltration via nuclear factor-kappaB activation. / Mol Endocrinol 2007,21(6):1422-429. CrossRef
    24. Impagnatiello MA, Weitzer S, Gannon G, Compagni A, Cotten M, Christofori G: Mammalian sprouty-1 and -2 are membrane-anchored phosphoprotein inhibitors of growth factor signaling in endothelial cells. / J Cell Biol 2001,152(5):1087-098. CrossRef
    25. Thijssen VL, Brandwijk RJ, Dings RP, Griffioen AW: Angiogenesis gene expression profiling in xenograft models to study cellular interactions. / Exp Cell Res 2004,299(2):286-93. CrossRef
    26. Cahir-McFarland ED, Carter K, Rosenwald A, Giltnane JM, Henrickson SE, Staudt LM, Kieff E: Role of NF-kappa B in cell survival and transcription of latent membrane protein 1-expressing or Epstein-Barr virus latency III-infected cells. / J Virol 2004,78(8):4108-119. CrossRef
    27. Gross I, Bassit B, Benezra M, Licht JD: Mammalian sprouty proteins inhibit cell growth and differentiation by preventing ras activation. / J Biol Chem 2001,276(49):46460-6468. CrossRef
    28. Meloche S, Pouyssegur J: The ERK1/2 mitogen-activated protein kinase pathway as a master regulator of the G1- to S-phase transition. / Oncogene 2007,26(22):3227-239. CrossRef
    29. Vermeulen K, Van Bockstaele DR, Berneman ZN: The cell cycle: a review of regulation, deregulation and therapeutic targets in cancer. / Cell Prolif 2003,36(3):131-49. CrossRef
    30. Cheng T: Cell cycle inhibitors in normal and tumor stem cells. / Oncogene 2004,23(43):7256-266. CrossRef
    31. Ho PY, Hsu SP, Liang YC, Kuo ML, Ho YS, Lee WS: Inhibition of the ERK phosphorylation plays a role in terbinafine-induced p21 up-regulation and DNA synthesis inhibition in human vascular endothelial cells. / Toxicol Appl Pharmacol 2008,229(1):86-3. CrossRef
    32. Eliceiri BP, Klemke R, Stromblad S, Cheresh DA: Integrin alphavbeta3 requirement for sustained mitogen-activated protein kinase activity during angiogenesis. / J Cell Biol 1998,140(5):1255-263. CrossRef
    33. Lee SH, Schloss DJ, Jarvis L, Krasnow MA, Swain JL: Inhibition of angiogenesis by a mouse sprouty protein. / J Biol Chem 2001,276(6):4128-133. CrossRef
    34. Kwabi-Addo B, Wang J, Erdem H, Vaid A, Castro P, Ayala G, Ittmann M: The expression of Sprouty1, an inhibitor of fibroblast growth factor signal transduction, is decreased in human prostate cancer. / Cancer Res 2004,64(14):4728-735. CrossRef
    35. Lo TL, Yusoff P, Fong CW, Guo K, McCaw BJ, Phillips WA, Yang H, Wong ES, Leong HF, Zeng Q, / et al.: The ras/mitogen-activated protein kinase pathway inhibitor and likely tumor suppressor proteins, sprouty 1 and sprouty 2 are deregulated in breast cancer. / Cancer Res 2004,64(17):6127-136. CrossRef
    36. Liu ZJ, Xiao M, Balint K, Soma A, Pinnix CC, Capobianco AJ, Velazquez OC, Herlyn M: Inhibition of endothelial cell proliferation by Notch1 signaling is mediated by repressing MAPK and PI3K/Akt pathways and requires MAML1. / Faseb J 2006,20(7):1009-011. CrossRef
    37. Pintucci G, Moscatelli D, Saponara F, Biernacki PR, Baumann FG, Bizekis C, Galloway AC, Basilico C, Mignatti P: Lack of ERK activation and cell migration in FGF-2-deficient endothelial cells. / Faseb J 2002,16(6):598-00.
    38. Yigzaw Y, Cartin L, Pierre S, Scholich K, Patel TB: The C terminus of sprouty is important for modulation of cellular migration and proliferation. / J Biol Chem 2001,276(25):22742-2747. CrossRef
    39. Poppleton HM, Edwin F, Jaggar L, Ray R, Johnson LR, Patel TB: Sprouty regulates cell migration by inhibiting the activation of Rac1 GTPase. / Biochem Biophys Res Commun 2004,323(1):98-03. CrossRef
    40. Lai CF, Chaudhary L, Fausto A, Halstead LR, Ory DS, Avioli LV, Cheng SL: Erk is essential for growth, differentiation, integrin expression, and cell function in human osteoblastic cells. / J Biol Chem 2001,276(17):14443-4450.
    41. Jin A, Kurosu T, Tsuji K, Mizuchi D, Arai A, Fujita H, Hattori M, Minato N, Miura O: BCR/ABL and IL-3 activate Rap1 to stimulate the B-Raf/MEK/Erk and Akt signaling pathways and to regulate proliferation, apoptosis, and adhesion. / Oncogene 2006,25(31):4332-340. CrossRef
    42. Edwin F, Patel TB: A novel role of Sprouty 2 in regulating cellular apoptosis. / J Biol Chem 2008,283(6):3181-190. CrossRef
    43. Lito P, Mets BD, Appledorn DM, Maher VM, McCormick JJ: Sprouty 2 regulates DNA damage-induced apoptosis in Ras-transformed human fibroblasts. / J Biol Chem 2009,284(2):848-54. CrossRef
    44. Gross I, Armant O, Benosman S, de Aguilar JL, Freund JN, Kedinger M, Licht JD, Gaiddon C, Loeffler JP: Sprouty2 inhibits BDNF-induced signaling and modulates neuronal differentiation and survival. / Cell Death Differ 2007,14(10):1802-812. CrossRef
    45. Gupta K, Kshirsagar S, Li W, Gui L, Ramakrishnan S, Gupta P, Law PY, Hebbel RP: VEGF prevents apoptosis of human microvascular endothelial cells via opposing effects on MAPK/ERK and SAPK/JNK signaling. / Exp Cell Res 1999,247(2):495-04. CrossRef
    46. Lavoie JN, L'Allemain G, Brunet A, Muller R, Pouyssegur J: Cyclin D1 expression is regulated positively by the p42/p44MAPK and negatively by the p38/HOGMAPK pathway. / J Biol Chem 1996,271(34):20608-0616. CrossRef
    47. Beier F, Taylor AC, LuValle P: The Raf-1/MEK/ERK pathway regulates the expression of the p21(Cip1/Waf1) gene in chondrocytes. / J Biol Chem 1999,274(42):30273-0279. CrossRef
    48. Han S, Sidell N, Roman J: Fibronectin stimulates human lung carcinoma cell proliferation by suppressing p21 gene expression via signals involving Erk and Rho kinase. / Cancer Lett 2005,219(1):71-1. CrossRef
    49. Gospodarowicz D, Massoglia S, Cheng J, Fujii DK: Effect of fibroblast growth factor and lipoproteins on the proliferation of endothelial cells derived from bovine adrenal cortex, brain cortex, and corpus luteum capillaries. / J Cell Physiol 1986,127(1):121-36. CrossRef
    50. Sun J, Blaskovich MA, Jain RK, Delarue F, Paris D, Brem S, Wotoczek-Obadia M, Lin Q, Coppola D, Choi K, / et al.: Blocking angiogenesis and tumorigenesis with GFA-116, a synthetic molecule that inhibits binding of vascular endothelial growth factor to its receptor. / Cancer Res 2004,64(10):3586-592. CrossRef
    51. Livak KJ, Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. / Methods 2001,25(4):402-08. CrossRef
  • 作者单位:Céline Sabatel (1)
    Anne M Cornet (1)
    Sébastien P Tabruyn (1)
    Ludovic Malvaux (1)
    Karolien Castermans (1)
    Joseph A Martial (1)
    Ingrid Struman (1)

    1. Unit of Molecular Biology and Genetic Engineering, GIGA-research, University of Liège, B34, Avenue de l'H?pital, 1, B-4000, Liège, Belgium
  • ISSN:1476-4598
文摘
Background Disorganized angiogenesis is associated with several pathologies, including cancer. The identification of new genes that control tumor neovascularization can provide novel insights for future anti-cancer therapies. Sprouty1 (SPRY1), an inhibitor of the MAPK pathway, might be one of these new genes. We identified SPRY1 by comparing the transcriptomes of untreated endothelial cells with those of endothelial cells treated by the angiostatic agent 16 K prolactin (16 K hPRL). In the present study, we aimed to explore the potential function of SPRY1 in angiogenesis. Results We confirmed 16 K hPRL induced up-regulation of SPRY1 in primary endothelial cells. In addition, we demonstrated the positive SPRY1 regulation in a chimeric mouse model of human colon carcinoma in which 16 K hPRL treatment was shown to delay tumor growth. Expression profiling by qRT-PCR with species-specific primers revealed that induction of SPRY1 expression by 16 K hPRL occurs only in the (murine) endothelial compartment and not in the (human) tumor compartment. The regulation of SPRY1 expression was NF-κB dependent. Partial SPRY1 knockdown by RNA interference protected endothelial cells from apoptosis as well as increased endothelial cell proliferation, migration, capillary network formation, and adhesion to extracellular matrix proteins. SPRY1 knockdown was also shown to affect the expression of cyclinD1 and p21 both involved in cell-cycle regulation. These findings are discussed in relation to the role of SPRY1 as an inhibitor of ERK/MAPK signaling and to a possible explanation of its effect on cell proliferation. Conclusions Taken together, these results suggest that SPRY1 is an endogenous angiogenesis inhibitor.
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