Thyroid hormone as a regulator of tumor induced angiogenesis

Cancer Letters

Volumn 301, Issue 2, 2011, Pages 119-126

  Pinto, Marta ^a   Soares, Paula ^a,b   Ribatti, Domenico ^c  

^a UNIVERSITY OF PORTO   (Portugal)

^b University of Porto   (Portugal)

^c UNIVERSITY OF BARI MEDICAL SCHOOL   (Italy)

Author keywords

Angiogenesis; Anti angiogenesis; Thyroid hormones; Tumor growth

Indexed keywords

BEVACIZUMAB; CISPLATIN; DOXORUBICIN; ETOPOSIDE; LIOTHYRONINE; PHOSPHOTRANSFERASE INHIBITOR; TETRAIODOTHYROACETIC ACID; THYROID HORMONE; THYROID HORMONE DERIVATIVE; THYROXINE; TRICHOSTATIN A; UNCLASSIFIED DRUG; VITRONECTIN RECEPTOR;

ADJUVANT THERAPY; ANTIANGIOGENIC THERAPY; CANCER ADJUVANT THERAPY; CARCINOGENESIS; CELL TRANSFORMATION; COLORECTAL CANCER; DRUG TARGETING; HORMONE BINDING; HUMAN; METASTASIS; NONHUMAN; PRIORITY JOURNAL; SHORT SURVEY; TISSUE DIFFERENTIATION; TISSUE GROWTH; TISSUE METABOLISM; TUMOR GROWTH; TUMOR VASCULARIZATION;

EID: 78651448387     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2010.11.011     Document Type: Review

References (98)

1. Yen P.M. Physiological and molecular basis of thyroid hormone action. Physiol. Rev. 2001, 81:1097-1142.
2. Bergh J.J., Lin H.Y., Lansing L., Mohamed S.N., Davis F.B., Mousa S., Davis P.J. Integrin alphaVbeta3 contains a cell surface receptor site for thyroid hormone that is linked to activation of mitogen-activated protein kinase and induction of angiogenesis. Endocrinology 2005, 146:2864-2871.
3. Moeller L.C., Cao X., Dumitrescu A.M., Seo H., Refetoff S. Thyroid hormone mediated changes in gene expression can be initiated by cytosolic action of the thyroid hormone receptor beta through the phosphatidylinositol 3-kinase pathway. Nucl. Recept Signal 2006, 4:e020.
4. Hiroi Y., Kim H.H., Ying H., Furuya F., Huang Z., Simoncini T., Noma K., Ueki K., Nguyen N.H., Scanlan T.S., Moskowitz M.A., Cheng S.Y., Liao J.K. Rapid nongenomic actions of thyroid hormone. Proc. Natl. Acad. Sci. USA 2006, 103:14104-14109.
5. Cheng S.Y., Leonard J.L., Davis P.J. Molecular aspects of thyroid hormone actions. Endocr. Rev. 2010, 31:139-170.
6. Ribatti D., Conconi M.T., Nussdorfer G.G. Nonclassic endogenous novel [corrected] regulators of angiogenesis. Pharmacol. Rev. 2007, 59:185-205.
7. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat. Med. 1995, 1:27-31.
8. Ribatti D., Vacca A., Dammacco F. The role of the vascular phase in solid tumor growth: a historical review. Neoplasia 1999, 1:293-302.
9. Risau W. Mechanisms of angiogenesis. Nature 1997, 386:671-674.
10. Carmeliet P. Mechanisms of angiogenesis and arteriogenesis. Nat. Med. 2000, 6:389-395.
11. Ribatti D., Nico B., Crivellato E. Morphological and molecular aspects of physiological vascular morphogenesis. Angiogenesis 2009, 12:101-111.
12. Pepper M.S. Manipulating angiogenesis. From basic science to the bedside. Arterioscler. Thromb. Vasc. Biol. 1997, 17:605-619.
13. Folkman J. Angiogenesis. Annu. Rev. Med. 2006, 57:1-18.
14. Folkman J. Antiangiogenesis in cancer therapy-endostatin and its mechanisms of action. Exp. Cell Res. 2006, 312:594-607.
15. Ruegg C., Hasmim M., Lejeune F.J., Alghisi G.C. Antiangiogenic peptides and proteins: from experimental tools to clinical drugs. Biochim. Biophys. Acta 2006, 1765:155-177.
16. Shweiki D., Itin A., Soffer D., Keshet E. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 1992, 359:843-845.
17. Kerbel R.S., Viloria-Petit A., Okada F., Rak J. Establishing a link between oncogenes and tumor angiogenesis. Mol. Med. 1998, 4:286-295.
18. Josko J., Mazurek M. Transcription factors having impact on vascular endothelial growth factor (VEGF) gene expression in angiogenesis. Med. Sci. Monit. 2004, 10:RA89-98.
19. Rak J., Yu J.L., Klement G., Kerbel R.S. Oncogenes and angiogenesis: signaling three-dimensional tumor growth. J. Investig. Dermatol. Symp. Proc. 2000, 5:24-33.
20. Rak J., Filmus J., Finkenzeller G., Grugel S., Marme D., Kerbel R.S. Oncogenes as inducers of tumor angiogenesis. Cancer Metast. Rev. 1995, 14:263-277.
21. Ferrari G., Cook B.D., Terushkin V., Pintucci G., Mignatti P. Transforming growth factor-beta 1 (TGF-beta1) induces angiogenesis through vascular endothelial growth factor (VEGF)-mediated apoptosis. J. Cell Physiol. 2009, 219:449-458.
22. Derynck R., Akhurst R.J., Balmain A. TGF-beta signaling in tumor suppression and cancer progression. Nat. Genet. 2001, 29:117-129.
23. Bierie B., Moses H.L. Tumour microenvironment: TGFbeta: the molecular Jekyll and Hyde of cancer. Nat. Rev. Cancer 2006, 6:506-520.
24. Pardali K., Moustakas A. Actions of TGF-beta as tumor suppressor and pro-metastatic factor in human cancer. Biochim. Biophys. Acta 2007, 1775:21-62.
25. Leivonen S.K., Kahari V.M. Transforming growth factor-beta signaling in cancer invasion and metastasis. Int. J. Cancer 2007, 121:2119-2124.
26. Massague J. TGFbeta in cancer. Cell 2008, 134:215-230.
27. Bernabeu C., Lopez-Novoa J.M., Quintanilla M. The emerging role of TGF-beta superfamily coreceptors in cancer. Biochim. Biophys. Acta 2009, 1792:954-973.
28. Pertovaara L., Kaipainen A., Mustonen T., Orpana A., Ferrara N., Saksela O., Alitalo K. Vascular endothelial growth factor is induced in response to transforming growth factor-beta in fibroblastic and epithelial cells. J. Biol. Chem. 1994, 269:6271-6274.
29. Lobov I.B., Brooks P.C., Lang R.A. Angiopoietin-2 displays VEGF-dependent modulation of capillary structure and endothelial cell survival in vivo. Proc. Natl. Acad. Sci. USA 2002, 99:11205-11210.
30. Kim I., Kim H.G., Moon S.O., Chae S.W., So J.N., Koh K.N., Ahn B.C., Koh G.Y. Angiopoietin-1 induces endothelial cell sprouting through the activation of focal adhesion kinase and plasmin secretion. Circ. Res. 2000, 86:952-959.
31. Fiedler U., Augustin H.G. Angiopoietins: a link between angiogenesis and inflammation. Trends Immunol. 2006, 27:552-558.
32. Thomas M., Augustin H.G. The role of the Angiopoietins in vascular morphogenesis. Angiogenesis 2009, 12:125-137.
33. Hu B., Cheng S.Y. Angiopoietin-2: development of inhibitors for cancer therapy. Curr. Oncol. Rep. 2009, 11:111-116.
34. Holash J., Maisonpierre P.C., Compton D., Boland P., Alexander C.R., Zagzag D., Yancopoulos G.D., Wiegand S.J. Vessel cooption, regression, and growth in tumors mediated by angiopoietins and VEGF. Science 1999, 284:1994-1998.
35. Yu Q. The dynamic roles of angiopoietins in tumor angiogenesis. Future Oncol. 2005, 1:475-484.
36. Bach F., Uddin F.J., Burke D. Angiopoietins in malignancy. Eur. J. Surg. Oncol. 2007, 33:7-15.
37. Hall L.C., Salazar E.P., Kane S.R., Liu N. Effects of thyroid hormones on human breast cancer cell proliferation. J. Steroid. Biochem. Mol. Biol. 2008, 109:57-66.
38. Conde S.J., Luvizotto R.A., Sibio M.T., Katayama M.L., Brentani M.M., Nogueira C.R. Tamoxifen inhibits transforming growth factor-alpha gene expression in human breast carcinoma samples treated with triiodothyronine. J. Endocrinol. Invest. 2008, 31:1047-1051.
39. Tang H.Y., Lin H.Y., Zhang S., Davis F.B., Davis P.J. Thyroid hormone causes mitogen-activated protein kinase-dependent phosphorylation of the nuclear estrogen receptor. Endocrinology 2004, 145:3265-3272.
40. Davis F.B., Tang H.Y., Shih A., Keating T., Lansing L., Hercbergs A., Fenstermaker R.A., Mousa A., Mousa S.A., Davis P.J., Lin H.Y. Acting via a cell surface receptor, thyroid hormone is a growth factor for glioma cells. Cancer Res. 2006, 66:7270-7275.
41. Hsieh M.L., Juang H.H. Cell growth effects of triiodothyronine and expression of thyroid hormone receptor in prostate carcinoma cells. J. Androl. 2005, 26:422-428.
42. Tsui K.H., Hsieh W.C., Lin M.H., Chang P.L., Juang H.H. Triiodothyronine modulates cell proliferation of human prostatic carcinoma cells by downregulation of the B-cell translocation gene 2. Prostate 2008, 68:610-619.
43. Yen C.C., Huang Y.H., Liao C.Y., Liao C.J., Cheng W.L., Chen W.J., Lin K.H. Mediation of the inhibitory effect of thyroid hormone on proliferation of hepatoma cells by transforming growth factor-beta. J. Mol. Endocrinol. 2006, 36:9-21.
44. Chen R.N., Huang Y.H., Lin Y.C., Yeh C.T., Liang Y., Chen S.L., Lin K.H. Thyroid hormone promotes cell invasion through activation of furin expression in human hepatoma cell lines. Endocrinology 2008, 149:3817-3831.
45. Iishi H., Tatsuta M., Baba M., Yamamoto R., Taniguchi H. Enhancement by thyroxine of gastric carcinogenesis induced by N-methyl-N′-nitro-N-nitrosoguanidine in Wistar rats. Brit. J. Cancer 1993, 68:515-518.
46. Liu R., Li Z., Bai S., Zhang H., Tang M., Lei Y., Chen L., Liang S., Zhao Y.L., Wei Y., Huang C. Mechanism of cancer cell adaptation to metabolic stress: proteomics identification of a novel thyroid hormone-mediated gastric carcinogenic signaling pathway. Mol. Cell Proteomics 2009, 8:70-85.
47. Lin H.Y., Tang H.Y., Shih A., Keating T., Cao G., Davis P.J., Davis F.B. Thyroid hormone is a MAPK-dependent growth factor for thyroid cancer cells and is anti-apoptotic. Steroids 2007, 72:180-187.
48. Chilian W.M., Wangler R.D., Peters K.G., Tomanek R.J., Marcus M.L. Thyroxine-induced left ventricular hypertrophy in the rat. Anatomical and physiological evidence for angiogenesis. Circ. Res. 1985, 57:591-598.
49. Tomanek R.J., Busch T.L. Coordinated capillary and myocardial growth in response to thyroxine treatment. Anat. Rec. 1998, 251:44-49.
50. Tomanek R.J., Doty M.K., Sandra A. Early coronary angiogenesis in response to thyroxine: growth characteristics and upregulation of basic fibroblast growth factor. Circ. Res. 1998, 82:587-593.
51. Wang X., Zheng W., Christensen L.P., Tomanek R.J. DITPA stimulates bFGF, VEGF, angiopoietin, and Tie-2 and facilitates coronary arteriolar growth. Am. J. Physiol. Heart Circ. Physiol. 2003, 284:H613-618.
52. Kuzman J.A., Tang Y., Vogelsang K.A., Said S., Anderson B.E., Morkin E., Gerdes A.M. Thyroid hormone analog, diiodothyropropionic acid (DITPA), exerts beneficial effects on chamber and cellular remodeling in cardiomyopathic hamsters. Cancer J. Physiol. Pharmacol. 2007, 85:311-318.
53. Mousa S.A., O'Connor L.J., Bergh J.J., Davis F.B., Scanlan T.S., Davis P.J. The proangiogenic action of thyroid hormone analogue GC-1 is initiated at an integrin. J. Cardiovasc. Pharmacol. 2005, 46:356-360.
54. Mousa S.A., O'Connor L., Davis F.B., Davis P.J. Proangiogenesis action of the thyroid hormone analog 3,5-diiodothyropropionic acid (DITPA) is initiated at the cell surface and is integrin mediated. Endocrinology 2006, 147:1602-1607.
55. Davis F.B., Mousa S.A., O'Connor L., Mohamed S., Lin H.Y., Cao H.J., Davis P.J. Proangiogenic action of thyroid hormone is fibroblast growth factor-dependent and is initiated at the cell surface. Circ. Res. 2004, 94:1500-1506.
56. Zhang L., Cooper-Kuhn C.M., Nannmark U., Blomgren K., Kuhn H.G. Stimulatory effects of thyroid hormone on brain angiogenesis in vivo and in vitro. J. Cereb. Blood Flow Metab. 2010, 30:323-335.
57. Otto T., Fandrey J. Thyroid hormone induces hypoxia-inducible factor 1alpha gene expression through thyroid hormone receptor beta/retinoid x receptor alpha-dependent activation of hepatic leukemia factor. Endocrinology 2008, 149:2241-2250.
58. D'Arezzo S., Incerpi S., Davis F.B., Acconcia F., Marino M., Farias R.N., Davis P.J. Rapid nongenomic effects of 3,5,3′-triiodo-l-thyronine on the intracellular pH of l-6 myoblasts are mediated by intracellular calcium mobilization and kinase pathways. Endocrinology 2004, 145:5694-5703.
59. Davis P.J., Leonard J.L., Davis F.B. Mechanisms of nongenomic actions of thyroid hormone. Front. Neuroendocrinol. 2008, 29:211-218.
60. Davis P.J., Davis F.B., Lin H.Y., Mousa S.A., Zhou M., Luidens M.K. Translational implications of nongenomic actions of thyroid hormone initiated at its integrin receptor. Am. J. Physiol. Endocrinol. Metab. 2009, 297:E1238-1246.
61. Davis P.J., Shih A., Lin H.Y., Martino L.J., Davis F.B. Thyroxine promotes association of mitogen-activated protein kinase and nuclear thyroid hormone receptor (TR) and causes serine phosphorylation of TR. J. Biol. Chem. 2000, 275:38032-38039.
62. Lin H.Y., Zhang S., West B.L., Tang H.Y., Passaretti T., Davis F.B., Davis P.J. Identification of the putative MAP kinase docking site in the thyroid hormone receptor-beta1 DNA-binding doma. Biochemistry 2003, 42:7571-7579.
63. Shih A., Lin H.Y., Davis F.B., Davis P.J. Thyroid hormone promotes serine phosphorylation of p53 by mitogen-activated protein kinase. Biochemistry 2001, 40:2870-2878.
64. Lin H.Y., Davis F.B., Gordinier J.K., Martino L.J., Davis P.J. Thyroid hormone induces activation of mitogen-activated protein kinase in cultured cells. Am. J. Physiol. 1999, 276:C1014-1024.
65. Lin H.Y., Shih A., Davis F.B., Davis P.J. Thyroid hormone promotes the phosphorylation of STAT3 and potentiates the action of epidermal growth factor in cultured cells. Biochem. J. 1999, 338(Pt 2):427-432.
66. Mousa S.A., Bergh J.J., Dier E., Rebbaa A., O'Connor L.J., Yalcin M., Aljada A., Dyskin E., Davis F.B., Lin H.Y., Davis P.J. Tetraiodothyroacetic acid, a small molecule integrin ligand, blocks angiogenesis induced by vascular endothelial growth factor and basic fibroblast growth factor. Angiogenesis 2008, 11:183-190.
67. Bockhorn M., Frilling A., Benko T., Best J., Sheu S.Y., Trippler M., Schlaak J.F., Broelsch C.E. Tri-iodothyronine as a stimulator of liver regeneration after partial and subtotal hepatectomy. Eur. Surg. Res. 2007, 39:58-63.
68. Lei J., Mariash C.N., Bhargava M., Wattenberg E.V., Ingbar D.H. T3 increases Na-K-ATPase activity via a MAPK/ERK1/2-dependent pathway in rat adult alveolar epithelial cells. Am. J. Physiol. Lung Cell Mol. Physiol. 2008, 294:L749-754.
69. Davis P.J., Zhou M., Davis F.B., Lansing L., Mousa S.A., Lin H.Y. Mini-review: Cell surface receptor for thyroid hormone and nongenomic regulation of ion fluxes in excitable cells. Physiol. Behav. 2010, 99:237-239.
70. Tsutsui S., Inoue H., Yasuda K., Suzuki K., Takeuchi H., Nishizaki T., Higashi H., Era S., Mori M. Angiopoietin 2 expression in invasive ductal carcinoma of the breast: its relationship to the VEGF expression and microvessel density. Breast Cancer Res. Treat. 2006, 98:261-266.
71. Yoshiji H., Kuriyama S., Noguchi R., Yoshii J., Ikenaka Y., Yanase K., Namisaki T., Kitade M., Uemura M., Masaki T., Fukui H. Angiopoietin 2 displays a vascular endothelial growth factor dependent synergistic effect in hepatocellular carcinoma development in mice. Gut 2005, 54:1768-1775.
72. Masson-Gadais B., Houle F., Laferriere J., Huot J. Integrin alphavbeta3, requirement for VEGFR2-mediated activation of SAPK2/p38 and for Hsp90-dependent phosphorylation of focal adhesion kinase in endothelial cells activated by VEGF. Cell Stress Chaperones 2003, 8:37-52.
73. Mahabeleshwar G.H., Feng W., Phillips D.R., Byzova T.V. Integrin signaling is critical for pathological angiogenesis. J. Exp. Med. 2006, 203:2495-2507.
74. Soldi R., Mitola S., Strasly M., Defilippi P., Tarone G., Bussolino F. Role of alphavbeta3 integrin in the activation of vascular endothelial growth factor receptor-2. EMBO J. 1999, 18:882-892.
75. Glinskii A.B., Glinsky G.V., Lin H.Y., Tang H.Y., Sun M., Davis F.B., Luidens M.K., Mousa S.A., Hercbergs A.H., Davis P.J. Modification of survival pathway gene expression in human breast cancer cells by tetraiodothyroacetic acid (tetrac). Cell Cycle 2009, 8:3554-3562.
76. Yalcin M., Dyskin E., Lansing L., Bharali D.J., Mousa S.S., Bridoux A., Hercbergs A.H., Lin H.Y., Davis F.B., Glinsky G.V., Glinskii A., Ma J., Davis P.J., Mousa S.A. Tetraiodothyroacetic acid (tetrac) and nanoparticulate tetrac arrest growth of medullary carcinoma of the thyroid. J. Clin. Endocrinol. Metab. 2010, 95:1972-1980.
77. Lin H.Y., Sun M., Tang H.Y., Lin C., Luidens M.K., Mousa S.A., Incerpi S., Drusano G.L., Davis F.B., Davis P.J. l-Thyroxine vs. 3,5,3′-triiodo-l-thyronine and cell proliferation: activation of mitogen-activated protein kinase and phosphatidylinositol 3-kinase. Am. J. Physiol. Cell Physiol. 2009, 296:C980-991.
78. Yalcin M., Bharali D.J., Dyskin E., Dier E., Lansing L., Mousa S.S., Davis F.B., Davis P.J., Mousa S.A. Tetraiodothyroacetic acid and tetraiodothyroacetic acid nanoparticle effectively inhibit the growth of human follicular thyroid cell carcinoma. Thyroid 2010, 20:281-286.
79. Shingu K., Fujimori M., Ito K., Hama Y., Kasuga Y., Kobayashi S., Itoh N., Amano J. Expression of fibroblast growth factor-2 and fibroblast growth factor receptor-1 in thyroid diseases: difference between neoplasms and hyperplastic lesions. Endocr. J. 1998, 45:35-43.
80. Giatromanolaki A., Lyberakidis G., Lyratzopoulos N., Koukourakis M.I., Sivridis E., Manolas C. Angiogenesis and angiogenic factor expression in thyroid cancer. J. Buon. 2010, 15:357-361.
81. Liang H., Zhong Y., Luo Z., Huang Y., Lin H., Luo M., Zhan S., Xie K., Ma Y., Li Q.Q. Assessment of biomarkers for clinical diagnosis of papillary thyroid carcinoma with distant metastasis. Int. J. Biol. Markers 2010, 25:38-45.
82. Jebreel A., England J., Bedford K., Murphy J., Karsai L., Atkin S. Vascular endothelial growth factor (VEGF), VEGF receptors expression and microvascular density in benign and malignant thyroid diseases. Int. J. Exp. Pathol. 2007, 88:271-277.
83. Klein M., Vignaud J.M., Hennequin V., Toussaint B., Bresler L., Plenat F., Leclere J., Duprez A., Weryha G. Increased expression of the vascular endothelial growth factor is a pejorative prognosis marker in papillary thyroid carcinoma. J. Clin. Endocrinol. Metab. 2001, 86:656-658.
84. Kerbel R.S. Antiangiogenic therapy: a universal chemosensitization strategy for cancer?. Science 2006, 312:1171-1175.
85. Ivy S.P., Wick J.Y., Kaufman B.M. An overview of small-molecule inhibitors of VEGFR signaling. Nat. Rev. Clin. Oncol. 2009, 6:569-579.
86. Schlumberger M., Sherman S.I. Clinical trials for progressive differentiated thyroid cancer: patient selection, study design, and recent advances. Thyroid 2009, 19:1393-1400.
87. Sherman S.I. Tyrosine kinase inhibitors and the thyroid. Best Pract. Res. Clin. Endocrinol. Metab. 2009, 23:713-722.
88. Sherman S.I. Targeted therapy of thyroid cancer. Biochem. Pharmacol. 2010, 80:592-601.
89. Jain R.K. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 2005, 307:58-62.
90. Salaun P.Y., Bodet-Milin C., Frampas E., Oudoux A., Sai-Maurel C., Faivre-Chauvet A., Barbet J., Paris F., Kraeber-Bodere F. Toxicity and efficacy of combined radioimmunotherapy and bevacizumab in a mouse model of medullary thyroid carcinoma. Cancer 2010, 116:1053-1058.
91. Cristofanilli M., Yamamura Y., Kau S.W., Bevers T., Strom S., Patangan M., Hsu L., Krishnamurthy S., Theriault R.L., Hortobagyi G.N. Thyroid hormone and breast carcinoma. Primary hypothyroidism is associated with a reduced incidence of primary breast carcinoma. Cancer 2005, 103:1122-1128.
92. Hercbergs A.A., Goyal L.K., Suh J.H., Lee S., Reddy C.A., Cohen B.H., Stevens G.H., Reddy S.K., Peereboom D.M., Elson P.J., Gupta M.K., Barnett G.H. Propylthiouracil-induced chemical hypothyroidism with high-dose tamoxifen prolongs survival in recurrent high grade glioma: a phase I/II study. Anticancer Res. 2003, 23:617-626.
93. Martinez-Iglesias O., Garcia-Silva S., Regadera J., Aranda A. Hypothyroidism enhances tumor invasiveness and metastasis development. PLoS One 2009, 4:e6428.
94. Rennert G., Rennert H.S., Pinchev M., Gruber S.B. A case-control study of levothyroxine and the risk of colorectal cancer. J. Natl. Cancer Inst. 2010, 102:568-572.
95. Rebbaa A., Chu F., Davis F.B., Davis P.J., Mousa S.A. Novel function of the thyroid hormone analog tetraiodothyroacetic acid: a cancer chemosensitizing and anti-cancer agent. Angiogenesis 2008, 11:269-276.
96. Yalcin M., Bharali D.J., Lansing L., Dyskin E., Mousa S.S., Hercbergs A., Davis F.B., Davis P.J., Mousa S.A. Tetraidothyroacetic acid (tetrac) and tetrac nanoparticles inhibit growth of human renal cell carcinoma xenografts. Anticancer Res. 2009, 29:3825-3831.
97. Bridoux A., Cui H., Dyskin E., Yalcin M., Mousa S.A. Semisynthesis and pharmacological activities of Tetrac analogs: angiogenesis modulators. Bioorg. Med. Chem. Lett. 2009, 19:3259-3263.
98. Bridoux A., Cui H., Dyskin E., Schmitzer A.R., Yalcin M., Mousa S.A. Semisynthesis and pharmacological activities of thyroxine analogs: development of new angiogenesis modulators. Bioorg. Med. Chem. Lett. 2010, 20:3394-3398.