TGFB1 disrupts the angiogenic potential of microvascular endothelial cells of the corpus luteum

Journal of Cell Science

Volumn 124, Issue 14, 2011, Pages 2501-2510

  Maroni, Dulce ^a   Davis, John S ^a,b  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b VA NEBRASKA WESTERN IOWA HEALTH CARE SYSTEM   (United States)

Author keywords

Angiogenesis; Corpus luteum; Fertility; Luteolysis; Reproduction; SMAD; TGFB1

Indexed keywords

DNA; FIBRILLAR COLLAGEN; FIBRILLAR COLLAGEN I; MATRIGEL; SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN;

ANGIOGENESIS; ANIMAL CELL; APOPTOSIS; ARTICLE; BASAL CELL; CAPILLARY; CELL CONTACT; CELL DEATH; CELL FUNCTION; CELL ISOLATION; CELL JUNCTION; CELL LOSS; CELL MIGRATION; CELL PERMEABILIZATION; CELL PROLIFERATION; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; CORPUS LUTEUM; COW; DNA SYNTHESIS; FETAL CALF SERUM; GEL; MICROVASCULAR ENDOTHELIAL CELL; MICROVASCULATURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANIMALS; CATTLE; CELL MOVEMENT; CORPUS LUTEUM; ENDOTHELIAL CELLS; FEMALE; HUMANS; LUTEOLYSIS; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA1;

BOVINAE;

EID: 79960398844     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.084558     Document Type: Article

References (70)

1. Alghisi, G. C., Ponsonnet, L. and Rüegg, C. (2009). The integrin antagonist cilengitide activates alphaVbeta3, disrupts VE-cadherin localization at cell junctions and enhances permeability in endothelial cells. PLoS ONE 4, e4449.
2. Alvarez, D. F., Huang, L., King, J. A., ElZarrad, M. K., Yoder, M. C. and Stevens, T. (2008). Lung microvascular endothelium is enriched with progenitor cells that exhibit vasculogenic capacity. Am J. Physiol. Lung Cell. Mol. Physiol. 294, L419-L430.
3. Behzadian, M. A., Wang, X. L., Windsor, L. J., Ghaly, N. and Caldwell, R. B. (2001). TGF-β increases retinal endothelial cell permeability by increasing MMP-9: possible role of glial cells in endothelial barrier function. Invest. Ophthalmol. Vis. Sci. 42, 85385-85389.
4. Bein, K., Odell-Fiddler, E. T. and Drinane, M. (2004). Role of TGF-beta1 and JNK signaling in capillary tube patterning. Am. J. Physiol. Cell Physiol. 287, C1012-C1022.
5. Berisha, B., Meyer, H. H. D. and Schams, D. (2010). Effect of prostaglandin F2 Alpha on local luteotropic and angiogenic factors during induced functional luteolysis in the bovine corpus luteum. Biol. Reprod. 82, 940-947.
6. Berrier, A. L. and Yamada, K. M. (2007). Cell-matrix adhesion. J. Cell. Physiol. 213, 565-573.
7. Bogan, R. L., Murphy, M. J., Stouffer, R. L. and Hennebold, J. D. (2008). Prostaglandin synthesis, metabolism, and signaling potential in the rhesus macaque corpus luteum throughout the luteal phase of the menstrual cycle. Endocrinology 149, 5861-5871.
8. Casey, O. M., Morris, D. G., Powell, R., Sreenan, J. M. and Fitzpatrick, R. (2005). Analysis of gene expression in non-regressed and regressed bovine corpus luteum tissue using a customized ovarian cDNA array. Theriogenology 64, 1963-1976.
9. Davis, G. E. and Senger, D. R. (2008). Extracellular matrix mediates a molecular balance between vascular morphogenesis and regression. Curr. Opin. Hematol. 15, 197-203.
10. Davis, J. S. and Rueda, B. R. (2002). The corpus luteum: an ovarian structure with maternal instincts and suicidal tendencies. Front. Biosci. 7, 1949-1978.
11. Davis, J. S., Rueda, B. R. and Spanel-Borowski, K. (2003). Microvascular endothelial cells of the corpus luteum. Reprod. Biol. Endocrinol. 10, 89-103.
12. Dejana, E., Orsenigo, F. and Lampugnani, M. G. (2008). The role of adherens junctions and VE-cadherin in the control of vascular permeability. J. Cell Sci. 121, 2115-2122.
13. Del Pozo, M. A. and Schwartz, M. A. (2007). Rac, membrane heterogeneity, caveolin and regulation of growth by integrins. Trends Cell Biol. 17, 246-250.
14. Duncan, W. C. (2000). The human corpus luteum: remodeling during luteolysis and maternal recognition of pregnancy. Rev. Reprod. 5, 12-17.
15. Ferrari, G., Cook, B. D., Terushkin, V., Pintucci, G. and Mignatti, P. (2009). Transforming growth factor-beta 1 (TGF-beta1) induces angiogenesis through vascular endothelial growth factor (VEGF)-mediated apoptosis. J. Cell. Physiol. 219, 449-458.
16. Fraser, H. M. and Duncan, W. C. (2005). Vascular morphogenesis in the primate ovary. Angiogenesis 8, 101-116.
17. Friedman, A., Weiss, S., Levy, N. and Meidan, R. (2000). Role of tumor necrosis factor alpha and its type I receptor in luteal regression: induction of programmed cell death in bovine corpus luteum-derived endothelial cells. Biol. Reprod. 63, 1905-1912.
18. Fukuchi, M., Miyazaki, T., Fukai, Y., Nakajima, M., Sohda, M., Masuda, N., Manda, R., Tsukada, K., Kato, H. and Kuwano, H. (2004). Plasma level of transforming growth factor beta1 measured from the azygos vein predicts prognosis in patients with esophageal cancer. Clin. Cancer Res. 10, 2738-2741.
19. Gangrade, B. K., Gotcher, E. D., Davis, J. S. and May, J. V. (1993). The secretion of transforming growth factor-beta by bovine luteal cells in vitro. Mol. Cell. Endocrinol. 93, 117-123.
20. Gordon, K. J. and Blobe, G. C. (2008). Role of transforming growth factor-beta superfamily signaling pathways in human disease. Biochim. Biophys. Acta 1782, 197-228.
21. Goumans, M. J., Liu, Z. and ten Dijke, P. (2009). TGF-β signaling in vascular biology and dysfunction. Cell Res. 19, 116-127.
22. Henkes, L. E., Sullivan, B. T., Lynch, M. P., Kolesnick, R., Arsenault, D., Puder, M., Davis, J. S. and Rueda, B. R. (2008). Acid sphingomyelinase involvement in tumor necrosis factor alpha-regulated vascular and steroid disruption during luteolysis in vivo. Proc. Natl. Acad. Sci. USA 105, 7670-7675.
23. Hou, X., Arvisais, E. W., Jiang, C., Chen, D. B., Roy, S. K., Pate, J. L., Hansen, T. R., Rueda, B. R. and Davis, J. S. (2008). Prostaglandin F2alpha stimulates the expression and secretion of transforming growth factor B1 via induction of the early growth response 1 gene (EGR1) in the bovine corpus luteum. Mol. Endocrinol. 22, 403-414.
24. Hou, X., Arvisais, E. W. and Davis, J. S. (2010). Luteinizing hormone stimulates mammalian target of rapamycin signaling in bovine luteal cells via pathways independent of AKT and mitogen-activated protein kinase: modulation of glycogen synthase kinase 3 and AMP-activated protein kinase. Endocrinology 151, 2846-2857.
25. Hurst, V., 5th, Goldberg, P. L., Minnear, F. L., Heimark, R. L. and Vincent, P. A. (1999). Rearrangement of adherens junctions by transforming growth factor-beta1: role of contraction. Am. J. Physiol. 276, L582-L595.
26. Inman, G. J., Nicolás, F. J., Callahan, J. F., Harling, J. D., Gaster, L. M., Reith, A. D., Laping, N. J. and Hill, C. S. (2002). SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol. Pharmacol. 62, 65-74.
27. Irving-Rodgers, H. F., Roger, J., Luck, M. R. and Rodgers, R. J. (2006). Extracellular matrix of the corpus luteum. Semin. Reprod. Med. 24, 242-250.
28. Kelly, J. J., Moore, T. M., Babal, P., Diwan, A. H., Stevens, T. and Thompson, W. J. (1998). Pulmonary microvascular and macrovascular endothelial cells: differential regulation of Ca2+ and permeability. Am. J. Physiol. 274, L810-L819.
29. Kiliç, Z. M., Ayaz, S., Ozin, Y., Nadir, I., Cakal, B. and Ulker, A. (2009). Plasma transforming growth factor-beta1 level in inflammatory bowel disease. Turk. J. Gastroenterol. 20, 165-170.
30. King, J., Hamil, T., Creighton, J., Wu, S., Bhat, P., McDonald, F. and Stevens, T. (2004). Structural and functional characteristics of lung macro- and microvascular endothelial cell phenotypes. Microvasc. Res. 67, 139-151.
31. Knight, P. G. and Glister, C. (2006). TGF-beta superfamily members and ovarian follicle development. Reproduction 132, 191-206.
32. Lebrin, F., Deckers, M., Bertolino, P. and ten Dijke, P. (2005). TGF-beta receptor function in the endothelium. Cardiovasc. Res. 65, 599-608.
33. Lu, Q. (2008). Transforming growth factor-beta1 protects against pulmonary artery endothelial cell apoptosis via ALK5. Am. J. Physiol. Lung Cell. Mol. Physiol. 295, L123-L133.
34. Lu, Q., Patel, B., Harrington, E. O. and Rounds, S. (2009). Transforming growth factorbeta1 causes pulmonary microvascular endothelial cell apoptosis via ALK5. Am. J. Physiol. Lung Cell. Mol. Physiol. 296, L825-L838.
35. Margadant, C. and Sonnenberg, A. (2010). Integrin-TGF-beta crosstalk in fibrosis, cancer and wound healing. EMBO Rep. 11, 97-105.
36. Massagué, J. (2008). TGFβ in cancer. Cell 134, 215-230.
37. Miyamoto, A., Okuda, K., Schweigert, F. J. and Schams, D. (1992). Effects of basic fibroblast growth factor, transforming growth factor-beta and nerve growth factor on the secretory function of the bovine corpus luteum in vitro. J. Endocrinol. 135, 103-114.
38. Nakhuda, G. S., Zimmermann, R. C., Bohlen, P., Liao, F., Sauer, M. V. and Kitajewski, J. (2005). Inhibition of the vascular endothelial cell (VE)-specific adhesion molecule VE-cadherin blocks gonadotropin-dependent folliculogenesis and corpus luteum formation and angiogenesis. Endocrinology 146, 1053-1059.
39. Neuvians, T. P., Berisha, B. and Schams, D. (2004). Vascular endothelial growth factor (VEGF) and fibroblast growth factor (FGF) expression during induced luteolysis in the bovine corpus luteum. Mol. Reprod. Dev. 67, 389-395.
40. Niswender, G. D., Juengel, J. L., Silva, P. J., Rollyson, M. K. and McIntush, E. W. (2000). Mechanisms controlling the function and life span of the corpus luteum. Physiol. Rev. 80, 1-29.
41. Niswender, G. D., Davis, T. L., Griffith, R. J., Bogan, R. L., Monser, K., Bott, R. C., Bruemmer, J. E. and Nett, T. M. (2007). Judge, jury and executioner: the autoregulation of luteal function. Soc. Reprod. Fertil. 64 Suppl, 191-206.
42. Ofori-Acquah, S. F., King, J., Voelkel, N., Schaphorst, K. L. and Stevens, T. (2008). Heterogeneity of barrier function in the lung reflects diversity in endothelial cell junctions. Microvasc. Res. 75, 391-402.
43. Ouellette, Y., Price, C. A. and Carrière, P. D. (2005). Follicular fluid concentration of transforming growth factor-beta1 is negatively correlated with estradiol and follicle size at the early stage of development of the first-wave cohort of bovine ovarian follicles. Domest. Anim. Endocrinol. 29, 623-633.
44. Pardali, E. and ten Dijke, P. (2009). Transforming growth factor-beta signaling and tumor angiogenesis. Front. Biosci. 14, 4848-4861.
45. Pauli, S. A., Tang, H., Wang, J., Bohlen, P., Posser, R., Hartman, T., Sauer, M. V., Kitajewski, J. and Zimmermann, R. C. (2005). The vascular endothelial growth factor (VEGF)/VEGF receptor 2 pathway is critical for blood vessel survival in corpora lutea of pregnancy in the rodent. Endocrinology 146, 1301-1311.
46. Plendl, J. (2000). Angiogenesis and vascular regression in the ovary. Anat. Histol. Embryol. 29, 257-266.
47. Pollman, M. J., Naumovski, L. and Gibbons, G. H. (1999). Vascular cell apoptosis: cell type-specific modulation by transforming growth factor-beta1 in endothelial cells versus smooth muscle cells. Circulation 99, 2019-2026.
48. Pru, J. K., Lynch, M. P., Davis, J. S. and Rueda, B. R. (2003). Signaling mechanisms in tumor necrosis factor alpha-induced death of microvascular endothelial cells of the corpus luteum. Reprod. Biol. Endocrinol. 1, 17.
49. Ramsauer, M. and D'Amore, P. A. (2007). Contextual role for angiopoietins and TGFbeta1 in blood vessel stabilization. J. Cell Sci. 120, 1810-1817.
50. Ricken, A. M., Spanel-Borowski, K., Saxer, M. and Huber, P. R. (1995). Cytokeratin expression in bovine corpora lutea. Histochem. Cell Biol. 103, 345-354.
51. Robinson, R. S., Woad, K. J., Hammond, A. J., Laird, M., Hunter, M. G. and Mann, G. E. (2009). Angiogenesis and vascular function in the ovary. Reproduction 138, 869-881.
52. Sankar, S., Mahooti-Brooks, N., Bensen, L., McCarthy, T. L., Centrella, M. and Madri, J. A. (1996). Modulation of transforming growth factor beta receptor levels on microvascular endothelial cells during in vitro angiogenesis. J. Clin. Invest. 97, 1436-1446.
53. Serratì, S., Margheri, F., Pucci, M., Cantelmo, A. R., Cammarota, R., Dotor, J., Borràs-Cuesta, F., Fibbi, G., Albini, A. and Del Rosso, M. (2009). TGFβ1 antagonistic peptides inhibit TGFβ1-dependent angiogenesis. Biochem. Pharmacol. 77, 813-825.
54. Shirasuna, K., Watanabe, S., Nagai, K., Sasahara, K., Shimizu, T., Ricken, A. M., Spanel-Borowski, K. and Miyamoto, A. (2007). Expression of mRNA for cell adhesion molecules in the bovine corpus luteum during the estrous cycle and PGF2alpha-induced luteolysis. J. Reprod. Dev. 53, 1319-1328.
55. Shirasuna, K., Sasahara, K., Matsui, M., Shimizu, T. and Miyamoto, A. (2010). Prostaglandin F2alpha differentially affects mRNA expression relating to angiogenesis, vasoactivation and prostaglandins in the early and mid corpus luteum in the cow. J. Reprod. Dev. 56, 428-436.
56. Stevens, T., Phan, S., Frid, M. G., Alvarez, D., Herzog, E. and Stenmark, K. R. (2008). Lung vascular cell heterogeneity: endothelium, smooth muscle, and fibroblasts. Proc. Am. Thorac. Soc. 5, 783-791.
57. Stocco, C., Callegari, E. and Gibori, G. (2001). Opposite effect of prolactin and prostaglandin F(2α) on the expression of luteal genes as revealed by rat cDNA expression array. Endocrinology 142, 4158-4161.
58. Stocco, C., Telleria, C. and Gibori, G. (2007). The molecular control of corpus luteum formation, function, and regression. Endocr. Rev. 28, 117-149.
59. Stouffer, R. L., Xu, F. and Duffy, D. M. (2007). Molecular control of ovulation and luteinization in the primate follicle. Front. Biosci. 12, 297-307.
60. Tanaka, J., Acosta, T. J., Berisha, B., Tetsuka, M., Matsui, M., Kobayashi, S., Schams, D. and Miyamoto, A. (2004). Relative changes in mRNA expression of angiopoietins and receptors tie in bovine corpus luteum during estrous cycle and prostaglandin F2alpha-induced luteolysis: a possible mechanism for the initiation of luteal regression. Reprod. Dev. 50, 619-626.
61. ten Dijke, P. and Arthur, H. M. (2007). Extracellular control of TGFbeta signalling in vascular development and disease. Nat. Rev. Mol. Cell Biol. 8, 857-869.
62. Townson, D. H. and Liptak, A. R. (2003). Chemokines in the corpus luteum: implications of leukocyte chemotaxis. Reprod. Biol. Endocrinol. 1, 94.
63. Tscheudschilsuren, G., Aust, G., Nieber, K., Schilling, N. and Spanel-Borowski, K. (2002). Microvascular endothelial cells differ in basal and hypoxia-regulated expression of angiogenic factors and their receptors. Microvasc. Res. 63, 243-251.
64. Villar, A. V., Cobo, M., Llano, M., Montalvo, C., González-Vílchez, F., Martín-Durán, R., Hurlé, M. A. and Nistal, J. F. (2009). Plasma levels of transforming growth factorb1 reflect left ventricular remodeling in aortic stenosis. PLoS ONE 4, e8476.
65. Vonnahme, K. A., Redmer, D. A., Borowczyk, E., Bilski, J. J., Luther, J. S., Johnson, M. L., Reynolds, L. P. and Grazul-Bilska, A. T. (2006). Vascular composition, apoptosis, and expression of angiogenic factors in the corpus luteum during prostaglandin F2alpha-induced regression in sheep. Reproduction 131, 1115-1126.
66. Wang, Z., Tamura, K., Yoshie, M., Tamura, H., Imakawa, K. and Kogo, H. (2003). Prostaglandin F2alpha-induced functional regression of the corpus luteum and apoptosis in rodents. J. Pharmacol. Sci. 92, 19-27.
67. Weis, S. M. (2007). Evaluating integrin function in models of angiogenesis and vascular permeability. Methods Enzymol. 426, 505-528.
68. Wu, M. Y. and Hill, C. S. (2009). TGF-beta superfamily signaling in embryonic development and homeostasis. Dev. Cell. 16, 329-343.
69. Yancopoulos, G. D., Davis, S., Gale, N. W., Rudge, J. S., Wiegand, S. J. and Holash, J. (2000). Vascular-specific growth factors and blood vessel formation. Nature 407, 242-248.
70. Zhao, Y. and Luck, M. R. (1995). Gene expression and protein distribution of collagen, fibronectin and laminin in bovine follicles and corpora lutea. J. Reprod. Fertil. 104, 115-123.