Hyperglycosylated human chorionic gonadotropin stimulates angiogenesis through TGF-β receptor activation

FASEB Journal

Volumn 27, Issue 4, 2013, Pages 1309-1321

  Berndt, Sarah ^a,b,c   Blacher, Silvia ^d   Munaut, Carine ^d   Detilleux, Julien ^d   D'hauterive, Sophie Perrier ^d,f   Huhtaniemi, Ilpo ^e   Evain Brion, Danièle ^a,b,c   Noël, Agnès ^d   Fournier, Thierry ^a,b,c   Foidart, Jean Michel ^d,f  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c Fondation PremUP   (France)

^d UNIVERSITY OF LIÈGE   (Belgium)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

^f UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Angiostimulation; Choriocarcinoma; Endothelial cells; Mural cells; Placenta

Indexed keywords

CHORIONIC GONADOTROPIN BETA SUBUNIT; LUTEINIZING HORMONE; SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CARCINOGENESIS; CELL MIGRATION; CELL PROLIFERATION; CHORIOCARCINOMA; CONTROLLED STUDY; CYTOTROPHOBLAST; ENDOTHELIUM CELL; GLYCOSYLATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; NONHUMAN; PLACENTA DEVELOPMENT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; REPORTER GENE; SIGNAL TRANSDUCTION; TROPHOBLAST;

ANGIOGENESIS INDUCING AGENTS; ANIMALS; CELLS, CULTURED; CHORIONIC GONADOTROPIN; EMBRYO IMPLANTATION; ENDOTHELIAL CELLS; FEMALE; GLYCOSYLATION; HUMANS; MICE; MICE, INBRED C57BL; NEOVASCULARIZATION, PHYSIOLOGIC; PLACENTA; PREGNANCY; RATS; RATS, WISTAR; RECEPTORS, LH; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; TROPHOBLASTS;

MUS;

EID: 84875743800     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-213686     Document Type: Article

References (54)

1. Charnock-Jones, D. S., Kaufmann, P., and Mayhew, T. M. (2004) Aspects of human fetoplacental vasculogenesis and angiogenesis. I. Molecular regulation. Placenta 25, 103-113.
2. Kaufmann, P., Mayhew, T. M., and Charnock-Jones, D. S. (2004) Aspects of human fetoplacental vasculogenesis and angiogenesis. II. Changes during normal pregnancy. Placenta 25, 114 -126.
3. Zygmunt, M., Herr, F., Munstedt, K., Lang, U., and Liang, O. D. (2003) Angiogenesis and vasculogenesis in pregnancy. Eur. J. Obstet. Gynecol. Reprod. Biol. 110(Suppl. 1), S10-S18.
4. Berndt, S., Perrier d'Hauterive, S., Blacher, S., Pequeux, C., Lorquet, S., Munaut, C., Applanat, M., Herve, M. A., Lamande, N., Corvol, P., van den Brule, F., Frankenne, F., Poutanen, M., Huhtaniemi, I., Geenen, V., Noel, A., and Foidart, J. M. (2006) Angiogenic activity of human chorionic gonadotropin through LH receptor activation on endothelial and epithelial cells of the endometrium. FASEB J. 20, 2630-2632.
5. Kornyei, J. L., Lei, Z. M., and Rao, C. V. (1993) Human myometrial smooth muscle cells are novel targets of direct regulation by human chorionic gonadotropin. Biol. Reprod. 49, 1149-1157.
6. Toth, P., Li, X., Rao, C. V., Lincoln, S. R., Sanfilippo, J. S., Spinnato, J. A., and Yussman, M. A. (1994) Expression of functional human chorionic gonadotropin/human luteinizing hormone receptor gene in human uterine arteries. J. Clin. Endocrinol. Metab. 79, 307-315.
7. Cole, L. A., and Butler, S. A. (2008) Hyperglycosylated human chorionic gonadotropin and human chorionic gonadotropin free beta-subunit: tumor markers and tumor promoters. J. Reprod. Med. 53, 499-512.
8. Guibourdenche, J., Handschuh, K., Tsatsaris, V., Gerbaud, P., Leguy, M. C., Muller, F., Brion, D. E., and Fournier, T. (2010) Hyperglycosylated hCG is a marker of early human trophoblast invasion. J. Clin. Endocrinol. Metab. 95, E240-E244.
9. Cole, L. A. (1997) Immunoassay of human chorionic gonadotropin, its free subunits, and metabolites. Clin. Chem. 43, 2233- 2243.
10. Hamada, A. L., Nakabayashi, K., Sato, A., Kiyoshi, K., Takamatsu, Y., Laoag-Fernandez, J. B., Ohara, N., and Maruo, T. (2005) Transfection of antisense chorionic gonadotropin beta gene into choriocarcinoma cells suppresses the cell proliferation and induces apoptosis. J. Clin. Endocrinol. Metab. 90, 4873- 4879.
11. Sasaki, Y., Ladner, D. G., and Cole, L. A. (2008) Hyperglycosylated human chorionic gonadotropin and the source of pregnancy failures. Fertil. Steril. 89, 1781-1786.
12. Cole, L. A. (2007) Hyperglycosylated hCG. Placenta 28, 977-986.
13. Cole, L. A., Butler, S. A., Khanlian, S. A., Giddings, A., Muller, C. Y., Seckl, M. J., and Kohorn, E. I. (2006) Gestational trophoblastic diseases: 2. Hyperglycosylated hCG as a reliable marker of active neoplasia. Gynecol. Oncol. 102, 151-159.
14. Kovalevskaya, G., Kakuma, T., Schlatterer, J., and O'Connor, J. F. (2007) Hyperglycosylated HCG expression in pregnancy: cellular origin and clinical applications. Mol. Cell. Endocrinol. 260, 262, 237-243.
15. Cole, L. A. (2010) Hyperglycosylated hCG, a review. Placenta 31, 653-664.
16. Bersinger, N. A., Wunder, D. M., Nicolas, M., Birkhauser, M. H., Porquet, D., and Guibourdenche, J. (2008) Serum hyperglycosylated human chorionic gonadotropin to predict the gestational outcome in in vitro fertilization/ intracytoplasmic sperm injection pregnancies. Fetal Diagn. Ther. 24, 74-78.
17. Wu, H., Lustbader, J. W., Liu, Y., Canfield, R. E., and Hendrickson, W. A. (1994) Structure of human chorionic gonadotropin at 2.6 A resolution from MAD analysis of the selenomethionyl protein. Structure 2, 545-558.
18. Iles, R. K., Delves, P. J., and Butler, S. A. (2010) Does hCG or hCGbeta play a role in cancer cell biology? Mol. Cell. Endocrinol. 329, 62-70.
19. Cole, L. A. (2010) Biological functions of hCG and hCG-related molecules. Reprod. Biol. Endocrinol. 8, 102.
20. Ingman, W. V., and Robertson, S. A. (2002) Defining the actions of transforming growth factor beta in reproduction. Bioessays 24, 904-914.
21. Herrler, A., von Rango, U., and Beier, H. M. (2003) Embryomaternal signalling: how the embryo starts talking to its mother to accomplish implantation. Reprod. Biomed. Online 6, 244 -256.
22. Dimitriadis, E., White, C. A., Jones, R. L., and Salamonsen, L. A. (2005) Cytokines, chemokines and growth factors in endometrium related to implantation. Hum. Reprod. Update 11, 613-630.
23. Feinberg, R. F., Kliman, H. J., and Wang, C. L. (1994) Transforming growth factor-beta stimulates trophoblast oncofetal fibronectin synthesis in vitro: implications for trophoblast implantation in vivo. J. Clin. Endocrinol. Metab. 78, 1241-1248.
24. Chung, I. B., Yelian, F. D., Zaher, F. M., Gonik, B., Evans, M. I., Diamond, M. P., and Svinarich, D. M. (2000) Expression and regulation of vascular endothelial growth factor in a first trimester trophoblast cell line. Placenta 21, 320-324.
25. Irving, J. A., and Lala, P. K. (1995) Functional role of cell surface integrins on human trophoblast cell migration: regulation by TGF-beta, IGF-II, and IGFBP-1. Exp. Cell Res. 217, 419-427.
26. Goumans, M. J., and Mummery, C. (2000) Functional analysis of the TGFbeta receptor/Smad pathway through gene ablation in mice. Int. J. Dev. Biol. 44, 253-265.
27. Goumans, M. J., Zwijsen, A., van Rooijen, M. A., Huylebroeck, D., Roelen, B. A., and Mummery, C. L. (1999) Transforming growth factor-beta signalling in extraembryonic mesoderm is required for yolk sac vasculogenesis in mice. Development 126, 3473-3483.
28. Hawinkels, L. J., Kuiper, P., Wiercinska, E., Verspaget, H. W., Liu, Z., Pardali, E., Sier, C. F., and ten Dijke, P. (2010) Matrix metalloproteinase-14 (MT1-MMP)-mediated endoglin shedding inhibits tumor angiogenesis. Cancer Res. 70, 4141-4150.
29. Caniggia, I., Taylor, C. V., Ritchie, J. W., Lye, S. J., and Letarte, M. (1997) Endoglin regulates trophoblast differentiation along the invasive pathway in human placental villous explants. Endocrinology 138, 4977-4988.
30. Fonsatti, E., Del Vecchio, L., Altomonte, M., Sigalotti, L., Nicotra, M. R., Coral, S., Natali, P. G., and Maio, M. (2001) Endoglin: An accessory component of the TGF-beta-binding receptor-complex with diagnostic, prognostic, and bioimmunotherapeutic potential in human malignancies. J. Cell. Physiol. 188, 1-7.
31. Lebrin, F., Goumans, M. J., Jonker, L., Carvalho, R. L., Valdimarsdottir, G., Thorikay, M., Mummery, C., Arthur, H. M., and ten Dijke, P. (2004) Endoglin promotes endothelial cell proliferation and TGF-beta/ALK1 signal transduction. EMBO J. 23, 4018-4028.
32. Pepper, M. S. (1997) Transforming growth factor-beta: vasculogenesis, angiogenesis, and vessel wall integrity. Cytokine Growth Factor Rev. 8, 21-43.
33. Orlova, V. V., Liu, Z., Goumans, M. J., and ten Dijke, P. (2011) Controlling angiogenesis by two unique TGF-beta type I receptor signaling pathways. Histol. Histopathol. 26, 1219-1230.
34. Owens, G. K. (1995) Regulation of differentiation of vascular smooth muscle cells. Physiol. Rev. 75, 487-517.
35. Hungerford, J. E., Owens, G. K., Argraves, W. S., and Little, C. D. (1996) Development of the aortic vessel wall as defined by vascular smooth muscle and extracellular matrix markers. Dev. Biol. 178, 375-392.
36. Birken, S., Berger, P., Bidart, J. M., Weber, M., Bristow, A., Norman, R., Sturgeon, C., and Stenman, U. H. (2003) Preparation and characterization of new WHO reference reagents for human chorionic gonadotropin and metabolites. Clin. Chem. 49, 144-154.
37. Zhang, F. P., Poutanen, M., Wilbertz, J., and Huhtaniemi, I. (2001) Normal prenatal but arrested postnatal sexual development of luteinizing hormone receptor knockout (LuRKO) mice. Mol. Endocrinol. 15, 172-183.
38. Berndt, S., Blacher, S., Perrier, d. S., Thiry, M., Tsampalas, M., Cruz, A., Pequeux, C., Lorquet, S., Munaut, C., Noel, A., and Foidart, J. M. (2009) Chorionic gonadotropin stimulation of angiogenesis and pericyte recruitment. J. Clin. Endocrinol. Metab. 94, 4567-4574.
39. Blacher, S., Devy, L., Burbridge, M. F., Roland, G., Tucker, G., Noel, A., and Foidart, J. M. (2001) Improved quantification of angiogenesis in the rat aortic ring assay. Angiogenesis 4, 133-142.
40. Myoken, Y., Kan, M., Sato, G. H., McKeehan, W. L., and Sato, J. D. (1990) Bifunctional effects of transforming growth factor-beta (TGF-beta) on endothelial cell growth correlate with phenotypes of TGF-beta binding sites. Exp. Cell Res. 191, 299- 304.
41. Ascoli, M. (1981) Characterization of several clonal lines of cultured Leydig tumor cells: gonadotropin receptors and steroidogenic responses. Endocrinology 108, 88-95.
42. Dennler, S., Itoh, S., Vivien, D., ten Dijke, P., Huet, S., and Gauthier, J. M. (1998) Direct binding of Smad3 and Smad4 to critical TGF beta-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. EMBO J. 17, 3091- 3100.
43. Cole, L. A., Khanlian, S. A., Riley, J. M., and Butler, S. A. (2006) Hyperglycosylated hCG in gestational implantation and in choriocarcinoma and testicular germ cell malignancy tumorigenesis. J. Reprod. Med. 51, 919-929.
44. Khoo, N. K., Bechberger, J. F., Shepherd, T., Bond, S. L., McCrae, K. R., Hamilton, G. S., and Lala, P. K. (1998) SV40 Tag transformation of the normal invasive trophoblast results in a premalignant phenotype. I. Mechanisms responsible for hyperinvasiveness and resistance to anti-invasive action of TGFbeta. Int. J. Cancer 77, 429-439.
45. Butler, S. A., Ikram, M. S., Mathieu, S., and Iles, R. K. (2000) The increase in bladder carcinoma cell population induced by the free beta subunit of human chorionic gonadotrophin is a result of an anti-apoptosis effect and not cell proliferation. Br. J. Cancer 82, 1553-1556.
46. Lapthorn, A. J., Harris, D. C., Littlejohn, A., Lustbader, J. W., Canfield, R. E., Machin, K. J., Morgan, F. J., and Isaacs, N. W. (1994) Crystal structure of human chorionic gonadotropin. Nature 369, 455-461.
47. Cole, L. A. (2012) HCG variants, the growth factors which drive human malignancies. Am. J. Cancer Res. 2, 22-35.
48. Zygmunt, M., Herr, F., Keller-Schoenwetter, S., Kunzi-Rapp, K., Munstedt, K., Rao, C. V., Lang, U., and Preissner, K. T. (2002) Characterization of human chorionic gonadotropin as a novel angiogenic factor. J. Clin. Endocrinol. Metab. 87, 5290-5296.
49. Cole, L. A., Dai, D., Butler, S. A., Leslie, K. K., and Kohorn, E. I. (2006) Gestational trophoblastic diseases: 1. Pathophysiology of hyperglycosylated hCG. Gynecol. Oncol. 102, 145-150.
50. Venkatesha, S., Toporsian, M., Lam, C., Hanai, J., Mammoto, T., Kim, Y. M., Bdolah, Y., Lim, K. H., Yuan, H. T., Libermann, T. A., Stillman, I. E., Roberts, D., D'Amore, P. A., Epstein, F. H., Sellke, F. W., Romero, R., Sukhatme, V. P., Letarte, M., and Karumanchi, S. A. (2006) Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat. Med. 12, 642-649.
51. Handschuh, K., Guibourdenche, J., Tsatsaris, V., Guesnon, M., Laurendeau, I., Evain-Brion, D., and Fournier, T. (2007) Human chorionic gonadotropin expression in human trophoblasts from early placenta: comparative study between villous and extravillous trophoblastic cells. Placenta 28, 175-184.
52. Handschuh, K., Guibourdenche, J., Tsatsaris, V., Guesnon, M., Laurendeau, I., Evain-Brion, D., and Fournier, T. (2007) Human chorionic gonadotropin produced by the invasive trophoblast but not the villous trophoblast promotes cell invasion and is down-regulated by peroxisome proliferator-activated receptor- gamma. Endocrinology 148, 5011-5019.
53. Cole, L. A., and Butler, S. (2012) Hyperglycosylated hCG, hCGbeta and Hyperglycosylated hCGbeta: Interchangeable cancer promoters. Mol. Cell. Endocrinol. 349, 232-238.
54. Iles, R. K., and Butler, S. A. (2010) Gonadotropins and gonadotropin receptors- evolutional genetics, signalling mechanisms, extra gonadal function and roles in oncogenesis. Mol. Cell. Endocrinol. 329, 1-2.