Reprint of: Betaglycan: A multifunctional accessory

Molecular and Cellular Endocrinology

Volumn 359, Issue 1-2, 2012, Pages 13-22

  Bilandzic, Maree ^a   Stenvers, Kaye L ^a  

^a HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

Betaglycan; Inhibin; TGF receptor III

Indexed keywords

ACTIVIN A; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; FOLLITROPIN; GLYCOSAMINOGLYCAN; GONADOTROPIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INHIBIN; INHIBIN A; INHIBIN B; MYELOPID; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 3; TRANSFORMING GROWTH FACTOR BETA2;

ADENOHYPOPHYSIS; ADRENAL GLAND; AMINO ACID COMPOSITION; ARTICLE; BINDING SITE; CANCER GROWTH; CANCER INHIBITION; CARBOXY TERMINAL SEQUENCE; CARCINOGENESIS; CELL FUNCTION; CYTOPLASM; ENDOCYTOSIS; EXTRACELLULAR SPACE; GENE OVEREXPRESSION; GENE SILENCING; GONAD; HETEROZYGOSITY LOSS; HORMONE RECEPTOR INTERACTION; HUMAN; HYPOPHYSIS; LIGAND BINDING; NONHUMAN; OVARY CANCER; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN TRANSPORT; REPRODUCTION; SIGNAL TRANSDUCTION; STEROIDOGENESIS; TRANSCRIPTION REGULATION;

EID: 84861692930     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2012.03.020     Document Type: Article

References (112)

1. Anderson R.A., Cambray N., Hartley P.S., McNeilly A.S. Expression and localization of inhibin alpha, inhibin/activin betaA and betaB and the activin type II and inhibin beta-glycan receptors in the developing human testis. Reproduction 2002, 123:779-788.
2. Andres J., DeFalcis D., Noda M., Massagué J. Binding of two growth factor families to separate domains of the proteoglycan betaglycan. J. Biol. Chem. 1992, 267:5927-5930.
3. Andres J.L., Stanley K., Cheifetz S., Massague J. Membrane-anchored and soluble forms of betaglycan, a polymorphic proteoglycan that binds transforming growth factor-beta. J. Cell Biol. 1989, 109:3137-3145.
4. Balanathan P., Williams E.D., Wang H., Pedersen J.S., Horvath L.G., Achen M.G., Stacker S.A., Risbridger G.P. Elevated level of inhibin-[alpha] subunit is pro-tumourigenic and pro-metastatic and associated with extracapsular spread in advanced prostate cancer. Br. J. Cancer 2009, 100:1784-1793.
5. Bernabeu C., Lopez-Novoa J.M., Quintanilla M. The emerging role of TGF-[beta] superfamily coreceptors in cancer. Biochim. Biophys. Acta (BBA): Mol. Basis Dis. 2009, 1792:954-973.
6. Bernard D.J. Editorial commentary: SMAD expression in the testis predicts age- and cell-specific responses to activin and TGFbeta. J. Androl. 2003, 24:201-203.
7. Bierie B., Moses H.L. TGF-b and cancer. Cytokine Growth Factor Rev. 2010, 17:29-40.
8. Bilandzic M., Chu S., Farnworth P.G., Harrison C., Nicholls P., Wang Y., Escalona R.M., Fuller P.J., Findlay J.K., Stenvers K.L. Loss of betaglycan contributes to the malignant properties of human granulosa tumor cells. Mol. Endocrinol. 2009, 23:539-548.
9. Blair C.R., Stone J.B., Wells R.G. The type III TGF-beta receptor betaglycan transmembrane-cytoplasmic domain fragment is stable after ectodomain cleavage and is a substrate of the intramembrane protease gamma-secretase. Biochim. Biophys. Acta 2011, 1813:332-339.
10. Blobe G.C., Liu X., Fang S.J., How T., Lodish H.F. A novel mechanism for regulating transforming growth factor β (TGF-β) signaling. J. Biol. Chem. 2001, 276:39608-39617.
11. Boggess J., Soules M., Goff B., Greer B., Cain J., Tamimi H. Serum inhibin and disease status in women with ovarian granulosa cell tumors. Gynecol. Oncol. 1997, 64:64-69.
12. Brown C.B., Boyer A.S., Runyan R.B., Barnett J.V. Requirement of type III TGF-b receptor for endocardial cell transformation in the heart. Science 1999, 283:2080-2082.
13. Chand A.L., Ooi G.T., Harrison C.A., Shelling A.N., Robertson D.M. Functional analysis of the human inhibin α subunit variant A257T and its potential role in premature ovarian failure. Hum. Reprod. 2007, 22:3241-3248.
14. Chand A.L., Robertson D.M., Shelling A.N., Harrison C.A. Mutational analysis of betaglycan/TGF-[beta]RIII in premature ovarian failure. Fertil. Steril. 2007, 87:210-212.
15. Cheifetz S., Andres J.L., Massague J. The transforming growth factor-b receptor type III is a membrane proteoglycan. J. Biol. Chem. 1988, 263:16984-16991.
16. Cheifetz S., Hernandez H., Laiho M., ten Dijke P., Iwata K., Massagué J. Distinct transforming growth factor-beta (TGF-beta) receptor subsets as determinants of cellular responsiveness to three TGF-beta isoforms. J. Biol. Chem. 1990, 265:20533-20538.
17. Chen W., Kirkbride K.C., How T., Nelson C.D., Mo J., Frederick J.P., Wang X.-F., Lefkowitz R.J., Blobe G.C. b-Arrestin 2 mediates endocytosis of type III TGF-b receptor and down-regulation of its signaling. Science 2003, 301:1394-1397.
18. Chen Y.-G. Endocytic regulation of TGF-beta signaling. Cell Res. 2009, 19:58-70.
19. Cheung H., Mei J., Xu R. Quantification of soluble betaglycan in porcine milk. Asia Pac. J. Clin. Nutr. 2004, 12.
20. Compton L.A., Potash D.A., Brown C.B., Barnett J.V. Coronary vessel development is dependent on the type III transforming growth factor {beta} receptor. Circ. Res. 2007, 101:784-791.
21. Cooper S.J., Zou H., LeGrand S.N., Marlow L.A., von Roemeling C.A., Radisky D.C., Wu K.J., Hempel N., Margulis V., Tun H.W., Blobe G.C., Wood C.G., Copland J.A. Loss of type III transforming growth factor-[beta] receptor expression is due to methylation silencing of the transcription factor GATA3 in renal cell carcinoma. Oncogene 2010, 29:2905-2915.
22. Copland J., Luxon B., Ajani L., Maity T., Campagnaro E., Guo H., LeGrand S., Tamboli P., Wood C. Genomic profiling identifies alterations in TGFbeta signaling through loss of TGFbeta receptor expression in human renal cell carcinogenesis and progression. Oncogene 2003, 22:8053-8062.
23. Criswell T.L., Arteaga C.L. Modulation of NF{kappa}B activity and E-cadherin by the type III transforming growth factor beta receptor regulates cell growth and motility. J. Biol. Chem. 2007, 282:32491-32500.
24. Criswell T.L., Dumont N., Barnett J.V., Arteaga C.L. Knockdown of the transforming growth factor-β type III receptor impairs motility and invasion of metastatic cancer cells. Cancer Res. 2008, 68:7304-7312.
25. de Fraipont F., El Atifi M., Cherradi N., Le Moigne G., Defaye G., Houlgatte R., Bertherat J., Bertagna X., Plouin P.F., Baudin E., Berger F., Gicquel C., Chabre O., Feige J.J. Gene expression profiling of human adrenocortical tumors using complementary deoxyribonucleic acid microarrays identifies several candidate genes as markers of malignancy. J. Clin. Endocrinol. Metab. 2005, 90:1819-1829.
26. Denzer K., Kleijmeer M.J., Heijnen H.F., Stoorvogel W., Geuze H.J. Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J. Cell Sci. 2000, 113:3365-3374.
27. Dixit H., Rao K.L., Padmalatha V.V., Kanakavalli M., Deenadayal M., Gupta N., Chakrabarty B.N., Singh L. Mutational analysis of the betaglycan gene-coding region in susceptibility for ovarian failure. Hum. Reprod. 2006, 21:2041-2046.
28. Dong M., How T., Kirkbride K., Gordon K., Lee J., Hempel N., Kelly P., Moeller B., Marks J., Blobe G. The type III TGF-beta receptor suppresses breast cancer progression. J. Clin. Invest. 2007, 117:206-217.
29. Drummond A.E., Le M.T., Ethier J.-F., Dyson M., Findlay J.K. Expression and localization of activin receptors, Smads, and {beta}glycan to the postnatal rat ovary. Endocrinology 2002, 143:1423-1433.
30. Drummond A.E., Mitzi D., Le M.T., Ethier J.-F., Findlay J.K. Ovarian follicle populations of the rat express TGF-[beta] signalling pathways. Proceedings of the Fifth Sapporo International Symposium on Ovarian Function: Basic and Clinical Updates in Ovarian Function, vol. 202 2003, 53-57.
31. Eickelberg O., Centrella M., Reiss M., Kashgarian M., Wells R.G. Betaglycan inhibits TGF-β signaling by preventing type I-type II receptor complex formation. J. Biol. Chem. 2002, 277:823-829.
32. Escalona R.M., Stenvers K.L., Farnworth P.G., Findlay J.K., Ooi G.T. Reducing betaglycan expression by RNA interference (RNAi) attenuates inhibin bioactivity in L[beta]T2 gonadotropes. Mol. Cell. Endocrinol. 2009, 307:149-156.
33. Esparza-López J., Montiel J.L., Vilchis-Landeros M.M., Okadome T., Miyazono K., López-Casillas F. Ligand binding and functional properties of betaglycan, a co-receptor of the transforming growth factor-β superfamily. J. Biol. Chem. 2001, 276:14588-14596.
34. Ethier J.-F., Farnworth P.G., Findlay J.K., Ooi G.T. Transforming growth factor-{beta} modulates inhibin A bioactivity in the L{beta}T2 gonadotrope cell line by competing for binding to betaglycan. Mol. Endocrinol. 2002, 16:2754-2763.
35. Farnworth P.G., Stanton P.G., Wang Y., Escalona R., Findlay J.K., Ooi G.T. Inhibins differentially antagonize activin and bone morphogenetic protein action in a mouse adrenocortical cell line. Endocrinology 2006, 147:3462-3471.
36. Farnworth P.G., Wang Y., Escalona R., Leembruggen P., Ooi G.T., Findlay J.K. Transforming growth factor-{beta} blocks inhibin binding to different target cell types in a context-dependent manner through dual mechanisms involving betaglycan. Endocrinology 2007, 148:5355-5368.
37. Farnworth P.G., Wang Y., Leembruggen P., Ooi G.T., Harrison C., Robertson D.M., Findlay J.K. Rodent adrenocortical cells display high affinity binding sites and proteins for inhibin A, and express components required for autocrine signalling by activins and bone morphogenetic proteins. J. Endocrinol. 2006, 188:451-465.
38. Finger E.C., Lee N.Y., You H.-J., Blobe G.C. Endocytosis of the type III transforming growth factor-β (TGF-β) receptor through the clathrin-independent/lipid raft pathway regulates TGF-β signaling and receptor down-regulation. J. Biol. Chem. 2008, 283:34808-34818.
39. Finger E.C., Turley R.S., Dong M., How T., Fields T.A., Blobe G.C. TGFBRIII suppresses non-small cell lung cancer invasiveness and tumorigenicity. Carcinogenesis 2008, 29:528-535.
40. Florio P., Ciarmela P., Reis F.M., Toti P., Galleri L., Santopietro R., Tiso E., Tosi P., Petraglia F. Inhibin {alpha}-subunit and the inhibin coreceptor betaglycan are downregulated in endometrial carcinoma. Eur. J. Endocrinol. 2005, 152:277-284.
41. Fuller P.J., Chu S. Signalling pathways in the molecular pathogenesis of ovarian granulosa cell tumours. Trends Endocrinol. Metab. 2004, 15:122-128.
42. Gatza C.E., Oh S.Y., Blobe G.C. Roles for the type III TGF-[beta] receptor in human cancer. Cell. Signal. 2010, 22:1163-1174.
43. Glister C., Satchell L., Knight P.G. Changes in expression of bone morphogenetic proteins (BMPs), their receptors and inhibin co-receptor betaglycan during bovine antral follicle development: inhibin can antagonize the suppressive effect of BMPs on thecal androgen production. Reproduction 2010, 140:699-712.
44. Gordon K.J., Dong M., Chislock E.M., Fields T.A., Blobe G.C. Loss of type III transforming growth factor b receptor expression increases motility and invasiveness associated with epithelial to mesenchymal transition during pancreatic cancer progression. Carcinogenesis 2008, 29:252-262.
45. Gordon K.J., Kirkbride K.C., How T., Blobe G.C. Bone morphogenetic proteins induce pancreatic cancer cell invasiveness through a Smad1-dependent mechanism that involves matrix metalloproteinase-2. Carcinogenesis 2009, 30:238-248.
46. Hamar B.D., Buhimschi I.A., Sfakianaki A.K., Pettker C.M., Magloire L.K., Funai E.F., Copel J.A., Buhimschi C.S. Serum and urine inhibin A but not free activin A are endocrine biomarkers of severe pre-eclampsia. Am. J. Obstet. Gynecol. 2006, 195:1636-1645.
47. Hempel N., How T., Cooper S.J., Green T.R., Dong M., Copland J.A., Wood C.G., Blobe G.C. Expression of the type III TGF-b receptor is negatively regulated by TGF-b. Carcinogenesis 2008, 29:905-912.
48. Hempel N., How T., Dong M., Murphy S.K., Fields T.A., Blobe G.C. Loss of betaglycan expression in ovarian cancer: role in motility and invasion. Cancer Res. 2007, 67:5231-5238.
49. Hill C.S. Nucleocytoplasmic shuttling of Smad proteins. Cell Res. 2009, 19:36-46.
50. Hofland J., Timmerman M.A., de Herder W.W., van Schaik R.H., de Krijger R.R., de Jong F.H. Expression of activin and inhibin subunits, receptors and binding proteins in human adrenocortical neoplasms. Clin. Endocrinol. (Oxf.) 2006, 65:792-799.
51. Hsueh A.J., Dahl K.D., Vaughan J., Tucker E., Rivier J., Bardin C.W., Vale W. Heterodimers and homodimers of inhibin subunits have different paracrine action in the modulation of luteinizing hormone-stimulated androgen biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 1987, 84:5082-5086.
52. Ikushima H., Miyazono K. TGFb signalling: a complex web in cancer progression. Nat. Rev. Cancer 2010, 10:415-424.
53. Itman C., Mendis S., Barakat B., Loveland K.L. All in the family: TGF-beta family action in testis development. Reproduction 2006, 132:233-246.
54. Jullien J., Gurdon J. Morphogen gradient interpretation by a regulated trafficking step during ligand-receptor transduction. Genes Dev. 2005, 19:2682-2694.
55. Kardassis D., Murphy C., Fotsis T., Moustakas A., Stournaras C. Control of transforming growth factor β signal transduction by small GTPases. FEBS J. 2009, 276:2947-2965.
56. Kirkbride K.C., Townsend T.A., Bruinsma M.W., Barnett J.V., Blobe G.C. Bone morphogenetic proteins signal through the transforming growth factor-{beta} type III receptor. J. Biol. Chem. 2008, 283:7628-7637.
57. Knight P.G., Glister C. TGF-{beta} superfamily members and ovarian follicle development. Reproduction 2006, 132:191-206.
58. Kovacs J.J., Hara M.R., Davenport C.L., Kim J., Lefkowitz R.J. Arrestin development: emerging roles for [beta]-arrestins in developmental signaling pathways. Dev. Cell 2009, 17:443-458.
59. Kumanov P., Nandipati K., Tomova A., Robeva R., Agarwal A. Significance of inhibin in reproductive pathophysiology and current clinical applications. Reprod. Biomed. 2005, 10:786-812.
60. Le Roy C., Leduque P., Yuan Li J., Saez J.M., Langlois D. Antisense oligonucleotide targeting the transforming growth factor beta1 increases expression of specific genes and functions of Leydig cells. Eur. J. Biochem. 1998, 257:506-514.
61. Le Roy C., Lejeune H., Chuzel F., Saez J.M., Langlois D. Autocrine regulation of Leydig cell differentiated functions by insulin-like growth factor I and transforming growth factor beta. J. Steroid Biochem. Mol. Biol. 1999, 69:379-384.
62. Lee J.D., Hempel N., Lee N.Y., Blobe G.C. The type III TGF-β receptor suppresses breast cancer progression through GIPC-mediated inhibition of TGF-β signaling. Carcinogenesis 2010, 31:175-183.
63. Lee N.Y., Kirkbride K.C., Sheu R.D., Blobe G.C. The transforming growth factor-{beta} type III receptor mediates distinct subcellular trafficking and downstream signaling of activin-like kinase (ALK)3 and ALK6 receptors. Mol. Biol. Cell 2009, 20:4362-4370.
64. Lewis K., Gray P., Blount A., MacConell L., Wiater E., Bilezikjian L., Vale W. Betaglycan binds inhibin and can mediate functional antagonism of activin signalling. Nature 2000, 404:411-414.
65. Lin T., Calkins J.K., Morris P.L., Vale W., Bardin C.W. Regulation of Leydig cell function in primary culture by inhibin and activin. Endocrinology 1989, 125:2134-2140.
66. Ling N., Ying S.-Y., Ueno N., Shimasaki S., Esch F., Hotta M., Guillemin R. Pituitary FSH is released by a heterodimer of the [beta]-subunits from the two forms of inhibin. Nature 1986, 321:779-782.
67. Liu J., Kuulasmaa T., Kosma V.-M., Butzow R., Vanttinen T., Hyden-Granskog C., Voutilainen R. Expression of betaglycan, an inhibin coreceptor, in normal human ovaries and ovarian sex cord-stromal tumors and its regulation in cultured human granulosa-luteal cells. J. Clin. Endocrinol. Metab. 2003, 88:5002-5008.
68. Lönn P., Morén A., Raja E., Dahl M., Moustakas A. Regulating the stability of TGFbold beta receptors and Smads. Cell Res. 2009, 19:21-35.
69. Looyenga B.D., Wiater E., Vale W., Hammer G.D. Inhibin-A antagonizes TGF{beta}2 signaling by down-regulating cell surface expression of the TGF{beta} coreceptor betaglycan. Mol. Endocrinol. 2010, 24:608-620.
70. López-Casillas F., Cheifetz S., Doody J., Andres J.L., Lane W.S., Massague J. Structure and expression of the membrane proteoglycan betaglycan, a component of the TGF-[beta] receptor system. Cell 1991, 67:785-795.
71. López-Casillas F., Payne H., Andres J., Massague J. Betaglycan can act as a dual modulator of TGF-beta access to signaling receptors: mapping of ligand binding and GAG attachment sites. J. Cell Biol. 1994, 124:557-568.
72. López-Casillas F., Wrana J.L., Massagué J. Betaglycan presents ligand to the TGF[beta] signaling receptor. Cell 1993, 73:1435-1444.
73. Loveland K.L., Dias V., Meachem S., Rajpert-De Meyts E. The transforming growth factor-beta superfamily in early spermatogenesis: potential relevance to testicular dysgenesis. Int. J. Androl. 2007, 30:377-384. discussion 384.
74. Makanji Y., Kl W., Mc W., Kl C., Dm R., Ca H. Suppression of inhibin A biological activity by alterations in the binding site for betaglycan. J. Biol. Chem. 2008, 283:16743-16751.
75. Makanji Y., Temple-Smith P.D., Walton K.L., Harrison C.A., Robertson D.M. Inhibin B is a more potent suppressor of rat follicle-stimulating hormone release than inhibin a in vitro and in vivo. Endocrinology 2009, 150:4784-4793.
76. Margulis V., Maity T., Zhang X.-Y., Cooper S.J., Copland J.A., Wood C.G. Type III transforming growth factor-b (TGF-b) receptor mediates apoptosis in renal cell carcinoma independent of the canonical TGF-b signaling pathway. Clin. Cancer Res. 2008, 14:5722-5730.
77. Matzuk M., Finegold M., Su J., Hsueh A., Bradley A. Alpha-inhibin is a tumour-suppressor gene with gonadal specificity in mice. Nature 1992, 360:313-319.
78. Mauduit C., Chauvin M.A., de Peretti E., Morera A.M., Benahmed M. Effect of activin A on dehydroepiandrosterone and testosterone secretion by primary immature porcine Leydig cells. Biol. Reprod. 1991, 45:101-109.
79. McLean S., Di Guglielmo G.M. TGFb(transforming growth factor b) receptor type III directs clathrin-mediated endocytosis of TGFb receptor types b I and II. Biochem. J. 2010, 429:137-145.
80. Mendoza V., Vilchis-Landeros M.M., Mendoza-Hernandez G., Huang T., Villarreal M.M., Hinck A.P., López-Casillas F., Montiel J.-L. Betaglycan has two independent domains required for high affinity TGFb binding: proteolytic cleavage separates the domains and inactivates the neutralizing activity of the soluble receptor. Biochemistry 2009, 48:11755-11765.
81. Mom C., Engelen M., Willemse P., Gietema J., ten Hoor K., de Vries E., van der Zee A. Granulosa cell tumors of the ovary: the clinical value of serum inhibin A and B levels in a large single center cohort. Gynecol. Oncol. 2007, 105:365-372.
82. Mythreye K., Blobe G.C. The type III TGF-b receptor regulates epithelial and cancer cell migration through b-arrestin2-mediated activation of Cdc42. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:8221-8226.
83. Olaso R., Pairault C., Saez J.M., Habert R. Transforming growth factor beta3 in the fetal and neonatal rat testis: immunolocalization and effect on fetal Leydig cell function. Histochem. Cell Biol. 1999, 112:247-254.
84. Omori Y., Nakamura K., Yamashita S., Matsuda H., Mizutani T., Miyamoto K., Minegishi T. Effect of follicle-stimulating hormone and estrogen on the expression of betaglycan messenger ribonucleic acid levels in cultured rat granulosa cells. Endocrinology 2005, 146:3379-3386.
85. Pepin M.C., Beauchemin M., Plamondon J., O'Connor-McCourt M.D. Mapping of the ligand binding domain of the transforming growth factor beta receptor type III by deletion mutagenesis. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:6997-7001.
86. Risbridger G.P., Clements J., Robertson D.M., Drummond A.E., Muir J., Burger H.G., de Kretser D.M. Immuno- and bioactive inhibin and inhibin alpha-subunit expression in rat Leydig cell cultures. Mol. Cell. Endocrinol. 1989, 66:119-122.
87. Robertson D.M., Oehler M.K. Emerging role of inhibin as a biomarker for ovarian cancer. Women's Health 2005, 1:51-57.
88. Sarraj M.A., Chua H.K., Umbers A., Loveland K.L., Findlay J.K., Stenvers K.L. Differential expression of TGFBR3 (betaglycan) in mouse ovary and testis during gonadogenesis. Growth Factors 2007, 25:334-345.
89. Sarraj M.A., Escalona R.M., Umbers A., Chua H.K., Small C., Griswold M., Loveland K., Findlay J.K., Stenvers K.L. Fetal testis dysgenesis and compromised leydig cell function in Tgfbr3 (Betaglycan) knockout mice. Biol. Reprod. 2010, 82:153-162.
90. Segarini P.R., Rosen D.M., Seyedin S.M. Binding of transforming growth factor-{beta} to cell surface proteins varies with cell type. Mol. Endocrinol. 1989, 3:261-272.
91. Sharifi N., Hurt E.M., Kawasaki B.T., Farrar W.L. TGFBR3 loss and consequences in prostate cancer. Prostate 2007, 67:301-311.
92. Steller M.D., Shaw T.J., Vanderhyden B.C., Ethier J.-F. Inhibin resistance is associated with aggressive tumorigenicity of ovarian cancer cells. Mol. Cancer Res. 2005, 3:50-61.
93. Stenvers K.L., Findlay J.K. Inhibins: from reproductive hormones to tumor suppressors. Trends Endocrinol. Metab. 2010, 21:174-180.
94. Stenvers K.L., Tursky M.L., Harder K.W., Kountouri N., Amatayakul-Chantler S., Grail D., Small C., Weinberg R.A., Sizeland A.M., Zhu H.-J. Heart and liver defects and reduced transforming growth factor {beta}2 sensitivity in transforming growth factor {beta} type III receptor-deficient embryos. Mol. Cell. Biol. 2003, 23:4371-4385.
95. Tsigkou A., Luisi S., De Leo V., Patton L., Gambineri A., Reis F.M., Pasquali R., Petraglia F. High serum concentration of total inhibin in polycystic ovary syndrome. Fertil. Steril. 2008, 90:1859-1863.
96. Tsigkou A., Luisi S., Reis F.M., Petraglia F. Inhibins as diagnostic markers in human reproduction. Adv. Clin. Chem. 2008, 45:1-29.
97. Tsigkou A., Marrelli D., Reis F.M., Luisi S., Silva-Filho A.L., Roviello F., Triginelli S.A., Petraglia F. Total inhibin is a potential serum marker for epithelial ovarian cancer. J. Clin. Endocrinol. Metab. 2007, 92:2526-2531.
98. Turley R.S., Finger E.C., Hempel N., How T., Fields T.A., Blobe G.C. The type III transforming growth factor-{beta} receptor as a novel tumor suppressor gene in prostate cancer. Cancer Res. 2007, 67:1090-1098.
99. Vale W., Rivier J., Vaughan J., McClintock R., Corrigan A., Woo W., Karr D., Spiess J. Purification and characterization of an FSH releasing protein from porcine ovarian follicular fluid. Nature 1986, 321:776-779.
100. Vanttinen T., Kuulasmaa T., Liu J., Voutilainen R. Expression of activin/inhibin receptor and binding protein genes and regulation of activin/inhibin peptide secretion in human adrenocortical cells. J. Clin. Endocrinol. Metab. 2002, 87:4257-4263.
101. Vanttinen T., Liu J., Kuulasmaa T., Kivinen P., Voutilainen R. Expression of activin/inhibin signaling components in the human adrenal gland and the effects of activins and inhibins on adrenocortical steroidogenesis and apoptosis. J. Endocrinol. 2003, 178:479-489.
102. Velasco-Loyden G., Arribas J., López-Casillas F. The shedding of betaglycan is regulated by pervanadate and mediated by membrane type matrix metalloprotease-1. J. Biol. Chem. 2004, 279:7721-7733.
103. Walker K.A., Sims-Lucas S., Caruana G., Cullen-McEwen L., Li J., Sarraj M.A., Bertram J.F., Stenvers K.L. Betaglycan is required for the establishment of nephron endowment in the mouse. PLoS ONE 2011, 6(4):e18723. 10.1371/journal.pone.0018723.
104. Wang X.-F., Lin H.Y., Ng-Eaton E., Downward J., Lodish H.F., Weinberg R.A. Expression cloning and characterization of the TGF-[beta] type III receptor. Cell 1991, 67:797-805.
105. Webber J., Steadman R., Mason M.D., Tabi Z., Clayton A. Cancer exosomes trigger fibroblast to myofibroblast differentiation. Cancer Res. 2010, 70:9621-9630.
106. Wiater E., Harrison C.A., Lewis K.A., Gray P.C., Vale W.W. Identification of distinct inhibin and transforming growth factor beta-binding sites on betaglycan: functional separation of betaglycan co-receptor actions. J. Biol. Chem. 2006, 281:17011-17022.
107. Wiater E., Lewis K.A., Donaldson C., Vaughan J., Bilezikjian L., Vale W. Endogenous betaglycan is essential for high-potency inhibin antagonism in gonadotropes. Mol. Endocrinol. 2009, 23:1033-1042.
108. Wiater E., Vale W. Inhibin is an antagonist of bone morphogenetic protein signaling. J. Biol. Chem. 2003, 278:7934-7941.
109. Wu D.T., Bitzer M., Ju W., Mundel P., Bottinger E.P. TGF-b concentration specifies differential signaling profiles of growth arrest/differentiation and apoptosis in podocytes. J. Am. Soc. Nephrol. 2005, 16:3211-3221.
110. You H.J., Bruinsma M.W., How T., Ostrander J.H., Blobe G.C. The type III TGF-b receptor signals through both Smad3 and the p38 MAP kinase pathways to contribute to inhibition of cell proliferation. Carcinogenesis 2007, 28:2491-2500.
111. You H.J., How T., Blobe G.C. The type III transforming growth factor-b receptor negatively regulates nuclear factor kappa B signaling through its interaction with b-arrestin2. Carcinogenesis 2009, 30:1281-1287.
112. Zhu R., Zhou X., Chen Y., Qiu C., Xu W., Shen Z. Aberrantly increased mRNA expression of betaglycan, an inhibin co-receptor in the ovarian tissues in women with polycystic ovary syndrome. J. Obstet. Gynaecol. Res. 2009, 36:138-146.