Prevention of cachexia-like syndrome development and reduction of tumor progression in inhibin-deficient mice following administration of a chimeric activin receptor type II-murine Fc protein

Molecular Human Reproduction

Volumn 13, Issue 9, 2007, Pages 675-683

  Li, Qinglei ^a   Kumar, Ravi ^b   Underwood, Kathryn ^b   O'Connor, Anne E ^c   Loveland, Kate L ^c   Seehra, Jasbir S ^b   Matzuk, Martin M ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b Acceleron Pharma   (United States)

^c MONASH UNIVERSITY   (Australia)

Author keywords

Activin receptor type II; Cachexia; Inhibin; Tumor

Indexed keywords

ACTIVIN RECEPTOR 2; ACTIVIN RECEPTOR 2 ANTAGONIST; ANTINEOPLASTIC AGENT; FOLLITROPIN; IMMUNOGLOBULIN FC FRAGMENT; IMMUNOGLOBULIN G2A; INHIBIN; UNCLASSIFIED DRUG;

ANEMIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CACHEXIA; CANCER INHIBITION; CARCINOGENESIS; CONTROLLED STUDY; FEMALE; FOLLITROPIN BLOOD LEVEL; GONAD TUMOR; HISTOPATHOLOGY; IN VIVO STUDY; LIVER; MALE; MOUSE; NONHUMAN; OVARY TUMOR; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STOMACH; SURVIVAL RATE; SURVIVAL TIME; TESTIS TUMOR; TUMOR VOLUME; WEIGHT REDUCTION;

ACTIVIN RECEPTORS, TYPE II; ACTIVINS; ANIMALS; CACHEXIA; DISEASE PROGRESSION; FEMALE; FOLLICLE STIMULATING HORMONE; IMMUNOGLOBULIN FC FRAGMENTS; IMMUNOGLOBULIN G; INHIBINS; LIVER; MALE; MICE; MICE, KNOCKOUT; RECOMBINANT FUSION PROTEINS; SEX CORD-GONADAL STROMAL TUMORS; STOMACH; SYNDROME; TESTICULAR NEOPLASMS; WASTING SYNDROME;

MURINAE; MUS;

EID: 34548388339     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gam055     Document Type: Article

References (59)

1. Attisano L, Carcamo J, Ventura F, Weis FM, Massague J, Wrana JL. Identification ofhuman activin and TGF beta type I receptors that form heteromeric kinase complexes with type II receptors. Cell 1993; 75:671-680.
2. Beuschlein F, Looyenga BD, Bleasdale SE, Mutch C, Bavers DL, Parlow AF, Nilson JH, Hammer GD. Activin induces x-zone apoptosis that inhibits luteinizing hormone-dependent adrenocortical tumor formation in inhibin-deficient mice. Mol Cell Biol 2003;23:3951-3964.
3. Brown CW, Li L, Houston-Hawkins DE, Matzuk MM. Activins are critical modulators of growth and survival. Mol Endocrinol 2003;17 2404-2417.
4. Burdette JE, Jeruss JS, Kurley SJ, Lee EJ, Woodruff TK. Activin A mediates growth inhibition and cell cycle arrest through Smads in human breast cancer cells. Cancer Res 2005;65:7968-7975.
5. Burns KH, Agno JE, Sicinski P, Matzuk MM. Cyclin D2 and p27 are tissue-specific regulators of tumorigenesis in inhibin alpha knockout mice. Mol Endocrinol 2003a;17:2053-2069.
6. Burns KH, Agno JE, Chen L, Haupt B, Ogbonna SC, Korach KS, Matzuk MM. Sexually dimorphic roles of steroid hormone receptor signaling in gonadal tumorigenesis. Mol Endocrinol 2003b;17:2039-2052.
7. Chang H, Brown CW, Matzuk MM. Genetic analysis of the mammalian transforming growth factor-beta superfamily. Endocr Rev 2002;23 787-823.
8. Cipriano SC, Chen L, Kumar TR, Matzuk MM. Follistatin is a modulator of gonadal tumor progression and the activin-induced wasting syndrome in inhibin-deficient mice. Endocrinology 2000;141:2319-2327.
9. Cipriano SC, Chen L, Burns KH, Koff A, Matzuk MM. Inhibin and p27 interact to regulate gonadal tumorigenesis. Mol Endocrinol 2001; 15:985-996.
10. Clotman F, Lemaigre FP. Control of hepatic differentiation by activin/ TGFbeta signaling. Cell Cycle 2006;5:168-171.
11. Coerver KA, Woodruff TK, Finegold MJ, Mather J, Bradley A, Matzuk MM. Activin signaling through activin receptor type II causes the cachexia-like symptoms in inhibin-deficient mice. Mol Endocrinol 1996;10:534-543.
12. De Winter JP, De Vries CJ, Van Achterberg TA, Ameerun RF, Feijen A, Sugino H, De Waele P, Huylebroeck D, Verschueren K, Van Den Eijden-Van Raaij AJ. Truncated activin type II receptors inhibit bioactivity by the formation of heteromeric complexes with activin type I receptors. Exp Cell Res 1996;224:323-334.
13. Derynck R, Zhang YE. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 2003;425:577-584.
14. Donaldson CJ, Vaughan JM, Corrigan AZ, Fischer WH, Vale WW. Activin and inhibin binding to the soluble extracellular domain of activin receptor II. Endocrinology 1999;140:1760-1766.
15. Fang J, Yin W, Smiley E, Wang SQ, Bonadio J. Molecular cloning of the mouse activin beta E subunit gene. Biochem Biophys Res Commun 1996;228:669-674.
16. Fang J, Wang SQ, Smiley E, Bonadio J. Genes coding for mouse activin beta C and beta E are closely linked and exhibit a liver-specific expression pattern in adult tissues. Biochem Biophys Res Commun 1997;231:655-661.
17. Hemmati-Brivanlou A, Melton DA. A truncated activin receptor inhibits mesoderm induction and formation of axial structures in Xenopus embryos. Nature 1992;359:609-614.
18. Hully JR, Chang L, Schwall RH, Widmer HR, Terrell TG, Gillett NA. Induction of apoptosis in the murine liver with recombinant human activin A. Hepatology 1994;20:854-862.
19. Knight PG, Muttukrishna S, Groome NP. Development and application of a two-site enzyme immunoassay for the determination of 'total' activin-A concentrations in serum and follicular fluid. J Endocrinol 1996; 148:267-279.
20. Kumar TR, Wang Y, Matzuk MM. Gonadotropins are essential modifier factors for gonadal tumor development in inhibin-deficient mice. Endocrinology 1996;137:4210-4216.
21. Kumar TR, Palapattu G, Wang P, Woodruff TK, Boime I, Byrne MC, Matzuk MM. Transgenic models to study gonadotropin function: The role of follicle-stimulating hormone in gonadal growth and tumorigenesis. Mol Endocrinol 1999;13:851-865.
22. Lau AL, Nishimori K, Matzuk MM. Structural analysis of the mouse activin beta C gene. Biochim Biophys Acta 1996;1307:145-148.
23. Lau AL, Kumar TR, Nishimori K, Bonadio J, Matzuk MM. Activin betaC and betaE genes are not essential for mouse liver growth, differentiation, and regeneration. Mol Cell Biol 2000;20:6127-6137.
24. Li Q, Karam SM, Coerver KA, Matzuk MM, Gordon JI. Stimulation of activin receptor II signaling pathways inhibits differentiation of multiple gastric epithelial lineages. Mol Endocrinol 1998;12:181-192.
25. Li Q, Graff JM, O'Connor A E, Loveland KL, Matzuk MM. SMAD3 regulates gonadal tumorigenesis. Mol Endocrinol 2007; in press.
26. Mabuchi Y, Yamoto M, Minami S, Umesaki N. The autocrine effect of activin A on human ovarian clear cell adenocarcinoma cells. Oncol Rep 2006;16:373-379.
27. Massague J. Receptors for the TGF-beta family. Cell 1992;69 1067-1070.
28. Massague J. TGF-beta signal transduction. Annu Rev Biochem 1998; 67:753-791.
29. Massague J. How cells read TGF-beta signals. Nat Rev Mol Cell Biol 2000;1:169-178.
30. Mathews LS. Activin receptors and cellular signaling by the receptor serine kinase family. Endocr Rev 1994;15:310-325.
31. Mathews LS, Vale WW. Expression cloning of an activin receptor, a predicted transmembrane serine kinase. Cell 1991;65:973-982.
32. Matsuo SE, Leoni SG, Colquhoun A, Kimura ET. Transforming growth factor-beta1 and activin A generate antiproliferative signaling in thyroid cancer cells. J Endocrinol 2006;190:141-150.
33. Matzuk MM, Bradley A. Cloning of the human activin receptor cDNA reveals high evolutionary conservation. Biochim Biophys Acta 1992;1130 105-108.
34. Matzuk MM, Finegold MJ, Su JG, Hsueh AJ, Bradley A. Alpha-inhibin is a tumour-suppressor gene with gonadal specificity in mice. Nature 1992;360:313-319.
35. Matzuk MM, Finegold MJ, Mather JP, Krummen L, Lu H, Bradley A. Development of cancer cachexia-like syndrome and adrenal tumors in inhibin-deficient mice. Proc Natl Acad Sci USA 1994;91 8817-8821.
36. Matzuk MM, Kumar TR, Bradley A. Different phenotypes for mice deficient in either activins or activin receptor type II. Nature 1995a; 374:356-360.
37. Matzuk MM, Finegold MJ, Mishina Y, Bradley A, Behringer RR. Synergistic effects of inhibins and mullerian-inhibiting substance on testicular tumorigenesis. Mol Endocrinol 1995b;9:1337-1345.
38. Matzuk MM, Kumar TR, Vassalli A, Bickenbach JR, Roop DR, Jaenisch R, Bradley A. Functional analysis of activins during mammalian development. Nature 1995c;374:354-356.
39. Matzuk MM, Kumar TR, Shou W, Coerver KA, Lau AL, Behringer RR, Finegold MJ. Transgenic models to study the roles of inhibins and activins in reproduction, oncogenesis, and development. Recent Prog Horm Res 1996;51:123-154; discussion 155-127.
40. Mehra A, Wrana JL. TGF-beta and the Smad signal transduction pathway. Biochem Cell Biol 2002;80:605-622.
41. Mishina Y, Rey R, Finegold MJ, Matzuk MM, Josso N, Cate RL, Behringer RR. Genetic analysis of the Mullerian-inhibiting substance signal transduction pathway in mammalian sexual differentiation. Genes Dev 1996;10:2577-2587.
42. Moustakas A, Souchelnytskyi S, Heldin CH. Smad regulation in TGF-beta signal transduction. J Cell Sci 2001;114:4359-4369.
43. O'Connor AE, McFarlane JR, Hayward S, Yohkaichiya T, Groome NP, de Kretser DM. Serum activin A and follistatin concentrations during human pregnancy: A cross-sectional and longitudinal study. Hum Reprod 1999;14:827-832.
44. Oda S, Nishimatsu S, Murakami K, Ueno N. Molecular cloning and functional analysis of a new activin beta subunit: A dorsal mesoderm-inducing activity in Xenopus. Biochem Biophys Res Commun 1995;210:581-588.
45. Pangas SA, Woodruff TK. Activin signal transduction pathways. Trends Endocrinol Metab 2000;11:309-314.
46. Pangas SA, Rademaker AW, Fishman DA, Woodruff TK. Localization of the activin signal transduction components in normal human ovarian follicles: Implications for autocrine and paracrine signaling in the ovary. J Clin Endocrinol Metab 2002;87:2644-2657.
47. del Re E, Sidis Y, Fabrizio DA, Lin HY, Schneyer A. Reconstitution and analysis of soluble inhibin and activin receptor complexes in a cell-free system. J Biol Chem 2004;279:53126-53135.
48. Risbridger GP, Schmitt JF, Robertson DM. Activins and inhibins in endocrine and other tumors. Endocr Rev 2001;22:836-858.
49. Schmitt J, Hotten G, Jenkins NA, Gilbert DJ, Copeland NG, Pohl J, Schrewe H. Structure, chromosomal localization, and expression analysis of the mouse inhibin/activin beta C (Inhbc) gene. Genomics 1996; 32:358-366.
50. Schwall RH, Robbins K, Jardieu P, Chang L, Lai C, Terrell TG. Activin induces cell death in hepatocytes in vivo and in vitro. Hepatology 1993;18:347-356.
51. Shikone T, Matzuk MM, Perlas E, Finegold MJ, Lewis KA, Vale W, Bradley A, Hsueh AJ. Characterization of gonadal sex cord-stromal tumor cell lines from inhibin-alpha and p53-deficient mice: The role of activin as an autocrine growth factor. Mol Endocrinol 1994;8:983-995.
52. Shou W, Woodruff TY, Matzuk MM. Role of androgens in testicular tumor development in inhibin-deficient mice. Endocrinology 1997;138 5000-5005.
53. Smith JC, Price BM, Van Nimmen K, Huylebroeck D. Identification of a potent Xenopus mesoderm-inducing factor as a homologue of activin A. Nature 1990;345:729-731.
54. Trudeau VL, Matzuk MM, Hache RJ, Renaud LP. Overexpression of activin-beta A subunit mRNA is associated with decreased activin type II receptor mRNA levels in the testes of alpha-inhibin deficient mice. Biochem Biophys Res Commun 1994;203:105-112.
55. Wang QF, Tilly KI, Tilly JL, Preffer F, Schneyer AL, Crowley WF, Jr, Sluss PM. Activin inhibits basal and androgen-stimulated proliferation and induces apoptosis in the human prostatic cancer cell line, LNCaP. Endocrinology 1996;137:5476-5483.
56. Wittbrodt J, Rosa FM. Disruption of mesoderm and axis formation in fish by ectopic expression of activin variants: The role of maternal activin. Genes Dev 1994;8:1448-1462.
57. Wu TC, Jih MH, Wang L, Wan YJ. Expression of activin receptor II and IIB mRNA isoforms in mouse reproductive organs and oocytes. Mol Reprod Dev 1994;38:9-15.
58. Xu J, McKeehan K, Matsuzaki K, McKeehan WL. Inhibin antagonizes inhibition of liver cell growth by activin by a dominant-negative mechanism. J Biol Chem 1995;270:6308-6313.
59. Yasuda H, Mine T, Shibata H, Eto Y, Hasegawa Y, Takeuchi T, Asano S, Kojima I. Activin A: An autocrine inhibitor of initiation of DNA synthesis in rat hepatocytes. J Clin Invest 1993;92 1491-1496.