Neuroendocrine control of female reproductive function by the activin receptor ALK7

FASEB Journal

Volumn 26, Issue 12, 2012, Pages 4966-4976

  Sandoval Guzmań, Tatiana ^a,b   Göngrich, Christina ^a   Moliner, Annalena ^a   Guo, Tingqing ^a   Wu, Haiya ^a   Broberger, Christian ^a   Ibáñez, Carlos F ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

Author keywords

Hypothalamus; NPY; Ovary; PCOS; Pituitary

Indexed keywords

ACTIVIN RECEPTOR LIKE KINASE 7; FOLLITROPIN; GONADOTROPIN; LUTEINIZING HORMONE; MESSENGER RNA; NEUROPEPTIDE Y; PROTEIN SERINE THREONINE KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; CELL DEGENERATION; CONTROLLED STUDY; ESTRUS CYCLE; FEMALE; FEMALE GENITAL SYSTEM; FOLLITROPIN BLOOD LEVEL; GENE EXPRESSION; GONADOTROPIN SECRETING CELL; GRANULOSA CELL; HYPOPHYSIS; HYPOTHALAMUS; LUTEINIZING HORMONE BLOOD LEVEL; MOUSE; NERVE CELL; NEUROENDOCRINE SYSTEM; NONHUMAN; OOCYTE; OVARY; OVARY FOLLICLE; OVARY POLYCYSTIC DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUBERTY; REPRODUCTION; WILD TYPE;

ACTIVIN RECEPTORS, TYPE I; ANIMALS; ESTROUS CYCLE; FEMALE; FOLLICLE STIMULATING HORMONE; GENE EXPRESSION; GREEN FLUORESCENT PROTEINS; IMMUNOHISTOCHEMISTRY; LUTEINIZING HORMONE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NEURONS; NEUROPEPTIDE Y; NEUROSECRETORY SYSTEMS; OVARY; PITUITARY GLAND; REPRODUCTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEXUAL MATURATION; SIGNAL TRANSDUCTION; TISSUE CULTURE TECHNIQUES;

MUS;

EID: 84870337660     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-199059     Document Type: Article

References (62)

1. Matsuo, H., Baba, Y., Nair, R. M., Arimura, A., and Schally, A. V. (1971) Structure of the porcine LH- and FSH-releasing hormone. I. The proposed amino acid sequence. Biochem. Biophys. Res. Commun. 43, 1334-1339
2. Vale, W., Rivier, C., Hsueh, A., Campen, C., Meunier, H., Bicsak, T., Vaughan, J., Corrigan, A. Z., Bardin, W., and Sawchenko, P. (1988) Chemical and biological characterization of the inhibin family of protein hormones. Recent Progr. Hormone Res. 44, 1-34
3. Bilezikjian, L. M. (1993) Activin-A regulates follistatin secretion from cultured rat anterior pituitary cells. Endocrinology 133, 2554-2560
4. Furuta, C., Arakawa, S., Shi, Z., Watanabe, G., and Taya, K. (2008) Placental activin A is required for follicular development during the second half of pregnancy in the golden hamster (Mesocricetus auratus). Endocrine 33, 126-134
5. Plotsky, P. M., Kjaer, A., Sutton, S. W., Sawchenko, P. E., and Vale, W. (1991) Central activin administration modulates corticotropin-releasing hormone and adrenocorticotropin secretion. Endocrinology 128, 2520-2525
6. Vassalli, A., Matzuk, M. M., Gardner, H. A., Lee, K.-F., and Jaenisch, R. (1994) Activin/inhibin beta B subunit gene disruption leads to defects in eyelid development and female reproduction. Genes Dev. 8, 414-427
7. Calogero, A. E., Burrello, N., Ossino, A. M., Polosa, P., and D'Agata, R. (1998) Activin-A stimulates hypothalamic gonadotropin-releasing hormone release by the explanted male rat hypothalamus: interaction with inhibin and androgens. J. Endocrinol. 156, 269-274 (Pubitemid 28105815)
8. González-Manchón, C., Bilezikjian, L. M., Corrigan, A. Z., Mellon, P. L., and Vale, W. (1991) Activin-A modulates gonadotropin-releasing hormone secretion from a gonadotropin-releasing hormone-secreting neuronal cell line. Neuroendocrinology 54, 373-377
9. Weng, Q., Wang, H. S. M. edan, M., Jin, W., Xia, G., Watanabe, G., and Taya, K. (2006) Expression of inhibin/activin subunits in the ovaries of fetal and neonatal mice. J. Reprod. Dev. 52, 607-616 (Pubitemid 44706383)
10. Wilson, M. E., and Handa, R. J. (1998) Activin subunit, follistatin, and activin receptor gene expression in the prepubertal female rat pituitary. Biol. Reprod. 59, 278-283 (Pubitemid 28354865)
11. Rydén, M., Imamura, T., Jörnvall, H., Belluardo, N., Neveu, I., Trupp, M., Okadome, T., Dijke, ten, P., and Ibanez, C. F. (1996) A novel type I receptor serine-threonine kinase predominantly expressed in the adult central nervous system. J. Biol. Chem. 271, 30603-30609 (Pubitemid 26404073)
12. Shi, Y., and Massagué, J. (2003) Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 113, 685-700 (Pubitemid 36724933)
13. Derynck, R., Akhurst, R. J., and Balmain, A. (2001) TGF-β signaling in tumor suppression and cancer progression. Nat. Genet. 29, 117-129
14. ten Dijke, P., Miyazono, K., and Heldin, C.-H. (2000) Signaling inputs converge on nuclear effectors in TGF-β signaling. Trends Biochem. Sci. 25, 64-70
15. Attisano, L., Cárcamo, J., Ventura, F., Weis, F. M., Massagué, J., and Wrana, J. L. (1993) Identification of human activin and TGF-β type I receptors that form heteromeric kinase complexes with type II receptors. Cell 75, 671-680 (Pubitemid 23346366)
16. Gu, Z., Nomura, M., Simpson, B. B., Lei, H., Feijen, A., van den Eijnden-van Raaij, A., Donahoe, P. K., and Li, E. (1998) The type I activin receptor ActRIB is required for egg cylinder organization and gastrulation in the mouse. Genes Dev. 12, 844-857 (Pubitemid 28150885)
17. Tsuchida, K., Nakatani, M., Yamakawa, N., Hashimoto, O., Hasegawa, Y., and Sugino, H. (2004) Activin isoforms signal through type I receptor serine/threonine kinase ALK7. Mol. Cell. Endocrinol. 220, 59-65 (Pubitemid 38757881)
18. Andersson, O., Bertolino, P., and Ibanez, C. F. (2007) Distinct and cooperative roles of mammalian Vg1 homologs GDF1 and GDF3 during early embryonic development. Dev. Biol. 311, 500-511 (Pubitemid 350046540)
19. Andersson, O., Reissmann, E., and Ibanez, C. F. (2006) Growth differentiation factor 11 signals through the transforming growth factor-β receptor ALK5 to regionalize the anterior-posterior axis. EMBO Rep. 7, 831-837 (Pubitemid 44275403)
20. Andersson, O., Reissmann, E., Jörnvall, H., and Ibanez, C. F. (2006) Synergistic interaction between Gdf1 and Nodal during anterior axis development. Dev. Biol. 293, 370-381
21. Andersson, O., Korach-Andre, M., Reissmann, E., Ibanez, C. F., and Bertolino, P. (2008) Growth/differentiation factor 3 signals through ALK7 and regulates accumulation of adipose tissue and diet-induced obesity. Proc. Natl. Acad. Sci. U. S. A. 105, 7252-7256 (Pubitemid 351754464)
22. Bertolino, P., Holmberg, R., Reissmann, E., Andersson, O., Berggren, P.-O., and Ibanez, C. F. (2008) Activin B receptor ALK7 is a negative regulator of pancreatic beta-cell function. Proc. Natl. Acad. Sci. U. S. A. 105, 7246-7251 (Pubitemid 351754463)
23. Reissmann, E., Jörnvall, H., Blokzijl, A., Andersson, O., Chang, C., Minchiotti, G., Persico, M. G., Ibanez, C. F., and Hemmati-Brivanlou, A. H. (2001) The orphan receptor ALK7 and the activin receptor ALK4 mediate signaling by Nodal proteins during vertebrate development. Genes Dev. 15, 2010-2022 (Pubitemid 32738629)
24. Jörnvall, H., Reissmann, E., Andersson, O., Mehrkash, M., and Ibanez, C. F. (2004) ALK7, a receptor for nodal, is dispensable for embryogenesis and left-right patterning in the mouse. Mol. Cell. Biol. 24, 9383-9389 (Pubitemid 39391676)
25. Gong, S., Zheng, C., Doughty, M. L., Losos, K., Didkovsky, N., Schambra, U. B., Nowak, N. J., Joyner, A., Leblanc, G., Hatten, M. E., and Heintz, N. (2003) A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425, 917-925 (Pubitemid 37376918)
26. Goldman, J. M., Murr, A. S., and Cooper, R. L. (2007) The rodent estrous cycle: characterization of vaginal cytology and its utility in toxicological studies. Birth Defects Res. B Dev.Reprod. Toxicol. 80, 84-97 (Pubitemid 46762318)
27. Peters, H. (1969) The development of the mouse ovary from birth to maturity. Acta Endocrinol. 62, 98-116
28. Paxinos, G., and Franklin, K. B. J. (2004) The Mouse Brain in Stereotaxic Coordinates, 2nd Ed., Gulf Publishing, Houston, TX, USA
29. Broberger, C., Johansen, J., Johansson, C., Schalling, M., and Hökfelt, T. (1998) The neuropeptide Y/agouti gene-related protein (AGRP) brain circuitry in normal, anorectic, and monosodium glutamate-treated mice. Proc. Natl. Acad. Sci. U. S. A. 95, 15043-15048 (Pubitemid 29003753)
30. Bondestam, J., Huotari, M. A., Morén, A., Ustinov, J., Kaivo-Oja, N., Kallio, J., Horelli-Kuitunen, N., Aaltonen, J., Fujii, M., Moustakas, A., ten Dijke, P., Otonkoski, T., and Ritvos, O. (2001) cDNA cloning, expression studies and chromosome mapping of human type I serine/threonine kinase receptor ALK7 (ACVR1C). Cytogenet. Cell Genet. 95, 157-162 (Pubitemid 34638952)
31. Lorentzon, M., Hoffer, B. J., Ebendal, T., Olson, L., and Tomac, A. C. (1996) Habrec1, a novel serine/threonine kinase TGF-β type I-like receptor, has a specific cellular expression suggesting function in the developing organism and adult brain. Exp. Neurol. 142, 351-360 (Pubitemid 26414067)
32. Bernard, D. J., Lee, K. B., and Santos, M. M. (2006) Activin B can signal through both ALK4 and ALK7 in gonadotrope cells. Reprod. Biol. Endocrinol. 4, 52
33. Nakane, P. K. (1970) Classifications of anterior pituitary cell types with immunoenzyme histochemistry. 18, 9-20
34. Kumar, T. R., Wang, Y., Lu, N., and Matzuk, M. M. (1997) Follicle-stimulating hormone is required for ovarian follicle maturation but not male fertility. Nat. Genet. 15, 201-204 (Pubitemid 27061644)
35. Crowley, W. R., and Kalra, S. P. (1987) Neuropeptide Y stimulates the release of luteinizing hormone-releasing hormone from medial basal hypothalamus in vitro: modulation by ovarian hormones. Neuroendocrinology 46, 97-103 (Pubitemid 17106405)
36. Urban, J. H., Das, I., and Levine, J. E. (1996) Steroid modulation of neuropeptide Y-induced luteinizing hormone releasing hormone release from median eminence fragments from male rats. Neuroendocrinology 63, 112-119 (Pubitemid 26049622)
37. Woller, M. J., and Terasawa, E. (1991) Infusion of neuropeptide Y into the stalk-median eminence stimulates in vivo release of luteinizing hormone-release hormone in gonadectomized rhesus monkeys. Endocrinology 128, 1144-1150
38. Bristol-Gould, S. K., Kreeger, P. K., Selkirk, C. G., Kilen, S. M., Cook, R. W., Kipp, J. L., Shea, L. D., Mayo, K. E., and Woodruff, T. K. (2006) Postnatal regulation of germ cells by activin: the establishment of the initial follicle pool. Dev. Biol. 298, 132-148 (Pubitemid 44414802)
39. Knight, P. G., and Glister, C. (2006) TGF-β superfamily members and ovarian follicle development. Reproduction 132, 191-206 (Pubitemid 44274724)
40. Pangas, S. A., Jorgez, C. J., Tran, M., Agno, J., Li, X., Brown, C. W., Kumar, T. R., and Matzuk, M. M. (2007) Intraovarian activins are required for female fertility. Mol. Endocrinol. 21, 2458-2471 (Pubitemid 47529358)
41. Murata, T., Takizawa, T., Funaba, M., Fujimura, H., Murata, E., Takahashi, M., and Torii, K. (1997) Quantitative RT-PCR for inhibin/activin subunits: measurements of rat hypothalamic and ovarian inhibin/activin subunit mRNAs during the estrous cycle. Endocrine J. 44, 35-42 (Pubitemid 27150158)
42. Xu, G., Zhong, Y., Munir, S., Yang, B. B., Tsang, B. K., and Peng, C. (2004) Nodal induces apoptosis and inhibits proliferation in human epithelial ovarian cancer cells via activin receptor-like kinase 7. J. Clin. Endocrinol. Metab. 89, 5523-5534 (Pubitemid 39518436)
43. Wang, H., Jiang, J.-Y., Zhu, C., Peng, C., and Tsang, B. K. (2006) Role and regulation of nodal/activin receptor-like kinase 7 signaling pathway in the control of ovarian follicular atresia. Mol. Endocrinol. 20, 2469-2482 (Pubitemid 44496415)
44. Cho, B. N., McMullen, M. L., Pei, L., Yates, C. J., and Mayo, K. E. (2001) Reproductive deficiencies in transgenic mice expressing the rat inhibin alpha-subunit gene. Endocrinology 142, 4994-5004 (Pubitemid 33022376)
45. Burger, L. L., Haisenleder, D. J., Wotton, G. M., Aylor, K. W., Dalkin, A. C., and Marshall, J. C. (2007) The regulation of FSHβ transcription by gonadal steroids: testosterone and estradiol modulation of the activin intracellular signaling pathway. Am. J. Physiol. Endocrinol. Metab. 293, E277-E285 (Pubitemid 47105942)
46. Hoggard, N., Cruickshank, M., Moar, K. M., Barrett, P., Bashir, S., and Miller, J. D. B. (2009) Inhibin βB expression in murine adipose tissue and its regulation by leptin, insulin and dexamethasone. J. Mol. Endocrinol. 43, 171-177
47. McGinnis, M. Y., Williams, G. W., and Lumia, A. R. (1996) Inhibition of male sex behavior by androgen receptor blockade in preoptic area or hypothalamus, but not amygdala or septum. Physiol. Behav. 60, 783-789 (Pubitemid 26284277)
48. Thackray, V. G., and Mellon, P. L. (2008) Synergistic induction of follicle-stimulating hormone β-subunit gene expression by gonadal steroid hormone receptors and Smad proteins. Endocrinology 149, 1091-1102 (Pubitemid 351397962)
49. Schwartz, M. W., Marks, J. L., Sipols, A. J., Baskin, D. G., Woods, S. C., Kahn, S. E., and Porte, D. (1991) Central insulin administration reduces neuropeptide Y mRNA expression in the arcuate nucleus of food-deprived lean (Fa/Fa) but not obese (fa/fa) Zucker rats. Endocrinology 128, 2645-2647
50. Campbell, R. E., Ffrench-Mullen, J. M., Cowley, M. A., Smith, M. S., and Grove, K. L. (2001) Hypothalamic circuitry of neuropeptide Y regulation of neuroendocrine function and food intake via the Y5 receptor subtype. Neuroendocrinology 74, 106-119 (Pubitemid 32727577)
51. Li, C., Chen, P., and Smith, M. S. (1999) Morphological evidence for direct interaction between arcuate nucleus neuropeptide Y (NPY) neurons and gonadotropin-releasing hormone neurons and the possible involvement of NPY Y1 receptors. Endocrinology 140, 5382-5390
52. Turi, G. F., Liposits, Z., Moenter, S. M., Fekete, C., and Hrabovszky, E. (2003) Origin of neuropeptide Y-containing afferents to gonadotropin-releasing hormone neurons in male mice. Endocrinology 144, 4967-4974 (Pubitemid 37378411)
53. Crowley, W. R., Hassid, A., and Kalra, S. P. (1987) Neuropeptide Y enhances the release of luteinizing hormone (LH) induced by LH-releasing hormone. Endocrinology 120, 941-945 (Pubitemid 17016736)
54. Broberger, C., de Lecea, L., Sutcliffe, J. G., and Hökfelt, T. (1998) Hypocretin/orexin- and melanin-concentrating hormone-expressing cells form distinct populations in the rodent lateral hypothalamus: relationship to the neuropeptide Y and agouti gene-related protein systems. J. Comp. Neurol. 402, 460-474 (Pubitemid 29001075)
55. Hahn, T. M., Breininger, J. F., Baskin, D. G., and Schwartz, M. W. (1998) Coexpression of Agrp and NPY in fasting-activated hypothalamic neurons. Nat. Neurosci. 1, 271-272 (Pubitemid 128652670)
56. Li, S., Hong, M., Fournier, A., St-Pierre, S., and Pelletier, G. (1994) Role of neuropeptide Y in the regulation of gonadotropin-releasing hormone gene expression in the rat preoptic area. Brain Res. Mol. Brain Res. 26, 69-73 (Pubitemid 24311025)
57. Xu, M., Hill, J. W., and Levine, J. E. (2000) Attenuation of luteinizing hormone surges in neuropeptide Y knockout mice. Neuroendocrinology 72, 263-271 (Pubitemid 32008828)
58. Bai, F. L., Yamano, M., Shiotani, Y., Emson, P. C., Smith, A. D., Powell, J. F., and Tohyama, M. (1985) An arcuato-paraventricular and -dorsomedial hypothalamic neuropeptide Y-containing system which lacks noradrenaline in the rat. Brain Res. 331, 172-175 (Pubitemid 15115377)
59. Shoji-Kasai, Y., Ageta, H., Hasegawa, Y., Tsuchida, K., Sugino, H., and Inokuchi, K. (2007) Activin increases the number of synaptic contacts and the length of dendritic spine necks by modulating spinal actin dynamics. J. Cell Sci. 120, 3830-3837 (Pubitemid 350187364)
60. Kupershmidt, L., Amit, T., Bar-Am, O., Youdim, M. B. H., and Blumenfeld, Z. (2007) The neuroprotective effect of activin A and B: implication for neurodegenerative diseases. J. Neurochem. 103, 962-971 (Pubitemid 47568714)
61. Goodarzi, M. O., Dumesic, D. A., Chazenbalk, G., and Azziz, R. (2011) Polycystic ovary syndrome: etiology, pathogenesis and diagnosis. Nat. Rev. Endocrinol. 7, 219-231
62. Ewens, K. G., Stewart, D. R., Ankener, W., Urbanek, M., McAllister, J. M., Chen, C., Baig, K. M., Parker, S. C. J., Margulies, E. H., Legro, R. S., Dunaif, A., Strauss, J. F., and Spielman, R. S. (2010) Family-based analysis of candidate genes for polycystic ovary syndrome. J. Clin. Endocrinol. Metab. 95, 2306-2315