Extragonadal LH/hCG action-Not yet time to rewrite textbooks

Molecular and Cellular Endocrinology

Volumn 269, Issue 1-2 SPEC. ISS., 2007, Pages 9-16

  Pakarainen, Tomi ^a   Ahtiainen, Petteri ^a   Zhang, Fu Ping ^b   Rulli, Susana ^c   Poutanen, Matti ^a   Huhtaniemi, Ilpo ^a,d  

^a UNIVERSITY OF TURKU   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Extragonadal LH hCG action; Gonadal function; Human chorionic gonadotropin (hCG); Knockout mouse; LH hCG receptor (R); Luteinizing hormone (LH); Ovary; Testis; Transgenic mouse

Indexed keywords

CHORIONIC GONADOTROPIN; LUTEINIZING HORMONE;

DNA MODIFICATION; GAMETOGENESIS; GENE DISRUPTION; GENE FUNCTION; GENE TARGETING; GONAD FUNCTION; MOLECULAR MODEL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SEX RATIO;

ANIMALS; BONE AND BONES; FEMALE; GONADOTROPINS; GONADS; HUMANS; MICE; MICE, TRANSGENIC; OVARY;

EID: 33947676416     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2006.10.019     Document Type: Review

References (72)

1. Abdallah M.A., Lei Z.M., Li X., Greenwold N., Nakajima S.T., Jauniaux E., and Rao Ch.V. Human fetal nongonadal tissues contain human chorionic gonadotropin/luteinizing hormone receptors. J. Clin. Endocrinol. Metab. 89 (2004) 952-956
2. Ahtiainen P., Rulli S.B., Shariatmadari R., Pelliniemi L.J., Toppari J., Poutanen M., and Huhtaniemi I.T. Fetal but not adult Leydig cells are susceptible to adenoma formation in response to persistently high hCG level: a study on hCG overexpressing transgenic mice. Oncogene 24 (2005) 7301-7309
3. Apaja P.M., Aatsinki J.T., Rajaniemi H.J., and Petäjä-Repo U.E. Expression of the mature luteinizing hormone receptor in rodent urogenital and adrenal tissues is developmentally regulated at a posttranslational level. Endocrinology 146 (2005) 3224-3232
4. Apaja P.M., Harju K.T., Aatsinki J.T., Petaja-Repo U.E., and Rajaniemi H.J. Identification and structural characterization of the neuronal luteinizing hormone receptor associated with sensory systems. J. Biol. Chem. 279 (2004) 1899-1906
5. Ascoli M., Fanelli F., and Segaloff D.L. The lutropin/choriogonadotropin receptor, a 2002 perspective. Endocr. Rev. 23 (2002) 141-174
6. Chudgar D., Lei Z., and Rao Ch.V. Orthotopic transplantation of LH receptor knockout and wild-type ovaries. Life Sci. 77 (2005) 2656-2662
7. Dufau M.L. The luteinizing hormone receptor. Annu. Rev. Physiol. 60 (1998) 461-496
8. Eblen A., Bao S., Lei Z.M., Nakajima S.T., and Rao C.V. The presence of functional luteinizing hormone/chorionic gonadotropin receptors in human sperm. J. Clin. Endocrinol. Metab. 86 (2001) 2643-2648
9. El-Gehani F., Zhang F.P., Pakarinen P., Rannikko A., and Huhtaniemi I. Gonadotropin-independent regulation of steroidogenesis in the fetal rat testis. Biol. Reprod. 58 (1998) 116-123
10. Fields M.J., and Shemesh M. Extragonadal luteinizing hormone receptors in the reproductive tract of domestic animals. Biol. Reprod. 71 (2004) 1412-1418
11. Filicori M., Fazleabas A.T., Huhtaniemi I., Licht P., Rao Ch.V., Tesarik J., and Zygmunt M. Novel concepts of human chorionic gonadotropin: reproductive system interactions and potential in the management of infertility. Fertil. Steril. 84 (2005) 275-284
12. Gougeon A. Regulation of ovarian follicular development in primates: facts and hypotheses. Endocr. Rev. 17 (1996) 121-155
13. Han S.W., Lei Z.M., and Rao C.V. Up-regulation of cyclooxygenase-2 gene expression by chorionic gonadotropin in mucosal cells from human fallopian tubes. Endocrinology 137 (1996) 2929-2937
14. Han S.W., Lei Z.M., and Rao C.V. Homologous down-regulation of luteinizing hormone/chorionic gonadotropin receptors by increasing the degradation of receptor transcripts in human uterine endometrial stromal cells. Biol. Reprod. 57 (1997) 158-164
15. Han S.W., Lei Z.M., and Rao C.V. Treatment of human endometrial stromal cells with chorionic gonadotropin promotes their morphological and functional differentiation into decidua. Mol. Cell. Endocrinol. 147 (1999) 7-16
16. Hickey G.J., Chen S.A., Besman M.J., Shively J.E., Hall P.F., Gaddy-Kurten D., and Richards J.S. Hormonal regulation, tissue distribution, and content of aromatase cytochrome P450 messenger ribonucleic acid and enzyme in rat ovarian follicles and corpora lutea: relationship to estradiol biosynthesis. Endocrinology 122 (1988) 1426-1436
17. Huhtaniemi I. Fetal testis-a very special endocrine organ. Eur. J. Endocrinol. 130 (1994) 25-31
18. Huhtaniemi I., and Pelliniemi L.J. Fetal Leydig cells: cellular origin, morphology, life span, and special functional features. Proc. Soc. Exp. Biol. Med. 201 (1992) 125-140
19. Huhtaniemi I.T., and Themmen A.P. Mutations in human gonadotropin and gonadotropin-receptor genes. Endocrine 26 (2005) 207-217
20. Huhtaniemi I.T., Korenbrot C.C., and Jaffe R.B. HCG binding and stimulation of testosterone biosynthesis in the human fetal testis. J. Clin. Endocrinol. Metab. 44 (1977) 963-967
21. Keri R.A., Lozada K.L., Abdul-Karim F.W., Nadeau J.H., and Nilson J.H. Luteinizing hormone induction of ovarian tumors: oligogenic differences between mouse strains dictates tumor disposition. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 383-387
22. Kero J.T., Savontaus E., Mikola M., Pesonen U., Koulu M., Keri R.A., Nilson J.H., Poutanen M., and Huhtaniemi I.T. Obesity in transgenic female mice with constitutively elevated luteinizing hormone secretion. Am. J. Physiol. Endocrinol. Metab. 285 (2003) E812-E818
23. Lavebratt C., Petersson S., Iwarsson K., Schalling M., and Ährlund-Richter L. Ovary transplantation method resulting in high reproductive performance in mice. Scand. J. Lab. Anim. Sci. 25 (1998) 53-58
24. Lei Z.M., Reshef E., and Rao V. The expression of human chorionic gonadotropin/luteinizing hormone receptors in human endometrial and myometrial blood vessels. J. Clin. Endocrinol. Metab. 75 (1992) 651-659
25. Lei Z.M., Toth P., Rao C.V., and Pridham D. Novel coexpression of human chorionic gonadotropin (hCG)/human luteinizing hormone receptors and their ligand hCG in human fallopian tubes. J. Clin. Endocrinol. Metab. 77 (1993) 863-872
26. Lei Z.M., Rao C.V., Kornyei J.L., Licht P., and Hiatt E.S. Novel expression of human chorionic gonadotropin/luteinizing hormone receptor gene in brain. Endocrinology 132 (1993) 2262-2270
27. Lei Z.M., Mishra S., Zou W., Xu B., Foltz M., Li X., and Rao C.V. Targeted disruption of luteinizing hormone/human chorionic gonadotropin receptor gene. Mol. Endocrinol. 15 (2001) 184-200
28. Lin J., Lojun S., Lei Z.M., Wu W.X., Peiner S.C., and Rao C.V. Lymphocytes from pregnant women express human chorionic gonadotropin/luteinizing hormone receptor gene. Mol. Cell. Endocrinol. 111 (1995) R13-R17
29. Lin P.C., Li X., Lei Z.M., and Rao C.V. Human cervix contains functional luteinizing hormone/human chorionic gonadotropin receptors. J. Clin. Endocrinol. Metab. 88 (2003) 3409-3414
30. Ma X., Dong Y., Matzuk M.M., and Kumar T.R. Targeted disruption of luteinizing hormone beta-subunit leads to hypogonadism, defects in gonadal steroidogenesis, and infertility. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 17294-17299
31. Mann R.J., Keri R.A., and Nilson J.H. Consequences of elevated luteinizing hormone on diverse physiological systems: use of the LHbetaCTP transgenic mouse as a model of ovarian hyperstimulation-induced pathophysiology. Recent Prog. Horm. Res. 58 (2003) 343-375
32. Markkula M., Hamalainen T., Loune E., and Huhtaniemi I. The follicle-stimulating hormone (FSH) beta- and common alpha-subunits are expressed in mouse testis, as determined in wild-type mice and those transgenic for the FSH beta-subunit/herpes simplex virus thymidine kinase fusion gene. Endocrinology 136 (1995) 4769-4775
33. Markkula M., Kananen K., Klemi P., and Huhtaniemi I. Pituitary and ovarian expression of the endogenous follicle-stimulating hormone (FSH) subunit genes and an FSH beta-subunit promoter-driven herpes simplex virus thymidine kinase gene in transgenic mice; specific partial ablation of FSH-producing cells by antiherpes treatment. J. Endocrinol. 150 (1996) 265-273
34. Matzuk M.M., DeMayo F.J., Hadsell L.A., and Kumar T.R. Overexpression of human chorionic gonadotropin causes multiple reproductive defects in transgenic mice. Biol. Reprod. 69 (2003) 338-346
35. McFarland K.C., Sprengel R., Phillips H.S., Kohler M., Rosemblit N., Nikolics K., Segaloff D.L., and Seeburg P.H. Lutropin-choriogonadotropin receptor: an unusual member of the G protein-coupled receptor family. Science 245 (1989) 494-499
36. Mizrachi D., and Shemesh M. Follicle-stimulating hormone receptor and its messenger ribonucleic acid are present in the bovine cervix and can regulate cervical prostanoid synthesis. Biol. Reprod. 61 (1999) 776-784
37. Mohammad H.P., Abbud R.A., Parlow A.F., Lewin J.S., and Nilson J.H. Targeted overexpression of luteinizing hormone causes ovary-dependent functional adenomas restricted to cells of the Pit-1 lineage. Endocrinology 144 (2003) 4626-4636
38. Pabon J.E., Li X., Lei Z.M., Sanfilippo J.S., Yussman M.A., and Rao C.V. Novel presence of luteinizing hormone/chorionic gonadotropin receptors in human adrenal glands. J. Clin. Endocrinol. Metab. 81 (1996) 2397-2400
39. Pabon J.E., Bird J.S., Li X., Huang Z.H., Lei Z.M., Sanfilippo J.S., Yussman M.A., and Rao C.V. Human skin contains luteinizing hormone/chorionic gonadotropin receptors. J. Clin. Endocrinol. Metab. 81 (1996) 2738-2741
40. Pakarainen T., Zhang F.P., Poutanen M., and Huhtaniemi I. Fertility in luteinizing hormone receptor-knockout mice after wild-type ovary transplantation demonstrates redundancy of extragonadal luteinizing hormone action. J. Clin. Invest. 115 (2005) 1862-1868
41. Pakarainen T., Zhang F.P., Nurmi L., Poutanen M., and Huhtaniemi I. Knockout of luteinizing hormone receptor abolishes the effects of follicle-stimulating hormone on preovulatory maturation and ovulation of mouse graafian follicles. Mol. Endocrinol. 19 (2005) 2591-2602
42. Pakarainen T., Zhang F.P., Makela S., Poutanen M., and Huhtaniemi I. Testosterone replacement therapy induces spermatogenesis and partially restores fertility in luteinizing hormone receptor knockout mice. Endocrinology 146 (2005) 596-606
43. Pakarinen P., Kimura S., El-Gehani F., Pelliniemi L.J., and Huhtaniemi I. Pituitary hormones are not required for sexual differentiation of male mice: phenotype of the T/ebp/Nkx2.1 null mutant mice. Endocrinology 143 (2002) 4477-4482
44. Raga F., Casan E.M., Kruessel J.S., Wen Y., Huang H.Y., Nezhat C., and Polan M.L. Quantitative gonadotropin-releasing hormone gene expression and immunohistochemical localization in human endometrium throughout the menstrual cycle. Biol. Reprod. 59 (1998) 661-669
45. Rao C.V., Li X., Toth P., Lei Z.M., and Cook V.D. Novel expression of functional human chorionic gonadotropin/luteinizing hormone receptor gene in human umbilical cords. J. Clin. Endocrinol. Metab. 77 (1993) 1706-1714
46. Rao C.V. Multiple novel roles of luteinizing hormone. Fertil. Steril. 76 (2001) 1097-1100
47. Rao S.C., Li X., Rao Ch.V., and Magnuson D.S. Human chorionic gonadotropin/luteinizing hormone receptor expression in the adult rat spinal cord. Neurosci. Lett. 336 (2003) 135-138
48. Rao C.V., and Lei Z.M. Consequences of targeted inactivation of LH receptors. Mol. Cell. Endocrinol. 187 (2002) 57-67
49. Reiter E., McNamara M., Closset J., and Hennen G. Expression and functionality of luteinizing hormone/chorionic gonadotropin receptor in the rat prostate. Endocrinology 136 (1995) 917-923
50. Reshef E., Lei Z.M., Rao C.V., Pridham D.D., Chegini N., and Luborsky J.L. The presence of gonadotropin receptors in nonpregnant human uterus, human placenta, fetal membranes, and decidua. J. Clin. Endocrinol. Metab. 70 (1990) 421-430
51. Richards J.S. Hormonal control of gene expression in the ovary. Endocr. Rev. 15 (1994) 725-751
52. Risma K.A., Clay C.M., Nett T.M., Wagner T., Yun J., and Nilson J.H. Targeted overexpression of luteinizing hormone in transgenic mice leads to infertility, polycystic ovaries, and ovarian tumors. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 1322-1326
53. Rulli S.B., Kuorelahti A., Karaer O., Pelliniemi L.J., Poutanen M., and Huhtaniemi I. Reproductive disturbances, pituitary lactotrope adenomas, and mammary gland tumors in transgenic female mice producing high levels of human chorionic gonadotropin. Endocrinology 143 (2002) 4084-4095
54. Rulli S.B., Ahtiainen P., Makela S., Toppari J., Poutanen M., and Huhtaniemi I. Elevated steroidogenesis, defective reproductive organs, and infertility in transgenic male mice overexpressing human chorionic gonadotropin. Endocrinology 144 (2003) 4980-4990
55. Schorpp M., Jager R., Schellander K., Schenkel J., Wagner E.F., Weiher H., and Angel P. The human ubiquitin C promoter directs high ubiquitous expression of transgenes in mice. Nucleic Acids Res. 24 (1996) 1787-1788
56. Segaloff D.L., and Ascoli M. The lutropin/choriogonadotropin receptor ... 4 years later. Endocr. Rev. 14 (1993) 324-347
57. Simoni M., Gromoll J., and Nieschlag E. The follicle-stimulating hormone receptor: biochemistry, molecular biology, physiology, and pathophysiology. Endocr. Rev. 18 (1997) 739-773
58. Stewart E.A. Gonadotropins and the uterus: is there a gonad-independent pathway?. J. Soc. Gynecol. Invest. 8 (2001) 319-326
59. Tao Y.X., Lei Z.M., Woodworth S.H., and Rao C.V. Novel expression of luteinizing hormone/chorionic gonadotropin receptor gene in rat prostates. Mol. Cell. Endocrinol. 111 (1995) R9-R12
60. Tao Y.X., Lei Z.M., and Rao C.V. The presence of luteinizing hormone/human chorionic gonadotropin receptors in lactating rat mammary glands. Life Sci. 60 (1997) 1297-1303
61. Tao Y.X., Lei Z.M., and Rao C.V. Seminal vesicles are novel sites of luteinizing hormone/human chorionic gonadotropin-receptor gene expression. J. Androl. 19 (1998) 343-347
62. Tao Y.X., Heit M., Lei Z.M., and Rao C.V. The urinary bladder of a woman is a novel site of luteinizing hormone-human chorionic gonadotropin receptor gene expression. Am. J. Obstet. Gynecol. 179 (1998) 1026-1031
63. Themmen A.P.N., and Huhtaniemi I.T. Mutations of gonadotropins and gonadotropin receptors: elucidating the physiology and pathophysiology of pituitary-gonadal function. Endocr. Rev. 21 (2000) 551-583
64. Venencie P.Y., Meduri G., Pissard S., Jolivet A., Loosfelt H., Milgrom E., and Misrahi M. Luteinizing hormone/human chorionic gonadotrophin receptors in various epidermal structures. Br. J. Dermatol. 141 (1999) 438-446
65. Wong T.T., and Zohar Y. Novel expression of gonadotropin subunit genes in oocytes of the gilthead seabream (Sparus aurata). Endocrinology 145 (2004) 5210-5220
66. Yarram S.J., Perry M.J., Christopher T.J., Westby K., Brown N.L., Lamminen T., Rulli S.B., Zhang F.P., Huhtaniemi I., Sandy J.R., and Mansell J.P. Luteinizing hormone receptor knockout (LuRKO) mice and transgenic human chorionic gonadotropin (hCG)-overexpressing mice (hCG alphabeta+) have bone phenotypes. Endocrinology 144 (2003) 3555-3564
67. Zhang F.P., Rannikko A., and Huhtaniemi I. Isolation and characterization of testis-specific cDNAs for luteinizing hormone beta-subunit in the rat. Biochem. Biophys. Res. Commun. 210 (1995) 858-865
68. Zhang F.P., Markkula M., Toppari J., and Huhtaniemi I. Novel expression of luteinizing hormone subunit genes in the rat testis. Endocrinology 136 (1995) 2904-2912
69. Zhang F.P., Poutanen M., Wilbertz J., and Huhtaniemi I. Normal prenatal but arrested postnatal sexual development of luteinizing hormone receptor knockout (LuRKO) mice. Mol. Endocrinol. 15 (2001) 172-183
70. Zhang F.P., Pakarainen T., Poutanen M., Toppari J., and Huhtaniemi I. The low gonadotropin-independent constitutive production of testicular testosterone is sufficient to maintain spermatogenesis. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 13692-13697
71. Zhang F.P., Pakarainen T., Zhu F., Poutanen M., and Huhtaniemi I. Molecular characterization of postnatal development of testicular steroidogenesis in luteinizing hormone receptor knockout mice. Endocrinology 145 (2004) 1453-1463
72. Zhang M., Shi H., Segaloff D.L., and Van Voorhis B.J. Expression and localization of luteinizing hormone receptor in the female mouse reproductive tract. Biol. Reprod. 64 (2001) 179-187