Insulin-like 3 signalling in testicular descent

International Journal of Andrology

Volumn 27, Issue 5, 2004, Pages 257-265

  Adham, Ibrahim M ^a   Agoulnik, Alexander I ^b  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Cryptorchidism; GREAT LGR8; Insulin like 3; Relaxin like peptide; Testis descent

Indexed keywords

G PROTEIN COUPLED RECEPTOR; HORMONE RECEPTOR; INSULIN RECEPTOR; RECEPTOR PROTEIN; TESTIS PEPTIDE HORMONE;

CANCER RISK; CRYPTORCHISM; EMBRYO DEVELOPMENT; GENE MUTATION; GENETIC ANALYSIS; HUMAN; INFERTILITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; SEX DIFFERENCE; SIGNAL TRANSDUCTION; TESTIS; TESTIS CANCER; TESTIS DESCENT; TRANSGENIC MOUSE;

ANIMALS; CRYPTORCHIDISM; HUMANS; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 3; MALE; MICE; MICE, TRANSGENIC; SIGNAL TRANSDUCTION; TESTIS;

EID: 5644233835     PISSN: 01056263     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2605.2004.00481.x     Document Type: Review

References (72)

1. Adham, I. M., Seeding, G., Thamm, T., Bullesbach, E. E., Schwabe, C., Paprotta, I. & Engel, W. (2002) The overexpression of the insl3 in female mice causes descent of the ovaries. Molecular Endocrinology 16, 244-252.
2. Baker, L. A., Nef, S., Nguyen, M. T., Stapleton, R., Nordenskjold, A., Pohl, H. & Parada, L. F. (2002) The insulin-3 gene: lack of a genetic basis for human cryptorchidism. Journal of Urology 167, 2534-2537.
3. Balvers, M., Spiess, A. N., Domagalski, R., Hunt, N., Kilic, E., Mukhopadhyay, A. K., Hanks, E., Charlton, H. M. & Ivell, R. (1998) Relaxin-like factor expression as a marker of differentiation in the mouse testis and ovary. Endocrinology 139, 2960-2970.
4. Bathgate, R. A., Samuel, C. S., Burazin, T. C., Gundlach, A. L. & Tregear, G. W. (2000) Relaxin: new peptides, receptors and novel actions. Trends in Endocrinology and Metabolism 14, 207-213.
5. Block, K., Kardana, A., Igarashi, P. & Taylor, H. S. (2000) In utero diethylstilbestrol (DES) exposure alters Hox gene expression in the developing mullerian system. FASEB Journal 14, 1101-1108.
6. Bogatcheva, N. V., Truong, A., Feng, S., Engel, W., Adham, I. M. & Agoulnik, A. I. (2003) GREAT/LGR8 is the only receptor for insulin-like 3 peptide. Molecular Endocrinology 17, 2639-2646.
7. Boockfor, F. R., Fullbright, G., Bullesbach, E. E. & Schwabe, C. (2001) Relaxin-like factor (RLF) serum concentrations and gubernaculum RLF receptor display in relation to pre- and neonatal development of rats. Reproduction 122, 899-906.
8. Bullesbach, E. E. & Schwabe, C. (1999) Tryptophan B27 in the relaxin-like factor (RLF) is crucial for RLF receptor-binding. Biochemistry 38, 3073-3078.
9. Bullesbach, E. E., Rhodes, R., Rembiesa, B. & Schwabe, C. (1999) The relaxin-like factor is a hormone. Endocrine 10, 167-169.
10. Canto, P., Escudero, I., Soderlund, D., Nishimura, E., Carranza-Lira, S., Gutierrez, J., Nava, A. & Mendez, J. P. (2003) A novel mutation of the insulin-like 3 gene in patients with cryptorch-idism. Journal of Human Genetics 48, 86-90.
11. Costa, W. S., Sampaio, F. J., Favorito, L. A. & Cardoso, L. E. (2002) Testicular migration: remodeling of connective tissue and muscle cells in human gubernaculum testis. Journal of Urology 167, 2171-2176.
12. Elder, J. S. (1988) The undescended testis. Hormonal and surgical management. The Surgical Clinics of North American 68, 983-1005.
13. Emmen, J. M. A., McLuskey, A., Adham, I. M., Engel, W., Verhoef-Post, M., Themmen, A. P. N., Grootegoed, J. A. & Brinkmann, A. O. (2000a) Involvement of insulin-like factor 3 (Insl3) in diethylstilbestrol-induced cryptorchidism. Endocrinology 141, 846-849.
14. Emmen, J. M. A., McLuskey, A., Adham, I. M., Engel, W., Grootegoed, J. A. & Brinkmann, A. O. (2000b) Hormonal control of gubernaculum development during testis descent: gubernaculum outgrowth in vitro requires both insulin-like factor and androgen. Endocrinology 141, 4720-4727.
15. Fentener van Vlissingen, J. M., van Zoelen, E. J. J., Ursem, P. J. F. & Wensing, C. J. G. (1988) In vitro model of the first phase of testicular descent: identification of a low molecular weight factor from fetal testis involved in proliferation of gubernaculum cells and distinct from specified polypeptide growth factors and fetal gonadal hormones. Endocrinology 123, 2868-2877.
16. Ferlin, A., Simonato, M., Bartoloni, L., Rizzo, G., Bettella, A., Dottorini, T., Dallapiccola, B. & Foresta, C. (2003) The INSL3-LGR8/GREAT ligand-receptor pair in human cryptorchidism. The Journal of Clinical Endocrinology & Metabolism 88, 4273-4279.
17. Fry, D. M. & Toone, C. K. (1981) DDT-induced feminization of gull embryos. Science 213, 922-924.
18. Garcia-Rodriguez, J., Garcia-Martin, M., Nogueras-Ocana, M., de Dios Luna-del-Castillo, J., Espigares Garcia, M., Olea, N. & Lardelli-Claret, P. (1996) Exposure to pesticides and cryptorchidism: geographical evidence of a possible association. Environmental Health Perspectives 104, 1090-1095.
19. Gorlov, I. P., Kamat, A., Bogatcheva, N. V., Jones, E., Lamb, D. J., Truong, A., Bishop, C. E., McElreavey, K. & Agoulnik, A. I. (2002) Mutations of the GREAT gene cause cryptorchidism. Human Molecular Genetics 11, 2309-2318.
20. Heyns, C. F. & Hutson, J. M. (1995) Historical review of theories on testicular descent. Journal of Urology 155, 2036-2038.
21. Hsu, S. Y., Nakabayashi, K., Nishi, S., Kumagai, J., Kudo, M., Sherwood, O. D. & Hsueh, A. J. (2002) Activation of orphan receptors by the hormone relaxin. Science 295, 671-674.
22. Hsu, S. Y., Nakabayashi, K., Nishi, S., Kumagai, J., Kudo, M., Bathgate, R. A., Sherwood, O. D. & Hsueh, A. J. (2003) Relaxin signalling in reproductive tissues. Molecular and Cellular Endocrinology 202, 165-170.
23. Hutson, J. M. (1986) Testicular feminization: a model for testicular descent in mice and men. Journal of Pediatric Surgery 21, 195-199.
24. Hutson, J. M. & Beasley, S. W. (1988) Embryological controversies in testicular descent. Seminars of Urology 6, 68-73.
25. Hutson, J. M., Hasthorpe, S. & Heyns, C. F. (1997) Anatomical and function aspects of testicular descent and cryptorchidism. Endocrine Review 18, 259-280.
26. Ikeda, Y., Shen, W. H., Ingraham, H. A. & Parker, K. L. (1994) Developmental expression of mouse steroidogenic factor-1, an essential regulator of the steroid hydroxylases. Molecular Endocrinology 8, 654-662.
27. Ivell, R. & Einspanier, A. (2002) Relaxin peptides are new global players. Trends in Endocrinology and Metabolism 13, 343-348.
28. Jost, A. (1953) Problem of fetal endocrinology: the gonadal and hypophysial hormones. Recent Progress of Hormone Research 8, 379-413.
29. Kersten, W., Molenaar, G. J., Emmen, J. M. & van der Schoot, P. (1996) Bilateral cryptorchidism in a dog with persistent cranial testis suspensory ligaments and inverted gubernacula: report of a case with implications for understanding normal and aberrant testis descent. Journal of Anatomy 189, 171-176.
30. Koskimies, P., Virtanen, H., Lindstrom, M., Kaleva, M., Poutanen, M., Huhtaniemi, I. & Toppari, J. (2000) A common polymorphism in the human relaxin-like factor (RLF) gene: no relationship with cryptorchidism. Pediatric Research 47, 538-541.
31. Koskimies, P., Levallet, J., Sipila, P., Huhtanierni, I. & Poutanen, M. (2002) Murine relaxin-like factor promoter: functional characterization and regulation by transcription factors steroidogenic factor 1 and DAX-1. Endocrinology 143, 909-919.
32. Koskimies, P., Suvanto, M., Nokkala, E., Huhtaniemi, I. T., McLuskey, A., Themmen, A. P. & Poutanen, M. (2003) Female mice carrying a ubiquitin promoter-Insl3 transgene have descended ovaries and inguinal hernias but normal fertility. Molecular and Cellular Endocrinology 206, 159-166.
33. Krausz, C., Quintana-Murci, L., Fellous, M., Siffroi, J. P. & McElreavey, K. (2000) Absence of mutations involving the INSL3 gene in human idiopathic cryptorchidism. Molecular Human Reproduction 6, 298-302.
34. Kubota, Y., Nef, S., Farmer, P. J., Temelcos, C., Parada, L. F. & Hutson, J. M. (2001) Leydig insulin-like hormone, gubernacular development and testicular descent. Journal of Urology 165, 1673-1675.
35. Kubota, Y., Temelcos, C., Bathgate, R. A., Smith, K. J., Scott, D., Zhao, C. & Hutson, J. M. (2002) The role of insulin 3, testosterone, Mullerian inhibiting substance and relaxin in rat gubernacular growth. Molecular Human Reproduction 8, 900-905.
36. Kumagai, J., Hsu, S. Y., Matsumi, H., Roh, J. S., Fu, P., Wade, J. D., Bathgate, R. A. & Hsueh, A. J. (2002) INSL3/Leydig insulin-like peptide activates the LGR8 receptor important in testis descent. Journal of Biological Chemistry 277, 31283-31286.
37. Lim, H. N., Raipert-de Meyts, E., Skakkebaek, N. E., Hawkins, J. R. & Hughes, I. A. (2001) Genetic analysis of the INSL3 gene in patients with maldescent of the testis. European Journal of Endocrinology 144, 129-137.
38. Lovell-Badge, R., Canning, C. & Sekido, R. (2002) Sex-determining genes in mice: building pathways. Novartis Foundation Symposium 244, 4-18.
39. Ma, L., Benson, G. V., Lim, H., Dey, S. K. & Maas, R. L. (1998) Abdominal B (AbdB) Hoxa genes: regulation in adult uterus by estrogen and progesterone and repression in mullerian duct by the synthetic estrogen diethylstilbestrol (DES). Developmental Biology 197, 141-154.
40. Marin, P., Ferlin, A., Moro, E., Rossi, A., Bartoloni, L., Rossato, M. & Foresta, C. (2001) Novel insulin-like 3 (INSL3) gene mutation associated with human cryptorchidism. American Journal of Medical Genetics 103, 348-349.
41. Nef, S. & Parada, L. F. (1999) Cryptorchidism in mice mutant for Insl3. Nature Genetics 22, 295-299.
42. Nef S., Shipman, T. & Parada, L. F. (2000) A molecular basis for estrogen-induced cryptorchidism. Developmental Biology 224, 354-361.
43. Newbold, R. R. & McLachlan, J. A. (1996) Transplacental hormonal carcinogenesis: diethylstilbestrol as an example. Progress in Clinical and Biological Research 394, 131-147.
44. Newbold, R. R., Hanson, R. B., Jefferson, W. N., Bullock, B. C., Haseman, J. & McLachlan, J. A. (2000) Proliferative lesions and reproductive tract tumors in male descendants of mice exposed developmentally to diethylstilbestrol. Carcinogenesis 21, 1355-1363.
45. Overbeek, P. A., Gorlov, I. P., Sutherland, R. W., Houston, J. B., Harrison, W. R., Boettger-Tong, H. L., Bishop, C. E. & Agoulnik, A. I. (2001) A transgenic insertion causing cryptorchidism in mice. Genesis 30, 26-35.
46. Pusch, W., Balvers, M. & Ivell, R. (1996) Molecular cloning and expression of the relaxin-like factor from the mouse testis. Endocrinology 137, 3009-3013.
47. Riegler, H. C. (1972) Torsion of intra-abdominal testis: an unusual problem in diagnosis of the acute surgical abdomen. The Surgical Clinics of North American 52, 371-374.
48. Rijli, F. M., Matyas, R., Pellegrini, M., Dierich, A., Gruss, P., Dolle, P. & Chambon, P. (1995) Cryptorchidism and homeotic transformations of spinal nerves and vertebrae in Hoxa-10 mutant mice. Proceedings of the National Academy of Sciences the United States of America 92, 8185-8189.
49. Roh, J., Virtanen, H., Kumangai, J., Sudo, S., Kaleva, M., Toparri, J. & Hsueh, A. J. (2003) Lack of LGR8 gene mutation in Finnish patients with a family history of cryptorchidism. Reproductive BioMedicine Online 7, 400-406.
50. Satokata, I., Benson, G. & Maas, R. (1995) Sexually dimorphic sterility phenotypes in Hoxa10-deficient mice. Nature 374, 460-463.
51. Shen, J. H. & Ingraham, H. A. (2002) Regulation of the orphan nuclear receptor steroidogenic factor 1 by Sox proteins. Molecular Endocrinology 16, 529-540.
52. Shono, T., Hutson, J. M., Watts, L., Goh, D. W., Momose, Y., Middlesworth, B., Zhou, B. & Ramm-Anderson, S. (1996) Scanning electron microscopy shows inhibited gubernacular development in relation to undescended testes in oestrogen-treated mice. International Journal of Andrology 19, 263-270.
53. Silvertown, J. D., Summerlee, A. J. & Klonisch, T. (2003) Relaxin-like peptides in cancer. International Journal of Cancer 107, 513-519.
54. Smith, K. J., Wade, J. D., Claasz, A. A., Otvos, L. Jr, Temelcos, C., Kubota, Y., Hutson, J. M., Tregear, G. W. & Bathgate, R. A. (2001) Chemical synthesis and biological activity of rat INSL3. Journal of Peptide Science 7, 495-501.
55. Sudo, S., Kumagai, J., Nishi, S., Layfield, S., Ferraro, T., Bathgate, R. A. & Hsueh, A. J. (2003) H3 relaxin is a specific ligand for LGR7 and activates the receptor by interacting with both the ectodomain and the exoloop 2. Journal of Biological Chemistry 278, 7855-7862.
56. Takahashi, I., Takahashi, T., Komatsu, M., Matsuda, J. & Takada, G. (2001) Ala/Thr60 variant of the Leydig insulin-like hormone is not associated with cryptorchidism in the Japanese population. Pediatrics International 43, 256-258.
57. Thonneau, P. F., Gandia, P. & Mieusset, R. (2003) Cryptorchidism: incidence, risk factors, and potential role of environment; an update. Journal of Andrology 24, 155-162.
58. Tomboc, M., Lee, P. A., Mitwally, M. F., Schneck, F. X., Bellinger, M. & Witchel, S. F. (2000) Insulin-like 3/relaxin-like factor gene mutations are associated with cryptorchidism. The Journal of Clinical Endocrinology & Metabolism 85, 4013-4018.
59. Tomiyama, H., Hutson, J. M., Truong, A. & Agoulnik, A. I. (2003) Transabdominal testicular descent is disrupted in mice with deletion of insulin-like factor 3 receptor. Journal of Pediatric Surgery 38, 1793-1798.
60. Toppari, J., Larsen, J. C., Christiansen, P., Giwercman, A., Grandjean, P., Guillette, L. J. et al. (1996) Male reproductive health and environmental xenoestrogens. Environmental Health Perspectives 104, 741-803.
61. Toppari, J., Kaleva, M. & Virtainen, H. E. (2001) Trends in the incidence of cryptorchidism and hypospadias and methodological limitations of registry-based data. Human Reproduction update 7, 282-286.
62. Truong, A., Bogatcheva, N. V., Schelling, C., Dolf, G. & Agoulnik, A. I. (2003) Isolation and expression analysis of the canine insulin-like factor 3 gene. Biology of Reproduction 69, 1658-1664.
63. Tyler, C. R., Jobling, S. & Sumpter, J. P. (1998) Endocrine disruption in wildlife: a critical review of the evidence. Critical Review of Toxicology 28, 319-361.
64. van der Schoot, P. & Elger, W. (1992) Androgen-induced prevention of the outgrowth of cranial suspensory ligaments in fetal rats. Journal of Andrology 31, 534-542.
65. Weidner, I. S., Moller, H., Jensen, T. K. & Skakkebaek, N. E. (1998) Cryptorchidism and hypospadias in sons of gardeners and farmers. Environmental Health Perspectives 106, 793-796.
66. Welch, R. M., Levin, W. & Conney, A. H. (1969) Estrogenic action of DDT and its analogs. Toxicology and Applied Pharmacology 14, 358-367.
67. Wensing, C. J. G. (1986) Testicular descent in the rat and a comparison of the process in the rat with that in the pig. Anatomical Record 214, 154-160.
68. Wensing, C. J. (1988) The embryology of testicular descent. Hormone Research 30, 144-152.
69. Zhao, L., Roche, P. J., Gunnersen, J. M., Hammond, V. E., Tregear, G. W., Wintour, E. M. & Beck, F. (1999) Mice without a functional relaxin gene are unable to deliver milk to their pups. Endocrinology 140, 445-453.
70. Zimmermann, S., Schöttler, P., Engel, W. & Adham, I. M. (1997) Mouse Leydig insulin-like (Ley I-L) gene: structure and expression during testis and ovary development. Molecular Reproduction and Development 47, 30-38.
71. Zimmermann, S., Schwarzler, A., Buth, S., Engel, W. & Adham, I. M. (1998) Transcription of the Leydig insulin-like gene is mediated by steroidogenic factor-1. Molecular Endocrinology 12, 706-713.
72. Zimmermann, S., Steding, G., Emmen, J. M. A., Brinkmann, A. O., Nayernia, K., Holstein, A. F., Engel, W. & Adham, I. M. (1999) Targeted disruption of the Insl3 gene causes bilateral cryptorchidism. Molecular Endocrinology 13, 681-691.