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Molecular Endocrinology 13 (5): 681-691
Copyright © 1999 by The Endocrine Society

Targeted Disruption of the Insl3 Gene Causes Bilateral Cryptorchidism

Stephan Zimmermann, Gerd Steding, Judith M. A. Emmen, Albert O. Brinkmann, Karim Nayernia, Adolf F. Holstein, Wolfgang Engel and Ibrahim M. Adham

Institut für Humangenetik der Universität Göttingen (S.Z., K.N., W.E., I.M.A.) D-37073 Göttingen, Germany
Abteilung Embryologie der Universität Göttingen (G.S.) D-37075 Göttingen, Germany
Endocrinology and Reproduction (J.M.A.E., A.O.B.) Erasmus University Rotterdam N-3000 DR Rotterdam, The Netherlands
Abteilung für Mikroskopische Anatomie (A.E.H.) Universität-Krankenhaus Eppendorf D-20251 Hamburg, Germany

The sexual dimorphic position of the gonads in mammals is dependent on differential development of two ligaments, the cranial suspensory ligament (CSL) and the gubernaculum. During male embryogenesis, outgrowth of the gubernaculum and regression of the CSL result in transabdominal descent of the testes, whereas in the female, development of the CSL in conjunction with failure of the gubernaculum development holds the ovaries in a position lateral to the kidneys. Several lines of evidence suggest that regression of the CSL and induction of gubernaculum development are mediated by testosterone and a yet unidentified testicular factor, respectively. The Insl3 gene (orginally designated Ley I-L), a member of the insulin-like superfamily, is specifically expressed in Leydig cells of the fetal and postnatal testis and in theca cells of the postnatal ovary. Here we show that male mice homozygous for a targeted deletion of the Insl3 locus exhibit bilateral cryptorchidism with free moving testes and genital ducts. These malformations are due to failure of gubernaculum development during embryogenesis. In double-mutant male mice for Insl3 and androgen receptor genes, testes are positioned adjacent to the kidneys and steadied in the abdomen by the CSL. These findings demonstrate, that the Insl3 induces gubernaculum development in an androgen-independent way, while androgen-mediated regression of the CSL occurs independently from Insl3.




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 Biol. Reprod.Home page
A. Truong, N. V. Bogatcheva, C. Schelling, G. Dolf, and A. I. Agoulnik
Isolation and Expression Analysis of the Canine Insulin-Like Factor 3 Gene
Biol Reprod, November 1, 2003; 69(5): 1658 - 1664.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
A. Ferlin, M. Simonato, L. Bartoloni, G. Rizzo, A. Bettella, T. Dottorini, B. Dallapiccola, and C. Foresta
The INSL3-LGR8/GREAT Ligand-Receptor Pair in Human Cryptorchidism
J. Clin. Endocrinol. Metab., September 1, 2003; 88(9): 4273 - 4279.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
J. D. Silvertown, B. J. Geddes, and A. J. S. Summerlee
Adenovirus-Mediated Expression of Human Prorelaxin Promotes the Invasive Potential of Canine Mammary Cancer Cells
Endocrinology, August 1, 2003; 144(8): 3683 - 3691.
[Abstract] [Full Text] [PDF]

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 J AndrolHome page
M. R. Maduro, K. C. Lo, W. W. Chuang, and D. J. Lamb
Genes and Male Infertility: What Can Go Wrong?
J Androl, July 1, 2003; 24(4): 485 - 493.
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 Biol. Reprod.Home page
T. Klonisch, K. Steger, A. Kehlen, W. R. Allen, C. Froehlich, J. Kauffold, M. Bergmann, and S. Hombach-Klonisch
INSL3 Ligand-Receptor System in the Equine Testis
Biol Reprod, June 1, 2003; 68(6): 1975 - 1981.
[Abstract] [Full Text] [PDF]

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 Mol Hum ReprodHome page
R. Ivell and S. Hartung
The molecular basis of cryptorchidism
Mol. Hum. Reprod., April 1, 2003; 9(4): 175 - 181.
[Abstract] [Full Text] [PDF]

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 J AndrolHome page
P. F. Thonneau, P. Candia, and R. Mieusset
Cryptorchidism: Incidence, Risk Factors, and Potential Role of Environment; An Update
J Androl, March 1, 2003; 24(2): 155 - 162.
[Full Text] [PDF]

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 Mol Hum ReprodHome page
Y. Kubota, C. Temelcos, R.A.D. Bathgate, K.J. Smith, D. Scott, C. Zhao, and J.M. Hutson
The role of insulin 3, testosterone, Mullerian inhibiting substance and relaxin in rat gubernacular growth
Mol. Hum. Reprod., October 1, 2002; 8(10): 900 - 905.
[Abstract] [Full Text] [PDF]

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 Hum Mol GenetHome page
I. P. Gorlov, A. Kamat, N. V. Bogatcheva, E. Jones, D. J. Lamb, A. Truong, C. E. Bishop, K. McElreavey, and A. I. Agoulnik
Mutations of the GREAT gene cause cryptorchidism
Hum. Mol. Genet., September 15, 2002; 11(19): 2309 - 2318.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
R. Ivell and R. A.D. Bathgate
Reproductive Biology of the Relaxin-Like Factor (RLF/INSL3)
Biol Reprod, September 1, 2002; 67(3): 699 - 705.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
J. Kumagai, S. Y. Hsu, H. Matsumi, J.-S. Roh, P. Fu, J. D. Wade, R. A. D. Bathgate, and A. J. W. Hsueh
INSL3/Leydig Insulin-like Peptide Activates the LGR8 Receptor Important in Testis Descent
J. Biol. Chem., August 23, 2002; 277(35): 31283 - 31286.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
H. F. Irving-Rodgers, R. A.D. Bathgate, R. Ivell, R. Domagalski, and R. J. Rodgers
Dynamic Changes in the Expression of Relaxin-Like Factor (Insl3), Cholesterol Side-Chain Cleavage Cytochrome P450, and 3{beta}-Hydroxysteroid Dehydrogenase in Bovine Ovarian Follicles During Growth and Atresia
Biol Reprod, April 1, 2002; 66(4): 934 - 943.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
P.J. O'Shaughnessy, L. Willerton, and P.J. Baker
Changes in Leydig Cell Gene Expression During Development in the Mouse
Biol Reprod, April 1, 2002; 66(4): 966 - 975.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
J. H.-C. Shen and H. A. Ingraham
Regulation of the Orphan Nuclear Receptor Steroidogenic Factor 1 by Sox Proteins
Mol. Endocrinol., March 1, 2002; 16(3): 529 - 540.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
P. Koskimies, J. Levallet, P. Sipila, I. Huhtaniemi, and M. Poutanen
Murine Relaxin-Like Factor Promoter: Functional Characterization and Regulation by Transcription Factors Steroidogenic Factor 1 and DAX-1
Endocrinology, March 1, 2002; 143(3): 909 - 919.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
I. M. Adham, G. Steding, T. Thamm, E. E. Bullesbach, C. Schwabe, I. Paprotta, and W. Engel
The Overexpression of the Insl3 in Female Mice Causes Descent of the Ovaries
Mol. Endocrinol., February 1, 2002; 16(2): 244 - 252.
[Abstract] [Full Text] [PDF]

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 ScienceHome page
S. Y. Hsu, K. Nakabayashi, S. Nishi, J. Kumagai, M. Kudo, O. D. Sherwood, and A. J. W. Hsueh
Activation of Orphan Receptors by the Hormone Relaxin
Science, January 25, 2002; 295(5555): 671 - 674.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
N. Pitteloud, F. J. Hayes, P. A. Boepple, S. DeCruz, S. B. Seminara, D. T. MacLaughlin, and W. F. Crowley Jr.
The Role of Prior Pubertal Development, Biochemical Markers of Testicular Maturation, and Genetics in Elucidating the Phenotypic Heterogeneity of Idiopathic Hypogonadotropic Hypogonadism
J. Clin. Endocrinol. Metab., January 1, 2002; 87(1): 152 - 160.
[Abstract] [Full Text] [PDF]

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 Endocr. Rev.Home page
J. Nakae, Y. Kido, and D. Accili
Distinct and Overlapping Functions of Insulin and IGF-I Receptors
Endocr. Rev., December 1, 2001; 22(6): 818 - 835.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
I. A. Hughes
Minireview: Sex Differentiation
Endocrinology, August 1, 2001; 142(8): 3281 - 3287.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
G. de Rienzo, F. Aniello, M. Branno, and S. Minucci
Isolation and Characterization of a Novel Member of the Relaxin/Insulin Family from the Testis of the Frog Rana esculenta
Endocrinology, July 1, 2001; 142(7): 3231 - 3238.
[Abstract] [Full Text] [PDF]

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 Endocr. Rev.Home page
L. O'Donnell, K. M. Robertson, M. E. Jones, and E. R. Simpson
Estrogen and Spermatogenesis
Endocr. Rev., June 1, 2001; 22(3): 289 - 318.
[Abstract] [Full Text] [PDF]

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 Endocr. Rev.Home page
J. A. McLachlan
Environmental Signaling: What Embryos and Evolution Teach Us About Endocrine Disrupting Chemicals
Endocr. Rev., June 1, 2001; 22(3): 319 - 341.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
D. T. MacLaughlin, J. Teixeira, and P. K. Donahoe
Perspective: Reproductive Tract Development--New Discoveries and Future Directions
Endocrinology, June 1, 2001; 142(6): 2167 - 2172.
[Full Text] [PDF]

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 EndocrinologyHome page
X. Li, E. Nokkala, W. Yan, T. Streng, N. Saarinen, A. Warri, I. Huhtaniemi, R. Santti, S. Makela, and M. Poutanen
Altered Structure and Function of Reproductive Organs in Transgenic Male Mice Overexpressing Human Aromatase
Endocrinology, June 1, 2001; 142(6): 2435 - 2442.
[Abstract] [Full Text] [PDF]

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 Hum ReprodHome page
N.E. Skakkebak, E. Rajpert-De Meyts, and K.M. Main
Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects: Opinion
Hum. Reprod., May 1, 2001; 16(5): 972 - 978.
[Abstract] [Full Text] [PDF]

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 Mol Hum ReprodHome page
S. Hombach-Klonisch, S. Seeger, G. Tscheudschilsuren, J. Buchmann, B. Huppertz, G. Seliger, B. Fischer, and T. Klonisch
Cellular localization of human relaxin-like factor in the cyclic endometrium and placenta
Mol. Hum. Reprod., April 1, 2001; 7(4): 349 - 356.
[Abstract] [Full Text] [PDF]

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 Mol Biol EvolHome page
T. Klonisch, C. Froehlich, F. Tetens, B. Fischer, and S. Hombach-Klonisch
Molecular Remodeling of Members of the Relaxin Family During Primate Evolution
Mol. Biol. Evol., March 1, 2001; 18(3): 393 - 403.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
T. Klonisch, J. Kauffold, K. Steger, M. Bergmann, R. Leiser, B. Fischer, and S. Hombach-Klonisch
Canine Relaxin-Like Factor: Unique Molecular Structure and Differential Expression Within Reproductive Tissues of the Dog
Biol Reprod, February 1, 2001; 64(2): 442 - 450.
[Abstract] [Full Text]

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 Mol. Endocrinol.Home page
F.-P. Zhang, M. Poutanen, J. Wilbertz, and I. Huhtaniemi
Normal Prenatal but Arrested Postnatal Sexual Development of Luteinizing Hormone Receptor Knockout (LuRKO) Mice
Mol. Endocrinol., January 1, 2001; 15(1): 172 - 183.
[Abstract] [Full Text]

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 Genes Dev.Home page
S. Nef and L. F. Parada
Hormones in male sexual development
Genes & Dev., December 15, 2000; 14(24): 3075 - 3086.
[Full Text]

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 EndocrinologyHome page
J. M. A. Emmen, A. McLuskey, I. M. Adham, W. Engel, J. A. Grootegoed, and A. O. Brinkmann
Hormonal Control of Gubernaculum Development during Testis Descent: Gubernaculum Outgrowth in Vitro Requires Both Insulin-Like Factor and Androgen
Endocrinology, December 1, 2000; 141(12): 4720 - 4727.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
M. Tomboc, P. A. Lee, M. F. Mitwally, F. X. Schneck, M. Bellinger, and S. F. Witchel
Insulin-like 3/Relaxin-Like Factor Gene Mutations Are Associated with Cryptorchidism
J. Clin. Endocrinol. Metab., November 1, 2000; 85(11): 4013 - 4018.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
S. Lok, D. S. Johnston, D. Conklin, C. E. Lofton-Day, R. L. Adams, A. C. Jelmberg, T. E. Whitmore, S. Schrader, M. D. Griswold, and S. R. Jaspers
Identification of INSL6, a New Member of the Insulin Family That Is Expressed in the Testis of the Human and Rat
Biol Reprod, June 1, 2000; 62(6): 1593 - 1599.
[Abstract] [Full Text]


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