Insulin-like 3 exposure of the fetal rat gubernaculum modulates expression of genes involved in neural pathways

Biology of Reproduction

Volumn 83, Issue 5, 2010, Pages 774-782

  Johnson, Kamin J ^a   Robbins, Alan K ^a   Wang, Yanping ^a   McCahan, Suzanne M ^a   Chacko, Job K ^a   Barthold, Julia S ^a  

^a NEMOURS ALFRED I DUPONT HOSPITAL FOR CHILDREN   (United States)

Author keywords

Cryptorchidism; Gene expression profiling; Gubernaculum; Hormone actions; Insulin like 3; Male reproduction; Male reproductive tract; Mechanisms of hormone action; Neuron

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; BONE MORPHOGENETIC PROTEIN; INSULIN LIKE 3; PEPTIDE HORMONE; PROTEIN MYB; TRANSCRIPTION FACTOR REL; UNCLASSIFIED DRUG; WNT PROTEIN;

ARTICLE; BIOINFORMATICS; CONSENSUS SEQUENCE; DNA RESPONSIVE ELEMENT; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE INDUCTION; GUBERNACULUM; MALE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RAT; TESTIS;

ANIMALS; EMBRYO, MAMMALIAN; FEMALE; FETAL DEVELOPMENT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENITALIA, FEMALE; GENITALIA, MALE; INSULIN; MALE; NEURAL PATHWAYS; NEUROGENESIS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OSMOLAR CONCENTRATION; PROTEINS; RATS; RATS, LONG-EVANS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEX CHARACTERISTICS; TESTIS; TISSUE CULTURE TECHNIQUES;

RATTUS; RODENTIA;

EID: 77958523300     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.110.085175     Document Type: Article

References (49)

1. Foresta C, Zuccarello D, Garolla A, Ferlin A. Role of hormones, genes, and environment in human cryptorchidism. Endocr Rev 2008; 29:560-580.
2. Barthold JS. Undescended testis: current theories of etiology. Curr Opin Urol 2008; 18:395-400.
3. Klonisch T, Fowler PA, Hombach-Klonisch S. Molecular and genetic regulation of testis descent and external genitalia development. Dev Biol 2004; 270:1-18.
4. Amann RP, Veeramachaneni DN. Cryptorchidism in common eutherian mammals. Reproduction 2007; 133:541-561.
5. Radhakrishnan J, Morikawa Y, Donahoe PK, Hendren WH. Observations on the gubernaculum during descent of the testis. Invest Urol 1979; 16:365-368.
6. van der Schoot P. Towards a rational terminology in the study of the gubernaculum testis: arguments in support of the notion that the cremasteric sac should be considered the gubernaculum in postnatal rats and other mammals. J Anat 1996; 189(Pt 1):97-108.
7. Emmen JM, McLuskey A, Adham IM, Engel W, Grootegoed JA, Brinkmann AO. Hormonal control of gubernaculum development during testis descent: gubernaculum outgrowth in vitro requires both insulin-like factor and androgen. Endocrinology 2000; 141:4720-4727.
8. Fiegel HC, Rolle U, Metzger R, Geyer C, Till H, Kluth D. The testicular descent in the rat: a scanning electron microscopic study. Pediatr Surg Int 2010; 26:643-647.
9. Kubota Y, Temelcos C, Bathgate RA, Smith KJ, Scott D, Zhao C, Hutson JM. The role of insulin 3, testosterone, mullerian-inhibiting substance and relaxin in rat gubernacular growth. Mol Hum Reprod 2002; 8:900-905.
10. Bogatcheva NV, Truong A, Feng S, Engel W, Adham IM, Agoulnik AI. GREAT/LGR8 is the only receptor for insulin-like 3 peptide. Mol Endocrinol 2003; 17:2639-2646.
11. McKinnell C, Sharpe RM, Mahood K, Hallmark N, Scott H, Ivell R, Staub C, Jegou B, Haag F, Koch-Nolte F, Hartung S. Expression of insulin-like factor 3 protein in the rat testis during fetal and postnatal development and in relation to cryptorchidism induced by in utero exposure to di(nbutyl) phthalate. Endocrinology 2005; 146:4536-4544.
12. Zimmermann S, Steding G, Emmen JM, Brinkmann AO, Nayernia K, Holstein AF, Engel W, Adham IM. Targeted disruption of the Insl3 gene causes bilateral cryptorchidism. Mol Endocrinol 1999; 13:681-691.
13. Nef S, Parada LF. Cryptorchidism in mice mutant for Insl3. Nat Genet 1999; 22:295-299.
14. Tomiyama H, Hutson JM, Truong A, Agoulnik AI. Transabdominal testicular descent is disrupted in mice with deletion of insulin-like factor 3 receptor. J Pediatr Surg 2003; 38:1793-1798.
15. Koskimies P, Suvanto M, Nokkala E, Huhtaniemi IT, McLuskey A, Themmen AP, Poutanen M. Female mice carrying a ubiquitin promoter-Insl3 transgene have descended ovaries and inguinal hernias but normal fertility. Mol Cell Endocrinol 2003; 206:159-166.
16. Adham IM, Steding G, Thamm T, Bullesbach EE, Schwabe C, Paprotta I, Engel W. The overexpression of the insl3 in female mice causes descent of the ovaries. Mol Endocrinol 2002; 16:244-252.
17. Halls ML, van der Westhuizen ET, Bathgate RA, Summers RJ. Relaxin family peptide receptors - former orphans reunite with their parent ligands to activate multiple signaling pathways. Br J Pharmacol 2007; 150:677-691.
18. Kumagai J, Hsu SY, Matsumi H, Roh JS, Fu P, Wade JD, Bathgate RA, Hsueh AJ. INSL3/Leydig insulin-like peptide activates the LGR8 receptor important in testis descent. J Biol Chem 2002; 277:31283-31286.
19. Bogatcheva NV, Ferlin A, Feng S, Truong A, Gianesello L, Foresta C, Agoulnik AI. T222P mutation of the insulin-like 3 hormone receptor LGR8 is associated with testicular maldescent and hinders receptor expression on the cell surface membrane. Am J Physiol Endocrinol Metab 2007; 292:E138-E144.
20. van der Schoot P. Fetal testes control the prenatal growth and differentiation of the gubernacular cones in rabbits - a tribute to the late Professor Alfred Jost. Development 1993; 118:1327-1334.
21. Barthold JS, McCahan SM, Singh AV, Knudsen TB, Si X, Campion L, Akins RE. Altered expression of muscle- and cytoskeleton-related genes in a rat strain with inherited cryptorchidism. J Androl 2008; 29:352-366.
22. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009; 4:44-57.
23. Gonye GE, Chakravarthula P, Schwaber JS, Vadigepalli R. From promoter analysis to transcriptional regulatory network prediction using PAINT. Methods Mol Biol 2007; 408:49-68.
24. Borlikova G, Endo S. Inducible cAMP early repressor (ICER) and brain functions. Mol Neurobiol 2009; 40:73-86.
25. Liu H, Palmer D, Jimmo SL, Tilley DG, Dunkerley HA, Pang SC, Maurice DH. Expression of phosphodiesterase 4D (PDE4D) is regulated by both the cyclic AMP-dependent protein kinase and mitogen-activated protein kinase signaling pathways. A potential mechanism allowing for the coordinated regulation of PDE4D activity and expression in cells. J Biol Chem 2000; 275:26615-26624.
26. Anand-Ivell R, Heng K, Hafen B, Setchell B, Ivell R. Dynamics of INSL3 peptide expression in the rodent testis. Biol Reprod 2009; 81:480-487.
27. Anand-Ivell R, Ivell R, Driscoll D, Manson J. Insulin-like factor 3 levels in amniotic fluid of human male fetuses. Hum Reprod 2008; 23:1180-1186.
28. Zaveri NT, Waleh N, Toll L. Regulation of the prepronociceptin gene and its effect on neuronal differentiation. Gene 2006; 384:27-36.
29. Houslay MD, Baillie GS, Maurice DH. cAMP-specific phosphodiesterase-4 enzymes in the cardiovascular system: a molecular toolbox for generating compartmentalized cAMP signaling. Circ Res 2007; 100:950-966.
30. Green MC. Mechanism of the pleiotropic effects of the short-ear mutant gene in the mouse. J Exp Zool 1968; 167:129-150.
31. Cook C, Vezina CM, Allgeier SH, Shaw A, Yu M, Peterson RE, Bushman W. Noggin is required for normal lobe patterning and ductal budding in the mouse prostate. Dev Biol 2007; 312:217-230.
32. Warr N, Siggers P, Bogani D, Brixey R, Pastorelli L, Yates L, Dean CH, Wells S, Satoh W, Shimono A, Greenfield A. Sfrp1 and Sfrp2 are required for normal male sexual development in mice. Dev Biol 2009; 326:273-284.
33. Charron F, Tessier-Lavigne M. The Hedgehog, TGF-beta/BMP and Wnt families of morphogens in axon guidance. Adv Exp Med Biol 2007; 621:116-133.
34. Hodge LK, Klassen MP, Han BX, Yiu G, Hurrell J, Howell A, Rousseau G, Lemaigre F, Tessier-Lavigne M, Wang F. Retrograde BMP signaling regulates trigeminal sensory neuron identities and the formation of precise face maps. Neuron 2007; 55:572-586.
35. Forger NG, Prevette D, deLapeyriere O, de Bovis B, Wang S, Bartlett P, Oppenheim RW. Cardiotrophin-like cytokine/cytokine-like factor 1 is an essential trophic factor for lumbar and facial motoneurons in vivo. J Neurosci 2003; 23:8854-8858.
36. Elson GC, Lelievre E, Guillet C, Chevalier S, Plun-Favreau H, Froger J, Suard I, de Coignac AB, Delneste Y, Bonnefoy JY, Gauchat JF, Gascan H. CLF associates with CLC to form a functional heteromeric ligand for the CNTF receptor complex. Nat Neurosci 2000; 3:867-872.
37. Chen H, Firestein BL. RhoA regulates dendrite branching in hippocampal neurons by decreasing cypin protein levels. J Neurosci 2007; 27:8378-8386.
38. O'Brien RJ, Xu D, Petralia RS, Steward O, Huganir RL, Worley P. Synaptic clustering of AMPA receptors by the extracellular immediateearly gene product Narp. Neuron 1999; 23:309-323.
39. Tsui CC, Copeland NG, Gilbert DJ, Jenkins NA, Barnes C, Worley PF. Narp, a novel member of the pentraxin family, promotes neurite outgrowth and is dynamically regulated by neuronal activity. J Neurosci 1996; 16:2463-2478.
40. Taniguchi M, Masuda T, Fukaya M, Kataoka H, Mishina M, Yaginuma H, Watanabe M, Shimizu T. Identification and characterization of a novel member of murine semaphorin family. Genes Cells 2005; 10:785-792.
41. Ango F, di Cristo G, Higashiyama H, Bennett V, Wu P, Huang ZJ. Ankyrin-based subcellular gradient of neurofascin, an immunoglobulin family protein, directs GABAergic innervation at purkinje axon initial segment. Cell 2004; 119:257-272.
42. Volkmer H, Leuschner R, Zacharias U, Rathjen FG. Neurofascin induces neurites by heterophilic interactions with axonal NrCAM while NrCAM requires F11 on the axonal surface to extend neurites. J Cell Biol 1996; 135:1059-1069.
43. Moore SW, Tessier-Lavigne M, Kennedy TE. Netrins and their receptors. Adv Exp Med Biol 2007; 621:17-31.
44. Allen RG, Peng B, Pellegrino MJ, Miller ED, Grandy DK, Lundblad JR, Washburn CL, Pintar JE. Altered processing of pro-orphanin FQ/nociceptin and pro-opiomelanocortin-derived peptides in the brains of mice expressing defective prohormone convertase 2. J Neurosci 2001; 21:5864-5870.
45. Capuano A, Curro D, Dello Russo C, Tringali G, Pozzoli G, Di Trapani G, Navarra P. Nociceptin (1-13)NH2 inhibits stimulated calcitonin-gene-related- peptide release from primary cultures of rat trigeminal ganglia neurones. Cephalalgia 2007; 27:868-876.
46. Pettersson LM, Sundler F, Danielsen N. Expression of orphanin FQ/nociceptin and its receptor in rat peripheral ganglia and spinal cord. Brain Res 2002; 945:266-275.
47. Momose Y, Griffiths AL, Hutson JM. Testicular descent. III. The neonatal mouse gubernaculum shows rhythmic contraction in organ culture in response to calcitonin gene-related peptide. Endocrinology 1992; 131:2881-2884.
48. Yamanaka J, Metcalfe SA, Hutson JM, Mendelsohn FA. Testicular descent. II. Ontogeny and response to denervation of calcitonin gene-related peptide receptors in neonatal rat gubernaculum. Endocrinology 1993; 132:280-284.
49. Hrabovszky Z, Farmer PJ, Hutson JM. Undescended testis is accompanied by calcitonin gene related peptide accumulation within the sensory nucleus of the genitofemoral nerve in trans-scrotal rats. J Urol 2001; 165:1015-1018.