The role of sonic hedgehog-Gli2 pathway in the masculinization of external genitalia

Endocrinology

Volumn 152, Issue 7, 2011, Pages 2894-2903

  Miyagawa, Shinichi ^a,b   Matsumaru, Daisuke ^a   Murashima, Aki ^a   Omori, Akiko ^a   Satoh, Yoshihiko ^a   Haraguchi, Ryuma ^a   Motoyama, Jun ^c   Iguchi, Taisen ^b   Nakagata, Naomi ^a   Hui, Chi Chung ^d   Yamada, Gen ^a,e  

^a KUMAMOTO UNIVERSITY   (Japan)

^b OKAZAKI INSTITUTE FOR INTEGRATIVE BIOSCIENCE   (Japan)

^c DOSHISHA UNIVERSITY   (Japan)

^d HOSPITAL FOR SICK CHILDREN   (Canada)

^e WAKAYAMA MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO DEVELOPMENT; EPITHELIUM CELL; FEMALE; GENE EXPRESSION; GENE MUTATION; HISTOPATHOLOGY; HORMONE RESPONSE; IMMUNOHISTOCHEMISTRY; MALE; MALE GENITAL SYSTEM; MESENCHYME; MOUSE; MUTANT; NONHUMAN; PREPUCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEX DIFFERENCE; SEX DIFFERENTIATION; SIGNAL TRANSDUCTION; URETHRA; VIRILIZATION;

ANDROGENS; ANIMALS; EPITHELIUM; FEMALE; GENE SILENCING; GENITALIA, FEMALE; GENITALIA, MALE; HEDGEHOG PROTEINS; HYPOSPADIAS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MALE; MESODERM; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MUTANT PROTEINS; SEX DETERMINATION PROCESSES; SIGNAL TRANSDUCTION; TESTOSTERONE PROPIONATE; URETHRA;

EID: 79959392823     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2011-0263     Document Type: Article

References (56)

1. Yamada G, Suzuki K, Haraguchi R, Miyagawa S, Satoh Y, Kamimura M, Nakagata N, Kataoka H, Kuroiwa A, Chen Y 2006 Molecular genetic cascades for external genitalia formation: an emerging organogenesis program. Dev Dyn 235:1738-1752 (Pubitemid 43902334)
2. Baskin LS, Himes K, Colborn T 2001 Hypospadias and endocrine disruption: is there a connection? Environ Health Perspect 109:1175-1183
3. Skakkebaek NE, Rajpert-De Meyts E, Main KM 2001 Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects. Hum Reprod 16:972-978 (Pubitemid 32451837)
4. Haraguchi R, Mo R, Hui C, Motoyama J, Makino S, Shiroishi T, Gaffield W, Yamada G 2001 Unique functions of sonic hedgehog signaling during external genitalia development. Development 128:4241-4250 (Pubitemid 33077035)
5. Haraguchi R, Suzuki K, Murakami R, Sakai M, Kamikawa M, Kengaku M, Sekine K, Kawano H, Kato S, Ueno N, Yamada G 2000 Molecular analysis of external genitalia formation: the role of fibroblast growth factor (Fgf) genes during genital tubercle formation. Development 127:2471-2479 (Pubitemid 30386584)
6. Perriton CL, Powles N, Chiang C, Maconochie MK, Cohn MJ 2002 Sonic hedgehog signaling from the urethral epithelium controls external genital development. Dev Biol 247:26-46 (Pubitemid 34681163)
7. Ingham PW, McMahon AP 2001 Hedgehog signaling in animal development: paradigms and principles. Genes Dev 15:3059-3087 (Pubitemid 33115673)
8. Nieuwenhuis E, Hui CC 2005 Hedgehog signaling and congenital malformations. Clin Genet 67:193-208 (Pubitemid 40277900)
9. Bai CB, Auerbach W, Lee JS, Stephen D, Joyner AL 2002 Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. Development 129:4753-4761 (Pubitemid 35277202)
10. MoR, Freer AM, Zinyk DL, Crackower MA, Michaud J, Heng HH, Chik KW, Shi XM, Tsui LC, Cheng SH, Joyner AL, Hui C 1997 Specific and redundant functions of Gli2 and Gli3 zinc finger genes in skeletal patterning and development. Development 124:113-123 (Pubitemid 27053011)
11. Motoyama J, Liu J, Mo R, Ding Q, Post M, Hui CC 1998 Essential function of Gli2 and Gli3 in the formation of lung, trachea and oesophagus. Nat Genet 20:54-57 (Pubitemid 28410344)
12. Park HL, Bai C, Platt KA, Matise MP, Beeghly A, Hui CC, Nakashima M, Joyner AL 2000 Mouse Gli1 mutants are viable but have defects in SHH signaling in combination with a Gli2 mutation. Development 127:1593-1605 (Pubitemid 30234917)
13. Cunha GR, Chung LW, Shannon JM, Reese BA 1980 Stromal-epithelial interactions in sex differentiation. Biol Reprod 22:19-42
14. Prins GS, Putz O 2008 Molecular signaling pathways that regulate prostate gland development. Differentiation 76:641-659 (Pubitemid 352032742)
15. Cunha GR, Battle E, Young P, Brody J, Donjacour A, Hayashi N, Kinbara H 1992 Role of epithelial-mesenchymal interactions in the differentiation and spatial organization of visceral smooth muscle. Epithelial Cell Biol 1:76-83
16. Hayward SW, Haughney PC, Rosen MA, Greulich KM, Weier HU, Dahiya R, Cunha GR 1998 Interactions between adult human prostatic epithelium and rat urogenital sinus mesenchyme in a tissue recombination model. Differentiation 63:131-140 (Pubitemid 28362377)
17. Kurzrock EA, Baskin LS, Li Y, Cunha GR 1999 Epithelial-mesenchymal interactions in development of the mouse fetal genital tubercle. Cells Tissues Organs 164:125-130 (Pubitemid 29313707)
18. Murakami R, Mizuno T 1986 Proximal-distal sequence of development of the skeletal tissues in the penis of rat and the inductive effect of epithelium. J Embryol Exp Morphol 92:133-143
19. Jost A 1953 Problems of fetal endocrinology: the gonadal and hypophyseal hormones. Recent Prog Horm Res 8:379-418
20. Hui CC, Joyner AL 1993 A mouse model of greig cephalopolysyndactyly syndrome: the extra-toesJ mutation contains an intragenic deletion of the Gli3 gene. Nat Genet 3:241-246 (Pubitemid 23096560)
21. Chiang C, Litingtung Y, Lee E, Young KE, Corden JL, Westphal H, Beachy PA 1996 Cyclopia and defective axial patterning in mice lacking sonic hedgehog gene function. Nature 383:407-413 (Pubitemid 26330823)
22. Dassule HR, Lewis P, Bei M, Maas R, McMahon AP 2000 Sonic hedgehog regulates growth and morphogenesis of the tooth. Development 127:4775-4785
23. Hayashi S, McMahon AP 2002 Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol 244:305-318 (Pubitemid 34450645)
24. Haraguchi R, Motoyama J, Sasaki H, Satoh Y, Miyagawa S, Nakagata N, Moon A, Yamada G 2007 Molecular analysis of coordinated bladder and urogenital organ formation by hedgehog signaling. Development 134:525-533 (Pubitemid 46332489)
25. Jeong J, Mao J, Tenzen T, Kottmann AH, McMahon AP 2004 Hedgehog signaling in the neural crest cells regulates the patterning and growth of facial primordia. Genes Dev 18:937-951 (Pubitemid 38529662)
26. Feil R, Wagner J, Metzger D, Chambon P 1997 Regulation of Cre recombinase activity by mutated estrogen receptor ligand-binding domains. Biochem Biophys Res Commun 237:752-757 (Pubitemid 27434760)
27. Nishida H, Miyagawa S, Vieux-Rochas M, Morini M, Ogino Y, Suzuki K, Nakagata N, Choi HS, Levi G, Yamada G 2008 Positive regulation of steroidogenic acute regulatory protein gene expression through the interaction between Dlx and GATA-4 for testicular steroidogenesis. Endocrinology 149:2090-2097 (Pubitemid 351574528)
28. Miyagawa S, Satoh Y, Haraguchi R, Suzuki K, Iguchi T, Taketo MM, Nakagata N, Matsumoto T, Takeyama K, Kato S, Yamada G 2009 Genetic interactions of the androgen and Wnt/β-catenin pathways for the masculinization of external genitalia. Mol Endocrinol 23:871-880
29. Huang CC, Yao HH 2010 Diverse functions of hedgehog signaling in formation and physiology of steroidogenic organs. Mol Reprod Dev 77:489-496
30. Yao HH, Whoriskey W, Capel B 2002 Desert hedgehog/patched 1 signaling specifies fetal Leydig cell fate in testis organogenesis. Genes Dev 16:1433-1440 (Pubitemid 34615095)
31. Welsh M, Saunders PT, Fisken M, Scott HM, Hutchison GR, Smith LB, Sharpe RM 2008 Identification in rats of a programming window for reproductive tract masculinization, disruption of which leads to hypospadias and cryptorchidism. J Clin Invest 118:1479-1490 (Pubitemid 351500441)
32. Wilson MJ 1983 Inhibition of development of both androgen-dependent and androgen-independent pigment cells in scrotal skin dermis of the rat by antiandrogen treatment during fetal growth. Endocrinology 112:321-325
33. Nishida H, Miyagawa S, Matsumaru D, Wada Y, Satoh Y, Ogino Y, Fukuda S, Iguchi T, Yamada G 2008 Gene expression analyses on embryonic external genitalia: identification of regulatory genes possibly involved in masculinization processes. Congenit Anom 48:63-67 (Pubitemid 351623876)
34. Yucel S, Liu W, Cordero D, Donjacour A, Cunha G, Baskin LS 2004 Anatomical studies of the fibroblast growth factor-10 mutant, sonic hedge hog mutant and androgen receptor mutant mouse genital tubercle. Adv Exp Med Biol 545:123-148 (Pubitemid 38580741)
35. Xie J, Murone M, Luoh SM, Ryan A, Gu Q, Zhang C, Bonifas JM, Lam CW, Hynes M, Goddard A, Rosenthal A, Epstein Jr EH, de Sauvage FJ 1998 Activating smoothened mutations in sporadic basal-cell carcinoma. Nature 391:90-92 (Pubitemid 28079221)
36. Barsoum IB, Bingham NC, Parker KL, Jorgensen JS, Yao HH 2009 Activation of the Hedgehog pathway in the mouse fetal ovary leads to ectopic appearance of fetal Leydig cells and female pseudohermaphroditism. Dev Biol 329:96-103
37. Miyagawa S, Moon A, Haraguchi R, Inoue C, Harada M, Nakahara C, Suzuki K, Matsumaru D, Kaneko T, Matsuo I, Yang L, Taketo MM, Iguchi T, Evans SM, Yamada G 2009 Dosage-dependent hedgehog signals integrated with Wnt/β-catenin signaling regulate external genitalia formation as an appendicular program. Development 136:3969-3978
38. Seifert AW, Zheng Z, Ormerod BK, Cohn MJ 2010 Sonic hedgehog controls growth of external genitalia by regulating cell cycle kinetics. Nat Commun 1:23
39. Huang L, Pu Y, Hu WY, Birch L, Luccio-Camelo D, Yamaguchi T, Prins GS 2009 The role of Wnt5a in prostate gland development. Dev Biol 328:188-199
40. Huang L, Pu Y, Alam S, Birch L, Prins GS 2005 The role of Fgf10 signaling in branching morphogenesis and gene expression of the rat prostate gland: lobe-specific suppression by neonatal estrogens. Dev Biol 278:396-414 (Pubitemid 40175038)
41. Grishina IB, Kim SY, Ferrara C, Makarenkova HP, Walden PD 2005 BMP7 inhibits branching morphogenesis in the prostate gland and interferes with notch signaling. Dev Biol 288:334-347 (Pubitemid 41790747)
42. Cook C, Vezina CM, Allgeier SH, Shaw A, Yu M, Peterson RE, Bushman W 2007 Noggin is required for normal lobe patterning and ductal budding in the mouse prostate. Dev Biol 312:217-230 (Pubitemid 350182443)
43. Lin C, Yin Y, Veith GM, Fisher AV, Long F, Ma L 2009 Temporal and spatial dissection of Shh signaling in genital tubercle development. Development 136:3959-3967
44. MoR, Kim JH, Zhang J, Chiang C, Hui CC, Kim PC 2001 Anorectal malformations caused by defects in sonic hedgehog signaling. Am J Pathol 159:765-774 (Pubitemid 32751104)
45. Seifert AW, Bouldin CM, Choi KS, Harfe BD, Cohn MJ 2009 Multiphasic and tissue-specific roles of sonic hedgehog in cloacal septation and external genitalia development. Development 136:3949-3957
46. Pu Y, Huang L, Birch L, Prins GS 2007 Androgen regulation of prostate morphoregulatory gene expression: Fgf10-dependent and -independent pathways. Endocrinology 148:1697-1706 (Pubitemid 46463894)
47. Pu Y, Huang L, Prins GS 2004 Sonic hedgehog-patched Gli signaling in the developing rat prostate gland: lobe-specific suppression by neonatal estrogens reduces ductal growth and branching. Dev Biol 273:257-275 (Pubitemid 39140902)
48. Lamm ML, Catbagan WS, Laciak RJ, Barnett DH, Hebner CM, Gaffield W, Walterhouse D, Iannaccone P, Bushman W 2002 Sonic hedgehog activates mesenchymal Gli1 expression during prostate ductal bud formation. Dev Biol 249:349-366
49. Podlasek CA, Barnett DH, Clemens JQ, Bak PM, Bushman W 1999 Prostate development requires sonic hedgehog expressed by the urogenital sinus epithelium. Dev Biol 209:28-39 (Pubitemid 29194310)
50. Barent RL, Nair SC, Carr DC, Ruan Y, Rimerman RA, Fulton J, Zhang Y, Smith DF 1998 Analysis of FKBP51/FKBP52 chimeras and mutants for Hsp90 binding and association with progesterone receptor complexes. Mol Endocrinol 12:342-354 (Pubitemid 30666265)
51. Febbo PG, Lowenberg M, Thorner AR, Brown M, Loda M, Golub TR 2005 Androgen mediated regulation and functional implications of fkbp51 expression in prostate cancer. J Urol 173:1772-1777 (Pubitemid 40524830)
52. Cheung-Flynn J, Prapapanich V, Cox MB, Riggs DL, Suarez-Quian C, Smith DF 2005 Physiological role for the cochaperone FKBP52 in androgen receptor signaling. Mol Endocrinol 19:1654-1666 (Pubitemid 41002993)
53. Clark AM, Garland KK, Russell LD 2000 Desert hedgehog (Dhh) gene is required in the mouse testis for formation of adult-type Leydig cells and normal development of peritubular cells and seminiferous tubules. Biol Reprod 63:1825-1838
54. Hu MC, Hsu NC, El Hadj NB, Pai CI, Chu HP, Wang CK, Chung BC 2002 Steroid deficiency syndromes in mice with targeted disruption of Cyp11a1. Mol Endocrinol 16:1943-1950
55. Shih MC, Hsu NC, Huang CC, Wu TS, Lai PY, Chung BC 2008 Mutation of mouse Cyp11a1 promoter caused tissue-specific reduction of gene expression and blunted stress response without affecting reproduction. Mol Endocrinol 22:915-923
56. Holmes NM, Miller WL, Baskin LS 2004 Lack of defects in androgen production in children with hypospadias. J Clin Endocrinol Metab 89:2811-2816 (Pubitemid 38766370)