Emerging roles for hedgehog-patched-Gli signal transduction in reproduction

Biology of Reproduction

Volumn 69, Issue 1, 2003, Pages 8-14

  Walterhouse, David O ^a   Lamm, Marilyn L G ^a   Villavicencio, Elisabeth ^a   Iannaccone, Philip M ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Developmental biology; Embryo; Mammary glands; Prostate; Testis

Indexed keywords

SEX HORMONE; SONIC HEDGEHOG PROTEIN;

ACCESSORY SEX GLAND; CELL DIFFERENTIATION; CELL PROLIFERATION; DROSOPHILA; EMBRYO DEVELOPMENT; EPITHELIUM; GENE TARGETING; GENETIC CONSERVATION; GONAD; MAMMARY GLAND; MESENCHYME; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROSTATE; PROTEIN EXPRESSION; REPRODUCTION; SHORT SURVEY; SIGNAL TRANSDUCTION; UTERUS;

ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; GENITALIA, FEMALE; GENITALIA, MALE; HEDGEHOG PROTEINS; MALE; MEMBRANE PROTEINS; ONCOGENE PROTEINS; PREGNANCY; RECEPTORS, CELL SURFACE; REPRODUCTION; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; VERTEBRATES;

ERINACEIDAE; MAMMALIA; VERTEBRATA;

EID: 0038452505     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.103.015941     Document Type: Short Survey

References (87)

1. Echelard Y, Epstein DJ, St-Jacques B, Shen L, Mohler J, McMahon JA, McMahon AP. Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 1993; 75:1417-1430.
2. Krauss S, Concordet JP, Ingham PW. A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell 1993; 75: 1431-1444.
3. Riddle RD, Johnson RL, Laufer E, Tabin C. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 1993; 75:1401-1416.
4. Roelink H, Augsburger A, Heemskerk J, Korzh V, Norlin S, Ruiz i Altaba A, Tanabe Y, Placzek M, Edlund T, Jessell TM, Dodd J. Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord. Cell 1994; 76:761-775.
5. Chang DT, Lopez A, von Kessler DP, Chiang C, Simandl BK, Zhao R, Seldin MF, Fallon JF, Beachy PA. Products, genetic linkage and limb patterning activity of a murine hedgehog gene. Development 1994; 120:3339-3353.
6. Odent S, Atti-Bitach T, Blayau M, Mathieu M, Aug J, Delezo de AL, Gall JY, Le Marec B, Munnich A, David V, Vekemans M. Expression of the sonic hedgehog (SHH) gene during early human development and phenotypic expression of new mutations causing holoprosencephaly. Hum Mol Genet 1999; 8:1683-1689.
7. Bitgood MJ, McMahon AP. Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev Biol 1995; 172:126-138.
8. Ingham PW, McMahon AP. Hedgehog signaling in animal development: paradigms and principles. Genes Dev 2001; 15:3059-3087.
9. Vortkamp A, Gessler M, Grzeschik KH. GLI3 zinc-finger gene interrupted by translocations in Greig syndrome families. Nature 1991; 352:539-540.
10. Belloni E, Muenke M, Roessler E, Traverso G, Siegel-Bartelt J, Frumkin A, Mitchell HF, Donis-Keller H, Helms C, Hing AV, Heng HH, Koop B, Martindale D, Rommens JM, Tsui LC, Scherer SW. Identification of sonic hedgehog as a candidate gene responsible for holoprosencephaly. Nat Genet 1996; 14:353-356.
11. Hahn H, Wicking C, Zaphiropoulous PG, Gailani MR, Shanley S, Chidambaram A, Vorechovsky I, Holmberg E, Unden AB, Gillies S, Negus K, Smyth I, Pressman C, Leffell DJ, Gerrard B, Goldstein AM, Dean M, Toftgard R, Chenevix-Trench G, Wainwright B, Bale AE. Mutations of the human homolog of Drosophila patched in the nevoid basal cell carcinoma syndrome. Cell 1996; 85:841-851.
12. Johnson RL, Rothman AL, Xie J, Goodrich LV, Bare JW, Bonifas JM, Quinn AG, Myers RM, Cox DR, Epstein EH Jr, Scott MP. Human homolog of patched, a candidate gene for the basal cell nevus syndrome. Science 1996; 272:1668-1671.
13. Roessler E, Belloni E, Gaudenz K, Jay P, Berta P, Scherer SW, Tsui LC, Muenke M. Mutations in the human sonic hedgehog gene cause holoprosencephaly. Nat Genet 1996; 14:357-360.
14. Kang S, Graham JM Jr, Olney AH, Biesecker LG. GLI3 frameshift mutations cause autosomal dominant Pallister-Hall syndrome. Nat Genet 1997; 15:266-268.
15. Radhakrishna U, Bornholdt D, Scott HS, Patel UC, Rossier C, Engel H, Bottani A, Chandal D, Blouin JL, Solanki JV, Grzeschik KH, Antonarakis SE. The phenotypic spectrum of GLI3 morphopathies includes autosomal dominant preaxial polydactyly type-IV and postaxial polydactyly type-A/B: no phenotype prediction from the position of GLI3 mutations. Am J Hum Genet 1999; 65:645-655.
16. Dahmane N, Lee J, Robins P, Heller P, Ruiz i Altaba A. Activation of the transcription factor Gli1 and the sonic hedgehog signalling pathway in skin tumours. Nature 1997; 389:876-881.
17. Goodrich LV, Milenkovic L, Higgins KM, Scott MP. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 1997; 277:1109-1113.
18. Hahn H, Wojnowski L, Zimmer AM, Hall J, Miller G, Zimmer A. Rhabdomyosarcomas and radiation hypersensitivity in a mouse model of Gorlin syndrome. Nat Med 1998; 4:619-622.
19. Reifenberger J, Wolter M, Weber RG, Megahed M, Ruzicka T, Lichter P, Reifenberger G. Missense mutations in SMOH in sporadic basal cell carcinomas of the skin and primitive neuroectodermal tumors of the central nervous system. Cancer Res 1998; 58:1798-1803.
20. Stein U, Eder C, Karsten U, Haensch W, Walther W, Schlag PM. GLI gene expression in bone and soft tissue sarcomas of adult patients correlates with tumor grade. Cancer Res 1999; 59:1890-1895.
21. Xie J, Murone M, Luoh SM, Ryan A, Gu Q, Zhang C, Bonifas JM, Lam CW, Hynes M, Goddard A, Rosenthal A, Epstein EH Jr, de Sauvage FJ. Activating smoothened mutations in sporadic basal-cell carcinoma. Nature 1998; 391:90-92.
22. Nusslein-Volhard C, Wieschaus E. Mutations affecting segment number and polarity in Drosophila. Nature 1980; 287:795-801.
23. Mohler J. Requirements for hedgehog, a segmental polarity gene, in patterning larval and adult cuticle of Drosophila. Genetics 1988; 120: 1061-1072.
24. Tabata T, Kornberg TB. Hedgehog is a signaling protein with a key role in patterning Drosophila imaginal discs. Cell 1994; 76:89-102.
25. Porter JA, Young KE, Beachy PA. Cholesterol modification of hedgehog signaling proteins in animal development. Science 1996; 274: 255-259.
26. Pepinsky RB, Zeng C, Wen D, Rayhorn P, Baker DP, Williams KP, Bixler SA, Ambrose CM, Garber EA, Miatkowski K, Taylor FR, Wang EA, Galdes A. Identification of a palmitic acid-modified form of human sonic hedgehog. J Biol Chem 1998; 273:14037-14045.
27. Chamoun Z, Mann RK, Nellen D, von Kessler DP, Bellotto M, Beachy PA, Basler K. Skinny hedgehog, an acyltransferase required for palmitoylation and activity of the hedgehog signal. Science 2001; 293: 2080-2084.
28. Denef N, Neubuser D, Perez L, Cohen SM. Hedgehog induces opposite changes in turnover and subcellular localization of patched and smoothened. Cell 2000; 102:521-531.
29. Ramirez-Weber FA, Casso DJ, Aza-Blanc P, Tabata T, Kornberg TB. Hedgehog signal transduction in the posterior compartment of the Drosophila wing imaginal disc. Mol Cell 2000; 6:479-485.
30. Sisson JC, Ho KS, Suyama K, Scott MP. Costal2, a novel kinesin-related protein in the hedgehog signaling pathway. Cell 1997; 90:235-245.
31. Robbins DJ, Nybakken KE, Kobayashi R, Sisson JC, Bishop JM, Therond PP. Hedgehog elicits signal transduction by means of a large complex containing the kinesin-related protein costal2. Cell 1997; 90: 225-234.
32. Monnier V, Dussillol F, Alves G, Lamour-Isnard C, Plessis A. Suppressor of fused links fused and cubitus interruptus on the hedgehog signalling pathway. Curr Biol 1998; 8:583-586.
33. Li W, Ohlmeyer JT, Lane ME, Kalderon D. Function of protein kinase A in hedgehog signal transduction and Drosophila imaginal disc development. Cell 1995; 80:553-562.
34. Aza-Blanc P, Ramirez-Weber FA, Laget MP, Schwartz C, Kornberg TB. Proteolysis that is inhibited by hedgehog targets cubitus interruptus protein to the nucleus and converts it to a repressor. Cell 1997; 89:1043-1053.
35. Chen Y, Gallaher N, Goodman RH, Smolik SM. Protein kinase A directly regulates the activity and proteolysis of cubitus interruptus. Proc Natl Acad Sci U S A 1998; 95:2349-2354.
36. Méthot N, Basler K. Hedgehog controls limb development by regulating the activities of distinct transcriptional activator and repressor forms of cubitus interruptus. Cell 1999; 96:819-831.
37. Alexandre C, Jacinto A, Ingham PW. Transcriptional activation of hedgehog target genes in Drosophila is mediated directly by the cubitus interruptus protein, a member of the GLI family of zinc finger DNA-binding proteins. Genes Dev 1996; 10:2003-2013.
38. Akimaru H, Chen Y, Dai P, Hou DX, Nonaka M, Smolik SM, Armstrong S, Goodman RH, Ishii S. Drosophila CBP is a co-activator of cubitus interruptus in hedgehog signalling. Nature 1997; 386:735-738.
39. Ding Q, Fukami S, Meng X, Nishizaki Y, Zhang X, Sasaki H, Dlugosza A, Nakafuku M, Hui C. Mouse suppressor of fused is a negative regulator of sonic hedgehog signaling and alters the subcellular distribution of Gli1. Curr Biol 1999; 9:1119-1122.
40. Pearse RV, Collier LS, Scott MP, Tabin CJ. Vertebrate homologs of Drosophila suppressor of fused interact with the Gli family of transcriptional regulators. Dev Biol 1999; 212:323-336.
41. Stone DM, Murone M, Luoh SM, Ye W, Armanini MP, Gurney A, Phillips H, Brush J, Goddard A, de Sauvage FJ, Rosenthal A. Characterization of the human suppressor of fused, a negative regulator of the zinc-finger transcription factor Gli. J Cell Sci 1999; 112:4437-4448.
42. Murone M, Luoh SM, Stone D, Li W, Gurney A, Armanini M, Grey C, Rosenthal A, de Sauvage FJ. Gli regulation by the opposing activities of fused and suppressor of fused. Nat Cell Biol 2000; 2:310-312.
43. Bitgood MJ, Shen L, McMahon AP. Sertoli cell signaling by desert hedgehog regulates the male germline. Curr Biol 1996; 6:298-304.
44. Carpenter D, Stone DM, Brush J, Ryan A, Armanini M, Frantz G, Rosenthal A, DeSauvage FJ. Characterization of two patched receptors for the vertebrate hedgehog protein family. Proc Natl Acad Sci U S A 1998; 95:13630-13634.
45. Marigo V, Johnson R, Vortkamp A, Tabin C. Sonic hedgehog differentially regulates expression of GLI and GLI3 during limb development. Dev Biol 1996; 180:273-283.
46. Dai P, Akimaru H, Tanaka Y, Maekawa T, Nakafuku M, Ishii S. Sonic hedgehog-induced activation of the Gli1 promoter is mediated by Gli3. J Biol Chem 1999; 274:8143-8152.
47. Sasaki H, Nishizaki Y, Hui CC, Nakafuku M, Kondoh H. Regulation of Gli2 and Gli3 activities by an amino-terminal repression domain: implication of Gli2 and Gli3 as primary mediators of Shh signaling. Development 1999; 126:3915-3924.
48. Ruiz i Altaba A. Gli proteins encode context-dependent positive and negative functions: implications for development and disease. Development 1999; 126:3205-3216.
49. Aza-Blanc P, Lin HY, Ruiz i Altaba A, Kornberg TB. Expression of the vertebrate Gli proteins in Drosophila reveals a distribution of activator and repressor activities. Development 2000; 127:4293-4301.
50. Yoon JW, Liu CZ, Yang JT, Swart R, Iannaccone P, Walterhouse D. GLI activates transcription through a herpes simplex viral protein 16-like activation domain. J Biol Chem 1998; 273:3496-3501.
51. Bellusci S, Furuta Y, Rush MG, Henderson R, Winnier G, Hogan BLM. Involvement of sonic hedgehog (Shh) in mouse embryonic lung growth and morphogenesis. Development 1997; 124:53-63.
52. Grindley JC, Bellusci S, Perkins D, Hogan BLM. Evidence for the involvement of the Gli gene family in embryonic mouse lung development. Dev Biol 1997; 188:337-348.
53. Yang JT, Liu CZ, Villavicencio EH, Yoon JW, Walterhouse D, Iannaccone PM. Expression of human GLI in mice results in failure to thrive, early death, and patchy Hirschsprung-like gastrointestinal dilatation. Mol Med 1997; 3:826-835.
54. Hardcastle Z, Mo R, Hui CC, Sharpe PT. The Shh signalling pathway in tooth development: defects in Gli2 and Gli3 mutants. Development 1998; 125:2803-2811.
55. Motoyama J, Liu J, Mo R, Ding Q, Post M, Hui CC. Essential function of GLI2 and GLI3 in the formation of lung, trachea and oesophagus. Nat Genet 1998; 20:54-57.
56. Motoyama J, Heng H, Crackower MA, Takabatake T, Takeshima K, Tsui LC, Hui C. Overlapping and non-overlapping Ptch2 expression with Shh during mouse embryogenesis. Mech Dev 1998; 78:81-84.
57. Pepicelli CV, Lewis PM, McMahon AP. Sonic hedgehog regulates branching morphogenesis in the mammalian lung. Curr Biol 1998; 8: 1083-1086.
58. Chiang C, Swan RZ, Grachtchouk M, Bolinger M, Litingtung Y, Robertson EK, Cooper MK, Gaffield W, Westphal H, Beachy PH, Dlugosz AA. Essential role for sonic hedgehog during hair follicle morphogenesis. Dev Biol 1999; 205:1-9.
59. Dassule HR, Lewis P, Bei M, Maas R, McMahon AP. Sonic hedgehog regulates growth and morphogenesis of the tooth. Development 2000; 127:4775-4785.
60. Sukegawa A, Narita T, Kameda T, Saitoh K, Nohno T, Iba H, Yasugi S, Fukuda K. The concentric structure of the developing gut is regulated by sonic hedgehog derived from endodermal epithelium. Development 2000; 127:1971-1980.
61. Ramalho-Santos M, Melton DA, McMahon AP. Hedgehog signals regulate multiple aspects of gastrointestinal development. Development 2000; 127:2673-2772.
62. Summersgill B, Goker H, Weber-Hall S, Huddart R, Horwich A, Shipley J. Molecular cytogenetic analysis of adult testicular germ cell tumours and identification of regions of consensus copy number change. Br J Cancer 1998; 77:305-313.
63. Persengiev SP, Kondova II, Millette CF, Kilpatrick DL. Gli family members are differentially expressed during the mitotic phase of spermatogenesis. Oncogene 1997; 14:2259-2264.
64. Kroft TL, Patterson J, Yoon JW, Doglio L, Walterhouse DO, Iannaccone PM, Goldberg E. GLI1 localization in the germinal epithelial cells alternates between cytoplasm and nucleus; upregulation in transgenic mice blocks spermatogenesis in pachytene. Biol Reprod 2001; 65:1663-1671.
65. Walterhouse D, Ahmed M, Slusarski D, Kalamaras J, Boucher D, Holmgren R, Iannaccone P. gli, A zinc finger transcription factor and oncogene is expressed during normal mouse development. Dev Dyn 1993; 196:91-102.
66. Yao HH, Capel B. Disruption of testis cords by cyclopamine or forskolin reveals independent cellular pathways in testis organogenesis. Dev Biol 2002; 246:356-365.
67. Clark AM, Garland KK, Russell LD. 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 2000; 63:1825-1838.
68. Pierucci-Alves F, Clark AM, Russell LD. A developmental study of the desert hedgehog-null mouse testis. Biol Reprod 2001; 65:1392-1402.
69. Yao HH, Whoriskey W, Capel B. Desert hedgehog/patched 1 signaling specifies fetal Leydig cell fate in testis organogenesis. Genes Dev 2002; 16:1433-1440.
70. Incardona JP, Gaffield W, Kapur RP, Roelink H. The teratogenic veratrum alkaloid cyclopamine inhibits sonic hedgehog signal transduction. Development 1998; 125:3553-3562.
71. Cooper MK, Porter JA, Young KE, Beachy PA. Teratogen-mediated inhibition of target tissue response to Shh signaling. Science 1998; 280:1603-1607.
72. Taipale J, Chen JK, Cooper JK, Wang B, Mann RK, Milenkovic L, Scott MP, Beachy PA. Effects of oncogenic mutations in smoothened and patched can be reversed by cyclopamine. Nature 2000; 406:1005-1009.
73. Cunha GR, Donjacour AA, Cooke PS, Mee S, Bigsby RM, Higgins SJ, Sugimura Y. The endocrinology and developmental biology of the prostate. Endocr Rev 1987; 8:338-362.
74. Cunha GR, Alarid ET, Turner T, Donjacour AA, Boutin EL, Foster BA. Normal and abnormal development of the male urogenital tract. Role of androgens, mesenchymal-epithelial interactions, and growth factors. J Androl 1992; 13:465-475.
75. Podlasek CA, Barnett DH, Clemens JQ, Bak PM, Bushman W. Prostate development requires sonic hedgehog expressed by the urogenital sinus epithelium. Dev Biol 1999; 209:28-39.
76. Lamm M, Catbagan W, Laciak R, Barnett D, Hebner C, Gaffield W, Walterhouse D, Iannaccone P, Bushman W. Sonic hedgehog activates mesenchymal Gli1 expression during prostate ductal bud formation. Dev Biol 2002; 249:349-366.
77. Forbes AJ, Lin H, Ingham PW, Spradling AC. Hedgehog is required for the proliferation and specification of ovarian somatic cells prior to egg chamber formation in Drosophila. Development 1996; 122:1125-1135.
78. Xie T, Spradling AC. Decapentaplegic is essential for the maintenance and division of germline stem cells in the Drosophila ovary. Cell 1998; 94:251-260.
79. Zhang Y, Kalderon D. Regulation of cell proliferation and patterning in Drosophila oogenesis by hedgehog signaling. Development 2000; 127:2165-2176.
80. Lewis MT, Ross S, Strickland PH, Sugnet CW, Jimenez E, Scott MP, Daniel CW. Defects in mouse mammary gland development caused by conditional haploinsufficiency of patched-1. Development 1999; 126:5181-5183.
81. Lewis MT, Ross S, Strickland PA, Sugnet CW, Jimenez E, Hui CC, Daniel CW. The Gli2 transcription factor is required for normal mouse mammary gland development. Dev Biol 2001; 238:133-144.
82. Stewart CL, Cullinan EB. Preimplantation development of the mammalian embryo and its regulation by growth factors. Dev Genet 1997; 21:91-101.
83. Carson DD, Bagchi I, Dey SK, Enders AC, Fazleabas AT, Lessey BA, Yoshinaga K. Embryo implantation. Dev Biol 2000; 223:217-237.
84. Paria BC, Ma W, Tan J, Raja S, Das SK, Dey SK, Hogan BLM. Cellular and molecular responses of the uterus to embryo implantation can be elicited by locally applied growth factors. Proc Natl Acad Sci U S A 2001; 98:1047-1052.
85. Matsumoto H, Zhao X, Das SK, Hogan BLM, Dey SK. Indian hedgehog as a progesterone-responsive factor mediating epithelial-mesenchymal interactions in the mouse uterus. Dev Biol 2002; 245:280-290.
86. Takamoto N, Zhao B, Tsai SY, Demayo FJ. Identification of Indian hedgehog as a progesterone-responsive gene in the murine uterus. Mol Endocrinol 2002; 16:2338-2348.
87. Tan J, Paria BC, Dey SK, Das SK. Differential uterine expression of estrogen and progesterone receptors correlates with uterine preparation for implantation and decidualization in the mouse. Endocrinology 1999; 140:5310-5321.