Retinoic acid induces prostatic bud formation

Developmental Dynamics

Volumn 237, Issue 5, 2008, Pages 1321-1333

  Vezina, Chad M ^a   Allgeier, Sarah H ^a   Fritz, Wayne A ^a   Moore, Robert W ^a   Strerath, Michael ^a   Bushman, Wade ^a,b   Peterson, Richard E ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

BMP4; Bud formation; Development; Mouse; Prostate; Retinoic acid; SHH; Urogenital sinus

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; NOGGIN; RETINOIC ACID; SONIC HEDGEHOG PROTEIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; FETUS; MALE; METABOLISM; MORPHOGENESIS; MOUSE; NONHUMAN; ORGAN CULTURE; ORGANOGENESIS; PRIORITY JOURNAL; PROSTATE; PROTEIN EXPRESSION; RECEPTOR GENE; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; UROGENITAL SINUS;

ALDEHYDE OXIDOREDUCTASES; ANIMALS; ANTINEOPLASTIC AGENTS; BONE MORPHOGENETIC PROTEINS; CARRIER PROTEINS; GENE EXPRESSION REGULATION; HEDGEHOG PROTEINS; ISOENZYMES; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MORPHOGENESIS; PROSTATE; RECEPTORS, RETINOIC ACID; RETINOID X RECEPTORS; SIGNAL TRANSDUCTION; TISSUE CULTURE TECHNIQUES; TRETINOIN;

ERINACEIDAE;

EID: 43449134690     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.21526     Document Type: Article

References (88)

1. Aboseif SR, Dahiya R, Narayan P, Cunha GR. 1997. Effect of retinoic acid on prostatic development. Prostate 31:161-167.
2. Abu-Abed S, Dolle P, Metzger D, Beckett B, Chambon P, Petkovich M. 2001. The retinoic acid-metabolizing enzyme, CYP26A1, is essential for normal hindbrain patterning, vertebral identity, and development of posterior structures. Genes Dev 15:226-240.
3. Akimenko MA, Ekker M. 1995. Anterior duplication of the sonic hedgehog expression pattern in the pectoral fin buds of zebrafish treated with retinoic acid. Dev Biol 170:243-247.
4. Almahbobi G, Hedwards S, Fricout G, Jeulin D, Bertram JF, Risbridger GP. 2005. Computer-based detection of neonatal changes to branching morphogenesis reveals different mechanisms of and predicts prostate enlargement in mice haplo-insufficient for bone morphogenetic protein 4. J Pathol 206:52-61.
5. Amthor H, Christ B, Patel K. 1999. A molecular mechanism enabling continuous embryonic muscle growth: a balance between proliferation and differentiation. Development 126:1041-1053.
6. Berman DM, Desai N, Wang X, Karhadkar SS, Reynon M, Abate-Shen C, Beachy PA, Shen MM. 2004. Roles for Hedgehog signaling in androgen production and prostate ductal morphogenesis. Dev Biol 267:387-398.
7. Chen J, Carney SA, Peterson RE, Heideman W. 2008. Retinoic acid induced cardiotoxicity in the zebrafish embryo: microarray studies identify Nr2f5 as a critical target. Physiol Genomics, in press.
8. Cheng TC, Wallace MC, Merlie JP, Olson EN. 1993. Separable regulatory elements governing myogenin transcription in mouse embryogenesis. Science 261:215-218.
9. Clagett-Dame M, DeLuca HF. 2002. The role of vitamin A in mammalian reproduction and embryonic development. Annu Rev Nutr 22:347-381.
10. 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.
11. Cooney AJ, Leng X, Tsai SY, O'Malley BW, Tsai MJ. 1993. Multiple mechanisms of chicken ovalbumin upstream promoter transcription factor-dependent repression of transactivation by the vitamin D, thyroid hormone, and retinoic acid receptors. J Biol Chem 268:4152-4160.
12. Cunha GR, Lung B. 1978. The possible influence of temporal factors in androgenic responsiveness of urogenital tissue recombinants from wild-type and androgen-insensitive (Tfm) mice. J Exp Zool 205:181-193.
13. Cunha GR, Donjacour AA, Cooke PS, Mee S, Bigsby RM, Higgins SJ, Sugimura Y. 1987. The endocrinology and developmental biology of the prostate. Endocr Rev 8:338-362.
14. Desai TJ, Malpel S, Flentke GR, Smith SM, Cardoso WV. 2004. Retinoic acid selectively regulates Fgf10 expression and maintains cell identity in the prospective lung field of the developing foregut. Dev Biol 273:402-415.
15. Desai TJ, Chen F, Lu J, Qian J, Niederreither K, Dolle P, Chambon P, Cardoso WV. 2006. Distinct roles for retinoic acid receptors alpha and beta in early lung morphogenesis. Dev Biol 291:12-24.
16. Diez del Corral R, Olivera-Martinez I, Goriely A, Gale E, Maden M, Storey K. 2003. Opposing FGF and retinoid pathways control ventral neural pattern, neuronal differentiation, and segmentation during body axis extension. Neuron 40:65-79.
17. Doles J, Cook C, Shi X, Valosky J, Lipinski R, Bushman W. 2006. Functional compensation in hedgehog signaling during mouse prostate development. Dev Biol 295:13-25.
18. Dolle P, Ruberte E, Leroy P, Morriss-Kay G, Chambon P. 1990. Retinoic acid receptors and cellular retinoid binding proteins. I. A systematic study of their differential pattern of transcription during mouse organogenesis. Development 110:1133-1151.
19. Fliniaux I, Viallet JP, Dhouailly D. 2004. Signaling dynamics of feather tract formation from the chick somatopleure. Development 131:3955-3966.
20. Freestone SH, Marker P, Grace OC, Tomlinson DC, Cunha GR, Harnden P, Thomson AA. 2003. Sonic hedgehog regulates prostatic growth and epithelial differentiation. Dev Biol 264:352-362.
21. Galdones E, Lohnes D, Hales BF. 2006. Role of retinoic acid receptors alpha1 and gamma in the response of murine limbs to retinol in vitro. Birth Defects Res A Clin Mol Teratol 76:39-45.
22. Ghyselinck NB, Dupe V, Dierich A, Messaddeq N, Garnier JM, Rochette-Egly C, Chambon P, Mark M. 1997. Role of the retinoic acid receptor beta (RARbeta) during mouse development. Int J Dev Biol 41:425-447.
23. Goldstein JL, Wilson JD. 1975. Genetic and hormonal control of male sexual differentiation. J Cell Physiol 85:365-377.
24. Grandel H, Lun K, Rauch GJ, Rhinn M, Piotrowski T, Houart C, Sordino P, Kuchler AM, Schulte-Merker S, Geisler R, Holder N, Wilson SW, Brand M. 2002. Retinoic acid signalling in the zebrafish embryo is necessary during pre-segmentation stages to pattern the anterior-posterior axis of the CNS and to induce a pectoral fin bud. Development 129:2851-2865.
25. 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.
26. Gulacsi A, Lillien L. 2003. Sonic hedgehog and bone morphogenetic protein regulate interneuron development from dorsal telencephalic progenitors in vitro. J Neurosci 23:9862-9872.
27. Gyftopoulos K, Perimenis P, Sotiropoulou-Bonikou G, Sakellaropoulos G, Varakis I, Barbalias GA. 2000. Immunohistochemical detection of retinoic acid receptor-alpha in prostate carcinoma: correlation with proliferative activity and tumor grade. Int Urol Nephrol 32:263-269.
28. Hayashi N, Cunha GR, Parker M. 1993. Permissive and instructive induction of adult rodent prostatic epithelium by heterotypic urogenital sinus mesenchyme. Epithelial Cell Biol 2:66-78.
29. Hayes C, Morriss-Kay GM. 2001. Retinoic acid specifically downregulates Fgf4 and inhibits posterior cell proliferation in the developing mouse autopod. J Anat 198:561-568.
30. Helms J, Thaller C, Eichele G. 1994. Relationship between retinoic acid and sonic hedgehog, two polarizing signals in the chick wing bud. Development 120:3267-3274.
31. Horton C, Maden M. 1995. Endogenous distribution of retinoids during normal development and teratogenesis in the mouse embryo. Dev Dyn 202:312-323.
32. Huang HF, Li MT, Von Hagen S, Zhang YF, Irwin RJ. 1997. Androgen modulation of the messenger ribonucleic acid of retinoic acid receptors in the prostate, seminal vesicles, and kidney in the rat. Endocrinology 138:553-559.
33. Huang J, Powell WC, Khodavirdi AC, Wu J, Makita T, Cardiff RD, Cohen MB, Sucov HM, Roy-Burman P. 2002. Prostatic intraepithelial neoplasia in mice with conditional disruption of the retinoid X receptor alpha allele in the prostate epithelium. Cancer Res 62:4812-4819.
34. Kane MA, Chen N, Sparks S, Napoli JL. 2005. Quantification of endogenous retinoic acid in limited biological samples by LC/MS/MS. Biochem J 388:363-369.
35. Kronmiller JE, Nguyen T, Berndt W. 1995. Instruction by retinoic acid of incisor morphology in the mouse embryonic mandible. Arch Oral Biol 40:589-595.
36. Lambrot R, Coffigny H, Pairault C, Donnadieu AC, Frydman R, Habert R, Rouiller-Fabre V. 2006. Use of organ culture to study the human fetal testis development: effect of retinoic acid. J Clin Endocrinol Metab 91:2696-2703.
37. Lamm ML, Podlasek CA, Barnett DH, Lee J, Clemens JQ, Hebner CM, Bushman W. 2001. Mesenchymal factor bone morphogenetic protein 4 restricts ductal budding and branching morphogenesis in the developing prostate. Dev Biol 232:301-314.
38. 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.
39. Lasnitzki I, Goodman DS. 1974. Inhibition of the effects of methylcholanthrene on mouse prostate in organ culture by vitamin A and its analogs. Cancer Res 34:1564-1571.
40. Lasnitzki I, Mizuno T. 1980. Prostatic induction: interaction of epithelium and mesenchyme from normal wild-type mice and androgen-insensitive mice with testicular feminization. J Endocrinol 85:423-428.
41. Lateef H, Stevens MJ, Varani J. 2004. All-trans-retinoic acid suppresses matrix metalloproteinase activity and increases collagen synthesis in diabetic human skin in organ culture. Am J Pathol 165:167-174.
42. Lee CT, Li L, Takamoto N, Martin JF, Demayo FJ, Tsai MJ, Tsai SY. 2004. The nuclear orphan receptor COUP-TFII is required for limb and skeletal muscle development. Mol Cell Biol 24:10835-10843.
43. Lin B, Chen GQ, Xiao D, Kolluri SK, Cao X, Su H, Zhang XK. 2000. Orphan receptor COUP-TF is required for induction of retinoic acid receptor beta, growth inhibition, and apoptosis by retinoic acid in cancer cells. Mol Cell Biol 20:957-970.
44. Lin TM, Rasmussen NT, Moore RW, Albrecht RM, Peterson RE. 2003. Region-specific inhibition of prostatic epithelial bud formation in the urogenital sinus of C57BL/6 mice exposed in utero to 2,3,7,8- tetrachlorodibenzo-p-dioxin. Toxicol Sci 76:171-181.
45. Livera G, Rouiller-Fabre V, Durand P, Habert R. 2000. Multiple effects of retinoids on the development of sertoli, germ, and leydig cells of fetal and neonatal rat testis in culture. Biol Reprod 62:1303-1314.
46. Livera G, Pairault C, Lambrot R, Lelievre-Pegorier M, Saez JM, Habert R, Rouiller-Fabre V. 2004. Retinoid-sensitive steps in steroidogenesis in fetal and neonatal rat testes: in vitro and in vivo studies. Biol Reprod 70:1814-1821.
47. Lohnes D, Kastner P, Dierich A, Mark M, LeMeur M, Chambon P. 1993. Function of retinoic acid receptor gamma in the mouse. Cell 73:643-658.
48. Luo J, Sucov HM, Bader JA, Evans RM, Giguere V. 1996. Compound mutants for retinoic acid receptor (RAR) beta and RAR alpha 1 reveal developmental functions for multiple RAR beta isoforms. Mech Dev 55:33-44.
49. Maden M. 2000. The role of retinoic acid in embryonic and post-embryonic development. Proc Nutr Soc 59:65-73.
50. Martin M, Gallego-Llamas J, Ribes V, Kedinger M, Niederreither K, Chambon P, Dolle P, Gradwohl G. 2005. Dorsal pancreas agenesis in retinoic acid-deficient Raldh2 mutant mice. Dev Biol 284:399-411.
51. McCaffery P, Lee MO, Wagner MA, Sladek NE, Drager UC. 1992. Asymmetrical retinoic acid synthesis in the dorsoventral axis of the retina. Development 115:371-382.
52. McCaffery P, Wagner E, O'Neil J, Petkovich M, Drager UC. 1999. Dorsal and ventral retinal territories defined by retinoic acid synthesis, break-down and nuclear receptor expression. Mech Dev 82:119-130.
53. Mic FA, Haselbeck RJ, Cuenca AE, Duester G. 2002. Novel retinoic acid generating activities in the neural tube and heart identified by conditional rescue of Raldh2 null mutant mice. Development 129:2271-2282.
54. Mollard R, Viville S, Ward SJ, Decimo D, Chambon P, Dolle P. 2000. Tissue-specific expression of retinoic acid receptor isoform transcripts in the mouse embryo. Mech Dev 94:223-232.
55. Niederreither K, Subbarayan V, Dolle P, Chambon P. 1999. Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat Genet 21:444-448.
56. Ohsaki K, Osumi N, Nakamura S. 2002. Altered whisker patterns induced by ectopic expression of Shh are topographically represented by barrels. Brain Res Dev Brain Res 137:159-170.
57. Pecorino LT, Brockes JP, Entwistle A. 1996. Semi-automated positional analysis using laser scanning microscopy of cells transfected in a regenerating newt limb. J Histochem Cytochem 44:559-569.
58. Plant MR, MacDonald ME, Grad LI, Ritchie SJ, Richman JM. 2000. Locally released retinoic acid repatterns the first branchial arch cartilages in vivo. Dev Biol 222:12-26.
59. Podlasek CA, Duboule D, Bushman W. 1997. Male accessory sex organ morphogenesis is altered by loss of function of Hoxd-13. Dev Dyn 208:454-465.
60. 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.
61. Prins GS, Chang WY, Wang Y, van Breemen RB. 2002. Retinoic acid receptors and retinoids are up-regulated in the developing and adult rat prostate by neonatal estrogen exposure. Endocrinology 143:3628-3640.
62. Richter F, Huang HF, Li MT, Danielpour D, Wang SL, Irwin RJ Jr. 1999. Retinoid and androgen regulation of cell growth, epidermal growth factor and retinoic acid receptors in normal and carcinoma rat prostate cells. Mol Cell Endocrinol 153:29-38.
63. Richter F, Joyce A, Fromowitz F, Wang S, Watson J, Watson R, Irwin RJ Jr, Huang HF. 2002. Immunohistochemical localization of the retinoic acid receptors in human prostate. J Androl 23:830-838.
64. Robens JF. 1970. Teratogenic effects of hypervitaminosis A in the hamster and the guinea pig. Toxicol Appl Pharmacol 16:88-99.
65. Rossant J, Zirngibl R, Cado D, Shago M, Giguere V. 1991. Expression of a retinoic acid response element-hsplacZ transgene defines specific domains of transcriptional activity during mouse embryogenesis. Genes Dev 5:1333-1344.
66. Saito M, Mizuno T. 1997. Prostatic bud induction by brief treatment with growth factors. C R Seances Soc Biol Fil 191:261-265.
67. Sasagawa S, Takabatake T, Takabatake Y, Muramatsu T, Takeshima K. 2002. Axes establishment during eye morphogenesis in Xenopus by coordinate and antagonistic actions of BMP4, Shh, and RA. Genesis 33:86-96.
68. Satre MA, Kochhar DM. 1989. Elevations in the endogenous levels of the putative morphogen retinoic acid in embryonic mouse limb-buds associated with limb dysmorphogenesis. Dev Biol 133:529-536.
69. Seo R, McGuire M, Chung M, Bushman W. 1997. Inhibition of prostate ductal morphogenesis by retinoic acid. J Urol 158:931-935.
70. Tang LS, Alger HM, Lin F, Pereira FA. 2005. Dynamic expression of COUP-TFI and COUP-TFII during development and functional maturation of the mouse inner ear. Gene Expr Patterns 5:587-592.
71. Thaller C, Eichele G. 1987. Identification and spatial distribution of retinoids in the developing chick limb bud. Nature 327:625-628.
72. Thompson DL, Gerlach-Bank LM, Barald KF, Koenig RJ. 2003. Retinoic acid repression of bone morphogenetic protein 4 in inner ear development. Mol Cell Biol 23:2277-2286.
73. Thomson AA, Cunha GR. 1999. Prostatic growth and development are regulated by FGF10. Development 126:3693-3701.
74. Tickle C. 1991. Retinoic acid and chick limb bud development. Dev (Suppl) 1:113-121.
75. Tickle C, Lee J, Eichele G. 1985. A quantitative analysis of the effect of all-trans-retinoic acid on the pattern of chick wing development. Dev Biol 109:82-95.
76. Timms BG, Lee CW, Aumuller G, Seitz J. 1995. Instructive induction of prostate growth and differentiation by a defined urogenital sinus mesenchyme. Microsc Res Tech 30:319-332.
77. Tsai SY, Tsai MJ. 1997. Chick ovalbumin upstream promoter-transcription factors (COUP-TFs): coming of age. Endocr Rev 18:229-240.
78. Vernet N, Dennefeld C, Rochette-Egly C, Oulad-Abdelghani M, Chambon P, Ghyselinck NB, Mark M. 2006. Retinoic acid metabolism and signaling pathways in the adult and developing mouse testis. Endocrinology 147:96-110.
79. Vilar J, Gilbert T, Moreau E, Merlet-Benichou C. 1996. Metanephros organogenesis is highly stimulated by vitamin A derivatives in organ culture. Kidney Int 49:1478-1487.
80. vom Saal FS, Timms BG, Montano MM, Palanza P, Thayer KA, Nagel SC, Dhar MD, Ganjam VK, Parmigiani S, Welshons WV. 1997. Prostate enlargement in mice due to fetal exposure to low doses of estradiol or diethylstilbestrol and opposite effects at high doses. Proc Natl Acad Sci USA 94:2056-2061.
81. Wang Z, Dolle P, Cardoso WV, Niederreither K. 2006. Retinoic acid regulates morphogenesis and patterning of posterior foregut derivatives. Dev Biol 297:433-445.
82. Warot X, Fromental-Ramain C, Fraulob V, Chambon P, Dolle P. 1997. Gene dosage-dependent effects of the Hoxa-13 and Hoxd-13 mutations on morphogenesis of the terminal parts of the digestive and urogenital tracts. Development 124:4781-4791.
83. Wilson JD, Warkany J. 1948. Malformations in the genitor-urinary tract induced by maternal vitamin A deficiency in the rat. Am J Anat 88:357-407.
84. Wilson JG, Roth CB, Warkany J. 1953. An analysis of the syndrome of malformations induced by maternal vitamin A deficiency. Effects of restoration of vitamin A at various times during gestation. Am J Anat 92:189-217.
85. Wolbach SB, Howe PR. 1925. Tissue changes following deprivation of fat-soluble A vitamin. J Exp Med 42:753-777.
86. Xing W, Danilovich N, Sairam MR. 2002. Orphan receptor chicken ovalbumin upstream promoter transcription factors inhibit steroid factor-1, upstream stimulatory factor, and activator protein-1 activation of ovine follicle-stimulating hormone receptor expression via composite cis-elements. Biol Reprod 66:1656-1666.
87. You LR, Lin FJ, Lee CT, DeMayo FJ, Tsai MJ, Tsai SY. 2005. Suppression of Notch signalling by the COUP-TFII transcription factor regulates vein identity. Nature 435:98-104.
88. Zhang P, Bennoun M, Gogard C, Bossard P, Leclerc I, Kahn A, Vasseur-Cognet M. 2002. Expression of COUP-TFII in metabolic tissues during development. Mech Dev 119:109-114.