Hormonal, cellular, and molecular control of prostatic development

Developmental Biology

Volumn 253, Issue 2, 2003, Pages 165-174

  Marker, Paul C ^a   Donjacour, Annemarie A ^a   Dahiya, Rajvir ^b   Cunha, Gerald R ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Androgens; Branching morphogenesis; Development; Epithelial; Genetic; Human; Mesenchymal; Mouse; Prostate; Testosterone

Indexed keywords

ANDROGEN; ANDROGEN BINDING PROTEIN; ANDROGEN RECEPTOR; ANDROSTANEDIOL; CYTOKERATIN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FIBROBLAST GROWTH FACTOR 10; FIBROBLAST GROWTH FACTOR 2; GENE PRODUCT; HERMES ANTIGEN; PROTEIN P63; STEROID REDUCTASE; TESTOSTERONE; TRANSCRIPTION FACTOR;

CELL COMMUNICATION; CLOACA; CYTOLOGY; DNA SYNTHESIS; EXPERIMENTATION; FETUS CIRCULATION; GENETIC CODE; GENETIC ENGINEERING; GENETIC MANIPULATION; GESTATIONAL AGE; GONAD DEVELOPMENT; HOMEOBOX; HORMONAL REGULATION; HORMONE ACTION; HORMONE DETERMINATION; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; MALE; MARSUPIAL; MESENCHYME; MORPHOGENESIS; MUTATION; NONHUMAN; PERINATAL PERIOD; PHENOTYPE; PRIORITY JOURNAL; PROSTATE; PROSTATE EPITHELIUM; PROTEIN SECRETION; REVIEW; SEX DIFFERENCE; SEXUAL MATURITY; SYNTHESIS; UROGENITAL SINUS;

MAMMALIA;

EID: 0037440475     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0012-1606(02)00031-3     Document Type: Review

References (72)

1. Aboseif S., El-Sakka A., Young P., Cunha G. Mesenchymal reprogramming of adult human epithelial differentiation. Differentiation. 65:1999;113-118.
2. Andersson S., Berman D.M., Jenkins E.P., Russell D.W. Deletion of steroid 5 alpha-reductase 2 gene in male pseudohermaphroditism. Nature. 354:1991;159-161.
3. Angelsen A., Mecsei R., Sandvik A.K., Waldum H.L. Neuroendocrine cells in the prostate of the rat, guinea pig, cat, and dog. Prostate. 33:1997;18-25.
4. Aumuller G., Leonhardt M., Janssen M., Konrad L., Bjartell A., Abrahamsson P.A. Neurogenic origin of human prostate endocrine cells. Urology. 53:1999;1041-1048.
5. Baker J., Hardy M.P., Zhou J., Bondy C., Lupu F., Bellve A.R., Efstratiadis A. Effects of an Igf1 gene null mutation on mouse reproduction. Mol. Endocrinol. 10:1996;903-918.
6. Bhatia-Gaur R., Donjacour A.A., Sciavolino P.J., Kim M., Desai N., Young P., Norton C.R., Gridley T., Cardiff R.D., Cunha G.R., Abate-Shen C., Shen M.M. Roles for Nkx3.1 in prostate development and cancer. Genes Dev. 13:1999;966-977.
7. Brown T.R., Lubahn D.B., Wilson E.M., Joseph D.R., French F.S., Migeon C.J. Deletion of the steroid-binding domain of the human androgen receptor gene in one family with complete androgen insensitivity syndrome evidence for further genetic heterogeneity in this syndrome . Proc. Natl. Acad. Sci. USA. 85:1988;8151-8155.
8. Cancilla B., Jarred R.A., Wang H., Mellor S.L., Cunha G.R., Risbridger G.P. Regulation of prostate branching morphogenesis by activin A and follistatin. Dev. Biol. 237:2001;145-158.
9. Charest N.J., Zhou Z.X., Lubahn D.B., Olsen K.L., Wilson E.M., French F.S. A frameshift mutation destabilizes androgen receptor messenger RNA in the Tfm mouse. Mol. Endocrinol. 5:1991;573-581.
10. Collins A.T., Habib F.K., Maitland N.J., Neal D.E. Identification and isolation of human prostate epithelial stem cells based on alpha(2)beta(1)-integrin expression. J. Cell Sci. 114:2001;3865-3872.
11. Cunha G.R., Donjacour A.A., Cooke P.S., Mee S., Bigsby R.M., Higgins S.J., Sugimura Y. The endocrinology and developmental biology of the prostate. Endocr. Rev. 8:1987;338-362.
12. Cunha G.R., Lung B. The possible influence of temporal factors in androgenic responsiveness of urogenital tissue recombinants from wild-type and androgen-insensitive (Tfm) mice. J. Exp. Zool. 205:1978;181-193.
13. Cunha G.R., Sekkingstad M., Meloy B.A. Heterospecific induction of prostatic development in tissue recombinants prepared with mouse, rat, rabbit and human tissues. Differentiation. 24:1983;174-180.
14. Deslypere J.P., Young M., Wilson J.D., McPhaul M.J. Testosterone and 5 alpha-dihydrotestosterone interact differently with the androgen receptor to enhance transcription of the MMTV-CAT reporter gene. Mol. Cell. Endocrinol. 88:1992;15-22.
15. Donjacour A.A., Cunha G.R. The effect of androgen deprivation on branching morphogenesis in the mouse prostate. Dev. Biol. 128:1988;1-14.
16. Donjacour A.A., Cunha G.R. Assessment of prostatic protein secretion in tissue recombinants made of urogenital sinus mesenchyme and urothelium from normal or androgen-insensitive mice. Endocrinology. 132:1993;2342-2350.
17. Donjacour A.A., Rosales A., Higgins S.J., Cunha G.R. Characterization of antibodies to androgen-dependent secretory proteins of the mouse dorsolateral prostate. Endocrinology. 126:1990;1343-1354.
18. Elfman F., Bok R., Conn M., Shuman M., Cunha G. Urokinase plasminogen activator amino-terminal peptides inhibit development of the rat ventral prostate. Differentiation. 69:2001;108-120.
19. Foster B.A., Cunha G.R. Efficacy of various natural and synthetic androgens to induce ductal branching morphogenesis in the developing anterior rat prostate. Endocrinology. 140:1999;318-328.
20. Gakunga P., Frost G., Shuster S., Cunha G., Formby B., Stern R. Hyaluronan is a prerequisite for ductal branching morphogenesis. Development. 124:1997;3987-3997.
21. Garabedian E.M., Humphrey P.A., Gordon J.I. A transgenic mouse model of metastatic prostate cancer originating from neuroendocrine cells. Proc. Natl. Acad. Sci. USA. 95:1998;15382-15387.
22. Gaspar M.L., Meo T., Bourgarel P., Guenet J.L., Tosi M. A single base deletion in the Tfm androgen receptor gene creates a short-lived messenger RNA that directs internal translation initiation. Proc. Natl. Acad. Sci. USA. 88:1991;8606-8610.
23. Hamilton W., Boyd J., Mossman H. Human Embryology. 1959;Williams and Wilkins Co. Baltimore.
24. Hayashi N., Cunha G.R., Parker M. Permissive and instructive induction of adult rodent prostatic epithelium by heterotypic urogenital sinus mesenchyme. Epithelial Cell Biol. 2:1993;66-78.
25. Hayward S.W., Baskin L.S., Haughney P.C., Cunha A.R., Foster B.A., Dahiya R., Prins G.S., Cunha G.R. Epithelial development in the rat ventral prostate, anterior prostate and seminal vesicle. Acta Anatomica. 155:1996;81-93.
26. Hayward S.W., Baskin L.S., Haughney P.C., Foster B.A., Cunha A.R., Dahiya R., Prins G.S., Cunha G.R. Stromal development in the ventral prostate, anterior prostate and seminal vesicle of the rat. Acta Anatomica. 155:1996;94-103.
27. Hayward S.W., Haughney P.C., Rosen M.A., Greulich K.M., Weier H.U., Dahiya R., Cunha G.R. Interactions between adult human prostatic epithelium and rat urogenital sinus mesenchyme in a tissue recombination model. Differentiation. 63:1998;131-140.
28. He W.W., Kumar M.V., Tindall D.J. A frameshift mutation in the androgen receptor gene causes complete androgen insensitivity in the testicular-feminized mouse. Nucleic Acids Res. 19:1991;2373-2378.
29. Jarred R.A., McPherson S.J., Bianco J.J., Couse J.F., Korach K.S., Risbridger G.P. Prostate phenotypes in estrogen-modulated transgenic mice. Trends Endocrinol. Metab. 13:2002;163-168.
30. Kellokumpu-Lehtonen P. Development of sexual dimorphism in human urogenital sinus complex. Biol. Neonate. 48:1985;157-167.
31. Lamm M.L., Podlasek C.A., Barnett D.H., Lee J., Clemens J.Q., Hebner C.M., Bushman W. Mesenchymal factor bone morphogenetic protein 4 restricts ductal budding and branching morphogenesis in the developing prostate. Dev. Biol. 232:2001;301-314.
32. Lee C., Sensibar J.A., Dudek S.M., Hiipakka R.A., Liao S.T. Prostatic ductal system in rats regional variation in morphological and functional activities . Biol. Reprod. 43:1990;1079-1086.
33. Lowsley O.S. The development of the human prostate gland with reference to the development of other structures at the neck of the urinary bladder. Am. J. Anat. 13:1912;299-349.
34. Lubahn D.B., Brown T.R., Simental J.A., Higgs H.N., Migcon C.J., Wilson E.M., French F.S. Sequence of the intron/exon junctions of the coding region of the human androgen receptor gene and identification of a point mutation in a family with complete androgen insensitivity. Proc. Natl. Acad. Sci. USA. 86:1989;9534-9538.
35. Mahendroo M.S., Cala K.M., Hess D.L., Russell D.W. Unexpected virilization in male mice lacking steroid 5 alpha-reductase enzymes. Endocrinology. 142:2001;4652-4662.
36. Marker P.C., Stephan J.P., Lee J., Bald L., Mather J.P., Cunha G.R. fucosyltransferase1 and H-type complex carbohydrates modulate epithelial cell proliferation during prostatic branching morphogenesis. Dev. Biol. 233:2001;95-108.
37. McNeal J.E. The prostate gland morphology and pathobiology . Monogr. Urol. 4:1983;3-37.
38. Mills J.S., Needham M., Parker M.G. Androgen regulated expression of a spermine binding protein gene in mouse ventral prostate. Nucleic Acids Res. 15:1987;7709-7724.
39. Mills J.S., Needham M., Parker M.G. A secretory protease inhibitor requires androgens for its expression in male sex accessory tissues but is expressed constitutively in pancreas. EMBO J. 6:1987;3711-3717.
40. Mills J.S., Needham M., Thompson T.C., Parker M.G. Androgen-regulated expression of secretory protein synthesis in mouse ventral prostate. Mol. Cell. Endocrinol. 53:1987;111-118.
41. Nagel S.C., vom Saal F.S., Welshons W.V. Developmental effects of estrogenic chemicals are predicted by an in vitro assay incorporating modification of cell uptake by serum. J. Steroid Biochem. Mol. Biol. 69:1999;343-357.
42. Podlasek C.A., Barnett D.H., Clemens J.Q., Bak P.M., Bushman W. Prostate development requires Sonic hedgehog expressed by the urogenital sinus epithelium. Dev. Biol. 209:1999;28-39.
43. Podlasek C.A., Clemens J.Q., Bushman W. Hoxa-13 gene mutation results in abnormal seminal vesicle and prostate development. J. Urol. 161:1999;1655-1661.
44. Podlasek C.A., Duboule D., Bushman W. Male accessory sex organ morphogenesis is altered by loss of function of Hoxd-13. Dev. Dyn. 208:1997;454-465.
45. Podlasek C.A., Seo R.M., Clemens J.Q., Ma L., Maas R.L., Bushman W. Hoxa-10 deficient male mice exhibit abnormal development of the accessory sex organs. Dev. Dyn. 214:1999;1-12.
46. Pointis G., Latreille M.T., Cedard L. Gonado-pituitary relationships in the fetal mouse at various times during sexual differentiation. J. Endocrinol. 86:1980;483-488.
47. Pointis G., Latreille M.T., Mignot T.M., Janssens Y., Cedard L. Regulation of testosterone synthesis in the fetal mouse testis. J. Steroid Biochem. 11:1979;1609-1612.
48. Prins G.S. Neonatal estrogen exposure induces lobe-specific alterations in adult rat prostate androgen receptor expression. Endocrinology. 130:1992;2401-2412.
49. Ruan W., Powell-Braxton L., Kopchick J.J., Kleinberg D.L. Evidence that insulin-like growth factor I and growth hormone are required for prostate gland development. Endocrinology. 140:1999;1984-1989.
50. Russell D.W., Wilson J.D. Steroid 5 alpha-reductase two genes/two enzymes . Annu. Rev. Biochem. 63:1994;25-61.
51. Schneider A., Brand T., Zweigerdt R., Arnold H. Targeted disruption of the Nkx3.1 gene in mice results in morphogenetic defects of minor salivary glands parallels to glandular duct morphogenesis in prostate . Mech. Dev. 95:2000;163-174.
52. Sciavolino P.J., Abrams E.W., Yang L., Austenberg L.P., Shen M.M., Abate-Shen C. Tissue-specific expression of murine Nkx3.1 in the male urogenital system. Dev. Dyn. 209:1997;127-138.
53. Shaw G., Renfree M.B., Leihy M.W., Shackleton C.H.L., Roitman E., Wilson J.D. Prostate formation in a marsupial is mediated by the testicular androgen 5alpha-androstane-3alpha, 17beta-diol. Proc. Natl. Acad. Sci. USA. 97:2000;12256-12259.
54. Signoretti S., Waltregny D., Dilks J., Isaac B., Lin D., Garraway L., Yang A., Montironi R., McKeon F., Loda M. p63 is a prostate basal cell marker and is required for prostate development. Am. J. Pathol. 157:2000;1769-1775.
55. Siiteri P.K., Wilson J.D. Testosterone formation and metabolism during male sexual differentiation in the human embryo. J. Clin. Endocrinol. Metab. 38:1974;113-125.
56. Steger R.W., Chandrashekar V., Zhao W., Bartke A., Horseman N.D. Neuroendocrine and reproductive functions in male mice with targeted disruption of the prolactin gene. Endocrinology. 139:1998;3691-3695.
57. Sugimura Y., Cunha G.R., Donjacour A.A. Morphogenesis of ductal networks in the mouse prostate. Biol. Reprod. 34:1986;961-971.
58. Sugimura Y., Cunha G.R., Donjacour A.A., Bigsby R.M., Brody J.R. Whole-mount autoradiography study of DNA synthetic activity during postnatal development and androgen-induced regeneration in the mouse prostate. Biol. Reprod. 34:1986;985-995.
59. Sugimura Y., Foster B.A., Hom Y.K., Lipschutz J.H., Rubin J.S., Finch P.W., Aaronson S.A., Hayashi N., Kawamura J., Cunha G.R. Keratinocyte growth factor (KGF) can replace testosterone in the ductal branching morphogenesis of the rat ventral prostate. Int. J. Dev. Biol. 40:1996;941-951.
60. Takeda H., Lasnitzki I., Mizuno T. Analysis of prostatic bud induction by brief androgen treatment in the fetal rat urogenital sinus. J. Endocrinol. 110:1986;467-470.
61. Tanaka M., Komuro I., Inagaki H., Jenkins N.A., Copeland N.G., Izumo S. Nkx3.1, a murine homolog of Drosophila bagpipe, regulates epithelial ductal branching and proliferation of the prostate and palatine glands. Dev. Dyn. 219:2000;248-260.
62. Thomson A.A., Cunha G.R. Prostatic growth and development are regulated by FGF10. Development. 126:1999;3693-3701.
63. Thomson A.A., Timms B.G., Barton L., Cunha G.R., Grace O.C. The role of smooth muscle in regulating prostatic induction. Development. 129:2002;1905-1912.
64. Timms B.G., Lee C.W., Aumuller G., Seitz J. Instructive induction of prostate growth and differentiation by a defined urogenital sinus mesenchyme. Microsc. Res. Tech. 30:1995;319-332.
65. Timms B.G., Mohs T.J., DiDio J.A. Ductal budding and branching patterns in the developing prostate. J. Urol. 151:1994;1427-1432.
66. Timms B.G., Mohs T.J., Didio L.J. Ductal budding and branching patterns in the developing prostate. J. Urol. 151:1994;1427-1432.
67. Timms B.G., Petersen S.L., vom Saal F.S. Prostate gland growth during development is stimulated in both male and female rat fetuses by intrauterine proximity to female fetuses. J. Urol. 161:1999;1694-1701.
68. vom Saal F.S., Timms B.G., Montano M.M., Palanza P., Thayer K.A., Nagel S.C., Dhar M.D., Ganjam V.K., Parmigiani S., Welshons W.V. 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. 94:1997;2056-2061.
69. Wang Y., Hayward S., Cao M., Thayer K., Cunha G. Cell differentiation lineage in the prostate. Differentiation. 68:2001;270-279.
70. Warot X., Fromental-Ramain C., Fraulob V., Chambon P., Dolle P. 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. 124:1997;4781-4791.
71. Xia T.G., Blackburn W.R., Gardner W.A. Jr. Fetal prostate growth and development. Pediatr. Pathol. 10:1990;527-537.
72. Xue Y., Smedts F., Verhofstad A., Debruyne F., de la Rosette J., Schalken J. Cell kinetics of prostate exocrine and neuroendocrine epithelium and their differential interrelationship new perspectives . Prostate Suppl. 8:1998;62-73.