Keratinocyte growth factor (KGF) can replace testosterone in the ductal branching morphogenesis of the rat ventral prostate

International Journal of Developmental Biology

Volumn 40, Issue 5, 1996, Pages 941-951

  Sugimura, Yoshiki ^a   Foster, Barbara A ^b   Hom, Yun K ^b   Lipschutz, Joshua H ^b   Rubin, Jeffrey S ^c   Finch, Paul W ^d   Aaronson, Stuart A ^d   Hayashi, Norio ^e   Kawamura, Juichi ^e   Cunha, Gerald R ^b  

^a AICHI CANCER CENTER HOSPITAL   (Japan)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^e MIE UNIVERSITY   (Japan)

Author keywords

branching morphogenesis; epithelial growth; keratinocyte growth factor; mesenchymal epithelial interactions; prostate; testosterone

Indexed keywords

CYPROTERONE ACETATE; GROWTH FACTOR; KERATINOCYTE GROWTH FACTOR; TESTOSTERONE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENT; EPITHELIUM; MALE; MESENCHYME; MORPHOGENESIS; NEWBORN; NONHUMAN; ORGAN CULTURE; PRIORITY JOURNAL; PROSTATE; RAT; TISSUE INTERACTION;

ANIMALS; ANTIBODIES, MONOCLONAL; DNA; FIBROBLAST GROWTH FACTOR 10; FIBROBLAST GROWTH FACTOR 7; FIBROBLAST GROWTH FACTORS; GROWTH SUBSTANCES; HISTOCYTOCHEMISTRY; IMAGE PROCESSING, COMPUTER-ASSISTED; IN SITU HYBRIDIZATION; MALE; MICE; MORPHOGENESIS; ORGAN CULTURE TECHNIQUES; POLYMERASE CHAIN REACTION; PROSTATE; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; TESTOSTERONE; TRANSCRIPTION, GENETIC;

ANIMALIA;

EID: 0005307025     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (76)

1. AARONSON, S.A., RUBIN, J.S., FINCH, P.W., WONG, J., MARCHESE, C., FALCO, J., TAYLOR, W G. and KRAUS, M.H. (1990). Growth factor-regulated pathways in epithelial cell proliferation. Am. Rev. Respir. Dis. 142: S7-S10.
2. ALARID, E.T., RUBIN, J.S., YOUNG, P., CHEDID, M., RON, D , AARONSON, S.A. and CUNHA, G.R. (1994). Keratinocyte growth factor functions in epithelial induction during seminal vesicle development. Proc. Natl. Acad. Sci. USA 91: 1074-1078
3. BANERJEE, P.P., BANERJEE, S., SPRANDO, R.L. and ZIRKIN, B.R. (1991). Regional cellular heterogeneity and DNA synthetic activity in rat ventral prostate during postnatal development. Biol. Reprod 45: 773-782.
4. BOTTARO, D.P., FORTNEY, E., RUBIN, J S and AARONSON, S.A. (1993). A keratinocyte growth factor receptor-derived peptide antagonist identifies part of the ligand binding site. J. Biol. Chem. 268. 9180-9183.
5. BOTTARO, D.P., RUBIN, J S , RON, D., FINCH, P.W., FLORIO, C. and AARONSON, S.A (1990). Characterization of the receptor for keratinocyte growth factor. Evidence for multiple fibroblast growth factor receptors. J. Biol. Chem. 265: 12767-12770
6. COOKE, P S., YOUNG, P. and CUNHA, G.R. (1991) Androgen receptor expression in developing male reproductive organs. Endocrinology 128: 2867-2873.
7. CROSSLEY, P.H. and MARTIN, G.R. (1995). The mouse fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development 121: 439-451
8. CULIG, Z., HOBISCH, A., CRONAUER, M.V , RADMAYR, C , TRAPMAN, J., HITTMAIR, A., BARTSCH, G. and KLOCKER, H. (1994). Androgen receptor activation in prostatic tumor cell lines by insulin-like growth factor-1, keratinocyte growth factor, and epidermal growth factor. Cancer Res. 54: 5474-5478.
9. CUNHA, G.R. (1994). Role of mesenchymal-epithelial interactions in normal and abnormal development of the mammary gland and prostate. Cancer (Suppl.) 74: 1030-1044
10. CUNHA, G.R. and LUNG, B. (1978). The possible influences of temporal factors in androgenic responsiveness of urogenital tissue recombinants from wild-type and androgen-insensitive (Tfm) mice. J. Exp Zool 205: 181-194.
11. CUNHA, G.R. and YOUNG, P. (1991). Inability of Tfm (testicular feminization) epithelial cells to express androgen-dependent seminal vesicle secretory proteins in chimeric tissue recombinants Endocrinology 128: 3293-3298.
12. CUNHA, G R., ALARID, E T , TURNER, T., DONJACOUR, A.A., BOUTIN, E.L. and FOSTER, B.A. (1992a). Normal and abnormal development of the male urogenital tract: role of androgens, mesenchymal-epithelial interactions and growth factors. J. Androl: 13 465-475.
13. CUNHA, G.R., BATTLE, E., YOUNG, P., BRODY, J., DONJACOUR, A., HAYASHI, N. and KINBARA, H (1992b) Role of epithelial-mesenchymal interactions in the differentiation and spatial organization of visceral smooth muscle. Epithelial Cell Biol. 1: 76-83.
14. CUNHA, G.R., CHUNG, L.W.K., SHANNON, J.M., TAGUCHI, O. and FUJII, H. (1983). Hormone-induced morphogenesis and growth: Role of mesenchymal-epithelial interactions. Recent Prog. Horm. Res. 39. 559-598.
15. CUNHA, G.R., DONJACOUR, A.A., COOKE, P.S., MEE, S., BIGSBY, R.M., HIGGINS, S.J. and SUGIMURA, Y. (1987). The endocrinology and developmental biology of the prostate. Endocr. Rev. 8: 338-363.
16. CUNHA, G.R., FOSTER, B.A., DONJACOUR, A., RUBIN, J.S , SUGIMURA, Y., FINCH, P.W., BRODY, J.R. and AARONSON, S A. (1994). Keratinocyte growth factor: a mediator of mesenchymal-epithelial interactions in the development of androgen target organs. In Sex Hormones and Antihormones in Endocrine Dependent Pathology: Basic and Clinical Aspects (Eds. M. Motta and L. Serio). Elsevier, New York, pp. 45-57.
17. CUNHA, G.R., REESE, B.A. and SEKKINGSTAD, M. (1980). Induction of nuclear androgen-binding sites in epithelium of the embryonic urinary bladder by mesenchyme of the urogenital sinus of embryonic mice. Endocrinology 107: 1767-1770.
18. DONJACOUR, A.A. and CUNHA, G.R. (1993). Assessment of prostatic protein secretion in tissue recombinants made of urogenital sinus mesenchyme and urothelium from normal or androgen-insensitive mice. Endocrinology 131: 2342-2350.
19. ERCOLANI, L., FLORENCE, B., DENARO, M. and ALEXANDER, M. (1988). Isolation and complete sequence of a functional human glyceraldehyde-3-phosphate dehydrogenase gene. J. Biol. Chem 263: 15335-15341.
20. FINCH, P.W., CUNHA, G.R., RUBIN, J.S., WONG, J. and RON, D. (1995). Pattern of KGF and KGFR expression during mouse fetal development suggests a role in mediating morphogenetic mesenchymal-epithelial interactions. Dev. Dynamics 203: 223-240.
21. FINCH, P.W., RUBIN, J.S., MIKI, T., RON, D. and AARONSON, S.A. (1989) Human KGF is FGF-related with properties of a paracrine effector of epithelial cell growth. Science 245: 752-755.
22. FRENCH, F.S., LUBAHN, D.B., BROWN, T.R., SIMENTAL, J.A., QUIGLEY, C.A., YARBROUGH, W.G., TAN, J.A., SAR, M., JOSEPH, D.R. and EVANS, B.A (1990). Molecular basis of androgen insensitivity. Recent Prog. Horm. Res 46: 1-38.
23. GELMANN, E. (1991). Oncogenes and growth factors in prostatic cancer. J. NIH Res. 3: 62-66.
24. GUO, L., DEGENSTEIN, L and FUCHS, E. (1996). Keratinocyte growth factor is required for hair development but not for wound healing Genes Dev 10: 165-175.
25. HAYASHI, N., SUGIMURA, Y., KAWAMURA, J., DONJACOUR, A.A. and CUNHA, G.R. (1991). Morphological and functional heterogeneity in the rat prostatic gland. Biol. Reprod. 45: 308-321.
26. HE, W W., KUMAR, M.V. and TINDALL, D.J. (1991). A frameshift mutation in the androgen receptor gene causes complete androgen insensitivity in the testicular-feminized mouse. Nucleic Acids Res 19: 2373-2378
27. HERBERT, J.H., ROSENQUIST, T , GOTZ, J. and MARTIN, G R (1994). FGF5 as a regulator of hair growth cycle evidence from targeted and spontaneous mutations Cell 78: 1017-1025.
28. HINEGARDNER, R T (1971). An improved fluorometric assay for DNA Anal. Biochem 39: 197-201.
29. HUSMANN, D.A., McPHAUL, M. and WILSON, J D. (1991). Androgen receptor expression in the developing rat prostate is not altered by castration, flutamide, or suppression of the adrenal axis Endocrinology 128: 1902-1906.
30. JOHNSON, D.E and WILLIAMS, L.T. (1993) Structural and functional diversity in the FGF receptor multigene family Adv. Cancer Res. 60: 1-41
31. KOJI, T., CHEDID, M., RUBIN, J.S., SLAYDEN, O.D , CSAKY, K.G., AARONSON, S.A. and BRENNER, R.M. (1994). Progesterone-dependent expression of keratinocyte growth factor mRNA in stromal cells of the primate endometrium: Keratinocyte growth factor as a progestomedin. J. Cell Biol. 125: 393-401.
32. LASNITZKI, I and 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
33. LIN, Y.C., CANATAN, H , CHANG, C.J., HU, Y.F., CHEN, R., YU, C.Y , BRUEGGEMEIER, R.W and SOMERS, W.J. (1994). Detection of keratinocyte growth factor (KGF) transcripts from normal human and archival canine benign prostatic hyperplastic tissues. J. Med. 25: 41-64.
34. LOPES, E.S., FOSTER, B.A., DONJACOUR, A.A. and CUNHA, G.R. (1996). Initiation of secretory activity of rat prostate epithelium in organ culture. Endocrinology. (In press)
35. LUMSDEN, A. (1990). The cellular basis of segmentation in the developing hindbrain. Trends Neurosci. 13: 329-335.
36. MARCHESE, C., RUBIN, J., RON, D , FAGGIONI, A., TORRISI, M.R., MESSINA, A., FRATI, L. and AARONSON, S.A. (1990). Human keratinocyte growth factor activity on proliferation and differentiation of human keratinocytes: differentiation response distinguishes KGF from EGF family. J Cell. Physiol. 144: 326-332.
37. MASON, I.J. (1994). The ins and outs of fibroblast growth factors. Cell 78: 547-552.
38. MASON, I.J., PACE, F.F., SMITH, R. and DICKSON, C. (1994). FGF-7 (keratinocyte growth factor) expression during mouse development suggests roles in myogenesis, forebrain regionalization and epithelial-mesenchymal interactions. Mech. Dev. 15: 15-30.
39. MIKI, T., BOTTARO, D.P., FLEMING, T.P , SMITH, C.L., BURGESS, W.H., CHAN, A.M-L. and AARONSON, S.A. (1992). Determination of ligand-binding specificity by alternative splicing: two distinct growth factor receptors encoded by a single gene. Proc. Natl. Acad. Sci. USA 89: 246-251.
40. MIKI, T., FLEMING, T.P., BOTTARO, D.P , RUBIN, J.S., RON, D. and AARONSON, S.A. (1991). Expression cDNA cloning of the KGF receptor by creation of a transforming autocrine loop. Science 251: 72-75.
41. NISWENDER, L., TICKLE, C., VOGEL, A., BOOTH, I. and MARTIN, G.R. (1993). FGF-4 replaces the apical ectodermal ridge and directs outgrowth and patterning of the limb. Cell 75: 579-587.
42. OHNO, S (1979). Major Sex Determining Genes. Springer-Verlag, New York.
43. ORR-URTREGER, A., BEDFORD, M.T., BURAKOVA, T., ARMAN, E., ZIMMER, Y., YAYON, A., GIVOL, D. and LONAI, P. (1993). Developmental localization of the splicing alternatives of fibroblast growth factor receptor-2 (FGFR2). Dev. Biol. 158: 475-486.
44. PEEHL, D. and RUBIN, J. (1995). Keratinocyte growth factor: an androgen-regulated mediator of stromal-epithelial interactions in the prostate. World J. Urol. 13: 312-317.
45. PETERS, K., WERNER, S., LIAO, X., WERT, S., WHITSETT, J. and WILLIAMS, L. (1994). Targeted expression of a dominant negative FGF receptor blocks branching morphogenesis and epithelial differentiation of the mouse lung. EMBO J. 12: 973-986.
46. PIERCE, G.F., YANAGIHARA, D., KLOPCHIN, K., DANILENKO, D.M., HSU, E., KENNEY, W.C. and MORRIS, C.F. (1994). Stimulation of all epithelial elements during skin regeneration by keratinocyte growth factor. J. Exp. Med. 179. 831-840.
47. PRICE, D. and ORTIZ, E. (1965). The role of fetal androgens in sex differentiation in mammals. In Organogenesis (Eds. R. L. Ursprung and H DeHaan). Holt, Rinehart and Winston, New York, pp. 629-652.
48. PRINS, G.S. and BIRCH, L. (1995). The developmental pattern of androgen receptor expression in rat prostate lobes is altered after neonatal exposure to estrogen. Endocrinology 136: 1303-1314.
49. PRINS, G.S , COOKE P.S., BIRCH, L., DONJACOUR, A.A., YALCINKAYA, T.M., SIITERI, P.K and CUNHA, G.R. (1992). Androgen receptor expression and 5α-reductase activity along the proximal-distal axis of the rat prostatic duct. Endocrinology 130: 3066-3073.
50. RAPPOLEE, D.A , BRENNER, C.A., SCHULTZ, R., MARK, D. and WERB, Z. (1988). Developmental expression of PDGF, TGF-alpha, and TGF-β genes in preimplantation mouse embryos. Science 241. 1823-1825.
51. RAPPOLEE, D A., WANG, A , MARK, D and WERB, Z (1989). Novel method for studying mRNA phenotypes in single or small numbers of cells. J. Cell. Biochem. 39: 1-11.
52. RON, D., BOTTARO, D.P., FINCH, P.W., MORRIS, D W , RUBIN, J.S and AARONSON, S A. (1993). Expression of biologically active recombinant KGF: structure/function analysis of N-terminal truncation mutants. J. Biol. Chem. 268: 2984-2988.
53. RUBIN, J.S., OSADA, H , FINCH, P W., TAYLOR, W.G., RUDIKOFF, S. and AARONSON, S.A. (1989). Purification and characterization of a newly identified growth factor specific for epithelial cells. Proc Natl Acad. Sci. USA 86: 802-806.
54. SHANNON, J M and CUNHA, G.R. (1984). Characterization of androgen binding and deoxyribonucleic acid synthesis in prostate-like structures induced in testicular feminized (Tfm/Y) mice. Biol. Reprod. 31: 175-183
55. SHIMA, H , TSUJI, M., YOUNG, P.F. and CUNHA, G.R. (1990). Postnatal growth of mouse seminal vesicle is dependent on 5α-dihydrotestosterone. Endocrinology 127: 3222-3233
56. SLACK, J.M. (1994) Inducing factors in Xenopus early embryos. Curr. Biol. 4: 116-126.
57. STORY, M.T. (1991) Polypeptide modulators of prostatic growth and development. In Prostate Cancer: Cell and Molecular Mechanisms in Diagnosis and Treatment (Eds. J. T Isaacs). Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 123-146.
58. SUGIMURA, Y., CUNHA, G.R and BIGSBY, R.M. (1986a). Androgenic induction of deoxyribonucleic acid synthesis in prostatic glands induced in the urothelium of testicular feminized (Tfm/y) mice. Prostate 9: 217-225.
59. SUGIMURA, Y., CUNHA, G.R. and DONJACOUR, A.A. (1986b). Morphogenesis of ductal networks in the mouse prostate. Biol. Reprod. 34: 961-971
60. SUGIMURA, Y., CUNHA, G.R., DONJACOUR, A.A., BIGSBY, R M and BRODY, J.R. (1986c) Whole-mount autoradiography study of DNA synthetic activity during postnatal development and androgen-induced regeneration in the mouse prostate Biol. Reprod 34: 985-995.
61. TAKEDA, H. and CHANG, C. (1991). Immunohistochemical and in situ hybridization analysis of androgen receptor expression during the development of the mouse prostate gland. J. Endocrinol. 129. 83-89.
62. TAKEDA, H., SUEMATSU, N. and MIZUNO, T. (1990). Transcription of prostatic steroid binding protein (PSBP) gene is induced by epithelial-mesenchymal interaction. Development 110: 273-282.
63. THOMPSON, T C. (1990). Growth factors and oncogenes in prostate cancer. Cancer Cells 11: 345-354.
64. TIMMS, B.G., MOHS, T.J. and DIDIO, J.A. (1994). Ductal budding and branching patterns in the developing prostate. J. Urol. 151: 1427-1432.
65. TUOHIMAA, P. (1980). Control of cell proliferation in male accessory sex glands. In Male Accessory Sex Glands (Eds E Spring-Mills and E.S.E. Hafez). Elsevier/ North Holland, New York, pp. 131-153.
66. ULICH, T.R., YI, E.S., CARDIFF, R., YIN, S., BIKHAZI, N., BILTZ, R., MORRIS, C.F. and PIERCE, G.F. (1994a). Keratinocyte growth factor is a growth factor for mammary epithelium in vivo. The mammary epithelium of lactating rats is resistant to the proliferative action of keratinocyte growth factor. Am. J. Pathol. 144: 862-868.
67. ULICH, T R., YI, E S., LONGMUIR, K , YIN, S , BILTZ, R , MORRIS, C.F., HOUSLEY, R M. and PIERCE, G.F. (1994b). Keratinocyte growth factor is a growth factor for type II pneumocytes in vivo. J. Clin. Invest. 93: 1298-1306.
68. VOGEL, A and TICKLE, C. (1993). FGF-4 maintains polarizing activity of posterior limb bud cells in vivo and in vitro. Development 119: 199-206.
69. WERNER, S., WEINBERG, W., LIAO, X., PETERS, K.G , BLESSING, M., YUSPA, S.H , WEINER, R L. and WILLIAMS, L.T. (1993). Targeted expression of a dominant-negative FGF receptor mutant in the epidermis of transgenic mice reveals a role of FGF in keratinocyte organization and differentiation. EMBO J, 12: 2635-2643.
70. WESSELLS, N.K. (1977). Tissue Interactions and Development. W.A. Benjamin, Inc., Menlo Park (CA).
71. WILSON, J.D (1992). Syndrome of androgen resistance Biol. Reprod. 46: 168-173.
72. YAN, G., FUKABORI, Y., McBRIDE, G., NIKOLAROPOLOUS, S. and McKEEHAN, W. (1993a) Exon switching and activation of stromal and embryonic FGF/FGF receptor genes in prostate epithelial cells accompanies stromal independence and malignancy. Mol. Cell. Biol. 13. 4513-4522.
73. YAN, G., FUKABORI, Y., NIKOLAROPOULOS, S., WANG, F. and McKEEHAN, W.L. (1992). Heparin-binding keratinocyte growth factor is a candidate stromal to epithelial cell andromedin. Mol. Endocrinol. 6: 2123-2128.
74. YAN, G., McBRIDE, G. and McKEEHAN, W.L (1993b). Exon skipping causes alteration of the COOH-terminus and deletion of the phospholipase C gamma 1 interaction site in the FGF receptor 2 kinase in normal prostate epithelial cells. Biochem. Biophys. Res. Commun. 194: 512-518.
75. YAN, G.G., NIKOLAROPOULOS, S., WANG, F. and McKEEHAN, W.L. (1991). Sequence of rat keratinocyte growth factor (heparin-binding growth factor type 7). In Vitro Cell Dev. Biol. 27A: 437-438.
76. YI, E.S., BEDOYA, A.A., LEE, H., KIM, S., HOUSLEY, R.M., AUKERMAN, S.L., TARPLEY, J.E., STARNES, C., YIN, S., PIERCE, G.F. et al. (1994). Keratinocyte growth factor causes cystic dilation of the mammary glands of mice. Interactions of keratinocyte growth factor, estrogen, and progesterone in vivo. Am. J. Pathol 145: 1015-1022.