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Regulation of c-fos mRNA expression in Sertoli cells by cyclic AMP, calcium, and protein kinase C mediated pathways

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Abstract

The role of second messenger pathways, cyclic AMP, calcium, and protein kinase C (PKC) in the transcriptional regulation of c-fos protooncogene expression in rat Sertoli cells was investigated. c-fos expression was monitored by Northern blot analysis. Although the action of FSH on Sertoli cells is considered to be mediated by CAMP, dibutyryl CAMP (dbcAMP), a potent membrane permeable analog of cAMP, induced much less c-fos mRNA expression than FSH (<50%) suggesting that additional cAMP-independent mechanisms may mediate the effect of FSH on c-fos. Specific intracellular inhibitors of PKC decreased c-fos induction in response to FSH by more than 50%. lonomycin, which increases intracellular free calcium concentration, induced c-fos expression significantly. These data demonstrate that Sertoli cell c-fos mRNA expression is under multifactorial regulation by CAMP, calcium, and PKC.

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References

  1. Lee KAW: Transcriptional regulation by cAMP. Curr Opin Cell Biol 3: 953–959, 1991

    Google Scholar 

  2. Karin M: Signal transduction and gene control. Curr Opin Cell Biol 3: 467–473, 1991

    Google Scholar 

  3. Treisman R: Structure and function of serum response factor. In: S.L. McKnight, K. Yamamoto (eds). Transcriptional Regulation. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 881–905, 1992

    Google Scholar 

  4. Sassone-Corci P, Visvader J, Ferland L, Mellon PL, Verma IM: Induction of protooncogene c fos transcription through the adenylate cyclase pathway: characterization of a CAMP-responsive element. Genes Dev 2: 1529–1538, 1988

    Google Scholar 

  5. Sheng M, McFadden G, Greenberg ME: Membrane depolarization and calcium induce c fos transcription via phosphorylation of transcription factor CREB. Neuron 4: 571–582, 1990

    Google Scholar 

  6. Sheng M, Dougan ST, McFadden G, Greenberg ME: Calcium and growth factor pathways of c-fos transcriptional activation require distinct upstream regulatory sequences. Mol Cell Biol 8: 2787–2796, 1988

    Google Scholar 

  7. Griswold MD, Solari A, Tung PS, Fritz IB: Stimulation by folliclestimulating hormone of DNA synthesis and of mitosis in cultured Sertoli cells prepared from testes of immature rats. Mol Cell Endocrinol 7: 151–165, 1977

    Google Scholar 

  8. Orth JM: The role of follicle-stimulating hormone in controlling Sertoli cell proliferation in testis of fetal rats. Endocrinol 115: 1248–1255, 1984

    Google Scholar 

  9. Griswold MD: Action of FSH on mammalian Sertoli cells. In: Russell LD, Griswold MD (eds) The Sertoli Cell. Cache River Press, Clearwater, FL, pp. 493–508, 1993

    Google Scholar 

  10. Hall SH, Joseph DR, French FS, Conti M: Follicle-stimulating hormone induces transient expression of the protooncogene c-fos in primary Sertoli cell cultures. Mol Endocrinol 2: 55–61, 1988

    Google Scholar 

  11. Papadopoulos V, Dym M: Sertoli cell differentiation on basement membrane is mediated by the c-fos protooncogene. Proc Natl Acad Sci USA 91: 7027–7031, 1994

    Google Scholar 

  12. Hadley MA, Weeks BS, Kleinman HK, Dym M: Laminin promotes formation of cord-like structures by Sertoli cells in vitro. Dev Biel 140: 318–327, 1990

    Google Scholar 

  13. Hidaka H, Inagaki M, Kawamoto S, Sasaki Y: Isoquinolinesulfonamides, novel and potent inhibitors of cyclic nucleotide dependent protein kinase and protein kinase C. Biochem 23: 5036–5040, 1984

    Google Scholar 

  14. Chijiwa T, Mishima A, Hagiwara M, Sano M, Hayashi K, Inoue T, Naito K, Toshioka T, Hidaka H: Inhibition of Forskolin-induced neurite outgrowth and protein phosphorylation by a newly synthesized selective inhibitor of cyclic AMP-dependent protein kinase, N-[2-(pbromosuccinamylamino) ethyl[-5]isoquinoline sulfonamide (H-89), of PC 12 pheochromocytoma cells. J Biol Chem 265: 5267–5272, 1990

    Google Scholar 

  15. Chomczynski P, Sacchi N: Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156–159, 1987

    Article  CAS  PubMed  Google Scholar 

  16. Curran T, Gordon MB, Rubino KL, Sambucetti LC: Isolation and characterization of the c-fos (rat) cDNA and analysis of post-translational modification in vitro. Oncogene 2: 79–84, 1987

    Google Scholar 

  17. Dym M, Lamsam-Casalotti S, Jia MC, Kleinman HK, Papadopoulos V: Basement membrane increases G-protein levels and follicle-stimulating hormone responsiveness of Sertoli cell adenylyl cyclase activity. Endocrinol 128: 1167–1176, 1991

    Google Scholar 

  18. Danielson PE, Forss-Petter S, Brow MA, Calavetta L, Douglass J, Milner RJ, Sutcliffe JG: p1B15: a cDNA clone of the rat mRNA encoding cyclophilin. DNA 7: 261–267, 1988

    Google Scholar 

  19. Papadopoulos V, Carreau S, Szerman-Joly E, Drosdowsky MA, Dehennin L, Scholler R: Rat testis 17β-estradiol: Identification by gas chromatography-mass spectrometry and age related cellular distribution. J Steroid Biochem 24: 1211–1216, 1986

    Google Scholar 

  20. Kuo JF, Andersson RGG, Wise BC, Mackerlova L, Salomonsson I, Brackett NL, Katoh N, Shoji M, Wrenn RW: Calcium-dependent protein kinase: widespread occurrence in various tissues and phyla of the animal kingdom and comparison of effects of phospholipid, calmodulin, and trifluoperazine. Proc Natl Acad Sci USA 77: 7039–7043, 1980

    Google Scholar 

  21. Papadopoulos V, Carreau S, Drosdowsky MA: Effect of phorbol ester and phospholipase C on LH-stimulated steroidgenesis in purified rat Leydig cells. FEBS Lett 188: 312–316, 1985

    Google Scholar 

  22. Messina JL, Standaert ML, Ishizuka T, Weinstock RS, Farese RV: Role of protein kinase C in insulin's regulation of c fos transcription. J Biol Chem 267: 9223–9228, 1992

    Google Scholar 

  23. Muller R: In: The Fos and Jun families of transcription factors. P. Angel, E Herdich (eds). CRC Press, Boca Raton, FL, pp. 189–197, 1993

  24. Smith EP, Hall SH, Monaco L, French FS, Wilson EM, Conti M: A rat Sertoli cell factor similar to basic fibroblast growth factor increases c-fos messenger ribonucleic acid in cultured Sertoli cells. Mol Endocrinol 3: 954–961, 1989

    Google Scholar 

  25. Norton JN, Skinner MK: Regulation of Sertoli cell differentiation by the testicular paracrine factor PModS: Potential role of immediateearly genes. Mol Endocrinol 6: 2018–2026, 1992

    Google Scholar 

  26. Schwartz MA: Spreading of human endothehal cells on fibronectin or vitronectin triggers elevation of intracellular free calcium. J Cell Biol 120: 1003–1010, 1993

    Google Scholar 

  27. Ravindranath N, Papadopoulos V, Brooker G, Kleinman HK, Dym M: Follicle stimulating hormone decreases intracellular free calcium in immature rat Sertoli cells cultured on basement membrane. 76th Annual Meeting of the Endocrine Society, Anaheim, CA, No 987 (Abstract), 1994

  28. Takai Y, Kikkawa U, Kaibuchi K, Nishizuka Y: Membrane phospholipid metabolism and signal transduction for protein phosphorylation. Adv Cycl Nucl Prot Phosph Res 18: 119–158, 1984

    Google Scholar 

  29. Hamil KG, Conti M, Shimasaki S, Hall SH: Follicle stimulating hormone regulation of AP- 1: inhibition of c-jun and stimulation of jun-B gene transcription in the rat Sertoli cell. Mol Cell Endocrinol 99: 269–277, 1994

    Google Scholar 

  30. Ginty DD, Bonni A, Greenberg ME: Nerve growth factor activates a ras-dependent protein kinase that stimulates c-fos transcription via phosphorylation of CREB. Cell 77: 713–725, 1994

    Google Scholar 

  31. Marti A, Jehn B, Costello E, Keon N, Ke G, Martin F, Jaggi R: Protein kinase A and AP-1 (c-fos/junD) are induced during apoptosis of mouse mammary epithelial cells. Oncogene 9: 1213–1223, 1994

    Google Scholar 

  32. Quirk SM, Reichert Jr LE: Regulation of the phosphoinositide pathway in cultured Sertoli cells from immature rats. Endocrinol 123: 230–237, 1988

    Google Scholar 

  33. Monaco L, Conti M: Inhibition by phorbol esters and other tumor promoters of the response of the Sertoli cell to FSH: evidence for dual site of action. Mol Cell Endocrinol 49: 227–233, 1987

    Google Scholar 

  34. Monaco L, Adamo S, Conti M: Follicle-stimulating hormone modulation of phosphoinositide turnover in the immature rat Sertoli cells in culture. Endocrinol 123: 2032–2039, 1988

    Google Scholar 

  35. Irving SG, June CH, Zipfel PF, Siebenlist U, Kelly K: Mitogen-induced genes are subject to multiple pathways of regulation in the initial stages of T-cell activation. Mol Cell Biol 9: 1034–1040, 1989

    Google Scholar 

  36. Grasso P, Reichert LE, Jr.: Follicle-stimulating hormone receptormediated uptake of 45Ca2+ by proteoliposomes and cultured rat Sertoli cells: evidence for involvement of voltage-activated and voltage-independent calcium channels. Endocrinol 125: 3029–3036, 1989

    Google Scholar 

  37. Gorczynska E, Handelsman DJ: The role of calcium in follicle-stimulating hormone signal transduction in Sertoli cells. J Biol Chem 266: 23739–23744, 1991

    Google Scholar 

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  1. Meng-Chun Jia

    Present address: National Research Institute for Family Planning, 100081, Beijing, China

Authors and Affiliations

  1. Department of Cell Biology, Georgetown University Medical Center, 20007, Washington, DC, USA

    Meng-Chun Jia, Neelakanta Ravindranath, Vassilios Papadopoulos & Martin Dym

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  1. Meng-Chun Jia
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  2. Neelakanta Ravindranath
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  3. Vassilios Papadopoulos
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  4. Martin Dym
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Jia, MC., Ravindranath, N., Papadopoulos, V. et al. Regulation of c-fos mRNA expression in Sertoli cells by cyclic AMP, calcium, and protein kinase C mediated pathways. Mol Cell Biochem 156, 43–49 (1996). https://doi.org/10.1007/BF00239318

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  • DOI: https://doi.org/10.1007/BF00239318

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