1,345
Views
3
CrossRef citations to date
0
Altmetric
Research Articles

Triiodothyronine stimulates VEGF expression and secretion via steroids and HIF-1α in murine Leydig cells

, , &
Pages 191-201 | Received 26 Jul 2017, Accepted 17 Dec 2017, Published online: 08 Feb 2018

References

  • Anand RJ, Paust HJ, Altenpohl K, Mukhopadhyay AK. 2003. Regulation of vascular endothelial growth factor production by Leydig cells in vitro: the role of protein kinase A and mitogen-activated protein kinase cascade. Biol Reprod. 68(5):1663–1673.
  • Ayub M, Levell MJ. 1987. Inhibition of testicular 17 alpha-hydroxylase and 17,20-lyase but not 3 beta-hydroxysteroid dehydrogenase-isomerase or 17 beta-hydroxysteroid oxidoreductase by ketoconazole and other imidazole drugs. J Steroid Biochem. 28(5):521–531.
  • Caires KC, De Avila JM, Cupp AS, McLean DJ. 2012. VEGFA family isoforms regulate spermatogonial stem cell homeostasis in vivo. Endocrinology. 153(2):887–900.
  • Carlsson PO, Palm F, Andersson A, Liss P. 2001. Markedly decreased oxygen tension in transplanted rat pancreatic islets irrespective of the implantation site. Diabetes. 50(3):489–495.
  • Chang CL, Fung HP. 2002. Effects of ketoconazole on progesterone and cAMP production in MA-10 mouse Leydig tumor cells. Biol Pharm Bull. 25(6):794–797.
  • Chaudhary LR, Stocco DM. 1989. Inhibition of hCG- and cAMP-stimulated progesterone production in MA-10 mouse Leydig tumor cells by ketoconazole. Biochem Int. 18(1):251–262.
  • Chen CY, Chung IH, Tsai MM, Tseng YH, Chi HC, Tsai CY, Lin YH, Wang YC, Chen CP, Wu TI, et al. 2014. Thyroid hormone enhanced human hepatoma cell motility involves brain-specific serine protease 4 activation via ERK signaling. Mol Cancer. 13:162.
  • Classen-Linke I, Alfer J, Krusche CA, Chwalisz K, Rath W, Beier HM. 2000. Progestins, progesterone receptor modulators, and progesterone antagonists change VEGF release of endometrial cells in culture. Steroids. 65(10–11):763–771.
  • Eisermann K, Broderick CJ, Bazarov A, Moazam MM, Fraizer GC. 2013. Androgen up-regulates vascular endothelial growth factor expression in prostate cancer cells via an Sp1 binding site. Mol Cancer. 12:7.
  • El-Hefnawy T, Manna PR, Luconi M, Baldi E, Slotte JP, Huhtaniemi I. 2000. Progesterone action in a murine Leydig tumor cell line (mLTC-1), possibly through a nonclassical receptor type. Endocrinology. 141(1):247–255.
  • Fandrey J, Pagel H, Frede S, Wolff M, Jelkmann W. 1994. Thyroid hormones enhance hypoxia-induced erythropoietin production in vitro. Exp Hematol. 22(3):272–277.
  • Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, Koos RD, Semenza GL. 1996. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol. 16(9):4604–4613.
  • Hwang GS, Wang SW, Tseng WM, Yu CH, Wang PS. 2007. Effect of hypoxia on the release of vascular endothelial growth factor and testosterone in mouse TM3 Leydig cells. Am J Physiol Endocrinol Metab. 292(6):E1763–E1769.
  • Hyder SM, Stancel GM, Chiappetta C, Murthy L, Boettger-Tong HL, Makela S. 1996. Uterine expression of vascular endothelial growth factor is increased by estradiol and tamoxifen. Cancer Res. 56(17):3954–3960.
  • Hyder SM, Murthy L, Stancel GM. 1998. Progestin regulation of vascular endothelial growth factor in human breast cancer cells. Cancer Res. 58(3):392–395.
  • Iitaka M, Miura S, Yamanaka K, Kawasaki S, Kitahama S, Kawakami Y, Kakinuma S, Oosuga I, Wada S, Katayama S. 1998. Increased serum vascular endothelial growth factor levels and intrathyroidal vascular area in patients with Graves’ disease and Hashimoto’s thyroiditis. J Clin Endocrinol Metab. 83(11):3908–3912.
  • Jana NR, Bhattacharya S. 1994. Binding of thyroid hormone to the goat testicular Leydig cell induces the generation of a proteinaceous factor which stimulates androgen release. J Endocrinol. 143(3):549–556.
  • Klotz T, Vorreuther R, Heidenreich A, Zumbé J, Engelmann U. 1996. Testicular tissue oxygen pressure. J Urol. 155(4):1488–1491.
  • Koh MY, Spivak-Kroizman T, Venturini S, Welsh S, Williams RR, Kirkpatrick DL, Powis G. 2008. Molecular mechanisms for the activity of PX-478, an antitumor inhibitor of the hypoxia-inducible factor-1alpha. Mol Cancer Ther. 7(1):90–100.
  • Konieczna A, Szczepańska A, Sawiuk K, Węgrzyn G, Łyżeń R. 2015. Effects of partial silencing of genes coding for enzymes involved in glycolysis and tricarboxylic acid cycle on the enterance of human fibroblasts to the S phase. BMC Cell Biol. 16:16.
  • Kumar A, Rani L, Dhole B, Chaturvedi PK. 2012. Oxygen as a regulator of MA-10 cell functions: effect of cobalt chloride on vascular endothelial growth factor production. Andrologia. 44(Suppl 1):615–620.
  • Kumar A, Rani L, Dhole B. 2014. Role of oxygen in the regulation of Leydig tumor derived MA-10 cell steroid production: the effect of cobalt chloride. Syst Biol Reprod Med. 60(2):112–118.
  • Levine AC, Liu XH, Greenberg PD, Eliashvili M, Schiff JD, Aaronson SA, Holland JF, Kirschenbaum A. 1998. Androgens induce the expression of vascular endothelial growth factor in human fetal prostatic fibroblasts. Endocrinology. 139(11):4672–4678.
  • Lysiak JJ, Kirby JL, Tremblay JJ, Woodson RI, Reardon MA, Palmer LA, Turner TT. 2009. Hypoxia-inducible factor-1alpha is constitutively expressed in murine Leydig cells and regulates 3beta-hydroxysteroid dehydrogenase type 1 promoter activity. J Androl. 30(2):146–156.
  • Ma Y, Freitag P, Zhou J, Brüne B, Frede S, Fandrey J. 2004. Thyroid hormone induces erythropoietin gene expression through augmented accumulation of hypoxia-inducible factor-1. Am J Physiol Regul Integr Comp Physiol. 287(3):R600–R607.
  • Mabjeesh NJ, Willard MT, Frederickson CE, Zhong H, Simons JW. 2003. Androgens stimulate hypoxia-inducible factor 1 activation via autocrine loop of tyrosine kinase receptor/phosphatidylinositol 3’-kinase/protein kinase B in prostate cancer cells. Clin Cancer Res. 9(7):2416–2425.
  • Manna PR, Tena-Sempere M, Huhtaniemi IT. 1999. Molecular mechanisms of thyroid hormone-stimulated steroidogenesis in mouse leydig tumor cells. Involvement of the steroidogenic acute regulatory (StAR) protein. J Biol Chem. 274(9):5909–5918.
  • Manna PR, Kero J, Tena-Sempere M, Pakarinen P, Stocco DM, Huhtaniemi IT. 2001. Assessment of mechanisms of thyroid hormone action in mouse Leydig cells: regulation of the steroidogenic acute regulatory protein, steroidogenesis, and luteinizing hormone receptor function. Endocrinology. 142(1):319–331.
  • Maran RR, Arunakaran J, Aruldhas MM. 2000. T3 directly stimulates basal and modulates LH induced testosterone and oestradiol production by rat Leydig cells in vitro. Endocr J. 47(4):417–428.
  • Otto T, Fandrey J. 2008. Thyroid hormone induces hypoxia-inducible factor 1alpha gene expression through thyroid hormone receptor beta/retinoid x receptor alpha-dependent activation of hepatic leukemia factor. Endocrinology. 149(5):2241–2250.
  • Richard C, Kim G, Koikawa Y, Salm SN, Tsujimura A, Wilson EL, Moscatelli D. 2002. Androgens modulate the balance between VEGF and angiopoietin expression in prostate epithelial and smooth muscle cells. Prostate. 50(2):83–91.
  • Salva A, Klinefelter GR, Hardy MP. 2001. Purification of rat leydig cells: increased yields after unit-gravity sedimentation of collagenase-dispersed interstitial cells. J Androl. 22(4):665–671.
  • Sargent KM, Clopton DT, Lu N, Pohlmeier WE, Cupp AS. 2016. VEGFA splicing: divergent isoforms regulate spermatogonial stem cell maintenance. Cell Tissue Res. 363(1):31–45.
  • Schwarzenbach H, Chakrabarti G, Paust HJ, Mukhopadhyay AK. 2004. Gonadotropin-mediated regulation of the murine VEGF expression in MA-10 Leydig cells. J Androl. 25(1):128–139.
  • Sterling K, Brenner MA, Sakurada T. 1980. Rapid effect of triiodothyronine on the mitochondrial pathway in rat liver in vivo. Science. 210(4467):340–342.
  • Sufi SB, Donaldson A, Jeffcoate SL. 1993. Programme for the provision of matched assay reagents for the radioimmunoassay of hormones in reproductive physiology. In: Method manual. Geneva, Switzerland: World Health Organization.
  • Veldscholte J, Voorhorst-Ogink MM, Bolt-De Vries J, Van Rooij HC, Trapman J, Mulder E. 1990. Unusual specificity of the androgen receptor in the human prostate tumor cell line LNCaP: high affinity for progestagenic and estrogenic steroids. Biochim Biophys Acta. 1052(1):187–194.
  • Yu DY, Cringle SJ. 2006. Oxygen distribution in the mouse retina. Invest Ophthalmol Vis Sci. 47(3):1109–1112.
  • Zamoner A, Barreto KP, Filho DW, Sell F, Woehl VM, Guma FC, Silva FR, Pessoa-Pureur R. 2007. Hyperthyroidism in the developing rat testis is associated with oxidative stress and hyperphosphorylated vimentin accumulation. Mol Cell Endocrinol. 267(1–2):116–126.
  • Zamoner A, Barreto KP, Filho DW, Sell F, Woehl VM, Guma FC, Pessoa-Pureur R, Silva FR. 2008. Propylthiouracil-induced congenital hypothyroidism upregulates vimentin phosphorylation and depletes antioxidant defenses in immature rat testis. J Mol Endocrinol. 40(3):125–135.
  • Zhang L, Cooper-Kuhn CM, Nannmark U, Blomgren K, Kuhn HG. 2010. Stimulatory effects of thyroid hormone on brain angiogenesis in vivo and in vitro. J Cereb Blood Flow Metab. 30(2):323–335.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.