Skip to main content

Advertisement

Log in

Regulation of expression of Sertoli cell glucose transporters 1 and 3 by FSH, IL1β, and bFGF at two different time-points in pubertal development

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Sertoli cells are necessary to provide adequate levels of lactate for germ cell development. Lactate production is hormonally regulated by follicle-stimulating hormone (FSH) and by a large set of intratesticular regulators such as interleukin-1β (IL1β) and basic fibroblast growth factor (bFGF). Little is known regarding the critical step in the production of this metabolite, viz., the entrance of glucose into the cell as mediated by GLUTs. The aim of the present study was to investigate the expression of the glucose transporters GLUT1 and GLUT3 and its possible regulation by FSH, IL1β, and bFGF in Sertoli cells at two different time-points in sexual development. Sertoli cells retaining the ability to undergo mitosis (obtained from 8-day-old rats) and in the process of terminal differentiation (obtained from 20-day-old rats) were examined. Testicular tissue sections and Sertoli cell monolayers obtained from 8- and 20-day-old rats showed positive immunostaining for GLUT1 and GLUT3 proteins. GLUT1 and GLUT3 mRNA levels were detected at the two ages analyzed. Treatment of Sertoli cells obtained from 8- and 20-day-old rats with FSH, IL1β, and bFGF for various periods of time (12, 24, and 48 h) increased GLUT1 without changing GLUT3 mRNA levels. Our results thus show that Sertoli cells express GLUT1 and GLUT3 throughout pubertal development, and that, in Sertoli cells, only GLUT1 is regulated by hormones during pubertal development. Hormonal regulation of GLUT1 expression and consequently glucose uptake and lactate production may be a key molecular event in the regulation of spermatogenesis by hormones.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Burant CF, Davidson NO (1994) GLUT3 glucose transporter isoform in rat testis: localization, effect of diabetes mellitus, and comparison to human testis. Am J Physiol 267:1488–1495

    Google Scholar 

  • Burkhalter J, Fiumelli H, Allaman I, Chatton JY, Martin JL (2003) Brain-derived neurotrophic factor stimulates energy metabolism in developing cortical neurons. J Neurosci 23:8212–8220

    PubMed  CAS  Google Scholar 

  • Carosa E, Radico C, Giansante N, Rossi S, D’Adamo F, Di Stasi SM, Lenzi A, Jannini EA (2005) Ontogenetic profile and thyroid hormone regulation of type-1 and type-8 glucose transporters in rat Sertoli cells. Int J Androl 28:99–106

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Courtens JL, Ploen L (1999) Improvement of spermatogenesis in adult cryptorchid rat testis by intratesticular infusion of lactate. Biol Reprod 61:154–161

    Article  PubMed  CAS  Google Scholar 

  • Czech MP (1995) Molecular actions of insulin on glucose transport. Annu Rev Nutr 15:441–471

    Article  PubMed  CAS  Google Scholar 

  • Froehner SC, Davies A, Baldwin SA, Lienhard GE (1988) The blood-nerve barrier is rich in glucose transporter. J Neurocytol 17:173–178

    Article  PubMed  CAS  Google Scholar 

  • Galardo MN, Riera MF, Pellizzari EH, Cigorraga SB, Meroni SB (2007) The AMP-activated protein kinase activator, 5-aminoimidazole-4-carboxamide-1-b-D-ribonucleoside, regulates lactate production in rat Sertoli cells. J Mol Endocrinol 39:279–288

    Article  PubMed  CAS  Google Scholar 

  • Garcia de Herreros A, Birnbaum MJ (1989) The regulation by insulin of glucose transporter gene expression in 3T3 adipocytes. J Biol Chem 264:9885–9890

    PubMed  CAS  Google Scholar 

  • Gnessi L, Fabbri A, Spera G (1997) Gonadal peptides as mediators of development and functional control of the testis: an integrated system with hormones and local environment. Endocr Rev 18:541–609

    Article  PubMed  CAS  Google Scholar 

  • Gorovits N, Charron M (2003) What we know about facilitative glucose transporters. Biochem Mol Biol Education 31:163–172

    Article  CAS  Google Scholar 

  • Gould GW, Holman GD (1993) The glucose transporter family: structure, function and tissue-specific expression. Biochem J 295:329–341

    PubMed  CAS  Google Scholar 

  • Kamei Y, Tsutsumi O, Yamakawa A, Oka Y, Taketani Y, Imaki J (1999) Maternal epidermal growth factor deficiency causes fetal hypoglycemia and intrauterine growth retardation in mice: possible involvement of placental glucose transporter GLUT3 expression. Endocrinology 140:4236–4243

    Article  PubMed  CAS  Google Scholar 

  • Kokk K, Veräjänkorva E, Wu XK, Tapfer H, Põldoja E, Simovart HE, Pöllänen P (2007) Expression of insulin signaling transmitters and glucose transporters at the protein level in the rat testis. Ann N Y Acad Sci 1095:262–273

    Article  PubMed  CAS  Google Scholar 

  • Kol S, Ben-Shlomo I, Ruutiainen K, Ando M, Davies-Hill TM, Rohan RM, Simpson IA, Adashi EY (1997) The midcycle increase in ovarian glucose uptake is associated with enhanced expression of glucose transporter 3. Possible role for interleukin-1, a putative intermediary in the ovulatory process. J Clin Invest 99:2274–2283

    Article  PubMed  CAS  Google Scholar 

  • Kumar A, Xiao YP, Laipis PJ, Fletcher BS, Frost SC (2004) Glucose deprivation enhances targeting of GLUT1 to lipid rafts in 3T3-L1 adipocytes. Am J Physiol Endocrinol Metab 286:568–576

    Article  Google Scholar 

  • Labarca C, Paigen K (1980) A simple, rapid, and sensitive DNA assay procedure. Anal Biochem 102:344–352

    Article  PubMed  CAS  Google Scholar 

  • Medina RA, Meneses AM, Vera JC, Gúzman C, Nualart F, Rodriguez F, los Angeles Garcia M de, Kato S, Espinoza N, Monsó C, Carvajal A, Pinto M, Owen GI (2004) Differential regulation of glucose transporter expression by estrogen and progesterone in Ishikawa endometrial cancer cells. J Endocrinol 182:467–478

    Article  PubMed  CAS  Google Scholar 

  • Meroni SB, Riera MF, Pellizzari EH, Cigorraga SB (2002) Regulation of rat Sertoli cell function by FSH: possible role of phosphatidylinositol 3-kinase/protein kinase B pathway. J Endocrinol 174:195–204

    Article  PubMed  CAS  Google Scholar 

  • Okamoto Y, Sakata M, Yamamoto T, Nishio Y, Adachi K, Ogura K, Yamaguchi M, Takeda T, Tasaka K, Murata Y (2001) Involvement of nuclear transcription factor Sp1 in regulating glucose transporter-1 gene expression during rat trophoblast differentiation. Biochem Biophys Res Commun 288:940–948

    Article  PubMed  CAS  Google Scholar 

  • Parvinen M (1982) Regulation of the seminiferous epithelium. Endocr Rev 3:404–417

    Article  PubMed  CAS  Google Scholar 

  • Piroli GG, Grillo CA, Hoskin EK, Znamensky V, Katz EB, Milner TA, McEwen BS, Charron MJ, Reagan LP (2002) Peripheral glucose administration stimulates the translocation of GLUT8 glucose transporter to the endoplasmic reticulum in the rat hippocampus. J Comp Neurol 452:103–114

    Article  PubMed  CAS  Google Scholar 

  • Reagan LP, Gorovits N, Hoskin EK, Alves SE, Katz EB, Grillo CA, Piroli GG, McEwen BS, Charron MJ (2000) Localization and regulation of GLUTx1 glucose transporter in the hippocampus of streptozotocin diabetic rats. Proc Natl Acad Sci USA 98:2820–2825

    Article  Google Scholar 

  • Riera MF, Meroni SB, Gómez GE, Schteingart HF, Pellizzari EH, Cigorraga SB (2001) Regulation of lactate production by FSH, IL1beta, and TNFalpha in rat Sertoli cells. Gen Comp Endocrinol 122:88–97

    Article  PubMed  CAS  Google Scholar 

  • Riera MF, Meroni SB, Schteingart HF, Pellizzari EH, Cigorraga SB (2002) Regulation of lactate production and glucose transport as well as of glucose transporter 1 and lactate dehydrogenase A mRNA levels by basic fibroblast growth factor in rat Sertoli cells. J Endocrinol 173:335–343

    Article  PubMed  CAS  Google Scholar 

  • Schteingart HF, Meroni SB, Pellizzari EH, Pérez AL, Cigorraga SB (1995) Regulation of Sertoli cell aromatase activity by cell density and prolonged stimulation with FSH, EGF, insulin and IGF-I at different moments of pubertal development. J Steroid Biochem Mol Biol 52:375–381

    Article  PubMed  CAS  Google Scholar 

  • Shen S, Wertheimer E, Sampson SR, Tennenbaum T (2000) Characterization of glucose transport system in keratinocytes: insulin and IGF-1 differentially affect specific transporters. J Invest Dermatol 115:949–954

    Article  PubMed  CAS  Google Scholar 

  • Shikhman AR, Brinson DC, Valbracht J, Lotz MK (2001) Cytokine regulation of facilitated glucose transport in human articular chondrocytes. J Immunol 167:7001–7008

    PubMed  CAS  Google Scholar 

  • Sweeney G, Somwar R, Ramlal T, Volchuk A, Ueyama A, Klip A (1999) An inhibitor of p38 mitogen-activated protein kinase prevents insulin-stimulated glucose transport but not glucose transporter translocation in 3T3-L1 adipocytes and L6 myotubes. J Biol Chem 274:10071–10078

    Article  PubMed  CAS  Google Scholar 

  • Takata K, Kasahara T, Kasahara M, Ezaki O, Hirano H (1992a) Localization of erythrocyte/HepG2-type glucose transporter (GLUT1) in human placental villi. Cell Tissue Res 267:407–412

    Article  PubMed  CAS  Google Scholar 

  • Takata K, Kasahara T, Kasahara M, Ezaki O, Hirano H (1992b) Ultracytochemical localization of the erythrocyte/HepG2-type glucose transporter (GLUT1) in cells of the blood-retinal barrier in the rat. Invest Ophthalmol Vis Sci 33:377–383

    PubMed  CAS  Google Scholar 

  • Ulisse S, Jannini EA, Pepe M, De Matteis S, D’Armiento M (1992) Thyroid hormone stimulates glucose transport and GLUT1 mRNA in rat Sertoli cells. Mol Cell Endocrinol 87:131–137

    Article  PubMed  CAS  Google Scholar 

  • Yano H, Seino Y, Inagaki N, Hinokio Y, Yamamoto T, Yasuda K, Masuda K, Someya Y, Imura H (1991) Tissue distribution and species difference of the brain type glucose transporter (GLUT3). Biochem Biophys Res Commun 174:470–477

    Article  PubMed  CAS  Google Scholar 

  • Yu ZW, Buren J, Enerback S, Nilsson E, Samuelsson L, Eriksson JW (2001) Insulin can enhance GLUT4 gene expression in 3T3-F442A cells and this effect is mimicked by vanadate but counteracted by cAMP and high glucose-potential implications for insulin resistance. Biochim Biophys Acta 1535:174–185

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors express their gratitude to Dr. Birnbaum (Philadelphia, USA) for providing GLUT1 cDNA, to Dr. Nagamatsu (Tokyo, Japan) for providing GLUT3 cDNA, and to Dr. Carter-Su (Michigan, USA) for providing the GLUT1 antibody. The technical help of Mercedes Astarloa is also gratefully acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Silvina Beatriz Meroni.

Additional information

The work was supported by grants from the Agencia Nacional de Promoción Científica y Tecnológica (PICT 25365) and CONICET (PIP 5479), Argentina. R.M.F., C.H.E., C.S.B., and M.S.B. are established investigators of CONICET. G.M.N. is a recipient of a CONICET fellowship and a teaching assistant of Departamento de Bioquímica Humana, Facultad de Medicina, UBA.

The authors declare that there is no conflict of interest that would prejudice the impartiality of this scientific work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Galardo, M.N., Riera, M.F., Pellizzari, E.H. et al. Regulation of expression of Sertoli cell glucose transporters 1 and 3 by FSH, IL1β, and bFGF at two different time-points in pubertal development. Cell Tissue Res 334, 295–304 (2008). https://doi.org/10.1007/s00441-008-0656-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-008-0656-y

Keywords

Navigation