Rapid Responses to Reverse T3 Hormone in Immature Rat Sertoli Cells: Calcium Uptake and Exocytosis Mediated by Integrin

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Zanatta, Ana Paula ^a   Zanatta, Leila ^b   Gonçalves, Renata ^a   Zamoner, Ariane ^a   Silva, Fátima Regina Mena Barreto ^a  

^a FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^b Universidade Comunitaria Regional de Chapeco   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

3,3',5' TRIIODOTHYRONINE; ALPHA5 INTEGRIN; ANTHRACENE; ARGINYLGLYCYLASPARTIC ACID; CALCIUM; CALCIUM CHANNEL T TYPE; FLUNARIZINE; INTEGRIN; INTEGRIN RECEPTOR; LIGAND; LIOTHYRONINE; MEMBRANE RECEPTOR; THYROID HORMONE; THYROID HORMONE RECEPTOR; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED CHLORIDE CHANNEL;

ANIMAL EXPERIMENT; ARTICLE; CALCIUM TRANSPORT; CELL MEMBRANE; CELLULAR SECRETION; CONTROLLED STUDY; EXOCYTOSIS; GENE EXPRESSION; HORMONE RESPONSE; INCUBATION TIME; MALE; NONHUMAN; RAT; SERTOLI CELL;

ANIMALS; BIOLOGICAL TRANSPORT; CALCIUM; CALCIUM CHANNELS; CELL MEMBRANE; CHLORIDE CHANNELS; EXOCYTOSIS; INTEGRINS; MALE; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; PROTEIN KINASE C; RATS; RATS, WISTAR; SERTOLI CELLS; TIME FACTORS; TRIIODOTHYRONINE, REVERSE;

EID: 84885397397     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0077176     Document Type: Article

References (64)

1. Gereben B, Zeöld A, Dentice M, Salvatore D, Bianco AC, (2008) Activation and inactivation of thyroid hormone by deiodinases: local action with general consequences. Endocrinol Rev 65: 570-590. PubMed: 17989921.
2. Dentice M, Salvatore D, (2011) Deiodinases: the balance of thyroid hormone - Local impact of thyroid hormone inactivation. J Endocrinol 209: 273-282. doi:10.1530/JOE-11-0002. PubMed: 21398344.
3. Bates JM, St Germain DL, Galton VA, (1999) Expression profiles of the three iodothyronine deiodinases, D1, D2, and D3, in the developing rat. Endocrinology 140: 844-851. doi:10.1210/en.140.2.844. PubMed: 9927314.
4. Jannini EA, Carosa E, Rucci N, Screponi E, D'Armiento M, (1999) Ontogeny and regulation of variant thyroid hormone receptor isoforms in developing rat testis. J Endocrinol Invest 22: 843-848. PubMed: 10710271.
5. Holsberger DR, Cooke PS, (2005) Understanding the role of thyroid hormone in Sertoli cell development: a mechanistic hypothesis. Cell Tissue Res 322: 133-140. doi:10.1007/s00441-005-1082-z. PubMed: 15856309.
6. Lazar MA, (1993) Thyroid hormone receptors: multiple forms, multiple possibilities. Endocrinol Rev 14: 184-193. doi:10.1210/er.14.2.184. PubMed: 8325251.
7. Kavok NS, Krasilnikova OA, Babenko NA, (2001) Thyroxine signal transduction in liver cells involves phospholipase C and phospholipase D activation: genomic independent action of thyroid hormone. BMC Cell Biol 2: 5. doi:10.1186/1471-2121-2-5. PubMed: 11312999.
8. Aranda A, Pascual A, (2001) Nuclear hormone receptors and gene expression. Physiol Rev 81: 1269-1304. PubMed: 11427696.
9. Davis PJ, Davis FB, Cody V, (2005) Membrane receptors mediating thyroid hormone action. Trends Endocrinol Metab 16: 429-435. doi:10.1016/j.tem.2005.09.007. PubMed: 16214361.
10. Scapin S, Leoni S, Spagnuolo S, Gnocchi D, De Vito P, et al. (2010) Short-term effects of thyroid hormones during development: Focus on signal transduction. Steroids 75: 576-584. doi:10.1016/j.steroids.2009.10.013. PubMed: 19900468.
11. Silva FR, Leite LD, Barreto KP, D'Agostini C, Zamoner A, (2001) Effect of 3,5,3′-triiodo-L-thyronine on amino acid accumulation and membrane potential in Sertoli cells on the rat testis. Life Sci 69: 977-986. doi:10.1016/S0024-3205(01)01186-9. PubMed: 11488410.
12. Volpato KC, Menegaz D, Leite LD, Barreto KP, Garcia EV, et al. (2004) Involvement of K+ channels and calcium-dependent pathways in the action of T3 on amino acid accumulation and membrane potential in Sertoli cells of immature rat testis. Life Sci 74: 1277-1288. doi:10.1016/j.lfs.2003.08.005. PubMed: 14697410.
13. Menegaz D, Zamoner A, Royer C, Leite LD, Bortolotto ZA, et al. (2006) Rapid responses to thyroxine in the testis: active protein synthesis-independent pathway. Mol Cell Endocrinol 246: 128-134. doi:10.1016/j.mce.2005.11.019. PubMed: 16387420.
14. Menegaz D, Royer C, Rosso A, De Souza AZP, Dos Santos ARS, et al. (2010) Rapid stimulatory effect of thyroxine on plasma membrane transport systems: Calcium uptake and neutral amino acid accumulation in immature rat testis. Int J Biochem Cell Biol 42: 1046-1051. doi:10.1016/j.biocel.2010.03.015. PubMed: 20348014.
15. Zamoner A, Corbelini PF, Funchal C, Menegaz D, Silva FR, et al. (2005) Involvement of calcium-dependent mechanisms in T3-induced phosphorylation of vimentin of immature rat testis. Life Sci 77: 3321-3335. doi:10.1016/j.lfs.2005.05.042. PubMed: 15985269.
16. Zanatta L, Zamoner A, Gonçalves R, Zanatta AP, Bouraïma-Lelong H, et al. (2011) 1α,25-Dihydroxyvitamin D(3) signaling pathways on calcium uptake in 30-day-old rat Sertoli cells. Biochemistry 50: 10284-10292. doi:10.1021/bi201113n. PubMed: 22035182.
17. Zanatta L, Zamoner A, Gonçalves R, Zanatta AP, Bouraïma-Lelong H, et al. (2011) Effect of 1α,25-dihydroxyvitamin D3 in plasma membrane targets in immature rat testis: ionic channels and gamma-glutamyl transpeptidase activity. Arch Biochem Biophys 515: 46-53. doi:10.1016/j.abb.2011.09.001. PubMed: 21933661.
18. Rosso A, Pansera M, Zamoner A, Zanatta L, Bouraïma-Lelong H, et al. (2012) 1α,25(OH)2-Vitamin D3 stimulates rapid plasma membrane calcium influx via MAPK activation in immature rat Sertoli cells. Biochimie 94: 146-154. doi:10.1016/j.biochi.2011.10.001. PubMed: 22015633.
19. Zamoner A, Bruno AN, Casali EA, Corbelini PF, Diniz GP, et al. (2006) Genomic-independent action of thyroid hormones on NTPDase activities in Sertoli cell cultures congenital hypothyroid rats. Life Sci 80: 51-58. doi:10.1016/j.lfs.2006.08.020. PubMed: 16978660.
20. Lei J, Nowbar S, Mariash CN, Ingbar DH, (2003) Thyroid hormone stimulates Na, K-ATPase activity and its plasma membrane insertion in rat alveolar epithelial cells. Am J Physiol 285: L762-L772.
21. Lei J, Mariash CN, Bhargava M, Wattenberg EV, Ingbar DH, (2008) T3 increases Na, K-ATPase activity via MAPK/ERK1/2-dependent pathway in rat adult alveolar epithelial cells. Am J Physiol 294: L749-L754.
22. Scapin S, Leoni S, Spagnuolo S, Fiore AM, Incerpi S, (2009) Short-term effects of thyroid hormone on the Na, K-ATPase activity of chick embryo hepatocytes during development: focus on signal transduction. Am J Physiol 296: C4-C12.
23. Zhu XG, Hanover JA, Hager GL, Cheng SY, (1998) Hormone-induced translocation of thyroid hormone receptors in living cells visualized using a receptor green fluorescent protein chimera. J Biol Chem 273: 27058-27063. doi:10.1074/jbc.273.42.27058. PubMed: 9765220.
24. Bunn CF, Neidig JA, Freidinger KE, Stankiewicz TA, Weaver BS, et al. (2001) Nucleocytoplasmic shuttling of the thyroid hormone receptor α. Mol Endocrinol 15: 512-533. doi:10.1210/me.15.4.512. PubMed: 11266504.
25. Farwell AP, Dubord-Tomasetti SA, Pietrzykowski AZ, Leonard JL, (2006) Dynamic nongenomic actions of thyroid hormone in the developing rat brain. Endocrinology 147: 2567-2574. doi:10.1210/en.2005-1272. PubMed: 16469804.
26. Russell LD, Griswold MD, (1993) The Sertoli Cell, third ed. Clearwater, FL: Cache River Press.
27. Lalevée N, Pluciennik F, Joffre M, (1997) Voltage-dependent calcium current with properties of T-type current in Sertoli cells from immature rat testis in primary cultures. Biol Reprod 56: 680-687. doi:10.1095/biolreprod56.3.680. PubMed: 9047014.
28. Lalevée N, Joffre M, (1999) Inhibition by cAMP of calcium-activated chloride currents in cultured Sertoli cells from immature testis. J Membr Biol 169: 167-174. doi:10.1007/s002329900528. PubMed: 10354463.
29. Taranta A, Morena AR, Barbacci E, D'Agostino A, (1997) ω-Conotoxin-sensitive Ca2+ voltage-gated channels modulate protein secretion in cultured rat Sertoli cells. Mol Cell Endocrinol 126: 117-123. doi:10.1016/S0303-7207(96)03973-1. PubMed: 9089649.
30. Berridge MJ, Bootman MD, Roderick HL, (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4: 517-529. doi:10.1038/nrm1155. PubMed: 12838335.
31. Voets T, (2000) Dissection of three Ca2+-dependent steps leading to secretion in chromaffin cells from mouse adrenal slices. Neuron 28: 537-545. doi:10.1016/S0896-6273(00)00131-8. PubMed: 11144362.
32. Fujisawa M, (2001) Cell-to-cell cross-talk in the testis. Urol Res 29: 144-151. doi:10.1007/s002400100179. PubMed: 11482437.
33. Gorczyńska-Fjälling E, (2004) The role of calcium in signal transduction processes in Sertoli cells. Reprod Biol 4: 219-241. PubMed: 15592583.
34. Zanatta AP, Zanatta L, Gonçalves R, Zamoner A, Silva FRMB, (2013) Integrin participates in the effect of thyroxine on plasma membrane in immature rat testis. Biochim Biophys Acta Gen Subj 1830: 2629-2637. doi:10.1016/j.bbagen.2012.10.022. PubMed: 23137442.
35. Farwell AP, Leonard JL, (2005) Nongenomic actions of thyroid hormone during fetal brain development. Curr Opin. Endocrinol Metab 12: 17-22.
36. Dorrington JH, Roller NF, Fritz IB, (1975) Effects of follicle-stimulating hormone on cultures of Sertoli cell preparations. Mol Cell Endocrinol 3: 57-70. doi:10.1016/0303-7207(75)90031-3. PubMed: 168104.
37. Galdieri M, Ziparo E, Palombi F, Russo M, Stefanini M, (1981) Pure Sertoli cell cultures: a new model for the study of somatic-germ cell interactions. J Androl 5: 249-254.
38. Lin HY, Sun M, Tang HY, Lin C, Luidens MK, et al. (2009) L-thyroxine vs. 3,5,3'-triiodo-l-thyronine and cell proliferation: activation of mitogen-activated protein kinase and phosphatidylinositol 3-kinase. Am J Physiol Cell Physiol 296: C980-C991. doi:10.1152/ajpcell.00305.2008. PubMed: 19158403.
39. Zamoner A, Pierozan P, Vidal LF, Lacerda BA, Dos Santos NG, et al. (2008) Vimentin phosphorylation as a target of cell signaling mechanisms induced by 1alpha,25-dihydroxyvitamin D3 in immature rat testes. Steroids 73: 1400-1408. doi:10.1016/j.steroids.2008.07.002. PubMed: 18687349.
40. Batra S, Sjögren C, (1983) Effect of estrogen treatment on calcium uptake by the rat uterine smooth muscle. Life Sci 32: 315-319. doi:10.1016/0024-3205(83)90076-0. PubMed: 6827896.
41. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ, (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193: 265-267. PubMed: 14907713.
42. Menegaz D, Barrientos-Duran A, Kline A, Silva FRMB, Norman AW, et al. (2010) 1α,25(OH)2-Vitamin D3 stimulation of secretion via chloride channel activation in Sertoli cells. J Steroid Biochem Mol Biol 74: 264-269.
43. Yen M, (2001) Physiological and molecular basis of thyroid hormone action. Physiol Rev 81: 1097-1142. PubMed: 11427693.
44. St Germain DL, Galton VA, Hernandez A, (2009) Defining the role of the iodothyronine deiodinases: current concepts and challenges. Endocrinology 150: 1097-1107. PubMed: 19179439.
45. Cheng SY, Leonard JL, Davis PJ, (2010) Molecular aspects of thyroid hormone actions. Endocrinol Rev 31: 139-170. doi:10.1210/er.2009-0007. PubMed: 20051527.
46. Zamoner A, Pessoa-Pureur R, Silva FR, (2011) Membrane-initiated actions of thyroid hormones on the male reproductive system. Life Sci 89: 507-514. doi:10.1016/j.lfs.2011.04.006. PubMed: 21557952.
47. Anguiano B, Aranda N, Delgado G, Aceves C, (2008) Epididymis expresses the highest 5-deiodinase activity in the male reproductive system: kinetic characterization, distribution, and hormonal regulation. Endocrinology 149: 4209-4217. doi:10.1210/en.2007-1679. PubMed: 18467445.
48. Köhrle J, (1999) Local activation and inactivation of thyroid hormones: the deiodinase family. Mol Cell Endocrinol 151: 103-119. doi:10.1016/S0303-7207(99)00040-4. PubMed: 10411325.
49. Van der Geyten S, Van den Eynde I, Segers IB, Kühn ER, Darras VM, (2002) Diferential expression of iodothyronine deiodinases in chicken tissues during the last week of embryonic development. Gen Comp Endocrinol 128: 65-73. doi:10.1016/S0016-6480(02)00065-5. PubMed: 12270789.
50. Bergh JJ, Lin HY, Lansing L, Mohamed SN, Davis FB, et al. (2005) Integrin αvβ3 contains a cell surface receptor site for thyroid hormone that is linked to activation of mitogen-activated protein kinase and induction of angiogenesis. Endocrinology 146: 2864-2871. doi:10.1210/en.2005-0102. PubMed: 15802494.
51. Plow EF, Haas TA, Zhang L, Loftus J, Smith JW, (2000) Ligand binding to integrins. J Biol Chem 275: 21785-21788. doi:10.1074/jbc.R000003200. PubMed: 10801897.
52. Tsou R, Isik FF, (2001) Integrin activation is required for VEGF and FGF receptor protein presence on human microvascular endothelial cells. Mol Cell Biochem 224: 81-89. doi:10.1023/A:1011947301849. PubMed: 11693202.
53. Vinatier D, (1995) Integrins and reproduction. Eur J Obstet Gynecol Reprod Biol 59: 71-81. doi:10.1016/0028-2243(94)01987-I. PubMed: 7781865.
54. Siu MK, Cheng CY, (2004) Interactions of proteases, protease inhibitors, and the b1 integrin/laminin protein complex in the regulation of ectoplasmic specialization dynamics in the testis. Biol Reprod 70: 945-964. PubMed: 14645107.
55. Lee JH, Kim JU, Kim C, Min CK, (2010) Inhibitory actions of mibefradil on steroidogenesis in mouse Leydig cells: involvement of Ca2+ entry via the T-type Ca2+ channel. Asian J Androl 12: 807-813. doi:10.1038/aja.2010.51. PubMed: 20694017.
56. Zamoner A, Royer C, Barreto KP, Pessoa-Pureur R, Silva FR, (2007) Ionic involvement and kinase activity on the mechanism of nongenomic action of thyroid hormones on 45 Ca2+ uptake in cerebral cortex from young rats. Neurosci Res 57: 98-103. doi:10.1016/j.neures.2006.09.012. PubMed: 17067709.
57. Chemin J, Traboulsie A, Lory P, (2006) Molecular pathways underlying the modulation of T-type calcium channels by neurotransmitters and hormones. Cell Calcium 40: 121-134. doi:10.1016/j.ceca.2006.04.015. PubMed: 16797700.
58. Iftinca MC, (2011) Neuronal T-type calcium channels: what's new? J Med Life 4: 126-138. PubMed: 21776294.
59. Zanatta L, Goulart PB, Gonçalves R, Pierozan P, Winkelmann-Duarte EC, et al. (2012) 1α,25-Dihydroxyvitamin D(3) mechanism of action: Modulation of L-type calcium channels leading to calcium uptake and intermediate filament phosphorylation in cerebral cortex of young rats. Biochim Biophys Acta 1823: 1708-1719. doi:10.1016/j.bbamcr.2012.06.023. PubMed: 22743040.
60. Costa RR, dos Reis RI, Aguiar JF, Varanda WA, (2011) Luteinizing hormone (LH) acts through PKA and PKC to modulate T-type calcium currents and intracellular calcium transients in mice Leydig cells. Cell Calcium 49: 191-199. doi:10.1016/j.ceca.2011.02.003. PubMed: 21367452.
61. Schönwasser DC, Marais RM, Marshall CJ, Parker PJ, (1998) Activation of the mitogen-activated protein kinase/extracellular signal-regulated kinase pathway by conventional, novel, and atypical protein kinase C isotypes. Mol Cell Biol 18: 790-798. PubMed: 9447975.
62. Weiss N, Hameed S, Fernández-Fernández JM, Fablet K, Karmazinova M, et al. (2012) Ca(v)3.2/syntaxin-1A signaling complex controls T-type channel activity and low-threshold exocytosis. J Biol Chem 287: 2810-2818. doi:10.1074/jbc.M111.290882. PubMed: 22130660.
63. Mahapatra S, Calorio C, Vandael DH, Marcantoni A, Carabelli V, et al. (2012) Calcium channel types contributing to chromaffin cell excitability, exocytosis and endocytosis. Cell Calcium 51: 321-330. doi:10.1016/j.ceca.2012.01.005. PubMed: 22317919.
64. Linnertz R, Wurm A, Pannicke T, Krügel K, Hollborn M, et al. (2011) Activation of voltage-gated Na+ and Ca2+ channels is required for glutamate release from retinal glial cells implicated in cell volume regulation. Neuroscience 188: 23-34. doi:10.1016/j.neuroscience.2011.04.058. PubMed: 21575684.