Calcium signaling of thyrocytes is modulated by TSH through calcium binding protein expression

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1803, Issue 3, 2010, Pages 352-360

  Lorenz, Stephan ^a,b   Eszlinger, Markus ^a   Paschke, Ralf ^a   Aust, Gabriela ^a   Weick, Michael ^a   Führer, Dagmar ^a   Krohn, Knut ^a,b  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b UNIVERSITY HOSPITAL LEIPZIG   (Germany)

Author keywords

Calcium signaling; Fischer rat thyroid FRTL 5; Follicular thyroid cancer FTC133; Microarray study; Primary human thyrocyte; S100A4 calcium binding protein; shRNA knockdown

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ION; CALCYCLIN; CALPHOBINDIN II; CALVASCULIN; COMPLEMENTARY DNA; HYDROGEN PEROXIDE; PROTEIN C FOS; PURINERGIC P2Y RECEPTOR; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SHORT HAIRPIN RNA; THAPSIGARGIN; THYROTROPIN;

ANIMAL CELL; ARTICLE; CALCIUM BINDING; CALCIUM SIGNALING; CANCER CELL CULTURE; CELL PROLIFERATION; CONTROLLED STUDY; DNA MICROARRAY; FISCHER 344 RAT; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; METASTASIS; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; RAT; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; RNA ISOLATION; THYROID CELL; THYROID FOLLICULAR CARCINOMA; WESTERN BLOTTING;

ADENOSINE TRIPHOSPHATE; ANIMALS; CALCIUM; CALCIUM SIGNALING; CALCIUM-BINDING PROTEINS; CELL LINE; ENZYME INHIBITORS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HUMANS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTO-ONCOGENE PROTEINS C-FOS; RATS; S100 PROTEINS; THAPSIGARGIN; THYROID GLAND; THYROTROPIN;

RATTUS;

EID: 77549086267     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2010.01.007     Document Type: Article

References (58)

1. Vassart G., and Dumont J.E. The thyrotropin receptor and the regulation of thyrocyte function and growth. Endocr. Rev. 13 (1992) 596
2. Kero J., Ahmed K., Wettschureck N., Tunaru S., Wintermantel T., Greiner E., Schutz G., and Offermanns S. Thyrocyte-specific Gq/G11 deficiency impairs thyroid function and prevents goiter development. J. Clin. Invest. 117 (2007) 2399
3. Zaballos M.A., Garcia B., and Santisteban P. G{beta}{gamma} dimers released in response to TSH activate phosphoinositide 3-kinase and regulate gene expression in thyroid cells. Mol. Endocrinol. 22 (2008) 1183
4. Bjorklund S., Palmberg S., Rask S., Westerdahl A.C., and Tornquist K. Effects of sphingosine 1-phosphate on calcium signaling, proliferation and S1P2 receptor expression in PC Cl3 rat thyroid cells. Mol. Cell Endocrinol. 231 (2005) 65
5. Tornquist K., Ekokoski E., and Dugue B. Purinergic agonist ATP is a comitogen in thyroid FRTL-5 cells. J. Cell. Physiol. 166 (1996) 241
6. Park Y.J., Lee Y.J., Kim S.H., Joung D.S., Kim B.J., So I., Park D.J., and Cho B.Y. Ghrelin enhances the proliferating effect of thyroid stimulating hormone in FRTL-5 thyroid cells. Mol. Cell. Endocrinol. 285 (2008) 19
7. Orrenius S., and Nicotera P. The calcium ion and cell death. J. Neural. Transm. Suppl. 43 (1994) 1
8. Ichas F., and Mazat J.P. From calcium signaling to cell death: two conformations for the mitochondrial permeability transition pore. Switching from low- to high-conductance state. Biochim. Biophys. Acta 1366 (1998) 33
9. Meziane-El-Hassani R., Morand S., Boucher J.L., Frapart Y.M., Apostolou D., Agnandji D., Gnidehou S., Ohayon R., Noel-Hudson M.S., Francon J., Lalaoui K., Virion A., and Dupuy C. Dual oxidase-2 has an intrinsic Ca2+-dependent H2O2-generating activity. J. Biol. Chem. 280 (2005) 30046
10. Krohn K., Maier J., and Paschke R. Mechanisms of disease: hydrogen peroxide, DNA damage and mutagenesis in the development of thyroid tumors. Nat. Clin. Pract. Endocrinol. Metab 3 (2007) 713
11. Song Y., Driessens N., Costa M., De Deken X., Detours V., Corvilain B., Maenhaut C., Miot F., Van S.J., Many M.C., and Dumont J.E. Roles of hydrogen peroxide in thyroid physiology and disease. J. Clin. Endocrinol. Metab. 92 (2007) 3764
12. Maier J., Van S.H., Van O.C., Paschke R., Weiss R.E., and Krohn K. Iodine deficiency activates antioxidant genes and causes DNA damage in the thyroid gland of rats and mice. Biochim. Biophys. Acta 1773 (2007) 990
13. Delange F. The disorders induced by iodine deficiency. Thyroid 4 (1994) 107
14. Okajima F., Sato K., and Kondo Y. P2-purinergic agonists activate phospholipase C in a guanine nucleotide- and Ca2+-dependent manner in FRTL-5 thyroid cell membranes. FEBS Lett. 253 (1989) 132
15. Raspe E., Laurent E., Andry G., and Dumont J.E. ATP, bradykinin, TRH and TSH activate the Ca(2+)-phosphatidylinositol cascade of human thyrocytes in primary culture. Mol. Cell. Endocrinol. 81 (1991) 175
16. Guerini D., Coletto L., and Carafoli E. Exporting calcium from cells. Cell Calcium 38 (2005) 281
17. Parmentier M., Libert F., Maenhaut C., Lefort A., Gerard C., Perret J., Van S.J., Dumont J.E., and Vassart G. Molecular cloning of the thyrotropin receptor. Science 246 (1989) 1620
18. Parma J., Duprez L., Van S.J., Cochaux P., Gervy C., Mockel J., Dumont J., and Vassart G. Somatic mutations in the thyrotropin receptor gene cause hyperfunctioning thyroid adenomas. Nature 365 (1993) 649
19. Parma J., Duprez L., Van S.J., Hermans J., Rocmans P., Van V.G., Costagliola S., Rodien P., Dumont J.E., and Vassart G. Diversity and prevalence of somatic mutations in the thyrotropin receptor and Gs alpha genes as a cause of toxic thyroid adenomas. J. Clin. Endocrinol. Metab. 82 (1997) 2695
20. Fuhrer D., Holzapfel H.P., Wonerow P., Scherbaum W.A., and Paschke R. Somatic mutations in the thyrotropin receptor gene and not in the Gs alpha protein gene in 31 toxic thyroid nodules. J. Clin. Endocrinol. Metab. 82 (1997) 3885
21. Führer D., Lewis M.D., Alkahajik F., Starkey R., Paschke R., Wynford-Thomas D., Eggo M., and Ludgate M. Biological activity of activating thyroid-stimulating hormone receptor mutants depends on the cellular context. Endocrinology 144 (2003) 4018
22. Eszlinger M., Holzapfel H.P., Voigt C., Arkenau C., and Paschke R. RGS 2 expression is regulated by TSH and inhibits TSH receptor signaling. Eur. J. Endocrinol. 151 (2004) 383
23. Rasband W.S. ImageJ (1997), National Institutes of Health, Bethesda, Maryland, USA
24. Harlow E., and Lane D. Using Antibodies (1999), Cold Spring Harbour Laboratory Press, Cold Spring Harbour, New York
25. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680
26. Towbin H., Staehelin T., and Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U. S. A. 76 (1979) 4350
27. Tusher V.G., Tibshirani R., and Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 5116
28. Fuhrer D., Lewis M.D., Alkhafaji F., Starkey K., Paschke R., Wynford-Thomas D., Eggo M., and Ludgate M. Biological activity of activating thyroid-stimulating hormone receptor mutants depends on the cellular context. Endocrinology 144 (2003) 4018
29. Huang D.W., Sherman B.T., and Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4 (2009) 44
30. Dennis Jr. G., Sherman B.T., Hosack D.A., Yang J., Gao W., Lane H.C., and Lempicki R.A. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol. 4 (2003) 3
31. Arikawa E., Sun Y., Wang J., Zhou Q., Ning B., Dial S.L., Guo L., and Yang J. Cross-platform comparison of SYBR Green real-time PCR with TaqMan PCR, microarrays and other gene expression measurement technologies evaluated in the MicroArray Quality Control (MAQC) study, BMC. Genomics 9 (2008) 328
32. Lytton J., Westlin M., and Hanley M.R. Thapsigargin inhibits the sarcoplasmic or endoplasmic reticulum Ca-ATPase family of calcium pumps. J. Biol. Chem. 266 (1991) 17067
33. Yamauchi M., Kambe F., Cao X., Lu X., Kozaki Y., Oiso Y., and Seo H. Thyroid hormone activates adenosine 5′-monophosphate-activated protein kinase via intracellular calcium mobilization and activation of calcium/calmodulin-dependent protein kinase kinase-beta. Mol. Endocrinol. 22 (2008) 893
34. Kimura T., Okajima F., Sho K., Kobayashi I., and Kondo Y. Thyrotropin-induced hydrogen peroxide production in FRTL-5 thyroid cells is mediated not by adenosine 3′, 5′-monophosphate, but by Ca2+ signaling followed by phospholipase-A2 activation and potentiated by an adenosine derivative. Endocrinology 136 (1995) 116
35. Dumont J.E., Christophe D., Vassart G., Roger P., and Maenhaut C. In: de Groot L. (Ed). The Phylogeny, Anatomy and Regulation of the Iodine Metabolizing Thyroid (2005), Endocrine Education Inc, South Dartmouth, MA. http://www.Thyroidmanger.org www.Thyroidmanger.org
36. Cetani F., Tonacchera M., and Vassart G. Differential effects of NaCl concentration on the constitutive activity of the thyrotropin and the luteinizing hormone/chorionic gonadotropin receptors. FEBS Lett. 378 (1996) 27
37. Kimura T., Van K.A., Golstein J., Fusco A., Dumont J.E., and Roger P.P. Regulation of thyroid cell proliferation by TSH and other factors: a critical evaluation of in vitro models. Endocr. Rev. 22 (2001) 631
38. Marenholz I., Heizmann C.W., and Fritz G. S100 proteins in mouse and man: from evolution to function and pathology (including an update of the nomenclature). Biochem. Biophys. Res. Commun. 322 (2004) 1111
39. Schmidt-Hansen B., Ornas D., Grigorian M., Klingelhofer J., Tulchinsky E., Lukanidin E., and Ambartsumian N. Extracellular S100A4(mts1) stimulates invasive growth of mouse endothelial cells and modulates MMP-13 matrix metalloproteinase activity. Oncogene 23 (2004) 5487
40. Zou M., Famulski K.S., Parhar R.S., Baitei E., Al-Mohanna F.A., Farid N.R., and Shi Y. Microarray analysis of metastasis-associated gene expression profiling in a murine model of thyroid carcinoma pulmonary metastasis: identification of S100A4 (Mts1) gene overexpression as a poor prognostic marker for thyroid carcinoma. J. Clin. Endocrinol. Metab 89 (2004) 6146
41. Zou M., Al-Baradie R.S., Al-Hindi H., Farid N.R., and Shi Y. S100A4 (Mts1) gene overexpression is associated with invasion and metastasis of papillary thyroid carcinoma. Br. J. Cancer 93 (2005) 1277
42. Nakamura N., Erickson L.A., Jin L., Kajita S., Zhang H., Qian X., Rumilla K., and Lloyd R.V. Immunohistochemical separation of follicular variant of papillary thyroid carcinoma from follicular adenoma. Endocr. Pathol. 17 (2006) 213
43. Puskas L.G., Juhasz F., Zarva A., Hackler Jr. L., and Farid N.R. Gene profiling identifies genes specific for well-differentiated epithelial thyroid tumors. Cell Mol. Biol. (Noisy. -Le-Grand) 51 (2005) 177
44. Ito Y., Yoshida H., Tomoda C., Uruno T., Miya A., Kobayashi K., Matsuzuka F., Kakudo K., Kuma K., and Miyauchi A. S100A4 expression is an early event of papillary carcinoma of the thyroid. Oncology 67 (2004) 397
45. Singh J., Hunt P., Eggo M.C., Sheppard M.C., Kirk C.J., and Michell R.H. Thyroid-stimulating hormone rapidly stimulates inositol polyphosphate formation in FRTL-5 thyrocytes without activating phosphoinositidase C. Biochem. J. 316 Pt 1 (1996) 175
46. Van S.J., Dequanter D., Lothaire P., Massart C., Dumont J.E., and Erneux C. Thyrotropin stimulates the generation of inositol 1, 4, 5-trisphosphate in human thyroid cells. J. Clin. Endocrinol. Metab. 91 (2006) 1099
47. Ekokoski E., Webb T.E., Simon J., and Tornquist K. Mechanisms of P2 receptor-evoked DNA synthesis in thyroid FRTL-5 cells. J. Cell. Physiol. 187 (2001) 166
48. Rapaport E. Experimental cancer therapy in mice by adenine nucleotides. Eur. J. Cancer Clin. Oncol. 24 (1988) 1491
49. Estrela J.M., Obrador E., Navarro J., Lasso De la Vega M.C., and Pellicer J.A. Elimination of Ehrlich tumours by ATP-induced growth inhibition, glutathione depletion and X-rays. Nat. Med. 1 (1995) 84
50. Nejime N., Tanaka N., Yoshihara R., Kagota S., Yoshikawa N., Nakamura K., Kunitomo M., Hashimoto M., and Shinozuka K. Effect of P2 receptor on the intracellular calcium increase by cancer cells in human umbilical vein endothelial cells. Naunyn Schmiedebergs Arch. Pharmacol. 377 (2008) 429
51. Hogan P.G., and Rao A. Dissecting ICRAC, a store-operated calcium current. Trends Biochem. Sci. 32 (2007) 235
52. Martin M.W., and Harden T.K. Agonist-induced desensitization of a P2Y-purinergic receptor-regulated phospholipase C. J. Biol. Chem. 264 (1989) 19535
53. Ulianich L., Secondo A., De M.S., Treglia S., Pacifico F., Liguoro D., Moscato F., Marsigliante S., Annunziato L., Formisano S., Consiglio E., and Di J.B. TSH/cAMP up-regulate sarco/endoplasmic reticulum Ca2+-ATPases expression and activity in PC Cl3 thyroid cells. Eur. J. Endocrinol. 150 (2004) 851
54. Chard P.S., Bleakman D., Christakos S., Fullmer C.S., and Miller R.J. Calcium buffering properties of calbindin D28k and parvalbumin in rat sensory neurones. J. Physiol. 472 (1993) 341
55. Grigorian M., Andresen S., Tulchinsky E., Kriajevska M., Carlberg C., Kruse C., Cohn M., Ambartsumian N., Christensen A., Selivanova G., and Lukanidin E. Tumor suppressor p53 protein is a new target for the metastasis-associated Mts1/S100A4 protein: functional consequences of their interaction. J. Biol. Chem. 276 (2001) 22699
56. Kriajevska M.V., Cardenas M.N., Grigorian M.S., Ambartsumian N.S., Georgiev G.P., and Lukanidin E.M. Non-muscle myosin heavy chain as a possible target for protein encoded by metastasis-related mts-1 gene. J. Biol. Chem. 269 (1994) 19679
57. Semov A., Moreno M.J., Onichtchenko A., Abulrob A., Ball M., Ekiel I., Pietrzynski G., Stanimirovic D., and Alakhov V. Metastasis-associated protein S100A4 induces angiogenesis through interaction with Annexin II and accelerated plasmin formation. J. Biol. Chem. 280 (2005) 20833
58. Ikura M., and Ames J.B. Genetic polymorphism and protein conformational plasticity in the calmodulin superfamily: two ways to promote multifunctionality. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 1159