Nicotinamide nucleotide transhydrogenase mutation analysis in Chinese patients with thyroid dysgenesis.
gene mutation
nicotinamide nucleotide transhydrogenase gene
proliferation and migration
redox balance
thyroid dysgenesis
Journal
American journal of medical genetics. Part A
ISSN: 1552-4833
Titre abrégé: Am J Med Genet A
Pays: United States
ID NLM: 101235741
Informations de publication
Date de publication:
01 2022
01 2022
Historique:
revised:
27
07
2021
received:
20
02
2021
accepted:
24
08
2021
pubmed:
22
9
2021
medline:
8
4
2022
entrez:
21
9
2021
Statut:
ppublish
Résumé
Thyroid dysgenesis (TD) accounts for 80% cases of congenital hypothyroidism, which is the most common neonatal disorder. Until now, the gene mutations have been reported associated with TD can only account for 5% cases, suggesting the genetic heterogeneity of the pathology. Nicotinamide nucleotide transhydrogenase (NNT) plays a crucial role in regulating redox homeostasis, patients carrying NNT mutations have been described with a clinical phenotype of hypothyroidism. As TD risk is increased in the context of several syndromes and redox homeostasis is vital for thyroid development and function, NNT might be a candidate gene involved in syndromic TD. Therefore, we performed target sequencing (TS) in 289 TD patients for causative mutations in NNT and conducted functional analysis of the gene mutations. TS and Sanger sequence were used to screen the novel mutations. For functional analysis, we performed western blot, measurement of NADPH/NADP
Identifiants
pubmed: 34545694
doi: 10.1002/ajmg.a.62493
doi:
Substances chimiques
Mitochondrial Proteins
0
NADP Transhydrogenases
EC 1.6.1.-
NADP Transhydrogenase, AB-Specific
EC 1.6.1.2
NNT protein, human
EC 1.6.1.2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
89-98Informations de copyright
© 2021 Wiley Periodicals LLC.
Références
Abu-Khudir, R., Larrivee-Vanier, S., Wasserman, J. D., & Deladoey, J. (2017). Disorders of thyroid morphogenesis. Best Practice & Research. Clinical Endocrinology & Metabolism, 31(2), 143-159. https://doi.org/10.1016/j.beem.2017.04.008
Bainbridge, M. N., Davis, E. E., Choi, W. Y., Dickson, A., Martinez, H. R., Wang, M., Dinh, H., Muzny, D. M., Pignatelli, R., Katsanis, N., Boerwinkle, E., Gibbs, R. A., & Jefferies, J. L. (2015). Loss of function mutations in NNT are associated with left ventricular noncompaction. Circulation-Cardiovascular Genetics, 8(4), 544-552. https://doi.org/10.1161/Circgenetics.115.001026
Carré, A., Stoupa, A., Kariyawasam, D., Gueriouz, M., Ramond, C., Monus, T., Léger, J., Gaujoux, S., Sebag, F., Glaser, N., Zenaty, D., Nitschke, P., Bole-Feysot, C., Hubert, L., Lyonnet, S., Scharfmann, R., Munnich, A., Besmond, C., Taylor, W., & Polak, M. (2017). Mutations in BOREALIN cause thyroid dysgenesis. Human Molecular Genetics, 26(3), 599-610. https://doi.org/10.1093/hmg/ddw419
Castanet, M., & Polak, M. (2010). Spectrum of human Foxe1/TTF2 mutations. Hormone Research in Paediatrics, 73(6), 423-429. https://doi.org/10.1159/000281438
Chortis, V., Taylor, A. E., Doig, C. L., Walsh, M. D., Meimaridou, E., Jenkinson, C., Rodriguez-Blanco, G., Ronchi, C. L., Jafri, A., Metherell, L. A., Hebenstreit, D., Dunn, W. B., Arlt, W., & Foster, P. A. (2018). Nicotinamide nucleotide transhydrogenase as a novel treatment target in adrenocortical carcinoma. Endocrinology, 159(8), 2836-2849. https://doi.org/10.1210/en.2018-00014
de Filippis, T., Marelli, F., Nebbia, G., Porazzi, P., Corbetta, S., Fugazzola, L., Gastaldi, R., Vigone, M. C., Biffanti, R., Frizziero, D., Mandarà, L., Prontera, P., Salerno, M., Maghnie, M., Tiso, N., Radetti, G., Weber, G., & Persani, L. (2016). JAG1 loss-of-function variations as a novel predisposing event in the pathogenesis of congenital thyroid defects. The Journal of Clinical Endocrinology and Metabolism, 101(3), 861-870. https://doi.org/10.1210/jc.2015-3403
Di Lauro, R., Damante, G., De Felice, M., Arnone, M. I., Sato, K., Lonigro, R., & Zannini, M. (1995). Molecular events in the differentiation of the thyroid gland. Journal of Endocrinological Investigation, 18(2), 117-119. https://doi.org/10.1007/BF03349716
Fernandez, L. P., Lopez-Marquez, A., & Santisteban, P. (2015). Thyroid transcription factors in development, differentiation and disease. Nature Reviews. Endocrinology, 11(1), 29-42. https://doi.org/10.1038/nrendo.2014.186
Guran, T., Buonocore, F., Saka, N., Ozbek, M. N., Aycan, Z., Bereket, A., Bas, F., Darcan, S., Bideci, A., Guven, A., Demir, K., Akinci, A., Buyukinan, M., Aydin, B. K., Turan, S., Agladioglu, S. Y., Atay, Z., Abali, Z. Y., Tarim, O., … Achermann, J. C. (2016). Rare causes of primary adrenal insufficiency: Genetic and clinical characterization of a large Nationwide cohort. Journal of Clinical Endocrinology & Metabolism, 101(1), 283-291. https://doi.org/10.1210/jc.2015-3250
Hermanns, P., Kumorowicz-Czoch, M., Grasberger, H., Refetoff, S., & Pohlenz, J. (2018). Novel mutations in the NKX2.1 gene and the PAX8 gene in a boy with brain-lung-thyroid syndrome. Experimental and Clinical Endocrinology & Diabetes, 126(2), 85-90. https://doi.org/10.1055/s-0043-119875
Ho, H. Y., Lin, Y. T., Lin, G. G., Wu, P. R., & Cheng, M. L. (2017). Nicotinamide nucleotide transhydrogenase (NNT) deficiency dysregulates mitochondrial retrograde signaling and impedes proliferation. Redox Biology, 12, 916-928. https://doi.org/10.1016/j.redox.2017.04.035
Jazayeri, O., Liu, X. Z., van Diemen, C. C., Bakker-van Waarde, W. M., Sikkema-Raddatz, B., Sinke, R. J., Zhang, J., & van Ravenswaaij-Arts, C. M. A. (2015). A novel homozygous insertion and review of published mutations in the NNT gene causing familial glucocorticoid deficiency (FGD). European Journal of Medical Genetics, 58(12), 642-649. https://doi.org/10.1016/j.ejmg.2015.11.001
Kizys, M. M. L., Louzada, R. A., Mitne-Neto, M., Jara, J. R., Furuzawa, G. K., de Carvalho, D. P., Dias-da-Silva, M. R., Nesi-França, S., Dupuy, C., & Maciel, R. M. B. (2017). DUOX2 mutations are associated with congenital hypothyroidism with ectopic thyroid gland. The Journal of Clinical Endocrinology and Metabolism, 102(11), 4060-4071. https://doi.org/10.1210/jc.2017-00832
Kostopoulou, E., Miliordos, K., & Spiliotis, B. (2021). Genetics of primary congenital hypothyroidism-a review. Hormones (Athens, Greece), 20, 225-236. https://doi.org/10.1007/s42000-020-00267-x
Kruiswijk, F., Labuschagne, C. F., & Vousden, K. H. (2015). p53 in survival, death and metabolic health: A lifeguard with a licence to kill. Nature Reviews Molecular Cell Biology, 16(7), 393-405. https://doi.org/10.1038/nrm4007
Li, S., Zhuang, Z. N., Wu, T., Lin, J. C., Liu, Z. X., Zhou, L. F., Dai, T., Lu, L., & Ju, H. Q. (2018). Nicotinamide nucleotide transhydrogenase-mediated redox homeostasis promotes tumor growth and metastasis in gastric cancer. Redox Biology, 18, 246-255. https://doi.org/10.1016/j.redox.2018.07.017
Liu, D. F., Zhang, J. J., Wu, Y., Shi, G. D., Yuan, H., Lu, Z. P., Zhu, Q., Wu, P., Lu, C., Guo, F., Chen, J., Jiang, K., & Miao, Y. (2018). YY1 suppresses proliferation and migration of pancreatic ductal adenocarcinoma by regulating the CDKN3/MdM2/P53/P21 signaling pathway. International Journal of Cancer, 142(7), 1392-1404. https://doi.org/10.1002/ijc.31173
Luxen, S., Noack, D., Frausto, M., Davanture, S., Torbett, B. E., & Knaus, U. G. (2009). Heterodimerization controls localization of Duox-DuoxA NADPH oxidases in airway cells. Journal of Cell Science, 122(Pt 8), 1238-1247. https://doi.org/10.1242/jcs.044123
Meimaridou, E., Goldsworthy, M., Chortis, V., Fragouli, E., Foster, P. A., Arlt, W., Cox, R., & Metherell, L. A. (2018). NNT is a key regulator of adrenal redox homeostasis and steroidogenesis in male mice. Journal of Endocrinology, 236(1), 13-28. https://doi.org/10.1530/Joe-16-0638
Meimaridou, E., Kowalczyk, J., Guasti, L., Hughes, C. R., Wagner, F., Frommolt, P., Nürnberg, P., Mann, N. P., Banerjee, R., Saka, H. N., Chapple, J. P., King, P. J., Clark, A. J. L., & Metherell, L. A. (2012). Mutations in NNT encoding nicotinamide nucleotide transhydrogenase cause familial glucocorticoid deficiency. Nature Genetics, 44(7), 740-742. https://doi.org/10.1038/ng.2299
Metherell, L. A., Guerra-Assuncao, J. A., Sternberg, M. J., & David, A. (2016). Three-dimensional model of human nicotinamide nucleotide transhydrogenase (NNT) and sequence-structure analysis of its disease-causing variations. Human Mutation, 37(10), 1074-1084. https://doi.org/10.1002/humu.23046
Mio, C., Grani, G., Durante, C., & Damante, G. (2020). Molecular defects in thyroid dysgenesis. Clinical Genetics, 97(1), 222-231. https://doi.org/10.1111/cge.13627
Murphy, M. P. (2015). Redox modulation by reversal of the mitochondrial nicotinamide nucleotide transhydrogenase. Cell Metabolism, 22(3), 363-365. https://doi.org/10.1016/j.cmet.2015.08.012
Nesci, S., Trombetti, F., & Pagliarani, A. (2020). Nicotinamide nucleotide transhydrogenase as a sensor of mitochondrial biology. Trends in Cell Biology, 30(1), 1-3. https://doi.org/10.1016/j.tcb.2019.11.001
Nilsson, M., & Fagman, H. (2013). Mechanisms of thyroid development and dysgenesis: An analysis based on developmental stages and concurrent embryonic anatomy. Current Topics in Developmental Biology, 106, 123-170. https://doi.org/10.1016/B978-0-12-416021-7.00004-3
Nilsson, M., & Fagman, H. (2017). Development of the thyroid gland. Development, 144(12), 2123-2140. https://doi.org/10.1242/dev.145615
Poncin, S., Gérard, A. C., Boucquey, M., Senou, M., Calderon, P. B., Knoops, B., Lengelé, B., Many, M. C., & Colin, I. M. (2008). Oxidative stress in the thyroid gland: From harmlessness to hazard depending on the iodine content. Endocrinology, 149(1), 424-433. https://doi.org/10.1210/en.2007-0951
Roucher-Boulez, F., Mallet-Motak, D., Samara-Boustani, D., Jilani, H., Ladjouze, A., Souchon, P. F., Simon, D., Nivot, S., Heinrichs, C., Ronze, M., Bertagna, X., Groisne, L., Leheup, B., Naud-Saudreau, C., Blondin, G., Lefevre, C., Lemarchand, L., & Morel, Y. (2016). NNT mutations: A cause of primary adrenal insufficiency, oxidative stress and extra-adrenal defects. European Journal of Endocrinology, 175(1), 73-84. https://doi.org/10.1530/EJE-16-0056
Santos-Silva, R., Rosário, M., Grangeia, A., Costa, C., Castro-Correia, C., Alonso, I., Leão, M., & Fontoura, M. (2019). Genetic analyses in a cohort of Portuguese pediatric patients with congenital hypothyroidism. Journal of Pediatric Endocrinology & Metabolism, 32(11), 1265-1273. https://doi.org/10.1515/jpem-2019-0047
Schieber, M., & Chandel, N. S. (2014). ROS function in redox signaling and oxidative stress. Current Biology, 24(10), R453-R462. https://doi.org/10.1016/j.cub.2014.03.034
Stoupa, A., Adam, F., Kariyawasam, D., Strassel, C., Gawade, S., Szinnai, G., Kauskot, A., Lasne, D., Janke, C., Natarajan, K., Schmitt, A., Bole-Feysot, C., Nitschke, P., Léger, J., Jabot-Hanin, F., Tores, F., Michel, A., Munnich, A., Besmond, C., … Carré, A. (2018). TUBB1 mutations cause thyroid dysgenesis associated with abnormal platelet physiology. EMBO Mol Med, 10(12), e9569. https://doi.org/10.15252/emmm.201809569
Stoupa, A., Kariyawasam, D., Carre, A., & Polak, M. (2016). Update of thyroid developmental genes. Endocrinology and Metabolism Clinics of North America, 45(2), 243-254. https://doi.org/10.1016/j.ecl.2016.01.007
Sun, F., Zhang, J. X., Yang, C. Y., Gao, G. Q., Zhu, W. B., Han, B., Zhang, L. L., Wan, Y. Y., Ye, X. P., Ma, Y. R., Zhang, M. M., Yang, L., Zhang, Q. Y., Liu, W., Guo, C. C., Chen, G., Zhao, S. X., Song, K. Y., & Song, H. D. (2018). The genetic characteristics of congenital hypothyroidism in China by comprehensive screening of 21 candidate genes. European Journal of Endocrinology, 178(6), 623-633. https://doi.org/10.1530/EJE-17-1017
Szinnai, G. (2014). Genetics of normal and abnormal thyroid development in humans. Best Practice & Research. Clinical Endocrinology & Metabolism, 28(2), 133-150. https://doi.org/10.1016/j.beem.2013.08.005
Tyurin-Kuzmin, P. A., Zhdanovskaya, N. D., Sukhova, A. A., Sagaradze, G. D., Albert, E. A., Ageeva, L. V., Sharonov, G. V., Vorotnikov, A. V., & Tkachuk, V. A. (2016). Nox4 and Duox1/2 mediate redox activation of mesenchymal cell migration by PDGF. PLoS One, 11(4), e0154157. https://doi.org/10.1371/journal.pone.0154157
Vogelauer, M., Krall, A. S., Mcbrian, M. A., Li, J. Y., & Kurdistani, S. K. (2012). Stimulation of histone deacetylase activity by metabolites of intermediary metabolism. Journal of Biological Chemistry, 287(38), 32006-32016. https://doi.org/10.1074/jbc.M112.362467
Weinberg-Shukron, A., Abu-Libdeh, A., Zhadeh, F., Carmel, L., Kogot-Levin, A., Kamal, L., Kanaan, M., Zeligson, S., Renbaum, P., Levy-Lahad, E., & Zangen, D. (2015). Combined mineralocorticoid and glucocorticoid deficiency is caused by a novel founder nicotinamide nucleotide transhydrogenase mutation that alters mitochondrial morphology and increases oxidative stress. Journal of Medical Genetics, 52(9), 636-641. https://doi.org/10.1136/jmedgenet-2015-103078
Yamaguchi, R., Kato, F., Hasegawa, T., Katsumata, N., Fukami, M., Matsui, T., Nagasaki, K., & Ogata, T. (2013). A novel homozygous mutation of the nicotinamide nucleotide transhydrogenase gene in a Japanese patient with familial glucocorticoid deficiency. Endocrine Journal, 60(7), 855-859. https://doi.org/10.1507/endocrj.ej13-0024
Zandalinas, S. I., & Mittler, R. (2018). ROS-induced ROS release in plant and animal cells. Free Radical Biology and Medicine, 122, 21-27. https://doi.org/10.1016/j.freeradbiomed.2017.11.028