Developmental hypothyroxinaemia and hypothyroidism limit dendritic growth of cerebellar Purkinje cells in rat offspring: Involvement of microtubule-associated protein 2 (MAP2) and stathmin

Neuropathology and Applied Neurobiology

Volumn 40, Issue 4, 2014, Pages 398-415

  Wang, Yuan ^a   Wang, Yi ^a   Dong, Jing ^a   Wei, Wei ^a   Song, Binbin ^a   Min, Hui ^a   Teng, Weiping ^a   Chen, Jie ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

Author keywords

Cerebellum; Dendrite; Hypothyroidism; Hypothyroxinaemia; Iodine deficiency; Purkinje cells

Indexed keywords

CALBINDIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; IODINE; LIOTHYRONINE; MICROTUBULE ASSOCIATED PROTEIN 2; STATHMIN; THIAMAZOLE; THYROID HORMONE; THYROTROPIN; THYROXINE; WATER; MICROTUBULE ASSOCIATED PROTEIN; MTAP2 PROTEIN, RAT; STMN1 PROTEIN, RAT;

ABNORMALLY LOW SUBSTRATE CONCENTRATION IN BLOOD; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; DIET; DISEASE SEVERITY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FEMALE; FREE LIOTHYRONINE INDEX; FREE THYROXINE INDEX; HYPOTHYROIDISM; HYPOTHYROXINEMIA; IMMUNOFLUORESCENCE; IODINE DEFICIENCY; NERVE CELL GROWTH; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROGENY; PROTEIN PHOSPHORYLATION; PURKINJE CELL; RAT; WESTERN BLOTTING; ANIMAL; CEREBELLUM; DEFICIENCY; DENDRITE; MALE; METABOLISM; PATHOLOGY; PHOSPHORYLATION; WISTAR RAT;

ANIMALS; CEREBELLUM; DENDRITES; FEMALE; HYPOTHYROIDISM; IODINE; MALE; MICROTUBULE-ASSOCIATED PROTEINS; PHOSPHORYLATION; PURKINJE CELLS; RATS; RATS, WISTAR; STATHMIN; THYROXINE;

EID: 84898804160     PISSN: 03051846     EISSN: 13652990     Source Type: Journal    
DOI: 10.1111/nan.12074     Document Type: Article

References (58)

1. Puig-Domingo M, Vila L. The implications of Iodine and its supplementation during pregnancy in fetal brain development. Curr Clin Pharmacol 2013; 8: 97-109
2. Glinoer D. Potential consequences of maternal hypothyroidism on the offspring: evidence and implications. Horm Res 2001; 55: 109-114
3. Zimmermann MB. Iodine deficiency. Endocr Rev 2009; 30: 376-408
4. Melse-Boonstra A, Jaiswal N. Iodine deficiency in pregnancy, infancy and childhood and its consequences for brain development. Best Pract Res Clin Endocrinol Metab 2010; 24: 29-38
5. Skeaff SA. Iodine deficiency in pregnancy: the effect on neurodevelopment in the child. Nutrients 2011; 3: 265-273
6. Berbel P, Obregon MJ, Bernal J, Escobar del Rey F, Morreale de Escobar G. Iodine supplementation during pregnancy: a public health challenge. Trends Endocrinol Metab 2007; 18: 338-343
7. Tang Z, Liu W, Yin H, Wang P, Dong J, Wang Y, Chen J. Investigation of intelligence quotient and psychomotor development in schoolchildren in areas with different degrees of iodine deficiency. Asia Pac J Clin Nutr 2007; 16: 731-737
8. Lavado-Autric R, Ausó E, García-Velasco JV, Arufe Mdel C, Escobar del Rey F, Berbel P, Morreale de Escobar G. Early maternal hypothyroxinemia alters histogenesis and cerebral cortex cytoarchitecture of the progeny. J Clin Invest 2003; 111: 1073-1082
9. Pop VJ, Kuijpens JL, van Baar AL, Verkerk G, van Son MM, de Vijlder JJ, Vulsma T, Wiersinga WM, Drexhage HA, Vader HL. Low maternal free thyroxine concentrations during early pregnancy are associated with impaired psychomotor development in infancy. Clin Endocrinol (Oxf) 1999; 50: 149-155
10. Morreale de Escobar G, Obregon MJ, Escobar del Rey F. Role of thyroid hormone during early brain development. Eur J Endocrinol 2004; 151: U25-U37
11. Morreale de Escobar G, Obregon MJ, Escobar del Rey F. Is neuropsychological development related to maternal hypothyroidism or to maternal hypothyroxinemia? J Clin Endocrinol Metab 2000; 85: 3975-3987
12. Bath SC, Steer CD, Golding J, Emmett P, Rayman MP. Effect of inadequate iodine status in UK pregnant women on cognitive outcomes in their children: results from the Avon Longitudinal Study of Parents and Children (ALSPAC). Lancet 2013; pii: S0140-6736(13)60436-5. doi: 10.1016/S0140-6736(13)60436-5 [Epub ahead of print]
13. Finken MJ, van Eijsden M, Loomans EM, Vrijkotte TG, Rotteveel J. Maternal hypothyroxinemia in early pregnancy predicts reduced performance in reaction time tests in 5- to 6-year-old offspring. J Clin Endocrinol Metab 2013; 98: 1417-1426
14. Henrichs J, Bongers-Schokking JJ, Schenk JJ, Ghassabian A, Schmidt HG, Visser TJ, Hooijkaas H, de Muinck Keizer-Schrama SM, Hofman A, Jaddoe VV, Visser W, Steegers EA, Verhulst FC, de Rijke YB, Tiemeier H. Maternal thyroid function during early pregnancy and cognitive functioning in early childhood: the generation R study. J Clin Endocrinol Metab 2010; 95: 4227-4234
15. Pop VJ, Brouwers EP, Vader HL, Vulsma T, van Baar AL, de Vijlder JJ. Maternal hypothyroxinaemia during early pregnancy and subsequent child development: a 3-year follow-up study. Clin Endocrinol (Oxf) 2003; 59: 282-288
16. Brooks VB. Cerebellar functions in motor control. Hum Neurobiol 1984; 2: 251-260
17. Velázquez-Zamora DA, Martínez-Degollado M, González-Burgos I. Morphological development of dendritic spines on rat cerebellar Purkinje cells. Int J Dev Neurosci 2011; 29: 515-520
18. Gutierrez DV, Mark MD, Masseck O, Maejima T, Kuckelsberg D, Hyde RA, Krause M, Kruse W, Herlitze S. Optogenetic control of motor coordination by Gi/o protein-coupled vertebrate rhodopsin in cerebellar Purkinje cells. J Biol Chem 2011; 286: 25848-25858
19. Tanaka M. Dendrite formation of cerebellar Purkinje cells. Neurochem Res 2009; 34: 2078-2088
20. Lein PJ, Yang D, Bachstetter AD, Tilson HA, Harry GJ, Mervis RF, Kodavanti PR. Ontogenetic alterations in molecular and structural correlates of dendritic growth after developmental exposure topolychlorinated biphenyls. Environ Health Perspect 2007; 115: 556-563
21. Rubenstein JL, Merzenich MM. Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav 2003; 2: 255-267
22. Ibhazehiebo K, Iwasaki T, Okano-Uchida T, Shimokawa N, Ishizaki Y, Koibuchi N. Suppression of thyroid hormone receptor-mediated transcription and disruption of thyroid hormone-induced cerebellar morphogenesis by the polybrominated biphenyl mixture, BP-6. Neurotoxicology 2011; 32: 400-409
23. Kimura-Kuroda J, Nagata I, Kuroda Y. Hydroxylated metabolites of polychlorinated biphenyls inhibit thyroid-hormone-dependent extension of cerebellar Purkinje cell dendrites. Brain Res Dev Brain Res 2005; 154: 259-263
24. Ohkawa N, Hashimoto K, Hino T, Migishima R, Yokoyama M, Kano M, Inokuchi K. Motor discoordination of transgenic mice overexpressing a microtubule destabilizer, stathmin, specifically in Purkinje cells. Neurosci Res 2007; 59: 93-100
25. Harada A, Teng J, Takei Y, Oguchi K, Hirokawa N. MAP2 is required for dendrite elongation, PKA anchoring in dendrites, and proper PKA signal transduction. J Cell Biol 2002; 158: 541-549
26. Avila J, Dominguez J, Di'az-Nido J. Regulation of microtubule dynamics by microtubule-associated protein expression and phosphorylation during neuronal development. Int J Dev Biol 1994; 38: 13-25
27. Drewes G, Ebneth A, Mandelkow EM. MAPs, MARKs and microtubule dynamics. Trends Biochem Sci 1998; 23: 307-311
28. Sánchez C, Díaz-Nido J, Avila J. Phosphorylation of microtubule-associated protein 2 (MAP2) and its relevance for the regulation of the neuronal cytoskeleton function. Prog Neurobiol 2000; 61: 133-168
29. Vaillant AR, Zanassi P, Walsh GS, Aumont A, Alonso A, Miller FD. Signaling mechanisms underlying reversible, activity-dependent dendrite formation. Neuron 2002; 34: 985-998
30. Cassimeris L. The oncoprotein 18/stathmin family of microtubule destabilizers. Curr Opin Cell Biol 2002; 14: 18-24
31. Grenningloh G, Soehrman S, Bondallaz P, Ruchti E, Cadas H. Role of the microtubule destabilizing proteins SCG10 and stathmin in neuronal growth. J Neurobiol 2004; 58: 60-69
32. Ohkawa N, Fujitani K, Tokunaga E, Furuya S, Inokuchi K. The microtubule destabilizer stathmin mediates the development of dendritic arbors in neuronal cells. J Cell Sci 2007; 120: 1447-1456
33. Fink CC, Bayer KU, Myers JW, Ferrell JE Jr, Schulman H, Meyer T. Selective regulation of neurite extension and synapse formation by the beta but not the alpha isoform of CaMKII. Neuron 2003; 39: 283-297
34. Gaudilliere B, Konishi Y, de la Iglesia N, Yao G, Bonni A. A CaMKII NeuroD signaling pathway specifies dendritic morphogenesis. Neuron 2004; 41: 229-241
35. Kimura-Kuroda J, Nagata I, Negishi-Kato M, Kuroda Y. Thyroid hormone-dependent development of mouse cerebellar Purkinje cells in vitro. Brain Res Dev Brain Res 2002; 137: 55-65
36. Koibuchi N, Chin WW. Thyroid hormone action and brain development. Trends Endocrinol Metab 2000; 11: 123-128
37. Isaia F, Aragoni MC, Arca M, Demartin F, Devillanova FA, Floris G, Garau A, Hursthouse MB, Lippolis V, Medda R, Oppo F, Pira M, Verani G. Interaction of methimazole with I2: X-ray crystal structure of the charge transfer complex methimazole-I2. implications for the mechanism of action of methimazole-based antithyroid drugs. J Med Chem 2008; 51: 4050-4053
38. Shin MS, Ko IG, Kim SE, Kim BK, Kim TS, Lee SH, Hwang DS, Kim CJ, Park JK, Lim BV. Treadmill exercise ameliorates symptoms of methimazole-induced hypothyroidism through enhancing neurogenesis and suppressing apoptosis in the hippocampus of rat pups. Int J Dev Neurosci 2013; 31: 214-223
39. Reeves PG, Nielsen FH, Fahey GC Jr. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 1993; 123: 1939-1951
40. Wang Y, Wei W, Wang Y, Dong J, Song B, Min H, Teng W, Chen J. Neurotoxicity of developmental hypothyroxinemia and hypothyroidism in rats: impairments of long-term potentiation are mediated by phosphatidylinositol 3-kinase signaling pathway. Toxicol Appl Pharmacol 2013; pii: S0041-008X(13)00218-4. doi: 10.1016/j.taap.2013.04.034 [Epub ahead of print]
41. Sánchez Martin C, Ledesma D, Dotti CG, Avila J. Microtubule-associated protein-2 located in growth regions of rat hippocampal neurons is highly phosphorylated at its proline-rich region. Neuroscience 2000; 101: 885-893
42. Pattinson D, Baccei M, Karadottir R, Torsney C, Moss A, McCutcheon J, Giese KP, Fitzgerald M. Aberrant dendritic branching and sensory inputs in the superficial dorsal horn of mice lacking CaMKIIalpha autophosphorylation. Mol Cell Neurosci 2006; 33: 88-95
43. Konur S, Ghosh A. Calcium signaling and the control of dendritic development. Neuron 2005; 46: 401-405
44. Koibuchi N. The role of thyroid hormone on cerebellar development. Cerebellum 2008; 7: 530-533
45. Barski JJ, Hartmann J, Rose CR, Hoebeek F, Mörl K, Noll-Hussong M, De Zeeuw CI, Konnerth A, Meyer M. Calbindin in cerebellar Purkinje cells is a critical determinant of the precision of motor coordination. J Neurosci 2003; 23: 3469-3477
46. Ranade SC, Sarfaraz Nawaz M, Kumar Rambtla P, Rose AJ, Gressens P, Mani S. Early protein malnutrition disrupts cerebellar development and impairs motor coordination. Br J Nutr 2012; 107: 1167-1175
47. Van Alphen AM, Schepers T, Luo C, De Zeeuw CI. Motor performance and motor learning in Lurcher mice. Ann N Y Acad Sci 2002; 978: 413-424
48. Holmfeldt P, Larsson N, Segerman B, Howell B, Morabito J, Cassimeris L, Gullberg M. The catastrophe-promoting activity of ectopic Op18/stathmin is required for disruption of mitotic spindles but not interphase microtubules. Mol Biol Cell 2001; 12: 73-83
49. Fujimoto T, Tanaka H, Kumamaru E, Okamura K, Miki N. Arc interacts with microtubules/microtubule-associated protein 2 and attenuates microtubule-associated protein 2 immunoreactivity in the dendrites. J Neurosci Res 2004; 76: 51-63
50. Guo Y, Sánchez C, Udin SB. MAP2 phosphorylation and visual plasticity in Xenopus. Brain Res 2001; 905: 134-141
51. Yamaguchi S, Katagiri S, Aoki N, Iikubo E, Kitajima T, Matsushima T, Homma KJ. Molecular function of microtubule-associated protein 2 for filial imprinting in domestic chicks (Gallus gallus domesticus). Neurosci Res 2011; 69: 32-40
52. Dehmelt L, Halpain S. The MAP2/Tau family of microtubule-associated proteins. Genome Biol 2005; 6: 204
53. Wang X, Wang R, Lin F, Dong K, Gao P, Zhang H. Expression of stathmin/op18 as a significant prognostic factor for cervical carcinoma patients. J Cancer Res Clin Oncol 2009; 135: 837-846
54. Poulain FE, Chauvin S, Wehrlé R, Desclaux M, Mallet J, Vodjdani G, Dusart I, Sobel A. SCLIP is crucial for the formation and development of the Purkinje cell dendritic arbor. J Neurosci 2008; 28: 7387-7398
55. Iwata T, Namikawa K, Honma M, Mori N, Yachiku S, Kiyama H. Increased expression of mRNAs for microtubule disassembly molecules during nerve regeneration. Brain Res Mol Brain Res 2002; 102: 105-109
56. Gavet O, El Messari S, Ozon S, Sobel A. Regulation and subcellular localization of the microtubule-destabilizing stathmin family phosphoproteins in cortical neurons. J Neurosci Res 2002; 68: 535-550
57. Dong J, Liu W, Wang Y, Xi Q, Chen J. Hypothyroidism following developmental iodine deficiency reduces hippocampal neurogranin, CaMK II and calmodulin and elevates calcineurin in lactational rats. Int J Dev Neurosci 2010; 28: 589-596
58. Dong J, Liu W, Wang Y, Hou Y, Xu H, Gong J, Xi Q, Chen J. Developmental iodine deficiency and hypothyroidism impair spatial memory in adolescent rat hippocampus: involvement of CaMKII, calmodulin and calcineurin. Neurotox Res 2011; 19: 81-93