Developmental hypothyroxinemia and hypothyroidism reduce proliferation of cerebellar granule neuron precursors in rat offspring by downregulation of the sonic hedgehog signaling pathway

Molecular Neurobiology

Volumn 49, Issue 3, 2014, Pages 1143-1152

  Wang, Yuan ^a   Wang, Yi ^a   Dong, Jing ^a   Wei, Wei ^a   Song, Binbin ^a   Min, Hui ^a   Yu, Ye ^a   Lei, Xibing ^a   Zhao, Ming ^a   Teng, Weiping ^a   Chen, Jie ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

Author keywords

Cerebellar granule neuron precursors; Hypothyroidism; Hypothyroxinemia; Iodine deficiency; Proliferation; Shh signaling pathway

Indexed keywords

CYCLINE; KI 67 ANTIGEN; SONIC HEDGEHOG PROTEIN; THIAMAZOLE; THYROXINE; SONIC HEDGEHOG PROTEIN, RAT;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; EXPERIMENTAL MODEL; FEMALE; GRANULE CELL; HORMONE DEFICIENCY; HYPOTHYROIDISM; HYPOTHYROXINEMIA; IMMUNOFLUORESCENCE; IODINE DEFICIENCY; NONHUMAN; PROGENY; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; THYROXINE BLOOD LEVEL; WISTAR RAT; ANIMAL; BIOSYNTHESIS; BLOOD; CELL CULTURE; CEREBELLUM; CYTOLOGY; DOWN REGULATION; MALE; METABOLISM; NEURAL STEM CELL; PATHOLOGY; PHYSIOLOGY;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; CEREBELLUM; DOWN-REGULATION; FEMALE; HEDGEHOG PROTEINS; HYPOTHYROIDISM; MALE; NEURAL STEM CELLS; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; THYROXINE;

EID: 84902465496     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-013-8587-3     Document Type: Article

References (55)

1. Puig-Domingo M, Vila L (2013) The implications of iodine and its supplementation during pregnancy in fetal brain development. Curr Clin Pharmacol 8:97-109
2. Zimmermann MB(2009) Iodine deficiency. Endocr Rev 30:376-408
3. Skeaff SA (2011) Iodine deficiency in pregnancy: the effect on neurodevelopment in the child. Nutrients 3:265-273
4. Berbel P, Obregon MJ, Bernal J, Escobar del Rey F, Morreale de Escobar G (2007) Iodine supplementation during pregnancy: a public health challenge. Trends Endocrinol Metab 18:338-343 (Pubitemid 350027791)
5. Glinoer D (2001) Potential consequences of maternal hypothyroidism on the offspring: evidence and implications. Horm Res 55:109-114
6. Tang Z, Liu W, Yin H, Wang P, Dong J, Wang Y, Chen J (2007) Investigation of intelligence quotient and psychomotor development in schoolchildren in areas with different degrees of iodine deficiency. Asia Pac J Clin Nutr 16:731-737 (Pubitemid 350291909)
7. Lavado-Autric R, Ausó E, García-Velasco JV, Arufe Mdel C, Escobar del Rey F, Berbel P, Morreale de Escobar G (2003) Early maternal hypothyroxinemia alters histogenesis and cerebral cortex cytoarchitecture of the progeny. J Clin Invest 111:1073-1082 (Pubitemid 36397484)
8. Pop VJ, Kuijpens JL, van Baar AL, Verkerk G, van Son MM, de Vijlder JJ, Vulsma T, Wiersinga WM, Drexhage HA, Vader HL (1999) Low maternal free thyroxine concentrations during early pregnancy are associated with impaired psychomotor development in infancy. Clin Endocrinol (Oxf) 50:149-155
9. Morreale de Escobar G, Obregon MJ, Escobar del Rey F (2004) Role of thyroid hormone during early brain development. Eur J Endocrinol 151:U25-U37 (Pubitemid 39627053)
10. Morreale de Escobar G, Obregon MJ, Escobar del Rey F (2000) Is neuropsychological development related to maternal hypothyroidism or to maternal hypothyroxinemia? J Clin Endocrinol Metab 85:3975-3987 (Pubitemid 32055337)
11. Brooks VB (1984) Cerebellar functions in motor control. Hum Neurobiol 2:251-260
12. Hibi M, Shimizu T (2012) Development of the cerebellum and cerebellar neural circuits. Dev Neurobiol 72(3):282-301
13. Sillitoe RV, Joyner AL (2007) Morphology, molecular codes, and circuitry produce the three-dimensional complexity of the cerebellum. Annu Rev Cell Dev Biol 23:549-577
14. Vaillant C, Monard D (2009) SHH pathway and cerebellar development. Cerebellum 8(3):291-301
15. Behesti H, Marino S (2009) Cerebellar granule cells: insights into proliferation, differentiation, and role in medulloblastoma pathogenesis. Int J Biochem Cell Biol 41(3):435-445
16. Kumar K, Patro N, Patro I (2013) Impaired structural and functional development of cerebellum following gestational exposure of delta methrin in rats: role of reelin. Cell Mol Neurobiol 33(5):731-746
17. Kenney AM, Cole MD, Rowitch DH (2003) N-Myc upregulation by sonic hedgehog signaling promotes proliferation in developing cerebellar granule neuron precursors. Development 130(1):15-28 (Pubitemid 36113940)
18. Dahmane N, Ruizi Altaba A (1999) Sonic hedgehog regulates the growth and patterning of the cerebellum. Development 126(14): 3089-3100 (Pubitemid 29378174)
19. Manto MU, Jissendi P (2012) Cerebellum: links between development, developmental disorders and motor learning. Front Neuroanat 6:1
20. Corrales JD, Rocco GL, Blaess S, Guo Q, Joyner AL (2004) Spatial pattern of sonic hedgehog signaling through Gli genes during cerebellum development. Development 131(22):5581-5590 (Pubitemid 39625202)
21. Oliver TG, Grasfeder LL, Carroll AL, Kaiser C, Gillingham CL, Lin SM, Wickramasinghe R, Scott MP, Wechsler-Reya RJ (2003) Transcriptional profiling of the sonic hedgehog response: a critical role for N-myc in proliferation of neuronal precursors. Proc Natl Acad Sci U S A 100(12):7331-7336 (Pubitemid 36706438)
22. Yun JS, Rust JM, Ishimaru T, Díaz E (2007) A novel role of the Mad family member Mad3 in cerebellar granule neuron precursor proliferation. Mol Cell Biol 27(23):8178-8189 (Pubitemid 350234232)
23. Kimura-Kuroda J, Nagata I, Negishi-Kato M, Kuroda Y (2002) Thyroid hormone-dependent development of mouse cerebellar Purkinje cells in vitro. Brain Res Dev Brain Res 137:55-65 (Pubitemid 34786636)
24. Koibuchi N, Chin WW (2000) Thyroid hormone action and brain development. Trends Endocrinol Metab 11:123-128 (Pubitemid 30238543)
25. Portella AC, Carvalho F, Faustino L, Wondisford FE, Ortiga-Carvalho TM, Gomes FC (2010) Thyroid hormone receptor beta mutation causes severe impairment of cerebellar development. Mol Cell Neurosci 44(1):68-77
26. Wang Y, Wei W, Wang Y, Dong J, Song B, Min H, Teng W, Chen J (2013) Neurotoxicity of developmental hypothyroxinemia and hypothyroidism in rats: impairments of long-term potentiation are mediated by phosphatidylinositol 3-kinase signaling pathway. Toxicol Appl Pharmacol 271(2):257-265
27. Reeves PG, Nielsen FH, Fahey GC Jr (1993) 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 123:1939-1951 (Pubitemid 23342492)
28. Mills J, Niewmierzycka A, Oloumi A, Rico B, St-Arnaud R, Mackenzie IR, Mawji NM, Wilson J, Reichardt LF, Dedhar S (2006) Critical role of integrin-linked kinase in granule cell precursor proliferation and cerebellar development. J Neurosci 26(3):830-840 (Pubitemid 43237076)
29. Argenti B, Gallo R, Di Marcotullio L, Ferretti E, Napolitano M, Canterini S, De Smaele E, Greco A, Fiorenza MT, Maroder M, Screpanti I, Alesse E, Gulino A (2005) Hedgehog antagonist REN(KCTD11) regulates proliferation and apoptosis of developing granule cell progenitors. J Neurosci 25(36):8338-8346 (Pubitemid 41292129)
30. Kenney AM, Widlund HR, Rowitch DH (2004) Hedgehog and PI-3 kinase signaling converge on Nmyc1 to promote cell cycle progression in cerebellar neuronal precursors. Development 131(1):217-228 (Pubitemid 38111428)
31. Kawamori A, Shimaji K, Yamaguchi M (2013) Control of e2f1 and PCNA by Drosophila transcription factor DREF. Genesis. doi: 10.1002/dvg.22419
32. Vermiglio F, Lo Presti VP, Moleti M, Sidoti M, Tortorella G, Scaffidi G, Castagna MG, Mattina F, Violi MA, Crisà A, Artemisia A, Trimarchi F (2004) Attention deficit and hyperactivity disorders in the offspring of mothers exposed to mild-moderate iodine deficiency: a possible novel iodine deficiency disorder in developed countries. J Clin Endocrinol Metab 89:6054-6060 (Pubitemid 39628414)
33. Pedraza PE, Obregon MJ, Escobar-Morreale HF, del Rey FE, de Escobar GM (2006) Mechanisms of adaptation to iodine deficiency in rats: thyroid status is tissue specific. Its relevance for man. Endocrinology 147:2098-2108
34. Dunn JT (1995) Thyroglobulin, hormone synthesis and thyroid disease. Eur J Endocrinol 132:603-604
35. Dunn JT, Dunn AD (2001) Update on intrathyroidal iodine metabolism. Thyroid 11:407-414 (Pubitemid 32494590)
36. 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 (2008) 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 51:4050-4053 (Pubitemid 351956532)
37. Shin MS, Ko IG, Kim SE, Kim BK, Kim TS, Lee SH, Hwang DS, Kim CJ, Park JK, Lim BV (2013) Treadmill exercise ameliorates symptoms of methimazole-induced hypothyroidism through enhancing neurogenesis and suppressing apoptosis in the hippocampus of rat pups. Int J Dev Neurosci 31:214-223
38. Manzano J, Cuadrado M, Morte B, Bernal J (2007) Influence of thyroid hormone and thyroid hormone recptors in the generation of cerebellar gamma-aminobutyric acid-ergic interneurons from precursor cells. Endocrinology 148(12):5746-5751 (Pubitemid 350146193)
39. Chantoux F, Francon J (2002) Thyroid hormone regulates the expression of NeuroD/BHF1 during the development of rat cerebellum. Mol Cell Endocrinol 194(1-2):157-163 (Pubitemid 35291930)
40. Pop VJ, Brouwers EP, Vader HL, Vulsma T, van Baar AL, Vijlder JJ (2003) Maternal hypothyroxinaemia during early pregnancy and subsequent child development: a 3 year follow-up study. Clin Endocrinol 59:282-288 (Pubitemid 37046980)
41. Axelstad M, Hansen PR, Boberg J, Bonnichsen M, Nellemann C, Lund SP, Hougaard KS, Hass U (2008) Developmental neurotoxicity of propylthiouracil (PTU) in rats: relationship between transient hypothyroxinemia during development and long-lasting behavioural and functional changes. Toxicol Appl Pharmacol 232(1):1-13
42. Farwell AP, Dubord-Tomasetti SA, Pietrzykowski AZ, Stachelek SJ, Leonard JL (2005) Regulation of cerebellar neuronal migration and neurite outgrowth by thyroxine and 3,3′,5′-triiodothyronine. Brain Res Dev Brain Res 154(1):121-135 (Pubitemid 40023136)
43. Galliano E, Gao Z, Schonewille M, Todorov B, Simons E, Pop AS, D'Angelo E, van den Maagdenberg AM, Hoebeek FE, De Zeeuw CI (2013) Silencing the majority of cerebellar granule cells uncovers their essential role in motor learning and consolidation. Plant Cell Rep 3(4):1239-1251
44. Jiao J, Nakajima A, Janssen WG, Bindokas VP, Xiong X, Morrison JH, Brorson JR, Tang YP (2008) Expression of NR2B in cerebellar granule cells specifically facilitates effect of motor training on motor learning. PLoS One 3(2):e1684
45. Kim JC, Cook MN, Carey MR, Shen C, Regehr WG, Dymecki SM (2009) Linking genetically defined neurons to behavior through a broadly applicable silencing allele. Neuron 63(3):305-315
46. Seja P, Schonewille M, Spitzmaul G, Badura A, Klein I, Rudhard Y, Wisden W, Hübner CA, De Zeeuw CI, Jentsch TJ (2012) Raising cytosolic Cl- in cerebellar granule cells affects their excitability and vestibule-ocular learning. EMBO J 31(5):1217-1230
47. Desouza LA, Sathanoori M, Kapoor R, Rajadhyaksha N, Gonzalez LE, Kottmann AH, Tole S, Vaidya VA (2011) Thyroid hormone regulates the expression of the sonic hedgehog signaling pathway in the embryonic and adult mammalian brain. Endocrinology 152(5): 1989-2000
48. Knoepfler PS, Cheng PF, Eisenman RN (2002) N-myc is essential during neurogenesis for the rapid expansion of progenitor cell populations and the inhibition of neuronal differentiation. Genes Dev 16: 2699-2712
49. Kenney AM, Rowitch DH (2000) Sonic hedgehog promotes G (1) cyclin expression and sustained cell cycle progression in mammalian neuronal precursors. Mol Cell Biol 20:9055-9067 (Pubitemid 32245934)
50. Pogoriler J, Millen K, Utset M, Du W (2006) Loss of cyclin D1 impairs cerebellar development and suppresses medulloblastoma formation. Development 133:3929-3937 (Pubitemid 44650970)
51. Huard JM, Forster CC, Carter ML, Sicinski P, Ross ME (1999) Cerebellar histogenesis is disturbed in mice lacking cyclin D2. Development 126:1927-1935 (Pubitemid 29240326)
52. Ciemerych MA, Kenney AM, Sicinska E, Kalaszczynska I, Bronson RT, Rowitch DH, Gardner H, Sicinski P (2002) Development of mice expressing a single D-type cyclin. Genes Dev 16:3277-3289 (Pubitemid 36025979)
53. Yang Y, Sun F, Zhang C, Wang H, Wu G, Wu Z (2013) Hypoxia promotes cell proliferation by modulating E2F1 in chicken pulmonary arterial smooth muscle cells. J Anim Sci Biotechnol 4(1): 28
54. Swarnalatha M, Singh AK, Kumar V (2013) Promoter occupancy of MLL1 histone methyltransferase seems to specify the proliferative and apoptotic functions of E2F1 in a tumour microenvironment. J Cell Sci 126: 4636-4646
55. Bhatia B, Hsieh M, Kenney AM, Nahlé Z (2011) Mitogenic sonic hedgehog signaling drives E2F1-dependent lipogenesis in progenitor cells and medulloblastoma. Oncogene 30(4):410-422