Developmental hypothyroxinaemia induced by maternal mild iodine deficiency delays hippocampal axonal growth in the rat offspring

Journal of Neuroendocrinology

Volumn 25, Issue 9, 2013, Pages 852-862

  Wei, W ^a   Wang, Y ^a   Dong, J ^a   Min, H ^a   Song, B ^a   Teng, W ^a   Xi, Q ^a,b   Chen, J ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Axon; Hippocampus; Hypothyroidism; Hypothyroxinaemia; Iodine deficiency

Indexed keywords

COLLAPSIN RESPONSE MEDIATOR PROTEIN 2; GLYCOGEN SYNTHASE KINASE 3BETA; IODINE; LIOTHYRONINE; NEUROMODULIN; SEMAPHORIN 3A; THYROTROPIN; THYROXINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIET; DOWN REGULATION; ENDOCRINE DISEASE; FEMALE; HIPPOCAMPUS; HYPOTHYROIDISM; HYPOTHYROXINEMIA; IMMUNOFLUORESCENCE; IODINE DEFICIENCY; MATERNAL NUTRITION; MEASUREMENT; NERVE CELL GROWTH; NONHUMAN; PRIORITY JOURNAL; PROGENY; PROTEIN PHOSPHORYLATION; RAT;

AXON; HIPPOCAMPUS; HYPOTHYROIDISM; HYPOTHYROXINAEMIA; IODINE DEFICIENCY;

ANIMALS; AXONS; CELL ENLARGEMENT; FEMALE; GAP-43 PROTEIN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCOGEN SYNTHASE KINASE 3; HIPPOCAMPUS; HYPOTHYROIDISM; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; IODINE; MALE; METHIMAZOLE; NERVE TISSUE PROTEINS; PHOSPHORYLATION; PREGNANCY; RATS; SEMAPHORIN-3A; TAU PROTEINS;

EID: 84882663298     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/jne.12058     Document Type: Article

References (50)

1. Koromilas C, Liapi C, Schulpis KH, Kalafatakis K, Zarros A, Tsakiris S. Structural and functional alterations in the hippocampus due to hypothyroidism. Metab Brain Dis 2010; 25: 339-354.
2. Bernal J. Thyroid hormones and brain development. Vitam Horm 2005; 71: 95-122.
3. Sui L, Gilbert ME. Pre- and postnatal propylthiouracil-induced hypothyroidism impairs synaptic transmission and plasticity in area CA1 of the neonatal rat hippocampus. Endocrinology 2003; 144: 4195-4203.
4. Berbel P, Obregón 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.
5. Zimmermann MB. Iodine deficiency. Endocr Rev 2009; 30: 376-408.
6. Chen ZP. New cretins discovered in southern Xinjiang, China. IDD Newsletter 2007; 23: 18.
7. Morreale de Escobar G, Obregón MJ, Escobar del Rey F. Is neuropsychological development related to maternal hypothyroidism or to maternal hypothyroxinemia? J Clin Endocrinol Metab 2000; 85: 3975-3987.
8. Zoeller RT, Rover J. Timing of thyroid hormone action in the developing brain: clinical observations and experimental findings. J Neuroendocrinol 2004; 16: 809-818.
9. 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.
10. Pop VJ, Brouwers EP, Vader HL, Vulsma T, van Baar AL, de Vijlder JJ. Maternal hypothyroxinemia during early pregnancy and subsequent child development: a 3-year follow-up study. Clin Endocrinol (Oxf) 2003; 59: 282-288.
11. Skeaff SA. Iodine deficiency in pregnancy: the effect on neurodevelopment in the child. Nutrients 2011; 3: 265-273.
12. Kannan M, Lee SJ, Schwedhelm-Domeyer N, Stegmüller J. The E3 ligase Cdh1-anaphase promoting complex operates upstream of the E3 ligase Smurf1 in the control of axon growth. Development 2012; 139: 3600-3612.
13. Di Giovanni S. Molecular targets for axon regeneration: focus on the intrinsic pathways. Expert Opin Ther Targets 2009; 13: 1387-1398.
14. Dani JW, Armstrongd DM, Benowitzl LI. Mapping the development of the rat brain by GAP-43 immunochemistry. Neuroscience 1999; 40: 277-287.
15. Aigner L, Arber S, Kapfhammer JP, Laux T, Schneider C, Botteri F, Brenner HR, Caroni P. Overexpression of the neural growth associated protein GAP-43 induces nerve sprouting in the adult nervous system of transgenic mice. Cell 1995; 83: 269-278.
16. Anderson CN, Ohta K, Quick MM, Fleming A, Keynes R, Tannahill D. Molecular analysis of axon repulsion by the notochord. Development 2003; 130: 1123-1133.
17. Pasterkamp RJ, Ruitenberg MJ, Verhaagen J. Semaphorins and their receptors in olfactory axon guidance. Cell Mol Biol 1999; 45: 763-779.
18. Yoshimura T, Arimura N, Kaibuchi K. Molecular mechanisms of axon specification and neuronal disorders. Ann NY Acad Sci 2006; 1086: 116-125.
19. Yoshimura T, Kawano Y, Arimura N, Kikuchi A, Kaibuchi K. GSK-3beta regulates phosphorylation of CRMP-2 and neuronal polarity. Cell 2005; 120: 137-149.
20. Inagaki N, Chihara K, Arimura N, Menager C, Kawano Y, Matsuo N, Nishimura T, Amano M, Kaibuchi K. CRMP-2 induces axons in cultured hippocampal neurons. Nat Neurosci 2001; 4: 781-782.
21. Puymirat J. Thyroid receptors in the rat brain. Prog Neurobiol 1992; 39: 281-294.
22. White AM, Matthews DB, Best PJ. Ethanol, memory, and hippocampal function: a review of recent findings. Hippocampus 2000; 10: 88-93.
23. 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.
24. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates-Compact Third Edition. San Diego, CA: Academic Press, 1996.
25. Jiang H, Guo W, Liang X, Rao Y. Both the establishment and the maintenance of neuronal polarity require active mechanisms critical roles of GSK3beta and its upstream regulators. Cell 2005; 120: 123-135.
26. Cole AR, Knebel A, Morrice NA, Robertson LA, Irving AJ, Connolly CN, Sutherland C. GSK-3 phosphorylation of the Alzheimer epitope within collapsin response mediator proteins regulates axon elongation in primary neurons. J Biol Chem 2004; 279: 50176-50180.
27. Pedraza PE, Obregon MJ, Escobar-Morreale HF, del Rey FE, de Escobar GM. Mechanisms of adaptation to iodine deficiency in rats: thyroid status is tissue specific. Its relevance for man. Endocrinology 2006; 147: 2098-2108.
28. 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.
29. 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. 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 2004; 89: 6054-6060.
30. Escobar del Rey F, Mallol J, Pastor R, Morreale de Escobar G. Effects of maternal iodine deficiency on thyroid hormone economy of lactating dams and pups: maintenance of normal cerebral 3, 5, 3′-triiodo-L-thyronine concentrations in pups during major phases of brain development. Endocrinology 1987; 121: 803-811.
31. Bretin S, Reibel S, Charrier E, Maus-Moatti M, Auvergnon N, Thevenoux A, Glowinski J, Rogemond V, Prémont J, Honnorat J, Gauchy C. Differential expression of CRMP1, CRMP2A, CRMP2B, and CRMP5 in axons or dendrites of distinct neurons in the mouse brain. J Comp Neurol 2005; 486: 1-17.
32. Suzuki Y, Nakagomi S, Namikawa K, Kiryu-Seo S, Inagaki N, Kaibuchi K, Aizawa H, Kikuchi K, Kiyama H. Collapsin response mediator protein-2 accelerates axon regeneration of nerve-injured motor neurons of rat. J Neurochem 2003; 86: 1042-1050.
33. Oestreicher AB, de Graan PN, Gispen WH, Verhaagen J, Schrama LH. B-50, the growth associated protein-43: modulation of cell morphology and communication in the nervous system. Prog Neurobiol 1997; 53: 627-686.
34. Wang P, Jeng CJ, Chien CL, Wang SM. Signaling mechanisms of daidzein-induced axonal outgrowth in hippocampal neuron. Biochem Biophys Res Commun 2008; 8: 366.
35. Wilcoxon JS, Nadolski GJ, Samarut J, Chassande O, Redei EE. Behavioral inhibition and impaired spatial learning and memory in hypothyroid mice lacking thyroid hormone receptor alpha. Behav Brain Res 2007; 177: 109-116.
36. Shelly M, Cancedda L, Lim BK, Popescu AT, Cheng PL, Gao H, Poo MM. Semaphorin3A regulates neuronal polarization by suppressing axon formation and promoting dendrite growth. Neuron 2011; 71: 433-446.
37. Montolio M, Messeguer J, Masip I, Guijarro P, Gavin R, Antonio Del Río J, Messeguer A, Soriano E. A semaphorin 3A inhibitor blocks axonal chemorepulsion and enhances axon regeneration. Chem Biol 2009; 16: 691-701.
38. Van Vactor DV, Lorenz LJ. Neural development: the semantics of axon guidance. Curr Biol 1999; 9: 201-204.
39. Takahashi M, Tomizawa K, Kato R, Sato K, Uchida T, Fujita SC, Imahori K. Localization and developmental changes of τ protein kinase I glycogen synthase kinase3β in rat brain. J Neurochem 1994; 63: 245-255.
40. Hur EM, Zhou FQ. GSK3 signalling in neural development. Nat Rev Neurosci 2010; 11: 539-551.
41. Grimes CA, Jope RS. The multifaceted roles of glycogen synthase kinase 3β in cellular signaling. Prog Neurobiol 2001; 65: 391-426.
42. Fukata Y, Itoh TJ, Kimura T, Menager C, Nishimura T, Shiromizu T, Watanabe H, Inagaki N, Iwamatsu A, Hotani H, Kaibuchi K. CRMP-2 binds to tubulin heterodimers to promote microtubule assembly. Nat Cell Biol 2002; 4: 583-591.
43. Rogemond V, Auger C, Giraudon P, Becchi M, Auvergnon N, Belin MF, Honnorat J, Moradi-Améli M. Processing and nuclear localization of CRMP2 during brain development induce neurite outgrowth inhibition. J Biol Chem 2008; 23: 283.
44. Yoshimura T, Arimura N, Kawano Y, Kawabata S, Wang S, Kaibuchi K. Ras regulates neuronal polarity via the PI3-kinase/Akt/GSK-3beta/CRMP-2 pathway. Biochem Biophys Res Commun 2006; 340: 62-68.
45. Calvo R.M., Jauniaux E, Gulbis B, Asunción M, Gervy C, Contempré B, Morreale de Escobar G. Fetal tissues are exposed to biologically relevant free thyroxine concentrations during early phases of development. J Clin Endocrinol Metab 2002; 87: 1768-1777.
46. Gereben B, Zavacki AM, Ribich S, Kim BW, Huang SA, Simonides WS, Zeöld A, Bianco AC. Cellular and molecular basis of deiodinase-regulated thyroid hormone signaling. Endocr Rev 2008; 29: 898-938.
47. Arrojo E, Drigo R, Fonseca TL, Werneck-de-Castro JP, Bianco AC. Role of the type 2 iodothyronine deiodinase (D2) in the control of thyroid hormone signaling. Biochim Biophys Acta 2013; 1830: 3956-3964.
48. Lin HY, Hopkins R, Cao HJ, Tang HY, Alexander C, Davis FB, Davis PJ. Acetylation of nuclear hormone receptor superfamily members: thyroid hormone causes acetylation of its own receptor by a mitogen-activated protein kinase dependent mechanism. Steroids 2005; 70: 444-449.
49. Davis PJ, Shih A, Lin HY, Martino LJ, Davis FB. Thyroxine promotes association of mitogen-activated protein kinase and nuclear thyroid hormone receptor (TR) and causes serine phosphorylation of TR. J Biol Chem 2000; 275: 38032-38039.
50. Babu S, Sinha RA, Mohan V, Rao G, Pal A, Pathak A, Singh M, Godbole MM. Effect of hypothyroxinemia on thyroid hormone responsiveness and action during rat postnatal neocortical development. Exp Neurol 2011; 228: 91-98.