Late maternal hypothyroidism alters the expression of CAMK4 in neocortical subplate neurons: A comparison with nurr1 labeling

Cerebral Cortex

Volumn 24, Issue 10, 2014, Pages 2694-2706

  Navarro, D ^a   Alvarado, M ^a,b   Morte, B ^c,d   Berbel, D ^a   Sesma, J ^a   Pacheco, P ^b   Morreale De Escobar, G ^c,d   Bernal, J ^c,d   Berbel, P ^a  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^b UNIVERSIDAD VERACRUZANA   (Mexico)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^d CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

Author keywords

Attention deficit hyperactivity disorder; Developmental neurological diseases; Hypothyroxinemia; Preterm encephalopathy; Schizophrenia

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE IV; NUCLEAR RECEPTOR RELATED FACTOR 1; CAMK4 PROTEIN, RAT; NR4A2 PROTEIN, RAT;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEMALE; FETUS DEVELOPMENT; GENE EXPRESSION; HYPOTHYROIDISM; IMMUNOREACTIVITY; MATERNAL DISEASE; NEOCORTEX; NERVE CELL; NERVE CELL DIFFERENTIATION; NONHUMAN; PARIETAL CORTEX; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAT; YOUNG ADULT; ANIMAL; FETOMATERNAL TRANSFUSION; MALE; METABOLISM; PREGNANCY; THYROIDECTOMY; TIME; WISTAR RAT;

ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 4; FEMALE; HYPOTHYROIDISM; MALE; MATERNAL-FETAL EXCHANGE; NEOCORTEX; NEURONS; NUCLEAR RECEPTOR SUBFAMILY 4, GROUP A, MEMBER 2; PREGNANCY; RATS; RATS, WISTAR; THYROIDECTOMY; TIME FACTORS;

EID: 84923272087     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bht129     Document Type: Article

References (77)

1. Addington AM, Gornick MC, Shaw P, Seal J, Gogtay N, Greenstein D, Clasen L, Coffey M, Gochman P, Long R et al. 2007. Neuregulin 1 (8p12) and childhood-onset schizophrenia: susceptibility haplotypes for diagnosis and brain developmental trajectories. Mol Psychiatry. 12:195-205.
2. Allendoerfer KL, Shatz CJ. 1994. The subplate, a transient neocortical structure: its role in the development of connections between thalamus and cortex. Annu Rev Neurosci. 17:185-218.
3. Ares S, Escobar-Morreale HF, Quero J, Durán S, Presas MJ, Herruzo R, Morreale de Escobar G. 1997. Neonatal hypothyroxinemia: effects of iodine intake and premature birth. J Clin Endocrinol Metab. 82:1704-1712.
4. Ausó E, Lavado-Autric R, Cuevas E, Escobar del Rey F, Morreale de Escobar G, Berbel P. 2004. A moderate and transient deficiency of maternal thyroid function at the beginning of fetal neocorticogenesis alters neuronal migration. Endocrinology. 145:4037-4047.
5. Bayatti N, Moss JA, Sun L, Ambrose P, Ward JF, Lindsay S, Clowry GJ. 2008. A molecular neuroanatomical study of the developing human neocortex from 8 to 17 postconceptional weeks revealing the early differentiation of the subplate and subventricular zone. Cereb Cortex. 18:1536-1548.
6. Berbel P, Marco P, Cerezo JR, DeFelipe J. 1996. Distribution of parvalbumin immunoreactivity in the neocortex of hypothyroid adult rats. Neurosci Lett. 204:65-68.
7. Berbel P, Navarro D, Ausó E, Varea E, Rodríguez AE, Ballesta JJ, de Escobar GM. 2010. Role of late maternal thyroid hormones in cerebral cortex development: an experimental model for human prematurity. Cereb Cortex. 20:1462-1475.
8. Berbel P, Obregón 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.
9. Carlezon WA Jr, Duman RS, Nestler EJ. 2005. The many faces of CREB. Trends Neurosci. 28:436-445.
10. Chawla S, Hardingham GE, Quinn DR, Bading H. 1998. CBP: a signalregulated transcriptional coactivator controlled by nuclear calcium and CaM kinase IV. Science. 281:1505-1509.
11. Chun JJ, Shatz CJ. 1989. The earliest-generated neurons of the cat cerebral cortex: characterization by MAP2 and neurotransmitter immunohistochemistry during fetal life. J Neurosci. 9:1648-1667.
12. Cuevas E, Ausó E, Telefont M, Morreale de Escobar G, Sotelo C, Berbel P. 2005. Transient maternal hypothyroxinemia at onset of corticogenesis alters tangential migration of medial ganglionic eminencederived neurons. Eur J Neurosci. 22:541-551.
13. De Carlos JA, O'Leary DD. 1992. Growth and targeting of subplate axons and establishment of major cortical pathways. J Neurosci. 12:1194-211.
14. den Ouden AL, Kok JH, Verkerk PH, Brand R, Verloove-Vanhorick SP. 1996. The relation between neonatal thyroxine levels and neurodevelopmental outcome at age 5 and 9 years in a national cohort of very preterm and/or very low birth weight premature infants. Pediatr Res. 39:142-145.
15. Eastwood SL, Harrison PJ. 2003. Interstitial white matter neurons express less reelin and are abnormally distributed in schizophrenia: towards an integration of molecular and morphologic aspects of the neurodevelopmental hypothesis. Mol Psychiatry. 8:821-831.
16. Friauf E, McConnell SK, Shatz CJ. 1990. Functional synaptic circuits in the subplate during fetal and early postnatal development of cat visual cortex. J Neurosci. 10:2601-2613.
17. Hanganu IL, Kilb W, Luhmann HJ. 2001. Spontaneous synaptic activity of subplate neurons in neonatal rat somatosensory cortex. Cereb Cortex. 11:400-410.
18. Harrison PJ, Eastwood SL. 2001. Neuropathological studies of synaptic connectivity in the hippocampal formation in schizophrenia. Hippocampus. 11:508-519.
19. Harrison PJ, Law AJ. 2006. Neuregulin 1 and schizophrenia: genetics, gene expression, and neurobiology. Biol Psychiatry. 60:132-140.
20. Hoerder-Suabiedissen A, Molnár Z. 2012. Morphology of mouse subplate cells with identified projection targets changes with age. J Comp Neurol. 520:174-185.
21. Hoerder-Suabedissen A, Molnár Z. 2013. Molecular diversity of earlyborn subplate neurons. Cereb Cortex. 23:1473-1483.
22. Hoerder-Suabedissen A, Wang WZ, Lee S, Davies KE, Goffinet AM, Rakic S, Parnavelas J, Reim K, Nicolic M, Paulsen O et al. 2009. Novel markers reveal subpopulations of subplate neurons in the murine cerebral cortex. Cereb Cortex. 19:1738-1750.
23. Johnson S. 2007. Cognitive and behavioural outcomes following very preterm birth. Semin Fetal Neonatal Med. 12:363-373.
24. Jones PB, Rantakallio P, Hartikainen AL, Isohanni M, Sipila P. 1998. Schizophrenia as a long-term outcome of pregnancy, delivery, and perinatal complications: a 28-year follow-up of the 1966 north Finland general population birth cohort. Am J Psychiatry. 155:355-364.
25. Kanold PO, Kara P, Reid RC, Shatz CJ. 2003. Role of subplate neurons in functional maturation of visual cortical columns. Science. 301:521-525.
26. Kanold PO, Kim YA, GrandPre T, Shatz CJ. 2009. Co-regulation of ocular dominance plasticity and NMDA receptor subunit expression in glutamic acid decarboxylase-65 knock-out mice. J Physiol. 587:2857-2867.
27. Kanold PO, Shatz CJ. 2006. Subplate neurons regulate maturation of cortical inhibition and outcome of ocular dominance plasticity. Neuron. 51:627-638.
28. Kester MH, Martínez de Mena R, Obregón MJ, Marinkovic D, Howatson A, Visser TJ, Hume R, Morreale de Escobar G. 2004. Iodothyronine levels in the human developing brain: major regulatory roles of iodothyronine deiodinases in different areas. J Clin Endocrinol Metab. 89:3117-3128.
29. Kinney HC, Haynes RL, Xu G, Andiman SE, Folkerth RD, Sleeper LA, Volpe JJ. 2012. Neuron deficit in the white matter and subplate in periventricular leukomalacia. Ann Neurol. 71:397-406.
30. Kostović I, Judas M. 2007. Transient patterns of cortical lamination during prenatal life: do they have implications for treatment? Neurosci Biobehav Rev. 31:1157-1168.
31. Kostović I, Rakic P. 1980. Cytology and time of origin of interstitial neurons in the white matter in infant and adult human and monkey telencephalon. J Neurocytol. 9:219-242.
32. Kostović I, Rakic P. 1990. Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J Comp Neurol. 297:441-470.
33. Krebs J, Means RL, Honegger P. 1996. Induction of calmodulin kinase IV by the thyroid hormone during the development of rat brain. J Biol Chem. 19:11055-11058.
34. Krueger DD, Bear MF. 2011. Toward fulfilling the promise of molecular medicine in fragile X syndrome. Annu Rev Med. 62:411-429.
35. 2+/calmodulin-dependent protein kinase type IV. Endocrinology. 141:2275-2278.
36. Lewis DA, Levitt P. 2002. Schizophrenia as a disorder of neurodevelopment. Annu Rev Neurosci. 25:409-432.
37. Liu YY, Brent GA. 2002. A complex deoxyribonucleic acid response element in the rat Ca(2+)/calmodulin-dependent protein kinase IV gene 5'-flanking region mediates thyroid hormone induction and chicken ovalbumin upstream promoter transcription factor 1 repression. Mol Endocrinol. 11:2439-2451.
38. Luskin MB, Shatz CJ. 1985a. Neurogenesis of the cat's primary visual cortex. J Comp Neurol. 242:611-631.
39. Luskin MB, Shatz CJ. 1985b. Studies of the earliest generated cells of the cat's visual cortex: cogeneration of subplate and marginal zones. J Neurosci. 5:1062-1075.
40. Marín-Padilla M. 1971. Early prenatal ontogenesis of the cerebral cortex (neocortex) of the cat (Felis domestica). A Golgi study. I. The primordial neocortical organization. Z Anat Entwicklungsgesch. 134:117-145.
41. 2+ and CaM kinase IV specify hormonal-and Notch-responsiveness. J Neurochem. 93:171-185.
42. McQuillen PS, Ferriero DM. 2005. Perinatal subplate neuron injury: implications for cortical development and plasticity. Brain Pathol. 15:250-260.
43. Molnár Z, Adams R, Blakemore C. 1998. Mechanisms underlying the early establishment of thalamocortical connections in the rat. J Neurosci. 18:5723-5745.
44. Molnár Z, Garel S, López-Bendito G, Maness P, Price DJ. 2012. Mechanisms controlling the guidance of thalamocortical axons through the embryonic forebrain. Eur J Neurosci. 35:1573-1585.
45. Morreale de Escobar G, Ares S. 1998. The hypothyroxinemia of prematurity. J Clin Endocrinol Metab. 83:713-715.
46. Morreale de Escobar G, Ares S, Berbel P, Obregón MJ, Escobar del Rey F. 2008. The changing role of maternal thyroid hormone in fetal brain development. Semin Perinatol. 32:380-386.
47. Morreale de Escobar G, Pastor R, Obregón MJ, Escobar del Rey F. 1985. Effects of maternal hypothyroidism on the weight and thyroid hormone content of rat embryonic tissues, before and after onset of fetal thyroid function. Endocrinology. 117:1890-1900.
48. 2+/calmodulin-dependent protein kinase IV pathway. Endocrinology. 151:810-820.
49. 2+-activated, CREB-dependent transcription in astrocytes. Glia. 57:828-834.
50. O'Callaghan MJ, Burns Y, Gray P, Harvey JM, Mohay HI, Rogers Y, Tudehope DI. 1995. Extremely low birth weight and control infants at 2 years corrected age: a comparison of intellectual abilities, motor performance, growth and health. Early Hum Dev. 40:115-128.
51. Oeschger FM, Wang WZ, Lee S, García-Moreno F, Goffinet AM, Arbonés ML, Rakic S, Molnár Z. 2012. Gene expression analysis of the embryonic subplate. Cereb Cortex. 22:1343-1359.
52. Opazo MC, Gianini A, Pancetti F, Azkcona G, Alarcón L, Lizana R, Noches V, González PA, Marassi MP, Mora S et al. 2008. Maternal hypothyroxinemia impairs spatial learning and synaptic nature and function in the offspring. Endocrinology. 149:5097-5106.
53. Piñón MC, Jethwa A, Jacobs E, Campagnoni A, Molnár Z. 2009. Dynamic integration of subplate neurons into the cortical barrel field circuitry during postnatal development in the Golli-tau-eGFP (GTE) mouse. J Physiol. 587:1903-1915.
54. Price DJ, Aslam S, Tasker L, Gillies K. 1997. Fates of the earliest generated cells in the developing murine neocortex. J Comp Neurol. 377:414-422.
55. Reuss L, Paneth N, Lorenz JM, Pinto-Martin J, Susser M. 1996. Transient hypothyroxinemia in preterm infants and neurodevelopment at age two. New Engl J Med. 334:821-827.
56. Robinson S, Li Q, Dechant A, Cohen ML. 2006. Neonatal loss of gamma-aminobutyric acid pathway expression after human perinatal brain injury. J Neurosurg. 104:396-408.
57. Rovet J, Simic N. 2008. The role of transient hypothyroxinemia of prematurity in development of visual abilities. Semin Perinatol. 32:431-437.
58. Samara M, Marlow N, Wolke D, EPICure Study Group. 2008. Pervasive behavior problems at 6 years of age in a total-population sample of children born at ≤25 weeks of gestation. Pediatrics. 122:562-573.
59. Simic N, Asztalos EV, Rovet J. 2009. Impact of neonatal thyroid hormone insufficiency and medical morbidity on infant neurodevelopment and attention following preterm birth. Thyroid. 19:395-401.
60. Smith GN, Flynn SW, McCarthy N, Meistrich B, Ehmann TS, MacEwan GW, Altman S, Kopala LC, Honer WG. 2001. Low birth weight in schizophrenia: prematurity or poor fetal growth? Schizophr Res. 47:177-184.
61. Sohn YC, Kwak E, Na Y, Lee JW, Lee SK. 2001. Silencing mediator of retinoid and thyroid hormone receptors and activating signal cointegrator-2 as transcriptional coregulators of the orphan nuclear receptor Nur77. J Biol Chem. 276:43734-43779.
62. Stolp H, Neuhaus A, Sundramoorthi R, Molnár Z. 2012. The long and the short of it: gene and environment interactions during early cortical development and consequences for long-term neurological disease. Front Psychiatry. 3:50. doi:10.3389/fpsyt.2012.00050.
63. Torres-Reveron J, Friedlander MJ. 2007. Properties of persistent postnatal cortical subplate neurons. J Neurosci. 27:9962-9974.
64. van Middlesworth L, Norris CH. 1980. Audiogenic seizures and cochlear damage in rats after perinatal antithyroid treatment. Endocrinology. 106:1686-1690.
65. van Wassenaer AG, Kok JH. 2004. Hypothyroxinaemia and thyroid function after preterm birth. Semin Neonatol. 9:3-11.
66. Volpe JJ 2009. Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol. 8:110-124.
67. Volpe JJ 1996. Subplate neurons-missing link in brain injury of the premature infant? Pediatrics. 97:112-113.
68. 2+/calmodulindependent protein kinase IV links group I metabotropic glutamate receptors to fragile X mental retardation protein in cingulate cortex. J Biol Chem. 284:18953-18962.
69. Wang H, Morishita Y, Miura D, Naranjo JR, Kida S, Zhuo M. 2012. Roles of CREB in the regulation of FMRP by group I metabotropic glutamate receptors in cingulate cortex. Mol Brain. 5:27. doi:10.1186/1756-6606-5-27.
70. 2+/calmodulindependent protein kinase IV (CaMKIV) messenger RNA during murine embryogenesis. Cell Growth Differ. 12:351-361.
71. Wang WZ, Oeschger FM, Montiel JF, García-Moreno F, HoerderSuabedissen A, Krubitzer L, Ek CJ, Saunders NR, Reim K, Villalón A et al. 2011. Comparative aspects of subplate zone studied with gene expression in sauropsids and mammals. Cereb Cortex. 21:2187-2203.
72. Watakabe A, Ichinohe N, Ohsawa S, Hashikawa T, Komatsu Y, Rockland KS, Yamamori T. 2007. Comparative analysis of layer-specific genes in mammalian neocortex. Cereb Cortex. 17:1918-1933.
73. Watterson DM, Mirzoeva S, Guo L, Whyte A, Bourguignon JJ, Hibert M, Haiech J, Van Eldik LJ 2001. Ligand modulation of glial activation: cell permeable, small molecule inhibitors of serine-threonine protein kinases can block induction of interleukin 1 beta and nitric oxide synthase II. Neurochem Int. 39:459-468.
74. Williams FL, Hume R. 2008. Perinatal factors affecting thyroid hormone status in extreme preterm infants. Semin Perinatol. 32:398-402.
75. Williams FL, Mires GJ, Barnett C, Ogston SA, van Toor H, Visser TJ, Hume R. 2005. Transient hypothyroxinemia in preterm infants: the role of cord sera thyroid hormone levels adjusted for prenatal and intrapartum factors. J Clin Endocrinol Metab. 90:4599-4606.
76. Xing G, Zhang L, Russell S, Post R. 2006. Reduction of dopamine-related transcription factors Nurr1 and NGFI-B in the prefrontal cortex in schizophrenia and bipolar disorders. Schizophr Res. 84:36-56.
77. Zoeller RT, Rovet J. 2004. Timing of thyroid hormone action in the developing brain: clinical observations and experimental findings. J Neuroendocrinol. 16:809-818.