Thyroid hormone level positively regulates nos and cgmp in the developing rat cerebellum

Neuroendocrinology

Volumn 89, Issue 3, 2009, Pages 337-350

  Serfz, Zoltán ^a   De Vente, Jan ^b   Elekes, Károly ^a  

^a BALATON LIMNOLOGICAL RESEARCH INSTITUTE   (Hungary)

^b MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Cerebellum; Cyclic guanosine monophosphate; Development; Nitric oxide synthase; Thyroid hormone

Indexed keywords

CALCIUM; CYCLIC GMP; LIOTHYRONINE; NEURONAL NITRIC OXIDE SYNTHASE; NEUROTROPHIN; PROPYLTHIOURACIL; THYROTROPIN; THYROXINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN DEVELOPMENT; CEREBELLUM; CONTROLLED STUDY; HYPERTHYROIDISM; HYPOTHYROIDISM; IMMUNOHISTOCHEMISTRY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; RAT; WESTERN BLOTTING;

AGING; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; CEREBELLUM; CYCLIC GMP; FEMALE; NITRIC OXIDE SYNTHASE; PROPYLTHIOURACIL; RATS; RATS, WISTAR; THYROTROPIN; THYROXINE; TRIIODOTHYRONINE; UP-REGULATION;

EID: 67349111304     PISSN: 00283835     EISSN: None     Source Type: Journal    
DOI: 10.1159/000203644     Document Type: Article

References (51)

1. Koibuchi N, Jingu H, Iwasaki T, Chin WW: Current perspectives on the role of thyroid hormone in growth and development of cerebellum. Cerebellum 2003; 2: 279-289.
2. Legrand J: Variations, en fonction de l'âgé, de la réponse du cervelet a l'action morphogénétique de la thyroïde chez la rat. Arch Anat Microsc Morphol Exp 1967; 56: 291-308.
3. Dong H, Wade M, Williams A, Lee A, Douglas GR, Yauk C: Molecular insight into the effects of hypothyroidism on the developing cerebellum. Biochem Biophys Res Commun 2005; 330: 1182-1193.
4. Gothe S, Wang Z, Ng L, Kindblom JM, Barros AC, Ohlsson C, Vennstrom B, Forrest D: Mice devoid of all known thyroid hormone receptors are viable but exhibit disorders of the pituitary-thyroid axis, growth, and bone maturation. Genes Dev 1999; 13: 1329-1341.
5. Gauthier K, Plateroti M, Harvey CB, Williams GR, Weiss RE, Refetoff S, Willott JF, Sundin V, Roux JP, Malaval L, Hara M, Samarut J, Chassande O: Genetic analysis reveals different functions for the products of the thyroid hormone receptor locus. Mol Cell Biol 2001; 21: 4748-4760.
6. Haas MJ, Mreyoud A, Fishman M, Mooradian AD: Microarray analysis of thyroid hormone-induced changes in mRNA expression in the adult rat brain. Neurosci Lett 2004; 365: 14-18.
7. Davis PJ, Leonard JL, Davis FB: Mechanisms of nongenomic actions of thyroid hormone. Front Neuroendocrinol 2008; 29: 211-218.
8. Garthwaite J, Charles SL, Chess-Williams R: Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain. Nature 1988; 336: 385-388.
9. Vincent SR: Nitric oxide and synaptic plasticity: NO news from the cerebellum. Behav Brain Sci 1996; 19: 362-367.
10. Ding JD, Burette A, Nedvetsky PI, Schmidt HH, Weinberg RJ: Distribution of soluble guanylyl cyclase in the rat brain. J Comp Neurol 2004; 472: 437-448.
11. El-Husseini AE, Williams J, Reiner PB, Pelech S, Vincent SR: Localization of the cGMP-dependent protein kinases in relation to nitric oxide synthase in the brain. J Chem Neuroanat 1999; 17: 45-55.
12. Shin JH, Linden DJ: An NMDA receptor/nitric oxide cascade is involved in cerebellar long-term depression but is not localized to the parallel fiber terminal. J Neurophysiol 2005; 94: 4281-4289.
13. Maffei A, Prestori F, Shibuki K, Rossi P, Taglietti V, D'Angelo E: NO enhances presynaptic currents during cerebellar mossy fiber-granule cell long-term potentiation. J Neurophysiol 2003; 90: 2478-2483.
14. Casado M, Dieudonne S, Ascher P: Presynaptic N -methyl-D -aspartate receptors at the parallel fiber-Purkinje cell synapse. Proc Natl Acad Sci USA 2000; 97: 11593-11597.
15. Smith SL, Otis TS: Persistent changes in spontaneous firing of Purkinje neurons triggered by the nitric oxide signaling cascade. J Neurosci 2003; 23: 367-372.
16. Jacoby S, Sims RE, Hartell NA: Nitric oxide is required for the induction and heterosynaptic spread of long-term potentiation in rat cerebellar slices. J Physiol 2001; 535: 825-839.
17. Ciani E, Calvanese V, Crochemore C, Bartesaghi R, Contestabile A: Proliferation of cerebellar precursor cells is negatively regulated by nitric oxide in newborn rat. J Cell Sci 2006; 119: 3161-3170.
18. Yan XX, Jen LS, Garey LJ: Parasagittal patches in the granule layer of the developing and adult rat cerebellum as demonstrated by NADPH-diaphorase histochemistry. Neuroreport 1993; 4: 1227-1230.
19. Dermon CR, Stamatakis A: Laminar pattern of NADPH-diaphorase activity in the developing avian cerebellum. Neuroreport 1994; 5: 1941-1945.
20. Ogilvie P, Schilling K, Billingsley ML, Schmidt HH: Induction and variants of neuronal nitric oxide synthase type I during synaptogenesis. FASEB J 1995; 9: 799-806.
21. Schilling K, Schmidt HH, Baader SL: Nitric oxide synthase expression reveals compartments of cerebellar granule cells and suggests a role for mossy fibers in their development. Neuroscience 1994; 59: 893-903.
22. Sinha RA, Pathak A, Mohan V, Bandyopadhyay S, Rastogi L, Godbole MM: Maternal thyroid hormone: a strong repressor of neuronal nitric oxide synthase (nNOS) in rat embryonic neocortex. Endocrinology 2008; 149: 4396-4401.
23. Serfozo Z, Kiss PB, Kukor Z, Lontay B, Palatka K, Varga V, Erdodi F, Elekes K: Thyroid hormones affect the level and activity of nitric oxide synthase in rat cerebral cortex during postnatal development. Neurochem Res 2008; 33: 569-578.
24. Ueta Y, Levy A, Chowdrey HS, Lightman SL: Hypothalamic nitric oxide synthase gene expression is regulated by thyroid hormones. Endocrinology 1995; 136: 4182-4187.
25. Chakrabarti N, Ray AK: Rise of intrasynaptosomal Ca 2+ level and activation of nitric oxide synthase in adult rat cerebral cortex pretreated with 3,5,3 - L -triiodothyronine. Neuropsychopharmacology 2000; 22: 36-41.
26. Vargas F, Moreno JM, Rodriguez-Gomez I, Wangensteen R, Osuna A, Alvarez-Guerra M, Garcia-Estan J: Vascular and renal function in experimental thyroid disorders. Eur J Endocrinol 2006; 154: 197-212.
27. Morreale de Escobar G, Pastor R, Obregon MJ, Escobar del Rey F: Effects of maternal hypothyroidism on the weight and thyroid hormone content of rat embryonic tissues, before and after onset of fetal thyroid function. Endocrinology 1985; 117: 1890-1900.
28. Tanaka J, Markerink-van Ittersum M, Steinbusch HW, De Vente J: Nitric oxide-mediated cGMP synthesis in oligodendrocytes in the developing rat brain. Glia 1997; 19: 286-297.
29. Goldberg ND, Haddox MK: Quantitation of cyclic GMP by enzymatic cycling. Methods Enzymol 1974; 38: 73-84.
30. Keilhoff G, Seidel B, Noack H, Tischmeyer W, Stanek D, Wolf G: Patterns of nitric oxide synthase at the messenger RNA and protein levels during early rat brain development. Neuroscience 1996; 75: 1193-1201.
31. Wang W, Nakayama T, Inoue N, Kato T: Quantitative analysis of nitric oxide synthase expressed in developing and differentiating rat cerebellum. Brain Res Dev Brain Res 1998; 111: 65-75.
32. Jurado S, Sanchez-Prieto J, Torres M: Expression of cGMP-dependent protein kinases (I and II) and neuronal nitric oxide synthase in the developing rat cerebellum. Brain Res Bull 2005; 65: 111-115.
33. Matsumoto T, Pollock JS, Nakane M, Forstermann U: Developmental changes of cytosolic and particulate nitric oxide synthase in rat brain. Brain Res Dev Brain Res 1993; 73: 199-203.
34. Tanaka M, Yoshida S, Yano M, Hanaoka F: Roles of endogenous nitric oxide in cerebellar cortical development in slice cultures. Neuroreport 1994; 5: 2049-2052.
35. Hindley S, Juurlink BH, Gysbers JW, Middlemiss PJ, Herman MA, Rathbone MP: Nitric oxide donors enhance neurotrophininduced neurite outgrowth through a cGMPdependent mechanism. J Neurosci Res 1997; 47: 427-439.
36. Peunova N, Enikolopov G: Nitric oxide triggers a switch to growth arrest during differentiation of neuronal cells. Nature 1995; 375: 68-73.
37. Hawkes R, Turner RW: Compartmentation of NADPH-diaphorase activity in the mouse cerebellar cortex. J Comp Neurol 1994; 346: 499-516.
38. Sakaue M, Kuno T, Tanaka C: Novel type of monoclonal antibodies against cyclic GMP and application to immunocytochemistry of the rat brain. Jpn J Pharmacol 1988; 48: 47-56.
39. Biggio G, Corda MG, Casu M, Salis M, Gessa GL: Disappearance of cerebellar cyclic GMP induced by kainic acid. Brain Res 1978; 154: 203-208.
40. De Vente J, Bol JG, Steinbusch HW: Localization of cGMP in the cerebellum of the adult rat: an immunohistochemical study. Brain Res 1989; 504: 332-337.
41. De Vente J, Bol JG, Berkelmans HS, Schipper J, Steinbusch HM: Immunocytochemistry of cGMP in the cerebellum of the immature, adult, and aged rat: the involvement of nitric oxide. A micropharmacological study. Eur J Neurosci 1990; 2: 845-862.
42. De Vente J, Steinbusch HW: On the stimulation of soluble and particulate guanylate cyclase in the rat brain and the involvement of nitric oxide as studied by cGMP immunocytochemistry. Acta Histochem 1992; 92: 13-38.
43. Cheng A, Wang S, Cai J, Rao MS, Mattson MP: Nitric oxide acts in a positive feedback loop with BDNF to regulate neural progenitor cell proliferation and differentiation in the mammalian brain. Dev Biol 2003; 258: 319-333.
44. Luo D, Leung E, Vincent SR: Nitric oxidedependent efflux of cGMP in rat cerebellar cortex: an in vivo microdialysis study. J Neurosci 1994; 14: 263-271.
45. Neveu I, Arenas E: Neurotrophins promote the survival and development of neurons in the cerebellum of hypothyroid rats in vivo. J Cell Biol 1996; 133: 631-646.
46. Samdani AF, Newcamp C, Resink A, Facchinetti F, Hoffman BE, Dawson VL, Dawson TM: Differential susceptibility to neurotoxicity mediated by neurotrophins and neuronal nitric oxide synthase. J Neurosci 1997; 17: 4633-4641.
47. Xiong H, Yamada K, Han D, Nabeshima T, Enikolopov G, Carnahan J, Nawa H: Mutual regulation between the intercellular messengers nitric oxide and brain-derived neurotrophic factor in rodent neocortical neurons. Eur J Neurosci 1999; 11: 1567-1576.
48. Baader SL, Bucher S, Schilling K: The developmental expression of neuronal nitric oxide synthase in cerebellar granule cells is sensitive to GABA and neurotrophins. Dev Neurosci 1997; 19: 283-290.
49. Sasaki M, Gonzalez-Zulueta M, Huang H, Herring WJ, Ahn S, Ginty DD, Dawson VL, Dawson TM: Dynamic regulation of neuronal NO synthase transcription by calcium influx through a CREB family transcription factor-dependent mechanism. Proc Natl Acad Sci USA 2000; 97: 8617-8622.
50. Xiao Q, Nikodem VM: Apoptosis in the developing cerebellum of the thyroid hormone- deficient rat. Front Biosci 1998; 3: A52-A57.
51. Singh R, Upadhyay G, Kumar S, Kapoor A, Kumar A, Tiwari M, Godbole MM: Hypothyroidism alters the expression of Bcl-2 family genes to induce enhanced apoptosis in the developing cerebellum. J Endocrinol 2003; 176: 39-46.