Prostaglandin E2 is an endogenous modulator of cerebellar development and complex behavior during a sensitive postnatal period

European Journal of Neuroscience

Volumn 35, Issue 8, 2012, Pages 1218-1229

  Dean, Shannon L ^a   Knutson, Jessica F ^a   Krebs Kraft, Desiree L ^a   Mccarthy, Margaret M ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Autism; Cerebellum; Cyclo oxygenase; Dendritic; Rat

Indexed keywords

PROSTAGLANDIN E2; PROSTAGLANDIN SYNTHASE; SPINOPHILIN;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL MATURATION; CEREBELLUM ATROPHY; CONTROLLED STUDY; ENZYME INHIBITION; FEMALE; MALE; NONHUMAN; PERCEPTIVE THRESHOLD; PERINATAL PERIOD; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS; PURKINJE CELL; RAT; SEX DIFFERENCE; SOCIAL INTERACTION; TASK PERFORMANCE;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; CELL COUNT; CEREBELLUM; DENDRITES; DINOPROSTONE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; EXPLORATORY BEHAVIOR; FEMALE; INJECTIONS, INTRAVENTRICULAR; INJECTIONS, SUBCUTANEOUS; MALE; MICROFILAMENT PROTEINS; NERVE TISSUE PROTEINS; ORGAN CULTURE TECHNIQUES; PLAY AND PLAYTHINGS; PSYCHOMOTOR PERFORMANCE; PURKINJE CELLS; RATS; REGRESSION ANALYSIS; SENSORY THRESHOLDS; SEX FACTORS; SILVER STAINING; TIME FACTORS;

EID: 84859959669     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2012.08032.x     Document Type: Article

References (72)

1. Abel, J.M., Witt, D.M. & Rissman, E.F. (2011) Sex differences in the cerebellum and frontal cortex: roles of estrogen receptor alpha and sex chromosome genes. Neuroendocrinology, 93, 230-240.
2. Akaneya, Y. & Tsumoto, T. (2006) Bidirectional trafficking of prostaglandin E2 receptors involved in long-term potentiation in visual cortex. J. Neurosci., 26, 10209-10221.
3. Ali, F.Y., Egan, K., FitzGerald, G.A., Desvergne, B., Wahli, W., Bishop-Bailey, D., Warner, T.D. & Mitchell, J.A. (2006) Role of prostacyclin versus peroxisome proliferator-activated receptor beta receptors in prostacyclin sensing by lung fibroblasts. Am. J. Respir. Cell Mol. Biol., 34, 242-246.
4. Allen, G. & Courchesne, E. (2003) Differential effects of developmental cerebellar abnormality on cognitive and motor functions in the cerebellum: an fMRI study of autism. Am. J. Psychiatry, 160, 262-273.
5. Allen, G., Buxton, R.B., Wong, E.C. & Courchesne, E. (1997) Attentional activation of the cerebellum independent of motor involvement. Science, 275, 1940-1943.
6. Altman, J. (1972) Postnatal development of the cerebellar cortex in the rat. II. Phases in the maturation of Purkinje cells and of the molecular layer. J. Comp. Neurol., 145, 399-463.
7. Amateau, S.K. & McCarthy, M.M. (2002) A novel mechanism of dendritic spine plasticity involving estradiol induction of prostaglandin-E2. J. Neurosci., 22, 8586-8596.
8. Amateau, S.K. & McCarthy, M.M. (2004) Induction of PGE2 by estradiol mediates developmental masculinization of sex behavior. Nat. Neurosci., 7, 643-650.
9. Ameteau, S.K., Alt, J.J., Stamps, C.L. & McCarthy, M.M. (2004) Brian estradiol content in newborn rats: sex differences, regional heterogeneity, and possible de novo synthesis by the female telencephalon. Endocrinology, 145, 2906-2917.
10. Andreasson, K. (2010) Emerging roles of PGE2 receptors in models of neurological disease. Prostalgandins Other Lipid Mediat., 91, 104-112.
11. Auger, A.P. & Olesen, K.M. (2009) Brain sex differences and the organisation of juvenile social play behaviour. J. Neuroendocrinol., 21, 519-525.
12. Bellebaum, C. & Daum, I. (2007) Cerebellar involvement in executive control. Cerebellum, 6, 184-192.
13. Berntson, G.G. & Schumacher, K.M. (1980) Effects of cerebellar lesions on activity, social interactions, and other motivated behaviors in the rat. J. Comp. Physiol. Psychol., 94, 706-717.
14. Blatteis, C.M. (2006) Endotoxic fever: new concepts of its regulation suggest new approaches to its management. Pharmacol. Ther., 111, 194-223.
15. Burks, S.R., Wright, C.L. & McCarthy, M.M. (2007) Exploration of prostanoid receptor subtype regulating estradiol and prostaglandin E2 induction of spinophilin in developing preoptic area neurons. Neuroscience, 146, 1117-1127.
16. Cauda, F., Geda, E., Sacco, K., D'Agata, F., Duca, S., Geminiani, G. & Keller, R. (2011) Grey matter abnormality in autism spectrum disorder: an activation likelihood estimation meta-analysis study. J. Neurol. Neurosurg. Psychiatry, 82, 1304-1313.
17. Chen, C., Magee, J.C. & Bazan, N.G. (2002) Cyclooxygenase-2 regulates prostaglandin E3 signaling in hippocampal long-term synaptic plasticity. J. Neurophysiol., 87, 2851-2857.
18. Courchesne, E., Hesselink, J.R., Jernigan, T.L. & Yeung-Courchesne, R. (1987) Abnormal neuroanatomy in a nonretarded person with autism. Unusual findings with magnetic resonance imaging. Arch. Neurol., 44, 335-341.
19. Courchesne, E., Yeung-Courchesne, R., Press, G.A., Hesselink, J.R. & Jernigan, T.L. (1988) Hypoplasia of cerebellar vermal lobules VI and VII in autism. N. Engl. J. Med., 318, 1349-1354.
20. Courchesne, E., Saitoh, O., Townsend, J.P., Yeung-Courchesne, R., Press, G.A., Lincoln, A.J., Haas, R.H. & Schriebman, L. (1994) Cerebellar hypoplasia and hyperplasia in infantile autism. Lancet, 343, 63-64.
21. Crepel, F., Delhaye-Bouchaud, N. & Dupont, J.L. (1981) Fate of the multiple innervation of cerebellar Purkinje cells by climbing fibers in immature control, X-irradiated and hypothyroid rats. Brain Res., 227, 59-71.
22. Darba, S., Garau, A., Balada, F., Sala, J. & Marti-Carbonell, M.A. (2003) Perinatal hypothyroidism effects on neuromotor competence, novelty-directed exploratory and anxiety-related behaviour and learning in rats. Behav. Brain Res., 143, 209-215.
23. Dean, S.L. & McCarthy, M.M. (2008) Steroids, sex and the cerebellar cortex: implications for human disease. Cerebellum, 7, 38-47.
24. Dean, R.L., Scozzafava, J., Goas, J.A., Regan, B., Beer, B. & Bartus, R.T. (1981) Age-related differences in behavior across the life-span of the C57BL/6 mouse. Exp. Aging Res., 7, 427-451.
25. Estes, A., Shaw, D.W., Sparks, B.F., Friedman, S., Giedd, J.N., Dawson, G., Bryan, M. & Dager, S.R. (2011) Basal ganglia morphometry and repetitive behavior in young children with autism spectrum disorder. Autism Res., 4, 212-220.
26. Feng, J., Yan, Z., Ferreira, A., Tomizawa, K., Liauw, J.A., Zhuo, M., Allen, P.B., Ouimet, C.C. & Greengard, P. (2000) Spinophilin regulates the formation and function of dendritic spines. Proc. Natl. Acad. Sci. USA, 97, 9287-9292.
27. Fester, L., Zhou, L., Voets, C., Ossig, C., Disteldorf, E., Bläute, F., Prange-Kiel, J., Dudzinski, D., Jarry, H. & Rune, G.M. (2011) The opposing roles of estradiol on synaptic protein expression in hippocampal cultures. Psychoneuroendocrino., 36, 148.
28. Giedd, J.N., Snell, J.W., Lange, N., Rajapakse, J.C., Casey, B.J., Kozuch, P.L., Vaituzis, A.C., Vauss, Y.C., Hamburger, S.D., Kaysen, D. & Rapoport, J.L. (1996) Quantitative magnetic resonance imaging of human brain development: ages 4-18. Cereb. Cortex, 6, 551-560.
29. Glaser, E.M. & Van der Loos, H. (1981) Analysis of thick brain sections by obverse-reverse computer microscopy: application of a new, high clarity Golgi-Nissl stain. J. Neurosci. Methods, 4, 117-125.
30. Goldblatt, M.W. (1935) Properties of human seminal plasma. J. Physiol., 84, 208-218.
31. Hamson, D.K., Csupity, A.S., Gaspar, J.M. & Watson, N.V. (2009) Analysis of Foxp2 expression in the cerebellum reveals a possible sex difference. NeuroReport, 20, 611-616.
32. Heath, R.G., Dempesy, C.W., Fontana, C.J. & Myers, W.A. (1978) Cerebellar stimulation: effects on septal region, hippocampus, and amygdala of cats and rats. Biol. Psychiatry, 13, 501-529.
33. Heitz, S., Gautheron, V., Lutz, Y., Rodeau, J.L., Zanjani, H.S., Sugihara, I., Bombarde, G., Richard, F., Fuchs, J.P., Vogel, M.W., Mariani, J. & Bailly, Y. (2008) BCL-2 counteracts doppel-induced apoptosis of prion-protein-deficient purkinje cells in the ngsk prnp(0/0) mouse. Dev. Neurobiol., 68, 332-348.
34. Helleberg, L. (1981) Clinical pharmacokinetics of indomethacin. Clin. Pharmacokinet., 6, 245-258.
35. Henery, C.C. & Mayhew, T.M. (1989) The cerebrum and cerebellum of the fixed human brain: efficient and unbiased estimates of volumes and cortical surface areas. J. Anat., 167, 167-180.
36. Hla, T. & Neilson, K. (1992) Human cyclooxygenase-2 cDNA. Proc. Natl. Acad. Sci. USA, 89, 7384-7388.
37. Katz, D.B. & Steinmetz, J.E. (2002) Psychological functions of the cerebellum. Behav. Cogn. Neurosci. Rev., 1, 229-241.
38. Kaufmann, W.E., Andreasson, K.I., Isakson, P.C. & Worley, P.F. (1997) Cyclooxygenases and the central nervous system. Prostaglandins, 54, 601-624.
39. Kaufmann, W.E., Worley, P.F., Pegg, J., Bremer, M. & Isakson, P. (1996) COX-2, a synaptically induced enzyme, is expressed by excitatory neurons at postsynaptic sites in rat cerebral cortex. Proc. Natl Acad. Sci. USA, 93, 2317-2321.
40. Kern, J.K. (2002) The possible role of the cerebellum in autism/PDD: disruption of a multisensory feedback loop. Med. Hypotheses, 59, 255-260.
41. Kimura-Kuroda, J., Nagata, I. & Kuroda, Y. (2007) Disrupting effects of hydroxy-polychlorinated biphenyl (PCB) congeners on neuronal development of cerebellar Purkinje cells: a possible causal factor for developmental brain disorders? Chemosphere, 67, S412-S420.
42. Konarski, J.Z., McIntyre, R.S., Grupp, L.A. & Kennedy, S.H. (2005) Is the cerebellum relevant in the circuitry of neuropsychiatric disorders? J. Psychiatry Neurosci., 30, 178-186.
43. Levitt, J.G., Blanton, R., Capetillo-Cunliffe, L., Guthrie, D., Toga, A. & McCracken, J.T. (1999) Cerebellar vermis lobules VIII-X in autism. Prog. Neuropsychopharmacol. Biol. Psychiatry, 23, 625-633.
44. Madeira, M.D., Azevedo, F.P. & Paula-Barbosa, M.M. (1988) Effects of long-term hypothyroidism in the morphology and synaptic organization of cerebellar ectopic granule cells. Histol. Histopathol., 3, 351-359.
45. Markowski, V.P., Cox, C. & Weiss, B. (1998) Prenatal cocaine exposure produces gender-specific motor effects in aged rats. Neurotoxicol. Teratol., 20, 43-53.
46. McCarthy, M.M., Schwarz, J.M., Wright, C.L. & Dean, S.L. (2008) Mechanisms mediating oestradiol modulation of the developing brain. J. Neuroendocrinol., 20, 777-783.
47. Meaney, M.J. & McEwen, B.S. (1986) Testosterone implants into the amygdala during the neonatal period masculinize the social play of juvenile female rats. Brain Res., 398, 324-328.
48. Mong, J.A., Glaser, E. & McCarthy, M.M. (1999) Gonadal steroids promote glial differentiation and alter neuronal morphology in the developing hypothalamus in a regionally specific manner. J. Neurosci., 19, 1464-1472.
49. Moulton, E.A., Schmahmann, J.D., Becerra, L. & Borsook, D. (2010) The Cerebellum and Pain: passive Integrator or Active Participator? Brain Res. Rev., 65, 14-27.
50. Nguon, K., Ladd, B., Baxter, M.G. & Sajdel-Sulkowska, E.M. (2005) Sexual dimorphism in cerebellar structure, function, and response to environmental perturbations. Prog. Brain Res., 148, 341-351.
51. Olesen, K.M., Jessen, H.M., Auger, C.J. & Auger, A.P. (2005) Dopaminergic activation of estrogen receptors in neonatal brain alters progestin receptor expression and juvenile social play behavior. Endocrinology, 146, 3705-3712.
52. Parsons, L.M., Bower, J.M., Gao, J.H., Xiong, J., Li, J. & Fox, P.T. (1997) Lateral cerebellar hemispheres actively support sensory acquisition and discrimination rather than motor control. Learn. Mem., 4, 49-62.
53. Pascuel, R., Ebner, D., Araneda, R., Urqueta, M. & Bustamante, C. (2010) Maternal stress induces long-lasting Purkinje cell developmental impairments in mouse offspring. Eur. J. Pediatr., 169, 1517-1522.
54. Pérez, S.E., Chen, E.Y. & Mufson, E.J. (2003) Distribution of estrogen receptor alpha and beta immunoreactive profiles in the postnatal rat brain. Brain Res. Dev. Brain Res., 145, 117-139.
55. Presti-Torres, J., de Lima, M.N., Scalco, F.S., Caldana, F., Garcia, V.A., Guimaraes, M.R., Schwartsmann, G., Roesler, R. & Schroder, N. (2007) Impairments of social behavior and memory after neonatalgastrin-releasing peptide receptor blockade in rats: implications for an animal model of neurodevelopmental disorders. Neuropharmacology, 52, 724-732.
56. Ren, K. (1999) An improved method for assessing mechanical allodynia in the rat. Physiol. Behav., 67, 711-716.
57. Rouzer, C.A. & Marnett, L.J. (2009) Cyclooxygenases: structural and functional insights. J. Lipid Res., 50(Suppl.), S29-S34.
58. Rudie, J.D., Shehzad, Z., Hernandez, L.M., Colich, N.L., Bookheimer, S.Y., Iacoboni, M. & Dapretto, M. (2011) Reduced functional integration and segregation of distributed neural systems underlying social and emotional information processing in autism spectrum disorders. Cereb. Cortex, [Epub ahead of print].
59. Sakamoto, H., Mezaki, Y., Shikimi, H., Ukena, K. & Tsutsui, K. (2003) Dendritic growth and spine formation in response to estrogen in the developing Purkinje cell. Endocrinology, 144, 4466-4477.
60. Shaw, K.N., Commins, S. & O'Mara, S.M. (2003) Deficits in spatial learning and synaptic plasticity induced by the rapid and competitive broad-spectrum cyclooxygenase inhibitor ibuprofen are reversed by increasing endogenous brain-derived neurotrophic factor. Eur. J. Neurosci., 17, 2438-2446.
61. Smith, S.B., Brown, C.B., Wright, M.E. & Yielding, K.L. (1987) Late-onset cerebellar degeneration in mice induced transplacentally by methylnitrosourea. Teratog. Carcinog. Mutagen., 7, 449-463.
62. Stoodley, C.J. & Schmahmann, J.D. (2009) The cerebellum and language: evidence from patients with cerebellar degeneration. Brain Lang., 110, 149-153.
63. Stoodley, C.J. & Schmahmann, J.D. (2010) Evidence for topographic organization in the cerebellum of motor control versus cognitive and affective processing. Cortex, 46, 831-844.
64. Strick, P.L., Dum, R.P. & Fiez, J.A. (2009) Cerebellum and nonmotor function. Annu. Rev. Neurosci., 32, 413-434.
65. Tai, T.C., Lye, S.J. & Adamson, S.L. (1998) Expression of prostaglandin E2 receptor subtypes in the developing sheep brainstem. Brain Res. Mol. Brain Res., 57, 161-166.
66. Tavano, A., Grasso, R., Gagliardi, C., Triulzi, F., Bresolin, N., Fabbro, F. & Borgatti, R. (2007) Disorders of cognitive and affective development in cerebellar malformations. Brain, 130, 2646-2660.
67. Todd, B.J., Schwarz, J.M. & McCarthy, M.M. (2005) Prostaglandin-E2: a point of divergence in estradiol-mediated sexual differentiation. Horm. Behav., 48, 512-521.
68. Wang, G. & Thompson, S.M. (2008) Maladaptive homeostatic plasticity in a rodent model of central pain syndrome: thalamic hyperexcitability after spinothalamic tract lesions. J. Neurosci., 28, 11959-11969.
69. Wills, S., Cabanlit, M., Bennett, J., Ashwood, P., Amaral, D.G. & Van de Water, J. (2009) Detection of autoantibodies to neural cells of the cerebellum in the plasma of subjects with autism spectrum disorders. Brain Behav. Immun., 23, 64-74.
70. Wright, C.L., Burks, S.R. & McCarthy, M.M. (2008) Identification of prostaglandin E2 receptors mediating perinatal masculinization of adult sex behavior and neuroanatomical correlates. Dev. Neurobiol., 68, 1406-1419.
71. Xu, J., Deng, X. & Disteche, C.M. (2008) Sex-specific expression of the X-linked histone demethylase gene Jarid1c in brain. PLoS ONE, 7, e2553.
72. Yamagata, K., Andreasson, K.I., Kaufmann, W.E., Barnes, C.A. & Worley, P.F. (1993) Expression of a mitogen-inducible cyclooxygenase in brain neurons: regulation by synaptic activity and glucocorticoids. Neuron, 11, 371-386.