Homocysteine activates calcium-mediated cell signaling mechanisms targeting the cytoskeleton in rat hippocampus

International Journal of Developmental Neuroscience

Volumn 26, Issue 5, 2008, Pages 447-455

  Loureiro, Samanta Oliveira ^a   Heimfarth, Luana ^a   Pelaez, Priscila de Lima ^a   Vanzin, Camila Simioni ^a   Viana, Lilian ^a   Wyse, Angela T S ^a   Pessoa Pureur, Regina ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

Cell signaling; Hippocampus; Homocysteine; Intermediate filaments; Phosphorylation

Indexed keywords

CYCLIC AMP; HOMOCYSTEINE; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C; PROTEIN KINASE (CALCIUM,CALMODULIN) II; PROTEIN KINASE C;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; CYTOSKELETON; ELECTRIC POTENTIAL; EXTRACELLULAR CALCIUM; HIPPOCAMPUS; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; BENZYLAMINES; CALCIUM; CALCIUM SIGNALING; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CYCLIC AMP; CYTOSKELETON; FLAVONOIDS; HIPPOCAMPUS; HOMOCYSTEINE; INOSITOL PHOSPHATES; INTERMEDIATE FILAMENTS; MITOGEN-ACTIVATED PROTEIN KINASES; MODELS, BIOLOGICAL; PHOSPHORYLATION; PROTEIN KINASE C; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SIGNAL TRANSDUCTION; STAUROSPORINE; SULFONAMIDES; TYPE C PHOSPHOLIPASES;

ANIMALIA; RATTUS;

EID: 43049181759     PISSN: 07365748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2008.03.001     Document Type: Article

References (92)

1. Ackerley S., Grierson A.J., Brownlees J., Thornhiel P., Anderton B.H., Leight P.N., Shew C.E., and Mielerc C.J. Glutamate slow axonal transport of neurofilaments in transfected neurons. Journal of Cell Biology 150 (2000) 165-175
2. Akama K.T., and McEwen B.S. Estrogen stimulates postsynaptic density-95 rapid protein synthesis via the Akt/protein kinase B pathway. Journal of Neuroscience 23 (2003) 2333-2339
3. Alberts B., Johnson A., Lewis J., Raff M., Roberts K., and Walter P. Molecular biology of the cell. In: Alberts B., Johnson A., Lewis J., Raff M., Roberts K., and Walter P. (Eds). The Cytoskeleton. 4th ed. (2002), Garland Science, New York 907-982
4. Allain P., Le Bouil A., Cordillet E., Le Quay L., Bagheri H., and Montastruc J.L. Sulfate and cysteine levels in the plasma of patients with Parkinson's disease. Neurotoxicology 16 (1995) 527-529
5. Atwal J.K., Massie B., Miller F.D., and Kaplan D.R. The TrkB-Shc site signals neuronal survival and local axon growth via MEK and P13-kinase. Neuron 27 (2000) 265-277
6. Atwal J.K., Singh K.K., Tessier-Lavigne M., Miller F.D., and Kaplan D.R. Semaphorin 3F antagonizes neurotrophin-induced phosphatidylinositol 3-kinase and mitogen-activated protein kinase kinase signaling: a mechanism for growth cone collapse. Journal of Neuroscience 23 (2003) 7602-7609
7. Baba A., Lee E., Tatsuno T., and Iwata H. Cysteine sulfinic acid in the central nervous system: antagonistic effect of taurine on cysteine sulfinic acid-stimulated formation of cyclic AMP in guinea pig hippocampal slices. Journal of Neurochemistry 38 (1982) 1280-1285
8. Baydas G., Reiter R.J., Akbulut M., Tuzcu M., and Tamer S. Melatonin inhibits neural apoptosis induced by homocysteine in hippocampus of rats via inhibition of cytochrome c translocation and caspase-3 activation and by regulating pro- and anti-apoptotic protein levels. Neuroscience 135 (2005) 879-886
9. Bleich S., Bandelow B., Javaheripour K., Muller A., Degner D., Wilhelm J., Havemann-Reinecke U., Sperling W., Ruther E., and Kornhuber J. Hyperhomocysteinemia as a new risk factor for brain shrinkage in patients with alcoholism. Neuroscience Letters 335 (2003) 179-182
10. Bleich S., Degner D., Bandelow B., Von Ahsen N., Ruther E., and Kornhuber J. Plasma homocysteine is a predictor of alcohol withdrawal seizures. Neuroreport 11 (2000) 2749-2752
11. Brunet A., Datta S.R., and Greenberg M.E. Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway. Current Opinion in Neurobiology 11 (2001) 297-305
12. Cattaneo M. Hyperhomocysteinemia, atherosclerosis and thrombosis. Thrombosis and Haemostasis 81 (1999) 165-176
13. Cattaneo M. Homocysteine and the risk of intrauterine growth retardation. Clinical Chemistry 49 (2003) 1432-1433
14. Cattaneo M. Hyperhomocysteinemia and venous thromboembolism. Seminars in Thrombosis and Hemostasis 32 (2006) 716-723
15. Coulombe P.A., and Wong P. Cytoplasmic intermediate filaments revealed as dynamic and multipurpose scaffolds. Nature Cell Biology 6 (2004) 699-706
16. Dardik R., Savion N., Gal N., and Varon D. Flow conditions modulate homocysteine induced changes in the gene expression of endothelial cell genes associated with cell-cell interaction and cytoskeletal rearrangement. Thrombosis and Haemostasis 88 (2002) 1047-1053
17. v during aging. Proceedings of the National Academy of Sciences of the United States of America 100 (2003) 16018-16023
18. 2+/calmodulin-dependent protein kinase participate in phosphorylation of neurofilaments induced by protein kinase C. Journal of Neuroscience Research 50 (1997) 514-521
19. Eng L.F., Ghirnikar R.S., and Lee Y.L. Glial fibrillary acidic protein: GFAP-thirty-one years (1969-2000). Neurochemical Research 25 (2000) 1439-1451
20. Funchal C., de Almeida L.M.V., Oliveira Loureiro S., Vivian L., Pelaez P.L., Pessutto F.D.B., Rosa A.M., Wajner M., and Pessoa-Pureur R. In vitro phosphorylation of cytoskeletal proteins from cerebral cortex of rats. Brain Research Protocols 11 (2003) 111-118
21. 2+ mediates the effect of alpha- ketoisocaproic acid on the phosphorylating system of cytoskeletal proteins from cerebral cortex of immature rats. Journal of the Neurological Sciences 238 (2005) 75-82
22. 2+ and cAMP. Neurochemical Research 30 (2005) 1139-1146
23. Gescher A. Analogs of staurosporine: potential anticancer drugs?. General Pharmacology 5 (1998) 721-728
24. Gotow T., Tanaka T., Nakamura Y., and Takeda M. Dephosphorylation of the largest neurofilament subunit protein influences the structure of crossbridges in reassembled neurofilaments. Journal of Cell Sciences 107 (1994) 1949-1957
25. Grant P., and Pant H.C. Nerofilament protein synthesis and phosphorylation. Journal of Neurocytology 29 (2000) 843-872
26. Grieco A.J. Homocystinuria: pathogenetic mechanisms. The American Journal of The Medical Sciences 273 (1977) 120-132
27. Guidato S., Tsai L.H., Woodgett J., and Miller C.C. Differential cellular phosphorylation of neurofilament heavy side arms by glycogen synthase kinase-3 and cyclin-dependent kinase-5. Journal of Neurochemistry 66 (1996) 1698-1706
28. Hashimoto R., Nakamura Y., Goto H., Wada Y., Sakoda S., and Kaibuchi K. Domain- and site-specific phosphorylation of bovine NF-L by Rho-associated kinase. Biochemistry and Biophysics Research Communication 245 (1998) 407-411
29. Hisanaga S., Yasugawa S., Yamakawa T., Miyamoto E., Ikebe M., Uchiyama M., and Kishimoto T. Dephosphorylation of microtubule-binding sites at the neurofilament-H tail domain by alkaline, acid, and protein phosphatases. Journal of Biochemistry 113 (1993) 705-709
30. Ho P.I., Ashline D., Dhitavat S., Ortiz D., Collins S.C., Shea T.B., and Rogers E. Folate deprivation induces neurodegeneration: roles of oxidative stress and increased homocysteine. Neurobiology of Disease 14 (2003) 32-42
31. Ho P.I., Ortiz D., Rogers E., and Shea T.B. Multiple aspects of homocysteine neurotoxicity: glutamate excitotoxicity, kinase hyperactivation and DNA damage. Journal of Neuroscience Research 70 (2002) 694-702
32. Hron G., Lombardi R., Eichinger S., Lecchi A., Kyrle P.A., and Cattaneo M. Low vitamin B6 levels and the risk of recurrent venous thromboembolism. Haematologica 92 (2007) 1250-1253
33. Hsieh S.T., Kidd G.J., Crawforg T.O., Xu Z., Lin W.M., and Trapp B.D. Regional modulation of neurofilament organization by myelination in normal axons. The Journal of Neuroscience 14 (1994) 6392-6401
34. 45Ca uptake by cortical slices of rat brain: stimulatory effect of l-glutamic acid. Brain Research 248 (1982) 305-311
35. Inagaki M., Gonda Y., Nishizawa K., Kitamura S., and Sato C. Phosphorylation sites linked to glial filament disassembly in vitro located in a non-alpha-helical head domain. Journal of Biological Chemistry 265 (1990) 4722-4729
36. Izawa I., and Inagaki M. Regulatory mechanisms and functions of intermediate filaments: a study using site- and phosphorylation state-specific antybodies. Cancer Science 97 (2006) 167-174
37. Jaworski J., Spangler S., Seeburg D.P., Hoogenraad C.C., and Sheng M. Control of dendritic arborization by the phosphoinositide-3′-kinase-Akt-mammalian target of rapamycin pathway. The Journal of Neuroscience 25 (2005) 11300-11312
38. Kim J.H., Cho S.Y., Lee J.H., Jeong S.M., Yoon I.S., Lee B.H., Lee J.H., Pyo M.K., Lee S.M., Chung J.M., Kim S., Rhim H., Oh J.W., and Nah S.Y. Neuroprotective effects of ginsenoside Rg3 against homocysteine-induced excitoxicity in rat hippocampus. Brain Research 1136 (2007) 190-199
39. Kolch W., Heidecker G., Kochs G., Hummel R., Vahidi H., Mischak H., Finkenzeller G., Marme D., and Rapp U.R. Protein kinase C alpha activates RAF-1 by direct phosphorylation. Nature 364 (1993) 249-252
40. Kruman I.I., Culmsee S.L., Chan Y., Kruman Z., Guo L., Penix M.P., and Mattson M.P. Homocysteine elicits a DNA damage response in neurons that promotes apoptosis and hypersensitivity to excitotoxicity. The Journal of Neuroscience 20 (2000) 6920-6926
41. Kuruvilla R., Ye H., and Ginty D.D. Spatially and functionally distinct roles of the PI3-K effector pathway during NGF signaling in sympathetic neurons. Neuron 27 (2000) 499-512
42. 4. Nature 277 (1970) 680-685
43. Langmeier M., Folbergrova J., Haugvicova R., Pokorny J., and Mares P. Neuronal cell death in hippocampus induced by homocysteic acid in immature rats. Epilepsia 44 (2003) 299-304
44. Leterrier J.F., Kas J., Hartwig J., Vegners R., and Janmey P.A. Mechanical effects of neurofilament cross-bridges. Modulation by phosphorylation, lipids, and interactions with F-actin. Journal of Biological Chemistry 271 (1996) 15687-15694
45. Levine J., Stahl Z., Sela B.A., Gavendo S., Ruderman V., and Belmaker R.H. Elevated homocysteine levels in young male patients with schizophrenia. The American Journal of Psychiatry 159 (2002) 1790-1792
46. Lhuillier L., and Dryer S.E. Developmental regulation of neuronal K(Ca) channels by TGFbeta1: an essential role for PI3 kinase signaling and membrane insertion. Journal of Neurophysiology 88 (2002) 954-964
47. Lipton S.A., Kim W.K., Choi Y.B., Kumar S., D'Emilia D.M., Rayudu P.V., Arnelle D.R., and Stamler J.S. Neurotoxicity associated with dual actions of homocysteine at the N-methyl-d-aspartate receptor. Proceedings of the National Academy of Sciences of the United States of the America 94 (1997) 5923-5928
48. Lowry O.H., Rosebrough N.J., Farr A.L., and Randall R.J. Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193 (1951) 265-267
49. Maler J.M., Seifert W., Hüther G., Wiltfang J., Rüther E., Kornhuber J., and Bleich S. Homocysteine induces cell death of rat astrocytes in vitro. Neuroscience Letters 347 (2003) 85-88
50. Man H.Y., Wang Q., Lu W.Y., Ju W., Ahmadian G., Liu L., D'Souza S., Wong T.P., Taghibiglou C., Lu J., Becker L.E., Pei L., Liu F., Wymann M.P., MacDonald J.F., and Wang Y.T. Activation of PI3-kinase is required for AMPA receptor insertion during LTP of mEPSCs in cultured hippocampal neurons. Neuron 38 (2003) 611-624
51. Marais R., Light Y., Mason C., Paterson H., Olson M.F., and Marshall C.J. Requirement of Ras-GTP-Raf complexes for activation of Raf-1 by protein kinase C. Science 280 (1998) 109-112 Erratum in: Science 1998 280; 987
52. Markus A., Zhong J., and Snider W.D. Raf and akt mediate distinct aspects of sensory axon growth. Neuron 35 (2002) 65-76
53. +-ATPase activity in parietal, prefrontal and cingulate cortex of young rats. International Journal of Developmental Neuroscience 22 (2004) 185-190
54. Miller J.W. Homocysteine and Alzheimer's disease. Nutrition Reviews 57 (1999) 126-129
55. Mudd S.H., Levy H.L., and Skovby F. Disorders of transulfuration. In: Scriver C.R., Beaudet A.L., Sly W.S., and Valled D. (Eds). The Metabolic Basis of Inherited Disease (2001), McGraw-Hill, New York 1279-1327
56. Mudd S.H., Skovby F., Levy H.L., Pettigrew K.D., Wilcken B., and Pyeritz R.E. The natural history of homocystinuria due to cystathionine beta-synthase deficiency. The American Journal of Human Genetics 37 (1985) 1-31
57. Nestler E.J., and Duman R.S. G proteins. In: Siegel G.J., Albers R.W., Brady S.T., and Price D.L. (Eds). Basic Neurochemistry - Molecular, Cellular, and Medical Aspects. 7th ed. (2006), Elsevier Academic Press, Canada
58. Niikura Y., Abe K., and Misawa M. Involvement of L-type Ca (2+) channels in the induction of long-term potentiation in the basolateral amygdala-dentate gyrus pathway of anesthetized rats. Brain Research 1017 (2004) 218-221
59. Nixon R.A., and Sihag R.K. Neurofilament phosphorylation: a new look at regulation and function. Trends in Neuroscience 14 (1991) 501-506
60. Obeid R., and Herrmann W. Mechanisms of homocysteine neurotoxicity in neurodegenerative diseases withspecial reference to dementia. FEBS Letters 580 (2006) 2994-3005
61. Oliveira-Loureiro S., de Lima Pelaez P., Heimfarth L., Souza D.O., Wajner M., and Pessoa-Pureur R. Propionic and methylmalonic acids increase cAMP levels in slices of cerebral cortex of young rats via adrenergic and glutamatergic mechanisms. Biochimica et Biophysica Acta - Molecular Basis of Disease 1740 (2005) 460-466
62. Ozawa S., Kamyia H., and Tsuzuki K. Glutamate receptors in the mammalian central nervous system. Progress in Neurobiology 54 (1998) 581-618
63. Peuchen S., Clark J.B., and Duchen M.R. Mechanisms of intracellular calcium regulation in adult astrocytes. Neuroscience 71 (1996) 871-883
64. Putney Jr. J.W. Calcium. In: Siegel G., Agranoff B.W., Alberts R.W., Fisher S.K., and Ulher M.D. (Eds). Basic Neurochemistry - Molecular, Cellular and Medical Aspects (1999), Lippincott-Raven Publishers, New York 453-469
65. Rice D., and Barone Jr. S. Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environmental Health Perspectives 108 (2000) 511-533
66. Roberson E.D., English J.D., Adams J.P., Selcher J.C., Kondratick C., and Sweatt J.D. The mitogen-activated protein kinase cascade couples PKA and PKC to cAMP response element binding protein phosphorylation in area CA1 of hippocampus. The Journal of Neuroscience 19 (1999) 4337-4348
67. Robert K., Pages C., Ledru A., Delabar J., Caboche J., and Janel N. Regulation of extracellular signal-regulated kinase by homocysteine in hippocampus. Neuroscience 133 (2005) 925-935
68. Robert K., Santiard-Baron D., Chassé J.F., Paly E., Aupetit J., Kamoun P., London J., and Janel N. The neuronal SAPK/JNK pathway is altered in a murine model of hyperhomocysteinemia. Journal of Neurochemistry 89 (2004) 33-43
69. Rodnight R., Gonçalves C.A., Wofchuk S.T., and Leal R. Control of the phosphorylation of the astrocyte marker glial fibrillary acidic protein (GFAP) in the immature rat hippocampus by glutamate and calcium ions: possible key factor in astrocytic plasticity. Brazilian Journal of Medical and Biological Research 30 (1997) 325-338
70. Sachdev P.S., Valenzuela M., Wang X.L., Looi J.C., and Brodaty H. Relationship between plasma homocysteine levels and brain atrophy in healthy elderly individuals. Neurology 58 (2002) 1539-1541
71. Sanna P.P., Cammalleri M., Berton F., Simpson C., Lutjens R., Bloom F.E., and Francesconi W. Phosphatidylinositol 3-kinase is required for the expression but not for the induction or the maintenance of long-term potentiation in the hippocampal CA1 region. The Journal of Neuroscience 22 (2002) 3359-3365
72. Schwarz S., and Zhou G.Z. N-Methyl-d-aspartate receptors and CNS symptoms of homocystinuria. The Lancet 337 (1991) 1226-1227
73. Scott J.M., and Weir D.G. Folic acid, homocysteine, and one-carbon metabolism: a review of the essential biochemistry. Journal of Cardiovascular Risk 5 (1998) 223-227
74. Seshadri S., Beiser A., Selhub J., Jacques P.F., Rosenberg I.H., D'Agostino R.B., Wilson P.W., and Wolf P.A. Plasma homocysteine as a risk factor for dementia and Alzheimer's disease. The New England Journal of Medicine 346 (2002) 476-483
75. Shetty K.T., Kink W.T., and Pant H.C. Cdc-like kinase from rat spinal cord specifically phosphorylates KSPXK motifs in neurofilament proteins: isolation and characterization. Proceedings of the National Academy of Science of the United States of America 90 (1993) 6844-6848
76. Sihag R.K., and Nixon R.A. Phosphorylation of the amino terminal head domain of the middle molecular mass 145 kDa subunit of neurofilaments. Journal of Biological Chemistry 265 (1990) 4166-4171
77. Sontag E., Nunbhakdi-Craig V., Sontag J.M., Diaz-Arrastia R., Dayal S., Lentz S.R., Arning E., and Bottiglieri T. Protein phosphatase 2A methyltransferase links homocysteine metabolism with tau and amyloid precursor protein regulation. The Journal of Neuroscience 27 (2007) 2751-2759
78. Streck E.L., Bavaresco C.S., Netto C.A., and Wyse A.T.S. Chronic hyperhomocysteinemia provokes memory deficit in rats in the Morris water maze. Behaviour Brain Research 153 (2004) 377-381
79. Streck E.L., Vieira P.S., Wannmacher C.M., Dutra-Filho C.S., Wajner M., and Wyse A.T. In vitro effect of homocysteine on some parameters of oxidative stress in rat hippocampus. Metabolic Brain Disease 2 (2003) 147-154
80. +-ATPase activity by the metabolites accumulating in homocystinuria. Metabolic Brain Disease 17 (2002) 83-91
81. 2+-dependent cell signaling through calmodulin-activated protein phosphatase and protein kinases minireview series. Journal of Biological Chemistry 276 (2001) 2311-2312
82. Sun D., Leung C.L., and Liem R.K.H. Phosphorylation of the high molecular weight neurofilament protein (NF-H) by Cdk5 and p35. Journal of Biological Chemistry 271 (1996) 14245-14251
83. Tasca C.I., Vendite D., Garcia K.L., and Souza D.O. Effects of adenosine on cAMP production during early development in the optic tectum of chicks. International Journal of Developmental Neuroscience 13 (1995) 545-553
84. 2+/calmodulin-dependent protein kinase II. Journal of Biological Chemistry. 265 (1990) 5315-5320
85. Tovey K.C., Oldham K.G., and Whelan J.A.M. A simple direct assay for cyclic AMP in plasma and other biological samples using an improved competitive protein binding technique. Clinica Chimica Acta 56 (1974) 221-234
86. Van den Berg M., Van der Knapp M.S., Boers G.H., Stehouwer C.D., Rauwerda J.A., and Valk J. Hyperhomocysteinaemia; with reference to its neuroradiological aspects. Neuroradiology 37 (1995) 403-411
87. Vieira de Almeida L.M.V., Funchal C., Pelaez P.L., Pessutto F.D.B., Loureiro S.O., Vivian L., Wajner M., and Pessoa-Pureur R. Effect of propionic and methylmalonic acids on the in vitro phosphorylation of intermediate filamentns from cerebral cortex of rats during development. Metabolic Brain Disease 18 (2003) 207-219
88. Yabe J.T., Jung C., Chan W.K., and Shea T.B. Phospho-dependent association of neurofilament proteins with kinesin in situ. Cell Motility and the Cytoskeleton 45 (2000) 249-262
89. Yudkoff M. Diseases of amino acid metabolism. In: Siegel G.J. (Ed). Basic Neurochemistry: Molecular, Cellular and Medical Aspects. 6th ed. (1999), Williams & Northgate, Philadelphia 887-915
90. Wang Q.J. PKD at the crossroads of DAG and PKC signaling. Trends in Pharmacological Sciences 27 (2006) 317-323
91. Wang Q., Liu L., Pei L., Ju W., Ahmadian G., Lu J., Wang Y., Liu F., and Wang Y.T. Control of synaptic strength, a novel function of Akt. Neuron 38 (2003) 915-928
92. Zieminska E., and Lazarewicz J. Excitotoxic neuronal injury in chronic homocysteine neurotoxicity studied in vitro: the role of NMDA and group I metabotropic glutamate receptors. Acta Neurobiologiae Experimentalis (Warsz) 66 (2006) 301-309