2009, Number 2
<< Back Next >>
Arch Neurocien 2009; 14 (2)
Corticogénesis and neurodegeneration: Implications of the reelin pathway in alzheimer´s disease
Rojas JC
Language: Spanish
References: 71
Page: 132-141
PDF size: 188.52 Kb.
ABSTRACT
The reelin pathway regulates interactions between migrating neurons and radial glia. The activation of this pathway is fundamental during the process of normalcorticogénesis. The reelin pathway influences the cytoskeleton dynamics as well as the neural mechanisms of learning and memory and it may also play a critical role during neurodegenerative events. The reelin pathway may be disrupted by oxidative stress, excitotoxicity and other cellular anomalies caused by endogenous and exogenous factors. When disrupted, cytoskeleton components are inefficiently processedgiving place to the protein aggregates that characterize Alzheimer’s disease. Such aggregates have been associated with the activation of the apoptotic cascade. Neuritic plaques and neurofibrillary tangles are not innocuous byproducts of neurodegeneration, since their presence induces neuroinflammation, cell death and cognitive impairment. However, it is possible that the clinical picture of Alzheimer’s disease is perpetuated, but not initially caused by these protein aggregates. Elements of the Reelin pathway could represent targets of neuronal vulnerability mediating degenerative changes in the cortical pathways associated to Alzheimer’s disease. Characterization of the reelin pathway could improve the understanding of the interactions between the risk factors associated with Alzheimer’s disease and could facilitate the development of novel and effective neuroprotective interventions.
REFERENCES
Hatten ME. Central nervous system neuronal migration. Ann Rev Neurosci 1999; 22: 511-39.
del Rio JA, Martinez A, Fonseca M, Auladell C, Soriano E. Glutamate-like immunoreactivity and fate of Cajal-Retzius cells in the murine cortex as identified with calretinin antibody. Cereb Cortex 1995; 5: 13-21.
Aguilo A, Schwartz TH, Kumar VS, Peterlin ZA, Tsiola A, Soriano E, et al. Involvement of cajal-retzius neurons in spontaneous correlated activity of embryonic and postnatal layer 1 from wild-type and reeler mice. J Neurosci 1999; 19: 10856-68.
Radnikow G, Feldmeyer D, Lubke J. Axonal projection, input and output synapses, and synaptic physiology of Cajal Retzius cells in the developing rat neocortex. J Neurosci 2002; 22: 6908-19.
H Abraham, G Meyer. Reelin-expressing neurons in the postnatal and adult human hippocampal formation. Hippocampus 2003; 13: 715-27.
Marin-Padilla M. Cajal-Retzius cells and the development of the neocortex. Trends Neurosci 1998; 21: 64-71.
Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR. Neurons derived from radial glial cells establish radial units in neocortex. Nature 2001; 409: 714-20.
Wichterle H, Turnbull DH, Nery S, Fishell G, Alvarez-Buylla A. In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 2001;128: 3759-71.
Caviness VS. Neocortical histogenesis in normal and reeler mice: a developmental study based upon [3H] thymidine autoradiography. Brain Res 1982; 256: 293-302.
Caviness VS, Sidman RL. Retrohippocampal, hippocampal and related structures of the forebrain in the reeler mutant mouse. J Comp Neurol 1973; 147: 235-54.
Herrup K. Roles of cell lineage in the developing mammalian brain. Cur Top Dev Biol 1987; 21: 65-97.
Rice DS, Curran T. Role of the Reelin signaling pathway in central nervous system development. Annu Rev Neurosci 2001; 24: 1005–39.
Sweet HO, Bronson RT, Johnson KR, Cook SA, Davisson MT. Scrambler, a new neurological mutation of the mouse with abnormalities of neuronal migration. Mamm Genome 1996; 7: 798-802.
Trommsdorff M, Gotthardt M, Hiesberger T, Shelton J, Stockinger W, Nimpf J, et al. Reeler/Disabled-like disruption of neuronalmigration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 1999; 97: 689-701.
Chae T, Kwon YT, Bronson R, Dikkes P, Li E, Tsai LH. Mice lacking p35, a neuronal specific activator of Cdk5, display cortical lamination defects, seizures, and adult lethality. Neuron 1997;18:29-42.
Kuo G, Arnaud L, Kronstad-O’Brien P, Cooper JA. Absence of fyn and src causes a reeler-like phenotype. J Neurosci 2005; 25: 8578-86.
de Bergeyck V, Naerhuyzen B, Goffinet AM, Lambert de Rouvroit C.A panel of monoclonal antibodies against reelin, the extracellular matrix protein defective in reeler mutant mice. J Neurosci Methods 1998; 82: 17-24.
D’Arcangelo G, Miao GG, Chen SC, Soares HD, Morgan JI, Curran T.A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 1995; 374: 719-23.
Lugli G, Krueger JM, Davis JM, Persico AM, Keller F, Smalheiser NR. Methodological factors influencing measurement and processing of plasma reelin in humans. BMC Biochem 2003;4: 9.
Utsunomiya-Tate N, Kubo K, Tate S, Kainosho M, Katayama E, Nakajima K, et al. Reelin molecules assemble together to form a large protein complex, which is inhibited by the functionblocking CR-50 antibody. Proc Natl Acad Sci USA 2000; 97: 9729-34.
D’Arcangelo G, Homayouni R, Keshvara L, Rice DS, Sheldon M, Curran T. Reelin is a ligand for lipoprotein receptors. Neuron 1999; 24: 471-9.
Hiesberger T, Trommsdorff M, Howell BW, Goffinet A, Mumby MC, Cooper JA, et al. Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron 1999; 24: 481-9.
Dulabon L, Olson EC, Taglienti MG, Eisenhuth S, McGrath B, Walsh CA, et al. Reelin binds alpha 3 beta 1 integrin and inhibits neuronal migration. Neuron 2000; 27: 33-44.
Lambert de Rouvroit C, de Bergeyck V, Cortvrindt C, Bar I, Eeckhout Y, Goffinet AM. Reelin, the extracellular matrix protein deficient in reeler mutant mice, is processed by a metalloproteinase. Exp Neurol 1999; 156: 214-7.
Jossin Y, Ignatova N, Hiesberger T, Herz J, Lambert de Rouvroit C, Goffinet AM. The central fragment of Reelin, generated by proteolytic processing in vivo, is critical to its function during cortical plate development. J Neurosci 2004; 24: 514-21.
Morimura T, Hattori M, Ogawa M, Mikoshiba K. Disabled regulates the intracellular trafficking of reelin receptors. J Biol Chem 2005; 17: 16901-8.
Howell BW, Herrick TM, Hildebrand JD, Zhang YN, CooperJA. Dab1 tyrosine phosphorylation sites relay positional signalsduring mouse brain development. Curr Biol 2000; 10: 877-85.
Grove M, Demyanenko G, Echarri A, Zipfel PA, Quiroz ME, Rodriguiz RM, et al. AbIed-deficient mice exhibit defective cell migration, aberrant dendritic spine morphogenesis, and deficits in learning and memory. Mol Cell Biol 2004; 24: 10905-22.
Zukerberg LR, Patrick GN, Nikolic M, Humbert S, Wu CL, Lanier LM, et al. Cables links Cdk5 and c-Abl and facilitates Cdk5 tyrosine phosphorylation, kinase upregulation, and neurite outgrowth. Neuron 2000; 26: 633-46.
Nikolic M, Chou MM, Lu W, Mayer BJ, Tsai LH. The p35/Cdk5 kinase is a neuron-specific Rac effector that inhibits Pak1 activity. Nature 1998; 395: 194-8.
Assadi AH, Zhang G, Beffert U, McNeil RS, Renfro AL, Niu S, et al. Interaction of reelin signaling and Lis1 in brain development. Nat Genet 2003; 35: 270-6.
Li BS, Zhang L, Gu JG, Amin ND, Pant HC. Integrin alpha(1) beta(1)-mediated activation of cyclin-dependent kinase 5 activityis involved in neurite outgrowth and human neurofilament protein H Lys-Ser-Pro tail domain phosphorylation. J Neurosci 2000; 20: 6055-62.
Alcantara S, Ruiz M, D’Arcangelo G, Ezan F, de Lecea L, Curran T, et al. Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J Neurosci 1998; 18: 7779-99.
Forster E, Tielsch A, Saum B, Weiss KH, Johanssen C, Graus- Porta D, et al. Reelin, Disabled 1, and beta 1 integrins are required for the formation of the radial glial scaffold in the hippocampus. Proc Natl Acad Sci USA 2002; 99:13178-83.
Hartfuss E, Forster E, Bock HH, Hack MA, Leprince P, Luque JM, et al. Reelin signaling directly affects radial glia morphology and biochemical maturation. Development 2003;130:4597-09. 36. Soriano E, del Rio JA. The cells of Cajal-Retzius: Still a mystery one century after. 2005 Neuron 2005; 46: 389-94.
Chedotal A, Del Rio JA, Ruiz M, He Z, Borrell V, de Castro F, et al. Semaphorins III and IV repel hippocampal axons via two distinct receptors. Development 1998; 125: 4313-23.
Celio MR, Blumcke I. Perineuronal nets–a specialized form of extracellular matrix in the adult nervous system. Brain Res Rev 1994;19:128-45.
Pappas GD, Kriho V, Pesold C. Reelin in the extracellular matrix and dendritic spines of the cortex and hippocampus: a comparison between wild type and heterozygous reeler mice by immunoelectron microscopy. J Neurocytol 2001;30:413-25.
Martinez-Cerdeno V, Galazo MJ, Cavada C, Clasca F. Reelin immunoreactivity in the adult primate brain: intracellular localization in projecting and local circuit neurons of the cerebral cortex, hippocampus and subcortical regions. Cereb Cortex 2002;12:1298-311.
Impagnatiello F, Guidotti AR, Pesold C, Dwivedi Y, Caruncho H, Pisu MG, et al. A decrease of reelin expression as a putative vulnerability factor in schizophrenia. Proc Natl Acad Sci USA 1998; 95: 15718-23.
Fatemi SH, Earle JA, McMenomy T. Reduction in Reelin immunoreactivity in hippocampus of subjects with schizophrenia, bipolar disorder and major depression. Mol Psychiatry 2000;5:654-63.
Weeber EJ, Beffert U, Jones C, Christian JM, Forster E, Sweatt JD, et al. Reelin and ApoE receptors cooperate to enhance hippocampal synaptic plasticity and learning. J Biol Chem 2002; 277: 39944-52.
Niu S, Renfro A, Quattrocchi CC, Sheldon M, D’Arcangelo G. Reelin promotes hippocampal dendrite development through the VLDLR/ApoER2-Dab1 pathway. Neuron 2004; 41:71-84.
Lacor PN, Grayson DR, Auta J, Sugaya I, Costa E, Guidotti A. Reelin secretion from glutamatergic neurons in culture is independent from neurotransmitter regulation. Proc Natl Acad Sci USA. 2000; 97: 3556-61.
Qiu S, Korwek KM, Pratt-Davis AR, Peters M, Bergman MY, Weeber EJ. Cognitive disruption and altered hippocampus synaptic function in Reelin haploinsufficient mice. Neurobiol Learn Mem 2006; 85: 228-42.
Cummings JL, Vinters HV, Cole GM, Khachaturian ZS. Alzheimer’s disease: etiologies, pathophysiology, cognitive reserve, and treatment opportunities. Neurology 1998;5:S2-S17.
48.Wirths O, Multhaup G, Czech C, Blanchard V, Tremp G, Pradier L, et al. Reelin in plaques of beta-amyloid precursor protein and presenilin-1 double-transgenic mice. Neurosci Lett 2001; 316: 145-8.
Lovell MA, Robertson JD, Teesdale WJ, Campbell JL, Markesbery WR. Copper, iron and zinc in Alzheimer’s disease senile plaques. J Neurol Sci 1998; 158: 47-52.
Dickson DW. The pathogenesis of senile plaques. J Neuropathol Exp Neurol 1997; 56: 321-39.
Oddo S, Caccamo A, Kitazawa M, Tseng BP, LaFerla FM. Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer’s disease. Neurobiol Aging 2003; 24:1063-70.
Knopman DS, Parisi JE, Salviati A, Floriach-Robert M, Boeve BF, Ivnik RJ, et al. Neuropathology of cognitively normal elderly. J Neuropathol Exp Neurol 2003; 62:1087-95.
Rosenberg NG. The molecular and genetic basis of AD: The end of the beginning. Neurology 2000; 54: 2045-54.
Nagy Z, Esiri MM, Jobst KA, Morris JH, King EM, McDonald B, et al. Relative roles of plaques and tangles in the dementia of Alzheimer’s disease: correlations using three sets of neuropathological criteria. Dementia 1995; 6: 21-31.
Gomez-Isla T, Hollister R, West H, Mui S, Growdon JH, Petersen RC, et al. Neuronal loss correlates with but exceeds neurofibrillary tangles in Alzheimer’s disease. Ann Neurol 1997; 41: 17-24.
Santacruz K, Lewis J, Spires T, Paulson J, Kotilinek L, Ingelsson M, et al. Tau suppression in a neurodegenerative mouse model improves memory function. Science 2005; 309: 476-81.
Saez-Valero J, Costell M, Sjogren M, Andreasen N, Blennow K, Luque JM. Altered levels of cerebrospinal fluid reelin in frontotemporal dementia and Alzheimer’s disease. J Neurosci Res 2003; 72: 132-6.
Helbecque N, Berr C, Cottel D, Fromentin-David I, Sazdovitch V, Ricolfi F, et al. VLDL receptor polymorphism, cognitive impairment, and dementia. Neurology 2001; 56: 1183-8.
Corder EH, Saunders AM, Strittmatter WJ, Schmechel DE, Gaskell PC, Small GW, et al. Genetic dose of apolipoprotein E type 4 allele and the risk of Alzheimer’s disease in late onset families. Science 1993; 261: 921-3.
Patrick GN, Zukerberg L, Nikolic M, de la Monte S, Dikkes P, Tsai LH. Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature 1999; 402: 615-22.
Alvarez AR, Sandoval PC, Leal NR, Castro PU, Kosik KS. Activation of the neuronal c-Abl tyrosine kinase by amyloidbeta- peptide and reactive oxygen species. Neurobiol Dis 2004; 17: 326-36.
Goldschmidt-Clermont PJ, Moldovan L. Stress, superoxide, and signal transduction. Gene Expr 1999; 7: 255-60.
Minden A, Lin A, Claret FX, Abo A, Karin M. Selective activation of the JNK signaling cascade and c-Jun transcriptional activity by the small GTPases Rac and Cdc42Hs. Cell 1995;81:1147-57.
Trommsdorff M, Borg JP, Margolis B, Herz J. Interaction of cytosolic adaptor proteinswith neuronal apolipoprotein E receptorsand the amyloid precursor protein. J Biol Chem 1998; 273: 33556-60.
Pappolla MA, Omar RA, Kim KS, Robakis NK. Immunohistochemical evidence of oxidative stress in Alzheimer’s disease. Am J Pathol 1992;140:621-8.
Bush AI. The metallobiology of Alzheimer’s disease. Trends Neurosci 2003; 26: 207-14.
Yao D, Gu Z, Nakamura T, Shi ZQ, Ma Y, Gaston B, et al. Nitrosative stress linked to sporadic Parkinson’s disease: Snitrosylation ofparkin regulates its E3 ubiquitin ligase activity. Proc Natl Acad Sci USA. 2004; 101: 10810-4.
Forman MS, Lee VM, Trojanowski JQ. ‘Unfolding’ pathways in neurodegenerative disease. Trends Neurosci 2003;26:407-10.
Sattler R, Tymiansky M. Molecular mechanisms of calciumdependent excitotoxicity. J Mol Med 2000; 78: 3-13.
Chen Y, Beffert U, Ertunc M, Tang TS, Kavalali ET, Bezprozvanny I, et al. Reelin modulates NMDA receptor activity in cortical neurons. J Neurosci 2005; 25: 8209-16.
Braak E, Braak H, Mandelkow EM. A sequence of cytoskeleton changes related to the formation of neurofibrillary tangles and neuropil threads. Acta Neuropathol 1994; 87: 554-67.
Koliatsos VE, Dawson TM, Kecojevic A, Zhou Y, Wang YF, Huang KX. Cortical interneurons become activated by deafferentation and instruct the apoptosis of pyramidal neurons. Proc Natl Acad Sci USA 2004;101:14264-9.