Periapical Disease and the Prefrontal Cortex. Is there a Relationship between Calcium-Binding Protein and Neurodegenerative Diseases?
DOI:
https://doi.org/10.21270/archi.v11i1.5350Palavras-chave:
Calcium-Binding Proteins, Inflammation, Neurodegenerative Diseases, Periodontal Diseases, Pre-Frontal CortexResumo
Apical periodontitis (AP) or periapical lesion (PL) is an inflammatory disease that causes pain, loss of bone and destruction of other tissues of teeth support. This condition could be caused by caries, dental trauma and/or periapical microleakage wich is regulated by the immune system or inflammatory response. Several analyses have shown that endodontic infection can cause systemic alterations like stroke, insulin resistance, cardiovascular diseases and to contribute to the appearance of neurodegenerative disorders. The prefrontal cortex (PfC), positioned in the most anterior region of the brain, is essentially involved behavioral abilities, intellectual roles, cognition, learning and other functions. Neurons with laminar distribution in the PfC, especially in the lower layers express several types of calcium-binding proteins (CaBPs) like parvalbumin, calbindin and calretinin that are involved in calcium buffering into the brain (CNS). These proteins are co-localized with GABAergic neurons, main inhibitory cells into the brain. Piece of evidence has pointed out a relationship between apical periodontitis and neurodegenerative diseases where microorganisms and/or toxins produced in the teeth infection can penetrate the bloodstream, infiltrate the blood-brain barrier limit and active astrocytes and microglial cells in the central nervous system (CNS) and increase the releasing of pro-inflammatory cytokines promoting pyramidal and non-pyramidal neuronal degeneration. Thus, is there a relationship among apical periodontitis, oral hygiene and prefrontal cortex and neurodegenerative disorders?
Downloads
Referências
Cintra LTA, Estrela C, Azuma MM, Queiroz IOA, Kawai T, Gomes-Filho JE. Endodontic medicine: interrelationships among apical periodontitis, systemic disorders, and tissue responses of dental materials. Braz Oral Res 2018;32(suppl 1):e68.
Gazivoda D, Dzopalic T, Bozic B, Tatomirovic Z, Brkic Z, Colic M. Production of proinflammatory and immunoregulatory cytokines by inflammatory cells from periapical lesions in culture. Journal of oral pathology & medicine : official publication of the International Association of Oral Pathologists and the American Academy of Oral Pathology 2009;38(7).
Sasaki H, Hirai K, Martins CM, Furusho H, Battaglino R, Hashimoto K. Interrelationship between Periapical Lesion and Systemic Metabolic Disorders. Curr Pharm Des 2016;22(15):2204-15.
Stashenko P, Teles R, D'Souza R. Periapical inflammatory responses and their modulation. Critical reviews in oral biology and medicine : an official publication of the American Association of Oral Biologists 1998;9(4).
Schulze A, Schönauer M, Busse M. Sudden improvement of insulin sensitivity related to an endodontic treatment. Journal of periodontology 2007;78(12).
Caplan DJ, Chasen JB, Krall EA, Cai J, Kang S, Garcia RI, et al. Lesions of endodontic origin and risk of coronary heart disease. J Dent Res 2006;85(11):996-1000.
Pasqualini D, Bergandi L, Palumbo L, Borraccino A, Dambra V, Alovisi M, et al. Association among oral health, apical periodontitis, CD14 polymorphisms, and coronary heart disease in middle-aged adults. J Endod 2012;38(12):1570-7.
Costa TH, de Figueiredo Neto JA, de Oliveira AE, Lopes e Maia Mde F, de Almeida AL. Association between chronic apical periodontitis and coronary artery disease. J Endod 2014;40(2):164-7.
Martins CM, Sasaki H, Hirai K, Andrada AC, Gomes-Filho JE. Relationship between hypertension and periapical lesion: an in vitro and in vivo study. Braz Oral Res 2016;30(1):e78.
Rashmi N, Galhotra V, Goel P, Rajguru JP, Jha SK, Kulkarni K. Assessment of C-reactive Proteins, Cytokines, and Plasma Protein Levels in Hypertensive Patients with Apical Periodontitis. J Contemp Dent Pract 2017;18(6):516-21.
Singhal RK, Rai B. sTNF-R Levels: Apical Periodontitis Linked to Coronary Heart Disease. Open Access Maced J Med Sci 2017;5(1):68-71.
Khalighinejad N, Aminoshariae A, Kulild JC, Sahly K, Mickel A. Association of End-stage Renal Disease with Radiographically and Clinically Diagnosed Apical Periodontitis: A Hospital-based Study. J Endod 2017;43(9):1438-41.
Gronkjaer LL, Holmstrup P, Schou S, Schwartz K, Kongstad J, Jepsen P, et al. Presence and consequence of tooth periapical radiolucency in patients with cirrhosis. Hepat Med 2016;8:97-103.
Ilievski V, Zuchowska PK, Green SJ, Toth PT, Ragozzino ME, Le K, et al. Chronic oral application of a periodontal pathogen results in brain inflammation, neurodegeneration and amyloid beta production in wild type mice. PLoS One 2018;13(10):e0204941.
Holmer J, Eriksdotter M, Schultzberg M, Pussinen PJ, Buhlin K. Association between periodontitis and risk of Alzheimer's disease, mild cognitive impairment and subjective cognitive decline: A case-control study. J Clin Periodontol 2018;45(11):1287-98.
Zhang J, Yu C, Zhang X, Chen H, Dong J, Lu W, et al. Porphyromonas gingivalis lipopolysaccharide induces cognitive dysfunction, mediated by neuronal inflammation via activation of the TLR4 signaling pathway in C57BL/6 mice. J Neuroinflammation 2018;15(1):37.
Bui FQ, Almeida-da-Silva CLC, Huynh B, Trinh A, Liu J, Woodward J, et al. Association between periodontal pathogens and systemic disease. Biomed J 2019;42(1):27-35.
Diaz-Zuniga J, Munoz Y, Melgar-Rodriguez S, More J, Bruna B, Lobos P, et al. Serotype b of Aggregatibacter actinomycetemcomitans triggers pro-inflammatory responses and amyloid beta secretion in hippocampal cells: a novel link between periodontitis and Alzheimer s disease? J Oral Microbiol 2019;11(1):1586423.
Singhrao SK, Olsen I. Assessing the role of Porphyromonas gingivalis in periodontitis to determine a causative relationship with Alzheimer's disease. J Oral Microbiol 2019;11(1):1563405.
Fuster JM. The prefrontal cortex--an update: time is of the essence. Neuron 2001;30(2).
Gabbott PL, Bacon SJ. Local circuit neurons in the medial prefrontal cortex (areas 24a,b,c, 25 and 32) in the monkey: I. Cell morphology and morphometrics. J Comp Neurol 1996; 364(4):567-608.
Boschin EA, Buckley MJ. Differential contributions of dorsolateral and frontopolar cortices to working memory processes in the primate. Front Syst Neurosci 2015;9:144.
Boschin EA, Piekema C, Buckley MJ. Essential functions of primate frontopolar cortex in cognition. Proc Natl Acad Sci U S A 2015;112(9):E1020-7.
Rushworth MF, Nixon PD, Eacott MJ, Passingham RE. Ventral prefrontal cortex is not essential for working memory. The Journal of neuroscience : the official journal of the Society for Neuroscience 1997;17(12).
Cruz-Rizzolo RJ, Horta-Júnior JdA, Bittencourt JC, Ervolino E, de Oliveira JA, Casatti CA. Distribution of NADPH-diaphorase-positive neurons in the prefrontal cortex of the Cebus monkey. Brain research 2006;1083(1).
Wilson CR, Gaffan D, Browning PG, Baxter MG. Functional localization within the prefrontal cortex: missing the forest for the trees? Trends Neurosci 2010;33(12):533-40.
Schmidt MJ, Mirnics K. Neurodevelopment, GABA system dysfunction, and schizophrenia. Neuropsychopharmacology 2015;40(1):190-206.
Celio MR. Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex. Science 1986;231(4741):995-7.
Kosaka T, Heizmann CW, Tateishi K, Hamaoka Y, Hama K. An aspect of the organizational principle of the gamma-aminobutyric acidergic system in the cerebral cortex. Brain Res 1987;409(2):403-8.
Demeulemeester H, Vandesande F, Orban GA, Heizmann CW, Pochet R. Calbindin D-28K and parvalbumin immunoreactivity is confined to two separate neuronal subpopulations in the cat visual cortex, whereas partial coexistence is shown in the dorsal lateral geniculate nucleus. Neurosci Lett 1989;99(1-2):6-11.
Hendry SH, Jones EG, Emson PC, Lawson DE, Heizmann CW, Streit P. Two classes of cortical GABA neurons defined by differential calcium binding protein immunoreactivities. Exp Brain Res 1989;76(2):467-72.
DeFelipe J, Hendry SH, Hashikawa T, Molinari M, Jones EG. A microcolumnar structure of monkey cerebral cortex revealed by immunocytochemical studies of double bouquet cell axons. Neuroscience 1990;37(3):655-73.
Rozycka A, Liguz-Lecznar M. The space where aging acts: focus on the GABAergic synapse. Aging Cell 2017;16(4):634-43.
DeFelipe J, Jones EG. High-Resolution Light and Electron Microscopic Immunocytochemistry of Colocalized GABA and Calbindin D-28k in Somata and Double Bouquet Cell Axons of Monkey Somatosensory Cortex. Eur J Neurosci 1992;4(1):46-60.
Hendry SH, Jones EG. GABA neuronal subpopulations in cat primary auditory cortex: co-localization with calcium binding proteins. Brain Res 1991;543(1):45-55.
Cintra LT, da Silva Facundo AC, Azuma MM, Sumida DH, Astolphi RD, Bomfim SR, et al. Pulpal and periodontal diseases increase triglyceride levels in diabetic rats. Clin Oral Investig 2013;17(6):1595-9.
Cintra LT, Samuel RO, Facundo AC, Prieto AK, Sumida DH, Bomfim SR, et al. Relationships between oral infections and blood glucose concentrations or HbA1c levels in normal and diabetic rats. Int Endod J 2014;47(3):228-37.
Pereira RF, Cintra LTA, Tessarin GWL, Chiba FY, de Lima Coutinho Mattera MS, Scaramele NF, et al. Periapical Lesions Increase Macrophage Infiltration and Inflammatory Signaling in Muscle Tissue of Rats. J Endod 2017;43(6):982-8.
Astolphi RD, Curbete MM, Chiba FY, Cintra LT, Ervolino E, da Mota MS, et al. Periapical Lesions Decrease Insulin Signaling in Rat Skeletal Muscle. J Endod 2015;41(8):1305-10.
Zoellner H. Dental infection and vascular disease. Semin Thromb Hemost 2011;37(3):181-92.
Moazzam AA, Rajagopal SM, Sedghizadeh PP, Zada G, Habibian M. Intracranial bacterial infections of oral origin. J Clin Neurosci 2015;22(5):800-6.
Aarabi G, Thomalla G, Heydecke G, Seedorf U. Chronic oral infection: An emerging risk factor of cerebral small vessel disease. Oral Dis 2019;25(3):710-9.
Tatullo M, Codispoti B, Makeeva I, Benincasa C, Spagnuolo G. From Mouth to Brain: Neuroendocrine Markers Play as a Crosstalk Among Oral and Neurodegenerative Diseases. Front Endocrinol (Lausanne) 2019;10:378.
Wang J, Geng X, Sun J, Zhang S, Yu W, Zhang X, et al. The risk of periodontitis for peripheral vascular disease: a systematic review. Rev Cardiovasc Med 2019;20(2):81-9.
Petroff OAC. GABA and glutamate in the human brain. The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry 2002;8(6).
Spiering MJ. The discovery of GABA in the brain. J Biol Chem. 2018, p. 19159-60.
Zeller A, Jurd R, Lambert S, Arras M, Drexler B, Grashoff C, et al. Inhibitory ligand-gated ion channels as substrates for general anesthetic actions. Handbook of experimental pharmacology 2008(182).
Ferguson BR, Gao WJ. PV Interneurons: Critical Regulators of E/I Balance for Prefrontal Cortex-Dependent Behavior and Psychiatric Disorders. Frontiers in neural circuits 2018;12.
Strandwitz P. Neurotransmitter modulation by the gut microbiota. Brain Res 2018;1693(Pt B):128-33.
Calvo-Flores BG, Vinnakota C, Govindpani K, Waldvogel HJ, Faull RLM, Kwakowsky A. The GABAergic system as a therapeutic target for Alzheimer's disease. Journal of neurochemistry 2018;146(6).
Auger ML, Floresco SB. Prefrontal cortical GABA modulation of spatial reference and working memory. The international journal of neuropsychopharmacology 2014;18(2).
Sun J, Jayathilake K, Zhao Z, Meltzer HY. Investigating association of four gene regions (GABRB3, MAOB, PAH, and SLC6A4) with five symptoms in schizophrenia. Psychiatry research 2012;198(2).
Royall DR, Lauterbach EC, Cummings JL, Reeve A, Rummans TA, Kaufer DI, et al. Executive control function: a review of its promise and challenges for clinical research. A report from the Committee on Research of the American Neuropsychiatric Association. The Journal of neuropsychiatry and clinical neurosciences 2002;14(4).
Berridge MJ. Neuronal calcium signaling. Neuron 1998;21(1):13-26.
Wojda U, Salinska E, Kuznicki J. Calcium ions in neuronal degeneration. IUBMB Life 2008;60(9):575-90.
Brini M, Cali T, Ottolini D, Carafoli E. Neuronal calcium signaling: function and dysfunction. Cell Mol Life Sci 2014;71(15):2787-814.
Gattoni G, Bernocchi G. Calcium-Binding Proteins in the Nervous System during Hibernation: Neuroprotective Strategies in Hypometabolic Conditions? Int J Mol Sci 2019;20(9).
Ijomone OM, Aluko OM, Okoh COA, Martins AC, Jr., Aschner M. Role for calcium signaling in manganese neurotoxicity. J Trace Elem Med Biol 2019;56:146-55.
Wypych D, Pomorski P. Calcium Signaling in Glioma Cells: The Role of Nucleotide Receptors. Adv Exp Med Biol 2020;1202:67-86.
Schwaller B. The continuing disappearance of "pure" Ca2+ buffers. Cell Mol Life Sci 2009;66(2):275-300.
Celio MR. Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 1990;35(2):375-475.
Lukas W, Jones KA. Cortical neurons containing calretinin are selectively resistant to calcium overload and excitotoxicity in vitro. Neuroscience 1994;61(2):307-16.
Molinari M, Dell'Anna ME, Rausell E, Leggio MG, Hashikawa T, Jones EG. Auditory thalamocortical pathways defined in monkeys by calcium-binding protein immunoreactivity. J Comp Neurol 1995;362(2):171-94.
Hof PR, Glezer, II, Conde F, Flagg RA, Rubin MB, Nimchinsky EA, et al. Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: phylogenetic and developmental patterns. J Chem Neuroanat 1999;16(2):77-116.
Zaitsev AV, Gonzalez-Burgos G, Povysheva NV, Kroner S, Lewis DA, Krimer LS. Localization of calcium-binding proteins in physiologically and morphologically characterized interneurons of monkey dorsolateral prefrontal cortex. Cereb Cortex 2005;15(8):1178-86.
Zakowski W. Neurochemistry of the Anterior Thalamic Nuclei. Mol Neurobiol 2017;54(7):5248-63.
Freund TF, Gulyas AI. GABAergic interneurons containing calbindin D28K or somatostatin are major targets of GABAergic basal forebrain afferents in the rat neocortex. J Comp Neurol 1991;314(1):187-99.
Hof PR, Mufson EJ, Morrison JH. Human orbitofrontal cortex: cytoarchitecture and quantitative immunohistochemical parcellation. J Comp Neurol 1995;359(1):48-68.
Eyles DW, McGrath JJ, Reynolds GP. Neuronal calcium-binding proteins and schizophrenia. Schizophr Res 2002;57(1):27-34.
Blumcke I, Celio MR. Parvalbumin and calbindin D-28k immunoreactivities coexist within cytochrome oxidase-rich compartments of squirrel monkey area 18. Exp Brain Res 1992;92(1):39-45.
Goodchild AK, Martin PR. The distribution of calcium-binding proteins in the lateral geniculate nucleus and visual cortex of a New World monkey, the marmoset, Callithrix jacchus. Vis Neurosci 1998;15(4):625-42.
Gibson CL, Clowry GJ. The effect on motor cortical neuronal development of focal lesions to the sub-cortical white matter in the neonatal rat: a model for periventricular leukomalacia. Int J Dev Neurosci 2003;21(4):171-82.
Pinheiro Botelho E, Guimaraes Martins Soares J, da Silva Pereira S, Fiorani M, Gattass R. Distribution of calbindin-28kD and parvalbumin in V1 in normal adult Cebus apella monkeys and in monkeys with retinal lesions. Brain Res 2006;1117(1):1-11.
Henny P, Jones BE. Projections from basal forebrain to prefrontal cortex comprise cholinergic, GABAergic and glutamatergic inputs to pyramidal cells or interneurons. Eur J Neurosci 2008;27(3):654-70.
Ahn JH, Hong S, Park JH, Kim IH, Cho JH, Lee TK, et al. Immunoreactivities of calbindinD28k, calretinin and parvalbumin in the somatosensory cortex of rodents during normal aging. Mol Med Rep 2017;16(5):7191-8.
Campos LM, Osorio EC, Santos GL, Nogueira MI, Cruz-Rizzolo RJ, Pinato L. Temporal changes in calcium-binding proteins in the medial geniculate nucleus of the monkey Sapajus apella. J Chem Neuroanat 2015;68:45-54.
Blumcke I, Hof PR, Morrison JH, Celio MR. Parvalbumin in the monkey striate cortex: a quantitative immunoelectron-microscopy study. Brain Res 1991;554(1-2):237-43.
Campos LM, Cruz-Rizzolo RJ, Pinato L. The primate seahorse rhythm. Brain Res 2015;1613:81-91.
Cueno ME, Ochiai K. Gingival Periodontal Disease (PD) Level-Butyric Acid Affects the Systemic Blood and Brain Organ: Insights Into the Systemic Inflammation of Periodontal Disease. Front Immunol 2018;9:1158.
Maldonado A, Laugisch O, Burgin W, Sculean A, Eick S. Clinical periodontal variables in patients with and without dementia-a systematic review and meta-analysis. Clin Oral Investig 2018;22(7):2463-74.
Campanella V, Oberti L, Gabrione F, Gonzalez-Valero L, Hernandez-Martinez V, Silvestre-Rangil J. Periodontitis and cerebrovascular disease: a new novel in medicine. J Biol Regul Homeost Agents 2019;33(3 Suppl. 1):135-44.
Fagundes NCF, Almeida A, Vilhena KFB, Magno MB, Maia LC, Lima RR. Periodontitis As A Risk Factor For Stroke: A Systematic Review And Meta-Analysis. Vasc Health Risk Manag 2019;15:519-32.
Hashioka S, Inoue K, Miyaoka T, Hayashida M, Wake R, Oh-Nishi A, et al. The Possible Causal Link of Periodontitis to Neuropsychiatric Disorders: More Than Psychosocial Mechanisms. Int J Mol Sci 2019;20(15).
Dioguardi M, Crincoli V, Laino L, Alovisi M, Sovereto D, Mastrangelo F, et al. The Role of Periodontitis and Periodontal Bacteria in the Onset and Progression of Alzheimer's Disease: A Systematic Review. J Clin Med 2020;9(2).
Gurav AN. Alzheimer's disease and periodontitis--an elusive link. Rev Assoc Med Bras (1992) 2014;60(2):173-80.
Ganesh P, Karthikeyan R, Muthukumaraswamy A, Anand J. A Potential Role of Periodontal Inflammation in Alzheimer's Disease: A Review. Oral Health Prev Dent 2017;15(1):7-12.
Ji MH, Qiu LL, Tang H, Ju LS, Sun XR, Zhang H, et al. Sepsis-induced selective parvalbumin interneuron phenotype loss and cognitive impairments may be mediated by NADPH oxidase 2 activation in mice. J Neuroinflammation 2015;12:182.
Rossignol E. Genetics and function of neocortical GABAergic interneurons in neurodevelopmental disorders. Neural Plast 2011;2011:649325.
McKenzie JA, Spielman LJ, Pointer CB, Lowry JR, Bajwa E, Lee CW, et al. Neuroinflammation as a Common Mechanism Associated with the Modifiable Risk Factors for Alzheimer's and Parkinson's Diseases. Curr Aging Sci 2017;10(3):158-76.
Wang RP, Ho YS, Leung WK, Goto T, Chang RC. Systemic inflammation linking chronic periodontitis to cognitive decline. Brain Behav Immun 2019;81:63-73.
Trindade SC, Olczak T, Gomes-Filho IS, Moura-Costa LF, Cerqueira EM, Galdino-Neto M, et al. Induction of interleukin (IL)-1beta, IL-10, IL-8 and immunoglobulin G by Porphyromonas gingivalis HmuY in humans. J Periodontal Res 2012;47(1):27-32.
Carvalho-Filho PC, Gomes-Filho IS, Meyer R, Olczak T, Xavier MT, Trindade SC. Role of Porphyromonas gingivalis HmuY in Immunopathogenesis of Chronic Periodontitis. Mediators Inflamm 2016;2016.
O'Boyle C, Haley MJ, Lemarchand E, Smith CJ, Allan SM, Konkel JE, et al. Ligature-induced periodontitis induces systemic inflammation but does not alter acute outcome after stroke in mice. Int J Stroke. 2020, p. 175-87.
Gomes B, Herrera DR. Etiologic role of root canal infection in apical periodontitis and its relationship with clinical symptomatology. Braz Oral Res 2018;32(suppl 1):e69.
Li ZG, Li JJ, Sun CA, Jin Y, Wu WW. Interleukin-18 promoter polymorphisms and plasma levels are associated with increased risk of periodontitis: a meta-analysis. Inflamm Res 2014;63(1):45-52.
Vaure C, Liu Y. A comparative review of toll-like receptor 4 expression and functionality in different animal species. Front Immunol 2014;5:316.
Pal D, Dasgupta S, Kundu R, Maitra S, Das G, Mukhopadhyay S, et al. Fetuin-A acts as an endogenous ligand of TLR4 to promote lipid-induced insulin resistance. Nat Med 2012;18(8):1279-85.
Reynolds JM, Martinez GJ, Chung Y, Dong C. Toll-like receptor 4 signaling in T cells promotes autoimmune inflammation. Proc Natl Acad Sci U S A 2012;109(32):13064-9.
Ardila CM, Guzman IC. Comparison of serum amyloid A protein and C-reactive protein levels as inflammatory markers in periodontitis. J Periodontal Implant Sci 2015;45(1):14-22.
Arimatsu K, Yamada H, Miyazawa H, Minagawa T, Nakajima M, Ryder MI, et al. Oral pathobiont induces systemic inflammation and metabolic changes associated with alteration of gut microbiota. Sci Rep 2014;4:4828.
Poole S, Singhrao SK, Kesavalu L, Curtis MA, Crean S. Determining the presence of periodontopathic virulence factors in short-term postmortem Alzheimer's disease brain tissue. J Alzheimers Dis 2013;36(4):665-77.
Kamer AR, Fortea JO, Videla S, Mayoral A, Janal M, Carmona-Iragui M, et al. Periodontal disease's contribution to Alzheimer's disease progression in Down syndrome. Alzheimers Dement (Amst) 2016;2:49-57.
Kamer AR, Morse DE, Holm-Pedersen P, Mortensen EL, Avlund K. Periodontal inflammation in relation to cognitive function in an older adult Danish population. Journal of Alzheimer's disease : JAD 2012;28(3).
Ding Y, Ren J, Yu H, Yu W, Zhou Y. Porphyromonas gingivalis, a periodontitis causing bacterium, induces memory impairment and age-dependent neuroinflammation in mice. Immun Ageing 2018;15:6.
Poole S, Singhrao SK, Chukkapalli S, Rivera M, Velsko I, Kesavalu L, et al. Active invasion of Porphyromonas gingivalis and infection-induced complement activation in ApoE-/- mice brains. J Alzheimers Dis 2015;43(1):67-80.
D'Orlando C, Fellay B, Schwaller B, Salicio V, Bloc A, Gotzos V, et al. Calretinin and calbindin D-28k delay the onset of cell death after excitotoxic stimulation in transfected P19 cells. Brain Res 2001;909(1-2):145-58.
Yang W, Jones LM, Isley L, Ye Y, Lee HW, Wilkins A, et al. Rational design of a calcium-binding protein. J Am Chem Soc 2003;125(20):6165-71.
Beasley CL, Reynolds GP. Parvalbumin-immunoreactive neurons are reduced in the prefrontal cortex of schizophrenics. Schizophr Res 1997;24(3):349-55.
Yew DT, Luo CB, Heizmann CW, Chan WY. Differential expression of calretinin, calbindin D28K and parvalbumin in the developing human cerebellum. Brain Res Dev Brain Res 1997;103(1):37-45.
Danos P, Baumann B, Bernstein HG, Franz M, Stauch R, Northoff G, et al. Schizophrenia and anteroventral thalamic nucleus: selective decrease of parvalbumin-immunoreactive thalamocortical projection neurons. Psychiatry Res 1998;82(1):1-10.
Cotter D, Landau S, Beasley C, Stevenson R, Chana G, MacMillan L, et al. The density and spatial distribution of GABAergic neurons, labelled using calcium binding proteins, in the anterior cingulate cortex in major depressive disorder, bipolar disorder, and schizophrenia. Biol Psychiatry 2002;51(5):377-86.
Lewis DA. Cortical circuit dysfunction and cognitive deficits in schizophrenia--implications for preemptive interventions. Eur J Neurosci 2012;35(12):1871-8.
Pehrson AL, Sanchez C. Altered gamma-aminobutyric acid neurotransmission in major depressive disorder: a critical review of the supporting evidence and the influence of serotonergic antidepressants. Drug Des Devel Ther 2015;9:603-24.
Gabbott PL, Bacon SJ. Local circuit neurons in the medial prefrontal cortex (areas 24a,b,c, 25 and 32) in the monkey: II. Quantitative areal and laminar distributions. J Comp Neurol 1996;364(4):609-36.
Gilabert-Juan J, Belles M, Saez AR, Carceller H, Zamarbide-Fores S, Molto MD, et al. A "double hit" murine model for schizophrenia shows alterations in the structure and neurochemistry of the medial prefrontal cortex and the hippocampus. Neurobiol Dis 2013;59:126-40.
Gilabert-Juan J, Castillo-Gomez E, Guirado R, Molto MD, Nacher J. Chronic stress alters inhibitory networks in the medial prefrontal cortex of adult mice. Brain Struct Funct 2013;218(6):1591-605.
Guzman-Martinez L, Maccioni RB, Andrade V, Navarrete LP, Pastor MG, Ramos-Escobar N. Neuroinflammation as a Common Feature of Neurodegenerative Disorders. Front Pharmacol 2019;10:1008.
Charlson FJ, Ferrari AJ, Santomauro DF, Diminic S, Stockings E, Scott JG, et al. Global Epidemiology and Burden of Schizophrenia: Findings From the Global Burden of Disease Study 2016. Schizophrenia bulletin 2018;44(6).
Yung AR, Firth J. How should physical exercise be used in schizophrenia treatment? Expert Rev Neurother 2017;17(3):213-4.
Terry RD, Gonatas NK, Weiss M. The ultrastructure of the cerebral cortex in Alzheimer's disease. Trans Am Neurol Assoc 1964;89:12.
Johnson GV, Hartigan JA. Tau protein in normal and Alzheimer's disease brain: an update. J Alzheimers Dis 1999;1(4-5):329-51.
Selkoe DJ. Alzheimer's disease results from the cerebral accumulation and cytotoxicity of amyloid beta-protein. J Alzheimers Dis 2001;3(1):75-80.
Querfurth HW, LaFerla FM. Alzheimer's disease. N Engl J Med 2010;362(4):329-44.
Du Y, Fu M, Wang YT, Dong Z. Neuroprotective Effects of Ginsenoside Rf on Amyloid-beta-Induced Neurotoxicity in vitro and in vivo. J Alzheimers Dis 2018;64(1):309-22.
Fung SJ, Webster MJ, Sivagnanasundaram S, Duncan C, Elashoff M, Weickert CS. Expression of interneuron markers in the dorsolateral prefrontal cortex of the developing human and in schizophrenia. Am J Psychiatry 2010;167(12):1479-88.
Fung SJ, Fillman SG, Webster MJ, Shannon Weickert C. Schizophrenia and bipolar disorder show both common and distinct changes in cortical interneuron markers. Schizophr Res 2014;155(1-3):26-30.
Chance SA, Walker M, Crow TJ. Reduced density of calbindin-immunoreactive interneurons in the planum temporale in schizophrenia. Brain Res 2005;1046(1-2):32-7.
Raghanti MA, Spocter MA, Butti C, Hof PR, Sherwood CC. A comparative perspective on minicolumns and inhibitory GABAergic interneurons in the neocortex. Front Neuroanat 2010;4:3.
Ferrer I, Tunon T, Serrano MT, Casas R, Alcantara S, Zujar MJ, et al. Calbindin D-28k and parvalbumin immunoreactivity in the frontal cortex in patients with frontal lobe dementia of non-Alzheimer type associated with amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry 1993;56(3):257-61.
Nishiyama E, Ohwada J, Iwamoto N, Arai H. Selective loss of calbindin D28K-immunoreactive neurons in the cortical layer II in brains of Alzheimer's disease: a morphometric study. Neurosci Lett 1993;163(2):223-6.
Gomez-Tortosa E, Sanders JL, Newell K, Hyman BT. Cortical neurons expressing calcium binding proteins are spared in dementia with Lewy bodies. Acta Neuropathol 2001;101(1):36-42.
Pugliese M, Carrasco JL, Geloso MC, Mascort J, Michetti F, Mahy N. Gamma-aminobutyric acidergic interneuron vulnerability to aging in canine prefrontal cortex. J Neurosci Res 2004;77(6):913-20.
Volk DW, Matsubara T, Li S, Sengupta EJ, Georgiev D, Minabe Y, et al. Deficits in transcriptional regulators of cortical parvalbumin neurons in schizophrenia. Am J Psychiatry 2012;169(10):1082-91.
Reynolds GP, Beasley CL. GABAergic neuronal subtypes in the human frontal cortex--development and deficits in schizophrenia. J Chem Neuroanat 2001;22(1-2):95-100.
Glausier JR, Fish KN, Lewis DA. Altered parvalbumin basket cell inputs in the dorsolateral prefrontal cortex of schizophrenia subjects. Mol Psychiatry 2014;19(1):30-6.
Torrey EF, Barci BM, Webster MJ, Bartko JJ, Meador-Woodruff JH, Knable MB. Neurochemical markers for schizophrenia, bipolar disorder, and major depression in postmortem brains. Biol Psychiatry 2005;57(3):252-60.
Sohal VS, Zhang F, Yizhar O, Deisseroth K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 2009;459(7247):698-702.
Acosta C, Anderson HD, Anderson CM. Astrocyte dysfunction in Alzheimer disease. J Neurosci Res 2017;95(12):2430-47.
Vincent AJ, Gasperini R, Foa L, Small DH. Astrocytes in Alzheimer's disease: emerging roles in calcium dysregulation and synaptic plasticity. J Alzheimers Dis 2010;22(3):699-714.
Jo S, Yarishkin O, Hwang YJ, Chun YE, Park M, Woo DH, et al. GABA from reactive astrocytes impairs memory in mouse models of Alzheimer's disease. Nat Med 2014;20(8):886-96.
Li K, Li J, Zheng J, Qin S. Reactive Astrocytes in Neurodegenerative Diseases. Aging Dis. 2019, p. 664-75.
Riviere GR, Riviere KH, Smith KS. Molecular and immunological evidence of oral Treponema in the human brain and their association with Alzheimer's disease. Oral Microbiol Immunol 2002;17(2):113-8.
Teixeira FB, Saito MT, Matheus FC, Prediger RD, Yamada ES, Maia CSF, et al. Periodontitis and Alzheimer's Disease: A Possible Comorbidity between Oral Chronic Inflammatory Condition and Neuroinflammation. Front Aging Neurosci 2017;9:327.
Li T, Chen X, Zhang C, Zhang Y, Yao W. An update on reactive astrocytes in chronic pain. J Neuroinflammation. 2019.
Ciesielska A, Joniec I, Kurkowska-Jastrzebska I, Cudna A, Przybylkowski A, Czlonkowska A, et al. The impact of age and gender on the striatal astrocytes activation in murine model of Parkinson's disease. Inflamm Res 2009;58(11):747-53.
Hirsch EC, Hunot S. Neuroinflammation in Parkinson's disease: a target for neuroprotection? Lancet Neurol 2009;8(4):382-97.
Lee HJ, Suk JE, Patrick C, Bae EJ, Cho JH, Rho S, et al. Direct transfer of alpha-synuclein from neuron to astroglia causes inflammatory responses in synucleinopathies. J Biol Chem 2010;285(12):9262-72.
Gu XL, Long CX, Sun L, Xie C, Lin X, Cai H. Astrocytic expression of Parkinson's disease-related A53T alpha-synuclein causes neurodegeneration in mice. Mol Brain 2010;3:12.
Halliday GM, Stevens CH. Glia: initiators and progressors of pathology in Parkinson's disease. Mov Disord 2011;26(1):6-17.
Barcia C, Ros CM, Annese V, Gomez A, Ros-Bernal F, Aguado-Llera D, et al. IFN-gamma signaling, with the synergistic contribution of TNF-alpha, mediates cell specific microglial and astroglial activation in experimental models of Parkinson's disease. Cell Death Dis 2012;3:e379.
Sofroniew MV. Astrogliosis. Cold Spring Harb Perspect Biol 2014;7(2):a020420.
Liberman AC, Trias E, da Silva Chagas L, Trindade P, Dos Santos Pereira M, Refojo D, et al. Neuroimmune and Inflammatory Signals in Complex Disorders of the Central Nervous System. Neuroimmunomodulation 2018;25(5-6):246-70.
Carroll JA, Chesebro B. Neuroinflammation, Microglia, and Cell-Association during Prion Disease. Viruses. 2019.
Kaur D, Sharma V, Deshmukh R. Activation of microglia and astrocytes: a roadway to neuroinflammation and Alzheimer's disease. Inflammopharmacology 2019;27(4):663-77.
