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Are Astrocytes Executive Cells Within the Central Nervous System? ¿Son Los Astrocitos Células Ejecutivas Dentro Del Sistema Nervioso Central? Roberto E

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Are Astrocytes Executive Cells Within the Central Nervous System? ¿Son Los Astrocitos Células Ejecutivas Dentro Del Sistema Nervioso Central? Roberto E DOI: 10.1590/0004-282X20160101 VIEW AND REVIEW Are astrocytes executive cells within the central nervous system? ¿Son los astrocitos células ejecutivas dentro del Sistema Nervioso Central? Roberto E. Sica1, Roberto Caccuri1, Cecilia Quarracino1, Francisco Capani1 ABSTRACT Experimental evidence suggests that astrocytes play a crucial role in the physiology of the central nervous system (CNS) by modulating synaptic activity and plasticity. Based on what is currently known we postulate that astrocytes are fundamental, along with neurons, for the information processing that takes place within the CNS. On the other hand, experimental findings and human observations signal that some of the primary degenerative diseases of the CNS, like frontotemporal dementia, Parkinson’s disease, Alzheimer’s dementia, Huntington’s dementia, primary cerebellar ataxias and amyotrophic lateral sclerosis, all of which affect the human species exclusively, may be due to astroglial dysfunction. This hypothesis is supported by observations that demonstrated that the killing of neurons by non-neural cells plays a major role in the pathogenesis of those diseases, at both their onset and their progression. Furthermore, recent findings suggest that astrocytes might be involved in the pathogenesis of some psychiatric disorders as well. Keywords: astrocytes; physiology; central nervous system; neurodegenerative diseases. RESUMEN Evidencias experimentales sugieren que los astrocitos desempeñan un rol crucial en la fisiología del sistema nervioso central (SNC) modulando la actividad y plasticidad sináptica. En base a lo actualmente conocido creemos que los astrocitos participan, en pie de igualdad con las neuronas, en los procesos de información del SNC. Además, observaciones experimentales y humanas encontraron que algunas de las enfermedades degenerativas primarias del SNC: la demencia fronto-temporal; las enfermedades de Parkinson, de Alzheimer, y de Huntington, las ataxias cerebelosas primarias y la esclerosis lateral amiotrófica, que afectan solo a los humanos, pueden deberse a astroglíopatía. Esta hipótesis se sustenta en hallazgos que demostraron que la muerte neuronal que en ellas ocurre es debida al compromiso de células no-neuronales que juegan rol principal en su iniciación y desarrollo. Más aún, observaciones recientes señalan que los astrocitos podrían estar implicados en la patogenia de algunas enfermedades psiquiátricas. Palabras clave: astrocitos; fisiología; sistema nervioso central; enfermedades neurodegenerativas. The physiological properties of astrocytes have been the homeostasis of the CNS extracellular medium6, the initiation subject of comprehensive reviews written in the last few of the inflammatory and immune responses7 and the build- years1, while other authors have highlighted the role that as- ing up of barriers between normal and damaged tissues8. trocytes play in the development of diseases previously at- Astrocytes can behave like phagocytic cells9, they sense the 2,3 10 tributed solely to neurons . partial pressure of O2 within the CNS and they can trans- Our aim is to present a brief overview of the interplay form into neurons when the brain is in need of rebuilding between astrocytes and neurons in normal and pathological damaged functional neural networks contributing to ner- conditions within the central nervous system (CNS). vous tissue repair11. Therefore, we believe that the astrocyte deserves to be considered, in its own right, one of the main players orchestrating fundamental functions within the CNS. ASTROCYTES IN PHYSIOLOGY Since Ramon y Cajal’s neuron theory was accepted in 1889, most researchers thought that neurons were the most Several investigations have described the capabilities of valuable cells in the functions performed by the CNS. If we the astrocytes in handling part of the workload of the CNS. critically analyze their properties, the foremost is their capac- They modulate the myelinating capacity of the oligoden- ity to convey messages at high speed by propagating action drocytes4, the synaptic cross-talk amongst neurons5, the potentials (APs) that travel through their dendrites, bodies 1Universidad de Buenos Aires, Escuela de Medicina, Instituto de Investigaciones Cardiológicas, Buenos Aires, Argentina. Correpondence: Roberto E. Sica; ININCA. Marcelo T. de Alvear 2480; ZIP 1221 Buenos Aires, Argentina. E-mail: [email protected] Conflict of interest: There is no conflict of interest to declare. Received 04 March 2016; Accepted 16 March 2016 671 and axons membranes. The electrical activity is of such para- Observations recently reported suggest that astro- mount importance for neurons that it consumes 75% of the cytes may have an even more intimate relationship with brain cortical energy; one fifth of it is employed to sustain APs, neurons by establishing contact with them through gap another fifth accounts for the maintenance of the membrane junctions (GJ)16 that allow both types of cells to exchange resting potential, and the remainder is consumed in synaptic molecules and ions, modifying their metabolism and the dynamics. “Housekeeping”, a term coined by Attwell’s group, expression of their genes17. meaning the non-signalling tasks performed by the neurons (such as proteins shuttle and turnover, axoplasmic flows and Anatomic phylogenetic remarks other intracellular processes), consumes only 25% of the to- In humans, glial cells are the largest family of cells with- tal energy. Knowing that the brain cortical energy has been in the CNS. Friede was the first to compare the numbers of estimated in 27.2 µmol ATP/g/min, neuronal signal activity glia and neurons and found that, in humans, glia outnum- requires 20.41 µmol ATP/g/min, more than twice the energy ber neurons by 1.48, a factor known in the literature as the consumed to carry out the intraneuronal metabolic process- glia/neuron ratio (G/Nr ratio)18. In species considered phy- es12. The conclusion that can be drawn from these observa- logenetically below humans, those ratios were smaller; for tions is that the function prioritized by neurons is signalling. instance in frogs it was 0.25, chickens 0.46, mice 0.36, rab- In order to maintain the integrity of the body, most chang- bits 0.43, pigs 1.20, cows 1.22 and horses 1.23. The higher es within the environment of a living being need a response human G/Nr ratio was initially considered a peculiarity of that, in special circumstances, must be achieved effectively the human species19. and quickly, such as happens with the reflex responses that However, in contrast to those findings, Hawkins et al. are below the conscious level. These responses occur in a found a 4.54 G/Nr ratio in the cortex of the fin whale20, sug- milliseconds time scale, which has always been regarded gesting that the G/Nr ratio is not related to the phylogenetic as an exclusive domain of neurons. However, some studies position of the species. Moreover, by estimating the number have found that astrocytes can release, by exocytosis, the of neurons within the brain of several species they concluded gliotransmitter glutamate into the synaptic cleft in the same that the density of neurons decreases as the volume of the time scale that neurons employ, suggesting that astrocytes brain increases. So, the number of neurons in the brains of may have a role in the fast synaptic activity, matching the ca- mice is 142,000/mm3, in humans the figure was estimated to pacities of the neurons in this aspect13. This observation in- be about 9,500 neurons/mm3, while the brain cortex of the fin dicates that astrocytes may have a role in the elaboration of whale and the Indian elephant has about 7,000 neurons/mm3, the reflex responses. a lower value than in humans21,22. One possible explanation for the reduced number of neu- Neuron-astrocyte dynamics rons in highly-developed phylogenetic species is that the Further reasoning leads to the question: What drives the neurons are larger in size, assembled with a greater number functions of neurons when a response has to be elaborated to of dendrites and thicker axons streaming through bigger ter- adapt the conditions of the self to the environs, differentiat- ritories. These morphological neuronal changes parallel the ing the right response amongst many possibilities? We know behaviour of the astroglia, which become larger in size, both that the synaptic transmitters carry information from one in humans and in apes, with thicker and longer processes de- neuron to another that receives the message through iono- picting bigger domains encompassing up to 2 million syn- tropic receptors. We also know that there is protein traffic apses in humans compared to, for example, a maximum of within the neuron’s body that is activated by second messen- 120,000 in mice. gers that are put to work by the stimulation of metabotropic In summary, it appears that the composition of the cells receptors located on the cell and neurite membranes. The in the cerebral cortex does not explain the different behav- post-synaptic neuron receiving the information from the pre- iours between species. Hence, human intellectual properties synaptic neuron will repeat the cycle stimulating other neu- cannot be attributed either to an increased number of neu- ron until the desired goal is achieved. But, are the neurons rons or to a larger number of astrocytes. free to deliver these types of messages just by themselves? Herculano-Houzel’s findings23 support what has been Synaptic activity is modulated by astrocytes, which stated above. The
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