Abstract
Maintenance of hydromineral balance (HB) is an essential condition for life activity at cellular, tissue, organ and system levels. This activity has been considered as a function of the osmotic regulatory system that focuses on hypothalamic vasopressin (VP) neurons, which can reflexively release VP into the brain and blood to meet the demand of HB. Recently, astrocytes have emerged as an essential component of the osmotic regulatory system in addition to functioning as a regulator of the HB at cellular and tissue levels. Astrocytes express all the components of osmoreceptors, including aquaporins, molecules of the extracellular matrix, integrins and transient receptor potential channels, with an operational dynamic range allowing them to detect and respond to osmotic changes, perhaps more efficiently than neurons. The resultant responses, i.e., astroglial morphological and functional plasticity in the supraoptic and paraventricular nuclei, can be conveyed, physically and chemically, to adjacent VP neurons, thereby influencing HB at the system level. In addition, astrocytes, particularly those in the circumventricular organs, are involved not only in VP-mediated osmotic regulation, but also in regulation of other osmolality-modulating hormones, including natriuretic peptides and angiotensin. Thus, astrocytes play a role in local/brain and systemic HB. The adaptive astrocytic reactions to osmotic challenges are associated with signaling events related to the expression of glial fibrillary acidic protein and aquaporin 4 to promote cell survival and repair. However, prolonged osmotic stress can initiate inflammatory and apoptotic signaling processes, leading to glial dysfunction and a variety of brain diseases. Among many diseases of brain injury and hydromineral disorders, cytotoxic and osmotic cerebral edemas are the most common pathological manifestation. Hyponatremia is the most common cause of osmotic cerebral edema. Overly fast correction of hyponatremia could lead to central pontine myelinolysis. Ischemic stroke exemplifies cytotoxic cerebral edema. In this review, we summarize and analyze the osmosensory functions of astrocytes and their implications in cerebral edema.
Highlights
Homeostasis of the internal environment is the prerequisite for normal activity of an organism and heavily depends on the hydromineral balance (HB) of the extracellular fluid
The sensitivity of osmosensors to hypoosmotic challenge gradually wears off during continuous stimulation; correspondingly, the initial inhibitory reaction vanishes during prolonged presence of hypoosmotic environment. This notion is partly supported by the recovery of firing rate of VP neurons after initial hypoosmotic inhibition, which is based on dual astrocytic morphological plasticity, i.e., extension and subsequent retraction of astroglial processes during the initial decrease in firing rate of VP neurons followed by its recovery, respectively (Wang et al, 2013a,b)
Astrocytes could exert self- modulation during osmotic challenges. This notion is supported by the observation that following 7 and 14 days of 2% NaCl (N.B., isotonic solution contains 0.9% NaCl) in drinking water, a significant increase in Ang angiotensin II (II) precursor, preproangiotensinogen mRNA was detected in astrocytes in regions of the anterior hypothalamus, including the paraventricular nucleus (PVN), the medial preoptic area and medial preoptic nucleus, while a decrease was observed in astrocytes in the supraoptic nucleus (SON) (Ryan and Gundlach, 1997)
Summary
Reviewed by: Robert Zorec, University of Ljubljana, Slovenia Sergey Kasparov, University of Bristol, United Kingdom.
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