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Circumventricular Organs Dysregulation Syndrome (CODS)

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Circumventricular Organs Dysregulation Syndrome (CODS) Circumventricular organs dysregulation syndrome (CODS) ● 第 70 回日本自律神経学会総会 / 理事長講演 司会：髙橋 昭 Circumventricular organs dysregulation syndrome (CODS) Yoshiyuki Kuroiwaa,b Kew words: aquaporin, cerebrospinal fluid, circadian rhythm, guanine nucleotide coupling protein, transient receptor potential Abstract: The biological origin of circumventricular organs (CVOs) evolutionally goes back to the inverte- brates and even further to plants. The CVOs are classified into sensory CVOs (subfornical organ, organum vasculosum of lamina terminalis, and area postrema) and secretory CVOs (neurohypophysis, pineal gland, subcommissural organ, and median eminence). Physiological mechanisms of life-saving homeostasis arising from CVOs consist of at least the following eight axes; neuroendocrine regulation axis, circadian rhythm regulation axis, innate immune regulation axis, nociceptive response regulation axis, body fluid regulation axis, cognitive regulation axis, locomotive driving regulation axis, and inhibitory regulation axis. Summarizing the above, the CVO physiologically contributes to a wide spectrum of autonomic, endocrine, cognitive, sensory gating, and motor regulations, whose impairments potentially result in the complex symptoms being composed of sleep- related, cardiovascular, gastrointestinal, menstrual, emotional, cognitive, sensory, and motor symptoms. I pro- pose the new clinical concept, “circumventricular organs dysregulation syndrome (CODS)” that is known to be seen in human papilloma virus vaccination-associated neuro-immunopathic syndrome (HANS), von Economo’s encephalitis lethargica, craniopharyngioma, interferon encephalopathy, metronidazole induced encephalopathy, Wernicke encephalopathy, schizohrenia with water intoxication, Alzheimer’s disease with overeating, neuromy- elitis optica, stiff-person syndrome, cerebrospinal fluid hypovolemia, heat stroke, fibromyalgia, chronic fatigue syndrome / myalgic encephalomyelitis, menopausal syndrome, and frailty syndrome (sarcopenia syndrome). （The Autonomic Nervous System, 56: 1 ～ 5, 2019） 1. Introduction 2. Anatomical Structures of the CVOs / Hypothalamus Complex Circumventricular organs (CVOs) are brain organs which regulate life-saving homeostasis of the vertebrates. The CVOs are structurally and functionally designed The biological origin of CVOs evolutionally goes back as specialized organs which defend the vertebrates to the invertebrates and even further to the plants. I against environmental stress. The autonomic and neu- referred clinical disorders occurring after their dys- roendocrine centers exist in the CVOs, and contribute regulation as to circumventricular organs dysregulation to homeostatic regulation of the vertebrates. The CVOs syndrome (CODS). The first half of this paper explains are located in the diencephalon and the medulla of the anatomical and physiological knowledges of CVOs, while vertebrates, and are characterized as symmetrical mid- the second half describes clinical spectrum of CODS. line organs around the third and the fourth ventricles. The CVOs around the third ventricle are adjacent to the thalamus (paraventricular organ) and the hypothalamus. The retina and the choroid plexus (CP) are not usually classified into the CVOs, but embryologically belong to a Medical Office, Ministry of Finance, 3-1-1 Kasumigaseki, the CVOs. The CP is adjacent to the lateral, the third Chiyoda-ku, Tokyo 100-8940, Japan b and the fourth ventricles. The CP not only secretes Department of Neurology and Stroke Center, Mizonokuchi Hospital, Teikyo University School of Medicine, 5-1-1 Futako, cerebrospinal fluid (CSF), but also regulates circadian Takatsu-ku, Kawasaki, Kanagawa 213-8507, Japan rhythm along with suprachiasmatic nucleus (SCN) of （1） 自律神経 56 巻 1 号 2019 年 the hypothalamus. Among the hypothalamus, only the as a neuro-glandular organ, to secrete vasopressin and median eminence (ME) is usually classified into the oxytocin. CVOs. However, the CVOs and the hypothalamus are The CVOs / hypothalamus complex has vital neuro- anatomically connected, and are closely related with immuno-endocrine network, and is essential for homeo- each other. The CVOs are classified into sensory and static activity of the vertebrates. Guanine nucleotide secretory organs. coupling protein (G protein) subfamilies in the CVOs / The subfornical organ (SFO), the organum vasculosum hypothalamus complex act as biological timer switches of the lamina terminalis (OVLT), and the area postrema which maintain and regulate neuro-immuno-endocrine (AP) are referred to as sensory CVOs, because they are homeostasis of the vertebrates. Summarizing the neuronal organs and are able to detect environmental above, life-saving homeostasis arises from the CVOs / stress. The SFO exists around the lateral and the third hypothalamus complex, which physiologically contributes ventricles, while the OVLT is adjacent to the ventral to a wide spectrum of autonomic, endocrine, cognitive, wall of the third ventricle. The AP in the lower medulla sensory gating, and motor regulations. The CVOs / is adjacent to the dorsal wall of the fourth ventricle. The hypothalamus complex has its regulatory mechanisms sensory CVOs have neural networks connecting with consisting of eight physiological axes, as described in the preoptic area (POA) and paraventricular nucleus (PVN) next paragraph. in the hypothalamus. 3. Physiological Axes of the CVOs / Hypothalamus The neurohypophysis, the pineal gland, the subcom- Complex missural organ (SCO), and the ME have glandular structures with secretory functions, and are referred 3.1. Neuroendocrine regulation axis to as secretory CVOs. The neurohypophysis (posterior Hypothalamic-pituitary-neuroendocrine pathways pituitary gland) is adjacent to the ventral wall of the consist of hypothalamic-pituitary-adrenal axis (HPA third ventricle, and secretes vasopressin and oxytocin, axis), hypothalamic-pituitary-gonadal axis (HPG axis), and while the pineal gland secretes melatonin. The SCO is hypothalamic-pituitary- thyroid axis (HPT axis). located in the dorsocaudal region of the third ventricle, The HPA axis plays an important role to protect the and at the entrance of the cerebral aqueduct. The life of the vertebrates from emergency stress, and is ependymal cells of the SCO secrete high molecular mass essential to their survival4). The HPA axis is our central glycoproteins (spondin in Reissner’s fiber) and brain stress response system, which contributes to regulation transthyretin. The ME is rich in mast cells, and secretes of homeostasis against environmental stress. The neuro- inflammation mediating substances. endocrine activation of the HPA axis triggers stress The window of the brain (CVOs) lacks blood brain response (Fight-or-flight response), such as elevation of barriers. The subependymal ventricular zone in CVOs blood pressure and blood sugar, and suppression of pain. and the hypothalamus are exceptional brain structures, This stress response system is characterized by hypo- where neurogenesis occurs even in adult brain. It is thalamic release of corticotropin-releasing factor (CRF). important to recognize the view point of the CVOs / hy- When CRF binds to CRF receptors on the anterior pothalamus complex from the perspective of functional pituitary gland, adrenocorticotropic hormone (ACTH) is differentiation; 1) OVLT, neurohypophysis, and saccus released. When ACTH binds to receptors on the adrenal vasculosus were differentiated as organs having blood cortex, it stimulates adrenal release of cortisol lasting for vessels in abundance, 2) SFO, OVLT, and AP were dif- several hours after encountering the stressor. ferentiated as neuro-sensory organs, 3) neurohypophysis, The HPG axis plays a critical part in the development pineal gland, SCO, and ME were differentiated as neuro- and regulation of the reproductive and immune systems. glandular organs, 4) SFO was differentiated as an organ Gonadotropin-releasing hormone (GnRH) expressing to regulate instinctive drinking behavior via angiotensin neurons in the hypothalamus secretes GnRH. Leptin II receptor, 5) POA was differentiated as a window of and insulin have stimulatory effects and ghrelin has the brain to detect harmful changes in external environ- inhibitory effects on GnRH secretion. In response to ment, such as hypoxia, toxic gas, chemical toxins, high GnRH stimulation, the anterior portion of the pituitary or low temperature, strong ultraviolet rays, and nuclear gland produces follicle-stimulating hormone (FSH) and radiation exposure, etc, and 6) PVN was differentiated luteinizing hormone (LH), which travel into the blood （2） Circumventricular organs dysregulation syndrome (CODS) stream. The gonads produce estrogen and testosterone, rich in perivascular mast cells19). As the front line of the which significantly influence the neurovascular coupling brain, the hypothalamic mast cells regulate innate im- system. Besides cortisol and estrogen, vitamin D is mune system via pattern-recognition receptors (PRRs)10) another steroid hormone, whose activating enzymes and via HPA axis. After bactrial infection or traumatic exist in the hypothalamus, and contributes to generation injury, hypothalamic PRRs recognize pathogen-associated of stress response. molecular patterns (PAMPs) and/or damage-associated The HPT axis contributes to thyrotropic feedback con- molecular patterns (DAMPs), and activate the innate trol as a part of the neuroendocrine system responsible immune system. Then, the hypothamic PRRs interact for metabolic regulation. The
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