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The Strength Training Anatomy Workout. Whereas normally sleeping, immunized mice were able to clear the virus from the respiratory tract within 3 days of challenge, in immunized, sleep-deprived animals, the extent of viral recovery was almost the same as in nonimmunized animals Figure Brown et al.

Phase shifts, as they are encountered in shift workers or after transmeridian flights, or rhythm disturbances in people under grossly irregular work schedules lead to internal desynchronization of immune-related circadian rhythms and to impairment of immune functions. In rats, weekly inversion of a light:dark LD lighting regimen led after 2 months to a decreased cellular immune response as measured by mitogen stimulation with concanavalin A ConA and by a popliteal lymph node assay Kort and Weijma, A rather severe immune impairment was found after 33 weeks of weekly phase shifting.

Spot checks of adrenal function in these animals, measured in vitro and in vivo at a single time point only, did not reveal substantial changes. The latter result has to be qualified since single time point sampling does not allow an evaluation of the adrenal cycle.

In studies of shift workers, Nakano et al. Since shift work is often accompanied by a certain degree of sleep deprivation, it is unclear whether the impaired immune function in shift workers is a consequence of circadian desynchronization, sleep deprivation, or both. Gonadal steroids contribute to the regulation of immune function Da Silva and Hall, ; H. Fox, b; Hasty et al.

Receptors for steroid hormones are present in circulating lymphocytes Bellido et al. Effect of sleep deprivation on ability to respond to challenge with antigen influenza virus in immunized mice. Challenge followed by 7 hours of sleep deprivation. Sleep deprivation leads to impairment of antibody response A and of elimination of antigen B. No or only minor changes in the number of circulating blood cells were reported during the menstrual cycle Eichler and Keiling, ; Fox et al. In a comparison between day 6 and day 22 of the menstrual cycle, there were no consistent changes in the proportion of lymphocyte subtypes, nor were there any significant changes in the absolute numbers or in the circadian rhythmicity in total white blood cell count, granulocytes, lymphocytes, T- and B-cells, T-helper and suppressor cells, and NK cells Dixon-Northern et al.

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The only apparent difference as a function of the day of the menstrual cycle was found in the circadian periodicity of monocytes, for which the trough was found at 12 noon for day 6 and at midnight for day 22 Dixon-Northern et al. The limited sampling and the small number of subjects in these studies do not allow the drawing of final conclusions. In contrast, the plasma IL-1 activity Cannon and Dinarello, is consistently increased after ovulation in the luteal phase of the menstrual cycle simultaneously with the elevation in body temperature. In view of the thermogenic effect of IL-1, this may be related and may also be consistent with the observation that progesterone and estrogen increase the macrophage production of IL-1 Olsen and Kovacs, Related to differences in the human immune response during different stages of the menstrual cycle may be the clinical observation of a greatly reduced overall and recurrence-free survival in women with breast cancer who were operated on during days 3 to 12 after onset of menstruation as compared with women operated on between days 0 through 2 or days 13 through 32 Badwe et al.

Changes of immune-related variables during different seasons may be caused by climatic differences, including day length, temperature, and related factors such as exposure to allergens and microorganisms, but they may also be the consequence of endogenous circannual rhythms that may or may not be synchronized by environmental climatic and other stimuli Haus and Touitou, b.

Circannual rhythms have been demonstrated in animals kept for their entire life, and in some instances for generations, in environments with a standardized lighting regimen and constant temperature Figure Brock, , ; Haus et al. The seasonal rhythmicity in lymphocyte blastogenic response persists in young mice kept in a constant environment Brock, Mortality in the young animals varied in a circannual fashion, with the peak occurring when the proliferation rates of both T- and B-cells were low Brock, In contrast in old animals, the amplitude of the circannual rhythm of T- and B-cells.

These studies suggested a rhythm with a period of about 6 months for circulating T-helper cells. There appeared to be circadian desynchronization of circulating lymphocytes during spring, which corresponded in its timing to the peak incidence of viral infections and of Hodgkin's disease Levi et al. Pati et al. Shifrine et al. Studying the whole-blood, lectin-induced, lymphocyte mitogen response, they observed a peak in summer and poor response to mitogens in winter. A circannual variation of rubella antibody titer was noted in a large number of patients who were followed for 7 years Rosenblatt et al.

In Finland, a country with marked climatic differences between the seasons, Katila et al. In contrast, no seasonal differences in this variable were found in Japan Kishida et al. Deficiency in erythrocyte adenosine aminohydrolase activity has been reported in patients with severe combined immunodeficiency disease Giblett et al.

In a study extending over 2 years, Nechaev et al. In healthy subjects and in patients with cancer, the circannual variation resulted in relatively low enzyme levels between April and June and higher levels between October and February. Seasonal modifications in immune response must be considered in clinical trials and in the planning of immunotherapeutic treatment strategies for various diseases. Physical exercise alters the circadian periodicity of several components of the immune system and of related neuroendocrine variables Shephard et al. With moderate exercise, these changes are short in duration and may only transiently mask the circadian rhythm of, for example, catecholamines, the numbers of polymorphonuclear leukocytes, and lymphocytes.

Physical performance and performance tolerance vary. Maximal performance e. While moderate physical exercise and training may improve certain immune functions, severe and exhaustive exercise is immunosuppressive for review, see Shephard et al. Severe and exhaustive exercise can also mark many of the neuroendocrine rhythms that are instrumental in regulating the rhythmicity and, to some degree, the integrity of the immune system Opstad, , However, no investigations of the effects of circadian and other periodicities in performance on the response of the immune system to exercise have been found in the available literature.

Investigations of the periodicity in exercise effects acute strenuous as well as endurance on the neuroendocrine-immune system network might be of considerable interest for military and sports medicine. The activity-rest and sleep-wakefulness pattern is not the only synchronizer acting on the mammalian circadian system. If a large proportion of the daily caloric intake is taken as one major meal at a certain circadian phase, the timing of food uptake may mask the circadian rhythms.

If such intake persists for a prolonged time, it may become the dominant synchronizer of some circadian periodic functions. In animal studies, many circadian rhythms related directly or indirectly to immune functions can be adjusted in their timing by time-restricted meal feeding at certain circadian stages Halberg and Stephens, ; Lakatua et al.

Other rhythms, however, will remain synchronized to the light-dark regimen in experimental animals or to the activity-rest pattern in humans. A number of endocrine and hematologic rhythms may show, under the influence of the ''competing'' synchronizers, some changes in their usual timing without the apparent predominance of either synchronizer. In human subjects, time adaptation of rhythms by timed food uptake is much less pronounced and can be achieved only by exposure to rigorous feeding schedules that would be uncommon in everyday life. Clinically healthy, young adult volunteers following a diurnal activity pattern with sleep during the night typically between and who received all their calories in the form of a single meal as breakfast or as dinner were studied over a h span at the end of 3 weeks on that regimen.

The circadian rhythms of plasma insulin, serum iron, and blood urea nitrogen concentration had adapted their timing to the time of food uptake, irrespective of the activity pattern of the subjects. In contrast, the timing of the circadian rhythms in growth hormone GH , plasma. In a shorter study in which all calories were given either as breakfast or as dinner, Sensi et al.

In urinary catecholamines, the evening mealonly schedule delayed the circadian peak for over 5 hours. Cortisol did not seem to be influenced by the short period of meal timing, and sodium and potassium excretion did not show consistent differences between the two diet regimens. After 18 days on the altered schedule of calorie uptake, plasma cortisol and thyroid-stimulating hormone TSH circadian rhythms were similar, as seen with a three-meal diet. The circadian rhythm in PRL was detectable when the single daily meal was given at but disappeared when the meal was given at From these and other studies in human subjects Goetz et al.

Also the circadian rhythms of many liver enzymes are synchronized primarily by the time of food uptake Fuller and Snoddy, In human subjects, some of the most stable rhythms such as plasma cortisol and circulating lymphocytes , which directly relate to the regulation of immune functions, are apparently synchronized predominantly by the activity-rest schedule and the related light-dark regimen.

However, with prolonged exposure to unusual feeding schedules, the changes observed in GH and insulin may well lead to changes in the timing of certain immune-related variables, although experimental evidence for such a relationship is thus far lacking. It appears that the phase adaptation of a number of circadian rhythms of physiologic importance in shift workers can be reinforced, delayed, or even prevented by the timing of food uptake in relation to the activity-rest pattern.

Internal desynchronization brought about by the independent alteration of two competing synchronizers may lead to functional or even organic disturbances, as has been suggested by a variety of problems, including the appearance of gastric ulcers in shift workers exposed to physiologically unacceptable alterations of their activity-rest pattern and the time of food uptake Carandente and Halberg, ; Gibinski et al.

The rhythmicity observed in the immune system is in part regulated by the multifrequency neuroendocrine rhythms that characterize the mammalian time structure and in some frequencies are environmentally synchronized for reviews, see, e. Interactions between the endocrine and the immune system are found at every level from the hypothalamic nuclei to the receptors in the cells of the target organs for reviews, see Auernhammer and Strasburger, ; Besedovsky and Del Rey, ; Blalock, ; Daynes et al.

The same classes of receptors as found in neural tissue have been identified on cells of the immune system Carr, ACTH and endorphins inhibit antibody production Johnson et al. In turn, mouse and human lymphocytes produce POMC-derived peptides, including ACTH, which are biologically active Blalock, , , as shown by the rise in corticosterone found in hypophysectomized animals exposed to infectious agents Bayle et al.

This effect was abolished in chicken if B-lymphocytes were deleted by bursectomy Bayle et al. Although the lymphocyte-produced hormones usually do not reach concentrations in the circulation that allow their measurement, their local production in an auto- or paracrine manner by cells of the immune system at the site of an immune process or inflammation can lead to immunomodulation Johnson et al.

At the present time, no information is available on the periodicity of hormone production by activated cells of the immune system, although some of these cells seem to respond to humoral neuroendocrine controls like CRF or ACTH. Glucocorticoids exert their powerful anti-inflammatory actions in part by downregulating the transcription of inflammatory mediators Russo, , including the cytokines IL-1 Kern et al. The large-amplitude circadian rhythm in plasma cortisol concentration in humans with peak values in the early morning hours in diurnally active subjects has been related to changes in immune response, with the minimum in response corresponding to the peak in cortisol concentrations Lee et al.

This same association has been observed for the circadian rhythm in plasma corticosterone in nocturnal rodents, which exhibit peak corticosterone values at the end of the daily light span and the beginning of the dark span. The anti-inflammatory action of cortisol is balanced at any one time by the immunostimulatory hormones, including GH, PRL, and melatonin Hooghe et al. The circadian rhythmicity in immune response appears to be, to a large extent, the net result of the balance at any one time between the immunosuppressive effect of glucocorticoids and the effect of immunostimulant hormones modulated by cytokine feedback and peripheral hormone production by cells of the immune system Weigent and Blalock, Immunomodulation also occurs at the target tissue level with selectivity of hormone effects and temporal variations due to the activity of specific enzyme systems metabolizing and transforming hormones at the level of the target cells.

DHEA modulates the immune response in lymphoid tissue after antigen exposure Daynes et al. Its decreased production e. The poor response of immunosenescent elderly subjects to vaccination Schwab et al. When aged animals were given oral supplementation with DHEA-S, the usual mature adult pattern of inducible T-cell lymphokines was restored, and a solid humoral immune response was obtained Daynes and Araneo, ; Garg and Bondada, Similarly, the direct incorporation of DHEA or DHEA-S into a protein vaccine formulation was found to promote the development of a strong immune response in age-compromised hosts Araneo et al.

There is a high-amplitude circadian rhythm of DHEA, which in its timing is comparable to that of cortisol Haus et al. In contrast, DHEA-S in humans characteristically shows a more flat circadian variation, with a peak later during the day Haus et al. DHEA-S also shows a circannual rhythm, which in its amplitude may be equal to or higher than that of the circadian rhythm Haus et al. No data are available relating these rhythmic variations in adrenal androgens to circadian or circannual changes in the immune system.

The serum PRL concentration shows a large-amplitude circadian rhythm, with peak values during the night hours Haus et al. This rhythm is modulated by a marked seasonal variation found in women but not in men. Haus et al. Also ethnic-geographic differences in the circadian and circannual amplitudes of PRL concentrations have been reported Haus et al. The circadian variation in plasma PRL concentrations is modulated by sleep but to a lesser degree than that of growth hormone hGH.

PRL is a major immunoregulating hormone. In animal experiments, hypophysectomy or suppression of PRL secretion by the dihydroxyphenylalanine DOPA agonist bromocryptine leads to a state of immunodeficiency with decreased resistance to infection, which can be reversed by treatment with PRL Bernton et al. Cyclosporine, an immunosuppressive fungal peptide, inhibits PRL binding to T-lymphocytes Hiestand et al.

Stimulation of PRL secretion can reverse the immunosuppression induced by cyclosporine Hiestand et al. The unbalanced prevalence of proinflammatory hormones like PRL and GH over the anti-inflammatory regulators like the hormones of the HPA axis is thought to favor the development of chronic inflammatory and autoimmune diseases like rheumatoid arthritis Berczi et al. Improvement of autoimmune uveitis occurred in patients treated for unrelated conditions with bromocryptine Hedner and Bynke, , an observation that seemed to be supported by observations in an animal model Palestine et al.

The relapse in patients with rheumatoid arthritis often seen after childbirth may be related to the high serum PRL concentrations encountered at this time Wilder, Events that affect PRL secretion, like chronic stress and sleep deprivation as experienced in military situations, and also the administration of many pharmacotherapeutic agents that are known to alter the secretion of PRL e. GH shows a marked circadian rhythm that is largely but not exclusively related to sleep, with a major spike in hormone secretion after sleep onset and a decrease in peak height reported during aging.

Sleep deprivation and irregular sleep-wakefulness patterns alter this rhythm through the "masking" effect of sleep. Receptors for GH have been found on immunocompetent cells, many of which also show receptors for growth hormone-releasing hormone GHRH for. IGF-I shows a low-amplitude circadian rhythm Haus et al. The local production of hGH and IGF-I, with the autocrine and paracrine effects of these factors on the immune system, may be at least as important as the circulating hormone concentrations. Melatonin represents an important endogenous immunomodulating agent Maestroni, that has been shown to amplify the immune effects of IL-2 and reduce its toxicity Lissoni et al.

Melatonin activates human monocytes and induces their cytotoxic properties along with IL-1 secretion Morrey et al. Especially the Th2 variant of T-helper cells is a target of the circadian melatonin signal. Immune competent cells like macrophages and their predecessors, monocytes, can also synthesize melatonin and serotonin from tryptophan in peripheral blood and tissues Finocchiaro et al.

The pineal-immune axis helps to maintain the Th1-Th2 balance, which is instrumental in developing a successful and balanced immune response. Melatonin can augment the immune response and correct these immunodeficiency states and those that may follow acute stress, viral diseases, or immunosuppressive drug treatment and those found during the process of aging Maestroni and Conti, In experimental autoimmune disorders, melatonin acts as an immune stimulant during the development of the disease and accentuates its severity Hansson et al.

The effects of melatonin and of drugs acting on melatonin synthesis are strictly circadian time dependent. Similarly, immune enhancement by melatonin in intact animals was found only when melatonin was injected during the late afternoon or evening Maestroni et al.

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Melatonin given in the morning was either ineffective or even immunosuppressive Maestroni et al. TSH shows a high-amplitude circadian rhythm and seasonal variation, presumably at least in part as a response to environmental temperature Haus et al. TSH was reported to augment both T-dependent and T-independent antibody production Blalock, , to increase the proliferative response of mouse lymphocytes to lectin mitogens, and to stimulate ILinduced NK cell activity Provinciali et al. TRH induces TSH production by lymphocytes and its effect on the immune system may be mediated by this mechanism Kruger et al.

Prolonged, hard, physical exercise combined with sleep and energy deprivation as experienced, for example, during military training courses may lead to rhythm alterations of numerous neuroendocrine variables interacting with the immune system Opstad, , Severe physical exercise together with sleep deprivation maintained throughout a span of 5 days leads to partial and, for some of the neuroendocrine variables, complete disappearance of circadian rhythmicity as a group phenomenon Opstad, This observation may be due to actual disappearance of a recognizable circadian rhythm due to the severe stress masking or due to a desynchronization among the members of the group studied.

Some changes e. Since optimal function in the human body depends on the "right" sequence of events as expressed by a certain phase relation "internal timing" of the biologic rhythms within a frequency range, a disruption of this sequence that results in the right metabolite not being provided at the right time may lead to malfunction and immune deficiencies, as seen during exposures to phase shift, sleep deprivation, severe stress, and other.

Some of these exposures may be unavoidable in a military setting, but they should be recognized as a problem for soldiers and should be included, wherever feasible, in the planning for military deployment and action. The rhythmicity of events in the immune system and in related functions provides an opportunity to predict the time when certain events are most likely to occur and allows the recognition of transient risk states for immune-related phenomena e. The prediction of such risk states allows one to initiate preventive measures or to treat an immune-related disorder at a time when optimal effects can be obtained.

Both the time-dependent changes in the pharmacokinetics of an agent chronopharmacokinetics and the time-dependent changes in the host response chronopharmacodynamics must be considered in the design of a chronotherapeutic treatment schedule Wood and Hrushesky, Fox, a; Maini et al. Immunosuppression by corticosteroids in patients with kidney allografts was most effective and accompanied by the fewest side effects if the dosing occurred in the morning, as compared with groups of patients taking the drug in the evening or throughout the day Knapp et al. The toxic effects of immunosuppressive drugs are still a major obstacle for use in human subjects Shaw et al.

Seasonal as well as circadian variations in the toxicity of chemotherapeutic agents were found for epirubicin and for doxorubicin Mormont et al. Manipulation of the feeding schedule in mice was shown to alter the circadian rhythm in toxicity of adriamycin Halberg, and of the immunosuppressant chemotherapeutic agent, methotrexate Song et al. In animal experiments, the timing of cyclosporine treatment, according to the circadian, circaseptan, and circannual rhythm of the toxicity of this agent, led to a substantial improvement of the toxic-therapeutic ratio and of the survival of the allografted animals Liu et al.

In human subjects, cyclosporine shows a circadian rhythm in its pharmacokinetics after oral dosing Ohlman et al. Peak plasma concentrations were found in the early morning hours, between , and the lowest values between and Heifets et al. The lowest rate of drug clearance occurred early in the morning, and the highest rate occurred in the afternoon. Monitoring of drug levels was recommended during the morning hours around — , which correspond to the nadir phase of the circadian variation of drug effect Heifets et al.

The importance of these findings for the therapeutic effect of cyclosporine in patients needs to be explored. The treatment with immunosuppressive agents can be timed for the stages in the circadian or other rhythms in the immune system either to achieve maximal immunosuppression with a minimal dose of the agent or to minimize immunosuppression if other effects of the agents are desired. Further exploration of the time structure of the immune system will provide the background for numerous chronotherapeutic applications to treatment with growth factors, cytokines, and their agonists and antagonists.

Immunoenhancement as well as immunosuppression can gain from chronotherapeutic consideration in dosing times Halberg and Halberg, ; Knapp et al. However, the observed changes were quantitative, and all subjects in these studies did achieve immunity irrespective of the circadian time of vaccination. Nevertheless, some investigators suggest that the timing of vaccination may have some importance in subjects with poor antibody formation. Abo, T. Kawate, K. Itoh, and K. Studies on the bioperiodicity of the immune response. Circadian rhythms of human T-, B-, and K-cell traffic in the peripheral blood.

Alevizatos, A. McKinney, and R. Live attenuated equine encephalomyelitis virus vaccine. Clinical response of man to immunization. Angeli, A. Gatti, M. Sartori, and R. Chronobiological aspects of the neuroendocrine immune network. Regulation of human natural killer NK cells as a model.

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Joseph Takahashi (UT Southwestern/HHMI) Part 2: Circadian Clocks: Genetics of Mammalian Clocks

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Endocrine regulation of circadian physiology

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