Sphinganine-1-phosphate protects kidney and liver after hepatic ischemia and reperfusion in mice through S1P1 receptor activation

Park, Sang Won; Kim, Mihwa; Chen, Sean W. C.; Brown, Kevin M.; D’Agati, Vivette D.; Lee, H Thomas

doi:10.1038/labinvest.2010.102

Cited by 63 publications

(60 citation statements)

References 53 publications

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“…S1P may serve a key function during the induction of torpor by regulating additional aspects of the immune system as well as other physiological changes that are not related primarily to immune function (30). Not only does S1P regulate the function of other types of leukocytes (31); it also is involved in other biological processes (32) and is implicated in governing protection against ischemia/reperfusion-induced injury in brain, heart, liver, and kidney (33)(34)(35)(36). Therapeutic hypothermia is used in patients with clinical conditions such as cardiac arrest and brain trauma and in patients undergoing cardiac or brain surgery because reducing cerebral metabolism has neuroprotective properties in periods of low oxygen supply (9).…”

Section: Discussionmentioning

confidence: 99%

Low body temperature governs the decline of circulating lymphocytes during hibernation through sphingosine-1-phosphate

Bouma¹,

Kroese

Kok

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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Hibernation is an energy-conserving behavior consisting of periods of inhibited metabolism ('torpor') with lowered body temperature. Torpor bouts are interspersed by arousal periods, in which metabolism increases and body temperature returns to euthermia. In deep torpor, the body temperature typically decreases to 2-10°C, and major physiological and immunological changes occur. One of these alterations constitutes an almost complete depletion of circulating lymphocytes that is reversed rapidly upon arousal. Here we show that torpor induces the storage of lymphocytes in secondary lymphoid organs in response to a temperature-dependent drop in plasma levels of sphingosine-1-phosphate (S1P). Regulation of lymphocyte numbers was mediated through the type 1 S1P receptor (S1P 1 ), because administration of a specific antagonist (W146) during torpor (in a Syrian hamster at ∼8°C) precluded restoration of lymphocyte numbers upon subsequent arousal. Furthermore, S1P release from erythrocytes via ATP-binding cassette (ABC)-transporters was significantly inhibited at low body temperature (4°C) but was restored upon rewarming. Reversible lymphopenia also was observed during daily torpor (in a Djungarian hamster at ± 25°C), during forced hypothermia in anesthetized (summer-active) hamsters (at ± 9°C), and in a nonhibernator (rat at ∼19°C). Our results demonstrate that lymphopenia during hibernation in small mammals is driven by body temperature, via altered plasma S1P levels. S1P is recognized as an important bioactive lipid involved in regulating several other physiological processes as well and may be an important factor regulating additional physiological processes in hibernation as well as in mediating the effects of therapeutic hypothermia in patients.ibernation is an energy-conserving behavior consisting of periods of significantly inhibited metabolism (torpor) that result in a largely reduced heart and ventilation rate (1-3) and body temperature. Torpor bouts are interspersed by arousal periods with durations of 8-24 h, during which metabolism increases and body temperature rapidly returns to euthermia (2, 4). Hibernating mammals display major changes in their physiology that lead (among other changes) to an increased resistance to ischemia/reperfusion (5, 6) and a reduced immune function (7). Remarkably, despite the repetitive cycles of cooling and rewarming, hibernating animals do not show gross signs of organ damage (8). In humans, therapeutic hypothermia is used frequently to limit neuronal injury in cardiac arrest and major surgery of brain and heart (9). However, hypothermia as used during cardiac surgery is associated with increased renal injury postoperatively (10). Therefore, unraveling the mechanisms underlying the changes in physiology of hibernating mammals might be of substantial clinical relevance.

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Section: Discussionmentioning

confidence: 99%

Low body temperature governs the decline of circulating lymphocytes during hibernation through sphingosine-1-phosphate

Bouma¹,

Kroese

Kok

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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“…We detected apoptosis after renal IR with terminal deoxynucleotidyl transferase dUTPmediated nick-end labeling (TUNEL) staining as described elsewhere (41) by using a commercially available in situ cell death detection kit (Roche, Indianapolis, IN) according to the instructions provided by the manufacturer. Kidney inflammation after renal IR was assessed by detection of neutrophil infiltration using immunohistochemistry 24 h after IR as described previously (41). Neutrophils infiltrating the kidney were quantified in 5-7 randomly chosen ϫ400 microscope image fields in the corticomedullary junction, and results are expressed as neutrophils counted per ϫ400 field.…”

Section: Methodsmentioning

confidence: 99%

Interleukin-11 protects against renal ischemia and reperfusion injury

Lee

Park

Kim

et al. 2012

American Journal of Physiology-Renal Physiology

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“…The expression and activity of sphingosine kinase have been detected in the kidneys (1, 10) and the mRNAs of S1P receptors are also present in the kidneys (17). It has been shown that S1P protects the kidneys from ischemic injury (2,27). It has also been demonstrated that S1P regulates vascular functions (14, 23).…”

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confidence: 99%

A novel lipid natriuretic factor in the renal medulla: sphingosine-1-phosphate

Zhu

Xia

Wang

et al. 2011

American Journal of Physiology-Renal Physiology

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Zhu Q, Xia M, Wang Z, Li P, Li N. A novel lipid natriuretic factor in the renal medulla: sphingosine-1-phosphate. Am J Physiol Renal Physiol 301: F35-F41, 2011. First published April 6, 2011 doi:10.1152/ajprenal.00014.2011.-Sphingosine-1-phosphate (S1P) is a bioactive sphingolipid metabolite formed by phosphorylation of sphingosine. S1P has been indicated to play a significant role in the cardiovascular system. It has been shown that the enzymes for S1P metabolism are expressed in the kidneys. The present study characterized the expression of S1P receptors in the kidneys and determined the role of S1P in the control of renal hemodynamics and sodium excretion. Real-time RT-PCR analyses showed that S1P receptors S1P1, S1P2, and S1P3 were most abundantly expressed in the renal medulla. Immunohistochemistry revealed that all three types of S1P receptors were mainly located in collecting ducts. Intramedullary infusion of FTY720, an S1P agonist, produced a dramatic increase in sodium excretion by twofold and a small but significant increase in medullary blood flow (16%). Administration of W146, an S1P1 antagonist, into the renal medulla blocked the effect of FTY720 and decreased the sodium excretion by 37% when infused alone. The antagonists of S1P2 and S1P3 had no effect. FTY720 produced additive natriuretic effects in combination with different sodium transporter inhibitors except amiloride, an epithelial sodium channel blocker. In the presence of nitric oxide synthase inhibitor L-NAME, FTY720 still increased sodium excretion. These data suggest that S1P produces natriuretic effects via activation of S1P1 in the renal medulla and this natriuretic effect may be through inhibition of epithelial sodium channel, which is nitric oxide independent. It is concluded that S1P is a novel diuretic factor in the renal medulla and may be an important regulator of sodium homeostasis. renal blood flow; sodium transporter; nitric oxide; collecting duct SPHINGOLIPIDS WERE ORIGINALLY thought to serve only as structural components of mammalian cell membranes. In recent years, sphingolipid metabolites are emerging as important lipid signaling molecules. Among them, sphingosine-1-phosphate (S1P) is known to play important roles in cellular processes in various organ systems including cardiovascular system and kidney (15,29). S1P is formed by phosphorylation of sphingosine catalyzed by sphingosine kinase and acts via its G protein-coupled receptors (17,29). Five members of S1P receptor family have been identified and termed S1P1-S1P5 (17, 29). The S1P1, S1P2, and S1P3 are ubiquitously expressed, while S1P4 is predominantly expressed in the lung and lymphoid system, and S1P5 is mainly in brain tissue (17,29). The expression and activity of sphingosine kinase have been detected in the kidneys (1, 10) and the mRNAs of S1P receptors are also present in the kidneys (17). It has been shown that S1P protects the kidneys from ischemic injury (2,27). It has also been demonstrated that S1P regulates vascular functions (14, 23). Therefore, it is p...

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Sphinganine-1-phosphate protects kidney and liver after hepatic ischemia and reperfusion in mice through S1P1 receptor activation

Cited by 63 publications

References 53 publications

Low body temperature governs the decline of circulating lymphocytes during hibernation through sphingosine-1-phosphate

Low body temperature governs the decline of circulating lymphocytes during hibernation through sphingosine-1-phosphate

Interleukin-11 protects against renal ischemia and reperfusion injury

A novel lipid natriuretic factor in the renal medulla: sphingosine-1-phosphate

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