Open Access

The role of sphingolipid signalling in diabetes‑associated pathologies (Review)

  • Authors:
    • Mei Li Ng
    • Carol Wadham
    • Olga A. Sukocheva
  • View Affiliations

  • Published online on: January 11, 2017     https://doi.org/10.3892/ijmm.2017.2855
  • Pages: 243-252
  • Copyright: © Ng et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Sphingosine kinase (SphK) is an important signalling enzyme that catalyses the phosphorylation of sphingosine (Sph) to form sphingosine‑1‑phosphate (S1P). The multifunctional lipid, S1P binds to a family of five G protein-coupled receptors (GPCRs). As an intracellular second messenger, S1P activates key signalling cascades responsible for the maintenance of sphingolipid metabolism, and has been implicated in the progression of cancer, and the development of other inflammatory and metabolic diseases. SphK and S1P are critical molecules involved in the regulation of various cellular metabolic processes, such as cell proliferation, survival, apoptosis, adhesion and migration. There is strong evidence supporting the critical roles of SphK and S1P in the progression of diabetes mellitus, including insulin sensitivity and insulin secretion, pancreatic β‑cell apoptosis, and the development of diabetic inflammatory state. In this review, we summarise the current state of knowledge for SphK/S1P signalling effects, associated with the development of insulin resistance, pancreatic β‑cell death and the vascular complications of diabetes mellitus.

References

1 

Danaei G, Finucane MM, Lu Y, Singh GM, Cowan MJ, Paciorek CJ, Lin JK, Farzadfar F, Khang YH, Stevens GA, et al: Global Burden of Metabolic Risk Factors of Chronic Diseases Collaborating Group (Blood Glucose): National, regional, and global trends in fasting plasma glucose and diabetes prevalence since 1980: Systematic analysis of health examination surveys and epidemiological studies with 370 country-years and 2·7 million participants. Lancet. 378:31–40. 2011. View Article : Google Scholar : PubMed/NCBI

2 

Expert Committee on the Diagnosis and Classification of Diabetes Mellitus: Report of the expert committee on the diagnosis and classification of diabetes mellitus. Diabetes Care. 26(Suppl 1): S5–S20. 2003. View Article : Google Scholar

3 

Shao S, Yang Y, Yuan G, Zhang M and Yu X: Signaling molecules involved in lipid-induced pancreatic beta-cell dysfunction. DNA Cell Biol. 32:41–49. 2013. View Article : Google Scholar : PubMed/NCBI

4 

Newsholme P, Keane D, Welters HJ and Morgan NG: Life and death decisions of the pancreatic beta-cell: The role of fatty acids. Clin Sci (Lond). 112:27–42. 2007. View Article : Google Scholar

5 

Alemany R, van Koppen CJ, Danneberg K, Ter Braak M and Meyer zu Heringdorf D: Regulation and functional roles of sphingosine kinases. Naunyn Schmiedebergs Arch Pharmacol. 374:413–428. 2007. View Article : Google Scholar : PubMed/NCBI

6 

Van Brocklyn JR, Lee MJ, Menzeleev R, Olivera A, Edsall L, Cuvillier O, Thomas DM, Coopman PJ, Thangada S, Liu CH, et al: Dual actions of sphingosine-1-phosphate: Extracellular through the Gi-coupled receptor Edg-1 and intracellular to regulate proliferation and survival. J Cell Biol. 142:229–240. 1998. View Article : Google Scholar : PubMed/NCBI

7 

Olivera A and Spiegel S: Sphingosine-1-phosphate as second messenger in cell proliferation induced by PDGF and FCS mitogens. Nature. 365:557–560. 1993. View Article : Google Scholar : PubMed/NCBI

8 

Cuvillier O, Pirianov G, Kleuser B, Vanek PG, Coso OA, Gutkind S and Spiegel S: Suppression of ceramide-mediated programmed cell death by sphingosine-1-phosphate. Nature. 381:800–803. 1996. View Article : Google Scholar : PubMed/NCBI

9 

Pyne S, Chapman J, Steele L and Pyne NJ: Sphingomyelin-derived lipids differentially regulate the extracellular signal-regulated kinase 2 (ERK-2) and c-Jun N-terminal kinase (JNK) signal cascades in airway smooth muscle. Eur J Biochem. 237:819–826. 1996. View Article : Google Scholar : PubMed/NCBI

10 

Qi Y, Chen J, Lay A, Don A, Vadas M and Xia P: Loss of sphingosine kinase 1 predisposes to the onset of diabetes via promoting pancreatic β-cell death in diet-induced obese mice. FASEB J. 27:4294–4304. 2013. View Article : Google Scholar : PubMed/NCBI

11 

Holland WL, Brozinick JT, Wang LP, Hawkins ED, Sargent KM, Liu Y, Narra K, Hoehn KL, Knotts TA, Siesky A, et al: Inhibition of ceramide synthesis ameliorates glucocorticoid-, saturated-fat-, and obesity-induced insulin resistance. Cell Metab. 5:167–179. 2007. View Article : Google Scholar : PubMed/NCBI

12 

Bruce CR, Risis S, Babb JR, Yang C, Kowalski GM, Selathurai A, Lee-Young RS, Weir JM, Yoshioka K, Takuwa Y, et al: Overexpression of sphingosine kinase 1 prevents ceramide accumulation and ameliorates muscle insulin resistance in high-fat diet-fed mice. Diabetes. 61:3148–3155. 2012. View Article : Google Scholar : PubMed/NCBI

13 

Spiegel S and Milstien S: The outs and the ins of sphingosine-1-phosphate in immunity. Nat Rev Immunol. 11:403–415. 2011. View Article : Google Scholar : PubMed/NCBI

14 

Pyne S and Pyne NJ: Translational aspects of sphingosine 1-phosphate biology. Trends Mol Med. 17:463–472. 2011. View Article : Google Scholar : PubMed/NCBI

15 

Maceyka M and Spiegel S: Sphingolipid metabolites in inflammatory disease. Nature. 510:58–67. 2014. View Article : Google Scholar : PubMed/NCBI

16 

Mendelson K, Evans T and Hla T: Sphingosine 1-phosphate signalling. Development. 141:5–9. 2014. View Article : Google Scholar :

17 

Hla T and Dannenberg AJ: Sphingolipid signaling in metabolic disorders. Cell Metab. 16:420–434. 2012. View Article : Google Scholar : PubMed/NCBI

18 

Pitson SM: Regulation of sphingosine kinase and sphingolipid signaling. Trends Biochem Sci. 36:97–107. 2011. View Article : Google Scholar

19 

Don AS and Rosen H: A lipid binding domain in sphingosine kinase 2. Biochem Biophys Res Commun. 380:87–92. 2009. View Article : Google Scholar : PubMed/NCBI

20 

Barr RK, Lynn HE, Moretti PA, Khew-Goodall Y and Pitson SM: Deactivation of sphingosine kinase 1 by protein phosphatase 2A. J Biol Chem. 283:34994–35002. 2008. View Article : Google Scholar : PubMed/NCBI

21 

Sutherland CM, Moretti PA, Hewitt NM, Bagley CJ, Vadas MA and Pitson SM: The calmodulin-binding site of sphingosine kinase and its role in agonist-dependent translocation of sphingosine kinase 1 to the plasma membrane. J Biol Chem. 281:11693–11701. 2006. View Article : Google Scholar : PubMed/NCBI

22 

Hait NC, Allegood J, Maceyka M, Strub GM, Harikumar KB, Singh SK, Luo C, Marmorstein R, Kordula T, Milstien S and Spiegel S: Regulation of histone acetylation in the nucleus by sphingosine-1-phosphate. Science. 325:1254–1257. 2009. View Article : Google Scholar : PubMed/NCBI

23 

Wattenberg BW, Pitson SM and Raben DM: The sphingosine and diacylglycerol kinase superfamily of signaling kinases: Localization as a key to signaling function. J Lipid Res. 47:1128–1139. 2006. View Article : Google Scholar : PubMed/NCBI

24 

Leclercq TM and Pitson SM: Cellular signalling by sphingosine kinase and sphingosine 1-phosphate. IUBMB Life. 58:467–472. 2006. View Article : Google Scholar : PubMed/NCBI

25 

Giussani P, Maceyka M, Le Stunff H, Mikami A, Lépine S, Wang E, Kelly S, Merrill AH Jr, Milstien S and Spiegel S: Sphingosine-1-phosphate phosphohydrolase regulates endoplasmic reticulum-to-golgi trafficking of ceramide. Mol Cell Biol. 26:5055–5069. 2006. View Article : Google Scholar : PubMed/NCBI

26 

Pitson SM, Moretti PA, Zebol JR, Lynn HE, Xia P, Vadas MA and Wattenberg BW: Activation of sphingosine kinase 1 by ERK1/2-mediated phosphorylation. EMBO J. 22:5491–5500. 2003. View Article : Google Scholar : PubMed/NCBI

27 

Stahelin RV, Hwang JH, Kim JH, Park ZY, Johnson KR, Obeid LM and Cho W: The mechanism of membrane targeting of human sphingosine kinase 1. J Biol Chem. 280:43030–43038. 2005. View Article : Google Scholar : PubMed/NCBI

28 

Siow D and Wattenberg B: The compartmentalization and trans-location of the sphingosine kinases: Mechanisms and functions in cell signaling and sphingolipid metabolism. Crit Rev Biochem Mol Biol. 46:365–375. 2011. View Article : Google Scholar : PubMed/NCBI

29 

Maceyka M, Sankala H, Hait NC, Le Stunff H, Liu H, Toman R, Collier C, Zhang M, Satin LS, Merrill AH Jr, et al: SphK1 and SphK2, sphingosine kinase isoenzymes with opposing functions in sphingolipid metabolism. J Biol Chem. 280:37118–37129. 2005. View Article : Google Scholar : PubMed/NCBI

30 

Ding G, Sonoda H, Yu H, Kajimoto T, Goparaju SK, Jahangeer S, Okada T and Nakamura S: Protein kinase D-mediated phosphorylation and nuclear export of sphingosine kinase 2. J Biol Chem. 282:27493–27502. 2007. View Article : Google Scholar : PubMed/NCBI

31 

Igarashi N, Okada T, Hayashi S, Fujita T, Jahangeer S and Nakamura S: Sphingosine kinase 2 is a nuclear protein and inhibits DNA synthesis. J Biol Chem. 278:46832–46839. 2003. View Article : Google Scholar : PubMed/NCBI

32 

Hait NC, Bellamy A, Milstien S, Kordula T and Spiegel S: Sphingosine kinase type 2 activation by ERK-mediated phosphorylation. J Biol Chem. 282:12058–12065. 2007. View Article : Google Scholar : PubMed/NCBI

33 

Alvarez SE, Milstien S and Spiegel S: Autocrine and paracrine roles of sphingosine-1-phosphate. Trends Endocrinol Metab. 18:300–307. 2007. View Article : Google Scholar : PubMed/NCBI

34 

Strub GM, Maceyka M, Hait NC, Milstien S and Spiegel S: Extracellular and intracellular actions of sphingosine-1-phosphate. Adv Exp Med Biol. 688:141–155. 2010. View Article : Google Scholar : PubMed/NCBI

35 

Venkataraman K, Thangada S, Michaud J, Oo ML, Ai Y, Lee YM, Wu M, Parikh NS, Khan F, Proia RL and Hla T: Extracellular export of sphingosine kinase-1a contributes to the vascular S1P gradient. Biochem J. 397:461–471. 2006. View Article : Google Scholar : PubMed/NCBI

36 

Maceyka M, Harikumar KB, Milstien S and Spiegel S: Sphingosine-1-phosphate signaling and its role in disease. Trends Cell Biol. 22:50–60. 2012. View Article : Google Scholar :

37 

Xia P, Wang L, Moretti PA, Albanese N, Chai F, Pitson SM, D'Andrea RJ, Gamble JR and Vadas MA: Sphingosine kinase interacts with TRAF2 and dissects tumor necrosis factor-alpha signaling. J Biol Chem. 277:7996–8003. 2002. View Article : Google Scholar : PubMed/NCBI

38 

Artal-Sanz M and Tavernarakis N: Prohibitin and mitochondrial biology. Trends Endocrinol Metab. 20:394–401. 2009. View Article : Google Scholar : PubMed/NCBI

39 

Parham KA, Zebol JR, Tooley KL, Sun WY, Moldenhauer LM, Cockshell MP, Gliddon BL, Moretti PA, Tigyi G, Pitson SM and Bonder CS: Sphingosine 1-phosphate is a ligand for peroxisome proliferator-activated receptor-γ that regulates neoangiogenesis. FASEB J. 29:3638–3653. 2015. View Article : Google Scholar : PubMed/NCBI

40 

Panneer Selvam S, De Palma RM, Oaks JJ, Oleinik N, Peterson YK, Stahelin RV, Skordalakes E, Ponnusamy S, Garrett-Mayer E, Smith CD and Ogretmen B: Binding of the sphingolipid S1P to hTERT stabilizes telomerase at the nuclear periphery by allosterically mimicking protein phosphorylation. Sci Signal. 8:ra582015. View Article : Google Scholar : PubMed/NCBI

41 

Takasugi N, Sasaki T, Suzuki K, Osawa S, Isshiki H, Hori Y, Shimada N, Higo T, Yokoshima S, Fukuyama T, et al: BACE1 activity is modulated by cell-associated sphingosine-1-phosphate. J Neurosci. 31:6850–6857. 2011. View Article : Google Scholar : PubMed/NCBI

42 

Pyne S, Adams DR and Pyne NJ: Sphingosine 1-phosphate and sphingosine kinases in health and disease: Recent advances. Prog Lipid Res. 62:93–106. 2016. View Article : Google Scholar : PubMed/NCBI

43 

Fox TE, Bewley MC, Unrath KA, Pedersen MM, Anderson RE, Jung DY, Jefferson LS, Kim JK, Bronson SK, Flanagan JM, et al: Circulating sphingolipid biomarkers in models of type 1 diabetes. J Lipid Res. 52:509–517. 2011. View Article : Google Scholar :

44 

Tao C, Sifuentes A and Holland WL: Regulation of glucose and lipid homeostasis by adiponectin: Effects on hepatocytes, pancreatic β cells and adipocytes. Best Pract Res Clin Endocrinol Metab. 28:43–58. 2014. View Article : Google Scholar : PubMed/NCBI

45 

Osawa Y, Seki E, Kodama Y, Suetsugu A, Miura K, Adachi M, Ito H, Shiratori Y, Banno Y, Olefsky JM, et al: Acid sphingomyelinase regulates glucose and lipid metabolism in hepatocytes through AKT activation and AMP-activated protein kinase suppression. FASEB J. 25:1133–1144. 2011. View Article : Google Scholar :

46 

Kowalski GM, Kloehn J, Burch ML, Selathurai A, Hamley S, Bayol SA, Lamon S, Watt MJ, Lee-Young RS, McConville MJ and Bruce CR: Overexpression of sphingosine kinase 1 in liver reduces triglyceride content in mice fed a low but not high-fat diet. Biochim Biophys Acta. 1851:210–219. 2015. View Article : Google Scholar

47 

Lee SY, Hong IK, Kim BR, Shim SM, Sung Lee J, Lee HY, Soo Choi C, Kim BK and Park TS: Activation of sphingosine kinase 2 by endoplasmic reticulum stress ameliorates hepatic steatosis and insulin resistance in mice. Hepatology. 62:135–146. 2015. View Article : Google Scholar : PubMed/NCBI

48 

Boden G: Endoplasmic reticulum stress: Another link between obesity and insulin resistance/inflammation? Diabetes. 58:518–519. 2009. View Article : Google Scholar : PubMed/NCBI

49 

Boslem E, Meikle PJ and Biden TJ: Roles of ceramide and sphingolipids in pancreatic β-cell function and dysfunction. Islets. 4:177–187. 2012. View Article : Google Scholar : PubMed/NCBI

50 

Zhu Q, Shan X, Miao H, Lu Y, Xu J, You N, Liu C, Liao DF and Jin J: Acute activation of acid ceramidase affects cytokine-induced cytotoxicity in rat islet beta-cells. FEBS Lett. 583:2136–2141. 2009. View Article : Google Scholar : PubMed/NCBI

51 

Maedler K, Oberholzer J, Bucher P, Spinas GA and Donath MY: Monounsaturated fatty acids prevent the deleterious effects of palmitate and high glucose on human pancreatic beta-cell turnover and function. Diabetes. 52:726–733. 2003. View Article : Google Scholar : PubMed/NCBI

52 

Veluthakal R, Palanivel R, Zhao Y, McDonald P, Gruber S and Kowluru A: Ceramide induces mitochondrial abnormalities in insulin-secreting INS-1 cells: Potential mechanisms underlying ceramide-mediated metabolic dysfunction of the beta cell. Apoptosis. 10:841–850. 2005. View Article : Google Scholar : PubMed/NCBI

53 

Lupi R, Dotta F, Marselli L, Del Guerra S, Masini M, Santangelo C, Patané G, Boggi U, Piro S, Anello M, et al: Prolonged exposure to free fatty acids has cytostatic and pro-apoptotic effects on human pancreatic islets: Evidence that beta-cell death is caspase mediated, partially dependent on ceramide pathway, and Bcl-2 regulated. Diabetes. 51:1437–1442. 2002. View Article : Google Scholar : PubMed/NCBI

54 

Boslem E, MacIntosh G, Preston AM, Bartley C, Busch AK, Fuller M, Laybutt DR, Meikle PJ and Biden TJ: A lipidomic screen of palmitate-treated MIN6 β-cells links sphingolipid metabolites with endoplasmic reticulum (ER) stress and impaired protein trafficking. Biochem J. 435:267–276. 2011. View Article : Google Scholar : PubMed/NCBI

55 

Véret J, Coant N, Berdyshev EV, Skobeleva A, Therville N, Bailbé D, Gorshkova I, Natarajan V, Portha B and Le Stunff H: Ceramide synthase 4 and de novo production of ceramides with specific N-acyl chain lengths are involved in glucolipotoxicity-induced apoptosis of INS-1 β-cells. Biochem J. 438:177–189. 2011. View Article : Google Scholar

56 

Kelpe CL, Moore PC, Parazzoli SD, Wicksteed B, Rhodes CJ and Poitout V: Palmitate inhibition of insulin gene expression is mediated at the transcriptional level via ceramide synthesis. J Biol Chem. 278:30015–30021. 2003. View Article : Google Scholar : PubMed/NCBI

57 

Guo J, Qian Y, Xi X, Hu X, Zhu J and Han X: Blockage of ceramide metabolism exacerbates palmitate inhibition of pro-insulin gene expression in pancreatic beta-cells. Mol Cell Biochem. 338:283–290. 2010. View Article : Google Scholar : PubMed/NCBI

58 

Jessup CF, Bonder CS, Pitson SM and Coates PT: The sphingolipid rheostat: A potential target for improving pancreatic islet survival and function. Endocr Metab Immune Disord Drug Targets. 11:262–272. 2011. View Article : Google Scholar : PubMed/NCBI

59 

Shimizu H, Okajima F, Kimura T, Ohtani K, Tsuchiya T, Takahashi H, Kuwabara A, Tomura H, Sato K and Mori M: Sphingosine 1-phosphate stimulates insulin secretion in HIT-T 15 cells and mouse islets. Endocr J. 47:261–269. 2000. View Article : Google Scholar : PubMed/NCBI

60 

Rütti S, Ehses JA, Sibler RA, Prazak R, Rohrer L, Georgopoulos S, Meier DT, Niclauss N, Berney T, Donath MY, et al: Low- and high-density lipoproteins modulate function, apoptosis, and proliferation of primary human and murine pancreatic beta-cells. Endocrinology. 150:4521–4530. 2009. View Article : Google Scholar : PubMed/NCBI

61 

Mastrandrea LD, Sessanna SM and Laychock SG: Sphingosine kinase activity and sphingosine-1 phosphate production in rat pancreatic islets and INS-1 cells: Response to cytokines. Diabetes. 54:1429–1436. 2005. View Article : Google Scholar : PubMed/NCBI

62 

Véret J, Coant N, Gorshkova IA, Giussani P, Fradet M, Riccitelli E, Skobeleva A, Goya J, Kassis N, Natarajan V, et al: Role of palmitate-induced sphingoid base-1-phosphate biosynthesis in INS-1 β-cell survival. Biochim Biophys Acta. 1831:251–262. 2013. View Article : Google Scholar

63 

Zhao Z, Choi J, Zhao C and Ma ZA: FTY720 normalizes hyperglycemia by stimulating β-cell in vivo re-generation in db/db mice through regulation of cyclin D3 and p57 (KIP2). J Biol Chem. 287:5562–5573. 2012. View Article : Google Scholar

64 

Cantrell Stanford J, Morris AJ, Sunkara M, Popa GJ, Larson KL and Özcan S: Sphingosine 1-phosphate (S1P) regulates glucose-stimulated insulin secretion in pancreatic beta cells. J Biol Chem. 287:13457–13464. 2012. View Article : Google Scholar : PubMed/NCBI

65 

Holland WL, Miller RA, Wang ZV, Sun K, Barth BM, Bui HH, Davis KE, Bikman BT, Halberg N, Rutkowski JM, et al: Receptor-mediated activation of ceramidase activity initiates the pleiotropic actions of adiponectin. Nat Med. 17:55–63. 2011. View Article : Google Scholar

66 

Imasawa T, Koike K, Ishii I, Chun J and Yatomi Y: Blockade of sphingosine 1-phosphate receptor 2 signaling attenuates streptozotocin-induced apoptosis of pancreatic beta-cells. Biochem Biophys Res Commun. 392:207–211. 2010. View Article : Google Scholar : PubMed/NCBI

67 

Ma MM, Chen JL, Wang GG, Wang H, Lu Y, Li JF, Yi J, Yuan YJ, Zhang QW, et al: Sphingosine kinase 1 participates in insulin signalling and regulates glucose metabolism and homeostasis in KK/Ay diabetic mice. Diabetologia. 50:891–900. 2007. View Article : Google Scholar : PubMed/NCBI

68 

Wang J, Badeanlou L, Bielawski J, Ciaraldi TP and Samad F: Sphingosine kinase 1 regulates adipose proinflammatory responses and insulin resistance. Am J Physiol Endocrinol Metab. 306:E756–E768. 2014. View Article : Google Scholar : PubMed/NCBI

69 

Mikłosz A, Łukaszuk B, Baranowski M, Górski J and Chabowski A: Effects of inhibition of serine palmitoyltransferase (SPT) and sphingosine kinase 1 (SphK1) on palmitate induced insulin resistance in L6 myotubes. PLoS One. 8:e855472013. View Article : Google Scholar

70 

Rapizzi E, Taddei ML, Fiaschi T, Donati C, Bruni P and Chiarugi P: Sphingosine 1-phosphate increases glucose uptake through trans-activation of insulin receptor. Cell Mol Life Sci. 66:3207–3218. 2009. View Article : Google Scholar : PubMed/NCBI

71 

Rapizzi E, Donati C, Cencetti F, Nincheri P and Bruni P: Sphingosine 1-phosphate differentially regulates proliferation of C2C12 reserve cells and myoblasts. Mol Cell Biochem. 314:193–199. 2008. View Article : Google Scholar : PubMed/NCBI

72 

Takuwa N, Ohkura S, Takashima S, Ohtani K, Okamoto Y, Tanaka T, Hirano K, Usui S, Wang F, Du W, et al: S1P3-mediated cardiac fibrosis in sphingosine kinase 1 transgenic mice involves reactive oxygen species. Cardiovasc Res. 85:484–493. 2010. View Article : Google Scholar :

73 

Patel SA, Hoehn KL, Lawrence RT, Sawbridge L, Talbot NA, Tomsig JL, Turner N, Cooney GJ, Whitehead JP, Kraegen EW and Cleasby ME: Overexpression of the adiponectin receptor AdipoR1 in rat skeletal muscle amplifies local insulin sensitivity. Endocrinology. 153:5231–5246. 2012. View Article : Google Scholar : PubMed/NCBI

74 

Zhang W, Mottillo EP, Zhao J, Gartung A, VanHecke GC, Lee JF, Maddipati KR, Xu H, Ahn YH, Proia RL, et al: Adipocyte lipolysis-stimulated interleukin-6 production requires sphingosine kinase 1 activity. J Biol Chem. 289:32178–32185. 2014. View Article : Google Scholar : PubMed/NCBI

75 

Tous M, Ferrer-Lorente R and Badimon L: Selective inhibition of sphingosine kinase-1 protects adipose tissue against LPS-induced inflammatory response in Zucker diabetic fatty rats. Am J Physiol Endocrinol Metab. 307:E437–E446. 2014. View Article : Google Scholar : PubMed/NCBI

76 

Janes K, Little JW, Li C, Bryant L, Chen C, Chen Z, Kamocki K, Doyle T, Snider A, Esposito E, et al: The development and maintenance of paclitaxel-induced neuropathic pain require activation of the sphingosine 1-phosphate receptor subtype 1. J Biol Chem. 289:21082–21097. 2014. View Article : Google Scholar : PubMed/NCBI

77 

Guan H, Song L, Cai J, Huang Y, Wu J, Yuan J, Li J and Li M: Sphingosine kinase 1 regulates the Akt/FOXO3a/Bim pathway and contributes to apoptosis resistance in glioma cells. PLoS One. 6:e199462011. View Article : Google Scholar : PubMed/NCBI

78 

Abuhusain HJ, Matin A, Qiao Q, Shen H, Kain N, Day BW, Stringer BW, Daniels B, Laaksonen MA, Teo C, et al: A metabolic shift favoring sphingosine 1-phosphate at the expense of ceramide controls glioblastoma angiogenesis. J Biol Chem. 288:37355–37364. 2013. View Article : Google Scholar : PubMed/NCBI

79 

Xie B, Shen J, Dong A, Rashid A, Stoller G and Campochiaro PA: Blockade of sphingosine-1-phosphate reduces macrophage influx and retinal and choroidal neovascularization. J Cell Physiol. 218:192–198. 2009. View Article : Google Scholar

80 

Maines LW, French KJ, Wolpert EB, Antonetti DA and Smith CD: Pharmacologic manipulation of sphingosine kinase in retinal endothelial cells: Implications for angiogenic ocular diseases. Invest Ophthalmol Vis Sci. 47:5022–5031. 2006. View Article : Google Scholar : PubMed/NCBI

81 

Lan T, Liu W, Xie X, Xu S, Huang K, Peng J, Shen X, Liu P, Wang L, Xia P and Huang H: Sphingosine kinase-1 pathway mediates high glucose-induced fibronectin expression in glomerular mesangial cells. Mol Endocrinol. 25:2094–2105. 2011. View Article : Google Scholar : PubMed/NCBI

82 

Liu Y: Renal fibrosis: New insights into the pathogenesis and therapeutics. Kidney Int. 69:213–217. 2006. View Article : Google Scholar : PubMed/NCBI

83 

Katsuma S, Hada Y, Ueda T, Shiojima S, Hirasawa A, Tanoue A, Takagaki K, Ohgi T, Yano J and Tsujimoto G: Signalling mechanisms in sphingosine 1-phosphate-promoted mesangial cell proliferation. Genes Cells. 7:1217–1230. 2002. View Article : Google Scholar : PubMed/NCBI

84 

Klawitter S, Hofmann LP, Pfeilschifter J and Huwiler A: Extracellular nucleotides induce migration of renal mesangial cells by upregulating sphingosine kinase-1 expression and activity. Br J Pharmacol. 150:271–280. 2007. View Article : Google Scholar : PubMed/NCBI

85 

Xin C, Ren S, Kleuser B, Shabahang S, Eberhardt W, Radeke H, Schäfer-Korting M, Pfeilschifter J and Huwiler A: Sphingosine 1-phosphate cross-activates the Smad signaling cascade and mimics transforming growth factor-beta-induced cell responses. J Biol Chem. 279:35255–35262. 2004. View Article : Google Scholar : PubMed/NCBI

86 

Yaghobian D, Don AS, Yaghobian S, Chen X, Pollock CA and Saad S: Increased sphingosine 1-phosphate mediates inflammation and fibrosis in tubular injury in diabetic nephropathy. Clin Exp Pharmacol Physiol. 43:56–66. 2016. View Article : Google Scholar

87 

Spiegel S and Milstien S: Sphingosine-1-phosphate: An enigmatic signalling lipid. Nat Rev Mol Cell Biol. 4:397–407. 2003. View Article : Google Scholar : PubMed/NCBI

88 

Geoffroy K, Troncy L, Wiernsperger N, Lagarde M and El Bawab S: Glomerular proliferation during early stages of diabetic nephropathy is associated with local increase of sphingosine-1-phosphate levels. FEBS Lett. 579:1249–1254. 2005. View Article : Google Scholar : PubMed/NCBI

89 

Lan T, Shen X, Liu P, Liu W, Xu S, Xie X, Jiang Q, Li W and Huang H: Berberine ameliorates renal injury in diabetic C57BL/6 mice: Involvement of suppression of SphK-S1P signaling pathway. Arch Biochem Biophys. 502:112–120. 2010. View Article : Google Scholar : PubMed/NCBI

90 

Huang K, Huang J, Chen C, Hao J, Wang S, Huang J, Liu P and Huang H: AP-1 regulates sphingosine kinase 1 expression in a positive feedback manner in glomerular mesangial cells exposed to high glucose. Cell Signal. 26:629–638. 2014. View Article : Google Scholar

91 

Liu W, Lan T, Xie X, Huang K, Peng J, Huang J, Shen X, Liu P and Huang H: S1P2 receptor mediates sphingosine-1-phosphate-induced fibronectin expression via MAPK signaling pathway in mesangial cells under high glucose condition. Exp Cell Res. 318:936–943. 2012. View Article : Google Scholar : PubMed/NCBI

92 

Imasawa T, Kitamura H, Ohkawa R, Satoh Y, Miyashita A and Yatomi Y: Unbalanced expression of sphingosine 1-phosphate receptors in diabetic nephropathy. Exp Toxicol Pathol. 62:53–60. 2010. View Article : Google Scholar

93 

Xia P, Wang L, Gamble JR and Vadas MA: Activation of sphingosine kinase by tumor necrosis factor-alpha inhibits apoptosis in human endothelial cells. J Biol Chem. 274:34499–34505. 1999. View Article : Google Scholar : PubMed/NCBI

94 

Vessey DA, Kelley M, Li L, Huang Y, Zhou HZ, Zhu BQ and Karliner JS: Role of sphingosine kinase activity in protection of heart against ischemia reperfusion injury. Med Sci Monit. 12:BR318–BR324. 2006.PubMed/NCBI

95 

Jin ZQ and Karliner JS: Low dose N, N-dimethylsphingosine is cardioprotective and activates cytosolic sphingosine kinase by a PKCepsilon dependent mechanism. Cardiovasc Res. 71:725–734. 2006. View Article : Google Scholar : PubMed/NCBI

96 

Jin ZQ, Goetzl EJ and Karliner JS: Sphingosine kinase activation mediates ischemic preconditioning in murine heart. Circulation. 110:1980–1989. 2004. View Article : Google Scholar : PubMed/NCBI

97 

Besler C, Heinrich K, Rohrer L, Doerries C, Riwanto M, Shih DM, Chroni A, Yonekawa K, Stein S, Schaefer N, et al: Mechanisms underlying adverse effects of HDL on eNOS-activating pathways in patients with coronary artery disease. J Clin Invest. 121:2693–2708. 2011. View Article : Google Scholar : PubMed/NCBI

98 

Park SW, Kim M, Kim JY, Brown KM, Haase VH, D'Agati VD and Lee HT: Proximal tubule sphingosine kinase-1 has a critical role in A1 adenosine receptor-mediated renal protection from ischemia. Kidney Int. 82:878–891. 2012. View Article : Google Scholar : PubMed/NCBI

99 

Paneni F, Beckman JA, Creager MA and Cosentino F: Diabetes and vascular disease: Pathophysiology, clinical consequences, and medical therapy: Part I. Eur Heart J. 34:2436–2443. 2013. View Article : Google Scholar : PubMed/NCBI

100 

Grundy SM, Benjamin IJ, Burke GL, Chait A, Eckel RH, Howard BV, Mitch W, Smith SC Jr and Sowers JR: Diabetes and cardiovascular disease: A statement for healthcare professionals from the American Heart Association. Circulation. 100:1134–1146. 1999. View Article : Google Scholar : PubMed/NCBI

101 

Schnell O, Cappuccio F, Genovese S, Standl E, Valensi P and Ceriello A: Type 1 diabetes and cardiovascular disease. Cardiovasc Diabetol. 12:1562013. View Article : Google Scholar : PubMed/NCBI

102 

Fioretto P, Dodson PM, Ziegler D and Rosenson RS: Residual microvascular risk in diabetes: Unmet needs and future directions. Nat Rev Endocrinol. 6:19–25. 2010. View Article : Google Scholar

103 

Rosenberg DE, Jabbour SA and Goldstein BJ: Insulin resistance, diabetes and cardiovascular risk: Approaches to treatment. Diabetes Obes Metab. 7:642–653. 2005. View Article : Google Scholar : PubMed/NCBI

104 

Li H, Horke S and Förstermann U: Vascular oxidative stress, nitric oxide and atherosclerosis. Atherosclerosis. 237:208–219. 2014. View Article : Google Scholar : PubMed/NCBI

105 

Keul P, Sattler K and Levkau B: HDL and its sphingosine-1-phosphate content in cardioprotection. Heart Fail Rev. 12:301–306. 2007. View Article : Google Scholar : PubMed/NCBI

106 

Karliner JS: Sphingosine kinase regulation and cardioprotection. Cardiovasc Res. 82:184–192. 2009. View Article : Google Scholar :

107 

Karliner JS: Sphingosine kinase and sphingosine 1-phosphate in the heart: A decade of progress. Biochim Biophys Acta. 1831:203–212. 2013. View Article : Google Scholar

108 

Whetzel AM, Bolick DT and Hedrick CC: Sphingosine-1-phosphate inhibits high glucose-mediated ERK1/2 action in endothelium through induction of MAP kinase phosphatase-3. Am J Physiol Cell Physiol. 296:C339–C345. 2009. View Article : Google Scholar :

109 

Whetzel AM, Bolick DT, Srinivasan S, Macdonald TL, Morris MA, Ley K and Hedrick CC: Sphingosine-1 phosphate prevents monocyte/endothelial interactions in type 1 diabetic NOD mice through activation of the S1P1 receptor. Circ Res. 99:731–739. 2006. View Article : Google Scholar : PubMed/NCBI

110 

Khafaji HA and Suwaidi JM: Atypical presentation of acute and chronic coronary artery disease in diabetics. World J Cardiol. 6:802–813. 2014. View Article : Google Scholar : PubMed/NCBI

111 

Jin ZQ, Karliner JS and Vessey DA: Ischaemic postconditioning protects isolated mouse hearts against ischaemia/reperfusion injury via sphingosine kinase isoform-1 activation. Cardiovasc Res. 79:134–140. 2008. View Article : Google Scholar : PubMed/NCBI

112 

Vessey DA, Kelley M, Li L and Huang Y: Sphingosine protects aging hearts from ischemia/reperfusion injury: Superiority to sphingosine 1-phosphate and ischemic pre- and post-conditioning. Oxid Med Cell Longev. 2:146–151. 2009. View Article : Google Scholar :

113 

Bonder CS, Sun WY, Matthews T, Cassano C, Li X, Ramshaw HS, Pitson SM, Lopez AF, Coates PT, Proia RL, et al: Sphingosine kinase regulates the rate of endothelial progenitor cell differentiation. Blood. 113:2108–2117. 2009. View Article : Google Scholar :

114 

Yu H, Yuan L, Xu M, Zhang Z and Duan H: Sphingosine kinase 1 improves cutaneous wound healing in diabetic rats. Injury. 45:1054–1058. 2014. View Article : Google Scholar : PubMed/NCBI

115 

Furuya H, Wada M, Shimizu Y, Yamada PM, Hannun YA, Obeid LM and Kawamori T: Effect of sphingosine kinase 1 inhibition on blood pressure. FASEB J. 27:656–664. 2013. View Article : Google Scholar :

116 

Igarashi J and Michel T: Sphingosine 1-phosphate and isoform-specific activation of phosphoinositide 3-kinase beta. Evidence for divergence and convergence of receptor-regulated endothelial nitric-oxide synthase signaling pathways. J Biol Chem. 276:36281–36288. 2001. View Article : Google Scholar : PubMed/NCBI

117 

De Palma C, Meacci E, Perrotta C, Bruni P and Clementi E: Endothelial nitric oxide synthase activation by tumor necrosis factor alpha through neutral sphingomyelinase 2, sphingosine kinase 1, and sphingosine 1 phosphate receptors: A novel pathway relevant to the pathophysiology of endothelium. Arterioscler Thromb Vasc Biol. 26:99–105. 2006. View Article : Google Scholar

118 

Yin Z, Fan L, Wei L, Gao H, Zhang R, Tao L, Cao F and Wang H: FTY720 protects cardiac microvessels of diabetes: A critical role of S1P1/3 in diabetic heart disease. PLoS One. 7:e429002012. View Article : Google Scholar : PubMed/NCBI

119 

Sukocheva O, Wadham C, Gamble J and Xia P: Sphingosine-1-phosphate receptor 1 transmits estrogens' effects in endothelial cells. Steroids. 104:237–245. 2015. View Article : Google Scholar : PubMed/NCBI

120 

Margolis KL, Bonds DE, Rodabough RJ, Tinker L, Phillips LS, Allen C, Bassford T, Burke G, Torrens J and Howard BV; Women's Health Initiative Investigators: Effect of oestrogen plus progestin on the incidence of diabetes in postmenopausal women: Results from the Women's Health Initiative Hormone Trial. Diabetologia. 47:1175–1187. 2004. View Article : Google Scholar : PubMed/NCBI

121 

Russo SB, Ross JS and Cowart LA: Sphingolipids in obesity, type 2 diabetes, and metabolic disease. Handb Exp Pharmacol. 216:373–401. 2013. View Article : Google Scholar

122 

Kontush A and Chapman MJ: Functionally defective high-density lipoprotein: A new therapeutic target at the crossroads of dyslipidemia, inflammation, and atherosclerosis. Pharmacol Rev. 58:342–374. 2006. View Article : Google Scholar : PubMed/NCBI

123 

Barter PJ, Puranik R and Rye KA: New insights into the role of HDL as an anti-inflammatory agent in the prevention of cardiovascular disease. Curr Cardiol Rep. 9:493–498. 2007. View Article : Google Scholar : PubMed/NCBI

124 

deGoma EM, deGoma RL and Rader DJ: Beyond high-density lipoprotein cholesterol levels evaluating high-density lipoprotein function as influenced by novel therapeutic approaches. J Am Coll Cardiol. 51:2199–2211. 2008. View Article : Google Scholar : PubMed/NCBI

125 

Levkau B: HDL-S1P: Cardiovascular functions, disease-associated alterations, and therapeutic applications. Front Pharmacol. 6:2432015. View Article : Google Scholar : PubMed/NCBI

126 

Tong X, Peng H, Liu D, Ji L, Niu C, Ren J, Pan B, Hu J, Zheng L and Huang Y: High-density lipoprotein of patients with type 2 diabetes mellitus upregulates cyclooxgenase-2 expression and prostacyclin I-2 release in endothelial cells: Relationship with HDL-associated sphingosine-1-phosphate. Cardiovasc Diabetol. 12:272013. View Article : Google Scholar : PubMed/NCBI

127 

Tong X, Lv P, Mathew AV, Liu D, Niu C, Wang Y, Ji L, Li J, Fu Z, Pan B, et al: The compensatory enrichment of sphingosine-1-phosphate harbored on glycated high-density lipoprotein restores endothelial protective function in type 2 diabetes mellitus. Cardiovasc Diabetol. 13:822014. View Article : Google Scholar

128 

Zhu D, Sreekumar PG, Hinton DR and Kannan R: Expression and regulation of enzymes in the ceramide metabolic pathway in human retinal pigment epithelial cells and their relevance to retinal degeneration. Vision Res. 50:643–651. 2010. View Article : Google Scholar :

129 

Mizugishi K, Yamashita T, Olivera A, Miller GF, Spiegel S and Proia RL: Essential role for sphingosine kinases in neural and vascular development. Mol Cell Biol. 25:11113–11121. 2005. View Article : Google Scholar : PubMed/NCBI

130 

Tsuji T, Inoue M, Yoshida Y, Fujita T, Kaino Y and Kohno T: Therapeutic approach for type 1 diabetes mellitus using the novel immunomodulator FTY720 (fingolimod) in combination with once-daily injection of insulin glargine in non-obese diabetic mice. J Diabetes Investig. 3:132–137. 2012. View Article : Google Scholar : PubMed/NCBI

131 

Gonzalez-Cabrera PJ, Brown S, Studer SM and Rosen H: S1P signaling: new therapies and opportunities. F1000Prime Rep. 6:1092014.

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February 2017
Volume 39 Issue 2

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APA
Ng, M.L., Wadham, C., & Sukocheva, O.A. (2017). The role of sphingolipid signalling in diabetes‑associated pathologies (Review). International Journal of Molecular Medicine, 39, 243-252. https://doi.org/10.3892/ijmm.2017.2855
MLA
Ng, M. L., Wadham, C., Sukocheva, O. A."The role of sphingolipid signalling in diabetes‑associated pathologies (Review)". International Journal of Molecular Medicine 39.2 (2017): 243-252.
Chicago
Ng, M. L., Wadham, C., Sukocheva, O. A."The role of sphingolipid signalling in diabetes‑associated pathologies (Review)". International Journal of Molecular Medicine 39, no. 2 (2017): 243-252. https://doi.org/10.3892/ijmm.2017.2855