Sphingosine 1-phosphate protects primary human keratinocytes from apoptosis via nitric oxide formation through the receptor subtype S1P3

Molecular and Cellular Biochemistry

Volumn 371, Issue 1-2, 2012, Pages 165-176

  Schmitz, Elisabeth I ^a,b   Potteck, Henrik ^b   Schüppel, Melanie ^b   Manggau, Marianti ^c   Wahydin, Elly ^c   Kleuser, Burkhard ^a  

^a UNIVERSITY OF POTSDAM   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c HASANUDDIN UNIVERSITY   (Indonesia)

Author keywords

Apoptosis; Endothelial nitric oxide synthase; Keratinocytes; Nitric oxide; S1P receptors; Sphingolipids; Sphingosine 1 phosphate

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; G PROTEIN COUPLED RECEPTOR; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRITE; RECEPTOR SUBTYPE; SMALL INTERFERING RNA; SPHINGOLIPID; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE 1 PHOSPHATE RECEPTOR;

APOPTOSIS; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; ENZYME ACTIVATION; FLOW CYTOMETRY; GENE SILENCING; HUMAN; HUMAN CELL; IC 50; IMMUNOFLUORESCENCE MICROSCOPY; KERATINOCYTE; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

APOPTOSIS; HUMANS; KERATINOCYTES; LYSOPHOSPHOLIPIDS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; RECEPTORS, LYSOSPHINGOLIPID; SIGNAL TRANSDUCTION; SPHINGOSINE;

EID: 84868545646     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-012-1433-5     Document Type: Article

References (70)

1. Jungersted JM, Scheer H, Mempel M, Baurecht H, Cifuentes L, Hogh JK, Hellgren LI, Jemec GB, Agner T, Weidinger S (2010) Stratum corneum lipids, skin barrier function and filaggrin mutations in patients with atopic eczema. Allergy 65:911-918
2. Choi H, Kim S, Kim HJ, Kim KM, Lee CH, Shin JH, Noh M (2010) Sphingosylphosphorylcholine down-regulates filaggrin gene transcription through NOX5-based NADPH oxidase and cyclooxygenase-2 in human keratinocytes. Biochem Pharmacol 80:95-103
3. Kim S, Hong I, Hwang JS, Choi JK, Rho HS, Kim DH, Chang I, Lee SH, Lee MO (2006) Phytosphingosine stimulates the differentiation of human keratinocytes and inhibits TPA-induced inflammatory epidermal hyperplasia in hairless mouse skin. Mol Med 12:17-24
4. Sandhoff R (2010) Very long chain sphingolipids: tissue expression, function and synthesis. FEBS Lett 584:1907-1913
5. Herzinger T, Kleuser B, Schafer-Korting M, Korting HC (2007) Sphingosine-1-phosphate signaling and the skin. Am J Clin Dermatol 8:329-336
6. Bektas M, Orfanos CE, Geilen CC (2000) Different vitamin D analogues induce sphingomyelin hydrolysis and apoptosis in the human keratinocyte cell line HaCaT. Cell Mol Biol (Noisy-le-grand) 46:111-119
7. Uchida Y, Murata S, Schmuth M, Behne MJ, Lee JD, Ichikawa S, Elias PM, Hirabayashi Y, Holleran WM (2002) Glucosylceramide synthesis and synthase expression protect against ceramide-induced stress. J Lipid Res 43:1293-1302
8. Schuppel M, Kurschner U, Kleuser U, Schafer-Korting M, Kleuser B (2008) Sphingosine 1-phosphate restrains insulin-mediated keratinocyte proliferation via inhibition of Akt through the S1P2 receptor subtype. J Invest Dermatol 128:1747-1756
9. Vogler R, Sauer B, Kim DS, Schafer-Korting M, Kleuser B (2003) Sphingosine-1-phosphate and its potentially paradoxical effects on critical parameters of cutaneous wound healing. J Invest Dermatol 120:693-700
10. Manggau M, Kim DS, Ruwisch L, Vogler R, Korting HC, Schafer-Korting M, Kleuser B (2001) 1Alpha, 25-dihydroxyvitamin D3 protects human keratinocytes from apoptosis by the formation of sphingosine-1-phosphate. J Invest Dermatol 117:1241-1249
11. Spiegel S, Milstien S (2011) The outs and the ins of sphingosine-1- phosphate in immunity. Nat Rev Immunol 11:403-415
12. Pyne NJ, Waters C, Moughal NA, Sambi BS, Pyne S (2003) Receptor tyrosine kinase-GPCR signal complexes. Biochem Soc Trans 31:1220-1225
13. Alvarez SE, Harikumar KB, Hait NC, Allegood J, Strub GM, Kim EY, Maceyka M, Jiang H, Luo C, Kordula T, Milstien S, Spiegel S (2010) Sphingosine-1- phosphate is a missing cofactor for the E3 ubiquitin ligase TRAF2. Nature 465:1084-1088
14. Hait NC, Allegood J, Maceyka M, Strub GM, Harikumar KB, Singh SK, Luo C, Marmorstein R, Kordula T, Milstien S, Spiegel S (2009) Regulation of histone acetylation in the nucleus by sphingosine-1-phosphate. Science 325:1254-1257
15. Nieuwenhuis B, Luth A, Chun J, Huwiler A, Pfeilschifter J, Schafer-Korting M, Kleuser B (2009) Involvement of the ABC-transporter ABCC1 and the sphingosine 1-phosphate receptor subtype S1P(3) in the cytoprotection of human fibroblasts by the glucocorticoid dexamethasone. J Mol Med (Berl) 87:645-657
16. Radeff-Huang J, Seasholtz TM, Matteo RG, Brown JH (2004) G protein mediated signaling pathways in lysophospholipid induced cell proliferation and survival. J Cell Biochem 92:949-966
17. Spiegel S, Milstien S (2003) Exogenous and intracellularly generated sphingosine 1-phosphate can regulate cellular processes by divergent pathways. Biochem Soc Trans 31:1216-1219
18. Cals-Grierson MM, Ormerod AD (2004) Nitric oxide function in the skin. Nitric Oxide 10:179-193
19. Weller R, Schwentker A, Billiar TR, Vodovotz Y (2003) Autologous nitric oxide protects mouse and human keratinocytes from ultraviolet B radiation-induced apoptosis. Am J Physiol Cell Physiol 284:C1140-C1148
20. Andrew PJ, Mayer B (1999) Enzymatic function of nitric oxide synthases. Cardiovasc Res 43:521-531
21. Marletta MA (1993) Nitric oxide synthase structure and mechanism. J Biol Chem 268:12231-12234
22. Geller DA, Billiar TR (1998) Molecular biology of nitric oxide synthases. Cancer Metastasis Rev 17:7-23
23. Kone BC, Kuncewicz T, Zhang W, Yu ZY (2003) Protein interactions with nitric oxide synthases: controlling the right time, the right place, and the right amount of nitric oxide. Am J Physiol Renal Physiol 285:F178-F190
24. Ikeyama K, Denda M (2010) Effect of endothelial nitric oxide synthase on epidermal permeability barrier recovery after disruption. Br J Dermatol 163:915-919
25. Ikeyama K, Denda S, Tsutsumi M, Denda M (2010) Neuronal nitric oxide synthase in epidermis is involved in cutaneous circulatory response to mechanical stimulation. J Invest Dermatol 130:1158-1166
26. Bruch-Gerharz D, Fehsel K, Suschek C, Michel G, Ruzicka T, Kolb-Bachofen V (1996) A proinflammatory activity of interleukin 8 in human skin: expression of the inducible nitric oxide synthase in psoriatic lesions and cultured keratinocytes. J Exp Med 184:2007-2012
27. Ormerod AD, Weller R, Copeland P, Benjamin N, Ralston SH, Grabowksi P, Herriot R (1998) Detection of nitric oxide and nitric oxide synthases in psoriasis. Arch Dermatol Res 290:3-8
28. Sirsjo A, Karlsson M, Gidlof A, Rollman O, Torma H (1996) Increased expression of inducible nitric oxide synthase in psoriatic skin and cytokine-stimulated cultured keratinocytes. Br J Dermatol 134:643-648
29. Hecker M, Cattaruzza M, Wagner AH (1999) Regulation of inducible nitric oxide synthase gene expression in vascular smooth muscle cells. Gen Pharmacol 32:9-16
30. Chung HT, Pae HO, Choi BM, Billiar TR, Kim YM (2001) Nitric oxide as a bioregulator of apoptosis. Biochem Biophys Res Commun 282:1075-1079
31. Dimmeler S, Zeiher AM (1997) Nitric oxide and apoptosis: another paradigm for the double-edged role of nitric oxide. Nitric Oxide 1:275-281
32. Fleming I, Fisslthaler B, Dimmeler S, Kemp BE, Busse R (2001) Phosphorylation of Thr(495) regulates Ca(2+)/calmodulin-dependent endothelial nitric oxide synthase activity. Circ Res 88:E68-E75
33. Li H, Wallerath T, Forstermann U (2002) Physiological mechanisms regulating the expression of endothelial-type NO synthase. Nitric Oxide 7:132-147
34. Sessa WC (2004) eNOS at a glance. J Cell Sci 117:2427-2429
35. Blot V, Jacquemard U, Reissig HU, Kleuser B (2009) Practical syntheses of sphingosine-1-phosphate and analogues. Synthesis 5:759-766
36. Yamaoka J, Sasaki M, Miyachi Y (2000) Ultraviolet B radiation downregulates inducible nitric oxide synthase expression induced by interferon-gamma or tumor necrosis factor-alpha in murine keratinocyte Pam 212 cells. Arch Dermatol Res 292:312-319
37. Salerno L, Sorrenti V, Di Giacomo C, Romeo G, Siracusa MA (2002) Progress in the development of selective nitric oxide synthase (NOS) inhibitors. Curr Pharm Des 8:177-200
38. Morales-Ruiz M, Lee MJ, Zollner S, Gratton JP, Scotland R, Shiojima I, Walsh K, Hla T, Sessa WC (2001) Sphingosine 1-phosphate activates Akt, nitric oxide production, and chemotaxis through a Gi protein/phosphoinositide 3-kinase pathway in endothelial cells. J Biol Chem 276:19672-19677
39. Tolle M, Levkau B, Keul P, Brinkmann V, Giebing G, Schonfelder G, Schafers M, von Wnuck Lipinski K, Jankowski J, Jankowski V, Chun J, Zidek W, Van der Giet M (2005) Immunomodulator FTY720 induces eNOS-dependent arterial vasodilatation via the lysophospholipid receptor S1P3. Circ Res 96:913-920
40. Bruch-Gerharz D, Ruzicka T, Kolb-Bachofen V (1998) Nitric oxide and its implications in skin homeostasis and diseasea review. Arch Dermatol Res 290:643-651
41. Weller R, Pattullo S, Smith L, Golden M, Ormerod A, Benjamin N (1996) Nitric oxide is generated on the skin surface by reduction of sweat nitrate. J Invest Dermatol 107:327-331
42. Lowes MA, Chamian F, Abello MV, Fuentes-Duculan J, Lin SL, Nussbaum R, Novitskaya I, Carbonaro H, Cardinale I, Kikuchi T, Gilleaudeau P, Sullivan-Whalen M, Wittkowski KM, Papp K, Garovoy M, Dummer W, Steinman RM, Krueger JG (2005) Increase in TNF-alpha and inducible nitric oxide synthase-expressing dendritic cells in psoriasis and reduction with efalizumab (anti-CD11a). Proc Natl Acad Sci USA 102:19057-19062
43. Massi D, Franchi A, Sardi I, Magnelli L, Paglierani M, Borgognoni L, Maria Reali U, Santucci M (2001) Inducible nitric oxide synthase expression in benign and malignant cutaneous melanocytic lesions. J Pathol 194:194-200
44. Kim YM, Bombeck CA, Billiar TR (1999) Nitric oxide as a bifunctional regulator of apoptosis. Circ Res 84:253-256
45. Yamaoka J, Kawana S, Miyachi Y (2004) Nitric oxide inhibits ultraviolet B-induced murine keratinocyte apoptosis by regulating apoptotic signaling cascades. Free Radic Res 38:943-950
46. Liu W, Wu S (2010) Differential roles of nitric oxide synthases in regulation of ultraviolet B light-induced apoptosis. Nitric Oxide 23:199-205
47. Albrecht EW, Stegeman CA, Heeringa P, Henning RH, van Goor H (2003) Protective role of endothelial nitric oxide synthase. J Pathol 199:8-17
48. Brouet A, Sonveaux P, Dessy C, Moniotte S, Balligand JL, Feron O (2001) Hsp90 and caveolin are key targets for the proangiogenic nitric oxide-mediated effects of statins. Circ Res 89:866-873
49. Duranski MR, Elrod JW, Calvert JW, Bryan NS, Feelisch M, Lefer DJ (2006) Genetic overexpression of eNOS attenuates hepatic ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 291:H2980-H2986
50. Gao F, Gao E, Yue TL, Ohlstein EH, Lopez BL, Christopher TA, Ma XL (2002) Nitric oxide mediates the antiapoptotic effect of insulin in myocardial ischemia-reperfusion: the roles of PI3-kinase, Akt, and endothelial nitric oxide synthase phosphorylation. Circulation 105:1497-1502
51. Lin LY, Lin CY, Ho FM, Liau CS (2005) Up-regulation of the association between heat shock protein 90 and endothelial nitric oxide synthase prevents high glucose-induced apoptosis in human endothelial cells. J Cell Biochem 94:194-201
52. Murphy PR, Limoges M, Dodd F, Boudreau RT, Too CK (2001) Fibroblast growth factor-2 stimulates endothelial nitric oxide synthase expression and inhibits apoptosis by a nitric oxide-dependent pathway in Nb2 lymphoma cells. Endocrinology 142:81-88
53. Prorock AJ, Hafezi-Moghadam A, Laubach VE, Liao JK, Ley K (2003) Vascular protection by estrogen in ischemia-reperfusion injury requires endothelial nitric oxide synthase. Am J Physiol Heart Circ Physiol 284:H133-H140
54. Goetzl EJ, Kong Y, Mei B (1999) Lysophosphatidic acid and sphingosine 1-phosphate protection of T cells from apoptosis in association with suppression of Bax. J Immunol 162:2049-2056
55. Osawa Y, Banno Y, Nagaki M, Brenner DA, Naiki T, Nozawa Y, Nakashima S, Moriwaki H (2001) TNF-alpha-induced sphingosine 1-phosphate inhibits apoptosis through a phosphatidylinositol 3-kinase/Akt pathway in human hepatocytes. J Immunol 167:173-180
56. Theilmeier G, Schmidt C, Herrmann J, Keul P, Schafers M, Herrgott I, Mersmann J, Larmann J, Hermann S, Stypmann J, Schober O, Hildebrand R, Schulz R, Heusch G, Haude M, von Wnuck Lipinski K, Herzog C, Schmitz M, Erbel R, Chun J, Levkau B (2006) High-density lipoproteins and their constituent, sphingosine-1-phosphate, directly protect the heart against ischemia/reperfusion injury in vivo via the S1P3 lysophospholipid receptor. Circulation 114:1403-1409
57. Xia P, Wang L, Gamble JR, Vadas MA (1999) Activation of sphingosine kinase by tumor necrosis factor-alpha inhibits apoptosis in human endothelial cells. J Biol Chem 274:34499-34505
58. Sauer B, Gonska H, Manggau M, Kim DS, Schraut C, Schafer-Korting M, Kleuser B (2005) Sphingosine 1-phosphate is involved in cytoprotective actions of calcitriol in human fibroblasts and enhances the intracellular Bcl-2/Bax rheostat. Pharmazie 60:298-304
59. Suschek CV, Krischel V, Bruch-Gerharz D, Berendji D, Krutmann J, Kroncke KD, Kolb-Bachofen V (1999) Nitric oxide fully protects against UVA-induced apoptosis in tight correlation with Bcl-2 up-regulation. J Biol Chem 274:6130-6137
60. Waeber C, Blondeau N, Salomone S (2004) Vascular sphingosine-1-phosphate S1P1 and S1P3 receptors. Drug News Perspect 17:365-382
61. Igarashi J, Michel T (2001) 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
62. Rikitake Y, Hirata K, Kawashima S, Ozaki M, Takahashi T, Ogawa W, Inoue N, Yokoyama M (2002) Involvement of endothelial nitric oxide in sphingosine-1-phosphate-induced angiogenesis. Arterioscler Thromb Vasc Biol 22:108-114
63. Kim JH, Go HY, Jin DH, Kim HP, Hong MH, Chung WY, Park JH, Jang JB, Jung H, Shin YC, Kim SH, Ko SG (2008) Inhibition of the PI3K-Akt/PKB survival pathway enhanced an ethanol extract of Rhus verniciflua. Stokes-induced apoptosis via a mitochondrial pathway in AGS gastric cancer cell lines. Cancer Lett 265:197-205
64. Lichte K, Rossi R, Danneberg K, ter Braak M, Kurschner U, Jakobs KH, Kleuser B, Meyer zu Heringdorf D (2008) Lysophospholipid receptor-mediated calcium signaling in human keratinocytes. J Invest Dermatol 128:1487-1498
65. Fieber CB, Eldridge J, Taha TA, Obeid LM, Muise-Helmericks RC (2006) Modulation of total Akt kinase by increased expression of a single isoform: requirement of the sphingosine-1-phosphate receptor, Edg3/S1P3, for the VEGF-dependent expression of Akt3 in primary endothelial cells. Exp Cell Res 312:1164-1173
66. Yamada M, Banno Y, Takuwa Y, Koda M, Hara A, Nozawa Y (2004) Overexpression of phospholipase D prevents actinomycin D-induced apoptosis through potentiation of phosphoinositide 3-kinase signalling pathways in Chinese-hamster ovary cells. Biochem J 378:649-656
67. Kwon YG, Min JK, Kim KM, Lee DJ, Billiar TR, Kim YM (2001) Sphingosine 1-phosphate protects human umbilical vein endothelial cells from serum-deprived apoptosis by nitric oxide production. J Biol Chem 276:10627-10633
68. Corsetti G, D'Antona G, Dioguardi FS, Rezzani R (2010) Topical application of dressing with amino acids improves cutaneous wound healing in aged rats. Acta Histochem 112:497-507
69. Debats IB, Wolfs TG, Gotoh T, Cleutjens JP, Peutz-Kootstra CJ, van der Hulst RR (2009) Role of arginine in superficial wound healing in man. Nitric Oxide 21:175-183
70. Prakash H, Luth A, Grinkina N, Holzer D, Wadgaonkar R, Gonzalez AP, Anes E, Kleuser B (2010) Sphingosine kinase-1 (SphK-1) regulates Mycobacterium smegmatis infection in macrophages. PLoS ONE 5:e10657