A novel role of a lipid species, sphingosine-1-phosphate, in epithelial innate immunity

Molecular and Cellular Biology

Volumn 33, Issue 4, 2013, Pages 752-762

  Park, Kyungho ^a   Elias, Peter M ^a   Shin, Kyoung Oh ^b   Lee, Yong Moon ^b   Hupe, Melanie ^a   Borkowski, Andrew W ^c   Gallo, Richard L ^c   Saba, Julie ^d   Holleran, Walter M ^a,e   Uchida, Yoshikazu ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Chungbuk National University   (South Korea)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d CHILDREN S HOSPITAL OAKLAND RESEARCH INSTITUTE   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATHELICIDIN; CCAAT ENHANCER BINDING PROTEIN ALPHA; CERAMIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; SPHINGOSINE 1 PHOSPHATE; THAPSIGARGIN;

ARTICLE; CELL STIMULATION; DOWNSTREAM PROCESSING; ENDOPLASMIC RETICULUM STRESS; EPITHELIUM; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; INNATE IMMUNITY; KERATINOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STAPHYLOCOCCUS AUREUS; UPREGULATION;

ANIMALS; CATHELICIDINS; CCAAT-ENHANCER-BINDING PROTEIN-ALPHA; CELLS, CULTURED; CERAMIDES; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, INNATE; KERATINOCYTES; LYSOPHOSPHOLIPIDS; MICE; MICE, INBRED C57BL; NF-KAPPA B; SKIN; SPHINGOSINE; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

EID: 84873843261     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01103-12     Document Type: Article

References (51)

1. Nijnik A, Hancock RE. 2009. The roles of cathelicidin LL-37 in immune defences and novel clinical applications. Curr. Opin. Hematol. 16:41-47.
2. Schauber J, Gallo RL. 2009. Antimicrobial peptides and the skin immune defense system. J. Allergy Clin. Immunol. 124:R13-R18.
3. Celli A, Mackenzie DS, Crumrine DS, Tu CL, Hupe M, Bikle DD, Elias PM, Mauro TM. 2011. Endoplasmic reticulum Ca(2_) depletion activates XBP1 and controls terminal differentiation in keratinocytes and epidermis. Br. J. Dermatol. 164:16-25.
4. Mera K, Kawahara K, Tada K, Kawai K, Hashiguchi T, Maruyama I, Kanekura T. 2010. ER signaling is activated to protect human HaCaT keratinocytes from ER stress induced by environmental doses of UVB. Biochem. Biophys. Res. Commun. 397:350-354.
5. Aberg KM, Man MQ, Gallo RL, Ganz T, Crumrine D, Brown BE, Choi EH, Kim DK, Schroder JM, Feingold KR, Elias PM. 2008. Co-regulation and interdependence of the mammalian epidermal permeability and antimicrobial barriers. J. Invest. Dermatol. 128:917-925.
6. Carretero M, Escamez MJ, Garcia M, Duarte B, Holguin A, Retamosa L, Jorcano JL, Rio MD, Larcher F. 2008. In vitro and in vivo wound healing-promoting activities of human cathelicidin LL-37. J. Invest. Dermatol. 128:223-236.
7. Hong SP, Kim MJ, Jung MY, Jeon H, Goo J, Ahn SK, Lee SH, Elias PM, Choi EH. 2008. Biopositive effects of low-dose UVB on epidermis: coordinate upregulation of antimicrobial peptides and permeability barrier reinforcement. J. Invest. Dermatol. 128:2880-2887.
8. Mendez-Samperio P. 2010. The human cathelicidin hCAP18/LL-37: a multifunctional peptide involved in mycobacterial infections. Peptides 31:1791-1798.
9. Park K, Elias PM, Oda Y, Mackenzie D, Mauro T, Holleran WM, Uchida Y. 2011. Regulation of cathelicidin antimicrobial peptide expression by an endoplasmic reticulum (ER) stress signaling, vitamin D receptor-independent pathway. J. Biol. Chem. 286:34121-34130.
10. Uchida Y, Houben E, Park K, Douangpanya S, Lee YM, Wu BX, Hannun YA, Radin NS, Elias PM, Holleran WM. 2010. Hydrolytic pathway protects against ceramide-induced apoptosis in keratinocytes exposed to UVB. J. Invest. Dermatol. 130:2472-2480.
11. Uchida Y, Nardo AD, Collins V, Elias PM, Holleran WM. 2003. De novo ceramide synthesis participates in the ultraviolet B irradiation-induced apoptosis in undifferentiated cultured human keratinocytes. J. Invest. Dermatol. 120:662-669.
12. Lei X, Zhang S, Bohrer A, Ramanadham S. 2008. Calcium-independent phospholipase A2 (iPLA2 beta)-mediated ceramide generation plays a key role in the cross-talk between the endoplasmic reticulum (ER) and mitochondria during ER stress-induced insulin-secreting cell apoptosis. J. Biol. Chem. 283:34819-34832.
13. Hannun YA, Obeid LM. 2002. The ceramide-centric universe of lipidmediated cell regulation: stress encounters of the lipid kind. J. Biol. Chem. 277:25847-25850.
14. Zhang K, Kaufman RJ. 2008. From endoplasmic-reticulum stress to the inflammatory response. Nature 454:455-462.
15. Zhang K, Kaufman RJ. 2008. Identification and characterization of endoplasmic reticulum stress-induced apoptosis in vivo. Methods Enzymol. 442:395-419.
16. Charruyer A, Bell SM, Kawano M, Douangpanya S, Yen TY, Macher BA, Kumagai K, Hanada K, Holleran WM, Uchida Y. 2008. Decreasedceramide transport protein, cert, function alters sphingomyelin production following UVB irradiation. J. Biol. Chem. 283:16682-16692.
17. Maceyka M, Sankala H, Hait NC, Le Stunff H, Liu H, Toman R, Collier C, Zhang M, Satin LS, Merrill AH, Jr, Milstien S, Spiegel S. 2005. SphK1 and SphK2, sphingosine kinase isoenzymes with opposing functions in sphingolipid metabolism. J. Biol. Chem. 280:37118-37129.
18. Hagen N, Hans M, Hartmann D, Swandulla D, van Echten-Deckert G. 2011. Sphingosine-1-phosphate links glycosphingolipid metabolism to neurodegeneration via a calpain-mediated mechanism. Cell Death Differ. 18:1356-1365.
19. Sanchez T, Hla T. 2004. Structural and functional characteristics of S1P receptors. J. Cell. Biochem. 92:913-922.
20. 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.
21. 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.
22. Lee YS, Choi KM, Choi MH, Ji SY, Yoo JM, Lee YM, Hong JT, Yun YP, Yoo HS. 2009. Simultaneous HPLC analysis of ceramide and dihydroceramide in human hairs. Arch. Pharm. Res. 32:1795-1801.
23. Bandhuvula P, Honbo N, Wang GY, Jin ZQ, Fyrst H, Zhang M, Borowsky AD, Dillard L, Karliner JS, Saba JD. 2011. S1P lyase: a novel therapeutic target for ischemia-reperfusion injury of the heart. Am. J. Physiol. Heart Circ. Physiol. 300:H1753-H1761.
24. Bernard JJ, Gallo RL. 2010. Cyclooxygenase-2 enhances antimicrobial peptide expression and killing of Staphylococcus aureus. J. Immunol. 185: 6535-6544.
25. Siboo IR, Cheung AL, Bayer AS, Sullam PM. 2001. Clumping factor A mediates binding of Staphylococcus aureus to human platelets. Infect. Immun. 69:3120-3127.
26. Inesi G, Wade R, Rogers T. 1998. The sarcoplasmic reticulum Ca2_ pump: inhibition by thapsigargin and enhancement by adenovirusmediated gene transfer. Ann. N. Y. Acad. Sci. 853:195-206.
27. Sultan I, Senkal CE, Ponnusamy S, Bielawski J, Szulc Z, Bielawska A, Hannun YA, Ogretmen B. 2006. Regulation of the sphingosine-recycling pathway for ceramide generation by oxidative stress, and its role in controlling c-Myc/Max function. Biochem. J. 393:513-521.
28. Ren S, Xin C, Pfeilschifter J, Huwiler A. 2010. A novel mode of action of the putative sphingosine kinase inhibitor 2-(p-hydroxyanilino)-4-(pchlorophenyl) thiazole (SKI II): induction of lysosomal sphingosine kinase 1 degradation. Cell. Physiol. Biochem. 26:97-104.
29. Yamasaki K, Schauber J, Coda A, Lin H, Dorschner RA, Schechter NM, Bonnart C, Descargues P, Hovnanian A, Gallo RL. 2006. Kallikreinmediated proteolysis regulates the antimicrobial effects of cathelicidins in skin. FASEB J. 20:2068-2080.
30. Schroder JM, Harder J. 1999. Human beta-defensin-2. Int. J. Biochem. Cell Biol. 31:645-651.
31. 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.
32. Blom T, Bergelin N, Meinander A, Lof C, Slotte JP, Eriksson JE, Tornquist K. 2010. An autocrine sphingosine-1-phosphate signaling loop enhances NF-kappaB-activation and survival. BMC Cell Biol. 11:45. doi: 10.1186/1471-2121-11-45.
33. Kimura T, Tomura H, Mogi C, Kuwabara A, Ishiwara M, Shibasawa K, Sato K, Ohwada S, Im DS, Kurose H, Ishizuka T, Murakami M, Okajima F. 2006. Sphingosine 1-phosphate receptors mediate stimulatory and inhibitory signalings for expression of adhesion molecules in endothelial cells. Cell. Signal. 18:841-850.
34. Okajima F, Tomura H, Sho K, Nochi H, Tamoto K, Kondo Y. 1996. Involvement of pertussis toxin-sensitive GTP-binding proteins in sphingosine 1-phosphate-induced activation of phospholipase C-Ca2_system in HL60 leukemia cells. FEBS Lett. 379:260-264.
35. Maceyka M, Milstien S, Spiegel S. 2009. Sphingosine-1-phosphate: the Swiss army knife of sphingolipid signaling. J. Lipid Res. 50(Suppl):S272-S276.
36. Lee AS, Wells S, Kim KS, Scheffler IE. 1986. Enhanced synthesis of the glucose/calcium-regulated proteins in a hamster cell mutant deficient intransfer of oligosaccharide core to polypeptides. J. Cell. Physiol. 129:277-282.
37. Ross SE, Radomska HS, Wu B, Zhang P, Winnay JN, Bajnok L, Wright WS, Schaufele F, Tenen DG, MacDougald OA. 2004. Phosphorylation of C/EBPalpha inhibits granulopoiesis. Mol. Cell. Biol. 24:675-686.
38. Zhang P, Liu B, Jenkins GM, Hannun YA, Obeid LM. 1997. Expression of neutral sphingomyelinase identifies a distinct pool of sphingomyelin involved in apoptosis. J. Biol. Chem. 272:9609-9612.
39. Jeschke MG, Finnerty CC, Herndon DN, Song J, Boehning D, Tompkins RG, Baker HV, Gauglitz GG. 2012. Severe injury is associated with insulin resistance, endoplasmic reticulum stress response, and unfolded protein response. Ann. Surg. 255:370-378.
40. Richardson CE, Kinkel S, Kim DH. 2011. Physiological IRE-1-XBP-1 and PEK-1 signaling in Caenorhabditis elegans larval development and immunity. PLoS Genet. 7:e1002391. doi:10.1371/journal.pgen.1002391.
41. Richardson CE, Kooistra T, Kim DH. 2010. An essential role for XBP-1 in host protection against immune activation in C. elegans. Nature 463: 1092-1095.
42. Gombart AF, Borregaard N, Koeffler HP. 2005. Human cathelicidin antimicrobial peptide (CAMP) gene is a direct target of the vitamin D receptor and is strongly up-regulated in myeloid cells by 1,25-dihydroxyvitamin D3. FASEB J. 19:1067-1077.
43. Lepine S, Allegood JC, Park M, Dent P, Milstien S, Spiegel S. 2011. Sphingosine-1-phosphate phosphohydrolase-1 regulates ER stressinduced autophagy. Cell Death Differ. 18:350-361.
44. van der Does AM, Beekhuizen H, Ravensbergen B, Vos T, Ottenhoff TH, van Dissel JT, Drijfhout JW, Hiemstra PS, Nibbering PH. 2010.LL-37 directs macrophage differentiation toward macrophages with a proinflammatory signature. J. Immunol. 185:1442-1449.
45. Davidson DJ, Currie AJ, Reid GS, Bowdish DM, MacDonald KL, Ma RC, Hancock RE, Speert DP. 2004. The cationic antimicrobial peptide LL-37 modulates dendritic cell differentiation and dendritic cell-induced T cell polarization. J. Immunol. 172:1146-1156.
46. Spiegel S, Milstien S. 2011. The outs and the ins of sphingosine-1-phosphate in immunity. Nat. Rev. Immunol. 11:403-415.
47. Arikawa K, Takuwa N, Yamaguchi H, Sugimoto N, Kitayama J, Nagawa H, Takehara K, Takuwa Y. 2003. Ligand-dependent inhibition of B16 melanoma cell migration and invasion via endogenous S1P2 G proteincoupled receptor. Requirement of inhibition of cellular RAC activity. J. Biol. Chem. 278:32841-32851.
48. Gonzalez-Diez M, Rodriguez C, Badimon L, Martinez-Gonzalez J. 2008. Prostacyclin induction by high-density lipoprotein (HDL) in vascular smooth muscle cells depends on sphingosine 1-phosphate receptors: effect of simvastatin. Thromb. Haemost. 100:119-126.
49. Ryu Y, Takuwa N, Sugimoto N, Sakurada S, Usui S, Okamoto H, Matsui O, Takuwa Y. 2002. Sphingosine-1-phosphate, a platelet-derived lysophospholipid mediator, negatively regulates cellular Rac activity and cell migration in vascular smooth muscle cells. Circ. Res. 90:325-332.
50. Maceyka M, Harikumar KB, Milstien S, Spiegel S. 2011. Sphingosine-1-phosphate signaling and its role in disease. Trends Cell Biol. 22:50-60.
51. Sugiura K, Muro Y, Futamura K, Matsumoto K, Hashimoto N, Nishizawa Y, Nagasaka T, Saito H, Tomita Y, Usukura J. 2009. The unfolded protein response is activated in differentiating epidermal keratinocytes. J. Invest. Dermatol. 129:2126-2135.