Autocrine regulation of UVA-induced IL-6 production via release of ATP and activation of P2Y receptors

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Kawano, Ayumi ^a   Kadomatsu, Remi ^a   Ono, Miyu ^a   Kojima, Shuji ^b   Tsukimoto, Mitsutoshi ^b   Sakamoto, Hikaru ^a  

^a KITASATO UNIVERSITY   (Japan)

^b TOKYO UNIVERSITY OF SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; INTERLEUKIN 6; MESSENGER RNA; PURINERGIC P2X7 RECEPTOR; PURINERGIC P2Y RECEPTOR; PURINERGIC P2Y11 RECEPTOR; PURINERGIC P2Y13 RECEPTOR; PURINERGIC P2X RECEPTOR;

ARTICLE; AUTOCRINE EFFECT; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; KERATINOCYTE; PROTEIN ANALYSIS; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN SECRETION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; ULTRAVIOLET A RADIATION; CELL LINE; CELL SURVIVAL; METABOLISM; RADIATION RESPONSE; ULTRAVIOLET RADIATION;

ADENOSINE TRIPHOSPHATE; CELL LINE; CELL SURVIVAL; HUMANS; INTERLEUKIN-6; RECEPTORS, PURINERGIC P2X; RECEPTORS, PURINERGIC P2X7; SIGNAL TRANSDUCTION; ULTRAVIOLET RAYS;

EID: 84934933976     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0127919     Document Type: Article

References (46)

1. Gilchrest BA, Yaar M. Ageing and photoageingoftheskin: observations at the cellular and molecular level. The British journal of dermatology. 1992;127 Suppl 41:25-30. Epub 1992/09/01. PubMed PMID: 1390183.
2. Scharffetter-Kochanek K, Wlaschek M, Brenneisen P, Schauen M, Blaudschun R, Wenk J. UV-induced reactive oxygen species in photocarcinogenesis and photoaging. Biological chemistry. 1997;378(11):1247-57. Epub 1998/01/13. PubMed PMID: 9426184.
3. De Gruijl FR. Photocarcinogenesis: UVA vs. UVB radiation. Skin pharmacology and applied skin physiology. 2002;15(5):316-20. Epub 2002/09/20. doi: 64535. PubMed PMID: 12239425.
4. Parisi AV, Wong JC. An estimation of biological hazards due to solar radiation. Journal of photochemistry and photobiology B, Biology. 2000;54(2-3):126-30. Epub 2000/06/03. PubMed PMID: 10836542.
5. Agar NS, Halliday GM, Barnetson RS, Ananthaswamy HN, Wheeler M, Jones AM. The basal layer in human squamous tumors harbors more UVA than UVB fingerprint mutations: a role for UVA in human skin carcinogenesis. Proceedings of the National Academy of Sciences of the United States of America. 2004;101(14):4954-9. Epub 2004/03/26. doi: 10.1073/pnas.0401141101 PubMed PMID: 15041750; PubMed Central PMCID: PMC387355.
6. Bachelor MA, Bowden GT. UVA-mediated activation of signaling pathways involved in skin tumor promotion and progression. Seminars in cancer biology. 2004;14(2):131-8. Epub 2004/03/17. doi: 10. 1016/j.semcancer.2003.09.017 PubMed PMID: 15018897.
7. Hwang YP, Oh KN, Yun HJ, Jeong HG. Theflavonoidsapigenin and luteolin suppress ultraviolet A-induced matrix metalloproteinase-1 expression via MAPKs and AP-1-dependent signaling in HaCaT cells. Journal of dermatological science. 2011;61(1):23-31. Epub 2010/11/30. doi: 10.1016/j.jdermsci. 2010.10.016 PubMed PMID: 21112745.
8. Scharffetter K, Wlaschek M, Hogg A, Bolsen K, Schothorst A, Goerz G, et al. UVA irradiation induces collagenase in human dermal fibroblasts in vitro and in vivo. Archives of dermatological research. 1991;283(8):506-11. Epub 1991/01/01. PubMed PMID: 1664713.
9. Grone A. Keratinocytes and cytokines. Veterinary immunology and immunopathology. 2002;88(1-2):1-12. Epub 2002/06/29. PubMed PMID: 12088639.
10. Urbanski A, Schwarz T, Neuner P, Krutmann J, Kirnbauer R, Kock A, et al. Ultraviolet light induces increased circulating interleukin-6 in humans. The Journal of investigative dermatology. 1990;94(6):808-11. Epub 1990/06/01. PubMed PMID: 2355183.
11. An L, Dong GQ, Gao Q, Zhang Y, Hu LW, Li JH, et al. Effects of UVAonTNF-alpha, IL-1beta, and IL-10 expression levels in human keratinocytes and intervention studies with an antioxidant and a JNK inhibitor. Photodermatology, photoimmunology & photomedicine. 2010;26(1):28-35. Epub 2010/01/15. doi:10.1111/j.1600-0781.2009.00481.x PubMed PMID: 20070836.
12. Fisher GJ, Datta SC, Talwar HS, Wang ZQ, Varani J, Kang S, et al. Molecular basis of sun-induced premature skin ageing and retinoid antagonism. Nature. 1996;379(6563):335-9. Epub 1996/01/25. doi:10.1038/379335a0 PubMed PMID: 8552187.
13. Fisher GJ, Wang ZQ, Datta SC, Varani J, Kang S, Voorhees JJ. Pathophysiology of premature skin aging induced by ultraviolet light. The New England journal of medicine. 1997;337(20):1419-28. Epub 1997/11/14. doi: 10.1056/NEJM199711133372003 PubMed PMID: 9358139.
14. Fagot D, Asselineau D, Bernerd F. Matrix metalloproteinase-1 production observed after solar-simulated radiation exposure is assumed by dermal fibroblasts but involves a paracrine activation through epidermal keratinocytes. Photochemistry and photobiology. 2004;79(6):499-505. Epub 2004/08/05. PubMed PMID: 15291299.
15. Wlaschek M, Bolsen K, Herrmann G, Schwarz A, Wilmroth F, Heinrich PC, et al. UVA-induced autocrine stimulation of fibroblast-derived-collagenase by IL-6: a possible mechanism in dermal photodamage? The Journal of investigative dermatology. 1993;101(2):164-8. Epub 1993/08/01. PubMed PMID: 7688402.
16. Ralevic V, Burnstock G. Receptors for purines and pyrimidines. Pharmacological reviews. 1998;50(3):413-92. Epub 1998/10/02. PubMed PMID: 9755289.
17. Yegutkin GG. Nucleotide- and nucleoside-converting ectoenzymes: Important modulators of purinergic signalling cascade. Biochimica et biophysica acta. 2008;1783(5):673-94. Epub 2008/02/28. doi: 10. 1016/j.bbamcr.2008.01.024 PubMed PMID: 18302942.
18. Barr TP, Albrecht PJ, Hou Q, Mongin AA, Strichartz GR, Rice FL. Air-stimulated ATP release from keratinocytes occurs through connexin hemichannels. PloSone. 2013;8(2):e56744. Epub 2013/03/05. doi: 10.1371/journal.pone.0056744 PubMed PMID: 23457608; PubMed Central PMCID: PMC3574084.
19. Burnstock G. Introduction: P2 receptors. Current topics in medicinal chemistry. 2004;4(8):793-803. Epub 2004/04/14. PubMed PMID: 15078211.
20. Greig AV, Linge C, Terenghi G, McGrouther DA, Burnstock G. Purinergic receptors are part of afunctional signaling system for proliferation and differentiation of human epidermal keratinocytes. The Journal of investigative dermatology. 2003;120(6):1007-15. Epub 2003/06/06. PubMed PMID: 12787128.
21. Yoshida H, Kobayashi D, Ohkubo S, Nakahata N. ATP stimulates interleukin-6 production via P2Y receptors in human HaCaT keratinocytes. European journal of pharmacology. 2006;540(1-3):1-9. Epub 2006/05/24. doi: 10.1016/j.ejphar.2006.04.008 PubMed PMID: 16716291.
22. Inoue K, Hosoi J, Denda M. Extracellular ATP has stimulatory effects on the expression and release of IL-6 via purinergic receptors in normal human epidermal keratinocytes. The Journal of investigative dermatology. 2007;127(2):362-71. Epub 2006/09/02. doi: 10.1038/sj.jid.5700526 PubMed PMID: 16946718.
23. Tsukimoto M, Homma T, Ohshima Y, Kojima S. Involvement of purinergic signaling in cellular response to gamma radiation. Radiation research. 2010;173(3):298-309. Epub 2010/03/05. doi: 10.1667/RR1732.1 PubMed PMID: 20199215.
24. Takai E, Tsukimoto M, Harada H, Kojima S. Involvement of P2Y6 receptor in p38 MAPK-mediated COX-2 expression in response to UVB irradiation of human keratinocytes. Radiation research. 2011;175(3):358-66. Epub 2011/03/11. doi: 10.1667/RR2375.1 PubMed PMID: 21388279.
25. Onami K, Kimura Y, Ito Y, Yamauchi T, Yamasaki K, Aiba S. Nonmetal haptens induce ATP release from keratinocytes through opening of pannexin hemichannels by reactive oxygen species. The Journal of investigative dermatology. 2014;134(7):1951-60. Epub 2014/02/18. doi: 10.1038/jid.2014.93 PubMed PMID: 24531690.
26. Communi D, Gonzalez NS, Detheux M, Brezillon S, Lannoy V, Parmentier M, et al. Identification of a novel human ADP receptor coupled to G (i). The Journal of biological chemistry. 2001;276(44):41479-85. Epub 2001/09/08. doi: 10.1074/jbc. M105912200 PubMed PMID: 11546776.
27. Kim S, Jin J, Kunapuli SP. Akt activation in platelets depends on Gi signaling pathways. The Journal of biological chemistry. 2004;279(6):4186-95. Epub 2003/11/19. doi: 10.1074/jbc. M306162200 PubMed PMID: 14623889.
28. Khakh BS, Burnstock G, Kennedy C, King BF, North RA, Seguela P, et al. International union of pharmacology. XXIV. Current status of the nomenclature and properties of P2X receptors and their subunits. Pharmacological reviews. 2001;53(1):107-18. Epub 2001/02/15. PubMed PMID: 11171941.
29. Baroja-Mazo A, Barbera-Cremades M, Pelegrin P. The participation of plasma membrane hemichannels to purinergic signaling. Biochimicaetbiophysica acta. 2013;1828(1):79-93. Epub 2012/01/24. doi: 10.1016/j.bbamem.2012.01.002 PubMed PMID: 22266266.
30. Iglesias R, Locovei S, Roque A, Alberto AP, Dahl G, Spray DC, et al. P2X7 receptor-Pannexin1 complex: pharmacology and signaling. American journal of physiology Cell physiology. 2008;295(3):C752-60. Epub 2008/07/04. doi: 10.1152/ajpcell.00228.2008 PubMed PMID: 18596211; PubMed Central PMCID: PMC2544446.
31. Ohshima Y, Tsukimoto M, Harada H, Kojima S. Involvement of connexin43 hemichannel in ATP release after gamma-irradiation. Journal of radiation research. 2012;53(4):551-7. Epub 2012/07/31. doi: 10.1093/jrr/rrs014 PubMed PMID: 22843620; PubMed Central PMCID: PMC3393350.
32. Bellei B, Mastrofrancesco A, Briganti S, Aspite N, Ale-Agha N, Sies H, et al. Ultraviolet A induced modulation of gap junctional intercellular communication by P38 MAPK activation in human keratinocytes. Experimental dermatology. 2008;17(2):115-24. Epub 2007/12/01. doi: 10.1111/j.1600-0625.2007. 00662.x PubMed PMID: 18047584.
33. Goliger JA, Paul DL. Expression of gap junction proteins Cx26, Cx31.1, Cx37, and C 3in developing and mature rat epidermis. Developmental dynamics: an official publication of the American Association of Anatomists. 1994;200(1):1-13. Epub 1994/05/01. doi: 10.1002/aja.1002000102 PubMed PMID: 8081010.
34. He YY, Huang JL, Chignell CF. Delayed and sustained activation of extracellular signal-regulated kinase in human keratinocytes by UVA: implications in carcinogenesis. The Journal of biological chemistry. 2004;279(51):53867-74. Epub 2004/10/09. doi: 10.1074/jbc. M405781200 PubMed PMID: 15471881.
35. Fang X, Yu S, La Pushin R, Lu Y, Furui T, Penn LZ, et al. Lysophosphatidic acid prevents apoptosis in fibroblasts via G (i)-protein-mediated activation of mitogen-activated protein kinase. The Biochemical journal. 2000;352 Pt 1:135-43. Epub 2000/11/04. PubMed PMID: 11062066; PubMed Central PMCID: PMC1221440.
36. Takeda H, Matozaki T, Takada T, Noguchi T, Yamao T, Tsuda M, et al. PI 3-kinase gamma and protein kinase C-zeta mediate RAS-independent activation of MAP kinase by a Gi protein-coupled receptor. The EMBOjournal. 1999;18(2):386-95. Epub 1999/01/16. doi: 10.1093/emboj/18.2.386 PubMed PMID: 9889195; PubMed Central PMCID: PMC1171133.
37. Ortega F, Perez-Sen R, Delicado EG, Teresa Miras-Portugal M. ERK1/2 activation is involved in the neuroprotective action of P2Y13 and P2X7 receptors against glutamate excitotoxicity in cerebellar granule neurons. Neuropharmacology. 2011;61(8):1210-21. Epub 2011/07/30. doi: 10.1016/j. neuropharm.2011.07.010 PubMed PMID: 21798274.
38. Chou CH, Wei LH, Kuo ML, Huang YJ, Lai KP, Chen CA, et al. Up-regulation of interleukin-6 in human ovarian cancer cell via a Gi/PI3K-Akt/NF-kappaB pathway by lysophosphatidic acid, an ovarian canceractivating factor. Carcinogenesis. 2005;26(1):45-52. Epub 2004/10/09. doi: 10.1093/carcin/bgh301 PubMed PMID: 15471896.
39. Wolfle U, Heinemann A, Esser PR, Haarhaus B, Martin SF, Schempp CM. Luteolin prevents solar radiation-induced matrix metalloproteinase-1 activation in human fibroblasts: a role for p38 mitogen-activated protein kinase and interleukin-20 released from keratinocytes. Rejuvenation research. 2012;15(5):466-75. Epub 2012/09/26. doi: 10.1089/rej.2011.1309 PubMed PMID: 23004935; PubMed Central PMCID: PMC3482844.
40. Lyubchenko T, Woodward H, Veo KD, Burns N, Nijmeh H, Liubchenko GA, et al. P2Y1 and P2Y13 purinergic receptors mediate Ca2+ signaling and proliferative responses in pulmonary artery vasa vasorum endothelial cells. American journal of physiology Cell physiology. 2011;300(2):C266-75. Epub 2010/10/22. doi: 10.1152/ajpcell.00237.2010 PubMed PMID: 20962269; PubMed Central PMCID: PMC3043637.
41. Romashkova JA, Makarov SS. NF-kappaB is a target of AKT in anti-apoptotic PDGF signalling. Nature. 1999;401(6748):86-90. Epub 1999/09/15. doi: 10.1038/43474 PubMed PMID: 10485711.
42. Takashima A, Bergstresser PR. Impact of UVB radiation on the epidermal cytokine network. Photochemistry and photobiology. 1996;63(4):397-400. Epub 1996/04/01. PubMed PMID: 8934748.
43. Nishimura N, Reeve VE, Nishimura H, Satoh M, Tohyama C. Cutaneous metallothionein induction by ultraviolet B irradiation in interleukin-6 null mice. The Journal of investigative dermatology. 2000;114(2):343-8. Epub 2000/01/29. doi: 10.1046/j.1523-1747.2000.00862.x PubMed PMID: 10651996.
44. Kuilman T, Michaloglou C, Vredeveld LC, Douma S, Van Doorn R, Desmet CJ, et al. Oncogene-induced senescence relayed by an interleukin-dependent inflammatory network. Cell. 2008;133(6):1019-31. Epub 2008/06/17. doi: 10.1016/j.cell.2008.03.039 PubMed PMID: 18555778.
45. Cho JL, Allanson M, Reeve VE. Hypoxia inducible factor-1alpha contributes to UV radiation-induced inflammation, epidermal hyperplasia and immunosuppression in mice. Photochemical & photobiological sciences: Official journal of the European Photochemistry Association and the European Society for Photobiology. 2012;11(2):309-17. Epub 2011/11/04. doi: 10.1039/c1pp05265a PubMed PMID: 22048469.
46. Lee Y, Kim H, Kim S, Shin MH, Kim YK, Kim KH, et al. Myeloid differentiation factor 88 regulates basal and UV-induced expressions of IL-6 and MMP-1 in human epidermal keratinocytes. The Journal of investigative dermatology. 2009;129(2):460-7. Epub 2008/08/23. doi: 10.1038/jid.2008.261 PubMed PMID: 18719610.