Regulation of epithelial-mesenchymal IL-1 signaling by PPARβ/δ is essential for skin homeostasis and wound healing

Journal of Cell Biology

Volumn 184, Issue 6, 2009, Pages 817-831

  Chong, Han Chung ^a   Tan, Ming Jie ^a   Philippe, Virginie ^b   Tan, Siew Hwey ^a   Tan, Chek Kun ^a   Ku, Chee Wai ^a   Goh, Yan Yih ^a   Wahli, Walter ^b   Michalik, Liliane ^b   Tan, Nguan Soon ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; CYTOKINE; INTERLEUKIN 1; MAP KINASE KINASE KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; SIGNAL PEPTIDE; TRANSCRIPTION FACTOR AP 1;

ANIMAL TISSUE; ARTICLE; CELL GROWTH; CELL INTERACTION; CELL PROLIFERATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; KERATINOCYTE; MESENCHYME CELL; MITOSIS RATE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN EPITHELIUM; SKIN FIBROBLAST; WOUND HEALING; ANIMAL; AUTOCRINE EFFECT; CELL CULTURE; CELL DIFFERENTIATION; ENZYMOLOGY; EPITHELIUM CELL; FIBROBLAST; GENE SILENCING; GENETICS; HOMEOSTASIS; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; ORGAN CULTURE TECHNIQUE; PROMOTER REGION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SKIN; TIME; TRANSCRIPTION INITIATION;

ANIMALS; AUTOCRINE COMMUNICATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CYTOKINES; EPITHELIAL CELLS; FIBROBLASTS; GENE KNOCKDOWN TECHNIQUES; HOMEOSTASIS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKIN-1; INTERLEUKIN-1ALPHA; INTERLEUKIN-1BETA; MAP KINASE KINASE KINASES; MICE; MICE, KNOCKOUT; ORGAN CULTURE TECHNIQUES; PARACRINE COMMUNICATION; PPAR DELTA; PPAR-BETA; PROMOTER REGIONS, GENETIC; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SKIN; TIME FACTORS; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTIONAL ACTIVATION; WOUND HEALING;

EID: 64049095625     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200809028     Document Type: Article

References (46)

1. Arend, W.P., M. Malyak, C.J. Guthridge, and C. Gabay. 1998. Interleukin-1 receptor antagonist: role in biology. Annu. Rev. Immunol. 16:27-55.
2. Banda, N.K., C. Guthridge, D. Sheppard, K.S. Cairns, M. Muggli, D. Bech- Otschir, W. Dubiel, and W.P. Arend. 2005. Intracellular IL-1 receptor antagonist type 1 inhibits IL-1-induced cytokine production in keratino- cytes through binding to the third component of the COP9 signalosome. J. Immunol. 174:3608-3616.
3. Barak, Y., D. Liao, W. He, E.S. Ong, M.C. Nelson, J.M. Olefsky, R. Boland, and R.M. Evans. 2002. Effects of peroxisome proliferator-activated receptor delta on placentation, adiposity, and colorectal cancer. Proc. Natl. Acad. Sci. USA. 99:303-308.
4. Beanes, S.R., C. Dang, C. Soo, and K. Ting. 2003. Skin repair and scar formation: the central role of TGF-beta. Expert Rev. Mol. Med. 5:1-22.
5. Burdick, A.D., D.J. Kim, M.A. Peraza, F.J. Gonzalez, and J.M. Peters. 2006. The role of peroxisome proliferator-activated receptor-beta/delta in epithelial cell growth and differentiation. Cell. Signal. 18:9-20.
6. Cataisson, C., E. Joseloff, R. Murillas, A. Wang, C. Atwell, S. Torgerson, M. Gerdes, J. Subleski, J.L. Gao, P.M. Murphy, et al. 2003. Activation of cutaneous protein kinase C alpha induces keratinocyte apoptosis and intraepidermal inflammation by independent signaling pathways. J. Immunol. 171:2703-2713.
7. Cheng, N., N.A. Bhowmick, A. Chytil, A.E. Gorksa, K.A. Brown, R. Muraoka, C.L. Arteaga, E.G. Neilson, S.W. Hayward, and H.L. Moses. 2005. Loss of TGF-beta type II receptor in fibroblasts promotes mammary carcinoma growth and invasion through upregulation of TGF-alpha-, MSP- and HGF-mediated signaling networks. Oncogene. 24:5053-5068.
8. Di Poi, N., N.S. Tan, L. Michalik, W. Wahli, and B. Desvergne. 2002. Antiapoptotic role of PPARbeta in keratinocytes via transcriptional control of the Akt1 signaling pathway. Mol. Cell. 10:721-733.
9. Florin, L., L. Hummerich, B.T. Dittrich, F. Kokocinski, G. Wrobel, S. Gack, M. Schorpp-Kistner, S. Werner, M. Hahn, P. Lichter, etal. 2004. Identification of novel AP-1 target genes in fibroblasts regulated during cutaneous wound healing. Oncogene. 23 : 7005 - 7017.
10. Florin, L., N. Maas-Szabowski, S. Werner, A. Szabowski, and P. Angel. 2005. Increased keratinocyte proliferation by JUN-dependent expression of PTN and SDF-1 in fibroblasts. J. Cell Sci. 118:1981-1989.
11. Fusenig, N.E. 1994. Epithelial-mesenchymal interactions regulate keratinocyte growth and differentiation in vitro. In The Keratinocyte Handbook. I.M. Leigh, E.B. Lane, and F.M. Watt, editors. Cambridge University Press, Cambridge/New York. 71-94.
12. Green, C.J., P. Lichtlen, N.T. Huynh, M. Yanovsky, K.R. Laderoute, W. Schaffner, and B.J. Murphy. 2001. Placenta growth factor gene expression is induced by hypoxia in fibroblasts: a central role for metal transcription factor-1. Cancer Res. 61:2696-2703.
13. Groves, R.W., T. Rauschmayr, K. Nakamura, S. Sarkar, I.R. Williams, and T.S. Kupper. 1996. Inflammatory and hyperproliferative skin disease in mice that express elevated levels of the IL-1 receptor (type I) on epidermal kera- tinocytes. Evidence that IL-1-inducible secondary cytokines produced by keratinocytes in vivo can cause skin disease. J. Clin. Invest. 98:336-344.
14. Gupta, R.A., J. Tan, W.F. Krause, M.W. Geraci, T.M. Willson, S.K. Dey, and R.N. DuBois. 2000. Prostacyclin-mediated activation of peroxisome pro- liferator-activated receptor delta in colorectal cancer. Proc. Natl. Acad. Sci. USA. 97 : 13275 - 13280.
15. Harman, F.S., C.J. Nicol, H.E. Marin, J.M. Ward, F.J. Gonzalez, and J.M. Peters. 2004. Peroxisome proliferator-activated receptor-delta attenuates colon carcinogenesis. Nat. Med. 10 : 481- 483.
16. Heiman, A.S., B.O. Abonyo, S.F. Darling-Reed, and M.S. Alexander. 2005. Cytokine-stimulated human lung alveolar epithelial cells release eotaxin-2 (CCL24) and eotaxin-3 (CCL26). J. Interferon Cytokine Res. 25 : 82 - 91.
17. IJpenberg, A., N.S. Tan, L. Gelman, S. Kersten, J. Seydoux, J. Xu, D. Metzger, L. Canaple, P. Chambon, W. Wahli, and B. Desvergne. 2004. In vivo activation of PPAR target genes by RXR homodimers. EMBO J. 23 : 2083 - 2091.
18. Kersten, S., B. Desvergne, and W. Wahli. 2000. Roles of PPARs in health and disease. Nature. 405 : 421 - 424.
19. Kim, D.J., T.E. Akiyama, F.S. Harman, A.M. Burns, W. Shan, J.M. Ward, M.J. Kennett, F.J. Gonzalez, and J.M. Peters. 2004. Peroxisome proliferator- activated receptor beta (delta)-dependent regulation of ubiquitin C expression contributes to attenuation of skin carcinogenesis. J. Biol. Chem. 279 : 23719 - 23727.
20. Kim, D.J., I.A. Murray, A.M. Burns, F.J. Gonzalez, G.H. Perdew, and J.M. Peters. 2005. Peroxisome proliferator-activated receptor-beta/delta inhibits epidermal cell proliferation by down-regulation of kinase activity. J. Biol. Chem. 280 : 9519 - 9527.
21. Letavernier, E., J. Perez, E. Joye, A. Bellocq, B. Fouqueray, J.P. Haymann, D. Heudes, W. Wahli, B. Desvergne, and L. Baud. 2005. Peroxisome prolif- erator-activated receptor beta/delta exerts a strong protection from isch- emic acute renal failure. J. Am. Soc. Nephrol. 16 : 2395 - 2402.
22. Lewis, A.M., S. Varghese, H. Xu, and H.R. Alexander. 2006. Interleukin-1 and cancer progression: the emerging role of interleukin-1 receptor antagonist as a novel therapeutic agent in cancer treatment. J. Transl. Med. 4 : 48
23. Maas-Szabowski, N., H.J. Stark, and N.E. Fusenig. 2000. Keratinocyte growth regulation in defined organotypic cultures through IL-1-induced keratinocyte growth factor expression in resting fibroblasts. J. Invest. Dermatol. 114 : 1075 - 1084.
24. Man, M.Q., G.D. Barish, M. Schmuth, D. Crumrine, Y. Barak, S. Chang, Y. Jiang, R.M. Evans, P.M. Elias, and K.R. Feingold. 2008. Deficiency of PPARbeta/delta in the epidermis results in defective cutaneous permeability barrier homeostasis and increased inflammation. J. Invest. Dermatol. 128 : 370 - 377.
25. Michalik, L., B. Desvergne, N.S. Tan, S. Basu-Modak, P. Escher, J. Rieusset, J.M. Peters, G. Kaya, F.J. Gonzalez, J. Zakany, et al. 2001. Impaired skin wound healing in peroxisome proliferator-activated receptor (PPAR)a and PPAR(3 mutant mice. J. Cell Biol. 154:799-814.
26. Mukhopadhyay, D., B. Knebelmann, H.T. Cohen, S. Ananth, and V.P. Sukhatme. 1997. The von Hippel-Lindau tumor suppressor gene product interacts with Sp1 to repress vascular endothelial growth factor promoter activity. Mol. Cell. Biol. 17 : 5629 - 5639.
27. Nuclear Receptors Nomenclature Committee. 1999. A unified nomenclature system for nuclear receptor superfamily. Cell. 97 : 161 - 163.
28. Ong, C.T., Y.T. Khoo, E.K. Tan, A. Mukhopadhyay, D.V. Do, H.C. Han, I.J. Lim, and T.T. Phan. 2007. Epithelial-mesenchymal interactions in keloid pathogenesis modulate vascular endothelial growth factor expression and secretion. J. Pathol. 211 : 95 - 108.
29. Peters, J.M., S.S. Lee, W. Li, J.M. Ward, O. Gavrilova, C. Everett, M.L. Reitman, L.D. Hudson, and F.J. Gonzalez. 2000. Growth, adipose, brain, and skin alterations resulting from targeted disruption of the mouse peroxisome pro-liferator-activated receptor beta(delta). Mol. Cell. Biol. 20 : 5119 - 5128
30. Podvinec, M., M.R. Kaufmann, C. Handschin, and U.A. Meyer. 2002. NUBIScan, an in silico approach for prediction of nuclear receptor response elements. Mol. Endocrinol. 16 : 1269 - 1279.
31. Rauschmayr, T., R.W. Groves, and T.S. Kupper. 1997. Keratinocyte expression of the type 2 interleukin 1 receptor mediates local and specific inhibition of interleukin 1-mediated inflammation. Proc. Natl. Acad. Sci. USA. 94 : 5814 - 5819.
32. Schmuth, M., C.M. Haqq, W.J. Cairns, J.C. Holder, S. Dorsam, S. Chang, P. Lau, A.J. Fowler, G. Chuang, A.H. Moser, et al. 2004. Peroxisome prolif- erator-activated receptor (PPAR)-beta/delta stimulates differentiation and lipid accumulation in keratinocytes. J. Invest. Dermatol. 122 : 971 - 983.
33. Schroder, J.M. 1995. Cytokine networks in the skin. J. Invest. Dermatol. 105 : 20S - 24S.
34. Schug, T.T., D.C. Berry, N.S. Shaw, S.N. Travis, and N. Noy. 2007. Opposing effects of retinoic Acid on cell growth result from alternate activation of two different nuclear receptors. Cell. 129 : 723 - 733.
35. Shim, J.H., C. Xiao, A.E. Paschal, S.T. Bailey, P. Rao, M.S. Hayden, K.Y. Lee, C. Bussey, M. Steckel, N. Tanaka, et al. 2005. TAK1, but not TAB1 or TAB2, plays an essential role in multiple signaling pathways in vivo. Genes Dev. 19 : 2668 - 2681.
36. Smith, M.F. Jr., D. Eidlen, W.P. Arend, and A. Gutierrez-Hartmann. 1994. LPS- induced expression of the human IL-1 receptor antagonist gene is controlled by multiple interacting promoter elements. J. Immunol. 153 : 3584 - 3593.
37. Smola, H., H.J. Stark, G. Thiekötter, N. Mirancea, T. Krieg, and N.E. Fusenig. 1998. Dynamic of basement membrane formation by keratinocyte-fibroblast interactions in organotypic skin culture. Exp. Cell Res. 239 : 399 - 410.
38. Steude, J., R. Kulke, and E. Christophers. 2002. Interleukin-1-stimulated secretion of interleukin-8 and growth-related oncogene-alpha demonstrates greatly enhanced keratinocyte growth in human raft cultured epidermis. J. Invest. Dermatol. 119 : 1254 - 1260.
39. Szabowski, A., N. Maas-Szabowski, S. Andrecht, A. Kolbus, M. Schorpp- Kistner, N.E. Fusenig, and P. Angel. 2000. c-Jun and JunB antagonistically control cytokine-regulated mesenchymal-epidermal interaction in skin. Cell. 103 : 745 - 755.
40. Tan, N.S., L. Michalik, N. Noy, R. Yasmin, C. Pacot, M. Heim, B. Fluhmann, B. Desvergne, and W. Wahli. 2001. Critical roles of PPAR beta/delta in keratinocyte response to inflammation. Genes Dev. 15:3263-3277.
41. Tan, N.S., L. Michalik, N. Di-Poi, C.Y. Ng, N. Mermod, A.B. Roberts, B. Desvergne, and W. Wahli. 2004. Essential role of Smad3 in the inhibition of inflammation-induced PPARbeta/delta expression. EMBO J. 23 : 4211 - 4221.
42. Tan, N.S., L. Michalik, B. Desvergne, and W. Wahli. 2005. Genetic- or transforming growth factor-beta1-induced changes in epidermal peroxisome proliferator-activated receptor beta/delta expression dictate wound repair kinetics. J. Biol. Chem. 280 : 18163 - 18170.
43. Tan, N.S., G. Icre, A. Montagner, B. Bordier-ten-Heggeler, W. Wahli, and L. Michalik. 2007. The nuclear hormone receptor peroxisome proliferator- activated receptor beta/delta potentiates cell chemotactism, polarization, and migration. Mol. Cell. Biol. 27 : 7161 - 7175.
44. Wang, H.Q., and R.C. Smart. 1999. Overexpression of protein kinase C-alpha in the epidermis of transgenic mice results in striking alterations in phorbol ester-induced inflammation and COX-2, MIP-2 and TNF-alpha expression but not tumor promotion. J. Cell Sci. 112(Pt20):3497-3506.
45. Watanabe, K., P.J. Jose, and S.M. Rankin. 2002. Eotaxin-2 generation is differentially regulated by lipopolysaccharide and IL-4 in monocytes and macrophages. J. Immunol. 168 : 1911 - 1918.
46. Wiener, Z., P. Pocza, M. Racz, G. Nagy, G. Tolgyesi, V. Molnar, J. Jaeger, E. Buzas, E. Gorbe, Z. Papp, et al. 2008. IL-18 induces a marked gene expression profile change and increased Ccl1 (I-309) production in mouse mucosal mast cell homologs. Int. Immunol. 20 : 1565 - 1573.