Epidermal hyperproliferation in mice lacking fatty acid transport protein 4 (FATP4) involves ectopic EGF receptor and STAT3 signaling

Developmental Biology

Volumn 344, Issue 2, 2010, Pages 707-719

  Lin, Meei Hua ^a   Chang, Kuo Wei ^b   Lin, Shu Chun ^b   Miner, Jeffrey H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

Amphiregulin; Epidermal hyperplasia; Epiregulin; Epithelial mitogen; PPAR; Skin barrier

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; FATTY ACID TRANSPORTER 4; STAT3 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL COUNT; CELL PROLIFERATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; GENE ACTIVATION; GENE EXPRESSION; GENE FUNCTION; GENE MUTATION; HOMEOSTASIS; KERATINOCYTE; LIPID METABOLISM; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REGULATORY MECHANISM; SKIN DISEASE; SKIN HYPERPLASIA; SKIN PERMEABILITY; UPREGULATION;

MUS;

EID: 77955269825     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.05.503     Document Type: Article

References (61)

1. Bharti A.C., Donato N., Aggarwal B.B. Curcumin (diferuloylmethane) inhibits constitutive and IL-6-inducible STAT3 phosphorylation in human multiple myeloma cells. J. Immunol. 2003, 171:3863-3871.
2. Blumberg H., Conklin D., Xu W.F., Grossmann A., Brender T., Carollo S., Eagan M., Foster D., Haldeman B.A., Hammond A., Haugen H., Jelinek L., Kelly J.D., Madden K., Maurer M.F., Parrish-Novak J., Prunkard D., Sexson S., Sprecher C., Waggie K., West J., Whitmore T.E., Yao L., Kuechle M.K., Dale B.A., Chandrasekher Y.A. Interleukin 20: discovery, receptor identification, and role in epidermal function. Cell 2001, 104:9-19.
3. Buettner R., Mora L.B., Jove R. Activated STAT signaling in human tumors provides novel molecular targets for therapeutic intervention. Clin. Cancer Res. 2002, 8:945-954.
4. Bustin S.A., Benes V., Garson J.A., Hellemans J., Huggett J., Kubista M., Mueller R., Nolan T., Pfaffl M.W., Shipley G.L., Vandesompele J., Wittwer C.T. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 2009, 55:611-622.
5. Caldenhoven E., van Dijk T., Raaijmakers J.A., Lammers J.W., Koenderman L., De Groot R.P. Activation of the STAT3/acute phase response factor transcription factor by interleukin-5. J. Biol. Chem. 1995, 270:25778-25784.
6. Chan K.S., Sano S., Kiguchi K., Anders J., Komazawa N., Takeda J., DiGiovanni J. Disruption of Stat3 reveals a critical role in both the initiation and the promotion stages of epithelial carcinogenesis. J. Clin. Invest. 2004, 114:720-728.
7. Demehri S., Liu Z., Lee J., Lin M.H., Crosby S.D., Roberts C.J., Grigsby P.W., Miner J.H., Farr A.G., Kopan R. Notch-deficient skin induces a lethal systemic B-lymphoproliferative disorder by secreting TSLP, a sentinel for epidermal integrity. PLoS Biol. 2008, 6:e123.
8. Dent P., Yacoub A., Contessa J., Caron R., Amorino G., Valerie K., Hagan M.P., Grant S., Schmidt-Ullrich R. Stress and radiation-induced activation of multiple intracellular signaling pathways. Radiat. Res. 2003, 159:283-300.
9. Di-Poi N., Michalik L., Desvergne B., Wahli W. Functions of peroxisome proliferator-activated receptors (PPAR) in skin homeostasis. Lipids 2004, 39:1093-1099.
10. Doniger S.W., Salomonis N., Dahlquist K.D., Vranizan K., Lawlor S.C., Conklin B.R. MAPPFinder: using Gene Ontology and GenMAPP to create a global gene-expression profile from microarray data. Genome Biol. 2003, 4:R7.
11. El-Abaseri T.B., Fuhrman J., Trempus C., Shendrik I., Tennant R.W., Hansen L.A. Chemoprevention of UV light-induced skin tumorigenesis by inhibition of the epidermal growth factor receptor. Cancer Res. 2005, 65:3958-3965.
12. Elias P.M., Jackson S.M. What does normal skin do?. An Integrated Program in Dermatology 1996, Vol. 1:46-57. W.B. Saunders, Philadelphia. K.A. Arndt (Ed.).
13. Feingold K.R. Thematic review series: skin lipids. The role of epidermal lipids in cutaneous permeability barrier homeostasis. J. Lipid Res. 2007, 48:2531-2546.
14. Fuchs E., Raghavan S. Getting under the skin of epidermal morphogenesis. Nat. Rev. Genet. 2002, 3:199-209.
15. Gazit A., Yaish P., Gilon C., Levitzki A. Tyrphostins I: synthesis and biological activity of protein tyrosine kinase inhibitors. J. Med. Chem. 1989, 32:2344-2352.
16. Gimeno R.E., Hirsch D.J., Punreddy S., Sun Y., Ortegon A.M., Wu H., Daniels T., Stricker-Krongrad A., Lodish H.F., Stahl A. Targeted deletion of fatty acid transport protein-4 results in early embryonic lethality. J. Biol. Chem. 2003, 278:49512-49516.
17. Grandis J.R., Drenning S.D., Chakraborty A., Zhou M.Y., Zeng Q., Pitt A.S., Tweardy D.J. Requirement of Stat3 but not Stat1 activation for epidermal growth factor receptor- mediated cell growth In vitro. J. Clin. Invest. 1998, 102:1385-1392.
18. Grone A. Keratinocytes and cytokines. Vet. Immunol. Immunopathol. 2002, 88:1-12.
19. Hall A.M., Wiczer B.M., Herrmann T., Stremmel W., Bernlohr D.A. Enzymatic properties of purified murine fatty acid transport protein 4 and analysis of acyl-CoA synthetase activities in tissues from FATP4 null mice. J. Biol. Chem. 2005, 280:11948-11954.
20. Hansen L.A., Woodson R.L., Holbus S., Strain K., Lo Y.C., Yuspa S.H. The epidermal growth factor receptor is required to maintain the proliferative population in the basal compartment of epidermal tumors. Cancer Res. 2000, 60:3328-3332.
21. Hardman M.J., Sisi P., Banbury D.N., Byrne C. Patterned acquisition of skin barrier function during development. Development 1998, 125:1541-1552.
22. Harris R.C., Chung E., Coffey R.J. EGF receptor ligands. Exp. Cell Res. 2003, 284:2-13.
23. Herrmann T., Buchkremer F., Gosch I., Hall A.M., Bernlohr D.A., Stremmel W. Mouse fatty acid transport protein 4 (FATP4): characterization of the gene and functional assessment as a very long chain acyl-CoA synthetase. Gene 2001, 270:31-40.
24. Herrmann T., van der Hoeven F., Grone H.J., Stewart A.F., Langbein L., Kaiser I., Liebisch G., Gosch I., Buchkremer F., Drobnik W., Schmitz G., Stremmel W. Mice with targeted disruption of the fatty acid transport protein 4 (Fatp 4, Slc27a4) gene show features of lethal restrictive dermopathy. J. Cell Biol. 2003, 161:1105-1115.
25. Howe L.R., Leevers S.J., Gomez N., Nakielny S., Cohen P., Marshall C.J. Activation of the MAP kinase pathway by the protein kinase raf. Cell 1992, 71:335-342.
26. Jaubert J., Cheng J., Segre J.A. Ectopic expression of kruppel like factor 4 (Klf4) accelerates formation of the epidermal permeability barrier. Development 2003, 130:2767-2777.
27. Jia Z., Moulson C.L., Pei Z., Miner J.H., Watkins P.A. Fatty acid transport protein 4 is the principal very long chain fatty acyl-CoA synthetase in skin fibroblasts. J. Biol. Chem. 2007, 282:20573-20583.
28. Kiuchi N., Nakajima K., Ichiba M., Fukada T., Narimatsu M., Mizuno K., Hibi M., Hirano T. STAT3 is required for the gp130-mediated full activation of the c-myc gene. J. Exp. Med. 1999, 189:63-73.
29. Klar J., Schweiger M., Zimmerman R., Zechner R., Li H., Torma H., Vahlquist A., Bouadjar B., Dahl N., Fischer J. Mutations in the fatty acid transport protein 4 gene cause the ichthyosis prematurity syndrome. Am. J. Hum. Genet. 2009, 85:248-253.
30. Komatsu N., Takata M., Otsuki N., Toyama T., Ohka R., Takehara K., Saijoh K. Expression and localization of tissue kallikrein mRNAs in human epidermis and appendages. J. Invest. Dermatol. 2003, 121:542-549.
31. Komuves L.G., Hanley K., Jiang Y., Elias P.M., Williams M.L., Feingold K.R. Ligands and activators of nuclear hormone receptors regulate epidermal differentiation during fetal rat skin development. J. Invest. Dermatol. 1998, 111:429-433.
32. Korutla L., Kumar R. Inhibitory effect of curcumin on epidermal growth factor receptor kinase activity in A431 cells. Biochim. Biophys. Acta 1994, 1224:597-600.
33. Lee S.S., Pineau T., Drago J., Lee E.J., Owens J.W., Kroetz D.L., Fernandez-Salguero P.M., Westphal H., Gonzalez F.J. Targeted disruption of the alpha isoform of the peroxisome proliferator-activated receptor gene in mice results in abolishment of the pleiotropic effects of peroxisome proliferators. Mol. Cell. Biol. 1995, 15:3012-3022.
34. Lin M.H., Leimeister C., Gessler M., Kopan R. Activation of the Notch pathway in the hair cortex leads to aberrant differentiation of the adjacent hair-shaft layers. Development 2000, 127:2421-2432.
35. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
36. Miettinen P.J., Berger J.E., Meneses J., Phung Y., Pedersen R.A., Werb Z., Derynck R. Epithelial immaturity and multiorgan failure in mice lacking epidermal growth factor receptor. Nature 1995, 376:337-341.
37. Milger K., Herrmann T., Becker C., Gotthardt D., Zickwolf J., Ehehalt R., Watkins P.A., Stremmel W., Fullekrug J. Cellular uptake of fatty acids driven by the ER-localized acyl-CoA synthetase FATP4. J. Cell Sci. 2006, 119:4678-4688.
38. Millar S.E. Molecular mechanisms regulating hair follicle development. J. Invest. Dermatol. 2002, 118:216-225.
39. Minner F., Poumay Y. Candidate housekeeping genes require evaluation before their selection for studies of human epidermal keratinocytes. J. Invest. Dermatol. 2009, 129:770-773.
40. Mondini M., Vidali M., Airo P., De Andrea M., Riboldi P., Meroni P.L., Gariglio M., Landolfo S. Role of the interferon-inducible gene IFI16 in the etiopathogenesis of systemic autoimmune disorders. Ann. NY Acad. Sci. 2007, 1110:47-56.
41. Moulson C.L., Martin D.R., Lugus J.J., Schaffer J.E., Lind A.C., Miner J.H. Cloning of wrinkle-free, a previously uncharacterized mouse mutation, reveals crucial roles for fatty acid transport protein 4 in skin and hair development. Proc. Natl. Acad. Sci. USA. 2003, 100:5274-5279.
42. Moulson C.L., Lin M.H., White J.M., Newberry E.P., Davidson N.O., Miner J.H. Keratinocyte-specific expression of fatty acid transport protein 4 rescues the wrinkle-free phenotype in Slc27a4/Fatp4 mutant mice. J. Biol. Chem. 2007, 282:15912-15920.
43. Natarajan C., Bright J.J. Curcumin inhibits experimental allergic encephalomyelitis by blocking IL-12 signaling through Janus kinase-STAT pathway in T lymphocytes. J. Immunol. 2002, 168. 6506-6013.
44. Patel S., Xi Z.F., Seo E.Y., McGaughey D., Segre J.A. Klf4 and corticosteroids activate an overlapping set of transcriptional targets to accelerate in utero epidermal barrier acquisition. Proc. Natl. Acad. Sci. USA 2006, 103:18668-18673.
45. Peters J.M., Lee S.S., Li W., Ward J.M., Gavrilova O., Everett C., Reitman M.L., Hudson L.D., Gonzalez F.J. Growth, adipose, brain, and skin alterations resulting from targeted disruption of the mouse peroxisome proliferator-activated receptor beta(delta). Mol. Cell. Biol. 2000, 20:5119-5128.
46. Proksch E., Feingold K.R., Man M.Q., Elias P.M. Barrier function regulates epidermal DNA synthesis. J. Clin. Invest. 1991, 87:1668-1673.
47. Reddy S., Aggarwal B.B. Curcumin is a non-competitive and selective inhibitor of phosphorylase kinase. FEBS Lett. 1994, 341:19-22.
48. Richards M.R., Harp J.D., Ory D.S., Schaffer J.E. Fatty acid transport protein 1 and long-chain acyl coenzyme A synthetase 1 interact in adipocytes. J. Lipid Res. 2006, 47:665-672.
49. Sa S.M., Valdez P.A., Wu J., Jung K., Zhong F., Hall L., Kasman I., Winer J., Modrusan Z., Danilenko D.M., Ouyang W. The effects of IL-20 subfamily cytokines on reconstituted human epidermis suggest potential roles in cutaneous innate defense and pathogenic adaptive immunity in psoriasis. J. Immunol. 2007, 178:2229-2240.
50. Sabat R., Philipp S., Hoflich C., Kreutzer S., Wallace E., Asadullah K., Volk H.D., Sterry W., Wolk K. Immunopathogenesis of psoriasis. Exp. Dermatol. 2007, 16:779-798.
51. Sano S., Itami S., Takeda K., Tarutani M., Yamaguchi Y., Miura H., Yoshikawa K., Akira S., Takeda J. Keratinocyte-specific ablation of Stat3 exhibits impaired skin remodeling, but does not affect skin morphogenesis. EMBO J. 1999, 18:4657-4668.
52. Sano S., Chan K.S., Carbajal S., Clifford J., Peavey M., Kiguchi K., Itami S., Nickoloff B.J., DiGiovanni J. Stat3 links activated keratinocytes and immunocytes required for development of psoriasis in a novel transgenic mouse model. Nat. Med. 2005, 11:43-49.
53. Schaffer J.E., Lodish H.F. Expression cloning and characterization of a novel adipocyte long chain fatty acid transport protein. Cell 1994, 79:427-436.
54. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 2008, 3:1101-1108.
55. Schmuth M., Haqq C.M., Cairns W.J., Holder J.C., Dorsam S., Chang S., Lau P., Fowler A.J., Chuang G., Moser A.H., Brown B.E., Mao-Qiang M., Uchida Y., Schoonjans K., Auwerx J., Chambon P., Willson T.M., Elias P.M., Feingold K.R. Peroxisome proliferator-activated receptor (PPAR)-beta/delta stimulates differentiation and lipid accumulation in keratinocytes. J. Invest. Dermatol. 2004, 122:971-983.
56. Schneider M.R., Werner S., Paus R., Wolf E. Beyond wavy hairs: the epidermal growth factor receptor and its ligands in skin biology and pathology. Am. J. Pathol. 2008, 173:14-24.
57. Segre J.A., Bauer C., Fuchs E. Klf4 is a transcription factor required for establishing the barrier function of the skin. Nat. Genet. 1999, 22:356-360.
58. Snyder M., Huang X.Y., Zhang J.J. Identification of novel direct Stat3 target genes for control of growth and differentiation. J. Biol. Chem. 2008, 283:3791-3798.
59. Vassar R., Fuchs E. Transgenic mice provide new insights into the role of TGF-alpha during epidermal development and differentiation. Genes Dev. 1991, 5:714-727.
60. Wang M., Tan Z., Zhang R., Kotenko S.V., Liang P. Interleukin 24 (MDA-7/MOB-5) signals through two heterodimeric receptors, IL-22R1/IL-20R2 and IL-20R1/IL-20R2. J. Biol. Chem. 2002, 277:7341-7347.
61. Weiss R.A., Eichner R., Sun T.T. Monoclonal antibody analysis of keratin expression in epidermal diseases: a 48- and 56-kdalton keratin as molecular markers for hyperproliferative keratinocytes. J. Cell Biol. 1984, 98:1397-1406.