IL-1α accelerates stratum corneum formation and improves permeability barrier homeostasis during murine fetal development

Journal of Dermatological Science

Volumn 54, Issue 2, 2009, Pages 88-98

  Jiang, Yan J ^a   Lu, Biao ^a   Crumrine, Debra ^a   Man, Mao Qing ^a   Elias, Peter M ^a   Feingold, Kenneth R ^a  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Cornified envelope; Cytokines; Epidermal differentiation; Filaggrin; Involucrin; Loricrin; TNF

Indexed keywords

ENVELOPE PROTEIN; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIRTH; CONTROLLED STUDY; ELECTRON MICROSCOPY; EPIDERMIS; EXPLANT; FEMALE; FETUS; FETUS DEVELOPMENT; GESTATIONAL AGE; HOMEOSTASIS; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; MEMBRANE; MORPHOLOGY; MOUSE; NEWBORN; NONHUMAN; ONTOGENY; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; SKIN PERMEABILITY; SKIN WATER LOSS; STRATUM CORNEUM; ULTRASTRUCTURE; WILD TYPE; ANIMAL; DRUG EFFECT; GENETICS; METABOLISM; MOUSE MUTANT; ORGAN CULTURE TECHNIQUE; PERMEABILITY; PHYSIOLOGY; PRENATAL DEVELOPMENT; SPRAGUE DAWLEY RAT; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; EPIDERMIS; HOMEOSTASIS; INTERLEUKIN-1ALPHA; INTERLEUKIN-1BETA; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, TRANSMISSION; ORGAN CULTURE TECHNIQUES; PERMEABILITY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, INTERLEUKIN-1; RECEPTORS, TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR-ALPHA;

EID: 63149142096     PISSN: 09231811     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jdermsci.2009.01.001     Document Type: Article

References (66)

1. Fuchs E. Epidermal differentiation: the bare essentials. J Cell Biol 111 (1990) 2807-2814
2. Jackson S.M., Williams M.L., Feingold K.R., and Elias P.M. Pathobiology of the stratum corneum. West J Med 158 (1993) 279-285
3. Madison K.C. Barrier function of the skin: "la raison d'etre" of the epidermis. J Invest Dermatol 121 (2003) 231-241
4. Elias P.M. Stratum corneum architecture, metabolic activity and interactivity with subjacent cell layers. Exp Dermatol 5 (1996) 191-201
5. Hammarlund K., and Sedin G. Transepidermal water loss in newborn infants. III. Relation to gestational age. Acta Paediatr Scand 68 (1979) 795-801
6. Harpin V.A., and Rutter N. Barrier properties of the newborn infant's skin. J Pediatr 102 (1983) 419-425
7. Cartlidge P.H., and Stewart J.H. Effect of changing the stillbirth definition on evaluation of perinatal mortality rates. Lancet 346 (1995) 486-488
8. Aszterbaum M., Menon G.K., Feingold K.R., and Williams M.L. Ontogeny of the epidermal barrier to water loss in the rat: correlation of function with stratum corneum structure and lipid content. Pediatr Res 31 (1992) 308-317
9. Hanley K., Rassner U., Jiang Y., Vansomphone D., Crumrine D., Komuves L., et al. Hormonal basis for the gender difference in epidermal barrier formation in the fetal rat. Acceleration by estrogen and delay by testosterone. J Clin Invest 97 (1996) 2576-2584
10. Hanley K., Devaskar U.P., Hicks S.J., Jiang Y., Crumrine D., Elias P.M., et al. Hypothyroidism delays fetal stratum corneum development in mice. Pediatr Res 42 (1997) 610-614
11. Hanley K., Jiang Y., Crumrine D., Bass N.M., Appel R., Elias P.M., et al. Activators of the nuclear hormone receptors PPARalpha and FXR accelerate the development of the fetal epidermal permeability barrier. J Clin Invest 100 (1997) 705-712
12. Hanley K., Komuves L.G., Bass N.M., He S.S., Jiang Y., Crumrine D., et al. Fetal epidermal differentiation and barrier development in vivo is accelerated by nuclear hormone receptor activators. J Invest Dermatol 113 (1999) 788-795
13. Hanley K., Komuves L.G., Ng D.C., Schoonjans K., He S.S., Lau P., et al. Farnesol stimulates differentiation in epidermal keratinocytes via PPARalpha. J Biol Chem 275 (2000) 11484-11491
14. Halgunset J., Johnsen H., Kjollesdal A.M., Qvigstad E., Espevik T., and Austgulen R. Cytokine levels in amniotic fluid and inflammatory changes in the placenta from normal deliveries at term. Eur J Obstet Gynecol Reprod Biol 56 (1994) 153-160
15. Sosenko I.R., Kallapur S.G., Nitsos I., Moss T.J., Newnham J.P., Ikegami M., et al. IL-1alpha causes lung inflammation and maturation by direct effects on preterm fetal lamb lungs. Pediatr Res 60 (2006) 294-298
16. Willet K.E., Kramer B.W., Kallapur S.G., Ikegami M., Newnham J.P., Moss T.J., et al. Intra-amniotic injection of IL-1 induces inflammation and maturation in fetal sheep lung. Am J Physiol Lung Cell Mol Physiol 282 (2002) L411-L420
17. Bry K., Lappalainen U., and Hallman M. Intraamniotic interleukin-1 accelerates surfactant protein synthesis in fetal rabbits and improves lung stability after premature birth. J Clin Invest 99 (1997) 2992-2999
18. Wood L.C., Elias P.M., Calhoun C., Tsai J.C., Grunfeld C., and Feingold K.R. Barrier disruption stimulates interleukin-1 alpha expression and release from a pre-formed pool in murine epidermis. J Invest Dermatol 106 (1996) 397-403
19. Wood L.C., Jackson S.M., Elias P.M., Grunfeld C., and Feingold K.R. Cutaneous barrier perturbation stimulates cytokine production in the epidermis of mice. J Clin Invest 90 (1992) 482-487
20. Jensen J.M., Schutze S., Forl M., Kronke M., and Proksch E. Roles for tumor necrosis factor receptor p55 and sphingomyelinase in repairing the cutaneous permeability barrier. J Clin Invest 104 (1999) 1761-1770
21. Hanley K., Jiang Y., Elias P.M., Feingold K.R., and Williams M.L. Acceleration of barrier ontogenesis in vitro through air exposure. Pediatr Res 41 (1997) 293-299
22. Komuves L.G., Hanley K., Man M.Q., Elias P.M., Williams M.L., and Feingold K.R. Keratinocyte differentiation in hyperproliferative epidermis: topical application of PPARalpha activators restores tissue homeostasis. J Invest Dermatol 115 (2000) 361-367
23. Komuves L.G., Schmuth M., Fowler A.J., Elias P.M., Hanley K., Man M.Q., et al. Oxysterol stimulation of epidermal differentiation is mediated by liver X receptor-beta in murine epidermis. J Invest Dermatol 118 (2002) 25-34
24. Fowler A.J., Sheu M.Y., Schmuth M., Kao J., Fluhr J.W., Rhein L., et al. Liver X receptor activators display anti-inflammatory activity in irritant and allergic contact dermatitis models: liver-X-receptor-specific inhibition of inflammation and primary cytokine production. J Invest Dermatol 120 (2003) 246-255
25. Nolte C.J., Oleson M.A., Bilbo P.R., and Parenteau N.L. Development of a stratum corneum and barrier function in an organotypic skin culture. Arch Dermatol Res 285 (1993) 466-474
26. Hanley K., Jiang Y., Katagiri C., Feingold K.R., and Williams M.L. Epidermal steroid sulfatase and cholesterol sulfotransferase are regulated during late gestation in the fetal rat. J Invest Dermatol 108 (1997) 871-875
27. Jackson S.M., Wood L.C., Lauer S., Taylor J.M., Cooper A.D., Elias P.M., et al. Effect of cutaneous permeability barrier disruption on HMG-CoA reductase, LDL receptor, and apolipoprotein E mRNA levels in the epidermis of hairless mice. J Lipid Res 33 (1992) 1307-1314
28. Jiang Y.J., Lu B., Kim P., Elias P.M., and Feingold K.R. Regulation of ABCA1 expression in human keratinocytes and murine epidermis. J Lipid Res 47 (2006) 2248-2258
29. Bickenbach J.R., Greer J.M., Bundman D.S., Rothnagel J.A., and Roop D.R. Loricrin expression is coordinated with other epidermal proteins and the appearance of lipid lamellar granules in development. J Invest Dermatol 104 (1995) 405-410
30. Hardman M.J., Sisi P., Banbury D.N., and Byrne C. Patterned acquisition of skin barrier function during development. Development 125 (1998) 1541-1552
31. Hardardottir I., Grunfeld C., and Feingold K.R. Effects of endotoxin and cytokines on lipid metabolism. Curr Opin Lipidol 5 (1994) 207-215
32. Shobokshi A., and Shaarawy M. Maternal serum and amniotic fluid cytokines in patients with preterm premature rupture of membranes with and without intrauterine infection. Int J Gynaecol Obstet 79 (2002) 209-215
33. Berner R., Niemeyer C.M., Leititis J.U., Funke A., Schwab C., Rau U., et al. Plasma levels and gene expression of granulocyte colony-stimulating factor, tumor necrosis factor-alpha, interleukin (IL)-1beta, IL-6, IL-8, and soluble intercellular adhesion molecule-1 in neonatal early onset sepsis. Pediatr Res 44 (1998) 469-477
34. Sadowsky D.W., Adams K.M., Gravett M.G., Witkin S.S., and Novy M.J. Preterm labor is induced by intraamniotic infusions of interleukin-1beta and tumor necrosis factor-alpha but not by interleukin-6 or interleukin-8 in a nonhuman primate model. Am J Obstet Gynecol 195 (2006) 1578-1589
35. Bourbon J.R., Farrell P.M., Doucet E., Brown D.J., and Valenza C. Biochemical maturation of fetal rat lung: a comprehensive study including surfactant determination. Biol Neonate 52 (1987) 48-60
36. Hodson W. Normal and abnormal structural development of the lung (1992), W.B. Saunders, Philadelphia
37. Schellhase D.E., Emrie P.A., Fisher J.H., and Shannon J.M. Ontogeny of surfactant apoproteins in the rat. Pediatr Res 26 (1989) 167-174
38. Shimizu H., Miyamura K., and Kuroki Y. Appearance of surfactant proteins, SP-A and SP-B, in developing rat lung and the effects of in vivo dexamethasone treatment. Biochim Biophys Acta 1081 (1991) 53-60
39. Hanley K., Feingold K.R., Komuves L.G., Elias P.M., Muglia L.J., Majzoub J.A., et al. Glucocorticoid deficiency delays stratum corneum maturation in the fetal mouse. J Invest Dermatol 111 (1998) 440-444
40. Hanley K., Rassner U., Elias P.M., Williams M.L., and Feingold K.R. Epidermal barrier ontogenesis: maturation in serum-free media and acceleration by glucocorticoids and thyroid hormone but not selected growth factors. J Invest Dermatol 106 (1996) 404-411
41. Kupper T.S., Ballard D.W., Chua A.O., McGuire J.S., Flood P.M., Horowitz M.C., et al. Human keratinocytes contain mRNA indistinguishable from monocyte interleukin 1 alpha and beta mRNA. Keratinocyte epidermal cell-derived thymocyte-activating factor is identical to interleukin 1. J Exp Med 164 (1986) 2095-2100
42. Schreiber S., Kilgus O., Payer E., Kutil R., Elbe A., Mueller C., et al. Cytokine pattern of Langerhans cells isolated from murine epidermal cell cultures. J Immunol 149 (1992) 3524-3534
43. Maret M., Chicheportiche R., Dayer J.M., and Gabay C. Production of intracellular IL-1alpha, IL-1beta, and IL-1Ra isoforms by activated human dermal and synovial fibroblasts: phenotypic differences between human dermal and synovial fibroblasts. Cytokine 25 (2004) 193-203
44. Dower S.K., Qwarnstrom E.E., Page R.C., Blanton R.A., Kupper T.S., Raines E., et al. Biology of the interleukin-1 receptor. J Invest Dermatol 94 (1990) 68S-73S
45. Dinarello C.A. Interleukin-1 and interleukin-1 antagonism. Blood 77 (1991) 1627-1652
46. Vilcek J., and Lee T.H. Tumor necrosis factor. New insights into the molecular mechanisms of its multiple actions. J Biol Chem 266 (1991) 7313-7316
47. Trefzer U., Brockhaus M., Loetscher H., Parlow F., Kapp A., Schopf E., et al. 55-kd tumor necrosis factor receptor is expressed by human keratinocytes and plays a pivotal role in regulation of human keratinocyte ICAM-1 expression. J Invest Dermatol 97 (1991) 911-916
48. Schmuth M., Schoonjans K., Yu Q.C., Fluhr J.W., Crumrine D., Hachem J.P., et al. Role of peroxisome proliferator-activated receptor alpha in epidermal development in utero. J Invest Dermatol 119 (2002) 1298-1303
49. Ristow H.J. A major factor contributing to epidermal proliferation in inflammatory skin diseases appears to be interleukin 1 or a related protein. Proc Natl Acad Sci U S A 84 (1987) 1940-1944
50. Sauder D.N., Monick M.M., and Hunninghake G.W. Epidermal cell-derived thymocyte activating factor (ETAF) is a potent T-cell chemoattractant. J Invest Dermatol 85 (1985) 431-433
51. Hancock G.E., Kaplan G., and Cohn Z.A. Keratinocyte growth regulation by the products of immune cells. J Exp Med 168 (1988) 1395-1402
52. Kamada M., Hirano K., Arase S., Daitoh T., Maegawa M., Irahara M., et al. Effect of IL-1 in amniotic fluid on the fetal keratinocyte. Biochem Mol Biol Int 39 (1996) 13-20
53. Romero R., Mazor M., Brandt F., Sepulveda W., Avila C., Cotton D.B., et al. Interleukin-1 alpha and interleukin-1 beta in preterm and term human parturition. Am J Reprod Immunol 27 (1992) 117-123
54. Feingold K.R., Soued M., Serio M.K., Moser A.H., Dinarello C.A., and Grunfeld C. Multiple cytokines stimulate hepatic lipid synthesis in vivo. Endocrinology 125 (1989) 267-274
55. Barland C.O., Zettersten E., Brown B.S., Ye J., Elias P.M., and Ghadially R. Imiquimod-induced interleukin-1 alpha stimulation improves barrier homeostasis in aged murine epidermis. J Invest Dermatol 122 (2004) 330-336
56. Baggia S., Gravett M.G., Witkin S.S., Haluska G.J., and Novy M.J. Interleukin-1 beta intra-amniotic infusion induces tumor necrosis factor-alpha, prostaglandin production, and preterm contractions in pregnant rhesus monkeys. J Soc Gynecol Investig 3 (1996) 121-126
57. Evans C.B., Pillai S., and Goldyne M.E. Endogenous prostaglandin E2 modulates calcium-induced differentiation in human skin keratinocytes. Prostaglandins Leukot Essent Fatty Acids 49 (1993) 777-781
58. Man M.Q., Wood L., Elias P.M., and Feingold K.R. Cutaneous barrier repair and pathophysiology following barrier disruption in IL-1 and TNF type I receptor deficient mice. Exp Dermatol 8 (1999) 261-266
59. Kao J.S., Fluhr J.W., Man M.Q., Fowler A.J., Hachem J.P., Crumrine D., et al. Short-term glucocorticoid treatment compromises both permeability barrier homeostasis and stratum corneum integrity: inhibition of epidermal lipid synthesis accounts for functional abnormalities. J Invest Dermatol 120 (2003) 456-464
60. Oxholm A., Oxholm P., Staberg B., and Bendtzen K. Immunohistological detection of interleukin I-like molecules and tumour necrosis factor in human epidermis before and after UVB-irradiation in vivo. Br J Dermatol 118 (1988) 369-376
61. Majewski S., Hunzelmann N., Nischt R., Eckes B., Rudnicka L., Orth G., et al. TGF beta-1 and TNF alpha expression in the epidermis of patients with epidermodysplasia verruciformis. J Invest Dermatol 97 (1991) 862-867
62. Pasparakis M., Alexopoulou L., Episkopou V., and Kollias G. Immune and inflammatory responses in TNF alpha-deficient mice: a critical requirement for TNF alpha in the formation of primary B cell follicles, follicular dendritic cell networks and germinal centers, and in the maturation of the humoral immune response. J Exp Med 184 (1996) 1397-1411
63. Goncalves L.F., Chaiworapongsa T., and Romero R. Intrauterine infection and prematurity. Ment Retard Dev Disabil Res Rev 8 (2002) 3-13
64. Rebarber A., Star Hampton B., Lewis V., and Bender S. Shigellosis complicating preterm premature rupture of membranes resulting in congenital infection and preterm delivery. Obstet Gynecol 100 (2002) 1063-1065
65. Romero R., Gotsch F., Pineles B., and Kusanovic J.P. Inflammation in pregnancy: its roles in reproductive physiology, obstetrical complications, and fetal injury. Nutr Rev 65 (2007) S194-202
66. Baud O., Emilie D., Pelletier E., Lacaze-Masmonteil T., Zupan V., Fernandez H., et al. Amniotic fluid concentrations of interleukin-1beta, interleukin-6 and TNF-alpha in chorioamnionitis before 32 weeks of gestation: histological associations and neonatal outcome. Br J Obstet Gynaecol 106 (1999) 72-77