Epidermal vascular endothelial growth factor production is required for permeability barrier homeostasis, dermal angiogenesis, and the development of epidermal hyperplasia: Implications for the pathogenesis of psoriasis

American Journal of Pathology

Volumn 173, Issue 3, 2008, Pages 689-699

  Elias, Peter M ^a,d   Arbiser, Jack ^b   Brown, Barbara E ^a   Rossiter, Heidemarie ^c   Man, Mao Qiang ^a   Cerimele, Francesca ^b   Crumrine, Debra ^a   Gunathilake, Roshan ^a   Eung, Ho Choi ^a   Uchida, Yoshikazu ^a   Tschachler, Erwin ^c   Feingold, Kenneth R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Universitatsklinik fur Dermatologie   (Austria)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATOPIC DERMATITIS; CONTROLLED STUDY; EPIDERMIS HYPERPLASIA; HAIRLESS MOUSE; HOMEOSTASIS; LAMELLAR BODY; MALE; MOUSE; NONHUMAN; PATHOGENESIS; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; PSORIASIS; SIGNAL TRANSDUCTION; SKIN INFLAMMATION; SKIN INJURY; UPREGULATION;

EID: 51349107424     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2008.080088     Document Type: Article

References (82)

1. Nickoloff BJ, Bonish BK, Marble DJ, Schriedel KA, DiPietro LA, Gordon KB, Lingen MW: Lessons learned from psoriatic plaques concerning mechanisms of tissue repair, remodeling, and inflammation. J Invest Dermatol Symp Proc 2006, 11:16-29
2. Elias PM: Stratum corneum defensive functions: an integrated view. J Invest Dermatol 2005, 125:183-200
3. Feingold KR, Schmuth M, Elias PM: The regulation of permeability barrier homeostasis. J Invest Dermatol 2007, 127:1574-1576
4. Wood LC, Elias PM, Calhoun C, Tsai JC, Grunfeld C, Feingold KR: Barrier disruption stimulates interleukin-1 alpha expression and release from a pre-formed pool in murine epidermis. J Invest Dermatol 1996, 106:397-403
5. Nickoloff BJ, Naidu Y: Perturbation of epidermal barrier function correlates with initiation of cytokine cascade in human skin. J Am Acad Dermatol 1994, 30:535-546
6. Wood LC, Jackson SM, Elias PM, Grunfeld C, Feingold KR: Cutaneous barrier perturbation stimulates cytokine production in the epidermis of mice. J Clin Invest 1992, 90:482-487
7. Liou A, Elias PM, Grunfeld C, Feingold KR, Wood LC: Amphiregulin and nerve growth factor expression are regulated by barrier status in murine epidermis. J Invest Dermatol 1997, 108:73-77
8. Ye J, Garg A, Calhoun C, Feingold KR, Elias PM, Ghadially R: Alterations in cytokine regulation in aged epidermis: implications for permeability barrier homeostasis and inflammation. I. IL-1 gene family. Exp Dermatol 2002, 11:209-216
9. Jensen JM, Schutze S, Forl M, Kronke M, Proksch E: Roles for tumor necrosis factor receptor p55 and sphingomyelinase in repairing the cutaneous permeability barrier. J Clin Invest 1999, 104:1761-1770
10. Ristow HJ: A major factor contributing to epidermal proliferation in inflammatory skin diseases appears to be interleukin 1 or a related protein. Proc Natl Acad Sci USA 1987, 84:1940-1944
11. Proksch E, Holleran WM, Menon GK, Elias PM, Feingold KR: Barrier function regulates epidermal lipid and DNA synthesis. Br J Dermatol 1993, 128:473-482
12. Grubauer G, Feingold KR, Elias PM: Relationship of epidermal lipogenesis to cutaneous barrier function. J Lipid Res 1987, 28:746-752
13. Denda M, Wood LC, Emami S, Calhoun C, Brown BE, Elias PM, Feingold KR: The epidermal hyperplasia associated with repeated barrier disruption by acetone treatment or tape stripping cannot be attributed to increased water loss. Arch Dermatol Res 1996, 288:230-238
14. Tagami H, Kikuchi K: Diseases that Affect Barrier Function. Edited by Elias PM, Feingold KR. New York, Taylor & Francis, 2006, pp 447-468
15. Elias PM: Stratum corneum architecture, metabolic activity and interactivity with subjacent cell layers. Exp Dermatol 1996, 5:191-201
16. Elias PM, Feingold KR: Does the tail wag the dog? Role of the barrier in the pathogenesis of inflammatory dermatoses and therapeutic implications. Arch Dermatol 2001, 137:1079-1081
17. Elias PM, Wood LC, Feingold KR: Epidermal pathogenesis of inflammatory dermatoses. Am J Contact Dermat 1999, 10:119-126
18. Taïeb A: Hypothesis: from epidermal barrier dysfunction to atopic disorders. Contact Dermatitis 1999, 41:177-180
19. Elias PM, Steinhoff M: "Outside-to-inside" (and now back to "outside") pathogenic mechanisms in atopic dermatitis. J Invest Dermatol 2008, 128:1067-1070
20. Eming SA, Krieg T: Molecular mechanisms of VEGF-A action during tissue repair. J Invest Dermatol Symp Proc 2006, 11:79-86
21. Ferrara N: Vascular endothelial growth factor: basic science and clinical progress. Endocr Rev 2004, 25:581-611
22. Detmar M: Evidence for vascular endothelial growth factor (VEGF) as a modifier gene in psoriasis. J Invest Dermatol 2004, 122:xiv-xv
23. Perry BN, Arbiser JL: The duality of angiogenesis: implications for therapy of human disease. J Invest Dermatol 2006, 126:2160-2166
24. Rosenberger C, Solovan C, Rosenberger AD, Jinping L, Treudler R, Frei U, Eckardt KU, Brown LF: Up-regulation of hypoxia-inducible factors in normal and psoriatic skin. J Invest Dermatol 2007, 127:2445-2452
25. Weninger W, Uthman A, Pammer J, Pichler A, Ballaun C, Lang IM, Plettenberg A, Bankl HC, Sturzl M, Tschachler E: Vascular endothelial growth factor production in normal epidermis and in benign and malignant epithelial skin tumors. Lab Invest 1996, 75:647-657
26. Jackson SM, Mao-Qiang M, Elias PM, Feingold KR: Role of exogenous oxygen in cutaneous barrier repair. Skin Pharmacol 1994, 7:316-319
27. Braverman IM, Yen A: Microcirculation in psoriatic skin. J Invest Dermatol 1974, 62:493-502
28. Braverman IM, Sibley J: Role of the microcirculation in the treatment and pathogenesis of psoriasis. J Invest Dermatol 1982, 78:12-17
29. Malhotra R, Stenn KS, Fernandez LA, Braverman IM: Angiogenic properties of normal and psoriatic skin associate with epidermis, not dermis. Lab Invest 1989, 61:162-165
30. Petzelbauer P, Pober JS, Keh A, Braverman IM: Inducibility and expression of microvascular endothelial adhesion molecules in lesional, perilesional, and uninvolved skin of psoriatic patients. J Invest Dermatol 1994, 103:300-305
31. Schön MP, Boehncke WH: Psoriasis. N Engl J Med 2005, 352:1899-1912
32. Rossiter H, Barresi C, Pammer J, Rendl M, Haigh J, Wagner EF, Tschachler E: Loss of vascular endothelial growth factor a activity in murine epidermal keratinocytes delays wound healing and inhibits tumor formation. Cancer Res 2004, 64:3508-3516
33. Man MQ, Wood L, Elias PM, Feingold KR: Cutaneous barrier repair and pathophysiology following barrier disruption in IL-1 and TNF type I receptor deficient mice. Exp Dermatol 1999, 8:261-266
34. Wood LC, Elias PM, Sequeira-Martin SM, Grunfeld C, Feingold KR: Occlusion lowers cytokine mRNA levels in essential fatty acid-deficient and normal mouse epidermis, but not after acute barrier disruption. J Invest Dermatol 1994, 103:834-838
35. Rossiter H, Barresi C, Ghannadan M, Gruber F, Mildner M, Fodinger D, Tschachler E: Inactivation of VEGF in mammary gland epithelium severely compromises mammary gland development and function. FASEB J 2007, 21:3994-4004
36. Pittelkow M, Scott R: New techniques for the in vitro culture of human skin keratinocytes and perspectives on their use for grafting of patients with extensive burns. Mayo Clin Proc 1986, 61:771-777
37. Uchida Y, Behne M, Quiec D, Elias PM, Holleran WM: Vitamin C stimulates sphingolipid production and markers of barrier formation in submerged human keratinocyte cultures. J Invest Dermatol 2001, 117:1307-1313
38. Harris IR, Farrell AM, Grunfeld C, Holleran WM, Elias PM, Feingold KR: Permeability barrier disruption coordinately regulates mRNA levels for key enzymes of cholesterol, fatty acid, and ceramide synthesis in the epidermis. J Invest Dermatol 1997, 109:783-787
39. Choi EH, Man MQ, Xu P, Xin S, Liu Z, Crumrine DA, Jiang YJ, Fluhr JW, Feingold KR, Elias PM, Mauro TM: Stratum corneum acidification is impaired in moderately aged human and murine skin. J Invest Dermatol 2007, 127:2847-2856
40. Uchida Y, Nardo AD, Collins V, Elias PM, Holleran WM: De novo ceramide synthesis participates in the ultraviolet B irradiation-induced apoptosis in undifferentiated cultured human keratinocytes. J Invest Dermatol 2003, 120:662-669
41. Man XY, Yang XH, Cai SQ, Yao YG, Zheng M: Immunolocalization and expression of vascular endothelial growth factor receptors (VEGFRs) and neuropilins (NRPs) on keratinocytes in human epidermis. Mol Med 2006, 12:127-136
42. Kömüves LG, Hanley K, Man MQ, Elias PM, Williams ML, Feingold KR: Keratinocyte differentiation in hyperproliferative epidermis: topical application of PPARalpha activators restores tissue homeostasis. J Invest Dermatol 2000, 115:361-367
43. Feingold KR: The regulation and role of epidermal lipid synthesis. Adv Lipid Res 1991, 24:57-82
44. Demerjian M, Hachem JP, Tschachler E, Denecker G, Declercq W, Vandenabeele P, Mauro T, Crumrine D, Roelandt T, Houben E, Elias PM, Feingold K: Acute modulations in permeability barrier functions regulate epidermal cornification: Role of caspase 14 and the protease-activated receptor type 2. Am J Pathol 2008, 172:86-97
45. Boutin AT, Weidemann A, Fu Z, Mesropian L, Gradin K, Jamora C, Wiesener M, Eckardt KU, Koch CJ, Ellies LG, Haddad G, Haase VH, Simon MC, Poellinger L, Powell FL, Johnson RS: Epidermal sensing oxygen is essential for systemic hypoxic response. Cell 2008, 133:223-234
46. Wood LC, Stalder AK, Liou A, Campbell IL, Grunfeld C, Elias PM, Feingold KR: Barrier disruption increases gene expression of cytokines and the 55 kD TNF receptor in murine skin. Exp Dermatol 1997, 6:98-104
47. Mottaz JH, Zelickson AS: Keratinosomes in psoriatic skin. Acta Derm Venereol 1975, 55:81-85
48. Braverman IM: The cutaneous microcirculation. J Invest Dermatol Symp Proc 2000, 5:3-9
49. Cao R, Eriksson A, Kubo H, Alitalo K, Cao Y, Thyberg J: Comparative evaluation of FGF-2-, VEGF-A-, and VEGF-C-induced angiogenesis, lymphangiogenesis, vascular fenestrations, and permeability. Circ Res 2004, 94:664-670
50. Strieter RM, Kunkel SL, Elner VM, Martonyi CL, Koch AE, Polverini Elner SG: Interleukin-8. A corneal factor that induces neovascularization. Am J Pathol 1992, 141:1279-1284
51. Diamond AG, Gonterman RM, Anderson AL, Menon K, Offutt CD, Weaver CH, Philbrick WM, Foley J: Parathyroid hormone hormone-related protein and the PTH receptor regulate angiogenesis of skin. J Invest Dermatol 2006, 126:2127-2134
52. Braverman IM, Yen A: Ultrastructure of the capillary loops in dermal papillae of psoriasis. J Invest Dermatol 1977, 68:53-60
53. Eddy DD, Aschheim E, Farber EM: Experimental analysis of isomorphic (Koebner) response in psoriasis. Arch Dermatol 1964, 89:579-588
54. Farber EM, Roth RJ, Aschheim E, Eddy DD, Epinette WW: Role trauma in isomorphic response in psoriasis. Arch Dermatol 1965, 91:246-251
55. Boyd AS, Neldner KH: The isomorphic response of Koebner. Int Dermatol 1990, 29:401-410
56. Wood LC, Feingold KR, Sequeira-Martin SM, Elias PM, Grunfeld Barrier function coordinately regulates epidermal IL-1 and IL-1 receptor antagonist mRNA levels. Exp Dermatol 1994, 3:56-60
57. Cohen T, Nahari D, Cerem LW, Neufeld G, Levi BZ: Interleukin induces the expression of vascular endothelial growth factor. J Biol Chem 1996, 271:736-741
58. Valter MM, Wiestler OD, Pietsche T: Differential control of VEGF synthesis and secretion in human glioma cells by IL-1 and EGF. Int Dev Neurosci 1999, 17:565-577
59. Kwon YW, Kwon KS, Moon HE, Park JA, Choi KS, Kim YS, Jang HS, Oh CK, Lee YM, Kwon YG, Lee YS, Kim KW: Insulin-like growth factor-II regulates the expression of vascular endothelial growth factor by the human keratinocyte cell line HaCaT. J Invest Dermatol 2004, 123:152-158
60. Malaguarnera L, Imbesi R, Di Rosa M, Scuto A, Castrogiovanni Messina A, Sanfilippo S: Action of prolactin, IFN-gamma, TNF-alpha and LPS on heme oxygenase-1 expression and VEGF release human monocytes/macrophages. Int Immunopharmacol 2005, 1458-1469
61. Bonifati C, Ameglio F: Cytokines in psoriasis. Int J Dermatol 1999, 38:241-251
62. Palmer CN, Irvine AD, Terron-Kwiatkowski A, Zhao Y, Liao H, Lee SP, Goudie DR, Sandilands A, Campbell LE, Smith FJ, O'Regan GM, Watson RM, Cecil JE, Bale SJ, Compton JG, DiGiovanna JJ, Fleckman P, Lewis-Jones S, Arseculeratne G, Sergeant A, Munro CS, El Houate B, McElreavey K, Halkjaer LB, Bisgaard H, Mukhopadhyay McLean WH: Common loss-of-function variants of the epidermal barrier protein filaggrin are a major predisposing factor for atopic dermatitis. Nat Genet 2006, 38:441-446
63. Irvine AD, McLean WH: Breaking the (un)sound barrier: filaggrin a major gene for atopic dermatitis. J Invest Dermatol 2006, 126:1200-1202
64. Weidinger S, Illig T, Baurecht H, Irvine AD, Rodriguez E, Diaz-Lacava A, Klopp N, Wagenpfeil S, Zhao Y, Liao H, Lee SP, Palmer CN, Jenneck C, Maintz L, Hagemann T, Behrendt H, Ring J, Nothen MM, McLean WH, Novak N: Loss-of-function variations within the filaggrin gene predispose for atopic dermatitis with allergic sensitizations. J Allergy Clin Immunol 2006, 118:214-219
65. Sandilands A, Smith FJ, Irvine AD, McLean WH: Filaggrin's fuller figure: a glimpse into the genetic architecture of atopic dermatitis. J Invest Dermatol 2007, 127:1282-1284
66. Ghadially R, Reed JT, Elias PM: Stratum corneum structure and function correlates with phenotype in psoriasis. J Invest Dermatol 1996, 107:558-564
67. Petzoldt DG, Braun-Falco O, Wenig KH: Effects of plastic-foil-occlusion on psoriatic lesions. Arch Klin Exp Dermatol 1970, 238:160-168
68. David M, Lowe NJ: Psoriasis therapy: comparative studies with a hydrocolloid dressing, plastic film occlusion, and triamcinolone acetonide cream. J Am Acad Dermatol 1989, 21:511-514
69. Gottlieb AB, Staiano-Coico L, Cohen SR, Varghese M, Carter DM: Occlusive hydrocolloid dressings decrease keratinocyte population growth fraction and clinical scale and skin thickness in active psoriatic plaques. J Dermatol Sci 1990, 1:93-96
70. Griffiths CE, Tranfaglia MG, Kang S: Prolonged occlusion in the treatment of psoriasis: a clinical and immunohistologic study. J Am Acad Dermatol 1995, 32:618-622
71. van de Kerkhof PC: The evolution of the psoriatic lesion. Br J Dermatol 2007, 157:4-15
72. Gudjonsson JE, Johnston A, Dyson M, Valdimarsson H, Elder JT: Mouse models of psoriasis. J Invest Dermatol 2007, 127:1292-1308
73. Xia YP, Li B, Hylton D, Detmar M, Yancopoulos GD, Rudge JS: Transgenic delivery of VEGF to mouse skin leads to an inflammatory condition resembling human psoriasis. Blood 2003, 102:161-168
74. Diaz BV, Lenoir MC, Ladoux A, Frelin C, Demarchez M, Michel S: Regulation of vascular endothelial growth factor expression in human keratinocytes by retinoids. J Biol Chem 2000, 275:642-650
75. Hernández GL, Volpert OV, Iniguez MA, Lorenzo E, Martinez-Martinez S, Grau R, Fresno M, Redondo JM: Selective inhibition of vascular endothelial growth factor-mediated angiogenesis by cyclosporin A: roles of the nuclear factor of activated T cells and cyclooxygenase 2. J Exp Med 2001, 193:607-620
76. Sauder DN, Dekoven J, Champagne P, Croteau D, Dupont E: Neovastat (AE-941), an inhibitor of angiogenesis: randomized phase I/II clinical trial results in patients with plaque psoriasis. J Am Acad Dermatol 2002, 47:535-541
77. Lachgar S, Moukadiri H, Jonca F, Charveron M, Bouhaddioui N, Gall Y, Bonafe JL, Plouet J: Vascular endothelial growth factor is an autocrine growth factor for hair dermal papilla cells. J Invest Dermatol 1996, 106:17-23
78. Le Gouill S, Podar K, Amiot M, Hideshima T, Chauhan D, Ishitsuka K, Kumar S, Raje N, Richardson PG, Harousseau JL, Anderson KC: VEGF induces Mcl-1 up-regulation and protects multiple myeloma cells against apoptosis. Blood 2004, 104:2886-2892
79. Bachelez H: Immunopathogenesis of psoriasis: recent insights on the role of adaptive and innate immunity. J Autoimmun 2005, 25(Suppl):69-73
80. Sabat R, Philipp S, Hoflich C, Kreutzer S, Wallace E, Asadullah K, Volk HD, Sterry W, Wolk K: Immunopathogenesis of psoriasis. Exp Dermatol 2007, 16:779-798
81. Lowes MA, Lew W, Krueger JG: Current concepts in the immunopathogenesis of psoriasis. Dermatol Clin 2004, 22:349-369, vii
82. Gira AK, Brown LF, Washington CV, Cohen C, Arbiser JL: Keloids demonstrate high-level epidermal expression of vascular endothelial growth factor. J Am Acad Dermatol 2004, 50:850-853