Collagen fragmentation promotes oxidative stress and elevates matrix metalloproteinase-1 in fibroblasts in aged human skin

American Journal of Pathology

Volumn 174, Issue 1, 2009, Pages 101-114

  Fisher, Gary J ^a,c   Quan, Taihao ^a   Purohit, Trupta ^a   Shao, Yuan ^a   Moon, Kyun Cho ^a,b   He, Tianyuan ^a   Varani, James ^a   Kang, Sewon ^a   Voorhees, John J ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b Soonchunhyang University College of Medicine   (South Korea)

^c Med Sci I   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; COLLAGEN FIBRIL; COLLAGEN TYPE 1; INTERSTITIAL COLLAGENASE; TISSUE INHIBITOR OF METALLOPROTEINASE; TRANSCRIPTION FACTOR AP 1; UBIDECARENONE; VERY LATE ACTIVATION ANTIGEN 2;

ADULT; AGED; AGING; ARTICLE; CONNECTIVE TISSUE; CONTROLLED STUDY; CUTANEOUS PARAMETERS; EXTRACELLULAR MATRIX; FIBROBLAST; GENE EXPRESSION REGULATION; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE; IN VIVO STUDY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUNCH BIOPSY; SKIN; SKIN CULTURE; WESTERN BLOTTING; ZYMOGRAPHY;

EID: 58249116543     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2009.080599     Document Type: Article

References (92)

1. Uitto J, Pulkkinen L, Chu M-L: Collagen. Dermatology in General Medicine. Edited by Fitzpatrick TB, Eisen AZ, Wolff K, Freedberg IM, Austen KF. New York, McGraw-Hill, 2003, pp 165-179
2. Smith J, Davidson E, Sams W, Clark R: Alterations in human dermal connective tissue with age and chronic sun damage. J Invest Dermatol 1962, 39:347-350
3. Uitto J: Biology of dermal cells and extracellular matrix. Dermatology in General Medicine. Edited by Fitzpatrick T, Eisen A, Wolff K, Freedberg I, Austen K. New York, McGraw-Hill, 1993, pp 299-314
4. Warren R, Gartstein V, Kligman A, Montagna W, Allendorf R, Ridder G: Age, sunlight, and facial skin: a histologic and quantitative study. J Am Acad Dermatol 1991, 25:751-760
5. West M: The cellular and molecular biology of skin aging. Arch Dermatol 1994, 130:87-95
6. Varani J, Dame MK, Rittie L, Fligiel SE, Kang S, Fisher GJ, Voorhees JJ: Decreased collagen production in chronologically aged skin: roles of age-dependent alteration in fibroblast function and defective mechanical stimulation. Am J Pathol 2006, 168:1861-1868
7. Andreotti L, Bussotti A, Cammelli D, Aiello E, Sampognaro S: Connective tissue in aging lung. Gerontology 1983, 29:377-387
8. Rittié L, Fisher G: UV-light-induced signal cascades and skin aging. Ageing Res Rev 2002, 1:705-720
9. Uitto J, Bernstein E: Molecular mechanisms of cutaneous aging: connective tissue alterations in the dermis. J Investig Dermatol Symp Proc 1998, 3:41-44
10. Fisher G, Kang S, Varani J, Bata-Csorgo Z, Wan Y, Datta S, Voorhees J: Mechanisms of photoaging and chronological skin aging. Arch Dermatol 2002, 138:1462-1470
11. Brakebusch C, Fassler R: The integrin-action connection, an eternal love affair. EMBO J 2003, 22:2324-2333
12. Delon I, Brown NH: Integrins and the actin cytoskeleton. Curr Opin Cell Biol 2007, 19:43-50
13. Alenghat FJ, Ingber DE: Mechanotransduction: all signals point to cytoskeleton, matrix, and integrins. Sci STKE 2002, 2002:PE6
14. Reed MJ, Ferara NS, Vernon RB: Impaired migration, integrin function, and actin cytoskeletal organization in dermal fibroblasts from a subset of aged human donors. Mech Ageing Dev 2001, 122:1203-1220
15. Wang N, Ingber DE: Control of cytoskeletal mechanics by extracellular matrix, cell shape, and mechanical tension. Biophys J 1994, 66:2181-2189
16. Grinnell F: Fibroblast biology in three-dimensional collagen matrices. Trends Cell Biol 2003, 13:264-269
17. Lecuit T, Lenne PF: Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat Rev Mol Cell Biol 2007, 8:633-644
18. Peyton SR, Ghajar CM, Khatiwala CB, Putnam AJ: The emergence of ECM mechanics and cytoskeletal tension as important regulators of cell function. Cell Biochem Biophys 2007, 47:300-320
19. Eckes B, Zweers MC, Zhang ZG, Hallinger R, Mauch C, Aumailley M, Krieg T: Mechanical tension and integrin alpha 2 beta 1 regulate fibroblast functions. J Investig Dermatol Symp Proc 2006, 11:66-72
20. Fisher GJ, Kang S, Varani J, Bata-Csorgo Z, Wan Y, Datta S, Voorhees JJ: Mechanisms of photoaging and chronological skin aging. Arch Dermatol 2002, 138:1462-1470
21. Birkedal-Hansen H, Moore W, Bodden M, Windsor L, Birkedal-Hansen B, DeCarlo A, Engler J: Matrix metalloproteinases: a review. Crit Rev Oral Biol Med 1993, 4:197-250
22. Kahäri V, Saarialho-Kere U: Matrix metalloproteinases in skin. Exp Dermatol 1997, 6:199-213
23. McCawley L, Matrisian L: Matrix metalloproteinases: they're not just for matrix anymore! Curr Opin Cell Biol 2001, 13:534-540
24. Page-McCaw A, Ewald AJ, Werb Z: Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 2007, 8:221-233
25. Holmbeck K, Bianco P, Caterina J, Yamada S, Kromer M, Kuznetsov SA, Mankani M, Robey PG, Poole AR, Pidoux I, Ward JM, Birkedal-Hansen H: MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell 1999, 99:81-92
26. Sounni NE, Noel A: Membrane type-matrix metalloproteinases and tumor progression. Biochimie 2005, 87:329-342
27. Fisher GJ, Choi HC, Bata-Csorgo Z, Shao Y, Datta S, Wang ZQ, Kang S, Voorhees JJ: Ultraviolet irradiation increases matrix metalloproteinase-8 protein in human skin in vivo. J Invest Dermatol 2001, 117:219-226
28. Fisher GJ, Datta SC, Talwar HS, Wang ZQ, Varani J, Kang S, Voorhees JJ: Molecular basis of sun-induced premature skin ageing and retinoid antagonism. Nature 1996, 379:335-339
29. Fisher GJ, Wang ZQ, Datta SC, Varani J, Kang S, Voorhees JJ: Pathophysiology of premature skin aging induced by ultraviolet light. N Engl J Med 1997, 337:1419-1428
30. Brennan M, Bhatti H, Nerusu K, Bhagavathula N, Kang S, Fisher G, Varani J, Voorhees J: Matrix metalloproteinase-1 is the collagenolytic enzyme responsible for collagen damage in UV-irradiated human skin. Photochem Photobiol 2003, 78:43-48
31. Varani J, Warner RL, Gharaee-Kermani M, Phan SH, Kang S, Chung JH, Wang ZQ, Datta SC, Fisher GJ, Voorhees JJ: Vitamin A antagonizes decreased cell growth and elevated collagen-degrading matrix metalloproteinases and stimulates collagen accumulation in naturally aged human skin. J Invest Dermatol 2000, 114:480-486
32. Wang F, Garza LA, Kang S, Varani J, Orringer JS, Fisher GJ, Voorhees JJ: In vivo stimulation of de novo collagen production caused by cross-linked hyaluronic acid dermal filler injections in photodamaged human skin. Arch Dermatol 2007, 143:155-163
33. Fligiel S, Varani J, Datta S, Kang S, Fisher G, Voorhees J: Collagen degradation in aged/photodamaged skin in vivo and after exposure to matrix metalloproteinase-1 in vitro. J Invest Dermatol 2003, 120:842-848
34. Jacob M: Extracellular matrix remodeling and matrix metalloproteinases in the vascular wall during aging and in pathological conditions. Biomed Pharmacother 2003, 57:195-202
35. Lahmann C, Bergemann J, Harrison G, Young A: Matrix metalloproteinase-1 and skin ageing in smokers. Lancet 2001, 357:935-936
36. Toy LW: Matrix metalloproteinases: their function in tissue repair. J Wound Care 2005, 14:20-22
37. Harman D: The aging process. Proc Natl Acad Sci USA 1981, 78:7124-7128
38. Harman D: Free radical theory of aging. Mutat Res 1992, 275:257-266
39. Cutler R: Antioxidants and aging. Am J Clin Nutr 1991, 53:373S-379S
40. Golden T, Hinerfield D, Melov S: Oxidative stress and aging: beyond correlation. Aging Cell 2002, 1:117-123
41. Lavrovsky Y, Chatterjee B, Clark R, Roy A: Role of redox-regulated transcription factors in inflammation, aging and age-related diseases. Exp Gerontol 2000, 35:521-532
42. Rattan SI: Theories of biological aging: genes, proteins, and free radicals. Free Radic Res 2006, 40:1230-1238
43. Stadtman E: Protein oxidation and aging. Science 1992, 257:1220-1224
44. Fisher GJ, Esmann J, Griffiths CEM, Voorhees JJ: Cellular, immunologic and biochemical characterization of topical retinoic acid-treated human skin. J Invest Dermatol 1991, 96:699-707
45. Quan T, He T, Shao Y, Lin L, Kang S, Voorhees J, Fisher G: Elevated cystein-rich 61 mediates aberrant collagen homeostasis in chronologically aged and photoaged human skin. Am J Pathol 2006, 169:482-490
46. Varani J, Perone P, Griffiths CE, Inman DR, Fligiel SE, Voorhees JJ: All-trans retinoic acid (RA) stimulates events in organ-cultured human skin that underlie repair. Adult skin from sun-protected and sun-exposed sites responds in an identical manner to RA while neonatal foreskin responds differently. J Clin Invest 1994, 94:1747-1756
47. Varani J, Fay K, Perone P: MDI 301, a non-irritating retinoid, induces changes in human skin that underlie repair. Arch Dermatol Res 2007, 298:439-448
48. Lateef H, Stevens MJ, Varani J: All-trans-retinoic acid suppresses matrix metalloproteinase activity and increases collagen synthesis in diabetic human skin in organ culture. Am J Pathol 2004, 165:167-174
49. Quan T, He T, Kang S, Voorhees J, Fisher G: Solar ultraviolet irradiation reduces collagen in photoaged human skin by blocking transforming growth factor-β type II receptor/Smad signaling. Am J Pathol 2004, 165:741-751
50. Quan T, He T, Kang S, Voorhees J, Fisher G: Connective tissue growth factor: expression in human skin in vivo and inhibition by ultraviolet irradiation. J Invest Dermatol 2002, 118:402-408
51. Quan T, He T, Voorhees J, Fisher G: Ultraviolet irradiation induces Smad7 via induction of transcription factor AP-1 in human skin fibroblasts. J Biol Chem 2005, 280:8079-8085
52. Fisher GJ, Datta S, Wang Z, Li XY, Quan T, Chung JH, Kang S, Voorhees JJ: c-Jun-dependent inhibition of cutaneous procollagen transcription following ultraviolet irradiation is reversed by all-trans retinoic acid. J Clin Invest 2000, 106:663-670
53. Fisher GJ, Voorhees JJ: Molecular mechanisms of photoaging and its prevention by retinoic acid: ultraviolet irradiation induces MAP kinase signal transduction cascades that induce AP-1-regulated matrix metalloproteinases that degrade human skin in vivo. J Investig Dermatol Symp Proc 1998, 3:61-68
54. Shukla A, Jung M, Sern M, Fukagawa N, Taatfes D, Sawyer D, Van Houten B, Mossman B: Asbestos induces mitochondrial DNA damage and dysfunction linked to the development of apoptosis. Am J Physiol 2003, 285:L1018-L1025
55. Brew K, Dinakarapandian D, Nagase H: Tissue inhibitors of metalloproteinases: evolution, structure, and function. Biochim Biophys Acta 2000, 1477:267-283
56. Fisher G, Datta S, Wang Z, Li X, Quan T, Chung J, Kang S, Voorhees J: c-Jun dependent inhibition of cutaneous procollagen transcription following ultraviolet irradiation is reversed by all-trans retinoid acid. J Clin Invest 2000, 106:663-670
57. Afonso V, Champy R, Mitrovic D, Collin P, Lomri A: Reactive oxygen species and superoxide dismutases: role in joint diseases. Joint Bone Spine 2007, 74:324-329
58. Hulbert AJ, Pamplona R, Buffenstein R, Buttemer WA: Life and death: metabolic rate, membrane composition, and life span of animals. Physiol Rev 2007, 87:1175-1213
59. Lovell MA, Markesbery WR: Oxidative DNA damage in mild cognitive impairment and late-stage Alzheimer's disease. Nucleic Acids Res 2007, 35:7497-7504
60. Terzioglu M, Larsson NG: Mitochondrial dysfunction in mammalian ageing. Novartis Found Symp 2007, 287:197-208; discussion 208-113
61. Danson EJ, Paterson DJ: Reactive oxygen species and autonomic regulation of cardiac excitability. J Cardiovasc Electrophysiol 2006, 17(Suppl 1):S104-S112
62. Boudreau N, Jones P: Extracellular matrix and integrin signalling: the shape of things to come. Biochem J 1999, 339:481-488
63. Hay ED (Ed): Cell Biology of Extracellular Matrix. New York, Plenum Press, 1991 pp. 221-249
64. Bissell MJ, Kenny PA, Radisky DC: Microenvironmental regulators of tissue structure and function also regulate tumor induction and progression: the role of extracellular matrix and its degrading enzymes. Cold Spring Harb Symp Quant Biol 2005, 70:343-356
65. Boitano S: From the extracellular matrix to cell and tissue function in the alveolar epithelium. Am J Physiol 2001, 280:L189-L190
66. Madri JA, Basson MD: Extracellular matrix-cell interactions: dynamic modulators of cell, tissue and organism structure and function. Lab Invest 1992, 66:519-521
67. Sorrell JM, Caplan AI: Fibroblast heterogeneity: more than skin deep. J Cell Sci 2004, 117:667-675
68. Ali-Bahar M, Bauer B, Tredget EE, Ghahary A: Dermal fibroblasts from different layers of human skin are heterogeneous in expression of collagenase and types I and III procollagen mRNA. Wound Repair Regener 2004, 12:175-182
69. Sorrell JM, Baber MA, Caplan AI: Clonal characterization of fibroblasts in the superficial layer of the adult human dermis. Cell Tissue Res 2007, 327:499-510
70. Wenk J, Brenneisen P, Wlaschek M, Poswig A, Briviba K, Oberley TD, Scharffetter-Kochanek K: Stable overexpression of manganese superoxide dismutase in mitochondria identifies hydrogen peroxide as a major oxidant in the AP-1-mediated induction of matrix-degrading metalloprotease-1. J Biol Chem 1999, 274:25869-25876
71. Schriner SE, Linford NJ, Martin GM, Treuting P, Ogburn CE, Emond M, Coskun PE, Ladiges W, Wolf N, Van Remmen H, Wallace DC, Rabinovitch PS: Extension of murine life span by overexpression of catalase targeted to mitochondria. Science 2005, 308:1909-1911
72. Uitto J: Connective tissue biochemistry of the aging dermis. Age-related alterations in collagen and elastin. Dermatol Clin 1986, 4:433-446
73. Monnier VM, Mustata GT, Biemel KL, Reihl O, Lederer MO, Zhenyu D, Sell DR: Cross-linking of the extracellular matrix by the maillard reaction in aging and diabetes: an update on "a puzzle nearing resolution." Ann NY Acad Sci 2005, 1043:533-544
74. Farout L, Friguet B: Proteasome function in aging and oxidative stress: implications in protein maintenance failure. Antioxid Redox Signal 2006, 8:205-216
75. Cortopassi G, Arnheim N: Detection of a specific mitochondrial DNA deletion in tissues of older humans. Nucleic Acids Res 1990, 18:6927-6933
76. Cortopassi G, Shibata D, Soong N-W, Arnheim N: A pattern of accumulation of a somatic deletion of mitochondrial DNA in aging human tissues. Proc Natl Acad Sci USA 1992, 89:7370-7374
77. Lee H-C, Pang C-Y, Hsu H-S, Wei Y-H: Differential accumulations of 4,977bp deletion in mitochondrial DNA of various tissues in human ageing. Biochim Biophys Acta 1994, 1226:37-43
78. Linnane A, Marzuki S, Ozawa T, Tanaka M: Mitochondrial DNA mutations as an important contributor to ageing and degenerative diseases. Lancet 1989, 1:642-645
79. Wei Y-H, Lee H-C: Oxidative stress, mitochondrial DNA mutation, and impairment of antioxidant enzymes in aging. Exp Biol Med (Maywood) 2002, 227:671-682
80. Birch-Machin M, Tindall M, Turner R, Haldane F, Rees J: Mitochondrial DNA deletions in human skin reflect photo-rather than chronologic aging. J Invest Dermatol 1998, 110:149-152
81. Chen CS, Gee KR: Redox-dependent trafficking of 2,3,4,5, 6-pentafluorodihydrotetramethylrosamine, a novel fluorogenic indicator of cellular oxidative activity. Free Radic Biol Med 2000, 28:1266-1278
82. Lambeth JD, Kawahara T, Diebold B: Regulation of Nox and Duox enzymatic activity and expression. Free Radic Biol Med 2007, 43:319-331
83. Lambeth JD: Nox enzymes, ROS, and chronic disease: an example of antagonistic pleiotropy. Free Radic Biol Med 2007, 43:332-347
84. Krause KH: Aging: a revisited theory based on free radicals generated by NOX family NADPH oxidases. Exp Gerontol 2007, 42:256-262
85. Varani J, Dame M, Rittie L, Fligiel S, Kang S, Fisher G, Voorhees J: Decreased collagen production in chronologically aged skin. Am J Pathol 2006, 168:1861-1868
86. Alenghat FJ, Nauli SM, Kolb R, Zhou J, Ingber DE: Global cytoskeletal control of mechanotransduction in kidney epithelial cells. Exp Cell Res 2004, 301:23-30
87. Ingber DE: Cellular mechanotransduction: putting all the pieces together again. FASEB J 2006, 20:811-827
88. Silver FH, Siperko LM, Seehra GP: Mechanobiology of force transduction in dermal tissue. Skin Res Technol 2003, 9:3-23
89. Wang N, Butler JP, Ingber DE: Mechanotransduction across the cell surface and through the cytoskeleton. Science 1993, 260:1124-1127
90. James AM, Cocheme HM, Smith RA, Murphy MP: Interactions of mitochondria-targeted and untargeted ubiquinones with the mitochondrial respiratory chain and reactive oxygen species. Implications for the use of exogenous ubiquinones as therapies and experimental tools. J Biol Chem 2005, 280:21295-21312
91. James AM, Sharpley MS, Manas AR, Frerman FE, Hirst J, Smith RA, Murphy MP: Interaction of the mitochondria-targeted antioxidant MitoQ with phospholipid bilayers and ubiquinone oxidoreductases. J Biol Chem 2007, 282:14708-14718
92. Wenk J, Brenneisen P, Wlaschek M, Poswig A, Briviba K, Oberley T, Scharffetter-Kochanek K: Stable overexpression of manganese superoxide dismutase in mitochondria identifies hydrogen peroxide as a major oxidant in the AP-1-mediated induction of matrix-degrading metalloproteinase-1. J Biol Chem 1999, 274:25869-25876