Enhancing structural support of the dermal microenvironment activates fibroblasts, endothelial cells, and keratinocytes in aged human skin in vivo

Journal of Investigative Dermatology

Volumn 133, Issue 3, 2013, Pages 658-667

  Quan, Taihao ^a   Wang, Frank ^a   Shao, Yuan ^a   Rittié, Laure ^a   Xia, Wei ^a   Orringer, Jeffrey S ^a   Voorhees, John J ^a   Fisher, Gary J ^a  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN FIBER; COLLAGEN TYPE 1; CONNECTIVE TISSUE GROWTH FACTOR; FILLER; HYALURONIC ACID; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

AGING; ARTICLE; CELL ACTIVATION; CELL ELONGATION; CELL FUNCTION; CELL PROLIFERATION; CELL SPREADING; CELL STIMULATION; CELL STRUCTURE; CELLULAR DISTRIBUTION; COLLAGEN SYNTHESIS; CONTROLLED STUDY; CROSS LINKING; CUTANEOUS PARAMETERS; DERMIS; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; KERATINOCYTE; MICROENVIRONMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SKIN BLOOD VESSEL; SKIN CULTURE; SKIN FIBROBLAST; SKINFOLD THICKNESS; UPREGULATION;

EID: 84873727210     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2012.364     Document Type: Article

References (58)

1. Barczyk M, Carracedo S, Gullberg D (2010) Integrins. Cell Tissue Res 339: 269-80
2. Brown RA, Sethi KK, Gwanmesia I et al. (2002) Enhanced fibroblast contraction of 3D collagen lattices and integrin expression by TGF-beta1 and-beta3: mechanoregulatory growth factors?. Exp Cell Res 274: 310-22
3. Chen CC, Mo FE, Lau LF (2001) The angiogenic factor Cyr61 activates a genetic program for wound healing in human skin fibroblasts. J Biol Chem 276: 47329-37
4. Chen CS, Mrksich M, Huang S et al. (1997) Geometric control of cell life and death. Science 276: 1425-8
5. Chen Y, Du XY (2007) Functional properties and intracellular signaling of CCN1/Cyr61. J Cell Biochem 100: 1337-45
6. Chung JH, Eun HC (2007) Angiogenesis in skin aging and photoaging. J Dermatol 34: 593-600
7. Croce MA, Dyne K, Boraldi F et al. (2001) Hyaluronan affects protein and collagen synthesis by in vitro human skin fibroblasts. Tissue Cell 33: 326-331
8. David-Raoudi M, Tranchepain F, Deschrevel B et al. (2008) Differential effects of hyaluronan and its fragments on fibroblasts: relation to wound healing. Wound Repair Regen 16: 274-87
9. Delon I, Brown NH (2007) Integrins and the actin cytoskeleton. Curr Opin Cell Biol 19: 43-50
10. Duncan MR, Frazier KS, Abramson S et al. (1999) Connective tissue growth factor mediates transforming growth factor beta-induced collagen synthesis: down-regulation by cAMP. FASEB J 13: 1774-86
11. Dupont S, Morsut L, Aragona M et al. (2011) Role of YAP/TAZ in mechanotransduction. Nature 474: 179-83
12. Eckes B, Zweers MC, Zhang ZG et al. (2006) Mechanical tension and integrin alpha 2 beta 1 regulate fibroblast functions. J Investig Dermatol Symp Proc 11: 66-72
13. Fisher GJ, Henderson PA, Voorhees JJ et al. (1991) Epidermal growth factorinduced hydrolysis of phosphatidylcholine by phospholipase D and phospholipase C in human dermal fibroblasts. J Cell Physiol 146: 309-17
14. Fisher GJ, Kang S, Varani J et al. (2002) Mechanisms of photoaging and chronological skin aging. Arch Dermatol 138: 1462-70
15. Fisher GJ, Quan T, Purohit T et al. (2009) Collagen fragmentation promotes oxidative stress and elevates matrix metalloproteinase-1 in fibroblasts in aged human skin. Am J Pathol 174: 101-14
16. Fisher GJ, Varani J, Voorhees JJ (2008) Looking older: fibroblast collapse and therapeutic implications. Arch Dermatol 144: 666-72
17. Fligiel SE, Varani J, Datta SC et al. (2003) Collagen degradation in aged/photodamaged skin in vivo and after exposure to matrix metalloproteinase-1 in vitro. J Invest Dermatol 120: 842-8
18. Flynn TC, Sarazin D, Bezzola A et al. (2011) Comparative histology of intradermal implantation of mono and biphasic hyaluronic acid fillers. Dermatol Surg 37: 637-43
19. Garrett Q, Khaw PT, Blalock TD et al. (2004) Involvement of CTGF in TGFbeta1-stimulation of myofibroblast differentiation and collagen matrix contraction in the presence of mechanical stress. Invest Ophthalmol Vis Sci 45: 1109-16
20. Grinnell F (2003) Fibroblast biology in three-dimensional collagen matrices. Trends Cell Biol 13: 264-9
21. Grinnell F, Ho CH (2002) Transforming growth factor beta stimulates fibroblast-collagen matrix contraction by different mechanisms in mechanically loaded and unloaded matrices. Exp Cell Res 273: 248-55
22. Holt DR, Kirk SJ, Regan MC et al. (1992) Effect of age on wound healing in healthy human beings. Surgery 112: 293-7
23. Huang L, Gu H, Burd A (2009) A reappraisal of the biological effects of hyaluronan on human dermal fibroblast. J BiomedMater Res A 90: 1177-85
24. Ingber DE (1997) Tensegrity: the architectural basis of cellular mechanotransduction. Annu Rev Physiol 59: 575-99
25. Ingber DE (2006) Cellular mechanotransduction: putting all the pieces together again. FASEB J 20: 811-27
26. Kablik J, Monheit GD, Yu L et al. (2009) Comparative physical properties of hyaluronic acid dermal fillers. Dermatol Surg 35(Suppl 1): 302-12
27. Kang S, Cho S, Chung JH et al. (2005) Inflammation and extracellular matrix degradation mediated by activated transcription factors nuclear factorkappaB and activator protein-1 in inflammatory acne lesions in vivo. Am J Pathol 166: 1691-9
28. Kessler D, Dethlefsen S, Haase I et al. (2001) Fibroblasts in mechanically stressed collagen lattices assume a "synthetic" phenotype. J Biol Chem 276: 36575-85
29. Klein EA, Yin L, Kothapalli D et al. (2009) Cell-cycle control by physiological matrix elasticity and in vivo tissue stiffening. Curr Biol 19: 1511-8
30. Lambert CA, Soudant EP, Nusgens BV et al. (1992) Pretranslational regulation of extracellular matrix macromolecules and collagenase expression in fibroblasts by mechanical forces. Lab Invest 66: 444-51
31. Lambert ChA, Nusgens BV, Lapiere ChM (1998) Mechano-sensing and mechano-reaction of soft connective tissue cells. Adv Space Res 21: 1081-91
32. Lapiere CM (1990) The ageing dermis: the main cause for the appearance of 'old' skin. Br J Dermatol 122(Suppl 35): 5-11
33. Massague J, Gomis RR (2006) The logic of TGFbeta signaling. FEBS Lett 580: 2811-20
34. Mast BA, Diegelmann RF, Krummel TM et al. (1993) Hyaluronic acid modulates proliferation, collagen and protein synthesis of cultured fetal fibroblasts. Matrix 13: 441-6
35. Oliver N, Sternlicht M, Gerritsen K et al. (2010) Could aging human skin use a connective tissue growth factor boost to increase collagen content?. J Invest Dermatol 130: 338-41
36. Olson EN, Nordheim A (2010) Linking actin dynamics and gene transcription to drive cellular motile functions. Nat Rev Mol Cell Biol 11: 353-65
37. Orringer JS, Rittie L, Hamilton T et al. (2011) Intraepidermal erbium: YAG laser resurfacing: impact on the dermal matrix. J Am Acad Dermatol 64: 119-28
38. Quan T, He T, Kang S et al. (2002a) Connective tissue growth factor: expression in human skin in vivo and inhibition by ultraviolet irradiation. J Invest Dermatol 118: 402-8
39. Quan T, He T, Kang S et al. (2002b) Ultraviolet irradiation alters transforming growth factor beta/smad pathway in human skin in vivo. J Invest Dermatol 119: 499-506
40. Quan T, He T, Kang S et al. (2004) Solar ultraviolet irradiation reduces collagen in photoaged human skin by blocking transforming growth factor-beta type II receptor/Smad signaling. Am J Pathol 165: 741-51
41. Quan T, He T, Shao Y et al. (2006) Elevated cysteine-rich 61 mediates aberrant collagen homeostasis in chronologically aged and photoaged human skin. Am J Pathol 169: 482-90
42. Quan T, Qin Z, Xia W et al. (2009) Matrix-degrading metalloproteinases in photoaging. J Investig Dermatol Symp Proc 14: 20-4
43. Quan T, Shao Y, He T et al. (2010) Reduced expression of connective tissue growth factor (CTGF/CCN2) mediates collagen loss in chronologically aged human skin. J Invest Dermatol 130: 415-24
44. Reichelt J (2007) Mechanotransduction of keratinocytes in culture and in the epidermis. Eur J Cell Biol 86: 807-16
45. Rittie L, Fisher GJ (2002) UV-light-induced signal cascades and skin aging. Ageing Res Rev 1: 705-20
46. Ruoslahti E (1997) Stretching is good for a cell. Science 276: 1345-6
47. Shirakata Y (2010) Regulation of epidermal keratinocytes by growth factors. J Dermatol Sci 59: 73-80
48. Silver FH, Siperko LM, Seehra GP (2003) Mechanobiology of force transduction in dermal tissue. Skin Res Technol 9: 3-23
49. Skutek M, van Griensven M, Zeichen J et al. (2001) Cyclic mechanical stretching modulates secretion pattern of growth factors in human tendon fibroblasts. Eur J Appl Physiol 86: 48-52
50. Uitto J, Bernstein EF (1998) Molecular mechanisms of cutaneous aging: connective tissue alterations in the dermis. J Investig Dermatol Symp Proc 3: 41-4
51. Varani J, Dame MK, Rittie L et al. (2006) Decreased collagen production in chronologically aged skin: roles of age-dependent alteration in fibroblast function and defective mechanical stimulation. Am J Pathol 168: 1861-8
52. Varani J, Perone P, Fligiel SE et al. (2002) Inhibition of type I procollagen production in photodamage: correlation between presence of high molecular weight collagen fragments and reduced procollagen synthesis. J Invest Dermatol 119: 122-9
53. Varani J, Schuger L, Dame MK et al. (2004) Reduced fibroblast interaction with intact collagen as a mechanism for depressed collagen synthesis in photodamaged skin. J Invest Dermatol 122: 1471-9
54. Varani J, Spearman D, Perone P et al. (2001) Inhibition of type I procollagen synthesis by damaged collagen in photoaged skin and by collagenasedegraded collagen in vitro. Am J Pathol 158: 931-42
55. Varga J, Jimenez SA (1995) Modulation of collagen gene expression: its relation to fibrosis in systemic sclerosis and other disorders. Ann Intern Med 122: 60-2
56. Verzijl N, DeGroot J, Thorpe SR et al. (2000) Effect of collagen turnover on the accumulation of advanced glycation end products. J Biol Chem 275: 39027-31
57. Wang F, Garza LA, Kang S et al. (2007) In vivo stimulation of de novo collagen production caused by cross-linked hyaluronic acid dermal filler injections in photodamaged human skin. Arch Dermatol 143: 155-63
58. Zouboulis CC, Makrantonaki E (2011) Clinical aspects and molecular diagnostics of skin aging. Clin Dermatol 29: 3-14