Aging fibroblasts resist phenotypic maturation because of impaired hyaluronan-dependent CD44/epidermal growth factor receptor signaling

American Journal of Pathology

Volumn 176, Issue 3, 2010, Pages 1215-1228

  Simpson, Russell M L ^a   Wells, Alan ^b   Thomas, David ^a   Stephens, Philip ^a   Steadman, Robert ^a   Phillips, Aled ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; EPIDERMAL GROWTH FACTOR RECEPTOR; HERMES ANTIGEN; HYALURONAN SYNTHASE 2; HYALURONIC ACID; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; SMAD PROTEIN; SYNTHETASE; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ARTICLE; CELL AGING; CONTROLLED STUDY; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPRECIPITATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

EID: 77749242728     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.090802     Document Type: Article

References (55)

1. Ashcroft GS, Mills SJ, Ashworth JJ: Ageing and wound healing. Biogerontology 2002, 3:337-345
2. Ashcroft GS, Roberts AB: Loss of Smad3 modulates wound healing. Cytokine Growth Factor Rev 2000, 11:125-131
3. Gabbiani G: The myofibroblast in wound healing and fibrocontractive diseases. J Pathol 2003, 200:500-503
4. Shiraha H, Gupta K, Drabik K, Wells A: Aging fibroblasts present reduced epidermal growth factor (EGF) responsiveness due to preferential loss of EGF receptors. J Biol Chem 2000, 275:19343-19351
5. Ashcroft GS, Horan MA, Ferguson MW: The effects of ageing on cutaneous wound healing in mammals. J Anat 1995, 187:1-26
6. Simpson R, Meran S, Thomas D, Stephens P, Bowen T, Steadman R, Phillips A: Age related changes in peri-cellular hyaluronan organisation leads to impaired dermal fibroblast to myofibroblast differentiation. Am J Pathol 2009, 175:1915-1928
7. Meran S, Thomas D, Stephens P, Martin J, Bowen T, Phillips A, Steadman R: Involvement of hyaluronan in regulation of fibroblast phenotype. J Biol Chem 2007, 282:25687-25697
8. Meran S, Thomas DW, Stephens P, Enoch S, Martin J, Steadman R, Phillips AO: Hyaluronan facilitates transforming growth factor-β1-mediated fibroblast proliferation. J Biol Chem 2008, 283:6530-6545
9. Webber J, Jenkins RH, Meran S, Phillips A, Steadman R: Modulation of TGFβ1-dependent myofibroblast differentiation by hyaluronan. Am J Pathol 2009, 175:148-160
10. Spicer AP, Kaback LA, Smith TJ, Seldin MF: Molecular cloning and characterisation of the human and mouse UDP-glucose dehydrogenase genes. J Biol Chem 1998, 271:25117-15124
11. Spicer AP, McDonald JA: Characterisation and molecular evolution of a vertebrate hyaluronan synthase gene family. J Biol Chem 1998, 272:1923-1932
12. Kosaki R, Watanabe K, Yamaguchi Y: Overproduction of hyaluronan by expression of the hyaluronan synthase Has2 enhances anchorage independent growth. Cancer Res 1999, 59:1141-1145
13. Itano N, Atsumi F, Sawai T, Yamada Y, Miyaishi O, Senga T, Hamagu-chi M, Kimata K: Abnormal accumulation of hyaluronan matrix diminishes contact inhibition of cell growth and promotes cell migration, Proc Natl Acad Sci USA 2002, 99:3609-3614
14. Ito T, Williams JD, Al-Assaf S, Phillips GO, Phillips AO: Hyaluronan and proximal tubular epithelial cell migration. Kidney Int 2004, 65:823-833
15. Legg JW, Lewis CA, Parsons M, Ng T, Isacke CM: A novel PKC-regulated mechanism controls CD44 ezrin association and directional cell motility. Nat Cell Biol 2002, 4:399-407
16. Zoltan-Jones A, Huang L, Ghatak S, Toole BP: Elevated hyaluronan production induces mesenchymal and transformed properties in epithelial cells. J Biol Chem 2003, 278:45801-45810
17. Brecht M, Mayer U, Schlosser E, Prehm P: Increased hyaluronate synthesis is required for fibroblast detachment and mitosis. Biochem J 1986, 239:445-450
18. Evanko SP, Angello JC, Wight TN: Formation of hyaluronan- and versican-rich pericellular matrix is required for proliferation and migration of vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 1999, 19:1004-1013
19. Ito T, Williams JD, Fraser DJ, Phillips AO: Hyaluronan attenuates TGF-β1 mediated signalling in renal proximal tubular epithelial cells. Am J Pathol 2004, 164:1979-1988
20. Ito T, Williams JD, Fraser DJ, Phillips AO: Hyaluronan regulates TGF-β1 receptor compartmentalisation. J Biol Chem 2004, 279:25326-25332
21. Shi Y, Massague J: Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 2003, 113:685-700
22. Miyazawa K, Shinozaki M, Hara T, Furuya T, Miyazono K: Two major Smad pathways in TGF-β superfamily signalling. Genes Cells 2002, 7:1191-1204
23. Bourguignon LY, Singleton PA, Zhu H, Zhou B: Hyaluronan promotes signaling interaction between CD44 and the transforming growth factor β receptor I in metastatic breast tumor cells. J Biol Chem 2002, 277:39703-39712
24. Derynck R, Zhang YE: Smad-dependent and Smad-independent pathways in TGF-β family signalling. Nature 2003, 425:577-584
25. Grände M, Franzen A, Karlsson JO, Ericson LE, Heldin NE, Nilsson M: Transforming growth factor-β and epidermal growth factor synergistically stimulate epithelial to mesenchymal transition (EMT) through a MEK-dependent mechanism in primary cultured pig thyrocytes. J Cell Sci 2002, 115:4227-4236
26. Song K, Krebs TL, Danielpour D: Novel permissive role of EGF in TGF-β signaling and growth suppression: Mediation by stabilization of TGF-β receptor type II. J Biol Chem 2006, 281:7765-7774
27. Docherty NG, O'Sullivan OE, Healy DA, Murphy M, O'Neill AJ, Fitzpatrick JM, Watson RWG: TGF-β1-induced EMT can occur independently of its proapoptotic effects and is aided by EGF receptor activation. Am J Physiol Renal Physiol 2006, 290:F1202-F1212
28. Tian Y-C, Chen Y-C, Chang C-T, Hung C-C, Wu M-S, Phillips A, Yang C-W: Epidermal growth factor and transforming growth factor-β1 enhance HK-2 cell migration through a synergistic increase of matrix metalloproteinase and sustained activation of ERK signaling pathway. Exp Cell Res 2007, 313:2367-2377
29. Uttamsingh S, Bao X, Nguyen KT, Bhanot M, Gong J, Chan JL-K, Liu FY, Chu TT: Synergistic effect between EGF and TFG-β1 in inducing oncogenic properties of intestinal epithelial cells. Oncogene 2008, 27:2626-2634
30. He J, Bazan HEP: Epidermal growth factor synergism with TGF-β1 via PI-3 kinase activity in corneal keratocyte differentiation. Invest Ophthalmol Vis Sci 2008, 49:2936-2945
31. Tsatas D, Kanagasundaram V, Kaye A, Novak U: EGF receptor modifies cellular responses to hyaluronan in glioblastoma cell lines. J Clin Neurosci 2002, 9:282-288
32. Vigetti D, Viola M, Karousou E, Rizzi M, Moretto P, Genasetti A, Clerici M, Hascall VC, De Luca G, Passi A: Hyaluronan-CD44-ERK1/2 regulate human aortic smooth muscle cell motility during aging. J Biol Chem 2008, 283:4448-4458
33. Vigetti D, Moretto P, Viola M, Genasetti A, Rizzi M, Karousou E, Pallotti F, De Luca G, Passi A: Matrix metalloproteinase 2 and tissue inhibitors of metalloproteinases regulate human aortic smooth muscle cell migration during in vitro aging. FASEB J 2006, 20:1118-1130
34. Stephens P, Davies KJ, Occleston N, Pleass RD, Kon C, Daniels J, Khaw PT, Thomas DW: Skin and oral fibroblasts exhibit phenotypic differences in extracellular matrix reorganization and matrix metalloproteinase activity. Br J Dermatol 2001, 144:229-237
35. Cristofalo VJ, Allen RG, Pignolo RJ, Martin BG, Beck JC: Relationship between donor age and the replicative lifespan of human cells in culture: a reevaluation. Proc Natl Acad Sci USA 1998, 95:10614-10619
36. Evans RA, Tian YC, Steadman R, Phillips AO: TGF-β1-mediated fibroblast-myofibroblast terminal differentiation-the role of Smad proteins. Exp Cell Res 2003, 282:90-100
37. Saavalainen K, Pasonen-Seppanen S, Dunlop TW, Tammi R, Tammi MI, Carlberg C: The human hyaluronan synthase 2 gene is a primary retinoic acid and epidermal growth factor responding gene. J Biol Chem 2005, 280:14636-14644
38. Wang SJ, Bourguignon LYW: Hyaluronan and the interaction between CD44 and epidermal growth factor receptor in oncogenic signaling and chemotherapy resistance in head and neck cancer. Arch Otolaryngol Head Neck Surg 2006, 132:771-778
39. Humes HD, Beals TF, Cieslinski DA, Sanchez IO, Page TP: Effects of transforming growth factor-β, and transforming growth factor-α, and other growth factors on renal proximal tubule cells. Lab Invest 1991, 64:538-545
40. 2+ signaling, and cytoskeleton modification in head and neck squamous cell carcinoma cells. J Biol Chem 2006, 281:14026-14040
41. Ashcroft GS, Horan MA, Ferguson MW: Aging alters the inflammatory and endothelial cell adhesion molecule profiles during human cutaneous wound healing. Lab Invest 1998, 78:47-58
42. Bruce SA, Deamond SF: Longitudinal study of in vivo wound repair and in vitro cellular senescence of dermal fibroblasts. Exp Gerontol 1991, 26:17-27
43. Pieraggi MJ, Bouissou H, Angelier C, Uhart D, Magnol J, Kokolo J: Le Fibroblaste. Ann Pathol 1985, 5:65-76
44. Rattan SI, Derventzi A: Altered cellular responsiveness during ageing. BioEssays 1991, 13:601-601
45. Reenstra WR, Yaar M, Gilchrest BA: Aging affects epidermal growth factor receptor phosphorylation and traffic kinetics. Exp Cell Res 1996, 227:252-255
46. Jenkins RH, Thomas GJ, Williams JD, Steadman R: Myofibroblastic differentiation leads to hyaluronan accumulation through reduced hyaluronan turnover. J Biol Chem 2004, 279:41453-41460
47. Webber J, Meran S, Steadman R, Phillips AO: Hyaluronan orchestrates TGF-β1 dependent maintenance of myofibroblast phenotype. J Biol Chem 2009, 284:9083-9092
48. Ellis IR, Schor AM, Schor SL: EGF AND TGF-α motogenic activities are mediated by the EGF receptor via distinct matrix-dependent mechanisms. Exp Cell Res 2007, 313:732-741
49. Liu Y, Guyton KZ, Gorospe M, Xu Q, Kokkonen GC, Mock YD, Roth GS, Holbrook NJ: Age-related decline in mitogen-activated protein kinase activity in epidermal growth factor-stimulated rat hepatocytes. J Biol Chem 1996, 271:3604-3607
50. Pasonen-Seppänen SM, Maytin EV, Torronen KJ, Hyttinen JM, Hascall VC, MacCallum DR, Kultti AH, Jokela TA, Tammi MI, Tammi RH: All-trans retinoic acid-induced hyaluronan production and hyperplasia are partly mediated by EGFR signaling in epidermal keratinocytes. J Invest Dermatol 2008, 128:797-807
51. Bourguignon LYW, Gilad E, Peyrollier K: Heregulin-mediated ErbB2-ERK signaling activates hyaluronan synthases leading to CD44-dependent ovarian tumor cell growth and migration. J Biol Chem 2007, 282:19426-19441
52. Herbst RS: Review of epidermal growth factor receptor biology. Int J Radiat Oncol Biol Phys 2004, 59:S21-S26
53. Wells A: EGF receptor. Int J Biochem Cell Biol 1999, 31:637-643
54. Hayashida T, Decaestecker M, Schnaper HW: Cross-talk between ERK MAP kinase and Smad signaling pathways enhances TGF-β-dependent responses in human mesangial cells. FASEB J 2003, 17:1576-1578
55. Zhang M, Fraser D, Phillips A: ERK, p38, and Smad signaling pathways differentially regulate transforming growth factor-β1 autoinduction in proximal tubular epithelial cells. Am J Pathol 2006, 169: 1282-1293