A keratinocyte hypermotility/growth-arrest response involving laminin 5 and p16INK4A activated in wound healing and senescence

American Journal of Pathology

Volumn 168, Issue 6, 2006, Pages 1821-1837

  Natarajan, Easwar ^a,b,d   Omobono II, John D ^a,b   Guo, Zongyou ^a,b   Hopkinson, Susan ^c   Lazar, Alexander J F ^a,e   Brenn, Thomas ^a   Jones, Jonathan C ^c   Rheinwald, James G ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

^d UNIVERSITY OF CONNECTICUT SCHOOL OF DENTAL MEDICINE   (United States)

^e UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 1; KALININ; KI 67 ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN P16INK4A; PROTEIN P53; SCLEROPROTEIN; SMAD PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1;

ARTICLE; CELL GROWTH; CELL IMMORTALIZATION; CELL MIGRATION; CELL SURVIVAL; CONTROLLED STUDY; CULTURE MEDIUM; GROWTH INHIBITION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; KERATINOCYTE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENESCENCE; TELOMERE; WESTERN BLOTTING; WOUND HEALING;

EID: 33744732501     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2006.051027     Document Type: Article

References (76)

1. Carter WG, Ryan MC, Gahr PJ: Epiligrin, a new cell adhesion ligand for integrin α3β1 in epithelial basement membranes. Cell 1991, 65:599-610
2. Rousselle P, Lunstrum GP, Keene DR, Burgeson RE: Kalinin: an epithelium-specific basement membrane adhesion molecule that is a component of anchoring filaments. J Cell Biol 1991, 114:567-576
3. Marinkovich MP, Lunstrum GP, Burgeson RE: The anchoring filament protein kalinin is synthesized and secreted as a high molecular weight precursor. J Biol Chem 1992, 267:17900-17906
4. Goldfinger LE, Stack MS, Jones JC: Processing of laminin-5 and its functional consequences: role of plasmin and tissue-type plasminogen activator. J Cell Biol 1998, 141:255-265
5. Amano S, Scott IC, Takahara K, Koch M, Champliaud MF, Gerecke DR, Keene DR, Hudson DL, Nishiyama T, Lee S, Greenspan DS, Burgeson RE: Bone morphogenetic protein 1 is an extracellular processing enzyme of the laminin 5 γ2 chain. J Biol Chem 2000, 275:22728-22735
6. Jones JC, Hopkinson SB, Goldfinger LE: Structure and assembly of hemidesmosomes. Bioessays 1998, 20:488-494
7. Larjava H, Salo T, Haapasalmi K, Kramer RH, Heino J: Expression of integrins and basement membrane components by wound keratinocytes. J Clin Invest 1993, 92:1425-1435
8. Dabelsteen E, Gron B, Mandel U, Mackenzie I: Altered expression of epithelial cell surface glycoconjugates and intermediate filaments at the margins of mucosal wounds. J Invest Dermatol 1998, 111:592-597
9. Kainulainen T, Hakkinen L, Hamidi S, Larjava K, Kallioinen M, Peltonen J, Salo T, Larjava H, Oikarinen A: Laminin-5 expression is independent of the injury and the microenvironment during reepithelialization of wounds. J Histochem Cytochem 1998, 46:353-360
10. Goldfinger LE, Hopkinson SB, deHart GW, Collawn S, Couchman JR, Jones JC: The α3 laminin subunit, α6β4 and α3β1 integrin coordinately regulate wound healing in cultured epithelial cells and in the skin. J Cell Sci 1999, 112:2615-2629
11. Nguyen BP, Ryan MC, Gil SG, Carter WG: Deposition of laminin 5 in epidermal wounds regulates integrin signaling and adhesion. Curr Opin Cell Biol 2000, 12:554-562
12. Hintermann E, Bilban M, Sharabi A, Quaranta V: Inhibitory role of α6β4-associated erbB-2 and phosphoinositide 3-kinase in keratinocyte haptotactic migration dependent on α3β1 integrin. J Cell Biol 2001, 153:465-478
13. Frank DE, Carter WG: Laminin 5 deposition regulates keratinocyte polarization and persistent migration. J Cell Sci 2004, 117:1351-1363
14. Pyke C, Salo S, Ralfkiaer E, Romer J, Dano K, Tryggvason K: Laminin-5 is a marker of invading cancer cells in some human carcinomas and is coexpressed with the receptor for urokinase plasminogen activator in budding cancer cells in colon adenocarcinomas. Cancer Res 1995, 55:4132-4139
15. Kainulainen T, Autio-Harmainen H, Oikarinen A, Salo S, Tryggvason K, Salo T: Altered distribution and synthesis of laminin-5 (kalinin) in oral lichen planus, epithelial dysplasias and squamous cell carcinomas. Br J Dermatol 1997, 136:331-336
16. Lohi J: Laminin-5 in the progression of carcinomas. Int J Cancer 2001, 94:763-767
17. INK4A and laminin 5 γ2 by microinvasive and superficial squamous cell carcinomas in vivo and by migrating wound and senescent keratinocytes in culture. Am J Pathol 2003, 163:477-491
18. Serrano M, Hannon GJ, Beach D: A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature 1993, 366:704-707
19. INK4/MTS1 tumour suppressor gene product. EMBO J 1995, 14:503-511
20. INK4A expression in normal human adult and infant tissues. Lab Invest 1999, 79:1137-1143
21. INK4 are complimentary surrogate biomarkers for human papilloma virus-related cervical neoplasia. Am J Surg Pathol 2001, 25:884-891
22. MTS-1/CDKN2/INK4a in cancer progression. Exp Cell Res 2001, 264:42-55
23. Garlick JA, Taichman LB: Fate of human keratinocytes during reepithelialization in an organotypic culture model. Lab Invest 1994, 70:916-924
24. Bartkova J, Gron B, Dabelsteen E, Bartek J: Cell-cycle regulatory proteins in human wound healing. Arch Oral Biol 2003, 48:125-132
25. INK4A and an intact Rb pathway illustrated by a model system of basal cell carcinoma. Cancer Res 2003, 63:1737-1742
26. INK4A with human head and neck keratinocyte replicative senescence: relationship of dysfunction to immortality and neoplasia. Oncogene 1996, 13:561-568
27. INK4A inactivation and telomerase activity are required to immortalize human epithelial cells. Nature 1998, 396:84-88
28. INK4A- enforced mechanism that limits life span become immortal yet retain normal growth and differentiation characteristics. Mol Cell Biol 2000, 20:1436-1447
29. INK4A- and p53-dependent keratinocyte senescence mechanism that limits replicative potential independent of telomere status. Mol Cell Biol 2002, 22:5157-5172
30. Rheinwald JG, Beckett MA: Tumorigenic keratinocyte lines requiring anchorage and fibroblast support cultures from human squamous cell carcinomas. Cancer Res 1981, 41:1657-1663
31. Pirisi L, Yasumoto S, Feller M, Doniger J, DiPaolo JA: Transformation of human fibroblasts and keratinocytes with human papillomavirus type 16 DNA. J Virol 1987, 61:1061-1066
32. Rheinwald JG, Green H: Serial cultivation of strains of human epidermal keratinocytes: the formation of keratinizing colonies from single cells. Cell 1975, 6:331-343
33. Allen-Hoffmann BL, Rheinwald JG: Polycyclic aromatic hydrocarbon mutagenesis of human epidermal keratinocytes in culture. Proc Natl Acad Sci USA 1984, 81:7802-7806
34. Izumi K, Hirao Y, Hopp L, Oyasu R: In vitro induction of ornithine decarboxylase in urinary bladder carcinoma cells. Cancer Res 1981, 41:405-409
35. Hormia M, Falk-Marzillier J, Plopper G, Tamura RN, Jones JC, Quaranta V: Rapid spreading and mature hemidesmosome formation in HaCaT keratinocytes induced by incubation with soluble larninin-5r. J Invest Dermatol 1995, 105:557-561
36. Baker SE, DiPasquale AP, Stock EL, Quaranta V, Fitchmun M, Jones JC: Morphogenetic effects of soluble laminin-5 on cultured epithelial cells and tissue explants. Exp Cell Res 1996, 228:262-270
37. Singh J, Ling LE, Sawyer JS, Lee WC, Zhang F, Yingling JM: Transforming the TGFβ pathway: convergence of distinct lead generation strategies on a novel kinase pharmacophore for TβRI (ALK5). Curr Opin Drug Discov Dev 2004, 7:437-445
38. Peng SB, Yan L, Xia X, Watkins SA, Brooks HB, Beight D, Herron DK, Jones ML, Lampe JW, McMillen WT, Mort N, Sawyer JS, Yingling JM: Kinetic characterization of novel pyrazole TGF-β receptor I kinase inhibitors and their blockade of the epithelial-mesenchymal transition. Biochemistry 2005, 44:2293-2304
39. Mizushima H, Koshikawa N, Moriyama K, Takamura H, Nagashima Y, Hirahara F, Miyazaki K: Wide distribution of laminin-5 γ2 chain in basement membranes of various human tissues. Horm Res 1998, 50(Suppl 2):7-14
40. Pierreux CE, Nicolas FJ, Hill CS: Transforming growth factor β-independent shuttling of Smad4 between the cytoplasm and nucleus. Mol Cell Biol 2000, 20:9041-9054
41. INK4A and laminin 5 by keratinocytes: a wound-healing response coupling hypermotility with growth arrest that goes awry during epithelial neoplastic progression. J Invest Dermatol Symp Proc 2005, 10:72-85
42. Lenander C, Roblick UJ, Habermann JK, Ost A, Tryggvason K, Auer G: Laminin 5 γ2 chain expression: a marker of early invasiveness in colorectal adenomas. Mol Pathol 2003, 56:342-346
43. Daniels JT, Geerling G, Alexander RA, Murphy G, Khaw PT, Saarialho-Kere U: Temporal and spatial expression of matrix metalloproteinases during wound healing of human corneal tissue. Exp Eye Res 2003, 77:653-664
44. Giannelli G, Falk-Marzillier J, Schiraldi O, Stetler-Stevenson WG, Quaranta V: Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5. Science 1997, 277:225-228
45. Zhang K, Kramer RH: Laminin 5 deposition promotes keratinocyte motility. Exp Cell Res 1996, 227:309-322
46. Li W, Nadelman C, Henry G, Fan J, Muellenhoff M, Medina E, Gratch NS, Chen M, Han J, Woodley D: The p38-MAPK/SAPK pathway is required for human keratinocyte migration on dermal collagen. J Invest Dermatol 2001, 117:1601-1611
47. Henry G, Li W, Garner W, Woodley DT: Migration of human keratinocytes in plasma and serum and wound re-epithelialisation. Lancet 2003, 361:574-576
48. Nickoloff BJ, Chaturvedi V, Bacon P, Qin JZ, Denning MF, Diaz MO: Id-1 delays senescence but does not immortalize keratinocytes. J Biol Chem 2000, 275:27501-27504
49. Kane CJ, Hebda PA, Mansbridge JN, Hanawalt PC: Direct evidence for spatial and temporal regulation of transforming growth factor β1 expression during cutaneous wound healing. J Cell Physiol 1991, 148:157-173
50. Gailit J, Welch MP, Clark RA: TGFβ1 stimulates expression of keratinocyte integrins during re-epithelialization of cutaneous wounds. J Invest Dermatol 1994, 103:221-227
51. Decline F, Okamoto O, Mallein-Gerin F, Helbert B, Bernaud J, Rigal D, Rousselle P: Keratinocyte motility induced by TGFβ1 is accompanied by dramatic changes in cellular interactions with laminin 5. Cell Motil Cytoskeleton 2003, 54:64-80
52. Shipley GD, Pittelkow MR, Wille JJ Jr, Scott RE, Moses HL: Reversible inhibition of normal human prokeratinocyte proliferation by type β transforming growth factor-growth inhibitor in serum-free medium. Cancer Res 1986, 46:2068-2071
53. Rollins BJ, O'Connell TM, Bennett G, Burton LE, Stiles CD, Rheinwald JG: Environment-dependent growth inhibition of human epidermal keratinocytes by recombinant human transforming growth factor-β. J Cell Physiol 1989, 139:455-462
54. McCawley LJ, O'Brien P, Hudson LG: Epidermal growth factor (EGF)- and scatter factor/hepatocyte growth factor (SF/HGF)-mediated keratinocyte migration is coincident with induction of matrix metalloproteinase (MMP)-9. J Cell Physiol 1998, 176:255-265
55. Mainiero F, Pepe A, Yeon M, Ren Y, Giancotti FG: The intracellular functions of α6β4 integrin are regulated by EGF. J Cell Biol 1996, 134:241-253
56. Shi Y, Massague J: Mechanisms of TGFβ signaling from cell membrane to the nucleus. Cell 2003, 113:685-700
57. ten Dijke P, Hill CS: New insights into TGFβ-Smad signalling. Trends Biochem Sci 2004, 29:265-273
58. Xu L, Massague J: Nucleocytoplasmic shuttling of signal transducers. Nat Rev Mol Cell Biol 2004, 5:209-219
59. Kamaraju AK, Roberts AB: Role of Rho/ROCK and p38 MAP kinase pathways in transforming growth factor-β-mediated Smad-dependent growth inhibition of human breast carcinoma cells in vivo. J Biol Chem 2005, 280:1024-1036
60. Bhowmick NA, Ghiassi M, Aakre M, Brown K, Singh V, Moses HL: TGF-beta-induced RhoA and p160ROCK activation is involved in the inhibition of Cdc25A with resultant cell-cycle arrest. Proc Natl Acad Sci USA 2003, 100:15548-15553
61. Reynisdottir I, Polyak K, Iavarone A, Massague J: Kip/Cip and Ink4 Cdk inhibitors cooperate to induce cell cycle arrest in response to TGF-beta. Genes Dev 1995, 9:1831-1845
62. Fortunel NO, Hatzfeld JA, Rosemary PA, Ferraris G, Monier MN, Haydont V, Longuet J, Brethon B, Lim B, Castiel I, Schmidt R, Hatzfeld A: Long-term expansion of human functional epidermal precursor cells: promotion of extensive amplification by low TGFβ1 concentrations. J Cell Sci 2003, 116:4043-4052
63. Ramirez RD, Morales CP, Herbert BS, Rohde JM, Passons C, Shay JW, Wright WE: Putative telomere-independent mechanisms of replicative aging reflect inadequate growth conditions. Genes Dev 2001, 15:398-403
64. Kikkawa Y, Umeda M, Miyazaki K: Marked stimulation of cell adhesion and motility by ladsin, a laminin-like scatter factor. J Biochem (Tokyo) 1994, 116:862-869
65. Russell AJ, Fincher EF, Millman L, Smith R, Vela V, Waterman EA, Dey CN, Guide S, Weaver VM, Marinkovich MP: α6β4 integrin regulates keratinocyte chemotaxis through differential GTPase activation and antagonism of α3β1 integrin. J Cell Sci 2003, 116:3543-3556
66. Geuijen CA, Sonnenberg A: Dynamics of the α6β4 integrin in keratinocytes. Mol Biol Cell 2002, 13:3845-3858
67. deHart GW, Healy KE, Jones JC: The role of α3β1 integrin in determining the supramolecular organization of laminin-5 in the extracellular matrix of keratinocytes. Exp Cell Res 2003, 283:67-79
68. Li W, Henry G, Fan J, Bandyopadhyay B, Pang K, Garner W, Chen M, Woodley DT: Signals that initiate, augment, and provide directionality for human keratinocyte motility. J Invest Dermatol 2004, 123:622-633
69. Zambruno G, Marchisio PC, Marconi A, Vaschieri C, Melchiori A, Giannetti A, De Luca M: Transforming growth factor β1 modulates β1 and β5 integrin receptors and induces the de novo expression of the αvβ6 heterodimer in normal human keratinocytes: implications for wound healing. J Cell Biol 1995, 129:853-865
70. Laping NJ, Grygielko E, Mathur A, Butter S, Bomberger J, Tweed C, Martin W, Fornwald J, Lehr R, Harling J, Gaster L, Callahan JF, Olson BA: Inhibition of transforming growth factor TGFβ1-induced extracellular matrix with a novel inhibitor of the TGFβ type I receptor kinase activity: sB-431542. Mol Pharmacol 2002, 62:58-64
71. Harper EG, Alvares SM, Carter WG: Wounding activates p38 map kinase and activation transcription factor 3 in leading keratinocytes. J Cell Sci 2005, 118:3471-3485
72. Chattopadhyay N, Wang Z, Ashman LK, Brady-Kalnay SM, Kreidberg JA: α3β1 integrin-CD151, a component of the cadherin-catenin complex, regulates PTPmu expression and cell-cell adhesion. J Cell Biol 2003, 163:1351-1362
73. Cowin AJ, Adams D, Geary SM, Wright MD, Jones JC, Ashman LK: Wound healing is defective in mice lacking tetraspanin CD151. J Invest Dermatol 2006, 126:680-689
74. INK4A and migratory genes in culture conditions that lead to premature senescence in human keratinocytes. J Invest Dermatol 2005, 125:499-509
75. Lindberg K, Rheinwald JG: Three distinct keratinocyte subtypes identified in human oral epithelium by their patterns of keratin expression in culture and in xenografts. Differentiation 1990, 45:230-241
76. Weichselbaum R, Dahlberg W, Little JB, Ervin TJ, Miller D, Hellman S, Rheinwald JG: Cellular X-ray repair parameters of early passage squamous cell carcinoma lines derived from patients with known responses to radiotherapy. Br J Cancer 1984, 49:595-601