An activating β1 integrin mutation increases the conversion of benign to malignant skin tumors

Cancer Research

Volumn 69, Issue 4, 2009, Pages 1334-1342

  Ferreira, Manuela ^a,b   Fujiwara, Hironobu ^a   Morita, Kazumasa ^c   Watt, Fiona M ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c TENRI HOSPITAL   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BETA1 INTEGRIN; CYTOKERATIN 14; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN SUBUNIT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; EPIDERMIS CELL; FEMALE; GENE MUTATION; GENETIC POLYMORPHISM; GENETIC VARIABILITY; IN VITRO STUDY; KERATINOCYTE; MALE; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; SKIN CANCER; SQUAMOUS CELL CARCINOMA; TRANSGENIC MOUSE; ANIMAL; CELL ADHESION; CELL DIVISION; CYTOLOGY; FLOW CYTOMETRY; GENETICS; HETEROZYGOTE DETECTION; HUMAN; IN SITU HYBRIDIZATION; MUTATION; PATHOLOGY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; SKIN; SKIN TUMOR;

ANIMALS; ANTIGENS, CD29; CARCINOMA, SQUAMOUS CELL; CELL ADHESION; CELL DIFFERENTIATION; CELL DIVISION; FEMALE; FLOW CYTOMETRY; HETEROZYGOTE DETECTION; HUMANS; IN SITU HYBRIDIZATION; KERATINOCYTES; MICE; MICE, TRANSGENIC; MUTATION; POLYMERASE CHAIN REACTION; POLYMORPHISM, GENETIC; SKIN; SKIN NEOPLASMS;

EID: 60549107350     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-3051     Document Type: Article

References (48)

1. Watt FM. Role of integrins in regulating epidermal adhesion, growth and differentiation. EMBO J 2002;21:3919-26.
2. Jones PH, Watt FM. Separation of human epidermal stem cells from transit amplifying cells on the basis of differences in integrin function and expression. Cell 1993;73:713-24.
3. Jones PH, Harper S, Watt FM. Stem cell patterning and fate in human epidermis. Cell 1995;80:83-93.
4. Jensen UB, Lowell S, Watt FM. The spatial relationship between stem cells and their progeny in the basal layer of human epidermis: a new view based on whole-mount labelling and lineage analysis. Development 1999;126:2409-18.
5. Zhu AJ, Haase I, Watt FM. Signaling via β1 integrins and mitogen-activated protein kinase determines human epidermal stem cell fate in vitro. Proc Natl Acad Sci U S A 1999;96:6728-33.
6. Janes SM, Watt FM. Switch from αvβ5to αvβ6 integrin expression protects squamous cell carcinomas from anoikis. J Cell Biol 2004;166:419-31.
7. Adams JC, Watt FM. Fibronectin inhibits the terminal differentiation of human keratinocytes. Nature 1989;340:307-9.
8. Levy L, Broad S, Diekmann D, Evans RD, Watt FM. β1 Integrins regulate keratinocyte adhesion and differentiation by distinct mechanisms. Mol Biol Cell 2000;11:453-66.
9. Benitah SA, Frye M, Glogauer M, Watt FM. Stem cell depletion through epidermal deletion of Rac1. Science 2005;309:933-5.
10. Watt FM, Frye M, Benitah SA. MYC in mammalian epidermis: how can an oncogene stimulate differentiation? Nat Rev Cancer 2007;8:234-42.
11. Guo W, Giancotti FG. Integrin signalling during tumour progression. Nat Rev Mol Cell Biol 2004;5:816-26.
12. Brakebusch C, Fassler R. β1 Integrin function in vivo: adhesion, migration and more. Cancer Metastasis Rev 2005;24:403-11.
13. Janes SM, Watt FM. New roles for integrins in squamous-cellcarcinoma. Nat RevCancer 2006;6:175-83.
14. Wilhelmsen K, Litjens SH, Sonnenberg A. Multiple functions of the integrin a6β4 in epidermal homeostasis and tumorigenesis. Mol Cell Biol 2006;26:2877-86.
15. Hobbs RM, Watt FM. Regulation of interleukin-1α expression by integrins and epidermal growth factor receptor in keratinocytes from a mouse model of inflammatory skin disease. J Biol Chem 2003;278:19798-807.
16. Hobbs RM, Silva-Vargas V, Groves R, Watt FM. Expression of activated MEK1 in differentiating epidermal cells is sufficient to generate hyperproliferative and inflammatory skin lesions. J Invest Dermatol 2004;123:503-15.
17. Owens DM, Watt FM. Influence of β1 integrins on epidermal squamous cell carcinoma formation in a transgenic mouse model: α3β1, but not α2β1, suppresses malignant conversion. Cancer Res 2001;61:5248-54.
18. Owens DM, Broad S, Yan X, Benitah SA, Watt FM. Suprabasal α5β1 integrin expression stimulates formation of epidermal squamous cell carcinomas without disrupting TGFβ signaling or inducing spindle cell tumors. Mol Carcinog 2005;44:60-6.
19. Owens DM, Romero MR, Gardner C, Watt FM. Suprabasal α6β4 integrin expression in epidermis results in enhanced tumourigenesis and disruption of TGFβ signalling. J Cell Sci 2003;116:3783-91.
20. Evans RD, Perkins VC, Henry A, Stephens PE, Robinson MK, Watt FM. A tumor-associated β1 integrin mutation that abrogates epithelial differentiation control. J Cell Biol 2003;160:589-96.
21. Takagi J, Kamata T, Meredith J, Puzon-McLaughlin W, Takada Y. Changing ligand specificities of αvβ1 and αvβ3 integrins by swapping a short diverse sequence of the β subunit. J Biol Chem 1997;272:19794-800.
22. Luo BH, Carman CV, Springer TA. Structural basis of integrin regulation and signaling. Annu Rev Immunol 2007;25:619-47.
23. Evans RD, Jones J, Taylor C, Watt FM. Sequence variation in the I-like domain of the β1 integrin subunit in human oral squamous cell carcinomas. Cancer Lett 2004;213:189-94.
24. Gebhardt A, Frye M, Herold S, et al. Myc regulates keratinocyte adhesion and differentiation via complex formation with Miz1. J Cell Biol 2006;172:139-49.
25. Braun KM, Niemann C, Jensen UB, Sundberg JP, Silva-Vargas V, Watt FM. Manipulation of stem cell proliferation and lineage commitment: visualisation of label-retaining cells in wholemounts of mouse epidermis. Development 2003;130:5241-55.
26. Carroll JM, Romero MR, Watt FM. Suprabasal integrin expression in the epidermis of transgenic mice results in developmental defects and a phenotype resembling psoriasis. Cell 1995;83:957-68.
27. Adams JC, Watt FM. Changes in keratinocyte adhesion during terminal differentiation: reduction in fibronectin binding precedes α5β1 integrin loss from the cell surface. Cell 1990;63:425-35.
28. Silva-Vargas V, Lo Celso C, Giangreco A, et al. Beta-catenin and Hedgehog signal strength can specify number and location of hair follicles in adult epidermis without recruitment of bulge stem cells. Dev Cell 2005;9:121-31.
29. Owens DM, Watt FM. Contribution of stem cells and differentiated cells to epidermal tumours. Nat Rev Cancer 2003;3:444-51.
30. Levy L, Broad S, Zhu AJ, et al. Optimised retroviral infection of human epidermal keratino-cytes: long-term expression of transduced integrin gene following grafting on to SCID mice. Gene Ther 1998;5:913-22.
31. Hotchin NA, Watt FM. Transcriptional and post-translational regulation of β1 integrin expression during keratinocyte terminal differentiation. J Biol Chem 1992;267:14852-8.
32. Cotsarelis G. Epithelial stem cells: a folliculocentric view. J Invest Dermatol 2006;126:1459-68.
33. Popova NV, Tryson KA, Wu KQ, Morris RJ. Evidence that the keratinocyte colony number is genetically controlled. Exp Dermatol 2002;11:503-8.
34. Haase I, Hobbs RM, Romero MR, Broad S, Watt FM. A role for mitogen-activated protein kinase activation by integrins in the pathogenesis of psoriasis. J Clin Invest 2001;108:527-36.
35. Brakebusch C, Grose R, Quondamatteo F, et al. Skin and hair follicle integrity is crucially dependent on β1 integrin expression on keratinocytes. EMBO J 2000;19:3990-4003.
36. Raghavan S, Bauer C, Mundschau G, Li Q, Fuchs E. Conditional ablation of β1 integrin in skin. Severe defects in epidermal proliferation, basement membrane formation, and hair follicle invagination. J Cell Biol 2000;150:1149-60.
37. Lopez-Róvira T, Silva-Vargas V, Watt FM. Different consequences of β1 integrin deletion in neonatal and adult mouse epidermis reveal a context-dependent role of integrins in regulating proliferation, differentiation, and intercellular communication. J Invest Dermatol 2005;125:1215-27.
38. Taddei I, Deugnier MA, Faraldo MM, et al. β1 integrin deletion from the basal compartment of the mammary epithelium affects stem cells. Nat Cell Biol 2008;10:716-22.
39. White DE, Kurpios NA, Zuo D, et al. Targeted disruption of β1-integrin in a transgenic mouse model of human breast cancer reveals an essential role in mammary tumor induction. Cancer Cell 2004;6:159-70.
40. Stoler AB, Stenback F, Balmain A. The conversion of mouse skin squamous cell carcinomas to spindle cell carcinomas is a recessive event. J Cell Biol 1993;122:1103-17.
41. Psichari E, Balmain A, Plows D, Zoumpourlis V Pintzas A. High activity of serum response factor in the mesenchymal transition of epithelial tumor cells is regulated by RhoA signaling. J Biol Chem 2002;277:29490-5.
42. Reynolds LE, Conti FJ, Silva R, et al. α3β1 integrin-controlled Smad7 regulates areepithelialization during wound healing in mice. J Clin Invest 2008;118:965-74.
43. Cui W, Fowlis DJ, Bryson S, et al. TGFβ1 inhibits the formationofbenignskintumors,butenhances progression to invasive spindle carcinomas in transgen-ic mice. Cell 1996;86:531-42.
44. Papathoma AS, Zoumpourlis V, Balmain A, Pintzas A. Role of matrix metalloproteinase-9 in progression of mouse skin carcinogenesis. Mol Carcinog 2001;31:74-82.
45. Scholl FA, Dumesic PA, Khavari PA. Mek1 alters epidermal growth and differentiation. Cancer Res 2004;64:6035-40.
46. McLean GW, Komiyama NH, Serrels B, et al. Specific deletion of focal adhesion kinase suppresses tumor formation and blocks malignant progression. Genes Dev 2004;18:2998-3003.
47. Nath SK, Han S, Kim-Howard X, et al. A non-synonymous functional variant in integrin-α(M) (encoded by ITGAM) is associated with systemic lupus erythematosus. Nat Genet 2008;40:152-4.
48. Harley JB, Alarcon-Riquelme ME, Criswell LA, et al. Genome-wide association scan in women with systemic lupus erythematosus identifies susceptibility variants in ITGAM, PXK, KIAA1542 and other loci. Nat Genet 2008;40:204-10.