Keratinocyte growth factor induces gene expression signature associated with suppression of malignant phenotype of cutaneous squamous carcinoma cells

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Toriseva, Mervi ^a,b,c   Ala aho, Risto ^a,b   Peltonen, Sirkku ^a   Peltonen, Juha ^c   Grénman, Reidar ^a   Kähäri, Veli Matti ^a,b  

^a TURKU UNIVERSITY HOSPITAL   (Finland)

^b UNIVERSITY OF TURKU   (Finland)

^c UNIVERSITY OF TURKU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; KERATINOCYTE GROWTH FACTOR; KERATINOCYTE GROWTH FACTOR RECEPTOR; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; CXCL10 PROTEIN, HUMAN; DUAL SPECIFICITY PHOSPHATASE; DUAL SPECIFICITY PHOSPHATASE 6; DUSP4 PROTEIN, HUMAN; DUSP6 PROTEIN, HUMAN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GLYCOPROTEIN; IGFBP3 PROTEIN, HUMAN; MATN2 PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE; SCLEROPROTEIN; SOMATOMEDIN BINDING PROTEIN 3;

ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CELL INVASION; CELL PROLIFERATION; CELL STIMULATION; CELL TRANSFORMATION; CLINICAL ARTICLE; CONTROLLED STUDY; CXCL10 GENE; DOWN REGULATION; DUSP4 GENE; DUSP6 GENE; ENZYME ACTIVATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IGFBP3 GENE; KERATINOCYTE; LRIG1 GENE; MATN2 GENE; MMP13 GENE; NUCLEOTIDE SEQUENCE; ONCOGENE H RAS; PHLDA1 GENE; PROTEIN FUNCTION; SKIN CARCINOMA; SPRY4 GENE; SQUAMOUS CELL CARCINOMA; TUMOR SUPPRESSOR GENE; UPREGULATION; CANCER INVASION; DNA MICROARRAY; DRUG EFFECT; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; METABOLISM; PHENOTYPE; REAL TIME POLYMERASE CHAIN REACTION; SKIN TUMOR; TUMOR CELL LINE; WESTERN BLOTTING;

BLOTTING, WESTERN; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CHEMOKINE CXCL10; DUAL SPECIFICITY PHOSPHATASE 6; DUAL-SPECIFICITY PHOSPHATASES; ENZYME-LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR MATRIX PROTEINS; FIBROBLAST GROWTH FACTOR 7; GENE EXPRESSION REGULATION, NEOPLASTIC; GLYCOPROTEINS; HUMANS; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 3; MITOGEN-ACTIVATED PROTEIN KINASE PHOSPHATASES; NEOPLASM INVASIVENESS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; REAL-TIME POLYMERASE CHAIN REACTION; SKIN NEOPLASMS;

EID: 84858025059     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033041     Document Type: Article

References (71)

1. Finch PW, Rubin JS, Miki T, Ron D, Aaronson SA, (1989) Human KGF is FGF-related with properties of a paracrine effector of epithelial cell growth. Science 245: 752-755.
2. Jameson J, Ugarte K, Chen N, Yachi P, Fuchs E, et al. (2002) A role for skin γδT cells in wound repair. Science 296: 747-749.
3. Miki T, Bottaro DP, Fleming TP, Smith CL, Burgess WH, et al. (1992) Determination of ligand-binding specificity by alternative splicing: two distinct growth factor receptors encoded by a single gene. Proc Natl Acad Sci U S A 89: 246-250.
4. Andreadis ST, Hamoen KE, Yarmush ML, Morgan JR, (2001) Keratinocyte growth factor induces hyperproliferation and delays differentiation in a skin equivalent model system. FASEB J 15: 898-906.
5. Grose R, Fantl V, Werner S, Chioni AM, Jarosz M, et al. (2007) The role of fibroblast growth factor receptor 2b in skin homeostasis and cancer development. EMBO J 26: 1268-1278.
6. Werner S, Smola H, Liao X, Longaker MT, Krieg T, et al. (1994) The function of KGF in morphogenesis of epithelium and reepithelialization of wounds. Science 266: 819-822.
7. Brauchle M, Angermeyer K, Hubner G, Werner S, (1994) Large induction of keratinocyte growth factor expression by serum growth factors and pro-inflammatory cytokines in cultured fibroblasts. Oncogene 9: 3199-3204.
8. Chedid M, Rubin JS, Csaky KG, Aaronson SA, (1994) Regulation of keratinocyte growth factor gene expression by interleukin 1. J Biol Chem 269: 10753-10757.
9. Marchese C, Chedid M, Dirsch OR, Csaky KG, Santanelli F, et al. (1995) Modulation of keratinocyte growth factor and its receptor in reepithelializing human skin. J Exp Med 182: 1369-1376.
10. Escámez MJ, Carretero M, Garcia M, Mártinez-Santamaría L, Mirones I, et al. (2008) Assessment of optimal virus-mediated growth factor gene delivery for human cutaneous wound healing enhancement. J Invest Dermatol 128: 1565-1575.
11. Geer DJ, Swartz DD, Andreadis ST, (2005) Biomimetic delivery of keratinocyte growth factor upon cellular demand for accelerated wound healing in vitro and in vivo. Am J Pathol 167: 1575-1586.
12. Marti G, Ferguson M, Wang J, Byrnes C, Dieb R, et al. (2004) Electroporative transfection with KGF-1 DNA improves wound healing in a diabetic mouse model. Gene Ther 11: 1780-1785.
13. Brake R, Starnes C, Lu J, Chen D, Yang S, et al. (2008) Effects of palifermin on antitumor activity of chemotherapeutic and biological agents in human head and neck and colorectal carcinoma xenograft models. Mol Cancer Res 6: 1337-1346.
14. Finch PW, Rubin JS, (2006) Keratinocyte growth factor expression and activity in cancer: implications for use in patients with solid tumors. J Natl Cancer Inst 98: 812-824.
15. Rotolo S, Ceccarelli S, Romano F, Frati L, Marchese C, et al. (2008) Silencing of keratinocyte growth factor receptor restores 5-fluorouracil and tamoxifen efficacy on responsive cancer cells. PLoS One 3: e2528.
16. Madan V, Lear JT, Szeimies RM, (2010) Non-melanoma skin cancer. Lancet 375: 673-685.
17. Alam M, Ratner D, (2001) Cutaneous squamous-cell carcinoma. N Engl J Med 344: 975-983.
18. Cho K, Ishiwata T, Uchida E, Nakazawa N, Korc M, et al. (2007) Enhanced expression of keratinocyte growth factor and its receptor correlates with venous invasion in pancreatic cancer. Am J Pathol 170: 1964-1974.
19. Yamayoshi T, Nagayasu T, Matsumoto K, Abo T, Hishikawa Y, et al. (2004) Expression of keratinocyte growth factor/fibroblast growth factor-7 and its receptor in human lung cancer: correlation with tumour proliferative activity and patient prognosis. J Pathol 204: 110-118.
20. Yoshino M, Ishiwata T, Watanabe M, Matsunobu T, Komine O, et al. (2007) Expression and roles of keratinocyte growth factor and its receptor in esophageal cancer cells. Int J Oncol 31: 721-728.
21. Diez de Medina SG, Chopin D, El Marjou A, Delouvée A, LaRochelle WJ, et al. (1997) Decreased expression of keratinocyte growth factor receptor in a subset of human transitional cell bladder carcinomas. Oncogene 14: 323-330.
22. Ricol D, Cappellen D, El Marjou A, Diez de Medina SG, Girault JM, et al. (1999) Tumour suppressive properties of fibroblast growth factor receptor 2-IIIb in human bladder cancer. Oncogene 18: 7234-7243.
23. Feng S, Wang F, Matsubara A, Kan M, McKeehan WL, (1997) Fibroblast growth factor receptor 2 limits and receptor 1 accelerates tumorigenicity of prostate epithelial cells. Cancer Res 57: 5369-5378.
24. Ning S, Shui C, Khan WB, Benson W, Lacey DL, et al. (1998) Effects of keratinocyte growth factor on the proliferation and radiation survival of human squamous cell carcinoma cell lines in vitro and in vivo. Int J Radiat Oncol Biol Phys 40: 177-187.
25. Boukamp P, Petrussevska RT, Breitkreutz D, Hornung J, Markham A, et al. (1988) Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J Cell Biol 106: 761-771.
26. Tennis MA, Van Scoyk MM, Freeman SV, Vandervest KM, Nemenoff RA, et al. (2010) Sprouty-4 inhibits transformed cell growth, migration and invasion, and epithelial-mesenchymal transition, and is regulated by Wnt7A through PPARγ in non-small cell lung cancer. Mol Cancer Res 8: 833-843.
27. Furukawa T, Sunamura M, Motoi F, Matsuno S, Horii A, (2003) Potential tumor suppressive pathway involving DUSP6/MKP-3 in pancreatic cancer. Am J Pathol 162: 1807-1815.
28. Sieben NL, Oosting J, Flanagan AM, Prat J, Roemen GM, et al. (2005) Differential gene expression in ovarian tumors reveals Dusp 4 and Serpina 5 as key regulators for benign behavior of serous borderline tumors. J Clin Oncol 23: 7257-7264.
29. Goldoni S, Iozzo RA, Kay P, Campbell S, McQuillan A, et al. (2007) A soluble ectodomain of LRIG1 nhibits cancer cell growth by attenuating basal and ligand-dependent EGFR activity. Oncogene 26: 368-381.
30. Neef R, Kuske MA, Prols E, Johnson JP, (2002) Identification of the human PHLDA1/TDAG51 gene: down-regulation in metastatic melanoma contributes to apoptosis resistance and growth deregulation. Cancer Res 62: 5920-5929.
31. Ala-aho R, Ahonen M, George SJ, Heikkilä J, Grénman R, et al. (2004) Targeted inhibition of human collagenase-3 (MMP-13) expression inhibits squamous cell carcinoma growth in vivo. Oncogene 23: 5111-5123.
32. Bodnar RJ, Yates CC, Rodgers ME, Du X, Wells A, (2009) IP-10 induces dissociation of newly formed blood vessels. J Cell Sci 122: 2064-2077.
33. Jogie-Brahim S, Feldman D, Oh Y, (2009) Unraveling insulin-like growth factor binding protein-3 actions in human disease. Endocr Rev 30: 417-437.
34. Mátés L, Korpos E, Déak F, Liu Z, Beier DR, et al. (2002) Comparative analysis of the mouse and human genes (Matn2 and MATN2) for matrilin-2, a filament-forming protein widely distributed in extracellular matrices. Matrix Biol 21: 163-174.
35. Zhong LP, Yang X, Zhang L, Wei KJ, Pan HY, et al. (2008) Overexpression of insulin-like growth factor binding protein 3 in oral squamous cell carcinoma. Oncol Rep 20: 1441-1447.
36. Lederle W, Hartenstein B, Meides A, Kunzelmann H, Werb Z, et al. (2010) MMP13 as a stromal mediator in controlling persistent angiogenesis in skin carcinoma. Carcinogenesis 31: 1175-1184.
37. Impola U, Jeskanen L, Ravanti L, Syrjänen S, Baldursson B, et al. (2005) Expression of matrix metalloproteinase (MMP)-7 and MMP-13 and loss of MMP-19 and p16 are associated with malignant progression in chronic wounds. Br J Dermatol 152: 720-726.
38. Kivisaari AK, Kallajoki M, Mirtti T, McGrath JA, Bauer JW, et al. (2008) Transformation-specific matrix metalloproteinases (MMP)-7 and MMP-13 are expressed by tumour cells in epidermolysis bullosa-associated squamous cell carcinomas. Br J Dermatol 158: 778-785.
39. Zeigler ME, Chi Y, Schmidt T, Varani J, (1999) Role of ERK and JNK pathways in regulating cell motility and matrix metalloproteinase 9 production in growth factor-stimulated human epidermal keratinocytes. J Cell Physiol 180: 271-284.
40. Mehta PB, Robson CN, Neal DE, Leung HY, (2001) Keratinocyte growth factor activates p38 MAPK to induce stress fibre formation in human prostate DU145 cells. Oncogene 20: 5359-5365.
41. Niu J, Chang Z, Peng B, Xia Q, Lu W, et al. (2007) Keratinocyte growth factor/fibroblast growth factor-7-regulated cell migration and invasion through activation of NF- χB transcription factors. J Biol Chem 282: 6001-6011.
42. Uzan B, Figeac F, Portha B, Movassat J, (2009) Mechanisms of KGF mediated signaling in pancreatic duct cell proliferation and differentiation. PLoS One 4: e4734.
43. Johansson N, Ala-aho R, Uitto V, Grénman R, Fusenig NE, et al. (2000) Expression of collagenase-3 (MMP-13) and collagenase-1 (MMP-1) by transformed keratinocytes is dependent on the activity of p38 mitogen-activated protein kinase. J Cell Sci 113: 227-235.
44. Boukamp P, Stanbridge EJ, Foo DY, Cerutti PA, Fusenig NE, (1990) c-Ha-ras oncogene expression in immortalized human keratinocytes (HaCaT) alters growth potential in vivo but lacks correlation with malignancy. Cancer Res 50: 2840-2847.
45. Mueller MM, Peter W, Mappes M, Huelsen A, Steinbauer H, et al. (2001) Tumor progression of skin carcinoma cells in vivo promoted by clonal selection, mutagenesis, and autocrine growth regulation by granulocyte colony-stimulating factor and granulocyte-macrophage colony-stimulating factor. Am J Pathol 159: 1567-1579.
46. Amann T, Bataille F, Spruss T, Dettmer K, Wild P, et al. (2010) Reduced expression of fibroblast growth factor receptor 2IIIb in hepatocellular carcinoma induces a more aggressive growth. Am J Pathol 176: 1433-1442.
47. Ekerot M, Stavridis MP, Delavaine L, Mitchell MP, Staples C, et al. (2008) Negative-feedback regulation of FGF signalling by DUSP6/MKP-3 is driven by ERK1/2 and mediated by Ets factor binding to a conserved site within the DUSP6/MKP-3 gene promoter. Biochem J 412: 287-298.
48. Muda M, Theodosiou A, Rodrigues N, Boschert U, Camps M, et al. (1996) The dual specificity phosphatases M3/6 and MKP-3 are highly selective for inactivation of distinct mitogen-activated protein kinases. J Biol Chem 271: 27205-27208.
49. Schilling D, Pittelkow MR, Kumar R, (2001) IEX-1, an immediate early gene, increases the rate of apoptosis in keratinocytes. Oncogene 20: 7992-7997.
50. Ozaki K, Miyazaki S, Tanimura S, Kohno M, (2005) Efficient suppression of FGF-2-induced ERK activation by the cooperative interaction among mammalian Sprouty isoforms. J Cell Sci 118: 5861-5871.
51. Piecha D, Hartmann K, Kobbe B, Haase I, Mauch C, et al. (2002) Expression of matrilin-2 in human skin. J Invest Dermatol 119: 38-43.
52. Piecha D, Wiberg C, Mörgelin M, Reinhardt DP, Deák F, et al. (2002) Matrilin-2 interacts with itself and with other extracellular matrix proteins. Biochem J 367: 715-721.
53. Szabo E, Korpos E, Batmunkh E, Lotz G, Holczbauer A, et al. (2008) Expression of matrilin-2 in liver cirrhosis and hepatocellular carcinoma. Pathol Oncol Res 14: 15-22.
54. Kainuma K, Katsuno S, Hashimoto S, Oguchi T, Suzuki N, et al. (2006) Differences in the expression of genes between normal tissue and squamous cell carcinomas of head and neck using cancer-related gene cDNA microarray. Acta Otolaryngol 126: 967-974.
55. Zipin-Roitman A, Meshel T, Sagi-Assif O, Shalmon B, Avivi C, et al. (2007) CXCL10 promotes invasion-related properties in human colorectal carcinoma cells. Cancer Res 67: 3396-3405.
56. Mitsui Y, Mochizuki S, Kodama T, Shimoda M, Ohtsuka T, et al. (2006) ADAM28 is overexpressed in human breast carcinomas: implications for carcinoma cell proliferation through cleavage of insulin-like growth factor binding protein-3. Cancer Res 66: 9913-9920.
57. Kim JH, Cho YH, Park YL, Sohn JH, Kim HS, (2010) Prognostic significance of insulin growth factor-I receptor and insulin growth factor binding protein-3 expression in primary breast cancer. Oncol Rep 23: 989-995.
58. Vaalamo M, Mattila L, Johansson N, Kariniemi A-L, Karjalainen-Lindsberg M-L, et al. (1997) Distinct populations of stromal cells express collagenase-3 (MMP-13) and collagenase-1(MMP-1) in chronic ulcers but not in normally healing wounds. J Invest Dermatol 109: 96-101.
59. Knäuper V, López-Otín C, Smith B, Knight G, Murphy G, (1996) Biochemical characterization of human collagenase-3. J Biol Chem 271: 1544-1550.
60. Ala-aho R, Johansson N, Grénman R, Fusenig NE, López-Otín C, et al. (2000) Inhibition of collagenase-3 (MMP-13) expression in transformed human keratinocytes by interferon-γ is associated with activation of extracellular signal-regulated kinase-1,2 and STAT1. Oncogene 19: 248-257.
61. Imai K, Yokohama Y, Nakanishi I, Ohuchi E, Fujii Y, et al. (1995) Matrix metalloproteinase 7 (matrilysin) from human rectal carcinoma cells. Activation of the precursor, interaction with other matrix metalloproteinases and enzymic properties. J Biol Chem 270: 6691-6697.
62. Remy L, Trespeuch C, Bachy S, Scoazec JY, Rousselle P, (2006) Matrilysin 1 influences colon carcinoma cell migration by cleavage of the laminin-5 β3 chain. Cancer Res 66: 11228-11237.
63. Chen P, Abacherli LE, Nadler ST, Wang Y, Li Q, et al. (2009) MMP7 shedding of syndecan-1 facilitates re-epithelialization by affecting α2β1 integrin activation. PLoS One 4: e6565.
64. Noe V, Fingleton B, Jacobs K, Crawford HC, Vermeulen S, et al. (2001) Release of an invasion promoter E-cadherin fragment by matrilysin and stromelysin-1. J Cell Sci 114: 111-118.
65. Kivisaari AK, Kallajoki M, Ala-aho R, McGrath JA, Bauer JW, et al. (2010) Matrix metalloproteinase-7 activates heparin-binding epidermal growth factor-like growth factor in cutaneous squamous cell carcinoma. Br J Dermatol 163: 726-735.
66. Junttila MR, Ala-aho R, Jokilehto T, Peltonen J, Kallajoki M, et al. (2007) p38α and p38δ mitogen-activated protein kinase isoforms regulate invasion and growth of head and neck squamous carcinoma cells. Oncogene 26: 5267-5279.
67. Leivonen SK, Chantry A, Häkkinen L, Han J, Kähäri VM, (2002) Smad3 mediates transforming growth factor-β-induced collagenase-3 (matrix metalloproteinase-13) expression in human gingival fibroblasts. Evidence for cross-talk between Smad3 and p38 signaling pathways. J Biol Chem 277: 46338-46346.
68. Wilkinson GW, Akrigg A, (1992) Constitutive and enhanced expression from the CMV major IE promoter in a defective adenovirus vector. Nucleic Acids Res 20: 2233-2239.
69. Foschi M, Chari S, Dunn MJ, Sorokin A, (1997) Biphasic activation of p21ras by endothelin-1 sequentially activates the ERK cascade and phosphatidylinositol 3-kinase. EMBO J 16: 6439-6451.
70. Pradervand S, Paillusson A, Thomas J, Weber J, Wirapati P, et al. (2008) Affymetrix Whole-Transcript Human Gene 1.0 ST array is highly concordant with standard 3′ expression arrays. Biotechniques 44: 759-762.
71. Toriseva MJ, Ala-aho R, Karvinen J, Baker AH, Marjomäki VS, et al. (2007) Collagenase-3 (MMP-13) enhances remodeling of three-dimensional collagen and promotes survival of human skin fibroblasts. J Invest Dermatol 127: 49-59.