Multiple stages and genetic alterations in immortalization, malignant transformation, and tumor progression of human skin keratinocytes

Molecular Carcinogenesis

Volumn 23, Issue 3, 1998, Pages 144-158

  Fusenig, Norbert E ^a   Boukamp, Petra ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

HaCaT; Multistage carcinogenesis; Skin cancer

Indexed keywords

TELOMERASE; THROMBOSPONDIN 1;

CELL IMMORTALIZATION; CHROMOSOME 15; CHROMOSOME 3P; CONFERENCE PAPER; GENE MUTATION; HUMAN; MALIGNANT TRANSFORMATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN CANCER; SKIN CARCINOGENESIS; SKIN FIBROBLAST; TELOMERE; TUMOR SUPPRESSOR GENE; TUMOR VASCULARIZATION; ULTRAVIOLET RADIATION;

CELL TRANSFORMATION, NEOPLASTIC; DISEASE PROGRESSION; HUMANS; KERATINOCYTES; NEOPLASMS, RADIATION-INDUCED; PHENOTYPE; SKIN; SKIN NEOPLASMS; TUMOR CELLS, CULTURED;

EID: 0031728635     PISSN: 08991987     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-2744(199811)23:3<144::AID-MC3>3.0.CO;2-U     Document Type: Conference Paper

References (78)

1. Fearon FR, Vogelstein B. A genetic model for colorectal carcinogenesis. Cell 61:759-761, 1990.
2. Stanbridge EJ. Human tumor suppressor genes. Annu Rev Gen 24:615-658, 1990.
3. Knudson AG. Antioncogenes and human cancer. Proc Natl Acad Sci USA 90:10914-10921, 1993.
4. Yuspa SH. The pathogenesis of squamous cell cancer: Lessons learned from studies of skin carcinogenesis. Cancer Res 54:1178-1198, 1994.
5. Greenhalgh DA, Wang X-J, Roop DR. Multistage epidermal carcinogenesis in transgenic mice: Cooperativity and paradox. J Invest Dermatol 1:162-176, 1996.
6. Soballe PW, Montone KT, Satyamoorthy K, Nesbit M, Herlyn M. Carcinogenesis in human skin grafted to SCID mice. Cancer Res 56:757-764, 1996.
7. Urano K, Katakai Y, Tokuda Y, Ueyama Y, Nomura T, Yamamoto S. Failure of genotoxic carcinogens to produce tumors in human skin xenografts transplanted to SCID mice. Carcinogenesis 16:2223-2226, 1995.
8. Fusenig NE, Boukamp P. Carcinogenesis studies in human cells: Reliable in vitro models. In: Fusenig NE, Graf H (eds), Cell Culture in Pharmaceutical Research. Springer-Verlag Berlin Inc., Berlin, 1994, pp. 79-102.
9. Namba M, Mihara K, Fushimi K. Immortalization of human cells and its mechanisms. Crit Rev Oncog 7:19-31, 1996.
10. Fusenig NE, Dzarlieva-Petrusevska RT, Breitkreutz D. Phenotypic and cytogenetic characteristics of different stages during spontaneous transformation of mouse keratinocytes in vitro. In: Barrett JC, Tennant RW (eds), Carcinogenesis, vol 9. Raven Press, New York, 1985, pp. 293-326.
11. Sager R. Resistance of human cells to oncogenic transformation. Cells 2:487-493, 1984.
12. Rhim JS, Yoo JH, Park JH, Thraves P, Salchi Z, Dritschilo A. Evidence for the multistep nature of in vitro human epithelial cell carcinogenesis. Cancer Res 50:5653-5657, 1990.
13. Boukamp P, Breitkreutz D, Hülsen A, Tomakidi P, Fusenig NE. In vitro transformation and tumor progression: A multistep model for skin carcinogenesis. In: Leigh I, Lane B, Watt F (eds), The Keratinocyte Handbook. Cambridge University Press, New York, 1994, pp. 485-499.
14. Bryan TM, Reddel RR. SV40-induced immortalization of human cells. Crit Rev Oncog 5:331-357, 1994.
15. Paraskeva C, Corfield AP, Harper S, Hague A, Audcent K, Williams AC. Colorectal carcinogenesis: Sequential steps in the in vitro immortalization and transformation of human colonic epithelial cells. Anticancer Res 10:1189-1200, 1990.
16. H oncogene activation and additional chromosome loss. Oncogene 11:961-969, 1995.
17. Fusenig NE, Boukamp P, Breitkreutz D, Hülsen A. Altered regulation of growth and differentiation at different stages of transformation of human skin keratinocytes. In: Rhim JS, Dritschilo A (eds) Neoplastic Transformation in Human Cell Culture. Humana Press, Totowa, NJ, 1991, pp. 235-250.
18. Rhim JS, Dritschilo A. Neoplastic Transformation in Human Cell Culture. Humana Press, Totowa, NJ, 1991.
19. Boring CC, Squires TS, Tong T, Montgomery S. Cancer statistics. CA Cancer J Clin 44:7-26, 1994.
20. Brash DE, Ziegler A, Jonason AS, Simon JA, Kunala S, Leffell DJ. Sunlight and sunburn in human skin cancer: p53, apoptosis, and tumor promotion. J Invest Dermatol 1:136-142, 1996.
21. Callen JP. Possible precursors to epidermal malignancies. In: Friedman RJ, Riegel DS, Kopf AW, Harris MN, Baker D (eds), Cancer of the Skin. WB Saunders Co., Philadelphia, 1991, pp. 27-34.
22. Lane DP. p53, guardian of the genome. Nature 358:15-16, 1992.
23. Boukamp P, Petrusevska RT, Breitkreutz D, Hornung J, Markham A, Fusenig NE. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J Cell Biol 106:761-771, 1988.
24. Boukamp P, Popp S, Altmeyer S, et al. Sustained nontumorigenic phenotype correlates with a largely stable chromosome content during long-term culture of the human keratinocyte line HaCaT. Genes Chromosomes Cancer 19:201-214, 1997.
25. Boyd JA, Barrett JC. Genetic and cellular basis of multistep carcinogenesis. Pharmacol Ther 46:469-486, 1990.
26. Pereira-Smith OM, Smith JR. Genetic analysis of indefinite division in human cells: Identification of four complementation groups. Proc Natl Acad Sci USA 85:6042-6046, 1988.
27. Sugawara O, Oshimura M, Koi M, Annab LA, Barrett JC. Induction of cellular senescence in immortalized cells by human chromosome 1. Science 247:707-710, 1990.
28. Ning Y, Weber JL, Killary AM, Ledbetter DH, Smith JR, Pereira-Smith OM. Genetic analysis of indefinite division in human cells: Evidence for a cell senescence-related gene(s) on human chromosome 4. Proc Natl Acad Sci USA 88:5635-5639, 1991.
29. Fusenig NE, Boukamp P, Breitkreutz D, Hülsen A, Dzarlieva-Petrusevska RT, Cerutti PA, Stanbridge EJ. In vitro transformation of human skin epithelial cells: Role of ras oncogene in malignant progression. Toxic in Vitro 4:627-634, 1990.
30. Brash DE, Rudolph JA, Simon JA, Lin A, McKenna GJ, Baden HP, Halperin AJ, et al. Role for sunlight in skin cancer: UV-induced p53 mutations in squamous cell carcinoma. Proc Natl Acad Sci USA 88:10124-10128, 1991.
31. Nakazawa H, English D, Randell PL, Nakazawa K, Martel N, Armstrong BK, Yamasaki H. UV and skin cancer: Specific p53 gene mutation in normal skin as a biologically relevant exposure measurement. Proc Natl Acad Sci USA 91:360-364, 1993.
32. Jenkins JR, Rudge K, Currie GA. Cellular immortalization by a cDNA clone encoding the transformation-associated phosphoprotein p53. Nature 312:651-654, 1984.
33. Ziegler A, Jonason AS, Leffel DJ, Simon JA, Sharma HW, Kimmelman J, Remington L, et al. Sunburn and p53 in the onset of skin cancer. Nature 372:773-776, 1994.
34. Lehman TA, Rama M, Boukamp P, Stanek J, Bennett WP, Welsh JA, Metcalf RA, et al. p53 mutations in human immortalized epithelial cell lines. Carcinogenesis 14:833-839, 1993.
35. Marczynska B, Bergholz CM, Wolfe LG. Role of elevated temperature in malignant transformation of mammalian cells in vitro. Int J Cancer 25:813-818, 1980.
36. INK4, and telomerase in immortalization of human cells. Oncogene 11:971-976, 1995.
37. Hayflick L. Mortality and immortality at the cellular level. A review. Biochemistry 62(11):1180-1190, 1997.
38. Harley CB. Human ageing and telomeres. Ciba Found Symp 211:129-139, 1997.
39. Härle-Bachor C, Boukamp P. Telomerase activity in the regenerative basal layer of the epidermis in human skin and in immortal and carcinoma-derived skin keratinocytes. Proc Natl Acad Sci USA 93:6476-6581, 1996.
40. Boukamp P, Rupniak THR, Fusenig NE. Environmental modulation of the expression of differentiation and malignancy in six human squamous cell carcinoma cell lines. Cancer Res 45:5582-5592, 1985.
41. Hülsen A. In-vitro-Analysen von Proliferations-und Differenzierungs-eigenschaften humaner Keratinozyten in unterschiedlichen Transformationsstadien. Ph.D. thesis, University of Kaiserslautern, Kaiserslautern, Germany, 1990.
42. Game SM, Hülsen A, Patel V, et al. Progressive abrogation of TGF-β1 and EGF growth control is associated with tumour progression in ras transfected human keratinocytes. Int J Cancer 52:461-570, 1992.
43. Ryle CM, Breitkreutz D, Stark H-J, et al. Density-dependent modulation of synthesis of keratins 1 and 10 in the human keratinocyte line HaCaT and in ras transfected tumorigenic clones. Differentiation 40:42-54, 1989.
44. 2+. Differentiation 54:201-217, 1993.
45. Boukamp P, Stanbridge EJ, Foo DY, Cerutti PA, Fusenig NE. 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, 1990.
46. Breitkreutz D, Boukamp P, Ryle CM, Stark H-J, Roop DR, Fusenig NE. Epidermal morphogenesis and keratin expression in c-Ha-ras transfected tumorigenic clones of the human HaCaT cell line. Cancer Res 51:4402-4409, 1991.
47. Breitkreutz D, Schoop VM, Mirancea N, Baur M, Stark H-J, Fusenig NE. Epidermal differentiation and basement membrane formation by HaCaT cells in surface transplants. Eur J Cell Biol 75:273-286, 1998.
48. Brown KW, Gallimore PH. Malignant progression of an SV40-transformed human epidermal keratinocyte cell line. Br J Cancer 56:545-554, 1987.
49. Ananthaswamy HN, Pierceall WE. Molecular alterations in human skin tumors. Proc Clin Biol Res 376:61-84, 1992.
50. Prendergast GC, Gibbs JP. Pathways of ras function: Connections to the actin cytoskeleton. Adv Cancer Res 62:19-64, 1993.
51. Kang J-S, Krauss RS. Ras induces anchorage-independent growth by subverting multiple adhesion-regulated cell cycle events. Mol Cell Biol 16:3370-3380, 1996.
52. Winston JT, Coats SR, Wang Y-Z, Pledger WJ. Regulation of the cell cycle machinery by oncogenic ras. Oncogene 12:127-134, 1996.
53. Rak J, Mitsuhashi Y, Erdos V, Huang S-N, Filmus J, Kerbel RS. Massive programmed cell death in intestinal epithelial cells induced by three-dimensional growth conditions: Suppression by expression of a mutant c-H-ras oncogene. J Cell Biol 131:1587-1598, 1995.
54. Rak J, Mitsuhashi Y, Bayko L, Filmus J, Sasazuki T, Kerbel RS. Mutant ras oncogenes upregulate VEGF/VPF expression: Implications for induction and inhibition of tumor angiogenesis. Cancer Res 55:4575-4580, 1995.
55. Grugel S, Finkenzeller G, Weindel K, Barleon B, Marmé D. Both v-Ha-ras and v-raf stimulate expression of the vascular endothelial growth factor in NIH 3T3 cells. J Biol Chem 270:25915-25919, 1995.
56. Rak JW, Filmus J, Kerbel RS. Reciprocal paracrine interactions between tumour cells and endothelial cells: The 'angiogenesis progression' hypothesis. Eur J Cancer 32A:2438-2450, 1996.
57. Fusenig NE. Epithelial-mesenchymal interactions regulate keratinocyte growth and differentiation in vitro. In: Leigh I, Lane B, Watt F (eds), The Keratinocyte Handbook. Cambridge University Press, New York, 1994, pp. 71-94.
58. Breitkreutz D, Stark H-J, Mirancea N, Tomakidi P, Steinbauer H, Fusenig NE. Integrin and basement membrane normalization in mouse grafts of human keratinocytes-implications for epidermal homeostasis. Differentiation 61:195-209, 1997.
59. Fusenig NE, Breitkreutz D, Boukamp P, Bohnert A, Mackenzie IC. Epithelial mesenchymal interaction in tissue homeostasis and malignant transformation. In: Johnson NW (ed), Oral Cancer: Detection of Patients and Lesions at Risk. Cambridge University Press, 1991, pp. 218-256.
60. Boukamp P, Bleuel K, Popp S, Vormwald-Dogan V, Fusenig NE. Functional evidence for tumor suppressor activity on chromosome 15 in human skin carcinoma cells and thrombospondin-1 as the potential suppressor. J Cell Physiol 173:256-260, 1997.
61. Hill M, Hillova J, Mariage-Samson R. Letter to the editor: Malignant transformation of human keratinocytes during adaptation to autotrophy. In vitro Cell Dev Biol Biol Anim 27A:270-272, 1991.
62. Fidler IJ. Critical factors in the biology of human cancer metastasis: Twenty-eighth GHA Clowes memorial lecture. Cancer Res 50:6130-6138, 1990.
63. Cornil J, Theodorescu D, Man S, Herlyn J, Jambrosic J, Kerbel RS. Fibroblast cell interactions with human melanoma cells affect tumor cell growth as a function of tumor progression. Proc Natl Acad Sci USA 88:6028-6032, 1991.
64. Gregoire M, Lieubeau B. The role of fibroblasts in tumor behavior. Cancer Metastasis Rev 14:339-350, 1995.
65. Heldin C-H, Westermark B. Role of platelet-derived growth factor in vivo. In: Clark RAF (ed), The Molecular and Cellular Biology of Wound Repair. Plenum Publishing Corp., New York, 1996, pp. 249-273.
66. Ponten F, Ren Z, Nister M, Westermark B, Ponten J. Epithelial-stromal interactions in basal cancer: The PDGF system. J Invest Dermatol 102:304-309, 1994.
67. Forsberg K, Valyi-Nagy I, Heldin C-H, Herlyn M, Westermark B. Platelet-derived growth factor (PDGF) in ontogenesis: Development of a vascular connective tissue stroma in xenotransplanted human melanoma producing PDGF-BB. Proc Natl Acad Sci USA 90:393-397, 1993.
68. Skobe M, Fusenig NE. Tumorigenic conversion of immortal human keratinocytes through stromal cell activation. Proc Natl Acad Sci USA 95:1050-1055, 1998.
69. Skobe M, Rockwell P, Goldstein N, Vosseler S, Fusenig NE. Halting angiogenesis suppresses carcinoma cell invasion. Nat Med 3(11):1222-1227, 1997.
70. Brauchle M, Angermeyer K, Hübner G, Werner S. Large induction of keratinocyte growth factor expression by serum growth factors and pro-inflammatory cytokines in cultured fibroblasts. Oncogene 9:3199-3204, 1994.
71. Furstenberger G, Rogers M, Schnapke R, Bauer G, Höfler P, Marks F. Stimulatory role of transforming growth factors in multistage skin carcinogenesis: Possible explanation for the tumor inducing effect of wounding in initiated mouse skin. Int J Cancer 43:915-921, 1989.
72. Hanahan D, Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86:353-364, 1996.
73. Weidner N. Intratumor microvessel density as a prognostic factor in cancer. Am J Pathol 147:9-15, 1995.
74. Brooks PC, Strömblad S, Klemke R, Visscher D, Sarkar FH, Cheresh DA. Antiintegrin αvβ3 blocks human breast cancer growth and angiogenesis in human skin. J Clin Invest 96:1815-1822, 1995.
75. Terman BI and Dougher-Vermazen M. Biological properties of VEGF/VPF receptors. Cancer Metastasis Rev 15:159-163, 1996.
76. Rockwell P, Neufeld G, Glassman A, Caron D, Goldstein N. In vitro neutralization of a vascular endothelial growth factor activation of flk-1 by a monodonalantibody. Molecular and Cellular Differentiation 3(1):91-109, 1995.
77. Tomakidi P. Differenzielle Regulation von Proliferation, Differenzierung und Zell-Matrix-Interaktion benigner und maligner Keratinozyten unter dem Einfluß des Bindegewebes: Ein Beitrag zu den molekularen Mechanismen der Invasion. Ph.D. thesis, University of Darmstadt, Darmstadt, Germany, 1995.
78. Peter W. Cytogenetische Veränderung und Modulation der Genexpression während der Tumorprogression am Modell der Hautcarcinogenese in vitro. Ph.D. thesis, University of Kaiserslautern, Kaiserslautern, Germany, 1997.