The neurofibromatosis type 1 (Nf1) tumor suppressor is a modifier of carcinogen-induced pigmentation and papilloma formation in C57BL/6 mice

Journal of Investigative Dermatology

Volumn 114, Issue 6, 2000, Pages 1093-1100

  Atit, Radhika P ^a   Mitchell, Kent ^b   Nguyen, Lam ^b   Warshawsky, David ^b   Ratner, Nancy ^a,b  

^a CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Carcinogenesis; Keratinocyte; Melanocyte; Phorbol ester; Ras

Indexed keywords

CARCINOGEN; DIMETHYLBENZ[A]ANTHRACENE; DNA; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; NEUROFIBROMIN; PHORBOL 13 ACETATE 12 MYRISTATE; RAS PROTEIN;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; GENE MUTATION; MALE; MOUSE; NEUROFIBROMATOSIS; NONHUMAN; PAPILLOMA; PIGMENTATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; TUMOR SUPPRESSOR GENE;

EID: 0034131165     PISSN: 0022202X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1523-1747.2000.00994.x     Document Type: Article

References (58)

1. Aaltonen V, Bostrom PJ, Soderstrom KO, et al: Urinary bladder transitional cell carcinogenesis is associated with down regulation of NF1 tumor suppressor gene in vivo and in vitro. Am J Pathol 154:755-765, 1999
2. Atit RP, Crowe M, Greenhalgh D, Wenstrup R, Ratner N: The Nf1 tumor suppressor is required for mouse skin wound healing, fibroblast proliferation and collagen deposited by fibroblasts. J Invest Dematol 112:835-842, 1999
3. Basu TN, Gutmann DH, Fletcher JA, Glover TW, Collins FS, Downward J: Aberrant regulation of ras proteins in malignant tumor cells from type 1 neurofibromatosis patients. Nature 356:713-715, 1992
4. Binder RL, Gallagher PM, Johnson GR, Stockman SL, Smith BJ, Sundberg JP, Conti CJ: Evidence that initiated keratinocytes clonally expand into multiple existing hair follicles during papilloma histogenesis in SENCAR mouse skin. Mol Carcinogenesis 20:151-158, 1997
5. Bollag G, Clapp D, Shih S, et al: Loss of NF1 results in activation of the Ras signaling pathway and leads to aberrant growth in haematopoietic cells. Nature Genet 12:144-148, 1996
6. Boutwell RK: Some biological aspects of skin carcinogenesis. Prog Exp Tumor Res 4:207-250, 1964
7. Brannan CI, Perkins AS, Vogel KS, et al. Targeted disruption of the neurofibromatosis type-1 gene leads to developmental abnormalities in heart and various neural crest-derived tissues. Genes Dev 8:1019-1029, 1994
8. Bremner R, Kemp CJ, Balmain A: Induction of different genetic changes by different classes of chemical carcinogens during progression of mouse skin tumors. Mol Carcinogenesis 11:90-97, 1994
9. Brown K, Strathdee D, Bryson S, Lambie W, Balmain A: The malignant capacity of skin tumours induced by expression of a mutant H-ras transgene depends on the cell type targeted. Curr Biol 8:516-524, 1998
10. Chase HB: Growth of the hair. Physiol Rev 34:113-126, 1954
11. Chouroulinkov I, Lasne C, Philliphs D, Grover P: Sensitivity of the skin of different mouse strains to the promoting effect of 12-O-tetradecanoyl-phorbol-13-acetate. Bull Cancer 75:557-565, 1988
12. Daston MM, Ratner N: Neurofibromin, a predominantly neuronal GTPase activating protein in the adult, is ubiquitously expressed during development. Dev Dyn 195:216-226, 1992
13. DeClue JE, Papageorge AG, Fletcher JA, Diehl SR, Ratner N, Vass WC, Lowy DR: Abnormal regulation of mammalian p21 ras contributes to malignant tumor growth in von Recklinghausen (type 1) neurofibromatosis, Cell 265-273, 1992
14. Deelman HT: The part played by injury and repair in the development of cancer. Br Med J 1:872, 1927
15. DiGiovanni J: Multistage carcinogenesis in mouse skin. Pharmacol Ther 54:63-128, 1992
16. Dunn J, Garde J, Dolan K, Gosney JR, Sutton R, Meltzer SJ, JKF: Multiple target sites of allelic imbalance on chromosome 17 in Barret's oesophageal cancer. Oncogene 18:987-993, 1999
17. Frenk E, Marazzi A: Neurofibromatosis of von Recklinghausen: a quantitative study of the epidermal keratinocyte and melanocyte populations, J. Invest Dermatol 83:23-25, 1984
18. Friedman JM, Birch PH: Type 1 neurofibromatosis: a descriptive analysis of the disorder in 1,728 patients. Am J Med Gen 70:138-143, 1997
19. Greenhalgh DA, Rothngel JA, Quintanilla MI, et al: Induction of epidermal hyperplasia, hyperkeratosis, and papillomas in transgenic mice by a targeted v-Ha-ras oncogene. Mol Carcinog 7:99-110, 1993
20. Griesser J, Kaufmann D, Eisenbarth I, Bauerle C, Krone W: Ras-GTP regulation is not altered in cultured melanocytes with reduced levels of neurofibromin derived from patients with neurofibromatosis 1 (NF1). Biol Chem Hoppe Seyler 376:91-101, 1995
21. Guo HF, The I, Hannan F, Bernards A, Zhong Y: Requirement for Drosophila NF1 for activation of adenylyl cyclase by PACAP38-like neuropeptides. Science 276:795-798, 1997
22. Hansen LS, Coggle JE, Charles MW: The influence of the hair cycle on the thickness of mouse skin. Anat Rec 210:569-573, 1984
23. Hermonen J, Hirvonen O, Yla-Outinen H, et al: Neurofibromin: expression by normal human keratinocytes in vivo and in vitro and in epidermal malignancies. Lab Invest 73:221-228, 1995
24. Huson S, M. Neurofibromatosis type 1: historical perspective and introductory-overview. In: Upadhyaya M, Cooper DN (eds). Neurofibromatosis Type 1: from Genotype to Phenotype. Oxford: BIOS Science Publications, 1998, pp 1-13
25. Iyengar TD, Ng S, Lau CC, Welch WR, Bell DA, Berkowitz RS, Mok SC: Differential expression of NF1 type I and type II isoforms in sporadic borderline and invasive epithelial ovarian tumors. Oncogene 18:257-262, 1999
26. Jacks T, Shih T, Schmitt EM, Bronson RT, Bernards A, Weinberg RA: Tumor predisposition in mice heterozygous for a targeted mutation of NF1. Nature Genet 7:353-361, 1994
27. Johnson MR, DeClue JE, Felzmann S, Vass WC, Xu G, White R, Lowy DR: Neurofibromin can inhibit ras-dependent growth by a mechanism independent of its GTPase-accelerating function. Mol Cell Biol 14:641-645, 1994
28. Kaufmann D, Wiandt S, Veser J, Krone W: Increased melanogenesis in cultured epidermal melanocytes from patients with neurofibromatosis 1 (NF1). Hum Genet 87:144-150, 1991
29. Kiguchi K, Beltran L, Dubowski A, DiGiovanni J: Analysis of the ability of 12-O-tetradecanoylphorbol-13-aceute to induce epidermal hyperplasia, transforming growth factor-alpha, and skin tumor promotion in wa-1 mice. J Invest Dermatol 108:784-791, 1997
30. Kim H, Rosenbaum T, Marchioni M, Ratner N, DeClue J: Schwann cells from neurofibromin-deficient mice exhibit activation of p21ras, inhibition of cell proliferation and morphologic changes, Oncogene 11:325-335, 1995
31. Kim HA, Ling B, Ratner N: Nf1-deficient mouse Schwann cells are angiogenic and invasive and can be induced to hyperproliferate: reversion of some phenotypes by an inhibitor of famesyl protein transferase. Mol Cell Biol 17:862-872, 1997
32. Kim MR, Tamanoi F. Neurofibromatosis 1 GTPase activating protein-related domain and its functional significance. In: Upadhyaya M, Cooper DN (eds). Neurofibromatosis Type 1: from Genotype to Phenotype. Oxford: BIOS Scientific Publishers, 1998, pp 89-112
33. Klaus SN, Winkelmann RK: Pigment changes induced in hairless mice by dimethylbenzanthracene. J Invest Dermatol 45:160-167, 1965
34. Korf B: Diagnostic outcome in children with multiple cafe au lait spots. Pediatrics 90:924-927, 1992
35. Largaespada DA, Brannan CI, Jenkins NA, Copeland NG: Nf1 deficiency causes Ras-mediated granulocyte/macrophage colony stimulating factor hypersensitivity and chronic myeloid leukemia. Nature Genet 12:137-143, 1996
36. Leder A, Kuo A, Cardiff RD, Sinn E, Leder P: v-Ha-ras transgene abrogates the initiation step in mouse skin tumorigenesis: effects of phorbol esters and retinoic acid. Proc Natl Acad Sci USA 87:9178-9182, 1990
37. Lee Y, Yuspa S, Dlugosz AA: Differentiation of cultured human epidermal keratinocytes at high cell densities is mediated by endogenous activation of protein kinase C signaling pathway. J Invest Dermatol 111:762-766, 1998
38. Lewis RA, Riccardi VM: von Recklinghausen neurofibromatosis: prevalence of iris hermartomas, Opthamology 88:348-354, 1981
39. Malhotra R, Ratner N: Localization of neurofibromin to keratinocytes and melanocytes in developing rat and human skin. J Invest Dermatol 102:812-818, 1994
40. Mangues R, Corral T, Kohl NE, Symmans WF, Liu L, Pellicer A: NF1 inactivation cooperates with N-Ras in in vivo lymphogenesis activating Erk by a mechanism independent of its Ras-GTPase accelerating activity. Oncogene 17:1705-1716, 1998
41. Miller SJ, Sun T, Lavker RM: Hair follicle, stem cells, and skin cancer. J Invest Dermatol 100:288S-294S, 1993
42. Mitchell KR, Warshawsky D: Mutational analysis using enriched PCR and cycle sequencing. Biotechniques 6:1028-1031, 1998
43. Naito M, Naito Y, DiGiovanni J: Comparison of the histological changes in the skin of DBA/2 and C57BL/6 mice following exposure to various promoting agents. Carcinogenesis 8:1807-1815, 1987
44. O'Brien TG, Megosh LC, Gilliard G, Soler AP: Ornithine decarboxylase overexpression is a sufficient condition for tumor promotion in mouse skin. Cancer Res 57:2630-2637, 1997
45. Quintanilla M, Brown K, Ramsden M, Balmain A: Carcinogen-specific mutation and amplification of Ha-ras during mouse skin carcinogenesis. Nature 322:78-80, 1986
46. Reiners JJ, Nesnow S, Slaga T: Murine susceptibility to two-stage skin carcinogenesis is influenced by the agent used for promotion. Carcinogenesis 5:301-307, 1984
47. Riccardi VM: Neurofibromatosis. Phenotype, Natural History and Pathogenesis, 2nd edn. Baltimore: Johns Hopkins University Press, 1992, p. 498
48. Roop DR, Lowy DR, Tambourin PE, et al: An activated Harvey ras oncogene produces benign tumours on mouse epidermal tissue. Nature 323:822-824, 1986
49. Scribner J, Suss R: Tumor initiation and promotion. Int Rev Exp Pathol 18:137-198, 1978
50. Side LE, Shannon KM. The NF1 gene as a tumor suppressor. In: Upadhyaya M, Cooper DN (eds). Neurofibromatosis Type 1: from Genotype to Phenotype. Oxford: BIOS Science Publications, 1998, pp 133-152
51. Slaga TJ. Cellular and molecular mechanisms involved in multistage skin carcinogenesis. In: Conti CJ, Slaga TJ, Klein-Szanto AJP (eds). Carcinogenesis, a Comprehensive Survey, Skin Tumors: Experimental and Clinical Aspects, Vol. 11. New York: Raven Press, 1989, pp 1-18
52. Slominski A, Paus R: Melanogenesis is coupled to murine anagen: toward new concepts for the role of melanocytes and the regulation of melanogenesis in hair growth. J Invest Dematol 101:90S-96S, 1993
53. Takahashi M: Studies on Cafe au lait spots in neurofibromatosis and pigmented macules of nevus spilus. Tohoku J Exp Med 118:255-273, 1976
54. Tognon CE, Kirk HE, Passmore LA, Der CJ, Whitehead IP, Kay RJ: Regulation of RasGRP via a phorbol ester-responsive C1 domain. Mol Cell Biol 18:6995-7008, 1998
55. Tsambaos D, Sampalis F, Berger H: Generalized cutaneous hyperpigmentation in hairless mice induced by topical dimethylbenzanthracene. Exp Cell Biol 57:292-299, 1989
56. Wertheim I, Tangir J, Muto MG, Welch WR, Berkowitz RS, Chen WY, Mok SC: Loss of heterozygosity of chromosome 17 in human borderline and invasive epithelial ovarian tumors. Oncogene 12:2147-2153, 1996
57. Yla-Outinen H, Aaltonen V, Bjorkstrand A, et al: Upregulation of tumor suppressor protein neurofibromin in normal human wound healing and in vitro evidence for platelet derived growth factor (PDGF) and transforming growth factor-β1 (TGF-β1) elicited increase in neurofibromin mRNA steady-state levels in dermal fibroblasts. J Invest Dematol 110:232-237, 1998
58. Zoller ME, Rembeck B, Oden A, Samuelsson M, Angervall L: Malignant and benign tumors in patients with neurofibromatosis type 1 in a defined Swedish population. Cancer 79:2125-2131, 1997