Abstract
We have characterized a family of transplantable melanomas in Syrian (golden) hamsters, which originated in 1959 as a spontaneous melanoma of hamster skin, and which has been maintained since then by serial passage. Emphasis has been placed on using the same method of transplantation, keeping strict records on all passages, and applying the same investigative techniques, in order to trace tumor behavior over long periods of time. This tumor family consists of five variants linked by common origin, but which differ with respect to differentiation level, malignancy, intermediary metabolism, chromosome number, and cell surface properties. Once established, these melanomas possessed a considerable degree of phenotypic stability over decades of passaging.
One tumor line in this family is emphasized. The Ab amelanotic melanoma lost its differentiated functions (the ability to synthetize melanin) a quarter of a century ago, and since then has remained dedifferentiated in serial passage in hamsters. After transfer to primary cell culture, the Ab melanoma cells differentiate readily and lose much of their proliferative potential. This process is reversible by reimplantation of the cells into a hamster.
Inasmuch as this hamster melanoma system meets many of the conditions required for an experimental tumor model, five melanoma variants are characterized concisely and compared to other melanomas in humans and animals. Mechanisms by which new melanoma variants arise are discussed and compared to some phenomena in the evolution of the species.
Similar content being viewed by others
References
Schirrmacher V: Cancer metastasis: experimental approaches, theoretical concepts, and impacts for treatment strategies. Adv Cancer Res 43: 1–73, 1985
Bagnara J, Klaus SN, Paul E, Shartl M (eds) Pigment Cell. Biological, Molecular and Clinical Aspects of Pigmentation. University of Tokyo Press, Tokyo, 1985
Fidler IJ, Talmadge JE: The evolution of biologic diversity in metastases. Transplantation Proc 96: 370–372, 1984
Wolman SR, McMorrow LE, Fidler IJ, Talmadge JE: Development and progression of karyotypic variability in melanoma K1735 following X-irradiation. Cancer Res 45: 1839–1843, 1985
Stackpole CW, Fornabaio DM, Alterman AL: Phenotypic interconversion of B16 melanoma clone cell populations. Int J Cancer 35: 667–674, 1985
Millikan LE, Smith LL, Ochsner JC: Animal models in melanoma. In: Maibach HI, Lowe NJ (eds) Models in Dermatology Vol. 1. Karger, Basel, 1985, pp 23–33
Loustalot P, Algire GH, Legallais FY, Anderson BF: Growth and histopathology of melanotic and amelanotic derivatives of the Cloudman melanoma S-91. J Natl Cancer Inst 12: 1079–1118, 1952
Harding HE, Passey RD: A transplantable melanoma of the mouse. J Path Bact 33: 417–427, 1930
Fortner JG, Mahy AG, Schrodt GR: Transplantable tumors of the Syrian (golden) hamster. Part I: Tumors of the alimentary tract, endocrine glands and melanomas. Cancer Res 21, Suppl 10: 161–198, 1961
Greene HSN: A spontaneous melanoma in the hamster with a propensity for amelanotic alteration and sarcomatous transformation during transplantation. Cancer Res 18: 422–425, 1958.
Moore GE: In vitro cultures of a pigmented hamster melanoma cell line. Exp Cell Res 36: 422–423, 1964
Rasheed S: Characterization of a differentiated cat melanoma cell line. Cancer Res 43: 3379–3384, 1983
Chernozemski I, Raichev R: Two transplantable lines from melanomas induced in Syrian hamsters with 9,10 dimethy,1,2-benz/a/anthracene (DMBA). Neoplasma 13: 577–582, 1966
Berkelhammer J, Oxenhandler RW, HookJr RR, Hennessy JM: Development of a new melanoma model in C57BL/6 mice. Cancer Res 42: 3157–3163, 1982
Kripke ML: Speculations on the role of ultraviolet radiation in the development of malignant melanoma. J Natl Cancer Inst 63: 541–548, 1979
Goerttler K, Loehrke H, Hesse B, Pyerin WG: Tumor initiation by 7,12-dimethylbenz/a/anthracene in dermal melanocytes of hamster: inhibition through 7,8-benzoflavone. Carcinogenesis 3: 791–795, 1982
Pawlowski A, Lea PJ: Nevi and melanoma induced by chemical carcinogens in laboratory animals: similarities and differences with human lesions. J Cut Pathol 10: 81–110, 1983
McCullough B, Schaller J, Shadduck JA, Yohn DS: Induction of malignant melanomas associated with fibrosarcomas in gnotobiotic cats inoculated with Gardner-feline fibrosarcoma virus. J Natl Cancer Inst 48: 1893–1896, 1972
Shadduck JA, Albert DM, Niederkorn JY: Feline uveal melanomas induced with feline sarcoma virus: potential model of the human counterpart. J Natl Cancer Inst 67: 619–627, 1981
Lerner AB, Cage GW: Melanoma in horses. Yale J Biol Med 46: 646–649, 1974
Hook RRJr, Berkelhammer J, Oxenhandler RW: Animal model of human disease. Melanoma. Sinclair swine melanoma. Am J Pathol 108: 130–133, 1982
Vielkind J, Vielkind U: Melanoma formation in fish of the genus Xiphophorus: a genetically-based disorder in the determination and differentiation of a specific pigment cell. Can J Genet Cytol 24: 133–149, 1982
Ghelelovitch S: Effect of the inhibition of nucleic acids and protein synthesis upon the development of melanotic tumors in Drosophila. Expl Cell Biol 51: 210–216, 1983
McCormick W, Wallace I, Kirk J, Dinsmore S, Allen I: The establishment and characterization of a cell line and mouse xenografts from a human malignant melanoma. Br J Exp Path 64: 103–115, 1983
Bomirski A: Biological properties of transplantable melanomas in the Syrian hamster during 16 years of maintenance by serial passages. Dissertation, Medical School, Gdansk, 1977
Bomirski A, Dominiczak T, Nowinska L: Spontaneous transplantable melanoma in the golden hamster (Mesocricetus auratus). Acta Un Int Cancer 18: 178–180, 1962
Bomirski A, Nowinska L, Pautsch F: The tyrosinase-positive amelanotic melanoma in the golden hamster. In: Della Porta G, Muhlbock O (eds) Structure and Control of the Melanocyte. Springer, Berlin, Heidelberg, New York, 1966, pp 252–259
Słominski A, Bomirski A: Phenotypic changes of Ab hamster melanoma during long-term culture. Anticancer Res 5: 403–410, 1985
Bomirski A, Wrzołkowa T, Arendarczyk M, Bomirska M, Kuklinska E, Słominski A, Moellmann G: Pathology and ultrastructural characteristics of a hypomelanotic variant of transplantable hamster melanoma with elevated tyrosinase activity. J Invest Dermatol 89: 469–473, 1987
Bomirski A, Wrzołkowa T, Arendarczyk M, Bomirska M: An origin, pathologic properties and ultrastructure of a new variant of transplantable melanoma in hamsters. Yale J Biol Med 57: 338, 1984
Słominski A, Bomirski A, Scisłowski PWD, Arendarczyk M: Effect of tissue selection on melanization of MI hamster melanoma. Neoplasma 31: 551–556, 1984
Moyer FH: Genetic effect on melanosome fine structure and ontogency in normal and malignant cells. Ann NY Acad Sci 100: 584–606, 1963
Garcia H, Baroni C, Rappaport HJ: Transplantable tumors of the Syrian golden hamster. J Natl Cancer Inst 27: 1323–1339, 1961
Billingham RE, Sawchuck GH, Silvers WK: Studies on the histocompatibility genes of the Syrian hamster. Proc Natl Acad Sci USA 46: 1079–1090, 1960
Słominski A, Kobzej D: Transplantability of Bomirski melanomas in Syrian hamsters. Neoplasma 30: 51–56, 1983
Steel GG, Adams K, Barret JC: Analysis of the cell population kinetics of transplanted tumours of widely-differing growth rate. Br J Cancer 20: 784–800, 1966
Leibovici J: Serial passage of tumors in mice in the study of tumor progression and testing of antineoplastic drugs. Cancer Res 44: 1981–1984, 1984
Fodstad Ø, Rofstafd EK, Tveit KM, Pihl A: Spontaneous alteration in growth rates of two human melanoma xenografts. Concurrent changes in chemosensitivity. Eur J Cancer Clin Oncol 19: 1175–1178, 1983
Nowell PC: Tumor progression and clonal evolution: the role of genetic instability. In: German J (ed) Chromosome Mutation and Neoplasia. Alan R. Liss Inc., New York, 1983, pp 413–432
Stackpole CW: Generation of phenotypic diversity in the B16 mouse melanoma relative to spontaneous metastasis. Cancer Res 43: 3057–3065, 1983
Poste G, Greig A: The experimental and clinical implications of cellular heterogeneity in malignant tumors. J Cancer Res Clin Oncol 106: 159–170, 1983
Heppner GH: Tumor heterogeneity. Cancer Res 44: 2259–2265, 1984
Nicolson GL: Generation of phenotypic diversity and progression in metastatic tumor cells. Cancer Met Rev 3: 25–42, 1984
Hill RP, Chambers AF, Ling V, Harris JF: Dynamic heterogeneity rapid generation of metastatic variants in mouse B16 melanoma cells. Science 224: 998–1001, 1984
Brodt P, Parhar P, Sankar P, Lala PK: Studies on clonal heterogeneity in two spontaneously metastasizing mammary carcinomas of recent origin. Int J Cancer 35: 265–273, 1985
Herlyn M, Thurin J, Balaban G, Bennicelli JL, Herlyn D, Elder DE, Bondi E, Guerry D, Nowell P, Clark WH, Koprowski H: Characteristics of cultured human melanocytes isolated from different stages of tumor progression. Cancer Res 45: 5670–5676, 1985
Isaacs J: Mechanisms for and implications of the development of heterogeneity of androgen sensitivity in prostatic cancer. In: Owens AH Jr, Coffey DS, Baylin SB (eds) Tumor Cell Heterogeneity. Origins and Implications. Academic Press, New York, London, 1982, pp 99–111
Sidebottom E, Clark SR: Cell fusion segregates progressive growth from metastasis. Br J Cancer 47: 399–406, 1983
Weiss L, Ward PM: Cell detachment and metastasis. Cancer Met Rev 2: 111–127, 1983
Rieber M, Rieber MS: Metastatic potential correlates with cell-surface protein alterations in B16 melanoma variants. Nature 293: 74–76, 1981
Sloane BF, Dunn JR, Honn KV: Lysosomal cathepsin B: correlation with metastatic potential. Science 212: 1151–1153, 1981
DelaMonte SM, Moore GW, Hutchins GM: Patterned distribution of metastases from malignant melanoma in humans. Cancer Res 43: 3427–3433, 1983
Nicolson GL: Cell surface molecules and tumor metastasis. Regulation of metastatic phenotypic diversity. Exp Cell Res 150: 3–22, 1984
Sugarbaker EV: The characteristics of metastasis in man. Am J Pathol 97: 623–632, 1979
Hart IR, Fidler IJ: Role of organ selectivity in the determination of metastatic patterns of B16 melanoma. Cancer Res 40: 2281–2287, 1980
Kozłowska K, Bomirski A, Zurawska-Czupa B: Surface glycoprotein components in isolated melanotic melanoma cells in the golden hamster. Arch Immunol Ther Exp 25: 107–110, 1977
Kozłowska K, Zurawska-Czupa B: Heterogeneity of the surface material in isolated cells of transplantable hamster melanomas. Cancer Res 43: 1168–1171, 1983
Hyrc K, Kapiszewska M, Cieszka K: Differences in the electrophoretic mobilities of pigmented and non-pigmented melanoma cells. In: Schütt W, Klinkmann H (eds) Cell Electrophoresis. Walter de Gruyter & Co., Berlin-New York, 1985, pp 451–457
Bomirski A: Studies on immunization of golden hamsters to transplantable melanomas. Arch Immunol Ther Exp 18: 481–490, 1970
Kozłowska K, Zurawska-Czupa B, Kostulak A: Studies on antigenicity and immunogenicity of transplantable melanoma in hamster by using migration inhibition test. Arch Immunol Ther Exp. 26: 445–447, 1978
Kozłowska K, Zurawska-Czupa B, Mierzewski P, Kostula A: Use of the macrophage migration inhibition test to evaluate antigenic differences in golden hamster transplantable melanomas. Int J Cancer 26: 211–215, 1980
Zbytniewski Z: Aktywnose arylosulfatazy w prezeszczepialnych czerniakach melanotycznych i amelanotycznych u chomika zlocistego (Mesocricetus auratus Waterhouse). Nowotwory 19: 165–176, 1969
Zbytniewski Z, Drewa G: Proteolytic activity of the homogenates of transplantable melanotic and amelanotic melanoma in golden hamster (Mesocricetus auratus, Waterhouse). Pol Med J 11: 397–404, 1972
Watts KP, Fairchild RG, Slatkin DN, Greenberg D, Packer S, Atkins HL, Hannon SJ: Melanin content of hamster tissues, human tissues, and various melanomas. Cancer Res 41: 467–472, 1981
Ito S, Jimbow K: Quantitative analysis of eumelanin and pheomelanin in hair and melanomas. In: Jimbow K (ed) Structure and Function of Melanin Vol. 1. Fuji Printing Co. Inc., Sapporo, 1984, pp 18–25
Bomirski A, Zawrocka-Wrzoŀkowa T, Pautsch F: Electron microscopic studies on transplantable melanotic and amelanotic melanomas in hamsters. Arch Derm Forsch 246: 284–298, 1973
Bomirski A, Wrzoŀkowa T: Ultrastructural tyrosinase reaction in hamster melanoma. Ann Med Sect Pol Acad Sci 20: 59–60, 1975
Bomirski A, Wrzoŀkowa T: Badania ultrastrukturalne nad wystepowaniem tyrozynazy w przeszczepialnym czerniaku amelanotycznym u chomika syryjskiego. Przeg Derm 63: 11–18, 1976
Takahashi H, Horikoshi T, Jimbow K: Fine structural characterization of melanosomes in dysplastic nevi. Cancer 56: 111–123, 1985
Clark WH Jr, Heggeler B, Bretton R: Electron microscopic observations of human cutaneous melanomas correlated with their biologic behavior. In: Bligh VCN (ed) Melanoma and Skin Cancer. Government Printer, New South Wales, 1972, pp 121–141
Hunter JAA, Zaynoun S, Paterson WD, Bleehen SS, Mackie R, Cochran AJ: Cellular fine structure in the invasive nodules of different histogenetic types of malignant melanoma. Br J Dermatol 98: 255–272, 1978
Clark WH Jr, Bretton R: A comparative fine structural study of melanogenesis in normal human epidermal melanocytes and in certain human malignant melanoma cells. In: Hetwig EB, Mostofi FK (eds) The Skin. Int Acad Pathol. Monograph. Williams and Wilkins Co., Baltimore, 1971, pp 197–214
Foa C, Aubert C: Ultrastructural comparison between cultured and tumor cells of human malignant melanoma. Cancer Res 37: 3957–3963, 1977
Tilgen W, Dzarlieva RT, Breitkreutz D, Hennes B, Engster M, Matzku S, Fusenig NE: Heterogeneity of human malignant melanoma cells in vivo and in vitro: role of experimental systems. In: Bagnara J, Klaus SN, Paul E, Schartl M (eds) Pigment Cell. Biological, Molecular and Clinical Aspects of Pigmentation. University of Tokyo Press, Tokyo, 1985, pp 435–437
Jimbow K, Miyake Y, Homma K, Yasuda K, Izumi Y, Tsutsumi A, Ito S: Characterization of melanogenesis and morphogenesis of melanosomes by physicochemical properties of melanin and melanosomes in malignant melanoma. Cancer Res 44: 1128–1134, 1984
Stanka P, Kinzel V, Mohr U: Elektronenmikroskopische Untersuchung über die Prämelanosomenentstehung an Melanomzellen in vitro. Virchows Arch Abpt B Zellpath 2: 91–102, 1969
Rappaport H, Nakai T, Swift H: The fine structure of normal and neoplastic melanocytes in the Syrian hamster, with particular reference to carcinogen-induced melanotic tumors. J Cell Biol 16: 171–186, 1963
Jimbow K, Takeuchi T: Ultrastructural comparison of pheo- and eumelanogenesis in animals. Pigment Cell 4: 308–317, 1979
Bomirski A, Sŀominski A: Ultrastructural aspects of melanization of hamster Ab amelanotic melanoma in primary cell culture. Acta Dermatol Venereol (Stockh) 66: 520–523, 1986
Jimbow K, Oikawa O, Sugiyama S, Takeuchi T: Comparison of eumelanogenesis and pheomelanogenesis in retinal and follicular melanocytes, role of vesiculo-globular bodies in melanosome differentiation. J Invest Dermatol 73: 278–284, 1979
Arstilla AU, Trump BF: Autophagocytosis: origin of membrane and hydrolytic enzymes. Virchows Arch Abpt B Zellpath 2: 85–90, 1969
Nakagawa H, Hori Y, Fitzpatrick TB: The nature and origin of the melanin macroglobule. In: Bagnara J, Klaus SN, Paul E, Schartl M (eds) Pigment Cell. Biological, Molecular and Clinical Aspects of Pigmentation. University of Tokyo Press, Tokyo, 1985, pp 25–34
Foa C, Aubert C: Cellular localization of tyrosinase in human malignant melanoma cell lines. J Invest Dermatol 68: 369–378, 1977
Rodriguez HA, McGavran MH: A modified dopa reaction for the diagnosis and investigation of pigment cells. Amer J Clin Pathol 52: 219–227, 1969
Shieh S-J, Bowers RR, Hadfield TL: An ultrastructural study of albinistic B16 melanoma cells. Exp Molec Pathol 35: 57–64, 1981
Voulot C, Ortonne JP, Benedetto JP, Khatchadourian C, Prota G: Amelanotic changes in B16 melanoma after transplantation to ‘yellow’ Ay/a mice. Arch Dermatol Res 273: 51–60, 1982
Pawelek J, Sansone M, Morowitz J, Moellmann G, Godawska E: Genetic control of melanization: isolation and analysis of amelanotic variants from cultured melanotic melanoma cells. Proc Natl Acad Sci USA 71: 35–84, 1974
Hu F, Swedo JL, Watson JHL: Cytological variations of B16 melanoma cells. Adv Biol Skin 8: 549–579, 1967
Rosenberg IC, Assimacoupoulos C, Lober P, Rosenberg SA, Zimmerman B: The malignant melanoma of hamsters. I. Pathologic characteristics of a transplanted melanotic and amelanotic tumor. Cancer Res 21: 627–631, 1961
Wrathall JR, Oliver C, Silagi S, Essner E: Suppression of pigmentation in mouse melanoma cells by 5-bromodeoxyuridine. Effects on tyrosinase activity and melanosome formation. J Cell Biol 57: 406–423, 1973
Dernaŀowicz E, Trojanowski J, Bomirski A, Dominiczak T: Tyrosinase activity in the amelanotic melanoma in golden hamsters. Nature 215: 188–189, 1967
Sŀominski A, Scislowski PWD, Bomirski A: Biochemical characterization of three hamster melanoma variants. I. Tyrosinase activity and melanin content. Int J Biochem 16: 323–326, 1984
Scislowski PWD, Sŀominski A, Bomirski A: Biochemical characterization of three hamster melanoma variants. II. Glycolysis and oxygen consumption. Int J Biochem 16: 327–331, 1984
Scislowski PWD, Sŀominski A, Bomirski A, Zydowo M: Metabolic characterization of three hamster melanoma variants. Neoplasma 32: 593–598, 1985
Scisŀowski PWD, Sŀominski A: The role of NADP-dependent dehydrogenases in hydroxylation of tyrosine in hamster melanoma. Neoplasma 30: 239–243, 1983
Weinhouse S: Oxidative metabolism of neoplastic tissues. Adv Cancer Res 3: 269–285, 1955
Cooper JA, Reiss NA, Schwartz RJ, Hunter J: Three glycolytic enzymes are phosphorylated at tyrosine in cells transformed by Rous sarcoma virus. Nature 302: 18–223, 1983
Warburg O: On the origin of cancer cells. Science 123: 309–314, 1956
Eigenbrodt E, Glossmann H: Glycolysis—one of the keys to cancer? Trends Pharmac Sci 1: 240–245, 1980
Racker E: Why do tumour cells have a high aerobic glycolysis? J Cell Physiol 89: 697–700, 1976
McKeehan WL: Glycolysis, glutaminolysis and cell proliferation. Cell Biol Int Rep 6: 635–649, 1982
Weiss DW: Tumor origin, progression, immunogenicity, and immunotherapy. Transplant Proc 16: 528–533, 1984
Kozlowska K, Bomirski A, Zurawska-Czupa B: Comparison of the surface glycoprotein components in the isolated cells of hamster melanotic and amelanotic melanomas. Arch Derm Res 256: 197–203, 1976
Hakomori S: Aberrant glycosylation in cancer cell membranes as focused on glycolipids: Overview and perspectives. Cancer Res 45: 2405–2414, 1985
Smets LA, VanBeek WP: Carbohydrates of the tumor cell surface. Biochim Biophys Acta 738: 237–249, 1984
Feizi T: Demonstration by monoclonal antibodies that carbohydrate structures of glycoproteins and glycolipids are onco-developmental antigens. Nature 314: 53–57, 1985
Crumpton MJ: Glycoproteins in relation to cell differentiation and malignancy. In: Akoyumoglou G (ed) Cell Function and Differentiation Part A. Progress in Clinical and Biological Research, vol 102. Alan R. Liss, Inc., New York, 1982, pp 359–370
Mishima Y, Imokawa G: Role of glycosylation in initial melanogenesis: post-inhibition dynamics. In: Bagnara J, Klaus SN, Paul E, Schartl M (eds) Pigment Cell. Biological, Molecular and Clinical Aspects of Pigmentation. University of Tokyo Press, Tokyo, 1985, pp 17–30
Limon J, Bomirski A, Babinska M, Beil B: Cytogenetical analysis of hamster transplantable amelanotic tumours. Scripta Medica (Brno) 51: 445–446, 1978
Limon J, Gibas Z, Babinska M, Bomirski A, Beil B: Cytogenetic analysis of transplantable hamster and mouse melanomas of different melanin contents and growth rate. Yale J Biol Med 57: 387, 1984
Limon J, Gibas Z, Babinska M, Beil B, Bomirski A, Mierzewski P, Sandberg AA: Chromosome changes associated with spontaneous phenotypic variation of transplantable melanoma. Cancer Genet Cytogenet 25: 123–129, 1987
Feinberg AP, Coffey DS: The concept of DNA rearrangement in carcinogenesis and development of tumor cell heterogeneity. In: Owens Jr AH, Coffey DS, Baylin SB (eds) Tumor Cell Heterogeneity, Academic Press, New York-London, 1982, pp 469–494
Sandberg AA: A chromosomal hypothesis of oncogenesis. Cancer Genet Cytogenet 8: 277–285, 1983
Klein G, Klein E: Evolution of tumours and the impact of molecular oncology. Nature 315: 190–195, 1985
Pedersen-Bjergaard J, Andersson P, Philip P: Possible pathogenetic significance of specific chromosome abnormalities and activated proto-oncogenes in malignant diseases of man. Scand J Haematol 36: 127–137, 1986
Zimmering AK, Mansell PWA, Dietrich RS, O'Neil C: Morphological, cytogenetic and ultrastructural observations on three lines of human melanoma kept in long-term culture. Pigment Cell 2: 79–93, 1976
Trent JM, Rosenfeld SB, Meyskens FL: Chromosome 6q involvement in human malignant melanoma. Cancer Genet Cytogenet 9: 177–180, 1983
Pathak S, Drwinga HL, Hsu TC: Involvement of chromosome 6 in rearrangements in human malignant melanoma cell lines. Cytogenet Cell Genet 36: 573–579, 1983
DeSalum SB, Slavutsky I, Besuschio S, Pavlovsky AA: Homogenously staining regions (HSR) in a human malignant melanoma. Cancer Genet Cytogenet 11: 53–60, 1984
Sŀominski A: Rapid melanization of Bomirski amelanotic melanoma cells in cell culture. Biosci Rep 3: 189–194, 1983
Sŀominski A: Some properties of Bomirski Ab amelanotic melanoma cells, which underwent spontaneous melanization in primary cell culture. Growth kinetics, cell morphology, melanin content and tumorigenicity. J Cancer Res Clin Oncol 109: 29–37, 1985
Sŀominski A, Scisŀowski PWD, Bomirski A: Tyrosinase activity in primary cell culture of amelanotic melanoma cells. Biosci Rep 3: 1027–1034, 1983
Sŀominski A, Bomirski A, Scisŀowski PWD, Zoŀnierowicz S: Effects of actinomycin D and cycloheximide on the increase in tyrosinase activity of hamster amelanotic melanoma cells in vitro. Biosci Rep 4: 1059–1064, 1984
Halaban R, Pomerantz SH, Marshall S, Lambert DT, Lerner AB: Regulation of tyrosinase in human melanocytes grown in culture. J Cell Biol 97: 480–488, 1983
Korner A, Pawelek J: Activation of melanoma tyrosinase by a cyclic AMP-dependent protein kinase in a cell-free system. Nature 267: 444–447, 1977
Ossowski I, Reich E: Changes in malignant phenotype of a human carcinoma conditioned by growth environment. Cell 33: 323–333, 1983
Freshney RI: Induction of differentiation in neoplastic cells. Anticancer Res 5: 111–130, 1985
Scott RE, Florine DL: Cell cycle models for the aberrant coupling of growth arrest and differentiation in hyperplasia, metaplasia, and neoplasia. Am J Pathol 107: 342–348, 1982
Bloch A: Induced cell differentiation in cancer therapy. Cancer Treat Rep 68: 199–205, 1984
Logan A, Weatherhead B: Post-tyrosinase inhibition of melanogenesis by melatonin in hair follicles in vitro. J Invest Dermatol 74: 47–50, 1980
Campbell S, Bard JBL: The acellular stroma of the chick cornea inhibits melanogenesis of the neural-crest-derived cells that colonize it. J Embryol Exp Morph 86: 143–154, 1985
Sachs L: Cell differentiation and bypassing of genetic defects in the suppression of malignancy. Cancer Res 47: 1981–1986, 1987
Metcalf D, Nicola NA: Autoinduction of differentiation in WEHI-3B leukemia cells. Int J Cancer 30: 773–780, 1982
Damjanov I, Andrews PW: Ultrastructural differentiation of a clonal human embryonal carcinoma cell line in vitro. Cancer Res 43: 2190–2198, 1983
Pinto M, Robine-Leon S, Appay MD, Kedinger M, Triadou M, Dussaulx E, Lacroix B, Simon-Assmann P, Haffen K, Fough J, Zweibaum A: Enterocyte-like differentiation and polarization of the human colon carcinoma cell line Caco-2 in culture. Biol Cell 47: 323–330, 1983
Mint B, Fleischman RA: Teratocarcinomas and other neoplasms as developmental defects in gene expression. Adv Cancer Res 34: 211–278, 1981
Yamaguchi Y, Kluge N, Ostertag W, Furusawa M: Erythroid differentiation and commitment in rat erythroleukemia cells with hypertonic culture conditions. Proc Natl Acad Sci USA 78: 2325–2329, 1981
peassano S, McNab A, Rovera G: Growth and differentiation of human and murine erythroleukemia cell lines in serum-free synthetic medium. Cancer Res 41: 3592–3596, 1981
Aubert C, Chirieceanu E, Foa C, Delain E: Ultrastructure of spontaneously differentiated human malignant melanocytes cultured from primary tumors. J Natl Cancer Inst 58: 29–35, 1977
Kuhn C, Vielkind U, Anders F: Cell cultures derived from embryos and melanoma of poeciliid fish. In vitro 15: 537–544, 1979
Aubert C, Rouge F, Galindo JR: Differentiation and tumorigenicity of human malignant melanocytes in relation to their culture conditions. J Natl Cancer Inst 72: 3–12, 1984
Wong G, Pawelek J: Melanocyte-stimulating hormone promotes activation of pre-existing tyrosinase molecules in Cloudman S91 melanoma cells. Nature 255: 644–646, 1975
Hu F, Mah K, Teramura DJ: Electron microscopic and cytochemical observations of theophylline and melanocyte-stimulating hormone effects on melanoma cells in culture. Cancer Res 42: 2786–2791, 1982
Van Tieghem N, Doyen A, Legros F, Temmerman A, Vercammen-Grandjean A, Frühling J, Lejeune FJ: Differentiation and retroviral markers in alpha-MSH-treated human melanoma cell lines. Arch Int Physiol Biochem 88: 301, 1980
Kreider JW, Rosenthal M, Lengle N: Cyclic adenosine 3′, 5′-monophosphate in the control of melanoma cell replication and differentiation. J Natl Cancer Inst 50: 555–558, 1973
Kreider JW, Wade DR, Rosenthal M, Densley T: Maturation and differentiation of B16 melanoma cells induced by theophylline treatment. J Natl Cancer Inst 54: 1457–1467, 1975
Hu F: Pigment cell differentiation in vitro. In: Bagnara J, Klaus SN, Paul E, Schartl M (eds) Pigment Cell. Biological, Molecular and Clinical Aspects of Pigmentation. University of Tokyo Press, Tokyo, 1985, pp 369–376
Silagi S: Control of pigment production in mouse melanoma cells in vitro. Evocation and maintenance. J Cell Biol 43: 260–270, 1969
Raz A: B16 melanoma cell variants: irreversible inhibition of growth and induction of morphologic differentiation by anthracycline antibiotics. J Natl Cancer Inst 68: 629–638, 1982
Huberman E, Weeks C, Solanki V, Callahan M, Slaga T: Cell differentiation, alterations in polyamine levels, and specific binding of phorbol diesters in cultured human cells. In: Hecker E (ed) Carcinogenesis, Vol. 7, Raven Press, New York, 1982, pp 405–416
Iwata K, Inui N: Stimulation of melanogenesis in melanoma cells growing in serum-free medium by fetal bovine serum and dimethylsulfoxide. Proc Jap Acad 56B: 562–567, 1980
Ziegler-Heibrock HWL, Munker R, Johnson J, Petersmann I, Schmoekel C, Riethmüller G: In vitro differentiation of human melanoma cells analyzed with monoclonal antibodies. Cancer Res 45: 1344–1350, 1985
Hoal E, Wilson EL, Dowdle EB: Variable effects of retinoids on two pigmenting human melanoma cell lines. Cancer Res 42: 5191–5195, 1982
Giotta GJ, Smith JR, Nicolson GL: Guanosine 5′-triphosphate inhibits growth and stimulates differentiated functions in B16 melanoma cells. Exp Cell Res 112: 385–393, 1978
Sheridan JW, Simmons RJ: Tritiated-thymidine-induced increased DNA content and irreversible differentiation in a human melanoma cell line. Br J Exp Path 62: 289–296, 1981
Käpyaho K, Jänne J: Stimulation of melanotic expression in murine melanoma cells exposed to polyamine antimetabolites. Biochem Biophys Res Commun 113: 18–23, 1983
Slominski A, Kuklinska E, Moellmann G, Pawelek J: Positive regulation of melanogenesis by L-tyrosine and L-dopa. J Invest Dermatol 88: 519, 1987
Slominski A, Moellmann G, Kuklinska E, Bomirski A, Pawelek J: Positive regulation of melanin pigmentation by two key substrates of the melanogenic pathway: L-tyrosine and L-dopa. J. Cell Sci. (in press)
Glass RE: In: Glass RE (ed) Gene Function: E Coli and Its Heritable Elements. Univ California Press, Great Britain, 1982
Hach P, Duchon J, Boronavsky J: Ultrastructural and biochemical characteristics of isolated melanosomes. Folia Morph 25: 407–410, 1977
Borovansky J, Pavel S, Duchon J, Vultrein K: Incorporation of L-3,4-dihydroxy/2-14C/phenylalanine into hamster melanoma melanosomes. FEBS Lett 104: 291–293, 1979
Vendralova E, Duchon J: Comparison of lipids between tumor and normal hamster melanosomes. Neoplasma 30: 317–321, 1983
Vachtenheim J, Pavel S, Duchon J: Dopa oxidase activity and ceruloplasmin in the sera of hamsters with melanoma. Neoplasma 28: 59–65, 1981
Vachtenheim J, Duchon J, Matous B: An animal model for the survival of tyrosinase isoenzymes in serum. Arch Dermatol Res 276: 111–114, 1984
Horcicko J, Pavel S, Borovansky J, Duchon J: Excretion of melanogens and zinc during the growth of melanoma in hamsters. Neoplasma 26: 471–475, 1979
Lukiewicz S: Interference with endogenous radioprotectors as a method of radiosensitization. In: Modification of Radiosensitivity of Biological Systems, International Atomic Energy Agnecy, Vienna, 1976, pp 61–76
Lukiewicz S, Pilas B, Nowicka J, Cieszka K, Gurbiel R: Molecular and cellular basis of different radiosensitivity in pigmented and nonpigmented hamster melanoma cells. In: Seiji M (ed) Pigment Cell. Phenotypic Expression in Pigment Cells. University of Tokyo Press, Tokyo, 1981, pp 647–653
Pajak S, Subczynski W, Panz T, Lukiewicz S: Rate of oxygen consumption of hamster melanoma cells as a factor influencing their radioresistance. Folia Histochem Cytochem 18: 33–40, 1980
Slomianko-Winnicka M: Grupy sulfhydrylowe jako przypuszczalne inhibitory melanogenezy w amelanotycznym czerniaku chomika zlocistego (Mesocricetus auratus Waterhouse). Pat Pol 28: 91–100, 1977
Kozielec T, Slomianko-Winnicka M, Stawarczyk W: Unaczynienie czerniaka zlosliwego u chomika zlocistego. Ann Acad Med Stet 25: 239–246, 1979
Hunter JAA, Paterson WD, Fairley DJ: Human malignant melanoma. Melanosomal polymorphism and the ultrastructural dopa reaction. Br J Dermatol 98: 381–390, 1978
Ito M, Hashimoto K, Organisciak D: Ultrastructural, histochemical and biochemical studies of the melanin metabolism in pallid mouse eye. Curr Eye Res 2: 13–28, 1982/1983
Jimbow K, Kato M, Makita A, Chiba M: Characterization of tyrosinase and structural matrix proteins in melanosomes of mouse melanomas. Pigment Cell 5: 276–285, 1979
Klinger WG, Montague PM, Hearing VJ: Unique melanosomal proteins in murine melanoma. Pigment Cell 2: 1–12, 1976
Nicolson JM, Montague PM, Ekel TM, Hearing VJ: Isolation and partial characterization of aberrant melanosomal proteins from normal and malignant murine melanocytes. Pigment Cell 5: 266–275, 1979
Mazur MT, Katzenstein A-LA: Metastatic melanoma: the spectrum of ultrastructural morphology. Ultrastruc Pathol 1: 337–356, 1980
Cartens PHB, Kuhns JG: Ultrastructural confirmation of malignant melanoma. Ultrastruc Pathol 2: 147–149, 1981
Van Duinen SG, Ruitter DJ, Scheffer E: A staining procedure for melanin in semithin and ultrathin epoxy sections. Histopathol 7: 35–48, 1983
Persky B, MeyskensJr FL, Hendrix MJC: Diagnostic electron microscopy for amelanotic melanoma: correlation of patient biopsy, soft agar assay and xenograft. J Pathol 141: 17–27, 1983
Chen Y, Chavin W: Melanogenesis in human melanomas. Cancer Res 35: 606–612, 1975
Hoperskaya PA, Golubeva ON: The spatio-temporal framework of melanogenic induction in pigmented retinal cells of Xenopus laevis. J Embryol Exp Morphol 60: 173–188, 1980
Bluemink JG, Hoperskaya OA: Ultrastructural evidence for the absence of premelanosomes in eggs of the albino mutant (ap) of Xenopus laevis. Wilhelm Roux' Arch 177: 75–79, 1975
Brumbaugh JA, Wilkins LM, Moore JW: Genetic dissection of eumelanogenesis. Pigment Cell 4: 150–158, 1979
Foster M: Mammalian pigment genetics. Adv Genet 13: 311–339, 1965
Searle AG: Comparative Genetics of Coat Colour in Mammals. Academic Press, London, 1968
Arstilla AU, Jauregui HO, Chang J, Trump BF: Studies on cellular autophagocytosis. Relationship between heterophagy and autophagy in HeLa cells. Lab Invest 24: 162–174, 1971
Jimbow K, Szabo G, Fitzpatrick TB: Ultrastructural investigation of autophagocytosis of melanosomes and programmed death of melanocytes in white leghorn feathers: a study of morphogenetic events leading to hypomelanosis. Develop Biol 36: 8–23, 1974
Boissy RE, Smyth JR, Fite KV: Progressive cytologic changes during the development of delayed feather amelanosis and associated choroidal defects in the DAM chicken line. A vitiligo model. Am J Pathol 111: 197–212, 1983
Boissy RE, Moellmann G, Trainer AT, Smyth JR, Lerner AB: Delayed-amelanotic (Dam or Smyth) chicken melanocyte dysfunction in vivo and in vitro. J Invest Dermatol 86: 149–156, 1986
Ito M, Hashimoto K, Organisciak DT: Ultrastructural, histochemical, and biochemical studies of the melanin metabolism in eye and skin of pallid mice. J Invest Dermatol 78: 414–424, 1982
Pawelek JM, Korner A, Bergstrom A, Bolognia J: New regulators of melanin biosynthesis and the autodestruction of melanoma cells. Nature 286: 617–169, 1980
Parsons PG, Morrison LE: DNA damage and selective toxicity of dopa and ascorbate: copper in human melanoma cells. Cancer Res 42: 3783–3788, 1982
Fidler IJ, Hart IR: The development of biological diversity and metastatic potential in malignant neoplasms. Oncodevelop Biol Med 4: 161–176, 1982
Varani J, Lovett EJ: Phenotypic stability of murine tumor cells in vitro and in vivo. J Natl Cancer Inst 68: 957–962, 1982
Layton MG, Franks LM: Heterogeneity in a spontaneous mouse lung carcinoma: selection and characterization of stable metastatic variants. Br J Cancer 49: 415–421, 1984
Foulds L: Neoplastic Development. Academic Press, New York, 1975
Heppner GH: Tumor subpopulation interactions. In: Owens Jr AH, Coffey DS, Baylin SB (eds) Tumor Cell Heterogeneity. Academic Press, New York, 1982, pp 225–236
Iglehart JD, Ward EC, Thiel K, Huper G, Geler SS, Bolognesi DP: in vivo antigenic modification of tumor cells. I. Introduction of murine leukemia virus antigens on non-virus-producing murine sarcomas. J Natl Cancer Inst 67: 107–115, 1981
Iglehart JD, Weinhold KJ, Huper G, Thiel K, Bolognesi DP: In vivo antigenic modifications of tumor cells. III. Metastatic thymic lymphoma specifically infected by thymotropic retrovirus. J Natl Inst 67: 123–130, 1981
Clark WH Jr, Fromm L, Bernardino EA, Mihm MC: The histogenesis and biological behavior of primary human malignant melanomas of the skin. Cancer Res 29: 705–526, 1969
Clark WH Jr, Min BH, Kligman HL: The developmental biology of induced malignant melanoma in guinea pig and a comparison with other neoplastic systems. Cancer Res 36: 4079–4091, 1976
Dobzhansky T: On some fundamental concepts of Darwinian biology. In: Dobzhansky T, Hecht MK, Steere WC (eds) Evolutionary Biology, Vol 2. North Holland Publishing Co, Amsterdam, 1968, pp 1–34
Gould SJ, Eldredge N: Punctuated equilibria: the tempo and mode of evolution reconsidered. Paleobiol (Chicago) 3: 115–151, 1977
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Bomirski, A., Słominski, A. & Bigda, J. The natural history of a family of transplantable melanomas in hamsters. Cancer Metast Rev 7, 95–118 (1988). https://doi.org/10.1007/BF00046481
Issue Date:
DOI: https://doi.org/10.1007/BF00046481