Ras Oncogenes in Human Cancer: A Review

Cancer Research

Volumn 49, Issue 17, 1989, Pages 4682-4689

  Bos, Johannes L ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

COLON CARCINOMA; GENE MUTATION; HUMAN; LUNG CARCINOMA; ONCOGENE; ONCOGENE H RAS; ONCOGENE K RAS; ONCOGENE N RAS; PANCREAS CARCINOMA; PRIORITY JOURNAL; REVIEW;

CARCINOMA, NON-SMALL-CELL LUNG; COLONIC NEOPLASMS; GENES, RAS; HUMAN; LEUKEMIA; LUNG NEOPLASMS; LYMPHOMA; MELANOMA; MUTATION; MYELODYSPLASTIC SYNDROMES; NEOPLASMS; PANCREATIC NEOPLASMS; SUPPORT, NON-U.S. GOV'T; THYROID NEOPLASMS;

EID: 0024376173     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: None     Document Type: Article

References (98)

1. Barbacid, M. ras genes. Annu. Rev. Biochem., 56: 779–827, 1987.
2. Trahey, M., and McCormick, F. A cytoplasmic protein stimulates normal N-ras p21 GTPase, but does not affect oncogenic mutants. Science (Wash. DC), 238: 542–545, 1987.
3. Adari, H., Lowy, D. R., Willumsen, B. M., Der, C. J., and McCormick, F. Guanosine triphosphatase activating protein (GAP) interacts with the p21 ras effector binding domain. Science (Wash. DC), 240: 518–521, 1988.
4. Calés, C., Hancock, J. F., Marshall, C. J., and Hall, A. The cytoplasmic protein GAP is implicated as the target for regulation by the ras gene product. Nature (Lond.), 332, 548–551, 1988.
5. Vogel, U. S., Dixon, R. A. F., Schaber, M. D., Diehl, R. E., Marshall, M. S., Scolnick, E. M., Sigal, I. S., and Gibbs, J. B. Cloning of bovine GAP and its interaction with oncogenic ras p21. Nature (Lond.), 335: 90–93, 1988.
6. McCormick, F. ras GTPase activating protein: signal transmitter and signal terminator. Cell, 56: 5–8, 1989.
7. Guerrero, I., and Pellicer, A. Mutational activation of oncogenes in animal model systems of carcinogenesis. Mutat. Res., 185: 293–308, 1987.
8. Bos, J. L. The ras gene family and human carcinogenesis. Mutat. Res., 195: 255–271, 1988.
9. Shih, C., and Weinberg, R. A. Isolation of transforming sequence from a human bladder carcinoma cell line. Cell, 29: 161–169, 1982.
10. Krontiris, T., and Cooper, G. M. Transforming activity in human tumor DNAs. Proc. Natl. Acad. Sci. USA, 78: 1181–1184, 1981.
11. Perucho, M., Goldfarb, M., Shimizu, K., Lama, C., Fogh, J., and Wigler, M. Human tumor-derived cell lines contain common and different transforming genes. Cell, 27: 461–466, 1981.
12. Bos, J. L., Verlaan-de Vries, M., Jansen, A. M., Veeneman, G. H., Van Boom, J. H., and Van der Eb, A. J. Three different mutations in codon 61 of the human N-ras gene detected by synthetic oligonucleotide hybridization. Nucleic Acids Res., 12: 9155–9163, 1984.
13. Verlaan-de Vries, M., Bogaard, M. E., Van den Eist, H., Van Boom, J. H., Van der Eb, A. J., and Bos, J. L. A dot-blot screening procedure for mutated ras oncogenes using synthetic oligodesoxynucleotides. Gene, 50: 313–320, 1986.
14. Winter, E., Yamamoto, F., Almoguera, C., and Perucho, M. A method to detect and characterize point mutations in transcribed genes: amplification and overexpression of the mutant c-Ki-ros allele in human tumor cells. Proc. Natl. Acad. Sci. USA, 82: 7575–7579, 1985.
15. Saiki, R., Sharf, S., Faloona, F., Mullis, K., Horn, G., Ehrlich, H. A., and Arnheim, N. Enzymatic amplification of 0-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science (Wash. DC), 250: 1350–1353, 1985.
16. McMahon, G., Davis, E., and Wogan, G. N. Characterization of c-Ki-ras oncogene alleles by direct sequencing of enzymatically amplified DNA from carcinogen-induced tumors. Proc. Natl. Acad. Sci. USA, 84: 4974–4978, 1987.
17. Collins, S. J. Direct sequencing of amplified genomic fragments documents N-ros point mutations in myeloid leukemia. Oncogene Res., 5: 117–123, 1988.
18. Blair, D. G., Cooper, C. S., Oskarsson, M. K., Eader, L. A., and Van de Woude, G. F. New method of detecting cellular transforming genes. Science (Wash. DC), 218: 1122–1125, 1982.
19. Fasano, O., Birnbaum, D., Edland, K., Fogh, J., and Wigler, M. New human transforming genes detected by a tumorigenicity assay. Mol. Cell. Biol., 4: 4926–4930, 1984.
20. Bos, J. L., Toksoz, D., Marshall, C. J., Verlaan-de Vries, M., Veeneman, G. H., Van der Eb, A. J., Van Boom, J. H., Janssen, J. W. G., and Steenvoorden, A. C. M. Amino-acid substitutions at codon 13 of the N-ras oncogene in human acute myeloid leukaemia. Nature (Lond.), 315: 726–730, 1985.
21. Noda, M., Ko, M., Oqura, A., Liu, D. G., Amano, T., Takano, T., and Ikawa, Y. Sarcoma viruses carrying ras oncogenes induce differentiation-associated properties in a neuronal cell line. Nature (Lond.), 318: 73–75, 1985.
22. Bar-Sagi, D., and Feramiso, J. R. Micro-injection of the ras oncogene protein on PC 12 cells induces morphological differentiation. Cell, 42: 841–848, 1985.
23. Zarbl, H., Sukumar, S., Arthur, A. V., Martin-Sanca, D., and Barbacid, M. Direct mutagenesis of Ha-ros-1 oncogenes by N-nitroso-N-methylurea during initiation of mammary carcinogenesis in rats. Nature (Lond.), 575: 382–385, 1985.
24. Sigal, I. S., Gibbs, J. B., D’Alonzo, J. S., and Scolnick, E. M. Identification of effector residues and a neutralizing epitope of Ha-ros-encoded p21. Proc. Natl. Acad. Sci. USA, 83: 4725–4729, 1986.
25. Willumsen, B. M., Christensen, A., Hubbert, N. L., Papageorge, A. G., and Lowly, D. R. The p21 ras C-terminus is required for transformation and membrane association. Nature (Lond.), 310: 583–586, 1984.
26. Leon, J., Guerrero, T., and Pellicer, A. Different expression of the ras gene family in mice. Mol. Cell. Biol., 7: 1535–1540, 1987.
27. Furth, M. E., Aldrich, T. H., and Cordon-Cardo, C. Expression of ras proto-oncogene proteins in normal human tissues. Oncogene, 1: 47–58, 1987.
28. Chesa, P. G., Rettig, W. J., Melamed, M. R., Old, L. J., and Niman, H. L. Expression of p21-ras in normal and malignant human tissues: lack of association with proliferation and malignancy. Proc. Natl. Acad. Sci. USA, 84: 3234–3238, 1987.
29. Wolff, W. I., and Shinya, H. Definitive treatment of “malignant” polyps of the colon. Ann. Surg., 182: 516–525, 1975.
30. Sugarbaker, J. P., Gunderson, L. L., and Wittes, R. E. Colorectal cancer. In: V. T. DeVita, S. Hellman, and S. A. Rosenberg (eds.), Cancer: Principles and Practices of Oncology, Ed. 2. pp. 800–803. Philadelphia: J. B. Lippincott, 1985.
31. Vogelstein, B., Fearon, E. R., Hamilton, S. R., Kern, S. E., Preisinger, A. C., Leppert, M., Nakamura, Y., Whyte, R., Smits, A. M. M., and Bos, J. L. Genetic alterations during colorectal tumor development. N. Engl. J. Med., 579: 525–532, 1988.
32. Bos, J. L., Fearon, E. R., Hamilton, S. R., Verlaan-de Vries, M., Van Boom, J. H., Van der Eb, A. J., and Vogelstein, B. Prevalence of ras mutations in human colorectal cancers. Nature (Lond.), 327: 293–297, 1987.
33. Forrester, K., Almoguera, C., Han, K., Grizzle, W. E., and Perucho, M. Detection of high incidence of K-ras oncogenes during human carcinogenesis. Nature (Lond.), 327: 298–303, 1987.
34. Farr, C. J., Marshall, C. J., Easty, D. J., Wright, N. A., Powell, S. C., and Paraskeva, C. A study of ras gene mutations in colonic adenomas from familial polyposis coli patients. Oncogene, 5: 673–678, 1988.
35. Topai, M. D. DNA repair, oncogenes and carcinogenesis. Carcinogenesis (Lond.), 9: 691–696, 1988.
36. Salomon, E., Voss, R., Hall, V., Bodmer, W. F., Jass, J. R., Jeffreys, A. J., Lucibello, F. C., Patel, I., and Rider, S. H. Chromosome 5 allele loss in human colorectal carcinomas. Nature (Lond.), 328: 616–619, 1987.
37. Fearon, E. R., Hamilton, S. R., and Vogelstein, B. Clonal analysis of human colorectal tumors. Science (Wash. DC), 238: 193–197, 1987.
38. Gazdar, A. F., Carney, D. N., and Minna, J. D. The biology of non-small cell lung cancer. Semin. Oncol., 10: 3–19, 1983.
39. Rodenhuis, S., Van de Wetering, M. L., Mooi, W. J., Evers, S. G., Van Zandwijk, N., and Bos, J. L. Mutational activation of the K-ras oncogene, a possible pathogenetic factor in adenocarcinoma of the lung. N. Engl. J. Med., 577: 929–935, 1987.
40. Rodenhuis, S., Slebos, R. J. C., Boot, A. J. M., Evers, S. G., Mooi, W. J., Wagenaar, S. S., Van Bodegom, P. C., and Bos, J. L. K-ras oncogene activation in adenocarcinoma of the lung: incidence and possible clinical significance. Cancer Res., 48: 5738–5741, 1988.
41. Suda, Y., Aizawa, S., Hirai, S., Inoue, T., Furuta, Y., Suzuki, M., Hirohashi, S., and Ikawa, Y. Driven by the same Ig enhancer and SV40 T promoter ras induced lung adenomatous tumors, myc induced pre-B cell lymphomas and SV40 large T gene a variety of tumor in transgenic mice. EMBO J., 6: 4055–4065, 1987.
42. Albino, A. P., Le Strange, R., Oliff, A. I., Furth, M. E., and Old, L. J. Transforming ras genes from human melanoma: a manifestation of tumour heterogeneity? Nature (Lond.), 308: 69–72, 1984.
43. Van’t Veer, L. J., Burgering, B. M. Th., Versteeg, R., Boot, A. J. M., Ruiter, D. J., Osanto, S., Schrier, P. I., and Bos, J. L. N-ras mutations in human cutaneous melanoma correlated with sun exposure. Mol. Cell. Biol., 9: 3114–3116, 1989.
44. Almoquera, C., Shibata, D., Forrester, K., Martin, J., Arnheim, N., and Perucho, M. Most human carcinomas of the exocrine pancreas contain mutant c-K-ras genes. Cell, 53: 549–554, 1988.
45. Smit, V. T. H. B. M., Boot, A. J. M., Smits, A. M. M., Fleuren, G. J., Cornelisse, C. J., and Bos, J. L. K-ras codon 12 mutations occur very frequently in pancreatic adenocarcinomas. Nucleic Acids Res., 16: 7773–7782, 1988.
46. Quaife, C. J., Pinkert, C. A., Ornitz, D. M., Palmiter, R. D., and Brinster, R. L. Pancreatic neoplasia induced by ras expression in acinar cells of transgenic mice. Cell, 48: 1023–1034, 1987.
47. Dotto, G. P., Parada, L. F., and Weinberg, R. A. Specific growth response of ras-transformed embryo fibroblasts to tumour promoters. Nature (Lond.), 575: 472–475, 1985.
48. Land, H., Chen, A. C., Morgenstern, J. P., Parada, L. F., and Weinberg, R. A. Behavior of myc and ras oncogenes in transformation of rat embryo fibroblasts. Mol. Cell. Biol., 6: 1917–1925, 1986.
49. Grunewald, K., Lyons, J., Fröhlich, A., Feichtinger, H., Weger, R. A., Schwab, G., Janssen, J. W. G., and Bartram, C. R. High frequency of Ki-ras codon 12 mutations in pancreatic adenocarcinomas. Int. J. Cancer, 43: 1037–1041, 1989.
50. Williams, E. D. Pathologic and natural history. The aetiology of thyroid tumors. Clin. Endocrinol. Metab., 8: 193–207, 1979.
51. Lemoine, N. R., Mayall, E. S., Wyllie, F. W., Farr, C. J., Hughes, D., Padua, R. A., Thurston, V., Williams, E. D., and Wynford-Thomas, D. Activated ras oncogenes in human thyroid cancers. Cancer Res., 48: 4459–4463, 1988.
52. Lemoine, N. R., Mayall, E. S., Wyllie, F. W., Williams, E. D., Goyns, M., Stringer, B., and Wynford-Thomas, D. High frequency of ras oncogene activation in all stages of human thyroid tumorigenesis. Oncogene, 4: 159–164, 1989.
53. Suarez, H. G., Du Villard, J. A., Caillou, B., Schlumberger, M., Tubiana, M., Parmentier, C., and Monier, R. Detection of activated ras oncogenes in human thyroid carcinomas. Oncogene, 2: 403–406, 1988.
54. Fusco, A., Grieco, M., Santoro, M., Berlingieri, M. J., Pilotti, S., Pierotti, M. A., Delia Porta, G., and Vecchio, G. A new oncogene in human thyroid papillary carcinomas and their lymph-node metastases. Nature (Lond.), 328: 170–172, 1987.
55. Raskind, W. H., Triumali, N., Jacobson, R., Singer, J., and Fialkow, P. J. Evidence for a multistep pathogenesis of myelodysplastic syndrome. Blood, 63: 1318–1323, 1984.
56. Nowell, P. C. The clonal evolution of tumor cell populations (Acquired genetic lability permits stepwise selection of variant sublines and underlies tumor progression). Science (Wash. DC), 194: 23–28, 1976.
57. Bos, J. L., Verlaan-de Vries, M., Van der Eb, A. J., Janssen, J. W. G., Delwel, R., Löwenberg, B., and Colly, L. P. Mutations in N-ras predominate in acute myeloid leukemia. Blood, 69: 1237–1241, 1987.
58. Needleman, S. W., Kraus, M. H., Srivastava, S. K., Levine, P. H., and Aaronson, S. A. High frequency of N-ras activation in acute myelogenous leukemia. Blood, 67: 753–757, 1986.
59. Janssen, J. W. G., Steenvoorden, A. C. M., Lyons, J., Anger, B., Böhlke, J. U., Bos, J. L., Seliger, H., and Bartram, C. R. ras gene mutations in acute and chronic myelocytic leukemias, chronic myeloproliferative disorders and myelodysplastic syndromes. Proc. Natl. Acad. Sci. USA, 84: 9228–9232, 1987.
60. Toksoz, D., Farr, C. J., and Marshall, C. J. ras gene activation in a minor proportion of the blast population in acute myeloid leukemia. Oncogene, 7: 409–413, 1987.
61. Farr, C. J., Saiki, R. K., Ehrlich, H. A., McCormick, F., and Marshall, C. J. Analysis of ras gene mutations in acute myeloid leukemia using the polymerase chain reaction and oligonucleotide probes. Proc. Natl. Acad. Sci. USA, 85: 1629–1633, 1988.
62. Senn, H. P., Tran-Thang, C., Wodnar-Filipowicz, A., Jirincy, J., Fopp, M., Gratwohl, A., Signer, E., Weber, W., and Moroni, C. Mutation analysis of the N-ras proto-oncogene in active and remission phase of human acute leukemias. Int. J. Cancer, 41: 59–64, 1988.
63. Hirai, H., Kobayashi, Y., Mano, H., Hagiwara, K., Mam, Y., Omine, M., Mizoguchi, H., Nishida, J., and Takaku, F. A point mutation at codon 13 of the N-ras oncogene in myelodysplastic syndrome. Nature (Lond.), 327: 430–432, 1987.
64. Liu, R., Hjelle, B., Morgan, R., Hecht, F., and Bishop, J. M. Mutations of the Kirsten-ros proto-oncogene in human preleukemia. Nature (Lond.), 330: 186–188, 1987.
65. Padua, R. A., Carter, G., Hughes, D., Gow, J., Farr, C., Oscier, D., McCormick, F., and Jacobs, A. ras mutations in myelodysplasia detected by amplification, oligonucleotide hybridization, and transformation. Leukemia (Baltimore), 2: 503–510, 1988.
66. Pedersen-Bjergaard, J., Janssen, J. W. G., Lyons, J., Philip, P., and Bartram, C. R., Point mutation of the ras oncogenes and chromosome aberrations in acute nonlymphocytic leukemia and preleukemia related to therapy with alkylating agents. Cancer Res., 48: 1812–1817, 1988.
67. Lyons, J., Janssen, J. W. G., Bartram, C., Layton, M., and Mufti, G. J. Mutation of Ki-ras oncogenes in myelodysplastic syndromes. Blood, 71: 1707–1712, 1988.
68. Bartram, C. R., Ludwig, W.-D., Hiddeman, W., Lyons, J., Buschle, M., Ritter, J., Harbott, J., Fröhlich, A., and Janssen, J. W. G. Acute myeloid leukemia: analysis of ras gene mutations and clonality defined by polymorphic X-linked loci. Leukemia (Baltimore), 3: 247–256, 1989.
69. Yunis, J. J., Boot, A. J. M., Mayer, M. G., and Bos, J. L. Mechanism of ras mutation in myelodysplastic syndrome. Oncogene, 4: 609–614, 1988.
70. Janssen, J. W. G., Buschle, M., Layton, M., Drexler, H. G., Lyons, J., Van den Berghe, H., Heimpel, H., Kubanek, B., Kleihauer, E., Mufti, G. J., and Bartram, C. R. Clonal analysis of myelodysplastic syndromes: evidence of multipotent stem cell origin. Blood, 73: 248–254, 1989.
71. Hirai, H., Okada, M., Mizoguchi, H., Mano, H., Kobayashi, Y., Nishida, J., and Takaku, F. Relationship between activated N-ros oncogene and chromosomal abnormality during leukemic progression from myelodysplastic syndrome. Blood, 77: 256–258, 1988.
72. Senn, H. P., Jiricny, J., Fopp, J. M., Schmid, L., and Moroni, C. Relapse cell population differs from acute onset clone as shown by absence of the initially activated N-ros oncogene in a patient with acute myelomonocytic leukemia. Blood, 72: 931–935, 1988.
73. Layton, D. M., Mufti, G. J., Lyons, J., Janssen, J. W. G., and Bartram, C. R. Loss of ras oncogene mutation in a myelodysplastic syndrome after low-dose cytarabine therapy. N. Engl. J. Med., 318: 1468–1469, 1988.
74. Rodenhuis, S., Bos, J. L., Slater, R. M., Behrendt, H., Van’t Veer, M., and Smets, L. A. Absence of oncogene amplifications and occasional activation of N-ros in lymphoblastic leukemia of childhood. Blood, 67: 1698–1704, 1986.
75. Neri, A., Knowles, D. M., Greco, A., McCormick, F., and Dalla-Favera, R. Analysis of ras oncogene mutations in human lymphoid malignancies. Proc. Natl. Acad. Sci. USA, 85: 9268–9272, 1988.
76. Kraus, M. H., Yuasa, Y., and Aaronson, S. A. A position 12-activated H-ras oncogene in all HS578T mammary carcinosarcoma cells but not in normal mammary cells of the same patient. Proc. Natl. Acad. Sci. USA, 81: 5384–5388, 1984.
77. Van de Vijver, M., Peterse, J. L., Mooi, W. J., Lohmans, J., Verbruggen, M., Van de Bersselaar, R., Devilee, P., Cornelisse, C., Bos, J. L., Yarnold, J., and Nusse, R. Oncogene activations in human breast cancer. Cancer Cells, in press, 1989.
78. Spandidos, D. A. Oncogene activation in malignant transformation: a study of H-ras in human breast cancer. Anticancer Res., 7: 991–996, 1987
79. Perucho, M., Forrester, K., Almoquera, C., Khan, S., Lama, C., Shibata, D., Arnheim, N., and Grizzle, W. E. Expression and mutational activation of the c-Ki-ras gene in human carcinomas. Cancer Cells, in press, 1989.
80. Van’t Veer, L. J., Hermens, R., Van den Berg-Bakker, L. A. M., Ching Cheng, N., Fleuren, G. J., Bos, J. L., Cleton, F. J., and Schrier, P. I. ras oncogene activation in human ovarian carcinoma. Oncogene, 2: 157–165, 1988.
81. Riou, G., Barrais, M., Sheng, Z.-M., Duvillard, P., and Lhomme, C. Somatic deletions and mutations of c-Ha-ros gene in human cervical cancers. Oncogene, 3: 329–333, 1988.
82. Hollstein, M. C., Smits, A. M., Galiana, C., Yamasaki, H., Bos, J. L., Mandard, A., Partensky, G., and Montesano, R. Amplification on EGF receptor gene but no evidence of ras mutations in primary human esophageal cancers. Cancer Res., 48: 5119–5123, 1988.
83. Ballas, K., Lyons, J., Janssen, J. W. G., and Bartram, C. R. Incidence of ras gene mutations in neuroblastoma. Eur. J. Pediatr., 147: 313–314, 1988.
84. Sakato, H., Mori, M., Taira, M., Yoshida, T., Matsukawa, S., Shimizu, K., Sekiguchi, M., Terada, M., and Sugimura, T. Transforming gene from human stomach cancers and a noncancerous portion of stomach mucosa. Proc. Natl. Acad. Sci. USA, 83: 3997–4001, 1986.
85. Fujita, J., Srivastava, S. K., Kraus, M. H., Rhim, J. S., Tronick, S. R., and Aaronson, S. A. Frequency of molecular alterations affecting ras protooncogenes in human urinary tract tumors. Proc. Natl. Acad. Sci. USA, 82: 3849–3853, 1985.
86. Leon, J., Kamino, H., Steinberg, J. J., and Pellicer, A. H-ras activation in benign and self-regressing skin tumors (keratoacanthomas) in both humans and an animal model system. Mol. Cell. Biol., 8: 786–793, 1988.
87. Mulder, M. P., Keijzer, W., Boot, A. J. M., Verkerk, T., Prins, E., Splinter, T., and Bos, J. L. Activated ras genes in human seminoma: evidence for tumor heterogeneity. Oncogene, in press, 1989.
88. Raybaud, F., Noguchi, T., Maries, I., Adelaide, J., Planche, J., Batoz, M., Aubert, C., de Lapeyriere, O., and Birnbaum, D. Detection of a low frequency of activated ras genes in human melanomas using a tumorigenicity assay. Cancer Res., 48: 950–953, 1988.
89. Malone, P. R., VisVanathan, K. V., Ponder, B. A., Shearer, R. J., and Summerhayes, I. C. Oncogene and bladder cancer. Br. J. Urol., 57: 664–667, 1985.
90. Fujita, K., Ohuchi, N., Yao, T., Okumura, M., Fukushima, Y., Kanakura, V., Kitamura, Y., and Fujita, J. Frequent overexpression, but not activation by point mutation, of ras genes in primary human gastric cancers. Gastroenterology, 6: 1339–1345, 1987.
91. VisVanathan, K. V., Pocock, R. D., and Summerhayes, I. C. Preferential and novel activation of H-ras in human bladder carcinomas. Oncogene Res., 3: 77–86, 1988.
92. Gu, J. R., Hu, L. F., Cheng, Y. C., and Wan, D. F. Oncogenes in human primary hepatic cancer. J. Cell. Physiol. Suppl., 4: 13–20, 1986.
93. Fujita, J., Kraus, M. H., Onoue, H., Srivastava, S. K., Ebi, Y., Kitamura, Y., and Rhim, J. S. Activated H-ras oncogenes in human kidney tumors. Cancer Res., 48: 5251–5255, 1988.
94. Buschle, M., Janssen, J. W. G., Drexler, H., Lyons, J., Anger, B., and Bartram, C. R. Evidence for pluripotent stem cell origin of idiopathic myelofibrosis: clonal analysis of a case characterized by a N-ros gene mutation. Leukemia (Baltimore), 2: 658–660, 1988.
95. Hirai, H., Nishida, J., and Takaku, F. Highly frequent detection of transforming genes in acute leukemias by transfection using in vivo selection assays. Biochim. Biophys. Res. Commun., 147: 108–114, 1987.
96. Liu, E., Hjelle, B., and Bishop, J. M. Transforming genes in chronic myelogenous leukemia. Proc. Natl. Acad. Sci. USA, 85: 1952–1956, 1988.
97. Steenvoorden, A. C. M., Janssen, J. W. G., Drexler, H. G., Lyons, J., Tesch, H., Jones, D. B., and Bartram, C. R. ros mutations in Hodgkin’s disease. Leukemia (Baltimore), 2: 325–326, 1988.
98. Sklar, M. D., and Kitchingman, G. R. Isolation of activated ros transforming genes from two patients with Hodgkin’s disease. Int. J. Radiât. Oncol. Biol. Phys., 77: 49–55, 1985.