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. 1997 Jun;105(Suppl 4):919–926. doi: 10.1289/ehp.97105s4919

Polymorphisms of H-ras-1 and p53 in breast cancer and lung cancer: a meta-analysis.

A Weston 1, J H Godbold 1
PMCID: PMC1470041  PMID: 9255581

Abstract

Certain polymorphic variants of H-ras-1 and p53 have been investigated for an association between inheritance and cancer risk. The results of a metaanalysis, which reviews studies of H-ras-1 rare alleles and p53 codon 72 allelic variants in breast and lung cancer, are presented. The data constituted evidence for elevated risk of both breast and lung cancer with inheritance of rare H-ras-1 alleles. Calculated population attributable risks are 0.092 and 0.037 for breast and lung cancer, respectively. The frequency of the rare H-ras-1 alleles was observed to be greater in African Americans than in Caucasians, and a specific allele (A3.5) that is common in African Americans was found only at low frequency in Caucasians. For p53 a consensus has yet to be reached. Lung cancer studies conducted in Caucasian and African-American populations have found no evidence of risk associated with the proline variant of codon 72. Two similar studies conducted in Japanese populations suggested an association between p53 genotype distribution and lung cancer risk. However, one implicates the proline allele but the other implicates the arginine allele. The frequency of the proline variant is significantly dependent on race. Frequencies have been reported for control populations of Japanese (0.347 and 0.401), Caucasian (0.295, 0.284, and 0.214), African American (0.628 and 0.527), and Mexican American (0.263).

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Selected References

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  1. Ahuja H. G., Testa M. P., Cline M. J. Variation in the protein coding region of the human p53 gene. Oncogene. 1990 Sep;5(9):1409–1410. [PubMed] [Google Scholar]
  2. Ara S., Lee P. S., Hansen M. F., Saya H. Codon 72 polymorphism of the TP53 gene. Nucleic Acids Res. 1990 Aug 25;18(16):4961–4961. doi: 10.1093/nar/18.16.4961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baker S. J., Fearon E. R., Nigro J. M., Hamilton S. R., Preisinger A. C., Jessup J. M., vanTuinen P., Ledbetter D. H., Barker D. F., Nakamura Y. Chromosome 17 deletions and p53 gene mutations in colorectal carcinomas. Science. 1989 Apr 14;244(4901):217–221. doi: 10.1126/science.2649981. [DOI] [PubMed] [Google Scholar]
  4. Barkardóttir R. B., Jóhannsson O. T., Arason A., Gudnason V., Egilsson V. Polymorphism of the c-Ha-ras-1 proto-oncogene in sporadic and familial breast cancer. Int J Cancer. 1989 Aug 15;44(2):251–255. doi: 10.1002/ijc.2910440211. [DOI] [PubMed] [Google Scholar]
  5. Birgander R., Själander A., Rannug A., Alexandrie A. K., Sundberg M. I., Seidegård J., Tornling G., Beckman G., Beckman L. P53 polymorphisms and haplotypes in lung cancer. Carcinogenesis. 1995 Sep;16(9):2233–2236. doi: 10.1093/carcin/16.9.2233. [DOI] [PubMed] [Google Scholar]
  6. Carbone D., Chiba I., Mitsudomi T. Polymorphism at codon 213 within the p53 gene. Oncogene. 1991 Sep;6(9):1691–1692. [PubMed] [Google Scholar]
  7. Castilla L. H., Couch F. J., Erdos M. R., Hoskins K. F., Calzone K., Garber J. E., Boyd J., Lubin M. B., Deshano M. L., Brody L. C. Mutations in the BRCA1 gene in families with early-onset breast and ovarian cancer. Nat Genet. 1994 Dec;8(4):387–391. doi: 10.1038/ng1294-387. [DOI] [PubMed] [Google Scholar]
  8. Cavenee W. K., Dryja T. P., Phillips R. A., Benedict W. F., Godbout R., Gallie B. L., Murphree A. L., Strong L. C., White R. L. Expression of recessive alleles by chromosomal mechanisms in retinoblastoma. 1983 Oct 27-Nov 2Nature. 305(5937):779–784. doi: 10.1038/305779a0. [DOI] [PubMed] [Google Scholar]
  9. Chen P. L., Chen Y. M., Bookstein R., Lee W. H. Genetic mechanisms of tumor suppression by the human p53 gene. Science. 1990 Dec 14;250(4987):1576–1580. doi: 10.1126/science.2274789. [DOI] [PubMed] [Google Scholar]
  10. Chumakov P. M., Jenkins J. R. BstNI/NciI polymorphism of the human p53 gene (TP53). Nucleic Acids Res. 1991 Dec 25;19(24):6969–6969. doi: 10.1093/nar/19.24.6969-a. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Corell B., Zoll B. Comparison between the allelic frequency distribution of the Ha-ras 1 locus in normal individuals and patients with lymphoma, breast, and ovarian cancer. Hum Genet. 1988 Jul;79(3):255–259. doi: 10.1007/BF00366247. [DOI] [PubMed] [Google Scholar]
  12. Fearon E. R., Cho K. R., Nigro J. M., Kern S. E., Simons J. W., Ruppert J. M., Hamilton S. R., Preisinger A. C., Thomas G., Kinzler K. W. Identification of a chromosome 18q gene that is altered in colorectal cancers. Science. 1990 Jan 5;247(4938):49–56. doi: 10.1126/science.2294591. [DOI] [PubMed] [Google Scholar]
  13. Feinberg A. P., Vogelstein B. Hypomethylation of ras oncogenes in primary human cancers. Biochem Biophys Res Commun. 1983 Feb 28;111(1):47–54. doi: 10.1016/s0006-291x(83)80115-6. [DOI] [PubMed] [Google Scholar]
  14. Felix C. A., Brown D. L., Mitsudomi T., Ikagaki N., Wong A., Wasserman R., Womer R. B., Biegel J. A. Polymorphism at codon 36 of the p53 gene. Oncogene. 1994 Jan;9(1):327–328. [PubMed] [Google Scholar]
  15. Felley-Bosco E., Weston A., Cawley H. M., Bennett W. P., Harris C. C. Functional studies of a germ-line polymorphism at codon 47 within the p53 gene. Am J Hum Genet. 1993 Sep;53(3):752–759. [PMC free article] [PubMed] [Google Scholar]
  16. Fields S., Jang S. K. Presence of a potent transcription activating sequence in the p53 protein. Science. 1990 Aug 31;249(4972):1046–1049. doi: 10.1126/science.2144363. [DOI] [PubMed] [Google Scholar]
  17. Futreal P. A., Barrett J. C., Wiseman R. W. An Alu polymorphism intragenic to the TP53 gene. Nucleic Acids Res. 1991 Dec 25;19(24):6977–6977. doi: 10.1093/nar/19.24.6977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Garrett P. A., Hulka B. S., Kim Y. L., Farber R. A. HRAS protooncogene polymorphism and breast cancer. Cancer Epidemiol Biomarkers Prev. 1993 Mar-Apr;2(2):131–138. [PubMed] [Google Scholar]
  19. Greenblatt M. S., Bennett W. P., Hollstein M., Harris C. C. Mutations in the p53 tumor suppressor gene: clues to cancer etiology and molecular pathogenesis. Cancer Res. 1994 Sep 15;54(18):4855–4878. [PubMed] [Google Scholar]
  20. Hahn M., Serth J., Fislage R., Wolfes H., Allhoff E., Jonas V., Pingoud A. Polymerase chain reaction detection of a highly polymorphic VNTR segment in intron 1 of the human p53 gene. Clin Chem. 1993 Mar;39(3):549–550. [PubMed] [Google Scholar]
  21. Hall J. M., Huey B., Morrow J., Newman B., Lee M., Jones E., Carter C., Buehring G. C., King M. C. Rare HRAS alleles and susceptibility to human breast cancer. Genomics. 1990 Jan;6(1):188–191. doi: 10.1016/0888-7543(90)90466-8. [DOI] [PubMed] [Google Scholar]
  22. Hall J. M., Lee M. K., Newman B., Morrow J. E., Anderson L. A., Huey B., King M. C. Linkage of early-onset familial breast cancer to chromosome 17q21. Science. 1990 Dec 21;250(4988):1684–1689. doi: 10.1126/science.2270482. [DOI] [PubMed] [Google Scholar]
  23. Harris C. C. p53: at the crossroads of molecular carcinogenesis and risk assessment. Science. 1993 Dec 24;262(5142):1980–1981. doi: 10.1126/science.8266092. [DOI] [PubMed] [Google Scholar]
  24. Heighway J., Thatcher N., Cerny T., Hasleton P. S. Genetic predisposition to human lung cancer. Br J Cancer. 1986 Apr;53(4):453–457. doi: 10.1038/bjc.1986.72. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Honda K., Ishizaki K., Ikenaga M., Toguchida J., Inamoto T., Tanaka K., Ozawa K. Increased frequency of specific alleles of the c-Ha-ras gene in Japanese cancer patients. Hum Genet. 1988 Aug;79(4):297–300. doi: 10.1007/BF00282164. [DOI] [PubMed] [Google Scholar]
  26. Ito T., Seyama T., Hayashi T., Mizuno T., Iwamoto K. S., Tsuyama N., Dohi K., Nakamura N., Akiyama M. HaeIII polymorphism in intron 1 of the human p53 gene. Hum Genet. 1994 Feb;93(2):222–222. doi: 10.1007/BF00210619. [DOI] [PubMed] [Google Scholar]
  27. Iwahana H., Orita M., Kanazawa H., Hayashi K., Sekiya T. A new RFLP in intron 1 of the human c-Ha-ras1 gene and its close relationship with the variable tandem repeats in the region 3' to the gene. Oncogene. 1990 Jul;5(7):1049–1053. [PubMed] [Google Scholar]
  28. Jin X., Wu X., Roth J. A., Amos C. I., King T. M., Branch C., Honn S. E., Spitz M. R. Higher lung cancer risk for younger African-Americans with the Pro/Pro p53 genotype. Carcinogenesis. 1995 Sep;16(9):2205–2208. doi: 10.1093/carcin/16.9.2205. [DOI] [PubMed] [Google Scholar]
  29. Kawajiri K., Nakachi K., Imai K., Watanabe J., Hayashi S. Germ line polymorphisms of p53 and CYP1A1 genes involved in human lung cancer. Carcinogenesis. 1993 Jun;14(6):1085–1089. doi: 10.1093/carcin/14.6.1085. [DOI] [PubMed] [Google Scholar]
  30. Kinzler K. W., Nilbert M. C., Vogelstein B., Bryan T. M., Levy D. B., Smith K. J., Preisinger A. C., Hamilton S. R., Hedge P., Markham A. Identification of a gene located at chromosome 5q21 that is mutated in colorectal cancers. Science. 1991 Mar 15;251(4999):1366–1370. doi: 10.1126/science.1848370. [DOI] [PubMed] [Google Scholar]
  31. Koufos A., Hansen M. F., Lampkin B. C., Workman M. L., Copeland N. G., Jenkins N. A., Cavenee W. K. Loss of alleles at loci on human chromosome 11 during genesis of Wilms' tumour. Nature. 1984 May 10;309(5964):170–172. doi: 10.1038/309170a0. [DOI] [PubMed] [Google Scholar]
  32. Krontiris T. G., Devlin B., Karp D. D., Robert N. J., Risch N. An association between the risk of cancer and mutations in the HRAS1 minisatellite locus. N Engl J Med. 1993 Aug 19;329(8):517–523. doi: 10.1056/NEJM199308193290801. [DOI] [PubMed] [Google Scholar]
  33. Krontiris T. G., DiMartino N. A., Colb M., Mitcheson H. D., Parkinson D. R. Human restriction fragment length polymorphisms and cancer risk assessment. J Cell Biochem. 1986;30(4):319–329. doi: 10.1002/jcb.240300405. [DOI] [PubMed] [Google Scholar]
  34. Krontiris T. G., DiMartino N. A., Colb M., Parkinson D. R. Unique allelic restriction fragments of the human Ha-ras locus in leukocyte and tumour DNAs of cancer patients. 1985 Jan 31-Feb 6Nature. 313(6001):369–374. doi: 10.1038/313369a0. [DOI] [PubMed] [Google Scholar]
  35. Krontiris T. G. Oncogenes. N Engl J Med. 1995 Aug 3;333(5):303–306. doi: 10.1056/NEJM199508033330508. [DOI] [PubMed] [Google Scholar]
  36. Kuritz S. J., Landis J. R. Summary attributable risk estimation from unmatched case-control data. Stat Med. 1988 Apr;7(4):507–517. doi: 10.1002/sim.4780070407. [DOI] [PubMed] [Google Scholar]
  37. Lazar V., Hazard F., Bertin F., Janin N., Bellet D., Bressac B. Simple sequence repeat polymorphism within the p53 gene. Oncogene. 1993 Jun;8(6):1703–1705. [PubMed] [Google Scholar]
  38. Lidereau R., Escot C., Theillet C., Champeme M. H., Brunet M., Gest J., Callahan R. High frequency of rare alleles of the human c-Ha-ras-1 proto-oncogene in breast cancer patients. J Natl Cancer Inst. 1986 Sep;77(3):697–701. doi: 10.1093/jnci/77.3.697. [DOI] [PubMed] [Google Scholar]
  39. Ludwig C. U., Raefle G., Dalquen P., Stulz P., Stahel R., Obrecht J. P. Allelic loss on the short arm of chromosome 11 in non-small-cell lung cancer. Int J Cancer. 1991 Nov 11;49(5):661–665. doi: 10.1002/ijc.2910490506. [DOI] [PubMed] [Google Scholar]
  40. MANTEL N., HAENSZEL W. Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst. 1959 Apr;22(4):719–748. [PubMed] [Google Scholar]
  41. Malkin D., Jolly K. W., Barbier N., Look A. T., Friend S. H., Gebhardt M. C., Andersen T. I., Børresen A. L., Li F. P., Garber J. Germline mutations of the p53 tumor-suppressor gene in children and young adults with second malignant neoplasms. N Engl J Med. 1992 May 14;326(20):1309–1315. doi: 10.1056/NEJM199205143262002. [DOI] [PubMed] [Google Scholar]
  42. Matlashewski G. J., Tuck S., Pim D., Lamb P., Schneider J., Crawford L. V. Primary structure polymorphism at amino acid residue 72 of human p53. Mol Cell Biol. 1987 Feb;7(2):961–963. doi: 10.1128/mcb.7.2.961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. McDaniel T., Carbone D., Takahashi T., Chumakov P., Chang E. H., Pirollo K. F., Yin J., Huang Y., Meltzer S. J. The MspI polymorphism in intron 6 of p53 (TP53) detected by digestion of PCR products. Nucleic Acids Res. 1991 Sep 11;19(17):4796–4796. doi: 10.1093/nar/19.17.4796-a. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Miki Y., Swensen J., Shattuck-Eidens D., Futreal P. A., Harshman K., Tavtigian S., Liu Q., Cochran C., Bennett L. M., Ding W. A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1. Science. 1994 Oct 7;266(5182):66–71. doi: 10.1126/science.7545954. [DOI] [PubMed] [Google Scholar]
  45. Murata M., Tagawa M., Kimura M., Kimura H., Watanabe S., Saisho H. Analysis of a germ line polymorphism of the p53 gene in lung cancer patients; discrete results with smoking history. Carcinogenesis. 1996 Feb;17(2):261–264. doi: 10.1093/carcin/17.2.261. [DOI] [PubMed] [Google Scholar]
  46. Nakamura Y., Leppert M., O'Connell P., Wolff R., Holm T., Culver M., Martin C., Fujimoto E., Hoff M., Kumlin E. Variable number of tandem repeat (VNTR) markers for human gene mapping. Science. 1987 Mar 27;235(4796):1616–1622. doi: 10.1126/science.3029872. [DOI] [PubMed] [Google Scholar]
  47. Nigro J. M., Baker S. J., Preisinger A. C., Jessup J. M., Hostetter R., Cleary K., Bigner S. H., Davidson N., Baylin S., Devilee P. Mutations in the p53 gene occur in diverse human tumour types. Nature. 1989 Dec 7;342(6250):705–708. doi: 10.1038/342705a0. [DOI] [PubMed] [Google Scholar]
  48. Olschwang S., Laurent-Puig P., Groden J., White R., Thomas G. Germ-line mutations in the first 14 exons of the adenomatous polyposis coli (APC) gene. Am J Hum Genet. 1993 Feb;52(2):273–279. [PMC free article] [PubMed] [Google Scholar]
  49. Phelan C. M., Rebbeck T. R., Weber B. L., Devilee P., Ruttledge M. H., Lynch H. T., Lenoir G. M., Stratton M. R., Easton D. F., Ponder B. A. Ovarian cancer risk in BRCA1 carriers is modified by the HRAS1 variable number of tandem repeat (VNTR) locus. Nat Genet. 1996 Mar;12(3):309–311. doi: 10.1038/ng0396-309. [DOI] [PubMed] [Google Scholar]
  50. Prosser J., Condie A. Biallelic ApaI polymorphism of the human p53 gene (TP53). Nucleic Acids Res. 1991 Sep 11;19(17):4799–4799. doi: 10.1093/nar/19.17.4799-a. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Prosser J., Elder P. A., Condie A., MacFadyen I., Steel C. M., Evans H. J. Mutations in p53 do not account for heritable breast cancer: a study in five affected families. Br J Cancer. 1991 Feb;63(2):181–184. doi: 10.1038/bjc.1991.44. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Prosser J., Thompson A. M., Cranston G., Evans H. J. Evidence that p53 behaves as a tumour suppressor gene in sporadic breast tumours. Oncogene. 1990 Oct;5(10):1573–1579. [PubMed] [Google Scholar]
  53. Runnebaum I. B., Tong X. W., König R., Zhao H., Körner K., Atkinson E. N., Kreienberg R., Kieback D. G., Hong Z [corrected to Zhao H. ]. p53-based blood test for p53PIN3 and risk for sporadic ovarian cancer. Lancet. 1995 Apr 15;345(8955):994–994. doi: 10.1016/s0140-6736(95)90745-9. [DOI] [PubMed] [Google Scholar]
  54. Runnebaum I. B., Tong X. W., Moebus V., Heilmann V., Kieback D. G., Kreienberg R. Multiplex PCR screening detects small p53 deletions and insertions in human ovarian cancer cell lines. Hum Genet. 1994 Jun;93(6):620–624. doi: 10.1007/BF00201559. [DOI] [PubMed] [Google Scholar]
  55. Ryberg D., Tefre T., Ovrebø S., Skaug V., Stangeland L., Naalsund A., Baera R., Børresen A. L., Haugen A. Ha-ras-1 alleles in Norwegian lung cancer patients. Hum Genet. 1990 Nov;86(1):40–44. doi: 10.1007/BF00205169. [DOI] [PubMed] [Google Scholar]
  56. Saglio G., Camaschella C., Giai M., Serra A., Guerrasio A., Peirone B., Gasparini P., Mazza U., Ceppellini R., Biglia N. Distribution of Ha-RAS-1 proto-oncogene alleles in breast cancer patients and in a control population. Breast Cancer Res Treat. 1988 May;11(2):147–153. doi: 10.1007/BF01805838. [DOI] [PubMed] [Google Scholar]
  57. Scrable H. J., Witte D. P., Lampkin B. C., Cavenee W. K. Chromosomal localization of the human rhabdomyosarcoma locus by mitotic recombination mapping. Nature. 1987 Oct 15;329(6140):645–647. doi: 10.1038/329645a0. [DOI] [PubMed] [Google Scholar]
  58. Sheng Z. M., Guerin M., Gabillot M., Spielmann M., Riou G. c-Ha-ras-1 polymorphism in human breast carcinomas: evidence for a normal distribution of alleles. Oncogene Res. 1988 Feb;2(3):245–250. [PubMed] [Google Scholar]
  59. Själander A., Birgander R., Athlin L., Stenling R., Rutegård J., Beckman L., Beckman G. P53 germ line haplotypes associated with increased risk for colorectal cancer. Carcinogenesis. 1995 Jul;16(7):1461–1464. doi: 10.1093/carcin/16.7.1461. [DOI] [PubMed] [Google Scholar]
  60. Själander A., Birgander R., Hallmans G., Cajander S., Lenner P., Athlin L., Beckman G., Beckman L. p53 polymorphisms and haplotypes in breast cancer. Carcinogenesis. 1996 Jun;17(6):1313–1316. doi: 10.1093/carcin/17.6.1313. [DOI] [PubMed] [Google Scholar]
  61. Själander A., Birgander R., Kivelä A., Beckman G. p53 polymorphisms and haplotypes in different ethnic groups. Hum Hered. 1995 May-Jun;45(3):144–149. doi: 10.1159/000154275. [DOI] [PubMed] [Google Scholar]
  62. Spirio L., Olschwang S., Groden J., Robertson M., Samowitz W., Joslyn G., Gelbert L., Thliveris A., Carlson M., Otterud B. Alleles of the APC gene: an attenuated form of familial polyposis. Cell. 1993 Dec 3;75(5):951–957. doi: 10.1016/0092-8674(93)90538-2. [DOI] [PubMed] [Google Scholar]
  63. Sugimura H., Caporaso N. E., Modali R. V., Hoover R. N., Resau J. H., Trump B. F., Longergan J. A., Krontiris T. G., Mann D. L., Weston A. Association of rare alleles of the Harvey ras protooncogene locus with lung cancer. Cancer Res. 1990 Mar 15;50(6):1857–1862. [PubMed] [Google Scholar]
  64. Toguchida J., Yamaguchi T., Dayton S. H., Beauchamp R. L., Herrera G. E., Ishizaki K., Yamamuro T., Meyers P. A., Little J. B., Sasaki M. S. Prevalence and spectrum of germline mutations of the p53 gene among patients with sarcoma. N Engl J Med. 1992 May 14;326(20):1301–1308. doi: 10.1056/NEJM199205143262001. [DOI] [PubMed] [Google Scholar]
  65. Trepicchio W. L., Krontiris T. G. Members of the rel/NF-kappa B family of transcriptional regulatory proteins bind the HRAS1 minisatellite DNA sequence. Nucleic Acids Res. 1992 May 25;20(10):2427–2434. doi: 10.1093/nar/20.10.2427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Warren W., Eeles R. A., Ponder B. A., Easton D. F., Averill D., Ponder M. A., Anderson K., Evans A. M., DeMars R., Love R. No evidence for germline mutations in exons 5-9 of the p53 gene in 25 breast cancer families. Oncogene. 1992 May;7(5):1043–1046. [PubMed] [Google Scholar]
  67. Weinberg R. A. Tumor suppressor genes. Science. 1991 Nov 22;254(5035):1138–1146. doi: 10.1126/science.1659741. [DOI] [PubMed] [Google Scholar]
  68. Weston A., Ling-Cawley H. M., Caporaso N. E., Bowman E. D., Hoover R. N., Trump B. F., Harris C. C. Determination of the allelic frequencies of an L-myc and a p53 polymorphism in human lung cancer. Carcinogenesis. 1994 Apr;15(4):583–587. doi: 10.1093/carcin/15.4.583. [DOI] [PubMed] [Google Scholar]
  69. Weston A., Pan C. F., Ksieski H. B., Wallenstein S., Berkowitz G. S., Tartter P. I., Bleiweiss I. J., Brower S. T., Senie R. T., Wolff M. S. p53 haplotype determination in breast cancer. Cancer Epidemiol Biomarkers Prev. 1997 Feb;6(2):105–112. [PubMed] [Google Scholar]
  70. Weston A., Perrin L. S., Forrester K., Hoover R. N., Trump B. F., Harris C. C., Caporaso N. E. Allelic frequency of a p53 polymorphism in human lung cancer. Cancer Epidemiol Biomarkers Prev. 1992 Sep-Oct;1(6):481–483. [PubMed] [Google Scholar]
  71. Weston A., Vineis P., Caporaso N. E., Krontiris T. G., Lonergan J. A., Sugimura H. Racial variation in the distribution of Ha-ras-1 alleles. Mol Carcinog. 1991;4(4):265–268. doi: 10.1002/mc.2940040404. [DOI] [PubMed] [Google Scholar]
  72. Weston A., Willey J. C., Modali R., Sugimura H., McDowell E. M., Resau J., Light B., Haugen A., Mann D. L., Trump B. F. Differential DNA sequence deletions from chromosomes 3, 11, 13, and 17 in squamous-cell carcinoma, large-cell carcinoma, and adenocarcinoma of the human lung. Proc Natl Acad Sci U S A. 1989 Jul;86(13):5099–5103. doi: 10.1073/pnas.86.13.5099. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. White G. R., Santibáez-Koref M., Heighway J., Thatcher N. Constitutional frequencies of c-Ha-ras alleles in patients with different types of lung cancer. Br J Cancer. 1990 Jan;61(1):186–186. doi: 10.1038/bjc.1990.33. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. de la Calle-Martín O., Fabregat V., Romero M., Soler J., Vives J., Yagüe J. AccII polymorphism of the p53 gene. Nucleic Acids Res. 1990 Aug 25;18(16):4963–4963. [PMC free article] [PubMed] [Google Scholar]

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