Cigarette smoking and K-ras mutations in pancreas, lung and colorectal adenocarcinomas: Etiopathogenic similarities, differences and paradoxes

Mutation Research - Reviews in Mutation Research

Volumn 682, Issue 2-3, 2009, Pages 83-93

  Porta, Miquel ^a,b,c   Crous Bou, Marta ^a,b,c   Wark, Petra A ^d,e   Vineis, Paolo ^e   Real, Francisco X ^f,g   Malats, Núria ^f   Kampman, Ellen ^h  

^a INST MUNIC D INVESTIGACIO MEDICA   (Spain)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^c CIBER EPIDEMIOLOGÍA Y SALUD PÚBLICA CIBERESP   (Spain)

^d LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

^f Centro Nacional de Investigaciones Oncológicas   (Spain)

^g UNIVERSITAT POMPEU FABRA   (Spain)

^h WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Adenocarcinoma; Carcinogenesis; Colorectal neoplasm; K ras oncogene; Lung cancer; Meta analysis; Mutation spectrum; Pancreatic neoplasms; Tobacco smoking

Indexed keywords

CIGARETTE SMOKING; COLORECTAL CARCINOMA; GENE MUTATION; HUMAN; LUNG ADENOCARCINOMA; ONCOGENE K RAS; PANCREAS ADENOCARCINOMA; PREVALENCE; PRIORITY JOURNAL; REVIEW;

ADENOCARCINOMA; COLORECTAL NEOPLASMS; GENES, RAS; HUMANS; LUNG NEOPLASMS; MUTATION; PANCREATIC NEOPLASMS; RISK FACTORS; SMOKING;

NICOTIANA TABACUM;

EID: 71849087381     PISSN: 13835742     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrrev.2009.07.003     Document Type: Review

References (94)

1. Malumbres M., and Barbacid M. RAS oncogenes: the first 30 years. Nat. Rev. Cancer 3 (2003) 459-465
2. Bos J.L. ras oncogenes in human cancer: a review. Cancer Res. 49 (1989) 4682-4689
3. Maitra A., Adsay N.V., Argani P., et al. Multicomponent analysis of the pancreatic adenocarcinoma progression model using a pancreatic intraepithelial neoplasia tissue microarray. Mod. Pathol. 16 (2003) 902-912
4. Schubbert S., Shannon K., and Bollag G. Hyperactive Ras in developmental disorders and cancer. Nat. Rev. Cancer 7 (2007) 295-308
5. Schuller H.M. Mechanisms of smoking-related lung and pancreatic adenocarcinoma development. Nat. Rev. Cancer 2 (2002) 455-463
6. Shields J.M., Pruitt K., McFall A., Shaub A., and Der C.J. Understanding Ras: 'it ain't over til it's over'. Trends Cell Biol. 10 (2000) 147-154
7. Porta M., Ayude D., Alguacil J., and Jariod M. Exploring environmental causes of altered ras effects: fragmentation plus integration?. Mol. Carcinog. 36 (2003) 45-52
8. Porta M., Malats N., Jariod M., et al. Serum concentrations of organochlorine compounds and K-ras mutations in exocrine pancreatic cancer. Lancet 354 (1999) 2125-2129
9. Porta M., Malats N., Guarner L., et al. Association between coffee drinking and K-ras mutations in exocrine pancreatic cancer. J. Epidemiol. Commun. Health 53 (1999) 702-709
10. Alguacil J., Porta M., Malats N., et al. Occupational exposure to organic solvents and K-ras mutations in exocrine pancreatic cancer. Carcinogenesis 23 (2002) 101-106
11. Slattery M.L., Wolff R.K., Curtin K., et al. Colon tumor mutations and epigenetic changes associated with genetic polymorphism: insight into disease pathways. Mutat. Res. 660 (2009) 12-21
12. Alguacil J., Porta M., Kauppinen T., Malats N., Kogevinas M., and Carrato A. Occupational exposure to dyes, metals, polycyclic aromatic hydrocarbons and other agents and K-ras activation in human exocrine pancreatic cancer. Int. J. Cancer 107 (2003) 635-641
13. Ekbom A., and Hunter D. Pancreatic cancer. In: Adami H.O., Hunter D., and Trichopoulos D. (Eds). Textbook of Cancer Epidemiology (2002), Oxford University Press, New York 233-247
14. Potter J.D., and Hunter D. Colorectal cancer. In: Adami H.O., Hunter D., and Trichopoulos D. (Eds). Textbook of Cancer Epidemiology (2002), Oxford University Press, New York 188-211
15. Boffeta P., and Trichopuolos D. Cancer of the lung, larynx, and pleura. In: Adami H.O., Hunter D., and Trichopoulos D. (Eds). Textbook of Cancer Epidemiology (2002), Oxford University Press, New York 248-280
16. Bardeesy N., and DePinho R.A. Pancreatic cancer biology and genetics. Nat. Rev. Cancer 2 (2002) 897-909
17. Hezel A.F., Kimmelman A.C., Stanger B.Z., Bardeesy N., and Depinho R.A. Genetics and biology of pancreatic ductal adenocarcinoma. Genes Dev. 20 (2006) 1218-1249
18. Catalogue Of Somatic Mutations In Cancer (COSMIC), Wellcome Trust, Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, UK, http://www.sanger.ac.uk/perl/genetics/CGP/cosmic?action=gene&ln=KRAS.
19. Yokota J., and Kohno T. Molecular footprints of human lung cancer progression. Cancer Sci. 95 (2004) 197-204
20. Rodenhuis S., Slebos R.J., Boot A.J., et al. Incidence and possible clinical significance of K-ras oncogene activation in adenocarcinoma of the human lung. Cancer Res. 48 (1988) 5738-5741
21. Vähäkangas K.H., Bennett W.P., Castrén K., et al. p53 and K-ras mutations in lung cancers from former and never-smoking women. Cancer Res. 61 (2001) 4350-4356
22. Forgacs E., Zöchbauer-Müller S., Oláh E., and Minna J.D. Molecular genetic abnormalities in the pathogenesis of human lung cancer. Pathol. Oncol. Res. 7 (2001) 6-13
23. Kuper H., Adami H.O., and Boffetta P. Tobacco use, cancer causation and public health impact. J. Intern. Med. 251 (2002) 455-466
24. IARC. Tobacco smoke and involuntary smoking. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans vol. 83 (2002), International Agency for Research on Cancer, Lyon
25. Kuper H., Boffetta P., and Adami H.O. Tobacco use and cancer causation: association by tumour type. J. Intern. Med. 252 (2002) 206-224
26. Sasco A.J., Secretan M.B., and Straif K. Tobacco smoking and cancer: a brief review of recent epidemiological evidence. Lung Cancer 45 (2004) 3-9
27. Weiderpass E., Partanen T., Kaaks R., et al. Pancreatic cancer: occurrence, trends, and environmental etiology. A review. Scand. J. Work Environ. Health 24 (1999) 165-174
28. Li D., and Jiao L. Epidemiology. In: von Hoff D.D., Evans D.B., and Hruban R.H. (Eds). Pancreatic Cancer (2005), Jones & Bartlett, Boston 103-117
29. Khuder S.A. Effect of cigarette smoking on major histological types of lung cancer: a meta-analysis. Lung Cancer 31 (2001) 139-148
30. Herbst R.S., Heymach J.V., and Lippman S.M. Lung cancer. N. Engl. J. Med. 359 (2008) 1367-1380
31. Sun S., Schiller J.H., and Gazdar A.F. Lung cancer in never smokers: a different disease. Nat. Rev. Cancer 7 (2007) 778-790
32. Toh C.K., Gao F., Lim W.T., et al. Never-smokers with lung cancer: epidemiologic evidence of a distinct disease entity. J. Clin. Oncol. 24 (2006) 2245-2251
33. Toyooka S., Tokumo M., Shigematsu H., et al. Mutational and epigenetic evidence for independent pathways for lung adenocarcinomas arising in smokers and never smokers. Cancer Res. 66 (2006) 1371-1375
34. Liang P.S., Chen T.Y., and Giovannucci E. Cigarette smoking and colorectal cancer incidence and mortality: systematic review and meta-analysis. Int. J. Cancer 124 (2009) 2406-2415
35. Botteri E., Iodice S., Raimondi S., Maisonneuve P., and Lowenfels A.B. Cigarette smoking and adenomatous polyps: a meta-analysis. Gastroenterology 134 (2008) 388-395
36. Giovannucci E. An updated review of the epidemiological evidence that cigarette smoking increases risk of colorectal cancer. Cancer Epidemiol. Biomarkers Prev. 10 (2001) 725-731
37. Botteri E., Iodice S., Bagnardi V., Raimondi S., Lowenfels A.B., and Maisonneuve P. Smoking and colorectal cancer: a meta-analysis. JAMA 300 (2008) 2765-2778
38. Hecht S.S. Cigarette smoking and lung cancer: chemical mechanisms and approaches to prevention. Lancet Oncol. 3 (2002) 461-469
39. Hecht S.S. Tobacco carcinogens, their biomarkers and tobacco-induced cancer. Nat. Rev. Cancer 3 (2003) 733-744
40. Mounawar M., Mukeria A., Le Calvez F., et al. Patterns of EGFR, HER2, TP53, and KRAS mutations of p14arf expression in non-small cell lung cancers in relation to smoking history. Cancer Res. 67 (2007) 5667-5672
41. Higgins J.P., Thompson S.G., Deeks J.J., and Altman D.G. Measuring inconsistency in meta-analyses. BMJ 327 (2003) 557-560
42. DerSimonian R., and Laird N. Meta-analysis in clinical trials. Control. Clin. Trials 7 (1986) 177-188
43. Mantel N., and Haenszel W. Statistical aspects of the analysis of data from retrospective studies of disease. J. Natl. Cancer Inst. 22 (1959) 719-748
44. Nagata Y., Abe M., Motoshima K., Nakayama E., and Shiku H. Frequent glycine-to-aspartic acid mutations at codon 12 of c-Ki-ras gene in human pancreatic cancer in Japanese. Jpn. J. Cancer Res. 81 (1990) 135-140
45. Hruban R.H., van Mansfeld A.D., Offerhaus G.J., et al. K-ras oncogene activation in adenocarcinoma of the human pancreas. A study of 82 carcinomas using a combination of mutant-enriched polymerase chain reaction analysis and allele-specific oligonucleotide hybridization. Am. J. Pathol. 143 (1993) 545-554
46. Malats N., Porta M., Corominas J.M., Piñol J.L., Rifà J., and Real F.X. Ki -ras mutations in exocrine pancreatic cancer: association with clinico-pathological characteristics and with tobacco and alcohol consumption. Int. J. Cancer 70 (1997) 661-667
47. Berger D.H., Chang H., Wood M., et al. Mutational activation of K-ras in nonneoplastic exocrine pancreatic lesions in relation to cigarette smoking status. Cancer 85 (1999) 326-332
48. Slebos R.J., Hoppin J.A., Tolbert P.E., et al. K-ras and p53 in pancreatic cancer: association with medical history, histopathology, and environmental exposures in a population-based study. Cancer Epidemiol. Biomarkers Prev. 9 (2000) 1223-1232
49. Fryzek J.P., Garabrant D.H., Schenk M., Kinnard M., Greenson J.K., and Sarkar F.H. The association between selected risk factors for pancreatic cancer and the expression of p53 and K-ras codon 12 mutations. Int. J. Gastrointest. Cancer 37 (2006) 139-145
50. Jiao L., Zhu J., Hassan M.M., Evans D.B., Abbruzzese J.L., and Li D. K-ras mutation and p16 and preproenkephalin promoter hypermethylation in plasma DNA of pancreatic cancer patients: in relation to cigarette smoking. Pancreas 34 (2007) 55-62
51. Crous-Bou M., Porta M., López T., et al. Lifetime history of tobacco consumption and K-ras mutations in exocrine pancreatic cancer. Pancreas 35 (2007) 135-141
52. Martínez M.E., Maltzman T., Marshall J.R., et al. Risk factors for Ki-ras protooncogene mutation in sporadic colorectal adenomas. Cancer Res. 59 (1999) 5181-5185
53. Lafuente M.J., Casterad X., Trias M., et al. NAD(P)H:quinone oxidoreductase-dependent risk for colorectal cancer and its association with the presence of K-ras mutations in tumors. Carcinogenesis 21 (2000) 1813-1819
54. Slattery M.L., Anderson K., Curtin K., et al. Lifestyle factors and Ki-ras mutations in colon cancer tumors. Mutat. Res. 483 (2001) 73-81
55. Miyaki M., Iijima T., Ishii R., et al. Increased frequency of p53 mutation in sporadic colorectal cancer from cigarette smokers. Jpn. J. Clin. Oncol. 32 (2002) 196-201
56. Diergaarde B., Vrieling A., van Kraats A.A., van Muijen G.N., Kok F.J., and Kampman E. Cigarette smoking and genetic alterations in sporadic colon carcinomas. Carcinogenesis 24 (2003) 565-571
57. Wark P.A., Van der Kuil W., Ploemacher J., et al. Diet, lifestyle and risk of K-ras mutation-positive and -negative colorectal adenomas. Int. J. Cancer 119 (2006) 398-405
58. Weijenberg M.P., Aardening P.W.M., De Kok T.M., De Goeij A.F.P.M., and Van den Brandt P.A. Cigarette smoking and K-ras mutations in sporadic colorectal cancer. Results from The Netherlands Cohort Study. Mutat. Res. 652 (2008) 54-64
59. Slebos R.J., Hruban R.H., Dalesio O., Mooi W.J., Offerhaus G.J., and Rodenhuis S. Relationship between K-ras oncogene activation and smoking in adenocarcinoma of the human lung. J. Natl. Cancer Inst. 83 (1991) 1024-1027
60. Vainio H., Husgafvel-Pursiainen K., Anttila S., Karjalainen A., Hackman P., and Partanen T. Interaction between smoking and asbestos in human lung adenocarcinoma: role of K-ras mutations. Environ. Health Perspect. 101 Suppl. 3 (1993) 189-192
61. Westra W.H., Slebos R.J., Offerhaus G.J., et al. K-ras oncogene activation in lung adenocarcinomas from former smokers. Evidence that K-ras mutations are an early and irreversible event in the development of adenocarcinoma of the lung. Cancer 72 (1993) 432-438
62. Marchetti A., Pellegrini S., Sozzi G., et al. Genetic analysis of lung tumours of non-smoking subjects: p53 gene mutations are constantly associated with loss of heterozygosity at the FHIT locus. Br. J. Cancer 78 (1998) 73-78
63. De Gregorio L., Manenti G., Incarbone M., et al. Prognostic value of loss of heterozygosity and KRAS2 mutations in lung adenocarcinoma. Int. J. Cancer 79 (1998) 269-272
64. Nelson H.H., Christiani D.C., Mark E.J., Wiencke J.K., Wain J.C., and Kelsey K.T. Implications and prognostic value of K-ras mutation for early-stage lung cancer in women. J. Natl. Cancer Inst. 91 (1999) 2032-2038
65. Le Calvez F., Mukeria A., Hunt J.D., et al. TP53 and KRAS mutation load and types in lung cancers in relation to tobacco smoke: distinct patterns in never, former, and current smokers. Cancer Res. 65 (2005) 5076-5083
66. Gealy R., Zhang L., Siegfried J.M., Luketich J.D., and Keohavong P. Comparison of mutations in the p53 and K-ras genes in lung carcinomas from smoking and nonsmoking women. Cancer Epidemiol. Biomarkers Prev. 8 (1999) 297-302
67. Ahrendt S.A., Decker P.A., Alawi E.A., Zhu Yr Y.R., Sanchez-Cespedes M., and Yang S.C. Cigarette smoking is strongly associated with mutation of the K-ras gene in patients with primary adenocarcinoma of the lung. Cancer 92 (2001) 1525-1530
68. Riely G.J., Kris M.G., Rosenbaum D., et al. Frequency and distinctive spectrum of KRAS mutations in never smokers with lung adenocarcinoma. Clin. Cancer Res. 14 (2008) 5731-5734
69. Wu C.C., Hsu H.Y., Liu H.P., et al. Reversed mutation rates of KRAS and EGFR genes in adenocarcinoma of the lung in Taiwan and their implications. Cancer 113 (2008) 3199-3208
70. Swede H., Bartos J.D., Chen N., et al. Genomic profiles of colorectal cancers differ based on patient smoking status. Cancer Genet. Cytogenet. 168 (2006) 98-104
71. Slattery M.L., Curtin K., Anderson K., et al. Associations between cigarette smoking, lifestyle factors, and microsatellite instability in colon tumors. J. Natl. Cancer Inst. 92 (2000) 1831-1836
72. Chia J.A., Simms L.A., Cozzi S.J., et al. SnoN expression is differently regulated in microsatellite unstable compared with microsatellite stable colorectal cancers. BMC Cancer 6 (2006) 252
73. Lüchtenborg M., Weijenberg M.P., Kampman E., et al. Cigarette smoking and colorectal cancer: APC mutations, hMLH1 expression, and GSTM1 and GSTT1 polymorphisms. Am. J. Epidemiol. 161 (2005) 806-815
74. Lüchtenborg M., Weijenberg M.P., Wark P.A., et al. Mutations in APC, CTNNB1 and K-ras genes and expression of hMLH1 in sporadic colorectal carcinomas from the Netherlands Cohort Study. BMC Cancer 5 (2005) 160
75. Porta M., and Crous M. La acumulación de alteraciones genéticas y epigenéticas: un proceso causal clave entre el medio ambiente y las enfermedades de etiología compleja [Editorial]. Gac. Sanit. 19 (2005) 273-276
76. Lyronis I.D., Baritaki S., Bizakis I., Krambovitis E., and Spandidos D.A. K-ras mutation, HPV infection and smoking or alcohol abuse positively correlate with esophageal squamous carcinoma. Pathol. Oncol. Res. 14 (2008) 267-273
77. Wada R., and Yamaguchi T. K-ras codon 12 mutations of the super-minute dysplasia in Barrett's esophagus by DNA extraction using a microdissection method. Dis. Esophagus 16 (2003) 214-217
78. Lord R.V., O'Grady R., Sheehan C., Field A.F., and Ward R.L. K-ras codon 12 mutations in Barrett's oesophagus and adenocarcinomas of the oesophagus and oesophagogastric junction. J. Gastroenterol. Hepatol. 15 (2000) 730-736
79. Arber N., Shapira I., Ratan J., et al. Activation of c-K-ras mutations in human gastrointestinal tumors. Gastroenterology 118 (2000) 1045-1050
80. Trautmann B., Wittekind C., Strobel D., et al. K-ras point mutations are rare events in premalignant forms of Barrett's oesophagus. Eur. J. Gastroenterol. Hepatol. 8 (1996) 799-804
81. Galiana C., Fusco A., Martel N., Nishihira T., Hirohashi S., and Yamasaki H. Possible role of activated ras genes in human esophageal carcinogenesis. Int. J. Cancer 54 (1993) 978-982
82. Victor T., Du Toit R., Jordaan A.M., Bester A.J., and van Helden P.D. No evidence for point mutations in codons 12, 13, and 61 of the ras gene in a high-incidence area for esophageal and gastric cancers. Cancer Res. 50 (1990) 4911-4914
83. Porta M., Hernández-Aguado I., Lumbreras B., et al. 'Omics' research, monetization of intellectual property and fragmentation of knowledge: can clinical epidemiology strengthen integrative research?. J. Clin. Epidemiol. 60 (2007) 1220-1225
84. Real F.X., Cibrián-Uhalte E., and Martinelli P. Pancreatic cancer development and progression: re-modelling the model. Gastroenterology 135 (2008) 724-728
85. Vineis P., Malats N., Porta M., and Real F.X. Human cancer, carcinogenic exposures and mutation spectra. Mutat. Res. Rev. 436 (1999) 185-194
86. Vogelstein B., Fearon E.R., Hamilton S.R., et al. Genetic alterations during colorectal-tumor development. N. Engl. J. Med. 319 (1988) 525-532
87. Fearon E.R., and Vogelstein B. A genetic model for colorectal tumorigenesis. Cell 61 (1990) 759-767
88. Powell S.M., Zilz N., Beazer-Barclay Y., et al. APC mutations occur early during colorectal tumorigenesis. Nature 359 (1992) 235-237
89. Bos J.L., Fearon E.R., Hamilton S.R., et al. Prevalence of ras gene mutations in human colorectal cancers. Nature 327 (1987) 293-297
90. Kikuchi-Yanoshita R., Konishi M., Ito S., et al. Genetic changes of both p53 alleles associated with the conversion from colorectal adenoma to early carcinoma in familial adenomatous polyposis and non-familial adenomatous polyposis patients. Cancer Res. 52 (1992) 3965-3971
91. Vineis P., and Porta M. Causal thinking, biomarkers and mechanisms of carcinogenesis. J. Clin. Epidemiol. 49 (1996) 951-956
92. Slebos R.J., and Rodenhuis S. The ras gene family in human non-small-cell lung cancer. J. Natl. Cancer Inst. Monogr. 13 (1992) 23-29
93. In: Soanes C., and Stevenson A. (Eds). The Concise Oxford English Dictionary. Twelfth edition (2008), Oxford University Press, Oxford. http://www.oxfordreference.com/views/ENTRY.html%3Fsubview=Main%26entry=t23.e1791 Oxford Reference Online, Accessed 13 July 2009
94. In: Porta M. (Ed). A Dictionary of Epidemiology. 5th edition (2008), Oxford University Press, New York 129-130