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[Cancer Research 60, 1949-1960, April 1, 2000]
© 2000 American Association for Cancer Research

Molecular Biology and Genetics

High Resolution Chromosome 3p Allelotyping of Human Lung Cancer and Preneoplastic/Preinvasive Bronchial Epithelium Reveals Multiple, Discontinuous Sites of 3p Allele Loss and Three Regions of Frequent Breakpoints1

Ignacio I. Wistuba, Carmen Behrens, Arvind K. Virmani, Gina Mele, Sara Milchgrub, Luc Girard, John W. Fondon, III, Harold R. Garner, Bruce McKay, Farida Latif, Michael I. Lerman, Stephen Lam, Adi F. Gazdar and John D. Minna2

Departments of Pathology [A. K. V., S. M., A. F. G.] and Internal Medicine and Pharmacology [J. D. M.], Hamon Center for Therapeutic Oncology Research [I. I. W., C. B., A. K. V., G. M., L. G., A. F. G., J. D. M.] and McDermott Center for Human Growth and Development and the Center for Biomedical Inventions, University of Texas Southwestern Medical Center [J. W. F., H. R. G.], Dallas, Texas 75390; Department of Pathology, Pontificia Universidad Catolica de Chile, Santiago, Chile [I. I. W.]; British Columbia Cancer Agency, Vancouver, British Columbia, V5Z 355 Canada [S. L.]; Department of Paediatrics and Child Health, University of Birmingham, Birmingham B15 2TT, United Kingdom [F. L.]; Laboratory of Immunobiology, National Cancer Institute-Frederick Cancer Research and Development Center, Frederick, Maryland 21702 [M. I. L.]; and Department of Pathology, The University of Texas M. D. Anderson Cancer Center, Houston, Texas 77030 [B. M.]

Allele loss involving chromosome arm 3p is one of the most frequent and earliest known genetic events in lung cancer pathogenesis and may affect several potential tumor suppressor gene regions. To further study the role of chromosome 3p allele loss in the pathogenesis of lung cancer, we performed high resolution loss of heterozygosity (LOH) studies on 97 lung cancer and 54 preneoplastic/preinvasive microdissected respiratory epithelial samples using a panel of 28 3p markers. Allelic losses of 3p were detected in 96% of the lung cancers and in 78% of the preneoplastic/preinvasive lesions. The allele losses were often multiple and discontinuous, with areas of LOH interspersed with areas of retention of heterozygosity. Most small cell lung carcinomas (91%) and squamous cell carcinomas (95%) demonstrated larger 3p segments of allele loss, whereas most (71%) of the adenocarcinomas and preneoplastic/preinvasive lesions had smaller chromosome areas of 3p allele loss. There was a progressive increase in the frequency and size of 3p allele loss regions with increasing severity of histopathological preneoplastic/preinvasive changes. In analyses of the specific parental allele lost comparing 42 preneoplastic/preinvasive foci with those lost in the lung cancer in the same patient (n = 10), the same parental allele was lost in 88% of 244 comparisons for 28 3p markers (P = 1.2 x 10-36 for this occurring by chance). This indicates the occurrence of allele-specific loss in these foci similar to that seen in the tumor by a currently unknown mechanism. Analysis of all of the data indicated multiple regions of localized 3p allele loss including telomere-D3S1597, D3S1111-D3S2432, D3S2432-D3S1537, D3S1537, D3S1537-D3S1612, D3S4604/Luca19.1-D3S4622/Luca4.1, D3S4624/Luca2.1, D3S4624/Luca2.1-D3S1582, D3S1766, D3S1234-D3S1300 (FHIT/FRA3B region centered on D3S1300), D3S1284-D3S1577 (U2020/DUTT1 region centered on D3S1274), and D3S1511-centromere. A panel of six markers in the 600-kb 3p21.3 deletion region showed loss in 77% of the lung cancers, 70% of normal or preneoplastic/preinvasive lesions associated with lung cancer, and 49% of 47 normal, mildly abnormal, or preneoplastic/preinvasive lesions found in smokers without lung cancer; however, loss was seen in 0% of 18 epithelial samples from seven never smokers. The 600-kb 3p21.3 region and the 3p14.2 (FHIT/FRA3B) and 3p12 (U2020/DUTT1) regions were common, independent sites of breakpoints (retention of heterozygosity by some markers and LOH by other markers in the immediate region). We conclude that 3p allele loss is nearly universal in lung cancer pathogenesis; involves multiple, discrete, 3p LOH sites that often show a "discontinuous LOH" pattern in individual tumors; occurs in preneoplastic/preinvasive lesions in smokers with and without lung cancer (multiple lesions often lose the same parental allele); frequently involves breakpoints in at least three very small defined genomic regions; and appears to have allele loss and breakpoints first occurring in the 600-kb 3p21.3 region. These findings are consistent with previously reported LOH studies in a variety of tumors showing allele loss occurring by mitotic recombination and induced by oxidative damage.




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J. A. O'Shaughnessy, G. J. Kelloff, G. B. Gordon, A. J. Dannenberg, W. K. Hong, C. J. Fabian, C. C. Sigman, M. M. Bertagnolli, S. P. Stratton, S. Lam, et al.
Treatment and Prevention of Intraepithelial Neoplasia: An Important Target for Accelerated New Agent Development : Recommendations of the American Association for Cancer Research Task Force on the Treatment and Prevention of Intraepithelial Neoplasia
Clin. Cancer Res., February 1, 2002; 8(2): 314 - 346.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
A. H. Banham, N. Beasley, E. Campo, P. L. Fernandez, C. Fidler, K. Gatter, M. Jones, D. Y. Mason, J. E. Prime, P. Trougouboff, et al.
The FOXP1 Winged Helix Transcription Factor Is a Novel Candidate Tumor Suppressor Gene on Chromosome 3p
Cancer Res., December 1, 2001; 61(24): 8820 - 8829.
[Abstract] [Full Text] [PDF]

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 CarcinogenesisHome page
T. Tsujiuchi, Y. Sasaki, N. Murata, M. Tsutsumi, Y. Konishi, and D. Nakae
FHIT alterations in lung adenocarcinomas induced by N-nitrosobis(2-hydroxypropyl)amine in rats
Carcinogenesis, December 1, 2001; 22(12): 2017 - 2022.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
J. Xian, K. J. Clark, R. Fordham, R. Pannell, T. H. Rabbitts, and P. H. Rabbitts
Inadequate lung development and bronchial hyperplasia in mice with a targeted deletion in the Dutt1/Robo1 gene
PNAS, November 29, 2001; (2001) 251407098.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
Y. Tomizawa, Y. Sekido, M. Kondo, B. Gao, J. Yokota, J. Roche, H. Drabkin, M. I. Lerman, A. F. Gazdar, and J. D. Minna
Inhibition of lung cancer cell growth and induction of apoptosis after reexpression of 3p21.3 candidate tumor suppressor gene SEMA3B
PNAS, November 20, 2001; 98(24): 13954 - 13959.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
Y. Aoyagi, T. Yokose, Y. Minami, A. Ochiai, T. Iijima, Y. Morishita, T. Oda, K. Fukao, and M. Noguchi
Accumulation of Losses of Heterozygosity and Multistep Carcinogenesis in Pulmonary Adenocarcinoma
Cancer Res., November 1, 2001; 61(21): 7950 - 7954.
[Abstract] [Full Text] [PDF]

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 Mol. Pathol.Home page
A Martinez, R A Walker, J A Shaw, S J Dearing, E R Maher, and F Latif
Chromosome 3p allele loss in early invasive breast cancer: detailed mapping and association with clinicopathological features
Mol. Pathol., October 1, 2001; 54(5): 300 - 306.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
D.-S. Byun, M.-G. Lee, K.-S. Chae, B.-G. Ryu, and S.-G. Chi
Frequent Epigenetic Inactivation of RASSF1A by Aberrant Promoter Hypermethylation in Human Gastric Adenocarcinoma
Cancer Res., October 1, 2001; 61(19): 7034 - 7038.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
M.-G. Lee, H.-Y. Kim, D.-S. Byun, S.-J. Lee, C.-H. Lee, J. I. Kim, S.-G. Chang, and S.-G. Chi
Frequent Epigenetic Inactivation of RASSF1A in Human Bladder Carcinoma
Cancer Res., September 1, 2001; 61(18): 6688 - 6692.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
S. Toyooka, H. I. Pass, N. Shivapurkar, Y. Fukuyama, R. Maruyama, K. O. Toyooka, M. Gilcrease, A. Farinas, J. D. Minna, and A. F. Gazdar
Aberrant Methylation and Simian Virus 40 Tag Sequences in Malignant Mesothelioma
Cancer Res., August 1, 2001; 61(15): 5727 - 5730.
[Abstract] [Full Text] [PDF]

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 Am. J. Pathol.Home page
A. Maitra, I. I. Wistuba, C. Washington, A. K. Virmani, R. Ashfaq, S. Milchgrub, A. F. Gazdar, and J. D. Minna
High-Resolution Chromosome 3p Allelotyping of Breast Carcinomas and Precursor Lesions Demonstrates Frequent Loss of Heterozygosity and a Discontinuous Pattern of Allele Loss
Am. J. Pathol., July 1, 2001; 159(1): 119 - 130.
[Abstract] [Full Text] [PDF]

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 JNCI J Natl Cancer InstHome page
D. G. Burbee, E. Forgacs, S. Zochbauer-Muller, L. Shivakumar, K. Fong, B. Gao, D. Randle, M. Kondo, A. Virmani, S. Bader, et al.
Epigenetic Inactivation of RASSF1A in Lung and Breast Cancers and Malignant Phenotype Suppression
J Natl Cancer Inst, May 2, 2001; 93(9): 691 - 699.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
S. Zöchbauer-Müller, K. M. Fong, A. Maitra, S. Lam, J. Geradts, R. Ashfaq, A. K. Virmani, S. Milchgrub, A. F. Gazdar, and J. D. Minna
5' CpG Island Methylation of the FHIT Gene Is Correlated with Loss of Gene Expression in Lung and Breast Cancer
Cancer Res., May 1, 2001; 61(9): 3581 - 3585.
[Abstract] [Full Text]

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 Cancer Res.Home page
I. I. Wistuba, M. Tang, A. Maitra, H. Alvarez, P. Troncoso, F. Pimentel, and A. F. Gazdar
Genome-wide Allelotyping Analysis Reveals Multiple Sites of Allelic Loss in Gallbladder Carcinoma
Cancer Res., May 1, 2001; 61(9): 3795 - 3800.
[Abstract] [Full Text]

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 Proc. Natl. Acad. Sci. USAHome page
N. Rosenberg
New transformation tricks from a barnyard retrovirus: Implications for human lung cancer
PNAS, April 10, 2001; 98(8): 4285 - 4287.
[Full Text] [PDF]

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 Cancer Res.Home page
R. Dammann, G. Yang, and G. P. Pfeifer
Hypermethylation of the CpG Island of Ras Association Domain Family 1A (RASSF1A), a Putative Tumor Suppressor Gene from the 3p21.3 Locus, Occurs in a Large Percentage of Human Breast Cancers
Cancer Res., April 1, 2001; 61(7): 3105 - 3109.
[Abstract] [Full Text]

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 Cancer Res.Home page
T. Liloglou, P. Maloney, G. Xinarianos, M. Hulbert, M. J. Walshaw, J. R. Gosney, L. Turnbull, and J. K. Field
Cancer-specific Genomic Instability in Bronchial Lavage: A Molecular Tool for Lung Cancer Detection
Cancer Res., February 1, 2001; 61(4): 1624 - 1628.
[Abstract] [Full Text]

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 Cancer Res.Home page
M. I. Lerman and J. D. Minna
The 630-kb Lung Cancer Homozygous Deletion Region on Human Chromosome 3p21.3: Identification and Evaluation of the Resident Candidate Tumor Suppressor Genes
Cancer Res., November 1, 2000; 60(21): 6116 - 6133.
[Abstract] [Full Text]

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 JNCI J Natl Cancer InstHome page
A. K. Virmani, A. Rathi, S. Zochbauer-Muller, N. Sacchi, Y. Fukuyama, D. Bryant, A. Maitra, S. Heda, K. M. Fong, F. Thunnissen, et al.
Promoter Methylation and Silencing of the Retinoic Acid Receptor-{beta} Gene in Lung Carcinomas
J Natl Cancer Inst, August 16, 2000; 92(16): 1303 - 1307.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
J. Xian, K. J. Clark, R. Fordham, R. Pannell, T. H. Rabbitts, and P. H. Rabbitts
Inadequate lung development and bronchial hyperplasia in mice with a targeted deletion in the Dutt1/Robo1 gene
PNAS, December 18, 2001; 98(26): 15062 - 15066.
[Abstract] [Full Text] [PDF]


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