Novel automated three-dimensional genome scanning based on the nuclear architecture of telomeres

Cytometry Part A

Volumn 79 A, Issue 2, 2011, Pages 159-166

  Klewes, Ludger ^a   Höbsch, Clemens ^a,b   Katzir, Nir ^c   Rourke, David ^d   Garini, Yuval ^e   Mai, Sabine ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

^b Bonn Rhine Sieg University of Applied Sciences   (Germany)

^c Applied Spectral Imaging   (Israel)

^d Applied Spectral Imaging   (United States)

^e BAR ILAN UNIVERSITY   (Israel)

Author keywords

3D nucleus; Automated 3D scanning; Cancer; Telomeres

Indexed keywords

ANIMAL; ARTICLE; CELL NUCLEUS; FLUORESCENCE IN SITU HYBRIDIZATION; GENETICS; GENOME; INTERPHASE; LYMPHOCYTE; MALE; METHODOLOGY; MICROSCOPY; MOUSE; NEOPLASM; PLASMACYTOMA; SENSITIVITY AND SPECIFICITY; TELOMERE; THREE DIMENSIONAL IMAGING; TUMOR CELL LINE; ULTRASTRUCTURE;

ANIMALS; CELL LINE, TUMOR; CELL NUCLEUS; GENOME; IMAGING, THREE-DIMENSIONAL; IN SITU HYBRIDIZATION, FLUORESCENCE; INTERPHASE; LYMPHOCYTES; MALE; MICE; MICROSCOPY; NEOPLASMS; PLASMACYTOMA; SENSITIVITY AND SPECIFICITY; TELOMERE;

EID: 79251516396     PISSN: 15524922     EISSN: 15524930     Source Type: Journal    
DOI: 10.1002/cyto.a.21012     Document Type: Article

References (68)

1. Charames GS, Bapat B. Genomic instability and cancer. Curr Mol Med 2003; 3: 589-596.
2. Mai S. Initiation of telomere-mediated chromosomal rearrangements in cancer. J Cell Biochem 2010; 109: 1095-1102.
3. Rai R, Zheng H, He H, Luo Y, Multani A, Carpenter PB, Chang S. The function of classical and alternative non-homologous end-joining pathways in the fusion of dysfunctional telomeres. EMBO J 2010; 29: 2598-2610.
4. Lamarche BJ, Orazio NI, Weitzman MD. The MRN complex in double-strand break repair and telomere maintenance. FEBS Lett 2010; 584: 3682-3695.
5. Griffith JK, Bryant JE, Fordyce CA, Gilliland FD, Joste NE, Moyzis RK. Reduced telomere DNA content is correlated with genomic instability and metastasis in invasive human breast carcinoma. Breast Cancer Res Treat 1999; 54: 59-64.
6. Meeker AK, Hicks JL, Gabrielson E, Strauss WM, De Marzo AM, Argani P. Telomere shortening occurs in subsets of normal breast epithelium as well as in situ and invasive carcinoma. Am J Pathol 2004; 164: 925-935.
7. Odagiri E, Kanada N, Jibiki K, Demura R, Aikawa E, Demura H. Reduction of telomeric length and c-erbB-2 gene amplification in human breast cancer, fibroadenoma, and gynecomastia. Relationship to histologic grade and clinical parameters. Cancer 1994; 73: 2978-2984.
8. Heaphy CM, Fleet TM, Treat EG, Lee SJ, Smith AY, Davis MS, Griffith JK, Fischer EG, Bisoffi M. Organ-wide telomeric status in diseased and disease-free prostatic tissues. Prostate 2010; 70: 1471-1479.
9. Meeker AK, Hicks JL, Platz EA, March GE, Bennett CJ, Delannoy MJ, De Marzo AM. Telomere shortening is an early somatic DNA alteration in human prostate tumorigenesis. Cancer Res 2002; 62: 6405-6409.
10. Mirabello L, Yu K, Kraft P, De Vivo I, Hunter DJ, Prescott J, Wong JY, Chatterjee N, Hayes RB, Savage SA. The association of telomere length and genetic variation in telomere biology genes. Hum Mutat 2010; 31: 1050-1058.
11. Gadji M, Fortin D, Tsanaclis AM, Garini Y, Katzir N, Wienburg Y, Yan J, Klewes L, Klonisch T, Drouin R, Mai S. Three-dimensional nuclear telomere architecture is associated with differential time to progression and overall survival in glioblastoma patients. Neoplasia 2010; 12: 183-191.
12. Ohali A, Avigad S, Ash S, Goshen Y, Luria D, Feinmesser M, Zaizov R, Yaniv I. Telomere length is a prognostic factor in neuroblastoma. Cancer 2006; 107: 1391-1399.
13. Zheng YL, Hu N, Sun Q, Wang C, Taylor PR. Telomere attrition in cancer cells and telomere length in tumor stroma cells predict chromosome instability in esophageal squamous cell carcinoma: A genome-wide analysis. Cancer Res 2009; 69: 1604-1614.
14. Knecht H, Bruderlein S, Mai S, Moller P, Sawan B. 3D structural and functional characterization of the transition from Hodgkin to Reed-Sternberg cells. Ann Anat 2010; 192: 302-308.
15. Knecht H, Mai S. 3D imaging of telomeres and nuclear architecture: An emerging tool of 3D nano-morphology based diagnosis. J Cell Physiol 2010; Sep 20 [Epub ahead of print].
16. Knecht H, Sawan B, Lichtensztejn D, Lemieux B, Wellinger RJ, Mai S. The 3D nuclear organization of telomeres marks the transition from Hodgkin to Reed-Sternberg cells. Leukemia 2009; 23: 565-573.
17. Knecht H, Sawan B, Lichtensztejn Z, Lichtensztejn D, Mai S. 3D telomere FISH defines LMP1-expressing reed-sternberg cells as end-stage cells with telomere-poor "ghost" nuclei and very short telomeres. Lab Invest 2010; 90: 611-619.
18. Mai S, Garini Y. The significance of telomeric aggregates in the interphase nuclei of tumor cells. J Cell Biochem 2006; 97: 904-915.
19. Denoix PF. Enquete permanent dans les centres anticancereaux. Bull Inst Nat Hyg 1946; 1: 70-75.
20. Rai KR, Sawitsky A, Cronkite EP, Chanana AD, Levy RN, Pasternack BS. Clinical staging of chronic lymphocytic leukemia. Blood 1975; 46: 219-234.
21. Binet JL, Auquier A, Dighiero G, Chastang C, Piguet H, Goasguen J, Vaugier G, Potron G, Colona P, Oberling F, et al. A new prognostic classification of chronic lymphocytic leukemia derived from a multivariate survival analysis. Cancer 1981; 48: 198-206.
22. van 't Veer LJ, Dai H, van de Vijver MJ, He YD, Hart AA, Mao M, Peterse HL, van der Kooy K, Marton MJ, Witteveen AT, et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature 2002; 415: 530-536.
23. Faca V, Pitteri SJ, Newcomb L, Glukhova V, Phanstiel D, Krasnoselsky A, Zhang Q, Struthers J, Wang H, Eng J, et al. Contribution of protein fractionation to depth ofanalysis of the serum and plasma proteomes. J Proteome Res 2007; 6: 3558-3565.
24. Hanash SM, Pitteri SJ, Faca VM. Mining the plasma proteome for cancer biomarkers. Nature 2008; 452: 571-579.
25. Pitteri SJ, JeBailey L, Faca VM, Thorpe JD, Silva MA, Ireton RC, Horton MB, Wang H, Pruitt LC, Zhang Q, et al. Integrated proteomic analysis of human cancer cells and plasma from tumor bearing mice for ovarian cancer biomarker discovery. PLoS One 2009; 4: e7916.
26. Sawyers CL. The cancer biomarker problem. Nature 2008; 452: 548-552.
27. Burke HB. Outcome prediction and the future of the TNM staging system. J Natl Cancer Inst 2004; 96: 1408-1409.
28. Hammond ME, Taube SE. Issues and barriers to development of clinically useful tumor markers: A development pathway proposal. Semin Oncol 2002; 29: 213-221.
29. Ludwig JA, Weinstein JN. Biomarkers in cancer staging, prognosis and treatment selection. Nat Rev Cancer 2005; 5: 845-856.
30. Yarbro JW, Page DL, Fielding LP, Partridge EE, Murphy GP. American Joint Committee on Cancer prognostic factors consensus conference. Cancer 1999; 86: 2436-2446.
31. Louis SF, Vermolen BJ, Garini Y, Young IT, Guffei A, Lichtensztejn Z, Kuttler F, Chuang TC, Moshir S, Mougey V, et al. c-Myc induces chromosomal rearrangements through telomere and chromosome remodeling in the interphase nucleus. Proc Natl Acad Sci USA 2005; 102: 9613-9618.
32. Rastan S. Non-random X-chromosome inactivation in mouse X-autosome translocation embryos-Location of the inactivation centre. J Embryol Exp Morphol 1983; 78: 1-22.
33. Wiener F, Schmälter A-K, Mowat MRA, Mai S. Duplication of subcytoband 11E2 of chromosome 11 is regularly associated with accelerated tumor development in v-abl/myc-induced mouse plasmacytomas. Genes and Cancer 2010; 1: 847-858
34. Caporali A, Wark L, Vermolen BJ, Garini Y, Mai S. Telomeric aggregates and end-to-end chromosomal fusions require myc box II. Oncogene 2007; 26: 1398-1406.
35. Chuang TC, Moshir S, Garini Y, Chuang AY, Young IT, Vermolen B, van den Doel R, Mougey V, Perrin M, Braun M, et al. The three-dimensional organization of telomeres in the nucleus of mammalian cells. BMC Biol 2004; 2: 12.
36. Kim SH, McQueen PG, Lichtman MK, Shevach EM, Parada LA, Misteli T. Spatial genome organization during T-cell differentiation. Cytogenet Genome Res 2004; 105: 292-301.
37. Mai S, Wiener F. Murine FISH. In: Beatty M, Mai S, Squire J, editors. FISH: A Practical Approach. Oxford, UK: Oxford University Press; 2002. pp 55-67.
38. Vermolen BJ, Garini Y, Mai S, Mougey V, Fest T, Chuang TC, Chuang AY, Wark L, Young IT. Characterizing the three-dimensional organization of telomeres. Cytometry A 2005; 67A: 144-150.
39. Mai S, Garini Y. Oncogenic remodeling of the three-dimensional organization of the interphase nucleus: c-Myc induces telomeric aggregates whose formation precedes chromosomal rearrangements. Cell Cycle 2005; 4: 1327-1331.
40. Knecht H, Kongruttanachok N, Sawan B, Lichtensztejn Z, Lichtensztejn D, Mai S. 3D Telomere Dynamics in Hodgkin's Lymphoma, 52nd ASH Meeting, Orlando, Florida; 2010.
41. Cremer T, Cremer M. Chromosome Territories. Cold Spring Harb Perspect Biol 2010; 2: a003889.
42. De Vos WH, Hoebe RA, Joss GH, Haffmans W, Baatout S, Van Oostveldt P, Manders EM. Controlled light exposure microscopy reveals dynamic telomere microterritories throughout the cell cycle. Cytometry A 2009; 75A: 428-439.
43. McClintock B. The fusion of broken ends of chromosomes following nuclear fusion. Proc Natl Acad Sci USA 1942; 28: 458-463.
44. Müller HJ. The making of chromosomes. Collecting Net 1938; 13: 181-198.
45. Fang DC, Yang SM, Zhou XD, Wang DX, Luo YH. Telomere erosion is independent of microsatellite instability but related to loss of heterozygosity in gastric cancer. World J Gastroenterol 2001; 7: 522-526.
46. Maruyama Y, Hanai H, Fujita M, Kaneko E. Telomere length and telomerase activity in carcinogenesis of the stomach. Jpn J Clin Oncol 1997; 27: 216-220.
47. Engelhardt M, Drullinsky P, Guillem J, Moore MA. Telomerase and telomere length in the development and progression of premalignant lesions to colorectal cancer. Clin Cancer Res 1997; 3: 1931-1941.
48. Lantuejoul S, Soria JC, Morat L, Lorimier P, Moro-Sibilot D, Sabatier L, Brambilla C, Brambilla E. Telomere shortening and telomerase reverse transcriptase expression in preinvasive bronchial lesions. Clin Cancer Res 2005; 11: 2074-2082.
49. Savage SA, Chanock SJ, Lissowska J, Brinton LA, Richesson D, Peplonska B, Bardin-Mikolajczak A, Zatonski W, Szeszenia-Dabrowska N, Garcia-Closas M. Genetic variation in five genes important in telomere biology and risk for breast cancer. Br J Cancer 2007; 97: 832-836.
50. Savage SA, Alter BP. The role of telomere biology in bone marrow failure and other disorders. Mech Ageing Dev 2008; 129: 35-47.
51. Cottliar A, Pedrazzini E, Corrado C, Engelberger MI, Narbaitz M, Slavutsky I. Telomere shortening in patients with plasma cell disorders. Eur J Haematol 2003; 71: 334-340.
52. Wu KD, Orme LM, Shaughnessy JJr, Jacobson J, Barlogie B, Moore MA. Telomerase and telomere length in multiple myeloma: Correlations with disease heterogeneity, cytogenetic status, and overall survival. Blood 2003; 101: 4982-4989.
53. Lin TT, Letsolo BT, Jones RE, Rowson J, Pratt G, Hewamana S, Fegan C, Pepper C, Baird DM. Telomere dysfunction and fusion during the progression of chronic lymphocytic leukemia: Evidence for a telomere crisis. Blood 2010; 116: 1899-1907.
54. Alter BP, Baerlocher GM, Savage SA, Chanock SJ, Weksler BB, Willner JP, Peters JA, Giri N, Lansdorp PM. Very short telomere length by flow fluorescence in situ hybridization identifies patients with dyskeratosis congenita. Blood 2007; 110: 1439-1447.
55. van Heek NT, Meeker AK, Kern SE, Yeo CJ, Lillemoe KD, Cameron JL, Offerhaus GJ, Hicks JL, Wilentz RE, Goggins MG, et al. Telomere shortening is nearly universal in pancreatic intraepithelial neoplasia. Am J Pathol 2002; 161: 1541-1547.
56. Finley JC, Reid BJ, Odze RD, Sanchez CA, Galipeau P, Li X, Self SG, Gollahon KA, Blount PL, Rabinovitch PS. Chromosomal instability in Barrett's esophagus is related to telomere shortening. Cancer Epidemiol Biomarkers Prev 2006; 15: 1451-1457.
57. Samassekou O, Gadji M, Drouin R, Yan J. Sizing the ends: Normal length of human telomeres. Ann Anat 2010; 192: 284-291.
58. Therkelsen AJ, Nielsen A, Koch J, Hindkjaer J, Kolvraa S. Staining of human telomeres with primed in situ labeling (PRINS). Cytogenet Cell Genet 1995; 68: 115-118.
59. Yan J, Chen BZ, Bouchard EF, Drouin R. The labeling efficiency of human telomeres is increased by double-strand PRINS. Chromosoma 2004; 113: 204-209.
60. Baerlocher GM, Lansdorp PM. Telomere length measurements in leukocyte subsets by automated multicolor flow-FISH. Cytometry A 2003; 55A: 1-6.
61. Baerlocher GM, Mak J, Tien T, Lansdorp PM. Telomere length measurement by fluorescence in situ hybridization and flow cytometry: Tips and pitfalls. Cytometry 2002; 47: 89-99.
62. Rufer N, Dragowska W, Thornbury G, Roosnek E, Lansdorp PM. Telomere length dynamics in human lymphocyte subpopulations measured by flow cytometry. Nat Biotechnol 1998; 16: 743-747.
63. Canela A, Vera E, Klatt P, Blasco MA. High-throughput telomere length quantification by FISH and its application to human population studies. Proc Natl Acad Sci USA 2007; 104: 5300-5305.
64. Narath R, Lorch T, Greulich-Bode KM, Boukamp P, Ambros PF. Automatic telomere length measurements in interphase nuclei by IQ-FISH. Cytometry A 2005; 68A: 113-120.
65. Hiyama E, Hiyama K. Telomerase as tumor marker. Cancer Lett 2003; 194: 221-233.
66. Poon SS, Lansdorp PM. Quantitative fluorescence in situ hybridization (Q-FISH). Curr Protoc Cell Biol 2001; 14. Chapter 18:unit 18.4.
67. Narath R, Lorch T, Rudas M, Ambros PF. Automatic quantification of gene amplification in clinical samples by IQ-FISH. Cytometry B Clin Cytom 2004; 57B: 15-22.
68. Xu T, Lu B, Tai YC, Goldkorn A. A cancer detection platform which measures telomerase activity from live circulating tumor cells captured on a microfilter. Cancer Res 2010; 70: 6420-6426.