Short Telomeres Initiate Telomere Recombination in Primary and Tumor Cells
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{"title"=>"Short telomeres initiate telomere recombination in primary and tumor cells", "type"=>"journal", "authors"=>[{"first_name"=>"Tammy A.", "last_name"=>"Morrish", "scopus_author_id"=>"6603257808"}, {"first_name"=>"Carol W.", "last_name"=>"Greider", "scopus_author_id"=>"7006510554"}], "year"=>2009, "source"=>"PLoS Genetics", "identifiers"=>{"isbn"=>"1553-7404 (Electronic)", "pmid"=>"19180191", "doi"=>"10.1371/journal.pgen.1000357", "pui"=>"354135266", "issn"=>"15537390", "sgr"=>"59249101446", "scopus"=>"2-s2.0-59249101446"}, "id"=>"c24d8af4-5d78-3c18-b582-224c41a3c87b", "abstract"=>"Human tumors that lack telomerase maintain telomeres by alternative lengthening mechanisms. Tumors can also form in telomerase-deficient mice; however, the genetic mechanism responsible for tumor growth without telomerase is unknown. In yeast, several different recombination pathways maintain telomeres in the absence of telomerase-some result in telomere maintenance with minimal effects on telomere length. To examine non-telomerase mechanisms for telomere maintenance in mammalian cells, we used primary cells and lymphomas from telomerase-deficient mice (mTR-/- and Emumyc+mTR-/-) and CAST/EiJ mouse embryonic fibroblast cells. These cells were analyzed using pq-ratio analysis, telomere length distribution outliers, CO-FISH, Q-FISH, and multicolor FISH to detect subtelomeric recombination. Telomere length was maintained during long-term growth in vivo and in vitro. Long telomeres, characteristic of human ALT cells, were not observed in either late passage or mTR-/- tumor cells; instead, we observed only minimal changes in telomere length. Telomere length variation and subtelomeric recombination were frequent in cells with short telomeres, indicating that length maintenance is due to telomeric recombination. We also detected telomere length changes in primary mTR-/- cells that had short telomeres. Using mouse mTR+/- and human hTERT+/- primary cells with short telomeres, we found frequent length changes indicative of recombination. We conclude that telomere maintenance by non-telomerase mechanisms, including recombination, occurs in primary cells and is initiated by short telomeres, even in the presence of telomerase. Most intriguing, our data indicate that some non-telomerase telomere maintenance mechanisms occur without a significant increase in telomere length.", "link"=>"http://www.mendeley.com/research/short-telomeres-initiate-telomere-recombination-primary-tumor-cells", "reader_count"=>66, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>4, "Researcher"=>10, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>27, "Student > Postgraduate"=>3, "Student > Master"=>3, "Other"=>2, "Student > Bachelor"=>9, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>4, "Researcher"=>10, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>27, "Student > Postgraduate"=>3, "Student > Master"=>3, "Other"=>2, "Student > Bachelor"=>9, "Professor"=>2}, "reader_count_by_subject_area"=>{"Engineering"=>2, "Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>6, "Agricultural and Biological Sciences"=>46, "Medicine and Dentistry"=>7, "Chemical Engineering"=>1, "Chemistry"=>1, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>2}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>7}, "Chemistry"=>{"Chemistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>46}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Unspecified"=>{"Unspecified"=>2}, "Chemical Engineering"=>{"Chemical Engineering"=>1}}, "reader_count_by_country"=>{"United States"=>5, "Serbia and Montenegro"=>1}, "group_count"=>4}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/910662"], "description"=>"<p>A and B. Shown are the Q-FISH results on lymphocytes from various individuals in a family harboring a mutation in hTERT (hTERT+/K902N) or from non-carriers hTERT+/+. C. Summary of Q-FISH analysis from related individuals with hTERT+/K902N (n = 4) and hTERT+/+ (n = 6) genotypes. D. The total number of chromosomes with telomere ratio values q/p≥5-fold is plotted on the left y-axis. The black circle denotes the mean telomere length plotted on the right y-axis. Using a T-test (α = .05), comparison of hTERT+/+ with hTERT+/K902N shows a significant difference (P = .02). E. The total number of outliers per metaphase is plotted on the left y-axis. Black circles represent the mean telomere length plotted on the right y-axis. Using a Wilcoxon rank sum test (α = .05) a significantly greater number of outliers were observed in hTERT+/K902N in comparison to hTERT+/+ (P = .034).</p>", "links"=>[], "tags"=>["individuals", "pq-ratio", "changes"], "article_id"=>581123, "categories"=>["Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Tammy A. Morrish", "Carol W. Greider"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000357.g008", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Lymphocytes_from_hTERT_8722_individuals_are_increased_for_pq_ratio_changes_and_outliers_/581123", "title"=>"Lymphocytes from hTERT+/− individuals are increased for pq-ratio changes and outliers.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-01-30 00:18:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/909868"], "description"=>"<p>Telomere fluorescence <i>in situ</i> hybridization on metaphase spreads from primary bone marrow cells isolated from C57BL/6J mice, (A) mTR+/+, (C) mTR−/−G1 and (E) mTR−/−G4. Telomeres were hybridized with a Cy3-5′ (CCCTAA)<sub>3</sub> telomere probe (red) and chromosomes are stained with DAPI (blue). Cy3-fluorescent intensity correlates with telomere length. B, D, F. The ratios (q/p) of the p and q telomere signals for each chromosome are plotted. 8–15 metaphases were examined for each genotype. Ratios (q/p) were calculated based on the telomere fluorescent intensity of the p- and q-arms of a given chromosome. The individual chromosomes assayed for each genotype are shown on the x-axis and the q/p ratio on the y-axis. The y-axis is on a log scale plot and excludes SFEs, since these values cannot be plotted on log scale. Changes in pq-ratios occurred for all metaphases, and were not specific to an individual metaphase, which is appreciated given that the chromosomes from each metaphase are graphed from left to right. G. The bar graph shows the percent of the total number of chromosomes with telomere ratio values of q/p≥5-fold (q/p≥5 or q/p≤0.2). Error bars represent the standard error of the mean. Values are shown for both primary bone marrow and splenocytes. Student T-tests, assuming α = .05, show statistical significance and were used to compare WT and mTR−/−G1 bone marrow (P = 3.8×10<sup>−6</sup>) and splenocytes (P = 8.3×10<sup>−7</sup>). Statistical significance was also observed between WT and mTR−/−G4 bone marrow (P = 3.6×10<sup>−26</sup>) and splenocytes (P = 8.8×10<sup>−18</sup>). Circles represent the mean telomere lengths plotted on the right y-axis. H. Pq-ratio changes determined for primary (pre-tumor) bone marrow and splenocytes as well as B-cell lymphomas plotted on the left y-axis. Error bars represent SEM. The circles represent the mean telomere length plotted on the right y-axis. Statistical significance was observed using a T-test (α = .05) between myc+mTR+/+ and myc+mTR−/−G1 primary bone marrow (P = 2.3×10<sup>−8</sup>) and splenocytes (P = 6.6×10<sup>−7</sup>). Similarly, statistical significance was observed between myc+mTR+/+ and myc+mTR−/−G4/G6 primary bone marrow (P = 1.4×10<sup>−18</sup>) and splenocytes (P = 3.3×10<sup>−15</sup>).</p>", "links"=>[], "tags"=>["changes", "cells"], "article_id"=>580329, "categories"=>["Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Tammy A. Morrish", "Carol W. Greider"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000357.g002", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Pq_ratio_changes_are_increased_in_early_and_late_generation_in_mTR_8722_8722_cells_with_short_telomeres_/580329", "title"=>"Pq-ratio changes are increased in early and late generation in mTR−/− cells with short telomeres.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-01-30 00:05:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/910000"], "description"=>"<p>Data acquired from Q-FISH were used to generate box plots. The darkened line within the box represents the 50<sup>th</sup> percentile, the median telomere length of the distribution. The box includes telomere length values and is approximately one standard deviation. The lines extending from outside the box represent approximately two standard deviations (95<sup>th</sup> and 5<sup>th</sup> percentile). Telomere lengths outside of these are outliers and appear as dots. Since some data points overlap, the total amount of outliers is graphically quantitated in B, and is normalized for the total number of metaphases examined. B. The graph shows the total number of outliers divided by the total number of metaphases (n) for each genotype plotted on the left y-axis. Error bars represent the standard error of the mean (SEM). Circles reflect the mean telomere length plotted on the right y-axis. Calculated p-values (α = .05) using the Wilcoxon rank sum test indicate a statistically significant difference between mTR+/+ and mTR−/−G4 bone marrow (P = .004). Similarly mTR−/−G4 splenocytes have a statistically greater number of outliers in comparison to mTR+/+ splenocytes (P = .008).</p>", "links"=>[], "tags"=>["cells", "greater", "telomere"], "article_id"=>580458, "categories"=>["Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Tammy A. Morrish", "Carol W. Greider"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000357.g003", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Late_generation_mTR_8722_8722_primary_cells_have_a_significantly_greater_number_of_telomere_outliers_/580458", "title"=>"Late generation mTR−/− primary cells have a significantly greater number of telomere outliers.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-01-30 00:07:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/910321"], "description"=>"<p>A and B. Q-FISH on primary bone marrow isolated from early generation (HG1×HG1) and late generation (HG5×HG5) CAST/EiJ mice. The breeding scheme used to generate the CAST/EiJ mice is shown above the Q-FISH plots. C. Southern analysis on bone marrow cells isolated from the same mice shown in A and B. D. The pq-ratios of primary bone marrow cells are plotted as described above. The percent of the total number of chromosomes with telomere ratio values q/p≥5-fold is plotted on the left y-axis. The circles represent the mean telomere lengths of each genotype plotted on the right y-axis. A T-test (α = .05) was used to determine statistical significance between WT bone marrow cells versus WT6* (P = .04), HG6 (P = .002), KO<sub>(G2)</sub> (P = 8.8×10<sup>−5</sup>), and KO<sub>(G6)</sub> (P = 5.9×10<sup>−11</sup>). E. Summary of outliers generated from box plots. The outliers per metaphase are plotted on the left y-axis. The circles represent the mean telomere length plotted on the right y-axis. A Wilcoxon rank sum test (α = .05) was used to calculate statistical significance between WT versus HG2 (P = .009), KO<sub>(G2)</sub> (P = .016) and KO<sub>(G6)</sub> (P = .0001).</p>", "links"=>[], "tags"=>["telomeres", "telomerase", "pq-ratio"], "article_id"=>580781, "categories"=>["Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Tammy A. Morrish", "Carol W. Greider"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000357.g006", "stats"=>{"downloads"=>2, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Short_CAST_EiJ_telomeres_even_in_the_presence_of_telomerase_show_increased_pq_ratio_changes_/580781", "title"=>"Short CAST/EiJ telomeres even in the presence of telomerase show increased pq-ratio changes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-01-30 00:13:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/909717"], "description"=>"<p>A. Growth curves for CAST/EiJ MEFs derived from littermates from an HG1×HG1 cross. Cells were passaged according to previous reports <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000357#pgen.1000357-Todaro1\" target=\"_blank\">[31]</a>. Cell growth increased after a brief period of senescence and cells were considered immortalized after passage 16. B. Q-FISH on myc+mTR+/+ lymphomas serially passaged in SCID mice. C. Q-FISH on myc+mTR−/−G5 lymphomas serially passaged in SCID mice. D–F. Shown are the Q-FISH analysis of MEFs at passage 3 (p3), passage 29 (p29), and passage 45 (p45). The telomere lengths of both the HG2 and KO<sub>(G2)</sub> were not dramatically lengthened. D. The WT2* mean telomere lengths are 3.1×10<sup>5</sup>, 3.5×10<sup>5</sup>, and 1.6×10<sup>5</sup>, the amount of signal free ends (SFEs) were, 1, 4, and 9, for p3, p29 and p45 respectively. E. For HG2 the mean telomere lengths were 2.6×10<sup>5</sup>, 2.0×10<sup>5</sup>, and 1.8×10<sup>5</sup> and the SFEs were, 2, 23, and 19 for p3, p29 and p45 respectively. F. The mean telomere lengths for the KO<sub>(G2)</sub> were 2.6×10<sup>5</sup>, 1.5×10<sup>5</sup>, and 1.3×10<sup>5</sup>, and the amount of SFEs were 16, 44, and 156 for P3, p29 and p45 respectively.</p>", "links"=>[], "tags"=>["occurs"], "article_id"=>580175, "categories"=>["Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Tammy A. Morrish", "Carol W. Greider"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000357.g001", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Telomere_maintenance_occurs_in_mTR_8722_8722_cells_/580175", "title"=>"Telomere maintenance occurs in mTR−/− cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-01-30 00:02:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/910198"], "description"=>"<p>A. The breeding scheme used to generate intergenerational (iG6) mice results in progeny with half short and half long telomeres. B. Q-FISH on primary bone marrow cells isolated from mTR−/− iG6 and mTR+/−iG6 mice. The arrow points to the class of shortest telomeres that persist in the iG6 mTR−/− mice. C. Summary of pq-ratio analysis on bone marrow cells. Circles represent the mean telomere length. Using a T-test (α = .05) statistical significance was observed between the number of ratios with q/p≥5-fold for mTR−/− iG6 and mTR+/− iG6 bone marrow cells (P = 2.2×10<sup>−15</sup>). D. Box plot analysis used to determine the number of telomere “outliers” is plotted on the left y-axis. Circles represent the mean telomere length and are plotted on the right y-axis. Using a Wilcoxon rank sum test (α = .05), mTR−/− iG6 bone marrow cells have a statistically greater number of outliers compared to mTR+/− iG6 (P = .003).</p>", "links"=>[], "tags"=>["cells", "intergenerational", "pq-ratio", "changes"], "article_id"=>580656, "categories"=>["Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Tammy A. Morrish", "Carol W. Greider"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000357.g005", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_iG6_mTR_8722_8722_cells_from_an_intergenerational_cross_have_an_increase_in_pq_ratio_changes_and_outliers_/580656", "title"=>"iG6 mTR−/− cells from an intergenerational cross have an increase in pq-ratio changes and outliers.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-01-30 00:10:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/910477"], "description"=>"<p>A. A diagram of CO-FISH analysis. In the CO-FISH assay, cells are grown in the presence of 5-bromo-2-deoxyuridine (BrdU). After one round of replication one strand (green) has incorporated BrdU. Metaphases are treated with Hoechst and UV treated, which nicks the BrdU incorporated strand. The nicked strands are then degraded with an exonuclease, followed by hybridization with a telomere probe. B–D. CO-FISH on primary bone marrow cells isolated from the progeny of late generation (HG5×HG5) CAST/EiJ mice WT6* (n = 3), HG6 (n = 3) and KO<sub>(G6)</sub> (n = 3). WT (n = 3) mice were also examined. E. Summary of T-SCEs in primary CAST/EiJ bone marrow cells. A T-test (α = .05) was used and showed a significant increase in the amount of T-SCEs in primary KO<sub>(G6)</sub> bone marrow (P = .003) compared to WT bone marrow.</p>", "links"=>[], "tags"=>["detects", "exchanges"], "article_id"=>580937, "categories"=>["Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Tammy A. Morrish", "Carol W. Greider"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000357.g007", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_CO_FISH_detects_frequent_exchanges_in_only_some_primary_mTR_8722_8722_cells_/580937", "title"=>"CO-FISH detects frequent exchanges in only some primary mTR−/− cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-01-30 00:15:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/449862", "https://ndownloader.figshare.com/files/449919", "https://ndownloader.figshare.com/files/449984", "https://ndownloader.figshare.com/files/450040"], "description"=>"<div><p>Human tumors that lack telomerase maintain telomeres by alternative lengthening mechanisms. Tumors can also form in telomerase-deficient mice; however, the genetic mechanism responsible for tumor growth without telomerase is unknown. In yeast, several different recombination pathways maintain telomeres in the absence of telomerase—some result in telomere maintenance with minimal effects on telomere length. To examine non-telomerase mechanisms for telomere maintenance in mammalian cells, we used primary cells and lymphomas from telomerase-deficient mice (mTR−/− and Eμmyc+mTR−/−) and CAST/EiJ mouse embryonic fibroblast cells. These cells were analyzed using pq-ratio analysis, telomere length distribution outliers, CO-FISH, Q-FISH, and multicolor FISH to detect subtelomeric recombination. Telomere length was maintained during long-term growth <em>in vivo</em> and <em>in vitro</em>. Long telomeres, characteristic of human ALT cells, were not observed in either late passage or mTR−/− tumor cells; instead, we observed only minimal changes in telomere length. Telomere length variation and subtelomeric recombination were frequent in cells with short telomeres, indicating that length maintenance is due to telomeric recombination. We also detected telomere length changes in primary mTR−/− cells that had short telomeres. Using mouse mTR+/− and human hTERT+/− primary cells with short telomeres, we found frequent length changes indicative of recombination. We conclude that telomere maintenance by non-telomerase mechanisms, including recombination, occurs in primary cells and is initiated by short telomeres, even in the presence of telomerase. Most intriguing, our data indicate that some non-telomerase telomere maintenance mechanisms occur without a significant increase in telomere length.</p></div>", "links"=>[], "tags"=>["telomeres", "telomere", "recombination", "cells"], "article_id"=>148668, "categories"=>["Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Tammy A. Morrish", "Carol W. Greider"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1000357.s001", "https://dx.doi.org/10.1371/journal.pgen.1000357.s002", "https://dx.doi.org/10.1371/journal.pgen.1000357.s003", "https://dx.doi.org/10.1371/journal.pgen.1000357.s004"], "stats"=>{"downloads"=>5, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Short_Telomeres_Initiate_Telomere_Recombination_in_Primary_and_Tumor_Cells/148668", "title"=>"Short Telomeres Initiate Telomere Recombination in Primary and Tumor Cells", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2009-01-30 02:24:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/910081"], "description"=>"<p>Multicolor FISH using a BAC that maps to the subtelomeric region (green) of mouse chromosome 2 hybridized to metaphase spreads. Chromosome 2 was hybridized with a chromosome specific probe (red). Chromosomes with subtelomeric amplification are indicated with a white arrow. A. mTR+/+ bone marrow. B–C. Eμmyc+mTR−/−G5 tumors have amplified this subtelomeric sequence to other chromosomes, white arrows. D. Percent of metaphases with subtelomeric amplification (left, y-axis) and the mean telomere length (right, y-axis). Error bars represent the standard deviation. Subtelomeric amplification is increased in cells with short telomeres, and also appears at reduced levels in myc+mTR+/+ lymphomas. Fifty metaphases were scored for each genotype. Student T-tests, assuming α = .05, show statistical significance difference between the myc+mTR+/+ and the myc+mTR−/−G5 lymphomas (P = 5.0×10<sup>−5</sup>). E. Cells with an increased number of pq-ratio changes are also elevated for subtelomeric amplification. Error bars represent the standard deviation. Student T-tests, assuming α = .05, show statistical significance difference between the myc+mTR+/+ and the myc+mTR−/−G5 lymphomas (P = 6.8×10<sup>−6</sup>).</p>", "links"=>[], "tags"=>["recombination"], "article_id"=>580542, "categories"=>["Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Tammy A. Morrish", "Carol W. Greider"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000357.g004", "stats"=>{"downloads"=>3, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Subtelomeric_recombination_is_frequent_in_E_956_myc_mTR_8722_8722_G5_tumors_/580542", "title"=>"Subtelomeric recombination is frequent in Eμmyc+mTR−/−G5 tumors.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-01-30 00:09:02"}

PMC Usage Stats | Further Information

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Relative Metric

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