Oncogene-like addiction to aneuploidy in human cancers
Most cancers exhibit aneuploidy, but its functional significance in tumor development is controversial. Here, we describe ReDACT (Restoring Disomy in Aneuploid cells using CRISPR Targeting), a set of chromosome engineering tools that allow us to eliminate specific aneuploidies from cancer genomes. U...
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| Published in | Science (American Association for the Advancement of Science) Vol. 381; no. 6660; p. eadg4521 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
The American Association for the Advancement of Science
25.08.2023
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Most cancers exhibit aneuploidy, but its functional significance in tumor development is controversial. Here, we describe ReDACT (Restoring Disomy in Aneuploid cells using CRISPR Targeting), a set of chromosome engineering tools that allow us to eliminate specific aneuploidies from cancer genomes. Using ReDACT, we created a panel of isogenic cells that have or lack common aneuploidies, and we demonstrate that trisomy of chromosome 1q is required for malignant growth in cancers harboring this alteration. Mechanistically, gaining chromosome 1q increases the expression of
MDM4
and suppresses p53 signaling, and we show that
TP53
mutations are mutually exclusive with 1q aneuploidy in human cancers. Thus, tumor cells can be dependent on specific aneuploidies, raising the possibility that these “aneuploidy addictions” could be targeted as a therapeutic strategy.
Aneuploidies, which are changes in the numbers of whole chromosomes or chromosome arms, are common in cancer, but their contributions to cancer cell survival have been difficult to pinpoint. Girish
et al
. developed a chromosome-engineering tool to orchestrate the targeted loss of aneuploid chromosome arms and thereby compare isogenic cancer cell lines with and without selected trisomies. The authors discovered that trisomy of chromosome 1q in particular is advantageous to cancer cells and phenocopies the loss of tumor suppressor
TP53
signaling. Tumors with this aneuploidy are sensitive to compounds activated by an enzyme encoded on chromosome 1q, suggesting a potential therapeutic approach. —Yevgeniya Nusinovich
Specific aneuploidies benefit cancer cells and may be sensitive to treatment |
|---|---|
| AbstractList | Most cancers exhibit aneuploidy, but its functional significance in tumor development is controversial. Here, we describe ReDACT (Restoring Disomy in Aneuploid cells using CRISPR Targeting), a set of chromosome engineering tools that allow us to eliminate specific aneuploidies from cancer genomes. Using ReDACT, we created a panel of isogenic cells that have or lack common aneuploidies, and we demonstrate that trisomy of chromosome 1q is required for malignant growth in cancers harboring this alteration. Mechanistically, gaining chromosome 1q increases the expression of
and suppresses p53 signaling, and we show that
mutations are mutually exclusive with 1q aneuploidy in human cancers. Thus, tumor cells can be dependent on specific aneuploidies, raising the possibility that these "aneuploidy addictions" could be targeted as a therapeutic strategy. Most cancers exhibit aneuploidy, but its functional significance in tumor development is controversial. Here, we describe ReDACT ( Re storing D isomy in A neuploid cells using C RISPR T argeting), a set of chromosome engineering tools that allow us to eliminate specific aneuploidies from cancer genomes. Using ReDACT, we created a panel of isogenic cells that have or lack common aneuploidies, and we demonstrate that trisomy of chromosome 1q is required for malignant growth in cancers harboring this alteration. Mechanistically, gaining chromosome 1q increases the expression of MDM4 and suppresses p53 signaling, and we show that TP53 mutations are mutually-exclusive with 1q aneuploidy in human cancers. Thus, tumor cells can be dependent on specific aneuploidies, raising the possibility that these “aneuploidy addictions” could be targeted as a therapeutic strategy. Most cancers exhibit aneuploidy, but its functional significance in tumor development is controversial. Here, we describe ReDACT (Restoring Disomy in Aneuploid cells using CRISPR Targeting), a set of chromosome engineering tools that allow us to eliminate specific aneuploidies from cancer genomes. Using ReDACT, we created a panel of isogenic cells that have or lack common aneuploidies, and we demonstrate that trisomy of chromosome 1q is required for malignant growth in cancers harboring this alteration. Mechanistically, gaining chromosome 1q increases the expression of MDM4 and suppresses p53 signaling, and we show that TP53 mutations are mutually exclusive with 1q aneuploidy in human cancers. Thus, tumor cells can be dependent on specific aneuploidies, raising the possibility that these “aneuploidy addictions” could be targeted as a therapeutic strategy. Aneuploidies, which are changes in the numbers of whole chromosomes or chromosome arms, are common in cancer, but their contributions to cancer cell survival have been difficult to pinpoint. Girish et al . developed a chromosome-engineering tool to orchestrate the targeted loss of aneuploid chromosome arms and thereby compare isogenic cancer cell lines with and without selected trisomies. The authors discovered that trisomy of chromosome 1q in particular is advantageous to cancer cells and phenocopies the loss of tumor suppressor TP53 signaling. Tumors with this aneuploidy are sensitive to compounds activated by an enzyme encoded on chromosome 1q, suggesting a potential therapeutic approach. —Yevgeniya Nusinovich Specific aneuploidies benefit cancer cells and may be sensitive to treatment Most cancers exhibit aneuploidy, but its functional significance in tumor development is controversial. Here, we describe ReDACT (Restoring Disomy in Aneuploid cells using CRISPR Targeting), a set of chromosome engineering tools that allow us to eliminate specific aneuploidies from cancer genomes. Using ReDACT, we created a panel of isogenic cells that have or lack common aneuploidies, and we demonstrate that trisomy of chromosome 1q is required for malignant growth in cancers harboring this alteration. Mechanistically, gaining chromosome 1q increases the expression of MDM4 and suppresses p53 signaling, and we show that TP53 mutations are mutually exclusive with 1q aneuploidy in human cancers. Thus, tumor cells can be dependent on specific aneuploidies, raising the possibility that these "aneuploidy addictions" could be targeted as a therapeutic strategy.Most cancers exhibit aneuploidy, but its functional significance in tumor development is controversial. Here, we describe ReDACT (Restoring Disomy in Aneuploid cells using CRISPR Targeting), a set of chromosome engineering tools that allow us to eliminate specific aneuploidies from cancer genomes. Using ReDACT, we created a panel of isogenic cells that have or lack common aneuploidies, and we demonstrate that trisomy of chromosome 1q is required for malignant growth in cancers harboring this alteration. Mechanistically, gaining chromosome 1q increases the expression of MDM4 and suppresses p53 signaling, and we show that TP53 mutations are mutually exclusive with 1q aneuploidy in human cancers. Thus, tumor cells can be dependent on specific aneuploidies, raising the possibility that these "aneuploidy addictions" could be targeted as a therapeutic strategy. Editor’s summaryAneuploidies, which are changes in the numbers of whole chromosomes or chromosome arms, are common in cancer, but their contributions to cancer cell survival have been difficult to pinpoint. Girish et al. developed a chromosome-engineering tool to orchestrate the targeted loss of aneuploid chromosome arms and thereby compare isogenic cancer cell lines with and without selected trisomies. The authors discovered that trisomy of chromosome 1q in particular is advantageous to cancer cells and phenocopies the loss of tumor suppressor TP53 signaling. Tumors with this aneuploidy are sensitive to compounds activated by an enzyme encoded on chromosome 1q, suggesting a potential therapeutic approach. —Yevgeniya NusinovichINTRODUCTIONIt has been known for more than 100 years that human cancers exhibit pervasive aneuploidy, or chromosome copy number changes. For instance, about 25% of cancers exhibit gains of the q arm of chromosome 1. However, despite the prevalence of aneuploidy across cancer types, its role in tumorigenesis has remained poorly defined. Our ability to uncover the function of these large-scale copy number alterations has been hampered by our inability to experimentally manipulate chromosome dosage in cancer. Nonetheless, as aneuploidy is common across malignancies but rare in normal tissue, drugs that exhibit selective toxicity toward aneuploid cells could be useful anticancer agents.RATIONALEAlthough aneuploidies have resisted close analysis, previous research has led to the discovery of a phenomenon called “oncogene addiction.” An oncogene-addicted cancer is dependent on the expression of an individual oncogene for continued malignant growth, and loss or inhibition of that oncogene is sufficient to induce cancer regression. As specific aneuploidies such as the gain of chromosome 1q are frequent events in diverse cancer types, we hypothesized that certain aneuploidies could themselves represent oncogene-like cancer addictions. To test this hypothesis, we developed ReDACT (Restoring Disomy in Aneuploid cells using CRISPR Targeting), a set of chromosome engineering tools that allow us to eliminate individual aneuploid chromosomes from cancer genomes. Using ReDACT, we created and then characterized a panel of isogenic cells that have or lack common cancer aneuploidies.RESULTSWe found that eliminating the trisomy of chromosome 1q from cancer cell lines harboring this alteration almost completely abolished anchorage-independent growth and xenograft formation. Similarly, eliminating the 1q trisomy from a nonmalignant cell line blocked RAS-mediated transformation. Prolonged growth in vitro or in vivo after aneuploidy elimination in cancer cell lines led to karyotype evolution, and 1q-disomic cells were eventually outcompeted by cells that had recovered the 1q trisomy. In contrast, removing other trisomic chromosomes from cancer cells had variable effects on malignant growth, demonstrating that different aneuploidies have distinct phenotypic consequences for cancer development.An analysis of clinical sequencing data demonstrated that chromosome 1q gains arise early during tumorigenesis and are mutually exclusive with mutations in the tumor suppressor TP53, suggesting that 1q trisomies could represent a mutation-independent mechanism for blocking p53 signaling. Consistent with this, we demonstrated that ReDACT-mediated elimination of chromosome 1q trisomies increased the expression of p53 target genes in TP53 wild-type cell lines. We traced this suppression of p53 function to the triplication of MDM4, a p53 inhibitor encoded on chromosome 1q, and we found that deleting a single copy of MDM4 impaired the growth of 1q-trisomic cells, whereas moderate overexpression of MDM4 rescued the growth of 1q-disomic cells.Finally, we demonstrated that chromosome 1q gains result in the overexpression of UCK2, a nucleotide kinase encoded on chromosome 1q that is also required for the cytotoxicity of certain anticancer nucleotide analogs. We determined that several different 1q-trisomic cell lines displayed enhanced sensitivity to these compounds owing to the up-regulation of UCK2, revealing that 1q aneuploidy can also represent a tractable cancer vulnerability.CONCLUSIONCertain aneuploidies that are commonly found in tumor genomes play a central role in cancer development, and eliminating these aneuploidies compromises malignant growth potential. At the same time, aneuploidy causes collateral therapeutic vulnerabilities that can be targeted to selectively eliminate cells with chromosome dosage imbalances. The development of flexible chromosome engineering methodologies like ReDACT will enable additional experiments to further unravel the consequences of aneuploidy in development and disease. |
| Author | Lukow, Devon A. Lee, Sophia N. Lakhani, Asad A. Thompson, Sarah L. Li, Wenxue Smith, Joan C. Stevens, Eric C. Salovska, Barbora Sun, Ruping Kandikuppa, Pranav K. Schukken, Klaske M. Vasudevan, Anand Martienssen, Robert A. Scaduto, Christine M. Sausville, Erin L. Zou, Charles Brown, Leanne M. Mendelson, Brianna E. Girish, Vishruth Akalu, Saron M. Liu, Yansheng Hagenson, Ryan A. Yuan, Monet Lou Taylor, Alison M. Sheltzer, Jason M. |
| AuthorAffiliation | 1. Yale University School of Medicine, New Haven, CT 06511 5. Howard Hughes Medical Institute, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724 4. Columbia University School of Medicine, New York, NY 10032 2. Johns Hopkins University School of Medicine, Baltimore, MD 21205 3. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724 6. Department of Laboratory Medicine and Pathology, University of Minnesota, Minneapolis, MN 55455 |
| AuthorAffiliation_xml | – name: 6. Department of Laboratory Medicine and Pathology, University of Minnesota, Minneapolis, MN 55455 – name: 3. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724 – name: 5. Howard Hughes Medical Institute, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724 – name: 2. Johns Hopkins University School of Medicine, Baltimore, MD 21205 – name: 1. Yale University School of Medicine, New Haven, CT 06511 – name: 4. Columbia University School of Medicine, New York, NY 10032 |
| Author_xml | – sequence: 1 givenname: Vishruth orcidid: 0000-0002-3848-7374 surname: Girish fullname: Girish, Vishruth organization: Yale University School of Medicine, New Haven, CT 06511, USA., Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA – sequence: 2 givenname: Asad A. orcidid: 0000-0001-9663-6051 surname: Lakhani fullname: Lakhani, Asad A. organization: Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA – sequence: 3 givenname: Sarah L. orcidid: 0000-0002-9062-2027 surname: Thompson fullname: Thompson, Sarah L. organization: Yale University School of Medicine, New Haven, CT 06511, USA – sequence: 4 givenname: Christine M. surname: Scaduto fullname: Scaduto, Christine M. organization: Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA – sequence: 5 givenname: Leanne M. surname: Brown fullname: Brown, Leanne M. organization: Yale University School of Medicine, New Haven, CT 06511, USA – sequence: 6 givenname: Ryan A. orcidid: 0000-0001-9750-1925 surname: Hagenson fullname: Hagenson, Ryan A. organization: Yale University School of Medicine, New Haven, CT 06511, USA – sequence: 7 givenname: Erin L. orcidid: 0000-0002-4386-703X surname: Sausville fullname: Sausville, Erin L. organization: Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA – sequence: 8 givenname: Brianna E. orcidid: 0000-0002-1844-3198 surname: Mendelson fullname: Mendelson, Brianna E. organization: Yale University School of Medicine, New Haven, CT 06511, USA – sequence: 9 givenname: Pranav K. orcidid: 0009-0001-9069-2762 surname: Kandikuppa fullname: Kandikuppa, Pranav K. organization: Yale University School of Medicine, New Haven, CT 06511, USA – sequence: 10 givenname: Devon A. orcidid: 0000-0001-6642-8649 surname: Lukow fullname: Lukow, Devon A. organization: Yale University School of Medicine, New Haven, CT 06511, USA – sequence: 11 givenname: Monet Lou surname: Yuan fullname: Yuan, Monet Lou organization: Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA – sequence: 12 givenname: Eric C. orcidid: 0009-0008-6037-756X surname: Stevens fullname: Stevens, Eric C. organization: Yale University School of Medicine, New Haven, CT 06511, USA – sequence: 13 givenname: Sophia N. orcidid: 0009-0004-3517-1990 surname: Lee fullname: Lee, Sophia N. organization: Yale University School of Medicine, New Haven, CT 06511, USA – sequence: 14 givenname: Klaske M. surname: Schukken fullname: Schukken, Klaske M. organization: Yale University School of Medicine, New Haven, CT 06511, USA – sequence: 15 givenname: Saron M. orcidid: 0000-0003-1430-0461 surname: Akalu fullname: Akalu, Saron M. organization: Yale University School of Medicine, New Haven, CT 06511, USA – sequence: 16 givenname: Anand surname: Vasudevan fullname: Vasudevan, Anand organization: Yale University School of Medicine, New Haven, CT 06511, USA – sequence: 17 givenname: Charles surname: Zou fullname: Zou, Charles organization: Yale University School of Medicine, New Haven, CT 06511, USA – sequence: 18 givenname: Barbora orcidid: 0000-0002-7093-4576 surname: Salovska fullname: Salovska, Barbora organization: Yale University School of Medicine, New Haven, CT 06511, USA – sequence: 19 givenname: Wenxue orcidid: 0000-0002-8902-0184 surname: Li fullname: Li, Wenxue organization: Yale University School of Medicine, New Haven, CT 06511, USA – sequence: 20 givenname: Joan C. surname: Smith fullname: Smith, Joan C. organization: Yale University School of Medicine, New Haven, CT 06511, USA – sequence: 21 givenname: Alison M. orcidid: 0000-0001-9341-535X surname: Taylor fullname: Taylor, Alison M. organization: Columbia University School of Medicine, New York, NY 10032, USA – sequence: 22 givenname: Robert A. orcidid: 0000-0003-1285-9608 surname: Martienssen fullname: Martienssen, Robert A. organization: Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA., Howard Hughes Medical Institute, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA – sequence: 23 givenname: Yansheng orcidid: 0000-0002-2626-3912 surname: Liu fullname: Liu, Yansheng organization: Yale University School of Medicine, New Haven, CT 06511, USA – sequence: 24 givenname: Ruping orcidid: 0000-0003-3702-9483 surname: Sun fullname: Sun, Ruping organization: Department of Laboratory Medicine and Pathology, University of Minnesota, Minneapolis, MN 55455, USA – sequence: 25 givenname: Jason M. orcidid: 0000-0003-1381-1323 surname: Sheltzer fullname: Sheltzer, Jason M. organization: Yale University School of Medicine, New Haven, CT 06511, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/37410869$$D View this record in MEDLINE/PubMed |
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| DOI | 10.1126/science.adg4521 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Author Contributions. Conceptualization: V.G., A.A.L., C.M.S., J.M.S. Methodology: V.G., A.A.L., C.M.S., S.L.T., A.M.T., Y.L., J.M.S. Software: R.A.H., J.C.S., R.S. Formal analysis: R.A.H., J.C.S., R.S. Investigation: V.G., A.A.L., C.M.S., S.L.T., L.M.B., R.A.H., E.L.S., B.E.M., D.A.L., M.L.Y., P.K.K., E.C.S., S.N.L., K.M.S., S.A.M., A.V., C.Z., B.S., W.L. Resources: A.M.T. Data Curation: R.A.H., J.C.S. Writing – original draft: V.G., A.A.L., J.M.S. Writing – review and editing: V.G., A.A.L., J.M.S. Visualization: V.G., A.A.L., S.L.T., L.B., R.A.H., R.S., J.M.S. Supervision: Y.L., R.A.M., R.S., J.M.S. Funding acquisition: J.M.S. Equal contribution |
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| Snippet | Most cancers exhibit aneuploidy, but its functional significance in tumor development is controversial. Here, we describe ReDACT (Restoring Disomy in Aneuploid... Editor’s summaryAneuploidies, which are changes in the numbers of whole chromosomes or chromosome arms, are common in cancer, but their contributions to cancer... Most cancers exhibit aneuploidy, but its functional significance in tumor development is controversial. Here, we describe ReDACT ( Re storing D isomy in A... |
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| SubjectTerms | Addictions Aneuploidy Anticancer properties Antitumor agents Biocompatibility Cancer Carcinogenesis - genetics Cell Cycle Proteins - genetics Cell survival Chromosome 1 Chromosomes Copy number CRISPR Cytotoxicity Dosage Engineering Exhibits Gene Editing - methods Gene expression Genomes Humans In vivo methods and tests Karyotypes Kinases Malignancy Mutation Neoplasms - genetics Neoplasms - therapy Nucleotide analogs Nucleotides Oncogenes p53 Protein Proto-Oncogene Proteins - metabolism Sensitivity enhancement Substance Abuse Toxicity Trisomy Tumor cell lines Tumor suppressor genes Tumor Suppressor Protein p53 - genetics Tumorigenesis Tumors Xenotransplantation |
| Title | Oncogene-like addiction to aneuploidy in human cancers |
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