Transposon mutagenesis identifies cooperating genetic drivers during keratinocyte transformation and cutaneous squamous cell carcinoma progression

• Aziz Aiderus ,

  Contributed equally to this work with: Aziz Aiderus, Justin Y. Newberg, Liliana Guzman-Rojas

  Roles Formal analysis, Investigation, Methodology, Visualization, Writing – original draft, Writing – review & editing

  Affiliation Department of Molecular Oncology, Moffitt Cancer Center & Research Institute, Tampa, Florida, United States of America

  https://orcid.org/0000-0002-5920-1929

  ⨯
• Justin Y. Newberg ,

  Contributed equally to this work with: Aziz Aiderus, Justin Y. Newberg, Liliana Guzman-Rojas

  Roles Data curation, Formal analysis, Methodology, Software, Visualization

  Current address: Foundation Medicine, Inc., Cambridge, Massachusetts, USA (J.Y.N.); Houston Methodist Cancer Center, Houston Methodist Research Institute, Houston, Texas, USA (L.G.-R.); Department of Genetics and Development, Columbia University, New York, New York, USA (D.J.J.); Monoclonal Antibody Core Facility, University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA (F.A.-M); Department of Head & Neck Surgery, University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA (R.R.); Global VetPathology, Montgomery Village, Maryland, USA (J.M.W.); Science Centre Singapore, Republic of Singapore (S.-C.L.); Department of Biochemistry, Yong Loo Lin School of Medicine, National University Singapore, Republic of Singapore (K.H.-K.B.); Pacific Edge Limited, Dunedin, Otago, New Zealand (L.S.); AgResearch Invermay Agricultural Centre, Mosgiel, Otago, New Zealand (L.A.M.); and Genetics Department, University of Texas M.D. Anderson Cancer Center, Houston, Texas (N.G.C. and N.A.J.).

  Affiliations Department of Molecular Oncology, Moffitt Cancer Center & Research Institute, Tampa, Florida, United States of America, Cancer Research Program, Houston Methodist Research Institute, Houston, Texas, United States of America

  ⨯
• Liliana Guzman-Rojas ,

  Contributed equally to this work with: Aziz Aiderus, Justin Y. Newberg, Liliana Guzman-Rojas

  Roles Formal analysis, Investigation, Methodology

  Current address: Foundation Medicine, Inc., Cambridge, Massachusetts, USA (J.Y.N.); Houston Methodist Cancer Center, Houston Methodist Research Institute, Houston, Texas, USA (L.G.-R.); Department of Genetics and Development, Columbia University, New York, New York, USA (D.J.J.); Monoclonal Antibody Core Facility, University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA (F.A.-M); Department of Head & Neck Surgery, University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA (R.R.); Global VetPathology, Montgomery Village, Maryland, USA (J.M.W.); Science Centre Singapore, Republic of Singapore (S.-C.L.); Department of Biochemistry, Yong Loo Lin School of Medicine, National University Singapore, Republic of Singapore (K.H.-K.B.); Pacific Edge Limited, Dunedin, Otago, New Zealand (L.S.); AgResearch Invermay Agricultural Centre, Mosgiel, Otago, New Zealand (L.A.M.); and Genetics Department, University of Texas M.D. Anderson Cancer Center, Houston, Texas (N.G.C. and N.A.J.).

  Affiliation Cancer Research Program, Houston Methodist Research Institute, Houston, Texas, United States of America

  ⨯
• Ana M. Contreras-Sandoval,

  Roles Formal analysis, Investigation, Methodology

  Affiliation Department of Molecular Oncology, Moffitt Cancer Center & Research Institute, Tampa, Florida, United States of America

  https://orcid.org/0000-0002-4324-9610

  ⨯
• Amanda L. Meshey,

  Roles Formal analysis, Investigation, Methodology

  Affiliation Department of Molecular Oncology, Moffitt Cancer Center & Research Institute, Tampa, Florida, United States of America

  ⨯
• Devin J. Jones,

  Roles Formal analysis, Investigation, Methodology

  Current address: Foundation Medicine, Inc., Cambridge, Massachusetts, USA (J.Y.N.); Houston Methodist Cancer Center, Houston Methodist Research Institute, Houston, Texas, USA (L.G.-R.); Department of Genetics and Development, Columbia University, New York, New York, USA (D.J.J.); Monoclonal Antibody Core Facility, University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA (F.A.-M); Department of Head & Neck Surgery, University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA (R.R.); Global VetPathology, Montgomery Village, Maryland, USA (J.M.W.); Science Centre Singapore, Republic of Singapore (S.-C.L.); Department of Biochemistry, Yong Loo Lin School of Medicine, National University Singapore, Republic of Singapore (K.H.-K.B.); Pacific Edge Limited, Dunedin, Otago, New Zealand (L.S.); AgResearch Invermay Agricultural Centre, Mosgiel, Otago, New Zealand (L.A.M.); and Genetics Department, University of Texas M.D. Anderson Cancer Center, Houston, Texas (N.G.C. and N.A.J.).

  Affiliation Cancer Research Program, Houston Methodist Research Institute, Houston, Texas, United States of America

  https://orcid.org/0000-0003-4364-1273

  ⨯
• Felipe Amaya-Manzanares,

  Roles Investigation, Methodology

  Current address: Foundation Medicine, Inc., Cambridge, Massachusetts, USA (J.Y.N.); Houston Methodist Cancer Center, Houston Methodist Research Institute, Houston, Texas, USA (L.G.-R.); Department of Genetics and Development, Columbia University, New York, New York, USA (D.J.J.); Monoclonal Antibody Core Facility, University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA (F.A.-M); Department of Head & Neck Surgery, University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA (R.R.); Global VetPathology, Montgomery Village, Maryland, USA (J.M.W.); Science Centre Singapore, Republic of Singapore (S.-C.L.); Department of Biochemistry, Yong Loo Lin School of Medicine, National University Singapore, Republic of Singapore (K.H.-K.B.); Pacific Edge Limited, Dunedin, Otago, New Zealand (L.S.); AgResearch Invermay Agricultural Centre, Mosgiel, Otago, New Zealand (L.A.M.); and Genetics Department, University of Texas M.D. Anderson Cancer Center, Houston, Texas (N.G.C. and N.A.J.).

  Affiliation Cancer Research Program, Houston Methodist Research Institute, Houston, Texas, United States of America

  ⨯
• Roberto Rangel,

  Roles Resources

  Current address: Foundation Medicine, Inc., Cambridge, Massachusetts, USA (J.Y.N.); Houston Methodist Cancer Center, Houston Methodist Research Institute, Houston, Texas, USA (L.G.-R.); Department of Genetics and Development, Columbia University, New York, New York, USA (D.J.J.); Monoclonal Antibody Core Facility, University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA (F.A.-M); Department of Head & Neck Surgery, University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA (R.R.); Global VetPathology, Montgomery Village, Maryland, USA (J.M.W.); Science Centre Singapore, Republic of Singapore (S.-C.L.); Department of Biochemistry, Yong Loo Lin School of Medicine, National University Singapore, Republic of Singapore (K.H.-K.B.); Pacific Edge Limited, Dunedin, Otago, New Zealand (L.S.); AgResearch Invermay Agricultural Centre, Mosgiel, Otago, New Zealand (L.A.M.); and Genetics Department, University of Texas M.D. Anderson Cancer Center, Houston, Texas (N.G.C. and N.A.J.).

  Affiliation Cancer Research Program, Houston Methodist Research Institute, Houston, Texas, United States of America

  ⨯
• Jerrold M. Ward,

  Roles Formal analysis, Investigation, Methodology

  Current address: Foundation Medicine, Inc., Cambridge, Massachusetts, USA (J.Y.N.); Houston Methodist Cancer Center, Houston Methodist Research Institute, Houston, Texas, USA (L.G.-R.); Department of Genetics and Development, Columbia University, New York, New York, USA (D.J.J.); Monoclonal Antibody Core Facility, University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA (F.A.-M); Department of Head & Neck Surgery, University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA (R.R.); Global VetPathology, Montgomery Village, Maryland, USA (J.M.W.); Science Centre Singapore, Republic of Singapore (S.-C.L.); Department of Biochemistry, Yong Loo Lin School of Medicine, National University Singapore, Republic of Singapore (K.H.-K.B.); Pacific Edge Limited, Dunedin, Otago, New Zealand (L.S.); AgResearch Invermay Agricultural Centre, Mosgiel, Otago, New Zealand (L.A.M.); and Genetics Department, University of Texas M.D. Anderson Cancer Center, Houston, Texas (N.G.C. and N.A.J.).

  Affiliation Institute of Molecular and Cell Biology, Agency for Science, Technology and Research (A*STAR), Biopolis, Singapore, Republic of Singapore

  https://orcid.org/0000-0002-6350-8982

  ⨯
• Song-Choon Lee,

  Roles Resources

  Current address: Foundation Medicine, Inc., Cambridge, Massachusetts, USA (J.Y.N.); Houston Methodist Cancer Center, Houston Methodist Research Institute, Houston, Texas, USA (L.G.-R.); Department of Genetics and Development, Columbia University, New York, New York, USA (D.J.J.); Monoclonal Antibody Core Facility, University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA (F.A.-M); Department of Head & Neck Surgery, University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA (R.R.); Global VetPathology, Montgomery Village, Maryland, USA (J.M.W.); Science Centre Singapore, Republic of Singapore (S.-C.L.); Department of Biochemistry, Yong Loo Lin School of Medicine, National University Singapore, Republic of Singapore (K.H.-K.B.); Pacific Edge Limited, Dunedin, Otago, New Zealand (L.S.); AgResearch Invermay Agricultural Centre, Mosgiel, Otago, New Zealand (L.A.M.); and Genetics Department, University of Texas M.D. Anderson Cancer Center, Houston, Texas (N.G.C. and N.A.J.).

  Affiliation Institute of Molecular and Cell Biology, Agency for Science, Technology and Research (A*STAR), Biopolis, Singapore, Republic of Singapore

  ⨯
• Kenneth Hon-Kim Ban,

  Roles Resources

  Current address: Foundation Medicine, Inc., Cambridge, Massachusetts, USA (J.Y.N.); Houston Methodist Cancer Center, Houston Methodist Research Institute, Houston, Texas, USA (L.G.-R.); Department of Genetics and Development, Columbia University, New York, New York, USA (D.J.J.); Monoclonal Antibody Core Facility, University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA (F.A.-M); Department of Head & Neck Surgery, University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA (R.R.); Global VetPathology, Montgomery Village, Maryland, USA (J.M.W.); Science Centre Singapore, Republic of Singapore (S.-C.L.); Department of Biochemistry, Yong Loo Lin School of Medicine, National University Singapore, Republic of Singapore (K.H.-K.B.); Pacific Edge Limited, Dunedin, Otago, New Zealand (L.S.); AgResearch Invermay Agricultural Centre, Mosgiel, Otago, New Zealand (L.A.M.); and Genetics Department, University of Texas M.D. Anderson Cancer Center, Houston, Texas (N.G.C. and N.A.J.).

  Affiliation Institute of Molecular and Cell Biology, Agency for Science, Technology and Research (A*STAR), Biopolis, Singapore, Republic of Singapore

  https://orcid.org/0000-0001-7165-8713

  ⨯
• Keith Rogers,

  Roles Data curation, Investigation, Methodology, Resources

  Affiliation Institute of Molecular and Cell Biology, Agency for Science, Technology and Research (A*STAR), Biopolis, Singapore, Republic of Singapore

  ⨯
• Susan M. Rogers,

  Roles Data curation, Investigation, Methodology, Resources

  Affiliation Institute of Molecular and Cell Biology, Agency for Science, Technology and Research (A*STAR), Biopolis, Singapore, Republic of Singapore

  ⨯
• Luxmanan Selvanesan,

  Roles Investigation, Methodology, Resources

  Current address: Foundation Medicine, Inc., Cambridge, Massachusetts, USA (J.Y.N.); Houston Methodist Cancer Center, Houston Methodist Research Institute, Houston, Texas, USA (L.G.-R.); Department of Genetics and Development, Columbia University, New York, New York, USA (D.J.J.); Monoclonal Antibody Core Facility, University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA (F.A.-M); Department of Head & Neck Surgery, University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA (R.R.); Global VetPathology, Montgomery Village, Maryland, USA (J.M.W.); Science Centre Singapore, Republic of Singapore (S.-C.L.); Department of Biochemistry, Yong Loo Lin School of Medicine, National University Singapore, Republic of Singapore (K.H.-K.B.); Pacific Edge Limited, Dunedin, Otago, New Zealand (L.S.); AgResearch Invermay Agricultural Centre, Mosgiel, Otago, New Zealand (L.A.M.); and Genetics Department, University of Texas M.D. Anderson Cancer Center, Houston, Texas (N.G.C. and N.A.J.).

  Affiliation Centre for Translational Cancer Research, Department of Biochemistry, University of Otago, Dunedin, New Zealand

  https://orcid.org/0000-0001-8382-0722

  ⨯
• Leslie A. McNoe,

  Roles Investigation, Methodology, Resources

  Current address: Foundation Medicine, Inc., Cambridge, Massachusetts, USA (J.Y.N.); Houston Methodist Cancer Center, Houston Methodist Research Institute, Houston, Texas, USA (L.G.-R.); Department of Genetics and Development, Columbia University, New York, New York, USA (D.J.J.); Monoclonal Antibody Core Facility, University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA (F.A.-M); Department of Head & Neck Surgery, University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA (R.R.); Global VetPathology, Montgomery Village, Maryland, USA (J.M.W.); Science Centre Singapore, Republic of Singapore (S.-C.L.); Department of Biochemistry, Yong Loo Lin School of Medicine, National University Singapore, Republic of Singapore (K.H.-K.B.); Pacific Edge Limited, Dunedin, Otago, New Zealand (L.S.); AgResearch Invermay Agricultural Centre, Mosgiel, Otago, New Zealand (L.A.M.); and Genetics Department, University of Texas M.D. Anderson Cancer Center, Houston, Texas (N.G.C. and N.A.J.).

  Affiliation Centre for Translational Cancer Research, Department of Biochemistry, University of Otago, Dunedin, New Zealand

  ⨯
• Neal G. Copeland,

  Roles Conceptualization, Funding acquisition, Project administration, Resources, Supervision, Writing – review & editing

  Current address: Foundation Medicine, Inc., Cambridge, Massachusetts, USA (J.Y.N.); Houston Methodist Cancer Center, Houston Methodist Research Institute, Houston, Texas, USA (L.G.-R.); Department of Genetics and Development, Columbia University, New York, New York, USA (D.J.J.); Monoclonal Antibody Core Facility, University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA (F.A.-M); Department of Head & Neck Surgery, University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA (R.R.); Global VetPathology, Montgomery Village, Maryland, USA (J.M.W.); Science Centre Singapore, Republic of Singapore (S.-C.L.); Department of Biochemistry, Yong Loo Lin School of Medicine, National University Singapore, Republic of Singapore (K.H.-K.B.); Pacific Edge Limited, Dunedin, Otago, New Zealand (L.S.); AgResearch Invermay Agricultural Centre, Mosgiel, Otago, New Zealand (L.A.M.); and Genetics Department, University of Texas M.D. Anderson Cancer Center, Houston, Texas (N.G.C. and N.A.J.).

  Affiliations Cancer Research Program, Houston Methodist Research Institute, Houston, Texas, United States of America, Institute of Molecular and Cell Biology, Agency for Science, Technology and Research (A*STAR), Biopolis, Singapore, Republic of Singapore

  ⨯
• Nancy A. Jenkins,

  Roles Conceptualization, Funding acquisition, Project administration, Resources, Supervision

  Current address: Foundation Medicine, Inc., Cambridge, Massachusetts, USA (J.Y.N.); Houston Methodist Cancer Center, Houston Methodist Research Institute, Houston, Texas, USA (L.G.-R.); Department of Genetics and Development, Columbia University, New York, New York, USA (D.J.J.); Monoclonal Antibody Core Facility, University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA (F.A.-M); Department of Head & Neck Surgery, University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA (R.R.); Global VetPathology, Montgomery Village, Maryland, USA (J.M.W.); Science Centre Singapore, Republic of Singapore (S.-C.L.); Department of Biochemistry, Yong Loo Lin School of Medicine, National University Singapore, Republic of Singapore (K.H.-K.B.); Pacific Edge Limited, Dunedin, Otago, New Zealand (L.S.); AgResearch Invermay Agricultural Centre, Mosgiel, Otago, New Zealand (L.A.M.); and Genetics Department, University of Texas M.D. Anderson Cancer Center, Houston, Texas (N.G.C. and N.A.J.).

  Affiliations Cancer Research Program, Houston Methodist Research Institute, Houston, Texas, United States of America, Institute of Molecular and Cell Biology, Agency for Science, Technology and Research (A*STAR), Biopolis, Singapore, Republic of Singapore

  ⨯
• Kenneth Y. Tsai,

  Roles Funding acquisition, Resources, Supervision, Writing – review & editing

  Affiliations Departments of Anatomic Pathology & Tumor Biology, Moffitt Cancer Center & Research Institute, Tampa, Florida, United States of America, Donald A. Adam Melanoma and Skin Cancer Research Center of Excellence, Moffitt Cancer Center & Research Institute, Tampa, Florida, United States of America, Department of Oncologic Sciences, Morsani College of Medicine, University of South Florida, Tampa, Florida, United States of America

  https://orcid.org/0000-0001-5325-212X

  ⨯
• Michael A. Black,

  Roles Data curation, Formal analysis, Investigation, Methodology, Resources, Software, Visualization, Writing – review & editing

  Affiliation Centre for Translational Cancer Research, Department of Biochemistry, University of Otago, Dunedin, New Zealand

  https://orcid.org/0000-0003-1174-6054

  ⨯
• Karen M. Mann,

  Roles Conceptualization, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Writing – original draft, Writing – review & editing

  Affiliations Department of Molecular Oncology, Moffitt Cancer Center & Research Institute, Tampa, Florida, United States of America, Cancer Research Program, Houston Methodist Research Institute, Houston, Texas, United States of America, Institute of Molecular and Cell Biology, Agency for Science, Technology and Research (A*STAR), Biopolis, Singapore, Republic of Singapore, Department of Oncologic Sciences, Morsani College of Medicine, University of South Florida, Tampa, Florida, United States of America, Departments of Gastrointestinal Oncology & Malignant Hematology, Moffitt Cancer Center & Research Institute, Tampa, Florida, United States of America, Cancer Biology and Evolution Program, Moffitt Cancer Center & Research Institute, Tampa, Florida, United States of America

  https://orcid.org/0000-0002-7161-4523

  ⨯
•  [ ... ],
• Michael B. Mann

  Roles Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing – original draft, Writing – review & editing

  * E-mail: Michael.Mann@moffitt.org

  Affiliations Department of Molecular Oncology, Moffitt Cancer Center & Research Institute, Tampa, Florida, United States of America, Cancer Research Program, Houston Methodist Research Institute, Houston, Texas, United States of America, Institute of Molecular and Cell Biology, Agency for Science, Technology and Research (A*STAR), Biopolis, Singapore, Republic of Singapore, Donald A. Adam Melanoma and Skin Cancer Research Center of Excellence, Moffitt Cancer Center & Research Institute, Tampa, Florida, United States of America, Department of Oncologic Sciences, Morsani College of Medicine, University of South Florida, Tampa, Florida, United States of America, Cancer Biology and Evolution Program, Moffitt Cancer Center & Research Institute, Tampa, Florida, United States of America, Department of Cutaneous Oncology, Moffitt Cancer Center & Research Institute, Tampa, Florida, United States of America

  https://orcid.org/0000-0002-7515-6515

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