Comparative Molecular Life History of Spontaneous Canine and Human Gliomas

Samirkumar B Amin; Kevin J Anderson; C Elizabeth Boudreau; Emmanuel Martinez-Ledesma; Emre Kocakavuk; Kevin C Johnson; Floris P Barthel; Frederick S Varn; Cynthia Kassab; Xiaoyang Ling; Hoon Kim; Mary Barter; Ching C Lau; Chew Yee Ngan; Margaret Chapman; Jennifer W Koehler; James P Long; Andrew D Miller; C Ryan Miller; Brian F Porter; Daniel R Rissi; Christina Mazcko; Amy K LeBlanc; Peter J Dickinson; Rebecca A Packer; Amanda R Taylor; John H Rossmeisl Jr; Kevin D Woolard; Amy B Heimberger; Jonathan M Levine; Roel G W Verhaak

doi:10.1016/j.ccell.2020.01.004

Comparative Molecular Life History of Spontaneous Canine and Human Gliomas

Cancer Cell. 2020 Feb 10;37(2):243-257.e7. doi: 10.1016/j.ccell.2020.01.004.

Authors

Samirkumar B Amin¹, Kevin J Anderson¹, C Elizabeth Boudreau², Emmanuel Martinez-Ledesma³, Emre Kocakavuk⁴, Kevin C Johnson¹, Floris P Barthel¹, Frederick S Varn¹, Cynthia Kassab⁵, Xiaoyang Ling⁵, Hoon Kim¹, Mary Barter⁶, Ching C Lau⁷, Chew Yee Ngan¹, Margaret Chapman¹, Jennifer W Koehler⁸, James P Long⁹, Andrew D Miller¹⁰, C Ryan Miller¹¹, Brian F Porter¹², Daniel R Rissi¹³, Christina Mazcko¹⁴, Amy K LeBlanc¹⁴, Peter J Dickinson¹⁵, Rebecca A Packer¹⁶, Amanda R Taylor¹⁷, John H Rossmeisl Jr¹⁸, Kevin D Woolard¹⁵, Amy B Heimberger⁵, Jonathan M Levine², Roel G W Verhaak¹⁹

Affiliations

¹ The Jackson Laboratory for Genomic Medicine, Farmington, CT 06032, USA.
² Department of Small Animal Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX 77843, USA.
³ Tecnologico de Monterrey, Escuela de Medicina y Ciencias de la Salud, Avenue Morones Prieto 3000, Monterrey, Nuevo Leon 64710, Mexico; Department of Neuro-Oncology, the University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
⁴ The Jackson Laboratory for Genomic Medicine, Farmington, CT 06032, USA; DKFZ Division of Translational Neurooncology at the West German Cancer Center (WTZ), German Cancer Consortium (DKTK) Partner Site & Department of Neurosurgery, University Hospital Essen, Essen, Germany.
⁵ Department of Neurosurgery, the University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
⁶ The Jackson Laboratory, Bar Harbor, ME 04609, USA.
⁷ The Jackson Laboratory for Genomic Medicine, Farmington, CT 06032, USA; Connecticut Children's Medical Center, Hartford, CT 06106, USA; University of Connecticut School of Medicine, Farmington, CT 06032, USA.
⁸ Department of Pathobiology, College of Veterinary Medicine, Auburn University, Auburn, AL, USA.
⁹ Department of Neurosurgery, the University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA; Department of Biostatistics, the University of Texas MD Anderson Cancer Center, Houston, TX, USA.
¹⁰ Department of Biomedical Sciences, Section of Anatomic Pathology, College of Veterinary Medicine, Cornell University, Ithaca, NY, USA.
¹¹ Departments of Pathology and Laboratory Medicine, Neurology, and Pharmacology, Lineberger Comprehensive Cancer Center and Neuroscience Center, University of North Carolina School of Medicine, Chapel Hill, NC, USA.
¹² Department of Veterinary Pathobiology, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX, USA.
¹³ Department of Pathology and Athens Veterinary Diagnostic Laboratory, College of Veterinary Medicine, University of Georgia, Athens, GA, USA.
¹⁴ Comparative Oncology Program, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.
¹⁵ Department of Surgical and Radiological Sciences, UC Davis School of Veterinary Medicine, Davis, CA, USA.
¹⁶ Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO, USA.
¹⁷ Auburn University College of Veterinary Medicine, Auburn, AL, USA.
¹⁸ VA-MD College of Veterinary Medicine, Blacksburg, VA, USA.
¹⁹ The Jackson Laboratory for Genomic Medicine, Farmington, CT 06032, USA. Electronic address: roel.verhaak@jax.org.

Abstract

Sporadic gliomas in companion dogs provide a window on the interaction between tumorigenic mechanisms and host environment. We compared the molecular profiles of canine gliomas with those of human pediatric and adult gliomas to characterize evolutionarily conserved mammalian mutational processes in gliomagenesis. Employing whole-genome, exome, transcriptome, and methylation sequencing of 83 canine gliomas, we found alterations shared between canine and human gliomas such as the receptor tyrosine kinases, TP53 and cell-cycle pathways, and IDH1 R132. Canine gliomas showed high similarity with human pediatric gliomas per robust aneuploidy, mutational rates, relative timing of mutations, and DNA-methylation patterns. Our cross-species comparative genomic analysis provides unique insights into glioma etiology and the chronology of glioma-causing somatic alterations.

Keywords: adult glioma; canine glioma; comparative genomics; comparative oncology; computational biology; life history; mutagenesis; pediatric glioma.

Publication types

Comparative Study
Research Support, N.I.H., Extramural
Research Support, N.I.H., Intramural
Research Support, Non-U.S. Gov't

MeSH terms

Animals
Brain Neoplasms / genetics*
DNA Methylation / genetics*
Dogs
Exome / genetics
Glioma / genetics*
Humans
Isocitrate Dehydrogenase / genetics
Mutation / genetics*
Tumor Suppressor Protein p53 / genetics

Substances

Tumor Suppressor Protein p53
Isocitrate Dehydrogenase

Abstract

Publication types

MeSH terms

Substances

Grants and funding