Haplotype-resolved germline and somatic alterations in renal medullary carcinomas.

Renal medullary carcinomas (RMCs) are rare kidney cancers that occur in adolescents and young adults of African ancestry. Although RMC is associated with the sickle cell trait and somatic loss of the tumor suppressor, SMARCB1, the ancestral origins of RMC remain unknown. Further, characterization of structural variants (SVs) involving SMARCB1 in RMC remains limited.

We used linked-read genome sequencing to reconstruct germline and somatic haplotypes in 15 unrelated patients with RMC registered on the Children's Oncology Group (COG) AREN03B2 study between 2006 and 2017 or from our prior study. We performed fine-mapping of the HBB locus and assessed the germline for cancer predisposition genes. Subsequently, we assessed the tumor samples for mutations outside of SMARCB1 and integrated RNA sequencing to interrogate the structural variants at the SMARCB1 locus.

We find that the haplotype of the sickle cell mutation in patients with RMC originated from three geographical regions in Africa. In addition, fine-mapping of the HBB locus identified the sickle cell mutation as the sole candidate variant. We further identify that the SMARCB1 structural variants are characterized by blunt or 1-bp homology events.

Our findings suggest that RMC does not arise from a single founder population and that the HbS allele is a strong candidate germline allele which confers risk for RMC. Furthermore, we find that the SVs that disrupt SMARCB1 function are likely repaired by non-homologous end-joining. These findings highlight how haplotype-based analyses using linked-read genome sequencing can be applied to identify potential risk variants in small and rare disease cohorts and provide nucleotide resolution to structural variants.

Genome medicine. 2021 Jul 14*** epublish ***

Kar-Tong Tan, Hyunji Kim, Jian Carrot-Zhang, Yuxiang Zhang, Won Jun Kim, Guillaume Kugener, Jeremiah A Wala, Thomas P Howard, Yueh-Yun Chi, Rameen Beroukhim, Heng Li, Gavin Ha, Seth L Alper, Elizabeth J Perlman, Elizabeth A Mullen, William C Hahn, Matthew Meyerson, Andrew L Hong

Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA, USA., Department of Genetics, Harvard Medical School, Boston, MA, USA., Broad Institute of MIT and Harvard, Cambridge, MA, USA., Department of Medicine, University of California San Francisco, San Francisco, CA, USA., Department of Pediatrics, University of Southern California, Los Angeles, CA, USA., Biostatistics and Computational Biology, Dana-Farber Cancer Institute, Boston, MA, USA., Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA., Department of Medicine, Beth Israel Deaconess Medical Center, Boston, MA, USA., Department of Pathology, Northwestern University, Chicago, IL, USA., Department of Hematology and Oncology, Boston Children's Hospital, Boston, MA, USA., Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA, USA. ., Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA, USA. ., Department of Pediatrics, Emory University, Atlanta, GA, USA. .