Multiomics in primary and metastatic breast tumors from the AURORA US network finds microenvironment and epigenetic drivers of metastasis

The AURORA US Metastasis Project was established with the goal to identify molecular features associated with metastasis. We assayed 55 females with metastatic breast cancer (51 primary cancers and 102 metastases) by RNA sequencing, tumor/germline DNA exome and low-pass whole-genome sequencing and g...

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Published in:	Nature cancer Vol. 4; no. 1; pp. 128 - 147
Main Authors:	Garcia-Recio, Susana, Hinoue, Toshinori, Wheeler, Gregory L, Kelly, Benjamin J, Garrido-Castro, Ana C, Pascual, Tomas, De Cubas, Aguirre A, Xia, Youli, Felsheim, Brooke M, McClure, Marni B, Rajkovic, Andrei, Karaesmen, Ezgi, Smith, Markia A, Fan, Cheng, Ericsson, Paula I Gonzalez, Sanders, Melinda E, Creighton, Chad J, Bowen, Jay, Leraas, Kristen, Burns, Robyn T, Coppens, Sara, Wheless, Amy, Rezk, Salma, Garrett, Amy L, Parker, Joel S, Foy, Kelly K, Shen, Hui, Park, Ben H, Krop, Ian, Anders, Carey, Gastier-Foster, Julie, Rimawi, Mothaffar F, Nanda, Rita, Lin, Nancy U, Isaacs, Claudine, Marcom, P Kelly, Storniolo, Anna Maria, Couch, Fergus J, Chandran, Uma, Davis, Michael, Silverstein, Jonathan, Ropelewski, Alexander, Liu, Minetta C, Hilsenbeck, Susan G, Norton, Larry, Richardson, Andrea L, Symmans, W Fraser, Wolff, Antonio C, Davidson, Nancy E, Carey, Lisa A, Lee, Adrian V, Balko, Justin M, Hoadley, Katherine A, Laird, Peter W, Mardis, Elaine R, King, Tari A, Perou, Charles M
Format:	Journal Article
Language:	English
Published:	England Nature Publishing Group US 01-01-2023
Subjects:	Animals Breast DNA Methylation - genetics Epigenesis, Genetic - genetics Female Humans Mammary Neoplasms, Animal - genetics Multiomics Resource Triple Negative Breast Neoplasms - genetics Tumor Microenvironment - genetics
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Abstract	The AURORA US Metastasis Project was established with the goal to identify molecular features associated with metastasis. We assayed 55 females with metastatic breast cancer (51 primary cancers and 102 metastases) by RNA sequencing, tumor/germline DNA exome and low-pass whole-genome sequencing and global DNA methylation microarrays. Expression subtype changes were observed in ~30% of samples and were coincident with DNA clonality shifts, especially involving HER2. Downregulation of estrogen receptor (ER)-mediated cell-cell adhesion genes through DNA methylation mechanisms was observed in metastases. Microenvironment differences varied according to tumor subtype; the ER /luminal subtype had lower fibroblast and endothelial content, while triple-negative breast cancer/basal metastases showed a decrease in B and T cells. In 17% of metastases, DNA hypermethylation and/or focal deletions were identified near HLA-A and were associated with reduced expression and lower immune cell infiltrates, especially in brain and liver metastases. These findings could have implications for treating individuals with metastatic breast cancer with immune- and HER2-targeting therapies.
AbstractList	The AURORA US Metastasis Project was established with the goal to identify molecular features associated with metastasis. We assayed 55 females with metastatic breast cancer (51 primary cancers and 102 metastases) by RNA sequencing, tumor/germline DNA exome and low-pass whole-genome sequencing and global DNA methylation microarrays. Expression subtype changes were observed in ~30% of samples and were coincident with DNA clonality shifts, especially involving HER2. Downregulation of estrogen receptor (ER)-mediated cell–cell adhesion genes through DNA methylation mechanisms was observed in metastases. Microenvironment differences varied according to tumor subtype; the ER + /luminal subtype had lower fibroblast and endothelial content, while triple-negative breast cancer/basal metastases showed a decrease in B and T cells. In 17% of metastases, DNA hypermethylation and/or focal deletions were identified near HLA-A and were associated with reduced expression and lower immune cell infiltrates, especially in brain and liver metastases. These findings could have implications for treating individuals with metastatic breast cancer with immune- and HER2-targeting therapies. The AURORA US Metastasis Project was established with the goal to identify molecular features associated with metastasis. We assayed 55 females with metastatic breast cancer (51 primary cancers and 102 metastases) by RNA sequencing, tumor/germline DNA exome and low-pass whole-genome sequencing and global DNA methylation microarrays. Expression subtype changes were observed in ~30% of samples and were coincident with DNA clonality shifts, especially involving HER2. Downregulation of estrogen receptor (ER)-mediated cell–cell adhesion genes through DNA methylation mechanisms was observed in metastases. Microenvironment differences varied according to tumor subtype; the ER + /luminal subtype had lower fibroblast and endothelial content, while triple-negative breast cancer/basal metastases showed a decrease in B and T cells. In 17% of metastases, DNA hypermethylation and/or focal deletions were identified near HLA-A and were associated with reduced expression and lower immune cell infiltrates, especially in brain and liver metastases. These findings could have implications for treating individuals with metastatic breast cancer with immune- and HER2-targeting therapies. Perou and colleagues perform genomic, transcriptomic and epigenetic analyses on pairs of primary and metastatic breast tumors, detecting subtype switching and changes in immune signatures and DNA methylation patterns associated with metastasis. The AURORA US Metastasis Project was established with the goal to identify molecular features associated with metastasis. We assayed 55 females with metastatic breast cancer (51 primary cancers and 102 metastases) by RNA sequencing, tumor/germline DNA exome and low-pass whole-genome sequencing and global DNA methylation microarrays. Expression subtype changes were observed in ~30% of samples and were coincident with DNA clonality shifts, especially involving HER2. Downregulation of estrogen receptor (ER)-mediated cell-cell adhesion genes through DNA methylation mechanisms was observed in metastases. Microenvironment differences varied according to tumor subtype; the ER /luminal subtype had lower fibroblast and endothelial content, while triple-negative breast cancer/basal metastases showed a decrease in B and T cells. In 17% of metastases, DNA hypermethylation and/or focal deletions were identified near HLA-A and were associated with reduced expression and lower immune cell infiltrates, especially in brain and liver metastases. These findings could have implications for treating individuals with metastatic breast cancer with immune- and HER2-targeting therapies. The AURORA US Metastasis Project was established with the goal to identify molecular features associated with metastasis. We assayed 55 females with metastatic breast cancer (51 primary cancers and 102 metastases) by RNA sequencing, tumor/germline DNA exome and low-pass whole-genome sequencing and global DNA methylation microarrays. Expression subtype changes were observed in ~30% of samples and were coincident with DNA clonality shifts, especially involving HER2. Downregulation of estrogen receptor (ER)-mediated cell-cell adhesion genes through DNA methylation mechanisms was observed in metastases. Microenvironment differences varied according to tumor subtype; the ER+/luminal subtype had lower fibroblast and endothelial content, while triple-negative breast cancer/basal metastases showed a decrease in B and T cells. In 17% of metastases, DNA hypermethylation and/or focal deletions were identified near HLA-A and were associated with reduced expression and lower immune cell infiltrates, especially in brain and liver metastases. These findings could have implications for treating individuals with metastatic breast cancer with immune- and HER2-targeting therapies.The AURORA US Metastasis Project was established with the goal to identify molecular features associated with metastasis. We assayed 55 females with metastatic breast cancer (51 primary cancers and 102 metastases) by RNA sequencing, tumor/germline DNA exome and low-pass whole-genome sequencing and global DNA methylation microarrays. Expression subtype changes were observed in ~30% of samples and were coincident with DNA clonality shifts, especially involving HER2. Downregulation of estrogen receptor (ER)-mediated cell-cell adhesion genes through DNA methylation mechanisms was observed in metastases. Microenvironment differences varied according to tumor subtype; the ER+/luminal subtype had lower fibroblast and endothelial content, while triple-negative breast cancer/basal metastases showed a decrease in B and T cells. In 17% of metastases, DNA hypermethylation and/or focal deletions were identified near HLA-A and were associated with reduced expression and lower immune cell infiltrates, especially in brain and liver metastases. These findings could have implications for treating individuals with metastatic breast cancer with immune- and HER2-targeting therapies.
Author	Wheeler, Gregory L Carey, Lisa A McClure, Marni B Couch, Fergus J Lin, Nancy U Parker, Joel S Garrett, Amy L Marcom, P Kelly Rimawi, Mothaffar F Storniolo, Anna Maria Felsheim, Brooke M Hoadley, Katherine A Karaesmen, Ezgi King, Tari A Fan, Cheng Davidson, Nancy E Rajkovic, Andrei Davis, Michael De Cubas, Aguirre A Creighton, Chad J Nanda, Rita Perou, Charles M Wheless, Amy Xia, Youli Chandran, Uma Kelly, Benjamin J Richardson, Andrea L Garrido-Castro, Ana C Hilsenbeck, Susan G Pascual, Tomas Lee, Adrian V Coppens, Sara Smith, Markia A Norton, Larry Ericsson, Paula I Gonzalez Leraas, Kristen Burns, Robyn T Foy, Kelly K Anders, Carey Symmans, W Fraser Mardis, Elaine R Bowen, Jay Ropelewski, Alexander Liu, Minetta C Garcia-Recio, Susana Krop, Ian Wolff, Antonio C Laird, Peter W Sanders, Melinda E Gastier-Foster, Julie Silverstein, Jonathan Isaacs, Claudine Hinoue, Toshinori Park, Ben H Rezk, Salma Shen, Hui Balko, Justin M
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Snippet	The AURORA US Metastasis Project was established with the goal to identify molecular features associated with metastasis. We assayed 55 females with metastatic...
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StartPage	128
SubjectTerms	Animals Breast DNA Methylation - genetics Epigenesis, Genetic - genetics Female Humans Mammary Neoplasms, Animal - genetics Multiomics Resource Triple Negative Breast Neoplasms - genetics Tumor Microenvironment - genetics
Title	Multiomics in primary and metastatic breast tumors from the AURORA US network finds microenvironment and epigenetic drivers of metastasis
URI	https://www.ncbi.nlm.nih.gov/pubmed/36585450 https://www.proquest.com/docview/2759962526 https://pubmed.ncbi.nlm.nih.gov/PMC9886551
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