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1. Loss of Pip4k2c confers liver-metastatic organotropism through insulin-dependent PI3K-AKT pathway activation

Author

Rogava, Meri, Aprati, Tyler J., Chi, Wei-Yu, Melms, Johannes C., Hug, Clemens, Davis, Stephanie H., Earlie, Ethan M., Chung, Charlie, Deshmukh, Sachin K., Wu, Sharon, Sledge, George, Tang, Stephen, Ho, Patricia, Amin, Amit Dipak, Caprio, Lindsay, Gurjao, Carino, Tagore, Somnath, Ngo, Bryan, Lee, Michael J., Zanetti, Giorgia, Wang, Yiping, Chen, Sean, Ge, William, Melo, Luiza Martins Nascentes, Allies, Gabriele, Rösler, Jonas, Gibney, Goeffrey T., Schmitz, Oliver J., Sykes, Megan, Creusot, Rémi J., Tüting, Thomas, Schadendorf, Dirk, Röcken, Martin, Eigentler, Thomas K., Molotkov, Andrei, Mintz, Akiva, Bakhoum, Samuel F., Beyaz, Semir, Cantley, Lewis C., Sorger, Peter K., Meckelmann, Sven W., Tasdogan, Alpaslan, Liu, David, Laughney, Ashley M., and Izar, Benjamin

Published
2024
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2. Non-cell-autonomous cancer progression from chromosomal instability

Author

Li, Jun, Hubisz, Melissa J., Earlie, Ethan M., Duran, Mercedes A., Hong, Christy, Varela, Austin A., Lettera, Emanuele, Deyell, Matthew, Tavora, Bernardo, Havel, Jonathan J., Phyu, Su M., Amin, Amit Dipak, Budre, Karolina, Kamiya, Erina, Cavallo, Julie-Ann, Garris, Christopher, Powell, Simon, Reis-Filho, Jorge S., Wen, Hannah, Bettigole, Sarah, Khan, Atif J., Izar, Benjamin, Parkes, Eileen E., Laughney, Ashley M., and Bakhoum, Samuel F.

Published
2023
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3. Loss of polycomb repressive complex 1 activity and chromosomal instability drive uveal melanoma progression.

Author

Bakhoum, Mathieu F, Francis, Jasmine H, Agustinus, Albert, Earlie, Ethan M, Di Bona, Melody, Abramson, David H, Duran, Mercedes, Masilionis, Ignas, Molina, Elsa, Shoushtari, Alexander N, Goldbaum, Michael H, Mischel, Paul S, Bakhoum, Samuel F, and Laughney, Ashley M

Subjects
Human Genome, Biotechnology, Genetics, Cancer, 2.1 Biological and endogenous factors
Abstract

Chromosomal instability (CIN) and epigenetic alterations have been implicated in tumor progression and metastasis; yet how these two hallmarks of cancer are related remains poorly understood. By integrating genetic, epigenetic, and functional analyses at the single cell level, we show that progression of uveal melanoma (UM), the most common intraocular primary cancer in adults, is driven by loss of Polycomb Repressive Complex 1 (PRC1) in a subpopulation of tumor cells. This leads to transcriptional de-repression of PRC1-target genes and mitotic chromosome segregation errors. Ensuing CIN leads to the formation of rupture-prone micronuclei, exposing genomic double-stranded DNA (dsDNA) to the cytosol. This provokes tumor cell-intrinsic inflammatory signaling, mediated by aberrant activation of the cGAS-STING pathway. PRC1 inhibition promotes nuclear enlargement, induces a transcriptional response that is associated with significantly worse patient survival and clinical outcomes, and enhances migration that is rescued upon pharmacologic inhibition of CIN or STING. Thus, deregulation of PRC1 can promote tumor progression by inducing CIN and represents an opportunity for early therapeutic intervention.

Published
2021

6. Chromosomal instability drives metastasis through a cytosolic DNA response

Author

Bakhoum, Samuel F, Ngo, Bryan, Laughney, Ashley M, Cavallo, Julie-Ann, Murphy, Charles J, Ly, Peter, Shah, Pragya, Sriram, Roshan K, Watkins, Thomas BK, Taunk, Neil K, Duran, Mercedes, Pauli, Chantal, Shaw, Christine, Chadalavada, Kalyani, Rajasekhar, Vinagolu K, Genovese, Giulio, Venkatesan, Subramanian, Birkbak, Nicolai J, McGranahan, Nicholas, Lundquist, Mark, LaPlant, Quincey, Healey, John H, Elemento, Olivier, Chung, Christine H, Lee, Nancy Y, Imielenski, Marcin, Nanjangud, Gouri, Pe’er, Dana, Cleveland, Don W, Powell, Simon N, Lammerding, Jan, Swanton, Charles, and Cantley, Lewis C

Subjects
Genetics, HIV/AIDS, Aetiology, 2.1 Biological and endogenous factors, Cancer, Animals, Brain Neoplasms, Breast Neoplasms, Carcinoma, Squamous Cell, Cell Line, Chromosomal Instability, Chromosome Segregation, Cytosol, DNA, Neoplasm, Female, Head and Neck Neoplasms, Humans, Inflammation, Membrane Proteins, Mesoderm, Mice, Micronuclei, Chromosome-Defective, NF-kappa B, Neoplasm Metastasis, Nucleotidyltransferases, Xenograft Model Antitumor Assays, General Science & Technology
Abstract

Chromosomal instability is a hallmark of cancer that results from ongoing errors in chromosome segregation during mitosis. Although chromosomal instability is a major driver of tumour evolution, its role in metastasis has not been established. Here we show that chromosomal instability promotes metastasis by sustaining a tumour cell-autonomous response to cytosolic DNA. Errors in chromosome segregation create a preponderance of micronuclei whose rupture spills genomic DNA into the cytosol. This leads to the activation of the cGAS-STING (cyclic GMP-AMP synthase-stimulator of interferon genes) cytosolic DNA-sensing pathway and downstream noncanonical NF-κB signalling. Genetic suppression of chromosomal instability markedly delays metastasis even in highly aneuploid tumour models, whereas continuous chromosome segregation errors promote cellular invasion and metastasis in a STING-dependent manner. By subverting lethal epithelial responses to cytosolic DNA, chromosomally unstable tumour cells co-opt chronic activation of innate immune pathways to spread to distant organs.

Published
2018

7. The Human Tumor Atlas Network: Charting Tumor Transitions across Space and Time at Single-Cell Resolution

Author

Aberle, Denise, Achilefu, Samuel I., Ademuyiwa, Foluso O., Adey, Andrew C., Aft, Rebecca L., Agarwal, Rachana, Aguilar, Ruben A., Alikarami, Fatemeh, Allaj, Viola, Amos, Christopher, Anders, Robert A., Angelo, Michael R., Anton, Kristen, Ashenberg, Orr, Aster, Jon C., Babur, Ozgun, Bahmani, Amir, Balsubramani, Akshay, Barrett, David, Beane, Jennifer, Bender, Diane E., Bernt, Kathrin, Berry, Lynne, Betts, Courtney B., Bletz, Julie, Blise, Katie, Boire, Adrienne, Boland, Genevieve, Borowsky, Alexander, Bosse, Kristopher, Bott, Matthew, Boyden, Ed, Brooks, James, Bueno, Raphael, Burlingame, Erik A., Cai, Qiuyin, Campbell, Joshua, Caravan, Wagma, Cerami, Ethan, Chaib, Hassan, Chan, Joseph M., Chang, Young Hwan, Chatterjee, Deyali, Chaudhary, Ojasvi, Chen, Alyce A., Chen, Bob, Chen, Changya, Chen, Chia-hui, Chen, Feng, Chen, Yu-An, Chheda, Milan G., Chin, Koei, Chiu, Roxanne, Chu, Shih-Kai, Chuaqui, Rodrigo, Chun, Jaeyoung, Cisneros, Luis, Coffey, Robert J., Colditz, Graham A., Cole, Kristina, Collins, Natalie, Contrepois, Kevin, Coussens, Lisa M., Creason, Allison L., Crichton, Daniel, Curtis, Christina, Davidsen, Tanja, Davies, Sherri R., de Bruijn, Ino, Dellostritto, Laura, De Marzo, Angelo, Demir, Emek, DeNardo, David G., Diep, Dinh, Ding, Li, Diskin, Sharon, Doan, Xengie, Drewes, Julia, Dubinett, Stephen, Dyer, Michael, Egger, Jacklynn, Eng, Jennifer, Engelhardt, Barbara, Erwin, Graham, Esplin, Edward D., Esserman, Laura, Felmeister, Alex, Feiler, Heidi S., Fields, Ryan C., Fisher, Stephen, Flaherty, Keith, Flournoy, Jennifer, Ford, James M., Fortunato, Angelo, Frangieh, Allison, Frye, Jennifer L., Fulton, Robert S., Galipeau, Danielle, Gan, Siting, Gao, Jianjiong, Gao, Long, Gao, Peng, Gao, Vianne R., Geiger, Tim, George, Ajit, Getz, Gad, Ghosh, Sharmistha, Giannakis, Marios, Gibbs, David L., Gillanders, William E., Goecks, Jeremy, Goedegebuure, Simon P., Gould, Alanna, Gowers, Kate, Gray, Joe W., Greenleaf, William, Gresham, Jeremy, Guerriero, Jennifer L., Guha, Tuhin K., Guimaraes, Alexander R., Guinney, Justin, Gutman, David, Hacohen, Nir, Hanlon, Sean, Hansen, Casey R., Harismendy, Olivier, Harris, Kathleen A., Hata, Aaron, Hayashi, Akimasa, Heiser, Cody, Helvie, Karla, Herndon, John M., Hirst, Gilliam, Hodi, Frank, Hollmann, Travis, Horning, Aaron, Hsieh, James J., Hughes, Shannon, Huh, Won Jae, Hunger, Stephen, Hwang, Shelley E., Iacobuzio-Donahue, Christine A., Ijaz, Heba, Izar, Benjamin, Jacobson, Connor A., Janes, Samuel, Jané-Valbuena, Judit, Jayasinghe, Reyka G., Jiang, Lihua, Johnson, Brett E., Johnson, Bruce, Ju, Tao, Kadara, Humam, Kaestner, Klaus, Kagan, Jacob, Kalinke, Lukas, Keith, Robert, Khan, Aziz, Kibbe, Warren, Kim, Albert H., Kim, Erika, Kim, Junhyong, Kolodzie, Annette, Kopytra, Mateusz, Kotler, Eran, Krueger, Robert, Krysan, Kostyantyn, Kundaje, Anshul, Ladabaum, Uri, Lake, Blue B., Lam, Huy, Laquindanum, Rozelle, Lau, Ken S., Laughney, Ashley M., Lee, Hayan, Lenburg, Marc, Leonard, Carina, Leshchiner, Ignaty, Levy, Rochelle, Li, Jerry, Lian, Christine G., Lim, Kian-Huat, Lin, Jia-Ren, Lin, Yiyun, Liu, Qi, Liu, Ruiyang, Lively, Tracy, Longabaugh, William J.R., Longacre, Teri, Ma, Cynthia X., Macedonia, Mary Catherine, Madison, Tyler, Maher, Christopher A., Maitra, Anirban, Makinen, Netta, Makowski, Danika, Maley, Carlo, Maliga, Zoltan, Mallo, Diego, Maris, John, Markham, Nick, Marks, Jeffrey, Martinez, Daniel, Mashl, Robert J., Masilionais, Ignas, Mason, Jennifer, Massagué, Joan, Massion, Pierre, Mattar, Marissa, Mazurchuk, Richard, Mazutis, Linas, Mazzilli, Sarah A., McKinley, Eliot T., McMichael, Joshua F., Merrick, Daniel, Meyerson, Matthew, Miessner, Julia R., Mills, Gordon B., Mills, Meredith, Mondal, Suman B., Mori, Motomi, Mori, Yuriko, Moses, Elizabeth, Mosse, Yael, Muhlich, Jeremy L., Murphy, George F., Navin, Nicholas E., Nawy, Tal, Nederlof, Michel, Ness, Reid, Nevins, Stephanie, Nikolov, Milen, Nirmal, Ajit Johnson, Nolan, Garry, Novikov, Edward, Oberdoerffer, Philipp, O’Connell, Brendan, Offin, Michael, Oh, Stephen T., Olson, Anastasiya, Ooms, Alex, Ossandon, Miguel, Owzar, Kouros, Parmar, Swapnil, Patel, Tasleema, Patti, Gary J., Pe’er, Dana, Pe'er, Itsik, Peng, Tao, Persson, Daniel, Petty, Marvin, Pfister, Hanspeter, Polyak, Kornelia, Pourfarhangi, Kamyar, Puram, Sidharth V., Qiu, Qi, Quintanal-Villalonga, Álvaro, Raj, Arjun, Ramirez-Solano, Marisol, Rashid, Rumana, Reeb, Ashley N., Regev, Aviv, Reid, Mary, Resnick, Adam, Reynolds, Sheila M., Riesterer, Jessica L., Rodig, Scott, Roland, Joseph T., Rosenfield, Sonia, Rotem, Asaf, Roy, Sudipta, Rozenblatt-Rosen, Orit, Rudin, Charles M., Ryser, Marc D., Santagata, Sandro, Santi-Vicini, Maria, Sato, Kazuhito, Schapiro, Denis, Schrag, Deborah, Schultz, Nikolaus, Sears, Cynthia L., Sears, Rosalie C., Sen, Subrata, Sen, Triparna, Shalek, Alex, Sheng, Jeff, Sheng, Quanhu, Shoghi, Kooresh I., Shrubsole, Martha J., Shyr, Yu, Sibley, Alexander B., Siex, Kiara, Simmons, Alan J., Singer, Dinah S., Sivagnanam, Shamilene, Slyper, Michal, Snyder, Michael P., Sokolov, Artem, Song, Sheng-Kwei, Sorger, Peter K., Southard-Smith, Austin, Spira, Avrum, Srivastava, Sudhir, Stein, Janet, Storm, Phillip, Stover, Elizabeth, Strand, Siri H., Su, Timothy, Sudar, Damir, Sullivan, Ryan, Surrey, Lea, Suvà, Mario, Tan, Kai, Terekhanova, Nadezhda V., Ternes, Luke, Thammavong, Lisa, Thibault, Guillaume, Thomas, George V., Thorsson, Vésteinn, Todres, Ellen, Tran, Linh, Tyler, Madison, Uzun, Yasin, Vachani, Anil, Van Allen, Eliezer, Vandekar, Simon, Veis, Deborah J., Vigneau, Sébastien, Vossough, Arastoo, Waanders, Angela, Wagle, Nikhil, Wang, Liang-Bo, Wendl, Michael C., West, Robert, Williams, Elizabeth H., Wu, Chi-yun, Wu, Hao, Wu, Hung-Yi, Wyczalkowski, Matthew A., Xie, Yubin, Yang, Xiaolu, Yapp, Clarence, Yu, Wenbao, Yuan, Yinyin, Zhang, Dadong, Zhang, Kun, Zhang, Mianlei, Zhang, Nancy, Zhang, Yantian, Zhao, Yanyan, Zhou, Daniel Cui, Zhou, Zilu, Zhu, Houxiang, Zhu, Qin, Zhu, Xiangzhu, Zhu, Yuankun, Zhuang, Xiaowei, Hupalowska, Anna, Rood, Jennifer E., Hanlon, Sean E., Hughes, Shannon K., Hwang, E. Shelley, Johnson, Bruce E., Shalek, Alex K., Spira, Avrum E., and West, Robert B.

Published
2020
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9. Adult Human Glioblastomas Harbor Radial Glia-like Cells

Author

Wang, Rong, Sharma, Roshan, Shen, Xiaojuan, Laughney, Ashley M., Funato, Kosuke, Clark, Philip J., Shpokayte, Monika, Morgenstern, Peter, Navare, Monalisa, Xu, Yichi, Harbi, Shaghayegh, Masilionis, Ignas, Nanjangud, Gouri, Yang, Yanhong, Duran-Rehbein, Gabriel, Hemberg, Martin, Pe'er, Dana, and Tabar, Viviane

Published
2020
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10. Numerical chromosomal instability mediates susceptibility to radiation treatment

Author

Bakhoum, Samuel F, Kabeche, Lilian, Wood, Matthew D, Laucius, Christopher D, Qu, Dian, Laughney, Ashley M, Reynolds, Gloria E, Louie, Raymond J, Phillips, Joanna, Chan, Denise A, Zaki, Bassem I, Murnane, John P, Petritsch, Claudia, and Compton, Duane A

Subjects
Biochemistry and Cell Biology, Biomedical and Clinical Sciences, Oncology and Carcinogenesis, Biological Sciences, Radiation Oncology, Human Genome, Cancer, Genetics, 2.1 Biological and endogenous factors, Aneuploidy, Animals, Brain Neoplasms, Cell Cycle, Cell Death, Cell Line, Tumor, Cell Survival, Chromosomal Instability, Chromosome Breakage, Chromosome Segregation, Glioblastoma, HCT116 Cells, Humans, Male, Mice, Mice, Nude, Micronucleus Tests, Mitosis, Neoplasm Transplantation, Neoplasms, Radiation, Ionizing
Abstract

The exquisite sensitivity of mitotic cancer cells to ionizing radiation (IR) underlies an important rationale for the widely used fractionated radiation therapy. However, the mechanism for this cell cycle-dependent vulnerability is unknown. Here we show that treatment with IR leads to mitotic chromosome segregation errors in vivo and long-lasting aneuploidy in tumour-derived cell lines. These mitotic errors generate an abundance of micronuclei that predispose chromosomes to subsequent catastrophic pulverization thereby independently amplifying radiation-induced genome damage. Experimentally suppressing whole-chromosome missegregation reduces downstream chromosomal defects and significantly increases the viability of irradiated mitotic cells. Further, orthotopically transplanted human glioblastoma tumours in which chromosome missegregation rates have been reduced are rendered markedly more resistant to IR, exhibiting diminished markers of cell death in response to treatment. This work identifies a novel mitotic pathway for radiation-induced genome damage, which occurs outside of the primary nucleus and augments chromosomal breaks. This relationship between radiation treatment and whole-chromosome missegregation can be exploited to modulate therapeutic response in a clinically relevant manner.

Published
2015

11. Regenerative lineages and immune-mediated pruning in lung cancer metastasis

Author

Laughney, Ashley M., Hu, Jing, Campbell, Nathaniel R., Bakhoum, Samuel F., Setty, Manu, Lavallée, Vincent-Philippe, and Xie, Yubin

Subjects
Care and treatment, Complications and side effects, Genetic aspects, Patient outcomes, Health aspects, Lung cancer -- Genetic aspects -- Complications and side effects -- Care and treatment, Regenerative medicine -- Patient outcomes, Cancer metastasis -- Genetic aspects, Gene expression -- Health aspects, Metastasis -- Genetic aspects
Abstract

Author(s): Ashley M. Laughney [sup.1] [sup.2] [sup.3] [sup.4] [sup.5] , Jing Hu [sup.1] , Nathaniel R. Campbell [sup.1] [sup.2] [sup.6] , Samuel F. Bakhoum [sup.7] [sup.8] , Manu Setty [sup.2] [...], Developmental processes underlying normal tissue regeneration have been implicated in cancer, but the degree of their enactment during tumor progression and under the selective pressures of immune surveillance, remain unknown. Here we show that human primary lung adenocarcinomas are characterized by the emergence of regenerative cell types, typically seen in response to lung injury, and by striking infidelity among transcription factors specifying most alveolar and bronchial epithelial lineages. In contrast, metastases are enriched for key endoderm and lung-specifying transcription factors, SOX2 and SOX9, and recapitulate more primitive transcriptional programs spanning stem-like to regenerative pulmonary epithelial progenitor states. This developmental continuum mirrors the progressive stages of spontaneous outbreak from metastatic dormancy in a mouse model and exhibits SOX9-dependent resistance to natural killer cells. Loss of developmental stage-specific constraint in macrometastases triggered by natural killer cell depletion suggests a dynamic interplay between developmental plasticity and immune-mediated pruning during metastasis. Single-cell analysis of lung cancer progression uncovers developmental and regenerative programs co-opted by cancer cells and immune-mediated pruning during metastatic outbreak

Published
2020
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12. L1CAM defines the regenerative origin of metastasis-initiating cells in colorectal cancer

Author

Ganesh, Karuna, Basnet, Harihar, Kaygusuz, Yasemin, Laughney, Ashley M., He, Lan, Sharma, Roshan, O’Rourke, Kevin P., Reuter, Vincent P., Huang, Yun-Han, Turkekul, Mesruh, Er, Ekrem Emrah, Masilionis, Ignas, Manova-Todorova, Katia, Weiser, Martin R., Saltz, Leonard B., Garcia-Aguilar, Julio, Koche, Richard, Lowe, Scott W., Pe’er, Dana, Shia, Jinru, and Massagué, Joan

Published
2020
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13. Spectral discrimination of breast pathologies in situ using spatial frequency domain imaging

Author

Laughney, Ashley M, Krishnaswamy, Venkataramanan, Rizzo, Elizabeth J, Schwab, Mary C, Barth, Richard J, Cuccia, David J, Tromberg, Bruce J, Paulsen, Keith D, Pogue, Brian W, and Wells, Wendy A

Abstract

Abstract Introduction Nationally, 25% to 50% of patients undergoing lumpectomy for local management of breast cancer require a secondary excision because of the persistence of residual tumor. Intraoperative assessment of specimen margins by frozen-section analysis is not widely adopted in breast-conserving surgery. Here, a new approach to wide-field optical imaging of breast pathology in situ was tested to determine whether the system could accurately discriminate cancer from benign tissues before routine pathological processing. Methods Spatial frequency domain imaging (SFDI) was used to quantify near-infrared (NIR) optical parameters at the surface of 47 lumpectomy tissue specimens. Spatial frequency and wavelength-dependent reflectance spectra were parameterized with matched simulations of light transport. Spectral images were co-registered to histopathology in adjacent, stained sections of the tissue, cut in the geometry imaged in situ. A supervised classifier and feature-selection algorithm were implemented to automate discrimination of breast pathologies and to rank the contribution of each parameter to a diagnosis. Results Spectral parameters distinguished all pathology subtypes with 82% accuracy and benign (fibrocystic disease, fibroadenoma) from malignant (DCIS, invasive cancer, and partially treated invasive cancer after neoadjuvant chemotherapy) pathologies with 88% accuracy, high specificity (93%), and reasonable sensitivity (79%). Although spectral absorption and scattering features were essential components of the discriminant classifier, scattering exhibited lower variance and contributed most to tissue-type separation. The scattering slope was sensitive to stromal and epithelial distributions measured with quantitative immunohistochemistry. Conclusions SFDI is a new quantitative imaging technique that renders a specific tissue-type diagnosis. Its combination of planar sampling and frequency-dependent depth sensing is clinically pragmatic and appropriate for breast surgical-margin assessment. This study is the first to apply SFDI to pathology discrimination in surgical breast tissues. It represents an important step toward imaging surgical specimens immediately ex vivo to reduce the high rate of secondary excisions associated with breast lumpectomy procedures.

Published
2013

14. System analysis of spatial frequency domain imaging for quantitative mapping of surgically resected breast tissues

Author

Laughney, Ashley M, Krishnaswamy, Venkataramanan, Rice, Tyler B, Cuccia, David J, Barth, Richard J, Tromberg, Bruce J, Paulsen, Keith D, Pogue, Brian W, and Wells, Wendy A

Subjects
Medical and Biological Physics, Biomedical and Clinical Sciences, Physical Sciences, Breast Cancer, Women's Health, Clinical Research, Biomedical Imaging, Cancer, Bioengineering, Animals, Breast, Breast Neoplasms, Computer Simulation, Female, Humans, Image Processing, Computer-Assisted, Mastectomy, Segmental, Models, Biological, Monte Carlo Method, Phantoms, Imaging, Scattering, Radiation, Spectroscopy, Near-Infrared, Swine, spatial frequency domain imaging, modulated imaging, near-infrared spectroscopy, tissue scattering, pathology discrimination, breast conserving surgery, margin assessment, Optical Physics, Biomedical Engineering, Opthalmology and Optometry, Optics, Ophthalmology and optometry, Biomedical engineering, Atomic, molecular and optical physics
Abstract

The feasibility of spatial frequency domain imaging (SFDI) for breast surgical margin assessment was evaluated in tissue-simulating phantoms and in fully intact lumpectomy specimens at the time of surgery. Phantom data was evaluated according to contrast-detail resolution, quantitative accuracy and model-data goodness of fit, where optical parameters were estimated by minimizing the residual sum of squares between the measured modulation amplitude and its solutions, modeled according to diffusion and scaled-Monte Carlo simulations. In contrast-detail phantoms, a 1.25-mm-diameter surface inclusion was detectable for scattering contrast >28%; a fraction of this scattering contrast (7%) was detectable for a 10 mm surface inclusion and at least 33% scattering contrast was detected up to 1.5 mm below the phantom surface, a probing depth relevant to breast surgical margin assessment. Recovered hemoglobin concentrations were insensitive to changes in scattering, except for overestimation at visible wavelengths for total hemoglobin concentrations

Published
2013

15. Spectral discrimination of breast pathologies in situusing spatial frequency domain imaging

Author

Laughney, Ashley M, Krishnaswamy, Venkataramanan, Rizzo, Elizabeth J, Schwab, Mary C, Barth, Richard J, Cuccia, David J, Tromberg, Bruce J, Paulsen, Keith D, Pogue, Brian W, and Wells, Wendy A

Subjects
Biomedical and Clinical Sciences, Oncology and Carcinogenesis, Clinical Research, Women's Health, Bioengineering, Cancer, Biomedical Imaging, Breast Cancer, 4.2 Evaluation of markers and technologies, Adult, Aged, Aged, 80 and over, Biomarkers, Tumor, Biopsy, Breast Neoplasms, Carcinoma in Situ, Female, Humans, Immunohistochemistry, Mastectomy, Segmental, Middle Aged, Neoplasm Grading, Prognosis, Reproducibility of Results, Sensitivity and Specificity, Spectroscopy, Near-Infrared, Tumor Burden, BCS/BCT, Breast-conserving surgery/therapy, Near-infrared spectroscopy, Spatial frequency domain imaging, Diagnostic pathology, Oncology & Carcinogenesis, Oncology and carcinogenesis
Abstract

IntroductionNationally, 25% to 50% of patients undergoing lumpectomy for local management of breast cancer require a secondary excision because of the persistence of residual tumor. Intraoperative assessment of specimen margins by frozen-section analysis is not widely adopted in breast-conserving surgery. Here, a new approach to wide-field optical imaging of breast pathology in situ was tested to determine whether the system could accurately discriminate cancer from benign tissues before routine pathological processing.MethodsSpatial frequency domain imaging (SFDI) was used to quantify near-infrared (NIR) optical parameters at the surface of 47 lumpectomy tissue specimens. Spatial frequency and wavelength-dependent reflectance spectra were parameterized with matched simulations of light transport. Spectral images were co-registered to histopathology in adjacent, stained sections of the tissue, cut in the geometry imaged in situ. A supervised classifier and feature-selection algorithm were implemented to automate discrimination of breast pathologies and to rank the contribution of each parameter to a diagnosis.ResultsSpectral parameters distinguished all pathology subtypes with 82% accuracy and benign (fibrocystic disease, fibroadenoma) from malignant (DCIS, invasive cancer, and partially treated invasive cancer after neoadjuvant chemotherapy) pathologies with 88% accuracy, high specificity (93%), and reasonable sensitivity (79%). Although spectral absorption and scattering features were essential components of the discriminant classifier, scattering exhibited lower variance and contributed most to tissue-type separation. The scattering slope was sensitive to stromal and epithelial distributions measured with quantitative immunohistochemistry.ConclusionsSFDI is a new quantitative imaging technique that renders a specific tissue-type diagnosis. Its combination of planar sampling and frequency-dependent depth sensing is clinically pragmatic and appropriate for breast surgical-margin assessment. This study is the first to apply SFDI to pathology discrimination in surgical breast tissues. It represents an important step toward imaging surgical specimens immediately ex vivo to reduce the high rate of secondary excisions associated with breast lumpectomy procedures.

Published
2013

17. Modeling collective cell behavior in cancer: Perspectives from an interdisciplinary conversation

Author

Adler, Frederick R., primary, Anderson, Alexander R.A., additional, Bhushan, Abhinav, additional, Bogdan, Paul, additional, Bravo-Cordero, Jose Javier, additional, Brock, Amy, additional, Chen, Yun, additional, Cukierman, Edna, additional, DelGiorno, Kathleen E., additional, Denis, Gerald V., additional, Ferrall-Fairbanks, Meghan C., additional, Gartner, Zev Jordan, additional, Germain, Ronald N., additional, Gordon, Deborah M., additional, Hunter, Ginger, additional, Jolly, Mohit Kumar, additional, Karacosta, Loukia Georgiou, additional, Mythreye, Karthikeyan, additional, Katira, Parag, additional, Kulkarni, Rajan P., additional, Kutys, Matthew L., additional, Lander, Arthur D., additional, Laughney, Ashley M., additional, Levine, Herbert, additional, Lou, Emil, additional, Lowenstein, Pedro R., additional, Masters, Kristyn S., additional, Pe’er, Dana, additional, Peyton, Shelly R., additional, Platt, Manu O., additional, Purvis, Jeremy E., additional, Quon, Gerald, additional, Richer, Jennifer K., additional, Riddle, Nicole C., additional, Rodriguez, Analiz, additional, Snyder, Joshua C., additional, Lee Szeto, Gregory, additional, Tomlin, Claire J., additional, Yanai, Itai, additional, Zervantonakis, Ioannis K., additional, and Dueck, Hannah, additional

Published
2023
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22. Author Correction: L1CAM defines the regenerative origin of metastasis-initiating cells in colorectal cancer

Author

Ganesh, Karuna, Basnet, Harihar, Kaygusuz, Yasemin, Laughney, Ashley M., He, Lan, Sharma, Roshan, O’Rourke, Kevin P., Reuter, Vincent P., Huang, Yun-Han, Turkekul, Mesruh, Er, Ekrem Emrah, Masilionis, Ignas, Manova-Todorova, Katia, Weiser, Martin R., Saltz, Leonard B., Garcia-Aguilar, Julio, Koche, Richard, Lowe, Scott W., Pe’er, Dana, Shia, Jinru, and Massagué, Joan

Published
2020
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23. Obesity promotes breast epithelium DNA damage in women carrying a germline mutation in BRCA1 or BRCA2

Author

Bhardwaj, Priya, primary, Iyengar, Neil M., additional, Zahid, Heba, additional, Carter, Katharine M., additional, Byun, Dong Jun, additional, Choi, Man Ho, additional, Sun, Qi, additional, Savenkov, Oleksandr, additional, Louka, Charalambia, additional, Liu, Catherine, additional, Piloco, Phoebe, additional, Acosta, Monica, additional, Bareja, Rohan, additional, Elemento, Olivier, additional, Foronda, Miguel, additional, Dow, Lukas E., additional, Oshchepkova, Sofya, additional, Giri, Dilip D., additional, Pollak, Michael, additional, Zhou, Xi Kathy, additional, Hopkins, Benjamin D., additional, Laughney, Ashley M., additional, Frey, Melissa K., additional, Ellenson, Lora Hedrick, additional, Morrow, Monica, additional, Spector, Jason A., additional, Cantley, Lewis C., additional, and Brown, Kristy A., additional

Published
2023
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24. Obesity promotes breast epithelium DNA damage in BRCA mutation carriers

Author

Bhardwaj, Priya, primary, Iyengar, Neil M., additional, Zahid, Heba, additional, Carter, Katharine M., additional, Byun, Dong Jun, additional, Choi, Man Ho, additional, Sun, Qi, additional, Savenkov, Oleksandr, additional, Louka, Charalambia, additional, Liu, Catherine, additional, Piloco, Phoebe, additional, Acosta, Monica, additional, Bareja, Rohan, additional, Elemento, Olivier, additional, Foronda, Miguel, additional, Dow, Lukas E., additional, Oshchepkova, Sofya, additional, Giri, Dilip D., additional, Pollak, Michael, additional, Zhou, Xi Kathy, additional, Hopkins, Benjamin D., additional, Laughney, Ashley M., additional, Frey, Melissa K., additional, Ellenson, Lora Hedrick, additional, Morrow, Monica, additional, Spector, Jason A., additional, Cantley, Lewis C., additional, and Brown, Kristy A., additional

Published
2022
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25. Measurement of pressure-displacement kinetics of hemoglobin in normal breast tissue with near-infrared spectral imaging

Author

Jiang, Shudong, Pogue, Brian W., Laughney, Ashley M., Kogel, Christine A., and Paulsen, Keith D.

Subjects
Hemoglobin -- Properties, Breast -- Properties, Tissues -- Properties, Imaging systems -- Methods, Infrared radiation -- Research, Breast cancer -- Research, Astronomy, Physics
Abstract

Applying localized external displacement to the breast surface can change the interstitial fluid pressure such that regional transient microvascular changes occur in oxygenation and vascular volume. Imaging these dynamic responses over time, while different pressures are applied, could provide selective temporal contrast for cancer relative to the surrounding normal breast. In order to investigate this possibility in normal breast tissue, a near-infrared spectral tomography system was developed that can simultaneously acquire data at three wavelengths with a 15 s time resolution per scan. The system was tested first with heterogeneous blood phantoms. Changes in regional blood concentrations were found to be linearly related to recovered mean hemoglobin concentration ([Hb.sub.T]) values ([R.sup.2] = 0.9). In a series of volunteer breast imaging exams, data from 17 asymptomatic subjects were acquired under increasing and decreasing breast compression. Calculations show that a 10 mm displacement applied to the breast results in surface pressures in the range of 0-55 kPa depending on breast density. The recovered human data indicate that [Hb.sub.T] was reduced under compression and the normalized change was significantly correlated to the applied pressure with a p value of 0.005. The maximum [Hb.sub.T] decreases in breast tissue were associated with body mass index (BMI), which is a surrogate indicator of breast density. No statistically valid correlations were found between the applied pressure and the changes in tissue oxygen saturation ([S.sub.t][O.sub.2]) or water percentage ([H.sub.2]O) across the range of BMI values studied. OCIS codes: 110.0110, 170.0170, 120.0120.

Published
2009

26. High resolution mouse subventricular zone stem cell niche transcriptome reveals features of lineage, anatomy, and aging

Author

Xie, Xuanhua P., primary, Laks, Dan R., additional, Sun, Daochun, additional, Poran, Asaf, additional, Laughney, Ashley M., additional, Wang, Zilai, additional, Sam, Jessica, additional, Belenguer, German, additional, Fariñas, Isabel, additional, Elemento, Olivier, additional, Zhou, Xiuping, additional, and Parada, Luis F., additional

Published
2020
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27. The Human Tumor Atlas Network: Charting Tumor Transitions across Space and Time at Single-Cell Resolution

Author

Rozenblatt-Rosen, Orit, primary, Regev, Aviv, additional, Oberdoerffer, Philipp, additional, Nawy, Tal, additional, Hupalowska, Anna, additional, Rood, Jennifer E., additional, Ashenberg, Orr, additional, Cerami, Ethan, additional, Coffey, Robert J., additional, Demir, Emek, additional, Ding, Li, additional, Esplin, Edward D., additional, Ford, James M., additional, Goecks, Jeremy, additional, Ghosh, Sharmistha, additional, Gray, Joe W., additional, Guinney, Justin, additional, Hanlon, Sean E., additional, Hughes, Shannon K., additional, Hwang, E. Shelley, additional, Iacobuzio-Donahue, Christine A., additional, Jané-Valbuena, Judit, additional, Johnson, Bruce E., additional, Lau, Ken S., additional, Lively, Tracy, additional, Mazzilli, Sarah A., additional, Pe’er, Dana, additional, Santagata, Sandro, additional, Shalek, Alex K., additional, Schapiro, Denis, additional, Snyder, Michael P., additional, Sorger, Peter K., additional, Spira, Avrum E., additional, Srivastava, Sudhir, additional, Tan, Kai, additional, West, Robert B., additional, Williams, Elizabeth H., additional, Aberle, Denise, additional, Achilefu, Samuel I., additional, Ademuyiwa, Foluso O., additional, Adey, Andrew C., additional, Aft, Rebecca L., additional, Agarwal, Rachana, additional, Aguilar, Ruben A., additional, Alikarami, Fatemeh, additional, Allaj, Viola, additional, Amos, Christopher, additional, Anders, Robert A., additional, Angelo, Michael R., additional, Anton, Kristen, additional, Aster, Jon C., additional, Babur, Ozgun, additional, Bahmani, Amir, additional, Balsubramani, Akshay, additional, Barrett, David, additional, Beane, Jennifer, additional, Bender, Diane E., additional, Bernt, Kathrin, additional, Berry, Lynne, additional, Betts, Courtney B., additional, Bletz, Julie, additional, Blise, Katie, additional, Boire, Adrienne, additional, Boland, Genevieve, additional, Borowsky, Alexander, additional, Bosse, Kristopher, additional, Bott, Matthew, additional, Boyden, Ed, additional, Brooks, James, additional, Bueno, Raphael, additional, Burlingame, Erik A., additional, Cai, Qiuyin, additional, Campbell, Joshua, additional, Caravan, Wagma, additional, Chaib, Hassan, additional, Chan, Joseph M., additional, Chang, Young Hwan, additional, Chatterjee, Deyali, additional, Chaudhary, Ojasvi, additional, Chen, Alyce A., additional, Chen, Bob, additional, Chen, Changya, additional, Chen, Chia-hui, additional, Chen, Feng, additional, Chen, Yu-An, additional, Chheda, Milan G., additional, Chin, Koei, additional, Chiu, Roxanne, additional, Chu, Shih-Kai, additional, Chuaqui, Rodrigo, additional, Chun, Jaeyoung, additional, Cisneros, Luis, additional, Colditz, Graham A., additional, Cole, Kristina, additional, Collins, Natalie, additional, Contrepois, Kevin, additional, Coussens, Lisa M., additional, Creason, Allison L., additional, Crichton, Daniel, additional, Curtis, Christina, additional, Davidsen, Tanja, additional, Davies, Sherri R., additional, de Bruijn, Ino, additional, Dellostritto, Laura, additional, De Marzo, Angelo, additional, DeNardo, David G., additional, Diep, Dinh, additional, Diskin, Sharon, additional, Doan, Xengie, additional, Drewes, Julia, additional, Dubinett, Stephen, additional, Dyer, Michael, additional, Egger, Jacklynn, additional, Eng, Jennifer, additional, Engelhardt, Barbara, additional, Erwin, Graham, additional, Esserman, Laura, additional, Felmeister, Alex, additional, Feiler, Heidi S., additional, Fields, Ryan C., additional, Fisher, Stephen, additional, Flaherty, Keith, additional, Flournoy, Jennifer, additional, Fortunato, Angelo, additional, Frangieh, Allison, additional, Frye, Jennifer L., additional, Fulton, Robert S., additional, Galipeau, Danielle, additional, Gan, Siting, additional, Gao, Jianjiong, additional, Gao, Long, additional, Gao, Peng, additional, Gao, Vianne R., additional, Geiger, Tim, additional, George, Ajit, additional, Getz, Gad, additional, Giannakis, Marios, additional, Gibbs, David L., additional, Gillanders, William E., additional, Goedegebuure, Simon P., additional, Gould, Alanna, additional, Gowers, Kate, additional, Greenleaf, William, additional, Gresham, Jeremy, additional, Guerriero, Jennifer L., additional, Guha, Tuhin K., additional, Guimaraes, Alexander R., additional, Gutman, David, additional, Hacohen, Nir, additional, Hanlon, Sean, additional, Hansen, Casey R., additional, Harismendy, Olivier, additional, Harris, Kathleen A., additional, Hata, Aaron, additional, Hayashi, Akimasa, additional, Heiser, Cody, additional, Helvie, Karla, additional, Herndon, John M., additional, Hirst, Gilliam, additional, Hodi, Frank, additional, Hollmann, Travis, additional, Horning, Aaron, additional, Hsieh, James J., additional, Hughes, Shannon, additional, Huh, Won Jae, additional, Hunger, Stephen, additional, Hwang, Shelley E., additional, Ijaz, Heba, additional, Izar, Benjamin, additional, Jacobson, Connor A., additional, Janes, Samuel, additional, Jayasinghe, Reyka G., additional, Jiang, Lihua, additional, Johnson, Brett E., additional, Johnson, Bruce, additional, Ju, Tao, additional, Kadara, Humam, additional, Kaestner, Klaus, additional, Kagan, Jacob, additional, Kalinke, Lukas, additional, Keith, Robert, additional, Khan, Aziz, additional, Kibbe, Warren, additional, Kim, Albert H., additional, Kim, Erika, additional, Kim, Junhyong, additional, Kolodzie, Annette, additional, Kopytra, Mateusz, additional, Kotler, Eran, additional, Krueger, Robert, additional, Krysan, Kostyantyn, additional, Kundaje, Anshul, additional, Ladabaum, Uri, additional, Lake, Blue B., additional, Lam, Huy, additional, Laquindanum, Rozelle, additional, Laughney, Ashley M., additional, Lee, Hayan, additional, Lenburg, Marc, additional, Leonard, Carina, additional, Leshchiner, Ignaty, additional, Levy, Rochelle, additional, Li, Jerry, additional, Lian, Christine G., additional, Lim, Kian-Huat, additional, Lin, Jia-Ren, additional, Lin, Yiyun, additional, Liu, Qi, additional, Liu, Ruiyang, additional, Longabaugh, William J.R., additional, Longacre, Teri, additional, Ma, Cynthia X., additional, Macedonia, Mary Catherine, additional, Madison, Tyler, additional, Maher, Christopher A., additional, Maitra, Anirban, additional, Makinen, Netta, additional, Makowski, Danika, additional, Maley, Carlo, additional, Maliga, Zoltan, additional, Mallo, Diego, additional, Maris, John, additional, Markham, Nick, additional, Marks, Jeffrey, additional, Martinez, Daniel, additional, Mashl, Robert J., additional, Masilionais, Ignas, additional, Mason, Jennifer, additional, Massagué, Joan, additional, Massion, Pierre, additional, Mattar, Marissa, additional, Mazurchuk, Richard, additional, Mazutis, Linas, additional, McKinley, Eliot T., additional, McMichael, Joshua F., additional, Merrick, Daniel, additional, Meyerson, Matthew, additional, Miessner, Julia R., additional, Mills, Gordon B., additional, Mills, Meredith, additional, Mondal, Suman B., additional, Mori, Motomi, additional, Mori, Yuriko, additional, Moses, Elizabeth, additional, Mosse, Yael, additional, Muhlich, Jeremy L., additional, Murphy, George F., additional, Navin, Nicholas E., additional, Nederlof, Michel, additional, Ness, Reid, additional, Nevins, Stephanie, additional, Nikolov, Milen, additional, Nirmal, Ajit Johnson, additional, Nolan, Garry, additional, Novikov, Edward, additional, O’Connell, Brendan, additional, Offin, Michael, additional, Oh, Stephen T., additional, Olson, Anastasiya, additional, Ooms, Alex, additional, Ossandon, Miguel, additional, Owzar, Kouros, additional, Parmar, Swapnil, additional, Patel, Tasleema, additional, Patti, Gary J., additional, Pe'er, Itsik, additional, Peng, Tao, additional, Persson, Daniel, additional, Petty, Marvin, additional, Pfister, Hanspeter, additional, Polyak, Kornelia, additional, Pourfarhangi, Kamyar, additional, Puram, Sidharth V., additional, Qiu, Qi, additional, Quintanal-Villalonga, Álvaro, additional, Raj, Arjun, additional, Ramirez-Solano, Marisol, additional, Rashid, Rumana, additional, Reeb, Ashley N., additional, Reid, Mary, additional, Resnick, Adam, additional, Reynolds, Sheila M., additional, Riesterer, Jessica L., additional, Rodig, Scott, additional, Roland, Joseph T., additional, Rosenfield, Sonia, additional, Rotem, Asaf, additional, Roy, Sudipta, additional, Rozenblatt-Rosen, Orit, additional, Rudin, Charles M., additional, Ryser, Marc D., additional, Santi-Vicini, Maria, additional, Sato, Kazuhito, additional, Schrag, Deborah, additional, Schultz, Nikolaus, additional, Sears, Cynthia L., additional, Sears, Rosalie C., additional, Sen, Subrata, additional, Sen, Triparna, additional, Shalek, Alex, additional, Sheng, Jeff, additional, Sheng, Quanhu, additional, Shoghi, Kooresh I., additional, Shrubsole, Martha J., additional, Shyr, Yu, additional, Sibley, Alexander B., additional, Siex, Kiara, additional, Simmons, Alan J., additional, Singer, Dinah S., additional, Sivagnanam, Shamilene, additional, Slyper, Michal, additional, Sokolov, Artem, additional, Song, Sheng-Kwei, additional, Southard-Smith, Austin, additional, Spira, Avrum, additional, Stein, Janet, additional, Storm, Phillip, additional, Stover, Elizabeth, additional, Strand, Siri H., additional, Su, Timothy, additional, Sudar, Damir, additional, Sullivan, Ryan, additional, Surrey, Lea, additional, Suvà, Mario, additional, Terekhanova, Nadezhda V., additional, Ternes, Luke, additional, Thammavong, Lisa, additional, Thibault, Guillaume, additional, Thomas, George V., additional, Thorsson, Vésteinn, additional, Todres, Ellen, additional, Tran, Linh, additional, Tyler, Madison, additional, Uzun, Yasin, additional, Vachani, Anil, additional, Van Allen, Eliezer, additional, Vandekar, Simon, additional, Veis, Deborah J., additional, Vigneau, Sébastien, additional, Vossough, Arastoo, additional, Waanders, Angela, additional, Wagle, Nikhil, additional, Wang, Liang-Bo, additional, Wendl, Michael C., additional, West, Robert, additional, Wu, Chi-yun, additional, Wu, Hao, additional, Wu, Hung-Yi, additional, Wyczalkowski, Matthew A., additional, Xie, Yubin, additional, Yang, Xiaolu, additional, Yapp, Clarence, additional, Yu, Wenbao, additional, Yuan, Yinyin, additional, Zhang, Dadong, additional, Zhang, Kun, additional, Zhang, Mianlei, additional, Zhang, Nancy, additional, Zhang, Yantian, additional, Zhao, Yanyan, additional, Zhou, Daniel Cui, additional, Zhou, Zilu, additional, Zhu, Houxiang, additional, Zhu, Qin, additional, Zhu, Xiangzhu, additional, Zhu, Yuankun, additional, and Zhuang, Xiaowei, additional

Published
2020
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31. Predicting therapeutic nanoparticle efficacy using a companion MR imaging nanoparticle

Author

Miller, Miles A., Gadde, Suresh, Pfirschke, Christina, Engblom, Camilla, Sprachman, Melissa M., Kohler, Rainer H., Yang, Katherine S., Laughney, Ashley M., Wojtkiewicz, Gregory, Kamaly, Nazila, Bhonagiri, Sushma, Pittet, Mikael, Farokhzad, Omid C., and Weissleder, Ralph

Subjects
Diagnostic Imaging, Drug Delivery Systems, Nanomedicine, Humans, Nanoparticles, Article
Abstract

Therapeutic nanoparticles (TNPs) have shown heterogeneous responses in human clinical trials, raising the question of whether imaging should be used to identify patients with a higher likelihood of nanoparticle accumulation, and thus therapeutic response. Despite extensive debate about the enhanced permeability and retention (EPR) effect in tumors, it is increasingly clear that EPR is extremely variable yet little experimental data exists to predict its clinical utility. Based on the hypothesis that an FDA-approved 30-nm magnetic nanoparticle (MNP) could predict co-localization of therapeutic nanoparticles by MRI, we performed single-cell resolution imaging of fluorescently labeled MNPs and TNPs and studied their intratumoral distribution. We visualized MNPs circulating in tumor microvasculature and found sustained uptake into cells of the tumor microenvironment within minutes. MNPs could predictably demonstrate areas of co-localization for a model TNP [poly(D,L-lactic-co-glycolic acid)-b-polyethylene glycol; PLGA-b-PEG] within the tumor microenvironment (> 85% accuracy) and circulating within the microvasculature (>95% accuracy) despite their markedly different sizes and compositions. Computational analysis of NP transport enabled predictive modeling of TNP distribution based on imaging data, and identified key parameters governing intratumoral NP accumulation and macrophage uptake. Finally, MRI imaging accurately predicted initial treatment response and drug accumulation in a therapeutic study testing for the efficacy of paclitaxel-encapsulated nanoparticle. These approaches yield valuable insight into the in vivo kinetics of NP distribution and suggest that clinically-relevant imaging can be used to select patients with high EPR for treatment with TNPs.

Published
2015

34. Predicting therapeutic nanomedicine efficacy using a companion magnetic resonance imaging nanoparticle

Author

Miller, Miles A., primary, Gadde, Suresh, additional, Pfirschke, Christina, additional, Engblom, Camilla, additional, Sprachman, Melissa M., additional, Kohler, Rainer H., additional, Yang, Katherine S., additional, Laughney, Ashley M., additional, Wojtkiewicz, Gregory, additional, Kamaly, Nazila, additional, Bhonagiri, Sushma, additional, Pittet, Mikael J., additional, Farokhzad, Omid C., additional, and Weissleder, Ralph, additional

Published
2015
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44. ICA-guided delineation of breast cancer pathology

Author

Eguizabal, Alma, primary, Laughney, Ashley M., additional, Garcia-Allende, Pilar Beatriz, additional, Krishnaswamy, Venkataramanan, additional, Wells, Wendy A., additional, Paulsen, Keith D., additional, Pogue, Brian W., additional, Lopez-Higuera, Jose M., additional, and Conde, Olga M., additional

Published
2012
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