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1. Integrated single-cell sequencing and histopathological analyses reveal diverse injury and repair responses in a participant with acute kidney injury: a clinical-molecular-pathologic correlation

Author

Rajasree Menon, Andrew S. Bomback, Blue B. Lake, Christy Stutzke, Stephanie M. Grewenow, Steven Menez, Vivette D. D’Agati, Sanjay Jain, Richard Knight, Stewart H. Lecker, Isaac Stillman, Steve Bogen, Laurence H. Beck, Sushrut Waikar, Gearoid M. McMahon, Astrid Weins, Mia R. Colona, Nir Hacohen, Paul J. Hoover, Mark Aulisio, William S. Bush, Dana C. Crawford, John O'toole, Emilio Poggio, John Sedor, Leslie Cooperman, Stacey Jolly, Leal Herlitz, Jane Nguyen, Agustin Gonzalez-Vicente, Ellen Palmer, Dianna Sendrey, Carissa Vinovskis, Petter M. Bjornstad, Paul Appelbaum, Jonathan M. Barasch, Vivette D. D'Agati, Krzysztof Kiryluk, Karla Mehl, Pietro A. Canetta, Ning Shang, Olivia Balderes, Satoru Kudose, Shweta Bansal, Theodore Alexandrov, Helmut Rennke, Tarek M. El-Achkar, Yinghua Cheng, Pierre C. Dagher, Michael T. Eadon, Kenneth W. Dunn, Katherine J. Kelly, Timothy A. Sutton, Daria Barwinska, Michael J. Ferkowicz, Seth Winfree, Sharon Bledsoe, Marcelino Rivera, James C. Williams, Ricardo Melo Ferreira, Chirag R. Parikh, Celia P. Corona-Villalobos, Avi Rosenberg, Sylvia E. Rosas, Neil Roy, Mark Williams, Evren U. Azeloglu, Cijang He, Ravi Iyengar, Jens Hansen, Yuguang Xiong, Brad Rovin, Samir Parikh, John P. Shapiro, Christopher R. Anderton, Ljiljana Pasa-Tolic, Dusan Velickovic, Jessica Lukowski, George Oliver, Joseph Ardayfio, Jack Bebiak, Keith Brown, Catherine E. Campbell, John Saul, Anna Shpigel, Robert Koewler, Taneisha Campbell, Lynda Hayashi, Nichole Jefferson, Glenda V. Roberts, Roy Pinkeney, Olga Troyanskaya, Rachel Sealfon, Katherine R. Tuttle, Yury Goltsev, Kun Zhang, Zoltan G. Laszik, Garry Nolan, Patrick Boada, Minnie Sarwal, Tara Sigdel, Paul J. Lee, Rita R. Alloway, E. Steve Woodle, Heather Ascani, Ulysses G.J. Balis, Jeffrey B. Hodgin, Matthias Kretzler, Chrysta Lienczewski, Laura H. Mariani, Becky Steck, Yougqun He, Edgar Otto, Jennifer Schaub, Victoria M. Blanc, Sean Eddy, Ninive C. Conser, Jinghui Luo, Paul M. Palevsky, Matthew Rosengart, John A. Kellum, Daniel E. Hall, Parmjeet Randhawa, Mitchell Tublin, Raghavan Murugan, Michele M. Elder, James Winters, Charles E. Alpers, Kristina N. Blank, Jonas Carson, Ian H. De Boer, Ashveena L. Dighe, Jonathan Himmelfarb, Sean D. Mooney, Stuart Shankland, Kayleen Williams, Christopher Park, Frederick Dowd, Robyn L. McClelland, Stephen Daniel, Andrew N. Hoofnagle, Adam Wilcox, Kumar Sharma, Manjeri Venkatachalam, Guanshi Zhang, Annapurna Pamreddy, Hongping Ye, Richard Montellano, Robert D. Toto, Miguel Vazquez, Simon C. Lee, R. Tyler Miller, Orson W. Moe, Jose Torrealba, Nancy Wang, Asra Kermani, Kamalanathan Sambandam, Harold Park, S. Susan Hedayati, Christopher Y. Lu, Anitha Vijayan, Joseph P. Gaut, Dennis Moledina, Francis P. Wilson, Ugochukwu Ugwuowo, and Tanima Arora

Subjects
Pathology, Clinical, Nephrology, Humans, Acute Kidney Injury, Kidney, Article
Published
2022

2. Cadherin-11, Sparc-related modular calcium binding protein-2, and Pigment epithelium-derived factor are promising non-invasive biomarkers of kidney fibrosis

Author

Mark E. Williams, Katherine R. Tuttle, Jing Liu, Jinghui Luo, Yougqun He, Laura Pyle, Blue B. Lake, Brad H. Rovin, Lynda Hayashi, Yuguang Xiong, Dennis G. Moledina, Andreas Bueckle, Steven Menez, Glenda V. Roberts, Anand Srivastava, Paul Appelbaum, Heather Ascani, Catherine Campbell, Stephanie M. Grewenow, Mark Aulisio, Jennifer Sun, Christopher R. Anderton, Jamie L. Marshall, Sharon Bledso, John P. Shapiro, Theodore Alexandrov, Richard M. Caprioli, Michele Elder, Leslie Cooperman, Shweta Bansal, Lakeshia Bush, Krzysztof Kiryluk, Mitchell Tublin, Olga G. Troyanskaya, Emilio D. Poggio, Kristina N. Blank, Andrew Janowczyk, Paul Hoover, Sabine M. Diettman, R. Tyler Miller, Katy Borner, Leonidas G. Alexopoulos, James Winters, Anant Madabhushi, Haojia Wu, Chirag R. Parikh, Yumeng Wen, Avi Z. Rosenberg, Agustin Gonzalez-Vicente, Leal Herlitz, Keith Brown, Matthew Gilliam, Joseph P. Gaut, Vidya S. Viswanathan, Karla Mehl, Stewart H. Lecker, Pierre C. Dagher, Dana C. Crawford, Camille Johansen, Anna Greka, Tiffany Shi, Ari Pollack, Renee Frey, Kavya Sharman, Isaac E. Stillman, Stuart J. Shankland, Ricardo Melo Ferreira, Jack Bebiak, Jing Su, Matthias Kretzler, Ellen Palmer, Yury Goltsev, Aaron K. Wong, Matthew R. Rosengart, Taneisha Campbell, Tina Vita, Helmut G. Rennke, Nir Hacohen, Satoru Kudose, Christine Limonte, Kun Zhang, Robyn L. McClelland, Ulysses J. Balis, Katherine J. Kelly, Simon Lee, Ninive C. Conser, Adele Rike, Frederick Dowd, Timothy A. Sutton, Steve Bogen, Petter M. Bjornstad, Zoltan Laszik, Dianbo Zhang, Benjamin D. Humphreys, Pinaki Sarder, Jeffrey M. Spraggins, Ravi Iyengar, Marcelino Rivera, Roy Pinkeney, James C. Williams, Tarek M. El-Achkar, Laura H. Mariani, Richard J. Knight, Manjeri A. Venkatachalam, Pietro A. Canetta, Lloyd G. Cantley, Kayleen Williams, Catherine P. Jayapandian, Edgar A. Otto, Jessica Lukowski, Kassandra Spates-Harden, Ashish Verma, John Saul, Tariq Mukatash, Mia R. Colona, Shana Maikhor, Laurence H. Beck, Titlayo Ilori, Charles E. Alpers, Ellen M. Quardokus, Mujeeb Basit, Dušan Veličković, Raf Van de Plas, Jonathan Himmelfarb, Michael T. Eadon, Chrysta Lienczewski, Christopher Y. Lu, Yijiang M. Chen, Kasra Rezaei, Richard Montellano, Pottumarthi V. Prasad, Francis P. Wilson, Christy Stutzke, Jane Nguyen, Kamalanathan K. Sambandam, Miguel A. Vazquez, Vishal S. Vaidya, Vivette D. D'Agati, Patrick Boada, Adam Wilcox, Astrid Weins, Jennifer A. Schaub, Harold Park, Kumar Sharma, M. Todd Valerius, Stephen Daniel, Sean Eddy, Bruce W. Herr, Kenneth W. Dunn, Jamie Snyder, E. Steve Woodle, Dianna Sendrey, Ljiljana Paša-Tolić, Raghavan Murugan, Brandon Ginley, Bryan Kestenbaum, Celia P. Corona-Villalobos, Olivia Balderes, Sushrut Waikar, Carissa Vinovskis, Brooke Berry, Parmjeet Randhawa, Seth Winfree, Jose R. Torrealba, Ning Shang, Rachel Sealfon, Michael J. Ferkowicz, William S. Bush, Jonas Carson, Robert Koewler, Guanshi Zhang, Robert D. Toto, Ian H. de Boer, Gearoid M. McMahon, Andrew N. Hoofnagle, Vijaykumar R. Kakade, Brendon Lutnick, Melissa M. Shaw, Rita R. Alloway, Rajasree Menon, Afolarin Amodu, Jeanine Basta, Paul J. Lee, Ingrid Onul, Sylvia E. Rosas, Cijang (John) He, Andrew S. Bomback, Yinghua Cheng, Jeffrey B. Hodgin, Samir M. Parikh, Garry Nolan, John A. Kellum, Anil Pillai, Annapurna Pamreddy, Orson W. Moe, Jiten Patel, Jonathan J. Taliercio, S. Susan Hedayati, Anitha Vijayan, Tanima Arora, Evren U. Azeloglu, Paul M. Palevsky, Nathan Heath Patterson, Asra Kermani, Becky Steck, Kavya Anjani, Ashley Berglund, Yashvardhan Jain, Stacey E. Jolly, John R. Sedor, George (Holt) Oliver, Natasha Wen, Nancy Wang, Ruikang Wang, Joseph Ardayfio, Michael Rauchman, Ashley R. Burg, Victoria Blanc, Minnie M. Sarwal, Daniel Hall, Sethu M. Madhavan, Sean D. Mooney, Sushrut S. Waikar, Daria Barwinska, Christopher Y. Park, Tara K. Sigdel, Ugochukwu Ugwuowo, John F. O'Toole, Ragnar Palsson, Insa M. Schmidt, Joel M. Henderson, Hongping Ye, Jens Hansen, Jonathan Barasch, Neil Roy, Nicholas Lucarelli, Anna Shpigel, Ashveena Dighe, Elizabeth Record, Sanjay Jain, and Nichole Jefferson

Subjects
0301 basic medicine, Pathology, medicine.medical_specialty, Urinary system, 030232 urology & nephrology, Kidney, Article, 03 medical and health sciences, 0302 clinical medicine, PEDF, Fibrosis, Biopsy, Humans, Medicine, Osteonectin, Nerve Growth Factors, Prospective Studies, Renal Insufficiency, Chronic, Eye Proteins, Serpins, medicine.diagnostic_test, urogenital system, business.industry, Calcium-Binding Proteins, Cadherins, medicine.disease, 030104 developmental biology, medicine.anatomical_structure, Nephrology, Cohort, Disease Progression, Biomarker (medicine), business, Biomarkers, Kidney disease
Abstract

Kidney fibrosis constitutes the shared final pathway of nearly all chronic nephropathies, but biomarkers for the non-invasive assessment of kidney fibrosis are currently not available. To address this, we characterize five candidate biomarkers of kidney fibrosis: Cadherin-11 (CDH11), Sparc-related modular calcium binding protein-2 (SMOC2), Pigment epithelium-derived factor (PEDF), Matrix-Gla protein, and Thrombospondin-2. Gene expression profiles in single-cell and single-nucleus RNA-sequencing (sc/snRNA-seq) datasets from rodent models of fibrosis and human chronic kidney disease (CKD) were explored, and Luminex-based assays for each biomarker were developed. Plasma and urine biomarker levels were measured using independent prospective cohorts of CKD: the Boston Kidney Biopsy Cohort, a cohort of individuals with biopsy-confirmed semiquantitative assessment of kidney fibrosis, and the Seattle Kidney Study, a cohort of patients with common forms of CKD. Ordinal logistic regression and Cox proportional hazards regression models were used to test associations of biomarkers with interstitial fibrosis and tubular atrophy and progression to end-stage kidney disease and death, respectively. Sc/snRNA-seq data confirmed cell-specific expression of biomarker genes in fibroblasts. After multivariable adjustment, higher levels of plasma CDH11, SMOC2, and PEDF and urinary CDH11 and PEDF were significantly associated with increasing severity of interstitial fibrosis and tubular atrophy in the Boston Kidney Biopsy Cohort. In both cohorts, higher levels of plasma and urinary SMOC2 and urinary CDH11 were independently associated with progression to end-stage kidney disease. Higher levels of urinary PEDF associated with end-stage kidney disease in the Seattle Kidney Study, with a similar signal in the Boston Kidney Biopsy Cohort, although the latter narrowly missed statistical significance. Thus, we identified CDH11, SMOC2, and PEDF as promising non-invasive biomarkers of kidney fibrosis.

Published
2021

3. Large-scale, three-dimensional tissue cytometry of the human kidney: a complete and accessible pipeline

Author

Michael J. Ferkowicz, Seth Winfree, Angela R. Sabo, Malgorzata M. Kamocka, Suraj Khochare, Daria Barwinska, Michael T. Eadon, Ying-Hua Cheng, Carrie L. Phillips, Timothy A. Sutton, Katherine J. Kelly, Pierre C. Dagher, Tarek M. El-Achkar, Kenneth W. Dunn, Richard Knight, Stewart Lecker, Isaac Stillman, Gearoid Mcmahon, Sus Waikar, Astrid Weins, Nir Hacohen, Paul Hoover, Mark Aulisio, Leslie Cooperman, Leal Herlitz, John O'toole, Emilio Poggio, John Sedor, Paul Appelbaum, Jonathan Barasch, Andrew Bomback, Vivette D'agati, Krzysztof Kiryluk, Karla Mehl, Ning (Sunny) Shang, Chenhua Weng, Laura Barisoni, Theodore Alexandrov, Tarek Ashkar, Pierre Dagher, Kenneth Dunn, Michael Eadon, Michael Ferkowicz, Katherine Kelly, Timothy Sutton, Steven Menez, Chirag Parikh, Avi Rosenberg, Pam Villalobos, Alison Slack, Sylvia Rosas, Mark Williams, Evren Azeloglu, Cijang (John) He, Ravi Iyengar, Samir Parikh, Chris Anderton, Ljiljana Pasa-Tolic, Dusan Velickovic, George (Holt) Oliver, Joseph Ardayfio, Jack Bebiak, Keith Brown, Taneisha Campbell, Catherine Campbell, Lynda Hayashi, Nichole Jefferson, Robert Koewler, Glenda Roberts, John Saul, Anna Shpigel, Edith Christine Stutzke, Lorenda Wright, Leslie Miegs, Roy Pinkeney, Rachel Sealfon, Olga Troyanskaya, Katherine Tuttle, Yury Goltsev, Blue Lake, Kun Zhang, Dejan Dobi, Maria Joanes, Zoltan Laszik, Garry Nolan, Andrew Schroeder, Ulysses Balis, Oliver He, Jeffrey Hodgin, Matthias Kretzler, Laura Mariani, Rajasree Menon, Edgar Otto, Jennifer Schaub, Becky Steck, Michele Elder, Daniel Hall, John Kellum, Mary Kruth, Raghav Murugan, Paul Palevsky, Parmjeet Randhawa, Matthew Rosengart, Sunny Sims-Lucas, Mary Stefanick, Stacy Stull, Mitchell Tublin, Charles Alpers, Ian De Boer, Malia Fullerton, Jonathan Himmelfarb, Robyn Mcclelland, Sean Mooney, Stuart Shankland, Kayleen Williams, Kristina Blank, Ashveena Dighe, Jonas Carson, Frederick Dowd, Zach Drager, Kumar Sharma, Guanshi Zhang, Asra Kermani, Simon Lee, Christopher Lu, Tyler Miller, Orson Moe, Harold Park, Kamalanathan Sambandam, Francisco Sanchez, Jose Torrealba, Toto Robert, Miguel Vazquez, Nancy Wang, Joe Gaut, Sanjay Jain, Anitha Vijayan, Randy Luciano, Dennis Moledina, Ugwuowo Ugochukwu, and Francis Perry Wilson

Subjects
0301 basic medicine, Computer science, Confocal, Cytological Techniques, Context (language use), Kidney, Article, Pathology and Forensic Medicine, law.invention, Flow cytometry, 03 medical and health sciences, 0302 clinical medicine, Imaging, Three-Dimensional, Confocal microscopy, law, Microscopy, medicine, Humans, Image analysis, Molecular Biology, Fluorescent Dyes, Microscopy, Confocal, medicine.diagnostic_test, Cell Biology, Autofluorescence, 030104 developmental biology, Microscopy, Fluorescence, Multiphoton, 030220 oncology & carcinogenesis, Cytometry, Software, Biomedical engineering
Abstract

The advent of personalized medicine has driven the development of novel approaches for obtaining detailed cellular and molecular information from clinical tissue samples. Tissue cytometry is a promising new technique that can be used to enumerate and characterize each cell in a tissue and, unlike flow cytometry and other single-cell techniques, does so in the context of the intact tissue, preserving spatial information that is frequently crucial to understanding a cell’s physiology, function, and behavior. However, the wide-scale adoption of tissue cytometry as a research tool has been limited by the fact that published examples utilize specialized techniques that are beyond the capabilities of most laboratories. Here we describe a complete and accessible pipeline, including methods of sample preparation, microscopy, image analysis, and data analysis for large-scale three-dimensional tissue cytometry of human kidney tissues. In this workflow, multiphoton microscopy of unlabeled tissue is first conducted to collect autofluorescence and second-harmonic images. The tissue is then labeled with eight fluorescent probes, and imaged using spectral confocal microscopy. The raw 16-channel images are spectrally deconvolved into 8-channel images, and analyzed using the Volumetric Tissue Exploration and Analysis (VTEA) software developed by our group. We applied this workflow to analyze millimeter-scale tissue samples obtained from human nephrectomies and from renal biopsies from individuals diagnosed with diabetic nephropathy, generating a quantitative census of tens of thousands of cells in each. Such analyses can provide useful insights that can be linked to the biology or pathology of kidney disease. The approach utilizes common laboratory techniques, is compatible with most commercially-available confocal microscope systems and all image and data analysis is conducted using the VTEA image analysis software, which is available as a plug-in for ImageJ. Tissue cytometry is a promising new microscopy technique that can be used to enumerate and characterize each cell in a tissue. Here the authors describe a complete and accessible pipeline, including methods of sample preparation, microscopy, image analysis, and data analysis for large-scale three-dimensional tissue cytometry of human kidney tissues.

Published
2020

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