Abnormal oxidative metabolism in a quiet genomic background underlies clear cell papillary renal cell carcinoma
Open accessAbstract
While genomic sequencing routinely identifies oncogenic alterations for the majority of cancers, many tumors harbor no discernable driver lesion. Here, we describe the exceptional molecular phenotype of a genomically quiet kidney tumor, clear cell papillary renal cell carcinoma (CCPAP). In spite of a largely wild-type nuclear genome, CCPAP tumors exhibit severe depletion of mitochondrial DNA (mtDNA) and RNA and high levels of oxidative stress, reflecting a shift away from respiratory metabolism. Moreover, CCPAP tumors exhibit a distinct metabolic phenotype uniquely characterized by accumulation of the sugar alcohol sorbitol. Immunohistochemical staining of primary CCPAP tumor specimens recapitulates both the depletion of mtDNA-encoded proteins and a lipid-depleted metabolic phenotype, suggesting that the cytoplasmic clarity in CCPAP is primarily related to the presence of glycogen. These results argue for non-genetic profiling as a tool for the study of cancers of unknown driver.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Detailed molecular analysis of CCPAP found a low genomic burden of point mutations and copy-number variants, no recurrent nonsynonymous mutations, and a DNA methylation pattern resembling nonmalignant kidney.
“Nevertheless, a detailed molecular analysis revealed a low genomic burden of point mutations and copy-number variants, no recurrent nonsynonymous mutations, and a DNA methylation pattern that resembles the nonmalignant kidney.”
From Metabolic reprogramming and cancer progression (2020) · cites this paper as [13]
CCPAP tumors have metabolomic signatures suggesting oxidative stress, suppressed oxidative metabolism, and depletion of mitochondrial DNA and RNA.
“These tumors bear metabolomic signatures that suggest oxidative stress, suppressed oxidative metabolism, and depletion of mitochondrial DNA and RNA.”
From Metabolic reprogramming and cancer progression (2020) · cites this paper as [13]
Some tumors lack recurrent mutations in canonical tumor suppressors and oncogenes but still have stereotyped metabolic properties that distinguish them from nonmalignant tissues.
“Some tumors lack recurrent mutations in canonical tumor suppressors and oncogenes but still harbor stereotyped metabolic properties that distinguish them from nonmalignant tissues.”
From Metabolic reprogramming and cancer progression (2020) · cites this paper as [13]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Fast and accurate short read alignment with Burrows-Wheeler transform
Li, H., & Durbin, R. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp324 · Cited by 58,607 · see citing works
Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., Lander, E. S., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506580102 · Cited by 53,625 · see citing works
Warburg, O. (1956) · Science · doi:10.1126/science.123.3191.309 · Cited by 13,425 · see citing works
Fast and accurate long-read alignment with Burrows-Wheeler transform.
Li, H., & Durbin, R. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp698 · Cited by 12,063 · see citing works
Enrichr: a comprehensive gene set enrichment analysis web server 2016 update
Kuleshov, M. V., Jones, M. R., Rouillard, A. D., Fernandez, N. F., Duan, Q., Wang, Z., Koplev, S., Jenkins, S. L., Jagodnik, K. M., Lachmann, A., et al. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw377 · Cited by 10,799 · see citing works
Statistical significance for genomewide studies
Storey, J. D., & Tibshirani, R. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1530509100 · Cited by 9,692 · see citing works
Velvet: Algorithms for de novo short read assembly using de Bruijn graphsPreprint
Zerbino, D. R., & Birney, E. (2008) · Genome Research · doi:10.1101/gr.074492.107 · Cited by 9,387 · see citing works
An integrated map of genetic variation from 1,092 human genomes
The 1000 Genomes Project Consortium (2012) · Nature · doi:10.1038/nature11632 · Cited by 7,711 · see citing works
Self-citation(1968) · Medical Entomology and Zoology · Cited by 4,924 · see citing works
On Respiratory Impairment in Cancer Cells
Warburg, O. H. (1956) · Science · doi:10.1126/science.124.3215.269 · Cited by 3,472 · see citing works
Zehir, A., Benayed, R., Shah, R. H., Syed, A., Middha, S., Kim, H. R., Srinivasan, P., Gao, J., Chakravarty, D., Devlin, S. M., et al. (2017) · Nature Medicine · doi:10.1038/nm.4333 · Cited by 3,380 · cited 2× · see citing works
“Within our own institution’s prospective sequencing cohort [16], nearly 8% of tumors show 108 no alterations in the 341 cancer-associated genes assayed by the clinical sequencing panel.”
BackgroundSelf-citationWallace, D. C. (2012) · Nature Reviews Cancer · doi:10.1038/nrc3365 · Cited by 2,404 · see citing works
Landscape of somatic mutations in 560 breast cancer whole-genome sequences
Nik-Zainal, S., Davies, H., Staaf, J., Ramakrishna, M., Glodzik, D., Zou, X., Martincorena, I., Alexandrov, L. B., Martin, S., Wedge, D. C., et al. (2016) · Nature · doi:10.1038/nature17676 · Cited by 2,218 · see citing works
Self-citationVyas, S., Zaganjor, E., & Haigis, M. C. (2016) · Cell · doi:10.1016/j.cell.2016.07.002 · Cited by 1,735 · see citing works
The Life History of 21 Breast Cancers
Nik-Zainal, S., Van Loo, P., Wedge, D. C., Alexandrov, L. B., Greenman, C. D., Lau, K. W., Raine, K., Jones, D., Marshall, J., Ramakrishna, M., et al. (2012) · Cell · doi:10.1016/j.cell.2012.04.023 · Cited by 1,443 · see citing works
Self-citationEvans, A. M., DeHaven, C. D., Barrett, T., Mitchell, M. W., & Milgram, K. E. (2009) · Analytical Chemistry · doi:10.1021/ac901536h · Cited by 1,315 · see citing works
Zong, W., Rabinowitz, J. D., & White, E. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.02.011 · Cited by 1,287 · see citing works
Shen, R., & Seshan, V. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw520 · Cited by 1,263 · see citing works
Allele-specific copy number analysis of tumors
Loo, P. V., Nord, S., Lingjærde, O. C., Russnes, H. G., Rye, I. H., Sun, W., Weigman, V., Marynen, P., Zetterberg, A., Naume, B., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1009843107 · Cited by 1,231 · see citing works
Rosenthal, R., McGranahan, N., Herrero, J., Taylor, B. S., & Swanton, C. (2016) · Genome biology · doi:10.1186/s13059-016-0893-4 · Cited by 1,217 · see citing works
A community-driven global reconstruction of human metabolism
Thiele, I., Swainston, N., Fleming, R. M. T., Hoppe, A., Sahoo, S., Aurich, M. K., Haraldsdottir, H., Mo, M. L., Rolfsson, O., Stobbe, M. D., et al. (2013) · Nature Biotechnology · doi:10.1038/nbt.2488 · Cited by 1,019 · see citing works
Zhang, H., Gao, P., Fukuda, R., Kumar, G., Krishnamachary, B., Zeller, K. I., Dang, C. V., & Semenza, G. L. (2007) · Cancer Cell · doi:10.1016/j.ccr.2007.04.001 · Cited by 885 · see citing works
Chang, M. T., Asthana, S., Gao, S. P., Lee, B. H., Chapman, J. S., Kandoth, C., Gao, J., Socci, N. D., Solit, D. B., Olshen, A. B., et al. (2016) · Nature Biotechnology · doi:10.1038/nbt.3391 · Cited by 808 · see citing works
Self-citationAn Integrated Metabolic Atlas of Clear Cell Renal Cell Carcinoma
Hakimi, A. A., Reznik, E., Lee, C., Creighton, C. J., Brannon, A. R., Luna, A., Aksoy, B. A., Liu, E. M., Shen, R., Lee, W., et al. (2016) · Cancer Cell · doi:10.1016/j.ccell.2015.12.004 · Cited by 791 · see citing works
Self-citationSoga, T., Baran, R., Suematsu, M., Ueno, Y., Ikeda, S., Sakurakawa, T., Kakazu, Y., Ishikawa, T., Robert, M., Nishioka, T., et al. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m601876200 · Cited by 740 · see citing works
Epigenomic alterations define lethal CIMP-positive ependymomas of infancy
Mack, S. C., Witt, H., Piro, R. M., Gu, L., Zuyderduyn, S., Stütz, A. M., Wang, X., Gallo, M., Garzia, L., Zayne, K., et al. (2014) · Nature · doi:10.1038/nature13108 · Cited by 607 · see citing works
Mansfield, K. D., Guzy, R. D., Pan, Y., Young, R. M., Cash, T. P., Schumacker, P. T., & Simon, M. C. (2005) · Cell Metabolism · doi:10.1016/j.cmet.2005.05.003 · Cited by 606 · see citing works
mtDNA Variation and Analysis Using Mitomap and Mitomaster
Lott, M. T., Leipzig, J. N., Derbeneva, O. A., Xie, H. M., Chalkia, D., Sarmady, M., Procaccio, V., & Wallace, D. C. (2013) · Current Protocols in Bioinformatics · doi:10.1002/0471250953.bi0123s44 · Cited by 557 · see citing works
Oxidative stress induces degradation of mitochondrial DNA
Shokolenko, I. N., Venediktova, N. I., Bochkareva, A., Wilson, G. L., & ALEXEYEV, M. F. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp100 · Cited by 556 · see citing works
Mitochondrial DNA copy number variation across human cancers
Reznik, E., Miller, M. L., Şenbabaoğlu, Y., Riaz, N., Sarungbam, J., Tickoo, S. K., Al‐Ahmadie, H. A., Lee, W., Seshan, V., Hakimi, A. A., et al. (2016) · eLife · doi:10.7554/elife.10769 · Cited by 515 · see citing works
Self-citationDetecting ultralow-frequency mutations by Duplex Sequencing
Kennedy, S. R., Schmitt, M. W., Fox, E. J., Kohrn, B. F., Salk, J. J., Ahn, E. H., Prindle, M. J., Kuong, K. J., Shen, J.-C., Risques, R.-A., et al. (2014) · Nature Protocols · doi:10.1038/nprot.2014.170 · Cited by 503 · see citing works
Self-citationSpectrum of Epithelial Neoplasms in End-Stage Renal Disease
Tickoo, S. K., de Peralta‐Venturina, M., Harik, L. R., Worcester, H. D., Salama, M. E., Young, A. N., Moch, H., & Amin, M. B. (2006) · The American Journal of Surgical Pathology · doi:10.1097/01.pas.0000185382.80844.b1 · Cited by 476 · see citing works
Self-citationMultilevel Genomics-Based Taxonomy of Renal Cell Carcinoma
Chen, F., Zhang, Y., Şenbabaoğlu, Y., Ciriello, G., Yang, L., Reznik, E., Shuch, B., Micevic, G., de Velasco, G., Shinbrot, E., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.02.024 · Cited by 360 · see citing works
Self-citationEl‐Hattab, A. W., & Scaglia, F. (2013) · Neurotherapeutics · doi:10.1007/s13311-013-0177-6 · Cited by 336 · see citing works
Molecular Characterization and Clinical Relevance of Metabolic Expression Subtypes in Human Cancers
Peng, X., Chen, Z., Farshidfar, F., Xiaoyan, X., Lorenzi, P. L., Wang, Y., Cheng, F., Tan, L., Mojumdar, K., Du, D., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.03.077 · Cited by 334 · see citing works
Self-citationPan, Y., Mansfield, K. D., Bertozzi, C. C., Rudenko, V., Chan, D. A., Giaccia, A. J., & Simon, M. C. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.01223-06 · Cited by 332 · see citing works
Clear Cell Papillary Renal Cell Carcinoma
Gobbo, S., Eble, J. N., Grignon, D. J., Martignoni, G., MacLennan, G. T., Shah, R. B., Zhang, S., Brunelli, M., & Liang Cheng, C. (2008) · The American Journal of Surgical Pathology · doi:10.1097/pas.0b013e318164bcbb · Cited by 271 · see citing works
An alcoholic binge causes massive degradation of hepatic mitochondrial DNA in mice
Mansouri, A., Gaou, I., de Kerguenec, C., Amsellem, S., Haouzi, D., Berson, A., Moreau, A., Feldmann, G., Lettéron, P., Pessayre, D., et al. (1999) · Gastroenterology · doi:10.1016/s0016-5085(99)70566-4 · Cited by 208 · see citing works
Rohan, S. M., Xiao, Y., Liang, Y., Dudas, M. E., Al‐Ahmadie, H. A., Fine, S. W., Gopalan, A., Reuter, V. E., Rosenblum, M. K., Russo, P., et al. (2011) · Modern Pathology · doi:10.1038/modpathol.2011.80 · Cited by 176 · see citing works
Self-citationA landscape of metabolic variation across tumor types
Reznik, E., Luna, A., Aksoy, B. A., Liu, E. M., La, K., Ostrovnaya, I., Creighton, C. J., Hakimi, A. A., & Sander, C. (2018) · Cell Systems · doi:10.1016/j.cels.2017.12.014 · Cited by 172 · see citing works
Self-citationThe Genomic Landscape of Renal Oncocytoma Identifies a Metabolic Barrier to Tumorigenesis
Joshi, S., Tolkunov, D., Aviv, H., Hakimi, A. A., Yao, M., Hsieh, J. J.-D., Ganesan, S., Chan, C. S., & White, E. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.10.059 · Cited by 161 · see citing works
Self-citationPostlipopolysaccharide Oxidative Damage of Mitochondrial DNA
Suliman, H. B., Carraway, M. S., & Piantadosi, C. A. (2003) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200206-518oc · Cited by 153 · see citing works
cgpPindel: Identifying Somatically Acquired Insertion and Deletion Events from Paired End Sequencing
Raine, K. M., Hinton, J., Butler, A. P., Teague, J. W., Davies, H. R., Tarpey, P. S., Nik‐Zainal, S., & Campbell, P. J. (2015) · Current Protocols in Bioinformatics · doi:10.1002/0471250953.bi1507s52 · Cited by 141 · see citing works
Williamson, S. R., Eble, J. N., Liang Cheng, C., & Grignon, D. J. (2012) · Modern Pathology · doi:10.1038/modpathol.2012.204 · Cited by 140 · see citing works
Mitochondrial respiratory gene expression is suppressed in many cancers
Reznik, E., Wang, Q., La, K., Schultz, N. D., & Sander, C. (2017) · eLife · doi:10.7554/elife.21592 · Cited by 136 · see citing works
Self-citationEarly loss of mitochondrial complex I and rewiring of glutathione metabolism in renal oncocytoma
Gopal, R. K., Calvo, S. E., Shih, A. R., Chaves, F. L., McGuone, D., Mick, E., Pierce, K. A., Li, Y., Garofalo, A., Allen, E. M. V., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1711888115 · Cited by 102 · see citing works
Renal Cell Carcinoma With Clear Cell and Papillary Features
Ross, H. M., Martignoni, G., & Argani, P. (2012) · Archives of Pathology & Laboratory Medicine · doi:10.5858/arpa.2011-0479-ra · Cited by 101 · see citing works
Adam, J., Couturier, J., Molinié, V., Vieillefond, A., & Sibony, M. (2011) · Histopathology · doi:10.1111/j.1365-2559.2011.03857.x · Cited by 95 · see citing works
Metabolomics of mitochondrial disease
Esterhuizen, K., van der Westhuizen, F. H., & Louw, R. (2017) · Mitochondrion · doi:10.1016/j.mito.2017.05.012 · Cited by 94 · see citing works
Priolo, C., Khabibullin, D., Reznik, E., Filippakis, H., Ogórek, B., Kavanagh, T. R., Nijmeh, J., Herbert, Z. T., Asara, J. M., Kwiatkowski, D. J., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1710849115 · Cited by 82 · see citing works
Self-citationGrandhi, S., Bosworth, C. M., Maddox, W. J., Sensiba, C., Akhavanfard, S., Ni, Y., & LaFramboise, T. (2017) · Human Molecular Genetics · doi:10.1093/hmg/ddx172 · Cited by 74 · see citing works
Of Mice and Men: Divergence of Gene Expression Patterns in Kidney
Cheval, L., Pierrat, F., Rajerison, R. M., Piquemal, D., & Doucet, A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0046876 · Cited by 69 · see citing works
Reduction and Restoration of Mitochondrial DNA Content After Focal Cerebral Ischemia/Reperfusion
Chen, H., Hu, C., He, Y. Y., Yang, D., Xu, J., & Hsu, C. Y. (2001) · Stroke · doi:10.1161/hs1001.097099 · Cited by 68 · see citing works
Self-citationLawrie, C. H., Larrea, E., Larrinaga, G., Goicoechea, I., Arestin, M., Fernández‐Mercado, M., Hes, O., Cáceres, F., Manterola, L., & Lopez, J. I. (2013) · The Journal of Pathology · doi:10.1002/path.4296 · Cited by 59 · see citing works
Lee, B. (2017) · Urologic Oncology Seminars and Original Investigations · doi:10.1016/j.urolonc.2017.07.023 · Cited by 46 · see citing works
VAGrENT: Variation Annotation Generator
Menzies, A., Teague, J. W., Butler, A. P., Davies, H. R., Tarpey, P. S., Nik‐Zainal, S., & Campbell, P. J. (2015) · Current Protocols in Bioinformatics · doi:10.1002/0471250953.bi1508s52 · Cited by 26 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Masson P 1929 Some histological methods: trichrome stainings and their preliminary technique Journal of Technical Methods 12 75 90
Cited by
Sorted by citations
Metabolic reprogramming and cancer progression
Faubert, B., Solmonson, A., & DeBerardinis, R. J. (2020) · Science · doi:10.1126/science.aaw5473 · Cited by 2,740 · see citing works
Trpkov, K., Hes, O., Williamson, S. R., Adeniran, A., Agaimy, A., Alaghehbandan, R., Amin, M. B., Argani, P., Chen, Y., Liang Cheng, C., et al. (2021) · Modern Pathology · doi:10.1038/s41379-021-00779-w · Cited by 269 · see citing works
Self-citationA Cellular Mechanism to Detect and Alleviate Reductive Stress.
Manford, A., Rodríguez-Pérez, F., Shih, K. Y., Shi, Z., Berdan, C. A., Choe, M., Titov, D., Nomura, D., & Rapé, M. (2020) · Cell · doi:10.1016/j.cell.2020.08.034 · Cited by 185 · see citing works
Liu, W.-W., Zheng, S.-Q., Tian, L., Fei, Y.-F., Wang, C., Zhang, S., Wang, F., Jiang, G., & Wang, H. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01777-5 · Cited by 182 · see citing works
Williamson, S. R., Gill, A. J., Argani, P., Chen, Y., Egevad, L., Kristiansen, G., Grignon, D. J., & Hes, O. (2020) · The American Journal of Surgical Pathology · doi:10.1097/pas.0000000000001476 · Cited by 110 · see citing works
Self-citationBădoiu, S. C., Greabu, M., Miricescu, D., Stănescu-Spînu, I.-I., Ilinca, R., Bălan, D. G., Balcangiu‐Stroescu, A.-E., Mihai, D. A., Văcăroiu, I. A., Ștefani, C., et al. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24098391 · Cited by 99 · see citing works
DiNatale, R. G., Gorelick, A. N., Makarov, V., Blum, K. A., Silagy, A. W., Freeman, B., Chowell, D., Marcon, J., Mano, R., Sanchez, A., et al. (2019) · European Urology Focus · doi:10.1016/j.euf.2019.11.013 · Cited by 56 · see citing works
Self-citationClear cell papillary renal cell carcinoma: an update after 15 years
Williamson, S. R. (2020) · Pathology · doi:10.1016/j.pathol.2020.10.002 · Cited by 55 · see citing works
Tretiakova, M. (2022) · Advances in Anatomic Pathology · doi:10.1097/pap.0000000000000332 · Cited by 50 · see citing works
Weng, S., DiNatale, R. G., Silagy, A. W., Mano, R., Attalla, K., Kashani, M., Weiss, K. L., Benfante, N. E., Winer, A., Coleman, J., et al. (2020) · European Urology · doi:10.1016/j.eururo.2020.09.027 · Cited by 46 · see citing works
Self-citationArima, K., Lau, M. C., Zhao, M. M., Haruki, K., Kosumi, K., Mima, K., Gu, M., Väyrynen, J. P., Twombly, T. S., Baba, Y., et al. (2020) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-19-1091 · Cited by 43 · see citing works
Macklin, P. S., Yamamoto, A., Browning, L., Hofer, M., Adam, J., & Pugh, C. W. (2020) · The Journal of Pathology · doi:10.1002/path.5402 · Cited by 33 · see citing works
Characteristics of Clear Cell Papillary Renal Cell Carcinoma (ccpRCC)
Rysz, J., Franczyk, B., Ławiński, J., & Gluba-Brzózka, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms23010151 · Cited by 33 · see citing works
Renal Cell Carcinoma in End-Stage Renal Disease: A Review and Update
El‐Zaatari, Z. M., & Truong, L. D. (2022) · Biomedicines · doi:10.3390/biomedicines10030657 · Cited by 32 · see citing works
Greene, C., Attwood, K. M., Sharma, N. J., Balderman, B., Deng, R., Muhitch, J. B., Smith, G. J., Gross, K. W., Xu, B., & KAUFFMAN, E. C. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.923043 · Cited by 22 · see citing works
Defining clear cell papillary renal cell carcinoma in routine clinical practice
Gupta, S., Inwards, C. Y., Dyke, D. L. V., Jiménez, R. E., & Cheville, J. C. (2020) · Histopathology · doi:10.1111/his.14071 · Cited by 22 · see citing works
DiNatale, R. G., Sánchez, A., Hakimi, A. A., & Reznik, E. (2019) · Urologic Oncology Seminars and Original Investigations · doi:10.1016/j.urolonc.2019.04.028 · Cited by 20 · see citing works
Self-citationA contemporary guide to chromosomal copy number profiling in the diagnosis of renal cell carcinoma
Gupta, S., Sukov, W. R., Vanderbilt, C., Shen, W., Herrera-Hernandez, L. P., Lohse, C. M., Thompson, R. H., Boorjian, S. A., Leibovich, B. C., Jiménez, R. E., et al. (2021) · Urologic Oncology Seminars and Original Investigations · doi:10.1016/j.urolonc.2021.04.042 · Cited by 18 · see citing works
Sanguedolce, F., Roberta Mazzucchelli, A., Falagario, U. G., Cormio, A., Zanelli, M., Palicelli, A., Zizzo, M., Eccher, A., Brunelli, M., Galosi, A. B., et al. (2024) · Cancers · doi:10.3390/cancers16101856 · Cited by 16 · see citing works
Metabolomics in cancer and cancer-associated inflammatory cells
dos Santos, G. C., Saldanha-Gama, R. F. G., de Brito, N. M., Renovato‐Martins, M., & Barja‐Fidalgo, C. (2021) · Journal of Cancer Metastasis and Treatment · doi:10.20517/2394-4722.2020.86 · Cited by 12 · see citing works
Saxena, S., Dagar, N., Shelke, V., Lech, M., Khare, P., & Gaikwad, A. B. (2023) · Drug Discovery Today · doi:10.1016/j.drudis.2023.103765 · Cited by 11 · see citing works
Molecular signature of renal cell carcinoma by means of a multiplatform metabolomics analysis
Kordalewska, M., Wawrzyniak, R., Jacyna, J., Godzień, J., López‐Gonzálvez, Á., Raczak‐Gutknecht, J., Markuszewski, M., Gutknecht, P. G., Matuszewski, M., Siebert, J., et al. (2022) · Biochemistry and Biophysics Reports · doi:10.1016/j.bbrep.2022.101318 · Cited by 10 · see citing works
Eggers, H., Güler, F., Ehlers, U., Ivanyi, P., Peters, I., & Grünwald, V. (2019) · Future Oncology · doi:10.2217/fon-2019-0397 · Cited by 9 · see citing works
Elfakharany, H. K., Ghoraba, H. M., Gaweesh, K. A., Eldeen, A. A. S., & Eid, A. (2024) · Pathology - Research and Practice · doi:10.1016/j.prp.2023.155070 · Cited by 6 · see citing works
Charakterisierung der unterschiedlichen Entitäten beim Nierenzellkarzinom
Rupp, N. J., & Moch, H. (2020) · Der Urologe · doi:10.1007/s00120-019-01108-5 · Cited by 5 · see citing works
Renal Cell Tumors: Molecular Findings Reshaping Clinico-pathological Practice
Tretiakova, M. (2020) · Archives of Medical Research · doi:10.1016/j.arcmed.2020.08.003 · Cited by 6 · see citing works
Zhao, X., Qin, Y., Wang, B., Liu, J., Wang, Y., Chen, K., Zhao, J., Zhang, L., Wu, Y., & Liu, L. (2024) · Nanoscale Advances · doi:10.1039/d4na00042k · Cited by 5 · see citing works
Self-citationMetastatic clear cell papillary renal cell ‘tumour’
Gupta, S., Dasari, S., Sharma, V., Atwell, T. D., Sivasankaran, G., Smoley, S. A., Hardcastle, J. J., Lohse, C. M., Tekin, B., Jiménez, R. E., et al. (2023) · Histopathology · doi:10.1111/his.15123 · Cited by 4 · see citing works
Gupta, S., Pitel, B. A., Knight, S. M., Halling, K. C., Jiménez, R. E., & Cheville, J. C. (2021) · European Urology · doi:10.1016/j.eururo.2021.05.011 · Cited by 3 · see citing works
Global Protein Profiling in Processed Immunohistochemistry Tissue Sections
Venz, S., Halbach, V. V. B. U., Hentschker, C., Junker, H., Kuss, A. W., Sura, T., Krüger, E., Völker, U., Halbach, O. V. B. U., Jensen, L. R., et al. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241411308 · Cited by 2 · see citing works
Filippou, P. L., Shuch, B. M., & Psutka, S. P. (2021) · European Urology · doi:10.1016/j.eururo.2021.01.023 · Cited by 2 · see citing works
[Histological subtypes of renal cell carcinoma : Overview and new developments].
Polifka, I., Agaimy, A., Moch, H., & Hartmann, A. (2021) · PubMed · doi:10.1007/s00292-021-00937-6 · Cited by 1 · see citing works
Targeting Metabolic Reprogramming: A New Frontier in Cancer Therapy
Thakur, R. K., & Kumari, N. (2025) · Springer eBooks · doi:10.1007/978-981-96-7336-0_9 · Cited by 1 · see citing works
Mitochondrial changes in clear cell renal cell carcinoma: mechanisms and potential targets
Yang, J., Pan, X., Luo, X., Zheng, X., & Wang, J. (2026) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2026.153354 · Cited by 1 · see citing works
Chen, Y., Liu, Z., Yu, Q., Sun, X., Wang, S., Zhu, Q., Yang, J., & Jiang, R. (2023) · International Journal of Genomics · doi:10.1155/2023/5542233 · Cited by 1 · see citing works
Self-citationUnique metabolic traits identify CCPAP
Wang, M. (2019) · Nature Reviews Nephrology · doi:10.1038/s41581-019-0151-6
Molekularpathologie bei urologischen Tumoren
Hommerding, O., Allory, Y., Argani, P., Bismar, T. A., Bubendorf, L., Cañete‐Portillo, S., Chaux, A., Chen, Y., Liang Cheng, C., Cubilla, A. L., et al. (2021) · Der Pathologe · doi:10.1007/s00292-020-00888-4
Self-citationHistologische Subtypen des Nierenzellkarzinoms : Übersicht und neue Entwicklungen
Polifka, I., Agaimy, A., Moch, H., & Hartmann, A. (2021) · Zurich Open Repository and Archive (University of Zurich) · doi:10.5167/uzh-203646
(2021) · American Registry of PathologyArlington, Virginia eBooks · doi:10.55418/9781933477176-2
What Is New in Pathologic Diagnosis and Classification of the Common Renal Cell Neoplasms?
Zalles, N., & Williamson, S. R. (2024) · Surgical pathology clinics · doi:10.1016/j.path.2024.08.011
Park, K., Wang, Y., Kim, K., Serrano, J., Chen, F., Vasudevaraja, V., Feng, X., Mirsadraei, L., Snuderl, M., & Deng, F.-M. (2026) · The American Journal of Surgical Pathology · doi:10.1097/pas.0000000000002568
Jakobsson, R. G., Lindström, M., Arvidsson, Y., Johansson, I., Nilsson, J. A., Marcussen, N., Karlsson, J. W., & Johansson, M. (2026) · Cancers · doi:10.3390/cancers18162713
- Authors
- Xu, J., Reznik, E., Lee, H.-J., Gundem, G., Jonsson, P., Sarungbam, J., Bialik, A., Sanchez-Vega, F., Creighton, C. J., Hoekstra, J., Zhang, L., Sajjakulnukit, P., Kremer, D., Tolstyka, Z., Casuscelli, J., Stirdivant, S., Tang, J., Schultz, N., Jeng, P., Dong, Y., Su, W., Cheng, E. H., Russo, P., Coleman, J. A., Papaemmanuil, E., Chen, Y.-B., Reuter, V. E., Sander, C., Kennedy, S. R., Hsieh, J. J., Lyssiotis, C. A., Tickoo, S. K., & Hakimi, A. A.
- Affiliations
- Memorial Sloan Kettering Cancer Center (US)
- University of Michigan (US)
- Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, United States
- Baylor College of Medicine (US)
- University of Washington (US)
- Ludwig-Maximilians-Universität München (DE)
- Metabolon Inc, Durham, United States
- Cedars-Sinai Medical Center (US)
- Harvard University (US)
- Washington University in St. Louis (US)
- Corresponding author
- Reznik, Ed
- Lyssiotis, Costas A
- Tickoo, Satish K
- Hakimi, A Ari
- ORCID
- Xu, Jianing
- Reznik, Ed
- Lee, Ho-Joon
- Gundem, Gunes
- Jonsson, Philip
- Sarungbam, Judy
- Creighton, Chad J
- Hoekstra, Jake
- Zhang, Li
- Sajjakulnukit, Peter
- Kremer, Daniel
- Casuscelli, Jozefina
- Tang, Jie
- Schultz, Nikolaus
- Dong, Yiyu
- Su, Wenjing
- Cheng, Emily H
- Russo, Paul
- Coleman, Jonathan A
- Papaemmanuil, Elli
- Chen, Ying-Bei
- Reuter, Victor E
- Sander, Chris
- Kennedy, Scott R
- Hsieh, James J
- Lyssiotis, Costas A
- Tickoo, Satish K
- Hakimi, A Ari
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2019-04-01
- Volume
- 8
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC6459676
- OpenAlex
- W2933385111
- Cited by
- 43
- References
- 56
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 5 · 2023: 5 · 2022: 4 · 2021: 11 · 2020: 10 · 2019: 4
- FWCI
- 2.29
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Digital Commons@Becker (Washington University School of Medicine) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Open access LMU (Ludwid Maxmilian's Universitat Munchen) (submittedVersion, cc-by)
- Funders
- Damon Runyon Cancer Research Foundation (Dale F. Frey Award for Breakthrough Scientists, DFS-09-14)
- V Foundation for Cancer Research (Junior Scholar Award, V2016-009)
- Sidney Kimmel Foundation for Cancer Research (Kimmel Scholar Award, SKF-16-005)
- National Institutes of Health (DK097153)
- Charles Woodson Research Fund
- The UM Pediatric Brain Tumor Initiative
- University of Michigan (Program in Chemical Biology - Graduate Assistance in Areas of National Need (GAANN) award)
- National Cancer Institute (P30 CA008748, P30 CA046592)
- American Urological Association (Research Scholar Award)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Renal cell carcinoma treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
- Keywords
- clear cell papillary renal cell carcinoma, oxidative stress, mitochondrial DNA depletion, mitochondrial dysfunction, respiratory metabolism, sorbitol accumulation, glycogen, lipid depletion, cancer metabolism
- MeSH terms
- Aerobiosis, Carcinoma, Renal Cell, Histocytochemistry, Humans, Immunohistochemistry, Kidney Neoplasms, Oxidation-Reduction, Cell Respiration, Metabolic Networks and Pathways
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
