Comprehensive proteogenomic characterization of rare kidney tumors

Clinical Proteomic Tumor Analysis Consortium; Ginny Xiaohe Li; Lijun Chen; Yi Hsiao; Rahul Mannan; Yuping Zhang; Jie Luo; Francesca Petralia; Hanbyul Cho; Noshad Hosseini; Felipe da Veiga Leprevost; Anna Calinawan; Yize Li; Shankara Anand; Aniket Dagar; Yifat Geffen; Chandan Kumar-Sinha; Seema Chugh; Anne Le; Sean Ponce; Shenghao Guo; Cissy Zhang; Michael Schnaubelt; Nataly Naser Al Deen; Feng Chen; Wagma Caravan; Andrew Houston; Alex Hopkins; Chelsea J. Newton; Xiaoming Wang; Daniel A. Polasky; Sarah Haynes; Fengchao Yu; Xiaojun Jing; Siqi Chen; Ana I. Robles; Mehdi Mesri; Mathangi Thiagarajan; Eunkyung An; Gad A. Getz; W. Marston Linehan; Galen Hostetter; Scott D. Jewell; Daniel W. Chan; Pei Wang; Gilbert S. Omenn; Rohit Mehra; Christopher J. Ricketts; Li Ding; Arul M. Chinnaiyan; Marcin P. Cieslik; Saravana M. Dhanasekaran; Hui Zhang; Alexey I. Nesvizhskii; Alexander J. Lazar; Amanda G. Paulovich; Andrzej Antczak; Anthony Green; Avi Ma'ayan; Barb Pruetz; Bing Zhang; Boris Reva; Brian J. Druker; Charles A. Goldthwaite; Chet Birger; D. R. Mani; David Chesla; David Fenyö; Eric E. Schadt; George Wilson; Iga Kołodziejczak; Ivy John; Jason Hafron; Josh Vo; Kakhaber Zaalishvili; Karen A. Ketchum; Karin D. Rodland; Kristen Nyce; Maciej Wiznerowicz; Marcin J. Domagalski; Meenakshi Anurag; Melissa Borucki; Michael A. Gillette; Michael J. Birrer; Nathan J. Edwards; Negin Vatanian; Pamela VanderKolk; Peter B. McGarvey; Rajiv Dhir; Ratna R. Thangudu; Reese Crispen; Richard D. Smith; Samuel H. Payne; Sandra Cottingham; Shuang Cai; Steven A. Carr; Tao Liu; Toan Le; Weiping Ma; Xu Zhang; Yin Lu; Yvonne Shutack; Zhen Zhang

doi:10.1016/j.xcrm.2024.101547

Comprehensive proteogenomic characterization of rare kidney tumors

Clinical Proteomic Tumor Analysis Consortium, Ginny Xiaohe Li, Lijun Chen, Yi Hsiao, Rahul Mannan, Yuping Zhang, Jie Luo, Francesca Petralia, Hanbyul Cho, Noshad Hosseini, Felipe da Veiga Leprevost, Anna Calinawan, Yize Li, Shankara Anand, Aniket Dagar, Yifat Geffen, Chandan Kumar-Sinha, Seema Chugh, Anne Le, Sean PonceShenghao Guo, Cissy Zhang, Michael Schnaubelt, Nataly Naser Al Deen, Feng Chen, Wagma Caravan, Andrew Houston, Alex Hopkins, Chelsea J. Newton, Xiaoming Wang, Daniel A. Polasky, Sarah Haynes, Fengchao Yu, Xiaojun Jing, Siqi Chen, Ana I. Robles, Mehdi Mesri, Mathangi Thiagarajan, Eunkyung An, Gad A. Getz, W. Marston Linehan, Galen Hostetter, Scott D. Jewell, Daniel W. Chan, Pei Wang, Gilbert S. Omenn, Rohit Mehra, Christopher J. Ricketts, Li Ding, Arul M. Chinnaiyan, Marcin P. Cieslik, Saravana M. Dhanasekaran, Hui Zhang, Alexey I. Nesvizhskii, Alexander J. Lazar, Amanda G. Paulovich, Andrzej Antczak, Anthony Green, Avi Ma'ayan, Barb Pruetz, Bing Zhang, Boris Reva, Brian J. Druker, Charles A. Goldthwaite, Chet Birger, D. R. Mani, David Chesla, David Fenyö, Eric E. Schadt, George Wilson, Iga Kołodziejczak, Ivy John, Jason Hafron, Josh Vo, Kakhaber Zaalishvili, Karen A. Ketchum, Karin D. Rodland, Kristen Nyce, Maciej Wiznerowicz, Marcin J. Domagalski, Meenakshi Anurag, Melissa Borucki, Michael A. Gillette, Michael J. Birrer, Nathan J. Edwards, Negin Vatanian, Pamela VanderKolk, Peter B. McGarvey, Rajiv Dhir, Ratna R. Thangudu, Reese Crispen, Richard D. Smith, Samuel H. Payne, Sandra Cottingham, Shuang Cai, Steven A. Carr, Tao Liu, Toan Le, Weiping Ma, Xu Zhang, Yin Lu, Yvonne Shutack, Zhen Zhang

Research output: Contribution to journal › Article › peer-review

4 Scopus citations

Abstract

Non-clear cell renal cell carcinomas (non-ccRCCs) encompass diverse malignant and benign tumors. Refinement of differential diagnosis biomarkers, markers for early prognosis of aggressive disease, and therapeutic targets to complement immunotherapy are current clinical needs. Multi-omics analyses of 48 non-ccRCCs compared with 103 ccRCCs reveal proteogenomic, phosphorylation, glycosylation, and metabolic aberrations in RCC subtypes. RCCs with high genome instability display overexpression of IGF2BP3 and PYCR1. Integration of single-cell and bulk transcriptome data predicts diverse cell-of-origin and clarifies RCC subtype-specific proteogenomic signatures. Expression of biomarkers MAPRE3, ADGRF5, and GPNMB differentiates renal oncocytoma from chromophobe RCC, and PIGR and SOSTDC1 distinguish papillary RCC from MTSCC. This study expands our knowledge of proteogenomic signatures, biomarkers, and potential therapeutic targets in non-ccRCC.

Original language	English
Article number	101547
Journal	Cell Reports Medicine
Volume	5
Issue number	5
DOIs	https://doi.org/10.1016/j.xcrm.2024.101547
State	Published - May 21 2024

Keywords

CPTAC
cell-of-origin
differential diagnosis biomarkers
glycoproteomics
metabolomics
non-clear cell renal cell carcinoma
phosphoproteomics
prognostic marker
proteogenomics
weighted genome instability index

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10.1016/j.xcrm.2024.101547

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Clinical Proteomic Tumor Analysis Consortium, Li, G. X., Chen, L., Hsiao, Y., Mannan, R., Zhang, Y., Luo, J., Petralia, F., Cho, H., Hosseini, N., Leprevost, F. D. V., Calinawan, A., Li, Y., Anand, S., Dagar, A., Geffen, Y., Kumar-Sinha, C., Chugh, S., Le, A., ... Zhang, Z. (2024). Comprehensive proteogenomic characterization of rare kidney tumors. Cell Reports Medicine, 5(5), Article 101547. https://doi.org/10.1016/j.xcrm.2024.101547

@article{5a4f8de942114c0ea5f557f6b05178f5,

title = "Comprehensive proteogenomic characterization of rare kidney tumors",

abstract = "Non-clear cell renal cell carcinomas (non-ccRCCs) encompass diverse malignant and benign tumors. Refinement of differential diagnosis biomarkers, markers for early prognosis of aggressive disease, and therapeutic targets to complement immunotherapy are current clinical needs. Multi-omics analyses of 48 non-ccRCCs compared with 103 ccRCCs reveal proteogenomic, phosphorylation, glycosylation, and metabolic aberrations in RCC subtypes. RCCs with high genome instability display overexpression of IGF2BP3 and PYCR1. Integration of single-cell and bulk transcriptome data predicts diverse cell-of-origin and clarifies RCC subtype-specific proteogenomic signatures. Expression of biomarkers MAPRE3, ADGRF5, and GPNMB differentiates renal oncocytoma from chromophobe RCC, and PIGR and SOSTDC1 distinguish papillary RCC from MTSCC. This study expands our knowledge of proteogenomic signatures, biomarkers, and potential therapeutic targets in non-ccRCC.",

keywords = "CPTAC, cell-of-origin, differential diagnosis biomarkers, glycoproteomics, metabolomics, non-clear cell renal cell carcinoma, phosphoproteomics, prognostic marker, proteogenomics, weighted genome instability index",

author = "{Clinical Proteomic Tumor Analysis Consortium} and Li, {Ginny Xiaohe} and Lijun Chen and Yi Hsiao and Rahul Mannan and Yuping Zhang and Jie Luo and Francesca Petralia and Hanbyul Cho and Noshad Hosseini and Leprevost, {Felipe da Veiga} and Anna Calinawan and Yize Li and Shankara Anand and Aniket Dagar and Yifat Geffen and Chandan Kumar-Sinha and Seema Chugh and Anne Le and Sean Ponce and Shenghao Guo and Cissy Zhang and Michael Schnaubelt and {Al Deen}, {Nataly Naser} and Feng Chen and Wagma Caravan and Andrew Houston and Alex Hopkins and Newton, {Chelsea J.} and Xiaoming Wang and Polasky, {Daniel A.} and Sarah Haynes and Fengchao Yu and Xiaojun Jing and Siqi Chen and Robles, {Ana I.} and Mehdi Mesri and Mathangi Thiagarajan and Eunkyung An and Getz, {Gad A.} and Linehan, {W. Marston} and Galen Hostetter and Jewell, {Scott D.} and Chan, {Daniel W.} and Pei Wang and Omenn, {Gilbert S.} and Rohit Mehra and Ricketts, {Christopher J.} and Li Ding and Chinnaiyan, {Arul M.} and Cieslik, {Marcin P.} and Dhanasekaran, {Saravana M.} and Hui Zhang and Nesvizhskii, {Alexey I.} and Lazar, {Alexander J.} and Paulovich, {Amanda G.} and Andrzej Antczak and Anthony Green and Avi Ma'ayan and Barb Pruetz and Bing Zhang and Boris Reva and Druker, {Brian J.} and Goldthwaite, {Charles A.} and Chet Birger and Mani, {D. R.} and David Chesla and David Feny{\"o} and Schadt, {Eric E.} and George Wilson and Iga Ko{\l}odziejczak and Ivy John and Jason Hafron and Josh Vo and Kakhaber Zaalishvili and Ketchum, {Karen A.} and Rodland, {Karin D.} and Kristen Nyce and Maciej Wiznerowicz and Domagalski, {Marcin J.} and Meenakshi Anurag and Melissa Borucki and Gillette, {Michael A.} and Birrer, {Michael J.} and Edwards, {Nathan J.} and Negin Vatanian and Pamela VanderKolk and McGarvey, {Peter B.} and Rajiv Dhir and Thangudu, {Ratna R.} and Reese Crispen and Smith, {Richard D.} and Payne, {Samuel H.} and Sandra Cottingham and Shuang Cai and Carr, {Steven A.} and Tao Liu and Toan Le and Weiping Ma and Xu Zhang and Yin Lu and Yvonne Shutack and Zhen Zhang",

note = "Publisher Copyright: {\textcopyright} 2024 The Author(s)",

year = "2024",

month = may,

day = "21",

doi = "10.1016/j.xcrm.2024.101547",

language = "English",

volume = "5",

journal = "Cell Reports Medicine",

issn = "2666-3791",

number = "5",

}

Clinical Proteomic Tumor Analysis Consortium, Li, GX, Chen, L, Hsiao, Y, Mannan, R, Zhang, Y, Luo, J, Petralia, F, Cho, H, Hosseini, N, Leprevost, FDV, Calinawan, A, Li, Y, Anand, S, Dagar, A, Geffen, Y, Kumar-Sinha, C, Chugh, S, Le, A, Ponce, S, Guo, S, Zhang, C, Schnaubelt, M, Al Deen, NN, Chen, F, Caravan, W, Houston, A, Hopkins, A, Newton, CJ, Wang, X, Polasky, DA, Haynes, S, Yu, F, Jing, X, Chen, S, Robles, AI, Mesri, M, Thiagarajan, M, An, E, Getz, GA, Linehan, WM, Hostetter, G, Jewell, SD, Chan, DW, Wang, P, Omenn, GS, Mehra, R, Ricketts, CJ, Ding, L, Chinnaiyan, AM, Cieslik, MP, Dhanasekaran, SM, Zhang, H, Nesvizhskii, AI, Lazar, AJ, Paulovich, AG, Antczak, A, Green, A, Ma'ayan, A, Pruetz, B, Zhang, B, Reva, B, Druker, BJ, Goldthwaite, CA, Birger, C, Mani, DR, Chesla, D, Fenyö, D, Schadt, EE, Wilson, G, Kołodziejczak, I, John, I, Hafron, J, Vo, J, Zaalishvili, K, Ketchum, KA, Rodland, KD, Nyce, K, Wiznerowicz, M, Domagalski, MJ, Anurag, M, Borucki, M, Gillette, MA, Birrer, MJ, Edwards, NJ, Vatanian, N, VanderKolk, P, McGarvey, PB, Dhir, R, Thangudu, RR, Crispen, R, Smith, RD, Payne, SH, Cottingham, S, Cai, S, Carr, SA, Liu, T, Le, T, Ma, W, Zhang, X, Lu, Y, Shutack, Y & Zhang, Z 2024, 'Comprehensive proteogenomic characterization of rare kidney tumors', Cell Reports Medicine, vol. 5, no. 5, 101547. https://doi.org/10.1016/j.xcrm.2024.101547

TY - JOUR

T1 - Comprehensive proteogenomic characterization of rare kidney tumors

AU - Clinical Proteomic Tumor Analysis Consortium

AU - Li, Ginny Xiaohe

AU - Chen, Lijun

AU - Hsiao, Yi

AU - Mannan, Rahul

AU - Zhang, Yuping

AU - Luo, Jie

AU - Petralia, Francesca

AU - Cho, Hanbyul

AU - Hosseini, Noshad

AU - Leprevost, Felipe da Veiga

AU - Calinawan, Anna

AU - Li, Yize

AU - Anand, Shankara

AU - Dagar, Aniket

AU - Geffen, Yifat

AU - Kumar-Sinha, Chandan

AU - Chugh, Seema

AU - Le, Anne

AU - Ponce, Sean

AU - Guo, Shenghao

AU - Zhang, Cissy

AU - Schnaubelt, Michael

AU - Al Deen, Nataly Naser

AU - Chen, Feng

AU - Caravan, Wagma

AU - Houston, Andrew

AU - Hopkins, Alex

AU - Newton, Chelsea J.

AU - Wang, Xiaoming

AU - Polasky, Daniel A.

AU - Haynes, Sarah

AU - Yu, Fengchao

AU - Jing, Xiaojun

AU - Chen, Siqi

AU - Robles, Ana I.

AU - Mesri, Mehdi

AU - Thiagarajan, Mathangi

AU - An, Eunkyung

AU - Getz, Gad A.

AU - Linehan, W. Marston

AU - Hostetter, Galen

AU - Jewell, Scott D.

AU - Chan, Daniel W.

AU - Wang, Pei

AU - Omenn, Gilbert S.

AU - Mehra, Rohit

AU - Ricketts, Christopher J.

AU - Ding, Li

AU - Chinnaiyan, Arul M.

AU - Cieslik, Marcin P.

AU - Dhanasekaran, Saravana M.

AU - Zhang, Hui

AU - Nesvizhskii, Alexey I.

AU - Lazar, Alexander J.

AU - Paulovich, Amanda G.

AU - Antczak, Andrzej

AU - Green, Anthony

AU - Ma'ayan, Avi

AU - Pruetz, Barb

AU - Zhang, Bing

AU - Reva, Boris

AU - Druker, Brian J.

AU - Goldthwaite, Charles A.

AU - Birger, Chet

AU - Mani, D. R.

AU - Chesla, David

AU - Fenyö, David

AU - Schadt, Eric E.

AU - Wilson, George

AU - Kołodziejczak, Iga

AU - John, Ivy

AU - Hafron, Jason

AU - Vo, Josh

AU - Zaalishvili, Kakhaber

AU - Ketchum, Karen A.

AU - Rodland, Karin D.

AU - Nyce, Kristen

AU - Wiznerowicz, Maciej

AU - Domagalski, Marcin J.

AU - Anurag, Meenakshi

AU - Borucki, Melissa

AU - Gillette, Michael A.

AU - Birrer, Michael J.

AU - Edwards, Nathan J.

AU - Vatanian, Negin

AU - VanderKolk, Pamela

AU - McGarvey, Peter B.

AU - Dhir, Rajiv

AU - Thangudu, Ratna R.

AU - Crispen, Reese

AU - Smith, Richard D.

AU - Payne, Samuel H.

AU - Cottingham, Sandra

AU - Cai, Shuang

AU - Carr, Steven A.

AU - Liu, Tao

AU - Le, Toan

AU - Ma, Weiping

AU - Zhang, Xu

AU - Lu, Yin

AU - Shutack, Yvonne

AU - Zhang, Zhen

PY - 2024/5/21

Y1 - 2024/5/21

N2 - Non-clear cell renal cell carcinomas (non-ccRCCs) encompass diverse malignant and benign tumors. Refinement of differential diagnosis biomarkers, markers for early prognosis of aggressive disease, and therapeutic targets to complement immunotherapy are current clinical needs. Multi-omics analyses of 48 non-ccRCCs compared with 103 ccRCCs reveal proteogenomic, phosphorylation, glycosylation, and metabolic aberrations in RCC subtypes. RCCs with high genome instability display overexpression of IGF2BP3 and PYCR1. Integration of single-cell and bulk transcriptome data predicts diverse cell-of-origin and clarifies RCC subtype-specific proteogenomic signatures. Expression of biomarkers MAPRE3, ADGRF5, and GPNMB differentiates renal oncocytoma from chromophobe RCC, and PIGR and SOSTDC1 distinguish papillary RCC from MTSCC. This study expands our knowledge of proteogenomic signatures, biomarkers, and potential therapeutic targets in non-ccRCC.

AB - Non-clear cell renal cell carcinomas (non-ccRCCs) encompass diverse malignant and benign tumors. Refinement of differential diagnosis biomarkers, markers for early prognosis of aggressive disease, and therapeutic targets to complement immunotherapy are current clinical needs. Multi-omics analyses of 48 non-ccRCCs compared with 103 ccRCCs reveal proteogenomic, phosphorylation, glycosylation, and metabolic aberrations in RCC subtypes. RCCs with high genome instability display overexpression of IGF2BP3 and PYCR1. Integration of single-cell and bulk transcriptome data predicts diverse cell-of-origin and clarifies RCC subtype-specific proteogenomic signatures. Expression of biomarkers MAPRE3, ADGRF5, and GPNMB differentiates renal oncocytoma from chromophobe RCC, and PIGR and SOSTDC1 distinguish papillary RCC from MTSCC. This study expands our knowledge of proteogenomic signatures, biomarkers, and potential therapeutic targets in non-ccRCC.

KW - CPTAC

KW - cell-of-origin

KW - differential diagnosis biomarkers

KW - glycoproteomics

KW - metabolomics

KW - non-clear cell renal cell carcinoma

KW - phosphoproteomics

KW - prognostic marker

KW - proteogenomics

KW - weighted genome instability index

UR - http://www.scopus.com/inward/record.url?scp=85193218690&partnerID=8YFLogxK

U2 - 10.1016/j.xcrm.2024.101547

DO - 10.1016/j.xcrm.2024.101547

M3 - Article

C2 - 38703764

AN - SCOPUS:85193218690

SN - 2666-3791

VL - 5

JO - Cell Reports Medicine

JF - Cell Reports Medicine

IS - 5

M1 - 101547

ER -

Comprehensive proteogenomic characterization of rare kidney tumors

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Keywords

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