Glioma progression is shaped by genetic evolution and microenvironment interactions

The GLASS Consortium; Frederick S. Varn; Kevin C. Johnson; Jan Martinek; Jason T. Huse; MacLean P. Nasrallah; Pieter Wesseling; Lee A.D. Cooper; Tathiane M. Malta; Taylor E. Wade; Thais S. Sabedot; Daniel Brat; Peter V. Gould; Adelheid Wöehrer; Kenneth Aldape; Azzam Ismail; Santhosh K. Sivajothi; Floris P. Barthel; Hoon Kim; Emre Kocakavuk; Nazia Ahmed; Kieron White; Indrani Datta; Hyo Eun Moon; Steven Pollock; Christine Goldfarb; Ga Hyun Lee; Luciano Garofano; Kevin J. Anderson; Djamel Nehar-Belaid; Jill S. Barnholtz-Sloan; Spyridon Bakas; Annette T. Byrne; Fulvio D'Angelo; Hui K. Gan; Mustafa Khasraw; Annemiek M.E. Walenkamp

doi:10.1016/j.cell.2022.04.038

Glioma progression is shaped by genetic evolution and microenvironment interactions

The GLASS Consortium, Frederick S. Varn, Kevin C. Johnson, Jan Martinek, Jason T. Huse, MacLean P. Nasrallah, Pieter Wesseling, Lee A.D. Cooper, Tathiane M. Malta, Taylor E. Wade, Thais S. Sabedot, Daniel Brat, Peter V. Gould, Adelheid Wöehrer, Kenneth Aldape, Azzam Ismail, Santhosh K. Sivajothi, Floris P. Barthel, Hoon Kim, Emre KocakavukNazia Ahmed, Kieron White, Indrani Datta, Hyo Eun Moon, Steven Pollock, Christine Goldfarb, Ga Hyun Lee, Luciano Garofano, Kevin J. Anderson, Djamel Nehar-Belaid, Jill S. Barnholtz-Sloan, Spyridon Bakas, Annette T. Byrne, Fulvio D'Angelo, Hui K. Gan, Mustafa Khasraw, Annemiek M.E. Walenkamp

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

232 Citations (Scopus)

Abstract

The factors driving therapy resistance in diffuse glioma remain poorly understood. To identify treatment-associated cellular and genetic changes, we analyzed RNA and/or DNA sequencing data from the temporally separated tumor pairs of 304 adult patients with isocitrate dehydrogenase (IDH)-wild-type and IDH-mutant glioma. Tumors recurred in distinct manners that were dependent on IDH mutation status and attributable to changes in histological feature composition, somatic alterations, and microenvironment interactions. Hypermutation and acquired CDKN2A deletions were associated with an increase in proliferating neoplastic cells at recurrence in both glioma subtypes, reflecting active tumor growth. IDH-wild-type tumors were more invasive at recurrence, and their neoplastic cells exhibited increased expression of neuronal signaling programs that reflected a possible role for neuronal interactions in promoting glioma progression. Mesenchymal transition was associated with the presence of a myeloid cell state defined by specific ligand-receptor interactions with neoplastic cells. Collectively, these recurrence-associated phenotypes represent potential targets to alter disease progression.

Original language	English
Pages (from-to)	2184-2199.e16
Journal	Cell
Volume	185
Issue number	12
DOIs	https://doi.org/10.1016/j.cell.2022.04.038
Publication status	Published - 9 Jun 2022

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10.1016/j.cell.2022.04.038

https://hdl.handle.net/11370/e3b32466-daf0-4c8a-ae94-c4a1133d9a1bLicence: Article 25fa Dutch Copyright Act

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The GLASS Consortium, Varn, F. S., Johnson, K. C., Martinek, J., Huse, J. T., Nasrallah, M. P., Wesseling, P., Cooper, L. A. D., Malta, T. M., Wade, T. E., Sabedot, T. S., Brat, D., Gould, P. V., Wöehrer, A., Aldape, K., Ismail, A., Sivajothi, S. K., Barthel, F. P., Kim, H., ... Walenkamp, A. M. E. (2022). Glioma progression is shaped by genetic evolution and microenvironment interactions. Cell, 185(12), 2184-2199.e16. https://doi.org/10.1016/j.cell.2022.04.038

@article{2097e9eaab84467e8b825c356deddadd,

title = "Glioma progression is shaped by genetic evolution and microenvironment interactions",

abstract = "The factors driving therapy resistance in diffuse glioma remain poorly understood. To identify treatment-associated cellular and genetic changes, we analyzed RNA and/or DNA sequencing data from the temporally separated tumor pairs of 304 adult patients with isocitrate dehydrogenase (IDH)-wild-type and IDH-mutant glioma. Tumors recurred in distinct manners that were dependent on IDH mutation status and attributable to changes in histological feature composition, somatic alterations, and microenvironment interactions. Hypermutation and acquired CDKN2A deletions were associated with an increase in proliferating neoplastic cells at recurrence in both glioma subtypes, reflecting active tumor growth. IDH-wild-type tumors were more invasive at recurrence, and their neoplastic cells exhibited increased expression of neuronal signaling programs that reflected a possible role for neuronal interactions in promoting glioma progression. Mesenchymal transition was associated with the presence of a myeloid cell state defined by specific ligand-receptor interactions with neoplastic cells. Collectively, these recurrence-associated phenotypes represent potential targets to alter disease progression.",

author = "{The GLASS Consortium} and Varn, {Frederick S.} and Johnson, {Kevin C.} and Jan Martinek and Huse, {Jason T.} and Nasrallah, {MacLean P.} and Pieter Wesseling and Cooper, {Lee A.D.} and Malta, {Tathiane M.} and Wade, {Taylor E.} and Sabedot, {Thais S.} and Daniel Brat and Gould, {Peter V.} and Adelheid W{\"o}ehrer and Kenneth Aldape and Azzam Ismail and Sivajothi, {Santhosh K.} and Barthel, {Floris P.} and Hoon Kim and Emre Kocakavuk and Nazia Ahmed and Kieron White and Indrani Datta and Moon, {Hyo Eun} and Steven Pollock and Christine Goldfarb and Lee, {Ga Hyun} and Luciano Garofano and Anderson, {Kevin J.} and Djamel Nehar-Belaid and Barnholtz-Sloan, {Jill S.} and Spyridon Bakas and Byrne, {Annette T.} and Fulvio D'Angelo and Gan, {Hui K.} and Mustafa Khasraw and Simona Migliozzi and Ormond, {D. Ryan} and Paek, {Sun Ha} and {Van Meir}, {Erwin G.} and Walenkamp, {Annemiek M.E.} and Colin Watts and Tobias Weiss and Michael Weller and Karolina Palucka and Stead, {Lucy F.} and Poisson, {Laila M.} and French, {Pim J.} and Kouwenhoven, {Mathilde CM} and {Sillevis Smitt}, Peter and Marion Smits",

note = "Publisher Copyright: {\textcopyright} 2022 Elsevier Inc.",

year = "2022",

month = jun,

day = "9",

doi = "10.1016/j.cell.2022.04.038",

language = "English",

volume = "185",

pages = "2184--2199.e16",

journal = "Cell",

issn = "0092-8674",

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number = "12",

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The GLASS Consortium, Varn, FS, Johnson, KC, Martinek, J, Huse, JT, Nasrallah, MP, Wesseling, P, Cooper, LAD, Malta, TM, Wade, TE, Sabedot, TS, Brat, D, Gould, PV, Wöehrer, A, Aldape, K, Ismail, A, Sivajothi, SK, Barthel, FP, Kim, H, Kocakavuk, E, Ahmed, N, White, K, Datta, I, Moon, HE, Pollock, S, Goldfarb, C, Lee, GH, Garofano, L, Anderson, KJ, Nehar-Belaid, D, Barnholtz-Sloan, JS, Bakas, S, Byrne, AT, D'Angelo, F, Gan, HK, Khasraw, M & Walenkamp, AME 2022, 'Glioma progression is shaped by genetic evolution and microenvironment interactions', Cell, vol. 185, no. 12, pp. 2184-2199.e16. https://doi.org/10.1016/j.cell.2022.04.038

TY - JOUR

T1 - Glioma progression is shaped by genetic evolution and microenvironment interactions

AU - The GLASS Consortium

AU - Varn, Frederick S.

AU - Johnson, Kevin C.

AU - Martinek, Jan

AU - Huse, Jason T.

AU - Nasrallah, MacLean P.

AU - Wesseling, Pieter

AU - Cooper, Lee A.D.

AU - Malta, Tathiane M.

AU - Wade, Taylor E.

AU - Sabedot, Thais S.

AU - Brat, Daniel

AU - Gould, Peter V.

AU - Wöehrer, Adelheid

AU - Aldape, Kenneth

AU - Ismail, Azzam

AU - Sivajothi, Santhosh K.

AU - Barthel, Floris P.

AU - Kim, Hoon

AU - Kocakavuk, Emre

AU - Ahmed, Nazia

AU - White, Kieron

AU - Datta, Indrani

AU - Moon, Hyo Eun

AU - Pollock, Steven

AU - Goldfarb, Christine

AU - Lee, Ga Hyun

AU - Garofano, Luciano

AU - Anderson, Kevin J.

AU - Nehar-Belaid, Djamel

AU - Barnholtz-Sloan, Jill S.

AU - Bakas, Spyridon

AU - Byrne, Annette T.

AU - D'Angelo, Fulvio

AU - Gan, Hui K.

AU - Khasraw, Mustafa

AU - Migliozzi, Simona

AU - Ormond, D. Ryan

AU - Paek, Sun Ha

AU - Van Meir, Erwin G.

AU - Walenkamp, Annemiek M.E.

AU - Watts, Colin

AU - Weiss, Tobias

AU - Weller, Michael

AU - Palucka, Karolina

AU - Stead, Lucy F.

AU - Poisson, Laila M.

AU - French, Pim J.

AU - Kouwenhoven, Mathilde CM

AU - Sillevis Smitt, Peter

AU - Smits, Marion

PY - 2022/6/9

Y1 - 2022/6/9

N2 - The factors driving therapy resistance in diffuse glioma remain poorly understood. To identify treatment-associated cellular and genetic changes, we analyzed RNA and/or DNA sequencing data from the temporally separated tumor pairs of 304 adult patients with isocitrate dehydrogenase (IDH)-wild-type and IDH-mutant glioma. Tumors recurred in distinct manners that were dependent on IDH mutation status and attributable to changes in histological feature composition, somatic alterations, and microenvironment interactions. Hypermutation and acquired CDKN2A deletions were associated with an increase in proliferating neoplastic cells at recurrence in both glioma subtypes, reflecting active tumor growth. IDH-wild-type tumors were more invasive at recurrence, and their neoplastic cells exhibited increased expression of neuronal signaling programs that reflected a possible role for neuronal interactions in promoting glioma progression. Mesenchymal transition was associated with the presence of a myeloid cell state defined by specific ligand-receptor interactions with neoplastic cells. Collectively, these recurrence-associated phenotypes represent potential targets to alter disease progression.

AB - The factors driving therapy resistance in diffuse glioma remain poorly understood. To identify treatment-associated cellular and genetic changes, we analyzed RNA and/or DNA sequencing data from the temporally separated tumor pairs of 304 adult patients with isocitrate dehydrogenase (IDH)-wild-type and IDH-mutant glioma. Tumors recurred in distinct manners that were dependent on IDH mutation status and attributable to changes in histological feature composition, somatic alterations, and microenvironment interactions. Hypermutation and acquired CDKN2A deletions were associated with an increase in proliferating neoplastic cells at recurrence in both glioma subtypes, reflecting active tumor growth. IDH-wild-type tumors were more invasive at recurrence, and their neoplastic cells exhibited increased expression of neuronal signaling programs that reflected a possible role for neuronal interactions in promoting glioma progression. Mesenchymal transition was associated with the presence of a myeloid cell state defined by specific ligand-receptor interactions with neoplastic cells. Collectively, these recurrence-associated phenotypes represent potential targets to alter disease progression.

UR - http://www.scopus.com/inward/record.url?scp=85131903367&partnerID=8YFLogxK

U2 - 10.1016/j.cell.2022.04.038

DO - 10.1016/j.cell.2022.04.038

M3 - Article

C2 - 35649412

AN - SCOPUS:85131903367

SN - 0092-8674

VL - 185

SP - 2184-2199.e16

JO - Cell

JF - Cell

IS - 12

ER -

Glioma progression is shaped by genetic evolution and microenvironment interactions

Abstract

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