Alterations in ALK/ROS1/NTRK/MET drive a group of infantile hemispheric gliomas

Ana S. Guerreiro Stucklin; Scott Ryall; Kohei Fukuoka; Michal Zapotocky; Alvaro Lassaletta; Christopher Li; Taylor Bridge; Byungjin Kim; Anthony Arnoldo; Paul E. Kowalski; Yvonne Zhong; Monique Johnson; Claire Li; Arun K. Ramani; Robert Siddaway; Liana Figueiredo Nobre; Pasqualino de Antonellis; Christopher Dunham; Sylvia Cheng; Daniel R. Boué; Jonathan L. Finlay; Scott L. Coven; Inmaculada de Prada; Marta Perez-Somarriba; Claudia C. Faria; Michael A. Grotzer; Elisabeth Rushing; David Sumerauer; Josef Zamecnik; Lenka Krskova; Miguel Garcia Ariza; Ofelia Cruz; Andres Morales La Madrid; Palma Solano; Keita Terashima; Yoshiko Nakano; Koichi Ichimura; Motoo Nagane; Hiroaki Sakamoto; Maria Joao Gil-da-Costa; Roberto Silva; Donna L. Johnston; Jean Michaud; Bev Wilson; Frank K.H. van Landeghem; Angelica Oviedo; P. Daniel McNeely; Bruce Crooks; Iris Fried; Nataliya Zhukova; Jordan R. Hansford; Amulya Nageswararao; Livia Garzia; Mary Shago; Michael Brudno; Meredith S. Irwin; Ute Bartels; Vijay Ramaswamy; Eric Bouffet; Michael D. Taylor; Uri Tabori; Cynthia Hawkins

doi:10.1038/s41467-019-12187-5

Alterations in ALK/ROS1/NTRK/MET drive a group of infantile hemispheric gliomas

Ana S. Guerreiro Stucklin, Scott Ryall, Kohei Fukuoka, Michal Zapotocky, Alvaro Lassaletta, Christopher Li, Taylor Bridge, Byungjin Kim, Anthony Arnoldo, Paul E. Kowalski, Yvonne Zhong, Monique Johnson, Claire Li, Arun K. Ramani, Robert Siddaway, Liana Figueiredo Nobre, Pasqualino de Antonellis, Christopher Dunham, Sylvia Cheng, Daniel R. BouéJonathan L. Finlay, Scott L. Coven, Inmaculada de Prada, Marta Perez-Somarriba, Claudia C. Faria, Michael A. Grotzer, Elisabeth Rushing, David Sumerauer, Josef Zamecnik, Lenka Krskova, Miguel Garcia Ariza, Ofelia Cruz, Andres Morales La Madrid, Palma Solano, Keita Terashima, Yoshiko Nakano, Koichi Ichimura, Motoo Nagane, Hiroaki Sakamoto, Maria Joao Gil-da-Costa, Roberto Silva, Donna L. Johnston, Jean Michaud, Bev Wilson, Frank K.H. van Landeghem, Angelica Oviedo, P. Daniel McNeely, Bruce Crooks, Iris Fried, Nataliya Zhukova, Jordan R. Hansford, Amulya Nageswararao, Livia Garzia, Mary Shago, Michael Brudno, Meredith S. Irwin, Ute Bartels, Vijay Ramaswamy, Eric Bouffet, Michael D. Taylor, Uri Tabori, Cynthia Hawkins

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Abstract

Infant gliomas have paradoxical clinical behavior compared to those in children and adults: low-grade tumors have a higher mortality rate, while high-grade tumors have a better outcome. However, we have little understanding of their biology and therefore cannot explain this behavior nor what constitutes optimal clinical management. Here we report a comprehensive genetic analysis of an international cohort of clinically annotated infant gliomas, revealing 3 clinical subgroups. Group 1 tumors arise in the cerebral hemispheres and harbor alterations in the receptor tyrosine kinases ALK, ROS1, NTRK and MET. These are typically single-events and confer an intermediate outcome. Groups 2 and 3 gliomas harbor RAS/MAPK pathway mutations and arise in the hemispheres and midline, respectively. Group 2 tumors have excellent long-term survival, while group 3 tumors progress rapidly and do not respond well to chemoradiation. We conclude that infant gliomas comprise 3 subgroups, justifying the need for specialized therapeutic strategies.

Original language	English
Article number	4343
Number of pages	13
Journal	Nature Communications
Volume	10
Issue number	1
DOIs	https://doi.org/10.1038/s41467-019-12187-5
Publication status	Published - 1 Dec 2019
Externally published	Yes

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300178965-oaFinal published version, 2.69 MBLicence: CC BY

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Guerreiro Stucklin, A. S., Ryall, S., Fukuoka, K., Zapotocky, M., Lassaletta, A., Li, C., Bridge, T., Kim, B., Arnoldo, A., Kowalski, P. E., Zhong, Y., Johnson, M., Li, C., Ramani, A. K., Siddaway, R., Nobre, L. F., de Antonellis, P., Dunham, C., Cheng, S., ... Hawkins, C. (2019). Alterations in ALK/ROS1/NTRK/MET drive a group of infantile hemispheric gliomas. Nature Communications, 10(1), Article 4343. https://doi.org/10.1038/s41467-019-12187-5

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abstract = "Infant gliomas have paradoxical clinical behavior compared to those in children and adults: low-grade tumors have a higher mortality rate, while high-grade tumors have a better outcome. However, we have little understanding of their biology and therefore cannot explain this behavior nor what constitutes optimal clinical management. Here we report a comprehensive genetic analysis of an international cohort of clinically annotated infant gliomas, revealing 3 clinical subgroups. Group 1 tumors arise in the cerebral hemispheres and harbor alterations in the receptor tyrosine kinases ALK, ROS1, NTRK and MET. These are typically single-events and confer an intermediate outcome. Groups 2 and 3 gliomas harbor RAS/MAPK pathway mutations and arise in the hemispheres and midline, respectively. Group 2 tumors have excellent long-term survival, while group 3 tumors progress rapidly and do not respond well to chemoradiation. We conclude that infant gliomas comprise 3 subgroups, justifying the need for specialized therapeutic strategies.",

author = "{Guerreiro Stucklin}, {Ana S.} and Scott Ryall and Kohei Fukuoka and Michal Zapotocky and Alvaro Lassaletta and Christopher Li and Taylor Bridge and Byungjin Kim and Anthony Arnoldo and Kowalski, {Paul E.} and Yvonne Zhong and Monique Johnson and Claire Li and Ramani, {Arun K.} and Robert Siddaway and Nobre, {Liana Figueiredo} and {de Antonellis}, Pasqualino and Christopher Dunham and Sylvia Cheng and Bou{\'e}, {Daniel R.} and Finlay, {Jonathan L.} and Coven, {Scott L.} and {de Prada}, Inmaculada and Marta Perez-Somarriba and Faria, {Claudia C.} and Grotzer, {Michael A.} and Elisabeth Rushing and David Sumerauer and Josef Zamecnik and Lenka Krskova and {Garcia Ariza}, Miguel and Ofelia Cruz and {Morales La Madrid}, Andres and Palma Solano and Keita Terashima and Yoshiko Nakano and Koichi Ichimura and Motoo Nagane and Hiroaki Sakamoto and Gil-da-Costa, {Maria Joao} and Roberto Silva and Johnston, {Donna L.} and Jean Michaud and Bev Wilson and {van Landeghem}, {Frank K.H.} and Angelica Oviedo and McNeely, {P. Daniel} and Bruce Crooks and Iris Fried and Nataliya Zhukova and Hansford, {Jordan R.} and Amulya Nageswararao and Livia Garzia and Mary Shago and Michael Brudno and Irwin, {Meredith S.} and Ute Bartels and Vijay Ramaswamy and Eric Bouffet and Taylor, {Michael D.} and Uri Tabori and Cynthia Hawkins",

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doi = "10.1038/s41467-019-12187-5",

language = "English",

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journal = "Nature Communications",

issn = "2041-1723",

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Guerreiro Stucklin, AS, Ryall, S, Fukuoka, K, Zapotocky, M, Lassaletta, A, Li, C, Bridge, T, Kim, B, Arnoldo, A, Kowalski, PE, Zhong, Y, Johnson, M, Li, C, Ramani, AK, Siddaway, R, Nobre, LF, de Antonellis, P, Dunham, C, Cheng, S, Boué, DR, Finlay, JL, Coven, SL, de Prada, I, Perez-Somarriba, M, Faria, CC, Grotzer, MA, Rushing, E, Sumerauer, D, Zamecnik, J, Krskova, L, Garcia Ariza, M, Cruz, O, Morales La Madrid, A, Solano, P, Terashima, K, Nakano, Y, Ichimura, K, Nagane, M, Sakamoto, H, Gil-da-Costa, MJ, Silva, R, Johnston, DL, Michaud, J, Wilson, B, van Landeghem, FKH, Oviedo, A, McNeely, PD, Crooks, B, Fried, I, Zhukova, N, Hansford, JR, Nageswararao, A, Garzia, L, Shago, M, Brudno, M, Irwin, MS, Bartels, U, Ramaswamy, V, Bouffet, E, Taylor, MD, Tabori, U & Hawkins, C 2019, 'Alterations in ALK/ROS1/NTRK/MET drive a group of infantile hemispheric gliomas', Nature Communications, vol. 10, no. 1, 4343. https://doi.org/10.1038/s41467-019-12187-5

TY - JOUR

T1 - Alterations in ALK/ROS1/NTRK/MET drive a group of infantile hemispheric gliomas

AU - Guerreiro Stucklin, Ana S.

AU - Ryall, Scott

AU - Fukuoka, Kohei

AU - Zapotocky, Michal

AU - Lassaletta, Alvaro

AU - Li, Christopher

AU - Bridge, Taylor

AU - Kim, Byungjin

AU - Arnoldo, Anthony

AU - Kowalski, Paul E.

AU - Zhong, Yvonne

AU - Johnson, Monique

AU - Li, Claire

AU - Ramani, Arun K.

AU - Siddaway, Robert

AU - Nobre, Liana Figueiredo

AU - de Antonellis, Pasqualino

AU - Dunham, Christopher

AU - Cheng, Sylvia

AU - Boué, Daniel R.

AU - Finlay, Jonathan L.

AU - Coven, Scott L.

AU - de Prada, Inmaculada

AU - Perez-Somarriba, Marta

AU - Faria, Claudia C.

AU - Grotzer, Michael A.

AU - Rushing, Elisabeth

AU - Sumerauer, David

AU - Zamecnik, Josef

AU - Krskova, Lenka

AU - Garcia Ariza, Miguel

AU - Cruz, Ofelia

AU - Morales La Madrid, Andres

AU - Solano, Palma

AU - Terashima, Keita

AU - Nakano, Yoshiko

AU - Ichimura, Koichi

AU - Nagane, Motoo

AU - Sakamoto, Hiroaki

AU - Gil-da-Costa, Maria Joao

AU - Silva, Roberto

AU - Johnston, Donna L.

AU - Michaud, Jean

AU - Wilson, Bev

AU - van Landeghem, Frank K.H.

AU - Oviedo, Angelica

AU - McNeely, P. Daniel

AU - Crooks, Bruce

AU - Fried, Iris

AU - Zhukova, Nataliya

AU - Hansford, Jordan R.

AU - Nageswararao, Amulya

AU - Garzia, Livia

AU - Shago, Mary

AU - Brudno, Michael

AU - Irwin, Meredith S.

AU - Bartels, Ute

AU - Ramaswamy, Vijay

AU - Bouffet, Eric

AU - Taylor, Michael D.

AU - Tabori, Uri

AU - Hawkins, Cynthia

PY - 2019/12/1

Y1 - 2019/12/1

N2 - Infant gliomas have paradoxical clinical behavior compared to those in children and adults: low-grade tumors have a higher mortality rate, while high-grade tumors have a better outcome. However, we have little understanding of their biology and therefore cannot explain this behavior nor what constitutes optimal clinical management. Here we report a comprehensive genetic analysis of an international cohort of clinically annotated infant gliomas, revealing 3 clinical subgroups. Group 1 tumors arise in the cerebral hemispheres and harbor alterations in the receptor tyrosine kinases ALK, ROS1, NTRK and MET. These are typically single-events and confer an intermediate outcome. Groups 2 and 3 gliomas harbor RAS/MAPK pathway mutations and arise in the hemispheres and midline, respectively. Group 2 tumors have excellent long-term survival, while group 3 tumors progress rapidly and do not respond well to chemoradiation. We conclude that infant gliomas comprise 3 subgroups, justifying the need for specialized therapeutic strategies.

AB - Infant gliomas have paradoxical clinical behavior compared to those in children and adults: low-grade tumors have a higher mortality rate, while high-grade tumors have a better outcome. However, we have little understanding of their biology and therefore cannot explain this behavior nor what constitutes optimal clinical management. Here we report a comprehensive genetic analysis of an international cohort of clinically annotated infant gliomas, revealing 3 clinical subgroups. Group 1 tumors arise in the cerebral hemispheres and harbor alterations in the receptor tyrosine kinases ALK, ROS1, NTRK and MET. These are typically single-events and confer an intermediate outcome. Groups 2 and 3 gliomas harbor RAS/MAPK pathway mutations and arise in the hemispheres and midline, respectively. Group 2 tumors have excellent long-term survival, while group 3 tumors progress rapidly and do not respond well to chemoradiation. We conclude that infant gliomas comprise 3 subgroups, justifying the need for specialized therapeutic strategies.

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U2 - 10.1038/s41467-019-12187-5

DO - 10.1038/s41467-019-12187-5

M3 - Article

C2 - 31554817

AN - SCOPUS:85072668903

SN - 2041-1723

VL - 10

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 4343

ER -

Alterations in ALK/ROS1/NTRK/MET drive a group of infantile hemispheric gliomas

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