CRISPR-Cas13d functional transcriptomics reveals widespread isoform-selective cancer dependencies on lncRNAs

E Eugenio Morelli (INOC - Istituto Nazionale Oncologico Candiolo, Candiolo, Italy) A Anil Aktas Samur (Dana Farber Cancer Institution, Boston, Massachusetts, United States) D Domenico Maisano (Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts, United States) C Claire Gao V Vanessa Katia Favasuli (Candiolo Cancer Institute, FPO-IRCCS, Candiolo (TO), Italy) D Dimitrios Papaioannou G Giovanni De Nola (3Massachusetts Institute of Technology, David H. Koch Institute for Integrative Cancer Research, Boston, United States) J Jonathan E Henninger (Whitehead Institute of Biomedical Research, Cambridge, Massachusetts, United States) N Na Liu M Marcello Turi (Candiolo Cancer Institute FPO-IRCCS, Candiolo, Italy) P Pietro Folino (1Dana Farber Cancer Institute, Harvard Medical School, Boston, United States) L Laure Vreux (Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts, United States) M Michela Cumerlato (Department of Medical Oncology, Dana-Farber Cancer Institute, 450 Brookline Avenue, Boston, MA 02215, United States) L Liang Chen I Iannis Aifantis M Mariateresa Fulciniti (Dana Farber Cancer Institute, Boston, Massachusetts, United States) K Kenneth C. Anderson A Abigail KR Lytton-Jean (David H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States) A Annamaria Gulla (Istituto nazionale Oncologico Candiolo INOC, Candiolo, Italy) R Richard Young (Whitehead Institute, Cambridge, Massachusetts, United States) M Mehmet K. Samur (Dana-Farber Cancer Institute and Harvard School of Public Health, Boston, Massachusetts, United States) N Nikhil C. Munshi

Abstract

Long noncoding RNAs (lncRNAs) are a significant yet largely uncharted component of the cancer transcriptome, with their isoform-specific functions remaining poorly understood. In this study, we employed RNA-targeting CRISPR-Cas13d to uncover and characterize hundreds of tumor-essential (te)-lncRNA isoforms with clinical relevance. Focusing on multiple myeloma (MM), we targeted the lncRNA transcriptome expressed in tumor cells from MM patients and revealed both MM-specific and pan-cancer dependencies across diverse cancer cell lines, which we further validated in animal models. Additionally, we mapped the subcellular localization of these te-lncRNAs, identifying over 30 cytosolic isoforms that proved essential when targeted by cytosol-localized Cas13d. Notably, a specific isoform of SNHG6, enriched in the endoplasmic reticulum, interacts with heat shock proteins to maintain cellular proteostasis. We also integrated functional and clinical data into the publicly accessible LongDEP Portal, providing a valuable resource for the research community. Our study offers a comprehensive characterization of te-lncRNAs, underscoring their oncogenic roles and therapeutic potential.

Article Details

Journal Blood
Volume / Issue Vol. 1, Issue 1
Published May 22, 2025
ISSN 0006-4971
Publisher Elsevier BV

Journal Info

Blood

Elsevier BV

ISSN: 0006-4971 Health Sciences

Authors (22)

E

Eugenio Morelli

INOC - Istituto Nazionale Oncologico Candiolo, Candiolo, Italy

A

Anil Aktas Samur

Dana Farber Cancer Institution, Boston, Massachusetts, United States

D

Domenico Maisano

Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts, United States

C

Claire Gao

V

Vanessa Katia Favasuli

Candiolo Cancer Institute, FPO-IRCCS, Candiolo (TO), Italy

D

Dimitrios Papaioannou

G

Giovanni De Nola

3Massachusetts Institute of Technology, David H. Koch Institute for Integrative Cancer Research, Boston, United States

J

Jonathan E Henninger

Whitehead Institute of Biomedical Research, Cambridge, Massachusetts, United States

N

Na Liu

M

Marcello Turi

Candiolo Cancer Institute FPO-IRCCS, Candiolo, Italy

P

Pietro Folino

1Dana Farber Cancer Institute, Harvard Medical School, Boston, United States

L

Laure Vreux

Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts, United States

M

Michela Cumerlato

Department of Medical Oncology, Dana-Farber Cancer Institute, 450 Brookline Avenue, Boston, MA 02215, United States

L

Liang Chen

I

Iannis Aifantis

M

Mariateresa Fulciniti

Dana Farber Cancer Institute, Boston, Massachusetts, United States

K

Kenneth C. Anderson

A

Abigail KR Lytton-Jean

David H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States

A

Annamaria Gulla

Istituto nazionale Oncologico Candiolo INOC, Candiolo, Italy

R

Richard Young

Whitehead Institute, Cambridge, Massachusetts, United States

M

Mehmet K. Samur

Dana-Farber Cancer Institute and Harvard School of Public Health, Boston, Massachusetts, United States

N

Nikhil C. Munshi