Tumor cell-based liquid biopsy using high-throughput microfluidic enrichment of entire leukapheresis product

A Avanish Mishra (Center for Engineering in Medicine and Surgery, Massachusetts General Hospital and Harvard Medical School) S Shih-Bo Huang (Krantz Family Center for Cancer Research, Massachusetts General Hospital Cancer Center and Harvard Medical School) T Taronish Dubash R Risa Burr (Krantz Family Center for Cancer Research, Massachusetts General Hospital, Harvard Medical School) J Jon F. Edd (Center for Engineering in Medicine and Surgery, Massachusetts General Hospital and Harvard Medical School) B Ben S. Wittner Q Quinn E. Cunneely V Victor R. Putaturo A Akansha Deshpande E Ezgi Antmen (Krantz Family Center for Cancer Research, Massachusetts General Hospital Cancer Center and Harvard Medical School) K Kaustav A. Gopinathan (Center for Engineering in Medicine and Surgery, Massachusetts General Hospital and Harvard Medical School) K Keisuke Otani Y Yoshiyuki Miyazawa J Ji Eun Kwak (Krantz Family Center for Cancer Research, Massachusetts General Hospital Cancer Center and Harvard Medical School) S Sara Y. Guay J Justin Kelly (Krantz Family Center for Cancer Research, Massachusetts General Hospital Cancer Center and Harvard Medical School) J John Walsh (Center for Engineering in Medicine and Surgery, Massachusetts General Hospital and Harvard Medical School) L Linda T. Nieman I Isabella Galler P PuiYee Chan M Michael S. Lawrence R Ryan J. Sullivan (Massachusetts General Hospital Cancer Center Boston Massachusetts USA) A Aditya Bardia D Douglas S. Micalizzi (Krantz Family Center for Cancer Research, Massachusetts General Hospital Cancer Center and Harvard Medical School) L Lecia V. Sequist R Richard J. Lee J Joseph W. Franses D David T. Ting P Patricia A. R. Brunker S Shyamala Maheswaran D David T. Miyamoto D Daniel A. Haber M Mehmet Toner

Abstract

AbstractCirculating Tumor Cells (CTCs) in blood encompass DNA, RNA, and protein biomarkers, but clinical utility is limited by their rarity. To enable tumor epitope-agnostic interrogation of large blood volumes, we developed a high-throughput microfluidic device, depleting hematopoietic cells through high-flow channels and force-amplifying magnetic lenses. Here, we apply this technology to analyze patient-derived leukapheresis products, interrogating a mean blood volume of 5.83 liters from seven patients with metastatic cancer. High CTC yields (mean 10,057 CTCs per patient; range 100 to 58,125) reveal considerable intra-patient heterogeneity. CTC size varies within patients, with 67% overlapping in diameter with WBCs. Paired single-cell DNA and RNA sequencing identifies subclonal patterns of aneuploidy and distinct signaling pathways within CTCs. In prostate cancers, a subpopulation of small aneuploid cells lacking epithelial markers is enriched for neuroendocrine signatures. Pooling of CNV-confirmed CTCs enables whole exome sequencing with high mutant allele fractions. High-throughput CTC enrichment thus enables cell-based liquid biopsy for comprehensive monitoring of cancer.

Article Details

Volume / Issue Vol. 16, Issue 1
Published January 02, 2025
ISSN 2041-1723
Publisher Nature Portfolio

Journal Info

Nature Communications

Nature Portfolio

ISSN: 2041-1723 Open Access Life Sciences

Authors (33)

A

Avanish Mishra

Center for Engineering in Medicine and Surgery, Massachusetts General Hospital and Harvard Medical School

S

Shih-Bo Huang

Krantz Family Center for Cancer Research, Massachusetts General Hospital Cancer Center and Harvard Medical School

T

Taronish Dubash

R

Risa Burr

Krantz Family Center for Cancer Research, Massachusetts General Hospital, Harvard Medical School

J

Jon F. Edd

Center for Engineering in Medicine and Surgery, Massachusetts General Hospital and Harvard Medical School

B

Ben S. Wittner

Q

Quinn E. Cunneely

V

Victor R. Putaturo

A

Akansha Deshpande

E

Ezgi Antmen

Krantz Family Center for Cancer Research, Massachusetts General Hospital Cancer Center and Harvard Medical School

K

Kaustav A. Gopinathan

Center for Engineering in Medicine and Surgery, Massachusetts General Hospital and Harvard Medical School

K

Keisuke Otani

Y

Yoshiyuki Miyazawa

J

Ji Eun Kwak

Krantz Family Center for Cancer Research, Massachusetts General Hospital Cancer Center and Harvard Medical School

S

Sara Y. Guay

J

Justin Kelly

Krantz Family Center for Cancer Research, Massachusetts General Hospital Cancer Center and Harvard Medical School

J

John Walsh

Center for Engineering in Medicine and Surgery, Massachusetts General Hospital and Harvard Medical School

L

Linda T. Nieman

I

Isabella Galler

P

PuiYee Chan

M

Michael S. Lawrence

R

Ryan J. Sullivan

Massachusetts General Hospital Cancer Center Boston Massachusetts USA

A

Aditya Bardia

D

Douglas S. Micalizzi

Krantz Family Center for Cancer Research, Massachusetts General Hospital Cancer Center and Harvard Medical School

L

Lecia V. Sequist

R

Richard J. Lee

J

Joseph W. Franses

D

David T. Ting

P

Patricia A. R. Brunker

S

Shyamala Maheswaran

D

David T. Miyamoto

D

Daniel A. Haber

M

Mehmet Toner