Clinical response to azacitidine in MDS is associated with distinct DNA methylation changes in HSPCs

J Julie A. I. Thoms F Feng Yan (Materials Science and Engineering Program, School for Engineering of Matter, Transport and Energy) H Henry R. Hampton S Sarah Davidson S Swapna Joshi J Jesslyn Saw C Chowdhury H. Sarowar X Xin Ying Lim A Andrea C. Nunez P Purvi M. Kakadia G Golam Sarower Bhuyan X Xiaoheng Zou M Mary Nguyen E Elaheh S. Ghodousi F Forrest C. Koch F Fatemeh Vafaee I I. Richard Thompson M Mohammad M. Karimi R Russell Pickford (Bioanalytical Mass Spectrometry Facility, Mark Wainwright Analytical Centre) M Mark J. Raftery S Sally Hough G Griselda Buckland M Michelle Bailey Y Yuvaraj Ghodke N Noorul Absar L Lachlin Vaughan L Leonardo Pasalic C Chun Y. Fong M Melita Kenealy (Cabrini Hospital, Malvern, VIC, Australia) D Devendra K. Hiwase R Rohanna I. Stoddart S Soma Mohammed L Linda Lee F Freda H. Passam (Haematology Research Group, Charles Perkins Centre) S Stephen R. Larsen K Kevin J. Spring K Kristen K. Skarratt P Patricia Rebeiro P Peter Presgrave W William S. Stevenson S Silvia Ling C Campbell Tiley S Stephen J. Fuller F Fernando Roncolato A Anoop K. Enjeti D Dirk Hoenemann C Charlotte Lemech C Christopher J. Jolly S Stefan K. Bohlander D David J. Curtis (Clinical Haematology, Alfred Health, Melbourne, VIC, Australia) J Jason W. H. Wong A Ashwin Unnikrishnan M Mark Hertzberg J Jake Olivier M Mark N. Polizzotto J John E. Pimanda

Abstract

Abstract Hypomethylating agents are frontline therapies for myelodysplastic neoplasms (MDS), yet clinical responses remain unpredictable. We conducted a phase 2 trial comparing injectable and oral azacitidine (AZA) administered over one or three weeks per four-week cycle, with the primary objective of investigating whether response is linked to in vivo drug incorporation or DNA hypomethylation. Our findings show that injection results in higher drug incorporation, but lower DNA demethylation per cycle, while global DNA methylation levels in mononuclear cells are comparable between responders and non-responders. However, hematopoietic stem and progenitor cells (HSPCs) from responders exhibit distinct baseline and early treatment-induced CpG methylation changes at regulatory regions linked to tissue patterning, cell migration, and myeloid differentiation. By cycle six—when clinical responses typically emerge—further differential hypomethylation in responder HSPCs suggests marrow adaptation as a driver of improved hematopoiesis. These findings indicate that intrinsic baseline and early drug-induced epigenetic differences in HSPCs may underlie the variable clinical response to AZA in MDS.

Article Details

Volume / Issue Vol. 16, Issue 1
Published May 13, 2025
ISSN 2041-1723
Publisher Nature Portfolio

Journal Info

Nature Communications

Nature Portfolio

ISSN: 2041-1723 Open Access Life Sciences

Authors (56)

J

Julie A. I. Thoms

F

Feng Yan

Materials Science and Engineering Program, School for Engineering of Matter, Transport and Energy

H

Henry R. Hampton

S

Sarah Davidson

S

Swapna Joshi

J

Jesslyn Saw

C

Chowdhury H. Sarowar

X

Xin Ying Lim

A

Andrea C. Nunez

P

Purvi M. Kakadia

G

Golam Sarower Bhuyan

X

Xiaoheng Zou

M

Mary Nguyen

E

Elaheh S. Ghodousi

F

Forrest C. Koch

F

Fatemeh Vafaee

I

I. Richard Thompson

M

Mohammad M. Karimi

R

Russell Pickford

Bioanalytical Mass Spectrometry Facility, Mark Wainwright Analytical Centre

M

Mark J. Raftery

S

Sally Hough

G

Griselda Buckland

M

Michelle Bailey

Y

Yuvaraj Ghodke

N

Noorul Absar

L

Lachlin Vaughan

L

Leonardo Pasalic

C

Chun Y. Fong

M

Melita Kenealy

Cabrini Hospital, Malvern, VIC, Australia

D

Devendra K. Hiwase

R

Rohanna I. Stoddart

S

Soma Mohammed

L

Linda Lee

F

Freda H. Passam

Haematology Research Group, Charles Perkins Centre

S

Stephen R. Larsen

K

Kevin J. Spring

K

Kristen K. Skarratt

P

Patricia Rebeiro

P

Peter Presgrave

W

William S. Stevenson

S

Silvia Ling

C

Campbell Tiley

S

Stephen J. Fuller

F

Fernando Roncolato

A

Anoop K. Enjeti

D

Dirk Hoenemann

C

Charlotte Lemech

C

Christopher J. Jolly

S

Stefan K. Bohlander

D

David J. Curtis

Clinical Haematology, Alfred Health, Melbourne, VIC, Australia

J

Jason W. H. Wong

A

Ashwin Unnikrishnan

M

Mark Hertzberg

J

Jake Olivier

M

Mark N. Polizzotto

J

John E. Pimanda