Multiomics analysis unveils the cellular ecosystem with clinical relevance in aldosterone-producing adenomas with <i>KCNJ5</i> mutations

M Maki Yokomoto-Umakoshi (Department of Medicine and Bioregulatory Science, Graduate School of Medical Sciences, Kyushu University) M Masamichi Fujita (Department of Medicine and Bioregulatory Science, Graduate School of Medical Sciences, Kyushu University) H Hironobu Umakoshi (Department of Medicine and Bioregulatory Science, Graduate School of Medical Sciences, Kyushu University) T Tatsuki Ogasawara (Department of Medicine and Bioregulatory Science, Graduate School of Medical Sciences, Kyushu University) N Norifusa Iwahashi (Department of Medicine and Bioregulatory Science, Graduate School of Medical Sciences, Kyushu University) K Kohta Nakatani (Division of Metabolomics, Medical Research Center for High Depth Omics, Medical Institute of Bioregulation, Kyushu University) H Hiroki Kaneko (Department of Medicine and Bioregulatory Science, Graduate School of Medical Sciences, Kyushu University) T Tazuru Fukumoto (Department of Medicine and Bioregulatory Science, Graduate School of Medical Sciences, Kyushu University) H Hiroshi Nakao (Department of Medicine and Bioregulatory Science, Graduate School of Medical Sciences, Kyushu University) S Shojiro Haji (Department of Medicine and Bioregulatory Science, Graduate School of Medical Sciences, Kyushu University) N Namiko Kawamura (Department of Medicine and Bioregulatory Science, Graduate School of Medical Sciences, Kyushu University) S Shuichi Shimma (Department of Biotechnology, Graduate School of Engineering, Osaka University) M Masahide Seki (Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, The University of Tokyo) Y Yutaka Suzuki Y Yoshihiro Izumi (Division of Metabolomics, Medical Research Center for High Depth Omics, Medical Institute of Bioregulation, Kyushu University) Y Yoshinao Oda (Department of Anatomic Pathology, Graduate School of Medical Sciences, Kyushu University) M Masatoshi Eto (Department of Urology, Graduate School of Medical Sciences, Kyushu University) S Seishi Ogawa T Takeshi Bamba Y Yoshihiro Ogawa (Department of Medicine and Bioregulatory Science, Graduate School of Medical Sciences, Kyushu University)

Abstract

Aldosterone-producing adenomas (APA), a major endocrine tumor and leading subtype of primary aldosteronism, cause secondary hypertension with high cardiometabolic risks. Despite potentially producing multiple steroid hormones, detailed cellular mechanisms in APA remain insufficiently studied. Our multiomics analysis focusing on APA with KCNJ5 mutations, which represent the most common genetic form, revealed marked cellular heterogeneity. Tumor cell reprogramming initiated from stress-responsive cells to aldosterone-producing or cortisol-producing cells, with the latter progressing to proliferative stromal-like cells. These cell subtypes showed spatial segregation, and APA exhibited genomic intratumor heterogeneity. Among the nonparenchymal cells, lipid-associated macrophages, which were abundant in APA, might promote the progression of cortisol-producing and stromal-like cells, suggesting their role in the tumor microenvironment. Intratumor cortisol synthesis was correlated with increased blood cortisol levels, which were associated with the development of vertebral fractures, a hallmark of osteoporosis. This study unveils the complex cellular ecosystem with clinical relevance in APA with KCNJ5 mutations, providing insights into tumor biology that could inform future clinical approaches.

Article Details

Volume / Issue Vol. 122, Issue 9
Published March 04, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (20)

M

Maki Yokomoto-Umakoshi

Department of Medicine and Bioregulatory Science, Graduate School of Medical Sciences, Kyushu University

M

Masamichi Fujita

Department of Medicine and Bioregulatory Science, Graduate School of Medical Sciences, Kyushu University

H

Hironobu Umakoshi

Department of Medicine and Bioregulatory Science, Graduate School of Medical Sciences, Kyushu University

T

Tatsuki Ogasawara

Department of Medicine and Bioregulatory Science, Graduate School of Medical Sciences, Kyushu University

N

Norifusa Iwahashi

Department of Medicine and Bioregulatory Science, Graduate School of Medical Sciences, Kyushu University

K

Kohta Nakatani

Division of Metabolomics, Medical Research Center for High Depth Omics, Medical Institute of Bioregulation, Kyushu University

H

Hiroki Kaneko

Department of Medicine and Bioregulatory Science, Graduate School of Medical Sciences, Kyushu University

T

Tazuru Fukumoto

Department of Medicine and Bioregulatory Science, Graduate School of Medical Sciences, Kyushu University

H

Hiroshi Nakao

Department of Medicine and Bioregulatory Science, Graduate School of Medical Sciences, Kyushu University

S

Shojiro Haji

Department of Medicine and Bioregulatory Science, Graduate School of Medical Sciences, Kyushu University

N

Namiko Kawamura

Department of Medicine and Bioregulatory Science, Graduate School of Medical Sciences, Kyushu University

S

Shuichi Shimma

Department of Biotechnology, Graduate School of Engineering, Osaka University

M

Masahide Seki

Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, The University of Tokyo

Y

Yutaka Suzuki

Y

Yoshihiro Izumi

Division of Metabolomics, Medical Research Center for High Depth Omics, Medical Institute of Bioregulation, Kyushu University

Y

Yoshinao Oda

Department of Anatomic Pathology, Graduate School of Medical Sciences, Kyushu University

M

Masatoshi Eto

Department of Urology, Graduate School of Medical Sciences, Kyushu University

S

Seishi Ogawa

T

Takeshi Bamba

Y

Yoshihiro Ogawa

Department of Medicine and Bioregulatory Science, Graduate School of Medical Sciences, Kyushu University