IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-44886-z.html
   My bibliography  Save this article

WNT-dependent interaction between inflammatory fibroblasts and FOLR2+ macrophages promotes fibrosis in chronic kidney disease

Author

Listed:
  • Camille Cohen

    (PSL Research University
    Inserm, U830)

  • Rana Mhaidly

    (PSL Research University
    Inserm, U830)

  • Hugo Croizer

    (PSL Research University
    Inserm, U830)

  • Yann Kieffer

    (PSL Research University
    Inserm, U830)

  • Renaud Leclere

    (Institut Curie Hospital Group)

  • Anne Vincent-Salomon

    (Institut Curie Hospital Group)

  • Catherine Robley

    (PSL Research University
    Inserm, U830)

  • Dany Anglicheau

    (Paris Cité University, Inserm U1151)

  • Marion Rabant

    (Paris Cité University)

  • Aurélie Sannier

    (Paris Cité University, Inserm, U1148)

  • Marc-Olivier Timsit

    (Paris Cité University)

  • Sean Eddy

    (University of Michigan)

  • Matthias Kretzler

    (University of Michigan
    University of Michigan)

  • Wenjun Ju

    (University of Michigan
    University of Michigan)

  • Fatima Mechta-Grigoriou

    (PSL Research University
    Inserm, U830)

Abstract

Chronic kidney disease (CKD) is a public health problem driven by myofibroblast accumulation, leading to interstitial fibrosis. Heterogeneity is a recently recognized characteristic in kidney fibroblasts in CKD, but the role of different populations is still unclear. Here, we characterize a proinflammatory fibroblast population (named CXCL-iFibro), which corresponds to an early state of myofibroblast differentiation in CKD. We demonstrate that CXCL-iFibro co-localize with macrophages in the kidney and participate in their attraction, accumulation, and switch into FOLR2+ macrophages from early CKD stages on. In vitro, macrophages promote the switch of CXCL-iFibro into ECM-secreting myofibroblasts through a WNT/β-catenin-dependent pathway, thereby suggesting a reciprocal crosstalk between these populations of fibroblasts and macrophages. Finally, the detection of CXCL-iFibro at early stages of CKD is predictive of poor patient prognosis, which shows that the CXCL-iFibro population is an early player in CKD progression and demonstrates the clinical relevance of our findings.

Suggested Citation

  • Camille Cohen & Rana Mhaidly & Hugo Croizer & Yann Kieffer & Renaud Leclere & Anne Vincent-Salomon & Catherine Robley & Dany Anglicheau & Marion Rabant & Aurélie Sannier & Marc-Olivier Timsit & Sean E, 2024. "WNT-dependent interaction between inflammatory fibroblasts and FOLR2+ macrophages promotes fibrosis in chronic kidney disease," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-44886-z
    DOI: 10.1038/s41467-024-44886-z
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-44886-z
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-44886-z?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Floriane Pelon & Brigitte Bourachot & Yann Kieffer & Ilaria Magagna & Fanny Mermet-Meillon & Isabelle Bonnet & Ana Costa & Anne-Marie Givel & Youmna Attieh & Jorge Barbazan & Claire Bonneau & Laetitia, 2020. "Cancer-associated fibroblast heterogeneity in axillary lymph nodes drives metastases in breast cancer through complementary mechanisms," Nature Communications, Nature, vol. 11(1), pages 1-20, December.
    2. Han Luo & Xuyang Xia & Li-Bin Huang & Hyunsu An & Minyuan Cao & Gyeong Dae Kim & Hai-Ning Chen & Wei-Han Zhang & Yang Shu & Xiangyu Kong & Zhixiang Ren & Pei-Heng Li & Yang Liu & Huairong Tang & Rongh, 2022. "Pan-cancer single-cell analysis reveals the heterogeneity and plasticity of cancer-associated fibroblasts in the tumor microenvironment," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    3. María Casanova-Acebes & Erica Dalla & Andrew M. Leader & Jessica LeBerichel & Jovan Nikolic & Blanca M. Morales & Markus Brown & Christie Chang & Leanna Troncoso & Steven T. Chen & Ana Sastre-Perona &, 2021. "Tissue-resident macrophages provide a pro-tumorigenic niche to early NSCLC cells," Nature, Nature, vol. 595(7868), pages 578-584, July.
    4. Subhrajit Saha & Evelyn Aranda & Yoku Hayakawa & Payel Bhanja & Safinur Atay & N Patrik Brodin & Jiufeng Li & Samuel Asfaha & Laibin Liu & Yagnesh Tailor & Jinghang Zhang & Andrew K. Godwin & Wolfgang, 2016. "Macrophage-derived extracellular vesicle-packaged WNTs rescue intestinal stem cells and enhance survival after radiation injury," Nature Communications, Nature, vol. 7(1), pages 1-16, December.
    5. Michael Bartoschek & Nikolay Oskolkov & Matteo Bocci & John Lövrot & Christer Larsson & Mikael Sommarin & Chris D. Madsen & David Lindgren & Gyula Pekar & Göran Karlsson & Markus Ringnér & Jonas Bergh, 2018. "Spatially and functionally distinct subclasses of breast cancer-associated fibroblasts revealed by single cell RNA sequencing," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    6. Christoph Kuppe & Ricardo O. Ramirez Flores & Zhijian Li & Sikander Hayat & Rebecca T. Levinson & Xian Liao & Monica T. Hannani & Jovan Tanevski & Florian Wünnemann & James S. Nagai & Maurice Halder &, 2022. "Spatial multi-omic map of human myocardial infarction," Nature, Nature, vol. 608(7924), pages 766-777, August.
    7. Anne-Marie Givel & Yann Kieffer & Alix Scholer-Dahirel & Philemon Sirven & Melissa Cardon & Floriane Pelon & Ilaria Magagna & Géraldine Gentric & Ana Costa & Claire Bonneau & Virginie Mieulet & Anne V, 2018. "miR200-regulated CXCL12β promotes fibroblast heterogeneity and immunosuppression in ovarian cancers," Nature Communications, Nature, vol. 9(1), pages 1-20, December.
    8. Yoshiharu Muto & Eryn E. Dixon & Yasuhiro Yoshimura & Haojia Wu & Kohei Omachi & Nicolas Ledru & Parker C. Wilson & Andrew J. King & N. Eric Olson & Marvin G. Gunawan & Jay J. Kuo & Jennifer H. Cox & , 2022. "Defining cellular complexity in human autosomal dominant polycystic kidney disease by multimodal single cell analysis," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    9. Neil C. Henderson & Florian Rieder & Thomas A. Wynn, 2020. "Fibrosis: from mechanisms to medicines," Nature, Nature, vol. 587(7835), pages 555-566, November.
    10. Junyue Cao & Malte Spielmann & Xiaojie Qiu & Xingfan Huang & Daniel M. Ibrahim & Andrew J. Hill & Fan Zhang & Stefan Mundlos & Lena Christiansen & Frank J. Steemers & Cole Trapnell & Jay Shendure, 2019. "The single-cell transcriptional landscape of mammalian organogenesis," Nature, Nature, vol. 566(7745), pages 496-502, February.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Agnes Forsthuber & Bertram Aschenbrenner & Ana Korosec & Tina Jacob & Karl Annusver & Natalia Krajic & Daria Kholodniuk & Sophie Frech & Shaohua Zhu & Kim Purkhauser & Katharina Lipp & Franziska Werne, 2024. "Cancer-associated fibroblast subtypes modulate the tumor-immune microenvironment and are associated with skin cancer malignancy," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    2. Lena Cords & Sandra Tietscher & Tobias Anzeneder & Claus Langwieder & Martin Rees & Natalie Souza & Bernd Bodenmiller, 2023. "Cancer-associated fibroblast classification in single-cell and spatial proteomics data," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    3. Hugo Croizer & Rana Mhaidly & Yann Kieffer & Geraldine Gentric & Lounes Djerroudi & Renaud Leclere & Floriane Pelon & Catherine Robley & Mylene Bohec & Arnaud Meng & Didier Meseure & Emanuela Romano &, 2024. "Deciphering the spatial landscape and plasticity of immunosuppressive fibroblasts in breast cancer," Nature Communications, Nature, vol. 15(1), pages 1-28, December.
    4. Julia M. Houthuijzen & Roebi Bruijn & Eline Burg & Anne Paulien Drenth & Ellen Wientjens & Tamara Filipovic & Esme Bullock & Chiara S. Brambillasca & Emilia M. Pulver & Marja Nieuwland & Iris Rink & F, 2023. "CD26-negative and CD26-positive tissue-resident fibroblasts contribute to functionally distinct CAF subpopulations in breast cancer," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    5. Luc Francis & Daniel McCluskey & Clarisse Ganier & Treasa Jiang & Xinyi Du-Harpur & Jeyrroy Gabriel & Pawan Dhami & Yogesh Kamra & Sudha Visvanathan & Jonathan N. Barker & Catherine H. Smith & Frances, 2024. "Single-cell analysis of psoriasis resolution demonstrates an inflammatory fibroblast state targeted by IL-23 blockade," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    6. Z. L. Liu & X. Y. Meng & R. J. Bao & M. Y. Shen & J. J. Sun & W. D. Chen & F. Liu & Y. He, 2024. "Single cell deciphering of progression trajectories of the tumor ecosystem in head and neck cancer," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    7. Chen-Rui Xia & Zhi-Jie Cao & Xin-Ming Tu & Ge Gao, 2023. "Spatial-linked alignment tool (SLAT) for aligning heterogenous slices," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    8. Swetha Anandhan & Shelley Herbrich & Sangeeta Goswami & Baoxiang Guan & Yulong Chen & Marc Daniel Macaluso & Sonali Jindal & Seanu Meena Natarajan & Samuel W. Andrewes & Liangwen Xiong & Ashwat Nagara, 2024. "TSG-6+ cancer-associated fibroblasts modulate myeloid cell responses and impair anti-tumor response to immune checkpoint therapy in pancreatic cancer," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    9. Monika Licaj & Rana Mhaidly & Yann Kieffer & Hugo Croizer & Claire Bonneau & Arnaud Meng & Lounes Djerroudi & Kevin Mujangi-Ebeka & Hocine R. Hocine & Brigitte Bourachot & Ilaria Magagna & Renaud Lecl, 2024. "Residual ANTXR1+ myofibroblasts after chemotherapy inhibit anti-tumor immunity via YAP1 signaling pathway," Nature Communications, Nature, vol. 15(1), pages 1-27, December.
    10. Irfete S. Fetahu & Wolfgang Esser-Skala & Rohit Dnyansagar & Samuel Sindelar & Fikret Rifatbegovic & Andrea Bileck & Lukas Skos & Eva Bozsaky & Daria Lazic & Lisa Shaw & Marcus Tötzl & Dora Tarlungean, 2023. "Single-cell transcriptomics and epigenomics unravel the role of monocytes in neuroblastoma bone marrow metastasis," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    11. Eun-Jung Kang & Jae-Hoon Kim & Young Eun Kim & Hana Lee & Kwang Bo Jung & Dong-Ho Chang & Youngjin Lee & Shinhye Park & Eun-Young Lee & Eun-Ji Lee & Ho Bum Kang & Moon-Young Rhyoo & Seungwoo Seo & Soh, 2024. "The secreted protein Amuc_1409 from Akkermansia muciniphila improves gut health through intestinal stem cell regulation," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    12. Sivakamasundari Vijayakumar & Roberta Sala & Gugene Kang & Angela Chen & Michelle Ann Pablo & Abidemi Ismail Adebayo & Andrea Cipriano & Jonas L. Fowler & Danielle L. Gomes & Lay Teng Ang & Kyle M. Lo, 2023. "Monolayer platform to generate and purify primordial germ-like cells in vitro provides insights into human germline specification," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    13. Brian DeVeale & Leqian Liu & Ryan Boileau & Jennifer Swindlehurst-Chan & Bryan Marsh & Jacob W. Freimer & Adam Abate & Robert Blelloch, 2022. "G1/S restriction point coordinates phasic gene expression and cell differentiation," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    14. Yasuaki Uehara & Yusuke Tanaka & Shuyang Zhao & Nikolaos M. Nikolaidis & Lori B. Pitstick & Huixing Wu & Jane J. Yu & Erik Zhang & Yoshihiro Hasegawa & John G. Noel & Jason C. Gardner & Elizabeth J. K, 2023. "Insights into pulmonary phosphate homeostasis and osteoclastogenesis emerge from the study of pulmonary alveolar microlithiasis," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    15. J. McClatchy & R. Strogantsev & E. Wolfe & H. Y. Lin & M. Mohammadhosseini & B. A. Davis & C. Eden & D. Goldman & W. H. Fleming & P. Conley & G. Wu & L. Cimmino & H. Mohammed & A. Agarwal, 2023. "Clonal hematopoiesis related TET2 loss-of-function impedes IL1β-mediated epigenetic reprogramming in hematopoietic stem and progenitor cells," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    16. Ci Fu & Xiang Zhang & Amanda O. Veri & Kali R. Iyer & Emma Lash & Alice Xue & Huijuan Yan & Nicole M. Revie & Cassandra Wong & Zhen-Yuan Lin & Elizabeth J. Polvi & Sean D. Liston & Benjamin VanderSlui, 2021. "Leveraging machine learning essentiality predictions and chemogenomic interactions to identify antifungal targets," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    17. Junyi Chen & Xiaoying Wang & Anjun Ma & Qi-En Wang & Bingqiang Liu & Lang Li & Dong Xu & Qin Ma, 2022. "Deep transfer learning of cancer drug responses by integrating bulk and single-cell RNA-seq data," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    18. Kotaro Shimizu & Junichi Kikuta & Yumi Ohta & Yutaka Uchida & Yu Miyamoto & Akito Morimoto & Shinya Yari & Takashi Sato & Takefumi Kamakura & Kazuo Oshima & Ryusuke Imai & Yu-Chen Liu & Daisuke Okuzak, 2023. "Single-cell transcriptomics of human cholesteatoma identifies an activin A-producing osteoclastogenic fibroblast subset inducing bone destruction," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    19. Young Hee Lee & Yu-Been Kim & Kyu Sik Kim & Mirae Jang & Ha Young Song & Sang-Ho Jung & Dong-Soo Ha & Joon Seok Park & Jaegeon Lee & Kyung Min Kim & Deok-Hyeon Cheon & Inhyeok Baek & Min-Gi Shin & Eun, 2023. "Lateral hypothalamic leptin receptor neurons drive hunger-gated food-seeking and consummatory behaviours in male mice," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    20. Sandra Curras-Alonso & Juliette Soulier & Thomas Defard & Christian Weber & Sophie Heinrich & Hugo Laporte & Sophie Leboucher & Sonia Lameiras & Marie Dutreix & Vincent Favaudon & Florian Massip & Tho, 2023. "An interactive murine single-cell atlas of the lung responses to radiation injury," Nature Communications, Nature, vol. 14(1), pages 1-16, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-44886-z. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.