The DOI matches its Crossref record; 231 of the 231 references it cites were found in a registry or an index.
Drugging the efferocytosis process: concepts and opportunities
Open accessAbstract
The daily removal of billions of apoptotic cells in the human body via the process of efferocytosis is essential for homeostasis. To allow for this continuous efferocytosis, rapid phenotypic changes occur in the phagocytes enabling them to engulf and digest the apoptotic cargo. In addition, efferocytosis is actively anti-inflammatory and promotes resolution. Owing to its ubiquitous nature and the sheer volume of cell turnover, efferocytosis is a point of vulnerability. Aberrations in efferocytosis are associated with numerous inflammatory pathologies, including atherosclerosis, cancer and infections. The recent exciting discoveries defining the molecular machinery involved in efferocytosis have opened many avenues for therapeutic intervention, with several agents now in clinical trials.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“efferocytosis in other settings can promote fibrosis as part of the tissue resolution process, for example, by secreting TGF-β1 (12, 13).”
From Impaired TIM4-mediated efferocytosis by liver macrophages contributes to fibrosis in metabolic dysfunction–associated steatohepatitis (2025) · cites this paper as [13]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“While some progress has been made with respect to the Fractalkine receptor (CX3C motif chemokine receptor 1), Axl, MerTK, CD47 and Tim4/3, no approaches have thus far been clinically approved (64).”
From Cholesterol efflux protein, ABCA1, supports anticancer functions of myeloid immune cells (2026) · cites this paper as [64]
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“The accumulation of dead cells in disease settings indicates impaired clearance of dead cells by macrophages (“efferocytosis”) (12, 13).”
From Impaired TIM4-mediated efferocytosis by liver macrophages contributes to fibrosis in metabolic dysfunction–associated steatohepatitis (2025) · cites this paper as [13]
The cited source says what the claim attributes to it.
In the citing paper
“Efferocytosis not only prevents dead cell accumulation but also reprograms macrophages to execute tissue resolution functions, and impaired efferocytosis contributes to many human chronic inflammatory diseases (12, 13).”
From Impaired TIM4-mediated efferocytosis by liver macrophages contributes to fibrosis in metabolic dysfunction–associated steatohepatitis (2025) · cites this paper as [13]
The check wasn’t confident either way, so it gives no verdict — never disputed.
In the citing paper
“It is seen as a major hurdle to using antigen presenting cells in cell-based therapies (61–64).”
From Cholesterol efflux protein, ABCA1, supports anticancer functions of myeloid immune cells (2026) · cites this paper as [64]
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
1 retracted
Items 201–231 of 231
Mertk Interacts with Tim-4 to Enhance Tim-4-Mediated Efferocytosis
Moon, B., Lee, J., Lee, S.-A., Min, C., Moon, H., Kim, D., Yang, S., Moon, H., Jeon, J., Joo, Y., et al. (2020) · Cells · doi:10.3390/cells9071625 · Cited by 34
Roohullah, A., Ganju, V., Zhang, F. P. Y., Zhang, L., Yu, T., Wilkinson, K. J., Cooper, A. J., & SOUZA, P. D. (2021) · Journal of Clinical Oncology · doi:10.1200/jco.2021.39.15_suppl.2517 · Cited by 34
Post, S. M., Ma, H., Malaney, P., Zhang, X., Aitken, M. J. L., Mak, P. Y., Ruvolo, V. R., Yasuhiro, T., Kozaki, R., Chan, L. E., et al. (2021) · Haematologica · doi:10.3324/haematol.2021.278369 · Cited by 33
Haddad, F., & Daver, N. G. (2021) · Journal of Immunotherapy and Precision Oncology · doi:10.36401/jipo-21-x2 · Cited by 32
Felip, E., Brunsvig, P. F., Viñolas, N., Ponce-Aix, S., Carcereny, E., Gómez, M. D., Perez, J. M. T., Arriola, E., Campelo, R. G., Spicer, J. F., et al. (2019) · Journal of Clinical Oncology · doi:10.1200/jco.2019.37.15_suppl.9098 · Cited by 31
Burris, H. A., Spira, A. I., Taylor, M. H., Yeku, O., Liu, J. F., Münster, P. N., Hamilton, E. P., Thomas, J. S., Gatlin, F., Penson, R. T., et al. (2021) · Journal of Clinical Oncology · doi:10.1200/jco.2021.39.15_suppl.2516 · Cited by 31
Context-dependent compensation among phosphatidylserine-recognition receptors
Penberthy, K. K., Rival, C., Shankman, L. S., Raymond, M. H., Zhang, J., Perry, J. S. A., Lee, C. S., Han, C. Z., Onengut-Gumuscu, S., Palczewski, K., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-15191-1 · Cited by 30
Self-citationZhen, Y., Lee, I. J., Finkelman, F. D., & Shao, W.-H. (2018) · Journal of Autoimmunity · doi:10.1016/j.jaut.2018.06.001 · Cited by 29
Mita, M. M., Gordon, M. S., Rosen, L. S., Kapoor, N., Choy, G. S., Redkar, S., Taverna, P., Oganesian, A., Sahai, A., Azab, M., et al. (2014) · Cancer Chemotherapy and Pharmacology · doi:10.1007/s00280-014-2481-1 · Cited by 28
Manega, C. M., Fiorelli, S., Porro, B., Turnu, L., Cavalca, V., Bonomi, A., Cosentino, N., Minno, A. D., Marenzi, G., Tremoli, E., et al. (2019) · Pharmacological Research · doi:10.1016/j.phrs.2019.03.012 · Cited by 28
ROCK Inhibition Drives Resolution of Acute Inflammation by Enhancing Neutrophil Apoptosis
Galvão, I., Athayde, R. M., Perez, D., Reis, A. C., Rezende, L., de Oliveira, V. L. S., Rezende, B. M., Gonçalves, W. A., Sousa, L. P., Teixeira, M. M., et al. (2019) · Cells · doi:10.3390/cells8090964 · Cited by 28
Tibes, R., Fine, G. D., Choy, G. S., Redkar, S., Taverna, P., Oganesian, A., Sahai, A., Azab, M., & Tolcher, A. W. (2012) · Cancer Chemotherapy and Pharmacology · doi:10.1007/s00280-012-2019-3 · Cited by 27
Zeidan, A. M., Esteve, J., Giagounidis, A. A. N., Kim, H., Miyazaki, Y., Platzbecker, U., Schuh, A. C., Sekeres, M. A., Westermann, J., Xiao, Z., et al. (2020) · Blood · doi:10.1182/blood-2020-134718 · Cited by 27
Deacetylation as a receptor-regulated direct activation switch for pannexin channels
Chiu, Y., Medina, C. B., Doyle, C. A., Zhou, M., Narahari, A. K., Sandilos, J. K., Gonye, E. C., Gao, H.-Y., Guo, S. Y., Parlak, M., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-24825-y · Cited by 27
Self-citationHarrison, S. A., Baum, S. J., Gunn, N., Younes, Z. H., Kohli, A., Patil, R., Koziel, M. J., Chera, H., Zhao, J., & Chakravarthy, M. V. (2021) · The American Journal of Gastroenterology · doi:10.14309/ajg.0000000000001375 · Cited by 26
Jorge, A. M., Lao, T., Kim, R., Licciardi, S., Khoury, J. B. E., Luster, A. D., Means, T. K., & Ramirez‐Ortiz, Z. G. (2022) · The Journal of Immunology · doi:10.4049/jimmunol.2100532 · Cited by 23
Protein S and Gas6 induce efferocytosis of HIV-1-infected cells
Chua, B. A., Ngo, J. A., Situ, K., Ramirez, C. M., Nakano, H., & Morizono, K. (2018) · Virology · doi:10.1016/j.virol.2017.12.025 · Cited by 22
Woo, S. M., Min, K., Seo, S. U., Kim, S., Kubatka, P., Park, J., & Kwon, T. K. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20133253 · Cited by 22
Patel, V. M., Keating, M. J., Wierda, W. G., & Gandhi, V. V. (2015) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.3109/10428194.2015.1102243 · Cited by 21
Dutta, S., Mukherjee, A., & Nongthomba, U. (2022) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2022.01.002 · Cited by 21
Lakhani, N. J., LoRusso, P. M., Hafez, N., Krishnamurthy, A., O’Rourke, T. J., Kamdar, M. K., Fanning, P., Zhao, Y., Jin, F., Wan, H., et al. (2018) · Journal of Clinical Oncology · doi:10.1200/jco.2018.36.15_suppl.3068 · Cited by 20
Song, D.-H., Garcia, G., Situ, K., Chua, B. A., Hong, M. L. O., Do, E. A., Ramirez, C. M., Harui, A., Arumugaswami, V., & Morizono, K. (2021) · Virology · doi:10.1016/j.virol.2021.04.013 · Cited by 19
Gan, H. K., Coward, J. I. G., Mislang, A. R., Cosman, R., Nagrial, A. M., Jin, X., Li, B., Wang, Z. M., Kwek, K. Y., Xia, D., et al. (2021) · Journal of Clinical Oncology · doi:10.1200/jco.2021.39.15_suppl.2630 · Cited by 18
Pharmaco‐metabolomics opportunities in drug development and clinical research
Phapale, P. (2021) · Analytical Science Advances · doi:10.1002/ansa.202000178 · Cited by 13
Salina, A. C. G., dos-Santos, D., Rodrigues, T. S., et al. (2021) · medRxiv · doi:10.1101/2021.02.18.21251504 · Cited by 12
Mitochondrial hyperpolarization and ATP depletion in patients with systemic lupus erythematosus
Gergely, P., Grossman, C., Niland, B., Puskas, F., Neupane, H., Allam, F., Banki, K., Phillips, P. E., & Perl, A. (2002) · Arthritis & Rheumatism · doi:10.1002/1529-0131(200201)46:1 · Cited by 5
Sarantopoulos, J., Beg, M. S., Fotopoulos, G., Taverna, J. A., Anthony, S. P., Weitman, S. D., Warner, S. L., Mouritsen, L., Bearss, D. J., Smith, S. C., et al. (2018) · Journal of Clinical Oncology · doi:10.1200/jco.2018.36.15_suppl.tps2612 · Cited by 5
Subbiah, V., Awad, M. M., DAUD, A. I., Gutierrez, M. E., McDermott, J. D., Ou, S. I., Hirohashi, T., Ingram, K., Oliver, C., Smith, D., et al. (2021) · Journal of Clinical Oncology · doi:10.1200/jco.2021.39.15_suppl.tps2671 · Cited by 5
Harnessing Apoptotic Cells for Transplantation Tolerance: Current Status and Future Perspectives
Dangi, A., & Luo, X. (2017) · Current Transplantation Reports · doi:10.1007/s40472-017-0167-4 · Cited by 4
Lysosomal Cholesterol Hydrolysis Couples Efferocytosis To Anti-Inflammatory Oxysterol Production
Ivanov, S., Viaud, M., Vujić, N., Duta-Mare, M., Dugail, I., Hainault, I., Stehlik, C., Marchetti, S., Boyer, L., Guinamard, R., et al. (2019) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2019.06.223 · Cited by 4
Toyama, T., Asano, Y., Nakamura, K., Yamashita, T., Saigusa, R., Takahashi, T., Ichimura, Y., Taniguchi, T., Yoshizaki, A., Trojanowska, M., et al. (2016) · Journal of Dermatological Science · doi:10.1016/j.jdermsci.2016.08.043 · Cited by 2
Research works printed but not linked: 4
- Urbani, L. et al. in Transplantation Proceedings 1175–1178 (Elsevier, 2004).
- Dalli, J., Colas, R., Shinohara, M. & Serhan, C. N. Aging delays resolution of acute inflammation in mice: reprogramming the host response with novel nano-proresolving. Medicines 193, 4235–4244 (2014).
- Noelia, A. et al. Apoptotic cells promote their own clearance and immune tolerance through activation of the nuclear receptor LXR. Immunity 31, 245–258 (2009). This important study highlights the role of nuclear receptors in anti-inflammatory effects of efferocytosis and plausible therapeutic advantages of targeting the pathway. · DOI
- Bohan, D. et al. Targeting the receptor AXL by bemcentinib prevents SARS-CoV-2 infection. Top. Antivir. Med. 29, 137–138 (2021).
Cited by
Sorted by citations
Targeting immunogenic cell stress and death for cancer therapy
Galluzzi, L., Guilbaud, E., Schmidt, D. R., Kroemer, G., & Marincola, F. M. (2024) · Nature Reviews Drug Discovery · doi:10.1038/s41573-024-00920-9 · Cited by 638
A second-generation M1-polarized CAR macrophage with antitumor efficacy
Lei, A., Yu, H., Lu, S., Lu, H., Ding, X., Tan, T., Zhang, H., Zhu, M., Tian, L., Wang, X., et al. (2023) · Nature Immunology · doi:10.1038/s41590-023-01687-8 · Cited by 326
Macrophage function in adipose tissue homeostasis and metabolic inflammation
Chavakis, T., Alexaki, V. I., & Ferrante, A. W. (2023) · Nature Immunology · doi:10.1038/s41590-023-01479-0 · Cited by 279
Dendritic cell maturation in cancer
Moon, C. Y., Belabed, M., Park, M. D., Mattiuz, R., Puleston, D. J., & Mérad, M. (2025) · Nature reviews. Cancer · doi:10.1038/s41568-024-00787-3 · Cited by 189
The role of efferocytosis‐fueled macrophage metabolism in the resolution of inflammation
Schilperoort, M., Ngai, D., Sukka, S. R., Avrampou, K., Shi, H., & Tabas, I. A. (2023) · Immunological Reviews · doi:10.1111/imr.13214 · Cited by 184
Metadata
- Authors
- Mehrotra, P., & Ravichandran, K. S.
- Affiliations
- VIB-UGent Center for Inflammation Research (BE)
- Washington University in St. Louis (US)
- Corresponding author
- Ravichandran, Kodi S.
- Venue
- Nature Reviews Drug Discovery
- Published
- 2022-06-01
- Volume
- 21
- Issue
- 8
- Pages
- 601-620
- ISSN
- 1474-1776 (ISSN-L)
- 1474-1784
- PMC
- PMC9157040
- OpenAlex
- W4281737563
- Cited by
- 459
- References
- 231
- Citations by year
- 2026: 130 · 2025: 153 · 2024: 104 · 2023: 66 · 2022: 6
- FWCI
- 8.88
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Nature Reviews Drug Discovery (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Ghent University Academic Bibliography (Ghent University) (submittedVersion)
- Funders
- National Heart, Lung, and Blood Institute (P01HL120840)
- National Institute of General Medical Sciences (R35GM122542)
- National Institute of Allergy and Infectious Diseases (R01AI159551)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
- Keywords
- efferocytosis, phagocytes, anti-inflammatory mechanism, inflammation resolution, therapeutic target, atherosclerosis, cancer, infection
- MeSH terms
- Homeostasis, Humans, Phagocytes, Phagocytosis, Apoptosis, Atherosclerosis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
