{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,24]],"date-time":"2026-04-24T18:21:23Z","timestamp":1777054883634,"version":"3.51.4"},"reference-count":32,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2022,8,15]],"date-time":"2022-08-15T00:00:00Z","timestamp":1660521600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100012226","name":"Fundamental Research Funds for the Central Universities","doi-asserted-by":"publisher","award":["XDJK2020B005"],"award-info":[{"award-number":["XDJK2020B005"]}],"id":[{"id":"10.13039\/501100012226","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012226","name":"Fundamental Research Funds for the Central Universities","doi-asserted-by":"publisher","award":["31802141"],"award-info":[{"award-number":["31802141"]}],"id":[{"id":"10.13039\/501100012226","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012226","name":"Fundamental Research Funds for the Central Universities","doi-asserted-by":"publisher","award":["cstc2018jcyj-yszxX0012"],"award-info":[{"award-number":["cstc2018jcyj-yszxX0012"]}],"id":[{"id":"10.13039\/501100012226","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["XDJK2020B005"],"award-info":[{"award-number":["XDJK2020B005"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["31802141"],"award-info":[{"award-number":["31802141"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["cstc2018jcyj-yszxX0012"],"award-info":[{"award-number":["cstc2018jcyj-yszxX0012"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Academician Fund of Chongqing\/Natural Science Foundation of Chongqing","award":["XDJK2020B005"],"award-info":[{"award-number":["XDJK2020B005"]}]},{"name":"Academician Fund of Chongqing\/Natural Science Foundation of Chongqing","award":["31802141"],"award-info":[{"award-number":["31802141"]}]},{"name":"Academician Fund of Chongqing\/Natural Science Foundation of Chongqing","award":["cstc2018jcyj-yszxX0012"],"award-info":[{"award-number":["cstc2018jcyj-yszxX0012"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Background: Microsporidia are a group of obligated intracellular fungus pathogens. Monocytes and the derivative macrophages are among the most important players in host immunity. The invasion of microsporidia may significantly affect the monocytes maturation and extravasation processes. Methods: We utilized a previously established microsporidia infection murine model to investigate the influences of microsporidia Encephalitozoon hellem (E. hellem) infection on monocyte maturation, releasing into the circulation and extravasation to the inflammation site. Flow cytometry and qPCR analysis were used to compare the monocytes and derivative macrophages isolated from bone marrow, peripheral blood and tissues of E. hellem-infected and control mice. Results: The results showed that the pro-inflammatory group of CD11b+Ly-6C+ monocytes are promoted in E. hellem-infected mice. Interestingly, the percentage of Ly-6C+ monocytes from E. hellem-infected mice are significantly lower in peripheral blood while significantly higher in the inflamed small intestine, together with up-regulated ratio of F4\/80 macrophage in small intestine as well. Conclusions: Our findings demonstrated that E. hellem infection leads to promoted monocytes maturation in bone marrow, up-regulation of extravasation from peripheral blood to inflammation site and maturation into macrophages. Our study is the first systematic analysis of monocytes maturation and trafficking during microsporidia infection, and will provide better understanding of the pathogen\u2013host interactions.<\/jats:p>","DOI":"10.3390\/pathogens11080914","type":"journal-article","created":{"date-parts":[[2022,8,15]],"date-time":"2022-08-15T03:33:20Z","timestamp":1660534400000},"page":"914","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Encephalitozoon hellem Infection Promotes Monocytes Extravasation"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0771-3057","authenticated-orcid":false,"given":"Yishan","family":"Lu","sequence":"first","affiliation":[{"name":"Sate Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400715, China"},{"name":"Chongqing Key Laboratory of Microsporidia Infection and Control, Southwest University, Chongqing 400715, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Guozhen","family":"An","sequence":"additional","affiliation":[{"name":"Sate Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400715, China"},{"name":"Chongqing Key Laboratory of Microsporidia Infection and Control, Southwest University, Chongqing 400715, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xue","family":"Wang","sequence":"additional","affiliation":[{"name":"Sate Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400715, China"},{"name":"Chongqing Key Laboratory of Microsporidia Infection and Control, Southwest University, Chongqing 400715, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yunlin","family":"Tang","sequence":"additional","affiliation":[{"name":"Sate Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400715, China"},{"name":"Chongqing Key Laboratory of Microsporidia Infection and Control, Southwest University, Chongqing 400715, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jiangyan","family":"Jin","sequence":"additional","affiliation":[{"name":"Sate Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400715, China"},{"name":"Chongqing Key Laboratory of Microsporidia Infection and Control, Southwest University, Chongqing 400715, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jialing","family":"Bao","sequence":"additional","affiliation":[{"name":"Sate Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400715, China"},{"name":"Chongqing Key Laboratory of Microsporidia Infection and Control, Southwest University, Chongqing 400715, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zeyang","family":"Zhou","sequence":"additional","affiliation":[{"name":"Sate Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400715, China"},{"name":"Chongqing Key Laboratory of Microsporidia Infection and Control, Southwest University, Chongqing 400715, China"},{"name":"College of Life Sciences, Chongqing Normal University, Chongqing 400038, China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,8,15]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/S0001-706X(00)00178-9","article-title":"Microsporidia: Emerging pathogenic protists","volume":"78","author":"Weiss","year":"2001","journal-title":"Acta Trop."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1097\/01.qco.0000244055.46382.23","article-title":"Microsporidiosis: Current status","volume":"19","author":"Didier","year":"2006","journal-title":"Curr. Opin. Infect. Dis."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"426","DOI":"10.1128\/CMR.7.4.426","article-title":"Human microsporidial infections","volume":"7","author":"Weber","year":"1994","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1016\/j.mib.2015.03.006","article-title":"Microsporidia-host interactions","volume":"26","author":"Szumowski","year":"2015","journal-title":"Curr. Opin. Microbiol."},{"key":"ref_5","first-page":"513","article-title":"Microsporidia: General characteristics, infections and laboratory diagnosis","volume":"39","author":"Sancak","year":"2005","journal-title":"Mikrobiyol. Bul."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"7461","DOI":"10.1073\/pnas.131202998","article-title":"How the immune system works to protect the host from infection: A personal view","volume":"98","author":"Janeway","year":"2001","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"905","DOI":"10.1016\/j.micinf.2009.06.004","article-title":"Innate immune responses to Encephalitozoon species infections","volume":"11","author":"Mathews","year":"2009","journal-title":"Microbes. Infect."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"e12828","DOI":"10.1111\/pim.12828","article-title":"Advancement in our understanding of immune response against Encephalitozoon infection","volume":"43","author":"Aseeja","year":"2021","journal-title":"Parasite Immunol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"569","DOI":"10.1017\/S0031182018001968","article-title":"Encephalitozoon cuniculi and Vittaforma corneae (Phylum Microsporidia) inhibit staurosporine-induced apoptosis in human THP-1 macrophages in vitro","volume":"146","author":"Sokolova","year":"2019","journal-title":"Parasitology"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Dalboni, L.C., Alvares Saraiva, A.M., Konno, F.T.C., Perez, E.C., Codeceira, J.F., Spadacci-Morena, D.D., and Lallo, M.A. (2021). Encephalitozoon cuniculi takes advantage of efferocytosis to evade the immune response. PLoS ONE, 16.","DOI":"10.1371\/journal.pone.0247658"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1468","DOI":"10.3389\/fmicb.2020.01468","article-title":"Innate and Adaptive Immune Responses Against Microsporidia Infection in Mammals","volume":"11","author":"Han","year":"2020","journal-title":"Front. Microbiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"656","DOI":"10.1126\/science.1178331","article-title":"Development of monocytes, macrophages, and dendritic cells","volume":"327","author":"Geissmann","year":"2010","journal-title":"Science"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1619","DOI":"10.1128\/IAI.01535-06","article-title":"Induction of host chemotactic response by Encephalitozoon spp","volume":"75","author":"Fischer","year":"2007","journal-title":"Infect. Immun."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1016\/S1074-7613(03)00174-2","article-title":"Blood monocytes consist of two principal subsets with distinct migratory properties","volume":"19","author":"Geissmann","year":"2003","journal-title":"Immunity"},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Morias, Y., Abels, C., Laoui, D., Van Overmeire, E., Guilliams, M., Schouppe, E., Tacke, F., Devries, C.J., De Baetselier, P., and Beschin, A. (2015). Ly6C\u2212 Monocytes Regulate Parasite-Induced Liver Inflammation by Inducing the Differentiation of Pathogenic Ly6C+ Monocytes into Macrophages. PLoS Pathog., 11.","DOI":"10.1371\/journal.ppat.1004873"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1361","DOI":"10.1084\/jem.194.9.1361","article-title":"Inflammatory chemokine transport and presentation in HEV: A remote control mechanism for monocyte recruitment to lymph nodes in inflamed tissues","volume":"194","author":"Palframan","year":"2001","journal-title":"J. Exp. Med."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"902","DOI":"10.1172\/JCI29919","article-title":"Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites","volume":"117","author":"Tsou","year":"2007","journal-title":"J. Clin. Investig."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"826","DOI":"10.1080\/09273948.2018.1455875","article-title":"Stromal Keratitis with Endophthalmitis Caused by Vittaforma Corneae in an Immunocompetent Patient: A Case Report","volume":"27","author":"Pariyakanok","year":"2019","journal-title":"Ocul. Immunol. Inflamm."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Chanthick, C., Suttitheptumrong, A., Rawarak, N., and Pattanakitsakul, S.N. (2018). Transcytosis Involvement in Transport System and Endothelial Permeability of Vascular Leakage during Dengue Virus Infection. Viruses, 10.","DOI":"10.3390\/v10020069"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"4410","DOI":"10.4049\/jimmunol.172.7.4410","article-title":"Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response","volume":"172","author":"Nikolic","year":"2004","journal-title":"J. Immunol."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"An, G., Tang, Y., Mo, B., Ran, M., He, X., Bao, J., and Zhou, Z. (2020). Characterization of a Murine Model for Encephalitozoon hellem Infection after Dexamethasone Immunosuppression. Microorganisms, 8.","DOI":"10.3390\/microorganisms8121891"},{"key":"ref_22","first-page":"105s","article-title":"Culture, electron microscopy, and immunoblot studies on a microsporidian parasite isolated from the urine of a patient with AIDS","volume":"38","author":"Visvesvara","year":"1991","journal-title":"J. Protozool."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1485","DOI":"10.1016\/j.biopha.2016.08.068","article-title":"Dexamethasone provoked mitochondrial perturbations in thymus: Possible role of N-acetylglucosamine in restoration of mitochondrial function","volume":"83","author":"Venugopalan","year":"2016","journal-title":"Biomed. Pharmacother."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"e1631","DOI":"10.21769\/BioProtoc.1631","article-title":"Immune Cell Isolation from Mouse Femur Bone Marrow","volume":"5","author":"Liu","year":"2015","journal-title":"Bio Protoc."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"612","DOI":"10.1126\/science.1175202","article-title":"Identification of splenic reservoir monocytes and their deployment to inflammatory sites","volume":"325","author":"Swirski","year":"2009","journal-title":"Science"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"669","DOI":"10.1146\/annurev.immunol.021908.132557","article-title":"Blood monocytes: Development, heterogeneity, and relationship with dendritic cells","volume":"27","author":"Auffray","year":"2009","journal-title":"Annu. Rev. Immunol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"232","DOI":"10.1016\/j.stem.2021.12.009","article-title":"The microbiota regulates hematopoietic stem cell fate decisions by controlling iron availability in bone marrow","volume":"29","author":"Zhang","year":"2022","journal-title":"Cell Stem Cell"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Bandeira Ferreira, F.L., S\u00e9guin, O., Descoteaux, A., and Heinonen, K.M. (2022). Persistent Cutaneous Leishmania major Infection Promotes Infection-Adapted Myelopoiesis. Microorganisms, 10.","DOI":"10.3390\/microorganisms10030535"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1016\/S0022-1759(98)00080-5","article-title":"Bone marrow cellular composition in Listeria monocytogenes infected mice detected using ER-MP12 and ER-MP20 antibodies: A flow cytometric alternative to differential counting","volume":"217","author":"Ploemacher","year":"1998","journal-title":"J. Immunol. Methods"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"De Trez, C., Magez, S., Akira, S., Ryffel, B., Carlier, Y., and Muraille, E. (2009). iNOS-producing inflammatory dendritic cells constitute the major infected cell type during the chronic Leishmania major infection phase of C57BL\/6 resistant mice. PLoS Pathog., 5.","DOI":"10.1371\/journal.ppat.1000494"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Pereira, A., Alvares-Saraiva, A.M., Konno, F.T.C., Spadacci-Morena, D.D., Perez, E.C., Mariano, M., and Lallo, M.A. (2019). B-1 cell-mediated modulation of M1 macrophage profile ameliorates microbicidal functions and disrupt the evasion mechanisms of Encephalitozoon cuniculi. PLoS Negl. Trop. Dis., 13.","DOI":"10.1101\/567404"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"4","DOI":"10.3389\/fcimb.2016.00004","article-title":"Encephalitozoon intestinalis Inhibits Dendritic Cell Differentiation through an IL-6-Dependent Mechanism","volume":"6","author":"Bernal","year":"2016","journal-title":"Front. Cell Infect. Microbiol."}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/11\/8\/914\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T00:08:42Z","timestamp":1760141322000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/11\/8\/914"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,8,15]]},"references-count":32,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2022,8]]}},"alternative-id":["pathogens11080914"],"URL":"https:\/\/doi.org\/10.3390\/pathogens11080914","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,8,15]]}}}