#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Trichinella spiralis-induced mastocytosis and erythropoiesis are simultaneously supported by a bipotent mast cell/erythrocyte precursor cell


Autoři: Juan M. Inclan-Rico aff001;  Christina M. Hernandez aff001;  Everett K. Henry aff001;  Hannah G. Federman aff001;  Chandler B. Sy aff001;  John J. Ponessa aff001;  Alexander D. Lemenze aff003;  Nathanael Joseph aff004;  Patricia Soteropoulos aff004;  Aimee M. Beaulieu aff001;  George S. Yap aff001;  Mark C. Siracusa aff001
Působiště autorů: Center for Immunity and Inflammation, New Jersey Medical School, Rutgers-The State University of New Jersey, Newark, New Jersey, United States of America aff001;  Department of Medicine, New Jersey Medical School, Rutgers-The State University of New Jersey, Newark, New Jersey, United States of America aff002;  The Department of Pathology, Immunology and Laboratory Medicine, New Jersey Medical School, Rutgers-The State University of New Jersey, Newark, New Jersey, United States of America aff003;  The Genomics Center, New Jersey Medical School, Rutgers-The State University of New Jersey, Newark, New Jersey, United States of America aff004;  Department of Microbiology, Biochemistry and Molecular Genetics, New Jersey Medical School, Rutgers-The State University of New Jersey, Newark, New Jersey, United States of America aff005
Vyšlo v časopise: Trichinella spiralis-induced mastocytosis and erythropoiesis are simultaneously supported by a bipotent mast cell/erythrocyte precursor cell. PLoS Pathog 16(5): e32767. doi:10.1371/journal.ppat.1008579
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.ppat.1008579

Souhrn

Anti-helminth responses require robust type 2 cytokine production that simultaneously promotes worm expulsion and initiates the resolution of helminth-induced wounds and hemorrhaging. However, how infection-induced changes in hematopoiesis contribute to these seemingly distinct processes remains unknown. Recent studies have suggested the existence of a hematopoietic progenitor with dual mast cell-erythrocyte potential. Nonetheless, whether and how these progenitors contribute to host protection during an active infection remains to be defined. Here, we employed single cell RNA-sequencing and identified that the metabolic enzyme, carbonic anhydrase (Car) 1 marks a predefined bone marrow-resident hematopoietic progenitor cell (HPC) population. Next, we generated a Car1-reporter mouse model and found that Car1-GFP positive progenitors represent bipotent mast cell/erythrocyte precursors. Finally, we show that Car1-expressing HPCs simultaneously support mast cell and erythrocyte responses during Trichinella spiralis infection. Collectively, these data suggest that mast cell/erythrocyte precursors are mobilized to promote type 2 cytokine responses and alleviate helminth-induced blood loss, developmentally linking these processes. Collectively, these studies reveal unappreciated hematopoietic events initiated by the host to combat helminth parasites and provide insight into the evolutionary pressure that may have shaped the developmental relationship between mast cells and erythrocytes.

Klíčová slova:

Bone marrow cells – Flow cytometry – Helminth infections – Helminths – Mast cells – Parasitic diseases – Red blood cells – Stem cells


Zdroje

1. Schistosomiasis and soil-transmitted helminthiases: number of people treated in 2015. Wkly Epidemiol Rec. 2016;91(49–50):585–95. 27934297.

2. Jourdan PM, Lamberton PHL, Fenwick A, Addiss DG. Soil-transmitted helminth infections. Lancet. 2017. doi: 10.1016/S0140-6736(17)31930-X 28882382.

3. Gause WC, Wynn TA, Allen JE. Type 2 immunity and wound healing: evolutionary refinement of adaptive immunity by helminths. Nature reviews Immunology. 2013;13(8):607–14. doi: 10.1038/nri3476 23827958; PubMed Central PMCID: PMC3789590.

4. Gieseck Iii RL, Wilson MS, Wynn TA. Type 2 immunity in tissue repair and fibrosis. Nature Reviews Immunology. 2017;18:62. doi: 10.1038/nri.2017.90 28853443

5. Allen JE, Wynn TA. Evolution of Th2 immunity: a rapid repair response to tissue destructive pathogens. PLoS Pathog. 2011;7(5):e1002003. Epub 2011/05/19. doi: 10.1371/journal.ppat.1002003 21589896; PubMed Central PMCID: PMC3093361.

6. Lloyd CM, Snelgrove RJ. Type 2 immunity: Expanding our view. Science immunology. 2018;3(25). Epub 2018/07/08. doi: 10.1126/sciimmunol.aat1604 29980619.

7. Siracusa MC, Saenz SA, Wojno ED, Kim BS, Osborne LC, Ziegler CG, et al. Thymic stromal lymphopoietin-mediated extramedullary hematopoiesis promotes allergic inflammation. Immunity. 2013;39(6):1158–70. doi: 10.1016/j.immuni.2013.09.016 24332033; PubMed Central PMCID: PMC3959827.

8. Saenz SA, Siracusa MC, Perrigoue JG, Spencer SP, Urban JF Jr., Tocker JE, et al. IL25 elicits a multipotent progenitor cell population that promotes T(H)2 cytokine responses. Nature. 2010;464(7293):1362–6. doi: 10.1038/nature08901 20200520; PubMed Central PMCID: PMC2861732.

9. Hui CC, McNagny KM, Denburg JA, Siracusa MC. In situ hematopoiesis: a regulator of TH2 cytokine-mediated immunity and inflammation at mucosal surfaces. Mucosal Immunol. 2015;8(4):701–11. doi: 10.1038/mi.2015.17 25783967.

10. Liu AY, Dwyer DF, Jones TG, Bankova LG, Shen S, Katz HR, et al. Mast Cells Recruited to Mesenteric Lymph Nodes during Helminth Infection Remain Hypogranular and Produce IL-4 and IL-6. The Journal of Immunology. 2013;190(4):1758–66. doi: 10.4049/jimmunol.1202567 23319739

11. Wakelin D. Trichinella spiralis: immunity, ecology, and evolution. The Journal of parasitology. 1993;79(4):488–94. Epub 1993/08/01. 8331470.

12. Henry EK, Sy CB, Inclan-Rico JM, Espinosa V, Ghanny SS, Dwyer DF, et al. Carbonic anhydrase enzymes regulate mast cell-mediated inflammation. The Journal of experimental medicine. 2016;213(9):1663–73. doi: 10.1084/jem.20151739 27526715; PubMed Central PMCID: PMC4995079.

13. Tusi BK, Wolock SL, Weinreb C, Hwang Y, Hidalgo D, Zilionis R, et al. Population snapshots predict early haematopoietic and erythroid hierarchies. Nature. 2018;555:54. doi: 10.1038/nature25741 https://www.nature.com/articles/nature25741 - supplementary-information. 29466336

14. Zheng S, Papalexi E, Butler A, Stephenson W, Satija R. Molecular transitions in early progenitors during human cord blood hematopoiesis. Molecular systems biology. 2018;14(3):e8041. Epub 2018/03/17. doi: 10.15252/msb.20178041 29545397; PubMed Central PMCID: PMC5852373.

15. Li Z, Liu S, Xu J, Zhang X, Han D, Liu J, et al. Adult Connective Tissue-Resident Mast Cells Originate from Late Erythro-Myeloid Progenitors. Immunity. 2018;49(4):640–53 e5. Epub 2018/10/18. doi: 10.1016/j.immuni.2018.09.023 30332630.

16. Villeval JL, Testa U, Vinci G, Tonthat H, Bettaieb A, Titeux M, et al. Carbonic anhydrase I is an early specific marker of normal human erythroid differentiation. Blood. 1985;66(5):1162–70. Epub 1985/11/01. 3931725.

17. Butler A, Hoffman P, Smibert P, Papalexi E, Satija R. Integrating single-cell transcriptomic data across different conditions, technologies, and species. Nature Biotechnology. 2018;36(5):411–20. doi: 10.1038/nbt.4096 29608179

18. Sullivan BM, Liang HE, Bando JK, Wu D, Cheng LE, McKerrow JK, et al. Genetic analysis of basophil function in vivo. Nature immunology. 2011;12(6):527–35. Epub 2011/05/10. doi: 10.1038/ni.2036 21552267; PubMed Central PMCID: PMC3271435.

19. Schechter AN. Hemoglobin research and the origins of molecular medicine. Blood. 2008;112(10):3927–38. Epub 2008/11/08. doi: 10.1182/blood-2008-04-078188 18988877; PubMed Central PMCID: PMC2581994.

20. Nishida K, Uchida R. Role of Zinc Signaling in the Regulation of Mast Cell-, Basophil-, and T Cell-Mediated Allergic Responses. Journal of immunology research. 2018;2018:5749120. Epub 2019/01/01. doi: 10.1155/2018/5749120 30596108; PubMed Central PMCID: PMC6286780.

21. Han X, Wang R, Zhou Y, Fei L, Sun H, Lai S, et al. Mapping the Mouse Cell Atlas by Microwell-Seq. Cell. 2018;172(5):1091–107 e17. Epub 2018/02/24. doi: 10.1016/j.cell.2018.02.001 29474909.

22. Innocenti A, Scozzafava A, Parkkila S, Puccetti L, De Simone G, Supuran CT. Investigations of the esterase, phosphatase, and sulfatase activities of the cytosolic mammalian carbonic anhydrase isoforms I, II, and XIII with 4-nitrophenyl esters as substrates. Bioorg Med Chem Lett. 2008;18(7):2267–71. Epub 2008/03/21. doi: 10.1016/j.bmcl.2008.03.012 18353640.

23. Sata M, Saiura A, Kunisato A, Tojo A, Okada S, Tokuhisa T, et al. Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nature medicine. 2002;8:403. doi: 10.1038/nm0402-403 11927948

24. Visnjic D, Kalajzic Z, Rowe DW, Katavic V, Lorenzo J, Aguila HL. Hematopoiesis is severely altered in mice with an induced osteoblast deficiency. Blood. 2004;103(9):3258–64. Epub 2004/01/17. doi: 10.1182/blood-2003-11-4011 14726388.

25. Voehringer D. Protective and pathological roles of mast cells and basophils. Nature reviews Immunology. 2013;13(5):362–75. Epub 2013/04/06. doi: 10.1038/nri3427 23558889.

26. Dahlin JS, Hallgren J. Mast cell progenitors: origin, development and migration to tissues. Mol Immunol. 2015;63(1):9–17. Epub 2014/03/07. doi: 10.1016/j.molimm.2014.01.018 24598075.

27. Mikkola HK, Fujiwara Y, Schlaeger TM, Traver D, Orkin SH. Expression of CD41 marks the initiation of definitive hematopoiesis in the mouse embryo. Blood. 2003;101(2):508–16. Epub 2002/10/24. doi: 10.1182/blood-2002-06-1699 12393529.

28. Lilla JN, Chen C-C, Mukai K, BenBarak MJ, Franco CB, Kalesnikoff J, et al. Reduced mast cell and basophil numbers and function in Cpa3-Cre; Mcl-1fl/fl mice. Blood. 2011;118(26):6930–8. Epub 10/14. doi: 10.1182/blood-2011-03-343962 22001390.

29. Wang Y, Navin NE. Advances and applications of single-cell sequencing technologies. Mol Cell. 2015;58(4):598–609. Epub 2015/05/23. doi: 10.1016/j.molcel.2015.05.005 26000845; PubMed Central PMCID: PMC4441954.

30. Drury KE, Schaeffer M, Silverberg JI. Association Between Atopic Disease and Anemia in US Children. JAMA pediatrics. 2016;170(1):29–34. Epub 2015/12/01. doi: 10.1001/jamapediatrics.2015.3065 26619045.

31. Nwaru BI, Hayes H, Gambling L, Craig LC, Allan K, Prabhu N, et al. An exploratory study of the associations between maternal iron status in pregnancy and childhood wheeze and atopy. The British journal of nutrition. 2014;112(12):2018–27. Epub 2014/10/25. doi: 10.1017/S0007114514003122 25342229.

32. Bener A, Ehlayel M, Hamid Q. The impact of anemia and hemoglobin level as a risk factor for asthma and allergic diseases. Indian Journal of Allergy, Asthma and Immunology. 2015;29(2):72–8. doi: 10.4103/0972-6691.178271

33. Lewis RA. Mastocytosis. J Allergy Clin Immunol. 1984;74(6):755–65. Epub 1984/12/01. doi: 10.1016/0091-6749(84)90172-6 6389650.

34. Jawhar M, Schwaab J, Alvarez-Twose I, Shoumariyeh K, Naumann N, Lubke J, et al. MARS: Mutation-Adjusted Risk Score for Advanced Systemic Mastocytosis. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2019:Jco1900640. Epub 2019/09/12. doi: 10.1200/jco.19.00640 31509472.

35. Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov. 2008;7(2):168–81. Epub 2008/01/03. doi: 10.1038/nrd2467 18167490.

36. Lavin Y, Winter D, Blecher-Gonen R, David E, Keren-Shaul H, Merad M, et al. Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell. 2014;159(6):1312–26. Epub 2014/12/07. doi: 10.1016/j.cell.2014.11.018 25480296; PubMed Central PMCID: PMC4437213.

37. Xu J, Xu X, Wang B, Ma Y, Zhang L, Xu H, et al. Nuclear carbonic anhydrase 6B associates with PRMT5 to epigenetically promote IL-12 expression in innate response. Proceedings of the National Academy of Sciences of the United States of America. 2017;114(32):8620–5. Epub 2017/07/26. doi: 10.1073/pnas.1700917114 28739930; PubMed Central PMCID: PMC5559001.

38. Urban JF Jr., Schopf L, Morris SC, Orekhova T, Madden KB, Betts CJ, et al. Stat6 signaling promotes protective immunity against Trichinella spiralis through a mast cell- and T cell-dependent mechanism. J Immunol. 2000;164(4):2046–52. Epub 2000/02/05. doi: 10.4049/jimmunol.164.4.2046 10657657.

39. Moreau R, Tshikudi Malu D, Dumais M, Dalko E, Gaudreault V, Roméro H, et al. Alterations in bone and erythropoiesis in hemolytic anemia: comparative study in bled, phenylhydrazine-treated and Plasmodium-infected mice. PloS one. 2012;7(9):e46101–e. Epub 09/28. doi: 10.1371/journal.pone.0046101 23029401.

40. Ray A, Dittel BN. Isolation of mouse peritoneal cavity cells. Journal of visualized experiments: JoVE. 2010;(35):1488. doi: 10.3791/1488 20110936.


Článek vyšel v časopise

PLOS Pathogens


2020 Číslo 5
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Hypertenze a hypercholesterolémie – synergický efekt léčby
nový kurz
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Multidisciplinární zkušenosti u pacientů s diabetem
Autoři: Prof. MUDr. Martin Haluzík, DrSc., prof. MUDr. Vojtěch Melenovský, CSc., prof. MUDr. Vladimír Tesař, DrSc.

Úloha kombinovaných preparátů v léčbě arteriální hypertenze
Autoři: prof. MUDr. Martin Haluzík, DrSc.

Halitóza
Autoři: MUDr. Ladislav Korábek, CSc., MBA

Terapie roztroušené sklerózy v kostce
Autoři: MUDr. Dominika Šťastná, Ph.D.

Všechny kurzy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#