Russian Journal of Allergy

Российский Аллергологический Журнал

1810-88302686-682X

Publishing House ABV Press

1363

10.36691/RJA1363

Reviews

Научные обзоры

Review Article

Interactions of mast cells and eosinophils in allergic response

Взаимодействие тучных клеток и эозинофилов в аллергическом ответе

https://orcid.org/0000-0002-4465-6509

Gushchin

Igor S.

Гущин

Игорь Сергеевич

Russian Federation

MD, PhD, professor, corresponding member of Russian Academy of Sciences, head of the Departament of Clinical Immunology and Allergology

член-корреспондент РАН, зав. отделом клинической иммунологии и аллергологии

igushchin@yandex.ru

NRC Institute of Immunology FMBA of RussiaФГБУ «ГНЦ Институт иммунологии» ФМБА России

23072020

172

5171006202010062020

2020

Pharmarus Print Media

Фармарус Принт Медиа

https://rusalljournal.ru/raj/article/view/1363

Mast cells (MCs) and eosinophils (EOs) appeared hundreds of millions of years ago during the evolutionary process and continue to be retained by all vertebrate species. There is no convincing evidence of the absence of these cells in vertebrates under normal conditions. These cells are involved in the reactions of innate and adaptive immunity, in the control of tissue growth and tissue remodeling, activation of adipose tissue, affect reproductive functions and have a wide range of mediators involved in homeostasis. It is known that the interaction of these cells is involved in the initiation and maintenance of allergic inflammation. Fc_εRI-mediated MC activation leads to mediators secretion, among which there are many chemotactic agents for EOs. These agents attract the EOs to the site of allergic inflammation. The EOs come into physical contact with the MCs, accompanied by the EO activation. As a result of the action of mediators released from MCs and EO, the active state of the cells is enhanced and maintained, and, accordingly, the process of inflammation is prolonged with the corresponding consequences in the form of triggering tissue remodeling. Eosinophil-derived active substances released during the reaction, having at least anti-mediator properties, contribute to the suppression and resolution of allergic inflammation. Such a look at the nature of the interactions between EOs and MCs justifies the comparative determination of the kinetics of the release of pro-allergic mediators from those cells and the formation of EO-derived compounds with antiallergic activity. It is expected that such studies will be carried out in the nearest future.

Тучные клетки (ТчК) и эозинофилы (ЭО) появились сотни миллионов лет тому назад в ходе эволюционного процесса и сохранились у всех видов позвоночных. Нет убедительных свидетельств отсутствия этих клеток у позвоночных в естественных условиях. Эти клетки участвуют в реакциях врожденного и адаптивного иммунитета, в контроле тканевого роста и ремоделирования тканей, активации жировой ткани, влияют на репродуктивные функции и обладают широким спектром посредников, участвующих в гомеостазе. Известно, что взаимодействие этих клеток участвует в инициации и поддержании аллергического воспаления. Fc_εRI-опосредованная активация ТчК приводит к секреции медиаторов, среди которых есть много хемотаксических агентов для ЭO. Хемоаттрактанты привлекают в зону аллергического воспаления ЭО, вступающие в физический контакт с ТчК, сопровождающийся активацией ЭО. В результате действия высвобождаемых из Тчк и ЭО посредников усиливается и поддерживается активное состояние клеток и, соответственно, удлиняется процесс воспаления с соответствующими последствиями в виде запуска ремоделирования ткани. Высвобождаемые в ходе реакции активные соединения эозинофильного происхождения, имеющие, по крайней мере, антимедиаторные свойства, способствуют подавлению и завершению процесса аллергического воспаления. Такой взгляд на характер взаимодействия ЭО и ТчК обосновывает одновременное определение кинетики высвобождения из тех и других клеток проаллергических медиаторов и образования эозинофилами соединений, имеющих противоаллергическую активность. Следует ожидать, что такие исследования будут проведены в ближайшем будущем.

allergymast cellseosinophilschemokinescytokinescationic proteinseosinophil enzymesFcεRI-mediated activationinflammationhomeostasis

аллергиятучные клеткиэозинофилыхемокиныцитокиныкатионные белкиферменты эозинофиловFcεRI-опосредованная активациявоспалениегомеостаз

Klion AD. Eosinophilia: a pragmatic approach to diagnosis and treatment. Hematology Am Soc Hematol Educ Program. 2015;2015:92-97. DOI: 10.1182/asheducation-2015.1.92.

Robida PA, Puzzovio PG, Pahima H, Levi-Schaffer F, Bochner BS. Human eosinophils and mast cells: Birds of a feather flock together. Immunol Rev. 2018;282(1):151-167. DOI: 10.1111/imr.12638.

Gangwar RS, Friedman S, Seaf M, Levi-Schaffer F. Mast cells and eosinophils in allergy: Close friends or just neighbors. Eur J Pharmacol. 2016;778:77-83. DOI: 10.1016/j.ejphar.2015.10.036.

Gangwar RS, Levi-Schaffer F. Eosinophils interaction with mast cells: the allergic effector unit. Methods Mol Biol. 2014;1178:231-249. DOI: 10.1007/978-1-4939-1016-8_20.

Chusid MJ. Eosinophils: Friends or Foes? J Allergy Clin Immunol Pract. 2018;6(5):1439-1444. DOI: 10.1016/j.jaip.2018.04.031.

Galdiero MR, Varricchi G, Seaf M, Marone G, Levi-Schaffer F, Marone G. Bidirectional mast cell-eosinophil interactions in inflammatory disorders and cancer. Front Med (Lausanne). 2017;4:103. Published 2017 Jul 24. DOI: 10.3389/fmed.2017.00103.

Kay AB. Paul Ehrlich and the early history of granulocytes. Microbiol Spectr. 2016;4(4):10.1128/microbiolspec.MCHD-0032-2016. DOI: 10.1128/microbiolspec.MCHD-0032-2016.

Kay AB. The early history of the eosinophil. Clin Exp Allergy. 2015;45(3):575-582. DOI: 10.1111/cea.

Stacy NI, Raskin RE. Reptilian eosinophils: beauty and diversity by light microscopy. Vet Clin Pathol. 2015;44(2):177-178. DOI: 10.1111/vcp.12246.

10.

Lenzi HL, Pacheco RG, Pelajo-Machado M, Panasco MS, Romanha WS, Lenzi JA. Immunological system and Schistosoma mansoni: co-evolutionary immunobiology. What is the eosinophil role in parasite-host relationship? Mem Inst Oswaldo Cruz. 1997;92 Suppl 2:19-32. DOI: 10.1590/s0074-02761997000800005.

11.

Гущин ИС. Аллергия – поздний продукт эволюции иммунной системы. Иммунология. 2019;40(2):43-57. DOI: 10.24411/0206-4952-2019-12007 [Gushchin IS. Allergy – late product of the immune system evolution. Immunologiya. 2019;40(2):43-57. DOI: 10.24411/0206-4952-2019-12007 (in Russian)].

12.

Mori Y, Iwasaki H, Kohno K et al. Identification of the human eosinophil lineage-committed progenitor: revision of phenotypic definition of the human common myeloid progenitor. J Exp Med. 2009;206(1):183-193. DOI: 10.1084/jem.20081756.

13.

Dahlin JS, Hallgren J. Mast cell progenitors: origin, development and migration to tissues. Mol Immunol. 2015;63(1):9-17. DOI: 10.1016/j.molimm.2014.01.018.

14.

Schmetzer O, Valentin P, Church MK, Maurer M, Siebenhaar F. Murine and human mast cell progenitors. Eur J Pharmacol. 2016;778:2-10. DOI: 10.1016/j.ejphar.2015.07.016.

15.

Bouffi C, Kartashov AV, Schollaert KL et al. Transcription factor repertoire of homeostatic eosinophilopoiesis. J Immunol. 2015;195(6):2683-2695. DOI: 10.4049/jimmunol.1500510.

16.

Bettigole SE, Lis R, Adoro S et al. The transcription factor XBP1 is selectively required for eosinophil differentiation. Nat Immunol. 2015;16(8):829-837. DOI:10.1038/ni.3225.

17.

Matthews SP, McMillan SJ, Colbert JD, Lawrence RA, Watts C. Cystatin F ensures eosinophil survival by regulating granule biogenesis. Immunity. 2016;44(4):795-806. DOI: 10.1016/j.immuni.2016.03.003.

18.

Dwyer DF, Barrett NA, Austen KF; Immunological Genome Project Consortium. Expression profiling of constitutive mast cells reveals a unique identity within the immune system. Nat Immunol. 2016;17(7):878-887. DOI: 10.1038/ni.3445.

19.

Drissen R, Buza-Vidas N, Woll P et al. Distinct myeloid progenitor-differentiation pathways identified through single-cell RNA sequencing. Nat Immunol. 2016;17(6):666-676. DOI: 10.1038/ni.3412.

20.

Frossi B, Mion F, Tripodo C, Colombo MP, Pucillo CE. Rheostatic functions of mast cells in the control of innate and adaptive immune responses. Trends Immunol. 2017;38(9):648-656. DOI: 10.1016/j.it.2017.04.001.

21.

22.

Johnston LK, Hsu CL, Krier-Burris RA et al. IL-33 Precedes IL-5 in regulating eosinophil commitment and is required for eosinophil homeostasis. J Immunol. 2016;197(9):3445-3453. DOI: 10.4049/jimmunol.1600611.

23.

Lamousé-Smith ES, Furuta GT. Eosinophils in the gastrointestinal tract. Curr Gastroenterol Rep. 2006;8(5):390-395. DOI: 10.1007/s11894-006-0024-6.

24.

Jung Y, Rothenberg ME. Roles and regulation of gastrointestinal eosinophils in immunity and disease. J Immunol. 2014;193(3):999-1005. DOI: 10.4049/jimmunol.1400413.

25.

Lee JJ, Jacobsen EA, Ochkur SI et al. Human versus mouse eosinophils: «that which we call an eosinophil, by any other name would stain as red». J Allergy Clin Immunol. 2012;130(3):572-584. DOI: 10.1016/j.jaci.2012.07.025.

26.

Foster PS, Mould AW, Yang M et al. Elemental signals regulating eosinophil accumulation in the lung. Immunol Rev. 2001;179:173-181. DOI: 10.1034/j.1600-065x.2001.790117.x.

27.

Simon HU, Yousefi S, Germic N et al. The cellular functions of eosinophils: Collegium Internationale Allergologicum (CIA) Update 2020. Int Arch Allergy Immunol. 2020;181(1):11-23. DOI: 10.1159/000504847.

28.

Abdala-Valencia H, Coden ME, Chiarella SE et al. Shaping eosinophil identity in the tissue contexts of development, homeostasis, and disease. J Leukoc Biol. 2018;104(1):95-108. DOI: 10.1002/JLB.1MR1117-442RR.

29.

Minai-Fleminger Y, Elishmereni M, Vita F et al. Ultrastructural evidence for human mast cell-eosinophil interactions in vitro. Cell Tissue Res. 2010;341(3):405-415. DOI: 10.1007/s00441-010-1010-8.

30.

Elishmereni M, Alenius HT, Bradding P et al. Physical interactions between mast cells and eosinophils: a novel mechanism enhancing eosinophil survival in vitro. Allergy. 2011;66(3):376-385. DOI: 10.1111/j.1398-9995.2010.02494.x.

31.

Elishmereni M, Bachelet I, Nissim Ben-Efraim AH, Mankuta D, Levi-Schaffer F. Interacting mast cells and eosinophils acquire an enhanced activation state in vitro. Allergy. 2013;68(2):171-179. DOI: 10.1111/all.12059.

32.

Ling P, Ngo K, Nguyen S et al. Histamine H4 receptor mediates eosinophil chemotaxis with cell shape change and adhesion molecule upregulation [published correction appears in Br J Pharmacol. 2004 Jul;142(6):1052]. Br J Pharmacol. 2004;142(1):161-171. DOI: 10.1038/sj.bjp.0705729.

33.

Church MK. Allergy, Histamine and Antihistamines. Handb Exp Pharmacol. 2017;241:321-331. DOI: 10.1007/164_2016_85.

34.

Hofstra CL, Desai PJ, Thurmond RL, Fung-Leung WP. Histamine H4 receptor mediates chemotaxis and calcium mobilization of mast cells. J Pharmacol Exp Ther. 2003;305(3):1212-1221. DOI: 10.1124/jpet.102.046581.

35.

Gervais FG, Cruz RP, Chateauneuf A et al. Selective modulation of chemokinesis, degranulation, and apoptosis in eosinophils through the PGD2 receptors CRTH2 and DP. J Allergy Clin Immunol. 2001;108(6):982-988. DOI: 10.1067/mai.2001.119919.

36.

Schratl P, Royer JF, Kostenis E et al. The role of the prostaglandin D2 receptor, DP, in eosinophil trafficking. J Immunol. 2007;179(7):4792-4799. DOI: 10.4049/jimmunol.179.7.4792.

37.

Nagasaka A, Matsue H, Matsushima H et al. Osteopontin is produced by mast cells and affects IgE-mediated degranulation and migration of mast cells. Eur J Immunol. 2008;38(2):489-499. DOI: 10.1002/eji.200737057.

38.

Takahashi A, Kurokawa M, Konno S et al. Osteopontin is involved in migration of eosinophils in asthma. Clin Exp Allergy. 2009;39(8):1152-1159. DOI: 10.1111/j.1365-2222.2009.03249.x.

39.

Puxeddu I, Berkman N, Ribatti D et al. Osteopontin is expressed and functional in human eosinophils. Allergy. 2010;65(2):168-174. DOI: 10.1111/j.1398-9995.2009.02148.x.

40.

Shakoory B, Fitzgerald SM, Lee SA, Chi DS, Krishnaswamy G. The role of human mast cell-derived cytokines in eosinophil biology. J Interferon Cytokine Res. 2004;24(5):271-281. DOI: 10.1089/107999004323065057.

41.

Velazquez JR, Teran LM. Chemokines and their receptors in the allergic airway inflammatory process. Clin Rev Allergy Immunol. 2011;41(1):76-88. DOI: 10.1007/s12016-010-8202-6.

42.

Mukai K, Tsai M, Saito H, Galli SJ. Mast cells as sources of cytokines, chemokines, and growth factors. Immunol Rev. 2018;282(1):121-150. DOI: 10.1111/imr.12634.

43.

Oliveira SH, Lukacs NW. The role of chemokines and chemokine receptors in eosinophil activation during inflammatory allergic reactions. Braz J Med Biol Res. 2003;36(11):1455-1463. DOI: 10.1590/s0100-879x2003001100002.

44.

Elishmereni M, Nissim Ben-Efraim AH, Bachelet I, Levi-Schaffer F. Mast cell-eosinophil cross-talk regulates function and viability of both cells in vitro. J Allergy Clin Immunol. 2008;121(2),S100. DOI: 10.1016/j.jaci.2007.12.438.

45.

Levi-Schaffer F, Temkin V, Malamud V, Feld S, Zilberman Y. Mast cells enhance eosinophil survival in vitro: role of TNF-alpha and granulocyte-macrophage colony-stimulating factor. J Immunol. 1998;160(11):5554-5562. PMID: 9605160.

46.

Baumann A, Gönnenwein S, Bischoff SC et al. The circadian clock is functional in eosinophils and mast cells. Immunology. 2013;140(4):465-474. DOI: 10.1111/imm.12157.

47.

Baumann A, Feilhauer K, Bischoff SC, Froy O, Lorentz A. IgE-dependent activation of human mast cells and fMLP-mediated activation of human eosinophils is controlled by the circadian clock. Mol Immunol. 2015;64(1):76-81. DOI: 10.1016/j.molimm.2014.10.026.

48.

Metcalfe DD, Pawankar R, Ackerman SJ et al. Biomarkers of the involvement of mast cells, basophils and eosinophils in asthma and allergic diseases. World Allergy Organ J. 2016;9:7. Published 2016 Feb 11. DOI: 10.1186/s40413-016-0094-3.

49.

Barata LT, Ying S, Grant JA et al. Allergen-induced recruitment of Fc epsilon RI+ eosinophils in human atopic skin. Eur J Immunol. 1997;27(5):1236-1241. DOI: 10.1002/eji.1830270527.

50.

Ying S, Barata LT, Meng Q et al. High-affinity immunoglobulin E receptor (Fc epsilon RI)-bearing eosinophils, mast cells, macrophages and Langerhans’ cells in allergen-induced late-phase cutaneous reactions in atopic subjects. Immunology. 1998;93(2):281-288. DOI: 10.1046/j.1365-2567.1998.00418.x’.

51.

Smith SJ, Ying S, Meng Q et al. Blood eosinophils from atopic donors express messenger RNA for the alpha, beta, and gamma subunits of the high-affinity IgE receptor (Fc epsilon RI) and intracellular, but not cell surface, alpha subunit protein. J Allergy Clin Immunol. 2000;105(2 Pt 1):309-317. DOI: 10.1016/s0091-6749(00)90081-2.

52.

Messingham KN, Holahan HM, Frydman AS, Fullenkamp C, Srikantha R, Fairley JA. Human eosinophils express the high affinity IgE receptor, FcεRI, in bullous pemphigoid. PLoS One. 2014;9(9):e107725. Published 2014 Sep 25. DOI: 10.1371/journal.pone.0107725.

53.

Iikura M, Yamaguchi M, Hirai K et al. Regulation of surface FcepsilonRI expression on human eosinophils by IL-4 and IgE. Int Arch Allergy Immunol. 2001;124(4):470-477. DOI: 10.1159/000053782.

54.

Jemima EA, Prema A, Thangam EB. Functional characterization of histamine H4 receptor on human mast cells. Mol Immunol. 2014;62(1):19-28. DOI: 10.1016/j.molimm.2014.05.007.

55.

Marquardt DL, Gruber HE, Wasserman SI. Adenosine release from stimulated mast cells. Proc Natl Acad Sci USA. 1984;81(19):6192-6196. DOI: 10.1073/pnas.81.19.6192.

56.

Rudich N, Ravid K, Sagi-Eisenberg R. Mast cell adenosine receptors function: a focus on the a3 adenosine receptor and inflammation. Front Immunol. 2012;3:134. Published 2012 Jun 4. DOI: 10.3389/fimmu.2012.00134.

57.

Ryzhov S, Zaynagetdinov R, Goldstein AE et al. Effect of A2B adenosine receptor gene ablation on proinflammatory adenosine signaling in mast cells. J Immunol. 2008;180(11):7212-7220. DOI: 10.4049/jimmunol.180.11.7212.

58.

Walker BA, Jacobson MA, Knight DA et al. Adenosine A3 receptor expression and function in eosinophils. Am J Respir Cell Mol Biol. 1997;16(5):531-537. DOI: 10.1165/ajrcmb.16.5.9160835.

59.

Reeves JJ, Harris CA, Hayes BP, Butchers PR, Sheehan MJ. Studies on the effects of adenosine A3 receptor stimulation on human eosinophils isolated from non-asthmatic or asthmatic donors. Inflamm Res. 2000;49(12):666-672. DOI: 10.1007/s000110050644.

60.

Kohno Y, Ji X, Mawhorter SD, Koshiba M, Jacobson KA. Activation of A3 adenosine receptors on human eosinophils elevates intracellular calcium. Blood. 1996;88(9):3569-3574.

61.

Knight D, Zheng X, Rocchini C, Jacobson M, Bai T, Walker B. Adenosine A3 receptor stimulation inhibits migration of human eosinophils. J Leukoc Biol. 1997;62(4):465-468. DOI: 10.1002/jlb.62.4.465.

62.

Hsu CL, Bryce PJ. Inducible IL-33 expression by mast cells is regulated by a calcium-dependent pathway. J Immunol. 2012;189(7):3421-3429. DOI: 10.4049/jimmunol.1201224.

63.

Angulo EL, McKernan EM, Fichtinger PS, Mathur SK. Comparison of IL-33 and IL-5 family mediated activation of human eosinophils. PLoS One. 2019;14(9):e0217807. Published 2019 Sep 6. DOI: 10.1371/journal.pone.0217807.

64.

Temkin V, Kantor B, Weg V, Hartman ML, Levi-Schaffer F. Tryptase activates the mitogen-activated protein kinase/activator protein-1 pathway in human peripheral blood eosinophils, causing cytokine production and release. J Immunol. 2002;169(5):2662-2669. DOI: 10.4049/jimmunol.169.5.2662.

65.

Ochi H, De Jesus NH, Hsieh FH, Austen KF, Boyce JA. IL-4 and -5 prime human mast cells for different profiles of IgE-dependent cytokine production. Proc Natl Acad Sci USA. 2000;97(19):10509-10513. DOI: 10.1073/pnas.180318697.

66.

Barata LT, Ying S, Meng Q et al. IL-4- and IL-5-positive T lymphocytes, eosinophils, and mast cells in allergen-induced late-phase cutaneous reactions in atopic subjects. J Allergy Clin Immunol. 1998;101(2 Pt 1):222-230. DOI: 10.1016/s0091-6749(98)70387-2.

67.

Meininger CJ, Yano H, Rottapel R, Bernstein A, Zsebo KM, Zetter BR. The c-kit receptor ligand functions as a mast cell chemoattractant. Blood. 1992;79(4):958-963.

68.

Hartman M, Piliponsky AM, Temkin V, Levi-Schaffer F. Human peripheral blood eosinophils express stem cell factor. Blood. 2001;97(4):1086-1091. DOI: 10.1182/blood.v97.4.1086.

69.

De Paulis A, Minopoli G, Arbustini E et al. Stem cell factor is localized in, released from, and cleaved by human mast cells. J Immunol. 1999;163(5):2799-2808.

70.

Oliveira SH, Taub DD, Nagel J et al. Stem cell factor induces eosinophil activation and degranulation: mediator release and gene array analysis. Blood. 2002;100(13):4291-4297. DOI: 10.1182/blood.V100.13.4291.

71.

Ogasawara H, Furuno M, Edamura K, Noguchi M. Peptides of major basic protein and eosinophil cationic protein activate human mast cells. Biochem Biophys Rep. 2019;21:100719. Published 2019 Dec 25. DOI: 10.1016/j.bbrep.2019.100719.

72.

Piliponsky AM, Pickholtz D, Gleich GJ, Levi-Schaffer F. Human eosinophils induce histamine release from antigen-activated rat peritoneal mast cells: a possible role for mast cells in late-phase allergic reactions. J Allergy Clin Immunol. 2001;107(6):993-1000. DOI: 10.1067/mai.2001.114656.

73.

O’Donnell MC, Ackerman SJ, Gleich GJ, Thomas LL. Activation of basophil and mast cell histamine release by eosinophil granule major basic protein. J Exp Med. 1983;157(6):1981-1991. DOI: 10.1084/jem.157.6.1981.

74.

Zheutlin LM, Ackerman SJ, Gleich GJ, Thomas LL. Stimulation of basophil and rat mast cell histamine release by eosinophil granule-derived cationic proteins. J Immunol. 1984;133(4):2180-2185.

75.

Varricchi G, Pecoraro A, Loffredo S et al. Heterogeneity of Human Mast Cells With Respect to MRGPRX2 Receptor Expression and Function. Front Cell Neurosci. 2019;13:299. Published 2019 Jul 3. DOI: 10.3389/fncel.2019.00299.

76.

Гущин ИС. Об элементах биологической целесообразности аллергической реактивности. Патологическая физиология и экспериментальная терапия. 1979;(4):3-11 [Gushchin IS. Ob elementakh biologicheskoi tselesoobraznosti allergicheskoi reaktivnosti. Patologicheskaya fiziologiya i eksperimental’naya terapiya. 1979;(4):3-11 (In Russian)].

77.

Zeiger RS, Twarog FJ, Colten HR. Histaminase release from human granulocytes. J Exp Med. 1976;144(4):1049-1061. DOI: 10.1084/jem.144.4.1049.

78.

Zeiger RS, Colten HR. Histaminase release from human eosinophils. J Immunol. 1977;118(2):540-543.

79.

Herman JJ. Eosinophil diamine oxidase activity in acute inflammation in humans. Agents Actions. 1982;12(1-2):46-48. DOI: 10.1007/bf01965105.

80.

Popper H, Knipping G, Czarnetzki BM, Steiner R, Helleis G, Auer H. Activation and release of enzymes and major basic protein from guinea pig eosinophil granulocytes induced by different inflammatory stimuli and other substances. A histochemical, biochemical, and electron microscopic study. Inflammation. 1989;13(2):147-162. DOI: 10.1007/bf00924786.

81.

Weller PF, Austen KF. Human eosinophil arylsulfatase B. Structure and activity of the purified tetrameric lysosomal hydrolase. J Clin Invest. 1983;71(1):114-123. DOI: 10.1172/jci110739.

82.

Wasserman SI, Goetzl EJ, Austen KF. Inactivation of slow reacting substance of anaphylaxis by human eosinophil arylsulfatase. J Immunol. 1975;114(2 Pt 1):645-649.

83.

Kater LA, Goetzl EJ, Austen KF. Isolation of human eosinophil phospholipase D. J Clin Invest. 1976;57(5):1173-1180. DOI: 10.1172/JCI108385.

84.

Bartemes KR, McKinney S, Gleich GJ, Kita H. Endogenous platelet-activating factor is critically involved in effector functions of eosinophils stimulated with IL-5 or IgG. J Immunol. 1999;162(5):2982-2989.

85.

Hubscher T. Role of the eosinophil in the allergic reactions. II. Release of prostaglandins from human eosinophilic leukocytes. J Immunol. 1975;114(4):1389-1393.

86.

Takeda K, Shiraishi Y, Ashino S et al. Eosinophils contribute to the resolution of lung-allergic responses following repeated allergen challenge. J Allergy Clin Immunol. 2015;135(2):451-460. DOI: 10.1016/j.jaci.2014.08.014.

87.

Arita M. Mediator lipidomics in acute inflammation and resolution. J Biochem. 2012;152(4):313-319. DOI: 10.1093/jb/mvs092.

88.

Miyata J, Fukunaga K, Iwamoto R et al. Dysregulated synthesis of protectin D1 in eosinophils from patients with severe asthma. J Allergy Clin Immunol. 2013;131(2):353-60.e602. DOI: 10.1016/j.jaci.2012.07.048.

89.

Gleich GJ, Klion AD, Lee JJ, Weller PF. The consequences of not having eosinophils. Allergy. 2013;68(7):829-835. DOI: 10.1111/all.12169.

90.

Marichal T, Mesnil C, Bureau F. Homeostatic Eosinophils: Characteristics and Functions. Front Med (Lausanne). 2017;4:101. Published 2017 Jul 11. DOI: 10.3389/fmed.2017.00101.

91.

Kanda A, Yasutaka Y, Van Bui D et al. Multiple Biological Aspects of Eosinophils in Host Defense, Eosinophil-Associated Diseases, Immunoregulation, and Homeostasis: Is Their Role Beneficial, Detrimental, Regulator, or Bystander? Biol Pharm Bull. 2020;43(1):20-30. DOI: 10.1248/bpb.b19-00892.

92.

Shah K, Ignacio A, McCoy KD, Harris NL. The emerging roles of eosinophils in mucosal homeostasis [published online ahead of print, 2020 Mar 10]. Mucosal Immunol. 2020;10.1038/s41385-020-0281-y. DOI: 10.1038/s41385-020-0281-y.