medigraphic.com
ISSN 2500-7106 (Electronic)
ISSN 0123-2576 (Print)
Medicina & Laboratorio

2022, Number 2

<< Back Next >>

Medicina & Laboratorio 2022; 26 (2)

Eosinophil depletion: many implications in murine models, few studied in humans

Gil GM, Cardona R

Language: Spanish
References: 71
Page: 141-157
PDF size: 187.06 Kb.


ABSTRACT

The eosinophil is a cell of the immune system, with an arsenal of substances that can alter the balance that exists in the different organs where they are found. With the advent of monoclonal antibodies, concern about their depletion has become an important turning point in their formulation. For this reason, it is of vital importance to investigate the consequences of the mechanism of action of biological agents, in the short and long term. This review tries to show the role of eosinophils in both homeostasis and disease, and their relationship and interaction with monoclonal drugs in diseases focused on the Th2 profile. It is expected that this article can be useful when making the decision to start treatment with monoclonals, specifically anti-interleukin-5 or against its receptor.


REFERENCES

  1. Rothenberg ME, Hogan SP. The eosinophil.Annu Rev Immunol 2006;24:147-174.https://doi.org/10.1146/annurev.immunol. 24.021605.090720.

  2. Renz H, Bachert C, Berek C, Hamelmann E,Levi-Schaffer F, Raap U, et al. Physiology andpathology of eosinophils: Recent developments:Summary of the Focus Workshop Organizedby DGAKI. Scand J Immunol 2021;93:e13032.https://doi.org/10.1111/sji.13032.

  3. Jackson DJ, Akuthota P, Roufosse F. Eosinophilsand eosinophilic immune dysfunction in healthand disease. Eur Respir Rev 2022;31:210150.https://doi.org/10.1183/16000617.0150-2021.

  4. Yamaguchi T, Takizawa F, Fischer U, DijkstraJM. Along the axis between type 1 and type2 immunity; principles conserved in evolutionfrom fish to mammals. Biology 2015;4:814-859.https://doi.org/10.3390/biology4040814.

  5. Gieseck RL, Wilson MS, Wynn TA. Type 2 immunityin tissue repair and fibrosis. Nat Rev Immunol2018;18:62-76. https://doi.org/10.1038/nri.2017.90.

  6. Lotfi R, Lee JJ, Lotze MT. Eosinophilic granulocytesand damage-associated molecularpattern molecules (DAMPs): role in the inflammatoryresponse within tumors. J Immunother2007;30:16-28. https://doi.org/10.1097/01.cji.0000211324.53396.f6.

  7. Elsas PX, Elsas MI. Eosinophilopoiesis atthe cross-roads of research on development,immunity and drug discovery. CurrMed Chem 2007;14:1925-1939. https://doi.org/10.2174/092986707781368487.

  8. Liu LY, Bates ME, Jarjour NN, Busse WW, BerticsPJ, Kelly EA. Generation of Th1 and Th2chemokines by human eosinophils: evidencefor a critical role of TNF-alpha. J Immunol2007;179:4840-4848. https://doi.org/10.4049/jimmunol.179.7.4840.

  9. Butterfield JH, Ackerman SJ, Scott RE, PierreRV, Gleich GJ. Evidence for secretionof human eosinophil granule major basicprotein and Charcot-Leyden crystal proteinduring eosinophil maturation. Exp Hematol1984;12:163-170.

  10. Furuta GT, Nieuwenhuis EE, Karhausen J,Gleich G, Blumberg RS, Lee JJ, et al. Eosinophilsalter colonic epithelial barrier function:role for major basic protein. Am J Physiol GastrointestLiver Physiol 2005;289:G890-897.https://doi.org/10.1152/ajpgi.00015.2005.

  11. Jung Y, Wen T, Mingler MK, Caldwell JM,Wang YH, Chaplin DD, et al. IL-1β in eosinophil-mediated small intestinal homeostasis andIgA production. Mucosal Immunol 2015;8:930-942. https://doi.org/10.1038/mi.2014.123.

  12. Chu VT, Beller A, Rausch S, Strandmark J,Zänker M, Arbach O, et al. Eosinophils promotegeneration and maintenance of immunoglobulin-A-expressing plasma cells and contributeto gut immune homeostasis. Immunity2014;40:582-593. https://doi.org/10.1016/j.immuni.2014.02.014.

  13. Sugawara R, Lee EJ, Jang MS, Jeun EJ, HongCP, Kim JH, et al. Small intestinal eosinophilsregulate Th17 cells by producing IL-1 receptorantagonist. J Exp Med 2016;213:555-567.https://doi.org/10.1084/jem.20141388.

  14. Withers SB, Forman R, Meza-Perez S, SorobeteaD, Sitnik K, Hopwood T, et al. Eosinophilsare key regulators of perivascularadipose tissue and vascular functionality. SciRep 2017;7:44571. https://doi.org/10.1038/srep44571.

  15. Uderhardt S, Ackermann JA, Fillep T, HammondVJ, Willeit J, Santer P, et al. Enzymaticlipid oxidation by eosinophils propagates coagulation,hemostasis, and thrombotic disease.J Exp Med 2017;214:2121-2138. https://doi.org/10.1084/jem.20161070.

  16. Throsby M, Herbelin A, Pléau JM, DardenneM. CD11c+ eosinophils in the murine thymus:developmental regulation and recruitmentupon MHC class I-restricted thymocyte deletion.J Immunol 2000;165:1965-1975. https://doi.org/10.4049/jimmunol.165.4.1965.

  17. Brestoff JR, Kim BS, Saenz SA, Stine RR,Monticelli LA, Sonnenberg GF, et al. Group2 innate lymphoid cells promote beiging ofwhite adipose tissue and limit obesity. Nature2015;519:242-246. https://doi.org/10.1038/nature14115.

  18. Suárez-Zamorano N, Fabbiano S, ChevalierC, Stojanović O, Colin DJ, Stevanović A, etal. Microbiota depletion promotes browningof white adipose tissue and reduces obesity.Nat Med 2015;21:1497-1501. https://doi.org/10.1038/nm.3994.

  19. Gouon-Evans V, Rothenberg ME, PollardJW. Postnatal mammary gland developmentrequires macrophages and eosinophils. Development

  20. 2000;127:2269-2282. https://doi.org/10.1242/dev.127.11.2269.20. Gouon-Evans V, Pollard JW. Eotaxin is requiredfor eosinophil homing into the stroma ofthe pubertal and cycling uterus. Endocrinology2001;142:4515-4521. https://doi.org/10.1210/endo.142.10.8459.

  21. Yu C, Cantor AB, Yang H, Browne C, WellsRA, Fujiwara Y, et al. Targeted deletion of ahigh-affinity GATA-binding site in the GATA-1promoter leads to selective loss of the eosinophillineage in vivo. J Exp Med 2002;195:1387-1395. https://doi.org/10.1084/jem.20020656.

  22. Mesnil C, Raulier S, Paulissen G, Xiao X, BirrellMA, Pirottin D, et al. Lung-resident eosinophilsrepresent a distinct regulatory eosinophilsubset. J Clin Invest 2016;126:3279-3295.https://doi.org/10.1172/jci85664.

  23. Zhu C, Weng QY, Zhou LR, Cao C, Li F, Wu YF,et al. Homeostatic and early-recruited CD101(-)eosinophils suppress endotoxin-induced acutelung injury. Eur Respir J 2020;56. https://doi.org/10.1183/13993003.02354-2019.

  24. Jacobsen EA, Jackson DJ, Heffler E, MathurSK, Bredenoord AJ, Pavord ID, et al. Eosinophilknockout humans: Uncovering the roleof eosinophils through eosinophil-directedbiological therapies. Annu Rev Immunol2021;39:719-757. https://doi.org/10.1146/annurev-immunol-093019-125918.

  25. Reichman H, Itan M, Rozenberg P, YarmolovskiT, Brazowski E, Varol C, et al.Activated eosinophils exert antitumorigenicactivities in colorectal cancer. CancerImmunol Res 2019;7:388-400. https://doi.org/10.1158/2326-6066.Cir-18-0494.

  26. Hollande C, Boussier J, Ziai J, Nozawa T,Bondet V, Phung W, et al. Inhibition of thedipeptidyl peptidase DPP4 (CD26) reveals IL-33-dependent eosinophil-mediated control oftumor growth. Nat Immunol 2019;20:257-264.https://doi.org/10.1038/s41590-019-0321-5.

  27. Fabre V, Beiting DP, Bliss SK, GebreselassieNG, Gagliardo LF, Lee NA, et al. Eosinophildeficiency compromises parasite survivalin chronic nematode infection. J Immunol2009;182:1577-1583. https://doi.org/10.4049/jimmunol.182.3.1577.

  28. Stein LH, Redding KM, Lee JJ, Nolan TJ,Schad GA, Lok JB, et al. Eosinophils utilizemultiple chemokine receptors for chemotaxisto the parasitic nematode Strongyloides stercoralis.J Innate Immun 2009;1:618-630. https://doi.org/10.1159/000233235.

  29. Puxeddu I, Berkman N, Nissim Ben EfraimAH, Davies DE, Ribatti D, Gleich GJ, et al. Therole of eosinophil major basic protein in angiogenesis.Allergy 2009;64:368-374. https://doi.org/10.1111/j.1398-9995.2008.01822.x.

  30. Heredia JE, Mukundan L, Chen FM, MuellerAA, Deo RC, Locksley RM, et al. Type 2innate signals stimulate fibro/adipogenic progenitorsto facilitate muscle regeneration. Cell2013;153:376-388. https://doi.org/10.1016/j.cell.2013.02.053.

  31. Puxeddu I, Berkman N, Ribatti D, Bader R,Haitchi HM, Davies DE, et al. Osteopontinis expressed and functional in human eosinophils.Allergy 2010;65:168-174. https://doi.org/10.1111/j.1398-9995.2009.02148.x.

  32. Percopo CM, Dyer KD, Ochkur SI, Luo JL, FischerER, Lee JJ, et al. Activated mouse eosinophilsprotect against lethal respiratory virusinfection. Blood 2014;123:743-752. https://doi.org/10.1182/blood-2013-05-502443.

  33. Samarasinghe AE, Melo RC, Duan S, Le-Messurier KS, Liedmann S, Surman SL, etal. Eosinophils promote antiviral immunity inmice infected with influenza a virus. J Immunol2017;198:3214-3226. https://doi.org/10.4049/jimmunol.1600787.

  34. Wehling-Henricks M, Sokolow S, Lee JJ,Myung KH, Villalta SA, Tidball JG. Major basicprotein-1 promotes fibrosis of dystrophicmuscle and attenuates the cellular immune responsein muscular dystrophy. Hum Mol Genet2008;17:2280-2292. https://doi.org/10.1093/hmg/ddn129.

  35. Padigel UM, Hess JA, Lee JJ, Lok JB, NolanTJ, Schad GA, et al. Eosinophils act asantigen-presenting cells to induce immunityto Strongyloides stercoralis in mice. J InfectDis 2007;196:1844-1851. https://doi.org/10.1086/522968.

  36. Mattes J, Yang M, Mahalingam S, Kuehr J,Webb DC, Simson L, et al. Intrinsic defect inT cell production of interleukin (IL)-13 in theabsence of both IL-5 and eotaxin precludes thedevelopment of eosinophilia and airways hyperreactivityin experimental asthma. J Exp Med2002;195:1433-1444. https://doi.org/10.1084/jem.20020009.

  37. Spencer LA, Szela CT, Perez SAC, KirchhofferCL, Neves JS, Radke AL, et al. Human eosinophilsconstitutively express multiple Th1, Th2,and immunoregulatory cytokines that are secretedrapidly and differentially. J Leukoc Biol2009;85:117-123. https://doi.org/10.1189/jlb.0108058.

  38. Odemuyiwa SO, Ghahary A, Li Y, PuttaguntaL, Lee JE, Musat-Marcu S, et al. Cutting edge:human eosinophils regulate T cell subset selectionthrough indoleamine 2,3-dioxygenase.J Immunol 2004;173:5909-5913. https://doi.org/10.4049/jimmunol.173.10.5909.

  39. Wong DT, Bowen SM, Elovic A, Gallagher GT,Weller PF. Eosinophil ablation and tumor development.Oral Oncol 1999;35:496-501. https://doi.org/10.1016/s1368-8375(99)00023-8.

  40. Simson L, Ellyard JI, Dent LA, Matthaei KI,Rothenberg ME, Foster PS, et al. Regulationof carcinogenesis by IL-5 and CCL11: a potentialrole for eosinophils in tumor immunesurveillance. J Immunol 2007;178:4222-4229.https://doi.org/10.4049/jimmunol.178.7.4222.

  41. Zaynagetdinov R, Sherrill TP, Gleaves LA,McLoed AG, Saxon JA, Habermann AC, etal. Interleukin-5 facilitates lung metastasis bymodulating the immune microenvironment.Cancer Res 2015;75:1624-1634. https://doi.org/10.1158/0008-5472.Can-14-2379.

  42. Carretero R, Sektioglu IM, Garbi N, SalgadoOC, Beckhove P, Hämmerling GJ. Eosinophilsorchestrate cancer rejection by normalizingtumor vessels and enhancing infiltration ofCD8(+) T cells. Nat Immunol 2015;16:609-617.https://doi.org/10.1038/ni.3159.

  43. Lee JJ, Protheroe CA, Luo H, Ochkur SI, ScottGD, Zellner KR, et al. Eosinophil-dependentskin innervation and itching followingcontact toxicant exposure in mice. J AllergyClin Immunol 2015;135:477-487. https://doi.org/10.1016/j.jaci.2014.07.003.

  44. Radonjic-Hoesli S, Brüggen MC, FeldmeyerL, Simon HU, Simon D. Eosinophils in skin diseases.Semin Immunopathol 2021;43:393-409.https://doi.org/10.1007/s00281-021-00868-7.

  45. Huang L, Appleton JA. Eosinophils in helminthinfection: Defenders and dupes. Trends Parasitol2016;32:798-807. https://doi.org/10.1016/j.pt.2016.05.004.

  46. Yasuda K, Kuroda E. Role of eosinophils in protectiveimmunity against secondary nematodeinfections. Immunol Med 2019;42:148-155.https://doi.org/10.1080/25785826.2019.1697135.

  47. Kuang FL. Approach to patients with eosinophilia.Med Clin North Am 2020;104:1-14. https://doi.org/10.1016/j.mcna.2019.08.005.

  48. Blumenthal KG, Youngster I, Rabideau DJ,Parker RA, Manning KS, Walensky RP, etal. Peripheral blood eosinophilia and hypersensitivityreactions among patients receivingoutpatient parenteral antibiotics. J Allergy ClinImmunol 2015;136:1288-1294. https://doi.org/10.1016/j.jaci.2015.04.005.

  49. Klion AD. Eosinophilia: a pragmatic approachto diagnosis and treatment. HematologyAm Soc Hematol Educ Program2015;2015:92-97. https://doi.org/10.1182/asheducation-2015.1.92.

  50. Doherty TA, Baum R, Newbury RO, YangT, Dohil R, Aquino M, et al. Group 2 innatelymphocytes (ILC2) are enriched in active eosinophilicesophagitis. J Allergy Clin Immunol2015;136:792-794. https://doi.org/10.1016/j.jaci.2015.05.048.

  51. Mishra A, Rothenberg ME. Intratracheal IL-13induces eosinophilic esophagitis by an IL-5, eotaxin-1, and STAT6-dependent mechanism. Gastroenterology2003;125:1419-1427. https://doi.org/10.1016/j.gastro.2003.07.007.

  52. Youngblood BA, Brock EC, Leung J, FalahatiR, Bochner BS, Rasmussen HS, et al. Siglec-8antibody reduces eosinophils and mast cells ina transgenic mouse model of eosinophilic gastroenteritis.JCI Insight 2019;4:e126219. https://doi.org/10.1172/jci.insight.126219.

  53. Yan B, Yang J, Xie Y, Tang X. Relationshipbetween blood eosinophil levels and COVID-19 mortality. World Allergy Organ J2021;14:100521. https://doi.org/10.1016/j.waojou.2021.100521.

  54. Jia Y, Yu H, Fernandes SM, Wei Y, Gonzalez-GilA, Motari MG, et al. Expression of ligands for Siglec-8 and Siglec-9 in human airways and airwaycells. J Allergy Clin Immunol 2015;135:799-810.https://doi.org/10.1016/j.jaci.2015.01.004.

  55. Rank MA, Ochkur SI, Lewis JC, Teaford HG,3rd, Wesselius LJ, Helmers RA, et al. Nasaland pharyngeal eosinophil peroxidase levels inadults with poorly controlled asthma correlatewith sputum eosinophilia. Allergy 2016;71:567-570. https://doi.org/10.1111/all.12817.

  56. Lee JJ, Jacobsen EA, McGarry MP, SchleimerRP, Lee NA. Eosinophils in health and disease:the LIAR hypothesis. Clin Exp Allergy2010;40:563-575. https://doi.org/10.1111/j.1365-2222.2010.03484.x.

  57. Shen HH, Ochkur SI, McGarry MP, Crosby JR,Hines EM, Borchers MT, et al. A causative relationshipexists between eosinophils and thedevelopment of allergic pulmonary pathologiesin the mouse. J Immunol 2003;170:3296-3305.https://doi.org/10.4049/jimmunol.170.6.3296.

  58. Jacobsen EA, Ochkur SI, Doyle AD, LeSuerWE, Li W, Protheroe CA, et al. Lung pathologiesin a chronic inflammation mouse model areindependent of eosinophil degranulation. AmJ Respir Crit Care Med 2017;195:1321-1332.https://doi.org/10.1164/rccm.201606-1129OC.

  59. Doyle AD, Mukherjee M, LeSuer WE, BittnerTB, Pasha SM, Frere JJ, et al. Eosinophil-derived IL-13 promotes emphysema.Eur Respir J 2019;53:1801291. https://doi.org/10.1183/13993003.01291-2018.

  60. Bou-Ghanem EN. mSphere of influence:Adenosine in host defense against bacterialpneumonia-friend or foe? mSphere2019;4:e00326-00319. https://doi.org/10.1128/mSphere.00326-19.

  61. Jacobsen EA, LeSuer WE, Nazaroff CD,Ochkur SI, Doyle AD, Wright BL, et al. Eosinophilsinduce recruitment and activation of ILC2s.J Allergy Clin Immunol Pract 2019;143:AB289.https://doi.org/10.1016/j.jaci.2018.12.885.

  62. Kuang FL, Bochner BS. Lessons learned fromtargeting eosinophils in human disease. SeminImmunopathol 2021;43:459-475. https://doi.org/10.1007/s00281-021-00849-w.

  63. Akdis CA, Arkwright PD, Brüggen MC, BusseW, Gadina M, Guttman-Yassky E, et al.Type 2 immunity in the skin and lungs. Allergy2020;75:1582-1605. https://doi.org/10.1111/all.14318.

  64. Moran AM, Ramakrishnan S, Borg CA, ConnollyCM, Couillard S, Mwasuku CM, et al.Blood eosinophil depletion with mepolizumab,benralizumab, and prednisolone in eosinophilicasthma. Am J Respir Crit Care Med2020;202:1314-1316. https://doi.org/10.1164/rccm.202003-0729LE.

  65. Nair P, Wenzel S, Rabe KF, Bourdin A, LugogoNL, Kuna P, et al. Oral glucocorticoid-sparingeffect of benralizumab in severe asthma. NEngl J Med 2017;376:2448-2458. https://doi.org/10.1056/NEJMoa1703501.

  66. Bleecker ER, FitzGerald JM, Chanez P, PapiA, Weinstein SF, Barker P, et al. Efficacy andsafety of benralizumab for patients with severeasthma uncontrolled with high-dosageinhaled corticosteroids and long-acting β(2)-agonists (SIROCCO): a randomised, multicentre,placebo-controlled phase 3 trial. Lancet2016;388:2115-2127. https://doi.org/10.1016/s0140-6736(16)31324-1.

  67. Busse WW, Bleecker ER, FitzGerald JM, FergusonGT, Barker P, Sproule S, et al. Long-termsafety and efficacy of benralizumab in patientswith severe, uncontrolled asthma: 1-year resultsfrom the BORA phase 3 extension trial.Lancet Respir Med 2019;7:46-59. https://doi.org/10.1016/s2213-2600(18)30406-5.

  68. Jackson DJ, Korn S, Mathur SK, Barker P,Meka VG, Martin UJ, et al. Safety of eosino-phil-depleting therapy for severe, eosinophilicasthma: Focus on benralizumab. Drug Saf2020;43:409-425. https://doi.org/10.1007/s40264-020-00926-3.

  69. Har D, Bird JA. Efficacy and safety of benralizumabfor patients with severe asthma uncontrolledwith high-dosage inhaled corticosteroidsand long-acting β2-agonists (SIROCCO): Arandomised, multicentre, placebo-controlledphase 3 trial. Pediatrics 2017;140:S224-S225.https://doi.org/10.1542/peds.2017-2475LLLL.

  70. FitzGerald JM, Bleecker ER, Nair P, Korn S,Ohta K, Lommatzsch M, et al. Benralizumab,an anti-interleukin-5 receptor α monoclonalantibody, as add-on treatment for patientswith severe, uncontrolled, eosinophilic asthma(CALIMA): a randomised, double-blind,placebo-controlled phase 3 trial. Lancet2016;388:2128-2141. https://doi.org/10.1016/s0140-6736(16)31322-8.

  71. Khatri S, Moore W, Gibson PG, Leigh R,Bourdin A, Maspero J, et al. Assessment ofthe long-term safety of mepolizumab and durabilityof clinical response in patients withsevere eosinophilic asthma. J Allergy ClinImmunol 2019;143:1742-1751. https://doi.org/10.1016/j.jaci.2018.09.033.




2020     |     www.medigraphic.com