Expression of the secondary granule proteins major basic protein 1 (MBP-1) and eosinophil peroxidase (EPX) is required for eosinophilopoiesis in mice

Blood

Volumn 122, Issue 5, 2013, Pages 781-790

  Doyle, Alfred D ^a   Jacobsen, Elizabeth A ^a   Ochkur, Sergei I ^a   McGarry, Michael P ^a   Shim, Kevin G ^a   Nguyen, David T C ^a   Protheroe, Cheryl ^a   Colbert, Dana ^a   Kloeber, Jake ^a   Neely, Joseph ^a   Shim, Kelly P ^a   Dyer, Kimberly D ^b   Rosenberg, Helene F ^b   Lee, James J ^a   Lee, Nancy A ^a  

^a MAYO GRADUATE SCHOOL   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EOSINOPHIL PEROXIDASE; INTERLEUKIN 5; MAJOR BASIC PROTEIN; MAJOR BASIC PROTEIN 1; TRANSCRIPTION FACTOR GATA 1; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE MARROW TRANSPLANTATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; EOSINOPHIL; EOSINOPHILOPOIESIS; EX VIVO STUDY; GENE INACTIVATION; HEMATOPOIESIS; IN VIVO STUDY; LEUKOCYTE COUNT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; ANIMAL; BONE MARROW CELL; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECT; GENETICS; KNOCKOUT MOUSE; METABOLISM; MYELOPOIESIS; PHYSIOLOGY;

ANIMALS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; EOSINOPHIL MAJOR BASIC PROTEIN; EOSINOPHIL PEROXIDASE; EOSINOPHILS; INTERLEUKIN-5; LEUKOCYTE COUNT; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOPOIESIS;

EID: 84886404834     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-01-473405     Document Type: Article

References (47)

1. Erlich P. Ueber die Specifischen granulationen des Blutes. [in German] Arch Anat Physiol. 1879; 3:571-579.
2. Lee JJ. In: Rosenberg HF, ed. Eosinophils in Health and Disease. Waltham, MA: Elsevier; 2012.
3. 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.
4. Barker RL, Gundel RH, Gleich GJ, Checkel JL, Loegering DA, Pease LR, Hamann KJ. Acidic polyamino acids inhibit human eosinophil granule major basic protein toxicity. Evidence of a functional role for ProMBP. J Clin Invest. 1991; 88(3):798-805.
5. Larson KA, Horton MA, Madden BJ, Gleich GJ, Lee NA, Lee JJ. The identification and cloning of a murine major basic protein gene expressed in eosinophils. J Immunol. 1995;155(6):3002-3012.
6. Macias MP, Welch KC, Denzler KL, Larson KA, Lee NA, Lee JJ. Identification of a new murine eosinophil major basic protein (mMBP) gene: cloning and characterization of mMBP-2. J Leukoc Biol. 2000;67(4):567-576.
7. Plager DA, Loegering DA, Weiler DA, et al. A novel and highly divergent homolog of human eosinophil granule major basic protein. J Biol Chem. 1999;274(20):14464-14473.
8. Rosenberg HF, Tenen DG, Ackerman SJ. Molecular cloning of the human eosinophilderived neurotoxin: a member of the ribonuclease gene family. Proc Natl Acad Sci USA. 1989; 86(12):4460-4464.
9. Rosenberg HF, Ackerman SJ, Tenen DG. Human eosinophil cationic protein. Molecular cloning of a cytotoxin and helminthotoxin with ribonuclease activity. J Exp Med. 1989;170(1):163-176.
10. Cormier SA, Larson KA, Yuan S, et al. Mouse eosinophil-associated ribonucleases: a unique subfamily expressed during hematopoiesis. Mamm Genome. 2001;12(5):352-361.
11. Larson KA, Olson EV, Madden BJ, Gleich GJ, Lee NA, Lee JJ. Two highly homologous ribonuclease genes expressed in mouse eosinophils identify a larger subgroup of the mammalian ribonuclease superfamily. Proc Natl Acad Sci USA. 1996; 93(22):12370-12375.
12. Horton MA, Larson KA, Lee JJ, Lee NA. Cloning of the murine eosinophil peroxidase gene (mEPO): characterization of a conserved subgroup of mammalian hematopoietic peroxidases. J Leukoc Biol. 1996;60(2):285-294.
13. Ten RM, Pease LR, McKean DJ, Bell MP, Gleich GJ. Molecular cloning of the human eosinophil peroxidase. Evidence for the existence of a peroxidase multigene family. J Exp Med. 1989; 169(5):1757-1769.
14. Ackerman SJ, Loegering DA, Venge P, Olsson I, Harley JB, Fauci AS, Gleich GJ. Distinctive cationic proteins of the human eosinophil granule: major basic protein, eosinophil cationic protein, and eosinophil-derived neurotoxin. J Immunol. 1983;131(6):2977-2982.
15. Rothenberg ME, Hogan SP. The eosinophil. Annu Rev Immunol. 2006;24:147-174.
16. Denzler KL, Farmer SC, Crosby JR, et al. Eosinophil major basic protein-1 does not contribute to allergen-induced airway pathologies in mouse models of asthma. J Immunol. 2000; 165(10):5509-5517.
17. Denzler KL, Borchers MT, Crosby JR, et al. Extensive eosinophil degranulation and peroxidase-mediated oxidation of airway proteins do not occur in a mouse ovalbumin-challenge model of pulmonary inflammation. J Immunol. 2001;167(3):1672-1682.
18. O'Connell AE, Hess JA, Santiago GA, Nolan TJ, Lok JB, Lee JJ, Abraham D. Major basic protein from eosinophils and myeloperoxidase from neutrophils are required for protective immunity to Strongyloides stercoralis in mice. Infect Immun. 2011;79(7):2770-2778.
19. Wehling-Henricks M, Sokolow S, Lee JJ, Myung KH, Villalta SA, Tidball JG. Major basic protein-1 promotes fibrosis of dystrophic muscle and attenuates the cellular immune response in muscular dystrophy. Hum Mol Genet. 2008; 17(15):2280-2292.
20. Specht S, Saeftel M, Arndt M, et al. Lack of eosinophil peroxidase or major basic protein impairs defense against murine filarial infection. Infect Immun. 2006;74(9):5236-5243.
21. Forbes E, Murase T, Yang M, et al. Immunopathogenesis of experimental ulcerative colitis is mediated by eosinophil peroxidase. J Immunol. 2004;172(9):5664-5675.
22. Mori Y, Iwasaki H, Akashi K. Eosinophil Lineage-Committed Progenitors. In: Lee JJ, Rosenberg HF, eds. Eosinophils in Health and Disease. Waltham, MA: Academic Press, Elsevier; 2012: 89-97.
23. Wintrobe MM, Greer JP. Wintrobe's clinical hematology, 12th ed. Philadelphia: Wolters Kluwer/Lippincott Williams & Wilkins Health; 2009.
24. Hartmann J, Scepek S, Lindau M. Regulation of granule size in human and horse eosinophils by number of fusion events among unit granules. J Physiol. 1995;483(Pt 1):201-209.
25. Hammel I, Lagunoff D, Galli SJ. Regulation of secretory granule size by the precise generation and fusion of unit granules. J Cell Mol Med. 2010; 14(7):1904-1916.
26. Jacobsen EA, Helmers RA, Lee JJ, Lee NA. The expanding role(s) of eosinophils in health and disease. Blood. 2012;120(19):3882-3890.
27. Lee JJ, Dimina D, Macias MP, et al. Defining a link with asthma in mice congenitally deficient in eosinophils. Science. 2004;305(5691):1773-1776.
28. Lee NA, McGarry MP, Larson KA, Horton MA, Kristensen AB, Lee JJ. Expression of IL-5 in thymocytes/T cells leads to the development of a massive eosinophilia, extramedullary eosinophilopoiesis, and unique histopathologies. J Immunol. 1997;158(3):1332-1344.
29. McGarry MP, Protheroe CA, Lee JJ. Mouse Hematology. A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Laboratory Press; 2009.
30. Obata K, Mukai K, Tsujimura Y, et al. Basophils are essential initiators of a novel type of chronic allergic inflammation. Blood. 2007;110(3): 913-920.
31. Iwasaki H, Mizuno S, Mayfield R, et al. Identification of eosinophil lineage-committed progenitors in the murine bone marrow. J Exp Med. 2005;201(12):1891-1897.
32. de Bruin AM, Buitenhuis M, van der Sluijs KF, van Gisbergen KP, Boon L, Nolte MA. Eosinophil differentiation in the bone marrow is inhibited by T cell-derived IFN-gamma. Blood. 2010;116(14): 2559-2569.
33. Ochkur SI, Jacobsen EA, Protheroe CA, et al. Coexpression of IL-5 and eotaxin-2 in mice creates an eosinophil-dependent model of respiratory inflammation with characteristics of severe asthma. J Immunol. 2007;178(12): 7879-7889.
34. Cormier SA, Yuan S, Crosby JR, et al. T(H)2-mediated pulmonary inflammation leads to the differential expression of ribonuclease genes by alveolar macrophages. Am J Respir Cell Mol Biol. 2002;27(6):678-687.
35. Dyer KD, Moser JM, Czapiga M, Siegel SJ, Percopo CM, Rosenberg HF. Functionally competent eosinophils differentiated ex vivo in high purity from normal mouse bone marrow. J Immunol. 2008;181(6):4004-4009.
36. Doyle AD, Jacobsen EA, Ochkur SI, et al. Homologous recombination into the eosinophil peroxidase locus generates a strain of mice expressing Cre recombinase exclusively in eosinophils. J Leukoc Biol. 2013;94:17-24.
37. Yu C, Cantor AB, Yang H, Browne C, Wells RA, Fujiwara Y, Orkin SH. Targeted deletion of a highaffinity GATA-binding site in the GATA-1 promoter leads to selective loss of the eosinophil lineage in vivo. J Exp Med. 2002;195(11):1387-1395.
38. Lee JJ, Lee NA. Eosinophil degranulation: an evolutionary vestige or a universally destructive effector function? Clin Exp Allergy. 2005;35(8): 986-994.
39. Butterfield JH, Ackerman SJ, Scott RE, Pierre RV, Gleich GJ. Evidence for secretion of human eosinophil granule major basic protein and Charcot-Leyden crystal protein during eosinophil maturation. Exp Hematol. 1984;12(3):163-170.
40. Donadieu J, Fenneteau O, Beaupain B, Mahlaoui N, Chantelot CB. Congenital neutropenia: diagnosis, molecular bases and patient management. Orphanet J Rare Dis. 2011;6:26.
41. Klein C. Genetic defects in severe congenital neutropenia: emerging insights into life and death of human neutrophil granulocytes. Annu Rev Immunol. 2011;29:399-413.
42. Grenda DS, Johnson SE, Mayer JR, McLemore ML, Benson KF, Horwitz M, Link DC. Mice expressing a neutrophil elastase mutation derived from patients with severe congenital neutropenia have normal granulopoiesis. Blood. 2002;100(9): 3221-3228.
43. Nanua S, Murakami M, Xia J, Grenda DS, Woloszynek J, Strand M, Link DC. Activation of the unfolded protein response is associated with impaired granulopoiesis in transgenic mice expressing mutant Elane. Blood. 2011;117(13): 3539-3547.
44. Lu TX, Lim EJ, Besse JA, et al. MiR-223 deficiency increases eosinophil progenitor proliferation. J Immunol. 2013;190(4):1576-1582.
45. Wagner LA, Christensen CJ, Dunn DM, et al. EGO, a novel, noncoding RNA gene, regulates eosinophil granule protein transcript expression. Blood. 2007;109(12):5191-5198.
46. Wills-Karp M, Karp CL. Biomedicine. Eosinophils in asthma: remodeling a tangled tale. Science. 2004;305(5691):1726-1729.
47. Ferreira R, Ohneda K, Yamamoto M, Philipsen S. GATA1 function, a paradigm for transcription factors in hematopoiesis. Mol Cell Biol. 2005; 25(4):1215-1227.