molecular and cellular properties of eosinophils

Department of Pathology, Harvard Medical School and the Brigham and Women's Hospital, Boston, Mass.

MOLECULAR AND CELLULAR PROPERTIES OF EOSINOPHILS

(A review)

JOHN A. SMITH

Akhough the morphology of the eosinophil was described initially by WHARTON- JONES TM, its sanguine chromaticity led EHRLICH 34 to name the cell. Two mono- graphs H,s5 and several reviews ~*'53,n'gg'ns,ns,~29 devoted exclusively to the structure and function of the eosinophil have been published. However, the specific biochemical details regarding the eosinophit's affector and effector mechanisms, the differences between blood and tissue eosinophils, and the alterations among eosinophil subpopulations, are still largely enigmatic.

Peripheral blood and tissue eosinophilia are frequently associated with immunologic, parasitic, and neoplastic conditions. However, the chemical mechanisms used by eosinophils to regulate immediate-type hypersensitivity reactions or to destroy antibody-coated, invasive parasites are, with rare exception, undetermined. Recent advances establishing the composition of the Charcot-Leyden crystals, the failure of arylsulfatase B to inactivate slow reacting substance (SRS-A), and the likelihood of a membrane chaotropic role for reduced and alkylated major basic protein are among the signal observations that are discussed herein. In addition, this review summarizes and emphasizes the biochemistry of the known eosinophilic affector/ef- lector mechanisms and their relationship to certain pathogenetic conditions.

It should be emphasized that contemporary knowledge of the biochemical and cellular aspects of the eosinophil is incomplete and, although this review purports to give a summary of what is known, many details are still uncertain.

Key-words: Arylsulfatase B; Biological properties; Cationic proteins; Charcot-Leyden crystals; Chemical properties; Chemo- taxis; Complement receptors; Eosinophils; Eosinopoiesis; Hetminthie infections; Histaminase; Immediate hypersensitivity; Lysophaspholipase; Major basic protein; Peroxidase; Phospholipase D; Phospholipid exchange protein; Slow reacting substance of anaphylaxis.

Accepted for publication on May 29, 1981. La Ricerca Cfin. Lab. 11, 181, 1981.

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l . M O L E C U L A R P R O P E R T I E S OF E O S I N O P H I L I C P R O T E I N S

Until recently most of the biochemical information about the eosinophil's enzymes, major basic protein, and cationic proteins was derived from studies of eosinophils isolated from horses, rats, and guinea pigs. Rat and horse eosinophils contain peroxidase, acid phosphatase, alkaline phosphatase, arylsulfatase B, ~-glucuronidase, ribonuclease, and cathepsin 4. WEST et aI.~33 demonstrated a two-fold (or greater) concentration of peroxidase, ~-glucuronidase, and acid phosphatase in human eosinophils, as compared to human neutrophils, and they determined that these enzymes were located in the cytoplasmic large granule. In the light of the known occurrence of alkaline phosphatase in other species 4, their failure to demonstrate this enzyme in the human eosinophil is probably an artefact.

All of these enzymes are recognized because there are available biochemical as- says for detecting them. Many of these enzymes are ubiquitous, and, unless unique biological function(s) can be attributed to an eosinophit enzyme per se, it is unlikely that these enzymes are functionally important in vivo. Undoubtedly, there are nu- merous other biologically active secretory and membrane-bound proteins, which remain to be isolated and characterized. This review discusses only the following eosinophil proteins: histaminase, peroxidase, arylsulfatase B, phospholipase D, lysophospholipase, phospholipid exchange protein, major basic protein, and cationic proteins.

a. Histaminase

Both neutrophilic and eosinophilic granulocytes contain histaminase 136. Although eosinophilic histaminase is touted as a regulator of immediate hypersensitivity reactions by virtue of its propensity to degrade histamine 49, there is no evidence to support that this selective degradative pathway exists in vivo.

b. P eroxidase

Human eosinophilic peroxidase (EPO) has the capability of iodinating proteins via the peroxidase-H202-halogen reaction - a bactericidal pathway - as does neutrophilic peroxidase (MPO) 93. However, in contrast to a decrease in neutrophilic bactericidal activity that results from sodium azide inhibition, azide inhibition of EPO leads to an enhancement of eosinophilic bactericidal activity 13. This functional dif- ference cannot be attributed to differences in enzymic inhibition by azide, since EPO is more suscepdble to azide (and less susceptible to cyanide) inhibition than MPO 5,29,92. The failure of EPO to function bactericidally may result from its inability to decarboxylate amino acids effectively or to catalyze the necessary tripartite reaction in the presence of chloride 29. In addition to these biochemical differences, there are spectral differences between EPO and MPO in both the visible and Soret regions 3.

c. Arylsulfatase B

Arylsulfatase B (ASB) is a tetrameric protein with 15,000 dalton subunits 132. Pre- sumably, these are distinct ~x- and ~-subunits, although amino acid sequence analysis and structure-functional analysis have not been completed.

The eosinophil contains ten to twenty times more ASB than the neutrophi113~. Previous studies with the partially purified enzyme indicate that sulfur-containing slow reacting substance of anaphylaxis (SRS-A) was inactivated by ASB, although the

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mechanism of this inactivation was unclear ns. The substrate specificity of ASB re-

R i I

quires the presence of a sulfone O=S=O or aromatic sulfate for enzymic cleavage 97.

Recently, it has been shown that one constituent of SRS-A, designated leukotriene C4 (LTC4), is a lipoxygenase-derived 5-hydroxy-7,9,1 1,14-eicosatetraenoic acid with a thioether-linked glutathione (i.e. glutamyl-cysteinyt-glycyl) located at the sixth carbon atom of the fatty acid moiety 59,96. Such a thioether linkage should not be susceptible to enzyme degradation by ASB and indeed is not apparently cleaved by highly purified enzyme i31. The inactivation of SRS-A in earlier studies with impure enzyme may have resulted from cleavage of constituent amino acids from the glu- tathionyl moiety of LTC4 by contaminating proteases 100

Alternatively, other active, non-leukotriene SRS-A compounds susceptible to cleavage by ASB may also exist 97. The binding of SRS-A and its family of leukotrienes in a specific inhibitory manner to one (or more) of the subunits of ASB is also a possible mechanism accounting for apparendy diminished guinea pig ileal contractile activity in the earlier studies i25. At present, it is not certain whether ASB has a role in synthetic or degradative pathways involving leukotrienes (or other mediator substances). Furthermore, its role in the in vivo degradation of proteoglycans and gly- cosaminoglycans is also unprovenSS.

d. Phospholipase D

Eosinophilic phospholipase D (EPD) has purportedly been purified by sequential anion exchange, cation exchange, and gel permeation chromatography and has been shown to have a molecular weight (MW) of 60,000 daltons, an isoelectric point of 5.8-6.2, and a pH optimum of 4.5-6.0 for choline liberation 7~. There is some doubt about the validity of these observations since this 'purified' enzyme had an activity of 24-560 nmot choline liberated/h/106 eosinophils for a mixed leukocyte population, which is 65-1,600 times greater than that measured by WF.LLER et al. i32 using a more sensitive I"C-phosphatidyl choline assay. Since neither neutrophils nor lymphocytes contain an appreciable amount of phospholipase D activity 132, it is unlikely that additional EPD-like activity from other leukocyte types in the mixed leukocytes used by KAXER et al. 7~ can explain these significant differences in enzyme activity. Until these disparate results are rectified, any conclusions about the physicochemical properties of EPD or the propensity of this enzyme to inactivate platelet activating factor are equivocal. Furthermore, there is no definite evidence that this enzyme in vivo catalyzes hydrolysis, rather than transfer, o f choline.

e. L ysophospholipase (Charcot-Leyden protein)

Eosinophilic lysophospholipase (ELP) supposedly catalyzes the cleavage of a fatty acid moiety from lysophospholipids, although in vivo catalysis of the reverse (i.e. transfer) reaction has not been excluded. The eosinophil has eight times more enzymic activity than neutrophilic leukocytes but has only three times more than mononuclear cells 132. Regardless of how ubiquitous this enzyme is, ELP has been demonstrated to be the major constituent of the Charcot-Leyden crystals 130. Such crystals were first described in the nineteenth century ~9"82 and have been found in tissue in- filtrates, feces, sputum, but not blood. In all cases, there is a direct relationship be-

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tween eosinophilia and the presence of Charcot-Leyden crystals. At present, no specific in vivo function has been attributed to ELP, and no definite evidence exists that ELP can injure endothelial cells or trigger intravascular coagulation: pathogen- ic mechanisms proposed to cause the thrombotic cardiovascular lesions observed in some patients with the hypereosinophilic syndrome ~°.

The purifmd enzyme has a MW of circa 17,000 daltons, has no divalent cation requirement, and is membrane bound ~'13°,m. Since ELP is a glycoprotein i, it is likely to be an intrinsic membrane protein, although this localization has not been demonstrated. Furthermore, the mechanisms by which ELP is shed from membranes and Charcot-Leyden protein crystals are formed are currently unknown. However, the differences in physicochemical properties of ELP following lyophilization lend credence to the suggestion that subtle changes in carbohydrate and/or protein conformation may be important for controlling packing in Charcot-Leyden crystalsL Whether one (or more) carbohydrate degradative enzyme(s) might function in con- cert with ELP in order to modulate its in vivo enzymic activity is still a matter of speculation.

f. Phospholipid exchange protein

This protein is capable of transferring intact phospholipid molecules from one biological membrane to another '3v. The human eosinophil protein has a MW of 80-90,000 daltons and a pH maximum of 5.5'32. The eosinophil possesses considera- bly more phospholipid exchange activity than either neutrophils or mononuclear cells m, and, although no in vivo functional role for this protein has been determined, its eosinophilic preponderance makes this highly likely.

g. Major basic protein

Human eosinophilic major basic protein (MBP) is a major constituent of the core of the eosinophil granule 4s'8' and is characterized as a non-histone protein with MW of 9,250 daltons (11,000 daltons for guinea pig MBP), an isoelectric point of 10, increased arginine content, and six half cystine residues including two free sulfhydryl groups 44"~. Since all reported biological studies with MBP were done with the reduced and alkylated pro te in 17"4°'43'~27, it is likely that the conformation and the in

vitro biological function of the chemically modified protein bear little resemblance to the native molecule's in vivo function. Since the cytotoxic effects of reduced and alkylated MBP on newborn larvae of Trichinella spiralis can be mimicked by polyarginine i27, it is possible that the chemically modified MBP with its multiple arginine residues may simulate polyarginine. Since polylysine (and by analogy polyarginine) is known to interact with biomembranes in a non-specific fashion 'Is'n6, it is likely that reduced and alkylated MBP's cytotoxic effects on guinea pig tracheal epithelium 4°,43, parasites ~v,~27, murine ascites tumor cells, guinea pig spleen cells 43, guinea pig jejunal epithelial cells% human epidermal cells 43, porcine endothelial cells 43, and human mononuclear cells 43 are unrelated to the true in vivo biological function of MBP and are artefactual. Furthermore, it remains to be determined whether the 'true' biological function of native MBP in vivo is enzymic, rather than membrane chaotropic.

h. Cationic proteins

Human eosinophils also contain other arginine-rich cationic proteins with MW's higher than MBP TM. The same caveats given for MBP apply to this group of proteins.

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2 . C E L L U L A R P R O P E R T I E S OF E O S I N O P H I L S

a. Production and distribution of eosinophils

1. Eosinopoiesis - Fetal and neonatal eosinopoiesis occurs in bone marrow and in extramedullary sites (liver, spleen, thymus and lymph nodes) ~9,I3s, but by adulthood, most eosinophils are bone marrow-derived ~°9. Although a common progenitor cell may give rise to both neutrophils and eosinophils, three experimental observations make this unlikely. First, certain forms of agranulocytosis and neutropenia are associated with increased numbers of circulating eosinophils ~s:l. Secondly, the eosinophil peroxidase differs structurally and functionally from the neutrophil peroxidase. Such differences include ultraviolet absorption, antigenicity, substrate specificity, and enzymic inhibition 3's'n'm. Furthermore, normal functional levels of eosinophil peroxidase have been observed in association with a severe congenital deficiency of neutrophil myeloperoxidase 8°'m, as has the opposite distribution 10s.

Eosinopoietins, chemical substances which stimulate eosinopoiesis, are defined by their functional activity in animal models. McGARRY and MILLER s9 initially posit- ed the existence of eosinopoietins. Later, using a specific rabbit anti-mouse eosinophil serum to induce eosinopenia, MAHMOUD et al. s7 were able to generate suffmient quantities o f murine eosinopoietin to propose that it was an heat-labile peptide (MW 200-1,400), whose cell of origin and mechanism of action are still unknown 84,s6. Without amino acid analysis and N-terminal amino acid determination, no definite conclusion about the chemical nature or purity of murine eosinopoietin can be made. Furthermore, non-specific binding or non-protease cleavage of eosinopoietin, whether pepdde or not, by contaminants in impure commercial pronase might account for an apparent pronase susceptibility. These and other caveats apply for lymphoid-derived 21-23.56.94 and mast cell-derived 12.48.74,76 'eosinophil specific' polypeptides and preclude structural comparisons among these factors.

Inhibitors o f eosinopoiesis, operating independently of the pituitary-adrenal axis 7, may contribute to the eosinopenia observed in certain inflammatory states s. An increase in the amount of such an inhibitor or a decrease in its degradation may account in part for the reduced proliferative activity of eosinophilic precursor cells observed in eosinophilic leukemic bone marrows m. The isolation of these functional inhibitors and the determination of their structure are required to define their mechanism of action and their relationship, if any, to eosinopoietin(s). At present, this has not been achieved.

Subpopulations of eosinophils exist within human bone marrow 69. These eosinophil precursors differ in their rate of sedimentation, as measured by velocity sedimentation, and when grown in semisolid cukures, result in colonies with different cellular morphology. In addition, sedimentation velocity fractionation of human peripheral eosinophils with discontinuous metrizamide gradients "9 shows ceil buoyancy heterogeneity among peripheral blood eosinophil populations (unpub- fished observations). However, functional differences among these subpopulations remain to be demonstrated.

The bone marrow kinetics of eosinophific granulocytes have been incompletely assessed, and no estimate of the turnover rate of normal eosinophils in the bone marrow has been published.

The eosinophil bone marrow reserve is estimated to be 0.3 x 109/kg body weight by assuming that the eosinophil to neutrophil ratio in the bone mimics that in the

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peripheral blood and that the bone marrow neutrophil reserve is 5.6-8.8 x 109/kg body weight 27,3°'n'33'7s.

2. Release f rom bone marrow of sequestered eosinophils - The biochemical factors and mechanisms controlling the release of eosinophils from bone marrow are complete- ly unknown, although B~soN and BASSI1 have suggested that eosinophil stimulation promotor (ESP), a lymphokine, or other agonists stimulating migration might be important. Speculating further, such a factor might also have the potential to diminish eosinophil adherence and to increase membrane fluidity of bone marrow-sequestered eosinophilic precursors m

3. Distribution of eosinophils between tissue and blood. Peripheral blood eosinophils from normal patients have a half-life of 8 h ~01. The clearance of SaCr-labelled eosinophils from hypereosinophilic subjects is biphasic: rapid disappearance (3 h), reappearance (0.6 h), and slow redistribution and clearance (half-life: 44 h). The tissue and blood distributions during the clearance and reappearance phases are unknown. However, the majority of normal eosinophils usually resides in the bone marrow and tissues, with less than 5% of the total body eosinophilic pool present in the circulation 63"n6.

In normal adult humans, the average number of eosinophils in peripheral blood is between 122/mm362 and 240/mm33~. There is an age and sex variation among the pediatric age group with means of 259/mm3 for males and 218/mm3 for females 26. In addition, atopy causes these averages to increase significantly (1,000/mm3 versus 202/mm3)36.

The peripheral btoocl eosinophii count varies inversely with the endogenous cor- ticosteroid level 2"24'99:°7. Hence, for patients with a complete hypothalamic-pituitary- adrenal axis, there is a diurnal variation with a midday nadir 6,~°'. The mechanism of ~-adrenergic-induced eosinopenia is unclear, but either ~1- or ~2-adrenoreceptor activation can induce pronounced eosinopenia ns. Administration of exogenous ACTH or cortisol also leads to an eosinopenia 35:,s~.Hg. The most likely explanation of this effect is that corticosteroids induce the migration of eosinophils into tissue no.

There is also evidence that T lymphocytes have an influence on the tissue accu- mulation of eosinophils in Trichinella spiralis infections 9,10,m, i24, intraperitoneally in sites of secondary tetanus toxoid injection in mice ~°:°2-~°4,n4"m, and in egg granulo- mas observed in murine experimental schistosomiasis 3'. Recently, JOHNSON et al. 7° used depletion experiments to determine that the subpopulation of T lymphocytes that efficiendy induce these eosinophilias have the Lyl, not Ly23, phenotype (i.e. helper, not cytotoxic/suppressor, T lymphocytes) 68,9~.

4. Eosinophil elimination - The mechanisms by which eosinophils are removed from tissue are unclear. However, eosinophils are eliminated in respiratory tract and gastrointestinal tract secretions ~7, phagocytized by macrophages 98, and degrad- ed following degranulation 57.

b. Eosinophilic chemotaxis

The mechanisms modulating in vivo eosinophit chemotaxis are incompletely un- derstood. However, a multitude of factors invoke in vitro eosinophil chemotaxis. Activation of the complement pathways (classical or alternative) or the plasmin- dependent fibrinotytic cascade results in the formation of CSa, C567, and fibrino- peptides with chemotactic activity for eosinophils and other leukocytes37:5:t Eosino- phil selective chemotactic factors are produced by lymphocytes 21'22 and mast cells.

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j . A. S M I T H

The mast celt-derived factors include lipids (HETE 52,s4, HHT s°, and lipid chemotactic factor i20), histamine 20, and peptides ~2,48,51.74.76,~2~. Although the amino acid-derived factors are synthesized and stored intracellularly, the lipid factors are formed de novo by the cyclo-oxygenase and lipoxygenase pathways of arachidonic acid metabolism.

The peptide factors, with one possible exception 48, have not been purified and sequenced. The exception is a tetrapeptide, H-Val(or Ala)-Gly-Ser-Glu-OH, which ac- counts for approximately 50% of the eosinophilotactic activity of the human lung- derived eosinophit chemotactic factor of anaphylaxis (ECF-A) 85. In addition, 'ECF-A tetrapeptides' increase the number of eosinophil C3b receptors and enhance eosinophil.mediated killing of complement-coated schistosomula 73.

Specific eosinophil receptors for chemotactic factors have not been demonstrated. Furthermore, the mechanism(s) by which these diverse chemical factors induce selective eosinophil chemotaxis in vitro is (are) unknown.

c. Interactions between eosinophils and mast cells in immediate hypersensitivity reactions

This topic has been discussed extensively by AUSTEN et al. 49'5~'85"m'128. Their cen- tral tenet is that the eosinophil's raison d't tre is the attenuation of the adverse biological effects caused by mast cell-derived factors, including histamine, slow reacting substance of anaphylaxis, and platelet activating factor. However, recently published data regarding the molecular properties of eosinophilic histaminase, arylsulfatase B, and phospholipase D, enzymes purportedly responsible for mast celt mediator substance degradation, are seemingly incompatible with this hypothesis (see sections 1.a., 1.c. and 1.d.).

d. Eosinophils and helminthic parasites

There is in vitro evidence indicating that eosinophils effect antibody- and /or complement-dependent damage to the larval-tissue stages of helminthic parasites (Schistosoma mansoni 15"16"42'67'73"s3"I°*'I19 and Trichinella spiralis77). However, there are no rigorous experimental models to assess whether or not the eosinophil has a parasiticidal role in vivo ~4,95, although mice treated chronically with anti-eosinophil serum appear to be more susceptible to infestation by Schistosoma mansoni g8 and Tri- chinella spiralis ss. It is important to emphasize that no relationship between in vivo

immunity to helminthic infection and eosinophilic parasiticidal effects in vitro is prov- en. Furthermore, in vivo there may be a role for neutrophils 2s and macrophages Is, as well as eosinophils.

Eosino.phils apparendy bind to parasites (e.g. Schistosoma mansoni eggs and schistosomula, as well as Trichinella spiralis newborn larvae). Since eosinophils bear receptors for the Fc portion of IgG, it is postulated that they bind to antibody-coated schistosomula by these receptors. However, it is unknown if antibody bound to a parasite functions as an intercellular bridge between the 'cytotoxic' eosinophils and a parasite or if humoral mechanisms are potentiated by 'non-cytotoxic' eosinophils 95.

Although the mechanisms of eosinophll-mediated cytotoxicity are unknown, there is evidence that oxidation, involving superoxides and hydrogen peroxide, and/or halogenation inflict damage to parasites '4. Although eosinophilic major basic protein (MBP) offers an alternative cytotoxic mechanism in vitro 17'127, these conclusions are based on studies using reduced and alkylated MBP (i.e. a molecule with a 'non.native' conformation) and are likely to resuk from polycationic-induced biological membrane perturbations 4~, unrelated to MBP's actual biological function

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MOLECULAR AND CELLULAR PROPERTIES OF EOS1NOPHILS

in vivo (see s e c t i o n 1.g.). In s u m m a r y , t h e e f f e c t o r m e c h a n i s m s , i f a n y , u s e d b y t h e

e o s i n o p h i l to i n d u c e p a r a s i t i c c y t o t o x i c i t y a r e u n f a t h o m e d .

SUMMARY

This review summarizes the eosinophil's affector and effector mechanisms, emphasizes their biochemical aspects, and details their function in certain immunologic and parasitic conditions.

ACKNOWLEDGEMENTS

The author gratefully acknowledges the support and encouragement of" Drs. Ramzi S. Cotran and K. Frank Austen.

The author was supported in part as a Milton Research Fellow by a grant to RSC from the william T. Milton Fund of Harvard University.

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MOLECULAR AND CELLULAR PROPERTIES OF EOSINOPHIL~

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51. GOETZL E.J., TASHyAN A. H. Jr., RUmN R. R., AUSTEN K. F.: Production of a low molecular weight eosinophil polyrnorphonuctear leukocyte chemotactic factor by anaplastic squamous cell ca rdnoma of human lung-J , cIin. Invest. 61, 770, 1978.

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67. JAMES S. L., COLLEY D. G.: Eosinophil-mediated destruction of Schistosoma mansoni eggs in vitro. II. The role of cytophilic antibody - Cell. Immunol. 38, 35, 1978.

68. JANEWAV C. A. Jr., JAson j . M.: How T lymphocytes recognize andgens - CRC crit. Rev. Immunol. 1, 133, 1980.

69. JoHnsoN G. R., D~SCH C., METCALF D.: Heterogeneity in human neutrophil, macrophage and eosinophil progenitor cells demonstrated by velocity sedimentation separation- Blood 50, 823, 1977.

70. JOHNSON G. R., NICHOLAS W. L., METCAt.F D., MCKENzm I. F. C., MITCHELL G. F.: Peritoneal cell population of mice infected with Mesocestoide5 corti as a source o f eosinophils - Int. Arch. Allergy 59, 315, 1979.

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74. KAY A. B., AUSTEN K. F.: The IgE-mediated release of an eosinophil leukocyte chemotactic factor from human tung-J. ImmunoI. 107, 899, I971.

75. KAy A. B., PEPPER D. S., MCKENZIE R.: The identification of fibrinopepfide B as a chemotactic agent derived from human fibrinogen - Brit. J. Haemat. 27, 669, 1974.

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78. KrLLMANN S. A., CRONKITE E. P., FLIEDNER T. M., BOND V. P.: Mitotic indices of human bone marrow cells. I13. Duration of some phases of erythrocytic and granulocytic proliferation computed from mitotic indices - Blood 24, 267, 1964.

79. LACHMANN P-J-, KAy A. B., THOMPSON R. A.: The chemotactic activity for neutrophil and eosinophil leukocytes of the__ trimolecular complex of the fifth, sixth, and seventh components of human complement (C567) prepared in free solution by the 'reactive lysis' procedure- Immunology 19, 895, 1970.

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193

molecular and cellular properties of eosinophils

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