Adhesion of leukocytes to the aortic endothelium of conventional, specific pathogen free (SPF) and hypercholesterolemic SPF rats

  • María Gabaldón
    Correspondence to: Dr. Maria Gabaldón, Unidad de histoquímica, Centro de Investigation, Hospital “La Fe”, Avenida Campanar 21, E-46009 Valencia, Spain.
    Unidad de Histoquimia, Centro de Investigacíon, Hospital “La Fe”, 46009 Valencia, Spain
    Search for articles by this author
  • Carmen Capdevila
    Unidad de Histoquimia, Centro de Investigacíon, Hospital “La Fe”, 46009 Valencia, Spain
    Search for articles by this author
      This paper is only available as a PDF. To read, Please Download here.


      Adhesion of leukocytes to the aortic endothelium was studied in specific pathogen-free (SPF) and conventional rats and in SPF rats with diet-induced hypercholesterolemia. Nonspecific esterase activity with α-naphthyl acetate as substrate was used to characterize the adhered cells. Phagocytic activity was determined by injecting i.v. 0.1–0.4 ml/100 g doses of Monastral blue B® (MbB). Adhesion in SPF rats was 8 ± 4 esterase (+) cells/mm2. Adhesion in conventional rats was of the same order except in 2 cases with antibodies to Mycoplasma pulmonis and Kilham rat virus, where adhesion was 44 and 68 esterase ( + ) cells/mm2, respectively. For all MbB doses studied, phagocytic activity arose in a percentage of the adherent cells, ranging from 5 to 85%. Rats fed the hyperlipidic diet for 15 days developed severe hypercholesterolemia and adhesion was drastically increased to 200–700 esterase (+) cells/mm2. Results indicate that: (1) spontaneous pathology in rats may produce an increased adhesion of leukocytes to the endothelium, and (2) phagocytic activity is only expressed in a fraction of the esterase (+) cells adhered to the endothelium.


      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'


      Subscribe to Atherosclerosis
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect


        • Shankar R.
        • Tuyethong N.
        • Sallis J.D.
        Atherogenesis. Mitigation of monocyte adhesion to arterial endothelium in hyperlipidemic rats by phosphocitrate, a phosphorylated polycarboxylic acid.
        Atherosclerosis. 1986; 62: 47
        • Schwartz C.J.
        • Sprague E.A.
        • Kelley J.L.
        • Valente A.J.
        • Suenram C.A.
        Aortic intimal monocyte recruitment in the normo and hypercholesterolemic baboon (Papio cynocephalus). An ultrastructural study: Implications in atherogenesis.
        Virchows Arch. Pathol. Anat. 1985; 405: 175
        • Faggiotto A.
        • Ross R.
        • Harker L.
        Studies of hypercholesterolemia in the nonhuman primate. I. Changes that lead to fatty streak formation.
        Arteriosclerosis. 1984; 4: 323
        • Jerome W.G.
        • Lewis J.C.
        Early atherogenesis in white carneau pigeons. I. Leukocyte margination and endothelial alterations at the celiac bifurcation.
        Am. J. Pathol. 1984; 116: 56
        • Gerrity R.G.
        • Naito H.K.
        • Richardson M.
        • Schwartz C.J.
        Dietary induced atherogenesis in swine. Morphology of the intima in prelesion stages.
        Am. J. Pathol. 1979; 95: 775
        • De Bono D.
        Endothelial-lymphocyte interactions in vitro. I. Adherence of nonallergised lymphocytes.
        Cell. Immunol. 1976; 26: 78
        • Zweiman B.
        • Moskovitz A.R.
        • Lisak R.P.
        Quantitative assessment of the adherence of normal human blood mononuclear cells to vascular endothelial cell monolayers.
        Cell. Immunol. 1982; 68: 165
        • Hansson G.K.
        • Björnheden T.
        • Bylock A.
        • Bondjers G.
        Fc-dependent binding of monocytes to areas with endothelial injury in the rabbit aorta.
        Exp. Mol. Pathol. 1981; 34: 264
        • Joris I.
        • Stetz E.
        • Majno G.
        Lymphocytes and monocytes in the aortic intima. An electron microscopic study in the rat.
        Atherosclerosis. 1979; 34: 21
        • Freudenberg N.
        • Riese K.H.
        Characterization of cells of the normal aortic endothelium of adult rats and changes due to endotoxin shock. I. Communication: light microscopy, autoradiography, DNA cytophotometry and enzyme histochemistry.
        Beitr. Pathol. Bd. 1976; 159: 125
        • Joris I.
        • Zand T.
        • Nunnari J.J.
        • Krolikowski F.J.
        • Majno G.
        Studies on the pathogenesis of atherosclerosis. I. Adhesion and emigration of mononuclear cells in the aorta of hypercholesterolemic rats.
        Am. J. Pathol. 1983; 113: 341
        • Reidy M.A.
        • Schwartz S.M.
        Endothelial injury and regeneration IV. Endotoxin: a nondenuding injury to aortic endothelium.
        Lab. Invest. 1983; 48: 25
        • Huttner I.
        • Boutet M.
        • More R.H.
        Studies on protein passage through arterial endothelium II. Regional differences in permeability to fine structural protein tracers in arterial endothelium of normotensive rat.
        Lab. Invest. 1973; 28: 678
        • Katora M.E.
        • Hollis T.M.
        Regional variation in rat aortic endothelial surface morphology: relationship to regional aortic permeability.
        Exp. Mol. Pathol. 1976; 24: 23
        • Gabaldń M.
        Methodological approaches for the study of the aortic endothelium of the rat.
        Atherosclerosis. 1987; 65: 139
        • Cassell G.H.
        • Lindsey J.R.
        • Baker H.J.
        • Davis J.K.
        Mycoplasmal and rickettsial diseases.
        in: 7th edn. The Laboratory Rat. Vol 1. Academic Press, New York1979: 243
        • Lindsey J.R.
        • Davidson M.K.
        • Schoeb T.R.
        • Cassell G.H.
        Mycoplasma pulmonis — host relationships in a breeding colony of Sprague-Dawley rats with enzootic murine respiratory mycoplasmosis.
        Lab. Anim. Sci. 1985; 35: 597
        • Malmström P.
        • Jn̈sson A.
        • Sjögren H.O.
        ANAE staining pattern of rat lymphocytes. Lack of correlation with lymphocyte subclasses.
        Scand. J. Immunol. 1981; 14: 523
        • Netland P.A.
        • Zetter B.R.
        • Via D.P.
        • Voyta J.C.
        In situ labelling of vascular endothelium with fluorescent acetylated low density lipoprotein.
        Histochem. J. 1985; 17: 1309
        • Joris I.
        • DeGirolami V.
        • Wortham K.
        • Majno G.
        Vascular labelling with Monastral Blue B®.
        Stain Technol. 1982; 57: 177
        • Thomas W.A.
        • Jones R.
        • Scott R.F.
        • Morrison E.
        • Goodale F.
        • Imai H.
        Production of early atherosclerotic lesions in rats characterized by proliferation of “modified smooth muscle cells”.
        Exp. Mol. Pathol. 1963; 2: 40
        • Suzuki M.
        • O'Neal R.M.
        Accumulation of lipids in the leukocytes of rats fed atherogenic diets.
        J. Lipid Res. 1964; 5: 624
        • Yam L.T.
        • Li C.Y.
        • Crosby W.H.
        Cytochemical identification of monocytes and granulocytes.
        Am. J. Clin. Pathol. 1971; 55: 283
        • Koski I.R.
        • Poplack D.G.
        • Blaese R.M.
        A nonspecific esterase stain for the identification of monocytes and macrophages.
        in: Bloom B.R. David J.R. In vitro Methods in Cell-Mediated and Tumor Immunity. Academic Press, New York1976: 359
        • Monahan-Earley R.A.
        • Isomura T.
        • García R.I.
        • Galli S.J.
        • Dvorak H.F.
        • Dvorak A.M.
        Nonspecific esterase activity expressed in Weibel-Palade bodies of cloned guinea pig aortic endothelial cells.
        J. Histochem. Cytochem. 1987; 35: 531
      1. Diem K. Lentner C. Scientific Tables. 7th edn. Ciba-Geigy, Basel1970
        • Freudenberg N.
        • Häublein U.
        The effect of endotoxin shock on the aortic endothelium of young rats.
        Beitr. Pathol. Bd. 1975; 156: 1
        • Jacoby R.O.
        • Bhatt P.N.
        • Jonas A.M.
        Viral diseases.
        in: The Laboratory Rat. Vol. 1. Academic Press, New York1979: 272
        • Robinson G.W.
        • Nathanson N.
        • Hodous J.
        Seroepidemiological study of rat virus infection in a closed laboratory colony.
        Am. J. Epidemiol. 1971; 94: 91
        • Margolis G.
        • Kilham L.
        Parvovirus infections, vascular endothelium and hemorrhagic encephalopathy.
        Lab. Invest. 1970; 22: 478
        • Baringer J.R.
        • Nathanson N.
        Parvovirus hemorrhagic encephalopathy of rats. Electron microscopic observations of the vascular lesions.
        Lab. Invest. 1972; 27: 514
        • Robey R.E.
        • Woodman D.R.
        • Hetrick F.M.
        Studies on the natural infection of rats with the Kilham rat virus.
        Am. J. Epidemiol. 1968; 88: 139
        • Ranki A.
        • Hayry P.
        Histochemical identification of esterases responsible for the ANAE-activity in rodent T and B lymphocytes.
        Thymus. 1980; 1: 329
        • Cuenoud H.F.
        • Joris I.
        • Langer R.S.
        • Majno G.
        Focal arteriolar insudation. A response of arterioles to chronic nonspecific irritation.
        Am. J. Pathol. 1987; 127: 592
        • Clowes A.W.
        • Ryan G.B.
        • Breslow J.L.
        • Karovsky M.J.
        Absence of enhanced intimal thickening in the response of the carotid arterial wall to endothelial injury in hypercholesterolemic rats.
        Lab. Invest. 1976; 35: 6