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Disease-associated glycosylated molecular variants of human C-reactive protein activate complement-mediated hemolysis of erythrocytes in tuberculosis and Indian visceral leishmaniasis

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Abstract

Human C-reactive protein (CRP), as a mediator of innate immunity, removed damaged cells by activating the classical complement pathway. Previous studies have successfully demonstrated that CRPs are differentially induced as glycosylated molecular variants in certain pathological conditions. Affinity-purified CRPs from two most prevalent diseases in India viz. tuberculosis (TB) and visceral leishmaniasis (VL) have differential glycosylation in their sugar composition and linkages. As anemia is a common manifestation in TB and VL, we assessed the contributory role of glycosylated CRPs to influence hemolysis via CRP-complement-pathway as compared to healthy control subjects. Accordingly, the specific binding of glycosylated CRPs with erythrocytes was established by flow-cytometry and ELISA. Significantly, deglycosylated CRPs showed a 7–8-fold reduced binding with erythrocytes confirming the role of glycosylated moieties. Scatchard analysis revealed striking differences in the apparent binding constants (104–105 M−1) and number of binding sites (106–107sites/erythrocyte) for CRP on patients’ erythrocytes as compared to normal. Western blotting along with immunoprecipitation analysis revealed the presence of distinct molecular determinants on TB and VL erythrocytes specific to disease-associated CRP. Increased fragility, hydrophobicity and decreased rigidity of diseased-erythrocytes upon binding with glycosylated CRP suggested membrane damage. Finally, the erythrocyte-CRP binding was shown to activate the CRP-complement-cascade causing hemolysis, even at physiological concentration of CRP (10 μg/ml). Thus, it may be postulated that CRP have a protective role towards the clearance of damaged-erythrocytes in these two diseases.

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Abbreviations

αGalNAc:

alpha-N-acetyl Galactosamine

αGlcNAc:

alpha-N-acetyl Glucosamine

α-L-Fuc:

alpha-L-fucose

ABTS:

2, 2′-azino-bis (3-ethylbenzthiazole-6-sulfonic acid)

ANS:

8-anilino-1-napthalenesulfonic acid

BSA:

Bovine Serum Albumin

CaCl2 :

Calcium Chloride

CHAPS:

3-(3-cholamidopropyl) dimethylammonio)-1-propanesulfonic acid

Con A:

Concanavalin A

CRP:

C-reactive protein

CRPTB and CRPVL :

Purified CRP from patients with TB and VL

CRPSigma :

CRP purified from human plasma purchased from Sigma Chemical Company

DAB:

3, 3-diaminobenzidine

DBA:

Dolichos biflorus agglutinin

DIG:

Dioxigenin

DPH:

1,6-diphenyl-1, 3, 5-hexatriene

DSA:

Datura stramonium agglutinin

E:

Erythrocytes

ETB, EVL and EN :

Erythrocytes from TB, VL and normal (N) individuals

EDTA:

Ethylene diamine tetra acetic acid

ELISA:

Enzyme-linked immunosorbent assay

FACS:

Fluorescence activated cell sorter

FITC:

Fluorescein isothiocynate

GLC:

Gas liquid chromatography

GNA:

Galanthus nivalis agglutinin

GVB:

Gelatin-veronal-buffered

HRP:

Horseradish peroxidase

I:

Iodine

IEF:

Isoelectric focussing

IgG:

Immunoglobulin G

kDa:

kilo Dalton

MAA:

Maackia amurensis agglutinin

MAC:

Membrane attack complex

NaCl:

Sodium Chloride

NHS:

Normal human serum

PAGE:

Polyacrylamide gel electrophoresis

PC:

Phosphocholine

PNA:

Peanut agglutinin

SPR:

Surface plasmon resonance

SD:

Standard Deviation

SDS:

Sodium Dodecyl sulphate

SNA:

Sambucus nigra agglutinin

TB:

Tuberculosis

TCA:

Trichloro acetic acid

UEA:

Ulex europaeus agglutinin

VL:

Visceral leishmaniasis

WGA:

Wheat germ agglutinin

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Acknowledgement

This work was supported by the Council of Scientific and Industrial Research (CSIR), I.I.C.B, Department of Science and Technology and the Indian Council of Medical Research, Govt. of India. W.A and S.M receive their Senior Research fellowships from CSIR; S.B from University Grants Commission. We are thankful to Sajal Samanta and Biswajit Khatua; Suchandra Chowdhury, Kaushik Bhattacharya for FACS; Asish Mallick for their help; Samir Roy for SPR and Sandip Chakrabarty for MALDI-TOF analysis.

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  1. Sumi Mukhopadhyay

    Present address: School of Tropical Medicine, Kolkata, India

Authors and Affiliations

  1. Infectious disease and Immunology Division, Indian Institute of Chemical Biology, 4, Raja S.C Mullick Road, Jadavpur, Kolkata, 700 032, India

    Waliza Ansar, Sumi Mukhopadhyay, SK. Hasan Habib, Shyamasree Basu & Chitra Mandal

  2. Structural Biology and Bioinformatics Division, Indian Institute of Chemical Biology, 4, Raja S.C Mullick Road, Jadavpur, Kolkata, 700 032, India

    CN. Mandal

  3. Department of Organic Chemistry, Indian Institute of Chemical Biology, 4, Raja S.C Mullick Road, Jadavpur, Kolkata, 700 032, India

    Asish Kumar Sen

  4. Department of Tropical Medicine, School of Tropical Medicine, Chittaranjan Avenue, Kolkata, 700073, India

    Bibhuti Saha

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Ansar, W., Mukhopadhyay, S., Habib, S.H. et al. Disease-associated glycosylated molecular variants of human C-reactive protein activate complement-mediated hemolysis of erythrocytes in tuberculosis and Indian visceral leishmaniasis. Glycoconj J 26, 1151–1169 (2009). https://doi.org/10.1007/s10719-009-9236-y

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