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Cited by 88Malaria Research and ControlHemoglobinopathies and Related DisordersBlood groups and transfusion

Plasmodium vivax Adherence to Placental Glycosaminoglycans

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Chotivanich, Kesinee, Udomsangpetch, Rachanee, Suwanarusk, Rossarin, Pukrittayakamee, Sasithon, Wilairatana, Polrat, Beeson, James G., Day, Nicholas P. J., White, Nicholas J.·2012·PLoS ONE
DOI 10.1371/journal.pone.0034509PMC PMC3328474
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Abstract

BACKGROUND: Plasmodium vivax infections seldom kill directly but do cause indirect mortality by reducing birth weight and causing abortion. Cytoadherence and sequestration in the microvasculature are central to the pathogenesis of severe Plasmodium falciparum malaria, but the contribution of cytoadherence to pathology in other human malarias is less clear. METHODOLOGY: The adherence properties of P. vivax infected red blood cells (PvIRBC) were evaluated under static and flow conditions. PRINCIPAL FINDINGS: P. vivax isolates from 33 patients were studied. None adhered to immobilized CD36, ICAM-1, or thrombospondin, putative ligands for P. falciparum vascular cytoadherence, or umbilical vein endothelial cells, but all adhered to immobilized chondroitin sulphate A (CSA) and hyaluronic acid (HA), the receptors for adhesion of P. falciparum in the placenta. PvIRBC also adhered to fresh placental cells (N = 5). Pre-incubation with chondroitinase prevented PvIRBC adherence to CSA, and reduced binding to HA, whereas preincubation with hyaluronidase prevented adherence to HA, but did not reduce binding to CSA significantly. Pre-incubation of PvIRBC with soluble CSA and HA reduced binding to the immobilized receptors and prevented placental binding. PvIRBC adhesion was prevented by pre-incubation with trypsin, inhibited by heparin, and reduced by EGTA. Under laminar flow conditions the mean (SD) shear stress reducing maximum attachment by 50% was 0.06 (0.02) Pa but, having adhered, the PvIRBC could then resist detachment by stresses up to 5 Pa. At 37 °C adherence began approximately 16 hours after red cell invasion with maximal adherence at 30 hours. At 39 °C adherence began earlier and peaked at 24 hours. SIGNIFICANCE: Adherence of P. vivax-infected erythrocytes to glycosaminoglycans may contribute to the pathogenesis of vivax malaria and lead to intrauterine growth retardation.

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  • Sequestration of P. vivax in the placenta has been described, with the involvement of ICAM-1 and CSA as receptors.

    “The sequestration of P. vivax in the placenta, though until recently thought not to occur, has been described,77–78 with the involvement of ICAM-1 and CSA as receptors.”

    From Malaria in pregnancy. (2013) · cites this paper as [77]

    The Results (Binding to putative receptors) report that P. vivax-infected red blood cells adhered to CSA and fresh placental sections, but none adhered to ICAM-1. The Discussion also says the extent of placental sequestration in vivo is unknown. Thus this paper does not support ICAM-1 involvement and does not establish placental sequestration in vivo. (LLM, conf=0.90)

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  • Placental sequestration has been described for P. vivax infections.

    “Recently, placental sequestration has been described also for P.vivax infections.”

    From Malaria in pregnancy. (2013) · cites this paper as [77]

    The Discussion reports that P. vivax-infected red cells adhered to placental glycosaminoglycans and fresh placental cells. It also states that the extent of placental sequestration in vivo is not known, so the paper supports placental adherence as a possible mechanism, not established sequestration during infection. Page numbers are unavailable in our copy. (LLM, conf=0.88)

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References 35 · Cited by 88

Research works printed but not linked: 28

  1. [1]Beeson JG Duffy PE 2005 The immunology and pathogenesis of malaria during pregnancy. Curr Top Microbiol Immunol 297 187 227 16265906
  2. [2]Rogerson SJ Hviid L Duffy PE Leke RF Taylor DW 2007 Malaria in pregnancy: pathogenesis and immunity. Lancet Infect Dis 7 105 117 17251081
  3. [4]Buffet PA Gamain B Scheidig C Baruch D Smith JD 1999 Plasmodium falciparum domain mediating adhesion to chondroitin sulphate A: a receptor for human placental infection. Proc Natl Acad Sci U S A 96 12743 12748 10535993 PMC23079
  4. [6]Price RN Tjitra E Guerra CA Yeung S White NJ 2007 Vivax malaria: neglected and not benign. Am J Trop Med Hyg 77 79 87 18165478 PMC2653940
  5. [7]Mendis K Sina BJ Marchesini P Carter R 2001 The neglected burden of Plasmodium vivax malaria. Am J Trop Med Hyg 64 97 106 11425182
  6. [8]Udomsangpetch R Thanikkul K Pukrittayakamee S White NJ 1995 Rosette formation by Plasmodium vivax. Trans R Soc Trop Med Hyg 89 635 637 8594679
  7. [12]Snounou G 1996 Detection and identification of the four malaria parasite species infecting humans by PCR amplification. Methods Mol Biol 50 263 291 8751365
  8. [13]Chotivanich K Silamut K Udomsangpetch R Stepniewska KA Pukrittayakamee S 2001 Ex-vivo short-term culture and developmental assessment of Plasmodium vivax. Trans R Soc Trop Med Hyg 95 677 680 11816444
  9. [14]Andrysiak PM Collins WE Campbell GH 1986 Concentration of Plasmodium ovale- and Plasmodium vivax-infected erythrocytes from nonhuman primate blood using Percoll gradients. Am J Trop Med Hyg 35 251 254 3006527
  10. [15]Ribaut C 2008 Concentration and purification by magnetic separation of the erythrocytic stages of all human Plasmodium species. Malar J 7 45 18321384 PMC2292734
  11. [16]Chai W Beeson JG Lawson AM 2002 The structural motif in chondroitin sulphate for adhesion of Plasmodium falciparum-infected erythrocytes comprises disaccharide units of 4-O-sulphated and non-sulphated N-acetylgalactosamine linked to glucuronic acid. J Biol Chem 277 22438 22446 11956186
  12. [17]Beeson JG Rogerson SJ Brown GV 2002 Evaluating specific adhesion of Plasmodium falciparum-infected erythrocytes to immobilised hyaluronic acid with comparison to binding of mammalian cells. Int J Parasitol 32 1245 1252 12204224
  13. [18]Chotivanich KT Pukrittayakamee S Simpson JA White NJ Udomsangpetch R 1998 Characteristics of Plasmodium vivax-infected erythrocyte rosettes. Am J Trop Med Hyg 59 73 76 9684631
  14. [19]Udomsangpetch R Webster HK Pattanapanyasat K Pitchayangkul S Thaithong S 1992 Cytoadherence characteristics of rosette-forming Plasmodium falciparum. Infect Immun; 60 4483 90 1383150 PMC258192
  15. [20]Beeson JG Rogerson SJ Cooke BM Reeder JC Chai W 2000 Adhesion of Plasmodium falciparum-infected erythrocytes to hyaluronic acid in placental malaria. Nat Med 6 86 90 10613830 PMC2613479
  16. [21]Stamper HB Jr Woodruff JJ 1977 An in vitro model of lymphocyte homing. I. Characterization of the interaction between thoracic duct lymphocytes and specialized high-endothelial venules of lymph nodes. J Immunol 119 772 780 407305
  17. [22]Udomsangpetch R Reinhardt PH Schollaardt T Elliott JF Kubes P 1997 Promiscuity of clinical Plasmodium falciparum isolates for multiple adhesion molecules under flow conditions. J Immunol 158 4358 4364 9126999
  18. [23]Suwanarusk R Cooke BM Dondorp AM Silamut K Sattabongkot J 2004 The deformability of red blood cells parasitized by Plasmodium falciparum and P. vivax. J Infect Dis 189 190 194 14722882
  19. [24]Williams TN Maitland K Phelps L Bennett S Peto TE 1997 Plasmodium vivax: a cause of malnutrition in young children. QJM. 90 751 757 9536339
  20. [25]Fernando SD Gunawardena DM Bandara MR De Silva D Carter R 2003 The impact of repeated malaria attacks on the school performance of children. Am J Trop Med Hyg 69 582 588 14740872
  21. [26]Tjitra E Anstey NM Sugiarto P Warikar N Kenangalem E 2008 Multidrug-resistant Plasmodium vivax associated with severe and fatal malaria: a prospective study in Papua, Indonesia. PLoS Med 5 e128 18563962 PMC2429950
  22. [27]Anstey NM Handojo T Pain MC Kenangalem E Tjitra E 2007 Lung injury in vivax malaria: pathophysiological evidence for pulmonary vascular sequestration and posttreatment alveolar-capillary inflammation. J Infect Dis 195 589 596 17230420 PMC2532499
  23. [29]Beeson JG Rogerson SJ Cooke BM Reeder JC Chai W 2000 Adhesion of Plasmodium falciparum –infected erythrocytes to hyaluronic acid in placental malaria. Nat Med 6 86 90 10613830 PMC2613479
  24. [30]Beeson JG Brown GV 2004 Plasmodium falciparum-infected erythrocytes demonstrate dual specificity for adhesion to hyaluronic acid and chondroitin sulphate A and have distinct adhesive properties. J Infect Dis 189 169 179 14722880
  25. [31]Luxemburger C McGready R Kham A Morison L Cho T 2001 Effects of malaria during pregnancy on infant mortality in an area of low malaria transmission Am J Epidemiol 154 459 465 11532788
  26. [32]Gardner JP Pinches RA Roberts DJ Newbold CI 1996 Variant antigens and endothelial receptor adhesion in Plasmodium falciparum. Proc Natl Acad Sci USA 93 3503 3508 8622966 PMC39639
  27. [33]Udomsangpetch R Pipitaporn B Silamut K Pinches R Kyes S 2002 Febrile temperatures induce cytoadherence of ring-stage Plasmodium falciparum-infected erythrocytes. Proc Natl Acad Sci USA 99 11825 11829 12177447 PMC129353
  28. [36]Fried M Nosten F Brockman A Brabin BJ Duffy PE 1998 Maternal antibodies block malaria. Nature 395 851 852 9804416

Authors
Chotivanich, K., Udomsangpetch, R., Suwanarusk, R., Pukrittayakamee, S., Wilairatana, P., Beeson, J. G., Day, N. P. J., & White, N. J.
Affiliations
  • Mahidol University (TH)
  • Agency for Science, Technology and Research (SG)
  • Walter and Eliza Hall Institute of Medical Research (AU)
Corresponding author
White, Nicholas J.
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2012-04-17
Volume
7
Issue
4
Pages
e34509
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0034509
PMC
PMC3328474
OpenAlex
W1984552320
Cited by
88
References
35
Citations by year
2025: 1 · 2024: 1 · 2023: 1 · 2022: 4 · 2021: 13 · 2020: 5 · 2019: 4 · 2018: 4 · 2017: 7 · 2016: 6 · 2015: 6 · 2014: 11 · 2013: 16 · 2012: 9
FWCI
12.98
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Minerva Access (University of Melbourne) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Greater South Information System
Funders
  • Wellcome Trust (089275, 093956, 093956/Z/10/Z)
  • Mahidol University
  • Faculty of Tropical Medicine, Mahidol University
Topics
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Malaria Research and Control
  • Health Sciences › Medicine › Genetics › Hemoglobinopathies and Related Disorders
  • Health Sciences › Medicine › Hematology › Blood groups and transfusion
Keywords
Plasmodium vivax, cytoadherence, placental adhesions, glycosaminoglycans, chondroitin sulfate A, hyaluronic acid, infected erythrocytes, chondroitinase, hyaluronidase, shear stress, temperature dependence, fetal growth restriction, malaria pathogenesis, placenta
MeSH terms
Adult, Cell Adhesion, Chondroitin Sulfates, Egtazic Acid, Erythrocytes, Female, Glycosaminoglycans, Heparin, Humans, Hyaluronic Acid, Placenta, Plasmodium vivax, Pregnancy, Temperature, Trypsin, Malaria, Vivax

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