Complement Receptor 1 Is a Sialic Acid-Independent Erythrocyte Receptor of
Plasmodium falciparum is a highly lethal malaria parasite of humans. A major portion of its life cycle is dedicated to invading and multiplying inside erythrocytes. The molecular mechanisms of erythrocyte invasion are incompletely understood. P. falciparum depends heavily on sialic acid present on glycophorins to invade erythrocytes. However, a significant proportion of laboratory and field isolates are also able to invade erythrocytes in a sialic acid-independent manner. The identity of the erythrocyte sialic acid-independent receptor has been a mystery for decades. We report here that the complement receptor 1 (CR1) is a sialic acid-independent receptor for the invasion of erythrocytes by P. falciparum. We show that soluble CR1 (sCR1) as well as polyclonal and monoclonal antibodies against CR1 inhibit sialic acid-independent invasion in a variety of laboratory strains and wild isolates, and that merozoites interact directly with CR1 on the erythrocyte surface and with sCR1-coated microspheres. Also, the invasion of neuraminidase-treated erythrocytes correlates with the level of CR1 expression. Finally, both sialic acid-independent and dependent strains invade CR1 transgenic mouse erythrocytes preferentially over wild-type erythrocytes but invasion by the latter is more sensitive to neuraminidase. These results suggest that both sialic acid-dependent and independent strains interact with CR1 in the normal red cell during the invasion process. However, only sialic acid-independent strains can do so without the presence of glycophorin sialic acid. Our results close a longstanding and important gap in the understanding of the mechanism of erythrocyte invasion by P. falciparum that will eventually make possible the development of an effective blood stage vaccine.
Vyšlo v časopise:
Complement Receptor 1 Is a Sialic Acid-Independent Erythrocyte Receptor of. PLoS Pathog 6(6): e32767. doi:10.1371/journal.ppat.1000968
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1000968
Souhrn
Plasmodium falciparum is a highly lethal malaria parasite of humans. A major portion of its life cycle is dedicated to invading and multiplying inside erythrocytes. The molecular mechanisms of erythrocyte invasion are incompletely understood. P. falciparum depends heavily on sialic acid present on glycophorins to invade erythrocytes. However, a significant proportion of laboratory and field isolates are also able to invade erythrocytes in a sialic acid-independent manner. The identity of the erythrocyte sialic acid-independent receptor has been a mystery for decades. We report here that the complement receptor 1 (CR1) is a sialic acid-independent receptor for the invasion of erythrocytes by P. falciparum. We show that soluble CR1 (sCR1) as well as polyclonal and monoclonal antibodies against CR1 inhibit sialic acid-independent invasion in a variety of laboratory strains and wild isolates, and that merozoites interact directly with CR1 on the erythrocyte surface and with sCR1-coated microspheres. Also, the invasion of neuraminidase-treated erythrocytes correlates with the level of CR1 expression. Finally, both sialic acid-independent and dependent strains invade CR1 transgenic mouse erythrocytes preferentially over wild-type erythrocytes but invasion by the latter is more sensitive to neuraminidase. These results suggest that both sialic acid-dependent and independent strains interact with CR1 in the normal red cell during the invasion process. However, only sialic acid-independent strains can do so without the presence of glycophorin sialic acid. Our results close a longstanding and important gap in the understanding of the mechanism of erythrocyte invasion by P. falciparum that will eventually make possible the development of an effective blood stage vaccine.
Zdroje
1. MillerLH
HaynesJD
McAuliffeFM
ShiroishiT
DurocherJR
1977 Evidence for differences in erythrocyte surface receptors for the malarial parasites, Plasmodium falciparum and Plasmodium knowlesi. J Exp Med 146 277 281
2. DeasJE
LeeLT
1981 Competitive inhibition by soluble erythrocyte glycoproteins of penetration by Plasmodium falciparum. Am J Trop Med Hyg 30 1164 1167
3. PerkinsM
1981 Inhibitory effects of erythrocyte membrane proteins on the in vitro invasion of the human malarial parasite (Plasmodium falciparum) into its host cell. J Cell Biol 90 563 567
4. PasvolG
JungeryM
WeatherallDJ
ParsonsSF
AnsteeDJ
1982 Glycophorin as a possible receptor for Plasmodium falciparum. Lancet 2 947 950
5. MaierAG
DuraisinghMT
ReederJC
PatelSS
KazuraJW
2003 Plasmodium falciparum erythrocyte invasion through glycophorin C and selection for Gerbich negativity in human populations. Nat Med 9 87 92
6. HadleyTJ
KlotzFW
PasvolG
HaynesJD
McGinnissMH
1987 Falciparum malaria parasites invade erythrocytes that lack glycophorin A and B (MkMk). Strain differences indicate receptor heterogeneity and two pathways for invasion. J Clin Invest 80 1190 1193
7. HoltEH
NicholsME
EtzionZ
PerkinsME
1989 Erythrocyte invasion by two Plasmodium falciparum isolates differing in sialic acid dependency in the presence of glycophorin A antibodies. Am J Trop Med Hyg 40 245 251
8. DolanSA
MillerLH
WellemsTE
1990 Evidence for a switching mechanism in the invasion of erythrocytes by Plasmodium falciparum. J Clin Invest 86 618 624
9. DolanSA
ProctorJL
AllingDW
OkuboY
WellemsTE
1994 Glycophorin B as an EBA-175 independent Plasmodium falciparum receptor of human erythrocytes. Mol Biochem Parasitol 64 55 63
10. MitchellGH
HadleyTJ
McGinnissMH
KlotzFW
MillerLH
1986 Invasion of erythrocytes by Plasmodium falciparum malaria parasites: evidence for receptor heterogeneity and two receptors. Blood 67 1519 1521
11. BaumJ
PinderM
ConwayDJ
2003 Erythrocyte invasion phenotypes of Plasmodium falciparum in The Gambia. Infect Immun 71 1856 1863
12. DeansAM
NeryS
ConwayDJ
KaiO
MarshK
2007 Invasion Pathways and Malaria Severity in Kenyan Plasmodium falciparum Clinical Isolates. Infect Immun 75 3014 3020
13. SimRB
1985 Large-scale isolation of complement receptor type 1 (CR1) from human erythrocytes. Proteolytic fragmentation studies. Biochem J 232 883 889
14. Da SilvaRP
HallBF
JoinerKA
SacksDL
1989 CR1, the C3b receptor, mediates binding of infective Leishmania major metacyclic promastigotes to human macrophages. J Immunol 143 617 622
15. ZimmerliS
EdwardsS
ErnstJD
1996 Selective receptor blockade during phagocytosis does not alter the survival and growth of Mycobacterium tuberculosis in human macrophages. Am J Respir Cell Mol Biol 15 760 770
16. AhearnJM
FearonDT
1989 Structure and function of the complement receptors, CR1 (CD35) and CR2 (CD21). Adv Immunol 46 183 219
17. MeriS
JarvaH
1998 Complement regulation. Vox Sang 74 Suppl 2 291 302
18. RoweJA
MouldsJM
NewboldCI
MillerLH
1997 P. falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1. Nature 388 292 295
19. WeismanHF
BartowT
LeppoMK
MarshHCJr
CarsonGR
1990 Soluble human complement receptor type 1: in vivo inhibitor of complement suppressing post-ischemic myocardial inflammation and necrosis. Science 249 146 151
20. NickellsM
HauhartR
KrychM
SubramanianVB
Geoghegan-BarekK
1998 Mapping epitopes for 20 monoclonal antibodies to CR1. Clin Exp Immunol 112 27 33
21. RoweJA
RogersonSJ
RazaA
MouldsJM
KazatchkineMD
2000 Mapping of the region of complement receptor (CR) 1 required for Plasmodium falciparum rosetting and demonstration of the importance of CR1 in rosetting in field isolates. J Immunol 165 6341 6346
22. BaruchDI
GormelyJA
MaC
HowardRJ
PasloskeBL
1996 Plasmodium falciparum erythrocyte membrane protein 1 is a parasitized erythrocyte receptor for adherence to CD36, thrombospondin, and intercellular adhesion molecule 1. Proc Natl Acad Sci U S A 93 3497 3502
23. RepikA
PincusSE
GhiranI
Nicholson-WellerA
AsherDR
2005 A transgenic mouse model for studying the clearance of blood-borne pathogens via human complement receptor 1 (CR1). Clin Exp Immunol 140 230 240
24. KinoshitaT
TakedaJ
HongK
KozonoH
SakaiH
1988 Monoclonal antibodies to mouse complement receptor type 1 (CR1). Their use in a distribution study showing that mouse erythrocytes and platelets are CR1-negative. J Immunol 140 3066 3072
25. KlotzFW
ChulayJD
DanielW
MillerLH
1987 Invasion of mouse erythrocytes by the human malaria parasite, Plasmodium falciparum. J Exp Med 165 1713 1718
26. TerajimaM
MatsuiY
CopelandNG
GilbertDJ
JenkinsNA
1994 Structural organization of the mouse glycophorin A gene. J Biochem (Tokyo) 116 1105 1110
27. SoubesSC
ReidME
KanekoO
MillerLH
1999 Search for the sialic acid-independent receptor on red blood cells for invasion by Plasmodium falciparum. Vox Sang 76 107 114
28. PascualM
DuchosalMA
SteigerG
GiostraE
PechereA
1993 Circulating soluble CR1 (CD35). Serum levels in diseases and evidence for its release by human leukocytes. J Immunol 151 1702 1711
29. GardnerB
ParsonsSF
MerryAH
AnsteeDJ
1989 Epitopes on sialoglycoprotein alpha: evidence for heterogeneity in the molecule. Immunology 68 283 289
30. BaumJ
MaierAG
GoodRT
SimpsonKM
CowmanAF
2005 Invasion by P. falciparum merozoites suggests a hierarchy of molecular interactions. PLoS Pathog 1 e37
31. DesimoneTM
JenningsCV
BeiAK
ComeauxC
ColemanBI
2009 Cooperativity between Plasmodium falciparum adhesive proteins for invasion into erythrocytes. Mol Microbiol 72 578 589
32. AdamsJH
BlairPL
KanekoO
PetersonDS
2001 An expanding ebl family of Plasmodium falciparum. Trends Parasitol 17 297 299
33. GaurD
MayerDC
MillerLH
2004 Parasite ligand-host receptor interactions during invasion of erythrocytes by Plasmodium merozoites. Int J Parasitol 34 1413 1429
34. GaurD
FuruyaT
MuJ
JiangLB
SuXZ
2006 Upregulation of expression of the reticulocyte homology gene 4 in the Plasmodium falciparum clone Dd2 is associated with a switch in the erythrocyte invasion pathway. Mol Biochem Parasitol 145 205 215
35. StubbsJ
SimpsonKM
TrigliaT
PlouffeD
TonkinCJ
2005 Molecular mechanism for switching of P. falciparum invasion pathways into human erythrocytes. Science 309 1384 1387
36. ThamWH
WilsonDW
ReilingL
ChenL
BeesonJG
2009 Antibodies to Reticulocyte Binding Like Homologue 4 Inhibit Invasion of P. falciparum into Human Erythrocytes. Infect Immun
37. GaurD
SinghS
SinghS
JiangL
DioufA
2007 Recombinant Plasmodium falciparum reticulocyte homology protein 4 binds to erythrocytes and blocks invasion. Proc Natl Acad Sci U S A 104 17789 17794
38. PerssonKE
McCallumFJ
ReilingL
ListerNA
StubbsJ
2008 Variation in use of erythrocyte invasion pathways by Plasmodium falciparum mediates evasion of human inhibitory antibodies. J Clin Invest 118 342 351
39. GrechK
ChanBH
AndersRF
ReadAF
2008 The impact of immunization on competition within Plasmodium infections. Evolution 62 2359 2371
40. 2008 Methods in malaria research Manassas MR4/ATCC
41. TokumasuF
DvorakJ
2003 Development and application of quantum dots for immunocytochemistry of human erythrocytes. J Microsc 211 256 261
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2010 Číslo 6
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Requirement of NOX2 and Reactive Oxygen Species for Efficient RIG-I-Mediated Antiviral Response through Regulation of MAVS Expression
- Formation of Complexes at Plasmodesmata for Potyvirus Intercellular Movement Is Mediated by the Viral Protein P3N-PIPO
- Insight into the Mechanisms of Adenovirus Capsid Disassembly from Studies of Defensin Neutralization
- Two Novel Point Mutations in Clinical Reduce Linezolid Susceptibility and Switch on the Stringent Response to Promote Persistent Infection