Placental Syncytiotrophoblast Constitutes a Major Barrier to Vertical Transmission of

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Listeria monocytogenes is an important cause of maternal-fetal infections and serves as a model organism to study these important but poorly understood events. L. monocytogenes can infect non-phagocytic cells by two means: direct invasion and cell-to-cell spread. The relative contribution of each method to placental infection is controversial, as is the anatomical site of invasion. Here, we report for the first time the use of first trimester placental organ cultures to quantitatively analyze L. monocytogenes infection of the human placenta. Contrary to previous reports, we found that the syncytiotrophoblast, which constitutes most of the placental surface and is bathed in maternal blood, was highly resistant to L. monocytogenes infection by either internalin-mediated invasion or cell-to-cell spread. Instead, extravillous cytotrophoblasts—which anchor the placenta in the decidua (uterine lining) and abundantly express E-cadherin—served as the primary portal of entry for L. monocytogenes from both extracellular and intracellular compartments. Subsequent bacterial dissemination to the villous stroma, where fetal capillaries are found, was hampered by further cellular and histological barriers. Our study suggests the placenta has evolved multiple mechanisms to resist pathogen infection, especially from maternal blood. These findings provide a novel explanation why almost all placental pathogens have intracellular life cycles: they may need maternal cells to reach the decidua and infect the placenta.

Vyšlo v časopise: Placental Syncytiotrophoblast Constitutes a Major Barrier to Vertical Transmission of. PLoS Pathog 6(1): e32767. doi:10.1371/journal.ppat.1000732
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1000732

Souhrn

Zdroje

1. MoffettA

LokeC

2006 Immunology of placentation in eutherian mammals. Nat Rev Immunol 6 584 594

2. TrowsdaleJ

BetzAG

2006 Mother's little helpers: mechanisms of maternal-fetal tolerance. Nat Immunol 7 241 246

3. MedawarPB

1953 320 338 Some immunological and endocrinological problems raised by the evolution of viviparity in vertebrates

4. DrevetsDA

BronzeMS

2008 Listeria monocytogenes: epidemiology, human disease, and mechanisms of brain invasion. FEMS Immunol Med Microbiol

5. SwaminathanB

Gerner-SmidtP

2007 The epidemiology of human listeriosis. Microbes Infect 9 1236 1243

6. LecuitM

2007 Human listeriosis and animal models. Microbes Infect 9 1216 1225

7. MylonakisE

PaliouM

HohmannEL

CalderwoodSB

WingEJ

2002 Listeriosis during pregnancy: a case series and review of 222 cases. Medicine (Baltimore) 81 260 269

8. KajiiT

FerrierA

NiikawaN

TakaharaH

OhamaK

1980 Anatomic and chromosomal anomalies in 639 spontaneous abortuses. Hum Genet 55 87 98

9. KirkbrideCA

1993 Bacterial agents detected in a 10-year study of bovine abortions and stillbirths. J Vet Diagn Invest 5 64 68

10. KaurS

MalikSV

VaidyaVM

BarbuddheSB

2007 Listeria monocytogenes in spontaneous abortions in humans and its detection by multiplex PCR. J Appl Microbiol 103 1889 1896

11. LallemandAV

GaillardDA

ParadisPH

ChippauxCG

1992 Fetal listeriosis during the second trimester of gestation. Pediatr Pathol 12 665 671

12. TebergAJ

YonekuraML

SalminenC

PavlovaZ

1987 Clinical manifestations of epidemic neonatal listeriosis. Pediatr Infect Dis J 6 817 820

13. PamerEG

2004 Immune responses to Listeria monocytogenes. Nat Rev Immunol 4 812 823

14. PortnoyDA

2005 Manipulation of innate immunity by bacterial pathogens. Curr Opin Immunol 17 25 28

15. CossartP

Toledo-AranaA

2008 Listeria monocytogenes, a unique model in infection biology: an overview. Microbes Infect 10 1041 1050

16. BierneH

SabetC

PersonnicN

CossartP

2007 Internalins: a complex family of leucine-rich repeat-containing proteins in Listeria monocytogenes. Microbes Infect 9 1156 1166

17. MengaudJ

OhayonH

GounonP

MegeRM

CossartP

1996 E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell 84 923 932

18. ShenY

NaujokasM

ParkM

IretonK

2000 InIB-dependent internalization of Listeria is mediated by the Met receptor tyrosine kinase. Cell 103 501 510

19. O'RiordanM

PortnoyDA

2002 The host cytosol: front-line or home front? Trends Microbiol 10 361 364

20. PortnoyDA

JacksPS

HinrichsDJ

1988 Role of hemolysin for the intracellular growth of Listeria monocytogenes. J Exp Med 167 1459 1471

21. RobbinsJR

BarthAI

MarquisH

de HostosEL

NelsonWJ

1999 Listeria monocytogenes exploits normal host cell processes to spread from cell to cell. J Cell Biol 146 1333 1350

22. KocksC

GouinE

TabouretM

BercheP

OhayonH

1992 L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein. Cell 68 521 531

23. TheriotJA

MitchisonTJ

TilneyLG

PortnoyDA

1992 The rate of actin-based motility of intracellular Listeria monocytogenes equals the rate of actin polymerization. Nature 357 257 260

24. TilneyLG

PortnoyDA

1989 Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J Cell Biol 109 1597 1608

25. CarterAM

2007 Animal models of human placentation--a review. Placenta 28 Suppl A S41 47

26. CantleSJ

KaufmannP

LuckhardtM

SchweikhartG

1987 Interpretation of syncytial sprouts and bridges in the human placenta. Placenta 8 221 234

27. SchieblerTH

KaufmannP

1981

BeckerV

SchieblerTH

KubliF

Reife Placenta Stuttgart Thieme

28. BenirschkeK

KaufmannP

BaergenRN

2006 Pathology of the human placenta. 30 41 p

29. Red-HorseK

ZhouY

GenbacevO

PrakobpholA

FoulkR

2004 Trophoblast differentiation during embryo implantation and formation of the maternal-fetal interface. J Clin Invest 114 744 754

30. BakardjievAI

StacyBA

FisherSJ

PortnoyDA

2004 Listeriosis in the pregnant guinea pig: a model of vertical transmission. Infect Immun 72 489 497

31. LecuitM

NelsonDM

SmithSD

KhunH

HuerreM

2004 Targeting and crossing of the human maternofetal barrier by Listeria monocytogenes: role of internalin interaction with trophoblast E-cadherin. Proc Natl Acad Sci U S A 101 6152 6157

32. ZhouY

FisherSJ

JanatpourM

GenbacevO

DejanaE

1997 Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion? J Clin Invest 99 2139 2151

33. CoutifarisC

KaoLC

SehdevHM

ChinU

BabalolaGO

1991 E-cadherin expression during the differentiation of human trophoblasts. Development 113 767 777

34. BrownLM

LaceyHA

BakerPN

CrockerIP

2005 E-cadherin in the assessment of aberrant placental cytotrophoblast turnover in pregnancies complicated by pre-eclampsia. Histochem Cell Biol 124 499 506

35. VicovacL

AplinJD

1996 Epithelial-mesenchymal transition during trophoblast differentiation. Acta Anat (Basel) 156 202 216

36. FloridonC

NielsenO

HolundB

SundeL

WestergaardJG

2000 Localization of E-cadherin in villous, extravillous and vascular trophoblasts during intrauterine, ectopic and molar pregnancy. Mol Hum Reprod 6 943 950

37. DissonO

GrayoS

HuilletE

NikitasG

Langa-VivesF

2008 Conjugated action of two species-specific invasion proteins for fetoplacental listeriosis. Nature 455 1114 1118

38. LecuitM

DramsiS

GottardiC

Fedor-ChaikenM

GumbinerB

1999 A single amino acid in E-cadherin responsible for host specificity towards the human pathogen Listeria monocytogenes. Embo J 18 3956 3963

39. WollertT

PascheB

RochonM

DeppenmeierS

van den HeuvelJ

2007 Extending the host range of Listeria monocytogenes by rational protein design. Cell 129 891 902

40. BakardjievAI

TheriotJA

PortnoyDA

2006 Listeria monocytogenes traffics from maternal organs to the placenta and back. PLoS Pathog 2 e66 doi:10.1371/journal.ppat.0020066

41. DrevetsDA

JelinekTA

FreitagNE

2001 Listeria monocytogenes-infected phagocytes can initiate central nervous system infection in mice. Infect Immun 69 1344 1350

42. BakardjievAI

StacyBA

PortnoyDA

2005 Growth of Listeria monocytogenes in the guinea pig placenta and role of cell-to-cell spread in fetal infection. J Infect Dis 191 1889 1897

43. Le MonnierA

AutretN

Join-LambertOF

JaubertF

CharbitA

2007 ActA is required for crossing of the fetoplacental barrier by Listeria monocytogenes. Infect Immun 75 950 957

44. FisherSJ

LeitchMS

KantorMS

BasbaumCB

KramerRH

1985 Degradation of extracellular matrix by the trophoblastic cells of first-trimester human placentas. J Cell Biochem 27 31 41

45. MillerRK

GenbacevO

TurnerMA

AplinJD

CaniggiaI

2005 Human placental explants in culture: approaches and assessments. Placenta 26 439 448

46. HunkapillerNM

FisherSJ

2008 Chapter 12. Placental remodeling of the uterine vasculature. Methods Enzymol 445 281 302

47. FisherSJ

CuiTY

ZhangL

HartmanL

GrahlK

1989 Adhesive and degradative properties of human placental cytotrophoblast cells in vitro. J Cell Biol 109 891 902

48. DrakePM

GunnMD

CharoIF

TsouCL

ZhouY

2001 Human placental cytotrophoblasts attract monocytes and CD56(bright) natural killer cells via the actions of monocyte inflammatory protein 1alpha. J Exp Med 193 1199 1212

49. HuangY

ZhuXY

DuMR

LiDJ

2008 Human trophoblasts recruited T lymphocytes and monocytes into decidua by secretion of chemokine CXCL16 and interaction with CXCR6 in the first-trimester pregnancy. J Immunol 180 2367 2375

50. Red-HorseK

DrakePM

FisherSJ

2004 Human pregnancy: the role of chemokine networks at the fetal-maternal interface. Expert Rev Mol Med 6 1 14

51. GoldenbergRL

HauthJC

AndrewsWW

2000 Intrauterine infection and preterm delivery. N Engl J Med 342 1500 1507

52. FornerL

LarsenT

KilianM

HolmstrupP

2006 Incidence of bacteremia after chewing, tooth brushing and scaling in individuals with periodontal inflammation. J Clin Periodontol 33 401 407

53. CobeHM

1954 Transitory bacteremia. Oral Surg Oral Med Oral Pathol 7 609 615

54. NotermansS

DufrenneJ

TeunisP

ChackrabortyT

1998 Studies on the risk assessment of Listeria monocytogenes. J Food Prot 61 244 248

55. PentecostM

OttoG

TheriotJA

AmievaMR

2006 Listeria monocytogenes invades the epithelial junctions at sites of cell extrusion. PLoS Pathog 2 e3 doi:10.1371/journal.ppat.0020003

56. OcklefordCD

WakelyJ

BadleyRA

1981 Morphogenesis of human placental chorionic villi: cytoskeletal, syncytioskeletal and extracellular matrix proteins. Proc R Soc Lond B Biol Sci 212 305 316

57. BerrymanM

GaryR

BretscherA

1995 Ezrin oligomers are major cytoskeletal components of placental microvilli: a proposal for their involvement in cortical morphogenesis. J Cell Biol 131 1231 1242

58. BehamA

DenkH

DesoyeG

1988 The distribution of intermediate filament proteins, actin and desmoplakins in human placental tissue as revealed by polyclonal and monoclonal antibodies. Placenta 9 479 492

59. KingBF

1983 The organization of actin filaments in human placental villi. J Ultrastruct Res 85 320 328

60. VacekZ

1969 Electron microscopic observations on the filaments in the trophoblast of the human placenta. Folia Morphol (Praha) 17 382 388

61. ScheunerG

RuckhaberleKE

FlemmingG

ReissigD

1980 [Submicroscopic detection of oriented protein filaments in the plasmoditrophoblast of the human placenta (author's transl)]. Anat Anz 147 145 151

62. RajabianT

GavicherlaB

HeisigM

Muller-AltrockS

GoebelW

2009 The bacterial virulence factor InlC perturbs apical cell junctions and promotes cell-to-cell spread of Listeria. Nat Cell Biol 11 1212 1218

63. KoiH

ZhangJ

MakrigiannakisA

GetsiosS

MacCalmanCD

2002 Syncytiotrophoblast is a barrier to maternal-fetal transmission of herpes simplex virus. Biol Reprod 67 1572 1579

64. MaidjiE

McDonaghS

GenbacevO

TabataT

PereiraL

2006 Maternal antibodies enhance or prevent cytomegalovirus infection in the placenta by neonatal Fc receptor-mediated transcytosis. Am J Pathol 168 1210 1226

65. FisherS

GenbacevO

MaidjiE

PereiraL

2000 Human cytomegalovirus infection of placental cytotrophoblasts in vitro and in utero: implications for transmission and pathogenesis. J Virol 74 6808 6820

66. SoorannaSR

Oteng-NtimE

MeahR

RyderTA

BajoriaR

1999 Characterization of human placental explants: morphological, biochemical and physiological studies using first and third trimester placenta. Hum Reprod 14 536 541

67. GenbacevO

SchubachSA

MillerRK

1992 Villous culture of first trimester human placenta–model to study extravillous trophoblast (EVT) differentiation. Placenta 13 439 461

68. GlomskiIJ

DecaturAL

PortnoyDA

2003 Listeria monocytogenes mutants that fail to compartmentalize listerolysin O activity are cytotoxic, avirulent, and unable to evade host extracellular defenses. Infect Immun 71 6754 6765

69. GenbacevO

McMasterMT

FisherSJ

2000 A repertoire of cell cycle regulators whose expression is coordinated with human cytotrophoblast differentiation. Am J Pathol 157 1337 1351

70. GenbacevO

ZhouY

LudlowJW

FisherSJ

1997 Regulation of human placental development by oxygen tension. Science 277 1669 1672

71. BarnesPD

BergmanMA

MecsasJ

IsbergRR

2006 Yersinia pseudotuberculosis disseminates directly from a replicating bacterial pool in the intestine. J Exp Med 203 1591 1601

72. KimKS

2008 Mechanisms of microbial traversal of the blood-brain barrier. Nat Rev Microbiol 6 625 634

73. BishopDK

HinrichsDJ

1987 Adoptive transfer of immunity to Listeria monocytogenes. The influence of in vitro stimulation on lymphocyte subset requirements. J Immunol 139 2005 2009

74. SkobleJ

PortnoyDA

WelchMD

2000 Three regions within ActA promote Arp2/3 complex-mediated actin nucleation and Listeria monocytogenes motility. J Cell Biol 150 527 538

75. ShenA

HigginsDE

2005 The 5′ untranslated region-mediated enhancement of intracellular listeriolysin O production is required for Listeria monocytogenes pathogenicity. Mol Microbiol 57 1460 1473

76. JonesS

PortnoyDA

1994 Intracellular growth of bacteria. Methods Enzymol 236 463 467

77. SundstromC

NilssonK

1976 Establishment and characterization of a human histiocytic lymphoma cell line (U-937). Int J Cancer 17 565 577