Skip to main content

Polarised Transfer of Proteins Through the Syncytiotrophobalst and Tissue Culture Cell Lines

  • Chapter
  • First Online:
Maternal Fetal Transmission of Human Viruses and their Influence on Tumorigenesis

Abstract

Transfer of polar, high-molecular weight solutes across the placenta is facilitated by a specialized, vesicular transport mechanism termed transcytosis. In contrast to the ex vivo polarised tissue culture systems, the syncytiotrophoblast at the maternal-fetal interface does not allow intercellular transfer, but probably transcellular transfer of cells and substances are allowed.

Series of transporters, (i) phagocytosis, (ii) macropinocytosis, (iii) the classical clathrin-mediated endocytosis, (iv) dynamin-dependent endocytosis via (v) glycolipid rafts, (vi) clathrin, caveolae, and dynamin-independent endocytosis that requires lipid rafts, and (vii) dynamin-independent endocytosis that does not involve clathrin-coated pits, caveolae or lipid rafts were shown to provide the fetus with substances required for its development and growth.

The Fc- and other receptor mediated transport is of essential importance for the development of fetal immune system. Nanoparticles, however also can be transferred through the human placenta and deposited in different organs of the fetus.

The transcytosis of antibodies, antigen-antibody complexes and anti-idiotypic antibodies (Ab2) is probably the most important for the development of the fetal immune system. Induction of TREG cells, priming of fetal B- and T-cells, induction of memory cells, breakage of immunotolerance are the most important consequences suggested. HLA haplotypes were found to be important for the responses elicited by changes of the Id-anti-Id network. Anti-idiotypic antibodies were shown to react with T-cell receptors and induce antigen specific clones of oncolytic properties.

Transplacental transfer of anti-Ids were found to reduce the risk of diabetes of fetuses who’s mother were suffering from lupus. The long term interaction of B-cell and T-cell receptors and anti-idiotypic antibody networks can have therapeutic effects to malignancies of lymphocyte origin similar to the effect of monoclonal antibodies discussed in other chapters of this volume.

The “non-cytocydal” long term elimination of vertically transmitted hepatitis B carrier state seems to occur by the interplay of the partially resolved mechanisms described in this chapter.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abrahams VM, Bole-Aldo P, Kim YM, Straszewski-Chavez SL, Chaiworapongsa T, Romero R, Mor G (2004) Divergent trophoblast responses to bacterial products mediated by TLRs. J Immunol 173:4286–4296

    PubMed  CAS  Google Scholar 

  • Abrahams VM, Aldo PB, Murphy SP, Visintin I, Koga K, Wilson G, Romero R, Sharma S, Mor G (2008) TLR6 modulates first trimester trophoblast responses to peptidoglycan. J Immunol 180:6035–6043

    PubMed  CAS  Google Scholar 

  • Akilesh S, Petkova S, Sproule TJ, Shaffer DJ, Christianson GJ, Roopenian DC (2004) The MHC class I like Fc receptor promotes humorally mediated autoimmune disease. J Clin Invest 113:1328–1333. doi:10.1172/JCI18838

    PubMed  CAS  Google Scholar 

  • Amu S, Brisslert M (2011) Phenotype and function of CD25-expressing B lymphocytes isolated from human umbilical cord blood. Clin Dev Immunol 2011:481948. doi:10.1155/2011/481948

    PubMed  Google Scholar 

  • Apps R, Murphy SP, Fernando R, Gardner L, Ahad T, Moffett A (2009) Human leucocyte antigen (HLA) expression of primary trophoblast cells and placental cell lines, determined using single antigen beads to characterize allotype specificities of anti-HLA antibodies. Immunology 127:26–39. doi:10.1111/j.1365-2567.2008.03019.x DOI:dx.doi.org

    PubMed  CAS  Google Scholar 

  • Balogh A, Pozsgay J, Matkó J, Dong Z, Kim CJ, Várkonyi T, Sammar M, Rigó J Jr, Meiri H, Romero R, Papp Z, Than NG (2011) Placental protein 13 (PP13/galectin-13) undergoes lipid raft-associated subcellular redistribution in the syncytiotrophoblast in preterm preeclampsia and HELLP syndrome. Am J Obstet Gynecol 205:156.e1. doi:10.1016/j.ajog.2011.03.023

    Google Scholar 

  • Baranov VI, Sopova EA, Zemlianoĭ PV (2009) Occupational hygiene and hygienic regulations during the manufacture, use and utilization of nanomaterials; Russian. Gig Sanit 6:53–55

    Google Scholar 

  • Basha S, Vaidhyanathan S, Pauletti GM (2011) Selection of peptide ligands for human placental transcytosis systems using in vitro phage display. Methods Mol Biol 716:141–156

    PubMed  CAS  Google Scholar 

  • Baskar S, Kobrin CB, Kwak LW (2004) Autologous lymphoma vaccines induce human T cell responses against multiple, unique epitopes. J Clin Invest 113:1498–1510. doi:10.1172/JCI200420312

    PubMed  CAS  Google Scholar 

  • Belkacemi L, Bédard I, Simoneau L, Lafond J (2005) Calcium channels, transporters and exchangers in placenta: a review. Cell Calcium 37:1–8, review

    PubMed  CAS  Google Scholar 

  • Berencsi Gy, Csire M, Kapusinszky B, Takács M (2009) The modifications of the fetal immune system by maternal antibodies, anti-idiotypes, viruses and virus-antibody complexes. In Hungarian. Focus Med 10:3–10

    Google Scholar 

  • Berencsi Gy, Csire M, Takács M (2010) Maternal antibodies, virus-antibody complexes and transfer of anti-idiotype antibodies into the fetal tissues, in Hungarian. Egeszsegtudomany 54:48–62

    Google Scholar 

  • Bhat P, Anderson DA (2007) Hepatitis B virus translocates across a trophoblastic barrier. J Virol 81:7200–7207. doi:10.1128/JVI.02371-06

    PubMed  CAS  Google Scholar 

  • Bhattacharya-Chatterjee M, Chatterjee SK, Foon KA (2002) Anti-idiotype antibody vaccine therapy for cancer. Expert Opin Biol Ther 2:869–881. doi:10.1517/14712598.2.8.869

    PubMed  CAS  Google Scholar 

  • Birn H (2006) The kidney in vitamin B12 and folate homeostasis: characterization of receptors for tubular uptake of vitamins and carrier proteins. Am J Physiol Renal Physiol 291:F22–F36. doi:10.1152/ajprenal.00385.2005

    PubMed  CAS  Google Scholar 

  • Bode CJ, Jin H, Rytting E, Silverstein PS, Young AM, Audus KL (2006) In vitro models for studying trophoblast transcellular transport. Methods Mol Med 122:225–239

    PubMed  CAS  Google Scholar 

  • Bodo A, Bakos E, Szeri F, Varadi A, Sarkadi B (2003) The role of multidrug transporters in drug availability, metabolism and toxicity. Toxicol Lett 140–1:133–143

    Google Scholar 

  • Bogen B, Ruffini P (2009) Review: to what extent are T cells tolerant to immunoglobulin variable regions? Scand J Immunol 70:526–530. doi:10.1111/j.1365-3083.2009.02340.x

    PubMed  CAS  Google Scholar 

  • Botos E, Turi A, Müllner N, Kovalszky I, Tátrai P, Kiss AL (2007) Regulatory role of kinases and phosphatases on the internalisation of caveolae in HepG2 cells. Micron 38:313–320. doi:10.1016/j.micron.2006.03.012

    PubMed  CAS  Google Scholar 

  • Brambell FW, Hemmings WA, Morris IG (1964) A theoretical model of γ-globulin catabolism. Nature 203:1352–1354

    PubMed  CAS  Google Scholar 

  • Bu HF, Wang X, Tang Y, Koti V, Tan XD (2010) Toll-like receptor 2-mediated peptidoglycan uptake by immature intestinal epithelial cells from apical side and exosome-associated transcellular transcytosis. J Cell Physiol 222:658–668

    PubMed  CAS  Google Scholar 

  • Bullen BE, Bloxam DL, Ryder TA, Mobberley MA, Bax CM (1990) Two-sided culture of human placental trophoblast. Morphology, immunocytochemistry and permeability properties. Placenta 11:431–450. doi:10.1016/S0143-4004(05)80217-6

    PubMed  CAS  Google Scholar 

  • Cerneus DP, van der Ende A (1991) Apical and basolateral transferrin receptors in polarized BeWo cells recycle through separate endosomes. J Cell Biol 114:1149–1158. doi:10.1083/jcb.114.6.1149

    PubMed  CAS  Google Scholar 

  • Chang MH, Hsu HY, Huang LM, Lee PI, Lin HH, Lee CY (1996) The role of transplacental hepatitis B core antibody in the mother-to-infant transmission of hepatitis B virus. J Hepatol 24:674–679. doi:10.1016/S0168-8278(96)80262-5 DOI:dx.doi.org

    PubMed  CAS  Google Scholar 

  • Cheng ZJ, Singh RD, Marks DL, Pagano RE (2006) Membrane microdomains, caveolae, and caveolar endocytosis of sphingolipids. Mol Membr Biol 23:101–110. doi:10.1080/09687860500460041, Review

    PubMed  CAS  Google Scholar 

  • Chomont N, Hocini H, Gody JC, Bouhlal H, Becquart P, Krief-Bouillet C, Kazatchkine M, Bélec L (2008) Neutralizing monoclonal antibodies to human immunodeficiency virus type 1 do not inhibit viral transcytosis through mucosal epithelial cells. Virology 370:246–254. doi:10.1016/j.virol.2007.09.006

    PubMed  CAS  Google Scholar 

  • Conner SD, Schmid SL (2003) Regulated portals of entry into the cell. Nature 422:37–44. doi:10.1038/nature01451

    PubMed  CAS  Google Scholar 

  • Cozens AL, Yezzi MJ, Kunzelmann K, Ohrui T, Chin L, Eng K, Finkbeiner WE, Widdicombe JH, Gruenert DC (1994) CFTR expression and chloride secretion in polarized immortal human bronchial epithelial cells. Am J Respir Cell Mol Biol 10:38–47

    Google Scholar 

  • Cui S, Verroust PJ, Moestrup SK, Christensen EI (1996) Megalin/gp330 mediates uptake of albumin in renal proximal tubule. Am J Physiol 271:F900–F907

    PubMed  CAS  Google Scholar 

  • Cupps TR, Hoofnagle JH, Ellis RW, Miller WJ, Seeff L, Guerrera A, Gerin JL, Haas-Smith SA (1989a) In vitro immune responses to hepatitis B surface antigen (pre-S2 and S) following remote infection by hepatitis B virus in humans. J Clin Immunol 9:229–241. doi:10.1007/BF00916819

    PubMed  CAS  Google Scholar 

  • Cupps TR, Haas-Smith SA, Gerin JL, Tibbles JL, Kennedy RC (1989b) Anti-idiotype modulation of the in vitro immune response to hepatitis B surface antigen (HBsAg) following remote infection by hepatitis B virus in man. Cell Immunol 122:244–250. doi:10.1016/0008-8749(89)90164-0

    PubMed  CAS  Google Scholar 

  • Dankers PY, Boomker JM, Huizinga-van der Vlag A, Wisse E, Appel WP, Smedts FM, Harmsen MC, Bosman AW, Meijer W, van Luyn MJ (2011) Bioengineering of living renal membranes consisting of hierarchical, bioactive supramolecular meshes and human tubular cells. Biomaterials 32:723–733. doi:10.1016/j.biomaterials.2010.09.020

    PubMed  CAS  Google Scholar 

  • Demanet C, Brissinck J, Leo O, Moser M, Thielemans K (1994) Role of T-cell subsets in the bispecific antibody (anti-idiotype x anti-CD3) treatment of the BCL1 lymphoma. Cancer Res 54:2973–2978

    PubMed  CAS  Google Scholar 

  • Dickinson BL, Badizadegan K, Wu Z, Ahouse JC, Zhu X, Simister NE, Blumberg RS, Lencer WI (1999) Bidirectional FcRn-dependent IgG transport in a polarized human intestinal epithelial cell line. J Clin Invest 104:903–911. doi:10.1172/JCI6968

    PubMed  CAS  Google Scholar 

  • Duff C, Murphy PG, Callaghan M, McClean S (2006) Differences in invasion and translocation of Burkholderia cepacia complex species in polarised lung epithelial cells in vitro. Microb Pathog 41:183–192. doi:10.1016/j.micpath.2006.07.005 DOI:dx.doi.org

    PubMed  CAS  Google Scholar 

  • Durrant LG, Parsons T, Moss R, Spendlove I, Carter G, Carr F (2001) Human anti-idiotypic antibodies can be good immunogens as they target FC receptors on antigen-presenting cells allowing efficient stimulation of both helper and cytotoxic T-cell responses. Int J Cancer 92:414–420. doi:10.1002/ijc.1194

    PubMed  CAS  Google Scholar 

  • Errasti-Murugarren E, Diaz P, Godoy V, Riquelme G, Pastor-Anglada M (2011) Expression and distribution of nucleoside transporter in the human syncytiotrophoblast. Mol Pharmacol 80(5):809–817. doi:10.1124/mol.111.071837

    PubMed  CAS  Google Scholar 

  • Falcioni F, Vidović D, Ward ES, Bolin D, Singh G, Shah H, Ober B, Nagy ZA (1995) Self tolerance to T cell receptor V beta sequences. J Exp Med 182:249–254. doi:10.1084/jem.182.1.249

    PubMed  CAS  Google Scholar 

  • Firan M, Bawdon R, Radu C, Ober RJ, Eaken D, Antohe F, Ghetie V, Ward ES (2001) The MHC class I related receptor, FcRn, plays an essential role in the maternofetal transfer of γ-globulin in humans. Int Immunol 13:993–1002

    PubMed  CAS  Google Scholar 

  • Foraker AB, Ray A, Da Silva TC, Bareford LM, Hillgren KM, Schmittgen TD, Swaan PW (2007) Dynamin 2 regulates riboflavin endocytosis in human placental trophoblasts. Mol Pharmacol 72:553–562. doi:10.1124/mol.107.037101

    PubMed  CAS  Google Scholar 

  • Fujisawa T, Sogo T, Komatsu H, Inui A (2007) Autoimmune hepatitis in childhood. Hepatol Res 37:S496. doi:10.1111/j.1872-034X.2007.00248.x

    PubMed  CAS  Google Scholar 

  • Ghetie V, Ward ES (2000) Multiple roles for the major histocompatibility complex class I-related receptor FcRn. Annu Rev Immunol 18:739–766. doi:10.1146/annurev.immunol.18.1.739

    PubMed  CAS  Google Scholar 

  • Ghinea N, Hai MTV, Groyer-Picard M-T, Milgrom E (1994) How protein hormones reach their target cells. Receptor-mediated transcytosis of hCG through endothelial cells. J Cell Biol 125:87–97. doi:10.1083/jcb.125.1.87 DOI:dx.doi.org

    PubMed  CAS  Google Scholar 

  • Graham CH, Hawley TS, Hawley RG, MacDougall JR, Kerbel RS, Khoo N, Lala PK (1993) Establishment and characterization of first trimester human trophoblast cells with extended lifespan. Exp Cell Res 206:204–211. doi:10.1006/excr.1993.1139 DOI:dx.doi.org

    PubMed  CAS  Google Scholar 

  • Hill E, van der Kaay J, Downes CP, Smythe E (2001) The role of dynamin and its binding partners in coated pit invagination. J Cell Biol 152:309–323. doi:10.1083/jcb.152.2.309

    PubMed  CAS  Google Scholar 

  • Hunziker W, Mellman I (1989) Expression of macrophage-lymphocyte Fc receptors in Madin-Darby canine kidney cells: polarity and transcytosis differ for isoforms with or without coated pit localization domains. J Cell Biol 109(6 Pt 2):3291–3302. doi:10.1083/jcb.109.6.3291

    PubMed  CAS  Google Scholar 

  • Irving WL, James DK, Stephenson T, Laing P, Jameson C, Oxford JS, Chakraverty P, Brown DW, Boon AC, Zambon MC (2000) Influenza virus infection in the second and third trimesters of pregnancy: a clinical and seroepidemiological study. BJOG 107:1282–1289. doi:10.1111/j.1471-0528.2000.tb11621.x

    PubMed  CAS  Google Scholar 

  • Jørgensen T, Hannestad K (1980) H–2-linked genes control immune response to V-domains of myeloma protein 315. Nature 288:396–397. doi:10.1038/288396a0

    PubMed  Google Scholar 

  • Jørgensen T, Gaudernack G, Hannestad K (1980) Immunization with the light chain and the VL domain of the isologous myeloma protein 315 inhibits growth of mouse plasmacytoma MOPC315. Scand J Immunol 11:29–35

    PubMed  Google Scholar 

  • Kekuda R, Leibach FH, Furesz TC, Smith CH, Ganapathy V (2000) Polarized distribution of interleukin-1 receptors and their role in regulation of serotonin transporter in placenta. J Pharmacol Exp Ther 292:1032–1041

    PubMed  CAS  Google Scholar 

  • Kim D, Huey D, Oglesbee M, Niewiesk S (2011) Insights into the regulatory mechanism controlling the inhibition of vaccine-induced seroconversion by maternal antibodies. Blood 117:6143–6151. doi:10.1182/blood-2010-11-320317

    PubMed  CAS  Google Scholar 

  • Kronenberg M, Siu G, Hood LH, Shastri N (1986) The molecular genetics of the T-cell antigen receptor and T-cell antigen recognition. Annu Rev Immunol 4:529–591. doi:10.1146/annurev.iy.04.040186.002525

    PubMed  CAS  Google Scholar 

  • Kwak LW, Young HA, Pennington RW, Weeks SD (1996) Vaccination with syngeneic, lymphoma-derived immunoglobulin idiotype combined with granulocyte/macrophage colony-stimulating factor primes mice for a protective T-cell response. Proc Natl Acad Sci USA 93:10972–10977

    PubMed  CAS  Google Scholar 

  • Lambot N, Lybaert P, Boom A, Delogne-Desnoeck J, Vanbellinghen AM, Graff G, Lebrun P, Meuris S (2006) Evidence for a clathrin-mediated recycling of albumin in human term placenta. Biol Reprod 75:90–97. doi:10.1095/biolreprod.105.050021

    PubMed  CAS  Google Scholar 

  • Lauritzsen GF, Weiss S, Dembic Z, Bogen B (1994) Naive idiotype specific CD4? T cells and immunosurveillance of B-cell tumors. Proc Natl Acad Sci USA 91:5700–5704. doi:10.1073/pnas.91.12.5700

    PubMed  CAS  Google Scholar 

  • Lee WK, Choi JK, Cha SH (2008) Co-localization and interaction of human organic anion transporter 4 with caveolin-1 in primary cultured human placental trophoblasts. Exp Mol Med 40:505–513. doi:10.3858/emm.2008.40.5.505

    PubMed  CAS  Google Scholar 

  • Lemke H, Tanasa RI, Trad A, Lange H (2009) Benefits and burden of the maternally-mediated immunological imprinting. Autoimmun Rev 8:394–399. doi:10.1016/j.autrev.2008.12.005, Review

    PubMed  CAS  Google Scholar 

  • Levitsky HI, Montgomery J, Ahmadzadeh M, Staveley-O’Carroll K, Guarnieri F, Longo DL, Kwak LW (1996) Immunization with granulocyte-macrophage colony-stimulating factor-transduced, but not B7–1-transduced, lymphoma cells primes idiotype-specific T cells and generates potent systemic antitumor immunity. J Immunol 156:3858–3865

    PubMed  CAS  Google Scholar 

  • Levy R, Robertson M, Leonard J, Vose J, Denney D (2008) Results of a phase 3 trial evaluating safety and efficacy of specific immunotherapy, recombinant idiotype (Id) conjugated to KLH (Id-KLH) with GM-CSF, compared to non-specific immunotherapy, KLH with GM-CSF, in patients with follicular nonhodgkin’s lymphoma (fNHL). Ann Oncol 19(Suppl 4):iv101

    Google Scholar 

  • Li H, Nowak-Wegrzyn A, Charlop-Powers Z, Shreffler W, Chehade M, Thomas S, Roda G, Dahan S, Sperber K, Berin MC (2006) Transcytosis of IgE-antigen complexes by CD23a in human intestinal epithelial cells and its role in food allergy. Gastroenterology 131:47–58. doi:10.1053/j.gastro.2006.03.044

    PubMed  CAS  Google Scholar 

  • Lim HW, Broxmeyer HE, Kim CH (2006) Regulation of trafficking receptor expression in human forkhead box P3+regulatory T cells. J Immunol 177:840–851

    PubMed  CAS  Google Scholar 

  • Liu X, Ye L, Christianson GJ, Yang JQ, Roopenian DC, Zhu X (2007) NF-kappaB signaling regulates functional expression of the MHC class I-related neonatal Fc receptor for IgG via intronic binding sequences. J Immunol 179:2999–3011

    PubMed  CAS  Google Scholar 

  • Liu X, Ye L, Bai Y, Mojidi H, Simister NE, Zhu X (2008) Activation of the JAK/STAT-1 signaling pathway by IFN-gamma can down-regulate functional expression of the MHC class I-related neonatal Fc receptor for IgG. J Immunol 181:449–463

    PubMed  CAS  Google Scholar 

  • Lopez V, Kelleher SL, Lonnerdal B (2008) Lactoferrin receptor mediates apo- but not holo-lactoferrin internalization via clathrin-mediated endocytosis in trophoblasts. Biochem J 411:271. doi:10.1042/BJ20070393

    CAS  Google Scholar 

  • Lyden TW, Anderson CL, Robinson JM (2002) The endothelium but not the syncytiotrophoblast of human placenta expresses caveolae. Placenta 23:640–652. doi:10.1053/plac.2002.0847

    PubMed  Google Scholar 

  • Malley A, Dresser DW (1982) Anti-idiotype regulation of timothy grass pollen IgE antibody formation. I. In vivo induction of suppressor T cells. Immunology 46:653–659

    PubMed  CAS  Google Scholar 

  • Malley A, Dresser DW (1983) Anti-idiotype regulation of the formation of IgE antibody to timothy grass pollen. II. In vitro induction of suppressor T cells in mini-Marbrook cultures. Immunology 48:93–99

    PubMed  CAS  Google Scholar 

  • Mandic Havelka A, Yektaei-Karin E, Hultenby K, Sørensen OE, Lundahl J, Berggren V, Marchini G (2010) Maternal plasma level of antimicrobial peptide LL37 is a major determinant factor of neonatal plasma LL37 level. Acta Paediatr 99:836–841. doi:10.1111/j.1651-2227.2010.01726.x

    PubMed  CAS  Google Scholar 

  • Marsh M, McMahon HT (1999) The structural era of endocytosis. Science 285:215–220. doi:10.1126/science.285.5425.215

    PubMed  CAS  Google Scholar 

  • Marski M, Kandula S, Turner JR, Abraham C (2005) CD18 is required for optimal development and function of CD4+ CD25+ T regulatory cells. J Immunol 175:7889–7897

    PubMed  CAS  Google Scholar 

  • Mazza G, Housset D, Piras C, Grégoire C, Fontecilla-Camps JC, Malissen B (1999) Structural features of the interaction between an anti-clonotypic antibody and its cognate T-cell antigen receptor. J Mol Biol 287:773–780. doi:10.1006/jmbi.1999.2645 DOI:dx.doi.org

    PubMed  CAS  Google Scholar 

  • Menezes V, Malek A, Keelan JA (2011) Nanoparticulate drug delivery in pregnancy: placental passage and fetal exposure. Curr Pharm Biotechnol 12:731–742, Review

    PubMed  CAS  Google Scholar 

  • Mezo AR, Sridhar V, Badger J, Sakorafas P, Nienaber V (2010) X-ray crystal structures of monomeric and dimeric peptide inhibitors in complex with the human neonatal Fc receptor, FcRn. J Biol Chem 285:27694–27701. doi:10.1074/jbc.M110.120667

    PubMed  CAS  Google Scholar 

  • Mishima T, Kurasawa G, Ishikawa G, Mori M, Kawahigashi Y, Ishikawa T, Luo SS, Takizawa T, Goto T, Matsubara S, Takeshita T, Robinson JM, Takizawa T (2007) Endothelial expression of Fc gamma receptor IIb in the full-term human placenta. Placenta 28:170. doi:10.1016/j.placenta.2006.01.024 DOI:dx.doi.org

    PubMed  CAS  Google Scholar 

  • Mitchell AM, Yap AS, Payne EJ, Manley SW, Mortimer RH (1995) Characterization of cell polarity and epithelial junctions in the choriocarcinoma cell line, JAR. Placenta 16:31–39. doi:10.1016/0143-4004(95)90079-9

    PubMed  CAS  Google Scholar 

  • Mohanty S, Anderson CL, Robinson JM (2010) The expression of caveolin-1 and the distribution of caveolae in the murine placenta and yolk sac: parallels to the human placenta. Placenta 31:144–150. doi:10.1016/j.placenta.2009.11.007

    PubMed  CAS  Google Scholar 

  • Mostov K, Deitcher DL (1986) Polymeric immunoglobulin receptor expressed in MDCK cells transcytoses IgA. Cell 46:613–621. doi:10.1016/0092-8674(86)90887-1 DOI:dx.doi.org

    PubMed  CAS  Google Scholar 

  • Nabi IR, Le PU (2003) Caveolae/raft-dependent endocytosis. J Cell Biol 161:673–677. doi:10.1083/jcb.200302028

    PubMed  CAS  Google Scholar 

  • Naslavsky N, Weigert R, Donaldson JG (2003) Convergence of non-clathrin-and clathrin-derived endosomes involves Arf6 inactivation and changes in phosphoinositides. Mol Biol Cell 14:417–431. doi:10.1091/mbc.02-04-0053

    PubMed  CAS  Google Scholar 

  • Naslavsky N, Weigert R, Donaldson JG (2004) Characterization of a nonclathrin endocytic pathway: membrane cargo and lipid requirements. Mol Biol Cell 15:3542–3552. doi:10.1091/mbc.E04-02-0151

    PubMed  CAS  Google Scholar 

  • Navarrete MA, Heining-Mikesch K, Bertinetti-Lapatki C, Duehren-von Minden M, Hafkemeyer A, Veelken H (2008) Vaccination with recombinant idiotype Fab fragments induces specific cellular immunity and clinical responses in untreated Bcell lymphoma patients. Blood 112:235

    Google Scholar 

  • Nishimura T, Seki Y, Sato K, Chishu T, Kose N, Terasaki T, Kang YS, Sai Y, Nakashima E (2008) Enhancement of zidovudine uptake by dehydroepiandrosterone sulfate in rat syncytiotrophoblast cell line TR-TBT 18d-1. Drug Metab Dispos 36:2080–2085. doi:10.1124/dmd.108.021345 DOI:dx.doi.org

    PubMed  CAS  Google Scholar 

  • Oestreich KJ, Yoon H, Ahmed R, Boss JM (2008) NFATc1 regulates PD-1 expression upon T cell activation. J Immunol 181:4832–4839

    PubMed  CAS  Google Scholar 

  • Okazaki T, Honjo T (2007) PD-1 and PD-1 ligands: from discovery to clinical application. Int Immunol 19:813–824. doi:10.1093/intimm/dxm057 DOI:dx.doi.org

    PubMed  CAS  Google Scholar 

  • Ördög K, Szendrői A, Szarka K, Kugler Z, Csire M, Kapusinszky B, Xie J, Csizmadia K, Brojnás J, Rusvai E, Tempfli A, Berencsi G (2003) Perinatal and intrafamily transmission of hepatitis B virus in three generations of a low-prevalence population. J Med Virol 70:194–204. doi:10.1002/jmv.10378

    PubMed  Google Scholar 

  • Osterroth F, Garbe A, Fisch P, Veelken H (2000) Stimulation of cytotoxic T cells against idiotype immunoglobulin of malignant lymphoma with protein-pulsed or idiotype-transduced dendritic cells. Blood 95:1342–1349

    PubMed  CAS  Google Scholar 

  • Ozben T (2006) Mechanisms and strategies to overcome multiple drug resistance in cancer. FEBS Lett 580:2903–2909. doi:10.1016/j.febslet.2006.02.020

    PubMed  CAS  Google Scholar 

  • Parry S, Zhang J (2007) Multidrug resistance proteins affect drug transmission across the placenta. Am J Obstet Gynecol 196:476.e1-6. doi:10.1016/j.ajog.2007.02.019

    PubMed  Google Scholar 

  • Parry S, Zhang J, Koi H, Arechavaleta-Velasco F, Elovitz MA (2006) Transcytosis of Human immunodeficiency virus 1 across the placenta is enhanced by treatment with tumour necrosis factor alpha. J Gen Virol 87:2269–2278. doi:10.1099/vir.0.81071-0

    PubMed  CAS  Google Scholar 

  • Patni S, Wynen LP, Seager AL, Morgan G, White JO, Thornton CA (2009) Expression and activity of Toll-like receptors 1–9 in the human term placenta and changes associated with labor at term. Biol Reprod 80:243–248. doi:10.1095/biolreprod.108.069252 DOI:dx.doi.org

    PubMed  CAS  Google Scholar 

  • Pelkmans L, Helenius A (2003) Insider information: what viruses tell us about endocytosis. Curr Opin Cell Biol 15:414–422. doi:10.1016/S0955-0674(03)00081-4

    PubMed  CAS  Google Scholar 

  • Perret E, Lakkaraju A, Deborde S, Schreiner R, Rodriguez-Boulan E (2005) Evolving endosomes: how many varieties and why? Curr Opin Cell Biol 17:423–434. doi:10.1016/j.ceb.2005.06.008

    PubMed  CAS  Google Scholar 

  • Peterson MD, Mooseker MS (1992) Characterization of the enterocyte-like brush border cytoskeleton of the C2BBe clones of the human intestinal cell line, Caco-2. J Cell Sci 102:581–600

    PubMed  CAS  Google Scholar 

  • Prabhat P, Gan Z, Chao J, Ram S, Vaccaro C, Gibbons S, Ober RJ, Ward ES (2007) Elucidation of intracellular recycling pathways leading to exocytosis of the Fc receptor, FcRn, by using multifocal plane microscopy. Proc Natl Acad Sci USA 104:5889–5894. doi:10.1073/pnas.0700337104

    PubMed  CAS  Google Scholar 

  • Praetor A, Ellinger I, Hunziker W (1999) Intracellular traffic of the MHC class I-like IgG Fc receptor, FcRn, expressed in epithelial MDCK cells. J Cell Sci 112(Pt 14):2291–2299

    PubMed  CAS  Google Scholar 

  • Raghavan MV, Bonagura R, Morrison SL, Bjorkman PJ (1995) Analysis of the pH dependence of the neonatal Fc receptor/immunoglobulin G interaction using antibody and receptor variants. Biochemistry 34:14649–14657. doi:10.1021/bi00045a005

    PubMed  CAS  Google Scholar 

  • Rastogi D, Wang C, Mao X, Lendor C, Rothman PB, Miller RL (2007) Antigen-specific immune responses to influenza vaccine in utero. J Clin Invest 117:1637–1646

    PubMed  CAS  Google Scholar 

  • Reinartz S, Pfisterer J, du Bois A, Jackisch C, Baumann KH, Wagner U (2010) Suppressive activity rather than frequency of FoxP3(+) regulatory T cells is essential for CA-125-specific T-cell activation after abagovomab treatment. Hum Immunol 71:36–44. doi:10.1016/j.humimm.2009.09.356

    PubMed  CAS  Google Scholar 

  • Reiser JB, Darnault C, Grégoire C, Mosser T, Mazza G, Kearney A, van der Merwe PA, Fontecilla-Camps JC, Housset D, Malissen B (2003) CDR3 loop flexibility contributes to the degeneracy of TCR recognition. Nat Immunol 4:241–247. doi:10.1038/ni891

    PubMed  CAS  Google Scholar 

  • Riley JL (2009) PD-1 signaling in primary T cells. Immunol Rev 229:114–125. doi:10.1111/j.1600-065X.2009.00767.x

    PubMed  CAS  Google Scholar 

  • Sabharanjak S, Sharma P, Parton RG, Mayor S (2002) GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev Cell 2:411–423. doi:10.1016/S1534-5807(02)00145-4

    PubMed  CAS  Google Scholar 

  • Saha A, Baral RN, Chatterjee SK, Mohanty K, Pal S, Foon KA, Primus FJ, Krieg AM, Weiner GJ, Bhattacharya-Chatterjee M (2006a) CpG oligonucleotides enhance the tumor antigen-specific immune response of an anti-idiotype antibody-based vaccine strategy in CEA transgenic mice. Cancer Immunol Immunother 55:515–527. doi:10.1007/s00262-005-0009-6

    PubMed  Google Scholar 

  • Saha A, Chatterjee SK, Foon KA, Bhattacharya-Chatterjee M (2006b) Anti-idiotype antibody induced cellular immunity in mice transgenic for human carcinoembryonic antigen. Immunology 118:483–496. Erratum in: Immunology 119:143. doi:10.1111/j.1365-2567.2006.02391.x

    Google Scholar 

  • Saha A, Chatterjee SK, Foon KA, Celis E, Bhattacharya-Chatterjee M (2007) Therapy of established tumors in a novel murine model transgenic for human carcinoembryonic antigen and HLA-A2 with a combination of anti-idiotype vaccine and CTL peptides of carcinoembryonic antigen. Cancer Res 67:2881–2892. doi:10.1158/0008-5472.CAN-06-3045

    PubMed  CAS  Google Scholar 

  • Sai Y, Nishimura T, Shimpo S, Chishu T, Sato K, Kose N, Terasaki T, Mukai C, Kitagaki S, Miyakoshi N, Kang YS, Nakashima E (2008) Characterization of the mechanism of zidovudine uptake by rat conditionally immortalized syncytiotrophoblast cell line TR-TBT. Pharm Res 25:1647–1653. doi:10.1007/s11095-008-9564-9 DOI:dx.doi.org

    PubMed  CAS  Google Scholar 

  • Saïdi H, Magri G, Nasreddine N, Réquena M, Bélec L (2007) R5- and X4-HIV-1 use differentially the endometrial epithelial cells HEC-1A to ensure their own spread: implication for mechanisms of sexual transmission. Virology 358:55–68. doi:10.1016/j.virol.2006.07.029

    PubMed  Google Scholar 

  • Saïdi H, Magri G, Carbonneil C, Bouhlal H, Hocini H, Belec L (2009) Apical interactions of HIV type 1 with polarized HEC-1 cell monolayer modulate R5-HIV type 1 spread by submucosal macrophages. AIDS Res Hum Retroviruses 25:497–509

    PubMed  Google Scholar 

  • Saïdi H, Carbonneil C, Magri G, Eslahpazir J, Sekaly RP, Bélec L (2010) Differential modulation of CCR5-tropic human immunodeficiency virus-1 transfer from macrophages towards T cells under interleukin-4/interleukin-13 microenvironment. Hum Immunol 71:1–13. doi:10.1016/j.humimm.2009.08.011

    PubMed  Google Scholar 

  • Sajjan U, Wang Q, Zhao Y, Gruenert DC, Hershenson MB (2008) Rhinovirus disrupts the barrier function of polarized airway epithelial cells. Am J Respir Crit Care Med 178:1271–1281. doi:10.1164/rccm.200801-136OC

    PubMed  CAS  Google Scholar 

  • Sato K, Sai Y, Nishimura T, Chishu T, Shimpo S, Kose N, Nakashima E (2009) Influx mechanism of 2′,3′- dideoxyinosine and uridine at the blood–placenta barrier. Placenta 30:263–269

    PubMed  CAS  Google Scholar 

  • Saunders M (2009) Transplacental transport of nanomaterials. Wiley Interdiscip Rev Nanomed Nanobiotechnol 1:671–684, Review. 10.1002/wnan.053

    PubMed  CAS  Google Scholar 

  • Sawicki G, Radomski MW, Winkler-Lowen B, Krzymien A, Guilbert LJ (2000) Polarized release of matrix metalloproteinase-2 and -9 from cultured human placental syncytiotrophoblasts. Biol Reprod 63:1390–1395

    PubMed  CAS  Google Scholar 

  • Shen R, Drelichman ER, Bimczok D, Ochsenbauer C, Kappes JC, Cannon JA, Tudor D, Bomsel M, Smythies LE, Smith PD (2010) GP41-specific antibody blocks cell-free HIV type 1 transcytosis through human rectal mucosa and model colonic epithelium. J Immunol 184:3648–3655. doi:10.4049/jimmunol.0903346

    PubMed  CAS  Google Scholar 

  • St-Pierre MV, Serrano MA, Macias RI, Dubs U, Hoechli M, Lauper U, Meier PJ, Marin JJ (2000) Expression of members of the multidrug resistance protein family in human term placenta. Am J Physiol Regul Integr Comp Physiol 279:R1495–R1503

    PubMed  CAS  Google Scholar 

  • Strothmeyer AM, Papaioannou D, Duhren-von Minden M, Navarrete M, Zirlik K, Heining-Mikesch K, Veelken H (2010) Comparative analysis of predicted HLA binding of immunoglobulin idiotype sequences indicates T-cell-mediated immunosurveillance in follicular lymphoma. Blood 116:1734–1736. doi:10.1182/blood-2010-02-270199

    PubMed  CAS  Google Scholar 

  • Sverdlov M, Shajahan AN, Minshall RD (2007) Tyrosine phosphorylation-dependence of caveolae-mediated endocytosis. J Cell Mol Med 11:1239–1250. doi:10.1111/j.1582-4934.2007.00127.x DOI:dx.doi.org

    PubMed  CAS  Google Scholar 

  • Tamura M, Kuwano K, Kurane I, Ennis FA (1998) Definition of amino acid residues on the epitope responsible for recognition by influenza a virus H1-specific, H2-specific, and H1- and H2-crossreactive murine cytotoxic T-lymphocyte clones. J Virol 72:9404–9406

    PubMed  CAS  Google Scholar 

  • Tomi M, Nishimura T, Nakashima E (2011) Mother-to-fetus transfer of antiviral drugs and the involvement of transporters at the placental barrier. J Pharm Sci 100(9):3708–3718. doi:10.1002/jps.22642

    PubMed  CAS  Google Scholar 

  • Toye AM, Banting G, Tanner MJ (2004) Regions of human kidney anion exchanger 1 (kAE1) required for basolateral targeting of kAE1 in polarised kidney cells: mis-targeting explains dominant renal tubular acidosis (dRTA). J Cell Sci 117(Pt 8):1399–1410. doi:10.1242/jcs.00974

    PubMed  CAS  Google Scholar 

  • Trinh QD, Izumi Y, Komine-Aizawa S, Shibata T, Shimotai Y, Kuroda Y, Mizuguchi M, Ushijima Y, Mor G, Hayakawa S (2009) H3N2 influenza a virus replicates in immortalized human first trimester trophoblast cell lines and induces their rapid apoptosis. Am J Reprod Immunol 62:139–146. doi:10.1111/j.1600-0897.2009.00723.x

    PubMed  CAS  Google Scholar 

  • Tzioufas AG, Routsias JG (2010) Idiotype, anti-idiotype network of autoantibodies: pathogenetic considerations and clinical application. Autoimmun Rev 9:631–633. doi:10.1016/j.autrev.2010.05.013

    PubMed  CAS  Google Scholar 

  • van Houwelingen AH, Weathington NM, Verweij V, Blalock JE, Nijkamp FP, Folkerts G (2008) Induction of lung emphysema is prevented by L-arginine-threonine-arginine. FASEB J 22:3403–3408. doi:10.1096/fj.07-096230

    PubMed  Google Scholar 

  • Vidricaire G, Tremblay MJ (2007) A clathrin, caveolae, and dynamin-independent endocytic pathway requiring free membrane cholesterol drives HIV-1 internalization and infection in polarized trophoblastic cells. J Mol Biol 368:1267–1283. doi:10.1016/j.jmb.2007.03.003

    PubMed  CAS  Google Scholar 

  • Vidricaire G, Tardif MR, Tremblay MJ (2003) The low viral production in trophoblastic cells is due to a high endocytic internalization of the human immunodeficiency virus type 1 and can be overcome by the pro-inflammatory cytokines tumor necrosis factor-alpha and interleukin-1. J Biol Chem 278:15832–15841. doi:10.1074/jbc.M210470200

    PubMed  CAS  Google Scholar 

  • Vidricaire G, Imbeault M, Tremblay MJ (2004) Endocytic host cell machinery plays a dominant role in intracellular trafficking of incoming human immunodeficiency virus type 1 in human placental trophoblasts. J Virol 78:11904–11915. doi:10.1128/JVI.78.21.11904-11915.2004

    PubMed  CAS  Google Scholar 

  • Wang MW, Heap RB, Taussig MJ (1989) Blocking of pregnancy in mice by immunization with anti-idiotype directed against monoclonal anti-progesterone antibody. Proc Natl Acad Sci USA 86:7098–7102

    PubMed  CAS  Google Scholar 

  • Wang J, Li Y, Li Y, Li G (2010) In vitro anti-tumor immune mechanism of nasopharyngeal carcinoma bispecific anti-idiotype antibody. Zhong Nan Da Xue Xue Bao Yi Xue Ban 35:777–783

    PubMed  CAS  Google Scholar 

  • Warncke M, Dodero A, Dierbach H, Follo M, Veelken H (2006) Murine dendritic cells generated under serum-free conditions have a mature phenotype and efficiently induce primary immune responses. J Immunol Methods 310(1–2):1–11. doi:10.1016/j.jim.2005.09.012, 20 Mar 2006

  • Warncke M, Buchner M, Thaller G, Dodero A, Bulashevska A, Pfeifer D, Timmer J, Veelken H (2011) Control of the specificity of T cell-mediated anti-idiotype immunity by natural regulatory T cells. Cancer Immunol Immunother 60:49–60. doi:10.1007/s00262-010-0918-x

    PubMed  CAS  Google Scholar 

  • Warrington RJ, Wong SK, Ramdahin S, Rutherford WJ (1995) Normal human cord blood B cells can produce high affinity IgG antibodies to dsDNA that are recognized by cord blood-derived anti-idiotypic antibodies. Scand J Immunol 42:397–406

    PubMed  CAS  Google Scholar 

  • Weathington NM, Blalock JE (2003) Rational design of peptide vaccines for autoimmune disease: harnessing molecular recognition to fix a broken network. Expert Rev Vaccines 2:61–73

    PubMed  CAS  Google Scholar 

  • Weng WK, Czerwinski D, Timmerman J, Hsu FJ, Levy R (2004) Clinical outcome of lymphoma patients after idiotype vaccination is correlated with humoral immune response and immunoglobulin G Fc receptor genotype. J Clin Oncol 22:4717–4724. doi:10.1200/JCO.2004.06.003

    PubMed  CAS  Google Scholar 

  • Wewer C, Seibt A, Wolburg H, Greune L, Schmidt MA, Berger J, Galla HJ, Quitsch U, Schwerk C, Schroten H, Tenenbaum T (2011) Transcellular migration of neutrophil granulocytes through the blood-cerebrospinal fluid barrier after infection with Streptococcus suis. J Neuroinflammation 8:51. http://www.jneuroinflammation.com/content/8/1/51

    Google Scholar 

  • Wick P, Malek A, Manser P, Meili D, Maeder-Althaus X, Diener L, Diener PA, Zisch A, Krug HF, von Mandach U (2010) Barrier capacity of human placenta for nanosized materials. Environ Health Perspect 118:432–436. doi:10.1289/ehp. 0901200

    PubMed  CAS  Google Scholar 

  • Xiao P, Zhao J, Patterson LJ, Brocca-Cofano E, Venzon D, Kozlowski PA, Hidajat R, Demberg T, Robert-Guroff M (2010) Multiple vaccine-elicited nonneutralizing antienvelope antibody activities contribute to protective efficacy by reducing both acute and chronic viremia following simian/human immunodeficiency virus SHIV89.6P challenge in rhesus macaques. J Virol 84:7161–7173. doi:10.1128/JVI.00410-10

    PubMed  CAS  Google Scholar 

  • Yamamoto T, Kuniki K, Takekuma Y, Hirano T, Iseki K, Sugawara M (2007) Ribavirin uptake by cultured human choriocarcinoma (BeWo) cells and Xenopus laevis oocytes expressing recombinant plasma membrane human nucleoside transporters. Eur J Pharmacol 557:1–8. doi:10.1016/j.ejphar.2006.10.062

    PubMed  CAS  Google Scholar 

  • Ye L, Liu X, Rout SN, Li Z, Yan Y, Lu L, Kamala T, Nanda NK, Song W, Samal SK, Zhu X (2008) The MHC class II-associated invariant chain interacts with the neonatal Fc gamma receptor and modulates its trafficking to endosomal/lysosomal compartments. J Immunol 181:2572–2585

    PubMed  CAS  Google Scholar 

  • Younes SA, Csire M, Kapusinszky B, Szomor K, Takács M (2009) Berencsi Gy: heterogeneous pathways of maternal-fetal transmission of human viruses (review). Pathol Oncol Res 15:451–465. doi:10.1007/s12253-009-9166-9

    PubMed  Google Scholar 

  • Youngblood B, Oestreich KJ, Ha SJ, Duraiswamy J, Akondy RS, West EE, Wei Z, Lu P, Austin JW, Riley JL, Boss JM, Ahmed R (2011) Chronic virus infection enforces demethylation of the locus that encodes PD-1 in antigen-specific CD8(+) T cells. Immunity 35:400–412. doi:10.1016/j.immuni.2011.06.015

    PubMed  CAS  Google Scholar 

  • Zhu X, Peng J, Chen D, Liu X, Ye L, Iijima H, Kadavil K, Lencer WI, Blumberg RS (2005) Calnexin and ERp57 facilitate the assembly of the neonatal Fc receptor for IgG with beta 2-microglobulin in the endoplasmic reticulum. J Immunol 175:967–976

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to György Berencsi III .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Berencsi, G., Ördög, K. (2012). Polarised Transfer of Proteins Through the Syncytiotrophobalst and Tissue Culture Cell Lines. In: Berencsi III, G. (eds) Maternal Fetal Transmission of Human Viruses and their Influence on Tumorigenesis. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4216-1_7

Download citation

Publish with us

Policies and ethics