Placenta
Volume 28, Issue 5 , Pages 527-537 , May 2007

Cytotrophoblasts Infected with a Pathogenic Human Cytomegalovirus Strain Dysregulate Cell–Matrix and Cell–Cell Adhesion Molecules: A Quantitative Analysis

  • T. Tabata

      Affiliations

    • Department of Cell and Tissue Biology, University of California, San Francisco, 513 Parnassus Avenue, San Francisco, CA 94143-0512, USA
  • ,
  • S. McDonagh

      Affiliations

    • Department of Cell and Tissue Biology, University of California, San Francisco, 513 Parnassus Avenue, San Francisco, CA 94143-0512, USA
  • ,
  • H. Kawakatsu

      Affiliations

    • Lung Biology Center, Box 2922, San Francisco, CA 94143-2922, USA
  • ,
  • L. Pereira

      Affiliations

    • Department of Cell and Tissue Biology, University of California, San Francisco, 513 Parnassus Avenue, San Francisco, CA 94143-0512, USA
    • Corresponding Author InformationCorresponding author. Tel.: +1 415 476 8248; fax: +1 415 502 7338.

,Accepted 16 May 2006.

References 

  1. McMaster MT, Librach CL, Zhou Y, Lim KH, Janatpour MJ, DeMars R, et al. Human placental HLA-G expression is restricted to differentiated cytotrophoblasts. J Immunol. 1995;154:3771–3778
  2. Damsky CH, Librach C, Lim KH, Fitzgerald ML, McMaster MT, Janatpour M, et al. Integrin switching regulates normal trophoblast invasion. Development. 1994;120:3657–3666
  3. Damsky CH, Fisher SJ. Trophoblast pseudo-vasculogenesis: faking it with endothelial adhesion receptors. Curr Opin Cell Biol. 1998;10:660–666
  4. Zhou Y, Fisher SJ, Janatpour M, Genbacev O, Dejana E, Wheelock M, et al. Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion?. J Clin Invest. 1997;99:2139–2151
  5. Britt WJ. Congenital cytomegalovirus infection. In:  Hitchcock PJ,  MacKay HT,  Wasserheit JN editor. Sexually transmitted diseases and adverse outcomes of pregnancy. Washington, D.C.: ASM Press; 1999;p. 269–281
  6. Demmler GJ. Congenital cytomegalovirus infection and disease. Adv Pediatr Infect Dis. 1996;11:135–162
  7. Fisher S, Genbacev O, Maidji E, Pereira L. Human cytomegalovirus infection of placental cytotrophoblasts in vitro and in utero: implications for transmission and pathogenesis. J Virol. 2000;74:6808–6820
  8. Pereira L, Maidji E, McDonagh S, Genbacev O, Fisher S. Human cytomegalovirus transmission from the uterus to the placenta correlates with the presence of pathogenic bacteria and maternal immunity. J Virol. 2003;77:13301–13314
  9. Maidji E, McDonagh S, Genbacev O, Tabata T, Pereira L. Maternal antibodies enhance or prevent cytomegalovirus infection in the human placenta by neonatal Fc receptor-mediated transport. Am J Pathol. 2006;168:1210–1226
  10. McDonagh S, Maidji E, Chang H-T, Pereira L. Patterns of human cytomegalovirus infection in term placentas: a preliminary analysis. J Clin Virol. 2006;35:210–215
  11. Yamamoto-Tabata T, McDonagh S, Chang H-T, Fisher S, Pereira L. Human cytomegalovirus interleukin-10 downregulates matrix metalloproteinase activity and impairs endothelial cell migration and placental cytotrophoblast invasiveness in vitro. J Virol. 2004;78:2831–2840
  12. McDonagh S, Maidji E, Ma W, Chang HT, Fisher S, Pereira L. Viral and bacterial pathogens at the maternal–fetal interface. J Infect Dis. 2004;190:826–834
  13. Librach CL, Werb Z, Fitzgerald ML, Chiu K, Corwin NM, Esteves RA, et al. 92-kD type IV collagenase mediates invasion of human cytotrophoblasts. J Cell Biol. 1991;113:437–449
  14. Genbacev O, Schubach SA, Miller RK. Villous culture of first trimester human placenta – model to study extravillous trophoblast (EVT) differentiation. Placenta. 1992;13:439–461
  15. Damsky CH, Fitzgerald ML, Fisher SJ. Distribution patterns of extracellular matrix components and adhesion receptors are intricately modulated during first trimester cytotrophoblast differentiation along the invasive pathway, in vivo. J Clin Invest. 1992;89:210–222
  16. Hahn G, Revello MG, Patrone M, Percivalle E, Campanini G, Sarasini A, et al. Human cytomegalovirus UL131–128 genes are indispensable for virus growth in endothelial cells and virus transfer to leukocytes. J Virol. 2004;78:10023–10033
  17. Maidji E, Percivalle E, Gerna G, Fisher S, Pereira L. Transmission of human cytomegalovirus from infected uterine microvascular endothelial cells to differentiating/invasive placental cytotrophoblasts. Virology. 2002;304:53–69
  18. Dittel BN, McCarthy JB, Wayner EA, LeBien TW. Regulation of human B-cell precursor adhesion to bone marrow stromal cells by cytokines that exert opposing effects on the expression of vascular cell adhesion molecule-1 (VCAM-1). Blood. 1993;81:2272–2282
  19. Byzova TV, Goldman CK, Pampori N, Thomas KA, Bett A, Shattil SJ, et al. A mechanism for modulation of cellular responses to VEGF: activation of the integrins. Mol Cell. 2000;6:851–860
  20. Weinacker A, Chen A, Agrez M, Cone RI, Nishimura S, Wayner E, et al. Role of the integrin alpha v beta 6 in cell attachment to fibronectin. Heterologous expression of intact and secreted forms of the receptor. J Biol Chem. 1994;269:6940–6948
  21. Weinreb PH, Simon KJ, Rayhorn P, Yang WJ, Leone DR, Dolinski BM, et al. Function-blocking integrin alphavbeta6 monoclonal antibodies: distinct ligand-mimetic and nonligand-mimetic classes. J Biol Chem. 2004;279:17875–17887
  22. Mu D, Cambier S, Fjellbirkeland L, Baron JL, Munger JS, Kawakatsu H, et al. The integrin alpha(v)beta8 mediates epithelial homeostasis through MT1-MMP-dependent activation of TGF-beta1. J Cell Biol. 2002;157:493–507
  23. Dondero DV, Pereira L. Monoclonal antibody production. In:  Emmons R,  Schmidt N editor. Diagnostic procedures for viral, rickettsial and chlamydial infections. Washington, D.C.: American Public Health Association; 1990;p. 101–124
  24. Qadri I, Navarro D, Paz P, Pereira L. Assembly of conformation-dependent neutralizing domains on human cytomegalovirus glycoprotein B. J Gen Virol. 1992;73:2913–2921
  25. Taooka Y, Chen J, Yednock T, Sheppard D. The integrin alpha9beta1 mediates adhesion to activated endothelial cells and transendothelial neutrophil migration through interaction with vascular cell adhesion molecule-1. J Cell Biol. 1999;145:413–420
  26. Yokosaki Y, Palmer EL, Prieto AL, Crossin KL, Bourdon MA, Pytela R, et al. The integrin alpha 9 beta 1 mediates cell attachment to a non-RGD site in the third fibronectin type III repeat of tenascin. J Biol Chem. 1994;269:26691–26696
  27. Munger JS, Huang X, Kawakatsu H, Griffiths MJ, Dalton SL, Wu J, et al. The integrin alpha v beta 6 binds and activates latent TGF beta 1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell. 1999;96:319–328
  28. Abe M, Harpel JG, Metz CN, Nunes I, Loskutoff DJ, Rifkin DB. An assay for transforming growth factor-beta using cells transfected with a plasminogen activator inhibitor-1 promoter–luciferase construct. Anal Biochem. 1994;216:276–284
  29. Feire AL, Koss H, Compton T. Cellular integrins function as entry receptors for human cytomegalovirus via a highly conserved disintegrin-like domain. Proc Natl Acad Sci U S A. 2004;101:15470–15475
  30. Wang X, Huong SM, Chiu ML, Raab-Traub N, Huang ES. Epidermal growth factor receptor is a cellular receptor for human cytomegalovirus. Nature. 2003;424:456–461
  31. Wang X, Huang DY, Huong SM, Huang ES. Integrin alphavbeta3 is a coreceptor for human cytomegalovirus. Nat Med. 2005;11:515–521
  32. Pittet JF, Griffiths MJ, Geiser T, Kaminski N, Dalton SL, Huang X, et al. TGF-beta is a critical mediator of acute lung injury. J Clin Invest. 2001;107:1537–1544
  33. Pereira L, Maidji E, McDonagh S, Tabata T. Insights into viral transmission at the uterine–placental interface. Trends Microbiol. 2005;13:164–174
  34. Hemmings DG, Kilani R, Nykiforuk C, Preiksaitis J, Guilbert LJ. Permissive cytomegalovirus infection of primary villous term and first trimester trophoblasts. J Virol. 1998;72:4970–4979
  35. Halwachs-Baumann G, Wilders-Truschnig M, Desoye G, Hahn T, Kiesel L, Klingel K, et al. Human trophoblast cells are permissive to the complete replicative cycle of human cytomegalovirus. J Virol. 1998;72:7598–7602
  36. Takahashi H, Isobe T, Horibe S, Takagi J, Yokosaki Y, Sheppard D, et al. Tissue transglutaminase, coagulation factor XIII, and the pro-polypeptide of von Willebrand factor are all ligands for the integrins alpha 9beta 1 and alpha 4beta 1. J Biol Chem. 2000;275:23589–23595
  37. Williams DA, Rios M, Stephens C, Patel VP. Fibronectin and VLA-4 in haematopoietic stem cell–microenvironment interactions. Nature. 1991;352:438–441
  38. Smith LL, Cheung HK, Ling LE, Chen J, Sheppard D, Pytela R, et al. Osteopontin N-terminal domain contains a cryptic adhesive sequence recognized by alpha9beta1 integrin. J Biol Chem. 1996;271:28485–28491
  39. Yokosaki Y, Matsuura N, Higashiyama S, Murakami I, Obara M, Yamakido M, et al. Identification of the ligand binding site for the integrin alpha9 beta1 in the third fibronectin type III repeat of tenascin-C. J Biol Chem. 1998;273:11423–11428
  40. Vlahakis NE, Young BA, Atakilit A, Sheppard D. The lymphangiogenic vascular endothelial growth factors VEGF-C and -D are ligands for the integrin alpha9beta1. J Biol Chem. 2005;280:4544–4552
  41. Makinen T, Veikkola T, Mustjoki S, Karpanen T, Catimel B, Nice EC, et al. Isolated lymphatic endothelial cells transduce growth, survival and migratory signals via the VEGF-C/D receptor VEGFR-3. EMBO J. 2001;20:4762–4773
  42. Oh SJ, Jeltsch MM, Birkenhager R, McCarthy JE, Weich HA, Christ B, et al. VEGF and VEGF-C: specific induction of angiogenesis and lymphangiogenesis in the differentiated avian chorioallantoic membrane. Dev Biol. 1997;188:96–109
  43. Munger JS, Harpel JG, Giancotti FG, Rifkin DB. Interactions between growth factors and integrins: latent forms of transforming growth factor-beta are ligands for the integrin alphavbeta1. Mol Biol Cell. 1998;9:2627–2638
  44. Ludbrook SB, Barry ST, Delves CJ, Horgan CM. The integrin alphavbeta3 is a receptor for the latency-associated peptides of transforming growth factors beta1 and beta3. Biochem J. 2003;369:311–318
  45. Breuss JM, Gillett N, Lu L, Sheppard D, Pytela R. Restricted distribution of integrin beta 6 mRNA in primate epithelial tissues. J Histochem Cytochem. 1993;41:1521–1527
  46. Breuss JM, Gallo J, DeLisser HM, Klimanskaya IV, Folkesson HG, Pittet JF, et al. Expression of the beta 6 integrin subunit in development, neoplasia and tissue repair suggests a role in epithelial remodeling. J Cell Sci. 1995;108(Pt 6):2241–2251
  47. Moyle M, Napier MA, McLean JW. Cloning and expression of a divergent integrin subunit beta 8. J Biol Chem. 1991;266:19650–19658
  48. Zhu J, Motejlek K, Wang D, Zang K, Schmidt A, Reichardt LF. Beta8 integrins are required for vascular morphogenesis in mouse embryos. Development. 2002;129:2891–2903
  49. Revello MG, Gerna G. Pathogenesis and prenatal diagnosis of human cytomegalovirus infection. J Clin Virol. 2004;29:71–83
  50. Nigro G, Adler SP, La Torre R, Best AM. Passive immunization during pregnancy for congenital cytomegalovirus infection. N Engl J Med. 2005;353:1350–1362
  51. Hoang VM, Foulk R, Clauser K, Burlingame A, Gibson BW, Fisher SJ. Functional proteomics: examining the effects of hypoxia on the cytotrophoblast protein repertoire. Biochemistry. 2001;40:4077–4086

PII: S0143-4004(06)00127-5

doi: 10.1016/j.placenta.2006.05.006

Placenta
Volume 28, Issue 5 , Pages 527-537 , May 2007