A novel mother-to-child human T-cell leukaemia virus type 1 (HTLV-1) transmission model for investigating the role of maternal anti-HTLV-1 antibodies using orally infected mother rats Free

Abstract

Human T-cell leukaemia virus type 1 (HTLV-1) is a human retrovirus that is a causative agent of adult T-cell leukaemia/lymphoma (ATL) and is mainly transmitted from an infected mother to her child via breastfeeding. Such an HTLV-1 infection during childhood is believed to be a risk factor for ATL development. Although it has been suggested that an increased proviral load (PVL), a higher titre of antibody (Ab) in the infected mother and prolonged breastfeeding are associated with an increased risk of mother-to-child transmission (MTCT), the mechanisms underlying MTCT of HTLV-1 remain largely unknown. In this study, we developed an MTCT model using orally HTLV-1-infected rats that have no Ab responses against viral antigens, such as Gag and Env. In this model, HTLV-1 could be transmitted from the infected mother rats to their offspring at a high rate (50–100 %), and the rate of MTCT tended to be correlated with the PVL of the infected mother rats. Furthermore, passive immunization of uninfected adult rats and an infected mother rat with a rat anti-HTLV-1 Env gp46-neutralizing mAb was unable to suppress primary oral HTLV-1 infection to the adult rats and vertical HTLV-1 transmission to the offspring, respectively. Our findings indicate that this MTCT model would be useful to investigate not only the mechanisms of MTCT but also the role of anti-HTLV-1 Ab in MTCT of HTLV-1. They also provide some information on the role of maternal Abs in MTCT, which should be considered when designing a strategy for prevention of MTCT of HTLV-1.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000733
2017-04-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/98/4/835.html?itemId=/content/journal/jgv/10.1099/jgv.0.000733&mimeType=html&fmt=ahah

References

  1. Hinuma Y, Nagata K, Hanaoka M, Nakai M, Matsumoto T et al. Adult T-cell leukemia: antigen in an ATL cell line and detection of antibodies to the antigen in human sera. Proc Natl Acad Sci USA 1981; 78:6476–6480 [View Article][PubMed]
    [Google Scholar]
  2. Poiesz BJ, Ruscetti FW, Gazdar AF, Bunn PA, Minna JD et al. Detection and isolation of type C retrovirus particles from fresh and cultured lymphocytes of a patient with cutaneous T-cell lymphoma. Proc Natl Acad Sci USA 1980; 77:7415–7419 [View Article][PubMed]
    [Google Scholar]
  3. Uchiyama T. Human T cell leukemia virus type I (HTLV-I) and human diseases. Annu Rev Immunol 1997; 15:15–37 [View Article][PubMed]
    [Google Scholar]
  4. de Thé G, Bomford R. An HTLV-I vaccine: why, how, for whom?. AIDS Res Hum Retroviruses 1993; 9:381–386 [View Article][PubMed]
    [Google Scholar]
  5. Ishitsuka K, Tamura K. Human T-cell leukaemia virus type I and adult T-cell leukaemia-lymphoma. Lancet Oncol 2014; 15:e517–e526 [View Article][PubMed]
    [Google Scholar]
  6. Ando Y, Nakano S, Saito K, Shimamoto I, Ichijo M et al. Transmission of adult T-cell leukemia retrovirus (HTLV-I) from mother to child: comparison of bottle- with breast-fed babies. Jpn J Cancer Res 1987; 78:322–324[PubMed]
    [Google Scholar]
  7. Hino S. Establishment of the milk-borne transmission as a key factor for the peculiar endemicity of human T-lymphotropic virus type 1 (HTLV-1): the ATL prevention program Nagasaki. Proc Jpn Acad Ser B Phys Biol Sci 2011; 87:152–166 [View Article][PubMed]
    [Google Scholar]
  8. Hino S, Sugiyama H, Doi H, Ishimaru T, Yamabe T et al. Breaking the cycle of HTLV-I transmission via carrier mothers' milk. Lancet 1987; 2:158–159 [View Article][PubMed]
    [Google Scholar]
  9. Murphy EL, Hanchard B, Figueroa JP, Gibbs WN, Lofters WS et al. Modelling the risk of adult T-cell leukemia/lymphoma in persons infected with human T-lymphotropic virus type I. Int J Cancer 1989; 43:250–253 [View Article][PubMed]
    [Google Scholar]
  10. Iwanaga M, Watanabe T, Utsunomiya A, Okayama A, Uchimaru K et al. Human T-cell leukemia virus type I (HTLV-1) proviral load and disease progression in asymptomatic HTLV-1 carriers: a nationwide prospective study in Japan. Blood 2010; 116:1211–1219 [View Article][PubMed]
    [Google Scholar]
  11. Hasegawa A, Ohashi T, Hanabuchi S, Kato H, Takemura F et al. Expansion of human T-cell leukemia virus type 1 (HTLV-1) reservoir in orally infected rats: inverse correlation with HTLV-1-specific cellular immune response. J Virol 2003; 77:2956–2963 [View Article][PubMed]
    [Google Scholar]
  12. Wiktor SZ, Pate EJ, Rosenberg PS, Barnett M, Palmer P et al. Mother-to-child transmission of human T-cell lymphotropic virus type I associated with prolonged breast-feeding. J Hum Virol 1997; 1:37–44[PubMed]
    [Google Scholar]
  13. Sugiyama H, Doi H, Yamaguchi K, Tsuji Y, Miyamoto T et al. Significance of postnatal mother-to-child transmission of human T-lymphotropic virus type-I on the development of adult T-cell leukemia/lymphoma. J Med Virol 1986; 20:253–260 [View Article][PubMed]
    [Google Scholar]
  14. Ureta-Vidal A, Angelin-Duclos C, Tortevoye P, Murphy E, Lepère JF et al. Mother-to-child transmission of human T-cell-leukemia/lymphoma virus type I: implication of high antiviral antibody titer and high proviral load in carrier mothers. Int J Cancer 1999; 82:832–836 [View Article][PubMed]
    [Google Scholar]
  15. Hino S, Doi H, Yoshikuni H, Sugiyama H, Ishimaru T et al. HTLV-I carrier mothers with high-titer antibody are at high risk as a source of infection. Jpn J Cancer Res 1987; 78:1156–1158[PubMed]
    [Google Scholar]
  16. Ami Y, Kushida S, Matsumura M, Yoshida Y, Kameyama T et al. Vertical transmission of HTLV-1 in HTLV-1 carrier rat. Jpn J Cancer Res 1992; 83:1241–1243 [View Article][PubMed]
    [Google Scholar]
  17. Iwahara Y, Takehara N, Kataoka R, Sawada T, Ohtsuki Y et al. Transmission of HTLV-I to rabbits via semen and breast milk from seropositive healthy persons. Int J Cancer 1990; 45:980–983 [View Article][PubMed]
    [Google Scholar]
  18. Yamanouchi K, Kinoshita K, Moriuchi R, Katamine S, Amagasaki T et al. Oral transmission of human T-cell leukemia virus type-I into a common marmoset (Callithrix jacchus) as an experimental model for milk-borne transmission. Jpn J Cancer Res 1985; 76:481–487[PubMed]
    [Google Scholar]
  19. Hori M, Ami Y, Kushida S, Kobayashi M, Uchida K et al. Intrauterine transmission of human T-cell leukemia virus type I in rats. J Virol 1995; 69:1302–1305[PubMed]
    [Google Scholar]
  20. Igakura T, Stinchcombe JC, Goon PK, Taylor GP, Weber JN et al. Spread of HTLV-I between lymphocytes by virus-induced polarization of the cytoskeleton. Science 2003; 299:1713–1716 [View Article][PubMed]
    [Google Scholar]
  21. Jones KS, Lambert S, Bouttier M, Bénit L, Ruscetti FW et al. Molecular aspects of HTLV-1 entry: functional domains of the HTLV-1 surface subunit (SU) and their relationships to the entry receptors. Viruses 2011; 3:794–810 [View Article][PubMed]
    [Google Scholar]
  22. Tanaka Y, Zeng L, Shiraki H, Shida H, Tozawa H. Identification of a neutralization epitope on the envelope gp46 antigen of human T cell leukemia virus type I and induction of neutralizing antibody by peptide immunization. J Immunol 1991; 147:354–360[PubMed]
    [Google Scholar]
  23. Tanaka Y, Takahashi Y, Tanaka R, Kodama A, Fujii H et al. Elimination of human T cell leukemia virus type-1-infected cells by neutralizing and antibody-dependent cellular cytotoxicity-inducing antibodies against human t cell leukemia virus type-1 envelope gp46. AIDS Res Hum Retroviruses 2014; 30:542–552 [View Article][PubMed]
    [Google Scholar]
  24. Fujii H, Shimizu M, Miyagi T, Kunihiro M, Tanaka R et al. A potential of an anti-HTLV-I gp46 neutralizing monoclonal antibody (LAT-27) for passive immunization against both horizontal and Mother-to-Child vertical infection with human T cell leukemia virus Type-I. Viruses 2016; 8:41 [View Article][PubMed]
    [Google Scholar]
  25. Kato H, Koya Y, Ohashi T, Hanabuchi S, Takemura F et al. Oral administration of human T-cell leukemia virus type 1 induces immune unresponsiveness with persistent infection in adult rats. J Virol 1998; 72:7289–7293[PubMed]
    [Google Scholar]
  26. Gessain A, Cassar O. Epidemiological aspects and world distribution of HTLV-1 infection. Front Microbiol 2012; 3:388 [View Article][PubMed]
    [Google Scholar]
  27. Paré ME, Gauthier S, Landry S, Sun J, Legault E et al. A new sensitive and quantitative HTLV-I-mediated cell fusion assay in T cells. Virology 2005; 338:309–322 [View Article][PubMed]
    [Google Scholar]
  28. Hino S, Yamaguchi K, Katamine S, Sugiyama H, Amagasaki T et al. Mother-to-child transmission of human T-cell leukemia virus type-I. Jpn J Cancer Res 1985; 76:474–480[PubMed]
    [Google Scholar]
  29. Kinoshita K, Amagasaki T, Hino S, Doi H, Yamanouchi K et al. Milk-borne transmission of HTLV-I from carrier mothers to their children. Jpn J Cancer Res 1987; 78:674–680[PubMed]
    [Google Scholar]
  30. Matsubara F, Haraguchi K, Harada K, Koizumi A. Screening for antibodies to human T-cell leukemia virus type I in Japanese breast milk. Biol Pharm Bull 2012; 35:773–776 [View Article][PubMed]
    [Google Scholar]
  31. Uemura Y, Kotani S, Yoshimoto S, Fujishita M, Yamashita M et al. Mother-to-offspring transmission of human T cell leukemia virus type I in rabbits. Blood 1987; 69:1255–1258[PubMed]
    [Google Scholar]
  32. Maloney EM, Yamano Y, Vanveldhuisen PC, Sawada T, Kim N et al. Natural history of viral markers in children infected with human T lymphotropic virus type I in Jamaica. J Infect Dis 2006; 194:552–560 [View Article][PubMed]
    [Google Scholar]
  33. Kataoka R, Takehara N, Iwahara Y, Sawada T, Ohtsuki Y et al. Transmission of HTLV-I by blood transfusion and its prevention by passive immunization in rabbits. Blood 1990; 76:1657–1661[PubMed]
    [Google Scholar]
  34. Maidji E, Mcdonagh S, Genbacev O, Tabata T, Pereira L. Maternal antibodies enhance or prevent Cytomegalovirus infection in the placenta by neonatal Fc receptor-mediated transcytosis. Am J Pathol 2006; 168:1210–1226 [View Article][PubMed]
    [Google Scholar]
  35. Gupta S, Gach JS, Becerra JC, Phan TB, Pudney J et al. The neonatal Fc receptor (FcRn) enhances human immunodeficiency virus type 1 (HIV-1) transcytosis across epithelial cells. PLoS Pathog 2013; 9:e1003776 [View Article][PubMed]
    [Google Scholar]
  36. Ohsugi T, Urano T, Masunaga K, Shingu M. HTLV-I infections in offspring derived from HTLV-I carrier rats during the suckling period. Kurume Med J 1996; 43:1–9 [View Article][PubMed]
    [Google Scholar]
  37. Kinoshita K, Hino S, Amagaski T, Ikeda S, Yamada Y et al. Demonstration of adult T-cell leukemia virus antigen in milk from three sero-positive mothers. Gan 1984; 75:103–105[PubMed]
    [Google Scholar]
  38. Kinoshita K, Yamanouchi K, Ikeda S, Momita S, Amagasaki T et al. Oral infection of a common marmoset with human T-cell leukemia virus type-I (HTLV-I) by inoculating fresh human milk of HTLV-I carrier mothers. Jpn J Cancer Res 1985; 76:1147–1153[PubMed]
    [Google Scholar]
  39. Percher F, Jeannin P, Martin-Latil S, Gessain A, Afonso PV et al. Mother-to-child transmission of HTLV-1 epidemiological aspects, mechanisms and determinants of mother-to-child transmission. Viruses 2016; 8:40 [View Article][PubMed]
    [Google Scholar]
  40. Zacharopoulos VR, Perotti ME, Phillips DM. Lymphocyte-facilitated infection of epithelia by human T-cell lymphotropic virus type I. J Virol 1992; 66:4601–4605[PubMed]
    [Google Scholar]
  41. Martin-Latil S, Gnädig NF, Mallet A, Desdouits M, Guivel-Benhassine F et al. Transcytosis of HTLV-1 across a tight human epithelial barrier and infection of subepithelial dendritic cells. Blood 2012; 120:572–580 [View Article][PubMed]
    [Google Scholar]
  42. Hino S, Katamine S, Kawase K, Miyamoto T, Doi H et al. Intervention of maternal transmission of HTLV-1 in Nagasaki, Japan. Leukemia 1994; 8:S68–S70[PubMed]
    [Google Scholar]
  43. Proietti FA, Carneiro-Proietti AB, Catalan-Soares BC, Murphy EL. Global epidemiology of HTLV-I infection and associated diseases. Oncogene 2005; 24:6058–6068 [View Article][PubMed]
    [Google Scholar]
  44. Ando Y, Kakimoto K, Tanigawa T, Furuki K, Saito K et al. Effect of freeze-thawing breast milk on vertical HTLV-I transmission from seropositive mothers to children. Jpn J Cancer Res 1989; 80:405–407 [View Article][PubMed]
    [Google Scholar]
  45. Kannagi M, Harada S, Maruyama I, Inoko H, Igarashi H et al. Predominant recognition of human T cell leukemia virus type I (HTLV-I) pX gene products by human CD8+ cytotoxic T cells directed against HTLV-I-infected cells. Int Immunol 1991; 3:761–767 [View Article][PubMed]
    [Google Scholar]
  46. Tanaka Y, Mizuguchi M, Takahashi Y, Fujii H, Tanaka R et al. Human T-cell leukemia virus type-I tax induces the expression of CD83 on T cells. Retrovirology 2015; 12:56 [View Article][PubMed]
    [Google Scholar]
  47. Fujisawa J, Toita M, Yoshimura T, Yoshida M. The indirect association of human T-cell leukemia virus tax protein with DNA results in transcriptional activation. J Virol 1991; 65:4525–4528[PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000733
Loading
/content/journal/jgv/10.1099/jgv.0.000733
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most cited Most Cited RSS feed