HIV-1 infection in early human placenta in vitro: Effects of Tumor Necrosis Factor (TNF-α) and Interleukins IL-1 and IL-6
Keywords:
HIV-l, virus infection, trophoblast, in situ PCR, human placentaAbstract
The placenta plays a pivotal role in the pathogenesis for the vertical transmission of HIV-1 during pregnancy. To understand HIV-1 infection during the first trimester of pregnancy and its association with inflammatory cytokines, we developed an in vitro HIV infection model using the early human placental explant cultures (5.5-7.5 wks). Ba-L, a laboratory-adapted, chemokine receptor CCR5-using strain of HIV-l, was used to infect the explants. DNA-PCR and Southern blot results show that HIV-l is able to infect the early human placenta in a viral load-dependent manner. In situ PCR demonstrated that the majority of HIV-l-infected cells are cytotrophoblast, Hofbauer cells, and with few syncytiotrophoblast. Viral protein p24 and reverse transcriptase (RT) levels return to control levels after 24h viral exposure, indicating a latent HIV-infection in placental explant culture, though the placenta remained positive by in situ PCR. Viral protein p24 and RT increase by approximately three-fold in the culture supernatants when exogenous cytokines tumor necrosis factor-alpha (TNF-α) alone or in combination with interleukin-1-beta (IL-1β) and IL-6 were added to these virus-exposed explants. Taken together, these data support the hypothesis that the early human placenta is susceptible to HIV-l and latent vs. active HIV-l infection in human placenta may be an important factor in determining whether the baby becomes infected.
[N A J Med Sci. 2016;9(4):151-160. DOI: 10.7156/najms.2016.0904151]
Key Words: HIV-l, virus infection, trophoblast, in situ PCR, human placenta
References
1. Luzuriaga K, MofensonLM. Challenges in the Elimination of Pediatric HIV-1 Infection. NEngl JMed. 2016;374:761-770.
2. Scarlatti G. Paediatric HIV infection. Lancet. 1996;348:863-868.
3. Ryder RW, Nsa W, Hassig SE,et al. Peinatal transmission of the human immunodeficiency virus type I to infants of seropositive women in Zaire. N Engl J Med. 1989; 320:1637-1642.
4. Papp E, Mohammadi H, LoutfyMR, et al. HIV protease inhibitor use during pregnancy is associated with decreased progesterone levels, suggesting a potential mechanism contributing to fetal growth restriction. J Infect Dis. 2015;211:10-18.
5. Boyer PJ, Dillon M, Navaie M, et al. Factors predictive of maternal-fetal transmission of HIV-1. Preliminary analysis of zidovudine given during pregnancy and/or delivery. JAMA. 1994;271:1925-1930.
6. Dunn DT, Newell ML, Ades AE, Peckham CS. Risk of human immunodeficiency virus type 1 transmission through breastfeeding. Lancet. 1992;340:585-588.
7. Bertolli J, St Louis ME, Simonds Ri, et al. Estimating the timing of mother-to-child transmission of human immunodeficiency virus in a breast-feeding population in Kinshasa, Zaire. J Infect Dis. 1996;174:722-726.
8. Bryson YJ, Luzuriaga K, Sullivan JL, Wara DW. Proposed definitions for in utero versus intrapartum transmission of HIV-1. N Engl J Med. 1992;327:1246-1247.
9. Lapointe N, Michaud J, Pekovic D, Chausseau JP, Dupuy JM. Transplacental transmission of HTL-VIII virus. N Engl J Med. 1985;312:1325-1326.
10. Lewis SH, Reynolds-Kohler C, Fox HE, Nelson JA. HIV-1 in trophoblast and villous Hofbauer cells, and haematological precursors in eight-week fetuses. Lancet. 1990;335:565-568.
11. Scott GB, Fischl, MA, Klimas N. Mothers of infants with acquired immunodeficiency syndrome. JAMA. 1985;253:363-366.
12. Backe E, Jimenez E, Unger M, et al. Vertical human immunodeficiency virus transmission: a study of placental pathology in relation to maternal risk factors. Am J Perinatol. 1994;11:326-330.
13. Chandwani S, Greco MA, Mittal K, Antoine C, Krasinski K, Borkowsky W. Pathology and human immunodeficiency virus expression in placenta of seropositive women. J Infect Dis. 1991;163:1134-1138.
14. Mauiy W, Potts Bi, Rabson AB. HIV-l infection of first-trimester and term human placental tissue: a possible mode of maternal-fetal transmission. J Infect Dis. 1989;160:583-588.
15. Bagasra O, Hauptman SP, Lischner HW, Sachs M, Pomerantz Ri. Detection of human immunodeficiency virus type 1 provirus in mononuclear cells by in situ polymerase chain reaction. N Engl J Med. 1992;326:1385-1391.
16. Nuovo GJ, Forde A, MacConnell P, Fahrenwald R. In situ detection of PCR-amplified HIV-1 nucleic acids and tumor necrosis factor cDNA in cervical tissues. Am J Pathol, 1993;143:40-48.
17. Brunstein J. In situ PCR: MDx meets histology. MLO Med Lab Obs. 2015;47:48-50.
18. Zevailos EA, Anderson VM, Bard E, Gu, J. Detection of HIV-1 sequences in placenta of HIV-infected mothers by n situ PCR. Cell Vision. 1994;1:116-121.
19. Sheikh AU, Polliotti, BM, Miller RK. In situ PCR discriminates between infected and uninfected human placental explants after in vitro exposure to HIV-l. Trophohiast Research. 1998;12:191-204.
20. Johnson EL, Chu H, Byrareddy SN, Spearman P, Chakraborty R. Placental Hofbauer cells assemble and sequester HIV-1 in tetraspanin-positive compartments that are accessible to broadly neutralizing antibodies. J Int AIDS Soc. 2015;18:19385.
21. Johnson EL, R Chakraborty. Placental Hofbauer cells limit HIV-1 replication and potentially offset mother to child transmission (MTCT) by induction of immunoregulatory cytokines. Retrovirology. 2012;9:101.
22. Al-Husaini AM. Role of placenta in the vertical transmission of human immunodeficiency virus. J Perinatol. 2009;29:331-336.
23. Mattern CF, Munay K, Jensen A, Farzadegan H, Pang J, Modlin IF. Localization of human immunodeficiency virus core antigen in term human placenta. Pediatrics. 1992;89:207-209.
24. David FJ, Autran B, Tran HC, et al. Human trophoblast cells express CD4 and are permissive for productive infection with HIV-1. Clin Exp Immunol. 1992;88:1016.
25. Dorsamy V, Vallen C. The role of trophoblast cell receptor expression in HIV-1 passage across the placenta in pre-eclampsia: an observational study. BJOG. 2016;10:1471-1528.
26. Toth FD, Mosborg-Petersen P, Kiss J, et al. Antibody-dependent enhancement of HIV-l infectionin human term syncytiotrophoblast
cells cultured in vitro. Clin Exp Immunol. 1994;96:389-394.
27. Zachar V, Norskov-Lauitsen N, Juhi C, Spire B, Chermann JC, Ebbesen P. Susceptibility of cultured human trophoblasts to infection with human immunodeficiency virus type 1. J Gen Virol. 1991;72:1253-1260.
28. Chisanga C, Eggert D, Mitchell CD, Wood C, Angeletti PC. Evidence for Placental HPV Infection in Both HIV Positive and Negative Women. J Cancer Ther. 2015;6:1276-1289.
29. Douglas GC, Fry GN, Thirkill T. Cell-mediated infection of human placental trophoblast with HIV in vitro. AIDS Res Hum Retroviruses. 1991;7:735-740.
30. McGann KA, Collman R, Kolson DL, et al. Human immunodeficiency virus type 1 causes productive infection of macrophages in p1maiy placental cell cultures. J Infect Dis, 1994;169:746-753.
31. De Andreis C, Simoni G, Rossella F, et al. HIV-l proviral DNA polymerase chain reaction detection in chorionic villi after exclusion of maternal contamination by variable number of tandem repeats analysis. AIDS. 1996;10:711-715.
32. Vicenzi E, Poli G. Regulation of HIV expression by viral genes and cytokines. J Leukoc Biol. 1994;56:328-334.
33. Griffin GE, Leung K, Folks TM, Kunkel S, Nabel GJ. Activation of HIV gene expression during monocyte differentiation by induction of NF-kappa B. Nature. 1989;339:70-73.
34. Nishitsuji H, Sugiyama R, Abe M, Takaku H. ATP1B3 Protein Modulates the Restriction of HIV-1 Production and Nuclear Factor κ Light Chain Enhancer of Activated B Cells (NF-κB) Activation by BST-2. J Biol Chem. 2016;291:4754-4762.
35. Johnson EL, R Chakraborty. HIV-1 at the placenta: immune correlates of protection and infection. Curr Opin Infect Dis. 2016;29:248-255.
36. Temmerman M, Nyongo AO, Bwayo J, Fransen K, Coppens M, Piot P. Risk factors for mother-to-child transmission of human immunodeficiency virus-I infection. Am J Obstet Gynecol. 1995;172:700-705.
37. Genbacev O, White, TEK, Gavin CE, Miller RK. Human trophoblast cultures: models for implantation and pen-implantation toxicology. Repro Toxicol, 1993;7:Suppl.175-194.
38. Dickover RE, Garratty EM, Herman SA, et al. Stiehm ER, Bryson YJ. Identification of levels of maternal HIV-1 RNA associated with risk of peninatal transmission. Effect of maternal zidovudine treatment on viral load. JAMA. 1996;275:599-605.
39. Schuitemaker H, Kootstra NA, Koppelman MH, et al. Proliferation-dependent HIV-1 infection of monocytes occurs during differentiation into macrophages. J Clin Invest. 1992;89:1154-1160.
40. Zack JA, Aivigo SJ, Weitsman SR, Go AS, Haislip A, Chen IS. HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell. 1990;61:213-222.
41. Yui J, Garcia-Lloret M, Brown AJ, et al. Functional long-term cultures of human term trophoblasts purified by column-elimination of CD9 expressing cells. Placenta.1994;15:231-246.
42. Kilani RT, Chang Li, Garcia-Lloret MI, Hemmings D, Winkler-Lowen B, Guilbert U. Placental trophoblasts resist infection by multiple human immunodeficiency virus (HIV) type 1 variants even with cytomegalovirus coinfection but support HIV replication after provirus transfection. J Virol. 1997;71:6359-6372.
43. Amirhessami-Aghili N, Spector SA. Human immunodeficiency virus type-1 infection of human placenta: potential route for fetal infection. J Virol. 1991;65:2231-2236.
44. Ding Y. Distribution of the human immunodeficiency virus receptor CD4 and chemokine receptors: CCR5, CXCR4, and CCR3 in the early human placenta. J Immunol. in press.
45. Caccuri F, Rueckert C, Giagulli C, et al. HIV-1 matrix protein p17 promotes lymphangiogenesis and activates the endothelin-1/endothelin B receptor axis. Arterioscler Thromb Vasc Biol. 2014;34:846-856.
46. Kesson AM, Fear WR, Kazazi F, et al. Human immunodeficiency virus type 1 infection of human placental macrophages in vitro. J Infect Dis, l993;168:571-579.
47. David FJ, Tran HC, Serpente N, et al. HIV infection of choriocarcinoma cell lines derived from human placenta: the role of membrane CD4 and Fc-Rs into HIV entry. Virology. 1995;208:784-788.
48. Bourinbaiar AS, Nagorny R. Human immunodeficiency virus type I infection of choriocarcinoma-derived trophoblasts. Acta Virol. 1993;37:21-28.
49. Tscherning-Casper C, Papadogiannakis N, Anvret M, et al. The trophoblast epithelial barrier is not infected in full-term placentae of human immunodeficiency virus-seropositive mothers undergoing antiretroviral therapy. J Virol. 1999;73:9673-9678.
50. Douglas GC, Fly GN, Thirkill T, et al. Cell-mediated infection of human placental trophoblast with HIV in vitro. AIDS Res Hum Retroviruses. 1991;7:735-740.
51. Fowler MG. Update: transmission of HIV-1 from mother to child. Curr Opin Obstet Gynecol. 1997;9:343-348.
52. Zhang GY, Beltchev B, Fournier A, et al. Thang MN. High levels of 2,5’-oligoadenylate synthetase and 2,5’-oligoadenylate-dependent endonuclease in human trophoblast. AIDS Res Hum Retroviruses. 1993;9:189-196.
53. Mak VC, Wong OG, Siu MK, et al. FBI-1 Is Overexpressed in Gestational Trophoblastic Disease and Promotes Tumor Growth and Cell Aggressiveness of Choriocarcinoma via PI3K/Akt Signaling. Am J Pathol. 2015;185:2038-2048.
54. Ebbesen P, Hager H, Norskov-Lauritsen N, et al. Concurrence of high levels of interferons alpha and beta in cord and maternal blood and simultaneous presence of interferon in trophoblast in an African population. J Interferon Cytokine Res. 1995;15:123-128.
55. Bourinbaiar AS, Krasinski K, Borkowsky W, Lee-Huang S. Protective effect of interferon- alpha against cell-mediated human immunodeficiency virus transmission resulting from coculture of infected lymphocytes with fetal trophoblasts. J Interferon Cytokine Res. 1995;15:503-508.
56. Guedia J, Brun P, Bhave S, et al. HIV-1 Tat exacerbates lipopolysaccharide-induced cytokine release via TLR4 signaling in the enteric nervous system. Sci Rep. 2016;6:31203.
57. Nabel G, Baltimore D. An inducible transcription factor activates expression of human immunodeficiency virus in T cells. Nature. 1987;326:711-713.
58. Folks TM, Justement J, Kinter A, Dinarello CA, Fauci AS. Cytokine-induced expression of HIV-1 in a chronically infected promonocyte cell line. Science. 1987;238:800-802.
59. Duh EJ, Maury WJ, Folks TM. Tumor necrosis factor alpha activates human immunodeficiency virus type 1 through induction of nuclear factor binding to the NF-kappa B sites in the long terminal repeat. Proc Nail Acad Sci USA. 1989;86:5974-5978.
60. Kinter AL, Poli G, Fox L. HIV replication in IL-2 -stimulated peripheral blood mononuclear cells is driven in an autocrine/paracrine manner by endogenous cytokines. J mniunol. 1995;154:2449-2459.
61. Li M, Tucker LD, Asara JM, et al. Stem-loop binding protein is a multifaceted cellular regulator of HIV-1 replication. J Clin Invest. 2016;126(8):3117-3129.
62. Koyanagi Y, O’Bien WA, Zhao JQ. Cytokines alter production of HIV-1 from primary mononuclear phagocytes. Science. 1988;241:1673-1675.
63. Latham PS, Lewis AM, Varesio L, et al. Expression of human immunodeficiency virus long terminal repeat in the human promonocyte cell line U937: effect of endotoxin and cytokines. Cell Immunol. 1990;129:513-518.
64. Poll G, Kinter AL, Fauci AS. Interleukin 1 induces expression of the human immunodeficiency virus alone and in synergy with interleukin 6 in chronically infected Ui cells: inhibition of inductive effects by the interleukin 1 receptor antagonist. Proc Nati Acad Sci USA. 1994,91:108-112.
65. Mazzuca P, Caruso A, Caccuri F. HIV-1 infection, microenvironment and endothelial cell dysfunction. New Microbiol. 2016;39:163-173.
2. Scarlatti G. Paediatric HIV infection. Lancet. 1996;348:863-868.
3. Ryder RW, Nsa W, Hassig SE,et al. Peinatal transmission of the human immunodeficiency virus type I to infants of seropositive women in Zaire. N Engl J Med. 1989; 320:1637-1642.
4. Papp E, Mohammadi H, LoutfyMR, et al. HIV protease inhibitor use during pregnancy is associated with decreased progesterone levels, suggesting a potential mechanism contributing to fetal growth restriction. J Infect Dis. 2015;211:10-18.
5. Boyer PJ, Dillon M, Navaie M, et al. Factors predictive of maternal-fetal transmission of HIV-1. Preliminary analysis of zidovudine given during pregnancy and/or delivery. JAMA. 1994;271:1925-1930.
6. Dunn DT, Newell ML, Ades AE, Peckham CS. Risk of human immunodeficiency virus type 1 transmission through breastfeeding. Lancet. 1992;340:585-588.
7. Bertolli J, St Louis ME, Simonds Ri, et al. Estimating the timing of mother-to-child transmission of human immunodeficiency virus in a breast-feeding population in Kinshasa, Zaire. J Infect Dis. 1996;174:722-726.
8. Bryson YJ, Luzuriaga K, Sullivan JL, Wara DW. Proposed definitions for in utero versus intrapartum transmission of HIV-1. N Engl J Med. 1992;327:1246-1247.
9. Lapointe N, Michaud J, Pekovic D, Chausseau JP, Dupuy JM. Transplacental transmission of HTL-VIII virus. N Engl J Med. 1985;312:1325-1326.
10. Lewis SH, Reynolds-Kohler C, Fox HE, Nelson JA. HIV-1 in trophoblast and villous Hofbauer cells, and haematological precursors in eight-week fetuses. Lancet. 1990;335:565-568.
11. Scott GB, Fischl, MA, Klimas N. Mothers of infants with acquired immunodeficiency syndrome. JAMA. 1985;253:363-366.
12. Backe E, Jimenez E, Unger M, et al. Vertical human immunodeficiency virus transmission: a study of placental pathology in relation to maternal risk factors. Am J Perinatol. 1994;11:326-330.
13. Chandwani S, Greco MA, Mittal K, Antoine C, Krasinski K, Borkowsky W. Pathology and human immunodeficiency virus expression in placenta of seropositive women. J Infect Dis. 1991;163:1134-1138.
14. Mauiy W, Potts Bi, Rabson AB. HIV-l infection of first-trimester and term human placental tissue: a possible mode of maternal-fetal transmission. J Infect Dis. 1989;160:583-588.
15. Bagasra O, Hauptman SP, Lischner HW, Sachs M, Pomerantz Ri. Detection of human immunodeficiency virus type 1 provirus in mononuclear cells by in situ polymerase chain reaction. N Engl J Med. 1992;326:1385-1391.
16. Nuovo GJ, Forde A, MacConnell P, Fahrenwald R. In situ detection of PCR-amplified HIV-1 nucleic acids and tumor necrosis factor cDNA in cervical tissues. Am J Pathol, 1993;143:40-48.
17. Brunstein J. In situ PCR: MDx meets histology. MLO Med Lab Obs. 2015;47:48-50.
18. Zevailos EA, Anderson VM, Bard E, Gu, J. Detection of HIV-1 sequences in placenta of HIV-infected mothers by n situ PCR. Cell Vision. 1994;1:116-121.
19. Sheikh AU, Polliotti, BM, Miller RK. In situ PCR discriminates between infected and uninfected human placental explants after in vitro exposure to HIV-l. Trophohiast Research. 1998;12:191-204.
20. Johnson EL, Chu H, Byrareddy SN, Spearman P, Chakraborty R. Placental Hofbauer cells assemble and sequester HIV-1 in tetraspanin-positive compartments that are accessible to broadly neutralizing antibodies. J Int AIDS Soc. 2015;18:19385.
21. Johnson EL, R Chakraborty. Placental Hofbauer cells limit HIV-1 replication and potentially offset mother to child transmission (MTCT) by induction of immunoregulatory cytokines. Retrovirology. 2012;9:101.
22. Al-Husaini AM. Role of placenta in the vertical transmission of human immunodeficiency virus. J Perinatol. 2009;29:331-336.
23. Mattern CF, Munay K, Jensen A, Farzadegan H, Pang J, Modlin IF. Localization of human immunodeficiency virus core antigen in term human placenta. Pediatrics. 1992;89:207-209.
24. David FJ, Autran B, Tran HC, et al. Human trophoblast cells express CD4 and are permissive for productive infection with HIV-1. Clin Exp Immunol. 1992;88:1016.
25. Dorsamy V, Vallen C. The role of trophoblast cell receptor expression in HIV-1 passage across the placenta in pre-eclampsia: an observational study. BJOG. 2016;10:1471-1528.
26. Toth FD, Mosborg-Petersen P, Kiss J, et al. Antibody-dependent enhancement of HIV-l infectionin human term syncytiotrophoblast
cells cultured in vitro. Clin Exp Immunol. 1994;96:389-394.
27. Zachar V, Norskov-Lauitsen N, Juhi C, Spire B, Chermann JC, Ebbesen P. Susceptibility of cultured human trophoblasts to infection with human immunodeficiency virus type 1. J Gen Virol. 1991;72:1253-1260.
28. Chisanga C, Eggert D, Mitchell CD, Wood C, Angeletti PC. Evidence for Placental HPV Infection in Both HIV Positive and Negative Women. J Cancer Ther. 2015;6:1276-1289.
29. Douglas GC, Fry GN, Thirkill T. Cell-mediated infection of human placental trophoblast with HIV in vitro. AIDS Res Hum Retroviruses. 1991;7:735-740.
30. McGann KA, Collman R, Kolson DL, et al. Human immunodeficiency virus type 1 causes productive infection of macrophages in p1maiy placental cell cultures. J Infect Dis, 1994;169:746-753.
31. De Andreis C, Simoni G, Rossella F, et al. HIV-l proviral DNA polymerase chain reaction detection in chorionic villi after exclusion of maternal contamination by variable number of tandem repeats analysis. AIDS. 1996;10:711-715.
32. Vicenzi E, Poli G. Regulation of HIV expression by viral genes and cytokines. J Leukoc Biol. 1994;56:328-334.
33. Griffin GE, Leung K, Folks TM, Kunkel S, Nabel GJ. Activation of HIV gene expression during monocyte differentiation by induction of NF-kappa B. Nature. 1989;339:70-73.
34. Nishitsuji H, Sugiyama R, Abe M, Takaku H. ATP1B3 Protein Modulates the Restriction of HIV-1 Production and Nuclear Factor κ Light Chain Enhancer of Activated B Cells (NF-κB) Activation by BST-2. J Biol Chem. 2016;291:4754-4762.
35. Johnson EL, R Chakraborty. HIV-1 at the placenta: immune correlates of protection and infection. Curr Opin Infect Dis. 2016;29:248-255.
36. Temmerman M, Nyongo AO, Bwayo J, Fransen K, Coppens M, Piot P. Risk factors for mother-to-child transmission of human immunodeficiency virus-I infection. Am J Obstet Gynecol. 1995;172:700-705.
37. Genbacev O, White, TEK, Gavin CE, Miller RK. Human trophoblast cultures: models for implantation and pen-implantation toxicology. Repro Toxicol, 1993;7:Suppl.175-194.
38. Dickover RE, Garratty EM, Herman SA, et al. Stiehm ER, Bryson YJ. Identification of levels of maternal HIV-1 RNA associated with risk of peninatal transmission. Effect of maternal zidovudine treatment on viral load. JAMA. 1996;275:599-605.
39. Schuitemaker H, Kootstra NA, Koppelman MH, et al. Proliferation-dependent HIV-1 infection of monocytes occurs during differentiation into macrophages. J Clin Invest. 1992;89:1154-1160.
40. Zack JA, Aivigo SJ, Weitsman SR, Go AS, Haislip A, Chen IS. HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell. 1990;61:213-222.
41. Yui J, Garcia-Lloret M, Brown AJ, et al. Functional long-term cultures of human term trophoblasts purified by column-elimination of CD9 expressing cells. Placenta.1994;15:231-246.
42. Kilani RT, Chang Li, Garcia-Lloret MI, Hemmings D, Winkler-Lowen B, Guilbert U. Placental trophoblasts resist infection by multiple human immunodeficiency virus (HIV) type 1 variants even with cytomegalovirus coinfection but support HIV replication after provirus transfection. J Virol. 1997;71:6359-6372.
43. Amirhessami-Aghili N, Spector SA. Human immunodeficiency virus type-1 infection of human placenta: potential route for fetal infection. J Virol. 1991;65:2231-2236.
44. Ding Y. Distribution of the human immunodeficiency virus receptor CD4 and chemokine receptors: CCR5, CXCR4, and CCR3 in the early human placenta. J Immunol. in press.
45. Caccuri F, Rueckert C, Giagulli C, et al. HIV-1 matrix protein p17 promotes lymphangiogenesis and activates the endothelin-1/endothelin B receptor axis. Arterioscler Thromb Vasc Biol. 2014;34:846-856.
46. Kesson AM, Fear WR, Kazazi F, et al. Human immunodeficiency virus type 1 infection of human placental macrophages in vitro. J Infect Dis, l993;168:571-579.
47. David FJ, Tran HC, Serpente N, et al. HIV infection of choriocarcinoma cell lines derived from human placenta: the role of membrane CD4 and Fc-Rs into HIV entry. Virology. 1995;208:784-788.
48. Bourinbaiar AS, Nagorny R. Human immunodeficiency virus type I infection of choriocarcinoma-derived trophoblasts. Acta Virol. 1993;37:21-28.
49. Tscherning-Casper C, Papadogiannakis N, Anvret M, et al. The trophoblast epithelial barrier is not infected in full-term placentae of human immunodeficiency virus-seropositive mothers undergoing antiretroviral therapy. J Virol. 1999;73:9673-9678.
50. Douglas GC, Fly GN, Thirkill T, et al. Cell-mediated infection of human placental trophoblast with HIV in vitro. AIDS Res Hum Retroviruses. 1991;7:735-740.
51. Fowler MG. Update: transmission of HIV-1 from mother to child. Curr Opin Obstet Gynecol. 1997;9:343-348.
52. Zhang GY, Beltchev B, Fournier A, et al. Thang MN. High levels of 2,5’-oligoadenylate synthetase and 2,5’-oligoadenylate-dependent endonuclease in human trophoblast. AIDS Res Hum Retroviruses. 1993;9:189-196.
53. Mak VC, Wong OG, Siu MK, et al. FBI-1 Is Overexpressed in Gestational Trophoblastic Disease and Promotes Tumor Growth and Cell Aggressiveness of Choriocarcinoma via PI3K/Akt Signaling. Am J Pathol. 2015;185:2038-2048.
54. Ebbesen P, Hager H, Norskov-Lauritsen N, et al. Concurrence of high levels of interferons alpha and beta in cord and maternal blood and simultaneous presence of interferon in trophoblast in an African population. J Interferon Cytokine Res. 1995;15:123-128.
55. Bourinbaiar AS, Krasinski K, Borkowsky W, Lee-Huang S. Protective effect of interferon- alpha against cell-mediated human immunodeficiency virus transmission resulting from coculture of infected lymphocytes with fetal trophoblasts. J Interferon Cytokine Res. 1995;15:503-508.
56. Guedia J, Brun P, Bhave S, et al. HIV-1 Tat exacerbates lipopolysaccharide-induced cytokine release via TLR4 signaling in the enteric nervous system. Sci Rep. 2016;6:31203.
57. Nabel G, Baltimore D. An inducible transcription factor activates expression of human immunodeficiency virus in T cells. Nature. 1987;326:711-713.
58. Folks TM, Justement J, Kinter A, Dinarello CA, Fauci AS. Cytokine-induced expression of HIV-1 in a chronically infected promonocyte cell line. Science. 1987;238:800-802.
59. Duh EJ, Maury WJ, Folks TM. Tumor necrosis factor alpha activates human immunodeficiency virus type 1 through induction of nuclear factor binding to the NF-kappa B sites in the long terminal repeat. Proc Nail Acad Sci USA. 1989;86:5974-5978.
60. Kinter AL, Poli G, Fox L. HIV replication in IL-2 -stimulated peripheral blood mononuclear cells is driven in an autocrine/paracrine manner by endogenous cytokines. J mniunol. 1995;154:2449-2459.
61. Li M, Tucker LD, Asara JM, et al. Stem-loop binding protein is a multifaceted cellular regulator of HIV-1 replication. J Clin Invest. 2016;126(8):3117-3129.
62. Koyanagi Y, O’Bien WA, Zhao JQ. Cytokines alter production of HIV-1 from primary mononuclear phagocytes. Science. 1988;241:1673-1675.
63. Latham PS, Lewis AM, Varesio L, et al. Expression of human immunodeficiency virus long terminal repeat in the human promonocyte cell line U937: effect of endotoxin and cytokines. Cell Immunol. 1990;129:513-518.
64. Poll G, Kinter AL, Fauci AS. Interleukin 1 induces expression of the human immunodeficiency virus alone and in synergy with interleukin 6 in chronically infected Ui cells: inhibition of inductive effects by the interleukin 1 receptor antagonist. Proc Nati Acad Sci USA. 1994,91:108-112.
65. Mazzuca P, Caruso A, Caccuri F. HIV-1 infection, microenvironment and endothelial cell dysfunction. New Microbiol. 2016;39:163-173.
Published
2016-10-31
How to Cite
Wu, MD, F., Zhang, MD, F., Ding, E., & Ding, MD, PhD, Y. (2016). HIV-1 infection in early human placenta in vitro: Effects of Tumor Necrosis Factor (TNF-α) and Interleukins IL-1 and IL-6. North American Journal of Medicine and Science, 9(4). Retrieved from https://najms.com/index.php/najms/article/view/318
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