Abstract
Variation in the env (V3 region) and gag (p17 region) genes of genomic RNA of human immunodeficiency virus type 1 was studied in three mother-child pairs. One infant was human immunodeficiency virus type 1 RNA positive at birth (pair 114), one became positive 6 weeks after birth (pair 127), and one became positive 30 months after birth (pair 564). The first two children were born to seropositive mothers, and the last child was infected by breast-feeding following seroconversion of the mother after delivery. In both V3 and p17gag, intrasample variability was much higher in the maternal samples, including the first seropositive sample of the seroconverted mother, than in the infants' samples. Variability was less in p17gag than in V3, except in the postnatally infected child. In all three cases, infection of the child was established by variants representing a minority of the cell-free virus population in the maternal samples. For the two infants born to seropositive mothers, V3 sequences were more similar to the sequence populations of maternal samples collected during pregnancy than to those of samples collected at delivery or thereafter. However, in pair 114 a V3 variant identical to the child's virus was also detected in the sample collected at delivery. In contrast to the V3 region, p17gag sequences of maternal samples of the first trimester of pregnancy and at delivery had comparable resemblance to the child's sequences in pair 114, while in pair 127, similarity to sequences of the sample collected at delivery was higher than that to sequences of the sample from early in pregnancy. In the last pair, V3 and p17gag sequences from a maternal sample collected 18 months prior to the first RNA-positive sample of the child resembled the infant's sequences as much as the sample collected close to the presumed time of infection. Taken together, the evolutionary characteristics for genomic RNA env and gag genes did not point to a particular time of mother-to-child transmission.
Full Text
The Full Text of this article is available as a PDF (380.7 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Abimiku A. G., Stern T. L., Zwandor A., Markham P. D., Calef C., Kyari S., Saxinger W. C., Gallo R. C., Robert-Guroff M., Reitz M. S. Subgroup G HIV type 1 isolates from Nigeria. AIDS Res Hum Retroviruses. 1994 Nov;10(11):1581–1583. doi: 10.1089/aid.1994.10.1581. [DOI] [PubMed] [Google Scholar]
- Boom R., Sol C. J., Salimans M. M., Jansen C. L., Wertheim-van Dillen P. M., van der Noordaa J. Rapid and simple method for purification of nucleic acids. J Clin Microbiol. 1990 Mar;28(3):495–503. doi: 10.1128/jcm.28.3.495-503.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Borkowsky W., Krasinski K., Pollack H., Hoover W., Kaul A., Ilmet-Moore T. Early diagnosis of human immunodeficiency virus infection in children less than 6 months of age: comparison of polymerase chain reaction, culture, and plasma antigen capture techniques. J Infect Dis. 1992 Sep;166(3):616–619. doi: 10.1093/infdis/166.3.616. [DOI] [PubMed] [Google Scholar]
- Bryson Y. J., Luzuriaga K., Sullivan J. L., Wara D. W. Proposed definitions for in utero versus intrapartum transmission of HIV-1. N Engl J Med. 1992 Oct 22;327(17):1246–1247. doi: 10.1056/NEJM199210223271718. [DOI] [PubMed] [Google Scholar]
- Burgard M., Mayaux M. J., Blanche S., Ferroni A., Guihard-Moscato M. L., Allemon M. C., Ciraru-Vigneron N., Firtion G., Floch C., Guillot F. The use of viral culture and p24 antigen testing to diagnose human immunodeficiency virus infection in neonates. The HIV Infection in Newborns French Collaborative Study Group. N Engl J Med. 1992 Oct 22;327(17):1192–1197. doi: 10.1056/NEJM199210223271702. [DOI] [PubMed] [Google Scholar]
- Cornelissen M., Mulder-Kampinga G., Veenstra J., Zorgdrager F., Kuiken C., Hartman S., Dekker J., van der Hoek L., Sol C., Coutinho R. Syncytium-inducing (SI) phenotype suppression at seroconversion after intramuscular inoculation of a non-syncytium-inducing/SI phenotypically mixed human immunodeficiency virus population. J Virol. 1995 Mar;69(3):1810–1818. doi: 10.1128/jvi.69.3.1810-1818.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- De Jong J. J., De Ronde A., Keulen W., Tersmette M., Goudsmit J. Minimal requirements for the human immunodeficiency virus type 1 V3 domain to support the syncytium-inducing phenotype: analysis by single amino acid substitution. J Virol. 1992 Nov;66(11):6777–6780. doi: 10.1128/jvi.66.11.6777-6780.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- De Wolf F., Hogervorst E., Goudsmit J., Fenyö E. M., Rübsamen-Waigmann H., Holmes H., Galvao-Castro B., Karita E., Wasi C., Sempala S. D. Syncytium-inducing and non-syncytium-inducing capacity of human immunodeficiency virus type 1 subtypes other than B: phenotypic and genotypic characteristics. WHO Network for HIV Isolation and Characterization. AIDS Res Hum Retroviruses. 1994 Nov;10(11):1387–1400. doi: 10.1089/aid.1994.10.1387. [DOI] [PubMed] [Google Scholar]
- Fantini J., Yahi N., Baghdiguian S., Chermann J. C. Human colon epithelial cells productively infected with human immunodeficiency virus show impaired differentiation and altered secretion. J Virol. 1992 Jan;66(1):580–585. doi: 10.1128/jvi.66.1.580-585.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fouchier R. A., Groenink M., Kootstra N. A., Tersmette M., Huisman H. G., Miedema F., Schuitemaker H. Phenotype-associated sequence variation in the third variable domain of the human immunodeficiency virus type 1 gp120 molecule. J Virol. 1992 May;66(5):3183–3187. doi: 10.1128/jvi.66.5.3183-3187.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goedert J. J., Duliège A. M., Amos C. I., Felton S., Biggar R. J. High risk of HIV-1 infection for first-born twins. The International Registry of HIV-exposed Twins. Lancet. 1991 Dec 14;338(8781):1471–1475. doi: 10.1016/0140-6736(91)92297-f. [DOI] [PubMed] [Google Scholar]
- Goudsmit J., Debouck C., Meloen R. H., Smit L., Bakker M., Asher D. M., Wolff A. V., Gibbs C. J., Jr, Gajdusek D. C. Human immunodeficiency virus type 1 neutralization epitope with conserved architecture elicits early type-specific antibodies in experimentally infected chimpanzees. Proc Natl Acad Sci U S A. 1988 Jun;85(12):4478–4482. doi: 10.1073/pnas.85.12.4478. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Holmes E. C., Zhang L. Q., Simmonds P., Ludlam C. A., Brown A. J. Convergent and divergent sequence evolution in the surface envelope glycoprotein of human immunodeficiency virus type 1 within a single infected patient. Proc Natl Acad Sci U S A. 1992 Jun 1;89(11):4835–4839. doi: 10.1073/pnas.89.11.4835. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hwang S. S., Boyle T. J., Lyerly H. K., Cullen B. R. Identification of the envelope V3 loop as the primary determinant of cell tropism in HIV-1. Science. 1991 Jul 5;253(5015):71–74. doi: 10.1126/science.1905842. [DOI] [PubMed] [Google Scholar]
- Janssens W., Heyndrickx L., Fransen K., Motte J., Peeters M., Nkengasong J. N., Ndumbe P. M., Delaporte E., Perret J. L., Atende C. Genetic and phylogenetic analysis of env subtypes G and H in central Africa. AIDS Res Hum Retroviruses. 1994 Jul;10(7):877–879. doi: 10.1089/aid.1994.10.877. [DOI] [PubMed] [Google Scholar]
- Javaherian K., Langlois A. J., McDanal C., Ross K. L., Eckler L. I., Jellis C. L., Profy A. T., Rusche J. R., Bolognesi D. P., Putney S. D. Principal neutralizing domain of the human immunodeficiency virus type 1 envelope protein. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6768–6772. doi: 10.1073/pnas.86.17.6768. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kimura M. Estimation of evolutionary distances between homologous nucleotide sequences. Proc Natl Acad Sci U S A. 1981 Jan;78(1):454–458. doi: 10.1073/pnas.78.1.454. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kliks S. C., Wara D. W., Landers D. V., Levy J. A. Features of HIV-1 that could influence maternal-child transmission. JAMA. 1994 Aug 10;272(6):467–474. [PubMed] [Google Scholar]
- Koup R. A., Safrit J. T., Cao Y., Andrews C. A., McLeod G., Borkowsky W., Farthing C., Ho D. D. Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J Virol. 1994 Jul;68(7):4650–4655. doi: 10.1128/jvi.68.7.4650-4655.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Krivine A., Firtion G., Cao L., Francoual C., Henrion R., Lebon P. HIV replication during the first weeks of life. Lancet. 1992 May 16;339(8803):1187–1189. doi: 10.1016/0140-6736(92)91131-q. [DOI] [PubMed] [Google Scholar]
- Lamers S. L., Sleasman J. W., She J. X., Barrie K. A., Pomeroy S. M., Barrett D. J., Goodenow M. M. Persistence of multiple maternal genotypes of human immunodeficiency virus type I in infants infected by vertical transmission. J Clin Invest. 1994 Jan;93(1):380–390. doi: 10.1172/JCI116970. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lewis S. H., Reynolds-Kohler C., Fox H. E., Nelson J. A. HIV-1 in trophoblastic and villous Hofbauer cells, and haematological precursors in eight-week fetuses. Lancet. 1990 Mar 10;335(8689):565–568. doi: 10.1016/0140-6736(90)90349-a. [DOI] [PubMed] [Google Scholar]
- Mano H., Chermann J. C. Fetal human immunodeficiency virus type 1 infection of different organs in the second trimester. AIDS Res Hum Retroviruses. 1991 Jan;7(1):83–88. doi: 10.1089/aid.1991.7.83. [DOI] [PubMed] [Google Scholar]
- McGann K. A., Collman R., Kolson D. L., Gonzalez-Scarano F., Coukos G., Coutifaris C., Strauss J. F., Nathanson N. Human immunodeficiency virus type 1 causes productive infection of macrophages in primary placental cell cultures. J Infect Dis. 1994 Apr;169(4):746–753. doi: 10.1093/infdis/169.4.746. [DOI] [PubMed] [Google Scholar]
- Milman G., Sharma O. Mechanisms of HIV/SIV mucosal transmission. AIDS Res Hum Retroviruses. 1994 Oct;10(10):1305–1312. doi: 10.1089/aid.1994.10.1305. [DOI] [PubMed] [Google Scholar]
- Mulder-Kampinga G. A., Kuiken C., Dekker J., Scherpbier H. J., Boer K., Goudsmit J. Genomic human immunodeficiency virus type 1 RNA variation in mother and child following intra-uterine virus transmission. J Gen Virol. 1993 Sep;74(Pt 9):1747–1756. doi: 10.1099/0022-1317-74-9-1747. [DOI] [PubMed] [Google Scholar]
- Nei M., Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 1986 Sep;3(5):418–426. doi: 10.1093/oxfordjournals.molbev.a040410. [DOI] [PubMed] [Google Scholar]
- Pang S., Shlesinger Y., Daar E. S., Moudgil T., Ho D. D., Chen I. S. Rapid generation of sequence variation during primary HIV-1 infection. AIDS. 1992 May;6(5):453–460. doi: 10.1097/00002030-199205000-00003. [DOI] [PubMed] [Google Scholar]
- Pantaleo G., Graziosi C., Demarest J. F., Cohen O. J., Vaccarezza M., Gantt K., Muro-Cacho C., Fauci A. S. Role of lymphoid organs in the pathogenesis of human immunodeficiency virus (HIV) infection. Immunol Rev. 1994 Aug;140:105–130. doi: 10.1111/j.1600-065x.1994.tb00867.x. [DOI] [PubMed] [Google Scholar]
- Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
- Scarlatti G., Albert J., Rossi P., Hodara V., Biraghi P., Muggiasca L., Fenyö E. M. Mother-to-child transmission of human immunodeficiency virus type 1: correlation with neutralizing antibodies against primary isolates. J Infect Dis. 1993 Jul;168(1):207–210. doi: 10.1093/infdis/168.1.207. [DOI] [PubMed] [Google Scholar]
- Scarlatti G., Leitner T., Halapi E., Wahlberg J., Marchisio P., Clerici-Schoeller M. A., Wigzell H., Fenyö E. M., Albert J., Uhlén M. Comparison of variable region 3 sequences of human immunodeficiency virus type 1 from infected children with the RNA and DNA sequences of the virus populations of their mothers. Proc Natl Acad Sci U S A. 1993 Mar 1;90(5):1721–1725. doi: 10.1073/pnas.90.5.1721. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schuitemaker H., Koot M., Kootstra N. A., Dercksen M. W., de Goede R. E., van Steenwijk R. P., Lange J. M., Schattenkerk J. K., Miedema F., Tersmette M. Biological phenotype of human immunodeficiency virus type 1 clones at different stages of infection: progression of disease is associated with a shift from monocytotropic to T-cell-tropic virus population. J Virol. 1992 Mar;66(3):1354–1360. doi: 10.1128/jvi.66.3.1354-1360.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Simmonds P., Zhang L. Q., McOmish F., Balfe P., Ludlam C. A., Brown A. J. Discontinuous sequence change of human immunodeficiency virus (HIV) type 1 env sequences in plasma viral and lymphocyte-associated proviral populations in vivo: implications for models of HIV pathogenesis. J Virol. 1991 Nov;65(11):6266–6276. doi: 10.1128/jvi.65.11.6266-6276.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smith J. M., Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Feb;23(1):23–35. [PubMed] [Google Scholar]
- Soeiro R., Rubinstein A., Rashbaum W. K., Lyman W. D. Maternofetal transmission of AIDS: frequency of human immunodeficiency virus type 1 nucleic acid sequences in human fetal DNA. J Infect Dis. 1992 Oct;166(4):699–703. doi: 10.1093/infdis/166.4.699. [DOI] [PubMed] [Google Scholar]
- Stamatatos L., Cheng-Mayer C. Evidence that the structural conformation of envelope gp120 affects human immunodeficiency virus type 1 infectivity, host range, and syncytium-forming ability. J Virol. 1993 Sep;67(9):5635–5639. doi: 10.1128/jvi.67.9.5635-5639.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Van de Perre P., Hitimana D. G., Simonon A., Dabis F., Msellati P., Karita P., Lepage P. Postnatal transmission of HIV-1 associated with breast abscess. Lancet. 1992 Jun 13;339(8807):1490–1491. doi: 10.1016/0140-6736(92)92097-y. [DOI] [PubMed] [Google Scholar]
- Van de Perre P., Simonon A., Msellati P., Hitimana D. G., Vaira D., Bazubagira A., Van Goethem C., Stevens A. M., Karita E., Sondag-Thull D. Postnatal transmission of human immunodeficiency virus type 1 from mother to infant. A prospective cohort study in Kigali, Rwanda. N Engl J Med. 1991 Aug 29;325(9):593–598. doi: 10.1056/NEJM199108293250901. [DOI] [PubMed] [Google Scholar]
- Wike C. M., Korber B. T., Daniels M. R., Hutto C., Muñoz J., Furtado M., Parks W., Saah A., Bulterys M., Kurawige J. B. HIV-1 sequence variation between isolates from mother-infant transmission pairs. AIDS Res Hum Retroviruses. 1992 Jul;8(7):1297–1300. doi: 10.1089/aid.1992.8.1297. [DOI] [PubMed] [Google Scholar]
- Wolfs T. F., Zwart G., Bakker M., Goudsmit J. HIV-1 genomic RNA diversification following sexual and parenteral virus transmission. Virology. 1992 Jul;189(1):103–110. doi: 10.1016/0042-6822(92)90685-i. [DOI] [PubMed] [Google Scholar]
- Wolfs T. F., Zwart G., Bakker M., Valk M., Kuiken C. L., Goudsmit J. Naturally occurring mutations within HIV-1 V3 genomic RNA lead to antigenic variation dependent on a single amino acid substitution. Virology. 1991 Nov;185(1):195–205. doi: 10.1016/0042-6822(91)90767-6. [DOI] [PubMed] [Google Scholar]
- Wolfs T. F., de Jong J. J., Van den Berg H., Tijnagel J. M., Krone W. J., Goudsmit J. Evolution of sequences encoding the principal neutralization epitope of human immunodeficiency virus 1 is host dependent, rapid, and continuous. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9938–9942. doi: 10.1073/pnas.87.24.9938. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wolinsky S. M., Wike C. M., Korber B. T., Hutto C., Parks W. P., Rosenblum L. L., Kunstman K. J., Furtado M. R., Muñoz J. L. Selective transmission of human immunodeficiency virus type-1 variants from mothers to infants. Science. 1992 Feb 28;255(5048):1134–1137. doi: 10.1126/science.1546316. [DOI] [PubMed] [Google Scholar]
- Zachar V., Nørskov-Lauritsen N., Juhl C., Spire B., Chermann J. C., Ebbesen P. Susceptibility of cultured human trophoblasts to infection with human immunodeficiency virus type 1. J Gen Virol. 1991 Jun;72(Pt 6):1253–1260. doi: 10.1099/0022-1317-72-6-1253. [DOI] [PubMed] [Google Scholar]
- Zhang L. Q., MacKenzie P., Cleland A., Holmes E. C., Brown A. J., Simmonds P. Selection for specific sequences in the external envelope protein of human immunodeficiency virus type 1 upon primary infection. J Virol. 1993 Jun;67(6):3345–3356. doi: 10.1128/jvi.67.6.3345-3356.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhu T., Mo H., Wang N., Nam D. S., Cao Y., Koup R. A., Ho D. D. Genotypic and phenotypic characterization of HIV-1 patients with primary infection. Science. 1993 Aug 27;261(5125):1179–1181. doi: 10.1126/science.8356453. [DOI] [PubMed] [Google Scholar]
- Ziegler J. B., Cooper D. A., Johnson R. O., Gold J. Postnatal transmission of AIDS-associated retrovirus from mother to infant. Lancet. 1985 Apr 20;1(8434):896–898. doi: 10.1016/s0140-6736(85)91673-3. [DOI] [PubMed] [Google Scholar]
- de Jong J. J., Goudsmit J., Keulen W., Klaver B., Krone W., Tersmette M., de Ronde A. Human immunodeficiency virus type 1 clones chimeric for the envelope V3 domain differ in syncytium formation and replication capacity. J Virol. 1992 Feb;66(2):757–765. doi: 10.1128/jvi.66.2.757-765.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- van't Wout A. B., Kootstra N. A., Mulder-Kampinga G. A., Albrecht-van Lent N., Scherpbier H. J., Veenstra J., Boer K., Coutinho R. A., Miedema F., Schuitemaker H. Macrophage-tropic variants initiate human immunodeficiency virus type 1 infection after sexual, parenteral, and vertical transmission. J Clin Invest. 1994 Nov;94(5):2060–2067. doi: 10.1172/JCI117560. [DOI] [PMC free article] [PubMed] [Google Scholar]