HIV-1 Infection: The Role of the Gastrointestinal Tract

American Journal of Reproductive Immunology

Volumn 71, Issue 6, 2014, Pages 537-542

  Cavarelli, Mariangela ^a   Scarlatti, Gabriella ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

Author keywords

HIV; Intestinal mucosa; Transmission

Indexed keywords

ANTIBODY; CD209 ANTIGEN; CHEMOKINE; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR4; CYTOKINE;

ANTIGEN PRESENTING CELL; ARTICLE; CD4+ T LYMPHOCYTE; DENDRITIC CELL; GASTROINTESTINAL MUCOSA; GASTROINTESTINAL TRACT; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; INFECTION PREVENTION; INTESTINE EPITHELIUM; INTESTINE LYMPHATIC TISSUE; INTESTINE MUCOSA; LANGERHANS CELL; MACROPHAGE; MEMBRANE PERMEABILITY; MUCOSAL IMMUNITY; NONHUMAN; OROPHARYNX; PEYER PATCH; PRIORITY JOURNAL; RECTUM; SEXUAL TRANSMISSION; TARGET CELL; VAGINA MUCOSA; VERTICAL TRANSMISSION; VIRUS REPLICATION; VIRUS TRANSMISSION; CYTOLOGY; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; PATHOGENICITY; PATHOLOGY; TRANSMISSION; VIROLOGY;

CD4-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; GASTROINTESTINAL TRACT; HIV INFECTIONS; HIV-1; HUMANS; INFECTIOUS DISEASE TRANSMISSION, VERTICAL; INTESTINAL MUCOSA; LANGERHANS CELLS; MACROPHAGES; VIRUS REPLICATION;

EID: 84900801990     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/aji.12245     Document Type: Article

References (59)

1. Rousseau CM, Nduati RW, Richardson BA, Steele MS, John-Stewart GC, Mbori-Ngacha DA, Kreiss JK, Overbaugh J: Longitudinal analysis of human immunodeficiency virus type 1 RNA in breast milk and of its relationship to infant infection and maternal disease. J Infect Dis 2003; 187:741-747.
2. Royce RA, Sena A, Cates W Jr, Cohen MS: Sexual transmission of HIV. N Engl J Med 1997; 336:1072-1078.
3. Baggaley RF, Dimitrov D, Owen BN, Pickles M, Butler AR, Masse B, Boily MC: Heterosexual anal intercourse: a neglected risk factor for HIV? Am J Reprod Immunol 2013; 69(Suppl 1):95-105.
4. Baggaley RF, White RG, Boily MC: HIV transmission risk through anal intercourse: systematic review, meta-analysis and implications for HIV prevention. Int J Epidemiol 2010; 39:1048-1063.
5. Klot JF, Auerbach JD, Veronese F, Brown G, Pei A, Wira CR, Hope TJ, M'Boup S: Greentree white paper: sexual violence, genitoanal injury, and HIV: priorities for research, policy, and practice. AIDS Res Hum Retroviruses 2012; 28:1379-1388.
6. Gray RH, Wawer MJ, Brookmeyer R, Sewankambo NK, Serwadda D, Wabwire-Mangen F, Lutalo T, Li X, vanCott T, Quinn TC: Probability of HIV-1 transmission per coital act in monogamous, heterosexual, HIV-1-discordant couples in Rakai, Uganda. Lancet 2001; 357:1149-1153.
7. Vittinghoff E, Douglas J, Judson F, McKirnan D, MacQueen K, Buchbinder SP: Per-contact risk of human immunodeficiency virus transmission between male sexual partners. Am J Epidemiol 1999; 150:306-311.
8. Wawer MJ, Gray RH, Sewankambo NK, Serwadda D, Li X, Laeyendecker O, Kiwanuka N, Kigozi G, Kiddugavu M, Lutalo T, Nalugoda F, Wabwire-Mangen F, Meehan MP, Quinn TC: Rates of HIV-1 transmission per coital act, by stage of HIV-1 infection, in Rakai, Uganda. J Infect Dis 2005; 191:1403-1409.
9. Guler T, Uygur D, Uncu M, Yayci E, Atacag T, Bas K, Gunay M, Yakicier C: Coexisting anal human papilloma virus infection in heterosexual women with cervical HPV infection. Arch Gynecol Obstet 2013; 288:667-672.
10. Kraehenbuhl JP, Neutra MR: Molecular and cellular basis of immune protection of mucosal surfaces. Physiol Rev 1992; 72:853-879.
11. Langman JM, Rowland R: The number and distribution of lymphoid follicles in the human large intestine. J Anat 1986; 149:189-194.
12. O'Leary AD, Sweeney EC: Lymphoglandular complexes of the colon: structure and distribution. Histopathology 1986; 10:267-283.
13. Schieferdecker HL, Ullrich R, Hirseland H, Zeitz M: T cell differentiation antigens on lymphocytes in the human intestinal lamina propria. J Immunol 1992; 149:2816-2822.
14. Bunders MJ, van der Loos CM, Klarenbeek PL, van Hamme JL, Boer K, Wilde JC, de Vries N, van Lier RA, Kootstra N, Pals ST, Kuijpers TW: Memory CD4(+)CCR5(+) T cells are abundantly present in the gut of newborn infants to facilitate mother-to-child transmission of HIV-1. Blood 2012; 120:4383-4390.
15. Li Q, Duan L, Estes JD, Ma ZM, Rourke T, Wang Y, Reilly C, Carlis J, Miller CJ, Haase AT: Peak SIV replication in resting memory CD4 + T cells depletes gut lamina propria CD4 + T cells. Nature 2005; 434:1148-1152.
16. Mattapallil JJ, Douek DC, Hill B, Nishimura Y, Martin M, Roederer M: Massive infection and loss of memory CD4 + T cells in multiple tissues during acute SIV infection. Nature 2005; 434:1093-1097.
17. Veazey RS, DeMaria M, Chalifoux LV, Shvetz DE, Pauley DR, Knight HL, Rosenzweig M, Johnson RP, Desrosiers RC, Lackner AA: Gastrointestinal tract as a major site of CD4 + T cell depletion and viral replication in SIV infection. Science 1998; 280:427-431.
18. Guadalupe M, Sankaran S, George MD, Reay E, Verhoeven D, Shacklett BL, Flamm J, Wegelin J, Prindiville T, Dandekar S: Viral suppression and immune restoration in the gastrointestinal mucosa of human immunodeficiency virus type 1-infected patients initiating therapy during primary or chronic infection. J Virol 2006; 80:8236-8247.
19. Cicala C, Martinelli E, McNally JP, Goode DJ, Gopaul R, Hiatt J, Jelicic K, Kottilil S, Macleod K, O'Shea A, Patel N, Van Ryk D, Wei D, Pascuccio M, Yi L, McKinnon L, Izulla P, Kimani J, Kaul R, Fauci AS, Arthos J: The integrin alpha4beta7 forms a complex with cell-surface CD4 and defines a T-cell subset that is highly susceptible to infection by HIV-1. Proc Natl Acad Sci USA 2009; 106:20877-20882.
20. Kader M, Bixler S, Roederer M, Veazey R, Mattapallil JJ: CD4 T cell subsets in the mucosa are CD28 + Ki-67-HLA-DR-CD69 + but show differential infection based on alpha4beta7 receptor expression during acute SIV infection. J Med Primatol 2009; 38(Suppl 1):24-31.
21. Kader M, Wang X, Piatak M, Lifson J, Roederer M, Veazey R, Mattapallil JJ: Alpha4(+)beta7(hi)CD4(+) memory T cells harbor most Th-17 cells and are preferentially infected during acute SIV infection. Mucosal Immunol 2009; 2:439-449.
22. Martinelli E, Veglia F, Goode D, Guerra-Perez N, Aravantinou M, Arthos J, Piatak M Jr, Lifson JD, Blanchard J, Gettie A, Robbiani M: The frequency of alpha(4)beta(7)(high) memory CD4(+) T cells correlates with susceptibility to rectal simian immunodeficiency virus infection. J Acquir Immune Defic Syndr 2013; 64:325-331.
23. Iwasaki A: Mucosal dendritic cells. Annu Rev Immunol 2007; 25:381-418.
24. Smith PD, Ochsenbauer-Jambor C, Smythies LE: Intestinal macrophages: unique effector cells of the innate immune system. Immunol Rev 2005; 206:149-159.
25. Shen R, Smythies LE, Clements RH, Novak L, Smith PD: Dendritic cells transmit HIV-1 through human small intestinal mucosa. J Leukoc Biol 2010; 87:663-670.
26. Preza GC, Tanner K, Elliott J, Yang OO, Anton PA, Ochoa MT. Antigen-Presenting Cell Candidates for HIV-1 Transmission in Human Distal Colonic Mucosa Defined by CD207 Dendritic Cells and CD209 Macrophages. AIDS Res Hum Retroviruses. 2014; 30:241-249.
27. Jameson B, Baribaud F, Pohlmann S, Ghavimi D, Mortari F, Doms RW, Iwasaki A: Expression of DC-SIGN by dendritic cells of intestinal and genital mucosae in humans and rhesus macaques. J Virol 2002; 76:1866-1875.
28. Cavarelli M, Foglieni C, Rescigno M, Scarlatti G: R5 HIV-1 envelope attracts dendritic cells to cross the human intestinal epithelium and sample luminal virions via engagement of the CCR5. EMBO Mol Med 2013; 5:776-794.
29. Li L, Meng G, Graham MF, Shaw GM, Smith PD: Intestinal macrophages display reduced permissiveness to human immunodeficiency virus 1 and decreased surface CCR5. Gastroenterology 1999; 116:1043-1053.
30. Shen R, Meng G, Ochsenbauer C, Clapham PR, Grams J, Novak L, Kappes JC, Smythies LE, Smith PD: Stromal down-regulation of macrophage CD4/CCR5 expression and NF-kappaB activation mediates HIV-1 non-permissiveness in intestinal macrophages. PLoS Pathog 2011; 7:e1002060.
31. McElrath MJ, Smythe K, Randolph-Habecker J, Melton KR, Goodpaster TA, Hughes SM, Mack M, Sato A, Diaz G, Steinbach G, Novak RM, Curlin ME, Lord JD, Maenza J, Duerr A, Frahm N, Hladik F: Comprehensive assessment of HIV target cells in the distal human gut suggests increasing HIV susceptibility toward the anus. J Acquir Immune Defic Syndr 2013; 63:263-271.
32. Madara JL, Nash S, Moore R, Atisook K: Structure and function of the intestinal epithelial barrier in health and disease. Monogr Pathol 1990; 31:306-324.
33. Carias AM, McCoombe S, McRaven M, Anderson M, Galloway N, Vandergrift N, Fought AJ, Lurain J, Duplantis M, Veazey RS, Hope TJ: Defining the interaction of HIV-1 with the mucosal barriers of the female reproductive tract. J Virol 2013; 87:11388-11400.
34. Shukair SA, Allen SA, Cianci GC, Stieh DJ, Anderson MR, Baig SM, Gioia CJ, Spongberg EJ, Kauffman SM, McRaven MD, Lakougna HY, Hammond C, Kiser PF, Hope TJ: Human cervicovaginal mucus contains an activity that hinders HIV-1 movement. Mucosal Immunol 2013; 6:427-434.
35. Ito S: Form and function of the glycocalyx on free cell surfaces. Philos Trans R Soc Lond B Biol Sci 1974; 268:55-66.
36. Maury J, Nicoletti C, Guzzo-Chambraud L, Maroux S: The filamentous brush border glycocalyx, a mucin-like marker of enterocyte hyper-polarization. Eur J Biochem 1995; 228:323-331.
37. Shattock RJ, Moore JP: Inhibiting sexual transmission of HIV-1 infection. Nat Rev Microbiol 2003; 1:25-34.
38. Surawicz CM, Goodell SE, Quinn TC, Roberts PL, Corey L, Holmes KK, Schuffler MD, Stamm WE: Spectrum of rectal biopsy abnormalities in homosexual men with intestinal symptoms. Gastroenterology 1986; 91:651-659.
39. Miller CJ, Alexander NJ, Sutjipto S, Joye SM, Hendrickx AG, Jennings M, Marx PA: Effect of virus dose and nonoxynol-9 on the genital transmission of SIV in rhesus macaques. J Med Primatol 1990; 19:401-409.
40. Miller CJ, Alexander NJ, Sutjipto S, Lackner AA, Gettie A, Hendrickx AG, Lowenstine LJ, Jennings M, Marx PA: Genital mucosal transmission of simian immunodeficiency virus: animal model for heterosexual transmission of human immunodeficiency virus. J Virol 1989; 63:4277-4284.
41. Brenchley JM, Douek DC: The mucosal barrier and immune activation in HIV pathogenesis. Curr Opin HIV AIDS 2008; 3:356-361.
42. Nazli A, Chan O, Dobson-Belaire WN, Ouellet M, Tremblay MJ, Gray-Owen SD, Arsenault AL, Kaushic C: Exposure to HIV-1 directly impairs mucosal epithelial barrier integrity allowing microbial translocation. PLoS Pathog 2010; 6:e1000852.
43. Nazli A, Kafka JK, Ferreira VH, Anipindi V, Mueller K, Osborne BJ, Dizzell S, Chauvin S, Mian MF, Ouellet M, Tremblay MJ, Mossman KL, Ashkar AA, Kovacs C, Bowdish DM, Snider DP, Kaul R, Kaushic C: HIV-1 gp120 induces TLR2- and TLR4-mediated innate immune activation in human female genital epithelium. J Immunol 2013; 191:4246-4258.
44. Madara JL, Stafford J: Interferon-gamma directly affects barrier function of cultured intestinal epithelial monolayers. J Clin Invest 1989; 83:724-727.
45. Schmitz H, Fromm M, Bentzel CJ, Scholz P, Detjen K, Mankertz J, Bode H, Epple HJ, Riecken EO, Schulzke JD: Tumor necrosis factor-alpha (TNFalpha) regulates the epithelial barrier in the human intestinal cell line HT-29/B6. J Cell Sci 1999; 112(Pt 1):137-146.
46. Quaranta MG, Vincentini O, Felli C, Spadaro F, Silano M, Moricoli D, Giordani L, Viora M: Exogenous HIV-1 Nef upsets the IFN-gamma-induced impairment of human intestinal epithelial integrity. PLoS ONE 2011; 6:e23442.
47. Fantini J, Cook DG, Nathanson N, Spitalnik SL, Gonzalez-Scarano F: Infection of colonic epithelial cell lines by type 1 human immunodeficiency virus is associated with cell surface expression of galactosylceramide, a potential alternative gp120 receptor. Proc Natl Acad Sci USA 1993; 90:2700-2704.
48. Adachi A, Koenig S, Gendelman HE, Daugherty D, Gattoni-Celli S, Fauci AS, Martin MA: Productive, persistent infection of human colorectal cell lines with human immunodeficiency virus. J Virol 1987; 61:209-213.
49. Bourinbaiar AS, Phillips DM: Transmission of human immunodeficiency virus from monocytes to epithelia. J Acquir Immune Defic Syndr 1991; 4:56-63.
50. Fox CH, Kotler D, Tierney A, Wilson CS, Fauci AS: Detection of HIV-1 RNA in the lamina propria of patients with AIDS and gastrointestinal disease. J Infect Dis 1989; 159:467-471.
51. Stahl-Hennig C, Steinman RM, Tenner-Racz K, Pope M, Stolte N, Matz-Rensing K, Grobschupff G, Raschdorff B, Hunsmann G, Racz P: Rapid infection of oral mucosal-associated lymphoid tissue with simian immunodeficiency virus. Science 1999; 285:1261-1265.
52. Tugizov SM, Herrera R, Veluppillai P, Greenspan D, Soros V, Greene WC, Levy JA, Palefsky JM: HIV is inactivated after transepithelial migration via adult oral epithelial cells but not fetal epithelial cells. Virology 2011; 409:211-222.
53. Bomsel M: Transcytosis of infectious human immunodeficiency virus across a tight human epithelial cell line barrier. Nat Med 1997; 3:42-47.
54. Meng G, Wei X, Wu X, Sellers MT, Decker JM, Moldoveanu Z, Orenstein JM, Graham MF, Kappes JC, Mestecky J, Shaw GM, Smith PD: Primary intestinal epithelial cells selectively transfer R5 HIV-1 to CCR5 + cells. Nat Med 2002; 8:150-156.
55. Lore K, Larsson M: The role of dendritic cells in the pathogenesis of HIV-1 infection. APMIS 2003; 111:776-788.
56. Wu L, KewalRamani VN: Dendritic-cell interactions with HIV: infection and viral dissemination. Nat Rev Immunol 2006; 6:859-868.
57. Hladik F, Sakchalathorn P, Ballweber L, Lentz G, Fialkow M, Eschenbach D, McElrath MJ: Initial events in establishing vaginal entry and infection by human immunodeficiency virus type-1. Immunity 2007; 26:257-270.
58. Miller CJ, Shattock RJ: Target cells in vaginal HIV transmission. Microbes Infect 2003; 5:59-67.
59. Hladik F, McElrath MJ: Setting the stage: host invasion by HIV. Nat Rev Immunol 2008; 8:447-457.