Immunophenotypic characterization of simian immunodeficiency virus- infected dendritic cells in cervix, vagina, and draining lymph nodes of rhesus monkeys

Laboratory Investigation

Volumn 78, Issue 4, 1998, Pages 435-451

  Hu, Jinjie ^a   Pope, Melissa ^c   Brown, Charles ^d   O'Doherty, Una ^e   Miller, Christopher J ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^e HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS RNA;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; DENDRITIC CELL; FEMALE GENITAL TRACT INFECTION; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOPHENOTYPING; IN SITU HYBRIDIZATION; LANGERHANS CELL; LYMPH NODE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SEXUALLY TRANSMITTED DISEASE; SIMIAN IMMUNODEFICIENCY VIRUS; T LYMPHOCYTE; UTERINE CERVIX; VAGINA; VIRUS DETECTION; VIRUS INFECTION; VIRUS REPLICATION;

ANIMALS; CERVIX UTERI; DENDRITIC CELLS; DNA, VIRAL; FEMALE; IMMUNOPHENOTYPING; LYMPH NODES; MACACA MULATTA; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VAGINA;

EID: 0031957662     PISSN: 00236837     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (66)

1. Austyn JM, Kupiec-Weglinski JW, Hankins DF, and Morris PJ (1988). Migration patterns of dendritic cells in the mouse: Homing to T cell-dependent areas of spleen, and binding within marginal zone. J Exp Med 167:646-651.
2. Ayehunie S, Groves RW, Bruzzese AM, Ruprecht RM, Kupper TS, and Langhoff E (1995). Acutely infected Langerhans cells are more efficient than T cells in disseminating HIV type 1 to activated T cells following a short cell-cell contact. AIDS Res Hum Retroviruses 11:877-884.
3. Berger RS, Gartner S, Rappersberger K, Foster CA, Wolff K, and Stingl G (1992). Isolation of human immunodeficiency virus type 1 from human epidermis: Virus replication and transmission studies. J Invest Dermatol 99:271-277.
4. Birbeck MS, Breathnach AS, and Everall JD (1961). An electron microscope study of basal melanocytes and high-level clear cells (Langerhans cells) in vitiligo. J Invest Dermatol 37:51-64.
5. Bjercke S, Scott H, Braathen LR, and Thorsby E (1983). HLA-DR-expressing Langerhans-like cells in vaginal and cervical epithelium. Acta Obstet Gynecol Scand 62:585-589.
6. Blauvelt A, Asada H, Seville MW, Klaus-Kovuton V, Altman DJ, Yarchoan R, and Katz SI (1997). Productive infection of dendritic cells by HIV-1 and their abiltiy to capture virus are mediated by separate pathways. J Clin Invest 100:2043-2053.
7. Daniels TE (1984). Human mucosal Langerhans cells: Post-mortem identification of regional variations in oral mucosa. J Invest Dermatol 82:21-24.
8. Desrosiers RC and Letvin NL (1987). Animal models for acquired immunodeficiency syndrome. Rev Infect Dis 9:438-446.
9. Edwards JNT and Morris HB (1985). Langerhans cells and lymphocyte subsets in the female genital tract. Br J Obstet Gynaecol 92:974-982.
10. Embretson J, Zupancic M, Ribas JL, Burke A, Racz P, Tenner-Racz K, and Haase AT (1993). Massive covert infection of helper T lymphocytes and macrophages by HIV during the incubation period of AIDS. Nature 362:359-362.
11. Fithian E, Kung P, Goldstein G, Rubenfeld M, Fenoglio C, and Edelson R (1988). Reactivity of Langerhans cells with hybridoma antibody. Proc Natl Acad Sci U S A 78:2541-2544.
12. Grouard G, Durand I, Filgueira L, Banchereau J, and Liu YJ (1996). Dendritic cells capable of stimulating T cells in germinal centres. Nature 384:364-367.
13. Hackemann M, Grubb C, and Hill KR (1968). The ultrastructure of normal squamous epithelium of the human cervix uteri. J Ultrastruct Res 22:443-457.
14. Hendrickx AG and Cukierski MA (1987). Reproductive and developmental toxicology in nonhuman primates. In: Graham CR, editor: Preclinical safety of biotechnology products intended for human use. New York: Alan R. Liss, Inc., 73-88.
15. Hirsch V, Martin J, Lawson M, and Brown C (1995). Induction of AIDS by simian immunodeficiency virus from an African Green monkey: Species-specific variation in pathogenicity correlates with extent of in vivo replication. J Virol 69:955-967.
16. Hirsch V, Riedel N, and Mullins JI (1987). The genome organization of STLV-3 is similar to that of the AIDS virus except for a truncated transmembrane protein. Cell 49:307-319.
17. sm) closely related to HIV-2. Nature 339:389-392.
18. Hoefsmit ECM, Duijvestijn AM, and Kamperdijk EWA (1982). Relation between Langerhans cells, veiled cells, and interdigitating cells, Immunobiology 161:255-265.
19. Hoxie JA, Haggarty BS, Bonser SE, Rackowski JL, Shan H, and Kanki PJ (1988). Biological characterization of a simian immunodeficiency virus-like retrovirus (HTLV-iv): Evidence for CD4-associated molecules required for infection. J Virol 62:2557-2568.
20. Kraal G, Breel M, Janse M, and Bruin G (1986). Langerhans cells, vieled cells and interdigitating cells in the mouse recognized by a monoclonal antibody. J Exp Med 163:981-997.
21. Kripke ML, Munn CG, Jeevan A, Tang J-M, and Bucana C (1990). Evidence that cutaneous antigen-presenting cells migrate to regional lymph nodes during contact sensitization. J Immunol 145:2833-2837.
22. Kupiec-Weglinski J, Austyn J, and Morris P (1988). Migration patterns of dendritic cells in the mouse: Traffic from the blood, and T-cell-dependent and independent entry into lymphoid tissue. J Exp Med 167:632-645.
23. Langerhans P (1868). Uber die nerven der menschlichen haut. Virchows Arch Pathol Anat 44:325-337.
24. Lenz A, Heine M, Schuler G, and Romani N (1993). Human and murine dermis contain dendritic cells: Isolation by means of a novel method and phenotypical and functional characterization. J Clin Invest 92:2587-2596.
25. Lohman B, Higgins J, Marthas M, Marx P, and Pedersen N (1991). Development of simian immunodeficiency virus isolation, titration, and neutralization assays which use whole blood from rhesus monkeys and an antigen capture enzyme-linked immunosorbent assay. J Clin Microbiol 29:2187-2192.
26. Lu Y, Brosio PB, Lafaile M, Li J, Collman RG, Sodroski J, and Miller CJ (1996). Vaginal transmission of chimeric simian/ human immunodeficiency viruses in rhesus macaques. J Virol 70:3045-3050.
27. Ludewig B, Gelderblom HR, Becker Y, Schafer A, and Pauli G (1996). Transmission of HIV-1 from productively infected mature Langerhans cells to primary CD4+ lymphocytes results in altered T cell responses with enhanced production of IFN-γ and IL-10. Virology 215:51-60.
28. Marthas ML, Banapour B, Sutjipto S, Siegel ME, Marx PA, Gardner MB, Pedersen NC, and Luciw PA (1989). Rhesus macaques inoculated with molecularly cloned simian immunodeficiency virus. J Med Primatol 18:311-319.
29. Marthas ML, Ramos RA, Lohman BL, Van Rompay KKA, Unger RE, Miller CJ, Banapour B, Pedersen NC, and Luciw PA (1993). Viral determinants of simian immunodeficiency (SIV) virulence in rhesus macaques assessed by using attenuated and pathogenic molecular clones of SIVmac. J Virol 67:6047-6055.
30. Miller CJ (1994). Mucosal transmission of SIV. In: Desrosiers RC and Letvin NL, editors: Current topics in microbiology and immunology. Berlin: Springer-Verlag, 107-122.
31. Miller CJ, Alexander NJ, Sutjipto S, Hendrickx AG, Jennings M, and Marx PA (1990). Effect of virus dose and nonoxynol-9 on the genital transmission of SIV in rhesus macaques. J Med Primatol 19:401-409.
32. Miller CJ, Alexander NJ, Sutjipto S, Lackner AA, Hendrickx AG, Gettie A, Lowenstine LJ, Jennings M, and Marx PA (1989). Genital mucosal transmission of simian immunodeficiency virus: Animal model for heterosexual transmission of human immunodeficiency virus. J Virol 63:4277-4284.
33. Miller CJ, Alexander NJ, Vogel P, Anderson J, and Marx PA (1992a). Mechanism of genital transmission of SIV: A hypothesis based on transmission studies and the location of SIV in the genital tract of chronically infected female rhesus macaques. J Med Primatol 21:64-68.
34. Miller CJ, Marthas M, Torten J, Alexander NJ, Moore JP, Doncel GF, and Hendrickx AG (1994). Intravaginal inoculation of rhesus macaques with cell-free simian immunodeficiency virus results in persistent or transient viremia. J Virol 68: 6391-6400.
35. Miller CJ, McChesney M, and Moore PF (1992b). Langerhans cells, macrophages and lymphocyte subsets in the cervix and vagina of rhesus macaques. Lab Invest 67:628-634.
36. Miller CJ, McChesney MB, Lü XS, Dailey PJ, Chutkowski C, Lu D, Brosio P, Roberts B, and Lu Y (1997). Rhesus macaques previously-infected with SHIV are protected from vaginal challenge with pathogenic SIVmac239. J Virol 71: 1911-1921.
37. Miller CJ, McGhee JR, and Gardner MB (1992c). Mucosal immunity, HIV transmission and AIDS. Lab Invest 68-129-145.
38. Miller CJ, Vogel P, Alexander NJ, Sutjipto S, Hendrickx AG, and Marx PA (1992d). Localization of SIV in the genital tract of chronically infected female rhesus macaques. Am J Pathol 141:655-660.
39. Morris HHB, Gatter KC, Stein H, and Mason DY (1983). Langerhans cells in human cervical epithelium: An immunohistologic study. Br J Obstet Gynaecol 90:400-411.
40. Mosialos G, Birkenback M, Ayehunie S, Matsumura F, Pinkus GS, Kieff E, and Langhoff E (1996). Circulating human dendritic cells differentially express high levels of a 55-kd actin-budling protein. Am J Pathol 148:593-600.
41. Nestle FO, Zheng X-G, Thompson CB, Turka LA, and Nickoloff BJ (1993). Characterization of dermal dendritic cells obtained from normal human skin reveals phenotypic and functionally distinctive subsets. J Immunol 151:6535-6545.
42. Pantaleo G, Graziosi C, Butini L, Pizzo P, Schnittman S, Kotler D, and Fauci A (1991). Lymphoid organs function as major resevoirs for human immunodeficiency virus. Proc Natl Acad Sci U S A 88:9838-9842.
43. Parr MB, Kepple L, and Parr EL (1991). Antigen recognition in the female reproductive tract: II - Endocytosis of horseradish peroxidase by Langerhans cells in murine vaginal epithelium. Biol Reprod 45:261-265.
44. Peterman TA and Curran JW (1988a). Sexual transmission of human immunodeficiency virus. J Am Med Assoc 256:2222-2226.
45. Peterman TA, Stoneburner RL, Allen JR, Jaffe HW, and Curran JW (1988b). Risk of human immunodeficiency virus from heterosexual adults with transfusion associated infections. J Am Med Assoc 259:55-58.
46. Pomerantz RJ, de la Monte SM, Donegan CE, Rota TR, Vogt MW, Craven DE, and Hirsch MS (1988). Human immunodeficiency virus (HIV) infection of the uterine cervix. Ann Intern Med 108:321-327.
47. Pope M, Betjes MGH, Hirmand H, Hoffman L, and Steinman RM (1995a). Both dendritic cells and memory T lympocytes emigrate from organ cultures of human skin and form distinctive dendritic-T cell conjugates. J Invest Dermatol 104: 11-17.
48. Pope M, Betjes MGH, Romani N, Cameron PU, Hoffman L, Gezelter S, Schuler G, and Steinman RM (1994). Conjugates of dendritic cells and memory T lymphocytes from skin facilitate productive infection with HIV-1. Cell 78:389-398.
49. Pope M, Elmore D, Ho D, and Marx P (1997a). Dendritic cell-T cell mixtures, isolated from the skin and mucosae of macaques, support the replication of SIV. AIDS Res Hum Retroviruses 13:819-827.
50. Pope M, Frankel SS, Mascola JR, Trkola A, Isdell F, Birx DL, Ho DD, and Moore JP (1997b). Human immunodeficiency virus type 1 strains of subtype B and E replicate in cutaneous dendritic cell-T-cell mixtures without displaying subtype-specific tropism. J Virol 71:8001-8007.
51. Pope M, Gezelter S, Gallo N, Hoffman L, and Steinman RM (1995b). Low levels of HIV-1 infection in cutaneous dendritic cells promote extensive viral replication upon binding to memory CD4+ T cells. J Exp Med 182:2045-2056.
52. Ramazzotti E, Marconi A, Re MC, Girolomoni G, Cenacchi G, Vignoli M, Zambruno G, Furlini G, Placa ML, and Giannetti A (1995). In vitro infection of human epidermal Langerhans' cells with HIV-1. Immunology 85:94-98.
53. Reed LJ and Muench H (1938). A simple method of estimating fifty percent endpoints. Am J Hyg 27:493-497.
54. Roncalli M, Sideri M, Gie P, and Servida E (1988). Immunophenotypic analysis of the transformation zone of human cervix. Lab Invest 58:141-149.
55. Shelley W and Juhlin L (1976). Langerhans cells form a reticuloepithelial trap for external contact allergens. Nature 261:46-47.
56. Shelley W and Juhlin L (1977). Selective uptake of contact allergens by the Langerhans cell. Arch Dermatol 113:187-192.
57. Silberberg-Sinakin I, Thorbecke GJ, Baer RL, Rosenthal SA, and Berezowsky V (1976). Antigen-bearing Langerhans cells in skin, dermal lymphatics and in lymph nodes. Cell Immunol 25:137-151.
58. Soto-Ramirez LE, Renjifo B, McLane MF, Marlink R, O'Hara C, Sutthent R, Wasi C, Vithayasi P, Vithayasi V, Apichartpiyakul C, Auewarakul P, Pena Cruz V, Chui D-S, Osathanondh R, Mayer K, Lee T-H, and Essex M (1996). HIV-1 Langerhans cell tropism associated with heterosexual transmission of HIV. Science 271:1291-1293.
59. Spira AI, Marx PA, Patterson BK, Mahoney J, Koup RA, Wolinsky SM, and Ho DD (1996). Cellular targets of infection and route of viral dissemination after an intravaginal inoculation of simian immunodeficiency virus into rhesus macaques. J Exp Med 183:215-225.
60. Steinman RM (1991). The dendritic cell system and its role in immunogenicity. In: Paul WE, Fatham CG, and Metzger H, editors: Annual review of immunology. Palo Alto: Annual Reviews Inc., 271-296.
61. Unger RE, Marthas ML, Lackner AA, Pratt-Lowe E, Lohman BL, Van Rompay K, and Luciw PA (1992). Detection of simian immunodeficiency virus DNA in macrophages from infected rhesus macaques. J Med Primatol 21:74-81.
62. Williams PL and Warwick R (1980). Lymphatic drainage of the female reproductive organs. In: Williams PL and Warwick R, editors: Gray's Anatomy, 36th Br. ed. Philadelphia: W.B. Saunders Co., 798.
63. Wolff K (1967). The fine structure of the Langerhans cell granule. J Cell Biol 35:468-473.
64. Yamashiro-Matsumura S and Matsumura F (1985). Purification and characterization of an F-actin-bundling 55-kilodalton protein from HeLa cells. Biol Chem 260:5087-5097.
65. Yamashiro-Matsumura S and Matsumura F (1986). Modulation of actin-bundling activity of 55-kDa protein by multiple isoforms of tropomyosin. J Biol Chem 261:4655-4659.
66. Younes MS, Robertson EM, and Bencosme SA (1968). Electron microscope observations on Langerhans cells in the cervix. Am J Obstet Gynecol 102:397-403.