The feline immunodeficiency virus-infected cat: A model for lentivirus-induced placental immunopathology and reproductive failure (mini-review)

American Journal of Reproductive Immunology

Volumn 54, Issue 4, 2005, Pages 169-185

  Coats, Karen S ^a  

^a MISSISSIPPI STATE UNIVERSITY   (United States)

Author keywords

Feline immunodeficiency virus; HIV animal model; Placental immunopathology

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 1BETA;

CAT DISEASE; CESAREAN SECTION; CLINICAL FEATURE; FELINE IMMUNODEFICIENCY VIRUS; FEMALE; FETUS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOPATHOLOGY; LITTER SIZE; NONHUMAN; PLACENTA DISORDER; PLACENTAL TRANSFER; POLYMERASE CHAIN REACTION; PREGNANCY DISORDER; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SPONTANEOUS ABORTION; TH1 CELL; TH2 CELL; VERTICAL TRANSMISSION; VIRUS DETECTION; VIRUS INFECTION; VIRUS PATHOGENESIS;

ANIMALS; CATS; DISEASE MODELS, ANIMAL; FEMALE; FETAL DEATH; HUMANS; IMMUNODEFICIENCY VIRUS, FELINE; LENTIVIRUS INFECTIONS; PLACENTA; PREGNANCY; PREGNANCY COMPLICATIONS, INFECTIOUS; PREGNANCY, ANIMAL;

EID: 24944464305     PISSN: 10467408     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-0897.2005.00296.x     Document Type: Review

References (137)

1. AIDS Epidemic Update: December 2004: UNAIDS Joint United Nations Programme on HIV/AIDS. Accessed December 14, 2004, http://www.unaids.org/wad2004/report.html.
2. Mother to Child Transmission: HIV/AIDS UNICEF Statistics. Accessed December 6, 2004, http://www.childinfo.org/eddb/hiv_aids/mtct.htm.
3. HIV AIDS Surveillance Report Cases of HIV infections and AIDS in the United States, 2003. Centers for Disease Control and Prevention. Accessed December 14, 2004, http://www.cdc.gov/hiv/STATS/2003SurveillanceReport.pdf
4. NIAID Division of AIDS General Info. 2004: Accessed December 14, 2004, http://www.niaid.nih.gov/daids.
5. Langston C, Lewis DE, Hammill HA, Popek EJ, Kozinetz CA, Kline MW, Hanson IC, Shearer WT: Excess intrauterine fetal demise associated with maternal human immunodeficiency virus infection. J Infect Dis 1995; 172:1451-1460.
6. D'Ubaldo C, Pezzotti P, Rezza G, Branca M, Ippolito G: Association between HIV-1 infection and miscarriage: a retrospective study. DIANAIDS Collaborative Study Group. Diagnosi Iniziale Anomalie Neoplastiche AIDS. AIDS 1998; 2:1087-1093.
7. Kumar RM, Uduman SA, Khurranna AK: Impact of maternal HIV-1 infection on perinatal outcome. Int J Gynaecol Obstet 1995; 49:137-143.
8. Bendinelli M, Pistello M, Lombardi S, Poli A, Garzelli C, Matteucci D, Ceccherini-Nelli L, Malvaldi G, Tozzini F: Feline immunodeficiency virus: an interesting model for AIDS studies and an important cat pathogen. Clin Microbiol Rev 1995; 8:87-112.
9. Willett BJ, Flynn N, Hosie MJ: FIV infection of the domestic cat: an animal model for AIDS. Immunol Today 1997; 18:182-189.
10. Brown WC, Bissey L, Logan KS, Pedersen NC, Elder JH, Collison EW: Feline immunodeficiency virus infects both CD4+ and CD8+ T lymphocytes. J Virol 1991; 65:3359-3364.
11. Brunner D, Pedersen NC: Infection of peritoneal macrohages in vitro and in vivo with feline immunodeficiency virus. J Virol 1989; 63:5483-5488.
12. English RV, Johnson CM, Gebhard DH, Tompkins MB: In vivo lymphocyte tropism of feline immunodeficiency virus. J Virol 1993; 67:5175-5186.
13. Dow SW, Dreitz MJ, Hoover EA: Feline immunodeficiency virus neurotropism: evidence that astrocytes and microglia are the primary target cells. Vet Immunol Immunopathol 1992; 35:23-35.
14. Shimojima M, Miyazawa T, Ikeda Y, McMonagle EL, Haining H, Akashi H, Takeuchi Y, Hosie MJ, Willett BJ: Use of CD134 as a primary receptor by the feline immunodeficiency virus. Science 2004; 303:1192-1195.
15. de Parseval A, Chatterji U, Sun P, Elder JH: Feline immunodeficiency virus targets activated CD4+ T cells by using CD134 as a binding receptor. Proc Natl Acad Sci USA 2004; 101:13044-13049.
16. de Parseval A, Ngo S, Sun P, Elder JH: Factors that increase the effective concentration of CXCR4 dictate feline immunodeficiency virus tropism and kinetics of replication. J Virol 2004; 78:9132-9143.
17. de Parseval A, Ngo S, Sun P, Elder JH, Lee B: Specific interaction of feline immunodeficiency virus surface glycoprotein with human DC-SIGN. J Virol 2004; 78:2597-2600.
18. Richardson J, Pancino G, Merat R, Leste-Lasserre T, Moraillon A, Schneider-Mergener J, Alizon M, Sonigo P, Heveker N: Shared usage of the chemokine receptor CXCR4 by primary and laboratory-adapted strains of feline immunodeficiency virus. J Virol 1999; 73:3661-3671.
19. Willett BJ, Picard L, Hosie MJ, Turner JD, Adema K, Clapham PR: Shared usage of the chemokine receptor CXCR4 by the feline and human immunodeficiency virus. J Virol 1997; 71:6407-6415.
20. Willett BJ, Cannon CA, Hosie MJ: Upregulation of surface feline CXCR4 expression following ectopic expression of CCR5: implications for studies of the cell tropism of feline immunodeficiency virus. J Virol 2002; 76:9242-9252.
21. Winkler IG, L'chelt M, Flower RLP: Epidemiology of feline foamy virus and feline immunodeficiency virus infections in domestic and feral cats: a seroepidemiological study. J Clin Microbiol 1999; 37:2848-2851.
22. Jordan HL, Howard J, Barr MC, Kennedy-Stoskopf S, Levy JK, Tompkins WA: Feline immunodeficiency virus is shed in semen from experimentally and naturally infected cats. AIDS Res Human Retroviruses 1998; 14:1087-1092.
23. Jordan HL, Liang Y, Hudson LC, Tompkins WA: Shedding of feline immunodeficiency virus in semen of domestic cats during acute infection. Am J Vet Res 1999; 60:211-215.
24. Jordan HL, Howard JG, Bucci JG, Butterworth JL, English R, Kennedy-Stoskopf S, Tompkins MB, Tompkins WA: Horizontal transmission of feline immunodeficiency virus with semen from seropositive cats. J Reprod Immunol 1998; 41:341-357.
25. Bishop SA, Stokes CR, Gruffydd-Jones TJ, Whiting CV, Harbour DA: Vaginal and rectal infection of cats with feline immunodeficiency virus. Vet Microbiol 1996; 51:217-227.
26. Burkhard MJ, Obert LA, O'Neil LL, Diehl LJ, Hoover EA: Mucosal transmission of cell-associated and cell-free feline immunodeficiency virus. AIDS Res Hum Retroviruses 1997; 13:347-355.
27. Callanan JJ, Hosie MUJ, Jarrett O: Transmission of feline immunodeficiency virus from mother to kitten. Vet Rec 1991; 128:332-333.
28. Ueland K, Nesse LL: No evidence of vertical transmission of naturally acquired feline immunodeficiency virus. Vet Immunol Immunopathol 1992; 33:301-308.
29. Carpenter MA, Brown EW, Culver M, Johnson WE, Pecon-Slattery J, Brousset D, O'Brien SJ: Genetic and phylogenetic divergence of feline immunodeficiency virus in the puma (Puma concolor). J Virol 1996; 70:6682-6693.
30. Wasmoen T, Armiger-Luhman S, Egan C, Hall V, Chu H-J, Chavez L, Acree W: Transmission of feline immunodeficiency virus from infected queens to kittens. Vet Immunol Immunopathol 1992; 35:83-93.
31. O'Neil LL, Burkhard MJ, Hoover EA: Frequent perinatal transmission of feline immunodeficiency virus by chronically infected cats. J Virol 1996; 70:2894-2901.
32. O'Neil LL, Burkhard MJ, Diehl LJ, Hoover EA: Vertical transmission of feline immunodeficiency virus. AIDS Res Hum Retroviruses 1995; 11:171-182.
33. Rogers AB, Hoover EA: Maternal-fetal feline immunodeficiency virus transmission: timing and tissue tropisms. J Infect Dis 1998; 178:960-967.
34. Rogers AB, Hoover EA: Fetal feline immunodeficiency virus is prevalent and occult. J Infect Dis 2002; 186:895-904.
35. Allison RW, Hoover EA: Covert vertical transmission of feline immunodeficiency virus. AIDS Res Hum Retroviruses 2003; 19:421-434.
36. Weaver CC, Burgess SC, Nelson PD, Wilkinson M, Ryan PL, Nail CA, Kelly-Quagliana KA, May ML, Reeves RK, Boyle CR, Coats KS: Placental immunopathology and pregnancy failure in the FIV-infected cat. Placenta 2005; 26:138-147.
37. Javaherian K, Langlois AJ, McDanal C, Ross KL, Eckler LI, Jellis CL, Profy AT, Rusche JR, Bolognesi DP, Putney SK, Matthews TJ: Principal neutralizing domain of the human immunodeficiency virus type 1 envelope protein. Proc Natl Acad Sci USA 1989; 86:6768-6772.
38. Cann AJ, Churcher MJ, Boyd M, O'Brien W, Zhao J-Q, Zack J, Chen ISY: The region of the envelope gene of human immunodeficiency virus type 1 responsible for determination of cell tropism. J Virol 1992; 66:305-309.
39. Chesebro B, Nisihio J, Perryman S, Cann A, O'Brien W, Chen ISY, Wehrly K: Identification of human immunodeficiency virus envelope gene sequences influencing viral entry into CD4-positive HeLa cells, T-leukemia cells, and macrophages. J Virol 1991; 65:5782-5789.
40. Chesebro B, Wehrly K, Nishio J, Perryman S: Mapping of independent V3 determinants of human immunodeficiency virus type 1 macrophage tropism and syncytium formation in lymphocytes. J Virol 1996; 70:9055-9059.
41. Hwang SS, Boyle TJ, Lyerly KH, Cullen BR: Identification of the envelope V3 loop as the primary determinant of cell tropism in HIV-1. Science 1991; 253:1590-1593.
42. Verrier F, Borman AM, Brand, Girard M: Role of the HIV type 1 glycoprotein 120 V3 loop in determining coreceptor usage. AIDS Res Hum Retroviruses 1999; 15:731-743.
43. Menu E, M'bopi-Keou FX, Lagaye S, Pissard S, Mauclere P, Scarlatti G, Martin J, Goossens M, Chaouat G, Barre-Sinoussi F: Selection of maternal HIV-1 variants in human placenta. European Network for In Utero Transmission of HIV-1. J Infect Dis 1999; 179:44-51.
44. Matala E, Hahn T, Yedavalli VR, Ahmad N: Biological characterization of HIV type 1 envelope V3 regions from mothers and infants associated with perinatal transmission. AIDS Res Hum Retroviruses 2001; 17:1725-1735.
45. Amedee AM, Lacour N, Gierman JL, Martin LN, Clements JE, Bohm R Jr, Harrison RM, Murphey-Corb M: Genotypic selection of simian immunodeficiency virus in macaque infants infected transplacentally. J Virol 1995; 69:7982-7990.
46. Pancino G, Fossati I, Chappey C, Castelot S, Hurtrel B, Moraillon A, Klatzmann D, Sonigo P: Structure and variations of feline immunodeficiency virus envelope glycoproteins. Virology 1993; 192:659-662.
47. Lombardi S, Garzelli C, La Rosa C, Zaccaro L, Specter S, Malvaldi G, Tozzini F, Esposito F, Bendinelli M: Identification of a linear neutralization site within the third variable region of feline immunodeficiency virus envelope. J Virol 1993; 67:4742-4749.
48. de Ronde A, Stam JG, Boers P, Langedijk H, Meloen R, Hesselink W, Keldermans CEJM, Van Vliet ALW, Verschoor EJ, Horzinek MC, Egberink HF: Antibody response in cats to the envelope proteins of feline immunodeficiency virus: identification of an immunodominant neutralization domain. Virology 1994; 198:257-264.
49. Johnston JB, Power C: Feline immunodeficiency virus xenoinfection: the role of chemokine receptors and envelope diversity. J Virol 2002; 76:3626-3636.
50. Vahlenkamp TW, de Ronde A, Schuurman NN, Van Vliet AL, Van Drunen J, Horzinek MC, Egberink HF: Envelope gene sequences encoding variable regions 3 and 4 are involved in macrophage tropism of feline immunodeficiency virus. J Gen Virol 1999; 80:2639-2646.
51. Vahlenkamp TW, Verschoor EJ, Schuurman NNMP, Van Vliet ALW, Horzinek MC, Egberink HF, De Rond A: A single amino acid substitution in the transmembrane envelope glycoprotein of feline immunodeficiency virus alter cellular tropism. J Virol 1997; 71:7132-7135.
52. Greene WK, Meers J, del Fierro G, Carnegie PR, Robinson WF: Extensive sequence variation of feline immunodeficiency virus env genes in isolates from naturally infected cats. Arch Virol 1993; 133:51-62.
53. Ikeda Y, Miyazawa T, Nishimura Y, Nakamura K, Tohya Y, Mikami T: High genetic stability of TM1 and TM2 strains of subtype B feline immunodeficiency virus in long-term infection. J Vet Med Sci 2004; 66:287-289.
54. Motokawa K, Hohdatsu T, Imori A, Arai S, Koyama H: Mutations in feline immunodeficiency (FIV) virus envelope gene V3-V5 regions in FIV-infected cats. Vet Microbiol 2005; 106:33-40.
55. Brossard Y, Aubin JT, Mandelbrot L, Bognozzi C, Brand D, Chaput A, Roume J, Mulliez N, Mallet F, Agut H: Frequency of early in utero HIV-1 infection: a blind DNA polymerase chain reaction study on 100 fetal thymuses. AIDS 1995; 9:359-366.
56. Chouquet C, Richardson S, Burgard M, Blanche S, Mayaux MJ, Rouzio C, Costagliola D: Timing of human immunodeficiency virus type 1 (HIV-1) transmission from mother to child: bayesian estimation using a mixture. Stat Med 1999; 18:815-833.
57. Ehrnst A, Lindgren S, Dictor M, Johansson B, Sonnerborg A, Czajkows J, Sundin G, Bohlin AB: HIV in pregnant women and their offspring: evidence for late transmission. Lancet 1991; 338:203-207.
58. Lewis SH, Reynolds-Kohler C, Fox HE, Nelson JA: HIV-1 in trophoblastic and villous Hofbauer cells, and haematological precursors in eight-week fetuses. Lancet 1990; 335:565-568.
59. Courgnaud V, Laure F, Brossard A, Bignozzi C, Goudeau A, Barin F, Brechot C: Frequent and early in utero HIV-1 infection. AIDS Res Hum Retroviruses 1991; 7:337-341.
60. Goldstein PJ, Smit R, Stevens M, Sever JL: Association between HIV in pregnancy and antiretroviral thrapy including protease inhibitors and low birth weight infants. Infect Dis Obstet Gynecol 2000; 8:94-98.
61. Anderson V, Carneiro M, Bulterys M, Douglas G, Polliotti B, Slikker W Jr: HIV in pregnancy. Perinatal infections: HIV and co-infections in the placenta and therapeutic interventions- a workshop report. Placenta 2001; 22(Suppl. A), Trophoblast Research 15:S34-S37.
62. Cohen D: Perinatal HIV: special considerations. Topics HIV Med 2003; 11:200-213.
63. Massad LS, Springer G, Jacobson L, Watts H, Anastos K, Korn A, Cejti H, Stek A, Young M, Schmidt J, Minkoff H: Pregnancy rates and predictors of conception, miscarriage, and abortion in US women with HIV. AIDS 2004; 18:281-286.
64. Weetman AP: The immunology of pregnancy. Thyroid 1999; 9:643-646.
65. Denison FC, Kelly RW, Calder AA, Riley SC: Cytokine secretion by human fetal membranes, decidua and placenta at term. Hum Reprod 1998; 13:3560-3565.
66. Ben-Rafael Z, Orvieto R: Cytokines-involvement in reproduction. Fertil Steril 1992; 58:1093-1099.
67. Mitchell MD, Trautman MS, Dudley DJ: Cytokine networking in the placenta. Placenta 1993; 14:249-275.
68. Baergen R, Benirschke K, Ulich TR: Cytokine expression in the placenta: the role of interleukin 1 and interleukin 1 receptor antagonist expression in chorioamnionitis and parturition. Arch Pathol Lab Med 1994; 118:52-55.
69. Lin H, Mosmann TR, Guilbert L, Tuntipopipat S, Wegmann TG: Synthesis of T helper 2-type cytokines at the maternal-fetal interface. J Immunol 1993; 151:4562-4573.
70. Lim KJ, Odukoya OA, Ajjan RA, Li TC, Weetman AP, Cooke ID: Profile of cytokine mRNA expression in peri-implantation human endometrium. Mol Hum Reprod 1998; 4:77-81.
71. Lim KJ, Odukoya OA, Ajjan RA, Li TC, Weetman AP, Cooke ID: The role of t-helper cytokines in human reproduction. Fertil Steril 2000; 73:136-142.
72. H2 phenomenon? Immunol Today 1993; 14:353-356.
73. Raghupathy R: Th1-type immunity is compatible with successful pregnancy. Immunol Today 1997; 18:478-482.
74. Chaouat G, Menu E, Clark DA, Dy M, Minkowski M, Wegmann TG: Control of fetal survival in CBA X DBA/2 mice by lymphokine therapy. J Reprod Fertil 1990; 89:447-458.
75. Hill JA, Polger K, Anderson DJ: T-helper 1-type immunity to trophoblast in women with recurrent spontaneous abortion. J Am Med Assoc 1995; 273:1933-1937.
76. Marzi M, Vigano A, Trabattoni D, Villa ML, Salvaggio A, Clerici E, Clerici M: Characterization of type 1 and type 2 cytokine production profile in physiologic and pathologic human pregnancy. Clin Exp Immunol 1996; 106:127-133.
77. Chaouat G, Zourbas S, Ostojic S, Lappree-Delage G, Dubanchet S, Ledee N, Martal J: A brief review of recent data on some cytokine expressions at the materno-foetal interface which might challenge the classical Th1/Th2 dichotomy. J Reprod Immunol 2002; 53:241-256.
78. Chaouat G, Ledee-Bataille N, Dubanchet S, Zourbas S, Sandra O, Martal J: Th1/Th2 paradigm in pregnancy: paradigm lost? Int Arch Allergy Immunol 2004; 134:93-119.
79. Ostojic S, Dubanchet S, Chaouat G, Abdelkarim M, Truyens C, Capron F: Demonstration of the presence of IL-16, IL-17, and IL-18 at the murine fetomaternal interface during murine pregnancy. Am J Reprod Immunol 2003; 49:101-112.
80. Zourbas S, Dubanchet S, Martal J, Chaouat G: Localization of pro-inflammatory (IL-12, IL-15) and anti-inflammatory (IL-11, IL-13) cytokines at the foetomaternal interface during murine pregnancy. Clin Exp Immunol 2001; 126:519-528.
81. Zenclussen AC, Fest S, Busse P, Joachim R, Klapp BF, Arck PC: Questioning the Th1/Th2 paradigm in reproduction: peripheral levels of IL-12 are down-regulated in miscarriage patients. Am J Reprod Immunol 2002; 48:245-251.
82. Bates MD, Quenby S, Takakuwa K, Johnson PM, Vince GS: Aberrant cytokine production by peripheral blood mononuclear cells in recurrent pregnancy loss? Human Reprod 2002; 17:2439-2444.
83. Shearer WT, Reuben J, Lee B-N, Popek EJ, Lewis DE, Hammill HH, Hanson IC, Kline MW, Langston C: Role of placental cytokines and inflammation in vertical transmission of HIV infection. Acta Paediatr Suppl. 1997; 421:33-38.
84. Douglas GC, Fry GN, Thirkill T, Holmes E, Hakim H, Jennings M, King BF: Cell-mediated infection of human placental trophoblast with HIV in vitro. AIDS Res Hum Retroviruses 1991; 7:735-740.
85. Bourinbaiar AS, Nagorny R: Human immunodeficiency virus type 1 infection of choriocarcinoma-derived trophoblasts. Arch Virol 1993; 37:21-28.
86. McGann KA, Collman R, Kolson DL, Gonzales-Scarano F, Coukos G, Coutifaris C, Strauss JF, Nathanson N: Human immunodeficiency virus type 1 causes productive infection of macrophages in primary placental cell cultures. J Infect Dis 1994; 169:746-753.
87. Kilani RT, Chang L-J, Garcia-Lloret MI, Hemmings D, Winkler-Lowen B, Guilbert LJ: Placental trophoblasts resist infection by multiple human immunodeficiency virus (HIV) type 1 variants even with cytomegalovirus coinfection by support HIV replication after provirus transfection. J Virol 1997; 71:6359-6372.
88. Al-Harthi L, Guilbert LJ, Hoxie JA, Landay A: Trophoblasts are productively infected by CD4-independent isolate of HIV type 1. AIDS Res Hum Retroviruses 2002; 18:13-17.
89. Arias RA, Munoz LD, Munoz-Fernandez MA: Transmission of HIV-1 infection between trophoblast placental cells takes place via an LFA-1-mediated cell to cell contact. Virology 2003; 307:266-277.
90. Backe E, Jimenez E, Unger M, Schafer A, Jauniaux E, Vogel M: Demonstration of HIV-1 infected cells in human placenta by in situ hybridisation and immunostaining. J Clin Pathol 1992; 45:871-874.
91. David FJE, Autran B, Tran HC, Menu E, Raphael M, Debre P, His BL, Wegman TG, Barre-Sinoussi F, Chaouat G: Human trophoblast cells express CD4 and are permissive for productive infection with HIV-1. Clin Exp Immunol 1992; 88:10-16.
92. Lee B-N, Ordonez N, Popek EJ, Lu J-G, Helfgott A, Eriksen N, Hammill H, Kozinetz C, Doyle M, Kline M, Langston C, Shearer WT, Reuben JM: Inflammatory cytokine expression is correlated with the level of human immunodeficiency virus (HIV) transcripts in HIV-infected placental trophoblastic cells. J Virol 1997; 71:3628-3635.
93. Lewis SH, Reynolds-Kohler C, Fox HE, Nelson JA: HIV-1 in trophoblastic and villous Hofbauer cells, and haematological precursors in eight-week fetuses. Lancet 1990; 335:565-568.
94. Zachar V, Fink T, Koppelhus U, Ebbesen P: Role of placental cytokines in transcriptional modulation of HIV type 1 in the isolated trophoblast. AIDS Res Hum Retroviruses 2002; 18:839-847.
95. Vidricaire G, Imbeault M, Tramblay MJ: Endocytic host cell machinery plays a dominant role in intracellular trafficking of incoming human immunodeficiency virus type 1 in human placental trophoblasts. J Virol 2004; 78:11904-11915.
96. Vidricaire G, Tardif M, Tremblay M: The low viral production in trophoblastic cells is due to a high endocytic internalization of human immunodeficiency virus type 1 and can be overcome by the pro-inflammatory cytokines tumor necrosis factor-alpha and interleukin 1. J Biol Chem 2003; 278:15832-15841.
97. Lee BN, Hammill H, Popek EJ, Cron S, Kozinetz C, Paul M, Shearer WT, Reuben JM: Production of interferons and beta-chemokines by placental trophoblasts of HIV-1-infected women. Infect Dis Obstet Gynecol 2001; 9:95-104.
98. Dean GA, Pederson NC: Cytokine response in multiple lymphoid tissues during the primary phase of feline immunodeficiency virus infection. J Virol 1998; 72:9436-9440.
99. Lawrence CE, Callanan JJ, Willett BJ, Jarrett O: Cytokine production by cats infected with feline immunodeficiency virus: a longitudinal study. Immunology 1995; 85:568-574.
100. Kipar A, Boretti FS, Meli MM, Failing K, Reinacher M, Lutz H: Reduced constitutive cytokine transcription in isolated monocytes of clinically healthy cats, infected with an FIV strain of low pathogenicity. Vet Immunol Immunopathol 2004; 98:215-221.
101. Ma J, Kennedy-Stoskopt S, Sellon R, Tonkonogy S, Hawkins EC, Tompkins MB, Tompkins WA: Tumor necrosis factor-α responses are depressed and interleukin-6 responses unaltered in feline immunodeficiency virus infected cats. Vet Immunol Immunopathol 1995; 46:35-50.
102. Ritchey JW, Levy JK, Bliss SK, Tompkins WAF, Tompkins MB: Constitutive expression of types 1 and 2 cytokines by alveolar macrophages from feline immunodeficiency virus-infected cats. Vet Immunol Immunopathol 2001; 79:83-100.
103. Sirriyah J, Dean GA, LaVoy A, Burkhard MJ: Assessment of CD4+ and CD8+ IFN-gamma producing cells by ELISPOT in naïve and FIV-infected cats. Vet Immunol Immunopathol 2004;102:77-84.
104. Lerner DL, Grant CK, Parseval AD, Elder JH: FIV infection of IL-2-dependent and -independent feline lymphocyte lines: host cells range distinctions and specific cytokine upregulation. Vet Immunol Immunopathol 1998;65:277-297.
105. Kraus LA, Bradley WG, Engleman RW, Brown KM, Good RA, Day NK: Relationship between tumor necrosis factor alpha and feline immunodeficiency virus expressions. J Virol 1996; 70:566-569.
106. Mortola E, Endo Y, Mizuno T, Ohno K, Watari T, Tsujimoto H, Hasegawa A: Effect of interleukin-12 and interleukin-10 on the virus replication and apoptosis in T-cells infected with feline immunodeficiency virus. J Vet Med Sci 1998; 60:1181-1185.
107. King A, Gardner L, Loke YW: Human decidual leukocytes do not proliferate in response to either extravillous trophoblast or allogeneic peripheral blood lymphocytes. J Reprod Immunol 1996; 30:67-74.
108. Vassiliadou N, Bulmer JN: Immunohistochemical evidence for increased numbers of classic CD57+ natural killer cells in the endometrium of women suffering spontaneous early pregnancy loss. Human Reprod 1996; 11:1569-1574.
109. Dosiou C, Giudice LC: Natural killer cells in pregnancy and recurrent pregnancy loss: endocrine and immunologic perspectives. Endocr Rev 2005; 26:44-62.
110. Beer AE, Kwak JYH, Ruiz JE: Immunophenotypic profiles of peripheral blood lymphocytes in women with recurrent pregnancy loses and in infertile women with multiple failed in vitro fertilization cycles. Am J Reprod Immunol 1996; 35:376-382.
111. Sehmsdorf US, Zenclussen AC, Arck P, Hertwig K, Joachim RA, Klapp B, Hildebrandt MO: Human miscarriage is associated with increased number of CD26+ decidual lymphocytes. Scand J Immunol 2004; 59:400-407.
112. Michimata T, Ogasawara MS, Tsuda H, Suzumori K, Aoki K, Sakai M, Fujimura M, Nagata K, Nakamura M, Saito S: Distributions of endometrial NK cells, B cells, T cells, and Th2/Tc2 cells fail to predict pregnancy outcome following recurrent abortion. Am J Reprod Immunol 2002; 47:196-202.
113. Hunt JS: Current topic: the role of macrophages in the uterine response to pregnancy. Placenta 1990; 11:467-475.
114. Mor G, Abrahams VM: Potential role of macrophages as immunoregulators of pregnancy. Reprod Biol Endocrinol 2003; 1:119-130.
115. Maloy K, Powrie F: Regulatory T cells in the control of immune pathology. Nature Immunol 2001; 2:816-822.
116. R cells suppress innate immune pathology though cytokine-dependent mechanisms. J Exp Med 2003; 197:111-119.
117. + T cells with regulatory properties isolated from peripheral blood. J Exp Med 2001; 193:1285-1294.
118. Caramalho I, Lopes-Carvalho T, Ostler D, Zelenay S, Haury M, Demengeot J: Regulatory T cells selectively express toll-like receptors and are activated by lipopolysaccharide. J Exp Med 2003; 4:397-401.
119. Cederbom L, Hall H, Ivars F: CD4+CD25+ regulatory T cells down-regulate co-stimulatory molecules on antigen-presenting cells. Eur J Immunol 2000; 30:1538-1543.
120. + immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J Exp Med 1998; 188:287-296.
121. + regulatory T-cell subset. Immunology 2004; 112:38-43.
122. + T lymphocytes in normal pregnancies. Mol Hum Reprod 2002; 8:667-673.
123. Heikkinen J, Möttönen M, Alanen A, Lassila O: Phenotypic characterization of regulatory T cells in the human deciduas. Clin Exp Immunol 2004; 136:373-378.
124. + regulatory T cells in early pregnancy subjects and spontaneous abortion cases. Mol Hum Reprod 2004; 10:347-353.
125. + regulatory T cells to rescue abortion-prone fetuses. Bio Reprod 2005; 72:338-345.
126. + T regulatory cells prevents fetal rejection in a murine abortion model. Am J Pathol 2005; 166:811-822.
127. + T regulatory cells. J Immunol 2004; 172:4752-4761.
128. +T cells independent of cellular proliferation. J Virol 2004; 321:307-322.
129. - cells. J Virol 2005; 335:212-221.
130. - T cells in acute HIV infection in vitro. J Immunol 1993; 150:5202-5208.
131. + T-regulatory cells correlates both with surface expression of CXCR4 and activation of FIV long terminal repeat binding celllular transcriptional factors. J Virol 2005; 79:4965-4976.
132. + T cell apoptosis. J Inf Dis 2002; 185:1077-1093.
133. Ishii M, Hayakawa S, Suzuki M-K, Yoshino N, Honda M, Nishinarita S, Chishima F, Hagaishi M, Satoh K: Expression of functional chemokine receptors of human placental cells. Am J Reprod Immunol 2000; 44:365-373.
134. Moussa M, Mognetti B, Dubanchet S, Menu E, Roques P, Gras G, Dormont D, Barre-Sinoussi F, Chaouat G: Vertical transmission of HIV: parameters which might affect infection of placental trophoblasts by HIV-1: a review. Am J Reprod Immunol 1999; 41:312-319.
135. Kumar A, Kumar S, Dinda AK, Luthra K: Differential expression of CXCR4 receptor in early and term human placenta. Placenta 2004; 25:347-351.
136. Behbahani H, Popek E, Garcia P, Andersson J, Spetz A-L, Landay A, Flener Z, Patterson BK: Up-regulation of CCR5 expression in the placenta is associated with human immunodeficiency virus-I vertical transmission. Am J Pathol 2000; 157:1811-1818.
137. Senger PL: Pathways to Pregnancy and Parturition. Pullman, WA: Current Conceptions Inc., 1997.