CCR5 is essential for NK cell trafficking and host survival following Toxoplasma gondii infection

PLoS Pathogens

Volumn 2, Issue 6, 2006, Pages 0484-0500

  Khan, Imtiaz A ^a,c   Thomas, Seddon Y ^b   Moretto, Magali M ^a   Lee, Frederick S ^b   Islam, Sabina A ^b   Combe, Crescent ^a   Schwartzman, Joseph D ^c   Luster, Andrew D ^b  

^a LOUISIANA STATE UNIV MEDICAL CENTER   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON TETRACHLORIDE; CHEMOKINE; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR3; GAMMA INTERFERON; INTERLEUKIN 12; LIGAND; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; PROTOZOAL DNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL TRANSFER; CHEMOTAXIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFECT; HEPATITIS; HISTOPATHOLOGY; IMMUNE MEDIATED INJURY; IMMUNE RESPONSE; INBRED STRAIN; INFECTION SENSITIVITY; INFLAMMATION; MOUSE; NATURAL KILLER CELL; NONHUMAN; PHENOTYPE; SPLEEN; SURVIVAL; TOXOPLASMA GONDII; WILD TYPE; ADOPTIVE TRANSFER; ANIMAL; C57BL MOUSE; CELL MOTION; DISEASE PREDISPOSITION; GENETICS; HYBRIDIZATION; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; MOUSE STRAIN; PARASITOLOGY; PATHOLOGY; PATHOPHYSIOLOGY; TIME; TOXOPLASMA; TOXOPLASMOSIS;

PROTOZOA; TOXOPLASMA GONDII;

ADOPTIVE TRANSFER; ANIMALS; CELL MOVEMENT; DISEASE SUSCEPTIBILITY; DNA, PROTOZOAN; HYBRIDIZATION, GENETIC; INFLAMMATION; INTERFERON TYPE II; INTERLEUKIN-12; KILLER CELLS, NATURAL; LIGANDS; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; MICE, KNOCKOUT; PHENOTYPE; RECEPTORS, CCR5; SURVIVAL; TIME FACTORS; TOXOPLASMA; TOXOPLASMOSIS;

EID: 33745728267     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.0020049     Document Type: Article

References (54)

1. Sher A, Denkers E, Gazzinelli R (1995) Induction and regulation of host cell-mediated immunity by Toxoplasma gondii. Ciba Found Symp 195: 95-104.
2. Bliss SK, Butcher BA, Denkers EY (2000) Rapid recruitment of neutrophils containing prestored IL-12 during microbial infection. J Immunol 165: 4515-4521.
3. Khan IA, Murphy PM, Casciotti L, Schwartzman JD, Collins J, et al. (2001) Mice lacking the chemokine receptor CCR1 show increased susceptibility to Toxoplasma gondii infection. J Immunol 166: 1930-1937.
4. Suzuki Y, Orellana M, Schreiber R, Remington J (1988) Interferon-gammon: The major mediator of resistance against Toxoplasma gondii. Science 22: 516-518.
5. + T cells in mice. J Immunol 140: 3943-3946.
6. Gazzinelli RT, Hieny S, Wynn TA, Wolf S, Sher A (1993) Interleukin 12 is required for the T-lymphocyte-independent induction of interferon gamma by an intracellular parasite and induces resistance in T-cell-deficient hosts. Proc Natl Acad Sci U S A 90: 6115-6119.
7. + cells as effectors of IFN-gamma dependent immunity to Toxoplasma gondii in MHC class I-deficient mice. J Exp Med 178: 1465-1472.
8. Hunter CA, Subauste CS, Van Cleave VH, Remington JS (1994) Production of gamma interferon by natural killer cells from Toxoplasma gondii-infected SCID mice: Regulation by interleukin-10, interleukin-12, and tumor necrosis factor alpha. Infect Immun 62: 2818-2824.
9. Boehm U, Klamp T, Groot M, Howard JC (1997) Cellular responses to interferon-gamma. Annu Rev Immunol 15: 749-795.
10. Akiyama K, Yokota K, Kagawa S, Shimbara N, Tamura T, et al. (1994) cDNA cloning and interferon gamma down-regulation of proteasomal subunits X and Y. Science 265: 1231-1234.
11. Inngjerdingen M, Damaj B, Maghazachi AA (2000) Human NK cells express CC chemokine receptors 4 and 8 and respond to thymus and activation-regulated chemokine, macrophage-derived chemokine, and I-309. J Immunol 164: 4048-4054.
12. + NK and NK-T peripheral blood lymphocytes identified by chemokine receptor expression repertoire. J Immunol 166: 6477-6482.
13. Inngjerdingen M, Damaj B, Maghazachi AA (2001) Expression and regulation of chemokine receptors in human natural killer cells. Blood 97: 367-375.
14. Mack M, Cihak J, Simonis C, Luckow B, Proudfoot AE, et al. (2001) Expression and characterization of the chemokine receptors CCR2 and CCR5 in mice. J Immunol 166: 4697-4704.
15. Salazar-Mather TP, Orange JS, Biron CA (1998) Early murine cytomegalovirus (MCMV) infection induces liver natural killer (NK) cell inflammation and protection through macrophage inflammatory protein 1alpha (MIP-1alpha)-dependent pathways. J Exp Med 187: 1-14.
16. Salazar-Mather TP, Hamilton TA, Biron CA (2000) A chemokine-to-cytokine- to-chemokine cascade critical in antiviral defense. J Clin Invest 105: 985-993.
17. Khan I, MacLean JA, Lee F, Casciotti L, DeHaan E, et al. (2000) The IP-10 chemokine is critical for effector T cell trafficking and host survival in Toxoplasma gondii infection. Immunity 12: 483-494.
18. McLeod R, Skamene E, Brown CR, Eisenhauer PB, Mack DG (1989) Genetic regulation of early survival and cyst number after peroral Toxoplasma gondii infection of A X B/B X A recombinant inbred and B10 congenic mice. J Immunol 143: 3031-3034.
19. Khan IA, Schwartzman JD, Matsuura T, Kasper LH (1997) A dichotomous role for nitric oxide during acute Toxoplasma gondii infection in mice. Proc Natl Acad Sci U S A 94: 13955-13960.
20. + T cell-dependent, interferon-gamma-mediated necrosis of the small intestine with genetic susceptibility of mice to peroral infection with Toxoplasma gondii. J Exp Med 184: 597-607.
21. + dendritic cells. Nat Immunol 1: 83-87.
22. Trinchieri G (1998) Proinflammatory and immunoregulatory functions of interleukin-12. Int Rev Immunol 16: 365-396.
23. Khan IA, Matsuura T, Kasper LH (1994) Interleukin-12 enhances murine survival against acute toxoplasmosis. Infect Immun 62: 1639-1642.
24. Tomasello E, Desmoulins PO, Chemin K, Guia S, Cremer H, et al. (2000) Combined natural killer cell and dendritic cell functional deficiency in KARAP/DAP12 loss-of-function mutant mice. Immunity 13: 355-364.
25. Martin-Fontecha A, Thomsen LL, Brett S, Gerard C, Lipp M, et al. (2004) Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat Immunol 5: 1260-1265.
26. Chantakru S, Kuziel WA, Maeda N, Croy BA (2001) A study on the density and distribution of uterine natural killer cells at mid pregnancy in mice genetically-ablated for CCR2, CCR 5 and the CCR5 receptor ligand, MIP-1 alpha. J Reprod Immunol 49: 33-47.
27. 2+ mobilization, and enzyme release. J Immunol 156: 322-327.
28. Drake PM, Gunn MD, Charo IF, Tsou CL, Zhou Y, et al. (2001) Human placental cytotrophoblasts attract monocytes and CD56(bright) natural killer cells via the actions of monocyte inflammatory protein 1alpha. J Exp Med 193: 1199-1212.
29. Johnson LL (1992) SCID mouse models of acute and relapsing chronic Toxoplasma gondii infections. Infect Immun 60: 3719-3724.
30. Luangsay S, Kasper LH, Rachinel N, Minns LA, Mennechet FJ, et al. (2003) CCR5 mediates specific migration of Toxoplasma gondii-primed CD8 lymphocytes to inflammatory intestinal epithelial cells. Gastroenterology 125: 491-500.
31. Aliberti J, Valenzuela JG, Carruthers VB, Hieny S, Andersen J, et al. (2003) Molecular mimicry of a CCR5 binding-domain in the microbial activation of dendritic cells. Nat Immunol 4: 485-490.
32. Zhou Y, Kurihara T, Ryseck R-P, Yang Y, Ryan C, et al. (1998) Impaired macrophage function and enhanced T cell-dependent immune response in mice lacking CCR5, the mouse homologue of the major HIV-1 coreceptor. J Immunol 160: 4018-4025.
33. Dawson TC, Beck MA, Kuziel WA, Henderson F, Maeda N (2000) Contrasting effects of CCR5 and CCR2 deficiency in the pulmonary inflammatory response to influenza A virus. Am J Pathol 156: 1951-1959.
34. Sato N, Kuziel WA, Melby PC, Reddick RL, Kostecki V, et al. (1999) Defects in the generation of IFN-gamma are overcome to control infection with Leishmania donovani in CC chemokine receptor (CCR) 5-, macrophage inflammatory protein-1 alpha-, or CCR2-deficient mice. J Immunol 163: 5519-5525.
35. + lymphocyte-associated Th2-type immune response in the intestine. J Immunol 164: 6303-6312.
36. Deng H, Liu R, Ellmeier W, Choe S, Unutmaz D, et al. (1996) Identification of a major co-receptor for primary isolates of HIV-1. Nature 381: 661-666.
37. + cells is mediated by the chemokine receptor CC-CKR-5. Nature 381: 667-673.
38. Dean M, Carrington M, Winkler C, Huttley GA, Smith MW, et al. (1996) Genetic restriction of HIV-1 infection and progression to AIDS by a deletion allele of the CKR5 structural gene. Science 273: 1856-1862.
39. Samson M, Libert F, Doranz BJ, Rucker J, Liesnard C, et al. (1996) Resistance to HIV-1 infection in caucasion individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature 332: 722-725.
40. Liu R, Paxton WA, Choe S, Ceradini D, Martin SR, et al. (1996) Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell 86: 367-377.
41. Gomez-Reino JJ, Pablos JL, Carreira PE, Santiago B, Serrano L, et al. (1999) Association of rheumatoid arthritis with a functional chemokine receptor, CCR5. Arthritis Rheum 42: 989-992.
42. Zapico I, Coto E, Rodriguez A, Alvarez C, Torre JC, et al. (2000) CCR5 (chemokine receptor-5) DNA-polymorphism influences the severity of rheumatoid arthritis. Genes Immun 1: 288-289.
43. Garred P, Madsen HO, Petersen J, Marquart H, Hansen TM, et al. (1998) CC chemokine receptor 5 polymorphism in rheumatoid arthritis. J Rheumatol 25: 1462-1465.
44. Rector A, Vermeire S, Thoelen I, Keyaerts E, Struyf F, et al. (2001) Analysis of the CC chemokine receptor 5 (CCR5) delta-32 polymorphism in inflammatory bowel disease. Hum Genet 108: 190-193.
45. Bennetts BH, Teutsch SM, Buhler MM, Heard R.N., Stewart GJ (1997) The CCR5 deletion mutation fails to protect against multiple sclerosis. Hum Immunol 58: 52-59.
46. Barcellos LF, Schito AM, Rimmler JB, Vittinghoff E, Shih A, et al. (2000) CC-chemokine receptor 5 polymorphism and age of onset in familial multiple sclerosis. Multiple Sclerosis Genetics Group. Immunogenetics 51: 281-288.
47. Hokeness KL, Kuziel WA, Biron CA, Salazar-Mather TP (2005) Monocyte chemoattractant protein-1 and CCR2 interactions are required for IFNalpha/beta-induced inflammatory responses and antiviral defense in liver. J Immunol 174: 1549-1556.
48. Kuziel WA, Maeda N (1998) CCR5. In: Mak T, editor. The gene knockout factsbook. London: Academic Press. pp. 120-121.
49. Burg JL, Grover CM, Pouletty P, Boothroyd JC (1989) Direct and sensitive detection of a pathogenic protozoan, Toxoplasma gondii, by polymerase chain reaction. J Clin Microbiol 27: 1787-1792.
50. Kirists MJ, Mui E, Mcleod R (2000) Measurement of the efficacy of vaccines and antimicrobial therapy against infection with Toxoplasma gondii. Int J Parasit 30: 149-155.
51. Watanabe H, Ohtsuka K, Kimura M, Ikarashi Y, Ohmori K, et al. (1992) Details of an isolation method for hepatic lymphocytes in mice. J Immunol Methods 146: 145-154.
52. + T cell response. J Exp Med 195: 1463-1470.
53. Means TK, Hayashi F, Smith KD, Aderem A, Luster AD (2003) The Toll-like receptor 5 stimulus bacterial flagellin induces maturation and chemokine production in human dendritic cells. J Immunol 170: 5165-5175.
54. Arase H, Saito T, Phillips JH, Lanier LL (2001) Cutting edge: The mouse NK cell-associated antigen recognized by DX5 monoclonal antibody is CD49b (alpha 2 integrin, very late antigen-2). J Immunol 167: 1141-1144.