Skin-derived macrophages from Leishmania major-susceptible mice exhibit interleukin-12- and interferon-γ-independent nitric oxide production and parasite killing after treatment with immunostimulatory DNA

Journal of Investigative Dermatology

Volumn 119, Issue 3, 2002, Pages 621-628

  Von Stebut, Esther ^a,b   Belkaid, Yasmine ^c   Nguyen, Bai ^b   Wilson, Mark ^b   Sacks, David L ^c   Udey, Mark C ^b  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

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

Author keywords

CpG motif; Cytokines; Leishmania; Macrophages; Monocytes; Nitric oxide

Indexed keywords

GAMMA INTERFERON; IMMUNOSTIMULATING AGENT; INTERLEUKIN 12; LIPOPOLYSACCHARIDE; NITRIC OXIDE; OLIGODEOXYNUCLEOTIDE; PARASITE ANTIGEN; RECOMBINANT GAMMA INTERFERON; RECOMBINANT INTERLEUKIN 12;

AMASTIGOTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ARTICLE; CONTROLLED STUDY; CPG ISLAND; CYTOKINE PRODUCTION; DERIVATIZATION; DISEASE PREDISPOSITION; FEMALE; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOSTIMULATION; IN VIVO STUDY; LEISHMANIA MAJOR; LEISHMANIASIS; MACROPHAGE; MACROPHAGE FUNCTION; MOUSE; MOUSE STRAIN; NONHUMAN; PARASITE; PARASITE IDENTIFICATION; PRIORITY JOURNAL; PROTECTION; SKIN; SKIN DEFECT; SKIN INFECTION;

EID: 0036380796     PISSN: 0022202X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1523-1747.2002.01850.x     Document Type: Article

References (51)

1. Alleva DG, Kaser SB, Beller DI: Intrinsic defects in macrophage IL-12 production associated with immune dysfunction in the MRL/++ and New Zealand Black/White F1 lupus-prone mice and the Leishmania major-susceptible BALB/c strain. J Immunol 161:6878-6884, 1998
2. Ballas ZK, Rasmussen WL, Krieg AM: Induction of NK activity in murine and human cells by CpG motifs in oligodeoxynucleotides and bacterial DNA. J Immunol 157:1840-1845, 1996
3. Belkaid Y, Butcher B, Sacks DL: Analysis of cytokine production by inflammatory mouse macrophages at the single-cell level: selective impairment of IL-12 induction in Leishmania-infected cells. Eur J Immunol 28:1389-1400, 1998
4. Belkaid Y, Mendez S, Lira R, Kadambi N, Milon G, Sacks D: A natural model of Leishmania major infection reveals a prolonged 'silent' phase of parasite amplification in the skin before the onset of lesion formation and immunity. J Immunol 165:969-977, 2000
5. Bendigs S, Salzer U, Lipford GB, Wagner H, Heeg K: CpG-oligodeoxynucleotides co-stimulate primary T cells in the absence of antigen-presenting cells. Eur J Immunol 29:1209-1218, 1999
6. Carrera L, Gazzinelli RT, Badolato R, Hieny S, Muller W, Kuhn R, Sacks DL: Leishmania promastigotes selectively inhibit interleukin 12 induction in bone marrow-derived macrophages from susceptible and resistant mice. J Exp Med 183:515-526, 1996
7. Carson DA, Raz E: Oligonucleotide adjuvants for T helper 1 (Th1)-specific vaccination. J Exp Med 186:1621-1622, 1997
8. Dalton DK, Pitts-Meek S, Keshav S, Figari IS, Bradley A, Stewart TA: Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science 259:1739-1742, 1993
9. Fauve RM, Jusforgues H, Hevin B: Maintenance of granuloma macrophages in serum-free medium. J Immunol Meth 64:345-351, 1983
10. Gao JJ, Zuvanich EG, Xue Q, Horn DL, Silverstein R, Morrison DC: Cutting edge: bacterial DNA and LPS act in synergy in inducing nitric oxide production in RAW 264.7 macrophages. J Immunol 163:4095-4099-4095-9, 1999
11. Gessani S, Belardelli F: IFN-gamma expression in macrophages and its possible biological significance. Cytokine Growth Factor Rev 9:117-123, 1998
12. Gorak PM, Engwerda CR, Kaye PM: Dendritic cells, but not macrophages, produce IL-12 immediately following Leishmania donovani infection. Eur J Immunol 28:687-695, 1998
13. Green SJ, Crawford RM, Hockmeyer JT, Meltzer MS, Nacy CA: Leishmania major amastigotes initiate the L-arginine-dependent killing mechanism in IFN-gamma-stimulated macrophages by induction of tumor necrosis factor-alpha. J Immunol 145:4290-4297, 1990
14. Green SJ, Scheller LF, Marletta MA, et al: Nitric oxide: cytokine-regulation of nitric oxide in host resistance to intracellular pathogens. Immunol Lett 43:87-94, 1994
15. Jakob T, Walker PS, Krieg AM, von Stebut E, Udey MC, Vogel JC: Bacterial DNA and CpG-containing oligodeoxynucleotides activate cutaneous dendritic cells and induce IL-12 production: implications for the augmentation of Th1 responses. Int Arch Allergy Immunol 118:457-461, 1999
16. Jüttner S, Bernhagen J, Metz CN, Röllinghoff M, Bucala R, Gessner A: Migration inhibitory factor induces killing of Leishmania major by macrophages: dependence on reactive nitrogen intermediates and endogenous TNF-alpha. J Immunol 161:2383-2390, 1998
17. Kline JN, Waldschmidt TJ, Businga TR, Lemish JE, Weinstock JV, Thorne PS, Krieg AM: Modulation of airway inflammation by CpG oligodeoxynucleotides in a murine model of asthma. J Immunol 160:2555-2559, 1998
18. Klinman DM, Barnhart KM, Conover J: CpG motifs as immune adjuvants. Vaccine 17:19-25, 1999
19. Liew FY, Li Y, Moss D, Parkinson C, Rogers MV, Moncada S: Resistance to Leishmania major infection correlates with the induction of nitric oxide synthase in murine macrophages. Eur J Immunol 21:3009-3014, 1991
20. Locksley RM, Pingel S, Lacy D, Wakil AE, Bix M, Fowell DJ: Susceptibility to infectious diseases: Leishmania as a paradigm. J Infect Dis 179:S305-S308, 1999
21. MacMicking J, Xie QW, Nathan C: Nitric oxide and macrophage function. Annu Rev Immunol 15:323-350, 1997
22. Magram J, Connaughton SE, Warrier RR, et al: IL-12-deficient mice are defective in IFN gamma production and type 1 cytokine responses. Immunity 4:471-481, 1996
23. Mills CD, Kincaid K, Alt JM, Heilman MJ, Hill AM: M-1/M-2 macrophages and the Th1/Th2 paradigm. J Immunol 164:6166-6173, 2000
24. Mohrs M, Ledermann B, Kohler G, Dorfmuller A, Gessner A, Brombacher F: Differences between IL-4 and IL-4 receptor alpha-deficient mice in chronic leishmaniasis reveal a protective role for IL-13 receptor signaling. J Immunol 162:7302-7308, 1999
25. Munder M, Mallo M, Eichmann K, Modolell M: Murine macrophages secrete interferon gamma upon combined stimulation with interleukin (IL)-12 and IL-18: a novel pathway of autocrine macrophage activation. J Exp Med 187:2103-2108, 1998
26. Murray HW, Nathan CF: Macrophage microbicidal mechanisms in vivo: reactive nitrogen versus oxygen intermediates in the killing of intracellular visceral Leishmania donovani. J Exp Med 189:741-746, 1999
27. Murray HW, Jungbluth A, Ritter E, Montelibano C, Marino MW: Visceral leishmaniasis in mice devoid of tumor necrosis factor and response to treatment. Infect Immun 68:6289-6293, 2000
28. Nabors GS, Afonso LC, Farrell JP, Scott P: Switch from a type 2 to a type 1 T helper cell response and cure of established Leishmania major infection in mice is induced by combined therapy with interleukin 12 and Pentostam. Proc Natl Acad Sci USA 92:3142-3146, 1995
29. Nashleanas M, Kanaly S, Scott P: Control of Leishmania major infection in mice lacking TNF receptors. J Immunol 160:5506-5513, 1998
30. Ohashi K, Burkart V, Flohe S, Kolb H: Cutting edge: heat shock protein 60 is a putative endogenous ligand of the toll-like receptor-4 complex. J Immunol 164:558-561, 2000
31. Oswald IP, Afroun S, Bray D, Petit JF, Lemaire G: Low response of BALB/c macrophages to priming and activating signals. J Leukoc Biol 52:315-322-315-22, 1992
32. Puddu P, Fantuzzi L, Borghi P, et al: IL-12 induces IFN-gamma expression and secretion in mouse peritoneal macrophages. J Immunol 159:3490-3497, 1997
33. Reiner SL, Locksley RM: The regulation of immunity to Leishmania major. Annu Rev Immunol 13:151-177, 1995
34. Reis e Sousa C, Hieny S, Scharton-Kersten T, Jankovic D, Charest H, Germain RN, Sher A: In vivo microbial stimulation induces rapid CD40 ligand-independent production of interleukin 12 by dendritic cells and their redistribution to T cell areas. J Exp Med 186:1819-1829, 1997
35. Scott P: Th cell development and regulation in experimental cutaneous leishmaniasis. Chem Immunol 63:98-114, 1996
36. Sester DP, Naik S, Beasley SJ, Hume DA, Stacey KJ: Phosphorothioate backbone modification modulates macrophage activation by CpG DNA. J Immunol 165:4165-4173, 2000
37. Shoda LK, Kegerreis KA, Suarez CE, Mwangi W, Knowles DP, Brown WC: Immunostimulatory CpG-modified plasmid DNA enhances IL-12, TNF-alpha, and NO production by bovine macrophages. J Leukoc Biol 70:103-112, 2001
38. Sparwasser T, Koch ES, Vabulas RM, Heeg K, Lipford GB, Ellwart JW, Wagner H: Bacterial DNA and immunostimulatory CpG oligonucleotides trigger maturation and activation of murine dendritic cells. Eur J Immunol 28:2045-2054, 1998
39. Stacey KJ, Blackwell JM: Immunostimulatory DNA as an adjuvant in vaccination against Leishmania major. Infect Immun 67:3719-3726, 1999
40. Stacey KJ, Sweet MJ, Hume DA: Macrophages ingest and are activated by bacterial DNA. J Immunol 157:2116-2122, 1996
41. von Stebut E, Belkaid Y, Jakob T, Sacks DL, Udey MC: Uptake of Leishmania major amastigotes results in activation and interleukin 12 release from murine skin-derived dendritic cells: implications for the initiation of anti-Leishmania immunity. J Exp Med 188:1547-1552, 1998
42. von Stebut E, Belkaid Y, Nguyen BV, Cushing M, Sacks DL, Udey MC: Leishmania major-infected murine Langerhans cell-like dendritic cells from susceptible mice release IL-12 after infection and vaccinate against experimental cutaneous leishmaniasis. Eur J Immunol 30:3498-3506, 2000
43. Stuehr DJ, Nathan CF: Nitric oxide. A macrophage product responsible for cytostasis and respiratory inhibition in tumor target cells. J Exp Med 169:1543-1555, 1989
44. Sunderkötter C, Kunz M, Steinbrink K, Meinardus-Hager G, Goebeler M, Bildau H, Sorg C: Resistance of mice to experimental leishmaniasis is associated with more rapid appearance of mature macrophages in vitro and in vivo. J Immunol 151:4891-4901, 1993
45. Sweet MJ, Stacey KJ, Kakuda DK, Markovich D, Hume DA: IFN-gamma primes macrophage responses to bacterial DNA. J Interferon Cytokine Res 18:263-271, 1998
46. Taylor AP, Murray HW: Intracellular antimicrobial activity in the absence of interferon-gamma: effect of interleukin-12 in experimental visceral leishmaniasis in interferon-gamma gene-disrupted mice. J Exp Med 185:1231-1239, 1997
47. Walker PS, Scharton-Kersten T, Krieg AM, Love-Homan L, Rowton ED, Udey MC, Vogel JC: Immunostimulatory oligodeoxynucleotides promote protective immunity and provide systemic therapy for leishmaniasis via IL-12- and IFN-gamma-dependent mechanisms. Proc Natl Acad Sci USA 96:6970-6975, 1999
48. Wilhelm P, Ritter U, Labbow S, Donhauser N, Rollinghoff M, Bogdan C, Korner H: Rapidly fatal leishmaniasis in resistant C57BL/6 mice lacking TNF. J Immunol 166:4012-4019, 2001
49. Yi AK, Hornbeck P, Lafrenz DE, Krieg AM: CpG DNA rescue of murine B lymphoma cells from anti-IgM-induced growth arrest and programmed cell death is associated with increased expression of c-myc and bcl-xL. J Immunol 157:4918-4925, 1996
50. Zhu FG, Reich CF, Pisetsky DS: The role of the macrophage scavenger receptor in immune stimulation by bacterial DNA and synthetic oligonucleotides. Immunology 103:226-234, 2001
51. Zimmermann S, Egeter O, Hausmann S, Lipford GB, Roecken M, Wagner H, Heeg K: CpG oligodeoxynucleotides trigger protective and curative Th1 responses in lethal murine leishmaniasis. J Immunol 160:3627-3630, 1998