Bacillus Calmette-Guerin Infection in NADPH Oxidase Deficiency: Defective Mycobacterial Sequestration and Granuloma Formation

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The vaccine Mycobacterium bovis BCG is administrated to prevent early age tuberculosis in endemic areas. BCG is a live vaccine with a low incidence of complications. However, local or disseminated BCG infection may occur, in particular in immunodeficient individuals. Chronic granulomatous disease (CGD), a deficiency in the superoxide-producing phagocyte NADPH oxidase, is a primary immune deficiency and one of the most frequent congenital defects of phagocyte in humans. Here we analyze the role of the phagocyte NADPH oxidase NOX2 in the defense against BCG. An extensive literature review suggested that BCG infection is by far the most common mycobacterial disease in CGD patients (220 published cases). We therefore studied BCG infection in several CGD mouse models showing that these were highly susceptible to BCG infection with a mortality rate of ∼50%. As compared to the wild type, CGD mice showed a markedly increased release of cytokines, an altered granuloma structure, and were unable to restrain mycobacteria within granulomas. Rescue of the phagocyte NADPH oxidase in macrophages was sufficient to protect mice from BCG infection and to sequester the mycobacteria within granulomas. Thus, superoxide generation by macrophages plays an important role for the defense against BCG infection and prevents overshooting release of proinflammatory cytokines.

Vyšlo v časopise: Bacillus Calmette-Guerin Infection in NADPH Oxidase Deficiency: Defective Mycobacterial Sequestration and Granuloma Formation. PLoS Pathog 10(9): e32767. doi:10.1371/journal.ppat.1004325
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004325

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1. AndersenP, DohertyTM (2005) The success and failure of BCG -⁠ implications for a novel tuberculosis vaccine. Nat Rev Microbiol 3 : 656–662.

2. KeijsersRR, BovenschenHJ, SeygerMM (2011) Cutaneous complication after BCG vaccination: case report and review of the literature. J Dermatolog Treat 22 : 315–318.

3. BustamanteJ, PicardC, Boisson-DupuisS, AbelL, CasanovaJL (2011) Genetic lessons learned from X-linked Mendelian susceptibility to mycobacterial diseases. Ann N Y Acad Sci 1246 : 92–101.

4. van der MeijdenAP, SteerenbergPA, de JongWH, DebruyneFM (1991) Intravesical Bacillus Calmette-Guerin treatment for superficial bladder cancer: results after 15 years of experience. Anticancer research 11 : 1253–1258.

5. StegA, LeleuC, DebreB, Boccon-GibodL, SicardD (1989) Systemic bacillus Calmette-Guerin infection, ‘BCGitis’, in patients treated by intravesical bacillus Calmette-Guerin therapy for bladder cancer. Eur Urol 16 : 161–164.

6. BustamanteJ, AksuG, VogtG, de BeaucoudreyL, GenelF, et al. (2007) BCG-osis and tuberculosis in a child with chronic granulomatous disease. J Allergy Clin Immunol 120 : 32–38.

7. LiHM, ZhaoSY, HeJX, JiangZF (2010) [Clinical analysis of 18 children with disseminated Bacille Calmette-Guerin infection]. Zhonghua Er Ke Za Zhi 48 : 65–68.

8. YingWJ, WangXC, SunJQ, LiuDR, YuYH, et al. (2012) [Clinical features of chronic granulomatous disease]. Zhonghua Er Ke Za Zhi 50 : 380–385.

9. NorouziS, AghamohammadiA, MamishiS, RosenzweigSD, RezaeiN (2012) Bacillus Calmette-Guerin (BCG) complications associated with primary immunodeficiency diseases. J Infect 64 : 543–554.

10. FattahiF, BadalzadehM, SedighipourL, MovahediM, FazlollahiMR, et al. (2011) Inheritance pattern and clinical aspects of 93 Iranian patients with chronic granulomatous disease. J Clin Immunol 31 : 792–801.

11. BedardK, KrauseKH (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87 : 245–313.

12. SchappiM, DeffertC, FietteL, GavazziG, HerrmannF, et al. (2008) Branched fungal beta-glucan causes hyperinflammation and necrosis in phagocyte NADPH oxidase-deficient mice. J Pathol 214 : 434–444.

13. NathanC, ShilohMU (2000) Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc Natl Acad Sci U S A 97 : 8841–8848.

14. DeffertC, CachatJ, KrauseKH (2014) Phagocyte NADPH oxidase, chronic granulomatous disease and mycobacterial infections. Cell Microbiol 16 : 1168–1178.

15. Garcia I, Olleros ML (2009) The roles of tumor necrosis factor and other macrophage-derived cytokines in host defense mechanisms during the course of Mycobacterium tuberculosis infection. In: Current Topics on the Profiles of Host Immunological Response to Mycobacterial Infections pp. 1–46.

16. GarciaI, OllerosML, QuesniauxVF, JacobsM, AllieN, et al. (2011) Roles of soluble and membrane TNF and related ligands in mycobacterial infections: effects of selective and non-selective TNF inhibitors during infection. Adv Exp Med Biol 691 : 187–201.

17. LoweDM, RedfordPS, WilkinsonRJ, O'GarraA, MartineauAR (2012) Neutrophils in tuberculosis: friend or foe? Trends Immunol 33 : 14–25.

18. BustamanteJ, AriasAA, VogtG, PicardC, GaliciaLB, et al. (2011) Germline CYBB mutations that selectively affect macrophages in kindreds with X-linked predisposition to tuberculous mycobacterial disease. Nat Immunol 12 : 213–221.

19. KokerMY, CamciogluY, van LeeuwenK, KilicSS, BarlanI, et al. (2013) Clinical, functional, and genetic characterization of chronic granulomatous disease in 89 Turkish patients. J Allergy Clin Immunol 132 : 1156–1163 e1155.

20. LeeWI, HuangJL, YehKW, JaingTH, LinTY, et al. (2011) Immune defects in active mycobacterial diseases in patients with primary immunodeficiency diseases (PIDs). J Formos Med Assoc 110 : 750–758.

21. LinCJ, WangSC, KuCL, KaoJK, ChenM, et al. (2013) Successful Unrelated Cord Blood Stem Cell Transplantation in an X-linked Chronic Granulomatous Disease Patient with Disseminated BCG-induced Infection. Pediatr Neonatol DOI: 10.1016/j.pedneo.2013.04.001

22. KhotaeiG, Hirbod-MobarakehA, AmirkashaniD, ManafiF, RezaeiN (2012) Mycobacterium tuberculosis meningitis as the first presentation of chronic granulomatous disease. Braz J Infect Dis 16 : 491–492.

23. NaidooR, JordaanN, ChanKW, Le RouxDM, PienaarS, et al. (2011) A novel CYBB mutation with the first genetically confirmed case of chronic granulomatous disease in South Africa. S Afr Med J 101 : 768–769.

24. Afshar PaimanS, SiadatiA, MamishiS, TabatabaieP, KhotaeeG (2006) Disseminated Mycobacterium bovis infection after BCG vaccination. Iran J Allergy Asthma Immunol 5 : 133–137.

25. LeePP, ChanKW, JiangL, ChenT, LiC, et al. (2008) Susceptibility to mycobacterial infections in children with X-linked chronic granulomatous disease: a review of 17 patients living in a region endemic for tuberculosis. Pediatr Infect Dis J 27 : 224–230.

26. Sadeghi-ShanbestariM, AnsarinK, MaljaeiSH, RafeeyM, PezeshkiZ, et al. (2009) Immunologic aspects of patients with disseminated bacille Calmette-Guerin disease in north-west of Iran. Ital J Pediatr 35 : 42.

27. KusuharaK, OhgaS, HoshinaT, SaitoM, SasakiY, et al. (2009) Disseminated Bacillus Calmette-Guerin lymphadenitis in a patient with gp91phox -⁠ chronic granulomatous disease 25 years after vaccination. Eur J Pediatr 168 : 745–747.

28. MovahediZ, NorouziS, MamishiS, RezaeiN (2011) BCGiosis as a presenting feature of a child with chronic granulomatous disease. Braz J Infect Dis 15 : 83–86.

29. DeffertC, CarnesecchiS, YuanH, RougemontAL, KelkkaT, et al. (2012) Hyperinflammation of chronic granulomatous disease is abolished by NOX2 reconstitution in macrophages and dendritic cells. J Pathol 228 : 341–350.

30. SareilaO, JaakkolaN, OlofssonP, KelkkaT, HolmdahlR (2013) Identification of a region in p47phox/NCF1 crucial for phagocytic NADPH oxidase (NOX2) activation. J Leukoc Biol 93 : 427–435.

31. GeldermanKA, HultqvistM, PizzollaA, ZhaoM, NandakumarKS, et al. (2007) Macrophages suppress T cell responses and arthritis development in mice by producing reactive oxygen species. J Clin Invest 117 : 3020–3028.

32. PizzollaA, HultqvistM, NilsonB, GrimmMJ, EneljungT, et al. (2012) Reactive oxygen species produced by the NADPH oxidase 2 complex in monocytes protect mice from bacterial infections. J Immunol 188 : 5003–5011.

33. MorgensternDE, GiffordMA, LiLL, DoerschukCM, DinauerMC (1997) Absence of respiratory burst in X-linked chronic granulomatous disease mice leads to abnormalities in both host defense and inflammatory response to Aspergillus fumigatus. J Exp Med 185 : 207–218.

34. GarciaI, GulerR, VesinD, OllerosML, VassalliP, et al. (2000) Lethal Mycobacterium bovis Bacillus Calmette Guerin infection in nitric oxide synthase 2-deficient mice: cell-mediated immunity requires nitric oxide synthase 2. Lab Invest 80 : 1385–1397.

35. PacherP, BeckmanJS, LiaudetL (2007) Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87 : 315–424.

36. ChtanovaT, SchaefferM, HanSJ, van DoorenGG, NollmannM, et al. (2008) Dynamics of neutrophil migration in lymph nodes during infection. Immunity 29 : 487–496.

37. VesoskyB, RottinghausEK, StrombergP, TurnerJ, BeamerG (2010) CCL5 participates in early protection against Mycobacterium tuberculosis. J Leukoc Biol 87 : 1153–1165.

38. BreenAP, MurphyJA (1995) Reactions of oxyl radicals with DNA. Free Radic Biol Med 18 : 1033–1077.

39. SanmunD, WitaspE, JitkaewS, TyurinaYY, KaganVE, et al. (2009) Involvement of a functional NADPH oxidase in neutrophils and macrophages during programmed cell clearance: implications for chronic granulomatous disease. Am J Physiol Cell Physiol 297: C621–631.

40. von Kockritz-BlickwedeM, NizetV (2009) Innate immunity turned inside-out: antimicrobial defense by phagocyte extracellular traps. J Mol Med (Berl) 87 : 775–783.

41. BianchiM, NiemiecMJ, SilerU, UrbanCF, ReichenbachJ (2011) Restoration of anti-Aspergillus defense by neutrophil extracellular traps in human chronic granulomatous disease after gene therapy is calprotectin-dependent. J Allergy Clin Immunol 127 : 1243–1252 e1247.

42. HatanakaE, CarvalhoBT, Condino-NetoA, CampaA (2004) Hyperresponsiveness of neutrophils from gp 91phox deficient patients to lipopolysaccharide and serum amyloid A. Immunol Lett 94 : 43–46.

43. HultqvistM, OlofssonP, HolmbergJ, BackstromBT, TordssonJ, et al. (2004) Enhanced autoimmunity, arthritis, and encephalomyelitis in mice with a reduced oxidative burst due to a mutation in the Ncf1 gene. Proc Natl Acad Sci U S A 101 : 12646–12651.

44. HanusM, MatouskovaM, VernerP, HyrslL (1994) Immunotherapy of superficial bladder tumors: preliminary results with ImmuCyst–BCG Connaught, Toronto. Neoplasma 41 : 25–27.

45. OllerosML, VesinD, BisigR, Santiago-RaberML, Schuepbach-MallepellS, et al. (2012) Membrane-bound TNF induces protective immune responses to M. bovis BCG infection: regulation of memTNF and TNF receptors comparing two memTNF molecules. PLoS One 7: e31469.

46. OllerosML, GulerR, CorazzaN, VesinD, EugsterHP, et al. (2002) Transmembrane TNF induces an efficient cell-mediated immunity and resistance to Mycobacterium bovis bacillus Calmette-Guerin infection in the absence of secreted TNF and lymphotoxin-alpha. J Immunol 168 : 3394–3401.

47. OllerosML, GulerR, VesinD, ParapanovR, MarchalG, et al. (2005) Contribution of transmembrane tumor necrosis factor to host defense against Mycobacterium bovis bacillus Calmette-guerin and Mycobacterium tuberculosis infections. Am J Pathol 166 : 1109–1120.

48. FotioAL, OllerosML, VesinD, TauzinS, BisigR, et al. (2010) In vitro inhibition of lipopolysaccharide and mycobacterium bovis bacillus Calmette Guerin-induced inflammatory cytokines and in vivo protection from D-galactosamine/LPS -mediated liver injury by the medicinal plant Sclerocarya birrea. Int J Immunopathol Pharmacol 23 : 61–72.

49. BedardK, AttarH, BonnefontJ, JaquetV, BorelC, et al. (2009) Three common polymorphisms in the CYBA gene form a haplotype associated with decreased ROS generation. Hum Mutat 30 : 1123–1133.

50. GulerR, OllerosML, VesinD, ParapanovR, VesinC, et al. (2004) Inhibition of inducible nitric oxide synthase protects against liver injury induced by mycobacterial infection and endotoxins. J Hepatol 41 : 773–781.

51. GulerR, OllerosML, VesinD, ParapanovR, GarciaI (2005) Differential effects of total and partial neutralization of tumor necrosis factor on cell-mediated immunity to Mycobacterium bovis BCG infection. Infect Immun 73 : 3668–3676.

52. SchiavoneS, SorceS, Dubois-DauphinM, JaquetV, ColaiannaM, et al. (2009) Involvement of NOX2 in the development of behavioral and pathologic alterations in isolated rats. Biol Psychiatry 66 : 384–392.

53. VigneS, PalmerG, MartinP, LamacchiaC, StrebelD, et al. (2012) IL-36 signaling amplifies Th1 responses by enhancing proliferation and Th1 polarization of naive CD4+ T cells. Blood 120 : 3478–3487.

54. DeffertC, OllerosML, HuipingY, HerrmannFR, ZekryD, et al. (2011) TNF-alpha blockade in chronic granulomatous disease-induced hyperinflammation: patient analysis and murine model. J Allergy Clin Immunol 128 : 675–677.