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Published in: BMC Infectious Diseases 1/2010

Open Access 01-12-2010 | Research article

CD36 deficiency attenuates experimental mycobacterial infection

Authors: Michael Hawkes, Xiaoming Li, Maryanne Crockett, Angelina Diassiti, Constance Finney, Gundula Min-Oo, W Conrad Liles, Jun Liu, Kevin C Kain

Published in: BMC Infectious Diseases | Issue 1/2010

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Abstract

Background

Members of the CD36 scavenger receptor family have been implicated as sensors of microbial products that mediate phagocytosis and inflammation in response to a broad range of pathogens. We investigated the role of CD36 in host response to mycobacterial infection.

Methods

Experimental Mycobacterium bovis Bacillus Calmette-Guérin (BCG) infection in Cd36 +/+ and Cd36 -/- mice, and in vitro co-cultivation of M. tuberculosis, BCG and M. marinum with Cd36 +/+ and Cd36 -/- murine macrophages.

Results

Using an in vivo model of BCG infection in Cd36 +/+ and Cd36 -/- mice, we found that mycobacterial burden in liver and spleen is reduced (83% lower peak splenic colony forming units, p < 0.001), as well as the density of granulomas, and circulating tumor necrosis factor (TNF) levels in Cd36 -/- animals. Intracellular growth of all three mycobacterial species was reduced in Cd36 -/- relative to wild type Cd36 +/+ macrophages in vitro. This difference was not attributable to alterations in mycobacterial uptake, macrophage viability, rate of macrophage apoptosis, production of reactive oxygen and/or nitrogen species, TNF or interleukin-10. Using an in vitro model designed to recapitulate cellular events implicated in mycobacterial infection and dissemination in vivo (i.e., phagocytosis of apoptotic macrophages containing mycobacteria), we demonstrated reduced recovery of viable mycobacteria within Cd36 -/- macrophages.

Conclusions

Together, these data indicate that CD36 deficiency confers resistance to mycobacterial infection. This observation is best explained by reduced intracellular survival of mycobacteria in the Cd36 -/- macrophage and a role for CD36 in the cellular events involved in granuloma formation that promote early bacterial expansion and dissemination.
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Literature
2.
go back to reference Saunders BM, Britton WJ: Life and death in the granuloma: immunopathology of tuberculosis. Immunol Cell Biol. 2007, 85 (2): 103-111. 10.1038/sj.icb.7100027.CrossRefPubMed Saunders BM, Britton WJ: Life and death in the granuloma: immunopathology of tuberculosis. Immunol Cell Biol. 2007, 85 (2): 103-111. 10.1038/sj.icb.7100027.CrossRefPubMed
3.
go back to reference Egen JG, Rothfuchs AG, Feng CG, Winter N, Sher A, Germain RN: Macrophage and T cell dynamics during the development and disintegration of mycobacterial granulomas. Immunity. 2008, 28 (2): 271-284. 10.1016/j.immuni.2007.12.010.CrossRefPubMedPubMedCentral Egen JG, Rothfuchs AG, Feng CG, Winter N, Sher A, Germain RN: Macrophage and T cell dynamics during the development and disintegration of mycobacterial granulomas. Immunity. 2008, 28 (2): 271-284. 10.1016/j.immuni.2007.12.010.CrossRefPubMedPubMedCentral
4.
go back to reference Davis JM, Ramakrishnan L: The role of the granuloma in expansion and dissemination of early tuberculous infection. Cell. 2009, 136 (1): 37-49. 10.1016/j.cell.2008.11.014.CrossRefPubMedPubMedCentral Davis JM, Ramakrishnan L: The role of the granuloma in expansion and dissemination of early tuberculous infection. Cell. 2009, 136 (1): 37-49. 10.1016/j.cell.2008.11.014.CrossRefPubMedPubMedCentral
5.
go back to reference Lau YL, Chan GC, Ha SY, Hui YF, Yuen KY: The role of phagocytic respiratory burst in host defense against Mycobacterium tuberculosis. Clin Infect Dis. 1998, 26 (1): 226-227. 10.1086/517036.CrossRefPubMed Lau YL, Chan GC, Ha SY, Hui YF, Yuen KY: The role of phagocytic respiratory burst in host defense against Mycobacterium tuberculosis. Clin Infect Dis. 1998, 26 (1): 226-227. 10.1086/517036.CrossRefPubMed
6.
go back to reference Winkelstein JA, Marino MC, Johnston RB, Boyle J, Curnutte J, Gallin JI, Malech HL, Holland SM, Ochs H, Quie P, et al: Chronic granulomatous disease. Report on a national registry of 368 patients. Medicine (Baltimore). 2000, 79 (3): 155-169. 10.1097/00005792-200005000-00003.CrossRef Winkelstein JA, Marino MC, Johnston RB, Boyle J, Curnutte J, Gallin JI, Malech HL, Holland SM, Ochs H, Quie P, et al: Chronic granulomatous disease. Report on a national registry of 368 patients. Medicine (Baltimore). 2000, 79 (3): 155-169. 10.1097/00005792-200005000-00003.CrossRef
7.
go back to reference Picard C, Fieschi C, Altare F, Al-Jumaah S, Al-Hajjar S, Feinberg J, Dupuis S, Soudais C, Al-Mohsen IZ, Genin E, et al: Inherited interleukin-12 deficiency: IL12B genotype and clinical phenotype of 13 patients from six kindreds. Am J Hum Genet. 2002, 70 (2): 336-348. 10.1086/338625.CrossRefPubMed Picard C, Fieschi C, Altare F, Al-Jumaah S, Al-Hajjar S, Feinberg J, Dupuis S, Soudais C, Al-Mohsen IZ, Genin E, et al: Inherited interleukin-12 deficiency: IL12B genotype and clinical phenotype of 13 patients from six kindreds. Am J Hum Genet. 2002, 70 (2): 336-348. 10.1086/338625.CrossRefPubMed
8.
go back to reference Altare F, Durandy A, Lammas D, Emile JF, Lamhamedi S, Le Deist F, Drysdale P, Jouanguy E, Doffinger R, Bernaudin F, et al: Impairment of mycobacterial immunity in human interleukin-12 receptor deficiency. Science. 1998, 280 (5368): 1432-1435. 10.1126/science.280.5368.1432.CrossRefPubMed Altare F, Durandy A, Lammas D, Emile JF, Lamhamedi S, Le Deist F, Drysdale P, Jouanguy E, Doffinger R, Bernaudin F, et al: Impairment of mycobacterial immunity in human interleukin-12 receptor deficiency. Science. 1998, 280 (5368): 1432-1435. 10.1126/science.280.5368.1432.CrossRefPubMed
9.
go back to reference Jouanguy E, Lamhamedi-Cherradi S, Altare F, Fondaneche MC, Tuerlinckx D, Blanche S, Emile JF, Gaillard JL, Schreiber R, Levin M, et al: Partial interferon-gamma receptor 1 deficiency in a child with tuberculoid bacillus Calmette-Guerin infection and a sibling with clinical tuberculosis. J Clin Invest. 1997, 100 (11): 2658-2664. 10.1172/JCI119810.CrossRefPubMedPubMedCentral Jouanguy E, Lamhamedi-Cherradi S, Altare F, Fondaneche MC, Tuerlinckx D, Blanche S, Emile JF, Gaillard JL, Schreiber R, Levin M, et al: Partial interferon-gamma receptor 1 deficiency in a child with tuberculoid bacillus Calmette-Guerin infection and a sibling with clinical tuberculosis. J Clin Invest. 1997, 100 (11): 2658-2664. 10.1172/JCI119810.CrossRefPubMedPubMedCentral
10.
go back to reference Dupuis S, Dargemont C, Fieschi C, Thomassin N, Rosenzweig S, Harris J, Holland SM, Schreiber RD, Casanova JL: Impairment of mycobacterial but not viral immunity by a germline human STAT1 mutation. Science. 2001, 293 (5528): 300-303. 10.1126/science.1061154.CrossRefPubMed Dupuis S, Dargemont C, Fieschi C, Thomassin N, Rosenzweig S, Harris J, Holland SM, Schreiber RD, Casanova JL: Impairment of mycobacterial but not viral immunity by a germline human STAT1 mutation. Science. 2001, 293 (5528): 300-303. 10.1126/science.1061154.CrossRefPubMed
11.
go back to reference Bellamy R: NRAMP1 and susceptibility to tuberculosis. Int J Tuberc Lung Dis. 2002, 6 (9): 747-PubMed Bellamy R: NRAMP1 and susceptibility to tuberculosis. Int J Tuberc Lung Dis. 2002, 6 (9): 747-PubMed
12.
go back to reference Bellamy R, Ruwende C, Corrah T, McAdam KP, Whittle HC, Hill AV: Variations in the NRAMP1 gene and susceptibility to tuberculosis in West Africans. N Engl J Med. 1998, 338 (10): 640-644. 10.1056/NEJM199803053381002.CrossRefPubMed Bellamy R, Ruwende C, Corrah T, McAdam KP, Whittle HC, Hill AV: Variations in the NRAMP1 gene and susceptibility to tuberculosis in West Africans. N Engl J Med. 1998, 338 (10): 640-644. 10.1056/NEJM199803053381002.CrossRefPubMed
13.
go back to reference Bellamy R, Ruwende C, Corrah T, McAdam KP, Thursz M, Whittle HC, Hill AV: Tuberculosis and chronic hepatitis B virus infection in Africans and variation in the vitamin D receptor gene. J Infect Dis. 1999, 179 (3): 721-724. 10.1086/314614.CrossRefPubMed Bellamy R, Ruwende C, Corrah T, McAdam KP, Thursz M, Whittle HC, Hill AV: Tuberculosis and chronic hepatitis B virus infection in Africans and variation in the vitamin D receptor gene. J Infect Dis. 1999, 179 (3): 721-724. 10.1086/314614.CrossRefPubMed
14.
go back to reference Bellamy R, Beyers N, McAdam KP, Ruwende C, Gie R, Samaai P, Bester D, Meyer M, Corrah T, Collin M, et al: Genetic susceptibility to tuberculosis in Africans: a genome-wide scan. Proc Natl Acad Sci USA. 2000, 97 (14): 8005-8009. 10.1073/pnas.140201897.CrossRefPubMedPubMedCentral Bellamy R, Beyers N, McAdam KP, Ruwende C, Gie R, Samaai P, Bester D, Meyer M, Corrah T, Collin M, et al: Genetic susceptibility to tuberculosis in Africans: a genome-wide scan. Proc Natl Acad Sci USA. 2000, 97 (14): 8005-8009. 10.1073/pnas.140201897.CrossRefPubMedPubMedCentral
15.
go back to reference Casanova JL, Abel L: Genetic dissection of immunity to mycobacteria: the human model. Annu Rev Immunol. 2002, 20: 581-620. 10.1146/annurev.immunol.20.081501.125851.CrossRefPubMed Casanova JL, Abel L: Genetic dissection of immunity to mycobacteria: the human model. Annu Rev Immunol. 2002, 20: 581-620. 10.1146/annurev.immunol.20.081501.125851.CrossRefPubMed
16.
go back to reference Flynn JL: Lessons from experimental Mycobacterium tuberculosis infections. Microbes Infect. 2006, 8 (4): 1179-1188. 10.1016/j.micinf.2005.10.033.CrossRefPubMed Flynn JL: Lessons from experimental Mycobacterium tuberculosis infections. Microbes Infect. 2006, 8 (4): 1179-1188. 10.1016/j.micinf.2005.10.033.CrossRefPubMed
17.
go back to reference Costello RT, Izumi T, Sakurami T: Behavior of attenuated mycobacteria in organs of neonatal and adult mice. J Exp Med. 1971, 134 (2): 366-380. 10.1084/jem.134.2.366.CrossRefPubMedPubMedCentral Costello RT, Izumi T, Sakurami T: Behavior of attenuated mycobacteria in organs of neonatal and adult mice. J Exp Med. 1971, 134 (2): 366-380. 10.1084/jem.134.2.366.CrossRefPubMedPubMedCentral
18.
go back to reference Cosma CL, Humbert O, Sherman DR, Ramakrishnan L: Trafficking of superinfecting Mycobacterium organisms into established granulomas occurs in mammals and is independent of the Erp and ESX-1 mycobacterial virulence loci. J Infect Dis. 2008, 198 (12): 1851-1855. 10.1086/593175.CrossRefPubMedPubMedCentral Cosma CL, Humbert O, Sherman DR, Ramakrishnan L: Trafficking of superinfecting Mycobacterium organisms into established granulomas occurs in mammals and is independent of the Erp and ESX-1 mycobacterial virulence loci. J Infect Dis. 2008, 198 (12): 1851-1855. 10.1086/593175.CrossRefPubMedPubMedCentral
19.
go back to reference Kremer L, Estaquier J, Wolowczuk I, Biet F, Ameisen JC, Locht C: Ineffective cellular immune response associated with T-cell apoptosis in susceptible Mycobacterium bovis BCG-infected mice. Infect Immun. 2000, 68 (7): 4264-4273. 10.1128/IAI.68.7.4264-4273.2000.CrossRefPubMedPubMedCentral Kremer L, Estaquier J, Wolowczuk I, Biet F, Ameisen JC, Locht C: Ineffective cellular immune response associated with T-cell apoptosis in susceptible Mycobacterium bovis BCG-infected mice. Infect Immun. 2000, 68 (7): 4264-4273. 10.1128/IAI.68.7.4264-4273.2000.CrossRefPubMedPubMedCentral
20.
go back to reference Tonjum T, Welty DB, Jantzen E, Small PL: Differentiation of Mycobacterium ulcerans, M. marinum, and M. haemophilum: mapping of their relationships to M. tuberculosis by fatty acid profile analysis, DNA-DNA hybridization, and 16S rRNA gene sequence analysis. J Clin Microbiol. 1998, 36 (4): 918-925.PubMedPubMedCentral Tonjum T, Welty DB, Jantzen E, Small PL: Differentiation of Mycobacterium ulcerans, M. marinum, and M. haemophilum: mapping of their relationships to M. tuberculosis by fatty acid profile analysis, DNA-DNA hybridization, and 16S rRNA gene sequence analysis. J Clin Microbiol. 1998, 36 (4): 918-925.PubMedPubMedCentral
21.
go back to reference Cosma CL, Sherman DR, Ramakrishnan L: The secret lives of the pathogenic mycobacteria. Annu Rev Microbiol. 2003, 57: 641-676. 10.1146/annurev.micro.57.030502.091033.CrossRefPubMed Cosma CL, Sherman DR, Ramakrishnan L: The secret lives of the pathogenic mycobacteria. Annu Rev Microbiol. 2003, 57: 641-676. 10.1146/annurev.micro.57.030502.091033.CrossRefPubMed
22.
go back to reference Cosma CL, Humbert O, Ramakrishnan L: Superinfecting mycobacteria home to established tuberculous granulomas. Nat Immunol. 2004, 5 (8): 828-835. 10.1038/ni1091.CrossRefPubMed Cosma CL, Humbert O, Ramakrishnan L: Superinfecting mycobacteria home to established tuberculous granulomas. Nat Immunol. 2004, 5 (8): 828-835. 10.1038/ni1091.CrossRefPubMed
23.
go back to reference Cosma CL, Swaim LE, Volkman H, Ramakrishnan L, Davis JM: Zebrafish and frog models of Mycobacterium marinum infection. Curr Protoc Microbiol. 2006, Chapter 10 (Unit 10B): 12- Cosma CL, Swaim LE, Volkman H, Ramakrishnan L, Davis JM: Zebrafish and frog models of Mycobacterium marinum infection. Curr Protoc Microbiol. 2006, Chapter 10 (Unit 10B): 12-
24.
go back to reference Decostere A, Hermans K, Haesebrouck F: Piscine mycobacteriosis: a literature review covering the agent and the disease it causes in fish and humans. Vet Microbiol. 2004, 99 (3-4): 159-166. 10.1016/j.vetmic.2003.07.011.CrossRefPubMed Decostere A, Hermans K, Haesebrouck F: Piscine mycobacteriosis: a literature review covering the agent and the disease it causes in fish and humans. Vet Microbiol. 2004, 99 (3-4): 159-166. 10.1016/j.vetmic.2003.07.011.CrossRefPubMed
25.
go back to reference Volkman HE, Clay H, Beery D, Chang JC, Sherman DR, Ramakrishnan L: Tuberculous granuloma formation is enhanced by a mycobacterium virulence determinant. PLoS Biol. 2004, 2 (11): e367-10.1371/journal.pbio.0020367.CrossRefPubMedPubMedCentral Volkman HE, Clay H, Beery D, Chang JC, Sherman DR, Ramakrishnan L: Tuberculous granuloma formation is enhanced by a mycobacterium virulence determinant. PLoS Biol. 2004, 2 (11): e367-10.1371/journal.pbio.0020367.CrossRefPubMedPubMedCentral
26.
go back to reference Tan T, Lee WL, Alexander DC, Grinstein S, Liu J: The ESAT-6/CFP-10 secretion system of Mycobacterium marinum modulates phagosome maturation. Cell Microbiol. 2006, 8 (9): 1417-1429. 10.1111/j.1462-5822.2006.00721.x.CrossRefPubMed Tan T, Lee WL, Alexander DC, Grinstein S, Liu J: The ESAT-6/CFP-10 secretion system of Mycobacterium marinum modulates phagosome maturation. Cell Microbiol. 2006, 8 (9): 1417-1429. 10.1111/j.1462-5822.2006.00721.x.CrossRefPubMed
27.
go back to reference van der Wel N, Hava D, Houben D, Fluitsma D, van Zon M, Pierson J, Brenner M, Peters PJ: M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell. 2007, 129 (7): 1287-1298. 10.1016/j.cell.2007.05.059.CrossRefPubMed van der Wel N, Hava D, Houben D, Fluitsma D, van Zon M, Pierson J, Brenner M, Peters PJ: M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell. 2007, 129 (7): 1287-1298. 10.1016/j.cell.2007.05.059.CrossRefPubMed
28.
go back to reference Febbraio M, Hajjar DP, Silverstein RL: CD36: a class B scavenger receptor involved in angiogenesis, atherosclerosis, inflammation, and lipid metabolism. J Clin Invest. 2001, 108 (6): 785-791.CrossRefPubMedPubMedCentral Febbraio M, Hajjar DP, Silverstein RL: CD36: a class B scavenger receptor involved in angiogenesis, atherosclerosis, inflammation, and lipid metabolism. J Clin Invest. 2001, 108 (6): 785-791.CrossRefPubMedPubMedCentral
29.
go back to reference Voll RE, Herrmann M, Roth EA, Stach C, Kalden JR, Girkontaite I: Immunosuppressive effects of apoptotic cells. Nature. 1997, 390 (6658): 350-351. 10.1038/37022.CrossRefPubMed Voll RE, Herrmann M, Roth EA, Stach C, Kalden JR, Girkontaite I: Immunosuppressive effects of apoptotic cells. Nature. 1997, 390 (6658): 350-351. 10.1038/37022.CrossRefPubMed
30.
go back to reference Stuart LM, Deng J, Silver JM, Takahashi K, Tseng AA, Hennessy EJ, Ezekowitz RA, Moore KJ: Response to Staphylococcus aureus requires CD36-mediated phagocytosis triggered by the COOH-terminal cytoplasmic domain. J Cell Biol. 2005, 170 (3): 477-485. 10.1083/jcb.200501113.CrossRefPubMedPubMedCentral Stuart LM, Deng J, Silver JM, Takahashi K, Tseng AA, Hennessy EJ, Ezekowitz RA, Moore KJ: Response to Staphylococcus aureus requires CD36-mediated phagocytosis triggered by the COOH-terminal cytoplasmic domain. J Cell Biol. 2005, 170 (3): 477-485. 10.1083/jcb.200501113.CrossRefPubMedPubMedCentral
31.
go back to reference Hoebe K, Georgel P, Rutschmann S, Du X, Mudd S, Crozat K, Sovath S, Shamel L, Hartung T, Zahringer U, et al: CD36 is a sensor of diacylglycerides. Nature. 2005, 433 (7025): 523-527. 10.1038/nature03253.CrossRefPubMed Hoebe K, Georgel P, Rutschmann S, Du X, Mudd S, Crozat K, Sovath S, Shamel L, Hartung T, Zahringer U, et al: CD36 is a sensor of diacylglycerides. Nature. 2005, 433 (7025): 523-527. 10.1038/nature03253.CrossRefPubMed
32.
go back to reference Baranova IN, Kurlander R, Bocharov AV, Vishnyakova TG, Chen Z, Remaley AT, Csako G, Patterson AP, Eggerman TL: Role of human CD36 in bacterial recognition, phagocytosis, and pathogen-induced JNK-mediated signaling. J Immunol. 2008, 181 (10): 7147-7156.CrossRefPubMedPubMedCentral Baranova IN, Kurlander R, Bocharov AV, Vishnyakova TG, Chen Z, Remaley AT, Csako G, Patterson AP, Eggerman TL: Role of human CD36 in bacterial recognition, phagocytosis, and pathogen-induced JNK-mediated signaling. J Immunol. 2008, 181 (10): 7147-7156.CrossRefPubMedPubMedCentral
33.
go back to reference Patel SN, Lu Z, Ayi K, Serghides L, Gowda DC, Kain KC: Disruption of CD36 impairs cytokine response to Plasmodium falciparum glycosylphosphatidylinositol and confers susceptibility to severe and fatal malaria in vivo. J Immunol. 2007, 178 (6): 3954-3961.CrossRefPubMed Patel SN, Lu Z, Ayi K, Serghides L, Gowda DC, Kain KC: Disruption of CD36 impairs cytokine response to Plasmodium falciparum glycosylphosphatidylinositol and confers susceptibility to severe and fatal malaria in vivo. J Immunol. 2007, 178 (6): 3954-3961.CrossRefPubMed
34.
go back to reference Serghides L, Smith TG, Patel SN, Kain KC: CD36 and malaria: friends or foes?. Trends Parasitol. 2003, 19 (10): 461-469. 10.1016/j.pt.2003.08.006.CrossRefPubMed Serghides L, Smith TG, Patel SN, Kain KC: CD36 and malaria: friends or foes?. Trends Parasitol. 2003, 19 (10): 461-469. 10.1016/j.pt.2003.08.006.CrossRefPubMed
35.
go back to reference Philips JA, Rubin EJ, Perrimon N: Drosophila RNAi screen reveals CD36 family member required for mycobacterial infection. Science. 2005, 309 (5738): 1251-1253. 10.1126/science.1116006.CrossRefPubMed Philips JA, Rubin EJ, Perrimon N: Drosophila RNAi screen reveals CD36 family member required for mycobacterial infection. Science. 2005, 309 (5738): 1251-1253. 10.1126/science.1116006.CrossRefPubMed
36.
go back to reference Sanchez MD, Garcia Y, Montes C, Paris SC, Rojas M, Barrera LF, Arias MA, Garcia LF: Functional and phenotypic changes in monocytes from patients with tuberculosis are reversed with treatment. Microbes Infect. 2006, 8 (9-10): 2492-2500. 10.1016/j.micinf.2006.06.005.CrossRefPubMed Sanchez MD, Garcia Y, Montes C, Paris SC, Rojas M, Barrera LF, Arias MA, Garcia LF: Functional and phenotypic changes in monocytes from patients with tuberculosis are reversed with treatment. Microbes Infect. 2006, 8 (9-10): 2492-2500. 10.1016/j.micinf.2006.06.005.CrossRefPubMed
37.
go back to reference Sulahian TH, Imrich A, Deloid G, Winkler AR, Kobzik L: Signaling pathways required for macrophage scavenger receptor-mediated phagocytosis: analysis by scanning cytometry. Respir Res. 2008, 9: 59-10.1186/1465-9921-9-59.CrossRefPubMedPubMedCentral Sulahian TH, Imrich A, Deloid G, Winkler AR, Kobzik L: Signaling pathways required for macrophage scavenger receptor-mediated phagocytosis: analysis by scanning cytometry. Respir Res. 2008, 9: 59-10.1186/1465-9921-9-59.CrossRefPubMedPubMedCentral
38.
go back to reference Malo D, Vogan K, Vidal S, Hu J, Cellier M, Schurr E, Fuks A, Bumstead N, Morgan K, Gros P: Haplotype mapping and sequence analysis of the mouse Nramp gene predict susceptibility to infection with intracellular parasites. Genomics. 1994, 23 (1): 51-61. 10.1006/geno.1994.1458.CrossRefPubMed Malo D, Vogan K, Vidal S, Hu J, Cellier M, Schurr E, Fuks A, Bumstead N, Morgan K, Gros P: Haplotype mapping and sequence analysis of the mouse Nramp gene predict susceptibility to infection with intracellular parasites. Genomics. 1994, 23 (1): 51-61. 10.1006/geno.1994.1458.CrossRefPubMed
39.
go back to reference Kumar S, Lavin MF: The ICE family of cysteine proteases as effectors of cell death. Cell Death Differ. 1996, 3 (3): 255-267.PubMed Kumar S, Lavin MF: The ICE family of cysteine proteases as effectors of cell death. Cell Death Differ. 1996, 3 (3): 255-267.PubMed
40.
go back to reference Nau GJ, Liaw L, Chupp GL, Berman JS, Hogan BL, Young RA: Attenuated host resistance against Mycobacterium bovis BCG infection in mice lacking osteopontin. Infect Immun. 1999, 67 (8): 4223-4230.PubMedPubMedCentral Nau GJ, Liaw L, Chupp GL, Berman JS, Hogan BL, Young RA: Attenuated host resistance against Mycobacterium bovis BCG infection in mice lacking osteopontin. Infect Immun. 1999, 67 (8): 4223-4230.PubMedPubMedCentral
41.
go back to reference Bhatt K, Salgame P: Host Innate Immune Response to Mycobacterium tuberculosis. J Clin Immunol. 2007, 27 (4): 347-362. 10.1007/s10875-007-9084-0.CrossRefPubMed Bhatt K, Salgame P: Host Innate Immune Response to Mycobacterium tuberculosis. J Clin Immunol. 2007, 27 (4): 347-362. 10.1007/s10875-007-9084-0.CrossRefPubMed
42.
go back to reference Wintergerst ES, Jelk J, Rahner C, Asmis R: Apoptosis induced by oxidized low density lipoprotein in human monocyte-derived macrophages involves CD36 and activation of caspase-3. Eur J Biochem. 2000, 267 (19): 6050-6059. 10.1046/j.1432-1327.2000.01682.x.CrossRefPubMed Wintergerst ES, Jelk J, Rahner C, Asmis R: Apoptosis induced by oxidized low density lipoprotein in human monocyte-derived macrophages involves CD36 and activation of caspase-3. Eur J Biochem. 2000, 267 (19): 6050-6059. 10.1046/j.1432-1327.2000.01682.x.CrossRefPubMed
43.
go back to reference Balcewicz-Sablinska MK, Keane J, Kornfeld H, Remold HG: Pathogenic Mycobacterium tuberculosis evades apoptosis of host macrophages by release of TNF-R2, resulting in inactivation of TNF-alpha. J Immunol. 1998, 161 (5): 2636-2641.PubMed Balcewicz-Sablinska MK, Keane J, Kornfeld H, Remold HG: Pathogenic Mycobacterium tuberculosis evades apoptosis of host macrophages by release of TNF-R2, resulting in inactivation of TNF-alpha. J Immunol. 1998, 161 (5): 2636-2641.PubMed
44.
go back to reference Loeuillet C, Martinon F, Perez C, Munoz M, Thome M, Meylan PR: Mycobacterium tuberculosis subverts innate immunity to evade specific effectors. J Immunol. 2006, 177 (9): 6245-6255.CrossRefPubMed Loeuillet C, Martinon F, Perez C, Munoz M, Thome M, Meylan PR: Mycobacterium tuberculosis subverts innate immunity to evade specific effectors. J Immunol. 2006, 177 (9): 6245-6255.CrossRefPubMed
45.
go back to reference Winau F, Weber S, Sad S, de Diego J, Hoops SL, Breiden B, Sandhoff K, Brinkmann V, Kaufmann SH, Schaible UE: Apoptotic vesicles crossprime CD8 T cells and protect against tuberculosis. Immunity. 2006, 24 (1): 105-117. 10.1016/j.immuni.2005.12.001.CrossRefPubMed Winau F, Weber S, Sad S, de Diego J, Hoops SL, Breiden B, Sandhoff K, Brinkmann V, Kaufmann SH, Schaible UE: Apoptotic vesicles crossprime CD8 T cells and protect against tuberculosis. Immunity. 2006, 24 (1): 105-117. 10.1016/j.immuni.2005.12.001.CrossRefPubMed
46.
go back to reference Chan ED, Chan J, Schluger NW: What is the role of nitric oxide in murine and human host defense against tuberculosis?Current knowledge. Am J Respir Cell Mol Biol. 2001, 25 (5): 606-612.CrossRefPubMed Chan ED, Chan J, Schluger NW: What is the role of nitric oxide in murine and human host defense against tuberculosis?Current knowledge. Am J Respir Cell Mol Biol. 2001, 25 (5): 606-612.CrossRefPubMed
47.
go back to reference Moncada S, Palmer RM, Higgs EA: Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev. 1991, 43 (2): 109-142.PubMed Moncada S, Palmer RM, Higgs EA: Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev. 1991, 43 (2): 109-142.PubMed
48.
go back to reference Heldwein KA, Liang MD, Andresen TK, Thomas KE, Marty AM, Cuesta N, Vogel SN, Fenton MJ: TLR2 and TLR4 serve distinct roles in the host immune response against Mycobacterium bovis BCG. J Leukoc Biol. 2003, 74 (2): 277-286. 10.1189/jlb.0103026.CrossRefPubMed Heldwein KA, Liang MD, Andresen TK, Thomas KE, Marty AM, Cuesta N, Vogel SN, Fenton MJ: TLR2 and TLR4 serve distinct roles in the host immune response against Mycobacterium bovis BCG. J Leukoc Biol. 2003, 74 (2): 277-286. 10.1189/jlb.0103026.CrossRefPubMed
49.
go back to reference Sugawara I, Yamada H, Li C, Mizuno S, Takeuchi O, Akira S: Mycobacterial infection in TLR2 and TLR6 knockout mice. Microbiol Immunol. 2003, 47 (5): 327-336.CrossRefPubMed Sugawara I, Yamada H, Li C, Mizuno S, Takeuchi O, Akira S: Mycobacterial infection in TLR2 and TLR6 knockout mice. Microbiol Immunol. 2003, 47 (5): 327-336.CrossRefPubMed
50.
go back to reference Thoma-Uszynski S, Stenger S, Takeuchi O, Ochoa MT, Engele M, Sieling PA, Barnes PF, Rollinghoff M, Bolcskei PL, Wagner M, et al: Induction of direct antimicrobial activity through mammalian toll-like receptors. Science. 2001, 291 (5508): 1544-1547. 10.1126/science.291.5508.1544.CrossRefPubMed Thoma-Uszynski S, Stenger S, Takeuchi O, Ochoa MT, Engele M, Sieling PA, Barnes PF, Rollinghoff M, Bolcskei PL, Wagner M, et al: Induction of direct antimicrobial activity through mammalian toll-like receptors. Science. 2001, 291 (5508): 1544-1547. 10.1126/science.291.5508.1544.CrossRefPubMed
51.
go back to reference Rojas-Espinosa O, Wek-Rodriguez K, Arce-Paredes P, Aguilar-Torrentera F, Truyens C, Carlier Y: Contrary to BCG, MLM fails to induce the production of TNF alpha and NO by macrophages. Int J Lepr Other Mycobact Dis. 2002, 70 (2): 111-118.PubMed Rojas-Espinosa O, Wek-Rodriguez K, Arce-Paredes P, Aguilar-Torrentera F, Truyens C, Carlier Y: Contrary to BCG, MLM fails to induce the production of TNF alpha and NO by macrophages. Int J Lepr Other Mycobact Dis. 2002, 70 (2): 111-118.PubMed
52.
go back to reference Gordon AH, Hart PD: Stimulation or inhibition of the respiratory burst in cultured macrophages in a mycobacterium model: initial stimulation is followed by inhibition after phagocytosis. Infect Immun. 1994, 62 (10): 4650-4651.PubMedPubMedCentral Gordon AH, Hart PD: Stimulation or inhibition of the respiratory burst in cultured macrophages in a mycobacterium model: initial stimulation is followed by inhibition after phagocytosis. Infect Immun. 1994, 62 (10): 4650-4651.PubMedPubMedCentral
53.
go back to reference Bellamy R: The natural resistance-associated macrophage protein and susceptibility to intracellular pathogens. Microbes Infect. 1999, 1 (1): 23-27. 10.1016/S1286-4579(99)80010-0.CrossRefPubMed Bellamy R: The natural resistance-associated macrophage protein and susceptibility to intracellular pathogens. Microbes Infect. 1999, 1 (1): 23-27. 10.1016/S1286-4579(99)80010-0.CrossRefPubMed
54.
go back to reference Flesch IE, Hess JH, Oswald IP, Kaufmann SH: Growth inhibition of Mycobacterium bovis by IFN-gamma stimulated macrophages: regulation by endogenous tumor necrosis factor-alpha and by IL-10. Int Immunol. 1994, 6 (5): 693-700. 10.1093/intimm/6.5.693.CrossRefPubMed Flesch IE, Hess JH, Oswald IP, Kaufmann SH: Growth inhibition of Mycobacterium bovis by IFN-gamma stimulated macrophages: regulation by endogenous tumor necrosis factor-alpha and by IL-10. Int Immunol. 1994, 6 (5): 693-700. 10.1093/intimm/6.5.693.CrossRefPubMed
55.
go back to reference Murray PJ, Wang L, Onufryk C, Tepper RI, Young RA: T cell-derived IL-10 antagonizes macrophage function in mycobacterial infection. J Immunol. 1997, 158 (1): 315-321.PubMed Murray PJ, Wang L, Onufryk C, Tepper RI, Young RA: T cell-derived IL-10 antagonizes macrophage function in mycobacterial infection. J Immunol. 1997, 158 (1): 315-321.PubMed
56.
go back to reference Murray PJ, Young RA: Increased antimycobacterial immunity in interleukin-10-deficient mice. Infect Immun. 1999, 67 (6): 3087-3095.PubMedPubMedCentral Murray PJ, Young RA: Increased antimycobacterial immunity in interleukin-10-deficient mice. Infect Immun. 1999, 67 (6): 3087-3095.PubMedPubMedCentral
57.
go back to reference Jacobs M, Brown N, Allie N, Gulert R, Ryffel B: Increased resistance to mycobacterial infection in the absence of interleukin-10. Immunology. 2000, 100 (4): 494-501. 10.1046/j.1365-2567.2000.00053.x.CrossRefPubMedPubMedCentral Jacobs M, Brown N, Allie N, Gulert R, Ryffel B: Increased resistance to mycobacterial infection in the absence of interleukin-10. Immunology. 2000, 100 (4): 494-501. 10.1046/j.1365-2567.2000.00053.x.CrossRefPubMedPubMedCentral
58.
go back to reference Jacobs M, Fick L, Allie N, Brown N, Ryffel B: Enhanced immune response in Mycobacterium bovis bacille calmette guerin (BCG)-infected IL-10-deficient mice. Clin Chem Lab Med. 2002, 40 (9): 893-902. 10.1515/CCLM.2002.158.CrossRefPubMed Jacobs M, Fick L, Allie N, Brown N, Ryffel B: Enhanced immune response in Mycobacterium bovis bacille calmette guerin (BCG)-infected IL-10-deficient mice. Clin Chem Lab Med. 2002, 40 (9): 893-902. 10.1515/CCLM.2002.158.CrossRefPubMed
59.
go back to reference Roach TI, Barton CH, Chatterjee D, Liew FY, Blackwell JM: Opposing effects of interferon-gamma on iNOS and interleukin-10 expression in lipopolysaccharide- and mycobacterial lipoarabinomannan-stimulated macrophages. Immunology. 1995, 85 (1): 106-113.PubMedPubMedCentral Roach TI, Barton CH, Chatterjee D, Liew FY, Blackwell JM: Opposing effects of interferon-gamma on iNOS and interleukin-10 expression in lipopolysaccharide- and mycobacterial lipoarabinomannan-stimulated macrophages. Immunology. 1995, 85 (1): 106-113.PubMedPubMedCentral
60.
go back to reference Chung EY, Liu J, Homma Y, Zhang Y, Brendolan A, Saggese M, Han J, Silverstein R, Selleri L, Ma X: Interleukin-10 expression in macrophages during phagocytosis of apoptotic cells is mediated by homeodomain proteins Pbx1 and Prep-1. Immunity. 2007, 27 (6): 952-964. 10.1016/j.immuni.2007.11.014.CrossRefPubMedPubMedCentral Chung EY, Liu J, Homma Y, Zhang Y, Brendolan A, Saggese M, Han J, Silverstein R, Selleri L, Ma X: Interleukin-10 expression in macrophages during phagocytosis of apoptotic cells is mediated by homeodomain proteins Pbx1 and Prep-1. Immunity. 2007, 27 (6): 952-964. 10.1016/j.immuni.2007.11.014.CrossRefPubMedPubMedCentral
61.
go back to reference Devadoss P, Klegerman ME, Groves MJ: Surface morphology of Mycobacterium bovis BCG: relation to mechanisms of cellular aggregation. Microbios. 1991, 65 (263): 111-125.PubMed Devadoss P, Klegerman ME, Groves MJ: Surface morphology of Mycobacterium bovis BCG: relation to mechanisms of cellular aggregation. Microbios. 1991, 65 (263): 111-125.PubMed
62.
go back to reference Gough PJ, Gordon S: The role of scavenger receptors in the innate immune system. Microbes Infect. 2000, 2 (3): 305-311. 10.1016/S1286-4579(00)00297-5.CrossRefPubMed Gough PJ, Gordon S: The role of scavenger receptors in the innate immune system. Microbes Infect. 2000, 2 (3): 305-311. 10.1016/S1286-4579(00)00297-5.CrossRefPubMed
63.
go back to reference Court N, Vasseur V, Vacher R, Fremond C, Shebzukhov Y, Yeremeev VV, Maillet I, Nedospasov SA, Gordon S, Fallon PG, et al: Partial redundancy of the pattern recognition receptors, scavenger receptors, and C-type lectins for the long-term control of Mycobacterium tuberculosis infection. J Immunol. 184 (12): 7057-7070. 10.4049/jimmunol.1000164. Court N, Vasseur V, Vacher R, Fremond C, Shebzukhov Y, Yeremeev VV, Maillet I, Nedospasov SA, Gordon S, Fallon PG, et al: Partial redundancy of the pattern recognition receptors, scavenger receptors, and C-type lectins for the long-term control of Mycobacterium tuberculosis infection. J Immunol. 184 (12): 7057-7070. 10.4049/jimmunol.1000164.
64.
go back to reference Doz E, Rose S, Nigou J, Gilleron M, Puzo G, Erard F, Ryffel B, Quesniaux VF: Acylation determines the toll-like receptor (TLR)-dependent positive versus TLR2-, mannose receptor-, and SIGNR1-independent negative regulation of pro-inflammatory cytokines by mycobacterial lipomannan. J Biol Chem. 2007, 282 (36): 26014-26025. 10.1074/jbc.M702690200.CrossRefPubMed Doz E, Rose S, Nigou J, Gilleron M, Puzo G, Erard F, Ryffel B, Quesniaux VF: Acylation determines the toll-like receptor (TLR)-dependent positive versus TLR2-, mannose receptor-, and SIGNR1-independent negative regulation of pro-inflammatory cytokines by mycobacterial lipomannan. J Biol Chem. 2007, 282 (36): 26014-26025. 10.1074/jbc.M702690200.CrossRefPubMed
65.
go back to reference Gowda DC: TLR-mediated cell signaling by malaria GPIs. Trends Parasitol. 2007, 23 (12): 596-604. 10.1016/j.pt.2007.09.003.CrossRefPubMed Gowda DC: TLR-mediated cell signaling by malaria GPIs. Trends Parasitol. 2007, 23 (12): 596-604. 10.1016/j.pt.2007.09.003.CrossRefPubMed
66.
go back to reference Fortune SM, Solache A, Jaeger A, Hill PJ, Belisle JT, Bloom BR, Rubin EJ, Ernst JD: Mycobacterium tuberculosis inhibits macrophage responses to IFN-gamma through myeloid differentiation factor 88-dependent and -independent mechanisms. J Immunol. 2004, 172 (10): 6272-6280.CrossRefPubMed Fortune SM, Solache A, Jaeger A, Hill PJ, Belisle JT, Bloom BR, Rubin EJ, Ernst JD: Mycobacterium tuberculosis inhibits macrophage responses to IFN-gamma through myeloid differentiation factor 88-dependent and -independent mechanisms. J Immunol. 2004, 172 (10): 6272-6280.CrossRefPubMed
67.
go back to reference Banaiee N, Kincaid EZ, Buchwald U, Jacobs WR, Ernst JD: Potent inhibition of macrophage responses to IFN-gamma by live virulent Mycobacterium tuberculosis is independent of mature mycobacterial lipoproteins but dependent on TLR2. J Immunol. 2006, 176 (5): 3019-3027.CrossRefPubMed Banaiee N, Kincaid EZ, Buchwald U, Jacobs WR, Ernst JD: Potent inhibition of macrophage responses to IFN-gamma by live virulent Mycobacterium tuberculosis is independent of mature mycobacterial lipoproteins but dependent on TLR2. J Immunol. 2006, 176 (5): 3019-3027.CrossRefPubMed
68.
go back to reference Noss EH, Pai RK, Sellati TJ, Radolf JD, Belisle J, Golenbock DT, Boom WH, Harding CV: Toll-like receptor 2-dependent inhibition of macrophage class II MHC expression and antigen processing by 19-kDa lipoprotein of Mycobacterium tuberculosis. J Immunol. 2001, 167 (2): 910-918.CrossRefPubMed Noss EH, Pai RK, Sellati TJ, Radolf JD, Belisle J, Golenbock DT, Boom WH, Harding CV: Toll-like receptor 2-dependent inhibition of macrophage class II MHC expression and antigen processing by 19-kDa lipoprotein of Mycobacterium tuberculosis. J Immunol. 2001, 167 (2): 910-918.CrossRefPubMed
69.
go back to reference Weiss DJ, Souza CD, Evanson OA, Sanders M, Rutherford M: Bovine monocyte TLR2 receptors differentially regulate the intracellular fate of Mycobacterium avium subsp. paratuberculosis and Mycobacterium avium subsp. avium. J Leukoc Biol. 2008, 83 (1): 48-55. 10.1189/jlb.0707490.CrossRefPubMed Weiss DJ, Souza CD, Evanson OA, Sanders M, Rutherford M: Bovine monocyte TLR2 receptors differentially regulate the intracellular fate of Mycobacterium avium subsp. paratuberculosis and Mycobacterium avium subsp. avium. J Leukoc Biol. 2008, 83 (1): 48-55. 10.1189/jlb.0707490.CrossRefPubMed
70.
go back to reference Hu X, Paik PK, Chen J, Yarilina A, Kockeritz L, Lu TT, Woodgett JR, Ivashkiv LB: IFN-gamma suppresses IL-10 production and synergizes with TLR2 by regulating GSK3 and CREB/AP-1 proteins. Immunity. 2006, 24 (5): 563-574. 10.1016/j.immuni.2006.02.014.CrossRefPubMed Hu X, Paik PK, Chen J, Yarilina A, Kockeritz L, Lu TT, Woodgett JR, Ivashkiv LB: IFN-gamma suppresses IL-10 production and synergizes with TLR2 by regulating GSK3 and CREB/AP-1 proteins. Immunity. 2006, 24 (5): 563-574. 10.1016/j.immuni.2006.02.014.CrossRefPubMed
71.
go back to reference Yamamoto N, Ikeda H, Tandon NN, Herman J, Tomiyama Y, Mitani T, Sekiguchi S, Lipsky R, Kralisz U, Jamieson GA: A platelet membrane glycoprotein (GP) deficiency in healthy blood donors: Naka-platelets lack detectable GPIV (CD36). Blood. 1990, 76 (9): 1698-1703.PubMed Yamamoto N, Ikeda H, Tandon NN, Herman J, Tomiyama Y, Mitani T, Sekiguchi S, Lipsky R, Kralisz U, Jamieson GA: A platelet membrane glycoprotein (GP) deficiency in healthy blood donors: Naka-platelets lack detectable GPIV (CD36). Blood. 1990, 76 (9): 1698-1703.PubMed
72.
go back to reference Curtis BR, Aster RH: Incidence of the Nak(a)-negative platelet phenotype in African Americans is similar to that of Asians. Transfusion. 1996, 36 (4): 331-334. 10.1046/j.1537-2995.1996.36496226147.x.CrossRefPubMed Curtis BR, Aster RH: Incidence of the Nak(a)-negative platelet phenotype in African Americans is similar to that of Asians. Transfusion. 1996, 36 (4): 331-334. 10.1046/j.1537-2995.1996.36496226147.x.CrossRefPubMed
73.
go back to reference Tomiyama Y, Take H, Ikeda H, Mitani T, Furubayashi T, Mizutani H, Yamamoto N, Tandon NN, Sekiguchi S, Jamieson GA, et al: Identification of the platelet-specific alloantigen, Naka, on platelet membrane glycoprotein IV. Blood. 1990, 75 (3): 684-687.PubMed Tomiyama Y, Take H, Ikeda H, Mitani T, Furubayashi T, Mizutani H, Yamamoto N, Tandon NN, Sekiguchi S, Jamieson GA, et al: Identification of the platelet-specific alloantigen, Naka, on platelet membrane glycoprotein IV. Blood. 1990, 75 (3): 684-687.PubMed
75.
go back to reference Aitman TJ, Cooper LD, Norsworthy PJ, Wahid FN, Gray JK, Curtis BR, McKeigue PM, Kwiatkowski D, Greenwood BM, Snow RW, et al: Malaria susceptibility and CD36 mutation. Nature. 2000, 405 (6790): 1015-1016. 10.1038/35016636.CrossRefPubMed Aitman TJ, Cooper LD, Norsworthy PJ, Wahid FN, Gray JK, Curtis BR, McKeigue PM, Kwiatkowski D, Greenwood BM, Snow RW, et al: Malaria susceptibility and CD36 mutation. Nature. 2000, 405 (6790): 1015-1016. 10.1038/35016636.CrossRefPubMed
76.
go back to reference Fry AE, Ghansa A, Small KS, Palma A, Auburn S, Diakite M, Green A, Campino S, Teo YY, Clark TG, et al: Positive selection of a CD36 nonsense variant in sub-Saharan Africa, but no association with severe malaria phenotypes. Hum Mol Genet. 2009, 18 (14): 2683-2692. 10.1093/hmg/ddp192.CrossRefPubMedPubMedCentral Fry AE, Ghansa A, Small KS, Palma A, Auburn S, Diakite M, Green A, Campino S, Teo YY, Clark TG, et al: Positive selection of a CD36 nonsense variant in sub-Saharan Africa, but no association with severe malaria phenotypes. Hum Mol Genet. 2009, 18 (14): 2683-2692. 10.1093/hmg/ddp192.CrossRefPubMedPubMedCentral
Metadata
Title
CD36 deficiency attenuates experimental mycobacterial infection
Authors
Michael Hawkes
Xiaoming Li
Maryanne Crockett
Angelina Diassiti
Constance Finney
Gundula Min-Oo
W Conrad Liles
Jun Liu
Kevin C Kain
Publication date
01-12-2010
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2010
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/1471-2334-10-299

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