Perturbed microRNA expression by Mycobacterium tuberculosis promotes macrophage polarization leading to pro-survival foam cell

Frontiers in Immunology

Volumn 8, Issue FEB, 2017, Pages

  Ahluwalia, Pankaj Kumar ^a   Pandey, Rajan Kumar ^b   Sehajpal, Prabodh Kumar ^a   Prajapati, Vijay Kumar ^b  

^a GURU NANAK DEV UNIVERSITY   (India)

^b CENTRAL UNIVERSITY OF RAJASTHAN   (India)

Author keywords

Foam cells; Granuloma; Macrophage polarization; MiRNAs; Mycobacterium tuberculosis

Indexed keywords

MICRORNA; MICRORNA 130A; MICRORNA 130B; MICRORNA 135A 5P; MICRORNA 135B 5P; MICRORNA 155; MICRORNA 27A; MICRORNA 27B; MICRORNA 302C; MICRORNA 33; MICRORNA 454; MICRORNA 455 3P; MICRORNA 520B; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BIOINFORMATICS; CELL SURVIVAL; DOWN REGULATION; FOAM CELL; HUMAN; HUMAN CELL; MACROPHAGE; MRNA EXPRESSION ASSAY; MYCOBACTERIUM TUBERCULOSIS; PHENOTYPE; POLARIZATION; PROTEIN ANALYSIS; RNA SEQUENCE;

EID: 85014386847     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2017.00107     Document Type: Article

References (67)

1. O'Garra A, Redford PS, McNab FW, Bloom CI, Wilkinson RJ, Berry MP. The immune response in tuberculosis. Annu Rev Immunol (2013) 31:475-527. doi: 10.1146/annurev-immunol-032712-095939
2. Bates JH, Potts WE, Lewis M. Epidemiology of primary tuberculosis in an industrial school. N Engl J Med (1965) 272:714-7. doi:10.1056/NEJM196504082721403
3. World Health Organization. Global Tuberculosis Report. (2016).
4. Zumla A, Rao M, Wallis RS, Kaufmann SH, Rustomjee R, Mwaba P, et al. Host-directed therapies for infectious diseases: current status, recent progress, and future prospects. Lancet Infect Dis (2016) 16:e47-63. doi:10.1016/S1473-3099(16)00078-5
5. Srinivasan L, Ahlbrand S, Briken V. Interaction of Mycobacterium tuberculosis with host cell death pathways. Cold Spring Harb Perspect Med (2014) 4:a022459. doi:10.1101/cshperspect.a022459
6. Armstrong J, Hart PA. Response of cultured macrophages to Mycobacterium tuberculosis, with observations on fusion of lysosomes with phagosomes. J Exp Med (1971) 134:713-40. doi:10.1084/jem.134.3.713
7. Vergne I, Fratti RA, Hill PJ, Chua J, Belisle J, Deretic V. Mycobacterium tuberculosis phagosome maturation arrest: mycobacterial phosphatidylinositol analog phosphatidylinositol mannoside stimulates early endosomal fusion. Mol Biol Cell (2004) 15:751-60. doi:10.1091/mbc. E03-05-0307
8. Pandey RK, Sundar S, Prajapati VK. Differential expression of miRNA regulates T cell differentiation and plasticity during visceral leishmaniasis infection. Front Microbiol (2016) 7:206. doi:10.3389/fmicb.2016.00206
9. Hasan Z, Jamil B, Ashraf M, Islam M, Yusuf MS, Khan JA, et al. ESAT6-induced IFNγ and CXCL9 can differentiate severity of tuberculosis. PLoS One (2009) 4:e5158. doi:10.1371/journal.pone.0005158
10. Mantovani A, Sica A, Locati M. Macrophage polarization comes of age. Immunity (2005) 23:344-6. doi:10.1016/j.immuni.2005.10.001
11. Gordon S. Alternative activation of macrophages. Nat Rev Immunol (2003) 3:23-35. doi:10.1038/nri978
12. Ramakrishnan L. Revisiting the role of the granuloma in tuberculosis. Nat Rev Immunol (2012) 12:352-66. doi:10.1038/nri3211
13. Galkina E, Ley K. Immune and inflammatory mechanisms of atherosclerosis (*). Annu Rev Immunol (2009) 27:165-97. doi:10.1146/annurev.immunol.021908.132620
14. Singh V, Jamwal S, Jain R, Verma P, Gokhale R, Rao KV. Mycobacterium tuberculosis-driven targeted recalibration of macrophage lipid homeostasis promotes the foamy phenotype. Cell Host Microbe (2012) 12:669-81. doi:10.1016/j.chom.2012.09.012
15. Bouhlel MA, Derudas B, Rigamonti E, Dièvart R, Brozek J, Haulon S, et al. PPARγ activation primes human monocytes into alternative M2 macrophages with anti-inflammatory properties. Cell Metab (2007) 6:137-43. doi:10.1016/j.cmet.2007.06.010
16. Peyron P, Vaubourgeix J, Poquet Y, Levillain F, Botanch C, Bardou F, et al. Foamy macrophages from tuberculous patients' granulomas constitute a nutrient-rich reservoir for M. tuberculosis persistence. PLoS Pathog (2008) 4:e1000204. doi:10.1371/journal.ppat.1000204
17. Huang Z, Luo Q, Guo Y, Chen J, Xiong G, Peng Y, et al. Mycobacterium tuberculosis-induced polarization of human macrophage orchestrates the formation and development of tuberculous granulomas in vitro. PLoS One (2015) 10:e0129744. doi:10.1371/journal.pone.0129744
18. Ellwanger DC, Buttner FA, Mewes HW, Stumpflen V. The sufficient minimal set of miRNA seed types. Bioinformatics (2011) 27:1346-50. doi:10.1093/bioinformatics/btr149
19. Bartel DP. microRNAs: genomics, biogenesis, mechanism, and function. Cell (2004) 116:281-97. doi:10.1016/S0092-8674(04)00045-5
20. Mehta A, Baltimore D. microRNAs as regulatory elements in immune system logic. Nat Rev Immunol (2016) 16:279-94. doi:10.1038/nri.2016.65
21. Baer M, Dillner A, Schwartz RC, Sedon C, Nedospasov S, Johnson PF. Tumor necrosis factor alpha transcription in macrophages is attenuated by an autocrine factor that preferentially induces NF-kappaB p50. Mol Cell Biol (1998) 18:5678-89. doi:10.1128/MCB.18.10.5678
22. Roy S, Charboneau R, Cain K, DeTurris S, Melnyk D, Barke RA. Deficiency of the transcription factor c-fos increases lipopolysaccharide-induced macrophage interleukin 12 production. Surgery (1999) 126:239-47. doi:10.1016/S0039-6060(99)70161-3
23. Wang J, Li BX, Ge PP, Li J, Wang Q, Gao GF, et al. Mycobacterium tuberculosis suppresses innate immunity by coopting the host ubiquitin system. Nat Immunol (2015) 16:237-45. doi:10.1038/ni.3096
24. Dai Y, Zhou X. Computational methods for the identification of microRNA targets. Open Access Bioinformatics (2010) 2:29-39. doi:10.2147/OAB.S6902
25. To KK. microRNA: a prognostic biomarker and a possible druggable target for circumventing multidrug resistance in cancer chemotherapy. J Biomed Sci (2013) 20:99. doi:10.1186/1423-0127-20-99
26. Krausgruber T, Blazek K, Smallie T, Alzabin S, Lockstone H, Sahgal N, et al. IRF5 promotes inflammatory macrophage polarization and TH1-TH17 responses. Nat Immunol (2011) 12:231-8. doi:10.1038/ni.1990
27. Negishi H, Fujita Y, Yanai H, Sakaguchi S, Ouyang X, Shinohara M, et al. Evidence for licensing of IFN-gamma-induced IFN regulatory factor 1 transcription factor by MyD88 in toll-like receptor-dependent gene induction program. Proc Natl Acad Sci U S A (2006) 103:15136-41. doi:10.1073/pnas.0607181103
28. Wilson HM. SOCS proteins in macrophage polarization and function. Front Immunol (2014) 5:357. doi:10.3389/fimmu.2014.00357
29. Lawrence T, Natoli G. Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat Rev Immunol (2011) 11:750-61. doi:10.1038/nri3088
30. Tone M, Powell MJ, Tone Y, Thompson SA, Waldmann H. IL-10 gene expression is controlled by the transcription factors Sp1 and Sp3. J Immunol (2000) 165:286-91. doi:10.4049/jimmunol.165.1.286
31. Odegaard JI, Chawla A. Alternative macrophage activation and metabolism. Annu Rev Pathol (2011) 6:275-97. doi:10.1146/annurev-pathol-011110-130138
32. Straus DS, Glass CK. Anti-inflammatory actions of PPAR ligands: new insights on cellular and molecular mechanisms. Trends Immunol (2007) 28:551-8. doi:10.1016/j.it.2007.09.003
33. Liao X, Sharma N, Kapadia F, Zhou G, Lu Y, Hong H, et al. Kruppel-like factor 4 regulates macrophage polarization. J Clin Invest (2011) 121:2736-49. doi:10.1172/JCI45444
34. Agarwal V, Bell GW, Nam JW, Bartel DP. Predicting effective microRNA target sites in mammalian mRNAs. Elife (2015) 4:e05005. doi:10.7554/eLife.05005
35. Maragkakis M, Alexiou P, Papadopoulos GL, Reczko M, Dalamagas T, Giannopoulos G, et al. Accurate microRNA target prediction correlates with protein repression levels. BMC Bioinformatics (2009) 10:295. doi:10.1186/1471-2105-10-295
36. Wang X, El Naqa IM. Prediction of both conserved and nonconserved microRNA targets in animals. Bioinformatics (2008) 24:325-32. doi:10.1093/bioinformatics/btm595
37. Betel D, Koppal A, Agius P, Sander C, Leslie C. Comprehensive modeling of microRNA targets predicts functional non-conserved and non-canonical sites. Genome Biol (2010) 11:R90. doi:10.1186/gb-2010-11-8-r90
38. Hsu SD, Chu CH, Tsou AP, Chen SJ, Chen HC, Hsu PW, et al. miRNAMap 2.0: genomic maps of microRNAs in metazoan genomes. Nucleic Acids Res (2008) 36:D165-9. doi:10.1093/nar/gkm1012
39. Wang X. miRDB: a microRNA target prediction and functional annotation database with a wiki interface. RNA (2008) 14:1012-7. doi:10.1261/rna.965408
40. Miranda KC, Huynh T, Tay Y, Ang YS, Tam WL, Thomson AM, et al. A pattern-based method for the identification of microRNA binding sites and their corresponding heteroduplexes. Cell (2006) 126:1203-17. doi:10.1016/j.cell.2006.07.031
41. Verreck FA, de Boer T, Langenberg DM, Hoeve MA, Kramer M, Vaisberg E, et al. Human IL-23-producing type 1 macrophages promote but IL-10-producing type 2 macrophages subvert immunity to (myco)bacteria. Proc Natl Acad Sci U S A (2004) 101:4560-5. doi:10.1073/pnas.0400983101
42. Latchman DS. Transcription factors: an overview. Int J Biochem Cell Biol (1997) 29:1305-12. doi:10.1016/S1357-2725(97)00085-X
43. Rao A, Luo C, Hogan PG. Transcription factors of the NFAT family: regulation and function. Annu Rev Immunol (1997) 15:707-47. doi:10.1146/annurev.immunol.15.1.707
44. Furci L, Schena E, Miotto P, Cirillo DM. Alteration of human macrophages microRNA expression profile upon infection with Mycobacterium tuberculosis. Int J Mycobacteriol (2013) 2:128-34. doi:10.1016/j.ijmyco.2013.04.006
45. Zheng L, Leung E, Lee N, Lui G, To KF, Chan RC, et al. Differential microRNA expression in human macrophages with Mycobacterium tuberculosis infection of Beijing/W and non-Beijing/W strain types. PLoS One (2015) 10:e0126018. doi:10.1371/journal.pone.0126018
46. Rajaram MV, Ni B, Morris JD, Brooks MN, Carlson TK, Bakthavachalu B, et al. Mycobacterium tuberculosis lipomannan blocks TNF biosynthesis by regulating macrophage MAPK-activated protein kinase 2 (MK2) and microRNA miR-125b. Proc Natl Acad Sci U S A (2011) 108:17408-13. doi:10.1073/pnas.1112660108
47. Xu G, Zhang Z, Wei J, Zhang Y, Zhang Y, Guo L, et al. microR-142-3p down-regulates IRAK-1 in response to Mycobacterium bovis BCG infection in macrophages. Tuberculosis (Edinb) (2013) 93:606-11. doi:10.1016/j.tube.2013.08.006
48. Ni B, Rajaram MV, Lafuse WP, Landes MB, Schlesinger LS. Mycobacterium tuberculosis decreases human macrophage IFN-gamma responsiveness through miR-132 and miR-26a. J Immunol (2014) 193:4537-47. doi:10.4049/jimmunol.1400124
49. Borden EC, Sen GC, Uze G, Silverman RH, RansohoffRM, Foster GR, et al. Interferons at age 50: past, current and future impact on biomedicine. Nat Rev Drug Discov (2007) 6:975-90. doi:10.1038/nrd2422
50. Roy S, Guler R, Parihar SP, Schmeier S, Kaczkowski B, Nishimura H, et al. Batf2/Irf1 induces inflammatory responses in classically activated macrophages, lipopolysaccharides, and mycobacterial infection. J Immunol (2015) 194:6035-44. doi:10.4049/jimmunol.1402521
51. Satoh T, Takeuchi O, Vandenbon A, Yasuda K, Tanaka Y, Kumagai Y, et al. The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection. Nat Immunol (2010) 11:936-44. doi:10.1038/ni.1920
52. Darnell JE Jr, Kerr IM, Stark GR. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science (1994) 264:1415-21. doi:10.1126/science.8197455
53. Whyte CS, Bishop ET, Ruckerl D, Gaspar-Pereira S, Barker RN, Allen JE, et al. Suppressor of cytokine signaling (SOCS)1 is a key determinant of differential macrophage activation and function. J Leukoc Biol (2011) 90:845-54. doi:10.1189/jlb.1110644
54. Arnold CE, Whyte CS, Gordon P, Barker RN, Rees AJ, Wilson HM. A critical role for suppressor of cytokine signalling 3 in promoting M1 macrophage activation and function in vitro and in vivo. Immunology (2014) 141:96-110. doi:10.1111/imm.12173
55. Takeda K, Tanaka T, Shi W, Matsumoto M, Minami M, Kashiwamura S, et al. Essential role of Stat6 in IL-4 signalling. Nature (1996) 380:627-30. doi:10.1038/380627a0
56. Daniel J, Maamar H, Deb C, Sirakova TD, Kolattukudy PE. Mycobacterium tuberculosis uses host triacylglycerol to accumulate lipid droplets and acquires a dormancy-like phenotype in lipid-loaded macrophages. PLoS Pathog (2011) 7:e1002093. doi:10.1371/journal.ppat.1002093
57. Chinetti G, Lestavel S, Bocher V, Remaley AT, Neve B, Torra IP, et al. PPAR-alpha and PPAR-gamma activators induce cholesterol removal from human macrophage foam cells through stimulation of the ABCA1 pathway. Nat Med (2001) 7:53-8. doi:10.1038/83348
58. Miner MD, Chang JC, Pandey AK, Sassetti CM, Sherman DR. Role of cholesterol in Mycobacterium tuberculosis infection. Indian J Exp Biol (2009) 47:407-11.
59. Tian FJ, An LN, Wang GK, Zhu JQ, Li Q, Zhang YY, et al. Elevated microRNA-155 promotes foam cell formation by targeting HBP1 in atherogenesis. Cardiovasc Res (2014) 103:100-10. doi:10.1093/cvr/cvu070
60. Kumar R, Halder P, Sahu SK, Kumar M, Kumari M, Jana K, et al. Identification of a novel role of ESAT-6-dependent miR-155 induction during infection of macrophages with Mycobacterium tuberculosis. Cell Microbiol (2012) 14:1620-31. doi:10.1111/j.1462-5822.2012.01827.x
61. Wu J, Lu C, Diao N, Zhang S, Wang S, Wang F, et al. Analysis of microRNA expression profiling identifies miR-155 and miR-155* as potential diagnostic markers for active tuberculosis: a preliminary study. Hum Immunol (2012) 73:31-7. doi:10.1016/j.humimm.2011.10.003
62. Harris J, De Haro SA, Master SS, Keane J, Roberts EA, Delgado M, et al. T helper 2 cytokines inhibit autophagic control of intracellular Mycobacterium tuberculosis. Immunity (2007) 27:505-17. doi:10.1016/j.immuni.2007.07.022
63. Najafi-Shoushtari SH, Kristo F, Li Y, Shioda T, Cohen DE, Gerszten RE, et al. microRNA-33 and the SREBP host genes cooperate to control cholesterol homeostasis. Science (2010) 328:1566-9. doi:10.1126/science.1189123
64. Rayner KJ, Suarez Y, Davalos A, Parathath S, Fitzgerald ML, Tamehiro N, et al. miR-33 contributes to the regulation of cholesterol homeostasis. Science (2010) 328:1570-3. doi:10.1126/science.1189862
65. Brooks MN, Rajaram MV, Azad AK, Amer AO, Valdivia-Arenas MA, Park JH, et al. NOD2 controls the nature of the inflammatory response and subsequent fate of Mycobacterium tuberculosis and M. bovis BCG in human macrophages. Cell Microbiol (2011) 13:402-18. doi:10.1111/j.1462-5822.2010.01544.x
66. Ouimet M, Koster S, Sakowski E, Ramkhelawon B, van Solingen C, Oldebeken S, et al. Mycobacterium tuberculosis induces the miR-33 locus to reprogram autophagy and host lipid metabolism. Nat Immunol (2016) 17:677-86. doi:10.1038/ni.3434
67. Zhang M, Wu JF, Chen WJ, Tang SL, Mo ZC, Tang YY, et al. microRNA-27a/b regulates cellular cholesterol efflux, influx and esterification/hydrolysis in THP-1 macrophages. Atherosclerosis (2014) 234:54-64. doi:10.1016/j.atherosclerosis.2014.02.008