Mycobacterium tuberculosis infection of the 'non-classical immune cell'

Immunology and Cell Biology

Volumn 93, Issue 9, 2015, Pages 789-795

  Randall, Philippa J ^a   Hsu, Nai Jen ^a   Quesniaux, Valerie ^b   Ryffel, Bernhard ^b   Jacobs, Muazzam ^a,c  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b UNIVERSITÉ D'ORLÉANS   (France)

^c NATIONAL HEALTH LABORATORY SERVICE   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOCYTE; ANTIGEN PRESENTATION; BACILLI; BACTERIAL GROWTH; ENDOTHELIUM CELL; EPITHELIUM CELL; FIBROBLAST; GLIA; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; NONHUMAN; OUTCOME ASSESSMENT; REVIEW; TUBERCULOSIS; BIOLOGICAL MODEL; IMMUNOLOGY; MICROBIOLOGY; MYCOBACTERIUM TUBERCULOSIS; NERVE CELL; PHYSIOLOGY;

ADIPOCYTES; ENDOTHELIAL CELLS; EPITHELIAL CELLS; FIBROBLASTS; HUMANS; MODELS, IMMUNOLOGICAL; MYCOBACTERIUM TUBERCULOSIS; NEUROGLIA; NEURONS; TUBERCULOSIS;

EID: 84945481706     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2015.43     Document Type: Review

References (97)

1. Garg RK. Tuberculosis of the central nervous system. Postgrad Med J 1999; 75: 133-140
2. Be NA, Kim KS, Bishai WR, Jain SK. Pathogenesis of central nervous system tuberculosis. Curr Mol Med 2009; 9: 94-99
3. WHO. Global Tuberculosis Report. WHO Press: Geneva, 2013
4. Balasubramanian V, Wiegeshaus EH, Taylor BT, Smith DW. Pathogenesis of tuberculosis: pathway to apical localization. Tuber Lung Dis 1994; 75: 168-178
5. Mehta PK, King CH, White EH, Murtagh JJ Jr, Quinn FD. Comparison of in vitro models for the study of Mycobacterium tuberculosis invasion and intracellular replication. Infect Immun 1996; 64: 2673-2679
6. Arriaga AK, Orozco EH, Aguilar LD, Rook GA, Hernandez Pando R. Immunological and pathological comparative analysis between experimental latent tuberculous infection and progressive pulmonary tuberculosis. Clin Exp Immunol 2002; 128: 229-237
7. Hernandez-Pando R, Jeyanathan M, Mengistu G, Aguilar D, Orozco H, Harboe M, et al. Persistence of DNA from Mycobacterium tuberculosis in superficially normal lung tissue during latent infection. Lancet 2000; 356: 2133-2138
8. Barrios-Payan J, Saqui-Salces M, Jeyanathan M, Alcantara-Vazquez A, Castanon-Arreola M, Rook G, et al. Extrapulmonary locations of Mycobacterium tuberculosis DNA during latent infection. J Infect Dis 2012; 206: 1194-1205
9. Garcia-Perez BE, Mondragon-Flores R, Luna-Herrera J. Internalization of Mycobacterium tuberculosis by macropinocytosis in non-phagocytic cells. Microb Pathog 2003; 35: 49-55
10. Teitelbaum R, Schubert W, Gunther L, Kress Y, Macaluso F, Pollard JW, et al. The M cell as a portal of entry to the lung for the bacterial pathogen Mycobacterium tuberculosis. Immunity 1999; 10: 641-650
11. Shepard CC. Growth characteristics of tubercle bacilli and certain other mycobacteria in HeLa cells. J Exp Med 1957; 105: 39-48
12. Shepard CC. A comparison of the growth of selected mycobacteria in HeLa, monkey kidney, and human amnion cells in tissue culture. J Exp Med 1958; 107: 237-246
13. Boots AM, Wimmers-Bertens AJ, Rijnders AW. Antigen-presenting capacity of rheumatoid synovial fibroblasts. Immunology 1994; 82: 268-274
14. Desruisseaux MS, Nagajyothi, Trujillo ME, Tanowitz HB, Scherer PE. Adipocyte, adipose tissue, and infectious disease. Infect Immun 2007; 75: 1066-1078
15. Garcia-Perez BE, Villagomez-Palatto DA, Castaneda-Sanchez JI, Coral-Vazquez RM, Ramirez-Sanchez I, Ordonez-Razo RM, et al. Innate response of human endothelial cells infected with mycobacteria. Immunobiology 2011; 216: 925-935
16. Jin Y, Lundkvist G, Dons L, Kristensson K, Rottenberg ME. Interferon-gamma mediates neuronal killing of intracellular bacteria. Scand J Immunol 2004; 60: 437-448
17. Roy S, Sharma S, Sharma M, Aggarwal R, Bose M. Induction of nitric oxide release from the human alveolar epithelial cell line A549: an in vitro correlate of innate immune response to Mycobacterium tuberculosis. Immunology 2004; 112: 471-480
18. Desvignes L, Ernst JD. Interferon-gamma-responsive nonhematopoietic cells regulate the immune response to Mycobacterium tuberculosis. Immunity 2009; 31: 974-985
19. Wieland CW, Florquin S, Chan ED, Leemans JC, Weijer S, Verbon A, et al. Pulmonary Mycobacterium tuberculosis infection in leptin-deficient ob/ob mice. Int Immunol 2005; 17: 1399-1408
20. van Crevel R, Ottenhoff TH, van der Meer JW. Innate immunity to Mycobacterium tuberculosis. Clin Microbiol Rev 2002; 15: 294-309
21. Saiga H, Shimada Y, Takeda K. Innate immune effectors in mycobacterial infection. Clin Dev Immunol 2011; 2011: 347594
22. Vir P, Gupta D, Agarwal R, Verma I. Immunomodulation of alveolar epithelial cells by Mycobacterium tuberculosis phosphatidylinositol mannosides results in apoptosis. APMIS 2014; 122: 268-282
23. Hallstrand TS, Hackett TL, Altemeier WA, Matute-Bello G, Hansbro PM, Knight DA. Airway epithelial regulation of pulmonary immune homeostasis and inflammation. Clin Immunol 2014; 151: 1-15
24. Lin Y, Zhang M, Barnes PF. Chemokine production by a human alveolar epithelial cell line in response to Mycobacterium tuberculosis. Infect Immun 1998; 66: 1121-1126
25. Sato K, Tomioka H, Shimizu T, Gonda T, Ota F, Sano C. Type II alveolar cells play roles in macrophage-mediated host innate resistance to pulmonary mycobacterial infections by producing proinflammatory cytokines. J Infect Dis 2002; 185: 1139-1147
26. Sharma M, Sharma S, Roy S, Varma S, Bose M. Pulmonary epithelial cells are a source of interferon-gamma in response to Mycobacterium tuberculosis infection. Immunol Cell Biol 2007; 85: 229-237
27. Nouailles G, Dorhoi A, Koch M, Zerrahn J, Weiner J 3rd, Fae KC, et al. CXCL5-secreting pulmonary epithelial cells drive destructive neutrophilic inflammation in tuberculosis. J Clin Invest 2014; 124: 1268-1282
28. Petursdottir DH, Chuquimia OD, Freidl R, Fernandez C. Macrophage control of phagocytosed mycobacteria is increased by factors secreted by alveolar epithelial cells through nitric oxide independent mechanisms. PLoS ONE 2014; 9: e103411
29. Smith KD. Iron metabolism at the host pathogen interface: lipocalin 2 and the pathogen-Associated iroA gene cluster. Int J Biochem Cell Biol 2007; 39: 1776-1780
30. Saiga H, Nishimura J, Kuwata H, Okuyama M, Matsumoto S, Sato S, et al. Lipocalin 2-dependent inhibition of mycobacterial growth in alveolar epithelium. J Immunol 2008; 181: 8521-8527
31. Guglani L, Gopal R, Rangel-Moreno J, Junecko BF, Lin Y, Berger T, et al. Lipocalin 2 regulates inflammation during pulmonary mycobacterial infections. PLoS ONE 2012; 7: e50052
32. Harriff MJ, Cansler ME, Toren KG, Canfield ET, Kwak S, Gold MC, et al. Human lung epithelial cells contain Mycobacterium tuberculosis in a late endosomal vacuole and are efficiently recognized by CD8+ T cells. PLoS ONE 2014; 9: e97515
33. McDonough KA, Kress Y. Cytotoxicity for lung epithelial cells is a virulence-Associated phenotype of Mycobacterium tuberculosis. Infect Immun 1995; 63: 4802-4811
34. Vir P, Gupta D, Agarwal R, Verma I. Interaction of alveolar epithelial cells with CFP21, a mycobacterial cutinase-like enzyme. Mol Cell Biochem 2014; 396: 187-199
35. Kinhikar AG, Verma I, Chandra D, Singh KK, Weldingh K, Andersen P, et al. Potential role for ESAT6 in dissemination of M. tuberculosis via human lung epithelial cells. Mol Microbiol 2010; 75: 92-106
36. Elkington PT, Emerson JE, Lopez-Pascua LD, O'Kane CM, Horncastle DE, Boyle JJ, et al. Mycobacterium tuberculosis up-regulates matrix metalloproteinase-1 secretion from human airway epithelial cells via a p38 MAPK switch. J Immunol 2005; 175: 5333-5340
37. Elkington PT, Green JA, Emerson JE, Lopez-Pascua LD, Boyle JJ, O'Kane CM, et al. Synergistic up-regulation of epithelial cell matrix metalloproteinase-9 secretion in tuberculosis. Am J Respir Cell Mol Biol 2007; 37: 431-437
38. Walker NF, Clark SO, Oni T, Andreu N, Tezera L, Singh S, et al. Doxycycline and HIV infection suppress tuberculosis-induced matrix metalloproteinases. Am J Respir Crit Care Med 2012; 185: 989-997
39. Kwan CK, Ernst JD. HIV and tuberculosis: a deadly human syndemic. Clin Microbiol Rev 2011; 24: 351-376
40. Price NM, Gilman RH, Uddin J, Recavarren S, Friedland JS. Unopposed matrix metalloproteinase-9 expression in human tuberculous granuloma and the role of TNF-Alpha-dependent monocyte networks. J Immunol 2003; 171: 5579-5586
41. Volkman HE, Pozos TC, Zheng J, Davis JM, Rawls JF, Ramakrishnan L. Tuberculous granuloma induction via interaction of a bacterial secreted protein with host epithelium. Science 2010; 327: 466-469
42. Shiryaev SA, Cieplak P, Aleshin AE, Sun Q, Zhu W, Motamedchaboki K, et al. Matrix metalloproteinase proteolysis of the mycobacterial HSP65 protein as a potential source of immunogenic peptides in human tuberculosis. FEBS J 2011; 278: 3277-3286
43. Neutra MR, Frey A, Kraehenbuhl JP. Epithelial M cells: gateways for mucosal infection and immunization. Cell 1996; 86: 345-348
44. Jones BD, Ghori N, Falkow S. Salmonella typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer's patches. J Exp Med 1994; 180: 15-23
45. Owen RL, Pierce NF, Apple RT, Cray WC Jr. M cell transport of Vibrio cholerae from the intestinal lumen into Peyer's patches: a mechanism for antigen sampling and for microbial transepithelial migration. J Infect Dis 1986; 153: 1108-1118
46. Allan CH, Mendrick DL, Trier JS. Rat intestinal M cells contain acidic endosomallysosomal compartments and express class II major histocompatibility complex determinants. Gastroenterology 1993; 104: 698-708
47. Finzi G, Cornaggia M, Capella C, Fiocca R, Bosi F, Solcia E, et al. Cathepsin E in follicle associated epithelium of intestine and tonsils: localization to M cells and possible role in antigen processing. Histochemistry 1993; 99: 201-211
48. Ueki T, Mizuno M, Uesu T, Kiso T, Tsuji T. Expression of ICAM-I on M cells covering isolated lymphoid follicles of the human colon. Acta Med Okayama 1995; 49: 145-151
49. Sumpio BE, Riley JT, Dardik A. Cells in focus: endothelial cell. Int J Biochem Cell Biol 2002; 34: 1508-1512
50. Birkness KA, Deslauriers M, Bartlett JH, White EH, King CH, Quinn FD. An in vitro tissue culture bilayer model to examine early events in Mycobacterium tuberculosis infection. Infect Immun 1999; 67: 653-658
51. Bermudez LE, Sangari FJ, Kolonoski P, Petrofsky M, Goodman J. The efficiency of the translocation of Mycobacterium tuberculosis across a bilayer of epithelial and endothelial cells as a model of the alveolar wall is a consequence of transport within mononuclear phagocytes and invasion of alveolar epithelial cells. Infect Immun 2002; 70: 140-146
52. Hoppe HC, de Wet BJ, Cywes C, Daffe M, Ehlers MR. Identification of phosphatidylinositol mannoside as a mycobacterial adhesin mediating both direct and opsonic binding to nonphagocytic mammalian cells. Infect Immun 1997; 65: 3896-3905
53. Haraldsen G, Sollid LM, Bakke O, Farstad IN, Kvale D, Molberg, et al. Major histocompatibility complex class II-dependent antigen presentation by human intestinal endothelial cells. Gastroenterology 1998; 114: 649-656
54. Mehta PK, Karls RK, White EH, Ades EW, Quinn FD. Entry and intracellular replication of Mycobacterium tuberculosis in cultured human microvascular endothelial cells. Microb Pathog 2006; 41: 119-124
55. Baltierra-Uribe SL, Garcia-Vasquez Mde J, Castrejon-Jimenez NS, Estrella-Pinon MP, Luna-Herrera J, Garcia-Perez BE. Mycobacteria entry and trafficking into endothelial cells. Can J Microbiol 2014; 60: 569-577
56. Ragno S, Romano M, Howell S, Pappin DJ, Jenner PJ, Colston MJ. Changes in gene expression in macrophages infected with Mycobacterium tuberculosis: a combined transcriptomic and proteomic approach. Immunology 2001; 104: 99-108
57. Feng CG, Britton WJ, Palendira U, Groat NL, Briscoe H, Bean AG. Up-regulation of VCAM-1 and differential expansion of beta integrin-expressing T lymphocytes are associated with immunity to pulmonary Mycobacterium tuberculosis infection. J Immunol 2000; 164: 4853-4860
58. Roberts LL, Robinson CM. Mycobacterium tuberculosis infection of human dendritic cells decreases integrin expression, adhesion and migration to chemokines. Immunology 2014; 141: 39-51
59. Blomgran R, Ernst JD. Lung neutrophils facilitate activation of naive antigen-specific CD4+ T cells during Mycobacterium tuberculosis infection. J Immunol 2011; 186: 7110-7119
60. Mariotti S, Sargentini V, Pardini M, Giannoni F, De Spirito M, Gagliardi MC, et al. Mycobacterium tuberculosis may escape helper T cell recognition by infecting human fibroblasts. Hum Immunol 2013; 74: 722-729
61. O'Kane CM, Boyle JJ, Horncastle DE, Elkington PT, Friedland JS. Monocyte-dependent fibroblast CXCL8 secretion occurs in tuberculosis and limits survival of mycobacteria within macrophages. J Immunol 2007; 178: 3767-3776
62. Gonzalez-Avila G, Sandoval C, Herrera MT, Ruiz V, Sommer B, Sada E, et al. Mycobacterium tuberculosis effects on fibroblast collagen metabolism. Respiration 2009; 77: 195-202
63. O'Kane CM, Elkington PT, Jones MD, Caviedes L, Tovar M, Gilman RH, et al. STAT3, p38 MAPK, and NF-kappaB drive unopposed monocyte-dependent fibroblast MMP-1 secretion in tuberculosis. Am J Respir Cell Mol Biol 2010; 43: 465-474
64. O'Kane CM, Elkington PT, Friedland JS. Monocyte-dependent oncostatin M and TNF-Alpha synergize to stimulate unopposed matrix metalloproteinase-1/3 secretion from human lung fibroblasts in tuberculosis. Eur J Immunol 2008; 38: 1321-1330
65. Singh S, Kubler A, Singh U, Singh A, Gardiner H, Prasad R, et al. Anti-mycobacterial drugs modulate immunopathogenic matrix metalloproteinases in a cellular model of pulmonary tuberculosis. Antimicrob Agents Chemother 2014; 58: 4657-4665
66. Rastogi N, Labrousse V, de Sousa JP. Mycobacterial growth and ultrastructure in mouse L-929 fibroblasts and bone marrow-derived macrophages: evidence that infected fibroblasts secrete mediators capable of modulating bacterial growth in macrophages. Curr Microbiol 1992; 25: 203-213
67. Khader SA, Guglani L, Rangel-Moreno J, Gopal R, Junecko BA, Fountain JJ, et al. IL-23 is required for long-Term control of Mycobacterium tuberculosis and B cell follicle formation in the infected lung. J Immunol 2011; 187: 5402-5407
68. Bechah Y, Paddock CD, Capo C, Mege JL, Raoult D. Adipose tissue serves as a reservoir for recrudescent Rickettsia prowazekii infection in a mouse model. PLoS ONE 2010; 5: e8547
69. Combs TP, Nagajyothi, Mukherjee S, de Almeida CJ, Jelicks LA, Schubert W, et al. The adipocyte as an important target cell for Trypanosoma cruzi infection. J Biol Chem 2005; 280: 24085-24094
70. Kim JS, Ryu MJ, Byun EH, Kim WS, Whang J, Min KN, et al. Differential immune response of adipocytes to virulent and attenuated Mycobacterium tuberculosis. Microbes Infect 2011; 13: 1242-1251
71. Neyrolles O, Hernandez-Pando R, Pietri-Rouxel F, Fornes P, Tailleux L, Barrios Payan JA, et al. Is adipose tissue a place for Mycobacterium tuberculosis persistence? PLoS ONE 2006; 1: e43
72. Agarwal P, Khan SR, Verma SC, Beg M, Singh K, Mitra K, et al. Mycobacterium tuberculosis persistence in various adipose depots of infected mice and the effect of anti-Tubercular therapy. Microbes Infect 2014; 16: 571-580
73. van Crevel R, Karyadi E, Netea MG, Verhoef H, Nelwan RH, West CE, et al. Decreased plasma leptin concentrations in tuberculosis patients are associated with wasting and inflammation. J Clin Endocrinol Metab 2002; 87: 758-763
74. Yuksel I, Sencan M, Dokmetas HS, Dokmetas I, Ataseven H, Yonem O. The relation between serum leptin levels and body fat mass in patients with active lung tuberculosis. Endocr Res 2003; 29: 257-264
75. Lord GM, Matarese G, Howard JK, Baker RJ, Bloom SR, Lechler RI. Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression. Nature 1998; 394: 897-901
76. Perna V, Perez-Perez A, Fernandez-Riejos P, Polo-Padillo J, Batista N, Dominguez-Castellano A, et al. Effective treatment of pulmonary tuberculosis restores plasma leptin levels. Eur Cytokine Netw 2013; 24: 157-161
77. Drevets DA, Leenen PJ, Greenfield RA. Invasion of the central nervous system by intracellular bacteria. Clin Microbiol Rev 2004; 17: 323-347
78. Carson MJ, Doose JM, Melchior B, Schmid CD, Ploix CC. CNS immune privilege: hiding in plain sight. Immunol Rev 2006; 213: 48-65
79. Farina C, Aloisi F, Meinl E. Astrocytes are active players in cerebral innate immunity. Trends Immunol 2007; 28: 138-145
80. Hanisch UK, Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 2007; 10: 1387-1394
81. Rock RB, Hu S, Gekker G, Sheng WS, May B, Kapur V, et al. Mycobacterium tuberculosis-induced cytokine and chemokine expression by human microglia and astrocytes: effects of dexamethasone. J Infect Dis 2005; 192: 2054-2058
82. Randall PJ, Hsu NJ, Lang D, Cooper S, Sebesho B, Allie N, et al. Neurons are host cells for Mycobacterium tuberculosis. Infect Immun 2014; 82: 1880-1890
83. Saito H, Tomioka H, Sato K, Watanabe T. Abilities of human oligodendroglial cells and mouse Schwann cells to phagocytose Mycobacterium leprae and other mycobacteria. Infect Immun 1986; 51: 157-162
84. Saito H, Tomioka H, Watanabe T, Sato K. Mechanisms of phagocytosis of Mycobacterium leprae and other mycobacteria by human oligodendroglial cells. Infect Immun 1986; 51: 163-167
85. Merrill JE, Scolding NJ. Mechanisms of damage to myelin and oligodendrocytes and their relevance to disease. Neuropathol Appl Neurobiol 1999; 25: 435-458
86. Appelt DM, Roupas MR, Way DS, Bell MG, Albert EV, Hammond CJ, et al. Inhibition of apoptosis in neuronal cells infected with Chlamydophila (Chlamydia) pneumoniae. BMC Neurosci 2008; 9: 13
87. Ovcinnikov NM, Delektorskij VV. Treponema pallidum in nerve fibres. Br J Vener Dis 1975; 51: 10-18
88. Pachner AR, Steiner I. Lyme neuroborreliosis: infection, immunity, and inflammation. Lancet Neurol 2007; 6: 544-552
89. Parra MC, Baquero F, Perez-Diaz JC. The role of apoptosis in Listeria monocytogenes neural infection: listeriolysin O interaction with neuroblastoma Neuro-2a cells. Infect Genet Evol 2008; 8: 59-67
90. Scollard DM. Endothelial cells and the pathogenesis of lepromatous neuritis: insights from the armadillo model. Microbes Infect 2000; 2: 1835-1843
91. Bowen S, Ateh DD, Deinhardt K, Bird MM, Price KM, Baker CS, et al. The phagocytic capacity of neurones. Eur J Neurosci 2007; 25: 2947-2955
92. van der Kleij H, Charles N, Karimi K, Mao YK, Foster J, Janssen L, et al. Evidence for neuronal expression of functional Fc (epsilon and gamma) receptors. J Allergy Clin Immunol 2010; 125: 757-760
93. Cebrian C, Zucca FA, Mauri P, Steinbeck JA, Studer L, Scherzer CR, et al. MHC-I expression renders catecholaminergic neurons susceptible to T-cell-mediated degeneration. Nat Commun 2014; 5: 3633
94. Chevalier G, Suberbielle E, Monnet C, Duplan V, Martin-Blondel G, Farrugia F, et al. Neurons are MHC class I-dependent targets for CD8 T cells upon neurotropic viral infection. PLoS Pathog 2011; 7: e1002393
95. Neumann H, Cavalie A, Jenne DE, Wekerle H. Induction of MHC class I genes in neurons. Science 1995; 269: 549-552
96. Andersson M, Lutay N, Hallgren O, Westergren-Thorsson G, Svensson M, Godaly G. Mycobacterium bovis bacilli Calmette-Guerin regulates leukocyte recruitment by modulating alveolar inflammatory responses. Innate Immun 2012; 18: 531-540
97. Bermudez LE, Goodman J. Mycobacterium tuberculosis invades and replicates within type II alveolar cells. Infect Immun 1996; 64: 1400-1406