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Abstract:

During mycobacterial infection, macroautophagy/autophagy, a process modulated by cytokines, is essential for mounting successful host responses. Autophagy collaborates with human immune responses against Mycobacterium tuberculosis (Mt) in association with specific IFNG secreted against the pathogen. However, IFNG alone is not sufficient to the complete bacterial eradication, and other cytokines might be required. Actually, induction of Th1 and Th17 immune responses are required for protection against Mt. Accordingly, we showed that IL17A and IFNG expression in lymphocytes from tuberculosis patients correlates with disease severity. Here we investigate the role of IFNG and IL17A during autophagy in monocytes infected with Mt H37Rv or the mutant MtΔRD1. Patients with active disease were classified as high responder (HR) or low responder (LR) according to their T cell responses against Mt. IL17A augmented autophagy in infected monocytes from HR patients through a mechanism that activated MAPK1/ERK2-MAPK3/ERK1 but, during infection of monocytes from LR patients, IL17A had no effect on the autophagic response. In contrast, addition of IFNG to infected monocytes, increased autophagy by activating MAPK14/p38 α both in HR and LR patients. Interestingly, proteins codified in the RD1 region did not interfere with IFNG and IL17A autophagy induction. Therefore, in severe tuberculosis patients' monocytes, IL17A was unable to augment autophagy because of a defect in the MAPK1/3 signaling pathway. In contrast, both IFNG and IL17A increased autophagy levels in patients with strong immunity to Mt, promoting mycobacterial killing. Our findings might contribute to recognize new targets for the development of novel therapeutic tools to fight the pathogen. © 2017 Taylor & Francis.

Registro:

Documento: Artículo
Título:IL17A augments autophagy in Mycobacterium tuberculosis-infected monocytes from patients with active tuberculosis in association with the severity of the disease
Autor:Tateosian, N.L.; Pellegrini, J.M.; Amiano, N.O.; Rolandelli, A.; Casco, N.; Palmero, D.J.; Colombo, M.I.; García, V.E.
Filiación:Departamento de Química Biológica. Facultad de Ciencias Exactas y Naturales. UBA, Ciudad Universitaria, Buenos Aires, Argentina
Universidad de Buenos Aires. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales (IQUIBICEN). Facultad de Ciencias Exactas y Naturales, Ciudad Universitaria, Buenos Aires, Argentina
División Tisioneumonología Hospital F.J. Muñiz, Buenos Aires, Argentina
Instituto de Histología y Embriología de Mendoza, Facultad de Ciencias Médicas, Universidad Nacional de Cuyo-CONICET, Mendoza, Argentina
Palabras clave:autophagy; cytokines; IFNG; IL17A; immune response; Mycobacterium tuberculosis; patients; tuberculosis; BCG vaccine; CD14 antigen; gamma interferon; interleukin 17; interleukin 17 receptor; interleukin 17 receptor A; mitogen activated protein kinase 1; mitogen activated protein kinase 14; mitogen activated protein kinase 3; phosphatidylinositol 3 kinase; tuberculostatic agent; unclassified drug; gamma interferon; IFNG protein, human; IL17A protein, human; interleukin 17; adherent cell; Article; autophagosome; autophagy; bacterial genome; bacterial growth; bactericidal activity; controlled study; disease classification; disease severity; enzyme activation; human; human cell; intracellular signaling; lung tuberculosis; lysosome; monocyte; Mycobacterium tuberculosis; peripheral blood mononuclear cell; phagosome; protein phosphorylation; upregulation; cell culture; immunology; microbiology; monocyte; Mycobacterium tuberculosis; physiology; signal transduction; tuberculosis; Autophagy; Cells, Cultured; Humans; Interferon-gamma; Interleukin-17; Monocytes; Mycobacterium tuberculosis; Signal Transduction; Tuberculosis
Año:2017
Volumen:13
Número:7
Página de inicio:1191
Página de fin:1204
DOI: http://dx.doi.org/10.1080/15548627.2017.1320636
Título revista:Autophagy
Título revista abreviado:Autophagy
ISSN:15548627
CAS:gamma interferon, 82115-62-6; mitogen activated protein kinase 1, 137632-08-7; mitogen activated protein kinase 3, 137632-07-6; phosphatidylinositol 3 kinase, 115926-52-8; IFNG protein, human; IL17A protein, human; Interferon-gamma; Interleukin-17
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_15548627_v13_n7_p1191_Tateosian

Referencias:

  • WHO (2016) Global tuberculosis report 2016
  • Cooper, A.M., Dalton, D.K., Stewart, T.A., Griffin, J.P., Russell, D.G., Orme, I.M., Disseminated tuberculosis in interferon gamma gene-disrupted mice (1993) J Exp Med, 178, pp. 2243-2247. , 8245795
  • Flynn, J.L., Chan, J., Triebold, K.J., Dalton, D.K., Stewart, T.A., Bloom, B.R., An essential role for interferon gamma in resistance to mycobacterium tuberculosis infection (1993) J Exp Med, 178, pp. 2249-2254. , 7504064
  • Newport, M.J., Huxley, C.M., Huston, S., Hawrylowicz, C.M., Oostra, B.A., Williamson, R., Levin, M., A mutation in the interferon-gamma-receptor gene and susceptibility to mycobacterial infection (1996) N Engl J Med, 335, pp. 1941-1949. , 8960473
  • Gong, J.H., Zhang, M., Modlin, R.L., Linsley, P.S., Iyer, D., Lin, Y., Barnes, P.F., Interleukin-10 downregulates mycobacterium tuberculosis-induced Th1 responses and CTLA-4 expression (1996) Infect Immun, 64, pp. 913-918. , 8641800
  • Scriba, T.J., Kalsdorf, B., Abrahams, D.A., Isaacs, F., Hofmeister, J., Black, G., Hassan, H.Y., Gelderbloem, S.J., Distinct, specific IL-17- and IL-22-producing CD4+ T cell subsets contribute to the human anti-mycobacterial immune response (2008) J Immunol, 180, pp. 1962-1970. , 18209095
  • Lockhart, E., Green, A.M., Flynn, J.L., IL-17 production is dominated by gammadelta T cells rather than CD4 T cells during mycobacterium tuberculosis infection (2006) J Immunol, 177, pp. 4662-4669. , 16982905
  • Etna, M.P., Giacomini, E., Severa, M., Coccia, E.M., Pro- and anti-inflammatory cytokines in tuberculosis: A two-edged sword in TB pathogenesis (2014) Semin Immunol, 26, pp. 543-551. , 25453229
  • Khader, S.A., Bell, G.K., Pearl, J.E., Fountain, J.J., Rangel-Moreno, J., Cilley, G.E., Shen, F., Swain, S.L., IL-23 and IL-17 in the establishment of protective pulmonary CD4+ T cell responses after vaccination and during mycobacterium tuberculosis challenge (2007) Nat Immunol, 8, pp. 369-377. , 17351619
  • Torrado, E., Robinson, R.T., Cooper, A.M., Cellular response to mycobacteria: Balancing protection and pathology (2011) Trends Immunol, 32, pp. 66-72. , 21216195
  • Khader, S.A., Cooper, A.M., IL-23 and IL-17 in tuberculosis (2008) Cytokine, 41, pp. 79-83. , 18218322
  • Okamoto Yoshida, Y., Umemura, M., Yahagi, A., O'Brien, R.L., Ikuta, K., Kishihara, K., Hara, H., Matsuzaki, G., Essential role of IL-17A in the formation of a mycobacterial infection-induced granuloma in the lung (2010) J Immunol, 184, pp. 4414-4422. , 20212094
  • Gopal, R., Rangel-Moreno, J., Slight, S., Lin, Y., Nawar, H.F., Fallert Junecko, B.A., Reinhart, T.A., Connell, T.D., Interleukin-17-dependent CXCL13 mediates mucosal vaccine-induced immunity against tuberculosis (2013) Mucosal Immunol, 6, pp. 972-984. , 23299616
  • Lazar-Molnar, E., Chen, B., Sweeney, K.A., Wang, E.J., Liu, W., Lin, J., Porcelli, S.A., Jacobs, W.R., Jr., Programmed death-1 (PD-1)-deficient mice are extraordinarily sensitive to tuberculosis (2010) Proc Natl Acad Sci U S A, 107, pp. 13402-13407. , 20624978
  • Jurado, J.O., Pasquinelli, V., Alvarez, I.B., Pena, D., Rovetta, A.I., Tateosian, N.L., Romeo, H.E., Chuluyán, H.E., IL-17 and IFN-gamma expression in lymphocytes from patients with active tuberculosis correlates with the severity of the disease (2012) J Leukoc Biol, 91, pp. 991-1002. , 22416258
  • Cooper, A.M., Editorial: Be careful what you ask for: Is the presence of IL-17 indicative of immunity? (2010) J Leukoc Biol, 88, pp. 221-223. , 20679070
  • Gutierrez, M.G., Master, S.S., Singh, S.B., Taylor, G.A., Colombo, M.I., Deretic, V., Autophagy is a defense mechanism inhibiting BCG and mycobacterium tuberculosis survival in infected macrophages (2004) Cell, 119, pp. 753-766. , 15607973
  • Ponpuak, M., Davis, A.S., Roberts, E.A., Delgado, M.A., Dinkins, C., Zhao, Z., Virgin, V.H.W., Vergne, I., Delivery of cytosolic components by autophagic adaptor protein p62 endows autophagosomes with unique antimicrobial properties (2010) Immunity, 32, pp. 329-341. , 20206555
  • Sambandamurthy, V.K., Jacobs, W.R., Jr., Live attenuated mutants of mycobacterium tuberculosis as candidate vaccines against tuberculosis (2005) Microbes Infect, 7, pp. 955-961. , 15914065
  • Kim, J.J., Lee, H.M., Shin, D.M., Kim, W., Yuk, J.M., Jin, H.S., Lee, S.H., Lee, Z.W., Host cell autophagy activated by antibiotics is required for their effective antimycobacterial drug action (2012) Cell Host Microbe, 11, pp. 457-468. , 22607799
  • Djavaheri-Mergny, M., Amelotti, M., Mathieu, J., Besancon, F., Bauvy, C., Souquere, S., Pierron, G., Codogno, P., NF-kappaB activation represses tumor necrosis factor-alpha-induced autophagy (2006) J Biol Chem, 281, pp. 30373-30382. , 16857678
  • Goletti, D., Petruccioli, E., Romagnoli, A., Piacentini, M., Fimia, G.M., Autophagy in Mycobacterium tuberculosis infection: A passepartout to flush the intruder out? (2013) Cytokine Growth Factor Rev, 24, pp. 335-343. , 23395260
  • Pyo, J.O., Jang, M.H., Kwon, Y.K., Lee, H.J., Jun, J.I., Woo, H.N., Cho, D.H., Kim, J.H., Essential roles of Atg5 and FADD in autophagic cell death: Dissection of autophagic cell death into vacuole formation and cell death (2005) J Biol Chem, 280, pp. 20722-20729. , 15778222
  • Harris, J., De Haro, S.A., Master, S.S., Keane, J., Roberts, E.A., Delgado, M., Deretic, V., T helper 2 cytokines inhibit autophagic control of intracellular mycobacterium tuberculosis (2007) Immunity, 27, pp. 505-517. , 17892853
  • Park, H.J., Lee, S.J., Kim, S.H., Han, J., Bae, J., Kim, S.J., Park, C.G., Chun, T., IL-10 inhibits the starvation induced autophagy in macrophages via class I phosphatidylinositol 3-kinase (PI3K) pathway (2011) Mol Immunol, 48, pp. 720-727. , 21095008
  • Rovetta, A.I., Pena, D., Hernandez Del Pino, R.E., Recalde, G.M., Pellegrini, J., Bigi, F., Musella, R.M., Colombo, M.I., IFNG-mediated immune responses enhance autophagy against mycobacterium tuberculosis antigens in patients with active tuberculosis (2014) Autophagy, 10, pp. 2109-2121. , 25426782
  • Man, N., Chen, Y., Zheng, F., Zhou, W., Wen, L.P., Induction of genuine autophagy by cationic lipids in mammalian cells (2010) Autophagy, 6, pp. 289-254. , 20383065
  • Pasquinelli, V., Quiroga, M.F., Martinez, G.J., Zorrilla, L.C., Musella, R.M., Bracco, M.M., Belmonte, L., Sieling, P.A., Expression of signaling lymphocytic activation molecule-associated protein interrupts IFN-gamma production in human tuberculosis (2004) J Immunol, 172, pp. 1177-1185. , 14707094
  • Matsuzawa, T., Kim, B.H., Shenoy, A.R., Kamitani, S., Miyake, M., Macmicking, J.D., IFN-gamma elicits macrophage autophagy via the p38 MAPK signaling pathway (2012) J Immunol, 189, pp. 813-818. , 22675202
  • Smith, S.G., Lalor, M.K., Gorak-Stolinska, P., Blitz, R., Beveridge, N.E., Worth, A., McShane, H., Dockrell, H.M., Mycobacterium tuberculosis PPD-induced immune biomarkers measurable in vitro following BCG vaccination of UK adolescents by multiplex bead array and intracellular cytokine staining (2010) BMC Immunol, 11, p. 35. , 20609237
  • Torrado, E., Cooper, A.M., IL-17 and Th17 cells in tuberculosis (2010) Cytokine Growth Factor Rev, 21, pp. 455-462. , 21075039
  • Yuan, J., Yu, M., Li, H.H., Long, Q., Liang, W., Wen, S., Wang, M., Liao, Y.H., Autophagy contributes to IL-17-induced plasma cell differentiation in experimental autoimmune myocarditis (2014) Int Immunopharmacol, 18, pp. 98-105. , 24269624
  • Orosz, L., Papanicolaou, E.G., Seprenyi, G., Megyeri, K., IL-17A and IL-17F induce autophagy in RAW 264.7 macrophages (2016) Biomed Pharmacother, 77, pp. 129-134. , 26796276
  • Liu, H., Mi, S., Li, Z., Hua, F., Hu, Z.W., Interleukin 17A inhibits autophagy through activation of PIK3CA to interrupt the GSK3B-mediated degradation of BCL2 in lung epithelial cells (2013) Autophagy, 9, pp. 730-742. , 23514933
  • Zhou, Y., Wu, P.W., Yuan, X.W., Li, J., Shi, X.L., Interleukin-17A inhibits cell autophagy under starvation and promotes cell migration via TAB2/TAB3-p38 mitogen-activated protein kinase pathways in hepatocellular carcinoma (2016) Eur Rev Med Pharmacol Sci, 20, pp. 250-263. , 26875893
  • Matsuzawa, T., Fujiwara, E., Washi, Y., Autophagy activation by interferon-gamma via the p38 mitogen-activated protein kinase signalling pathway is involved in macrophage bactericidal activity (2014) Immunology, 141, pp. 61-69. , 24032631
  • Freches, D., Korf, H., Denis, O., Havaux, X., Huygen, K., Romano, M., Mice genetically inactivated in interleukin-17A receptor are defective in long-term control of mycobacterium tuberculosis infection (2013) Immunology, 140, pp. 220-231. , 23721367
  • Shen, F., Hu, Z., Goswami, J., Gaffen, S.L., Identification of common transcriptional regulatory elements in interleukin-17 target genes (2006) J Biol Chem, 281, pp. 24138-24148. , 16798734
  • Sebkova, L., Pellicano, A., Monteleone, G., Grazioli, B., Guarnieri, G., Imeneo, M., Pallone, F., Luzza, F., Extracellular signal-regulated protein kinase mediates interleukin 17 (IL-17)-induced IL-8 secretion in helicobacter pylori-infected human gastric epithelial cells (2004) Infect Immun, 72, pp. 5019-5026. , 15321994
  • Fang, J.W., Li, J.C., Au, K.Y., Yim, H.C., Lau, A.S., Interleukin-17A differentially modulates BCG induction of cytokine production in human blood macrophages (2011) J Leukoc Biol, 90, pp. 333-341. , 21521755
  • Anand, P.K., Tait, S.W., Lamkanfi, M., Amer, A.O., Nunez, G., Pages, G., Pouysségur, J., Kanneganti, T.D., TLR2 and RIP2 pathways mediate autophagy of listeria monocytogenes via extracellular signal-regulated kinase (ERK) activation (2011) J Biol Chem, 286, pp. 42981-42991. , 22033934
  • Xu, Y., Eissa, N.T., Autophagy in innate and adaptive immunity (2010) Proc Am Thorac Soc, 7, pp. 22-28. , 20160145
  • Buffen, K., Oosting, M., Quintin, J., Ng, A., Kleinnijenhuis, J., Kumar, V., van de Vosse, E., Oosterwijk, E., Autophagy controls BCG-induced trained immunity and the response to intravesical BCG therapy for bladder cancer (2014) PLoS Pathog, 10, p. e1004485. , 25356988
  • Ni Cheallaigh, C., Keane, J., Lavelle, E.C., Hope, J.C., Harris, J., Autophagy in the immune response to tuberculosis: Clinical perspectives (2011) Clin Exp Immunol, 164, pp. 291-300. , 21438870
  • Kim, J.J., Lee, H.M., Shin, D.M., Kim, W., Yuk, J.M., Jin, H.S., Lee, S.H., Lee, Z.W., Host cell autophagy activated by antibiotics is required for their effective antimycobacterial drug action (2013) Cell Host Microbe, 11, pp. 457-468. , 22607799
  • Jo, E.K., Autophagy as an innate defense against mycobacteria (2013) Pathog Dis, 67, pp. 108-118. , 23620156
  • Duan, L., Yi, M., Chen, J., Li, S., Chen, W., Mycobacterium tuberculosis EIS gene inhibits macrophage autophagy through up-regulation of IL-10 by increasing the acetylation of histone H3 (2016) Biochem Biophys Res Commun, 473, pp. 1229-1234. , 27079235
  • Mayer-Barber, K.D., Andrade, B.B., Barber, D.L., Hieny, S., Feng, C.G., Caspar, P., Oland, S., Sher, A., Innate and adaptive interferons suppress IL-1alpha and IL-1beta production by distinct pulmonary myeloid subsets during mycobacterium tuberculosis infection (2011) Immunity, 35, pp. 1023-1034. , 22195750
  • Saitoh, T., Fujita, N., Jang, M.H., Uematsu, S., Yang, B.G., Satoh, T., Omori, H., Komatsu, M., Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production (2008) Nature, 456, pp. 264-268. , 18849965
  • Sakowski, E.T., Koster, S., Portal Celhay, C., Park, H.S., Shrestha, E., Hetzenecker, S.E., Ubiquilin 1 Promotes IFN-gamma-Induced xenophagy of mycobacterium tuberculosis (2015) PLoS Pathog, 11, p. e1005076. , 26225865
  • Huang, D., Bao, L., Mycobacterium tuberculosis EspB protein suppresses interferon-gamma-induced autophagy in murine macrophages (2014) J Microbiol Immunol Infect, 49 (6), pp. 859-865
  • Pasquinelli, V., Rovetta, A.I., Alvarez, I.B., Jurado, J.O., Musella, R.M., Palmero, D.J., Malbrán, A., García, V.E., Phosphorylation of mitogen-activated protein kinases contributes to interferon gamma production in response to mycobacterium tuberculosis (2013) J Infect Dis, 207, pp. 340-350. , 23125442
  • Rolandelli, A., Hernandez Del Pino, R.E., Pellegrini, J.M., Tateosian, N.L., Amiano, N.O., de la Barrera, S., Casco, N., García, V.E., The IL-17A rs2275913 single nucleotide polymorphism is associated with protection to tuberculosis but related to higher disease severity in Argentina (2017) Sci Rep, 7, p. 40666. , 28098168
  • Ouyang, W., Kolls, J.K., Zheng, Y., The biological functions of T helper 17 cell effector cytokines in inflammation (2008) Immunity, 28, pp. 454-467. , 18400188
  • Iwakura, Y., Ishigame, H., Saijo, S., Nakae, S., Functional specialization of interleukin-17 family members (2011) Immunity, 34, pp. 149-162. , 21349428
  • Vergne, I., Fratti, R.A., Hill, P.J., Chua, J., Belisle, J., Deretic, V., Mycobacterium tuberculosis phagosome maturation arrest: Mycobacterial phosphatidylinositol analog phosphatidylinositol mannoside stimulates early endosomal fusion (2004) Mol Biol Cell, 15, pp. 751-760. , 14617817
  • Hart, P.D., Young, M.R., Gordon, A.H., Sullivan, K.H., Inhibition of phagosome-lysosome fusion in macrophages by certain mycobacteria can be explained by inhibition of lysosomal movements observed after phagocytosis (1987) J Exp M, 166, pp. 933-946. , 3309128
  • Yuk, J.M., Shin, D.M., Lee, H.M., Yang, C.S., Jin, H.S., Kim, K.K., Lee, Z.W., Jo, E.K., Vitamin D3 induces autophagy in human monocytes/macrophages via cathelicidin (2009) Cell Host Microbe, 6, pp. 231-243. , 19748465
  • Fabri, M., Stenger, S., Shin, D.M., Yuk, J.M., Liu, P.T., Realegeno, S., Lee, H.M., Sieling, P.A., Vitamin D is required for IFN-gamma-mediated antimicrobial activity of human macrophages (2011) Sci Transl Med, 3, p. 104ra2. , 21998409
  • Kimmey, J.M., Huynh, J.P., Weiss, L.A., Park, S., Kambal, A., Debnath, J., Virgin, H.W., Stallings, C.L., Unique role for ATG5 in neutrophil-mediated immunopathology during M. tuberculosis infection (2015) Nature, 528, pp. 565-569. , 26649827
  • Deretic, V., Autophagy in leukocytes and other cells: Mechanisms, subsystem organization, selectivity, and links to innate immunity (2016) J Leukoc Biol, 100, pp. 969-978. , 27493243
  • Pym, A.S., Brodin, P., Brosch, R., Huerre, M., Cole, S.T., Loss of RD1 contributed to the attenuation of the live tuberculosis vaccines mycobacterium bovis BCG and Mycobacterium microti (2002) Mol Microbiol, 46, pp. 709-717. , 12410828
  • Romagnoli, A., Etna, M.P., Giacomini, E., Pardini, M., Remoli, M.E., Corazzari, M., Falasca, L., Simeone, R., ESX-1 dependent impairment of autophagic flux by mycobacterium tuberculosis in human dendritic cells (2012) Autophagy, 8, pp. 1357-1370. , 22885411
  • Petruccioli, E., Romagnoli, A., Corazzari, M., Coccia, E.M., Butera, O., Delogu, G., Piacentini, M., Goletti, D., Specific T cells restore the autophagic flux inhibited by Mycobacterium tuberculosis in human primary macrophages (2012) J Infect Dis, 205, pp. 1425-1435. , 22457295
  • Yang, D., Chen, J., Zhang, L., Cha, Z., Han, S., Shi, W., Ding, R., Shi, C., Mycobacterium leprae upregulates IRGM expression in monocytes and monocyte-derived macrophages (2014) Inflammation, 37, pp. 1028-1034. , 24469081
  • Akoumianaki, T., Kyrmizi, I., Valsecchi, I., Gresnigt, M.S., Samonis, G., Drakos, E., Boumpas, D., Kontoyiannis, D.P., Aspergillus cell wall melanin blocks LC3-Associated phagocytosis to promote pathogenicity (2016) Cell Host Microbe, 19, pp. 79-90. , 26749442
  • Martinez, J., Almendinger, J., Oberst, A., Ness, R., Dillon, C.P., Fitzgerald, P., Hengartner, M.O., Green, D.R., Microtubule-associated protein 1 light chain 3 alpha (LC3)-associated phagocytosis is required for the efficient clearance of dead cells (2011) Proc Natl Acad Sci U S A, 108, pp. 17396-17401. , 21969579
  • Martinez, J., Malireddi, R.K., Lu, Q., Cunha, L.D., Pelletier, S., Gingras, S., Orchard, R., Peng, J., Molecular characterization of LC3-associated phagocytosis reveals distinct roles for rubicon, NOX2 and autophagy proteins (2015) Nat Cell Biol, 17, pp. 893-906. , 26098576
  • Li, X., Prescott, M., Adler, B., Boyce, J.D., Devenish, R.J., Beclin 1 is required for starvation-enhanced, but not rapamycin-enhanced, LC3-associated phagocytosis of burkholderia pseudomallei in RAW 264.7 cells (2013) Infect Immun, 81, pp. 271-277. , 23115045
  • Romao, S., Munz, C., LC3-associated phagocytosis (2014) Autophagy, 10, pp. 526-528. , 24413059
  • Eng, K.E., Panas, M.D., Karlsson Hedestam, G.B., McInerney, G.M., A novel quantitative flow cytometry-based assay for autophagy (2010) Autophagy, 6, pp. 634-641. , 20458170

Citas:

---------- APA ----------
Tateosian, N.L., Pellegrini, J.M., Amiano, N.O., Rolandelli, A., Casco, N., Palmero, D.J., Colombo, M.I.,..., García, V.E. (2017) . IL17A augments autophagy in Mycobacterium tuberculosis-infected monocytes from patients with active tuberculosis in association with the severity of the disease. Autophagy, 13(7), 1191-1204.
http://dx.doi.org/10.1080/15548627.2017.1320636
---------- CHICAGO ----------
Tateosian, N.L., Pellegrini, J.M., Amiano, N.O., Rolandelli, A., Casco, N., Palmero, D.J., et al. "IL17A augments autophagy in Mycobacterium tuberculosis-infected monocytes from patients with active tuberculosis in association with the severity of the disease" . Autophagy 13, no. 7 (2017) : 1191-1204.
http://dx.doi.org/10.1080/15548627.2017.1320636
---------- MLA ----------
Tateosian, N.L., Pellegrini, J.M., Amiano, N.O., Rolandelli, A., Casco, N., Palmero, D.J., et al. "IL17A augments autophagy in Mycobacterium tuberculosis-infected monocytes from patients with active tuberculosis in association with the severity of the disease" . Autophagy, vol. 13, no. 7, 2017, pp. 1191-1204.
http://dx.doi.org/10.1080/15548627.2017.1320636
---------- VANCOUVER ----------
Tateosian, N.L., Pellegrini, J.M., Amiano, N.O., Rolandelli, A., Casco, N., Palmero, D.J., et al. IL17A augments autophagy in Mycobacterium tuberculosis-infected monocytes from patients with active tuberculosis in association with the severity of the disease. Autophagy. 2017;13(7):1191-1204.
http://dx.doi.org/10.1080/15548627.2017.1320636