Phenylbutyrate induces LL-37-dependent autophagy and intracellular killing of mycobacterium tuberculosis in human macrophages

Autophagy

Volumn 11, Issue 9, 2015, Pages 1688-1699

  Sultana Rekha, Rokeya ^a,b   Rao Muvva, Ssv Jagadeeswara ^a   Wan, Min ^a   Raqib, Rubhana ^b   Bergman, Peter ^a   Brighenti, Susanna ^a   Gudmundsson, Gudmundur H ^c   Agerberth, Birgitta ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b INTERNATIONAL CENTRE FOR DIARRHOEAL DISEASE RESEARCH   (Bangladesh)

^c UNIVERSITY OF ICELAND   (Iceland)

Author keywords

Antimicrobial peptides; Cathelicidin; Innate immunity; P2RX7; Tuberculosis; Vitamin D

Indexed keywords

4 PHENYLBUTYRIC ACID; AUTOPHAGY PROTEIN 5; BECLIN 1; CALCITRIOL; CALCIUM ION; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; CYCLIC AMP; MESSENGER RNA; 4-PHENYLBUTYRIC ACID; ADENYLATE KINASE; ANTIMICROBIAL CATIONIC PEPTIDE; APOPTOSIS REGULATORY PROTEIN; ARYLBUTYRIC ACID DERIVATIVE; ATG5 PROTEIN, HUMAN; AUTOPHAGY RELATED PROTEIN 5; BECN1 PROTEIN, HUMAN; CALCIUM; CAP18 LIPOPOLYSACCHARIDE-BINDING PROTEIN; LIGHT CHAIN 3, HUMAN; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; P2RX7 PROTEIN, HUMAN; PHOSPHATIDYLINOSITOL 3 KINASE; PURINERGIC P2X7 RECEPTOR; VITAMIN D;

ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BACTERIAL GROWTH; BACTERICIDAL ACTIVITY; CALCIUM CELL LEVEL; CELL STIMULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSOL; DOWN REGULATION; GENE EXPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; GROWTH REGULATION; HUMAN; HUMAN CELL; INTRACELLULAR KILLING; MACROPHAGE; MACROPHAGE ACTIVATION; MONOCYTE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TUBERCULOSIS; CELL LINE; CYTOLOGY; DRUG EFFECTS; GENETICS; GROWTH, DEVELOPMENT AND AGING; INTRACELLULAR SPACE; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY;

ADENYLATE KINASE; ANTIMICROBIAL CATIONIC PEPTIDES; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; AUTOPHAGY-RELATED PROTEIN 5; BECLIN-1; CALCIUM; CELL LINE; HUMANS; INTRACELLULAR SPACE; MACROPHAGES; MEMBRANE PROTEINS; MICROBIAL VIABILITY; MICROTUBULE-ASSOCIATED PROTEINS; MYCOBACTERIUM TUBERCULOSIS; PHENYLBUTYRATES; PHOSPHATIDYLINOSITOL 3-KINASES; RECEPTORS, PURINERGIC P2X7; RNA, MESSENGER; VITAMIN D;

EID: 84953887472     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.1080/15548627.2015.1075110     Document Type: Article

References (33)

1. WHO. WHO Global Tuberculosis Report, Drug- Resistant TB, Surveillance & Response, http://www. who.int/tb/challenges/mdr/MDR_TB_2014. 2014
2. Kumar D, Rao KV. Regulation between survival, persistence, and elimination of intracellular mycobacteria: a nested equilibrium of delicate balances. Microbes Infect 2011; 13:121-33 ; PMID:20971210
3. Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 2004; 119:753-66 ; PMID:15607973
4. MacMicking JD. Cell-autonomous effector mechanisms against mycobacterium tuberculosis. Cold Spring Harb Perspect Med 2014; 4:a018507 ; PMID:25081628
5. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008; 132:27-42; PMID:18191218
6. Songane M, Kleinnijenhuis J, Netea MG, van Crevel R. The role of autophagy in host defence against Mycobacterium tuberculosis infection. Tuberculosis 2012; 92:388-96 ; PMID:22683183
7. Sonawane A, Santos JC, Mishra BB, Jena P, Progida C, Sorensen OE, Gallo R, Appelberg R, Griffiths G. Cathelicidin is involved in the intracellular killing of mycobacteria in macrophages. Cell Microbiol 2011; 13:1601-17 ; PMID:21790937
8. Verma RK, Agrawal AK, Singh AK, Mohan M, Gupta A, Gupta P, Gupta UD, Misra A. Inhalable microparticles of nitric oxide donors induce phagosome maturation and kill Mycobacterium tuberculosis. Tuberculosis 2013; 93:412-7 ; PMID:23562366
9. Wilmes M, Cammue BP, Sahl HG, Thevissen K. Antibiotic activities of host defense peptides: more to it than lipid bilayer perturbation. Nat Prod Rep 2011; 28:1350-8 ; PMID:21617811
10. Gudmundsson GH, Agerberth B, Odeberg J, Bergman T, Olsson B, Salcedo R. The human gene FALL39 and processing of the cathelin precursor to the antibacterial peptide LL-37 in granulocytes. Eur J Biochem 1996; 238:325-32 ; PMID:8681941
11. Liu PT, Stenger S, Li H, Wenzel L, Tan BH, Krutzik SR, Ochoa MT, Schauber J, Wu K, Meinken C, et al. Toll-like receptor triggering of a vitamin D-mediatedhuman antimicrobial response. Science 2006; 311:1770-3 ; PMID:16497887
12. Liu PT, Stenger S, Tang DH, Modlin RL. Cutting edge: vitamin D-mediated human antimicrobial activity against Mycobacterium tuberculosis is dependent on the induction of cathelicidin. J Immunol 2007; 179:2060-3; PMID:17675463
13. Islam D, Bandholtz L, Nilsson J, Wigzell H, Christensson B, Agerberth B, Gudmundsson G. Downregulation of bactericidal peptides in enteric infections: a novel immune escape mechanism with bacterial DNA as a potential regulator. Nat Med 2001; 7:180-5; PMID:11175848
14. Bergman P, Johansson L, Asp V, Plant L, Gudmundsson GH, Jonsson AB, Agerberth B. Neisseria gonorrhoeae downregulates expression of the human antimicrobial peptide LL-37. Cellular Microbiol 2005; 7:1009-17; PMID:15953032
15. Raqib R, Sarker P, Bergman P, Ara G, Lindh M, Sack DA, Nasirul Islam KM, Gudmundsson GH, Andersson J, Agerberth B. Improved outcome in shigellosis associated with butyrate induction of an endogenous peptide antibiotic. Proc Natl Acad Sci USA 2006; 103:9178-83 ; PMID:16740661
16. Steinmann J, Halldorsson S, Agerberth B, Gudmundsson GH. Phenylbutyrate induces antimicrobial peptide expression. Antimicrob Agents Chemother 2009; 53:5127-33 ; PMID:19770273
17. Mily A, Rekha RS, Kamal SM, Akhtar E, Sarker P, Rahim Z, Gudmundsson GH, Agerberth B, Raqib R. Oral intake of phenylbutyrate with or without vitamin D3 upregulates the cathelicidin LL-37 in human macrophages: a dose finding study for treatment of tuberculosis. BMC Pulm Med 2013; 13:23 ; PMID:23590701; http://dx.doi.org/10.1186/1471-2466-13-23
18. Yuk JM, Shin DM, Lee HM, Yang CS, Jin HS, Kim KK, Lee ZW, Lee SH, Kim JM, Jo EK. Vitamin D3 induces autophagy in human monocytes/macrophages via cathelicidin. Cell Host Microbe 2009; 6:231-43; PMID:19748465; http://dx.doi.org/10.1016/j.chom.2009.08.004
19. Bjorkoy G, Lamark T, Brech A, Outzen H, Perander M, Overvatn A, Stenmark H, Johansen T. p62/ SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtininduced cell death. J Cell Biol 2005; 171:603-14 ; PMID:16286508; http://dx.doi.org/10.1083/ jcb.200507002
20. Pursiheimo JP, Rantanen K, Heikkinen PT, Johansen T, Jaakkola PM. Hypoxia-activated autophagy accelerates degradation of SQSTM1/p62. Oncogene 2009; 28:334-44 ; PMID:18931699; http://dx.doi.org/ 10.1038/onc.2008.392
21. Hoyer-Hansen M, Jaattela M. AMP-activated protein kinase: a universal regulator of autophagy? Autophagy 2007; 3:381-3 ; PMID:17457036; http://dx.doi.org/ 10.4161/auto.4240
22. Heras-Sandoval D, Perez-Rojas JM, Hernandez-Damian J, Pedraza-Chaverri J. The role of PI3K/AKT/ mTOR pathway in the modulation of autophagy and the clearance of protein aggregates in neurodegeneration. Cell Signal 2014; 26:2694-701; PMID:25173700; http://dx.doi.org/10.1016/j. cellsig.2014.08.019
23. Nijnik A, Hancock RE. The roles of cathelicidin LL-37 in immune defences and novel clinical applications. Curr Opin Hematol 2009; 16:41-7; PMID:19068548; http://dx.doi.org/10.1097/MOH.0b013e32831ac517
24. Elssner A, Duncan M, Gavrilin M, Wewers MD. A novel P2_7 receptor activator, the human cathelicidinderived peptide LL37, induces IL-1 b processing and release. J Immunol 2004; 172:4987-94 ; PMID:15067080; http://dx.doi.org/10.4049/jimmunol.172.8.4987
25. Sorensen OE, Follin P, Johnsen AH, Calafat J, Tja bringa GS, Hiemstra PS, Borregaard N. Human cathelicidin,hCAP-18, is processed to the antimicrobial peptide LL-37 by extracellular cleavage with proteinase3. Blood 2001; 97:3951-9; PMID:11389039; http://dx.doi.org/10.1182/blood.V97.12.3951
26. Wan M, van der Does AM, Tang X, Lindbom L, Agerberth B, Haeggstrom JZ. Antimicrobial peptide LL-37 promotes bacterial phagocytosis by human macrophages. J Leukoc Biol 2014; 95:971-81; PMID:24550523; http://dx.doi.org/10.1189/jlb.0513304
27. Kulkarni NN, Yi Z, Huehnken C, Agerberth B, Gudmundsson GH. Phenylbutyrate induces cathelicidin expression via the vitamin D receptor: Linkage to inflammatory and growth factor cytokines pathways. Mol Immunol 2014; 63:530-9; PMID:25458314; http://dx.doi.org/10.1016/j.molimm.2014.10.007
28. Shao Y, Gao Z, Marks P A, Jiang X. Apoptotic and autophagic cell death induced by histone deacetylase inhibitors. Proc Natl Acad Sci USA 2004; 101:18030-5; PMID:15596714; http://dx.doi.org/10.1073/ pnas.0408345102
29. Gade P, Ramachandran G, Maachani UB, Rizzo MA, Okada T, Prywes R, Cross AS, Mori K, Kalvakolanu V. An IFN-gamma-stimulated ATF6-C/EBP-b-signaling pathway critical for the expression of Death Associated Protein Kinase 1 and induction of autophagy. Proc Natl Acad Sci USA 2012; 109:10316-21; PMID:22699507; http://dx.doi.org/10.1073/pnas.1119273109
30. Schauber J, Svanholm C, Termen S, Iffland K, Menzel T, Scheppach W, Melcher R, Agerberth B, Luhrs H, Gudmundsson GH. Expression of the cathelicidin LL- 37 is modulated by short chain fatty acids in colonocytes: relevance of signalling pathways. Gut 2003; 52:735-41; PMID:12692061; http://dx.doi.org/10.1136/gut.52.5.735
31. Dhawan P, Wei R, Sun C, Gombart AF, Koeffler HP, Diamond G, Christakos S. C/EBPalpha and the Vitamin D Receptor Cooperate in the Regulation of Cathelicidin in Lung Epithelial Cells. J Cell Physiol 2014; 230(2):464-72; PMID:25078430
32. Hou H, Zhang Y, Huang Y, Yi Q, Lv L, Zhang T, Chen D, Hao Q, Shi Q. Inhibitors of phosphatidylinositol 3'-kinases promote mitotic cell death in HeLa cells. PloS one 2012; 7:e35665; PMID:22545128; http://dx.doi.org/10.1371/journal.pone.0035665
33. Yoshio H, Tollin M, Gudmundsson GH, Lagercrantz H, Jornvall H, Marchini G, Agerberth B. Antimicrobial polypeptides of human vernix caseosa and amniotic fluid: implications for newborn innate defense. Pediatr Res 2003; 53:211-6; PMID:12538777; http://dx.doi.org/10.1203/00006450-200302000-00003