Loss of mitochondrial protein Fus1 augments host resistance to acinetobacter baumannii infection

Infection and Immunity

Volumn 81, Issue 12, 2013, Pages 4461-4469

  Hood, M Indriati ^a   Uzhachenko, Roman ^b   Boyd, Kelli ^a   Skaar, Eric P ^a   Ivanova, Alla V ^c  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MEHARRY MEDICAL COLLEGE   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 17; INTERLEUKIN 6; MAMMALIAN TARGET OF RAPAMYCIN; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL PROTEIN FUS1; MONOCYTE CHEMOTACTIC PROTEIN 1; PHOSPHATIDYLINOSITOL 3 KINASE; TUMOR NECROSIS FACTOR ALPHA; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ACINETOBACTER BAUMANNII; ACINETOBACTER INFECTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL INFECTION; BACTERIAL PNEUMONIA; BLOOD CELL COUNT; CONTROLLED STUDY; CYTOKINE PRODUCTION; HISTOPATHOLOGY; HOSPITAL INFECTION; HOST RESISTANCE; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOREGULATION; INFLAMMATION; LUNG INFECTION; MACROPHAGE; MALE; MOUSE; NEUTROPHIL; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; WESTERN BLOTTING;

ACINETOBACTER BAUMANNII; ACINETOBACTER INFECTIONS; ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; INTERLEUKIN-10; INTERLEUKIN-17; LUNG; MACROPHAGES; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, KNOCKOUT; NEUTROPHILS; NF-KAPPA B; PHOSPHATIDYLINOSITOL 3-KINASE; PNEUMONIA, BACTERIAL; PROTO-ONCOGENE PROTEINS C-AKT; REACTIVE OXYGEN SPECIES; TOR SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEINS;

EID: 84890173785     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00771-13     Document Type: Article

References (52)

1. Ivanova AV, Ivanov SV, Prudkin L, Nonaka D, Liu Z, Tsao A, Wistuba I, Roth J, Pass HI. 2009. Mechanisms of FUS1/TUSC2 deficiency in mesothelioma and its tumorigenic transcriptional effects. Mol. Cancer 8:91.
2. Prudkin L, Behrens C, Liu DD, Zhou X, Ozburn NC, Bekele BN, Minna JD, Moran C, Roth JA, Ji L, Wistuba II. 2008. Loss and reduction of FUS1 protein expression is a frequent phenomenon in the pathogenesis of lung cancer. Clin. Cancer Res. 14:41-47.
3. Wistuba II, Behrens C, Virmani AK, Mele G, Milchgrub S, Girard L, Fondon JW, III, Garner HR, McKay B, Latif F, Lerman MI, Lam S, Gazdar AF, Minna JD. 2000. High resolution chromosome 3p allelotyping of human lung cancer and preneoplastic/preinvasive bronchial epithelium reveals multiple, discontinuous sites of 3p allele loss and three regions of frequent breakpoints. Cancer Res. 60:1949-1960.
4. Ivanova AV, Ivanov SV, Pascal V, Lumsden JM, Ward JM, Morris N, Tessarolo L, Anderson SK, Lerman MI. 2007. Autoimmunity, spontaneous tumourigenesis, and IL-15 insufficiency in mice with a targeted disruption of the tumour suppressor gene Fus1. J. Pathol. 211:591-601.
5. Uzhachenko R, Issaeva N, Boyd K, Ivanov SV, Carbone DP, Ivanova AV. 2012. Tumour suppressor Fus1 provides a molecular link between inflammatory response and mitochondrial homeostasis. J. Pathol. 227:456-469.
6. West AP, Shadel GS, Ghosh S. 2011. Mitochondria in innate immune responses. Nat. Rev. Immunol. 11:389-402.
7. West AP, Brodsky IE, Rahner C, Woo DK, Erdjument-Bromage H, Tempst P, Walsh MC, Choi Y, Shadel GS, Ghosh S. 2011. TLR signaling augments macrophage bactericidal activity through mitochondrial ROS. Nature 472:476-480.
8. Erdem I, Ozgultekin A, Sengoz Inan A, Dincer E, Turan G, Ceran N, Ozturk Engin D, Senbayrak Akcay S, Akgun N, Goktas P. 2008. Incidence, etiology, and antibiotic resistance patterns of gram-negative microorganisms isolated from patients with ventilator-associated pneumonia in a medical-surgical intensive care unit of a teaching hospital in Istanbul, Turkey (2004-2006). Jpn. J. Infect. Dis. 61:339-342.
9. Garza-González E, Llaca-Díaz JM, Bosques-Padilla FJ, González GM. 2010. Prevalence of multidrug-resistant bacteria at a tertiary-care teaching hospital in Mexico: Special focus on Acinetobacter baumannii. Chemotherapy 56:275-279.
10. Gaynes R, Edwards JR, System NNIS. 2005. Overview of nosocomial infections caused by gram-negative bacilli. Clin. Infect. Dis. 41:848-854.
11. Jean SS, Hsueh PR. 2011. High burden of antimicrobial resistance in Asia. Int. J. Antimicrob. Agents 37:291-295.
12. Jean SS, Hsueh PR, Lee WS, Chang HT, Chou MY, Chen IS, Wang JH, Lin CF, Shyr JM, Ko WC, Wu JJ, Liu YC, Huang WK, Teng LJ, Liu CY. 2009. Nationwide surveillance of antimicrobial resistance among non-fermentative Gram-negative bacteria in intensive care units in Taiwan: SMART programme data 2005. Int. J. Antimicrob. Agents 33:266-271.
13. van Faassen H, KuoLee R, Harris G, Zhao X, Conlan JW, Chen W. 2007. Neutrophils play an important role in host resistance to respiratory infection with Acinetobacter baumannii in mice. Infect. Immun. 75:5597-5608.
14. Breslow JM, Meissler JJ, Jr, Hartzell RR, Spence PB, Truant A, Gaughan J, Eisenstein TK. 2011. Innate immune responses to systemic Acinetobacter baumannii infection in mice: neutrophils, but not interleukin-17, mediate host resistance. Infect. Immun. 79:3317-3327.
15. Qiu H, KuoLee R, Harris G, Chen W. 2009. Role of NADPH phagocyte oxidase in host defense against acute respiratory Acinetobacter baumannii infection in mice. Infect. Immun. 77:1015-1021.
16. + cells regulate neutrophil migration in mice with Acinetobacter baumannii pneumonia. Microbiol. Immunol. 56:107-116.
17. Zhao L, KuoLee R, Harris G, Tram K, Yan H, Chen W. 2011. c-di-GMP protects against intranasal Acinetobacter baumannii infection in mice by chemokine induction and enhanced neutrophil recruitment. Int. Immunopharmacol. 11:1378-1383.
18. Qiu H, KuoLee R, Harris G, Van Rooijen N, Patel GB, Chen W. 2012. Role of macrophages in early host resistance to respiratory Acinetobacter baumannii infection. PLoS One 7:e40019. doi:10.1371/journal.pone.0040019.
19. Hood MI, Mortensen BL, Moore JL, Zhang Y, Kehl-Fie TE, Sugitani N, Chazin WJ, Caprioli RM, Skaar EP. 2012. Identification of an Acinetobacter baumannii zinc acquisition system that facilitates resistance to calprotectin-mediated zinc sequestration. PLoS Pathog. 8:e1003068. doi:10.1371/journal.ppat.1003068.
20. Jacobs AC, Hood I, Boyd KL, Olson PD, Morrison JM, Carson S, Sayood K, Iwen PC, Skaar EP, Dunman PM. 2010. Inactivation of phospholipase D diminishes Acinetobacter baumannii pathogenesis. Infect. Immun. 78:1952-1962.
21. Pizzolla A, Hultqvist M, Nilson B, Grimm MJ, Eneljung T, Jonsson IM, Verdrengh M, Kelkka T, Gjertsson I, Segal BH, Holmdahl R. 2012. Reactive oxygen species produced by the NADPH oxidase 2 complex in monocytes protect mice from bacterial infections. J. Immunol. 188:5003-5011.
22. Emre Y., Nubel T. Uncoupling protein UCP2: When mitochondrial activity meets immunity. FEBS Lett. 584:1437-1442.
23. Rousset S, Emre Y, Join-Lambert O, Hurtaud C, Ricquier D, Cassard-Doulcier AM. 2006. The uncoupling protein 2 modulates the cytokine balance in innate immunity. Cytokine 35:135-142.
24. Qiu H, KuoLee R, Harris G, Chen W. 2009. High susceptibility to respiratory Acinetobacter baumannii infection in A/J. mice is associated with a delay in early pulmonary recruitment of neutrophils. Microbes Infect. Inst. Pasteur 11:946-955.
25. Pantano C, Ather JL, Alcorn JF, Poynter ME, Brown AL, Guala AS, Beuschel SL, Allen GB, Whittaker LA, Bevelander M, Irvin CG, Janssen-Heininger YM. 2008. Nuclear factor-κB activation in airway epithelium induces inflammation and hyperresponsiveness. Am. J. Respir. Crit. Care Med. 177:959-969.
26. Poynter ME, Irvin CG, Janssen-Heininger YM. 2003. A prominent role for airway epithelial NF-κB activation in lipopolysaccharide-induced airway inflammation. J. Immunol. 170:6257-6265.
27. Chen SM, Cheng DS, Williams BJ, Sherrill TP, Han W, Chont M, Saint-Jean L, Christman JW, Sadikot RT, Yull FE, Blackwell TS. 2008. The nuclear factor kappa-B pathway in airway epithelium regulates neutrophil recruitment and host defence following Pseudomonas aeruginosa infection. Clin. Exp. Immunol. 153:420-428.
28. Jiang D, Nelson ML, Gally F, Smith S, Wu Q, Minor M, Case S, Thaikoottathil J, Chu HW. 2012. Airway epithelial NF-κB activation promotes Mycoplasma pneumoniae clearance in mice. PLoS One 7:e52969. doi:10.1371/journal.pone.0052969.
29. March C, Regueiro V, Llobet E, Moranta D, Morey P, Garmendia J, Bengoechea JA. 2010. Dissection of host cell signal transduction during Acinetobacter baumannii-triggered inflammatory response. PLoS One 5:e10033. doi:10.1371/journal.pone.0010033.
30. +T cells. Antiox. Redox Signal., in press.
31. Gloire G, Legrand-Poels S, Piette J. 2006. NF-κB activation by reactive oxygen species: Fifteen years later. Biochem. Pharmacol. 72:1493-1505.
32. Khajah M, Millen B, Cara DC, Waterhouse C, McCafferty DM. 2011. Granulocyte-macrophage colony-stimulating factor (GM-CSF): A chemo-attractive agent for murine leukocytes in vivo. J. Leukoc. Biol. 89:945-953.
33. Liu L, Das S, Losert W, Parent CA. 2010. mTORC2 regulates neutrophil chemotaxis in a cAMP- and RhoA-dependent fashion. Developmental Cell 19:845-857.
34. Pani G. 2010. P66SHC and ageing: ROS and TOR? Aging 2:514-518.
35. Alcamo E, Mizgerd JP, Horwitz BH, Bronson R, Beg AA, Scott M, Doerschuk CM, Hynes RO, Baltimore D. 2001. Targeted mutation of TNF receptor I rescues the RelA-deficient mouse and reveals a critical role for NF-κB in leukocyte recruitment. J. Immunol. 167:1592-1600.
36. Sadikot RT, Han W, Everhart MB, Zoia O, Peebles RS, Jansen ED, Yull FE, Christman JW, Blackwell TS. 2003. Selective I κB kinase expression in airway epithelium generates neutrophilic lung inflammation. J. Immunol. 170:1091-1098.
37. Skerrett SJ, Liggitt HD, Hajjar AM, Ernst RK, Miller SI, Wilson CB. 2004. Respiratory epithelial cells regulate lung inflammation in response to inhaled endotoxin. Am. J. Physiol. Lung Cell. Mol. Physiol. 287:L143-L152.
38. Chow JY, Ban M, Wu HL, Nguyen F, Huang M, Chung H, Dong H, Carethers JM. 2010. TGF-ß downregulates PTEN via activation of NF-κB in pancreatic cancer cells. Am. J. Physiol. Gastrointest. Liver Physiol. 298: G275-G282.
39. Vasudevan KM, Gurumurthy S, Rangnekar VM. 2004. Suppression of PTEN expression by NF-κB prevents apoptosis. Mol. Cell. Biol. 24:1007-1021.
40. Xia D, Srinivas H, Ahn YH, Sethi G, Sheng X, Yung WK, Xia Q, Chiao PJ, Kim H, Brown PH, Wistuba II, Aggarwal BB, Kurie JM. 2007. Mitogen-activated protein kinase kinase-4 promotes cell survival by decreasing PTEN expression through an NF κB-dependent pathway. J. Biol. Chem. 282:3507-3519.
41. Li Y, Jia Y, Pichavant M, Loison F, Sarraj B, Kasorn A, You J, Robson BE, Umetsu DT, Mizgerd JP, Ye K, Luo HR. 2009. Targeted deletion of tumor suppressorPTENaugments neutrophil function and enhances host defense in neutropenia-associated pneumonia. Blood 113:4930-4941.
42. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A. 2004. Neutrophil extracellular traps kill bacteria. Science 303:1532-1535.
43. Bianchi M, Hakkim A, Brinkmann V, Siler U, Seger RA, Zychlinsky A, Reichenbach J. 2009. Restoration of NET formation by gene therapy in CGD controls aspergillosis. Blood 114:2619-2622.
44. Yost CC, Cody MJ, Harris ES, Thornton NL, McInturffAM, Martinez ML, Chandler NB, Rodesch CK, Albertine KH, Petti CA, Weyrich AS, Zimmerman GA. 2009. Impaired neutrophil extracellular trap (NET) formation: A novel innate immune deficiency of human neonates. Blood 113:6419-6427.
45. McInturffAM, Cody MJ, Elliott EA, Glenn JW, Rowley JW, Rondina MT, Yost CC. 2012. Mammalian target of rapamycin regulates neutrophil extracellular trap formation via induction of hypoxia-inducible factor 1α. Blood 120:3118-3125.
46. Bianchi M, Niemiec MJ, Siler U, Urban CF, Reichenbach J. 2011. Restoration of anti-Aspergillus defense by neutrophil extracellular traps in human chronic granulomatous disease after gene therapy is calprotectindependent. J. Allergy Clin. Immunol. 127:1243-1252.e1247.
47. Urban CF, Ermert D, Schmid M, Abu-Abed U, Goosmann C, Nacken W, Brinkmann V, Jungblut PR, Zychlinsky A. 2009. Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog. 5:e1000639. doi:10.1371/journal.ppat.1000639.
48. Liang SC, Tan XY, Luxenberg DP, Karim R, Dunussi-Joannopoulos K, Collins M, Fouser LA. 2006. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J. Exp. Med. 203:2271-2279.
49. Zhang J, Khvorostov I, Hong JS, Oktay Y, Vergnes L, Nuebel E, Wahjudi PN, Setoguchi K, Wang G, Do A, Jung HJ, McCaffery JM, Kurland IJ, Reue K, Lee WN, Koehler CM, Teitell MA. 2011. UCP2 regulates energy metabolism and differentiation potential of human pluripotent stem cells. EMBO J. 30:4860-4873.
50. Park D, Han CZ, Elliott MR, Kinchen JM, Trampont PC, Das S, Collins S, Lysiak JJ, Hoehn KL, Ravichandran KS. 2011. Continued clearance of apoptotic cells critically depends on the phagocyte Ucp2 protein. Nature 477:220-224.
51. Arsenijevic D, Onuma H, Pecqueur C, Raimbault S, Manning BS, Miroux B, Couplan E, Alves-Guerra MC, Goubern M, Surwit R, Bouillaud F, Richard D, Collins S, Ricquier D. 2000. Disruption of the uncoupling protein-2 gene in mice reveals a role in immunity and reactive oxygen species production. Nat. Genet. 26:435-439.
52. Blanc J, Alves-Guerra MC, Esposito B, Rousset S, Gourdy P, Ricquier D, Tedgui A, Miroux B, Mallat Z. 2003. Protective role of uncoupling protein 2 in atherosclerosis. Circulation 107:388-390.