Activation of hypoxia inducible factor 1 is a general phenomenon in infections with human pathogens

PLoS ONE

Volumn 5, Issue 7, 2010, Pages 1-12

  Werth, Nadine ^a   Beerlage, Christiane ^b   Rosenberger, Christian ^c   Yazdi, Amir S ^a,d   Edelmann, Markus ^a   Amr, Amro ^a   Bernhardt, Wanja ^e   von Eiff, Christof ^f   Becker, Karsten ^f   Schäfer, Andrea ^a   Peschel, Andreas ^a   Kempf, Volkhard A J ^b  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^b UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d UNIVERSITY OF LAUSANNE   (Switzerland)

^e UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^f UNIVERSITY HOSPITAL MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL PERITONITIS; CELL CULTURE; CONTROLLED STUDY; FEMALE; GENE ACTIVATION; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; INFECTION; MOUSE; NONHUMAN; OXYGEN CONSUMPTION; PROTEIN FUNCTION; REPORTER GENE; SKIN BIOPSY; SKIN INFECTION; STAPHYLOCOCCUS AUREUS; SURVIVAL RATE; ANIMAL; CELL HYPOXIA; CELL LINE; GENETICS; HELA CELL; IN VITRO STUDY; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PERITONITIS; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION INITIATION;

ANIMALS; CELL HYPOXIA; CELL LINE; FEMALE; HELA CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; IMMUNOHISTOCHEMISTRY; MICE; OXYGEN CONSUMPTION; PERITONITIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SKIN DISEASES, INFECTIOUS; STAPHYLOCOCCUS AUREUS; TRANSCRIPTIONAL ACTIVATION;

EID: 77955384915     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011576     Document Type: Article

References (48)

1. Shimoda LA, Manalo DJ, Sham JS, Semenza GL, Sylvester JT (2001) Partial HIF-1alpha deficiency impairs pulmonary arterial myocyte electrophysiological responses to hypoxia. Am J Physiol Lung Cell Mol Physiol 281: 202-208.
2. Pugh CW, Ratcliffe PJ (2003) Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med 9: 677-684.
3. Ivan M, Kondo K, Yang H, Kim W, Valiando J, et al. (2001) HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292: 464-468.
4. Mazure NM, Brahimi-Horn MC, Berta MA, Benizri E, Bilton RL, et al. (2004) HIF-1: master and commander of the hypoxic world. A pharmacological approach to its regulation by siRNAs. Biochem Pharmacol 68: 971-980.
5. Cramer T, Yamanishi Y, Clausen BE, Forster I, Pawlinski R, et al. (2003) HIF-1alpha is essential for myeloid cell-mediated inflammation. Cell 112: 645-657.
6. Peyssonnaux C, Datta V, Cramer T, Doedens A, Theodorakis EA, et al. (2005) HIF-1alpha expression regulates the bactericidal capacity of phagocytes. J Clin Invest 115: 1806-1815.
7. Kempf VA, Lebiedziejewski M, Alitalo K, Wälzlein JH, Ehehalt U, et al. (2005) Activation of hypoxia-inducible factor-1 in bacillary angiomatosis: evidence for a role of hypoxia-inducible factor-1 in bacterial infections. Circulation 111: 1054-1062.
8. Kaiser PO, Riess T, Wagner CL, Linke D, Lupas AN, et al. (2008) The head of Bartonella adhesin A is crucial for host cell interaction of Bartonella henselae. Cell Microbiol 10: 2223-2234.
9. Kempf VA, Volkmann B, Schaller M, Sander CA, Alitalo K, et al. (2001) Evidence of a leading role for VEGF in Bartonella henselae-induced endothelial cell proliferations. Cell Microbiol 3: 623-632.
10. Riess T, Andersson SG, Lupas A, Schaller M, Schäfer A, et al. (2004) Bartonella adhesin A mediates a proangiogenic host cell response. J Exp Med 200: 1267-1278.
11. Hartmann H, Eltzschig HK, Wurz H, Hantke K, Rakin A, et al. (2008) Hypoxia-independent activation of HIF-1 by enterobacteriaceae and their siderophores. Gastroenterology 134: 756-767.
12. Blouin CC, Page EL, Soucy GM, Richard DE (2004) Hypoxic gene activation by lipopolysaccharide in macrophages: implication of hypoxia-inducible factor 1alpha. Blood 103: 1124-1130.
13. Frede S, Stockmann C, Freitag P, Fandrey J (2006) Bacterial lipopolysaccharides induce HIF-1 activation in human monocytes via p44/42 MAPK and NFkappaB. Biochem J 396: 517-527.
14. Peyssonnaux C, Cejudo-Martin P, Doedens A, Zinkernagel AS, Johnson RS, et al. (2007) Essential role of hypoxia inducible factor-1alpha in development of lipopolysaccharide-induced sepsis. J Immunol 178: 7516-7519.
15. Yano K, Liaw PC, Mullington JM, Shih SC, Okada H, et al. (2006) Vascular endothelial growth factor is an important determinant of sepsis morbidity and mortality. J Exp Med 203: 1447-1458.
16. von Eiff C, Heilmann C, Proctor RA, Woltz C, Peters G, et al. (1997) A sitedirected Staphylococcus aureus hemB mutant is a small-colony variant which persists intracellularly. J Bacteriol 179: 4706-4712.
17. von Eiff C (2008) Staphylococcus aureus small colony variants: a challenge to microbiologists and clinicians. Int J Antimicrob Agents 31: 507-510.
18. Fedtke I, Mader D, Kohler T, Moll H, Nicholson G, et al. (2007) A Staphylococcus aureus ypfP mutant with strongly reduced lipoteichoic acid (LTA) content: LTA governs bacterial surface properties and autolysin activity. Mol Microbiol 65: 1078-1091.
19. Weidenmaier C, Kokai-Kun JF, Kristian SA, Chanturiya T, Kalbacher H, et al. (2004) Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat Med 10: 243-245.
20. Hussain M, Haggar A, Heilmann C, Peters G, Flock JI, et al. (2002) Insertional inactivation of Eap in Staphylococcus aureus strain Newman confers reduced staphylococcal binding to fibroblasts. Infect Immun 70: 2933-2940.
21. Lannergard J, von Eiff C, Sander G, Cordes T, Seggewiss J, et al. (2008) Identification of the genetic basis for clinical menadione-auxotrophic smallcolony variant isolates of Staphylococcus aureus. Antimicrob Agents Chemother 52: 4017-4022.
22. Sifri CD, Baresch-Bernal A, Calderwood SB, von Eiff C (2006) Virulence of Staphylococcus aureus small colony variants in the Caenorhabditis elegans infection model. Infect Immun 74: 1091-1096.
23. Essin K, Salanova B, Kettritz R, Sausbier M, Luft FC, et al. (2007) Largeconductance calcium-activated potassium channel activity is absent in human and mouse neutrophils and is not required for innate immunity. Am J Physiol Cell Physiol 293: 45-54.
24. Chavakis T, Hussain M, Kanse SM, Peters G, Bretzel RG, et al. (2002) Staphylococcus aureus extracellular adherence protein serves as anti-inflammatory factor by inhibiting the recruitment of host leukocytes. Nat Med 8: 687-693.
25. Lang SA, Moser C, Gaumann A, Klein D, Glockzin G, et al. (2007) Targeting heat shock protein 90 in pancreatic cancer impairs insulin-like growth factor-I receptor signaling, disrupts an interleukin-6/signal-transducer and activator of transcription 3/hypoxia-inducible factor-1alpha autocrine loop, and reduces orthotopic tumor growth. Clin Cancer Res 13: 6459-6468.
26. Huang LE, Gu J, Schau M, Bunn HF (1998) Regulation of hypoxia-inducible factor 1alpha is mediated by an O2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc Natl Acad Sci U. S. A 95: 7987-7992.
27. Jaakkola P, Mole DR, Tian YM, Wilson MI, Gielbert J, et al. (2001) Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292: 468-472.
28. Berra E, Benizri E, Ginouves A, Volmat V, Roux D, et al. (2003) HIF prolylhydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1alpha in normoxia. EMBO J 22: 4082-4090.
29. Rupp J, Gieffers J, Klinger M, van Zandbergen G, Wrase R, et al. (2007) Chlamydia pneumoniae directly interferes with HIF-1alpha stabilization in human host cells. Cell Microbiol 9: 2181-2191.
30. Yeo M, Kim DK, Han SU, Lee JE, Kim YB, et al. (2006) Novel action of gastric proton pump inhibitor on suppression of Helicobacter pylori induced angiogenesis. Gut 55: 26-33.
31. Haeberle HA, Dürrstein C, Rosenberger P, Hosakote YM, Kuhlicke J, et al. (2008) Oxygen-independent stabilization of hypoxia inducible factor (HIF)-1 during RSV infection. PLoS ONE 3: e3352.
32. Proctor RA, von Eiff C, Kahl BC, Becker K, McNamara P, et al. (2006) Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat Rev Microbiol 4: 295-305.
33. Kempf VA, Hitziger N, Riess T, Autenrieth IB (2002) Do plant and human pathogens have a common pathogenicity strategy? Trends Microbiol 10: 269-275.
34. Dehio C (2005) Bartonella-host-cell interactions and vascular tumour formation. Nat Rev Microbiol 3: 621-631.
35. Jantsch J, Chakravortty D, Turza N, Prechtel AT, Buchholz B, et al. (2008) Hypoxia and hypoxia-inducible factor-1 alpha modulate lipopolysaccharideinduced dendritic cell activation and function. J Immunol 180: 4697-4705.
36. Meyer-Hoffert U, Hornef MW, Henriques-Normark B, Axelsson LG, Midtvedt T, et al. (2008) Secreted enteric antimicrobial activity localises to the mucus surface layer. Gut 57: 764-771.
37. Karhausen J, Furuta GT, Tomaszewski JE, Johnson RS, Colgan SP, et al. (2004) Epithelial hypoxia-inducible factor-1 is protective in murine experimental colitis. J Clin Invest 114: 1098-1106.
38. Enkhbaatar P (2008) Methicillin-resistant Staphylococcus aureus-induced sepsis: role of nitric oxide. In: Yearbook of intensive care and emergency medicine. Traber L, Traber D, eds. Springer Verlag. Berlin, Heidelberg, New York. pp 404-412.
39. van der Flier M, van Leeuwen HJ, van Kessel KP, Kimpen JL, Hoepelman AI, et al. (2005) Plasma vascular endothelial growth factor in severe sepsis. Shock 23: 35-38.
40. van der Flier M, Stockhammer G, Vonk GJ, Nikkels PG, van Diemen-Steenvoorde RA, et al. (2001) Vascular endothelial growth factor in bacterial meningitis: detection in cerebrospinal fluid and localization in postmortem brain. J Infect Dis 183: 149-153.
41. Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, et al. (1983) Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 219: 983-985.
42. Pickkers P, Sprong T, Eijk L, Hoeven H, Smits P, et al. (2005) Vascular endothelial growth factor is increased during the first 48 hours of human septic shock and correlates with vascular permeability. Shock 24: 508-512.
43. Wiesener MS, Turley H, Allen WE, Willam C, Eckardt KU, et al. (1998) Induction of endothelial PAS domain protein-1 by hypoxia: characterization and comparison with hypoxia-inducible factor-1alpha. Blood 92: 2260-2268.
44. Bernhardt WM, Schmitt R, Rosenberger C, Münchenhagen PM, Grone HJ, et al. (2006) Expression of hypoxia-inducible transcription factors in developing human and rat kidneys. Kidney Int 69: 114-122.
45. Sheta EA, Trout H, Gildea JJ, Harding MA, Theodorescu D (2001) Cell density mediated pericellular hypoxia leads to induction of HIF-1alpha via nitric oxide and Ras/MAP kinase mediated signaling pathways. Oncogene 20: 7624-7634.
46. Doege K, Heine S, Jensen I, Jelkmann W, Metzen E (2005) Inhibition of mitochondrial respiration elevates oxygen concentration but leaves regulation of hypoxia-inducible factor (HIF) intact. Blood 106: 2311-2317.
47. Raleigh JA, Koch CJ (1990) Importance of thiols in the reductive binding of 2- nitroimidazoles to macromolecules. Biochem Pharmacol 40: 2457-2464.
48. Kerl H, Garbe C, Cerroni L, Wolff H (2003) Histopathologie der Haut. Springer Verlag, Berlin, Heidelberg, New York. pp 3-7.