Attenuation of biopterin synthesis prevents escherichia coli K1 invasion of brain endothelial cells and the development of meningitis in newborn mice

Journal of Infectious Diseases

Volumn 207, Issue 1, 2013, Pages 61-71

  Shanmuganathan, Muthusamy V ^a   Krishnan, Subramanian ^a   Fu, Xiaowei ^a,b   Prasadarao, Nemani V ^a,b  

^a CHILDREN S HOSPITAL LOS ANGELES   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Biopterin; Brain; Endothelial cells; Escherichia coli K1; Inducible nitric oxide; Invasion; Outer membrane protein A

Indexed keywords

2,4 DIAMINOPYRIMIDINE DERIVATIVE; BIOPTERIN; GUANOSINE TRIPHOSPHATE CYCLOHYDROLASE I; NITRIC OXIDE; OUTER MEMBRANE PROTEIN; SMALL INTERFERING RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL MENINGITIS; BACTERIAL STRAIN; CELL MEMBRANE; CONTROLLED STUDY; ESCHERICHIA COLI; ESCHERICHIA COLI K 1; FLOW CYTOMETRY; IMMUNOPRECIPITATION; MICROVASCULAR ENDOTHELIAL CELL; MOUSE; NEWBORN; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; BACTERIAL OUTER MEMBRANE PROTEINS; BIOPTERIN; BRAIN; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; ENZYME INHIBITORS; ESCHERICHIA COLI; FEMALE; GTP CYCLOHYDROLASE; HUMANS; HYPOXANTHINES; MENINGITIS, ESCHERICHIA COLI; MICE; MICE, INBRED C57BL; MICROVESSELS; NITRIC OXIDE; PROTEIN BINDING; RECEPTORS, CELL SURFACE; VIRULENCE;

EID: 84872933446     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1093/infdis/jis656     Document Type: Article

References (36)

1. Scheld WM, Koedel U, Nathan B, Pfister HW. Pathophysiology of bacterial meningitis: mechanism(s) of neuronal injury. J Infect Dis 2002; 186(Suppl 2):S225-33.
2. Unhanand M, Mustafa MM, McCracken GH Jr., Nelson JD. Gramnegative enteric bacillary meningitis: a twenty-one-year experience. J Pediatr 1993; 122:15-21.
3. Prasadarao NV, Wass CA, Weiser JN, Stins MF, Huang SH, Kim KS. Outer membrane protein A of Escherichia coli contributes to invasion of brain microvascular endothelial cells. Infect Immun 1996; 64:146-53.
4. Mittal R, Prasadarao NV. Nitric oxide/cGMP signalling induces Escherichia coli K1 receptor expression and modulates the permeability in human brain endothelial cell monolayers during invasion. Cell Microbiol 2010; 12:67-83.
5. Alderton WK, Cooper CE, Knowles RG. Nitric oxide synthases: structure, function and inhibition. Biochem J 2001; 357:593-615.
6. Thony B, Auerbach G, Blau N. Tetrahydrobiopterin biosynthesis, regeneration and functions. Biochem J 2000; 347 (Pt 1):1-16.
7. Swick L, Kapatos G. A yeast 2-hybrid analysis of human GTP cyclohydrolase I protein interactions. J Neurochem 2006; 97:1447-55.
8. Tanaka K, Kaufman S, Milstien S. Tetrahydrobiopterin, the cofactor for aromatic amino acid hydroxylases, is synthesized by and regulates proliferation of erythroid cells. Proc Natl Acad Sci U S A 1989; 86:5864-7.
9. Tegeder I, Costigan M, Griffin RS, et al. GTP cyclohydrolase and tetrahydrobiopterin regulate pain sensitivity and persistence. Nat Med 2006; 12:1269-77.
10. Linscheid P, Schaffner A, Schoedon G. Modulation of inducible nitric oxide synthase mRNA stability by tetrahydrobiopterin in vascular smooth muscle cells. Biochem Biophys Res Commun 1998; 243:137-41.
11. Murr C, Widner B, Wirleitner B, Fuchs D. Neopterin as a marker for immune system activation. Curr Drug Metab 2002; 3:175-87.
12. Hattori Y, Nakanishi N, Kasai K, Shimoda SI. GTP cyclohydrolase I mRNA induction and tetrahydrobiopterin synthesis in human endothelial cells. Biochim Biophys Acta 1997; 1358:61-6.
13. Hauser B, Bracht H, Matejovic M, Radermacher P, Venkatesh B. Nitric oxide synthase inhibition in sepsis? Lessons learned from largeanimal studies. Anesth Analg 2005; 101:488-98.
14. Azumagawa K, Suzuki S, Tanabe T, Wakamiya E, Kawamura N, Tamai H. Neopterin, biopterin, and nitric oxide concentrations in the cerebrospinal fluid of children with central nervous system infections. Brain Dev 2003; 25:200-2.
15. Franscini N, Blau N, Walter RB, Schaffner A, Schoedon G. Critical role of interleukin-1beta for transcriptional regulation of endothelial 6-pyruvoyltetrahydropterin synthase. Arterioscler Thromb Vasc Biol 2003; 23:e50-3.
16. Prasadarao NV, Srivastava PK, Rudrabhatla RS, Kim KS, Huang SH, Sukumaran SK. Cloning and expression of the Escherichia coli K1 outer membrane protein A receptor, a gp96 homologue. Infect Immun 2003; 71:1680-8.
17. Stins MF, Gilles F, Kim KS. Selective expression of adhesion molecules on human brain microvascular endothelial cells. J Neuroimmunol 1997; 76:81-90.
18. Fukushima T, Nixon JC. Analysis of reduced forms of biopterin in biological tissues and fluids. Anal Biochem 1980; 102:176-88.
19. Krishnan S, Fernandez GS, Sacks DB, Prasadarao NV. IQGAP1 mediates the disruption of adherens junctions to promote Escherichia coli K1 invasion of brain endothelial cells. Cell Microbiol 2012; 14:1415-33.
20. Sakai K, Suzuki H, Oda H, et al. Phosphoinositide 3-kinase in nitric oxide synthesis in macrophage: critical dimerization of inducible nitric-oxide synthase. J Biol Chem 2006; 281:17736-42.
21. Mittal R, Krishnan S, Gonzalez-Gomez I, Prasadarao NV. Deciphering the roles of outer membrane protein A extracellular loops in the pathogenesis of Escherichia coli K1 meningitis. J Biol Chem 2011; 286:2183-93.
22. Kobayashi T, Hasegawa H, Kaneko E, Ichiyama A. Gastrointestinal serotonin: depletion due to tetrahydrobiopterin deficiency induced by 2,4-diamino-6-hydroxypyrimidine administration. J Pharmacol Exp Ther 1991; 256:773-9.
23. Eissa NT, Yuan JW, Haggerty CM, Choo EK, Palmer CD, Moss J. Cloning and characterization of human inducible nitric oxide synthase splice variants: a domain, encoded by exons 8 and 9, is critical for dimerization. Proc Natl Acad Sci U S A 1998; 95:7625-30.
24. Yim JJ, Brown GM. Characteristics of guanosine triphosphate cyclohydrolase I purified from Escherichia coli. J Biol Chem 1976; 251:5087-94.
25. Fink AL. Chaperone-mediated protein folding. Physiol Rev 1999; 79:425-49.
26. Randow F, Seed B. Endoplasmic reticulum chaperone gp96 is required for innate immunity but not cell viability. Nat Cell Biol 2001; 3:891-6.
27. Rudrabhatla RS, Selvaraj SK, Prasadarao NV. Role of Rac1 in Escherichia coli K1 invasion of human brain microvascular endothelial cells. Microbes Infect 2006; 8:460-9.
28. Hwu WL, Lu MY, Hwa KY, Fan SW, Lee YM. Molecular chaperones affect GTP cyclohydrolase I mutations in dopa-responsive dystonia. Ann Neurol 2004; 55:875-8.
29. Togari A, Arai M, Mogi M, Kondo A, Nagatsu T. Coexpression of GTP cyclohydrolase I and inducible nitric oxide synthase mRNAs in mouse osteoblastic cells activated by proinflammatory cytokines. FEBS Lett 1998; 428:212-6.
30. Frank S, Madlener M, Pfeilschifter J, Werner S. Induction of inducible nitric oxide synthase and its corresponding tetrahydrobiopterin-cofactor- synthesizing enzyme GTP-cyclohydrolase I during cutaneous wound repair. J Invest Dermatol 1998; 111:1058-64.
31. Geller DA, Di Silvio M, Billiar TR, Hatakeyama K. GTP cyclohydrolase I is coinduced in hepatocytes stimulated to produce nitric oxide. Biochem Biophys Res Commun 2000; 276:633-41.
32. Li HY, Yao YM, Shi ZG, et al. Effect of 2,4-diamino-6-hydroxy-pyrimidine on postburn Staphylococcus aureus sepsis in rats. Crit Care Med 2002; 30:2520-7.
33. van Amsterdam JG, van den Berg C, Zuidema J, te Biesebeek JD, Rokos H. Effect of septicaemia on the plasma levels of biopterin and nitric oxide metabolites in rats and rabbits. Biochem Pharmacol 1996; 52:1447-51.
34. Melichar B, Malirova E, Bures J, et al. Gastric juice neopterin in Helicobacter pylori infection. FEMS Immunol Med Microbiol 1995; 10:335-8.
35. Villavicencio RT, Liu S, Kibbe MR, et al. Induced nitric oxide inhibits IL-6-induced stat3 activation and type II acute phase mRNA expression. Shock 2000; 13:441-5.
36. Terpolilli NA, Zweckberger K, Trabold R, et al. The novel nitric oxide synthase inhibitor 4-amino-tetrahydro-L-biopterine prevents brain edema formation and intracranial hypertension following traumatic brain injury in mice. J Neurotrauma 2009; 26:1963-75.