Membrane interaction of Pasteurella multocida toxin involves sphingomyelin

FEBS Journal

Volumn 278, Issue 23, 2011, Pages 4633-4648

  Brothers, Michael C ^a   Ho, Mengfei ^a   Maharjan, Ram ^a   Clemons, Nathan C ^a   Bannai, Yuka ^a   Waites, Mark A ^a   Faulkner, Melinda J ^a   Kuhlenschmidt, Theresa B ^a   Kuhlenschmidt, Mark S ^a   Blanke, Steven R ^a   Rienstra, Chad M ^a   Wilson, Brenda A ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

dermonecrotic toxin; ganglioside; phosphatidylcholine; surface plasmon resonance; thin layer chromatography

Indexed keywords

AMINO TERMINAL PASTEURELLA MULTOCIDA TOXIN; BACTERIAL TOXIN; CARBOXY TERMINAL PASTEURELLA MULTOCIDA TOXIN; GANGLIOSIDE GM1; GANGLIOSIDE GM2; GANGLIOSIDE GM3; GLYCEROPHOSPHOLIPID; MEMBRANE PHOSPHOLIPID; PASTEURELLA MULTOCIDA TOXIN; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLSERINE; PHOSPHOLIPASE D; SPHINGOMYELIN; SPHINGOMYELIN PHOSPHODIESTERASE; SPHINGOPHOSPHOLIPID; TRYPSIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CELL INTERACTION; CELL MEMBRANE; CONTROLLED STUDY; MEMBRANE BINDING; MEMBRANE COMPONENT; MEMBRANE STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEOLIPOSOME; SURFACE PLASMON RESONANCE; THIN LAYER CHROMATOGRAPHY;

ANIMALS; BACTERIAL PROTEINS; BACTERIAL TOXINS; BINDING SITES; CELL LINE; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; HUMANS; MICE; PASTEURELLA MULTOCIDA; SPHINGOMYELINS; SURFACE PLASMON RESONANCE;

PASTEURELLA MULTOCIDA;

EID: 81555228589     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08365.x     Document Type: Article

References (54)

1. Foged NT, (1992) Pasteurella multocida toxin. The characterisation of the toxin and its significance in the diagnosis and prevention of progressive atrophic rhinitis in pigs. APMIS Suppl 25, 1-56.
2. Pedersen KB, &, Barfod K, (1981) The aetiological significance of Bordetella bronchiseptica and Pasteurella multocida in atrophic rhinitis of swine. Nord Vet Med 33, 513-522.
3. Wilson BA, &, Ho MH, (2006) Pasteurella multocida toxin. In The Comprehensive Sourcebook of Bacterial Protein Toxins (, Alouf JE, &, Popoff MR, eds), pp. 430-447. Elsevier, Amsterdam, Boston.
4. Wilson BA, &, Ho M, (2004) Pasteurella multocida toxin as a tool for studying Gq signal transduction. Rev Physiol Biochem Pharmacol 152, 93-109. (Pubitemid 44404360)
5. Wilson BA, &, Ho MF, (2010) Recent insights into Pasteurella multocida toxin and other G-protein-modulating bacterial toxins. Future Microbiol 5, 1185-1201.
6. Mullan PB, &, Lax AJ, (1996) Pasteurella multocida toxin is a mitogen for bone cells in primary culture. Infect Immun 64, 959-965. (Pubitemid 26065573)
7. Rozengurt E, Higgins T, Chanter N, Lax AJ, &, Staddon JM, (1990) Pasteurella multocida toxin-potent mitogen for cultured fibroblasts. Proc Natl Acad Sci USA 87, 123-127.
8. Wilson BA, Aminova LR, Ponferrada VG, &, Ho MF, (2000) Differential modulation and subsequent blockade of mitogenic signaling and cell cycle progression by Pasteurella multocida toxin. Infect Immun 68, 4531-4538. (Pubitemid 30497720)
9. Orth JHC, Fester I, Preuss I, Agnoletto L, Wilson BA, &, Aktories K, (2008) Activation of G alpha(i) and subsequent uncoupling of receptor-G alpha(i) signaling by Pasteurella multocida toxin. J Biol Chem 283, 23288-23294.
10. Orth JHC, Lang S, Taniguchi M, &, Aktories K, (2005) Pasteurella multocida toxin-induced activation of RhoA is mediated via two families of G alpha proteins, G alpha(q) and G alpha(12/13). J Biol Chem 280, 36701-36707. (Pubitemid 41587748)
11. Orth JHC, Preuss I, Fester I, Schlosser A, Wilson BA, &, Aktories K, (2009) Pasteurella multocida toxin activation of heterotrimeric G proteins by deamidation. Proc Natl Acad Sci USA 106, 7179-7184.
12. Wilson BA, Zhu X, Ho M, &, Lu L, (1997) Pasteurella multocida toxin activates the inositol triphosphate signaling pathway in Xenopus oocytes via G(q)alpha-coupled phospholipase C-beta1. J Biol Chem 272, 1268-1275. (Pubitemid 27034627)
13. Zywietz A, Gohla A, Schmelz M, Schultz G, &, Offermanns S, (2001) Pleiotropic effects of Pasteurella multocida toxin are mediated by G(q)-dependent and -independent mechanisms-involvement of G(q) but not G(11). J Biol Chem 276, 3840-3845.
14. Kitadokoro K, Kamitani S, Miyazawa M, Hanajima-Ozawa M, Fukui A, Miyake M, &, Horiguchi Y, (2007) Crystal structures reveal a thiol protease-like catalytic triad in the C-terminal region of Pasteurella multocida toxin. Proc Natl Acad Sci USA 104, 5139-5144. (Pubitemid 47186189)
15. Kamitani S, Kitadokoro K, Miyazawa M, Toshima H, Fukui A, Abe H, Miyake M, &, Horiguchi Y, (2010) Characterization of the membrane-targeting C1 domain in Pasteurella multocida toxin. J Biol Chem 285, 25467-25475.
16. Aminova LR, Luo SH, Bannai Y, Ho MF, &, Wilson BA, (2008) The C3 domain of Pasteurella multocida toxin is the minimal domain responsible for activation of G(q)-dependent calcium and mitogenic signaling. Protein Sci 17, 945-949. (Pubitemid 351629589)
17. Baldwin MR, Lakey JH, &, Lax AJ, (2004) Identification and characterization of the Pasteurella multocida toxin translocation domain. Mol Microbiol 54, 239-250. (Pubitemid 39315172)
18. Pullinger GD, Sowdhamini R, &, Lax AJ, (2001) Localization of functional domains of the mitogenic toxin of Pasteurella multocida. Infect Immun 69, 7839-7850. (Pubitemid 33086615)
19. Falbo V, Pace T, Picci L, Pizzi E, &, Caprioli A, (1993) Isolation and nucleotide-sequence of the gene encoding cytotoxic necrotizing factor-I of Escherichia coli. Infect Immun 61, 4909-4914. (Pubitemid 23320556)
20. Oswald E, Sugai M, Labigne A, Wu HC, Fiorentini C, Boquet P, &, Obrien AD, (1994) Cytotoxic necrotizing factor type-2 produced by virulent Escherichia coli modifies the small GTP-binding proteins-Rho involved in assembly of actin stress fibers. Proc Natl Acad Sci USA 91, 3814-3818. (Pubitemid 24139522)
21. Stoll T, Markwirth G, Reipschlager S, &, Schmidt G, (2009) A new member of a growing toxin family-Escherichia coli cytotoxic necrotizing factor 3 (CNF3). Toxicon 54, 745-753.
22. Lockman HA, Gillespie RA, Baker BD, &, Shakhnovich E, (2002) Yersinia pseudotuberculosis produces a cytotoxic necrotizing factor. Infect Immun 70, 2708-2714. (Pubitemid 34408421)
23. Blumenthal B, Hoffmann C, Aktories M, Backert S, &, Schmidt G, (2007) The cytotoxic necrotizing factors from Yersinia pseudotuberculosis and from Escherichia coli bind to different cellular receptors but take the same route to the cytosol. Infect Immun 75, 3344-3353. (Pubitemid 47040935)
24. Chung JW, Hong SJ, Kim KJ, Goti D, Stins MF, Shin S, Dawson VL, Dawson TM, &, Kim KS, (2003) 37-kDa laminin receptor precursor modulates cytotoxic necrotizing factor 1-mediated RhoA activation and bacterial uptake. J Biol Chem 278, 16857-16862. (Pubitemid 36799556)
25. Kim KJ, Chung JW, &, Kim KS, (2005) 67-kDa laminin receptor promotes internalization of cytotoxic necrotizing factor 1-expressing Escherichia coli K1 into human brain microvascular endothelial cells. J Biol Chem 280, 1360-1368.
26. Lemichez E, Flatau G, Bruzzone M, Boquet P, &, Gauthier M, (1997) Molecular localization of the Escherichia coli cytotoxic necrotizing factor CNF1 cell-binding and catalytic domains. Mol Microbiol 24, 1061-1070. (Pubitemid 27286157)
27. Dudet LI, Chailler P, Dubreuil JD, &, MartineauDoize B, (1996) Pasteurella multocida toxin stimulates mitogenesis and cytoskeleton reorganization in Swiss 3T3 fibroblasts. J Cell Physiol 168, 173-182. (Pubitemid 26233446)
28. Pettit RK, Ackermann MR, &, Rimler RB, (1993) Receptor-mediated binding of Pasteurella multocida dermonecrotic toxin to canine osteosarcoma and monkey kidney (Vero) cells. Lab Invest 69, 94-100. (Pubitemid 23222251)
29. Merritt EA, Sarfaty S, Vandenakker F, Lhoir C, Martial JA, &, Hol WGJ, (1994) Crystal structure of cholera toxin B-pentamer bound to receptor G(M1) pentasaccharide. Protein Sci 3, 166-175. (Pubitemid 24086350)
30. Naglich JG, Metherall JE, Russell DW, &, Eidels L, (1992) Expression cloning of a diphtheria-toxin receptor-identity with a heparin-binding EGF-like growth-factor precursor. Cell 69, 1051-1061.
31. Binz T, &, Rummel A, (2009) Cell entry strategy of clostridial neurotoxins. J Neurochem 109, 1584-1595.
32. Dong M, Yeh F, Tepp WH, Dean C, Johnson EA, Janz R, &, Chapman ER, (2006) SV2 is the protein receptor for botulinum neurotoxin A. Science 312, 592-596.
33. Cumar FA, Maggio B, &, Caputto R, (1982) Ganglioside-cholera toxin interactions-a binding and lipid monolayer study. Mol Cell Biochem 46, 155-160. (Pubitemid 13228938)
34. Berenson CS, Nawar HF, Yohe HC, Castle SA, Ashline DJ, Reinhold VN, Hajishengallis G, &, Connell TD, (2010) Mammalian cell ganglioside-binding specificities of E. coli enterotoxins LT-IIb and variant LT-IIb(T13I). Glycobiology 20, 41-54.
35. Griffitts JS, Haslam SM, Yang T, Garczynski SF, Mulloy B, Morris H, Cremer PS, Dell A, Adang MJ, &, Aroian RV, (2005) Glycolipids as receptors for Bacillus thuringiensis crystal toxin. Science 307, 922-925. (Pubitemid 40229228)
36. Walton KM, Sandberg K, Rogers TB, &, Schnaar RL, (1988) Complex ganglioside expression and tetanus toxin binding by PC12 pheochromocytoma cells. J Biol Chem 263, 2055-2063. (Pubitemid 18052169)
37. Takamizawa K, Iwamori M, Kozaki S, Sakaguchi G, Tanaka R, Takayama H, &, Nagai Y, (1986) TLC immunostaining characterization of Clostridium botulinum type A neurotoxin binding to gangliosides and free fatty acids. FEBS Lett 201, 229-232. (Pubitemid 16060736)
38. Flagler MJ, Mahajan SS, Kulkarni AA, Iyer SS, &, Weiss AA, (2010) Comparison of binding platforms yields insights into receptor binding differences between Shiga toxins 1 and 2. Biochemistry 49, 1649-1657.
39. Kuziemko GM, Stroh M, &, Stevens RC, (1996) Cholera toxin binding affinity and specificity for gangliosides determined by surface plasmon resonance. Biochemistry 35, 6375-6384. (Pubitemid 26164071)
40. Wigelsworth DJ, Krantz BA, Christensen KA, Lacy DB, Juris SJ, &, Collier RJ, (2004) Binding stoichiometry and kinetics of the interaction of a human anthrax toxin receptor, CMG2, with protective antigen. J Biol Chem 279, 23349-23356. (Pubitemid 38685644)
41. MacKenzie CR, Hirama T, Lee KK, Altman E, &, Young NM, (1997) Quantitative analysis of bacterial toxin affinity and specificity for glycolipid receptors by surface plasmon resonance. J Biol Chem 272, 5533-5538. (Pubitemid 27102376)
42. Yowler BC, &, Schengrund CL, (2004) Botulinum neurotoxin A changes conformation upon binding to ganglioside GT1b. Biochemistry 43, 9725-9731. (Pubitemid 38993822)
43. O'Shannessy DJ, Brighamburke M, Soneson KK, Hensley P, &, Brooks I, (1993) Determination of rate and equilibrium binding constants for macromolecular interactions using surface-plasmon resonance-use of nonlinear least-squares analysis-methods. Anal Biochem 212, 457-468. (Pubitemid 23245098)
44. Oda M, Takahashi M, Matsuno T, Uoo K, Nagahama M, &, Sakurai J, (2010) Hemolysis induced by Bacillus cereus sphingomyelinase. Biochim Biophys Acta 1798, 1073-1080.
45. Yang HY, &, Roberts MF, (2003) Phosphohydrolase and transphosphatidylation reactions of two Streptomyces phospholipase D enzymes: covalent versus noncovalent catalysis. Protein Sci 12, 2087-2098. (Pubitemid 37022830)
46. Dippe M, &, Ulbrich-Hofmann R, (2009) Substrate specificity in phospholipid transformations by plant phospholipase D isoenzymes. Phytochemistry 70, 361-365.
47. Hashiramoto A, Mizukami H, &, Yamashita T, (2006) Ganglioside GM3 promotes cell migration by regulating MAPK and c-Fos/AP-1. Oncogene 25, 3948-3955. (Pubitemid 43990750)
48. Rusnati M, Tanghetti E, Urbinati C, Tulipano G, Marchesini S, Ziche M, &, Presta M, (1999) Interaction of fibroblast growth factor-2 (FGF-2) with free gangliosides: biochemical characterization and biological consequences in endothelial cell cultures. Mol Biol Cell 10, 313-327. (Pubitemid 29156475)
49. Yates AJ, VanBrocklyn J, Saqr HE, Guan Z, Stokes BT, &, O'Dorisio MS, (1993) Mechanisms through which gangliosides inhibit PDGF-stimulated mitogenesis in intact Swiss 3T3 cells: receptor tyrosine phosphorylation, intracellular calcium, and receptor binding. Exp Cell Res 204, 38-45. (Pubitemid 23203083)
50. Cremesti AE, Goni FM, &, Kolesnick R, (2002) Role of sphingomyelinase and ceramide in modulating rafts: do biophysical properties determine biologic outcome? FEBS Lett 531, 47-53. (Pubitemid 35232783)
51. Gupta VR, Patel HK, Kostolansky SS, Ballivian RA, Eichberg J, &, Blanke SR, (2008) Sphingomyelin functions as a novel receptor for Helicobacter pylori VacA. PLoS Pathogens 4, e1000073.
52. Gupta VR, Wilson BA, &, Blanke SR, (2010) Sphingomyelin is important for the cellular entry and intracellular localization of Helicobacter pylori VacA. Cell Microbiol 12, 1517-1533.
53. Ames BN, (1966) Assay of inorganic phosphate, total phosphate and phosphatase. In Methods in Enzymology (, Neufeld E, &, Ginsburg V, eds), pp. 115-118. Academic Press, New York.
54. Boone CW, Ford LE, Bond HE, Stuart DC, &, Lorenz D, (1969) Isolation of plasma membrane fragments from Hela cells. J Cell Biol 41, 378.