Commercially available recombinant sonic hedgehog up-regulates Ptc and modulates the cytokine and chemokine expression of human macrophages: An effect mediated by endotoxin contamination?

Immunobiology

Volumn 213, Issue 1, 2008, Pages 25-38

  Wakelin, Sonia J ^a,b   Forsythe, John L R ^b   Garden, O James ^b   Howie, Sarah E M ^a,c  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b ROYAL INFIRMARY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Chemokines; Cytokines; Endotoxin; Macrophages; Sonic hedgehog

Indexed keywords

CD14 ANTIGEN; CHEMOKINE; CYCLOPAMINE; CYTOKINE; ENDOTOXIN; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1; POLYMYXIN B; PROTEIN PATCHED; RANTES; RECOMBINANT PROTEIN; SONIC HEDGEHOG PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN;

ARTICLE; CONTAMINATION; CONTROLLED STUDY; CULTURE MEDIUM; CYTOKINE PRODUCTION; FETAL CALF SERUM; HUMAN; HUMAN CELL; IMMUNOMODULATION; IN VITRO STUDY; INHIBITION KINETICS; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 38149120774     PISSN: 01712985     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imbio.2007.06.006     Document Type: Article

References (67)

1. Alcedo J., Ayzenzon M., Von Ohlen T., Noll M., and Hooper J.E. The Drosophila smoothened gene encodes a seven-pass membrane protein, a putative receptor for the hedgehog signal. Cell 86 (1996) 221-232
2. Altaba A. Gli proteins encode context-dependent positive and negative functions: implications for development and disease. Development 126 (1999) 3205-3216
3. Anspach F.B., and Hilbeck O. Removal of endotoxins by affinity sorbents. J. Chromatogr. A 711 (1995) 81-92
4. Ardeshna K.M., Pizzey A.R., Devereux S., and Khwaja A. The PI3 kinase, p38 SAP kinase, and NF-kappaB signal transduction pathways are involved in the survival and maturation of lipopolysaccharide-stimulated human monocyte-derived dendritic cells. Blood 96 (2000) 1039-1046
5. Asea A., Kraeft S.K., Kurt-Jones E.A., Stevenson M.A., Chen L.B., Finberg R.W., Koo G.C., and Calderwood S.K. HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat. Med. 6 (2000) 435-442
6. Asea A., Rehli M., Kabingu E., Boch J.A., Bare O., Auron P.E., Stevenson M.A., and Calderwood S.K. Novel signal transduction pathway utilized by extracellular HSP70: role of toll-like receptor (TLR) 2 and TLR4. J. Biol. Chem. 277 (2002) 15028-15034
7. Bethke K., Staib F., Distler M., Schmitt U., Jonuleit H., Enk A.H., Galle P.R., and Heike M. Different efficiency of heat shock proteins (HSP) to activate human monocytes and dendritic cells: superiority of HSP60. J. Immunol. 169 (2002) 6141-6148
8. Bhardwaj G., Murdoch B., Wu D., Baker D.P., Williams K.P., Chadwick K., Linq L.E., Karanu F.N., and Bhatia M. Sonic hedgehog induces the proliferation of primitive human hematopoietic cells via BMP regulation. Nat. Immunol. 2 (2001) 172-180
9. Biragyn A., Ruffini P.A., Leifer C.A., Klyushnenkova E., Shakhov A., Chertov O., Shirakawa A.K., Farber J.M., Oppebheim J.J., and Kwak L.W. Toll-like receptor 4-dependent activation of dendritic cells by beta-defensin 2. Science 298 (2002) 1025-1029
10. Bitgood M.J., and McMahon A.P. Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev. Biol. 172 (1995) 126-138
11. Bruneau S., and Rosa F.M. Dynamo, a new zebrafish DVR member of the TGF-beta superfamily is expressed in the posterior neural tube and is up-regulated by sonic hedgehog. Mech. Dev. 61 (1997) 199-212
12. Bulut Y., Faure E., Thomas L., Karahashi H., Michelsen K.S., Equils O., Morrison S.G., Morrison R.P., and Arditi M. Chlamydial heat shock protein 60 activates macrophages and endothelial cells through Toll-like receptor 4 and MD2 in a MyD88-dependent pathway. J. Immunol. 168 (2002) 1435-1440
13. Bumcrot D.A., Takada R., and McMahon A.P. Proteolytic processing yields two secreted forms of sonic hedgehog. Mol. Cell. Biol. 15 (1995) 2294-2303
14. Chen W., Syldath U., Bellmann K., Burkart V., and Kolb H. Human 60-kDa heat-shock protein: a danger signal to the innate immune system. J. Immunol. 162 (1999) 3212-3219
15. Chen J.K., Taipale J., Cooper M.K., and Beachy P.A. Inhibition of Hedgehog signaling by direct binding of cyclopamine to Smoothened. Genes. Dev. 16 (2002) 2743-2748
16. Chiang C., Litingtung Y., Lee E., Young K.E., Corden J.L., Westphal H., and Beachy P.A. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383 (1996) 407-413
17. Chtanova T., Kemp R.A., Sutherland A.P., Ronchese F., and Mackay C.R. Gene microarrays reveal extensive differential gene expression in both CD4(+) and CD8(+) type 1 and type 2 T cells. J. Immunol. 167 (2001) 3057-3063
18. Dybdahl B., Wahba A., Lien E., Flo T.H., Waage A., Qureshi N., Sellevold O.F., Espevik T., and Sundan A. Inflammatory response after open heart surgery: release of heat-shock protein 70 and signaling through toll-like receptor-4. Circulation 105 (2002) 685-690
19. Fan H., and Khavari P.A. Sonic hedgehog opposes epithelial cell cycle arrest. J. Cell. Biol. 147 (1999) 71-76
20. Fan J., Frey R.S., and Malik A.B. TLR4 signaling induces TLR2 expression in endothelial cells via neutrophil NADPH oxidase. J. Clin. Invest. 112 (2003) 1234-1243
21. Ferguson C.M., Miclau T., Hu D., Alpern E., and Helms J.A. Common molecular pathways in skeletal morphogenesis and repair. Ann. NY Acad. Sci. 857 (1998) 33-42
22. Gao B., and Tsan M.F. Recombinant human heat shock protein 60 does not induce the release of tumor necrosis factor alpha from murine macrophages. J. Biol. Chem. 278 (2003) 22523-22529
23. Gao B., and Tsan M.F. Endotoxin contamination in recombinant human heat shock protein 70 (Hsp70) preparation is responsible for the induction of tumor necrosis factor alpha release by murine macrophages. J. Biol. Chem. 278 (2003) 174-179
24. Goodrich L.V., Johnson R.L., Milenkovic L., McMahon J.A., and Scott M.P. Conservation of the hedgehog/patched signaling pathway from flies to mice: induction of a mouse patched gene by Hedgehog. Genes. Dev. 10 (1996) 301-312
25. Goodrich L.V., Milenkovic L., Higgins K.M., and Scott M.P. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277 (1997) 1109-1113
26. Gordon S. Alternative activation of macrophages. Nat. Rev. Immunol. 3 (2003) 23-35
27. Granucci F., Castagnoli P.R., Rogge L., and Sinigaglia F. Gene expression profiling in immune cells using microarray. Int. Arch. Allergy. Immunol. 126 (2001) 257-266
28. Hammerschmidt M., Brook A., and McMahon A.P. The world according to hedgehog. Trends Genet. 13 (1997) 14-21
29. Incardona J.P., Gaffield W., Kapur R.P., and Roelink H. The teratogenic Veratrum alkaloid cyclopamine inhibits sonic hedgehog signal transduction. Development 125 (1998) 3553-3562
30. Ingham P.W. Transducing Hedgehog: the story so far. EMBO J. 17 (1998) 3505-3511
31. Ingham P.W., Nystedt S., Nakano Y., Brown W., Stark D., van den Heuvel M., and Taylor A.M. Patched represses the Hedgehog signalling pathway by promoting modification of the Smoothened protein. Curr. Biol. 10 (2000) 1315-1318
32. Issekutz A.C. Removal of Gram-negative endotoxin from solutions by affinity chromatography. J. Immunol. Meth. 61 (1983) 275-281
33. Kanda S., Mochizuki Y., Suematsu T., Miyata Y., Nomata K., and Kanetake H. Sonic hedgehog induces capillary morphogenesis by endothelial cells through phosphoinositide 3-kinase. J. Biol. Chem. 278 (2003) 8244-8249
34. Karahashi H., and Amano F. Endotoxin-tolerance to the cytotoxicity toward a macrophage-like cell line, J774.1, induced by lipopolysaccharide and cycloheximide: role of p38 MAPK in induction of the cytotoxicity. Biol. Pharm. Bull. 26 (2003) 1249-1259
35. Kaufmann A., Gemsa D., and Sprenger H. Differential desensitization of lipopolysaccharide-inducible chemokine gene expression in human monocytes and macrophages. Eur. J. Immunol. 30 (2000) 1562-1567
36. Kenney A.M., and Rowitch D.H. Sonic hedgehog promotes G(1) cyclin expression and sustained cell cycle progression in mammalian neuronal precursors. Mol. Cell. Biol. 20 (2000) 9055-9067
37. Kol A., Bourcier T., Lichtman A.H., and Libby P. Chlamydial and human heat shock protein 60 s activate human vascular endothelium, smooth muscle cells, and macrophages. J. Clin. Invest. 103 (1999) 571-577
38. Kol A., Lichtman A.H., Finberg R.W., Libby P., and Kurt-Jones E.A. Cutting edge: heat shock protein (HSP) 60 activates the innate immune response: CD14 is an essential receptor for HSP60 activation of mononuclear cells. J. Immunol. 164 (2000) 13-17
39. Lee J.J., Ekker S.C., von Kessler D.P., Porter J.A., Sun B.I., and Beachy P.A. Autoproteolysis in hedgehog protein biogenesis. Science 266 (1994) 1528-1537
40. Lin G., Pearson A.E., Scamurra R.W., Zhou Y., Baarsch M.J., Weiss D.J., and Murtaugh M.P. Regulation of interleukin-8 expression in porcine alveolar macrophages by bacterial lipopolysaccharide. J. Biol. Chem. 269 (1994) 77-85
41. Lindsay G.K., Roslansky P.F., and Novitsky T.J. Single-step, chromogenic Limulus amebocyte lysate assay for endotoxin. J. Clin. Microbiol. 27 (1989) 947-951
42. Lowrey J.A., Stewart G.A., Lindey S., Hoyne G.F., Dallman M.J., Howie S.E., and Lamb J.R. Sonic hedgehog promotes cell cycle progression in activated peripheral CD4(+) T lymphocytes. J. Immunol. 169 (2002) 1869-1875
43. Marigo V., and Tabin C.J. Regulation of patched by sonic hedgehog in the developing neural tube. Proc. Natl. Acad. Sci. USA 93 (1996) 9346-9351
44. McMahon A.P., Ingham P.W., and Tabin C.J. Developmental roles and clinical significance of hedgehog signaling. Curr. Top. Dev. Biol. 53 (2003) 1-114
45. Mosser D.M. The many faces of macrophage activation. J. Leukoc. Biol. 73 (2003) 209-212
46. Murone M., Rosenthal A., and de Sauvage F.J. Sonic hedgehog signaling by the patched-smoothened receptor complex. Curr. Biol. 9 (1999) 76-84
47. Nielsen C.M., Williams J., van den Brink G.R., Lauwers G.Y., and Roberts D.J. Hh pathway expression in human gut tissues and in inflammatory gut diseases. Lab. Invest. 84 (2004) 1631-1642
48. Nishita M., Hashimoto M.K., Ogata S., Laurent M.N., Ueno N., Shibuya H., and Cho K.W. Interaction between Wnt and TGF-beta signalling pathways during formation of Spemann's organizer. Nature 403 (2000) 781-785
49. Nusslein-Volhard C., and Wieschaus E. Mutations affecting segment number and polarity in Drosophila. Nature 287 (1980) 795-801
50. Ohashi K., Burkart V., Flohe S., and Kolb H. Cutting edge: heat shock protein 60 is a putative endogenous ligand of the toll-like receptor-4 complex. J. Immunol. 164 (2000) 558-561
51. Ojaniemi M., Glumoff V., Harju K., Liljeroos M., Vuori K., and Hallman M. Phosphatidylinositol 3-kinase is involved in Toll-like receptor 4-mediated cytokine expression in mouse macrophages. Eur. J. Immunol. 33 (2003) 597-605
52. Okamura Y., Watari M., Jerud E.S., Young D.W., Ishizaka S.T., Rose J., Chow J.C., and Strauss J.F.III. The extra domain A of fibronectin activates Toll-like receptor 4. J. Biol. Chem. 276 (2001) 10229-10233
53. Pola R., Ling L.E., Silver M., Corbley M.J., Kearney M., Blake P.R., Shapiro R., Taylor F.R., Baker D.P., Asahara T., and Isner J.M. The morphogen Sonic hedgehog is an indirect angiogenic agent upregulating two families of angiogenic growth factors. Nat. Med. 7 (2001) 706-711
54. Porter J.A., von Kessler D.P., Ekker S.C., Young K.E., Lee J.J., Moses K., and Beachy P.A. The product of hedgehog autoproteolytic cleavage active in local and long-range signalling. Nature 374 (1995) 363-366
55. Ramalho-Santos M., Melton D.A., and McMahon A.P. Hedgehog signals regulate multiple aspects of gastrointestinal development. Development 127 (2000) 2763-2772
56. Ravasi T., Wells C., Forest A., Underhill D.M., Wainwright B.J., Aderem A., Grimmond S., and Hume D.A. Generation of diversity in the innate immune system: macrophage heterogeneity arises from gene-autonomous transcriptional probability of individual inducible genes. J. Immunol. 168 (2002) 44-50
57. Sasaki H., Nishizaki Y., Hui C., Nakafuku M., and Kondoh H. Regulation of Gli2 and Gli3 activities by an amino-terminal repression domain: implication of Gli2 and Gli3 as primary mediators of Shh signaling. Development 126 (1999) 3915-3924
58. Sato S., Nomura F., Kawai T., Takeuchi O., Muhlradt P.F., Takeda K., and Akira S. Synergy and cross-tolerance between toll-like receptor (TLR) 2- and TLR4-mediated signaling pathways. J. Immunol. 165 (2000) 7096-7101
59. Smiley S.T., King J.A., and Hancock W.W. Fibrinogen stimulates macrophage chemokine secretion through toll-like receptor 4. J. Immunol. 167 (2001) 2887-2894
60. Stewart G.A., Lowrey J.A., Wakelin S.J., Fitch P.M., Lindey S., Dallman M.J., Lamb J.R., and Howie S.E.M. Sonic hedgehog signaling modulates activation of and cytokine production by human peripheral CD4+T cells. J. Immunol. 169 (2002) 5451-5457
61. Stewart G.A., Hoyne G.F., Ahmad S.A., Jarman E., Wallace W.A., Harrison D.J., Haslett C., Lamb J.R., and Howie S.E. Expression of the developmental Sonic hedgehog (Shh) signalling pathway is up-regulated in chronic lung fibrosis and the Shh receptor patched 1 is present in circulating T lymphocytes. J. Pathol. 199 (2003) 488-495
62. Stone D.M., Hynes M., Armanini M., Swanson T.A., Gu Q., Johnson R.L., Scott M.P., Pennica D., Goddard A., Phillips H., Noll M., Hooper J.E., de Sauvage F., and Rosenthal A. The tumour-suppressor gene patched encodes a candidate receptor for Sonic hedgehog. Nature 384 (1996) 129-134
63. Taipale J., Chen J.K., Cooper M.K., Wang B., Mann R.K., Milenkovic L., Scott M.P., and Beachy P.A. Effects of oncogenic mutations in smoothened and patched can be reversed by cyclopamine. Nature 406 (2000) 1005-1009
64. Talmadge K.W., and Siebert C.J. Efficient endotoxin removal with a new sanitizable affinity column: affi-Prep Polymyxin. J. Chromatogr. 476 (1989) 175-185
65. Vabulas R.M., Ahmad-Nejad P., Ghose S., Kirschning C.J., Issels R.D., and Wagner H. HSP70 as endogenous stimulus of the Toll/interleukin-1 receptor signal pathway. J. Biol. Chem. 277 (2002) 15107-15112
66. Wakelin S.J., Sabroe I., Gregory C.D., Poxton I.R., Forsythe J.L., Garden O.J., and Howie S.E. "Dirty little secrets"-Endotoxin contamination of recombinant proteins. Immunol. Lett. 106 (2006) 1-7
67. Watkins D.N., Berman D.M., Burkholder S.G., Wang B., Beachy P.A., and Baylin S.B. Hedgehog signalling within airway epithelial progenitors and in small-cell lung cancer. Nature 422 (2003) 313-317