Therapeutic effects of Clostridium botulinum C3 exoenzyme

Naunyn-Schmiedeberg's Archives of Pharmacology

Volumn 383, Issue 3, 2011, Pages 247-252

  Just, Ingo ^a   Rohrbeck, Astrid ^a   Huelsenbeck, Stefanie C ^a   Hoeltje, Markus ^b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

ARTT loop; Axon; C3 exoenzyme; Growth cone; Neuronal injury; Neurone; Rho

Indexed keywords

BA 210; CETHRIN; EXOENZYME C3; NEUROPROTECTIVE AGENT; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; RHO FACTOR; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ASTROCYTE; CELL DIFFERENTIATION; CELL GROWTH; CLOSTRIDIUM BOTULINUM; DENDRITE; ENZYME ACTIVITY; HIPPOCAMPUS; HUMAN; MICROGLIA; NERVE CELL; NERVE FIBER; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SPINAL CORD INJURY;

ADP RIBOSE TRANSFERASES; ANIMALS; BOTULINUM TOXINS; HUMANS; NERVE REGENERATION; RHO GTP-BINDING PROTEINS; SPINAL CORD INJURIES;

EID: 79954574423     PISSN: 00281298     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00210-010-0589-3     Document Type: Review

References (56)

1. G Ahnert-Hilger M Höltje G Groe G Pickert C Mucke B Nixdorf-Bergweiler P Boquet F Hofmann I Just 2004 Differential effects of Rho GTPases on axonal and dendritic development in hippocampal neurons J Neurochem 90 9 18 1:CAS:528:DC%2BD2cXlvFKlsrk%3D 10.1111/j.1471-4159.2004.02475.x 15198662 (Pubitemid 38879157)
2. K Aktories I Just 2005 Clostridial Rho-inhibiting protein toxins Curr Top Microbiol Immunol 291 113 145 1:CAS:528:DC%2BD2MXnslyitbg%3D 10.1007/3-540-27511-8-7 15981462 (Pubitemid 40674913)
3. K Aktories M Bärmann I Ohishi S Tsuyama KH Jakobs E Habermann 1986 Botulinum C2 toxin ADP-ribosylates actin Nature 322 390 392 1:CAS:528: DyaL28XltFShtr8%3D 10.1038/322390a0 3736664 (Pubitemid 16098143)
4. K Aktories U Weller GS Chhatwal 1987 Clostridium botulinum type C produces a novel ADP-ribosyltransferase distinct from botulinum C2 toxin FEBS Lett 212 109 113 1:CAS:528:DyaL2sXitV2rtLw%3D 10.1016/0014-5793(87)81566-1 3100333 (Pubitemid 17028086)
5. K Aktories C Wilde M Vogelsgesang 2004 Rho-modifying C3-like ADP-ribosyltransferases Rev Physiol Biochem Pharmacol 152 1 22 1:CAS:528:DC%2BD2MXhsVagu7c%3D 10.1007/s10254-004-0034-4 15372308 (Pubitemid 44417934)
6. P Aspenström A Fransson J Saras 2004 Rho GTPases have diverse effects on the organization of the actin filament system Biochem J 377 327 337 10.1042/BJ20031041 14521508 (Pubitemid 38142188)
7. J Bertrand MJ Winton N Rodriguez-Hernandez RB Campenot L McKerracher 2005 Application of Rho antagonist to neuronal cell bodies promotes neurite growth in compartmented cultures and regeneration of retinal ganglion cell axons in the optic nerve of adult rats J Neurosci 25 1113 1121 1:CAS:528: DC%2BD2MXhsVahs74%3D 10.1523/JNEUROSCI.3931-04.2005 15689547 (Pubitemid 40268952)
8. J Bertrand A Di Polo L McKerracher 2007 Enhanced survival and regeneration of axotomized retinal neurons by repeated delivery of cell-permeable C3-like Rho antagonists Neurobiol Dis 25 65 72 1:CAS:528:DC%2BD28Xht1Cls7rM 10.1016/j.nbd.2006.08.008 17011202 (Pubitemid 44773793)
9. Bigalke H, Shoer LF (2000) Clostridial Neurotoxins. In: Aktories and Just (eds) Handbook of Experimental Pharmacology, vol 145 Bacterial Toxins pp 407-443
10. F Boato S Hendrix SC Hülsenbeck F Hofmann G Groe S Djalali L Klimaschewski M Auer I Just G Ahnert-Hilger M Höltje 2010 C3 peptide enhances recovery from spinal cord injury by improved regenerative growth of descending fiber tracts J Cell Sci 123 1652 1662 10.1242/jcs.066050 20406886
11. P Chardin P Boquet P Madaule MR Popoff EJ Rubin DM Gill 1989 The mammalian G protein rhoC is ADP-ribosylated by Clostridium botulinum exoenzyme C3 and affects actin microfilament in Vero cells EMBO J 8 1087 1092 1:CAS:528:DyaL1MXktF2lsLY%3D 2501082 (Pubitemid 19273274)
12. P Dergham B Ellezam C Essagian H Avedissian WD Lubell L McKerracher 2002 Rho signaling pathway targeted to promote spinal cord repair J Neurosci 22 6570 6577 1:CAS:528:DC%2BD38XlvFKnsbY%3D 12151536 (Pubitemid 35386413)
13. BJ Dickson 2001 Rho GTPases in growth cone guidance Curr Opin Neurobiol 11 103 110 1:CAS:528:DC%2BD3MXhslGltb0%3D 10.1016/S0959-4388(00)00180-X 11179879 (Pubitemid 32155956)
14. CI Dubreuil MJ Winton L McKerracher 2003 Rho activation patterns after spinal cord injury and the role of activated Rho in apoptosis in the central nervous system J Cell Biol 162 233 243 1:CAS:528:DC%2BD3sXlvVCgurs%3D 10.1083/jcb.200301080 12860969 (Pubitemid 36928837)
15. CI Dubrueil N Marklund K Deschamps TK McIntosh L McKerracher 2006 Activation of Rho after traumatic brain injury and seizure in rats Exp Neurol 198 361 369 10.1016/j.expneurol.2005.12.002
16. S Etienne-Manneville A Hall 2002 Rho GTPases in cell biology Nature 420 629 635 1:CAS:528:DC%2BD38XpsVSitbw%3D 10.1038/nature01148 12478284 (Pubitemid 36764489)
17. J Fahrer J Kuban K Heine G Rupps E Kaiser E Felder R Benz H Barth 2010 Selective and specific internalization of clostridial C3 ADP-ribosyltransferases into macrophages and monocytes Cell Microbiol 12 233 247 1:CAS:528: DC%2BC3cXhtFGlsb4%3D 10.1111/j.1462-5822.2009.01393.x 19840027
18. H Fujihara LA Walker MC Gong E Lemichez P Boquet AV Somlyo, et al. 1997 Inhibition of RhoA translocation and calcium sensitization by in vivo ADP-ribosylation with the chimeric toxin DC3B Mol Biol Cell 8 2437 2447 1:CAS:528:DyaK2sXotVWgu7g%3D 9398666 (Pubitemid 27528212)
19. H Genth R Gerhard A Maeda M Amano K Kaibuchi K Aktories, et al. 2003 Entrapment of Rho ADP-ribosylated by Clostridium botulinum C3 exoenzyme in the Rho-guanine nucleotide dissociation inhibitor-1 complex J Biol Chem 278 28523 28527 1:CAS:528:DC%2BD3sXlsl2ntL0%3D 10.1074/jbc.M301915200 12750364 (Pubitemid 36935755)
20. H Genth M Schmidt R Gerhard K Aktories I Just 2003 Activation of phospholipase D1 by ADP-ribosylated RhoA Biochem Biophys Res Commun 302 127 132 1:CAS:528:DC%2BD3sXht1Cqtbk%3D 10.1016/S0006-291X(03)00112-8 12593858 (Pubitemid 36268929)
21. EE Govek SE Newey AL Van 2005 The role of the Rho GTPases in neuronal development Genes Dev 19 1 49 1:CAS:528:DC%2BD2MXktVakuw%3D%3D 10.1101/gad.1256405 15630019 (Pubitemid 40095815)
22. A Hall G Lalli 2010 Rho and Ras GTPases in axon growth, guidance, and branching Cold Spring Harb Perspect Biol 2 a001818 10.1101/cshperspect.a001818 20182621
23. S Han AS Arvai SB Clancy JA Tainer 2001 Crystal structure and novel recognition motif of rho ADP-ribosylating C3 exoenzyme from Clostridium botulinum: structural insights for recognition specificity and catalysis J Mol Biol 305 95 107 1:CAS:528:DC%2BD3cXoslSmsrc%3D 10.1006/jmbi.2000.4292 11114250 (Pubitemid 32039748)
24. SJ Heasman AJ Ridley 2008 Mammalian Rho GTPases: new insights into their functions from in vivo studies Nat Rev Mol Cell Biol 9 690 701 1:CAS:528:DC%2BD1cXhtVWgu7jF 10.1038/nrm2476 18719708
25. A Hoffmann F Hofmann I Just S Lehnardt UK Hanisch W Brück H Kettenmann G Ahnert-Hilger M Höltje 2008 Inhibition of Rho-dependent pathways by Clostridium botulinum C3 protein induces a proinflammatory profile in microglia Glia 56 1162 1175 10.1002/glia.20687 18442097
26. M Höltje A Hoffmann F Hofmann C Mucke G Grosse N Van Rooijen H Kettenmann I Just G Ahnert-Hilger 2005 Role of Rho GTPase in astrocyte morphology and migratory response during in vitro wound healing J Neurochem 95 1237 1248 10.1111/j.1471-4159.2005.03443.x 16150054 (Pubitemid 41779250)
27. M Höltje F Hofmann R Lux RW Veh I Just G Ahnert-Hilger 2008 Glutamate uptake and release by astrocytes are enhanced by Clostridium botulinum C3 protein J Biol Chem 283 9289 9299 10.1074/jbc.M706499200 18234672
28. M Höltje S Djalali F Hofmann A Münster-Wandowski S Hendrix F Boato S Dreger G Groe C Henneberger R Grantyn I Just G Ahnert-Hilger 2009 A 29 amino acid fragment of Clostridium botulinum C3 protein enhances neuronal outgrowth, connectivity, and reinnervation FASEB J 23 1115 1126 10.1096/fj.08-116855 19047066
29. J Huelsenbeck S Dreger R Gerhard G Fritz I Just H Genth 2007 Up-regulation of the immediate early gene product RhoB by exoenzyme C3 from Clostridium limosum and toxin B from Clostridium difficile Biochemistry 46 4923 4931 1:CAS:528:DC%2BD2sXjs1SktLo%3D 10.1021/bi602465z 17397186 (Pubitemid 46651213)
30. S Inoue M Sugai Y Murooka S-Y Paik Y-M Hong H Ohgai H Suginaka 1991 Molecular cloning and sequencing of the epidermal cell differentiation inhibitor gene from Staphylococcus aureus Biochem Biophys Res Commun 174 459 464 1:CAS:528:DyaK3MXksVegsLk%3D 10.1016/0006-291X(91)91438-I 1993048
31. K Jalink EJ Van Corven T Hengeveld N Morii S Narumiya WH Moolenaar 1994 Inhibition of lysophosphatidate- and thrombin-induced neurite retraction and neuronal cell rounding by ADP ribosylation of the small GTP-binding protein Rho J Cell Biol 126 801 810 1:CAS:528:DyaK2cXltVGhtro%3D 10.1083/jcb.126.3.801 8045941 (Pubitemid 24241391)
32. I Just P Boquet 2000 Large clostridial cytotoxins as tools in cell biology Curr Top Microbiol Immunol 250 97 107 1:CAS:528:DC%2BD3cXlvFymtLg%3D 10981359 (Pubitemid 30463104)
33. I Just C Mohr G Schallehn L Menard JR Didsbury J Vandekerckhove, et al. 1992 Purification and characterization of an ADP-ribosyltransferase produced by Clostridium limosum J Biol Chem 267 10274 10280 1:CAS:528:DyaK38XktVeisbg%3D 1587816
34. I Just G Schallehn K Aktories 1992 ADP-ribosylation of small GTP-binding proteins by Bacillus cereus Biochem Biophys Res Commun 183 931 936 1:CAS:528:DyaK38XltVKqu70%3D 10.1016/S0006-291X(05)80279-7 1567406
35. I Just SC Huelsenbeck H Genth 2010 Clostridium Botulinum C3 Exoenzyme: Rho-inactivating tool in cell biology and a neurotrophic agent The Open Toxinology Journal 3 19 23 1:CAS:528:DC%2BC3cXktVals7o%3D 10.2174/ 1875414701003020019
36. DA Linseman FA Loucks 2008 Diverse roles of Rho family GTPases in neuronal development, survival, and death Front Biosci 13 657 676 1:CAS:528:DC%2BD1cXhs1Cht7s%3D 10.2741/2710 17981578 (Pubitemid 351599775)
37. S Lord-Fontaine F Yang Q Diep P Dergham S Munzer P Tremblay L McKerracher 2008 Local inhibition of Rho signaling by cell-permeable recombinant protein BA-210 prevents secondary damage and promotes functional recovery following acute spinal cord injury J Neurotrauma 25 1309 1322 10.1089/neu.2008.0613 19061375
38. DJG Mackay CD Nobes A Hall 1995 The Rho's progress: a potential role during neuritogenesis for the Rho family of GTPases Trends Neurosci 18 496 501 1:CAS:528:DyaK2MXptFalt7w%3D 10.1016/0166-2236(95)92773-J 8592759
39. L McKerracher H Higuchi 2006 Targeting Rho to stimulate repair after spinal cord injury J Neurotrauma 23 309 317 10.1089/neu.2006.23.309 16629618 (Pubitemid 43726312)
40. J Ménétrey G Flatau EA Stura J-B Charbonnier F Gas J-M Teulon, et al. 2002 NAD binding induces conformational changes in Rho ADP-ribosylating clostridium botulinum C3 exoenzyme J Biol Chem 277 30950 30957 10.1074/jbc.M201844200 12029083 (Pubitemid 34970797)
41. J Ménétrey G Flatau P Boquet A Ménez EA Stura 2008 Structural basis for the NAD-hydrolysis mechanism and the ARTT-loop plasticity of C3 exoenzymes Protein Sci 17 878 886 10.1110/ps.073398508 18369192 (Pubitemid 351629582)
42. F Mimura S Yamagishi N Arimura M Fujitani T Kubo K Kaibuchi K Yamashita 2006 Myelin-associated glycoprotein inhibits microtubule assembly by a Rho-kinase-dependent mechanism J Biol Chem 281 15970 15979 1:CAS:528: DC%2BD28Xlt1Ckur0%3D 10.1074/jbc.M510934200 16595691 (Pubitemid 43848490)
43. KN Nadif AL Van 2008 Rho-linked genes and neurological disorders Pflugers Arch 455 787 797 10.1007/s00424-007-0385-1 (Pubitemid 50003204)
44. AJ Ridley A Hall 1992 The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors Cell 70 389 399 1:CAS:528:DyaK38XlsVyisro%3D 10.1016/0092-8674(92)90163- 7 1643657
45. AJ Ridley A Hall 1994 Signal transduction pathways regulating Rho-mediated stress fibre formation: requirement for a tyrosine kinase EMBO J 13 2600 2610 1:CAS:528:DyaK2cXksl2hs7k%3D 7516876 (Pubitemid 24188393)
46. EJ Rubin DM Gill P Boquet MR Popoff 1988 Functional modification of a 21-Kilodalton G protein when ADP-ribosylated by exoenzyme C3 of Clostridium botulinum Mol Cell Biol 8 418 426 1:CAS:528:DyaL1cXhtVyks70%3D 3122025
47. A Schmandke A Schmandke SM Strittmatter 2007 ROCK and Rho: biochemistry and neuronal functions of Rho-associated protein kinases Neuroscientist 13 454 469 1:CAS:528:DC%2BD2sXhtFyju73P 10.1177/1073858407303611 17901255 (Pubitemid 47437930)
48. P Sehr G Joseph H Genth I Just E Pick K Aktories 1998 Glucosylation and ADP-ribosylation of rho proteins: effects on nucleotide binding, GTPase activity, and effector coupling Biochemistry 37 5296 5304 1:CAS:528: DyaK1cXisVylur8%3D 10.1021/bi972592c 9548761 (Pubitemid 28176531)
49. A Sekine M Fujiwara S Narumiya 1989 Asparagine residue in the rho gene product is the modification site for botulinum ADP-ribosyltransferase J Biol Chem 264 8602 8605 1:CAS:528:DyaL1MXktVehsrc%3D 2498316 (Pubitemid 19151574)
50. M Vogelsgesang A Pautsch K Aktories 2007 C3 exoenzymes, novel insights into structure and action of Rho-ADP-ribosylating toxins Naunyn Schmiedebergs Arch Pharmacol 374 347 360 1:CAS:528:DC%2BD2sXhsVersr0%3D 10.1007/s00210-006- 0113-y 17146673 (Pubitemid 46215285)
51. M Watabe-Uchida EE Govek L Van Aelst 2006 Regulators of Rho GTPases in neuronal development J Neurosci 26 10633 10635 1:CAS:528:DC%2BD28XhtFygu7nJ 10.1523/JNEUROSCI.4084-06.2006 17050702
52. K Wennerberg CJ Der 2004 Rho-family GTPases: it's not only Rac and Rho (and I like it) J Cell Sci 117 1301 1312 1:CAS:528:DC%2BD2cXjs1ygtbY%3D 10.1242/jcs.01118 15020670 (Pubitemid 38559808)
53. W Wiegers I Just H Müller A Hellwig P Traub K Aktories 1991 Alteration of the cytoskeleton of mammalian cells cultured in vitro by Clostridium botulinum C2 toxin and C3 ADP-ribosyltransferase Eur J Cell Biol 54 237 245 1:CAS:528:DyaK3MXks1KmtLw%3D 1908779
54. C Wilde GS Chhatwal G Schmalzing K Aktories I Just 2001 A novel C3-like ADP-ribosyltransferase from Staphylococcus aureus modifying RhoE and Rnd3 J Biol Chem 276 9537 9542 1:CAS:528:DC%2BD3MXisVCmtr0%3D 10.1074/jbc.M011035200 11124969
55. C Wilde M Vogelsang K Aktories 2003 Rho-specific Bacillus cereus ADP-ribosyltransferase C3cer cloning and characterization Biochemistry 42 9694 9702 1:CAS:528:DC%2BD3sXlslegtrc%3D 10.1021/bi034583b 12911311 (Pubitemid 36993142)
56. T Yamashita H Higuchi M Tohyama 2002 The p75 receptor transduces the signal from myelin-associated glycoprotein to Rho J Cell Biol 157 565 570 1:CAS:528:DC%2BD38XjslGlsL8%3D 10.1083/jcb.200202010 12011108 (Pubitemid 34839785)