Calpain-dependent cytoskeletal rearrangement exploited for anthrax toxin endocytosis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 42, 2013, Pages

  Jeong, Sun Young ^a   Martchenko, Mikhail ^a,b   Cohen, Stanley N ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KECK GRADUATE INSTITUTE   (United States)

Author keywords

Calpastatin; Lethal factor; MDL28170

Indexed keywords

ANTHRAX TOXIN; CALPAIN; CALPAIN 2; CALPASTATIN; CELL SURFACE RECEPTOR; CYSTEINE PROTEINASE; INTEGRIN; TALIN; TALIN 1; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ANIMAL CELL; ANTHRAX; ARTICLE; CELL ADHESION; CELL ISOLATION; CELL VIABILITY; CONTROLLED STUDY; CYTOSKELETON; ENDOCYTOSIS; LETHALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION;

CALPASTATIN; LETHAL FACTOR; MDL28170;

AMINO ACID SUBSTITUTION; ANIMALS; ANTIGENS, BACTERIAL; BACILLUS ANTHRACIS; BACTERIAL TOXINS; CALPAIN; CELL LINE; CYTOSKELETON; DOWN-REGULATION; ENDOCYTOSIS; FOCAL ADHESIONS; GENE EXPRESSION REGULATION; MICE; MUTATION, MISSENSE; PROTEIN TRANSPORT; RECEPTORS, PEPTIDE; TALIN;

EID: 84885776126     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1316852110     Document Type: Article

References (83)

1. Grove J, Marsh M (2011) The cell biology of receptor-mediated virus entry. J Cell Biol 195(7): 1071-1082.
2. Hartlova A, Cerveny L, Hubalek M, Krocova Z, Stulik J (2010) Membrane rafts: A potential gateway for bacterial entry into host cells. Microbiol Immunol 54(4): 237-245.
3. Mañes S, del Real G, Martínez-A C (2003) Pathogens: Raft hijackers. Nat Rev Immunol 3(7): 557-568.
4. Lin AE, Guttman JA (2010) Hijacking the endocytic machinery by microbial pathogens. Protoplasma 244(1-4): 75-90.
5. Gupta VR, et al. (2008) Sphingomyelin functions as a novel receptor for Helicobacter pylori VacA. PLoS Pathog 4(5):e1000073.
6. Kounnas MZ, et al. (1992) The alpha 2-macroglobulin receptor/low density lipoprotein receptor-related protein binds and internalizes Pseudomonas exotoxin A. J Biol Chem 267(18): 12420-12423.
7. Spooner RA, Lord JM (2012) How ricin and Shiga toxin reach the cytosol of target cells: Retrotranslocation from the endoplasmic reticulum. Curr Top Microbiol Immunol 357: 19-40.
8. Abrami L, Liu S, Cosson P, Leppla SH, van der Goot FG (2003) Anthrax toxin triggers endocytosis of its receptor via a lipid raft-mediated clathrin-dependent process. J Cell Biol 160(3): 321-328.
9. van der Goot G, Young JA (2009) Receptors of anthrax toxin and cell entry. Mol Aspects Med 30(6): 406-412.
10. Abrami L, Bischofberger M, Kunz B, Groux R, van der Goot FG (2010) Endocytosis of the anthrax toxin is mediated by clathrin, actin and unconventional adaptors. PLoS Pathog 6(3):e1000792.
11. Scobie HM, Rainey GJ, Bradley KA, Young JA (2003) Human capillary morphogenesis protein 2 functions as an anthrax toxin receptor. Proc Natl Acad Sci USA 100(9): 5170-5174.
12. Liu S, et al. (2009) Capillary morphogenesis protein-2 is the major receptor mediating lethality of anthrax toxin in vivo. Proc Natl Acad Sci USA 106(30): 12424-12429.
13. Bradley KA, Mogridge J, Mourez M, Collier RJ, Young JA (2001) Identification of the cellular receptor for anthrax toxin. Nature 414(6860): 225-229.
14. Wei W, Lu Q, Chaudry GJ, Leppla SH, Cohen SN (2006) The LDL receptor-related protein LRP6 mediates internalization and lethality of anthrax toxin. Cell 124(6): 1141-1154.
15. Lu Q, Wei W, Kowalski PE, Chang AC, Cohen SN (2004) EST-based genome-wide gene inactivation identifies ARAP3 as a host protein affecting cellular susceptibility to anthrax toxin. Proc Natl Acad Sci USA 101(49): 17246-17251.
16. Martchenko M, Jeong SY, Cohen SN (2010) Heterodimeric integrin complexes containing beta1-integrin promote internalization and lethality of anthrax toxin. Proc Natl Acad Sci USA 107(35): 15583-15588.
17. Lacy DB, Wigelsworth DJ, Scobie HM, Young JA, Collier RJ (2004) Crystal structure of the von Willebrand factor A domain of human capillary morphogenesis protein 2: An anthrax toxin receptor. Proc Natl Acad Sci USA 101(17): 6367-6372.
18. Muehlbauer SM, et al. (2007) Anthrax lethal toxin kills macrophages in a strainspecific manner by apoptosis or caspase-1-mediated necrosis. Cell Cycle 6(6): 758-766.
19. Reig N, et al. (2008) Maturation modulates caspase-1-independent responses of dendritic cells to Anthrax lethal toxin. Cell Microbiol 10(5): 1190-1207.
20. Moayeri M, Leppla SH (2009) Cellular and systemic effects of anthrax lethal toxin and edema toxin. Mol Aspects Med 30(6): 439-455.
21. Goll DE, Thompson VF, Li H, Wei W, Cong J (2003) The calpain system. Physiol Rev 83(3): 731-801.
22. Sorimachi H, Hata S, Ono Y (2010) Expanding members and roles of the calpain superfamily and their genetically modified animals. Exp Anim 59(5): 549-566.
23. Croall DE, Ersfeld K (2007) The calpains: Modular designs and functional diversity. Genome Biol 8(6): 218.
24. Lebart MC, Benyamin Y (2006) Calpain involvement in the remodeling of cytoskeletal anchorage complexes. FEBS J 273(15): 3415-3426.
25. Jánossy J, et al. (2004) Calpain as a multi-site regulator of cell cycle. Biochem Pharmacol 67(8): 1513-1521.
26. Perez-Cordon G, Nie W, Schmidt D, Tzipori S, Feng H (2011) Involvement of host calpain in the invasion of Cryptosporidium parvum. Microbes Infect 13(1): 103-107.
27. Bozym RA, Morosky SA, Kim KS, Cherry S, Coyne CB (2010) Release of intracellular calcium stores facilitates coxsackievirus entry into polarized endothelial cells. PLoS Pathog 6(10):e1001135.
28. Schmeck B, et al. (2004) Streptococcus pneumoniae-induced caspase 6-dependent apoptosis in lung epithelium. Infect Immun 72(9): 4940-4947.
29. Lee SY, Lee MS, Cherla RP, Tesh VL (2008) Shiga toxin 1 induces apoptosis through the endoplasmic reticulum stress response in human monocytic cells. Cell Microbiol 10(3): 770-780.
30. Müller A, et al. (1999) Neisserial porin (PorB) causes rapid calcium influx in target cells and induces apoptosis by the activation of cysteine proteases. EMBO J 18(2): 339-352.
31. Kennedy CL, Smith DJ, Lyras D, Chakravorty A, Rood JI (2009) Programmed cellular necrosis mediated by the pore-forming alpha-toxin from Clostridium septicum. PLoS Pathog 5(7):e1000516.
32. Franco SJ, et al. (2004) Calpain-mediated proteolysis of talin regulates adhesion dynamics. Nat Cell Biol 6(10): 977-983.
33. Lopes JP, Oliveira CR, Agostinho P (2010) Neurodegeneration in an Abeta-induced model of Alzheimer's disease: The role of Cdk5. Aging Cell 9(1): 64-77.
34. Arataki S, et al. (2005) Calpain inhibitors prevent neuronal cell death and ameliorate motor disturbances after compression-induced spinal cord injury in rats. J Neurotrauma 22(3): 398-406.
35. Wang CH, et al. (2004) Protective effect of MDL28170 against thioacetamide-induced acute liver failure in mice. J Biomed Sci 11(5): 571-578.
36. Chang AC, et al. (2006) Phenotype-based identification of host genes required for replication of African swine fever virus. J Virol 80(17): 8705-8717.
37. Piccone ME, et al. (2009) Identification of cellular genes affecting the infectivity of foot-and-mouth disease virus. J Virol 83(13): 6681-6688.
38. Mehdi S (1991) Cell-penetrating inhibitors of calpain. Trends Biochem Sci 16(4): 150-153.
39. Vitale G, et al. (1999) Anthrax lethal factor cleaves the N-terminus of MAPKKS and induces tyrosine/threonine phosphorylation of MAPKS in cultured macrophages. J Appl Microbiol 87(2): 288.
40. Liu S, Leppla SH (2003) Cell surface tumor endothelium marker 8 cytoplasmic tailindependent anthrax toxin binding, proteolytic processing, oligomer formation, and internalization. J Biol Chem 278(7): 5227-5234.
41. Deuquet J, Lausch E, Superti-Furga A, van der Goot FG (2012) The dark sides of capillary morphogenesis gene 2. EMBO J 31(1): 3-13.
42. Milne JC, Furlong D, Hanna PC, Wall JS, Collier RJ (1994) Anthrax protective antigen forms oligomers during intoxication of mammalian cells. J Biol Chem 269(32): 20607-20612.
43. Franco S, Perrin B, Huttenlocher A (2004) Isoform specific function of calpain 2 in regulating membrane protrusion. Exp Cell Res 299(1): 179-187.
44. Azam M, et al. (2001) Disruption of the mouse mu-calpain gene reveals an essential role in platelet function. Mol Cell Biol 21(6): 2213-2220.
45. Morford LA, et al. (2002) Calpain II colocalizes with detergent-insoluble rafts on human and Jurkat T-cells. Biochem Biophys Res Commun 295(2): 540-546.
46. Nuzzi PA, Senetar MA, Huttenlocher A (2007) Asymmetric localization of calpain 2 during neutrophil chemotaxis. Mol Biol Cell 18(3): 795-805.
47. Vassilieva EV, Gerner-Smidt K, Ivanov AI, Nusrat A (2008) Lipid rafts mediate internalization of beta1-integrin in migrating intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 295(5):G965-G976.
48. Franco SJ, Huttenlocher A (2005) Regulating cell migration: Calpains make the cut. J Cell Sci 118(Pt 17): 3829-3838.
49. Cortesio CL, Boateng LR, Piazza TM, Bennin DA, Huttenlocher A (2011) Calpainmediated proteolysis of paxillin negatively regulates focal adhesion dynamics and cell migration. J Biol Chem 286(12): 9998-10006.
50. Xu Y, et al. (2010) Filamin A regulates focal adhesion disassembly and suppresses breast cancer cell migration and invasion. J Exp Med 207(11): 2421-2437.
51. Nayal A, Webb DJ, Horwitz AF (2004) Talin: An emerging focal point of adhesion dynamics. Curr Opin Cell Biol 16(1): 94-98.
52. Goult BT, et al. (2013) RIAM and vinculin binding to talin are mutually exclusive and regulate adhesion assembly and turnover. J Biol Chem 288(12): 8238-8249.
53. Castanon I, et al. (2013) Anthrax toxin receptor 2a controls mitotic spindle positioning. Nat Cell Biol 15(1): 28-39.
54. Go MY, Chow EM, Mogridge J (2009) The cytoplasmic domain of anthrax toxin receptor 1 affects binding of the protective antigen. Infect Immun 77(1): 52-59.
55. Woronowicz K, et al. (2010) The platelet actin cytoskeleton associates with SNAREs and participates in alpha-granule secretion. Biochemistry 49(21): 4533-4542.
56. Brown S, Levinson W, Spudich JA (1976) Cytoskeletal elements of chick embryo fibroblasts revealed by detergent extraction. J Supramol Struct 5(2): 119-130.
57. Taylor MJ, Lampe M, Merrifield CJ (2012) A feedback loop between dynamin and actin recruitment during clathrin-mediated endocytosis. PLoS Biol 10(4):e1001302.
58. Boulant S, Kural C, Zeeh JC, Ubelmann F, Kirchhausen T (2011) Actin dynamics counteract membrane tension during clathrin-mediated endocytosis. Nat Cell Biol 13(9): 1124-1131.
59. Gu C, et al. (2010) Direct dynamin-actin interactions regulate the actin cytoskeleton. EMBO J 29(21): 3593-3606.
60. Bridgewater RE, Norman JC, Caswell PT (2012) Integrin trafficking at a glance. J Cell Sci 125(Pt 16): 3695-3701.
61. Mooren OL, Galletta BJ, Cooper JA (2012) Roles for actin assembly in endocytosis. Annu Rev Biochem 81: 661-686.
62. Coué M, Brenner SL, Spector I, Korn ED (1987) Inhibition of actin polymerization by latrunculin A. FEBS Lett 213(2): 316-318.
63. Moyen C, et al. (2004) Involvement of micro-calpain (CAPN 1) in muscle cell differentiation. Int J Biochem Cell Biol 36(4): 728-743.
64. Dean P, Mühlen S, Quitard S, Kenny B (2010) The bacterial effectors EspG and EspG2 induce a destructive calpain activity that is kept in check by the co-delivered Tir effector. Cell Microbiol 12(9): 1308-1321.
65. Young VB, Falkow S, Schoolnik GK (1992) The invasin protein of Yersinia enterocolitica: Internalization of invasin-bearing bacteria by eukaryotic cells is associated with reorganization of the cytoskeleton. J Cell Biol 116(1): 197-207.
66. Veiga E, Cossart P (2005) Listeria hijacks the clathrin-dependent endocytic machinery to invade mammalian cells. Nat Cell Biol 7(9): 894-900.
67. Humphreys D, Davidson A, Hume PJ, Koronakis V (2012) Salmonella virulence effector SopE and Host GEF ARNO cooperate to recruit and activate WAVE to trigger bacterial invasion. Cell Host Microbe 11(2): 129-139.
68. Sumitomo T, et al. (2011) Streptolysin S contributes to group A streptococcal translocation across an epithelial barrier. J Biol Chem 286(4): 2750-2761.
69. Bergounioux J, et al. (2012) Calpain activation by the Shigella flexneri effector VirA regulates key steps in the formation and life of the bacterium's epithelial niche. Cell Host Microbe 11(3): 240-252.
70. Briñas L, Vassilopoulos S, Bonne G, Guicheney P, Bitoun M (2013) Role of dynamin 2 in the disassembly of focal adhesions. J Mol Med (Berl) 91(7): 803-809.
71. Wehrle-Haller B (2012) Assembly and disassembly of cell matrix adhesions. Curr Opin Cell Biol 24(5): 569-581.
72. Alexander RA, et al. (2012) VEGF-induced endothelial cell migration requires urokinase receptor (uPAR)-dependent integrin redistribution. Cardiovasc Res 94(1): 125-135.
73. Du J, et al. (2011) Integrin activation and internalization on soft ECM as a mechanism of induction of stem cell differentiation by ECM elasticity. Proc Natl Acad Sci USA 108(23): 9466-9471.
74. Legate KR, Fässler R (2009) Mechanisms that regulate adaptor binding to betaintegrin cytoplasmic tails. J Cell Sci 122(Pt 2): 187-198.
75. Squires RC, Muehlbauer SM, Brojatsch J (2007) Proteasomes control caspase-1 activation in anthrax lethal toxin-mediated cell killing. J Biol Chem 282(47): 34260-34267.
76. Alileche A, Squires RC, Muehlbauer SM, Lisanti MP, Brojatsch J (2006) Mitochondrial impairment is a critical event in anthrax lethal toxin-induced cytolysis of murine macrophages. Cell Cycle 5(1): 100-106.
77. Liu S, Zhang Y, Hoover B, Leppla SH (2013) The receptors that mediate the direct lethality of anthrax toxin. Toxins (Basel) 5(1): 1-8.
78. Garlick KM, Mogridge J (2009) Direct interaction between anthrax toxin receptor 1 and the actin cytoskeleton. Biochemistry 48(44): 10577-10581.
79. Dal Molin F, et al. (2006) Cell entry and cAMP imaging of anthrax edema toxin. EMBO J 25(22): 5405-5413.
80. Arora N, Klimpel KR, Singh Y, Leppla SH (1992) Fusions of anthrax toxin lethal factor to the ADP-ribosylation domain of Pseudomonas exotoxin A are potent cytotoxins which are translocated to the cytosol of mammalian cells. J Biol Chem 267(22): 15542-15548.
81. Buki KG, Bauer PI, Kun E (1997) Isolation and identification of a proteinase from calf thymus that cleaves poly(ADP-ribose) polymerase and histone H1. Biochim Biophys Acta 1338(1): 100-106.
82. Chao WT, Kunz J (2009) Focal adhesion disassembly requires clathrin-dependent endocytosis of integrins. FEBS Lett 583(8): 1337-1343.
83. Ezratty EJ, Bertaux C, Marcantonio EE, Gundersen GG (2009) Clathrin mediates integrin endocytosis for focal adhesion disassembly in migrating cells. J Cell Biol 187(5): 733-747.