Release of intracellular calcium stores facilitates coxsackievirus entry into polarized endothelial cells

PLoS Pathogens

Volumn 6, Issue 10, 2010, Pages

  Bozym, Rebecca A ^a   Morosky, Stefanie A ^a   Kim, Kwang S ^b   Cherry, Sara ^c   Coyne, Carolyn B ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; CALPAIN 2; CALPASTATIN; CALPEPTIN; DECAY ACCELERATING FACTOR; DIDEOXYADNESOINE; DYNASORE; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; GENISTEIN; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; PHOSPHOLIPASE C; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN BLOOD VESSEL; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL MIGRATION; CELL POLARITY; CONTROLLED STUDY; COXSACKIE VIRUS B; COXSACKIE VIRUS INFECTION; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; HOST CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; MICROVASCULATURE; MOUSE; NONHUMAN; VIRUS ATTACHMENT; VIRUS ENTRY; VIRUS PARTICLE;

CALCIUM; CALCIUM SIGNALING; CALPAIN; CELL POLARITY; CELLS, CULTURED; COXSACKIEVIRUS INFECTIONS; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; ENTEROVIRUS; EPITHELIUM; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; INTRACELLULAR SPACE; PHOSPHOLIPASE C GAMMA; VIRUS INTERNALIZATION;

COXSACKIEVIRUS;

EID: 78449239909     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001135     Document Type: Article

References (56)

1. Morens DM, Pallansch MA (1995) Human Enterovirus Infections; Rotbart HA, editor. Washington, D.C.: American Society for Microbiology.
2. Coyne CB, Bergelson JM (2006) Virus-induced Abl and Fyn kinase signals permit coxsackievirus entry through epithelial tight junctions. Cell 124: 119-131.
3. Coyne CB, Shen L, Turner JR, Bergelson JM (2007) Coxsackievirus entry across epithelial tight junctions requires occludin and the small GTPases Rab34 and Rab5. Cell Host Microbe 2: 181-192.
4. Bergelson JM, Cunningham JA, Droguett G, Kurt-Jones EA, Krithivas A, et al. (1997) Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5, Science 275: 1320-1323.
5. Shieh JT, Bergelson JM (2002) Interaction with decay-accelerating factor facilitates coxsackievirus B infection of polarized epithelial cells. J Virol 76: 9474-9480.
6. Bergelson JM, Mohanty JG, Crowell RL, St John NF, Lublin DM, et al. (1995) Coxsackievirus B3 adapted to growth in RD cells binds to decay-accelerating factor (CD55). J Virol 69: 1903-1906.
7. Nicholson-Weller A, Wang CE (1994) Structure and function of decay accelerating factor CD55. J Lab Clin Med 123: 485-491.
8. Shafren DR, Bates RC, Agrez MV, Herd RL, Burns GF, et al. (1995) Coxsackieviruses B1, B3, and B5 use decay accelerating factor as a receptor for cell attachment. J Virol 69: 3873-3877.
9. Reagan KJ, Goldberg B, Crowell RL (1984) Altered receptor specificity of coxsackievirus B3 after growth in rhabdomyosarcoma cells. J Virol 49: 635-640.
10. Legler DF, Doucey MA, Schneider P, Chapatte L, Bender FC, et al. (2005) Differential insertion of GPI-anchored GFPs into lipid rafts of live cells. FASEB J 19: 73-75.
11. Rosenberger CM, Brumell JH, Finlay BB (2000) Microbial pathogenesis: lipid rafts as pathogen portals. Curr Biol 10: R823-825.
12. Parton RG, Richards AA (2003) Lipid rafts and caveolae as portals for endocytosis: new insights and common mechanisms. Traffic 4: 724-738.
13. Suzuki KG, Fujiwara TK, Edidin M, Kusumi A (2007) Dynamic recruitment of phospholipase C gamma at transiently immobilized GPI-anchored receptor clusters induces IP3-Ca2+ signaling: single-molecule tracking study 2. J Cell Biol 177: 731-742.
14. Kimberley FC, Sivasankar B, Paul Morgan B (2007) Alternative roles for CD59. Mol Immunol 44: 73-81.
15. Peiffer I, Servin AL, Bernet-Camard MF (1998) Piracy of decay-accelerating factor (CD55) signal transduction by the diffusely adhering strain Escherichia coli C1845 promotes cytoskeletal F-actin rearrangements in cultured human intestinal INT407 cells. Infect Immun 66: 4036-4042.
16. Shibuya K, Abe T, Fujita T (1992) Decay-accelerating factor functions as a signal transducing molecule for human monocytes. J Immunol 149: 1758-1762.
17. Zhou Y, Frey TK, Yang JJ (2009) Viral calciomics: interplays between Ca2+ and virus. Cell Calcium 46: 1-17.
18. Coyne CB, Kim KS, Bergelson JM (2007) Poliovirus entry into human brain microvascular cells requires receptor-induced activation of SHP-2. EMBO J 26: 4016-4028.
19. Sieczkarski SB, Whittaker GR (2002) Dissecting virus entry via endocytosis. J Gen Virol 83: 1535-1545.
20. Macia E, Ehrlich M, Massol R, Boucrot E, Brunner C, et al. (2006) Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell 10: 839-850.
21. Damke H, Baba T, Warnock DE, Schmid SL (1994) Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol 127: 915-934.
22. van Kuppeveld FJ, Hoenderop JG, Smeets RL, Willems PH, Dijkman HB, et al. (1997) Coxsackievirus protein 2B modifies endoplasmic reticulum membrane and plasma membrane permeability and facilitates virus release. EMBO J 16: 3519-3532.
23. Kelly JJ, Moore TM, Babal P, Diwan AH, Stevens T, et al. (1998) Pulmonary microvascular and macrovascular endothelial cells: differential regulation of Ca2+ and permeability. Am J Physiol 274: L810-819.
24. Blacklow NR, Rose FB, Whalen RA (1975) Organ culture of human aorta: prolonged survival with support of viral replication. J Infect Dis 131: 575-578.
25. Burch GE, Harb JM, Hiramoto Y (1974) Coxsackie viral infection of the aorta of man. South Med J 67: 166-169.
26. Foskett JK, White C, Cheung KH, Mak DO (2007) Inositol trisphosphate receptor Ca2+ release channels. Physiol Rev 87: 593-658.
27. Irurzun A, Arroyo J, Alvarez A, Carrasco L (1995) Enhanced intracellular calcium concentration during poliovirus infection. J Virol 69: 5142-5146.
28. Jayaraman T, Ondrias K, Ondriasova E, Marks AR (1996) Regulation of the inositol 1,4,5-trisphosphate receptor by tyrosine phosphorylation. Science 272: 1492-1494.
29. Tovey SC, Dedos SG, Taylor EJ, Church JE, Taylor CW (2008) Selective coupling of type 6 adenylyl cyclase with type 2 IP3 receptors mediates direct sensitization of IP3 receptors by cAMP. J Cell Biol 183: 297-311.
30. Mountian I, Manolopoulos VG, De Smedt H, Parys JB, Missiaen L, et al. (1999) Expression patterns of sarco/endoplasmic reticulum Ca(2+)-ATPase and inositol 1,4,5-trisphosphate receptor isoforms in vascular endothelial cells. Cell Calcium 25: 371-380.
31. Grayson TH, Haddock RE, Murray TP, Wojcikiewicz RJ, Hill CE (2004) Inositol 1,4,5-trisphosphate receptor subtypes are differentially distributed between smooth muscle and endothelial layers of rat arteries. Cell Calcium 36: 447-458.
32. Cui J, Matkovich SJ, deSouza N, Li S, Rosemblit N, et al. (2004) Regulation of the type 1 inositol 1,4,5-trisphosphate receptor by phosphorylation at tyrosine 353. J Biol Chem 279: 16311-16316.
33. Goll DE, Thompson VF, Li H, Wei W, Cong J (2003) The calpain system. Physiol Rev 83: 731-801.
34. Hayashi M, Saito Y, Kawashima S (1992) Calpain activation is essential for membrane fusion of erythrocytes in the presence of exogenous Ca2+. Biochem Biophys Res Commun 182: 939-946.
35. Sato K, Saito Y, Kawashima S (1995) Identification and characterization of membrane-bound calpains in clathrin-coated vesicles from bovine brain. Eur J Biochem 230: 25-31.
36. Aldabe R, Irurzun A, Carrasco L (1997) Poliovirus protein 2BC increases cytosolic free calcium concentrations. J Virol 71: 6214-6217.
37. Chami M, Oules B, Paterlini-Brechot P (2006) Cytobiological consequences of calcium-signaling alterations induced by human viral proteins. Biochim Biophys Acta 1763: 1344-1362.
38. de Jong AS, de Mattia F, Van Dommelen MM, Lanke K, Melchers WJ, et al. (2008) Functional analysis of picornavirus 2B proteins: effects on calcium homeostasis and intracellular protein trafficking. J Virol 82: 3782-3790.
39. de Jong AS, Visch HJ, de Mattia F, van Dommelen MM, Swarts HG, et al. (2006) The coxsackievirus 2B protein increases efflux of ions from the endoplasmic reticulum and Golgi, thereby inhibiting protein trafficking through the Golgi. J Biol Chem 281: 14144-14150.
40. Ruiz MC, Cohen J, Michelangeli F (2000) Role of Ca2+in the replication and pathogenesis of rotavirus and other viral infections. Cell Calcium 28: 137-149.
41. van Kuppeveld FJ, de Jong AS, Melchers WJ, Willems PH (2005) Enterovirus protein 2B po(u)res out the calcium: a viral strategy to survive? Trends Microbiol 13: 41-44.
42. Cheshenko N, Del Rosario B, Woda C, Marcellino D, Satlin LM, et al. (2003) Herpes simplex virus triggers activation of calcium-signaling pathways. J Cell Biol 163: 283-293.
43. Cheshenko N, Liu W, Satlin LM, Herold BC (2007) Multiple receptor interactions trigger release of membrane and intracellular calcium stores critical for herpes simplex virus entry. Mol Biol Cell 18: 3119-3130.
44. Schelhaas M, Malmstrom J, Pelkmans L, Haugstetter J, Ellgaard L, et al. (2007) Simian Virus 40 depends on ER protein folding and quality control factors for entry into host cells. Cell 131: 516-529.
45. Melford SK, Turner M, Briddon SJ, Tybulewicz VL, Watson SP (1997) Syk and Fyn are required by mouse megakaryocytes for the rise in intracellular calcium induced by a collagen-related peptide. J Biol Chem 272: 27539-27542.
46. Dhar A, Shukla SD (1994) Electrotransjection of pp60v-src monoclonal antibody inhibits activation of phospholipase C in platelets. A new mechanism for plateletactivating factor responses. J Biol Chem 269: 9123-9127.
47. Marrero MB, Schieffer B, Paxton WG, Schieffer E, Bernstein KE (1995) Electroporation of pp60c-src antibodies inhibits the angiotensin II activation of phospholipase C-gamma 1 in rat aortic smooth muscle cells. J Biol Chem 270: 15734-15738.
48. Sverdlov M, Shajahan AN, Minshall RD (2007) Tyrosine phosphorylationdependence of caveolae-mediated endocytosis. J Cell Mol Med 11: 1239-1250.
49. Donaldson JG, Porat-Shliom N, Cohen LA (2009) Clathrin-independent endocytosis: a unique platform for cell signaling and PM remodeling. Cell Signal 21: 1-6.
50. Sundivakkam PC, Kwiatek AM, Sharma TT, Minshall RD, Malik AB, et al. (2009) Caveolin-1 scaffold domain interacts with TRPC1 and IP3R3 to regulate Ca2+ store release-induced Ca2+ entry in endothelial cells. Am J Physiol Cell Physiol 296: C403-413.
51. Murata T, Lin MI, Stan RV, Bauer PM, Yu J, et al. (2007) Genetic evidence supporting caveolae microdomain regulation of calcium entry in endothelial cells. J Biol Chem 282: 16631-16643.
52. Teranishi F, Liu ZQ, Kunimatsu M, Imai K, Takeyama H, et al. (2003) Calpain is involved in the HIV replication from the latently infected OM10.1 cells. Biochem Biophys Res Commun 303: 940-946.
53. Kalamvoki M, Mavromara P (2004) Calcium-dependent calpain proteases are implicated in processing of the hepatitis C virus NS5A protein. J Virol 78: 11865-11878.
54. Upla P, Marjomaki V, Nissinen L, Nylund C, Waris M, et al. (2008) Calpain 1 and 2 are required for RNA replication of echovirus 1. J Virol 82: 1581-1590.
55. Nakamura M, Mori M, Nakazawa S, Tange T, Hayashi M, et al. (1992) Replacement of m-calpain by mu-calpain during maturation of megakaryocytes and possible involvement in platelet formation. Thromb Res 66: 757-764.
56. Stins MF, Badger J, Kim KS (2001) Bacterial invasion and transcytosis in transfected human brain microvascular endothelial cells. Microb Pathog 30: 19-28.