Identification of Cellular Calcium Binding Protein Calmodulin as a Regulator of Rotavirus A Infection during Comparative Proteomic Study

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Chattopadhyay, Shiladitya ^a   Basak, Trayambak ^b   Nayak, Mukti Kant ^c   Bhardwaj, Gourav ^b   Mukherjee, Anupam ^a   Bhowmick, Rahul ^a   Sengupta, Shantanu ^c   Chakrabarti, Oishee ^d   Chatterjee, Nabendu S ^a   Chawla Sarkar, Mamta ^a  

^a NATIONAL INSTITUTE OF CHOLERA AND ENTERIC DISEASES   (India)

^b CSIR INSTITUTE OF GENOMICS AND INTEGRATIVE BIOLOGY   (India)

^c UNIVERSITY OF CALCUTTA   (India)

^d SAHA INSTITUTE OF NUCLEAR PHYSICS   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CALMODULIN; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; N (6 AMINOHEXYL) 5 CHLORO 1 NAPHTHALENESULFONAMIDE; PROTEIN VP6;

ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEOMICS; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; ROTAVIRUS INFECTION; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS; VIRUS PATHOGENESIS; VIRUS STRAIN; WESTERN BLOTTING;

ANIMALS; ANTIGENS, VIRAL; CALCIUM; CALMODULIN; CAPSID PROTEINS; DYSENTERY; EGTAZIC ACID; HT29 CELLS; HUMANS; MICE; MICE, INBRED BALB C; PROTEIN BINDING; ROTAVIRUS; ROTAVIRUS INFECTIONS; TWO-DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS; VIRUS REPLICATION;

EID: 84874251161     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056655     Document Type: Article

References (66)

1. Centers for Disease Control and Prevention (CDC) (2008) Rotavirus surveillance-worldwide, 2001-2008. MMWR Morb Mortal Wkly Rep 5746: 1255-7.
2. Estes MK, Kapikian AZ (2007) Rotaviruses. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, et al., editors. Fields Virology. 5th ed. Philadelphia: Lippincott, Williams and Wilkins. 1917-1974.
3. Hoshino Y, Kapikian AZ, (2000) Rotavirus serotypes: classification and importance in epidemiology, immunity, and vaccine development. J Health Popul Nutr 18: 5-14.
4. Rollo EE, Kumar KP, Reich NC, Cohen J, Angel J, et al. (1999) The epithelial cell response to rotavirus infection. J Immunol 15: 4442-52.
5. Rossen JW, Bouma J, Raatgeep RH, Büller HA, Einerhand AW, (2004) Inhibition of cyclooxygenase activity reduces rotavirus infection at a postbinding step. J Virol 78: 9721-30.
6. Holloway G, Coulson BS, (2006) Rotavirus activates JNK and p38 signaling pathways in intestinal cells, leading to AP-1-driven transcriptional responses and enhanced virus replication. J Virol 80: 10624-33.
7. Dutta D, Bagchi P, Chatterjee A, Nayak MK, Mukherjee A, et al. (2009) The molecular chaperone heat shock protein-90 positively regulates rotavirus infection. Virology 391: 325-33.
8. Chaplin PJ, Entrican G, Gelder KI, Collins RA, (1996) Cloning and biologic acivities of a bovine interferon-alpha isolated from the epithelium of a rotavirus-infected calf. J Interferon Cytokine Res 16: 25-30.
9. Holloway G, Truong TT, Coulson BS, (2009) Rotavirus antagonizes cellular antiviral responses by inhibiting the nuclear accumulation of STAT1, STAT2, and NF-kappaB. J Virol 83: 4942-51.
10. Barro M, Patton JT, (2007) Rotavirus NSP1 inhibits expression of type I interferon by antagonizing the function of interferon regulatory factors IRF3, IRF5, and IRF7. J Virol 81: 4473-81.
11. Graff JW, Ettayebi K, Hardy ME, (2009) Rotavirus NSP1 inhibits NFkappaB activation by inducing proteasome-dependent degradation of beta-TrCP: a novel mechanism of IFN antagonism. PLoS Pathog 5: e1000280.
12. Cuadras MA, Feigelstock DA, Sungwhan A, Greenberg HB, (2002) Gene expression pattern in Caco-2 cells following rotavirus infection. J Virol 76: 4467-82.
13. Bagchi P, Nandi S, Chattopadhyay S, Bhowmick R, Halder UC, et al. (2012) Identification of common human host genes involved in pathogenesis of different rotavirus strains: An attempt to recognize probable antiviral targets. Virus Res 169: 144-53.
14. Aimin Xu, Bellamy AR, Taylor JA, (1998) BiP (GRP78) and Endoplasmin (GRP94) Are Induced following Rotavirus Infection and Bind Transiently to an Endoplasmic Reticulum-Localized Virion Component. J Virol 72: 9865-72.
15. Xu A, Bellamy AR, Taylor JA, (1999) Expression of translationally controlled tumour protein is regulated by calcium at both the transcriptional and post-transcriptional level. Biochem J 342 Pt 3: 683-9.
16. Zambrano JL, Ettayebi K, Maaty WS, Faunce NR, Bothner B, et al. (2011) Rotavirus infection activates the UPR but modulates its activity. Virol J 20: 348-359.
17. Bagchi P, Dutta D, Chattopadhyay S, Mukherjee A, Halder UC, et al. (2010) Rotavirus nonstructural protein 1 suppresses virus-induced cellular apoptosis to facilitate viral growth by activating the cell survival pathways during early stages of infection. J Virol 84: 6834-45.
18. Bradford MM, (1976) Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
19. Smith EM, Estes MK, Graham DY, Gerba PC, (1979) A plaque assay for the simian rotavirus SA11. J Gen Virol 43: 513-19.
20. Albrecht D, Guthke R, Brakhage AA, Kniemeyer O, (2010) Integrative analysis of the heat shock response in Aspergillus fumigatus. BMC Genomics 15: 11-32.
21. Ponnudurai RP, Basak T, Ahmad S, Bhardwaj G, Chauhan RK, et al. (2012) Proteomic analysis of zebrafish (Danio rerio) embryos exposed to cyclosporine A. J Proteomics. 75: 1004-17.
22. Yadav AK, Bhardwaj G, Basak T, Kumar D, Ahmad S, et al. (2011) Systematic analysis of eluted fraction of plasma post immunoaffinity depletion: implications in biomarker discovery. PLoS One 6: e24442.
23. Chawla-Sarkar M, Bae SI, Reu FJ, Jacobs BS, Lindner DJ, et al. (2004) Downregulation of Bcl-2, FLIP or IAPs (XIAP and survivin) by siRNAs sensitizes resistant melanoma cells to Apo2L/TRAIL-induced apoptosis. Cell Death Differ 11: 915-23.
24. Schmittgen TD, Livak KJ, (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-8.
25. Murthy AK, Sharma J, Coalson JJ, Zhong G, Arulanandam BP, (2004) Chlamydia trachomatis pulmonary infection induces greater inflammatory pathology in immunoglobulin A deficient mice. Cell Immunol 230: 56-64.
26. Pammit MA, Budhavarapu VN, Raulie EK, Klose KE, Teale JM, et al. (2004) Intranasal interleukin-12 treatment promotes antimicrobial clearance and survival in pulmonary Francisella tularensis subsp. novicida infection. Antimicrob Agents Chemother 48: 4513-19.
27. Formal Sb, Kundel D, Schneider H, Kunev N, Sprinz H, (1961) Studies with Vibrio cholerae in the ligated loop of the rabbit intestine. Br J Exp Pathol 42: 504-10.
28. Takehiro S, Sakaguchi S, Nakamura I, (1988) Positive Reaction in Mouse Ligated Intestinal Loop Assay with Nonenterotoxigenic and Nonhemolytic Strains of Staphylococcus aureus. J Clin Microbiol 26: 600-01.
29. Dutta D, Chattopadhyay S, Bagchi P, Halder UC, Nandi S, et al. (2011) Active participation of cellular chaperone Hsp90 in regulating the function of rotavirus nonstructural protein 3 (NSP3). J Biol Chem 286: 20065-77.
30. Bhowmick R, Halder UC, Chattopadhyay S, Chanda S, Nandi S, et al. (2012) Rotaviral Enterotoxin Nonstructural Protein 4 Targets Mitochondria for Activation of Apoptosis during Infection. J Biol Chem 287: 35004-20.
31. Adebiyi A, Narayanan D, Jaggar JH, (2011) Caveolin-1 assembles type 1 inositol 1,4,5-trisphosphate receptors and canonical transient receptor potential 3 channels into a functional signaling complex in arterial smooth muscle cells. J Biol Chem 286: 4341-8.
32. Yap KL, Kim J, Truong K, Sherman M, Yuan T, Ikura M, (2000) Calmodulin Target Database. J Struct Funct Genomics 1: 8-14.
33. Brunet JP, Cotte-Laffitte J, Linxe C, Quero AM, Géniteau-Legendre M, et al. (2000) Rotavirus infection induces an increase in intracellular calcium concentration in human intestinal epithelial cells: role in microvillar actin alteration. J Virol 74: 2323-32.
34. Pérez JF, Chemello ME, Liprandi F, Ruiz MC, Michelangeli F, (1998) Oncosis in MA104 cells is induced by rotavirus infection through an increase in intracellular Ca2+ concentration. Virology 252: 17-27.
35. Buttke TM, McCubrey JA, Owen TC, (1993) Use of an aqueous soluble tetrazolium/formazan assay to measure viability and proliferation of lymphokine-dependent cell lines. J Immunol Methods 157: 233-240.
36. Dhillon NK, Sharma S, Khuller GK, (2003) Influence of W-7, a calmodulin antagonist on phospholipid biosynthesis in Candida albicans. Lett Appl Microbiol 36: 382-6.
37. Sen A, Feng N, Ettayebi K, Hardy ME, Greenberg HB, (2009) IRF3 inhibition by rotavirus NSP1 is host cell and virus strain dependent but independent of NSP1 proteasomal degradation. J Virol 83: 10322-35.
38. Carpio M, Bellamy JE, Babiuk LA, (1981) Comparative virulence of different bovine rotavirus isolates. Can J Comp Med 45: 38-42.
39. Chin D, Means AR, (2000) Calmodulin: a prototypical calcium sensor. Trends Cell Biol 10: 322-8.
40. Kahl CR, Means AR, (2003) Regulation of cell cycle progression by calcium/calmodulin dependent pathways. Endocr Rev 24: 719-36.
41. Choi J, Husain M, (2006) Calmodulin-mediated cell cycle regulation: new mechanisms for old observations. Cell Cycle 5: 2183-6.
42. Yamniuk AP, Vogel HJ, (2004) Calmodulin's flexibility allows for promiscuity in its interactions with target proteins and peptides. Mol Biotechnol 27: 33-57.
43. Jurado LA, Chockalingam PS, Jarrett HW, (1999) Apocalmodulin. Physiol Rev 79: 661-82.
44. Rhoads AR, Friedberg F, (1997) Sequence motifs for calmodulin recognition. FASEB J 11: 331-40.
45. Ikura M, Clore GM, Gronenborn AM, Zhu G, Klee CB, et al. (1992) Solution structure of a calmodulin-target peptide complex by multidimensional NMR Science. 256: 632-38.
46. Meador WE, Means AR, Quiocho FA, (1992) Target enzyme recognition by calmodulin: 2.4 A structure of a calmodulin-peptide complex. Science 257: 1251-55.
47. Zhang M, Yuan T, (1998) Molecular mechanisms of calmodulin's functional versatility. Biochem Cell Biol 76: 313-23.
48. Joyal JL, Burks DJ, Pons S, Matter WF, Vlahos CJ, et al. (1997) Calmodulin activates phosphatidylinositol 3-kinase. J Biol Chem 272: 28183-6.
49. Rasmussen CD, Means AR, (1992) Increased calmodulin affects cell morphology and mRNA levels of cytoskeletal protein genes. Cell Motil Cytoskeleton 21: 45-57.
50. Saha A, Halder S, Upadhyay SK, Lu J, Kumar P, et al. (2011) Epstein-Barr virus nuclear antigen 3C facilitates G1-S transition by stabilizing and enhancing the function of cyclin D1. PLoS Pathog 7: e1001275.
51. Wang J, Reuschel EL, Shackelford JM, Jeang L, Shivers DK, et al. (2011) HIV-1 Vif promotes the G1- to S-phase cell-cycle transition. Blood 117: 1260-9.
52. Crawford SE, Hyser JM, Utama B, Estes MK (2012) Autophagy hijacked through viroporin activated calcium/calmodulin-dependent kinase kinase-β signaling is required for rotavirus replication. Proc Natl Acad Sci U S A. In press.
53. Mathieu M, Petitpas I, Navaza J, Lepault J, Kohli E, et al. (2001) Atomic structure of the major capsid protein of rotavirus: implications for the architecture of the virion. The EMBO Journal 20: 1485-97.
54. Tsunemitsu H, Kamiyama M, Kawashima K, Katsuda K, Kohmoto M, et al. (2005) Molecular characterization of the major capsid protein VP6 of bovine group B rotavirus and its use in seroepidemiology. J Gen Virol 86: 2569-75.
55. Jain V, Das BK, Bhan MK, Glass RI, Gentsch JR, (2001) Indian Strain Surveillance Collaborating Laboratories. Great diversity of group A rotavirus strains and high prevalence of mixed rotavirus infections in India. J Clin Microbiol 39: 3524-9.
56. Kalica AR, Greenberg HB, Wyatt RG, Flores J, Serreno MM, et al. (1981) Genes of human (strain Wa) and bovine (strain UK) rotaviruses that code for neutralization and subgroup antigens. Virology 112: 385-90.
57. Kapikian AZ, Cline WL, Greenberg HB, Wyatt RG, Kalica AR, et al. (1981) Antigenic characterization of human and animal rotaviruses by immune adherence hemagglutination assay (IAHA): evidence for distinctness of IAHA and neutralization antigens. Infect Immun 33: 415-25.
58. Banos DM, Lopez S, Arias CF, Esquivel FR, (1997) Identification of a T-Helper Cell Epitope on the Rotavirus VP6 Protein. Journal of Virology 71: 419-426.
59. Parez N, Garbarg-Chenon A, Fourgeux C, Le Deist F, Servant-Delmas A, et al. (2004) The VP6 Protein of Rotavirus Interacts with a Large Fraction of Human Naive B Cells via Surface Immunoglobulins. Journal of Virology 78: 12489-12496.
60. Franco MA, Lefevre P, Willems P, Tosser G, Lintermanns P, et al. (1994) Identification of cytotoxic T cell epitopes on the VP3 and VP6 rotavirus proteins. Journal of General Virology 75: 589-96.
61. McNeal MM, Stone SC, Basu M, Clements JD, Choi AH, et al. (2007) IFN-gamma is the only anti-rotavirus cytokine found after in vitro stimulation of memory CD4+ T cells from mice immunized with a chimeric VP6 protein. Viral Immunol 20: 571-84.
62. Garaicoechea L, Olichon A, Marcoppido G, Wigdorovitz A, Mozgovoj M, et al. (2008) Llama-Derived Single-Chain Antibody Fragments Directed to Rotavirus VP6 Protein Possess Broad Neutralizing Activity In Vitro and Confer Protection against Diarrhea in Mice. Journal of Virology 82: 9753-9764.
63. Ginn DI, Ward RL, Hamparian VV, Hughes JH, (1992) Inhibition of rotavirus in vitro transcription by optimal concentrations of monoclonal antibodies specific for rotavirus VP6. Journal of General Virology 73: 3017-3022.
64. Campagna M, Marcos-Villar L, Arnoldi F, de la Cruz-Herrera CF, Gallego P, et al. (2012) Rotavirus Viroplasm Proteins Interact with the Cellular SUMOylation System: Implications for Viroplasm-Like Structures Formation. J Virol In press.
65. Brunet JP, Jourdan N, Cotte-Laffitte J, Linxe C, Géniteau-Legendre M, et al. (2000) Rotavirus infection induces cytoskeleton disorganization in human intestinal epithelial cells: implication of an increase in intracellular calcium concentration. J Virol 74: 10801-6.
66. Nishikawa M, Tanaka T, Hidaka H, (1980) Ca2+-calmodulin-dependent phosphorylation and platelet secretion. Nature 287: 863-5.