Identification of prohibitin as a Chikungunya virus receptor protein

Journal of Medical Virology

Volumn 84, Issue 11, 2012, Pages 1757-1770

  Wintachai, Phitchayapak ^a   Wikan, Nitwara ^a   Kuadkitkan, Atichat ^a   Jaimipuk, Thitigun ^a   Ubol, Sukathida ^a   Pulmanausahakul, Rojjanaporn ^a   Auewarakul, Prasert ^a,b   Kasinrerk, Watchara ^c   Weng, Wen Yu ^a   Panyasrivanit, Mingkwan ^a   Paemanee, Atchara ^d   Kittisenachai, Suthathip ^d   Roytrakul, Sittiruk ^d   Smith, Duncan R ^a  

^a MAHIDOL UNIVERSITY   (Thailand)

^b MAHIDOL UNIVERSITY   (Thailand)

^c CHIANG MAI UNIVERSITY   (Thailand)

^d NATIONAL SCIENCE AND TECHNOLOGY DEVELOPMENT AGENCY   (Thailand)

Author keywords

Alphavirus; Arbovirus; Microglia, receptor

Indexed keywords

BINDING PROTEIN; GREEN FLUORESCENT PROTEIN; HEAT SHOCK PROTEIN 60; MEMBRANE PROTEIN; MESSENGER RNA; MONOCLONAL ANTIBODY; PHOSPHOGLYCERATE MUTASE; POLYCLONAL ANTIBODY; PROHIBITIN; RECEPTOR PROTEIN; SMALL INTERFERING RNA; VIRUS RECEPTOR; VIRUS RNA;

ALPHA VIRUS; ANIMAL CELL; ANTIBODY TITER; ARBOVIRUS; ARTICLE; ASSAY; CELL MEMBRANE; CELL TYPE; CHIKUNGUNYA; CHIKUNGUNYA ALPHAVIRUS; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INTERNALIZATION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MICROGLIA; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TARGET CELL; VIRUS CELL INTERACTION; VIRUS INFECTION; VIRUS INHIBITION; VIRUS OVERLAY PROTEIN BINDING ASSAY; WESTERN BLOTTING;

ANIMALS; CELL LINE; CHIKUNGUNYA VIRUS; GENE SILENCING; HUMANS; IMMUNOPRECIPITATION; MICROGLIA; NEUROGLIA; RECEPTORS, VIRUS; REPRESSOR PROTEINS; VIRUS ATTACHMENT;

ALPHAVIRUS; ARBOVIRUS; CHIKUNGUNYA VIRUS;

EID: 84866485831     PISSN: 01466615     EISSN: 10969071     Source Type: Journal    
DOI: 10.1002/jmv.23403     Document Type: Article

References (73)

1. Abere B, Wikan N, Ubol S, Auewarakul P, Paemanee A, Kittisenachai S, Roytrakul S, Smith DR. 2012. Proteomic analysis of chikungunya virus infected microgial cells. PLoS ONE 7:e34800.
2. Acosta EG, Castilla V, Damonte EB. 2008. Functional entry of dengue virus into Aedes albopictus mosquito cells is dependent on clathrin-mediated endocytosis. J Gen Virol 89:474-484.
3. Arankalle VA, Shrivastava S, Cherian S, Gunjikar RS, Walimbe AM, Jadhav SM, Sudeep AB, Mishra AC. 2007. Genetic divergence of Chikungunya viruses in India (1963-2006) with special reference to the 2005-2006 explosive epidemic. J Gen Virol 88:1967-1976.
4. Artal-Sanz M, Tsang WY, Willems EM, Grivell LA, Lemire BD, van der Spek H, Nijtmans LG. 2003. The mitochondrial prohibitin complex is essential for embryonic viability and germline function in Caenorhabditis elegans. J Biol Chem 278:32091-32099.
5. Beesoon S, Funkhouser E, Kotea N, Spielman A, Robich RM. 2008. Chikungunya fever, Mauritius, 2006. Emerg Infect Dis 14:337-338.
6. Berger KH, Yaffe MP. 1998. Prohibitin family members interact genetically with mitochondrial inheritance components in Saccharomyces cerevisiae. Mol Cell Biol 18:4043-4052.
7. Bernard E, Solignat M, Gay B, Chazal N, Higgs S, Devaux C, Briant L. 2010. Endocytosis of chikungunya virus into mammalian cells: Role of clathrin and early endosomal compartments. PLoS ONE 5:e11479.
8. Borgherini G, Poubeau P, Staikowsky F, Lory M, Le Moullec N, Becquart JP, Wengling C, Michault A, Paganin F. 2007. Outbreak of chikungunya on Reunion Island: Early clinical and laboratory features in 157 adult patients. Clin Infect Dis 44:1401-1407.
9. Bradford M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
10. Brehin AC, Rubrecht L, Navarro-Sanchez ME, Marechal V, Frenkiel MP, Lapalud P, Laune D, Sall AA, Despres P. 2008. Production and characterization of mouse monoclonal antibodies reactive to Chikungunya envelope E2 glycoprotein. Virology 371:185-195.
11. Cabrera-Hernandez A, Thepparit C, Suksanpaisan L, Smith DR. 2007. Dengue virus entry into liver (HepG2) cells is independent of hsp90 and hsp70. J Med Virol 79:386-392.
12. Cappello F, Conway de Macario E, Marasa L, Zummo G, Macario AJ. 2008. Hsp60 expression, new locations, functions and perspectives for cancer diagnosis and therapy. Cancer Biol Ther 7:801-809.
13. Das T, Jaffar-Bandjee MC, Hoarau JJ, Krejbich Trotot P, Denizot M, Lee-Pat-Yuen G, Sahoo R, Guiraud P, Ramful D, Robin S, Alessandri JL, Gauzere BA, Gasque P. 2010. Chikungunya fever: CNS infection and pathologies of a re-emerging arbovirus. Prog Neurobiol 91:121-129.
14. Davis-Smyth T, Duncan RC, Zheng T, Michelotti G, Levens D. 1996. The far upstream element-binding proteins comprise an ancient family of single-strand DNA-binding transactivators. J Biol Chem 271:31679-31687.
15. Gerardin P, Barau G, Michault A, Bintner M, Randrianaivo H, Choker G, Lenglet Y, Touret Y, Bouveret A, Grivard P, Le Roux K, Blanc S, Schuffenecker I, Couderc T, Arenzana-Seisdedos F, Lecuit M, Robillard PY. 2008. Multidisciplinary prospective study of mother-to-child chikungunya virus infections on the island of La Reunion. PLoS Med 5:e60.
16. Gherzi R, Lee KY, Briata P, Wegmuller D, Moroni C, Karin M, Chen CY. 2004. A KH domain RNA binding protein, KSRP, promotes ARE-directed mRNA turnover by recruiting the degradation machinery. Mol Cell 14:571-583.
17. Hapuarachchi HC, Bandara KB, Sumanadasa SD, Hapugoda MD, Lai YL, Lee KS, Tan LK, Lin RT, Ng LF, Bucht G, Abeyewickreme W, Ng LC. 2010. Re-emergence of Chikungunya virus in South-east Asia: Virological evidence from Sri Lanka and Singapore. J Gen Virol 91:1067-1076.
18. He B, Feng Q, Mukherjee A, Lonard DM, DeMayo FJ, Katzenellenbogen BS, Lydon JP, O'Malley BW. 2008. A repressive role for prohibitin in estrogen signaling. Mol Endocrinol 22:344-360.
19. Her Z, Malleret B, Chan M, Ong EK, Wong SC, Kwek DJ, Tolou H, Lin RT, Tambyah PA, Renia L, Ng LF. 2010. Active infection of human blood monocytes by Chikungunya virus triggers an innate immune response. J Immunol 184:5903-5913.
20. Ikonen E, Fiedler K, Parton RG, Simons K. 1995. Prohibitin, an antiproliferative protein, is localized to mitochondria. FEBS Lett 358:273-277.
21. Jaffar-Bandjee MC, Ramful D, Gauzere BA, Hoarau JJ, Krejbich-Trotot P, Robin S, Ribera A, Selambarom J, Gasque P. 2010. Emergence and clinical insights into the pathology of Chikungunya virus infection. Expert Rev Anti Infect Ther 8:987-996.
22. Janabi N, Peudenier S, Heron B, Ng KH, Tardieu M. 1995. Establishment of human microglial cell lines after transfection of primary cultures of embryonic microglial cells with the SV40 large T antigen. Neurosci Lett 195:105-108.
23. Josseran L, Paquet C, Zehgnoun A, Caillere N, Le Tertre A, Solet JL, Ledrans M. 2006. Chikungunya disease outbreak, Reunion Island. Emerg Infect Dis 12:1994-1995.
24. Kasashima K, Sumitani M, Satoh M, Endo H. 2008. Human prohibitin 1 maintains the organization and stability of the mitochondrial nucleoids. Exp Cell Res 314:988-996.
25. Kolonin MG, Saha PK, Chan L, Pasqualini R, Arap W. 2004. Reversal of obesity by targeted ablation of adipose tissue. Nat Med 10:625-632.
26. Kroll TT, Zhao WM, Jiang C, Huber PW. 2002. A homolog of FBP2/KSRP binds to localized mRNAs in Xenopus oocytes. Development 129:5609-5619.
27. Kuadkitkan A, Wikan N, Fongsaran C, Smith DR. 2010. Identification and characterization of prohibitin as a receptor protein mediating DENV-2 entry into insect cells. Virology 406:149-161.
28. La Linn M, Eble JA, Lubken C, Slade RW, Heino J, Davies J, Suhrbier A. 2005. An arthritogenic alphavirus uses the alpha1beta1 integrin collagen receptor. Virology 336:229-239.
29. Labadie K, Larcher T, Joubert C, Mannioui A, Delache B, Brochard P, Guigand L, Dubreil L, Lebon P, Verrier B, de Lamballerie X, Suhrbier A, Cherel Y, Le Grand R, Roques P. 2010. Chikungunya disease in nonhuman primates involves long-term viral persistence in macrophages. J Clin Invest 120:894-906.
30. Lakshmi V, Neeraja M, Subbalaxmi MV, Parida MM, Dash PK, Santhosh SR, Rao PV. 2008. Clinical features and molecular diagnosis of Chikungunya fever from South India. Clin Infect Dis 46:1436-1442.
31. Leecharoenkiat A, Wannatung T, Lithanatudom P, Svasti S, Fucharoen S, Chokchaichamnankit D, Srisomsap C, Smith DR. 2011. Increased oxidative metabolism is associated with erythroid precursor expansion in beta0-thalassaemia/Hb E disease. Blood Cells Mol Dis 47:143-157.
32. Lin JY, Li ML, Shih SR. 2009. Far upstream element binding protein 2 interacts with enterovirus 71 internal ribosomal entry site and negatively regulates viral translation. Nucleic Acids Res 37:47-59.
33. Liu K, Qian L, Wang J, Li W, Deng X, Chen X, Sun W, Wei H, Qian X, Jiang Y, He F. 2009. Two-dimensional blue native/SDS-PAGE analysis reveals heat shock protein chaperone machinery involved in hepatitis B virus production in HepG2.2.15 cells. Mol Cell Proteomics 8:495-505.
34. Merkwirth C, Langer T. 2009. Prohibitin function within mitochondria: Essential roles for cell proliferation and cristae morphogenesis. Biochim Biophys Acta 1793:27-32.
35. Merkwirth C, Dargazanli S, Tatsuta T, Geimer S, Lower B, Wunderlich FT, von Kleist-Retzow JC, Waisman A, Westermann B, Langer T. 2008. Prohibitins control cell proliferation and apoptosis by regulating OPA1-dependent cristae morphogenesis in mitochondria. Genes Dev 22:476-488.
36. Mishra S, Murphy LC, Murphy LJ. 2006. The prohibitins: Emerging roles in diverse functions. J Cell Mol Med 10:353-363.
37. Nagy PD, Wang RY, Pogany J, Hafren A, Makinen K. 2011. Emerging picture of host chaperone and cyclophilin roles in RNA virus replication. Virology 411:374-382.
38. Ng LC, Hapuarachchi HC. 2010. Tracing the path of Chikungunya virus-Evolution and adaptation. Infect Genet Evol 10:876-885.
39. Ng LC, Tan LK, Tan CH, Tan SS, Hapuarachchi HC, Pok KY, Lai YL, Lam-Phua SG, Bucht G, Lin RT, Leo YS, Tan BH, Han HK, Ooi PL, James L, Khoo SP. 2009. Entomologic and virologic investigation of Chikungunya, Singapore. Emerg Infect Dis 15:1243-1249.
40. Nijtmans LG, de Jong L, Artal Sanz M, Coates PJ, Berden JA, Back JW, Muijsers AO, van der Spek H, Grivell LA. 2000. Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins. Embo J 19:2444-2451.
41. Nijtmans LG, Artal SM, Grivell LA, Coates PJ. 2002. The mitochondrial PHB complex: Roles in mitochondrial respiratory complex assembly, ageing and degenerative disease. Cell Mol Life Sci 59:143-155.
42. Padwad YS, Mishra KP, Jain M, Chanda S, Karan D, Ganju L. 2009. RNA interference mediated silencing of Hsp60 gene in human monocytic myeloma cell line U937 revealed decreased dengue virus multiplication. Immunobiology 214:422-429.
43. Paingankar MS, Gokhale MD, Deobagkar DN. 2010. Dengue-2-virus-interacting polypeptides involved in mosquito cell infection. Arch Virol 155:1453-1461.
44. Powers AM. 2010. Chikungunya. Clin Lab Med 30:209-219.
45. Pulmanausahakul R, Roytrakul S, Auewarakul P, Smith DR. 2011. Chikungunya in Southeast Asia: Understanding the emergence and finding solutions. Int J Infect Dis 15:671-676.
46. Reyes-del Valle J, Chavez-Salinas S, Medina F, Del Angel RM. 2005. Heat shock protein 90 and heat shock protein 70 are components of dengue virus receptor complex in human cells. J Virol 79:4557-4567.
47. Rezza G, Nicoletti L, Angelini R, Romi R, Finarelli AC, Panning M, Cordioli P, Fortuna C, Boros S, Magurano F, Silvi G, Angelini P, Dottori M, Ciufolini MG, Majori GC, Cassone A. 2007. Infection with chikungunya virus in Italy: An outbreak in a temperate region. Lancet 370:1840-1846.
48. Richter K, Haslbeck M, Buchner J. 2010. The heat shock response: Life on the verge of death. Mol Cell 40:253-266.
49. Robinson MC. 1955. An epidemic of virus disease in Southern Province, Tanganyika Territory, in 1952-53. I. Clinical features. Trans R Soc Trop Med Hyg 49:28-32.
50. Ross RW. 1956. The Newala epidemic. III. The virus: Isolation, pathogenic properties and relationship to the epidemic. J Hyg (Lond) 54:177-191.
51. Rydziel S, Delany AM, Canalis E. 2004. AU-rich elements in the collagenase 3 mRNA mediate stabilization of the transcript by cortisol in osteoblasts. J Biol Chem 279:5397-5404.
52. Sakoda S, Shanske S, DiMauro S, Schon EA. 1988. Isolation of a cDNA encoding the B isozyme of human phosphoglycerate mutase (PGAM) and characterization of the PGAM gene family. J Biol Chem 263:16899-16905.
53. Sam IC, Kamarulzaman A, Ong GS, Veriah RS, Ponnampalavanar S, Chan YF, AbuBakar S. 2010. Chikungunya virus-associated death in Malaysia. Trop Biomed 27:343-347.
54. Santhosh SR, Dash PK, Parida MM, Khan M, Tiwari M, Lakshmana Rao PV. 2008. Comparative full genome analysis revealed E1:A226V shift in 2007 Indian Chikungunya virus isolates. Virus Res 135:36-41.
55. Schuffenecker I, Iteman I, Michault A, Murri S, Frangeul L, Vaney MC, Lavenir R, Pardigon N, Reynes JM, Pettinelli F, Biscornet L, Diancourt L, Michel S, Duquerroy S, Guigon G, Frenkiel MP, Brehin AC, Cubito N, Despres P, Kunst F, Rey FA, Zeller H, Brisse S. 2006. Genome microevolution of chikungunya viruses causing the Indian Ocean outbreak. PLoS Med 3:e263.
56. Schwartz O, Albert ML. 2010. Biology and pathogenesis of chikungunya virus. Nat Rev Microbiol 8:491-500.
57. Sharma A, Qadri A. 2004. Vi polysaccharide of Salmonella typhi targets the prohibitin family of molecules in intestinal epithelial cells and suppresses early inflammatory responses. Proc Natl Acad Sci USA 101:17492-17497.
58. Solignat M, Gay B, Higgs S, Briant L, Devaux C. 2009. Replication cycle of chikungunya: A re-emerging arbovirus. Virology 393:183-197.
59. Sourisseau M, Schilte C, Casartelli N, Trouillet C, Guivel-Benhassine F, Rudnicka D, Sol-Foulon N, Le Roux K, Prevost MC, Fsihi H, Frenkiel MP, Blanchet F, Afonso PV, Ceccaldi PE, Ozden S, Gessain A, Schuffenecker I, Verhasselt B, Zamborlini A, Saib A, Rey FA, Arenzana-Seisdedos F, Despres P, Michault A, Albert ML, Schwartz O. 2007. Characterization of reemerging chikungunya virus. PLoS Pathog 3:e89.
60. Sriiam S, Leecharoenkiat A, Lithanatudom P, Wannatung T, Svasti S, Fucharoen S, Svasti J, Chokchaichamnankit D, Srisomsap C, Smith DR. 2012. Proteomic analysis of Hemoglobin H-Constant Spring (Hb H-CS) erythroblasts. Blood Cells Mol Dis 48:77-85.
61. Su HX, Xu DZ, Zhang YH, Men K, Zhao XN, Li D, Zhang L, Zhang JX, Yan YP. 2007. Screening cellular proteins binding to the core region of hepatitis C virus RNA genome with digoxin-labeled nucleic acids. Intervirology 50:303-309.
62. Suksanpaisan L, Susantad T, Smith DR. 2009. Characterization of dengue virus entry into HepG2 cells. J Biomed Sci 16:17.
63. Thepparit C, Smith DR. 2004. Serotype-specific entry of dengue virus into liver cells: Identification of the 37-kilodalton/67-kilodalton high-affinity laminin receptor as a dengue virus serotype 1 receptor. J Virol 78:12647-12656.
64. Thompson WE, Branch A, Whittaker JA, Lyn D, Zilberstein M, Mayo KE, Thomas K. 2001. Characterization of prohibitin in a newly established rat ovarian granulosa cell line. Endocrinology 142:4076-4085.
65. Tsetsarkin KA, Vanlandingham DL, McGee CE, Higgs S. 2007. A single mutation in chikungunya virus affects vector specificity and epidemic potential. PLoS Pathog 3:e201.
66. Tsetsarkin KA, McGee CE, Volk SM, Vanlandingham DL, Weaver SC, Higgs S. 2009. Epistatic roles of E2 glycoprotein mutations in adaption of chikungunya virus to Aedes albopictus and Ae. aegypti mosquitoes. PLoS ONE 4:e6835.
67. Ubol S, Griffin DE. 1991. Identification of a putative alphavirus receptor on mouse neural cells. J Virol 65:6913-6921.
68. Vazeille M, Moutailler S, Coudrier D, Rousseaux C, Khun H, Huerre M, Thiria J, Dehecq JS, Fontenille D, Schuffenecker I, Despres P, Failloux AB. 2007. Two Chikungunya isolates from the outbreak of La Reunion (Indian Ocean) exhibit different patterns of infection in the mosquito, Aedes albopictus. PLoS One 2:e1168.
69. Voss JE, Vaney MC, Duquerroy S, Vonrhein C, Girard-Blanc C, Crublet E, Thompson A, Bricogne G, Rey FA. 2010. Glycoprotein organization of Chikungunya virus particles revealed by X-ray crystallography. Nature 468:709-712.
70. Wang KS, Kuhn RJ, Strauss EG, Ou S, Strauss JH. 1992. High-affinity laminin receptor is a receptor for Sindbis virus in mammalian cells. J Virol 66:4992-5001.
71. Wang S, Fusaro G, Padmanabhan J, Chellappan SP. 2002. Prohibitin co-localizes with Rb in the nucleus and recruits N-CoR and HDAC1 for transcriptional repression. Oncogene 21:8388-8396.
72. Wikan N, Sakoonwatanyoo P, Ubol S, Yoksan S, Smith DR. 2012. Chikungunya virus infection of cell lines: Analysis of the East, central and South african lineage. PLoS ONE 7:e31102.
73. Yergolkar PN, Tandale BV, Arankalle VA, Sathe PS, Sudeep AB, Gandhe SS, Gokhle MD, Jacob GP, Hundekar SL, Mishra AC. 2006. Chikungunya outbreaks caused by African genotype, India. Emerg Infect Dis 12:1580-1583.