Characterization of the Resistance of SJL/J Mice to Pneumonia Virus of Mice, a Model for Infantile Bronchiolitis Due to a Respiratory Syncytial Virus

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Glineur, Stephanie ^a   Tran Anh, Dao Bui ^a   Sarlet, Michaël ^a   Michaux, Charles ^a   Desmecht, Daniel ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE IMMUNITY; ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; GAMMA IRRADIATION; GENETIC CODE; HEMATOPOIETIC CELL; HERITABILITY; HOST RESISTANCE; IN VIVO STUDY; LUNG ALVEOLUS EPITHELIUM; LUNG ALVEOLUS MACROPHAGE; MOUSE; MOUSE STRAIN; MURINE PNEUMONIA VIRUS; NONHUMAN; RADIOSENSITIVITY; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; SEGREGATION ANALYSIS; VIRAL BRONCHIOLITIS; VIRUS IDENTIFICATION; VIRUS RESISTANCE;

ANIMALS; BRONCHIOLITIS; DISEASE MODELS, ANIMAL; GENETIC PREDISPOSITION TO DISEASE; HUMANS; INFANT; MICE; MURINE PNEUMONIA VIRUS; RESPIRATORY SYNCYTIAL VIRUSES;

EID: 84867561691     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044581     Document Type: Article

References (89)

1. Glezen WP, Taber LH, Frank AL, Kasel JA, (1986) Risk of primary infection and reinfection with respiratory syncytial virus. American Journal of Diseases of Children 140: 543-546.
2. Leader S, Kohlhase K, (2003) Recent trends in severe respiratory syncytial virus (RSV) among US infants, 1997 to 2000. J Pediatr 143: S127-132.
3. Nair H, Nokes DJ, Gessner BD, Dherani M, Madhi SA, et al. (2010) Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: a systematic review and meta-analysis. Lancet 375: 1545-1555.
4. Ogra PL, (2004) Respiratory syncytial virus: the virus, the disease and the immune response. Paediatr Respir Rev 5 (Suppl A):: S119-126.
5. Hall CB, Weinberg GA, Iwane MK, Blumkin AK, Edwards KM, et al. (2009) The burden of respiratory syncytial virus infection in young children. N Engl J Med 360: 588-598.
6. Tregoning JS, Schwarze J, (2010) Respiratory viral infections in infants: causes, clinical symptoms, virology, and immunology. Clin Microbiol Rev 23: 74-98.
7. Thomsen SF, Stensballe LG, Skytthe A, Kyvik KO, Backer V, et al. (2008) Increased concordance of severe respiratory syncytial virus infection in identical twins. Pediatrics 121: 493-496.
8. Risch NJ, (2000) Searching for genetic determinants in the new millennium. Nature 405: 847-856.
9. Cordell HJ, Clayton DG, (2005) Genetic association studies. Lancet 366: 1121-1131.
10. Choi EH, Lee HJ, Yoo T, Chanock SJ, (2002) A common haplotype of interleukin-4 gene IL4 is associated with severe respiratory syncytial virus disease in Korean children. J Infect Dis 186: 1207-1211.
11. Hoebee B, Rietveld E, Bont L, Oosten M, Hodemaekers HM, et al. (2003) Association of severe respiratory syncytial virus bronchiolitis with interleukin-4 and interleukin-4 receptor alpha polymorphisms. J Infect Dis 187: 2-11.
12. Puthothu B, Krueger M, Forster J, Heinzmann A, (2006) Association between severe respiratory syncytial virus infection and IL13/IL4 haplotypes. J Infect Dis 193: 438-441.
13. Forton JT, Rowlands K, Rockett K, Hanchard N, Herbert M, et al. (2009) Genetic association study for RSV bronchiolitis in infancy at the 5q31 cytokine cluster. Thorax 64: 345-352.
14. Hull J, Ackerman H, Isles K, Usen S, Pinder M, et al. (2001) Unusual haplotypic structure of IL8, a susceptibility locus for a common respiratory virus. Am J Hum Genet 69: 413-419.
15. Hacking D, Knight JC, Rockett K, Brown H, Frampton J, et al. (2004) Increased in vivo transcription of an IL-8 haplotype associated with respiratory syncytial virus disease-susceptibility. Genes Immun 5: 274-282.
16. Lu A, Wang L, Zhang X, (2010) Haplotype of IL-8-251T and 781C is associated with the susceptibility to respiratory syncytial virus. J Trop Pediatr 56: 242-246.
17. Schuurhof A, Bont L, Siezen CL, Hodemaekers H, van Houwelingen HC, et al. (2010) Interleukin-9 polymorphism in infants with respiratory syncytial virus infection: an opposite effect in boys and girls. Pediatr Pulmonol 45: 608-613.
18. Hoebee B, Bont L, Rietveld E, van Oosten M, Hodemaekers HM, et al. (2004) Influence of promoter variants of interleukin-10, interleukin-9, and tumor necrosis factor-alpha genes on respiratory syncytial virus bronchiolitis. J Infect Dis 189: 239-247.
19. Wilson J, Rowlands K, Rockett K, Moore C, Lockhart E, et al. (2005) Genetic variation at the IL10 gene locus is associated with severity of respiratory syncytial virus bronchiolitis. J Infect Dis 191: 1705-1709.
20. Puthothu B, Krueger M, Forster J, Heinze J, Weckmann M, et al. (2007) Interleukin (IL)-18 polymorphism 133C/G is associated with severe respiratory syncytial virus infection. Pediatr Infect Dis J 26: 1094-1098.
21. Hull J, Rowlands K, Lockhart E, Moore C, Sharland M, et al. (2003) Variants of the chemokine receptor CCR5 are associated with severe bronchiolitis caused by respiratory syncytial virus. J Infect Dis 188: 904-907.
22. Amanatidou V, Sourvinos G, Apostolakis S, Neonaki P, Tsilimigaki A, et al. (2008) RANTES promoter gene polymorphisms and susceptibility to severe respiratory syncytial virus-induced bronchiolitis. Pediatr Infect Dis J 27: 38-42.
23. Amanatidou V, Sourvinos G, Apostolakis S, Tsilimigaki A, Spandidos DA, (2006) T280M variation of the CX3C receptor gene is associated with increased risk for severe respiratory syncytial virus bronchiolitis. Pediatr Infect Dis J 25: 410-414.
24. Aurivillius M, Oymar K, Oxelius VA, (2005) Immunoglobulin heavy G2 chain (IGHG2) gene restriction in the development of severe respiratory syncytial virus infection. Acta Paediatr 94: 414-418.
25. Tal G, Mandelberg A, Dalal I, Cesar K, Somekh E, et al. (2004) Association between common Toll-like receptor 4 mutations and severe respiratory syncytial virus disease. J Infect Dis 189: 2057-2063.
26. Puthothu B, Forster J, Heinzmann A, Krueger M, (2006) TLR-4 and CD14 polymorphisms in respiratory syncytial virus associated disease. Dis Markers 22: 303-308.
27. Awomoyi AA, Rallabhandi P, Pollin TI, Lorenz E, Sztein MB, et al. (2007) Association of TLR4 polymorphisms with symptomatic respiratory syncytial virus infection in high-risk infants and young children. J Immunol 179: 3171-3177.
28. Lofgren J, Ramet M, Renko M, Marttila R, Hallman M, (2002) Association between surfactant protein A gene locus and severe respiratory syncytial virus infection in infants. J Infect Dis 185: 283-289.
29. El Saleeby CM, Li R, Somes GW, Dahmer MK, Quasney MW, et al. (2010) Surfactant protein A2 polymorphisms and disease severity in a respiratory syncytial virus-infected population. J Pediatr 156: 409-414.
30. Thomas NJ, DiAngelo S, Hess JC, Fan R, Ball MW, et al. (2009) Transmission of surfactant protein variants and haplotypes in children hospitalized with respiratory syncytial virus. Pediatr Res 66: 70-73.
31. Puthothu B, Forster J, Heinze J, Heinzmann A, Krueger M, (2007) Surfactant protein B polymorphisms are associated with severe respiratory syncytial virus infection, but not with asthma. BMC Pulm Med 7: 6.
32. Puthothu B, Krueger M, Heinze J, Forster J, Heinzmann A, (2006) Haplotypes of surfactant protein C are associated with common paediatric lung diseases. Pediatr Allergy Immunol 17: 572-577.
33. Lahti M, Lofgren J, Marttila R, Renko M, Klaavuniemi T, et al. (2002) Surfactant protein D gene polymorphism associated with severe respiratory syncytial virus infection. Pediatr Res 51: 696-699.
34. Hattersley AT, McCarthy MI, (2005) What makes a good genetic association study? Lancet 366: 1315-1323.
35. Easton AJ, Domachowske JB, Rosenberg HF, (2004) Animal pneumoviruses: molecular genetics and pathogenesis. Clin Microbiol Rev 17: 390-412.
36. Welliver TP, Garofalo RP, Hosakote Y, Hintz KH, Avendano L, et al. (2007) Severe human lower respiratory tract illness caused by respiratory syncytial virus and influenza virus is characterized by the absence of pulmonary cytotoxic lymphocyte responses. J Infect Dis 195: 1126-1136.
37. Welliver TP, Reed JL, Welliver RC Sr, (2008) Respiratory syncytial virus and influenza virus infections: observations from tissues of fatal infant cases. Pediatr Infect Dis J 27: S92-96.
38. Rosenberg HF, Domachowske JB, (2008) Pneumonia virus of mice: severe respiratory infection in a natural host. Immunol Lett 118: 6-12.
39. Bem RA, Domachowske JB, Rosenberg HF, (2011) Animal models of human respiratory syncytial virus disease. American journal of physiology Lung cellular and molecular physiology 301: L148-156.
40. Anh DB, Faisca P, Desmecht DJ, (2006) Differential resistance/susceptibility patterns to pneumovirus infection among inbred mouse strains. Am J Physiol Lung Cell Mol Physiol 291: L426-435.
41. Glineur S, Antoine-Moussiaux N, Michaux C, Desmecht D, (2011) Immune depression of the SJL/J mouse, a radioresistant and immunologically atypical inbred strain. Immunobiology 216: 213-217.
42. Flandre TD, Leroy PL, Desmecht DJ, (2003) Effect of somatic growth, strain, and sex on double-chamber plethysmographic respiratory function values in healthy mice. Journal of Applied Physiology 94: 1129-1136.
43. Mather K, Jinks J L (1982) Biometrical Genetics. The study of continuous variation. London.: Chapman, Hall. 396 p.
44. Fulker DW, (1981) Biometrical genetics and individual differences. Br Med Bull 37: 115-120.
45. Evans DM, Gillespie NA, Martin NG, (2002) Biometrical genetics. Biol Psychol 61: 33-51.
46. SAS Institute Inc (1989) SAS/STAT User's Guide. Cary: NC:SAS Institute Inc. 846 p.
47. SAS Institute Inc (1997) SAS/STAT Software: Changes and Enhancements through Release 6.12. Cary: NC: SAS Institute Inc.
48. Guenet JL, (2005) Assessing the genetic component of the susceptibility of mice to viral infections. Brief Funct Genomic Proteomic 4: 225-240.
49. Lindenmann J, (1964) Inheritance of Resistance to Influenza Virus in Mice. Proc Soc Exp Biol Med 116: 506-509.
50. Brahic M, Bureau JF, Michiels T, (2005) The genetics of the persistent infection and demyelinating disease caused by Theiler's virus. Annu Rev Microbiol 59: 279-298.
51. Welton AR, Chesler EJ, Sturkie C, Jackson AU, Hirsch GN, et al. (2005) Identification of quantitative trait loci for susceptibility to mouse adenovirus type 1. Journal of Virology 79: 11517-11522.
52. Bodmer WF, Cavalli-Sforza LL (1976) Genetics, Evolution, and Man. San Francisco: W H Freeman and Company. 782 p.
53. Russel PJ (2006) iGenetics. A Molecular Approach. San Francisco: Pearson - Benjamin Cummings. 842 p.
54. Hager R, Cheverud JM, Wolf JB, (2008) Maternal effects as the cause of parent-of-origin effects that mimic genomic imprinting. Genetics 178: 1755-1762.
55. Sandor C, Georges M, (2008) On the detection of imprinted quantitative trait loci in line crosses: effect of linkage disequilibrium. Genetics 180: 1167-1175.
56. Kaplan C, Healing TD, Evans N, Healing L, Prior A, (1980) Evidence of infection by viruses in small British field rodents. J Hyg (Lond) 84: 285-294.
57. Ceccaldi PE, Marquette C, Weber P, Gourmelon P, Tsiang H, (1996) Ionizing radiation modulates the spread of an apathogenic rabies virus in mouse brain. Int J Radiat Biol 70: 69-75.
58. Pelka A, Olsberg C, Miller S, Waltenbaugh C, Creighton TM, et al. (1993) Effects of irradiation on development of Theiler's murine encephalomyelitis virus (TMEV)-induced demyelinating disease in genetically resistant mice. Cell Immunol 152: 440-455.
59. Spindler KR, Fang L, Moore ML, Hirsch GN, Brown CC, et al. (2001) SJL/J mice are highly susceptible to infection by mouse adenovirus type 1. J Virol 75: 12039-12046.
60. Downing L, Sawarynski KE, Li J, McGonagle M, Sims MD, et al. (2010) A simple quantitative method for assessing pulmonary damage after x irradiation. Radiat Res 173: 536-544.
61. Rube CE, Uthe D, Wilfert F, Ludwig D, Yang K, et al. (2005) The bronchiolar epithelium as a prominent source of pro-inflammatory cytokines after lung irradiation. Int J Radiat Oncol Biol Phys 61: 1482-1492.
62. Bogman MJ, Cornelissen IM, Berden JH, De Jong J, Koene RA, (1984) A comparative study of total body irradiation as a method of inducing granulocyte depletion in mice. Journal of immunological methods 70: 31-38.
63. Garg S, Boerma M, Wang J, Fu Q, Loose DS, et al. (2010) Influence of sublethal total-body irradiation on immune cell populations in the intestinal mucosa. Radiation research 173: 469-478.
64. Ossetrova NI, Sandgren DJ, Gallego S, Blakely WF, (2010) Combined approach of hematological biomarkers and plasma protein SAA for improvement of radiation dose assessment triage in biodosimetry applications. Health physics 98: 204-208.
65. Behlke MA, Chou HS, Huppi K, Loh DY, (1986) Murine T-cell receptor mutants with deletions of beta-chain variable region genes. Proc Natl Acad Sci U S A 83: 767-771.
66. Claassen EA, van der Kant PA, Rychnavska ZS, van Bleek GM, Easton AJ, et al. (2005) Activation and inactivation of antiviral CD8 T cell responses during murine pneumovirus infection. J Immunol 175: 6597-6604.
67. Claassen EA, van Bleek GM, Rychnavska ZS, de Groot RJ, Hensen EJ, et al. (2007) Identification of a CD4 T cell epitope in the pneumonia virus of mice glycoprotein and characterization of its role in protective immunity. Virology 368: 17-25.
68. Cullen SE, Schwartz BD, Nathenson SG, Cherry M, (1972) The molecular basis of codominant expression of the histocompatibility-2 genetic region. Proc Natl Acad Sci U S A 69: 1394-1397.
69. Trowsdale J, Campbell RD (2001) Mouse MHC genes and products. Curr Protoc Immunol Appendix 1: Appendix 1L.
70. Shanley JD, (1984) Host genetic factors influence murine cytomegalovirus lung infection and interstitial pneumonitis. J Gen Virol 65 (Pt 12) (): 2121-2128.
71. Siezen CL, Bont L, Hodemaekers HM, Ermers MJ, Doornbos G, et al. (2009) Genetic susceptibility to respiratory syncytial virus bronchiolitis in preterm children is associated with airway remodeling genes and innate immune genes. Pediatr Infect Dis J 28: 333-335.
72. Janssen R, Bont L, Siezen CL, Hodemaekers HM, Ermers MJ, et al. (2007) Genetic susceptibility to respiratory syncytial virus bronchiolitis is predominantly associated with innate immune genes. J Infect Dis 196: 826-834.
73. Matsushima GK, Stohlman SA (1991) Immunological disorders in SJL/J mice. Immunological disorders in mice. CRC Press ed: Vetvicka and Rihova. pp. 77-94.
74. Chambers KA, Harrington NP, Ross WM, Filion LG, (1998) Relative alterations in blood mononuclear cell populations reflect radiation injury in mice. Cytometry 31: 45-52.
75. Kajioka EH, Andres ML, Li J, Mao XW, Moyers MF, et al. (2000) Acute effects of whole-body proton irradiation on the immune system of the mouse. Radiat Res 153: 587-594.
76. Gross NJ, (1977) Alveolar macrophage number: an index of the effect of radiation on the lungs. Radiat Res 72: 325-332.
77. Bowden DH, Adamson IY, (1980) Role of monocytes and interstitial cells in the generation of alveolar macrophages I. Kinetic studies of normal mice. Lab Invest 42: 511-517.
78. Meyer OT, Dannenberg AM Jr, (1970) Radiation, infection, and macrophage function. II. Effect of whole body radiation on the number of pulmonary alveolar macrophages and their levels of hydrolytic enzymes. J Reticuloendothel Soc 7: 79-90.
79. Collins PL, Melero JA, (2011) Progress in understanding and controlling respiratory syncytial virus: still crazy after all these years. Virus research 162: 80-99.
80. Lukens MV, van de Pol AC, Coenjaerts FE, Jansen NJ, Kamp VM, et al. (2010) A systemic neutrophil response precedes robust CD8(+) T-cell activation during natural respiratory syncytial virus infection in infants. Journal of virology 84: 2374-2383.
81. Kaminsky SG, Nakamura I, Cudkowicz G, (1985) Genetic control of the natural killer cell activity in SJL and other strains of mice. J Immunol 135: 665-671.
82. Kaminsky SG, Nakamura I, Cudkowicz G, (1983) Selective defect of natural killer and killer cell activity against lymphomas in SJL mice: low responsiveness to interferon inducers. J Immunol 130: 1980-1984.
83. Dahlberg A, Auble MR, Petro TM, (2006) Reduced expression of IL-12 p35 by SJL/J macrophages responding to Theiler's virus infection is associated with constitutive activation of IRF-3. Virology 353: 422-432.
84. Spann KM, Tran KC, Chi B, Rabin RL, Collins PL, (2004) Suppression of the induction of alpha, beta, and lambda interferons by the NS1 and NS2 proteins of human respiratory syncytial virus in human epithelial cells and macrophages [corrected]. J Virol 78: 4363-4369.
85. Heinze B, Frey S, Mordstein M, Schmitt-Graff A, Ehl S, et al. (2011) Both Nonstructural Proteins 1 and 2 of Pneumonia Virus of Mice are Inhibitors of the Interferon Type I and III Response In Vivo. J Virol.
86. Buchholz UJ, Ward JM, Lamirande EW, Heinze B, Krempl CD, et al. (2009) Deletion of nonstructural proteins NS1 and NS2 from pneumonia virus of mice attenuates viral replication and reduces pulmonary cytokine expression and disease. J Virol 83: 1969-1980.
87. Rigaux P, Killoran KE, Qiu Z, Rosenberg HF, (2011) Depletion of alveolar macrophages prolongs survival in response to acute pneumovirus infection. Virology.
88. Pribul PK, Harker J, Wang B, Wang H, Tregoning JS, et al. (2008) Alveolar macrophages are a major determinant of early responses to viral lung infection but do not influence subsequent disease development. J Virol 82: 4441-4448.
89. Reed JL, Brewah YA, Delaney T, Welliver T, Burwell T, et al. (2008) Macrophage impairment underlies airway occlusion in primary respiratory syncytial virus bronchiolitis. J Infect Dis 198: 1783-1793.