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Animal Models of Sjögren’s Syndrome

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Abstract

Sjögren’s syndrome is an autoimmune, chronic inflammatory disease characterized by focal mononuclear cell infiltration of exocrine tissues, accompanied by loss of secretory function. The pathogenesis of autoimmune diseases is complex and, therefore, difficult to study in vitro. As of today, the role of initiating factors remains obscure, clinical symptoms develop late, and there are no tests for early diagnosis of SS. Hence, the disease is difficult to detect and treat. Animal models may provide insights into the identification of target antigens, narrowing the relevant pathological immune mechanisms, and to study the evolution of tissue pathology. This review summarizes current knowledge on murine strains, both spontaneous and induced models, used to study Sjögren’s syndrome. Special attention is paid to the characteristics of different strains regarding their properties to mimic specific aspects or stages of the disease.

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References

  1. Jonsson R, Bowman SJ, Gordon TP (2005) In: Arthritis and Allied Conditions, Koopman WJ (ed) Lippincott Williams & Wilkins, Philadelphia, pp 1681–1705

  2. Jonsson R, Kroneld U, Backman K, Magnusson B, Tarkowski A (1993) Br J Rheumatol 32:578–581

    Article  PubMed  CAS  Google Scholar 

  3. Humphreys-Beher MG, Brayer J, Yamachika S, Peck AB, Jonsson R (1999) Scand J Immunol 49:7–10

    Article  PubMed  CAS  Google Scholar 

  4. Garberg H, Jonsson R, Brokstad KA (2005) Scand J Rheumatol 34:49–55

    Article  PubMed  CAS  Google Scholar 

  5. Bolstad AI, Jonsson R (1998) Ann Med Interne (Paris) 149:25–29

    CAS  Google Scholar 

  6. Jonsson R, Nginamau E, Szyszko E, Brokstad KA (2007) Front Biosci 12:2159–2170

    Article  PubMed  CAS  Google Scholar 

  7. Vogelsang P, Jonsson MV, Dalvin ST, Appel S (2006) Scand J Immunol 64:219–226

    Article  PubMed  CAS  Google Scholar 

  8. Jonsson R, Skarstein K (2001) In: Theofilopoulos AN, Bona CA (eds) The molecular pathology of autoimmune diseases. Taylor & Francis, New York, pp 437–452

  9. Tarkowski A, Jonsson R, Klareskog L (1986) Scand J Rheumatol Suppl 61:274–279

    PubMed  CAS  Google Scholar 

  10. Hoffmann RW, Walker SE (1987) In: Talal N, Moutsopoulos HM, Kassan SS (eds) Sjögren’s syndrome—clinical and immunological aspects. Springer, Berlin, pp 266–288

  11. Hayashi Y, Deguchi H, Nakahata A, Kurashima C, Utsuyama M, Hirokawa K (1990) Autoimmunity 5:215–228

    PubMed  CAS  Google Scholar 

  12. Hayashi Y, Haneji N, Hamano H (1994) Pathol Int 44:559–568

    PubMed  CAS  Google Scholar 

  13. Horsfall A, Skarstein K, Jonsson R (1994) In: Isenberg DA, Horsfall A (eds) Autoimmune diseases: focus on Sjögren’s syndrome. BIOS Scientific, London, pp 67–88

  14. Humphreys-Beher MG (1996) Adv Dent Res 10:73–75

    Article  PubMed  CAS  Google Scholar 

  15. Kessler HS (1968) Am J Pathol 52:671–685

    PubMed  CAS  Google Scholar 

  16. Hoffman RW, Alspaugh MA, Waggie KS, Durham JB, Walker SE (1984) Arthritis Rheum 27:157–165

    Article  PubMed  CAS  Google Scholar 

  17. Miyagawa J, Hanafusa T, Miyazaki A, Yamada K, Fujino-Kurihara H, Nakajima H, Kono N, Nonaka K, Tochino Y, Tarui S (1986) Virchows Arch B Cell Pathol Incl Mol Pathol 51:215–225

    PubMed  CAS  Google Scholar 

  18. Kessler HS, Cubberly M, Manski W (1971) Arch Ophthalmol 85:211–219

    PubMed  CAS  Google Scholar 

  19. Keyes GG, Vickers RA, Kersey JH (1977) J Oral Pathol 6:288–295

    Article  PubMed  CAS  Google Scholar 

  20. Jonsson R, Tarkowski A, Bäckman K, Klareskog L (1987) Clin Immunol Immunopathol 42:93–101

    Article  PubMed  CAS  Google Scholar 

  21. Hang L, Theofilopoulos AN, Dixon FJ (1982) J Exp Med 155:1690–1701

    Article  PubMed  CAS  Google Scholar 

  22. Jonsson R, Tarkowski A, Bäckman K, Holmdahl R, Klareskog L (1987) Immunology 60:611–616

    PubMed  CAS  Google Scholar 

  23. Hoffman RW, Yang HK, Waggie KS, Durham JB, Burge JR, Walker SE (1983) Arthritis Rheum 26:645–652

    Article  PubMed  CAS  Google Scholar 

  24. Scott J, Wolff A, Fox PC (1990) J Oral Pathol Med 19:131–135

    Article  PubMed  CAS  Google Scholar 

  25. Watanabe-Fukunaga R, Brannan CI, Copeland NG, Jenkins NA, Nagata S (1992) Nature 356:314–317

    Article  PubMed  CAS  Google Scholar 

  26. Singer GG, Abbas AK (1994) Immunity 1:365–371

    Article  PubMed  CAS  Google Scholar 

  27. Skarstein K, Nerland AH, Eidsheim M, Mountz JD, Jonsson R (1997) Scand J Immunol 46:373–378

    Article  PubMed  CAS  Google Scholar 

  28. Toda I, Wickham LA, Sullivan DA (1998) Clin Immunol Immunopathol 86:59–71

    Article  PubMed  CAS  Google Scholar 

  29. Jonsson R, Holmdahl R (1990) J Oral Pathol Med 19:330–334

    Article  PubMed  CAS  Google Scholar 

  30. Skarstein K, Johannessen AC, Holmdahl R, Jonsson R (1997) Clin Immunol Immunopathol 84:177–184

    Article  PubMed  CAS  Google Scholar 

  31. Skarstein K, Holmdahl R, Johannessen AC, Goldschmidt T, Jonsson R (1995) Scand J Immunol 42:529–534

    Article  PubMed  CAS  Google Scholar 

  32. Jonsson R, Pitts A, Mestecky J, Koopman W (1991) Autoimmunity 10:7–14

    Article  PubMed  CAS  Google Scholar 

  33. Hamano H, Saito I, Haneji N, Mitsuhashi Y, Miyasaka N, Hayashi Y (1993) Eur J Immunol 23:2387–2391

    Article  PubMed  CAS  Google Scholar 

  34. Mustafa W, Zhu J, Deng G, Diab A, Link H, Frithiof L, Klinge B (1998) Clin Exp Immunol 112:389–396

    Article  PubMed  CAS  Google Scholar 

  35. Bolstad AI, Jonsson R (2002) Arthritis Res 4:353–359

    Article  PubMed  Google Scholar 

  36. Robinson CP, Yamachika S, Bounous DI, Brayer J, Jonsson R, Holmdahl R, Peck AB, Humphreys-Beher MG (1998) Arthritis Rheum 41:150–156

    Article  PubMed  CAS  Google Scholar 

  37. Lindqvist AK, Nakken B, Sundler M, Kjellen P, Jonsson R, Holmdahl R, Skarstein K (2005) Scand J Immunol 61:119–127

    Article  PubMed  CAS  Google Scholar 

  38. Shoda LK, Young DL, Ramanujan S, Whiting CC, Atkinson MA, Bluestone JA, Eisenbarth GS, Mathis D, Rossini AA, Campbell SE, Kahn R, Kreuwel HT (2005) Immunity 23:115–126

    Article  PubMed  CAS  Google Scholar 

  39. Anderson MS, Bluestone JA (2005) Annu Rev Immunol 23:447–485

    Article  PubMed  CAS  Google Scholar 

  40. Skarstein K, Wahren M, Zaura E, Hattori M, Jonsson R (1995) Autoimmunity 22:9–16

    PubMed  CAS  Google Scholar 

  41. Yamachika S, Nanni JM, Nguyen KH, Garces L, Lowry JM, Robinson CP, Brayer J, Oxford GE, da Silveira A, Kerr M, Peck AB, Humphreys-Beher MG (1998) J Rheumatol 25:2371–2380

    PubMed  CAS  Google Scholar 

  42. Perez P, Goicovich E, Alliende C, Aguilera S, Leyton C, Molina C, Pinto R, Romo R, Martinez B, Gonzalez MJ (2000) Arthritis Rheum 43:2807–2817

    Article  PubMed  CAS  Google Scholar 

  43. Goicovich E, Molina C, Perez P, Aguilera S, Fernandez J, Olea N, Alliende C, Leyton C, Romo R, Leyton L, Gonzalez MJ (2003) Arthritis Rheum 48:2573–2584

    Article  PubMed  CAS  Google Scholar 

  44. Jonsson MV, Salomonsson S, Øijordsbakken G, Skarstein K (2005) Scand J Immunol 62:552–559

    Article  PubMed  CAS  Google Scholar 

  45. Jonsson MV, Delaleu N, Brokstad KA, Berggreen E, Skarstein K (2006) Arthritis Rheum 54:2300–2305

    Article  PubMed  CAS  Google Scholar 

  46. Salam MA, Matin K, Matsumoto N, Tsuha Y, Hanada N, Senpuku H (2004) J Immunol 173:4908–4918

    PubMed  CAS  Google Scholar 

  47. Winer S, Astsaturov I, Cheung R, Tsui H, Song A, Gaedigk R, Winer D, Sampson A, McKerlie C, Bookman A, Dosch HM (2002) Lancet 360:1063–1069

    Article  PubMed  CAS  Google Scholar 

  48. Gordaon TP, Cavill D, Neufing P, Zhang YJ, Pietropaolo M (2004) Lupus 13:483–484

    Article  Google Scholar 

  49. Robinson CP, Brayer J, Yamachika S, Esch TR, Peck AB, Stewart CA, Peen E, Jonsson R, Humphreys-Beher MG (1998) Proc Natl Acad Sci U S A 95:7538–7543

    Article  PubMed  CAS  Google Scholar 

  50. Gao J, Killedar S, Cornelius JG, Nguyen C, Cha S, Peck AB (2006) J Autoimmun 26:90–103

    Article  PubMed  CAS  Google Scholar 

  51. Masago R, Aiba-Masago S, Talal N, Zuluaga FJ, Al-Hashimi I, Moody M, Lau CA, Peck AB, Brayer J, Humphreys-Beher MG, Dang H (2001) Arthritis Rheum 44:693–702

    Article  PubMed  CAS  Google Scholar 

  52. Serreze DV, Chapman HD, Post CM, Johnson EA, Suarez-Pinzon WL, Rabinovitch A (2001) J Immunol 166:1352–1359

    PubMed  CAS  Google Scholar 

  53. Yanagi K, Ishimaru N, Haneji N, Saegusa K, Saito I, Hayashi Y (1998) Eur J Immunol 28:3336–3345

    Article  PubMed  CAS  Google Scholar 

  54. Yamano S, Atkinson JC, Baum BJ, Fox PC (1999) Clin Immunol 92:265–275

    Article  PubMed  CAS  Google Scholar 

  55. Brayer JB, Cha S, Nagashima H, Yasunari U, Lindberg A, Diggs S, Martinez J, Goa J, Humphreys-Beher MG, Peck AB (2001) Scand J Immunol 54:133–140

    Article  PubMed  CAS  Google Scholar 

  56. Cha S, Brayer J, Gao J, Brown V, Killedar S, Yasunari U, Peck AB (2004) Scand J Immunol 60:552–565

    Article  PubMed  CAS  Google Scholar 

  57. Haneji N, Hamano H, Yanagi K, Hayashi Y (1994) J Immunol 153:2769–2777

    PubMed  CAS  Google Scholar 

  58. Haneji N, Nakamura T, Takio K, Yanagi K, Higashiyama H, Saito I, Noji S, Sugino H, Hayashi Y (1997) Science 276:604–607

    Article  PubMed  CAS  Google Scholar 

  59. Zandbelt MM, Vogelzangs J, Van De Putte LB, Van Venrooij WJ, Van Den Hoogen FH (2004) Arthritis Res Ther 6:R33–R38

    Article  PubMed  CAS  Google Scholar 

  60. Hayashi Y (2006) NFS/sld mouse model for primary Sjögren’s syndrome. In: IXth international symposium on Sjögren’s syndrome, Washington, DC

  61. Saegusa J, Kubota H (1997) J Vet Med Sci 59:897–903

    Article  PubMed  CAS  Google Scholar 

  62. Takada K, Takiguchi M, Konno A, Inaba M (2004) Rheumatology (Oxford) 43:858–862

    Article  CAS  Google Scholar 

  63. Takada K, Takiguchi M, Konno A, Inaba M (2005) J Biol Chem 280:3982–3988

    Article  PubMed  CAS  Google Scholar 

  64. Kimura T, Suzuki K, Inada S, Hayashi A, Saito H, Miyai T, Ohsugi Y, Matsuzaki Y, Tanaka N, Osuga T et al (1994) Clin Exp Immunol 95:525–529

    Article  PubMed  CAS  Google Scholar 

  65. Saito I, Haruta K, Shimuta M, Inoue H, Sakurai H, Yamada K, Ishimaru N, Higashiyama H, Sumida T, Ishida H, Suda T, Noda T, Hayashi Y, Tsubota K (1999) J Immunol 162:2488–2494

    PubMed  CAS  Google Scholar 

  66. Shull MM, Ormsby I, Kier AB, Pawlowski S, Diebold RJ, Yin M, Allen R, Sidman C, Proetzel G, Calvin D et al (1992) Nature 359:693–699

    Article  PubMed  CAS  Google Scholar 

  67. McCartney-Francis NL, Mizel DE, Redman RS, Frazier-Jessen M, Panek RB, Kulkarni AB, Ward JM, McCarthy JB, Wahl SM (1996) J Immunol 157:1306–1312

    PubMed  CAS  Google Scholar 

  68. Mackay F, Schneider P, Rennert P, Browning J (2003) Annu Rev Immunol 21:231–264

    Article  PubMed  CAS  Google Scholar 

  69. Szodoray P, Jonsson R (2005) Scand J Immunol 62:421–428

    Article  PubMed  CAS  Google Scholar 

  70. Gross JA, Johnston J, Mudri S, Enselman R, Dillon SR, Madden K, Xu W, Parrish-Novak J, Foster D, Lofton-Day C, Moore M, Littau A, Grossman A, Haugen H, Foley K, Blumberg H, Harrison K, Kindsvogel W, Clegg CH (2000) Nature 404:995–999

    Article  PubMed  CAS  Google Scholar 

  71. Mackay F, Woodcock SA, Lawton P, Ambrose C, Baetscher M, Schneider P, Tschopp J, Browning JL (1999) J Exp Med 190:1697–1710

    Article  PubMed  CAS  Google Scholar 

  72. Groom J, Kalled SL, Cutler AH, Olson C, Woodcock SA, Schneider P, Tschopp J, Cachero TG, Batten M, Wheway J, Mauri D, Cavill D, Gordon TP, Mackay CR, Mackay F (2002) J Clin Invest 109:59–68

    Article  PubMed  CAS  Google Scholar 

  73. Batten M, Fletcher C, Ng LG, Groom J, Wheway J, Laabi Y, Xin X, Schneider P, Tschopp J, Mackay CR, Mackay F (2004) J Immunol 172:812–822

    PubMed  CAS  Google Scholar 

  74. Voulgarelis M, Dafni UG, Isenberg DA, Moutsopoulos HM (1999) Arthritis Rheum 42:1765–1772

    Article  PubMed  CAS  Google Scholar 

  75. Green JE, Hinrichs SH, Vogel J, Jay G (1989) Nature 341:72–74

    Article  PubMed  CAS  Google Scholar 

  76. Yokota Y (2001) Oncogene 20:8290–8298

    Article  PubMed  CAS  Google Scholar 

  77. Quong MW, Romanow WJ, Murre C (2002) Annu Rev Immunol 20:301–322

    Article  PubMed  CAS  Google Scholar 

  78. Alani RM, Silverthorn CF, Orosz K (2004) Cancer Biol Ther 3:498–500

    PubMed  Google Scholar 

  79. Li H, Dai M, Zhuang Y (2004) Immunity 21:551–560

    Article  PubMed  CAS  Google Scholar 

  80. Nishimori I, Bratanova T, Toshkov I, Caffrey T, Mogaki M, Shibata Y, Hollingsworth MA (1995) J Immunol 154:4865–4873

    PubMed  CAS  Google Scholar 

  81. Inagaki Y, Jinno-Yoshida Y, Hamasaki Y, Ueki H (1991) J Dermatol Sci 2:147–154

    Article  PubMed  CAS  Google Scholar 

  82. Topfer F, Gordon T, McCluskey J (1995) Proc Natl Acad Sci U S A 92:875–879

    Article  PubMed  CAS  Google Scholar 

  83. Keech CL, Gordon TP, McCluskey J (1996) J Immunol 157:3694–3699

    PubMed  CAS  Google Scholar 

  84. Tseng CE, Chan EK, Miranda E, Gross M, Di Donato F, Buyon JP (1997) Arthritis Rheum 40:936–944

    Article  PubMed  CAS  Google Scholar 

  85. Reynolds P, Gordon TP, Purcell AW, Jackson DC, McCluskey J (1996) J Exp Med 184:1857–1870

    Article  PubMed  CAS  Google Scholar 

  86. Kurien BT, Asfa S, Li C, Dorri Y, Jonsson R, Scofield RH (2005) Scand J Immunol 61:418–425

    Article  PubMed  CAS  Google Scholar 

  87. Scofield RH, Asfa S, Obeso D, Jonsson R, Kurien BT (2005) J Immunol 175:8409–8414

    PubMed  CAS  Google Scholar 

  88. Fleck M, Kern ER, Zhou T, Lang B, Mountz JD (1998) Arthritis Rheum 41:2175–2184

    Article  PubMed  CAS  Google Scholar 

  89. Fleck M, Zhang HG, Kern ER, Hsu HC, Muller-Ladner U, Mountz JD (2001) Arthritis Rheum 44:964–973

    Article  PubMed  CAS  Google Scholar 

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Acknowledgment

This work was supported by grants from the Faculty of Odontology, University of Bergen, the L. Meltzer Foundation, the Olaf og Gullborg Johannessens Legacy, the Research Council of Norway, the NDD Fond for Dental Research, the Broegelmann Foundation, Helse Vest, and the Strategic Research Program at Helse Bergen.

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  1. Broegelmann Research Laboratory, The Gade Institute, University of Bergen, Armauer Hansen Building, 5021, Bergen, Norway

    Malin V. Jonsson, Nicolas Delaleu & Roland Jonsson

  2. Department of Oral Sciences–Oral Pathology and Forensic Odontology, University of Bergen, Bergen, Norway

    Malin V. Jonsson

  3. Department of Rheumatology, Haukeland University Hospital, Bergen, Norway

    Roland Jonsson

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  1. Malin V. Jonsson
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  2. Nicolas Delaleu
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Correspondence to Roland Jonsson.

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Jonsson, M.V., Delaleu, N. & Jonsson, R. Animal Models of Sjögren’s Syndrome. Clinic Rev Allerg Immunol 32, 215–224 (2007). https://doi.org/10.1007/s12016-007-8012-7

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