The myths we believed in familial mediterranean fever: What have we learned in the past years?

Seminars in Immunopathology

Volumn 37, Issue 4, 2015, Pages 363-369

  Ozen, Seza ^a   Batu, Ezgi Deniz ^a  

^a HACETTEPE UNIVERSITY   (Turkey)

Author keywords

Autoinflammation; Familial Mediterranean fever; MEFV gene; Pyrin

Indexed keywords

C REACTIVE PROTEIN; CANAKINUMAB; COLCHICINE; CRYOPYRIN; FERRITIN; FIBRINOGEN; INFLAMMASOME; INTERLEUKIN 1; INTERLEUKIN 1 ANTIBODY; INTERLEUKIN 1BETA; RILONACEPT; CYTOSKELETON PROTEIN; MARENOSTRIN;

ABDOMINAL PAIN; AUTOSOMAL RECESSIVE INHERITANCE; CLINICAL FEATURE; DISEASE ACTIVITY; DISEASE SEVERITY; E148Q GENE; ENVIRONMENTAL FACTOR; ERYTHROCYTE SEDIMENTATION RATE; ETHNIC DIFFERENCE; EXON; FAMILIAL MEDITERRANEAN FEVER; GENE; GENE MUTATION; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC POLYMORPHISM; GENETIC RISK; GENETIC VARIABILITY; GENOTYPE; HETEROZYGOTE; HUMAN; INFLAMMATION; LOSS OF FUNCTION MUTATION; M694V GENE; MEFV GENE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; RISK FACTOR; SINGLE NUCLEOTIDE POLYMORPHISM; TREATMENT OUTCOME; DISEASE MANAGEMENT; GENETIC ASSOCIATION STUDY; GENETICS; METABOLISM; MUTATION; RECESSIVE GENE; SEVERITY OF ILLNESS INDEX;

CYTOSKELETAL PROTEINS; DISEASE MANAGEMENT; FAMILIAL MEDITERRANEAN FEVER; GENES, RECESSIVE; GENETIC ASSOCIATION STUDIES; HUMANS; MUTATION; PHENOTYPE; SEVERITY OF ILLNESS INDEX;

EID: 84943365154     PISSN: 18632297     EISSN: 18632300     Source Type: Journal    
DOI: 10.1007/s00281-015-0484-6     Document Type: Review

References (63)

1. Masters SL, Simon A, Aksentijevich I, Kastner DL (2009) Horror autoinflammaticus: the molecular pathophysiology of autoinflammatory disease (*). Annu Rev Immunol 27:621–668. doi:10.1146/annurev.immunol.25.022106.141627
2. Ozen S (2009) Mutations/polymorphisms in a monogenetic autoinflammatory disease may be susceptibility markers for certain rheumatic diseases: lessons from the bedside for the benchside. Clin Exp Rheumatol 27(2 Suppl 53):S29–31
3. Toplak N, Frenkel J, Ozen S, Lachmann HJ, Woo P, Kone-Paut I, De Benedetti F, Neven B, Hofer M, Dolezalova P, Kummerle- Deschner J, Touitou I, Hentgen V, Simon A, Girschick H, Rose C, Wouters C, Vesely R, Arostegui J, Stojanov S, Ozgodan H, Martini A, Ruperto N, Gattorno M, Paediatric Rheumatology International Trials Organisation E, Eurofever P (2012) An international registry on autoinflammatory diseases: the Eurofever experience. Ann Rheum Dis 71(7):1177–1182. doi:10.1136/annrheumdis-2011-200549
4. Tunca M, Akar S, Onen F, Ozdogan H, Kasapcopur O, Yalcinkaya F, Tutar E, Ozen S, Topaloglu R, Yilmaz E, Arici M, Bakkaloglu A, Besbas N, Akpolat T, Dinc A, Erken E, Turkish FMFSG (2005) Familial Mediterranean fever (FMF) in Turkey: results of a nationwide multicenter study. Medicine 84(1):1–11
5. Balow JE Jr, Shelton DA, Orsborn A, Mangelsdorf M, Aksentijevich I, Blake T, Sood R, Gardner D, Liu R, Pras E, Levy EN, Centola M, Deng Z, Zaks N, Wood G, Chen X, Richards N, Shohat M, Livneh A, Pras M, Doggett NA, Collins FS, Liu PP, Rotter JI, Kastner DL et al (1997) A high-resolution genetic map of the familial Mediterranean fever candidate region allows identification of haplotype-sharing among ethnic groups. Genomics 44(3):280–291
6. French FMFC (1997) A candidate gene for familial Mediterranean fever. Nat Genet 17(1):25–31. doi:10.1038/ng0997-25
7. Booty MG, Chae JJ, Masters SL, Remmers EF, Barham B, Le JM, Barron KS, Holland SM, Kastner DL, Aksentijevich I (2009) Familial Mediterranean fever with a single MEFV mutation: where is the second hit? Arthritis Rheum 60(6):1851–1861. doi:10.1002/art.24569
8. Shinar Y, Obici L, Aksentijevich I, Bennetts B, Austrup F, Ceccherini I, Costa JM, De Leener A, Gattorno M, Kania U, Kone-Paut I, Lezer S, Livneh A, Moix I, Nishikomori R, Ozen S, Phylactou L, Risom L, Rowczenio D, Sarkisian T, van Gijn ME, Witsch-Baumgartner M, Morris M, Hoffman HM, Touitou I, European Molecular Genetics Quality N (2012) Guidelines for the genetic diagnosis of hereditary recurrent fevers. Ann Rheum Dis 71(10):1599–1605. doi:10.1136/annrheumdis-2011-201271
9. Cazeneuve C, Hovannesyan Z, Genevieve D, Hayrapetyan H, Papin S, Girodon-Boulandet E, Boissier B, Feingold J, Atayan K, Sarkisian T, Amselem S (2003) Familial Mediterranean fever among patients from Karabakh and the diagnostic value of MEFV gene analysis in all classically affected populations. Arthritis Rheum 48(8):2324–2331. doi:10.1002/art.11102
10. Padeh S, Shinar Y, Pras E, Zemer D, Langevitz P, Pras M, Livneh A (2003) Clinical and diagnostic value of genetic testing in 216 Israeli children with familial Mediterranean fever. J Rheumatol 30(1):185–190
11. Marek-Yagel D, Berkun Y, Padeh S, Abu A, Reznik-Wolf H, Livneh A, Pras M, Pras E (2009) Clinical disease among patients heterozygous for familial Mediterranean fever. Arthritis Rheum 60(6):1862–1866. doi:10.1002/art.24570
12. Kalyoncu M, Acar BC, Cakar N, Bakkaloglu A, Ozturk S, Dereli E, Tunca M, Kasapcopur O, Yalcinkaya F, Ozen S (2006) Are carriers for MEFV mutations “healthy”? Clin Exp Rheumatol 24(5 Suppl 42):S120–122
13. Lachmann HJ, Sengul B, Yavuzsen TU, Booth DR, Booth SE, Bybee A, Gallimore JR, Soyturk M, Akar S, Tunca M, Hawkins PN (2006) Clinical and subclinical inflammation in patients with familialMediterranean fever and in heterozygous carriers ofMEFV mutations. Rheumatology (Oxford) 45(6):746–750. doi:10.1093/rheumatology/kei279
14. Federici S, Calcagno G, Finetti M, Gallizzi R, Meini A, Vitale A, Caroli F, Cattalini M, Caorsi R, Zulian F, Tommasini A, Insalaco A, Sormani MP, Baldi M, Ceccherini I, Martini A, Gattorno M (2012) Clinical impact of MEFV mutations in children with periodic fever in a prevalent western European Caucasian population. Ann Rheum Dis 71(12):1961–1965. doi:10.1136/annrheumdis-2011-200977
15. Omenetti A, Carta S, Delfino L, Martini A, Gattorno M, Rubartelli A (2014) Increased NLRP3-dependent interleukin 1beta secretion in patients with familial Mediterranean fever: correlation with MEFV genotype. Ann Rheum Dis 73(2):462–469. doi:10.1136/annrheumdis-2012-202774
16. Migita K, Agematsu K, Masumoto J, Ida H, Honda S, Jiuchi Y, Izumi Y, Maeda Y, Uehara R, Nakamura Y, Koga T, Kawakami A, Nakashima M, Fujieda Y, Nonaka F, Eguchi K, Furukawa H, Nakamura T, Nakamura M, Yasunami M (2013) The contribution of SAA1 polymorphisms to Familial Mediterranean fever susceptibility in the Japanese population. PLoS One 8(2):e55227. doi:10.1371/journal.pone.0055227
17. Niemi K, Teirila L, Lappalainen J, Rajamaki K, Baumann MH, Oorni K, Wolff H, Kovanen PT, Matikainen S, Eklund KK (2011) Serum amyloid A activates the NLRP3 inflammasome via P2X7 receptor and a cathepsin B-sensitive pathway. J Immunol 186(11): 6119–6128. doi:10.4049/jimmunol.1002843
18. Schwabe AD, Peters RS (1974) Familial Mediterranean fever in Armenians. Analysis of 100 cases. Medicine 53(6):453–462
19. Touitou I, Sarkisian T, Medlej-Hashim M, Tunca M, Livneh A, Cattan D, Yalcinkaya F, Ozen S, Majeed H, Ozdogan H, Kastner D, Booth D, Ben-Chetrit E, Pugnere D, Michelon C, Seguret F, Gershoni-Baruch R, International Study Group for Phenotype- Genotype Correlation in Familial Mediterranean F (2007) Country as the primary risk factor for renal amyloidosis in familial Mediterranean fever. Arthritis Rheum 56(5):1706–1712. doi:10.1002/art.22507
20. Ozen S, Aktay N, Lainka E, Duzova A, Bakkaloglu A, Kallinich T (2009) Disease severity in children and adolescents with familial Mediterranean fever: a comparative study to explore environmental effects on a monogenic disease. Ann Rheum Dis 68(2):246–248. doi:10.1136/ard.2008.092031
21. Ozen S, Demirkaya E, Amaryan G, Kone-Paut I, Polat A, Woo P, Uziel Y, Modesto C, Finetti M, Quartier P, Papadopoulou-Alataki E, Al-Mayouf SM, Fabio G, Gallizzi R, Cantarini L, Frenkel J, Nielsen S, Hofer M, Insalaco A, Acikel C, Ozdogan H, Martini A, Ruperto N, Gattorno M, Paediatric Rheumatology International Trials O, Eurofever P (2014) Results from a multicentre international registry of familial Mediterranean fever: impact of environment on the expression of a monogenic disease in children. Ann Rheum Dis 73(4):662–667. doi:10.1136/annrheumdis-2012-202708
22. Xu H, Yang J, Gao W, Li L, Li P, Zhang L, Gong YN, Peng X, Xi JJ, Chen S, Wang F, Shao F (2014) Innate immune sensing of bacterial modifications of Rho GTPases by the pyrin inflammasome. Nature 513(7517):237–241. doi:10.1038/nature13449
23. Gavrilin MA, Abdelaziz DH, Mostafa M, Abdulrahman BA, Grandhi J, Akhter A, Abu Khweek A, Aubert DF, Valvano MA, Wewers MD, Amer AO (2012) Activation of the pyrin inflammasome by intracellular Burkholderia cenocepacia. J Immunol 188(7):3469–3477. doi:10.4049/jimmunol.1102272
24. Jones JD, Dangl JL (2006) The plant immune system. Nature 444(7117):323–329. doi:10.1038/nature05286
25. Ozen S, Balci B, Ozkara S, Ozcan A, Yilmaz E, Besbas N, Ozguc M, Kastner DL, Bakkaloglu A (2002) Is there a heterozygote advantage for familial Mediterranean fever carriers against tuberculosis infections: speculations remain? Clin Exp Rheumatol 20(4 Suppl 26):S57–58
26. Ben-Zvi I, Krichely-Vachdi T, Feld O, Lidar M, Kivity S, Livneh A (2014) Colchicine-free remission in familial Mediterranean fever: featuring a unique subset of the disease-a case control study. Orphanet J Rare Dis 9:3. doi:10.1186/1750-1172-9-3
27. Papin S, Cuenin S, Agostini L, Martinon F, Werner S, Beer HD, Grutter C, Grutter M, Tschopp J (2007) The SPRY domain of Pyrin, mutated in familial Mediterranean fever patients, interacts with inflammasome components and inhibits proIL-1beta processing. Cell Death Differ 14(8):1457–1466. doi:10.1038/sj.cdd.4402142
28. Hesker PR, Nguyen M, Kovarova M, Ting JP, Koller BH (2012) Genetic loss of murine pyrin, the familialMediterranean Fever protein, increases interleukin-1beta levels. PLoS One 7(11):e51105. doi:10.1371/journal.pone.0051105
29. Yu JW, Fernandes-Alnemri T, Datta P, Wu J, Juliana C, Solorzano L, McCormick M, Zhang Z, Alnemri ES (2007) Pyrin activates the ASC pyroptosome in response to engagement by autoinflammatory PSTPIP1 mutants. Mol Cell 28(2):214–227. doi:10.1016/j.molcel.2007.08.029
30. Chae JJ, Cho YH, Lee GS, Cheng J, Liu PP, Feigenbaum L, Katz SI, Kastner DL (2011) Gain-of-function pyrin mutations induce NLRP3 protein-independent interleukin-1beta activation and severe autoinflammation in mice. Immunity 34(5):755–768. doi:10.1016/j.immuni.2011.02.020
31. Yalcinkaya F, Akar N, Misirlioglu M (1998) Familial Mediterranean fever—amyloidosis and the Val726Ala mutation. N Eng l J Med 338 (14):993–994. doi:10.1056/NEJM199804023381414
32. Akpolat T, Ozkaya O, Ozen S (2012) Homozygous M694 Vas a risk factor for amyloidosis in Turkish FMF patients. Gene 492(1):285–289. doi:10.1016/j.gene.2011.10.012
33. Giancane GTHN, Wulffraat N, Vastert B, Barron K, Hentgen V, Tilmann K, Ozdogan H, Lopez JA, Brogan P, Cantarini L, Frenkel J, Galeotti C, Gattorno M, Grateau G, Hofer M, Kone- Paut I, Kuemmerle-Deschner J, Lachmann H, Simon A, Feldman B, Uziel Y, Ozen S (2014) Evidence based recommendations for genetic diagnosis of familial Mediterranean fever. Pediatr Rheumatol 12(Suppl 1):241
34. Yilmaz E, Ozen S, Balci B, Duzova A, Topaloglu R, Besbas N, Saatci U, Bakkaloglu A, Ozguc M (2001) Mutation frequency of familial Mediterranean fever and evidence for a high carrier rate in the Turkish population. Eur J Hum Genet 9(7):553–555. doi:10.1038/sj.ejhg.5200674
35. Ozen S, Besbas N, Bakkaloglu A, Yilmaz E (2002) Pyrin Q148 mutation and familial Mediterranean fever. QJM 95(5):332–333
36. Topaloglu R, Ozaltin F, Yilmaz E, Ozen S, Balci B, Besbas N, Bakkaloglu A (2005) E148Q is a disease-causing MEFV mutation: a phenotypic evaluation in patients with familial Mediterranean fever. Ann Rheum Dis 64(5):750–752. doi:10.1136/ard.2004.026963
37. Ozen S, Bilginer Y (2014) A clinical guide to autoinflammatory diseases: familial Mediterranean fever and next-of-kin. Nat Rev Rheumatol 10(3):135–147. doi:10.1038/nrrheum.2013.174
38. Daniels M, Shohat T, Brenner-Ullman A, Shohat M (1995) Familial Mediterranean fever: high gene frequency among the non- Ashkenazic and Ashkenazic Jewish populations in Israel. Am J Med Genet 55(3):311–314. doi:10.1002/ajmg.1320550313
39. Ozen S, Karaaslan Y, Ozdemir O, Saatci U, Bakkaloglu A, Koroglu E, Tezcan S (1998) Prevalence of juvenile chronic arthritis and familial Mediterranean fever in Turkey: a field study. J Rheumatol 25(12):2445–2449
40. Kishida D, Nakamura A, Yazaki M, Tsuchiya-Suzuki A, Matsuda M, Ikeda SI (2014) Genotype-phenotype correlation in Japanese patients with familial Mediterranean fever: differences in genotype and clinical features between Japanese and Mediterranean populations. Arthritis Res Ther 16(5):439. doi:10.1186/s13075-014-0439-7
41. Brik R, Shinawi M, Kasinetz L, Gershoni-Baruch R (2001) The musculoskeletal manifestations of familial Mediterranean fever in children genetically diagnosed with the disease. Arthritis Rheum 44(6):1416–1419. doi :10.1002/1529-0131(200106) 44:6<1416::AID-ART236>3.0.CO;2-6
42. Cefle A, Kamali S, Sayarlioglu M, Inanc M, Ocal L, Aral O, Konice M, Gul A (2005) A comparison of clinical findings of familialMediterranean fever patients with and without amyloidosis. Rheumatol Int 25(6):442–446. doi:10.1007/s00296-004-0471-z43.
43. Kasifoglu T, Calisir C, Cansu DU, Korkmaz C (2009) The frequency of sacroiliitis in familial Mediterranean fever and the role of HLA-B27 and MEFV mutations in the development of sacroiliitis. Clin Rheumatol 28(1):41–46. doi:10.1007/s10067-008-0980-3
44. Langevitz P, Livneh A, Zemer D, Shemer J, Pras M (1997) Seronegative spondyloarthropathy in familial Mediterranean fever. Semin Arthritis Rheum 27(2):67–72
45. Livneh A, Langevitz P, Zemer D, Padeh S, Migdal A, Sohar E, Pras M (1996) The changing face of familial Mediterranean fever. Semin Arthritis Rheum 26(3):612–627
46. Ozdogan H, Arisoy N, Kasapcapur O, Sever L, Caliskan S, Tuzuner N, Mat C, Yazici H (1997) Vasculitis in familial Mediterranean fever. J Rheumatol 24(2):323–327
47. Ozen S, Ben-Chetrit E, Bakkaloglu A, Gur H, Tinaztepe K, Calguneri M, Turgan C, Turkmen A, Akpolat I, Danaci M, Besbas N, Akpolat T (2001) Polyarteritis nodosa in patients with familial Mediterranean Fever (FMF): a concomitant disease or a feature of FMF? Semin Arthritis Rheum 30(4):281–287. doi:10.1053/sarh.2001.19958
48. Kogan A, Shinar Y, Lidar M, Revivo A, Langevitz P, Padeh S, Pras M, Livneh A (2001) Common MEFV mutations among Jewish ethnic groups in Israel: high frequency of carrier and phenotype III states and absence of a perceptible biological advantage for the carrier state. Am J Med Genet 102(3):272–276
49. Ozen S, Bakkaloglu A, Yilmaz E, Duzova A, Balci B, Topaloglu R, Besbas N (2003) Mutations in the gene for familial Mediterranean fever: do they predispose to inflammation? J Rheumatol 30(9): 2014–2018
50. Rabinovich E, Livneh A, Langevitz P, Brezniak N, Shinar E, Pras M, Shinar Y (2005) Severe disease in patients with rheumatoid arthritis carrying a mutation in the Mediterranean fever gene. Ann Rheum Dis 64(7):1009–1014. doi:10.1136/ard.2004.029447
51. Ayaz NA, Ozen S, Bilginer Y, Erguven M, Taskiran E, Yilmaz E, Besbas N, Topaloglu R, Bakkaloglu A (2009) MEFV mutations in systemic onset juvenile idiopathic arthritis. Rheumatology 48(1): 23–25. doi:10.1093/rheumatology/ken409
52. Berkun Y, Levy R, Hurwitz A, Meir-Harel M, Lidar M, Livneh A, Padeh S (2011) The familialMediterranean fever gene as amodifier of periodic fever, aphthous stomatitis, pharyngitis, and adenopathy syndrome. Semin Arthritis Rheum 40(5):467–472. doi:10.1016/j.semarthrit.2010.06.009
53. Korkmaz C, Ozdogan H, Kasapcopur O, Yazici H (2002) Acute phase response in familial Mediterranean fever. Ann Rheum Dis 61(1):79–81
54. Duzova A, Bakkaloglu A, Besbas N, Topaloglu R, Ozen S, Ozaltin F, Bassoy Y, Yilmaz E (2003) Role of A-SAA in monitoring subclinical inflammation and in colchicine dosage in familial Mediterranean fever. Clin Exp Rheumatol 21(4):509–514
55. Ozturk MA, Kanbay M, Kasapoglu B, Onat AM, Guz G, Furst DE, Ben-Chetrit E (2011) Therapeutic approach to familial Mediterranean fever: a review update. Clin Exp Rheumatol 29(4 Suppl 67):S77–86
56. Hacihamdioglu DO, Ozen S (2012) Canakinumab induces remission in a patient with resistant familial Mediterranean fever. Rheumatology 51(6):1041. doi:10.1093/rheumatology/kes021
57. Meinzer U, Quartier P, Alexandra JF, Hentgen V, Retornaz F, Kone- Paut I (2011) Interleukin-1 targeting drugs in familial Mediterranean fever: a case series and a review of the literature. Semin Arthritis Rheum 41(2):265–271. doi:10.1016/j.semarthrit.2010.11.003
58. Ozen S, Bilginer Y, Aktay Ayaz N, Calguneri M (2011) Antiinterleukin 1 treatment for patients with familial Mediterranean fever resistant to colchicine. J Rheumatol 38(3):516–518. doi:10.3899/jrheum.100718
59. Hashkes PJ, Spalding SJ, Giannini EH, Huang B, Johnson A, Park G, Barron KS, Weisman MH, Pashinian N, Reiff AO, Samuels J, Wright DA, Kastner DL, Lovell DJ (2012) Rilonacept for colchicine-resistant or -intolerant familial Mediterranean fever: a randomized trial. Ann Intern Med 157(8):533–541. doi:10.7326/0003-4819-157-8-201210160-00003
60. Brik R, Butbul-Aviel Y, Lubin S, Ben Dayan E, Rachmilewitz- Minei T, Tseng L, Hashkes PJ (2014) Canakinumab for the treatment of children with colchicine-resistant familial Mediterranean fever: a 6 month open-label, single-arm pilot study. Arthritis Rheum 66(11):3241–3243. doi:10.1002/art.38777
61. Piram M, Frenkel J, Gattorno M, Ozen S, Lachmann HJ, Goldbach-Mansky R, Hentgen V, Neven B, Stojanovic KS, Simon A, Kuemmerle-Deschner J, Hoffman H, Stojanov S, Duquesne A, Pillet P, Martini A, Pouchot J, Kone-Paut I, Eurofever, networks E (2011) A preliminary score for the assessment of disease activity in hereditary recurrent fevers: results from the AIDAI (auto-inflammatory diseases activity index) consensus conference. Ann Rheum Dis 70(2):309–314. doi:10.1136/ard.2010.132613
62. Piram M, Kone-Paut I, Lachmann HJ, Frenkel J, Ozen S, Kuemmerle-Deschner J, Stojanov S, Simon A, Finetti M, Sormani MP, Martini A, Gattorno M, Ruperto N, on the behalf of Eurofever E, the Paediatric Rheumatology International Trials Organisation n (2013) Validation of the autoinflammatory diseases activity index (AIDAI) for hereditary recurrent fever syndromes. Ann Rheum Dis. doi:10.1136/annrheumdis-2013-203666
63. Ozen S, Demirkaya E, Duzova A, Erdogan O, Erken E, Gul A, Kasapcopur O, Kasifoglu T, Kisacik B, Ozdogan H, Tunca M, Acikel C, Vasculitis FMFA, Orphan disease Research in pediatric r, Turkish FMFsg (2014) FMF50: a score for assessing outcome in familial Mediterranean fever. Ann Rheum Dis 73(5):897–901. doi: 10.1136/annrheumdis-2013-204719