Elevated blood Hsp60, its structural similarities and cross-reactivity with thyroid molecules, and its presence on the plasma membrane of oncocytes point to the chaperonin as an immunopathogenic factor in Hashimoto's thyroiditis

Cell Stress and Chaperones

Volumn 19, Issue 3, 2014, Pages 343-353

  Marino Gammazza, Antonella ^a,b   Rizzo, Manfredi ^a,b   Citarrella, Roberto ^a   Rappa, Francesca ^a,b   Campanella, Claudia ^a,b   Bucchieri, Fabio ^a,b   Patti, Angelo ^a,b   Nikolic, Dragana ^a   Cabibi, Daniela ^a   Amico, Giandomenico ^c   Conaldi, Pier Giulio ^c   San Biagio, Pier Luigi ^d   Montalto, Giuseppe ^a   Farina, Felicia ^a   Zummo, Giovanni ^a   Conway De Macario, Everly ^e   Macario, Alberto J L ^b,e   Cappello, Francesco ^a,b,d  

^a UNIVERSITY OF PALERMO   (Italy)

^b Euro Mediterranean Institute of Science and Technology   (Italy)

^c MEDITERRANEAN INSTITUTE FOR TRANSPLANTATION AND ADVANCED SPECIALIZED THERAPIES ISMETT   (Italy)

^d CNR   (Italy)

^e UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Autoantibodies; Autoimmunity; Chaperonin; Hashimoto's thyroiditis (HT); Hsp60; Hurthle cells; Oncocytes; Thyrocytes; Thyroglobulin (TG); Thyroid peroxidase (TPO)

Indexed keywords

CHAPERONIN 60; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6; THYROGLOBULIN; THYROID PEROXIDASE; TUMOR NECROSIS FACTOR; ANTI-THYROGLOBULIN; AUTOANTIBODY; HSPD1 PROTEIN, HUMAN; INTEGRIN; IODIDE PEROXIDASE; MITOCHONDRIAL PROTEIN;

ADULT; ARTICLE; ASPIRATION CYTOLOGY; BIOINFORMATICS; CANCER CELL; CELL DESTRUCTION; CELL MEMBRANE; CELL STIMULATION; CELL SURFACE; CLINICAL ARTICLE; CONTROLLED STUDY; CROSS REACTION; CYTOKINE PRODUCTION; ELISA KIT; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FINE NEEDLE ASPIRATION BIOPSY; HASHIMOTO DISEASE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MALE; PATHOGENESIS; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; THYROID CELL; AMINO ACID SEQUENCE; BIOLOGY; BLOOD; CHEMISTRY; GOITER; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; MONONUCLEAR CELL; PATHOLOGY; STRUCTURAL HOMOLOGY; THYROID GLAND; THYROID PARAFOLLICULAR CELL; YOUNG ADULT;

ADULT; AMINO ACID SEQUENCE; AUTOANTIBODIES; CELL MEMBRANE; CHAPERONIN 60; COMPUTATIONAL BIOLOGY; CROSS REACTIONS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GOITER; HASHIMOTO DISEASE; HUMANS; IMMUNOHISTOCHEMISTRY; INTEGRINS; IODIDE PEROXIDASE; LEUKOCYTES, MONONUCLEAR; MALE; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; OXYPHIL CELLS; STRUCTURAL HOMOLOGY, PROTEIN; THYROGLOBULIN; THYROID GLAND; YOUNG ADULT;

EID: 84898906460     PISSN: 13558145     EISSN: 14661268     Source Type: Journal    
DOI: 10.1007/s12192-013-0460-9     Document Type: Article

References (43)

1. Ahmed R, Al-Shaikh S, Akhtar M (2012) Hashimoto thyroiditis: a century later. Adv Anat Pathol 19:181-186
2. Asea A (2003) Chaperokine-induced signal transduction pathways. Exerc Immunol Rev 9:25-33
3. Bethke K, Staib F, Distler M, Schmitt U, Jonuleit H, Enk AH, Galle PR, Heike M (2002) Different efficiency of heat shock proteins (HSP) to activate human monocytes and dendritic cells: superiority of HSP60. J Immunol 169:6141-6148
4. Bougacha-Elleuch N, Rebai A, Mnif M, Makni H, Bellassouad M, Jouida J, Abid M, Hammadi A (2004) Analysis of MHC genes in a Tunisian isolate with autoimmune thyroid diseases: implication of TNF -308 gene polymorphism. J Autoimmun 23:75-80
5. Campanella C, Bucchieri F, Merendino AM, Fucarino A, Burgio G, Corona DF, Barbieri G, David S, Farina F, Zummo G, Conway de Macario E, Macario AJL, Cappello F (2012) The odyssey of Hsp60 from tumor cells to other destinations includes plasma membrane-associated stages and Golgi and exosomal protein-trafficking modalities. PLoS One 7:e42008
6. Cappello F, Conway de Macario E, Marasà L, Zummo G, Macario AJL (2008) Hsp60 expression, new locations, functions and perspectives for cancer diagnosis and therapy. Cancer Biol Ther 7:801-809
7. Cappello F, Conway de Macario E, Di Felice V, Zummo G, Macario AJL (2009) Chlamydia trachomatis infection and anti-Hsp60 immunity: the two sides of the coin. PLoS Pathog 5(8):e1000552
8. Cappello F, Caramori G, Campanella C, Vicari C, Gnemmi I, Zanini A, Spanevello A, Capelli A, La Rocca G, Anzalone R, Bucchieri F, D'Anna SE, Ricciardolo FL, Brun P, Balbi B, Carone M, Zummo G, Conway de Macario E, Macario AJL, Di Stefano A (2011) Convergent sets of data from in vivo and in vitro methods point to an active role of Hsp60 in chronic obstructive pulmonary disease pathogenesis. PLoS One 6:e28200
9. Cechetto JD, Soltys BJ, Gupta RS (2000) Localization of mitochondrial 60-kD heat shock chaperonin protein (Hsp60) in pituitary growth hormone secretory granules and pancreatic zymogen granules. J Histochem Cytochem 48:45-56
10. Collins DP, Luebering BJ, Shaut DM (1998) T-lymphocyte functionality assessed by analysis of cytokine receptor expression, intracellular cytokine expression, and femtomolar detection of cytokine secretion by quantitative flow cytometry. Cytometry 33:249-255
11. Frankild S, de Boer RJ, Lund O, Nielsen M, Kesmir C (2008) Amino acid similarity accounts for T cell cross-reactivity and for "holes" in the T cell repertoire. PLoS One 3:e1831
12. Gazali A (2012) Conference scene: taking the heat out of chaperokine function. Immunotherapy 4:773-775
13. Gupta S, Knowlton AA (2007) HSP60 trafficking in adult cardiac myocytes: role of the exosomal pathway. Am J Physiol Heart Circ Physiol 292:H3052-H3056
14. Hansen JJ, Dürr A, Cournu-Rebeix I, Georgopoulos C, Ang D, Nielsen MN, Davoine CS, Brice A, Fontaine B, Gregersen N, Bross P (2002) Hereditary spastic paraplegia SPG13 is associated with a mutation in the gene encoding the mitochondrial chaperonin Hsp60. Am J Hum Genet 70:1328-1332
15. Hartl FU (1991) Heat shock proteins in protein folding and membrane translocation. Semin Immunol 3:5-16
16. Henderson B, Pockley AG (2010) Molecular chaperones and protein-folding catalysts as intercellular signaling regulators in immunity and inflammation. J Leukoc Biol 88:445-462
17. Heufelder AE, Goellner JR, Wenzel BE, Bahn RS (1992) Immunohistochemical detection and localization of a72-kilodalton heat shock protein in autoimmune thyroid disease. J Clin Endocrinol Metab 74:724-731
18. Jones DB, Coulson AF, Duff GW (1993) Sequence homologies between Hsp60 and autoantigens. Immunol Today 14:115-118
19. Jorgensen JL, Reay PA, Ehrich EW, Davis MM (1992) Molecular components of T-cell recognition. Annu Rev Immunol 10:835-873
20. Kotani T, Aratake Y, Hirai K, Hirai I, Ohtaki S (1996) High expression of heat shock protein 60 in follicular cells of Hashimoto's thyroiditis. Autoimmunity 25:1-8
21. Kotlarz A, Tukaj S, Krzewski K, Brycka E, Lipinska B (2013) Human Hsp40 proteins, DNAJA1 and DNAJA2, as potential targets of the immune response triggered by bacterial DnaJ in rheumatoid arthritis. Cell Stress Chaperones. doi: 10.1007/s12192-013-0407-1
22. Lorini R, Gastaldi R, Traggiai C, Perucchin PP (2003) Hashimoto's thyroiditis. Pediatr Endocrinol Rev Suppl 2:205-211
23. Macario AJL, Conway de Macario E, Cappello F (2013) The chaperonopathies. Diseases with defective molecular chaperones. Springer, London-New York. http://www.springer.com/biomed/book/978-94-007-4666-4
24. Marino Gammazza A, Bucchieri F, Grimaldi LM, Benigno A, Conway de Macario E, Macario AJL, Zummo G, Cappello F (2012) The molecular anatomy of human Hsp60 and its similarity with that of bacterial orthologs and acetylcholine receptor reveal a potential pathogenetic role of anti-chaperonin immunity in myasthenia gravis. Cell Mol Neurobiol 32:943-947
25. Merendino AM, Bucchieri F, Campanella C, Marcianò V, Ribbene A, David S, Zummo G, Burgio G, Corona DF, Conway de Macario E, Macario AJL, Cappello F (2010) Hsp60 is actively secreted by human tumor cells. PLoS One 5:e9247
26. Misaki T, Takeuchi R, Miyamoto S, Hirano A, Kasagi K, Konishi J (1994) Induction in vitro of 72-kD heat shock protein in a continuous culture of rat thyroid cells, FRTL5. Clin Exp Immunol 98:234-239
27. Osterloh A, Kalinke U, Weiss S, Fleischer B, Breloer M (2007) Synergistic and differential modulation of immune responses by Hsp60 and lipopolysaccharide. J Biol Chem 282:4669-4680
28. Pace A, Barone G, Lauria A, Martorana A, Piccionello AP, Pierro P, Terenzi A, Almerico AM, Buscemi S, Campanella C, Angileri F, Carini F, Zummo G, Conway de Macario E, Cappello F, Macario AJL (2013) Hsp60, a novel target for antitumor therapy: structure-function features and prospective drugs design. Curr Pharm Des 19:2757-2764
29. Pockley AG, Bulmer J, Hanks BM, Wright BH (1999) Identification of human heat shock protein 60 (Hsp60) and anti-Hsp60 antibodies in the peripheral circulation of normal individuals. Cell Stress Chaperones 4:29-35
30. Pockley AG, Muthana M, Calderwood SK (2008) The dual immunoregulatory roles of stress proteins. Trends Biochem Sci 33:71-79
31. Rappa F, Farina F, Zummo G, David S, Campanella C, Carini F, Tomasello G, Damiani P, Cappello F, Conway de Macario E, Macario AJL (2012) HSP-molecular chaperones in cancer biogenesis and tumor therapy: an overview. Anticancer Res 32:5139-5150
32. Rea IM, McNerlan S, Pockley AG (2001) Serum heat shock protein and anti-heat shock protein antibody levels in aging. Exp Gerontol 36:341-352
33. Rizzo M, Cappello F, Marfil R, Nibali L, Marino Gammazza A, Rappa F, Bonaventura G, Galindo-Moreno P, O'Valle F, Zummo G, Conway de Macario E, Macario AJL, Mesa F (2012) Heat-shock protein 60 kDa and atherogenic dyslipidemia in patients with untreated mild periodontitis: a pilot study. Cell Stress Chaperones 17:399-407
34. Rodolico V, Tomasello G, Zerilli M, Martorana A, Pitruzzella A, Gammazza AM, David S, Zummo G, Damiani P, Accomando S, Conway de Macario E, Macario AJL, Cappello F (2010) Hsp60 and Hsp10 increase in colon mucosa of Crohn's disease and ulcerative colitis. Cell Stress Chaperones 15:877-884
35. Serradifalco C, Catanese P, Rizzuto L, Cappello F, Puleio R, Barresi V, Nunnari CM, Zummo G, Di Felice V (2011) Embryonic and foetal Islet-1 positive cells in human hearts are also positive to c-Kit. Eur J Histochem 55:e41
36. Singh H, Ansari HR, Raghava GP (2013) Improved method for linear B-cell epitope prediction using antigen's primary sequence. PLoS One 8(5):e62216
37. Tomasello G, Rodolico V, Zerilli M, Martorana A, Bucchieri F, Pitruzzella A, Marino Gammazza A, David S, Rappa F, Zummo G, Damiani P, Accomando S, Rizzo M, Conway de Macario E, Macario AJL, Cappello F (2011a) Changes in immunohistochemical levels and subcellular localization after therapy and correlation and colocalization with CD68 suggest a pathogenetic role of Hsp60 in ulcerative colitis. Appl Immunohistochem Mol Morphol 19:552-561
38. Tomasello G, Sciumé C, Rappa F, Rodolico V, Zerilli M, Martorana A, Cicero G, De Luca R, Damiani P, Accardo FM, Romeo M, Farina F, Bonaventura G, Modica G, Zummo G, Conway de Macario E, Macario AJL, Cappello F (2011b) Hsp10, Hsp70, and Hsp90 immunohistochemical levels change in ulcerative colitis after therapy. Eur J Histochem 55:e38
39. Tulecke MA, Wang HH (2004) ThinPrep for cytologic evaluation of follicular thyroid lesions: correlation with histologic findings. Diagn Cytopathol 30:7-13
40. Vanderpump MP, Tunbridge WM (2002) Epidemiology and prevention of clinical and subclinical hypothyroidism. Thyroid 12:839-847
41. Xie J, Zhu H, Guo L, Ruan Y, Wang L, Sun L, Zhou L, Wu W, Yun X, Shen A, Gu J (2010) Lectin-like oxidized low-density lipoprotein receptor-1 delivers heat shock protein 60-fused antigen into the MHC class I presentation pathway. J Immunol 185:2306-2313
42. Yokota SI, Hirata D, Minota S, Higashiyama T, Kurimoto M, Yanagi H, Yura T, Kubota H (2000) Autoantibodies against chaperonin CCT in human sera with rheumatic autoimmune diseases: comparison with antibodies against other Hsp60 family proteins. Cell Stress Chaperones 5:337-346
43. Zanin-Zhorov A, Cahalon L, Tal G, Margalit R, Lider O, Cohen IR (2006) Heat shock protein 60 enhances CD4+ CD25+ regulatory T cell function via innate TLR2 signaling. J Clin Invest 116:2022-2032