Human IAPP amyloidogenic properties and pancreatic β-cell death

Cell Calcium

Volumn 56, Issue 5, 2014, Pages 416-427

  Fernández, Marta S ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

Author keywords

Amylin; Amyloid; HIAPP; Human islet amyloid polypeptide; Ion channels; T2DM; Type 2 diabetes mellitus; Cell death

Indexed keywords

AMYLIN; INTERLEUKIN 1BETA; THIOREDOXIN INTERACTING PROTEIN; INSULIN;

APOPTOSIS; AUTOPHAGY; CELL DEATH; CELL MEMBRANE; CHANNEL GATING; CYTOTOXICITY; ENDOPLASMIC RETICULUM STRESS; HUMAN; MEMBRANE BINDING; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PATHOPHYSIOLOGY; PHYSICAL CHEMISTRY; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN HOMEOSTASIS; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE; AMINO ACID SEQUENCE; GENETICS; METABOLISM; PANCREAS ISLET; PATHOLOGY;

AMINO ACID SEQUENCE; APOPTOSIS; DIABETES MELLITUS, TYPE 2; HUMANS; INSULIN; INSULIN-SECRETING CELLS; ISLET AMYLOID POLYPEPTIDE; ISLETS OF LANGERHANS;

EID: 84912064413     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2014.08.011     Document Type: Review

References (108)

1. Hayden M.R. Islet amyloid, metabolic syndrome, and the natural progressive history of type 2 diabetes mellitus. JOP J. Pancreas (Online) 2002, 3:126-138.
2. Weir G.C., Bonner-Weir S. Five stages of evolving β-cell dysfunction during progression to diabetes. Diabetes 2004, 53:S16-S21.
3. Kahn S.E., Cooper M.E., Del Prato S. Pathophysiology and treatment of type 2 diabetes: perspectives on the past, present, and future. Lancet 2014, 383:1068-1083.
4. Butler A.E., Janson J., Bonner-Weir S., Ritzel R., et al. β-Cell deficit and increased β-cell apoptosis in humans with type 2 diabetes. Diabetes 2003, 52:102-110.
5. Schnabel J. The dark side of proteins. Nature 2010, 464:828-829.
6. Hoppener J.W.M., Ahren B., Lips C.J.M. Islet amyloid and type 2 diabetes mellitus. N. Engl. J. Med. 2000, 343:411-419.
7. Uversky V.N., Oldfield C.J., Dunker A.K. Intrinsically disordered proteins in human diseases: introducing the D2 concept. Annu. Rev. Biophys. 2008, 37:215-246.
8. Westwell-Roper C., Ehses J.A. Is there a role for the adaptive immune system in pancreatic beta cell failure in type 2 diabetes?. Diabetologia 2014, 57:447-450.
9. Guardado-Mendoza R., Davalli A.M., Chavez A.O., Hubbard G.B., et al. Pancreatic isletamyloidosis, beta-cell apoptosis, and alpha-cell proliferation are determinants of islet remodeling in type-2 diabetic baboons. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:13992-13997.
10. Westermark P., Anderson A., Westermark G. Islet amyloid polypeptide, islet amyloid, and diabetes mellitus. Physiol. Rev. 2011, 91:795-826.
11. Opie E.L. The relation of diabetes mellitus to lesions of the pancreas. Hyaline degeneration of the islands of Langerhans. J. Exp. Med. 1901, 5:527-540.
12. Ehrlich J., Ratner I.M. Amyloidosis of the islets of Langerhans. A restudy of islet hyalin in diabetic and nondiabetic individuals. Am. J. Pathol. 1961, 38:49-59.
13. Sunde M., Serpell L.C., Bartlam M., Fraser P.E., et al. Common core structure of amyloid fibrils by synchrotron X-ray diffraction. J. Mol. Biol. 1997, 273:729-739.
14. Westermark P., Wilander E., Westermark G.T., Johnson K.H. Islet amyloid polypeptide-like immunoreactivity in the islet B cells of type 2 (non-insulin-dependent) diabetic and non-diabetic individuals. Diabetologia 1987, 30:887-892.
15. Westermark P., Wernstedt C., Wilander E., Hayden D.W., O'Brien T.D., Johnson K.H. Amyloid fibrils in human insulinoma and islets of Langerhans of the diabetic cat are derived from a neuropeptide-like protein also present in normal islet cells. Proc. Natl. Acad. Sci. U.S.A. 1987, 84:3881-3885.
16. Janson J., Soeller W.C., Roche P.C., Nelson R.T., Torchia A.J., Kreutter D.K., Butler P.C. Spontaneous diabetes mellitus in transgenic mice expressing human islet amyloid polypeptide. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:7283-7288.
17. Mather K.J., Paradisi G., Leaming R., Hook G., et al. Role of amylin in insulin secretion and action in humans: antagonist studies across the spectrum of insulin sensitivity. Diabetes Metab. Res Rev. 2002, 18:118-126.
18. Wimalawansa S.J. Amylin, calcitonin gene-related peptide, calcitonin, and adrenomedullin: a peptide superfamily. Crit. Rev. Neurobiol. 1997, 11:167-239.
19. Sanke T., Bell G.I., Sample C., Rubenstein A.H., et al. An islet amyloid peptide is derived from an 89-amino acid precursor by proteolytic processing. J. Biol. Chem. 1988, 26:17243-17246.
20. Seino S. S20G mutation of the amylin gene is associated with Type II diabetes in Japanese. Diabetologia 2001, 44:906-909.
21. Inoue K., Hisatomi A., Umeda F., Nawata H. Relative hypersecretion of amylin to insulin from rat pancreas after neonatal STZ treatment. Diabetes 1992, 41:723-727.
22. Mulder H., Ahren B., Stridsberg M., Sundler F. Non-parallelism of islet amyloid polypeptide (amylin) and insulin gene expression in rat islets following dexamethasone treatment. Diabetologia 1995, 38:395-402.
23. Pieber T.R., Stein D.T., Ogawa A., Alam T., et al. Amylin-insulin relationships in insulin resistance with and without diabetic hyperglycemia. Am. J. Physiol. 1993, 265:E446-E453.
24. Hebda J.A., Miranker A.D. The interplay of catalysis and toxicity by amyloid intermediates on lipid bilayers: insights from tipe II diabetes. Annu. Rev. Biophys. 2009, 38:125-152.
25. Qiao Q., Bowman G.R., Huang X. Dynamics of an intrinsically disordered protein. Reveal metastable conformations that potentially seed aggregation. J. Am. Chem. Soc. 2013, 135:16092-16101.
26. Dunker A.K., Oldfield C.J., Meng J., Romero P. The unfoldomics decade: an update on intrinsically disordered proteins. BMC Genomics 2008, 9(Suppl 2):S1. 10.1186/1471-2164-9-S2-S1.
27. Mészáros B., Tompa P., Simon I., Dosztányi Z. Molecular principles of the interactions of disordered proteins. J. Mol. Biol. 2007, 372:549-561.
28. Anfinsen C.B. Principles that govern the folding of protein chains. Science 1973, 181:223-230.
29. Jiang P., Xu W., Mu Y. Amyloidogenesis abolished by proline substitutions but enhanced by lipid binding. PLoS Comput. Biol. 2009, 5:e1000357. 10.1371/journal.pcbi.1000357.
30. Sumner Makin O., Serpell L.C. Structural characterisation of islet amyloid polypeptide fibrils. J. Mol. Biol. 2004, 335:1279-1288.
31. Wiltzius J.J.W., Sievers S.A., Sawaya M.R., Cascio D., et al. Atomic structure of the cross-β spine of islet amyloid polypeptide (amylin). Protein Sci. 2008, 17:1467-1474.
32. Sawaya M.R., Sambashivan S., Nelson R., Ivanova M.I., et al. Atomic structures of amyloid cross-β spines reveal varied steric zippers. Nature 2007, 447:453-457.
33. Eisenberg D., Jucker M. The amyloid state of proteins in human diseases. Cell 2012, 148:1188-1203.
34. Wiltzius J.J.W., Sievers S.A., Sawaya M.R., Eisenberg D. Atomic structures of IAPP (amylin) fusions suggest a mechanism for fibrillation and the role of insulin in the process. Protein Sci. 2009, 18:1521-1530.
35. Singh S., Chiu C.C., Reddy A.S., de Pablo J.J. α-Helix to β-hairpin transition of human amylin monomer. J. Chem. Phys. 2013, 138:155101-155106.
36. Logue S.E., Gorman A.M., Cleary P., Keogh N., et al. Current concepts in ER stress induced apoptosis. J. Carcinog. Mutag. 2013, S6-002. 10.4172/2157-2518.
37. Johnson J.D., Luciani D.S. Mechanisms of pancreatic beta-cell apoptosis in diabetes and its therapies, in M.S. Islam et al. The Islets of Langerhans. Adv. Exp. Med. Biol. 2010, 654:447-462.
38. Eizirik D.L., Cnop M. ER stress in pancreatic β-cells: the thin red line between adaptation and failure. Sci. Signal. 2010, 3:pe7.
39. Xu C., Bailly-Maitre B., Reed J.C. Endoplasmic reticulum stress: cell life and death decisions. J. Clin. Invest. 2005, 115:2656-2664.
40. Haataja L., Gurlo T., Huang C.J., Butler P.C. Islet amyloid in type 2 diabetes, and the toxic oligomer hypothesis. Endoc. Rev. 2008, 29:303-316.
41. Huang C., Lin C., Haataja L., Gurlo T., et al. High expression rates of human islet amyloid polypeptide induce endoplasmic reticulum stress-mediated β-cell apopotosis, a characteristic of humans with type 2 but not type 1 diabetes. Diabetes 2007, 56:2016-2027.
42. Marciniak S.J., Yun C.Y., Oyadomari S., Novoa I., Zhang Y., Jungreis R., Nagata K., Harding H.P., Ron D. CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev. 2004, 18:3066-3077.
43. Chiribau C.B., Gaccioli F., Huang C.C., Yuan C.L., et al. Molecular symbiosis of CHOP and C/EBPβ isoform LIP contributes to endoplasmic reticulum stress-induced apoptosis. Mol. Cell. Biol. 2010, 30:3722-3731.
44. Hull R.L., Zraika S., Udayasankar J., Aston-Mourney K., et al. Amyloid formation in human IAPP transgenic mouse islets and pancreas and human pancreas is not associated with endoplasmic reticulum stress. Diabetologia 2009, 52:1102-1111.
45. Matveyenko A.V., Gurlo T., Daval M., Butler A.E., Butler P.C. Successful versus failed adaptation to high-fat diet-induced insulin resistance. The role of IAPP-induced β-cell endoplasmic reticulum stress. Diabetes 2009, 58:906-916.
46. Subramanian S.L., Hull R.L., Zraika S., Aston-Mourney K., et al. cJUN N-terminal kinase (JNK) activation mediates islet amyloid-induced beta cell apoptosis in cultured human islet amyloid polypeptide transgenic mouse islets. Diabetologia 2012, 55(1):166-174.
47. Win S., Than T.A., Fernández-Checa J.C., Klapowitz N. JNK interaction with SAB mediates ER stress induced inhibition of mitochondrial respiration and cell death. Cell Death Dis. 2014, 5:e989. 10.1038/cddis.2013.522.
48. Gurlo T., Ryazantsev S., Huang C., Yeh M.W., et al. Evidence for proteotoxicity in β cells in type 2 diabetes. Toxic islet amyloid polypeptide oligomers form intracellularly in the secretory pathway. Am. J. Pathol. 2010, 176(Feb (2)):861-869.
49. Lin C.Y., Gurlo T., Kayed R., Butler A.E., Haataja L., Glabe C.G., Butler P.C. Toxic human islet amyloid polypeptide (h-IAPP) misfolded oligomers are intracellular, and vaccination to induce anti-toxic oligomer antibodies does not prevent h-IAPP-induced-βcell apoptosis in h-IAPP transgenic mice. Diabetes 2007, 56:1324-1332.
50. Johnson J.D., Bround M.J., White S.A., Sarah A A. Nanospaces between endoplasmic reticulum and mitochondria as control centres of pancreatic β-cell metabolism and survival. Protoplasma 2012, 249:49-58.
51. Csordas G., Varnai P., Golenar T., Roy S., Purkins G., Schneider T.G., Balla T., Hajnoczky G. Imaging interoganelle contacts and local calcium dynamics at the ER-mitochondrial interface. Mol. Cell 2010, 39:121-132.
52. Chu K.Y., Li H., Wada K., Johnson J.D. Ubiquitin C-terminal hydrolase L1 is required for pancreatic beta cell survival and function in lipotoxic conditions. Diabetologia 2012, 55:128-140.
53. Costes S., Huang C., Gurlo T., Daval M., et al. β-Cell dysfunctional ERAD/ubiquitin/proteasome system in type 2 diabetes mediated by islet amyloid polypeptide-induced UCH-L1 deficiency. Diabetes 2011, 60:227-238.
54. Choi J., Levey A.I., Weintraub S.T., Rees H.D., et al. Oxidative modifications and down-regulation of ubiquitin carboxyl-terminal hydrolase L1 associated with idiopathic Parkinson's and Alzheimer's diseases. J. Biol. Chem. 2004, 279:13256-13264.
55. Lam Y.A., Pickart C.M., Alban A., Landon M., et al. Inhibition of the ubiquitin-proteasome system in Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:9902-9906.
56. Naught K.S.P., Jenner P. Proteasomal function is impaired in substantia nigra in Parkinson's disease. Neurosci. Lett. 2001, 297:191-194.
57. Choi J., Levey A., Weintraub S.T., Rees H.D., et al. Oxidative modifications and down-regulation of ubiquitin carboxyl-terminal hydrolase L1 associated with idiopathic Parkinson's and Alzheimer's diseases. J. Biol. Chem. 2004, 279:13256-13313.
58. Casas S., Gomis R., Gribble F.M., Altirriba J., et al. Impairment of the ubiquitin-proteasome pathway is a downstream endoplasmic reticulum stress response induced by extracellular human islet amyloid polypeptide and contributes to pancreatic beta-cell apoptosis. Diabetes 2007, 56:2284-2294.
59. Levine B., Yuan J. Autophagy in cell death: an innocent convict?. J. Clin. Invest. 2005, 115:2679-2688.
60. Mizushima N., Levine B., Cuervo A.M., Klionsky D. Autophagy fights disease through cellular self-digestion. Nature 2008, 451:1069-1075.
61. Jung H.S., Lee M.S. Macroautophagy in homeostasis of pancreatic β-cell. Autophagy 2009, 5:241-243.
62. Delgado M.E., Dyck L., Laussmann M.A., Rehm M. Modulation of apoptosis sensitivity through the interplay with autophagic and proteasomal degradation pathways. Cell Death Dis. 2014, 5:e1011. 10.1038/cddis.2013.520.
63. Rivera J.F., Gurlo T., Daval M., Huang C.J., et al. Human-IAPP disrupts the autophagy/lysosomal pathway in pancreatic β-cells: protective role of p62-positive cytoplasmic inclusions. Cell Death Differ. 2011, 18:415-426.
64. Montane J., Cadavez L., Novials A. Stress and the inflammatory process: a major cause of pancreatic cell death in type 2 diabetes. Diabetes Metab. Syndr. Obes. 2014, 7:25-34.
65. Masters S.L., Dunne A., Subramanian S.L., Hull R.L., et al. Activation of the Nlrp3 inflammasome by islet amyloid polypeptide provides a mechanism for enhanced IL-1β in type 2 diabetes. Nat. Immunol. 2010, 11:897-904.
66. Halle A., et al. The NALP3 inflammasome is involved in the innate inmmune response to amyloid-β. Nat. Immunol. 2008, 9:857-865.
67. Badman M.K., Price R.A., Charge S.B., Morris J.F., Clark A. Fibrillar islet amyloid polypeptide (amylin) is internalised by macrophages but resists proteolytic degradation. Cell Tissue Res. 1998, 291:285-294.
68. de Koning E.J., et al. Macrophages and pancreatic islet amyloidosis. Amyloid 1998, 5:247-254.
69. Gitter B.D., Cox L.M., Carlson C.D., May P.C. Human amylin stimulates inflammatory cytokine secretion by human glioma cells. Neuroimmunomodulation 2000, 7:147-152.
70. Yates S.L., et al. Amyloid beta and amylin fibrils induce increases in proinflammatory cytokine and chemokine production by THP-1 cells and murine microglia. J. Neurochem. 2000, 74:1017-1025.
71. Westwell-Roper C., Dai D.L., Soukhatcheva G., van Rooijen N., et al. IL-1 blockade attenuates islet amyloid polypeptide-induced proinflammatory cytokine release and pancreatic islet graft dysfunction. J. Immunol. 2011, 187:2755-2765.
72. Chen J., Saxena G., Mungrue I.N., Lusis A.J., et al. Thioredoxin-interacting protein: a critical link between glucose toxicity and β-cell apoptosis. Diabetes 2008, 57:938-944.
73. Oslowski C.M., Hara T., O'Sullivan-Murphy B., Kanekura K., et al. Thioredoxin-interacting protein mediates ER stress-induced β-cell death through initiation of the inflammasome. Cell Metab. 2012, 16:265-273.
74. Zhou D., Palam L.R., Jiang L., Narasimhan J., Staschke K.A., Wek R.C. Phosphorylation of eIF2 directs ATF5 translational control in response to diverse stress conditions. J. Biol. Chem. 2008, 283:7064-7073.
75. Xu G., Chen J., Jin G., Shalev A. Thioredoxin-interacting protein regulates insulin transcription through microRNA-204. Nat. Med. 2013, 19:1141-1146.
76. Jing G., Westwell-Roper C., Chen J., Xu G., et al. Thioredoxin-interacting protein promotes islet amyloid polypeptide expression through MIR-124A and FoxA2. J. Biol. Chem. 2014, 289:11807-11815.
77. Corbett J.A. Thioredoxin-interacting protein is killing my β-cells!. Diabetes 2008, 57:797-798.
78. Pannuzzo M., Raudino A., Milardi D., La Rosa C., Karttunen M. α-Helical structures drive early stages of self-assembly of amyloidogenic amyloid polypeptide aggregate formation in membranes. Sci. Rep. 2013, 3:2781. 10.1038/srep02781.
79. Brender J.R., Lee E.L., Cavitt M.A., Gafni A., et al. Amyloid fiber formation and membrane disruption are separate processes localized in two distinct regions of IAPP, the type-2-diabetes-related peptide, J. Am. Chem. Soc. 2008, 130:6424-6429.
80. Brender J.R., Salamekh S., Ramamoorthy A. Membrane disruption and early events in the aggregation of the diabetes related peptide IAPP from a molecular perspective. Acc. Chem. Res. 2012, 45:454-462.
81. Mirzabekov T.A., Lin M.C., Kagan B.L. Pore formation by the cytotoxic islet amyloid peptide amylin. J. Biol. Chem. 1996, 271:1988-1992.
82. Sciacca M.F.M., Milardi D., Messina G.M.L., Marletta G., Brender J.R., Ramamoorthy A., Rosa C.L. Cations as switches of amyloid-mediated membrane disruption mechanisms: calcium and IAPP. Biophys. J. 2013, 104:173-184.
83. Hirakura Y., Yiu W.W., Yamamoto A., Kagan B.L. Amyloid peptide channels: blockade by zinc and inhibition by congo red (amyloid channel block). Amyloid 2000, 7:194-199.
84. Demuro A., Mina E., Kayed R., Milton S.C., Parker I., Glabe C.G. Calcium dysregulation and membrane disruption as a ubiquitous neurotoxic mechanism of soluble amyloid oligomers. J. Biol. Chem. 2005, 280:17294-17300.
85. Zhao J., Luo Y., Jang H., Yu X., Nussinov R., Zheng J., et al. Probing ion channel activity of human islet amyloid polypeptide (amylin). Biochim. Biophys. Acta 2012, 1818:3121-3130.
86. Zhao J., Hu R., Sciacca M.F.M., Brender J.R., et al. Non-selective ion channel activity of polymorphic human islet amyloid polypeptide (amylin) double channels. Phys. Chem. Chem. Phys. 2014, 16:2368-2377.
87. Poojari C., Xiao D., Batista V.S., Strodel B. Membrane permeation induced by aggregates of human islet amyloid polypeptides. Biophys. J. 2013, 105:2323-2332.
88. Casa S., Novials A., Reiman F., Gomis R., Gribble F.M. Calcium elevation in mouse pancreatic beta cells evoked by extracellular human islet amyloid polypeptide involves activation of the mechanosensitive ion channel TRPV4. Diabetologia 2008, 51:2252-2262.
89. Everaerts W., Nilius B., Owsianik G. The vanilloid transient receptor potential channel TRPV4: from structure to disease. Prog. Biophys. Mol. Biol. 2010, 103:2-17.
90. Gu Y., Gu C. Physiological and pathological functions of mechanosensitive ion channels. Mol. Neurobiol. 2014, (Feb). 10.1007/s12035-014-8654-4.
91. Potter K.J., Scrocchi L.A., Warnock G.L., et al. Amyloid inhibitors enhance survival of cultured human islets. Biochim Biophys Acta 2009, 1790(6):566-574.
92. Ohsawa H., Kanatsuka A., Yamaguchi T., Makino H., Yoshida S. Islet amyloid polypeptide inhibits glucose-stimulated insulin secretion from isolated rat pancreatic islets. Biochem. Biophys. Res. Commun. 1989, 160:961-967.
93. Zhu T., Wang Y., He B., Zang J., He Q., Zhang W. Islet amyloid polypeptide acts on glucose stimulated beta cells to reduce voltage-gated calcium channel activation, intracellular Ca2+ concentration, and insulin secretion. Diabetes Metab. Res. Rev. 2011, 27:28-34.
94. ATP) channels in the loss of β-cell function induced by human islet amyloid polypeptide. J. Biol. Chem. 2011, 286:40857-40866.
95. Craig T.J., Ashcroft F.M., Proks P.J. How ATP inhibits the open K(ATP) channel. J. Gen. Physiol 2008, 132:131-144.
96. Chien V., Aitken J.F., Zhang S., Buchanan C.M., et al. The chaperone proteins HSP70, HSP40/DnaJ and GRP78/BiP suppress misfolding and formation of β-sheet-containing aggregates by human amylin: a potential role for defective chaperone biology in type 2 diabetes. Biochem. J. 2010, 432:113-121.
97. Peinado J.R., Sami F., Rajpurohit N., Lindberg I. Blockade of islet amyloid polypeptide fibrillation and cytotoxicity by the secretory chaperones 7B2 and proSAAS. FEBS Lett. 2013, 587:3406-3411.
98. Gidalevitz T., Ben-Zvi A., Ho K.H., Brignull H.R., et al. Progressive disruption of cellular protein folding in models of polyglutamine diseases. Science 2006, 311:1471-1474.
99. Feder M.E., Hofmann G.E. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu. Rev. Physiol. 1999, 61:243-282.
100. Morimoto R.I. The heat shock response: systems biology of proteotoxic stress in aging and disease. Cold Spring Harbor Symposia on Quantitative Biology 2011, vol. LXXVI:91-99.
101. Mejía R., Gómez-Eichelmann M.C., Fernández M.S. Membrane fluidity of Escherichia coli during heat-shock. Biochim. Biophys. Acta 1995, 1239:195-200.
102. Mejía R., Gómez-Eichelmann M.C., Fernández M.S. Fatty acid profile of Escherichia coli during the heat-shock response. Biochem. Mol. Biol. Int. 1999, 47:835-844. (1999).
103. Labbadia J., Morimoto R.I. Proteostasis and longevity: when does aging begin?. F1000 Prime Reports 2014, 6:7. 10.12703/P6-7.
104. Gidalevitz T., Kikis E.A., Morimoto R.I. A cellular perspective on conformational disease: the role of genetic background and proteostasis networks. Curr. Opin. Struct. Biol. 2010, 20:23-32.
105. Lindquist S.L., Kelly J.W. Chemical and biological approaches for adapting proteostasis to ameliorate protein misfolding and aggregation diseases-progress and prognosis. Cold Spring Harb. Perspect. Biol. 2011, 3:a004507.
106. Taylor R.C., Dillin A. Aging as an event of proteostasis collapse. Cold Spring Harb. Perspect. Biol. 2011, 3:a004440.
107. Whitesell L., Lindquist S. Inhibiting the transcription factor HSF1 as an anticancer strategy. Expert Opin. Ther. Targets 2009, 13:469-478.
108. Calderwood S.K., Khaleque M.A., Sawyer D.B., Ciocca D.R. Heat shock-proteins in cancer: chaperones of tumorigenesis. Trends Biochem. Sci. 2006, 31:164-172.