REVIEW PAPER
αB-crystallin as a promising target in pathological conditions – A review
1
Cancer Cell Biology Students Research Group, Medical University, Warsaw, Poland
2
Department of Cancer Prevention, Faculty of Health Sciences, Medical University, Warsaw, Poland
3
Department of Health Economics and Medical Law, Medical University, Warsaw, Poland
4
Department of Economic and System Analyses, National Institute of Public Health, Warsaw, Poland
Corresponding author
Ann Agric Environ Med. 2020;27(3):326-334
KEYWORDS
TOPICS
Prevention of occupational diseases in agriculture, forestry, food industry and wood industryState of the health of rural communities depending on various factors: social factors, accessibility of medical care, etc.
ABSTRACT
Introduction and objective:
αB-crystallin belongs to the ubiquitous family of small heat-shock proteins. It was discovered as a physiological protein of the eye lens, maintaining its liquid-like property. Furthermore, αB-crystallin was proved to playa bipolar role in both physiological and pathophysiological conditions. This review discusses current knowledge about the biology and genetics of αB-crystallin, and summarizes recent advances in understanding its role in ophthalmic and neurological disorders, as well as breast cancer, renal cancer and other malignancies.
State of knowledge:
α-crystallins are established as important elements of the protein quality control network, and consequently their defects are related to multiple human diseases. New studies highlight αB-crystallin’s involvement in proliferative diabetic retinopathy angiogenesis and point out its therapeutic potential in age-related macular degeneration. αB-crystallin is thought to be associated with the disease-causing protein aggregates, leading to its connection with such neurological disturbances as anaplastic astrocytoma, Parkinson disease, aging deficits in the peripheral nervous system and multiple sclerosis. In breast cancer, it was proven to be a marker of aggressive behaviur and cerebral metastases. Strong expression of αB-crystallin promoted growth and migration of clear cell renal cell carcinoma cells and was correlated with lower overall survival rate. Considering other malignancies, its various roles were established in colorectal and gastric cancers, head and neck squamous cell carcinomas and osteosarcomas.
Conclusions:
Further studies concerning αB-crystallin seem to be enormously promising, as they might improve our understanding of common human pathologies as well as contemporary diagnostics and treatment.
αB-crystallin belongs to the ubiquitous family of small heat-shock proteins. It was discovered as a physiological protein of the eye lens, maintaining its liquid-like property. Furthermore, αB-crystallin was proved to playa bipolar role in both physiological and pathophysiological conditions. This review discusses current knowledge about the biology and genetics of αB-crystallin, and summarizes recent advances in understanding its role in ophthalmic and neurological disorders, as well as breast cancer, renal cancer and other malignancies.
State of knowledge:
α-crystallins are established as important elements of the protein quality control network, and consequently their defects are related to multiple human diseases. New studies highlight αB-crystallin’s involvement in proliferative diabetic retinopathy angiogenesis and point out its therapeutic potential in age-related macular degeneration. αB-crystallin is thought to be associated with the disease-causing protein aggregates, leading to its connection with such neurological disturbances as anaplastic astrocytoma, Parkinson disease, aging deficits in the peripheral nervous system and multiple sclerosis. In breast cancer, it was proven to be a marker of aggressive behaviur and cerebral metastases. Strong expression of αB-crystallin promoted growth and migration of clear cell renal cell carcinoma cells and was correlated with lower overall survival rate. Considering other malignancies, its various roles were established in colorectal and gastric cancers, head and neck squamous cell carcinomas and osteosarcomas.
Conclusions:
Further studies concerning αB-crystallin seem to be enormously promising, as they might improve our understanding of common human pathologies as well as contemporary diagnostics and treatment.
REFERENCES (111)
1.
Boelens WC. Cell biological roles of αB-crystallin. Progress in Biophysics and Molecular Biology. 2017; 115(1): 3–10.
2.
Mymrikov EV, Daake M, Richter B, Haslbeck M, Buchner J. The Chaperone Activity and Substrate Spectrum of Human Small Heat Shock Proteins. J Biol Chem. 2017; 292(2): 672–684. https://doi.org/10.1074/jbc.M1....
3.
Bakthisaran R, Tangirala R, Rao Ch M. Small heat shock proteins: Role in cellular functions and pathology. Biochim Biophys Acta. 2015; 1854(4): 291–319. https://doi.org/10.1016/j.bbap....
4.
Kriehuber T, Rattei T, Weinmaier T, Bepperling A, Haslbeck M, Buchner J. Independent evolution of the core domain and its flanking sequences in small heat shock proteins. FASEB J. 2010; 24(10): 3633–3642. https://doi.org/10.1096/fj.10-....
5.
Basha E, O’Neill H, Vierling E. Small heat shock proteins and alpha-crystallins: dynamic proteins with flexible functions. Trends Biochem Sci. 2012; 37(3): 106–117. https://doi.org/10.1016/j.tibs....
6.
Liu Z, Wang C, Li Y, Zhao C, Li T, Li D, et al. Mechanistic insights into the switch of alphaB-crystallin chaperone activity and self-multimerization. J Biol Chem. 2018; 293(38): 14880–14890. https://doi.org/10.1074/jbc.RA....
7.
Dong Y, Dong Z, Kase S, Ando R, Fukuhara J, Kinoshita S, et al. Phosphorylation of alphaB-crystallin in epiretinal membrane of human proliferative diabetic retinopathy. Int J Ophthalmol. 2016; 9(8): 1100–1105. https://doi.org/10.18240/ijo.2....
8.
Liu Y, Zhang X, Luo L, Wu M, Zeng R, Cheng G, et al. A novel alphaB-crystallin mutation associated with autosomal dominant congenital lamellar cataract. Invest Ophthalmol Vis Sci. 2006; 47(3): 1069–1075. https://doi.org/10.1167/iovs.0....
9.
Koletsa T, Stavridi F, Bobos M, Kostopoulos I, Kotoula V, Eleftheraki AG, et al. alphaB-crystallin is a marker of aggressive breast cancer behavior but does not independently predict for patient outcome: a combined analysis of two randomized studies. BMC Clin Pathol. 2014; 14: 28. https://doi.org/10.1186/1472-6....
10.
Kase S, He S, Sonoda S, Kitamura M, Spee C, Wawrousek E, et al. alphaB-crystallin regulation of angiogenesis by modulation of VEGF. Blood. 2010; 115(16): 3398–3406. https://doi.org/10.1182/blood-....
11.
Ho PY, Chueh SC, Chiou SH, Wang SM, Lin WC, Lee IL, et al. AlphaB-crystallin in clear cell renal cell carcinoma: tumor progression and prognostic significance. Urol Oncol. 2013; 31(7): 1367–1377. https://doi.org/10.1016/j.urol....
12.
Kappe G, Leunissen JA, de Jong WW. Evolution and diversity of prokaryotic small heat shock proteins. Prog Mol Subcell Biol. 2002; 28: 1–17.
13.
Jehle S, Vollmar BS, Bardiaux B, Dove KK, Rajagopal P, Gonen T, et al. N-terminal domain of alphaB-crystallin provides a conformational switch for multimerization and structural heterogeneity. Proc Natl Acad Sci U S A. 2011; 108(16): 6409–6414. https://doi.org/10.1073/pnas.1....
14.
Braun N, Zacharias M, Peschek J, Kastenmuller A, Zou J, Hanzlik M, et al. Multiple molecular architectures of the eye lens chaperone alphaB-crystallin elucidated by a triple hybrid approach. Proc Natl Acad Sci U S A. 2011; 108(51): 20491–20496. https://doi.org/10.1073/pnas.1....
15.
Mainz A, Peschek J, Stavropoulou M, Back KC, Bardiaux B, Asami S, et al. The chaperone alphaB-crystallin uses different interfaces to capture an amorphous and an amyloid client. Nat Struct Mol Biol. 2015; 22(11): 898–905. https://doi.org/10.1038/nsmb.3....
16.
Mymrikov EV, Seit-Nebi AS, Gusev NB. Large potentials of small heat shock proteins. Physiol Rev. 2011; 91(4): 1123–1159. https://doi.org/10.1152/physre....
17.
Peschek J, Braun N, Rohrberg J, Back KC, Kriehuber T, Kastenmuller A, et al. Regulated structural transitions unleash the chaperone activity of alphaB-crystallin. Proc Natl Acad Sci U S A. 2013; 110(40): E3780–3789. https://doi.org/10.1073/pnas.1....
18.
Carra S, Rusmini P, Crippa V, Giorgetti E, Boncoraglio A, Cristofani R, et al. Different anti-aggregation and pro-degradative functions of the members of the mammalian sHSP family in neurological disorders. Philos Trans R Soc Lond B Biol Sci. 2013; 368(1617): 20110409. https://doi.org/10.1098/rstb.2....
19.
D’Agostino M, Lemma V, Chesi G, Stornaiuolo M, Cannata Serio M, D’Ambrosio C, et al. The cytosolic chaperone alpha-crystallin B rescues folding and compartmentalization of misfolded multispan transmembrane proteins. J Cell Sci. 2013; 126(Pt 18): 4160–4172. https://doi.org/10.1242/jcs.12....
20.
Ciano M, Allocca S, Ciardulli MC, Della Volpe L, Bonatti S, D’Agostino M. Differential phosphorylation-based regulation of alphaB-crystallin chaperone activity for multipass transmembrane proteins. Biochem Biophys Res Commun. 2016; 479(2): 325–330. https://doi.org/10.1016/j.bbrc....
21.
Huang Y, Wang Z, Liu Y, Xiong H, Zhao Y, Wu L, et al. alphaB-Crystallin Interacts with Nav1.5 and Regulates Ubiquitination and Internalization of Cell Surface Nav1.5. J Biol Chem. 2016; 291(21): 11030–11041. https://doi.org/10.1074/jbc.M1....
22.
Mao YW, Liu YP, Xiang H, Li WC. Human αA- and αB-crystallins bind to Bax and Bcl-XS to sequester their translocation during staurosporine-induced apoptosis. Cell Death & Differentiation 2004; 11: 512–526.
23.
Ngo JT, Klisak I, Dubin RA, Piatigorsky J, Mohandas T, Sparkes RS, et al. Assignment of the alpha B-crystallin gene to human chromosome 11. Genomics. 1989; 5(4): 665–669.
24.
Wistow G. The human crystallin gene families. Hum Genomics. 2012; 6: 26. https://doi.org/10.1186/1479-7....
25.
Dubin RA, Gopal-Srivastava R, Wawrousek EF, Piatigorsky J. Expression of the murine alpha B-crystallin gene in lens and skeletal muscle: identification of a muscle-preferred enhancer. Mol Cell Biol. 1991; 11(9): 4340–4349.
26.
Srinivasan AN, Bhat SP. Complete structure and expression of the rat alpha B-crystallin gene. DNA Cell Biol. 1994; 13(6): 651–661. https://doi.org/10.1089/dna.19....
27.
Jing Z, Gangalum RK, Lee JZ, Mock D, Bhat SP. Cell-type-dependent access of HSF1 and HSF4 to αB-crystallin promoter during heat shock. Cell Stress Chaperones. 2013; 18(3): 377–387. https://doi.org/10.1007/s12192....
28.
Sadamitsu C, Nagano T, Fukumaki Y, Iwaki A. Heat shock factor 2 is involved in the upregulation of alphaB-crystallin by high extracellular potassium. Journal of biochemistry. 2001; 129(5): 813–820.
29.
Jing Z, Gangalum RK, Mock DC, Bhat SP. A gene-specific non-enhancer sequence is critical for expression from the promoter of the small heat shock protein gene alphaB-crystallin. Hum Genomics. 2014; 8: 5. https://doi.org/10.1186/1479-7....
30.
Gopal-Srivastava R, Piatigorsky J. Identification of a lens-specific regulatory region (LSR) of the murine alpha B-crystallin gene. Nucleic Acids Res. 1994; 22(7): 1281–1286.
31.
Gopal-Srivastava R, Cvekl A, Piatigorsky J. Pax-6 and alphaB-crystallin/small heat shock protein gene regulation in the murine lens. Interaction with the lens-specific regions, LSR1 and LSR2. J Biol Chem. 1996; 271(38): 23029–23036.
32.
Chauhan BK, Yang Y, Cveklová K, Cvekl A. Functional interactions between alternatively spliced forms of Pax6 in crystallin gene regulation and in haploinsufficiency. Nucleic Acids Res. 2004; 32(5): 1696–1709. https://doi.org/10.1093/nar/gk....
33.
Gopal-Srivastava R, Cvekl A, Piatigorsky J. Involvement of retinoic acid/retinoid receptors in the regulation of murine alphaB-crystallin/small heat shock protein gene expression in the lens. J Biol Chem. 1998; 273(28): 17954–17961.
34.
Gopal-Srivastava R, Kays WT, Piatigorsky J. Enhancer-independent promoter activity of the mouse αB-crystallin/small heat shock protein gene in the lens and cornea of transgenic mice. Mechanisms of Developement. 2000; 92: 125–134.
35.
Gopal-Srivastava R, Piatigorsky J. The murine alpha B-crystallin/small heat shock protein enhancer: identification of alpha BE-1, alpha BE-2, alpha BE-3, and MRF control elements. Mol Cell Biol. 1993; 13(11): 7144–7152.
36.
Liu S, Piatigorsky J. Regulation of mouse small heat shock protein αb-crystallin gene by aryl hydrocarbon receptor. PLoS One. 2011; 6(4): e17904. https://doi.org/10.1371/journa....
37.
Gopal-Srivastava R, Haynes JI, 2nd, Piatigorsky J. Regulation of the murine alpha B-crystallin/small heat shock protein gene in cardiac muscle. Mol Cell Biol. 1995; 15(12): 7081–7090.
38.
Xiao X, Benjamin IJ. Stress-response proteins in cardiovascular disease. Am J Hum Genet. 1999; 64(3): 685–690. https://doi.org/10.1086/302305.
39.
Manukyan I, Galatioto J, Mascareno E, Bhaduri S, Siddiqui MA. Cross-talk between calcineurin/NFAT and Jak/STAT signalling induces cardioprotective alphaB-crystallin gene expression in response to hypertrophic stimuli. J Cell Mol Med. 2010; 14(6B): 1707–1716. https://doi.org/10.1111/j.1582....
40.
Chen Q, Ma J, Yan M, Mothobi ME, Liu Y, Zheng F. A novel mutation in CRYAB associated with autosomal dominant congenital nuclear cataract in a Chinese family. Mol Vis. 2009; 15: 1359–1365.
41.
Jiao X, Khan SY, Irum B, Khan AO, Wang Q, Kabir F, et al. Missense Mutations in CRYAB Are Liable for Recessive Congenital Cataracts. PloS one. 2015; 10(9): e0137973. https://doi.org/10.1371/journa....
42.
Xia XY, Wu QY, An LM, Li WW, Li N, Li TF, et al. A novel P20R mutation in the alpha-B crystallin gene causes autosomal dominant congenital posterior polar cataracts in a Chinese family. BMC Ophthalmol. 2014; 14: 108. https://doi.org/10.1186/1471-2....
43.
Li H, Li C, Lu Q, Su T, Ke T, Li DW, et al. Cataract mutation P20S of alphaB-crystallin impairs chaperone activity of alphaA-crystallin and induces apoptosis of human lens epithelial cells. Biochim Biophys Acta. 2008; 1782(5): 303–309. https://doi.org/10.1016/j.bbad....
44.
Del Bigio MR, Chudley AE, Sarnat HB, Campbell C, Goobie S, Chodirker BN, et al. Infantile muscular dystrophy in Canadian aboriginals is an alphaB-crystallinopathy. Ann Neurol. 2011; 69(5): 866–871. https://doi.org/10.1002/ana.22....
45.
Safieh LA, Khan AO, Alkuraya FS. Identification of a novel CRYAB mutation associated with autosomal recessive juvenile cataract in a Saudi family. Mol Vis. 2009; 15: 980–984.
46.
Khan AO, Abu Safieh L, Alkuraya FS. Later retinal degeneration following childhood surgical aphakia in a family with recessive CRYAB mutation (p.R56W). Ophthalmic Genet. 2010; 31(1): 30–36. https://doi.org/10.3109/138168....
47.
Sun W, Xiao X, Li S, Guo X, Zhang Q. Mutation analysis of 12 genes in Chinese families with congenital cataracts. Mol Vis. 2011; 17: 2197–2206.
48.
Sacconi S, Feasson L, Antoine JC, Pecheux C, Bernard R, Cobo AM, et al. A novel CRYAB mutation resulting in multisystemic disease. Neuromuscul Disord. 2012; 22(1): 66–72. https://doi.org/10.1016/j.nmd.....
49.
Fichna JP, Potulska-Chromik A, Miszta P, Redowicz MJ, Kaminska AM, Zekanowski C, et al. A novel dominant D109A CRYAB mutation in a family with myofibrillar myopathy affects alphaB-crystallin structure. BBA Clin. 2017; 7: 1–7. https://doi.org/10.1016/j.bbac....
50.
Brodehl A, Gaertner-Rommel A, Klauke B, Grewe SA, Schirmer I, Peterschroder A, et al. The novel alphaB-crystallin (CRYAB) mutation p.D109G causes restrictive cardiomyopathy. Hum Mutat. 2017; 38(8): 947–952. https://doi.org/10.1002/humu.2....
51.
Forrest KM, Al-Sarraj S, Sewry C, Buk S, Tan SV, Pitt M, et al. Infantile onset myofibrillar myopathy due to recessive CRYAB mutations. Neuromuscul Disord. 2011; 21(1): 37–40. https://doi.org/10.1016/j.nmd.....
52.
Vicart P, Caron A, Guicheney P, Li Z, Prevost MC, Faure A, et al. A missense mutation in the alphaB-crystallin chaperone gene causes a desmin-related myopathy. Nat Genet. 1998; 20(1): 92–95. 10.1038/1765.
53.
Berry V, Francis P, Reddy MA, Collyer D, Vithana E, MacKay I, et al. Alpha-B crystallin gene (CRYAB) mutation causes dominant congenital posterior polar cataract in humans. Am J Hum Genet. 2001; 69(5): 1141–1145. https://doi.org/10.1086/324158.
54.
Selcen D, Engel AG. Myofibrillar myopathy caused by novel dominant negative alpha B-crystallin mutations. Ann Neurol. 2003; 54(6): 804–810. https://doi.org/10.1002/ana.10....
55.
Pilotto A, Marziliano N, Pasotti M, Grasso M, Costante AM, Arbustini E. alphaB-crystallin mutation in dilated cardiomyopathies: low prevalence in a consecutive series of 200 unrelated probands. Biochem Biophys Res Commun. 2006; 346(4): 1115–1117. https://doi.org/10.1016/j.bbrc....
56.
Reilich P, Schoser B, Schramm N, Krause S, Schessl J, Kress W, et al. The p.G154S mutation of the alpha-B crystallin gene (CRYAB) causes late-onset distal myopathy. Neuromuscul Disord. 2010; 20(4): 255–259. https://doi.org/10.1016/j.nmd.....
57.
Inagaki N, Hayashi T, Arimura T, Koga Y, Takahashi M, Shibata H, et al. Alpha B-crystallin mutation in dilated cardiomyopathy. Biochem Biophys Res Commun. 2006; 342(2): 379–386. https://doi.org/10.1016/j.bbrc....
58.
Devi RR, Yao W, Vijayalakshmi P, Sergeev YV, Sundaresan P, Hejtmancik JF. Crystallin gene mutations in Indian families with inherited pediatric cataract. Mol Vis. 2008; 14: 1157–1170.
59.
van der Smagt JJ, Vink A, Kirkels JH, Nelen M, ter Heide H, Molenschot MM, et al. Congenital posterior pole cataract and adult onset dilating cardiomyopathy: expanding the phenotype of alphaB-crystallinopathies. Clin Genet. 2014; 85(4): 381–385. https://doi.org/10.1111/cge.12....
60.
Wistow GJ, Piatigorsky J. Lens crystallins: the evolution and expression of proteins for a highly specialized tissue. Annu Rev Biochem. 1988; 57: 479–504. 10.1146/annurev.bi.57.070188.002403.
61.
Clark JI. Functional sequences in human alphaB crystallin. Biochim Biophys Acta. 2016; 1860(1 Pt B): 240–245. https://doi.org/10.1016/j.bbag....
62.
Gangalum RK, Bhat SP. AlphaB-crystallin: a Golgi-associated membrane protein in the developing ocular lens. Invest Ophthalmol Vis Sci. 2009; 50(7): 3283–3290. https://doi.org/10.1167/iovs.0....
63.
Gangalum RK, Schibler MJ, Bhat SP. Small heat shock protein alphaB-crystallin is part of cell cycle-dependent Golgi reorganization. J Biol Chem. 2004; 279(42): 43374–43377. https://doi.org/10.1074/jbc.C4....
64.
Dong Z, Kase S, Ando R, Fukuhara J, Saito W, Kanda A, et al. Alphab-crystallin expression in epiretinal membrane of human proliferative diabetic retinopathy. Retina. 2012; 32(6): 1190–1196. https://doi.org/10.1097/IAE.0b....
65.
Chen W, Lu Q, Lu L, Guan H. Increased levels of alphaB-crystallin in vitreous fluid of patients with proliferative diabetic retinopathy and correlation with vascular endothelial growth factor. Clin Exp Ophthalmol. 2017; 45(4): 379–384. https://doi.org/10.1111/ceo.12....
66.
Yang J, Zhou S, Guo M, Li Y, Gu J. Different alpha crystallin expression in human age-related and congenital cataract lens epithelium. BMC Ophthalmol. 2016; 16: 67. 10.1186/s12886-016-0241-1.
67.
Javadiyan S, Craig JE, Souzeau E, Sharma S, Lower KM, Pater J, et al. Recurrent mutation in the crystallin alpha A gene associated with inherited paediatric cataract. BMC Res Notes. 2016; 9: 83. https://doi.org/10.1186/s13104....
68.
Song Z, Si N, Xiao W. A novel mutation in the CRYAA gene associated with congenital cataract and microphthalmia in a Chinese family. BMC Med Genet. 2018; 19(1): 190. https://doi.org/gr10.1186/s128....
69.
Kannan R, Sreekumar PG, Hinton DR. Alpha crystallins in the retinal pigment epithelium and implications for the pathogenesis and treatment of age-related macular degeneration. Biochim Biophys Acta. 2016; 1860(1 Pt B): 258–268. https://doi.org/10.1016/j.bbag....
70.
Cai J, Zhang H, Zhang YF, Zhou Z, Wu S. MicroRNA-29 enhances autophagy and cleanses exogenous mutant αB-crystallin in retinal pigment epithelial cells. Experimental Cell Research. 2019; 374(1): 231–248.
71.
Golenhofen N, Bartelt-Kirbach B. HspB5/αB-Crystallin in the Brain. In: Tanguay R, Hightower L, editors. The Big Book on Small Heat Shock Proteins. 8: Springer; 2015.
72.
Avliyakulov NK, Rajavel KS, Le KM, Guo L, Mirsadraei L, Yong WH, et al. C-terminally truncated form of alphaB-crystallin is associated with IDH1 R132H mutation in anaplastic astrocytoma. J Neurooncol. 2014; 117(1): 53–65. https://doi.org/10.1007/s11060....
73.
Liu Y, Zhou Q, Tang M, Fu N, Shao W, Zhang S, et al. Upregulation of alphaB-crystallin expression in the substantia nigra of patients with Parkinson’s disease. Neurobiol Aging. 2015; 36(4): 1686–1691. https://doi.org/10.1016/j.neur....
74.
Lim EF, Musa A, Frederick A, Ousman SS. AlphaB-crystallin expression correlates with aging deficits in the peripheral nervous system. Neurobiol Aging. 2017; 53: 138–149. https://doi.org/10.1016/j.neur....
75.
Cwiklinska H, Mycko MP, Luvsannorov O, Walkowiak B, Brosnan CF, Raine CS, et al. Heat shock protein 70 associations with myelin basic protein and proteolipid protein in multiple sclerosis brains. Int Immunol. 2003; 15(2): 241–249.
76.
Iwaki T, Wisniewski T, Iwaki A, Corbin E, Tomokane N, Tateishi J, et al. Accumulation of alpha B-crystallin in central nervous system glia and neurons in pathologic conditions. Am J Pathol. 1992; 140(2): 345–356.
77.
Ma CH, Omura T, Cobos EJ, Latremoliere A, Ghasemlou N, Brenner GJ, et al. Accelerating axonal growth promotes motor recovery after peripheral nerve injury in mice. J Clin Invest. 2011; 121(11): 4332–4347. https://doi.org/10.1172/JCI586....
78.
Lim EF, Nakanishi ST, Hoghooghi V, Eaton SE, Palmer AL, Frederick A, et al. AlphaB-crystallin regulates remyelination after peripheral nerve injury. Proc Natl Acad Sci U S A. 2017; 114(9): E1707-E1716. https://doi.org/10.1073/pnas.1....
79.
Bsibsi M, Peferoen LA, Holtman IR, Nacken PJ, Gerritsen WH, Witte ME, et al. Demyelination during multiple sclerosis is associated with combined activation of microglia/macrophages by IFN-gamma and alpha B-crystallin. Acta Neuropathol. 2014; 128(2): 215–229. https://doi.org/10.1007/s00401....
80.
van Noort JM, Bsibsi M, Nacken PJ, Verbeek R, Venneker EH. Therapeutic Intervention in Multiple Sclerosis with Alpha B-Crystallin: A Randomized Controlled Phase IIa Trial. PLoS One. 2015; 10(11): e0143366. https://doi.org/10.1371/journa....
81.
Moyano JV, Evans JR, Chen F, Lu M, Werner ME, Yehiely F, et al. AlphaB-crystallin is a novel oncoprotein that predicts poor clinical outcome in breast cancer. J Clin Invest. 2006; 116(1): 261–270. https://doi.org/10.1172/JCI258....
82.
Tsang JY, Lai MW, Wong KH, Chan SK, Lam CC, Tsang AK, et al. alphaB-crystallin is a useful marker for triple negative and basal breast cancers. Histopathology. 2012; 61(3): 378–386. https://doi.org/10.1111/j.1365....
83.
Chan SK, Lui PC, Tan PH, Yamaguchi R, Moriya T, Yu AM, et al. Increased alpha-B-crystallin expression in mammary metaplastic carcinomas. Histopathology. 2011; 59(2): 247–255. https://doi.org/10.1111/j.1365....
84.
Kim MS, Lee HW, Jun SY, Lee EH. Expression of alpha B crystallin and BCL2 in patients with infiltrating ductal carcinoma. Int J Clin Exp Pathol. 2015; 8(8): 8842–8856.
85.
Kabbage M, Trimeche M, Ben Nasr H, Hammann P, Kuhn L, Hamrita B, et al. Expression of the molecular chaperone alphaB-crystallin in infiltrating ductal breast carcinomas and the significance thereof: an immunohistochemical and proteomics-based strategy. Tumour Biol. 2012; 33(6): 2279–2288. https://doi.org/10.1007/s13277....
86.
Chen Z, Ruan Q, Han S, Xi L, Jiang W, Jiang H, et al. Discovery of structure-based small molecular inhibitor of alphaB-crystallin against basal-like/triple-negative breast cancer development in vitro and in vivo. Breast Cancer Res Treat. 2014; 145(1): 45–59. https://doi.org/10.1007/s10549....
87.
Chelouche-Lev D, Kluger HM, Berger AJ, Rimm DL, Price JE. alphaB-crystallin as a marker of lymph node involvement in breast carcinoma. Cancer. 2004; 100(12): 2543–2548. https://doi.org/10.1002/cncr.2....
88.
Malin D, Strekalova E, Petrovic V, Deal AM, Al Ahmad A, Adamo B, et al. alphaB-crystallin: a novel regulator of breast cancer metastasis to the brain. Clin Cancer Res. 2014; 20(1): 56–67. https://doi.org/10.1158/1078-0....
89.
Voduc KD, Nielsen TO, Perou CM, Harrell JC, Fan C, Kennecke H, et al. alphaB-crystallin Expression in Breast Cancer is Associated with Brain Metastasis. NPJ Breast Cancer. 2015; 1. https://doi.org/10.1038/npjbca....
90.
Michl M, Ouyang N, Fraek ML, Beck FX, Neuhofer W. Expression and regulation of alphaB-crystallin in the kidney in vivo and in vitro. Pflugers Arch. 2006; 452(4): 387–395. https://doi.org/10.1007/s00424....
91.
Kim MS, Lee HW, Lee EH. Renal tumor with alpha B crystallin expression. Int J Clin Exp Pathol. 2015; 8(8): 9383–9389.
92.
Dasgupta S, Hohman TC, Carper D. Hypertonic stress induces alpha B-crystallin expression. Exp Eye Res. 1992; 54(3): 461–470.
93.
Canales L, Chen J, Kelty E, Musah S, Webb C, Pisano MM, et al. Developmental cigarette smoke exposure: liver proteome profile alterations in low birth weight pups. Toxicology. 2012; 300(1–2): 1–11. https://doi.org/10.1016/j.tox.....
94.
Lou Q, Hu Y, Ma Y, Dong Z. Heat shock factor 1 induces crystallin-alphaB to protect against cisplatin nephrotoxicity. Am J Physiol Renal Physiol. 2016; 311(1): F94-F102. https: //doi.org/10.1152/ajprenal.00201.2016.
95.
Shi T, Dong F, Liou LS, Duan ZH, Novick AC, DiDonato JA. Differential protein profiling in renal-cell carcinoma. Mol Carcinog. 2004; 40(1): 47–61. https://doi.org/10.1002/mc.200....
96.
Thedieck C, Kalbacher H, Kratzer U, Lammers R, Stevanovic S, Klein G. alpha B-crystallin is a cytoplasmic interaction partner of the kidney-specific cadherin-16. J Mol Biol. 2008; 378(1): 145–153. https://doi.org/10.1016/j.jmb.....
97.
Horstmann M, Geiger LM, Vogel U, Schmid H, Hennenlotter J, Kuehs U, et al. Kidney-specific cadherin correlates with the ontogenetic origin of renal cell carcinoma subtypes: an indicator of a malignant potential? World J Urol. 2012; 30(4): 525–531. https://doi.org/10.1007/s00345....
98.
Shi C, He Z, Hou N, Ni Y, Xiong L, Chen P. Alpha B-crystallin correlates with poor survival in colorectal cancer. Int J Clin Exp Pathol. 2014; 7(9): 6056–6063.
99.
Shi C, Yang X, Bu X, Hou N, Chen P. Alpha B-crystallin promotes the invasion and metastasis of colorectal cancer via epithelial-mesenchymal transition. Biochem Biophys Res Commun. 2017; 489(4): 369–374. https://doi.org/10.1016/j.bbrc....
100.
Li Q, Wang Y, Lai Y, Xu P, Yang Z. HspB5 correlates with poor prognosis in colorectal cancer and prompts epithelial-mesenchymal transition through ERK signaling. PLoS One. 2017; 12(8): e0182588. https://doi.org/10.1371/journa....
101.
Wu X, Zheng YZ, Han B, Wang K. Alpha B-crystallin C-802G polymorphism and colorectal cancer susceptibility and clinical outcome in Chinese population. Sci Rep. 2018; 8(1): 11731. https://doi.org/10.1038/s41598....
102.
Shi QM, Luo J, Wu K, Yin M, Gu YR, Cheng XG. High level of αB-crystallin contributes to the progression of osteosarcoma. Oncotarget. 2016; 7(8): 9007–9016. https://doi.org/10.18632/oncot....
103.
Wang SN, Luo S, Liu C, Piao Z, Gou W, Wang Y, et al. miR-491 Inhibits Osteosarcoma Lung Metastasis and Chemoresistance by Targeting αB-crystallin. Molecular therapy: the journal of the American Society of Gene Therapy. 2017; 25(9): 2140–2149. https://doi.org/10.1016/j.ymth....
104.
Chen D, Cao G, Qiao C, Liu G, Zhou H, Liu Q. Alpha B-crystallin promotes the invasion and metastasis of gastric cancer via NF-κB-induced epithelial-mesenchymal transition. J Cell Mol Med. 2018; 22(6): 3215–3222. https://doi.org/10.1111/jcmm.1....
105.
Annertz K, Enoksson J, Williams R, Jacobsson H, Coman WB, Wennerberg J. Alpha B-crystallin – a validated prognostic factor for poor prognosis in squamous cell carcinoma of the oral cavity. Acta Otolaryngol. 2014; 134(5): 543–550. https://doi.org/10.3109/000164....
106.
Yilmaz M, Karatas OF, Yuceturk B, Dag H, Yener M, Ozen M. Alpha-B-crystallin expression in human laryngeal squamous cell carcinoma tissues. Head Neck. 2015; 37(9): 1344–1348. https://doi.org/10.1002/hed.23....
107.
van de Schootbrugge C, Schults EM, Bussink J, Span PN, Grenman R, Pruijn GJ, et al. Effect of hypoxia on the expression of alphaB-crystallin in head and neck squamous cell carcinoma. BMC Cancer. 2014; 14: 252. https://doi.org/10.1186/1471-2....
108.
Cherneva R, Petrov D, Georgiev O, Slavova Y, Toncheva D, Stamenova M, et al. Expression profile of the small heat-shock protein alpha-B-crystallin in operated-on non-small-cell lung cancer patients: clinical implication. Eur J Cardiothorac Surg. 2010; 37(1): 44–50. https://doi.org/10.1016/j.ejct....
109.
Campbell-Lloyd AJ, Mundy J, Deva R, Lampe G, Hawley C, Boyle G, et al. Is alpha-B crystallin an independent marker for prognosis in lung cancer? Heart Lung Circ. 2013; 22(9): 759–766. https://doi.org/10.1016/j.hlc.....
110.
Volkmann J, Reuning U, Rudelius M, Hafner N, Schuster T, Becker VRA, et al. High expression of crystallin alphaB represents an independent molecular marker for unfavourable ovarian cancer patient outcome and impairs TRAIL- and cisplatin-induced apoptosis in human ovarian cancer cells. Int J Cancer. 2013; 132(12): 2820–2832. https://doi.org/10.1002/ijc.27....
111.
Tang Q, Liu YF, Zhu XJ, Li YH, Zhu J, Zhang JP, et al. Expression and prognostic significance of the alpha B-crystallin gene in human hepatocellular carcinoma. Hum Pathol. 2009; 40(3): 300–305. https://doi.org/10.1016/j.hump....
Share
RELATED ARTICLE
| eISSN: | 1898-2263 |
| ISSN: | 1232-1966 |
Improvement of visual identification of the journal - task financed under the agreement No. 618/P-DUN/2019 by the Minister of Science and Higher Education allocated to the activities of disseminating science.
Generation of the DOI (Digital Object Identifier) - task financed under the agreement No. 618/P-DUN/2019 by the Minister of Science and Higher
© 2006-2024 Journal hosting platform by Bentus
We process personal data collected when visiting the website. The function of obtaining information about users and their behavior is carried out by voluntarily entered information in forms and saving cookies in end devices. Data, including cookies, are used to provide services, improve the user experience and to analyze the traffic in accordance with the Privacy policy. Data are also collected and processed by Google Analytics tool (more).
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.
