The human 343delT HSPB5 Chaperone associated with early-onset skeletal myopathy causes defects in protein solubility

Journal of Biological Chemistry

Volumn 291, Issue 29, 2016, Pages 14939-14953

  Mitzelfelt, Katie A ^a   Limphong, Pattraranee ^b   Choi, Melinda J ^c   Kondrat, Frances D L ^d   Lai, Shuping ^c   Kolander, Kurt D ^c   Kwok, Wai Meng ^c   Dai, Qiang ^c   Grzybowski, Michael N ^c   Zhang, Huali ^e   Taylor, Graydon M ^a   Lui, Qiang ^a   Thao, Mai T ^c   Hudson, Judith A ^f   Barresi, Rita ^g   Bushby, Kate ^h   Jungbluth, Heinz ^i,j,k   Wraige, Elizabeth ⁱ   Geurts, Aron M ^c   Benesch, Justin L P ^d   Riedel, Michael ^l   Christians, Elisabeth S ^m   Minella, Alex C ⁿ   Benjamina, Ivor J ^a,c   more..

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b Arcturus   (United States)

^c MEDICAL COLLEGE OF WISCONSIN   (United States)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e Central South University   (China)

^f NEWCASTLE UPON TYNE HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

^g NEWCASTLE DENTAL HOSPITAL   (United Kingdom)

^h NEWCASTLE UNIVERSITY   (United Kingdom)

ⁱ EVELINA LONDON CHILDREN S HOSPITAL   (United Kingdom)

^j KING'S COLLEGE LONDON   (United Kingdom)

^k KING'S COLLEGE LONDON   (United Kingdom)

^l Pharmacell   (Netherlands)

^m SORBONNE UNIVERSITÉ   (France)

ⁿ BLOOD RESEARCH INSTITUTE   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELLS; CYTOLOGY; GENE EXPRESSION; GENES; SOLUBILITY; STEM CELLS;

CELLULAR STRESS RESPONSE; FUNCTION MODELING; HEAT SHOCK PROTEIN; INDUCED PLURIPOTENT STEM CELLS; MOLECULAR CHAPERONES; PLURIPOTENT STEM CELLS; PROTEIN DYNAMICS; PROTEIN SOLUBILITY;

PROTEINS;

CHAPERONE; HSPB5 PROTEIN; MUTANT PROTEIN; UNCLASSIFIED DRUG; ALPHA CRYSTALLIN; CRYAB PROTEIN, HUMAN; MESSENGER RNA; RECOMBINANT PROTEIN;

ARTICLE; BHK21 CELL LINE; CARDIAC MUSCLE CELL; CASE REPORT; CELL CULTURE; CELL LINE; CELL STRESS; CHILD; CONTROLLED STUDY; FEMALE; GAIN OF FUNCTION MUTATION; GENE; GENE DELETION; GENE EXPRESSION; GENE OVEREXPRESSION; HOMOZYGOTE; HSPB5 GENE; HUMAN; HUMAN CELL; IN VITRO STUDY; INFANT; LOSS OF FUNCTION MUTATION; MALE; MYOPATHY; MYOTUBE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SOLUBILITY; RECESSIVE INHERITANCE; SKELETAL MYOPATHY; SOLUBILITY; WT KI GENE; BIOLOGICAL MODEL; CARDIOMYOPATHIES; CATARACT; CHEMISTRY; GENETICS; INDUCED PLURIPOTENT STEM CELL; METABOLISM; MUSCULAR DISEASES; PEDIGREE; PROTEINOSIS; SKELETAL MUSCLE CELL;

ALPHA-CRYSTALLIN B CHAIN; CARDIOMYOPATHIES; CATARACT; FEMALE; HOMOZYGOTE; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MALE; MODELS, BIOLOGICAL; MUSCLE FIBERS, SKELETAL; MUSCULAR DISEASES; MUTANT PROTEINS; MYOCYTES, CARDIAC; PEDIGREE; PROTEIN AGGREGATION, PATHOLOGICAL; RECOMBINANT PROTEINS; RNA, MESSENGER; SEQUENCE DELETION; SOLUBILITY;

EID: 84978431927     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.730481     Document Type: Article

References (49)

1. Morimoto, R. I. (1998) Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev. 12, 3788-3796
2. Christians, E. S., Yan, L. J., and Benjamin, I. J. (2002) Heat shock factor 1 and heat shock proteins: critical partners in protection against acute cell injury. Crit. Care Med. 30, S43-S50
3. Gopal-Srivastava, R., and Piatigorsky, J. (1993) The murine α B-crystallin/ small heat shock protein enhancer: identification of BE-1, α BE-2, α BE-3 and MRF control elements. Mol. Cell. Biol. 13, 7144-7152
4. Gopal-Srivastava, R., Haynes, J. I., 2nd, and Piatigorsky, J. (1995) Regulation of the murine aB-crystallin/small heath shock protein gene in cardiac muscle. Mol. Cell. Biol. 15, 7081-7090
5. Poulain, P., Gelly, J. C., and Flatters, D. (2010) Detection and architecture of small heat shock protein monomers. PLoS ONE 5, e9990
6. Hochberg, G. K., and Benesch, J. L. (2014) Dynamical structure of ôBcrystallin. Prog. Biophys. Mol. Biol. 115, 11-20
7. Hochberg, G. K., Ecroyd, H., Liu, C., Cox, D., Cascio, D., Sawaya, M. R., Collier, M. P., Stroud, J., Carver, J. A., Baldwin, A. J., Robinson, C. V., Eisenberg, D. S., Benesch, J. L., and Laganowsky, A. (2014) The structured core domain of αB-crystallin can prevent amyloid fibrillation and associated toxicity. Proc. Natl. Acad. Sci. U.S.A. 111, E1562-1570
8. Peschek, J., Braun, N., Rohrberg, J., Back, K. C., Kriehuber, T., Kastenmüller, A., Weinkauf, S., and Buchner, J. (2013) Regulated structural transitions unleash the chaperone activity of αB-crystallin. Proc. Natl. Acad. Sci. U.S.A. 110, E3780-E3789
9. Rajagopal, P., Tse, E., Borst, A. J., Delbecq, S. P., Shi, L., Southworth, D. R., and Klevit, R. E. (2015) A conserved histidine modulates HSPB5 structure to trigger chaperone activity in response to stress-related acidosis. eLife 4, 1-21
10. Clark, A. R., Naylor, C. E., Bagnéris, C., Keep, N. H., and Slingsby, C. (2011) Crystal structure of R120G disease mutant of human αB-crystallin domain dimer shows closure of a groove. J. Mol. Biol. 408, 118-134
11. Mainz, A., Peschek, J., Stavropoulou, M., Back, K. C., Bardiaux, B., Asami, S., Prade, E., Peters, C., Weinkauf, S., Buchner, J., and Reif, B. (2015) The chaperone αB-crystallin uses different interfaces to capture an amorphous and an amyloid client. Nat. Struct. Mol. Biol. 22, 898-905
12. Houck, S. A., Landsbury, A., Clark, J. I., and Quinlan, R. A. (2011) Multiple sites in αB-crystallin modulate its interaction with desmin filaments assembled in vitro. PLoS ONE 6, e25859
13. Perng, M. D., Cairns, L., van den Ijssel, P., Prescott, A., Hutcheson, A. M., and Quinlan, R. A. (1999) Intermediate filament interactions can be altered by HSP27 and αB-crystallin. J. Cell Sci. 112, 2099-2112
14. Bennardini, F., Wrzosek, A., and Chiesi, M. (1992) α B-crystallin in cardiac tissue: association with actin and desmin filaments. Circ. Res. 71, 288-294
15. Bullard, B., Ferguson, C., Minajeva, A., Leake, M. C., Gautel, M., Labeit, D., Ding, L., Labeit, S., Horwitz, J., Leonard, K. R., and Linke, W. A. (2004) Association of the chaperone αB-crystallin with titin in heart muscle. J. Biol. Chem. 279, 7917-7924
16. Golenhofen, N., Arbeiter, A., Koob, R., and Drenckhahn, D. (2002) Ischemia-induced association of the stress protein α B-crystallin with I-band portion of cardiac titin. J. Mol. Cell. Cardiol. 34, 309-319
17. Golenhofen, N., Perng, M. D., Quinlan, R. A., and Drenckhahn, D. (2004) Comparison of the small heat shock proteins α B-crystallin, MKBP, HSP25, HSP20, and cvHSP in heart and skeletal muscle. Histochem. Cell Biol. 122, 415- 425
18. Kötter, S., Unger, A., Hamdani, N., Lang, P., Vorgerd, M., Nagel-Steger, L., and Linke, W. A. (2014) Human myocytes are protected from titin aggregation-induced stiffening by small heat shock proteins. J. Cell Biol. 204, 187-202
19. Singh, B. N., Rao, K. S., Ramakrishna, T., Rangaraj, N., and Rao, C. M. (2007) Association of α B-crystallin, a small heat shock protein, with actin: role in modulating actin filament dynamics in vivo. J. Mol. Biol. 366, 756-767
20. Brady, J. P., Garland, D. L., Green, D. E., Tamm, E. R., Giblin, F. J., and Wawrousek, E. F. (2001) aB-Crystallin in Lens development and muscle integrity: a gene knockout approach. Invest. Ophthalmol. Vis. Sci. 42, 2924-2934
21. Morrison, L. E., Whittaker, R. J., Klepper, R. E., Wawrousek, E. F., and Glembotski, C. C. (2004) Roles for α B-crystallin and HSPB2 in protecting the myocardium from ischemia-reperfusion-induced damage in a KO mouse model. Am. J. Physiol. Heart Circ. Physiol. 286, H847-H855
22. Kumarapeli, A. R., Su, H., Huang, W., Tang, M., Zheng, H., Horak, K. M., Li, M., and Wang, X. (2008) α B-crystallin suppresses pressure overload cardiac hypertrophy. Circ. Res. 103, 1473-1482
23. Neppl, R. L., Kataoka, M., and Wang, D. Z. (2014) Crystallin-α B regulates skeletal muscle homeostasis via modulation of Argonaute2 activity. J. Biol. Chem. 289, 17240-17248
24. Christians, E. S., Ishiwata, T., and Benjamin, I. J. (2012) Small heat shock proteins in redox metabolism: implications for cardiovascular diseases. Int. J. Biochem. Cell Biol. 44, 1632-1645
25. Mitzelfelt, K. A., and Benjamin, I. J. (2015) in The Big Book on Small Heat Shock Proteins (Tanguay, R. M., and Hightower, L. E., eds.), 1st ed., pp. 269-299, Springer International Publishing, Switzerland
26. Vicart, P., Caron, A., Guicheney, P., Li, Z., Prévost, M. C., Faure, A., Chateau, D., Chapon, F., Tomé, F., Dupret, J. M., Paulin, D., and Fardeau, M. (1998) A missense mutation in the α B-crystallin chaperone gene causes a desmin-related myopathy. Nat. Genet. 20, 92-95
27. Elliott, J. L., Der Perng, M., Prescott, A. R., Jansen, K. A., Koenderink, G. H., and Quinlan, R. A. (2013) The specificity of the interaction between α B-crystallin and desmin filaments and its impact on filament aggregation and cell viability. Philos. Trans. R Soc. Lond. B Biol. Sci. 368, 20120375
28. Wang, X., Osinska, H., Klevitsky, R., Gerdes, A. M., Nieman, M., Lorenz, J., Hewett, T., and Robbins, J. (2001) Expression of R120G- B-crystallin causes aberrant Desmin and B-Crystallin aggregation and cardiomyopathy in mice. Circ. Res. 89, 84-91
29. Forrest, K. M., Al-Sarraj, S., Sewry, C., Buk, S., Tan, S. V., Pitt, M., Durward, A., McDougall, M., Irving, M., Hanna, M. G., Matthews, E., Sarkozy, A., Hudson, J., Barresi, R., Bushby, K., et al. (2011) Infantile onset myofibrillar myopathy due to recessive CRYAB mutations. Neuromuscul. Disord. 21, 37-40
30. Takahashi, K., Okita, K., Nakagawa, M., and Yamanaka, S. (2007) Induction of pluripotent stem cells from fibroblast cultures. Nat. Protoc. 2, 3081-3089
31. Christians, E. S., Banerjee Mustafi, S., and Benjamin, I. J. (2014) Chaperones and cardiac misfolding protein diseases. Curr. Protein Pept. Sci. 15, 189-204
32. Yusa, K., Rashid, S. T., Strick-Marchand, H., Varela, I., Liu, P. Q., Paschon, D. E., Miranda, E., Ordóñez, A., Hannan, N. R., Rouhani, F. J., Darche, S., Alexander, G., Marciniak, S. J., Fusaki, N., Hasegawa, M., et al. (2011) Targeted gene correction of α1-antitrypsin deficiency in induced pluripotent stem cells. Nature 478, 391-394
33. Amrani, N., Sachs, M. S., and Jacobson, A. (2006) Early nonsense: mRNA decay solves a translational problem. Nat. Rev. Mol. Cell Biol. 7, 415-425
34. Lee, D. H., and Goldberg, A. L. (1998) Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol. 8, 397-403
35. Bloom, J., Amador, V., Bartolini, F., DeMartino, G., and Pagano, M. (2003) Proteasome-mediated degradation of p21 via N-terminal ubiquitinylation. Cell 115, 71-82
36. Yamamoto, A., Tagawa, Y., Yoshimori, T., Moriyama, Y., Masaki, R., and Tashiro, Y. (1998) Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct. Funct. 23, 33- 42
37. Nawrocki, S. T., Carew, J. S., Dunner, K., Jr., Boise, L. H., Chiao, P. J., Huang, P., Abbruzzese, J. L., and McConkey, D. J. (2005) Bortezomib inhibits PKR-like endoplasmic reticulum (ER) kinase and induces apoptosis via ER stress in human pancreatic cancer cells. Cancer Res. 65, 11510-11519
38. Flores-Jasso, C. F., Arenas-Huertero, C., Reyes, J. L., Contreras-Cubas, C., Covarrubias, A., and Vaca, L. (2009) First step in pre-miRNAs processing by human Dicer. Acta Pharmacol. Sin. 30, 1177-1185
39. Jackstadt, R., and Hermeking, H. (2015) MicroRNAs as regulators and mediators of c-MYC function. Biochim. Biophys. Acta 1849, 544-553
40. Perng, M. D., Wen, S. F., van den Ijssel, P., Prescott, A. R., and Quinlan, R. A. (2004) Desmin aggregate formation by R120G α B-crystallin is caused by altered filament interactions and is dependent upon network status in cells. Mol. Biol. Cell 15, 2335-2346
41. Vabulas, R. M., Raychaudhuri, S., Hayer-Hartl, M., and Hartl, F. U. (2010) Protein folding in the cytoplasm and the heat shock response. Cold Spring Harb. Perspect. Biol. 2, 1-18
42. Kondrat, F. L., Struwe, W., and Benesch, J. P. (2015) in Structural Proteomics (Owens, R. J., ed.) pp. 349-371, Springer, New York
43. Aquilina, J. A., Benesch, J. L., Bateman, O. A., Slingsby, C., and Robinson, C. V. (2003) Polydispersity of a mammalian chaperone: mass spectrometry reveals the population of oligomers in α B-crystallin. Proc. Natl. Acad. Sci. U.S.A. 100, 10611-10616
44. Peroutka, R. J., Elshourbagy, N., Piech, T., and Butt, T. R. (2008) Enhanced protein expression in mammalian cells using engineered SUMO fusions: secreted phospholipase A(2). Protein Sci. 17, 1586-1595
45. Panavas, T., Sanders, C., and Butt, T. (2009) SUMO fusion technology for enhanced protein production in prokaryotic and eukaryotic expression systems. Methods Mol. Biol. 497, 303-317
46. Békés, M., Prudden, J., Srikumar, T., Raught, B., Boddy, M. N., and Salvesen, G. S. (2011) The dynamics and mechanism of SUMO chain deconjugation by SUMO-specific proteases. J. Biol. Chem. 286, 10238-10247
47. Lian, X., Zhang, J., Azarin, S. M., Zhu, K., Hazeltine, L. B., Bao, X., Hsiao, C., Kamp, T. J., and Palecek, S. P. (2013) Directed cardiomyocyte differentiation from human pluripotent stem cells by modulating Wnt/α-catenin signaling under fully defined conditions. Nat. Protoc. 8, 162-175
48. Hosoyama, T., McGivern, J. V., Van Dyke, J. M., Ebert, A. D., and Suzuki, M. (2014) Derivation of myogenic progenitors directly from human pluripotent stem cells using a sphere-based culture. Stem Cells Transl. Med. 3, 564-574
49. Zhang, H., Rajasekaran, N. S., Orosz, A., Xiao, X., Rechsteiner, M., and Benjamin, I. J. (2010) Selective degradation of aggregate-prone CryAB mutants by HSPB1 is mediated by ubiquitin-proteasome pathways. J. Mol. Cell. Cardiol. 49, 918-930