The mechanism for thermal-enhanced chaperone-like activity of α-crystallin against UV irradiation-induced aggregation of γD-crystallin.


Journal

Biophysical journal
ISSN: 1542-0086
Titre abrégé: Biophys J
Pays: United States
ID NLM: 0370626

Informations de publication

Date de publication:
21 06 2022
Historique:
received: 25 02 2022
revised: 11 05 2022
accepted: 20 05 2022
pubmed: 28 5 2022
medline: 25 6 2022
entrez: 27 5 2022
Statut: ppublish

Résumé

Exposure to solar UV irradiation damages γ-crystallin, leading to cataract formation via aggregation. α-Crystallin, as a small heat shock protein, efficiently suppresses this irreversible aggregation by selectively binding the denatured γ-crystallin monomer. In this study, liquid chromatography tandem mass spectrometry was used to evaluate UV-325 nm irradiation-induced photodamage of human γD-crystallin in the presence of bovine α-crystallin, atomic force microscope (AFM) and dynamic light scattering (DLS) techniques were used to detect the quaternary structure changes of the α-crystallin oligomer, and Fourier transform infrared spectroscopy and temperature-jump nanosecond time-resolved IR absorbance difference spectroscopy were used to probe the secondary structure changes of bovine α-crystallin. We find that the thermal-induced subunit dissociation of the α-crystallin oligomer involves the breaking of hydrogen bonds at the dimeric interface, leading to three different spectral components at varied temperature regions as resolved from temperature-dependent IR spectra. Under UV-325 nm irradiation, unfolded γD-crystallin binds to the dissociated α-crystallin subunit to form an αγ-complex, then follows the reassociation of the αγ-complex to the partially dissociated α-crystallin oligomer. This prevents the aggregation of denatured γD-crystallin. The formation of the γD-bound α-crystallin oligomer is further confirmed by AFM and DLS analysis, which reveals an obvious size expansion in the reassociated αγ-oligomers. In addition, UV-325 nm irradiation causes a peptide bond cleavage of γD-crystallin at Ala158 in the presence of α-crystallin. Our results suggest a very effective protection mechanism for subunits dissociated from α-crystallin oligomers against UV irradiation-induced aggregation of γD-crystallin, at the expense of a loss of a short C-terminal peptide in γD-crystallin.

Identifiants

pubmed: 35619565
pii: S0006-3495(22)00425-8
doi: 10.1016/j.bpj.2022.05.032
pmc: PMC9279354
pii:
doi:

Substances chimiques

Molecular Chaperones 0
alpha-Crystallins 0
gamma-Crystallins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2233-2250

Informations de copyright

Copyright © 2022 Biophysical Society. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Références

Exp Eye Res. 2019 May;182:10-18
pubmed: 30849387
Biochemistry. 2005 Nov 15;44(45):14854-69
pubmed: 16274233
J Protein Chem. 1997 May;16(4):283-9
pubmed: 9188067
J Am Chem Soc. 2009 Nov 25;131(46):16751-7
pubmed: 19919143
Trends Mol Med. 2012 May;18(5):273-82
pubmed: 22520268
Exp Eye Res. 1997 Aug;65(2):255-66
pubmed: 9268594
Biochemistry. 2013 Sep 10;52(36):6169-81
pubmed: 23957864
Langmuir. 2009 Aug 18;25(16):9384-91
pubmed: 19382785
J Biol Chem. 2004 Mar 19;279(12):11222-8
pubmed: 14722093
Hum Mutat. 2011 Jan;32(1):E1939-47
pubmed: 21031598
IUBMB Life. 2006 Nov;58(11):632-41
pubmed: 17085382
J Am Chem Soc. 2001 Dec 5;123(48):12048-58
pubmed: 11724613
J Mol Biol. 2003 May 16;328(5):1137-47
pubmed: 12729747
J Am Chem Soc. 2015 May 13;137(18):5990-9
pubmed: 25909499
Biochem Biophys Res Commun. 1997 Aug 18;237(2):277-82
pubmed: 9268700
FEBS Lett. 1995 Aug 7;369(2-3):321-5
pubmed: 7649280
J Pharm Sci. 2007 Jun;96(6):1468-79
pubmed: 17230445
Int J Biol Macromol. 2018 Oct 1;117:1289-1298
pubmed: 29870813
J Biol Chem. 1994 Nov 4;269(44):27264-8
pubmed: 7961635
J Biol Chem. 1998 Jun 19;273(25):15474-8
pubmed: 9624133
J Biol Chem. 1991 Oct 25;266(30):20079-84
pubmed: 1939070
Microbiol Mol Biol Rev. 2002 Mar;66(1):64-93; table of contents
pubmed: 11875128
Biochim Biophys Acta. 2016 Jan;1860(1 Pt B):149-66
pubmed: 26116912
Q Rev Biophys. 2002 Nov;35(4):369-430
pubmed: 12621861
J Phys Chem B. 2019 Sep 19;123(37):7771-7776
pubmed: 31448608
J Phys Chem B. 2012 Aug 16;116(32):9796-802
pubmed: 22816990
Protein Sci. 2013 Apr;22(4):367-80
pubmed: 23389822
Biochem Biophys Res Commun. 1997 Oct 9;239(1):217-22
pubmed: 9345298
EMBO J. 1999 Dec 1;18(23):6744-51
pubmed: 10581247
Proc Natl Acad Sci U S A. 1992 Nov 1;89(21):10449-53
pubmed: 1438232
Biochemistry. 2008 Apr 1;47(13):4071-81
pubmed: 18321068
J Mol Biol. 2009 Feb 6;385(5):1481-97
pubmed: 19041879
Biochemistry. 2000 Apr 18;39(15):4483-92
pubmed: 10757997
Biochemistry. 2009 May 5;48(17):3708-16
pubmed: 19358562
Invest Ophthalmol Vis Sci. 2006 Jul;47(7):2990-6
pubmed: 16799044
Exp Eye Res. 2003 Feb;76(2):145-53
pubmed: 12565801
Biochem Biophys Res Commun. 2000 Sep 24;276(2):619-25
pubmed: 11027522
Angew Chem Int Ed Engl. 1999 Mar 15;38(6):736-749
pubmed: 29711793
Biochim Biophys Acta. 2016 Jan;1860(1 Pt B):211-21
pubmed: 26073614
Prog Biophys Mol Biol. 1993;59(1):23-56
pubmed: 8419985
Exp Eye Res. 2010 Nov;91(5):691-9
pubmed: 20732317
Int J Biol Macromol. 2019 Nov 1;140:736-748
pubmed: 31445149
FEBS Lett. 1995 May 29;365(2-3):133-6
pubmed: 7781765
Nat Struct Mol Biol. 2010 Sep;17(9):1037-42
pubmed: 20802487
Sci Rep. 2014 Apr 29;4:4834
pubmed: 24776652
Mol Cell Biochem. 2001 Apr;220(1-2):127-33
pubmed: 11451372
Biochem J. 1971 Sep;124(2):337-43
pubmed: 5158502
Biochim Biophys Acta. 2007 Sep;1767(9):1073-101
pubmed: 17692815
Sci China Chem. 2020 Aug;63(8):1121-1133
pubmed: 33163014
Q Rev Biophys. 1997 Nov;30(4):365-429
pubmed: 9634652
J Biol Chem. 2019 Feb 8;294(6):2121-2132
pubmed: 30385502
J Biol Chem. 1999 Nov 19;274(47):33209-12
pubmed: 10559193
Proc Natl Acad Sci U S A. 2011 Dec 20;108(51):20491-6
pubmed: 22143763
PLoS One. 2012;7(3):e34438
pubmed: 22479631
J Biol Chem. 1998 Apr 10;273(15):8965-70
pubmed: 9535881
J Mol Biol. 1999 Jun 4;289(2):397-411
pubmed: 10366513
Protein Sci. 2005 Mar;14(3):569-81
pubmed: 15722442
Proteins. 2010 Aug 15;78(11):2546-53
pubmed: 20535821
Nat Struct Mol Biol. 2019 Dec;26(12):1141-1150
pubmed: 31792453
Eur J Biochem. 2000 Apr;267(7):1923-32
pubmed: 10727931
Exp Eye Res. 2018 Sep;174:185-195
pubmed: 29782825
Exp Eye Res. 1996 Feb;62(2):141-8
pubmed: 8698074
Annu Rev Biophys Biomol Struct. 2000;29:327-59
pubmed: 10940252
Protein Sci. 2016 Jun;25(6):1115-28
pubmed: 26991007
Protein Sci. 2004 Aug;13(8):2223-35
pubmed: 15273315
Exp Eye Res. 2009 Feb;88(2):190-4
pubmed: 18703051
Biochemistry. 2006 Sep 26;45(38):11552-63
pubmed: 16981715
Graefes Arch Clin Exp Ophthalmol. 1999 Feb;237(2):157-60
pubmed: 9987633
Food Res Int. 2017 Jun;96:132-153
pubmed: 28528093
J Mol Biol. 2004 Oct 15;343(2):445-55
pubmed: 15451672
Rev Sci Instrum. 2015 May;86(5):053105
pubmed: 26026512
Chembiochem. 2013 Nov 25;14(17):2362-70
pubmed: 24222572
Prog Biophys Mol Biol. 2004 Nov;86(3):407-85
pubmed: 15302206
Ann Occup Hyg. 1991 Feb;35(1):1-12
pubmed: 2035949
J Biol Chem. 1996 Nov 8;271(45):28558-66
pubmed: 8910485
Biochim Biophys Acta Gen Subj. 2020 Mar;1864(3):129502
pubmed: 31812542
J Biol Chem. 2000 Jan 14;275(2):1035-42
pubmed: 10625643

Auteurs

Hao Li (H)

Laboratory of Soft Matter Physics, Institute of Physics, Chinese Academy of Sciences, Beijing, China; College of Chemical Biology and Biotechnology, Beijing University Shenzhen Graduate School, Shenzhen, China; Institute of Systems and Physical Biology, Shenzhen Bay Laboratory, Shenzhen, China; University of Chinese Academy of Sciences, Beijing, China.

Yingying Yu (Y)

Department of Ophthalmology, Peking University People's Hospital, Eye Diseases and Optometry Institute, Beijing Key Laboratory of Diagnosis and Therapy of Retinal and Choroid Diseases, College of Optometry, Peking University Health Science Center, Beijing, China.

Meixia Ruan (M)

Laboratory of Soft Matter Physics, Institute of Physics, Chinese Academy of Sciences, Beijing, China; University of Chinese Academy of Sciences, Beijing, China.

Fang Jiao (F)

Laboratory of Soft Matter Physics, Institute of Physics, Chinese Academy of Sciences, Beijing, China; University of Chinese Academy of Sciences, Beijing, China.

Hailong Chen (H)

Laboratory of Soft Matter Physics, Institute of Physics, Chinese Academy of Sciences, Beijing, China; University of Chinese Academy of Sciences, Beijing, China.

Jiali Gao (J)

College of Chemical Biology and Biotechnology, Beijing University Shenzhen Graduate School, Shenzhen, China; Institute of Systems and Physical Biology, Shenzhen Bay Laboratory, Shenzhen, China.

Yuxiang Weng (Y)

Laboratory of Soft Matter Physics, Institute of Physics, Chinese Academy of Sciences, Beijing, China; University of Chinese Academy of Sciences, Beijing, China. Electronic address: yxweng@iphy.ac.cn.

Yongzhen Bao (Y)

Department of Ophthalmology, Peking University People's Hospital, Eye Diseases and Optometry Institute, Beijing Key Laboratory of Diagnosis and Therapy of Retinal and Choroid Diseases, College of Optometry, Peking University Health Science Center, Beijing, China. Electronic address: drbaoyz@sina.com.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH