Skip to main content
SpringerLink
Log in

Structural Transition of Trichocyte Keratin Intermediate Filaments During Development in the Hair Follicle

  • Chapter
  • First Online:
Fibrous Proteins: Structures and Mechanisms

Part of the book series: Subcellular Biochemistry ((SCBI,volume 82))

Abstract

The intermediate filaments (IF) in trichocyte (hard α-) keratin are unique amongst the various classes of IF in having not one but two topologically-distinct structures. The first is formed at an early stage of hair development in a reducing environment within the cells in the lower part of the follicle. The second structure occurs at a later stage of hair development in the upper part of the follicle, where there is a transition to an oxidizing environment. Crosslinking studies reveal that molecular slippage occurs within the IF upon oxidation and that this results in many cysteine residues lying in near axial alignment, thereby facilitating disulphide bond formation. The disulphide bonds so formed stabilize the assembly of IF molecules and convert the keratin fibre into a tough, resilient and insoluble structure suitable for its function in vivo as a thermo-regulator and a protector of the animal against its external environment.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

DST:

disulpho-succinimidyl tartrate

IF:

intermediate filament

HPLC:

high-performance liquid chromatography

TEM:

transmission electron microscopy

STEM:

scanning transmission electron microscopy

References

  • Al-Amoudi A, Chang J-J, Leforestier A, McDowall A, Salomin LM, Norlén LPO, Richter K, Sartori Blanc N, Studer D, Dubochet J (2004) Cryo-electron microscopy of vitreous sections. EMBO J 23:3583–3588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Astbury WT, Woods HJ (1930) The X-ray interpretation of the structure and elastic properties of hair keratin. Nature 126:913–914

    Article  CAS  Google Scholar 

  • Astbury WT, Woods HJ (1933) X-ray studies on the structure of hair, wool and related fibres II. The molecular structure and elastic properties of hair keratin. Phil Trans Roy Soc Lond A 232:333–394

    Article  Google Scholar 

  • Aziz A, Hess JF, Budamagunta MS, Voss JC, Kuzin AP, Huang YJ, Xiao R, Montelione GT, FitzGerald PG, Hunt JF (2012) The structure of vimentin linker 1 and rod 1b domains characterized by site-directed spin-labeling electron paramagnetic resonance (SDSL-EPR) and X-ray crystallography. J Biol Chem 287:28349–28361

    Google Scholar 

  • Bear RS (1944) X-ray diffraction studies on protein fibers. II Feather keratin, porcupine quill and clam muscle. J Am Chem Soc 66:2043–2050

    Article  CAS  Google Scholar 

  • Birbeck MSC, Mercer EH (1957) The electron microscopy of human hair follicle. J Biophys Biochem Cytol 3:203–214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chernyatina AA, Nicolet S, Aebi U, Herrmann H, Strelkov SV (2012) Atomic structure of the vimentin central α-helical domain and its implications for intermediate filament assembly. Proc Natl Acad Sci U S A 109:13620–13625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chernyatina AA, Guzenko D, Strelkov SV (2015) Intermediate filament structure: the bottom-up approach. Curr Opin Cell Biol 32:65–72

    Article  CAS  PubMed  Google Scholar 

  • Crewther WG, Fraser RDB, Lennox FG, Lindley H (1965) The chemistry of keratins. Adv Protein Chem 20:191–346

    Article  CAS  PubMed  Google Scholar 

  • Crewther WG, Dowling LM, Steinert PM, Parry DAD (1983) Structure of intermediate filaments. Int J Biol Macromol 5:267–274

    Article  CAS  Google Scholar 

  • Crick FHC (1953) The packing of alpha-helices – simple coiled-coils. Acta Cryst 6:689–697

    Article  CAS  Google Scholar 

  • Coulombe PA, Fuchs E (1990) Elucidating the early stages of keratin filament assembly. J Cell Biol 111:153–169

    Article  CAS  PubMed  Google Scholar 

  • Filshie BK, Rogers GE (1961) The fine structure of α-keratin. J Mol Biol 3:784–786

    Article  CAS  PubMed  Google Scholar 

  • Fraser RDB, MacRae TP (1958) Structural implications of the equatorial X-ray diffraction pattern of α-keratin. Biochim Biophys Acta 29:229–240

    Article  CAS  PubMed  Google Scholar 

  • Fraser RDB, MacRae TP (1971) Structure of α-keratin. Nature (London) 233:138–140

    Article  CAS  Google Scholar 

  • Fraser RDB, MacRae TP (1980) Molecular structure and mechanical properties of keratins. In: Vincent JFV, Currey JD (eds) The mechanical properties of biological materials. Cambridge University Press, Cambridge, pp 211–246

    Google Scholar 

  • Fraser RDB, MacRae TP (1983) The structure of the α-keratin microfibril. Biosci Rep 3:517–525

    Article  CAS  PubMed  Google Scholar 

  • Fraser RDB, MacRae TP (1985) Intermediate filament structure. Biosci Rep 5:573–579

    Article  CAS  PubMed  Google Scholar 

  • Fraser RDB, Parry DAD (2003) Macrofibril assembly in trichocyte (hard α-) keratins. J Struct Biol 142:319–325

    Article  PubMed  Google Scholar 

  • Fraser RDB, Parry DAD (2005) The three-dimensional structure of trichocyte (hard α-) keratin intermediate filaments: features of the molecular packing deduced from the sites of induced crosslinks. J Struct Biol 151:171–181

    Article  CAS  PubMed  Google Scholar 

  • Fraser RDB, Parry DAD (2007) Structural changes in the trichocyte intermediate filaments accompanying the transition from the reduced to the oxidized form. J Struct Biol 159:36–45

    Google Scholar 

  • Fraser RDB, Parry DAD (2012) The role of disulfide bond formation in the structural transition observed in the intermediate filaments of the developing hair. J Struct Biol 180:117–124

    Article  Google Scholar 

  • Fraser RDB, Parry DAD (2014) Keratin intermediate filaments: differences in the sequences of the type I and type II chains explain the origin of the stability of an enzyme-resistant four-chain fragment. J Struct Biol 185:317–326

    Google Scholar 

  • Fraser RDB, MacRae TP, Miller A (1964) The coiled-coil model of α-keratin structure. J Mol Biol 10:147–156

    Article  CAS  PubMed  Google Scholar 

  • Fraser RDB, MacRae TP, Miller A (1965) X-ray diffraction pattern of α-fibrous proteins. J Mol Biol 14:432–442

    Article  CAS  PubMed  Google Scholar 

  • Fraser RDB, MacRae TP, Parry DAD (1967) The substructure of the α-keratin microfibril. In: Crewther WG (ed) Symposium on fibrous proteins (Australia 1967), Butterworths, Australia, pp 279–286

    Google Scholar 

  • Fraser RDB, MacRae TP, Millward GR, Parry DAD, Suzuki E, Tulloch PA (1971) The molecular structure of keratins. Appl Polym Symp No 18:65–83

    Google Scholar 

  • Fraser RDB, MacRae TP, Rogers GE (1972) Keratins – their composition, structure and biosynthesis. Thomas, Springfield

    Google Scholar 

  • Fraser RDB, MacRae TP, Suzuki E (1976) Structure of the α-keratin microfibril. J Mol Biol 108:435–452

    Article  CAS  PubMed  Google Scholar 

  • Fraser RDB, MacRae TP, Parry DAD, Suzuki E (1986) Intermediate filaments in α-keratins. Proc Natl Acad Sci U S A 83:1179–1183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fraser RDB, MacRae TP, Parry DAD (1990) The three-dimensional structure of IF. In: RD Goldman, PM Steinert (eds) Cellular and molecular biology of intermediate filaments. Plenum, New York, pp 205–231

    Chapter  Google Scholar 

  • Fraser RDB, Steinert PM, Parry DAD (2003) Structural changes in trichocyte keratin intermediate filaments during keratinization. J Struct Biol 142:266–271

    Article  PubMed  Google Scholar 

  • Fujikawa H, Fujimoto A, Farooq M, Ito M, Shimomura Y (2012) Characterization of the human hair keratin-associated protein 2 (KRTAP2) gene family. J Invest Dermatol 132:1806–1813

    Article  CAS  PubMed  Google Scholar 

  • Geisler N, Kaufman E, Weber K (1982) Protein-chemical characterization of three structurally distinct domains along the protofilament unit of 10 nm filaments. Cell 30:277–286

    Article  CAS  PubMed  Google Scholar 

  • Hatzfeld, M. and Weber, K. 1990. The coiled-coil of in vitro assembled keratin filaments is a heterodimer of type I and II keratin: use of site-specific mutagenesis and recombinant protein expression. J Cell Biol 110:1199–1210

    Google Scholar 

  • Herrmann H, Aebi U (2004) Intermediate filaments: Molecular structure, assembly mechanism, and integration into functionally distinct intracellular scaffolds. Annu Rev Biochem 73:749–789

    Article  CAS  PubMed  Google Scholar 

  • Jones LN (1976) Studies on microfibrils from α-keratin. Biochim Biophys Acta 446:515–524

    Article  CAS  PubMed  Google Scholar 

  • Jones LN, Simon M, Watts NR, Booey FP, Steven AC, Parry DAD (1997) Intermediate filament structure: Hard alpha-keratin. Biophys Chem 68:83–93

    Article  CAS  PubMed  Google Scholar 

  • Klug A, Crick FHC, Wyckoff HW (1958) Diffraction by helical structures. Acta Cryst 11:199–213

    Article  CAS  Google Scholar 

  • Lee CH, Kim MS, Chung BM, Leahy DJ, Coulombe PA (2012) Structural basis for heteromeric assembly and perinuclear organization of keratin filaments. Nat Struct Mol Biol 19:707–715

    Article  CAS  PubMed  Google Scholar 

  • MacArthur I (1943) Structure of α-keratin. Nature 152:38–41

    Article  CAS  Google Scholar 

  • Matsunaga R, Abe R, Ishii D, Watanabe S-I, Kiyoshi M, Nöcker B, Tsuchiya M, Tsumoto K (2013) Bidirectional binding property of high glycine-tyrosine keratin-associated protein contributes to the mechanical strength and shape of hair. J Struct Biol 183:484–494

    Article  CAS  PubMed  Google Scholar 

  • Meier M, Padilla GP, Herrmann H, Wedig T, Hergt M, Patel TR, Stetefeld J, Aebi U, Burkhard P (2009) Vimentin coil 1A – a molecular switch involved in the initiation of filament elongation. J Mol Biol 390:245–261

    Google Scholar 

  • Millward GR (1970) The sub-structure of α-keratin microfibrils. J Ultrastruct Res 31:349–355

    Article  CAS  PubMed  Google Scholar 

  • Nicolet S, Herrmann H, Aebi U, Strelkov SV (2010) Atomic structure of vimentin coil 2. J Struct Biol 170:369–376

    Article  CAS  PubMed  Google Scholar 

  • Parry DAD (1996) Hard α-keratin intermediate filaments: an alternative explanation of the low-angle equatorial X-ray diffraction pattern, and the axial disposition of putative disulphide bonds in the intra- and inter-protofilamentous networks. Int J Biol Macromol 19:45–50

    Article  CAS  PubMed  Google Scholar 

  • Parry DAD (2006) Hendecad repeat in segment 2A and linker L2 of intermediate filament chains implies the possibility of a right-handed coiled coil structure. J Struct Biol 155:370–374

    Article  CAS  PubMed  Google Scholar 

  • Parry DAD, Steinert PM (1995) Intermediate filament structure, Springer, Heidelberg, pp 1–183

    Google Scholar 

  • Parry DAD, Steinert PM (1999) Intermediate filaments: molecular architecture, assembly, dynamics and polymorphism. Q Rev Biophys 32:99–187

    Article  CAS  PubMed  Google Scholar 

  • Parry DAD, Crewther WG, Fraser RDB, MacRae TP (1977) Structure of α-keratin: structural implication of the amino acid sequences of the type I and type II chain segments. J Mol Biol 113:449–454

    Article  CAS  PubMed  Google Scholar 

  • Parry DAD, Fraser RDB, MacRae TP (1979) Repeating patterns of amino acid residues in the sequences of some high-sulphur proteins from α-keratin. Int J Biol Macromol 1:17–22

    Google Scholar 

  • Parry DAD, Steven AC, Steinert PM (1985) The coiled-coil molecules of intermediate filaments consist of two parallel chains in exact axial register. Biochem Biophys Res Commun 127:1012–1018

    Article  CAS  PubMed  Google Scholar 

  • Parry DAD, Marekov LN, Steinert PM (2001) Subfilamentous protofibril structures in fibrous proteins: cross-linking evidence for protofibrils in intermediate filaments. J Biol Chem 276:39253–39258

    Google Scholar 

  • Rogers GE (1959) Electron microscope studies of hair and wool. Ann N Y Acad Sci 83:378–399

    Article  CAS  PubMed  Google Scholar 

  • Rogers GE, Filshie BK (1962) Electron staining and fine structure of keratins. Proc. Intern. Congr. Electron Microscopy, 5th Philadelphia, vol 2, O-2. Academic, New York

    Google Scholar 

  • Ruan J, Xu C, Bian C, Lam R, Wang JP, Kania J, Min J, Zang J (2012) Crystal structures of the coil 2B fragment and the globular tail domain of human lamin B1. FEBS Lett 586:314–318

    Article  CAS  PubMed  Google Scholar 

  • Steinert PM (1990) The two-chain coiled-coil molecule of native epidermal keratin intermediate filaments is a type I –type II heterodimer. J Biol Chem 265:8766–8774

    CAS  PubMed  Google Scholar 

  • Steinert PM, Gullino MI (1976) Bovine epidermal keratin filament assembly in vitro. Biochem Biophys Res Commun 70:221–227

    Article  CAS  PubMed  Google Scholar 

  • Steinert PM, Marekov LN, Fraser RDB, Parry DAD (1993a) Keratin intermediate filament structure: crosslinking studies yield quantitative information on molecular dimensions and mechanism of assembly. J Mol Biol 230:436–452

    Article  CAS  PubMed  Google Scholar 

  • Steinert PM, Marekov LN, Parry DAD (1993b) Conservation of the structure of keratin intermediate filaments: molecular mechanism by which different keratin molecules integrate into pre-existing keratin intermediate filaments during differentiation. Biochemistry 32:10046–10056

    Article  CAS  PubMed  Google Scholar 

  • Steinert PM, Marekov LN, Parry DAD (1993c) Diversity of intermediate filament structure: evidence that the alignment of coiled-coil molecules in vimentin is different from that in keratin intermediate filaments. J Biol Chem 268:24916–24925

    CAS  PubMed  Google Scholar 

  • Steinert PM, Chou Y-H, Prahlad V, Parry DAD, Marekov LN, Wu KC, Jang S-I, Goldman RD (1999a) A high molecular weight intermediate filament-associated protein in BHK-21 cells is nestin, a type VI intermediate filament protein: limited co-assembly in vitro to form heteropolymers with type III vimentin and type IV α-internexin. J Biol Chem 274:9881–9890

    Google Scholar 

  • Steinert PM, Marekov LN, Parry DAD (1999b) Molecular parameters of type IV α-internexin and type IV-type III α-internexin-vimentin copolymer intermediate filaments. J Biol Chem 274:1657–1666

    Article  CAS  PubMed  Google Scholar 

  • Strelkov SV, Herrmann H, Geisler N, Wedig T, Zimbelmann R, Aebi U (2002) Conserved segments 1A and 2B of the intermediate filament dimer: their atomic structures and role in filament assembly. EMBO J 21:1255–1266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strelkov SV, Schumacher J, Burkhard P, Aebi U, Herrmann H (2004) Crystal structure of the human lamin A coil 2B dimer: implications for the head-to-tail association of nuclear lamins. J Mol Biol 343:1067–1080

    Google Scholar 

  • Strnad P, Usachov V, Debes C, Gräter F, Parry DAD, Omary MB (2011) Unique amino acid signatures that are evolutionarily conserved distinguish simple-type, epidermal and hair keratins. J Cell Sci 124:4221–4232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H, Parry DAD, Jones LN, Idler WW, Marekov LN, Steinert PM (2000) In vitro assembly and structure of trichocyte keratin intermediate filaments: a novel role for stabilization by disulfide bonding. J Cell Biol 151:1459–1468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watts NR, Jones LN, Cheng N, Wall JS, Parry DAD, Steven AC (2002) Cryo-electron microscopy of trichocyte (hard α-keratin) intermediate filaments reveals a low-density core. J Struct Biol 137:109–118

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Fundamental Sciences, Massey University, Private Bag 11-222, Palmerston North, 4442, New Zealand

    R. D. Bruce Fraser

  2. 28 Satinay Drive, Noosa Parklands, Tewantin, Qld, 4565, Australia

    R. D. Bruce Fraser

  3. Institute of Fundamental Sciences and Riddet Institute, Massey University, Private Bag 11-222, Palmerston North, 4442, New Zealand

    David A. D. Parry

Authors
  1. R. D. Bruce Fraser
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David A. D. Parry
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David A. D. Parry .

Editor information

Editors and Affiliations

  1. Institute of Fundamental Sciences and Riddet Institute, Massey University, Palmerston North, New Zealand

    David A.D. Parry

  2. Muscle Contraction Group, School of Physiology, Pharmacology and Neuroscience, University of Bristol, Bristol, United Kingdom

    John M. Squire

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Fraser, R.D.B., Parry, D.A.D. (2017). Structural Transition of Trichocyte Keratin Intermediate Filaments During Development in the Hair Follicle. In: Parry, D., Squire, J. (eds) Fibrous Proteins: Structures and Mechanisms. Subcellular Biochemistry, vol 82. Springer, Cham. https://doi.org/10.1007/978-3-319-49674-0_5

Download citation

Publish with us

Policies and ethics

Search

Navigation