1932

Abstract

Hagfishes thwart attacks by fish predators by producing liters of defensive slime. The slime is produced when slime gland exudate is released into the predator's mouth, where it deploys in a fraction of a second and clogs the gills. Slime exudate is composed mainly of secretory products from two cell types, gland mucous cells and gland thread cells, which produce the mucous and fibrous components of the slime, respectively. Here, we review what is known about the composition of the slime, morphology of the slime gland, and physiology of the cells that produce the slime. We also discuss several of the mechanisms involved in the deployment of both mucous and thread cells during the transition from thick glandular exudate to ultradilute material. We review biomechanical aspects of the slime, along with recent efforts to produce biomimetic slime thread analogs, and end with a discussion of how hagfish slime may have evolved.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biochem-060614-034048
2015-06-02
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/biochem/84/1/annurev-biochem-060614-034048.html?itemId=/content/journals/10.1146/annurev-biochem-060614-034048&mimeType=html&fmt=ahah

Literature Cited

  1. Fudge DS, Levy N, Chiu S, Gosline JM. 1.  2005. Composition, morphology and mechanics of hagfish slime. J. Exp. Biol. 208:4613–25 [Google Scholar]
  2. Lim J, Fudge DS, Levy N, Gosline JM. 2.  2006. Hagfish slime ecomechanics: testing the gill-clogging hypothesis. J. Exp. Biol. 209:702–10 [Google Scholar]
  3. Koch EA, Spitzer RH, Pithawalla RB, Downing SW. 3.  1991. Keratin-like components of gland thread cells modulate the properties of mucus from hagfish (Eptatretus stoutii). Cell Tissue Res. 264:79–86 [Google Scholar]
  4. Downing SW, Spitzer RH, Salo WL, Downing JS, Saidel LJ, Koch EA. 4.  1981. Threads in the hagfish slime gland thread cells: organization, biochemical features, and length. Science 212:326–28 [Google Scholar]
  5. Fernholm B. 5.  1981. Thread cells from the slime glands of hagfish (Myxinidae). Acta Zool. 62:137–45 [Google Scholar]
  6. Zintzen V, Roberts CD, Anderson MJ, Stewart AL, Struthers CD, Harvey ES. 6.  2011. Hagfish predatory behaviour and slime defence mechanism. Sci. Rep. 1:131 [Google Scholar]
  7. Linnaeus C. 7.  1758. Systema naturae Holmiae [Stockholm]: Laurentii Salvii, 10th ed..
  8. Spitzer RH, Koch EA. 8.  1998. Hagfish skin and slime glands. The Biology of Hagfishes JM Jørgensen, JP Lomholt, RE Weber, H Malte 109–32 Dordrecht, Neth.: Springer [Google Scholar]
  9. Lametschwandtner A, Lametschwandtner U, Patzner R. 9.  1986. The different vascular patterns of slime glands in the hagfishes, Myxine glutinosa Linnaeus and Eptatretus stoutii Lockington: a scanning electron microscope study of vascular corrosion casts. Acta Zool. 67:243–48 [Google Scholar]
  10. Luchtel DL, Martin AW, Deyrup-Olsen I. 10.  1991. Ultrastructure and permeability characteristics of the membranes of mucous granules of the hagfish. Tissue Cell 23:939–48 [Google Scholar]
  11. Herr JE, Clifford A, Goss GG, Fudge DS. 11.  2014. Defensive slime formation in Pacific hagfish requires Ca2+ and aquaporin mediated swelling of released mucin vesicles. J. Exp. Biol. 217:2288–96 [Google Scholar]
  12. Herr JE, Winegard TM, O'Donnell MJ, Yancey PH, Fudge DS. 12.  2010. Stabilization and swelling of hagfish slime mucin vesicles. J. Exp. Biol. 213:1092–99 [Google Scholar]
  13. Salo WL, Downing SW, Lidinsky WA, Gallagher WH, Spitzer RH, Koch EA. 13.  1983. Fractionation of hagfish slime gland secretions: partial characterization of the mucous vesicle fraction. Prep. Biochem. 13:103–35 [Google Scholar]
  14. Moniaux N, Escande F, Porchet N, Aubert JP, Batra SK. 14.  2001. Structural organization and classification of the human mucin genes. Front. Biosci. 6:D1192–206 [Google Scholar]
  15. Subramanian S, Ross NW, Mackinnon SL. 15.  2008. Comparison of the biochemical composition of normal epidermal mucus and extruded slime of hagfish (Myxine glutinosa L.). Fish Shellfish Immunol. 25:625–32 [Google Scholar]
  16. Spitzer RH, Downing SW, Koch EA, Salo WL, Saidel LJ. 16.  1984. Hagfish slime gland thread cells. II. Isolation and characterization of intermediate filament components associated with the thread. J. Cell Biol. 98:670–77 [Google Scholar]
  17. Spitzer RH, Koch EA, Downing SW. 17.  1988. Maturation of hagfish gland thread cells: composition and characterization of intermediate filament polypeptides. Cell Motil. Cytoskelet. 11:31–45 [Google Scholar]
  18. Koch EA, Spitzer RH, Pithawalla RB, Parry DA. 18.  1994. An unusual intermediate filament subunit from the cytoskeletal biopolymer released extracellularly into seawater by the primitive hagfish (Eptatretus stoutii). J. Cell Sci. 107:3133–44 [Google Scholar]
  19. Koch EA, Spitzer RH, Pithawalla RB, Castillos FA 3rd, Parry DA. 19.  1995. Hagfish biopolymer: a type I/type II homologue of epidermal keratin intermediate filaments. Int. J. Biol. Macromol. 17:283–92 [Google Scholar]
  20. Schaffeld M, Schultess J. 20.  2006. Genes coding for intermediate filament proteins closely related to the hagfish “thread keratins (TK)” α and γ also exist in lamprey, teleosts and amphibians. Exp. Cell Res. 312:1447–62 [Google Scholar]
  21. Riemer D, Weber K. 21.  1998. Common and variant properties of intermediate filament proteins from lower chordates and vertebrates; two proteins from the tunicate styela and the identification of a type III homologue. J. Cell Sci. 111:2967–75 [Google Scholar]
  22. Winegard T, Herr J, Mena C, Lee B, Dinov I. 22.  et al. 2014. Coiling and maturation of a high-performance fibre in hagfish slime gland thread cells. Nat. Commun. 5:3534 [Google Scholar]
  23. Downing SW, Spitzer RH, Koch EA, Salo WL. 23.  1984. The hagfish slime gland thread cell. I. A unique cellular system for the study of intermediate filaments and intermediate filament–microtubule interactions. J. Cell Biol. 98:653–69 [Google Scholar]
  24. Terakado K, Ogawa M, Hashimoto Y, Matsuzaki H. 24.  1975. Ultrastructure of the thread cells in the slime gland of Japanese hagfishes, Paramyxine atami and Eptatretus burgeri. Cell Tissue Res. 159:311–23 [Google Scholar]
  25. Negishi A, Armstrong CL, Kreplak L, Rheinstadter MC, Lim LT. 25.  et al. 2012. The production of fibers and films from solubilized hagfish slime thread proteins. Biomacromolecules 13:3475–82 [Google Scholar]
  26. Pinto N, Yang FC, Negishi A, Rheinstadter MC, Gillis TE, Fudge DS. 26.  2014. Self-assembly enhances the strength of fibers made from vimentin intermediate filament proteins. Biomacromolecules 15:574–81 [Google Scholar]
  27. Newby WW. 27.  1946. The slime glands and thread cells of the hagfish, Polistrotrema stouti.. J. Morphol. 78:397–409 [Google Scholar]
  28. Winegard TM. 28.  2012. Slime gland cytology and mechanisms of slime thread production in the Atlantic hagfish (Myxine glutinosa). MSc thesis, Univ. Guelph, Ont., Can. 137 pp.
  29. Currie S, Edwards SL. 29.  2010. The curious case of the chemical composition of hagfish tissues—50 years on. Comp. Biochem. Physiol. A 157:111–15 [Google Scholar]
  30. McFarland WN, Munz FW. 30.  1965. Regulation of body weight and serum composition by hagfish in various media. Comp. Biochem. Physiol. 14:383–98 [Google Scholar]
  31. Bernards MA Jr, Oke I, Heyland A, Fudge DS. 31.  2014. Spontaneous unraveling of hagfish slime thread skeins is mediated by a seawater-soluble protein adhesive. J. Exp. Biol. 217:1263–68 [Google Scholar]
  32. Downing SW, Salo WL, Spitzer RH, Koch EA. 32.  1981. The hagfish slime gland: a model system for studying the biology of mucus. Science 214:1143–45 [Google Scholar]
  33. Verdugo P. 33.  1991. Mucin exocytosis. Am. Rev. Respir. Dis. 144:S33–37 [Google Scholar]
  34. Winegard TM, Fudge DS. 34.  2010. Deployment of hagfish slime thread skeins requires the transmission of mixing forces via mucin strands. J. Exp. Biol. 213:1235–40 [Google Scholar]
  35. Ewoldt RH, Winegard TM, Fudge DS. 35.  2011. Non-linear viscoelasticity of hagfish slime. Int. J. Nonlinear Mech. 46:627–36 [Google Scholar]
  36. Greenberg DA, Fudge DS. 36.  2013. Regulation of hard α-keratin mechanics via control of intermediate filament hydration: matrix squeeze revisited. Proc. Biol. Sci. 280:20122158 [Google Scholar]
  37. Fudge DS, Gardner KH, Forsyth VT, Riekel C, Gosline JM. 37.  2003. The mechanical properties of hydrated intermediate filaments: Insights from hagfish slime threads. Biophys. J. 85:2015–27 [Google Scholar]
  38. Fudge DS, Gosline JM. 38.  2004. Molecular design of the α-keratin composite: insights from a matrix-free model, hagfish slime threads. Proc. Biol. Sci. 271:291–99 [Google Scholar]
  39. Fudge DS, Hillis S, Levy N, Gosline JM. 39.  2010. Hagfish slime threads as a biomimetic model for high performance protein fibres. Bioinspir. Biomim. 5:035002 [Google Scholar]
  40. Fudge D, Russell D, Beriault D, Moore W, Lane EB, Vogl AW. 40.  2008. The intermediate filament network in cultured human keratinocytes is remarkably extensible and resilient. PLOS ONE 3:e2327 [Google Scholar]
  41. Beriault DR, Haddad O, McCuaig JV, Robinson ZJ, Russell D. 41.  et al. 2012. The mechanical behavior of mutant K14-R125P keratin bundles and networks in NEB-1 keratinocytes. PLOS ONE 7:e31320 [Google Scholar]
  42. Gosline JM, Guerette PA, Ortlepp CS, Savage KN. 42.  1999. The mechanical design of spider silks: from fibroin sequence to mechanical function. J. Exp. Biol. 202:3295–303 [Google Scholar]
  43. Bardack D. 43.  1991. First fossil hagfish (Myxinoidea): a record from the Pennsylvanian of Illinois. Science 254:701–3 [Google Scholar]
  44. Leppi TJ. 44.  1968. Morphochemical analysis of mucous cells in the skin and slime glands of hagfishes. Histochemie 15:68–78 [Google Scholar]
  45. Tsuneki K, Suzuki A, Ouji M. 45.  1985. Sex difference in the cloacal gland in the hagfish, Eptatretus burgeri, and its possible significance in reproduction. Acta Zool. 66:151–58 [Google Scholar]
  46. Nance JM, Braithwaite LF. 46.  1979. The function of the mucous secretions in the cushion star Pteraster tesselatus Ives. J. Exp. Mar. Biol. Ecol. 40:259–66 [Google Scholar]
  47. Lane E, Whitear M. 47.  1980. Skein cells in lamprey epidermis. Can. J. Zool. 58:450–55 [Google Scholar]
  48. Herrmann H, Aebi U. 48.  2000. Intermediate filaments and their associates: multi-talented structural elements specifying cytoarchitecture and cytodynamics. Curr. Opin. Cell Biol. 12:79–90 [Google Scholar]
  49. Omary MB, Coulombe PA, McLean WH. 49.  2004. Intermediate filament proteins and their associated diseases. N. Engl. J. Med. 351:2087–100 [Google Scholar]
  50. Fuchs E, Marchuk D. 50.  1983. Type I and type II keratins have evolved from lower eukaryotes to form the epidermal intermediate filaments in mammalian skin. PNAS 80:5857–61 [Google Scholar]
  51. Capetanaki Y. 51.  2002. Desmin cytoskeleton: a potential regulator of muscle mitochondrial behavior and function. Trends Cardiovasc. Med. 12:339–48 [Google Scholar]
  52. Larsson A, Wilhelmsson U, Pekna M, Pekny M. 52.  2004. Increased cell proliferation and neurogenesis in the hippocampal dentate gyrus of old GFAP−/−Vim−/− mice. Neurochem. Res. 29:2069–73 [Google Scholar]
  53. Eriksson KS, Zhang S, Lin L, Lariviere RC, Julien JP, Mignot E. 53.  2008. The type III neurofilament peripherin is expressed in the tuberomammillary neurons of the mouse. BMC Neurosci. 9:26 [Google Scholar]
  54. Franke WW, Schmid E, Winter S, Osborn M, Weber K. 54.  1979. Widespread occurrence of intermediate-sized filaments of the vimentin-type in cultured cells from diverse vertebrates. Exp. Cell Res. 123:25–46 [Google Scholar]
  55. Collard JF, Cote F, Julien JP. 55.  1995. Defective axonal transport in a transgenic mouse model of amyotrophic lateral sclerosis. Nature 375:61–64 [Google Scholar]
  56. Lammerding J, Fong LG, Ji JY, Reue K, Stewart CL. 56.  et al. 2006. Lamins A and C but not lamin B1 regulate nuclear mechanics. J. Biol. Chem. 281:25768–80 [Google Scholar]
  57. Steinert PM, Chou YH, Prahlad V, Parry DA, Marekov LN. 57.  et al. 1999. 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. 274:9881–90 [Google Scholar]
/content/journals/10.1146/annurev-biochem-060614-034048
Loading
/content/journals/10.1146/annurev-biochem-060614-034048
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error