Skip to main content
SpringerLink
Log in

Review: mapping proteins localized in adhesive setae of the tokay gecko and their possible influence on the mechanism of adhesion

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

The digital adhesive pads that allow gecko lizards to climb vertical surfaces result from the modification of the oberhautchen layer of the epidermis in normal scales. This produces sticky filaments of 10–100 μm in length, called setae that are composed of various proteins. The prevalent types, termed corneous beta proteins (CBPs), have a low molecular weight (12–20 kDa) and contain a conserved central region of 34 amino acids with a beta-conformation. This determines their polymerization into long beta-filaments that aggregate into corneous beta-bundles that form the framework of setae. Previous studies showed that the prevalent CBPs in the setae of Gekko gecko are cysteine-rich and are distributed from the base to the tip of adhesive setae, called spatulae. The molecular analysis of these proteins, although the three-dimensional structure remains undetermined, indicates that most of them are charged positively and some contain aromatic amino acids. These characteristics may impede adhesion by causing the setae to stick together but may also potentiate the van der Waals interactions responsible for most of the adhesion process on hydrophobic or hydrophilic substrates. The review stresses that not only the nanostructural shape and the high number of setae present in adhesive pads but also the protein composition of setae influence the strength of adhesion to almost any type of substrate. Therefore, formulation of dry materials mimicking gecko adhesiveness should also consider the chemical nature of the polymers utilized to fabricate the future dry adhesives in order to obtain the highest performance.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Alibardi L (1997) Ultrastructural and autoradiographic analysis of setae development in the embryonic pad lamellae of the lizard Anolis lineatopus. Ann Sci Nat Zool (Paris) 18:51–61

    Google Scholar 

  • Alibardi L (1999) Keratohyalin-like granules in embryonic and regenerating epidermis of lizards and Sphenodon punctatus (Reptilia, Lepidosauria). Amphibia-Reptilia 20:11–23

    Article  Google Scholar 

  • Alibardi L (2009) Cell biology of adhesive setae in gecko lizards. Zoology 112:403–424

    Article  CAS  Google Scholar 

  • Alibardi L (2013a) Immunolocalization of keratin-associated beta-proteins (beta-keratins) in pad lamellae of geckos suggest that glycine-cysteine-rich proteins contribute to their flexibility and adhesiveness. J Exp Zool 319A:166–178

    Article  Google Scholar 

  • Alibardi L (2013b) Immunolocalization of specific keratin-associated beta-proteins (beta-keratins) in the adhesive sete of Gekko gecko. Tiss Cell 45:231–240

    Article  CAS  Google Scholar 

  • Alibardi L (2013c) Ultrastructural immunocytochemistry for the central region of keratin associated-beta-proteins (beta-keratins) shows the epitope is constantly expressed in reptilian epidermis. Tiss Cell 45:241–252

    Article  CAS  Google Scholar 

  • Alibardi L (2014) Presence of a glycine-cysteine-rich beta-protein in the oberhautchen layer of snake epidermis marks the formation of the shedding layer. Protoplasma 251:1511–1520

    Article  CAS  Google Scholar 

  • Alibardi L (2015) Immunolocalization of large corneous Beta-proteins in the green anole lizard (Anolis carolinensis) suggests that they form filaments that associate to the smaller Beta-proteins in the Beta-layer of the epidermis. J Morphol 276:1244–1257

    Article  CAS  Google Scholar 

  • Alibardi L (2016a) Review. The process of cornification evolved from the initial keratinization in the epidermis and epidermal derivatives of vertebrates: a new synthesis and the case of sauropsids. Int Rev Cell Mol Biol 327:264–319

    Google Scholar 

  • Alibardi L (2016b) Sauropsid cornification is based on corneous beta-proteins, a special type of proteins of the epidermis. J Exp Zool 326B:338–351

    Article  Google Scholar 

  • Alibardi L (2016c) Review: mapping epidermal beta-proteins distribution in the lizard Anolis carolinensis shows a specific localization for the formation of scales, pads and claws. Protoplasma 253:1405–1420

    Article  CAS  Google Scholar 

  • Alibardi L, Toni M (2005) Distribution and characterization of proteins associated with cornification in the epidermis of gecko lizard. Tiss Cell 37:423–433

    Article  CAS  Google Scholar 

  • Alibardi L, Meyer-Rochow VB (2017) Regeneration of tail adhesive pad scales in the New Zealand gecko Hoplodactylus maculatus (Reptilia, Squamata, Lacertilia) can serve as an experimental model to analyze setal formation in lizards generally. Zool Res 38:1–11

    Article  Google Scholar 

  • Alibardi L, Toni M, Dalla Valle L (2007) Expression of beta-keratin mRNAs and proline-uptake in epidermal cells of growing scales and pad lamellae of gecko lizards. J Anat 211:104–116

    Article  CAS  Google Scholar 

  • Alibardi L, Edward DP, Patil L, Bouhenni R, Dhinojwala A, Niewiarowski PH (2011) Histochemical and ultrastructural analysis of adhesive setae of lizards indicate that they contain lipids in addition to keratins. J Morph 272:758–768

    Article  CAS  Google Scholar 

  • Alibardi L, Segalla A, Dalla Valle L (2012) Distribution of specific keratin associated beta-proteins (beta-keratins) in the epidermis of the lizard Anolis carolinensis helps to clarify the process of cornification in lepidosaurians. J Exp Zool 318B:388–403

    Article  Google Scholar 

  • Autumn K, Peattie AM (2002) Mechanisms of adhesion in geckos. Integr Comp Biol 42:1081–1090

    Article  Google Scholar 

  • Autumn K, Gravish N (2008) Gecko adhesion: evolutionary nanotechnology. Phil Trans R Soc A 366:1575–1590

    Article  CAS  Google Scholar 

  • Badge I, Stark AY, Paoloni EL, Niewiarowski PH, Dhinojwala A (2014) The role of surface chemistry in adhesion and wetting of gecko toe pads. Sci Rep 4:6643

    Article  CAS  Google Scholar 

  • Bauer AM (1998) Morphology of the adhesive tail tips of Carphodactyline geckos (Reptilia: Diplodactylidae). J Morph 235:41–58

    Article  Google Scholar 

  • Berengueres J, Saito S, Tadakuma K (2007) Structural properties of a scaled gecko foot-hair. Bioinspir Biomim 2:1–8

    Article  Google Scholar 

  • Calvaresi M, Eckhart L, Alibardi L (2016) The molecular organization of the beta-sheet region in corneous beta-proteins (beta-keratins) of sauropsids explains its stability and polymerization into filaments. J Struct Biol 194:282–291

    Article  CAS  Google Scholar 

  • Dalla Valle L, Nardi A, Toffolo V, Niero C, Toni M, Alibardi L (2007) Cloning and characterization of scale beta-keratins in the differentiating epidermis of geckos show they are glycine-proline-serine-rich proteins with a central motif homologous to avian beta-keratins. Dev Dyn 236:374–388

    Article  CAS  Google Scholar 

  • Hallahan DL, Keiper-Hrynko NM, Shang TQ, Ganzke TS, Toni M, Dalla Valle L, Alibardi L (2008) Analysis of gene expression in gecko digital adhesive pads indicates significant production of cysteine- and glycine-rich beta-keratins. J Exp Zool 312B:58–73

    Article  Google Scholar 

  • Hiller U (1972) Licht- und elektronenmikroskopische Untersuchungen zur Haftborstenentwicklung bei Tarentola mauritanica L. (Reptilia, Gekkonidae). Zeitsch Morpholog der Tiere 73:263–278

    Article  Google Scholar 

  • Holthaus KB, Strasser B, Sipos W, Schmidt HA, Mlitz V, Sukseree S, Weissenbacher A, Tschchler E, Alibardi L, Eckhart L (2015) Comparative genomics identifies epidermal proteins associated with the evolution of the turtle shell. Mol Biol Evol 33:726–737

    Article  Google Scholar 

  • Holthaus KB, Mlitz V, Strasser B, Tschachler E, Alibardi L, Eckhart L (2017) Comparative genomics of the epidermal differentiation complex suggests evolutionary adaptions of snake skin. Sci Rep (Nature) 7:45338

    Article  Google Scholar 

  • Hsu PH, Ge L, Li X, Stark AY, Wesdemiotis C, Niewiarowski PH, Dhinojawala A (2011) Direct evidence of phospholipids in gecko footprints and spatula-substrate contact interface detected using surface-sensitive spectroscopy. J R Soc Interface 9:657–664

    Article  Google Scholar 

  • Huber G, Mantz H, Spolenak R, Mecke K, Jacobs K, Gorb SN, Arzt E (2005) Evidence for capillary contributions to gecko adhesion from single spatula nanomechanical measurements. PNAS 102:16293–16296

    Article  CAS  Google Scholar 

  • Izadi H, Stewart KME, Penlidis A (2014) Role of contact electrification and electrostatic interactions in gecko adhesion. J R Soc Interface 11:20140371

    Article  Google Scholar 

  • Jain D, Stark AY, Niewiarowski PH, Miyoshi T, Dhinojwala A (2015) NMR spectroscopy reveals the presence and association of lipids and keratin in adhesive gecko setae. Sci Rep 5:9594

    Article  CAS  Google Scholar 

  • Liu Y, Zhou Q, Wang Y, Luo L, Yang J, Yang L, Liu M, Qian YT, Zheng Y, Li M, Li J, Gu Y, Han Z, Xu M, Wang Y, Zhu C, Yu B, Yang Y, Ding F, Jiand J, Yang H, Gu X (2015) Gekko japonicus genome reveal evolution of adhesive toe pads and tail regeneration. Nat Commun 6:100333

    Google Scholar 

  • Maderson PFA (1970) Lizard glands and lizard hands: models for evolutionary study. Forma et Functio 3:179–204

    Google Scholar 

  • Maderson PFA (1971) The regeneration of caudal epidermal specializations in Lygodactylus picturatus keniensis (Gekkonidae, Lacertilia). J Morphol 134:467–478

    Article  CAS  Google Scholar 

  • Niewiarowski PH, Lopez S, Ge L, Hagan E, Dhinojawala A (2008) Sticky gecko feet: the role of temperature and humidity. Plosone 3:e2192

    Article  Google Scholar 

  • Niewiarowski PH, Stark AY, Dhinojwaia A (2016) Sticking to the story: outstanding challenges in gecko-inspired adhesives. J Exp Biol 219:912–919

    Article  Google Scholar 

  • Puthoff JB, Prowse MS, Wilkinson M, Autumn K (2010) Changes in material properties explain the effects of humidity on gecko adhesion. J Exp Biol 213:3699–3704

    Article  Google Scholar 

  • Rizzo NW, Gardner KH, Walls DJ, Keiper-Hrynko NM, Ganzke TS, Hallahan DL (2006) Characterization of the structure of gecko adhesive setae. J R Soc Interface 3:441–451

    Article  CAS  Google Scholar 

  • Russel AP (1985) The morphological basis of weight. Bearing in the scansors of the tokay gecko (Reptilia: Sauria). Canad. J Zool 64:948–955

    Google Scholar 

  • Russel AP (2002) Integrative functional morphology of the gekkotan adhesive system (Reptilia: Gekkota). Integr Comp Biol 42:1154–1163

    Article  Google Scholar 

  • Sawyer RH, Glenn TC, French JO, Mays B, Shames RB, Barnes GL, Rhodes W, Ishikawa Y (2000) The expression of beta (β) keratins in the epidermal appendages of reptiles and birds. Am Zool 40:530–539

    CAS  Google Scholar 

  • Strasser B, Mlitz V, Hermann M, Rice RH, Eigenheer RA, Alibardi L, Tschachler E, Eckhart L. (2014) Evolutionary origin and diversification of epidermal barrier proteins in amniotes. Mol Biol Evol 31: 3194–3205

    Article  CAS  Google Scholar 

  • Sun W, Neuzii P, Kustandi TS, Oh S, Samper VD (2005) The nature of the gecko lizard adhesive force. Biophys J Biophys Lett:L14–l17

    Article  CAS  Google Scholar 

  • Thorpe RS, Giddings MR (1981) A novel biochemical systematic technique for herpetology based on epidermal keratins. Cell Mol Life Sci 37:700–702

    Article  CAS  Google Scholar 

  • Toni M, Dalla Valle L, Alibardi L (2007) The epidermis of scales in gecko lizards contains multiple forms of beta-keratins including basic glycine-proline-serine-rich proteins. J Proteome Res 6:1792–1805

    Article  CAS  Google Scholar 

  • Wagner C, Fournier N, Ruiz VG, Li C, Mullen K, Rohlfing M, Tkatchenko A, Temirov R, Tautz SF (2014) Non-additivity of molecule-surface van der Waals potentials from force measurements. Nat Commun 5:5568

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Study self-supported, in particular for the ultrastructural analysis (Comparative Histolab). A preliminary communication on the protein localization in gecko setae was presented during the Belnstein Symposium on September 2016, held in Postdam, Berlin, Germany. The comments of referees helped in improving the MS.

Author information

Authors and Affiliations

  1. Comparative Histolab Padua, Bologna, Italy

    Lorenzo Alibardi

  2. Dipartimento di Biologia, Universita’ di Bologna, via Selmi 3, 40126, Universita’ di Bologna, Bologna, Italy

    Lorenzo Alibardi

Authors
  1. Lorenzo Alibardi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lorenzo Alibardi.

Ethics declarations

Conflict of interest

The author declares that there is no conflict of interest.

Additional information

Handling Editor: Douglas Chandler

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alibardi, L. Review: mapping proteins localized in adhesive setae of the tokay gecko and their possible influence on the mechanism of adhesion. Protoplasma 255, 1785–1797 (2018). https://doi.org/10.1007/s00709-018-1270-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-018-1270-9

Keywords

Search

Navigation