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Wilkie, I.C.; Carnevali, M.D.C. Strength in Weakness: The Mutable Collagenous Tissue of Echinoderms. Encyclopedia. Available online: https://encyclopedia.pub/entry/59236 (accessed on 05 December 2025).
Wilkie IC, Carnevali MDC. Strength in Weakness: The Mutable Collagenous Tissue of Echinoderms. Encyclopedia. Available at: https://encyclopedia.pub/entry/59236. Accessed December 05, 2025.
Wilkie, Iain C., M. Daniela Candia Carnevali. "Strength in Weakness: The Mutable Collagenous Tissue of Echinoderms" Encyclopedia, https://encyclopedia.pub/entry/59236 (accessed December 05, 2025).
Wilkie, I.C., & Carnevali, M.D.C. (2025, November 06). Strength in Weakness: The Mutable Collagenous Tissue of Echinoderms. In Encyclopedia. https://encyclopedia.pub/entry/59236
Wilkie, Iain C. and M. Daniela Candia Carnevali. "Strength in Weakness: The Mutable Collagenous Tissue of Echinoderms." Encyclopedia. Web. 06 November, 2025.
Strength in Weakness: The Mutable Collagenous Tissue of Echinoderms
This entry is adapted from the peer-reviewed paper 10.3390/encyclopedia5040185

Mutable collagenous tissue (MCT) is a type of connective tissue that is characterized by its capacity to undergo rapid, nervously mediated changes in mechanical properties. In terms of both the magnitude of these changes and the timescale within which they occur (less than one second to a few minutes), this tissue appears to be unique to the phylum Echinodermata and, as it is ubiquitous in all five extant echinoderm classes, it represents one of the four major defining features of the phylum, together with pentaradial symmetry, endoskeletal stereom (calcite meshwork), and the water vascular system. MCT has been the subject of intensive scientific investigation for over 50 years. The primary aim of this contribution is to provide a comprehensive and definitive survey of the current state of knowledge of this remarkable tissue. After outlining the history of the scientific investigation of MCT, we review current information on its anatomical distribution, organization at the histological, ultrastructural and molecular levels, and physiology—focusing on its mechanical behavior and the regulation of this behavior; its significance for echinoderm biology, including pathology; and biomedical and other applications that exploit MCT-derived components or biological principles. We conclude by drawing attention to more serious deficiencies in the current knowledge base and suggesting how these should be rectified.

autotomy basement membrane biomimetic nanocomposite glycosaminoglycan juxtaligamental cell proteoglycan stiffness tuning tensilin
It has long been recognized that the collagens constitute the most abundant and widely distributed protein family in the animal kingdom [1]. According to a classification based on domain structure and supramolecular organization, 28 distinct collagen proteins have been identified, the most prevalent of which occur as parallel fibril-like aggregates or three-dimensional meshworks in the extracellular matrix (ECM) of connective tissue [2][3]. Connective tissue consisting mainly of fibril- or meshwork-forming collagens is present in all but the simplest multicellular animals. It is by far the most important structural material in the bodies of all non-arthropods [4][5], has essential regulatory functions by virtue of its involvement in cell adhesion, differentiation, and intercellular signaling [6][7][8], and in some animals may function as a body-wide mechanosensitive signaling network [9].
As a structural material, the roles of collagenous connective tissue are mainly to resist, transmit, and dissipate mechanical forces and to store and release elastic strain energy [10]. However, the specific tensile properties of different collagenous structures vary according to the functional demands for which these structures are adapted [3][11][12][13]. The tensile properties of individual structures may also change during development and aging and during homeostatic and other physiological processes. Such changes usually occur within timescales of hours to years, are due primarily to the modulation of the composition and supramolecular organization of the ECM, and are controlled proximally by endocrine, paracrine, and gene regulatory mechanisms [13][14][15][16]. By way of contrast, collagenous structures in echinoderms (starfish, sea-urchins, and their close relatives) can undergo drastic changes in mechanical properties within timescales of less than one second to a few minutes, which result mainly from the neural regulation of factors responsible for cohesion between their collagen fibrils [13][17].
The term ‘mutable’ was first applied to echinoderm collagenous tissue evincing such variable tensility by J.P. Eylers in 1979 (in litt.). It is also known as ‘catch connective tissue’ [18][19], a designation that the present authors avoid because it invites comparison with the ‘catch muscle’ of bivalve molluscs [20] and encourages misconceptions about the possible involvement of actin-myosin-based active contractility in the mechanical adaptability of mutable collagenous structures. It is also inappropriate for certain such structures that exhibit only irreversible destabilization and are likely to lack ‘catch’-like activity, i.e., reversible stiffening and destiffening (see Section 3).
Mutable collagenous tissue (MCT) occurs widely throughout the five extant echinoderm classes, i.e., Asteroidea (starfish), Crinoidea (sea-lilies and featherstars), Echinoidea (sea-urchins), Holothuroidea (sea-cucumbers), and Ophiuroidea (brittlestars and basket stars) [17], and there is indirect evidence for its presence in extinct Paleozoic echinoderm classes [21][22]. Since it also appears to be unique to the Echinodermata, it represents one of the major defining features of the phylum, together with pentaradial symmetry, endoskeletal stereom (calcite meshwork), and the water vascular system [23]. MCT plays an important role in many facets of echinoderm biology including locomotion, defense, alimentation, and reproduction, and is conjectured to have been a major contributor to the evolutionary success of the phylum [24][25][26].
This review first outlines the history of the scientific investigation of MCT, then summarizes current knowledge of its anatomical distribution, organization at the histological, ultrastructural, and molecular levels and physiology—focusing on its mechanical behavior and the regulation of this behavior. It continues with a consideration of the pervasive significance of MCT for the biology of echinoderms in health and disease, and an overview of biomedical and other applications that exploit MCT-derived components or biological principles. It concludes by drawing attention to the more serious deficiencies in current knowledge of MCT biology and suggesting how these should be rectified. The review cites 140 papers on MCT biology, around 60% of the total published since interest in this subject was reawakened in the 1960s (see Section 2). Parts of Section 4 and Section 5 are adapted and updated from refs. [13][17].

References

  1. Baccetti, B. Collagen and animal phylogeny. In Biology of Invertebrate and Lower Vertebrate Collagens; Bairati, A., Garrone, R., Eds.; Plenum Press: New York, NY, USA, 1985; pp. 29–47.
  2. Gordon, M.K.; Hahn, R.A. Collagens. Cell Tissue Res. 2010, 339, 247–257.
  3. Mienaltowski, M.J.; Gonzales, N.L.; Beall, J.M.; Pechanec, M.Y. Basic structure, physiology, and biochemistry of connective tissues and extracellular matrix collagens. In Progress in Heritable Soft Connective Tissue Diseases, 2nd ed.; Halper, J., Ed.; Springer: Cham, Switzerland, 2021; pp. 5–43.
  4. Rahman, M.A. Collagen of extracellular matrix from marine invertebrates and its medical applications. Mar. Drugs 2019, 17, 118.
  5. Jayadev, R.; Sherwood, D.R. Basement membranes. Current Biol. 2017, 27, R207–R211.
  6. Heinoa, J.; Huhtalab, M.; Käpyläa, J.; Johnson, M.S. Evolution of collagen-based adhesion systems. Int. J. Biochem. Cell Biol. 2009, 41, 341–348.
  7. Rasmussen, C.H.; Petersen, D.R.; Moeller, J.B.; Hansson, M.; Dufva, M. Collagen type I improves the differentiation of human embryonic stem cells towards definitive endoderm. PLoS ONE 2015, 10, e0145389.
  8. Wareham, L.K.; Baratta, R.O.; Del Buono, B.J.; Schlumpf, E.; Calkins, D.J. Collagen in the central nervous system: Contributions to neurodegeneration and promise as a therapeutic target. Mol. Neurodegener. 2024, 19, 11.
  9. Langevin, H.M. Connective tissue: A body-wide signaling network? Med. Hypotheses 2006, 66, 1074–1077.
  10. Silver, F.H.; Landis, W.J. Viscoelasticity, energy storage and transmission and dissipation by extracellular matrices in vertebrates. In Collagen: Structure and Mechanics; Fratzl, P., Ed.; Springer: New York, NY, USA, 2008; pp. 133–154.
  11. Jung, H.J.; Fisher, M.B.; Woo, S.L.Y. Role of biomechanics in the understanding of normal, injured, and healing ligaments and tendons. Sports Med. Arthrosc. Rehab. Ther. Technol. 2009, 1, 9.
  12. Matson, A.; Konow, N.; Miller, S.; Konow, P.P.; Roberts, T.J. Tendon material properties vary and are interdependent among turkey hindlimb muscles. J. Exp. Biol. 2012, 215, 3552–3558.
  13. Wilkie, I.C. Basement membranes, brittlestar tendons, and their mechanical adaptability. Biology 2024, 13, 375.
  14. Svensson, R.B.; Heinemeier, K.M.; Couppé, C.; Kjaer, M.; Magnusson, S.P. Effect of aging and exercise on the tendon. J. Appl. Physiol. 2016, 121, 1237–1246.
  15. Yoshida, K.; Jayyosi, C.; Lee, N.; Mahendroo, M.; Myers, K.M. Mechanics of cervical remodelling: Insights from rodent models of pregnancy. Interface Focus 2019, 9, 20190026.
  16. Khalilgharibi, N.; Mao, Y. To form and function: On the role of basement membrane mechanics in tissue development, homeostasis and disease. Open Biol. 2021, 11, 200360.
  17. Candia Carnevali, M.D.; Sugni, M.; Bonasoro, F.; Wilkie, I.C. Mutable collagenous tissue: A concept generator for biomimetic materials and devices. Mar. Drugs 2024, 22, 37.
  18. Motokawa, T. Skin of sea cucumbers: The smart connective tissue that alters mechanical properties in response to external stimuli. J. Aero Aqua Bio-Mech. 2019, 8, 2–5.
  19. Tamori, M.; Yamada, A. Possible mechanisms of stiffness changes induced by stiffeners and softeners in catch connective tissue of echinoderms. Mar. Drugs 2023, 21, 140.
  20. Sugi, H.; Ohno, T.; Moriya, M. Mechanism and function of the catch state in molluscan smooth muscle: A historical perspective. Int. J. Mol. Sci. 2020, 21, 7576.
  21. Saleh, F.; Lefebvre, B.; Dupichaud, C.; Martin, E.L.O.; Nohejlová, M.; Spaccesi, L. Skeletal elements controlled soft-tissue preservation in echinoderms from the Early Ordovician Fezouata Biota. Geobios 2023, 81, 51–66.
  22. Waters, J.A.; Bohatý, J.; Macurda, D.B. Feeding postures as indicators of mutable collagenous tissue in extinct echinoderms. Comm. Biol. 2024, 7, 1516.
  23. Rahman, I.A.; Zamora, S. Origin and early evolution of echinoderms. Ann. Rev. Earth Planet. Sci. 2024, 52, 295–320.
  24. Emson, R.H. Bone idle—A recipe for success? In Echinodermata; Keegan, B.F., O’Connor, B.D.S., Eds.; A.A. Balkema: Rotterdam, The Netherlands, 1985; pp. 25–30.
  25. Motokawa, T. Catch connective tissue: A key character for echinoderms’ success. In Echinoderm Biology; Burke, R.D., Mladenov, P.V., Lambert, P., Parsley, R.L., Eds.; A.A. Balkema: Rotterdam, The Netherlands, 1988; pp. 39–54.
  26. Wilkie, I.C.; Emson, R.H. Mutable collagenous tissues and their significance for echinoderm palaeontology and phylogeny. In Echinoderm Phylogeny and Evolutionary Biology; Paul, C.R.C., Smith, A.B., Eds.; Clarendon Press: Oxford, UK, 1988; pp. 311–330.
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Subjects: Marine & Freshwater Biology
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register : Iain C. Wilkie , M. Daniela Candia Carnevali
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