The Understanding of the Metazoan Skeletal System, Based on the Initial Discoveries with Siliceous and Calcareous Sponges

Overview

Journal Mar Drugs

Publisher MDPI

Specialties Biology
Pharmacology

Date 2017 Jun 13

PMID 28604622

Citations 5

Authors

Werner E G Muller

Heinz C Schroder

Xiaohong Wang

Affiliations

Soon will be listed here.

Abstract

Initiated by studies on the mechanism of formation of the skeletons of the evolutionary oldest still extant multicellular animals, the sponges (phylum Porifera) have provided new insights into the mechanism of formation of the Ca-phosphate/hydroxyapatite skeleton of vertebrate bone. Studies on the formation of the biomineral skeleton of sponges revealed that both the formation of the inorganic siliceous skeletons (sponges of the class of Hexactinellida and Demospongiae) and of the calcareous skeletons (class of Calcarea) is mediated by enzymes (silicatein: polymerization of biosilica; and carbonic anhydrase: deposition of Ca-carbonate). Detailed studies of the initial mineralization steps in human bone-forming cells showed that this process is also controlled by enzymes, starting with the deposition of Ca-carbonate bio-seeds, mediated by carbonic anhydrases-II and -IX, followed by non-enzymatic transformation of the formed amorphous Ca-carbonate deposits into amorphous Ca-phosphate and finally hydroxyapatite crystals. The required phosphate is provided by enzymatic (alkaline phosphatase-mediated) degradation of an inorganic polymer, polyphosphate (polyP), which also acts as a donor for chemically useful energy in this process. These new discoveries allow the development of novel biomimetic strategies for treatment of bone diseases and defects.

Citing Articles

Evaluation of Current Studies to Elucidate Processes in Dental Follicle Cells Driving Osteogenic Differentiation.

Morsczeck C, De Pellegrin M, Reck A, Reichert T Biomedicines. 2023; 11(10).

PMID: 37893160 PMC: 10604663. DOI: 10.3390/biomedicines11102787.

[1, 8]-Naphthyridine derivatives as dual inhibitor of alkaline phosphatase and carbonic anhydrase.

Alrokayan S, Hussain T, Alamery S, Mohammed A, Mahmood A, Ejaz S BMC Chem. 2023; 17(1):142.

PMID: 37880684 PMC: 10599030. DOI: 10.1186/s13065-023-01052-8.

The structural pathology for hypophosphatasia caused by malfunctional tissue non-specific alkaline phosphatase.

Yu Y, Rong K, Yao D, Zhang Q, Cao X, Rao B Nat Commun. 2023; 14(1):4048.

PMID: 37422472 PMC: 10329691. DOI: 10.1038/s41467-023-39833-3.

Aerophobin-1 from the Marine Sponge   Modulates Osteogenesis in Zebrafish Larvae.

Carnovali M, Ciavatta M, Mollo E, Roussis V, Banfi G, Carbone M Mar Drugs. 2022; 20(2).

PMID: 35200664 PMC: 8880152. DOI: 10.3390/md20020135.

Osteodystrophies of jaws.

Santana N, Mehazabin S, Sangeetha K, Kumari M J Oral Maxillofac Pathol. 2021; 24(2):405.

PMID: 33456267 PMC: 7802870. DOI: 10.4103/jomfp.JOMFP_225_19.

References

Nosenko T, Schreiber F, Adamska M, Adamski M, Eitel M, Hammel J . Deep metazoan phylogeny: when different genes tell different stories. Mol Phylogenet Evol. 2013; 67(1):223-33. DOI: 10.1016/j.ympev.2013.01.010. View

Muller W, Schroder H, Schlossmacher U, Grebenjuk V, Ushijima H, Wang X . Induction of carbonic anhydrase in SaOS-2 cells, exposed to bicarbonate and consequences for calcium phosphate crystal formation. Biomaterials. 2013; 34(34):8671-80. DOI: 10.1016/j.biomaterials.2013.07.096. View

Kruse M, Muller I, Muller W . Early evolution of metazoan serine/threonine and tyrosine kinases: identification of selected kinases in marine sponges. Mol Biol Evol. 1997; 14(12):1326-34. DOI: 10.1093/oxfordjournals.molbev.a025742. View

Krasko A, Gamulin V, Seack J, Steffen R, Schroder H, Muller W . Cathepsin, a major protease of the marine sponge Geodia cydonium: purification of the enzyme and molecular cloning of cDNA. Mol Mar Biol Biotechnol. 1998; 6(4):296-307. View

Wang X, Ackermann M, Wang S, Tolba E, Neufurth M, Feng Q . Amorphous polyphosphate/amorphous calcium carbonate implant material with enhanced bone healing efficacy in a critical-size defect in rats. Biomed Mater. 2016; 11(3):035005. DOI: 10.1088/1748-6041/11/3/035005. View

Li W, Chen W, Zhou P, Cao L, Yu L . Influence of initial pH on the precipitation and crystal morphology of calcium carbonate induced by microbial carbonic anhydrase. Colloids Surf B Biointerfaces. 2012; 102:281-7. DOI: 10.1016/j.colsurfb.2012.08.042. View

Jekely G, Paps J, Nielsen C . The phylogenetic position of ctenophores and the origin(s) of nervous systems. Evodevo. 2015; 6:1. PMC: 4406211. DOI: 10.1186/2041-9139-6-1. View

Seack J, Pancer Z, Muller I, Muller W . Molecular cloning and primary structure of a Rhesus (Rh)-like protein from the marine sponge Geodia cydonium. Immunogenetics. 1997; 46(6):493-8. DOI: 10.1007/s002510050310. View

Schroder H, Wang X, Manfrin A, Yu S, Grebenjuk V, Korzhev M . Acquisition of structure-guiding and structure-forming properties during maturation from the pro-silicatein to the silicatein form. J Biol Chem. 2012; 287(26):22196-205. PMC: 3381181. DOI: 10.1074/jbc.M112.351486. View

10.

Muller W, Tolba E, Schroder H, Neufurth M, Wang S, Link T . A new printable and durable N,O-carboxymethyl chitosan-Ca-polyphosphate complex with morphogenetic activity. J Mater Chem B. 2020; 3(8):1722-1730. DOI: 10.1039/c4tb01586j. View

11.

Beniash E . Biominerals--hierarchical nanocomposites: the example of bone. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2010; 3(1):47-69. PMC: 3012754. DOI: 10.1002/wnan.105. View

12.

Muller W, Schroder H, Tolba E, Diehl-Seifert B, Wang X . Mineralization of bone-related SaOS-2 cells under physiological hypoxic conditions. FEBS J. 2015; 283(1):74-87. DOI: 10.1111/febs.13552. View

13.

Muller W, Schroder H, Burghard Z, Pisignano D, Wang X . Silicateins--a novel paradigm in bioinorganic chemistry: enzymatic synthesis of inorganic polymeric silica. Chemistry. 2013; 19(19):5790-804. DOI: 10.1002/chem.201204412. View

14.

Simion P, Philippe H, Baurain D, Jager M, Richter D, Di Franco A . A Large and Consistent Phylogenomic Dataset Supports Sponges as the Sister Group to All Other Animals. Curr Biol. 2017; 27(7):958-967. DOI: 10.1016/j.cub.2017.02.031. View

15.

Worheide G, Dohrmann M, Erpenbeck D, Larroux C, Maldonado M, Voigt O . Deep phylogeny and evolution of sponges (phylum Porifera). Adv Mar Biol. 2012; 61:1-78. DOI: 10.1016/B978-0-12-387787-1.00007-6. View

16.

Pancer Z, Kruse M, Muller I, Muller W . On the origin of Metazoan adhesion receptors: cloning of integrin alpha subunit from the sponge Geodia cydonium. Mol Biol Evol. 1997; 14(4):391-8. DOI: 10.1093/oxfordjournals.molbev.a025775. View

17.

Boonrungsiman S, Gentleman E, Carzaniga R, Evans N, McComb D, Porter A . The role of intracellular calcium phosphate in osteoblast-mediated bone apatite formation. Proc Natl Acad Sci U S A. 2012; 109(35):14170-5. PMC: 3435222. DOI: 10.1073/pnas.1208916109. View

18.

Muller W, Schlossmacher U, Schroder H, Lieberwirth I, Glasser G, Korzhev M . Enzyme-accelerated and structure-guided crystallization of calcium carbonate: role of the carbonic anhydrase in the homologous system. Acta Biomater. 2013; 10(1):450-62. DOI: 10.1016/j.actbio.2013.08.025. View

19.

Rey C, Kim H, Gerstenfeld L, Glimcher M . Characterization of the apatite crystals of bone and their maturation in osteoblast cell culture: comparison with native bone crystals. Connect Tissue Res. 1996; 35(1-4):343-9. DOI: 10.3109/03008209609029210. View

20.

Deans M, Peterson J, Wong G . Mammalian Otolin: a multimeric glycoprotein specific to the inner ear that interacts with otoconial matrix protein Otoconin-90 and Cerebellin-1. PLoS One. 2010; 5(9):e12765. PMC: 2939893. DOI: 10.1371/journal.pone.0012765. View