276
Views
0
CrossRef citations to date
0
Altmetric
REVIEW

The Physiological Inorganic Polymers Biosilica and Polyphosphate as Key Drivers for Biomedical Materials in Regenerative Nanomedicine

ORCID Icon, ORCID Icon, , ORCID Icon & ORCID Icon
Pages 1303-1337 | Received 24 Oct 2023, Accepted 18 Jan 2024, Published online: 08 Feb 2024

References

  • Kenny NJ, Francis WR, Rivera-Vicéns RE, et al. Tracing animal genomic evolution with the chromosomal-level assembly of the freshwater sponge Ephydatia muelleri. Nat Commun. 2020;11(1):3676. doi:10.1038/s41467-020-17397-w
  • Pertea M, Salzberg SL. Between a chicken and a grape: estimating the number of human genes. Genome Biol. 2010;11(5):206. doi:10.1186/gb-2010-11-5-206
  • Williams D. The essential materials paradigms for regenerative medicine. JOM. 2011;63(4):51–55. doi:10.1007/s11837-011-0067-5
  • Chiang B, Essick E, Ehringer W, et al. Enhancing skin wound healing by direct delivery of intracellular adenosine triphosphate. Am J Surg. 2007;193(2):213–218. doi:10.1016/j.amjsurg.2006.08.069
  • Müller WEG, Schröder HC, Wang XH. Inorganic polyphosphates as storage for and generator of metabolic energy in the extracellular matrix. Chem Rev. 2019;119(24):12337–12374. doi:10.1021/acs.chemrev.9b00460
  • Trackman PC. Diverse biological functions of extracellular collagen processing enzymes. J Cell Biochem. 2005;96(5):927–937. doi:10.1002/jcb.20605
  • Wang XH, Schröder HC, Müller WEG. Enzyme-based biosilica and biocalcite: biomaterials for the future in regenerative medicine. Trends Biotechnol. 2014;32(9):441–447. doi:10.1016/j.tibtech.2014.05.004
  • Wang Y, Li M, Li P, et al. Progress and applications of polyphosphate in bone and cartilage regeneration. Biomed Res Int. 2019;2019:5141204. doi:10.1155/2019/5141204
  • Schröder HC, Wang XH, Neufurth M, Wang SF, Tan R, Müller WEG. Inorganic polymeric materials for injured tissue repair: biocatalytic formation and exploitation. Biomedicines. 2022;10(3):658. doi:10.3390/biomedicines10030658
  • Vallesius F. Controversiarum medicarum et philosophicarum. W.C. Hanoviae: Marnium; 1606.
  • Trembley A. Mémoires pour servir à l’histoire d’un genre de polypes d’eau douce à bra sen forme de cornes. Verbeek: Leide; 1744.
  • Galtsoff PS. The amoeboid movement of dissociated sponge cells. Biol Bull. 1923;45(3):153–161. doi:10.2307/1536625
  • Müller WEG. The stem cell concept in sponges (Porifera): metazoan traits. Semin Cell Dev Biol. 2006;17(4):481–491. doi:10.1016/j.semcdb.2006.05.006
  • Morgan TH. Regeneration. New York/London: Macmillan; 1901.
  • Bely AE, Nyberg KG. Evolution of animal regeneration: re-emergence of a field. Trends Ecol Evol. 2010;25(3):161–170. doi:10.1016/j.tree.2009.08.005
  • Ereskovsky A, Borisenko IE, Bolshakov FV, Lavrov AI. Whole-body regeneration in sponges: diversity, fine mechanisms, and future prospects. Genes. 2021;12(4):506. doi:10.3390/genes12040506
  • Ricci L, Srivastava M. Wound-induced cell proliferation during animal regeneration. Wiley Interdiscip Rev Dev Biol. 2018;7(5):e321. doi:10.1002/wdev.321
  • Wu YC, Franzenburg S, Ribes M, Pita L. Wounding response in Porifera (sponges) activates ancestral signaling cascades involved in animal healing, regeneration, and cancer. Sci Rep. 2022;12(1):1307. doi:10.1038/s41598-022-05230-x
  • Cary GA, Wolff A, Zueva O, Pattinato J, Hinman VF. Analysis of sea star larval regeneration reveals conserved processes of whole-body regeneration across the metazoa. BMC Biol. 2019;17(1):16. doi:10.1186/s12915-019-0633-9
  • Rybicka-Jasińska K, Derr JB, Vullev VI. What defines biomimetic and bioinspired science and engineering?. Pure Appl Chem. 2021;93(11):1275–1292. doi:10.1515/pac-2021-0323
  • Gough A, Soto-Gutierrez A, Vernetti L, Ebrahimkhani MR, Stern AM, Taylor DL. Human biomimetic liver microphysiology systems in drug development and precision medicine. Nat Rev Gastroenterol Hepatol. 2021;18(4):252–268. doi:10.1038/s41575-020-00386-1
  • Benyus JM. Biomimicry: Innovation Inspired by Nature. Perennial, New York: HaperCollins Pub; 2002.
  • Furth JJ, Cohen SS. Inhibition of mammalian DNA polymerase by the 5’-triphosphate of 1-β-D-arabinofuranosylcytosine and the 5’-triphosphate of 9-β-D-arabinofuranoxyladenine. Cancer Res. 1968;28(10):2061–2067.
  • Schabel FM. The antiviral activity of 9-β-D-arabinofuranosyladenine (ARA-A). Chemotherapy. 1968;13(6):321–338. doi:10.1159/000220567
  • Müller WEG, Zahn RK, Bittlingmaier K, Falke D. Inhibition of herpesvirus DNA-synthesis by 9-ß-D-arabinofuranosyladenosine in vitro and in vivo. Ann New York Acad Sci. 1977;284(1):34–48. doi:10.1111/j.1749-6632.1977.tb21935.x
  • Seack J, Pancer Z, Müller IM, Müller WEG. Molecular cloning and primary structure of a Rhesus (Rh)-like protein from the marine sponge Geodia cydonium. Immunogenetics. 1997;46(6):493–498. doi:10.1007/s002510050310
  • Müller WEG, Blumbach B, Müller IM. Evolution of the innate and adaptive immune systems: relationships between potential immune molecules in the lowest metazoan phylum [Porifera] and those in vertebrates. Transplantation. 1999;68(9):1215–1227. doi:10.1097/00007890-199911150-00001
  • Krasko A, Lorenz B, Batel R, Schröder HC, Müller IM, Müller WEG. Expression of silicatein and collagen genes in the marine sponge Suberites domuncula is controlled by silicate and myotrophin. Eur J Biochem. 2000;267(15):4878–4887. doi:10.1046/j.1432-1327.2000.01547.x
  • Müller WEG, Wang XH, Grebenjuk V, et al. Common genetic denominators for Ca++-based skeleton in metazoan: role of osteoclast stimulating factor and carbonic anhydrase in a calcareous sponge. PLoS One. 2012;7(4):e34617. doi:10.1371/journal.pone.0034617
  • Müller WEG, Ackermann M, Al-Nawas B, et al. Amplified morphogenetic and bone forming activity of amorphous versus crystalline calcium phosphate/polyphosphate. Acta Biomater. 2020;118:233–247. doi:10.1016/j.actbio.2020.10.023
  • Müller WEG, Wendt K, Geppert C, Wiens M, Reiber A, Schröder HC. Novel photoreception system in sponges? Unique transmission properties of the stalk spicules from the hexactinellid Hyalonema sieboldi. Biosens Bioelectron. 2006;21(7):1149–1155. doi:10.1016/j.bios.2005.04.017
  • Liu S, Yu JM, Gan YC, et al. Biomimetic natural biomaterials for tissue engineering and regenerative medicine: new biosynthesis methods, recent advances, and emerging applications. Mil Med Res. 2023;10(1):16. doi:10.1186/s40779-023-00448-w
  • Omidian H, Wilson RL, Babanejad N. Bioinspired polymers: transformative applications in biomedicine and regenerative medicine. Life. 2023;13:1673.
  • Weiner S, Dove PM. An overview of biomineralization processes and the problem of the vital effect. Rev Mineral Geochem. 2003;54(1):1–29. doi:10.2113/0540001
  • Westbroek P. Biological metal accumulation and biomineralization in a geological perspective. In: Westbroek P, de Jong EW, editors. Biomineralization and Biological Metal Accumulation. Dordrecht, Holland: D. Reidel Publishing Co; 1983:1–11.
  • Krasko A, Gamulin V, Seack J, Steffen R, Schröder HC, Müller WEG. Cathepsin, a major protease of the marine sponge Geodia cydonium: purification of the enzyme and molecular cloning of cDNA. Molec Marine Biol Biotechnol. 1997;6:296–307.
  • Shimizu K, Cha J, Stucky GD, Morse DE. Silicatein α: cathepsin L-like protein in sponge biosilica. Proc Natl Acad Sci USA. 1998;95(11):6234–6238. doi:10.1073/pnas.95.11.6234
  • Mărgineanu DG. Equilibrium and non-equilibrium approaches in biomembrane thermodynamics. Arch Internat Physiol Biochim. 1987;95:381–422.
  • Seibel MJ. Biochemical markers of bone turnover. Part I Biochemistry and variability. Clin Biochem Rev. 2005;26(4):97–122.
  • Harris H. The human alkaline phosphatases: what we know and what we don’t know. Clin Chim Acta. 1990;186(2):133–150. doi:10.1016/0009-8981(90)90031-M
  • Schini M, Vilaca T, Gossiel F, Salam S, Eastell R. Bone turnover markers: basic biology to clinical applications. Endocr Rev. 2023;44:417–473.
  • Müller WEG, Schröder HC, Schloßmacher U, Grebenjuk VA, Ushijima H, Wang XH. Induction of carbonic anhydrase in SaOS-2 cells, exposed to bicarbonate and consequences for calcium phosphate crystal formation. Biomaterials. 2013;34(34):8671–8680. doi:10.1016/j.biomaterials.2013.07.096
  • Andrilli LHS, Sebinelli HG, Favarin BZ, et al. NPP1 and TNAP hydrolyze ATP synergistically during biomineralization. Purinergic Signal. 2023;19:353–366.
  • Morrison MS, Turin L, King BF, Burnstock G, Arnett TR. ATP is a potent stimulator of the activation and formation of rodent osteoclasts. J Physiol. 1998;511(2):495–500. doi:10.1111/j.1469-7793.1998.495bh.x
  • de Paula FJ, Rosen CJ. Bone remodeling and energy metabolism: new perspectives. Bone Res. 2013;1:72–84.
  • Motyl KJ, Guntur AR, Carvalho AL, Rosen CJ. Energy metabolism of bone. Toxicol Pathol. 2017;45(7):887–893. doi:10.1177/0192623317737065
  • Müller WEG, Wang SF, Ackermann M, et al. Biologization of allogeneic bone grafts with polyphosphate: a route to a biomimetic periosteum. Adv Funct Mater. 2019;29(44):1905220. doi:10.1002/adfm.201905220
  • Schepler H, Neufurth M, Wang SF, .et al. Acceleration of chronic wound healing by bio-inorganic polyphosphate: in vitro studies and first clinical applications. Theranostics. 2022;12(1):18–34. doi:10.7150/thno.67148
  • Müller WEG, Schepler H, Neufurth M, et al. The physiological polyphosphate as a healing biomaterial for chronic wounds: crucial roles of its antibacterial and unique metabolic energy supplying properties. J Mat Sci Technol. 2023;135:170–185.
  • Müller WEG, Wang SF, Neufurth M, Kokkinopoulou M, Feng Q, Schröder HC. Polyphosphate as a donor of high-energy phosphate for the synthesis of ADP and ATP. J Cell Sci. 2017;130:2747–2756.
  • Müller WEG, Ackermann M, Tolba E, et al. Role of ATP during the initiation of microvascularization. Acceleration of an autocrine sensing mechanism facilitating chemotaxis by inorganic polyphosphate. Biochem J. 2018;475(20):3255–3273. doi:10.1042/BCJ20180535
  • Michaëlsson E, Malmström V, Reis S, Engström A, Burkhardt H, Holmdahl R. T cell recognition of carbohydrates on type II collagen. J Exp Med. 1994;180:745–749.
  • Müller WEG, Wiens M, Adell T, Gamulin V, Schröder HC, Müller IM. Bauplan of Urmetazoa: basis for genetic complexity of Metazoa. Intern Rev Cytol. 2004;235:53–92.
  • Uriz MJ, Turon X, Becerro MA, Agell G. Siliceous spicules and skeleton frameworks in sponges: origin, diversity, ultrastructural patterns, and biological functions. Microsc Res Tech. 2003;62:279–299.
  • Müller WEG, Blumbach B, Wagner-Hülsmann C, Lessel U. Galectins in the phylogenetically oldest metazoa, the sponges [Porifera]. Trends Glycosci Glycotechnol. 1997;9(45):123–130. doi:10.4052/tigg.9.123
  • Weaver JC, Aizenberg J, Fantner GE, et al. Hierarchical assembly of the siliceous skeletal lattice of the hexactinellid sponge Euplectella aspergillum. J Struct Biol. 2007;158(1):93–106. doi:10.1016/j.jsb.2006.10.027
  • Wang XH, Schröder HC, Müller WEG. Giant siliceous spicules from the deep-sea glass sponge Monorhaphis chuni: morphology, biochemistry and molecular biology. Int Rev Cell Mol Biol. 2009;273:69–115.
  • Zhou Y, Shimizu K, Cha JN, Stucky GD, Morse DE. Efficient catalysis of polysiloxane synthesis by silicatein α requires specific hydroxy and imidazole functionalities. Angew Chem Int Ed Engl. 1999;38:779–782.
  • Schröder HC, Borejko A, Krasko A, Reiber A, Schwertner H, Müller WEG. Mineralization of SaOS-2 cells on enzymatically (Silicatein) modified bioactive osteoblast-stimulating surfaces. J Biomed Mat Res Part B Appl Biomater. 2005;75B:387–392.
  • Schloßmacher U, Wiens M, Schröder HC, Wang XH, Jochum KP, Müller WEG. Silintaphin-1: interaction with silicatein during structure-guiding biosilica formation. FEBS J. 2011;278(7):1145–1155. doi:10.1111/j.1742-4658.2011.08040.x
  • Müller WEG, Boreiko A, Wang XH, et al. Silicateins, the major biosilica forming enzymes present in demosponges: protein analysis and phylogenetic relationship. Gene. 2007;395(1–2):62–71. doi:10.1016/j.gene.2007.02.014
  • Tabatabaei Dakhili SY, Caslin SA, Faponle AS, Quayle P, de Visser SP, Wong LS. Recombinant silicateins as model biocatalysts in organosiloxane chemistry. Proc Natl Acad Sci USA. 2017;114:E5285–E5291.
  • Müller WEG, Wiens M, Batel R, et al. Establishment of a primary cell culture from a sponge: primmorphs from Suberites domuncula. Mar Ecol Progr Ser. 1999;178:205–219. doi:10.3354/meps178205
  • Walenta S, Dötsch J, Mueller-Klieser W. ATP concentrations in multicellular tumor spheroids assessed by single photon imaging and quantitative bioluminescence. Eur J Cell Biol. 1990;52(2):389–393.
  • Boury-Esnault N, Rützler K. Thesaurus of sponge morphology. Smithson Contrib Zool. 1997;596(596):1–55. doi:10.5479/si.00810282.596
  • Weiner S, Mahamid J, Politi Y, Ma Y, Addadi L. Overview of the amorphous precursor phase strategy in biomineralization. Frontiers Mat Sci China. 2009;3:104–108.
  • Jackson DJ, Macis L, Reitner J, Degnan BM, Wörheide G. Sponge paleogenomics reveals an ancient role for carbonic anhydrase in skeletogenesis. Science. 2007;316(5833):1893–1895. doi:10.1126/science.1141560
  • Tolba E, Müller WEG, El-Hady BMA, et al. High biocompatibility and improved osteogenic potential of amorphous calcium carbonate/vaterite. J Mat Chem B. 2016;4(3):376–386. doi:10.1039/C5TB02228B
  • Müller WEG, Neufurth M, Ushijima H, et al. Molecular and biochemical approach for understanding the transition of amorphous to crystalline calcium phosphate deposits in human teeth. Dental Mater. 2022;38:2014–2029.
  • Crundwell FK. On the mechanism of the dissolution of quartz and silica in aqueous solutions. ACS Omega. 2017;2(3):1116–1127. doi:10.1021/acsomega.7b00019
  • Schröder HC, Perović-Ottstadt S, Rothenberger M, et al. Silica transport in the demosponge Suberites domuncula: fluorescence emission analysis using the PDMPO probe and cloning of a potential transporter. Biochem J. 2004;381(3):665–673. doi:10.1042/BJ20040463
  • Müller WEG, Schloßmacher U, Wang XH, et al. Poly(silicate)-metabolizing silicatein in siliceous spicules and silicasomes of demosponges comprises dual enzymatic activities (silica-polymerase and silica-esterase). FEBS J. 2008;275:362–370.
  • Wang XH, Schröder HC, Brandt D, et al. Sponge biosilica formation involves syneresis following polycondensation in vivo. Chembiochem. 2011;12(15):2316–2324. doi:10.1002/cbic.201100345
  • Belton DJ, Deschaume O, Patwardhan SV, Perry CC. A solution study of silica condensation and speciation with relevance to in vitro investigations of biosilicification. J Phys Chem B. 2010;114(31):9947–9955. doi:10.1021/jp101347q
  • Belton DJ, Deschaume O, Perry CC. An overview of the fundamentals of the chemistry of silica with relevance to biosilicification and technological advances. FEBS J. 2012;279(10):1710–1720. doi:10.1111/j.1742-4658.2012.08531.x
  • Cha JN, Shimizu K, Zhou Y, et al. Silicatein filaments and subunits from a marine sponge direct the polymerization of silica and silicones in vitro. Proc Natl Acad Sci USA. 1999;96:361–365.
  • Müller WEG, Belikov SI, Tremel W, et al. Siliceous spicules in marine demosponges (example Suberites domuncula). Micron. 2006;37(2):107–120. doi:10.1016/j.micron.2005.09.003
  • Schröder HC, Wang XH, Manfrin A, et al. Silicatein: acquisition of structure-guiding and structure-forming properties during maturation from the pro-silicatein to the silicatein form. J Biol Chem. 2012;287(26):22196–22205. doi:10.1074/jbc.M112.351486
  • Stöber W, Fink A, Bohn E. Controlled growth of monodisperse silica spheres in the micron size range. J Colloid Interface Sci. 1968;26(1):62–69. doi:10.1016/0021-9797(68)90272-5
  • Müller WEG, Boreiko A, Wang XH, et al. Morphogenetic activity of silica and bio-silica on the expression of genes, controlling biomineralization using SaOS-2 cells. Calcif Tissue Int. 2007;81(5):382–393. doi:10.1007/s00223-007-9075-4
  • Görlich S, Pawolski D, Zlotnikov I, Kröger N. Control of biosilica morphology and mechanical performance by the conserved diatom gene Silicanin-1. Commun Biol. 2019;2(1):245. doi:10.1038/s42003-019-0436-0
  • Ege D, Zheng K, Boccaccini AR. Borate Bioactive Glasses (BBG): bone regeneration, wound healing applications, and future directions. ACS Appl Bio Mater. 2022;5(8):3608–3622. doi:10.1021/acsabm.2c00384
  • Wang SF, Wang XH, Draenert FG, et al. Bioactive and biodegradable silica biomaterial for bone regeneration. Bone. 2014;67:292–304. doi:10.1016/j.bone.2014.07.025
  • Carlisle EM. Silicon: an essential element for the chick. Science. 1972;178(4061):619–621. doi:10.1126/science.178.4061.619
  • Burton EJ, Scholey DV, Belton DJ, Bedford MR, Perry CC. Efficacy and stability of a novel silica supplement for improving bone development in broilers. Br Poult Sci. 2020;61(6):719–724. doi:10.1080/00071668.2020.1799328
  • Wiens M, Wang XH, Schloßmacher U, et al. Osteogenic potential of bio-silica on human osteoblast-like (SaOS-2) cells. Calcif Tissue Int. 2010;87(6):513–524. doi:10.1007/s00223-010-9408-6
  • Pettersson LF, Kingham PJ, Wiberg M, Kelk P. In vitro osteogenic differentiation of human mesenchymal stem cells from jawbone compared with dental tissue. Tissue Eng Regen Med. 2017;14:763–774.
  • Pautke C, Vogt S, Kreutzer K, et al. Characterization of eight different tetracyclines: advances in fluorescence bone labeling. J Anat. 2010;217(1):76–82. doi:10.1111/j.1469-7580.2010.01237.x
  • Hench LL. Bioceramics. J Am Ceram Soc. 1998;81(7):1705–1728. doi:10.1111/j.1151-2916.1998.tb02540.x
  • Wang Y, Jiang S, Pan H, Tang R. Less is more: silicate in the crystallization of hydroxyapatite in simulated body fluids. CrystEngComm. 2016;18(3):379–383. doi:10.1039/C5CE01861G
  • Kellermeier M, Melero-García E, Glaab F, et al. Stabilization of amorphous calcium carbonate in inorganic silica-rich environments. J Am Chem Soc. 2010;132(50):17859–17866. doi:10.1021/ja106959p
  • Sahai N. Modeling apatite nucleation in the human body and in the geochemical environment. Am J Sci. 2000;305(6–8):661–672. doi:10.2475/ajs.305.6-8.661
  • Sahai N, Tossell JA. Molecular orbital study of apatite (Ca5(PO4)3OH) nucleation at silica bioceramic surfaces. J Phys Chem B. 2000;104(18):4321–4322. doi:10.1021/jp9935889
  • Salih E, Flückiger R. Complete topographical distribution of both the in vivo and in vitro phosphorylation sites of bone sialoprotein and their biological significance. J Biol Chem. 2004;279(19):19808–19815. doi:10.1074/jbc.M310299200
  • Wysokowski M, Jesionowski T, Ehrlich H. Biosilica as a source for inspiration in biological materials science. Amer Mineral. 2018;103:665–691.
  • Lorenz B, Batel R, Bachinski N, Müller WEG, Schröder HC. Purification and characterization of two exopolyphosphatases from the marine sponge Tethya lyncurium. Biochim Biophys Acta. 1995;1245(1):17–28. doi:10.1016/0304-4165(95)00067-L
  • Kulaev IS. Biochemistry of inorganic polyphosphates. Rev Physiol Biochem Pharmacol. 1975;73:131–158.
  • Kumble KD, Kornberg A. Inorganic polyphosphate in mammalian cells and tissues. J Biol Chem. 1995;270(11):5818–5822. doi:10.1074/jbc.270.11.5818
  • Achbergerová L, Nahálka J. Polyphosphate--an ancient energy source and active metabolic regulator. Microb Cell Fact. 2011;10(1):63. doi:10.1186/1475-2859-10-63
  • Desfougères Y, Saiardi A, Azevedo C. Inorganic polyphosphate in mammals: where’s Wally?. Biochem Soc Trans. 2020;48(1):95–101. doi:10.1042/BST20190328
  • Docampo R, Huang G. Acidocalcisomes of eukaryotes. Curr Opin Cell Biol. 2016;41:66–72. doi:10.1016/j.ceb.2016.04.007
  • Lander N, Cordeiro C, Huang G, Docampo R. Polyphosphate and acidocalcisomes. Biochem Soc Trans. 2016;44(1):1–6. doi:10.1042/BST20150193
  • Babes V. Beobachtungen über die metachromatischen Körperchen, Sporenbildung, Verzweigung, Kolben- und Kapselbildung pathogener Bakterien. Zentralbl Bakteriol Parasitenkd Infektionskr Hyg. 1895;20:412–420.
  • Meyer A. Orientierende Untersuchungen über Verbreitung, Morphologie, und Chemie des Volutins. Bot Zeit. 1904;62:113–152.
  • Ruiz FA, Lea CR, Oldfield E, Docampo R. Human platelet dense granules contain polyphosphate and are similar to acidocalcisomes of bacteria and unicellular eukaryotes. J Biol Chem. 2004;279(43):44250–44257. doi:10.1074/jbc.M406261200
  • Langen P, Hucho F. Karl Lohmann and the discovery of ATP. Angew Chem Int Ed Engl. 2008;47(10):1824–1827. doi:10.1002/anie.200702929
  • Langen P, Liss E, Lohmann K. Art, Bildung und Umsatz der Polyphosphate der Hefe [Formation and turnover of polyphosphates in yeast]. In: Jacquinot P, editor. Acides Ribonucléiques Et Polyphosphates: Structure, Synthèse Et Fonctions. CNRS No 105. Paris: Centre National de la Recherche Scientifique; 1962:604–614.
  • Lohmann K. Über das Vorkommen, und den Umsatz von Pyrophosphat in Zellen. I. Mitteilung: nachweis und Isolierung des Pyrophosphates. Biochem Z. 1928;202:466–493.
  • Bowlin MQ, Gray MJ. Inorganic polyphosphate in host and microbe biology. Trends Microbiol. 2021;29(11):1013–1023. doi:10.1016/j.tim.2021.02.002
  • Hooley P, Whitehead MP, Brown MR. Eukaryote polyphosphate kinases: is the ‘Kornberg’ complex ubiquitous?. Trends Biochem Sci. 2008;33(12):577–582. doi:10.1016/j.tibs.2008.09.007
  • Pavlov E, Zakharian E, Bladen C, et al. A large, voltage-dependent channel, isolated from mitochondria by water-free chloroform extraction. Biophys J. 2005;88(4):2614–2625. doi:10.1529/biophysj.104.057281
  • Pavlov E, Aschar-Sobbi R, Campanella M, Turner RJ, Gomez-Garcia MR, Abramov AY. Inorganic polyphosphate and energy metabolism in mammalian cells. J Biol Chem. 2010;285(13):9420–9428. doi:10.1074/jbc.M109.013011
  • Abramov AY, Fraley C, Diao CT, et al. Targeted polyphosphatase expression alters mitochondrial metabolism and inhibits calcium-dependent cell death. Proc Natl Acad Sci USA. 2007;104(46):18091–18096. doi:10.1073/pnas.0708959104
  • Budavari S. The Merck Index: An Encyclopedia of Chemicals, Drugs, and Biologicals. 11th ed. Rahway, NJ: Merck & Co; 1989.
  • Soga N, Kinosita K, Yoshida M, Suzuki T. Efficient ATP synthesis by thermophilic Bacillus Fo F1-ATP synthase. FEBS J. 2011;278(15):2647–2654. doi:10.1111/j.1742-4658.2011.08191.x
  • Hothorn M, Neumann H, Lenherr ED, et al. Catalytic core of a membrane-associated eukaryotic polyphosphate polymerase. Science. 2009;324(5926):513–516. doi:10.1126/science.1168120
  • Guan Z, Chen J, Liu R, et al. The cytoplasmic synthesis and coupled membrane translocation of eukaryotic polyphosphate by signal-activated VTC complex. Nat Commun. 2023;14(1):718. doi:10.1038/s41467-023-36466-4
  • Verhoef JJ, Barendrecht AD, Nickel KF, et al. Polyphosphate nanoparticles on the platelet surface trigger contact system activation. Blood. 2017;129(12):1707–1717. doi:10.1182/blood-2016-08-734988
  • Morrissey JH, Smith SA. Polyphosphate as modulator of hemostasis, thrombosis, and inflammation. J Thromb Haemost. 2015;13(Suppl 1):S92–S97. doi:10.1111/jth.12896
  • Polasek J. Platelet lysosomal acid phosphatase enzyme activity as a marker of platelet procoagulant activity. Blood Transfus. 2009;7(2):155–156. doi:10.2450/2008.0053-08
  • Buxton IL, Kaiser RA, Oxhorn BC, Cheek DJ. Evidence supporting the nucleotide axis hypothesis: ATP release and metabolism by coronary endothelium. Am J Physiol Heart Circ Physiol. 2001;281(4):H1657–H1666. doi:10.1152/ajpheart.2001.281.4.H1657
  • Weitz JI, Fredenburgh JC. Platelet polyphosphate: the long and the short of it. Blood. 2017;129(12):1574–1575. doi:10.1182/blood-2017-01-761593
  • Sharda A, Flaumenhaft R. The life cycle of platelet granules. F1000Res. 2018;7:236. doi:10.12688/f1000research.13283.1
  • Tyagi T, Jain K, Gu SX, et al. A guide to molecular and functional investigations of platelets to bridge basic and clinical sciences. Nat Cardiovasc Res. 2022;1(3):223–237. doi:10.1038/s44161-022-00021-z
  • Lorenz B, Leuck J, Köhl D, Müller WEG, Schröder HC. Anti-HIV-1 activity of inorganic polyphosphates. J Acquir Immune Defic Syndr Hum Retrovirol. 1997;14(2):110–118. doi:10.1097/00042560-199702010-00003
  • Lorenz B, Schröder HC. Mammalian intestinal alkaline phosphatase acts as highly active exopolyphosphatase. Biochim Biophys Acta. 2001;1547(2):254–261. doi:10.1016/S0167-4838(01)00193-5
  • Ho-Tin-Noé B, Boulaftali Y, Camerer E. Platelets and vascular integrity: how platelets prevent bleeding in inflammation. Blood. 2018;131(3):277–288. doi:10.1182/blood-2017-06-742676
  • Harrison P, Alsousou J, Andia I; Subcommittee on Platelet Physiology. The use of platelets in regenerative medicine and proposal for a new classification system: guidance from the SSC of the ISTH. J Thromb Haemost. 2018;16(9):1895–1900. doi:10.1111/jth.14223
  • Bizzozero J. Ueber einen neuen Formbestandtheil des Blutes und dessen Rolle bei der Thrombose und der Blutgerinnung. Virchow’s Arch Pathol Anat Physiol Klin Med. 1882;90(2):261–332. doi:10.1007/BF01931360
  • Roewe J, Stavrides G, Strueve M, et al. Bacterial polyphosphates interfere with the innate host defense to infection. Nat Commun. 2020;11(1):4035. doi:10.1038/s41467-020-17639-x
  • Ruggeri ZM, Mendolicchio GL. Adhesion mechanisms in platelet function. Circ Res. 2007;100(12):1673–1685. doi:10.1161/01.RES.0000267878.97021.ab
  • Jackson LE, Kariuki BM, Smith ME, Barralet JE, Wright AJ. Synthesis and structure of a calcium polyphosphate with an unique criss-cross arrangement of helical phosphate chains. Chem Mater. 2005;17(18):4642–4646. doi:10.1021/cm050984x
  • Shiba T, Nishimura D, Kawazoe Y, et al. Modulation of mitogenic activity of fibroblast growth factors by inorganic polyphosphate. J Biol Chem. 2003;278(29):26788–26792. doi:10.1074/jbc.M303468200
  • Lorenz B, Marmé S, Müller WEG, Unger K, Schröder HC. Preparation and use of polyphosphate-modified zirconia for purification of nucleic acids and proteins. Anal Biochem. 1994;16(1):118–126. doi:10.1006/abio.1994.1015
  • Müller WEG, Tolba E, Schröder HC, et al. A new polyphosphate calcium material with morphogenetic activity. Mater Lett. 2015;148:166. doi:10.1016/j.matlet.2015.02.070
  • Wang XH, Ackermann M, Tolba E, et al. Artificial cartilage bio-matrix formed of hyaluronic acid and Mg2+-polyphosphate. Eur Cell Mater. 2016;32:271–283. doi:10.22203/eCM.v032a18
  • Müller WEG, Tolba E, Ackermann M, et al. Fabrication of amorphous strontium polyphosphate microparticles that induce mineralization of bone cells in vitro and in vivo. Acta Biomater. 2017;50:89–101. doi:10.1016/j.actbio.2016.12.045
  • Müller WEG, Neufurth M, Wang SF, et al. Amorphous, smart, and bioinspired polyphosphate nano/microparticles: a biomaterial for regeneration and repair of osteo-articular impairments in-situ. Int J Mol Sci. 2018;19(2):427. doi:10.3390/ijms19020427
  • Müller WEG, Schröder HC, Neufurth M, Wang XH. An unexpected biomaterial against SARS-CoV-2: bio-polyphosphate blocks binding of the viral spike to the cell receptor. Mater Today. 2021;51:504–524. doi:10.1016/j.mattod.2021.07.029
  • Neufurth M, Wang XH, Tolba E, et al. The inorganic polymer, polyphosphate, blocks binding of SARS-CoV-2 spike protein to ACE2 receptor at physiological concentrations. Biochem Pharmacol. 2020;182:114215. doi:10.1016/j.bcp.2020.114215
  • Ferrucci V, Kong DY, Asadzadeh F, et al. Long-chain polyphosphates impair SARS-CoV-2 infection and replication. Sci Signal. 2021;14(690):eabe5040. doi:10.1126/scisignal.abe5040
  • Wang XH, Schröder HC, Müller WEG. Amorphous polyphosphate, a smart bioinspired nano-/bio-material for bone and cartilage regeneration: towards a new paradigm in tissue engineering. J Mat Chem B. 2018;6(16):2385–2412. doi:10.1039/C8TB00241J
  • Müller WEG, Wang SF, Tolba E, et al. Transformation of amorphous polyphosphate nanoparticles into coacervate complexes: an approach for the encapsulation of mesenchymal stem cells. Small. 2018;14(27):1801170. doi:10.1002/smll.201801170
  • Müller WEG, Neufurth M, Lieberwirth I, Wang SF, Schröder HC, Wang XH. Functional importance of coacervation to convert calcium polyphosphate nanoparticles into the physiologically active state. Mater Today Bio. 2022;16:100404. doi:10.1016/j.mtbio.2022.100404
  • Fernandes-Cunha GM, McKinlay CJ, Vargas JR, Jessen HJ, Waymouth RM, Wender PA. Delivery of inorganic polyphosphate into cells using amphipathic oligocarbonate transporters. ACS Cent Sci. 2018;4(10):1394–1402. doi:10.1021/acscentsci.8b00470
  • Barbeck M, Alkildani S, Jung O. Editorial of the Special Issue: “Soft and Hard Tissue Regeneration”. Biomedicines. 2022;10(2):356. doi:10.3390/biomedicines10020356
  • Lehn JM. Supramolecular chemistry: receptors, catalysts, and carriers. Science. 1985;227(4689):849–856. doi:10.1126/science.227.4689.849
  • Fasting C, Schalley CA, Weber M, et al. Multivalency as a chemical organization and action principle. Angew Chem Int Ed Engl. 2012;51(42):10472–10498. doi:10.1002/anie.201201114
  • Müller WEG, Neufurth M, Wang S, Tolba E, Schröder HC, Wang XH. Morphogenetically active scaffold for osteochondral repair (polyphosphate/alginate/N,O-carboxymethyl chitosan). Eur Cell Mater. 2016;31:174–190. doi:10.22203/eCM.v031a12
  • Müller WEG, Neufurth M, Ackermann M, et al. Fabrication of a new physiological macroporous hybrid biomaterial/bioscaffold material based on polyphosphate and collagen by freeze-extraction. J Mat Chem B. 2017;5(21):3823–3835. doi:10.1039/C7TB00306D
  • Tolba E, Wang XH, Ackermann M, et al. In-situ polyphosphate nanoparticle formation in hybrid poly(vinyl alcohol)/karaya gum-hydrogels: a porous scaffold inducing infiltration of mesenchymal stem cells. Adv Sci. 2018;2018:1801452.
  • Neufurth M, Wang SF, Schröder HC, Al-Nawas B, Wang XH, Müller WEG. 3D bioprinting of tissue units with mesenchymal stem cells, retaining their proliferative and differentiating potential, in polyphosphate-containing bio-ink. Biofabrication. 2022;14(1):015016. doi:10.1088/1758-5090/ac3f29
  • Krieg E, Bastings MM, Besenius P, Rybtchinski B. Supramolecular polymers in aqueous media. Chem Rev. 2016;116(4):2414–2477. doi:10.1021/acs.chemrev.5b00369
  • Samperi M, Pérez-García L, Amabilino DB. Quantification of energy of activation to supramolecular nanofibre formation reveals enthalpic and entropic effects and morphological consequence. Chem Sci. 2019;10(44):10256–10266. doi:10.1039/C9SC03280K
  • Harris JR, Lewis RJ. The collagen type I segment long spacing (SLS) and fibrillar forms: formation by ATP and sulphonated diazo dyes. Micron. 2016;86:36–47. doi:10.1016/j.micron.2016.04.008
  • Trautmann A. Extracellular ATP in the immune system: more than just a “danger signal”. Sci Signal. 2009;2(56):pe6. doi:10.1126/scisignal.256pe6
  • Huang H, Zhang X, Li S, et al. Physiological levels of ATP negatively regulate proteasome function. Cell Res. 2010;20(12):1372–1385. doi:10.1038/cr.2010.123
  • Schenk U, Westendorf AM, Radaelli E, et al. Purinergic control of T cell activation by ATP released through pannexin-1 hemichannels. Sci Signal. 2008;1(39):ra6. doi:10.1126/scisignal.1160583
  • Etulain J. Platelets in wound healing and regenerative medicine. Platelets. 2018;29(6):556–568. doi:10.1080/09537104.2018.1430357
  • Swieringa F, Spronk HMH, Heemskerk JWM, van der Meijden PEJ. Integrating platelet and coagulation activation in fibrin clot formation. Res Pract Thromb Haemost. 2018;2(3):450–460. doi:10.1002/rth2.12107
  • Zuk PA, Zhu M, Mizuno H, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 2001;7(2):211–228. doi:10.1089/107632701300062859
  • Yang J, Zhang YS, Yue K, Khademhosseini A. Cell-laden hydrogels for osteochondral and cartilage tissue engineering. Acta Biomater. 2017;57:1–25. doi:10.1016/j.actbio.2017.01.036
  • Laverdet B, Micallef L, Lebreton C, et al. Use of mesenchymal stem cells for cutaneous repair and skin substitute elaboration. Pathol Biol. 2014;62(2):108–117. doi:10.1016/j.patbio.2014.01.002
  • Leyhausen G, Lorenz B, Zhu H, et al. Inorganic polyphosphate in human osteoblast-like cells. J Bone Mineral Res. 1998;13(5):803–812. doi:10.1359/jbmr.1998.13.5.803
  • Schröder HC, Kurz L, Müller WEG, Lorenz B. Polyphosphate in bone. Biochemistry. 2000;65(3):296–303.
  • Morimoto D, Tomita T, Kuroda S, et al. Inorganic polyphosphate differentiates human mesenchymal stem cells into osteoblastic cells. J Bone Miner Metab. 2010;28(4):418–423. doi:10.1007/s00774-010-0157-4
  • Müller WEG, Tolba E, Schröder HC, Muñoz-Espí R, Diehl-Seifert B, Wang XH. Amorphous polyphosphate-hydroxyapatite: a morphogenetically active substrate for bone-related SaOS-2 cells in vitro. Acta Biomater. 2016;31:358–367. doi:10.1016/j.actbio.2015.11.060
  • Bolander J, Ji W, Geris L, et al. The combined mechanism of bone morphogenetic protein- and calcium phosphate-induced skeletal tissue formation by human periosteum derived cells. Eur Cell Mater. 2016;31:11–25. doi:10.22203/eCM.v031a02
  • Morrissey JH, Choi SH, Smith SA. Polyphosphate: an ancient molecule that links platelets, coagulation, and inflammation. Blood. 2012;119(25):5972–5979. doi:10.1182/blood-2012-03-306605
  • Hill T, Morales M. On “High energy phosphate bonds” of biochemical interest 1. J Am Chem Soc. 1951;73(4):1656–1660. doi:10.1021/ja01148a072
  • Lipman F. Metabolic generation and utilization of phosphate bond energy. In: Nord FF, Werkman CH, editors. Advances in Enzymology and Related Subjects of Biochemistry. Vol. 1. New York: Interscience Publishers Inc; 1941:99–162.
  • Hessle L, Johnson KA, Anderson HC, et al. Tissue-nonspecific alkaline phosphatase and plasma cell membrane glycoprotein-1 are central antagonistic regulators of bone mineralization. Proc Natl Acad Sci USA. 2002;99(14):9445–9449. doi:10.1073/pnas.142063399
  • Klepinin A, Zhang S, Klepinina L, et al. Adenylate kinase and metabolic signaling in cancer cells. Front Oncol. 2020;10:660. doi:10.3389/fonc.2020.00660
  • Ishikawa HO, Xu A, Ogura E, Manning G, Irvine KD, Giniger E. The Raine syndrome protein FAM20C is a Golgi kinase that phosphorylates bio-mineralization proteins. PLoS One. 2012;7(8):e42988. doi:10.1371/journal.pone.0042988
  • Tagliabracci VS, Xiao J, Dixon JE. Phosphorylation of substrates destined for secretion by the Fam20 kinases. Biochem Soc Trans. 2013;41(4):1061–1065. doi:10.1042/BST20130059
  • Tagliabracci VS, Wiley SE, Guo X, et al. A single kinase generates the majority of the secreted phosphoproteome. Cell. 2015;161(7):1619–1632. doi:10.1016/j.cell.2015.05.028
  • Raine J, Winter RM, Davey A, Tucker SM. Unknown syndrome: microcephaly, hypoplastic nose, exophthalmos, gum hyperplasia, cleft palate, low set ears, and osteosclerosis. J Med Genet. 1989;26(12):786–788. doi:10.1136/jmg.26.12.786
  • Lowenstam HA. Minerals formed by organisms. Science. 1981;211(4487):1126–1131. doi:10.1126/science.7008198
  • Ruben JA, Bennett AA. The evolution of bone. Evolution. 1987;41(6):1187–1197. doi:10.2307/2409087
  • Mann S, Parker SB, Ross MD, Skarnulis AJ, Williams RJ. The ultrastructure of the calcium carbonate balance organs of the inner ear: an ultra-high resolution electron microscopy study. Proc R Soc Lond B Biol Sci. 1983;218:415–424.
  • Setiawati R, Rahardjo P. Bone development and growth. In: Yang HS, editor. Osteogenesis and Bone Regeneration. Intechopen; 2019. doi:10.5772/intechopen.82452
  • Müller WEG, Neufurth M, Huang J, et al. Nonenzymatic transformation of amorphous CaCO3 into calcium phosphate mineral after exposure to sodium phosphate in vitro: implications for in vivo hydroxyapatite bone formation. ChemBioChem. 2015;16(9):1323–1332. doi:10.1002/cbic.201500057
  • Tadier S, Rokidi S, Rey C, Combes C, Koutsoukos PG. Crystal growth of aragonite in the presence of phosphate. J Crystal Growth. 2017;458:44–52. doi:10.1016/j.jcrysgro.2016.10.046
  • Boskey AL, Guidon P, Doty SB, Stiner D, Leboy P, Binderman I. The mechanism of β-glycerophosphate action in mineralizing chick limb-bud mesenchymal cell cultures. J Bone Miner Res. 1996;11(11):1694–1702. doi:10.1002/jbmr.5650111113
  • Sharif PS, Abdollahi M. The role of platelets in bone remodeling. Inflamm Allergy Drug Targets. 2010;9(5):393–399. doi:10.2174/187152810793938044
  • Müller WEG, Wang XH, Diehl-Seifert B, et al. Inorganic polymeric phosphate/polyphosphate as an inducer of alkaline phosphatase and a modulator of intracellular Ca2+ level in osteoblasts (SaOS-2 cells) in vitro. Acta Biomater. 2011;7(6):2661–2671. doi:10.1016/j.actbio.2011.03.007
  • Khersonsky O, Tawfik DS. Enzyme promiscuity: a mechanistic and evolutionary perspective. Annu Rev Biochem. 2010;79(1):471–505. doi:10.1146/annurev-biochem-030409-143718
  • Lotsari A, Rajasekharan AK, Halvarsson M, Andersson M. Transformation of amorphous calcium phosphate to bone-like apatite. Nat Commun. 2018;9(1):4170. doi:10.1038/s41467-018-06570-x
  • Wang XH, Wang SF, He F, et al. Polyphosphate as a bioactive and biodegradable implant material: induction of bone regeneration in rats. Adv Engin Mat. 2016;18(8):1406–1417. doi:10.1002/adem.201600057
  • Meldrum FC, Cölfen H. Controlling mineral morphologies and structures in biological and synthetic systems. Chem Rev. 2008;108(11):4332–4432. doi:10.1021/cr8002856
  • Mayr-Wohlfart U, Waltenberger J, Hausser H, et al. Vascular endothelial growth factor stimulates chemotactic migration of primary human osteoblasts. Bone. 2002;30(3):472–477. doi:10.1016/S8756-3282(01)00690-1
  • Martineau I, Lacoste E, Gagnon G. Effects of calcium and thrombin on growth factor release from platelet concentrates: kinetics and regulation of endothelial cell proliferation. Biomaterials. 2004;25(18):4489–4502. doi:10.1016/j.biomaterials.2003.11.013
  • Marenzana M, Arnett TR. The key role of the blood supply to bone. Bone Res. 2013;1(3):203–215. doi:10.4248/BR201303001
  • Bilgen F, Ural A, Bekerecioglu M. Platelet-rich fibrin: an effective chronic wound healing accelerator. J Tissue Viability. 2021;30(4):616–620. doi:10.1016/j.jtv.2021.04.009
  • Schultz GS, Chin GA, Moldawer L, Diegelmann RF. Principles of wound healing. In: Fitridge R, Thompson M, editors. Mechanisms of Vascular Disease: A Reference Book for Vascular Specialists, Chapter 23. Adelaide (AU): University of Adelaide Press; 2011. Available from: https://www.ncbi.nlm.nih.gov/books/NBK534261. Accessed January 31, 2024.
  • Rodriguez-Diaz A, Toyama Y, Abravanel DL, et al. Actomyosin purse strings: renewable resources that make morphogenesis robust and resilient. HFSP J. 2008;2(4):220–237. doi:10.2976/1.2955565
  • Jacinto A, Martinez-Arias A, Martin P. Mechanisms of epithelial fusion and repair. Nat Cell Biol. 2001;3(5):E117–E123. doi:10.1038/35074643
  • Santamaría R, González-álvarez M, Delgado R, Esteban S, Arroyo AG. Remodeling of the microvasculature: may the blood flow be with you. Front Physiol. 2020;11:586852. doi:10.3389/fphys.2020.586852
  • Schwiebert EM, Zsembery A. Extracellular ATP as a signaling molecule for epithelial cells. Biochim Biophys Acta. 2003;1615(1–2):7–32. doi:10.1016/S0005-2736(03)00210-4
  • De Bock K, Georgiadou M, Schoors S, et al. Role of PFKFB3-driven glycolysis in vessel sprouting. Cell. 2013;154(3):651–663. doi:10.1016/j.cell.2013.06.037
  • Leung SWS, Shi Y. The glycolytic process in endothelial cells and its implications. Acta Pharmacol Sin. 2022;43(2):251–259. doi:10.1038/s41401-021-00647-y
  • Spampinato SF, Caruso GI, De Pasquale R, Sortino MA, Merlo S. The treatment of impaired wound healing in diabetes: looking among old drugs. Pharmaceuticals. 2020;13(4):60. doi:10.3390/ph13040060
  • Sreekumar R, Halvatsiotis P, Schimke JC, Nair KS. Gene expression profile in skeletal muscle of type 2 diabetes and the effect of insulin treatment. Diabetes. 2002;51(6):1913–1920. doi:10.2337/diabetes.51.6.1913
  • Patti ME, Butte AJ, Crunkhorn S, et al. Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: potential role of PGC1 and NRF1. Proc Natl Acad Sci USA. 2003;100(14):8466–8471. doi:10.1073/pnas.1032913100
  • Sarojini H, Bajorek A, Wan R, et al. Enhanced skin incisional wound healing with intracellular ATP delivery via macrophage proliferation and direct collagen production. Front Pharmacol. 2021;12:594586. doi:10.3389/fphar.2021.594586
  • Yang JY, Chen CC, Chang SC, et al. ENERGI-F703 gel, as a new topical treatment for diabetic foot and leg ulcers: a multicenter, randomized, double-blind, Phase II trial. EClinicalMedicine. 2022;51:101497. doi:10.1016/j.eclinm.2022.101497
  • Müller WEG, Relkovic D, Ackermann M, et al. Enhancement of wound healing in normal and diabetic mice by topical application of amorphous polyphosphate. Polymers. 2017;9(12):300. doi:10.3390/polym9070300
  • Stan D, Tanase C, Avram M, et al. Wound healing applications of creams and “smart” hydrogels. Exp Dermatol. 2021;30(9):1218–1232. doi:10.1111/exd.14396
  • Rosso F, Marino G, Giordano A, Barbarisi M, Parmeggiani D, Barbarisi A. Smart materials as scaffolds for tissue engineering. J Cell Physiol. 2005;203(3):465–470. doi:10.1002/jcp.20270
  • Budharaju H, Suresh S, Sekar MP, et al. Ceramic materials for 3D printing of biomimetic bone scaffolds – current state-of-The-art & future perspectives. Mater Des. 2023;231:112064. doi:10.1016/j.matdes.2023.112064
  • Ananth KP, Jayram ND. A comprehensive review of 3D printing techniques for biomaterial-based scaffold fabrication in bone tissue engineering. Ann 3D Print Med. 2024;13:100141. doi:10.1016/j.stlm.2023.100141
  • Budharaju H, Sundaramurthi D, Sethuraman S. Embedded 3D bioprinting – an emerging strategy to fabricate biomimetic & large vascularized tissue constructs. Bioact Mater. 2024;32:356–384. doi:10.1016/j.bioactmat.2023.10.012
  • Müller WEG, Schröder HC, Feng QL, Schlossmacher U, Link T, Wang XH. Development of a morphogenetically active scaffold for three-dimensional growth of bone cells: biosilica-alginate hydrogel for SaOS-2 cell cultivation. J Tissue Eng Regen Med. 2015;9(11):E39–E50. doi:10.1002/term.1745
  • Neufurth M, Wang XH, Wang SF, et al. 3D printing of hybrid biomaterials for bone tissue engineering: calcium-polyphosphate microparticles encapsulated by polycaprolactone. Acta Biomater. 2017;64:377–388. doi:10.1016/j.actbio.2017.09.031
  • Neufurth M, Wang XH, Schröder HC, et al. Engineering a morphogenetically active hydrogel for bioprinting of bioartificial tissue derived from human osteoblast-like SaOS-2 cells. Biomaterials. 2014;35(31):8810–8819. doi:10.1016/j.biomaterials.2014.07.002
  • Müller WEG, Tolba E, Schröder HC, Diehl-Seifert B, Link T, Wang XH. Biosilica-loaded poly(ϵ-caprolactone) nanofibers mats provide a morphogenetically active surface scaffold for the growth and mineralization of the osteoclast-related SaOS-2 cells. Biotechnol J. 2014;9(10):1312–1321. doi:10.1002/biot.201400277
  • Müller WEG, Tolba E, Dorweiler B, Schröder HC, Diehl-Seifert B, Wang XH. Electrospun bioactive mats enriched with Ca-polyphosphate/retinol nanospheres as potential wound dressing. Biochem Biophys Rep. 2015;3:150–160. doi:10.1016/j.bbrep.2015.08.007
  • Wang XH, Ackermann M, Wang SF, et al. 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
  • Schloßmacher U, Schröder HC, Wang XH, et al. Alginate/silica composite hydrogel as a potential morphogenetically active scaffold for three-dimensional tissue engineering. RSC Adv. 2013;3(28):11185–11194. doi:10.1039/c3ra23341c
  • Braun S, Rappoport S, Zusman R, Avnir D, Ottolenghi M. Biochemically active sol-gel glasses: the trapping of enzymes. Mater Lett. 1990;10(1–2):1–5. doi:10.1016/0167-577X(90)90002-4
  • Nassif N, Roux C, Coradin T, Rager MN, Bouvet OMM, Livage J. A sol–gel matrix to preserve the viability of encapsulated bacteria. J Mat Chem. 2003;13(2):203–208. doi:10.1039/b210167j
  • Müller WEG, Engel S, Wang XH, et al. Bioencapsulation of living bacteria (Escherichia coli) with poly(silicate) after transformation with silicatein-α gene. Biomaterials. 2008;29(7):771–779. doi:10.1016/j.biomaterials.2007.10.038
  • Müller WEG, Wang XH, Proksch P, et al. Principles of biofouling protection in marine sponges: a model for the design of novel biomimetic and bio-inspired coatings in the marine environment?. Mar Biotechnol. 2013;15(4):375–398. doi:10.1007/s10126-013-9497-0
  • Müller WEG, Tolba E, Schröder HC, et al. A new printable and durable N,O-carboxymethyl chitosan-Ca2+ -polyphosphate complex with morphogenetic activity. J Mat Chem B. 2015;3(8):1722–1730. doi:10.1039/C4TB01586J
  • Wang SF, Neufurth M, Schepler H, et al. Acceleration of wound healing through amorphous calcium carbonate, stabilized with high-energy polyphosphate. Pharmaceutics. 2023;15(2):494. doi:10.3390/pharmaceutics15020494
  • Ackermann M, Tolba E, Neufurth M, et al. Biomimetic transformation of polyphosphate microparticles during restoration of damaged teeth. Dent Mater. 2019;35(2):244–256. doi:10.1016/j.dental.2018.11.014
  • Müller WEG, Neufurth M, Tolba E, et al. A biomimetic approach to ameliorate dental hypersensitivity by amorphous polyphosphate microparticles. Dent Mater. 2016;32(6):775–783. doi:10.1016/j.dental.2016.03.027
  • Müller WEG, Tolba E, Wang SF, et al. Nanoparticle-directed and ionically forced polyphosphate coacervation: a versatile and reversible core-shell system for drug delivery. Sci Rep. 2020;10(1):17147. doi:10.1038/s41598-020-73100-5
  • Neufurth M, Wang XH, Tolba E, et al. Modular small diameter vascular grafts with bioactive functionalities. PLoS One. 2015;10(7):e0133632. doi:10.1371/journal.pone.0133632
  • Ackermann M, Wang XH, Wang SF, et al. Collagen-inducing biologization of prosthetic material for hernia repair: polypropylene meshes coated with polyP/collagen. J Biomed Mater Res B. 2018;106(6):2109–2121. doi:10.1002/jbm.b.34016
  • Smith SA, Morrissey JH. Polyphosphate as a general procoagulant agent. J Thromb Haemost. 2008;6(10):1750–1756. doi:10.1111/j.1538-7836.2008.03104.x
  • Smith SA, Mutch NJ, Baskar D, Rohloff P, Docampo R, Morrissey JH. Polyphosphate modulates blood coagulation and fibrinolysis. Proc Natl Acad Sci USA. 2006;103(4):903–908. doi:10.1073/pnas.0507195103
  • Moon JH, Park JH, Lee JY. Antibacterial Action of Polyphosphate on Porphyromonas gingivalis. Antimicrob Agents Chemother. 2011;55(2):806–812. doi:10.1128/AAC.01014-10
  • Wiens M, Elkhooly TA, Schröder HC, Mohamed TH, Müller WEG. Characterization and osteogenic activity of a silicatein/biosilica-coated chitosan-graft-polycaprolactone. Acta Biomater. 2014;10(10):4456–4464. doi:10.1016/j.actbio.2014.06.036
  • Phang JM, Liu W, Zabirnyk O. Proline metabolism and microenvironmental stress. Annu Rev Nutr. 2010;30(1):441–463. doi:10.1146/annurev.nutr.012809.104638
  • Zhou Z, Fan Y, Jiang Y, et al. Mineralized enzyme-based biomaterials with superior bioactivities for bone regeneration. ACS Appl Mater Interfaces. 2022;14(32):36315–36330. doi:10.1021/acsami.2c05794
  • Yang J, Ueharu H, Mishina Y. Energy metabolism: a newly emerging target of BMP signaling in bone homeostasis. Bone. 2020;138:115467. doi:10.1016/j.bone.2020.115467
  • Imsiecke G, Münkner J, Lorenz B, Bachinski N, Müller WEG, Schröder HC. Inorganic polyphosphates in the developing freshwater sponge Ephydatia muelleri: effect of stress by polluted waters. Environ Toxicol Chem. 1996;15(8):1329–1334. doi:10.1002/etc.5620150811
  • Müller WEG, Wang XH, Sinha B, Wiens M, Schröder HC, Jochum KP. NanoSIMS: insights into the organization of the proteinaceous scaffold within hexactinellid sponge spicules. ChemBioChem. 2010;11(8):1077–1082. doi:10.1002/cbic.201000078
  • Hench LL, Splinter RJ, Allen WC, Greenlee TK. Bonding mechanisms at the interface of ceramic prosthetic materials. J Biomed Mater Res Symp. 1971;5:117–141.
  • Zhu H, Zheng K, Boccaccini AR. Multi-functional silica-based mesoporous materials for simultaneous delivery of biologically active ions and therapeutic biomolecules. Acta Biomater. 2021;129:1–17. doi:10.1016/j.actbio.2021.05.007
  • Hench LL. The story of Bioglass. J Mater Sci Mater Med. 2006;17(11):967–978. doi:10.1007/s10856-006-0432-z
  • Rahaman MN, Day DE, Bal BS, et al. Bioactive glass in tissue engineering. Acta Biomater. 2011;7(6):2355–2373. doi:10.1016/j.actbio.2011.03.016
  • Moffa M, Camposeo A, Fasano V, et al. Biomineral amorphous lasers through light-scattering surfaces assembled by electrospun fiber templates. Laser Photonics Rev. 2018;12(1):1700224. doi:10.1002/lpor.201700224
  • Szwed-Georgiou A, Płociński P, Kupikowska-Stobba B, et al. Bioactive materials for bone regeneration: biomolecules and delivery systems. ACS Biomater Sci Eng. 2023;9(9):5222–5254. doi:10.1021/acsbiomaterials.3c00609
  • Schneider LA, Korber A, Grabbe S, Dissemond J. Influence of pH on wound-healing: a new perspective for wound-therapy?. Arch Dermatol Res. 2007;298(9):413–420. doi:10.1007/s00403-006-0713-x
  • Raghunand N, Gatenby RA, Gillies RJ. Microenvironmental and cellular consequences of altered blood flow in tumours. Br J Radiol. 2003;76(Spec No 1):S11–S22. doi:10.1259/bjr/12913493
  • Yan GX, Kléber AG. Changes in extracellular and intracellular pH in ischemic rabbit papillary muscle. Circ Res. 1992;71(2):460–470. doi:10.1161/01.RES.71.2.460
  • Gan Q, Zhu J, Yuan Y, Liu H, Zhu Y, Liu C. A proton-responsive ensemble using mesocellular foam supports capped with N,O-carboxymethyl chitosan for controlled release of bioactive proteins. J Mater Chem B. 2015;3(11):2281–2285. doi:10.1039/C5TB00219B
  • Tao B, Deng Y, Song L, et al. BMP2-loaded titania nanotubes coating with pH-responsive multilayers for bacterial infections inhibition and osteogenic activity improvement. Colloids Surf B Biointerfaces. 2019;177:242–252. doi:10.1016/j.colsurfb.2019.02.014
  • Banerjee I, Mishra D, Das T, Maiti TK. Wound pH-responsive sustained release of therapeutics from a poly(NIPAAm-co-AAc) hydrogel. J Biomater Sci Polym Ed. 2012;23(1–4):111–132. doi:10.1163/092050610X545049
  • Schäcke H, Müller IM, Müller WEG. Tyrosine kinase from the marine sponge Geodia cydonium: the oldest member belonging to the receptor tyrosine kinase class II family. In: Müller WEG, editor. Use of Aquatic Invertebrates as Tools for Monitoring of Environmental Hazards. Stuttgart, New York: Gustav Fischer Verlag; 1994:201–211.
  • Schopf JW. Microfossils of the early Archean apex chert: new evidence of the antiquity of life. Science. 1993;260(5108):640–646. doi:10.1126/science.260.5108.640
  • Müller WEG, Brümmer F, Batel R, Müller IM, Schröder HC. Molecular biodiversity. Case study: porifera (sponges). Naturwissenschaften. 2003;90(3):103–120. doi:10.1007/s00114-003-0407-6