Significance of Premature Vertebral Mineralization in Zebrafish Models in Mechanistic and Pharmaceutical Research on Hereditary Multisystem Diseases
Abstract
:1. Introduction
2. Materials and Methods
3. A Brief Overview of the Normal Development of the Axial Skeleton in Zebrafish
4. Pseudoxanthoma Elasticum
5. Generalized Arterial Calcification of Infancy
6. Schorderet–Munier–Franceschetti Syndrome
7. Hyperphosphatemic Familial Tumoral Calcinosis
8. LTBP1-Related Cutis Laxa Syndrome
9. Discussion
Disease | Human Gene | Zebrafish Orthologue | Knockout Vertebral Phenotype | References |
---|---|---|---|---|
Bruck Syndrome type II | PLOD2 | plod2 | Shortened body axis, kyphoscoliosis, compressed vertebrae, excess bone at vertebral end plates that results in loss of hourglass shape of vertebra, increased TMD and thickness | [8] |
FOP | ACVR1 | acvr1l | Dorsalization of the embryonic axis | [95,96,97] |
Craniosynostosis | CYP26B1 | cyp26b1 | Outgrowth of cartilaginous endochondral disc in pectoral fins, coronal craniosynostosis | [171,172] |
Osteoporosis | ATP6V1H | atp6v1h | Premature death, reduction in/absence of bone cells, almost complete absence of mineralized bone | [94] |
Osteogenesis imperfecta | COL1A1 COL1A2 BMP1 SP7 | col1a1a, col1a1b col1a2 bmp1a, bmp1b sp7 | Variable phenotype including callus formation, bending of ribs, short stature, craniofacial abnormalities, malformation of vertebral column | [8,99,100,101,102,103,104,105] |
Ehlers-Danlos syndrome | B4GALT7 | b4galt7 | Scoliosis; small, bent pectoral fins; reduced or absent mineralized bone | [10,173] |
Spinal curvature disorders | COL8A1 KIF6 PTK7 TBX6 | col8a1a, col8a1b kif6 ptk7a tbx6 | Extensive scoliosis in thoracic and caudal parts of the spine, deformed and fused vertebrae, fused neural and hemal arches | [10,174,175,176,177] |
Gaucher disease | GBA1 | gba1 | Reduced osteoblast differentiation and bone mineralization, slight curvature of the trunk | [178] |
10. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Tonelli, F.; Bek, J.W.; Besio, R.; De Clercq, A.; Leoni, L.; Salmon, P.; Coucke, P.J.; Willaert, A.; Forlino, A. Zebrafish: A Resourceful Vertebrate Model to Investigate Skeletal Disorders. Front. Endocrinol. 2020, 11, 489. [Google Scholar] [CrossRef] [PubMed]
- Spoorendonk, K.M.; Hammond, C.L.; Huitema, L.F.A.; Vanoevelen, J.; Schulte-Merker, S. Zebrafish as a unique model system in bone research: The power of genetics and in vivo imaging. J. Appl. Ichthyol. 2010, 26, 219–224. [Google Scholar] [CrossRef]
- Kwon, R.Y.; Watson, C.J.; Karasik, D. Using zebrafish to study skeletal genomics. Bone 2019, 126, 37–50. [Google Scholar] [CrossRef] [PubMed]
- Bird, N.C.; Mabee, P.M. Developmental morphology of the axial skeleton of the zebrafish, Danio rerio (Ostariophysi: Cyprinidae). Dev. Dyn. 2003, 228, 337–357. [Google Scholar] [CrossRef]
- Kimmel, C.B. Genetics and early development of zebrafish. Trends Genet. 1989, 5, 283–288. [Google Scholar] [CrossRef]
- Howe, K.; Clark, M.D.; Torroja, C.F.; Torrance, J.; Berthelot, C.; Muffato, M.; Collins, J.E.; Humphray, S.; McLaren, K.; Matthews, L.; et al. The zebrafish reference genome sequence and its relationship to the human genome. Nature 2013, 496, 498–503. [Google Scholar] [CrossRef]
- Du, S.J.; Frenkel, V.; Kindschi, G.; Zohar, Y. Visualizing normal and defective bone development in zebrafish embryos using the fluorescent chromophore calcein. Dev. Biol. 2001, 238, 239–246. [Google Scholar] [CrossRef]
- Gistelinck, C.; Witten, P.E.; Huysseune, A.; Symoens, S.; Malfait, F.; Larionova, D.; Simoens, P.; Dierick, M.; Van Hoorebeke, L.; De Paepe, A.; et al. Loss of Type I Collagen Telopeptide Lysyl Hydroxylation Causes Musculoskeletal Abnormalities in a Zebrafish Model of Bruck Syndrome. J. Bone Miner. Res. 2016, 31, 1930–1942. [Google Scholar] [CrossRef]
- Carnovali, M.; Banfi, G.; Mariotti, M. Zebrafish Models of Human Skeletal Disorders: Embryo and Adult Swimming Together. BioMed Res. Int. 2019, 2019, 1253710. [Google Scholar] [CrossRef]
- Gray, R.S.; Gonzalez, R.; Ackerman, S.D.; Minowa, R.; Griest, J.F.; Bayrak, M.N.; Troutwine, B.; Canter, S.; Monk, K.R.; Sepich, D.S.; et al. Postembryonic screen for mutations affecting spine development in zebrafish. Dev. Biol. 2021, 471, 18–33. [Google Scholar] [CrossRef]
- Driever, W.; Solnica-Krezel, L.; Schier, A.F.; Neuhauss, S.C.; Malicki, J.; Stemple, D.L.; Stainier, D.Y.; Zwartkruis, F.; Abdelilah, S.; Rangini, Z.; et al. A genetic screen for mutations affecting embryogenesis in zebrafish. Development 1996, 123, 37–46. [Google Scholar] [CrossRef] [PubMed]
- Solnica-Krezel, L.; Stemple, D.L.; Mountcastle-Shah, E.; Rangini, Z.; Neuhauss, S.C.; Malicki, J.; Schier, A.F.; Stainier, D.Y.; Zwartkruis, F.; Abdelilah, S.; et al. Mutations affecting cell fates and cellular rearrangements during gastrulation in zebrafish. Development 1996, 123, 67–80. [Google Scholar] [CrossRef] [PubMed]
- Amsterdam, A.; Burgess, S.; Golling, G.; Chen, W.; Sun, Z.; Townsend, K.; Farrington, S.; Haldi, M.; Hopkins, N. A large-scale insertional mutagenesis screen in zebrafish. Genes. Dev. 1999, 13, 2713–2724. [Google Scholar] [CrossRef] [PubMed]
- Mullins, M.C.; Hammerschmidt, M.; Haffter, P.; Nüsslein-Volhard, C. Large-scale mutagenesis in the zebrafish: In search of genes controlling development in a vertebrate. Curr. Biol. 1994, 4, 189–202. [Google Scholar] [CrossRef]
- Henke, K.; Farmer, D.T.; Niu, X.; Kraus, J.M.; Galloway, J.L.; Youngstrom, D.W. Genetically engineered zebrafish as models of skeletal development and regeneration. Bone 2023, 167, 116611. [Google Scholar] [CrossRef] [PubMed]
- Kettleborough, R.N.; Busch-Nentwich, E.M.; Harvey, S.A.; Dooley, C.M.; de Bruijn, E.; van Eeden, F.; Sealy, I.; White, R.J.; Herd, C.; Nijman, I.J.; et al. A systematic genome-wide analysis of zebrafish protein-coding gene function. Nature 2013, 496, 494–497. [Google Scholar] [CrossRef]
- Pasquier, J.; Braasch, I.; Batzel, P.; Cabau, C.; Montfort, J.; Nguyen, T.; Jouanno, E.; Berthelot, C.; Klopp, C.; Journot, L.; et al. Evolution of gene expression after whole-genome duplication: New insights from the spotted gar genome. J. Exp. Zool. B Mol. Dev. Evol. 2017, 328, 709–721. [Google Scholar] [CrossRef]
- Ogawa, Y.; Corbo, J.C. Partitioning of gene expression among zebrafish photoreceptor subtypes. Sci. Rep. 2021, 11, 17340. [Google Scholar] [CrossRef]
- Yan, Y.L.; Titus, T.; Desvignes, T.; BreMiller, R.; Batzel, P.; Sydes, J.; Farnsworth, D.; Dillon, D.; Wegner, J.; Phillips, J.B.; et al. A fish with no sex: Gonadal and adrenal functions partition between zebrafish NR5A1 co-orthologs. Genetics 2021, 217, iyaa030. [Google Scholar] [CrossRef]
- Dietrich, K.; Fiedler, I.A.; Kurzyukova, A.; López-Delgado, A.C.; McGowan, L.M.; Geurtzen, K.; Hammond, C.L.; Busse, B.; Knopf, F. Skeletal Biology and Disease Modeling in Zebrafish. J. Bone Miner. Res. 2021, 36, 436–458. [Google Scholar] [CrossRef]
- Cotti, S.; Huysseune, A.; Larionova, D.; Koppe, W.; Forlino, A.; Witten, P.E. Compression Fractures and Partial Phenotype Rescue with a Low Phosphorus Diet in the Chihuahua Zebrafish Osteogenesis Imperfecta Model. Front. Endocrinol. 2022, 13, 851879. [Google Scholar] [CrossRef] [PubMed]
- Prince, V.E.; Joly, L.; Ekker, M.; Ho, R.K. Zebrafish hox genes: Genomic organization and modified colinear expression patterns in the trunk. Development 1998, 125, 407–420. [Google Scholar] [CrossRef] [PubMed]
- Lleras Forero, L.; Narayanan, R.; Huitema, L.F.; VanBergen, M.; Apschner, A.; Peterson-Maduro, J.; Logister, I.; Valentin, G.; Morelli, L.G.; Oates, A.C.; et al. Segmentation of the zebrafish axial skeleton relies on notochord sheath cells and not on the segmentation clock. eLife 2018, 7, e33843. [Google Scholar] [CrossRef]
- Sheth, R.; Bastida, M.F.; Kmita, M.; Ros, M. “Self-regulation,” a new facet of Hox genes’ function. Dev. Dyn. 2014, 243, 182–191. [Google Scholar] [CrossRef] [PubMed]
- Sordino, P.; van der Hoeven, F.; Duboule, D. Hox gene expression in teleost fins and the origin of vertebrate digits. Nature 1995, 375, 678–681. [Google Scholar] [CrossRef] [PubMed]
- Ahn, D.; Ho, R.K. Tri-phasic expression of posterior Hox genes during development of pectoral fins in zebrafish: Implications for the evolution of vertebrate paired appendages. Dev. Biol. 2008, 322, 220–233. [Google Scholar] [CrossRef]
- Mork, L.; Crump, G. Zebrafish Craniofacial Development: A Window into Early Patterning. Curr. Top. Dev. Biol. 2015, 115, 235–269. [Google Scholar] [CrossRef]
- Le Pabic, P.; Dranow, D.B.; Hoyle, D.J.; Schilling, T.F. Zebrafish endochondral growth zones as they relate to human bone size, shape and disease. Front. Endocrinol. 2022, 13, 1060187. [Google Scholar] [CrossRef]
- Witten, P.E.; Huysseune, A. A comparative view on mechanisms and functions of skeletal remodelling in teleost fish, with special emphasis on osteoclasts and their function. Biol. Rev. Camb. Philos. Soc. 2009, 84, 315–346. [Google Scholar] [CrossRef]
- Weigele, J.; Franz-Odendaal, T.A. Functional bone histology of zebrafish reveals two types of endochondral ossification, different types of osteoblast clusters and a new bone type. J. Anat. 2016, 229, 92–103. [Google Scholar] [CrossRef]
- Witten, P.E.; Harris, M.P.; Huysseune, A.; Winkler, C. Small teleost fish provide new insights into human skeletal diseases. Methods Cell Biol. 2017, 138, 321–346. [Google Scholar] [CrossRef] [PubMed]
- Cubbage, C.C.; Mabee, P.M. Development of the cranium and paired fins in the zebrafish Danio rerio (Ostariophysi, Cyprinidae). J. Morphol. 1996, 229, 121–160. [Google Scholar] [CrossRef]
- Kimmel, C.B.; Ballard, W.W.; Kimmel, S.R.; Ullmann, B.; Schilling, T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 1995, 203, 253–310. [Google Scholar] [CrossRef] [PubMed]
- Kimmel, C.B.; DeLaurier, A.; Ullmann, B.; Dowd, J.; McFadden, M. Modes of developmental outgrowth and shaping of a craniofacial bone in zebrafish. PLoS ONE 2010, 5, e9475. [Google Scholar] [CrossRef]
- Nguyen, S.V.; Lanni, D.; Xu, Y.; Michaelson, J.S.; McMenamin, S.K. Dynamics of the Zebrafish Skeleton in Three Dimensions During Juvenile and Adult Development. Front. Physiol. 2022, 13, 875866. [Google Scholar] [CrossRef] [PubMed]
- Giffin, J.L.; Gaitor, D.; Franz-Odendaal, T.A. The Forgotten Skeletogenic Condensations: A Comparison of Early Skeletal Development Amongst Vertebrates. J. Dev. Biol. 2019, 7, 4. [Google Scholar] [CrossRef]
- El Fersioui, Y.; Pinton, G.; Allaman-Pillet, N.; Schorderet, D.F. Premature Vertebral Mineralization in hmx1-Mutant Zebrafish. Cells 2022, 11, 1088. [Google Scholar] [CrossRef]
- Witten, P.; Hall, B. The Ancient Segmented Active and Permanent Notochord. In Ancient Fishes and their Living Relatives: A Tribute to John G. Maisey; Verlag Dr. Friedrich Pfeil: Munich, Germany, 2021. [Google Scholar]
- Pogoda, H.M.; Riedl-Quinkertz, I.; Löhr, H.; Waxman, J.S.; Dale, R.M.; Topczewski, J.; Schulte-Merker, S.; Hammerschmidt, M. Direct activation of chordoblasts by retinoic acid is required for segmented centra mineralization during zebrafish spine development. Development 2018, 145, dev159418. [Google Scholar] [CrossRef]
- Wopat, S.; Bagwell, J.; Sumigray, K.D.; Dickson, A.L.; Huitema, L.F.A.; Poss, K.D.; Schulte-Merker, S.; Bagnat, M. Spine Patterning Is Guided by Segmentation of the Notochord Sheath. Cell Rep. 2018, 22, 2026–2038. [Google Scholar] [CrossRef]
- Pogoda, H.M.; Riedl-Quinkertz, I.; Hammerschmidt, M. Direct BMP signaling to chordoblasts is required for the initiation of segmented notochord sheath mineralization in zebrafish vertebral column development. Front. Endocrinol. 2023, 14, 1107339. [Google Scholar] [CrossRef]
- Huxley, F.R.S. On the Structure and Development of the Vertebrate Skeleton. Chic. Med. J. 1863, 20, 539–546. [Google Scholar] [CrossRef] [PubMed]
- Flores, M.V.; Tsang, V.W.; Hu, W.; Kalev-Zylinska, M.; Postlethwait, J.; Crosier, P.; Crosier, K.; Fisher, S. Duplicate zebrafish runx2 orthologues are expressed in developing skeletal elements. Gene Expr. Patterns 2004, 4, 573–581. [Google Scholar] [CrossRef]
- Sims, N.; Baron, R. Bone Cells and Their Function; Lippincott Williams & Wilkins: Philadelphia, PA, USA, 2000; pp. 1–16. [Google Scholar]
- Cotti, S.; Huysseune, A.; Koppe, W.; Rücklin, M.; Marone, F.; Wölfel, E.M.; Fiedler, I.A.K.; Busse, B.; Forlino, A.; Witten, P.E. More Bone with Less Minerals? The Effects of Dietary Phosphorus on the Post-Cranial Skeleton in Zebrafish. Int. J. Mol. Sci. 2020, 21, 5429. [Google Scholar] [CrossRef] [PubMed]
- Bonjour, J.P. Calcium and phosphate: A duet of ions playing for bone health. J. Am. Coll. Nutr. 2011, 30, 438s–448s. [Google Scholar] [CrossRef] [PubMed]
- Nitschke, Y.; Baujat, G.; Botschen, U.; Wittkampf, T.; du Moulin, M.; Stella, J.; Le Merrer, M.; Guest, G.; Lambot, K.; Tazarourte-Pinturier, M.F.; et al. Generalized arterial calcification of infancy and pseudoxanthoma elasticum can be caused by mutations in either ENPP1 or ABCC6. Am. J. Hum. Genet. 2012, 90, 25–39. [Google Scholar] [CrossRef]
- Ralph, D.; Levine, M.A.; Richard, G.; Morrow, M.M.; Flynn, E.K.; Uitto, J.; Li, Q. Mutation update: Variants of the ENPP1 gene in pathologic calcification, hypophosphatemic rickets, and cutaneous hypopigmentation with punctate keratoderma. Hum. Mutat. 2022, 43, 1183–1200. [Google Scholar] [CrossRef]
- Bergen, A.A.; Plomp, A.S.; Hu, X.; de Jong, P.T.; Gorgels, T.G. ABCC6 and pseudoxanthoma elasticum. Pflugers Arch. 2007, 453, 685–691. [Google Scholar] [CrossRef]
- Shimada, B.K.; Pomozi, V.; Zoll, J.; Kuo, S.; Martin, L.; Le Saux, O. ABCC6, Pyrophosphate and Ectopic Calcification: Therapeutic Solutions. Int. J. Mol. Sci. 2021, 22, 4555. [Google Scholar] [CrossRef]
- Li, Q.; van de Wetering, K.; Uitto, J. Pseudoxanthoma Elasticum as a Paradigm of Heritable Ectopic Mineralization Disorders: Pathomechanisms and Treatment Development. Am. J. Pathol. 2019, 189, 216–225. [Google Scholar] [CrossRef]
- Terry, S.F.; Uitto, J. Pseudoxanthoma Elasticum. In GeneReviews®; Adam, M.P., Mirzaa, G.M., Pagon, R.A., Wallace, S.E., Bean, L.J.H., Gripp, K.W., Amemiya, A., Eds.; University of Washington: Seattle, WA, USA, 1993. [Google Scholar]
- Li, Q.; Sadowski, S.; Frank, M.; Chai, C.; Váradi, A.; Ho, S.Y.; Lou, H.; Dean, M.; Thisse, C.; Thisse, B.; et al. The abcc6a gene expression is required for normal zebrafish development. J. Investig. Dermatol. 2010, 130, 2561–2568. [Google Scholar] [CrossRef]
- Van Gils, M.; Vanakker, O.M. Morpholino-Mediated Gene Knockdown in Zebrafish: It Is All About Dosage and Validation. J. Investig. Dermatol. 2019, 139, 1599–1600. [Google Scholar] [CrossRef] [PubMed]
- Van Gils, M.; Willaert, A.; De Vilder, E.Y.G.; Coucke, P.J.; Vanakker, O.M. Generation and Validation of a Complete Knockout Model of abcc6a in Zebrafish. J. Investig. Dermatol. 2018, 138, 2333–2342. [Google Scholar] [CrossRef] [PubMed]
- Kok, F.O.; Shin, M.; Ni, C.W.; Gupta, A.; Grosse, A.S.; van Impel, A.; Kirchmaier, B.C.; Peterson-Maduro, J.; Kourkoulis, G.; Male, I.; et al. Reverse genetic screening reveals poor correlation between morpholino-induced and mutant phenotypes in zebrafish. Dev. Cell 2015, 32, 97–108. [Google Scholar] [CrossRef] [PubMed]
- Mackay, E.W.; Apschner, A.; Schulte-Merker, S. Vitamin K reduces hypermineralisation in zebrafish models of PXE and GACI. Development 2015, 142, 1095–1101. [Google Scholar] [CrossRef] [PubMed]
- Sun, J.; She, P.; Liu, X.; Gao, B.; Jin, D.; Zhong, T.P. Disruption of Abcc6 Transporter in Zebrafish Causes Ocular Calcification and Cardiac Fibrosis. Int. J. Mol. Sci. 2020, 22, 278. [Google Scholar] [CrossRef] [PubMed]
- Czimer, D.; Porok, K.; Csete, D.; Gyüre, Z.; Lavró, V.; Fülöp, K.; Chen, Z.; Gyergyák, H.; Tusnády, G.E.; Burgess, S.M.; et al. A New Zebrafish Model for Pseudoxanthoma Elasticum. Front. Cell Dev. Biol. 2021, 9, 628699. [Google Scholar] [CrossRef]
- Apschner, A.; Huitema, L.F.; Ponsioen, B.; Peterson-Maduro, J.; Schulte-Merker, S. Zebrafish enpp1 mutants exhibit pathological mineralization, mimicking features of generalized arterial calcification of infancy (GACI) and pseudoxanthoma elasticum (PXE). Dis. Models Mech. 2014, 7, 811–822. [Google Scholar] [CrossRef]
- Singh, A.P.; Sosa, M.X.; Fang, J.; Shanmukhappa, S.K.; Hubaud, A.; Fawcett, C.H.; Molind, G.J.; Tsai, T.; Capodieci, P.; Wetzel, K.; et al. αKlotho Regulates Age-Associated Vascular Calcification and Lifespan in Zebrafish. Cell Rep. 2019, 28, 2767–2776.e2765. [Google Scholar] [CrossRef]
- Stevenson, N.L.; Bergen, D.J.M.; Skinner, R.E.H.; Kague, E.; Martin-Silverstone, E.; Robson Brown, K.A.; Hammond, C.L.; Stephens, D.J. Giantin-knockout models reveal a feedback loop between Golgi function and glycosyltransferase expression. J. Cell Sci. 2017, 130, 4132–4143. [Google Scholar] [CrossRef]
- Pottie, L.; Adamo, C.S.; Beyens, A.; Lütke, S.; Tapaneeyaphan, P.; De Clercq, A.; Salmon, P.L.; De Rycke, R.; Gezdirici, A.; Gulec, E.Y.; et al. Bi-allelic premature truncating variants in LTBP1 cause cutis laxa syndrome. Am. J. Hum. Genet. 2021, 108, 2386–2388. [Google Scholar] [CrossRef]
- Ziegler, S.G.; Gahl, W.A.; Ferreira, C.R. Generalized Arterial Calcification of Infancy. In GeneReviews®; Adam, M.P., Mirzaa, G.M., Pagon, R.A., Wallace, S.E., Bean, L.J.H., Gripp, K.W., Amemiya, A., Eds.; University of Washington: Seattle, WA, USA, 1993. [Google Scholar]
- Schorderet, D.F.; Nichini, O.; Boisset, G.; Polok, B.; Tiab, L.; Mayeur, H.; Raji, B.; de la Houssaye, G.; Abitbol, M.M.; Munier, F.L. Mutation in the human homeobox gene NKX5-3 causes an oculo-auricular syndrome. Am. J. Hum. Genet. 2008, 82, 1178–1184. [Google Scholar] [CrossRef] [PubMed]
- Gillespie, R.L.; Urquhart, J.; Lovell, S.C.; Biswas, S.; Parry, N.R.; Schorderet, D.F.; Lloyd, I.C.; Clayton-Smith, J.; Black, G.C. Abrogation of HMX1 function causes rare oculoauricular syndrome associated with congenital cataract, anterior segment dysgenesis, and retinal dystrophy. Investig. Ophthalmol. Vis. Sci. 2015, 56, 883–891. [Google Scholar] [CrossRef] [PubMed]
- Amendt, B.A.; Sutherland, L.B.; Russo, A.F. Transcriptional antagonism between Hmx1 and Nkx2.5 for a shared DNA-binding site. J. Biol. Chem. 1999, 274, 11635–11642. [Google Scholar] [CrossRef] [PubMed]
- El Fersioui, Y.; Pinton, G.; Allaman-Pillet, N.; Schorderet, D.F. Hmx1 regulates urfh1 expression in the craniofacial region in zebrafish. PLoS ONE 2021, 16, e0245239. [Google Scholar] [CrossRef]
- Marcelli, F.; Boisset, G.; Schorderet, D.F. A dimerized HMX1 inhibits EPHA6/epha4b in mouse and zebrafish retinas. PLoS ONE 2014, 9, e100096. [Google Scholar] [CrossRef]
- Boisset, G.; Schorderet, D.F. Zebrafish hmx1 promotes retinogenesis. Exp. Eye Res. 2012, 105, 34–42. [Google Scholar] [CrossRef]
- Pomreinke, A.P.; Soh, G.H.; Rogers, K.W.; Bergmann, J.K.; Bläßle, A.J.; Müller, P. Dynamics of BMP signaling and distribution during zebrafish dorsal-ventral patterning. eLife 2017, 6, e25861. [Google Scholar] [CrossRef]
- Fisher, S.; Halpern, M.E. Patterning the zebrafish axial skeleton requires early chordin function. Nat. Genet. 1999, 23, 442–446. [Google Scholar] [CrossRef]
- Stafford, D.A.; Monica, S.D.; Harland, R.M. Follistatin interacts with Noggin in the development of the axial skeleton. Mech. Dev. 2014, 131, 78–85. [Google Scholar] [CrossRef]
- Wijgerde, M.; Karp, S.; McMahon, J.; McMahon, A.P. Noggin antagonism of BMP4 signaling controls development of the axial skeleton in the mouse. Dev. Biol. 2005, 286, 149–157. [Google Scholar] [CrossRef]
- Chefetz, I.; Heller, R.; Galli-Tsinopoulou, A.; Richard, G.; Wollnik, B.; Indelman, M.; Koerber, F.; Topaz, O.; Bergman, R.; Sprecher, E.; et al. A novel homozygous missense mutation in FGF23 causes Familial Tumoral Calcinosis associated with disseminated visceral calcification. Hum. Genet. 2005, 118, 261–266. [Google Scholar] [CrossRef] [PubMed]
- Kurpas, A.; Supeł, K.; Idzikowska, K.; Zielińska, M. FGF23: A Review of Its Role in Mineral Metabolism and Renal and Cardiovascular Disease. Dis. Markers 2021, 2021, 8821292. [Google Scholar] [CrossRef] [PubMed]
- Shimada, T.; Kakitani, M.; Yamazaki, Y.; Hasegawa, H.; Takeuchi, Y.; Fujita, T.; Fukumoto, S.; Tomizuka, K.; Yamashita, T. Targeted ablation of Fgf23 demonstrates an essential physiological role of FGF23 in phosphate and vitamin D metabolism. J. Clin. Investig. 2004, 113, 561–568. [Google Scholar] [CrossRef]
- Ogura, Y.; Kaneko, R.; Ujibe, K.; Wakamatsu, Y.; Hirata, H. Loss of αklotho causes reduced motor ability and short lifespan in zebrafish. Sci. Rep. 2021, 11, 15090. [Google Scholar] [CrossRef] [PubMed]
- Kurosu, H.; Ogawa, Y.; Miyoshi, M.; Yamamoto, M.; Nandi, A.; Rosenblatt, K.P.; Baum, M.G.; Schiavi, S.; Hu, M.C.; Moe, O.W.; et al. Regulation of fibroblast growth factor-23 signaling by klotho. J. Biol. Chem. 2006, 281, 6120–6123. [Google Scholar] [CrossRef]
- Ten Hagen, K.G.; Fritz, T.A.; Tabak, L.A. All in the family: The UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferases. Glycobiology 2003, 13, 1R–16R. [Google Scholar] [CrossRef]
- Tiwari, V.; Zahra, F. Hyperphosphatemic Tumoral Calcinosis. In StatPearls; StatPearls Publishing: Treasure Island, FL, USA, 2023. [Google Scholar]
- Kato, K.; Jeanneau, C.; Tarp, M.A.; Benet-Pagès, A.; Lorenz-Depiereux, B.; Bennett, E.P.; Mandel, U.; Strom, T.M.; Clausen, H. Polypeptide GalNAc-transferase T3 and familial tumoral calcinosis. Secretion of fibroblast growth factor 23 requires O-glycosylation. J. Biol. Chem. 2006, 281, 18370–18377. [Google Scholar] [CrossRef]
- Gok, F.; Chefetz, I.; Indelman, M.; Kocaoglu, M.; Sprecher, E. Newly discovered mutations in the GALNT3 gene causing autosomal recessive hyperostosis-hyperphosphatemia syndrome. Acta Orthop. 2009, 80, 131–134. [Google Scholar] [CrossRef]
- Mangos, S.; Amaral, A.P.; Faul, C.; Jüppner, H.; Reiser, J.; Wolf, M. Expression of fgf23 and αklotho in developing embryonic tissues and adult kidney of the zebrafish, Danio rerio. Nephrol. Dial. Transplant. 2012, 27, 4314–4322. [Google Scholar] [CrossRef]
- Kuro-o, M. Klotho, phosphate and FGF-23 in ageing and disturbed mineral metabolism. Nat. Rev. Nephrol. 2013, 9, 650–660. [Google Scholar] [CrossRef]
- Nollet, L.L.; Vanakker, O.M. Mitochondrial Dysfunction and Oxidative Stress in Hereditary Ectopic Calcification Diseases. Int. J. Mol. Sci. 2022, 23, 15288. [Google Scholar] [CrossRef] [PubMed]
- Burton, D.G.; Krizhanovsky, V. Physiological and pathological consequences of cellular senescence. Cell. Mol. Life Sci. 2014, 71, 4373–4386. [Google Scholar] [CrossRef] [PubMed]
- Eren, M.; Boe, A.E.; Murphy, S.B.; Place, A.T.; Nagpal, V.; Morales-Nebreda, L.; Urich, D.; Quaggin, S.E.; Budinger, G.R.; Mutlu, G.M.; et al. PAI-1-regulated extracellular proteolysis governs senescence and survival in Klotho mice. Proc. Natl. Acad. Sci. USA 2014, 111, 7090–7095. [Google Scholar] [CrossRef] [PubMed]
- Mohamed, M.; Voet, M.; Gardeitchik, T.; Morava, E. Cutis Laxa. Adv. Exp. Med. Biol. 2014, 802, 161–184. [Google Scholar] [CrossRef]
- Xiong, Y.; Sun, R.; Li, J.; Wu, Y.; Zhang, J. Latent TGF-beta binding protein-1 plays an important role in craniofacial development. J. Appl. Oral. Sci. 2020, 28, e20200262. [Google Scholar] [CrossRef]
- Abrial, M.; Basu, S.; Huang, M.; Butty, V.; Schwertner, A.; Jeffrey, S.; Jordan, D.; Burns, C.E.; Burns, C.G. Latent TGFβ-binding proteins 1 and 3 protect the larval zebrafish outflow tract from aneurysmal dilatation. Dis. Models Mech. 2022, 15, dmm046979. [Google Scholar] [CrossRef]
- Choi, T.Y.; Choi, T.I.; Lee, Y.R.; Choe, S.K.; Kim, C.H. Zebrafish as an animal model for biomedical research. Exp. Mol. Med. 2021, 53, 310–317. [Google Scholar] [CrossRef]
- Ban, H.; Yokota, D.; Otosaka, S.; Kikuchi, M.; Kinoshita, H.; Fujino, Y.; Yabe, T.; Ovara, H.; Izuka, A.; Akama, K.; et al. Transcriptional autoregulation of zebrafish tbx6 is required for somite segmentation. Development 2019, 146, dev177063. [Google Scholar] [CrossRef]
- Zhang, Y.; Huang, H.; Zhao, G.; Yokoyama, T.; Vega, H.; Huang, Y.; Sood, R.; Bishop, K.; Maduro, V.; Accardi, J.; et al. ATP6V1H Deficiency Impairs Bone Development through Activation of MMP9 and MMP13. PLoS Genet. 2017, 13, e1006481. [Google Scholar] [CrossRef]
- Shen, Q.; Little, S.C.; Xu, M.; Haupt, J.; Ast, C.; Katagiri, T.; Mundlos, S.; Seemann, P.; Kaplan, F.S.; Mullins, M.C.; et al. The fibrodysplasia ossificans progressiva R206H ACVR1 mutation activates BMP-independent chondrogenesis and zebrafish embryo ventralization. J. Clin. Investig. 2009, 119, 3462–3472. [Google Scholar] [CrossRef]
- Mintzer, K.A.; Lee, M.A.; Runke, G.; Trout, J.; Whitman, M.; Mullins, M.C. Lost-a-fin encodes a type I BMP receptor, Alk8, acting maternally and zygotically in dorsoventral pattern formation. Development 2001, 128, 859–869. [Google Scholar] [CrossRef] [PubMed]
- Bauer, H.; Lele, Z.; Rauch, G.J.; Geisler, R.; Hammerschmidt, M. The type I serine/threonine kinase receptor Alk8/Lost-a-fin is required for Bmp2b/7 signal transduction during dorsoventral patterning of the zebrafish embryo. Development 2001, 128, 849–858. [Google Scholar] [CrossRef] [PubMed]
- LaBonty, M.; Pray, N.; Yelick, P.C. A Zebrafish Model of Human Fibrodysplasia Ossificans Progressiva. Zebrafish 2017, 14, 293–304. [Google Scholar] [CrossRef] [PubMed]
- Henke, K.; Daane, J.M.; Hawkins, M.B.; Dooley, C.M.; Busch-Nentwich, E.M.; Stemple, D.L.; Harris, M.P. Genetic Screen for Postembryonic Development in the Zebrafish (Danio rerio): Dominant Mutations Affecting Adult Form. Genetics 2017, 207, 609–623. [Google Scholar] [CrossRef]
- Gistelinck, C.; Kwon, R.Y.; Malfait, F.; Symoens, S.; Harris, M.P.; Henke, K.; Hawkins, M.B.; Fisher, S.; Sips, P.; Guillemyn, B.; et al. Zebrafish type I collagen mutants faithfully recapitulate human type I collagenopathies. Proc. Natl. Acad. Sci. USA 2018, 115, E8037–E8046. [Google Scholar] [CrossRef]
- Enderli, T.A.; Burtch, S.R.; Templet, J.N.; Carriero, A. Animal models of osteogenesis imperfecta: Applications in clinical research. Orthop. Res. Rev. 2016, 8, 41–55. [Google Scholar] [CrossRef]
- Fisher, S.; Jagadeeswaran, P.; Halpern, M.E. Radiographic analysis of zebrafish skeletal defects. Dev. Biol. 2003, 264, 64–76. [Google Scholar] [CrossRef]
- Fiedler, I.A.K.; Schmidt, F.N.; Wölfel, E.M.; Plumeyer, C.; Milovanovic, P.; Gioia, R.; Tonelli, F.; Bale, H.A.; Jähn, K.; Besio, R.; et al. Severely Impaired Bone Material Quality in Chihuahua Zebrafish Resembles Classical Dominant Human Osteogenesis Imperfecta. J. Bone Miner. Res. 2018, 33, 1489–1499. [Google Scholar] [CrossRef]
- Asharani, P.V.; Keupp, K.; Semler, O.; Wang, W.; Li, Y.; Thiele, H.; Yigit, G.; Pohl, E.; Becker, J.; Frommolt, P.; et al. Attenuated BMP1 function compromises osteogenesis, leading to bone fragility in humans and zebrafish. Am. J. Hum. Genet. 2012, 90, 661–674. [Google Scholar] [CrossRef]
- Kague, E.; Witten, P.E.; Soenens, M.; Campos, C.L.; Lubiana, T.; Fisher, S.; Hammond, C.; Brown, K.R.; Passos-Bueno, M.R.; Huysseune, A. Zebrafish sp7 mutants show tooth cycling independent of attachment, eruption and poor differentiation of teeth. Dev. Biol. 2018, 435, 176–184. [Google Scholar] [CrossRef]
- Giachelli, C.M. Ectopic calcification: Gathering hard facts about soft tissue mineralization. Am. J. Pathol. 1999, 154, 671–675. [Google Scholar] [CrossRef] [PubMed]
- Martin, L.; Hoppé, E.; Kauffenstein, G.; Omarjee, L.; Navasiolava, N.; Henni, S.; Willoteaux, S.; Leftheriotis, G. Early arterial calcification does not correlate with bone loss in pseudoxanthoma elasticum. Bone 2017, 103, 88–92. [Google Scholar] [CrossRef] [PubMed]
- Gielis, W.P.; de Jong, P.A.; Bartstra, J.W.; Foppen, W.; Spiering, W.; den Harder, A.M. Osteoarthritis in Pseudoxanthoma Elasticum Patients: An Explorative Imaging Study. J. Clin. Med. 2020, 9, 3898. [Google Scholar] [CrossRef] [PubMed]
- Van Gils, M.; Willaert, A.; Coucke, P.J.; Vanakker, O.M. The Abcc6a Knockout Zebrafish Model as a Novel Tool for Drug Screening for Pseudoxanthoma Elasticum. Front. Pharmacol. 2022, 13, 822143. [Google Scholar] [CrossRef]
- Nollet, L.; Van Gils, M.; Willaert, A.; Coucke, P.J.; Vanakker, O.M. Minocycline Attenuates Excessive DNA Damage Response and Reduces Ectopic Calcification in Pseudoxanthoma Elasticum. J. Investig. Dermatol. 2022, 142, 1629–1638.e6. [Google Scholar] [CrossRef]
- Kauffenstein, G.; Chappard, D.; Leftheriotis, G.; Martin, L. ABCC6 deficiency and bone loss: A double benefit of etidronate for patient presenting with pseudoxanthoma elasticum? Exp. Dermatol. 2022, 31, 1635–1637. [Google Scholar] [CrossRef]
- Brampton, C.; Yamaguchi, Y.; Vanakker, O.; Van Laer, L.; Chen, L.H.; Thakore, M.; De Paepe, A.; Pomozi, V.; Szabó, P.T.; Martin, L.; et al. Vitamin K does not prevent soft tissue mineralization in a mouse model of pseudoxanthoma elasticum. Cell Cycle 2011, 10, 1810–1820. [Google Scholar] [CrossRef]
- Gorgels, T.G.; Waarsing, J.H.; Herfs, M.; Versteeg, D.; Schoensiegel, F.; Sato, T.; Schlingemann, R.O.; Ivandic, B.; Vermeer, C.; Schurgers, L.J.; et al. Vitamin K supplementation increases vitamin K tissue levels but fails to counteract ectopic calcification in a mouse model for pseudoxanthoma elasticum. J. Mol. Med. 2011, 89, 1125–1135. [Google Scholar] [CrossRef]
- Greenblatt, M.B.; Ono, N.; Ayturk, U.M.; Debnath, S.; Lalani, S. The Unmixing Problem: A Guide to Applying Single-Cell RNA Sequencing to Bone. J. Bone Miner. Res. 2019, 34, 1207–1219. [Google Scholar] [CrossRef]
- Alvarez, M.; Schrey, A.W.; Richards, C.L. Ten years of transcriptomics in wild populations: What have we learned about their ecology and evolution? Mol. Ecol. 2015, 24, 710–725. [Google Scholar] [CrossRef]
- Boneski, P.K.; Madhu, V.; Tomlinson, R.E.; Shapiro, I.M.; van de Wetering, K.; Risbud, M.V. Abcc6 Null Mice-a Model for Mineralization Disorder PXE Shows Vertebral Osteopenia without Enhanced Intervertebral Disc Calcification with Aging. Front. Cell Dev. Biol. 2022, 10, 823249. [Google Scholar] [CrossRef] [PubMed]
- Van Gils, M.; Depauw, J.; Coucke, P.J.; Aerts, S.; Verschuere, S.; Nollet, L.; Vanakker, O.M. Inorganic Pyrophosphate Plasma Levels Are Decreased in Pseudoxanthoma Elasticum Patients and Heterozygous Carriers but Do Not Correlate with the Genotype or Phenotype. J. Clin. Med. 2023, 12, 1893. [Google Scholar] [CrossRef] [PubMed]
- Jansen, R.S.; Duijst, S.; Mahakena, S.; Sommer, D.; Szeri, F.; Váradi, A.; Plomp, A.; Bergen, A.A.; Oude Elferink, R.P.; Borst, P.; et al. ABCC6-mediated ATP secretion by the liver is the main source of the mineralization inhibitor inorganic pyrophosphate in the systemic circulation-brief report. Arterioscler. Thromb. Vasc. Biol. 2014, 34, 1985–1989. [Google Scholar] [CrossRef] [PubMed]
- Sánchez-Tévar, A.M.; García-Fernández, M.; Murcia-Casas, B.; Rioja-Villodres, J.; Carrillo, J.L.; Camacho, M.; Van Gils, M.; Sánchez-Chaparro, M.A.; Vanakker, O.; Valdivielso, P. Plasma inorganic pyrophosphate and alkaline phosphatase in patients with pseudoxanthoma elasticum. Ann. Transl. Med. 2019, 7, 798. [Google Scholar] [CrossRef]
- Leftheriotis, G.; Navasiolava, N.; Clotaire, L.; Duranton, C.; Le Saux, O.; Bendahhou, S.; Laurain, A.; Rubera, I.; Martin, L. Relationships between Plasma Pyrophosphate, Vascular Calcification and Clinical Severity in Patients Affected by Pseudoxanthoma Elasticum. J. Clin. Med. 2022, 11, 2588. [Google Scholar] [CrossRef]
- Ferreira, C.R.; Kintzinger, K.; Hackbarth, M.E.; Botschen, U.; Nitschke, Y.; Mughal, M.Z.; Baujat, G.; Schnabel, D.; Yuen, E.; Gahl, W.A.; et al. Ectopic Calcification and Hypophosphatemic Rickets: Natural History of ENPP1 and ABCC6 Deficiencies. J. Bone Miner. Res. 2021, 36, 2193–2202. [Google Scholar] [CrossRef]
- Li, C.; Chai, Y.; Wang, L.; Gao, B.; Chen, H.; Gao, P.; Zhou, F.Q.; Luo, X.; Crane, J.L.; Yu, B.; et al. Programmed cell senescence in skeleton during late puberty. Nat. Commun. 2017, 8, 1312. [Google Scholar] [CrossRef]
- Wan, M.; Gray-Gaillard, E.F.; Elisseeff, J.H. Cellular senescence in musculoskeletal homeostasis, diseases, and regeneration. Bone Res. 2021, 9, 41. [Google Scholar] [CrossRef]
- Miglionico, R.; Ostuni, A.; Armentano, M.F.; Milella, L.; Crescenzi, E.; Carmosino, M.; Bisaccia, F. ABCC6 knockdown in HepG2 cells induces a senescent-like cell phenotype. Cell. Mol. Biol. Lett. 2017, 22, 7. [Google Scholar] [CrossRef]
- Tiemann, J.; Wagner, T.; Lindenkamp, C.; Plümers, R.; Faust, I.; Knabbe, C.; Hendig, D. Linking ABCC6 Deficiency in Primary Human Dermal Fibroblasts of PXE Patients to p21-Mediated Premature Cellular Senescence and the Development of a Proinflammatory Secretory Phenotype. Int. J. Mol. Sci. 2020, 21, 9665. [Google Scholar] [CrossRef]
- Sato, C.; Iso, Y.; Mizukami, T.; Otabe, K.; Sasai, M.; Kurata, M.; Sanbe, T.; Sekiya, I.; Miyazaki, A.; Suzuki, H. Fibroblast growth factor-23 induces cellular senescence in human mesenchymal stem cells from skeletal muscle. Biochem. Biophys. Res. Commun. 2016, 470, 657–662. [Google Scholar] [CrossRef] [PubMed]
- Cheikhi, A.; Barchowsky, A.; Sahu, A.; Shinde, S.N.; Pius, A.; Clemens, Z.J.; Li, H.; Kennedy, C.A.; Hoeck, J.D.; Franti, M.; et al. Klotho: An Elephant in Aging Research. J. Gerontol. A Biol. Sci. Med. Sci. 2019, 74, 1031–1042. [Google Scholar] [CrossRef] [PubMed]
- Hosen, M.J.; Coucke, P.J.; Le Saux, O.; De Paepe, A.; Vanakker, O.M. Perturbation of specific pro-mineralizing signalling pathways in human and murine pseudoxanthoma elasticum. Orphanet J. Rare Dis. 2014, 9, 66. [Google Scholar] [CrossRef] [PubMed]
- Wu, M.; Chen, G.; Li, Y.P. TGF-β and BMP signaling in osteoblast, skeletal development, and bone formation, homeostasis and disease. Bone Res. 2016, 4, 16009. [Google Scholar] [CrossRef] [PubMed]
- Guo, X.; Wang, X.F. Signaling cross-talk between TGF-beta/BMP and other pathways. Cell Res. 2009, 19, 71–88. [Google Scholar] [CrossRef]
- Feng, X.H.; Derynck, R. Specificity and versatility in tgf-beta signaling through Smads. Annu. Rev. Cell Dev. Biol. 2005, 21, 659–693. [Google Scholar] [CrossRef]
- Bernabeu, C.; Lopez-Novoa, J.M.; Quintanilla, M. The emerging role of TGF-beta superfamily coreceptors in cancer. Biochim. Biophys. Acta 2009, 1792, 954–973. [Google Scholar] [CrossRef]
- Chen, G.; Deng, C.; Li, Y.P. TGF-β and BMP signaling in osteoblast differentiation and bone formation. Int. J. Biol. Sci. 2012, 8, 272–288. [Google Scholar] [CrossRef]
- Koba, T.; Watanabe, K.; Goda, S.; Kitagawa, M.; Mutoh, N.; Hamada, N.; Tani-Ishii, N. The Effect of Transforming Growth Factor Beta 1 on the Mineralization of Human Cementoblasts. J. Endod. 2021, 47, 606–611. [Google Scholar] [CrossRef]
- Payne, T.L.; Postlethwait, J.H.; Yelick, P.C. Functional characterization and genetic mapping of alk8. Mech. Dev. 2001, 100, 275–289. [Google Scholar] [CrossRef]
- Tylzanowski, P.; Verschueren, K.; Huylebroeck, D.; Luyten, F.P. Smad-interacting protein 1 is a repressor of liver/bone/kidney alkaline phosphatase transcription in bone morphogenetic protein-induced osteogenic differentiation of C2C12 cells. J. Biol. Chem. 2001, 276, 40001–40007. [Google Scholar] [CrossRef]
- Zhang, D.; Schwarz, E.M.; Rosier, R.N.; Zuscik, M.J.; Puzas, J.E.; O’Keefe, R.J. ALK2 functions as a BMP type I receptor and induces Indian hedgehog in chondrocytes during skeletal development. J. Bone Miner. Res. 2003, 18, 1593–1604. [Google Scholar] [CrossRef] [PubMed]
- Hendig, D.; Zarbock, R.; Szliska, C.; Kleesiek, K.; Götting, C. The local calcification inhibitor matrix Gla protein in pseudoxanthoma elasticum. Clin. Biochem. 2008, 41, 407–412. [Google Scholar] [CrossRef] [PubMed]
- Price, P.A.; Nguyen, T.M.; Williamson, M.K. Biochemical characterization of the serum fetuin-mineral complex. J. Biol. Chem. 2003, 278, 22153–22160. [Google Scholar] [CrossRef] [PubMed]
- Miura, Y.; Iwazu, Y.; Shiizaki, K.; Akimoto, T.; Kotani, K.; Kurabayashi, M.; Kurosu, H.; Kuro, O.M. Identification and quantification of plasma calciprotein particles with distinct physical properties in patients with chronic kidney disease. Sci. Rep. 2018, 8, 1256. [Google Scholar] [CrossRef]
- Gelli, R.; Pucci, V.; Ridi, F.; Baglioni, P. A study on biorelevant calciprotein particles: Effect of stabilizing agents on the formation and crystallization mechanisms. J. Colloid Interface Sci. 2022, 620, 431–441. [Google Scholar] [CrossRef]
- Smith, E.R.; Hewitson, T.D.; Jahnen-Dechent, W. Calciprotein particles: Mineral behaving badly? Curr. Opin. Nephrol. Hypertens. 2020, 29, 378–386. [Google Scholar] [CrossRef]
- Kutikhin, A.G.; Feenstra, L.; Kostyunin, A.E.; Yuzhalin, A.E.; Hillebrands, J.L.; Krenning, G. Calciprotein Particles: Balancing Mineral Homeostasis and Vascular Pathology. Arterioscler. Thromb. Vasc. Biol. 2021, 41, 1607–1624. [Google Scholar] [CrossRef]
- Köppert, S.; Büscher, A.; Babler, A.; Ghallab, A.; Buhl, E.M.; Latz, E.; Hengstler, J.G.; Smith, E.R.; Jahnen-Dechent, W. Cellular Clearance and Biological Activity of Calciprotein Particles Depend on Their Maturation State and Crystallinity. Front. Immunol. 2018, 9, 1991. [Google Scholar] [CrossRef]
- Hendig, D.; Schulz, V.; Arndt, M.; Szliska, C.; Kleesiek, K.; Götting, C. Role of serum fetuin-A, a major inhibitor of systemic calcification, in pseudoxanthoma elasticum. Clin. Chem. 2006, 52, 227–234. [Google Scholar] [CrossRef]
- Nollet, L.; Van Gils, M.; Fischer, S.; Campens, L.; Karthik, S.; Pasch, A.; De Zaeytijd, J.; Leroy, B.P.; Devos, D.; De Backer, T.; et al. Serum Calcification Propensity T50 Associates with Disease Severity in Patients with Pseudoxanthoma Elasticum. J. Clin. Med. 2022, 11, 3727. [Google Scholar] [CrossRef] [PubMed]
- Gheduzzi, D.; Boraldi, F.; Annovi, G.; DeVincenzi, C.P.; Schurgers, L.J.; Vermeer, C.; Quaglino, D.; Ronchetti, I.P. Matrix Gla protein is involved in elastic fiber calcification in the dermis of pseudoxanthoma elasticum patients. Lab. Investig. 2007, 87, 998–1008. [Google Scholar] [CrossRef] [PubMed]
- Blazquez-Medela, A.M.; Guihard, P.J.; Yao, J.; Jumabay, M.; Lusis, A.J.; Boström, K.I.; Yao, Y. ABCC6 deficiency is associated with activation of BMP signaling in liver and kidney. FEBS Open Bio 2015, 5, 257–263. [Google Scholar] [CrossRef] [PubMed]
- Pasch, A. Novel assessments of systemic calcification propensity. Curr. Opin. Nephrol. Hypertens. 2016, 25, 278–284. [Google Scholar] [CrossRef] [PubMed]
- Pasch, A.; Farese, S.; Gräber, S.; Wald, J.; Richtering, W.; Floege, J.; Jahnen-Dechent, W. Nanoparticle-based test measures overall propensity for calcification in serum. J. Am. Soc. Nephrol. 2012, 23, 1744–1752. [Google Scholar] [CrossRef]
- Pasch, A.; Jahnen-Dechent, W.; Smith, E.R. Phosphate, Calcification in Blood, and Mineral Stress: The Physiologic Blood Mineral Buffering System and Its Association with Cardiovascular Risk. Int. J. Nephrol. 2018, 2018, 9182078. [Google Scholar] [CrossRef]
- Komori, T. Regulation of Proliferation, Differentiation and Functions of Osteoblasts by Runx2. Int. J. Mol. Sci. 2019, 20, 1694. [Google Scholar] [CrossRef]
- Lee, K.S.; Kim, H.J.; Li, Q.L.; Chi, X.Z.; Ueta, C.; Komori, T.; Wozney, J.M.; Kim, E.G.; Choi, J.Y.; Ryoo, H.M.; et al. Runx2 is a common target of transforming growth factor beta1 and bone morphogenetic protein 2, and cooperation between Runx2 and Smad5 induces osteoblast-specific gene expression in the pluripotent mesenchymal precursor cell line C2C12. Mol. Cell. Biol. 2000, 20, 8783–8792. [Google Scholar] [CrossRef]
- van der Meulen, T.; Kranenbarg, S.; Schipper, H.; Samallo, J.; van Leeuwen, J.L.; Franssen, H. Identification and characterisation of two runx2 homologues in zebrafish with different expression patterns. Biochim. Biophys. Acta 2005, 1729, 105–117. [Google Scholar] [CrossRef]
- Liu, D.D.; Zhang, C.Y.; Liu, Y.; Li, J.; Wang, Y.X.; Zheng, S.G. RUNX2 Regulates Osteoblast Differentiation via the BMP4 Signaling Pathway. J. Dent. Res. 2022, 101, 1227–1237. [Google Scholar] [CrossRef]
- Feger, M.; Hase, P.; Zhang, B.; Hirche, F.; Glosse, P.; Lang, F.; Föller, M. The production of fibroblast growth factor 23 is controlled by TGF-β2. Sci. Rep. 2017, 7, 4982. [Google Scholar] [CrossRef] [PubMed]
- Sasaki, T.; Ito, Y.; Bringas, P., Jr.; Chou, S.; Urata, M.M.; Slavkin, H.; Chai, Y. TGFbeta-mediated FGF signaling is crucial for regulating cranial neural crest cell proliferation during frontal bone development. Development 2006, 133, 371–381. [Google Scholar] [CrossRef] [PubMed]
- Lavi-Moshayoff, V.; Wasserman, G.; Meir, T.; Silver, J.; Naveh-Many, T. PTH increases FGF23 gene expression and mediates the high-FGF23 levels of experimental kidney failure: A bone parathyroid feedback loop. Am. J. Physiol. Renal Physiol. 2010, 299, F882–F889. [Google Scholar] [CrossRef] [PubMed]
- Qiu, T.; Wu, X.; Zhang, F.; Clemens, T.L.; Wan, M.; Cao, X. TGF-beta type II receptor phosphorylates PTH receptor to integrate bone remodelling signalling. Nat. Cell Biol. 2010, 12, 224–234. [Google Scholar] [CrossRef] [PubMed]
- Zerr, P.; Vollath, S.; Palumbo-Zerr, K.; Tomcik, M.; Huang, J.; Distler, A.; Beyer, C.; Dees, C.; Gela, K.; Distler, O.; et al. Vitamin D receptor regulates TGF-β signalling in systemic sclerosis. Ann. Rheum. Dis. 2015, 74, e20. [Google Scholar] [CrossRef]
- Irani, M.; Seifer, D.B.; Grazi, R.V.; Julka, N.; Bhatt, D.; Kalgi, B.; Irani, S.; Tal, O.; Lambert-Messerlian, G.; Tal, R. Vitamin D Supplementation Decreases TGF-β1 Bioavailability in PCOS: A Randomized Placebo-Controlled Trial. J. Clin. Endocrinol. Metab. 2015, 100, 4307–4314. [Google Scholar] [CrossRef]
- Subramaniam, N.; Leong, G.M.; Cock, T.A.; Flanagan, J.L.; Fong, C.; Eisman, J.A.; Kouzmenko, A.P. Cross-talk between 1,25-dihydroxyvitamin D3 and transforming growth factor-beta signaling requires binding of VDR and Smad3 proteins to their cognate DNA recognition elements. J. Biol. Chem. 2001, 276, 15741–15746. [Google Scholar] [CrossRef]
- Doi, S.; Zou, Y.; Togao, O.; Pastor, J.V.; John, G.B.; Wang, L.; Shiizaki, K.; Gotschall, R.; Schiavi, S.; Yorioka, N.; et al. Klotho inhibits transforming growth factor-beta1 (TGF-beta1) signaling and suppresses renal fibrosis and cancer metastasis in mice. J. Biol. Chem. 2011, 286, 8655–8665. [Google Scholar] [CrossRef] [PubMed]
- Urakawa, I.; Yamazaki, Y.; Shimada, T.; Iijima, K.; Hasegawa, H.; Okawa, K.; Fujita, T.; Fukumoto, S.; Yamashita, T. Klotho converts canonical FGF receptor into a specific receptor for FGF23. Nature 2006, 444, 770–774. [Google Scholar] [CrossRef]
- de Las Rivas, M.; Paul Daniel, E.J.; Narimatsu, Y.; Compañón, I.; Kato, K.; Hermosilla, P.; Thureau, A.; Ceballos-Laita, L.; Coelho, H.; Bernadó, P.; et al. Molecular basis for fibroblast growth factor 23 O-glycosylation by GalNAc-T3. Nat. Chem. Biol. 2020, 16, 351–360. [Google Scholar] [CrossRef]
- Li, Y.; Hu, F.; Xue, M.; Jia, Y.J.; Zheng, Z.J.; Wang, L.; Guan, M.P.; Xue, Y.M. Klotho down-regulates Egr-1 by inhibiting TGF-β1/Smad3 signaling in high glucose treated human mesangial cells. Biochem. Biophys. Res. Commun. 2017, 487, 216–222. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Xue, M.; Hu, F.; Jia, Y.; Zheng, Z.; Yang, Y.; Liu, X.; Yang, Y.; Wang, Y. Klotho prevents epithelial-mesenchymal transition through Egr-1 downregulation in diabetic kidney disease. BMJ Open Diabetes Res. Care 2021, 9, e002038. [Google Scholar] [CrossRef] [PubMed]
- Toan, N.K.; Tai, N.C.; Kim, S.A.; Ahn, S.G. Soluble Klotho regulates bone differentiation by upregulating expression of the transcription factor EGR-1. FEBS Lett. 2020, 594, 290–300. [Google Scholar] [CrossRef] [PubMed]
- Roberts, A.B.; McCune, B.K.; Sporn, M.B. TGF-beta: Regulation of extracellular matrix. Kidney Int. 1992, 41, 557–559. [Google Scholar] [CrossRef] [PubMed]
- Robertson, I.B.; Rifkin, D.B. Regulation of the Bioavailability of TGF-β and TGF-β-Related Proteins. Cold Spring Harb. Perspect. Biol. 2016, 8, a021907. [Google Scholar] [CrossRef]
- Laue, K.; Pogoda, H.M.; Daniel, P.B.; van Haeringen, A.; Alanay, Y.; von Ameln, S.; Rachwalski, M.; Morgan, T.; Gray, M.J.; Breuning, M.H.; et al. Craniosynostosis and multiple skeletal anomalies in humans and zebrafish result from a defect in the localized degradation of retinoic acid. Am. J. Hum. Genet. 2011, 89, 595–606. [Google Scholar] [CrossRef]
- Spoorendonk, K.M.; Peterson-Maduro, J.; Renn, J.; Trowe, T.; Kranenbarg, S.; Winkler, C.; Schulte-Merker, S. Retinoic acid and Cyp26b1 are critical regulators of osteogenesis in the axial skeleton. Development 2008, 135, 3765–3774. [Google Scholar] [CrossRef]
- Delbaere, S.; Van Damme, T.; Syx, D.; Symoens, S.; Coucke, P.; Willaert, A.; Malfait, F. Hypomorphic zebrafish models mimic the musculoskeletal phenotype of β4GalT7-deficient Ehlers-Danlos syndrome. Matrix Biol. 2020, 89, 59–75. [Google Scholar] [CrossRef]
- Buchan, J.G.; Gray, R.S.; Gansner, J.M.; Alvarado, D.M.; Burgert, L.; Gitlin, J.D.; Gurnett, C.A.; Goldsmith, M.I. Kinesin family member 6 (kif6) is necessary for spine development in zebrafish. Dev. Dyn. 2014, 243, 1646–1657. [Google Scholar] [CrossRef]
- Grimes, D.T.; Boswell, C.W.; Morante, N.F.; Henkelman, R.M.; Burdine, R.D.; Ciruna, B. Zebrafish models of idiopathic scoliosis link cerebrospinal fluid flow defects to spine curvature. Science 2016, 352, 1341–1344. [Google Scholar] [CrossRef]
- Gray, R.S.; Wilm, T.P.; Smith, J.; Bagnat, M.; Dale, R.M.; Topczewski, J.; Johnson, S.L.; Solnica-Krezel, L. Loss of col8a1a function during zebrafish embryogenesis results in congenital vertebral malformations. Dev. Biol. 2014, 386, 72–85. [Google Scholar] [CrossRef] [PubMed]
- Van Gennip, J.L.M.; Boswell, C.W.; Ciruna, B. Neuroinflammatory signals drive spinal curve formation in zebrafish models of idiopathic scoliosis. Sci. Adv. 2018, 4, eaav1781. [Google Scholar] [CrossRef] [PubMed]
- Zancan, I.; Bellesso, S.; Costa, R.; Salvalaio, M.; Stroppiano, M.; Hammond, C.; Argenton, F.; Filocamo, M.; Moro, E. Glucocerebrosidase deficiency in zebrafish affects primary bone ossification through increased oxidative stress and reduced Wnt/β-catenin signaling. Hum. Mol. Genet. 2015, 24, 1280–1294. [Google Scholar] [CrossRef] [PubMed]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Van Wynsberghe, J.; Vanakker, O.M. Significance of Premature Vertebral Mineralization in Zebrafish Models in Mechanistic and Pharmaceutical Research on Hereditary Multisystem Diseases. Biomolecules 2023, 13, 1621. https://doi.org/10.3390/biom13111621
Van Wynsberghe J, Vanakker OM. Significance of Premature Vertebral Mineralization in Zebrafish Models in Mechanistic and Pharmaceutical Research on Hereditary Multisystem Diseases. Biomolecules. 2023; 13(11):1621. https://doi.org/10.3390/biom13111621
Chicago/Turabian StyleVan Wynsberghe, Judith, and Olivier M. Vanakker. 2023. "Significance of Premature Vertebral Mineralization in Zebrafish Models in Mechanistic and Pharmaceutical Research on Hereditary Multisystem Diseases" Biomolecules 13, no. 11: 1621. https://doi.org/10.3390/biom13111621
APA StyleVan Wynsberghe, J., & Vanakker, O. M. (2023). Significance of Premature Vertebral Mineralization in Zebrafish Models in Mechanistic and Pharmaceutical Research on Hereditary Multisystem Diseases. Biomolecules, 13(11), 1621. https://doi.org/10.3390/biom13111621