Zebrafish enpp1 mutants exhibit pathological mineralization, mimicking features of generalized arterial calcification of infancy (GACI) and pseudoxanthoma elasticum (PXE)

DMM Disease Models and Mechanisms

Volumn 7, Issue 7, 2014, Pages 811-822

  Apschner, Alexander ^a   Huitema, Leonie F A ^a   Ponsioen, Bas ^a   Peterson Maduro, Josi ^a   Schulte Merker, Stefan ^a,b,c  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b WUR Experimental Zoology ^*  (Netherlands)

^c UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Ectopic mineralization; GACI; Generalized arterial calcification of infancy; Pseudoxanthoma elasticum; PXE; Pyrophosphate; Zebrafish

Indexed keywords

ETIDRONIC ACID; INORGANIC PYROPHOSPHATASE; OSTEOPONTIN; PYROPHOSPHATE; BIOLOGICAL MARKER; CALCIUM; ECTONUCLEOTIDE PYROPHOSPHATASE PHOSPHODIESTERASE 1; PHOSPHATE; PHOSPHODIESTERASE;

ANIMAL CELL; ARTERY CALCIFICATION; ARTICLE; BIOMINERALIZATION; CONTROLLED STUDY; GENE EXPRESSION; GENERALIZED ARTERIAL CALCIFICATION OF INFANCY; MUTANT; NONHUMAN; NOTOCHORD; OSTEOBLAST; PHOSPHATE METABOLISM; PRIORITY JOURNAL; PSEUDOXANTHOMA ELASTICUM; ZEBRA FISH; ANIMAL; CALCINOSIS; CHORISTOMA; COMPLICATION; DRUG EFFECTS; ENZYMOLOGY; GENETICS; HOMEOSTASIS; HUMAN; METABOLISM; MUTATION; OSTEOCLAST; PATHOLOGY; PHENOTYPE; VASCULAR CALCIFICATION;

ANIMALS; BIOLOGICAL MARKERS; CALCINOSIS; CALCIUM; CHORISTOMA; ETIDRONIC ACID; HOMEOSTASIS; HUMANS; MUTATION; NOTOCHORD; OSTEOCLASTS; PHENOTYPE; PHOSPHATES; PHOSPHORIC DIESTER HYDROLASES; PSEUDOXANTHOMA ELASTICUM; PYROPHOSPHATASES; VASCULAR CALCIFICATION; ZEBRAFISH;

EID: 84903942398     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.015693     Document Type: Article

References (73)

1. Aiba, A., Nakajima, A., Okawa, A., Koda, M. and Yamazaki, M. (2009). Evidence of enhanced expression of osteopontin in spinal hyperostosis of the twy mouse. Spine 34, 1644-1649.
2. Apschner, A., Schulte-Merker, S. and Witten, P. E. (2011). Chapter 10 - Not all bones are created equal - using zebrafish and other teleost species in osteogenesis research. In Methods in Cell Biology, Vol. 105 (ed. M. Westerfield, H. William Dietrich and L. I. Zon). Waltham, MA: Academic Press.
3. Asakawa, K., Suster, M. L., Mizusawa, K., Nagayoshi, S., Kotani, T., Urasaki, A., Kishimoto, Y., Hibi, M. and Kawakami, K. (2008). Genetic dissection of neural circuits by Tol2 transposon-mediated Gal4 gene and enhancer trapping in zebrafish. Proc. Natl. Acad. Sci. USA 105, 1255-1260. (Pubitemid 351397040)
4. Balciunas, D., Wangensteen, K. J., Wilber, A., Bell, J., Geurts, A., Sivasubbu, S., Wang, X., Hackett, P. B., Largaespada, D. A., McIvor, R. S. et al. (2006). Harnessing a high cargo-capacity transposon for genetic applications in vertebrates. PLoS Genet. 2, e169.
5. Bancroft, J. S. A. (1996a). van Gieson Theory and Practice of Histological Techniques. pp. 127-188. New York, NY: Churchill Livingstone.
6. Bancroft, J. S. A. (1996b). von Kossa Theory and Practice of Histological Techniques. p. 332. New York, NY: Churchill Livingstone.
7. Bas, A., Lopez, I., Perez, J., Rodriguez, M. and Aguilera-Tejero, E. (2006). Reversibility of calcitriol-induced medial artery calcification in rats with intact renal function. J. Bone Miner. Res. 21, 484-490.
8. Beis, D., Bartman, T., Jin, S. W., Scott, I. C., D'Amico, L. A., Ober, E. A., Verkade, H., Frantsve, J., Field, H. A., Wehman, A. et al. (2005). Genetic and cellular analyses of zebrafish atrioventricular cushion and valve development. Development 132, 4193-4204. (Pubitemid 41488867)
9. Bensimon-Brito, A., Cardeira, J., Cancela, M. L., Huysseune, A. and Witten, P. E. (2012). Distinct patterns of notochord mineralization in zebrafish coincide with the localization of Osteocalcin isoform 1 during early vertebral centra formation. BMC Dev. Biol. 12, 28.
10. Brand, M. G. M. and Nuesslein-Vollhard, C. (2002). Keeping and raising zebrafish. In Zebrafish, A Practical Approach (ed. C. Nüsslein-Volhard and R. Dahm), pp. 7-37 New York, NY: Oxford University Press.
11. Bussmann, J. and Schulte-Merker, S. (2011). Rapid BAC selection for tol2-mediated transgenesis in zebrafish. Development 138, 4327-4332.
12. Chatani, M., Takano, Y. and Kudo, A. (2011). Osteoclasts in bone modeling, as revealed by in vivo imaging, are essential for organogenesis in fish. Dev. Biol. 360, 96-109.
13. d'Alençon, C. A., Peña, O. A., Wittmann, C., Gallardo, V. E., Jones, R. A., Loosli, F., Liebel, U., Grabher, C. and Allende, M. L. (2010). A high-throughput chemically induced inflammation assay in zebrafish. BMC Biol. 8, 151.
14. Dale, R. M. and Topczewski, J. (2011). Identification of an evolutionarily conserved regulatory element of the zebrafish col2a1a gene. Dev. Biol. 357, 518-531.
15. Doherty, T. M., Uzui, H., Fitzpatrick, L. A., Tripathi, P. V., Dunstan, C. R., Asotra, K. and Rajavashisth, T. B. (2002). Rationale for the role of osteoclast-like cells in arterial calcification. FASEB J. 16, 577-582. (Pubitemid 34273241)
16. Edouard, T., Chabot, G., Miro, J., Buhas, D. C., Nitschke, Y., Lapierre, C., Rutsch, F. and Alos, N. (2011). Efficacy and safety of 2-year etidronate treatment in a child with generalized arterial calcification of infancy. Eur. J. Pediatr. 170, 1585-1590.
17. Edsall, S. C. and Franz-Odendaal, T. A. (2010). A quick whole-mount staining protocol for bone deposition and resorption. Zebrafish 7, 275-280.
18. Ellett, F., Pase, L., Hayman, J. W., Andrianopoulos, A. and Lieschke, G. J. (2011). mpeg1 promoter transgenes direct macrophage-lineage expression in zebrafish. Blood 117, e49-e56.
19. Ertzer, R., Müller, F., Hadzhiev, Y., Rathnam, S., Fischer, N., Rastegar, S. and Strähle, U. (2007). Cooperation of sonic hedgehog enhancers in midline expression. Dev. Biol. 301, 578-589. (Pubitemid 46073986)
20. Fang, M., Adams, J. S., McMahan, B. L., Brown, R. J. and Oxford, J. T. (2010). The expression patterns of minor fibrillar collagens during development in zebrafish. Gene Expr. Patterns 10, 315-322.
21. Ganesh, S. K., Stack, A. G., Levin, N. W., Hulbert-Shearon, T. and Port, F. K. (2001). Association of elevated serum PO(4), Ca × PO(4) product, and parathyroid hormone with cardiac mortality risk in chronic hemodialysis patients. J. Am. Soc. Nephrol. 12, 2131-2138. (Pubitemid 32880350)
22. Giachelli, C. M. (1999). Ectopic calcification: gathering hard facts about soft tissue mineralization. Am. J. Pathol. 154, 671-675. (Pubitemid 29122585)
23. Giachelli, C. M. (2008). Ectopic Mineralization: New Concepts in Etiology and Regulation. Weinheim, Germany: Wiley-VCH Verlag GmbH.
24. Giachelli, C. M. and Steitz, S. (2000). Osteopontin: a versatile regulator of inflammation and biomineralization. Matrix Biol. 19, 615-622.
25. Giachelli, C. M., Lombardi, D., Johnson, R. J., Murry, C. E. and Almeida, M. (1998). Evidence for a role of osteopontin in macrophage infiltration in response to pathological stimuli in vivo. Am. J. Pathol. 152, 353-358. (Pubitemid 28106380)
26. Goodman, W. G., Goldin, J., Kuizon, B. D., Yoon, C., Gales, B., Sider, D., Wang, Y., Chung, J., Emerick, A., Greaser, L. et al. (2000). Coronary-artery calcification in young adults with end-stage renal disease who are undergoing dialysis. N. Engl. J. Med. 342, 1478-1483. (Pubitemid 30318271)
27. Gordon, K., Schulte, D., Brice, G., Simpson, M. A., Roukens, M. G., van Impel, A., Connell, F., Kalidas, K., Jeffery, S., Mortimer, P. S. et al. (2013). Mutation in vascular endothelial growth factor-C, a ligand for vascular endothelial growth factor receptor-3, is associated with autosomal dominant milroy-like primary lymphedema. Circ. Res. 112, 956-960.
28. Grotmol, S., Nordvik, K., Kryvi, H. and Totland, G. K. (2005). A segmental pattern of alkaline phosphatase activity within the notochord coincides with the initial formation of the vertebral bodies. J. Anat. 206, 427-436. (Pubitemid 40711582)
29. Hammond, C. L. and Schulte-Merker, S. (2009). Two populations of endochondral osteoblasts with differential sensitivity to Hedgehog signalling. Development 136, 3991-4000.
30. Hori, M., Shimizu, Y. and Fukumoto, S. (2011). Minireview: fibroblast growth factor 23 in phosphate homeostasis and bone metabolism. Endocrinology 152, 4-10.
31. Hu, N., Yost, H. J. and Clark, E. B. (2001). Cardiac morphology and blood pressure in the adult zebrafish. Anat. Rec. 264, 1-12. (Pubitemid 32800517)
32. Huang, C. J., Tu, C. T., Hsiao, C. D., Hsieh, F. J. and Tsai, H. J. (2003). Germ-line transmission of a myocardium-specific GFP transgene reveals critical regulatory elements in the cardiac myosin light chain 2 promoter of zebrafish. Dev. Dyn. 228, 30-40.
33. Huitema, L. F., Apschner, A., Logister, I., Spoorendonk, K. M., Bussmann, J., Hammond, C. L. and Schulte-Merker, S. (2012). Entpd5 is essential for skeletal mineralization and regulates phosphate homeostasis in zebrafish. Proc. Natl. Acad. Sci. USA 109, 21372-21377.
34. Hynie, I., Meuffels, M. and Poznanski, W. J. (1975). Determination of phosphodiesterase I activity in human blood serum. Clin. Chem. 21, 1383-1387.
35. Ichikawa, S., Imel, E. A., Kreiter, M. L., Yu, X., Mackenzie, D. S., Sorenson, A. H., Goetz, R., Mohammadi, M., White, K. E. and Econs, M. J. (2007). A homozygous missense mutation in human KLOTHO causes severe tumoral calcinosis. J. Clin. Invest. 117, 2684-2691. (Pubitemid 47494368)
36. Jansen, R. S., Küçükosmanoglu, A., de Haas, M., Sapthu, S., Otero, J. A., Hegman, I. E. M., Bergen, A. A. B., Gorgels, T. G. M. F., Borst, P. and van de Wetering, K. (2013). ABCC6 prevents ectopic mineralization seen in pseudoxanthoma elasticum by inducing cellular nucleotide release. Proc. Natl. Acad. Sci. USA 110, 20206-20211.
37. Jeziorska, M., McCollum, C. and Wooley, D. E. (1998). Observations on bone formation and remodelling in advanced atherosclerotic lesions of human carotid arteries. Virchows Arch. 433, 559-565. (Pubitemid 28561189)
38. Johnson, K., Goding, J., van Etten, D., Sali, A., Hu, S. I., Farley, D., Krug, H., Hessle, L., Millán, J. L. and Terkeltaub, R. (2003). Linked deficiencies in extracellular PP(i) and osteopontin mediate pathologic calcification associated with defective PC-1 and ANK expression. J. Bone Miner. Res. 18, 994-1004. (Pubitemid 37294935)
39. Johnson, K., Polewski, M., van Etten, D. and Terkeltaub, R. (2005). Chondrogenesis mediated by PPi depletion promotes spontaneous aortic calcification in NPP1-/-mice. Arterioscler. Thromb. Vasc. Biol. 25, 686-691. (Pubitemid 40463854)
40. Kato, K., Nishimasu, H., Okudaira, S., Mihara, E., Ishitani, R., Takagi, J., Aoki, J. and Nureki, O. (2012). Crystal structure of Enpp1, an extracellular glycoprotein involved in bone mineralization and insulin signaling. Proc. Natl. Acad. Sci. USA 109, 16876-16881.
41. Kirsch, T. (2012). Biomineralization - an active or passive process? Connect. Tissue Res. 53, 438-445.
42. Krukowski, M. and Kahn, A. J. (1982). Inductive specificity of mineralized bone matrix in ectopic osteoclast differentiation. Calcif. Tissue Int. 34, 474-479. (Pubitemid 13222871)
43. Le Guellec, D., Morvan-Dubois, G. and Sire, J. Y. (2004). Skin development in bony fish with particular emphasis on collagen deposition in the dermis of the zebrafish (Danio rerio). Int. J. Dev. Biol. 48, 217-231. (Pubitemid 38807937)
44. Li, Q., Schumacher, W., Jablonski, D., Siegel, D. and Uitto, J. (2012). Cutaneous features of pseudoxanthoma elasticum in a patient with generalized arterial calcification of infancy due to a homozygous missense mutation in the ENPP1 gene. Br. J. Dermatol. 166, 1107-1111.
45. Li, Q., Guo, H., Chou, D. W., Berndt, A., Sundberg, J. P. and Uitto, J. (2013). Mutant Enpp1asj mice as a model for generalized arterial calcification of infancy. Dis. Model. Mech. 6, 1227-1235.
46. Ljusberg, J., Wang, Y., Lång, P., Norgård, M., Dodds, R., Hultenby, K., Ek-Rylander, B. and Andersson, G. (2005). Proteolytic excision of a repressive loop domain in tartrate-resistant acid phosphatase by cathepsin K in osteoclasts. J. Biol. Chem. 280, 28370-28381. (Pubitemid 41105735)
47. Lorenz-Depiereux, B., Schnabel, D., Tiosano, D., Häusler, G. and Strom, T. M. (2010). Loss-of-function ENPP1 mutations cause both generalized arterial calcification of infancy and autosomal-recessive hypophosphatemic rickets. Am. J. Hum. Genet. 86, 267-272.
48. Luo, G., Ducy, P., McKee, M. D., Pinero, G. J., Loyer, E., Behringer, R. R. and Karsenty, G. (1997). Spontaneous calcification of arteries and cartilage in mice lacking matrix GLA protein. Nature 386, 78-81. (Pubitemid 27130923)
49. Mackay, E. W., Apschner, A. and Schulte-Merker, S. (2013). A bone to pick with zebrafish. Bonekey Rep. 2, 445.
50. Mackenzie, N. C., Huesa, C., Rutsch, F. and MacRae, V. E. (2012a). New insights into NPP1 function: lessons from clinical and animal studies. Bone 51, 961-968.
51. Mackenzie, N. C., Zhu, D., Milne, E. M., van 't Hof, R., Martin, A., Darryl Quarles, L., Millán, J. L., Farquharson, C. and MacRae, V. E. (2012b). Altered bone development and an increase in FGF-23 expression in Enpp1(-/-) mice. PLoS ONE 7, e32177.
52. Merry, K., Dodds, R., Littlewood, A. and Gowen, M. (1993). Expression of osteopontin mRNA by osteoclasts and osteoblasts in modelling adult human bone. J. Cell Sci. 104, 1013-1020. (Pubitemid 23154308)
53. Min, H., Morony, S., Sarosi, I., Dunstan, C. R., Capparelli, C., Scully, S., Van, G., Kaufman, S., Kostenuik, P. J., Lacey, D. L. et al. (2000). Osteoprotegerin reverses osteoporosis by inhibiting endosteal osteoclasts and prevents vascular calcification by blocking a process resembling osteoclastogenesis. J. Exp. Med. 192, 463-474. (Pubitemid 30666247)
54. Mitchell, R. E., Huitema, L. F., Skinner, R. E., Brunt, L. H., Severn, C., Schulte-Merker, S. and Hammond, C. L. (2013). New tools for studying osteoarthritis genetics in zebrafish. Osteoarthritis Cartilage 21, 269-278.
55. Murshed, M., Harmey, D., Millán, J. L., McKee, M. D. and Karsenty, G. (2005). Unique coexpression in osteoblasts of broadly expressed genes accounts for the spatial restriction of ECM mineralization to bone. Genes Dev. 19, 1093-1104. (Pubitemid 40632454)
56. Neven, E., Dauwe, S., De Broe, M. E., D'Haese, P. C. and Persy, V. (2007). Endochondral bone formation is involved in media calcification in rats and in men. Kidney Int. 72, 574-581. (Pubitemid 47312790)
57. 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. (2012). Generalized arterial calcification of infancy and pseudoxanthoma elasticum can be caused by mutations in either ENPP1 or ABCC6. Am. J. Hum. Genet. 90, 25-39.
58. Rowe, P. S. (2012). The chicken or the egg: PHEX, FGF23 and SIBLINGs unscrambled. Cell Biochem. Funct. 30, 355-375.
59. Rutsch, F., Ruf, N., Vaingankar, S., Toliat, M. R., Suk, A., Höhne, W., Schauer, G., Lehmann, M., Roscioli, T., Schnabel, D. et al. (2003). Mutations in ENPP1 are associated with 'idiopathic' infantile arterial calcification. Nat. Genet. 34, 379-381. (Pubitemid 36935330)
60. Rutsch, F., Böyer, P., Nitschke, Y., Ruf, N., Lorenz-Depierieux, B., Wittkampf, T., Weissen-Plenz, G., Fischer, R. J., Mughal, Z., Gregory, J. W. et al.; GACI Study Group (2008). Hypophosphatemia, hyperphosphaturia, and bisphosphonate treatment are associated with survival beyond infancy in generalized arterial calcification of infancy. Circ Cardiovasc Genet 1, 133-140.
61. Schulte-Merker, S. (2002). Looking at embryos. In Zebrafish, A Practical Approach (ed. C. Nüsslein-Volhard and R. Dahm), pp. 41-43. New York, NY: Oxford University Press.
62. Sodek, J., Ganss, B. and McKee, M. D. (2000). Osteopontin. Crit. Rev. Oral Biol. Med. 11, 279-303.
63. Spoorendonk, K. M., Hammond, C. L., Huitema, L. F. A., Vanoevelen, J. and Schulte-Merker, S. (2010). Zebrafish as a unique model system in bone research: the power of genetics and in vivo imaging. J. Applied Ichthyology 26, 219-224.
64. Spoorendonk, K. M., Peterson-Maduro, J., Renn, J., Trowe, T., Kranenbarg, S., Winkler, C. and Schulte-Merker, S. (2008). Retinoic acid and Cyp26b1 are critical regulators of osteogenesis in the axial skeleton. Development 135, 3765-3774.
65. Steitz, S. A., Speer, M. Y., McKee, M. D., Liaw, L., Almeida, M., Yang, H. and Giachelli, C. M. (2002). Osteopontin inhibits mineral deposition and promotes regression of ectopic calcification. Am. J. Pathol. 161, 2035-2046. (Pubitemid 35434850)
66. Terkeltaub, R. A. (2001). Inorganic pyrophosphate generation and disposition in pathophysiology. Am. J. Physiol. 281, C1-C11.
67. To, T. T., Witten, P. E., Renn, J., Bhattacharya, D., Huysseune, A. and Winkler, C. (2012). Rankl-induced osteoclastogenesis leads to loss of mineralization in a medaka osteoporosis model. Development 139, 141-150.
68. Vanoevelen, J., Janssens, A., Huitema, L. F., Hammond, C. L., Metz, J. R., Flik, G., Voets, T. and Schulte-Merker, S. (2011). Trpv5/6 is vital for epithelial calcium uptake and bone formation. FASEB J. 25, 3197-3207.
69. Walker, M. B. and Kimmel, C. B. (2007). A two-color acid-free cartilage and bone stain for zebrafish larvae. Biotech. Histochem. 82, 23-28. (Pubitemid 46839257)
70. Wang, S., Kryvi, H., Grotmol, S., Wargelius, A., Krossøy, C., Epple, M., Neues, F., Furmanek, T. and Totland, G. K. (2013). Mineralization of the vertebral bodies in Atlantic salmon (Salmo salar L.) is initiated segmentally in the form of hydroxyapatite crystal accretions in the notochord sheath. J. Anat. 223, 159-170.
71. Witten, P. E., Bendahmane, M. and Abou-Haila, A. (1997). Enzyme histochemical characteristics of osteoblasts and mononucleated osteoclasts in a teleost fish with acellular bone (Oreochromis niloticus, Cichlidae). Cell Tissue Res. 287, 591-599. (Pubitemid 27113139)
72. Witten, P. E., Hansen, A. and Hall, B. K. (2001). Features of mono- and multinucleated bone resorbing cells of the zebrafish Danio rerio and their contribution to skeletal development, remodeling, and growth. J. Morphol. 250, 197-207. (Pubitemid 33087222)
73. Yamamoto, M., Morita, R., Mizoguchi, T., Matsuo, H., Isoda, M., Ishitani, T., Chitnis, A. B., Matsumoto, K., Crump, J. G., Hozumi, K. et al. (2010). Mib-Jag1-Notch signalling regulates patterning and structural roles of the notochord by controlling cell-fate decisions. Development 137, 2527-2537.