GALNT3, a gene associated with hyperphosphatemic familial tumoral calcinosis, is transcriptionally regulated by extracellular phosphate and modulates matrix metalloproteinase activity

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1792, Issue 1, 2009, Pages 61-67

  Chefetz, Ilana ^a,b   Kohno, Kimitoshi ^c   Izumi, Hiroto ^c   Uitto, Jouni ^d   Richard, Gabriele ^d,e   Sprecher, Eli ^a,b  

^a Laboratory of Molecular Dermatology   (Israel)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^c UNIVERSITY OF OCCUPATIONAL AND ENVIRONMENTAL HEALTH   (Japan)

^d THOMAS JEFFERSON UNIVERSITY   (United States)

^e GENEDX   (United States)

Author keywords

Calcification; Calcinosis; Phosphate

Indexed keywords

CALCITRIOL; CALCIUM; KERATINOCYTE GROWTH FACTOR; MATRIX METALLOPROTEINASE; N ACETYLGALACTOSAMINYLTRANSFERASE; N ACETYLGALACTOSAMINYLTRANSFERASE 3; PHOSPHATE; UNCLASSIFIED DRUG;

ARTICLE; AUTOSOMAL RECESSIVE DISORDER; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; EXTRACELLULAR SPACE; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HYPERPHOSPHATEMIA; HYPERPHOSPHATEMIC FAMILIAL TUMORAL CALCINOSIS; PATHOGENESIS; PHOSPHATE METABOLISM; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN FIBROBLAST; TUMOR CALCINOSIS;

BASE SEQUENCE; CALCINOSIS; CELLS, CULTURED; DNA PRIMERS; DOWN-REGULATION; EXTRACELLULAR FLUID; FIBROBLAST GROWTH FACTOR 7; FIBROBLASTS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; HYPERPHOSPHATEMIA; MATRIX METALLOPROTEINASES; MUTATION; N-ACETYLGALACTOSAMINYLTRANSFERASES; PHOSPHATES; RNA, SMALL INTERFERING; SKIN;

EID: 57849151929     PISSN: 09254439     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbadis.2008.09.016     Document Type: Article

References (64)

1. Renkema K.Y., Alexander R.T., Bindels R.J., and Hoenderop J.G. Calcium and phosphate homeostasis: concerted interplay of new regulators. Ann. Med. 40 (2008) 82-91
2. Kestenbaum B. Phosphate metabolism in the setting of chronic kidney disease: significance and recommendations for treatment. Semin. Dial. 20 (2007) 286-294
3. Melamed M.L., Eustace J.A., Plantinga L., Jaar B.G., Fink N.E., Coresh J., Klag M.J., and Powe N.R. Changes in serum calcium, phosphate, and PTH and the risk of death in incident dialysis patients: a longitudinal study. Kidney Int. 70 (2006) 351-357
4. Tonelli M., Sacks F., Pfeffer M., Gao Z., and Curhan G. Relation between serum phosphate level and cardiovascular event rate in people with coronary disease. Circulation 112 (2005) 2627-2633
5. Caudarella R., Vescini F., Buffa A., and Francucci C.M. Hyperphosphatemia: effects on bone metabolism and cardiovascular risk. J. Endocrinol. Invest. 30 (2007) 29-34
6. White K.E., Larsson T.E., and Econs M.J. The roles of specific genes implicated as circulating factors involved in normal and disordered phosphate homeostasis: frizzled related protein-4, matrix extracellular phosphoglycoprotein, and fibroblast growth factor 23. Endocrine Rev. 27 (2006) 221-241
7. Sprecher E. Tumoral calcinosis: new insights for the rheumatologist into a familial crystal deposition disease. Curr. Rheumatol. Re. 9 (2007) 237-242
8. Garringer H.J., Mortazavi S.M., Esteghamat F., Malekpour M., Boztepe H., Tanakol R., Davis S.I., and White K.E. Two novel GALNT3 mutations in familial tumoral calcinosis. Am. J. Med. Genet. 143A (2007) 2390-2396
9. Barbieri A.M., Filopanti M., Bua G., and Beck-Peccoz P. Two novel nonsense mutations in GALNT3 gene are responsible for familial tumoral calcinosis. J. Hum. Gen. 52 (2007) 464-468
10. Ichikawa S., Imel E.A., Sorenson A.H., Severe R., Knudson P., Harris G.J., Shaker J.L., and Econs M.J. Tumoral calcinosis presenting with eyelid calcifications due to novel missense mutations in the glycosyl transferase domain of the GALNT3 gene. J. Clin. Endocrinol. Metabol. 91 (2006) 4472-4475
11. Garringer H.J., Fisher C., Larsson T.E., Davis S.I., Koller D.L., Cullen M.J., Draman M.S., Conlon N., Jain A., Fedarko N.S., Dasgupta B., and White K.E. The role of mutant UDP-N-acetyl-alpha-D-galactosamine-polypeptide N-acetylgalactosaminyltransferase 3 in regulating serum intact fibroblast growth factor 23 and matrix extracellular phosphoglycoprotein in heritable tumoral calcinosis. J. Clin. Endocrinol. Metabol. 91 (2006) 4037-4042
12. Campagnoli M.F., Pucci A., Garelli E., Carando A., Defilippi C., Lala R., Ingrosso G., Dianzani I., Forni M., and Ramenghi U. Familial tumoral calcinosis and testicular microlithiasis associated with a new mutation of GALNT3 in a white family. J. Clin. Pathol. 59 (2006) 440-442
13. Specktor P., Cooper J.G., Indelman M., and Sprecher E. Hyperphosphatemic familial tumoral calcinosis caused by a mutation in GALNT3 in a European kindred. J. Hum. Genet. 51 (2006) 487-490
14. Ichikawa S., Lyles K.W., and Econs M.J. A novel GALNT3 mutation in a pseudoautosomal dominant form of tumoral calcinosis: evidence that the disorder is autosomal recessive. J. Clin. Endocrinol. Metabol. 90 (2005) 2420-2423
15. Topaz O., Shurman D.L., Bergman R., Indelman M., Ratajczak P., Mizrachi M., Khamaysi Z., Behar D., Petronius D., Friedman V., Zelikovic I., Raimer S., Metzker A., Richard G., and Sprecher E. Mutations in GALNT3, encoding a protein involved in O-linked glycosylation, cause familial tumoral calcinosis. Nat. Genet. 36 (2004) 579-581
16. Bennett E.P., Hassan H., and Clausen H. cDNA cloning and expression of a novel human UDP-N-acetyl-alpha-D-galactosamine. Polypeptide N-acetylgalactosaminyltransferase, GalNAc-t3. J. Biol. Chem. 271 (1996) 17006-17012
17. Araya K., Fukumoto S., Backenroth R., Takeuchi Y., Nakayama K., Ito N., Yoshii N., Yamazaki Y., Yamashita T., Silver J., Igarashi T., and Fujita T. A novel mutation in fibroblast growth factor 23 gene as a cause of tumoral calcinosis. J. Clin. Endocrinol. Metabol. 90 (2005) 5523-5527
18. Benet-Pages A., Orlik P., Strom T.M., and Lorenz-Depiereux B. An FGF23 missense mutation causes familial tumoral calcinosis with hyperphosphatemia. Hum. Mol. Genet. 14 (2005) 385-390
19. Chefetz I., Heller R., Galli-Tsinopoulou A., Richard G., Wollnik B., Indelman M., Koerber F., Topaz O., Bergman R., Sprecher E., and Schoenau E. A novel homozygous missense mutation in FGF23 causes Familial Tumoral Calcinosis associated with disseminated visceral calcification. Hum. Genet. 118 (2005) 261-266
20. Larsson T., Yu X., Davis S.I., Draman M.S., Mooney S.D., Cullen M.J., and White K.E. A novel recessive mutation in fibroblast growth factor-23 causes familial tumoral calcinosis. J. Clin. Endocrinol. Metabol. 90 (2005) 2424-2427
21. Stubbs J., Liu S., and Quarles L.D. Role of fibroblast growth factor 23 in phosphate homeostasis and pathogenesis of disordered mineral metabolism in chronic kidney disease. Semin. Dial. 20 (2007) 302-308
22. Yu X., and White K.E. FGF23 and disorders of phosphate homeostasis. Cytokine Growth Factor Rev. 16 (2005) 221-232
23. Frishberg Y., Ito N., Rinat C., Yamazaki Y., Feinstein S., Urakawa I., Navon-Elkan P., Becker-Cohen R., Yamashita T., Araya K., Igarashi T., Fujita T., and Fukumoto S. Hyperostosis-hyperphosphatemia syndrome: a congenital disorder of O-glycosylation associated with augmented processing of fibroblast growth factor 23. J. Bone Miner. Res. 22 (2007) 235-242
24. Kato K., Jeanneau C., Tarp M.A., Benet-Pages A., Lorenz-Depiereux B., Bennett E.P., Mandel U., Strom T.M., and Clausen H. Polypeptide GalNAc-transferase T3 and familial tumoral calcinosis. Secretion of fibroblast growth factor 23 requires O-glycosylation. J. Biol. Chem. 281 (2006) 18370-18377
25. Larsson T., Davis S.I., Garringer H.J., Mooney S.D., Draman M.S., Cullen M.J., and White K.E. Fibroblast growth factor-23 mutants causing familial tumoral calcinosis are differentially processed. Endocrinology 146 (2005) 3883-3891
26. 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. A homozygous missense mutation in human KLOTHO causes severe tumoral calcinosis. J. Muscul. Neuron. Inter. 7 (2007) 318-319
27. 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. A homozygous missense mutation in human KLOTHO causes severe tumoral calcinosis. J. Clin. Invest. 117 (2007) 2684-2691
28. Urakawa I., Yamazaki Y., Shimada T., Iijima K., Hasegawa H., Okawa K., Fujita T., Fukumoto S., and Yamashita T. Klotho converts canonical FGF receptor into a specific receptor for FGF23. Nature 444 (2006) 770-774
29. Saito H., Kusano K., Kinosaki M., Ito H., Hirata M., Segawa H., Miyamoto K., and Fukushima N. Human fibroblast growth factor-23 mutants suppress Na+-dependent phosphate co-transport activity and 1alpha,25-dihydroxyvitamin D3 production. J. Biol. Chem. 278 (2003) 2206-2211
30. Bouvet C., Moreau S., Blanchette J., de Blois D., and Moreau P. Sequential activation of matrix metalloproteinase 9 and transforming growth factor beta in arterial elastocalcinosis. Arterioscler. Thromb.Vasc. Biol. 28 (2008) 856-862
31. Qin X., Corriere M.A., Matrisian L.M., and Guzman R.J. Matrix metalloproteinase inhibition attenuates aortic calcification. Arterioscler. Thromb. Vasc. Biol. 26 (2006) 1510-1516
32. Scatena M., Liaw L., and Giachelli C.M. Osteopontin: a multifunctional molecule regulating chronic inflammation and vascular disease. Arterioscler. Thromb. Vasc. Biol. 27 (2007) 2302-2309
33. Simionescu A., Simionescu D.T., and Vyavahare N.R. Osteogenic responses in fibroblasts activated by elastin degradation products and transforming growth factor-beta1: role of myofibroblasts in vascular calcification. Am. J. Pathol. 171 (2007) 116-123
34. Bodnar A.G., Ouellette M., Frolkis M., Holt S.E., Chiu C.P., Morin G.B., Harley C.B., Shay J.W., Lichtsteiner S., and Wright W.E. Extension of life-span by introduction of telomerase into normal human cells. Science 279 (1998) 349-352
35. Nomoto M., Izumi H., Ise T., Kato K., Takano H., Nagatani G., Shibao K., Ohta R., Imamura T., Kuwano M., Matsuo K., Yamada Y., Itoh H., and Kohno K. Structural basis for the regulation of UDP-N-acetyl-alpha-D-galactosamine: polypeptide N-acetylgalactosaminyl transferase-3 gene expression in adenocarcinoma cells. Cancer Res. 59 (1999) 6214-6222
36. Dosaka-Akita H., Kinoshita I., Yamazaki K., Izumi H., Itoh T., Katoh H., Nishimura M., Matsuo K., Yamada Y., and Kohno K. N-acetylgalactosaminyl transferase-3 is a potential new marker for non-small cell lung cancers. Br. J. Cancer 87 (2002) 751-755
37. White A.R., Du T., Laughton K.M., Volitakis I., Sharples R.A., Xilinas M.E., Hoke D.E., Holsinger R.M., Evin G., Cherny R.A., Hill A.F., Barnham K.J., Li Q.X., Bush A.I., and Masters C.L. Degradation of the Alzheimer disease amyloid beta-peptide by metal-dependent up-regulation of metalloprotease activity. J. Biol. Chem. 281 (2006) 17670-17680
38. Meleti Z., Shapiro I.M., and Adams C.S. Inorganic phosphate induces apoptosis of osteoblast-like cells in culture. Bone 27 (2000) 359-366
39. Szczepanska-Konkel M., Yusufi A.N., VanScoy M., Webster S.K., and Dousa T.P. Phosphonocarboxylic acids as specific inhibitors of Na+-dependent transport of phosphate across renal brush border membrane. J. Biol. Chem. 261 (1986) 6375-6383
40. Carpenter T.O., Ellis B.K., Insogna K.L., Philbrick W.M., Sterpka J., and Shimkets R. Fibroblast growth factor 7: an inhibitor of phosphate transport derived from oncogenic osteomalacia-causing tumors. J. Clin. Endocrinol. Metabol. 90 (2005) 1012-1020
41. auf demKeller U., Krampert M., Kumin A., Braun S., and Werner S. Keratinocyte growth factor: effects on keratinocytes and mechanisms of action. Eur. J. Cell Biol. 83 (2004) 607-612
42. Topaz O., Bergman R., Mandel U., Maor G., Goldberg R., Richard G., and Sprecher E. Absence of intraepidermal glycosyltransferase ppGalNac-T3 expression in familial tumoral calcinosis. Am. J. Dermatopathol. 27 (2005) 211-215
43. Madlener M., Mauch C., Conca W., Brauchle M., Parks W.C., and Werner S. Regulation of the expression of stromelysin-2 by growth factors in keratinocytes: implications for normal and impaired wound healing. Biochem. J. 320 Pt 2 (1996) 659-664
44. Ropiquet F., Huguenin S., Villette J.M., Ronfle V., Le Brun G., Maitland N.J., Cussenot O., Fiet J., and Berthon P. FGF7/KGF triggers cell transformation and invasion on immortalised human prostatic epithelial PNT1A cells. Int. J. Cancer 82 (1999) 237-243
45. Shin E.Y., Ma E.K., Kim C.K., Kwak S.J., and Kim E.G. Src/ERK but not phospholipase D is involved in keratinocyte growth factor-stimulated secretion of matrix metalloprotease-9 and urokinase-type plasminogen activator in SNU-16 human stomach cancer cell. J. Cancer Res. Clin. Oncol. 128 (2002) 596-602
46. Simian M., Hirai Y., Navre M., Werb Z., Lochter A., and Bissell M.J. The interplay of matrix metalloproteinases, morphogens and growth factors is necessary for branching of mammary epithelial cells. Development 128 (2001) 3117-3131
47. Fukumoto S. Physiological regulation and disorders of phosphate metabolism-pivotal role of fibroblast growth factor 23. Intern. Med. 47 (2008) 337-343
48. Uribarri J. Phosphorus homeostasis in normal health and in chronic kidney disease patients with special emphasis on dietary phosphorus intake. Semin. Dial. 20 (2007) 295-301
49. Antonarakis S.E., and Beckmann J.S. Mendelian disorders deserve more attention. Nat. Rev. Genet. 7 (2006) 277-282
50. Olauson H., Krajisnik T., Larsson C., Lindberg B., and Larsson T.E. A novel missense mutation in GALNT3 causing hyperostosis-hyperphosphataemia syndrome. Eur. J. Endocrinol. 158 (2008) 929-934
51. Ichikawa S., Guigonis V., Imel E.A., Courouble M., Heissat S., Henley J.D., Sorenson A.H., Petit B., Lienhardt A., and Econs M.J. Novel GALNT3 mutations causing hyperostosis-hyperphosphatemia syndrome result in low intact fibroblast growth factor 23 concentrations. J. Clin. Endocrinol. Metabol. 92 (2007) 1943-1947
52. Ten Hagen K.G., Fritz T.A., and Tabak L.A. All in the family: the UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferases. Glycobiology 13 (2003) 1R-16R
53. E.S. Molloy, M.P. Morgan, G.A. Doherty, B. McDonnell, J. O'Byrne, D.J. Fitzgerald, G.M. McCarthy, Mechanism of basic calcium phosphate crystal-stimulated matrix metalloproteinase-13 expression in osteoarthritic synovial fibroblasts: inhibition by prostaglandin E2, Ann. Rheum. Dis. (2008), in press.
54. Reuben P.M., Wenger L., Cruz M., and Cheung H.S. Induction of matrix metalloproteinase-8 in human fibroblasts by basic calcium phosphate and calcium pyrophosphate dihydrate crystals: effect of phosphocitrate. Connect. Tissue Res. 42 (2001) 1-12
55. Bai G., Howell D.S., Howard G.A., Roos B.A., and Cheung H.S. Basic calcium phosphate crystals up-regulate metalloproteinases but down-regulate tissue inhibitor of metalloproteinase-1 and -2 in human fibroblasts. Osteoarthritis Cartilage 9 (2001) 416-422
56. McCarthy G.M., Macius A.M., Christopherson P.A., Ryan L.M., and Pourmotabbed T. Basic calcium phosphate crystals induce synthesis and secretion of 92 kDa gelatinase (gelatinase B/matrix metalloprotease 9) in human fibroblasts. Ann. Rheum. Dis. 57 (1998) 56-60
57. Boulman N., Slobodin G., Rozenbaum M., and Rosner I. Calcinosis in rheumatic diseases. Semin. Arthritis Rheum. 34 (2005) 805-812
58. Cohen H., Solomon V., Alferiev I.S., Breuer E., Ornoy A., Patlas N., Eidelman N., Hagele G., and Golomb G. Bisphosphonates and tetracycline: experimental models for their evaluation in calcium-related disorders. Pharm. Res. 15 (1998) 606-613
59. Slavin R.E., Wen J., Kumar D., and Evans E.B. Familial tumoral calcinosis. A clinical, histopathologic, and ultrastructural study with an analysis of its calcifying process and pathogenesis. Am. J. Surg. Pathol. 17 (1993) 788-802
60. Steinherz R., Chesney R.W., Eisenstein B., Metzker A., DeLuca H.F., and Phelps M. Elevated serum calcitriol concentrations do not fall in response to hyperphosphatemia in familial tumoral calcinosis. Am. J. Dis. Child. (1960) 139 (1985) 816-819
61. Metzker A., Eisenstein B., Oren J., and Samuel R. Tumoral calcinosis revisited-common and uncommon features. Report of ten cases and review. Eur. J. Ped. 147 (1988) 128-132
62. Hendig D., Schulz V., Arndt M., Szliska C., Kleesiek K., and Gotting C. Role of serum fetuin-A, a major inhibitor of systemic calcification, in pseudoxanthoma elasticum. Clin. Chem. 52 (2006) 227-234
63. Hendig D., Arndt M., Szliska C., Kleesiek K., and Gotting C. SPP1 promoter polymorphisms: identification of the first modifier gene for pseudoxanthoma elasticum. Clin. Chem. 53 (2007) 829-836
64. Jiang Q., Li Q., and Uitto J. Aberrant mineralization of connective tissues in a mouse model of pseudoxanthoma elasticum: systemic and local regulatory factors. J. Invest. Dermatol. 127 (2007) 1392-1402