Impaired osteoblast and osteoclast function characterize the osteoporosis of Snyder - Robinson syndrome

Orphanet Journal of Rare Diseases

Volumn 10, Issue 1, 2015, Pages

  Albert, Jessica S ^a,b   Bhattacharyya, Nisan ^c   Wolfe, Lynne A ^a,b   Bone, William P ^a   Maduro, Valerie ^a   Accardi, John ^a   Adams, David R ^a,b   Schwartz, Charles E ^d   Norris, Joy ^c   Wood, Tim ^d   Gafni, Rachel I ^c   Collins, Michael T ^c   Tosi, Laura L ^e,f   Markello, Thomas C ^a,b   Gahl, William A ^a,b   Boerkoel, Cornelius F ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^c NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^d GREENWOOD GENETIC CENTER   (United States)

^e GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^f CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

Author keywords

Osteoblast; Osteoclast; Osteoporosis; Snyder Robinson syndrome; Spermine

Indexed keywords

POLYAMINE; SPERMIDINE; SPERMINE; SPERMINE SYNTHASE; VISUAL PIGMENT;

ARTICLE; BONE; BONE MASS; BONE MINERALIZATION; BONE RADIOGRAPHY; CASE REPORT; CHILD; CRANIOFACIAL MALFORMATION; FIBROBLAST CULTURE; HISTOPATHOLOGY; HUMAN; HYPOGLYCEMIA; INTELLECTUAL IMPAIRMENT; KIDNEY CALCIFICATION; KIDNEY CYST; LOSS OF FUNCTION MUTATION; MALE; NUCLEOTIDE SEQUENCE; OSSIFICATION; OSTEOBLAST; OSTEOCLAST; OSTEOPOROSIS; POLYAMINE METABOLISM; RARE DISEASE; RESPIRATORY TRACT INFECTION; SCOLIOSIS; SNYDER ROBINSON SYNDROME; SYNDROME; TISSUE SPECIFICITY; X CHROMOSOME LINKED DISORDER; FIBROBLAST; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM; MUTATION; PATHOLOGY; X LINKED MENTAL RETARDATION;

FIBROBLASTS; HUMANS; MALE; MENTAL RETARDATION, X-LINKED; MESENCHYMAL STROMAL CELLS; MUTATION; OSTEOBLASTS; OSTEOCLASTS; OSTEOPOROSIS; SPERMIDINE; SPERMINE; SPERMINE SYNTHASE;

EID: 84929081676     PISSN: None     EISSN: 17501172     Source Type: Journal    
DOI: 10.1186/s13023-015-0235-8     Document Type: Article

References (57)

1. D'Agostino L, Di Luccia A. Polyamines interact with DNA as molecular aggregates. Eur J Biochem. 2002;269(17):4317-25.
2. Watanabe S, Ksama-Equchi K, Kobayashi H, Igarashi K. Estimation of polyamine binding to macromolecules and ATP in bovine lymphocytes and rat liver. J Biol Chem. 1991;266(31):20803-9.
3. Minois N, Carmona-Gutierrez D, Madeo F. Polyamines in aging and disease. Aging. 2011;3(8):716-32.
4. Raina A, Janne J. Physiology of the natural polyamines putrescine, spermidine and spermine. Med Biol. 1975;53(3):121-47.
5. Pegg AE, Michael AJ. Spermine synthase. Cell Mol Life Sci. 2010;67(1):113-21.
6. Williams K. Interactions of polyamines with ion channels. Biochem J. 1997;325(Pt 2):289-97.
7. Janne O, Bardin CW, Jacob ST. DNA-dependent RNA polymerases I and II from kidney. Effect of polyamines on the in vitro transcription of DNA and chromatin. Biochemistry. 1975;14(16):3589-97.
8. Friedman ME, Bachrach U. Inhibition of protein synthesis by spermine in growing cells of Staphylococcus aureus. J Bacteriol. 1966;92(1):49-55.
9. Nichols CG, Lopatin AN. Inward rectifier potassium channels. Annu Rev Physiol. 1997;59:171-91.
10. Snyder RD, Robinson A. Recessive sex-linked mental retardation in the absence of other recognizable abnormalities. Report of a family. Clin Pediatr. 1969;8(11):669-74.
11. Arena JF, Schwartz C, Ouzts L, Stevenson R, Miller M, Garza J, et al. X-linked mental retardation with thin habitus, osteoporosis, and kyphoscoliosis: linkage to Xp21.3-p22.12. Am J Med Genet. 1996;64(1):50-8.
12. Cason AL, Ikequchi Y, Skinner C, Wood TC, Holder KR, Lubs JA, et al. X-linked spermine synthase gene (SMS) defect: the first polyamine deficiency syndrome. Eur J Hum Genet. 2003;11(12):937-44.
13. de Alencastro G, McCloskey DE, Kliemann SE, Maranduba CM, Pegg AE, Wang X, et al. New SMS mutation leads to a striking reduction in spermine synthase protein function and a severe form of Snyder-Robinson X-linked recessive mental retardation syndrome. J Med Genet. 2008;45(8):539-43.
14. Becerra-Solano LE, Butler J, Castaneda-Cisneros G, McCloskey DE, Wang X, Pegg AE, et al. A missense mutation, p.V132G, in the X-linked spermine synthase gene (SMS) causes Snyder-Robinson syndrome. Am J Med Genet. 2009;149A(3):328-35.
15. Schwartz CE, Wang X, Stevenson RE, Pegg AE. Spermine Synthase Deficiency Resulting in X-Linked Intellectual Disability (Snyder-Robinson Syndrome). In: Pegg AE, Castero Jr RA, editors. Polyamines: Methods and Protocols. New York: Humana Press; 2011. p. 437-45.
16. Peron A, Spaccini L, Norris J, Bova SM, Selicorni A, Weber G, et al. Snyder-Robinson syndrome: a novel nonsense mutation in spermine synthase and expansion of the phenotype. Am J Med Genet A. 2013;161(9):2316-20.
17. Zhang Z, Norris J, Kalscheuer V, Wood T, Wang L, Schwartz C, et al. A Y328C missense mutation in spermine synthase causes a mild form of Snyder-Robinson syndrome. Hum Mol Genet. 2013;22(18):3789-97.
18. Raisz LG. Pathogenesis of osteoporosis: concepts, conflicts, and prospects. J Clin Invest. 2005;115(12):3318-25.
19. Guntur AR, Rosen CJ. Bone as an endocrine organ. Endocr Pract. 2012;18(5):758-62.
20. Albert J, Schwartz CE, Boerkoel CF, Stevenson RE. Snyder-Robinson Syndrome. In: Pagon RA, Adam MP, Ardinger HH, Bird TD, Dolan CR, Fong CT, et al., editors. Seattle (WA): GeneReviews(R); 1993.
21. Zemel BS, Leonard MB, Kelly A, Lappe JM, Gilsanz V, Oberfield S, et al. Height adjustment in assessing dual energy x-ray absorptiometry measurements of bone mass and density in children. J Clin Endocrinol Metab. 2010;95(3):1265-73.
22. Wang K, Li M, Hadley D, Liu R, Glessner J, Grant SF, et al. PennCNV: an integrated hidden Markov model designed for high-resolution copy number variation detection in whole-genome SNP genotyping data. Genome Res. 2007;17(11):1665-74.
23. Manoli I, Golas G, Westbroek W, Vilboux T, Markello TC, Introne W, et al. Chediak-Higashi syndrome with early developmental delay resulting from paternal heterodisomy of chromosome 1. Am J Med Genet A. 2010;152A(6):1474-83.
24. Markello TC, Adams DR, Genome-scale sequencing to identify genes involved in Mendelian disorders. Current protocols in human genetics / editorial board, Jonathan L. Haines [et al], 2013. 79: p. Unit 6 13.
25. Adams DR, Sincan M, Fuentes Fajardo K, Mullikin JC, Pierson TM, et al. Analysis of DNA sequence variants detected by highthroughput sequencing. Hum Mutat. 2012;33(4):599-608.
26. Markello TC, Han T, Carlson-Donohoe H, Ahaghotu C, Harper U, Jones M, et al. Recombination mapping using Boolean logic and highdensity SNP genotyping for exome sequence filtering. Mol Genet Metab. 2012;105(3):382-9.
27. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, et al. A method and server for predicting damaging missense mutations. Nat Methods. 2010;7(4):248-9.
28. Johnston JJ, Teer JK, Cherukuri PF, Hansen NF, Loftus SK, NIH Intramural Sequencing Center (NISC), et al. Massively parallel sequencing of exons on the X chromosome identifies RBM10 as the gene that causes a syndromic form of cleft palate. Am J Hum Genet. 2010;86(5):743-8.
29. Kumar P, Henikoff S, Ng PC. Predicting the effects of coding nonsynonymous variants on protein function using the SIFT algorithm. Nat Protoc. 2009;4(7):1073-81.
30. Ng PC, Henikoff S. Predicting the effects of amino acid substitutions on protein function. Annu Rev Genomics Hum Genet. 2006;7:61-80.
31. Ng PC, Henikoff S. SIFT: Predicting amino acid changes that affect protein function. Nucleic Acids Res. 2003;31(13):3812-4.
32. Ng PC, Henikoff S. Accounting for human polymorphisms predicted to affect protein function. Genome Res. 2002;12(3):436-46.
33. Ng PC, Henikoff S. Predicting deleterious amino acid substitutions. Genome Res. 2001;11(5):863-74.
34. Henikoff S, Henikoff JG. Amino acid substitution matrices from protein blocks. Proc Natl Acad Sci U S A. 1992;89(22):10915-9.
35. McCarthy EF, Earnest K, Rossiter K, Shapiro J. Bone histomorphometry in adults with type IA osteogenesis imperfecta. Clin Orthop Relat Res. 1997;336:254-62.
36. Sowell J, Norris J, Jones K, Schwartz C, Wood T. Diagnostic screening for spermine synthase deficiency by liquid chromatography tandem mass spectrometry. Clin Chim Acta. 2011;412(7-8):655-60.
37. Bhattacharyya N, Wiench M, Dumitrescu C, Connolly BM, Bugge TH, Patel HV, et al. Mechanism of FGF23 processing in fibrous dysplasia. J Bone Miner Res Off J Am Soc Bone Miner Res. 2012;27(5):1132-41.
38. Kodiha M, Umar R, Stochaj U. Optimized immunofluorescence staining protocol to detect the nucleoporin Nup98 in different subcellular compartments. Protocol Exchange, 2009.
39. Wu H, Min J, Zeng H, McCloskey DE, Ikeguchi Y, Loppnau P, et al. Crystal structure of human spermine synthase: implications of substrate binding and catalytic mechanism. J Biol Chem. 2008;283(23):16135-46.
40. Schrodinger, LLC. The PyMOL Molecular Graphics System, Version 1.5.0.5, 2010.
41. Piton A, Gauthier J, Hamdan FF, Lafreniere RG, Yang Y, Henrion E, et al. Systematic resequencing of X-chromosome synaptic genes in autism spectrum disorder and schizophrenia. Mol Psychiatry. 2011;16(8):867-80.
42. Lee HW, Choi J, Shin H, Kim K, Yang J, Na M, et al. Preso, a novel PSD-95-interacting FERM and PDZ domain protein that regulates dendritic spine morphogenesis. J Neurosci Off J Soc Neurosci. 2008;28(53):14546-56.
43. Nagao M, Feinstein TN, Ezura Y, Hayata T, Notomi T, Saita Y, et al. Sympathetic control of bone mass regulated by osteopontin. Proc Natl Acad Sci U S A. 2011;108(43):17767-72.
44. Kajimura D, Hinoi E, Ferron M, Kode A, Riley KJ, Zhou B, et al. Genetic determination of the cellular basis of the sympathetic regulation of bone mass accrual. J Exp Med. 2011;208(4):841-51.
45. Takeda S, Karsenty G. Molecular bases of the sympathetic regulation of bone mass. Bone. 2008;42(5):837-40.
46. Takeda S, Elefteriou F, Levasseur R, Liu X, Zhao L, Parker KL, et al. Leptin regulates bone formation via the sympathetic nervous system. Cell. 2002;111(3):305-17.
47. Elefteriou F, Ahn JD, Takeda S, Starbuck M, Yang X, Liu X, et al. Leptin regulation of bone resorption by the sympathetic nervous system and CART. Nature. 2005;434(7032):514-20.
48. Kondo H, Nifuji A, Takeda S, Ezura Y, Rittling SR, Denhardt DT, et al. Unloading induces osteoblastic cell suppression and osteoclastic cell activation to lead to bone loss via sympathetic nervous system. J Biol Chem. 2005;280(34):30192-200.
49. Fu L, Patel MS, Bradley A, Wagner EF, Karsenty G. The molecular clock mediates leptin-regulated bone formation. Cell. 2005;122(5):803-15.
50. Jackson L, Jones DR, Scotting P, Sottile V. Adult mesenchymal stem cells: differentiation potential and therapeutic applications. J Postgrad Med. 2007;53(2):121-7.
51. Sottile V, Halleux C, Bassilana F, Keller H, Seuwen K. Stem cell characteristics of human trabecular bone-derived cells. Bone. 2002;30(5):699-704.
52. Ikeguchi Y, Bewley MC, Pegg AE. Aminopropyltransferases: function, structure and genetics. J Biochem. 2006;139(1):1-9.
53. Williams-Ashman HG, Seidenfeld J, Galletti P. Trends in the biochemical pharmacology of 5'-deoxy-5'-methylthioadenosine. Biochem Pharmacol. 1982;31(3):277-88.
54. Raina A, Tuomi K, Pajula RL. Inhibition of the synthesis of polyamines and macromolecules by 5'-methylthioadenosine and 5'-alkylthiotubercidins in BHK21 cells. Biochem J. 1982;204(3):697-703.
55. Dupree K, Dobs A. Osteopenia and male hypogonadism. Rev Urol. 2004;6 Suppl 6:S30-4.
56. Ross AC. The 2011 report on dietary reference intakes for calcium and vitamin D. Public Health Nutr. 2011;14(5):938-9.
57. Lee RH, Lyles KW, Colon-Emeric C. A review of the effect of anticonvulsant medications on bone mineral density and fracture risk. Am J Geriatr Pharmacother. 2010;8(1):34-46.