Hypophosphatasia: Enzyme Replacement Therapy Brings New Opportunities and New Challenges

Journal of Bone and Mineral Research

Volumn 32, Issue 4, 2017, Pages 667-675

  Whyte, Michael P ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

ALKALINE PHOSPHATASE; CALCIFICATION; CHONDROCALCINOSIS; HYDROXYAPATITE; HYPERCALCEMIA; INBORN ERROR OF METABOLISM; INORGANIC PYROPHOSPHATE; MATRIX VESICLE; MINERALIZATION; OSTEOMALACIA; RICKETS; VITAMIN B6

Indexed keywords

ASFOTASE ALFA; PYRIDOXINE; PYROPHOSPHATE; ALKALINE PHOSPHATASE; ALPL PROTEIN, HUMAN; HYBRID PROTEIN; IMMUNOGLOBULIN G; PYRIDOXAL 5 PHOSPHATE;

ARTHROPATHY; ARTICLE; CHILD; ENZYME REPLACEMENT; HUMAN; HYPOPHOSPHATASIA; OSTEOMALACIA; PATHOGENESIS; PERIODONTAL DISEASE; PROGNOSIS; RICKETS; ANIMAL; BONE DEVELOPMENT; DRUG EFFECTS; FEMALE; GENETICS; INFANT; MALE; METABOLISM; MUTATION; PRESCHOOL CHILD;

ALKALINE PHOSPHATASE; ANIMALS; CHILD; CHILD, PRESCHOOL; ENZYME REPLACEMENT THERAPY; FEMALE; HUMANS; HYPOPHOSPHATASIA; IMMUNOGLOBULIN G; INFANT; MALE; MUTATION; OSTEOGENESIS; PYRIDOXAL PHOSPHATE; RECOMBINANT FUSION PROTEINS;

EID: 85011407669     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.3075     Document Type: Article

References (71)

1. Rosen CJ. Primer on the metabolic bone diseases and disorders of mineral metabolism. 8th ed. American Society for Bone and Mineral Research. Ames, IA: Wiley-Blackwell; 2013.
2. Rathbun JC. Hypophosphatasia: a new developmental anomaly. Am J Dis Child. 1948; 75:822–31.
3. Whyte MP. Hypophosphatasia: aetiology, nosology, pathogenesis, diagnosis and treatment. Nat Rev Endocrinol. 2016; 12:233–46.
4. Whyte MP. Hypophosphatasia. In: Genetics of bone biology and skeletal disease. 1st ed. Thakker RV, Whyte MP, Eisman J, Igarashi T, editors. San Diego, CA: Academic Press; 2013. p. 337–60.
5. Whyte MP, Greenberg CR, Salman NJ, et al. Enzyme replacement therapy in life-threatening hypophosphatasia. N Engl J Med. 2012; 366:904–13.
6. Whyte MP, Madson KL, Phillips D, et al. Asfotase alfa therapy for children with hypophosphatasia. JCI Insight. 2016; 1:e85971:1–10.
7. Whyte MP, Rockman-Greenberg C, Ozono K, et al. Asfotase alfa treatment improves survival for perinatal and infantile hypophosphatasia. J Clin Endocrinol Metab. 2016; 101:334–42.
8. Millan JL, Whyte MP. Alkaline phosphatase and hypophosphatasia. Calcif Tissue Int. 2016; 98(4):398–416.
9. Russell RG. Excretion of inorganic pyrophosphate in hypophosphatasia. Lancet. 1965; 10:461–4.
10. Fleisch H, Russell RG, Straumann F. Effect of pyrophosphate on hydroxyapatite and its implications in calcium homeostasis. Nature. 1966; 212:901–3.
11. Anderson HC, Hsu HH, Morris DC, Fedde KN, Whyte MP. Matrix vesicles in osteomalacic hypophosphatasia bone contain apatite-like mineral crystals. Am J Pathol. 1997; 151:1555–61.
12. Baumgartner-Sigl SB, Haberlandt E, Mumm S, et al. Pyridoxine-responsive seizures as the first symptom of infantile hypophosphatasia caused by two novel missense mutations (c.677T>C, p.M226T; c.1112C>T, p.T371I) of the tissue-nonspecific alkaline phosphatase gene. Bone. 2007; 40:1655–61.
13. Guanabens N, Mumm S, Möller I, et al. Calcific periarthritis as the only clinical manifestation of hypophosphatasia in middle-aged sisters. J Bone Miner Res. 2014; 29:929–34.
14. Whyte MP, Zhang F, Wenkert D, et al. Hypophosphatasia: validation and expansion of the clinical nosology for children from 25 years experience with 173 pediatric patients. Bone. 2015; 75:229–39.
15. Mornet E. Tissue nonspecific alkaline phosphatase gene mutations database [Internet]. 2015. Available at: http://www.sesep.uvsq.fr/03_hypo_mutations.php.
16. Fraser D. Hypophosphatasia. Am J Med. 1957; 22:730–46.
17. Mornet E, Yvard A, Taillandier A, Fauvert D, Simon-Bouy B. A molecular-based estimation of the prevalence of hypophosphatasia in the European population. Ann Hum Genet. 2011; 75:439–45.
18. 317→Asp mutation in ALPL causes the perinatal (lethal) form of hypophosphatasia in Canadian mennonites. Genomics. 1993; 17:215–7.
19. Ozono K, Michigami T. Hypophosphatasia now draws more attention of both clinicians and researchers: a commentary on prevelance of c. 1559delT in ALPL, a common mutation resulting in the perinatal (lethal) form of hypophosphatasias in Japanese and effects of the mutation on heterozygous carriers. J Hum Genet. 2011; 56:174–5.
20. Whyte MP, Essmyer K, Geimer M, Mumm S. Homozygosity for TNSALP mutation 1348C>T (Arg 433Cys) causes infantile hypophosphatasia manifesting transient disease correction and variably lethal outcome in a kindred of black ancestry. J Pediatr. 2006; 148:753–8.
21. Mumm S, Wenkert D, Zhang X, Geimer M, Zerega J, Whyte MP. Hypophosphatasia: the c.1133A>T, p.D378V transversion is the most common American TNSALP mutation [abstract]. J Bone Miner Res. 2006; 21:S115.
22. Wenkert D, McAlister WH, Mumm S, Whyte MP. c.1250A>G, p.N417S is a common American TNSALP mutation involved in all clinical forms of hypophosphatasia (HPP), including pseudo-HPP [Internet]. Available at: http://www.abstractsonline.com/viewer/?mkey={DCB70C83-5B38-431A-B0E1-9221D66718D0}.
23. Wenkert D, McAlister WH, Coburn SP, et al. Hypophosphatasia: non-lethal disease despite skeletal presentation in utero (17 new cases and literature review). J Bone Miner Res. 2011; 26:2389–98.
24. Whyte MP, Zhang F, Wenkert D, et al. Hypophosphatasia: validation and expansion of the clinical nosology for children from 25 years experience with 173 pediatric patients. Bone. 2015; 75:229–39.
25. Whyte MP, Wenkert D, Zhang F. Hypophosphatasia: natural history study of 101 affected children studied at a single research center. Bone. 2016; 93:125–38.
26. Whyte MP, Teitelbaum SL, Murphy WA, Bergfeld MA, Avioli LV. Adult hypophosphatasia. Clinical, laboratory, and genetic investigation of a large kindred with review of the literature. Medicine (Baltimore). 1979; 58:329–47.
27. Khandwala HM, Mumm S, Whyte MP. Low serum alkaline phosphatase activity and pathologic fracture: case report and brief review of hypophosphatasia diagnosed in adulthood. Endocr Pract. 2006; 12:676–81.
28. Sutton RA, Mumm S, Coburn SP, Ericson KL, Whyte MP. “ Atypical femoral fractures” during bisphosphonate exposure in adult hypophosphatasia. J Bone Miner Res. 2012; 27:987–94.
29. Coe JD, Murphy WA, Whyte MP. Management of femoral fractures and pseudofractures in adult hypophosphatasia. J Bone Joint Surg (Am). 1986; 68:981–90.
30. Whyte MP. Atypical femoral fractures, bisphosphonates, and adult hypophosphatasia. J Bone Miner Res. 2009; 24:1132–4.
31. Chuck AJ, Pattrick MG, Hamilton E, Wilson R, Doherty M. Crystal deposition in hypophosphatasia: a reappraisal. Ann Rheum Dis. 1989; 48:571–6.
32. Whyte MP, Murphy WA, Fallon MD. Adult hypophosphatasia with chondrocalcinosis and arthropathy. Variable penetrance of hypophosphatasemia in a large Oklahoma kindred. Am J Med. 1982; 72:631–41.
33. Weinstein RS, Whyte MP. Fifty-year follow-up of hypophosphatasia. Arch Int Med. 1981; 141:1720–1.
34. Seshia SS, Derbyshire G, Haworth JC, Hoogstraten J. Myopathy with hypophosphatasia. Arch Dis Child. 1990; 65:130–1.
35. Whyte MP, Valdes R Jr, Ryan LM, McAlister WH. Infantile hypophosphatasia: enzyme replacement therapy by intravenous infusion of alkaline phosphatase-rich plasma from patients with Paget bone disease. J Pediatr. 1982; 101:379–86.
36. Leung ECW, Mhanni AA, Reed M, Whyte MP, Landy H, Greenberg CR. Outcome of perinatal hypophosphatasia in Manitoba Mennonites: a retrospective cohort analysis. JIMD Rep. 2013; 11:73–8.
37. Taillard F, Desbois JC, Delepine N, Gretillat F, Allaneau C, Herrault A. L'hypophosphatasie affection polymorphe de fréquence peut-ětre sous estimée [French]. La Médecine Infantile. 1984; 91:559–76.
38. Silver MM, Vilos GA, Milne KJ. Pulmonary hypoplasia in neonatal hypophosphatasia. Pediatr Pathol. 1988; 8:483–93.
39. McCance RA, Morrison AB, Dent CE. The excretion of phosphoethanolamine and hypophosphatasia. Lancet. 1955; 268:131.
40. 6 metabolism. J Clin Invest. 1985; 76:752–6.
41. Whyte MP, Seino Y. Circulating vitamin D metabolite levels in hypophosphatasia. J Clin Endocrinol Metab. 1982; 55:178–80.
42. Xu Y, Cruz TF, Pritzker KP. Alkaline phosphatase dissolves calcium pyrophosphate dihydrate crystals. J Rheumatol. 1991; 18:1606–10.
43. Caswell AM, Whyte MP, Russell RG. Hypophosphatasia and the extracellular metabolism of inorganic pyrophosphate: clinical and laboratory aspects. Crit Rev Clin Lab Sci. 1991; 28:175–232.
44. Whyte MP, Mumm S, Deal C. Adult hypophosphatasia treated with teriparatide. J Clin Endocrinol Metab. 2007; 92:1203–8.
45. Whyte MP, Rettinger SD. Hyperphosphatemia due to enhanced renal reclamation of phosphate in hypophosphatasia [abstract]. J Bone Miner Res. 1987; 2 (Suppl 1):399.
46. Otero JE, Gottesman GS, McAlister WH, et al. Severe skeletal toxicity from protracted etidronate therapy for generalized arterial calcification of infancy. J Bone Miner Res. 2013; 28:419–30.
47. Rutsch F, Böyer P, Nitschke Y, et al. Hypophosphatemia, hyperphosphaturia, and bisphosphonate treatment are associated with survival beyond infancy in generalized arterial calcification of infancy. Circ Cardiovasc Genet. 2008; 1:133–40.
48. Whyte MP, McAlister WH, Patton LS, et al. Enzyme replacement therapy for infantile hypophosphatasia attempted by intravenous infusions of alkaline phosphatase-rich Paget plasma: results in three additional patients. J Pediatr. 1984; 105:926–33.
49. Fallon MD, Weinstein RS, Goldfischer S, Brown DS, Whyte MP. Hypophosphatasia: clinicopathologic comparison of the infantile, childhood, and adult forms. Medicine (Baltimore). 1984; 63:12–24.
50. McKiernan FE, Berg RL, Fuehrer J. Clinical and radiographic findings in adults with persistent hypophosphatasemia. J Bone Miner Res. 2014; 29:1651–60.
51. Royce PM, Blumberg A, Zurbrügg RP, Zimmermann A, Colombo JP, Steinmann B. Lethal osteogenesis imperfecta: abnormal collagen metabolism and biochemical characteristics of hypophosphatasia. Eur J Ped. 1988; 147:626–31.
52. El-Gharbawy AH, Peeden JN Jr, Lachman RS, Graham JM Jr, Moore SR, Rimoin DL. Severe cleidocranial dysplasia and hypophosphatasia in a child with microdeletion of the C-terminal region of RUNX2. Am J Med Genet A. 2010; 152A:169–74.
53. Chodirker BN, Coburn SP, Seargeant LE, Whyte MP, Greenberg CR. Increased plasma pyridoxal-5′-phosphate levels before and after pyridoxine loading in carriers of perinatal/infantile hypophosphatasia. J Inherit Metab Dis. 1990; 13:891–6.
54. Rasmussen K. Phosphorylethanolamine and hypophosphatasia. Dan Med Bulletin. 1968; 15:1–112.
55. Licata AA, Radfar N, Bartter FC, Bou E. The urinary excretion of phosphoethanolamine in diseases other than hypophosphatasia. Am J Med. 1978; 64:133–8.
56. Whyte MP, Wenkert D, McAlister WH, et al. Chronic recurrent multifocal osteomyelitis mimicked in childhood hypophosphatasia. J Bone Miner Res. 2009; 24:1493–505.
57. Zhang F, Whyte MP, Wenkert D. Improving dual-energy X-ray absorptiometry (DXA) interpretation: a simple equation for height correction for pre-teenage children. J Clin Densitom. 2012; 15:267–74.
58. Watanabe A, Satoh S, Fujita A, Naing BT, Orimo H, Shimada T. Perinatal hypophosphatasia caused by uniparental isodisomy. Bone. 2014; 60:93–7.
59. Henthorn PS, Whyte MP. Infantile hypophosphatasia: successful prenatal assessment by testing for tissue-non-specific alkaline phosphatase isoenzyme gene mutations. Prenat Diagn. 1995; 15:1001–6.
60. Rodriguez E, Bober MB, Davey L, et al. Respiratory mechanics in an infant with perinatal lethal hypophosphatasia treated with human recombinant enzyme replacement therapy. Pediatr Pulmonol. 2012; 47:917–22.
61. Phillips D, Case LE, Griffin D, et al. Physical therapy management of infants and children with hypophosphatasia. Mol Genet Metab. 2016; 119:14–9.
62. Whyte MP, Habib D, Coburn SP, et al. Failure of hyperphosphatasemia by intravenous infusion of purified placental alkaline phosphatase (ALP) to correct severe hypophosphatasia: evidence against a role for circulating ALP in skeletal mineralization [abstract]. J Bone Miner Res. 1992; 7:S155.
63. Whyte MP, Kurtzburg J, McAlister WH, et al. Marrow cell transplantation for infantile hypophosphatasia. J Bone Miner Res. 2003; 18:624–36.
64. Cahill RA, Wenkert D, Perlman SA, et al. Infantile hypophosphatasia: trial of transplantation therapy using bone fragments and cultured osteoblasts. J Clin Endocrinol Metab. 2007; 92:2923–30.
65. Camacho PM, Mazhari AM, Wilczynski C, Kadanoff R, Mumm S, Whyte MP. Adult hypophosphatasia treated with teriparatide: report of two patients and review of the literature. Endocr Pract. 2016; 22:941–50.
66. Millán JL, Narisawa S, Lemire I, et al. Enzyme replacement therapy for murine hypophosphatasia. J Bone Miner Res. 2008; 23:777–87.
67. Fedde KN, Blair L, Silverstein J, et al. Alkaline phosphatase knock-out mice recapitulate the metabolic and skeletal defects of infantile hypophosphatasia. J Bone Miner Res. 1999; 14:2015–26.
68. Liese J, Hofmann C, Harmatz P, et al. Efficacy and safety of asfotase alfa in patients with infantile hypophosphatasia treated for up to 3.5 years: results from a phase II, open-label, uncontrolled study [Abstract]. Proceedings of the 98th Annual Endocrine Society Meeting; Boston, MA; April 1–4, 2016.
69. Kishnani PS, Rockman-Greenberg C, Madson KL, Gayron M, Iloeje U, Whyte MP. Ambulatory performance in adolescents and adults with hypophosphatasia treated wtih Asfotase alfa: data from a phase II, randomized, dose-ranging open-label, multi-center study [Abstract]. J Bone Miner Res. 2016;Suppl 1:S108.
70. Okazaki Y, Kitajima H, Mochizuki N, Kitaoka T, Michigami T, Ozono K. Lethal hypophosphatasia successfully treated with enzyme replacement from day 1 after birth. Eur J Pediatr. 2016; 175:433–7.
71. Sheen CR, Kuss P, Narisawa S, et al. Pathophysiological role of vascular smooth muscle alkaline phosphatase in medial artery calcification. J Bone Miner Res. 2015; 30:824–36.