Non-myeloablative preconditioning with ACK2 (anti-c-kit antibody) is efficient in bone marrow transplantation for murine models of mucopolysaccharidosis type II

Molecular Genetics and Metabolism

Volumn 119, Issue 3, 2016, Pages 232-238

  Yokoi, Takayuki ^a   Yokoi, Kentarou ^a   Akiyama, Kazumasa ^a,b   Higuchi, Takashi ^a   Shimada, Yohta ^a   Kobayashi, Hiroshi ^a   Sato, Taku ^c   Ohteki, Toshiaki ^c   Otsu, Makoto ^d   Nakauchi, Hiromitsu ^d,e   Ida, Hiroyuki ^a   Ohashi, Toya ^a  

^a JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b KITASATO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

^e STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

ACK2; Hematopoietic cell transplantation; Mucopolysaccharidosis type II; Non myeloablative preconditioning

Indexed keywords

STEM CELL FACTOR; ANTIIDIOTYPIC ANTIBODY; DERMATAN SULFATE; GLYCOPROTEIN; HEPARAN SULFATE; IDS PROTEIN, HUMAN; STEM CELL FACTOR RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD; BONE MARROW TRANSPLANTATION; CHIMERA; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; FLOW CYTOMETRY; HEART; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUNTER SYNDROME; INTESTINE; IRRADIATION; LIVER; MALE; MOUSE; NONHUMAN; NONMYELOABLATIVE CONDITIONING; PRIORITY JOURNAL; SPLEEN; ANIMAL; ANTAGONISTS AND INHIBITORS; DISEASE MODEL; ENZYMOLOGY; GENETICS; HUMAN; IMMUNOLOGY; KNOCKOUT MOUSE; LYSOSOME; METABOLISM; PATHOLOGY;

ANIMALS; ANTIBODIES, ANTI-IDIOTYPIC; BONE MARROW TRANSPLANTATION; DERMATAN SULFATE; DISEASE MODELS, ANIMAL; GLYCOPROTEINS; HEPARITIN SULFATE; HUMANS; LYSOSOMES; MICE; MICE, KNOCKOUT; MUCOPOLYSACCHARIDOSIS II; PROTO-ONCOGENE PROTEINS C-KIT;

EID: 84992550301     PISSN: 10967192     EISSN: 10967206     Source Type: Journal    
DOI: 10.1016/j.ymgme.2016.08.003     Document Type: Article

References (43)

1. [1] Bach, G., Eisenberg, F. Jr., Cantz, M., Neufeld, E.F., The defect in the Hunter syndrome: deficiency of sulfoiduronate sulfatase. Proc. Natl. Acad. Sci. U. S. A. 70 (1973), 2134–2138.
2. [2] Martin, R., Beck, M., Eng, C., Giugliani, R., Harmatz, P., Munoz, V., Muenzer, J., Recognition and diagnosis of mucopolysaccharidosis II (Hunter syndrome). Pediatrics 121 (2008), e377–e386.
3. [3] Muenzer, J., Wraith, J.E., Beck, M., Giugliani, R., Harmatz, P., Eng, C.M., et al. A phase II/III clinical study of enzyme replacement therapy with idursulfase in mucopolysaccharidosis II (Hunter syndrome). Genet. Med. 8 (2006), 465–473.
4. [4] Okuyama, T., Tanaka, A., Suzuki, Y., Ida, H., Tanaka, T., Cox, G.F., et al. Japan elaprase treatment (JET) study: idursulfase enzyme replacement therapy in adult patients with attenuated Hunter syndrome (Mucopolysaccharidosis II, MPS II). Mol. Genet. Metab 99 (2010), 18–25.
5. [5] Muenzer, J., Beck, M., Eng, C.M., Giugliani, R., Harmatz, P., Martin, R., et al. Long-term, open-labeled extension study of idursulfase in the treatment of Hunter syndrome. Genet. Med 13 (2011), 95–101.
6. [6] Wraith, J.E., Scarpa, M., Beck, M., Bodamer, O.A., DeMeirleir, L., Guffon, N., et al. Mucopolysaccharidosis type II (Hunter syndrome): a clinical review and recommendations for treatment in the era of enzyme replacement therapy. Eur. J. Pediatr. 167 (2008), 267–277.
7. [7] Al Sawaf, S., Mayatepek, E., Hoffmann, B., Neurological findings in Hunter disease: pathology and possible therapeutic effects reviewed. J. Inherit. Metab. Dis. 31 (2008), 473–480.
8. [8] Ohashi, T., Iizuka, S., Ida, H., Eto, Y., Reduced alpha-Gal A enzyme activity in Fabry fibroblast cells and Fabry mice tissues induced by serum from antibody positive patients with Fabry disease. Mol. Genet. Metab. 94 (2008), 313–318.
9. [9] Ohashi, T., Sakuma, M., Kitagawa, T., Suzuki, K., Ishige, N., Eto, Y., Influence of antibody formation on reduction of globotriaosylceramide (GL-3) in urine from Fabry patients during agalsidase beta therapy. Mol. Genet. Metab. 92 (2007), 271–273.
10. [10] Linthorst, G.E., Hollak, C.E., Donker-Koopman, W.E., Strijland, A., Aerts, J.M., Enzyme therapy for Fabry disease: neutralizing antibodies toward agalsidase alpha and beta. Kidney Int. 66 (2004), 1589–1595.
11. [11] Schiffmann, R., Ries, M., Timmons, M., Flaherty, J.T., Brady, R.O., Long-term therapy with agalsidase alfa for Fabry disease: safety and effects on renal function in a home infusion setting. Nephrol. Dial. Transplant. 21 (2006), 345–354.
12. [12] Krivit, W., Aubourg, P., Shapiro, E., Bone marrow transplantation as effective treatment of central nervous system disease in globoid cell leukodystrophy, metachromatic leukodystrophy, adrenoleukodystrophy, mannosidosis, fucosidosis, aspartylglucosaminuria, Hurler, Maroteaux-Lamy, and Sly syndromes, and Gaucher disease type III. Curr. Opin. Neurol. 12 (1999), 167–176.
13. [13] Ohshima, T., Schiffmann, R., Murray, G.J., Quirk, J.M., Stahl, S., et al. Aging accentuates and bone marrow transplantation ameliorates metabolic defects in Fabry disease mice. Proc. Natl. Acad. Sci. U. S. A. 96 (1999), 6423–6427.
14. [14] Takenaka, T., Murray, G.J., Qin, G., Quirk, J.M., Ohshima, T., Qasba, P., et al. Long-term enzyme correction and lipid reduction in multiple organs of primary and secondary transplanted Fabry mice receiving transduced bonemarrow cells. Proc. Natl. Acad. Sci. U. S. A. 97 (2000), 7515–7520.
15. [15] Shapiro, E.G., Lockman, L.A., Balthazor, M., Krivit, W., Neuropsychological outcomes of several storage diseases with and without bone marrow transplantation. J. Inherit. Metab. Dis. 18 (1995), 413–429.
16. [16] McKinnis, E.J., Sulzbacher, S., Rutledge, J.C., Sanders, J., Scott, C.R., Bone marrow transplantation in Hunter syndrome. J. Pediatr. 129 (1996), 145–148.
17. [17] Vellodi, A., Young, E., Cooper, A., Lidchi, V., Winchester, B., Wraith, J.E., et al. Long-term follow-up following bone marrow transplantation for Hunter disease. J. Inherit. Metab. Dis. 22 (1999), 638–648.
18. [18] Guffon, N., Bertrand, Y., Forest, I., Fouilhoux, A., Froissart, R., Bone marrow transplantation in children with Hunter syndrome: outcome after 7 to 17 years. J. Pediatr. 154 (2009), 733–737.
19. [19] Akiyama, K., Shimada, Y., Higuchi, T., Ohtsu, M., Nakauchi, H., Kobayashi, H., et al. Enzyme augmentation therapy enhances the therapeutic efficacy of bone marrow transplantation in mucopolysaccharidosis type II mice. Mol. Genet. Metab. 111 (2014), 139–146.
20. [20] Tanaka, A., Okuyama, T., Suzuki, Y., Sakai, N., Takakura, H., Sawada, T., et al. Long-term efficacy of hematopoietic stem cell transplantation on brain involvement in patients with mucopolysaccharidosis type II: a nationwide survey in Japan. Mol. Genet. Metab. 107 (2012), 513–520.
21. [21] Wakabayashi, T., Shimada, Y., Akiyama, K., Higuchi, T., Fukuda, T., Kobayashi, H., et al. Hematopoietic stem cell gene therapy corrects neuropathic phenotype in murine model of mucopolysaccharidosis type II. Hum. Gene Ther. 26 (2015), 357–366.
22. [22] Chen, J., Larochelle, A., Fricker, S., Bridger, G., Dunbar, C.E., Abkowitz, J.L., Mobilization as a preparative regimen for hematopoietic stem cell transplantation. Blood 107 (2006), 3764–3771.
23. [23] Yoshihara, H., Arai, F., Hosokawa, K., Hagiwara, T., Takubo, K., Nakamura, Y., et al. Thrombopoietin/MPL signaling regulates hematopoietic stem cell quiescence and interaction with the osteoblastic niche. Cell Stem Cell 13 (2007), 685–697.
24. [24] Sato, T., Onai, N., Yoshihara, H., Arai, F., Suda, T., Ohteki, T., Interferon regulatory factor-2 protects quiescent hematopoietic stem cells from type I interferon-dependent exhaustion. Nat. Med. 15 (2009), 696–700.
25. [25] Sato, T., Ikeda, M., Yotsumoto, S., Shimada, Y., Higuchi, T., Kobayashi, H., et al. Novel interferon-based pre-transplantation conditioning in the treatment of a congenital metabolic disorder. Blood 121 (2013), 3267–3273.
26. [26] Ogawa, M., Matsuzaki, Y., Nishikawa, S., Hayashi, S., Kunisada, T., Sudo, T., et al. Expression and function of c-kit in hemopoietic progenitor cells. J. Exp. Med. 174 (1991), 63–71.
27. [27] Czechowicz, A., Kraft, D., Weissman, I.L., Bhattacharya, D., Efficient transplantation via antibody-based clearance of hematopoietic stem cell niches. Science 318 (2007), 1296–1299.
28. [28] Xue, X., Pech, N.K., Shelley, W.C., Srour, E.F., Yoder, M.C., Dinauer, M.C., Antibody targeting KIT as pretransplantation conditioning in immunocompetent mice. Blood 116 (2010), 5419–5422.
29. [29] Garcia, A.R., Pan, J., Lamsa, J.C., Muenzer, J., The characterization of a murine model of mucopolysaccharidosis II (Hunter syndrome). J. Inherit. Metab. Dis. 30 (2007), 924–934.
30. [30] Garcia, A.R., DaCosta, J.M., Pan, J., Muenzer, J., Lamsa, J.C., Preclinical dose ranging studies for enzyme replacement therapy with idursulfase in a knock-out mouse model of MPS II. Mol. Genet. Metab. 91 (2007), 183–190.
31. [31] Faraci, M., Lanino, E., Dini, G., Fondelli, M.P., Morreale, G., Dallorso, S., et al. Severe neurologic complications after hematopoietic stem cell transplantation in children. Neurology 59 (2002), 1895–1904.
32. [32] Suzuki, Y., Isogaki, K., Teramoto, T., Tashita, H., Shimozawa, N., Nishimura, M., et al. Bone marrow transplantation for the treatment of X-linked adrenoleuko-dystrophy. J. Inherit. Metab. Dis. 23 (2000), 453–458.
33. [33] AL, E., GD, A., JS, B., JS, M.C., Optimal prevention of seizures induced by high-dose busulfan. Pharmacotherapy 28 (2008), 1502–1510.
34. [34] Caselli, D., Rosati, A., Faraci, M., Podda, M., Ripaldi, M., Longoni, D., et al. Risk of seizures in children receiving busulphan-containing regimens for stem cell transplantation. Biol. Blood Marrow Transplant. 20 (2014), 282–285.
35. [35] Kato, S., Yabe, H., Takakura, H., Mugishima, H., Ishige, M., Tanaka, A., et al. Hematopoietic stem cell transplantation for inborn errors of metabolism: a report from the research committee on transplantation for inborn errors of metabolism of the Japanese ministry of health, labour and welfare and the working group of the Japan society for hematopoietic cell transplantation. Pediatr. Transplant. 20 (2016 Mar), 203–214.
36. [36] Galbiati, F., Clementi, G., Superchi, D., Givogri, M.I., Bongarzone, E.R., Effects of irradiation on the postnatal development of the brain in a genetic mouse model of globoid cell leukodystrophy. Neurochem. Res. 32 (2007), 377–388.
37. [37] Ohira, T., Ando, R., Okada, Y., Suzuki, H., Saito, T., Nakazawa, T., et al. Sequence of busulfan-induced neural progenitor cell damage in the fetal rat brain. Exp. Toxicol. Pathol. 65 (2013), 523–530.
38. [38] Yokoi, K., Akiyama, K., Kaneshiro, E., Higuchi, T., Shimada, Y., Kobayashi, H., et al. Effect of donor chimerism to reduce the level of glycosaminoglycans following bone marrow transplantation in a murine model of mucopolysaccharidosis type II. J. Inherit. Metab. Dis. 38 (2015), 333–340.
39. [39] Enquist, I.B., Nilsson, E., Månsson, J.E., Ehinger, M., Richter, J., Karlsson, S., Successful low-risk hematopoietic cell therapy in a mouse model of type 1 Gaucher disease. Stem Cells 3 (2009 Mar), 744–752.
40. [40] Soper, B.W., Lessard, M.D., Vogler, C.A., Levy, B., Beamer, W.G., Sly, W.S., et al. Nonablative neonatal marrow transplantation attenuates functional and physical defects of beta-glucuronidase deficiency. Blood 97 (2001), 1498–1504.
41. [41] Yokoi, T., Kobayashi, H., Shimada, Y., Eto, Y., Ishige, N., Kitagawa, T., et al. Minimum requirement of donor cells to reduce the glycolipid storage following bone marrow transplantation in a murine model of Fabry disease. J. Gene Med. 13 (2011), 262–268.
42. [42] Cartier, N., Hacein-Bey-Abina, S., Bartholomae, C.C., Veres, G., Schmidt, M., Kutschera, I., et al. Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science 326 (2009), 818–823.
43. [43] Chhabra, A., Ring, A.M., Weiskopf, K., Schnorr, P.J., Gordon, S., Le, A.C., et al. Hematopoietic stem cell transplantation in immunocompetent hosts without radiation or chemotherapy. Sci. Transl. Med., 351, 2016, 351ra105.