Attenuation of murine lysosomal storage disease by allogeneic neonatal bone marrow transplantation using costimulatory blockade and donor lymphocyte infusion without myeloablation

Clinical Immunology

Volumn 119, Issue 2, 2006, Pages 166-179

  Lessard, Mark D ^a   Alley, Travis L ^a   Proctor, Jennifer L ^a   Levy, Beth ^b   Galvin, Nancy ^b   Vogler, Carole A ^b   Soper, Brian W ^a  

^a JACKSON LABORATORY   (United States)

^b SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bone marrow transplantation; CD40L; Chronic GvHD; Costimulatory blockade; CTLA 4Ig; Donor lymphocyte infusion (DLI); Lysosomal storage disease; Mucopolysaccharidosis type VII (MPS VII); Neonate; Tolerance

Indexed keywords

ABATACEPT; BETA GLUCURONIDASE; CD40 LIGAND MONOCLONAL ANTIBODY;

ALLOGENIC BONE MARROW TRANSPLANTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CHRONIC GRAFT VERSUS HOST DISEASE; CONTROLLED STUDY; ENZYME ACTIVITY; IMMUNOLOGICAL TOLERANCE; LIFESPAN; LYMPHOCYTE; LYSOSOME; LYSOSOME STORAGE DISEASE; MAJOR HISTOCOMPATIBILITY COMPLEX; MICROCHIMERISM; MOUSE; MUCOPOLYSACCHARIDOSIS TYPE 7; MYELOABLATIVE CONDITIONING; NEWBORN; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; RECIPIENT; TREATMENT OUTCOME;

ANIMALS; BONE MARROW TRANSPLANTATION; CHIMERA; GRAFT VS HOST DISEASE; HEART DISEASES; IMMUNOHISTOCHEMISTRY; KIDNEY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE CULTURE TEST, MIXED; LYMPHOCYTE TRANSFUSION; LYSOSOMAL STORAGE DISEASES; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MYELOABLATIVE AGONISTS; TRANSPLANTATION, HOMOLOGOUS;

EID: 33645983624     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2005.12.015     Document Type: Article

References (72)

1. Starzl T.E. History of clinical transplantation. World J. Surg. 24 (2000) 759-782
2. Rao K., Amrolia P.J., Jones A., et al. Improved survival after unrelated donor bone marrow transplantation in children with primary immunodeficiency using a reduced-intensity conditioning regimen. Blood 105 (2005) 879-885
3. Tanphaichitr V.S., Suvatte V., Issaragrisil S., et al. Successful bone marrow transplantation in a child with red blood cell pyruvate kinase deficiency. Bone Marrow Transplant. 26 (2000) 689-690
4. Brodsky R.A., and Jones R.J. Aplastic anaemia. Lancet 365 (2005) 1647-1656
5. La Nasa G., Caocci G., and Argiolu F. Unrelated donor stem cell transplantation in adult patients with thalassemia. Bone Marrow Transplant 36 11 (2005) 971-975
6. Schulz A.S., Classen C.F., Mihatsch W.A., et al. HLA-haploidentical blood progenitor cell transplantation in osteopetrosis. Blood 99 (2002) 3458-3460
7. George B., Mathews V., Shaji R.V., et al. Fludarabine-based conditioning for allogeneic stem cell transplantation for multiply transfused patients with Fanconi's anemia. Bone Marrow Transplant. 35 (2005) 341-343
8. Grewal S.S., Krivit W., Defor T.E., et al. Outcome of second hematopoietic cell transplantation in Hurler syndrome. Bone Marrow Transplant. 29 (2002) 491-496
9. Hsu Y.S., Hwu W.L., Huang S.F., et al. Niemann-Pick disease type C (a cellular cholesterol lipidosis) treated by bone marrow transplantation. Bone Marrow Transplant. 24 (1999) 103-107
10. Krivit W., Peters C., and Shapiro E.G. 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
11. Koc O.N., Peters C., Aubourg P., et al. Bone marrow-derived mesenchymal stem cells remain host-derived despite successful hematopoietic engraftment after allogeneic transplantation in patients with lysosomal and peroxisomal storage diseases. Exp. Hematol. 27 (1999) 1675-1681
12. Birkenmeier E.H., Barker J.E., Vogler C.A., et al. Increased life span and correction of metabolic defects in murine mucopolysaccharidosis type VII after syngeneic bone marrow transplantation. Blood 78 (1991) 3081-3092
13. Sands M.S., Barker J.E., and Vogler C. Treatment of murine mucopolysaccharidosis type VII by syngeneic bone marrow transplantation in neonates. Lab. Invest. 68 (1993) 676-686
14. Soper B.W., Lessard M.D., Vogler C., et al. Nonablative neonatal marrow transplantation attenuates functional and physical defects of b-glucuronidase deficiency. Blood 97 (2001) 1498-1505
15. Birkenmeier E.H., Davisson M.T., Beamer W.G., et al. Murine mucopolysaccharidosis type VII. Characterization of a mouse with b-glucuronidase. J. Clin. Invest. 83 (1989) 1258-1266
16. Sands M.S., and Birkenmeier E.H. A single-base-pair deletion in the beta-glucuronidase gene accounts for the phenotype of murine mucopolysaccharidosis type VII. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 6567-6571
17. Sly W.S., Brot F.E., Glaser J., et al. Beta-glucuronidase deficiency mucopolysaccharidosis. Birth Defects Orig. Artic. Ser. 10 (1974) 239-245
18. Neufeld E.F., and Muenzer J. The mucopolysaccharidoses. In: Scriver C.R., Beaudet A.L., Sly W.S., and Valle D. (Eds). Metabolic Basis of Inherited Disease (1995), McGraw-Hill, New York 2465-2494
19. Bosi A., Bartolozzi B., and Guidi S. Allogeneic stem cell transplantation. Transplant. Proc. 37 (2005) 2667-2669
20. Billingham R.E., Brent L., and Medawar P.B. Actively acquired tolerance of foreign cells. Nature 172 (1953) 603-606
21. Soper B.W., Lessard M.D., Jude C.D., et al. Successful allogeneic neonatal bone marrow transplantation devoid of myeloablation requires costimulatory blockade. J. Immunol. 171 (2003) 3270-3277
22. Adkins B. T-cell function in newborn mice and humans [see comments]. Immunol. Today 20 (1999) 330-335
23. Larsen C.P., Alexander D.Z., Hollenbaugh D., et al. CD40-gp39 interactions play a critical role during allograft rejection. Suppression of allograft rejection by blockade of the CD40-gp39 pathway. Transplantation 61 (1996) 4-9
24. Dazzi F., Szydlo R.M., and Goldman J.M. Donor lymphocyte infusions for relapse of chronic myeloid leukemia after allogeneic stem cell transplant: where we now stand. Exp. Hematol. 27 (1999) 1477-1486
25. Yui M.A., Muralidharan K., Moreno-Altamirano B., et al. Production of congenic mouse strains carrying NOD-derived diabetogenic genetic intervals: an approach for the genetic dissection of complex traits. Mamm. Genome 7 (1996) 331-334
26. Sands M.S., and Barker J.E. Percutaneous intravenous injection in neonatal mice. Lab. Anim. Sci. 49 (1999) 328-330
27. Eicher E.M., and Washburn L.L. Assignment of genes to regions of mouse chromosomes. Proc. Natl. Acad. Sci. U. S. A. 75 (1978) 946-950 (issn: 0027-8424)
28. Eppig J.J., Kozak L.P., Eicher E.M., et al. Ovarian teratomas in mice are derived from oocyts that have completed the first meiotic division. Nature 269 (1977) 517-519
29. Soper B.W., Duffy T.M., Vogler C.A., et al. A genetically myeloablated MPS VII model detects the expansion and curative properties of as few as 100 enriched murine stem cells. Exp. Hematol. 27 (1999) 1691-1704
30. Wolfe J.H., and Sands M.S. Murine mucopolysaccharidosis type VII: a model system for somatic gene therapy of the central nervous system. In: Lowenstein P.R., and Enquist L.W. (Eds). Protocols for Gene Therapy in Neuroscience: Towards Gene Therapy of Neurological Disorders (1996), John Wiley and Sons Ltd., Chichester 263-274
31. Vogler C., Sands M.S., Levy B., et al. Enzyme replacement with recombinant beta-glucuronidase in murine mucopolysaccharidosis type VII: impact of therapy during the first six weeks of life on subsequent lysosomal storage, growth, and survival. Pediatr. Res. 39 (1996) 1050-1054
32. Levy S. Diagnostic approach to cardiac arrhythmias. J. Cardiovasc. Pharmacol. 17 Suppl. 6 (1991) S24-S31
33. Nave C., Nardi S., Gaudino M., et al. The electrophysiological bases of aberrant intraventricular conduction during atrial fibrillation. Cardiologia 41 (1996) 1193-1198
34. Krege J.H., Hodgin J.B., Hagaman J.R., et al. A noninvasive computerized tail-cuff system for measuring blood pressure in mice. Hypertension 25 (1995) 1111-1115
35. Dangel J.H. Cardiovascular changes in children with mucopolysaccharide storage diseases and related disorders-clinical and echocardiographic findings in 64 patients. Eur. J. Pediatr. 157 (1998) 534-538
36. Mohan U.R., Hay A.A., Cleary M.A., et al. Cardiovascular changes in children with mucopolysaccharide disorders. Acta Paediatr. 91 (2002) 799-804
37. Schuldt A.J., Hampton T.J., Chu V., et al. Electrocardiographic and other cardiac anomalies in beta-glucuronidase-null mice corrected by nonablative neonatal marrow transplantation. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 603-608
38. Wekerle T., Kurtz J., Ito H., et al. Allogeneic bone marrow transplantation with co-stimulatory blockade induces macrochimerism and tolerance without cytoreductive host treatment. Nat. Med. 6 (2000) 464-469
39. Daly T.M., Lorenz R.G., and Sands M.S. Abnormal immune function in vivo in a murine model of lysosomal storage disease. Pediatr. Res. 47 (2000) 757-762
40. Barker J.E., and McFarland E. The hematopoietic stem cells of alpha-thalassemic mice. Blood 66 (1985) 595-601
41. Barker J.E., and Compton S.T. Hematopoietic repopulation of adult mice with beta-thalassemia. Blood 83 (1994) 828-832
42. Piomelli S., Lerner N., Cohen A., et al. Bone marrow transplantation for thalassemia. N. Engl. J. Med. 317 (1987) 964
43. Silber G.M., Winkelstein J.A., Moen R.C., et al. Reconstitution of T- and B-cell function after T-lymphocyte-depleted haploidentical bone marrow transplantation in severe combined immunodeficiency due to adenosine deaminase deficiency. Clin. Immunol. Immunopathol. 44 (1987) 317-320
44. Fehr T., and Sykes M. Tolerance induction in clinical transplantation. Transpl. Immunol. 13 (2004) 117-130
45. Dey B., Sykes M., and Spitzer T.R. Outcomes of recipients of both bone marrow and solid organ transplants. A review. Medicine (Baltimore) 77 (1998) 355-369
46. Sands M.S., Vogler C., Torrey A., et al. Murine mucopolysaccharidosis type VII: long term therapeutic effects of enzyme replacement and enzyme replacement followed by bone marrow transplantation. J. Clin. Invest. 99 (1997) 1596-1605
47. Vogler C., Levy B., Galvin N., et al. Early onset of lysosomal storage disease in a murine model of mucopolysacharidosis type VII: undegraded substrate accumulates in many tissues in the fetus and very young MPS VII mouse. Pediatr. Dev. Pathol. 8 4 (2005) 453-462
48. Hiesse C., Goldschmidt E., Santelli G., et al. Membranous nephropathy in a bone marrow transplant recipient. Am. J. Kidney Dis. 11 (1988) 188-191
49. Barbara J.A., Thomas A.C., Smith P.S., et al. Membranous nephropathy with graft-versus-host disease in a bone marrow transplant recipient. Clin. Nephrol. 37 (1992) 115-118
50. Sato N., Kishi K., Yagisawa K., et al. Nephrotic syndrome in a bone marrow transplant recipient with chronic graft-versus-host disease. Bone Marrow Transplant. 16 (1995) 303-305
51. Yu J., Cui R., and Tong S. Membranous nephropathy after allogeneic peripheral blood hematopoietic stem cell transplantation-clinicopathologic manifestations of a rare chronic GVHD. Zhonghua Xueyexue Zazhi 22 (2001) 415-417
52. Kim K.W., Yoon C.H., Kay C.S., et al. Membranous nephropathy after allogeneic hematopoietic stem cell transplantation in a patient with aplastic anemia: a case report. J. Korean Med. Sci. 18 (2003) 287-289
53. Papiha S.S., Pareek S.K., Rodger R.S., et al. HLA-A, B, DR and Bf allotypes in patients with idiopathic membranous nephropathy (IMN). Kidney Int. 31 (1987) 130-134
54. Hiki Y., Kobayashi Y., and Itoh I. Strong association of HLA-DR2 and MT1 with idiopathic membranous nephropathy in Japan. Kidney Int. 25 (1984) 953-957
55. Bergijk E.C., Munaut C., and Baelde J.J. A histologic study of the extracellular matrix during the development of glomerulosclerosis in murine chronic graft-versus-host disease. Am. J. Pathol. 140 (1992) 1147-1156
56. Rolink A.G., Gleichmann H., and Gleichmann E. Diseases caused by reactions of T lymphocytes to incompatible structures of the major histocompatibility complex: VII. Immune-complex glomerulonephritis. J. Immunol. 130 (1983) 209-215
57. Clynes R., Dumitru C., and Ravetch J.V. Uncoupling of immune complex formation and kidney damage in autoimmune glomerulonephritis. Science 279 (1998) 1052-1054
58. Radeke H.H., Gessner J.E., Uciechowski P., et al. Intrinsic human glomerular mesangial cells can express receptors for IgG complexes (hFc gamma RIII-A) and the associated Fc epsilon RI gamma-chain. J. Immunol. 153 (1994) 1281-1292
59. Metcalf D., Mifsud S., Di Rago L., et al. Polycystic kidneys and chronic inflammatory lesions are the delayed consequences of loss of the suppressor of cytokine signaling-1 (SOCS-1). Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 943-948
60. Krebs D.L., and Hilton D.J. SOCS: physiological suppressors of cytokine signaling. J. Cell Sci. 113 Pt. 16 (2000) 2813-2819
61. Marine J.C., Topham D.J., McKay C., et al. SOCS1 deficiency causes a lymphocyte-dependent perinatal lethality. Cell 98 (1999) 609-616
62. Billiau A.D., Fevery S., Rutgeerts O., et al. Transient expansion of Mac1+Ly6-G+Ly6-C+ early myeloid cells with suppressor activity in spleens of murine radiation marrow chimeras: possible implications for the graft-versus-host and graft-versus-leukemia reactivity of donor lymphocyte infusions. Blood 102 (2003) 740-748
63. Kemeny D.M., Noble A., Holmes B.J., et al. Immune regulation: a new role for the CD8+ T cell. Immunol. Today 15 (1994) 107-110
64. Serafini P., De Santo C., Marigo I., et al. Derangement of immune responses by myeloid suppressor cells. Cancer Immunol. Immunother. 53 (2004) 64-72
65. Vigouroux S., Yvon E., Biagi E., et al. Antigen-induced regulatory T cells. Blood 104 (2004) 26-33
66. Xystrakis E., Dejean A.S., Bernard I., et al. Identification of a novel natural regulatory CD8 T-cell subset and analysis of its mechanism of regulation. Blood 104 (2004) 3294-3301
67. Hoffmann P., Ermann J., Edinger M., et al. Donor-type CD4(+)CD25(+) regulatory T cells suppress lethal acute graft-versus-host disease after allogeneic bone marrow transplantation. J. Exp. Med. 196 (2002) 389-399
68. Cohen J.L., Trenado A., Vasey D., et al. CD4(+)CD25(+) immunoregulatory T Cells: new therapeutics for graft-versus-host disease. J. Exp. Med. 196 (2002) 401-406
69. Trenado A., Charlotte F., Fisson S., et al. Recipient-type specific CD4+CD25+ regulatory T cells favor immune reconstitution and control graft-versus-host disease while maintaining graft-versus-leukemia. J. Clin. Invest. 112 (2003) 1688-1696
70. Jones S.C., Murphy G.F., and Korngold R. Post-hematopoietic cell transplantation control of graft-versus-host disease by donor CD425 T cells to allow an effective graft-versus-leukemia response. Biol. Blood Marrow Transplant. 9 (2003) 243-256
71. Xia G., Kovochich M., Truitt R.L., et al. Tracking ex vivo-expanded CD4+CD25+ and CD8+CD25+ regulatory T cells after infusion to prevent donor lymphocyte infusion-induced lethal acute graft-versus-host disease. Biol. Blood Marrow Transplant. 10 (2004) 748-760
72. Johnson B.D., Konkol M.C., and Truitt R.L. CD25+ immunoregulatory T-cells of donor origin suppress alloreactivity after BMT. Biol. Blood Marrow Transplant. 8 (2002) 525-535