A roadmap toward clinical translation of genetically-modified stem cells for treatment of HIV

Trends in Molecular Medicine

Volumn 20, Issue 11, 2014, Pages 632-642

  Abou El Enein, Mohamed ^a   Bauer, Gerhard ^b   Reinke, Petra ^a   Renner, Matthias ^c   Schneider, Christian K ^d,e,f  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c PAUL EHRLICH INSTITUT   (Germany)

^d EUROPEAN MEDICINES AGENCY   (United Kingdom)

^e Danish Health and Medicines Authority   (Denmark)

^f INSTITUTE OF INFECTION IMMUNOLOGY   (Germany)

Author keywords

European medicines agency (EMA); Food and drug administration (FDA); Gene therapy; Lentiviral vector: HIV; Translational challenges

Indexed keywords

ALLOGENIC BONE MARROW TRANSPLANTATION; AUTOLOGOUS HEMATOPOIETIC STEM CELL TRANSPLANTATION; CELLULAR IMMUNITY; CLINICAL RESEARCH; CLINICAL TRIAL (TOPIC); DEVELOPMENTAL STAGE; DNA MODIFICATION; GENE DELIVERY SYSTEM; GENE TARGETING; GOOD MANUFACTURING PRACTICE; HEMATOPOIETIC STEM CELL; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE DEFICIENCY; NONHUMAN; PATIENT SAFETY; PRACTICE GUIDELINE; REVIEW; RISK ASSESSMENT; STEM CELL GENE THERAPY; THERAPY EFFECT; TRANSLATION REGULATION; ADVERSE EFFECTS; ANIMAL; BIOLOGICAL THERAPY; DISEASE MODEL; GENE THERAPY; GENETICS; HIV INFECTIONS; METABOLISM; PROCEDURES; STANDARDS; STEM CELL; TRANSLATIONAL RESEARCH;

ANIMALS; CELL- AND TISSUE-BASED THERAPY; DISEASE MODELS, ANIMAL; GENETIC THERAPY; HIV INFECTIONS; HUMANS; STEM CELLS; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84909644152     PISSN: 14714914     EISSN: 1471499X     Source Type: Journal    
DOI: 10.1016/j.molmed.2014.08.004     Document Type: Review

References (66)

1. Candotti F., et al. Gene therapy for adenosine deaminase-deficient severe combined immune deficiency: clinical comparison of retroviral vectors and treatment plans. Blood 2012, 120:3635-3646.
2. Kay M.A. 'State-of-the-art gene-based therapies: the road ahead. Nat. Rev. Genet. 2011, 12:316-328.
3. Battiwalla M., Barrett A.J. Bone marrow mesenchymal stromal cells to treat complications following allogeneic stem cell transplantation. Tissue Eng. Part B. Rev. 2014, 20:211-217.
4. Macpherson J.L., Rasko J.E.J. Clinical potential of gene therapy: towards meeting the demand. Intern. Med. J. 2014, 44:224-233.
5. Stan R., Zaia R.A. Practical considerations in gene therapy for HIV cure. Curr. HIV/AIDS Rep. 2014, 11:11-19.
6. Bauer G., Anderson J.S. Stem cell transplantation in the context of HIV - how can we cure HIV infection?. Expert Rev. Clin. Immunol. 2014, 10:107-116.
7. Klug B., et al. Regulatory structures for gene therapy medicinal products in the European Union. Methods Enzymol. 2012, 507:337-354.
8. Bai J.P.F., et al. Strategic applications of gene expression: from drug discovery/development to bedside. AAPS J. 2013, 15:427-437.
9. Maciulaitis R., et al. Clinical development of advanced therapy medicinal products in Europe: evidence that regulators must be proactive. Mol. Ther. 2012, 20:479-482.
10. Abou-El-Enein M. Improving the current translational research structure in academia for the progress of regenerative medicine. JSM Regen. Med. 2014, 2:2-4.
11. Freiberg M.S., et al. HIV infection and the risk of acute myocardial infarction. JAMA Intern. Med. 2013, 173:614-622.
12. Van Lint C., et al. HIV-1 transcription and latency: an update. Retrovirology 2013, 10:67.
13. von Wyl V., et al. Early antiretroviral therapy during primary HIV-1 infection results in a transient reduction of the viral setpoint upon treatment interruption. PLoS ONE 2011, 6:e27463.
14. Finzi D., et al. Identification of a reservoir for HIV-1 in patients on highly active antiretroviral therapy. Science 1997, 278:1295-1300.
15. Chun T.-W., et al. HIV-infected individuals receiving effective antiviral therapy for extended periods of time continually replenish their viral reservoir. J. Clin. Invest. 2005, 115:3250-3255.
16. Zhang L., et al. Quantifying residual HIV-1 replication in patients receiving combination antiretroviral therapy. N. Engl. J. Med. 1999, 340:1605-1613.
17. Siliciano J.D., et al. Long-term follow-up studies confirm the stability of the latent reservoir for HIV-1 in resting CD4+ T cells. Nat. Med. 2003, 9:727-728.
18. Barouch D.H. The quest for an HIV-1 vaccine--moving forward. N. Engl. J. Med. 2013, 369:2073-2076.
19. Schackman B.R., et al. The lifetime cost of current human immunodeficiency virus care in the United States. Med. Care 2006, 44:990-997.
20. Montessori V., et al. Adverse effects of antiretroviral therapy for HIV infection. CMAJ 2004, 170:229-238.
21. Schaecher K.L. The importance of treatment adherence in HIV. Am. J. Manag. Care 2013, 19(12 Suppl):s231-s237.
22. Savoldo B., et al. Treatment of solid organ transplant recipients with autologous Epstein Barr virus-specific cytotoxic T lymphocytes (CTLs). Blood 2006, 108:2942-2949.
23. Brestrich G., et al. Adoptive T-cell therapy of a lung transplanted patient with severe CMV disease and resistance to antiviral therapy. Am. J. Transplant. 2009, 9:1679-1684.
24. Anderson J.S., et al. Specific transduction of HIV-susceptible cells for CCR5 knockdown and resistance to HIV infection: a novel method for targeted gene therapy and intracellular immunization. J. Acquir. Immune Defic. Syndr. 2009, 52:152-161.
25. Nathwani A.C., et al. Adenovirus-associated virus vector-mediated gene transfer in hemophilia B. N. Engl. J. Med. 2011, 365:2357-2365.
26. DiGiusto D.L., et al. RNA-based gene therapy for HIV with lentiviral vector-modified CD34(+) cells in patients undergoing transplantation for AIDS-related lymphoma. Sci. Transl. Med. 2010, 2:36ra43.
27. Kiem H-P., et al. Hematopoietic-stem-cell-based gene therapy for HIV disease. Cell Stem Cell 2012, 10:137-147.
28. Anderson J.S., Bauer G. Fighting HIV with stem cell therapy: one step closer to human trials?. Expert Rev. Anti. Infect. Ther. 2012, 10:1071-1073.
29. Hütter G., et al. Long-term control of HIV by CCR5 Delta32/Delta32 stem-cell transplantation. N. Engl. J. Med. 2009, 360:692-698.
30. Bauer G., et al. In vivo biosafety model to assess the risk of adverse events from retroviral and lentiviral vectors. Mol. Ther. 2008, 16:1308-1315.
31. Walker J.E., et al. Generation of an HIV-1-resistant immune system with CD34(+) hematopoietic stem cells transduced with a triple-combination anti-HIV lentiviral vector. J. Virol. 2012, 86:5719-5729.
32. Voltz-Girolt C., et al. The advanced therapy classification procedure. Overview of experience gained so far. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 2011, 54:811-815.
33. Koehler R.N., et al. Oversight and Review of Clinical Gene Transfer Protocols: Assessing the Role of the Recombinant DNA Advisory Committee 2014, National Academies Press (US), Washington (DC).
34. Gavaghan H. Gene therapy approval may be rocky road for industry. Nature 1995, 374:202.
35. Arcidiacono J.A., et al. US Food and Drug Administration international collaborations for cellular therapy product regulation. Stem Cell Res. Ther. 2012, 3:38.
36. Candotti F. Gene transfer into hematopoietic stem cells as treatment for primary immunodeficiency diseases. Int. J. Hematol. 2014, 99:383-392.
37. Schmidt M., et al. Efficient characterization of retro-, lenti-, and foamyvector-transduced cell populations by high-accuracy insertion site sequencing. Ann. N. Y. Acad. Sci. 2003, 996:112-121.
38. Hacein-Bey-Abina S., et al. Efficacy of gene therapy for X-linked severe combined immunodeficiency. N. Engl. J. Med. 2010, 363:355-364.
39. Gaspar H.B., et al. Long-term persistence of a polyclonal T cell repertoire after gene therapy for X-linked severe combined immunodeficiency. Sci. Transl. Med. 2011, 3:97ra79.
40. Aiuti A., et al. The committee for advanced therapies of the European Medicines Agency reflection paper on management of clinical risks deriving from insertional mutagenesis. Hum. Gene Ther. Clin. Dev. 2013, 24:47-54.
41. Liu Y.P., Berkhout B. HIV-1-based lentiviral vectors. Methods Mol. Biol. 2014, 1087:273-284.
42. Ramezani A., Hawley R.G. Overview of the HIV-1 lentiviral vector system. Curr. Protoc. Mol. Biol. 2002, Chapter 16 Unit 16.21.
43. DiGiusto D.L. Development of hematopoietic stem cell based gene therapy for HIV-1 infection: considerations for proof of concept studies and translation to standard medical practice. Viruses 2013, 5:2898-2919.
44. Verma S., et al. Gene transfer into human umbilical cord blood-derived CD34+ cells by particle-mediated gene transfer. Gene Ther. 1998, 5:692-699.
45. Kohn D.B., et al. A clinical trial of retroviral-mediated transfer of a rev-responsive element decoy gene into CD34(+) cells from the bone marrow of human immunodeficiency virus-1-infected children. Blood 1999, 94:368-371.
46. Kambal A., et al. Generation of HIV-1 resistant and functional macrophages from hematopoietic stem cell-derived induced pluripotent stem cells. Mol. Ther. 2011, 19:584-593.
47. O'Donnell J.C. Personalized medicine and the role of health economics and outcomes research: issues, applications, emerging trends, and future research. Value Health 2013, 16(6 Suppl):S1-S3.
48. Maziarz R.T., Driscoll D. Hematopoietic stem cell transplantation and implications for cell therapy reimbursement. Cell Stem Cell 2011, 8:609-612.
49. Abou-El-Enein M., et al. Good Manufacturing Practices (GMP) manufacturing of advanced therapy medicinal products: a novel tailored model for optimizing performance and estimating costs. Cytotherapy 2013, 15:362-383.
50. van der Loo J.C.M., et al. Scale-up and manufacturing of clinical-grade self-inactivating γ-retroviral vectors by transient transfection. Gene Ther. 2012, 19:246-254.
51. Ansorge S., et al. Development of a scalable process for high-yield lentiviral vector production by transient transfection of HEK293 suspension cultures. J. Gene Med. 2009, 11:868-876.
52. Bennett M.S., Akkina R. Gene therapy strategies for HIV/AIDS: preclinical modeling in humanized mice. Viruses 2013, 5:3119-3141.
53. Kalomoiris S., et al. CD25 preselective anti-HIV vectors for improved HIV gene therapy. Hum. Gene Ther. Methods 2012, 23:366-375.
54. Morgan R.A., et al. Preferential survival of CD4+ T lymphocytes engineered with anti-human immunodeficiency virus (HIV) genes in HIV-infected individuals. Hum. Gene Ther. 2005, 16:1065-1074.
55. Amado R.G., et al. Anti-human immunodeficiency virus hematopoietic progenitor cell-delivered ribozyme in a phase I study: myeloid and lymphoid reconstitution in human immunodeficiency virus type-1-infected patients. Hum. Gene Ther. 2004, 15:251-262.
56. van Lunzen J., et al. Transfer of autologous gene-modified T cells in HIV-infected patients with advanced immunodeficiency and drug-resistant virus. Mol. Ther. 2007, 15:1024-1033.
57. Younan P.M., et al. Positive selection of mC46-expressing CD4+ T cells and maintenance of virus specific immunity in a primate AIDS model. Blood 2013, 122:179-187.
58. Trobridge G.D., et al. Protection of stem cell-derived lymphocytes in a primate AIDS gene therapy model after in vivo selection. PLoS ONE 2009, 4:e7693.
59. Cohn S.K., Weaver L.T. The Black Death and AIDS: CCR5-Delta32 in genetics and history. QJM 2006, 99:497-503.
60. Anderson, J.S. and Akkina, R., Complete knockdown of CCR5 and CXCR4 by siRNAs confers strong protection against HIV-1 infection in CD34 cell derived macrophages in vitro and SCID-hu derived thymocytes in vivo. Poster exhibition: 4th IAS Conference on HIV Pathogenesis, Treatment and Prevention. Abstract no: MOPEA065.
61. Allers K., et al. Evidence for the cure of HIV infection by CCR5δ32/δ32 stem cell transplantation. Blood 2011, 117:2791-2799.
62. Committee for Advanced Therapies (CAT), et al. Challenges with advanced therapy medicinal products and how to meet them. Nat. Rev. Drug Discov. 2010, 9:195-201.
63. Ziegele B., et al. The Innovation Office of the Paul-Ehrlich-Institut. Regulatory support during the scientific development of ATMP. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 2011, 54:857-866.
64. Takefman D., Bryan W. The state of gene therapies: the FDA perspective. Mol. Ther. 2012, 20:877-878.
65. Henrich T.J., et al. Long-term reduction in peripheral blood HIV type 1 reservoirs following reduced-intensity conditioning allogeneic stem cell transplantation. J. Infect. Dis. 2013, 207:1694-1702.
66. Henrich T.J., et al. Antiretroviral-free HIV-1 remission and viral rebound after allogeneic stem cell transplantation: report of 2 cases. Ann. Intern. Med. 2014, 10.7326/M14-1027.