Induced pluripotent stem cell reprogramming by integration-free sendai virus vectors from peripheral blood of patients with craniometaphyseal dysplasia

Cellular Reprogramming

Volumn 15, Issue 6, 2013, Pages 503-513

  Chen, I Ping ^a   Fukuda, Keiichi ^b   Fusaki, Noemi ^b,c,d   Iida, Akihiro ^c   Hasegawa, Mamoru ^c   Lichtler, Alexander ^a   Reichenberger, Ernst J ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b KEIO UNIVERSITY   (Japan)

^c DNAVEC Corporation   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DNA POLYMERASE; FICOLL; GENOMIC DNA; KRUPPEL LIKE FACTOR 4; OCTAMER TRANSCRIPTION FACTOR 4; SMALL CYTOPLASMIC RNA; T LYMPHOCYTE RECEPTOR; THROMBOPOIETIN; VIRUS VECTOR;

ADHERENT CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOSOMAL DOMINANT INHERITANCE; BONE DISEASE; BONE DYSPLASIA; CELL CULTURE; CELL DIFFERENTIATION; CELL EXPANSION; CONTROLLED STUDY; CRANIOMETAPHYSEAL DYSPLASIA; CYTOKINE RELEASE; EMBRYOID BODY; EXON; FIBROBLAST; GENE CASSETTE; GENE DELETION; GENE EXPRESSION; GENE MUTATION; GENE REARRANGEMENT; HOST CELL; HUMAN; HUMAN CELL; HYPEROSTOSIS; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; IN VITRO STUDY; KARYOTYPE; METAPHASE CHROMOSOME; MONOGENIC DISORDER; MOUSE; MUSCULOSKELETAL DISEASE; NONHUMAN; ONCOGENE C MYC; OSTEOBLAST; OSTEOCLAST; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA VECTOR; SENDAI VIRUS; SKULL; STEM CELL; T LYMPHOCYTE RECEPTOR GENE; TERATOMA; TRANSGENE;

ADULT; BASE SEQUENCE; BONE DISEASES, DEVELOPMENTAL; CASE-CONTROL STUDIES; CHILD; CRANIOFACIAL ABNORMALITIES; DNA PRIMERS; FEMALE; GENE REARRANGEMENT, T-LYMPHOCYTE; GENETIC VECTORS; HUMANS; HYPEROSTOSIS; HYPERTELORISM; INDUCED PLURIPOTENT STEM CELLS; MALE; MIDDLE AGED; NUCLEAR REPROGRAMMING; POLYMERASE CHAIN REACTION; SENDAI VIRUS;

EID: 84888185205     PISSN: 21524971     EISSN: 21524998     Source Type: Journal    
DOI: 10.1089/cell.2013.0037     Document Type: Article

References (65)

1. Aasen, T., Raya, A., Barrero, M.J., Garreta, E., Consiglio, A., Gonzalez, F., Vassena, R., Bilic, J., Pekarik, V., Tiscornia, G., Edel, M., Boué, S., and Izpisúa Belmonte, J.C. (2008). Efficient and rapid generation of induced pluripotent stem cells from human keratinocytes. Nat. Biotechnol. 26, 1276-1284.
2. Ab Kadir, R., Zainal Ariffin, S.H., Megat Abdul Wahab, R., Kermani, S., and Senafi, S. (2012). Characterization of mononucleated human peripheral blood cells. Scientific World Journal 2012, 843843.
3. Ban, H., Nishishita, N., Fusaki, N., Tabata, T., Saeki, K., Shikamura, M., Takada, N., Inoue, M., Hasegawa, M., Kawamata, S., and Nishikawa, S. (2011). Efficient generation of transgenefree human induced pluripotent stem cells (iPSCs) by temperature-sensitive Sendai virus vectors. Proc. Natl. Acad. Sci. USA 108, 14234-14239.
4. Beighton, P., Hamersma, H., and Horan, F. (1979). Craniometaphyseal dysplasia-variability of expression within a large family. Clin. Genet. 15, 252-258. (Pubitemid 9126928)
5. Bitzer, M., Armeanu, S., Lauer, U.M., and Neubert, W.J. (2003). Sendai virus vectors as an emerging negative-strand RNA viral vector system. J. Gene Med. 5, 543-553. (Pubitemid 40310397)
6. Chen, C., Wang, Y., Goh, S.S., Yang, J., Lam, D.H., Choudhury, Y., Tay, F.C., Du, S., Tan, W.K., Purwanti, Y.I., Fan, W., and Wang, S. (2013). Inhibition of neuronal nitric oxide synthase activity promotes migration of human-induced pluripotent stem cell-derived neural stem cells toward cancer cells. J. Neurochem. 126, 318-330.
7. Chen, I.P., Wang, C.J., Strecker, S., Koczon-Jaremko, B., Boskey, A., and Reichenberger, E.J. (2009). Introduction of a Phe377del mutation in ANK creates a mouse model for craniometaphyseal dysplasia. J. Bone Min. Res. 24, 1206-1215.
8. Chen, I.P., Wang, L., Jiang, X., Aguila, H.L., and Reichenberger, E.J. (2011). A Phe377del mutation in ANK leads to impaired osteoblastogenesis and osteoclastogenesis in a mouse model for craniometaphyseal dysplasia (CMD). Hum. Mol. Genet. 20, 948-961.
9. Cherry, A.B., and Daley, G.Q. (2013). Reprogrammed cells for disease modeling and regenerative medicine. Annu. Rev. Med. 64, 277-290.
10. Choi, K.D., Vodyanik, M., and Slukvin, II (2011). Hematopoietic differentiation and production of mature myeloid cells from human pluripotent stem cells. Nat. Protoc. 6, 296-313.
11. Dimos, J.T., Rodolfa, K.T., Niakan, K.K., Weisenthal, L.M., Mitsumoto, H., Chung, W., Croft, G.F., Saphier, G., Leibel, R., Goland, R., Wichterle, H., Henderson, C.E., and Eggan. K. (2008). Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 321, 1218-1221.
12. Ding, Q., Lee, Y.K., Schaefer, E.A., Peters, D.T., Veres, A., Kim, K., Kuperwasser, N., Motola, D.L., Meissner, T.B., Hendriks, W.T., Trevisan, M., Gupta, R.M., Moisan, A., Banks, E., Friesen, M., Schinzel, R.T., Xia, F., Tang, A., Xia, Y., Figueroa, E., Wann, A., Ahfeldt, T., Daheron, L., Zhang, F., Rubin, L.L., Peng, L.F., Chung, R.T., Musunuru, K., and Cowan, C.A. (2013). A TALEN genome-editing system for generating human stem cell-based disease models. Cell Stem Cell 12, 238-251.
13. Emborg, M.E., Liu, Y., Xi, J., Zhang, X., Yin, Y., Lu, J., Joers, V., Swanson, C., Holden, J.E., and Zhang, S.C. (2013). Induced pluripotent stem cell-derived neural cells survive and mature in the nonhuman primate brain. Cell Rep. 3, 646-650.
14. Fang, L., Moore, X.L., Chan, W., White, D.A., Chin-Dusting, J., and Dart, A.M. (2012). Decreased fibrocyte number is associated with atherosclerotic plaque instability in man. Cardiovasc. Res. 95, 124-133.
15. Franz, D.C., Horn, K.L., and Aase, J. (1996). Craniometaphyseal dysplasia: Operative findings and treatment. Am. J. Otol. 17, 283-287. (Pubitemid 26173101)
16. Fusaki, N., Ban, H., Nishiyama, A., Saeki, K., and Hasegawa, M. (2009). Efficient induction of transgene-free human pluripotent stem cells using a vector based on Sendai virus, an RNA virus that does not integrate into the host genome. Proc. Japan Acad. Ser. B, Phys. Biol. Sci. 85, 348-362.
17. Giorgetti, A., Montserrat, N., Aasen, T., Gonzalez, F., Rodrguez-Piza , I., Vassena, R., Raya, A., Boué, S., Barrero, M.J., Corbella, B.A., Torrabadella, M., Veiga, A., Izpisua, and Belmonte, J.C. (2009). Generation of induced pluripotent stem cells from human cord blood using OCT4 and SOX2. Cell Stem Cell 5, 353-357.
18. Gonzalez, F., Boue, S., and Izpisua Belmonte, J.C. (2011). Methods for making induced pluripotent stem cells: Reprogramming a la carte. Nat. Rev. Genet. 12, 231-242.
19. Grabel, L. (2012). Prospects for pluripotent stem cell therapies: Into the clinic and back to the bench. J. Cell. Biochem. 113, 381-387.
20. Grigoriadis, A.E., Kennedy, M., Bozec, A., Brunton, F., Stenbeck, G., Park, I.H., Wagner, E.F., and Keller, G.M. (2010). Directed differentiation of hematopoietic precursors and functional osteoclasts from human ES and iPS cells. Blood 115, 2769-2776.
21. Ho, A.M., Johnson, M.D., and Kingsley, D.M. (2000). Role of the mouse ank gene in control of tissue calcification and arthritis. Science 289, 265-270. (Pubitemid 30469899)
22. Jackson, W.P., Albright, F., Drewry, G., Hanelin, J., and Rubin, M.I. (1954). Metaphyseal dysplasia, epiphyseal dysplasia, diaphyseal dysplasia, and related conditions. I. Familial metaphyseal dysplasia and craniometaphyseal dysplasia; their relation to leontiasis ossea and osteopetrosis; disorders of bone remodeling. AMA Arch. Int. Med. 94, 871-885.
23. Jahner, D., Stuhlmann, H., Stewart, C.L., Harbers, K., Lohler, J., Simon, I., and Jaenisch, R. (1982). De novo methylation and expression of retroviral genomes during mouse embryogenesis. Nature 298, 623-628. (Pubitemid 12099716)
24. Kim, J., Shin, J.M., Jeon, Y.J., Chung, H.M., and Chae, J.I. (2012). Proteomic validation of multifunctional molecules in mesenchymal stem cells derived from human bone marrow, umbilical cord blood and peripheral blood. PloS One 7, e32350.
25. Knight, S.C., Stagg, A., Hill, S., Fryer, P., and Griffiths, S. (1992). Development and function of dendritic cells in health and disease. J. Invest. Dermatol. 99, 33S-38S.
26. Kudva, Y.C., Ohmine, S., Greder, L.V., Dutton, J.R., Armstrong, A., De Lamo, J.G., Khan, Y.K., Thatava, T., Hasegawa, M., Fusaki, N., Slack, J.M., and Ikeda, Y. (2012). Transgene-free disease-specific induced pluripotent stem cells from patients with type 1 and type 2 diabetes. Stem Cells Transl. Med. 1, 451-461.
27. Kunisato, A., Wakatsuki, M., Shinba, H., Ota, T., Ishida, I., and Nagao, K. (2011). Direct generation of induced pluripotent stem cells from human nonmobilized blood. Stem Cells Dev. 20, 159-168.
28. Kuo, S.Y., Liu, H., Liao, Y.L., Chang, S.T., Hsieh, Y.C., Bandoh, B.A., Du, M.Q., and Chuang, S.S. (2011). A parallel comparison of T-cell clonality assessment between an in-house PCR assay and the BIOMED-2 assay leading to an efficient and cost-effective strategy. J. Clin. Pathol. 64, 536-542.
29. Lowry, W.E., Richter, L., Yachechko, R., Pyle, A.D., Tchieu, J., Sridharan, R., Clark, A.T., and Plath, K. (2008). Generation of human induced pluripotent stem cells from dermal fibroblasts. Proc. Natl. Acad. Sci. USA 105, 2883-2888. (Pubitemid 351723638)
30. Maehr, R., Chen, S., Snitow, M., Ludwig, T., Yagasaki, L., Goland, R., Leibel, R.L., and Melton, D.A. (2009). Generation of pluripotent stem cells from patients with type 1 diabetes. Proc. Natl. Acad. Sci. USA 106, 15768-15773.
31. Maherali, N., and Hochedlinger, K. (2008). Guidelines and techniques for the generation of induced pluripotent stem cells. Cell Stem Cell 3, 595-605.
32. McCarthy, K.P., Sloane, J.P., Kabarowski, J.H., Matutes, E., and Wiedemann, L.M. (1992). A simplified method of detection of clonal rearrangements of the T-cell receptor-gamma chain gene. Diagn. Mol. Pathol. 1, 173-179.
33. Merling, R.K., Sweeney, C.L., Choi, U., De Ravin, S.S., Myers, T.G., Otaizo-Carrasquero, F., Pan, J., Linton, G., Chen, L., Koontz, S., Theobald, N.L., and Malech, H.L. (2013). Transgene-free iPSCs generated from small volume peripheral blood nonmobilized CD34 + cells. Blood 121, e98-e107.
34. Nurnberg, P., Thiele, H., Chandler, D., Hohne, W., Cunningham, M.L., Ritter, H., Leschik, G., Uhlmann, K., Mischung, C., Harrop, K., Goldblatt, J., Borochowitz, Z.U., Kotzot, D., Westermann, F., Mundlos, S., Braun, H.S., Laing, N., and Tinschert, S. (2001). Heterozygous mutations in ANKH, the human ortholog of the mouse progressive ankylosis gene, result in craniometaphyseal dysplasia. Nat. Genet. 28, 37-41. (Pubitemid 32405813)
35. Papapetrou, E.P., Tomishima, M.J., Chambers, S.M., Mica, Y., Reed, E., Menon, J., Tabar, V., Mo, Q., Studer, L., and Sadelain, M. (2009). Stoichiometric and temporal requirements of Oct4, Sox2, Klf4, and c-Myc expression for efficient human iPSC induction and differentiation. Proc. Natl. Acad. Sci. USA 106, 12759-12764.
36. Park, I.H., Arora, N., Huo, H., Maherali, N., Ahfeldt, T., Shimamura, A., Lensch, M.W., Cowan, C., Hochedlinger, K., and Daley, G.Q. (2008a). Disease-specific induced pluripotent stem cells. Cell 134, 877-886.
37. Park, I.H., Zhao, R., West, J.A., Yabuuchi, A., Huo, H., Ince, T.A., Lerou, P.H., Lensch, M.W., and Daley, G.Q. (2008b). Reprogramming of human somatic cells to pluripotency with defined factors. Nature 451, 141-146.
38. Puliafito, C.A., Wray, S.H., Murray, J.E., and Boger, W.P., 3rd (1981). Optic atrophy and visual loss in craniometaphyseal dysplasia. Am. J. Ophthalmol. 92, 696-701. (Pubitemid 11031744)
39. Reichenberger, E., Tiziani, V., Watanabe, S., Park, L., Ueki, Y., Santanna, C., Baur, S.T., Shiang, R., Grange, D.K., Beighton, P., Gardner, J., Hamersma, H., Sellars, S., Ramesar, R., Lidral, A.C., Sommer, A., Raposo do Amaral, C.M., Gorlin, R.J., Mulliken, J.B., and Olsen, B.R. (2001). Autosomal dominant craniometaphyseal dysplasia is caused by mutations in the transmembrane protein ANK. Am. J. Hum. Genet. 68, 1321-1326. (Pubitemid 32510607)
40. Richards, A., Brain, C., Dillon, M.J., and Bailey, C.M. (1996). Craniometaphyseal and craniodiaphyseal dysplasia, head and neck manifestations and management. J. Laryngol. Otol. 110, 328-338. (Pubitemid 26137539)
41. Satoh, K., Iwata, T., and Ikeda, H. (1994). Unsuccessful consequence of optic canal decompression for a case of craniometaphyseal dysplasia. Plastic Reconstr. Surg. 94, 705-708. (Pubitemid 24314073)
42. Seki, T., Yuasa, S., Oda, M., Egashira, T., Yae, K., Kusumoto, D., Nakata, H., Tohyama, S., Hashimoto, H., Kodaira, M., Okada, Y., Seimiya, H., Fusaki, N., Hasegawa, M., and Fukuda, K. (2010). Generation of induced pluripotent stem cells from human terminally differentiated circulating T cells. Cell Stem Cell 7, 11-14.
43. Shea, J., Gerbe, R., and Ayani, N. (1981). Craniometaphyseal dysplasia: the first successful surgical treatment for associated hearing loss. The Laryngoscope 91, 1369-1374. (Pubitemid 12216066)
44. Sommer, C.A., Stadtfeld, M., Murphy, G.J., Hochedlinger, K., Kotton, D.N., and Mostoslavsky, G. (2009). Induced pluripotent stem cell generation using a single lentiviral stem cell cassette. Stem Cells 27, 543-549.
45. Sommer, C.A., Sommer, A.G., Longmire, T.A., Christodoulou, C., Thomas, D.D., Gostissa, M., Alt, F.W., Murphy, G.J., Kotton, D.N., and Mostoslavsky, G. (2010). Excision of reprogramming transgenes improves the differentiation potential of iPS cells generated with a single excisable vector. Stem Cells 28, 64-74.
46. Stadtfeld, M., Nagaya, M., Utikal, J., Weir, G., and Hochedlinger, K. (2008). Induced pluripotent stem cells generated without viral integration. Science 322, 945-949.
47. Staerk, J., Dawlaty, M.M., Gao, Q., Maetzel, D., Hanna, J., Sommer, C.A., Mostoslavsky, G., and Jaenisch, R. (2010). Reprogramming of human peripheral blood cells to induced pluripotent stem cells. Cell Stem Cell 7, 20-24.
48. Susa, M., Luong-Nguyen, N.H., Cappellen, D., Zamurovic, N., and Gamse, R. (2004). Human primary osteoclasts:I vitro generation and applications as pharmacological and clinical assay. J. Transl. Med. 2, 6.
49. Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., Tomoda, K., and Yamanaka, S. (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861-872. (Pubitemid 350138099)
50. Teo, A.K., Windmueller, R., Johansson, B.B., Dirice, E., Njolstad, P.R., Tjora, E., Raeder, H., and Kulkarni, R.N. (2013). Derivation of human induced pluripotent stem cells from patients with maturity onset diabetes of the young. J. Biol. Chem. 288, 5353-5356.
51. Tokusumi, T., Iida, A., Hirata, T., Kato, A., Nagai, Y., and Hasegawa, M. (2002). Recombinant Sendai viruses expressing different levels of a foreign reporter gene. Virus Res. 86, 33-38. (Pubitemid 34655571)
52. Villa-Diaz, L.G., Brown, S.E., Liu, Y., Ross, A.M., Lahann, J., Parent, J.M., and Krebsbach, P.H. (2012). Derivation of mesenchymal stem cells from human induced pluripotent stem cells cultured on synthetic substrates. Stem Cells 30, 1174-1181.
53. von Bergwelt-Baildon, M.S., Vonderheide, R.H., Maecker, B., Hirano, N., Anderson, K.S., Butler, M.O., Xia, Z., Zeng, W.Y., Wucherpfennig, K.W., Nadler, L.M., and Schultze, J.L. (2002). Human primary and memory cytotoxic T lymphocyte responses are efficiently induced by means of CD40-activated B cells as antigen-presenting cells: Potential for clinical application. Blood 99, 3319-3325. (Pubitemid 34525313)
54. Warren, L., Manos, P.D., Ahfeldt, T., Loh, Y.H., Li, H., Lau, F., Ebina, W., Mandal, P.K., Smith, Z.D., Meissner, A., Daley, G.Q., Brack, A.S., Collins, J.J., Cowan, C., Schlaeger, T.M., and Rossi, D.J. (2010). Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell 7, 618-630.
55. Wernig, M., Meissner, A., Foreman, R., Brambrink, T., Ku, M., Hochedlinger, K., Bernstein, B.E., and Jaenisch, R. (2007). In vitro reprogramming of fibroblasts into a pluripotent ES-celllike state. Nature 448, 318-324. (Pubitemid 47080337)
56. Woltjen, K., Michael, I.P., Mohseni, P., Desai, R., Mileikovsky, M., Hämäläinen, R., Cowling, R., Wang, W., Liu, P., Gertsenstein, M., Kaji, K., Sung, H.K., and Nagy, A. (2009). piggyBac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature 458, 766-770.
57. Yan, X., Qin, H., Qu, C., Tuan, R.S., Shi, S., and Huang, G.T. (2010). iPS cells reprogrammed from human mesenchymallike stem/progenitor cells of dental tissue origin. Stem Cells Dev. 19, 469-480.
58. Yang, L., Scott, P.G., Giuffre, J., Shankowsky, H.A., Ghahary, A., and Tredget, E.E. (2002). Peripheral blood fibrocytes from burn patients: identification and quantification of fibrocytes in adherent cells cultured from peripheral blood mononuclear cells. Lab. Invest. 82, 1183-1192. (Pubitemid 35014852)
59. Ye, Z., Zhan, H., Mali, P., Dowey, S., Williams, D.M., Jang, Y.Y., Dang, C.V., Spivak, J.L., Moliterno, A.R., and Cheng, L. (2009). Human-induced pluripotent stem cells from blood cells of healthy donors and patients with acquired blood disorders. Blood 114, 5473-5480.
60. Young, L.J., and Deane, E.M. (2005). Culture and characterisation of peripheral blood monocytes and monocyte-derived adherent cells of the tammar wallaby, Macropus eugenii. Immunol. Lett. 96, 253-259. (Pubitemid 39600783)
61. Yu, J., Vodyanik, M.A., Smuga-Otto, K., Antosiewicz-Bourget, J., Frane, J.L., Tian, S., Nie, J., Jonsdottir, G.A., Ruotti, V., Stewart, R., Slukvin, I.I., and Thomson, J.A. (2007). Induced pluripotent stem cell lines derived from human somatic cells. Science 318, 1917-1920.
62. Yu, J., Hu, K., Smuga-Otto, K., Tian, S., Stewart, R., Slukvin, II, and Thomson, J.A. (2009). Human induced pluripotent stem cells free of vector and transgene sequences. Science 324, 797-801.
63. Zhou, H., Wu, S., Joo, J.Y., Zhu, S., Han, D.W., Lin, T., Trauger, S., Bien, G., Yao, S., Zhu, Y., Siuzdak, G., Schöler, H.R., Duan, L., and Ding, S. (2009). Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 4, 381-384.
64. Zhou, L.J., and Tedder, T.F. (1995). Human blood dendritic cells selectively express CD83, a member of the immunoglobulin superfamily. J. Immunol. 154, 3821-3835.
65. Zhou, T., Benda, C., Dunzinger, S., Huang, Y., Ho, J.C., Yang, J., Wang, Y., Zhang, Y., Zhuang, Q., Li, Y., Bao, X., Tse, H.F., Grillari, J., Grillari-Voglauer, R., Pei, D., and Esteban, M.A. (2012). Generation of human induced pluripotent stem cells from urine samples. Nat. Protoc. 7, 2080-2089.