Plant-produced human recombinant erythropoietic growth factors support erythroid differentiation in vitro

Stem Cells and Development

Volumn 22, Issue 16, 2013, Pages 2326-2340

  Musiychuk, Konstantin ^a   Sivalenka, Rajarajeswari ^b   Jaje, Jennifer ^a   Bi, Hong ^a   Flores, Rosemary ^a   Shaw, Brenden ^a   Jones, R Mark ^a   Golovina, Tatiana ^a   Schnipper, Jacob ^b   Khandker, Luipa ^b   Sun, Ruiqiang ^b   Li, Chang ^b   Kang, Lin ^b   Voskinarian Berse, Vanessa ^b   Zhang, Xiaokui ^b   Streatfield, Stephen ^a   Hambor, John ^b   Abbot, Stewart ^b   Yusibov, Vidadi ^a  

^a USA Center for Molecular Biotechnology   (United States)

^b CELGENE CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; ERYTHROPOIETIN; INTERLEUKIN 3; SOMATOMEDIN C; STEM CELL FACTOR;

ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CYTOKINE PRODUCTION; ERYTHROID CELL; NICOTIANA BENTHAMIANA; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN PURIFICATION; STEM CELL EXPANSION; TOBACCO MOSAIC VIRUS; UMBILICAL CORD BLOOD; WESTERN BLOTTING;

EID: 84881182657     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2012.0489     Document Type: Article

References (92)

1. Lelubre C and JL Vincent. (2011). Red blood cell transfusion in the critically ill patient. Ann Intensive Care 1:43
2. Sakr Y, S Lobo, S Knuepfer, E Esser, M Bauer, U Settmacher, D Barz and K Reinhart. (2010). Anemia and blood transfusion in a surgical intensive care unit. Crit Care 14:R92
3. Calabrich A and A Katz. (2011). Management of anemia in cancer patients. Future Oncol 7:507-517
4. Sharma S, P Sharma and LN Tyler. (2011). Transfusion of blood and blood products: Indications and complications. Am Fam Physician 83:719-724
5. Curinga G, A Jain, M Feldman, M Prosciak, B Phillips and S Milner. (2011). Red blood cell transfusion following burn. Burns 37:742-752
6. Jelkmann W. (1992). Erythropoietin: Structure, control of production, and function. Physiol Rev 72:449-489
7. Lin FK, S Suggs, CH Lin, JK Browne, R Smalling, JC Egrie, KK Chen, GM Fox, F Martin, et al. (1985). Cloning and expression of the human erythropoietin gene. Proc Natl Acad Sci U S A 82:7580-7584
8. Sasaki H, B Bothner, A Dell and M Fukuda. (1987). Carbohydrate structure of erythropoietin expressed in Chinese hamster ovary cells by a human erythropoietin cDNA. J Biol Chem 262:12059-12076
9. Sasaki H, N Ochi, A Dell and M Fukuda. (1988). Site-specific glycosylation of human recombinant erythropoietin: Analysis of glycopeptides or peptides at each glycosylation site by fast atom bombardment mass spectrometry. Biochemistry 27:8618-8626
10. Takeuchi M, S Takasaki, H Miyazaki, T Kato, S Hoshi, N Kochibe and A Kobata. (1988). Comparative study of the asparagine-linked sugar chains of human erythropoietins purified from urine and the culture medium of recombinant Chinese hamster ovary cells. J Biol Chem 263:3657-3663
11. Delorme E, T Lorenzini, J Giffin, F Martin, F Jacobsen, T Boone and S Elliott. (1992). Role of glycosylation on the secretion and biological activity of erythropoietin. Biochemistry 31:9871-9876
12. Fukuda MN, H Sasaki, L Lopez and M Fukuda. (1989). Survival of recombinant erythropoietin in the circulation: The role of carbohydrates. Blood 73:84-89
13. Yamaguchi K, K Akai, G Kawanishi, M Ueda, S Masuda and R Sasaki. (1991). Effects of site-directed removal of N-glycosylation sites in human erythropoietin on its production and biological properties. J Biol Chem 266:20434-20439
14. Spivak JL and BB Hogans. (1989). The in vivo metabolism of recombinant human erythropoietin in the rat. Blood 73:90-99
15. Takeuchi M, N Inoue, TW Strickland, M Kubota, M Wada, R Shimizu, S Hoshi, H Kozutsumi, S Takasaki and A Kobata. (1989). Relationship between sugar chain structure and biological activity of recombinant human erythropoietin produced in Chinese hamster ovary cells. Proc Natl Acad Sci U S A 86:7819-7822
16. Geissler EN, M Liao, JD Brook, FH Martin, KM Zsebo, DE Housman and SJ Galli. (1991). Stem cell factor (SCF), a novel hematopoietic growth factor and ligand for c-kit tyrosine kinase receptor, maps on human chromosome 12 between 12q14.3 and 12qter. Somat Cell Mol Genet 17:207-214
17. Palacios R and S Nishikawa. (1992). Developmentally regulated cell surface expression and function of c-kit receptor during lymphocyte ontogeny in the embryo and adult mice. Development 115:1133-1147
18. Ogawa M, Y Matsuzaki, S Nishikawa, S Hayashi, T Kunisada, T Sudo, T Kina, H Nakauchi and S Nishikawa. (1991). Expression and function of c-kit in hemopoietic progenitor cells. J Exp Med 174:63-71
19. Yoshinaga K, S Nishikawa, M Ogawa, S Hayashi, T Kunisada, T Fujimoto, and S Nishikawa. (1991). Role of c-kit in mouse spermatogenesis: Identification of spermatogonia as a specific site of c-kit expression and function. Development 113:689-699
20. Nishikawa S, M Kusakabe, K Yoshinaga, M Ogawa, S Hayashi, T Kunisada, T Era, T Sakakura and S Nishikawa. (1991). In utero manipulation of coat color formation by a monoclonal anti-c-kit antibody: Two distinct waves of c-kitdependency during melanocyte development. EMBO J 10:2111-2118
21. Broudy VC. (1997). Stem cell factor and hematopoiesis. Blood 90:1345-1364
22. Huang EJ, KH Nocka, J Buck and P Besmer. (1992). Differential expression and processing of two cell associated forms of the kit-ligand: KL-1 and KL-2. Mol Biol Cell 3:349-362
23. Toksoz D, KM Zsebo, KA Smith, S Hu, D Brankow, SV Suggs, FH Martin and DA Williams. (1992). Support of human hematopoiesis in long-Term bone marrow cultures by murine stromal cells selectively expressing the membranebound and secreted forms of the human homolog of the steel gene product, stem cell factor. Proc Natl Acad Sci U S A 89:7350-7354
24. Martin FH, SV Suggs, KE Langley, HS Lu, J Ting, KH Okino, CF Morris, IK McNiece, FW Jacobsen, et al. (1990). Primary structure and functional expression of rat and human stem cell factor DNAs. Cell 63:203-211
25. Arakawa T, DA Yphantis, JW Lary, LO Narhi, HS Lu, SJ Prestrelski, CL Clogston, KM Zsebo, EA Mendiaz, J Wypych and KE Langley. (1991). Glycosylated and unglycosylated recombinant-derived human stem cell factors are dimeric and have extensive regular secondary structure. J Biol Chem 266:18942-18948
26. Zsebo KM, J Wypych, IK McNiece, HS Lu, KA Smith, SB Karkare, RK Sachdev, VN Yuschenkoff, NC Birkett, et al. (1990). Identification, purification, and biological characterization of hematopoietic stem cell factor from buffalo rat liver -conditioned medium. Cell 63:195-201
27. Leary AG, HQ Zeng, SC Clark and M Ogawa. (1992). Growth factor requirements for survival in G0 and entry into the cell cycle of primitive human hemopoietic progenitors. Proc Natl Acad Sci U S A 89:4013-4017
28. Li CL and GR Johnson. (1994). Stem cell factor enhances the survival but not the self-renewal of murine hematopoietic long-Term repopulating cells. Blood 84:408-414
29. Bernstein ID, RG Andrews and KM Zsebo. (1991). Recombinant human stem cell factor enhances the formation of colonies by CD34 + and CD34 + lin-cells, and the generation of colony-forming cell progeny from CD34 + lin-cells cultured with interleukin-3, granulocyte colony-stimulating factor, or granulocyte-macrophage colony-stimulating factor. Blood 77:2316-2321
30. Lu HS, CL Clogston, J Wypych, VP Parker, TD Lee, K Swiderek, RF Baltera Jr, AC Patel, DC Chang, DW Brankow, et al. (1992). Post-Translational processing of membraneassociated recombinant human stem cell factor expressed in Chinese hamster ovary cells. Arch Biochem Biophys 298: 150-158
31. Whetton AD and TM Dexter. (1988). The mode of action of interleukin 3 in promoting survival, proliferation, and differentiation of hemopoietic progenitor cells. Lymphokines 15:355-374
32. Mangi MH and AC Newland. (1999). Interleukin-3 in hematology and oncology: Current state of knowledge and future directions. Cytokines Cell Mol Ther 5:87-95
33. Yang YC, AB Ciarletta, PA Temple, MP Chung, S Kovacic, JS Witek-Giannotti, AC Leary, R Kriz, RE Donahue, GG Wong and SC Clark. (1986). Human IL-3 (multi-CSF): Identification by expression cloning of a novel hematopoietic growth factor related to murine IL-3. Cell 47:3-10
34. Yang YC and SC Clark. (1987). Structure of the gene for human interleukin-3 or multi-CSF. Prog Clin Biol Res 251:3-11
35. Böhmer RM. (2004). Stem Cells IL-3-dependent early erythropoiesis is stimulated by autocrine transforming growth factor beta. Stem Cells 22:216-224
36. Umemura T, A al-Khatti, RE Donahue, T Papayannopoulou and G Stamatoyannopoulos. (1989). Effects of interleukin-3 and erythropoietin on in vivo erythropoiesis and F-cell formation in primates. Blood 74:1571-1576
37. Daughaday WH and P Rotwein. (1989). Insulin-like growth factors I and II. Peptide, messenger ribonucleic acid and gene structures, serum, and tissue concentrations. Endocr Rev 10:68-91
38. Jones JI and DR Clemmons. (1995). Insulin-like growth factors and their binding proteins: Biological actions. Endocr Rev 16:3-34
39. Kurtz A, J Zapf, KU Eckardt, G Clemons, ER Froesch and C Bauer. (1988). Insulin-like growth factor I stimulates erythropoiesis in hypophysectomized rats. Proc Natl Acad Sci U S A 85:7825-7829
40. Ratajczak J, Q Zhang, E Pertusini, BS Wojczyk, MA Wasik and MZ Ratajczak. (1998). The role of insulin (INS) and insulin-like growth factor-I (IGF-I) in regulating human erythropoiesis. Studies in vitro under serum-free conditions -comparison to other cytokines and growth factors. Leukemia 12:371-381
41. Lee-Huang S. (1984). Cloning and expression of human erythropoietin cDNA in Escherichia coli. Proc Natl Acad Sci U S A 81:2708-2712
42. Hamilton SR, RC Davidson, N Sethuraman, JH Nett, Y Jiang, S Rios, P Bobrowicz, TA Stadheim, H Li, et al. (2006). Humanization of yeast to produce complex terminally sialylated glycoproteins. Science 313:1441-1443
43. Kim YK, HS Shin, N Tomiya, YC Lee, MJ Betenbaugh and HJ Cha. (2005). Production and N-glycan analysis of secreted human erythropoietin glycoprotein in stably transfected Drosophila S2 cells. Biotechnol Bioeng 92:452-461
44. Jacobs K, C Shoemaker, R Rudersdorf, SD Neill, RJ Kaufman, A Mufson, J Seehra, SS Jones, R Hewick, EF Fritsch, et al. (1985). Isolation and characterization of genomic and cDNA clones of human erythropoietin. Nature 313:806-810
45. Powell JS, KL Berkner, RV Lebo and JW Adamson. (1986). Human erythropoietin gene: High level expression in stably transfected mammalian cells and chromosome localization. Proc Natl Acad Sci U S A 83:6465-6469
46. Goto M, K Akai, A Murakami, C Hashimoto, E Tsuda, M Ueda, C Kawanishi, N Takahashi, A Ishimoto, H Chiba and R Sasaki. (1988). Production of recombinant human erythropoietin in mammalian cells: Host-cell dependency of the biological activity of the cloned glycoprotein. Bio/Technology 6:67-71
47. Han J, X Yan, J Zhu, X Zhi, Y Zang, B Shen and J Qin. (2003). Expression of a novel recombinant dual human stem cell factor in insect cells. Protein Expr Purif 31:311-317
48. Yang YC and SC Clark. (1988). Cloning of the human interleukin-3 gene. Lymphokines 15:375-391
49. Ding H, C Griesel, M Nimtz, HS Conradt, HA Weich and V Jä ger. (2003). Molecular cloning, expression, purification, and characterization of soluble full-length, human interleukin-3 with a baculovirus-insect cell expression system. Protein Expr Purif 31:34-41
50. Joly JC, WS Leung and JR Swartz. (1998). Overexpression of Escherichia coli oxidoreductases increases recombinant insulin-like growth factor-I accumulation. Proc Natl Acad Sci U S A 95:2773-2777
51. Elliott S, KD Fagin, LO Narhi, JA Miller, M Jones, R Koski, M Peters, P Hsieh, R Sachdev and RD Rosenfeld. (1990). Yeastderived recombinant human insulin-like growth factor I: Production, purification, and structural characterization. J Protein Chem 9:95-104
52. Yusibov V and S Rabindran. (2008). Recent progress in the development of plant derived vaccines. Expert Rev Vaccines 7:1173-1183
53. Gomord V, AC Fitchette, L Menu-Bouaouiche, C Saint-Jore-Dupas, C Plasson, D Michaud and L Faye. (2010). Plantspecific glycosylation patterns in the context of therapeutic protein production. Plant Biotechnol J 8:564-587
54. Castilho A, P Gattinger, J Grass, J Jez, M Pabst, F Altmann, M Gorfer, R Strasser and H Steinkellner. (2011). N-glycosylation engineering of plants for the biosynthesis of glycoproteins with bisected and branched complex N-glycans. Glycobiology 21:813-823
55. Yusibov V, SJ Streatfield and N Kushnir. (2011). Clinical development of plant-produced recombinant pharmaceuticals: Vaccines, antibodies and beyond. Hum Vaccin 7:313-321
56. Musiychuk K, N Stephenson, H Bi, CE Farrance, G Orozovic, M Brodelius, P Brodelius, A Horsey, N Ugulava, et al. (2007). A launch vector for the production of vaccine antigens in plants. Influenza Other Respi Viruses 1:19-25
57. Green BJ, M Fujiki, V Mett, J Kaczmarczyk, M Shamloul, K Musiychuk, S Underkoffler, V Yusibov and V Mett. (2009). Transient protein expression in three Pisum sativum (green pea) varieties. Biotechnol J 4:230-237
58. Mett V, K Musiychuk, H Bi, CE Farrance, A Horsey, N Ugulava, Y Shoji, P de la Rosa, GA Palmer, et al. (2008). A plant-produced influenza subunit vaccine protects ferrets against virus challenge. Influenza Other Respi Viruses 2: 33-40
59. Shoji Y, JA Chichester, H Bi, K Musiychuk, P de la Rosa, L Goldschmidt, A Horsey, N Ugulava, GA Palmer, V Mett and V Yusibov. (2008). Plant-expressed HA as a seasonal influenza vaccine candidate. Vaccine 26:2930-2934
60. Shoji Y, CE Farrance, H Bi, M Shamloul, B Green, S Manceva, A Rhee, N Ugulava, G Roy, et al. (2009). Immunogenicity of hemagglutinin from A/Bar-headed Goose/Qinghai/1A/05 and A/Anhui/1/05 strains of H5N1 influenza viruses produced in Nicotiana benthamiana plants. Vaccine 27:3467-3470
61. Shoji Y, H Bi, K Musiychuk, A Rhee, A Horsey, G Roy, B Green, M Shamloul, CE Farrance, et al. (2009). Plant-derived hemagglutinin protects ferrets against challenge infection with the A/Indonesia/05/05 strain of avian influenza. Vaccine 27:1087-1092
62. Shoji Y, JA Chichester, M Jones, SD Manceva, E Damon, V Mett, K 2Musiychuk, H Bi, C Farrance, et al. (2011). Plantbased rapid production of recombinant subunit hemagglutinin vaccines targeting H1N1 and H5N1 influenza. Hum Vaccin 7 Suppl:41-50
63. Mett V, J Lyons, K Musiychuk, JA Chichester, T Brasil, R Couch, R Sherwood, GA Palmer, SJ Streatfield and V Yusibov. (2007). A plant-produced plague vaccine candidate confers protection to monkeys. Vaccine 25:3014-3017
64. Chichester JA, K Musiychuk, CE Farrance, V Mett, J Lyons, V Mett and V Yusibov. (2009). A single component twovalent LcrV-F1 vaccine protects non-human primates against pneumonic plague. Vaccine 27:3471-3474
65. Chichester JA, K Musiychuk, P de la Rosa, A Horsey, N Stevenson, N Ugulava, S Rabindran, GA Palmer, V Mett and V Yusibov. (2007). Immunogenicity of a subunit vaccine against Bacillus anthracis. Vaccine 25:3111-3114
66. Massa S, R Franconi, R Brandi, A Muller, V Mett, V Yusibov and A Venuti. (2007). Anti-cancer activity of plant-produced HPV16 E7 vaccine. Vaccine 25:3018-3021
67. Venuti A, S Massa, V Mett, LD Vedova, F Paolini, R Franconi and V Yusibov. (2009). An E7-based therapeutic vaccine protects mice against HPV16 associated cancer. Vaccine 27: 3395-3397
68. Park JS, KY Han, JH Lee, JA Song, KY Ahn, HS Seo, SJ Sim, SW Kim and J Lee. (2008). Solubility enhancement of aggregation-prone heterologous proteins by fusion expression using stress-responsive Escherichia coli protein, RpoS. BMC Biotechnol 8:15
69. Fox JD and DS Waugh. (2003). Maltose-binding protein as a solubility enhancer. Methods Mol Biol 205:99-117
70. Carter J, J Zhang, TL Dang, H Hasegawa, JD Cheng, I Gianan, JW O'Neill, M Wolfson, S Siu, et al. (2010). Fusion partners can increase the expression of recombinant interleukins via transient transfection in 2936E cells. Protein Sci 19: 357-362
71. Goldenkova IV, KA Musiǐchuk and ES Piruzian. (2002). [A thermostable Clostridium thermocellum lichenase-based reporter system for studying the gene expression regulation in prokaryotic and eukaryotic cells]. Mol Biol (Mosk) 36:868-876. Russian
72. Matsuoka M, N Yamamoto, Y Kano-Murakami, Y Tanaka, Y Ozeki, H Hirano, H Kagawa, M Oshima and Y Ohashi. (1987). Classification and structural comparison of fulllength cDNAs for pathogenesis-related proteins. Plant Physiol 85:942-946
73. Rayon C, P Lerouge and L Faye. (1998). The protein Nglycosylation in plants. J Exp Bot 49:1463-1472
74. Matsumoto S, K Ikura, M Ueda and R Sasaki. (1995). Characterization of a human glycoprotein (erythropoietin) produced in cultured tobacco cells. Plant Mol Biol 27:1163-1172
75. Weise A, F Altmann, M Rodriguez-Franco, ER Sjoberg, W Bäumer, H Launhard, M Kietzmann and G Gorr. (2007). High-level expression of secreted complex glycosylated recombinant human erythropoietin in the Physcomitrella Delta-fuc-T Delta-xyl-T mutant. Plant Biotechnol J 5:389-401
76. Cheon BY, HJ Kim, KH Oh, SC Bahn, JH Ahn, JW Choi, SH Ok, JM Bae and JS Shin. (2004). Overexpression of human erythropoietin (EPO) affects plant morphologies: Retarded vegetative growth in tobacco and male sterility in tobacco and Arabidopsis. Transgenic Res 13:541-549
77. Musa TA, C-Y Hung, DE Darlington, DC Sane and J Xie. (2009). Overexpression of human erythropoietin in tobacco does not affect plant fertility or morphology. Plant Biotechnol Rep 3:157-165
78. Sperb F, IC Werlang, M Margis-Pinheiro, LA Basso, DS Santos and G Pasquali. (2011). Molecular cloning and transgenic expression of a synthetic human erythropoietin gene in tobacco. Appl Biochem Biotechnol 165:652-665
79. Conley AJ, K Mohib, AM Jevnikar and JE Brandle. (2009). Plant recombinant erythropoietin attenuates inflammatory kidney cell injury. Plant Biotechnol J 7:183-199
80. Patel J, H Zhu, R Menassa, L Gyenis, A Richman and J Brandle. (2007). Elastin-like polypeptide fusions enhance the accumulation of recombinant proteins in tobacco leaves. Transgenic Res 16:239-249
81. Scheller J, D Henggeler, A Viviani and U Conrad. (2004). Purification of spider silk-elastin from transgenic plants and application for human chondrocyte proliferation. Transgenic Res 13:51-57
82. Floss DM, M Sack, J Stadlmann, T Rademacher, J Scheller, E Stö ger, R Fischer and U Conrad. (2008). Biochemical and functional characterization of anti-HIV antibody-ELP fusion proteins from transgenic plants. Plant Biotechnol J 6: 379-391
83. Scheller J, M Leps and U Conrad. (2006). Forcing singlechain variable fragment production in tobacco seeds by fusion to elastin-like polypeptides. Plant Biotechnol J 4: 243-249
84. Hondred D, JM Walker, DE Mathews and RD Vierstra. (1999). Use of ubiquitin fusions to augment protein expression in transgenic plants. Plant Physiol 119:713-724
85. Gil F, A Brun, A Wigdorovitz, R Catalá, JL Martínez- Torrecuadrada, I Casal, J Salinas, MV Borca and JM Escribano. (2001). High-yield expression of a viral peptide vaccine in transgenic plants. FEBS Lett 488:13-17
86. Dus Santos MJ, A Wigdorovitz, K Trono, RD Ríos, PM Franzone, F Gil, J Moreno, C Carrillo, JM Escribano and MV Borca. (2002). A novel methodology to develop a foot and mouth disease virus (FMDV) peptide-based vaccine in transgenic plants. Vaccine 20:1141-1147
87. Obregon P, D Chargelegue, PM Drake, A Prada, J Nuttall, L Frigerio and JK Ma. (2006). HIV-1 p24-immunoglobulin fusion molecule: A new strategy for plant-based protein production. Plant Biotechnol J 4:195-207
88. PanahiM, Z Alli, X Cheng, L Belbaraka, J Belgoudi, R Sardana, J Phipps and I Altosaar. (2004). Recombinant protein expression plasmids optimized for industrial E. coli fermentation and plant systems produce biologically active human insulin-like growth factor-1 in transgenic rice and tobacco plants. Transgenic Res 13:245-259
89. Daniell H, G Ruiz, B Denes, L Sandberg and W Langridge. (2009). Optimization of codon composition and regulatory elements for expression of human insulin like growth factor-1 in transgenic chloroplasts and evaluation of structural identity and function. BMC Biotechnol 9:33
90. Hintz-Obertreis P, D Krumwieh and FR Seiler. (1991). Development of a rapid, highly sensitive, non-radioactive assay system for hematopoietic growth factors. Behring Inst Mitt 90:99-103
91. Elliott S, J Egrie, J Browne, T Lorenzini, L Busse, N Rogers and I Ponting. (2004). Control of rHuEPO biological activity: The role of carbohydrate. Exp Hematol 32:1146-1155
92. Timmins NE and LK Nielsen. (2009). Blood cell manufacture: Current methods and future challenges. Trends Biotechnol 27:415-422