Synthesis, regulation and production of urokinase using mammalian cell culture: A comprehensive review

Biotechnology Advances

Volumn 24, Issue 5, 2006, Pages 514-528

  Roychoudhury, Pradip K ^a   Khaparde, Shilpa S ^a   Mattiasson, Bo ^b   Kumar, Ashok ^c  

^a INDIAN INSTITUTE OF TECHNOLOGY DELHI   (India)

^b LUND UNIVERSITY   (Sweden)

^c INDIAN INSTITUTE OF TECHNOLOGY KANPUR   (India)

Author keywords

Process integration; Tissue plasminogen activator; Urokinase production; Urokinase synthesis and regulation

Indexed keywords

BIOCHEMISTRY; CATALYSIS; CELL CULTURE; DRUG PRODUCTS; SYNTHESIS (CHEMICAL); TISSUE;

PROCESS INTEGRATION; TISSUE PLASMINOGEN ACTIVATOR; UROKINASE PRODUCTION; UROKINASE SYNTHESIS AND REGULATION;

ENZYMES;

UROKINASE;

BLOOD; CELLS AND CELL COMPONENTS; DRUG; ENZYME; SEPARATION;

ANIMAL; BIOSYNTHESIS; CULTURE TECHNIQUE; ISOLATION AND PURIFICATION; MAMMAL; METABOLISM; REVIEW;

ANIMALS; CELL CULTURE TECHNIQUES; MAMMALS; URINARY PLASMINOGEN ACTIVATOR;

MAMMALIA;

EID: 33746267955     PISSN: 07349750     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biotechadv.2006.05.002     Document Type: Review

References (107)

1. Aguirre Ghiso J.A., Alonso D.F., FarõÂas E.F., and Bal de Kier Joffe Â.E. Overproduction of urokinase-type plasminogen activator is regulated by phospholipase D- and protein kinase C-dependent pathways in murine mammary adenocarcinoma cells. Biochim Biophys Acta 1356 (1997) 171-184
2. Aguirre Ghiso J.A., Alonso D.F., FarõÂas E.F., Gomez D.E., and Bal de Kier Joffe Á.E. Deregulation of the signaling pathways controlling urokinase production its relationship with the invasive phenotype. Eur J Biochem 263 (1999) 295-304
3. Avgerinos G.C., Drapeau D., Socolow J.S., Mao J.I., and Broese R.J. Spin filter perfusion system for high density cell culture: production of recombinant urinary type plasminogen activator in CHO cells. Biotechnology (NY) 8 (1990) 54-58
4. Bansal V., and Roychoudhury P.K. Production and purification of urokinase: a comprehensive review. Protein Expr Purif 45 (2006) 1-14
5. Bansal V, Roychoudhury PK, Mattiasson B, Kumar A. Recovery of urokinase from integrated mammalian cell culture cryogel bioreactor and purification of the enzyme using p-aminobenzamidine affinity chromatography. J. Mol. Recognition, in press.
6. Barnes L.M., Bentley C.M., and Dickson A.J. Stability of protein production from recombinant mammalian cells. Biotechnol Bioeng 81 (2003) 632-638
7. Behrendt N., List K., Anreasen P.A., and Sano K. The prourokinase plasminogen activation system in the presence of serpin type inhibitors and the urokinase receptor: rescue of activity through reciprocal proenzyme activation. Biochem J 371 (2003) 277-287
8. Bernik M.B., and Kwaan H.C. Plasminogen activator activity in cultures from human tissues. An immunological and histochemical study. J Clin Invest 48 (1969) 1740-1753
9. Blobe G.C., Obeid M.L., and Hannun Y.A. Regulation of protein kinase C and role in cancer biology. Cancer Metastasis Rev 13 (1994) 411-431
10. Booyse M., Lin P.H., Traylor M., and Bruce R. Purification and properties of a single-chain urokinase-type plasminogen activator form produced by subcultured human umbilical vein endothelial cells. J Biol Chem 263 (1988) 15139-15145
11. Burgering B.M.T., and Bos J.L. Regulation of Ras-mediated signalling: more than one way to skin a cat. Trends Biol. Sci. 20 (1995) 18-22
12. Chaniotakis N.A. Enzyme stabilization strategies based on electrolytes and polyelectrolytes for biosensor applications. Anal Bioanal Chem 378 (2004) 89-95
13. Chen Z., Wu B., Jia X., and Xiao C. Study on serum-free media for genetically engineered CHO cells producing prourokinase. Chin J Biotechnol 12 (1996) 169-175
14. Chen Z., Wu B., Liu H., Liu X., and Huang P. Temperature shift as a process optimization step for the production of Pro-urokinase by a recombinant Chinese hamster ovary cell line in high-density perfusion culture. J Biosci Bioeng 97 (2004) 239-243
15. Collen D. Ham-Wasserman lecture: role of the plasminogen system in fibrin-homeostasis and tissue remodeling. Hematology (2001) 1-9
16. Conese M., Nykjaer A., Petersen C.M., Cremona O., Pardi R., Andreasen P.A., et al. α-2 Macroglobulin receptor/Ldl receptor-related protein (Lrp)-dependent internalization of the urokinase receptor. J Cell Biol 131 (1995) 1609-1622
17. Cubellis M.V., Wun T.C., and Blasi F. Receptor-mediated internalization and degradation of urokinase is caused by its specific inhibitor PAI-1. EMBO J 9 (1990) 1079-1085
18. Dano K., Moller V., Ossowski L., and Nielsen L.S. Purification and characterization of a plasminogen activator from mouse cells transformed by an oncogenic virus. Biochim Biophys Acta 613 (1980) 542-555
19. Dumler I., Weis A., Mayboroda O.A., Maasch C., Jerke U., Haller H., et al. The Jak/Stat pathway and urokinase receptor signalling in human aortic vascular smooth muscle cells. J Biol Chem 273 (1998) 315-321
20. Ellaiah P., Saisha V., and Srinivasulu B. Effect of low frequency AC electric fields on urokinase production by MPGN kidney cells. Process Biochem 39 (2003) 1-4
21. Ellis V., and Dano K. Potentiation of plasminogen activation by an anti-urokinase monoclonal antibody due to ternary complex formation. A mechanistic model for receptor-mediated plasminogen activation. J Biol Chem 268 (1993) 4806-4813
22. Ellis V., Scully M.F., and Kakkar V.V. Plasminogen activation initiated by single-chain urokinase-type plasminogen activator. Potentiation by U937 monocytes. J Biol Chem 264 (1989) 2185-2188
23. Ellis V., Behrendt N., and Dano K. Plasminogen activation by receptor-bound urokinase. A kinetic study with both cell-associated and isolated receptor. J Biol Chem 266 (1991) 12752-12758
24. Feder J. Flat bed hollow fiber bioreactors for large scale cultivation of animal cells. Methods Enzymol 135 (1987) 393-399
25. Fukao H., Ikeda M., Ichikawa T., Inufusa H., Okada K., Ueshima S., et al. Effect of hyperthermia on the viability and fibrinolytic potential of human cancer cell lines. Clin Chim Acta 296 (2000) 17-33
26. Fust G.Y., and Keresztes M. Plasminogen-plasmin system in complement activation induced by endotoxin. Ann Immunol Hung 17 (1973) 29-31
27. Galliher P. Critical Factors in Cell Culture Media Development. Paper presented at: BioLOGIC USA; 2004; Boston, MA.
28. Gao L.H., Hu X.W., Wu Q.F., Xiao C.Z., Xu Z.P., and Zhang Z.G. Single-chain urokinase-type plasminogen activator (sc-uPA) purification by immuno-affinity chromatography. Sheng Wu Gong Cheng Xue Bao 18 (2002) 356-359
29. Gibson P.R., van de Pol E., and Doe W.F. Cell associated urokinase activity and colonic epithelial cells in health and disease. Gut 32 (1991) 191-195
30. Ginestra A., Monesa S., Seghzzi G., Dolo V., Nagase H., Mignatti P., et al. Urokinase plasminogen activator and gelatinases are associated with membrane vesicles shed by human HT-1080 fibrosarcoma cells. J Biol Chem 272 (1997) 17216-17222
31. Gomes G., Gayatri, and Roychoudhury P.K. Urokinase production using human kidney cell line-effect of amino acid supplementation. Chemcon (2000) 101-104 BIO
32. Griffiths J.B., and Electricwala A. Production of tissue plasminogen activators from animal cells. Adv Biochem Eng Biotechnol 34 (1987) 147-166
33. Hartnell G.G., and Gates J. The case of Abbokinase and the FDA: the events leading to the suspension of Abbokinase supplies in the United States. J Vasc Interv Radiol 11 (2000) 11841-11847
34. Heaton J.H., and Gelehrter T.D. Glucocorticoid induction of plasminogen activator-inhibitor messenger RNA in rat hepatoma cells. Mol Endocrinol 3 (1989) 349-355
35. Helenius G., Heydarkhan-Hagvall S., Siegbahn A., and Risberg B. Tissue engineering expression of fibrinolytic and coagulation factors in cocultured human endothelial and smooth muscle cells. Tissue Eng 10 (2004) 353-360
36. Holmberg L., Bladh B., and Astedt B. Purification of urokinase by affinity chromatography, Biochim. Biophys Acta 445 (1976) 215-222
37. Hu X.W., Xiao C.Z., Li Z.H., Guo L.H., Zhang Z.G., and Wang F. Production of u-PA with rCHO cell culture on porous microcarriers in serum-free growth medium. Sheng Wu Gong Cheng Xue Bao 16 (2000) 387-391
38. Hu X.W., Xiao C.Z., Huang Z., Guo Z., Zhang Z., and Li Z. Pilot production of u-PA with porous microcarrier cell culture. Cytotechnology 33 (2000) 13-19
39. Irigoyen J.P., Besser D., and Nagamine Y. Cytoskeleton reorganization induces the urokinase-type plasminogen activator gene via the Ras/extracellular signal-regulated kinase (ERK) signaling pathway. J Biol Chem 272 (1997) 1904-1909
40. Irigoyen J.P., Munoz-Canoves P., Montero L., and Nagaime Y. The plasminogen activator system: biology and regulation. Cell Mol Life Sci 56 (1999) 104-132
41. Jiang Q., Yasothornsrikul S., Taupenot L., Milesa L.A., and Parmer R.J. The local chromaffin cell plasminogen/plasmin system and the regulation of catecholamine secretion. Ann N Y Acad Sci 971 (2002) 445-449
42. Jo E.C., Yun J.W., Chung S.I., and Kim J.H. Performance study of perfusion cultures for production of single-chain urokinase-type plasminogen activator (scu-PA) in a 2.5 l spin filter bioreactor. Bioprocess Eng 19 (1998) 363-372
43. Kang J.K., Choi S.K., and Lee H.Y. Kinetics of producing pro-urokinase in perfusion cultures. Biotechnol Lett 12 (1990) 173-178
44. Khaparde S.S., and Roychoudhury P.K. Production of urokinase using hollow fiber bioreactor. Indian Chemical Engineering Conference. Tech Ses Transcript 6 (2004) 11
45. Khaparde S.S., and Roychoudhury P.K. Effect of temperature shift on urokinase production in hollow fiber bioreactor. Indian Chemical Engineering Conference. Tech Sess Transcript 2 (2005) 255
46. Kim D.M., and Swartz J.R. Efficient production of a bioactive, multiple disulfide-bonded protein using modified extracts of Escherichia coli. Biotechnol Bioeng 85 (2004) 122-129
47. Kohno T., Hopper P., Lillquist J.S., Suddith R.L., Greenlee R., and Moir D.T. Kidney plasminogen activator: a precursor form of human urokinase with high fibrin affinity. Bio/Technology 2 (1984) 628-634
48. Konakova M., Hucho F., and Schleuning W.D. Downstream targets of urokinase-type plasminogen-activator-mediated signal transduction. Eur J Biochem 253 (1998) 421-429
49. Kumar A., Bansal V., Nanadakumar K.S., Galaev I., Roychoudhury P.K., Holmdahl R., et al. Integrated bioprocess for the production and isolation of urokinase from animal cell culture using supermacroporous cryogels. Biotechnol Bioeng 93 (2006) 636-646
50. Kumar A., Bansal V., Andersson J., Roychoudhury P.K., and Mattiasson B. Supermacroporous cryogel matrix for integrated protein isolation: immobilized metal affinity chromatography purification of urokinase from cell culture broth of a human kidney cell line. J Chromatogr A 1103 (2006) 35-42
51. Kuo M. Urokinase production 1980; U.S. pat. 4,190,708.
52. Kusch A., Tkachuk S., Lutter S., Haller H., Dietz R., Lipp M., et al. Monocyte-expressed urokinase regulates human vascular smooth muscle cell migration in a coculture model. Biol Chem 383 (2002) 217-221
53. Lee M., and Severson D. Signal transduction in vascular smooth muscle: diacylglycerol second messengers and PKC action. Am J Physiol 267 (1994) C659-C678
54. Lesuk A., Terminiello L., and Traver J.H. Crystalline human urokinase: some properties. Science 147 (1965) 880-881
55. Lewis J.L. Plasminogen activator (urokinase) from cultured cells. Thromb Haemost 42 (1979) 700-895
56. Lewis JL. Production of urokinase 1976; U.S. Pat. 3,930,945.
57. Maciag T., Weibel M.K., and Pye E.K. Affinity chromatography of urokinase. In: Jakoby W.B., and Wilchek M. (Eds). Methods in enzymology (1974), Plenum, New York 451-459
58. Malluci M., Dunn M., Wells V., and Delia D. A cell cycle study of the effects of Con A on synchronized mouse embryo fibroblasts: arrest at the two specific stages of the cycle and dissociation between uptake of thymidine and DNA synthesis. J Cell Sci 46 (1980) 353-363
59. Mann G. Method of producing plasminogen activator. 1980; U.S. Pat. No. 4,232,124.
60. Matuli M., and Brdar B. Induction of urokinase-type plasminogen activator, induction of urokinase-type plasminogen activator by sodium salicylate in a glioblastoma cell strain. Food Technol Biotechnol 39 (2001) 5-11
61. McGuire P.G., and Alexander S.M. Urokinase production by embryonic endocardial-derived cells: regulation by substrate composition. Dev Biol 155 (1993) 442-451
62. Medcalf R.L., Van den Berg E., and Schleuning W.-D. Glucocorticoid-modulated gene expression of tissue-and urinary-type plasminogen activator and plasminogen activator inhibitor 1 and 2. J Cell Biol 106 (1988) 971-978
63. Medcalf R.L., and Hamilton J.A. Human synovial fibroblasts produce urokinase-type plasminogen activator. Arthritis Rheum 29 (1986) 1397-1401
64. Miles L.A., and Plow E.F. Plasminogen receptors: ubiquitous sites for cellular regulation of fibrinolysis. Fibrinolysis 2 (1988) 61-67
65. Möhäyen H. Regulation of plasminogen activators. Academic dissertation Department of Virology 27 (2000), University of Helsinki, Finland
66. Nguyen D.H., Hussaini I.M., and Gonias S.L. Binding of urokinase-type plasminogen activator to its receptor in MCF-7 cells activates extracellular signal-regulated kinase 1 and 2 which is required for increased cellular motility. J Biol Chem 273 (1998) 8502-8507
67. Nicol EC. The addition of specified amounts of pronase to the production medium for urokinase using live cells increases the production of urokinase by 50-100%. U.S patent. 1976; 3,930,944.
68. Nolli M.L., Sarubbi E., Corti A., Robbiati F., Soflientini A., Blasi F., et al. Production and characterization of human recombinant single chain urokinase-type plasminogen activator from mouse cells. Fibrinolysis 3 (1989) 101-106
69. Nykjaer A., Petersen C.M., Moller B., Jensen P.H., Moestrup S.K., Holtet T.L., et al. Purified alpha 2-macroglobulin receptor/LDL receptor-related protein binds urokinase.plasminogen activator inhibitor type-1 complex. Evidence that the alpha 2-macroglobulin receptor mediates cellular degradation of urokinase receptor-bound complexes. J Biol Chem 267 (1992) 14543-14546
70. Nykjær A., Conese1 A., Christensen E.I., Olson D., Cremona O., Gliemann J., et al. Recycling of the urokinase receptor upon internalization of the uPA: serpin complexes. EMBO J 16 (1997) 2610-2620
71. Ohta S., Niiya K., Sakuragawa N., and Fuse H. Induction of urokinase-type plasminogen activator by lipopolysaccharide in PC-3 human prostatic cancer cells. Thromb Res 97 (2000) 342-347
72. Oikarinen A., Hoytya M., and Jarvinen M. Dexamethasone-induced plasminogen activator inhibitor: characterization, purification, and preparation of monoclonal antibodies. Arch Dermatol Res 282 (1990) 153-158
73. Osterwalder T., Cinelli P., Baici A., Pennella A., Rueger S.R., Schrimpf S.P., et al. The axonally secreted serine proteinase inhibitor, neuroserpin, inhibits plasminogen activators and plasmin but not thrombin. J Biol Chem 273 (1998) 2312-2322
74. Ouriel K. Safety and efficacy of thrombolytic agents. Rev. Cardiovasc. Med. 3 suppl 2 (2003) S17-S24
75. Peterson L.C., Lund L.R., Nielson L.S., Dano K., and Skriver L. One chain urokinase type plasminogen activator from human sarcoma cells is a proenzyme with little or no intrinsic activity. J Biol Chem 263 (1988) 11189-11195
76. Plesner T., Ploug M., Ellis V., Ronne E., Hoyer-Hansen G., Wittrup M., et al. The receptor for urokinase-type plasminogen activator and urokinase is translocated from two distinct intracellular compartments to the plasma membrane on stimulation of human neutrophils. Blood 83 (1994) 808-815
77. Pollanen J., Saksela O., Salonen E.M., Andreasen P., Nielsen L., and Dano K. Distinct localization of urokinase-type plasminogen activator and its type 1 inhibitor under cultured human fibroblasts and sarcoma cells. J Cell Biol 104 (1987) 1085-1096
78. Quax P.H.A., Boxman I.L.A., van Kesteren C.A.M., Verheijen J.H., and Ponec M. Plasminogen activators are involved in keratinocyte and fibroblast migration in wounded cultures in vitro. Fibrinolysis 8 (1994) 221-228
79. Rodriguez-Fragoso L., Alvarez R., Esparaza J.A., and Garces M.E. Acetaldehyde increases the activity and gene expression of urokinase type plasminogen activator in hepatic stellate cell line. Toxicology 137 (1999) 1-11
80. Rouf S.A., Moo-Young M., and Chisti Y. Tissue-type plasminogen activator: characteristics, applications and production technology. Biotechnol Adv 14 (1996) 239-266
81. Roychoudhury P.K., Gomes J., Bhattacharyay S.K., and Abdullah N. Production of urokinase by HT 1080 human kidney cell line. Artif Cells Blood Substit Immobil Biotechnol 27 (1999) 399-402
82. Satoh M., Hosoi S., Miyaji H., Itoh S., and Sato S. Stable production of recombinant pro-urokinase by human lymphoblastoid Namalwa KJM-1 cells: host-cell dependency of the expressed-protein stability. Cytotechology 13 (1993) 79-88
83. Shatos M.A., Orfeo T., Doherty J.M., Penar P.L., Collen D., and Mann K.G. α-Thrombin stimulates srokinase production and DNA synthesis in cultured human cerebral microvascular endothelial cells. Arterioscler Thromb Vasc Biol 15 (1995) 903-911
84. Sidenius N., and Blasi F. The urokinase plasminogen activator system in cancer: recent advances and implication for prognosis and therapy. Cancer Metastasis Rev 22 (2003) 205-222
85. Singhal A. Operational strategies for production of urokinase by HT-1080 human fibrosarcoma cell line in a perfusion bioreactor, M. Tech Thesis, IIT Delhi, India, 1997.
86. Smith P.C., Shantibanez J.F., Morales J.P., and Martinez J. Epidermal growth factor stimulates urokinase gene expression in human gingivial fibroblasts. Possible modulation by genistein and curcumin. J Periodontal Res 39 (2004) 380-387
87. Sokabe T., Yamamoto K., Ohura N., Nakatsuka H., Qin K., Obi S., et al. Differential regulation of urokinase-type plasminogen activator expression by fluid shear stress in human coronary artery endothelial cells. Am J Physiol Heart Circ Physiol 287 (2004) 2027-2034
88. Stepanova V.V., and Tkachuk V.A. Urokinase as a multidomain protein and polyfunctional cell regulator. Biochemistry (Moscow) 67 (2002) 127-138
89. Stoppelli M.P., Verde P., Grimaldi G., Locatelli E.K., and Blasi F. Increase in urokinase plasminogen activator mRNA synthesis in human carcinoma cells is a primary effect of the potent tumor promoter, phorbol myristate acetate. J Cell Biol 102 (1986) 1235-1241
90. Stump D.C., Lijnen H.R., and Collen D. Purification and characterization of single-chain urokinase type plasminogen activator from human cell cultures. J Biol Chem 261 (1986) 1274-1278
91. Tang W., Sun Z., Pannell R., Gurewich V., and Liu J.N. An efficient system for production of recombinant urokinase-type plasminogen activator. Protein Expr Purif 11 (1997) 279-283
92. Tao T.Y., Bohn M.A., Ji G.Y., Einsele A., and Hu W.S. Kinetics of prourokinase production by human kidney cells in culture. J Biotechnol 6 (1987) 205-224
93. Turner B.G., Avgerinos G.C., Melnick L.M., and Moir D.T. Optimisation of pro-urokinase secretion from recombinant Saccharomyces cerevisiae. Biotechnol Bioeng 37 (1991) 869-875
94. Varani J., Hasday J.D., Sitrin R.G., Brubaker P.G., and Hillegas W.J. Proteolytic enzymes and arachidonic acid metabolites produced by MRC-5 cells on various microcarrier substrates. In Vitro Cell Dev Biol 22 (1986) 575-582
95. Varani J., Sitrin R.G., and Hillegas W. Expression of plasminogen activator and plasminogen activator inhibitor mRNA in human fibroblasts grown on different substrates. Cytotechnology 9 (1992) 157-162
96. Verde P., Stoppelli M.P., Galeffi P., Di Nocera P., and Blasi F. Identification of and primary sequence of an unspliced human urokinase poly(A)+RNA. Proc Natl Sci U S A 31 (1984) 4727-4731
97. Verde P., Boast S., Franze A., Robbiati F., and Blasi F. An upstream enhancer and a negative element in the 5′ flanking region of the human urokinase plasminogen activator gene. Nucleic Acids Res 16 (1988) 10699-10707
98. Vetterlein D., and Calton G.J. Purification of urokinase from complex mixtures using immobilized monoclonal antibody against urokinase light chain. Thromb Haemost 49 (1983) 24-27
99. Vetterlein D., Bell T.E., Young P.L., and Roblin R. Immunological quantitation and imunoadsorption of urokinase-like plasminogen activators secreted by human cells. J Biol Chem 255 (1980) 3665-3672
100. Wagner A., Marc A., and ENgasser J.M. Continuous production of prourokinase in feed harvest and perfusion cultures. Biotechnol Bioeng 36 (1990) 623-629
101. Williams J.R.B. The fibrinolytic activity of urine. Br J Exp Pathol 32 (1951) 530-537
102. Wun T.C., Ossowski L., and Reich E. Proenzyme form of human urokinase. J Biol Chem 257 (1982) 7262-7268
103. Wun T.C., Schleuning W.D., and Reich E. Isolation and characterization of urokinase from human plasma. J Biol Chem 257 (1982) 3276-3283
104. Xiao C., Huang Z., Li W., Hu X., Qu W., Gao L., et al. High density and scale-up cultivation of recombinant CHO cell line and hybridomas with porous microcarrier cytopore. Cytotechnology 30 (1999) 143-147
105. Xing R.H., and Rabbani S.A. Transcriptional regulation of urokinase (uPA) gene in breast cancer. Int J Cancer 81 (1999) 443-450
106. Zahm M., Kaplan H., Hérard A.L., Doriot F., Pierrot D., Somelette P., et al. Cell migration and proliferation during the in vitro wound repair of the respiratory epithelium. Cell motil Cytoskelet 37 (1997) 33-43
107. Ziche M., Parenti A., Ledda F., Dell'Era P., Granger H.J., Maggi C.A., et al. Nitric Oxide promotes proliferation and plasminogen activator production by coronary venular endothelium through endogenous bFGF. Circ Res 80 (1997) 845-852