TAT-mediated intracellular protein delivery to primary brain cells is dependent on glycosaminoglycan expression

Biotechnology and Bioengineering

Volumn 104, Issue 1, 2009, Pages 10-19

  Simon, Melissa J ^a   Gao, Shan ^b   Woo, Hyeun Kang ^a   Banta, Scott ^b   Morrison III, Barclay ^a  

^a MC 8904 ^*  (United States)

^b Columbia University ^*  (United States)

Author keywords

Cell penetrating peptide; Flow cytometry; Glycosaminoglycans; Intracellular protein delivery; Protein transduction domain; TAT

Indexed keywords

CELL PENETRATING PEPTIDE; GLYCOSAMINOGLYCANS; INTRACELLULAR PROTEIN DELIVERY; PROTEIN TRANSDUCTION DOMAIN; TAT;

AMINES; BACTERIOPHAGES; BIOCHEMICAL ENGINEERING; BODY FLUIDS; CELL MEMBRANES; FLOW CYTOMETRY; GENETIC ENGINEERING; INTERNET; NEURONS; PEPTIDES;

CELL CULTURE;

CELL PENETRATING PEPTIDE; CELL PROTEIN; GLYCOSAMINOGLYCAN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; NERVE GROWTH FACTOR RECEPTOR; TRANSACTIVATOR PROTEIN;

ARTICLE; ASTROCYTE; BRAIN CELL; CELL CULTURE; CELL DIFFERENTIATION; CELL LINE; CELL STRAIN; COCULTURE; CONTROLLED STUDY; CULTURE MEDIUM; HUMAN; HUMAN CELL; MONOCULTURE; NERVE CELL; PROTEIN EXPRESSION; PROTEIN PURIFICATION;

ANIMALS; ASTROCYTES; CELL LINE; CELLS, CULTURED; CULTURE MEDIA; CULTURE MEDIA, SERUM-FREE; GLYCOSAMINOGLYCANS; GREEN FLUORESCENT PROTEINS; NEURONS; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

EID: 69249146180     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.22377     Document Type: Article

References (71)

1. Asoh S, Ohsawa I, Mori T, Katsura K, Hiraide T, Katayama Y, Kimura M, Ozaki D, Yamagata K, Ohta S. 2002. Protection against ischemic brain injury by protein therapeutics. Proc Natl Acad Sci USA 99(26):17107-17112. (Pubitemid 36034106)
2. Audouy S, Mallet J, Privat A, Gimenez y Ribotta M. 1999. Adenovirusmediated suicide gene therapy in an in vitro model of reactive gliosis. GLIA 25(3):293-303.
3. Begley DJ. 2004. Delivery of therapeutic agents to the central nervous system: The problems and the possibilities. Pharmacol Ther 104(1): 29-45. (Pubitemid 39410561)
4. Bugatti A, Urbinati C, Ravelli C, De Clercq E, Liekens S, Rusnati M. 2007. Heparin-mimicking sulfonic acid polymers as multitarget inhibitors of human immunodeficiency virus type 1 Tat and gp120 proteins. Antimicrob Agents Chemother 51(7):2337-2345. (Pubitemid 47047308)
5. Cai SR, Xu G, Becker-Hapak M, Ma M, Dowdy SF, McLeod HL. 2006. The kinetics and tissue distribution of protein transduction in mice. Eur J Pharm Sci 27(4):311-319. (Pubitemid 43143256)
6. Cao G, Pei W, Ge H, Liang Q, Luo Y, Sharp FR, Lu A, Ran R, Graham SH, Chen J. 2002. In vivo delivery of a Bcl-xL fusion protein containing the TAT protein transduction domain protects against ischemic brain injury and neuronal apoptosis. J Neurosci 22(13):5423-5431.
7. Caron NJ, Torrente Y, Camirand G, Bujold M, Chapdelaine P, Leriche K, Bresolin N, Tremblay JP. 2001. Intracellular delivery of a Tat-eGFP fusion protein into muscle cells. Mol Ther 3(3):310-318. (Pubitemid 32514646)
8. Chauhan A, Tikoo A, Kapur AK, Singh M. 2007. The taming of the cell penetrating domain of the HIV Tat: Myths and realities. J Control Release 117(2):148-162. (Pubitemid 46172502)
9. Chou RC, Langan TJ. 2003. In vitro synchronization of mammalian astrocytic cultures by serum deprivation. Brain Res Brain Res Protoc 11(3):162-167.
10. Costa C, Tortosa R, Domenech A, Vidal E, Pumarola M, Bassols A. 2007. Mapping of aggrecan, hyaluronic acid, heparan sulphate proteoglycans and aquaporin 4 in the central nervous system of the mouse. J Chem Neuroanat 33(3):111-123. (Pubitemid 46528688)
11. David G. 1993. Integral membrane heparan sulfate proteoglycans. FASEB J 7(11):1023-1030. (Pubitemid 23243444)
12. Dietz GP, Bahr M. 2004. Delivery of bioactive molecules into the cell: The Trojan horse approach. Mol Cell Neurosci 27(2):85-131. (Pubitemid 39370094)
13. Duchardt F, Fotin-Mleczek M, Schwarz H, Fischer R, Brock R. 2007. A comprehensive model for the cellular uptake of cationic cell-penetrating peptides. Traffic 8(7):848-866. (Pubitemid 46971632)
14. Duport S, Robert F, Muller D, Grau G, Parisi L, Stoppini L. 1998. An in vitro blood-brain barrier model: Cocultures between endothelial cells and organotypic brain slice cultures. Proc Natl Acad Sci USA 95(4):1840-1845. (Pubitemid 28103481)
15. Farndale RW, Buttle DJ, Barrett AJ. 1986. Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim Biophys Acta 883(2):173-177.
16. Gao S, Simon MJ, Morrison B III, Banta S. 2009. Bifunctional chimeric fusion proteins engineered for DNA delivery: Optimization of the protein to DNA ratio. Biochim Biophys Acta 1790(3):198-208.
17. Gill SC, von Hippel PH. 1989. Calculation of protein extinction coefficients from amino acid sequence data. Anal Biochem 182(2):319-326. (Pubitemid 19277112)
18. Giordano JL. 1999. On reporting uncertainties of the straight-line regression parameters. Eur J Phys 20(5):343-349.
19. Greene LA, Tischler AS. 1976. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci USA 73(7):2424-2428.
20. Hallbrink M, Floren A, Elmquist A, Pooga M, Bartfai T, Langel U. 2001. Cargo delivery kinetics of cell-penetrating peptides. Biochim Biophys Acta 1515(2):101-109. (Pubitemid 33086827)
21. Han K, Jeon MJ, Kim SH, Ki D, Bahn JH, Lee KS, Park J, Choi SY. 2001. Efficient intracellular delivery of an exogenous protein GFP with genetically fused basic oligopeptides. Mol Cells 12(2):267-271. (Pubitemid 33731899)
22. Ho A, Schwarze SR, Mermelstein SJ, Waksman G, Dowdy SF. 2001. Synthetic protein transduction domains: Enhanced transduction potential in vitro and in vivo. Cancer Res 61(2):474-477. (Pubitemid 32128600)
23. Huynh GH, Deen DF, Szoka FC Jr. 2006. Barriers to carrier mediated drug and gene delivery to brain tumors. J Control Release 110(2):236-259. (Pubitemid 41827478)
24. Joliot A, Prochiantz A. 2004. Transduction peptides: From technology to physiology. Nat Cell Biol 6(3):189-196.
25. Kao J, Huey G, Kao R, Stern R. 1990. Ascorbic acid stimulates production of glycosaminoglycans in cultured fibroblasts. Exp Mol Pathol 53(1):1-10. (Pubitemid 20303146)
26. Katoh-Semba R, Oohira A, Kashiwamata S. 1990. Changes in glycosaminoglycans during the neuritogenesis in PC12 pheochromocytoma cells induced by nerve growth factor. J Neurochem 55(5):1749-1757. (Pubitemid 20351107)
27. Kilic E, Dietz GP, Hermann DM, Bahr M. 2002. Intravenous TAT-Bcl-Xl is protective after middle cerebral artery occlusion in mice. Ann Neurol 52(5):617-622. (Pubitemid 35246865)
28. Kilic U, Kilic E, Dietz GP, Bahr M. 2003. Intravenous TAT-GDNF is protective after focal cerebral ischemia in mice. Stroke 34(5):1304-1310. (Pubitemid 36547533)
29. Koppelhus U, Awasthi SK, Zachar V, Holst HU, Ebbesen P, Nielsen PE. 2002. Cell-dependent differential cellular uptake of PNA, peptides, and PNA-peptide conjugates. Antisense Nucleic Acid Drug Dev 12(2):51-63. (Pubitemid 34627600)
30. Kramer SD, Wunderli-Allenspach H. 2003. No entry for TAT(44-57) into liposomes and intact MDCK cells: Novel approach to study membrane permeation of cell-penetrating peptides. Biochim Biophys Acta 1609(2):161-169. (Pubitemid 36120723)
31. Krystek M, Anton M. 2007. A weighted total least-squares algorithm for fitting a straight line. Meas Sci Technol 18(11):3438-3442. (Pubitemid 350132695)
32. Kumarasuriyar A, Dombrowski C, Rider DA, Nurcombe V, Cool SM. 2007. A novel use of TAT-EGFP to validate techniques to alter osteosarcoma cell surface glycosaminoglycan expression. J Mol Histol 38(5):435-447. (Pubitemid 350056779)
33. Langan TJ, Slater MC. 1991. Quiescent astroglia in long-term primary cultures re-enter the cell cycle and require a non-sterol isoprenoid in late G1. Brain Res 548(1-2):9-17.
34. Lea NC, Buggins AG, Orr SJ, Mufti GJ, Thomas NS. 2003. High efficiency protein transduction of quiescent and proliferating primary hematopoietic cells. J Biochem Biophys Methods 55(3):251-258.
35. Lee JY, Chang MY, Park CH, Kim HY, Kim JH, Son H, Lee YS, Lee SH. 2003. Ascorbate-induced differentiation of embryonic cortical precursors into neurons and astrocytes. J Neurosci Res 73(2):156-165. (Pubitemid 36835416)
36. Matsushita M, Tomizawa K, Moriwaki A, Li ST, Terada H, Matsui H. 2001. A high-efficiency protein transduction system demonstrating the role of PKA in long-lasting long-term potentiation. J Neurosci 21(16):6000-6007. (Pubitemid 32737733)
37. Mortimer I, Tam P, MacLachlan I, Graham RW, Saravolac EG, Joshi PB. 1999. Cationic lipid-mediated transfection of cells in culture requires mitotic activity. Gene Ther 6(3):403-411. (Pubitemid 29132342)
38. Mueller J, Kretzschmar I, Volkmer R, Boisguerin P. 2008. Comparison of cellular uptake using 22 CPPs in 4 different cell lines. Bioconjug Chem 19(12):2363-2374.
39. Nagahara H, Vocero-Akbani AM, Snyder EL, Ho A, Latham DG, Lissy NA, Becker-Hapak M, Ezhevsky SA, Dowdy SF. 1998. Transduction of fulllength TAT fusion proteins into mammalian cells: TAT-p27Kip1 induces cell migration. Nat Med 4(12):1449-1452. (Pubitemid 28553472)
40. Nakagawa S, Deli MA, Nakao S, Honda M, Hayashi K, Nakaoke R, Kataoka Y, Niwa M. 2007. Pericytes from brain microvessels strengthen the barrier integrity in primary cultures of rat brain endothelial cells. Cell Mol Neurobiol 27(6):687-694. (Pubitemid 47476613)
41. Nakase I, Tadokoro A, Kawabata N, Takeuchi T, Katoh H, Hiramoto K, Negishi M, Nomizu M, Sugiura Y, Futaki S. 2007. Interaction of arginine-rich peptides with membrane-associated proteoglycans is crucial for induction of actin organization and macropinocytosis. Biochemistry 46(2):492-501. (Pubitemid 46105438)
42. Niesner U, Halin C, Lozzi L, Gunthert M, Neri P, Wunderli-Allenspach H, Zardi L, Neri D. 2002. Quantitation of the tumor-targeting properties of antibody fragments conjugated to cell-permeating HIV-1 TAT peptides. Bioconjug Chem 13(4):729-736. (Pubitemid 34801114)
43. Panizzon KL, Shin D, Frautschy S, Wallis RA. 1998. Neuroprotection with Bcl-2(20-34) peptide against trauma. Neuroreport 9(18):4131-4136. (Pubitemid 29030702)
44. Pardridge WM. 2005. The blood-brain barrier: Bottleneck in brain drug development. NeuroRx 2(1):3-14. (Pubitemid 40128022)
45. Park J, Ryu J, Kim KA, Lee HJ, Bahn JH, Han K, Choi EY, Lee KS, Kwon HY, Choi SY. 2002. Mutational analysis of a human immunodeficiency virus type 1 Tat protein transduction domain which is required for delivery of an exogenous protein into mammalian cells. J Gen Virol 83(Pt 5):1173-1181. (Pubitemid 34477291)
46. Poon GM, Gariepy J. 2007. Cell-surface proteoglycans as molecular portals for cationic peptide and polymer entry into cells. Biochem Soc Trans 35(Pt 4):788-793. (Pubitemid 47310369)
47. Rapraeger A, Jalkanen M, Bernfield M. 1986. Cell surface proteoglycan associates with the cytoskeleton at the basolateral cell surface of mouse mammary epithelial cells. J Cell Biol 103(6 Pt 2):2683-2696. (Pubitemid 17008014)
48. Richard JP, Melikov K, Vives E, Ramos C, Verbeure B, Gait MJ, Chernomordik LV, Lebleu B. 2003. Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake. J Biol Chem 278(1):585-590. (Pubitemid 36043612)
49. Ryu J, Han K, Park J, Choi SY. 2003. Enhanced uptake of a heterologous protein with an HIV-1 Tat protein transduction domains (PTD) at both termini. Mol Cells 16(3):385-391. (Pubitemid 41582867)
50. Sakurai H, Kawabata K, Sakurai F, Nakagawa S, Mizuguchi H. 2007. Innate immune response induced by gene delivery vectors. Int J Pharm 354(1-2):9-15.
51. Schwarze SR, Ho A, Vocero-Akbani A, Dowdy SF. 1999. In vivo protein transduction: Delivery of a biologically active protein into the mouse. Science 285(5433):1569-1572.
52. Sengoku T, Bondada V, Hassane D, Dubal S, Geddes JW. 2004. Tatcalpastatin fusion proteins transduce primary rat cortical neurons but do not inhibit cellular calpain activity. Exp Neurol 188(1):161-170. (Pubitemid 38748814)
53. Soane L, Fiskum G. 2005. TAT-mediated endocytotic delivery of the loop deletion Bcl-2 protein protects neurons against cell death. J Neurochem 95(1):230-243. (Pubitemid 41384441)
54. Suzuki T, Futaki S, Niwa M, Tanaka S, Ueda K, Sugiura Y. 2002. Possible existence of common internalization mechanisms among arginine-rich peptides. J Biol Chem 277(4):2437-2443. (Pubitemid 34953265)
55. Temsamani J, Vidal P. 2004. The use of cell-penetrating peptides for drug delivery. Drug Discov Today 9(23):1012-1019. (Pubitemid 39574557)
56. Trehin R, Merkle HP. 2004. Chances and pitfalls of cell penetrating peptides for cellular drug delivery. Eur J Pharm Biopharm 58(2):209-223. (Pubitemid 39037230)
57. Tunnemann G, Martin RM, Haupt S, Patsch C, Edenhofer F, Cardoso MC. 2006. Cargo-dependent mode of uptake and bioavailability of TATcontaining proteins and peptides in living cells. FASEB J 20(11):1775-1784. (Pubitemid 44933791)
58. Tyagi M, Rusnati M, Presta M, Giacca M. 2001. Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans. J Biol Chem 276(5): 3254-3261. (Pubitemid 37411619)
59. Vazquez J, Sun C, Du J, Fuentes L, Sumners C, Raizada MK. 2003. Transduction of a functional domain of the AT1 receptor in neurons by HIV-Tat PTD. Hypertension 41(3 Pt 2):751-756. (Pubitemid 36314586)
60. Violini S, Sharma V, Prior JL, Dyszlewski M, Piwnica-Worms D. 2002. Evidence for a plasma membrane-mediated permeability barrier to Tat basic domain in well-differentiated epithelial cells: Lack of correlation with heparan sulfate. Biochemistry 41(42):12652-12661. (Pubitemid 35192494)
61. Vives E. 2003. Cellular uptake [correction of uptake] of the Tat peptide: An endocytosis mechanism following ionic interactions. J Mol Recognit 16(5):265-271. (Pubitemid 37231695)
62. Vives E. 2005. Present and future of cell-penetrating peptide mediated delivery systems: "Is the Trojan horse too wild to go only to Troy?". J Control Release 109(1-3):77-85.
63. Wadia JS, Stan RV, Dowdy SF. 2004. Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat Med 10(3):310-315.
64. Warda M, Toida T, Zhang F, Sun P, Munoz E, Xie J, Linhardt RJ. 2006. Isolation and characterization of heparan sulfate from various murine tissues. Glycoconj J 23(7-8):555-563. (Pubitemid 44477397)
65. Washbourne P, McAllister AK. 2002. Techniques for gene transfer into neurons. Curr Opin Neurobiol 12(5):566-573.
66. Wender PA, Mitchell DJ, Pattabiraman K, Pelkey ET, Steinman L, Rothbard JB. 2000. The design, synthesis, and evaluation of molecules that enable or enhance cellular uptake: Peptoid molecular transporters. Proc Natl Acad Sci USA 97(24):13003-13008.
67. Wilke M, Fortunati E, van den Broek M, Hoogeveen AT, Scholte BJ. 1996. Efficacy of a peptide-based gene delivery system depends on mitotic activity. Gene Ther 3(12):1133-1142. (Pubitemid 27036117)
68. Yang TT, Cheng L, Kain SR. 1996. Optimized codon usage and chromophore mutations provide enhanced sensitivity with the green fluorescent protein. Nucleic Acids Res 24(22):4592-4593. (Pubitemid 26388650)
69. Yang Y, Ma J, Song Z, Wu M. 2002. HIV-1 TAT-mediated protein transduction and subcellular localization using novel expression vectors. FEBS Lett 532(1-2):36-44. (Pubitemid 35375863)
70. Yin W, Cao G, Johnnides MJ, Signore AP, Luo Y, Hickey RW, Chen J. 2006. TAT-mediated delivery of Bcl-xL protein is neuroprotective against neonatal hypoxic-ischemic brain injury via inhibition of caspases and AIF. Neurobiol Dis 21(2):358-371. (Pubitemid 43099859)
71. Yu DH, Lee KH, Lee JY, Kim S, Shin DM, Kim JH, Lee YS, Oh SK, Moon SY, Lee SH. 2004. Changes of gene expression profiles during neuronal differentiation of central nervous system precursors treated with ascorbic acid. J Neurosci Res 78(1):29-37. (Pubitemid 39305151)