Structural determinants of Trk receptor specificities using BDNF-based neurotrophin chimeras

Journal of Neuroscience Research

Volumn 46, Issue 5, 1996, Pages 618-629

  Lai, Kwok On ^a   Glass, David J ^b   Geis, David ^b   Yancopoulos, George D ^b   Ip, Nancy Y ^a  

^a HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

^b REGENERON PHARMACEUTICALS INC   (United States)

Author keywords

brain derived neurotrophic factor; chimeric neurotrophins; nerve growth factor; receptor tyrosine kinase

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CHIMERIC PROTEIN; COMPLEMENTARY DNA; NERVE GROWTH FACTOR; NEUROTROPHIN; NEUROTROPHIN RECEPTOR; PROTEIN TYROSINE KINASE;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL SURVIVAL; COLONY FORMATION; FIBROBLAST CULTURE; GENE EXPRESSION; MOLECULAR CLONING; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; STRUCTURE ACTIVITY RELATION;

EID: 0029830402     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4547(19961201)46:5<618::AID-JNR10>3.0.CO;2-T     Document Type: Article

References (53)

1. Barde YA, Edgar D, Thoenen H (1982): Purification of a new neurotrophic factor from mammalian brain. EMBO J 1:549-553.
2. Barker PA, Shooter EM (1994): Disruption of NGF binding to the low affinity neurotrophin receptor p75LNTR reduces NGF binding to TrkA on PC12 cells. Neuron 13:203-215.
3. Berkemeier LR, Winslow JW, Kaplan DR, Nikolics K, Goeddel DV, Rosenthal A (1991): Neurotrophin-5: A novel neurotrophic factor that activates trk and trkB. Neuron 7:857-866.
4. Bothwell M (1995): Functional interactions of neurotrophins and neurotrophin receptors. Annu Rev Neurosci 18:223-253.
5. Chao MV, Bothwell MA, Ross AH, Koprowski H, Lanahan AA, Buck CR, Sehgal A (1986): Gene transfer and molecular cloning of the human NGF receptor. Science 232:518-521.
6. Cohen S, Levi-Montalcini R, Hamburger V (1954): A nerve growth-stimulating factor isolated from snake venom. Proc Natl Acad Sci USA 40:1014-1018.
7. Cordon-Cardo C, Tapley P, Jing S, Nanduri V, O'Rourke E, Lamballe F, Kovary K, Klein R, Jones KR, Reichardt LF, Barbacid M (1991): The trk tyrosine kinase mediates the mitogenic properties of the nerve growth factor and neurotrophin-3. Cell 66:173-183.
8. Davies AM (1994): The role of neurotrophins in the developing nervous system. J Neurobiol 25:1334-1348.
9. Davies AM, Minichiello L, Klein R (1995): Developmental changes in NT3 signalling via TrkA and TrkB in embryonic neurons. EMBO J 14:4482-4489.
10. Ernfors P, Ibanez CF, Ebendal T, Olson L, Persson H (1990): Molecular cloning and neurotrophic activities of a protein with structural similarities to nerve growth factor: Developmental and topographical expression in the brain. Proc Natl Acad Sci USA 87:5454-5458.
11. Glass DJ, Nye SH, Hantzopoulos P, Macchi MJ, Squinto SP, Goldfarb M, Yancopoulos GD (1991): TrkB mediates BDNF/NT-3 dependent survival and proliferation in fibroblasts lacking the low affinity NGF receptor. Cell 66:405-413.
12. Götz R, Raulf F, Schartl M (1992): Brain-derived neurotrophic factor is more conserved in structure and function than nerve growth factor during vertebrate evolution. J Neurochem 59:432-442.
13. Hallböök F, Ibáñez CF, Persson H (1991): Evolutionary studies of the nerve growth factor family reveal a novel member abundantly expressed in Xenopus ovary. Neuron 6:845-858.
14. Hantzopoulos PA, Suri C, Glass DJ, Goldfarb MP, Yancopoulos GD (1994): The low affinity NGF receptor, p75, can collaborate with each of the Trks to potentiate functional responses to the neurotrophins. Neuron 13:187-201.
15. Hohn A, Leibrock J, Bailey K, Barde YA (1990): Identification and characterization of a novel member of the nerve growth factor/ brain-derived neurotrophic factor family. Nature 344:339-341.
16. Ibáñez CF, Ebendal T, Persson H (1991): Chimeric molecules with multiple neurotrophic activities reveal structural elements determining the specificities of NGF and BDNF. EMBO J 10:2105-2110.
17. Ibáñez CF, Hag LL, Murray-Rust J, Persson H (1993): An extended surface of binding to trk tyrosine kinase receptors in NGF and BDNF allows the engineering of a multifunctional pan-neurotrophin. EMBO J 12:2281-2293.
18. Ilag LL, Lonnerberg P, Persson H, Ibáñez CF (1994): Role of variable β-hairpin loop in determining biological specificities in neurotrophin family. J Biol Chem 269:19941-19946.
19. Ip NY, Yancopoulos GD (1994): Neurotrophic factor receptors: Just like other growth factor and cytokine receptors? Curr Opin Neurobiol 4:400-405.
20. Ip NY, Yancopoulos GD (1996): The neurotrophins and CNTF: Two families of collaborative neurotrophic factors. Annu Rev Neurosci 19:491-515.
21. Ip NY, Ibáñez CF, Nye SH, McClain J, Jones PF, Gies DR, Belluscio L, Le Beau MM, Espinosa III R, Squinto SP, Persson H, Yancopoulos GD (1992): Mammalian neurotrophin-4: Structure, chromosomal localization, tissue distribution, and receptor specificity. Proc Natl Acad Sci USA 89:3060-3064.
22. Ip NY, Stitt TN, Tapley P, Klein R, Glass DJ, Fandl J, Greene LA, Barbacid M, Yancopoulos GD (1993): Similarities and differences in the way neurotrophins interact with the Trk receptors in neuronal and nonneuronal cells. Neuron 10:137-149.
23. Jing S, Tapley P, Barbacid M (1992): Nerve growth factor mediates signal transduction through Trk homodimer receptors. Neuron 9:1067-1079.
24. Jones KR, Reichardt LF (1990): Molecular cloning of a human gene that is a member of the nerve growth factor family. Proc Natl Acad Sci USA 87:8060-8064.
25. Kaplan DR, Hempstead BL, Martin-Zanca D, Chao MV, Parada LF (1991): The Trk protooncogene product: A signal transducing receptor for nerve growth factor. Science 252:552-558.
26. Klein R, Nanduri V, Jing S, Lamballe F, Tapley P, Bryant S, Cordon-Cardo C, Jones KR, Reichardt LF, Barbacid M (1991): The trkB tyrosine protein kinase is a receptor for brain-derived neurotrophic factor and neurotrophin-3. Cell 66:395-403.
27. Klein R, Lambelle F, Bryant S, Barbacid M (1992): The trkB tyrosine protein kinase is a receptor for neurotrophin-4. Neuron 8:947-956.
28. Klein R, Smeyne RJ, Wurst W, Long LK, Auerbach BA, Joyner AL, Barbacid M (1993): Targeted disruption of the trkB neurotrophin receptor gene results in nervous system lesions and neonatal death. Cell 75:113-122.
29. Klein R, Silos-Santiago I, Smeyne RJ, Lira SA, Brambilla R, Bryant S, Zhang L, Snider WD, Barbacid M (1994): Disruption of the neurotrophin-3 receptor gene trkC eliminates la muscle afferents and results in abnormal movements. Nature 368:249-251.
30. Kullander K, Ebendal T (1994): Neurotrophin-3 acquires NGF-like activity after exchange to five NGF amino acid residues: Molecular analysis of the sites in NGF mediating the specific interaction with the NGF high affinity receptor. J Neurosci Res 39:195-210.
31. Lambelle F, Klein R, Barbacid M (1991): TrkC, a new member of the Trk family of tyrosine protein kinases, is a receptor for neurotrophin-3. Cell 66:967-979.
32. Leibrock J, Lottspeich F, Hohn A, Hofer M, Hengerer B, Masiakowski P, Thoenen H, Barde YA (1989): Molecular cloning and expression of brain-derived neurotrophic factor. Nature 341:149-152.
33. Levi-Montalcini R (1987): The nerve growth factor: Thirty-five years later. EMBO J 6:2856-2867.
34. Levi-Montalcini R, Hamburger V (1953): A diffusible agent of mouse sarcoma, producing hyperplasia of sympathetic ganglia and hyperneurotization of viscera in the chick embryo. J Exp Zool 123:233-287.
35. Lindsay RM (1988): The role of neurotrophic factors in development, maintenance, and regeneration of sensory neurons. In Parnavelas JG, Stern CD, Stirling RV (eds): "The Making of the Nervous System." Oxford: Oxford University Press, pp 148-165.
36. Maisonpierre PC, Belluscio L, Squinto S, Ip NY, Furth ME, Lindsay RM, Yancopoulos GD (1990): Neurotrophin-3: A neurotrophic factor related to NGF and BDNF. Science 247:1446-51.
37. Maisonpierre PC, Le-Beau MM, Espinosa R III, Ip NY, Belluscio L, de la Monte SM, Squinto S, Furth ME, Yancopoulos GD (1991): Human and rat brain-derived neurotrophic factor and neurotrophin-3: Gene structures, distributions, and chromosomal localizations. Genomics 10:558-568.
38. Maisonpierre PC, Belluscio L, Conover JC, Yancopoulos GD (1992): Gene sequences of chicken BDNF and NT-3. DNA Seq 3:49-54.
39. Martin-Zanca D, Barbacid M, Parada LF (1990): Expression of the Trk protooncogene is restricted to the sensory cranial and spinal ganglia of neural crest origin in mouse development. Genes Dev 4:683-694.
40. McDonald N, Lapatto R, Murray-Rust J, Gunning J, Wlodawer A, Blundell TL (1991): New protein fold revealed by a 2.3-Å resolution crystal structure of nerve growth factor. Nature 354:411-414.
41. Meakin SO, Shooter EM (1992): The nerve growth factor family of receptors. Trends Nat Sci 15:323-331.
42. Meyer SL, Lang DM, Forbes ME, Knight E, Hirsch JD, Trusko SP, Scott RW (1994): Production and characterization of recombinant mouse brain-derived neurotrophic factor and rat neurotrophin-3 expressed in insect cells. J Neurochem 62:825-833.
43. Radeke MJ, Misko TP, Hsu H, Herzenberg LA, Shooter EM (1987): Gene transfer and molecular cloning of the rat nerve growth factor receptor. Nature 325:593-597.
44. Rosenthal A, Goeddel DV, Nguyen T, Lewis M, Shih A, Laramee GE, Nikolics K, Winslow JW (1990): Primary structure and biological activity of a novel human neurotrophic factor. Neuron 4:767-773.
45. Ruit KG, Osborne PA, Schmidt RE, Johnson EM, Snider WD (1990): Nerve growth factor regulates sympathetic ganglion cell morphology and survival in the adult mouse. J Neurosci 10:2412-2419.
46. Sanger F, Nicklen S, Coulson AR (1977): DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463-5467.
47. Smeyne RJ, Klein R, Schnapp A, Long LK, Bryant S, Lewin A, Lira SA, Barbacid M (1994): Severe sensory and sympathetic neuropathies in mice carrying a disrupted Trk/NGF receptor gene. Nature 368:246-249.
48. Snider WD (1994): Functions of the neurotrophins during nervous system development: What the knockouts are teaching us. Cell 77:627-638.
49. Soppet D, Escandon E, Maragos J, Middlemas DS, Reid SW, Blair J, Burton LE, Stanton BR, Kaplan DR, Hunter T, Nikolics K, Parada LF (1991): The neurotrophic factors brain-derived neurotrophic factor and neurotrophin-3 are ligands for the trkB tyrosine kinase receptor. Cell 65:895-903.
50. Squinto SP, Stitt TN, Aldrich TH, Davis S, Bianco SM, Radziejewski C, Glass DJ, Masiakowski P, Furth ME, Valenzuela DM, Di-Stefeno PS, Yancopoulos GD (1991): trkB encodes a functional receptor for brain-derived neurotrophic factor and neurotrophin-3 but not nerve growth factor. Cell 65:885-893.
51. Suter U, Angst C, Tien CL, Drinkwater CC, Lindsay RM, Shooter EM (1992): NGF/BDNF chimeric proteins: Analysis of neurotrophin specificity by homolog-scanning mutagenesis. J Neurosci 12:306-318.
52. Urfer R, Tsoulfas P, Soppet D, Escandon E, Parada LF, Presta LG (1994): The binding epitopes of neurotrophin-3 to its receptors TrkC and gp75 and the design of a multifunctional human neurotrophin. EMBO J 13:5896-5909.
53. Verdi JM, Ip NY, Yancopoulos GD, Anderson DJ (1994): Expression of trk in MAH cells lacking the p75 low-affinity nerve growth factor receptor is sufficient to permit nerve growth factor-induced differentiation to postmitotic neurons. Proc Natl Acad Sci USA 91:3949-3953.