The hippocampal laminin matrix is dynamic and critical for neuronal survival

Molecular Biology of the Cell

Volumn 14, Issue 7, 2003, Pages 2665-2676

  Chen, Zu Lin ^a   Indyk, Justin A ^b   Strickland, Sidney ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXCITOTOXIN; KAINIC ACID; LAMININ; LAMININ 1; LAMININ 10; MESSENGER RNA; PLASMIN; PROTEIN ANTIBODY; SCLEROPROTEIN; UNCLASSIFIED DRUG;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DISRUPTION; CELL SURVIVAL; CELL VIABILITY; EXTRACELLULAR MATRIX; HIPPOCAMPUS; MALE; MOUSE; NERVE CELL; NERVE CELL NECROSIS; NERVE DEGENERATION; NERVE GROWTH; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION;

ANIMALS; BINDING, COMPETITIVE; CELL ADHESION; CELL SURVIVAL; EXTRACELLULAR MATRIX; HIPPOCAMPUS; KAINIC ACID; LAMININ; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE DEGENERATION; NEURONS; PLASMIN; PLASMINOGEN; PROTEIN BINDING;

ANIMALIA; HIPPOCAMPUS HIPPOCAMPUS;

EID: 0037769931     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E02-12-0832     Document Type: Article

References (52)

1. Baranes, D., Lederfein, D., Huan, Y., Chen, M., Bailey, C.H., and Kandel, E.R. (1998). Tissue plasminogen activator contributes to the late phase of LTP and to synaptic growth in the hippocampal mossy fiber pathway. Neuron 21, 813-825.
2. Boudreau, N., Sympson, C.J., Werb, Z., and Bissell, M.J. (1995). Suppression of ICE and apoptosois in mammary epithelial cells by extracellular matrix. Science 267, 891-893.
3. Bugge, T.H., Flick, M.J., Daugherty, C.C., and Degen, J.L. (1995). Plasminogen deficiency causes severe thrombosis but is compatible with development and reproduction. Genes Dev. 9, 794-807.
4. Carmeliet, P., Schoonjans, L., Kieckens, L., Ream, B., Degen, J.L., Bronson, R., De Vos, J.J., van den Oord, D., Collen, D., and Mulligan, R.C. (1994). Physiological consequences of loss of plasminogen activator gene function in mice. Nature 368, 419-424.
5. Chen, Z.-L., Indyk, J.A., Bugge, T.H., Kombrinck, K.W., Degen, J.L., and Strickland, S. (1999). Neuronal death and blood-brain barrier breakdown after excitotoxic injury are independent processes. J. Neurosci. 19, 9813-9820.
6. Chen, Z.-L., and Strickland, S. (1997). Neuronal death in the hippocampus is promoted by plasmin-catalyzed degradation of laminin. Cell 91, 917-925.
7. Chen, Z.L., et al. (1995). Expression and activity-dependent changes of a novel limbic-serine protease gene in the hippocampus. J. Neurosci. 15, 5088-5097.
8. Colognato, H., and Yurchenco, P.D. (2000). Form and function: the laminin family of heterotrimers. Dev. Dynamics 218, 213-234.
9. Coucouvanis, E., and Martin, G.R. (1995). Signals for death and survival: a two-step mechanism for cavitation in the vertebrate embryo. Cell 83, 279-287.
10. Coyle, J.T., Molliver, M.E., and Kuhar, M.J. (1978). In situ injection of kainic acid: a new method for selectively lesioning neural cell bodies while sparing axons of passage. J. Comp. Neurol. 180, 301-323.
11. Doi, M., Thyboll, J., Kortesmaa, J., Jansson, K., Iivanainen, A., Parvardeh, M., Timpl, R., Hedin, U., Swedenborg, J., and Tryggvason, K. (2002). Recombinant human laminin-10 (α5β1γ1). Production, purification, and migration-promoting activity on vascular endothelial cells. J. Biol. Chem. 277, 12741-12748.
12. Ernsberger, U., Edgar, D., and Rohrer, H. (1989). The survival of early chick sympathetic neurons in vitro is dependent on a suitable substrate but independent of NGF. Dev. Biol. 135, 250-262.
13. Ferletta, M., and Ekblom, P. (1999). Identification of laminin-10/11 as a strong cell adhesive complex for a normal and a malignant human epithelial cell line. J. Cell Sci. 112, 1-10.
14. Frisch, S.M., and Screaton, R.A. (2001). Anoikis mechanisms. Curr. Opin. Cell Biol. 13, 555-562.
15. Grimpe, B., Dong, S., Doller, C., Temple, K., Malouf, A.T., and Silver, J. (2002). The critical role of basement membrane-independent laminin gamma1 chain during axon regeneration in the CNS. J. Neurosci. 22, 3144-3160.
16. Gu, Y., Sorokin, L., Durbeej, M., Hjalt, T., Jonsson, J.I., and Ekblom, M. (1999). Characterization of bone marrow laminins and identification of alpha5-containing laminins as adhesive proteins for multipotent hematopoietic FDCP-Mix cells. Blood 93, 2533-2542.
17. Gualandris, A., Jones, T.E., Strickland, S., and Tsirka, S.E. (1996). Membrane depolarization induces calcium-dependent secretion of tissue plasminogen activator. J. Neurosci. 16, 2220-2225.
18. Hagg, T., Muir, D., Engvall, E., Varon, S., and Manthorpe, M. (1989). Laminin-like antigen in rat CNS neurons: distribution and changes upon brain injury and nerve growth factor treatment. Neuron 3, 721-732.
19. Hagg, T., Portera-Cailliau, C., Jucker, M., and Engvall, E. (1997). Laminins of the adult mammalian CNS; laminin-alpha2 (merosin M-) chain immunoreactivity is associated with neuronal processes. Brain Res. 764, 17-27.
20. Hayman, E.G., Pierschbacher, M.D., and Ruoslahti, E. (1985). Detachment of cells from culture substrate by soluble fibronectin peptides. J. Cell Biol. 100, 1948-1954.
21. Huang, Y.-Y., et al. (1996). Mice lacking the gene encoding tissue-type plasminogen activator show a selective interference with late-phase long-term potentiation in both Schaffer collateral and mossy fiber pathways. Proc. Natl. Acad. Sci. USA 93, 8699-8704.
22. Indyk, J.A., Chen, Z.-L., and Strickland, S. (2003). Laminin chain expression suggests that laminin-10 is a major isoform in the mouse hippocampus and is degraded by the tPA/plasmin system during excitotoxic injury. Neuroscience 116, 359-371.
23. Jucker, M., Tian, M., and Ingram, D.K. (1996). Laminins in the adult and aged brain. Mol. Chem. Neuropathol. 28, 209-218.
24. Kikkawa, Y., Sanzen, N., Fujiwara, H., Sonnenberg, A., and Sekiguchi, K. (2000). Integrin binding specificity of laminin-10/11: laminin-10/11 are recognized by α3β1, α6β1 and α6β4 integrins. J. Cell Sci. 113, 869-876.
25. Levey, A.I., Kitt, C.A., Simonds, W.F., Price, D.L., and Brann, M.R. (1991). Identification and localization of muscarinic acetylcholine receptor proteins in brain with subtype-specific antibodies. J. Neurosci. 11, 3218-3226.
26. Liesi, P., Fried, G., and Stewart, R.R. (2001). Neurons and glial cells of the embryonic human brain and spinal cord express multiple and distinct isoforms of laminin. J. Neurosci. Res. 64, 144-167.
27. Luckenbill-Edds, L. (1997). Laminin and the mechanism of neuronal outgrowth. Brain Res. Brain Res. Rev. 23, 1-27.
28. Lukashev, M.E., and Werb, Z. (1998). ECM signalling: orchestrating cell behaviour and misbehaviour. Trends Cell Biol. 8, 437-441.
29. Madani, R., Hulo, S., Toni, N., Madani, H., Steimer, T., Muller, D., and Vassalli, J.-D. (1999). Enhanced hippocampal long-term potentiation and learning by increased neuronal expression of tissue-type plasminogen activator in transgenic mice. EMBO J. 18, 3007-3012.
30. Matsuoka, Y., Kitamura, Y., and Taniguchi, T. (1998). Induction of plasminogen in rat hippocampal pyramidal neurons by kainic acid. Neurosci. Lett. 252, 119-122.
31. Meredith, J., Fazeli, J.B., and Schwartz, M.A. (1993). The extracellular matrix as a cell survival factor. Mol. Biol. Cell 4, 953-961.
32. Miner, J.H., Cunningham, J., and Sanes, J.R. (1998). Roles for laminin in embryogenesis: exencephaly, syndactyly, and placentopathy in mice lacking the laminin alpha5 chain. J. Cell Biol. 143, 1713-1723.
33. Müller, C.M., and Griesinger, C.B. (1998). Tissue plasminogen activator mediates reverse occlusion plasticity in visual cortex. Nat. Neurosci. 1, 47-53.
34. Murtomaki, S., Risteli, J., Risteli, L., Koivisto, U.M., Johansson, S., and Liesi, P. (1992). Laminin and its neurite outgrowth-promoting domain in the brain in Alzheimer's disease and Down's syndrome patients. J. Neurosci. Res. 32, 261-273.
35. Nagai, N., Urano, T., Endo, A., Takahashi, H., Takada, Y., and Takada, A. (1999). Neuronal degeneration and a decrease in laminin-like immunoreactivity is associated with elevated tissue-type plasminogen activator in the rat hippocampus after kainic acid injection. Neurosci. Res. 33, 147-154.
36. Nakagami, Y., Abe, K., Nishiyama, N., and Matsuki, N. (2000). Laminin degradation by plasmin regulates long-term potentiation. J. Neurosci. 20, 2003-2010.
37. Nielsen, P.K., and Yamada, Y. (2001). Identification of cell-binding sites on the laminin alpha 5 N-terminal domain by site-directed mutagenesis. J. Biol. Chem. 276, 10906-10912.
38. Noakes, P.G., Gautam, M., Mudd, J., Sanes, J.R., and Merlie, J.P. (1995). Aberrant differentiation of neuromuscular junctions in mice lacking s-laminin/laminin beta 2. Nature 374, 258-262.
39. Parmer, R.J., Mahata, M., Mahata, S., Sebald, M.T., O'Connor, D.T., and Miles, L.A. (1997). Tissue plasminogen activator (t-PA) is targeted to the regulated secretory pathway. Catecholamine storage vesicles as a reservoir for the rapid release of t-PA. J. Biol. Chem. 272, 1976-1982.
40. Patton, B.L., Chiu, A.Y., and Sanes, J.R. (1998). Synaptic laminin prevents glial entry into the synaptic cleft. Nature 393, 698-701.
41. Patton, B.L., Cunningham, J.M., Thyboll, J., Kortesmaa, J., Westerblad, H., Edstrom, L., Tryggvason, K., and Sanes, J.R. (2001). Properly formed but improperly localized synaptic specializations in the absence of laminin alpha4. Nat. Neurosci. 4, 597-604.
42. Ploplis, V.A., Carmeliet, P., Vazirzadeh, S., Van Vlaenderen, I., Moons, L., Plow, E.F., and Collen, D. (1995). Effects of disruption of the plasminogen gene on thrombosis, growth and health in mice. Circulation 92, 2585-2593.
43. Pouliot, N., Connolly, L.M., Moritz, R.L., Simpson, R.J., and Burgess, A.W. (2000). Colon cancer cells adhesion and spreading on autocrine laminin-10 is mediated by multiple integrin receptors and modulated by EGF receptor stimulation. Exp. Cell Res. 261, 360-371.
44. Ruoslahti, E. (1996). RGD and other recognition sequences for integrins. Annu. Rev. Cell Dev. Biol. 12, 697-715.
45. Sanes, J.R., and Lichtman, J.W. (2001). Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat. Rev. Neurosci. 2, 791-805.
46. Sappino, A.-P., Madani, R., Huarte, J., Belin, D., Kiss, J.Z., Wohlwend, A., and Vassalli, J.-D. (1993). Extracellular proteolysis in the adult murine brain. J. Clin. Investig. 92, 679-685.
47. Schmued, L.C., and Hopkins, K.J. (2000). Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res. 874, 123-130.
48. Tani, T., Lehto, V.P., and Virtanen, I. (1999). Expression of laminins 1 and 10 in carcinoma cells and comparison of their roles in cell adhesion. Exp. Cell Res. 248, 115-121.
49. Tian, M., Hagg, T., Denisova, N., Knusel, B., Engvall, E., and Jucker, M. (1997). Laminin-alpha2 chain-like antigens in CNS dendritic spines. Brain Res. 764, 28-38.
50. Tsirka, S.E., Gualandris, A., Amaral, D.G., and Strickland, S. (1995). Excitotoxin-induced neuronal degerneration and seizure are mediated by tissue plasminogen activator. Nature 377, 340-344.
51. Tsirka, S.E., Rogove, A.D., Bugge, T.H., Degen, J.L., and Strickland, S. (1997). An extracellular proteolytic cascade promotes neuronal degeneration in the mouse hippocampus. J. Neurosci. 17, 543-552.
52. Venstrom, K.A., and Reichardt, L.F. (1993). Extracellular matrix. 2: role of extracellular matrix molecules and their receptors in the nervous system. FASEB J. 7, 996-1003.