Identification of active sequences in the L4a domain of laminin α5 promoting neurite elongation

Biochemistry

Volumn 51, Issue 24, 2012, Pages 4950-4958

  Katagiri, Fumihiko ^a   Sudo, Misuzu ^a   Hamakubo, Takayuki ^a   Hozumi, Kentaro ^a   Nomizu, Motoyoshi ^a   Kikkawa, Yamato ^a  

^a TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

293 CELLS; ACTIVE SEQUENCES; ACTIVE SITE; AMINO ACID RESIDUES; AMINO ACID SEQUENCE; BIOLOGICAL PROCESS; CELL ATTACHMENTS; CELLULAR INTERACTION; EXTRACELLULAR MATRIX PROTEIN; GLOBULAR DOMAINS; INHIBITION ASSAYS; INTEGRINS; LAMININ; LEC; MULTIPLE DOMAINS; NEURITE OUTGROWTH; NEURITES; PHEOCHROMOCYTOMA; RENAL FUNCTIONS; SYNTHETIC PEPTIDE;

AMINO ACIDS; CELL ADHESION; ELONGATION; MONOCLONAL ANTIBODIES; PEPTIDES;

RECOMBINANT PROTEINS;

ALPHA1 INTEGRIN; ARGININE; BETA1 INTEGRIN; FC RECEPTOR; LAMININ; MONOCLONAL ANTIBODY; NEURITE PROMOTING FACTOR; PHENYLALANINE; PROTEIN LAMININ ALPHA5; RECOMBINANT PROTEIN; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ADHESION; CELL ASSAY; CELL INTERACTION; CELL STRAIN; CELL STRAIN HEK293; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOUSE; MUTAGENESIS; NERVE CELL DIFFERENTIATION; NERVE ELONGATION; NERVE FIBER GROWTH; NONHUMAN; PEPTIDE SYNTHESIS; PHEOCHROMOCYTOMA CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; RAT;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES; CELL ADHESION; HEK293 CELLS; HUMANS; INTEGRINS; LAMININ; MICE; MOLECULAR SEQUENCE DATA; NEURITES; PC12 CELLS; PROTEIN STRUCTURE, TERTIARY; RATS; RECOMBINANT PROTEINS;

EID: 84862561544     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300214g     Document Type: Article

References (52)

1. Durbeej, M. (2010) Laminins. Cell Tissue Res. 339, 259-268.
2. Miner, J. H., Patton, B. L., Lentz, S. I., Gilbert, D. J., Snider, W. D., Jenkins, N. A., Copeland, N. G., and Sanes, J. R. (1997) The laminin α chains: Expression, developmental transitions, and chromosomal locations of α1-5, identification of heterotrimeric laminins 8-11, and cloning of a novel α3 isoform. J. Cell Biol. 137, 685-701. (Pubitemid 27200670)
3. Sorokin, L. M., Pausch, F., Frieser, M., Kroger, S., Ohage, E., and Deutzmann, R. (1997) Developmental regulation of the laminin α5 chain suggests a role in epithelial and endothelial cell maturation. Dev. Biol. 189, 285-300. (Pubitemid 27428370)
4. Libby, R. T., Champliaud, M. F., Claudepierre, T., Xu, Y., Gibbons, E. P., Koch, M., Burgeson, R. E., Hunter, D. D., and Brunken, W. J. (2000) Laminin expression in adult and developing retinae: Evidence of two novel CNS laminins. J. Neurosci. 20, 6517-6528.
5. Miner, J. H., Cunningham, J., and Sanes, J. R. (1998) Roles for laminin in embryogenesis: Exencephaly, syndactyly, and placentopathy in mice lacking the laminin α5 chain. J. Cell Biol. 143, 1713-1723. (Pubitemid 29006514)
6. Miner, J. H., and Li, C. (2000) Defective glomerulogenesis in the absence of laminin α5 demonstrates a developmental role for the kidney glomerular basement membrane. Dev. Biol. 217, 278-289. (Pubitemid 30060876)
7. Nguyen, N. M., Miner, J. H., Pierce, R. A., and Senior, R. M. (2002) Laminin α5 is required for lobar septation and visceral pleural basement membrane formation in the developing mouse lung. Dev. Biol. 246, 231-244. (Pubitemid 34775344)
8. Bolcato-Bellemin, A. L., Lefebvre, O., Arnold, C., Sorokin, L., Miner, J. H., Kedinger, M., and Simon-Assmann, P. (2003) Laminin α5 chain is required for intestinal smooth muscle development. Dev. Biol. 260, 376-390. (Pubitemid 36960086)
9. Fukumoto, S., Miner, J. H., Ida, H., Fukumoto, E., Yuasa, K., Miyazaki, H., Hoffman, M. P., and Yamada, Y. (2006) Laminin α5 is required for dental epithelium growth and polarity and the development of tooth bud and shape. J. Biol. Chem. 281, 5008-5016. (Pubitemid 43847764)
10. Coles, E. G., Gammill, L. S., Miner, J. H., and Bronner-Fraser, M. (2006) Abnormalities in neural crest cell migration in laminin α5 mutant mice. Dev. Biol. 289, 218-228. (Pubitemid 41804100)
11. Rebustini, I. T., Patel, V. N., Stewart, J. S., Layvey, A., Georges-Labouesse, E., Miner, J. H., and Hoffman, M. P. (2007) Laminin α5 is necessary for submandibular gland epithelial morphogenesis and influences FGFR expression through β1 integrin signaling. Dev. Biol. 308, 15-29. (Pubitemid 47087775)
12. Li, J., Tzu, J., Chen, Y., Zhang, Y. P., Nguyen, N. T., Gao, J., Bradley, M., Keene, D. R., Oro, A. E., Miner, J. H., and Marinkovich, M. P. (2003) Laminin-10 is crucial for hair morphogenesis. EMBO J. 22, 2400-2410. (Pubitemid 36604979)
13. Gao, J., DeRouen, M. C., Chen, C. H., Nguyen, M., Nguyen, N. T., Ido, H., Harada, K., Sekiguchi, K., Morgan, B. A., Miner, J. H., Oro, A. E., and Marinkovich, M. P. (2008) Laminin-511 is an epithelial message promoting dermal papilla development and function during early hair morphogenesis. Genes Dev. 22, 2111-2124.
14. Nguyen, N. M., Kelley, D. G., Schlueter, J. A., Meyer, M. J., Senior, R. M., and Miner, J. H. (2005) Epithelial laminin α5 is necessary for distal epithelial cell maturation, VEGF production, and alveolization in the developing murine lung. Dev. Biol. 282, 111-125. (Pubitemid 40779932)
15. Timpl, R., Tisi, D., Talts, J. F., Andac, Z., Sasaki, T., and Hohenester, E. (2000) Structure and function of laminin LG modules. Matrix Biol. 19, 309-317. (Pubitemid 30665654)
16. Suzuki, N., Yokoyama, F., and Nomizu, M. (2005) Functional sites in the laminin α chains. Connect. Tissue Res. 46, 142-152.
17. Kikkawa, Y., Sasaki, T., Nguyen, M. T., Nomizu, M., Mitaka, T., and Miner, J. H. (2007) The LG1-3 tandem of laminin α5 harbors the binding sites of Lutheran/basal cell adhesion molecule and α3β1/ α6β1 integrins. J. Biol. Chem. 282, 14853-14860. (Pubitemid 47093350)
18. Ido, H., Nakamura, A., Kobayashi, R., Ito, S., Li, S., Futaki, S., and Sekiguchi, K. (2007) The requirement of the glutamic acid residue at the third position from the carboxyl termini of the laminin γ chains in integrin binding by laminins. J. Biol. Chem. 282, 11144-11154. (Pubitemid 47100774)
19. Yu, H., and Talts, J. F. (2003) β1 integrin and α-dystroglycan binding sites are localized to different laminin-G-domain-like (LG) modules within the laminin α5 chain G domain. Biochem. J. 371, 289-299. (Pubitemid 36547611)
20. Kikkawa, Y., Virtanen, I., and Miner, J. H. (2003) Mesangial cells organize the glomerular capillaries by adhering to the G domain of laminin α5 in the glomerular basement membrane. J. Cell Biol. 161, 187-196. (Pubitemid 36459090)
21. Kikkawa, Y ., and Miner, J. H. (2006) Molecular dissection of laminin α5 in vivo reveals separable domain-specific roles in embryonic development and kidney function. Dev. Biol. 296, 265-277. (Pubitemid 44061768)
22. Nishimune, H., Valdez, G., Jarad, G., Moulson, C. L., Muller, U., Miner, J. H., and Sanes, J. R. (2008) Laminins promote postsynaptic maturation by an autocrine mechanism at the neuromuscular junction. J. Cell Biol. 182, 1201-1215.
23. Aumailley, M., Bruckner-Tuderman, L., Carter, W. G., Deutzmann, R., Edgar, D., Ekblom, P., Engel, J., Engvall, E., Hohenester, E., Jones, J. C., Kleinman, H. K., Marinkovich, M. P., Martin, G. R., Mayer, U., Meneguzzi, G., Miner, J. H., Miyazaki, K., Patarroyo, M., Paulsson, M., Quaranta, V., Sanes, J. R., Sasaki, T., Sekiguchi, K., Sorokin, L. M., Talts, J. F., Tryggvason, K., Uitto, J., Virtanen, I., von der Mark, K., Wewer, U. M., Yamada, Y., and Yurchenco, P. D. (2005) A simplified laminin nomenclature. Matrix Biol. 24, 326-332. (Pubitemid 41021635)
24. Miner, J. H., Lewis, R. M., and Sanes, J. R. (1995) Molecular cloning of a novel laminin chain, α5, and widespread expression in adult mouse tissues. J. Biol. Chem. 270, 28523-28526.
25. Nielsen, P. K., and Yamada, Y. (2001) Identification of cellbinding sites on the laminin α5 N-terminal domain by site-directed mutagenesis. J. Biol. Chem. 276, 10906-10912. (Pubitemid 38089268)
26. Nomizu, M., Yokoyama, F., Suzuki, N., Okazaki, I., Nishi, N., Ponce, M. L., Kleinman, H. K., Yamamoto, Y., Nakagawa, S., and Mayumi, T. (2001) Identification of homologous biologically active sites on the N-terminal domain of laminin α chains. Biochemistry 40, 15310-15317. (Pubitemid 33151945)
27. Sasaki, T., and Timpl, R. (2001) Domain IVa of laminin α5 chain is cell-adhesive and binds β1 and αVβ3 integrins through Arg-Gly-Asp. FEBS Lett. 509, 181-185. (Pubitemid 34015939)
28. Colognato, H., and Yurchenco, P. D. (2000) Form and function: The laminin family of heterotrimers. Dev. Dyn. 218, 213-234.
29. Garbe, J. H., Gohring, W., Mann, K., Timpl, R., and Sasaki, T. (2002) Complete sequence, recombinant analysis and binding to laminins and sulphated ligands of the N-terminal domains of laminin α3B and α5 chains. Biochem. J. 362, 213-221.
30. Hussain, S. A., Carafoli, F., and Hohenester, E. (2011) Determinants of laminin polymerization revealed by the structure of the α5 chain amino-terminal region. EMBO Rep. 12, 276-282.
31. Round, J., and Stein, E. (2007) Netrin signaling leading to directed growth cone steering. Curr. Opin. Neurobiol. 17, 15-21. (Pubitemid 46237743)
32. Nakagawa, M., Miyagoe-Suzuki, Y., Ikezoe, K., Miyata, Y., Nonaka, I., Harii, K., and Takeda, S. (2001) Schwann cell myelination occurred without basal lamina formation in laminin α2 chain-null mutant (dy3K/dy3K) mice. Glia 35, 101-110.
33. Nomizu, M., Kuratomi, Y., Malinda, K. M., Song, S. Y., Miyoshi, K., Otaka, A., Powell, S. K., Hoffman, M. P., Kleinman, H. K., and Yamada, Y. (1998) Cell binding sequences in mouse laminin α1 chain. J. Biol. Chem. 273, 32491-32499. (Pubitemid 28557624)
34. Tomaselli, K. J., Doherty, P., Emmett, C. J., Damsky, C. H., Walsh, F. S., and Reichardt, L. F. (1993) Expression of β1 integrins in sensory neurons of the dorsal root ganglion and their functions in neurite outgrowth on two laminin isoforms. J. Neurosci. 13, 4880-4888.
35. Culley, B., Murphy, J., Babaie, J., Nguyen, D., Pagel, A., Rousselle, P., and Clegg, D. O. (2001) Laminin-5 promotes neurite outgrowth from central and peripheral chick embryonic neurons. Neurosci. Lett. 301, 83-86. (Pubitemid 32206691)
36. Smith, B. E., Bradshaw, A. D., Choi, E. S., Rouselle, P., Wayner, E. A., and Clegg, D. O. (1996) Human SY5Y neuroblastoma cell interactions with laminin isoforms: Neurite outgrowth on laminin-5 is mediated by integrin α3β1. Cell Adhes. Commun. 3, 451-462. (Pubitemid 26193834)
37. Zhang, Z., Tarone, G., and Turner, D. C. (1993) Expression of integrin α1β1 is regulated by nerve growth factor and dexamethasone in PC12 cells. Functional consequences for adhesion and neurite outgrowth. J. Biol. Chem. 268, 5557-5565. (Pubitemid 23090877)
38. Colognato-Pyke, H., O'Rear, J. J., Yamada, Y., Carbonetto, S., Cheng, Y. S., and Yurchenco, P. D. (1995) Mapping of network-forming, heparin-binding, and α1β1 integrin-recognition sites within the α-chain short arm of laminin-1. J. Biol. Chem. 270, 9398-9406.
39. Kikkawa, Y., Sudo, R., Kon, J., Mizuguchi, T., Nomizu, M., Hirata, K., and Mitaka, T. (2008) Laminin α5 mediates ectopic adhesion of hepatocellular carcinoma through integrins and/or Lutheran/basal cell adhesion molecule. Exp. Cell Res. 314, 2579-2590.
40. Makino, M., Okazaki, I., Kasai, S., Nishi, N., Bougaeva, M., Weeks, B. S., Otaka, A., Nielsen, P. K., Yamada, Y., and Nomizu, M. (2002) Identification of cell binding sites in the laminin α5-chain G domain. Exp. Cell Res. 277, 95-106. (Pubitemid 34948343)
41. Gu, J., Sumida, Y., Sanzen, N., and Sekiguchi, K. (2001) Laminin-10/11 and fibronectin differentially regulate integrin-dependent Rho and Rac activation via p130(Cas)-CrkII-DOCK180 pathway. J. Biol. Chem. 276, 27090-27097.
42. Kato, K., Utani, A., Suzuki, N., Mochizuki, M., Yamada, M., Nishi, N., Matsuura, H., Shinkai, H., and Nomizu, M. (2002) Identification of neurite outgrowth promoting sites on the laminin α3 chain G domain. Biochemistry 41, 10747-10753. (Pubitemid 34971050)
43. Ichikawa, N., Kasai, S., Suzuki, N., Nishi, N., Oishi, S., Fujii, N., Kadoya, Y., Hatori, K., Mizuno, Y., Nomizu, M., and Arikawa- Hirasawa, E. (2005) Identification of neurite outgrowth active sites on the laminin α4 chain G domain. Biochemistry 44, 5755-5762. (Pubitemid 40525112)
44. Urushibata, S., Katagiri, F., Takaki, S., Yamada, Y., Fujimori, C., Hozumi, K., Kikkawa, Y., Kadoya, Y., and Nomizu, M. (2009) Biologically active sequences in the mouse laminin α3 chain G domain. Biochemistry 48, 10522-10532.
45. Hozumi, K., Akizuki, T., Yamada, Y., Hara, T., Urushibata, S., Katagiri, F., Kikkawa, Y., and Nomizu, M. (2010) Cell adhesive peptide screening of the mouse laminin α1 chain G domain. Arch. Biochem. Biophys. 503, 213-222.
46. Urushibata, S., Hozumi, K., Ishikawa, M., Katagiri, F., Kikkawa, Y., and Nomizu, M. (2010) Identification of biologically active sequences in the laminin α2 chain G domain. Arch. Biochem. Biophys. 497, 43-54.
47. Son, Y. J., Scranton, T. W., Sunderland, W. J., Baek, S. J., Miner, J. H., Sanes, J. R., and Carlson, S. S. (2000) The synaptic vesicle protein SV2 is complexed with an α5-containing laminin on the nerve terminal surface. J. Biol. Chem. 275, 451-460. (Pubitemid 30039005)
48. Dong, M., Yeh, F., Tepp, W. H., Dean, C., Johnson, E. A., Janz, R., and Chapman, E. R. (2006) SV2 is the protein receptor for botulinum neurotoxin A. Science 312, 592-596.
49. Mochizuki, M., Kadoya, Y., Wakabayashi, Y., Kato, K., Okazaki, I., Yamada, M., Sato, T., Sakairi, N., Nishi, N., and Nomizu, M. (2003) Laminin-1 peptide-conjugated chitosan membranes as a novel approach for cell engineering. FASEB J. 17, 875-877.
50. Mochizuki, M., Yamagata, N., Philp, D., Hozumi, K., Watanabe, T., Kikkawa, Y., Kadoya, Y., Kleinman, H. K., and Nomizu, M. (2007) Integrin-dependent cell behavior on ECM peptide-conjugated chitosan membranes. Biopolymers 88, 122-130. (Pubitemid 46657978)
51. Hozumi, K., Otagiri, D., Yamada, Y., Sasaki, A., Fujimori, C., Wakai, Y., Uchida, T., Katagiri, F., Kikkawa, Y., and Nomizu, M. (2010) Cell surface receptor-specific scaffold requirements for adhesion to laminin-derived peptide-chitosan membranes. Biomaterials 31, 3237-3243.
52. Hozumi, K., Yamagata, N., Otagiri, D., Fujimori, C., Kikkawa, Y., Kadoya, Y., and Nomizu, M. (2009) Mixed peptide-chitosan membranes to mimic the biological activities of a multifunctional laminin α1 chain LG4 module. Biomaterials 30, 1596-1603.