Kinesin KIF4A transports integrin β1 in developing axons of cortical neurons

Molecular and Cellular Neuroscience

Volumn 63, Issue , 2014, Pages 60-71

  Heintz, Tristan G ^a   Heller, Janosch P ^a   Zhao, Rongrong ^a   Caceres, Alfredo ^b   Eva, Richard ^a   Fawcett, James W ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b INSTITUTO DE INVESTIGACIÓN MÉDICA MERCEDES Y MARTÍN FERREYRA   (Argentina)

Author keywords

Axon; Axon growth; Axon transport; Integrin; Kinesin; Trafficking

Indexed keywords

BETA1 INTEGRIN; KINESIN; KINESIN KIF4A; LAMININ; RIBOSOME PROTEIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN CELL; CELL ELONGATION; CELL SURVIVAL; COMPARATIVE STUDY; DOWN REGULATION; FEMALE; GENE OVEREXPRESSION; GENETIC TRANSFECTION; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; IN VITRO STUDY; NERVE FIBER; NERVE FIBER GROWTH; NERVE FIBER TRANSPORT; NEURITE; NONHUMAN; PROTEIN TRANSPORT; RAT; REGENERATIVE ABILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ANIMAL; BRAIN CORTEX; CYTOLOGY; EMBRYOLOGY; GENETICS; METABOLISM; SPRAGUE DAWLEY RAT;

ANIMALS; ANTIGENS, CD29; APOPTOSIS; AXONAL TRANSPORT; AXONS; CEREBRAL CORTEX; KINESIN; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84908352136     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2014.09.003     Document Type: Article

References (54)

1. Abe N., Almenar-Queralt A., Lillo C., Shen Z., Lozach J., Briggs S.P., Williams D.S., Goldstein L.S., Cavalli V. Sunday driver interacts with two distinct classes of axonal organelles. J. Biol. Chem. 2009, 284:34628-34639.
2. Andrews M.R., Czvitkovich S., Dassie E., Vogelaar C.F., Faissner A., Blits B., Gage F.H., Ffrench-Constant C., Fawcett J.W. Alpha9 integrin promotes neurite outgrowth on tenascin-C and enhances sensory axon regeneration. J. Neurosci. 2009, 29:5546-5557.
3. Babayan A.H., Kramar E.A., Barrett R.M., Jafari M., Haettig J., Chen L.Y., Rex C.S., Lauterborn J.C., Wood M.A., Gall C.M., Lynch G. Integrin dynamics produce a delayed stage of long-term potentiation and memory consolidation. J. Neurosci. 2012, 32:12854-12861.
4. Bi X., Lynch G., Zhou J., Gall C.M. Polarized distribution of alpha5 integrin in dendrites of hippocampal and cortical neurons. J. Comp. Neurol. 2001, 435:184-193.
5. Bisbal M., Wojnacki J., Peretti D., Ropolo A., Sesma J., Jausoro I., Caceres A. KIF4 mediates anterograde translocation and positioning of ribosomal constituents to axons. J. Biol. Chem. 2009, 284:9489-9497.
6. Blackmore M., Letourneau P.C. L1, beta1 integrin, and cadherins mediate axonal regeneration in the embryonic spinal cord. J. Neurobiol. 2006, 66:1564-1583.
7. Boiko T., Vakulenko M., Ewers H., Yap C.C., Norden C., Winckler B. Ankyrin-dependent and -independent mechanisms orchestrate axonal compartmentalization of L1 family members neurofascin and L1/neuron-glia cell adhesion molecule. J. Neurosci. 2007, 27:590-603.
8. Bolte S., Cordelieres F.P. A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 2006, 224:213-232.
9. Bradke F., Fawcett J.W., Spira M.E. Assembly of a new growth cone after axotomy: the precursor to axon regeneration. Nat. Rev. Neurosci. 2012, 13:183-193.
10. Bridgewater R.E., Norman J.C., Caswell P.T. Integrin trafficking at a glance. J. Cell Sci. 2012, 125:3695-3701.
11. Caceres A., Ye B., Dotti C.G. Neuronal polarity: demarcation, growth and commitment. Curr. Opin. Cell Biol. 2012, 24:547-553.
12. Charrier C., Machado P., Tweedie-Cullen R.Y., Rutishauser D., Mansuy I.M., Triller A. A crosstalk between beta1 and beta3 integrins controls glycine receptor and gephyrin trafficking at synapses. Nat. Neurosci. 2010, 13:1388-1395.
13. Chew D.J., Fawcett J.W., Andrews M.R. The challenges of long-distance axon regeneration in the injured CNS. Prog. Brain Res. 2012, 201:253-294.
14. Cingolani L.A., Thalhammer A., Yu L.M., Catalano M., Ramos T., Colicos M.A., Goda Y. Activity-dependent regulation of synaptic AMPA receptor composition and abundance by beta3 integrins. Neuron 2008, 58:749-762.
15. Dillman A.A., Hauser D.N., Gibbs J.R., Nalls M.A., McCoy M.K., Rudenko I.N., Galter D., Cookson M.R. mRNA expression, splicing and editing in the embryonic and adult mouse cerebral cortex. Nat. Neurosci. 2013, 16:499-506.
16. Donaldson J.G., Jackson C.L. ARF family G proteins and their regulators: roles in membrane transport, development and disease. Nat. Rev. Mol. Cell Biol. 2011, 12:362-375.
17. Dotti C.G., Poo M.M. Neuronal polarization: building fences for molecular segregation. Nat. Cell Biol. 2003, 5:591-594.
18. Eva R., Fawcett J. Integrin signalling and traffic during axon growth and regeneration. Curr. Opin. Neurobiol. 2014, 27C:179-185.
19. Eva R., Dassie E., Caswell P.T., Dick G., Ffrench-Constant C., Norman J.C., Fawcett J.W. Rab11 and its effector Rab coupling protein contribute to the trafficking of {beta}1 integrins during axon growth in adult dorsal root ganglion neurons and PC12 cells. J. Neurosci. 2010, 30:11654-11669.
20. Eva R., Crisp S., Marland J.R., Norman J.C., Kanamarlapudi V., Ffrench-Constant C., Fawcett J.W. ARF6 directs axon transport and traffic of integrins and regulates axon growth in adult DRG neurons. J. Neurosci. 2012, 32:10352-10364.
21. Farias G.G., Cuitino L., Guo X., Ren X., Jarnik M., Mattera R., Bonifacino J.S. Signal-mediated, AP-1/clathrin-dependent sorting of transmembrane receptors to the somatodendritic domain of hippocampal neurons. Neuron 2012, 75:810-823.
22. Franker M.A., Hoogenraad C.C. Microtubule-based transport - basic mechanisms, traffic rules and role in neurological pathogenesis. J. Cell Sci. 2013, 126:2319-2329.
23. Franssen E.H.P., Zhao R.R., Kanamarlapudi V., Hoogenraad C.C., Eva R., Fawcett J.W. Exclusion of integrins from CNS axons is regulated by the AIS and Arf6 activation 2014, (submitted for publication).
24. Gardiner N.J., Fernyhough P., Tomlinson D.R., Mayer U., von der M.H., Streuli C.H. Alpha7 integrin mediates neurite outgrowth of distinct populations of adult sensory neurons. Mol. Cell. Neurosci. 2005, 28:229-240.
25. Gonzalez-Billault C., Munoz-Llancao P., Henriquez D.R., Wojnacki J., Conde C., Caceres A. The role of small GTPases in neuronal morphogenesis and polarity. Cytoskeleton (Hoboken) 2012, 69:464-485.
26. Grooms S.Y., Terracio L., Jones L.S. Anatomical localization of beta 1 integrin-like immunoreactivity in rat brain. Exp. Neurol. 1993, 122:253-259.
27. Gunawardena S., Goldstein L.S. Polyglutamine diseases and transport problems: deadly traffic jams on neuronal highways. Arch. Neurol. 2005, 62:46-51.
28. Gupton S.L., Gertler F.B. Integrin signaling switches the cytoskeletal and exocytic machinery that drives neuritogenesis. Dev. Cell 2010, 18:725-736.
29. Hirokawa N., Noda Y. Intracellular transport and kinesin superfamily proteins, KIFs: structure, function, and dynamics. Physiol. Rev. 2008, 88:1089-1118.
30. Hsu V.W., Prekeris R. Transport at the recycling endosome. Curr. Opin. Cell Biol. 2010, 22:528-534.
31. Hu F., Strittmatter S.M. The N-terminal domain of Nogo-A inhibits cell adhesion and axonal outgrowth by an integrin-specific mechanism. J. Neurosci. 2008, 28:1262-1269.
32. Jenkins B., Decker H., Bentley M., Luisi J., Banker G. A novel split kinesin assay identifies motor proteins that interact with distinct vesicle populations. J. Cell Biol. 2012, 198:749-761.
33. Kapitein L.C., Hoogenraad C.C. Which way to go? Cytoskeletal organization and polarized transport in neurons. Mol. Cell. Neurosci. 2011, 46:9-20.
34. Margadant C., Monsuur H.N., Norman J.C., Sonnenberg A. Mechanisms of integrin activation and trafficking. Curr. Opin. Cell Biol. 2011, 23:607-614.
35. Marland J.R., Pan D., Buttery P.C. Rac GTPase-activating protein (Rac GAP) α1-Chimaerin undergoes proteasomal degradation and is stabilized by diacylglycerol signaling in neurons. J. Biol. Chem. 2011, 286(1):199-207.
36. Midorikawa R., Takei Y., Hirokawa N. KIF4 motor regulates activity-dependent neuronal survival by suppressing PARP-1 enzymatic activity. Cell 2006, 125:371-383.
37. Mortillo S., Elste A., Ge Y., Patil S.B., Hsiao K., Huntley G.W., Davis R.L., Benson D.L. Compensatory redistribution of neuroligins and N-cadherin following deletion of synaptic beta1-integrin. J. Comp. Neurol. 2012, 520:2041-2052.
38. Namba T., Nakamuta S., Funahashi Y., Kaibuchi K. The role of selective transport in neuronal polarization. Dev. Neurobiol. 2011, 71:445-457.
39. Nishimura S.L., Boylen K.P., Einheber S., Milner T.A., Ramos D.M., Pytela R. Synaptic and glial localization of the integrin alphavbeta8 in mouse and rat brain. Brain Res. 1998, 791:271-282.
40. Peretti D., Peris L., Rosso S., Quiroga S., Caceres A. Evidence for the involvement of KIF4 in the anterograde transport of L1-containing vesicles. J. Cell Biol. 2000, 149:141-152.
41. Pernet V., Schwab M.E. The role of Nogo-A in axonal plasticity, regrowth and repair. Cell Tissue Res. 2012, 349:97-104.
42. Petersen J.D., Kaech S., Banker G. Selective microtubule-based transport of dendritic membrane proteins arises in concert with axon specification. J. Neurosci. 2014, 34:4135-4147.
43. Pinkstaff J.K., Detterich J., Lynch G., Gall C. Integrin subunit gene expression is regionally differentiated in adult brain. J. Neurosci. 1999, 19:1541-1556.
44. Pozo K., Cingolani L.A., Bassani S., Laurent F., Passafaro M., Goda Y. β3 integrin interacts directly with GluA2 AMPA receptor subunit and regulates AMPA receptor expression in hippocampal neurons. Proc. Natl. Acad. Sci. U S A 2012, 109(4):1323-1328.
45. Rodriguez M.A., Pesold C., Liu W.S., Kriho V., Guidotti A., Pappas G.D., Costa E. Colocalization of integrin receptors and reelin in dendritic spine postsynaptic densities of adult nonhuman primate cortex. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:3550-3555.
46. Sekine Y., Okada Y., Noda Y., Kondo S., Aizawa H., Takemura R., Hirokawa N. A novel microtubule-based motor protein (KIF4) for organelle transports, whose expression is regulated developmentally. J. Cell Biol. 1994, 127:187-201.
47. Tan C.L., Kwok J.C., Patani R., Ffrench-Constant C., Chandran S., Fawcett J.W. Integrin activation promotes axon growth on inhibitory chondroitin sulfate proteoglycans by enhancing integrin signaling. J. Neurosci. 2011, 31:6289-6295.
48. Tan C.L., Andrews M.R., Kwok J.C., Heintz T.G., Gumy L.F., Fassler R., Fawcett J.W. Kindlin-1 enhances axon growth on inhibitory chondroitin sulfate proteoglycans and promotes sensory axon regeneration. J. Neurosci. 2012, 32:7325-7335.
49. Theisen U., Straube E., Straube A. Directional persistence of migrating cells requires Kif1C-mediated stabilization of trailing adhesions. Dev. Cell 2012, 23:1153-1166.
50. Tomaselli K.J., Doherty P., Emmett C.J., Walsh F.S., Reichardt L.F. Expression of beta-1 integrins in sensory neurons of the dorsal-root ganglion and their functions in neurite outgrowth on 2 laminin isoforms. J. Neurosci. 1993, 13:4880-4888.
51. Verma P., Chierzi S., Codd A.M., Campbell D.S., Meyer R.L., Holt C.E., Fawcett J.W. Axonal protein synthesis and degradation are necessary for efficient growth cone regeneration. J. Neurosci. 2005, 25:331-342.
52. Vogelezang M., Forster U.B., Han J., Ginsberg M.H., Ffrench-Constant C. Neurite outgrowth on a fibronectin isoform expressed during peripheral nerve regeneration is mediated by the interaction of paxillin with alpha4beta1 integrins. BMC Neurosci. 2007, 8:44.
53. Werner A., Willem M., Jones L.L., Kreutzberg G.W., Mayer U., Raivich G. Impaired axonal regeneration in a7 integrin-deficient mice. J. Neurosci. 2000, 20:1822-1830.
54. Zhang H., Berg J.S., Li Z., Wang Y., Lang P., Sousa A.D., Bhaskar A., Cheney R.E., Stromblad S. Myosin-X provides a motor-based link between integrins and the cytoskeleton. Nat. Cell Biol. 2004, 6:523-531.