Localized Alteration of Microtubule Polymerization in Response to Guidance Cues

Overview

Journal J Neurosci Res

Specialty Neurology

Date 2010 Sep 1

PMID 20806407

Citations 9

Authors

Terri-Ann N Kelly

Yasuhiro Katagiri

Keri B Vartanian

Pramukta Kumar

Inn-Inn Chen

William J Rosoff

Jeffery S Urbach

Herbert M Geller

Affiliations

Soon will be listed here.

Abstract

Inhibition of microtubule dynamic instability prevents growth cone turning in response to guidance cues, yet specific changes in microtubule polymerization as growth cones encounter boundaries have not been investigated. In this study, we examined the rate and direction of microtubule polymerization in response to soluble nerve growth factor (NGF) and immobilized chondroitin sulfate proteoglycans (CSPGs) by expressing enhanced GFP-EB3 in rat pheochromocytoma (PC12) cells. GFP-EB3 comets were monitored in live cells using time-lapse epifluorescent microscopy. With an automated tracking system, the rate of microtubule polymerization was calculated as the frame-to-frame displacement of EB3 comets. Our results demonstrate that the rate of microtubule polymerization is increased following NGF treatment, whereas contact with CSPGs decreases microtubule polymerization rates. This reduction in microtubule polymerization rates was specifically localized to neurites in direct contact with CSPGs and not at noncontacting neurites. Additionally, we found an increase in the percentage of microtubules polymerizing in the retrograde direction in neurites at CSPG boundaries, with a concomitant decrease in the rate of retrograde microtubule polymerization. These results implicate localized changes in microtubule dynamics as an important component of the growth cone response to guidance cues.

Citing Articles

Alpha 7 nicotinic receptors attenuate neurite development through calcium activation of calpain at the growth cone.

King J, Kabbani N PLoS One. 2018; 13(5):e0197247.

PMID: 29768467 PMC: 5955587. DOI: 10.1371/journal.pone.0197247.

CSPGs inhibit axon branching by impairing mitochondria-dependent regulation of actin dynamics and axonal translation.

Sainath R, Ketschek A, Grandi L, Gallo G Dev Neurobiol. 2016; 77(4):454-473.

PMID: 27429169 PMC: 5243930. DOI: 10.1002/dneu.22420.

Mycalolide B dissociates dynactin and abolishes retrograde axonal transport of dense-core vesicles.

Cavolo S, Zhou C, Ketcham S, Suzuki M, Ukalovic K, Silverman M Mol Biol Cell. 2015; 26(14):2664-72.

PMID: 26023088 PMC: 4501363. DOI: 10.1091/mbc.E14-11-1564.

Microtubule dynamics at the growth cone are mediated by α7 nicotinic receptor activation of a Gαq and IP3 receptor pathway.

Nordman J, Kabbani N FASEB J. 2014; 28(7):2995-3006.

PMID: 24687992 PMC: 4062821. DOI: 10.1096/fj.14-251439.

Global analysis of neuronal phosphoproteome regulation by chondroitin sulfate proteoglycans.

Yu P, Pisitkun T, Wang G, Wang R, Katagiri Y, Gucek M PLoS One. 2013; 8(3):e59285.

PMID: 23527152 PMC: 3601063. DOI: 10.1371/journal.pone.0059285.

References

Poulain F, Sobel A . The microtubule network and neuronal morphogenesis: Dynamic and coordinated orchestration through multiple players. Mol Cell Neurosci. 2009; 43(1):15-32. DOI: 10.1016/j.mcn.2009.07.012. View

Stepanova T, Slemmer J, Hoogenraad C, Lansbergen G, Dortland B, De Zeeuw C . Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein). J Neurosci. 2003; 23(7):2655-64. PMC: 6742099. View

Challacombe J, Snow D, Letourneau P . Dynamic microtubule ends are required for growth cone turning to avoid an inhibitory guidance cue. J Neurosci. 1997; 17(9):3085-95. PMC: 6573642. View

Ma Y, Shakiryanova D, Vardya I, Popov S . Quantitative analysis of microtubule transport in growing nerve processes. Curr Biol. 2004; 14(8):725-30. DOI: 10.1016/j.cub.2004.03.061. View

Schaefer A, Kabir N, Forscher P . Filopodia and actin arcs guide the assembly and transport of two populations of microtubules with unique dynamic parameters in neuronal growth cones. J Cell Biol. 2002; 158(1):139-52. PMC: 2173029. DOI: 10.1083/jcb.200203038. View

Marsh L, Letourneau P . Growth of neurites without filopodial or lamellipodial activity in the presence of cytochalasin B. J Cell Biol. 1984; 99(6):2041-7. PMC: 2113555. DOI: 10.1083/jcb.99.6.2041. View

Lee A, Suter D . Quantitative analysis of microtubule dynamics during adhesion-mediated growth cone guidance. Dev Neurobiol. 2008; 68(12):1363-77. PMC: 2745986. DOI: 10.1002/dneu.20662. View

Tessier-Lavigne M, Goodman C . The molecular biology of axon guidance. Science. 1996; 274(5290):1123-33. DOI: 10.1126/science.274.5290.1123. View

Kim T, Chang S . Quantitative evaluation of the mode of microtubule transport in Xenopus neurons. Mol Cells. 2006; 21(1):76-81. View

10.

Koprivica V, Cho K, Park J, Yiu G, Atwal J, Gore B . EGFR activation mediates inhibition of axon regeneration by myelin and chondroitin sulfate proteoglycans. Science. 2005; 310(5745):106-10. DOI: 10.1126/science.1115462. View

11.

Shen Y, Tenney A, Busch S, Horn K, Cuascut F, Liu K . PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science. 2009; 326(5952):592-6. PMC: 2811318. DOI: 10.1126/science.1178310. View

12.

Dergham P, Ellezam B, Essagian C, Avedissian H, Lubell W, McKerracher L . Rho signaling pathway targeted to promote spinal cord repair. J Neurosci. 2002; 22(15):6570-7. PMC: 6758168. DOI: 20026637. View

13.

Powell E, Mercado M, Geller H . Protein kinase C mediates neurite guidance at an astrocyte boundary. Glia. 2001; 33(4):288-97. DOI: 10.1002/1098-1136(20010315)33:4<288::aid-glia1027>3.0.co;2-r. View

14.

Greene L, Tischler A . Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci U S A. 1976; 73(7):2424-8. PMC: 430592. DOI: 10.1073/pnas.73.7.2424. View

15.

Suter D, Forscher P . An emerging link between cytoskeletal dynamics and cell adhesion molecules in growth cone guidance. Curr Opin Neurobiol. 1998; 8(1):106-16. DOI: 10.1016/s0959-4388(98)80014-7. View

16.

Miller K, Joshi H . Tubulin transport in neurons. J Cell Biol. 1996; 133(6):1355-66. PMC: 2120892. DOI: 10.1083/jcb.133.6.1355. View

17.

Burton P . Dendrites of mitral cell neurons contain microtubules of opposite polarity. Brain Res. 1988; 473(1):107-15. DOI: 10.1016/0006-8993(88)90321-6. View

18.

Harrison R, Turley E . Active erk regulates microtubule stability in H-ras-transformed cells. Neoplasia. 2001; 3(5):385-94. PMC: 1506201. DOI: 10.1038/sj.neo.7900180. View

19.

Sivasankaran R, Pei J, Wang K, Zhang Y, Shields C, Xu X . PKC mediates inhibitory effects of myelin and chondroitin sulfate proteoglycans on axonal regeneration. Nat Neurosci. 2004; 7(3):261-8. DOI: 10.1038/nn1193. View

20.

Tanaka E, Kirschner M . The role of microtubules in growth cone turning at substrate boundaries. J Cell Biol. 1995; 128(1-2):127-37. PMC: 2120338. DOI: 10.1083/jcb.128.1.127. View