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The Journal of Neuroscience, May 18, 2005, 25(20):4964-4973; doi:10.1523/JNEUROSCI.0773-05.2005

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Development/Plasticity/Repair
Adaptation of Sensory Neurons to Hyalectin and Decorin Proteoglycans

Michele L. Lemons,1 Suman Barua,1 Michael L. Abanto,1 Willi Halfter,2 and Maureen L. Condic1

1Department of Neurobiology and Anatomy, University of Utah, School of Medicine, Salt Lake City, Utah 84132-3401, and 2Department of Neurobiology, University of Pittsburgh, Pittsburgh, Pennsylvania 15261

Proteoglycans are abundantly expressed in the pathways of developing and regenerating neurons, yet the responses of neurons to specific proteoglycans are not well characterized. We have shown previously that one chondroitin sulfate proteoglycan (CSPG), aggrecan, is potently inhibitory to sensory axon extension in short-term assays and that over time, embryonic neurons adapt to aggrecan-mediated inhibition through the transcriptional upregulation of integrin expression (Condic et al., 1999). Here, we have compared the response of embryonic sensory neurons to structurally distinct CSPGs that belong to either the hyalectin (or lectican) family of large, aggregating proteoglycans or the decorin (or small leucine-rich proteoglycan) family of smaller proteoglycans. Both of these structurally diverse proteoglycan families are expressed in developing embryos and inhibit outgrowth of embryonic sensory neurons in short-term cultures. These results document a previously uncharacterized inhibitory function for the decorin-family proteoglycan biglycan. Interestingly, embryonic neurons adapt to these diverse proteoglycans over time. Adaptation is associated with upregulation of select integrin {alpha} subunits in a proteoglycan-specific manner. Overexpression of specific integrin {alpha} subunits improves neuronal regeneration on some but not all decorin-family CSPGs, suggesting that neurons adapt to inhibition mediated by closely related proteoglycans using distinct mechanisms. Our findings indicate that CSPGs with diverse core proteins and distinct numbers of chondroitin sulfate substitution sites mediate a similar response in sensory neurons, suggesting that increased integrin expression may be an effective means of promoting axonal regeneration in the presence of diverse inhibitory proteoglycan species in vivo.

Key words: integrin; aggrecan; decorin; biglycan; versican; CSPG; chondroitin sulfate

Received Nov 29, 2004; revised April 11, 2005; accepted April 12, 2005.






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