Caenorhabditis elegans body mechanics are regulated by body wall muscle tone

Biophysical Journal

Volumn 100, Issue 8, 2011, Pages 1977-1985

  Petzold, Bryan C ^a   Park, Sung Jin ^a,b   Ponce, Pierre ^a   Roozeboom, Clifton ^a   Powell, Chloé ^a,c   Goodman, Miriam B ^a   Pruitt, Beth L ^a  

^a STANFORD UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; CAENORHABDITIS ELEGANS; NEMATODA;

EID: 79959766992     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.02.035     Document Type: Article

References (47)

1. Chalfie, M., J. E. Sulston, S. Brenner. 1985. The neural circuit for touch sensitivity in Caenorhabditis elegans. J. Neurosci. 5:956-964. (Pubitemid 15123043)
2. White, J. G., E. Southgate, S. Brenner. 1986. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos. Trans. R. Soc. (Lond.). B. 314:1-340.
3. Kaplan, J. M., and H. R. Horvitz. 1993. A dual mechanosensory and chemosensory neuron in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA. 90:2227-2231. (Pubitemid 23078599)
4. Wicks, S. R., and C. H. Rankin. 1995. Integration of mechanosensory stimuli in Caenorhabditis elegans. J. Neurosci. 15:2434-2444.
5. Suzuki, H., R. Kerr, W. R. Schafer. 2003. In vivo imaging of C. elegans mechanosensory neurons demonstrates a specific role for the MEC-4 channel in the process of gentle touch sensation. Neuron. 39:1005-1017. (Pubitemid 37130215)
6. O'Hagan, R., M. Chalfie, and M. B. Goodman. 2005. The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals. Nat. Neurosci. 8:43-50. (Pubitemid 41236730)
7. Korta, J., D. A. Clark, A. D. Samuel. 2007. Mechanosensation and mechanical load modulate the locomotory gait of swimming C. elegans. J. Exp. Biol. 210:2383-2389. (Pubitemid 47080216)
8. Karbowski, J., C. J. Cronin, P. W. Sternberg. 2006. Conservation rules, their breakdown, and optimality in Caenorhabditis sinusoidal locomotion. J. Theor. Biol. 242:652-669. (Pubitemid 44291695)
9. Sznitman, J., P. K. Purohit, P. E. Arratia. 2010. Material properties of Caenorhabditis elegans swimming at low Reynolds number. Biophys. J. 98:617-626.
10. Park, S.-J., M. B. Goodman, and B. L. Pruitt. 2007. Analysis of nematode mechanics by piezoresistive displacement clamp. Proc. Natl. Acad. Sci. USA. 104:17376-17381. (Pubitemid 350219830)
11. Richmond, J. E., W. S. Davis, and E. M. Jorgensen. 1999. UNC-13 is required for synaptic vesicle fusion in C. elegans. Nat. Neurosci. 2:959-964. (Pubitemid 30599557)
12. Sznitman, J., X. Shen, P. E. Arratia. 2010. The effects of fluid viscosity on the kinematics and material properties of C. elegans swimming at low Reynolds number. Exp. Mech. 50:1303-1311.
13. Petzold, B. C., S.-J. Park, B. L. Pruitt. 2009. The contribution of body wall muscles to C. elegans body mechanics determined using piezoresistive microcantilevers. 2009 MicroTAS Meeting Abstracts. 1306-1308.
14. Altun, Z. F., and D. H. Hall. 2009. Muscle system, somatic muscle. WormAtlas. DOI:10.3908/wormatlas.1.7.
15. Moerman, D. G., and B. D. Williams. 2006. Sarcomere assembly in C. elegans muscle. WormBook. DOI:10.1895/wormbook.1.81.1.
16. Cox, G. N., M. Kusch, and R. S. Edgar. 1981. Cuticle of Caenorhabditis elegans: its isolation and partial characterization. J. Cell Biol. 90:7-17.
17. Hahn, B.-S., and M. Labouesse. 2001. Tissue integrity: hemidesmosomes and resistance to stress. Curr. Biol. 11:R858-R861. (Pubitemid 33037767)
18. Cox, E. A., C. Tuskey, and J. Hardin. 2004. Cell adhesion receptors in C. elegans. J. Cell Sci. 117:1867-1870. (Pubitemid 38745120)
19. Boyle, J. H., and N. Cohen. 2008. Caenorhabditis elegans body wall muscles are simple actuators. Biosystems. 94:170-181.
20. Burr, A. H., and C. Gans. 1998. Mechanical significance of obliquely striated architecture in nematode muscle. Biol. Bull. 194:1-6. (Pubitemid 28190127)
21. Nagel, G., T. Szellas, E. Bamberg. 2003. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl. Acad. Sci. USA. 100:13940-13945. (Pubitemid 37499170)
22. Nagel, G., M. Brauner, A. Gottschalk. 2005. Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr. Biol. 15:2279-2284. (Pubitemid 41790623)
23. Liu, Q., G. Hollopeter, and E. M. Jorgensen. 2009. Graded synaptic transmission at the Caenorhabditis elegans neuromuscular junction. Proc. Natl. Acad. Sci. USA. 106:10823-10828.
24. Guo, Z. V., A. C. Hart, and S. Ramanathan. 2009. Optical interrogation of neural circuits in Caenorhabditis elegans. Nat. Methods. 6:891-896.
25. Zhang, F., L.-P. Wang, K. Deisseroth. 2007. Multimodal fast optical interrogation of neural circuitry. Nature. 446:633-639. (Pubitemid 46606891)
26. Oesterhelt, D. 1998. The structure and mechanism of the family of retinal proteins from halophilic archaea. Curr. Opin. Struct. Biol. 8:489-500. (Pubitemid 28409960)
27. Lewis, J. A., J. T. Fleming, C. Wu. 1987. The levamisole receptor, a cholinergic receptor of the nematode Caenorhabditis elegans. Mol. Pharmacol. 31:185-193. (Pubitemid 17038898)
28. McIntire, S. L., E. Jorgensen, and H. R. Horvitz. 1993. Genes required for GABA function in Caenorhabditis elegans. Nature. 364:334-337. (Pubitemid 23265273)
29. Hope, I. 1999. C. elegans: A Practical Approach. Oxford University Press, Oxford, UK.
30. Brenner, S. 1974. The genetics of Caenorhabditis elegans. Genetics. 77:71-94.
31. Doll, J. C., S.-J. Park, and B. L. Pruitt. 2009. Design optimization of piezoresistive cantilevers for force sensing in air and water. J. Appl. Phys. 106:64310.
32. Park, S.-J., J. C. Doll, and B. L. Pruitt. 2010. Piezoresistive cantilever performance. Part I. Analytical model for sensitivity. J. Microelectromech. Syst. 19:137-148.
33. Park, S.-J., J. C. Doll, B. L. Pruitt. 2010. Piezoresistive cantilever performance. Part II. Optimization. J. Microelectromech. Syst. 19:149-161.
34. Pruitt, B. L., and T. W. Kenny. 2003. Piezoresistive cantilevers and measurement systems for characterizing low force electrical contacts. Sens. Actuators A. 104:68-77.
35. Croll, N. A. 1975. Behavioral analysis of nematode movement. Adv. Parasitol. 13:71-122.
36. Thein, M. C., G. McCormack, A. P. Page. 2003. Caenorhabditis elegans exoskeleton collagen COL-19: an adult-specific marker for collagen modification and assembly, and the analysis of organismal morphology. Dev. Dyn. 226:523-539. (Pubitemid 36278482)
37. Mulieri, L. A., and N. R. Alpert. 1984. Differential effects of 2, 3-butanedione monoxime (BDM) on activation and contraction. Biophys. J. 45:47a.
38. Ward, A., J. Liu, X. Z. Xu. 2008. Light-sensitive neurons and channels mediate phototaxis in C. elegans. Nat. Neurosci. 11:916-922.
39. Edwards, S. L., N. K. Charlie, K. G. Miller. 2008. A novel molecular solution for ultraviolet light detection in Caenorhabditis elegans. PLoS Biol. 6:e198.
40. Fang-Yen, C., M. Wyart, A. D. Samuel. 2010. Biomechanical analysis of gait adaptation in the nematode Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA. 107:20323-20328.
41. Tytell, E. D., C.-Y. Hsu, L. J. Fauci. 2010. Interactions between internal forces, body stiffness, and fluid environment in a neuromechanical model of lamprey swimming. Proc. Natl. Acad. Sci. USA. 107:19832-19837.
42. Ogneva, I. V., D. V. Lebedev, and B. S. Shenkman. 2010. Transversal stiffness and Young's modulus of single fibers from rat soleus muscle probed by atomic force microscopy. Biophys. J. 98:418-424.
43. Page, A. P., and I. L. Johnstone. 2007. The cuticle. WormBook. DOI:10.1895/wormbook.1.138.1.
44. vander Rijt, J. A. J., K. O. van der Werf, J. Feijen. 2006. Micromechanical testing of individual collagen fibrils. Macromol. Biosci. 6:697-702.
45. Ashby, M. F., L. J. Gibson, R. Olive. 1995. The mechanical properties of natural materials. I. Material property charts. Proc. R. Soc. Lond. A. 450:123-140.
46. Cox, G. N., S. Staprans, and R. S. Edgar. 1981. The cuticleof Caenorhabditis elegans. II. Stage-specific changes in ultrastructure and protein composition during postembryonic development. Dev. Biol. 86:456-470.
47. Harris, J. E., and H. D. Crofton. 1957. Structure and function in the nematodes: internal pressure and cuticular structure in Ascaris. J. Exp. Biol. 34:116-130.