Smooth muscle caldesmon modulates peristalsis in the wild type and non-innervated zebrafish intestine

Neurogastroenterology and Motility

Volumn 24, Issue 3, 2012, Pages 288-299

  Abrams, J ^a   Davuluri, G ^a   Seiler, C ^a   Pack, M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Enteric nervous system; Gastrointestinal motility; Hypomotility; Myosin light chain; Zebrafish

Indexed keywords

ACTIN; CALDESMON; MYOSIN;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION; GENE SILENCING; GENOMICS; INTESTINE MOTILITY; LARVA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEQUENCE HOMOLOGY; SMOOTH MUSCLE; ZEBRA FISH;

ACTINS; ALTERNATIVE SPLICING; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CALMODULIN-BINDING PROTEINS; HUMANS; INTESTINES; MUSCLE CONTRACTION; MUSCLE, SMOOTH; MYOSINS; PERISTALSIS; PROTEIN ISOFORMS; ZEBRAFISH;

EID: 84856768815     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/j.1365-2982.2011.01844.x     Document Type: Article

References (57)

1. Kamm KE, Stull JT. The function of myosin and myosin light chain kinase phosphorylation in smooth muscle. Annu Rev Pharmacol Toxicol 1985; 25: 593-620.
2. Murphy RA. Contraction in smooth muscle cells. Annu Rev Physiol 1989; 51: 275-83.
3. Siegman MJ, Butler TM, Mooers SU, Michalek A. Ca2+ can affect Vmax without changes in myosin light chain phosphorylation in smooth muscle. Pflugers Arch 1984; 401: 385-90.
4. Gerthoffer WT. Dissociation of myosin phosphorylation and active tension during muscarinic stimulation of tracheal smooth muscle. J Pharmacol Exp Ther 1987; 240: 8-15.
5. Haeberle JR, Hott JW, Hathaway DR. Regulation of isometric force and isotonic shortening velocity by phosphorylation of the 20, 000 dalton myosin light chain of rat uterine smooth muscle. Pflugers Arch 1985; 403: 215-9.
6. Moreland S, Moreland RS. Effects of dihydropyridines on stress, myosin phosphorylation, and V0 in smooth muscle. Am J Physiol 1987; 252: H1049-58.
7. Gusev NB. Some properties of caldesmon and calponin and the participation of these proteins in regulation of smooth muscle contraction and cytoskeleton formation. Biochemistry 2001; 66: 1112-21.
8. Sobue K, Muramoto Y, Fujita M, Kakiuchi S. Purification of a calmodulin-binding protein from chicken gizzard that interacts with F-actin. Proc Natl Acad Sci USA 1981; 78: 5652-5.
9. Kordowska J, Huang R, Wang CL. Phosphorylation of caldesmon during smooth muscle contraction and cell migration or proliferation. J Biomed Sci 2006; 13: 159-72.
10. Helfman DM, Levy ET, Berthier C et al. Caldesmon inhibits nonmuscle cell contractility and interferes with the formation of focal adhesions. Mol Biol Cell 1999; 10: 3097-112.
11. Wang CL, Chalovich JM, Graceffa P, Lu RC, Mabuchi K, Stafford WF. A long helix from the central region of smooth muscle caldesmon. J Biol Chem 1991; 266: 13958-63.
12. Horiuchi KY, Miyata H, Chacko S. Modulation of smooth muscle actomyosin ATPase by thin filament associated proteins. Biochem Biophys Res Commun 1986; 136: 962-8.
13. Earley JJ, Su X, Moreland RS. Caldesmon inhibits active crossbridges in unstimulated vascular smooth muscle: an antisense oligodeoxynucleotide approach. Circ Res 1998; 83: 661-7.
14. Szpacenko A, Wagner J, Dabrowska R, Ruegg JC. Caldesmon-induced inhibition of ATPase activity of actomyosin and contraction of skinned fibres of chicken gizzard smooth muscle. FEBS Lett 1985; 192: 9-12.
15. Ansari S, Alahyan M, Marston SB, El-Mezgueldi M. Role of caldesmon in the Ca2+ regulation of smooth muscle thin filaments: evidence for a cooperative switching mechanism. J Biol Chem 2008; 283: 47-56.
16. Wang CL. Caldesmon and smooth-muscle regulation. Cell Biochem Biophys 2001; 35: 275-88.
17. Smith CW, Marston SB. Disassembly and reconstitution of the Ca2+ -sensitive thin filaments of vascular smooth muscle. FEBS Lett 1985; 184: 115-9.
18. Ikebe M, Reardon S. Phosphorylation of smooth muscle caldesmon by calmodulin-dependent protein kinase II Identification of the phosphorylation sites. J Biol Chem 1990; 265: 17607-12.
19. Childs TJ, Watson MH, Sanghera JS, Campbell DL, Pelech SL, Mak AS. Phosphorylation of smooth muscle caldesmon by mitogen-activated protein (MAP) kinase and expression of MAP kinase in differentiated smooth muscle cells. J Biol Chem 1992; 267: 22853-9.
20. Katsuyama H, Wang CL, Morgan KG. Regulation of vascular smooth muscle tone by caldesmon. J Biol Chem 1992; 267: 14555-8.
21. Horiuchi KY, Chacko S. Caldesmon inhibits the cooperative turning-on of the smooth muscle heavy meromyosin by tropomyosin-actin. Biochemistry 1989; 28: 9111-6.
22. Lu C, Liu Y, Tang X, Ye H, Zhu D. Role of 15-hydroxyeicosatetraenoic acid in phosphorylation of ERK1/2 and caldesmon in pulmonary arterial smooth muscle cells. Can J Physiol Pharmacol 2006; 84: 1061-9.
23. Zhang H, Zhang L. Regulation of alpha1-adrenoceptor-mediated contractions of the uterine artery by protein kinase C: role of the thick- and thin-filament regulatory pathways. J Pharmacol Exp Ther 2007; 322: 1253-60.
24. Chacko S, Chang S, Hypolite J, Disanto M, Wein A. Alteration of contractile and regulatory proteins following partial bladder outlet obstruction. Scand J Urol Nephrol Suppl 2004; 215: 26-36.
25. Smolock EM, Trappanese DM, Chang S, Wang T, Titchenell P, Moreland RS. siRNA-mediated knockdown of h-caldesmon in vascular smooth muscle. Am J Physiol Heart Circ Physiol 2009; 297: H1930-9.
26. Gerthoffer WT, Pohl J. Caldesmon and calponin phosphorylation in regulation of smooth muscle contraction. Can J Physiol Pharmacol 1994; 72: 1410-4.
27. Guo H, Wang CL. Specific disruption of smooth muscle caldesmon expression in mice. Biochem Biophys Res Commun 2005; 330: 1132-7.
28. Wallace KN, Akhter S, Smith EM, Lorent K, Pack M. Intestinal growth and differentiation in zebrafish. Mech Dev 2005; 122: 157-73.
29. Lee YH, Gallant C, Guo H, Li Y, Wang CA, Morgan KG. Regulation of vascular smooth muscle tone by N-terminal region of caldesmon. Possible role of tethering actin to myosin. J Biol Chem 2000; 275: 3213-20.
30. Davuluri G, Seiler C, Abrams J, Soriano AJ, Pack M. Differential effects of thin and thick filament disruption on zebrafish smooth muscle regulatory proteins. Neurogastroenterol Motil 2010; 22: 1100-e1285.
31. Amores A, Force A, Yan YL et al. Zebrafish hox clusters and vertebrate genome evolution. Science 1998; 282: 1711-4.
32. Zheng PP, Severijnen LA, van der Weiden M, Willemsen R, Kros JM. A crucial role of caldesmon in vascular development in vivo. Cardiovasc Res 2009; 81: 362-9.
33. Bryan J. Caldesmon, acidic amino acids and molecular weight determinations. J Muscle Res Cell Motil 1989; 10: 95-6.
34. Seiler C, Abrams J, Pack M. Characterization of zebrafish intestinal smooth muscle development using a novel sm22alpha-b promoter. Dev Dyn 2010; 239: 2806-12.
35. Ikebe M, Reardon S. Binding of caldesmon to smooth muscle myosin. J Biol Chem 1988; 263: 3055-8.
36. Wang Z, Jiang H, Yang ZQ, Chacko S. Both N-terminal myosin-binding and C-terminal actin-binding sites on smooth muscle caldesmon are required for caldesmon-mediated inhibition of actin filament velocity. Proc Natl Acad Sci USA 1997; 94: 11899-904.
37. Zhan QQ, Wong SS, Wang CL. A calmodulin-binding peptide of caldesmon. J Biol Chem 1991; 266: 21810-4.
38. Provost E, Rhee J, Leach SD. Viral 2A peptides allow expression of multiple proteins from a single ORF in transgenic zebrafish embryos. Genesis 2007; 45: 625-9.
39. Kelsh RN, Eisen JS. The zebrafish colourless gene regulates development of non-ectomesenchymal neural crest derivatives. Development 2000; 127: 515-25.
40. Dutton KA, Pauliny A, Lopes SS et al. Zebrafish colourless encodes sox10 and specifies non-ectomesenchymal neural crest fates. Development 2001; 128: 4113-25.
41. Mabuchi K, Wang CL. Electron microscopic studies of chicken gizzard caldesmon and its complex with calmodulin. J Muscle Res Cell Motil 1991; 12: 145-51.
42. Suveges D, Gaspari Z, Toth G, Nyitray L. Charged single alpha-helix: a versatile protein structural motif. Proteins 2009; 74: 905-16.
43. Rich A, Leddon SA, Hess SL et al. Kit-like immunoreactivity in the zebrafish gastrointestinal tract reveals putative ICC. Dev Dyn 2007; 236: 903-11.
44. Shepherd I, Eisen J. Development of the zebrafish enteric nervous system. Methods Cell Biol 2011; 101: 143-60.
45. Albrecht K, Schneider A, Liebetrau C, Ruegg JC, Pfitzer G. Exogenous caldesmon promotes relaxation of guinea-pig skinned taenia coli smooth muscles: inhibition of cooperative reattachment of latch bridges? Pflugers Arch 1997; 434: 534-42.
46. Roberts RR, Murphy JF, Young HM, Bornstein JC. Development of colonic motility in the neonatal mouse-studies using spatiotemporal maps. Am J Physiol Gastrointest Liver Physiol 2007; 292: G930-8.
47. Roberts RR, Ellis M, Gwynne RM et al. The first intestinal motility patterns in fetal mice are not mediated by neurons or interstitial cells of Cajal. J Physiol 2010; 588: 1153-69.
48. Holmberg A, Olsson C, Hennig GW. TTX-sensitive and TTX-insensitive control of spontaneous gut motility in the developing zebrafish (Danio rerio) larvae. J Exp Biol 2007; 210: 1084-91.
49. Miettinen M, Lasota J. Gastrointestinal stromal tumors: review on morphology, molecular pathology, prognosis, and differential diagnosis. Arch Pathol Lab Med 2006; 130: 1466-78.
50. McCluggage WG. A critical appraisal of the value of immunohistochemistry in diagnosis of uterine neoplasms. Adv Anat Pathol 2004; 11: 162-71.
51. Word RA, Stull JT, Casey ML, Kamm KE. Contractile elements and myosin light chain phosphorylation in myometrial tissue from nonpregnant and pregnant women. J Clin Invest 1993; 92: 29-37.
52. Li Y, Reznichenko M, Tribe RM et al. Stretch activates human myometrium via ERK, caldesmon and focal adhesion signaling. PLoS ONE 2009; 4: e7489.
53. Li Y, Je HD, Malek S, Morgan KG. Role of ERK1/2 in uterine contractility and preterm labor in rats. Am J Physiol Regul Integr Comp Physiol 2004; 287: R328-35.
54. Somara S, Bitar KN. Phosphorylated HSP27 modulates the association of phosphorylated caldesmon with tropomyosin in colonic smooth muscle. Am J Physiol Gastrointest Liver Physiol 2006; 291: G630-9.
55. He WQ, Peng YJ, Zhang WC et al. Myosin light chain kinase is central to smooth muscle contraction and required for gastrointestinal motility in mice. Gastroenterology 2008; 135: 610-20.
56. Somara S, Gilmont RR, Martens JR, Bitar KN. Ectopic expression of caveolin-1 restores physiological contractile response of aged colonic smooth muscle. Am J Physiol Gastrointest Liver Physiol 2007; 293: G240-9.
57. Farrugia G. Interstitial cells of Cajal in health and disease. Neurogastroenterol Motil 2008; 20: 54-63.