SMB myosin heavy chain knockout enhances tonic contraction and reduces the rate of force generation in ileum and stomach antrum

American Journal of Physiology - Cell Physiology

Volumn 304, Issue 2, 2013, Pages

  Huang, Qian ^a   Babu, Gopal J ^b   Periasamy, Muthu ^c   Eddinger, Thomas J ^a  

^a Marquette University   (United States)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

Myosin; Phasic contraction; Second messenger pathways; SMA; SMB; Smooth muscle; Tonic contraction

Indexed keywords

CARBACHOL; MYOSIN HEAVY CHAIN; PHORBOL DIBUTYRATE; POTASSIUM; PROTEIN KINASE C; PROTEIN KINASE C ALPHA; PROTEIN KINASE C DELTA; REGULATOR PROTEIN; RHO FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE INACTIVATION; ILEUM; INTESTINE MUSCLE; MOUSE; MUSCLE CONTRACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STOMACH ANTRUM; STOMACH FUNDUS; STOMACH MUSCLE; UPREGULATION;

ANIMALS; CARBACHOL; CHOLINERGIC AGONISTS; ILEUM; MICE; MICE, KNOCKOUT; MUSCLE CONTRACTION; MUSCLE STRENGTH; MUSCLE, SMOOTH; MYOSIN HEAVY CHAINS; PHORBOL 12,13-DIBUTYRATE; PHOSPHORYLATION; POTASSIUM; PROTEIN KINASE C-ALPHA; PYLORIC ANTRUM; SECOND MESSENGER SYSTEMS; SMOOTH MUSCLE MYOSINS;

MUS;

EID: 84872387287     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00280.2012     Document Type: Article

References (65)

1. Babij P, Kelly C, Periasamy M. Characterization of a mammalian smooth muscle myosin heavy-chain gene: complete nucleotide and protein coding sequence and analysis of the 5' end of the gene. Proc Natl Acad Sci USA 88: 10676-10680, 1991.
2. Babu GJ, Celia G, Rhee AY, Yamamura H, Takahashi K, Brozovich FV, Osol G, Periasamy M. Effects of h1-calponin ablation on the contractile properties of bladder versus vascular smooth muscle in mice lacking SM-B myosin. J Physiol 577: 1033-1042, 2006.
3. Babu GJ, Loukianov E, Loukianova T, Pyne GJ, Huke S, Osol G, Low RB, Paul RJ, Periasamy M. Loss of SM-B myosin affects muscle shortening velocity and maximal force development. Nat Cell Biol 3: 1025-1029, 2001.
4. Babu GJ, Pyne GJ, Zhou Y, Okwuchukuasanya C, Brayden JE, Osol G, Paul RJ, Low RB, Periasamy M. Isoform switching from SM-B to SM-A myosin results in decreased contractility and altered expression of thin filament regulatory proteins. Am J Physiol Cell Physiol 287: C723-C729, 2004.
5. Bornstein JC, Costa M, Grider JR. Enteric motor and interneuronal circuits controlling motility. Neurogastroenterol Motil 16 Suppl 1: 34-38, 2004.
6. Borrione AC, Zanellato AM, Scannapieco G, Pauletto P, Sartore S. Myosin heavy-chain isoforms in adult and developing rabbit vascular smooth muscle. Eur J Biochem 183: 413-417, 1989.
7. Dillon PF, Aksoy MO, Driska SP, Murphy RA. Myosin phosphorylation and the cross-bridge cycle in arterial smooth muscle. Science 211: 495-497, 1981.
8. Driska SP, Aksoy MO, Murphy RA. Myosin light chain phosphorylation associated with contraction in arterial smooth muscle. Am J Physiol Cell Physiol 240: C222-C233, 1981.
9. Eddinger TJ. Unique contractile and structural protein expression in dog ileal inner circular smooth muscle. J Smooth Muscle Res 45: 217-230, 2009.
10. Eddinger TJ, Meer DP. Myosin II isoforms in smooth muscle: heterogeneity and function. Am J Physiol Cell Physiol 293: C493-C508, 2007.
11. Eddinger TJ, Meer DP. Single rabbit stomach smooth muscle cell myosin heavy chain SMB expression and shortening velocity. Am J Physiol Cell Physiol 280: C309-C316, 2001.
12. Eddinger TJ, Murphy RA. Developmental changes in actin and myosin heavy chain isoform expression in smooth muscle. Arch Biochem Biophys 284: 232-237, 1991.
13. Eddinger TJ, Wolf JA. Expression of four myosin heavy chain isoforms with development in mouse uterus. Cell Motil Cytoskeleton 25: 358-368, 1993.
14. Ehlert FJ, Sawyer GW, Esqueda EE. Contractile role of M2 and M3 muscarinic receptors in gastrointestinal smooth muscle. Life Sci 64: 387-394, 1999.
15. Frid MG, Printesva OY, Chiavegato A, Faggin E, Scatena M, Koteliansky VE, Pauletto P, Glukhova MA, Sartore S. Myosin heavy-chain isoform composition and distribution in developing and adult human aortic smooth muscle. J Vasc Res 30: 279-292, 1993.
16. Fuglsang A, Khromov A, Torok K, Somlyo AV, Somlyo AP. Flash photolysis studies of relaxation and cross-bridge detachment: higher sensitivity of tonic than phasic smooth muscle to MgADP. J Muscle Res Cell Motil 14: 666-677, 1993.
17. Furness JB. The enteric nervous system and neurogastroenterology. Nat Rev Gastroenterol Hepatol 9: 286-294, 2012.
18. Furness JB, Young HM, Pompolo S, Bornstein JC, Kunze WA, McConalogue K. Plurichemical transmission and chemical coding of neurons in the digestive tract. Gastroenterology 108: 554-563, 1995.
19. Gerthoffer WT, Gunst SJ. Invited review: focal adhesion and small heat shock proteins in the regulation of actin remodeling and contractility in smooth muscle. J Appl Physiol 91: 963-972, 2001.
20. Giuriato L, Scatena M, Chiavegato A, Tonello M, Scannapieco G, Pauletto P, Sartore S. Non-muscle myosin isoforms and cell heterogeneity in developing rabbit vascular smooth muscle. J Cell Sci 101: 233-246, 1992.
21. Hai CM, Murphy RA. Cross-bridge dephosphorylation and relaxation of vascular smooth muscle. Am J Physiol Cell Physiol 256: C282-C287, 1989.
22. Hamada Y, Yanagisawa M, Katsuragawa Y, Coleman JR, Nagata S, Matsuda G, Masaki T. Distinct vascular and intestinal smooth muscle myosin heavy chain mRNAs are encoded by a single-copy gene in the chicken. Biochem Biophys Res Commun 170: 53-58, 1990.
23. Han S, Speich JE, Eddinger TJ, Berg KM, Miner AS, Call C, Ratz PH. Evidence for absence of latch-bridge formation in muscular saphenous arteries. Am J Physiol Heart Circ Physiol 291: H138-H146, 2006.
24. Harnett KM, Cao W, Biancani P. Signal-transduction pathways that regulate smooth muscle function I. Signal transduction in phasic (esophageal) and tonic (gastroesophageal sphincter) smooth muscles. Am J Physiol Gastrointest Liver Physiol 288: G407-G416, 2005.
25. Herlihy JT, Murphy RA. Length-tension relationship of smooth muscle of the hog carotid artery. Circ Res 33: 275-283, 1973.
26. Hu K, Ji L, Applegate KT, Danuser G, Waterman-Storer CM. Differential transmission of actin motion within focal adhesions. Science 315: 111-115, 2007.
27. Hypolite JA, Chang S, LaBelle E, Babu GJ, Periasamy M, Wein AJ, Chacko S. Deletion of SM-B, the high ATPase isoform of myosin, upregulates the PKC-mediated signal transduction pathway in murine urinary bladder smooth muscle. Am J Physiol Renal Physiol 296: F658-F665, 2009.
28. Jiang MJ, Morgan KG. Intracellular calcium levels in phorbol esterinduced contractions of vascular muscle. Am J Physiol Heart Circ Physiol 253: H1365-H1371, 1987.
29. Karagiannis P, Babu GJ, Periasamy M, Brozovich FV. Myosin heavy chain isoform expression regulates shortening velocity in smooth muscle: studies using an SMB KO mouse line. J Muscle Res Cell Motil 25: 149-158, 2004.
30. Karagiannis P, Babu GJ, Periasamy M, Brozovich FV. The smooth muscle myosin seven amino acid heavy chain insert's kinetic role in the crossbridge cycle for mouse bladder. J Physiol 547: 463-473, 2003.
31. Kelley CA, Takahashi M, Yu JH, Adelstein RS. An insert of seven amino acids confers functional differences between smooth muscle myosins from the intestines and vasculature. J Biol Chem 268: 12848-12854, 1993.
32. Khromov A, Somlyo AV, Somlyo AP. MgADP promotes a catch-like state developed through force-calcium hysteresis in tonic smooth muscle. Biophys J 75: 1926-1934, 1998.
33. Khromov A, Somlyo AV, Trentham DR, Zimmermann B, Somlyo AP. The role of MgADP in force maintenance by dephosphorylated crossbridges in smooth muscle: a flash photolysis study. Biophys J 69: 2611-2622, 1995.
34. Kiernan JA. Histological and Histochemical Methods: Theory and Practice. Bloxham, UK: Scion, 2008, p. zvi 606.
35. Kim HR, Gallant C, Leavis PC, Gunst SJ, Morgan KG. Cytoskeletal remodeling in differentiated vascular smooth muscle is actin isoform dependent and stimulus dependent. Am J Physiol Cell Physiol 295: C768-C778, 2008.
36. Kitazawa T, Hashiba K, Cao J, Unno T, Komori S, Yamada M, Wess J, Taneike T. Functional roles of muscarinic M2 and M3 receptors in mouse stomach motility: studies with muscarinic receptor knockout mice. Eur J Pharmacol 554: 212-222, 2007.
37. Kovacs M, Thirumurugan K, Knight PJ, Sellers JR. Load-dependent mechanism of nonmuscle myosin 2. Proc Natl Acad Sci USA 104: 9994-9999, 2007.
38. Kovacs M, Wang F, Hu A, Zhang Y, Sellers JR. Functional divergence of human cytoplasmic myosin II: kinetic characterization of the nonmuscle IIA isoform. J Biol Chem 278: 38132-38140, 2003.
39. Lofgren M, Ekblad E, Morano I, Arner A. Nonmuscle Myosin motor of smooth muscle. J Gen Physiol 121: 301-310, 2003.
40. Loukianov E, Loukianova T, Periasamy M. Myosin heavy chain isoforms in smooth muscle. Comp Biochem Physiol B Biochem Mol Biol 117: 13-18, 1997.
41. Mehta D, Gunst SJ. Actin polymerization stimulated by contractile activation regulates force development in canine tracheal smooth muscle. J Physiol 519: 829-840, 1999.
42. Morano I, Chai GX, Baltas LG, Lamounier-Zepter V, Lutsch G, Kott M, Haase H, Bader M. Smooth-muscle contraction without smoothmuscle myosin. Nat Cell Biol 2: 371-375, 2000.
43. Murthy KS. Signaling for contraction and relaxation in smooth muscle of the gut. Annu Rev Physiol 68: 345-374, 2006.
44. Patzak A, Petzhold D, Wronski T, Martinka P, Babu GJ, Periasamy M, Haase H, Morano I. Constriction velocities of renal afferent and efferent arterioles of mice are not related to SMB expression. Kidney Int 68: 2726-2734, 2005.
45. Pavalko FM, Adam LP, Wu MF, Walker TL, Gunst SJ. Phosphorylation of dense-plaque proteins talin and paxillin during tracheal smooth muscle contraction. Am J Physiol Cell Physiol 268: C563-C571, 1995.
46. Phillips CL, Yamakawa K, Adelstein RS. Cloning of the cDNA encoding human nonmuscle myosin heavy chain-B and analysis of human tissues with isoform-specific antibodies. J Muscle Res Cell Motil 16: 379-389, 1995.
47. Poole DP, Furness JB. PKC delta-isoform translocation and enhancement of tonic contractions of gastrointestinal smooth muscle. Am J Physiol Gastrointest Liver Physiol 292: G887-G898, 2007.
48. Rattan S, De Godoy MA, Patel CA. Rho kinase as a novel molecular therapeutic target for hypertensive internal anal sphincter. Gastroenterology 131: 108-116, 2006.
49. Ratz PH, Berg KM, Urban NH, Miner AS. Regulation of smooth muscle calcium sensitivity: KCl as a calcium-sensitizing stimulus. Am J Physiol Cell Physiol 288: C769-C783, 2005.
50. Rembold CM, Murphy RA. Myoplasmic calcium, myosin phosphorylation, and regulation of the crossbridge cycle in swine arterial smooth muscle. Circ Res 58: 803-815, 1986.
51. Rosenfeld SS, Xing J, Chen LQ, Sweeney HL. Myosin IIb is unconventionally conventional. J Biol Chem 278: 27449-27455, 2003.
52. Sinn DH, Min BH, Ko EJ, Lee JY, Kim JJ, Rhee JC, Kim S, Ward SM, Rhee PL. Regional differences of the effects of acetylcholine in the human gastric circular muscle. Am J Physiol Gastrointest Liver Physiol 299: G1198-G1203, 2010.
53. Sohn UD, Cao W, Tang DC, Stull JT, Haeberle JR, Wang CL, Harnett KM, Behar J, Biancani P. Myosin light chain kinase- and PKC- dependent contraction of LES and esophageal smooth muscle. Am J Physiol Gastrointest Liver Physiol 281: G467-G478, 2001.
54. 2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol Rev 83: 1325-1358, 2003.
55. Somlyo AP, Somlyo AV. Vascular smooth muscle. I. Normal structure, pathology, biochemistry, and biophysics. Pharmacol Rev 20: 197-272, 1968.
56. Somlyo AV, Matthew JD, Wu X, Khromov AS, Somlyo AP. Regulation of the cross-bridge cycle: the effects of MgADP, LC17 isoforms and telokin. Acta Physiol Scand 164: 381-388, 1998.
57. Sutherland C, Walsh MP. Phosphorylation of caldesmon prevents its interaction with smooth muscle myosin. J Biol Chem 264: 578-583, 1989.
58. Sweeney HL, Rosenfeld SS, Brown F, Faust L, Smith J, Xing J, Stein LA, Sellers JR. Kinetic tuning of myosin via a flexible loop adjacent to the nucleotide binding pocket. J Biol Chem 273: 6262-6270, 1998.
59. Szymanski PT, Tao T. Localization of protein regions involved in the interaction between calponin and myosin. J Biol Chem 272: 11142-11146, 1997.
60. Tuck SA, Maghni K, Poirier A, Babu GJ, Periasamy M, Bates JH, Leguillette R, Lauzon AM. Time course of airway mechanics of the (+)insert myosin isoform knockout mouse. Am J Respir Cell Mol Biol 30: 326-332, 2004.
61. Tullio AN, Accili D, Ferrans VJ, Yu ZX, Takeda K, Grinberg A, Westphal H, Preston YA, Adelstein RS. Nonmuscle myosin II-B is required for normal development of the mouse heart. Proc Natl Acad Sci USA 94: 12407-12412, 1997.
62. Unno T, Matsuyama H, Izumi Y, Yamada M, Wess J, Komori S. Roles of M2 and M3 muscarinic receptors in cholinergic nerve-induced contractions in mouse ileum studied with receptor knockout mice. Br J Pharmacol 149: 1022-1030, 2006.
63. 2+ sensitization of arterial muscle. Am J Physiol Cell Physiol 285: C1377-C1385, 2003.
64. Wahl M, Eddinger TJ, Hai CM. Sinusoidal length oscillation- and receptor-mediated mRNA expression of myosin isoforms and α-SM actin in airway smooth muscle. Am J Physiol Cell Physiol 287: C1697-C1708, 2004.
65. Wang F, Kovacs M, Hu A, Limouze J, Harvey EV, Sellers JR. Kinetic mechanism of non-muscle myosin IIB: functional adaptations for tension generation and maintenance. J Biol Chem 278: 27439-27448, 2003.