Calponin 3 regulates stress fiber formation in dermal fibroblasts during wound healing

Archives of Dermatological Research

Volumn 305, Issue 7, 2013, Pages 571-584

  Daimon, Etsuko ^a   Shibukawa, Yukinao ^a   Wada, Yoshinao ^a  

^a RESEARCH INSTITUTE FOR MATERNAL AND CHILD HEALTH   (Japan)

Author keywords

Smooth muscle actin; Calponin 3; Mechanical tension; Stress fiber; Wound healing

Indexed keywords

ACTIN BINDING PROTEIN; ALPHA SMOOTH MUSCLE ACTIN; BLEBBISTATIN; CALPONIN 3; MESSENGER RNA; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MOTILITY; CELL PROLIFERATION; CONTROLLED STUDY; GENE EXPRESSION; GENE SILENCING; IN SITU HYBRIDIZATION; MOUSE; MUSCLE FIBER CONTRACTION; MYOFIBROBLAST; NEWBORN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKIN FIBROBLAST; STRESS FIBER; TENSION; TRANSCRIPTION REGULATION; WOUND HEALING;

ACTIN CYTOSKELETON; ACTINS; ANIMALS; CALCIUM-BINDING PROTEINS; CELL MOVEMENT; CELLS, CULTURED; DERMIS; FIBROBLASTS; GRANULATION TISSUE; HETEROCYCLIC COMPOUNDS WITH 4 OR MORE RINGS; MICE; MICROFILAMENT PROTEINS; MUSCLE CONTRACTION; MYOFIBROBLASTS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, SMALL INTERFERING; STRESS FIBERS; WOUND HEALING;

EID: 84883242384     PISSN: 03403696     EISSN: 1432069X     Source Type: Journal    
DOI: 10.1007/s00403-013-1343-8     Document Type: Article

References (54)

1. Appel S, Allen PG, Vetterkind S, Jin JP, Morgan KG (2010) h3/Acidic calponin: an actin-binding protein that controls extracellular signal-regulated kinase 1/2 activity in nonmuscle cells. Mol Biol Cell 21(8):1409-1422
2. Applegate D, Feng W, Green RS, Taubman MB (1994) Cloning and expression of a novel acidic calponin isoform from rat aortic vascular smooth muscle. J Biol Chem 269(14):10683-10690
3. Barisic-Dujmovic T, Boban I, Clark SH (2010) Fibroblasts/myofibroblasts that participate in cutaneous wound healing are not derived from circulating progenitor cells. J Cell Physiol 222(3):703-712
4. Byers HR, White GE, Fujiwara K (1984) Organization and function of stress fibers in cells in vitro and in situ. A review. Cell Muscle Motil 5:83-137
5. Condeelis J, Singer RH (2005) How and why does beta-actin mRNA target? Biol Cell 97(1):97-110
6. Cramer LP, Siebert M, Mitchison TJ (1997) Identification of novel graded polarity actin filament bundles in locomoting heart fibroblasts: implications for the generation of motile force. J Cell Biol 136(6):1287-1305
7. Danninger C, Gimona M (2000) Live dynamics of GFP-calponin: isoform-specific modulation of the actin cytoskeleton and autoregulation by C-terminal sequences. J Cell Sci 113(Pt 21):3725-3736
8. Desmouliere A, Redard M, Darby I, Gabbiani G (1995) Apoptosis mediates the decrease in cellularity during the transition between granulation tissue and scar. Am J Pathol 146(1):56-66
9. Ehrlich HP, Hembry RM (1984) A comparative study of fibroblasts in healing freeze and burn injuries in rats. Am J Pathol 117(2):218-224
10. Ehrlich HP, Rajaratnam JB (1990) Cell locomotion forces versus cell contraction forces for collagen lattice contraction: an in vitro model of wound contraction. Tissue Cell 22(4):407-417
11. Gabbiani G (2003) The myofibroblast in wound healing and fibrocontractive diseases. J Pathol 200(4):500-503
12. Griffin MA, Sen S, Sweeney HL, Discher DE (2004) Adhesion-contractile balance in myocyte differentiation. J Cell Sci 117(Pt 24):5855-5863
13. Hinz B (2007) Formation and function of the myofibroblast during tissue repair. J Invest Dermatol 127(3):526-537
14. Hinz B, Celetta G, Tomasek JJ, Gabbiani G, Chaponnier C (2001) Alpha-smooth muscle actin expression upregulates fibroblast contractile activity. Mol Biol Cell 12(9):2730-2741
15. Hinz B, Mastrangelo D, Iselin CE, Chaponnier C, Gabbiani G (2001) Mechanical tension controls granulation tissue contractile activity and myofibroblast differentiation. Am J Pathol 159(3):1009-1020
16. Hossain MM, Crish JF, Eckert RL, Lin JJ, Jin JP (2005) h2-Calponin is regulated by mechanical tension and modifies the function of actin cytoskeleton. J Biol Chem 280(51):42442-42453
17. Hossain MM, Smith PG, Wu K, Jin JP (2006) Cytoskeletal tension regulates both expression and degradation of h2-calponin in lung alveolar cells. Biochemistry 45(51):15670-15683
18. Huang QQ, Hossain MM, Wu K, Parai K, Pope RM, Jin JP (2008) Role of H2-calponin in regulating macrophage motility and phagocytosis. J Biol Chem 283(38):25887-25899
19. Huttelmaier S, Zenklusen D, Lederer M, Dictenberg J, Lorenz M, Meng X, Bassell GJ, Condeelis J, Singer RH (2005) Spatial regulation of beta-actin translation by Src-dependent phosphorylation of ZBP1. Nature 438(7067):512-515
20. Kaneko T, Amano M, Maeda A, Goto H, Takahashi K, Ito M, Kaibuchi K (2000) Identification of calponin as a novel substrate of Rho-kinase. Biochem Biophys Res Commun 273(1):110-116
21. Katoh K, Kano Y, Amano M, Onishi H, Kaibuchi K, Fujiwara K (2001) Rho-kinase-mediated contraction of isolated stress fibers. J Cell Biol 153(3):569-584
22. Katoh K, Kano Y, Masuda M, Onishi H, Fujiwara K (1998) Isolation and contraction of the stress fiber. Mol Biol Cell 9(7):1919-1938
23. Kislauskis EH, Zhu X, Singer RH (1994) Sequences responsible for intracellular localization of beta-actin messenger RNA also affect cell phenotype. J Cell Biol 127(2):441-451
24. Kovacs M, Toth J, Hetenyi C, Malnasi-Csizmadia A, Sellers JR (2004) Mechanism of blebbistatin inhibition of myosin II. J Biol Chem 279(34):35557-35563
25. Kreis TE, Birchmeier W (1980) Stress fiber sarcomeres of fibroblasts are contractile. Cell 22(2 Pt 2):555-561
26. Lauffenburger DA, Horwitz AF (1996) Cell migration: a physically integrated molecular process. Cell 84(3):359-369
27. Lawrence JB, Singer RH (1986) Intracellular localization of messenger RNAs for cytoskeletal proteins. Cell 45(3):407-415
28. Leung T, Chen XQ, Manser E, Lim L (1996) The p160 RhoA-binding kinase ROK alpha is a member of a kinase family and is involved in the reorganization of the cytoskeleton. Mol Cell Biol 16(10):5313-5327
29. Leung T, Manser E, Tan L, Lim L (1995) A novel serine/threonine kinase binding the Ras-related RhoA GTPase which translocates the kinase to peripheral membranes. J Biol Chem 270(49):29051-29054
30. Li B, Wang JH (2011) Fibroblasts and myofibroblasts in wound healing: force generation and measurement. J Tissue Viability 20(4):108-120
31. Liu Z, van Grunsven LA, Van Rossen E, Schroyen B, Timmermans JP, Geerts A, Reynaert H (2010) Blebbistatin inhibits contraction and accelerates migration in mouse hepatic stellate cells. Br J Pharmacol 159(2):304-315
32. Martinez-Ferrer M, Afshar-Sherif AR, Uwamariya C, de Crombrugghe B, Davidson JM, Bhowmick NA (2009) Dermal transforming growth factor-beta responsiveness mediates wound contraction and epithelial closure. Am J Pathol 176(1):98-107
33. Miyoshi H (2004) Gene delivery to hematopoietic stem cells using lentiviral vectors. Methods Mol Biol 246:429-438
34. Morgan KG, Gangopadhyay SS (2001) Invited review: cross-bridge regulation by thin filament-associated proteins. J Appl Physiol 91(2):953-962
35. Patel VL, Mitra S, Harris R, Buxbaum AR, Lionnet T, Brenowitz M, Girvin M, Levy M, Almo SC, Singer RH, Chao JA (2012) Spatial arrangement of an RNA zipcode identifies mRNAs under post-transcriptional control. Genes Dev 26(1):43-53
36. Paterson HF, Self AJ, Garrett MD, Just I, Aktories K, Hall A (1990) Microinjection of recombinant p21rho induces rapid changes in cell morphology. J Cell Biol 111(3):1001-1007
37. Pellegrin S, Mellor H (2007) Actin stress fibres. J Cell Sci 120(Pt 20):3491-3499
38. Rhee S, Grinnell F (2007) Fibroblast mechanics in 3D collagen matrices. Adv Drug Deliv Rev 59(13):1299-1305
39. Rodriguez AJ, Czaplinski K, Condeelis JS, Singer RH (2008) Mechanisms and cellular roles of local protein synthesis in mammalian cells. Curr Opin Cell Biol 20(2):144-149
40. Sandbo N, Dulin N (2011) Actin cytoskeleton in myofibroblast differentiation: ultrastructure defining form and driving function. Transl Res 158(4):181-196
41. Serini G, Gabbiani G (1999) Mechanisms of myofibroblast activity and phenotypic modulation. Exp Cell Res 250(2):273-283
42. Shibukawa Y, Yamazaki N, Daimon E, Wada Y (2012) Rock-dependent calponin 3 phosphorylation regulates myoblast fusion. Exp Cell Res 319(5):633-648
43. Shibukawa Y, Yamazaki N, Kumasawa K, Daimon E, Tajiri M, Okada Y, Ikawa M, Wada Y (2010) Calponin 3 regulates actin cytoskeleton rearrangement in trophoblastic cell fusion. Mol Biol Cell 21(22):3973-3984
44. Small JV, Gimona M (1998) The cytoskeleton of the vertebrate smooth muscle cell. Acta Physiol Scand 164(4):341-348
45. Strasser P, Gimona M, Moessler H, Herzog M, Small JV (1993) Mammalian calponin. Identification and expression of genetic variants. FEBS Lett 330(1):13-18
46. Takahashi K, Kaneko I (1986) DNA fragments of 300 base pairs released from metaphase chromosomes by digestion with deoxyribonuclease I. Biochem Biophys Res Commun 138(1):413-418
47. Tang J, Hu G, Hanai J, Yadlapalli G, Lin Y, Zhang B, Galloway J, Bahary N, Sinha S, Thisse B, Thisse C, Jin JP, Zon LI, Sukhatme VP (2006) A critical role for calponin 2 in vascular development. J Biol Chem 281(10):6664-6672
48. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA (2002) Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 3(5):349-363
49. Tomasek JJ, Haaksma CJ, Eddy RJ, Vaughan MB (1992) Fibroblast contraction occurs on release of tension in attached collagen lattices: dependency on an organized actin cytoskeleton and serum. Anat Rec 232(3):359-368
50. Watanabe N, Kato T, Fujita A, Ishizaki T, Narumiya S (1999) Cooperation between mDia1 and ROCK in Rho-induced actin reorganization. Nat Cell Biol 1(3):136-143
51. Winder SJ, Allen BG, Fraser ED, Kang HM, Kargacin GJ, Walsh MP (1993) Calponin phosphorylation in vitro and in intact muscle. Biochem J 296(Pt 3):827-836
52. Yeung T, Georges PC, Flanagan LA, Marg B, Ortiz M, Funaki M, Zahir N, Ming W, Weaver V, Janmey PA (2005) Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil Cytoskeleton 60(1):24-34
53. Yoshimoto R, Hori M, Ozaki H, Karaki H (2000) Proteolysis of acidic calponin by mu-calpain. J Biochem 128(6):1045-1049
54. Zufferey R, Nagy D, Mandel RJ, Naldini L, Trono D (1997) Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat Biotechnol 15(9):871-875