Lumican binds ALK5 to promote epithelium wound healing

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Yamanaka, Osamu ^a   Yuan, Yong ^a   Coulson Thomas, Vivien Jane ^a   Gesteira, Tarsis Ferreira ^b   Call, Mindy K ^a   Zhang, Yujin ^a   Zhang, Jianhua ^a   Chang, Shao Hsuan ^a   Xie, Changchun ^a   Liu, Chia Yang ^a   Saika, Shizuya ^c   Jester, James V ^d   Kao, Winston W Y ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^c WAKAYAMA MEDICAL UNIVERSITY   (Japan)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LUMICAN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BINDING AFFINITY; CELL CYCLE; CELL MIGRATION; CELL PROLIFERATION; EPITHELIUM CELL; ESCHERICHIA COLI; GLYCOSYLATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; WOUND HEALING;

ADULT; AGED; ANIMALS; BLOTTING, WESTERN; CELL LINE; CELLS, CULTURED; CHONDROITIN SULFATE PROTEOGLYCANS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; KERATAN SULFATE; MALE; MICE; MICE, KNOCKOUT; MIDDLE AGED; MOLECULAR DYNAMICS SIMULATION; PROTEIN-SERINE-THREONINE KINASES; PROTEOGLYCANS; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; WOUND HEALING;

EID: 84893194712     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082730     Document Type: Article

References (89)

1. Kao WW, Liu CY (2002) Roles of lumican and keratocan on corneal transparency. Glycoconj J 19: 275-285. (Pubitemid 37174556)
2. Kao WW, Funderburgh JL, Xia Y, Liu CY, Conrad GW (2006) Focus on molecules: lumican. Exp Eye Res 82: 3-4. (Pubitemid 43063391)
3. Saika S, Shiraishi A, Saika S, Liu C-Y, Funderburgh JL, et al. (2000) Role of Lumican in the Corneal Epithelium during Wound Healing. J Biol Chem 275: 2607-2612. (Pubitemid 30082027)
4. Moreth K, Iozzo RV, Schaefer L (2012) Small leucine-rich proteoglycans orchestrate receptor crosstalk during inflammation. Cell Cycle 11: 2084-2091. 20316 [pii];10.4161/cc.20316 [doi].
5. Chen S, Birk DE (2013) The regulatory roles of small leucine-rich proteoglycans in extracellular assembly. FEBS J. 10.1111/febs.12136 [doi].
6. Chen S, Sun M, Iozzo RV, Kao WW, Birk DE (2013) Intracellularly-Retained Decorin Lacking the C-Terminal Ear Repeat Causes ER Stress: A Cell-Based Etiological Mechanism for Congenital Stromal Corneal Dystrophy. Am J Pathol 183: 247-256. S0002-9440(13)00267-8 [pii];10.1016/j.ajpath.2013.04.001 [doi].
7. Dellett M, Hu W, Papadaki V, Ohnuma S (2012) Small leucine rich proteoglycan family regulates multiple signalling pathways in neural development and maintenance. Dev Growth Differ 54: 327-340. 10.1111/j.1440-169X.2012.01339. x [doi].
8. Feugaing DD, Tammi R, Echtermeyer FG, Stenmark H, Kresse H, et al. (2007) Endocytosis of the dermatan sulfate proteoglycan decorin utilizes multiple pathways and is modulated by epidermal growth factor receptor signaling. Biochimie 89: 637-657. S0300-9084(07)00012-0 [pii];10.1016/j.biochi.2006.12.012 [doi].
9. Schaefer L, Grone HJ, Raslik I, Robenek H, Ugorcakova J, et al. (2000) Small proteoglycans of normal adult human kidney: distinct expression patterns of decorin, biglycan, fibromodulin, and lumican. Kidney Int 58: 1557-1568.
10. Bidanset DJ, Guidry C, Rosenberg LC, Choi HU, Timpl R, et al. (1992) Binding of the proteoglycan decorin to collagen type VI. J Biol Chem 267: 5250-5256.
11. Font B, Eichenberger D, Rosenberg LM, van der Rest M (1996) Characterization of the interactions of type XII collagen with two small proteoglycans from fetal bovine tendon, decorin and fibromodulin. Matrix Biol 15: 341-348. (Pubitemid 26419879)
12. Ehnis T, Dieterich W, Bauer M, Kresse H, Schuppan D (1997) Localization of a binding site for the proteoglycan decorin on collagen XIV (undulin). J Biol Chem 272: 20414-20419. (Pubitemid 27355593)
13. Font B, Aubert-Foucher E, Goldschmidt D, Eichenberger D, van der Rest M (1993) Binding of collagen XIV with the dermatan sulfate side chain of decorin. Journal of Biological Chemistry 268: 25015-25018. (Pubitemid 23335523)
14. Schmidt G, Hausser H, Kresse H (1991) Interaction of the small proteoglycan decorin with fibronectin. Involvement of the sequence NKISK of the core protein. Biochem J 280 (Pt 2): 411-414.
15. Groeneveld TWL, Oroszl+ín M, Owens RT, Faber-Krol MC, Bakker AC, et al.(2005) Interactions of the Extracellular Matrix Proteoglycans Decorin and Biglycan with C1q and Collectins. J Immunol 175: 4715-4723.
16. Casar JC, McKechnie BA, Fallon JR, Young MF, Brandan E (2004) Transient up-regulation of biglycan during skeletal muscle regeneration: delayed fiber growth along with decorin increase in biglycan-deficient mice. Dev Biol 268: 358-371. (Pubitemid 38519849)
17. Sulochana KN, Fan H, Jois S, Vivekanandan S, Sun F, et al. (2005) Peptides derived from human decorin leucine rich repeat 5 inhibit angiogenesis. J Biol Chem.
18. Gressner AM, Krull N, Bachem MG (1994) Regulation of proteoglycan expression in fibrotic liver and cultured fat-storing cells. [Review] [31 refs]. Pathology, Research & Practice 190: 864-882. (Pubitemid 24370097)
19. Santra M, Eichstetter I, Iozzo RV (2000) An anti-oncogenic role for decorin: downregulation of ErbB2 leads to growth suppression and cytodifferentiation of mammary carcinoma cells. J Biol Chem.
20. Santra M, Reed CC, Iozzo RV (2002) Decorin binds to a narrow region of the epidermal growth factor (EGF) receptor, partially overlapping but distinct from the EGF-binding epitope. J Biol Chem 277: 35671-35681. 10.1074/jbc. M205317200 [doi];M205317200 [pii].
21. Tralhao JG, Schaefer L, Micegova M, Evaristo C, Schonherr E, et al. (2003) In vivo selective and distant killing of cancer cells using adenovirus-mediated decorin gene transfer. FASEB J 17: 464-466. 10.1096/fj.02-0534fje [doi];02-0534fje [pii].
22. Schonherr E, Sunderkotter C, Iozzo RV, Schaefer L (2005) Decorin, a novel player in the insulin-like growth factor system. J Biol Chem 280: 15767-15772. M500451200 [pii];10.1074/jbc.M500451200 [doi].
23. Hayashi Y, Liu CY, Jester JJ, Hayashi M, Wang IJ, et al.(2005) Excess biglycan causes eyelid malformation by perturbing muscle development and TGF-alpha signaling. Dev Biol 277: 222-234. (Pubitemid 39574265)
24. Hildebrand A, Romaris M, Rasmussen LM, Heinegard D, Twardzik DR, et al. (1994) Interaction of the small interstitial proteoglycans biglycan, decorin and fibromodulin with transforming growth factor beta. Biochem J 302 (Pt 2): 527-534. (Pubitemid 24280108)
25. Schaefer L, Babelova A, Kiss E, Hausser HJ, Baliova M, et al. (2005) The matrix component biglycan is proinflammatory and signals through Toll-like receptors 4 and 2 in macrophages. J Clin Invest 115: 2223-2233. 10.1172/JCI23755 [doi]. (Pubitemid 41134165)
26. Chen Z, de Paiva CS, Luo L, Kretzer FL, Pflugfelder SC, et al. (2004) Characterization of putative stem cell phenotype in human limbal epithelia. Stem Cells 22: 355-366. (Pubitemid 38736619)
27. Moreno M, Munoz R, Aroca F, Labarca M, Brandan E, et al. (2005) Biglycan is a new extracellular component of the Chordin-BMP4 signaling pathway. EMBO J 24: 1397-1405. 7600615 [pii];10.1038/sj.emboj.7600615 [doi].
28. Chakravarti S, Magnuson T, Lass JH, Jepsen KJ, LaMantia C, et al. (1998) Lumican regulates collagen fibril assembly: skin fragility and corneal opacity in the absence of lumican. J Cell Biol 141: 1277-1286. (Pubitemid 28265620)
29. Liu H, Zhang J, Liu CY, Wang IJ, Sieber M, et al. (2010) Cell therapy of congenital corneal diseases with umbilical mesenchymal stem cells: lumican null mice. PLoS ONE 5: e10707. 10.1371/journal.pone.0010707 [doi].
30. Yeh JT, Yeh LK, Jung SM, Chang TJ, Wu HH, et al. (2010) Impaired skin wound healing in lumican-null mice. Br J Dermatol 163: 1174-1180. BJD10008 [pii];10.1111/j.1365-2133.2010.10008.x [doi].
31. Austin BA, Coulon C, Liu CY, Kao WW, Rada JA (2002) Altered collagen fibril formation in the sclera of lumican-deficient mice. !Lost Data 43: 1695-1701. (Pubitemid 34587008)
32. Carlson EC, Liu CY, Chikama T, Hayashi Y, Kao CW, et al. (2005) Keratocan, a cornea-specific keratan sulfate proteoglycan, is regulated by lumican. J Biol Chem 280: 25541-25547. (Pubitemid 40962260)
33. Carlson EC, Lin M, Liu CY, Kao WW, Perez VL, et al. (2007) Keratocan and lumican regulate neutrophil infiltration and corneal clarity in lipopolysaccharide- induced keratitis by direct interaction with CXCL1. J Biol Chem 282: 35502-35509. (Pubitemid 350277127)
34. Carlson EC, Sun Y, Auletta J, Kao WW, Liu CY, et al. (2010) Regulation of corneal inflammation by neutrophil-dependent cleavage of keratan sulfate proteoglycans as a model for breakdown of the chemokine gradient. J Leukoc Biol. jlb.0310134 [pii];10.1189/jlb.0310134 [doi].
35. Hayashi Y, Call MK, Chikama T, Liu H, Carlson EC, et al. (2010) Lumican is required for neutrophil extravasation following corneal injury and wound healing. J Cell Sci 123: 2987-2995. jcs.068221 [pii];10.1242/jcs.068221 [doi].
36. Meij JT, Carlson EC, Wang L, Liu CY, Jester JV, et al. (2007) Targeted expression of a lumican transgene rescues corneal deficiencies in lumican-null mice. Mol Vis 13: 2012-2018. (Pubitemid 350011658)
37. Saika S, Miyamoto T, Tanaka S, Tanaka T, Ishida I, et al. (2003) Response of lens epithelial cells to injury: role of lumican in epithelial-mesenchymal transition. !Lost Data 44: 2094-2102. (Pubitemid 36520304)
38. Yeh LK, Chen WL, Li W, Espana EM, Ouyang J, et al. (2005) Soluble lumican glycoprotein purified from human amniotic membrane promotes corneal epithelial wound healing. Invest Ophthalmol Vis Sci 46: 479-486. 46/2/479 [pii];10.1167/iovs.04-1014 [doi].
39. Lohr K, Sardana H, Lee S, Wu F, Huso DL, et al. (2012) Extracellular matrix protein lumican regulates inflammation in a mouse model of colitis. Inflamm Bowel Dis 18: 143-151. 10.1002/ibd.21713 [doi].
40. Wu F, Vij N, Roberts L, Lopez-Briones S, Joyce S, et al. (2007) A novel role of the lumican core protein in bacterial lipopolysaccharide-induced innate immune response. J Biol Chem 282: 26409-26417. M702402200 [pii];10.1074/jbc. M702402200 [doi].
41. Wu F, Chakravarti S (2007) Differential expression of inflammatory and fibrogenic genes and their regulation by NF-kappaB inhibition in a mouse model of chronic colitis. J Immunol 179: 6988-7000. 179/10/6988 [pii].
42. Funderburgh JL, Mitschler RR, Funderburgh ML, Roth MR, Chapes SK, et al. (1997) Macrophage receptors for lumican. A corneal keratan sulfate proteoglycan. Invest Ophthalmol Vis Sci 38: 1159-1167. (Pubitemid 27227045)
43. Saika S, Okada Y, Miyamoto T, Yamanaka O, Ohnishi Y, et al. (2004) Role of p38 MAP Kinase in Regulation of Cell Migration and Proliferation in Healing Corneal Epithelium. Invest Ophthalmol Vis Sci 45: 100-109. (Pubitemid 38055674)
44. Terai K, Call MK, Liu H, Saika S, Liu CY, et al. (2011) Crosstalk between TGF-{beta} and MAPK Signaling during Corneal Wound Healing. Invest Ophthalmol Vis Sci. iovs.11-8017 [pii];10.1167/iovs.11-8017 [doi].
45. Hayashi Y, Call M, Liu CY, Hayashi M, Babcock G, et al. (2010) Monoallelic Expression of Krt12 Gene during Corneal-type Epithelium Differentiation of Limbal Stem Cells. Invest Ophthalmol Vis Sci. iovs.10-5331 [pii];10.1167/iovs.10-5331 [doi].
46. Seomun Y, Joo CK (2008) Lumican induces human corneal epithelial cell migration and integrin expression via ERK 1/2 signaling. Biochem Biophys Res Commun 372: 221-225. S0006-291X(08)00924-8 [pii];10.1016/j.bbrc.2008.05.014 [doi].
47. Radwanska A, Baczynska D, Nowak D, Brezillon S, Popow A, et al. (2008) Lumican affects actin cytoskeletal organization in human melanoma A375 cells. Life Sci 83: 651-660. S0024-3205(08)00371-8 [pii];10.1016/j.lfs.2008.09.008 [doi].
48. Radwanska A, Litwin M, Nowak D, Baczynska D, Wegrowski Y, et al. (2012) Overexpression of lumican affects the migration of human colon cancer cells through up-regulation of gelsolin and filamentous actin reorganization. Exp Cell Res 318: 2312-2323. S0014-4827(12)00325-4 [pii];10.1016/j.yexcr.2012.07.005 [doi].
49. Coulson-Thomas VJ, Coulson-Thomas YM, Gesteira TF, Andrade de Paula CA, Carneiro CR, et al. (2013) Lumican expression, localization and antitumor activity in prostate cancer. Exp Cell Res 319: 967-981. S0014-4827(13)00041-4 [pii];10.1016/j.yexcr.2013.01.023 [doi].
50. yamamoto t, Matsuda Y, Kawahara K, Ishiwata T, Naito Z (2012) Secreted 70kDa lumican stimulates growth and inhibits invasion of human pancreatic cancer. Cancer Lett 320: 31-39. S0304-3835(12)00056-0 [pii];10.1016/j.canlet. 2012.01.023 [doi].
51. Nikitovic D, Chalkiadaki G, Berdiaki A, Aggelidakis J, Katonis P, et al. (2011) Lumican regulates osteosarcoma cell adhesion by modulating TGFbeta2 activity. Int J Biochem Cell Biol 43: 928-935. S1357-2725(11)00084-7 [pii];10.1016/j.biocel.2011.03.008 [doi].
52. Robertson DM, Li L, Fisher S, Pearce VP, Shay JW, et al. (2005) Characterization of growth and differentiation in a telomerase-immortalized human corneal epithelial cell line. Invest Ophthalmol Vis Sci 46: 470-478. 46/2/470 [pii];10.1167/iovs.04-0528 [doi].
53. Tuli SS, Liu R, Chen C, Blalock TD, Goldstein M, et al. (2006) Immunohistochemical localization of EGF, TGF-alpha, TGF-beta, and their receptors in rat corneas during healing of excimer laser ablation. Curr Eye Res 31: 709-719. (Pubitemid 44373542)
54. Zelenka PS, Arpitha P (2008) Coordinating cell proliferation and migration in the lens and cornea. Semin Cell Dev Biol 19: 113-124. S1084-9521(07)00159-0 [pii];10.1016/j.semcdb.2007.10.001 [doi].
55. Kane CJ, Hebda PA, Mansbridge JN, Hanawalt PC (1991) Direct evidence for spatial and temporal regulation of transforming growth factor beta 1 expression during cutaneous wound healing. J Cell Physiol 148: 157-173. 10.1002/jcp.1041480119 [doi]. (Pubitemid 21910138)
56. Ciacci C, Lind SE, Podolsky DK (1993) Transforming growth factor beta regulation of migration in wounded rat intestinal epithelial monolayers. Gastroenterology 105: 93-101. S0016508593002392 [pii].
57. Zieske JD, Hutcheon AEK, Guo X, Chung EH, Joyce NC (2001) TGF-+| Receptor Types I and II Are Differentially Expressed during Corneal Epithelial Wound Repair. Invest Ophthalmol Vis Sci 42: 1465-1471. (Pubitemid 32520736)
58. Secker GA, Shortt AJ, Sampson E, Schwarz QP, Schultz GS, et al. (2008) TGFbeta stimulated re-epithelialisation is regulated by CTGF and Ras/MEK/ERK signalling. Exp Cell Res 314: 131-142. S0014-4827(07)00411-9 [pii];10.1016/j.yexcr.2007.09.001 [doi].
59. Saika S, Okada Y, Miyamoto T, Ooshima A, McAvoy JW (2001) Smad translocation and growth suppression in lens epithelial cells by endogenous TGFbeta2 during wound repair. Exp Eye Res 72: 679-686. (Pubitemid 32977214)
60. Hutcheon AE, Guo XQ, Stepp MA, Simon KJ, Weinreb PH, et al. (2005) Effect of wound type on Smad 2 and 4 translocation. !Lost Data 46: 2362-2368. (Pubitemid 43119481)
61. Feng XH, Lin X, Derynck R (2000) Smad2, Smad3 and Smad4 cooperate with Sp1 to induce p15(Ink4B) transcription in response to TGF-beta. EMBO J 19: 5178-5193. 10.1093/emboj/19.19.5178 [doi].
62. Wang T, Li BY, Danielson PD, Shah PC, Rockwell S, et al. (1996) The immunophilin FKBP12 functions as a common inhibitor of the TGF beta family type I receptors. Cell 86: 435-444. S0092-8674(00)80116-6 [pii].
63. Chen YG, Liu F, Massague J (1997) Mechanism of TGFbeta receptor inhibition by FKBP12. EMBO J 16: 3866-3876. 10.1093/emboj/16.13.3866 [doi]. (Pubitemid 27281003)
64. Huse M, Muir TW, Xu L, Chen YG, Kuriyan J, et al. (2001) The TGF beta receptor activation process: an inhibitor- to substrate-binding switch. Mol Cell 8: 671-682. S1097-2765(01)00332-X [pii].
65. Lee MK, Pardoux C, Hall MC, Lee PS, Warburton D, et al. (2007) TGF-beta activates Erk MAP kinase signalling through direct phosphorylation of ShcA. EMBO J 26: 3957-3967. 7601818 [pii];10.1038/sj.emboj.7601818 [doi].
66. Derynck R, Zhang YE (2003) Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 425: 577-584. (Pubitemid 37280136)
67. Yu L, Hebert MC, Zhang YE (2002) TGF-beta receptor-activated p38 MAP kinase mediates Smad-independent TGF-beta responses. EMBO J 21: 3749-3759. (Pubitemid 34787048)
68. Zhang YE (2009) Non-Smad pathways in TGF-beta signaling. Cell Res 19: 128-139. cr2008328 [pii];10.1038/cr.2008.328 [doi].
69. Csordas G, Santra M, Reed CC, Eichstetter I, McQuillan DJ, et al. (2000) Sustained downregulation of the epidermal growth factor receptor by decorin: A mechanism for controlling tumor growth in vivo. J Biol Chem.
70. Iozzo RV, Moscatello DK, McQuillan DJ, Eichstetter I (1999) Decorin is a biological ligand for the epidermal growth factor receptor. J Biol Chem 274: 4489-4492.
71. Carlson EC, Mamiya K, Liu CY, Gendron RL, Birk DE, et al. (2003) Role of Cys41 in the N-terminal domain of lumican in ex vivo collagen fibrillogenesis by cultured corneal stromal cells. Biochem J 369: 461-468. (Pubitemid 36246229)
72. Scott PG, McEwan PA, Dodd CM, Bergmann EM, Bishop PN, et al. (2004) Crystal structure of the dimeric protein core of decorin, the archetypal small leucine-rich repeat proteoglycan. Proc Natl Acad Sci U S A 101: 15633-15638. 0402976101 [pii];10.1073/pnas.0402976101 [doi].
73. Gesteira TF, Coulson-Thomas VJ, Ogata FT, Farias EH, Cavalheiro RP, et al. (2011) A novel approach for the characterisation of proteoglycans and biosynthetic enzymes in a snail model. Biochim Biophys Acta 1814: 1862-1869. S1570-9639(11)00219-6 [pii];10.1016/j.bbapap.2011.07.024 [doi].
74. Shen MY, Sali A (2006) Statistical potential for assessment and prediction of protein structures. Protein Sci 15: 2507-2524. 15/11/2507 [pii];10.1110/ps.062416606 [doi].
75. van der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, et al. (2005) GROMACS: fast, flexible, and free. J Comput Chem 26: 1701-1718. 10.1002/jcc.20291 [doi]. (Pubitemid 43076182)
76. Fraternali F, van Gunsteren WF (1996) An efficient mean solvation force model for use in molecular dynamics simulations of proteins in aqueous solution. J Mol Biol 256: 939-948. S0022-2836(96)90139-4 [pii];10.1006/jmbi.1996.0139 [doi].
77. Peng JW, Schiffer CA, Xu P, van Gunsteren WF, Ernst RR (1996) Investigations of peptide hydration using NMR and molecular dynamics simulations: A study of effects of water on the conformation and dynamics of antamanide. J Biomol NMR 8: 453-476. 10.1007/BF00228147 [doi]. (Pubitemid 126706800)
78. Roth GJ, Heckel A, Brandl T, Grauert M, Hoerer S, et al. (2010) Design, synthesis, and evaluation of indolinones as inhibitors of the transforming growth factor beta receptor I (TGFbetaRI). J Med Chem 53: 7287-7295. 10.1021/jm100812a [doi].
79. Radaev S, Zou Z, Huang T, Lafer EM, Hinck AP, et al. (2010) Ternary complex of transforming growth factor-beta1 reveals isoform-specific ligand recognition and receptor recruitment in the superfamily. J Biol Chem 285: 14806-14814. M109.079921 [pii];10.1074/jbc.M109.079921 [doi].
80. London NaS-FO (2012) Chapter 8: High-resolution Protein-ProteinDocking. in Protein-Proten Complexes: Snalysis, Modeling and Drug Design, M. Zacharias, ed. 209-235.
81. Gesteira TF, Pol-Fachin L, Coulson-Thomas VJ, Lima MA, Verli H, et al. (2013) Insights into the N-sulfation mechanism: molecular dynamics simulations of the N-sulfotransferase domain of ndst1 and mutants. PLoS One 8: e70880. 10.1371/journal.pone.0070880 [doi];PONE-D-13-03843 [pii].
82. Berendsen HJC (1987) Biophysical Applications of Molecular-Dynamics. Computer Physics Communications 44: 233-242.
83. de Groot BL, Grubmuller H (2001) Water permeation across biological membranes: mechanism and dynamics of aquaporin-1 and GlpF. Science 294: 2353-2357. 10.1126/science.1062459 [doi];294/5550/2353 [pii].
84. Hess B, Bekker H, Berendsen HJC, Fraaije JGEM (1997) LINCS: A linear constraint solver for molecular simulations. Journal of Computational Chemistry 18: 1463-1472. (Pubitemid 127637344)
85. Darden T, York D, Pedersen L (1993) Particle Mesh Ewald - An N.Log(N) Method for Ewald Sums in Large Systems. Journal of Chemical Physics 98: 10089-10092.
86. Berendsen HJC, Postma JPM, Vangunsteren WF, Dinola A, Haak JR (1984) Molecular-Dynamics with Coupling to An External Bath. Journal of Chemical Physics 81: 3684-3690.
87. Humphrey W, Dalke A, Schulten K (1996) VMD: Visual molecular dynamics. Journal of Molecular Graphics & Modelling 14: 33-38. (Pubitemid 26152973)
88. Zhang Y, Kao WW, Pelosi E, Schlessinger D, Liu CY (2011) Notch gain of function in mouse periocular mesenchyme downregulates FoxL2 and impairs eyelid levator muscle formation, leading to congenital blepharophimosis. J Cell Sci 124: 2561-2572. jcs.085001 [pii];10.1242/jcs.085001 [doi].
89. Everitt BS (2002) Cambridge Dictionary of Statistics (2nd ed.). Cambridge, New York: Cambridge University Press.