Gene signatures in wound tissue as evidenced by molecular profiling in the chick embryo model

BMC Genomics

Volumn 11, Issue 1, 2010, Pages

  Soulet, Fabienne ^a,b   Kilarski, Witold W ^a,b   Antczak, Philipp ^c   Herbert, John ^c   Bicknell, Roy ^c   Falciani, Francesco ^c   Bikfalvi, Andreas ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MOTION; CHORIOALLANTOIS; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DOWN REGULATION; EMBRYO; ENDOTHELIUM CELL; FEMALE; GENE CONTROL; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GRANULATION TISSUE; HISTOPATHOLOGY; IMMUNE SYSTEM; INFLAMMATORY DISEASE; MOLECULAR GENETICS; NONHUMAN; NUCLEOTIDE SEQUENCE; TISSUE INJURY; TISSUE REGENERATION; TISSUE STRUCTURE; UPREGULATION; WOUND HEALING; ANIMAL; BIOLOGICAL MODEL; BIOLOGY; CHICK EMBRYO; CLUSTER ANALYSIS; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; METABOLISM; PATHOLOGY;

ANIMALS; CHICK EMBRYO; CHORIOALLANTOIC MEMBRANE; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; DOWN-REGULATION; ENDOTHELIAL CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; GRANULATION TISSUE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MODELS, BIOLOGICAL; UP-REGULATION; WOUND HEALING;

EID: 77956456399     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-11-495     Document Type: Article

References (74)

1. Martin P, Leibovich SJ. Inflammatory cells during wound repair: the good, the bad and the ugly. Trends Cell Biol 2005, 15(11):599-607. 10.1016/j.tcb.2005.09.002, 16202600.
2. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 2002, 3(5):349-363. 10.1038/nrm809, 11988769.
3. Singer AJ, Clark RA. Cutaneous wound healing. N Engl J Med 1999, 341(10):738-746. 10.1056/NEJM199909023411006, 10471461.
4. Virag JI, Murry CE. Myofibroblast and endothelial cell proliferation during murine myocardial infarct repair. The American journal of pathology 2003, 163(6):2433-2440. 1892355, 14633615.
5. Menke NB, Ward KR, Witten TM, Bonchev DG, Diegelmann RF. Impaired wound healing. Clin Dermatol 2007, 25(1):19-25. 10.1016/j.clindermatol.2006.12.005, 17276197.
6. Ribatti D. Chick embryo chorioallantoic membrane as a useful tool to study angiogenesis. Int Rev Cell Mol Biol 2008, 270:181-224. full_text, 19081537.
7. Jones EA, le Noble F, Eichmann A. What determines blood vessel structure? Genetic prespecification vs. hemodynamics. Physiology (Bethesda) 2006, 21:388-395.
8. Redd MJ, Cooper L, Wood W, Stramer B, Martin P. Wound healing and inflammation: embryos reveal the way to perfect repair. Philosophical transactions of the Royal Society of London 2004, 359(1445):777-784. 10.1098/rstb.2004.1466, 1693361, 15293805.
9. Zijlstra A, Seandel M, Kupriyanova TA, Partridge JJ, Madsen MA, Hahn-Dantona EA, Quigley JP, Deryugina EI. Proangiogenic role of neutrophil-like inflammatory heterophils during neovascularization induced by growth factors and human tumor cells. Blood 2006, 107(1):317-327. 10.1182/blood-2005-04-1458, 1895349, 16174763.
10. Kilarski WW, Samolov B, Petersson L, Kvanta A, Gerwins P. Biomechanical regulation of blood vessel growth during tissue vascularization. Nat Med 2009, 15(6):657-664. 10.1038/nm.1985, 19483693.
11. Javerzat S, Franco M, Herbert J, Platonova N, Peille AL, Pantesco V, De Vos J, Assou S, Bicknell R, Bikfalvi A, et al. Correlating global gene regulation to angiogenesis in the developing chick extra-embryonic vascular system. PLoS One 2009, 4(11):e7856. 10.1371/journal.pone.0007856, 2774277, 19924294.
12. Saidi A, Javerzat S, Bellahcene A, De Vos J, Bello L, Castronovo V, Deprez M, Loiseau H, Bikfalvi A, Hagedorn M. Experimental anti-angiogenesis causes upregulation of genes associated with poor survival in glioblastoma. International journal of cancer 2008, 122(10):2187-2198.
13. Lawson A, England MA. Surface ectodermal wound healing in the chick embryo. Journal of anatomy 1998, 192(Pt 4):497-506. 10.1046/j.1469-7580.1998.19240497.x, 1467804, 9723977.
14. Martin P, Lewis J. Actin cables and epidermal movement in embryonic wound healing. Nature 1992, 360(6400):179-183. 10.1038/360179a0, 1436096.
15. Armstrong MT, Turlo K, Elges CJ, Dayton SM, Lee J, Armstrong PB. A novel form of epithelial wound healing of the embryonic epidermis. Experimental cell research 2006, 312(13):2415-2423. 10.1016/j.yexcr.2006.04.006, 16730706.
16. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4(1):44-57. 10.1038/nprot.2008.211, 19131956.
17. Dennis G, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 2003, 4(5):P3. 10.1186/gb-2003-4-5-p3, 12734009.
18. Lu P, Li L, Liu G, Zhang X, Mukaida N. Enhanced experimental corneal neovascularization along with aberrant angiogenic factor expression in the absence of IL-1 receptor antagonist. Investigative ophthalmology & visual science 2009, 50(10):4761-4768.
19. Song KW, Talamas FX, Suttmann RT, Olson PS, Barnett JW, Lee SW, Thompson KD, Jin S, Hekmat-Nejad M, Cai TZ, et al. The kinase activities of interleukin-1 receptor associated kinase (IRAK)-1 and 4 are redundant in the control of inflammatory cytokine expression in human cells. Mol Immunol 2009, 46(7):1458-1466. 10.1016/j.molimm.2008.12.012, 19181383.
20. Schweighofer B, Testori J, Sturtzel C, Sattler S, Mayer H, Wagner O, Bilban M, Hofer E. The VEGF-induced transcriptional response comprises gene clusters at the crossroad of angiogenesis and inflammation. Thromb Haemost 2009, 102(3):544-554. 2886966, 19718476.
21. Liu W, Ding I, Chen K, Olschowka J, Xu J, Hu D, Morrow GR, Okunieff P. Interleukin 1beta (IL1B) signaling is a critical component of radiation-induced skin fibrosis. Radiat Res 2006, 165(2):181-191. 10.1667/RR3478.1, 16435917.
22. Wiegand C, Schonfelder U, Abel M, Ruth P, Kaatz M, Hipler UC. Protease and pro-inflammatory cytokine concentrations are elevated in chronic compared to acute wounds and can be modulated by collagen type I in vitro. Archives of dermatological research 2009,
23. Koumas L, King AE, Critchley HO, Kelly RW, Phipps RP. Fibroblast heterogeneity: existence of functionally distinct Thy 1(+) and Thy 1(-) human female reproductive tract fibroblasts. The American journal of pathology 2001, 159(3):925-935. 1850439, 11549585.
24. Kofler S, Nickel T, Weis M. Role of cytokines in cardiovascular diseases: a focus on endothelial responses to inflammation. Clin Sci (Lond) 2005, 108(3):205-213. 10.1042/CS20040174, 15540988.
25. Martin D, Galisteo R, Gutkind JS. CXCL8/IL8 stimulates vascular endothelial growth factor (VEGF) expression and the autocrine activation of VEGFR2 in endothelial cells by activating NFkappaB through the CBM (Carma3/Bcl10/Malt1) complex. The Journal of biological chemistry 2009, 284(10):6038-6042. 10.1074/jbc.C800207200, 2649103, 19112107.
26. Lu Y, Yang W, Qin C, Zhang L, Deng J, Liu S, Qin Z. Responsiveness of stromal fibroblasts to IFN-gamma blocks tumor growth via angiostasis. J Immunol 2009, 183(10):6413-6421. 10.4049/jimmunol.0901073, 19841170.
27. Bujak M, Dobaczewski M, Gonzalez-Quesada C, Xia Y, Leucker T, Zymek P, Veeranna V, Tager AM, Luster AD, Frangogiannis NG. Induction of the CXC chemokine interferon-gamma-inducible protein 10 regulates the reparative response following myocardial infarction. Circulation research 2009, 105(10):973-983. 10.1161/CIRCRESAHA.109.199471, 19797174.
28. Elmasri H, Karaaslan C, Teper Y, Ghelfi E, Weng M, Ince TA, Kozakewich H, Bischoff J, Cataltepe S. Fatty acid binding protein 4 is a target of VEGF and a regulator of cell proliferation in endothelial cells. Faseb J 2009, 23(11):3865-3873. 10.1096/fj.09-134882, 19625659.
29. Wu Y, Li YY, Matsushima K, Baba T, Mukaida N. CCL3-CCR5 axis regulates intratumoral accumulation of leukocytes and fibroblasts and promotes angiogenesis in murine lung metastasis process. J Immunol 2008, 181(9):6384-6393.
30. Ryschich E, Lizdenis P, Ittrich C, Benner A, Stahl S, Hamann A, Schmidt J, Knolle P, Arnold B, Hammerling GJ, et al. Molecular fingerprinting and autocrine growth regulation of endothelial cells in a murine model of hepatocellular carcinoma. Cancer Res 2006, 66(1):198-211. 10.1158/0008-5472.CAN-05-1636, 16397233.
31. Yamaguchi S, Asanoma K, Takao T, Kato K, Wake N. Homeobox gene HOPX is epigenetically silenced in human uterine endometrial cancer and suppresses estrogen-stimulated proliferation of cancer cells by inhibiting serum response factor. International journal of cancer 2009, 124(11):2577-2588.
32. Liu F, Levin MD, Petrenko NB, Lu MM, Wang T, Yuan LJ, Stout AL, Epstein JA, Patel VV. Histone-deacetylase inhibition reverses atrial arrhythmia inducibility and fibrosis in cardiac hypertrophy independent of angiotensin. J Mol Cell Cardiol 2008, 45(6):715-723. 10.1016/j.yjmcc.2008.08.015, 2630487, 18926829.
33. Buxbaum JN, Reixach N. Transthyretin: the servant of many masters. Cell Mol Life Sci 2009, 66(19):3095-3101. 10.1007/s00018-009-0109-0, 19644733.
34. Fleming CE, Nunes AF, Sousa MM. Transthyretin: more than meets the eye. Prog Neurobiol 2009, 89(3):266-276. 10.1016/j.pneurobio.2009.07.007, 19665514.
35. Vongsa RA, Zimmerman NP, Dwinell MB. CCR6 regulation of the actin cytoskeleton orchestrates human beta defensin-2- and CCL20-mediated restitution of colonic epithelial cells. The Journal of biological chemistry 2009, 284(15):10034-10045. 10.1074/jbc.M805289200, 2665058, 19233848.
36. McGrory K, Flaitz CM, Klein JR. Chemokine changes during oral wound healing. Biochem Biophys Res Commun 2004, 324(1):317-320. 10.1016/j.bbrc.2004.09.056, 15465020.
37. Uehara N, Matsuoka Y, Tsubura A. Mesothelin promotes anchorage-independent growth and prevents anoikis via extracellular signal-regulated kinase signaling pathway in human breast cancer cells. Mol Cancer Res 2008, 6(2):186-193. 10.1158/1541-7786.MCR-07-0254, 18245228.
38. Bharadwaj U, Li M, Chen C, Yao Q. Mesothelin-induced pancreatic cancer cell proliferation involves alteration of cyclin E via activation of signal transducer and activator of transcription protein 3. Mol Cancer Res 2008, 6(11):1755-1765. 10.1158/1541-7786.MCR-08-0095, 2929833, 19010822.
39. Quaggin SE, Schwartz L, Cui S, Igarashi P, Deimling J, Post M, Rossant J. The basic-helix-loop-helix protein pod1 is critically important for kidney and lung organogenesis. Development (Cambridge, England) 1999, 126(24):5771-5783.
40. Smith LT, Lin M, Brena RM, Lang JC, Schuller DE, Otterson GA, Morrison CD, Smiraglia DJ, Plass C. Epigenetic regulation of the tumor suppressor gene TCF21 on 6q23-q24 in lung and head and neck cancer. Proceedings of the National Academy of Sciences of the United States of America 2006, 103(4):982-987. 10.1073/pnas.0510171102, 1348006, 16415157.
41. Plotkin M, Mudunuri V. Pod1 induces myofibroblast differentiation in mesenchymal progenitor cells from mouse kidney. Journal of cellular biochemistry 2008, 103(2):675-690. 10.1002/jcb.21441, 17551956.
42. Hamm A, Veeck J, Bektas N, Wild PJ, Hartmann A, Heindrichs U, Kristiansen G, Werbowetski-Ogilvie T, Del Maestro R, Knuechel R, et al. Frequent expression loss of Inter-alpha-trypsin inhibitor heavy chain (ITIH) genes in multiple human solid tumors: a systematic expression analysis. BMC cancer 2008, 8:25. 10.1186/1471-2407-8-25, 2268946, 18226209.
43. Veeck J, Chorovicer M, Naami A, Breuer E, Zafrakas M, Bektas N, Durst M, Kristiansen G, Wild PJ, Hartmann A, et al. The extracellular matrix protein ITIH5 is a novel prognostic marker in invasive node-negative breast cancer and its aberrant expression is caused by promoter hypermethylation. Oncogene 2008, 27(6):865-876. 10.1038/sj.onc.1210669, 17653090.
44. Bocock JP, Edgell CJ, Marr HS, Erickson AH. Human proteoglycan testican-1 inhibits the lysosomal cysteine protease cathepsin L. European journal of biochemistry/FEBS 2003, 270(19):4008-4015. 10.1046/j.1432-1033.2003.03789.x, 14511383.
45. Vered M, Dayan D, Yahalom R, Dobriyan A, Barshack I, Bello IO, Kantola S, Salo T. Cancer-associated fibroblasts and epithelial-mesenchymal transition in metastatic oral tongue squamous cell carcinoma. International journal of cancer
46. Chlenski A, Guerrero LJ, Yang Q, Tian Y, Peddinti R, Salwen HR, Cohn SL. SPARC enhances tumor stroma formation and prevents fibroblast activation. Oncogene 2007, 26(31):4513-4522. 10.1038/sj.onc.1210247, 17260013.
47. Herbert JM, Stekel D, Sanderson S, Heath VL, Bicknell R. A novel method of differential gene expression analysis using multiple cDNA libraries applied to the identification of tumour endothelial genes. BMC Genomics 2008, 9:153. 10.1186/1471-2164-9-153, 2346479, 18394197.
48. Bangsow T, Baumann E, Bangsow C, Jaeger MH, Pelzer B, Gruhn P, Wolf S, von Melchner H, Stanimirovic DB. The epithelial membrane protein 1 is a novel tight junction protein of the blood-brain barrier. J Cereb Blood Flow Metab 2008, 28(6):1249-1260. 10.1038/jcbfm.2008.19, 18382472.
49. Rothermund K, Rogulski K, Fernandes E, Whiting A, Sedivy J, Pu L, Prochownik EV. C-Myc-independent restoration of multiple phenotypes by two C-Myc target genes with overlapping functions. Cancer Res 2005, 65(6):2097-2107. 10.1158/0008-5472.CAN-04-2928, 15781619.
50. Rogulski KR, Cohen DE, Corcoran DL, Benos PV, Prochownik EV. Deregulation of common genes by c-Myc and its direct target, MT-MC1. Proceedings of the National Academy of Sciences of the United States of America 2005, 102(52):18968-18973. 10.1073/pnas.0507902102, 1323176, 16365299.
51. Qiu GB, Gong LG, Hao DM, Zhen ZH, Sun KL. Expression of MTLC gene in gastric carcinoma. World J Gastroenterol 2003, 9(10):2160-2163.
52. Okada M, Suzuki K, Takada K, Nakashima M, Nakanishi T, Shinohara T. Detection of up-regulated genes in thrombin-stimulated human umbilical vein endothelial cells. Thromb Res 2006, 118(6):715-721. 10.1016/j.thromres.2005.11.008, 16356540.
53. Oyama T, Miura S, Watanabe C, Hokari R, Fujiyama Y, Komoto S, Tsuzuki Y, Hosoe N, Nagata H, Hibi T. CXCL12 and CCL20 play a significant role in mucosal T-lymphocyte adherence to intestinal microvessels in mice. Microcirculation 2007, 14(7):753-766. 10.1080/10739680701409993, 17885999.
54. Sawa Y, Tsuruga E, Iwasawa K, Ishikawa H, Yoshida S. Leukocyte adhesion molecule and chemokine production through lipoteichoic acid recognition by toll-like receptor 2 in cultured human lymphatic endothelium. Cell Tissue Res 2008, 333(2):237-252. 10.1007/s00441-008-0625-5, 18523807.
55. Beider K, Abraham M, Begin M, Wald H, Weiss ID, Wald O, Pikarsky E, Abramovitch R, Zeira E, Galun E, et al. Interaction between CXCR4 and CCL20 pathways regulates tumor growth. PLoS One 2009, 4(4):e5125. 10.1371/journal.pone.0005125, 2659745, 19340288.
56. Theodosiou M, Laudet V, Schubert M. From carrot to clinic: an overview of the retinoic acid signaling pathway. Cell Mol Life Sci 67(9):1423-1445. 10.1007/s00018-010-0268-z, 20140749.
57. Vogel S, Piantedosi R, O'Byrne SM, Kako Y, Quadro L, Gottesman ME, Goldberg IJ, Blaner WS. Retinol-binding protein-deficient mice: biochemical basis for impaired vision. Biochemistry 2002, 41(51):15360-15368. 10.1021/bi0268551, 12484775.
58. Xu G, Redard M, Gabbiani G, Neuville P. Cellular retinol-binding protein-1 is transiently expressed in granulation tissue fibroblasts and differentially expressed in fibroblasts cultured from different organs. The American journal of pathology 1997, 151(6):1741-1749. 1858370, 9403724.
59. Clagett-Dame M, DeLuca HF. The role of vitamin A in mammalian reproduction and embryonic development. Annual review of nutrition 2002, 22:347-381. 10.1146/annurev.nutr.22.010402.102745E, 12055350.
60. Tan NS, Shaw NS, Vinckenbosch N, Liu P, Yasmin R, Desvergne B, Wahli W, Noy N. Selective cooperation between fatty acid binding proteins and peroxisome proliferator-activated receptors in regulating transcription. Molecular and cellular biology 2002, 22(14):5114-5127. 10.1128/MCB.22.14.5114-5127.2002, 139777, 12077340.
61. Kitano Y, Yoshimura K, Uchida G, Sato K, Harii K. Pretreatment with topical all-trans-retinoic acid is beneficial for wound healing in genetically diabetic mice. Archives of dermatological research 2001, 293(10):515-521. 10.1007/PL00007466, 11820728.
62. Matsuda M, Ubels JL, Edelhauser HF. Corneal endothelial healing rate and the effect of topical retinoic acid. Investigative ophthalmology & visual science 1986, 27(8):1193-1198.
63. Roy S, Khanna S, Rink C, Biswas S, Sen CK. Characterization of the acute temporal changes in excisional murine cutaneous wound inflammation by screening of the wound-edge transcriptome. Physiological genomics 2008, 34(2):162-184. 10.1152/physiolgenomics.00045.2008, 2494843, 18460641.
64. Roy S, Biswas S, Khanna S, Gordillo G, Bergdall V, Green J, Marsh CB, Gould LJ, Sen CK. Characterization of a preclinical model of chronic ischemic wound. Physiological genomics 2009, 37(3):211-224. 10.1152/physiolgenomics.90362.2008, 2685508, 19293328.
65. Roy S, Patel D, Khanna S, Gordillo GM, Biswas S, Friedman A, Sen CK. Transcriptome-wide analysis of blood vessels laser captured from human skin and chronic wound-edge tissue. Proceedings of the National Academy of Sciences of the United States of America 2007, 104(36):14472-14477. 10.1073/pnas.0706793104, 1964861, 17728400.
66. Pearl EJ, Barker D, Day RC, Beck CW. Identification of genes associated with regenerative success of Xenopus laevis hindlimbs. BMC developmental biology 2008, 8:66. 10.1186/1471-213X-8-66, 2483965, 18570684.
67. Nishidate M, Nakatani Y, Kudo A, Kawakami A. Identification of novel markers expressed during fin regeneration by microarray analysis in medaka fish. Dev Dyn 2007, 236(9):2685-2693. 10.1002/dvdy.21274, 17676638.
68. Janse EM, Jeurissen SH. Ontogeny and function of two non-lymphoid cell populations in the chicken embryo. Immunobiology 1991, 182(5):472-481.
69. Lelievre E, Hinek A, Lupu F, Buquet C, Soncin F, Mattot V. VE-statin/egfl7 regulates vascular elastogenesis by interacting with lysyl oxidases. The EMBO journal 2008, 27(12):1658-1670. 10.1038/emboj.2008.103, 2435125, 18497746.
70. Dumartin L, Quemener C, Laklai H, Herbert J, Bicknell R, Bousquet C, Pyronnet S, Castronovo V, Schilling MK, Bikfalvi A, et al. Netrin-1 mediates early events in pancreatic adenocarcinoma progression, acting on tumor and endothelial cells. Gastroenterology 138(4):1595-1606. 1606 e1591-1598, 10.1053/j.gastro.2009.12.061, 20080097.
71. Pan W. A comparative review of statistical methods for discovering differentially expressed genes in replicated microarray experiments. Bioinformatics 2002, 18(4):546-554. 10.1093/bioinformatics/18.4.546, 12016052.
72. Herbert JM, Buffa FM, Vorschmitt H, Egginton S, Bicknell R. A new procedure for determining the genetic basis of a physiological process in a non-model species, illustrated by cold induced angiogenesis in the carp. BMC Genomics 2009, 10:490. 10.1186/1471-2164-10-490, 2771047, 19852815.
73. Darnell DK, Kaur S, Stanislaw S, Davey S, Konieczka JH, Yatskievych TA, Antin PB. GEISHA: an in situ hybridization gene expression resource for the chicken embryo. Cytogenetic and genome research 2007, 117(1-4):30-35. 10.1159/000103162, 17675842.
74. Beckstead JH. A simple technique for preservation of fixation-sensitive antigens in paraffin-embedded tissues. J Histochem Cytochem 1994, 42(8):1127-1134.