Emergence of differentially regulated pathways associated with the development of regional specificity in chicken skin
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- 作者：Kai-Wei Chang (1) (2)
Nancy A Huang (3)
I-Hsuan Liu (4) (5)
Yi-Hui Wang (4)
Ping Wu (6)
Yen-Tzu Tseng (7)
Michael W Hughes (6) (8)
Ting Xin Jiang (6)
Mong-Hsun Tsai (10) (11) (7)
Chien-Yu Chen (11) (9)
Yen-Jen Oyang (11) (3)
En-Chung Lin (4)
Cheng-Ming Chuong (5) (6)
Shau-Ping Lin (10) (11) (5) (7)
1. Genome and Systems Biology Degree Program ; National Taiwan University ; Taipei ; Taiwan
2. Genome and Systems Biology Degree Program ; Academia Sinica ; Taipei ; Taiwan
3. Department of Computer Science and Information Engineering ; National Taiwan University ; Taipei ; Taiwan
4. Department of Animal Science and Technology ; National Taiwan University ; Taipei ; Taiwan
5. Research Center for Developmental Biology and Regenerative Medicine ; National Taiwan University ; Taipei ; Taiwan
6. Department of Pathology ; School of Medicine ; University of Southern California ; Los Angeles ; CA ; USA
7. Institute of Biotechnology ; National Taiwan University ; Taipei ; Taiwan
8. International Research Center for Wound Repair and Regeneration ; National Cheng-Kung University ; Tainan ; Taiwan
10. Agricultural Biotechnology Research Centre ; Academia Sinica ; Taipei ; Taiwan
11. Center for Systems Biology ; National Taiwan University ; Taipei ; Taiwan
9. Department of Bio-Industrial Mechatronics Engineering ; National Taiwan University ; Taipei ; Taiwan - 关键词：Development ; Chicken ; Skin ; Cosine similarity ; Calcium ; Histone modifications
- 刊名：BMC Genomics
- 出版年：2015
- 出版时间：December 2015
- 年：2015
- 卷：16
- 期：1
- 全文大小：1,873 KB
- 参考文献：1. Prin F, Dhouailly D. How and when the regional competence of chick epidermis is established: feathers vs. scutate and reticulate scales, a problem en route to a solution. Int J Dev Biol. 2004;48(2鈥?):137鈥?8. CrossRef
2. Stettenheim PR. The integumentary morphology of modern birds鈥攁n overview. Am Zool. 2000;40(4):461鈥?7. 668/0003-1569(2000)040[0461:TIMOMB]2.0.CO;2" target="_blank" title="It opens in new window">CrossRef
3. Chang CH, Jiang TX, Lin CM, Burrus LW, Chuong CM, Widelitz R. Distinct Wnt members regulate the hierarchical morphogenesis of skin regions (spinal tract) and individual feathers. Mech Dev. 2004;121(2):157鈥?1. 6/j.mod.2003.12.004" target="_blank" title="It opens in new window">CrossRef
4. Yue Z, Jiang TX, Widelitz RB, Chuong CM. Mapping stem cell activities in the feather follicle. Nature. 2005;438(7070):1026鈥?. CrossRef
5. Yue Z, Jiang TX, Widelitz RB, Chuong CM. Wnt3a gradient converts radial to bilateral feather symmetry via topological arrangement of epithelia. Proc Natl Acad Sci U S A. 2006;103(4):951鈥?. 6894103" target="_blank" title="It opens in new window">CrossRef
6. Jiang T-X, Wideltz R, Shen W, Will P, Wu D, Lin C, et al. Integument pattern formation involves genetic and epigenetic controls operated at different levels: Feather arrays simulated by a digital hormone model. Int J Developmental Biol. 2004;48:117鈥?6. CrossRef
7. Mandler M, Neubuser A. FGF signaling is required for initiation of feather placode development. Development. 2004;131(14):3333鈥?3. CrossRef
8. Noramly S, Morgan BA. BMPs mediate lateral inhibition at successive stages in feather tract development. Development. 1998;125(19):3775鈥?7.
9. McKinnell IW, Turmaine M, Patel K. Sonic Hedgehog functions by localizing the region of proliferation in early developing feather buds. Dev Biol. 2004;272(1):76鈥?8. 6/j.ydbio.2004.04.019" target="_blank" title="It opens in new window">CrossRef
10. Noramly S, Freeman A, Morgan BA. beta-catenin signaling can initiate feather bud development. Development. 1999;126(16):3509鈥?1.
11. Chodankar R, Chang CH, Yue Z, Jiang TX, Suksaweang S, Burrus L, et al. Shift of localized growth zones contributes to skin appendage morphogenesis: role of the Wnt/beta-catenin pathway. J Invest Dermatol. 2003;120(1):20鈥?. 6/j.1523-1747.2003.12008.x" target="_blank" title="It opens in new window">CrossRef
12. Lin CM, Jiang TX, Widelitz RB, Chuong CM. Molecular signaling in feather morphogenesis. Curr Opin Cell Biol. 2006;18(6):730鈥?1. 6/j.ceb.2006.10.009" target="_blank" title="It opens in new window">CrossRef
13. Harris MP, Fallon JF, Prum RO. Shh-Bmp2 signaling module and the evolutionary origin and diversification of feathers. J Exp Zool. 2002;294(2):160鈥?6. CrossRef
14. Dhouailly D, Hardy MH, Sengel P. Formation of feathers on chick foot scales: a stage-dependent morphogenetic response to retinoic acid. J Embryol Exp Morphol. 1980;58:63鈥?8.
15. Crowe R, Niswander L. Disruption of scale development by Delta-1 misexpression. Dev Biol. 1998;195(1):70鈥?. 6/dbio.1997.8844" target="_blank" title="It opens in new window">CrossRef
16. Widelitz RB, Jiang TX, Lu J, Chuong CM. beta-catenin in epithelial morphogenesis: conversion of part of avian foot scales into feather buds with a mutated beta-catenin. Dev Biol. 2000;219(1):98鈥?14. 6/dbio.1999.9580" target="_blank" title="It opens in new window">CrossRef
17. Zou H, Niswander L. Requirement for BMP signaling in interdigital apoptosis and scale formation. Science. 1996;272(5262):738鈥?1. 6/science.272.5262.738" target="_blank" title="It opens in new window">CrossRef
18. Mou C, Pitel F, Gourichon D, Vignoles F, Tzika A, Tato P, et al. Cryptic patterning of avian skin confers a developmental facility for loss of neck feathering. PLoS Biol. 2011;9(3):e1001028. CrossRef
19. Rawles ME. Tissue interactions in scale and feather development as studied in dermal-epidermal recombinations. J Embryol Exp Morphol. 1963;11:765鈥?9.
20. Dhouailly D. Dermo-epidermal interactions between birds and mammals: differentiation of cutaneous appendages. J Embryol Exp Morphol. 1973;30(3):587鈥?03.
21. Hughes MW, Wu P, Jiang TX, Lin SJ, Dong CY, Li A, et al. In search of the golden fleece: unraveling principles of morphogenesis by studying the integrative biology of skin appendages. Integr Biol. 2011;3(4):388鈥?07. CrossRef
22. R Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2014.
23. Gautier L, Cope L, Bolstad BM, Irizarry RA. affy鈥揳nalysis of Affymetrix GeneChip data at the probe level. Bioinformatics. 2004;20(3):307鈥?5. CrossRef
24. Frohlich H, Speer N, Poustka A, Beissbarth T. GOSim鈥揳n R-package for computation of information theoretic GO similarities between terms and gene products. BMC Bioinformatics. 2007;8:166. 6/1471-2105-8-166" target="_blank" title="It opens in new window">CrossRef
25. Cheng J, Xie Q, Kumar V, Hurle M, Freudenberg JM, Yang L, Agarwal P. Evaluation of analytical methods for connectivity map data. Pacific Symposium on Biocomputing Pacific Symposium on Biocomputing 2013. 5-16.
26. Sethi P, Alagiriswamy S. Association rule based similarity measures for the clustering of gene expression data. Open Medical informatics J. 2010;4:63鈥?3.
27. Dzuida DM. Data mining for genomics and proteomics : analysis of gene and protein expression data. Hoboken, N.J.: Wiley; 2010. CrossRef
28. Revelle W. Psych: procedures for psychological, psychometric, and personality research. Evanston, Illinois: Northwestern University; 2014.
29. Hamburger V, Hamilton HL. A series of normal stages in the development of the chick embryo. Dev Dyn. 1951;195(4):231鈥?2. CrossRef
30. Jiang T-X, Stott S, Widelitz RB, Chuong C-M. Current methods in the study of avian skin appendages. In: Chuong C-M, editor. Molecular basis of epithelial appendage morphogenesis. Austin TX: Landes Bioscience; 1998. p. 395鈥?08.
31. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9(4):357鈥?. CrossRef
32. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 2008;9(9):R137. 6/gb-2008-9-9-r137" target="_blank" title="It opens in new window">CrossRef
33. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005;102(43):15545鈥?0. 6580102" target="_blank" title="It opens in new window">CrossRef
34. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet. 2003;34(3):267鈥?3. CrossRef
35. Ille F, Atanasoski S, Falk S, Ittner LM, Marki D, Buchmann-Moller S, et al. Wnt/BMP signal integration regulates the balance between proliferation and differentiation of neuroepithelial cells in the dorsal spinal cord. Dev Biol. 2007;304(1):394鈥?08. 6/j.ydbio.2006.12.045" target="_blank" title="It opens in new window">CrossRef
36. Katoh M. Networking of WNT, FGF, Notch, BMP, and Hedgehog signaling pathways during carcinogenesis. Stem Cell Rev. 2007;3(1):30鈥?. 6-6" target="_blank" title="It opens in new window">CrossRef
37. Parikh JR, Klinger B, Xia Y, Marto JA, Bluthgen N. Discovering causal signaling pathways through gene-expression patterns. Nucleic Acids Res. 2010;38(Web Server issue):W109鈥?7. CrossRef
38. Omori Y, Katoh K, Sato S, Muranishi Y, Chaya T, Onishi A, et al. Analysis of transcriptional regulatory pathways of photoreceptor genes by expression profiling of the Otx2-deficient retina. PLoS One. 2011;6(5):e19685. 685" target="_blank" title="It opens in new window">CrossRef
39. Glass K, Ott E, Losert W, Girvan M. Implications of functional similarity for gene regulatory interactions. J Royal Society, Interface/the Royal Society. 2012;9(72):1625鈥?6. CrossRef
40. Fisher R. Frequency distribution of the values of the correlation coefficient in samples from an indefinitely large population. Biometrika. 1915;10(4):507鈥?1.
41. Franceschini A, Szklarczyk D, Frankild S, Kuhn M, Simonovic M, Roth A, et al. STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res. 2013;41(Database issue):D808鈥?5. CrossRef
42. Rivals I, Personnaz L, Taing L, Potier MC. Enrichment or depletion of a GO category within a class of genes: which test? Bioinformatics. 2007;23(4):401鈥?. 633" target="_blank" title="It opens in new window">CrossRef
43. Jiang TX, Jung HS, Widelitz RB, Chuong CM. Self-organization of periodic patterns by dissociated feather mesenchymal cells and the regulation of size, number and spacing of primordia. Development. 1999;126(22):4997鈥?009.
44. Jiang TX, Widelitz RB, Shen WM, Will P, Wu DY, Lin CM, et al. Integument pattern formation involves genetic and epigenetic controls: feather arrays simulated by digital hormone models. Int J Dev Biol. 2004;48(2鈥?):117鈥?5. CrossRef
45. Dhouailly D. Dermo-epidermal interactions during morphogenesis of cutaneous appendages in amniotes. Frontiers of Matrix Biology. 1977;4:86鈥?21.
46. Hardy MH. The secret life of the hair follicle. Trends Genet. 1992;8(2):55鈥?1. 6/0168-9525(92)90350-D" target="_blank" title="It opens in new window">CrossRef
47. Chuong CM, Widelitz RB, Ting-Berreth S, Jiang TX. Early events during avian skin appendage regeneration: dependence on epithelial-mesenchymal interaction and order of molecular reappearance. J Invest Dermatol. 1996;107(4):639鈥?6. CrossRef
48. Park HY, Russakovsky V, Ohno S, Gilchrest BA. The beta isoform of protein kinase C stimulates human melanogenesis by activating tyrosinase in pigment cells. J Biol Chem. 1993;268(16):11742鈥?.
49. Mammucari C, Tommasi di Vignano A, Sharov AA, Neilson J, Havrda MC, Roop DR, et al. Integration of Notch 1 and calcineurin/NFAT signaling pathways in keratinocyte growth and differentiation control. Dev Cell. 2005;8(5):665鈥?6. 6/j.devcel.2005.02.016" target="_blank" title="It opens in new window">CrossRef
50. Kuhl M, Sheldahl LC, Malbon CC, Moon RT. Ca(2+)/calmodulin-dependent protein kinase II is stimulated by Wnt and Frizzled homologs and promotes ventral cell fates in Xenopus. J Biol Chem. 2000;275(17):12701鈥?1. CrossRef
51. Pillai S, Bikle DD, Mancianti ML, Cline P, Hincenbergs M. Calcium regulation of growth and differentiation of normal human keratinocytes: modulation of differentiation competence by stages of growth and extracellular calcium. J Cell Physiol. 1990;143(2):294鈥?02. CrossRef
52. Hernon CA, Harrison CA, Thornton DJ, MacNeil S. Enhancement of keratinocyte performance in the production of tissue-engineered skin using a low-calcium medium. Wound Repair Regen. 2007;15(5):718鈥?6. CrossRef
53. Tanaka S, Kato Y. Epigenesis in developing avian scales. I. Qualitative and quantitative characterization of finite cell populations. J Exp Zool. 1983;225(2):257鈥?9. CrossRef
54. Rada-Iglesias A, Bajpai R, Swigut T, Brugmann SA, Flynn RA, Wysocka J. A unique chromatin signature uncovers early developmental enhancers in humans. Nature. 2011;470(7333):279鈥?3. 692" target="_blank" title="It opens in new window">CrossRef
55. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, et al. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature. 2009;459(7243):108鈥?2. CrossRef
56. Hardingham GE, Chawla S, Cruzalegui FH, Bading H. Control of recruitment and transcription-activating function of CBP determines gene regulation by NMDA receptors and L-type calcium channels. Neuron. 1999;22(4):789鈥?8. 6/S0896-6273(00)80737-0" target="_blank" title="It opens in new window">CrossRef
57. Shibasaki M, Mizuno K, Kurokawa K, Ohkuma S. L-type voltage-dependent calcium channels facilitate acetylation of histone H3 through PKCgamma phosphorylation in mice with methamphetamine-induced place preference. J Neurochem. 2011;118(6):1056鈥?6. CrossRef
58. Bikle DD, Xie Z, Tu CL. Calcium regulation of keratinocyte differentiation. Expert Review of Endocrinology & Metabolism. 2012;7(4):461鈥?2. 6/eem.12.34" target="_blank" title="It opens in new window">CrossRef
59. Raya A, Kawakami Y, Rodriguez-Esteban C, Ibanes M, Rasskin-Gutman D, Rodriguez-Leon J, et al. Notch activity acts as a sensor for extracellular calcium during vertebrate left-right determination. Nature. 2004;427(6970):121鈥?. CrossRef
60. Schneider RA. How to tweak a beak: molecular techniques for studying the evolution of size and shape in Darwin鈥檚 finches and other birds. Bioessays. 2007;29(1):1鈥?. CrossRef
61. Kohn AD, Moon RT. Wnt and calcium signaling: beta-catenin-independent pathways. Cell Calcium. 2005;38(3鈥?):439鈥?6. 6/j.ceca.2005.06.022" target="_blank" title="It opens in new window">CrossRef
62. Flentke GR, Garic A, Amberger E, Hernandez M, Smith SM. Calcium-mediated repression of beta-catenin and its transcriptional signaling mediates neural crest cell death in an avian model of fetal alcohol syndrome. Birth Defects Res A Clin Mol Teratol. 2011;91(7):591鈥?02. CrossRef
63. Rey O, Chang W, Bikle D, Rozengurt N, Young SH, Rozengurt E. Negative cross-talk between calcium-sensing receptor and beta-catenin signaling systems in colonic epithelium. J Biol Chem. 2012;287(2):1158鈥?7. CrossRef - 刊物主题：Life Sciences, general; Microarrays; Proteomics; Animal Genetics and Genomics; Microbial Genetics and Genomics; Plant Genetics & Genomics;
- 出版者：BioMed Central
- ISSN：1471-2164
文摘
Background Regional specificity allows different skin regions to exhibit different characteristics, enabling complementary functions to make effective use of the integumentary surface. Chickens exhibit a high degree of regional specificity in the skin and can serve as a good model for when and how these regional differences begin to emerge. Results We used developing feather and scale regions in embryonic chickens as a model to gauge the differences in their molecular pathways. We employed cosine similarity analysis to identify the differentially regulated and co-regulated genes. We applied low cell techniques for expression validation and chromatin immunoprecipitation (ChIP)-based enhancer identification to overcome limited cell availabilities from embryonic chicken skin. We identified a specific set of genes demonstrating a high correlation as being differentially expressed during feather and scale development and maturation. Some members of the WNT, TGF-beta/BMP, and Notch family known to be involved in feathering skin differentiation were found to be differentially regulated. Interestingly, we also found genes along calcium channel pathways that are differentially regulated. From the analysis of differentially regulated pathways, we used calcium signaling pathways as an example for further verification. Some voltage-gated calcium channel subunits, particularly CACNA1D, are expressed spatio-temporally in the skin epithelium. These calcium signaling pathway members may be involved in developmental decisions, morphogenesis, or epithelial maturation. We further characterized enhancers associated with histone modifications, including H3K4me1, H3K27ac, and H3K27me3, near calcium channel-related genes and identified signature intensive hotspots that may be correlated with certain voltage-gated calcium channel genes. Conclusion We demonstrated the applicability of cosine similarity analysis for identifying novel regulatory pathways that are differentially regulated during development. Our study concerning the effects of signaling pathways and histone signatures on enhancers suggests that voltage-gated calcium signaling may be involved in early skin development. This work lays the foundation for studying the roles of these gene pathways and their genomic regulation during the establishment of skin regional specificity.