ETS family transcriptional regulators drive chromatin dynamics and malignancy in squamous cell carcinomas

eLife

Volumn 4, Issue NOVEMBER2015, 2015, Pages

  Yang, Hanseul ^a   Schramek, Daniel ^a,c,d   Adam, Rene C ^a   Keyes, Brice E ^a   Wang, Ping ^b   Zheng, Deyou ^b   Fuchs, Elaine ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c MOUNT SINAI HOSPITAL   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; KRUPPEL LIKE FACTOR 5; LENTIVIRUS VECTOR; PROTEIN C FOS; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR ETS; TRANSCRIPTION FACTOR JUNB; CHROMATIN;

ALLOGRAFT; ANIMAL CELL; ARTICLE; CANCER STEM CELL; CELL CULTURE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA FLANKING REGION; EPIGENETICS; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; GENE SILENCING; GENETIC TRANSDUCTION; IMAGING; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MALIGNANT NEOPLASTIC DISEASE; MOUSE; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; RNA SEQUENCE; SQUAMOUS CELL CARCINOMA; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TUMOR MICROENVIRONMENT; UPREGULATION; CELL PROLIFERATION; CHROMATIN; GENE REGULATORY NETWORK; GENETIC EPIGENESIS; HUMAN; METABOLISM; PATHOLOGY;

CARCINOMA, SQUAMOUS CELL; CELL PROLIFERATION; CHROMATIN; EPIGENESIS, GENETIC; GENE REGULATORY NETWORKS; HUMANS;

EID: 84955279894     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.10870     Document Type: Article

References (75)

1. Acharyya S, Oskarsson T, Vanharanta S, Malladi S, Kim J, Morris PG, Manova-Todorova K, Leversha M, Hogg N, Seshan VE, Norton L, Brogi E, MassaguéJ. 2012. A CXCL1 paracrine network links cancer chemoresistance and metastasis. Cell 150:165-178. doi: 10.1016/j.cell.2012.04.042
2. Adam RC, Yang H, Rockowitz S, Larsen SB, Nikolova M, Oristian DS, Polak L, Kadaja M, Asare A, Zheng D, Fuchs E. 2015. Pioneer factors govern super-enhancer dynamics in stem cell plasticity and lineage choice. Nature 521: 366-370. doi: 10.1038/nature14289
3. Adli M, Bernstein BE. 2011. Whole-genome chromatin profiling from limited numbers of cells using nano-ChIP- seq. Nature Protocols 6:1656-1668. doi: 10.1038/nprot.2011.402
4. Aguirre-Gamboa R, Gomez-Rueda H, Martínez-Ledesma E, Martínez-Torteya A, Chacolla-Huaringa R, Rodriguez- Barrientos A, Tamez-Peña JG, Treviño V, Cho WCS. 2013. SurvExpress: an online biomarker validation tool and database for cancer gene expression data using survival analysis. PLoS ONE 8:e74250. doi: 10.1371/journal. pone.0074250
5. Avraham R, Yarden Y. 2011. Feedback regulation of EGFR signalling: decision making by early and delayed loops. Nature Reviews Molecular Cell Biology 12:104-117. doi: 10.1038/nrm3048
6. Beronja S, Livshits G, Williams S, Fuchs E. 2010. Rapid functional dissection of genetic networks via tissue- specific transduction and RNAi in mouse embryos. Nature Medicine 16:821-827. doi: 10.1038/nm.2167
7. Bian Y, Terse A, Du J, Hall B, Molinolo A, Zhang P, Chen W, Flanders KC, Gutkind JS, Wakefield LM, Kulkarni AB. 2009. Progressive tumor formation in mice with conditional deletion of TGF- signaling in head and neck epithelia is associated with activation of the PI3K/Akt pathway. Cancer Research 69:5918-5926. doi: 10.1158/ 0008-5472.CAN-08-4623
8. Blanpain C, Fuchs E. 2014. Plasticity of epithelial stem cells in tissue regeneration. Science 344:1242281. doi: 10. 1126/science.1242281
9. Blanpain C, Lowry WE, Geoghegan A, Polak L, Fuchs E. 2004. Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell 118:635-648. doi: 10.1016/j.cell.2004.08.012
10. Boumahdi S, Driessens G, Lapouge G, Rorive S, Nassar D, Le Mercier M, Delatte B, Caauwe A, Lenglez S, Nkusi E, Brohée S, Salmon I, Dubois C, Marmol Veronique del, Fuks F, Beck B, Blanpain C. 2014. SOX2 controls tumour initiation and cancer stem-cell functions in squamous-cell carcinoma. Nature 511:246-250. doi: 10. 1038/nature13305
11. Briso EM, Guinea-Viniegra J, Bakiri L, Rogon Z, Petzelbauer P, Eils R, Wolf R, Rincon M, Angel P, Wagner EF.2013. Inflammation-mediated skin tumorigenesis induced by epidermal c-fos. Genes & Development 27:1959-1973. doi: 10.1101/gad.223339.113
12. Brunner D, Dücker K, Oellers N, Hafen E, Scholzi H, Klambt C. 1994. The ETS domain protein pointed-P2 is a target of MAP kinase in the sevenless signal transduction pathway. Nature 370:386-389. doi: 10.1038/ 370386a0
13. Buenrostro JD, Wu B, Chang HY, Greenleaf WJ. 2015. ATAC-seq: a method for assaying chromatin accessibility genome-wide. Current Protocols in Molecular Biology 109:21.29.1-21.2921. doi: 10.1002/0471142727. mb2129s109
14. Cataisson C, Ohman R, Patel G, Pearson A, Tsien M, Jay S, Wright L, Hennings H, Yuspa SH. 2009. Inducible cutaneous inflammation reveals a protumorigenic role for keratinocyte CXCR2 in skin carcinogenesis. Cancer Research 69:319-328. doi: 10.1158/0008-5472.CAN-08-2490
15. Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA, Jacobsen A, Byrne CJ, Heuer ML, Larsson E, Antipin Y, Reva B, Goldberg AP, Sander C, Schultz N. 2012. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discovery 2:401-404. doi: 10.1158/ 2159-8290.CD-12-0095
16. Chapuy B, McKeown MR, Lin CY, Monti S, Roemer MGM, Qi J, Rahl PB, Sun HH, Yeda KT, Doench JG, Reichert E, Kung AL, Rodig SJ, Young RA, Shipp MA, Bradner JE. 2013. Discovery and characterization of super- enhancer-associated dependencies in diffuse large b cell lymphoma. Cancer Cell 24:777-790. doi: 10.1016/j. ccr.2013.11.003
17. Chen C-C, Wang L, Plikus MV, Jiang TX, Murray PJ, Ramos R, Guerrero-Juarez CF, Hughes MW, Lee OK, Shi S, Widelitz RB, Lander AD, Chuong CM. 2015. Organ-level quorum sensing directs regeneration in hair stem cell populations. Cell 161:277-290. doi: 10.1016/j.cell.2015.02.016
18. Chen X, Mitsutake N, LaPerle K, Akeno N, Zanzonico P, Longo VA, Mitsutake S, Kimura ET, Geiger H, Santos E, Wendel HG, Franco A, Knauf JA, Fagin JA. 2009. Endogenous expression of HrasG12V induces developmental defects and neoplasms with copy number imbalances of the oncogene. Proceedings of the National Academy of Sciences of the United States of America 106:7979-7984. doi: 10.1073/pnas.0900343106
19. Chipumuro E, Marco E, Christensen CL, Kwiatkowski N, Zhang T, Hatheway CM, Abraham BJ, Sharma B, Yeung C, Altabef A, Perez-Atayde A, Wong K-K, Yuan G-C, Gray NS, Young RA, George RE. 2014. CDK7 inhibition suppresses super-enhancer-linked oncogenic transcription in MYCN-driven cancer. Cell 159:1126-1139. doi: 10.1016/j.cell.2014.10.024
20. Ding X, Pan H, Li J, Zhong Q, Chen X, Dry SM, Wang C-Y. 2013. Epigenetic activation of AP1 promotes squamous cell carcinoma metastasis. Science Signaling 6:ra28-15. doi: 10.1126/scisignal.2003884
21. Dowen JM, Fan ZP, Hnisz D, Ren G, Abraham BJ, Zhang LN, Weintraub AS, Schuijers J, Lee TI, Zhao K, Young RA. 2014. Control of cell identity genes occurs in insulated neighborhoods in mammalian chromosomes. Cell 159:374-387. doi: 10.1016/j.cell.2014.09.030
22. Eferl R, Wagner EF. 2003. AP-1: a double-edged sword in tumorigenesis. Nature Reviews Cancer 3:859-868. doi: 10.1038/nrc1209
23. Foos G, Garcia-Ramirez JJ, Galang CK, Hauser CA. 1998. Elevated expression of Ets2 or distinct portions of Ets2 can reverse ras-mediated cellular transformation. Journal of Biological Chemistry 273:18871-18880. doi: 10. 1074/jbc.273.30.18871
24. Foulds CE, Nelson ML, Blaszczak AG, Graves BJ. 2004. Ras/Mitogen-activated protein kinase signaling activates ets-1 and ets-2 by CBP/p300 recruitment. Molecular and Cellular Biology 24:10954-10964. doi: 10.1128/MCB. 24.24.10954-10964.2004
25. Fuchs E, Green H. 1980. Changes in keratin gene expression during terminal differentiation of the keratinocyte. Cell 19:1033-1042. doi: 10.1016/0092-8674(80)90094-X
26. Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO, Sun Y, Jacobsen A, Sinha R, Larsson E, Cerami E, Sander C, Schultz N. 2013. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Science Signaling 6:pl1. doi: 10.1126/scisignal.2004088
27. Gao Y-B, Chen Z-L, Li J-G, Hu X-D, Shi X-J, Sun Z-M, Zhang F, Zhao Z-R, Li Z-T, Liu Z-Y, Zhao Y-D, Sun J, Zhou C- C, Yao R, Wang S-Y, Wang P, Sun N, Zhang B-H, Dong J-S, Yu Y, Luo M, Feng X-L, Shi S-S, Zhou F, Tan F-W, Qiu B, Li N, Shao K, Zhang L-J, Zhang L-J, Xue Q, Gao S-G, He J. 2014. Genetic landscape of esophageal squamous cell carcinoma. Nature Genetics 46:1097-1102. doi: 10.1038/ng.3076
28. Gosselin D, Link VM, Romanoski CE, Fonseca GJ, Eichenfield DZ, Spann NJ, Stender JD, Chun HB, Garner H, Geissmann F, Glass CK. 2014. Environment drives selection and function of enhancers controlling tissue-specific macrophage identities. Cell 159:1327-1340. doi: 10.1016/j.cell.2014.11.023
29. Guasch G, Schober M, Pasolli HA, Conn EB, Polak L, Fuchs E. 2007. Loss of TGFb signaling destabilizes homeostasis and promotes squamous cell carcinomas in stratified epithelia. Cancer Cell 12:313-327. doi: 10. 1016/j.ccr.2007.08.020
30. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK. 2010. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and b cell identities. Molecular Cell 38:576-589. doi: 10.1016/j.molcel.2010.05.004
31. Hnisz D, Abraham BJ, Lee TI, Lau A, Saint-AndréV, Sigova AA, Hoke HA, Young RA. 2013. Super-enhancers in the control of cell identity and disease. Cell 155:934-947. doi: 10.1016/j.cell.2013.09.053
32. Hollenhorst PC, Ferris MW, Hull MA, Chae H, Kim S, Graves BJ. 2011. Oncogenic ETS proteins mimic activated RAS/MAPK signaling in prostate cells. Genes & Development 25:2147-2157. doi: 10.1101/gad.17546311
33. Jemal A, Siegel R, Xu J, Ward E. 2010. Cancer statistics, 2010. A Cancer Journal for Clinicians 60:277-300. doi: 10.3322/caac.20073
34. Kholodenko BN. 2006. Cell-signalling dynamics in time and space. Nature Reviews Molecular Cell Biology 7: 165-176. doi: 10.1038/nrm1838
35. Lane SW, Williams DA, Watt FM. 2014. Modulating the stem cell niche for tissue regeneration. Nature Biotechnology 32:795-803. doi: 10.1038/nbt.2978
36. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology 10:R25. doi: 10.1186/gb-2009-10-3-r25
37. Lapouge G, Beck B, Nassar D, Dubois C, Dekoninck S, Blanpain C. 2012. Skin squamous cell carcinoma propagating cells increase with tumour progression and invasiveness. The EMBO Journal 31:4563-4575. doi: 10.1038/emboj.2012.312
38. Lapouge G, Youssef KK, Vokaer B, Achouri Y, Michaux C, Sotiropoulou PA, Blanpain C. 2011. Identifying the cellular origin of squamous skin tumors. Proceedings of the National Academy of Sciences of the United States of America 108:7431-7436. doi: 10.1073/pnas.1012720108
39. Lavin Y, Winter D, Blecher-Gonen R, David E, Keren-Shaul H, Merad M, Jung S, Amit I. 2014. Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell 159:1312-1326. doi: 10. 1016/j.cell.2014.11.018
40. Leveen P. 2002. Induced disruption of the transforming growth factor beta type II receptor gene in mice causes a lethal inflammatory disorder that is transplantable. Blood 100:560-568. doi: 10.1182/blood.V100.2.560
41. Li X. 2003. Overexpression of ETS2 in human esophageal squamous cell carcinoma. World Journal of Gastroenterology 9:205-208. doi: 10.3748/wjg.v9.i2.205
42. Lien W-H, Guo X, Polak L, Lawton LN, Young RA, Zheng D, Fuchs E. 2011. Genome-wide maps of histone modifications unwind in vivo chromatin states of the hair follicle lineage. Cell Stem Cell 9:219-232. doi: 10. 1016/j.stem.2011.07.015
43. Liu K, Jiang M, Lu Y, Chen H, Sun J, Wu S, Ku W-Y, Nakagawa H, Kita Y, Natsugoe S, Peters JH, Rustgi Anil k., Onaitis MW, Kiernan A, Chen X, Que J. 2013. Sox2 cooperates with inflammation-mediated Stat3 activation in the malignant transformation of foregut basal progenitor cells. Cell Stem Cell 12:304-315. doi: 10.1016/j.stem. 2013.01.007
44. Lovén J, Hoke HA, Lin CY, Lau A, Orlando DA, Vakoc CR, Bradner JE, Lee TI, Young RA. 2013. Selective inhibition of tumor oncogenes by disruption of super-enhancers. Cell 153:320-334. doi: 10.1016/j.cell.2013.03. 036
45. Lu S-L. 2006. Loss of transforming growth factor-beta type II receptor promotes metastatic head-and-neck squamous cell carcinoma. Genes & Development 20:1331-1342. doi: 10.1101/gad.1413306
46. Manoranjan B, Wang X, Hallett RM, Venugopal C, Mack SC, McFarlane N, Nolte SM, Scheinemann K, Gunnarsson T, Hassell JA, Taylor MD, Lee C, Triscott J, Foster CM, Dunham C, Hawkins C, Dunn SE, Singh SK. 2013. FoxG1 interacts with Bmi1 to regulate self-renewal and tumorigenicity of medulloblastoma stem cells. Stem Cells 31:1266-1277. doi: 10.1002/stem.1401
47. Maston GA, Evans SK, Green MR. 2006. Transcriptional regulatory elements in the human genome. Annual Review of Genomics and Human Genetics 7:29-59. doi: 10.1146/annurev.genom.7.080505.115623
48. McLean CY, Bristor D, Hiller M, Clarke SL, Schaar BT, Lowe CB, Wenger AM, Bejerano G. 2010. GREAT improves functional interpretation of cis-regulatory regions. Nature Biotechnology 28:495-501. doi: 10.1038/nbt.1630
49. Morrison SJ, Scadden DT. 2014. The bone marrow niche for haematopoietic stem cells. Nature 505:327-334. doi: 10.1038/nature12984
50. Nassar D, Latil M, Boeckx B, Lambrechts D, Blanpain C. 2015. Genomic landscape of carcinogen-induced and genetically induced mouse skin squamous cell carcinoma. Nature Medicine 21:946-954. doi: 10.1038/nm.3878
51. Nguyen H, Rendl M, Fuchs E. 2006. Tcf3 governs stem cell features and represses cell fate determination in skin. Cell 127:171-183. doi: 10.1016/j.cell.2006.07.036
52. O'Neill EM, Rebay I, Tjian R, Rubin GM. 1994. The activities of two ets-related transcription factors required for drosophila eye development are modulated by the Ras/MAPK pathway. Cell 78:137-147. doi: 10.1016/0092- 8674(94)90580-0
53. Oshimori N, Oristian D, Fuchs E. 2015. TGF-b promotes heterogeneity and drug resistance in squamous cell carcinoma. Cell 160:963-976. doi: 10.1016/j.cell.2015.01.043
54. Parker SCJ, Stitzel ML, Taylor DL, Orozco JM, Erdos MR, Akiyama JA, van Bueren KL, Chines PS, Narisu N, Black BL, Visel A, Pennacchio LA, Collins FS, Becker J, Benjamin B, Blakesley R, Bouffard G, Brooks S, Coleman H, Dekhtyar M, Gregory M, Guan X, Gupta J, Han J, Hargrove A, Ho S.-l., Johnson T, Legaspi R, Lovett S, Maduro Q, Masiello C, Maskeri B, McDowell J, Montemayor C, Mullikin J, Park M, Riebow N, Schandler K, Schmidt B, Sison C, Stantripop M, Thomas J, Thomas P, Vemulapalli M, Young A.NISC Comparative Sequencing Program, National Institutes of Health Intramural Sequencing Center Comparative Sequencing Program Authors, NISC Comparative Sequencing Program Authors. 2013. Chromatin stretch enhancer states drive cell-specific gene regulation and harbor human disease risk variants. Proceedings of the National Academy of Sciences of the United States of America 110:17921-17926. doi: 10.1073/pnas.1317023110
55. Plaks V, Kong N, Werb Z. 2015. The cancer stem cell niche: how essential is the niche in regulating stemness of tumor cells? Cell Stem Cell 16:225-238. doi: 10.1016/j.stem.2015.02.015
56. Rebay I, Rubin GM. 1995. Yan functions as a general inhibitor of differentiation and is negatively regulated by activation of the Ras1/MAPK pathway. Cell 81:857-866. doi: 10.1016/0092-8674(95)90006-3
57. Rogers HW, Weinstock MA, Harris AR, Hinckley MR, Feldman SR, Fleischer AB, Coldiron BM. 2010. Incidence estimate of nonmelanoma skin cancer in the united states, 2006. Archives of Dermatology 146:283-287. doi: 10.1001/archdermatol.2010.19
58. Scadden DT. 2014. Nice neighborhood: emerging concepts of the stem cell niche. Cell 157:41-50. doi: 10.1016/ j.cell.2014.02.013
59. Scheitz CJF, Lee TS, McDermitt DJ, Tumbar T. 2012. Defining a tissue stem cell-driven Runx1/Stat3 signalling axis in epithelial cancer. The EMBO Journal 31:4124-4139. doi: 10.1038/emboj.2012.270
60. Schober M, Fuchs E. 2011. Tumor-initiating stem cells of squamous cell carcinomas and their control by TGF- and integrin/focal adhesion kinase (FAK) signaling. Proceedings of the National Academy of Sciences of the United States of America 108:10544-10549. doi: 10.1073/pnas.1107807108
61. Schofield R. 1978. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 4:7-25.
62. Sgarra R, Rustighi A, Tessari MA, Di Bernardo J, Altamura S, Fusco A, Manfioletti G, Giancotti V. 2004. Nuclear phosphoproteins HMGA and their relationship with chromatin structure and cancer. FEBS Letters 574:1-8. doi: 10.1016/j.febslet.2004.08.013
63. Siegle JM, Basin A, Sastre-Perona A, Yonekubo Y, Brown J, Sennett R, Rendl M, Tsirigos A, Carucci JA, Schober M. 2014. SOX2 is a cancer-specific regulator of tumour initiating potential in cutaneous squamous cell carcinoma. Nature Communications 5. doi: 10.1038/ncomms5511
64. Sur I. 2006. Epidermal and craniofacial defects in mice overexpressing Klf5 in the basal layer of the epidermis. Journal of Cell Science 119:3593-3601. doi: 10.1242/jcs.03070
65. Swamy M, Jamora C, Havran W, Hayday A. 2010. Epithelial decision makers: in search of the 'epimmunome'. Nature Immunology 11:656-665. doi: 10.1038/ni.1905
66. Trakatelli M, Ulrich C, del Marmol V, Euvrard S, Stockfleth E, Abeni D. 2007. Epidemiology of nonmelanoma skin cancer (nMSC) in europe: accurate and comparable data are needed for effective public health monitoring and interventions. British Journal of Dermatology 156:1-7. doi: 10.1111/j.1365-2133.2007.07861.x
67. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. 2012. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and cufflinks. Nature Protocols 7:562-578. doi: 10.1038/nprot.2012.016
68. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. 2010. Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology 28:511-515. doi: 10.1038/nbt.1621
69. Tumbar T. 2004. Defining the epithelial stem cell niche in skin. Science 303:359-363. doi: 10.1126/science. 1092436
70. White AC, Tran K, Khuu J, Dang C, Cui Y, Binder SW, Lowry WE. 2011. Defining the origins of Ras/p53-mediated squamous cell carcinoma. Proceedings of the National Academy of Sciences of the United States of America 108:7425-7430. doi: 10.1073/pnas.1012670108
71. Whyte WA, Orlando DA, Hnisz D, Abraham BJ, Lin CY, Kagey MH, Rahl PB, Lee TI, Young RA. 2013. Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 153:307-319. doi: 10.1016/j.cell.2013.03.035
72. Wilson WR, Hay MP. 2011. Targeting hypoxia in cancer therapy. Nature Reviews Cancer 11:393-410. doi: 10. 1038/nrc3064
73. Yamamoto H, Flannery ML, Kupriyanov S, Pearce J, McKercher SR, Henkel GW, Maki RA, Werb Z, Oshima RG. 1998. Defective trophoblast function in mice with a targeted mutation of Ets2. Genes & Development 12:1315-1326. doi: 10.1101/gad.12.9.1315
74. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nussbaum C, Myers RM, Brown M, Li W, Liu XS. 2008. Model-based analysis of ChIP-seq (MACS). Genome Biology 9:R137. doi: 10.1186/gb-2008-9-9-r137
75. Zlotnik A, Yoshie O, Nomiyama H. 2006. The chemokine and chemokine receptor superfamilies and their molecular evolution. Genome Biology 7:243. doi: 10.1186/gb-2006-7-12-243