Identification of novel genes involved in the development of the sword and gonopodium in swordtail fish

Developmental Dynamics

Volumn 238, Issue 7, 2009, Pages 1674-1687

  Offen, Nils ^a   Meyer, Axel ^a   Begemann, Gerrit ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

dusp1; Fin metamorphosis; Gonopodium; klf2; rack1; SSH; Sword; Sword development; Swordtail; tms ; Xiphophorus

Indexed keywords

ARTICLE; DUSP1 GENE; FISH; GENE; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; KLF2 GENE; METAMORPHOSIS; NONHUMAN; ORGANOGENESIS; PRIORITY JOURNAL; RACK1 GENE; REGENERATION; SEXUAL SELECTION; SUBTRACTIVE HYBRIDIZATION; TMSBETA LIKE GENE; XIPHOPHORUS;

ANIMALS; COMPARATIVE GENOMIC HYBRIDIZATION; CYPRINODONTIFORMES; EXTREMITIES; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE LIBRARY; GENES, DEVELOPMENTAL; MALE; MODELS, BIOLOGICAL; REGENERATION; TAIL; TESTOSTERONE;

XIPHOPHORUS;

EID: 67649579871     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.21983     Document Type: Article

References (62)

1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215:403-410. (Pubitemid 20364473)
2. Atkins GB, Jain MK. 2007. Role of Kruppel-like transcription factors in endothelial biology. Circ Res 100:1686-1695. (Pubitemid 46987860)
3. Basolo AL. 1990. Female preference predates the evolution of the sword in swordtail fish. Science 250:808-810. (Pubitemid 120034304)
4. Basolo AL. 1995. A further examination of a pre-existing bias favouring a sword in the genus Xiphophorus. Anim Behav 50: 365-375. (Pubitemid 26447842)
5. Basolo AL, Alcaraz G. 2003. The turn of the sword: length increases male swimming costs in swordtails. Proc Biol Sci 270: 1631-1636. (Pubitemid 36960295)
6. Basolo AL, Trainor BC. 2002. The conformation of a female preference for a composite male trait in green swordtails. Anim Behav 63:469-474. (Pubitemid 34938091)
7. Bayliss PE, Bellavance KL, Whitehead GG, Abrams JM, Aegerter S, Robbins HS, Cowan DB, Keating MT, O'Reilly T, Wood JM, Roberts TM, Chan J. 2006. Chemical modulation of receptor signaling inhibits regenerative angiogenesis in adult zebrafish. Nat Chem Biol 2:265-273.
8. Bechara IJ, Joazeiro PP, Mari-Beffa M, Becerra J, Montes GS. 2000. Collagen-affecting drugs impair regeneration of teleost tail fins. J Submicrosc Cytol Pathol 32:273-280.
9. Bhattacharya R, Senbanerjee S, Lin Z, Mir S, Hamik A, Wang P, Mukherjee P, Mukhopadhyay D, Jain MK. 2005. Inhibition of vascular permeability factor/vascular endothelial growth factor-mediated angiogenesis by the Kruppel-like factor KLF2. J Biol Chem 280:28848-28851. (Pubitemid 41161328)
10. Caunt CJ, Rivers CA, Conway-Campbell BL, Norman MR, McArdle CA. 2008. Epidermal growth factor receptor and protein kinase C signaling to ERK2: spatiotemporal regulation of ERK2 by dual specificity phosphatases. J Biol Chem 283:6241-6252.
11. Chakroborty D, Chowdhury UR, Sarkar C, Baral R, Dasgupta PS, Basu S. 2008. Dopamine regulates endothelial progenitor cell mobilization from mouse bone marrow in tumor vascularization. J Clin Invest 118:1380-1389.
12. Darwin C. 1871. The descent of man, and selection in relation to sex. London: J. Murray.
13. Diatchenko L, Lau YF, Campbell AP, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov ED, Siebert PD. 1996. Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 93:6025-6030. (Pubitemid 26190796)
14. Dzwillo M. 1962. Einfluss von Methyltestosteron auf die Aktivierung sekundärer Geschlechtsmerkmale über den arttypischen Zustand hinaus (Untersuchungen an xiphophorinen Zahnkarpfen). [Influence of methyltestosterone on the activation of secondary sexual characteristics beyond the species-specific character state (Examination of xiphophorine toothcarps).] Verh Deutsch Zool Gesellsch Wien 151-159.
15. Dzwillo M. 1964. Sekundäre Geschlechtsmerkmale einiger Xiphophorini unter dem Einfluss von Methyl-testosteron. [Secondary sexual characteristics of some Xiphophorini under the influence of methyltestosterone.] Kosswig-Festschrift15-22.
16. Eibner C, Pittlik S, Meyer A, Begemann G. 2008. The developmental basis of evolutionary innovation: Inductive signals coordinate the development of a sexually selected trait in swordtail fish. Evol Dev 10:403-412. (Pubitemid 351991475)
17. Fischer S, Draper BW, Neumann CJ. 2003. The zebrafish fgf24 mutant identifies an additional level of Fgf signaling involved in vertebrate forelimb initiation. Development 130:3515-3524.
18. Gordon M, Cohen H, Nigrelli RF. 1942. A hormone-produced taxonomic character in Platypoecilius maculatus diagnostic of wild P. xiphidium. Am Nat 77:569-572.
19. Grillon C, Rieger K, Bakala J, Schott D, Morgat JL, Hannappel E, Voelter W, Lenfant M. 1990. Involvement of thymosin beta 4 and endoproteinase Asp-N in the biosynthesis of the tetrapeptide Ac-SerAspLysPro a regulator of the hematopoietic system. FEBS Lett 274:30-34. (Pubitemid 20378114)
20. Grobstein C. 1942. Endocrine and developmental studies of gonopod differentiation in certain Poeciliid fishes. II. Effect of testosterone propionate on the normal and regenerating anal fin of adult Platypoecilus maculatus females. J Exp Zool 89:305-328.
21. Hornshøj H, Bendixen E, Conley LN, Andersen PK, Hedegaard J, Panitz F, Bendixen C. 2009. Transcriptomic and proteomic profiling of two porcine tissues using high-throughput technologies. BMC Genomics 10:30.
22. Huang WQ, Wang QR. 2001. Bone marrow endothelial cells secrete thymosin beta4 and AcSDKP. Exp Hematol 29:12-18. (Pubitemid 32054762)
23. Iovine MK. 2007. Conserved mechanisms regulate outgrowth in zebrafish fins. Nat Chem Biol 3:613-618. (Pubitemid 47417710)
24. Johnson JB, Basolo AL. 2003. Predator exposure alters female mate choice in the green swordtail. Behav Ecol 14:619-625. (Pubitemid 37274404)
25. Katogi R, Nakatani Y, Shin-i T, Kohara Y, Inohaya K, Kudo A. 2004. Large-scale analysis of the genes involved in fin regeneration and blastema formation in the medaka, Oryzias latipes. Mech Dev 121:861-872. (Pubitemid 38813142)
26. Kinney CM, Chandrasekharan UM, Mavrakis L, DiCorleto PE. 2008. VEGF and thrombin induce MKP-1 through distinct signaling pathways: role for MKP-1 in endothelial cell migration. Am J Physiol Cell Physiol 294:C241-250.
27. Kuraku S, Usuda R, Kuratani S. 2005. Comprehensive survey of carapacial ridge-specific genes in turtle implies cooption of some regulatory genes in carapace evolution. Evol Dev 7:3-17. (Pubitemid 40210828)
28. Laforest L, Brown CW, Poleo G, Geraudie J, Tada M, Ekker M, Akimenko MA. 1998. Involvement of the sonic hedgehog, patched 1 and bmp2 genes in patterning of the zebrafish dermal fin rays. Development 125:4175-4184.
29. Langer WF. 1913. Beiträge zur Morphologie der viviparen Cyprinodontiden. Gegenbauer's Morph Jahrb 47:193-307.
30. Lee JS, Yu Q, Shin JT, Sebzda E, Bertozzi C, Chen M, Mericko P, Stadtfeld M, Zhou D, Cheng L, Graf T, MacRae CA, Lepore JJ, Lo CW, Kahn ML. 2006. Klf2 is an essential regulator of vascular hemodynamic forces in vivo. Dev Cell 11:845-857. (Pubitemid 44804271)
31. Liang P, Averboukh L, Keyomarsi K, Sager R, Pardee AB. 1992. Differential display and cloning of messenger RNAs from human breast cancer versus mammary epithelial cells. Cancer Res 52:6966-6968. (Pubitemid 23006309)
32. Liu JM, Lawrence F, Kovacevic M, Bignon J, Papadimitriou E, Lallemand JY, Katsoris P, Potier P, Fromes Y, Wdzieczak-Bakala J. 2003. The tetrapeptide AcSDKP, an inhibitor of primitive hematopoietic cell proliferation, induces angiogenesis in vitro and in vivo. Blood 101:3014-3020. (Pubitemid 36857989)
33. Lu HC, Swindell EC, Sierralta WD, Eichele G, Thaller C. 2001. Evidence for a role of protein kinase C in FGF signal transduction in the developing chick limb bud. Development 128:2451-2460. (Pubitemid 32685087)
34. Malinda KM, Goldstein AL, Kleinman HK. 1997. Thymosin beta 4 stimulates directional migration of human umbilical vein endothelial cells. Faseb J 11:474-481. (Pubitemid 27259989)
35. Malinda KM, Sidhu GS, Mani H, Banaudha K, Maheshwari RK, Goldstein AL, Kleinman HK. 1999. Thymosin beta4 accelerates wound healing. J Invest Dermatol 113:364-368. (Pubitemid 29449075)
36. McCahill A, Warwicker J, Bolger GB, Houslay MD, Yarwood SJ. 2002. The RACK1 scaffold protein: a dynamic cog in cell response mechanisms. Mol Pharmacol 62:1261-1273. (Pubitemid 35403822)
37. Meyer A. 1997. The evolution of sexually selected traits in male swordtail fishes (Xiphophorus: Poeciliidae). Heredity 79: 329-337.
38. Meyer A, Morrissey JM, Schartl M. 1994. Recurrent origin of a sexually selected trait in Xiphophorus fishes inferred from a molecular phylogeny. Nature 368:539-542.
39. Meyer A, Salzburger W, Schartl M. 2006. Hybrid origin of a swordtail species (Teleostei: Xiphophorus clemenciae) driven by sexual selection. Mol Ecol 15:721-730.
40. Nechiporuk A, Poss KD, Johnson SL, Keating MT 2003. Positional cloning of a temperature-sensitive mutant emmental reveals a role for sly1 during cell proliferation in zebrafish fin regeneration. Dev Biol 258:291-306. (Pubitemid 36683132)
41. Nishidate M, Nakatani Y, Kudo A, Kawakami A. 2007. Identification of novel markers expressed during fin regeneration by microarray analysis in medaka fish. Dev Dyn 236:2685-2693. (Pubitemid 47450958)
42. Oates AC, Pratt SJ, Vail B, Yan Y, Ho RK, Johnson SL, Postlethwait JH, Zon LI. 2001. The zebrafish klf gene family. Blood 98:1792-1801.
43. Offen N, Blum N, Meyer A, Begemann G. 2008. Fgfr1 signalling in the development of a sexually selected trait in vertebrates, the sword of swordtail fish. BMC Dev Biol 8:98.
44. Ogino Y, Katoh H, Yamada G. 2004. Androgen dependent development of a modified anal fin, gonopodium, as a model to understand the mechanism of secondary sexual character expression in vertebrates. FEBS Lett 575:119-126. (Pubitemid 39237692)
45. Padhi BK, Joly L, Tellis P, Smith A, Nanjappa P, Chevrette M, Ekker M, Akimenko MA. 2004. Screen for genes differentially expressed during regeneration of the zebrafish caudal fin. Dev Dyn 231: 527-541. (Pubitemid 39410887)
46. Poss KD, Shen J, Nechiporuk A, McMahon G, Thisse B, Thisse C, Keating MT. 2000. Roles for Fgf signaling during zebrafish fin regeneration. Dev Biol 222:347-358. (Pubitemid 30416373)
47. Poss KD, Nechiporuk A, Hillam AM, Johnson SL, Keating MT. 2002. Mps1 defines a proximal blastemal proliferative compartment essential for zebrafish fin regeneration. Development 129, 5141-5149. (Pubitemid 35460678)
48. Quint E, Smith A, Avaron F, Laforest L, Miles J, Gaffield W, Akimenko MA. 2002. Bone patterning is altered in the regenerating zebrafish caudal fin after ectopic expression of sonic hedgehog and bmp2b or exposure to cyclopamine. Proc Natl Acad Sci USA 99:8713-8718.
49. Rosenthal GG, Evans CS. 1998. Female preference for swords in Xiphophorus helleri reflects a bias for large apparent size. Proc Natl Acad Sci USA 95:4431-4436.
50. Rosenthal GG, Garcià de Leon FJ. 2006. Sexual behavior, genes, and evolution in Xiphophorus. Zebrafish 3:85-90.
51. Rosenthal GG, Martinez TYF, Garcià de Leon FJ, Ryan MJ. 2001. Shared preferences by predators and females for male ornaments in swordtails. Am Nat 158: 146-154. (Pubitemid 32682541)
52. Roth LW, Bormann P, Bonnet A, Reinhard E. 1999. beta-thymosin is required for axonal tract formation in developing zebrafish brain. Development 126:1365-1374.
53. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
54. Schebesta M, Lien CL, Engel FB, Keating MT. 2006. Transcriptional profiling of caudal fin regeneration in zebrafish. Sci World J 6:38-54. (Pubitemid 46155752)
55. Smith A, Avaron F, Guay D, Padhi BK, Akimenko MA. 2006. Inhibition of BMP signaling during zebrafish fin regeneration disrupts fin growth and scleroblast differentiation and function. Dev Biol 299:438-454. (Pubitemid 44740418)
56. Smith A, Zhang J, Guay D, Quint E, Johnson A, Akimenko MA. 2008. Gene expression analysis on sections of zebrafish regenerating fins reveals limitations in the whole-mount in situ hybridization method. Dev Dyn 237:417-425. (Pubitemid 351312114)
57. Teng CH, Huang WN, Meng TC. 2007. Several dual specificity phosphatases coordinate to control the magnitude and duration of JNK activation in signaling response to oxidative stress. J Biol Chem 282:28395-28407. (Pubitemid 47606056)
58. Whitehead GG, Makino S, Lien CL, Keating MT. 2005. fgf20 is essential for initiating zebrafish fin regeneration. Science 310:1957-1960.
59. Yamada S, Wirtz D, Coulombe PA. 2002. Pairwise assembly determines the intrinsic potential for self-organization and mechanical properties of keratin filaments. Mol Biol Cell 13:382-391. (Pubitemid 34106082)
60. Zakrzewicz A, Hecker M, Marsh LM, Kwapiszewska G, Nejman B, Long L, Seeger W, Schermuly RT, Morrell NW, Morty RE, Eickelberg O. 2007. Receptor for activated C-kinase 1, a novel interaction partner of type II bone morphogenetic protein receptor, regulates smooth muscle cell proliferation in pulmonary arterial hypertension. Circulation 115:2957-2968. (Pubitemid 46912099)
61. Zander CD, Dzwillo M. 1969. Untersuchungen zur Entwicklung und Vererbung des Caudalfortsatzes der Xiphophorus-Arten (Pices). [Investigations regarding development and inheritance of the caudal process of Xiphophorus species (Pisces).] Z Wissenschaftliche Zool 178:276-315.
62. Zauner H, Begemann G, Mari-Beffa M, Meyer A. 2003. Differential regulation of msx genes in the development of the gonopodium, an intromittent organ, and of the "sword," a sexually selected trait of swordtail fishes (Xiphophorus). Evol Dev 5:466-477.