Melanophore Migration and Survival during Zebrafish Adult Pigment Stripe Development Require the Immunoglobulin Superfamily Adhesion Molecule Igsf11

English version České info

The zebrafish adult pigment pattern has emerged as a useful model for understanding the development and evolution of adult form as well as pattern-forming mechanisms more generally. In this species, a series of horizontal melanophore stripes arises during the larval-to-adult transformation, but the genetic and cellular bases for stripe formation remain largely unknown. Here, we show that the seurat mutant phenotype, consisting of an irregular spotted pattern, arises from lesions in the gene encoding Immunoglobulin superfamily member 11 (Igsf11). We find that Igsf11 is expressed by melanophores and their precursors, and we demonstrate by cell transplantation and genetic rescue that igsf11 functions autonomously to this lineage in promoting adult stripe development. Further analyses of cell behaviors in vitro, in vivo, and in explant cultures ex vivo demonstrate that Igsf11 mediates adhesive interactions and that mutants for igsf11 exhibit defects in both the migration and survival of melanophores and their precursors. These findings identify the first in vivo requirements for igsf11 as well as the first instance of an immunoglobulin superfamily member functioning in pigment cell development and patterning. Our results provide new insights into adult pigment pattern morphogenesis and how cellular interactions mediate pattern formation.

Vyšlo v časopise: Melanophore Migration and Survival during Zebrafish Adult Pigment Stripe Development Require the Immunoglobulin Superfamily Adhesion Molecule Igsf11. PLoS Genet 8(8): e32767. doi:10.1371/journal.pgen.1002899
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002899

Souhrn

Zdroje

1. KelshRN (2004) Genetics and evolution of pigment patterns in fish. Pigment Cell Res 17: 326–336.

2. StreelmanJT, PeichelCL, ParichyDM (2007) Developmental genetics of adaptation in fishes: The case of novelty. Annual Review of Ecology Evolution and Systematics 38: 655–681.

3. ParichyDM (2006) Evolution of danio pigment pattern development. Heredity 97: 200–210.

4. MillsMG, PattersonLB (2008) Not just black and white: Pigment pattern development and evolution in vertebrates. Semin Cell Dev Biol 20: 72–81.

5. Houde AE (1997) Sex, Color, and Mate Choice in Guppies. Princeton, NJ: Princeton University Press.

6. EngeszerRE, WangG, RyanMJ, ParichyDM (2008) Sex-specific perceptual spaces for a vertebrate basal social aggregative behavior. Proc Natl Acad Sci U S A 105: 929–933.

7. PriceAC, WeadickCJ, ShimJ, RoddFH (2008) Pigments, Patterns, and Fish Behavior. Zebrafish 5: 297–307.

8. SeehausenO, SchluterD (2004) Male-male competition and nuptial-colour displacement as a diversifying force in Lake Victoria cichlid fishes. Proceedings of the Royal Society of London Series B-Biological Sciences 271: 1345–1353.

9. JohnsonSL, AfricaD, WalkerC, WestonJA (1995) Genetic control of adult pigment stripe development in zebrafish. Dev Biol 167: 27–33.

10. ParichyDM, TurnerJM (2003) Zebrafish puma mutant decouples pigment pattern and somatic metamorphosis. Developmental Biology 256: 242–257.

11. ParichyDM, ElizondoMR, MillsMG, GordonTN, EngeszerRE (2009) Normal table of postembryonic zebrafish development: staging by externally visible anatomy of the living fish. Developmental Dynamics 238: 2975–3015.

12. KirschbaumF (1975) Untersuchungen über das Farbmuster der Zebrabarbe Brachydanio rerio (Cyprinidae, Teleostei). Wilhelm Roux's Arch 177: 129–152.

13. HirataM, NakamuraK-i, KanemaruT, ShibataY, KondoS (2003) Pigment cell organization in the hypodermis of zebrafish. Developmental Dynamics 227: 497–503.

14. ParichyDM, RawlsJF, PrattSJ, WhitfieldTT, JohnsonSL (1999) Zebrafish sparse corresponds to an orthologue of c-kit and is required for the morphogenesis of a subpopulation of melanocytes, but is not essential for hematopoiesis or primordial germ cell development. Development 126: 3425–3436.

15. ListerJA, RobertsonCP, LepageT, JohnsonSL, RaibleDW (1999) nacre encodes a zebrafish microphthalmia-related protein that regulates neural-crest-derived pigment cell fate. Development 126: 3757–3767.

16. BudiEH, PattersonLB, ParichyDM (2008) Embryonic requirements for ErbB signaling in neural crest development and adult pigment pattern formation. Development 135: 2603–2614.

17. LarsonTA, GordonTN, LauHE, ParichyDM (2010) Defective adult oligodendrocyte and Schwann cell development, pigment pattern, and craniofacial morphology in puma mutant zebrafish having an alpha tubulin mutation. Dev Biol 346: 296–309.

18. ParichyDM, RansomDG, PawB, ZonLI, JohnsonSL (2000) An orthologue of the kit-related gene fms is required for development of neural crest-derived xanthophores and a subpopulation of adult melanocytes in the zebrafish, Danio rerio. Development 127: 3031–3044.

19. ParichyDM, MellgrenEM, RawlsJF, LopesSS, KelshRN, et al. (2000) Mutational analysis of endothelin receptor b1 (rose) during neural crest and pigment pattern development in the zebrafish Danio rerio. Dev Biol 227: 294–306.

20. LopesSS, YangX, MullerJ, CarneyTJ, McAdowAR, et al. (2008) Leukocyte tyrosine kinase functions in pigment cell development. PLoS Genet 4: e1000026 doi:10.1371/journal.pgen.1000026.

21. ParichyDM, TurnerJM (2003) Temporal and cellular requirements for Fms signaling during zebrafish adult pigment pattern development. Development 130: 817–833.

22. MaderspacherF (2003) Formation of the adult pigment pattern in zebrafish requires leopard and obelix dependent cell interactions. Development 130: 3447–3457.

23. YamaguchiM, YoshimotoE, KondoS (2007) Pattern regulation in the stripe of zebrafish suggests an underlying dynamic and autonomous mechanism. Proc Natl Acad Sci U S A 104: 4790–4793.

24. TakahashiG, KondoS (2008) Melanophores in the stripes of adult zebrafish do not have the nature to gather, but disperse when they have the space to move. Pigment Cell Melanoma Res 21: 677–686.

25. NakamasuA, TakahashiG, KanbeA, KondoS (2009) Interactions between zebrafish pigment cells responsible for the generation of Turing patterns. Proc Natl Acad Sci U S A 106: 8429–8434.

26. KondoS, MiuraT (2010) Reaction-diffusion model as a framework for understanding biological pattern formation. Science 329: 1616–1620.

27. MaderspacherF, Nusslein-VolhardC (2003) Formation of the adult pigment pattern in zebrafish requires leopard and obelix dependent cell interactions. Development 130: 3447–3457.

28. InabaM, YamanakaH, KondoS (2012) Pigment pattern formation by contact-dependent depolarization. Science 335: 677.

29. HaffterP, OdenthalJ, MullinsM, LinS, FarrellMJ, et al. (1996) Mutations affecting pigmentation and shape of the adult zebrafish. Dev Genes Evol 206: 260–276.

30. IwashitaM, WatanabeM, IshiiM, ChenT, JohnsonSL, et al. (2006) Pigment pattern in jaguar/obelix zebrafish is caused by a Kir7.1 mutation: Implications for the regulation of melanosome movement. PLoS Genet 2: e197 doi:10.1371/journal.pgen.0020197.

31. WatanabeM, IwashitaM, IshiiM, KurachiY, KawakamiA, et al. (2006) Spot pattern of leopard Danio is caused by mutation in the zebrafish connexin41.8 gene. EMBO Rep 7: 893–897.

32. LangMR, PattersonLB, GordonTN, JohnsonSL, ParichyDM (2009) Basonuclin-2 requirements for zebrafish adult pigment pattern development and female fertility. PLoS Genet 5: e1000744 doi:10.1371/journal.pgen.1000744.

33. KawakamiK, AmsterdamA, ShimodaN, BeckerT, MuggJ, et al. (2000) Proviral insertions in the zebrafish hagoromo gene, encoding an F-box/WD40-repeat protein, cause stripe pattern anomalies. Curr Biol 10: 463–466.

34. BudiEH, PattersonLB, ParichyDM (2011) Post-embryonic nerve-associated precursors to adult pigment cells: genetic requirements and dynamics of morphogenesis and differentiation. PLoS Genet 7: e1002044 doi:10.1371/journal.pgen.1002044.

35. CurranK, ListerJA, KunkelGR, PrendergastA, ParichyDM, et al. (2010) Interplay between Foxd3 and Mitf regulates cell fate plasticity in the zebrafish neural crest. Dev Biol 344: 107–118.

36. ThisseB, ThisseC, WrightGJ (2008) Embryonic and Larval Expression Patterns from a Large Scale Screening for Novel Low Affinity Extracellular Protein Interactions. ZFIN Direct Data Submission (Available at: http://zfinorg, ZDB-PUB-080227-22, Accessed 2012 July 17).

37. MoreiraJ, DeutschA (2005) Pigment pattern formation in zebrafish during late larval stages: a model based on local interactions. Dev Dyn 232: 33–42.

38. ParichyDM (1996) Salamander pigment patterns: how can they be used to study developmental mechanisms and their evolutionary transformation? Int J Dev Biol 40: 871–884.

39. Parichy DM, Reedy MV, Erickson CA (2006) Chapter 5. Regulation of melanoblast migration and differentiation. In: Nordland JJ, Boissy RE, Hearing VJ, King RA, Oetting WS, et al.., editors. The Pigmentary System: Physiology and Pathophysiology 2nd Edition. New York, New York: Oxford University Press.

40. MacmillanGJ (1976) Melanoblast-tissue interactions and the development of pigment pattern in Xenopus larvae. J Embryol Exp Morphol 35: 463–484.

41. EpperleinHH, LofbergJ (1990) The development of the larval pigment patterns in Triturus alpestris and Ambystoma mexicanum. Adv Anat Embryol Cell Biol 118: 1–99.

42. CrossinKL, KrushelLA (2000) Cellular signaling by neural cell adhesion molecules of the immunoglobulin superfamily. Dev Dyn 218: 260–279.

43. BarclayAN (2003) Membrane proteins with immunoglobulin-like domains–a master superfamily of interaction molecules. Semin Immunol 15: 215–223.

44. RougonG, HobertO (2003) New insights into the diversity and function of neuronal immunoglobulin superfamily molecules. Annu Rev Neurosci 26: 207–238.

45. KatidouM, VidakiM, StriginiM, KaragogeosD (2008) The immunoglobulin superfamily of neuronal cell adhesion molecules: lessons from animal models and correlation with human disease. Biotechnol J 3: 1564–1580.

46. LongH, OuY, RaoY, van MeyelDJ (2009) Dendrite branching and self-avoidance are controlled by Turtle, a conserved IgSF protein in Drosophila. Development 136: 3475–3484.

47. SiebertM, BanovicD, GoellnerB, AberleH (2009) Drosophila motor axons recognize and follow a Sidestep-labeled substrate pathway to reach their target fields. Genes Dev 23: 1052–1062.

48. DermodyTS, KirchnerE, GuglielmiKM, StehleT (2009) Immunoglobulin superfamily virus receptors and the evolution of adaptive immunity. PLoS Pathog 5: e1000481 doi:10.1371/journal.ppat.1000481.

49. GoliasC, BatistatouA, BablekosG, CharalabopoulosA, PeschosD, et al. (2011) Physiology and pathophysiology of selectins, integrins, and IgSF cell adhesion molecules focusing on inflammation. A paradigm model on infectious endocarditis. Cell Commun Adhes 18: 19–32.

50. MontgomeryBC, CortesHD, Mewes-AresJ, VerheijenK, StaffordJL (2011) Teleost IgSF immunoregulatory receptors. Dev Comp Immunol 35: 1223–1237.

51. IrintchevA, SchachnerM (2011) The Injured and Regenerating Nervous System: Immunoglobulin Superfamily Members as Key Players. Neuroscientist

52. MohMC, ShenS (2009) The roles of cell adhesion molecules in tumor suppression and cell migration: a new paradox. Cell Adh Migr 3: 334–336.

53. Wai WongC, DyeDE, CoombeDR (2012) The role of immunoglobulin superfamily cell adhesion molecules in cancer metastasis. Int J Cell Biol 2012: 340296.

54. SatyamoorthyK, MuyrersJ, MeierF, PatelD, HerlynM (2001) Mel-CAM-specific genetic suppressor elements inhibit melanoma growth and invasion through loss of gap junctional communication. Oncogene 20: 4676–4684.

55. HaassNK, SmalleyKS, LiL, HerlynM (2005) Adhesion, migration and communication in melanocytes and melanoma. Pigment Cell Res 18: 150–159.

56. FukuzawaT, ObikaM (1995) N-CAM and N-cadherin are specifically expressed in xanthophores, but not in the other types of pigment cells, melanophores, and iridiphores. Pigment Cell Res 8: 1–9.

57. SuzuS, HayashiY, HarumiT, NomaguchiK, YamadaM, et al. (2002) Molecular cloning of a novel immunoglobulin superfamily gene preferentially expressed by brain and testis. Biochem Biophys Res Commun 296: 1215–1221.

58. KatohM (2003) IGSF11 gene, frequently up-regulated in intestinal-type gastric cancer, encodes adhesion molecule homologous to CXADR, FLJ22415 and ESAM. Int J Oncol 23: 525–531.

59. HaradaH, SuzuS, HayashiY, OkadaS (2005) BT-IgSF, a novel immunoglobulin superfamily protein, functions as a cell adhesion molecule. J Cell Physiol 204: 919–926.

60. PatzkeC, MaxKE, BehlkeJ, SchreiberJ, SchmidtH, et al. (2010) The coxsackievirus-adenovirus receptor reveals complex homophilic and heterophilic interactions on neural cells. J Neurosci 30: 2897–2910.

61. PetersenTN, BrunakS, von HeijneG, NielsenH (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785–786.

62. VerdinoP, WitherdenDA, HavranWL, WilsonIA (2010) The molecular interaction of CAR and JAML recruits the central cell signal transducer PI3K. Science 329: 1210–1214.

63. UrasakiA, MorvanG, KawakamiK (2006) Functional dissection of the Tol2 transposable element identified the minimal cis-sequence and a highly repetitive sequence in the subterminal region essential for transposition. Genetics 174: 639–649.

64. KwanKM, FujimotoE, GrabherC, MangumBD, HardyME, et al. (2007) The Tol2kit: A multisite gateway-based construction kit forTol2 transposon transgenesis constructs. Developmental Dynamics 236: 3088–3099.

65. HoSN, HuntHD, HortonRM, PullenJK, PeaseLR (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77: 51–59.

66. ProvostE, RheeJ, LeachSD (2007) Viral 2A peptides allow expression of multiple proteins from a single ORF in transgenic zebrafish embryos. Genesis 45: 625–629.

67. KelshR (2000) Genetic Analysis of Melanophore Development in Zebrafish Embryos. Developmental Biology 225: 277–293.

68. Sokal RR, Rohlf FJ (1981) Biometry. New York, New York: W. H. Freeman and Company.