CoChat
Sign Up
Cited by 88melanin and skin pigmentationZebrafish Biomedical Research ApplicationsDevelopmental Biology and Gene Regulation

Melanophore migration and survival during zebrafish adult pigment stripe development require the immunoglobulin superfamily adhesion molecule Igsf11

Open access
Eom, Dae Seok, Inoue, Shinya, Patterson, Larissa B., Gordon, Tiffany N., Slingwine, Rebecca, Kondo, Shigeru, Watanabe, Masakatsu, Parichy, David M.·2012·PLoS Genetics
DOI 10.1371/journal.pgen.1002899PMC PMC3420941
Open this paper in CoChat — free accountOpen PDF

Abstract

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.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1371/journal.pgen.1002899

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • mitfa was expressed in melanophores and progenitors, but also in xanthophores, consistent with prior reports.

    “for example mitfa, encoding a transcription factor required for melanophore fate specification (Lister et al., 1999) was expressed in melanophores and progenitors, but also xanthophores (Figure 3C), consistent with prior reports (Eom et al., 2012; Parichy et al., 2000b).”

    From Thyroid hormone regulates distinct paths to maturation in pigment cell lineages (2019) · cites this paper as Eom et al., 2012

    In the Results section on igsf11 expression (Figure 5C,E), mitfa:GFP marks pigment-cell precursors, and the paper also uses a mitfa-driven transgene in melanophores (Figure 4). It does not establish mitfa expression in xanthophores: Figure 5F measures igsf11, not mitfa, in xanthophore-enriched cells. Page numbers were not provided in our copy. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 65

  1. [1]Kelsh RN (2004) Genetics and evolution of pigment patterns in fish. Pigment Cell Res 17: 326– 336. 15250934
  2. [2]Streelman JT, Peichel CL, Parichy DM (2007) Developmental genetics of adaptation in fishes: The case of novelty. Annual Review of Ecology Evolution and Systematics 38: 655– 681.
  3. [3]Parichy DM (2006) Evolution of danio pigment pattern development. Heredity 97: 200– 210. 16835593
  4. [4]Mills MG, Patterson LB (2008) Not just black and white: Pigment pattern development and evolution in vertebrates. Semin Cell Dev Biol 20: 72– 81. 19073271 PMC4241852
  5. [5]Houde AE (1997) Sex, Color, and Mate Choice in Guppies. Princeton, NJ: Princeton University Press.
  6. [6]Engeszer RE, Wang G, Ryan MJ, Parichy DM (2008) Sex-specific perceptual spaces for a vertebrate basal social aggregative behavior. Proc Natl Acad Sci U S A 105: 929– 933. 18199839 PMC2242707
  7. [7]Price AC, Weadick CJ, Shim J, Rodd FH (2008) Pigments, Patterns, and Fish Behavior. Zebrafish 5: 297– 307. 19133828
  8. [8]Seehausen O, Schluter D (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. PMC1691729 15306332
  9. [9]Johnson SL, Africa D, Walker C, Weston JA (1995) Genetic control of adult pigment stripe development in zebrafish. Dev Biol 167: 27– 33. 7851648
  10. [10]Parichy DM, Turner JM (2003) Zebrafish puma mutant decouples pigment pattern and somatic metamorphosis. Developmental Biology 256: 242– 257. 12679100
  11. [11]Parichy DM, Elizondo MR, Mills MG, Gordon TN, Engeszer RE (2009) Normal table of postembryonic zebrafish development: staging by externally visible anatomy of the living fish. Developmental Dynamics 238: 2975– 3015. 19891001 PMC3030279
  12. [12]Kirschbaum F (1975) Untersuchungen über das Farbmuster der Zebrabarbe Brachydanio rerio (Cyprinidae, Teleostei). Wilhelm Roux's Arch 177: 129– 152. 28304951
  13. [13]Hirata M, Nakamura K-i, Kanemaru T, Shibata Y, Kondo S (2003) Pigment cell organization in the hypodermis of zebrafish. Developmental Dynamics 227: 497– 503. 12889058
  14. [14]Parichy DM, Rawls JF, Pratt SJ, Whitfield TT, Johnson SL (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. 10393121
  15. [15]Lister JA, Robertson CP, Lepage T, Johnson SL, Raible DW (1999) nacre encodes a zebrafish microphthalmia-related protein that regulates neural-crest-derived pigment cell fate. Development 126: 3757– 3767. 10433906
  16. [16]Budi EH, Patterson LB, Parichy DM (2008) Embryonic requirements for ErbB signaling in neural crest development and adult pigment pattern formation. Development 135: 2603– 2614. 18508863 PMC2704560
  17. [17]Larson TA, Gordon TN, Lau HE, Parichy DM (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. 20692250 PMC2957186
  18. [18]Parichy DM, Ransom DG, Paw B, Zon LI, Johnson SL (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. 10862741
  19. [19]Parichy DM, Mellgren EM, Rawls JF, Lopes SS, Kelsh RN, 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. 11071756
  20. [20]Lopes SS, Yang X, Muller J, Carney TJ, McAdow AR, et al (2008) Leukocyte tyrosine kinase functions in pigment cell development. PLoS Genet 4: e1000026 doi:10.1371/journal.pgen.1000026. 18369445 PMC2265441 · DOI · Paper page
  21. [21]Parichy DM, Turner JM (2003) Temporal and cellular requirements for Fms signaling during zebrafish adult pigment pattern development. Development 130: 817– 833. 12538511
  22. [22]Maderspacher F (2003) Formation of the adult pigment pattern in zebrafish requires leopard and obelix dependent cell interactions. Development 130: 3447– 3457. 12810592
  23. [23]Yamaguchi M, Yoshimoto E, Kondo S (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. 17360399 PMC1820822
  24. [24]Takahashi G, Kondo S (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. 19067972
  25. [25]Nakamasu A, Takahashi G, Kanbe A, Kondo S (2009) Interactions between zebrafish pigment cells responsible for the generation of Turing patterns. Proc Natl Acad Sci U S A 106: 8429– 8434. 19433782 PMC2689028
  26. [26]Kondo S, Miura T (2010) Reaction-diffusion model as a framework for understanding biological pattern formation. Science 329: 1616– 1620. 20929839
  27. [27]Maderspacher F, Nusslein-Volhard C (2003) Formation of the adult pigment pattern in zebrafish requires leopard and obelix dependent cell interactions. Development 130: 3447– 3457. 12810592
  28. [28]Inaba M, Yamanaka H, Kondo S (2012) Pigment pattern formation by contact-dependent depolarization. Science 335: 677. 22323812
  29. [29]Haffter P, Odenthal J, Mullins M, Lin S, Farrell MJ, et al (1996) Mutations affecting pigmentation and shape of the adult zebrafish. Dev Genes Evol 206: 260– 276. 24173565
  30. [30]Iwashita M, Watanabe M, Ishii M, Chen T, Johnson SL, 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. 17121467 PMC1657052 · DOI · Paper page
  31. [31]Watanabe M, Iwashita M, Ishii M, Kurachi Y, Kawakami A, et al (2006) Spot pattern of leopard Danio is caused by mutation in the zebrafish connexin41.8 gene. EMBO Rep 7: 893– 897. 16845369 PMC1559663
  32. [32]Lang MR, Patterson LB, Gordon TN, Johnson SL, Parichy DM (2009) Basonuclin-2 requirements for zebrafish adult pigment pattern development and female fertility. PLoS Genet 5: e1000744 doi:10.1371/journal.pgen.1000744. 19956727 PMC2776513 · DOI · Paper page
  33. [33]Kawakami K, Amsterdam A, Shimoda N, Becker T, Mugg J, 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. 10801422
  34. [34]Budi EH, Patterson LB, Parichy DM (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. 21625562 PMC3098192 · DOI · Paper page
  35. [35]Curran K, Lister JA, Kunkel GR, Prendergast A, Parichy DM, et al (2010) Interplay between Foxd3 and Mitf regulates cell fate plasticity in the zebrafish neural crest. Dev Biol 344: 107– 118. 20460180 PMC2909359
  36. [37]Moreira J, Deutsch A (2005) Pigment pattern formation in zebrafish during late larval stages: a model based on local interactions. Dev Dyn 232: 33– 42. 15543601
  37. [38]Parichy DM (1996) Salamander pigment patterns: how can they be used to study developmental mechanisms and their evolutionary transformation? Int J Dev Biol 40: 871– 884. 8877461
  38. [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.
  39. [40]Macmillan GJ (1976) Melanoblast-tissue interactions and the development of pigment pattern in Xenopus larvae. J Embryol Exp Morphol 35: 463– 484. 947992
  40. [41]Epperlein HH, Lofberg J (1990) The development of the larval pigment patterns in Triturus alpestris and Ambystoma mexicanum. Adv Anat Embryol Cell Biol 118: 1– 99. 2368640
  41. [42]Crossin KL, Krushel LA (2000) Cellular signaling by neural cell adhesion molecules of the immunoglobulin superfamily. Dev Dyn 218: 260– 279. 10842356
  42. [43]Barclay AN (2003) Membrane proteins with immunoglobulin-like domains–a master superfamily of interaction molecules. Semin Immunol 15: 215– 223. 14690046
  43. [44]Rougon G, Hobert O (2003) New insights into the diversity and function of neuronal immunoglobulin superfamily molecules. Annu Rev Neurosci 26: 207– 238. 12598678
  44. [45]Katidou M, Vidaki M, Strigini M, Karagogeos D (2008) The immunoglobulin superfamily of neuronal cell adhesion molecules: lessons from animal models and correlation with human disease. Biotechnol J 3: 1564– 1580. 19072911
  45. [46]Long H, Ou Y, Rao Y, van Meyel DJ (2009) Dendrite branching and self-avoidance are controlled by Turtle, a conserved IgSF protein in Drosophila. Development 136: 3475– 3484. 19783736
  46. [47]Siebert M, Banovic D, Goellner B, Aberle H (2009) Drosophila motor axons recognize and follow a Sidestep-labeled substrate pathway to reach their target fields. Genes Dev 23: 1052– 1062. 19369411 PMC2682951
  47. [48]Dermody TS, Kirchner E, Guglielmi KM, Stehle T (2009) Immunoglobulin superfamily virus receptors and the evolution of adaptive immunity. PLoS Pathog 5: e1000481 doi:10.1371/journal.ppat.1000481. 19956667 PMC2777377 · DOI
  48. [49]Golias C, Batistatou A, Bablekos G, Charalabopoulos A, Peschos D, 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. 21892874
  49. [50]Montgomery BC, Cortes HD, Mewes-Ares J, Verheijen K, Stafford JL (2011) Teleost IgSF immunoregulatory receptors. Dev Comp Immunol 35: 1223– 1237. 21414352
  50. [51]Irintchev A, Schachner M (2011) The Injured and Regenerating Nervous System: Immunoglobulin Superfamily Members as Key Players. Neuroscientist 21903634
  51. [52]Moh MC, Shen S (2009) The roles of cell adhesion molecules in tumor suppression and cell migration: a new paradox. Cell Adh Migr 3: 334– 336. 19949308 PMC2802741
  52. [53]Wai Wong C, Dye DE, Coombe DR (2012) The role of immunoglobulin superfamily cell adhesion molecules in cancer metastasis. Int J Cell Biol 2012: 340296. 22272201 PMC3261479
  53. [54]Satyamoorthy K, Muyrers J, Meier F, Patel D, Herlyn M (2001) Mel-CAM-specific genetic suppressor elements inhibit melanoma growth and invasion through loss of gap junctional communication. Oncogene 20: 4676– 4684. 11498790
  54. [55]Haass NK, Smalley KS, Li L, Herlyn M (2005) Adhesion, migration and communication in melanocytes and melanoma. Pigment Cell Res 18: 150– 159. 15892711
  55. [56]Fukuzawa T, Obika M (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. 7792250
  56. [57]Suzu S, Hayashi Y, Harumi T, Nomaguchi K, Yamada M, et al (2002) Molecular cloning of a novel immunoglobulin superfamily gene preferentially expressed by brain and testis. Biochem Biophys Res Commun 296: 1215– 1221. 12207903
  57. [58]Katoh M (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. 12851705
  58. [59]Harada H, Suzu S, Hayashi Y, Okada S (2005) BT-IgSF, a novel immunoglobulin superfamily protein, functions as a cell adhesion molecule. J Cell Physiol 204: 919– 926. 15795899
  59. [60]Patzke C, Max KE, Behlke J, Schreiber J, Schmidt H, et al (2010) The coxsackievirus-adenovirus receptor reveals complex homophilic and heterophilic interactions on neural cells. J Neurosci 30: 2897– 2910. 20181587 PMC6633923
  60. [62]Verdino P, Witherden DA, Havran WL, Wilson IA (2010) The molecular interaction of CAR and JAML recruits the central cell signal transducer PI3K. Science 329: 1210– 1214. 20813955 PMC2951132
  61. [63]Urasaki A, Morvan G, Kawakami K (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. 16959904 PMC1602067
  62. [64]Kwan KM, Fujimoto E, Grabher C, Mangum BD, Hardy ME, et al (2007) The Tol2kit: A multisite gateway-based construction kit forTol2 transposon transgenesis constructs. Developmental Dynamics 236: 3088– 3099. 17937395
  63. [65]Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77: 51– 59. 2744487
  64. [66]Provost E, Rhee J, Leach SD (2007) Viral 2A peptides allow expression of multiple proteins from a single ORF in transgenic zebrafish embryos. Genesis 45: 625– 629. 17941043
  65. [67]Kelsh R (2000) Genetic Analysis of Melanophore Development in Zebrafish Embryos. Developmental Biology 225: 277– 293. 10985850

Cited by

Sorted by citations

Authors
Eom, D. S., Inoue, S., Patterson, L. B., Gordon, T. N., Slingwine, R., Kondo, S., Watanabe, M., & Parichy, D. M.
Affiliations
  • University of Washington (US)
  • The University of Osaka (JP)
Corresponding author
  • Watanabe, Masakatsu
  • Parichy, David M.
ORCID
Venue
PLoS Genetics
Publisher
Public Library of Science (PLoS)
Published
2012-08-16
Volume
8
Issue
8
Pages
e1002899
ISSN
  • 1553-7390 (ISSN-L)
  • 1553-7404
DOI
10.1371/journal.pgen.1002899
PMC
PMC3420941
OpenAlex
W2015151811
Cited by
88
References
1
Citations by year
2026: 4 · 2025: 4 · 2024: 5 · 2023: 8 · 2022: 6 · 2021: 8 · 2020: 8 · 2019: 4 · 2018: 4 · 2017: 14 · 2016: 6 · 2015: 7 · 2014: 5 · 2013: 4 · 2012: 1
FWCI
2.40
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS Genetics (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • eScholarship (California Digital Library) (submittedVersion)
  • eScholarship (California Digital Library) (submittedVersion, cc-by)
  • Figshare (submittedVersion, cc-by)
Funders
  • National Institutes of Health (NIH-R01)
  • Japan Society for the Promotion of Science (23770247, 22127003, 22370079)
  • National Institute of General Medical Sciences (R01GM096906, R01GM062182)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (T32HD007183)
  • Institute of Genetics
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › melanin and skin pigmentation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords
immunoglobulin superfamily adhesion molecules, zebrafish, cell adhesion, cell transplantation, genetic rescue
MeSH terms
Animals, Cell Differentiation, Cell Movement, Cell Survival, Embryo, Nonmammalian, Biological Evolution, Immunoglobulins, Larva, Melanophores, Mutation, Phenotype, Pigmentation, Zebrafish, Cell Adhesion Molecules, Gene Expression Regulation, Developmental, Body Patterning, Fish Proteins, Zebrafish Proteins

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review