Cited by 86melanin and skin pigmentationZebrafish Biomedical Research ApplicationsDevelopmental Biology and Gene Regulation

Basonuclin-2 requirements for zebrafish adult pigment pattern development and female fertility

Open access
Lang, Michael R., Patterson, Larissa B., Gordon, Tiffany N., Johnson, Stephen L., Parichy, David M.·2009·PLoS Genetics

Abstract

Relatively little is known about the generation of adult form. One complex adult trait that is particularly amenable to genetic and experimental analysis is the zebrafish pigment pattern, which undergoes extensive remodeling during post-embryonic development to form adult stripes. These stripes result from the arrangement of three classes of neural crest-derived pigment cells, or chromatophores: melanophores, xanthophores, and iridophores. Here, we analyze the zebrafish bonaparte mutant, which has a normal early pigment pattern but exhibits a severe disruption to the adult stripe pattern. We show that the bonaparte mutant phenotype arises from mutations in basonuclin-2 (bnc2), encoding a highly conserved, nuclear-localized zinc finger protein of unknown function. We show that bnc2 acts non-autonomously to the melanophore lineage and is expressed by hypodermal cells adjacent to chromatophores during adult pigment pattern formation. In bonaparte (bnc2) mutants, all three types of chromatophores differentiate but then are lost by extrusion through the skin. We further show that while bnc2 promotes the development of two genetically distinct populations of melanophores in the body stripes, chromatophores of the fins and scales remain unaffected in bonaparte mutants, though a requirement of fin chromatophores for bnc2 is revealed in the absence of kit and colony stimulating factor-1 receptor activity. Finally, we find that bonaparte (bnc2) mutants exhibit dysmorphic ovaries correlating with infertility and bnc2 is expressed in somatic ovarian cells, whereas the related gene, bnc1, is expressed within oocytes; and we find that both bnc2 and bnc1 are expressed abundantly within the central nervous system. These findings identify bnc2 as an important mediator of adult pigment pattern formation and identify bonaparte mutants as an animal model for dissecting bnc2 functions.

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.1000744

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?

  • Stromal cells of the hypodermis and iridophores regulate melanophore and xanthophore numbers during adult pigment pattern formation.

    “stromal cells of the hypodermis (Lang et al., 2009) and also iridophores (Frohnhöfer et al., 2013; Patterson and Parichy, 2013) regulate melanophore and xanthophore numbers during adult pigment pattern formation”

    From Thyroid hormone regulates distinct paths to maturation in pigment cell lineages (2019) · cites this paper as Lang et al., 2009

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: 78

  1. [1]Kelsh RN Harris ML Colanesi S Erickson CA 2008 Stripes and belly-spots-A review of pigment cell morphogenesis in vertebrates. Semin Cell Dev Biol PMC2744437 18977309
  2. [2]Kondo S Shirota H 2008 Theoretical analysis of mechanisms that generate the pigmentation pattern of animals. Semin Cell Dev Biol 18996494
  3. [3]Mills MG Patterson LB 2008 Not just black and white: Pigment pattern development and evolution in vertebrates. Semin Cell Dev Biol PMC4241852 19073271
  4. [4]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
  5. [5]Price AC Weadick CJ Shim J Rodd FH 2008 Pigments, patterns, and fish behavior. Zebrafish 5 297 307 19133828
  6. [7]Le Douarin NM 1999 The Neural Crest. Cambridge Cambride University Press
  7. [8]Parichy DM Reedy MV Erickson CA 2006 Chapter 5. Regulation of melanoblast migration and differentiation. Nordland JJ Boissy RE Hearing VJ King RA Oetting WS The Pigmentary System: Physiology and Pathophysiology 2nd Edition New York, New York Oxford University Press
  8. [9]Quigley AK Turner JM Nuckels RJ Manuel JL Budi EH 2004 Pigment pattern evolution by differential deployment of neural crest and post-embryonic melanophore lineages in Danio fishes. Development 131 6053 6069 15537688
  9. [10]Nishimura EK Jordan SA Oshima H Yoshida H Osawa M 2002 Dominant role of the niche in melanocyte stem-cell fate determination. Nature 416 854 860 11976685
  10. [11]Sieber-Blum M Grim M Hu YF Szeder V 2004 Pluripotent neural crest stem cells in the adult hair follicle. Dev Dyn 231 258 269 15366003
  11. [12]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
  12. [13]Robinson KC Fisher DE 2009 Specification and loss of melanocyte stem cells. Semin Cell Dev Biol 20 111 116 19124082
  13. [14]Bennett DC Lamoreux ML 2003 The color loci of mice–a genetic century. Pigment Cell Res 16 333 344 12859616
  14. [15]Geissler EN Ryan MA Housman DE 1988 The dominant-white spotting (W) locus of the mouse encodes the c-kit proto-oncogene. Cell 55 185 192 2458842
  15. [16]Zsebo KM Williams DA Geissler EN Broudy VC Martin FH 1990 Stem cell factor is encoded at the Sl locus of the mouse and is the ligand of the c-kit tyrosine kinase receptor. Cell 213 224 1698556
  16. [17]Besmer P Manova K Duttlinger R Huang EJ Packer A 1993 The kit-ligand (steel factor) and its receptor c-kit/W: pleiotropic roles in gametogenesis and melanogenesis. Dev Suppl 125 137 7519481
  17. [18]Parichy DM 2006 Evolution of danio pigment pattern development. Heredity 97 200 210 16835593
  18. [20]Johnson SL Africa D Walker C Weston JA 1995 Genetic control of adult pigment stripe development in zebrafish. Dev Biol 167 27 33 7851648
  19. [21]Hirata M Nakamura K Kanemaru T Shibata Y Kondo S 2003 Pigment cell organization in the hypodermis of zebrafish. Dev Dyn 227 497 503 12889058
  20. [22]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
  21. [23]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
  22. [24]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
  23. [25]Kondo S Shirota H 2009 Theoretical analysis of mechanisms that generate the pigmentation pattern of animals. Semin Cell Dev Biol 20 82 89 18996494
  24. [26]Iwashita M Watanabe M Ishii M Chen T Johnson SL 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
  25. [27]Watanabe M Iwashita M Ishii M Kurachi Y Kawakami A 2006 Spot pattern of leopard Danio is caused by mutation in the zebrafish connexin41.8 gene. EMBO Rep PMC1559663 16845369
  26. [28]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
  27. [29]Parichy DM Mellgren EM Rawls JF Lopes SS Kelsh RN 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
  28. [30]Shin MK Levorse JM Ingram RS Tilghman SM 1999 The temporal requirement for endothelin receptor-B signalling during neural crest development. Nature 402 496 501 10591209
  29. [31]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
  30. [32]Hodgkinson CA Moore KJ Nakayama A Steingrimsson E Copeland NG 1993 Mutations at the mouse microphthalmia locus are associated with defects in a gene encoding a novel basic-helix-loop-helix-zipper protein. Cell 74 395 404 8343963
  31. [33]Lister JA Close J Raible DW 2001 Duplicate mitf genes in zebrafish: complementary expression and conservation of melanogenic potential. Dev Biol 237 333 344 11543618
  32. [34]Hultman KA Bahary N Zon LI Johnson SL 2007 Gene Duplication of the zebrafish kit ligand and partitioning of melanocyte development functions to kit ligand a. PLoS Genet 3 e17 doi: 10.1371/journal.pgen.0030017 17257055 PMC1781495 · DOI
  33. [35]Braasch I Volff JN Schartl M 2008 The evolution of teleost pigmentation and the fish-specific genome duplication. Journal of Fish Biology 73 1891 1918
  34. [36]Honjo Y Kniss J Eisen JS 2008 Neuregulin-mediated ErbB3 signaling is required for formation of zebrafish dorsal root ganglion neurons. Development 135 2615 2625 18599505 PMC2756296
  35. [37]Vanhoutteghem A Djian P 2006 Basonuclins 1 and 2, whose genes share a common origin, are proteins with widely different properties and functions. Proc Natl Acad Sci U S A 103 12423 12428 16891417 PMC1567895
  36. [38]Vanhoutteghem A Djian P 2004 Basonuclin 2: an extremely conserved homolog of the zinc finger protein basonuclin. Proc Natl Acad Sci U S A 101 3468 3473 14988505 PMC373485
  37. [39]Hirata M Nakamura K Kondo S 2005 Pigment cell distributions in different tissues of the zebrafish, with special reference to the striped pigment pattern. Dev Dyn 234 293 300 16110504
  38. [40]Hawkes JW 1974 The structure of fish skin. I. General organization. Cell Tissue Res 149 147 158 4424315
  39. [41]Hawkes JW 1974 The structure of fish skin. II. The chromatophore unit. Cell Tissue Res 149 159 172 4424316
  40. [42]Parichy DM Turner JM 2003 Temporal and cellular requirements for Fms signaling during zebrafish adult pigment pattern development. Development 130 817 833 12538511
  41. [43]Quigley IK Manuel JL Roberts RA Nuckels RJ Herrington ER 2005 Evolutionary diversification of pigment pattern in Danio fishes: differential fms dependence and stripe loss in D. albolineatus. Development 132 89 104 15563521
  42. [44]Parichy DM Turner JM Parker NB 2003 Essential role for puma in development of postembryonic neural crest-derived cell lineages in zebrafish. Dev Biol 256 221 241 12679099
  43. [45]Romano RA Li H Tummala R Maul R Sinha S 2004 Identification of Basonuclin2, a DNA-binding zinc-finger protein expressed in germ tissues and skin keratinocytes. Genomics 83 821 833 15081112
  44. [46]Vanhoutteghem A Djian P 2007 The human basonuclin 2 gene has the potential to generate nearly 90,000 mRNA isoforms encoding over 2000 different proteins. Genomics 89 44 58 16942855
  45. [47]Iuchi S Easley K Matsuzaki K Weiner L O'Connor N 2000 Alternative subcellular locations of keratinocyte basonuclin. Exp Dermatol 9 178 184 10839715
  46. [48]Parichy DM Turner JM 2003 Cellular interactions during adult pigment stripe development in zebrafish; 2003. Academic Press Inc Elsevier Science 486
  47. [49]Vanhoutteghem A Maciejewski-Duval A Bouche C Delhomme B Herve F 2009 Basonuclin 2 has a function in the multiplication of embryonic craniofacial mesenchymal cells and is orthologous to disco proteins. Proc Natl Acad Sci U S A 106 14432 14437 19706529 PMC2732838
  48. [50]Mahoney MG Tang W Xiang MM Moss SB Gerton GL 1998 Translocation of the zinc finger protein basonuclin from the mouse germ cell nucleus to the midpiece of the spermatozoon during spermiogenesis. Biol Reprod 59 388 394 9687312
  49. [51]Yang Z Gallicano GI Yu QC Fuchs E 1997 An unexpected localization of basonuclin in the centrosome, mitochondria, and acrosome of developing spermatids. J Cell Biol 137 657 669 9151672 PMC2139879
  50. [52]Parichy DM Tumer JM 2003 Zebrafish puma mutant decouples pigment pattern and somatic metamorphosis. Developmental Biology 256 242 257 12679100
  51. [53]Rawls JF Mellgren EM Johnson SL 2001 How the zebrafish gets its stripes. Dev Biol 240 301 314 11784065
  52. [54]Lopes SS Yang XY Muller J Carney TJ McAdow AR 2008 Leukocyte tyrosine kinase functions in pigment cell development. Plos Genet 4 e1000026 doi: 10.1371/journal.pgen.1000026 18369445 PMC2265441 · DOI · Paper page
  53. [55]Mills MG Nuckels RJ Parichy DM 2007 Deconstructing evolution of adult phenotypes: genetic analyses of kit reveal homology and evolutionary novelty during adult pigment pattern development of Danio fishes. Development 134 1081 1090 17287252
  54. [56]Rawls JF Johnson SL 2001 Requirements for the kit receptor tyrosine kinase during regeneration of zebrafish fin melanocytes. Development 128 1943 1949 11493518
  55. [57]Tseng H Green H 1992 Basonuclin: a keratinocyte protein with multiple paired zinc fingers. Proc Natl Acad Sci U S A 89 10311 10315 1332044 PMC50328
  56. [58]Ma J Zeng F Schultz RM Tseng H 2006 Basonuclin: a novel mammalian maternal-effect gene. Development 133 2053 2062 16624857
  57. [59]Tseng H Matsuzaki K Lavker RM 1999 Basonuclin in murine corneal and lens epithelia correlates with cellular maturation and proliferative ability. Differentiation 65 221 227 10653358
  58. [60]Iuchi S Green H 1997 Nuclear localization of basonuclin in human keratinocytes and the role of phosphorylation. Proc Natl Acad Sci U S A 94 7948 7953 9223293 PMC21535
  59. [61]Zhang S Wang J Tseng H 2007 Basonuclin regulates a subset of ribosomal RNA genes in HaCaT cells. PLoS ONE 2 e902 doi: 10.1371/journal.pone.0000902 17878937 PMC1975673 · DOI
  60. [62]Zhang X Tseng H 2007 Basonuclin-null mutation impairs homeostasis and wound repair in mouse corneal epithelium. PLoS ONE 2 e1087 doi: 10.1371/journal.pone.0001087 17971852 PMC2034529 · DOI
  61. [63]Tian Q Kopf GS Brown RS Tseng H 2001 Function of basonuclin in increasing transcription of the ribosomal RNA genes during mouse oogenesis. Development 128 407 416 11152639
  62. [64]Wang J Zhang S Schultz RM Tseng H 2006 Search for basonuclin target genes. Biochem Biophys Res Commun 348 1261 1271 16919236 PMC1630671
  63. [65]Javerzat S Jackson IJ 1998 White-based brown (Tyrp1B-w) is a dominant mutation causing reduced hair pigmentation owing to a chromosomal inversion. Mamm Genome 9 469 471 9585436
  64. [66]Jackson IJ Chambers D Rinchik EM Bennett DC 1990 Characterization of TRP-1 mRNA levels in dominant and recessive mutations at the mouse brown (b) locus. Genetics 126 451 459 2245917 PMC1204199
  65. [67]Smyth IM Wilming L Lee AW Taylor MS Gautier P 2006 Genomic anatomy of the Tyrp1 (brown) deletion complex. Proc Natl Acad Sci U S A 103 3704 3709 16505357 PMC1450144
  66. [68]Sugimoto M 2002 Morphological color changes in fish: regulation of pigment cell density and morphology. Microsc Res Tech 58 496 503 12242707
  67. [69]Gibson MC Perrimon N 2005 Extrusion and death of DPP/BMP-compromised epithelial cells in the developing Drosophila wing. Science 307 1785 1789 15774762
  68. [70]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
  69. [71]Rawls JF Johnson SL 2003 Temporal and molecular separation of the kit receptor tyrosine kinase's roles in zebrafish melanocyte migration and survival. Dev Biol 262 152 161 14512025
  70. [72]Hultman KA Budi EH Teasley DC Gottlieb AY Parichy DM 2009 Defects in ErbB-dependent establishment of adult melanocyte stem cells reveal independent origins for embryonic and regeneration melanocytes. PLoS Genet 5 e1000544 doi: 10.1371/journal.pgen.1000544 19578401 PMC2699538 · DOI
  71. [73]Yang CT Hindes AE Hultman KA Johnson SL 2007 Mutations in gfpt1 and skiv2l2 cause distinct stage-specific defects in larval melanocyte regeneration in zebrafish. PLoS Genet 3 e88 doi: 10.1371/journal.pgen.0030088 17542649 PMC1885281 · DOI
  72. [74]Aoki H Yamada Y Hara A Kunisada T 2009 Two distinct types of mouse melanocyte: differential signaling requirement for the maintenance of non-cutaneous and dermal versus epidermal melanocytes. Development 19553284
  73. [75]Smalley KS Sondak VK Weber JS 2009 c-KIT signaling as the driving oncogenic event in sub-groups of melanomas. Histol Histopathol 24 643 650 19283671
  74. [76]Sato T Han F Yamamoto A 2008 The biology and management of uveal melanoma. Curr Oncol Rep 10 431 438 18706273
  75. [77]Wong CW Fan YS Chan TL Chan AS Ho LC 2005 BRAF and NRAS mutations are uncommon in melanomas arising in diverse internal organs. J Clin Pathol 58 640 644 15917418 PMC1770697
  76. [78]Kimmel CB Ballard WW Kimmel SR Ullmann B Schilling TF 1995 Stages of embryonic development of the zebrafish. Dev Dyn 203 253 310 8589427
  77. [79]Parichy DM Elizondo MR Mills MG Gordon TN Engeszer RE 2009 Normal table of post-embryonic zebrafish development: staging by externally visible anatomy of the living fish. Developmental Dynamics In press PMC3030279 19891001
  78. [80]Huelsenbeck JP Ronquist F 2001 MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17 754 755 11524383

Cited by

Sorted by citations

Authors
Lang, M. R., Patterson, L. B., Gordon, T. N., Johnson, S. L., & Parichy, D. M.
Affiliations
  • University of Washington (US)
  • Washington University in St. Louis (US)
Corresponding author
Parichy, David M.
Venue
PLoS Genetics
Published
2009-11-26
Volume
5
Issue
11
Pages
e1000744
ISSN
  • 1553-7390 (ISSN-L)
  • 1553-7404
OpenAlex
W2077684781
Cited by
86
References
1
Citations by year
2026: 4 · 2025: 1 · 2024: 4 · 2023: 7 · 2022: 1 · 2021: 7 · 2020: 3 · 2019: 9 · 2018: 3 · 2017: 5 · 2016: 6 · 2015: 4 · 2014: 10 · 2013: 7 · 2012: 8
FWCI
2.07
Type
journal article
Language
en
Open access
Locations
  • PLoS Genetics (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Institutes of Health
  • National Institute of General Medical Sciences (GM56988, R01GM062182, R01GM056988)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (T32HD007183)
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
zebrafish, chromatophores, melanophores, xanthophores, iridophores, zinc finger proteins, female fertility, KIT signaling, colony-stimulating factor 1 receptor, postembryonic development
MeSH terms
Animals, Carrier Proteins, Female, Fertility, Melanophores, Mutation, Ovary, Pigmentation, Zebrafish, Zinc Fingers, Body Patterning, 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