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

PLoS Genetics

Volumn 5, Issue 11, 2009, Pages

  Lang, Michael R ^a,c   Patterson, Larissa B ^a   Gordon, Tiffany N ^a   Johnson, Stephen L ^b   Parichy, David M ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PIGMENT; BASONUCLIN 2 PROTEIN, ZEBRAFISH; BASONUCLIN-2 PROTEIN, ZEBRAFISH; CARRIER PROTEIN; ZEBRAFISH PROTEIN; ZINC FINGER PROTEIN;

ANIMAL TISSUE; ARTICLE; BASONUCLIN 2 GENE; BONAPARTE GENE; CHROMATOPHORE; FEMALE; FEMALE FERTILITY; GENE; GENE MUTATION; MELANOPHORE; NONHUMAN; PIGMENTATION; SUBCUTANEOUS TISSUE; ZEBRA FISH; ANIMAL; FERTILITY; GENETICS; MORPHOGENESIS; MUTATION; OVARY; PATHOLOGY; PHYSIOLOGY;

ANIMALIA; DANIO RERIO;

ANIMALS; BODY PATTERNING; CARRIER PROTEINS; FEMALE; FERTILITY; MELANOPHORES; MUTATION; OVARY; PIGMENTATION; ZEBRAFISH; ZEBRAFISH PROTEINS; ZINC FINGERS;

EID: 73649124931     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000744     Document Type: Article

References (80)

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.
2. Kondo S, Shirota H (2008) Theoretical analysis of mechanisms that generate the pigmentation pattern of animals. Semin Cell Dev Biol.
3. Mills MG, Patterson LB (2008) Not just black and white: Pigment pattern development and evolution in vertebrates. Semin Cell Dev Biol.
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.
5. Price AC, Weadick CJ, Shim J, Rodd FH (2008) Pigments, patterns, and fish behavior. Zebrafish 5: 297-307.
6. Booth CL (1990) Evolutionary significance of ontogenetic colour change in animals. Biol J Linn Soc 40: 125-163.
7. Le Douarin NM (1999) The Neural Crest. Cambridge: Cambride University Press.
8. 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.
9. Quigley AK, Turner JM, Nuckels RJ, Manuel JL, Budi EH, et al. (2004) Pigment pattern evolution by differential deployment of neural crest and post-embryonic melanophore lineages in Danio fishes. Development 131: 6053-6069.
10. Nishimura EK, Jordan SA, Oshima H, Yoshida H, Osawa M, et al. (2002) Dominant role of the niche in melanocyte stem-cell fate determination. Nature 416: 854-860.
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.
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.
13. Robinson KC, Fisher DE (2009) Specification and loss of melanocyte stem cells. Semin Cell Dev Biol 20: 111-116.
14. Bennett DC, Lamoreux ML (2003) The color loci of mice - a genetic century. Pigment Cell Res 16: 333-344.
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.
16. Zsebo KM, Williams DA, Geissler EN, Broudy VC, Martin FH, et al. (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. pp 213-224.
17. Besmer P, Manova K, Duttlinger R, Huang EJ, Packer A, et al. (1993) The kit-ligand (steel factor) and its receptor c-kit/W: pleiotropic roles in gametogenesis and melanogenesis. Dev Suppl. pp 125-137.
18. Parichy DM (2006) Evolution of danio pigment pattern development. Heredity 97: 200-210.
19. Herbomel P, Thisse B, Thisse C (2001) Zebrafish early macrophages colonize cephalic mesenchyme and developing brain, retina, and epidermis through a MCSF receptor-dependent invasive process. Dev Biol 238: 274-288.
20. Johnson SL, Africa D, Walker C, Weston JA (1995) Genetic control of adult pigment stripe development in zebrafish. Dev Biol 167: 27-33.
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.
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.
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.
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.
25. Kondo S, Shirota H (2009) Theoretical analysis of mechanisms that generate the pigmentation pattern of animals. Semin Cell Dev Biol 20: 82-89.
26. 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.
27. 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.
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.
29. 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.
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.
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.
32. Hodgkinson CA, Moore KJ, Nakayama A, Steingrimsson E, Copeland NG, et al. (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.
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.
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.
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.
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.
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.
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.
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.
40. Hawkes JW (1974) The structure of fish skin. I. General organization. Cell Tissue Res 149: 147-158.
41. Hawkes JW (1974) The structure of fish skin. II. The chromatophore unit. Cell Tissue Res 149: 159-172.
42. Parichy DM, Turner JM (2003) Temporal and cellular requirements for Fms signaling during zebrafish adult pigment pattern development. Development 130: 817-833.
43. Quigley IK, Manuel JL, Roberts RA, Nuckels RJ, Herrington ER, et al. (2005) Evolutionary diversification of pigment pattern in Danio fishes: differential fms dependence and stripe loss in D. albolineatus. Development 132: 89-104.
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.
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.
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.
47. Iuchi S, Easley K, Matsuzaki K, Weiner L, O'Connor N, et al. (2000) Alternative subcellular locations of keratinocyte basonuclin. Exp Dermatol 9: 178-184.
48. Parichy DM, Turner JM (2003) Cellular interactions during adult pigment stripe development in zebrafish; 2003. Academic Press Inc Elsevier Science. pp 486.
49. Vanhoutteghem A, Maciejewski-Duval A, Bouche C, Delhomme B, Herve F, et al. (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.
50. Mahoney MG, Tang W, Xiang MM, Moss SB, Gerton GL, et al. (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.
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.
52. Parichy DM, Tumer JM (2003) Zebrafish puma mutant decouples pigment pattern and somatic metamorphosis. Developmental Biology 256: 242-257.
53. Rawls JF, Mellgren EM, Johnson SL (2001) How the zebrafish gets its stripes. Dev Biol 240: 301-314.
54. Lopes SS, Yang XY, 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.
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.
56. Rawls JF, Johnson SL (2001) Requirements for the kit receptor tyrosine kinase during regeneration of zebrafish fin melanocytes. Development 128: 1943-1949.
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.
58. Ma J, Zeng F, Schultz RM, Tseng H (2006) Basonuclin: a novel mammalian maternal-effect gene. Development 133: 2053-2062.
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.
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.
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.
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.
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.
64. Wang J, Zhang S, Schultz RM, Tseng H (2006) Search for basonuclin target genes. Biochem Biophys Res Commun 348: 1261-1271.
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.
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.
67. Smyth IM, Wilming L, Lee AW, Taylor MS, Gautier P, et al. (2006) Genomic anatomy of the Tyrp1 (brown) deletion complex. Proc Natl Acad Sci U S A 103: 3704-3709.
68. Sugimoto M (2002) Morphological color changes in fish: regulation of pigment cell density and morphology. Microsc Res Tech 58: 496-503.
69. Gibson MC, Perrimon N (2005) Extrusion and death of DPP/BMP-compromised epithelial cells in the developing Drosophila wing. Science 307: 1785-1789.
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.
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.
72. Hultman KA, Budi EH, Teasley DC, Gottlieb AY, Parichy DM, et al. (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.
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.
74. Aoki H, Yamada Y, Hara A, Kunisada T (2009) Two distinct types of mouse melanocyte: differential signaling requirement for the maintenance of noncutaneous and dermal versus epidermal melanocytes. Development.
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.
76. Sato T, Han F, Yamamoto A (2008) The biology and management of uveal melanoma. Curr Oncol Rep 10: 431-438.
77. Wong CW, Fan YS, Chan TL, Chan AS, Ho LC, et al. (2005) BRAF and NRAS mutations are uncommon in melanomas arising in diverse internal organs. J Clin Pathol 58: 640-644.
78. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203: 253-310.
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.
80. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17: 754-755.