Post-embryonic nerve-associated precursors to adult pigment cells: Genetic requirements and dynamics of morphogenesis and differentiation

PLoS Genetics

Volumn 7, Issue 5, 2011, Pages

  Budi, Erine H ^a   Patterson, Larissa B ^a   Parichy, David M ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 3; MOLECULAR MARKER;

ANIMAL TISSUE; ARTICLE; CELL LINEAGE; CELL MATURATION; CELL REGENERATION; CELL TRANSFORMATION; CONTROLLED STUDY; EMBRYO DEVELOPMENT; GENETIC REGULATION; LEUKOCYTE DIFFERENTIAL COUNT; MELANOPHORE; MORPHOGENESIS; MUTATIONAL ANALYSIS; NONHUMAN; PIGMENT CELL; REGENERATIVE ABILITY; STEM CELL NICHE; TRANSGENICS; AGING; ANIMAL; CELL DIFFERENTIATION; CELL SHAPE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LARVA; METABOLISM; NERVE CELL; PIGMENTATION; ZEBRA FISH;

DANIO RERIO; VERTEBRATA;

AGING; ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELL SHAPE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LARVA; MELANOPHORES; NEURONS; PIGMENTATION; RECEPTOR, ERBB-3; ZEBRAFISH;

EID: 79957975047     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002044     Document Type: Article

References (98)

1. Bedelbaeva K, Snyder A, Gourevitch D, Clark L, Zhang XM, et al. (2010) Lack of p21 expression links cell cycle control and appendage regeneration in mice. Proc Natl Acad Sci U S A 107: 5845-5850.
2. Salewski RP, Eftekharpour E, Fehlings MG, (2010) Are induced pluripotent stem cells the future of cell-based regenerative therapies for spinal cord injury? J Cell Physiol 222: 515-521.
3. Guo JK, Cantley LG, (2010) Cellular maintenance and repair of the kidney. Annu Rev Physiol 72: 357-376.
4. Voog J, Jones DL, (2010) Stem cells and the niche: a dynamic duo. Cell Stem Cell 6: 103-115.
5. Inomata K, Aoto T, Binh NT, Okamoto N, Tanimura S, et al. (2009) Genotoxic stress abrogates renewal of melanocyte stem cells by triggering their differentiation. Cell 137: 1088-1099.
6. Mayack SR, Shadrach JL, Kim FS, Wagers AJ, (2010) Systemic signals regulate ageing and rejuvenation of blood stem cell niches. Nature 463: 495-500.
7. Nishimura EK, Granter SR, Fisher DE, (2005) Mechanisms of hair graying: incomplete melanocyte stem cell maintenance in the niche. Science 307: 720-724.
8. Alison MR, Islam S, Wright NA, (2010) Stem cells in cancer: instigators and propagators? J Cell Sci 123: 2357-2368.
9. Youssef KK, Van Keymeulen A, Lapouge G, Beck B, Michaux C, et al. (2010) Identification of the cell lineage at the origin of basal cell carcinoma. Nat Cell Biol 12: 299-305.
10. Le LQ, Shipman T, Burns DK, Parada LF, (2009) Cell of origin and microenvironment contribution for NF1-associated dermal neurofibromas. Cell Stem Cell 4: 453-463.
11. Le Douarin NM, (1999) The Neural Crest. Cambridge Cambride University Press.
12. Kelsh RN, Harris ML, Colanesi S, Erickson CA, (2009) Stripes and belly-spots-A review of pigment cell morphogenesis in vertebrates. Semin Cell Dev Biol 20: 90-104.
13. Thomas AJ, Erickson CA, (2008) The making of a melanocyte: the specification of melanoblasts from the neural crest. Pigment Cell Melanoma Res 21: 598-610.
14. Cooper CD, Raible DW, (2008) Mechanisms for reaching the differentiated state: Insights from neural crest-derived melanocytes. Semin Cell Dev Biol.
15. 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.
16. Wong CE, Paratore C, Dours-Zimmermann MT, Rochat A, Pietri T, et al. (2006) Neural crest-derived cells with stem cell features can be traced back to multiple lineages in the adult skin. J Cell Biol 175: 1005-1015.
17. Robinson KC, Fisher DE, (2009) Specification and loss of melanocyte stem cells. Semin Cell Dev Biol 20: 111-116.
18. White RM, Zon LI, (2008) Melanocytes in development, regeneration, and cancer. Cell Stem Cell 3: 242-252.
19. Nordlund JJ, Boissy RE, Hearing VJ, King RA, Oetting WS, et al.eds. (2006) The Pigmentary System: Physiology and Pathophysiology. 2nd Edition ed:Blackwell Publishing, Inc.
20. Rigel DS, (1997) Malignant melanoma: incidence issues and their effect on diagnosis and treatment in the 1990s. Mayo Clin Proc 72: 367-371.
21. Jemal A, Siegel R, Ward E, Hao Y, Xu J, et al. (2009) Cancer statistics, 2009. CA Cancer J Clin 59: 225-249.
22. Balch CM, Gershenwald JE, Soong SJ, Thompson JF, Ding S, et al. (2010) Multivariate analysis of prognostic factors among 2,313 patients with stage III melanoma: comparison of nodal micrometastases versus macrometastases. J Clin Oncol 28: 2452-2459.
23. Balch CM, Gershenwald JE, Soong SJ, Thompson JF, Atkins MB, et al. (2009) Final version of 2009 AJCC melanoma staging and classification. J Clin Oncol 27: 6199-6206.
24. Balch CM, Soong SJ, Gershenwald JE, Thompson JF, Reintgen DS, et al. (2001) Prognostic factors analysis of 17,600 melanoma patients: validation of the American Joint Committee on Cancer melanoma staging system. J Clin Oncol 19: 3622-3634.
25. Uong A, Zon LI, (2010) Melanocytes in development and cancer. J Cell Physiol 222: 38-41.
26. Mouawad R, Sebert M, Michels J, Bloch J, Spano JP, et al. (2010) Treatment for metastatic malignant melanoma: old drugs and new strategies. Crit Rev Oncol Hematol 74: 27-39.
27. Bhatia S, Tykodi SS, Thompson JA, (2009) Treatment of metastatic melanoma: an overview. Oncology (Williston Park) 23: 488-496.
28. Jilaveanu LB, Aziz SA, Kluger HM, (2009) Chemotherapy and biologic therapies for melanoma: do they work? Clin Dermatol 27: 614-625.
29. Barth A, Wanek LA, Morton DL, (1995) Prognostic factors in 1,521 melanoma patients with distant metastases. J Am Coll Surg 181: 193-201.
30. Gupta PB, Kuperwasser C, Brunet JP, Ramaswamy S, Kuo WL, et al. (2005) The melanocyte differentiation program predisposes to metastasis after neoplastic transformation. Nat Genet 37: 1047-1054.
31. Devoto SH, Stoiber W, Hammond CL, Steinbacher P, Haslett JR, et al. (2006) Generality of vertebrate developmental patterns: evidence for a dermomyotome in fish. Evol Dev 8: 101-110.
32. Hawkes JW, (1974) The structure of fish skin. I. General organization. Cell Tissue Res 149: 147-158.
33. 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.
34. Ceol CJ, Houvras Y, White RM, Zon LI, (2008) Melanoma Biology and the Promise of Zebrafish. Zebrafish 5: 247-255.
35. Patton EE, Widlund HR, Kutok JL, Kopani KR, Amatruda JF, et al. (2005) BRAF mutations are sufficient to promote nevi formation and cooperate with p53 in the genesis of melanoma. Curr Biol 15: 249-254.
36. Parichy DM, Turner JM, (2003) Zebrafish puma mutant decouples pigment pattern and somatic metamorphosis. Developmental Biology 256: 242-257.
37. Johnson SL, Africa D, Walker C, Weston JA, (1995) Genetic control of adult pigment stripe development in zebrafish. Dev Biol 167: 27-33.
38. 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.
39. Hirata M, Nakamura K, Kanemaru T, Shibata Y, Kondo S, (2003) Pigment cell organization in the hypodermis of zebrafish. Dev Dyn 227: 497-503.
40. Hawkes JW, (1974) The structure of fish skin. II. The chromatophore unit. Cell Tissue Res 149: 159-172.
41. Parichy DM, Turner JM. Cellular interactions during adult pigment stripe development in zebrafish; (2003) Academic Press Inc Elsevier Science.
42. 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.
43. 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.
44. 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.
45. 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.
46. Kelsh RN, Dutton K, Medlin J, Eisen JS, (2000) Expression of zebrafish fkd6 in neural crest-derived glia. Mech Dev pp. 161-164.
47. Lister JA, Cooper C, Nguyen K, Modrell M, Grant K, et al. (2006) Zebrafish Foxd3 is required for development of a subset of neural crest derivatives. Developmental Biology 290: 92-104.
48. Stewart RA, Arduini BL, Berghmans S, George RE, Kanki JP, et al. (2006) Zebrafish foxd3 is selectively required for neural crest specification, migration and survival. Developmental Biology 292: 174-188.
49. Dutton KA, Pauliny A, Lopes SS, Elworthy S, Carney TJ, et al. (2001) Zebrafish colourless encodes sox10 and specifies non-ectomesenchymal neural crest fates. Development 128: 4113-4125.
50. Luo R, An M, Arduini BL, Henion PD, (2001) Specific pan-neural crest expression of zebrafish Crestin throughout embryonic development. Dev Dyn 220: 169-174.
51. 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.
52. 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.
53. Hou L, Pavan WJ, (2008) Transcriptional and signaling regulation in neural crest stem cell-derived melanocyte development: do all roads lead to Mitf? Cell Res 18: 1163-1176.
54. Curran K, Raible DW, Lister JA, (2009) Foxd3 controls melanophore specification in the zebrafish neural crest by regulation of Mitf. Dev Biol 332: 408-417.
55. 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.
56. Elworthy S, Lister JA, Carney TJ, Raible DW, Kelsh RN, (2003) Transcriptional regulation of mitfa accounts for the sox10 requirement in zebrafish melanophore development. Development 130: 2809-2818.
57. Harris ML, Baxter LL, Loftus SK, Pavan WJ, (2010) Sox proteins in melanocyte development and melanoma. Pigment Cell Melanoma Res 23: 496-513.
58. 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.
59. 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.
60. Parichy DM, Turner JM, (2003) Temporal and cellular requirements for Fms signaling during zebrafish adult pigment pattern development. Development 130: 817-833.
61. Thomas AJ, Erickson CA, (2009) FOXD3 regulates the lineage switch between neural crest-derived glial cells and pigment cells by repressing MITF through a non-canonical mechanism. Development 136: 1849-1858.
62. Adameyko I, Lallemend F, Aquino JB, Pereira JA, Topilko P, et al. (2009) Schwann cell precursors from nerve innervation are a cellular origin of melanocytes in skin. Cell 139: 366-379.
63. Nichols DH, Weston JA, (1977) Melanogenesis in cultures of peripheral nervous tissue. I. The origin and prospective fate of cells giving rise to melanocytes. Dev Biol 60: 217-225.
64. Dupin E, Glavieux C, Vaigot P, Le Douarin NM, (2000) Endothelin 3 induces the reversion of melanocytes to glia through a neural crest-derived glial-melanocytic progenitor. Proc Natl Acad Sci U S A 97: 7882-7887.
65. Dupin E, Real C, Glavieux-Pardanaud C, Vaigot P, Le Douarin NM, (2003) Reversal of developmental restrictions in neural crest lineages: transition from Schwann cells to glial-melanocytic precursors in vitro. Proc Natl Acad Sci U S A 100: 5229-5233.
66. Watanabe K, Washio Y, Fujinami Y, Aritaki M, Uji S, et al. (2008) Adult-type pigment cells, which color the ocular sides of flounders at metamorphosis, localize as precursor cells at the proximal parts of the dorsal and anal fins in early larvae. Dev Growth Differ 50: 731-741.
67. Yamada T, Okauchi M, Araki K, (2010) Origin of adult-type pigment cells forming the asymmetric pigment pattern, in Japanese flounder (Paralichthys olivaceus). Dev Dyn 239: 3147-3162.
68. Liu Y, Labosky PA, (2008) Regulation of embryonic stem cell self-renewal and pluripotency by Foxd3. Stem Cells 26: 2475-2484.
69. Hanna LA, Foreman RK, Tarasenko IA, Kessler DS, Labosky PA, (2002) Requirement for Foxd3 in maintaining pluripotent cells of the early mouse embryo. Genes Dev pp. 2650-2661.
70. Teng L, Mundell NA, Frist AY, Wang Q, Labosky PA, (2008) Requirement for Foxd3 in the maintenance of neural crest progenitors. Development 135: 1615-1624.
71. Mundell NA, Labosky PA, (2011) Neural crest stem cell multipotency requires Foxd3 to maintain neural potential and repress mesenchymal fates. Development.
72. Ignatius MS, Moose HE, El-Hodiri HM, Henion PD, (2008) colgate/hdac1 Repression of foxd3 expression is required to permit mitfa-dependent melanogenesis. Dev Biol 313: 568-583.
73. Buac K, Xu M, Cronin J, Weeraratna AT, Hewitt SM, et al. (2009) NRG1/ERBB3 signaling in melanocyte development and melanoma: inhibition of differentiation and promotion of proliferation. Pigment Cell Melanoma Res 22: 773-784.
74. 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.
75. Yang CT, Johnson SL, (2006) Small molecule-induced ablation and subsequent regeneration of larval zebrafish melanocytes. Development 133: 3563-3573.
76. Yang CT, Sengelmann RD, Johnson SL, (2004) Larval melanocyte regeneration following laser ablation in zebrafish. J Invest Dermatol 123: 924-929.
77. 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.
78. Rawls JF, Johnson SL, (2001) Requirements for the kit receptor tyrosine kinase during regeneration of zebrafish fin melanocytes. Development 128: 1943-1949.
79. Lee Y, Nachtrab G, Klinsawat PW, Hami D, Poss KD, (2010) Ras controls melanocyte expansion during zebrafish fin stripe regeneration. Dis Model Mech 3: 496-503.
80. Kondo S, Shirota H, (2009) Theoretical analysis of mechanisms that generate the pigmentation pattern of animals. Semin Cell Dev Biol 20: 82-89.
81. 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.
82. Goodrich HB, Greene JM, (1959) An experimental analysis of the development of a color pattern in the fish Brachydanio albolineatus Blyth. J exp Zool 141: 15-45.
83. Goodrich HB, Marzullo CM, Bronson WR, (1954) An analysis of the formation of color patterns in two fresh-water fish. J exp Zool 125: 487-505.
84. 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.
85. Greco V, Guo S, (2010) Compartmentalized organization: a common and required feature of stem cell niches? Development 137: 1586-1594.
86. Li L, Clevers H, (2010) Coexistence of quiescent and active adult stem cells in mammals. Science 327: 542-545.
87. Zammit PS, (2008) All muscle satellite cells are equal, but are some more equal than others? J Cell Sci 121: 2975-2982.
88. Quigley IK, 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.
89. Bafaloukos D, Gogas H, (2004) The treatment of brain metastases in melanoma patients. Cancer Treat Rev 30: 515-520.
90. Palmieri D, Chambers AF, Felding-Habermann B, Huang S, Steeg PS, (2007) The biology of metastasis to a sanctuary site. Clin Cancer Res 13: 1656-1662.
91. 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.
92. 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.
93. Budi EH, Patterson LB, Parichy DM, (2010) Morphogenesis of post-embryonic neural crest-derived pigment cell precursors revealed by time lapse imaging during zebrafish adult pigment pattern formation. Dev Biol 344: 448.
94. Park HC, Boyce J, Shin J, Appel B, (2005) Oligodendrocyte specification in zebrafish requires notch-regulated cyclin-dependent kinase inhibitor function. J Neurosci 25: 6836-6844.
95. Lyons DA, Pogoda HM, Voas MG, Woods IG, Diamond B, et al. (2005) erbb3 and erbb2 are essential for schwann cell migration and myelination in zebrafish. Curr Biol 15: 513-524.
96. Kelsh RN, Schmid B, Eisen JS, (2000) Genetic analysis of melanophore development in zebrafish embryos. Dev Biol 225: 277-293.
97. Guyonneau L, Murisier F, Rossier A, Moulin A, Beermann F, (2004) Melanocytes and pigmentation are affected in dopachrome tautomerase knockout mice. Mol Cell Biol 24: 3396-3403.
98. Carney TJ, Dutton KA, Greenhill E, Delfino-Machin M, Dufourcq P, et al. (2006) A direct role for Sox10 in specification of neural crest-derived sensory neurons. Development 133: 4619-4630.