Abstract
In amniotes, the developmental potentials of neural crest cells differ between the cranium and the trunk. These differences may be attributable to the different expression patterns of Hox genes between cranial and trunk neural crest cells. However, little is known about the factors that control Hox genes expression in neural crest cells. The present data demonstrate that retinoic acid (RA) treatment and the activation of Wnt signaling induce Hoxa2 and Hoxd9 expression, respectively, in mouse mesencephalic neural crest cells, which never express Hox genes in vivo. Furthermore, Wnt signaling suppresses the induction of Hoxa2. We also demonstrate that these factors participate in the maintenance of Hoxa2 and Hoxd9 expression in mouse trunk neural crest cells. Our results suggest that RA and Wnt signaling function as environmental factors that regulate the expression of Hoxa2 and Hoxd9 in mouse neural crest cells.
Similar content being viewed by others
References
Abzhanov A, Tzahor E, Lassar AB, Tabin CJ (2003) Dissimilar regulation of cell differentiation in mesencephalic (cranial) and sacral (trunk) neural crest cells in vitro. Development 130:4567–4579
Bel-Vialar S, Itasaki N, Krumlauf R (2002) Initiating Hox gene expression: in the early chick neural tube differential sensitivity to FGF and RA signaling subdivides the HoxB genes in two distinct groups. Development 129:5103–5115
Burke AC, Nelson CE, Morgan BA, Tabin C (1995) Hox genes and the evolution of vertebrate axial morphology. Development 121:333–346
Canning CA, Lee L, Irving C, Mason I, Jones CM (2007) Sustained interactive Wnt and FGF signaling is required to maintain isthmic identity. Dev Biol 305:276–286
Castelo-Branco G, Wagner J, Rodriguez FJ, Kele J, Sousa K, Rawal N, Pasolli HA, Fuchs E, Kitajewski J, Arenas E (2003) Differential regulation of midbrain dopaminergic neuron development by Wnt-1, Wnt-3a, and Wnt-5a. Proc Natl Acad Sci USA 100:12747–12752
Chung EJ, Hwang SG, Nguyen P, Lee S, Kim JS, Kim JW, Henkart PA, Bottaro DP, Soon L, Bonvini P, Lee SJ, Karp JE, Oh HJ, Rubin JS, Trepel JB (2002) Regulation of leukemic cell adhesion, proliferation, and survival by β-catenin. Blood 100:982–990
Ciruna B, Rossant J (2001) FGF signaling regulates mesoderm cell fate specification and morphogenetic movement at the primitive streak. Dev Cell 1:37–49
Couly G, Creuzet S, Bennaceur S, Vincent C, Le Douarin NM (2002) Interactions between Hox-negative cephalic neural crest cells and the foregut endoderm in patterning the facial skeleton in the vertebrate head. Development 129:1061–1073
Creuzet S, Couly G, Vincent C, Le Douarin NM (2002) Negative effect of Hox gene expression on the development of the neural crest-derived facial skeleton. Development 129:4301–4313
Deschamps J, Nes J van (2005) Developmental regulation of the Hox genes during axial morphogenesis in the mouse. Development 132:2931–2942
Hall BK (1999) The neural crest in development and evolution. Springer, New York
Hao Z, Yeung J, Wolf L, Doucette R, Nazarali A (1999) Differential expression of Hoxa-2 protein along the dorsal-ventral axis of the developing and adult mouse spinal cord. Dev Dyn 216:201–217
Hunt P, Gulisano M, Cook M, Sham MH, Faiella A, Wilkinson D, Boncinelli E, Krumlauf R (1991) A distinct Hox code for the branchial region of the vertebrate head. Nature 353:861–864
Ido A, Ito K (2006) Expression of chondrogenic potential of mouse trunk neural crest cells by FGF2 treatment. Dev Dyn 235:361–367
Iimura T, Pourquié O (2007) Hox genes in time and space during vertebrate body formation. Dev Growth Differ 49:265–275
Irioka T, Watanabe K, Mizusawa H, Mizuseki K, Sasai Y (2005) Distinct effects of caudalizing factors on regional specification of embryonic stem cell-derived neural precursors. Brain Res Dev Brain Res 154:63–70
Ito K, Morita T (1995) Role of retinoic acid in mouse neural crest cell development in vitro. Dev Dyn 204:211–218
Ito K, Morita T, Sieber-Blum M (1993) In vitro clonal analysis of mouse neural crest development. Dev Biol 157:517–525
Kappen C (1996) Theoretical approaches to the analysis of homeobox gene evolution. Comput Chem 20:49–59
Korinek V, Barker N, Morin PJ, Wichen D van, Weger R de, Kinzler KW, Vogelstein B, Clevers H (1997) Constitutive transcriptional activation by a β-catenin-Tcf complex in APC-/- colon carcinoma. Science 275:1784–1787
Krumlauf R (1993) Hox genes and pattern formation in the branchial region of the vertebrate head. Trends Genet 9:106–112
Le Douarin NM, Kalcheim C (1999) The neural crest, 2nd edn. Cambridge University Press, Cambridge
Le Douarin NM, Creuzet S, Couly G, Dupin E (2004) Neural crest cell plasticity and its limits. Development 131:4637–4650
Liu JP, Laufer E, Jessell TM (2001) Assigning the positional identity of spinal motor neurons: rostrocaudal patterning of Hox-c expression by FGFs, Gdf11, and retinoids. Neuron 32:997–1012
Maretto S, Cordenonsi M, Dupont S, Braghetta P, Broccoli V, Hassan AB, Volpin D, Bressan GM, Piccolo S (2003) Mapping Wnt/β-catenin signaling during mouse development and in colorectal tumors. Proc Natl Acad Sci USA 100:3299–3304
Martinsen BJ, Bronner-Fraser M (1998) Neural crest specification regulated by the helix-loop-helix repressor Id2. Science 281:988–991
Meijer L, Skaltsounis AL, Magiatis P, Polychronopoulos P, Knockaert M, Leost M, Ryan XP, Vonica CA, Brivanlou A, Dajani R, Crovace C, Tarricone C, Musacchio A, Roe SM, Pearl L, Greengard P (2003) GSK-3-selective inhibitors derived from Tyrian purple indirubins. Chem Biol 10:1255–1266
Nakamura H, Ayer-Le Lièvre CS (1982) Mesectodermal capabilities of the trunk neural crest of birds. J Embryol Exp Morphol 70:1–18
Nakanishi K, Chan YS, Ito K (2007) Notch signaling is required for the chondrogenic specification of mouse mesencephalic neural crest cells. Mech Dev 124:190–203
Noden DM (1978) The control of avian cephalic neural crest cytodifferentiation. I. Skeletal and connective tissues. Dev Biol 67:296–312
Noden DM (1983) The role of the neural crest in patterning of avian cranial skeletal, connective, and muscle tissues. Dev Biol 96:144–165
Nordström U, Maier E, Jessell TM, Edlund T (2006) An early role for WNT signaling in specifying neural patterns of Cdx and Hox gene expression and motor neuron subtype identity. PLoS Biol 4:1438–1452
Prince V, Lumsden A (1994) Hoxa-2 expression in normal and transposed rhombomeres: independent regulation in the neural tube and neural crest. Development 120:911–923
Rockman SP, Currie SA, Ciavarella M, Vincan E, Dow C, Thomas RJ, Phillips WA (2001) Id2 is a target of the β-catenin/T cell factor pathway in colon carcinoma. J Biol Chem 276:45113–45119
Santagati F, Minoux M, Ren SY, Rijli FM (2005) Temporal requirement of Hoxa2 in cranial neural crest skeletal morphogenesis. Development 132:4927–4936
Sato N, Meijer L, Skaltsounis L, Greengard P, Brivanlou AH (2004) Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat Med 10:55–63
Tetsu O, McCormick F (1999) β-Catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398:422–426
Trainor PA, Krumlauf R (2000a) Plasticity in mouse neural crest cells reveals a new patterning role for cranial mesoderm. Nat Cell Biol 2:96–102
Trainor PA, Krumlauf R (2000b) Patterning the cranial neural crest: hindbrain segmentation and Hox gene plasticity. Nat Rev Neurosci 1:116–124
Trainor PA, Ariza-McNaughton L, Krumlauf R (2002) Role of the isthmus and FGFs in resolving the paradox of neural crest plasticity and prepatterning. Science 295:1288–1291
Ying QL, Wray J, Nichols J, Batlle-Morera L, Doble B, Woodgett J, Cohen P, Smith A (2008) The ground state of embryonic stem cell self-renewal. Nature 453:519–523
Acknowledgements
We thank the following investigators for generous gifts of materials: Drs. Jane B. Trepel (pcDNA3 expression vector encoding the human dn TCF and pcDNA4 expression vector encoding the mouse dn β-catenin) and Adil J. Nazarali (rabbit anti-Hoxa2 antibody).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ishikawa, S., Ito, K. Plasticity and regulatory mechanisms of Hox gene expression in mouse neural crest cells. Cell Tissue Res 337, 381–391 (2009). https://doi.org/10.1007/s00441-009-0827-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00441-009-0827-5