Spatiotemporal changes in cell adhesiveness during vertebrate limb morphogenesis

Developmental Dynamics

Volumn 240, Issue 5, 2011, Pages 969-978

  Wada, Naoyuki ^a  

^a TOKYO UNIVERSITY OF SCIENCE   (Japan)

Author keywords

Cell adhesiveness; Cell motility; Limb development; Limb initiation; Limb regeneration; Mesenchymal condensation

Indexed keywords

CADHERIN; EPHRIN; EPHRIN A2; EPHRIN A4; EPHRIN A5; EPHRIN B1; EPHRIN RECEPTOR; FIBROBLAST GROWTH FACTOR 4; FIBROBLAST GROWTH FACTOR 8; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; HOMEODOMAIN PROTEIN; HOX PROTEIN; PROTEIN PROD 1; RETINOIC ACID; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TBX5; UNCLASSIFIED DRUG; WNT5A PROTEIN;

BLASTEMA; CELL ADHESION; CELL AGGREGATION; CELL MIGRATION; CELL SELECTION; CELL SURFACE; CELLULAR DISTRIBUTION; CHONDROGENESIS; EMBRYO PATTERN FORMATION; HOMEOBOX; HOX GENE; LIMB DEVELOPMENT; LIMB REGENERATION; MESENCHYME; MESENCHYME CELL; MESODERM; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; SURFACE PROPERTY; SURFACE TENSION;

ANIMALS; CELL ADHESION; CELL MOVEMENT; EXTREMITIES; LIMB BUDS; MESODERM; MORPHOGENESIS; REGENERATION; VERTEBRATES;

VERTEBRATA;

EID: 79955027607     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22552     Document Type: Review

References (82)

1. Ahn DG, Kourakis MJ, Rohde LA, Silver LM, Ho RK. 2002. T-box gene tbx5 is essential for formation of the pectoral limb bud. Nature 417: 754-758.
2. Ahrens MJ, Li Y, Jiang H, Dudley AT. 2009. Convergent extension movements in growth plate chondrocytes require gpi-anchored cell surface proteins. Development 136: 3463-3474.
3. Arques CG, Doohan R, Sharpe J, Torres M. 2007. Cell tracing reveals a dorsoventral lineage restriction plane in the mouse limb bud mesenchyme. Development 134: 3713-3722.
4. Baker RK, Vanderboom AK, Bell GW, Antin PB. 2001. Expression of the receptor tyrosine kinase gene EphB3 during early stages of chick embryo development. Mech Dev 104: 129-132.
5. Barna M, Niswander L. 2007. Visualization of cartilage formation: Insight into cellular properties of skeletal progenitors and chondrodysplasia syndromes. Dev Cell 12: 931-941.
6. Chen H, Lun Y, Ovchinnikov D, Kokubo H, Oberg KC, Pepicelli CV, Gan L, Lee B, Johnson RL. 1998. Limb and kidney defects in Lmx1b mutant mice suggest an involvement of LMX1B in human nail patella syndrome. Nat Genet 19: 51-55.
7. Cobb J, Duboule D. 2005. Comparative analysis of genes downstream of the Hoxd cluster in developing digits and external genitalia. Development 132: 3055-3067.
8. Cohn MJ, Izpisua-Belmonte J-C, Abud H, Heath J, Tickle C. 1995. Fibroblast growth factors induce additional limb development from the flank of chick embryos. Cell 80: 739-746.
9. Compagni A, Logan M, Klein R, Adams RH. 2003. Control of skeletal patterning by ephrinB1-EphB interactions. Dev Cell 5: 217-230.
10. Crawford K, Stocum DL. 1988. Retinoic acid coordinately proximalizes regenerate pattern and blastema differential affinity in axolotl limbs. Development 102: 687-698.
11. Creuzet S, Schuler B, Couly G, Le Douarin NM. 2004. Reciprocal relationships between Fgf8 and neural crest cells in facial and forebrain development. Proc Natl Acad Sci USA 101: 4843-4847.
12. Crossley PH, Minowada G, MacArthur CA, Martin GR. 1996. Roles for FGF8 in the induction, initiation, and maintenance of chick limb development. Cell 84: 127-136.
13. Damon BJ, Mezentseva NV, Kumaratilake JS, Forgacs G, Newman SA. 2008. Limb bud and flank mesoderm have distinct "physical phenotypes" that may contribute to limb budding. Dev Biol 321: 319-330.
14. da Silva SM, Gates PB, Brockes JP. 2002. The newt ortholog of CD59 is implicated in proximodistal identity during amphibian limb regeneration. Dev Cell 3: 547-555.
15. Davy A, Aubin J, Soriano P. 2004. Ephrin-B1 forward and reverse signaling are required during mouse development. Genes Dev 18: 572-583.
16. Dealy CN, Roth A, Ferrari D, Brown AM, Kosher RA. 1993. Wnt-5a and Wnt-7a are expressed in the developing chick limb bud in a manner suggesting roles in pattern formation along the proximodistal and dorsoventral axes. Mech Dev 43: 175-186.
17. Echeverri K, Tanaka EM. 2005. Proximodistal patterning during limb regeneration. Dev Biol 279: 391-401.
18. Ede DA. 1983. Cellular condensations and chondrogenesis. In: Hall BK, editors. Cartilage, vol. 2. San Diego: Academic Press. p 143-186.
19. Ede DA, Agerbak GS. 1968. Cell adhesion and movement in relation to the developing limb pattern in normal and talpid mutant chick embryos. J Embryol Exp Morphol 20: 81-100.
20. Ede DA, Flint OP. 1975. Cell movement and adhesion in the developing chick wing bud: studies on cultured mesenchyme cells from normal and talpid mutant embryos. J Cell Sci 18: 301-313.
21. Flenniken AM, Gale NW, Yancopoulos GD, Wilkinson DG. 1996. Distinct and overlapping expression patterns of ligands for Eph-related receptor tyrosine kinases during mouse embryogenesis. Dev Biol 179: 382-401.
22. Fromental-Ramain C, Warot X, Massadecq N, Lemeur M, Dolle P, Chambon P. 1996. Hoxa-13 and Hoxd-13 play a crucial role in the patterning of the limb autopod. Development 122: 2297-3011.
23. Garza-Garcia AA, Driscoll PC, Brockes JP. 2010. Evidence for the local evolution of mechanisms underlying limb regeneration in salamanders. Integr Comp Biol 50: 528-535.
24. Hall BK, Miyake T. 2000. All for one and one for all: condensations and the initiation of skeletal development. Bioessays 22: 138-147.
25. Heintzelman KF, Phillips HM, Davis GS. 1978. Liquid-tissue behavior and differential cohesiveness during chick limb budding. J Embryol Exp Morphol 47: 1-15.
26. Holder N, Klein R. 1999. Eph receptors and ephrins: effectors of morphogenesis. Development 126: 2033-2044.
27. Ide H, Wada N, Uchiyama K. 1994. Sorting out of cells from different parts and stages of the chick limb bud. Dev Biol 162: 71-76.
28. Kania A, Jessell TM. 2003. Topographic motor projections in the limb imposed by LIM homeodomain protein regulation of Ephrin-A:EphA interactions. Neuron 38: 581-596.
29. Kawakami Y, Wada N, Nishimatsu S-i, Ishikawa T, Noji S, Nohno T. 1999. Involvement of Wnt-5a in chondrogenic pattern formation in the chick limb bud. Dev Growth Differ 41: 29-40.
30. Kawakami Y, Capdevila J, Büscher D, Itoh T, Rodríguez-Esteban C, Izpisúa-Belmonte JC. 2001. WNT signals control FGF-dependent limb initiation and AER induction in the chick embryo. Cell 104: 891-900.
31. Kawakami Y, Uchiyama Y, Rodriguez-Esteban C, Inenaga T, Koyano-Nakagawa N, Kawakami H, Marti M, Kmita M, Monaghan-Nichols P, Nishinakamura R, Izpisua-Belmonte JC. 2009. Sall genes regulate region-specific morphogenesis in the mouse limb by modulating Hox activities. Development 136: 585-594.
32. Kim D, Kang SS, Jin EJ. 2009. Alterations in the temporal expression and function of cadherin-7 inhibit cell migration and condensation during chondrogenesis of chick limb mesenchymal cells in vitro. J Cell Physiol 221: 161-170.
33. Kimura Y, Matsunami H, Inoue T, Shimamura K, Uchida N, Ueno T, Miyazaki T, Takeichi M. 1995. Cadherin-11 expressed in association with mesenchymal morphogenesis in the head, somite, and limb bud of early mouse embryos. Dev Biol 169: 347-358.
34. Kitajima K, Koshimizu U, Nakamura T, 1999. Expression of a novel type of classic cadherin, PB-cadherin in developing brain and limb buds. Dev Dyn 215: 206-214.
35. Koibuchi N, Tochinai S. 1998. Existence of gradient in cell adhesiveness along the developing Xenopus hindlimb bud, shown by a cellular sorting-out experiment in vitro. Dev Growth Differ 40: 355-362.
36. Kragl M, Knapp D, Nacu E, Khattak S, Maden M, Epperlein HH, Tanaka EM. 2009. Cells keep a memory of their tissue origin during axolotl limb regeneration. Nature 460: 60-65.
37. Kullander K, Klein R. 2002. Mechanisms and functions of Eph and ephrin signalling. Nat Rev Mol Cell Biol 3: 475-486.
38. Li S, Muneoka K. 1999. Cell migration and chick limb development: Chemotactic action of FGF-4 and the AER. Dev Biol 211: 335-347.
39. Maden M. 1983. The effect of vitamin A on the regenerating axolotl limb. J Embryol Exp Morphol 77: 273-295.
40. Mercader N, Leonardo E, Azpiazu N, Serrano A, Morata G, Carlos-Martinez A, Torres M. 1999. Conserved regulation of proximodistal limb axis development by Meis1/Hth. Nature 402: 425-429.
41. Mercader N., Leonardo E., Piedra ME., Carlos-Martinez A, Ros MA., Torres M. 2000. Opposing RA and FGF signals control proximodistal vertebrate limb development through regulation of Meis genes. Development 127: 3961-3970.
42. Mercader N, Selleri L, Criado LM, Pallares P, Parras C, Cleary ML, Torres M. 2009. Ectopic Meis1 expression in the mouse limb bud alters P-D patterning in a Pbx1-independent manner. Int J Dev Biol 53: 1483-1494.
43. Minguillon C, Del Buono J, Logan MP. 2005. Tbx5 and Tbx4 are not sufficient to determine limb-specific morphologies but have common roles in initiating limb outgrowth. Dev Cell 8: 75-84.
44. Moscona A. 1956. Development of heterotypic combinations of dissociated embryonic chick cells. Proc Soc Exp Biol Med 92: 410-416.
45. Nardi JB, Stocum DL. 1983. Surface properties of regenerating limb cells: Evidence for gradiation along the proximodistal axis. Differentiation 25: 27-31.
46. Nelson CE, Morgan BA, Burke AC, Laufer E, DiMambro E, Murtaugh LC, Gonzales E, Tessarollo L, Parada LF. Tabin CJ. 1996. Analysis of Hox gene expression in the chick limb bud. Development 122: 1449-1466.
47. Ohta K, Nakamura M, Hirosawa K, Tanaka S, Iwama A, Suda T, Ando M. Tanaka H. 1996. The tyrosine kinase, Cek8, is transiently expressed on subtypes of motoneurons in the spinal cord during development. Mech Dev 54: 59-69.
48. Ohgo S, Itoh A, Suzuki M, Satoh A, Yokoyama H, Tamura K. 2010. Analysis of hoxa11 and hoxa13 expression during patternless limb regeneration in Xenopus. Dev Biol 338: 148-157.
49. Ohuchi H, Nakagawa T, Yamaguchi M, Ohata T, Yoshioka H, Kuwana T, Miwa T, Mikawa T, Nohno T, Noji S. 1995. An additional limb can be induced from the flank of the chick embryo by FGF4. Biochem Biophys Res Commun 209: 809-386.
50. Ohuchi H, Nakagawa T, Yamamoto A, Araga A, Ohata T, Ishimaru Y, Yoshioka H, Kuwana T, Nohno T, Yamasaki M, Itoh N, Noji S. 1997. The mesenchymal factor, FGF10, initiates and maintains the outgrowth of the chick limb bud through interaction with FGF8, an apical ectodermal factor. Development. 124: 2235-2244.
51. Omi M, Anderson R, Muneoka K. 2002. Differential cell affinity and sorting of anterior and posterior cells during outgrowth of recombinant avian limb buds. Dev Biol 250: 292-304.
52. Pasquale EB. 2005. Eph receptor signalling casts a wide net on cell behaviour. Nat Rev Mol Cell Biol 6: 462-475.
53. Patel K, Nittenberg R, D'Souza D, Irving C, Burt D, Wilkinson DG, Tickle C. 1996. Expression and regulation of Cek-8, a cell to cell signaling receptor in developing chick limb buds. Development 122: 1147-1155.
54. Pearson JC, Lemons D, McGinnis W. 2005. Modulating Hox gene functions during animal body patterning. Nat Rev Genet 6: 893-904.
55. Pecorino LT, Entwistle A, Brockes JP. 1996. Activation of a single retinoic acid receptor isoform mediates proximodistal respecification. Curr Biol. 6: 563-569.
56. Qiu Q, Chen H, Johnson RL. 2009. Lmx1b-expressing cells in the mouse limb bud define a dorsal mesenchymal lineage compartment. Genesis 47: 224-233.
57. Rallis C, Bruneau BG, Del Buono J, Seidman CE, Seidman JG, Nissim S, Tabin CJ, Logan MP. 2003. Tbx5 is required for forelimb bud formation and continued outgrowth. Development. 130: 2741-2751.
58. Riddle R, Ensini M, Nelson C, Tsuchida T, Jessell TM, Tabin CJ. 1995. Induction of the LIM homeobox gene Lmx1 by WNT7a establishes dorsoventral pattern in the vertebrate limb. Cell 83: 631-640.
59. Salsi V, Zappavigna V. 2006. Hoxd13 and Hoxa13 directly control the expression of the EphA7 Ephrin tyrosine kinase receptor in developing limbs. J Biol Chem 281: 1992-1999.
60. Stadler HS, Higgins KM, Capecchi MR. 2001. Loss of Eph-receptor expression correlates with loss of cell adhesion and chondrogenic capacity in Hoxa13 mutant limbs. Development 128: 4177-4188.
61. Steinberg MS. 1970. Does differential adhesion govern self-assembly processes in histogenesis? Equilibrium configurations and the emergence of a hierarchy among populations of embryonic cells. J Exp Zool 173: 395-433.
62. Stott NS, Jiang T-X, Chuong C-M. 1999. Successive formative stages of precartilaginous mesenchymal condensations in vitro: modulation of cell adhesion by Wnt-7A and BMP-2. J Cell Physiol 180: 314-324.
63. Shubin NH, Alberch P. 1986. A morphogenetic approach to the origin and basic organization of the tetrapod limb. Evol Biol 20: 319-387.
64. Tamura K, Yokouchi Y, Kuroiwa A, Ide H. 1997. Retinoic acid changes the proximodistal developmental competence and affinity of distal cells in the developing chick limb bud. Dev Biol 188: 224-234.
65. Towers M, Tickle C. 2009a. Growing models of vertebrate limb development. Development 136: 179-190.
66. Towers M, Tickle C. 2009b. Generation of pattern and form in the developing limb. Int J Dev Biol 53: 805-812.
67. Townes PL. Holtfreter J. 1955. Directed movements and selective adhesion of embryonic amphibian cells. J Exp Zool 128: 53-120.
68. Vogel A, Rodriguez C, Izpisua-Belmonte JC. 1996. Involvement of FGF-8 in initiation, outgrowth and patterning of the vertebrate limb. Development 122: 1737-1750.
69. Wada N, Ide H. 1994. Sorting out of limb bud cells in monolayer culture. Int J Dev Biol 38: 351-356.
70. Wada N, Uchiyama K, Ide H. 1993. Cell sorting out and chondrogenic aggregate formation in limb bud recombinant and in culture. Dev Growth Differ 35: 421-430.
71. Wada N, Kimura I, Tanaka H, Ide H, Nohno T. 1998. Glycosylphosphatidylinositol-anchored cell surface proteins regulate position-specific cell affinity in the limb bud. Dev Biol 202: 244-252.
72. Wada N, Tanaka H, Ide H, Nohno T. 2003. Ephrin-A2 regulates position-specific cell affinity and is involved in cartilage morphogenesis in the chick limb bud. Dev Biol 264: 550-563.
73. Wilkinson DG. 2001. Multiple roles of Eph receptors and ephrins in neural development. Nat Rev Neurosci 2: 155-164.
74. Wyngaarden LA, Vogeli KM, Ciruna BG, Wells M, Hadjantonakis AK, Hopyan S. 2010. Oriented cell motility and division underlie early limb bud morphogenesis. Development 137: 25512558.
75. Yamaguchi TP, Bradley A, McMahon AP, Jones S. 1999. A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 126: 1211-1223.
76. Yajima H, Yonei-Tamura S, Wanatabe N, Tamura K, Ide H. 1999. Role of N-cadherin in the sorting-out of mesenchymal cells and in the positional identity along the proximodistal axis of the chick limb bud. Dev Dyn 216: 274-284.
77. Yajima H, Hara H, Ide H, Tamura K. 2002. Cell adhesiveness and affinity for limb pattern formation. Int J Dev Biol 46: 897-904.
78. Yashiro K, Zhao X, Uehara M, Yamashita K, Nishijima M, Nishino J, Saijoh Y, Sakai Y, Hamada H. 2004. Regulation of retinoic acid distribution is required for proximodistal patterning and outgrowth of the developing mouse limb. Dev Cell 6: 411-422.
79. Yokouchi Y, Sasaki H. Kuroiwa A. 1991. Homeobox gene expression correlated with the bifurcation process of limb cartilage development. Nature 353: 443-445.
80. Yokouchi Y, Nakazato S, Yamamoto M, Goto Y, Kameda K, Iba H, Kuroiwa A. 1995. Misexpression of Hoxa-13 induces cartilage homeotic transformation and changes cell adhesiveness in chick limb buds. Genes Dev 9: 2509-2522.
81. Zeller R, López-Ríos J, Zuniga A. 2009. Vertebrate limb bud development: moving towards integrative analysis of organogenesis. Nat Rev Genet 10: 845-858.
82. Zhu J, Nakamura E, Nguyen MT, Bao X, Akiyama H, Mackem S. 2008. Uncoupling Sonic hedgehog control of pattern and expansion of the developing limb bud. Dev Cell 14: 624-632.