The therapeutic potential of stem cells in the treatment of craniofacial abnormalities

Expert Opinion on Biological Therapy

Volumn 4, Issue 5, 2004, Pages 645-657

  Jones, Natalie C ^a   Trainor, Paul A ^a  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

Craniofacial development; Neural crest; Stem cells

Indexed keywords

BIRTH DEFECT; CRANIOFACIAL MALFORMATION; CRANIOFACIAL SYNOSTOSIS; EMBRYO DEVELOPMENT; HUMAN; MANDIBULOFACIAL DYSOSTOSIS; MESENCHYME; NEURAL CREST; REVIEW; STEM CELL; STEM CELL TRANSPLANTATION;

ANIMALS; CRANIOFACIAL ABNORMALITIES; HUMANS; NERVE REGENERATION; NEURAL CREST; STEM CELL TRANSPLANTATION; STEM CELLS;

VERTEBRATA;

EID: 2442647623     PISSN: 14712598     EISSN: None     Source Type: Journal    
DOI: 10.1517/14712598.4.5.645     Document Type: Review

References (118)

1. GORLIN RJ, COHEN MM, LEVIN LS: Syndromes of the Head Neck. Gorlin RJ, Cohen MM, Levin LS (Eds), Oxford University Press, Oxford, UK (1990).
2. NODEN DM: Origins and patterning of craniofacial mesenchymal tissues. J. Craniofacial Genet. Dev. Biol. Suppl. (1986) 2:15-31.
3. ROSENQUIST GC: Epiblast origin and early migration of neural crest cells in the chick embryo. Dev. Biol. (1981) 87:201-211.
4. TAN SS, MORRISS-KAY G: The development and distribution of the cranial neural crest in the rat embryo. Cell Tissue Res. (1985) 240:403-416.
5. BRONNER-FRASER M: Origins and developmental potential of the neural crest. Exp. Cell Res. (1995) 218:405-417.
6. LE DOUARIN NM: The Neural Crest. Le Douarin NM (Ed.) Cambridge University Press, Cambridge, (1982).
7. TRAINOR PA, TAM PPL: Cranial paraxial mesoderm and neural crest of the mouse embryo-codistribution in the craniofacial mesenchyme but distinct segregation in the branchial arches. Development (1995) 121:2569-2582.
8. NODEN DM: An analysis of migratory behavior of avian cephalic neural crest cells. Dev. Biol. (1975) 42:106-130.
9. JOHNSTON MC: A radioautographic study of the migration and fate of cranial neural crest cells in the chick embryo. Anat. Rec. (1966) 156:143-156.
10. TOSNEY K: The segregation and early migration of cranial neural crest cells in the avian embryo. Dev. Biol. (1982) 89:13-24.
11. NICHOLS DH: Formation and distribution of neural crest mesenchyme to the first pharyngeal arch region of the mouse embryo. Am. J. Anat. (1986) 176:221-231.
12. KNECHT AK, BRONNER-FRASER M: Induction of the neural crest: a multigene process. Nat. Rev. Genet. (2002) 3:453-461.
13. VAAGE S: The segmentation of the primitive neural tube in chick embryos (Gallus domesticus). Adv. Anat. Embryol. Cell Biol. (1969) 41:1-88.
14. FRASER S, KEYNES R, LUMSDEN A: Segmentation in the chick embryo hindbrain is defined by cell lineage restrictions. Nature (1990) 344:431-435.
15. LUMSDEN A, KRUMLAUF R: Patterning the vertebrate neuraxis. Science (1996) 274:1109-1115.
16. MARÍN F, PUELLES L: Morphological fate of rhombomeres in quail/chick chimeras: a segmental analysis of hindbrain nuclei. Eur. J. Neurosci. (1995) 7:1714-1738.
17. LUMSDEN A, SPRAWSON N, GRAHAM A: Segmental origin and migration of neural crest cells in the hindbrain region of the chick embryo. Development (1991) 113:1281-1291.
18. FARLIE PG, KERR R, THOMAS P et al.: A paraxial exclusion zone creates patterned cranial neural crest cell outgrowth adjacent to rhombomeres 3 and 5. Dev. Biol. (1999) 213:70-84.
19. LE LIEVRE CS, LE DOUARIN NM: Mesenchymal derivatives of the neural crest: Analysis of chimaeric quail and chick embryos. J. Embryol. Exp. Morphol (1975) 34:125-154.
20. NODEN DM: The migratory behavior of neural crest cells. Symp. Oral Sens. Percept. (1973) (4):9-36.
21. COULY G, LE DOUARIN NM: Head morphogenesis in embryonic avian chimeras: evidence for a segmental pattern in the ectoderm corresponding to the neuromeres. Development (1990) 108:543-558.
22. LUMSDEN AG: Spatial organization of the epithelium and the role of neural crest cells in the initiation of the mammalian tooth germ. Development (1988) 103(Suppl.):155-169.
23. COULY G, CREUZET S, BENNACEUR S, VINCENT C, LE DOUARIN NM: Interactions between Hox-negative cephalic neural crest cells and the foregut endoderm in patterning the facial skeleton in the vertebrate head. Development (2002) 129:1061-1073. This technically demanding, landmark study demonstrated the instructive patterning role of the endoderm in neural crest cell differentiation into cartilage and bone.
24. NODEN D: Patterning of avian craniofacial muscles. Dev. Biol. (1986) 116:347-356.
25. BRONNER-FRASER M, FRASER S: Cell lineage analysis reveals multipotency of some avian neural crest cells. Nature (1988) 335:161-164. This was the first demonstration that individual neural crest cells were multipotent and capable of self-renewal, features they share with stem cells.
26. CANO A, PEREZ-MORENO MA, RODRIGO I et al.: The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat. Cell Biol. (2000) 2:76-83.
27. WILSON P, HEMMATI-BRIVANLOU A: Vertebrate neural induction: inducers, inhibitors and a new synthesis. Neuron (1997) 18:699-710.
28. MAYOR R, MORGAN R, SARGENT MG: Induction of the prospective neural crest of Xenopus. Development (1995) 121:767-777.
29. LA BONNE C, BRONNER-FRASER M: Induction and patterning of the neural crest, a stem cell-like precursor population. J. Neurobiol. (1998) 36:175-189.
30. STREIT A, LEE KJ, WOO I et al.: Chordin regulates primitive streak development and the stability of induced neural cells, but is not sufficient for neural induction in the chick embryo. Development (1998) 125:507-519.
31. FAURE S, DE SANTA BARBARA P, ROBERTS DJ, WHITMAN M: Endogenous patterns of BMP signaling during early chick development. Dev. Biol. (2002) 244:44-65.
32. WILSON SI, GRAZIANO E, HARLAND R, JESSELL TM, EDLUND T: An early requirement for FGF signalling in the acquisition of neural cell fate in the chick embryo. Curr. Biol. (2000) 10:421-429.
33. SELLECK MA, GARCIA-CASTRO MI, ARTINGER KB, BRONNER-FRASER M: Effects of Shh and Noggin on neural crest formation demonstrate that BMP is required in the neural tube but not ectoderm. Development (1998) 125:4919-4930.
34. LIEM KF JR, JESSELL TM, BRISCOE J: Regulation of the neural patterning activity of sonic hedgehog by secreted BMP inhibitors expressed by notochord and somites. Development (2000) 127:4855-4866.
35. GARCIA-CASTRO MI, MARCELLE C, BRONNER-FRASER M: Ectodermal Wnt function as a neural crest inducer. Science (2002) 297:848-851.
36. IKEYA M, LEE SM, JOHNSON JE, MCMAHON AP, TAKADA S: Wnt signalling required for expansion of neural crest and CNS progenitors. Nature (1997) 389:966-970.
37. SAINT-JEANNET JP, HE X, VARMUS HE, DAWID IB: Regulation of dorsal fate in the neuraxis by Wnt-1 and Wnt-3a. Proc. Natl. Acad. Sci. USA (1997) 94:13713-13718.
38. WU J, SAINT-JEANNET JP, KLEIN PS: Wnt-frizzled signaling in neural crest formation. Trends Neurosci. (2003) 26:40-45.
39. TRAINOR P, KRUMLAUF R: Development. Riding the crest of the Wnt signaling wave. Science (2002) 297:781-783.
40. MONSORO-BURQ AH, FLETCHER RB, HARLAND RM: Neural crest induction by paraxial mesoderm in Xenopus embryos requires FGF signals. Development (2003) 130:3111-3124.
41. BAREMBAUM M, MORENO TA, LABONNE C, SECHRIST J, BRONNER-FRASER M: Noelin-1 is a secreted glycoprotein involved in generation of the neural crest. Nat. Cell Biol. (2000) 2:219-225.
42. REEVES FC, BURDGE GC, FREDERICKS WJ, RAUSCHER FJ, LILLYCROP KA: Induction of antisense Pax-3 expression leads to the rapid morphological differentiation of neuronal cells and an altered response to the mitogenic growth factor bFGF. J. Cell Sci. (1999) 112(Pt 2):253-261.
43. DOTTORI M, GROSS MK, LABOSKY P, GOULDING M: The winged-helix transcription factor Foxd3 suppresses interneuron differentiation and promotes neural crest cell fate. Development (2001) 128:4127-4138.
44. CHEUNG M, BRISCOE J: Neural crest development is regulated by the transcription factor Sox9. Development (2003) 130:5681-5693.
45. CORNELL RA, EISEN JS: Delta signaling mediates segregation of neural crest and spinal sensory neurons from zebrafish lateral neural plate. Development (2000) 127:2873-2882.
46. ENDO Y, OSUMI N, WAKAMATSU Y: Bimodal functions of Notch-mediated signaling are involved in neural crest formation during avian ectoderm development. Development (2002) 129:863-873.
47. GAMMILL LS, BRONNER-FRASER M: Genomic analysis of neural crest induction. Development (2002) 129:5731-5741.
48. HUNT P, GULISANO M, COOK M et al.: A distinct Hox code for the branchial region of the head. Nature (1991) 353:861-864.
49. NODEN D: The role of the neural crest in patterning of avian cranial skeletal, connective, and muscle tissues. Dev. Biol. (1983) 96:144-165.
50. TRAINOR P, KRUMLAUF R: Plasticity in mouse neural crest cells reveals a new patterning role for cranial mesoderm. Nat. Cell Biol. (2000) 2:96-102. See [52].
51. GOLDING J, TRAINOR P, KRUMLAUF R, GASSMAN M: Defects in pathfinding by cranial neural crest cells in mice lacking the Neuregulin receptor ErbB4. Nat. Cell Biol. (2000) 2:103-109. See [52].
52. SCHILLING TF, PRINCE V, INGHAM PW: Plasticity in zebrafish hox expression in the hindbrain and cranial neural crest. Dev. Biol. (2001) 231:201-216. These studies collectively provided evidence for neural crest plasticity and the extrinsic control of neural crest patterning.
53. SALDIVAR J, KRULL C, KRUMLAUF R, ARIZA-MCNAUGHTON L, BRONNER-FRASER M: Rhombomere of origin determines autonomous versus environmentally regulated expression of Hoxa3 in the avian embryo. Development (1996) 122:895-904.
54. TRAINOR P, KRUMLAUF R: Patterning the cranial neural crest: Hindbrain segmentation and Hox gene plasticity. Nat. Rev. Neurosci. (2000) 1:116-124.
55. MACONOCHIE M, KRISHNAMURTHY R, NONCHEV S et al.: Regulation of Hoxa2 in cranial neural crest cells involves members of the AP-2 family. Development (1999) 126:1483-1494.
56. NORTHCUTT RG, GANS C: The genesis of neural crest and epidermal placodes: a reinterpretation of vertebrate origins. Q. Rev. Biol. (1983) 58:1-28.
57. PHELPS PD, POSWILLO D, LLOYD GA: The ear deformities in mandibulofacial dysostosis (Treacher Collins syndrome). Clin. Otolaryngol. (1981) 6:15-28.
58. ROVIN S, DACHI SF, BORENSTEIN DB, COTTER WB: Mandibulofacial dysostosis, a familial study of five generations. J. Pediatr. (1964) 65:215-221.
59. FAZEN LE, ELMORE J, NADLER HL: Mandibulo-facial dysostosis. (Treacher-Collins syndrome). Am. J. Dis. Child. (1967) 113:405-410.
60. DIXON J, EDWARDS SJ, ANDERSON I et al.: Identification of the complete coding sequence and genomic organization of the Treacher Collins syndrome gene. Genome Res. (1997) 7:223-234.
61. WISE CA, CHIANG LC, PAZNEKAS WA et al.: TCOF1 gene encodes a putative nucleolar phosphoprotein that exhibits mutations in Treacher Collins Syndrome throughout its coding region. Proc. Natl. Acad. Sci. USA (1997) 94:3110-3115.
62. MARSH KL, DIXON J, DIXON MJ: Mutations in the Treacher Collins syndrome gene lead to mislocalization of the nucleolar protein treacle. Hum. Mol. Genet. (1998) 7:1795-1800.
63. WINOKUR ST, SHIANG R: The Treacher Collins syndrome (TCOF1) gene product, treacle, is targeted to the nucleolus by signals in its C-terminus. Hum. Mol. Genet. (1998) 7:1947-1952.
64. DIXON J, BRAKEBUSCH C, FASSLER R, DIXON MJ: Increased levels of apoptosis in the prefusion neural folds underlie the craniofacial disorder, Treacher Collins syndrome. Hum. Mol. Genet. (2000) 9:1473-1480.
65. WILEY MJ, CAUWENBERGS P, TAYLOR IM: Effects of retinoic acid on the development of the facial skeleton in hamsters: early changes involving cranial neural crest cells. Acta Anat. (Basel) (1983) 116:180-192.
66. POSWILLO D: The pathogenesis of the Treacher Collins syndrome (mandibulofacial dysostosis). Br. J. Oral Surg. (1975) 13:1-26.
67. THOROGOOD P: Embryos, Genes and Birth Defects. Thorogood P (Ed.), John Wiley & Sons Ltd (1997).
68. MOORE KL: The Developing Human, Clinically Oriented Embryology. Moore KL, Persaud TVN, Schmitt W (Eds), W.B. Saunders, Philadelphia, USA (1988).
69. LARSON WJ: Essentials of Human Embryology. Larson WJ (Ed.), Churchill Livingstone, Inc., (1993).
70. WARREN SM, LONGAKER MT: The pathogenesis of craniosynostosis in the fetus. Yonsei Med. J. (2001) 42:646-659.
71. NUCKOLLS GH, SHUM L, SLAVKIN HC: Progress toward understanding craniofacial malformations. Cleft Palate Craniofac. J. (1999) 36:12-26.
72. COHEN MM JR: Craniosynostoses: phenotypic/molecular correlations. Am. J. Med. Genet. (1995) 56:334-339.
73. COHEN MM JR: Short-limb skeletal dysplasias and craniosynostosis: what do they have in common? Pediatr. Radiol. (1997) 27:442-446.
74. DE MOERLOOZE L, DICKSON C: Skeletal disorders associated with fibroblast growth factor receptor mutations. Curr. Opin. Genet. Dev. (1997) 7:378-385.
75. MUENKE M, WILKIE AO: The Metabolic and Molecular Bases of Inherited Disease. Scriver CR, Sly WS (Eds), McGraw-Hill, New York, USA (2001):6117-6146.
76. REARDON W, WINTER RM, RUTLAND P et al.: Mutations in the fibroblast growth factor receptor 2 gene cause Crouzon syndrome. Nat. Genet. (1994) 8:98-103.
77. PAZNEKAS WA, CUNNINGHAM ML, HOWARD TD et al.: Genetic heterogeneity of Saethre-Chotzen syndrome, due to TWIST and FGFR mutations. Am. J. Hum. Genet. (1998) 62:1370-1380.
78. WILKIE AO, SLANEY SF, OLDRIDGE M et al.: Apert syndrome results from localized mutations of FGFR2 and is allelic with Crouzon syndrome. Nat. Genet. (1995) 9:165-172.
79. JABS EW, MULLER U, LI X et al.: A mutation in the homeodomain of the human MSX2 gene in a family affected with autosomal dominant craniosynostosis. Cell (1993) 75:443-450.
80. WILKIE AO, TANG Z, ELANKO N et al.: Functional haploinsufliciency of the human homeobox gene MSX2 causes defects in skull ossification. Nat. Genet. (2000) 24:387-390.
81. EL GHOUZZI V, LE MERRER M, PERRIN-SCHMITT F et al.: Mutations of the TWIST gene in the Saethre-Chotzen syndrome. Nat. Genet. (1997) 15:42-46.
82. GAGE FH, RAY J, FISHER LJ: Isolation, characterization, and use of stem cells from the CNS. Ann. Rev. Neurosci. (1995) 18:159-192.
83. MORRISON SJ, SHAH NM, ANDERSON DJ: Regulatory mechanisms in stem cell biology. Cell (1997) 88:287-298.
84. HALL PA, WATT FM: Stem cells: the generation and maintenance of cellular diversity. Development (1989) 106:619-633.
85. POTTEN CS, LOEFFLER M: Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development (1990) 110:1001-1020.
86. NODEN DM: Patterns and organization of craniofacial skeletogenic and myogenic mesenchyme: a perspective. Prog. Clin. Biol. Res. (1982) 101:167-203.
87. BRONNER-FRASER M, FRASER S: Developmental potential of avian trunk neural crest cells in situ. Neuron (1989) 3:755-766.
88. RUFFINS S, ARTINGER KB, BRONNER-FRASER M: Early migrating neural crest cells can form ventral neural tube derivatives when challenged by transplantation. Dev. Biol. (1998) 203:295-304.
89. SHAH NM, ANDERSON DJ: Integration of multiple instructive cues by neural crest stem cells reveals cell-intrinsic biases in relative growth factor responsiveness. Proc. Natl. Acad Sci USA (1997) 94:11369-11374.
90. STEMPLE DL, ANDERSON DJ: Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell (1992) 71:973-985. This was the first demonstration and characterisation of neural crest stem cells.
91. ZAPPONE MV, GALLI R, CATENA R et al.: Sox2 regulatory sequences direct expression of a (beta)-geo transgene to telencephalic neural stem cells and precursors of the mouse embryo, revealing regionalization of gene expression in CNS stem cells. Development (2000) 127:2367-2382.
92. REX M, ORME A, UWANOGHO D et al.: Dynamic expression of chicken Sox2 and Sox3 genes in ectoderm induced to form neural tissue. Dev. Dyn. (1997) 209:323-332.
93. KIM J, LO L, DORMAND E, ANDERSON DJ: SOX10 maintains multipotency and inhibits neuronal differentiation of neural crest stem cells. Neuron (2003) 38:17-31. See [94].
94. SHAH NM, GROVES AK, ANDERSON DJ: Alternative neural crest cell fates are instructively promoted by TGFbeta superfamily members. Cell (1996) 85:331-343. These studies revealed the importance of extrinsic factors on stem cell fate.
95. BITGOOD MJ, MCMAHON AP: Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev. Biol. (1995) 172:126-138.
96. AKHURST RJ, LEHNERT SA, GATHERER D, DUFFIE E: The role of TGF beta in mouse development. Ann. NY Acad. Sci. (1990) 593:259-271.
97. MILLAN FA, DENHEZ F, KONDAIAH P, AKHURST RJ: Embryonic gene expression patterns of TGF beta 1, beta 2 and beta 3 suggest different developmental functions in vivo. Development (1991) 111:131-143.
98. SHAH NM, MARCHIONNI MA, ISAACS I, STROOBANT P, ANDERSON DJ: Glial growth factor restricts mammalian neural crest stem cells to a glial fate. Cell (1994) 77:349-360.
99. MEYER D, BIRCHMEIER C: Distinct isoforms of neuregulin are expressed in mesenchymal and neuronal cells during mouse development. Proc. Natl. Acad Sci. USA (1994) 91:1064-1068.
100. ARTAVANIS-TSAKONAS S, MATSUNO K, FORTINI ME: Notch signaling. Science (1995) 268:225-232.
101. ARTAVANIS-TSAKONAS S, RAND MD, LAKE RJ: Notch signaling: cell fate control and signal integration in development. Science (1999) 284:770-776.
102. HENRIQUE D, HIRSINGER E, ADAM J et al.: Maintenance of neuroepithelial progenitor cells by Delta-Notch signalling in the embryonic chick retina. Curr. Biol. (1997) 7:661-670.
103. FORTINI ME, REBAY I, CARON LA, ARTAVANIS-TSAKONAS S: An activated Notch receptor blocks cell-fate commitment in the developing Drosophila eye. Nature (1993) 365:555-557.
104. COFFMAN CR, SKOGLUND P, HARRIS WA, KINTNER CR: Expression of an extracellular deletion of Xotch diverts cell fate in Xenopus embryos. Cell (1993) 73:659-671.
105. MORRISON SJ, PEREZ SE, QIAO Z et al.: Transient Notch activation initiates an irreversible switch from neurogenesis to giogenesis by neural crest stem cells. Cell (2000) 101:499-510.
106. ANDERSON DJ: Stem cells and pattern formation in the nervous system: the possible versus the actual. Neuron (2001) 30:19-35.
107. GHI T, PEROLO A, BANZI C et al.: Two-dimensional ultrasound is accurate in the diagnosis of fetal craniofacial malformation. Ultrasound Obstet. Gynecol. (2002) 19:543-551. A retrospective comparison of postnatal craniofacial abnormalities with prenatal diagnosis using two-dimensional ultrasound.
108. LEWANDA AF, MEYERS GA, JABS EW: Craniosynostosis and skeletal dysplasias: fibroblast growth factor receptor defects. Proc. Assoc. Am. Physicians (1996) 108:19-24.
109. GLICK PL, HARRISON MR, GOLBUS MS et al.: Management of the fetus with congenital hydronephrosis II: Prognostic criteria and selection for treatment. J. Pediatr. Surg. (1985) 20:376-387. Applications of in utero fetal surgery and the establishment of important criteria for future practice.
110. HARRISON MR, ADZICK NS, FLAKE AW et al.: Correction of congenital diaphragmatic hernia in utero: VI. Hard-earned lessons. J. Pediatr. Surg. (1993) 28:1411-1417; discussion 1417-1418.
111. LUKS FI: Fetal surgery. Br. Med. J. (1995) 311:1449-1450.
112. ADZICK NS, LONGAKER MT: Fetal Wound Healing. Adzick NS, Longaker MT (Eds), Elsevier Science, New York, USA (1991).
113. DODSON TB, SCHMIDT B, LONGAKER MT, KABAN LB: Fetal cleft lip repair in rabbits: postnatal facial growth after repair. J. Oral Maxillofac. Surg. (1991) 49:603-611.
114. STERN M, SCHMIDT B, DODSON TB, STERN R, KABAN LB: Fetal cleft lip repair in rabbits: histology and role of hyaluronic acid. J. Oral Mixillofac. Surg. (1992) 50:263-268; discussion 269.
115. TOURAINE JL, RAUDRANT D, REBAUD A et al.: In utero transplantation of stem cells in humans: immunological aspects and clinical follow-up of patients. Bone Marrow Transpl. (1992) 9(Suppl. 1):121-126. The first demonstration of in utero fetal stem cell transplantations.
116. DEPREST JA, LUKS FI, PEERS KH et al.: Intrauterine endoscopic creation of urinary tract obstruction in the fetal lamb: a model for fetal surgery. Am. J. Obstet. Gynecol. (1995) 172:1422-1426.
117. DEPREST JA, VAN BALLAER P, EVRARD V et al.: Leuven experience with in-utero vascular obliteration techniques. Ultrasound Obstet. Gynecol. (1995) 6:23.
118. VILLE Y, FRYDMAN R, HECHTER K et al.: Le syndrome transfuseur-transfuse, diagnostic antenatal et nouvelle approche therapeutique. Gynecologie-Obstetrique (1993) 1:440-446.