Malformations of the axial skeleton in Museum Vrolik I: Homeotic transformations and numerical anomalies

American Journal of Medical Genetics

Volumn 134 A, Issue 3, 2005, Pages 268-281

  Oostra, Roelof Jan ^a   Hennekam, Raoul C M ^a   De Rooij, Laurens ^a   Moorman, Antoon F M ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Anatomical collection; Atlas assimilation; Axial skeleton; Cervical ribs; Homeotic transformations; Lodewijk bolk; Lumbar ribs; Museum Vrolik; Occipital vertebra; Somite segmentation; Super numerary vertebrae; Transitional vertebrae; Willem Vrolik

Indexed keywords

ARTICLE; GENE MUTATION; HEAT SHOCK; HOX GENE; HUMAN; HUMAN TISSUE; INFORMATION CENTER; MALFORMATION SYNDROME; MESODERM; NETHERLANDS; NUMERICAL CHROMOSOME ABERRATION; PRIORITY JOURNAL; SCLEROTOME; SKELETON MALFORMATION; SOMITE; VERTEBRA MALFORMATION;

ANIMALS; BODY PATTERNING; BONE AND BONES; GENES, HOMEOBOX; HUMANS; MUSEUMS; NETHERLANDS; SPINE;

EID: 16344369595     PISSN: 15524825     EISSN: None     Source Type: Journal    
DOI: 10.1002/ajmg.a.30639     Document Type: Article

References (96)

1. Abu-Abed S, Dollé P, Metzger D, Beckett B, Chambon P, Petkovich M. 2001. The retinoic acid-metabolizing enzyme, CYP26A1, is essential for normal hindbrain patterning, vertebral identity, and development of posterior structures. Genes Dev 15:226-240.
2. Akasaka T, Kanno M, Balling R, Mieza MA, Taniguchi M, Koseki H. 1996. A role for mel-18, a Polycomb group-related vertebrate gene, during the anteroposterior specification of the axial skeleton. Development 122:1513-1522.
3. Alkema MJ, van der Lugt NM, Bobeldijk RC, Berns A, van Lohuizen M. 1995. Transformation of axial skeleton due to overexpression of bmi-1 in transgenic mice. Nature 374:724-727.
4. Allan D, Houle M, Bouchard N, Meyer BI, Grass P, Lohnes D. 2001. RARgamma and Cdx1 interactions in vertebral patterning. Dev Biol 240:46-60.
5. Anbazhagan R, Raman V. 1997. Homeobox genes: Molecular link between congenital anomalies and cancer. Eur J Cancer 33:635-637.
6. Aoyama H, Asamoto K. 2000. The developmental fate of the rostral/caudal half of a somite for vertebra and rib formation: Experimental confirmation of the resegmentation theory using chick-quail chimeras. Mech Dev 99:71-82.
7. Argao EA, Kern MJ, Branford WW, Scott WJ Jr, Potter SS. 1995. Malformations of the heart, kidney, palate, and skeleton in alpha-MHC-Hoxb-7 transgenic mice. Mech Dev 52:291-303.
8. Baljet B, Oostra RJ. 1998. Historical aspects of the study of malformations in The Netherlands. Am J Med Genet 77:91-99.
9. Barlow JC. 1984. Xenarthrans and pholidotes. In: Anderson S, Jones JK, editors. Orders and families of recent mammals of the world. New York: John Wiley & Sons, pp 219-239.
10. Bland JH. 1987. Disorders of the cervical spine. Toronto: WB Saunders Company.
11. Bolk L. 1899a. De varieties in het grensgebied tusschen hoofd en halswervelkolom bij den mensch en hun beteekenis I. Ned Tijdschr Geneesk 43:625-633.
12. Bolk L. 1899b. De varieties in het grensgebied tusschen hoofd en halswervelkolom bij den mensch en hun beteekenis II. Ned Tijdschr Geneesk 43:751-768.
13. Bolk L. 1900a. De variaties in het grensgebied tusschen hoofd en halswervelkolom bij den mensch en hun beteekenis III. Ned Tijdschr Geneesk 44:46-53.
14. Bolk L. 1900b. Kürzere Mittheilungen aus dem anatomischen Institut zu Amsterdam. Morphol Jahrb 29:79-93.
15. Bornstein PE, Peterson RR. 1966. Numerical variation of the presacral vertebral column in three population groups in North America. Am J Phys Anthropol 25:139-146.
16. Charité J, de Graaff W, Deschamps J. 1995. Specification of multiple vertebral identities by ectopically expressed Hoxb-8. Dev Dyn 204:13-21.
17. Chawengsaksophak K, James R, Hammond VE, Kontgen F, Beck F. 1997. Homeosis and intestinal tumours in Cdx2 mutant mice. Nature 386:84-87.
18. Chen Y, Huang L, Russo AF, Solursh M. 1992. Retinoic acid is enriched in Hensen's node and is developmentally regulated in the early chicken embryo. Proc Natl Acad Sci USA 89:10056-10059.
19. Conlon RA, Rossant J. 1992. Exogenous retinoic acid rapidly induces anterior ectopic expression of murine Hox-2 genes in vivo. Development 116:357-368.
20. Cordes R, Schuster-Gossler K, Serth K, Gossler A. 2004. Specification of vertebral identity is coupled to Notch signalling and the segmentation clock. Development 131:1221-1233.
21. Dusseau JL. 1865. Musée Vrolik. Catalogue de la collection d'anatomie humaine, comparée et pathologique. De M.M. Ger. et W. Vrolik, professeurs à l'Athénée Illustre d'Amsterdam. Amsterdam: J. Roever-Kröber.
22. Faiella A, Wernig M, Consalez GG, Hostick U, Hofmann C, Hustert E, Boncinelli E, Balling R, Nadeau JH. 2000. A mouse model for valproate teratogenicity: Parental effects, homeotic transformations, and altered HOX expression. Hum Mol Genet 9:227-236.
23. Fleming A, Keynes R, Tannahill D. 2004. A central role for the notochord in vertebral patterning. Development 131:873-880.
24. Fromental-Ramain C, Warot X, Lakkaraju S, Favier B, Haack H, Birling C, Dierich A, Dollé P, Chambon P. 1996. Specific and redundant functions of the paralogous Hoxa-9 and Hoxd-9 genes in forelimb and axial skeleton patterning. Development 122:461-472.
25. Frydman M, Cohen HA, Ashkenazi A, Varsano I. 1993. Familial segregation of cervical ribs, sprengel anomaly, preaxial polydactyly, anal atresia, and urethral obstruction: A new syndrome? Am J Med Genet 45:717-720.
26. Fully G, Pineau H. 1960. Détermination de la stature au moyen du squelette. Ann Méd Lég Criminol Police Sci Toxicol 40:145-154.
27. Galis F. 1999. Why do almost all mammals have seven cervical vertebrae? Developmental constraints, Hox genes, and cancer. J Exp Zool/Mol Dev Evol 285:19-26.
28. Hanson RD, Hess JL, Yu BD, Ernst P, van Lohuizen M, Berns A, van der Lugt NM, Shashikant CS, Ruddle FH, Seto M, Korsmeyer SJ. 1999. Mammalian Trithorax and Polycomb-group homologues are antagonistic regulators of homeotic development. Proc Natl Acad Sci USA 96:14372-14377.
29. Hogan BL, Thaller C, Eichele G. 1992. Evidence that Hensen's node is a site of retinoic acid synthesis. Nature 359:237-241.
30. Horan GS, Wu K, Wolgemuth DJ, Behringer RR. 1994. Homeotic transformation of cervical vertebrae in Hoxa-4 mutant mice. Proc Natl Acad Sci USA 91:12644-12648.
31. Horan GS, Kovacs EN, Behringer RR, Featherstone MS. 1995a. Mutations in paralogous Hox genes result in overlapping homeotic transformations of the axial skeleton: Evidence for unique and redundant function. Dev Biol 169:359-372.
32. Horan GS, Ramirez-Solis R, Featherstone MS, Wolgemuth DJ, Bradley A, Behringer RR. 1995b. Compound mutants for the paralogous Hoxa-4, Hoxb-4, and Hoxd-4 genes show more complete homeotic transformations and a dose-dependent increase in the number of vertebrae transformed. Genes Dev 9:1667-1677.
33. Huang R, Zhi Q, Brand-Saberi B, Christ B. 2000. New experimental evidence for somite resegmentation. Anat Embryol (Berl) 202:195-200.
34. Jacobs JJ, van Lohuizen M. 1999. Cellular memory of transcriptional states by Polycomb-group proteins. Semin Cell Dev Biol 10:227-235.
35. Jap-A-Joe SM, Oostra RJ, Maas M, Stoker J, van der Horst CM. 2003. Thanatophoric dysplasia type II with encephalocele and aortic hypoplasia diagnosed in an anatomical specimen. Am J Med Genet 118A: 64-67.
36. Jouve C, Palmeirim I, Henrique D, Seekers J, Gossler A, Ish-Horowicz D, Pourquie O. 2000. Notch signalling is required for cyclic expression of the hairy-like gene HES1 in the presomitic mesoderm. Development 127:1421-1429.
37. Jouve C, Iimura T, Pourquie O. 2002. Onset of the segmentation clock in the chick embryo: Evidence for oscillations in the somite precursors in the primitive streak. Development 129:1107-1117.
38. Kessel M, Gruss P. 1991. Homeotic transformations of murine vertebrae and concomitant alteration of Hox codes induced by retinoic acid. Cell 67:89-104.
39. Kjaer I. 1998. Neuro-osteology. Crit Rev Oral Biol Med 9:224-244.
40. Lanier RR. 1939. The presacral vertebrae of American White and Negro males. Am J Phys Anthropol 25:341-420.
41. Lewis EB. 1978. A gene complex controlling segmentation in Drosophila. Nature 276:565-570.
42. Li ZL, Shiota K. 1999. Stage-specific homeotic vertebral transformations in mouse fetuses induced by maternal hyperthermia during somitogenesis. Dev Dyn 216:336-348.
43. Li ZL, Chisaka O, Koseki H, Akasaka T, Ishibashi M, Shiota K. 1997. Heat shock-induced homeotic transformations of the axial skeleton and associated shifts of Hox gene expression domains in mouse embryos. Reprod Toxicol 11:761-770.
44. Lohnes D, Kastner P, Dierich A, Mark M, LeMeur M, Chambon P. 1993. Function of retinoic acid receptor gamma in the mouse. Cell 73:643-658.
45. Lohnes D, Mark M, Mendelsohn C, Dolle P, Dierich A, Gorry P, Gansmuller A, Chambon P. 1994. Function of the retinoic acid receptors (RARs) during development (I). Craniofacial and skeletal abnormalities in RAR double mutants. Development 120:2723-2748.
46. Lombardi G. 1961. The occipital vertebra. Am J Roentgenol Radium Ther Nucl Med 86:260-269.
47. Luboga S. 2000. Supernumerary lumbar vertebrae in human skeletons at the Galloway Osteological Collection of Makerere University, Kampala. East Afr Med J 77:16-19.
48. Lufkin T, Mark M, Hart CP, Dolle P, LeMeur M, Chambon P. 1992. Homeotic transformation of the occipital bones of the skull by ectopic expression of a homeobox gene. Nature 359:835-841.
49. Lundy JK. 1988. Sacralization of a sixth lumbar vertebra and its effect upon the estimation of living stature. J Forensic Sci 33:1045-1049.
50. Müller F, O'Rahilly R. 1986. Somitic-vertebral correlation and vertebral levels in the human embryo. Am J Anat 177:3-19.
51. Müller F, O'Rahilly R. 2003. Segmentation in staged human embryos: The occipitocervical region revisited. J Anat 203:297-315.
52. Mavilio F, Simeone A, Boncinelli E, Andrews P. 1988. Activation of four homeobox gene clusters in human embryonal carcinoma cells induced to differentiate by retinoic acid. Differentiation 37:73-79.
53. McGinnis W, Krumlauf R. 1992. Homeobox genes and axial patterning. Cell 68:283-302.
54. McGrew MJ, Dale JK, Fraboulet S, Pourquie O. 1998. The lunatic fringe gene is a target of the molecular clock linked to somite segmentation in avian embryos. Curr Biol 8:979-982.
55. McLain K, Schreiner C, Yager KL, Stock JL, Potter SS. 1992. Ectopic expression of Hox-2.3 induces craniofacial and skeletal malformations in transgenic mice. Mech Dev 39:3-16.
56. McPherron AC, Lawler AM, Lee SJ. 1999. Regulation of anterior/posterior patterning of the axial skeleton by growth/differentiation factor 11. Nat Genet 22:260-264.
57. Medina-Martinez O, Bradley A, Ramirez-Solis R. 2000. A large targeted deletion of Hoxb1-Hoxb9 produces a series of single-segment anterior homeotic transformations. Dev Biol 222:71-83.
58. Merks JHM, Smets AM, Van Rijn RR, Kobes J, Caron HN, Maas M, Hennekam RCM. 2005. High incidence of cervical rib anomalies in pediatric leukemia, astrocytoma and germ cell tumor patients. (submitted).
59. Morin-Kensicki EM, Melancon E, Eisen JS. 2002. Segmental relationship between somites and vertebral column in zebrafish. Development 129:3851-3860.
60. Nicolas JF, Mathis L, Bonnerot C, Saurin W. 1996. Evidence in the mouse for self-renewing stem cells in the formation of a segmented longitudinal structure, the myotome. Development 122:2933-2946.
61. Nowak RM. 1999. Walker's mammals of the world. Baltimore: The Johns Hopkins University Press.
62. O'Rahilly R, Muller F, Meyer DB. 1990. The human vertebral column at the end of the embryonic period proper. 4. The sacrococcygeal region. J Anat 168:95-111.
63. Oh SP, Li E. 1997. The signaling pathway mediated by the type IIB activin receptor controls axial patterning and lateral asymmetry in the mouse. Genes Dev 11:1812-1826.
64. Oostra RJ, Baljet B, Hennekam RC. 1994. Brachmann-de Lange syndrome "avant la lettre". Am J Med Genet 52:267-268.
65. Oostra RJ, Baljet B, Schutgens RB, Hennekam RC. 1997. Smith-Lemli-Opitz syndrome diagnosed in a 130-year-old anatomical specimen. Am J Med Genet 68:257-259.
66. Oostra RJ, Baljet B, Dijkstra PF, Hennekam RC. 1998a. Congenital anomalies in the teratological collection of Museum Vrolik in Amsterdam, The Netherlands. I: Syndromes with multiple congenital anomalies. Am J Med Genet 77:100-115.
67. Oostra RJ, Baljet B, Dijkstra PF, Hennekam RC. 1998b. Congenital anomalies in the teratological collection of Museum Vrolik in Amsterdam, The Netherlands. II: Skeletal dysplasias. Am J Med Genet 77:116-134.
68. Oostra RJ, Baljet B, Hennekam RC. 1998c. Severe acrofacial dysostosis with orofacial clefting and tetraphocomelia diagnosed in the plaster cast of a 100-year-old anatomical specimen. Am J Med Genet 78:195-197.
69. Oostra RJ, Baljet B, Verbeeten BW, Hennekam RC. 1998d. Congenital anomalies in the teratological collection of Museum Vrolik in Amsterdam, The Netherlands. III: Primary field defects, sequences, and other complex anomalies. Am J Med Genet 80:46-59.
70. Oostra RJ, Baljet B, Hennekam RC. 1998e. Congenital anomalies in the teratological collection of Museum Vrolik in Amsterdam, The Netherlands. IV: Closure defects of the neural tube. Am J Med Genet 80:60-73.
71. Oostra RJ, Baljet B, Verbeeten BW, Hennekam RC. 1998f. Congenital anomalies in the teratological collection of Museum Vrolik in Amsterdam, The Netherlands. V: Conjoined and acardiac twins. Am J Med Genet 80:74-89.
72. Oostra RJ, Dijkstra PF, Baljet B, Verbeeten BW, Hennekam RC. 1999. A 100-year-old anatomical specimen presenting with boomerang-like skeletal dysplasia: Diagnostic strategies and outcome. Am J Med Genet 85:134-139.
73. Oostra RJ, Van der Wolk S, Hennekam RCM. 2005. Malformations of the axial skeleton in Museum Vrolik: II: Craniosynostoses and suture related anomalies. Am J Med Genet (in press).
74. Palmeirim I, Henrique D, Ish-Horowicz D, Pourquie O. 1997. Avian hairy gene expression identifies a molecular clock linked to vertebrate segmentation and somitogenesis. Cell 91:639-648.
75. Pourquie O. 1999. Notch around the clock. Curr Opin Genet Dev 9:559-565.
76. Remak R. 1850. Untersuchungen über die entwicklung der wirbelthiere. Berlin: Reimer.
77. Saegusa H, Takahashi N, Noguchi S, Suemori H. 1996. Targeted disruption in the mouse Hoxc-4 locus results in axial skeleton homeosis and malformation of the xiphoid process. Dev Biol 174:55-64.
78. Sauser G. 1933. Manifestation der okzipitalplatte an einem menschlichen Schädel. Z Anat Entwicklungsgesch 102:51-67.
79. Schapera J. 1987. Autosomal dominant inheritance of cervical ribs. Clin Genet 31:386-388.
80. Schierhorn H, Schmidt R. 1969. Beitrag zur genealogie und kraniologie der familie meckel. Verh Anat Ges 63:591-599.
81. Schumacher R, Mai A, Gutjahr P. 1992. Association of rib anomalies and malignancy in childhood. Eur J Pediatr 151:432-434.
82. Stern CD, Keynes RJ. 1987. Interactions between somite cells: The formation and maintenance of segment boundaries in the chick embryo. Development 99:261-272.
83. Stiemens MJ. 1929. Über die concrescentia atlanto-occipitalis. Verh Kon Akad Wetensch Amst 24(5):1-51.
84. Subramanian V, Meyer BI, Gruss P. 1995. Disruption of the murine homeobox gene Cdx1 affects axial skeletal identities by altering the mesodermal expression domains of Hox genes. Cell 83:641-653.
85. Suzuki M, Mizutani-Koseki Y, Fujimura Y, Miyagishima H, Kaneko T, Takada Y, Akasaka T, Tanzawa H, Takihara Y, Nakano M, Masumoto H, Vidal M, Isono K, Koseki H. 2002. Involvement of the Polycomb-group gene Ring1B in the specification of the anterior-posterior axis in mice. Development 129:4171-4183.
86. Takihara Y, Tomotsune D, Shirai M, Katoh-Fukui Y, Nishii K, Motaleb MA, Nomura M, Tsuchiya R, Fujita Y, Shibata Y, Higashinakagawa T, Shimada K. 1997. Targeted disruption of the mouse homologue of the Drosophila polyhomeotic gene leads to altered anteroposterior patterning and neural crest defects. Development 124:3673-3682.
87. Tini PG, Wieser C, Zinn WM. 1977. The transitional vertebra of the lumbosacral spine: Its radiological classification, incidence, prevalence, and clinical significance. Rheumatol Rehabil 16:180-185.
88. Trotter M, Gleser G. 1958. Re-evaluation of stature based on measurements taken during life and of long bones after death. Am J Phys Anthropol 16:79-123.
89. Usher BM, Christensen MN. 2000. A sequential developmental field defect of the vertebrae, ribs, and sternum, in a young woman of the 12th century AD. Am J Phys Anthropol 111:355-367.
90. Van der Lugt NM, Domen J, Linders K, van Roon M, Robanus-Maandag E, te Riele H, van der Valk M, Deschamps J, Sofroniew M, van Lohuizen M. 1994. Posterior transformation, neurological abnormalities, and severe hematopoietic defects in mice with a targeted deletion of the bmi-1 protooncogene. Genes Dev 8:757-769.
91. Van Tulder MW, Assendelft WJ, Koes BW, Bouter LM. 1997. Spinal radiographic findings and nonspecific low back pain. A systematic review of observational studies. Spine 22:427-434.
92. Weston WJ. 1956. Genetically determined cervical ribs: A family study. Br J Radiol 29:455-456.
93. Wigh RE. 1980. The thoracolumbar and lumbosacral transitional junctions. Spine 5:215-222.
94. Winter RM, Baraitser M. 2001. London dysmorphology database. London: Oxford University Press.
95. Yu BD, Hess JL, Horning SE, Brown GA, Korsmeyer SJ. 1995. Altered Hox expression and segmental identity in Mll-mutant mice. Nature 378:505-508.
96. Zákány J, Kmita M, Alarcon P, de la Pompa JL, Duboule D. 2001. Localized and transient transcription of Hox genes suggests a link between patterning and the segmentation clock. Cell 106:207-217.