CALL interrupted in a patient with non-specific mental retardation: Gene dosage-dependent alteration of murine brain development and behavior

Human Molecular Genetics

Volumn 12, Issue 13, 2003, Pages 1463-1474

  Frints, Suzanna G M ^a,b   Marynen, Peter ^a   Hartmann, Dieter ^a   Fryns, Jean Pierre ^b   Steyaert, Jean ^b   Schachner, Melitta ^c   Rolf, Bettina ^c   Craessaerts, Katleen ^a   Snellinx, An ^a   Hollanders, Karen ^a   D'Hooge, Rudi ^d   De Deyn, Peter P ^d   Froyen, Guy ^a  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^c UNIVERSITY OF HAMBURG   (Germany)

^d UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CALL PROTEIN; NERVE CELL ADHESION MOLECULE; SYNAPTOPHYSIN; UNCLASSIFIED DRUG; WATER;

AGGRESSIVENESS; ALLELE; ANIMAL BEHAVIOR; ANIMAL CELL; AUTOSOMAL DISORDER; BRAIN DEVELOPMENT; BRAIN REGION; CENTRAL NERVOUS SYSTEM; CHROMOSOME 3P; CHROMOSOME ABERRATION; CHROMOSOME BREAKAGE; CHROMOSOME TRANSLOCATION; CHROMOSOME TRANSLOCATION 3; CHROMOSOME TRANSLOCATION X; CHROMOSOME XP; COGNITIVE DEFECT; CONTROLLED STUDY; DISEASE ASSOCIATION; EXPLORATORY BEHAVIOR; GENE EXPRESSION; GENE FUSION; GENE LOCATION; GENE MUTATION; HIPPOCAMPUS; HUMAN; HUMAN CELL; HYPOTHESIS; IMMUNOHISTOCHEMISTRY; INTRON; KNOCKOUT MOUSE; MAZE TEST; MENTAL DEFICIENCY; MOSSY FIBER; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL NERVOUS SYSTEM; PHENOTYPE; PREDICTION; PRIORITY JOURNAL; PYRAMIDAL TRACT; REVIEW; SOCIAL BEHAVIOR; STAINING; SYNAPSE; WILD TYPE;

AGED; ALLELES; ANIMALS; CHROMOSOMES, HUMAN, PAIR 3; CLONING, MOLECULAR; DNA MUTATIONAL ANALYSIS; DNA, COMPLEMENTARY; GENE DOSAGE; GENE FREQUENCY; GENOTYPE; HIPPOCAMPUS; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION, FLUORESCENCE; MALE; MENTAL RETARDATION; MICE; MICE, TRANSGENIC; MODELS, GENETIC; MUTATION; NEURAL CELL ADHESION MOLECULE L1; PHENOTYPE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SILVER STAINING; TIME FACTORS; TRANSLOCATION, GENETIC;

ANIMALIA; MAMMALIA; MURINAE;

EID: 10744233700     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/ddg165     Document Type: Review

References (78)

1. Riegel, M., Baumer, A., Jamar, M., Delbecque, K., Herens, C., Verloes, A. and Schinzel, A. (2001) Submicroscopic terminal deletions and duplications in retarded patients with unclassified malformation syndromes. Hum. Genet., 109, 286-294.
2. Conte, R.A., Pitter, J.H. and Verma, R.S. (1995) Molecular characterization of trisomic segment 3p24.1→3pter: a case with review of the literature. Clin. Genet., 48, 49-53.
3. Drumheller, T., McGillivray, B.C., Behrner, D., MacLeod, P., McFadden, D.E., Roberson, J., Venditti, C., Chorney, K., Chorney, M. and Smith, D.I. (1996) Precise localisation of 3p25 breakpoints in four patients with the 3p syndrome. J. Med. Genet., 33, 842-847.
4. Reiss, J.A., Sheffield, L.J. and Sutherland, G.R. (1986) Partial trisomy 3p syndrome. Clin. Genet., 30, 50-58.
5. Angeloni, D., Lindor, N.M., Pack, S., Latif, F., Wei, M.H. and Lerman, M.I. (1999) CALL gene is haploinsufficient in a 3p- syndrome patient. Am. J. Med. Genet., 86, 482-485.
6. Cargile, C.B., Goh, D.L., Goodman, B.K., Chen, X.N., Korenberg, J.R., Semenza, G.L. and Thomas, G.H. (2002) Molecular cytogenetic characterization of a subtle interstitial del(3)(p25.3p26.2) in a patient with deletion 3p syndrome. Am. J. Med. Genet., 109, 133-138.
7. Frints, S., Froyen, G., Marynen, P. and Fryns, J.P. (2002) X-linked mental retardation: vanishing boundaries between non-specific (MRX) and syndromic (MRXS) forms. Clin. Genet., 62, 423-432.
8. Molinari, F., Rio, M., Meskenaite, V., Encha-Razavi, F., Auge, J., Bacq, D., Briault, S., Vekemans, M., Munnich, A., Attie-Bitach, T. et al. (2002) Truncating neurotrypsin mutation in autosomal recessive nonsyndromic mental retardation. Science, 298, 1779-1781.
9. Higgins, J.J., Rosen, D.R., Loveless, J.M., Clyman, J.C. and Gran, M.J. (2000) A gene for nonsyndromic mental retardation maps to chromosome 3p25-pter. Neurology, 55, 335-340.
10. Sakurai, K., Migita, O., Toru, M. and Arinami, T. (2002) An association between a missense polymorphism in the close homologue of L1 (CHL1, CALL) gene and schizophrenia. Mol. Psychiat., 7, 412-415.
11. Wei, M.H., Karavanova, I., Ivanov, S.V., Popescu, N.C., Keck, C.L., Pack, S., Eisen, J.A. and Lerman, M.I. (1998) In silico-initiated cloning and molecular characterization of a novel human member of the L1 gene family of neural cell adhesion molecules. Hum. Genet., 103, 355-364.
12. Angeloni, D., Wei, M.H. and Lerman, M.I. (1999) Two single nucleotide polymorphisms (SNPs) in the CALL gene for association studies with IQ. Psychiatr. Genet., 9, 165-167.
13. Kamei, Y., Tsutsumi, O., Taketani, Y. and Watanabe, K. (1998) cDNA cloning and chromosomal localization of neural adhesion molecule NB-3 in human. J. Neurosci. Res., 51, 275-283.
14. Lucas, S., De Plaen, E. and Boon, T. (2000) MAGE-B5, MAGE-B6, MAGE-C2, and MAGE-C3: four new members of the MAGE family with tumor-specific expression. Int. J. Cancer, 87, 55-60.
15. Lurquin, C., De Smet, C., Brasseur, F., Muscatelli, F., Martelange, V., De Plaen, E., Brasseur, R., Monaco, A.P. and Boon, T. (1997) Two members of the human MAGEB gene family located in Xp21.3 are expressed in tumors of various histological origins. Genomics, 46, 397-408.
16. Moreau-Aubry, A., Le Guiner, S., Labarriere, N., Gesnel, M.C., Jotereau, F. and Breathnach, R. (2000) A processed pseudogene codes for a new antigen recognized by a CD8(+) T cell clone on melanoma. J. Exp. Med., 191, 1617-1624.
17. Holm, J., Hillenbrand, R., Steuber, V., Bartsch, U., Moos, M., Lubbert, H., Montag, D. and Schachner, M. (1996) Structural features of a close homologue of L1 (CHL1) in the mouse: a new member of the L1 family of neural recognition molecules. Eur. J. Neurosci., 8, 1613-1629.
18. Liu, Q., Dwyer, N.D. and O'Leary, D.D. (2000) Differential expression of COUP-TFI, CHL1, and two novel genes in developing neocortex identified by differential display PCR. J. Neurosci., 20, 7682-7690.
19. Hillenbrand, R., Molthagen, M., Montag, D. and Schachner, M. (1999) The close homologue of the neural adhesion molecule L1 (CHL1): patterns of expression and promotion of neurite outgrowth by heterophilic interactions. Eur. J. Neurosci., 11, 813-826.
20. Montag-Sallaz, M., Schachner, M. and Montag, D. (2002) Misguided axonal projections, neural cell adhesion molecule 180 mRNA upregulation, and altered behavior in mice deficient for the close homolog of L1. Mol. Cell. Biol., 22, 7967-7981.
21. Lukusa, T., Devriendt, K. and Fryns, J.P. (1999) A 3p deletion syndrome in a child with both del(3)(p25→pter) and dup(17)(q23→qter). Ann. Genet., 42, 91-94.
22. Kleczkowska, A., Fryns, J.P. and Van den Berghe, H. (1984) Partial trisomy of chromosome 3(p14→p22) due to maternal insertional translocation. Ann. Genet., 27, 180-183.
23. Parloir, C., Fryns, J.P. and Van den Berghe H. (1979) Partial trisomy of the short arm of chromosome 3 (3p25 to 3pter). A distinct clinical entity. Hum. Genet., 47, 239-244.
24. Fryns, J.P., Kleczkowska, A., Casaer, P. and Van den Berghe, H. (1986) Double autosomal chromosomal aberration (3p trisomy/9p monosomy) and sex-reversal. Ann. Genet., 29, 49-52.
25. Smeets, E., Vandenbossche, L. and Fryns, J.P. (2001) Partial distal trisomy 3p. A partial autosomal trisomy without major dysmorphic features. Genet. Couns., 12, 85-89.
26. Neri, G., Reynolds, J.F., Westphal, J., Hinz, J. and Daniel, A. (1984) Interstitial deletion of chromosome 3p: report of a patient and delineation of a proximal 3p deletion syndrome. Am. J. Med. Genet., 19, 189-193.
27. Naritomi, K., Hirayama, K., Sameshima, K. and Ohdo, S. (1988) Proximal 3p deletion: case report and review of the literature. Acta Paediatr. Jpn., 30, 78-83.
28. Kenwrick, S., Watkins, A. and De Angelis, E. (2000) Neural cell recognition molecule L1: relating biological complexity to human disease mutations. Hum. Mol. Genet., 9, 879-886.
29. Walsh, F.S. and Doherty, P. (1997) Neural cell adhesion molecules of the immunoglobulin superfamily: role in axon growth and guidance. A. Rev. Cell Dev. Biol., 13, 425-456.
30. Haspel, J., Friedlander, D.R., Ivgy-May, N., Chickramane, S., Roonprapunt, C., Chen, S., Schachner, M. and Grumet, M. (2000) Critical and optimal Ig domains for promotion of neurite outgrowth by L1/Ng-CAM. J. Neurobiol., 42, 287-302.
31. Tessier-Lavigne, M. and Goodman, C.S. (1996) The molecular biology of axon guidance. Science, 274, 1123-1133.
32. Kadmon, G. and Altevogt, P. (1997) The cell adhesion molecule L1: species- and cell-type-dependent multiple binding mechanisms. Differentiation, 61, 143-150.
33. Brummendorf, T., Kenwrick, S. and Rathjen, F.G. (1998) Neural cell recognition molecule L1: from cell biology to human hereditary brain malformations. Curr. Opin. Neurobiol., 8, 87-97.
34. Crossin, K.L. and Krushel, L.A. (2000) Cellular signaling by neural cell adhesion molecules of the immunoglobulin superfamily. Dev. Dyn., 218, 260-279.
35. Rosenthal, A., Jouet, M. and Kenwrick, S. (1992) Aberrant splicing of neural cell adhesion molecule L1 mRNA in a family with X-linked hydrocephalus. Nat. Genet., 2, 107-112.
36. Jouet, M., Rosenthal, A., MacFarlane, J., Kenwrick, S. and Donnai, D. (1993) A missense mutation confirms the L1 defect in X-linked hydrocephalus (HSAS). Nat. Genet., 4, 331.
37. Jouet, M., Rosenthal, A., Armstrong, G., MacFarlane, J., Stevenson, R., Paterson, J., Metzenberg, A., Ionasescu, V., Temple, K. and Kenwrick, S. (1994) X-linked spastic paraplegia (SPG1), MASA syndrome and X-linked hydrocephalus result from mutations in the L1 gene. Nat. Genet., 7, 402-407.
38. Vits, L., Van Camp, G., Coucke, P., Fransen, E., De Boulle, K., Reyniers, E., Korn, B., Poustka, A., Wilson, G., Schrander-Stumpel, C. et al. (1994) MASA syndrome is due to mutations in the neural cell adhesion gene L1CAM. Nat. Genet., 7, 408-413.
39. Fransen, E., Van Camp, G., Vits, L. and Willems, P.J. (1997) L1-associated diseases: clinical geneticists divide, molecular geneticists unite. Hum. Mol. Genet., 6, 1625-1632.
40. De Angelis, E., Watkins, A., Schafer, M., Brummendorf, T. and Kenwrick, S. (2002) Disease-associated mutations in L1 CAM interfere with ligand interactions and cell-surface expression. Hum. Mol. Genet., 11, 1-12.
41. Dobson, C.B., Villagra, F., Clowry, G.J., Smith, M., Kenwrick, S., Donnai, D., Miller, S. and Eyre, J.A. (2001) Abnormal corticospinal function but normal axonal guidance in human L1CAM mutations. Brain, 124, 2393-2406.
42. Kaepernick, L., Legius, E., Higgins, J. and Kapur, S. (1994) Clinical aspects of the MASA syndrome in a large family, including expressing females. Clin. Genet., 45, 181-185.
43. Edelman, G.M. and Jones, F.S. (1998) Gene regulation of cell adhesion: a key step in neural morphogenesis. Brain Res. Brain Res. Rev., 26, 337-352.
44. Thelen, K., Kedar, V., Panicker, A.K., Schmid, R.S., Midkiff, B.R. and Maness, P.F. (2002) The neural cell adhesion molecule L1 potentiates integrin-dependent cell migration to extracellular matrix proteins. J. Neurosci., 22, 4918-4931.
45. Fransen, E., D'Hooge, R., Van Camp, G., Verhoye, M., Sijbers, J., Reyniers, E., Soriano, P., Kamiguchi, H., Willemsen, R., Koekkoek, S.K. et al. (1998) L1 knockout mice show dilated ventricles, vermis hypoplasia and impaired exploration patterns. Hum. Mol. Genet., 7, 999-1009.
46. Fransen, E., Van Camp, G., D'Hooge, R., Vits, L. and Willems, P.J. (1998) Genotype-phenotype correlation in L1 associated diseases. J. Med. Genet., 35, 399-404.
47. Kleinjan, D.J. and van Heyningen, V. (1998) Position effect in human genetic disease. Hum. Mol. Genet., 7, 1611-1618.
48. Crisponi, L., Deiana, M., Loi, A., Chiappe, F., Uda, M., Amati, P., Bisceglia, L., Zelante, L., Nagaraja, R., Porcu, S. et al. (2001) The putative forkhead transcription factor FOXL2 is mutated in blepharophimosis/ptosis/epicanthus inversus syndrome. Nat. Genet., 27, 159-166.
49. Lettice, L.A., Horikoshi, T., Heaney, S.J., van Baren, M.J., van der Linde, H.C., Breedveld, G.J., Joosse, M., Akarsu, N., Oostra, B.A., Endo, N. et al. (2002) Disruption of a long-range cis-acting regulator for Shh causes preaxial polydactyly. Proc. Natl Acad. Sci. USA, 99, 7548-7553.
50. Dong, L., Chen, S., Richter, M. and Schachner, M. (2002) Single-chain variable fragment antibodies against the neural adhesion molecule CHL1 (close homolog of L1) enhance neurite outgrowth. J. Neurosci. Res., 69, 437-447.
51. Chen, S., Mantei, N., Dong, L. and Schachner, M. (1999) Prevention of neuronal cell death by neural adhesion molecules L1 and CHL1. J. Neurobiol., 38, 428-439.
52. Chaisuksunt, V., Campbell, G., Zhang, Y., Schachner, M., Lieberman, A.R. and Anderson, P.N. (2000) The cell recognition molecule CHL1 is strongly upregulated by injured and regenerating thalamic neurons. J. Comp. Neurol., 425, 382-392.
53. Zhang, Y., Roslan, R., Lang, D., Schachner, M., Lieberman, A.R. and Anderson, P.N. (2000) Expression of CHL1 and L1 by neurons and glia following sciatic nerve and dorsal root injury. Mol. Cell Neurosci., 16, 71-86.
54. Cremer, H., Chazal, G., Carleton, A., Goridis, C., Vincent, J.D. and Lledo, P.M. (1998) Long-term but not short-term plasticity at mossy fiber synapses is impaired in neural cell adhesion molecule-deficient mice. Proc. Natl Acad. Sci. USA, 95, 13242-13247.
55. Stork, O., Welzl, H., Wolfer, D., Schuster, T., Mantei, N., Stork, S., Hoyer, D., Lipp, H., Obata, K. and Schachner, M. (2000) Recovery of emotional behaviour in neural cell adhesion molecule (NCAM) null mutant mice through transgenic expression of NCAM180. Eur. J. Neurosci., 12, 3291-3306.
56. D'Adamo, P., Welzl, H., Papadimitriou, S., Raffaele, D.B., Tiveron, C., Tatangelo, L., Pozzi, L., Chapman, P.F., Knevett, S.G., Ramsay, M.F. et al. (2002) Deletion of the mental retardation gene Gdi1 impairs associative memory and alters social behavior in mice. Hum. Mol. Genet., 11, 2567-2580.
57. D'Hooge, R., Nagels, G., Franck, F., Bakker, C.E., Reyniers, E., Storm, K., Kooy, R.F., Oostra, B.A., Willems, P.J. and De Deyn, P.P. (1997) Mildly impaired water maze performance in male Fmr1 knockout mice. Neuroscience, 76, 367-376.
58. Stork, O., Welzl, H., Cremer, H. and Schachner, M. (1997) Increased intermale aggression and neuroendocrine response in mice deficient for the neural cell adhesion molecule (NCAM). Eur. J. Neurosci., 9, 1117-1125.
59. Wolfer, D.P. and Lipp, H.P. (2000) Dissecting the behaviour of transgenic mice: is it the mutation, the genetic background, or the environment? Exp. Physiol., 85, 627-634.
60. D'Hooge, R. and De Deyn, P.P. (2001) Applications of the Morris water maze in the study of learning and memory. Brain Res. Brain Res. Rev., 36, 60-90.
61. Ivanco, T.L. and Greenough, W.T. (2002) Altered mossy fiber distributions in adult Fmr1 (FVB) knockout mice. Hippocampus, 12, 47-54.
62. Mineur, Y.S., Sluyter, F., de Wit, S., Oostra, B.A. and Crusio, W.E. (2002) Behavioral and neuroanatomical characterization of the Fmr1 knockout mouse. Hippocampus, 12, 39-46.
63. Dahme, M., Bartsch, U., Martini, R., Anliker, B., Schachner, M. and Mantei, N. (1997) Disruption of the mouse L1 gene leads to malformations of the nervous system. Nat. Genet., 17, 346-349.
64. Demyanenko, G.P., Tsai, A.Y. and Maness, P.F. (1999) Abnormalities in neuronal process extension, hippocampal development, and the ventricular system of L1 knockout mice. J. Neurosci., 19, 4907-4920.
65. Endris, V., Wogatzky, B., Leimer, U., Bartsch, D., Zatyka, M., Latif, F., Maher, E.R., Tariverdian, G., Kirsch, S., Karch, D. and Rappold, G.A. (2002) The novel Rho-GTPase activating gene MEGAP/srGAP3 has a putative role in severe mental retardation. Proc. Natl Acad. Sci. USA, 99, 11754-11759.
66. Sakurai, K., Migita, O., Toru, M. and Arinami, T. (2002) An association between a missense polymorphism in the close homologue of L1 (CHL1, CALL) gene and schizophrenia. Mol. Psychiat., 7, 412-415.
67. Kermouni, A., Van Roost, E., Arden, K.C., Vermeesch, J.R., Weiss, S., Godelaine, D., Flint, J., Lurquin, C., Szikora, J.P. and Higgs, D.R. (1995) The IL-9 receptor gene (IL9R): genomic structure, chromosomal localization in the pseudoautosomal region of the long arm of the sex chromosomes, and identification of IL9R pseudogenes at 9qter, 10pter, 16pter, and 18pter. Genomics, 29, 371-382.
68. van der Meulen, B.F. and Smrkovsky, M. (1986) MOS 2 6/12-8 6/12 McCarthy Ontwikkelingsschalen. Handleiding. Swets & Zeitlinger, Lisse.
69. Bryant, B., Taylor, R. and Rivera, D.P. (1996) Assessment of Adaptive Areas. A Method for Obtaining Scores that Correspond to the American Association on Mental Retardation's Adaptive Areas. Examiner's Manual, PRO-ED Inc., pp. 1-23.
70. Willis, T.G., Jadayel, D.M., Coignet, L.J., Abdul-Rauf M., Treleaven, J.G., Catovsky, D. and Dyer, M.J. (1997) Rapid molecular cloning of rearrangements of the IGHJ locus using long-distance inverse polymerase chain reaction. Blood, 90, 2456-2464.
71. Cools, J., Bilhou-Nabera, C., Wlodarska, I., Cabrol, C., Talmant, P., Bernard, P., Hagemeijer, A. and Marynen, P. (1999) Fusion of a novel gene, BTL, to ETV6 in acute myeloid leukemias with a t(4;12)(q11-q12;p13). Blood, 94, 1820-1824.
72. Giulietti, A., Overbergh, L., Valckx, D., Decallonne, B., Bouillon, R. and Mathieu, C. (2001) An overview of real-time quantitative PCR: applications to quantify cytokine gene expression. Methods, 25, 386-401.
73. Herreman, A., Hartmann, D., Annaert, W., Saftig, P., Craessaerts, K., Serneels, L., Umans, L., Schrijvers, V., Checler, F., Vanderstichele, H. et al. (1999) Presenilin 2 deficiency causes a mild pulmonary phenotype and no changes in amyloid precursor protein processing but enhances the embryonic lethal phenotype of presenilin 1 deficiency. Proc. Natl Acad. Sci. USA, 96, 11872-11877.
74. Danscher, G. and Zimmer, J. (1978) An improved Timm sulphide silver method for light and electron microscopic localization of heavy metals in biological tissues. Histochemistry, 55, 27-40.
75. Crawley, J.N. and Paylor, R. (1997) A proposed test battery and constellations of specific behavioral paradigms to investigate the behavioral phenotypes of transgenic and knockout mice. Horm. Behav., 31, 197-211.
76. Rogers, D.C., Peters, J., Martin, J.E., Ball, S., Nicholson, S.J., Witherden, A.S., Hafezparast, M., Latcham, J., Robinson, T.L., Quilter, C.A. and Fisher, E.M. (2001) SHIRPA, a protocol for behavioral assessment: validation for longitudinal study of neurological dysfunction in mice. Neurosci. Lett., 306, 89-92.
77. D'Hooge, R., Van Dam, D., Franck, F., Gieselmann, V. and De Deyn, P.P. (2001) Hyperactivity, neuromotor defects, and impaired learning and memory in a mouse model for metachromatic leukodystrophy. Brain Res., 907, 35-43.
78. Van Dam, D., D'Hooge, R., Hauben, E., Reyniers, E., Gantois, I., Bakker, C.E., Oostra, B.A., Kooy, R.F. and De Deyn, P.P. (2000) Spatial learning, contextual fear conditioning and conditioned emotional response in Fmr1 knockout mice. Behav. Brain Res., 117, 127-136.