Behavioral abnormalities of fetal growth retardation model rats with reduced amounts of brain proteoglycans

Experimental Neurology

Volumn 219, Issue 1, 2009, Pages 81-92

  Saito, Akiko ^a,b   Matsui, Fumiko ^c   Hayashi, Kanako ^b   Watanabe, Kimi ^b   Ichinohashi, Yuko ^d   Sato, Yoshiaki ^a,e   Hayakawa, Masahiro ^f   Kojima, Seiji ^a   Oohira, Atsuhiko ^b  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b AICHI MEDICAL UNIVERSITY   (Japan)

^c INSTITUTE FOR DEVELOPMENTAL RESEARCH   (Japan)

^d AICHI MEDICAL UNIVERSITY HOSPITAL   (Japan)

^e UNIVERSITY OF GOTHENBURG   (Sweden)

^f NAGOYA UNIVERSITY HOSPITAL   (Japan)

Author keywords

Brain development; Chondroitin sulfate proteoglycan; Fetal growth retardation; Learning disability; Thromboxane A2

Indexed keywords

NEUROCAN; NEUROGLYCAN C; PHOSPHACAN; PROTEOCHONDROITIN SULFATE; THROMBOXANE A2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; BRAIN LEVEL; CELL DENSITY; CONTROLLED STUDY; FEMALE; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; INTRAUTERINE GROWTH RETARDATION; LEARNING DISORDER; MALE; NICK END LABELING; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; BRAIN; CELL COUNT; CEREBRAL CORTEX; DEVELOPMENTAL DISABILITIES; DISEASE MODELS, ANIMAL; FEMALE; FETAL GROWTH RETARDATION; GROWTH INHIBITORS; HUMANS; INFANT, NEWBORN; LEARNING DISORDERS; MALE; MEMBRANE PROTEINS; PREGNANCY; PROTEOCHONDROITIN SULFATES; PROTEOGLYCANS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 5; THROMBOXANE A2;

EID: 68549122642     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2009.04.012     Document Type: Article

References (64)

1. Alexander B.T. Placental insufficiency leads to development of hypertension in growth-restricted offspring. Hypertension 41 (2003) 457-462
2. Aucott S.W., Donohue P.K., and Northington F.J. Increased morbidity in severe early intrauterine growth restriction. J. Perinatal. 24 (2004) 435-440
3. Bandtlow C.E., and Zimmermann D.R. Proteoglycans in the developing brain: new conceptual insights for old proteins. Physiol. Rev. 80 (2000) 1267-1290
4. Bassan H., Bassan M., Pinhasov A., Kariv N., Giladi E., Gozes I., and Harel S. The pregnant spontaneously hypertensive rat as a model of asymmetric intrauterine growth retardation and neurodevelopmental delay. Hypetens. Pregnancy 24 (2005) 201-211
5. Bergvall N., Liadou A., Johansson S., Tuvemo T., and Cnattingius S. Risks for low intellectual performance related to being born small for gestational age are modified by gestational age. Pediatrics 117 (2006) 460-467
6. Dieni S., and Rees S. Dendric morphology is altered in hippocampal neurons following prenatal compromise. J. Nerubiol. 55 (2003) 41-52
7. Dzwonek K. NG2 expressing cells in hippocampal cultures survive neurotoxic insult and retain the ability to divide. Acta Neurobiol. Exp. 65 (2005) 173-176
8. Feldman R., and Eidelman A.I. Neonatal state organization, neuromaturation, mother-infant interaction, and cognitive development in small-for-gestational age premature infants. Pediatrics 118 (2006) 869-878
9. Fukami E., Nakayama A., Sasaki J., Mimura S., Mori N., and Watanabe K. Underexpression of neural cell adhesion molecule and neurotrophic factors in rat brain following thromboxane A(2)-induced intrauterine growth retardation. Early Hum. Dev. 58 (2000) 101-110
10. Galtrey C.M., and Fawcett J.W. The role of chondroitin sulfate proteoglycans in regeneration and plasticity in the central nervous system. Brain Res. Rev. 54 (2007) 1-18
11. Geva R., Eshel R., Leitne Y., Fattal-Valevski A., and Harel S. Memory functions of children born with asymmetric intrauterine growth restriction. Brain Res. 30 (2006) 186-194
12. Hartmann U., and Maurer P. Proteoglycans in the nervous system-the quest for functional roles in vivo. Matrix Biol. 20 (2001) 23-35
13. Hayakawa M., Mimura S., Sasaki J., and Watanabe K. Neuropathological changes in the cerebrum of IUGR rat induced by synthetic thromboxane A2. Early Hum. Dev. 5 (1999) 125-136
14. Hayakawa M., Takemoto K., Nakayama A., Saito A., Sato Y., Hasegawa M., Ieda K., and Mimura S. An animal model of intrauterine growth retardation induced by synthetic thromboxane A2. J. Soc. Gynecol. Investig. 13 (2006) 566-572
15. Hayashi N., Oohira A., and Miyata S. Synaptic localization of receptor-type protein tyrosine phosphatase ζ/β in the cerebral and hippocampal neurons of adult rats. Brain Res. 1050 (2005) 163-169
16. Huang P., Gou W.L., Jiang M.L., Zhang R., and Sun Y.P. Impact of fetal growth restriction on spatial learning and memory abilities of the offspring of rats. Sichuan Da Xue Xue Bao Yi Ban. 39 (2008) 627-630
17. Ida M., Shuo T., Hirano K., Tokita Y., Nakanishi K., Matsui F., Aono S., Fujita H., Fujiwara Y., Kaji T., and Oohira A. Identification and functions of chondroitin sulfate in the milieu of neural stem cell. J. Biol. Chem. 281 (2006) 5982-5991
18. Ishii M., and Maeda N. Oversulfated chondroitin sulfate plays critical roles in the neuronal migration in the cerebral cortex. J. Biol. Chem. 283 (2008) 32610-32620
19. Jüttner R., Moré M.I., Das D., Babich A., Meier J., Henning M., Erdmann B., Mu Ller E.C., Otto A., Grantyn R., and Rathjen F.G. Impaired synapse function during postnatal development in the absence of CALEB, an EGF-like protein processed by neuronal activity. Neuron 46 (2005) 233-245
20. Kawano H., and Kawamura K. Molecular mechanisms of the pathway formation in the fetal rat cerebral neocortex. Nihon Shinkei Seisin Yakurigaku Zassi. 19 (1999) 79-84
21. Kihara T., Surjono T.W., Sakamoto M., Matsuo T., Yasuda Y., and Tanimura T. Effects of prenatal rubratoxin-B exposure on behaviors of mouse offspring. Toxicol. Sci. 61 (2001) 368-373
22. Lodygensky G.A., Seghier M.L., Warfield S.K., Tolsa C.B., Sizonenko S., Lazeyras F., and Huppi P.S. Intrauterine growth restriction affects the preterm infant's hippocampus. Pediatr. Res. 63 (2008) 438-443
23. Maeda N., and Noda M. Involvement of receptor-like protein tyrosine phosphatase ζ/RPTPβ and its ligand pleiotrophin/heparin-binding growth-associated molecule (HB-GAM) in neuronal migration. J. Cell Biol. 142 (1998) 203-216
24. Maeda N., Hamanaka H., Oohira A., and Noda M. Purification, characterization and developmental expression of a brain-specific chondroitin sulfate proteoglycan, 6B4 proteoglycan/phosphacan. Neuroscience 67 (1995) 23-35
25. Mallard C., Loeliger M., Copolov D., and Rees S. Reduced number of neurons in the hippocampus and the cerebellum in the postnatal guinea-pig following intrauterine growth restriction. Neuroscience 100 (2000) 327-333
26. Markestad T., Vik T., Ahlsten G., Gebre-Medhin M., Skjaerven R., Jacobsen G., Hoffman H.J., and Bakketeig L.S. Small-for-gestational-age (SGA) infants born at term: growth and development during the first year of life. Acta Obstet Gynecol. Scand., Suppl. 165 (1997) 93-101
27. Martikainen M.A., Airaksinen E.M., Heinonen K.M., and Castren M.L. The neurological condition of the newborn infant with maternal hypertension, examined at term. Early Hum. Dev. 16 (1988) 107-118
28. Martinez A., and Simmons R. Abnormalities of fetal growth. In: William H.T., Roberta A.B., Christine A.G., and Mary E.A. (Eds). Avery's Diseases of the Newborn. 8th ed. (2004), WB Saunders, Philadelphia 32-45
29. Matsui F., Watanabe E., and Oohira A. Immunological identification of two proteoglycan fragments derived from neurocan, a brain-specific chondroitin sulfate proteoglycan. Neurochem. Int. 25 (1994) 425-431
30. Matsui F., Kakizawa H., Nishizuka M., Hirano K., Shuo T., Ida M., Tokita Y., Aono S., Keino H., and Oohira A. Changes in the amounts of chondroitin sulfate proteoglycans in rat brain after neonatal hypoxia-ischemia. J. Neurosci. Res. 81 (2005) 837-845
31. Mesquita A.R., Pego J.M., Summavielle T., Maciel P., Almeida O.F., and Sousa N. Neurodevelopment milestone abnormalities in rats exposed to stress in early life. Neuroscience 147 (2007) 1022-1033
32. Morgenstern D.A., Asher R.A., and Fawcett J.W. Chondroitin sulphate proteoglycans in the CNS injury response. Prog. Brain Res. 137 (2002) 313-332
33. Neitzke U., Harder T., Schellong K., Melchior K., Ziska T., Rodekamp E., Dudenhausen J.W., and Plagemann A. Intrauterine growth restriction in a rodent model and developmental programming of the metabolic syndrome: a critical appraisal of the experimental evidence. Placenta 29 (2008) 246-254
34. Ohyama K., Kawano H., Asou H., Fukuda T., Oohira A., Uyemura K., and Kawamura K. Coordinate expression of L1 and 6B4 proteoglycan/phosphacan is correlated with the migration of mesencephalic dopaminergic neurons in mice. Brain Res. Dev. Brain Res. 107 (1998) 219-226
35. Oohira A. Multiple species and functions of proteoglycans in the central nervous system. In: Kamerling J.P. (Ed). Comprehensive Glycoscience; From Chemistry to Systems Biology. Vol. 4 (Cell Glycobiology and Development) (2007), Elsevier, Oxford 297-322
36. Oohira A., Matsui F., Watanabe E., Kushima Y., and Maeda N. Developmentally regulated expression of a brain specific species of chondroitin sulfate proteoglycan, neurocan, identified with a monoclonal antibody IG2 in the rat cerebrum. Neuroscience 60 (1994) 145-157
37. Oohira A., Matsui F., Tokita Y., Yamauchi S., and Aono S. Molecular interactions of neural chondroitin sulfate proteoglycans in the brain development. Arch. Biochem. Biophys. 374 (2000) 24-34
38. Paxinos G., Tork I., Tecott L.H., and Valentino K.L. Atlas of the Developing Rat Brain (1991), Academic Press, Inc., San Diego Fig. 96.
39. Peng Y., Huang B., Biro F., Feng L., Guo Z., and Slap G. Outcome of low birthweight in China: a 16-year longitudinal study. Acta Paediatr. 94 (2005) 843-849
40. Robert H.L., Rolando J.R., Anna E.T., Jennifer L.K., Margaret K.M., Elisa M.G., and Sherin U.D. Uteroplacental insufficiency lowers the threshold toward hypoxia-induced cerebral apoptosis in growth-retarded fetal rats. Brain Res. 895 (2001) 186-193
41. Robinson J., Moore M., Owens J.A., and McMillen C. Origins of fetal growth restriction. Eur. J. Obstet. Gynecol. Reprod. Biol. 92 (2000) 113-119
42. Rosso P. Maternal-fetal exchange during protein malnutrition in the rat. Placental transfer of alpha-amino isobutyric acid. J. Nutr. 107 (1977) 2002-2005
43. Sakaguchi N., Muramatsu H., Ichihara-Tanaka K., Maeda N., Noda M., Yamamoto T., Michikawa M., Ikematsu S., Sakuma S., and Muramatsu T. Receptor-type protein tyrosine phosphatase ζ as a component of the signaling receptor complex for midkine-dependent survival of embryonic neurons. Neurosci. Res. 45 (2003) 219-224
44. Sasaki J., Fukami E., Mimura S., Hayakawa M., Kitoh J., and Watanabe K. Abnormal cerebral neuronal migration in a rat model of intrauterine growth retardation induced by synthetic thromboxane A2. Early Hum. Dev. 58 (2000) 91-99
45. Sato Y., Nakanishi K., Tokita Y., Kakizawa H., Ida M., Maeda H., Matsui F., Aono S., Saito A., Kuroda Y., Hayakawa M., Kojima S., and Oohira A. A highly sulfated chondroitin sulfate preparation, CS-E, prevents excitatory amino acid-induced neuronal cell death. J. Neurochem. 104 (2008) 1565-1576
46. Sheng W., Wang G., Wang Y., Liang J., Wen J., Zheng P.S., Wu Y., Lee V., Slingerland J., Dumont D., and Yang B.B. The roles of versican V1 and V2 isoforms in cell proliferation and apoptosis. Mol. Biol. Cell. 16 (2005) 1330-1340
47. Simmons R. Developmental origins of adult metabolic disease: concepts and controversies. Trends Endocrinol. Metab. 16 (2005) 390-394
48. Simmons R.A., Templeton L.J., and Gertz S.J. Intrauterine growth retardation leads to the development of type 2 diabetes in the rat. Diabetes 50 (2001) 2279-2286
49. Sirko S., von Holst A., Wizenmann A., Götz M., and Faissner A. Chondroitin sulfate glycosaminoglycans control proliferation, radial glia cell differentiation and neurogenesis in neural stem/progenitor cells. Development 134 (2007) 2727-2738
50. 1A receptor response in NCAM null mutant mice. J. Neurobiol. 40 (1999) 343-355
51. Streissguth A.P., Landesman-Dwyer S., Martin J.C., and Smith D.W. Teratogenic effects of alcohol in humans and laboratory animals. Science 209 (1980) 353-361
52. Takahashi T., Goto T., Miyama S., Nowakowski R.S., and Caviness Jr. V.S. Sequence of neuron origin and neocortical laminar fate: relation to cell cycle of origin in the developing murine cerebral wall. J. Neurosci. 19 (1999) 10357-10371
53. Tolsa C.B., Zimine S., Warfield S.K., Fredchi M., Sancho R.A., Lazeyras F., Hanquinet S., Pfizenmaier M., and Huppi P.S. Early alteration of structural and functional brain development in premature infants born with intrauterine growth restriction. Pediatr. Res. 56 (2004) 132-138
54. Van Geijn H.P., Kaylor Jr. W.M., Nicola K.R., and Zuspan F.P. Induction of severe intrauterine growth retardation in the Sprague-Dawley rat. Am. J. Obstet. Gynecol. 137 (1980) 43-47
55. Vik T., Markestad T., Ahlsten G., Gebre-Medhin M., Jacobsen G., Hoffman H.J., and Bakketeig L.S. Body proportions and early neonatal morbidity in small-for-gestational-age infants of successive births. Acta Obstet. Gynecol. Scand., Suppl. 165 (1997) 76-81
56. Walker D.M., and Marlow N. Neurocognitive outcome following fetal growth restriction. Arch. Dis. Child Fetal Neonatal Ed. 93 (2008) 322-325
57. Walsh R.N., and Cummins R.A. The open-field test: a critical review. Psychol. Bull. 83 (1976) 482-504
58. Wigglesworth J.S. Experimental growth retardation in the foetal rat. J. Pathol. Bacteriol. 88 (1964) 1-13
59. Xiao R., Sorensen T.K., Williams M.A., and Luthy D.A. Influence of pre-eclampsia on fetal growth. J. Matern. Fetal Neonatal Med. 13 (2003) 157-162
60. Xuelan L., Gou W.L., Huang P., Chunfanga L., and Sun Y.P. Effect of behavior training on learning and memory of young rats with fetal growth restriction. J. Med. Coll. PLA 23 (2008) 283-288
61. Yanagisawa M., and Yu R.K. The expression and functions of glycoconjugates in neural stem cells. Glycobiology 17 (2007) 57R-74R
62. Yasuda Y., Tokita Y., Aono S., Matsui F., Ono T., Sonta S., Watanabe E., Nakanishi Y., and Oohira A. Cloning and chromosomal mapping of the human gene of neuroglycan C (NGC), a neural transmembrane chondroitin sulfate proteoglycan with an EGF module. Neurosci. Res. 32 (1998) 313-322
63. Zhou X.H., Brakebusch C., Matthies H., Oohashi T., Hirsch E., Moser M., Krug M., Seidenbecher C.I., Boeckers T.M., Rauch U., Buettner R., Gundelfinger E.D., and Fässler R. Neurocan is dispensable for brain development. Mol. Cell Biol. 21 (2001) 5970-5978
64. Zuk L., Harel S., Leitner Y., and Fattal-Valevski A. Neonatal general movements: an early predictor for neurodevelopmental outcome in infants with intrauterine growth retardation. J. Child Neurol. 19 (2004) 14-18