Perinatal thiamine deficiency-induced spontaneous abortion and pup-killing responses in rat dams

Nutritional Neuroscience

Volumn 16, Issue 2, 2013, Pages 69-77

  Bâ, Abdoulaye ^a  

^a UNIVERSITÉ FÉLIX HOUPHOUËT BOIGNY   (Côte d’Ivoire)

Author keywords

Chronic alcohol intake; Pregnant and lactating rats; Pup killing responses; Spontaneous abortion; Thiamine deficiency

Indexed keywords

ALCOHOL; SUCROSE; THIAMINE; WATER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIRTH; CANNIBALISM; CONTROLLED STUDY; FEMALE; LACTATION; LITTER SIZE; LOW BIRTH WEIGHT; MALE; MATERNAL BEHAVIOR; NONHUMAN; PERINATAL PERIOD; PREGNANCY; PRENATAL PERIOD; PRIORITY JOURNAL; RAT; SPONTANEOUS ABORTION; STARVATION; THIAMINE DEFICIENCY;

ABORTION, SPONTANEOUS; ANIMALS; ANIMALS, NEWBORN; BIRTH WEIGHT; CANNIBALISM; FEMALE; LACTATION; MALNUTRITION; MATERNAL BEHAVIOR; PREGNANCY; RATS; RATS, WISTAR; THIAMINE; THIAMINE DEFICIENCY;

RATTUS; RATTUS NORVEGICUS;

EID: 84873076927     PISSN: 1028415X     EISSN: 14768305     Source Type: Journal    
DOI: 10.1179/1476830512Y.0000000032     Document Type: Article

References (92)

1. Bâ A. Metabolic and structural role of thiamine in nervous tissues. Cell Mol Neurobiol 2008;28:923-931.
2. Vinogradov VV, Vodoyevich VP, Rozhko AV, Vinogradov SV. Concept of the noncoenzymatic thiamine effect. Med Hypotheses 1997;49:487-495.
3. Dhillon RS, Hooda MS, Pundeer JS, Ahlawat KS, Chopra I. Effects of auxins and thiamine on the efficacy of techniques of clonal propagation in Jatropha curcas L. Biomass Bioenergy 2011;35:1502-1510.
4. Kruszewski SP, Jacobs WP. Polarity of thiamine movement through tomato petioles. Plant Physiol 1974;54:301-310.
5. Greewood J, Love ER, Pratt OE. The effects of alcohol or of thiamine deficiency upon reproduction in the female rat and fetal development. Alcohol Alcohol 1983;18:45-51.
6. Subramanian S, Rao J, Adiga PR. Active immunization of rats with chicken egg thiamin carrier protein results in early embryonic loss at periimplantation stages. Indian J Exp Biol 1996;34: 302-306.
7. Bâ A. Alcohol and B1 vitamin deficiency-related stillbirths. J Matern Fetal Neonatal Med 2009;22:452-7.
8. Bennett MR, Schwartz WJ. Altered circadian rhythmicity is an early sign of murine dietary thiamine deficiency. J Neurol Sci 1999;163:6-10.
9. Bâ A. Comparative effects of alcohol and thiamine deficiency on the developing central nervous system. Behav Brain Res 2011; 225:235-242.
10. Molina PE, Fan J, Boxer R, Gelato MC, Lang CH, Abumrad NN. Modulation of insulin-like growth factor-I: a specific role for vitamin B1 (thiamine). J Nutr Biochem 1996;7:207-213.
11. Scalabrino G. Vitamin-regulated cytokines and growth factors in the CNS and elsewhere. J Neurochem 2009;111:1309-1326.
12. Frédérich M, Delvaux D, Gigliobianco T, Gangolf M, Dive G, Mazzucchelli G, et al. Thiaminylated adenine nucleotides. Chemical synthesis, structural characterization and natural occurrence. FEBS J 2009;276:3256-3268.
13. Neher R, Milani A. Pyruvate and thiamine pyrophosphate potentiate cyclic nucleotide-induced steroidogenesis in isolated rat adrenocortical cells. J Steroid Biochem 1983;18:1-6.
14. ′-adenosinemonophosphate and thiamine phosphorylation. Comp Biochem Physiol A Physiol 1981;70:643-647.
15. Faou P, Tropschug M. A novel binding protein for a member of cyp40-type cyclophilins: n. Crassa cypbp37, a growth and thia-mine regulated protein homolog to yeast thi4p. J Mol Biol 2003;333:831-844.
16. ′-adenosinemo-nophosphate and uptake of thiamine in jejunum of chickens (Gallus domesticus) fed on glycine. Comp Biochem Physiol A Physiol 1981;69:305-309.
17. Onodera K. Effects of decarboxylase inhibitors on muricidal suppression by L-dopa in thiamine deficient rats. Arch Int Pharmacodyn Ther 1987;285:263-276.
18. Gaffori O, Le Moal M. Disruption of maternal behavior and appearance of cannibalism after ventral mesencephalic tegmen-tum lesions. Physiol Behav 1979;23:317-323.
19. Abe Y, Tadano T, Yonezawa A, Kisara K. Suppressive effects of intraventricular injected dopamine and nomifensine on muricide induced by thiamine deficiency. Pharmacol Biochem Behav 1987;26:77-81.
20. Keer SE, Stern JM. Dopamine receptor blockade in the nucleus accumbens inhibits maternal retrieval and licking, but enhances nursing behavior in lactating rats. Physiol Behav 1999;67:659-669.
21. Byrnes EM, Rigero BA, Bridges RS. Dopamine antagonists during parturition disrupt maternal care and retention of maternal behavior in rats. Pharmacol Biochem Behav 2002;73: 869-875.
22. Numan M. Hypothalamic neural circuits regulating maternal responsiveness toward infants. Behav Cogn Neurosci Rev 2006; 5:163-190.
23. Stolzenberg DS, Zhang KY, Luskin K, Ranker L, Bress J, Numan M. Dopamine D1 receptor activation of adenylyl cyclase, not phospholipase C, in the nucleus accumbens promotes maternal behavior onset in rats. Horm Behav 2010;57: 96-104.
24. Bâ A, Seri BV, Aka KJ, Glin L, Tako A. Comparative effects of developmental thiamine deficiencies and ethanol exposure on the morphometry of the CA3 pyramidal cells. Neurotoxicol Teratol 1999;21:579-586.
25. Bâ A, N'Douba V, d'Almeida MA, Seri BV. Effects of maternal thiamine deficiencies on the pyramidal and granule cells of the hippocampus of rat pups. Acta Neurobiol Exp 2005;65:387-398.
26. Mulholland PJ, Self RL, Stepanyan TD, Little HJ, Littleton JM, Prendergast MA. Thiamine deficiency in the pathogenesis of chronic ethanol-associated cerebellar damage in vitro. Neuroscience 2005;135:1129-1139.
27. Jaatinen P, Rintala J. Mechanisms of ethanol-induced degeneration in the developing, mature, and aging cerebellum. Cerebellum 2008;7:332-347.
28. Mancinelli R, Ceccanti M. Biomarkers in alcohol misuse: their role in the prevention and detection of thiamine deficiency. Alcohol Alcohol 2009;44:177-182.
29. de Freitas-Silva DM, Resende Lde S, Pereira SR, Franco GC, Ribeiro AM. Maternal thiamine restriction during lactation induces cognitive impairments and changes in glutamate and GABA concentrations in brain of rat offspring. Behav Brain Res 2010;211:33-40.
30. Fattal-Valevski A. Thiamine (vitamin B1). JBCAM 2011;16: 12-20.
31. Bâ A, Seri BV, Han SH. Thiamine administration during chronic alcohol intake in pregnant and lactating rats: effects on the offspring neurobehavioral development. Alcohol Alcohol 1996;31: 27-40.
32. Ciccia RM, Langlais PJ. An examination of the synergistic interaction of ethanol and thiamine deficiency in the development of neurological signs and long-term cognitive and memory impairments. Alcohol Clin Exp Res 2000;24:622-634.
33. Berman RF, Hannigan JH. Effects of prenatal alcohol exposure on the hippocampus: spatial behavior, electrophysiology and neuroanatomy. Hippocampus 2000;10:94-110.
34. Bâ A. Functional vulnerability of developing central nervous system to maternal thiamine deficiencies in the rat. Dev Psychobiol 2005;47:408-414.
35. Donnino MW, Vega J, Miller J, Walsh M. Myths and misconceptions of Wernicke's encephalopathy: what every emergency physician should know. Ann Emerg Med 2007;50:715-721.
36. Wayne WD. Biostatistics: A foundation for analysis in the health sciences. 4th ed. Hoboken, NJ: John Wiley & Sons; 1987.
37. Tadano T, Abe Y, Morikawa Y, Asao T, Hozumi M, Takahashi N, et al. Involvement of dopaminergic neurons in mouse-killing aggression in rats. Methods Find Exp Clin Pharmacol 1997;19: 527-531.
38. Stolzenberg DS, McKenna JB, Keough S, Hancock R, Numan MJ, Numan M. Dopamine D1 receptor stimulation of the nucleus accumbens or the medial preoptic area promotes the onset of maternal behavior in pregnancy-terminated rats. Behav Neurosci 2007;121:907-919.
39. Numan M. Motivational systems and the neural circuitry of maternal behavior in the rat. Dev Psychobiol 2007;49:12-21.
40. Maharjan S, Serova LI, Sabban EL. Membrane-initiated estra-diol signaling increases tyrosine hydroxylase promoter activity with ER alpha in PC12 cells. J Neurochem 2010;112:42-55.
41. Roepke TA, Qiu J, Bosch MA, Rønnekleiv OK, Kelly MJ. Cross-talk between membrane-initiated and nuclear-initiated oestrogen signalling in the hypothalamus. J Neuroendocrinol 2009;21:263-270.
42. Daubner SC, Le T, Wang S. Tyrosine hydroxylase and regulation of dopamine synthesis. Arch Biochem Biophys 2011;508:1-12.
43. Maharjan S, Serova L, Sabban EL. Transcriptional regulation of tyrosine hydroxylase by estrogen: opposite effects with estrogen receptors alpha and beta and interactions with cyclic AMP. J Neurochem 2005;93:1502-1514.
44. Faou P, Tropschug M. Neurospora crassa CyPBP37: a cytosolic stress protein that is able to replace yeast Thi4p function in the synthesis of vitamin B1. J Mol Biol 2004;344:1147-1157.
45. Lazarov Y, Bohorov O, Doncheva A. Effect of L- and D-tyrosine on in vitro transport and phosphorylation of thiamine in rats. Comp Biochem Physiol A Physiol 1980;66:145-147.
46. Nakagawasai O, Yamadera F, Iwasaki K, Asao T, Tan-No K, Niijima F, et al. Preventive effect of kami-untan-to on performance in the forced swimming test in thiamine-deficient mice: relationship to functions of catecholaminergic neurons. Behav Brain Res 2007;177:315-321.
47. Sjöquist B, Johnson HA, Neri A, Lindén S. The influence of thiamine deficiency and ethanol on rat brain catecholamines. Drug Alcohol Depend 1988;22:187-193.
48. Gunagab KP, Menon KMJ. Effect of catecholamines and ovarian hormones on cyclic AMP accumulation in rat hypo-thalamus. Biochem Biophys Res Commun 1973;54:440-448.
49. Muniyappa K, Adiga PR. Oestrogen-induced synthesis of thiamin-binding protein in immature chicks. Kinetics of induction, hormonal specificity and modulation. Biochem J 1980; 186:201-210.
50. Hansen S. Maternal behavior of the female rats with 6-OHDA lesions in the ventral striatum: characterization of the pup retrieval deficit. Physiol Behav 1994;55:615-620.
51. Stern JM, Keer SE. Maternal motivation of lactating rats is disrupted by low dosages of haloperidol. Behav Brain Res 1999;99: 231-239.
52. Silva MR, Bernardi MM, Felicio LF. Effects of dopamine receptor antagonists on ongoing maternal behavior in rats. Pharmacol Biochem Behav 2001;68:461-8.
53. Olazabal D, Abercrombie E, Rosenblatt J, Morrell J. The content of DA, serotonin, and their metabolites in the neural circuit that mediates maternal behavior in juvenile rats. Brain Res Bull 2004;63:259-268.
54. Johns JM, Joyner PW, McMurray MS, Elliott DL, Hofler VE, Middleton CL, et al. The effects of dopaminergic/serotonergic reuptake inhibition on maternal behavior, maternal aggression, and oxytocin in the rat. Pharmacol Biochem Behav 2005;81: 769-785.
55. Numan M, Stolzenberg DS. Medial preoptic area interactions with dopamine neural systems in the control of the onset and maintenance of maternal behavior in rats. Front Neuroendocrinol 2009;30:46-64.
56. Fahrbach SE, Morrell JI, Pfaff DW. Role of oxytocin in onset of estrogen-facilitated maternal behavior. In: Amico J, Robinson AG, (eds.) Oxytocin: clinical and laboratory studies. Amsterdam: Elsevier; 1985. p. 372-388.
57. Pedersen CA, Caldwell JD, Johnson MF, Fort SA, Prange AJ. Oxytocin antiserum delays onset of ovarian-steroid induced maternal behavior. Neuropeptides 1985;6:175-182.
58. Pedersen CA, Caldwell JD, Walker CH, Ayers G, Mason GA. Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas. Behav Neurosci 1994;108:1163-1171.
59. Van Leengoed E, Kerker E, Swanson HH. Inhibition of postpar-tum maternal behavior in the rat by injecting an oxytocin antagonist into the cerebral ventricles. J Endocrinol 1987;112:275-282.
60. Lubin DA, Elliot JC, Black MC, John JM. An oxytocin antagonist infused into the central nucleus of the amygdala increases maternal aggressive behavior. Behav Neurosci 2003;117: 195-201.
61. Bosch OJ, Sartori SB, Singewald N, Neumann ID. Extracellular amino acid levels in the paraventricular nucleus and the central amygdala in high- and low-anxiety dams rats during maternal aggression: regulation by oxytocin. Stress 2007;10:261-270.
62. McMurray MS, Joyner PW, Middleton CW, Jarrett TM, Elliott DL, Black MA, et al. Intergenerational effects of cocaine on maternal aggressive behavior and brain oxytocin in rat dams. Stress 2008;11:398-411.
63. Macbeth AH, Stepp JE, Lee H-J, Young WS, Caldwell HK. Normal maternal behavior, but increased pup mortality, in conditional oxytocin receptor knockout females. Behav Neurosci 2010;124:677-685.
64. Kimble D, Rogers L, Hendrickson C. Hippocampal lesions disrupt maternal, not sexual behavior in the albino rat. J Comp Physiol Psychol 1967;63:401-407.
65. Elliott JC, Lubin DA, Walker CH, Johns JM. Acute cocaine alters oxytocin levels in the medial preoptic area and amygdala in lactating rat dams: implications for cocaine-induced changes in maternal behavior and maternal aggression. Neuropeptides 2001;35:127-134.
66. Russell JA, Brunton PJ. Neuroactive steroids attenuate oxytocin stress responses in late pregnancy. Neuroscience 2006;138: 879-889.
67. Shughrue PJ, Dellovade TL, Merchenthaler I. Estrogen modulates oxytocin gene expression in regions of the rat supraoptic and paraventricular nuclei that contain estrogen receptor-beta. Prog Brain Res 2002;139:15-29.
68. Rosenblatt JS, Ceus K. Estrogen implants in the medial preoptic area stimulate maternal behavior in male rats. Horm Behav 1998; 33:23-30.
69. Paolo TD, Poyet P, Labrie F. Prolactin and estradiol increase striatal dopamine receptor density in intact, castred and hypo-physectomized rats. Prog Neuropsychopharmacol Biol Psychiatry 1982;6:377-382.
70. Nomura M, Andersson S, Korach KS, Gustafsson JA, Pfaff DW, Ogawa S. Estrogen receptor-beta gene disruption potentiates estrogen-inducible aggression but not sexual behaviour in male mice. Eur J Neurosci 2006;23:1860-1868.
71. Trainor BC, Finyb MS, Nelsonb RJ. Rapid effects of estradiol on male aggression depend on photoperiod in reproductively non-responsive mice. Horm Behav 2008;53:192-199.
72. Trainor BC, Greiwe KM, Nelson RJ. Individual differences in estrogen receptor α in select brain nuclei are associated with individual differences in aggression. Horm Behav 2006;50:338-345.
73. Garris DR, Billiar RB, Takaoka Y, White R, Little B. Autoradiographic localization of estradiol- and progesterone-concentrating neurons in the isolated rhesus monkey hypothala-mus. Neurosci Lett 1983;37:149-154.
74. Mayer AD, Ahdieh HB, Rosenblatt JS. Effects of prolonged estrogen-progesterone treatment and hypophysectomy on the stimulation of short-latency maternal behavior and aggression in female rats. Horm Behav 1990;24:152-173.
75. Klier CM, Muzik M, Dervic K, Mossaheb N, Benesch T, Ulm B, et al. The role of estrogen and progesterone in depression after birth. J Psychiatr Res 2007;41:273-279.
76. Burd L, Roberts D, Olson M, Hein Odendaal H. Ethanol and the placenta: a review. J Matern Fetal Neonatal Med 2007;20:361-375.
77. Han VK, Bassett N, Walton J, Challis JR. The expression of insulin-like growth factor (IGF) and IGF-binding protein (IGFBP) genes in the human placenta and membranes: evidence for IGF-IGFBP interactions at the feto-maternal interface. J Clin Endocrinol Metab 1996;81:2680-2693.
78. Setia S, Sridhar MG. Changes in GH/IGF-1 axis in intrauterine growth retardation: consequences of fetal programming? Horm Metab Res 2009;41:791-798.
79. Han VK. The ontogeny of growth hormone, insulin-like growth factors and sex steroids: molecular aspects. Horm Res 1996;45: 61-66.
80. Fowden AL. The insulin-like growth factors and fetoplacental growth. Placenta 2003;24:803-812.
81. Carter AM, Kingston MJ, Han KK, Mazzuca DM, Nygard K, Han VK. Altered expression of IGFs and IGF-binding proteins during intrauterine growth restriction in guinea pigs. J Endocrinol 2005;184:179-189.
82. de Vrijer B, Davidsen ML, Wilkening RB, Anthony RV, Regnault TR. Altered placental and fetal expression of IGFs and IGF-binding proteins associated with intrauterine growth restriction in fetal sheep during early and mid-pregnancy. Pediatr Res 2006;60:507-512.
83. Akram SK, Sahlin L, Ostlund E, Hagenäs L, Fried G, SÃ der O. Placental IGF-I, estrogen receptor, and progesterone receptor expression, and maternal anthropometry in growth-restricted pregnancies in the Swedish population. Horm Res Paediatr 2011;75:131-137.
84. Hickman TN, Shih LM, Zacur HA, Kurman RJ, Diener-West M, Gearhart JD. Decreased progesterone receptor expression in the intermediate trophoblastic cells of spontaneous abortions. Fertil Steril 2002;77:1001-1005.
85. Papamitsou T, Chatzistamatiou M, Grammatikopoulou D, Papadopoulou K, Lakis S, Economou Z, et al. Low expression of progesterone receptor A in intermediate trophoblast of miscarriages. Histol Histopathol 2011;26:609-614.
86. Boos A, Kohtes J, Janssen V, Mülling C, Stelljes A, Zerbe H, et al. Pregnancy effects on distribution of progesterone receptors, oestrogen receptor α, glucocorticoid receptors, Ki-67 antigen and apoptosis in the bovine interplacentomal uterine wall and foetal membranes. Anim Reprod Sci 2006;91:55-76.
87. Thijssen JHH. Progesterone receptors in the human uterus and their possible role in parturition. J Steroid Biochem Mol Biol 2005;97:397-400.
88. Zollers WG Jr, Babischkin JS, Pepe GJ, Albrecht ED. Developmental regulation of placental insulin-like growth factor (IGF)-II and IGF-binding protein-1 and -2 messenger RNA expression during primate pregnancy. Biol Reprod 2001; 65:1208-1214.
89. Gerhardt A, Scharf RE, Mikat-Drozdzynski B, Krüssel JS, Bender HG, Zotz RB. Maternal IVS1-401 T allele of the estrogen receptor alpha is an independent predictor of late fetal loss. Fertil Steril 2006;86:448-453.
90. Pineda B, Hermenegildo C, Tarín JJ, Laporta P, Cano A, García-Pérez MA. Alleles and haplotypes of the estrogen receptor alpha gene are associated with an increased risk of spontaneous. Fertil Steril 2010;93:1809-1815.
91. Kanca H, Walter I, Schäfer-Somi S, Budik S, Ay SS, Kucukaslan I, et al. Induction of abortion with aglepristone significantly changed the expression of progesterone and estrogen receptors in canine endometrial stromal cells. Theriogenology 2008;70: 1439-1448.
92. de la Monte SM, Tong M, Cohen AC, Sheedy D, Harper C, Wands JR. Insulin and insulin-like growth factor resistance in alcoholic neurodegeneration. Alcohol Clin Exp Res 2008;32: 1630-1644.