Early Development of Parvalbumin-, Somatostatin-, and Cholecystokinin-Expressing Neurons in Rat Brain following Prenatal Immune Activation and Maternal Iron Deficiency

Developmental Neuroscience

Volumn 38, Issue 5, 2017, Pages 342-353

  Boksa, Patricia ^a   Zhang, Ying ^a   Nouel, Dominique ^a   Wong, Alice ^a   Wong, Tak Pan ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Animal model; Interneurons; Lipopolysaccharide; Prenatal infection; Schizophrenia; Aminobutyric acid

Indexed keywords

CHOLECYSTOKININ; DOPAMINE; ENDOCANNABINOID; LIPOPOLYSACCHARIDE; PARVALBUMIN; SOMATOSTATIN; 4 AMINOBUTYRIC ACID; IRON;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN BINDING; ARTICLE; CELL SUBPOPULATION; COGNITIVE DEFECT; CONTROLLED STUDY; DENTATE GYRUS; HIPPOCAMPAL CA1 REGION; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTERNEURON; IRON DEFICIENCY; NERVE EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSYCHOSIS; RAT; SCHIZOPHRENIA; VENTRAL SUBICULUM; ANIMAL; BRAIN; DEFICIENCY; FEMALE; METABOLISM; NERVE CELL; PATHOPHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE;

ANIMALS; BRAIN; CHOLECYSTOKININ; DOPAMINE; FEMALE; GAMMA-AMINOBUTYRIC ACID; IRON; NEURONS; PARVALBUMINS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; SOMATOSTATIN;

EID: 85013661836     PISSN: 03785866     EISSN: 14219859     Source Type: Journal    
DOI: 10.1159/000454677     Document Type: Article

References (63)

1. Schmidt MJ, Mirnics K: Neurodevelopment, GABA system dysfunction, and schizophrenia. Neuropsychopharmacology 2015; 40: 190-206.
2. Volk DW, Lewis DA: Early developmental disturbances of cortical inhibitory neurons: contribution to cognitive deficits in schizophrenia. Schizophr Bull 2014; 40: 952-957.
3. Brisch R, Bielau H, Saniotis A, Wolf R, Bogerts B, Krell D, Steiner J, Braun K, Krzyżanowska M, Krzyżanowski M, Jankowski Z, Kaliszan M, Bernstein HG, Gos T: Calretinin and parvalbumin in schizophrenia and affective disorders: a mini-review, a perspective on the evolutionary role of calretinin in schizophrenia, and a preliminary postmortem study of calretinin in the septal nuclei. Front Cell Neurosci 2015; 9: 393.
4. Hashimoto T, Volk DW, Eggan SM, Mirnics K, Pierri JN, Sun Z, Sampson AR, Lewis DA: Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia. J Neurosci 2003; 23: 6315-6326.
5. Fung SJ, Fillman SG, Webster MJ, Shannon Weickert C: Schizophrenia and bipolar disorder show both common and distinct changes in cortical interneuron markers. Schizophr Res 2014; 155: 26-30.
6. Joshi D, Fung SJ, Rothwell A, Weickert CS: Higher gamma-aminobutyric acid neuron density in the white matter of orbital frontal cortex in schizophrenia. Biol Psychiatry 2012; 72: 725-733.
7. Volk DW, Edelson JR, Lewis DA: Altered expression of developmental regulators of parvalbumin and somatostatin neurons in the prefrontal cortex in schizophrenia. Schizophr Res 2016; 177: 3-9.
8. Gonzalez-Burgos G, Cho RY, Lewis DA: Alterations in cortical network oscillations and parvalbumin neurons in schizophrenia. Biol Psychiatry 2015; 77: 1031-1040.
9. Lee SY, Foldy C, Szabadics J, Soltesz I: Celltype-specific CCK2 receptor signaling underlies the cholecystokinin-mediated selective excitation of hippocampal parvalbumin-positive fast-spiking basket cells. J Neurosci 2011; 31: 10993-11002.
10. Khandaker GM, Zimbron J, Lewis G, Jones PB: Prenatal maternal infection, neurodevelopment and adult schizophrenia: a systematic review of population-based studies. Psychol Med 2013; 43: 239-257.
11. Sorensen HJ, Nielsen PR, Pedersen CB, Mortensen PB: Association between prepartum maternal iron deficiency and offspring risk of schizophrenia: population-based cohort study with linkage of Danish national registers. Schizophr Bull 2011; 37: 982-987.
12. Insel BJ, Schaefer CA, McKeague IW, Susser ES, Brown AS: Maternal iron deficiency and the risk of schizophrenia in offspring. Arch Gen Psychiatry 2008; 65: 1136-1144.
13. Velu PP, Gravett CA, Roberts TK, Wagner TA, Zhang JS, Rubens CE, Gravett MG, Campbell H, Rudan I: Epidemiology and aetiology of maternal bacterial and viral infections in low-and middle-income countries. J Glob Health 2011; 1: 171-188.
14. Milman N: Anemia-still a major health problem in many parts of the world! Ann Hematol 2011; 90: 369-377.
15. McLean E, Cogswell M, Egli I, Wojdyla D, de Benoist B: Worldwide prevalence of anaemia, WHO Vitamin and Mineral Nutrition Information System, 1993-2005. Public Health Nutr 2009; 12: 444-454.
16. Nouel D, Burt M, Zhang Y, Harvey L, Boksa P: Prenatal exposure to bacterial endotoxin reduces the number of GAD67-and reelinimmunoreactive neurons in the hippocampus of rat offspring. Eur Neuropsychopharmacol 2012; 22: 300-307.
17. Wischhof L, Irrsack E, Osorio C, Koch M: Prenatal LPS-exposure-A neurodevelopmental rat model of schizophrenia-differentially affects cognitive functions, myelination and parvalbumin expression in male and female offspring. Prog Neuropsychopharmacol Biol Psychiatry 2015; 57: 17-30.
18. Baharnoori M, Bhardwaj SK, Srivastava LK: Effect of maternal lipopolysaccharide administration on the development of dopaminergic receptors and transporter in the rat. PLoS One 2013; 8:e54439.
19. Basta-Kaim A, Fijał K, Ślusarczyk J, Trojan E, Głombik K, Budziszewska B, Leśkiewicz M, Regulska M, Kubera M, Lasoń W, Wȩdzony K: Prenatal administration of lipopolysaccharide induces sex-dependent changes in glutamic acid decarboxylase and parvalbumin in the adult rat brain. Neuroscience 2015; 287: 78-92.
20. Callahan LS, Thibert KA, Wobken JD, Georgieff MK: Early-life iron deficiency anemia alters the development and long-term expression of parvalbumin and perineuronal nets in the rat hippocampus. Dev Neurosci 2013; 35: 427-436.
21. Harvey L, Boksa P: Do prenatal immune activation and maternal iron deficiency interact to affect neurodevelopment and early behavior in rat offspring? Brain Behav Immun 2014; 35: 144-154.
22. Harvey L, Boksa P: Additive effects of maternal iron deficiency and prenatal immune activation on adult behaviors in rat offspring. Brain Behav Immun 2014; 40: 27-37.
23. Rao R, de Ungria M, Sullivan D, Wu P, Wobken JD, Nelson CA, Georgieff MK: Perinatal brain iron deficiency increases the vulnerability of rat hippocampus to hypoxic ischemic insult. J Nutr 1999; 129: 199-206.
24. De Deungria M, Rao R, Wobken JD, Luciana M, Nelson CA, Georgieff MK: Perinatal iron deficiency decreases cytochrome c oxidase (CytOx) activity in selected regions of neonatal rat brain. Pediatr Res 2000; 48: 169-176.
25. Unger EL, Hurst AR, Georgieff MK, Schallert T, Rao R, Connor JR, Kaciroti N, Lozoff B, Felt B: Behavior and monoamine deficits in prenatal and perinatal iron deficiency are not corrected by early postnatal moderate-iron or high-iron diets in rats. J Nutr 2012; 142: 2040-2049.
26. Paxinos G, Watson C: The Rat Brain in Stereotaxic Coordinates, ed 7. San Diego, Academic Press, 2013.
27. Meyer-Lindenberg A: From maps to mechanisms through neuroimaging of schizophrenia. Nature 2010; 468: 194-202.
28. Grace AA: Dopamine system dysregulation by the hippocampus: implications for the pathophysiology and treatment of schizophrenia. Neuropharmacology 2012; 62: 1342-1348.
29. Benes FM, Lange N: Two-dimensional versus three-dimensional cell counting: a practical perspective. Trends Neurosci 2001; 24: 11-17.
30. Von Bartheld C: Counting particles in tissue sections: choices of methods and importance of calibration to minimize biases. Histol Histopathol 2002; 17: 639-648.
31. Diaz-Cintra S, Gonzalez-Maciel A, Morales MA, Aguilar A, Cintra L, Prado-Alcala RA: Protein malnutrition differentially alters the number of glutamic acid decarboxylase-67 interneurons in dentate gyrus and CA1-3 subfields of the dorsal hippocampus. Exp Neurol 2007; 208: 47-53.
32. Lema Tome CM, Miller R, Bauer C, Nottingham C, Smith C, Blackstone K, Brown L, Bryan R, Leigh A, Brady M, Busch J, Turner CP: Decline in age-dependent, MK801-induced injury coincides with developmental switch in parvalbumin expression: cingulate and retrosplenial cortex. Dev Psychobiol 2007; 49: 606-618.
33. Osterop SF, Virtanen MA, Loepke JR, Joseph B, Loepke AW, Vutskits L: Developmental stage-dependent impact of midazolam on calbindin, calretinin and parvalbumin expression in the immature rat medial prefrontal cortex during the brain growth spurt. Int J Dev Neurosci 2015; 45: 19-28.
34. Ouellet L, de Villers-Sidani E: Trajectory of the main GABAergic interneuron populations from early development to old age in the rat primary auditory cortex. Front Neuroanat 2014; 8: 40.
35. Lehmann K, Steinecke A, Bolz J: GABA through the ages: regulation of cortical function and plasticity by inhibitory interneurons. Neural Plast 2012; 2012: 892784.
36. Di Cristo G, Chattopadhyaya B, Kuhlman SJ, Fu Y, Belanger MC, Wu CZ, Rutishauser U, Maffei L, Huang ZJ: Activity-dependent PSA expression regulates inhibitory maturation and onset of critical period plasticity. Nat Neurosci 2007; 10: 1569-1577.
37. Patton MH, Bizup BT, Grace AA: The infralimbic cortex bidirectionally modulates mesolimbic dopamine neuron activity via distinct neural pathways. J Neurosci 2013; 33: 16865-16873.
38. Belujon P, Grace AA: Critical role of the prefrontal cortex in the regulation of hippocampus-accumbens information flow. J Neurosci 2008; 28: 9797-9805.
39. Valenti O, Lodge DJ, Grace AA: Aversive stimuli alter ventral tegmental area dopamine neuron activity via a common action in the ventral hippocampus. J Neurosci 2011; 3: 4280-4289.
40. Gill KM, Grace AA: Differential effects of acute and repeated stress on hippocampus and amygdala inputs to the nucleus accumbens shell. Int J Neuropsychopharmacol 2013; 16: 2013-2025.
41. Lisman JE, Coyle JT, Green RW, Javitt DC, Benes FM, Heckers S, Grace AA: Circuitbased framework for understanding neurotransmitter and risk gene interactions in schizophrenia. Trends Neurosci 2008; 31: 234-242.
42. Piontkewitz Y, Bernstein HG, Dobrowolny H, Bogerts B, Weiner I, Keilhoff G: Effects of risperidone treatment in adolescence on hippocampal neurogenesis, parvalbumin expression, and vascularization following prenatal immune activation in rats. Brain Behav Immun 2012; 26: 353-363.
43. Meyer U, Nyffeler M, Yee BK, Knuesel I, Feldon J: Adult brain and behavioral pathological markers of prenatal immune challenge during early/middle and late fetal development in mice. Brain Behav Immun 2008; 22: 469-486.
44. Zhang Z, van Praag H: Maternal immune activation differentially impacts mature and adult-born hippocampal neurons in male mice. Brain Behav Immun 2015; 45: 60-70.
45. Dickerson DD, Overeem KA, Wolff AR, Williams JM, Abraham WC, Bilkey DK: Association of aberrant neural synchrony and altered GAD67 expression following exposure to maternal immune activation, a risk factor for schizophrenia. Transl Psychiatry 2014; 4:e418.
46. Boksa P: Effects of prenatal infection on brain development and behavior: a review of findings from animal models. Brain Behav Immun 2010; 24: 881-897.
47. Miyoshi G, Butt SJ, Takebayashi H, Fishell G: Physiologically distinct temporal cohorts of cortical interneurons arise from telencephalic Olig2-expressing precursors. J Neurosci 2007; 27: 7786-7798.
48. Wonders CP, Taylor L, Welagen J, Mbata IC, Xiang JZ, Anderson SA: A spatial bias for the origins of interneuron subgroups within the medial ganglionic eminence. Dev Biol 2008; 314: 127-136.
49. Inan M, Welagen J, Anderson SA: Spatial and temporal bias in the mitotic origins of somatostatin-and parvalbumin-expressing interneuron subgroups and the chandelier subtype in the medial ganglionic eminence. Cereb Cortex 2012; 22: 820-827.
50. Marsicano G, Lutz B: Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain. Eur J Neurosci 1999; 11: 4213-4225.
51. Siegel RA, Duker EM, Fuchs E, Pahnke U, Wuttke W: Responsiveness of mesolimbic, mesocortical, septal and hippocampal cholecystokinin and substance P neuronal systems to stress, in the male rat. Neurochem Int 1984; 6: 783-789.
52. Vialou V, Bagot RC, Cahill ME, Ferguson D, Robison AJ, Dietz DM, Fallon B, Mazei-Robison M, Ku SM, Harrigan E, Winstanley CA, Joshi T, Feng J, Berton O, Nestler EJ: Prefrontal cortical circuit for depression-and anxiety-related behaviors mediated by cholecystokinin: role of ΔFosB. J Neurosci 2014; 34: 3878-3887.
53. Seillier A, Martinez AA, Giuffrida A: Phencyclidine-induced social withdrawal results from deficient stimulation of cannabinoid CB1 receptors: implications for schizophrenia. Neuropsychopharmacology 2013; 38: 1816-1824.
54. Akdeniz C, Tost H, Meyer-Lindenberg A: The neurobiology of social environmental risk for schizophrenia: an evolving research field. Soc Psychiatry Psychiatr Epidemiol 2014; 49: 507-517.
55. Radhakrishnan R, Wilkinson ST, D'Souza DC: Gone to pot-A review of the association between cannabis and psychosis. Front Psychiatry 2014; 5: 54.
56. Sultan KT, Brown KN, Shi SH: Production and organization of neocortical interneurons. Front Cell Neurosci 2013; 7: 221.
57. Jinno S, Kosaka T: Cellular architecture of the mouse hippocampus: a quantitative aspect of chemically defined GABAergic neurons with stereology. Neurosci Res 2006; 56: 229-245.
58. Dallman PR: Biochemical basis for the manifestations of iron deficiency. Annu Rev Nutr 1986; 6: 13-40.
59. Georgieff MK: Long-term brain and behavioral consequences of early iron deficiency. Nutr Rev 2011; 69(suppl 1):S43-S48.
60. Akakin D, Martinez-Diaz H, Chen HX, Roper SN: Reduced densities of parvalbumin-and somatostatin-expressing interneurons in experimental cortical dysplasia and heterotopia in early postnatal development. Epilepsy Res 2013; 104: 226-233.
61. Papadopoulos GC, Cavanagh ME, Antonopoulos J, Michaloudi H, Parnavelas JG: Postnatal development of somatostatin-containing neurons in the visual cortex of normal and dark-reared rats. Exp Brain Res 1993; 92: 473-478.
62. Naus CC, Morrison JH, Bloom FE: Development of somatostatin-containing neurons and fibers in the rat hippocampus. Brain Res 1988; 468: 113-121.
63. Tuncdemir SN, Wamsley B, Stam FJ, Osakada F, Goulding M, Callaway EM, Rudy B, Fishell G: Early somatostatin interneuron connectivity mediates the maturation of deep layer cortical circuits. Neuron 2016; 89: 521-535.