Generic placeholder image

Current Neurovascular Research

Author(s): Zhen He* and Tucker A. Patterson

DOI: 10.2174/1567202616666190627120135

DownloadDownload PDF Flyer Cite As
A Potential Role for the Existence of Pericytes in the Neurovascular Unit of the Sexually Dimorphic Nucleus of the Rat Preoptic Area to Control Blood-Brain Barrier Function

Page: [194 - 201] Pages: 8

  • * (Excluding Mailing and Handling)

Abstract

Background: The present study aimed at determining pericytes, a missing component in the previously proposed living neurovascular unit (NVU) of the sexually dimorphic nucleus of the preoptic area (SDN-POA) in rats.

Materials and Methods: Calbindin D28K-immunoreactivities (CB28-irs) were used to delineate the SDN-POA in which CD13-immunoreactivities (CD13-irs) or alpha-smooth muscle actinimmunoreactivities (αSMA-irs), two pericyte biomarkers serving the indexes of pericytes, were tagged using two adjacent brain sections (90-micron intervals). In addition, the nestinimmunoreactive (nestin-ir) cells in the SDN-POA were counted as pericytes referring to additional standards: location and nucleic and cellular morphology. Male SDN-POA volume (5.0±0.3x10-3 mm3) was significantly larger than the female (1.7±0.3x10-3 mm3). Within the SDN-POA, the CD13-irs were characterized as dots, densely packed and net-like in distribution, while the αSMAirs, excluding pipe-like or circular structures, appeared as short rod-like structures that were sparsely distributed.

Results: The immunoreactive counts of alpha-smooth muscle actin were 353±57/mm2 in males and 124±46/mm2 in females (p<0.05). On the other hand, densities of the dot-like CD13-irs were similar between males (4009±301/mm2) and females (4018±414/ mm2). There was no difference between the male and the female in the nestin-ir pericyte count in the SDN-POA.

Conclusion: In conclusion, the present study adds new information concerning pericytes to the living NVU of the SDN-POA. There is a difference of sex in the count of the αSMA-irs in the living NVU of the SDN-POA. However, why such a difference exists warrants further investigations.

Keywords: Alpha-smooth muscle actin, CD13-immunoreactivity, living neurovascular unit, nestin, pericyte, sexually dimorphic nucleus.

[1]
He Z, Cui L, Ferguson SA, Paule MG. A working module for the neurovascular unit in the sexually dimorphic nucleus of the preoptic area. Mol Neurobiol 2018; 55(1): 156-63.
[2]
Bergers G, Song S. The role of pericytes in blood-vessel formation and maintenance. Neuro-oncol 2005; 7(4): 452-64.
[3]
Rockey DC, Weymouth N, Shi Z. Smooth muscle α actin (Acta2) and myofibroblast function during hepatic wound healing. PLoS One 2013; 8(10): e77166.
[4]
Weymouth N, Shi Z, Rockey DC. Smooth muscle α actin is specifically required for the maintenance of lactation. Dev Biol 2012; 363(1): 1-14.
[5]
Rucker HK, Wynder HJ, Thomas WE. Cellular mechanisms of CNS pericytes Brain Res Bull 2000; 15; 51(5): 363-9.
[6]
Hurtado-Alvarado G, Cabañas-Morales AM, Gómez-Gónzalez B. Pericytes: Brain-immune interface modulators Front. Integr Neurosci 2014; 7: 80.
[7]
Kunz J, Krause D, Kremer M, Dermietzel R. The 140-kDa protein of blood-brain barrier-associated pericytes is identical to aminopeptidase N. J Neurochem 1994; 62(6): 2375-86.
[8]
Wang YY, Wu SX, Li YQ. Preproenkephalin-like immunoreactive and calcium-binding proteins-like immunoreactive double-labelled neurons in the spinal trigeminal nucleus caudalis of the rat. Histochem J 2002; 34(5): 241-5.
[9]
Merchenthaler I, Lennard DE, Cianchetta P, Merchenthaler A, Bronstein D. Induction of proenkephalin in tuberoinfundibular dopaminergic neurons by hyperprolactinemia: The role of sex steroids. Endocrinology 1995; 136(6): 2442-50.
[10]
Bodnar RJ. Endogenous opiates and behavior: 2015. Peptides 2017; 88: 126-88.
[11]
Bodnar RJ. Endogenous opiates and behavior: 2014. Peptides 2016; 75: 18-70.
[12]
Bialy M, Strefnel M, Nikolaev-Diak A, Socha A, Nikolaev E, Boguszewski PM. Sexual performance and precontact 50-kHz ultrasonic vocalizations in WAG/Rij rats: Effects of opioid receptor treatment. Epilepsy Behav 2014; 39: 66-72.
[13]
Cordes MA, Stevenson SA, Driessen TM, Eisinger BE, Riters LV. Sexually-motivated song is predicted by androgen-and opioid-related gene expression in the medial preoptic nucleus of male European starlings (Sturnus vulgaris). Behav Brain Res 2015; 278(278): 12-20.
[14]
Liu CH, Ren JQ, You Z, et al. Noninvasive detection of neural progenitor cells in living brains by MRI. FASEB J 2012; 26(4): 1652-62.
[15]
Tatebayashi K, Tanaka Y, Nakano-Doi A, et al. Identification of multipotent stem cells in human brain tissue following stroke. Stem Cells Dev 2017; 26(11): 787-97.
[16]
He Z, Cui L, Wu SS, et al. Increased severity of acute cerebral ischemic injury correlates with enhanced stem cell induction as well as with predictive behavioral profiling. Curr Neurovasc Res 2004; 1(5): 399-409.
[17]
He Z, Cui L, Meschia JF, et al. McKinney M. Hippocampal progenitor cells express nestin following cerebral ischemia in rats. Neuroreport 2005; 16(14): 1541-4.
[18]
He Z, Ferguson SA, Cui L, Greenfield LJ Jr, Paule MG. Role of neural stem cell activity in postweaning development of the sexually dimorphic nucleus of the preoptic area in rats. PLoS One 2013; 8(1): e54927.
[19]
He Z, Paule MG, Ferguson SA. Low oral doses of bisphenol A increase volume of the sexually dimorphic nucleus of the preoptic area in male, but not female, rats at postnatal day 21. Neurotoxicol Teratol 2012; 34(3): 331-7.
[20]
He Z, Liu X-S, Cui L, et al. Estrogen masculinizes the female rat sexually-dimorphic nucleus of the preoptic area at weaning via proliferative activity. Society for Neuroscience Abstract Viewer and Itinerary Planner 2013; p. 43.
[21]
He Z, Cui L, Paule MG, Ferguson SA. Estrogen selectively mobilizes neural stem cells in the third ventricle stem cell niche of postnatal day 21 rats. Mol Neurobiol 2015; 52(2): 927-33.
[22]
Gragera RR, Muñiz E, Martínez-Rodriguez R. Molecular and ultrastructural basis of the blood-brain barrier function. Immunohistochemical demonstration of Na+/K+ ATPase, alpha-actin, phosphocreatine and clathrin in the capillary wall and its microenvironment. Cell Mol Biol 1993; 39(8): 819-28.
[23]
Hatan M, Shinder V, Israeli D, et al. The Drosophila blood brain barrier is maintained by GPCR-dependent dynamic actin structures. J Cell Biol 2011; 192(2): 307-19.
[24]
Bittner S, Ruck T, Schuhmann MK, et al. Endothelial TWIK-related potassium channel-1 (TREK1) regulates immune-cell trafficking into the CNS. Nat Med 2013; 19(9): 1161-5.
[25]
Arendash GW, Gorski RA. Effects of discrete lesions of the sexually dimorphic nucleus of the preoptic area or other medial preoptic regions on the sexual behavior of male rats. Brain Res Bull 1983; 10(1): 147-54.
[26]
Rayen I, Steinbusch HW, Charlier TD, Pawluski JL. Developmental fluoxetine exposure and prenatal stress alter sexual differentiation of the brain and reproductive behavior in male rat offspring. Psychoneuroendocrinology 2013; 38(9): 1618-29.
[27]
Sickel MJ, McCarthy MM. Calbindin-D28k immunoreactivity is a marker for a subdivision of the sexually dimorphic nucleus of the preoptic area of the rat: Developmental profile and gonadal steroid modulation. J Neuroendocrinol 2000; 12(5): 397-402.
[28]
Wang Q, Wei J, Shi Y. Platelet microvesicles promote the recovery of neurological function in mouse model of cerebral infarction by inducing angiogenesis. Biochem Biophys Res Commun 2019; 513(4): 997-1004.
[29]
Saint-Pol J, Gosselet F. Oxysterols and the NeuroVascular Unit (NVU): A far true love with bright and dark sides. J Steroid Biochem Mol Biol 2019; 191(19): 105368.
[30]
Thuillier R, Wang Y, Culty M. Prenatal exposure to estrogenic compounds alters the expression pattern of platelet-derived growth factor receptors alpha and beta in neonatal rat testis: Identification of gonocytes as targets of estrogen exposure. Biol Reprod 2003; 68(3): 867-80.
[31]
Imai T, Iwata S, Hirayama T, et al. Intracellular Fe (2+) accumulation in endothelial cells and pericytes induces blood-brain barrier dysfunction in secondary brain injury after brain hemorrhage. Sci Rep 2019; 9(1): 6228.