Sustained alterations of hypothalamic tanycytes during posttraumatic hypopituitarism in male mice

Endocrinology

Volumn 155, Issue 5, 2014, Pages 1887-1898

  Osterstock, Guillaume ^a,b,c   Yandouzi, Taoufik El ^a,b,c   Romanò, Nicola ^a,b,c   Carmignac, Danielle ^a,b,c   Langlet, Fanny ^a,b,c   Coutry, Nathalie ^a,b,c   Guillou, Anne ^a,b,c   Schaeffer, Marie ^a,b,c   Chauvet, Norbert ^a,b,c   Vanacker, Charlotte ^d   Galibert, Evelyne ^a,b,c   Dehouck, Bénédicte ^d   Robinson, Iain C A F ^a,b,c   Prévot, Vincent ^d   Mollard, Patrice ^a,b,c   Plesnila, Nikolaus ^a,b,c   Méry, Pierre François ^a,b,c  

^a CNRS   (France)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^c ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^d Department of Development and Plasticity of the Postnatal Brain ^*  (France)

Author keywords

[No Author keywords available]

Indexed keywords

CLAUDIN 1; GLIAL FIBRILLARY ACIDIC PROTEIN; GROWTH HORMONE; GROWTH HORMONE RELEASING FACTOR; IMMUNOGLOBULIN G; LUTEINIZING HORMONE; PROLACTIN; PROTEIN ZO1;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; ASTROCYTE; BLOOD SAMPLING; BRAIN THIRD VENTRICLE; CONTROLLED CORTICAL IMPACT; CONTROLLED STUDY; GLIA CELL; GROWTH HORMONE DEFICIENCY; GROWTH HORMONE RELEASE; HISTOLOGY; HYPOPHYSIS; HYPOPITUITARISM; HYPOTHALAMUS; IMMUNOCYTOCHEMISTRY; MALE; MEDIAN EMINENCE; MOUSE; NONHUMAN; PATCH CLAMP TECHNIQUE; PHENOTYPE; PITUITARY STALK; POSTTRAUMATIC COMPLICATION; POSTTRAUMATIC HYPOPITUITARISM; PRIORITY JOURNAL; PROTEIN LOCALIZATION; QUALITY OF LIFE; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TANYCYTE; TIGHT JUNCTION; TRAUMATIC BRAIN INJURY;

ANIMALS; ARCUATE NUCLEUS; BIOLOGICAL MARKERS; BRAIN INJURIES; DISEASE MODELS, ANIMAL; EPENDYMOGLIAL CELLS; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; GROWTH HORMONE-RELEASING HORMONE; HYPOPITUITARISM; HYPOTHALAMUS; IMMUNOGLOBULIN G; MALE; MEDIAN EMINENCE; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEURONS; PERMEABILITY; RECOMBINANT FUSION PROTEINS; THIRD VENTRICLE; TIGHT JUNCTIONS;

EID: 84899460589     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-1336     Document Type: Article

References (76)

1. Maas AIR, Stocchetti N, Bullock R. Moderate and severe traumatic brain injury in adults. Lancet Neurol. 2008;7:728-741 (Pubitemid 351957931)
2. Maegele M, Engel D, Bouillon B, et al. Incidence and outcome of traumatic brain injury in an urban area in Western Europe over 10 years. Eur Surg Res. 2007;39:372-379 (Pubitemid 47614362)
3. Husson EC, Ribbers GM, Willemse-van Son AHP, Verhagen AP, Stam HJ. Prognosis of six-month functioning after moderate to severe traumatic brain injury: a systematic review of prospective cohort studies. J Rehabil Med. 2010;42:425-436
4. Yu S, Kaneko Y, Bae E, et al. Severity of controlled cortical impact traumatic brain injury in rats and mice dictates degree of behavioral deficits. Brain Res. 2009;1287:157-163
5. Silver J, Miller JH. Regeneration beyond the glial scar. Nat Rev Neurosci. 2004;5:146-156 (Pubitemid 38160289)
6. Benowitz LI, Carmichael ST. Promoting axonal rewiring to improve outcome after stroke. Neurobiol Dis. 2010;37:259-266
7. Fleiss B, Gressens P. Tertiary mechanisms of brain damage: a new hope for treatment of cerebral palsy? Lancet Neurol. 2012;11(6): 556-66
8. Smith DH, Chen XH, Pierce JE, et al. Progressive atrophy and neuron death for one year following brain trauma in the rat. J Neurotrauma. 1997;14:715-727 (Pubitemid 27479412)
9. Dixon CE, Kochanek PM, Yan HQ, et al. One-year study of spatial memory performance, brain morphology, and cholinergic markers after moderate controlled cortical impact in rats. J Neurotrauma. 1999;16:109-122 (Pubitemid 29113822)
10. Bramlett HM, Dietrich WD. Quantitative structural changes in white and gray matter 1 year following traumatic brain injury in rats. Acta Neuropathol. 2002;103:607-614 (Pubitemid 36067509)
11. Faden AI, Stoica B. Neuroprotection: challenges and opportunities. Arch Neurol. 2007;64:794-800 (Pubitemid 46919833)
12. Zohar O, Schreiber S, Getslev V, Schwartz JP, Mullins PG, Pick CG. Closed-head minimal traumatic brain injury produces long-term cognitive deficits in mice. Neuroscience. 2003;118:949-955 (Pubitemid 36561183)
13. Schneider HJ, Kreitschmann-Andermahr I, Ghigo E, Stalla GK, Agha A. Hypothalamopituitary dysfunction following traumatic brain injury and aneurismal subarachnoid hemorrhage: a systematic review. JAMA. 2007;298:1429-1438 (Pubitemid 47481609)
14. Tanriverdi F, Unluhizarci K, Kelestimur F. Pituitary function in subjects with mild traumatic brain injury: a review of literature and proposal of a screening strategy. Pituitary. 2010;13:146-153
15. Aberg ND, Brywe KG, Isgaard J. Aspects of growth hormone and insulin-like growth factor-I related to neuroprotection, regeneration, and functional plasticity in the adult brain. ScientificWorld- Journal. 2006;6:53-80
16. Scheepens A, Williams CE, Breier BH, Guan J, Gluckman PD.Arole for the somatotropic axis in neural development, injury and disease. J Pediatr Endocrinol Metab 2000;6(suppl 13):1483-1491 (Pubitemid 32063202)
17. Murray RD, Skillicorn CJ, Howell SJ, et al. Influences on quality of life in GH deficient adults and their effect on response to treatment. Clin Endocrinol (Oxf). 1999;51:565-573
18. Kelly DF, McArthur DL, Levin H, et al. Neurobehavioral and quality of life changes associated with growth hormone insufficiency after complicated mild, moderate, or severe traumatic brain injury. J Neurotrauma. 2006;23:928-942 (Pubitemid 43962852)
19. Giustina A, Veldhuis JD. Pathophysiology of the neuroregulation of growth hormone secretion in experimental animals and the human. Endocr Rev. 1998;19:717-797 (Pubitemid 128506521)
20. Daniel PM, Prichard MML, Treip CS. Traumatic infarction of the anterior lobe of the pituitary gland. Lancet. 1959;2(7109):927-931
21. Treip CS. Hypothalamic and pituitary injury. J Clin Pathol (R. Coll Pathol.). 1970;4(suppl 23):178-186
22. Benvenga S, Campenní A, RuggeriRM,Trimarchi F. Clinical review 113: hypopituitarism secondary to head trauma. J Clin Endocrinol Metab. 2000;85(4):1353-1361 (Pubitemid 32289472)
23. Kasturi BS, Stein DG. Traumatic brain injury causes long-term reduction in serum growth hormone and persistent astrocytosis in the cortico-hypothalamo- pituitary axis of adult male rats. J Neurotrauma. 2009;26:1315-1324
24. Cernak I. Animal models of head trauma. NeuroRx. 2005;2(3): 410-422 (Pubitemid 41444875)
25. Trabold R, Erös C, Zweckberger K, et al. The role of bradykinin B(1) and B(2) receptors for secondary brain damage after traumatic brain injury in mice. J Cereb Blood Flow Metab. 2010;30:130-139
26. Lafont C, Desarménien MG, Cassou M, et al. Cellular in vivo imaging reveals coordinated regulation of pituitary microcirculation and GH cell network function. Proc Natl Acad Sci USA. 2010;107: 4465-4470
27. Clark RG, Robinson ICAF. Growth hormone (GH) responses to multiple injections of a fragment of human GH-releasing factor in conscious male and female rats. J Endocrinol. 1985;106:281-289 (Pubitemid 16248576)
28. McGuinness L, Magoulas C, Sesay AK, et al. Autosomal dominant growth hormone deficiency disrupts secretory vesicles in vitro and in vivo in transgenic mice. Endocrinology. 2003;144(2):720-731 (Pubitemid 36205246)
29. Waite E, Lafont C, Carmignac D, et al. Different degrees of somatotroph ablation compromise pituitary growth hormone cell network structure and other pituitary endocrine cell types. Endocrinology. 2010;151:234-243
30. Steyn FJ, Huang L, Ngo ST, et al. Development of a method for the determination of pulsatile growth hormone secretion in mice. Endocrinology. 2011;152(8):3165-3171
31. Hanchate NK, Parkash J, Bellefontaine N, et al. Kisspeptin-GPR54 signaling in mouse NO-synthesizing neurons participates in the hypothalamic control of ovulation. J Neurosci. 2012;32:932-945
32. Luque RM, Kineman RD. Impact of obesity on the growth hormone axis: evidence for a direct inhibitory effect of hyperinsulinemia on pituitary function. Endocrinology. 2006;147:2754-2763 (Pubitemid 43764612)
33. Córdoba-Chacón J, Gahete MD, Castaño JP, Kineman RD, Luque RM. Somatostatin and its receptors contribute in a tissue-specific manner to the sex-dependent metabolic (fed/fasting) control of growth hormone axis in mice. Am J Physiol Endocrinol Metab. 2011;300(1):E46-E54
34. Phelps CJ, Romero MI, Hurley DL. Growth hormone-releasing hormone- producing and dopaminergic neurones in the mouse arcuate nucleus are independently regulated populations. J Neuroendocrinol. 2003;15:280-288 (Pubitemid 36266896)
35. Alonso G, Sanchez-Hormigo A, Loudes C, et al Selective alteration at the growth-hormone-releasing-hormone nerve terminals during aging in GHRH-green fluorescent protein mice. Aging Cell. 2007; 6:197-207 (Pubitemid 46455064)
36. Mullier A, Bouret SG, Prevot V, Dehouck B. Differential distribution of tight junction proteins suggests a role for tanycytes in bloodhypothalamus barrier regulation in the adult mouse brain. J Comp Neurol. 2010;518:943-962
37. Langlet F, Levin BE, Luquet S, et al. Tanycytic VEGF-A boosts blood-hypothalamus barrier plasticity and access of metabolic signals to the arcuate nucleus in response to fasting. Cell Metab. 2013; 17:607-617
38. Cetin A, Komai S, Eliava M, Seeburg PH, Osten P. Stereotaxic gene delivery in the rodent brain. Nat Protoc. 2006;1:3166-3173
39. Budry L, Lafont C, El Yandouzi T, et al. Related pituitary cell lineages develop into interdigitated 3D cell networks. Proc Natl Acad Sci USA. 2011;108(30):12515-12520
40. Balthasar N, Méry P-F, Magoulas CB, et al. Growth hormone-releasing hormone (GHRH) neurons in GHRH-enhanced green fluorescent protein transgenic mice: a ventral hypothalamic network. Endocrinology. 2003;144:2728-2740 (Pubitemid 36629926)
41. Ho KKY. Consensus guidelines for the diagnosis and treatment of adults withGHdeficiency II: a statement of theGHResearch Society in association with the European Society for Pediatric Endocrinology, Lawson Wilkins Society, European Society of Endocrinology, Japan Endocrine Society, and Endocrine Society of Australia. Eur J Endocrinol. 2007;157:695-700
42. Rodríguez EM, Blázquez JL, Pastor FE, et al. Hypothalamic tanycytes: a key component of brain-endocrine interaction. Int Rev Cytol. 2005;247:89-164 (Pubitemid 41782012)
43. Gordon GRJ, Iremonger KJ, Kantevari S, Ellis-Davies GCR, MacVicar BA, Bains JS. Astrocyte-mediated distributed plasticity at hypothalamic glutamate synapses. Neuron. 2009;64:391-403
44. Sofroniew MV. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci. 2009;32:638-647
45. Ortinski PI, Dong J, Mungenast A, et al. Selective induction of astrocytic gliosis generates deficits in neuronal inhibition. Nat Neurosci. 2010;13:584-591
46. Baccam N, Alonso G, Costecalde T, et al. Dual-level afferent control of growth hormone-releasing hormone(GHRH)neurons inGHRHgreen fluorescent protein transgenic mice. J Neurosci. 2007;27: 1631-1641 (Pubitemid 46280061)
47. WittCM,Raychaudhuri S, Schaefer B, Chakraborty AK, Robey EA. Directed migration of positively selected thymocytes visualized in real time. PLoS Biol. 2005;3:e160
48. Ciofi P. The arcuate nucleus as a circumventricular organ in the mouse. Neurosci Lett. 2011;487(2):187-907
49. Low MJ, Otero-Corchon V, Parlow AF, et al. Somatostatin is required for masculinization of growth hormone-regulated hepatic gene expression but not of somatic growth. J Clin Invest. 2001;107: 1571-1580 (Pubitemid 32574643)
50. Briard N, Guillaume V, Frachebois C, et al. Endotoxin injection increases growth hormone and somatostatin secretion in sheep. Endocrinology. 1998;139:2662-2669 (Pubitemid 28512372)
51. Le Tissier PR, Carmignac DF, Lilley S, et al. Hypothalamic growth hormone-releasing hormone (GHRH) deficiency: targeted ablation of GHRH neurons in mice using a viral ion channel transgene. Mol Endocrinol. 2005;19(5):1251-1262 (Pubitemid 40594122)
52. Sato M, Frohman LA. Differential effects of central and peripheral administration of growth hormone (GH) and insulin-like growth factor on hypothalamic GH-releasing hormone and somatostatin gene expression in GH-deficient dwarf rats. Endocrinology. 1993; 133:793-799 (Pubitemid 23238894)
53. Hurley DL,WeeBE, Phelps CJ.Growthhormone releasing hormone expression during postnatal development in growth hormone-deficient Ames dwarf mice: mRNA in situ hybridization. Neuroendocrinology. 1998;68:201-209 (Pubitemid 28427104)
54. Flavell DM, Wells T, Wells SE, Carmignac DF, Thomas GB, Robinson IC. Dominant dwarfism in transgenic rats by targeting human growth hormone (GH) expression to hypothalamic GH-releasing factor neurons. EMBO J. 1996;15:3871-3879 (Pubitemid 26289797)
55. Zheng H, Bailey A, Jiang MH, et al. Somatostatin receptor subtype 2 knockout mice are refractory to growth hormone-negative feedback on arcuate neurons. Mol Endocrinol. 1997;11:1709-1717 (Pubitemid 27435418)
56. Wettschureck N, Moers A, Wallenwein B, Parlow AF, Maser-Gluth C, Offermanns S. Loss of Gq/11 family G proteins in the nervous system causes pituitary somatotroph hypoplasia and dwarfism in mice. Mol Cell Biol. 2005;25:1942-1948 (Pubitemid 40280156)
57. Mantamadiotis T, Kretz O, Ridder S, et al. Hypothalamic 3',5'- cyclic adenosine monophosphate response element-binding protein loss causes anterior pituitary hypoplasia and dwarfism in mice. Mol Endocrinol. 2006;20:204-211 (Pubitemid 43011681)
58. D'Ambrosio R, Maris DO, Grady MS, Winn HR, Janigro D. Impaired K(+) homeostasis and altered electrophysiological properties of post-traumatic hippocampal glia. J Neurosci. 1999;19:8152- 8162 (Pubitemid 30225811)
59. Cohen AS, Pfister BJ, Schwarzbach E, Grady MS, Goforth PB, Satin LS. Injury-induced alterations inCNSelectrophysiology. Prog Brain Res. 2007;161:143-169
60. Sanders MJ, Sick TJ, Perez-Pinzon MA, Dietrich WD, Green EJ. Chronic failure in the maintenance of long-term potentiation following fluid percussion injury in the rat. Brain Res. 2000;861:69- 76 (Pubitemid 30177284)
61. Norris CM, Scheff SW. Recovery of afferent function and synaptic strength in hippocampal CA1 following traumatic brain injury. J Neurotrauma. 2009;26:2269-2278
62. Ramlackhansingh AF, Brooks DJ, Greenwood RJ, et al. Inflammation after trauma: microglial activation and traumatic brain injury. Ann Neurol. 2011;70(3):374-83
63. Lechan RM, Nestler JL, Molitch ME. Immunohistochemical identification of a novel substance with human growth hormone-like immunoreactivity in rat brain. Endocrinology. 1981;109(6):1950- 1962 (Pubitemid 12252319)
64. Pan W, Yu Y, Cain CM, Nyberg F, Couraud PO, Kastin AJ. Permeation of growth hormone across the blood-brain barrier. Endocrinology. 2005;146(11):4898-4904 (Pubitemid 41446628)
65. Addison ML, Rissman EF. Sexual dimorphism of growth hormone in the mouse hypothalamus: regulation by estradiol. Endocrinology. 2012;153:1898-1907
66. Sumi N, Nishioku T, Takata F, et al. Lipopolysaccharide-activated microglia induce dysfunction of the blood-brain barrier in rat microvascular endothelial cells co-cultured with microglia. Cell Mol Neurobiol. 2010;30:247-253
67. Sanders NM, Dunn-Meynell AA, Levin BE. Third ventricular alloxan reversibly impairs glucose counterregulatory responses. Diabetes. 2004;53(5):1230-1236 (Pubitemid 38569008)
68. Johanson C, Stopa E, Baird A, Sharma H. Traumatic brain injury and recovery mechanisms: peptide modulation of periventricular neurogenic regions by the choroid plexus-CSF nexus. J Neural Transm. 2011;118:115-133
69. Carraway CA, Carraway KL. Sequestration and segregation of receptor kinases in epithelial cells: implications for ErbB2 oncogenesis. Sci STKE 2007;2007(381):re3
70. Prévot V, Hanchate NK, Bellefontaine N, et al. Function-related structural plasticity of the GnRH system: a role for neuronal-glialendothelial interactions. Front Neuroendocrinol. 2010;31(3):241- 258
71. Carretero J, Burks D, RubioM,et al. Immunocytochemical evidence for growth hormone-releasing hormone in the tanycytes of the median eminence of the rat. Folia Morphol (Warsz). 2007;61(4):209- 216
72. Chauvet N, Prieto M, Alonso G. Tanycytes present in the adult rat mediobasal hypothalamus support the regeneration of monoaminergic axons. Exp Neurol. 1998;151:1-13 (Pubitemid 28223851)
73. Lee DA, Bedont JL, Pak T, et al. Tanycytes of the hypothalamic median eminence form a diet-responsive neurogenic niche. Nat Neurosci. 2012;15(5):700-702
74. Schwab JM, Beschorner R, Meyermann R, Gözalan F, Schluesener HJ. Persistent accumulation of cyclooxygenase-1-expressing microglial cells and macrophages and transient upregulation by endothelium in human brain injury. J Neurosurg. 2002;96:892-899 (Pubitemid 34415404)
75. Gentleman SM, Leclercq PD, Moyes L, et al. Long-term intracerebral inflammatory response after traumatic brain injury. Forensic Sci Int. 2004;146:97-104 (Pubitemid 39470145)
76. Beck KD, Nguyen HX, Galvan MD, Salazar DL, Woodruff TM, Anderson AJ. Quantitative analysis of cellular inflammation after traumatic spinal cord injury: evidence for a multiphasic inflammatory response in the acute to chronic environment. Brain. 2010;133: 433-447.