Effect of hyperoxic exposure during early development on neurotrophin expression in the carotid body and nucleus tractus solitarii

Journal of Applied Physiology

Volumn 112, Issue 10, 2012, Pages 1762-1772

  Chavez Valdez, Raul ^a,b   Mason, Ariel ^a   Nunes, Ana R ^a,c   Northington, Frances J ^a   Tankersley, Clarke ^d   Ahlawat, Rajni ^a   Johnson, Sheree M ^e   Gauda, Estelle B ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^c NOVA MEDICAL SCHOOL   (Portugal)

^d JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^e HOWARD UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Brain derived neurotrophic factor; Glial derived neurotrophic factor; Hypoxic ventilatory response; Peripheral arterial chemoreceptors; Plasticity

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CASP3 PROTEIN, RAT; CASPASE 3; MESSENGER RNA; NERVE GROWTH FACTOR RECEPTOR; PROTEIN KINASE; TNFRSF16 PROTEIN, RAT; TROPOMYOSIN KINASE; TYROSINE 3 MONOOXYGENASE;

AGE; ANIMAL; APOPTOSIS; ARTICLE; CAROTID BODY; CELL SURVIVAL; DISEASE MODEL; GENETICS; GROWTH, DEVELOPMENT AND AGING; HYPEROXIA; METABOLISM; NEWBORN; PATHOLOGY; PATHOPHYSIOLOGY; RAT; SOLITARY TRACT NUCLEUS; SPRAGUE DAWLEY RAT;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CAROTID BODY; CASPASE 3; CELL SURVIVAL; DISEASE MODELS, ANIMAL; HYPEROXIA; PROTEIN KINASES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NERVE GROWTH FACTOR; RNA, MESSENGER; SOLITARY NUCLEUS; TYROSINE 3-MONOOXYGENASE;

EID: 84862091085     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.01609.2011     Document Type: Article

References (54)

1. Balkowiec A, Katz DM. Activity-dependent release of endogenous brainderived neurotrophic factor from primary sensory neurons detected by ELISA in situ. J Neurosci 20: 7417-7423, 2000.
2. Balkowiec A, Kunze DL, Katz DM. Brain-derived neurotrophic factor acutely inhibits AMPA-mediated currents in developing sensory relay neurons. J Neurosci 20: 1904-1911, 2000. (Pubitemid 30220387)
3. 2 sensitivity following chronic postnatal hyperoxia in rats. Respir Physiol Neurobiol 177: 47-55, 2011.
4. Bavis RW, Mitchell GS. Long-term effects of the perinatal environment on respiratory control. J Appl Physiol 104: 1220-1229, 2008. (Pubitemid 351507966)
5. Bavis RW, Wenninger JM, Miller BM, Dmitrieff EF, Olson EB Jr, Mitchell GS, Bisgard GE. Respiratory plasticity after perinatal hyperoxia is not prevented by antioxidant supplementation. Respir Physiol Neurobiol 160: 301-312, 2008. (Pubitemid 351754802)
6. Bisgard GE, Olson EB Jr, Wang ZY, Bavis RW, Fuller DD, Mitchell GS. Adult carotid chemoafferent responses to hypoxia after 1, 2, and 4 wk of postnatal hyperoxia. J Appl Physiol 95: 946-952, 2003. (Pubitemid 37033986)
7. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254, 1976.
8. Brady R, Zaidi SI, Mayer C, Katz DM. BDNF is a target-derived survival factor for arterial baroreceptor and chemoafferent primary sensory neurons. J Neurosci 19: 2131-2142, 1999. (Pubitemid 29133391)
9. Carroll JL. Developmental plasticity in respiratory control. J Appl Physiol 94: 375-389, 2003.
10. 2 in the cat. J Appl Physiol 75: 2383-2391, 1993. (Pubitemid 24008349)
11. Cohen-Cory S, Kidane AH, Shirkey NJ, Marshak S. Brain-derived neurotrophic factor and the development of structural neuronal connectivity. Dev Neurobiol 70: 271-288, 2010.
12. Davies AM. The role of neurotrophins during successive stages of sensory neuron development. Prog Growth Factor Res 5: 263-289, 1994.
13. Dejours P. Chemoreflexes in breathing. Physiol Rev 42: 335-358, 1962.
14. Dmitrieff EF, Wilson JT, Dunmire KB, Bavis RW. Chronic hyperoxia alters the expression of neurotrophic factors in the carotid body of neonatal rats. Respir Physiol Neurobiol 175: 220-227, 2011.
15. Eide FF, Vining ER, Eide BL, Zang K, Wang XY, Reichardt LF. Naturally occurring truncated TrkB receptors have dominant inhibitory effects on brain-derived neurotrophic factor signaling. J Neurosci 16: 3123-3129, 1996. (Pubitemid 26142348)
16. Erickson JT, Brosenitsch TA, Katz DM. Brain-derived neurotrophic factor and glial cell line-derived neurotrophic factor are required simultaneously for survival of dopaminergic primary sensory neurons in vivo. J Neurosci 21: 581-589, 2001. (Pubitemid 32107447)
17. Erickson JT, Mayer C, Jawa A, Ling L, Olson EB Jr, Vidruk EH, Mitchell GS, Katz DM. Chemoafferent degeneration and carotid body hypoplasia following chronic hyperoxia in newborn rats. J Physiol 509: 519-526, 1998. (Pubitemid 28287009)
18. Erickson JT, Millhorn DE. Fos-like protein is induced in neurons of the medulla oblongata after stimulation of the carotid sinus nerve in awake and anesthetized rats. Brain Res 567: 11-24, 1991.
19. Felderhoff-Mueser U, Bittigau P, Sifringer M, Jarosz B, Korobowicz E, Mahler L, Piening T, Moysich A, Grune T, Thor F, Heumann R, Buhrer C, Ikonomidou C. Oxygen causes cell death in the developing brain. Neurobiol Dis 17: 273-282, 2004. (Pubitemid 39345782)
20. Finley JC, Katz DM. The central organization of carotid body afferent projections to the brainstem of the rat. Brain Res 572: 108-116, 1992.
21. Fukuchi M, Fujii H, Takachi H, Ichinose H, Kuwana Y, Tabuchi A, Tsuda M. Activation of tyrosine hydroxylase (TH) gene transcription induced by brain-derived neurotrophic factor (BDNF) and its selective inhibition through Ca(2+) signals evoked via the N-methyl-D-aspartate (NMDA) receptor. Brain Res 1366: 18-26, 2010.
22. Gauda EB, Carroll JL, Donnelly DF. Developmental maturation of chemosensitivity to hypoxia of peripheral arterial chemoreceptors-invited article. Adv Exp Med Biol 648: 243-255, 2009.
23. Gonzalez C, Almaraz L, Obeso A, Rigual R. Carotid body chemoreceptors: from natural stimuli to sensory discharges. Physiol Rev 74: 829-898, 1994. (Pubitemid 24328941)
24. Hertzberg T, Fan G, Finley JC, Erickson JT, Katz DM. BDNF supports mammalian chemoafferent neurons in vitro and following peripheral target removal in vivo. Dev Biol 166: 801-811, 1994.
25. Huang EJ, Reichardt LF. Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci 24: 677-736, 2001. (Pubitemid 32695243)
26. Hyman C, Hofer M, Barde YA, Juhasz M, Yancopoulos GD, Squinto SP, Lindsay RM. BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra. Nature 350: 230-232, 1991. (Pubitemid 21912205)
27. Izal-Azcarate A, Belzunegui S, San Sebastian W, Garrido-Gil P, Vazquez-Claverie M, Lopez B, Marcilla I, Luquin MA. Immunohistochemical characterization of the rat carotid body. Respir Physiol Neurobiol 161: 95-99, 2008. (Pubitemid 351324213)
28. Katz DM, Dutschmann M, Ramirez JM, Hilaire G. Breathing disorders in Rett syndrome: progressive neurochemical dysfunction in the respiratory network after birth. Respir Physiol Neurobiol 168: 101-108, 2009.
29. Kholodilov N, Yarygina O, Oo TF, Zhang H, Sulzer D, Dauer W, Burke RE. Regulation of the development of mesencephalic dopaminergic systems by the selective expression of glial cell line-derived neurotrophic factor in their targets. J Neurosci 24: 3136-3146, 2004. (Pubitemid 38405761)
30. Kholwadwala D, Donnelly DF. Maturation of carotid chemoreceptor sensitivity to hypoxia: in vitro studies in the newborn rat. J Physiol 453: 461-473, 1992.
31. Kline DD, Ogier M, Kunze DL, Katz DM. Exogenous brain-derived neurotrophic factor rescues synaptic dysfunction in Mecp2-null mice. J Neurosci 30: 5303-5310, 2010.
32. Kwak DJ, Kwak SD, Gauda EB. The effect of hyperoxia on reactive oxygen species (ROS) in rat petrosal ganglion neurons during development using organotypic slices. Pediatr Res 60: 371-376, 2006. (Pubitemid 44427585)
33. Leitner ML, Wang LH, Osborne PA, Golden JP, Milbrandt J, Johnson EM Jr. Expression and function of GDNF family ligands and receptors in the carotid body. Exp Neurol 191, Suppl 1: S68-S79, 2005. (Pubitemid 40075412)
34. Lessmann V. Neurotrophin-dependent modulation of glutamatergic synaptic transmission in the mammalian CNS. Gen Pharmacol 31: 667-674, 1998. (Pubitemid 28520041)
35. Ling L, Olson EB Jr, Vidruk EH, Mitchell GS. Attenuation of the hypoxic ventilatory response in adult rats following one month of perinatal hyperoxia. J Physiol 495: 561-571, 1996. (Pubitemid 26331836)
36. Ling L, Olson EB Jr, Vidruk EH, Mitchell GS. Integrated phrenic responses to carotid afferent stimulation in adult rats following perinatal hyperoxia. J Physiol 500: 787-796, 1997. (Pubitemid 27207835)
37. Massari VJ, Shirahata M, Johnson TA, Gatti PJ. Carotid sinus nerve terminals which are tyrosine hydroxylase immunoreactive are found in the commissural nucleus of the tractus solitarius. J Neurocytol 25: 197-208, 1996. (Pubitemid 26114878)
38. Mitchell GS, Baker TL, Nanda SA, Fuller DD, Zabka AG, Hodgeman BA, Bavis RW, Mack KJ, Olson EB Jr. Invited review: intermittent hypoxia and respiratory plasticity. J Appl Physiol 90: 2466-2475, 2001.
39. Mitchell GS, Johnson SM. Neuroplasticity in respiratory motor control. J Appl Physiol 94: 358-374, 2003.
40. Nunes AR, Monteiro EC, Johnson SM, Gauda EB. Bicarbonate-regulated soluble adenylyl cyclase (sAC) mRNA expression and activity in peripheral chemoreceptors. Adv Exp Med Biol 648: 235-241, 2009.
41. Pascual A, Hidalgo-Figueroa M, Gomez-Diaz R, Lopez-Barneo J. GDNF and protection of adult central catecholaminergic neurons. J Mol Endocrinol 46: R83-R92, 2011.
42. Pawar A, Peng YJ, Jacono FJ, Prabhakar NR. Comparative analysis of neonatal and adult rat carotid body responses to chronic intermittent hypoxia. J Appl Physiol 104: 1287-1294, 2008.
43. Peiris TS, Machaalani R, Waters KA. Brain-derived neurotrophic factor mRNA and protein in the piglet brainstem and effects of intermittent hypercapnic hypoxia. Brain Res 1029: 11-23, 2004. (Pubitemid 39463302)
44. Perrone S, Negro S, Tataranno ML, Buonocore G. Oxidative stress and antioxidant strategies in newborns. J Matern Fetal Neonatal Med 23 Suppl 3: 63-65, 2010.
45. Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30: e36, 2002.
46. Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP. Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper-Excel-based tool using pair-wise correlations. Biotechnol Lett 26: 509-515, 2004. (Pubitemid 38448421)
47. Pickel VM, Joh TH, Reis DJ. Ultrastructural localization of tyrosine hydroxylase in noradrenergic neurons of brain. Proc Natl Acad Sci USA 72: 659-663, 1975.
48. Shieh PB, Ghosh A. Molecular mechanisms underlying activitydependent regulation of BDNF expression. J Neurobiol 41: 127-134, 1999. (Pubitemid 29467612)
49. Tolosa JN, Cooper R, Myers AC, McLemore GL, Northington F, Gauda EB. Ontogeny of retrograde labeled chemoafferent neurons in the newborn rat nodose-petrosal ganglion complex: an ex vivo preparation. Neurosci Lett 384: 48-53, 2005. (Pubitemid 40826616)
50. Wang GP, Xu CS. Reference gene selection for real-time RT-PCR in eight kinds of rat regenerating hepatic cells. Mol Biotechnol 46: 49-57, 2010.
51. Wang ZY, Bisgard GE. Postnatal growth of the carotid body. Respir Physiol Neurobiol 149: 181-190, 2005. (Pubitemid 41406220)
52. Wiesel TN, Hubel DH. Effects of visual deprivation on morphology and physiology of cells in the cats lateral geniculate body. J Neurophysiol 26: 978-993, 1963.
53. Wong-Riley MT, Liu Q. Neurochemical and physiological correlates of a critical period of respiratory development in the rat. Respir Physiol Neurobiol 164: 28-37, 2008.
54. Zhuo H, Helke CJ. Presence and localization of neurotrophic receptor tyrosine kinase (TrkA, TrkB, TrkC) mRNAs in visceral afferent neurons of the nodose and petrosal ganglia. Brain Res Mol Brain Res 38: 63-70, 1996. (Pubitemid 26159193)