RNASeq-derived transcriptome comparisons reveal neuromodulatory deficiency in the CO2 insensitive brown Norway rat

Journal of Physiology

Volumn 593, Issue 2, 2015, Pages 415-430

  Puissant, Madeleine M ^a   Echert, Ashley E ^a   Yang, Chun ^a   Mouradian, Gary C ^a   Novotny, Tyler ^a   Liu, Pengyuan ^a   Liang, Mingyu ^a   Hodges, Matthew R ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; MONOAMINE; PROTIRELIN; SEROTONIN; TALTIRELIN; TRANSCRIPTOME; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; CARBON DIOXIDE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; BRAIN STEM; BROWN NORWAY RAT; CENTRAL NERVOUS SYSTEM; CHEMORECEPTOR REFLEX; CONTROLLED STUDY; DAHL SALT SENSITIVE RAT; GENE EXPRESSION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYPERCAPNIA; MALE; MEDULLA OBLONGATA; MEDULLARY RAPHE; NEUROMODULATION; NONHUMAN; PROTEIN DEFICIENCY; RAT; RESPIRATORY TRACT PARAMETERS; RNA SEQUENCE; SEROTONINERGIC SYSTEM; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; STRAIN DIFFERENCE; TRANSCRIPTOMICS; VENTILATORY CARBON DIOXIDE CHEMOREFLEX; ANALOGS AND DERIVATIVES; ANIMAL; DAHL RAT; DRUG EFFECTS; GENETICS; METABOLISM; RAPHE NUCLEUS; REFLEX; SPECIES DIFFERENCE;

ANIMALS; CARBON DIOXIDE; HYPERCAPNIA; NEUROTRANSMITTER AGENTS; RAPHE NUCLEI; RATS; RATS, INBRED BN; RATS, INBRED DAHL; RATS, SPRAGUE-DAWLEY; REFLEX; RNA, MESSENGER; SEROTONIN; SPECIES SPECIFICITY; THYROTROPIN-RELEASING HORMONE; TRANSCRIPTOME;

EID: 84921032820     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2014.285171     Document Type: Article

References (57)

1. Asai H, Asahi T, Yamamura M, Yamauchi-Kohno R & Saito A (2005). Lack of behavioral tolerance by repeated treatment with taltirelin hydrate, a thyrotropin-releasing hormone analog, in rats. Pharmacol Biochem Behav 82, 646-651.
2. Bang SJ, Jensen P, Dymecki SM & Commons KG (2012). Projections and interconnections of genetically defined serotonin neurons in mice. Eur J Neurosci 35, 85-96.
3. Bayliss DA, Viana F, Kanter RK, Szymeczek-Seay CL, Berger AJ & Millhorn DE (1994). Early postnatal development of thyrotropin-releasing hormone (TRH) expression, TRH receptor binding, and TRH responses in neurons of rat brainstem. J Neurosci 14, 821-833.
4. Blier P & El Mansari M (2013). Serotonin and beyond: therapeutics for major depression. Philos Trans R Soc Lond B Biol Sci 368, 20120536.
5. Coates EL, Li A & Nattie EE (1993). Widespread sites of brain stem ventilatory chemoreceptors. J Appl Physiol 75, 5-14.
6. Cream C, Nattie E & Li A (1999). TRH microdialysis into the RTN of the conscious rat increases breathing, metabolism, and temperature. J Appl Physiol 87, 673-682.
7. Dahlstrom A & Fuxe K (1964). Localization of monoamines in the lower brain stem. Experientia 20, 398-399.
8. Dean JB, Bayliss DA, Erickson JT, Lawing WL & Millhorn DE (1990). Depolarization and stimulation of neurons in nucleus tractus solitarii by carbon dioxide does not require chemical synaptic input. Neuroscience 36, 207-216.
9. Dean C, Marson L & Kampine JP (1993). Distribution and co-localization of 5-hydroxytryptamine, thyrotropin-releasing hormone and substance P in the cat medulla. Neuroscience 57, 811-822.
10. 2 dialysis in the retrotrapezoid nucleus. J Appl Physiol 105, 83-90.
11. 2. J Appl Physiol 103, 1780-1788.
12. Doi A, Ramirez JM (2010). State-dependent interactions between excitatory neuromodulators in the neuronal control of breathing. J Neurosci 30, 8251-8262.
13. 2 chemosensitivity, fatal central apnea, and specific loss of parafacial neurons. Proc Natl Acad Sci U S A 105, 1067-1072.
14. Duncan JR, Paterson DS, Hoffman JM, Mokler DJ, Borenstein NS, Belliveau RA, Krous HF, Haas EA, Stanley C, Nattie EE, Trachtenberg FL & Kinney HC (2010). Brainstem serotonergic deficiency in sudden infant death syndrome. JAMA 303, 430-437.
15. Edrey YH, Park TJ, Kang H, Biney A & Buffenstein R (2011). Endocrine function and neurobiology of the longest-living rodent, the naked mole-rat. Exp Gerontol 46, 116-123.
16. Eto K, Kim SK, Nabekura J & Ishibashi H (2011). Taltirelin, a thyrotropin-releasing hormone analog, alleviates mechanical allodynia through activation of descending monoaminergic neurons in persistent inflammatory pain. Brain Res 1414, 50-57.
17. Fukuchi I, Asahi T, Kawashima K, Kawashima Y, Yamamura M, Matsuoka Y & Kinoshita K (1998). Effects of taltirelin hydrate (TA-0910), a novel thyrotropin-releasing hormone analog, on in vivo dopamine release and turnover in rat brain. Arzneimittelforschung 48, 353-359.
18. Hodges MR, Best S & Richerson GB (2011). Altered ventilatory and thermoregulatory control in male and female adult Pet-1 null mice. Respir Physiol Neurobiol 177, 133-140.
19. 2 sensitivity in Brown Norway but not Sprague Dawley rats. Respir Physiol Neurobiol 186(2), 221-228.
20. Hodges MR, Forster HV, Papanek PE, Dwinell MR & Hogan GE (2002). Ventilatory phenotypes among four strains of adult rats. J Appl Physiol 93, 974-983.
21. Hodges MR & Richerson GB (2008). Contributions of 5-HT neurons to respiratory control: Neuromodulatory and trophic effects. Respir Physiol Neurobiol 164, 222-232.
22. Hodges MR, Tattersall G, Harris MB, McEvoy S, Richerson D, Deneris ES, Johnson RL, Chen ZF & Richerson GB (2008). Defects in breathing and thermoregulation in mice with near-complete absence of central serotonin neurons. J Neurosci 28, 2495-2505.
23. Jacobs BL & Azmitia EC (1992). Structure and function of the brain serotonin system. Physiol Rev 72, 165-229.
24. Jensen P, Farago AF, Awatramani RB, Scott MM, Deneris ES & Dymecki SM (2008). Redefining the serotonergic system by genetic lineage. Nat Neurosci 11, 417-419.
25. Kim IS, Ariyaratne HB & Mendis-Handagama SM (2002). Changes in the testis interstitium of Brown Norway rats with aging and effects of luteinizing and thyroid hormones on the aged testes in enhancing the steroidogenic potential. Biol Reprod 66, 1359-1366.
26. Kinney HC & Thach BT (2009). The sudden infant death syndrome. N Engl J Med 361, 795-805.
27. Kriegel AJ, Liu Y, Liu P, Baker MA, Hodges MR, Hua X & Liang M (2013). Characteristics of microRNAs enriched in specific cell types and primary tissue types in solid organs. Physiol Genomics 45, 1144-1156.
28. Krueger KC & Deneris ES (2008). Serotonergic transcription of human FEV reveals direct GATA factor interactions and fate of Pet-1-deficient serotonin neuron precursors. J Neurosci 28, 12748-12758.
29. Ladenson PW, Goldenheim PD & Ridgway EC (1988). Prediction and reversal of blunted ventilatory responsiveness in patients with hypothyroidism. Am J Med 84, 877-883.
30. Liang M, Lee NH, Wang H, Greene AS, Kwitek AE, Kaldunski ML, Luu TV, Frank BC, Bugenhagen S, Jacob HJ & Cowley AW Jr. (2008). Molecular networks in Dahl salt-sensitive hypertension based on transcriptome analysis of a panel of consomic rats. Physiol Genomics 34, 54-64.
31. Liu Y, Liu P, Yang C, Cowley AW Jr. & Liang M (2014). Base-resolution maps of 5-methylcytosine and 5-hydroxymethylcytosine in Dahl S rats: effect of salt and genomic sequence. Hypertension 63, 827-838.
32. Liu C, Maejima T, Wyler SC, Casadesus G, Herlitze S & Deneris ES (2010). Pet-1 is required across different stages of life to regulate serotonergic function. Nat Neurosci 13, 1190-1198.
33. + channel-expressing cells win chemosensory and nonchemosensory brainstem nuclei. J Appl Physiol 117(8), 848-856.
34. Moore RY & Bloom FE (1979). Central catecholamine neuron systems: anatomy and physiology of the norepinephrine and epinephrine systems. Annu Rev Neurosci 2, 113-168.
35. Mouradian GC, Forster HV & Hodges MR (2012). Acute and chronic effects of carotid body denervation (CBD) on ventilation and chemoreflexes in three rat strains. J Physiol 590, 3335-3347.
36. Mulkey DK, Rosin DL, West G, Takakura AC, Moreira TS, Bayliss DA & Guyenet PG (2007). Serotonergic neurons activate chemosensitive retrotrapezoid nucleus neurons by a pH-independent mechanism. J Neurosci 27, 14128-14138.
37. Mulkey DK, Stornetta RL, Weston MC, Simmons JR, Parker A, Bayliss DA & Guyenet PG (2004). Respiratory control by ventral surface chemoreceptor neurons in rats. Nat Neurosci 7, 1360-1369.
38. 2 dialysis in the medullary raphe of the rat increases ventilation in sleep. J Appl Physiol 90, 1247-1257.
39. Nink M, Krause U, Lehnert H, Heuberger W, Huber I, Schulz R, Hommel G & Beyer J (1991). Thyrotropin-releasing hormone has stimulatory effects on ventilation in humans. Acta Physiol Scand 141, 309-318.
40. Olea E, Gonzales C, Gallego R & Giejo-Barrientos ELA (2007). PTU-induced hypothyrodism reduces hypoxic ventilatory drive by impairing carotid body chemosensitivity in adult rats. Acta Physiol 190 (Suppl. 655), 51.
41. Pena F & Ramirez JM (2002). Endogenous activation of serotonin-2A receptors is required for respiratory rhythm generation in vitro. J Neurosci 22, 11055-11064.
42. Ptak K, Yamanishi T, Aungst J, Milescu LS, Zhang R, Richerson GB & Smith JC (2009). Raphé neurons stimulate respiratory circuit activity by multiple mechanisms via endogenously released serotonin and substance P. J Neurosci 29(12), 3720-3737.
43. 2 and acid signaling in chemosensitive neurons. Am J Physiol Cell Physiol 287, C1493-C1526.
44. Ray RS, Corcoran AE, Brust RD, Kim JC, Richerson GB, Nattie E & Dymecki SM (2011). Impaired respiratory and body temperature control upon acute serotonergic neuron inhibition. Science 333, 637-642.
45. Schulz R, Nink M, Werner GS, Andreas S, Kreuzer H, Beyer J & Lehnert H (1996). Human corticotropin-releasing hormone and thyrotropin-releasing hormone modulate the hypercapnic ventilatory response in humans. Eur J Clin Invest 26, 989-995.
46. Shannon DC, Kelly DH & O'Connell K (1977). Abnormal regulation of ventilation in infants at risk for sudden-infant-death syndrome. N Engl J Med 297, 747-750.
47. Stornetta RL, Moreira TS, Takakura AC, Kang BJ, Chang DA, West GH, Brunet JF, Mulkey DK, Bayliss DA & Guyenet PG (2006). Expression of Phox2b by brainstem neurons involved in chemosensory integration in the adult rat. J Neurosci 26, 10305-10314.
48. Strohl KP, Thomas AJ, St JP, Schlenker EH, Koletsky RJ & Schork NJ (1997). Ventilation and metabolism among rat strains. J Appl Physiol 82, 317-323.
49. Suzuki M, Sugano H, Matsumoto K, Yamamura M & Ishida R (1990). Synthesis and central nervous system actions of thyrotropin-releasing hormone analogues containing a dihydroorotic acid moiety. J Med Chem 33, 2130-2137.
50. Taylor NC, Li A & Nattie EE (2005). Medullary serotonergic neurones modulate the ventilatory response to hypercapnia, but not hypoxia in conscious rats. J Physiol 566, 543-557.
51. Wang W, Pizzonia JH & Richerson GB (1998). Chemosensitivity of rat medullary raphe neurones in primary tissue culture. J Physiol 511(Pt 2), 433-450.
52. Wang W, Tiwari JK, Bradley SR, Zaykin RV & Richerson GB (2001). Acidosis-stimulated neurons of the medullary raphe are serotonergic. J Neurophysiol 85, 2224-2235.
53. Weston MC, Stornetta RL & Guyenet PG (2004). Glutamatergic neuronal projections from the marginal layer of the rostral ventral medulla to the respiratory centers in rats. J Comp Neurol 473, 73-85.
54. Wylie CJ, Hendricks TJ, Zhang B, Wang L, Lu P, Leahy P, Fox S, Maeno H & Deneris ES (2010). Distinct transcriptomes define rostral and caudal serotonin neurons. J Neurosci 30, 670-684.
55. Yang C, Stingo FC, Ahn KW, Liu P, Vannucci M, Laud PW, Skelton M, O'Connor P, Kurth T, Ryan RP, Moreno C, Tsaih SW, Patone G, Hummel O, Jacob HJ, Liang M & Cowley AW Jr. (2013). Increased proliferative cells in the medullary thick ascending limb of the loop of Henle in the Dahl salt-sensitive rat. Hypertension 61, 208-215.
56. Zhang X & van den Pol AN (2012). Thyrotropin-releasing hormone (TRH) inhibits melanin-concentrating hormone neurons: implications for TRH-mediated anorexic and arousal actions. J Neurosci 32, 3032-3043.
57. Zwillich CW, Pierson DJ, Hofeldt FD, Lufkin EG & Weil JV (1975). Ventilatory control in myxedema and hypothyroidism. N Engl J Med 292, 662-665.