Cell-Type Specific Expression of Oxytocin and Vasopressin Genes: An Experimental Odyssey

Journal of Neuroendocrinology

Volumn 24, Issue 4, 2012, Pages 528-538

  Gainer, H ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

Cell type specific gene expression; Magnocellular neurones; Phenotype; Transcription factor binding sites; Transcription factors

Indexed keywords

ADENOVIRUS VECTOR; CIS ACTING ELEMENT; GREEN FLUORESCENT PROTEIN; OXYTOCIN; VASOPRESSIN;

BIOINFORMATICS; BRAIN; CELL SPECIFICITY; CELL TYPE; EXON; GENE CONSTRUCT; GENE DELETION; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROMOTER REGION; REPORTER GENE; REVIEW; SUPRAOPTIC NUCLEUS; TRANSCRIPTION INITIATION SITE; TRANSGENE; VIRAL GENE DELIVERY SYSTEM;

ANIMALS; ARGININE VASOPRESSIN; GENE EXPRESSION REGULATION; GENE TRANSFER TECHNIQUES; NEURONS; OXYTOCIN; PROMOTER REGIONS, GENETIC; SUPRAOPTIC NUCLEUS;

EID: 84858813952     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2011.02236.x     Document Type: Review

References (84)

1. Armstrong WE. Morphological and electrophysiological classification of hypothalamic supraoptic neurons. Prog Neurobiol 1995; 47: 291-339.
2. Hatton GI. Oxytocin and vasopressin neurones: vive la difference. J Physiol 1997; 500: 284.
3. Burbach JP, Luckman SM, Murphy D, Gainer H. Gene regulation in the magnocellular hypothalamo-neurohypophysial system. Physiol Rev 2001; 81: 1197-1267.
4. Vandesande F, Dierickx K. Identification of the vasopressin producing and of the oxytocin producing neurons in the hypothalamic magnocellular neurosecretroy system of the rat. Cell Tissue Res 1975; 164: 153-162.
5. Mohr E, Bahnsen U, Kiessling C, Richter D. Expression of the vasopressin and oxytocin genes in rats occurs in mutually exclusive sets of hypothalamic neurons. FEBS Lett 1988; 242: 144-148.
6. Kiyama H, Emson PC. Evidence for the co-expression of oxytocin and vasopressin messenger ribonucleic acids in magnocellular neurosecretory cells: simultaneous demonstration of two neurohypophysin messenger ribonucleic acids by hybridization histochemistry. J Neuroendocrinol 1990; 2: 257-259.
7. Mezey E, Kiss JZ. Coexpression of vasopressin and oxytocin in hypothalamic supraoptic neurons of lactating rats. Endocrinology 1991; 129: 1814-1820.
8. Glasgow E, Kusano K, Chin H, Mezey E, Young WS, Gainer H. Single cell reverse transcription-polymerase chain reaction analysis of rat supraoptic magnocellular neurons: neuropeptide phenotypes and high voltage-gated calcium channel subtypes. Endocrinology 1999; 140: 5391-5401.
9. Xi D, Kusano K, Gainer H. Quantitative analysis of oxytocin and vasopressin messenger ribonucleic acids in single magnocellular neurons isolated from supraoptic nucleus of rat hypothalamus. Endocrinology 1999; 140: 4677-4682.
10. Young WS III, Gainer H. Transgenesis and the study of expression, cellular targeting and function of oxytocin, vasopressin and their receptors. Neuroendocrinology 2003; 78: 185-203.
11. Murphy D, Wells S. In vivo gene transfer studies on the regulation and function of the vasopressin and oxytocin genes. J Neuroendocrinol 2003; 15: 109-125.
12. Ragnarsson U. The nobel trail of Vincent du Vigneaud. J Pept Sci 2007; 13: 431-433.
13. Takabatake Y, Sachs H. Vasopressin biosynthesis. 3. In vitro studies. Endocrinology 1964; 75: 934-942.
14. Sachs H, Takabatake Y. Evidence for a precursor in vasopressin biosynthesis. Endocrinology 1964; 75: 943-948.
15. Steiner DF, Cunningham D, Spigelman L, Aten B. Insulin biosynthesis: evidence for a precursor. Science 1967; 157: 697-700.
16. Gainer H, Sarne Y, Brownstein MJ. Biosynthesis and axonal transport of rat neurohypophysial proteins and peptides. J Cell Biol 1977; 73: 366-381.
17. Gainer H, Sarne Y, Brownstein MJ. Neurophysin biosynthesis: conversion of a putative precursor during axonal transport. Science 1977; 195: 1354-1356.
18. Ivell R, Richter D. Structure and comparison of the oxytocin and vasopressin genes from rat. Proc Natl Acad Sci USA 1984; 81: 2006-2010.
19. Ruppert S, Scherer G, Schutz G. Recent gene conversion involving bovine vasopressin and oxytocin precursor genes suggested by nucleotide sequence. Nature 1984; 308: 554-557.
20. Schmale H, Richter D. Single base deletion in the vasopressin gene is the cause of diabetes insipidus in Brattleboro rats. Nature 1984; 308: 705-709.
21. Hara Y, Battey J, Gainer H. Structure of mouse vasopressin and oxytocin genes. Brain Res Mol Brain Res 1990; 8: 319-324.
22. Mohr E, Schmitz E, Richter D. A single rat genomic DNA fragment encodes both the oxytocin and vasopressin genes separated by 11 kilobases and oriented in opposite transcriptional directions. Biochimie 1988; 70: 649-654.
23. Richter D. Molecular events in expression of vasopressin and oxytocin and their cognate receptors. Am J Physiol 1988; 255: F207-F219.
24. Sausville E, Carney D, Battey J. The human vasopressin gene is linked to the oxytocin gene and is selectively expressed in a cultured lung cancer cell line. J Biol Chem 1985; 260: 10236-10241.
25. Schmitz E, Mohr E, Richter D. Rat vasopressin and oxytocin genes are linked by a long interspersed repeated DNA element (LINE): sequence and transcriptional analysis of LINE. DNA Cell Biol 1991; 10: 81-91.
26. Mohr E, Richter D. Sequence analysis of the promoter region of the rat vasopressin gene. FEBS Lett 1990; 260: 305-308.
27. Kim HH, Wolfe A, Smith GR, Tobet SA, Radovick S. Promoter sequences targeting tissue-specific gene expression of hypothalamic and ovarian gonadotropin-releasing hormone in vivo. J Biol Chem 2002; 277: 5194-5202.
28. Iyer AK, Miller NLG, Yip K, Tran BH, Mellon PL. Enhancers of GnRH transcription embedded in an upstream gene use homeodomain proteins to specify hypothalamic expression. Mol Endocrinol 2010; 24: 1949-1964.
29. Novaira HJ, Yates M, Diaczok D, Kim H, Wolfe A, Radovick S. The gonadotropin-releasing hormone cell-specific element is required for normal puberty and estrous cyclicity. J Neurosci 2011; 31: 3336-3343.
30. Murphy D, Bishop A, Rindi G, Murphy MN, Stamp GW, Hanson J, Polak JM, Hogan B. Mice transgenic for a vasopressin-SV40 hybrid oncogene develop tumors of the endocrine pancreas and the anterior pituitary. A possible model for human multiple endocrine neoplasia type 1. Am J Pathol 1987; 129: 552-566.
31. Stefaneanu L, Rindi G, Horvath E, Murphy D, Polak JM, Kovacs K. Morphology of adenohypophysial tumors in mice transgenic for vasopressin-SV40 hybrid oncogene. Endocrinology 1992; 130: 1789-1795.
32. Ang HL, Ungefroren H, De Bree F, Foo NC, Carter D, Burbach JP, Ivell R, Murphy D. Testicular oxytocin gene expression in seminiferous tubules of cattle and transgenic mice. Endocrinology 1991; 128: 2110-2117.
33. Jeong SW, Castel M, Zhang BJ, Fields RL, Paras P, Arnheiter H, Chin H, Gainer H. Cell-specific expression and subcellular localization of neurophysin-CAT-fusion proteins expressed from oxytocin and vasopressin gene promoter-driven constructs in transgenic mice. Exp Neurol 2001; 171: 255-271.
34. Lee JW, Park JH, Kim KS, Lee EJ, Kim MO, Kim SH, Jeong SW, Kim CW, Lee HJ, Kang KS, Chang KT, Hyun BH, Ryoo ZY. Vasopressin-SV40 T antigen expression in transgenic mice induces brain tumor and lymphoma. Biochem Biophys Res Commun 2003; 302: 785-792.
35. Russo AF, Crenshaw EB III, Lira SA, Simmons DM, Swanson LW, Rosenfeld MG. Neuronal expression of chimeric genes in transgenic mice. Neuron 1988; 1: 311-320.
36. Wilson C, Bellen HJ, Gehring WJ. Position effects on eukaryotic gene expression. Annu Rev Cell Biol 1990; 6: 679-714.
37. Palmiter RD, Sandgren EP, Avarbock MR, Allen DD, Brinster RL. Heterologous introns can enhance expression of transgenes in mice. Proc Natl Acad Sci USA 1991; 88: 478-482.
38. Schoenherr CJ, Anderson DJ. Silencing is golden: negative regulation in the control of neuronal gene transcription. Curr Opin Neurobiol 1995; 5: 566-571.
39. Habener JF, Cwikel BJ, Hermann H, Hammer RE, Palmiter RD, Brinster RL. Metallothionein-vasopressin fusion gene expression in transgenic mice. Nephrogenic diabetes insipidus and brain transcripts localized to magnocellular neurons. J Biol Chem 1989; 264: 18844-18852.
40. Young WS III, Reynolds K, Shepard EA, Gainer H, Castel M. Cell-specific expression of the rat oxytocin gene in transgenic mice. J Neuroendocrinol 1990; 2: 917-925.
41. Belenky M, Castel M, Young WS III, Gainer H, Cohen S. Ultrastructural immunolocalization of rat oxytocin-neurophysin in transgenic mice expressing the rat oxytocin gene. Brain Res 1992; 583: 279-286.
42. Grant FD, Reventos J, Gordon JW, Kawabata S, Miller M, Majzoub JA. Expression of the rat arginine vasopressin gene in transgenic mice. Mol Endocrinol 1993; 7: 659-667.
43. Waller S, Fairhall KM, Xu J, Robinson IC, Murphy D. Neurohypophyseal and fluid homeostasis in transgenic rats expressing a tagged rat vasopressin prepropeptide in hypothalamic neurons. Endocrinology 1996; 137: 5068-5077.
44. Zeng Q, Carter DA, Murphy D. Cell specific expression of a vasopressin transgene in rats. J Neuroendocrinol 1994; 6: 469-477.
45. Young WS III, Iacangelo A, Luo XZ, King C, Duncan K, Ginns EI. Transgenic expression of green fluorescent protein in mouse oxytocin neurones. J Neuroendocrinol 1999; 11: 935-939.
46. Zhang BJ, Kusano K, Zerfas P, Iacangelo A, Young WS III, Gainer H. Targeting of green fluorescent protein to secretory granules in oxytocin magnocellular neurons and its secretion from neurohypophysial nerve terminals in transgenic mice. Endocrinology 2002; 143: 1036-1046.
47. Ueta Y, Fujihara H, Serino R, Dayanithi G, Ozawa H, Matsuda K, Kawata M, Yamada J, Ueno S, Fukuda A, Murphy D. Transgenic expression of enhanced green fluorescent protein enables direct visualization for physiological studies of vasopressin neurons and isolated nerve terminals of the rat. Endocrinology 2005; 146: 406-413.
48. Suzuki H, Kawasaki M, Ohnishi H, Otsubo H, Ohbuchi T, Katoh A, Hashimoto H, Yokoyama T, Fujihara H, Dayanithi G, Murphy D, Nakamura T, Ueta Y. Exaggerated response of a vasopressin-enhanced green fluorescent protein transgene to nociceptive stimulation in the rat. J Neurosci 2009; 29: 13182-13189.
49. Shibata M, Fujihara H, Suzuki H, Ozawa H, Kawata M, Dayanithi G, Murphy D, Ueta Y. Physiological studies of stress responses in the hypothalamus of vasopressin-enhanced green fluorescent protein transgenic rat. J Neuroendocrinol 2007; 19: 285-292.
50. Fields RL, House SB, Gainer H. Regulatory domains in the intergenic region of the oxytocin and vasopressin genes that control their hypothalamus-specific expression in vitro. J Neurosci 2003; 23: 7801-7809.
51. Burger C, Gorbatyuk OS, Velardo MJ, Peden CS, Williams P, Zolotukhin S, Reier PJ, Mandel RJ, Muzyczka N. Recombinant AAV viral vectors pseudotyped with viral capsids from serotypes 1, 2, and 5 display differential efficiency and cell tropism after delivery to different regions of the central nervous system. Mol Ther 2004; 10: 302-317.
52. Osten P, Grinevich V, Cetin A. Viral vectors: a wide range of choices and high levels of service. Handb Exp Pharmacol 2007; 178: 177-202.
53. Papale A, Cerovic M, Brambilla R. Viral vector approaches to modify gene expression in the brain. J Neurosci Methods 2009; 185: 1-14.
54. Lim ST, Airavaara M, Harvey BK. Viral vectors for neurotrophic factor delivery: a gene therapy approach for neurodegenerative diseases of the CNS. Pharmacol Res 2010; 61: 14-26.
55. van den Pol AN, Ozduman K, Wollmann G, Ho WS, Simon I, Yao Y, Rose JK, Ghosh P. Viral strategies for studying the brain, including a replication-restricted self-amplifying delta-G vesicular stomatis virus that rapidly expresses transgenes in brain and can generate a multicolor golgi-like expression. J Comp Neurol 2009; 516: 456-481.
56. Garza JC, Kim CS, Liu J, Zhang W, Lu X-Y. Adeno-associated virus-mediated knockdown of melanocortin-4 receptor in the paraventricular nucleus of the hypothalamus promotes high-fat diet-induced hyperphagia and obesity. J Endocrinol 2008; 197: 471-482.
57. de Backer MW, Fitzsimons CP, Brans MA, Luijendijk MC, Garner KM, Vreugdenhil E, Adan RA. An adeno-associated viral vector transduces the rat hypothalamus and amygdala more efficient than a lentiviral vector. BMC Neurosci 2010; 11: 81.
58. Bienemann AS, Martin-Rendon E, Cosgrave AS, Glover CP, Wong LF, Kingsman SM, Mitrophanous KA, Mazarakis ND, Uney JB. Long-term replacement of a mutated nonfunctional CNS gene: reversal of hypothalamic diabetes insipidus using an EIAV-based lentiviral vector expressing arginine vasopressin. Mol Ther 2003; 7: 588-596.
59. Geddes BJ, Harding TC, Hughes DS, Byrnes AP, Lightman SL, Conde G, Uney JB. Persistent transgene expression in the hypothalamus following stereotaxic delivery of a recombinant adenovirus: suppression of the immune response with cyclosporin. Endocrinology 1996; 137: 5166-5169.
60. Ideno J, Mizukami H, Honda K, Okada T, Hanazono Y, Kume A, Saito T, Ishibashi S, Ozawa K. Persistent phenotypic correction of central diabetes insipidus using adeno-associated virus vector expressing arginine-vasopressin in Brattleboro rats. Mol Ther 2003; 8: 895-902.
61. Chen H, McCarty DM, Bruce AT, Suzuki K. Gene transfer and expression in oligodendrocytes under the control of myelin basic protein transcriptional control region mediated by adeno-associated virus. Gene Ther 1998; 5: 50-58.
62. Geller SF, Ge PS, Visel M, Greenberg KP, Flannery JG. Functional promoter testing using a modified lentiviral transfer vector. Mol Vis 2007; 13: 730-739.
63. Kuroda H, Kutner RH, Bazan NG, Reiser J. A comparative analysis of constitutive and cell-specific promoters in the adult mouse hippocampus using lentivirus vector-mediated gene transfer. J Gene Med 2008; 10: 1163-1175.
64. Li C, Hirsch M, Carter P, Asokan A, Zhou X, Wu Z, Samulski RJ. A small regulatory element from chromosome 19 enhances liver-specific gene expression. Gene Ther 2009; 16: 43-51.
65. Wang B, Li J, Fu FH, Chen C, Zhu X, Zhou L, Jiang X, Xiao X. Construction and analysis of compact muscle-specific promoters for AAV vectors. Gene Ther 2008; 15: 1489-1499.
66. Keir SD, House SB, Li J, Xiao X, Gainer H. Gene transfer into hypothalamic organotypic cultures using an adeno-associated virus vector. Exp Neurol 1999; 160: 313-316.
67. Doherty FC, Schaack JB, Sladek CD. Comparison of the efficacy of four viral vectors for transducing hypothalamic magnocellular neurosecretory neurons in the rat supraoptic nucleus. J Neurosci Methods 2011; 197: 238-248.
68. de Backer MW, Brans MA, Luijendijk MC, Garner KM, Adan RA. Optimization of adeno-associated viral vector-mediated gene delivery to the hypothalamus. Hum Gene Ther 2010; 21: 673-682.
69. Burbach JP. Regulation of gene promoters of hypothalamic peptides. Front Neuroendocrinol 2002; 23: 342-369.
70. Adan RA, Walther N, Cox JJ, Ivell R, Burbach JP. Comparison of the estrogen responsiveness of the rat and bovine oxytocin gene promoters. Biochem Biophys Res Commun 1991; 175: 117-122.
71. Adan RA, Cox JJ, van Kats JP, Burbach JP. Thyroid hormone regulates the oxytocin gene. J Biol Chem 1992; 267: 3771-3777.
72. Adan RA, Cox JJ, Beischlag TV, Burbach JP. A composite hormone response element mediates the transactivation of the rat oxytocin gene by different classes of nuclear hormone receptors. Mol Endocrinol 1993; 7: 47-57.
73. Richard S, Zingg HH. The human oxytocin gene promoter is regulated by estrogens. J Biol Chem 1990; 265: 6098-6103.
74. Richard S, Zingg HH. Identification of cis-acting regulatory elements in the human oxytocin gene promoter. Mol Cell Neurosci 1991; 2: 501-510.
75. Chu K, Zingg HH. Activation of the mouse oxytocin promoter by the orphan receptor RORalpha. J Mol Endocrinol 1999; 23: 337-346.
76. Burbach JP, Lopes da Silva S, Cox JJ, Adan RA, Cooney AJ, Tsai MJ, Tsai SY. Repression of estrogen-dependent stimulation of the oxytocin gene by chicken ovalbumin upstream promoter transcription factor I. J Biol Chem 1994; 269: 15046-15053.
77. Chu K, Zingg HH. The nuclear orphan receptors COUP-TFII and Ear-2 act as silencers of the human oxytocin gene promoter. J Mol Endocrinol 1997; 19: 163-172.
78. Lipkin SM, Nelson CA, Glass CK, Rosenfeld MG. A negative retinoic acid response element in the rat oxytocin promoter restricts transcriptional stimulation by heterologous transactivation domains. Proc Natl Acad Sci USA 1992; 89: 1209-1213.
79. Lopes da Silva S, Burbach JP. The nuclear hormone-receptor family in the brain: classics and orphans. Trends Neurosci 1995; 18: 542-548.
80. Bradley DJ, Towle HC, Young WS III. Spatial and temporal expression of alpha- and beta-thyroid hormone receptor mRNAs, including the beta 2-subtype, in the developing mammalian nervous system. J Neurosci 1992; 12: 2288-2302.
81. Lopes da Silva S, Cox JJ, Jonk LJ, Kruijer W, Burbach JP. Localization of transcripts of the related nuclear orphan receptors COUP-TF I and ARP-1 in the adult mouse brain. Brain Res Mol Brain Res 1995; 30: 131-136.
82. Hindmarch C, Yao S, Beighton G, Paton J, Murphy D. A comprehensive description of the transcriptome of the hypothalamoneurohypophyseal system in euhydrated and dehydrated rats. Proc Natl Acad Sci USA 2006; 103: 1609-1614.
83. Mutsuga N, Shahar T, Verbalis JG, Brownstein MJ, Xiang CC, Bonner RF, Gainer H. Selective gene expression in magnocellular neurons in rat supraoptic nucleus. J Neurosci 2004; 24: 7174-7185.
84. Yue C, Mutsuga N, Verbalis J, Gainer H. Microarray analysis of gene expression in the supraoptic nucleus of normoosmotic and hypoosmotic rats. Cell Mol Neurobiol 2006; 6: 959-978.