Novel potential regulators of maternal adaptations during lactation: Tuberoinfundibular peptide 39 and amylin

Journal of Neuroendocrinology

Volumn 23, Issue 11, 2011, Pages 1002-1008

  Dobolyi, A ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

Hypothalamus; Kisspeptin; Maternal brain; Neuropeptide expression; Rat dams

Indexed keywords

AMYLIN; KISSPEPTIN; NEUROPEPTIDE; PARATHYROID HORMONE RECEPTOR 2; PROLACTIN; TUBEROINFUNDIBULAR PEPTIDE 39; UNCLASSIFIED DRUG;

ADAPTATION; ARCUATE NUCLEUS; DORSOMEDIAL HYPOTHALAMIC NUCLEUS; HUMAN; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; HYPOTHALAMUS; HYPOTHALAMUS PERIVENTRICULAR NUCLEUS; LACTATION; MATERNAL BEHAVIOR; NERVE CELL; NONHUMAN; OVARY CYCLE; PARATHYROID GLAND; PREOPTIC AREA; PRIORITY JOURNAL; PROLACTIN RELEASE; PROTEIN PROTEIN INTERACTION; REVIEW; STRESS; SUCKLING; THALAMUS; TUBEROHYPOPHYSEAL TRACT;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; FEMALE; ISLET AMYLOID POLYPEPTIDE; LACTATION; NEUROPEPTIDES; RATS;

EID: 80054728810     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2011.02127.x     Document Type: Review

References (109)

1. Knobil E, Neill JD. Knobil and Neill's Physiology of Reproduction. San Diego, CA: Academic Press, 2006.
2. Numan M, Insel TR. The Neurobiology of Parental Behavior. New York, NY: Springer, 2003.
3. Neumann ID. Brain mechanisms underlying emotional alterations in the peripartum period in rats. Depress Anxiety 2003; 17: 111-121.
4. Carter CS, Altemus M, Chrousos GP. Neuroendocrine and emotional changes in the post-partum period. Prog Brain Res 2001; 133: 241-249.
5. Neville MC. Lactation and its hormonal control. Neill JD, ed. Physiology of Reproduction. Amsterdam: Academic Press, 2006: 2993-3054.
6. Burbach JPH, Young LJ, Russell JA. Oxytocin: synthesis, secretion, and reproductive functions. Neill JD, ed. Knobil and Neill's Physiology of Reproduction. Oxford: Academic Press, 2006: 3055-3128.
7. McNeilly AS. Suckling and the control of gonadotropin secretion. Neill JD, ed. Knobil and Neill's Physiology of Reproduction. Oxford: Academic Press, 2006: 2511-2552.
8. Smith MS, Grove KL. Integration of the regulation of reproductive function and energy balance: lactation as a model. Front Neuroendocrinol 2002; 23: 225-256.
9. Lamming GE, ed. Marshall's Physiology of Reproduction. London: Chapman & Hall, 1994.
10. Rosenblatt JS. Nonhormonal basis of maternal behavior in the rat. Science 1967; 156: 1512-1514.
11. Fleming AS, Rosenblatt JS. Maternal behavior in the virgin and lactating rat. J Comp Physiol Psychol 1974; 86: 957-972.
12. Numan M, Woodside B. Maternity: neural mechanisms, motivational processes, and physiological adaptations. Behav Neurosci 2010; 124: 715-741.
13. Gray P, Brooks PJ. Effect of lesion location within the medial preoptic-anterior hypothalamic continuum on maternal and male sexual behaviors in female rats. Behav Neurosci 1984; 98: 703-711.
14. Numan M. The role of the medial preoptic area in the regulation of maternal behavior in the rat. Ann NY Acad Sci 1986; 474: 226-233.
15. Lonstein JS, Simmons DA, Swann JM, Stern JM. Forebrain expression of c-fos due to active maternal behaviour in lactating rats. Neuroscience 1998; 82: 267-281.
16. Stack EC, Numan M. The temporal course of expression of c-Fos and Fos B within the medial preoptic area and other brain regions of postpartum female rats during prolonged mother - young interactions. Behav Neurosci 2000; 114: 609-622.
17. Tsukamura H, Maeda K. Non-metabolic and metabolic factors causing lactational anestrus: rat models uncovering the neuroendocrine mechanism underlying the suckling-induced changes in the mother. Prog Brain Res 2001; 133: 187-205.
18. Freeman ME, Kanyicska B, Lerant A, Nagy G. Prolactin: structure, function, and regulation of secretion. Physiol Rev 2000; 80: 1523-1631.
19. Grattan DR, Kokay IC. Prolactin: a pleiotropic neuroendocrine hormone. J Neuroendocrinol 2008; 20: 752-763.
20. Wakerley JB, O'Neill DS, ter Haar MB. Relationship between the suckling-induced release of oxytocin and prolactin in the urethane-anaesthetized lactating rat. J Endocrinol 1978; 76: 493-500.
21. Neumann ID. Brain oxytocin: a key regulator of emotional and social behaviours in both females and males. J Neuroendocrinol 2008; 20: 858-865.
22. Slattery DA, Neumann ID. No stress please! Mechanisms of stress hyporesponsiveness of the maternal brain. J Physiol 2008; 586: 377-385.
23. Terenzi MG, Ingram CD. Oxytocin-induced excitation of neurones in the rat central and medial amygdaloid nuclei. Neuroscience 2005; 134: 345-354.
24. Xu J, Kirigiti MA, Grove KL, Smith MS. Regulation of food intake and gonadotropin-releasing hormone/luteinizing hormone during lactation: role of insulin and leptin. Endocrinology 2009; 150: 4231-4240.
25. Woodside B. Prolactin and the hyperphagia of lactation. Physiol Behav 2007; 91: 375-382.
26. Chen P, Smith MS. Suckling-induced activation of neuronal input to the dorsomedial nucleus of the hypothalamus: possible candidates for mediating the activation of DMH neuropeptide Y neurons during lactation. Brain Res 2003; 984: 11-20.
27. Rondini TA, Donato J Jr, Rodrigues Bde C, Bittencourt JC, Elias CF. Chemical identity and connections of medial preoptic area neurons expressing melanin-concentrating hormone during lactation. J Chem Neuroanat 2010; 39: 51-62.
28. Bosch OJ, Pfortsch J, Beiderbeck DI, Landgraf R, Neumann ID. Maternal behaviour is associated with vasopressin release in the medial preoptic area and bed nucleus of the stria terminalis in the rat. J Neuroendocrinol 2010; 22: 420-429.
29. Numan M, Fleming AS, Levy F. Maternal behavior. Neill JD, ed. Knobil and Neill's Physiology of Reproduction. Oxford: Academic Press, 2006: 1921-1994.
30. Lehman MN, Merkley CM, Coolen LM, Goodman RL. Anatomy of the kisspeptin neural network in mammals. Brain Res 2010; 1364: 90-102.
31. Roa J, Vigo E, Castellano JM, Navarro VM, Fernandez-Fernandez R, Casanueva FF, Dieguez C, Aguilar E, Pinilla L, Tena-Sempere M. Hypothalamic expression of KiSS-1 system and gonadotropin-releasing effects of kisspeptin in different reproductive states of the female Rat. Endocrinology 2006; 147: 2864-2878.
32. Topaloglu AK, Kotan LD, Yuksel B. Neurokinin B signalling in human puberty. J Neuroendocrinol 2010; 22: 765-770.
33. Smith MS, True C, Grove KL. The neuroendocrine basis of lactation-induced suppression of GnRH: role of kisspeptin and leptin. Brain Res 2010; 1364: 139-152.
34. Wojcik-Gladysz A, Polkowska J. Neuropeptide Y - a neuromodulatory link between nutrition and reproduction at the central nervous system level. Reprod Biol 2006; 6(Suppl. 2): 21-28.
35. Pralong FP. Insulin and NPY pathways and the control of GnRH function and puberty onset. Mol Cell Endocrinol 2010; 324: 82-86.
36. Bodnar I, Olah M, Nejad KS, Nagy GM. Neuropeptides and the regulation of prolactin secretion. Kovacs M, Merchenthaler I, eds. Neuropeptides and Peptide Analogs. Kerala: Research Signpost, 2009: 91-100.
37. Lyons DJ, Horjales-Araujo E, Broberger C. Synchronized network oscillations in rat tuberoinfundibular dopamine neurons: switch to tonic discharge by thyrotropin-releasing hormone. Neuron 2010; 65: 217-229.
38. Yamada M, Shibusawa N, Ishii S, Horiguchi K, Umezawa R, Hashimoto K, Monden T, Satoh T, Hirato J, Mori M. Prolactin secretion in mice with thyrotropin-releasing hormone deficiency. Endocrinology 2006; 147: 2591-2596.
39. Fjeldheim AK, Hovring PI, Loseth OP, Johansen PW, Glover JC, Matre V, Olstad OK, Reppe S, Gordeladze JO, Walaas SI, Gautvik KM. Thyrotrophin-releasing hormone receptor 1 and prothyrotrophin-releasing hormone mRNA expression in the central nervous system are regulated by suckling in lactating rats. Eur J Endocrinol 2005; 152: 791-803.
40. Tavakoli-Nezhad M, Arbogast LA. Mu and kappa opioid receptor expression in the mediobasal hypothalamus and effectiveness of selective antagonists on prolactin release during lactation. Neuroscience 2010; 166: 359-367.
41. Arbogast LA, Voogt JL. Endogenous opioid peptides contribute to suckling-induced prolactin release by suppressing tyrosine hydroxylase activity and messenger ribonucleic acid levels in tuberoinfundibular dopaminergic neurons. Endocrinology 1998; 139: 2857-2862.
42. Callahan P, Klosterman S, Prunty D, Tompkins J, Janik J. Immunoneutralization of endogenous opioid peptides prevents the suckling-induced prolactin increase and the inhibition of tuberoinfundibular dopaminergic neurons. Neuroendocrinology 2000; 71: 268-276.
43. Selmanoff M, Gregerson KA. Suckling-induced prolactin release is suppressed by naloxone and simulated by beta-endorphin. Neuroendocrinology 1986; 42: 255-259.
44. Palkovits M. Hypothalamic regulation of food intake. Clin Neurosci 2003; 56: 288-302.
45. Meister B. Neurotransmitters in key neurons of the hypothalamus that regulate feeding behavior and body weight. Physiol Behav 2007; 92: 263-271.
46. Ladyman SR, Augustine RA, Grattan DR. Hormone interactions regulating energy balance during pregnancy. J Neuroendocrinol 2010; 22: 805-817.
47. Crowley WR, Ramoz G, Torto R, Keefe KA, Wang JJ, Kalra SP. Neuroendocrine actions and regulation of hypothalamic neuropeptide Y during lactation. Peptides 2007; 28: 447-452.
48. Usdin TB, Hoare SR, Wang T, Mezey E, Kowalak JA. TIP39: a new neuropeptide and PTH2-receptor agonist from hypothalamus. Nat Neurosci 1999; 2: 941-943.
49. Usdin TB, Dobolyi A. TIP39 (Tuberoinfundibular peptide 39). Squire LR, ed. Encyclopedia of Neuroscience. Oxford: Academic Press, 2009: 1009-1017.
50. Dobolyi A, Palkovits M, Usdin TB. The TIP39-PTH2 receptor system: unique peptidergic cell groups in the brainstem and their interactions with central regulatory mechanisms. Prog Neurobiol 2010; 90: 29-59.
51. Usdin TB. The PTH2 receptor and TIP39: a new peptide-receptor system. Trends Pharmacol Sci 2000; 21: 128-130.
52. Dobolyi A, Ueda H, Uchida H, Palkovits M, Usdin TB. Anatomical and physiological evidence for involvement of tuberoinfundibular peptide of 39 residues in nociception. Proc Natl Acad Sci USA 2002; 99: 1651-1656.
53. Hoare SR, Bonner TI, Usdin TB. Comparison of rat and human parathyroid hormone 2 (PTH2) receptor activation: PTH is a low potency partial agonist at the rat PTH2 receptor. Endocrinology 1999; 140: 4419-4425.
54. Gensure RC, Gardella TJ, Juppner H. Parathyroid hormone and parathyroid hormone-related peptide, and their receptors. Biochem Biophys Res Commun 2005; 328: 666-678.
55. Hoare SR, de Vries G, Usdin TB. Measurement of agonist and antagonist ligand-binding parameters at the human parathyroid hormone type 1 receptor: evaluation of receptor states and modulation by guanine nucleotide. J Pharmacol Exp Ther 1999; 289: 1323-1333.
56. Faber CA, Dobolyi A, Sleeman M, Usdin TB. Distribution of tuberoinfundibular peptide of 39 residues and its receptor, parathyroid hormone 2 receptor, in the mouse brain. J Comp Neurol 2007; 502: 563-583.
57. Dobolyi A, Irwin S, Wang J, Usdin TB. The distribution and neurochemistry of the parathyroid hormone 2 receptor in the rat hypothalamus. Neurochem Res 2006; 31: 227-236.
58. Dobolyi A, Palkovits M, Usdin TB. Expression and distribution of tuberoinfundibular peptide of 39 residues in the rat central nervous system. J Comp Neurol 2003; 455: 547-566.
59. Dobolyi A, Wang J, Irwin S, Usdin TB. Postnatal development and gender-dependent expression of TIP39 in the rat brain. J Comp Neurol 2006; 498: 375-389.
60. Cservenak M, Bodnar I, Usdin TB, Palkovits M, Nagy GM, Dobolyi A. Tuberoinfundibular peptide of 39 residues is activated during lactation and participates in the suckling-induced prolactin release in rat. Endocrinology 2010; 151: 5830-5840.
61. Dobolyi A, Palkovits M, Bodnar I, Usdin TB. Neurons containing tuberoinfundibular peptide of 39 residues project to limbic, endocrine, auditory and spinal areas in rat. Neuroscience 2003; 122: 1093-1105.
62. Palkovits M, Usdin TB, Makara GB, Dobolyi A. Tuberoinfundibular peptide of 39 residues-immunoreactive fibers in the zona incerta and the supraoptic decussations terminate in the neuroendocrine hypothalamus. Neurochem Res 2010; 35: 2078-2085.
63. Szabo FK, Snyder N, Usdin TB, Hoffman GE. A direct neuronal connection between the subparafascicular and ventrolateral arcuate nuclei in non-lactating female rats. Could this pathway play a role in the suckling-induced prolactin release? Endocrine 2010; 37: 62-70.
64. Li C, Chen P, Smith MS. Neural populations in the rat forebrain and brainstem activated by the suckling stimulus as demonstrated by cFos expression. Neuroscience 1999; 94: 117-129.
65. Lin SH, Miyata S, Matsunaga W, Kawarabayashi T, Nakashima T, Kiyohara T. Metabolic mapping of the brain in pregnant, parturient and lactating rats using fos immunohistochemistry. Brain Res 1998; 787: 226-236.
66. Dubois-Dauphin M, Armstrong WE, Tribollet E, Dreifuss JJ. Somatosensory systems and the milk-ejection reflex in the rat. I. Lesions of the mesencephalic lateral tegmentum disrupt the reflex and damage mesencephalic somatosensory connections. Neuroscience 1985; 15: 1111-1129.
67. Tindal JS, Knaggs GS. Determination of the detailed hypothalamic route of the milk-ejection reflex in the guinea-pig. J Endocrinol 1971; 50: 135-152.
68. Tindal JS, Knaggs GS. Pathways in the forebrain of the rat concerned with the release of prolactin. Brain Res 1977; 119: 211-221.
69. Factor EM, Mayer AD, Rosenblatt JS. Peripeduncular nucleus lesions in the rat: I. Effects on maternal aggression, lactation, and maternal behavior during pre- and postpartum periods. Behav Neurosci 1993; 107: 166-185.
70. Hansen S, Kohler C. The importance of the peripeduncular nucleus in the neuroendocrine control of sexual behavior and milk ejection in the rat. Neuroendocrinology 1984; 39: 563-572.
71. Arbogast LA. Tuberoinfundibular peptide of 39 residues (TIP39): a new player in the translation of sensory input to prolactin release during lactation. Endocrinology 2010; 151: 5568-5569.
72. Tsutsui K, Bentley GE, Kriegsfeld LJ, Osugi T, Seong JY, Vaudry H. Discovery and evolutionary history of gonadotrophin-inhibitory hormone and kisspeptin: new key neuropeptides controlling reproduction. J Neuroendocrinol 2010; 22: 716-727.
73. Murphy KG. Kisspeptins: regulators of metastasis and the hypothalamic-pituitary-gonadal axis. J Neuroendocrinol 2005; 17: 519-525.
74. Hameed S, Jayasena CN, Dhillo WS. Kisspeptin and fertility. J Endocrinol 2011; 208: 97-105.
75. Pineda R, Aguilar E, Pinilla L, Tena-Sempere M. Physiological roles of the kisspeptin/GPR54 system in the neuroendocrine control of reproduction. Prog Brain Res 2011; 181: 55-77.
76. Yamada S, Uenoyama Y, Kinoshita M, Iwata K, Takase K, Matsui H, Adachi S, Inoue K, Maeda KI, Tsukamura H. Inhibition of metastin (kisspeptin-54)-GPR54 signaling in the arcuate nucleus-median eminence region during lactation in rats. Endocrinology 2007; 148: 2226-2232.
77. True C. Characterisation of arcuate nucleus kisspeptin/neurokinin B neuronal projections and regulation during lactation in the rat. J Neuroendocrinol 2011; 23: 52-64.
78. Dobolyi A. Central amylin expression and its induction in rat dams. J Neurochem 2009; 111: 1490-1500.
79. LaBuda CJ, Dobolyi A, Usdin TB. Tuberoinfundibular peptide of 39 residues produces anxiolytic and antidepressant actions. Neuroreport 2004; 15: 881-885.
80. Fegley DB, Holmes A, Riordan T, Faber CA, Weiss JR, Ma S, Batkai S, Pacher P, Dobolyi A, Murphy A, Sleeman MW, Usdin TB. Increased fear- and stress-related anxiety-like behavior in mice lacking tuberoinfundibular peptide of 39 residues. Genes Brain Behav 2008; 7: 933-942.
81. Ward HL, Small CJ, Murphy KG, Kennedy AR, Ghatei MA, Bloom SR. The actions of tuberoinfundibular peptide on the hypothalamo-pituitary axes. Endocrinology 2001; 142: 3451-3456.
82. Dimitrov E, Usdin TB. Tuberoinfundibular peptide of 39 residues modulates the mouse hypothalamic-pituitary-adrenal axis via paraventricular glutamatergic neurons. J Comp Neurol 2010; 518: 4375-4394.
83. Walker CD, Lightman SL, Steele MK, Dallman MF. Suckling is a persistent stimulus to the adrenocortical system of the rat. Endocrinology 1992; 130: 115-125.
84. Wimalawansa SJ. Amylin, calcitonin gene-related peptide, calcitonin, and adrenomedullin: a peptide superfamily. Crit Rev Neurobiol 1997; 11: 167-239.
85. Oliver KR, Kane SA, Salvatore CA, Mallee JJ, Kinsey AM, Koblan KS, Keyvan-Fouladi N, Heavens RP, Wainwright A, Jacobson M, Dickerson IM, Hill RG. Cloning, characterization and central nervous system distribution of receptor activity modifying proteins in the rat. Eur J Neurosci 2001; 14: 618-628.
86. Poyner DR, Sexton PM, Marshall I, Smith DM, Quirion R, Born W, Muff R, Fischer JA, Foord SM. International Union of Pharmacology. XXXII. The mammalian calcitonin gene-related peptides, adrenomedullin, amylin, and calcitonin receptors. Pharmacol Rev 2002; 54: 233-246.
87. Hay DL, Christopoulos G, Christopoulos A, Sexton PM. Amylin receptors: molecular composition and pharmacology. Biochem Soc Trans 2004; 32: 865-867.
88. Leffert JD, Newgard CB, Okamoto H, Milburn JL, Luskey KL. Rat amylin: cloning and tissue-specific expression in pancreatic islets. Proc Natl Acad Sci USA 1989; 86: 3127-3130.
89. Lutz TA. Amylinergic control of food intake. Physiol Behav 2006; 89: 465-471.
90. Mulder H, Leckstrom A, Uddman R, Ekblad E, Westermark P, Sundler F. Islet amyloid polypeptide (amylin) is expressed in sensory neurons. J Neurosci 1995; 15: 7625-7632.
91. Gebre-Medhin S, Mulder H, Zhang Y, Sundler F, Betsholtz C. Reduced nociceptive behavior in islet amyloid polypeptide (amylin) knockout mice. Brain Res Mol Brain Res 1998; 63: 180-183.
92. Rushing PA, Hagan MM, Seeley RJ, Lutz TA, Woods SC. Amylin: a novel action in the brain to reduce body weight. Endocrinology 2000; 141: 850-853.
93. Osto M, Wielinga PY, Alder B, Walser N, Lutz TA. Modulation of the satiating effect of amylin by central ghrelin, leptin and insulin. Physiol Behav 2007; 91: 566-572.
94. Lutz TA. The role of amylin in the control of energy homeostasis. Am J Physiol Regul Integr Comp Physiol 2010; 298: R1475-R1484.
95. Potes CS, Lutz TA. Brainstem mechanisms of amylin-induced anorexia. Physiol Behav 2010; 100: 511-518.
96. Rushing PA, Hagan MM, Seeley RJ, Lutz TA, D'Alessio DA, Air EL, Woods SC. Inhibition of central amylin signaling increases food intake and body adiposity in rats. Endocrinology 2001; 142: 5035.
97. Lutz TA. Roles of amylin in satiation, adiposity and brain development. Forum Nutr 2010; 63: 64-74.
98. Sexton PM, Paxinos G, Kenney MA, Wookey PJ, Beaumont K. In vitro autoradiographic localization of amylin binding sites in rat brain. Neuroscience 1994; 62: 553-567.
99. Becskei C, Riediger T, Zund D, Wookey P, Lutz TA. Immunohistochemical mapping of calcitonin receptors in the adult rat brain. Brain Res 2004; 1030: 221-233.
100. Sheward WJ, Lutz EM, Harmar AJ. The expression of the calcitonin receptor gene in the brain and pituitary gland of the rat. Neurosci Lett 1994; 181: 31-34.
101. Simerly RB, Swanson LW. Projections of the medial preoptic nucleus: a Phaseolus vulgaris leucoagglutinin anterograde tract-tracing study in the rat. J Comp Neurol 1988; 270: 209-242.
102. Numan M, Numan MJ. Projection sites of medial preoptic area and ventral bed nucleus of the stria terminalis neurons that express Fos during maternal behavior in female rats. J Neuroendocrinol 1997; 9: 369-384.
103. Sheehan TP, Cirrito J, Numan MJ, Numan M. Using c-Fos immunocytochemistry to identify forebrain regions that may inhibit maternal behavior in rats. Behav Neurosci 2000; 114: 337-352.
104. Riediger T, Zuend D, Becskei C, Lutz TA. The anorectic hormone amylin contributes to feeding-related changes of neuronal activity in key structures of the gut-brain axis. Am J Physiol Regul Integr Comp Physiol 2004; 286: R114-R122.
105. Rushing PA. Central amylin signaling and the regulation of energy homeostasis. Curr Pharm Des 2003; 9: 819-825.
106. Tasker JG, Theodosis DT, Poulain DA. Afferent projections from the mammary glands to the spinal cord in the lactating rat-I. A neuroanatomical study using the transganglionic transport of horseradish peroxidase-wheatgerm agglutinin. Neuroscience 1986; 19: 495-509.
107. Dubois-Dauphin M, Armstrong WE, Tribollet E, Dreifuss JJ. Somatosensory systems and the milk-ejection reflex in the rat. II. The effects of lesions in the ventroposterior thalamic complex, dorsal columns and lateral cervical nucleus-dorsolateral funiculus. Neuroscience 1985; 15: 1131-1140.
108. Stern JM, Yu YL, Crockett DP. Dorsolateral columns of the spinal cord are necessary for both suckling-induced neuroendocrine reflexes and the kyphotic nursing posture in lactating rats. Brain Res 2002; 947: 110-121.
109. Tindal JS, Knaggs GS. An ascending pathway for release of prolactin in the brain of the rabbit. J Endocrinol 1969; 45: 111-120.