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Abstract
This list is an update of the bibliography published in 2001. The dramatic development of the field is reflected in the growth of the previous list of 29 references to more than 150 in the space of 4 years. There are now mutant mouse strains for almost every nuclear receptor gene in the mammalian genome, with some genes having multiple different alleles. These include selective deletions of alternative products of a given gene and conditional or knock-in alleles. Most of the strains have been derived by targeted mutagenesis, although a few spontaneous mutations have also been identified. The list offers a glimpse into the remarkable role of this gene family with functions in reproduction, embryogenesis, metabolism, cardiac function, behavior, and the senses, amongst other areas.
For each gene, systematic nomenclature is used in addition to commonly used names (see Cell 97:161, 1999; or Nuclear Receptor Signaling Atlas, www.nursa.org). The gene symbols are in italics. The Mouse Genome Informatics web site (http://www.informatics.jax.org/) provides valuable information on nomenclature, alleles, and background strains.
The goal in the current list is limited, restricting the references to first reports of new mutations or combinations of mutations. There is scope to extend the list in the future to include many additional studies of these mouse strains. Human mutations or nonmurine models such as Drosophila could also be included. It is recognized that the present list may not be complete, and apologies are offered for any omissions. Comments by K. Parker, K. Korach, F. Gonzalez, J. Samarut, M-J. Tsai, S. Tsai, and V. Giguère are gratefully acknowledged. Additions or suggestions are welcomed.
Nuclear Hormone Receptors
Androgen Receptors Nr3c4
AR/Ar/Nr3c4
De Gendt K, Swinnen JV, Saunders PT, Schoonjans L, Dewerchin M, Devos A, Tan K, Atanassova N, Claessens F, Lecureuil C, Heyns W, Carmeliet P, Guillou F, Sharpe RM, Verhoeven G 2004 A Sertoli cell-selective knockout of the androgen receptor causes spermatogenic arrest in meiosis. Proc Natl Acad Sci USA 101:1327–1332
Holdcraft RW, Braun RE 2004 Androgen receptor function is required in Sertoli cells for the terminal differentiation of haploid spermatids. Development 131:459–467
Sato T, Matsumoto T, Yamada T, Watanabe T, Kawano H, Kato S 2003 Late onset of obesity in male androgen receptor-deficient (AR KO) mice. Biochem Biophys Res Commun 300:167–171[CrossRef][Medline]
Yeh S, Tsai MY, Xu Q, Mu XM, Lardy H, Huang KE, Lin H, Yeh SD, Altuwaijri S, Zhou X, Xing L, Boyce BF, Hung MC, Zhang S, Gan L, Chang C 2002 Generation and characterization of androgen receptor knockout (ARKO) mice: an in vivo model for the study of androgen functions in selective tissues. Proc Natl Acad Sci USA 99:13498–13503
Lyon MF, Hawkes SG 1970 X-linked gene for testicular feminization in the mouse. Nature 227:1217–1219[CrossRef][Medline]
Charest NJ, Zhou ZX, Lubahn DB, Olsen KL, Wilson EM, French FS 1991 A frameshift mutation destabilizes androgen receptor messenger RNA in the Tfm mouse. Mol Endocrinol 5:573–581
Politch JA, Fox TO, Houben P, Bullock L, Lovell D 1988 TfmLac: a second isolation of testicular feminization in mice. Biochem Genet 26:213–221[CrossRef][Medline]
Tanaka S, Kaneko T, Moriyama T, Matsuzawa A 1994 A new testicular feminization mutation found in C57BL/6J mice. Lab Anim 28:262–264
Estrogen Receptors Nr3a
ER
/Esr1/Nr3a1
Lubahn DB, Moyer JS, Golding TS, Couse JF, Korach KS, Smithies O 1993 Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci USA 90:11162–11166
Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P, Mark M 2000 Effect of single and compound knockouts of estrogen receptors (ER) and ß (ERß) on mouse reproductive phenotypes. Development 127:4277–4291[Abstract]
ERß knock-in/point mutations
Jakacka M, Ito M, Martinson F, Ishikawa T, Lee EJ, Jameson JL 2002 An estrogen receptor (ER) deoxyribonucleic acid-binding domain knock-in mutation provides evidence for nonclassical ER pathway signaling in vivo. Mol Endocrinol 16:2188–2201
Swope DL, Castranio T, Harrell JC, Mishina Y, Korach KS 2002 AF-2 knock-in mutation of estrogen receptor : Cre-loxP excision of a PGK-neo cassette from the 3' UTR. Genesis 32:99–101[CrossRef][Medline]
ERß/Esr2/Nr3a2
Krege JH, Hodgin JB, Couse JF, Enmark E, Warner M, Mahler JF, Sar M, Korach KS, Gustafsson JA, Smithies O 1998 Generation and reproductive phenotypes of mice lacking estrogen receptor ß. Proc Natl Acad Sci USA 95:15677–15682
Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P, Mark M 2000 Effect of single and compound knockouts of estrogen receptors (ER) and ß (ERß) on mouse reproductive phenotypes. Development 127:4277–4291[Abstract]
ER and ERß combinations
Couse JF, Hewitt SC, Bunch DO, Sar M, Walker VR, Davis BJ, Korach KS 1999 Postnatal sex reversal of the ovaries in mice lacking estrogen receptors and ß. Science 286:2328–2331
Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P, Mark M 2000 Effect of single and compound knockouts of estrogen receptors (ER) and ß (ERß) on mouse reproductive phenotypes. Development 127:4277–4291[Abstract]
Glucocorticoid Receptors Nr3c1
GR/Nr3c1
Cole TJ, Blendy JA, Monaghan AP, Krieglstein K, Schmid W, Aguzzi A, Fantuzzi G, Hummler E, Unsicker K, Schutz G 1995 Targeted disruption of the glucocorticoid receptor gene blocks adrenergic chromaffin cell development and severely retards lung maturation. Genes Dev 9:1608–1621
Finotto S, Krieglstein K, Schober A, Deimling F, Lindner K, Bruhl B, Beier K, Metz J, Garcia-Arraras JE, Roig-Lopez JL, Monaghan P, Schmid W, Cole TJ, Kellendonk C, Tronche F, Schutz G, Unsicker K 1999 Analysis of mice carrying targeted mutations of the glucocorticoid receptor gene argues against an essential role of glucocorticoid signalling for generating adrenal chromaffin cells. Development 126:2935–2944[Abstract]
Tronche F, Kellendonk C, Kretz O, Gass P, Anlag K, Orban PC, Bock R, Klein R, Schutz G 1999 Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat Genet 23:99–103[CrossRef][Medline]
Brewer JA, Sleckman BP, Swat W, Muglia LJ 2002 Green fluorescent protein-glucocorticoid receptor knockin mice reveal dynamic receptor modulation during thymocyte development. J Immunol 169:1309–1318
Brewer JA, Kanagawa O, Sleckman BP, Muglia LJ 2002 Thymocyte apoptosis induced by T cell activation is mediated by glucocorticoids in vivo. J Immunol 169:1837–1843
Brewer JA, Khor B, Vogt SK, Muglia LM, Fujiwara H, Haegele KE, Sleckman BP, Muglia LJ 2003 T-cell glucocorticoid receptor is required to suppress COX-2-mediated lethal immune activation. Nat Med 9:1318–1322[CrossRef][Medline]
Tronche F, Opherk C, Moriggl R, Kellendonk C, Reimann A, Schwake L, Reichardt HM, Stangl K, Gau D, Hoeflich A, Beug H, Schmid W, Schutz G 2004 Glucocorticoid receptor function in hepatocytes is essential to promote postnatal body growth. Genes Dev 18:492–497
Wintermantel TM, Bock D, Fleig V, Greiner EF, Schutz G 2005 The epithelial glucocorticoid receptor is required for the normal timing of cell proliferation during mammary lobuloalveolar development but is dispensable for milk production. Mol Endocrinol 19:340–349
GR knock-in/point mutations
Reichardt HM, Kaestner KH, Tuckermann J, Kretz O, Wessely O, Bock R, Gass P, Schmid W, Herrlich P, Angel P, Schutz G 1998 DNA binding of the glucocorticoid receptor is not essential for survival. Cell 93:531–541[CrossRef][Medline]
Mineralocorticoid Receptors, Aldosterone Receptors Nr3c2
MR/Nr3c2
Berger S, Bleich M, Schmid W, Cole TJ, Peters J, Watanabe H, Kriz W, Warth R, Greger R, Schutz G 1998 Mineralocorticoid receptor knockout mice: pathophysiology of Na+ metabolism. Proc Natl Acad Sci USA 95:9424–9429
Progesterone Receptors Nr3c3
PR/Pgr/Nr3c3
Lydon JP, DeMayo FJ, Funk CR, Mani SK, Hughes AR, Montgomery CA, Jr., Shyamala G, Conneely OM, O’Malley BW 1995 Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev 9:2266–2278
Ismail PM, Li J, DeMayo FJ, O’Malley BW, Lydon JP 2002 A novel LacZ reporter mouse reveals complex regulation of the progesterone receptor promoter during mammary gland development. Mol Endocrinol 16:2475–2489
Soyal SM, Mukherjee A, Lee KY, Li J, Li H, DeMayo FJ, Lydon JP 2005 Cre-mediated recombination in cell lineages that express the progesterone receptor. Genesis 41:58–66[CrossRef][Medline]
PR-A
Mulac-Jericevic B, Mullinax RA, DeMayo FJ, Lydon JP, Conneely OM 2000 Subgroup of reproductive functions of progesterone mediated by progesterone receptor-B isoform. Science 289:1751–1754
PR-B
Mulac-Jericevic B, Lydon JP, DeMayo FJ, Conneely OM 2003 Defective mammary gland morphogenesis in mice lacking the progesterone receptor B isoform. Proc Natl Acad Sci USA 100:9744–9749
Retinoid Receptors
Retinoic acid receptors Nr1b
RAR/Rara/Nr1b1
RAR or RAR1
Lufkin T, Lohnes D, Mark M, Dierich A, Gorry P, Gaub MP, LeMeur M, Chambon P 1993 High postnatal lethality and testis degeneration in retinoic acid receptor mutant mice. Proc Natl Acad Sci USA 90:7225–7229
Chapellier B, Mark M, Garnier JM, LeMeur M, Chambon P, Ghyselinck NB 2002 A conditional floxed (loxP-flanked) allele for the retinoic acid receptor (RAR) gene. Genesis 32:87–90[CrossRef][Medline]
Li E, Sucov HM, Lee KF, Evans RM, Jaenisch R 1993 Normal development and growth of mice carrying a targeted disruption of the 1 retinoic acid receptor gene. Proc Natl Acad Sci USA 90:1590–1594
RARß/Rarb/Nr1b2
RARß2
Mendelsohn C, Mark M, Dolle P, Dierich A, Gaub MP, Krust A, Lampron C, Chambon P 1994 Retinoic acid receptor ß2 (RAR ß2) null mutant mice appear normal. Dev Biol 166:246–258[CrossRef][Medline]
RARß
Luo J, Pasceri P, Conlon RA, Rossant J, Giguere V 1995 Mice lacking all isoforms of retinoic acid receptor ß develop normally and are susceptible to the teratogenic effects of retinoic acid. Mech Dev 53:61–71[CrossRef][Medline]
Ghyselinck NB, Dupe V, Dierich A, Messaddeq N, Garnier JM, Rochette-Egly C, Chambon P, Mark M 1997 Role of the retinoic acid receptor ß (RARß) during mouse development. Int J Dev Biol 41:425–447[Medline]
Chapellier B, Mark M, Bastien J, Dierich A, LeMeur M, Chambon P, Ghyselinck NB 2002 A conditional floxed (loxP-flanked) allele for the retinoic acid receptor ß (RARß) gene. Genesis 32:91–94[CrossRef][Medline]
RAR
/Rarg/Nr1b3
RAR or RAR2
Lohnes D, Kastner P, Dierich A, Mark M, LeMeur M, Chambon P 1993 Function of retinoic acid receptor in the mouse. Cell 73:643–658[CrossRef][Medline]
Look J, Landwehr J, Bauer F, Hoffmann AS, Bluethmann H, LeMotte P 1995 Marked resistance of RAR -deficient mice to the toxic effects of retinoic acid. Am J Physiol 269:E91–E98
Chapellier B, Mark M, Garnier JM, Dierich A, Chambon P, Ghyselinck NB 2002 A conditional floxed (loxP-flanked) allele for the retinoic acid receptor (RAR) gene. Genesis 32:95–98[CrossRef][Medline]
RAR1
Subbarayan V, Kastner P, Mark M, Dierich A, Gorry P, Chambon P 1997 Limited specificity and large overlap of the functions of the mouse RAR 1 and RAR 2 isoforms. Mech Dev 66:131–142[CrossRef][Medline]
RAR knock-in/point mutation
Iulianella A, Lohnes D 2002 Chimeric analysis of retinoic acid receptor function during cardiac looping. Dev Biol 247:62–75[CrossRef][Medline]
RAR, RARß, and RAR combinations
Lohnes D, Mark M, Mendelsohn C, Dolle P, Dierich A, Gorry P, Gansmuller A, Chambon P 1994 Function of the retinoic acid receptors (RARs) during development (I). Craniofacial and skeletal abnormalities in RAR double mutants. Development 120:2723–2748[Abstract]
Ghyselinck NB, Dupe V, Dierich A, Messaddeq N, Garnier JM, Rochette-Egly C, Chambon P, Mark M 1997 Role of the retinoic acid receptor ß (RARß) during mouse development. Int J Dev Biol 41:425–447[Medline]
Retinoid X Receptors Nr2b
RXR/Rxra/Nr2b1
RXR or RXR1
Kastner P, Grondona JM, Mark M, Gansmuller A, LeMeur M, Decimo D, Vonesch JL, Dolle P, Chambon P 1994 Genetic analysis of RXR developmental function: convergence of RXR and RAR signaling pathways in heart and eye morphogenesis. Cell 78:987–1003[CrossRef][Medline]
Sucov HM, Dyson E, Gumeringer CL, Price J, Chien KR, Evans RM 1994 RXR mutant mice establish a genetic basis for vitamin A signaling in heart morphogenesis. Genes Dev 8:1007–1018
Chen J, Kubalak SW, Chien KR 1998 Ventricular muscle-restricted targeting of the RXR gene reveals a non-cell-autonomous requirement in cardiac chamber morphogenesis. Development 125:1943–1949[Abstract]
Li M, Indra AK, Warot X, Brocard J, Messaddeq N, Kato S, Metzger D, Chambon P 2000 Skin abnormalities generated by temporally controlled RXR mutations in mouse epidermis. Nature 407:633–636[CrossRef][Medline]
Li M, Chiba H, Warot X, Messaddeq N, Gerard C, Chambon P, Metzger D 2001 RXR- ablation in skin keratinocytes results in alopecia and epidermal alterations. Development 128:675–688[Abstract]
RXR knock-in/point mutations
Mascrez B, Mark M, Dierich A, Ghyselinck NB, Kastner P, Chambon P 1998 The RXR ligand-dependent activation function 2 (AF-2) is important for mouse development. Development 125:4691–4707[Abstract]
Mascrez B, Mark M, Krezel W, Dupe V, LeMeur M, Ghyselinck NB, Chambon P 2001 Differential contributions of AF-1 and AF-2 activities to the developmental functions of RXR. Development 128:2049–2062
RXRß/Rxrb/Nr2b2
Kastner P, Mark M, Leid M, Gansmuller A, Chin W, Grondona JM, Decimo D, Krezel W, Dierich A, Chambon P 1996 Abnormal spermatogenesis in RXRß mutant mice. Genes Dev 10:80–92
RXR/Rxrg/Nr2b3
RXR
Krezel W, Dupe V, Mark M, Dierich A, Kastner P, Chambon P 1996 RXR null mice are apparently normal and compound RXR+/–/RXRß–/–/RXR–/– mutant mice are viable. Proc Natl Acad Sci USA 93:9010–9014
Chiang MY, Misner D, Kempermann G, Schikorski T, Giguere V, Sucov HM, Gage FH, Stevens CF, Evans RM 1998 An essential role for retinoid receptors RARß and RXR in long-term potentiation and depression. Neuron 21:1353–1361[CrossRef][Medline]
RXR1
Saga Y, Kobayashi M, Ohta H, Murai N, Nakai N, Oshima M, Taketo MM 1999 Impaired extrapyramidal function caused by the targeted disruption of retinoid X receptor RXR1 isoform. Genes Cells 4:219–228[Abstract]
RXR, RXRß, and RXR combinations
Krezel W, Ghyselinck N, Samad TA, Dupe V, Kastner P, Borrelli E, Chambon P 1998 Impaired locomotion and dopamine signaling in retinoid receptor mutant mice. Science 279:863–867
Wendling O, Chambon P, Mark M 1999 Retinoid X receptors are essential for early mouse development and placentogenesis. Proc Natl Acad Sci USA 96:547–551
Thyroid Hormone Receptors Nr1a
TR/Thra/Nr1a1
TR1
Wikstrom L, Johansson C, Salto C, Barlow C, Campos Barros A, Baas F, Forrest D, Thoren P, Vennstrom B 1998 Abnormal heart rate and body temperature in mice lacking thyroid hormone receptor 1. EMBO J 17:455–461[CrossRef][Medline]
TR2
Salto C, Kindblom JM, Johansson C, Wang Z, Gullberg H, Nordstrom K, Mansen A, Ohlsson C, Thoren P, Forrest D, Vennstrom B 2001 Ablation of TR2 and a concomitant overexpression of 1 yields a mixed hypo- and hyperthyroid phenotype in mice. Mol Endocrinol 15:2115–2128
TR products
Fraichard A, Chassande O, Plateroti M, Roux JP, Trouillas J, Dehay C, Legrand C, Gauthier K, Kedinger M, Malaval L, Rousset B, Samarut J 1997 The T3R gene encoding a thyroid hormone receptor is essential for post-natal development and thyroid hormone production. EMBO J 16:4412–4420[CrossRef][Medline]
Gauthier K, Plateroti M, Harvey CB, Williams GR, Weiss RE, Refetoff S, Willott JF, Sundin V, Roux JP, Malaval L, Hara M, Samarut J, Chassande O 2001 Genetic analysis reveals different functions for the products of the thyroid hormone receptor locus. Mol Cell Biol 21:4748–4760
Plateroti M, Gauthier K, Domon-Dell C, Freund JN, Samarut J, Chassande O 2001 Functional interference between thyroid hormone receptor (TR) and natural truncated TR
isoforms in the control of intestine development. Mol Cell Biol 21:4761–4772
TR knock-in/point mutations
Kaneshige M, Suzuki H, Kaneshige K, Cheng J, Wimbrow H, Barlow C, Willingham MC, Cheng S 2001 A targeted dominant negative mutation of the thyroid hormone 1 receptor causes increased mortality, infertility, and dwarfism in mice. Proc Natl Acad Sci USA 98:15095–15100
Tinnikov A, Nordstrom K, Thoren P, Kindblom JM, Malin S, Rozell B, Adams M, Rajanayagam O, Pettersson S, Ohlsson C, Chatterjee K, Vennstrom B 2002 Retardation of post-natal development caused by a negatively acting thyroid hormone receptor 1. EMBO J 21:5079–5087[CrossRef][Medline]
Liu YY, Schultz JJ, Brent GA 2003 A thyroid hormone receptor gene mutation (P398H) is associated with visceral adiposity and impaired catecholamine-stimulated lipolysis in mice. J Biol Chem 278:38913–38920
TRß/Thrb/Nr1a2
TRß
Forrest D, Hanebuth E, Smeyne RJ, Everds N, Stewart CL, Wehner JM, Curran T 1996 Recessive resistance to thyroid hormone in mice lacking thyroid hormone receptor ß: evidence for tissue-specific modulation of receptor function. EMBO J 15:3006–3015[Medline]
Gauthier K, Chassande O, Plateroti M, Roux JP, Legrand C, Pain B, Rousset B, Weiss R, Trouillas J, Samarut J 1999 Different functions for the thyroid hormone receptors TR and TRß in the control of thyroid hormone production and post-natal development. EMBO J 18:623–631[CrossRef][Medline]
Shibusawa N, Hashimoto K, Nikrodhanond AA, Liberman MC, Applebury ML, Liao XH, Robbins JT, Refetoff S, Cohen RN, Wondisford FE 2003 Thyroid hormone action in the absence of thyroid hormone receptor DNA-binding in vivo. J Clin Invest 112:588–597[CrossRef][Medline]
Suzuki H, Zhang XY, Forrest D, Willingham MC, Cheng SY 2003 Marked potentiation of the dominant negative action of a mutant thyroid hormone receptor ß in mice by the ablation of one wild-type ß allele. Mol Endocrinol 17:895–907
TRß2
Abel ED, Boers ME, Pazos-Moura C, Moura E, Kaulbach H, Zakaria M, Lowell B, Radovick S, Liberman MC, Wondisford F 1999 Divergent roles for thyroid hormone receptor ß isoforms in the endocrine axis and auditory system. J Clin Invest 104:291–300[Medline]
Ng L, Hurley JB, Dierks B, Srinivas M, Salto C, Vennstrom B, Reh TA, Forrest D 2001 A thyroid hormone receptor that is required for the development of green cone photoreceptors. Nat Genet 27:94–98[Medline]
TRß knock-in/point mutations
Kaneshige M, Kaneshige K, Zhu X, Dace A, Garrett L, Carter TA, Kazlauskaite R, Pankratz DG, Wynshaw-Boris A, Refetoff S, Weintraub B, Willingham MC, Barlow C, Cheng S 2000 Mice with a targeted mutation in the thyroid hormone ß receptor gene exhibit impaired growth and resistance to thyroid hormone. Proc Natl Acad Sci USA 97:13209–13214
Hashimoto K, Curty FH, Borges PP, Lee CE, Abel ED, Elmquist JK, Cohen RN, Wondisford FE 2001 An unliganded thyroid hormone receptor causes severe neurological dysfunction. Proc Natl Acad Sci USA 98:3998–4003
Shibusawa N, Hashimoto K, Nikrodhanond AA, Liberman MC, Applebury ML, Liao XH, Robbins JT, Refetoff S, Cohen RN, Wondisford FE 2003 Thyroid hormone action in the absence of thyroid hormone receptor DNA-binding in vivo. J Clin Invest 112:588–597[CrossRef][Medline]
Ortiga-Carvalho TM, Shibusawa N, Nikrodhanond A, Oliveira KJ, Machado DS, Liao XH, Cohen RN, Refetoff S, Wondisford FE 2005 Negative regulation by thyroid hormone receptor requires an intact coactivator-binding surface. J Clin Invest 115:2517–2523[CrossRef][Medline]
TRß/ TR combinations
Gothe S, Wang Z, Ng L, Kindblom JM, Barros AC, Ohlsson C, Vennstrom B, Forrest D 1999 Mice devoid of all known thyroid hormone receptors are viable but exhibit disorders of the pituitary-thyroid axis, growth, and bone maturation. Genes Dev 13:1329–1341
Gauthier K, Chassande O, Plateroti M, Roux JP, Legrand C, Pain B, Rousset B, Weiss R, Trouillas J, Samarut J 1999 Different functions for the thyroid hormone receptors TR and TRß in the control of thyroid hormone production and post-natal development. EMBO J 18:623–631[CrossRef][Medline]
Ng L, Rusch A, Amma LL, Nordstrom K, Erway LC, Vennstrom B, Forrest D 2001 Suppression of the deafness and thyroid dysfunction in Thrb-null mice by an independent mutation in the Thra thyroid hormone receptor gene. Hum Mol Genet 10:2701–2708
Suzuki H, Cheng SY 2003 Compensatory role of thyroid hormone receptor (TR) 1 in resistance to thyroid hormone: study in mice with a targeted mutation in the TRß gene and deficient in TR1. Mol Endocrinol 17:1647–1655
Vitamin D Receptors Nr1i1
VDR/Vdr/Nr1i1
Li YC, Pirro AE, Amling M, Delling G, Baron R, Bronson R, Demay MB 1997 Targeted ablation of the vitamin D receptor: an animal model of vitamin D-dependent rickets type II with alopecia. Proc Natl Acad Sci USA 94:9831–9835
Yoshizawa T, Handa Y, Uematsu Y, Takeda S, Sekine K, Yoshihara Y, Kawakami T, Arioka K, Sato H, Uchiyama Y, Masushige S, Fukamizu A, Matsumoto T, Kato S 1997 Mice lacking the vitamin D receptor exhibit impaired bone formation, uterine hypoplasia and growth retardation after weaning. Nat Genet 16:391–396[CrossRef][Medline]
Erben RG, Soegiarto DW, Weber K, Zeitz U, Lieberherr M, Gniadecki R, Moller G, Adamski J, Balling R 2002 Deletion of deoxyribonucleic acid binding domain of the vitamin D receptor abrogates genomic and nongenomic functions of vitamin D. Mol Endocrinol 16:1524–1537
Van Cromphaut SJ, Dewerchin M, Hoenderop JG, Stockmans I, Van Herck E, Kato S, Bindels RJ, Collen D, Carmeliet P, Bouillon R, Carmeliet G 2001 Duodenal calcium absorption in vitamin D receptor-knockout mice: functional and molecular aspects. Proc Natl Acad Sci USA 98:13324–13329
Orphan/Adopted Orphan Receptors
Peroxisome proliferator-activated receptors Nr1c
PPAR/Ppara/Nr1c1
Lee SS, Pineau T, Drago J, Lee EJ, Owens JW, Kroetz DL, Fernandez-Salguero PM, Westphal H, Gonzalez FJ 1995 Targeted disruption of the isoform of the peroxisome proliferator-activated receptor gene in mice results in abolishment of the pleiotropic effects of peroxisome proliferators. Mol Cell Biol 15:3012–3022
PPAR
or PPARß/Ppard or Pparb/Nr1c2
Peters JM, Lee SS, Li W, Ward JM, Gavrilova O, Everett C, Reitman ML, Hudson LD, Gonzalez FJ 2000 Growth, adipose, brain, and skin alterations resulting from targeted disruption of the mouse peroxisome proliferator-activated receptor ß(). Mol Cell Biol 20:5119–5128
Barak Y, Liao D, He W, Ong ES, Nelson MC, Olefsky JM, Boland R, Evans RM 2002 Effects of peroxisome proliferator-activated receptor on placentation, adiposity, and colorectal cancer. Proc Natl Acad Sci USA 99:303–308
Michalik L, Desvergne B, Tan NS, Basu-Modak S, Escher P, Rieusset J, Peters JM, Kaya G, Gonzalez FJ, Zakany J, Metzger D, Chambon P, Duboule D, Wahli W 2001 Impaired skin wound healing in peroxisome proliferator-activated receptor (PPAR) and PPARß mutant mice. J Cell Biol 154:799–814
PPAR/Pparg/Nr1c3
PPAR
Barak Y, Nelson MC, Ong ES, Jones YZ, Ruiz-Lozano P, Chien KR, Koder A, Evans RM 1999 PPAR is required for placental, cardiac, and adipose tissue development. Mol Cell 4:585–595[CrossRef][Medline]
Kubota N, Terauchi Y, Miki H, Tamemoto H, Yamauchi T, Komeda K, Satoh S, Nakano R, Ishii C, Sugiyama T, Eto K, Tsubamoto Y, Okuno A, Murakami K, Sekihara H, Hasegawa G, Naito M, Toyoshima Y, Tanaka S, Shiota K, Kitamura T, Fujita T, Ezaki O, Aizawa S, Kadowaki T, et al. 1999 PPAR mediates high-fat diet-induced adipocyte hypertrophy and insulin resistance. Mol Cell 4:597–609[CrossRef][Medline]
Rieusset J, Seydoux J, Anghel SI, Escher P, Michalik L, Soon Tan N, Metzger D, Chambon P, Wahli W, Desvergne B 2004 Altered growth in male peroxisome proliferator-activated receptor (PPAR) heterozygous mice: involvement of PPAR in a negative feedback regulation of growth hormone action. Mol Endocrinol 18:2363–2377
Akiyama TE, Sakai S, Lambert G, Nicol CJ, Matsusue K, Pimprale S, Lee YH, Ricote M, Glass CK, Brewer Jr HB, Gonzalez FJ 2002 Conditional disruption of the peroxisome proliferator-activated receptor gene in mice results in lowered expression of ABCA1, ABCG1, and apoE in macrophages and reduced cholesterol efflux. Mol Cell Biol 22:2607–2619
Imai T, Takakuwa R, Marchand S, Dentz E, Bornert JM, Messaddeq N, Wendling O, Mark M, Desvergne B, Wahli W, Chambon P, Metzger D 2004 Peroxisome proliferator-activated receptor is required in mature white and brown adipocytes for their survival in the mouse. Proc Natl Acad Sci USA 101:4543–4547
Jones JR, Shelton KD, Guan Y, Breyer MD, Magnuson MA 2002 Generation and functional confirmation of a conditional null PPAR allele in mice. Genesis 32:134–137[CrossRef][Medline]
He W, Barak Y, Hevener A, Olson P, Liao D, Le J, Nelson M, Ong E, Olefsky JM, Evans RM 2003 Adipose-specific peroxisome proliferator-activated receptor knockout causes insulin resistance in fat and liver but not in muscle. Proc Natl Acad Sci USA 100:15712–15717
PPAR2
Koutnikova H, Cock TA, Watanabe M, Houten SM, Champy MF, Dierich A, Auwerx J 2003 Compensation by the muscle limits the metabolic consequences of lipodystrophy in PPAR hypomorphic mice. Proc Natl Acad Sci USA 100:14457–14462
Zhang J, Fu M, Cui T, Xiong C, Xu K, Zhong W, Xiao Y, Floyd D, Liang J, Li E, Song Q, Chen YE 2004 Selective disruption of PPAR2 impairs the development of adipose tissue and insulin sensitivity. Proc Natl Acad Sci USA 101:10703–10708
PPAR knock-in/point mutations
Tsai YS, Kim HJ, Takahashi N, Kim HS, Hagaman JR, Kim JK, Maeda N 2004 Hypertension and abnormal fat distribution but not insulin resistance in mice with P465L PPAR. J Clin Invest 114:240–249[CrossRef][Medline]
Freedman BD, Lee EJ, Park Y, Jameson JL 2005 A dominant negative peroxisome proliferator-activated receptor- knock-in mouse exhibits features of the metabolic syndrome. J Biol Chem 280:17118–17125
Oxysterol Receptors Nr1h
LXR/Nr1h3
Peet DJ, Turley SD, Ma W, Janowski BA, Lobaccaro JM, Hammer RE, Mangelsdorf DJ 1998 Cholesterol and bile acid metabolism are impaired in mice lacking the nuclear oxysterol receptor LXR. Cell 93:693–704[CrossRef][Medline]
Alberti S, Schuster G, Parini P, Feltkamp D, Diczfalusy U, Rudling M, Angelin B, Bjorkhem I, Pettersson S, Gustafsson JA 2001 Hepatic cholesterol metabolism and resistance to dietary cholesterol in LXRß-deficient mice. J Clin Invest 107:565–573[Medline]
LXRß/Nr1h2
Repa JJ, Turley SD, Lobaccaro JA, Medina J, Li L, Lustig K, Shan B, Heyman RA, Dietschy JM, Mangelsdorf DJ 2000 Regulation of absorption and ABC1-mediated efflux of cholesterol by RXR heterodimers. Science 289:1524–1529
Alberti S, Schuster G, Parini P, Feltkamp D, Diczfalusy U, Rudling M, Angelin B, Bjorkhem I, Pettersson S, Gustafsson JA 2001 Hepatic cholesterol metabolism and resistance to dietary cholesterol in LXRß-deficient mice. J Clin Invest 107:565–573[Medline]
Farnesoid X/Bile Acid Receptors Nr1h4
FXR/Nr1h4
Sinal CJ, Tohkin M, Miyata M, Ward JM, Lambert G, Gonzalez FJ 2000 Targeted disruption of the nuclear receptor FXR/BAR impairs bile acid and lipid homeostasis. Cell 102:731–744[CrossRef][Medline]
Kok T, Hulzebos CV, Wolters H, Havinga R, Agellon LB, Stellaard F, Shan B, Schwarz M, Kuipers F 2003 Enterohepatic circulation of bile salts in farnesoid X receptor-deficient mice: efficient intestinal bile salt absorption in the absence of ileal bile acid-binding protein. J Biol Chem 278:41930–41937
Constitutive Androstane Receptor Nr1i3
CAR/Nr1i3
Wei P, Zhang J, Egan-Hafley M, Liang S, Moore DD 2000 The nuclear receptor CAR mediates specific xenobiotic induction of drug metabolism. Nature 407:920–923[CrossRef][Medline]
Maglich JM, Stoltz CM, Goodwin B, Hawkins-Brown D, Moore JT, Kliewer SA 2002 Nuclear pregnane x receptor and constitutive androstane receptor regulate overlapping but distinct sets of genes involved in xenobiotic detoxification. Mol Pharmacol 62:638–646
Pregnane X Receptor Nr1i2
PXR/Nr1i2
Xie W, Barwick JL, Downes M, Blumberg B, Simon CM, Nelson MC, Neuschwander-Tetri BA, Brunt EM, Guzelian PS, Evans RM 2000 Humanized xenobiotic response in mice expressing nuclear receptor SXR. Nature 406:435–439[CrossRef][Medline]
Staudinger JL, Goodwin B, Jones SA, Hawkins-Brown D, MacKenzie KI, LaTour A, Liu Y, Klaassen CD, Brown KK, Reinhard J, Willson TM, Koller BH, Kliewer SA 2001 The nuclear receptor PXR is a lithocholic acid sensor that protects against liver toxicity. Proc Natl Acad Sci USA 98:3369–3374
GCNF1/Nr6a1
Chung AC, Katz D, Pereira FA, Jackson KJ, DeMayo FJ, Cooney AJ, O’Malley BW 2001 Loss of orphan receptor germ cell nuclear factor function results in ectopic development of the tail bud and a novel posterior truncation. Mol Cell Biol 21:663–677
Lan ZJ, Chung AC, Xu X, DeMayo FJ, Cooney AJ 2002 The embryonic function of germ cell nuclear factor is dependent on the DNA binding domain. J Biol Chem 277:50660–50667
Lan ZJ, Gu P, Xu X, Jackson KJ, DeMayo FJ, O’Malley BW, Cooney AJ 2003 GCNF-dependent repression of BMP-15 and GDF-9 mediates gamete regulation of female fertility. EMBO J 22:4070–4081[CrossRef][Medline]
HNF4/Nr2a1
Chen WS, Manova K, Weinstein DC, Duncan SA, Plump AS, Prezioso VR, Bachvarova RF, Darnell Jr JE 1994 Disruption of the HNF-4 gene, expressed in visceral endoderm, leads to cell death in embryonic ectoderm and impaired gastrulation of mouse embryos. Genes Dev 8:2466–2477
Hayhurst GP, Lee YH, Lambert G, Ward JM, Gonzalez FJ 2001 Hepatocyte nuclear factor 4 (nuclear receptor 2A1) is essential for maintenance of hepatic gene expression and lipid homeostasis. Mol Cell Biol 21:1393–1403
Parviz F, Li J, Kaestner KH, Duncan SA 2002 Generation of a conditionally null allele of hnf4. Genesis 32:130–133[CrossRef][Medline]
Vincent SD, Robertson EJ 2004 Targeted insertion of an IRES Cre into the Hnf4 locus: Cre-mediated recombination in the liver, kidney, and gut epithelium. Genesis 39:206–211[CrossRef][Medline]
Reverb/Nr1d1
Chomez P, Neveu I, Mansen A, Kiesler E, Larsson L, Vennstrom B, Arenas E 2000 Increased cell death and delayed development in the cerebellum of mice lacking the rev-erbA() orphan receptor. Development 127:1489–1498[Abstract]
Preitner N, Damiola F, Lopez-Molina L, Zakany J, Duboule D, Albrecht U, Schibler U 2002 The orphan nuclear receptor REV-ERB controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 110:251–260[CrossRef][Medline]
Retinoid-Related Orphan Receptors Nr1f
ROR/Rora/Nr1f1
Hamilton BA, Frankel WN, Kerrebrock AW, Hawkins TL, FitzHugh W, Kusumi K, Russell LB, Mueller KL, van Berkel V, Birren BW, Kruglyak L, Lander ES 1996 Disruption of the nuclear hormone receptor ROR in staggerer mice. Nature 379:736–739[CrossRef][Medline]
Dussault I, Fawcett D, Matthyssen A, Bader JA, Giguere V 1998 Orphan nuclear receptor ROR-deficient mice display the cerebellar defects of staggerer. Mech Dev 70:147–153[CrossRef][Medline]
Steinmayr M, Andre E, Conquet F, Rondi-Reig L, Delhaye-Bouchaud N, Auclair N, Daniel H, Crepel F, Mariani J, Sotelo C, Becker-Andre M 1998 staggerer phenotype in retinoid-related orphan receptor -deficient mice. Proc Natl Acad Sci USA 95:3960–3965
RORß/Rorb/Nr1f2
Andre E, Conquet F, Steinmayr M, Stratton SC, Porciatti V, Becker-Andre M 1998 Disruption of retinoid-related orphan receptor ß changes circadian behavior, causes retinal degeneration and leads to vacillans phenotype in mice. EMBO J 17:3867–3877[CrossRef][Medline]
ROR/Rorg/Nr1f3
Kurebayashi S, Ueda E, Sakaue M, Patel DD, Medvedev A, Zhang F, Jetten AM 2000 Retinoid-related orphan receptor (ROR) is essential for lymphoid organogenesis and controls apoptosis during thymopoiesis. Proc Natl Acad Sci USA 97:10132–10137
Sun Z, Unutmaz D, Zou YR, Sunshine MJ, Pierani A, Brenner-Morton S, Mebius RE, Littman DR 2000 Requirement for ROR in thymocyte survival and lymphoid organ development. Science 288:2369–2373
NGF1/NURR Group Nr4a
NGF1B/Nr4a1
Lee SL, Wesselschmidt RL, Linette GP, Kanagawa O, Russell JH, Milbrandt J 1995 Unimpaired thymic and peripheral T cell death in mice lacking the nuclear receptor NGFI-B (Nur77). Science 269:532–535
NURR1/Nr4a2
Zetterstrom RH, Solomin L, Jansson L, Hoffer BJ, Olson L, Perlmann T 1997 Dopamine neuron agenesis in Nurr1-deficient mice. Science 276:248–250
Saucedo-Cardenas O, Quintana-Hau JD, Le WD, Smidt MP, Cox JJ, De Mayo F, Burbach JP, Conneely OM 1998 Nurr1 is essential for the induction of the dopaminergic phenotype and the survival of ventral mesencephalic late dopaminergic precursor neurons. Proc Natl Acad Sci USA 95:4013–4018
Castillo SO, Baffi JS, Palkovits M, Goldstein DS, Kopin IJ, Witta J, Magnuson MA, Nikodem VM 1998 Dopamine biosynthesis is selectively abolished in substantia nigra/ventral tegmental area but not in hypothalamic neurons in mice with targeted disruption of the Nurr1 gene. Mol Cell Neurosci 11:36–46[CrossRef][Medline]
NOR1/Nr4a3
Ponnio T, Burton Q, Pereira FA, Wu DK, Conneely OM 2002 The nuclear receptor Nor-1 is essential for proliferation of the semicircular canals of the mouse inner ear. Mol Cell Biol 22:935–945
DeYoung RA, Baker JC, Cado D, Winoto A 2003 The orphan steroid receptor Nur77 family member Nor-1 is essential for early mouse embryogenesis. J Biol Chem 278:47104–47109
SF1/LRH1 Group Nr5a
SF1/Nr5a1
Luo X, Ikeda Y, Parker KL 1994 A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation. Cell 77:481–490[CrossRef][Medline]
Luo X, Ikeda Y, Schlosser DA, Parker KL 1995 Steroidogenic factor 1 is the essential transcript of the mouse Ftz-F1 gene. Mol Endocrinol 9:1233–1239
Sadovsky Y, Crawford PA, Woodson KG, Polish JA, Clements MA, Tourtellotte LM, Simburger K, Milbrandt J 1995 Mice deficient in the orphan receptor steroidogenic factor 1 lack adrenal glands and gonads but express P450 side-chain-cleavage enzyme in the placenta and have normal embryonic serum levels of corticosteroids. Proc Natl Acad Sci USA 92:10939–10943
Shinoda K, Lei H, Yoshii H, Nomura M, Nagano M, Shiba H, Sasaki H, Osawa Y, Ninomiya Y, Niwa O, et al. 1995 Developmental defects of the ventromedial hypothalamic nucleus and pituitary gonadotroph in the Ftz-F1 disrupted mice. Dev Dyn 204:22–29[Medline]
Zhao L, Bakke M, Krimkevich Y, Cushman LJ, Parlow AF, Camper SA, Parker KL 2001 Steroidogenic factor 1 (SF1) is essential for pituitary gonadotrope function. Development 128:147–154[Abstract]
Jeyasuria P, Ikeda Y, Jamin SP, Zhao L, de Rooij DG, Themmen APN, Behringer RR, and Parker KL 2004 Cell-specific knockouts of steroidogenic factor 1 reveal its essential roles in gonadal function. Mol Endocrinol 18:1610–1619
LRH1/Nr5a2
Botrugno OA, Fayard E, Annicotte JS, Haby C, Brennan T, Wendling O, Tanaka T, Kodama T, Thomas W, Auwerx J, Schoonjans K 2004 Synergy between LRH-1 and ß-catenin induces G1 cyclin-mediated cell proliferation. Mol Cell 15:499–509[CrossRef][Medline]
Pare JF, Malenfant D, Courtemanche C, Jacob-Wagner M, Roy S, Allard D, Belanger L 2004 The fetoprotein transcription factor (FTF) gene is essential to embryogenesis and cholesterol homeostasis and is regulated by a DR4 element. J Biol Chem 279:21206–21216
Gu P, Goodwin B, Chung AC, Xu X, Wheeler DA, Price RR, Galardi C, Peng L, Latour AM, Koller BH, Gossen J, Kliewer SA, Cooney AJ 2005 Orphan nuclear receptor LRH-1 is required to maintain Oct4 expression at the epiblast stage of embryonic development. Mol Cell Biol 25:3492–3505
Nr2e Group
TLX/Nr2e1
Monaghan AP, Bock D, Gass P, Schwager A, Wolfer DP, Lipp HP, Schutz G 1997 Defective limbic system in mice lacking the tailless gene. Nature 390:515–517[CrossRef][Medline]
Yu RT, Chiang MY, Tanabe T, Kobayashi M, Yasuda K, Evans RM, Umesono K 2000 The orphan nuclear receptor Tlx regulates Pax2 and is essential for vision. Proc Natl Acad Sci USA 97:2621–2625
Young KA, Berry ML, Mahaffey CL, Saionz JR, Hawes NL, Chang B, Zheng QY, Smith RS, Bronson RT, Nelson RJ, Simpson EM 2002 Fierce: a new mouse deletion of Nr2e1; violent behaviour and ocular abnormalities are background-dependent. Behav Brain Res 132:145–158[CrossRef][Medline]
PNR/rd7/Nr2e3
Akhmedov NB, Piriev NI, Chang B, Rapoport AL, Hawes NL, Nishina PM, Nusinowitz S, Heckenlively JR, Roderick TH, Kozak CA, Danciger M, Davisson MT, Farber DB 2000 A deletion in a photoreceptor-specific nuclear receptor mRNA causes retinal degeneration in the rd7 mouse. Proc Natl Acad Sci USA 97:5551–5556
Haider NB, Naggert JK, Nishina PM 2001 Excess cone cell proliferation due to lack of a functional NR2E3 causes retinal dysplasia and degeneration in rd7/rd7 mice. Hum Mol Genet 10:1619–1626
DAX1/SHP Group Nr0b
DAX1/Ahch/Nr0b1
Yu RN, Ito M, Saunders TL, Camper SA, Jameson JL 1998 Role of Ahch in gonadal development and gametogenesis. Nat Genet 20:353–357[CrossRef][Medline]
SHP1/Nr0b2
Wang L, Lee YK, Bundman D, Han Y, Thevananther S, Kim CS, Chua SS, Wei P, Heyman RA, Karin M, Moore DD 2002 Redundant pathways for negative feedback regulation of bile acid production. Dev Cell 2:721–731[CrossRef][Medline]
Estrogen-Related Receptors Nr3b
ERR/Esrra/Nr3b1
Luo J, Sladek R, Carrier J, Bader JA, Richard D, Giguere V 2003 Reduced fat mass in mice lacking orphan nuclear receptor estrogen-related receptor . Mol Cell Biol 23:7947–7456
ERRß/Esrrb/Nr3b2
Luo J, Sladek R, Bader JA, Matthyssen A, Rossant J, Giguere V 1997 Placental abnormalities in mouse embryos lacking the orphan nuclear receptor ERR-ß. Nature 388:778–782[CrossRef][Medline]
Mitsunaga K, Araki K, Mizusaki H, Morohashi K-I, Haruna K, Nakagata N, Giguère V, Yamamura KI, Abe K 2004 Loss of PGC-specific expression of the orphan nuclear receptor ERR-ß results in reduction of germ cell number in mouse embryos. Mech Dev 121:237–246[CrossRef][Medline]
Testicular Orphan Nuclear Receptors Nr2c
TR2/Nr2c1
Shyr CR, Collins LL, Mu XM, Platt KA, Chang C 2002 Spermatogenesis and testis development are normal in mice lacking testicular orphan nuclear receptor 2. Mol Cell Biol 22:4661–4666
TR4/Nr2c2
Collins LL, Lee YF, Heinlein CA, Liu NC, Chen YT, Shyr CR, Meshul CK, Uno H, Platt KA, Chang C 2004 Growth retardation and abnormal maternal behavior in mice lacking testicular orphan nuclear receptor 4. Proc Natl Acad Sci USA 101:15058–15063
COUP Group Nr2f
COUP-TF1/Nr2f1
Qiu Y, Pereira FA, DeMayo FJ, Lydon JP, Tsai SY, Tsai MJ 1997 Null mutation of mCOUP-TFI results in defects in morphogenesis of the glossopharyngeal ganglion, axonal projection, and arborization. Genes Dev 11:1925–1937
COUP-TF2/Nr2f2
Pereira FA, Qiu Y, Zhou G, Tsai MJ, Tsai SY 1999 The orphan nuclear receptor COUP-TFII is required for angiogenesis and heart development. Genes Dev 13:1037–1049
Lee CT, Li R, Takamoto N, Martin JF, DeMayo FJ, Tsai, M-J, Tsai SY 2004 The nuclear orphan receptor COUP-TFII is required for limb and skeletal muscle development. Mol Cell Biol 24: 10835–10843
Takamoto N, You LR, Moses K, Chiang C, Zimmer WE, Schwartz RJ, DeMayo FJ, Tsai MJ, Tsai SY 2005 COUP-TFII is essential for radial and anteroposterior patterning of the stomach. Development 132:2179–2189
You L-R, Lin F-J, Lee CT, DeMayo FJ, Tsai M-J, Tsai SY 2005 Suppression of Notch signaling by the nuclear receptor COUP-TFII is required for the establishment of vein identity. Nature 435:98–104[CrossRef][Medline]
Bardoux P, Zhang P, Flamez D, Perilhou A, Lavin TA, Tanti JF, Hellemans K, Gomas E, Godard C, Andreelli F, Buccheri MA, Kahn A, Le Marchand-Brustel Y, Burcelin R, Schuit F, Vasseur-Cognet M 2005 Essential role of chicken ovalbumin upstream promoter-transcription factor II in insulin secretion and insulin sensitivity revealed by conditional gene knockout. Diabetes 54:1357–1363
EAR2/COUP-TF3/Nr2f6
Warnecke M, Oster H, Revelli JP, Alvarez-Bolado G, Eichele G 2005 Abnormal development of the locus coeruleus in Ear2(Nr2f6)-deficient mice impairs the functionality of the forebrain clock and affects nociception. Genes Dev 19:614–625
Footnotes
1 We thank Douglas Forrest for providing this segment of the Genetically Modified Animals in Endocrinology Bibliography Project. Dr. Forrest is with the National Institutes of Diabetes and Digestive and Kidney Diseases at the National Institutes of Health. 
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