Effects of deficiency of the G protein Gsα on energy and glucose homeostasis

European Journal of Pharmacology

Volumn 660, Issue 1, 2011, Pages 119-124

  Chen, Min ^a   Nemechek, Nicholas M ^a   Mema, Eralda ^a,b   Wang, Jie ^a   Weinstein, Lee S ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b STONY BROOK UNIVERSITY   (United States)

Author keywords

G protein; Genomic imprinting; Insulin resistance; Melanocortin; Obesity; Sympathetic nervous system

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT;

ADRENERGIC SYSTEM; ENERGY BALANCE; ENERGY EXPENDITURE; ENERGY METABOLISM; EPIGENETICS; GENE; GENE FREQUENCY; GENE MUTATION; GENOME IMPRINTING; GLUCOSE HOMEOSTASIS; GLUCOSE INTOLERANCE; GLUCOSE METABOLISM; GNAS GENE; HETEROZYGOSITY; HOMOZYGOSITY; HUMAN; INSULIN SENSITIVITY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; THERMOGENESIS;

ANIMALS; CENTRAL NERVOUS SYSTEM; ENERGY METABOLISM; GLUCOSE; GTP-BINDING PROTEIN ALPHA SUBUNITS, GS; HOMEOSTASIS; HUMANS; MUTATION;

EID: 79955936334     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2010.10.105     Document Type: Review

References (90)

1. Bachman, E.S., Dhillon, H., Zhang, C.Y., Cinti, S., Bianco, A.C., Kobilka, B.K., Lowell, B.B., 2002. ßAR signaling required for diet-induced thermogenesis and obesity resistance. Science 297, 843-845. (Pubitemid 34839635)
2. Bagnol, D., Lu, X.Y., Kaelin, C.B., Day, H.E., Ollmann, M., Gantz, I., Akil, H., Barsh, G.S., Watson, S.J., 1999. Anatomy of an endogenous antagonist: relationship between Agouti-related protein and proopiomelanocortin in brain. J. Neurosci. 19 (RC26), 1-7.
3. Bastepe, M., Gunes, Y., Perez-Villamil, B., Hunzelman, J., Weinstein, L.S., Jüppner, H., 2002. Receptor-mediated adenylyl cyclase activation through XLαs, the extra-large variant of the stimulatory G protein α subunit. Mol. Endocrinol. 16, 1912-1919.
4. Bastepe, M., Pincus, J.E., Sugimoto, T., Tojo, K., Kanatani, M., Azuma, Y., Kruse, K., Rosenbloom, A.L., Koshiyama, H., Jüppner, H., 2001. Positional dissociation between the genetic mutation responsible for pseudohypoparathyroidism type Ib and the associated methylation defect at exon A/B: evidence for a long-range regulatory element within the imprinted GNAS1 locus. Hum. Mol. Genet. 10, 1231-1241.
5. Brito, M.N., Brito, N.A., Baro, D.J., Song, C.K., Bartness, T.J., 2007. Differential activation of the sympathetic innervation of adipose tissues by melanocortin receptor stimulation. Endocrinology 148, 5339-5347. (Pubitemid 350012626)
6. Butler, A.A., Cone, R.D., 2002. The melanocortin receptors: lessons from knockout models. Neuropeptides 36, 77-84.
7. Butler, A.A., Marks, D.L., Fan, W., Kuhn, C.M., Bartolome, M., Cone, R.D., 2001. Melanocortin-4 receptor is required for acute homeostatic responses to increased dietary fat. Nat. Neurosci. 4, 605-611.
8. Campbell, R., Gosden, C.M., Bonthron, D.T., 1994. Parental origin of transcription from the human GNAS1 gene. J. Med. Genet. 31, 607-614.
9. s deficiency. J. Clin. Endocrinol. Metab. 84, 4127-4131.
10. Chen, A.S., Marsh, D.J., Trumbauer, M.E., Frazier, E.G., Guan, X.M., Yu, H., Rosenblum, C.I., Vongs, A., Feng, Y., Cao, L., Metzger, J.M., Strack, A.M., Camacho, R.E., Mellin, T.N., Nunes, C.N., Min, W., Fisher, J., Gopal-Truter, S., MacIntyre, D.E., Chen, H.Y., Van der Ploeg, L.H., 2000a. Inactivation of the mouse melanocortin-3 receptor results in increased fat mass and reduced lean body mass. Nat. Genet. 26, 97-102.
11. Chen, A.S., Metzger, J.M., Trumbauer, M.E., Guan, X.M., Yu, H., Frazier, E.G., Marsh, D.J., Forrest, M.J., Gopal-Truter, S., Fisher, J., Camacho, R.E., Strack, A.M., Mellin, T.N., MacIntyre, D.E., Chen, H.Y., Van der Ploeg, L.H., 2000b. Role of the melanocortin-4 receptor in metabolic rate and food intake in mice. Transgenic Res. 9, 145-154. (Pubitemid 30610232)
12. sα deficiency in adipose tissue leads to a lean phenotype with divergent effects on cold tolerance and diet-induced thermogenesis. Cell Metab. 11, 320-330.
13. sα deficiency in skeletal muscle leads to reduced muscle mass, fiber-type switching, and glucose intolerance without insulin resistance or deficiency. Am. J. Physiol. Cell Physiol. 296, C930-C940.
14. Chen, M., Gavrilova, O., Liu, J., Xie, T., Deng, C., Nguyen, A.T., Nackers, L.M., Lorenzo, J., Shen, L., Weinstein, L.S., 2005a. Alternative Gnas gene products have opposite effects on glucose and lipid metabolism. Proc. Natl Acad. Sci. USA 102, 7386-7391.
15. sα deficiency. J. Clin. Invest. 115, 3217-3227.
16. sα and its role in metabolic regulation. Cell Metab. 9, 548-555.
17. Cone, R.D., 2005. Anatomy and regulation of the central melanocortin system. Nat. Neurosci. 8, 571-578.
18. Cowley, M.A., Pronchuk, N., Fan, W., Dinulescu, D.M., Colmers, W.F., Cone, R.D., 1999. Integration of NPY, AGRP, and melanocortin signals in the hypothalamic paraventricular nucleus: evidence of a cellular basis for the adipostat. Neuron 24, 155-163. (Pubitemid 29466155)
19. Davies, S.J., Hughes, H.E., 1993. Imprinting in Albright's hereditary osteodystrophy. J. Med. Genet. 30, 101-103.
20. de Rooij, J., Zwartkruis, F.J., Verheijen, M.H., Cool, R.H., Nijman, S.M., Wittinghofer, A., Bos, J.L., 1998. Epac is a Rap1 guanine-nucleotide- exchange factor directly activated by cyclic AMP. Nature 396, 474-477. (Pubitemid 28553318)
21. Dekelbab, B.H., Aughton, D.J., Levine, M.A., 2009. Pseudohypoparathyroidism type 1A and morbid obesity in infancy. Endocr. Pract. 15, 249-253.
22. Dong, C., Li, W.D., Geller, F., Lei, L., Li, D., Gorlova, O.Y., Hebebrand, J., Amos, C.I., Nicholls, R.D., Price, R.A., 2005. Possible genomic imprinting of three human obesity-related genetic loci. Am. J. Hum. Genet. 76, 427-437.
23. Elias, C.F., Lee, C., Kelly, J., Aschkenasi, C., Ahima, R.S., Couceyro, P.R., Kuhar, M.J., Saper, C.B., Elmquist, J.K., 1998. Leptin activates hypothalamic CART neurons projecting to the spinal cord. Neuron 21, 1375-1385. (Pubitemid 29022539)
24. Faivre, L., Cormier-Daire, V., Lapierre, J.M., Colleaux, L., Jacquemont, S., Genevieve, D., Saunier, P., Munnich, A., Turleau, C., Romana, S., Prieur, M., De Blois, M.C., Vekemans, M., 2002. Deletion of the SIM1 gene (6q16.2) in a patient with a Prader-Willi-like phenotype. J. Med. Genet. 39, 594-596.
25. Fan, W., Dinulescu, D.M., Butler, A.A., Zhou, J., Marks, D.L., Cone, R.D., 2000. The central melanocortin system can directly regulate serum insulin levels. Endocrinology 141, 3072-3079. (Pubitemid 32268993)
26. Farooqi, I.S., Keogh, J.M., Yeo, G.S., Lank, E.J., Cheetham, T., O'Rahilly, S., 2003. Clinical spectrum of obesity and mutations in the melanocortin 4 receptor gene. N. Engl. J. Med. 348, 1085-1095.
27. Frey, U.H., Hauner, H., Jockel, K.H., Manthey, I., Brockmeyer, N., Siffert, W., 2008a. A novel promoter polymorphism in the human gene GNAS affects binding of transcription factor upstream stimulatory factor 1, Gαs protein expression and body weight regulation. Pharmacogenet. Genomics 18, 141-151.
28. Frey, U.H., Michalsen, A., Merse, S., Dobos, G.J., Siffert, W., 2008b. A functional GNAS promoter polymorphism is associated with altered weight loss during short-term fasting. Eur. J. Med. Res. 13, 576-578.
29. Germain-Lee, E.L., Ding, C., Deng, Z., Crane, J.L., Saji, M., Ringel, M.D., Levine, M.A., 2002. Paternal imprinting of Gás in the human thyroid as the basis of TSH resistance in pseudohypoparathyroidism type 1a. Biochem. Biophys. Res. Commun. 296, 67-72.
30. Germain-Lee, E.L., Schwindinger, W., Crane, J.L., Zewdu, R., Zweifel, L.S., Wand, G., Huso, D.L., Saji, M., Ringel, M.D., Levine, M.A., 2005. A mouse model of Albright hereditary osteodystrophy generated by targeted disruption of exon 1 of the Gnas gene. Endocrinology 146, 4697-4709. (Pubitemid 41446607)
31. Gorlova, O.Y., Amos, C.I., Wang, N.W., Shete, S., Turner, S.T., Boerwinkle, E., 2003. Genetic linkage and imprinting effects on body mass index in children and young adults. Eur. J. Hum. Genet. 11, 425-432.
32. Hahn, S., Frey, U.H., Siffert, W., Tan, S., Mann, K., Janssen, O.E., 2006. The CC genotype of the GNAS T393C polymorphism is associated with obesity and insulin resistance in women with polycystic ovary syndrome. Eur. J. Endocrinol. 155, 763-770.
33. Haig, D., 2004. Genomic imprinting and kinship: how good is the evidence. Annu. Rev. Genet. 38, 553-585.
34. sα gene GNAS1 in the pathogenesis of acromegaly. J. Clin. Invest. 107, R31-R36.
35. Hayward, B.E., Kamiya, M., Strain, L., Moran, V., Campbell, R., Hayashizaki, Y., Bonthron, D.T., 1998a. The human GNAS1 gene is imprinted and encodes distinct paternally and biallelically expressed G proteins. Proc. Natl Acad. Sci. USA 95, 10038-10043.
36. Hayward, B.E., Moran, V., Strain, L., Bonthron, D.T., 1998b. Bidirectional imprinting of a single gene: GNAS1 encodes maternally, paternally, and biallelically derived proteins. Proc. Natl Acad. Sci. USA 95, 15475-15480.
37. Holder Jr., J.L., Butte, N.F., Zinn, A.R., 2000. Profound obesity associated with a balanced translocation that disrupts the SIM1 gene. Hum. Mol. Genet. 9, 101-108.
38. Holder Jr., J.L., Zhang, L., Kublaoui, B.M., DiLeone, R.J., Oz, O.K., Bair, C.H., Lee, Y.H., Zinn, A.R., 2004. Sim1 gene dosage modulates the homeostatic feeding response to increased dietary fat in mice. Am. J. Physiol. Endocrinol. Metab. 287, E105-E113.
39. Huszar, D., Lynch, C.A., Fairchild-Huntress, V., Dunmore, J.H., Fang, Q., Berkemeier, L.R., Gu, W., Kesterson, R.A., Boston, B.A., Cone, R.D., Smith, F.J., Campfield, L.A., Burn, P., Lee, F., 1997. Targeted disruption of the melanocortin-4 receptor results in obesity in mice. Cell 88, 131-141. (Pubitemid 27180337)
40. Ischia, R., Lovisetti-Scamihorn, P., Hogue-Angeletti, R., Wolkersdorfer, M., Winkler, H., Fischer-Colbrie, R., 1997. Molecular cloning and characterization of NESP55, a novel chromogranin-like precursor of a peptide with 5-HT1B receptor antagonist activity. J. Biol. Chem. 272, 11657-11662.
41. sα mRNA. J. Biol. Chem. 265, 8458-8462.
42. Jan de Beur, S., Ding, C., Germain-Lee, E.L., Cho, J., Maret, A., Levine, M.A., 2003. Discordance between genetic and epigenetic defects in pseudohypoparathyroidism type 1b revealed by inconsistent loss of maternal imprinting at GNAS1. Am. J. Hum. Genet. 73, 314-322.
43. Kehlenbach, R.H., Matthey, J., Huttner, W.B., 1994. XLαs is a new type of G protein. Nature 372, 804-809.
44. Kelly, M.L., Moir, L., Jones, L., Whitehill, E., Anstee, Q.M., Goldin, R.D., Hough, A., Cheeseman, M., Jansson, J.O., Peters, J., Cox, R.D., 2009. A missense mutation in the non-neural G-protein α-subunit isoforms modulates susceptibility to obesity. Int. J. Obes. (Lond.) 33, 507-518.
45. Kelsey, G., Bodle, D., Miller, H.J., Beechey, C.V., Coombes, C., Peters, J., Williamson, C.M., 1999. Identification of imprinted loci by methylation-sensitive representational difference analysis: application to mouse distal chromosome 2. Genomics 62, 129-138. (Pubitemid 30053926)
46. Kishi, T., Aschkenasi, C.J., Lee, C.E., Mountjoy, K.G., Saper, C.B., Elmquist, J.K., 2003. Expression of melanocortin 4 receptor mRNA in the central nervous system of the rat. J. Comp. Neurol. 457, 213-235.
47. Kozasa, T., Itoh, H., Tsukamoto, T., Kaziro, Y., 1988. Isolation and characterization of the human Gsá gene. Proc. Natl Acad. Sci. USA 85, 2081-2085.
48. Krude, H., Biebermann, H., Luck, W., Horn, R., Brabant, G., Gruters, A., 1998. Severe early-onset obesity, adrenal insufficiency and red hair pigmentation caused by POMC mutations in humans. Nat. Genet. 19, 155-157.
49. Kublaoui, B.M., Gemelli, T., Tolson, K.P., Wang, Y., Zinn, A.R., 2008. Oxytocin deficiency mediates hyperphagic obesity of Sim1 haploinsufficient mice. Mol. Endocrinol. 22, 1723-1734.
50. Kublaoui, B.M., Holder Jr., J.L., Gemelli, T., Zinn, A.R., 2006a. Sim1 haploinsufficiency impairs melanocortin-mediated anorexia and activation of paraventricular nucleus neurons. Mol. Endocrinol. 20, 2483-2492.
51. Kublaoui, B.M., Holder Jr., J.L., Tolson, K.P., Gemelli, T., Zinn, A.R., 2006b. SIM1 overexpression partially rescues agouti yellow and diet-induced obesity by normalizing food intake. Endocrinology 147, 4542-4549. (Pubitemid 44402157)
52. Lindsay, R.S., Kobes, S., Knowler, W.C., Bennett, P.H., Hanson, R.L., 2001. Genome-wide linkage analysis assessing parent-of-origin effects in the inheritance of type 2 diabetes and BMI in Pima Indians. Diabetes 50, 2850-2857. (Pubitemid 33733138)
53. Liu, J., Chen, M., Deng, C., Bourc'his, D., Nealon, J.G., Erlichman, B., Bestor, T.H., Weinstein, L.S., 2005a. Identification of the control region for tissue-specific imprinting of the stimulatory G protein α-subunit. Proc. Natl Acad. Sci. USA 102, 5513-5518.
54. sα is imprinted in human thyroid glands: implications for thyroid function in pseudohypoparathyroidism types 1A and 1B. J. Clin. Endocrinol. Metab. 88, 4336-4341.
55. Liu, J., Litman, D., Rosenberg, M.J., Yu, S., Biesecker, L.G., Weinstein, L.S., 2000a. A GNAS1 imprinting defect in pseudohypoparathyroidism type IB. J. Clin. Invest. 106, 1167-1174.
56. Liu, J., Nealon, J.G., Weinstein, L.S., 2005b. Distinct patterns of abnormal GNAS imprinting in familial and sporadic pseudohypoparathyroidism type IB. Hum. Mol. Genet. 14, 95-102.
57. Liu, J., Yu, S., Litman, D., Chen, W., Weinstein, L.S., 2000b. Identification of a methylation imprint mark within the mouse Gnas locus. Mol. Cell. Biol. 20, 5808-5817.
58. s in the development of human obesity J. Clin. Endocrinol. Metab. 92, 1073-1079.
59. Mantovani, G., Ballare, E., Giammona, E., Beck-Peccoz, P., Spada, A., 2002. The Gsα gene: predominant maternal origin of transcription in human thyroid gland and gonads. J. Clin. Endocrinol. Metab. 87, 4736-4740.
60. Mantovani, G., Bondioni, S., Locatelli, M., Pedroni, C., Lania, A.G., Ferrante, E., Filopanti, M., Beck-Peccoz, P., Spada, A., 2004. Biallelic expression of the Gsα gene in human bone and adipose tissue. J. Clin. Endocrinol. Metab. 89, 6316-6319.
61. Marsh, D.J., Hollopeter, G., Huszar, D., Laufer, R., Yagaloff, K.A., Fisher, S.L., Burn, P., Palmiter, R.D., 1999. Response of melanocortin-4 receptor-deficient mice to anorectic and orexigenic peptides. Nat. Genet. 21, 119-122.
62. Mattera, R., Graziano, M.P., Yatani, A., Zhou, Z., Graf, R., Codina, J., Birnbaumer, L., Gilman, A.G., Brown, A.M., 1989. Splice variants of the alpha subunit of the G protein Gs activate both adenylyl cyclase and calcium channels. Science 243, 804-807. (Pubitemid 19062636)
63. Montminy, M., 1997. Transcriptional regulation by cyclic AMP. Annu. Rev. Biochem. 66, 807-822.
64. Nogueiras, R., Wiedmer, P., Perez-Tilve, D., Veyrat-Durebex, C., Keogh, J.M., Sutton, G.M., Pfluger, P.T., Castanada, T.R., Neschen, S., Hofmann, S.M., Howles, P.N., Morgan, D.A., Benoit, S.C., Szanto, I., Schrott, B., Schurmann, A., Joost, H.-G., Hammond, C., Hui, D.Y., Woods, S.C., Rahmouni, K., Butler, A.A., Farooqi, I.S., O'Rahilly, S., Rohner-Jeanrenaud, F., Tschop, M.H., 2007. The central melanocortin system directly controls peripheral lipid metabolism. J. Clin. Invest. 117, 3475-3488.
65. Nwosu, B.U., Lee, M.M., 2009. Pseudohypoparathyroidism type 1a and insulin resistance in a child. Nat. Rev. Endocrinol. 5, 345-350.
66. Obici, S., Feng, Z., Tan, J., Liu, L., Karkanias, G., Rossetti, L., 2001. Central melanocortin receptors regulate insulin action. J. Clin. Invest. 108, 1079-1085.
67. Pasolli, H.A., Klemke, M., Kehlenbach, R.H., Wang, Y., Huttner, W.B., 2000. Characterization of the extra-large G protein α-subunit XLαs. I. Tissue distribution and subcellular localization. J. Biol. Chem. 275, 33622-33632.
68. Peters, J., Wroe, S.F., Wells, C.A., Miller, H.J., Bodle, D., Beechey, C.V., Williamson, C.M., Kelsey, G., 1999. A cluster of oppositely imprinted transcripts at the Gnas locus in the distal imprinting region of mouse chromosome 2. Proc. Natl Acad. Sci. USA 96, 3830-3835.
69. Plagge, A., Gordon, E., Dean, W., Boiani, R., Cinti, S., Peters, J., Kelsey, G., 2004. The imprinted signaling protein XLαs is required for postnatal adaptation to feeding. Nat. Genet. 36, 818-826.
70. Plagge, A., Isles, A.R., Gordon, E., Humby, T., Dean, W., Gritsch, S., Fischer-Colbrie, R., Wilkinson, L.S., Kelsey, G., 2005. Imprinted Nesp55 influences behavioral reactivity to novel environments. Mol. Cell. Biol. 25, 3019-3026.
71. Rance, K.A., Fustin, J.M., Dalgleish, G., Hambly, C., Bunger, L., Speakman, J.R., 2005. A paternally imprinted QTL for mature body mass on mouse chromosome 8. Mamm. Genome 16, 567-577. (Pubitemid 41355919)
72. Reik, W., Walter, J., 2001. Genomic imprinting: parental influence on the genome. Nat. Rev. Genet. 2, 21-32.
73. Saper, C.B., Chou, T.C., Elmquist, J.K., 2002. The need to feed: homeostatic and hedonic control of eating. Neuron 36, 199-211. (Pubitemid 35217887)
74. Saper, C.B., Loewy, A.D., Swanson, L.W., Cowan, W.M., 1976. Direct hypothalamoautonomic connections. Brain Res. 117, 305-312.
75. s. J. Biol. Chem. 272, 5413-5420.
76. Swanson, L.W., Kuypers, H.G., 1980. The paraventricular nucleus of the hypothalamus: cytoarchitectonic subdivisions and organization of projections to the pituitary, dorsal vagal complex, and spinal cord as demonstrated by retrograde fluorescence double-labeling methods. J. Comp. Neurol. 194, 555-570.
77. Vaisse, C., Clement, K., Guy-Grand, B., Froguel, P., 1998. A frameshift mutation in human MC4R is associated with a dominant form of obesity. Nat. Genet. 20, 113-114.
78. Voss-Andreae, A., Murphy, J.G., Ellacott, K.L., Stuart, R.C., Nillni, E.A., Cone, R.D., Fan, W., 2007. Role of the central melanocortin circuitry in adaptive thermogenesis of brown adipose tissue. Endocrinology 148, 1550-1560. (Pubitemid 46457101)
79. Weinstein, L.S., Chen, M., Xie, T., Liu, J., 2006. Genetic diseases associated with heterotrimeric G proteins. Trends Pharmacol. Sci. 27, 260-266.
80. sα gene Gnas using gene targeting technology. Pharmacol. Ther. 115, 271-291.
81. Weinstein, L.S., Yu, S., Warner, D.R., Liu, J., 2001. Endocrine manifestations of stimulatory G protein α-subunit mutations and the role of genomic imprinting. Endocr. Rev. 22, 675-705.
82. Williamson, C.M., Ball, S.T., Nottingham, W.T., Skinner, J.A., Plagge, A., Turner, M.D., Powles, N., Hough, T., Papworth, D., Fraser, W.D., Maconochie, M., Peters, J., 2004. A cis-acting control region is required exclusively for the tissue-specific imprinting of Gnas. Nat. Genet. 36, 894-899.
83. sα imprint control region. Endocrinology 149, 2443-2450.
84. sα deficiency has divergent effects on pancreatic α and β cell proliferation. J. Endocrinol. 11, 2010 published online June.
85. sα leads to reduced β cell mass and insulin-deficient diabetes. Proc. Natl Acad. Sci. USA 104, 19601-19606.
86. Xie, T., Plagge, A., Gavrilova, O., Pack, S., Jou, W., Lai, E.W., Frontera, M., Kelsey, G., Weinstein, L.S., 2006. The alternative stimulatory G protein α-subunit XLαs is a critical regulator of energy and glucose metabolism and sympathetic nerve activity in adult mice. J. Biol. Chem. 281, 18989-18999.
87. Xu, B., Goulding, E.H., Zang, K., Cepoi, D., Cone, R.D., Jones, K.R., Tecott, L.H., Reichardt, L. F., 2003. Brain-derived neurotrophic factor regulates energy balance downstream of melanocortin-4 receptor. Nat. Neurosci. 6, 736-742.
88. Yeo, G.S., Farooqi, I.S., Aminian, S., Halsall, D.J., Stanhope, R.G., O'Rahilly, S., 1998. A frameshift mutation in MC4R associated with dominantly inherited human obesity. Nat. Genet. 20, 111-112.
89. Yu, S., Gavrilova, O., Chen, H., Lee, R., Liu, J., Pacak, K., Parlow, A.F., Quon, M.J., Reitman, M.L., Weinstein, L.S., 2000. Paternal versus maternal transmission of a stimulatory G protein α subunit knockout produces opposite effects on energy metabolism. J. Clin. Invest. 105, 615-623.
90. sα gene. Proc. Natl Acad. Sci. USA 95, 8715-8720.