Regulation of facilitative glucose transporters and AKT/MAPK/PRKAA signaling via estradiol and progesterone in the mouse uterine epithelium

Biology of Reproduction

Volumn 81, Issue 1, 2009, Pages 188-198

  Sung, Tae Kim ^a   Moley, Kelle H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Epithelium; Estradiol; Female reproductive tract; Implantation; Progesterone; Uterine epithelium; Uterus

Indexed keywords

ESTRADIOL; GLUCOSE TRANSPORTER; GLUCOSE TRANSPORTER 1; GLUCOSE TRANSPORTER 4; GLUCOSE TRANSPORTER 8; GLUCOSE TRANSPORTER 9B; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHOPROTEIN; PROGESTERONE; PROTEIN KINASE B; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DECIDUA; DELAYED IMPLANTATION; DIESTRUS; ENDOMETRIUM; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; EPITHELIUM CELL; ESTROGEN ACTIVITY; ESTRUS CYCLE; EXPERIMENTAL MODEL; FEMALE; HORMONAL REGULATION; METESTRUS; MOUSE; NIDATION; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; EMBRYO IMPLANTATION; EPITHELIUM; ESTRADIOL; ESTROUS CYCLE; FEMALE; GLUCOSE TRANSPORT PROTEINS, FACILITATIVE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; PREGNANCY; PREGNANCY MAINTENANCE; PROGESTERONE; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; UTERUS;

EID: 67649662579     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.108.072629     Document Type: Article

References (45)

1. Joost HG, Bell GI, Best JD, Birnbaum MJ, Charron MJ, Chen YT, Doege H, James DE, Lodish HF, Moley KH, Moley JF, Mueckler M, et al. Nomenclature of the GLUT/SLC2A family of sugar/polyol transport facilitators. Am J Physiol Endocrinol Metab 2002; 282:E974-E976. (Pubitemid 34654762)
2. Joost HG, Thorens B. The extended GLUT-family of sugar/polyol transport facilitators: nomenclature, sequence characteristics, and potential function of its novel members (review). Mol Membr Biol 2001; 18:247-256. (Pubitemid 34052684)
3. Wood IS, Trayhurn P. Glucose transporters (GLUT and SGLT): expanded families of sugar transport proteins. Br J Nutr 2003; 89:3-9. (Pubitemid 36187532)
4. Riley JK, Moley KH. Glucose utilization and the PI3-K pathway: mechanisms for cell survival in preimplantation embryos. Reproduction 2006; 131:823-835. (Pubitemid 43805427)
5. Mueckler M. Family of glucose-transporter genes: implications for glucose homeostasis and diabetes. Diabetes 1990; 39:6-11. (Pubitemid 20022878)
6. Fukumoto H, Kayano T, Buse JB, Edwards Y, Pilch PF, Bell GI, Seino S. Cloning and characterization of the major insulin-responsive glucose transporter expressed in human skeletal muscle and other insulin-responsive tissues. J Biol Chem 1989; 264:7776-7779. (Pubitemid 19137249)
7. Birnbaum MJ. Identification of a novel gene encoding an insulin-responsive glucose transporter protein. Cell 1989; 57:305-315. (Pubitemid 19112369)
8. Carayannopoulos MO, Chi MM, Cui Y, Pingsterhaus JM, McKnight RA, Mueckler M, Devaskar SU, Moley KH. GLUT8 is a glucose transporter responsible for insulin-stimulated glucose uptake in the blastocyst. Proc Natl Acad Sci U S A 2000; 97:7313-7318. (Pubitemid 30431460)
9. Kim ST, Moley KH. The expression of GLUT8, GLUT9a, and GLUT9b in the mouse testis and sperm. Reprod Sci 2007; 14:445-455.
10. Gomez O, Romero A, Terrado J, Mesonero JE. Differential expression of glucose transporter GLUT8 during mouse spermatogenesis. Reproduction 2006; 131:63-70. (Pubitemid 43230704)
11. Doege H, Schurmann A, Bahrenberg G, Brauers A, Joost HG. GLUT8, a novel member of the sugar transport facilitator family with glucose transport activity. J Biol Chem 2000; 275:16275-16280. (Pubitemid 30366941)
12. Kim ST, Moley K. Paternal effect on embryo quality in diabetic mice is related to poor sperm quality and associated with decreased GLUT expression. Reproduction 2008; 136:313-322.
13. Carayannopoulos MO, Schlein A, Wyman A, Chi M, Keembiyehetty C, Moley KH. GLUT9 is differentially expressed and targeted in the preimplantation embryo. Endocrinology 2004; 145:1435-1443. (Pubitemid 38281029)
14. Keembiyehetty C, Augustin R, Carayannopoulos MO, Steer S, Manolescu A, Cheeseman CI, Moley KH. Mouse glucose transporter 9 splice variants are expressed in adult liver and kidney and are up-regulated in diabetes. Mol Endocrinol 2006; 20:686-697. (Pubitemid 43291218)
15. Zhou J, Bondy CA. Placental glucose transporter gene expression and metabolism in the rat. J Clin Invest 1993; 91:845-852. (Pubitemid 23095258)
16. Bryant NJ, Govers R, James DE. Regulated transport of the glucose transporter GLUT4. Nat Rev Mol Cell Biol 2002; 3:267-277.
17. Pessin JE, Saltiel AR. Signaling pathways in insulin action: molecular targets of insulin resistance. J Clin Invest 2000; 106:165-169. (Pubitemid 30483117)
18. Gubbay O, Critchley HO, Bowen JM, King A, Jabbour HN. Prolactin induces ERK phosphorylation in epithelial and CD56(+) natural killer cells of the human endometrium. J Clin Endocrinol Metab 2002; 87:2329-2335. (Pubitemid 34521527)
19. Klotz DM, Hewitt SC, Ciana P, Raviscioni M, Lindzey JK, Foley J, Maggi A, DiAugustine RP, Korach KS. Requirement of estrogen receptor-alpha in insulin-like growth factor-1 (IGF-1)-induced uterine responses and in vivo evidence for IGF-1/estrogen receptor cross-talk. J Biol Chem 2002; 277:8531-8537. (Pubitemid 34968316)
20. Corton JM, Gillespie JG, Hardie DG. Role of the AMP-activated protein kinase in the cellular stress response. Curr Biol 1994; 4:315-324. (Pubitemid 124000994)
21. Kemp BE, Mitchelhill KI, Stapleton D, Michell BJ, Chen ZP, Witters LA. Dealing with energy demand: the AMP-activated protein kinase. Trends Biochem Sci 1999; 24:22-25.
22. Hardie DG, Scott JW, Pan DA, Hudson ER. Management of cellular energy by the AMP-activated protein kinase system. FEBS Lett 2003; 546:113-120. (Pubitemid 36782291)
23. Russell RR III, Bergeron R, Shulman GI, Young LH. Translocation of myocardial GLUT-4 and increased glucose uptake through activation of AMPK by AICAR. Am J Physiol 1999; 277:H643-H649. (Pubitemid 29415978)
24. Li J, Hu X, Selvakumar P, Russell RR III, Cushman SW, Holman GD, Young LH. Role of the nitric oxide pathway in AMPK-mediated glucose uptake and GLUT4 translocation in heart muscle. Am J Physiol Endocrinol Metab 2004; 287:E834-E841. (Pubitemid 39382917)
25. Marshall BA, Murata H, Hresko RC, Mueckler M. Domains that confer intracellular sequestration of the Glut4 glucose transporter in Xenopus oocytes. J Biol Chem 1993; 268:26193-26199. (Pubitemid 23361686)
26. Marshall BA, Ren JM, Johnson DW, Gibbs EM, Lillquist JS, Soeller WC, Holloszy JO, Mueckler M. Germline manipulation of glucose homeostasis via alteration of glucose transporter levels in skeletal muscle. J Biol Chem 1993; 268:18442-18445. (Pubitemid 23273771)
27. Tordjman KM, Leingang KA, James DE, Mueckler MM. Differential regulation of two distinct glucose transporter species expressed in 3T3-L1 adipocytes: effect of chronic insulin and tolbutamide treatment. Proc Natl Acad Sci U S A 1989; 86:7761-7765. (Pubitemid 19265265)
28. Deb K, Reese J, Paria BC. Methodologies to study implantation in mice. Methods Mol Med 2006; 121:9-34.
29. von Wolff M, Ursel S, Hahn U, Steldinger R, Strowitzki T. Glucose transporter proteins (GLUT) in human endometrium: expression, regulation, and function throughout the menstrual cycle and in early pregnancy. J Clin Endocrinol Metab 2003; 88:3885-3892. (Pubitemid 37034543)
30. Goldman NA, Katz EB, Glenn AS, Weldon RH, Jones JG, Lynch U, Fezzari MJ, Runowicz CD, Goldberg GL, Charron MJ. GLUT1 and GLUT8 in endometrium and endometrial adenocarcinoma. Mod Pathol 2006; 19:1429-1436. (Pubitemid 44624161)
31. Korgun ET, Demir R, Hammer A, Dohr G, Desoye G, Skofitsch G, Hahn T. Glucose transporter expression in rat embryo and uterus during decidualization, implantation, and early postimplantation. Biol Reprod 2001; 65:1364-1370. (Pubitemid 33031493)
32. Yamaguchi M, Sakata M, Ogura K, Miyake A. Gestational changes of glucose transporter gene expression in the mouse placenta and decidua. J Endocrinol Invest 1996; 19:567-569. (Pubitemid 26372272)
33. Heilig CW, Saunders T, Brosius FC III, Moley K, Heilig K, Baggs R, Guo L, Conner D. Glucose transporter-1-deficient mice exhibit impaired development and deformities that are similar to diabetic embryopathy. Proc Natl Acad Sci U S A 2003; 100:15613-15618. (Pubitemid 38021038)
34. Pascoe WS, Inukai K, Oka Y, Slot JW, James DE. Differential targeting of facilitative glucose transporters in polarized epithelial cells. Am J Physiol 1996; 271:C547-C554. (Pubitemid 26298915)
35. Carayannopoulos M, Chi M, Cui Y, Pingsterhaus J, Moley K. GLUT8, a glucose transporter responsible for insulin-stimulated uptake in the blastocyst. Proc Natl Acad Sci U S A 2000; 97:7313-7318. (Pubitemid 30431460)
36. Augustin R, Riley J, Moley KH. GLUT8 contains a [DE]XXXL[LI] sorting motif and localizes to a late endosomal/lysosomal compartment. Traffic 2005; 6:1196-1212. (Pubitemid 41632270)
37. Wyman AH, Chi M, Riley J, Carayannopoulos MO, Yang C, Coker KJ, Pessin JE, Moley KH. Syntaxin 4 expression affects glucose transporter 8 translocation and embryo survival. Mol Endocrinol 2003; 17:2096-2102. (Pubitemid 37281800)
38. Louden E, Chi M, Moley K. Crosstalk between the AMP-activated kinase and insulin signaling pathways rescues murine blastocyst cells from insulin resistance. Reproduction 2008; 136:335-344.
39. Augustin R, Carayannopoulos MO, Dowd LO, Phay JE, Moley JF, Moley KH. Identification and characterization of human glucose transporter-like protein-9 (GLUT9): alternative splicing alters trafficking. J Biol Chem 2004; 279:16229-16236. (Pubitemid 38509316)
40. Manolescu A, Augustin R, Moley KH, Cheeseman CI. A highly conserved hydrophobic motif in the exofacial vestibule of fructose transporting SLC2A proteins acts as a critical determinant of their substrate selectivity. Mol Membr Biol 2007; 24:455-463. (Pubitemid 47290684)
41. Caulfield MJ, Munroe PB, O'Neill D, Witkowska K, Charchar FJ, Doblado M, Evans S, Eyheramendy S, Onipinla A, Howard P, Shaw-Hawkins S, Dobson RJ, et al. SLC2A9 is a high-capacity urate transporter in humans. PLoS Med 2008; 5:e197.
42. Yoshino O, Osuga Y, Hirota Y, Koga K, Yano T, Tsutsumi O, Taketani Y. Akt as a possible intracellular mediator for decidualization in human endometrial stromal cells. Mol Hum Reprod 2003; 9:265-269. (Pubitemid 36748829)
43. Toyofuku A, Hara T, Taguchi T, Katsura Y, Ohama K, Kudo Y. Cyclic and characteristic expression of phosphorylated Akt in human endometrium and decidual cells in vivo and in vitro. Hum Reprod 2006; 21:1122-1128.
44. Maroulakou IG, Oemler W, Naber SP, Klebba I, Kuperwasser C, Tsichlis PN. Distinct roles of the three Akt isoforms in lactogenic differentiation and involution. J Cell Physiol 2008; 217:468-477.
45. Prast J, Saleh L, Husslein H, Sonderegger S, Helmer H, Knofler M. Human chorionic gonadotropin stimulates trophoblast invasion through extracellularly regulated kinase and AKT signaling. Endocrinology 2008; 149:979-987.