Folate transport in mouse cumulus-oocyte complexes and preimplantation embryos

Biology of Reproduction

Volumn 89, Issue 3, 2013, Pages

  Kooistra, Megan ^a,b   Trasler, Jacquetta M ^c,d,e   Baltz, Jay M ^a,b  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

^c RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^d MCGILL UNIVERSITY   (Canada)

^e MCGILL UNIVERSITY   (Canada)

Author keywords

Cumulus cells; Methotrexate; Oocyte; Preimplantation embryo; Rodents (rats, mice, guinea pigs, voles)

Indexed keywords

DYNASORE; FOLATE RECEPTOR 1; FOLATE RECEPTOR 2; FOLIC ACID; FOLINIC ACID; MESSENGER RNA; METHOTREXATE; PROTEIN INHIBITOR; PROTON COUPLED FOLATE TRANSPORTER; REDUCED FOLATE CARRIER; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BLASTOCYST; CONTROLLED STUDY; CUMULUS CELL; CUMULUS OOCYTE COMPLEX; EMBRYO; EMBRYO DEVELOPMENT; ENDOCYTOSIS; FEMALE; FOLATE METABOLISM; GAP JUNCTION; MOUSE; NONHUMAN; OOCYTE; OOCYTE TRANSPORT; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION;

CUMULUS CELLS; GUINEA PIGS; METHOTREXATE; MICE; OOCYTE; PREIMPLANTATION EMBRYO; RODENTS (RATS; VOLES);

ANIMALS; BIOLOGICAL TRANSPORT; BLASTOCYST; CELLS, CULTURED; CLEAVAGE STAGE, OVUM; CUMULUS CELLS; FEMALE; FOLATE RECEPTOR 1; FOLATE RECEPTOR 2; FOLIC ACID; MICE; MICE, INBRED C57BL; OOCYTES; REDUCED FOLATE CARRIER PROTEIN;

EID: 84889598404     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.113.111146     Document Type: Article

References (49)

1. Tibbetts AS, Appling DR. Compartmentalization of mammalian folatemediated one-carbon metabolism. Annu Rev Nutr 2010; 30:57-81.
2. Fowler B. The folate cycle and disease in humans. Kidney Int Suppl 2001; 78:S221-S229.
3. Lu SC. S-adenosylmethionine. Int J Biochem Cell Biol 2000; 32:391-395.
4. Bolusani S, Young BA, Cole NA, Tibbetts AS, Momb J, Bryant JD, Solmonson A, Appling DR. Mammalian MTHFD2L encodes a mitochondrial methylenetetrahydrofolate dehydrogenase isozyme expressed in adult tissues. J Biol Chem 2011; 286:5166-5174.
5. Qiu A, Jansen M, Sakaris A, Min SH, Chattopadhyay S, Tsai E, Sandoval C, Zhao R, Akabas MH, Goldman ID. Identification of an intestinal folate transporter and the molecular basis for hereditary folate malabsorption. Cell 2006; 127:917-928.
6. Qiu A, Min SH, Jansen M, Malhotra U, Tsai E, Cabelof DC, Matherly LH, Zhao R, Akabas MH, Goldman ID. Rodent intestinal folate transporters (SLC46A1): secondary structure, functional properties, and response to dietary folate restriction. Am J Physiol Cell Physiol 2007; 293: C1669-C1678.
7. Dixon KH, Lanpher BC, Chiu J, Kelley K, Cowan KH. A novel cDNA restores reduced folate carrier activity and methotrexate sensitivity to transport deficient cells. J Biol Chem 1994; 269:17-20.
8. Ganapathy V, Smith SB, Prasad PD. SLC19: the folate/thiamine transporter family. Pflugers Arch 2004; 447:641-646.
9. Antony AC. Folate receptors. Annu Rev Nutr 1996; 16:501-521.
10. Zhao R, Matherly LH, Goldman ID. Membrane transporters and folate homeostasis: intestinal absorption and transport into systemic compartments and tissues. Expert Rev Mol Med 2009; 11:e4.
11. Zhao R, Diop-Bove N, Visentin M, Goldman ID. Mechanisms of membrane transport of folates into cells and across epithelia. Annu Rev Nutr 2011; 31:177-201.
12. Brzezinska A, Winska P, Balinska M. Cellular aspects of folate and antifolate membrane transport. Acta Biochim Pol 2000; 47:735-749.
13. Kamen BA, Wang MT, Streckfuss AJ, Peryea X, Anderson RG. Delivery of folates to the cytoplasm of MA104 cells is mediated by a surface membrane receptor that recycles. J Biol Chem 1988; 263:13602-13609.
14. Sierra EE, Brigle KE, Spinella MJ, Goldman ID. Comparison of transport properties of the reduced folate carrier and folate receptor in murine L1210 leukemia cells. Biochem Pharmacol 1995; 50:1287-1294.
15. Spinella MJ, Brigle KE, Sierra EE, Goldman ID. Distinguishing between folate receptor-mediated transport and reduced folate carrier-mediated transport in L1210 leukemia cells. J Biol Chem 1995; 270:7842-7849.
16. Moscow JA, Gong M, He R, Sgagias MK, Dixon KH, Anzick SL, Meltzer PS, Cowan KH. Isolation of a gene encoding a human reduced folate carrier (RFC1) and analysis of its expression in transport-deficient, methotrexate-resistant human breast cancer cells. Cancer Res 1995; 55: 3790-3794.
17. Ikeda S, Koyama H, Sugimoto M, Kume S. Roles of one-carbon metabolism in preimplantation period-effects on short-term development and long-term programming. J Reprod Dev 2012; 58:38-43.
18. Ikeda S, Namekawa T, Sugimoto M, Kume S. Expression of methylation pathway enzymes in bovine oocytes and preimplantation embryos. J Exp Zool A Ecol Genet Physiol 2010; 313:129-136.
19. Kwong WY, Adamiak SJ, Gwynn A, Singh R, Sinclair KD. Endogenous folates and single-carbon metabolism in the ovarian follicle, oocyte and pre-implantation embryo. J Reprod Fertil 2010; 139:705-715.
20. Benkhalifa M, Montjean D, Cohen-Bacrie P, Menezo Y. Imprinting: RNA expression for homocysteine recycling in the human oocyte. Fertil Steril 2010; 93:1585-1590.
21. Steele W, Allegrucci C, Singh R, Lucas E, Priddle H, Denning C, Sinclair K, Young L. Human embryonic stem cell methyl cycle enzyme expression: modelling epigenetic programming in assisted reproduction? Reprod Biomed Online 2005; 10:755-766.
22. Menezo Y, Khatchadourian C, Gharib A, Hamidi J, Greenland T, Sarda N. Regulation of S-adenosyl methionine synthesis in the mouse embryo. Life Sci 1989; 44:1601-1609.
23. Ikeda S, Sugimoto M, Kume S. Importance of methionine metabolism in morula-to-blastocyst transition in bovine preimplantation embryos. J Reprod Dev 2012; 58:91-97.
24. Patkin EL, Kustova ME, Perticone P. The influence of demethylating agents on preimplantation development of mice. Zygote 1998; 6:351-358.
25. O'Neill C. Endogenous folic acid is essential for normal development of preimplantation embryos. Hum Reprod 1998; 13:1312-1316.
26. Biggers JD, McGinnis LK, Raffin M. Amino acids and preimplantation development of the mouse in protein-free potassium simplex optimized medium. Biol Reprod 2000; 63:281-293.
27. Van Winkle LJ. Amino Acid Transport Regulation and Early Embryo Development. Biol Reprod 2001; 64:1-12.
28. Lawitts JA, Biggers JD. Culture of preimplantation embryos. Methods Enzymol 1993; 225:153-164.
29. Pelland AM, Corbett HE, Baltz JM. Amino acid transport mechanisms in mouse oocytes during growth and meiotic maturation. Biol Reprod 2009; 81:1041-1054.
30. Zhou C, Baltz JM. JAK2 mediates the acute response to decreased cell volume in mouse preimplantation embryos by activating NHE1. J Cell Physiol 2013; 228:428-438.
31. Zhang M, Su YQ, Sugiura K, Xia G, Eppig JJ. Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science 2010; 330:366-369.
32. Zhang M, Su YQ, Sugiura K, Wigglesworth K, Xia G, Eppig JJ. Estradiol promotes and maintains cumulus cell expression of natriuretic peptide receptor 2 (NPR2) and meiotic arrest in mouse oocytes in vitro. Endocrinology 2011; 152:4377-4385.
33. Lee MB, Kooistra M, Zhang B, Slow S, Fortier AL, Garrow TA, Lever M, Trasler JM, Baltz JM. Betaine homocysteine methyltransferase is active in the mouse blastocyst and promotes inner cell mass development. J Biol Chem 2012; 287:33094-33103.
34. Mamo S, Gal AB, Bodo S, Dinnyes A. Quantitative evaluation and selection of reference genes in mouse oocytes and embryos cultured in vivo and in vitro. BMC Dev Biol 2007; 7:14.
35. Jeong YJ, Choi HW, Shin HS, Cui XS, Kim NH, Gerton GL, Jun JH. Optimization of real time RT-PCR methods for the analysis of gene expression in mouse eggs and preimplantation embryos. Mol Reprod Dev 2005; 71:284-289.
36. Baltz JM, Corbett HE, Richard S. Measuring transport and accumulation of radiolabeled substrates in oocytes and embryos. Methods Mol Biol 2013; 957:163-178.
37. Anas MK, Lee MB, Zhou C, Hammer MA, Slow S, Karmouch J, Liu XJ, Broer S, Lever M, Baltz JM. SIT1 is a betaine/proline transporter that is activated in mouse eggs after fertilization and functions until the 2-cell stage. Development 2008; 135:4123-4130.
38. Tartia AP, Rudraraju N, Richards T, Hammer MA, Talbot P, Baltz JM. Cell volume regulation is initiated in mouse oocytes after ovulation. Development 2009; 136:2247-2254.
39. Anas MKI, Hammer MA, Lever M, Stanton JA, Baltz JM. The organic osmolytes betaine and proline are transported by a shared system in early preimplantation mouse embryos. J Cell Physiol 2007; 210:266-277.
40. +-dependent transporter of zwitterionic amino acids in preimplantation mouse conceptuses. Biochim Biophys Acta 1990; 1025:225-233.
41. Eppig JJ. The relationship between cumulus cell-oocyte coupling, oocyte meiotic maturation, and cumulus expansion. Dev Biol 1982; 89:268-272.
42. Kirchhausen T, Macia E, Pelish HE. Use of dynasore, the small molecule inhibitor of dynamin, in the regulation of endocytosis. Methods Enzymol 2008; 438:77-93.
43. Newton AJ, Kirchhausen T, Murthy VN. Inhibition of dynamin completely blocks compensatory synaptic vesicle endocytosis. Proc Natl Acad Sci U S A 2006; 103:17955-17960.
44. Heller DT, Cahill DM, Schultz RM. Biochemical studies of mammalian oogenesis: metabolic cooperativity between granulosa cells and growing mouse oocytes. Dev Biol 1981; 84:455-464.
45. Su YQ, Sugiura K, Eppig JJ. Mouse oocyte control of granulosa cell development and function: paracrine regulation of cumulus cell metabolism. Semin Reprod Med 2009; 27:32-42.
46. Neuhouser ML, Nijhout HF, Gregory JF III, Reed MC, James SJ, Liu A, Shane B, Ulrich CM. Mathematical modeling predicts the effect of folate deficiency and excess on cancer-related biomarkers. Cancer Epidemiol Biomarkers Prev 2011; 20:1912-1917.
47. Boxmeer JC, Brouns RM, Lindemans J, Steegers EA, Martini E, Macklon NS, Steegers-Theunissen RP. Preconception folic acid treatment affects the microenvironment of the maturing oocyte in humans. Fertil Steril 2008; 89:1766-1770.
48. Munuce MJ, Quintero I, Caille AM, Ghersevich S, Berta CL. Comparative concentrations of steroid hormones and proteins in human peri-ovulatory peritoneal and follicular fluids. Reprod Biomed Online 2006; 13:202-207.
49. Heller DT, Schultz RM. Ribonucleoside metabolism by mouse oocytes: metabolic cooperativity between the fully grown oocyte and cumulus cells. J Exp Zool 1980; 214:355-364.