Lactate production by the mammalian blastocyst: Manipulating the microenvironment for uterine implantation and invasion?

BioEssays

Volumn 37, Issue 4, 2015, Pages 364-371

  Gardner, David K ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Implantation; Lactate; Microenvironment; Signalling

Indexed keywords

GLUCOSE; LACTIC ACID; OXYGEN;

ANGIOGENESIS; ANIMAL EMBRYO; ARTICLE; BLASTOCYST; BLOOD VESSEL PERMEABILITY; CELL MIGRATION; EMBRYO DEVELOPMENT; ENDOMETRIUM; ENDOMETRIUM CELL; ENERGY YIELD; GLUCOSE METABOLISM; GLYCOLYSIS; HUMAN; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; NIDATION; NONHUMAN; OXYGEN TENSION; PH; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; TROPHOBLAST; UTERUS; ANIMAL; FEMALE; MAMMAL; METABOLISM; PHYSIOLOGY; PREGNANCY;

MAMMALIA;

ANIMALS; BLASTOCYST; EMBRYO IMPLANTATION; FEMALE; HUMANS; LACTIC ACID; MAMMALS; PREGNANCY; TROPHOBLASTS;

EID: 84925161115     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201400155     Document Type: Article

References (94)

1. Hamatani T, Ko MSH, Yamada M, Kuji N, et al. 2006. Global gene expression profiling of preimplantation embryos. Hum Cell 19: 98-117.
2. Leese HJ, Biggers JD, Mroz EA, Lechene C. 1984. Nucleotides in a single mammalian ovum or preimplantation embryo. Anal Biochem 140: 443-8.
3. Gardner DK, Wale PL. 2013. Analysis of metabolism to select viable human embryos for transfer. Fertil Steril 99: 1062-72.
4. Watson AJ, Natale DR, Barcroft LC. 2004. Molecular regulation of blastocyst formation. Anim Reprod Sci 82-83: 583-92.
5. Gardner DK, Leese HJ. 1987. Assessment of embryo viability prior to transfer by the noninvasive measurement of glucose uptake. J Exp Zool 242: 103-5.
6. Gardner DK, Wale PL, Collins R, Lane M. 2011. Glucose consumption of single post-compaction human embryos is predictive of embryo sex and live birth outcome. Hum Reprod 26: 1981-6.
7. Houghton FD, Thompson JG, Kennedy CJ, Leese HJ. 1996. Oxygen consumption and energy metabolism of the early mouse embryo. Mol Reprod Dev 44: 476-85.
8. Trimarchi JR, Liu L, Porterfield DM, Smith PJ, et al. 2000. Oxidative phosphorylation-dependent and -independent oxygen consumption by individual preimplantation mouse embryos. Biol Reprod 62: 1866-74.
9. Hume DA, Weidemann MJ. 1979. Role and regulation of glucose metabolism in proliferating cells. J Natl Cancer Inst 62: 3-8.
10. Morgan MJ, Faik P. 1981. Carbohydrate metabolism in cultured animal cells. Biosci Rep 1: 669-86.
11. Mandel LJ. 1986. Energy metabolism of cellular activation, growth, and transformation. Curr Top Memb Trans 27: 261-91.
12. Warburg O. 1956. On respiratory impairment in cancer cells. Science 124: 269-70.
13. Wang T, Marquardt C, Foker J. 1976. Aerobic glycolysis during lymphocyte proliferation. Nature 261: 702-5.
14. Gott AL, Hardy K, Winston RM, Leese HJ. 1990. Non-invasive measurement of pyruvate and glucose uptake and lactate production by single human preimplantation embryos. Hum Reprod 5: 104-8.
15. Jha MK, Suk K. 2013. Pyruvate dehydrogenase kinase as a potential therapeutic target for malignant gliomas. Brain Tumor Res Treat 1: 57-63.
16. Newsholme EA, Crabtree B, Ardawi MS. 1985. The role of high rates of glycolysis and glutamine utilization in rapidly dividing cells. Biosci Rep 5: 393-400.
17. Reitzer LJ, Wice BM, Kennell D. 1980. The pentose cycle. Control and essential function in HeLa cell nucleic acid synthesis. J Biol Chem 255: 5616-26.
18. Rieger D. 1992. Relationships between energy metabolism and development of early mammalian embryos. Theriogenology 37: 75-93.
19. Cha J, Sun X, Dey SK. 2012. Mechanisms of implantation: strategies for successful pregnancy. Nat Med 18: 1754-67.
20. Hoversland RC, Weitlauf HM. 1981. The volume of uterine fluid in 'implanting' and 'delayed implanting' mice. J Reprod Fertil 62: 105-9.
21. Salleh N, Baines DL, Naftalin RJ, Milligan SR. 2005. The hormonal control of uterine luminal fluid secretion and absorption. J Membr Biol 206: 17-28.
22. Fischer B, Bavister BD. 1993. Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. J Reprod Fertil 99: 673-9.
23. Rogers PAW, Murphy CR, Gannon BJ. 1982. Absense of capillaries in the endometrium surrounding the implanting rat blastocyst. Micron 13: 373-4.
24. Rinaudo PF, Giritharan G, Talbi S, Dobson AT, et al. 2006. Effects of oxygen tension on gene expression in preimplantation mouse embryos. Fertil Steril 86(4 Suppl): 1252-65.
25. Harvey AJ, Kind KL, Pantaleon M, Armstrong DT, et al. 2004. Oxygen-regulated gene expression in bovine blastocysts. Biol Reprod 71: 1108-19.
26. Katz-Jaffe MG, Linck DW, Schoolcraft WB, Gardner DK. 2005. A proteomic analysis of mammalian preimplantation embryonic development. Reproduction 130: 899-905.
27. Wale PL, Gardner DK. 2012. Oxygen regulates amino acid turnover and carbohydrate uptake during the preimplantation period of mouse embryo development. Biol Reprod 87: 24, 1-8.
28. Clough JR, Whittingham DG. 1983. Metabolism of [14C]glucose by postimplantation mouse embryos in vitro. J Embryol Exp Morphol 74: 133-42.
29. Auerbach S, Brinster RL. 1967. Lactate dehydrogenase isozymes in the early mouse embryo. Exp Cell Res 46: 89-92.
30. Fantin VR, St-Pierre J, Leder P. 2006. Attenuation of LDH-A expression uncovers a link between glycolysis, mitochondrial physiology, and tumor maintenance. Cancer Cell 9: 425-34.
31. Yao F, Zhao T, Zhong C, Zhu J, et al. 2013. LDHA is necessary for the tumorigenicity of esophageal squamous cell carcinoma. Tumour Biol 34: 25-31.
32. Halestrap AP, Wilson MC. 2012. The monocarboxylate transporter family-role and regulation. IUBMB Life 64: 109-19.
33. Dimmer KS, Friedrich B, Lang F, Deitmer JW, et al. 2000. The low-affinity monocarboxylate transporter MCT4 is adapted to the export of lactate in highly glycolytic cells. Biochem J 350: 219-27.
34. Draoui N, Feron O. 2011. Lactate shuttles at a glance: from physiological paradigms to anti-cancer treatments. Dis Model Mech 4: 727-32.
35. Herubel F, El Mouatassim S, Guerin P, Frydman R, et al. 2002. Genetic expression of monocarboxylate transporters during human and murine oocyte maturation and early embryonic development. Zygote 10: 175-81.
36. Deuticke B. 1982. Monocarboxylate transport in erythrocytes. J Membr Biol 70: 89-103.
37. Murray CM, Hutchinson R, Bantick JR, Belfield GP, et al. 2005. Monocarboxylate transporter MCT1 is a target for immunosuppression. Nat Chem Biol 1: 371-6.
38. Pinheiro C, Reis RM, Ricardo S, Longatto-Filho A, et al. 2010. Expression of monocarboxylate transporters 1, 2, and 4 in human tumours and their association with CD147 and CD44. J Biomed Biotechnol 2010: 427694.
39. Spencer TL, Lehninger AL. 1976. L-lactate transport in Ehrlich ascites-tumour cells. Biochem J 154: 405-14.
40. Griffiths JR. 1991. Are cancer cells acidic? Br J Cancer 64: 425-7.
41. Gillies RJ, Liu Z, Bhujwalla Z. 1994. 31P-MRS measurements of extracellular pH of tumors using 3-aminopropylphosphonate. Am J Physiol 267: C195-203.
42. Hashim AI, Zhang X, Wojtkowiak JW, Martinez GV, et al. 2011. Imaging pH and metastasis. NMR Biomed 24: 582-91.
43. Webb BA, Chimenti M, Jacobson MP, Barber DL. 2011. Dysregulated pH: a perfect storm for cancer progression. Nat Rev Cancer 11: 671-7.
44. Hunt TK, Aslam RS, Beckert S, Wagner S, et al. 2007. Aerobically derived lactate stimulates revascularization and tissue repair via redox mechanisms. Antioxid Redox Signal 9: 1115-24.
45. Chen L, Nakai M, Belton RJ, Jr., Nowak RA. 2007. Expression of extracellular matrix metalloproteinase inducer and matrix metalloproteinases during mouse embryonic development. Reproduction 133: 405-14.
46. Kato Y, Nakayama Y, Umeda M, Miyazaki K. 1992. Induction of 103-kDa gelatinase/type IV collagenase by acidic culture conditions in mouse metastatic melanoma cell lines. J Biol Chem 267: 11424-30.
47. Kato Y, Lambert CA, Colige AC, Mineur P, et al. 2005. Acidic extracellular pH induces matrix metalloproteinase-9 expression in mouse metastatic melanoma cells through the phospholipase D-mitogen-activated protein kinase signaling. J Biol Chem 280: 10938-44.
48. Kato Y, Ozawa S, Tsukuda M, Kubota E, et al. 2007. Acidic extracellular pH increases calcium influx-triggered phospholipase D activity along with acidic sphingomyelinase activation to induce matrix metalloproteinase-9 expression in mouse metastatic melanoma. FEBS J 274: 3171-83.
49. Baumann F, Leukel P, Doerfelt A, Beier CP, et al. 2009. Lactate promotes glioma migration by TGF-beta2-dependent regulation of matrix metalloproteinase-2. Neuro Oncol 11: 368-80.
50. Wahl SM, Swisher J, McCartney-Francis N, Chen W. 2004. TGF-beta: the perpetrator of immune suppression by regulatory T cells and suicidal T cells. J Leukoc Biol 76: 15-24.
51. Singh M, Chaudhry P, Asselin E. 2011. Bridging endometrial receptivity and implantation: network of hormones, cytokines, and growth factors. J Endocrinol 210: 5-14.
52. Das SK, Flanders KC, Andrews GK, Dey SK. 1992. Expression of transforming growth factor-beta isoforms (beta 2 and beta 3) in the mouse uterus: analysis of the periimplantation period and effects of ovarian steroids. Endocrinology 130: 3459-66.
53. Harvey MB, Leco KJ, Arcellana-Panlilio MY, Zhang X, et al. 1995. Proteinase expression in early mouse embryos is regulated by leukaemia inhibitory factor and epidermal growth factor. Development 121: 1005-14.
54. Whiteside EJ, Jackson MM, Herington AC, Edwards DR, et al. 2001. Matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-3 are key regulators of extracellular matrix degradation by mouse embryos. Biol Reprod 64: 1331-7.
55. Ho FM, Liu SH, Lin WW, Liau CS. 2007. Opposite effects of high glucose on MMP-2 and TIMP-2 in human endothelial cells. J Cell Biochem 101: 442-50.
56. Reuter B, Rodemer C, Grudzenski S, Couraud PO, et al. 2013. Temporal profile of matrix metalloproteinases and their inhibitors in a human endothelial cell culture model of cerebral ischemia. Cerebrovasc Dis 35: 514-20.
57. Razaq S, Wilkins RJ, Urban JP. 2003. The effect of extracellular pH on matrix turnover by cells of the bovine nucleus pulposus. Eur Spine J 12: 341-9.
58. Afonso S, Romagnano L, Babiarz B. 1999. Expression of cathepsin proteinases by mouse trophoblast in vivo and in vitro. Dev Dyn 216: 374-84.
59. Afonso S, Romagnano L, Babiarz B. 1997. The expression and function of cystatin C and cathepsin B and cathepsin L during mouse embryo implantation and placentation. Development 124: 3415-25.
60. Mohamed MM, Sloane BF. 2006. Cysteine cathepsins: multifunctional enzymes in cancer. Nat Rev Cancer 6: 764-75.
61. Rozhin J, Sameni M, Ziegler G, Sloane BF. 1994. Pericellular pH affects distribution and secretion of cathepsin B in malignant cells. Cancer Res 54: 6517-25.
62. Stern R, Shuster S, Neudecker BA, Formby B. 2002. Lactate stimulates fibroblast expression of hyaluronan and CD44: the Warburg effect revisited. Exp Cell Res 276: 24-31.
63. Rudrabhatla SR, Mahaffey CL, Mummert ME. 2006. Tumor microenvironment modulates hyaluronan expression: the lactate effect. J Invest Dermatol 126: 1378-87.
64. Rogers PA, Murphy CR, Rogers AW, Gannon BJ. 1983. Capillary patency and permeability in the endometrium surrounding the implanting rat blastocyst. Int J Microcirc Clin Exp 2: 241-9.
65. Ghani QP, Wagner S, Becker HD, Hunt TK, et al. 2004. Regulatory role of lactate in wound repair. Methods Enzymol 381: 565-75.
66. Trabold O, Wagner S, Wicke C, Scheuenstuhl H, et al. 2003. Lactate and oxygen constitute a fundamental regulatory mechanism in wound healing. Wound Repair Regen 11: 504-9.
67. Halder JB, Zhao X, Soker S, Paria BC, et al. 2000. Differential expression of VEGF isoforms and VEGF(164)-specific receptor neuropilin-1 in the mouse uterus suggests a role for VEGF(164) in vascular permeability and angiogenesis during implantation. Genesis 26: 213-24.
68. Shi Q, Le X, Wang B, Abbruzzese JL, et al. 2001. Regulation of vascular endothelial growth factor expression by acidosis in human cancer cells. Oncogene 20: 3751-6.
69. Beckert S, Farrahi F, Aslam RS, Scheuenstuhl H, et al. 2006. Lactate stimulates endothelial cell migration. Wound Repair Regen 14: 321-4.
70. Polet F, Feron O. 2013. Endothelial cell metabolism and tumour angiogenesis: glucose and glutamine as essential fuels and lactate as the driving force. J Intern Med 273: 156-65.
71. Ruan GX, Kazlauskas A. 2013. Lactate engages receptor tyrosine kinases Axl, Tie2, and vascular endothelial growth factor receptor 2 to activate phosphoinositide 3-kinase/Akt and promote angiogenesis. J Biol Chem 288: 21161-72.
72. Vegran F, Boidot R, Michiels C, Sonveaux P, et al. 2011. Lactate influx through the endothelial cell monocarboxylate transporter MCT1 supports an NF-kappaB/IL-8 pathway that drives tumor angiogenesis. Cancer Res 71: 2550-60.
73. Nakamura H, Kimura T, Ogita K, Nakamura T, et al. 2004. NF-kappaB activation at implantation window of the mouse uterus. Am J Reprod Immunol 51: 16-21.
74. Hannan NJ, Paiva P, Meehan KL, Rombauts LJ, et al. 2011. Analysis of fertility-related soluble mediators in human uterine fluid identifies VEGF as a key regulator of embryo implantation. Endocrinology 152: 4948-56.
75. Binder NK, Evans J, Gardner DK, Salamonsen LA, et al. 2014. Endometrial signals improve embryo outcome: functional role of vascular endothelial growth factor isoforms on embryo development and implantation in mice. Hum Reprod 29: 2278-86.
76. Nimbkar-Joshi S, Rosario G, Katkam RR, Manjramkar DD, et al. 2009. Embryo-induced alterations in the molecular phenotype of primate endometrium. J Reprod Immunol 83: 65-71.
77. Lardner A. 2001. The effects of extracellular pH on immune function. J Leukoc Biol 69: 522-30.
78. Choi SY, Collins CC, Gout PW, Wang Y. 2013. Cancer-generated lactic acid: a regulatory, immunosuppressive metabolite? J Pathol 230: 350-5.
79. Singer K, Gottfried E, Kreutz M, Mackensen A. 2011. Suppression of T-cell responses by tumor metabolites. Cancer Immunol Immunother 60: 425-31.
80. Gottfried E, Kreutz M, Mackensen A. 2012. Tumor metabolism as modulator of immune response and tumor progression. Semin Cancer Biol 22: 335-41.
81. Calcinotto A, Filipazzi P, Grioni M, Iero M, et al. 2012. Modulation of microenvironment acidity reverses anergy in human and murine tumor-infiltrating T lymphocytes. Cancer Res 72: 2746-56.
82. Fischer K, Hoffmann P, Voelkl S, Meidenbauer N, et al. 2007. Inhibitory effect of tumor cell-derived lactic acid on human T cells. Blood 109: 3812-9.
83. Aluvihare VR, Kallikourdis M, Betz AG. 2004. Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol 5: 266-71.
84. Gorelik L, Flavell RA. 2002. Transforming growth factor-beta in T-cell biology. Nat Revi Immunol 2: 46-53.
85. Chen W, Jin W, Hardegen N, Lei KJ, et al. 2003. Conversion of peripheral CD4 + CD25- naive T cells to CD4 + CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med 198: 1875-86.
86. Clark DA, Fernandes J, Banwatt D. 2008. Prevention of spontaneous abortion in the CBA x DBA/2 mouse model by intravaginal TGF-beta and local recruitment of CD4+8+ FOXP3+ cells. Am J Reprod Immunol 59: 525-34.
87. Seliger C, Leukel P, Moeckel S, Jachnik B, et al. 2013. Lactate-modulated induction of THBS-1 activates transforming growth factor (TGF)-beta2 and migration of glioma cells in vitro. PLoS One 8: e78935.
88. Yabu M, Shime H, Hara H, Saito T, et al. 2011. IL-23-dependent and -independent enhancement pathways of IL-17A production by lactic acid. Int Immunol 23: 29-41.
89. Hunt JS. 1989. Cytokine networks in the uteroplacental unit: macrophages as pivotal regulatory cells. J Reprod Immunol 16: 1-17.
90. Colegio OR, Chu NQ, Szabo AL, Chu T, et al. 2014. Functional polarization of tumour-associated macrophages by tumour-derived lactic acid. Nature 513: 559-63.
91. Zhang S, Lin H, Kong S, Wang S, et al. 2013. Physiological and molecular determinants of embryo implantation. Mol Aspects Med 34: 939-80.
92. Wang H, Dey SK. 2006. Roadmap to embryo implantation: clues from mouse models. Nat Rev Genet 7: 185-99.
93. Hall BV. 1936. Variations in acidity and oxidation-reduction potential of rodent uterine fluids. Phyiol Zool 9: 471-97.
94. Xiao S, Ye X. 2013. Acidification of uterine luminal epithelium is critical for embryo implantation in mice. Biol Reprod The Annual Meeting of the Society for the Study of Reproduction, abstract 869.