Гены и свет: много лет спустя
https://doi.org/10.18699/VJ17.265
Аннотация
Статья написана к 100-летию со дня рождения Д.К. Беляева и затрагивает его работы, посвященные влиянию фотопериодических условий на размножение и эмбриональное развитие млекопитающих. В качестве одной из моделей в этих исследованиях была использована грузинская белая мутация у лисиц (W G). В контрольных условиях способность гомозигот по этой мутации успешно пройти имплантацию резко снижена. Экспериментальное удлинение светового дня для беременных самок из W G/w × W G/w скрещиваний ведет к значительному возрастанию частоты мутантных гомозигот в потомстве. В статье предпринята попытка анализа результатов этой работы в свете современных данных. Грузинская белая мутация, вероятно, обусловливает снижение экспрессии гена KIT. Рассмотрение молекулярных и клеточных взаимодействий с участием белка KIT, его лиганда KITLG и их влияния на развитие бластоцист указывает на возможность замедленного развития W G/W G бластоцист и, как следствие, опоздание к началу имплантации. Изменение фотопериодических условий может через стимулирование развития W G/W G гомозиготных бластоцист, замедление роста трофобласта у зрелых бластоцист, повышение готовности эндометрия и вероятную задержку начала имплантации создавать более благоприятные обстоятельства для успешной имплантации W G/W G бластоцист.
Список литературы
1. An X., Song Y., Bu S., Ma H., Gao K., Hou J., Wang S., Lei Z., Cao B. Association of polymorphisms at the microRNA binding site of the caprine KITLG 3′-UTR with litter size. Sci. Rep. 2016;6:25691.
2. Arceci R.J., Pampfer S., Pollard J.W. Expression of CSF-1/c-fms and SF/c-kit mRNA during preimplantation mouse development. Dev. Biol. 1992;151(1):1-8.
3. Belyaev D.K., Klochkov D.V., Zhelezova A.I. Influence of light conditions on the reproductive function and fertility in mink (Mustela vison Schr). Byulleten Moskovskogo obshchestva ispytateley prirody = Bulletin of Moscow Society of Naturalists. 1963;68(2):107-125. (in Russian)
4. Belyaev D.K., Trut L.N., Ruvinsky A.O. Allelic relationship between the Georgian white, platinum, and white-faced mutations in foxes. Genetika = Genetics (Moscow). 1973a;IX(10):71-77. (in Russian)
5. Belyaev D.K., Trut L.N., Ruvinsky A.O. Genetically determined lethality and possibilities of eliminating its effect in foxes. Genetika = Genetics (Moscow). 1973b;IX(9):71-82. (in Russian)
6. Belyaev D.K., Trut L.N., Ruvinsky A.O. Genetics of the W locus in foxes and expression of its lethal effects. J. Heredity. 1975;66:331-338.
7. Berlinguer F., Leoni G.G., Succu S., Spezzigu A., Madeddu M., Satta V., Bebbere D., Contreras- Solis I., Gonzalez-Bulnes A., Naitana S. Exogenous melatonin positively influences follicular dynamics, oocyte developmental competence and blastocyst output in a goat model. J. Pineal Res. 2009;46(4):383-391.
8. Bernstein A., Chabot B., Dubreuil P., Reith A., Nocka K., Majumder S., Ray P., Besmer P. The mouse W/c-kit locus. Ciba Found. Symp. 1990;148:158-166.
9. Bilban M., Ghaffari-Tabrizi N., Hintermann E., Bauer S., Molzer S., Zoratti C., Malli R., Sharabi A., Hiden U., Graier W., Knöfler M., Andreae F., Wagner O., Quaranta V., Desoye G. Kisspeptin-10, a KiSS-1/ metastin-derived decapeptide, is a physiological invasion inhibitor of primary human trophoblasts. J. Cell Sci. 2004;117(8):1319-1328.
10. Blechman J.M., Lev S., Barg J., Eisenstein M., Vaks B., Vogel Z., Givol D., Yarden Y. The fourth immunoglobulin domain of the stem cell factor receptor couples ligand binding to signal transduction. Cell. 1995;80(1):103-113.
11. Bourdiec A., Calvo E., Rao C.V., Akoum A. Transcriptome analysis reveals new insights into the modulation of endometrial stromal cell receptive phenotype by embryo-derived signals interleukin-1 and human chorionic gonadotropin: possible involvement in early embryo implantation. PLoS ONE. 2013;8(5):e64829.
12. Bourdiec A., Shao R., Rao C.V., Akoum A. Human chorionic gonadotropin triggers angiogenesis via the modulation of endometrial stromal cell responsiveness to interleukin 1: a new possible mechanism underlying embryo implantation. Biol. Reprod. 2012;87(3):66.
13. Calder M., Chan Y.M., Raj R., Pampillo M., Elbert A., Noonan M., Gillio-Meina C., Caligioni C., Bérubé N.G., Bhattacharya M., Watson A.J., Seminara S.B., Babwah A.V. Implantation failure in female Kiss1–/– mice is independent of their hypogonadic state and can be partially rescued by leukemia inhibitory factor. Endocrinology. 2014;155(8):3065-3078.
14. Castellano J.M., Wright H., Ojeda S.R., Lomniczi A. An alternative transcription start site yields estrogen unresponsive Kiss1 mRNA transcripts in the hypothalamus of prepubertal female rats. Neuroendocrinology. 2014;99(2):94-107.
15. Chabot B., Stephenson D.A., Chapman V.M., Besmer P., Bernstein A. The proto-oncogene c- kit encoding a trans-membrane tyrosine kinase receptor maps to the mouse W locus. Nature. 1988;335:88-89.
16. Chuffa L.G., Seiva F.R., Fávaro W.J., Teixeira G.R., Amorim J.P., Mendes L.O., Fioruci B.A., Pinheiro P.F., Fernandes A.A., Franci J.A., Delella F.K., Martinez M., Martinez F.E. Melatonin reduces LH, 17 beta-estradiol and induces differential regulation of sex steroid receptors in reproductive tissues during rat ovulation. Reprod. Biol. Endocrinol. 2011;9:108.
17. Drube S., Schmitz F., Göpfert C., Weber F., Kamradt T. C-Kit controls IL-1β-induced effector functions in HMC-cells. Eur. J. Pharmacol. 2012;675(1-3):57-62.
18. Elvin J.A., Clark A.T., Wang P., Wolfman N.M., Matzuk M.M. Paracrine actions of growth differentiation factor-9 in the mammalian ovary. Mol. Endocrinol. 1999;13(6):1035-1048.
19. England G. Dog Breeding, Whelping and Puppy Care. John Wiley & Sons, 2012.
20. Farstad W. Reproduction in foxes: current research and future challenges. Anim. Reprod. Sci. 1998;53(1-4):35-42.
21. Fontanesi L., Vargiolu M., Scotti E., Latorre R., Faussone Pellegrini M.S., Mazzoni M., Asti M., Chiocchetti R., Romeo G., Clavenzani P., De Giorgio R. The KIT gene is associated with the English spotting coat color locus and congenital megacolon in Checkered Giant rabbits (Oryctolagus cuniculus). PLoS ONE. 2014; 9(4):e93750.
22. Furmento V.A., Marino J., Blank V.C., Cayrol M.F., Cremaschi G.A., Aguilar R.C., Roguin L.P. Granulocyte colony-stimulating factor (G-CSF) upregulates β1 integrin and increases migration of human trophoblast Swan 71 cells via PI3K and MAPK activation. Exp. Cell Res. 2016;342(2):125-134.
23. Gao Q., Lv J., Li W., Zhang P., Tao J., Xu Z. Disrupting the circadian photo-period alters the release of follicle-stimulating hormone, luteinizing hormone, progesterone, and estradiol in maternal and fetal sheep. J. Reprod. Dev. 2016;62(5):487-493.
24. Gilchrist R.B., Lane M., Thompson J.G. Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum. Reprod. Update. 2008;14(2):159-177.
25. Głabowski W. The protective effect of stem cell factor (SCF) on in vitro development of preimplantation mouse embryos. Ann. Acad. Med. Stetin. 2005;51:83-93.
26. Gómez-Brunet A., Santiago-Moreno J., del Campo A., Malpaux B., Chemineau P., Tortonese D.J., Gonzalez-Bulnes A., López-Sebastián A. Endogenous circannual cycles of ovarian activity and changes in prolactin and melatonin secretion in wild and domestic female sheep maintained under a long-day photoperiod. Biol. Reprod. 2008;78(3):552-562.
27. Gräs S., Georg B., Jørgensen H.L., Fahrenkrug J. Expression of the clock genes Per1 and Bmal1 during follicle development in the rat ovary. Effects of gonadotropin stimulation and hypophysectomy. Cell Tissue Res. 2012;350(3):539-548.
28. Hartley F.G.L., Follett B.K., Harris S., Hirst D., McNeilly A.S. The endocrinology of gestation failure in foxes (Vulpes vulpes). J. Reproduct. Fertility. 1994;100:341-346.
29. He C., Wang J., Li Y., Zhu K., Xu Z., Song Y., Song Y., Liu G. Melatoninrelated genes expressed in the mouse uterus during early gestation promote embryo implantation. J. Pineal Res. 2015;58(3):300-309.
30. Hirata M., He P.J., Shibuya N., Uchikawa M., Yamauchi N., Hashimoto S., Hattori M.A. Progesterone, but not estradiol, synchronizes circadian oscillator in the uterus endometrial stromal cells. Mol. Cell Biochem. 2009;324(1-2):31-38.
31. Huang E.J., Nocka K.H., Buck J., Besmer P. Differential expression and processing of two cell associated forms of the kit-ligand: KL-1 and KL-2. Mol. Biol. Cell. 1992;3(3):349-362.
32. Hutt K.J., McLaughlin E.A., Holland M.K. Kit ligand and c-Kit have diverse roles during mammalian oogenesis and folliculogenesis. Mol. Hum. Reprod. 2006;12(2):61-69.
33. Jeong W., Kim J., Bazer F.W., Song G. Proliferation-stimulating effect of colony stimulating factor 2 on porcine trophectoderm cells is mediated by activation of phosphatidylinositol 3- kinase and extracellular signal-regulated kinase 1/2 mitogen-activated protein kinase. PLoS ONE. 2014;9(2):e88731.
34. Johnson J.L., Kozysa A., Kharlamova A.V., Gulevich R.G., Perelman P.L., Fong H.W., Vladimirova A.V., Oskina I.N., Trut L.N., Kukekova A.V. Platinum coat color in red fox (Vulpes vulpes) is caused by a mutation in an autosomal copy of KIT. Anim. Genet. 2015;46(2):190-199.
35. Kameyoshi Y., Morita E., Tanaka T., Hiragun T., Yamamoto S. Interleukin-1α enhances mast cell growth by a fibroblast-dependent mechanism. Arch. Dermatol. Res. 2000;292(5):240-247.
36. Kandalepas P.C., Mitchell J.W., Gillette M.U. Melatonin signal transduction pathways require E-box-mediated transcription of Per1 and Per2 to reset the SCN clock at dusk. PLoS ONE. 2016;11(6): e0157824.
37. Kauma S., Huff T., Krystal G., Ryan J., Takacs P., Turner T. The expression of stem cell factor and its receptor, c-kit in human endometrium and placental tissues during pregnancy. J. Clin. Endocrinol. Metab. 1996;81(3):1261-1266.
38. Kim T.H., Lee D.K., Franco H.L., Lydon J.P., Jeong J.W. ERBB receptor feedback inhibitor 1 regulation of estrogen receptor activity is critical for uterine implantation in mice. Biol. Reprod. 2010;82(4): 706-713.
39. Kukekova A.V., Johnson J.L., Kharlamova A.V., Vladimirova A.V., Shepeleva D.V., Gulevich R.G., Trut L.N. Georgian white coat color of red fox (Vulpes vulpes) maps to fox chromosome 2 in the region containing KIT gene. Anim. Genet. 2016;47(4):514-515.
40. Lemmon M.A., Pinchasi D., Zhou M., Lax I., Schlessinger J. Kit receptor dimerization is driven by bivalent binding of stem cell factor. J. Biol. Chem. 1997;272(10):6311-6317.
41. Leung P.C.K., Adashi E.Y. The Ovary. Second edition. Elsevier Acad. Press, 2004.
42. Lim J.J., Eum J.H., Lee J.E., Kim E.S., Chung H.M., Yoon T.K., Kim K.S., Lee D.R. Stem cell factor/c-Kit signaling in in vitro cultures supports early mouse embryonic development by accelerating proliferation via a mechanism involving Akt-downstream genes. J. Assist. Reprod. Genet. 2010;27(11):619-627.
43. de Lima P.F., Ormond C.M., Caixeta E., Barros R.G., Price C., Buratini J. KITL regulates meiosis and expression of NPPC in bovine cumulus-oocyte complexes. Reproduction. 2016;16:0155.
44. Linde Forsberg C., Reynaud K. Ch. 14. Biology of reproduction and modern reproductive technology in the dog. The Genetics of the Dog. Ed. by E. Ostrander, A. Ruvinsky. 2012;295-320.
45. Liu Y., Johnson B.P., Shen A.L., Wallisser J.A., Krentz K.J., Moran S.M., Sullivan R., Glover E., Parlow A.F., Drinkwater N.R., Schuler L.A., Bradfield C.A. Loss of BMAL1 in ovarian steroidogenic cells results in implantation failure in female mice. Proc. Natl. Acad. Sci. USA. 2014;111(39):14295-14300.
46. Lu H.S., Clogston C.L., Wypych J., Parker V.P., Lee T.D., Swiderek K., Baltera R.F., Jr., Patel A.C., Chang D.C., Brankow D.W., Liu X.- D., Ogden S.G., Karkare S.B., Hu S.S., Zsebo K.M., Langley K.E. Posttranslational processing of membrane-associated recombinant human stem cell factor expressed in Chinese hamster ovary cells. Arch. Biochem. Biophys. 1992;298:150-158.
47. Mitsunari M., Harada T., Tanikawa M., Iwabe T., Taniguchi F., Terakawa N. The potential role of stem cell factor and its receptor c-kit in the mouse blastocyst implantation. Mol. Hum. Reprod. 1999;5:874-879.
48. Mizuno S., Takami K., Daitoku Y., Tanimoto Y., Dinh T.T., Mizuno-Iijima S., Hasegawa Y., Takahashi S., Sugiyama F., Yagami K. Periimplantation lethality in mice carrying megabase- scale deletion on 5qc3.3 is caused by Exoc1 null mutation. Sci. Rep. 2015;5:13632.
49. Nagle D.L., Kozak C.A., Mano H., Chapman V.M., Bućan M. Physical mapping of the Tec and Gabrb1 loci reveals that the Wsh mutation on mouse chromosome 5 is associated with an inversion. Hum. Mol. Genet. 1995;4(11):2073-2079.
50. Osadchuk L.V., Trut L.N. Photoperiodic control of the gonadal endocrine function in silver- gray foxes and its alteration during domestication. Zhurnal evolyutsionnoy biokhimii i fiziologii = Journal of Evolutionary Biochemistry and Physiology. 1988;24(2):176-183. (in Russian)
51. Otsuka F., Shimasaki S. A negative feedback system between oocyte bone morphogenetic protein 15 and granulosa cell kit ligand: its role in regulating granulosa cell mitosis. Proc. Natl. Acad. Sci. USA. 2002;99(12):8060-8065.
52. Paulson R.J. Hormonal induction of endometrial receptivity. Fertil Steril. 2011;96(3):530-535.
53. de Paula R.M., Lamb T.M., Bennett L., Bell-Pedersen D. A connection between MAPK pathways and circadian clocks. Cell Cycle. 2008; 7(17):2630-2634.
54. Pearson O.P., Enders R.K. Ovulation, maturation and fertilization in the fox. Anatom. Record. 1943;85(1):69-83.
55. Photoperiodism: 1415854_at: Kitl. http://photoperiodism.brainstars.org/probeset/1415854_at inspected on 27.11.2016.
56. Reith A.D., Rottapel R., Giddens E., Brady C., Forrester L., Bernstein A. W mutant mice with mild or severe developmental defects contain distinct point mutations in the kinase domain of the c-kit receptor. Genes Dev. 1990;4(3):390-400.
57. Revel F.G., Saboureau M., Masson-Pévet M., Pévet P., Mikkelsen J.D., Simonneaux V. Kisspeptin mediates the photoperiodic control of reproduction in hamsters. Curr. Biol. 2006;16(17):1730-1735.
58. Rijnberk A., Kooistra H.S. Clinical Endocrinology of Dogs and Cats: An Illustrated Text. Second, revised and extended edition. CRC Press, Taylor & Francis Group, 2010.
59. Saadeldin I.M., Koo O.J., Kang J.T., Kwon D.K., Park S.J., Kim S.J., Moon J.H., Oh H.J., Jang G., Lee B.C. Paradoxical effects of kisspeptin: it enhances oocyte in vitro maturation but has an adverse impact on hatched blastocysts during in vitro culture. Reprod. Fertil. Dev. 2012;24(5):656-668.
60. Sanders K.M., Ward S.M. Interstitial cells of Cajal: a new perspective on smooth muscle function. J. Physiol. 2006;576(Pt. 3):721-726.
61. Semaan S.J., Kauffman A.S. Emerging concepts on the epigenetic and transcriptional regulation of the Kiss1 gene. Int. J. Dev. Neurosci. 2013;31(6):452-462.
62. da Silva E.Z., Jamur M.C., Oliver C. Mast cell function: a new vision of an old cell. J. Histochem. Cytochem. 2014;62(10):698-738.
63. Simonneaux V., Bahougne T. A multi-oscillatory circadian system times female reproduction. Front. Endocrinol. (Lausanne). 2015;6:157.
64. Tamura H., Takayama H., Nakamura Y., Reiter R.J., Sugino N. Fetal/placental regulation of maternal melatonin in rats. J. Pineal. Res. 2008;44(3):335-340.
65. Taniguchi F., Harada T., Nara M., Deura I., Mitsunari M., Terakawa N. Coculture with a human granulosa cell line enhanced the development of murine preimplantation embryos via SCF/c-kit system. J. Assist. Reprod. Genet. 2004;21:223-228.
66. Tasaki H., Zhao L., Isayama K., Chen H., Yamauchi N., Shigeyoshi Y., Hashimoto S., Hattori M.A. Profiling of circadian genes expressed in the uterus endometrial stromal cells of pregnant rats as revealed by DNA microarray coupled with RNA interference. Front. Endocrinol. (Lausanne). 2013;4:82.
67. Tian X.Z., Wen Q., Shi J.M., Liang-Wang, Zeng S.M., Tian J.H., Zhou G.B., Zhu S.E., Liu G.S. Effects of melatonin on in vitro development of mouse two-cell embryos cultured in HTF medium. Endocr. Res. 2010;35(1):17-23.
68. Tuck A.R., Mottershead D.G., Fernandes H.A., Norman R.J., Tilley W.D., Robker R.L., Hickey T.E. Mouse GDF9 decreases KITL gene expression in human granulosa cells. Endocrine. 2015;48(2):686-695.
69. Valenzuela F.J., Vera J., Venegas C., Pino F., Lagunas C. Circadian system and melatonin hormone: risk factors for complications during pregnancy. Obstet. Gynecol. Int. 2015;2015:825802.
70. Valtonen M., Jalkanen L. Species-specific features of oestrous development and blastogenesis in domestic canine species. J. Reprod. Fertil Suppl. 1993;47:133-137.
71. Woidacki K., Popovic M., Metz M., Schumacher A., Linzke N., Teles A., Poirier F., Fest S., Jensen F., Rabinovich G.A., Maurer M., Zenclussen A.C. Mast cells rescue implantation defects caused by c-kit deficiency. Cell Death Dis. 2013;4:e462.
72. Wong A.K., Ruhe A.L., Robertson K.R., Loew E.R., Williams D.C., Neff M.W. A de novo mutation in KIT causes white spotting in a subpopulation of German Shepherd dogs. Anim. Genet. 2013;44(3): 305-310.
73. Yang Q., Gu Y., Zhang X., Wang J.M., He Y.P., Shi Y., Sun Z.G., Shi H.J., Wang J. Uterine expression of NDRG4 is induced by estrogen and up-regulated during embryo implantation process in mice. PLoS ONE. 2016;11(5):e0155491.
74. Yarden Y., Kuang W.J., Yang-Feng T., Coussens L., Munemitsu S., Dull T.J., Chen E., Schlessinger J., Francke U., Ullrich A. Human proto-oncogene c-kit: a new cell surface receptor tyrosine kinase for an unidentified ligand. EMBO J. 1987;6(11):3341-3351.
75. Ye Y., Kawamura K., Sasaki M., Kawamura N., Groenen P., Gelpke M.D., Rauch R., Hsueh A.J., Tanaka T. Kit ligand promotes first polar body extrusion of mouse preovulatory oocytes. Reprod. Biol. Endocrinol. 2009;7:26.
76. Yuzawa S., Opatowsky Y., Zhang Z., Mandiyan V., Lax I., Schlessinger J. Structural basis for activation of the receptor tyrosine kinase KIT by stem cell factor. Cell. 2007;130(2):323-334.
77. Zhang P., Tang M., Zhong T., Lin Y., Zong T., Zhong C., Zhang B., Ren M., Kuang H. Expression and function of kisspeptin during mouse decidualization. PLoS ONE. 2014;9(5):e97647.