Регуляция функций стволовых клеток при помощи циклического аденозинмонофосфата (цАМФ): механизмы и перспективы

Обложка

Цитировать

Полный текст

Открытый доступ Открытый доступ
Доступ закрыт Доступ предоставлен
Доступ закрыт Только для подписчиков

Аннотация

Непрерывное обновление тканей организма является залогом сохранения постоянства их функции в течение жизни человека. Необратимое угасание процессов обновления тканей со временем лежит в основе развития возраст-ассоциированных заболеваний и определяет процесс старения. Кроме того, с нарушением тканевого обновления связано развитие социально значимых заболеваний, таких как метаболический синдром, сахарный диабет 2 типа, остеопороз и многие другие. Определяющую роль в процессе обновления тканей и их адаптации к изменяющимся условиям играют постнатальные стволовые клетки. При этом в течение жизни происходит поддержание постоянного баланса между скоростью процессов клеточного роста и гибели. Нарушение этого баланса может вести как к развитию дегенеративных процессов, так и к развитию онкологических заболеваний. Поэтому активность стволовых клеток находится под строгим контролем со стороны нервной и эндокринной систем организма. В то же время, несмотря на широкий спектр гормонов и нейромедиаторов, действующих на стволовые клетки, спектр внутриклеточных сигналов, обеспечивающих проведение информации, крайне ограничен. Универсальные системы вторичных мессенджеров формируют уникальные клеточные ответы на различные стимулы, используя специализированные системы регуляции и модуляции сигнала. Одним из вторичных мессенджеров, обеспечивающих передачу внутриклеточных сигналов, является циклический аденозинмонофосфат (цАМФ), синтезируемый аденилатциклазой. Этот сигнальный путь включает в себя рецепторы, сопряженные с G-белками (GPCR), различные изоформы аденилатциклаз, а также широкий спектр каркасных и эффекторных белков. Работая вместе, они обеспечивают фокусировку сигнала цАМФ и реализуют программы либо по поддержанию стволовости, либо наоборот, по запуску дифференцировки в различных направлениях. Целью нашего обзора является обсудить организацию и компартментализацию сигнализации цАМФ в стволовых клетках, а также ее участие в регуляции процессов поддержания стволового состояния и индукции дифференцировки в различных направлениях.

Об авторах

В. А. Усачёв

Московский государственный университет им. М.В. Ломоносова

Email: usachjov-vova@mail.ru
ORCID iD: 0000-0003-1564-0644
аспирант Москва

П. А. Тюрин-Кузьмин

Московский государственный университет им. М.В. Ломоносова

Email: tyurinkuzminpa@my.msu.ru
ORCID iD: 0000-0002-1901-1637
д.б.н, доцент Москва

А. А. Зиновьева

Московский государственный университет им. М.В. Ломоносова

Email: zinovevaanna356@gmail.com
ORCID iD: 0009-0007-3068-1678
аспирант Москва

И. В. Зубарев

Московский физико-технический институт

Email: ilyamitozubarev@gmail.com
ORCID iD: 0000-0002-7827-498X
к.б.н., с.н.с., заведующий лабораторией Долгопрудный

К. Ю. Кулебякин

Московский государственный университет им. М.В. Ломоносова

Email: konstantin-kuleb@mail.ru
ORCID iD: 0000-0001-6954-5787
к.б.н, доцент Москва

М. В. Воронцова

Московский государственный университет им. М.В. Ломоносова

Email: maria.v.vorontsova@mail.ru
ORCID iD: 0000-0002-9124-294X
к.м.н., заведующая лабораторией Москва

В. А. Ткачук

Московский государственный университет им. М.В. Ломоносова

Email: tkachuk@fbm.msu.ru
ORCID iD: 0000-0002-7492-747
д.б.н., академик РАН, директор Москва

Список литературы

  1. Abdel-Halim S.M. et al. Increased Plasma Levels of Adenylate Cyclase 8 and cAMP Are Associated with Obesity and Type 2 Diabetes: Results from a Cross-Sectional Study // Biology. 2020. Vol. 9. № 9. P. 244. https://doi.org/10.3390/biology9090244
  2. Bayewitch M.L. et al. Inhibition of adenylyl cyclase isoforms V and Vol. by various Gβγ subunits // The FASEB Journal. 1998. Vol. 12. № 11. P. 1019–1025. https://doi.org/10.1096/fasebj.12.11.1019
  3. Beazely M.A., Watts V.J. Regulatory properties of adenylate cyclases type 5 and 6: A progress report // European Journal of Pharmacology. 2006. Vol. 535. P. 1–12. https://doi.org/10.1016/j.ejphar.2006.01.054
  4. Boguslawski G. et al. Activation of Osteocalcin Transcription Involves Interaction of Protein Kinase A- and Protein Kinase C-dependent Pathways // Journal of Biological Chemistry. 2000. Vol. 275. № 2. P. 999–1006. https://doi.org/10.1074/jbc.275.2.999
  5. Boyce A.M., Collins M.T. Fibrous dysplasia/McCune-Albright syndrome: a rare, mosaic disease of Gα s activation // Endocrine reviews. 2020. Vol. 41. № 2. P. 345–370. https://doi.org/10.1210/endrev/bnz011
  6. Brand T. The Popeye Domain-Containing Gene Family // CBB. 2005. Vol. 43. № 1. P. 95–104. https://doi.org/10.1385/CBB:43:1:095
  7. Bundey R.A., Insel P.A. Adenylyl Cyclase 6 Overexpression Decreases the Permeability of Endothelial Monolayers via Preferential Enhancement of Prostacyclin Receptor Function // Molecular Pharmacology November. 2006. V. 70. № 5. P. 1700–1707. https://doi.org/10.1124/mol.106.028035
  8. Carroll S.H., Ravid K. Differentiation of mesenchymal stem cells to osteoblasts and chondrocytes: a focus on adenosine receptors // Expert Rev. Mol. Med. 2013. Vol. 15. P. e1. https://doi.org/10.1017/erm.2013.2
  9. Chan W.C.W., Tan Z., To M.K.T., Chan D. Regulation and Role of Transcription Factors in Osteogenesis // IJMS. 2021. Vol. 22. № 11. P. 5445. https://doi.org/10.3390/ijms22115445
  10. Chen B., Lin T., Yang X., Li Y., Xie D., Cui H. Intermittent parathyroid hormone (1–34) application regulates cAMP-response element binding protein activity to promote the proliferation and osteogenic differentiation of bone mesenchymal stromal cells, via the cAMP/PKA signaling pathway // Experimental and Therapeutic Medicine. 2016. Vol. 11. № 6. P. 2399–2406. https://doi.org/10.3892/etm.2016.3177
  11. Chen H.Y., Liu Q., Salter A.M., Lomax M.A. Synergism between cAMP and PPAR γ Signalling in the Initiation of UCP1 Gene Expression in HIB1B Brown Adipocytes // PPAR Research. 2013. Vol. 2013. P. 1–8. https://doi.org/10.1155/2013/476049
  12. De Rooij J. et al. Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP // Nature. 1998. Vol. 396. № 6710. P. 474–477. https://doi.org/10.1038/24884
  13. Dessauer C.W. Adenylyl Cyclase–A-kinase Anchoring Protein Complexes: The Next Dimension in cAMP Signaling // Mol. Pharmacol. 2009. Vol. 76. № 5. P. 935–941. https://doi.org/10.1124/mol.109.059345
  14. Dessauer C.W., Watts V.J., Ostrom R.S., Conti M., Dove S., Seifert R. International Union of Basic and Clinical Pharmacology. CI. Structures and Small Molecule Modulators of Mammalian Adenylyl Cyclases // Pharmacol. Rev. 2017. Vol. 69. № 2. P. 93–139. https://doi.org/10.1124/pr.116.013078
  15. Devasani K., Yao Y. Expression and functions of adenylyl cyclases in the CNS // Fluids and Barriers of the CNS. 2022. Vol. 19. № 1. P. 23. https://doi.org/10.1186/s12987-022-00322-2
  16. Fan Q. et al. The CREB–Smad6–Runx2 axis contributes to the impaired osteogenesis potential of bone marrow stromal cells in fibrous dysplasia of bone // The Journal of Pathology. 2012. Vol. 228. № 1. P. 45–55. https://doi.org/10.1002/path.4033
  17. Farmer S.R. Transcriptional control of adipocyte formation // Cell Metabolism. 2006. Vol. 4. № 4. P. 263–273. https://doi.org/10.1016/j.cmet.2006.07.001
  18. Fesenko E.E., Kolesnikov S.S., Lyubarsky A.L. Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment // Nature. 1985. Vol. 313. № 6000. P. 310–313. https://doi.org/10.1038/313310a0
  19. Fritz A.L., Adil M.M., Mao S.R., Schaffer D.V. cAMP and EPAC Signaling Functionally Replace OCT4 During Induced Pluripotent Stem Cell Reprogramming // Molecular Therapy. 2015. Vol. 23. № 5. P. 952–963. https://doi.org/10.1038/mt.2015.28
  20. Gabrielli M., Martini C.N., Brandani J.N., Iustman L.J.R., Romero D.G., Vila M.D.C. Exchange protein activated by cyclic AMP is involved in the regulation of adipogenic genes during 3T3‐L1 fibroblasts differentiation // Dev. Growth Differ. 2014. Vol. 56. № 2. P. 143–151. https://doi.org/10.1111/dgd.12114
  21. Gancedo J.M. Biological roles of cAMP: variations on a theme in the different kingdoms of life // Biol. Rev. Camb. Philos. Soc. 2013. Vol. 88. № 3. P. 645–668. https://doi.org/10.1111/brv.12020
  22. Grarup N. et al. Loss-of-function variants in ADCY3 increase risk of obesity and type 2 diabetes // Nat. Genet. 2018. Vol. 50. № 2. P. 172–174. https://doi.org/10.1038/s41588-017-0022-7
  23. Hanoune J., Defer N. Regulation and Role of Adenylyl Cyclase Isoforms // Annu. Rev. Pharmacol. Toxicol. 2001. Vol. 41. № 1. P. 145–174. https://doi.org/10.1146/annurev.pharmtox.41.1.145
  24. He S., Choi Y.H., Choi J., Yeo C., Chun C., Lee K.Y. Protein Kinase A Regulates the Osteogenic Activity of Osterix // J. of Cellular Biochemistry. 2014. Vol. 115. № 10. P. 1808–1815. https://doi.org/10.1002/jcb.24851
  25. Herzig S., Hedrick S., Morantte I., Koo S.-H., Galimi F., Montminy M. CREB controls hepatic lipid metabolism through nuclear hormone receptor PPAR-g // Nature. 2003. Vol. 426. P. 190–193. https://doi.org/10.1038/nature02110
  26. Hirota K., Hirashima T., Horikawa K., Yasoda A., Matsuda M. C-type Natriuretic Peptide–induced PKA Activation Promotes Endochondral Bone Formation in Hypertrophic Chondrocytes // Endocrinology. 2022. Vol. 163. № 3. P. bqac005. https://doi.org/10.1210/endocr/bqac005
  27. Ho W.C., Greene R.M., Shanfeld J., Davidovitch Z. Cyclic nucleotides during chondrogenesis: Concentration and distribution in vivo and in vitro // Journal of Experimental Zoology. 1982. Vol. 224. № 3. P. 321–330. https://doi.org/10.1002/jez.1402240305
  28. Hong S.H.H., Lu X., Nanes M.S., Mitchell J. Regulation of osterix (Osx, Sp7) and the Osx promoter by parathyroid hormone in osteoblasts // Journal of Molecular Endocrinology. 2009. Vol. 43. № 5. P. 197–207. https://doi.org/10.1677/JME-09-0012
  29. Huang W., Zhou X., Lefebvre V., Crombrugghe B.D. Phosphorylation of SOX9 by Cyclic AMP-Dependent Protein Kinase A Enhances SOX9’s Ability To Transactivate a Col2a1 Chondrocyte-Specific Enhancer // MOL. CELL. BIOL. 2000. Vol. 20. P. 149–158. https://doi.org/10.1128/MCB.20.11.4149-4158.2000
  30. Jarnaess E., Taskén K. Spatiotemporal control of cAMP signalling processes by anchored signalling complexes // Biochemical Society Transactions. 2007. Vol. 35. № 5. P. 931–937. https://doi.org/10.1042/BST0350931
  31. Ji Z. Epac not PKA catalytic subunit is required for 3T3-L1 preadipocyte differentiation // Front. Biosci. 2010. V. E2. № 2. P. 392–398. https://doi.org/10.2741/e99
  32. Jia B. et al. Activation of Protein Kinase A and Exchange Protein Directly Activated by cAMP Promotes Adipocyte Differentiation of Human Mesenchymal Stem Cells // PLoS ONE. 2012. Vol. 7. № 3. P. e34114. https://doi.org/10.1371/journal.pone.0034114
  33. Juhász T. et al. Mechanical loading stimulates chondrogenesis via the PKA/CREB-Sox9 and PP2A pathways in chicken micromass cultures // Cellular Signalling. 2014. Vol. 26. № 3. P. 468–482. https://doi.org/10.1016/j.cellsig.2013.12.001
  34. Kao R., Lu W., Louie A., Nissenson R. Cyclic AMP signaling in bone marrow stromal cells has reciprocal effects on the ability of mesenchymal stem cells to differentiate into mature osteoblasts versus mature adipocytes // Endocrine. 2012. Vol. 42. P. 622–636. https://doi.org/10.1007/s12020-012-9717-9
  35. Khani S. et al. Cold-induced expression of a truncated Adenylyl Cyclase 3 acts as rheostat to brown fat function // Nature Metabolism. 2024. Vol. 6. P. 1053–1075. https://doi.org/10.1038/s42255-024-01033-8
  36. Kim J. et al. An activator of the cAMP/PKA/CREB pathway promotes osteogenesis from human mesenchymal stem cells // Journal Cellular Physiology. 2013. Vol. 228. № 3. P. 617–626. https://doi.org/10.1002/jcp.24171
  37. Kim J.S., Hong Y.J., Choi H.W., Choi S., Do J.T. Protein Kinase A Signaling Is Inhibitory for Reprogramming into Pluripotent Stem Cells // Stem Cells and Development. 2016. Vol. 25. № 5. P. 378–385. https://doi.org/10.1089/scd.2015.0333
  38. Kim K., Lee Y. Activation of CREB by PKA promotes the chondrogeneic differentiation of chick limb bud mesenchymal cells // Animal Cells and Systems. 2009. Vol. 13. № 3. P. 289–295. https://doi.org/10.1080/19768354.2009.9647221
  39. Kim S. et al. Transcriptional activation of peroxisome proliferator-activated receptor-γ requires activation of both protein kinase A and Akt during adipocyte differentiation // Biochemical and Biophysical Research Communications. 2010. Vol. 399. № 1. P. 55–59. https://doi.org/10.1016/j.bbrc.2010.07.038
  40. Kosher R.A. et al. Cartilage proteoglycan core protein gene expression during limb cartilage differentiation // Developmental Biology. 1986. Vol. 118. № 1. P. 112–117. https://doi.org/10.1016/0012-1606(86)90078-3
  41. Kulebyakin K. et al. Dynamic balance between pth1r-dependent signal cascades determines its pro-or anti-osteogenic effects on MSC // Cells. 2022. Vol. 11. № 21. P. 3519. https://doi.org/10.3390/cells11213519
  42. Layden B.T., Newman M., Chen F., Fisher A., Lowe W.L. G Protein Coupled Receptors in Embryonic Stem Cells: A Role for Gs-Alpha Signaling // PLoS ONE. 2010. Vol. 5. № 2. P. e9105. https://doi.org/10.1371/journal.pone.0009105
  43. Lazennec G., Canaple L., Saugy D., Wahli W. Activation of Peroxisome Proliferator-Activated Receptors (PPARs) by Their Ligands and Protein Kinase A Activators // Biochem. Biophys. Res. Commun. 2000. Vol. 14. № 12. P. 1962–1975. https://doi.org/10.1210/mend.14.12.0575
  44. Lee J.Y. et al. Pre-transplantational Control of the Post-transplantational Fate of Human Pluripotent Stem Cell-Derived Cartilage // Stem. Cell Reports. 2018. Vol. 11. № 2. P. 440–453. https://doi.org/10.1016/j.stemcr.2018.06.021
  45. Lo K.W.-H., Kan H.M., Ashe K.M., Laurencin C.T. The small molecule PKA-specific cyclic AMP analogue as an inducer of osteoblast-like cells differentiation and mineralization // J. Tissue Eng. Regen. Med. 2012. Vol. 6. № 1. P. 40–48. https://doi.org/10.1002/term.395
  46. Lohse C. et al. Experimental and mathematical analysis of cAMP nanodomains // PLoS ONE. 2017. Vol. 12. № 4. P. e0174856. https://doi.org/10.1371/journal.pone.0174856
  47. Malemud C.J., Papay R.S., Hering T.M. Forskolin Stimulates Aggrecan Gene Expression in Cultured Bovine Chondrocytes // American Journal of Therapeutics. 1996. Vol. 3. № 2. P. 120–128. https://doi.org/10.1097/00045391-199602000-00005
  48. McIntire W.E., MacCleery G., Garrison J.C. The G protein β subunit is a determinant in the coupling of Gs to the β1-adrenergic and A2a adenosine receptors // Journal of Biological Chemistry. 2001. Vol. 276. № 19. P. 15801–15809. https://doi.org/10.1074/jbc.M011233200
  49. Miki H., Okito A., Akiyama M., Ono T., Tachikawa N., Nakahama K. Genetic and epigenetic regulation of osteopontin by cyclic adenosine 3′ 5′-monophosphate in osteoblasts // Gene. 2020. Vol. 763. P. 145059. https://doi.org/10.1016/j.gene.2020.145059
  50. Miller R.P., Husain M., Lohin S. Long acting cAMP analogues enhance sulfate incorporation into matrix proteoglycans and suppress cell division of fetal rat chondrocytes in monolayer culture // J. Cell Physiol. 1979. Vol. 100. № 1. P. 63–76. https://doi.org/10.1002/jcp.1041000107
  51. Minakawa T., Kanki Y., Nakamura K., Yamashita J.K. Protein kinase A accelerates the rate of early stage differentiation of pluripotent stem cells // Biochemical and Biophysical Research Communications. 2020. Vol. 524. № 1. P. 57–63. https://doi.org/10.1016/j.bbrc.2019.12.098
  52. Mirsaidi A., Tiaden A.N., Richards P.J. Prostaglandin E2 inhibits matrix mineralization by human bone marrow stromal cell-derived osteoblasts via Epac-dependent cAMP signaling // Sci. Rep. 2017. Vol. 7. № 1. P. 2243. https://doi.org/10.1038/s41598-017-02650-y
  53. Norman D. et al. ACTH and a-MSH inhibit leptin expression and secretion in 3T3-L1 adipocytes: model for a centralÁ/peripheral melanocortin-leptin pathway // Molecular and Cellular Endocrinology. 2003. Vol. 200. P. 99–109. https://doi.org/10.1016/s0303-7207(02)00410-0
  54. Petersen R.K. et al. Cyclic AMP (cAMP)-Mediated Stimulation of Adipocyte Differentiation Requires the Synergistic Action of Epac- and cAMP-Dependent Protein Kinase-Dependent Processes // Molecular and Cellular Biology. 2008. Vol. 28. № 11. P. 3804–3816. https://doi.org/10.1128/MCB.00709-07
  55. Pidoux G. et al. Optic atrophy 1 is an A-kinase anchoring protein on lipid droplets that mediates adrenergic control of lipolysis: OPA1 is an AKAP for perilipin // The EMBO Journal. 2011. Vol. 30. № 21. P. 4371–4386. https://doi.org/10.1038/emboj.2011.365
  56. Pitman J.L., Wheeler M.C., Lloyd D.J., Walker J.R., Glynne R.J., Gekakis N. A Gain-of-Function Mutation in Adenylate Cyclase 3 Protects Mice from Diet-Induced Obesity // PLoS ONE. 2014. Vol. 9. № 10. P. e110226. https://doi.org/10.1371/journal.pone.0110226
  57. Riffault M., Johnson G.P., Owen M.M., Javaheri B., Pitsillides A.A., Hoey D.A. Loss of Adenylyl Cyclase 6 in Leptin Receptor‐Expressing Stromal Cells Attenuates Loading‐Induced Endosteal Bone Formation // JBMR Plus. 2020. Vol. 4. № 11. P. e10408. https://doi.org/10.1002/jbm4.10408
  58. Rogne M., Chu D.-T., Küntziger T.M., Mylonakou M.-N., Collas P., Tasken K. OPA1-anchored PKA phosphorylates perilipin 1 on S522 and S497 in adipocytes differentiated from human adipose stem cells // MBoC. 2018. Vol. 29. № 12. P. 1487–1501. https://doi.org/10.1091/mbc.E17-09-0538
  59. Rogne M., Taskén K. Compartmentalization of cAMP signaling in adipogenesis, lipogenesis, and lipolysis // Hormone and Metabolic Research. 2014. Vol. 46. № 12. P. 833–840. https://doi.org/10.1055/s-0034-1389955
  60. Rumiński S., Kalaszczyńska I., Lewandowska-Szumieł M. Effect of cAMP Signaling Regulation in Osteogenic Differentiation of Adipose-Derived Mesenchymal Stem Cells // Cells. 2020. Vol. 9. № 7. P. 1587. https://doi.org/10.3390/cells9071587
  61. Rybinska I., Mangano N., Tagliabue E., Triulzi T. Cancer-Associated Adipocytes in Breast Cancer: Causes and Consequences // IJMS. 2021. Vol. 22. № 7. P. 3775. https://doi.org/10.3390/ijms22073775
  62. Saeed S. et al. Loss-of-function mutations in ADCY3 cause monogenic severe obesity // Nat. Genet. 2018. Vol. 50. № 2. P. 175–179. https://doi.org/10.1038/s41588-017-0023-6
  63. Tansey J., Sztalryd C., Hlavin E., Kimmel A., Londos C. The Central Role of Perilipin A in Lipid Metabolism and Adipocyte Lipolysis // IUBMB Life. 2004. Vol. 56. № 7. P. 379–385. https://doi.org/10.1080/15216540400009968
  64. Tong T., Shen Y., Lee H.-W., Yu R., Park T. Adenylyl cyclase 3 haploinsufficiency confers susceptibility to diet-induced obesity and insulin resistance in mice // Sci. Rep. 2016. Vol. 6. № 1. P. 34179. https://doi.org/10.1038/srep34179
  65. Tyurin-Kuzmin P.A. et al. Functional Heterogeneity of Protein Kinase A Activation in Multipotent Stromal Cells // IJMS. 2020. Vol. 21. № 12. P. 4442. https://doi.org/10.3390/ijms21124442
  66. Uemura T., Ohta Y., Nakao Y., Manaka T., Nakamura H., Takaoka K. Epinephrine accelerates osteoblastic differentiation by enhancing bone morphogenetic protein signaling through a cAMP/protein kinase A signaling pathway // Bone. 2010. Vol. 47. № 4. P. 756–765. https://doi.org/10.1016/j.bone.2010.07.008
  67. Vallin B. et al. Novel short isoforms of adenylyl cyclase as negative regulators of cAMP production // Biochimica et Biophysica Acta (BBA) – Molecular Cell Research. 2018. Vol. 1865. № 9. P. 1326–1340. https://doi.org/10.1016/j.bbamcr.2018.06.012
  68. Wang H. et al. Identification of an Adenylyl Cyclase Inhibitor for Treating Neuropathic and Inflammatory Pain // Sci. Transl. Med. 2011. Vol. 3. P. 65ra3. https://doi.org/10.1126/scitranslmed.3001269
  69. Wang L. et al. By inhibiting ADCY5, miR-18a-3p promotes osteoporosis and possibly contributes to spinal fracture // Biochemical and Biophysical Research Communications. 2021. Vol. 550. P. 49–55. https://doi.org/10.1016/j.bbrc.2021.02.118
  70. Wang Q. et al. Differential dependence of the D1 and D5Dopamine receptors on the G protein γ7 subunit for activation of Adenylylcyclase // Journal of Biological Chemistry. 2001. Vol. 276. № 42. P. 39386–39393. https://doi.org/10.1074/jbc.M104981200
  71. Wang Q. et al. Ribozyme-mediated Suppression of the G Protein γ7Subunit Suggests a Role in Hormone Regulation of Adenylylcyclase Activity // Journal of Biological Chemistry. 1997. Vol. 272. № 41. P. 26040–26048. https://doi.org/10.1074/jbc.272.41.26040
  72. Wei J. et al. Phosphorylation and Inhibition of Olfactory Adenylyl Cyclase by CaM Kinase II in Neurons: a Mechanism for Attenuation of Olfactory Signals // Neuron. 1998. Vol. 21. № 3. P. 495–504. https://doi.org/10.1016/s0896-6273(00)80561-9
  73. Wilson L.C., Trembath R.C. Albright's hereditary osteodystrophy // Journal of medical genetics. 1994. Vol. 31. № 10. P. 779–784. https://doi.org/10.1136/jmg.31.10.779
  74. Xiong Y. et al. Short-chain fatty acids stimulate leptin production in adipocytes through the G protein-coupled receptor GPR41 // Proc. Natl. Acad. Sci. U.S.A. 2004. Vol. 101. № 4. P. 1045–1050. https://doi.org/10.1073/pnas.2637002100
  75. Yang D.-C. et al. cAMP/PKA Regulates Osteogenesis, Adipogenesis and Ratio of RANKL/OPG mRNA Expression in Mesenchymal Stem Cells by Suppressing Leptin // PLoS ONE. 2008. Vol. 3. № 2. P. e1540. https://doi.org/10.1371/journal.pone.0001540
  76. Yoon Y., Oh C., Kang S., Chun J. Protein Kinase A Regulates Chondrogenesis of Mesenchymal Cells at the Post‐Precartilage Condensation Stage via Protein Kinase C‐α Signaling // J. of Bone & Mineral Res. 2000. Vol. 15. № 11. P. 2197–2205. https://doi.org/10.1359/jbmr.2000.15.11.2197
  77. Zaccolo M., Zerio A., Lobo M.J. Subcellular Organization of the cAMP Signaling Pathway // Pharmacol. Rev. 2021. Vol. 73. P. 278–309. https://doi.org/10.1124/pharmrev.120.000086
  78. Zhang H. et al. Activation of PKA/CREB Signaling is Involved in BMP9-Induced Osteogenic Differentiation of Mesenchymal Stem Cells // Cell Physiol. Biochem. 2015. Vol. 37. № 2. P. 548–562. https://doi.org/10.1159/000430376
  79. Zhang R. et al. Transcriptional Regulation of BMP2 Expression by the PTH-CREB Signaling Pathway in Osteoblasts // PLoS ONE. 2011. Vol. 6. № 6. P. e20780. https://doi.org/10.1371/journal.pone.0020780
  80. Zhang X. et al. Crif1 Promotes Adipogenic Differentiation of Bone Marrow Mesenchymal Stem Cells After Irradiation by Modulating the PKA/CREB Signaling Pathway // Stem Cells. 2015. Vol. 33. № 6. P. 1915–1926. https://doi.org/10.1002/stem.2019
  81. Zhao L., Li G., Zhou G. SOX9 Directly Binds CREB as a Novel Synergism With the PKA Pathway in BMP‐2–Induced Osteochondrogenic Differentiation // J. of Bone & Mineral Res. 2009. Vol. 24. № 5. P. 826–836. https://doi.org/10.1359/jbmr.081236
  82. Zuo X. et al. ADCY2, ADCY5, and GRIA1 are the key genes of cAMP signaling pathway to participate in osteoporotic peripheral and spinal fracture after the manipulation of Wnt signaling // Preprint. 2020. https://doi.org/10.21203/rs.3.rs-25264/v1

Дополнительные файлы

Доп. файлы
Действие
1. JATS XML

© Российская академия наук, 2025

Согласие на обработку персональных данных

 

Используя сайт https://journals.rcsi.science, я (далее – «Пользователь» или «Субъект персональных данных») даю согласие на обработку персональных данных на этом сайте (текст Согласия) и на обработку персональных данных с помощью сервиса «Яндекс.Метрика» (текст Согласия).