Rab Proteins: Insights into Intracellular Trafficking in Endometrium.
Animals
Endometrium
/ metabolism
Estradiol
/ metabolism
Female
Host-Pathogen Interactions
Humans
Menstrual Cycle
/ metabolism
Progesterone
/ metabolism
Protein Transport
Sexually Transmitted Diseases, Bacterial
/ metabolism
Sexually Transmitted Diseases, Viral
/ metabolism
rab GTP-Binding Proteins
/ metabolism
Endometrial changes
Endometrial receptivity
Endometrial secretion
Hormonal regulation
Implantation
Intracellular transport
Rab proteins
Secretory processes
Small GTPases
Vesicular transport
Journal
Reproductive sciences (Thousand Oaks, Calif.)
ISSN: 1933-7205
Titre abrégé: Reprod Sci
Pays: United States
ID NLM: 101291249
Informations de publication
Date de publication:
01 2021
01 2021
Historique:
received:
06
01
2020
accepted:
30
06
2020
revised:
28
05
2020
pubmed:
9
7
2020
medline:
24
11
2021
entrez:
9
7
2020
Statut:
ppublish
Résumé
Rab proteins belong to the Ras superfamily of small monomeric GTPases. These G proteins are the main controllers of vesicular transport in every tissue, among them, the endometrium. They are in charge of to the functional subcellular compartmentalization and cargo transport between organelles and the plasma membrane. In turn, intracellular trafficking contributes to endometrial changes during the menstrual cycle, secretion to the uterine fluid, and trophoblast implantation; however, few reports analyze the role of Rab proteins in the uterus. In general, Rab proteins control the release of cytokines, growth factors, enzymes, hormones, cell adhesion molecules, and mucus. Further, the secretion of multiple compounds into the uterine cavity is required for successful implantation. Therefore, alterations in Rab-controlled intracellular transport likely impair secretory processes to the uterine fluid that may correlate with abnormal endometrial development and failed reproductive outcomes. Overall, they could explain recurrent miscarriages, female infertility, and/or assisted reproductive failure. Interestingly, estrogen (E2) and progesterone (P) regulate gene expression of Rab proteins involved in secretory pathways. This review aims to gather information regarding the role of Rab proteins and intracellular trafficking in the endometrium during the different menstrual phases, and in the generation of a receptive stage for embryo implantation, modulated by E2 and P. This knowledge might be useful for the development of novel reproductive therapies that overcome low implantation rates of assisted reproductive procedures.
Identifiants
pubmed: 32638281
doi: 10.1007/s43032-020-00256-w
pii: 10.1007/s43032-020-00256-w
doi:
Substances chimiques
Progesterone
4G7DS2Q64Y
Estradiol
4TI98Z838E
rab GTP-Binding Proteins
EC 3.6.5.2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
12-22Références
Evans J, Salamonsen LA, Winship A, Menkhorst E, Nie G, Gargett CE, et al. Fertile ground: human endometrial programming and lessons in health and disease. Nat Rev Endocrinol. 2016;12:654–67.
pubmed: 27448058
Pfeffer SR. Rab GTPases: master regulators that establish the secretory and endocytic pathways. Mol Biol Cell. 2017;28:712–5.
pubmed: 28292916
pmcid: 5349778
Blanc L, Vidal M. New insights into the function of Rab GTPases in the context of exosomal secretion. Small GTPases. 2018;9:95–106.
pubmed: 28135905
Greening DW, Nguyen HPT, Elgass K, Simpson RJ, Salamonsen LA. Human endometrial exosomes contain hormone-specific cargo modulating trophoblast adhesive capacity: insights into endometrial-embryo Interactions1. Biol Reprod. 2016;94:38.
pubmed: 26764347
Nguyen HPT, Simpson RJ, Salamonsen LA, Greening DW. Extracellular vesicles in the intrauterine environment: challenges and potential functions. Biol Reprod. 2016;95:109.
pubmed: 27655784
pmcid: 5333933
Salamonsen LA, Edgell T, Rombauts LJF, Stephens AN, Robertson DM, Rainczuk A, et al. Proteomics of the human endometrium and uterine fluid: a pathway to biomarker discovery. Fertil Steril. 2013;99:1086–92.
pubmed: 23043689
Ng YH, Rome S, Jalabert A, Forterre A, Singh H, Hincks CL, et al. Endometrial exosomes/microvesicles in the uterine microenvironment: a new paradigm for embryo-endometrial cross talk at implantation. Ward WS, editor. PLoS One. 2013;8:e58502.
pubmed: 23516492
pmcid: 3596344
Zaborowski MP, Balaj L, Breakefield XO, Lai CP. Extracellular vesicles: composition, biological relevance, and methods of study. Bioscience. 2015;65:783–97.
pubmed: 26955082
pmcid: 4776721
Kurian NK, Modi D (2018) Extracellular vesicle mediated embryo-endometrial cross talk during implantation and in pregnancy. J Assist Reprod Genet
Ye T-M, Pang RTK, Leung CON, Chiu J-F, Yeung WSB. Two-dimensional liquid chromatography with tandem mass spectrometry–based proteomic characterization of endometrial luminal epithelial surface proteins responsible for embryo implantation. Fertil Steril. 2015;103:853–861.e3.
pubmed: 25624195
Hood BL, Liu B, Alkhas A, Shoji Y, Challa R, Wang G, et al. Proteomics of the human endometrial glandular epithelium and Stroma from the proliferative and secretory phases of the menstrual cycle1. Biol Reprod. 2015;92:106.
pubmed: 25695723
Salamonsen LA, Evans J, Nguyen HPT, Edgell TA. The microenvironment of human implantation: determinant of reproductive success. Am J Reprod Immunol. 2016;75:218–25.
pubmed: 26661899
Gray CA, Burghardt RC, Johnson GA, Bazer FW, Spencer TE. Evidence that absence of endometrial gland secretions in uterine gland knockout ewes compromises conceptus survival and elongation. Reproduction. 2002;124:289–300.
pubmed: 12141942
Bhusane K, Bhutada S, Chaudhari U, Savardekar L, Katkam R, Sachdeva G. Secrets of endometrial receptivity: some are hidden in uterine Secretome. Am J Reprod Immunol. 2016;75:226–36.
pubmed: 26865379
Hutagalung AH, Novick PJ. Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev United States. 2011;91:119–49.
pubmed: 21248164
pmcid: 3710122
Blumer J, Rey J, Dehmelt L, Mazel T, Wu Y-W, Bastiaens P, et al. RabGEFs are a major determinant for specific Rab membrane targeting. J Cell Biol United States. 2013;200:287–300.
pubmed: 23382462
pmcid: 3563681
Müller MP, Goody RS (2018) Molecular control of Rab activity by GEFs, GAPs and GDI. Small GTPases. Taylor and Francis Inc. p. 5–21
Novick P, Medkova M, Dong G, Hutagalung A, Reinisch K, Grosshans B. Interactions between Rabs, tethers, SNAREs and their regulators in exocytosis. Biochem Soc Trans England. 2006;34:683–6.
pubmed: 17052174
Seabra MC, Coudrier E. Rab GTPases and myosin motors in organelle motility. Traffic England. 2004;5:393–9.
pubmed: 15117313
Wandinger-Ness A, Zerial M. Rab proteins and the compartmentalization of the endosomal system. Cold Spring Harb Perspect Biol. 2014;6:a022616.
pubmed: 25341920
pmcid: 4413231
Kelly EE, Horgan CP, Goud B, McCaffrey MW. The Rab family of proteins: 25 years on. Biochem Soc Trans. 2012;40:1337–47.
pubmed: 23176478
Ali BR, Wasmeier C, Lamoreux L, Strom M, Seabra MC. Multiple regions contribute to membrane targeting of Rab GTPases. J Cell Sci. 2004;117:6401–12.
pubmed: 15561774
Kofler N, Corti F, Rivera-Molina F, Deng Y, Toomre D, Simons M. The Rab-effector protein RABEP2 regulates endosomal trafficking to mediate vascular endothelial growth factor receptor-2 (VEGFR2)-dependent signaling. J Biol Chem. 2018;293:4805–17.
pubmed: 29425100
pmcid: 5880142
Shibata S, Teshima Y, Niimi K, Inagaki S. Involvement of ARHGEF10, GEF for RhoA, in Rab6/Rab8-mediating membrane traffic. Small GTPases. 2019;10:169–77.
pubmed: 28448737
Horgan CP, Hanscom SR, Jolly RS, Futter CE, McCaffrey MW. Rab11-FIP3 links the Rab11 GTPase and cytoplasmic dynein to mediate transport to the endosomal-recycling compartment. J Cell Sci. 2010;123:181–91.
pubmed: 20026645
Butterworth MB, Edinger RS, Silvis MR, Gallo LI, Liang X, Apodaca G, et al. Rab11b regulates the trafficking and recycling of the epithelial sodium channel (ENaC). Am J Physiol Ren Physiol. 2012;302:F581–90.
Casanova JE, Wang X, Kumar R, Bhartur SG, Navarre J, Woodrum JE, et al. Association of Rab25 and Rab11a with the apical recycling system of polarized Madin-Darby canine kidney cells. Mol Biol Cell. 1999;10:47–61.
pubmed: 9880326
pmcid: 25153
Capmany A, Damiani MT. Chlamydia trachomatis intercepts Golgi-derived sphingolipids through a Rab14-mediated transport required for bacterial development and replication. Valdivia RH, editor. PLoS One. 2010;5:e14084.
pubmed: 21124879
pmcid: 2989924
Tolmachova T, Anders R, Stinchcombe J, Bossi G, Griffiths GM, Huxley C, et al. A general role for Rab27a in secretory cells. Mol Biol Cell. 2004;15:332–44.
pubmed: 14617806
pmcid: 307551
Davila J, Laws MJ, Kannan A, Li Q, Taylor RN, Bagchi MK, et al. (2015) Rac1 regulates endometrial secretory function to control placental development. PLoS Genet Public Library of Science, 11
Lima PDA, Croy BA, Degaki KY, Tayade C, Yamada AT. Heterogeneity in composition of mouse uterine natural killer cell granules. J Leukoc Biol. 2012;92:195–204.
pubmed: 22566570
Gambarte Tudela J, Capmany A, Romao M, Quintero C, Miserey-Lenkei S, Raposo G, et al. The late endocytic Rab39a GTPase regulates the interaction between multivesicular bodies and chlamydial inclusions. J Cell Sci. 2015;128:3068–81.
pubmed: 26163492
Sun Y, Chiu TT, Foley KP, Bilan PJ, Klip A. Myosin Va mediates Rab8A-regulated GLUT4 vesicle exocytosis in insulin-stimulated muscle cells. Linstedt A, editor. Mol Biol Cell. 2014;25:1159–70.
pubmed: 24478457
pmcid: 3967978
Rosas C, Gabler F, Vantman D, Romero C, Vega M. Levels of Rabs and WAVE family proteins associated with translocation of GLUT4 to the cell surface in endometria from hyperinsulinemic PCOS women. Hum Reprod. 2010;25:2870–7.
pubmed: 20843777
Cheng KW, Lahad JP, Kuo W-L, Lapuk A, Yamada K, Auersperg N, et al. The RAB25 small GTPase determines aggressiveness of ovarian and breast cancers. Nat Med. 2004;10:1251–6.
pubmed: 15502842
Bie Y, Zhang Z. RAB8A a new biomarker for endometrial cancer? World J Surg Oncol. 2014;12:371.
pubmed: 25477298
pmcid: 4289371
Kelly EE, Horgan CP, McCaffrey MW. Rab11 proteins in health and disease. Biochem Soc Trans. 2012;40:1360–7.
pubmed: 23176481
Welz T, Wellbourne-Wood J, Kerkhoff E. Orchestration of cell surface proteins by Rab11. Trends Cell Biol. 2014;24:407–15.
pubmed: 24675420
Baetz NW, Goldenring JR. Rab11-family interacting proteins define spatially and temporally distinct regions within the dynamic Rab11a-dependent recycling system. Mol Biol Cell. 2013;24:643–58.
pubmed: 23283983
pmcid: 3583667
Leiva N, Capmany A, Damiani MT. Rab11-family of interacting protein 2 associates with chlamydial inclusions through its Rab-binding domain and promotes bacterial multiplication. Cell Microbiol. 2013;15:114–29.
pubmed: 23006599
Peden AA, Schonteich E, Chun J, Junutula JR, Scheller RH, Prekeris R. The RCP-Rab11 complex regulates endocytic protein sorting. Mol Biol Cell. 2004;15:3530–41.
pubmed: 15181150
pmcid: 491816
Junutula JR, De Maziére AM, Peden AA, Ervin KE, Advani RJ, van Dijk SM, et al. Rab14 is involved in membrane trafficking between the Golgi complex and endosomes. Mol Biol Cell. 2004;15:2218–29.
pubmed: 15004230
pmcid: 404017
Heaton SJ, Eady JJ, Parker ML, Gotts KL, Dainty JR, Fairweather-Tait SJ, et al. The use of BeWo cells as an in vitro model for placental iron transport. Am J Physiol Cell Physiol. 2008;295:C1445–53.
pubmed: 18815225
pmcid: 2584991
Gonzalez IM, Ackerman WE, Vandre DD, Robinson JM. Exocyst complex protein expression in the human placenta. Placenta WB Saunders Ltd. 2014;35:442–9.
pubmed: 24856041
pmcid: 4096856
Taglauer ES, Artemiuk PA, Hanscom SR, Lindsay AJ, Wuebbolt D, Breathnach FM, et al. (2017) Rab11 family expression in the human placenta: localization at the maternal-fetal interface. PLoS One Public Library of Science, 12
Yin YX, Shen F, Pei H, Ding Y, Zhao H, Zhao M, et al. Increased expression of Rab25 in breast cancer correlates with lymphatic metastasis. Tumor Biol. 2012;33:1581–7.
Chua CEL, Tang BL. The role of the small GTPase Rab31 in cancer. J Cell Mol Med. 2015;19:1–10.
pubmed: 25472813
Tudela JG, Buonfigli J, Luján A, Bivou MA, Cebrián I, Capmany A, et al. (2019) Rab39a and Rab39b display different intracellular distribution and function in sphingolipids and phospholipids transport. Int J Mol Sci MDPI AG, 20
Chen T, Han Y, Yang M, Zhang W, Li N, Wan T, et al. Rab39, a novel Golgi-associated Rab GTPase from human dendritic cells involved in cellular endocytosis. Biochem Biophys Res Commun. 2003;303:1114–20.
pubmed: 12684051
Becker CE, Creagh EM, O’Neill LAJ. RAB39a binds caspase-1 and is required for caspase-1-dependent interleukin-1β secretion. J Biol Chem. 2016;291:24800.
pubmed: 27864526
pmcid: 5114427
Seto S, Tsujimura K, Koide Y. Rab GTPases regulating Phagosome maturation are differentially recruited to mycobacterial Phagosomes. Traffic. 2011;12:407–20.
pubmed: 21255211
Seto S, Sugaya K, Tsujimura K, Nagata T, Horii T, Koide Y. Rab39a interacts with phosphatidylinositol 3-kinase and negatively regulates autophagy induced by lipopolysaccharide stimulation in macrophages. Chaves-Olarte E, editor. PLoS One. 2013;8:e83324.
pubmed: 24349490
pmcid: 3862771
Chen D, Ganapathy P, Zhu LJ, Xu X, Li Q, Bagchi IC, et al. Potential regulation of membrane trafficking by estrogen receptor alpha via induction of rab11 in uterine glands during implantation. Mol Endocrinol. 1999;13:993–1004.
pubmed: 10379897
Kakar-Bhanot R, Brahmbhatt K, Chauhan B, Katkam RR, Bashir T, Gawde H, et al. (2018) Rab11a drives adhesion molecules to the surface of endometrial epithelial cells. Hum Reprod
Patil VS, Sachdeva G, Modi DN, Katkam RR, Manjramkar DD, Hinduja I, et al. Rab coupling protein (RCP): a novel target of progesterone action in primate endometrium. J Mol Endocrinol. 2005;35:357–72.
pubmed: 16216915
Kao LC, Tulac S, Lobo S, Imani B, Yang JP, Germeyer A, et al. Global gene profiling in human endometrium during the window of implantation. Endocrinology Endocrine Society. 2002;143:2119–38.
pubmed: 12021176
Kurakado S, Kurogane R, Sugita T. 17β-estradiol inhibits estrogen binding protein-mediated hypha formation in Candida albicans. Microb Pathog. 2017;109:151–5.
pubmed: 28552809
Okai B, Lyall N, Gow NAR, Bain JM, Erwig L-P. Rab14 regulates maturation of macrophage phagosomes containing the fungal pathogen Candida albicans and outcome of the host-pathogen interaction. Deepe GS, editor. Infect Immun. 2015;83:1523–35.
pubmed: 25644001
pmcid: 4363425
Song W, Condron S, Mocca BT, Veit SJ, Hill D, Abbas A, et al. Local and humoral immune responses against primary and repeat Neisseria gonorrhoeae genital tract infections of 17β-estradiol-treated mice. Vaccine. 2008;26:5741–51.
pubmed: 18762223
pmcid: 2855896
Edwards JL. Neisseria gonorrhoeae survival during primary human cervical epithelial cell infection requires nitric oxide and is augmented by progesterone. Infect Immun. 2010;78:1202–13.
pubmed: 20048043
pmcid: 2825954
Shew ML, McGlennen R, Zaidi N, Westerheim M, Ireland M, Anderson S. Oestrogen receptor transcripts associated with cervical human papillomavirus infection. Sex Transm Infect England. 2002;78:210–4.
pubmed: 12238657
pmcid: 1744465
Lee Y, Dizzell S, Leung V, Nazli A, Zahoor M, Fichorova R, et al. Effects of female sex hormones on susceptibility to HSV-2 in vaginal cells grown in air-liquid Interface. Viruses. 2016;8:241.
pmcid: 5035955
Vicetti Miguel RD, Sheridan BS, Harvey SAK, Schreiner RS, Hendricks RL, Cherpes TL. 17-beta estradiol promotion of herpes simplex virus type 1 reactivation is estrogen receptor dependent. J Virol. 2010;84:565–72.
pubmed: 19846508
Rückert C, Stuepp C d S, Gottardi B, Rosa J, Cisilotto J, Borges FP, et al. Steroid hormones alter AMP hydrolysis in intact trophozoites of Trichomonas vaginalis. Parasitol Res. 2009;105:1701–6.
pubmed: 19756747
Damiani MT, Gambarte Tudela J, Capmany A. Targeting eukaryotic Rab proteins: a smart strategy for chlamydial survival and replication. Cell Microbiol. 2014;16:1329–38.
pubmed: 24948448
Amirshahi A, Wan C, Beagley K, Latter J, Symonds I, Timms P. Modulation of the Chlamydia trachomatis in vitro transcriptome response by the sex hormones estradiol and progesterone. BMC Microbiol. 2011;11:150.
pubmed: 21702997
pmcid: 3224131
Davis CH, Raulston JE, Wyrick PB. Protein disulfide isomerase, a component of the estrogen receptor complex, is associated with Chlamydia trachomatis serovar E attached to human endometrial epithelial cells. Infect Immun. 2002;70:3413–8.
pubmed: 12065480
pmcid: 128041
Borth N, Massier J, Franke C, Sachse K, Saluz H-P, Hänel F. Chlamydial protease CT441 interacts with SRAP1 co-activator of estrogen receptor alpha and partially alleviates its co-activation activity. J Steroid Biochem Mol Biol. 2010;119:89–95.
pubmed: 20079837