DECIPHERING CRUCIAL GENES IN PELVIC INFLAMMATORY DISEASE AND THEIR RELATIONSHIP WITH INFERTILITY THROUGH SYSTEMS BIOLOGY STUDIES



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Abstract

Abstract

Background: Pelvic inflammatory disease (PID) is an infection of the female reproductive system. PID is usually caused by infection with Chlamydia trachomatis (CT) and Neisseria gonorrhoeae (NG). Women with PID have an increased risk of becoming infertility. The aims of this study are to determine the molecular mechanisms that influence infertility and embryonic development in PID with CT and NG infections.

Methods: Microarray data were extracted from the Gene Expression Omnibus (GEO), and the protein-protein interaction network was constructed using Cytoscape software. Network analysis was performed to identify hub-bottlenecks and sub-networks. The functional mechanisms for critical genes were identified using the webgestalt server. Finally, new drug candidates were repurposed using the drug-gene interaction database.

Results: RPL13, EEF1G, JAK2, MYC, IL7R, CD74, IMPDH2, and NFAT5 were identified as crucial genes in protein-protein interactions and gene regulatory networks in CT and NG infections of PID. Ribosome, hematopoietic cell lineage, platelet activation, and Chagas disease, JAK-STAT pathway, eukaryotic translation elongation, Rap1 pathway, apoptosis, protein processing in the endoplasmic reticulum, progesterone-mediated oocyte maturation, and Epstein-Barr virus infection were identified as significant signaling pathways involving in CT and NG infections.

Conclusion: Our model suggests novel critical genes, and functional pathways involved in CT and NG infections, establishing a link between these infections and infertility. However, further studies in vitro and in vivo are needed.

About the authors

Fatemeh Saberi

Shahid Beheshti University of Medical Sciences, Tehran, Iran

Email: Fatemeh.saberi82@gmail.com

Student Research Committee, Department of Medical Biotechnology, School of Advanced Technologies in Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran;

Cellular and Molecular Biology Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran

Иран

Zeinab Dehghan

Shiraz University of Medical Sciences, Shiraz, Iran

Email: biomed1@sums.ac.ir

Department of Comparative Biomedical Sciences, School of Advanced Medical Sciences and Technologies, Shiraz University of Medical Sciences, Shiraz, Iran;

Иран

Tayyebeh Pilehchi

Shahid Beheshti University of Medical Sciences, Tehran, Iran

Email: t.pilechi@gmail.com

Student Research Committee, Department of Medical Biotechnology, School of Advanced Technologies in Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran;

Cellular and Molecular Biology Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran

Иран

Shayesteh Mehdinejadiani

Shiraz University of Medical Sciences, Shiraz, Iran

Email: mehdinejadiani@gmail.com

Department of Reproductive Biology, School of Advanced Medical Sciences and Technologies, Shiraz University of Medical Sciences, Shiraz, Iran

Иран

Zahra Taheri

Pavia University, Pavia, Italy

Email: z.biology87@gmail.com

Department of Biology and Biotechnology, Pavia University, Pavia, Italy

Италия

Hakimeh Zali

Shahid Beheshti University of Medical Sciences, Tehran, Iran

Author for correspondence.
Email: hakimehzali@gmail.com

Ph.D., Department of Tissue Engineering and Applied Cell Sciences, School of Advanced Technologies in Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran

Иран

References

  1. Ades A, Price MJ, Kounali D, Akande V, Wills GS, McClure MO, et al. Proportion of tubal factor infertility due to chlamydia: finite mixture modeling of serum antibody titers. Am J Epidemiol (2017)185(2):124-34.doi: 10.1093/aje/kww117
  2. Al Abdulmonem W, Rasheed Z, Al Ssadh H, Alkhamiss A, Aljohani AS, Fernández N. Bacterial lipopolysaccharide induces the intracellular expression of trophoblastic specific CD74 isoform in human first trimester trophoblast cells: correlation with unsuccessful early pregnancy. J Reprod Immunol (2020)141:103152.doi: 10.1016/j.jri.2020.103152
  3. Amin SM, Elkafrawy MA-S, El-Dawy DM, Abdelfttah AH. Relationship between Mean platelet volume and recurrent miscarriage. Al-Azhar Assiut Med j (2020)18(4):421-7.doi: 10.5114/aoms.2013.40095
  4. Brunham RC, Gottlieb SL, Paavonen J. Pelvic inflammatory disease. N Engl J Med (2015)372(21):2039-48.doi: 10.1056/NEJMra1411426
  5. Cai Y, Sukhova GK, Wong HK, Xu A, Tergaonkar V, Vanhoutte PM, et al. Rap1 induces cytokine production in pro-inflammatory macrophages through NFκB signaling and is highly expressed in human atherosclerotic lesions. Cell Cycle (2015)14(22):3580-92.doi: 10.1080/15384101.2015.1100771
  6. Ceppi M, Clavarino G, Gatti E, Schmidt EK, de Gassart A, Blankenship D, et al. Ribosomal protein mRNAs are translationally-regulated during human dendritic cells activation by LPS. Immunome Res (2009)5:1-12.doi: 10.1186/1745-7580-5-5
  7. Darville T. Pelvic inflammatory disease due to Neisseria gonorrhoeae and Chlamydia trachomatis: immune evasion mechanisms and pathogenic disease pathways. J Infect Dis (2021)224(Supplement_2):S39-S46.doi: 10.1093/infdis/jiab031
  8. Darville T. Pelvic inflammatory disease due to Neisseria gonorrhoeae and Chlamydia trachomatis: immune evasion mechanisms and pathogenic disease pathways. The Journal of infectious diseases (2021)224(Supplement_2):S39-S46
  9. Dehghanian M, Yarahmadi G, Sandoghsaz RS, Khodadadian A, Shamsi F, Mehrjardi MYV. Evaluation of Rap1GAP and EPAC1 gene expression in endometriosis disease. Adv Biomed Res (2023)12.doi: 10.4103/abr.abr_86_22
  10. Dix A, Vlaic S, Guthke R, Linde J. Use of systems biology to decipher host–pathogen interaction networks and predict biomarkers. CLIN MICROBIOL INFEC (2016)22(7):600-6.doi: 10.1016/j.cmi.2016.04.014
  11. Dzakah EE, Huang L, Xue Y, Wei S, Wang X, Chen H, et al. Host cell response and distinct gene expression profiles at different stages of Chlamydia trachomatis infection reveals stage-specific biomarkers of infection. BMC Microbiol (2021)21:1-13.doi: 10.1186/s12866-020-02061-6
  12. Fryer RH, Schwobe EP, Woods ML, Rodgers GM. Chlamydia species infect human vascular endothelial cells and induce procoagulant activity. J Investig Med (1997)45(4):168-74
  13. George Z, Omosun Y, Azenabor AA, Goldstein J, Partin J, Joseph K, et al. The molecular mechanism of induction of unfolded protein response by Chlamydia. Biochem Biophys Res Commun (2019)508(2):421-9.doi: 10.1016/j.bbrc.2018.11.034
  14. Ghoreschi K, Laurence A, O’Shea JJ. Janus kinases in immune cell signaling. Immunol Rev (2009)228(1):273-87.doi: 10.1111/j.1600-065X.2008.00754.x
  15. Gottlieb SL, Berman SM, Low N. Screening and treatment to prevent sequelae in women with Chlamydia trachomatis genital infection: how much do we know? J Infect Dis (2010)201(Supplement_2):S156-S67.doi: 10.1086/652396
  16. Guan J, Han S, Wu Je, Zhang Y, Bai M, Abdullah SW, et al. Ribosomal protein L13 participates in innate immune response induced by foot-and-mouth disease virus. Front immunol (2021)12:616402.doi: 10.3389/fimmu.2021.616402
  17. Guettler J, Forstner D, Gauster M. Maternal platelets at the first trimester maternal-placental interface–Small players with great impact on placenta development. Placenta (2022)125:61-7.doi: 10.1016/j.placenta.2021.12.009
  18. Gusse M, Ghysdael J, Evan G, Soussi T, Méchali M. Translocation of a store of maternal cytoplasmic c-myc protein into nuclei during early development. Mol Cell Biol (1989).doi: 10.1128/mcb.9.12.5395-5403.1989
  19. Hu Q, Bian Q, Rong D, Wang L, Song J, Huang H-S, et al. JAK/STAT pathway: Extracellular signals, diseases, immunity, and therapeutic regimens. Front Bioeng Biotechnol (2023)11:1110765.doi: 10.3389/fbioe.2023.1110765
  20. Hunt S, Vollenhoven B. Pelvic inflammatory disease and infertility. Aust J Gen Pract (2023)52(4):215-8.doi: 10.31128/AJGP-09-22-6576
  21. Ietta F, Ferro EAV, Bevilacqua E, Benincasa L, Maioli E, Paulesu L. Role of the macrophage migration inhibitory factor (MIF) in the survival of first trimester human placenta under induced stress conditions. Sci Rep (2018)8(1):12150.doi: 10.1038/s41598-018-29797-6
  22. Ito M, Nakasato M, Suzuki T, Sakai S, Nagata M, Aoki F. Localization of janus kinase 2 to the nuclei of mature oocytes and early cleavage stage mouse embryos. Biol Reprod (2004)71(1):89-96.doi: 10.1095/biolreprod.103.023226
  23. Iyyappan R, Aleshkina D, Ming H, Dvoran M, Kakavand K, Jansova D, et al. The translational oscillation in oocyte and early embryo development. Nucleic Acids Res (2023)51(22):12076-91.doi: 10.1093/nar/gkad996
  24. Knoke K, Rongisch RR, Grzes KM, Schwarz R, Lorenz B, Yogev N, et al. Tofacitinib suppresses IL-10/IL-10R signaling and modulates host defense responses in human macrophages. J Invest Dermatol (2022)142(3):559-70. e6.doi: 10.1016/j.jid.2021.07.180
  25. Köse C, Vatansever S, İnan S, Kırmaz C, Gürel Ç, Erışık D, et al. Evaluation of JAK/STAT Signaling Pathway-associated Protein Expression at Implantation Period: An Immunohistochemical Study in Rats. Anatol J Gen Med Res (2022)32(1).doi: 10.4274/terh.galenos.2021.22599
  26. Lad SP, Fukuda EY, Li J, de la Maza LM, Li E. Up-regulation of the JAK/STAT1 signal pathway during Chlamydia trachomatis infection. J Immun (2005)174(11):7186-93.doi: 10.4049/jimmunol.174.11.7186
  27. Lee N, Kim D, Kim W-U. Role of NFAT5 in the immune system and pathogenesis of autoimmune diseases. Front immunol (2019)10:270.doi: 10.3389/fimmu.2019.00270
  28. Lyons R, Saridogan E, Djahanbakhch O. The reproductive significance of human Fallopian tube cilia. Hum Reprod Update (2006)12(4):363-72.doi: 10.1093/humupd/dml012
  29. McGee ZA, Johnson AP, Taylor-Robinson D. Pathogenic mechanisms of Neisseria gonorrhoeae: observations on damage to human fallopian tubes in organ culture by gonococci of colony type 1 or type 4. J Infect Dis (1981)143(3):413-22.doi: 10.1093/infdis/143.3.413
  30. McGlade EA, Miyamoto A, Winuthayanon W. Progesterone and Inflammatory Response in the Oviduct during Physiological and Pathological Conditions. Cells (2022)11(7):1075.doi: 10.3390/cells11071075
  31. Mohr I, Sonenberg N. Host translation at the nexus of infection and immunity. Cell host & microbe (2012)12(4):470-83.doi: 10.1016/j.chom.2012.09.006
  32. Nasuhidehnavi A, McCall L-I. It takes two to tango: How immune responses and metabolic changes jointly shape cardiac Chagas disease. PLoS Pathog (2023)19(6):e1011399.doi: 10.1371/journal.ppat.1011399
  33. Negrutskii B, Shalak V, Novosylna O, Porubleva L, Lozhko D, El'skaya A. The eEF1 family of mammalian translation elongation factors. BBA advances (2023)3:100067.doi: 10.1016/j.bbadva.2022.100067
  34. Ni S, Zhang T, Zhou C, Long M, Hou X, You L, et al. Coordinated formation of IMPDH2 Cytoophidium in mouse oocytes and granulosa cells. Front cell dev biol (2021)9:690536.doi: 10.3389/fcell.2021.690536
  35. Peipert JF, Ness RB, Blume J, Soper DE, Holley R, Randall H, et al. Clinical predictors of endometritis in women with symptoms and signs of pelvic inflammatory disease. Am J Obstet Gynecol (2001)184(5):856-64.doi: 10.1067/mob.2001.113847
  36. Rödel J, Große C, Yu H, Wolf K, Otto GP, Liebler-Tenorio E, et al. Persistent Chlamydia trachomatis infection of HeLa cells mediates apoptosis resistance through a Chlamydia protease-like activity factor-independent mechanism and induces high mobility group box 1 release. Infect Immun (2012)80(1):195-205.doi: 10.1128/IAI.05619-11
  37. Rother M, Gonzalez E, da Costa ART, Wask L, Gravenstein I, Pardo M, et al. Combined human genome-wide RNAi and metabolite analyses identify IMPDH as a host-directed target against Chlamydia infection. Cell host & microbe (2018)23(5):661-71. e8.doi: 10.1016/j.chom.2018.04.002
  38. Sameni M, Mirmotalebisohi SA, Dehghan Z, Abooshahab R, Khazaei-Poul Y, Mozafar M, et al. Deciphering molecular mechanisms of SARS-CoV-2 pathogenesis and drug repurposing through GRN motifs: a comprehensive systems biology study. 3 Biotech (2023)13(4):117.doi: 10.1007/s13205-023-03518-x
  39. Scumpia PO, Kelly-Scumpia KM, Delano MJ, Weinstein JS, Cuenca AG, Al-Quran S, et al. Cutting edge: bacterial infection induces hematopoietic stem and progenitor cell expansion in the absence of TLR signaling. J Immun (2010)184(5):2247-51.doi: 10.4049/jimmunol.0903652
  40. Su H, Na N, Zhang X, Zhao Y. The biological function and significance of CD74 in immune diseases. Infect Immun (2017)66:209-16.doi: 10.1007/s00011-016-0995-1
  41. Tao H, Xiong Q, Ji Z, Zhang F, Liu Y, Chen M. NFAT5 is regulated by p53/miR-27a signal axis and promotes mouse ovarian granulosa cells proliferation. Int J Biol Sci (2019)15(2):287.doi: 10.7150/ijbs.29273
  42. Varol E. The relationship between mean platelet volume and pelvic inflammatory disease. Wien Klin Wochenschr (2014)126:659-60.doi: 10.1007/s00508-014-0587-4
  43. Virant-Klun I, Vogler A. In vitro maturation of oocytes from excised ovarian tissue in a patient with autoimmune ovarian insufficiency possibly associated with Epstein-Barr virus infection. Reprod biol endocrinol (2018)16(1):1-8.doi: 10.1186/s12958-018-0350-1
  44. Wang C, Kong L, Kim S, Lee S, Oh S, Jo S, et al. The role of IL-7 and IL-7R in cancer pathophysiology and immunotherapy. Int J Mol Sci (2022)23(18):10412.doi: 10.3390/ijms231810412
  45. Xin L, Xu B, Ma L, Hou Q, Ye M, Meng S, et al. Proteomics study reveals that the dysregulation of focal adhesion and ribosome contribute to early pregnancy loss. Proteom - Clin Appl (2016)10(5):554-63.doi: 10.1002/prca.201500136
  46. Xu H, Su X, Zhao Y, Tang L, Chen J, Zhong G. Innate lymphoid cells are required for endometrial resistance to Chlamydia trachomatis infection. Infect Immun (2020)88(7):10.1128/iai. 00152-20.doi: 10.1128/IAI.00152-20
  47. Yusuf H, Trent M. Management of pelvic inflammatory disease in clinical practice. Ther Clin Risk Manag (2023):183-92.doi: 10.2147/TCRM.S350750
  48. Zhang D, Zhu L, Wang F, Li P, Wang Y, Gao Y. Molecular mechanisms of eukaryotic translation fidelity and their associations with diseases. Int J Biol Macromol (2023):124680.doi: 10.1016/j.ijbiomac.2023.124680
  49. Zhang J, Chen Z, Fritz JH, Rochman Y, Leonard WJ, Gommerman JL, et al. Unusual timing of CD127 expression by mouse uterine natural killer cells. J Leukoc Biol (2012)91(3):417-26.doi: 10.1189/jlb.1011501
  50. Zhu H, Chen J, Liu K, Gao L, Wu H, Ma L, et al. Human PBMC scRNA-seq–based aging clocks reveal ribosome to inflammation balance as a single-cell aging hallmark and super longevity. Sci Adv (2023)9(26):eabq7599.doi: 10.1126/sciadv.abq7599
  52. Ades A, Price MJ, Kounali D, Akande V, Wills GS, McClure MO, et al. Proportion of tubal factor infertility due to chlamydia: finite mixture modeling of serum antibody titers. Am J Epidemiol
  53. Al Abdulmonem W, Rasheed Z, Al Ssadh H, Alkhamiss A, Aljohani AS, Fernández N. Bacterial lipopolysaccharide induces the intracellular expression of trophoblastic specific CD74 isoform in human first trimester trophoblast cells: correlation with unsuccessful early pregnancy. J Reprod Immunol
  54. Amin SM, Elkafrawy MA-S, El-Dawy DM, Abdelfttah AH. Relationship between Mean platelet volume and recurrent miscarriage. Al-Azhar Assiut Med j
  55. Brunham RC, Gottlieb SL, Paavonen J. Pelvic inflammatory disease. N Engl J Med
  56. Cai Y, Sukhova GK, Wong HK, Xu A, Tergaonkar V, Vanhoutte PM, et al. Rap1 induces cytokine production in pro-inflammatory macrophages through NFκB signaling and is highly expressed in human atherosclerotic lesions. Cell Cycle
  57. Ceppi M, Clavarino G, Gatti E, Schmidt EK, de Gassart A, Blankenship D, et al. Ribosomal protein mRNAs are translationally-regulated during human dendritic cells activation by LPS. Immunome Res
  58. Darville T. Pelvic inflammatory disease due to Neisseria gonorrhoeae and Chlamydia trachomatis: immune evasion mechanisms and pathogenic disease pathways. J Infect Dis
  59. Darville T. Pelvic inflammatory disease due to Neisseria gonorrhoeae and Chlamydia trachomatis: immune evasion mechanisms and pathogenic disease pathways. The Journal of infectious diseases
  60. Dehghanian M, Yarahmadi G, Sandoghsaz RS, Khodadadian A, Shamsi F, Mehrjardi MYV. Evaluation of Rap1GAP and EPAC1 gene expression in endometriosis disease. Adv Biomed Res
  61. Dix A, Vlaic S, Guthke R, Linde J. Use of systems biology to decipher host–pathogen interaction networks and predict biomarkers. CLIN MICROBIOL INFEC
  62. Dzakah EE, Huang L, Xue Y, Wei S, Wang X, Chen H, et al. Host cell response and distinct gene expression profiles at different stages of Chlamydia trachomatis infection reveals stage-specific biomarkers of infection. BMC Microbiol
  63. Fryer RH, Schwobe EP, Woods ML, Rodgers GM. Chlamydia species infect human vascular endothelial cells and induce procoagulant activity. J Investig Med
  64. George Z, Omosun Y, Azenabor AA, Goldstein J, Partin J, Joseph K, et al. The molecular mechanism of induction of unfolded protein response by Chlamydia. Biochem Biophys Res Commun
  65. Ghoreschi K, Laurence A, O’Shea JJ. Janus kinases in immune cell signaling. Immunol Rev
  66. Gottlieb SL, Berman SM, Low N. Screening and treatment to prevent sequelae in women with Chlamydia trachomatis genital infection: how much do we know? J Infect Dis
  67. Guan J, Han S, Wu Je, Zhang Y, Bai M, Abdullah SW, et al. Ribosomal protein L13 participates in innate immune response induced by foot-and-mouth disease virus. Front immunol
  68. Guettler J, Forstner D, Gauster M. Maternal platelets at the first trimester maternal-placental interface–Small players with great impact on placenta development. Placenta
  69. Gusse M, Ghysdael J, Evan G, Soussi T, Méchali M. Translocation of a store of maternal cytoplasmic c-myc protein into nuclei during early development. Mol Cell Biol
  70. Hu Q, Bian Q, Rong D, Wang L, Song J, Huang H-S, et al. JAK/STAT pathway: Extracellular signals, diseases, immunity, and therapeutic regimens. Front Bioeng Biotechnol
  71. Hunt S, Vollenhoven B. Pelvic inflammatory disease and infertility. Aust J Gen Pract
  72. Ietta F, Ferro EAV, Bevilacqua E, Benincasa L, Maioli E, Paulesu L. Role of the macrophage migration inhibitory factor (MIF) in the survival of first trimester human placenta under induced stress conditions. Sci Rep
  73. Ito M, Nakasato M, Suzuki T, Sakai S, Nagata M, Aoki F. Localization of janus kinase 2 to the nuclei of mature oocytes and early cleavage stage mouse embryos. Biol Reprod
  74. Iyyappan R, Aleshkina D, Ming H, Dvoran M, Kakavand K, Jansova D, et al. The translational oscillation in oocyte and early embryo development. Nucleic Acids Res
  75. Knoke K, Rongisch RR, Grzes KM, Schwarz R, Lorenz B, Yogev N, et al. Tofacitinib suppresses IL-10/IL-10R signaling and modulates host defense responses in human macrophages. J Invest Dermatol
  76. Köse C, Vatansever S, İnan S, Kırmaz C, Gürel Ç, Erışık D, et al. Evaluation of JAK/STAT Signaling Pathway-associated Protein Expression at Implantation Period: An Immunohistochemical Study in Rats. Anatol J Gen Med Res
  77. Lad SP, Fukuda EY, Li J, de la Maza LM, Li E. Up-regulation of the JAK/STAT1 signal pathway during Chlamydia trachomatis infection. J Immun
  78. Lee N, Kim D, Kim W-U. Role of NFAT5 in the immune system and pathogenesis of autoimmune diseases. Front immunol
  79. R, Saridogan E, Djahanbakhch O. The reproductive significance of human Fallopian tube cilia. Hum Reprod Update
  80. McGee ZA, Johnson AP, Taylor-Robinson D. Pathogenic mechanisms of Neisseria gonorrhoeae: observations on damage to human fallopian tubes in organ culture by gonococci of colony type 1 or type 4. J Infect Dis
  81. McGlade EA, Miyamoto A, Winuthayanon W. Progesterone and Inflammatory Response in the Oviduct during Physiological and Pathological Conditions. Cells
  82. Mohr I, Sonenberg N. Host translation at the nexus of infection and immunity. Cell host & microbe
  83. Nasuhidehnavi A, McCall L-I. It takes two to tango: How immune responses and metabolic changes jointly shape cardiac Chagas disease. PLoS Pathog
  84. Negrutskii B, Shalak V, Novosylna O, Porubleva L, Lozhko D, El'skaya A. The eEF1 family of mammalian translation elongation factors. BBA advances
  85. Ni S, Zhang T, Zhou C, Long M, Hou X, You L, et al. Coordinated formation of IMPDH2 Cytoophidium in mouse oocytes and granulosa cells. Front cell dev biol
  86. Peipert JF, Ness RB, Blume J, Soper DE, Holley R, Randall H, et al. Clinical predictors of endometritis in women with symptoms and signs of pelvic inflammatory disease. Am J Obstet Gynecol
  87. Rödel J, Große C, Yu H, Wolf K, Otto GP, Liebler-Tenorio E, et al. Persistent Chlamydia trachomatis infection of HeLa cells mediates apoptosis resistance through a Chlamydia protease-like activity factor-independent mechanism and induces high mobility group box 1 release. Infect Immun
  88. Rother M, Gonzalez E, da Costa ART, Wask L, Gravenstein I, Pardo M, et al. Combined human genome-wide RNAi and metabolite analyses identify IMPDH as a host-directed target against Chlamydia infection. Cell host & microbe
  89. Sameni M, Mirmotalebisohi SA, Dehghan Z, Abooshahab R, Khazaei-Poul Y, Mozafar M, et al. Deciphering molecular mechanisms of SARS-CoV-2 pathogenesis and drug repurposing through GRN motifs: a comprehensive systems biology study. 3 Biotech
  90. Scumpia PO, Kelly-Scumpia KM, Delano MJ, Weinstein JS, Cuenca AG, Al-Quran S, et al. Cutting edge: bacterial infection induces hematopoietic stem and progenitor cell expansion in the absence of TLR signaling. J Immun
  91. Su H, Na N, Zhang X, Zhao Y. The biological function and significance of CD74 in immune diseases. Infect Immun
  92. Tao H, Xiong Q, Ji Z, Zhang F, Liu Y, Chen M. NFAT5 is regulated by p53/miR-27a signal axis and promotes mouse ovarian granulosa cells proliferation. Int J Biol Sci
  93. Varol E. The relationship between mean platelet volume and pelvic inflammatory disease. Wien Klin Wochenschr
  94. Virant-Klun I, Vogler A. In vitro maturation of oocytes from excised ovarian tissue in a patient with autoimmune ovarian insufficiency possibly associated with Epstein-Barr virus infection. Reprod biol endocrinol
  95. Wang C, Kong L, Kim S, Lee S, Oh S, Jo S, et al. The role of IL-7 and IL-7R in cancer pathophysiology and immunotherapy. Int J Mol Sci
  96. Xin L, Xu B, Ma L, Hou Q, Ye M, Meng S, et al. Proteomics study reveals that the dysregulation of focal adhesion and ribosome contribute to early pregnancy loss. Proteom - Clin Appl
  97. Xu H, Su X, Zhao Y, Tang L, Chen J, Zhong G. Innate lymphoid cells are required for endometrial resistance to Chlamydia trachomatis infection. Infect Immun
  98. Yusuf H, Trent M. Management of pelvic inflammatory disease in clinical practice. Ther Clin Risk Manag
  99. Zhang D, Zhu L, Wang F, Li P, Wang Y, Gao Y. Molecular mechanisms of eukaryotic translation fidelity and their associations with diseases. Int J Biol Macromol
  100. Zhang J, Chen Z, Fritz JH, Rochman Y, Leonard WJ, Gommerman JL, et al. Unusual timing of CD127 expression by mouse uterine natural killer cells. J Leukoc Biol (2012)91(3):417-26.doi: 10.1189/jlb.1011501
  101. Zhu H, Chen J, Liu K, Gao L, Wu H, Ma L, et al. Human PBMC scRNA-seq–based aging clocks reveal ribosome to inflammation balance as a single-cell aging hallmark and super longevity. Sci Adv (2023)9(26):eabq7599.doi: 10.1126/sciadv.abq7599

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Copyright (c) Saberi F., Dehghan Z., Pilehchi T., Mehdinejadiani S., Taheri Z., Zali H.

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