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Combinatorial Chemistry & High Throughput Screening

Editor-in-Chief

ISSN (Print): 1386-2073
ISSN (Online): 1875-5402

Research Article

Pan-cancer Analysis Combined with Experiments Deciphers PHB Regulation for Breast Cancer Cell Survival and Predicts Biomarker Function

Author(s): Xiaoyan Zhou, Yue Li, Jiali Liu, Wei Lu, Sanyuan Liu, Jing Li and Qian He*

Volume 27, Issue 18, 2024

Published on: 07 November, 2023

Page: [2753 - 2763] Pages: 11

DOI: 10.2174/0113862073266248231024113533

Price: $65

Abstract

Background: Breast carcinoma has become the leading fatal disease among women. The location of prohibitin in the chromosome is close to the breast cancer susceptibility gene 1 (BRCA1). Accumulated research reported that prohibitin could interact with a variety of transcription factors and cell cycle-regulating proteins.

Objective: This present study aims to comprehensively explore and reveal the biological functions of prohibitin on breast cancer via The Cancer Genome Atlas (TCGA) and validation experiment in vitro.

Methods: Exploring the expression level of prohibitin across 27 tumors based on the TGGA database by bioinformatic methods and its relationship with tumor immune infiltration. Furthermore, we thus analyzed the biological roles of prohibitin on human breast cancer cell line MCF- 7 with pEGFP-prohibitin overexpression plasmid by western blotting and transwell-assay.

Results: Firstly, we found prohibitin is overexpressed in most tumors based on The Cancer Genome Atlas database, and the negative relationships between prohibitin and tumors infiltrating lymphocytes including B lymphocyte, CD4 T lymphocyte, CD8 T lymphocyte, Neutrophil, Macrophage and Dendritic, and its significant correlation with the prognosis of human cancer. In vitro, expression not only inhibited cell viability and invasive abilities but also increased the apoptosis percentage of cells with a decreased percentage of the S phase and an increased G2 phase. The reduction of Bcl-2 was observed when prohibitin was upregulated, although the expression of E2F-1 did not change.

Conclusion: Although prohibitin is over-expressed in various cancer types, it functions as an important tumor suppressor that may suppress breast cancer cell proliferation and the invasive ability of MCF-7 by influencing its DNA synthesis and promoting cell apoptosis. All these may be likely associated with P53, erbB-2, and Bcl-2.

[1]
Harbeck, N.; Gnant, M. Breast cancer. Lancet, 2017, 389(10074), 1134-1150.
[http://dx.doi.org/10.1016/S0140-6736(16)31891-8] [PMID: 27865536]
[2]
DeSantis, C.; Siegel, R.; Bandi, P.; Jemal, A. Breast cancer statistics, 2011. CA Cancer J. Clin., 2011, 61(6), 408-418.
[http://dx.doi.org/10.3322/caac.20134] [PMID: 21969133]
[3]
Fahad Ullah, M. Breast cancer: Current perspectives on the disease status. Adv. Exp. Med. Biol., 2019, 1152, 51-64.
[http://dx.doi.org/10.1007/978-3-030-20301-6_4] [PMID: 31456179]
[4]
Libson, S.; Lippman, M. A review of clinical aspects of breast cancer. Int. Rev. Psychiatry, 2014, 26(1), 4-15.
[http://dx.doi.org/10.3109/09540261.2013.852971] [PMID: 24716497]
[5]
Wang, W.; Xu, L.; Yang, Y.; Dong, L.; Zhao, B.; Lu, J.; Zhang, T.; Zhao, Y. A novel prognostic marker and immunogenic membrane antigen: prohibitin (PHB) in pancreatic cancer. Clin. Transl. Gastroenterol., 2018, 9(9), e178.
[http://dx.doi.org/10.1038/s41424-018-0044-1] [PMID: 30185797]
[6]
Wörmann, B. Breast cancer: Basics, screening, diagnostics and treatment. Med. Monatsschr. Pharm., 2017, 40(2), 55-64.
[PMID: 29952495]
[7]
Kawiak, A. Molecular research and treatment of breast cancer. Int. J. Mol. Sci., 2022, 23(17), 9617.
[http://dx.doi.org/10.3390/ijms23179617] [PMID: 36077013]
[8]
Barzaman, K.; Karami, J.; Zarei, Z.; Hosseinzadeh, A.; Kazemi, M.H.; Moradi-Kalbolandi, S.; Safari, E.; Farahmand, L. Breast cancer: Biology, biomarkers, and treatments. Int. Immunopharmacol., 2020, 84, 106535.
[http://dx.doi.org/10.1016/j.intimp.2020.106535] [PMID: 32361569]
[9]
Maughan, K.L.; Lutterbie, M.A.; Ham, P.S. Treatment of breast cancer. Am. Fam. Physician, 2010, 81(11), 1339-1346.
[PMID: 20521754]
[10]
Khokhar, A. Breast cancer in India: where do we stand and where do we go? Asian Pac. J. Cancer Prev., 2012, 13(10), 4861-4866.
[http://dx.doi.org/10.7314/APJCP.2012.13.10.4861] [PMID: 23244071]
[11]
Genetic tests to identify risk for breast cancer. In: Lynch, J.A.; Venne, V.; Berse, B., Eds.; Seminars in oncology nursing; Elsevier, 2015.
[12]
Francken, A.B.; Schouten, P.C.; Bleiker, E.M.A.; Linn, S.C.; Rutgers, E.J.T. Breast cancer in women at high risk: The role of rapid genetic testing for BRCA1 and -2 mutations and the consequences for treatment strategies. Breast, 2013, 22(5), 561-568.
[http://dx.doi.org/10.1016/j.breast.2013.07.045] [PMID: 23972475]
[13]
Merino Bonilla, J.A.; Torres Tabanera, M.; Ros Mendoza, L.H. Breast cancer in the 21st century: from early detection to new therapies. Radiologia (Madr.), 2017, 59(5), 368-379.
[http://dx.doi.org/10.1016/j.rx.2017.06.003] [PMID: 28712528]
[14]
Criscitiello, C.; Corti, C. Breast cancer genetics: Diagnostics and treatment. Genes (Basel), 2022, 13(9), 1593.
[http://dx.doi.org/10.3390/genes13091593] [PMID: 36140761]
[15]
Braden, A.; Stankowski, R.; Engel, J.; Onitilo, A. Breast cancer biomarkers: risk assessment, diagnosis, prognosis, prediction of treatment efficacy and toxicity, and recurrence. Curr. Pharm. Des., 2014, 20(30), 4879-4898.
[http://dx.doi.org/10.2174/1381612819666131125145517] [PMID: 24283956]
[16]
Majeed, W.; Aslam, B.; Javed, I.; Khaliq, T.; Muhammad, F.; Ali, A.; Raza, A. Breast cancer: Major risk factors and recent developments in treatment. Asian Pac. J. Cancer Prev., 2014, 15(8), 3353-3358.
[http://dx.doi.org/10.7314/APJCP.2014.15.8.3353] [PMID: 24870721]
[17]
Bécourt, S.; Espié, M. Hormonal treatment of breast cancer. In: Reference Module in Biomedical Sciences; , 2018.
[http://dx.doi.org/10.1016/B978-0-12-801238-3.64351-9]
[18]
Newman, L.A. Breast cancer in African-American women. Oncologist, 2005, 10(1), 1-14.
[http://dx.doi.org/10.1634/theoncologist.10-1-1] [PMID: 15632248]
[19]
Adrada, B.E.; Candelaria, R.; Rauch, G.M. MRI for the staging and evaluation of response to therapy in breast cancer. Top. Magn. Reson. Imaging, 2017, 26(5), 211-218.
[http://dx.doi.org/10.1097/RMR.0000000000000147] [PMID: 28961570]
[20]
Rooney, M.M.; Miller, K.N.; Plichta, J.K. Genetics of breast cancer. Surg. Clin. North Am., 2023, 103(1), 35-47.
[http://dx.doi.org/10.1016/j.suc.2022.08.016] [PMID: 36410352]
[21]
Noor, F.; Noor, A.; Ishaq, A.R.; Farzeen, I.; Saleem, M.H.; Ghaffar, K.; Aslam, M.F.; Aslam, S.; Chen, J.T. Recent Advances in diagnostic and therapeutic approaches for breast cancer: A comprehensive review. Curr. Pharm. Des., 2021, 27(20), 2344-2365.
[http://dx.doi.org/10.2174/18734286MTE06NzEAx] [PMID: 33655849]
[22]
Sachdev, J.C.; Sandoval, A.C.; Jahanzeb, M. Update on precision medicine in breast cancer. Cancer Treat. Res., 2019, 178, 45-80.
[http://dx.doi.org/10.1007/978-3-030-16391-4_2] [PMID: 31209841]
[23]
Rajalingam, K.; Wunder, C.; Brinkmann, V.; Churin, Y.; Hekman, M.; Sievers, C.; Rapp, U.R.; Rudel, T. Prohibitin is required for Ras-induced Raf–MEK–ERK activation and epithelial cell migration. Nat. Cell Biol., 2005, 7(8), 837-843.
[http://dx.doi.org/10.1038/ncb1283] [PMID: 16041367]
[24]
Fan, L.; Strasser-Weippl, K.; Li, J.J.; St Louis, J.; Finkelstein, D.M.; Yu, K.D.; Chen, W.Q.; Shao, Z.M.; Goss, P.E. Breast cancer in China. Lancet Oncol., 2014, 15(7), e279-e289.
[http://dx.doi.org/10.1016/S1470-2045(13)70567-9] [PMID: 24872111]
[25]
Ferzoco, R.M.; Ruddy, K.J. Unique aspects of caring for young breast cancer patients. Curr. Oncol. Rep., 2015, 17(2), 1.
[http://dx.doi.org/10.1007/s11912-014-0425-x] [PMID: 25645111]
[26]
Menen, R.S.; Hunt, K.K. Considerations for the treatment of young patients with breast cancer. Breast J., 2016, 22(6), 667-672.
[http://dx.doi.org/10.1111/tbj.12644] [PMID: 27542172]
[27]
Freedman, R.A.; Partridge, A.H. Management of breast cancer in very young women. Breast, 2013, 22(Suppl. 2), S176-S179.
[http://dx.doi.org/10.1016/j.breast.2013.07.034] [PMID: 24074783]
[28]
Anastasiadi, Z.; Lianos, G.D.; Ignatiadou, E.; Harissis, H.V.; Mitsis, M. Breast cancer in young women: An overview. Updates Surg., 2017, 69(3), 313-317.
[http://dx.doi.org/10.1007/s13304-017-0424-1] [PMID: 28260181]
[29]
Li, Y.; Dong, W.; Zhang, P.; Zhang, T.; Ma, L.; Qu, M.; Ma, X.; Zhou, X.; He, Q. Comprehensive analysis of regulatory factors and immune-associated patterns to decipher common and BRCA1/2 mutation-type-specific critical regulation in breast cancer. Front. Cell Dev. Biol., 2021, 9, 750897.
[http://dx.doi.org/10.3389/fcell.2021.750897] [PMID: 34733851]
[30]
Peng, Y.T.; Chen, P.; Ouyang, R.Y.; Song, L. Multifaceted role of prohibitin in cell survival and apoptosis. Apoptosis, 2015, 20(9), 1135-1149.
[http://dx.doi.org/10.1007/s10495-015-1143-z] [PMID: 26091791]
[31]
Artal-Sanz, M.; Tavernarakis, N. Prohibitin and mitochondrial biology. Trends Endocrinol. Metab., 2009, 20(8), 394-401.
[http://dx.doi.org/10.1016/j.tem.2009.04.004] [PMID: 19733482]
[32]
Merkwirth, C.; Dargazanli, S.; Tatsuta, T.; Geimer, S.; Löwer, B.; Wunderlich, F.T.; von Kleist-Retzow, J.C.; Waisman, A.; Westermann, B.; Langer, T. Prohibitins control cell proliferation and apoptosis by regulating OPA1-dependent cristae morphogenesis in mitochondria. Genes Dev., 2008, 22(4), 476-488.
[http://dx.doi.org/10.1101/gad.460708] [PMID: 18281461]
[33]
Sanz, M.A.; Tsang, W.Y.; Willems, E.M.; Grivell, L.A.; Lemire, B.D.; van der Spek, H.; Nijtmans, L.G.J. The mitochondrial prohibitin complex is essential for embryonic viability and germline function in Caenorhabditis elegans. J. Biol. Chem., 2003, 278(34), 32091-32099.
[http://dx.doi.org/10.1074/jbc.M304877200] [PMID: 12794069]
[34]
Webster, L.R.; Provan, P.J.; Graham, D.J.; Byth, K.; Walker, R.L.; Davis, S.; Salisbury, E.L.; Morey, A.L.; Ward, R.L.; Hawkins, N.J.; Clarke, C.L.; Meltzer, P.S.; Balleine, R.L. Prohibitin expression is associated with high grade breast cancer but is not a driver of amplification at 17q21.33. Pathology, 2013, 45(7), 629-636.
[http://dx.doi.org/10.1097/PAT.0000000000000004] [PMID: 24247619]
[35]
Fan, W.; Yang, H.; Liu, T.; Wang, J.; Li, T.W.H.; Mavila, N.; Tang, Y.; Yang, J.; Peng, H.; Tu, J.; Annamalai, A.; Noureddin, M.; Krishnan, A.; Gores, G.J.; Martínez-Chantar, M.L.; Mato, J.M.; Lu, S.C. Prohibitin 1 suppresses liver cancer tumorigenesis in mice and human hepatocellular and cholangiocarcinoma cells. Hepatology, 2017, 65(4), 1249-1266.
[http://dx.doi.org/10.1002/hep.28964] [PMID: 27981602]
[36]
Koushyar, S.; Jiang, W.G.; Dart, D.A. Unveiling the potential of prohibitin in cancer. Cancer Lett., 2015, 369(2), 316-322.
[http://dx.doi.org/10.1016/j.canlet.2015.09.012] [PMID: 26450374]
[37]
Fusaro, G.; Dasgupta, P.; Rastogi, S.; Joshi, B.; Chellappan, S. Prohibitin induces the transcriptional activity of p53 and is exported from the nucleus upon apoptotic signaling. J. Biol. Chem., 2003, 278(48), 47853-47861.
[http://dx.doi.org/10.1074/jbc.M305171200] [PMID: 14500729]
[38]
Rastogi, S.; Joshi, B.; Fusaro, G.; Chellappan, S. Camptothecin induces nuclear export of prohibitin preferentially in transformed cells through a CRM-1-dependent mechanism. J. Biol. Chem., 2006, 281(5), 2951-2959.
[http://dx.doi.org/10.1074/jbc.M508669200] [PMID: 16319068]
[39]
Zi Xu, Y.X.; Ande, S.R.; Mishra, S. Prohibitin: A new player in immunometabolism and in linking obesity and inflammation with cancer. Cancer Lett., 2018, 415, 208-216.
[http://dx.doi.org/10.1016/j.canlet.2017.12.001] [PMID: 29222040]
[40]
Yoshimaru, T.; Ono, M.; Bando, Y.; Chen, Y.A.; Mizuguchi, K.; Shima, H.; Komatsu, M.; Imoto, I.; Izumi, K.; Honda, J.; Miyoshi, Y.; Sasa, M.; Katagiri, T. A-kinase anchoring protein BIG3 coordinates oestrogen signalling in breast cancer cells. Nat. Commun., 2017, 8(1), 15427.
[http://dx.doi.org/10.1038/ncomms15427] [PMID: 28555617]
[41]
Sato, T.; Saito, H.; Swensen, J.; Olifant, A.; Wood, C.; Danner, D.; Sakamoto, T.; Takita, K.; Kasumi, F.; Miki, Y. The human prohibitin gene located on chromosome 17q21 is mutated in sporadic breast cancer. Cancer Res., 1992, 52(6), 1643-1646.
[PMID: 1540973]
[42]
Mishra, S.; Murphy, L.C.; Nyomba, B.L.G.; Murphy, L.J. Prohibitin: A potential target for new therapeutics. Trends Mol. Med., 2005, 11(4), 192-197.
[http://dx.doi.org/10.1016/j.molmed.2005.02.004] [PMID: 15823758]
[43]
Theiss, A.L.; Jenkins, A.K.; Okoro, N.I.; Klapproth, J.M.A.; Merlin, D.; Sitaraman, S.V. Prohibitin inhibits tumor necrosis factor alpha-induced nuclear factor-kappa B nuclear translocation via the novel mechanism of decreasing importin alpha3 expression. Mol. Biol. Cell, 2009, 20(20), 4412-4423.
[http://dx.doi.org/10.1091/mbc.e09-05-0361] [PMID: 19710421]
[44]
Yoshimaru, T.; Komatsu, M.; Miyoshi, Y.; Honda, J.; Sasa, M.; Katagiri, T. Therapeutic advances in BIG 3‐ PHB 2 inhibition targeting the crosstalk between estrogen and growth factors in breast cancer. Cancer Sci., 2015, 106(5), 550-558.
[http://dx.doi.org/10.1111/cas.12654] [PMID: 25736224]
[45]
Takagi, H.; Moyama, C.; Taniguchi, K.; Ando, K.; Matsuda, R.; Ando, S.; Ii, H.; Kageyama, S.; Kawauchi, A.; Chouha, N.; Désaubry, L.; Nakata, S. Fluorizoline blocks the interaction between prohibitin-2 and γ -glutamylcyclotransferase and induces p21 waf1/cip1 expression in MCF7 breast cancer cells. Mol. Pharmacol., 2022, 101(2), 78-86.
[http://dx.doi.org/10.1124/molpharm.121.000334] [PMID: 34862308]
[46]
He, Q.; Zhang, S.Q.; Chu, Y.L.; Jia, X.L.; Zhao, L.H.; Wang, X.L. Separation and identification of differentially expressed nuclear matrix proteins in breast carcinoma forming. Acta Oncol., 2010, 49(1), 76-84.
[http://dx.doi.org/10.3109/02841860903287213] [PMID: 19878069]
[47]
Kim, N.H.; Yoshimaru, T.; Chen, Y.A.; Matsuo, T.; Komatsu, M.; Miyoshi, Y.; Tanaka, E.; Sasa, M.; Mizuguchi, K.; Katagiri, T. BIG3 inhibits the estrogen-dependent nuclear translocation of PHB2 via multiple karyopherin-alpha proteins in breast cancer cells. PLoS One, 2015, 10(6), e0127707.
[http://dx.doi.org/10.1371/journal.pone.0127707] [PMID: 26052702]
[48]
Hwang, K.T. Clinical databases for breast cancer research. Adv. Exp. Med. Biol., 2021, 1187, 493-509.
[http://dx.doi.org/10.1007/978-981-32-9620-6_26] [PMID: 33983596]
[49]
Roulot, A.; Héquet, D.; Guinebretière, J.M.; Vincent-Salomon, A.; Lerebours, F.; Dubot, C.; Rouzier, R. Tumoral heterogeneity of breast cancer. Ann. Biol. Clin. (Paris), 2016, 74(6), 653-660.
[PMID: 27848916]
[50]
Printz, C. Breast cancer screening for women in their 40s reduces mortality. Cancer, 2021, 127(4), 497.
[http://dx.doi.org/10.1002/cncr.33439] [PMID: 33512720]
[51]
Kolak, A.; Kamińska, M.; Sygit, K.; Budny, A.; Surdyka, D.; Kukiełka-Budny, B.; Burdan, F. Primary and secondary prevention of breast cancer. Ann. Agric. Environ. Med., 2017, 24(4), 549-553.
[http://dx.doi.org/10.26444/aaem/75943] [PMID: 29284222]
[52]
Li, Z.; Wei, H.; Li, S.; Wu, P.; Mao, X. The role of progesterone receptors in breast cancer. Drug Des. Devel. Ther., 2022, 16, 305-314.
[http://dx.doi.org/10.2147/DDDT.S336643] [PMID: 35115765]
[53]
Liu, P.; Xu, Y.; Zhang, W.; Li, Y.; Tang, L.; Chen, W.; Xu, J.; Sun, Q.; Guan, X. Prohibitin promotes androgen receptor activation in ER-positive breast cancer. Cell Cycle, 2017, 16(8), 776-784.
[http://dx.doi.org/10.1080/15384101.2017.1295193] [PMID: 28272969]
[54]
Chigira, T.; Nagatoishi, S.; Tsumoto, K. Differential binding of prohibitin-2 to estrogen receptor α and to drug-resistant ERα mutants. Biochem. Biophys. Res. Commun., 2015, 463(4), 726-731.
[http://dx.doi.org/10.1016/j.bbrc.2015.06.002] [PMID: 26049107]
[55]
Kahlert, S.; Nuedling, S.; van Eickels, M.; Vetter, H.; Meyer, R.; Grohé, C. Estrogen receptor alpha rapidly activates the IGF-1 receptor pathway. J. Biol. Chem., 2000, 275(24), 18447-18453.
[http://dx.doi.org/10.1074/jbc.M910345199] [PMID: 10749889]
[56]
Rios, A.C.; van Rheenen, J.; Scheele, C.L.G.J. Multidimensional imaging of breast cancer. Cold Spring Harb. Perspect. Med., 2023, 13(5), a041330.
[http://dx.doi.org/10.1101/cshperspect.a041330] [PMID: 36167726]
[57]
Zhang, X. Molecular classification of breast cancer: Relevance and challenges. Arch. Pathol. Lab. Med., 2023, 147(1), 46-51.
[http://dx.doi.org/10.5858/arpa.2022-0070-RA] [PMID: 36136295]
[58]
Nuell, M.J.; Stewart, D.A.; Walker, L.; Friedman, V.; Wood, C.M.; Owens, G.A.; Smith, J.R.; Schneider, E.L.; Dell’ Orco, R.; Lumpkin, C.K. Prohibitin, an evolutionarily conserved intracellular protein that blocks DNA synthesis in normal fibroblasts and HeLa cells. Mol. Cell. Biol., 1991, 11(3), 1372-1381.
[PMID: 1996099]
[59]
Too, I.H.K.; Bonne, I.; Tan, E.L.; Chu, J.J.H.; Alonso, S. Prohibitin plays a critical role in Enterovirus 71 neuropathogenesis. PLoS Pathog., 2018, 14(1), e1006778.
[http://dx.doi.org/10.1371/journal.ppat.1006778] [PMID: 29324904]
[60]
Tortelli Junior, T.C.; de Godoy, L.M.F.; de Souza, G.A.; Bonatto, D.; Otake, A.H.; de Freitas Saito, R.; Rosa, J.C.; Greene, L.J.; Chammas, R. Accumulation of prohibitin is a common cellular response to different stressing stimuli and protects melanoma cells from ER stress and chemotherapy-induced cell death. Oncotarget, 2017, 8(26), 43114-43129.
[http://dx.doi.org/10.18632/oncotarget.17810] [PMID: 28562344]
[61]
Kahl, A.; Anderson, C.J.; Qian, L.; Voss, H.; Manfredi, G.; Iadecola, C.; Zhou, P. Neuronal expression of the mitochondrial protein prohibitin confers profound neuroprotection in a mouse model of focal cerebral ischemia. J. Cereb. Blood Flow Metab., 2018, 38(6), 1010-1020.
[http://dx.doi.org/10.1177/0271678X17720371] [PMID: 28714328]
[62]
Woodlock, T.J.; Bethlendy, G.; Segel, G.B. Prohibitin expression is increased in phorbol ester-treated chronic leukemic B-lymphocytes. Blood Cells Mol. Dis., 2001, 27(1), 27-34.
[http://dx.doi.org/10.1006/bcmd.2000.0348] [PMID: 11162143]
[63]
Raut, G.K.; Chakrabarti, M.; Pamarthy, D.; Bhadra, M.P. Glucose starvation-induced oxidative stress causes mitochondrial dysfunction and apoptosis via Prohibitin 1 upregulation in human breast cancer cells. Free Radic. Biol. Med., 2019, 145, 428-441.
[http://dx.doi.org/10.1016/j.freeradbiomed.2019.09.020] [PMID: 31614178]
[64]
Wang, S.; Fusaro, G.; Padmanabhan, J.; Chellappan, S.P. Prohibitin co-localizes with Rb in the nucleus and recruits N-CoR and HDAC1 for transcriptional repression. Oncogene, 2002, 21(55), 8388-8396.
[http://dx.doi.org/10.1038/sj.onc.1205944] [PMID: 12466959]
[65]
Fu, P.; Yang, Z.; Bach, L.A. Prohibitin-2 binding modulates insulin-like growth factor-binding protein-6 (IGFBP-6)-induced rhabdomyosarcoma cell migration. J. Biol. Chem., 2013, 288(41), 29890-29900.
[http://dx.doi.org/10.1074/jbc.M113.510826] [PMID: 24003225]
[66]
Bai, Y.; Ludescher, M.; Poschmann, G.; Stühler, K.; Wyrich, M.; Oles, J.; Franken, A.; Rivandi, M.; Abramova, A.; Reinhardt, F.; Ruckhäberle, E.; Niederacher, D.; Fehm, T.; Cahill, M.A.; Stamm, N.; Neubauer, H. PGRMC1 promotes progestin-dependent proliferation of breast cancer cells by binding prohibitins resulting in activation of ERα signaling. Cancers (Basel), 2021, 13(22), 5635.
[http://dx.doi.org/10.3390/cancers13225635] [PMID: 34830790]
[67]
Wang, K.; Long, B.; Zhou, L.Y.; Liu, F.; Zhou, Q.Y.; Liu, C.Y.; Fan, Y.Y.; Li, P.F. CARL lncRNA inhibits anoxia-induced mitochondrial fission and apoptosis in cardiomyocytes by impairing miR-539-dependent PHB2 downregulation. Nat. Commun., 2014, 5(1), 3596.
[http://dx.doi.org/10.1038/ncomms4596] [PMID: 24710105]
[68]
Huang, X.; Liu, J.; Ma, Q. Prohibitin participates in the HIRA complex to promote cell metastasis in breast cancer cell lines. FEBS Open Bio, 2020, 10(10), 2182-2190.
[http://dx.doi.org/10.1002/2211-5463.12966] [PMID: 32865342]
[69]
Zhong, N.; Cui, Y.; Zhou, X.; Li, T.; Han, J. Identification of prohibitin 1 as a potential prognostic biomarker in human pancreatic carcinoma using modified aqueous two-phase partition system combined with 2D-MALDI-TOF-TOF-MS/MS. Tumour Biol., 2015, 36(2), 1221-1231.
[http://dx.doi.org/10.1007/s13277-014-2742-y] [PMID: 25344214]
[70]
Satheesh Kumar, M.K.; Nair, S.; Mony, U.; Kalingavarman, S.; Venkat, R.; Sivanarayanan, T.B.; Unni, A.K.K.; Rajeshkannan, R.; Anandakuttan, A.; Radhakrishnan, S.; Menon, K.N. Significance of elevated Prohibitin 1 levels in Multiple Sclerosis patients lymphocytes towards the assessment of subclinical disease activity and its role in the central nervous system pathology of disease. Int. J. Biol. Macromol., 2018, 110, 573-581.
[http://dx.doi.org/10.1016/j.ijbiomac.2017.12.061] [PMID: 29242126]

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