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


Cite item

Full Text

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.

About the authors

Xiaoyan Zhou

Department of Clinical Laboratories, Second Affiliated Hospital of Xi’an Jiaotong University, Xi’an Jiaotong University

Email: info@benthamscience.net

Yue Li

Department of Clinical Laboratories, Second Affiliated Hospital of Xi’an Jiaotong University, Xi’an Jiaotong University

Email: info@benthamscience.net

Jiali Liu

Department of Clinical Laboratories, Second Affiliated Hospital of Xi’an Jiaotong University, Xi’an Jiaotong University

Email: info@benthamscience.net

Wei Lu

Department of Clinical Laboratories, Second Affiliated Hospital of Xi’an Jiaotong University, Xi’an Jiaotong University

Email: info@benthamscience.net

Sanyuan Liu

Department of Clinical Laboratories, Second Affiliated Hospital of Xi’an Jiaotong University, Xi’an Jiaotong University

Email: info@benthamscience.net

Jing Li

Department of Clinical Laboratories, Second Affiliated Hospital of Xi’an Jiaotong University, Xi’an Jiaotong University

Email: info@benthamscience.net

Qian He

Department of Clinical Laboratories, Second Affiliated Hospital of Xi’an Jiaotong University, Xi’an Jiaotong University

Author for correspondence.
Email: info@benthamscience.net

References

  1. Harbeck, N.; Gnant, M. Breast cancer. Lancet, 2017, 389(10074), 1134-1150. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.1016/j.ijbiomac.2017.12.061 PMID: 29242126

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2024 Bentham Science Publishers