Relationships of Prodiginins Mechanisms and Molecular Structures to their Antiproliferative Effects


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Abstract

:The Prodiginins (PGs) natural pigments are secondary metabolites produced by a broad spectrum of gram-negative and gram-positive bacteria, notably by species within the Serratia and Streptomyces genera. These compounds exhibit diverse and potent biological activities, including anticancer, immunosuppressive, antimicrobial, antimalarial, and antiviral effects. Structurally, PGs share a common tripyrrolic core but possess variable side chains and undergo cyclization, resulting in structural diversity. Studies have investigated their antiproliferative effects on various cancer cell lines, with some PGs advancing to clinical trials for cancer treatment. This review aims to illuminate the molecular mechanisms underlying PG-induced apoptosis in cancer cells and explore the structure-activity relationships pertinent to their anticancer properties. Such insights may serve as a foundation for further research in anticancer drug development, potentially leading to the creation of novel, targeted therapies based on PGs or their derivatives.

About the authors

El Abbassi Ayoub

Laboratory of Physiopathology and Molecular Genetics, Department of Biology, Faculty of Sciences Ben M’Sik, Hassan II University

Author for correspondence.
Email: info@benthamscience.net

Zineb Azoubi

Laboratory of Physiopathology and Molecular Genetics, Department of Biology, Faculty of Sciences Ben M’Sik, Hassan II University

Email: info@benthamscience.net

Zougagh Nadia

Laboratory of Physiopathology and Molecular Genetics, Department of Biology, Faculty of Sciences Ben M’Sik,, Hassan II University

Email: info@benthamscience.net

Mouslim Assia

Laboratory of Physiopathology and Molecular Genetics, Department of Biology, Faculty of Sciences Ben M’Sik, University of Hassan II Casablanca

Email: info@benthamscience.net

Menggad Mohammed

Laboratory of Physiopathology and Molecular Genetics, Department of Biology, Faculty of Sciences Ben M’Sik,, Hassan II University

Email: info@benthamscience.net

References

  1. Williamson, N.R.; Fineran, P.C.; Leeper, F.J.; Salmond, G.P.C. The biosynthesis and regulation of bacterial prodiginines. Nat. Rev. Microbiol., 2006, 4(12), 887-899. doi: 10.1038/nrmicro1531 PMID: 17109029
  2. Ullah, A.; Aziz, T.; Ullah, N.; Nawaz, T. Molecular mechanisms of sanguinarine in cancer prevention and treatment. Anticancer. Agents Med. Chem., 2023, 23(7), 765-778. doi: 10.2174/1871520622666220831124321 PMID: 36045531
  3. Ullah, A.; Razzaq, A.; Alfaifi, M.Y.; Elbehairi, S.E.I.; Menaa, F.; Ullah, N.; Shehzadi, S.; Nawaz, T.; Iqbal, H. Sanguinarine attenuates lung cancer progression via oxidative stress-induced cell apoptosis. Curr. Mol. Pharmacol., 2024, 17, e18761429269383. doi: 10.2174/0118761429269383231119062233 PMID: 38389415
  4. Wang, Z.; Li, B.; Zhou, L.; Yu, S.; Su, Z.; Song, J.; Sun, Q.; Sha, O.; Wang, X.; Jiang, W.; Willert, K.; Wei, L.; Carson, D.A.; Lu, D. Prodigiosin inhibits Wnt/β-catenin signaling and exerts anticancer activity in breast cancer cells. Proc. Natl. Acad. Sci. , 2016, 113(46), 13150-13155. doi: 10.1073/pnas.1616336113 PMID: 27799526
  5. Kapoor, R.; Saini, A.; Sharma, D. Indispensable role of microbes in anticancer drugs and discovery trends. Appl. Microbiol. Biotechnol., 2022, 106(13-16), 4885-4906. doi: 10.1007/s00253-022-12046-2 PMID: 35819512
  6. Law, J.W.F.; Law, L.N.S.; Letchumanan, V.; Tan, L.T.H.; Wong, S.H.; Chan, K.G.; Ab Mutalib, N.S.; Lee, L.H. Anticancer drug discovery from microbial sources: the unique mangrove streptomycetes. Molecules, 2020, 25(22), 5365. doi: 10.3390/molecules25225365 PMID: 33212836
  7. Baindara, P.; Mandal, S.M. Bacteria and bacterial anticancer agents as a promising alternative for cancer therapeutics. Biochimie, 2020, 177, 164-189. doi: 10.1016/j.biochi.2020.07.020 PMID: 32827604
  8. Rivankar, S. An overview of doxorubicin formulations in cancer therapy. J. Cancer Res. Ther., 2014, 10(4), 853-858. doi: 10.4103/0973-1482.139267 PMID: 25579518
  9. Takeuchi, T. Antitumor antibiotics discovered and studied at the Institute of Microbial Chemistry. J. Cancer Res. Clin. Oncol., 1995, 121(9-10), 505-510. doi: 10.1007/BF01197761 PMID: 7559728
  10. Hollstein, U. Actinomycin. Chemistry and mechanism of action. Chem. Rev., 1974, 74(6), 625-652. doi: 10.1021/cr60292a002
  11. Ramos, A.; Sadeghi, S.; Tabatabaeian, H. Battling chemoresistance in cancer: root causes and strategies to uproot them. Int. J. Mol. Sci., 2021, 22(17), 9451. doi: 10.3390/ijms22179451 PMID: 34502361
  12. Lazaro, J.E.H.; Nitcheu, J.; Predicala, R.Z.; Mangalindan, G.C.; Nesslany, F.; Marzin, D.; Concepcion, G.P.; Diquet, B. Heptyl prodigiosin, a bacterial metabolite, is antimalarial in vivo and non-mutagenic in vitro. J. Nat. Toxins, 2002, 11(4), 367-377. PMID: 12503881
  13. Yip, C.H.; Mahalingam, S.; Wan, K.L.; Nathan, S. Prodigiosin inhibits bacterial growth and virulence factors as a potential physiological response to interspecies competition. PLoS One, 2021, 16(6), e0253445. doi: 10.1371/journal.pone.0253445 PMID: 34161391
  14. Han, S.B.; Kim, H.M.; Kim, Y.H.; Lee, C.W.; Jang, E.S.; Son, K.H.; Kim, S.U.; Kim, Y.K. T-cell specific immunosuppression by prodigiosin isolated from Serratia marcescens. Int. J. Immunopharmacol., 1998, 20(1-3), 1-13. doi: 10.1016/S0192-0561(97)00062-3 PMID: 9717078
  15. Darshan, N.; Manonmani, H.K. Prodigiosin and its potential applications. J. Food Sci. Technol., 2015, 52(9), 5393-5407. doi: 10.1007/s13197-015-1740-4 PMID: 26344956
  16. Hu, D.X.; Withall, D.M.; Challis, G.L.; Thomson, R.J. Structure, chemical synthesis, and biosynthesis of prodiginine natural products. Chem. Rev., 2016, 116(14), 7818-7853. doi: 10.1021/acs.chemrev.6b00024 PMID: 27314508
  17. Mouslim, A.; Menggad, S.; Habti, N.; Affar, E.B.; Menggad, M. Antiproliferative effect on cancer cells of novel pink red-like pigments and derivatives produced by Streptomyces coelicoflavus strains. J. Cancer Res., 2019, 7(1), 27-33.
  18. Kim, D.; Lee, J.S.; Park, Y.K.; Kim, J.F.; Jeong, H.; Oh, T.K.; Kim, B.S.; Lee, C.H. Biosynthesis of antibiotic prodiginines in the marine bacterium Hahella chejuensis KCTC 2396. J. Appl. Microbiol., 2007, 102(4), 937-944. PMID: 17381736
  19. Lee, J.S.; Kim, Y.S.; Park, S.; Kim, J.; Kang, S.J.; Lee, M.H.; Ryu, S.; Choi, J.M.; Oh, T.K.; Yoon, J.H. Exceptional production of both prodigiosin and cycloprodigiosin as major metabolic constituents by a novel marine bacterium, Zooshikella rubidus S1-1. Appl. Environ. Microbiol., 2011, 77(14), 4967-4973. doi: 10.1128/AEM.01986-10 PMID: 21642414
  20. Cerdeño, A.M.; Bibb, M.J.; Challis, G.L. Analysis of the prodiginine biosynthesis gene cluster of Streptomyces coelicolor A3(2): new mechanisms for chain initiation and termination in modular multienzymes. Chem. Biol., 2001, 8(8), 817-829. doi: 10.1016/S1074-5521(01)00054-0 PMID: 11514230
  21. Jia, X. Identification of essential genes associated with prodigiosin production in serratia marcescens FZSF02. Front. Microbiol., 2021, 12, 705853. doi: 10.3389/fmicb.2021.705853
  22. Lu, Y.; Liu, D.; Jiang, R.; Li, Z.; Gao, X. Prodigiosin: unveiling the crimson wonder – a comprehensive journey from diverse bioactivity to synthesis and yield enhancement. Front. Microbiol., 2024, 15, 1412776. doi: 10.3389/fmicb.2024.1412776 PMID: 38903802
  23. Williamson, N.R.; Simonsen, H.T.; Ahmed, R.A.A.; Goldet, G.; Slater, H.; Woodley, L.; Leeper, F.J.; Salmond, G.P.C. Biosynthesis of the red antibiotic, prodigiosin, in Serratia: identification of a novel 2‐methyl‐3‐n‐amyl‐pyrrole (MAP) assembly pathway, definition of the terminal condensing enzyme, and implications for undecylprodigiosin biosynthesis in Streptomyces. Mol. Microbiol., 2005, 56(4), 971-989. doi: 10.1111/j.1365-2958.2005.04602.x PMID: 15853884
  24. Li, P.; He, S.; Zhang, X.; Gao, Q.; Liu, Y.; Liu, L. Structures, biosynthesis, and bioactivities of prodiginine natural products. Appl. Microbiol. Biotechnol., 2022, 106(23), 7721-7735. doi: 10.1007/s00253-022-12245-x PMID: 36319792
  25. Feitelson, J.S.; Malpartida, F.; Hopwood, D.A. Genetic and biochemical characterization of the red gene cluster of Streptomyces coelicolor A3(2). Microbiology, 1985, 131(9), 2431-2441. doi: 10.1099/00221287-131-9-2431 PMID: 2999302
  26. Gristwood, T.; McNeil, M.B.; Clulow, J.S.; Salmond, G.P.C.; Fineran, P.C. PigS and PigP regulate prodigiosin biosynthesis in Serratia via differential control of divergent operons, which include predicted transporters of sulfur-containing molecules. J. Bacteriol., 2011, 193(5), 1076-1085. doi: 10.1128/JB.00352-10 PMID: 21183667
  27. Kim, D. Analysis of a prodigiosin biosynthetic gene cluster from the marine bacterium Hahella chejuensis KCTC 2396. J. Microbiol. Biotechnol., 2006, 16(12), 1912.
  28. Kwon, S.K.; Park, Y.K.; Kim, J.F. Genome-wide screening and identification of factors affecting the biosynthesis of prodigiosin by Hahella chejuensis, using Escherichia coli as a surrogate host. Appl. Environ. Microbiol., 2010, 76(5), 1661-1668. doi: 10.1128/AEM.01468-09 PMID: 20038694
  29. Harris, A.K.P.; Williamson, N.R.; Slater, H.; Cox, A.; Abbasi, S.; Foulds, I.; Simonsen, H.T.; Leeper, F.J.; Salmond, G.P.C. The Serratia gene cluster encoding biosynthesis of the red antibiotic, prodigiosin, shows species- and strain-dependent genome context variation. Microbiology, 2004, 150(11), 3547-3560. doi: 10.1099/mic.0.27222-0 PMID: 15528645
  30. Borah, S.; Melvin, M.S.; Lindquist, N.; Manderville, R.A. Copper-mediated nuclease activity of a tambjamine alkaloid. J. Am. Chem. Soc., 1998, 120(19), 4557-4562. doi: 10.1021/ja9729746
  31. Zhao, W.; Gao, D.; Ning, L.; Jiang, Y.; Li, Z.; Huang, B.; Chen, A.; Wang, C.; Liu, Y. Prodigiosin inhibits the proliferation of glioblastoma by regulating the KIAA1524/PP2A signaling pathway. Sci. Rep., 2022, 12(1), 18527. doi: 10.1038/s41598-022-23186-w PMID: 36323805
  32. Anwar, M.M.; Shalaby, M.; Embaby, A.M.; Saeed, H.; Agwa, M.M.; Hussein, A. Prodigiosin/PU-H71 as a novel potential combined therapy for triple negative breast cancer (TNBC): preclinical insights. Sci. Rep., 2020, 10(1), 14706. doi: 10.1038/s41598-020-71157-w PMID: 32895397
  33. Melvin, M.S.; Ferguson, D.C.; Lindquist, N.; Manderville, R.A. DNA binding by 4-methoxypyrrolic natural products. Preference for intercalation at AT sites by tambjamine E and prodigiosin. J. Org. Chem., 1999, 64(18), 6861-6869. doi: 10.1021/jo990944a PMID: 11674696
  34. Melvin, M.S.; Tomlinson, J.T.; Saluta, G.R.; Kucera, G.L.; Lindquist, N.; Manderville, R.A. Double-strand DNA cleavage by copper⊙ prodigiosin. J. Am. Chem. Soc., 2000, 122(26), 6333-6334. doi: 10.1021/ja0000798
  35. Melvin, M.S.; Wooton, K.E.; Rich, C.C.; Saluta, G.R.; Kucera, G.L.; Lindquist, N.; Manderville, R.A. Copper-nuclease efficiency correlates with cytotoxicity for the 4-methoxypyrrolic natural products. J. Inorg. Biochem., 2001, 87(3), 129-135. doi: 10.1016/S0162-0134(01)00338-5 PMID: 11730894
  36. Montaner, B.; Castillo-Ávila, W.; Martinell, M.; Öllinger, R.; Aymami, J.; Giralt, E.; Pérez-Tomás, R. DNA interaction and dual topoisomerase I and II inhibition properties of the anti-tumor drug prodigiosin. Toxicol. Sci., 2005, 85(2), 870-879. doi: 10.1093/toxsci/kfi149 PMID: 15788728
  37. Nguyen, M.; Marcellus, R.C.; Roulston, A.; Watson, M.; Serfass, L.; Murthy Madiraju, S.R.; Goulet, D.; Viallet, J.; Bélec, L.; Billot, X.; Acoca, S.; Purisima, E.; Wiegmans, A.; Cluse, L.; Johnstone, R.W.; Beauparlant, P.; Shore, G.C. Small molecule obatoclax (GX15-070) antagonizes MCL-1 and overcomes MCL-1-mediated resistance to apoptosis. Proc. Natl. Acad. Sci., 2007, 104(49), 19512-19517. doi: 10.1073/pnas.0709443104 PMID: 18040043
  38. Hassankhani, R.; Sam, M.R.; Esmaeilou, M.; Ahangar, P. Prodigiosin isolated from cell wall of Serratia marcescens alters expression of apoptosis-related genes and increases apoptosis in colorectal cancer cells. Med. Oncol., 2015, 32(1), 366. doi: 10.1007/s12032-014-0366-0 PMID: 25429836
  39. Li, D.; Liu, J.; Wang, X.; Kong, D.; Du, W.; Li, H.; Hse, C.Y.; Shupe, T.; Zhou, D.; Zhao, K. Biological potential and mechanism of prodigiosin from Serratia marcescens subsp. lawsoniana in human choriocarcinoma and prostate cancer cell lines. Int. J. Mol. Sci., 2018, 19(11), 3465. doi: 10.3390/ijms19113465 PMID: 30400387
  40. Chonghaile, T.N.; Letai, A. Mimicking the BH3 domain to kill cancer cells. Oncogene, 2008, 27(1), S149. doi: 10.1038/onc.2009.52
  41. Boger, D.L.; Patel, M. Total synthesis of prodigiosin, prodigiosene, and desmethoxyprodigiosin: Diels-Alder reactions of heterocyclic azadienes and development of an effective palladium(II)-promoted 2,2′-bipyrrole coupling procedure. J. Org. Chem., 1988, 53(7), 1405-1415. doi: 10.1021/jo00242a013
  42. Montaner, B.; Pérez-Tomás, R. The cytotoxic prodigiosin induces phosphorylation of p38-MAPK but not of SAPK/JNK. Toxicol. Lett., 2002, 129(1-2), 93-98. doi: 10.1016/S0378-4274(01)00477-5 PMID: 11879978
  43. Lu, C.H.; Lin, S.C.; Yang, S.Y.; Pan, M.Y.; Lin, Y.W.; Hsu, C.Y.; Wei, Y.H.; Chang, J.S.; Chang, C.C. Prodigiosin-induced cytotoxicity involves RAD51 down-regulation through the JNK and p38 MAPK pathways in human breast carcinoma cell lines. Toxicol. Lett., 2012, 212(1), 83-89. doi: 10.1016/j.toxlet.2012.05.002 PMID: 22579953
  44. Forgac, M. Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat. Rev. Mol. Cell Biol., 2007, 8(11), 917-929. doi: 10.1038/nrm2272 PMID: 17912264
  45. Nilsson, C.; Johansson, U.; Johansson, A.C.; Kågedal, K.; Öllinger, K. Cytosolic acidification and lysosomal alkalinization during TNF-α induced apoptosis in U937 cells. Apoptosis, 2006, 11(7), 1149-1159. doi: 10.1007/s10495-006-7108-5 PMID: 16699952
  46. Lagadic-Gossmann, D.; Huc, L.; Lecureur, V. Alterations of intracellular pH homeostasis in apoptosis: origins and roles. Cell Death Differ., 2004, 11(9), 953-961. doi: 10.1038/sj.cdd.4401466 PMID: 15195071
  47. Gottlieb, R.A. Cell acidification in apoptosis. Apoptosis, 1996, 1(1), 40-48. doi: 10.1007/BF00142077
  48. Stransky, L.; Cotter, K.; Forgac, M. The function of V-ATPases in cancer. Physiol. Rev., 2016, 96(3), 1071-1091. doi: 10.1152/physrev.00035.2015 PMID: 27335445
  49. Sato, T.; Konno, H.; Tanaka, Y.; Kataoka, T.; Nagai, K.; Wasserman, H.H.; Ohkuma, S. Prodigiosins as a new group of H+/Cl- symporters that uncouple proton translocators. J. Biol. Chem., 1998, 273(34), 21455-21462. doi: 10.1074/jbc.273.34.21455 PMID: 9705273
  50. Francisco, R.; Pérez-Tomás, R.; Gimènez-Bonafé, P.; Soto-Cerrato, V.; Giménez-Xavier, P.; Ambrosio, S. Mechanisms of prodigiosin cytotoxicity in human neuroblastoma cell lines. Eur. J. Pharmacol., 2007, 572(2-3), 111-119. doi: 10.1016/j.ejphar.2007.06.054 PMID: 17678643
  51. Sessler, J.L.; Eller, L.R.; Cho, W.S.; Nicolaou, S.; Aguilar, A.; Lee, J.T.; Lynch, V.M.; Magda, D.J. Synthesis, anion-binding properties, and in vitro anticancer activity of prodigiosin analogues. Angew. Chem. Int. Ed., 2005, 44(37), 5989-5992. doi: 10.1002/anie.200501740 PMID: 16114075
  52. Seganish, J.L.; Davis, J.T. Prodigiosin is a chloride carrier that can function as an anion exchanger. Chem. Commun. , 2005, (46), 5781-5783. doi: 10.1039/b511847f PMID: 16307144
  53. Liu, P.; Wang, Y.; Qi, X.; Gu, Q.; Geng, M.; Li, J. Undecylprodigiosin induced apoptosis in P388 cancer cells is associated with its binding to ribosome. PLoS One, 2013, 8(6), e65381. doi: 10.1371/journal.pone.0065381 PMID: 23799011
  54. Melvin, M.S.; Calcutt, M.W.; Noftle, R.E.; Manderville, R.A. Influence of the a-ring on the redox and nuclease properties of the prodigiosins: importance of the bipyrrole moiety in oxidative DNA cleavage. Chem. Res. Toxicol., 2002, 15(5), 742-748. doi: 10.1021/tx025508p PMID: 12018997
  55. Povirk, L.F.; Hogan, M.; Dattagupta, N. Binding of bleomycin to DNA: intercalation of the bithiazole rings. Biochemistry, 1979, 18(1), 96-101. doi: 10.1021/bi00568a015 PMID: 84680
  56. Paul, V.J.; Lindquist, N.; Fenical, W. Chemical defenses of the tropical ascidian Atapozoa sp. and its nudibranch predators Nembrotha spp. Mar. Ecol. Prog. Ser., 1990, 59(1/2), 109-118. doi: 10.3354/meps059109
  57. Wasserman, H.H.; Friedland, D.J.; Morrison, D.A. A novel dipyrrolyldipyrromethene prodigiosin analog from. Tetrahedron Lett., 1968, 9(6), 641-644. doi: 10.1016/S0040-4039(00)75602-4 PMID: 4867609
  58. De Rosa, M.; Johnson, S.A.; Opresko, P.L. Roles for the 8-oxoguanine dna repair system in protecting telomeres from oxidative stress. Front. Cell Dev. Biol., 2021, 9, 758402. doi: 10.3389/fcell.2021.758402
  59. Ma, A.; Dai, X. The relationship between DNA single-stranded damage response and double-stranded damage response. Cell Cycle, 2018, 17(1), 73-79. doi: 10.1080/15384101.2017.1403681 PMID: 29157089
  60. Melvin, M.S.; Tomlinson, J.T.; Park, G.; Day, C.S.; Saluta, G.R.; Kucera, G.L.; Manderville, R.A. Influence of the a-ring on the proton affinity and anticancer properties of the prodigiosins. Chem. Res. Toxicol., 2002, 15(5), 734-741. doi: 10.1021/tx025507x PMID: 12018996
  61. D’Alessio, R.; Rossi, A. Short synthesis of undecylprodigiosine. A new route to 2,2′-bipyrrolyl-pyrromethene systems. Synlett, 1996, 1996(6), 513-514. doi: 10.1055/s-1996-5485
  62. D’Alessio, R.; Bargiotti, A.; Carlini, O.; Colotta, F.; Ferrari, M.; Gnocchi, P.; Isetta, A.; Mongelli, N.; Motta, P.; Rossi, A.; Rossi, M.; Tibolla, M.; Vanotti, E. Synthesis and immunosuppressive activity of novel prodigiosin derivatives. J. Med. Chem., 2000, 43(13), 2557-2565. doi: 10.1021/jm001003p PMID: 10891115
  63. Hayakawa, Y.; Kawakami, K.; Seto, H.; Furihata, K. Structure of a new antibiotic, roseophilin. Tetrahedron Lett., 1992, 33(19), 2701-2704. doi: 10.1016/S0040-4039(00)79061-7
  64. Park, G.; Tomlinson, J.T.; Melvin, M.S.; Wright, M.W.; Day, C.S.; Manderville, R.A. Zinc and copper complexes of prodigiosin: implications for copper-mediated double-strand DNA cleavage. Org. Lett., 2003, 5(2), 113-116. doi: 10.1021/ol027165s PMID: 12529118
  65. Park, G-S.; Tomlinson, J.T.; Misenheimer, J.A.; Kucera, G.L.; Manderville, R.A. Photo-induced cytotoxicity of prodigiosin analogues. Bull. Korean Chem. Soc., 2007, 28(1), 49-52. doi: 10.5012/bkcs.2007.28.1.049
  66. Meshnick, S.R. Chloroquine as intercalator: a hypothesis revived. Parasitol. Today, 1990, 6(3), 77-79. doi: 10.1016/0169-4758(90)90215-P PMID: 15463303
  67. Sevrioukova, I.F. Apoptosis-inducing factor: structure, function, and redox regulation. Antioxid. Redox Signal., 2011, 14(12), 2545-2579. doi: 10.1089/ars.2010.3445 PMID: 20868295
  68. Boedtkjer, E.; Pedersen, S.F. The acidic tumor microenvironment as a driver of cancer. Annu. Rev. Physiol., 2020, 82(1), 103-126. doi: 10.1146/annurev-physiol-021119-034627 PMID: 31730395
  69. Gerweck, L.E.; Seetharaman, K. Cellular pH gradient in tumor versus normal tissue: potential exploitation for the treatment of cancer. Cancer Res., 1996, 56(6), 1194-1198. PMID: 8640796
  70. Zhang, X.; Lin, Y.; Gillies, R.J. Tumor pH and its measurement. J. Nucl. Med., 2010, 51(8), 1167-1170. doi: 10.2967/jnumed.109.068981 PMID: 20660380
  71. Baldino, C.M.; Parr, J.; Wilson, C.J.; Ng, S.C.; Yohannes, D.; Wasserman, H.H. Indoloprodigiosins from the C-10 bipyrrolic precursor: New antiproliferative prodigiosin analogs. Bioorg. Med. Chem. Lett., 2006, 16(3), 701-704. doi: 10.1016/j.bmcl.2005.10.027 PMID: 16289814
  72. Regourd, J.; Al-Sheikh Ali, A.; Thompson, A. Synthesis and anti-cancer activity of C-ring-functionalized prodigiosin analogues. J. Med. Chem., 2007, 50(7), 1528-1536. doi: 10.1021/jm061088f PMID: 17348639
  73. Díaz, R.I.S.; Regourd, J.; Santacroce, P.V.; Davis, J.T.; Jakeman, D.L.; Thompson, A. Chloride anion transport and copper-mediated DNA cleavage by C-ring functionalized prodigiosenes. Chem. Commun. , 2007, (26), 2701-2703. doi: 10.1039/B701919J PMID: 17594025
  74. Kapoor, I.; Bodo, J.; Hill, B.T.; Hsi, E.D.; Almasan, A. Targeting BCL-2 in B-cell malignancies and overcoming therapeutic resistance. Cell Death Dis., 2020, 11(11), 941. doi: 10.1038/s41419-020-03144-y PMID: 33139702
  75. Yuan, B.; Hao, J.; Zhang, Q.; Wang, Y.; Zhu, Y. Role of Bcl 2 on drug resistance in breast cancer polyploidy induced spindle poisons. Oncol. Lett., 2020, 19(3), 1701-1710. doi: 10.3892/ol.2020.11256 PMID: 32194662
  76. Ploumaki, I.; Triantafyllou, E.; Koumprentziotis, I.A.; Karampinos, K.; Drougkas, K.; Karavolias, I.; Trontzas, I.; Kotteas, E.A. Bcl-2 pathway inhibition in solid tumors: a review of clinical trials. Clin. Transl. Oncol., 2023, 25(6), 1554-1578. doi: 10.1007/s12094-022-03070-9 PMID: 36639602
  77. Wolf, P. BH3 mimetics for the treatment of prostate cancer. Front. Pharmacol., 2017, 8, 557. doi: 10.3389/fphar.2017.00557
  78. Espona-Fiedler, M.; Manuel-Manresa, P.; Benítez-García, C.; Fontova, P.; Quesada, R.; Soto-Cerrato, V.; Pérez-Tomás, R. Antimetastatic properties of prodigiosin and the BH3-mimetic obatoclax (GX15-070) in melanoma. Pharmaceutics, 2022, 15(1), 97. doi: 10.3390/pharmaceutics15010097 PMID: 36678726
  79. Lima, K.; Vicari, H.P.; Carlos, J.A.E.G.; da Silva, J.C.L.; Figueiredo-Pontes, L.L.; Rego, E.M.; Machado-Neto, J.A. Obatoclax reduces cell viability of acute myeloid leukemia cell lines independently of their sensitivity to venetoclax. Hematol. Transfus. Cell Ther., 2022, 44(1), 124-127. doi: 10.1016/j.htct.2021.01.004 PMID: 33753045
  80. Gao, F.; Lan, H.; Jiao, L.; Zuo, T.; Sun, N.; Hu, Z.; Huang, J. Inhibitory effect of obatoclax mesylate-Loaded nanoparticles on lung cancer through Bcl-2 pathway. Mater. Express, 2023, 13(2), 283-289. doi: 10.1166/mex.2023.2344
  81. Daïri, K.; Yao, Y.; Faley, M.; Tripathy, S.; Rioux, E.; Billot, X.; Rabouin, D.; Gonzalez, G.; Lavallée, J-F.; Attardo, G. A scalable process for the synthesis of the bcl inhibitor obatoclax. Org. Process Res. Dev., 2007, 11(6), 1051-1054. doi: 10.1021/op7001613
  82. Maji, S. Chapter three - Bcl-2 antiapoptotic family proteins and chemoresistance in cancer.In: Advances in Cancer Research; Tew, K.D.; Fisher, P.B., Eds.; Academic Press, 2018, Vol. 137, pp. 37-75. doi: 10.1016/bs.acr.2017.11.001
  83. Lin, S.R.; Chen, Y.H.; Tseng, F.J.; Weng, C.F. The production and bioactivity of prodigiosin: quo vadis? Drug Discov. Today, 2020, 25(5), 828-836. doi: 10.1016/j.drudis.2020.03.017 PMID: 32251776
  84. Soto-Cerrato, V.; Viñals, F.; Lambert, J.R.; Pérez-Tomás, R. The anticancer agent prodigiosin induces p21WAF1/CIP1 expression via transforming growth factor-beta receptor pathway. Biochem. Pharmacol., 2007, 74(9), 1340-1349. doi: 10.1016/j.bcp.2007.07.016 PMID: 17765876
  85. Yenkejeh, R.A.; Sam, M.R.; Esmaeillou, M. Targeting survivin with prodigiosin isolated from cell wall of Serratia marcescens induces apoptosis in hepatocellular carcinoma cells. Hum. Exp. Toxicol., 2017, 36(4), 402-411. doi: 10.1177/0960327116651122 PMID: 27334973
  86. Zhu, Z. Unveiling the anticancer mechanisms of prodigiosin by inhibiting of CDK1, TOP2A, and AURKB expression in cervical carcinoma. Epub ahead of Print. 2024. doi: 10.21203/rs.3.rs-3829039/v1
  87. Hong, B.; Prabhu, V.V.; Zhang, S.; van den Heuvel, A.P.J.; Dicker, D.T.; Kopelovich, L.; El-Deiry, W.S. Prodigiosin rescues deficient p53 signaling and antitumor effects via upregulating p73 and disrupting its interaction with mutant p53. Cancer Res., 2014, 74(4), 1153-1165. doi: 10.1158/0008-5472.CAN-13-0955 PMID: 24247721
  88. Yamamoto, C.; Takemoto, H.; Kuno, K.; Yamamoto, D.; Nakai, K.; Baden, T.; Kamata, K.; Hirata, H.; Watanabe, T.; Inoue, K. Cycloprodigiosin hydrochloride, a H+/Cl- symporter, induces apoptosis in human colon cancer cell lines in vitro. Oncol. Rep., 2001, 8(4), 821-824. doi: 10.3892/or.8.4.821 PMID: 11410791
  89. Branco, P.C.; Pontes, C.A.; Rezende-Teixeira, P.; Amengual-Rigo, P.; Alves-Fernandes, D.K.; Maria-Engler, S.S.; da Silva, A.B.; Pessoa, O.D.L.; Jimenez, P.C.; Mollasalehi, N.; Chapman, E.; Guallar, V.; Machado-Neto, J.A.; Costa-Lotufo, L.V. Survivin modulation in the antimelanoma activity of prodiginines. Eur. J. Pharmacol., 2020, 888, 173465. doi: 10.1016/j.ejphar.2020.173465 PMID: 32814079
  90. Matarlo, J.S.; Krumpe, L.R.H.; Heinz, W.F.; Oh, D.; Shenoy, S.R.; Thomas, C.L.; Goncharova, E.I.; Lockett, S.J.; O’Keefe, B.R. The natural product butylcycloheptyl prodiginine binds pre-miR-21, inhibits Dicer-mediated processing of pre-miR-21, and blocks cellular proliferation. Cell Chem. Biol., 2019, 26(8), 1133-1142.e4. doi: 10.1016/j.chembiol.2019.04.011 PMID: 31155509
  91. Li, J.; Xu, J.; Li, Z. Obatoclax, the pan-Bcl-2 inhibitor sensitizes hepatocellular carcinoma cells to promote the anti-tumor efficacy in combination with immune checkpoint blockade. Transl. Oncol., 2021, 14(8), 101116. doi: 10.1016/j.tranon.2021.101116 PMID: 33975180
  92. Abrahantes-Pérez, M.C.; Reyes-González, J.; Véliz Ríos, G.; Bequet-Romero, M.; Gómez Riera, R.; Anais Gasmury, C.; Huerta, V.; González, L.J.; Canino, C.; Garcia, J.; Váldez, J.; Reyes, B.; Váldes, R.; Martínez, E. Cytotoxic proteins combined with prodigiosin obtained from Serratia marcescens have both broad and selective cytotoxic activity on tumor cells. In: J. Chemother., 2006, 18(2), 172-181. doi: 10.1179/joc.2006.18.2.172 PMID: 16736886
  93. Berning, L.; Schlütermann, D.; Friedrich, A.; Berleth, N.; Sun, Y.; Wu, W.; Mendiburo, M.J.; Deitersen, J.; Brass, H.U.C.; Skowron, M.A.; Hoffmann, M.J.; Niegisch, G.; Pietruszka, J.; Stork, B. Prodigiosin sensitizes sensitive and resistant urothelial carcinoma cells to cisplatin treatment. Molecules, 2021, 26(5), 1294. doi: 10.3390/molecules26051294 PMID: 33673611
  94. Brown, J.R.; Tesar, B.; Yu, L.; Werner, L.; Takebe, N.; Mikler, E.; Reynolds, H.M.; Thompson, C.; Fisher, D.C.; Neuberg, D.; Freedman, A.S. Obatoclax in combination with fludarabine and rituximab is well-tolerated and shows promising clinical activity in relapsed chronic lymphocytic leukemia. Leuk. Lymphoma, 2015, 56(12), 3336-3342. doi: 10.3109/10428194.2015.1048441 PMID: 25971907
  95. Chiappori, A.A.; Schreeder, M.T.; Moezi, M.M.; Stephenson, J.J.; Blakely, J.; Salgia, R.; Chu, Q.S.; Ross, H.J.; Subramaniam, D.S.; Schnyder, J.; Berger, M.S. A phase I trial of pan-Bcl-2 antagonist obatoclax administered as a 3-h or a 24-h infusion in combination with carboplatin and etoposide in patients with extensive-stage small cell lung cancer. Br. J. Cancer, 2012, 106(5), 839-845. doi: 10.1038/bjc.2012.21 PMID: 22333598
  96. Chiappori, A.; Williams, C.; Northfelt, D.W.; Adams, J.W.; Malik, S.; Edelman, M.J.; Rosen, P.; Van Echo, D.A.; Berger, M.S.; Haura, E.B. Obatoclax mesylate, a pan-bcl-2 inhibitor, in combination with docetaxel in a phase 1/2 trial in relapsed non-small-cell lung cancer. J. Thorac. Oncol., 2014, 9(1), 121-125. doi: 10.1097/JTO.0000000000000027 PMID: 24346101
  97. Paik, P.K.; Rudin, C.M.; Brown, A.; Rizvi, N.A.; Takebe, N.; Travis, W.; James, L.; Ginsberg, M.S.; Juergens, R.; Markus, S.; Tyson, L.; Subzwari, S.; Kris, M.G.; Krug, L.M. A phase I study of obatoclax mesylate, a Bcl-2 antagonist, plus topotecan in solid tumor malignancies. Cancer Chemother. Pharmacol., 2010, 66(6), 1079-1085. doi: 10.1007/s00280-010-1265-5 PMID: 20165849
  98. Paik, P.K.; Rudin, C.M.; Pietanza, M.C.; Brown, A.; Rizvi, N.A.; Takebe, N.; Travis, W.; James, L.; Ginsberg, M.S.; Juergens, R.; Markus, S.; Tyson, L.; Subzwari, S.; Kris, M.G.; Krug, L.M. A phase II study of obatoclax mesylate, a Bcl-2 antagonist, plus topotecan in relapsed small cell lung cancer. Lung Cancer, 2011, 74(3), 481-485. doi: 10.1016/j.lungcan.2011.05.005 PMID: 21620511
  99. Tunca Koyun, M.; Sirin, S.; Aslim, B.; Taner, G.; Nigdelioglu Dolanbay, S. Characterization of prodigiosin pigment by Serratia marcescens and the evaluation of its bioactivities. Toxicol. In Vitro, 2022, 82, 105368. doi: 10.1016/j.tiv.2022.105368 PMID: 35476923
  100. Guryanov, I.; Naumenko, E.; Akhatova, F.; Lazzara, G.; Cavallaro, G.; Nigamatzyanova, L.; Fakhrullin, R. Selective cytotoxic activity of prodigiosin@halloysite nanoformulation. Front. Bioeng. Biotechnol., 2020, 8, 424. doi: 10.3389/fbioe.2020.00424 PMID: 32528938

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